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The Colletotrichum acutatum species complex

The Colletotrichum acutatum species complex available online at www.studiesinmycology.org StudieS in Mycology 73: 37–113. 1* 2 1 1,3,4 U. Damm , P.F. Cannon , J.H.C. Woudenberg , and P.W. Crous 1 2 CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands; CABI Europe-UK, Bakeham Lane, Egham, Surrey TW20 9TY, UK and Royal 3 4 Botanic Gardens, Kew, Richmond TW9 3AB, UK; Microbiology, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands; Wageningen University and Research Centre (WUR), Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands *Correspondence: Ulrike Damm, u.damm@cbs.knaw.nl Abstract: Colletotrichum acutatum is known as an important anthracnose pathogen of a wide range of host plants worldwide. Numerous studies have reported subgroups within the C. acutatum species complex. Multilocus molecular phylogenetic analysis (ITS, ACT, TUB2, CHS-1, GAPDH, HIS3) of 331 strains previously identified as C. acutatum and other related taxa, including strains from numerous hosts with wide geographic distributions, confirmed the molecular groups previously recognised and identified a series of novel taxa. Thirty-one species are accepted, of which 21 have not previously been recognised. Colletotrichum orchidophilum clusters basal to the C. acutatum species complex. There is a high phenotypic diversity within this complex, and some of the species appear to have preferences to specific hosts or geographical regions. Others appear to be plurivorous and are present in multiple regions. In this study, only C. salicis and C. rhombiforme formed sexual morphs in culture, although sexual morphs have been described from other taxa (especially as laboratory crosses), and there is evidence of hybridisation between different species. One species with similar morphology to C. acutatum but not belonging to this species complex was also described here as new, namely C. pseudoacutatum. Key words: anthracnose, Ascomycota, Colletotrichum acutatum, Gloeosporium, Glomerella, phylogeny, systematics. Taxonomic novelties: New combinations - Colletotrichum limetticola (R.E. Clausen) Damm, P.F. Cannon & Crous, C. lupini (Bondar) Damm, P.F. Cannon & Crous, C. salicis (Fuckel) Damm, P.F. Cannon & Crous. New species - C. acerbum Damm, P.F. Cannon & Crous, C. australe Damm, P.F. Cannon & Crous, C. brisbanense Damm, P.F. Cannon & Crous, C. cosmi Damm, P.F. Cannon & Crous, C. costaricense Damm, P.F. Cannon & Crous, C. cuscutae Damm, P.F. Cannon & Crous, C. guajavae Damm, P.F. Cannon & Crous, C. indonesiense Damm, P.F. Cannon & Crous, C. johnstonii Damm, P.F. Cannon & Crous, C. kinghornii Damm, P.F. Cannon & Crous, C. laticiphilum Damm, P.F. Cannon & Crous, C. melonis Damm, P.F. Cannon & Crous, C. orchidophilum Damm, P.F. Cannon & Crous, C. paxtonii Damm, P.F. Cannon & Crous, C. pseudoacutatum Damm, P.F. Cannon & Crous C. pyricola Damm, P.F. Cannon & Crous, C. rhombiforme Damm, P.F. Cannon & Crous, C. scovillei Damm, P.F. Cannon & Crous, C. sloanei Damm, P.F. Cannon & Crous, C. tamarilloi Damm, P.F. Cannon & Crous, C. walleri Damm, P.F. Cannon & Crous. Typifications: Epitypifications - C. acutatum J.H. Simmonds, C. limetticola (R.E. Clausen) Damm, P.F. Cannon & Crous, C. nymphaeae (Pass.) Aa, C. phormii (Henn.) D.F. Farr & Rossman, C. salicis (Fuckel) Damm, P.F. Cannon & Crous. Lectotypifications - C. nymphaeae (Pass.) Aa, C. orchidearum Allesch. Published online: 16 August 2012; doi:10.3114/sim0010. Hard copy: September 2012. pathogen, C. acutatum was treated for many years as a regulated INTRODUCTION plant quarantine pest by the European and Mediterranean Plant Protection Organization (EPPO), though it is absent from the Colletotrichum acutatum is one of the most frequently reported current list (EPPO 2011) – presumably due to its now widespread species of the genus and causes diseases commonly known as distribution in Europe. Inoculum sources are frequently transplant anthracnose on numerous host plants worldwide (Farr & Rossman material, mostly with quiescent infections (Rahman & Louws 2008), 2012). Originally described from diseased tissues of Carica infected plants, weeds and other hosts (McInnes et al. 1992, papaya, Capsicum frutescens and Delphinium ajacis in Australia Parikka et al. 2006), while the survival rate of conidia in natural field by Simmonds (1965), the C. acutatum species complex is today soil is low (Freeman et al. 2002). known as especially destructive on fruits like strawberry (Garrido The most well-known morphological feature of C. acutatum (s. et al. 2009), citrus (Peres et al. 2008), apple (Lee et al. 2007), lat.) is the shape of its conidia, which have acute ends (Simmonds olive (Talhinhas et al. 2011), cranberry (Polashock et al. 2009) and 1965). However, other conidial shapes, especially ± cylindrical blueberry (Wharton & Schilder 2008). It is also implicated in the with only one acute end, are frequently encountered, especially in “terminal crook” disease of pine (Dingley & Gilmour 1972) and in the anthracnose of leather leaf fern (Schiller et al. 2006). There are strains that have been repeatedly subcultured, but these conidial also reports of a disseminated infection of a sea turtle (Manire et shapes can also occur in species outside the C. acutatum species al. 2002) and the infection of a scale insect (Marcelino et al. 2008). complex. Even the differentiation between C. acutatum (s. lat.) and Reviews of the species in its broad sense and its pathology were C. gloeosporioides (s. lat.) is difficult, because many intermediate strains exist with a restricted number of typical fusiform conidia and published by Wharton & Diéguez-Uribeondo (2004) and Peres et many cylindrical ones (Van der Aa et al. 1990). On the host, conidia al. (2005). On strawberry, C. acutatum mainly causes black spot of fruit are formed in acervuli; in culture, conidia are often also produced but can also attack crowns, roots and leaves (Freeman & Katan in the aerial mycelium (Johnston & Jones 1997). Colletotrichum 1997), and is one of the most serious diseases in commercial fruit acutatum has also been observed to form secondary conidia on the production. Largely due to its economic importance as a strawberry surface of living strawberry leaves (Leandro et al. 2001) that were Copyright CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 AD Utrecht, The Netherlands. You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. Studies in Mycology Damm et al . stimulated by strawberry plant extracts, especially flower extracts Our research aims to present a comprehensive revision of (Leandro et al. 2003). According to Buddie et al. (1999) secondary the C. acutatum species complex. We thoroughly survey the conidia may be produced directly from germinating primary conidia, constituent taxa and delineate additional species where needed. and are smaller and more variable in shape, thus obscuring We have examined a large number of C. acutatum s. lat. strains, differences between taxa. Additionally, C. acutatum forms simple isolated from various hosts and in various geographic areas. Multi- pigmented appressoria, but few or no setae (Simmonds 1965). locus molecular analysis is the basis of species recognition, but Guerber & Correll (1997, 2001) described Glomerella acutata, morphological and cultural characters allowing alternative means the sexual morph of C. acutatum, as the product of mating of species recognition are given where possible. experiments, while some related species are homothallic, including Ga. acutata var. fioriniae (Marcelino et al. 2008), later regarded as a separate species (C. fioriniae, Shivas & Tan 2009) and an isolate MATERIALS AND METHODS of a Glomerella species related to C. acutata from Acer platanoides in the USA (LoBuglio & Pfister 2008). Talgø et al. (2007) observed Isolates the sexual morph Ga. acutata on naturally infected fruits of highbush blueberry in Norway. Numerous studies have shown A total of 331 strains have been studied, mostly previously that C. acutatum is morphologically and phylogenetically diverse identified as C. acutatum, as well as other related strains from the (Sreenivasaprasad et al. 1994, Johnston & Jones 1997, Lardner CBS, IMI and other culture collections. Type material (holotypes et al. 1999, Freeman et al. 2001a, Nirenberg et al. 2002, Talhinhas and epitypes) of the species studied are located in the Herbarium et al. 2002, Guerber et al. 2003, Lubbe et al. 2004, Du et al. 2005, of the Centraalbureau voor Schimmelcultures (CBS), Utrecht, Peres et al. 2005, Sreenivasaprasad & Talhinhas 2005, Talhinhas The Netherlands, in the IMI Fungarium, which is based in the et al. 2005, Johnston et al. 2008). Sreenivasaprasad et al. (1996) Royal Botanic Gardens, Kew (IMI and K(M)), UK, US National were the first to recognise that C. acutatum was unusually diverse, Fungus Collections (BPI), Beltsville, Maryland, USA, the Botanic with strains showing divergence of 5.8 % in ITS-1 sequence Garden and Botanical Museum Berlin-Dahlem, Freie Universität compared with levels of 2–4 % frequently found within other Berlin (B), Germany and in the dried collection of the Botanische fungal species, and they suggested splitting C. acutatum into two Staatssammlung München (M), Germany. All descriptions are based species. Johnston & Jones (1997) recognised four morphological on the ex-type, ex-epitype or ex-neotype culture as appropriate. groups, C. acutatum A–C and Glomerella miyabeana. Three of Features of other strains are added if deviant. Subcultures of the these groups were supported by 28S nuclear ribosomal large types, epitypes and neotypes, respectively, as well as all other subunit rRNA (LSU) sequence data. Lardner et al. (1999), using a isolates used for morphological and sequence analyses are combination of RAPDs and morphological/cultural data, identified maintained in the culture collections of CBS and IMI (Table 1). seven subordinate groups within C. acutatum. Sequences of a 200-bp intron of the glyceraldehyde-3-phosphate dehydrogenase Morphological analysis (GAPDH) and a 900-bp intron of the glutamine synthetase GS distinguished seven main clades and several subclades within To enhance sporulation, autoclaved filter paper and double- strains that originated mainly from North America and New Zealand autoclaved stems of Anthriscus sylvestris were placed onto the (Guerber et al. 2003). The recognition of infraspecific groups surface of synthetic nutrient-poor agar medium (SNA; Nirenberg was more firmly established by Sreenivasaprasad & Talhinhas 1976). SNA and oatmeal agar (OA; Crous et al. 2009) cultures were (2005), who distinguished clades A1 to A8 based on rDNA ITS and incubated at 20 °C under near UV light with 12 h photoperiod for beta-tubulin DNA (TUB2) sequences. These clades were mostly 10 d. Measurements and photographs of characteristic structures correlated with the groups that had been distinguished previously. were made according to Damm et al. (2007). Appressoria on Whitelaw-Weckert et al. (2007) recognised an additional group A9. hyphae were observed on the reverse side of SNA plates. At this point, it was widely presumed that C. acutatum was Microscopic preparations were made in clear lactic acid, with 30 a species complex containing a number of constituent taxa, but measurements per structure and observed with a Nikon SMZ1000 there was substantial reluctance to recognise the clades involved dissecting microscope (DM) or with a Nikon Eclipse 80i microscope as independent species. This was due to the lack of differential using differential interference contrast (DIC) illumination. In the C. morphological and cultural characters. For example, C. lupini was acutatum species complex, conidia are usually formed in acervular not recognised as formally separate from C. acutatum by Talhinhas conidiomata and additionally in the aerial mycelium. Unless et al. (2002) or by Sreenivasaprasad & Talhinhas (2005). There mentioned otherwise, only conidia from conidiomata were used in were some attempts to address these concerns via adoption of this study for morphological examination. formae speciales e.g. C. acutatum f. sp. pineum (Dingley & Gilmour Colony characters and pigment production on SNA and 1972), C. acutatum f. sp. hakeae (Lubbe et al. 2004) and C. OA cultures incubated at 20 °C under near UV light with 12 h acutatum f. sp. fioriniae (Marcelino et al. 2008), but this mechanism photoperiod were noted after 10 d. Colony colours were rated for recognition of pathology-related taxa is now rarely used. according to Rayner (1970). Growth rates were measured after 7 Gradually, separate species were recognised or accepted as and 10 d. part of the C. acutatum species complex, e.g. C. lupini (Nirenberg et al. 2002) and C. phormii (Farr et al. 2006). In a study using two genes, ITS and TUB2, combined with morphological data, Shivas Phylogenetic analysis & Tan (2009) recognised three distinct groups within C. acutatum strains from Australia and accepted two new species, C. simmondsii Genomic DNA of the isolates was extracted using the method of Damm et al. (2008). The 5.8S nuclear ribosomal gene with the two and C. fioriniae (formerly C. acutatum f. sp. fioriniae ) for groups A2 flanking internal transcribed spacers (ITS), a 200-bp intron of the and A3. Recently, a new species was described for group A4, C. glyceraldehyde-3-phosphate dehydrogenase (GAPDH), and partial clavatum (Faedda et al. 2011). 38 The CotriC ollet hum aCtum a ut species complex CBS 109225 Lupinus Ukraine CBS 109216 Lupinus Bolivia 88 CBS 513.97 Lupinus Costa Rica CBS 109226 Lupinus Canada 1.00 CBS 509.97 Lupinus France CBS 466.76 Manihot Rwanda 0.99 IMI 375715 Lupinus Australia CBS 122746 Lupinus USA CBS 109217 Lupinus Germany CBS 485.97 Lupinus Germany 1.00 CBS 126371 Lupinus NL 0.99 J6 CBS 507.97 Lupinus France C. lupini A1 CBS 109219 Lupinus Germany J2 CBS 109220 Lupinus Germany CBS 109221 Lupinus Germany CBS 109222 Lupinus Germany 1.00 CBS 109223 Lupinus Germany CBS 109224 Lupinus Austria CBS 109227 Lupinus Poland CBS 126525 Lupinus NL CBS 119142 Lupinus ZA CBS 119143 Lupinus ZA IMI 351261 Camellia UK CBS 129944 Cinnamomum Portugal CBS 129814 Solanum Colombia CBS 129811 Solanum Colombia CBS 129812 Solanum Colombia CBS 129813 Solanum Colombia C. tamarilloi A8 1.00 CBS 129954 Solanum Colombia CBS 129955 Solanum Colombia CBS 129956 Solanum Colombia CBS 129810 Solanum Colombia CBS 101611 fern Costa Rica 0.97 CBS 129821 Passiflora Colombia CBS 129820 Passiflora Colombia 1.00 CBS 330.75 Coffea Costa Rica 1.00 94 C. costaricense CBS 211.78 Coffea Costa Rica 1.00 IMI 304802 Cuscuta Dominica C. cuscutae IMI 384185 Caryocar Brazil CBS 129823 Passiflora Colombia 1 change CBS 114.14 Citrus USA C. limetticola J3 CBS 159.84 Cucumis Brazil C. melonis Fig. 1. One of 830 most parsimonious trees obtained from a heuristic search of the combined ITS, GAPDH, CHS-1, ACT, HIS3 and TUB2 sequences alignment of the Colletotrichum acutatum species complex. Bootstrap support values above 70 % (bold) and Bayesian posterior probability values above 0.95 are shown at the nodes. Colletotrichum orchidophilum CBS 632.80, CBS 631.80, IMI 309357 and CBS 119291 are used as outgroup. Numbers of ex-holotype, ex-neotype and ex-epitype strains are emphasised in bold. Strain numbers are followed by substrate (host genus) and country of origin, NL = Netherlands, NZ = New Zealand, ZA = South Africa. Branches that are crossed by diagonal lines are shortened by 50 %. Corresponding groups of Sreenivasaprasad & Talhinhas 2005 are emphasised in red, mtDNA RFLP haplotypes of Guerber et al. (2003) are emphasised in blue. sequences of the chitin synthase 1 (CHS-1), histone3 (HIS3), actin random sequence additions and tree bisection and reconstruction (ACT) and beta-tubulin (TUB2) genes were amplified and sequenced (TBR) as the branch-swapping algorithm. Alignment gaps were using the primer pairs ITS-1F (Gardes & Bruns 1993) + ITS-4 (White treated as missing and all characters were unordered and of equal et al. 1990) or V9G (de Hoog & Gerrits van den Ende 1998) + ITS- weight. No more than 10 trees of score (length) greater than or equal 4, GDF1 + GDR1 (Guerber et al. 2003), CHS-354R + CHS-79F to 10 were saved in each replicate. The robustness of the trees (Carbone & Kohn 1999), CYLH3F + CYLH3R (Crous et al. 2004b), obtained was evaluated by 10 000 bootstrap replications using the ACT-512F + ACT-783R (Carbone & Kohn 1999) and BT2Fd + BT4R Fast-stepwise addition algorithm (Hillis & Bull 1993). Tree length, (Woudenberg et al. 2009) or T1 (O’Donnell & Cigelnik 1997) + Bt-2b consistency index (CI), retention index (RI), rescaled consistency (Glass & Donaldson 1995), respectively. The PCRs were performed index (RC) and homoplasy index (HI) were calculated for the in a 2720 Thermal Cycler (Applied Biosystems, Foster City, resulting tree. A Markov Chain Monte Carlo (MCMC) algorithm was California) in a total volume of 12.5 μL. The GAPDH, CHS-1, HIS3, used to generate phylogenetic trees with Bayesian probabilities ACT and TUB2 PCR mixture contained 1 μL 20x diluted genomic using MrBayes v. 3.1.1 (Ronquist & Huelsenbeck 2003) for the DNA, 0.2 μM of each primer, 1x PCR buffer (Bioline, Luckenwalde, combined sequence datasets. Models of nucleotide substitution Germany), 2 mM MgCl , 20 μM of each dNTP, 0.7 μL DMSO and for each gene determined by MrModeltest v. 2.3 were included for 0.25 U Taq DNA polymerase (Bioline). Conditions for PCR of these each gene partition. The analyses of two MCMC chains were run genes constituted an initial denaturation step of 5 min at 94 C, from random trees for 1000 000 generations and sampled every o o followed by 40 cycles of 30 s at 94 C, 30 s at 52 C and 30 s at 100 generations. The likelihood score of the two runs were 2 500 o o 72 C, and a final denaturation step of 7 min at 72 C, while the ITS and 2 200 and therefore, the first 2 350 (the average of both) trees PCR was performed as described by Woudenberg et al. (2009). The were discarded as the burn-in phase of the analysis and posterior DNA sequences generated with forward and reverse primers were probabilities determined from the remaining trees. For additional used to obtain consensus sequences using Bionumerics v. 4.60 comparison, a Neighbour-Joining analysis was performed on the (Applied Maths, St-Marthens-Lathem, Belgium), and the alignment multigene alignment using PAUP and 1000 bootstrap replications. assembled and manually adjusted using Sequence Alignment Editor Sequences derived in this study have been lodged at GenBank, the v. 2.0a11 (Rambaut 2002). alignment in TreeBASE (www.treebase.org/treebase-web/home. To determine whether the six sequence datasets were html), and taxonomic novelties in MycoBank (Crous et al. 2004a). congruent and combinable, tree topologies of 70 % reciprocal Neighbour-Joining bootstrap with Maximum Likelihood distances (10 000 replicates) with substitution models determined separately RESULTS for each partition using MrModeltest v. 2.3 (Nylander 2004) were compared visually (Mason-Gamer & Kellogg 1996). A maximum parsimony analysis was performed on the multilocus alignment Phylogeny (ITS, GAPDH, CHS-1, HIS3, ACT, TUB2) as well as for each gene separately with PAUP (Phylogenetic Analysis Using Parsimony) v. The six sequence data sets did not show any conflicts in tree 4.0b10 (Swofford 2000) using the heuristic search option with 100 topology for the 70 % reciprocal bootstrap trees, which allowed us www.studiesinmycology.org Clade 1 Damm et al . 0.96 CBS 515.78 Nymphaea NL CBS 516.78 Nuphar NL 1.00 CBS 526.77 Nymphaea NL CBS 173.51 Mahonia Italy 0.98 CBS 129945 Olea Portugal CBS 231.49 Olea Portugal CBS 126507 Oenothera NL 0.98 IMI 370491 Malus Brazil CBS 119294 Leucaena Mexico CBS 112992 Protea ZA 1.00 CBS 113002 Protea ZA CBS 113003 Protea ZA CBS 113004 Protea ZA CBS 113005 Protea ZA CBS 115408 Protea ZA CBS 482.82 Protea Australia CBS 114188 Protea unknown CBS 158.27 unknown unknown CSL 455 Photinia UK IMI 379162 Capsicum Zimbabwe IMI 360386 Pelargonium India CBS 129926 litter Thailand 1.00 CBS 126528 Capsicum Indonesia CBS 126382 Anemone NL CBS 126383 Anemone NL CBS 126511 Anemone NL 98 CBS 100064 Anemone NL CBS 130.80 Anemone Italy 1.00 CBS 129935 Anemone Israel CBS 127612 Fragaria USA CBS 361.79 Anemone NL CBS 126513 Anemone NL CBS 100065 Anemone NL C. nymphaeae CBS 129928 Fragaria USA D2 CBS 129929 Fragaria USA CBS 112202 Fragaria Spain CBS 122110 Fragaria Bulgaria D4 1.00 CBS 122111 Fragaria Bulgaria CBS 122121 Fragaria Bulgaria IMI 345053 Fragaria France IMI 348497 Fragaria France CBS 126372 Fragaria Italy IMI 360928 Fragaria Switzerland IMI 364856 Fragaria Spain CBS 125958 Fragaria NL CBS 125959 Fragaria NL 79 CBS 125966 Fragaria NL 1.00 CBS 125961 Fragaria NL A2 CBS 130239 Fragaria NL IMI 391664 Fragaria Israel CBS 129936 Fragaria Israel CBS 129937 Fragaria Israel CBS 129918 Fragaria unknown CBS 126366 Fragaria USA CBS 126367 Fragaria USA CBS 126370 Fragaria USA IMI 311743 Fragaria USA IMI 324995 Fragaria USA CBS 127609 Fragaria USA CBS 127610 Fragaria USA CBS 129933 Fragaria USA IMI 348177 Fragaria USA CBS 127608 Fragaria Canada CBS 126504 Fragaria ZA IMI 301119 Fragaria Kenya IMI 299103 Fragaria UK CBS 125973 Fragaria UK CBS 126377 Fragaria NL IMI 348502 Fragaria France IMI 345032 Fragaria Italy CBS 126529 Capsicum Indonesia CBS 126530 Capsicum Indonesia C. scovillei 1.00 D3 CBS 120708 Capsicum Thailand 1.00 IMI 350839 Psidium India C. guajavae CBS 126518 Carthamus NL CBS 126519 Chrysanthemum NL C. chrysanthemi 1.00 IMI 364540 Chrysanthemum China CBS 853.73 Cosmos NL C. cosmi CBS 125472 Coffea Vietnam C. walleri 1.00 CBS 122122 Carica Australia CBS 294.67 Carica Australia 0.99 1.00 CBS 295.67 Fragaria Australia IMI 345034 Fragaria Australia C. simmondsii IMI 354381 Fragaria Australia 99 CBS 126524 Cyclamen NL CBS 111531 Protea USA 1.00 99 CBS 114494 Protea USA 1.00 IMI 313840 Mangifera Australia 1.00 IMI 165753 Musa St. Lucia C. paxtonii 1.00 CBS 502.97 Musa West Indies 1.00 IMI 364297 Theobroma Malaysia C. sloanei CBS 127551 Eucalyptus Indonesia C. indonesiense 1.00 CBS 112989 Hevea India C. laticiphilum 1 change CBS 129827 Hevea Colombia 1.00 CBS 292.67 Capsicum Australia C. brisbanense Fig. 1. (Continued). to combine them. In the multigene analyses (gene boundaries of parsimonious trees were retained (length = 1008 steps, CI = 0.643, ITS: 1–546, GAPDH: 557–829, CHS-1: 840–1121, HIS3: 1131– RI = 0.981, RC = 0.681, HI = 0.357) of which one is shown in Fig. 1519, ACT: 1530–1786, TUB2: 1797–2290) of 330 isolates of C. 1. The topology of the 830 trees was similar, which was verified acutatum and related Colletotrichum species including the outgroup for a large selection of trees. They differed only in the position of (C. orchidophilum strains CBS 631.80, CBS 632.80, CBS 119291, taxa within the subclades. For Bayesian analysis, a HKY+I model IMI 309357), 2290 characters including the alignment gaps were was selected for ITS, a HKY+G model for GAPDH and TUB2, a processed, of which 468 characters were parsimony-informative, K80+I+G model for CHS-1, a HKY+I+G model for HIS3, a GTR+G 65 parsimony-uninformative and 1757 constant. One strain that model for ACT, and incorporated in the analysis. The consensus was revealed as not belonging to the C. acutatum species complex tree obtained from Bayesian analyses and the NJ tree (not shown) (CBS 436.77, C. pseudoacutatum) was not included in the analysis confirmed the tree topology obtained with parsimony. Bayesian presented in Fig. 1. After a heuristic search using PAUP, 830 most posterior probability values agreed with bootstrap supports (Fig. 1). Clade 2 The CotriC ollet hum aCtum a ut species complex CBS 128517 Fiorinia USA CBS 129931 Malus USA CBS 981.69 Coffea Angola 1.00 CBS 129932 Malus USA CBS 112995 Malus USA CBS 125396 Malus USA CBS 127538 Malus USA IMI 324996 Malus USA CBS 127611 Fragaria USA CBS 786 86 Malus Italy CBS 126523 Berberis NL CBS 129940 Grevillea Germany CBS 129941 Grevillea Germany CBS 124958 Pyrus USA ATCC 12097 Rhododendron USA CBS 293.67 Persea Australia IMI 363003 Camellia China CBS 126508 Vaccinium NL CBS 126509 Vaccinium NL CBS 127537 Vaccinium USA CBS 124962 Solanum USA CBS 124963 Solanum USA CBS 125956 Penstemon NL CBS 126526 Primula NL CBS 235.49 unknown unknown CSL 1295 Fragaria UK C1 IMI 324991 Piper unknown CSL 473 Liriodendron UK C. fioriniae A3 C2 CBS 129916 Vaccinium USA CBS 129948 Tulipa UK C3 CBS 200.35 Rubus USA CBS 129938 Malus USA CBS 126381 Malus NL CBS 127614 Fragaria USA CBS 125970 Cyclamen Italy CBS 167.86 Myriophyllum USA CBS 129930 Malus NZ CBS 128555 Malus NZ 1.00 CBS 127600 Persea Australia CBS 127601 Mangifera Australia CBS 119186 Vaccinium NZ CBS 490.92 Solanum unknown IMI 345583 Fragaria NZ IMI 345578 Fragaria NZ CSL 318 Magnolia UK CBS 127599 Persea Australia 1.00 CBS 119292 Vaccinium NZ CBS 128529 Fragaria NZ IMI 345575 Fragaria NZ CBS 128498 Actinidia NZ IMI 384569 Kalmia USA 0.97 CBS 129946 Olea Portugal CBS 129947 Vitis Portugal ATCC 28992 Malus USA CBS 119293 Vaccinium NZ CBS 112996 Carica Australia CBS 113599 Grevillea Australia CBS 113600 Grevillea Australia CBS 111993 Grevillea Australia CBS 369.73 Lupinus NZ 0.99 CBS 370.73 Pinus NZ CBS 371.73 Pinus NZ IMI 223120 Anemone Australia CBS 128499 Pyrus NZ CBS 110735 Pinus ZA CBS 112979 Pinus ZA CBS 112980 Pinus ZA CBS 112981 Pinus ZA CBS 127534 Pinus ZA CBS 127602 Fragaria Australia CBS 112990 Leucadendron ZA CBS 112994 Leucospermum ZA CBS 115202 Leucadendron ZA CBS 127598 Olea ZA CBS 115393 Mimetes ZA CBS 126521 Anemone NL CBS 129919 Hoodia ZA CBS 127539 Aspalathus ZA CBS 127542 Aspalathus ZA CBS 129921 Aspalathus ZA CBS 129922 Aspalathus ZA CBS 127543 Aspalathus ZA CBS 127545 Aspalathus ZA C. acutatum A5 J4 CBS 129914 Aspalathus ZA CBS 129915 Aspalathus ZA CBS 129925 Aspalathus ZA CBS 126505 Lobelia NL CBS 126506 Phlox NL CSL 287 Statice UK IMI 336479 Pistacia Australia IMI 384175 Nerium NZ CBS 129920 Hoodia ZA CBS 127544 Hoodia ZA CBS 127540 Aspalathus water ZA CBS 129923 Aspalathus water ZA CBS 129924 Aspalathus water ZA CBS 127546 Aspalathus water ZA CBS 127541 Aspalathus ZA CBS 112759 Hakea ZA CBS 112760 Hakea ZA CBS 112761 Hakea ZA CBS 112993 Hakea ZA 1.00 CBS 113007 Hakea ZA 0.87 CBS 113008 Hakea ZA 1.00 CBS 113009 Hakea ZA IMI 216370 Coffea Tanzania IMI 319423 Coffea Kenya CBS 129952 Olea Portugal 1 change CBS 113006 Protea ZA CBS 979.69 Coffea Kenya 1.00 CBS 144.29 Capsicum Sri Lanka Fig. 1. (Continued). The analyses resulted in detection of five main clades and numbers beginning with A) and Guerber et al. (2003, mtDNA 29 subclades within C. acutatum s. lat., which we accept as RFLP haplotypes, numbers beginning with C...K), which are the representing different Colletotrichum species. The corresponding most differential and comparable studies, are listed in brackets groups according to Sreenivasaprasad & Talhinhas (2005, below and are indicated in the phylogenetic tree (Fig. 1). The www.studiesinmycology.org Clade 4 Clade 3 Damm et al . CBS 133.44 Godetia Denmark CBS 285.50 Malus unknown CBS 131331 Juglans Austria CBS 126527 Prunus UK IMI 376331 Prunus Norway 1.00 CBS 155.25 nut shell unknown CBS 131332 Agrimonia Austria CBS 126522 Prunus NL CBS 126512 Bonzai NL CBS 125972 Fragaria NL CBS 126516 Fragaria NL CBS 126503 Fragaria UK IMI 351589 Fragaria Ireland CBS 125974 Fragaria UK IMI 351253 Fragaria UK IMI 345026 Fragaria Spain CBS 126520 Parthenocissus NL IMI 362149b Laurus UK CBS 129942 Mahonia Germany F1* CBS 129951 Vitis UK 1.00 C. godetiae CBS 130251 Olea Italy A4 F3 CBS 193.32 Olea Greece CBS 171.59 Juglans unknown 1.00 F7 CBS 160.50 Citrus unknown CBS 796.72 Aeschynomene USA CBS 126376 Fragaria NL IMI 345035 Fragaria France 1.00 CBS 130252 Olea Italy IMI 351262 Fragaria Belgium 0.99 CBS 198.53 Malus NL IMI 351248 Ceanothus UK 0.98 CBS 129911 Podocarpus ZA CBS 129912 Podocarpus ZA CBS 129913 Podocarpus ZA 1.00 0.97 CBS 129934 Prunus Israel CBS 862.70 Sambucus NL IMI 381927 Rubus Turkey CBS 129809 Solanum Colombia 1.00 1.00 CBS 129816 Solanum Colombia CBS 129917 Schinus Mexico 1.00 CBS 127561 Ugni Chile IMI 357027 Citrus NZ C. johnstonii F8 1.00 CBS 128532 Solanum NZ 1.00 C. pyricola CBS 128531 Pyrus NZ F2 CBS 118194 Phormium Germany CBS 199.35 Phormium UK CBS 102054 Phormium NZ 1.00 CBS 118201 Phormium NZ C. phormii 72 CBS 118197 Phormium NZ 1.00 CBS 483.82 Phormium NZ 1.00 CBS 124953 Phormium NL 0.99 CBS 118191 Phormium ZA 100 CBS 129953 Olea Portugal 0.98 C. rhombiforme 100 A6 CBS 131322 Vaccinium USA 1.00 F1* CBS 128530 Malus NZ C. acerbum 1.00 CBS 198.35 Phormium UK C. kinghornii 1.00 100 CBS 116478 Trachycarpus ZA C. australe CBS 131325 Hakea Australia 1.00 CBS 607.94 Salix NL 1.00 CBS 191.56 Salix Germany 1.00 CBS 159.27 unknown unknown CBS 115.14 Solanum Germany 0.96 CBS 113.14 unknown Germany CBS 128558 Salix NZ CBS 223.36 Populus NL CBS 129972 Acer USA CBS 129356 Rhododendron Latvia CBS 128559 Pyrus NZ C. salicis IMI 345581 Fragaria NZ A7 K1 1.00 IMI 345585 Fragaria NZ CBS 129973 Acer USA CBS 128557 Fragaria NZ CBS 192.56 Salix Germany CBS 465.83 Araucaria USA CBS 128556 Fragaria NZ CBS 239.49 unknown unknown CBS 180.97 Populus NL 1 change IMI 385055 Malus NZ CBS 632.80 Dendrobium USA CBS 631.80 Ascocenda USA C. orchidophilum IMI 309357 Phalaenopsis UK CBS 119291 Cygnoches Panama Fig. 1. (Continued). first clade is well supported with a bootstrap support of 100 % (99/1.00), C. laticiphilum (99/1.00), C. cosmi, C. walleri, C. sloanei, and a Bayesian posterior probability value of 1.00. It consists of C. indonesiense and C. brisbanense, the last five of which consist two frequently isolated, well-supported clades (bootstrap support/ of single-strain clades. Clades 3 and 4 are well-supported (100/1.00 Bayesian posterior probability value of both 100/1.00) comprising and 100/0.87) and on long branches; they represent C. fioriniae several strains each, representing C. lupini (A1, J2/J6) and C. (A3, C1/C2/C3) and C. acutatum (A5, J4). Clade 5 consists of two tamarilloi (A8). Other less frequently encountered subclades in the sister clades. Colletotrichum godetiae (A4, F1*, 99/1.00), formed first clade include C. costaricense (94/1.00) with two strains, C. by a large number of strains, belongs to the first sister clade and cuscutae and C. melonis both represented by single-strain clades groups (97/1.00) with C. johnstonii (F8, 100/1.00) and a single-strain on long branches, and several short-branched single-strain clades, clade representing C. pyricola (F2). The other sister clade (75/1.00) including the known species C. limetticola (J3) and six further consists of six subclades: a large, long-branched and almost unnamed strains. The majority of strains in clade 2 (A2, 86/1.00) homogenous subclade representing C. salicis (A7, K1, 100/1.00); belong to C. nymphaeae (98/1.00, D2/D4), while most of the other a short-branched subclade representing C. phormii (91/1.00); C. 11 subclades of this clade are occupied by only one or few strains. rhombiforme (A6, 100/1.00), which groups with a single-strain The clade representing C. scovillei (99/1.00) consists of three clade representing C. acerbum on a long branch (F1*, 100/1.00); strains and groups (98/1.00) with a single-strain clade formed by plus C. australe (100/1.00) and C. kinghornii on long branches. C. guajavae. These two adjacent clades probably correspond to Strains named F1 appear in the phylogeny of Guerber et al. (2003) clade D3 in Guerber et al. (2003). The other sister clades represent in different subclades, corresponding to C. acerbum, C. godetiae C. simmondsii (99/1.00), C. chrysanthemi (100/1.00), C. paxtonii and probably also C. rhombiforme. Colletotrichum pseudoacutatum Clade 5 The CotriC ollet hum aCtum a ut species complex Fig. 2. Colletotrichum acerbum (from ex-holotype strain CBS 128530). A–B. Conidiomata. C. Tip of a seta. D. Basis of a seta. E–J. Conidiophores. K–O. Appressoria. P–Q. Conidia. A, C–G, P. from Anthriscus stem. B, H–O, Q. from SNA. A–B. DM, C–Q. DIC, Scale bars: A = 100 µm, E = 10 µm. Scale bar of A applies to A–B. Scale bar of E applies to C–Q. is only distantly related to the C. acutatum complex and is therefore Colletotrichum acerbum Damm, P.F. Cannon & Crous, sp. not included in the phylogeny, while C. orchidophilum was found to nov. MycoBank MB800494. Fig. 2. be more closely related and was therefore used as outgroup. The phylogenetic position of these and all other species included here is Etymology: acerbus = Latin for bitter; referring to bitter rot, the exhibited in fig. 1 and 2 of Cannon et al. (2012, this issue). vernacular name for Colletotrichum disease of apple. The individual alignments and maximum parsimony analyses of the six single genes were compared with respect to their Sexual morph not observed. Asexual morph on SNA. Vegetative performance in species recognition. With ITS and CHS-1, only 11 hyphae 1–6 µm diam, hyaline, smooth-walled, septate, and 13 species, respectively, can be recognised. All subclades are branched. Chlamydospores not observed. Conidiomata absent, recognised with TUB2 and GAPDH. TUB2 performs better than conidiophores formed directly on hyphae. Setae not observed. GAPDH due to higher numbers of base pair differences, but even Conidiophores hyaline, smooth-walled, septate, branched, to 30 with TUB2 there are clades with differerences of only 1 bp, which µm long. Conidiogenous cells hyaline, smooth-walled, cylindrical to suggests that both genes should be used for identification. The ampulliform, sometimes lacking a basal septum and continuous with performance of the other two genes is intermediate between ITS the conidiophore, sometimes extending to form new conidiogenous and TUB2/GAPDH. loci, polyphialides sometimes observed, discrete phialides measure 7–18 × 3–4.5 µm, opening 1.5–2 µm diam, collarette 0.5–1.5 µm Taxonomy long, periclinal thickening distinct. Conidia hyaline, smooth-walled, aseptate, straight, cylindrical to clavate with one end round and Based on DNA sequence data and morphology, the 331 strains one end slightly acute or both ends round, 15.5–20.5(–29) × (4–) studied (Table 1) are assigned to 31 species, of which 29 species 4.5–5 µm, mean ± SD = 17.9 ± 2.4 × 4.7 ± 0.2 µm, L/W ratio = are within the C. acutatum species complex and two outside this 3.8. Appressoria single or in loose groups, medium to dark brown, group, including 21 species that proved to be new to science. Two smooth-walled, clavate, ovate or irregular outline, the edge entire species formed sexual morphs in vitro. All species studied in culture or undulate, sometimes lobate, (8–)9–14(–16.5) × (4–)5–7.5(–9.5) are characterised below. µm, mean ± SD = 11.3 ± 2.4 × 6.2 ± 1.2 µm, L/W ratio = 1.8. Asexual morph on Anthriscus stem. Conidiomata acervular, conidiophores formed on a cushion of pale brown angular cells, www.studiesinmycology.org 43 Damm et al . Table 1. Strains of Colletotrichum spp. studied, with collection details and GenBank accessions. Species Accession No. Host/Substrate Country GenBank No. ITS GAPDH CHS-1 HIS3 ACT TUB2 C. acerbum CBS 128530, ICMP 12921, PRJ 1199.3* Malus domestica, bitter rot of fruit New Zealand JQ948459 JQ948790 JQ949120 JQ949450 JQ949780 JQ950110 C. acutatum CBS 126521, PD 87/639 Anemone F1 hybride, cv. Melisande, curled leaf, Netherlands JQ948366 JQ948697 JQ949027 JQ949357 JQ949687 JQ950017 constriction of the stem IMI 223120, CPC 18870 Anemone sp., stem Australia JQ948353 JQ948684 JQ949014 JQ949344 JQ949674 JQ950004 CBS 127539, CPC 11738 Aspalathus linearis, anthracnose on stems and leaves South Africa JQ948377 JQ948708 JQ949038 JQ949368 JQ949698 JQ950028 CBS 127542, CPC 13880 Aspalathus linearis, anthracnose on stems and leaves South Africa JQ948379 JQ948710 JQ949040 JQ949370 JQ949700 JQ950030 CBS 129921, CPC 13881 Aspalathus linearis, anthracnose on stems and leaves South Africa JQ948380 JQ948711 JQ949041 JQ949371 JQ949701 JQ950031 CBS 129922, CPC 13885 Aspalathus linearis, anthracnose on stems and leaves South Africa JQ948381 JQ948712 JQ949042 JQ949372 JQ949702 JQ950032 CBS 127543, CPC 13886 Aspalathus linearis, anthracnose on stems and leaves South Africa JQ948382 JQ948713 JQ949043 JQ949373 JQ949703 JQ950033 CBS 127545, CPC 13947 Aspalathus linearis, anthracnose on stems and leaves South Africa JQ948383 JQ948714 JQ949044 JQ949374 JQ949704 JQ950034 CBS 129914, CPC 15490 Aspalathus linearis, anthracnose on stems and leaves South Africa JQ948384 JQ948715 JQ949045 JQ949375 JQ949705 JQ950035 CBS 129915, CPC 15512 Aspalathus linearis, anthracnose on stems and leaves South Africa JQ948385 JQ948716 JQ949046 JQ949376 JQ949706 JQ950036 CBS 129925, CPC 18023 Aspalathus linearis, anthracnose on stems and leaves South Africa JQ948386 JQ948717 JQ949047 JQ949377 JQ949707 JQ950037 CBS 127541, CPC 11751 Aspalathus linearis, anthracnose on stems and leaves South Africa JQ948378 JQ948709 JQ949039 JQ949369 JQ949699 JQ950029 CBS 127540, CPC 11749 Water that was used to irrigate Aspalathus linearis South Africa JQ948373 JQ948704 JQ949034 JQ949364 JQ949694 JQ950024 seedlings in a nursery CBS 129923, CPC 13887 Water that was used to irrigate Aspalathus linearis South Africa JQ948374 JQ948705 JQ949035 JQ949365 JQ949695 JQ950025 seedlings in a nursery CBS 129924, CPC 13891 Water that was used to irrigate Aspalathus linearis South Africa JQ948375 JQ948706 JQ949036 JQ949366 JQ949696 JQ950026 seedlings in a nursery CBS 127546, CPC 13950 Water that was used to irrigate Aspalathus linearis South Africa JQ948376 JQ948707 JQ949037 JQ949367 JQ949697 JQ950027 seedlings in a nursery CBS 144.29 Capsicum annuum, fruit Sri Lanka JQ948401 JQ948732 JQ949062 JQ949392 JQ949722 JQ950052 CBS 112996, ATCC 56816, STE-U 5292* Carica papaya Australia JQ005776 JQ948677 JQ005797 JQ005818 JQ005839 JQ005860 IMI 216370, CPC 18869 Coffea arabica, berry lesion Tanzania JQ948398 JQ948729 JQ949059 JQ949389 JQ949719 JQ950049 CBS 979.69 Coffea arabica Kenya JQ948400 JQ948731 JQ949061 JQ949391 JQ949721 JQ950051 IMI 319423, CPC 18877 Coffea arabica, berry lesion Kenya JQ948399 JQ948730 JQ949060 JQ949390 JQ949720 JQ950050 CBS 127602, BRIP 52691a, WAC 5416 Fragaria × ananassa, fruit rot Australia JQ948359 JQ948690 JQ949020 JQ949350 JQ949680 JQ950010 CBS 111993, STE-U 3037 Grevillea sp. Australia JQ948349 JQ948680 JQ949010 JQ949340 JQ949670 JQ950000 CBS 113599, STE-U 3038 Grevillea sp. Australia JQ948347 JQ948678 JQ949008 JQ949338 JQ949668 JQ949998 CBS 113600, STE-U 3039 Grevillea sp. Australia JQ948348 JQ948679 JQ949009 JQ949339 JQ949669 JQ949999 CBS 112759, STE-U 4470 Hakea sericea South Africa JQ948391 JQ948722 JQ949052 JQ949382 JQ949712 JQ950042 CBS 112760, STE-U 4468 Hakea sericea South Africa JQ948392 JQ948723 JQ949053 JQ949383 JQ949713 JQ950043 CBS 112993, STE-U 4469 Hakea sericea South Africa JQ948394 JQ948725 JQ949055 JQ949385 JQ949715 JQ950045 The CotriC ollet hum aCtum a ut species complex www.studiesinmycology.org Table 1. (Continued). Species Accession No. Host/Substrate Country GenBank No. ITS GAPDH CHS-1 HIS3 ACT TUB2 C. acutatum CBS 113007, STE-U 4462 Hakea sericea South Africa JQ948395 JQ948726 JQ949056 JQ949386 JQ949716 JQ950046 CBS 113009, STE-U 4467 Hakea sericea South Africa JQ948397 JQ948728 JQ949058 JQ949388 JQ949718 JQ950048 CBS 113008, STE-U 4463 Hakea sericea South Africa JQ948396 JQ948727 JQ949057 JQ949387 JQ949717 JQ950047 CBS 112761, STE-U 4461 Hakea sericea South Africa JQ948393 JQ948724 JQ949054 JQ949384 JQ949714 JQ950044 CBS 129919, CPC 13876 Hoodia sp. South Africa JQ948370 JQ948701 JQ949031 JQ949361 JQ949691 JQ950021 CBS 129920, CPC 13877 Hoodia sp. South Africa JQ948371 JQ948702 JQ949032 JQ949362 JQ949692 JQ950022 CBS 127544, CPC 13945 Hoodia sp. South Africa JQ948372 JQ948703 JQ949033 JQ949363 JQ949693 JQ950023 CBS 112990, STE-U 4448 Leucadendron sp., cv. Safari Sunset South Africa JQ948360 JQ948691 JQ949021 JQ949351 JQ949681 JQ950011 CBS 115202, STE-U 5233 Leucadendron sp., cv. Safari Sunset South Africa JQ948362 JQ948693 JQ949023 JQ949353 JQ949683 JQ950013 CBS 112994, STE-U 5122 Leucospermum sp. South Africa JQ948361 JQ948692 JQ949022 JQ949352 JQ949682 JQ950012 CBS 126505, PD 97/4384 Lobelia sp., cv. Blue Moon, leaf spots Netherlands JQ948387 JQ948718 JQ949048 JQ949378 JQ949708 JQ950038 CBS 369.73, NRCC 10081 Lupinus angustifolius New Zealand JQ948350 JQ948681 JQ949011 JQ949341 JQ949671 JQ950001 CBS 115393, STE-U 5433 Mimetes sp. South Africa JQ948365 JQ948696 JQ949026 JQ949356 JQ949686 JQ950016 IMI 384175, CPC 18936 Nerium oleander, leaf New Zealand JQ948369 JQ948700 JQ949030 JQ949360 JQ949690 JQ950020 CBS 127598, 223/09 Olea europaea South Africa JQ948363 JQ948694 JQ949024 JQ949354 JQ949684 JQ950014 CBS 129952, PT227, RB015 Olea europaea Portugal JQ948364 JQ948695 JQ949025 JQ949355 JQ949685 JQ950015 CBS 126506, PD 90/443 Phlox sp., leaf spots Netherlands JQ948388 JQ948719 JQ949049 JQ949379 JQ949709 JQ950039 CBS 110735, Lundquist 256, STE-U 163 Pinus radiata South Africa JQ948354 JQ948685 JQ949015 JQ949345 JQ949675 JQ950005 CBS 112979, Lundquist 258, STE-U 160 Pinus radiata South Africa JQ948355 JQ948686 JQ949016 JQ949346 JQ949676 JQ950006 CBS 112980, STE-U 164 Pinus radiata South Africa JQ948356 JQ948687 JQ949017 JQ949347 JQ949677 JQ950007 CBS 112981, Lundquist 253, STE-U 162 Pinus radiata South Africa JQ948357 JQ948688 JQ949018 JQ949348 JQ949678 JQ950008 CBS 127534, Lundquist 257, STE-U 161 Pinus radiata South Africa JQ948358 JQ948689 JQ949019 JQ949349 JQ949679 JQ950009 CBS 370.73, NRCC 10088 Pinus radiata New Zealand JQ948351 JQ948682 JQ949012 JQ949342 JQ949672 JQ950002 CBS 371.73, NRCC 10086 Pinus radiata New Zealand JQ948352 JQ948683 JQ949013 JQ949343 JQ949673 JQ950003 IMI 336479, CPC 18881 Pistacia vera, pericarp Australia JQ948367 JQ948698 JQ949028 JQ949358 JQ949688 JQ950018 CBS 113006, STE-U 4460 Protea cynaroides South Africa JQ948390 JQ948721 JQ949051 JQ949381 JQ949711 JQ950041 CBS 128499, ICMP 17992, PRJ 10.208 Pyrus pyrifolia, black spot on fallen, immature fruit New Zealand JQ948368 JQ948699 JQ949029 JQ949359 JQ949689 JQ950019 CSL 287, RB117 Statice sp. UK JQ948389 JQ948720 JQ949050 JQ949380 JQ949710 JQ950040 C. australe CBS 116478, HKUCC 2616* Trachycarpus fortunei South Africa JQ948455 JQ948786 JQ949116 JQ949446 JQ949776 JQ950106 CBS 131325, CPC 19820 Hakea sp. Australia JQ948456 JQ948787 JQ949117 JQ949447 JQ949777 JQ950107 C. brisbanense CBS 292.67, DPI 11711* Capsicum annuum Australia JQ948291 JQ948621 JQ948952 JQ949282 JQ949612 JQ949942 C. chrysanthemi IMI 364540, CPC 18930 Chrysanthemum coronarium, leaf spot China JQ948273 JQ948603 JQ948934 JQ949264 JQ949594 JQ949924 CBS 126518, PD 84/520 Carthamus sp., twisted stem Netherlands JQ948271 JQ948601 JQ948932 JQ949262 JQ949592 JQ949922 Damm et al . Table 1. (Continued). Species Accession No. Host/Substrate Country GenBank No. ITS GAPDH CHS-1 HIS3 ACT TUB2 C. chrysanthemi CBS 126519, PD 85/694 Chrysanthemum coronarium, vascular discoloration Netherlands JQ948272 JQ948602 JQ948933 JQ949263 JQ949593 JQ949923 C. cosmi CBS 853.73, PD 73/856* Cosmos sp., seed Netherlands JQ948274 JQ948604 JQ948935 JQ949265 JQ949595 JQ949925 C. costaricense CBS 330.75* Coffea arabica, cv. Typica, berry Costa Rica JQ948180 JQ948510 JQ948841 JQ949171 JQ949501 JQ949831 CBS 211.78, IMI 309622 Coffea sp., twig Costa Rica JQ948181 JQ948511 JQ948842 JQ949172 JQ949502 JQ949832 C. cuscutae IMI 304802, CPC 18873* Cuscuta sp. Dominica JQ948195 JQ948525 JQ948856 JQ949186 JQ949516 JQ949846 CBS 128498, ICMP 17991, PRJ 10.207 Actinidia sp., fruit rot of ripe fruit New Zealand JQ948337 JQ948667 JQ948998 JQ949328 JQ949658 JQ949988 CBS 126523, PD 88/642 Berberis sp., tips with black discolouration Netherlands JQ948322 JQ948652 JQ948983 JQ949313 JQ949643 JQ949973 IMI 363003, CPC 18928 Camellia reticulata China JQ948339 JQ948669 JQ949000 JQ949330 JQ949660 JQ949990 CBS 981.69 Coffea arabica, branch Angola JQ948327 JQ948657 JQ948988 JQ949318 JQ949648 JQ949978 CBS 125970, NB 852 Cyclamen sp., bulb, symptoms Italy JQ948341 JQ948671 JQ949002 JQ949332 JQ949662 JQ949992 CBS 128517, ARSEF 10222, ERL 1257, EHS 58* Fiorinia externa (elongate hemlock scale, insect) USA JQ948292 JQ948622 JQ948953 JQ949283 JQ949613 JQ949943 IMI 345578, CPC 19393, RB148 Fragaria × ananassa New Zealand JQ948334 JQ948664 JQ948995 JQ949325 JQ949655 JQ949985 IMI 345583, CPC 18889 Fragaria × ananassa, lesion New Zealand JQ948333 JQ948663 JQ948994 JQ949324 JQ949654 JQ949984 IMI 345575, CPC 18888 Fragaria × ananassa, lesion New Zealand JQ948332 JQ948662 JQ948993 JQ949323 JQ949653 JQ949983 CBS 128529, ICMP 1701, PRJ 659 Fragaria × ananassa, root New Zealand JQ948331 JQ948661 JQ948992 JQ949322 JQ949652 JQ949982 CSL 1259, RB057 Fragaria × ananassa, petiole UK JQ948330 JQ948660 JQ948991 JQ949321 JQ949651 JQ949981 CBS 127611, DAOM 213703, CF-132 Fragaria × ananassa USA JQ948328 JQ948658 JQ948989 JQ949319 JQ949649 JQ949979 CBS 127614, DAOM 213712 Fragaria × ananassa USA JQ948329 JQ948659 JQ948990 JQ949320 JQ949650 JQ949980 CBS 129940 Grevillea sp. Germany JQ948335 JQ948665 JQ948996 JQ949326 JQ949656 JQ949986 CBS 129941 Grevillea sp. Germany JQ948336 JQ948666 JQ948997 JQ949327 JQ949657 JQ949987 IMI 384569, CPC 18938 Kalmia sp. USA JQ948340 JQ948670 JQ949001 JQ949331 JQ949661 JQ949991 CSL 473, RB131 Liriodendron tulipifera UK JQ948345 JQ948675 JQ949006 JQ949336 JQ949666 JQ949996 CSL 318, RB132 Magnolia sp. UK JQ948346 JQ948676 JQ949007 JQ949337 JQ949667 JQ949997 CBS 786.86, Malus sylvestris, fruit Italy JQ948303 JQ948633 JQ948964 JQ949294 JQ949624 JQ949954 CBS 126381 Malus domestica, cv. Junami, fruit Netherlands JQ948302 JQ948632 JQ948963 JQ949293 JQ949623 JQ949953 CBS 129930, 2.7.3(T1326), ICMP 1791 Malus domestica New Zealand JQ948304 JQ948634 JQ948965 JQ949295 JQ949625 JQ949955 CBS 128555, ICMP 12923, PRJ 839-1 Malus domestica, bitter rot of fruit New Zealand JQ948305 JQ948635 JQ948966 JQ949296 JQ949626 JQ949956 CBS 129931, 1.4.51a(T1166) Malus domestica USA JQ948294 JQ948624 JQ948955 JQ949285 JQ949615 JQ949945 CBS 129932, 5.7.52 Malus domestica USA JQ948295 JQ948625 JQ948956 JQ949286 JQ949616 JQ949946 CBS 112995, STE-U 5287 Malus domestica USA JQ948298 JQ948628 JQ948959 JQ949289 JQ949619 JQ949949 CBS 127538, STE-U 5290 Malus domestica USA JQ948300 JQ948630 JQ948961 JQ949291 JQ949621 JQ949951 ATCC 28992, CPC 19391 Malus domestica USA JQ948297 JQ948627 JQ948958 JQ949288 JQ949618 JQ949948 CBS 129938, APPY3 Malus domestica USA JQ948296 JQ948626 JQ948957 JQ949287 JQ949617 JQ949947 The CotriC ollet hum aCtum a ut species complex www.studiesinmycology.org Table 1. (Continued). Species Accession No. Host/Substrate Country GenBank No. ITS GAPDH CHS-1 HIS3 ACT TUB2 C. fioriniae CBS 125396, GJS 08-140A Malus domestica, fruit lesion USA JQ948299 JQ948629 JQ948960 JQ949290 JQ949620 JQ949950 IMI 324996, CPC 18880 Malus pumila USA JQ948301 JQ948631 JQ948962 JQ949292 JQ949622 JQ949952 CBS 235.49 Malus sp. USA JQ948325 JQ948655 JQ948986 JQ949316 JQ949646 JQ949976 CBS 127601, BRIP 28761a Mangifera indica, stem endophyte Australia JQ948311 JQ948641 JQ948972 JQ949302 JQ949632 JQ949962 CBS 167.86 Myriophyllum spicatum, submerged stem USA JQ948324 JQ948654 JQ948985 JQ949315 JQ949645 JQ949975 CBS 129946, PT170, RB021 Olea europaea Portugal JQ948342 JQ948672 JQ949003 JQ949333 JQ949663 JQ949993 CBS 126509, PD 92/1060 Parthenocissus sp., cv. Disci, soft rot Netherlands JQ948316 JQ948646 JQ948977 JQ949307 JQ949637 JQ949967 CBS 125956 , NB 112 Penstemon sp., symptoms in the bottom part of the plant Netherlands JQ948321 JQ948651 JQ948982 JQ949312 JQ949642 JQ949972 CBS 293.67, DPI 13120 Persea americana Australia JQ948310 JQ948640 JQ948971 JQ949301 JQ949631 JQ949961 CBS 127600, BRIP 20127a Persea americana, fruit rot Australia JQ948308 JQ948638 JQ948969 JQ949299 JQ949629 JQ949959 CBS 127599, BRIP 29284a Persea americana, fruit rot Australia JQ948309 JQ948639 JQ948970 JQ949300 JQ949630 JQ949960 IMI 324991, CPC 18878 Piper nigrum Unknown JQ948338 JQ948668 JQ948999 JQ949329 JQ949659 JQ949989 CBS 126526, PD 93/1373, BBA 70343 Primula sp., leaf spots Netherlands JQ948323 JQ948653 JQ948984 JQ949314 JQ949644 JQ949974 CBS 124958 Pyrus sp., fruit rot USA JQ948306 JQ948636 JQ948967 JQ949297 JQ949627 JQ949957 ATCC 12097, CPC 19392 Rhododendron sp. USA JQ948307 JQ948637 JQ948968 JQ949298 JQ949628 JQ949958 CBS 200.35 Rubus sp. USA JQ948293 JQ948623 JQ948954 JQ949284 JQ949614 JQ949944 CBS 490.92, ATCC 60260 Solanum lycopersicum New Zealand JQ948326 JQ948656 JQ948987 JQ949317 JQ949647 JQ949977 CBS 124962 Solanum lycopersicum, fruit rot USA JQ948319 JQ948649 JQ948980 JQ949310 JQ949640 JQ949970 CBS 124963 Solanum lycopersicum, fruit rot USA JQ948320 JQ948650 JQ948981 JQ949311 JQ949641 JQ949971 CBS 129948, RB128 Tulipa sp. UK JQ948344 JQ948674 JQ949005 JQ949335 JQ949665 JQ949995 CBS 126508, PD 92/906, BBA 70339 Vaccinium corymbosum (blueberry), fruit rot Netherlands JQ948315 JQ948645 JQ948976 JQ949306 JQ949636 JQ949966 CBS 119293, MEP 1322 Vaccinium corymbosum (blueberry), fruit New Zealand JQ948314 JQ948644 JQ948975 JQ949305 JQ949635 JQ949965 CBS 119186, MEP 1325 Vaccinium sp., fruit New Zealand JQ948312 JQ948642 JQ948973 JQ949303 JQ949633 JQ949963 CBS 119292, MEP 1323 Vaccinium sp., fruit New Zealand JQ948313 JQ948643 JQ948974 JQ949304 JQ949634 JQ949964 CBS 127537, STE-U 5289 Vaccinium sp. (blueberry) USA JQ948318 JQ948648 JQ948979 JQ949309 JQ949639 JQ949969 CBS 129916, CPC 16823 Vaccinium sp. (blueberry) USA JQ948317 JQ948647 JQ948978 JQ949308 JQ949638 JQ949968 CBS 129947, CR46, RB022 Vitis vinifera Portugal JQ948343 JQ948673 JQ949004 JQ949334 JQ949664 JQ949994 C. godetiae CBS 796.72 Aeschynomene virginica USA JQ948407 JQ948738 JQ949068 JQ949398 JQ949728 JQ950058 CBS 131332 Agrimonia eupatoria, leaf spot Austria JQ948429 JQ948760 JQ949090 JQ949420 JQ949750 JQ950080 CBS 126512, PD 88/958 Bonzai, sunken brown spots on fruit Netherlands JQ948412 JQ948743 JQ949073 JQ949403 JQ949733 JQ950063 IMI 351248, CPC 18894 Ceanothus sp. UK JQ948433 JQ948764 JQ949094 JQ949424 JQ949754 JQ950084 CBS 160.50 Citrus aurantium, fruit rot Unknown JQ948406 JQ948737 JQ949067 JQ949397 JQ949727 JQ950057 CBS 133.44* Clarkia hybrida, cv. Kelvon Glory, seed Denmark JQ948402 JQ948733 JQ949063 JQ949393 JQ949723 JQ950053 Damm et al . Table 1. (Continued). Species Accession No. Host/Substrate Country GenBank No. ITS GAPDH CHS-1 HIS3 ACT TUB2 C. godetiae IMI 351262, CPC 18897 Fragaria × ananassa Belgium JQ948422 JQ948753 JQ949083 JQ949413 JQ949743 JQ950073 IMI 345035, CPC 18885 Fragaria vesca France JQ948425 JQ948756 JQ949086 JQ949416 JQ949746 JQ950076 IMI 351589, CPC 18921 Fragaria × ananassa Ireland JQ948423 JQ948754 JQ949084 JQ949414 JQ949744 JQ950074 CBS 125972, PD 85/456 Fragaria × ananassa Netherlands JQ948416 JQ948747 JQ949077 JQ949407 JQ949737 JQ950067 CBS 126376, PD 95/5903 Fragaria × ananassa Netherlands JQ948417 JQ948748 JQ949078 JQ949408 JQ949738 JQ950068 CBS 126516, PD 88/548 Fragaria × ananassa, fruit rot Netherlands JQ948418 JQ948749 JQ949079 JQ949409 JQ949739 JQ950069 IMI 345026, CPC 18882 Fragaria × ananassa Spain JQ948424 JQ948755 JQ949085 JQ949415 JQ949745 JQ950075 CBS 125974, PD 88/858 Fragaria × ananassa UK JQ948419 JQ948750 JQ949080 JQ949410 JQ949740 JQ950070 CBS 126503, PD 88/859, BBA 70342 Fragaria × ananassa UK JQ948420 JQ948751 JQ949081 JQ949411 JQ949741 JQ950071 IMI 351253, CPC 18895 Fragaria × ananassa UK JQ948421 JQ948752 JQ949082 JQ949412 JQ949742 JQ950072 CBS 171.59 Juglans regia Unknown JQ948405 JQ948736 JQ949066 JQ949396 JQ949726 JQ950056 CBS 131331 Juglans regia, leaf spot Austria JQ948404 JQ948735 JQ949065 JQ949395 JQ949725 JQ950055 IMI 362149b, CPC 18927 Laurus nobilis, dead fallen leaf UK JQ948427 JQ948758 JQ949088 JQ949418 JQ949748 JQ950078 CBS 129942 Mahonia aquifolium, leaf spots Germany JQ948428 JQ948759 JQ949089 JQ949419 JQ949749 JQ950079 CBS 198.53 Malus sylvestris, fruit Netherlands JQ948432 JQ948763 JQ949093 JQ949423 JQ949753 JQ950083 CBS 285.50 Malus sylvestris, fruit Unknown JQ948403 JQ948734 JQ949064 JQ949394 JQ949724 JQ950054 CBS 155.25 Nut shell Unknown JQ948410 JQ948741 JQ949071 JQ949401 JQ949731 JQ950061 CBS 193.32 Olea europaea Greece JQ948415 JQ948746 JQ949076 JQ949406 JQ949736 JQ950066 CBS 130251, OL 10, IMI 398854 Olea europaea Italy JQ948413 JQ948744 JQ949074 JQ949404 JQ949734 JQ950064 CBS 130252, IMI 398855, OL 20 Olea europaea Italy JQ948414 JQ948745 JQ949075 JQ949405 JQ949735 JQ950065 CBS 126520, PD 87/383 Parthenocissus sp., leaf and stem spots Netherlands JQ948426 JQ948757 JQ949087 JQ949417 JQ949747 JQ950077 CBS 129911, CPC 15124 Podocarpus sp. South Africa JQ948434 JQ948765 JQ949095 JQ949425 JQ949755 JQ950085 CBS 129912, CPC 15125 Podocarpus sp. South Africa JQ948435 JQ948766 JQ949096 JQ949426 JQ949756 JQ950086 CBS 129913, CPC 15126 Podocarpus sp. South Africa JQ948436 JQ948767 JQ949097 JQ949427 JQ949757 JQ950087 CBS 126527, PD 93/1748 Prunus avium UK JQ948408 JQ948739 JQ949069 JQ949399 JQ949729 JQ950059 CBS 126522, PD 88/472, BBA 70345 Prunus cerasus, fruit, die-back Netherlands JQ948411 JQ948742 JQ949072 JQ949402 JQ949732 JQ950062 CBS 129934, ALM-IKS-7Q Prunus dulcis Israel JQ948431 JQ948762 JQ949092 JQ949422 JQ949752 JQ950082 IMI 376331, CPC 18933 Prunus sp., fruit Norway JQ948409 JQ948740 JQ949070 JQ949400 JQ949730 JQ950060 IMI 381927, CPC 18935 Rubus idaeus, cane Turkey JQ948438 JQ948769 JQ949099 JQ949429 JQ949759 JQ950089 CBS 862.70 Sambucus nigra, fruit Netherlands JQ948437 JQ948768 JQ949098 JQ949428 JQ949758 JQ950088 CBS 129951, RB118 Vitis sp. UK JQ948430 JQ948761 JQ949091 JQ949421 JQ949751 JQ950081 CBS 129917, CPC 16002 Schinus molle Mexico JQ948441 JQ948772 JQ949102 JQ949432 JQ949762 JQ950092 CBS 129809, T.A.1 Solanum betaceum, fruit, anthracnose Colombia JQ948439 JQ948770 JQ949100 JQ949430 JQ949760 JQ950090 The CotriC ollet hum aCtum a ut species complex www.studiesinmycology.org Table 1. (Continued). Species Accession No. Host/Substrate Country GenBank No. ITS GAPDH CHS-1 HIS3 ACT TUB2 C. godetiae CBS 129816, T.A.8 Solanum betaceum, fruit, anthracnose Colombia JQ948440 JQ948771 JQ949101 JQ949431 JQ949761 JQ950091 CBS 127561, CPC 16426 Ugni molinae, twig, tip necrosis Chile JQ948442 JQ948773 JQ949103 JQ949433 JQ949763 JQ950093 C. guajavae IMI 350839, CPC 18893* Psidium guajava, fruit India JQ948270 JQ948600 JQ948931 JQ949261 JQ949591 JQ949921 C. indonesiense CBS 127551, CPC 14986* Eucalyptus sp. Indonesia JQ948288 JQ948618 JQ948949 JQ949279 JQ949609 JQ949939 C. johnstonii IMI 357027, CPC 18924, PRJ 1125.005 Citrus sp. New Zealand JQ948443 JQ948774 JQ949104 JQ949434 JQ949764 JQ950094 CBS 128532, ICMP 12926, PRJ 1139.3* Solanum lycopersicum, fruit rot New Zealand JQ948444 JQ948775 JQ949105 JQ949435 JQ949765 JQ950095 C. kinghornii CBS 198.35* Phormium sp. UK JQ948454 JQ948785 JQ949115 JQ949445 JQ949775 JQ950105 C. laticiphilum CBS 112989, IMI 383015, STE-U 5303* Hevea brasiliensis India JQ948289 JQ948619 JQ948950 JQ949280 JQ949610 JQ949940 CBS 129827, CH2 Hevea brasiliensis, leaf, anthracnose Colombia JQ948290 JQ948620 JQ948951 JQ949281 JQ949611 JQ949941 C. limetticola CBS 114.14* Citrus aurantifolia, young twig USA, Florida JQ948193 JQ948523 JQ948854 JQ949184 JQ949514 JQ949844 C. lupini IMI 351261, CPC 18896 Camellia sp. UK JQ948177 JQ948507 JQ948838 JQ949168 JQ949498 JQ949828 CBS 129944, CMG12, RB042 Cinnamomum verum Portugal JQ948178 JQ948508 JQ948839 JQ949169 JQ949499 JQ949829 IMI 375715, CPC 19390 Lupinus albus Australia JQ948161 JQ948491 JQ948822 JQ949152 JQ949482 JQ949812 CBS 109224, BBA 70399 Lupinus albus Austria JQ948172 JQ948502 JQ948833 JQ949163 JQ949493 JQ949823 CBS 109216, BBA 63879 Lupinus mutabilis Bolivia JQ948156 JQ948486 JQ948817 JQ949147 JQ949477 JQ949807 CBS 109226, BBA 71249 Lupinus albus Canada JQ948158 JQ948488 JQ948819 JQ949149 JQ949479 JQ949809 CBS 513.97, LARS 401 Lupinus polyphyllus Costa Rica JQ948157 JQ948487 JQ948818 JQ949148 JQ949478 JQ949808 CBS 509.97, LARS 178 Lupinus albus France JQ948159 JQ948489 JQ948820 JQ949150 JQ949480 JQ949810 CBS 507.97, LARS 163 Lupinus albus France JQ948166 JQ948496 JQ948827 JQ949157 JQ949487 JQ949817 CBS 109220, BBA 70317 Lupinus albus Germany JQ948168 JQ948498 JQ948829 JQ949159 JQ949489 JQ949819 CBS 109221, BBA 70352 Lupinus albus Germany JQ948169 JQ948499 JQ948830 JQ949160 JQ949490 JQ949820 CBS 109222, BBA 70358 Lupinus albus Germany JQ948170 JQ948500 JQ948831 JQ949161 JQ949491 JQ949821 CBS 485.97 Lupinus albus, cv. Minori Germany JQ948164 JQ948494 JQ948825 JQ949155 JQ949485 JQ949815 CBS 109223, BBA 70385 Lupinus angustifolius Germany JQ948171 JQ948501 JQ948832 JQ949162 JQ949492 JQ949822 CBS 109219, BBA 70073 Lupinus polyphyllus Germany JQ948167 JQ948497 JQ948828 JQ949158 JQ949488 JQ949818 CBS 109217, BBA 68334 Lupinus sp. Germany JQ948163 JQ948493 JQ948824 JQ949154 JQ949484 JQ949814 CBS 126525, PD 89/1303, BBA 70346 Lupinus sp., leaf spots Netherlands JQ948174 JQ948504 JQ948835 JQ949165 JQ949495 JQ949825 CBS 126371, PD 93/1436, BBA 70344 Lupinus sp., petiole with sunken spots Netherlands JQ948165 JQ948495 JQ948826 JQ949156 JQ949486 JQ949816 CBS 109227, BBA 71310 Lupinus luteus Poland JQ948173 JQ948503 JQ948834 JQ949164 JQ949494 JQ949824 CBS 119142, CMW 9931 Lupinus albus, anthracnose South Africa JQ948175 JQ948505 JQ948836 JQ949166 JQ949496 JQ949826 CBS 119143, CMW 9933 Lupinus albus, anthracnose South Africa JQ948176 JQ948506 JQ948837 JQ949167 JQ949497 JQ949827 CBS 122746, BPI 871840, AR 2826 Lupinus sp., Russell hybrid mix USA JQ948162 JQ948492 JQ948823 JQ949153 JQ949483 JQ949813 CBS 109225, BBA 70884* Lupinus albus Ukraine JQ948155 JQ948485 JQ948816 JQ949146 JQ949476 JQ949806 Damm et al . Table 1. (Continued). Species Accession No. Host/Substrate Country GenBank No. ITS GAPDH CHS-1 HIS3 ACT TUB2 C. lupini CBS 466.76 Manihot utilissima, leaf Rwanda JQ948160 JQ948490 JQ948821 JQ949151 JQ949481 JQ949811 C. melonis CBS 159.84* Cucumis melo, peel of fruit Brazil JQ948194 JQ948524 JQ948855 JQ949185 JQ949515 JQ949845 C. nymphaeae CBS 100064 Anemone sp. Netherlands JQ948224 JQ948554 JQ948885 JQ949215 JQ949545 JQ949875 CBS 100065 Anemone sp. Netherlands JQ948225 JQ948555 JQ948886 JQ949216 JQ949546 JQ949876 CBS 130.80 Anemone sp. Italy JQ948226 JQ948556 JQ948887 JQ949217 JQ949547 JQ949877 CBS 129935, ANE-4 Anemone sp. Israel JQ948227 JQ948557 JQ948888 JQ949218 JQ949548 JQ949878 CBS 361.79 Anemone coronaria Netherlands JQ948248 JQ948578 JQ948909 JQ949239 JQ949569 JQ949899 CBS 126383, PD 84/121 Anemone coronaria, cv. de Caen group Netherlands JQ948221 JQ948551 JQ948882 JQ949212 JQ949542 JQ949872 CBS 126382, PD 79/648 Anemone coronaria, cv. de Caen group, curl disease Netherlands JQ948220 JQ948550 JQ948881 JQ949211 JQ949541 JQ949871 CBS 126511, PD 88/673 Anemone coronaria, cv. de Caen group, stengeltop, Netherlands JQ948222 JQ948552 JQ948883 JQ949213 JQ949543 JQ949873 curled stengeltop CBS 126513, PD 91/1282, BBA 70350 Anemone sp., stem, curl disease Netherlands JQ948223 JQ948553 JQ948884 JQ949214 JQ949544 JQ949874 CBS 126528, PD 94/921-2, BBA 70348 Capsicum sp. Indonesia JQ948219 JQ948549 JQ948880 JQ949210 JQ949540 JQ949870 IMI 379162, CPC 18934 Capsicum annuum, seed Zimbabwe JQ948218 JQ948548 JQ948879 JQ949209 JQ949539 JQ949869 CBS 122110, AR 4455 Fragaria × ananassa, cv. Redchief, fruit rot Bulgaria JQ948235 JQ948565 JQ948896 JQ949226 JQ949556 JQ949886 CBS 122111, AR 4456 Fragaria × ananassa, cv. Redchief, fruit rot Bulgaria JQ948236 JQ948566 JQ948897 JQ949227 JQ949557 JQ949887 CBS 122121, AR 4457 Fragaria × ananassa, cv. Redchief, fruit rot Bulgaria JQ948237 JQ948567 JQ948898 JQ949228 JQ949558 JQ949888 CBS 127608, DAOM 212589, 89M-112 Fragaria × ananassa Canada JQ948264 JQ948594 JQ948925 JQ949255 JQ949585 JQ949915 IMI 348497, CPC 18891 Fragaria × ananassa, crown France JQ948240 JQ948570 JQ948901 JQ949231 JQ949561 JQ949891 IMI 345053, CPC 18887 Fragaria × ananassa France JQ948239 JQ948569 JQ948900 JQ949230 JQ949560 JQ949890 IMI 348502, CPC 18892 Fragaria × ananassa, crown France JQ948238 JQ948568 JQ948899 JQ949229 JQ949559 JQ949889 IMI 391664, CPC 18940 Fragaria × ananassa Israel JQ948251 JQ948581 JQ948912 JQ949242 JQ949572 JQ949902 CBS 129936, TUT137A Fragaria × ananassa Israel JQ948252 JQ948582 JQ948913 JQ949243 JQ949573 JQ949903 CBS 129937, TUT5954 Fragaria × ananassa Israel JQ948253 JQ948583 JQ948914 JQ949244 JQ949574 JQ949904 CBS 126372, PD 93/1666A Fragaria × ananassa, cv. Idea Italy JQ948242 JQ948572 JQ948903 JQ949233 JQ949563 JQ949893 IMI 345032, CPC 18883 Fragaria × ananassa, fruit Italy JQ948241 JQ948571 JQ948902 JQ949232 JQ949562 JQ949892 IMI 301119, CPC 18872 Fragaria vesca Kenya JQ948266 JQ948596 JQ948927 JQ949257 JQ949587 JQ949917 CBS 125966, NB 732 Fragaria × ananassa Netherlands JQ948247 JQ948577 JQ948908 JQ949238 JQ949568 JQ949898 CBS 126377, PD 95/9269 Fragaria × ananassa Netherlands JQ948233 JQ948563 JQ948894 JQ949224 JQ949554 JQ949884 CBS 130239 Fragaria × ananassa, fruit anthracnose Netherlands JQ948250 JQ948580 JQ948911 JQ949241 JQ949571 JQ949901 CBS 125961, NB 559 Fragaria × ananassa, root discoloration Netherlands JQ948249 JQ948579 JQ948910 JQ949240 JQ949570 JQ949900 CBS 125958, NB 155 Fragaria × ananassa, seed Netherlands JQ948245 JQ948575 JQ948906 JQ949236 JQ949566 JQ949896 CBS 125959, NB 156 Fragaria × ananassa, seed Netherlands JQ948246 JQ948576 JQ948907 JQ949237 JQ949567 JQ949897 The CotriC ollet hum aCtum a ut species complex www.studiesinmycology.org Table 1. (Continued). Species Accession No. Host/Substrate Country GenBank No. ITS GAPDH CHS-1 HIS3 ACT TUB2 C. nymphaeae CBS 126504, C 105 Fragaria × ananassa South Africa JQ948265 JQ948595 JQ948926 JQ949256 JQ949586 JQ949916 CBS 112202 Fragaria sp., fruit lesions Spain JQ948234 JQ948564 JQ948895 JQ949225 JQ949555 JQ949885 IMI 364856, CPC 18931 Fragaria × ananassa, crown Spain JQ948244 JQ948574 JQ948905 JQ949235 JQ949565 JQ949895 IMI 360928, CPC 18926 Fragaria × ananassa, fruit lesion Switzerland JQ948243 JQ948573 JQ948904 JQ949234 JQ949564 JQ949894 IMI 299103, CPC 18871 Fragaria vesca UK JQ948231 JQ948561 JQ948892 JQ949222 JQ949552 JQ949882 CBS 125973, PD 88/857 Fragaria × ananassa UK JQ948232 JQ948562 JQ948893 JQ949223 JQ949553 JQ949883 CBS 129918, MUCL 44838 Fragaria sp. Unknown JQ948254 JQ948584 JQ948915 JQ949245 JQ949575 JQ949905 IMI 311743, CPC 18874 Fragaria sp., fruit lesion USA JQ948258 JQ948588 JQ948919 JQ949249 JQ949579 JQ949909 CBS 127612, DAOM 213709, H-1984 Fragaria × ananassa USA JQ948230 JQ948560 JQ948891 JQ949221 JQ949551 JQ949881 CBS 129928, 216 Fragaria × ananassa USA JQ948228 JQ948558 JQ948889 JQ949219 JQ949549 JQ949879 CBS 129929, 2.6.23 Fragaria × ananassa USA JQ948229 JQ948559 JQ948890 JQ949220 JQ949550 JQ949880 CBS 126366, PD 92/785 Fragaria × ananassa USA JQ948255 JQ948585 JQ948916 JQ949246 JQ949576 JQ949906 CBS 126367, PD 92/786 Fragaria × ananassa USA JQ948256 JQ948586 JQ948917 JQ949247 JQ949577 JQ949907 CBS 126370, PD 92/790 Fragaria × ananassa USA JQ948257 JQ948587 JQ948918 JQ949248 JQ949578 JQ949908 IMI 324995, CPC 18879 Fragaria × ananassa USA JQ948259 JQ948589 JQ948920 JQ949250 JQ949580 JQ949910 CBS 127609, DAOM 213394, CA-37-2-2 Fragaria × ananassa USA JQ948260 JQ948590 JQ948921 JQ949251 JQ949581 JQ949911 CBS 127610, DAOM 213395, CA-37-2-4 Fragaria × ananassa USA JQ948261 JQ948591 JQ948922 JQ949252 JQ949582 JQ949912 CBS 129933, Goff99 Fragaria × ananassa USA JQ948262 JQ948592 JQ948923 JQ949253 JQ949583 JQ949913 IMI 348177, CPC 18890 Fragaria × ananassa, crown USA JQ948263 JQ948593 JQ948924 JQ949254 JQ949584 JQ949914 CBS 119294, MEP 1534 Leucaena sp., fruit Mexico JQ948205 JQ948535 JQ948866 JQ949196 JQ949526 JQ949856 CBS 129926, CPC 18719 Litter Thailand JQ948216 JQ948546 JQ948877 JQ949207 JQ949537 JQ949867 CBS 173.51 Mahonia aquifolium, leaf Italy JQ948200 JQ948530 JQ948861 JQ949191 JQ949521 JQ949851 IMI 370491, CPC 18932 Malus pumila, fruit Brazil JQ948204 JQ948534 JQ948865 JQ949195 JQ949525 JQ949855 CBS 516.78, IAM 14670 Nuphar luteum, leaf spot Netherlands JQ948198 JQ948528 JQ948859 JQ949189 JQ949519 JQ949849 CBS 526.77 Nymphaea alba, leaf Netherlands JQ948199 JQ948529 JQ948860 JQ949190 JQ949520 JQ949850 CBS 515.78* Nymphaea alba, leaf spot Netherlands JQ948197 JQ948527 JQ948858 JQ949188 JQ949518 JQ949848 CBS 126507, PD 91/1392 Oenothera sp., black staining of stem Netherlands JQ948203 JQ948533 JQ948864 JQ949194 JQ949524 JQ949854 CBS 129945, PT135, RB012 Olea europaea Portugal JQ948201 JQ948531 JQ948862 JQ949192 JQ949522 JQ949852 CBS 231.49 Olea europaea Portugal JQ948202 JQ948532 JQ948863 JQ949193 JQ949523 JQ949853 IMI 360386, CPC 18925 Pelargonium graveolens, petiole, leaf and twig India JQ948206 JQ948536 JQ948867 JQ949197 JQ949527 JQ949857 CSL 455, RB126 Photinia sp. UK JQ948217 JQ948547 JQ948878 JQ949208 JQ949538 JQ949868 CBS 482.82 Protea sp. Australia JQ948213 JQ948543 JQ948874 JQ949204 JQ949534 JQ949864 CBS 115408, STE-U 5357 Protea cynaroides South Africa JQ948212 JQ948542 JQ948873 JQ949203 JQ949533 JQ949863 Damm et al . Table 1. (Continued). Species Accession No. Host/Substrate Country GenBank No. ITS GAPDH CHS-1 HIS3 ACT TUB2 C. nymphaeae CBS 112992, STE-U 4452 Protea magnifica South Africa JQ948207 JQ948537 JQ948868 JQ949198 JQ949528 JQ949858 CBS 113002, STE-U 4456 Protea repens South Africa JQ948208 JQ948538 JQ948869 JQ949199 JQ949529 JQ949859 CBS 113003, STE-U 4457 Protea sp. South Africa JQ948209 JQ948539 JQ948870 JQ949200 JQ949530 JQ949860 CBS 113004, STE-U 4458 Protea sp. South Africa JQ948210 JQ948540 JQ948871 JQ949201 JQ949531 JQ949861 CBS 113005, STE-U 4459 Protea sp. South Africa JQ948211 JQ948541 JQ948872 JQ949202 JQ949532 JQ949862 CBS 114188, STE-U 2971 Protea sp., cv. Pink Ice Unknown JQ948214 JQ948544 JQ948875 JQ949205 JQ949535 JQ949865 CBS 158.27 Phaseolus sp. Netherlands JQ948215 JQ948545 JQ948876 JQ949206 JQ949536 JQ949866 C. orchidophilum CBS 631.80 Ascocenda sp. USA JQ948152 JQ948482 JQ948813 JQ949143 JQ949473 JQ949803 CBS 119291, MEP 1545 Cycnoches aureum Panama JQ948154 JQ948484 JQ948815 JQ949145 JQ949475 JQ949805 CBS 632.80* Dendrobium sp. USA JQ948151 JQ948481 JQ948812 JQ949142 JQ949472 JQ949802 IMI 309357, CPC 16815 Phalaenopsis sp. UK JQ948153 JQ948483 JQ948814 JQ949144 JQ949474 JQ949804 C. paxtonii CBS 502.97, LARS 58 Musa nana “West Indies” JQ948286 JQ948616 JQ948947 JQ949277 JQ949607 JQ949937 IMI 165753, CPC 18868* Musa sp. Saint Lucia JQ948285 JQ948615 JQ948946 JQ949276 JQ949606 JQ949936 C. phormii CBS 102054 Phormium sp., leaf spot New Zealand JQ948448 JQ948779 JQ949109 JQ949439 JQ949769 JQ950099 CBS 118201, MEP 1334 Phormium sp., leaf New Zealand JQ948449 JQ948780 JQ949110 JQ949440 JQ949770 JQ950100 CBS 199.35, DSM 1168 Phormium sp. UK JQ948447 JQ948778 JQ949108 JQ949438 JQ949768 JQ950098 CBS 118191, AR 3787 Phormium sp., leaf South Africa JQ948453 JQ948784 JQ949114 JQ949444 JQ949774 JQ950104 CBS 118197, AR 3389 Phormium sp. New Zealand JQ948450 JQ948781 JQ949111 JQ949441 JQ949771 JQ950101 CBS 124953 Phormium sp., leaf Netherlands JQ948452 JQ948783 JQ949113 JQ949443 JQ949773 JQ950103 CBS 483.82 Phormium tenax New Zealand JQ948451 JQ948782 JQ949112 JQ949442 JQ949772 JQ950102 CBS 118194, AR 3546* Phormium sp. Germany JQ948446 JQ948777 JQ949107 JQ949437 JQ949767 JQ950097 C. pseudoacutatum CBS 436.77* Pinus radiata Chile JQ948480 JQ948811 JQ949141 JQ949471 JQ949801 JQ950131 C. pyricola CBS 128531, ICMP 12924, PRJ 977.1* Pyrus communis, fruit rot New Zealand JQ948445 JQ948776 JQ949106 JQ949436 JQ949766 JQ950096 C. rhombiforme CBS 129953, PT250, RB011* Olea europaea Portugal JQ948457 JQ948788 JQ949118 JQ949448 JQ949778 JQ950108 CBS 131322, DAOM 233253, C10, MS1L34 Vaccinium macrocarpum USA JQ948458 JQ948789 JQ949119 JQ949449 JQ949779 JQ950109 C. salicis CBS 129972, MP1, RB096 Acer platanoides, symptomatic leaves USA JQ948466 JQ948797 JQ949127 JQ949457 JQ949787 JQ950117 CBS 129973, MP2, RB097 Acer platanoides, symptomatic leaves USA JQ948467 JQ948798 JQ949128 JQ949458 JQ949788 JQ950118 CBS 465.83 Araucaria excelsa, anthracnose and dieback USA JQ948468 JQ948799 JQ949129 JQ949459 JQ949789 JQ950119 IMI 345585, CPC 19376 Fragaria × ananassa, petiole spot New Zealand JQ948476 JQ948807 JQ949137 JQ949467 JQ949797 JQ950127 CBS 128556, ICMP 12954, PRJ 11071 Fragaria × ananassa, fruit rot New Zealand JQ948473 JQ948804 JQ949134 JQ949464 JQ949794 JQ950124 CBS 128557, ICMP 12955, PRJ 1115.1 Fragaria × ananassa, fruit rot New Zealand JQ948474 JQ948805 JQ949135 JQ949465 JQ949795 JQ950125 IMI 345581, CPC 19377 Fragaria × ananassa, lesion New Zealand JQ948475 JQ948806 JQ949136 JQ949466 JQ949796 JQ950126 CBS 113.14 Malus domestica, cv. Manks Küchenapfel, fruit Germany JQ948478 JQ948809 JQ949139 JQ949469 JQ949799 JQ950129 The CotriC ollet hum aCtum a ut species complex www.studiesinmycology.org Table 1. (Continued). Species Accession No. Host/Substrate Country GenBank No. ITS GAPDH CHS-1 HIS3 ACT TUB2 C. salicis IMI 385055, CPC 18939 Malus domestica, fruit New Zealand JQ948472 JQ948803 JQ949133 JQ949463 JQ949793 JQ950123 CBS 180.97, PD 96003647 Populus canadensis, cv. Dorschkamp Netherlands JQ948464 JQ948795 JQ949125 JQ949455 JQ949785 JQ950115 CBS 223.36 Populus sp. Netherlands JQ948465 JQ948796 JQ949126 JQ949456 JQ949786 JQ950116 CBS 128559, ICMP 12957, PRJ 1160.1 Pyrus pyrifolia, fruit rot New Zealand JQ948471 JQ948802 JQ949132 JQ949462 JQ949792 JQ950122 CBS 129356, MSCL 850 Rhododendron sp. Latvia, Riga JQ948470 JQ948801 JQ949131 JQ949461 JQ949791 JQ950121 CBS 191.56 Salix sp. Germany JQ948461 JQ948792 JQ949122 JQ949452 JQ949782 JQ950112 CBS 192.56 Salix sp., tissue Germany JQ948462 JQ948793 JQ949123 JQ949453 JQ949783 JQ950113 CBS 607.94* Salix sp., leaf, spot Netherlands JQ948460 JQ948791 JQ949121 JQ949451 JQ949781 JQ950111 CBS 128558, ICMP 12956, PRJ 1117.4 Salix sp., twig, lesion New Zealand JQ948463 JQ948794 JQ949124 JQ949454 JQ949784 JQ950114 CBS 159.27 Salix sp. UK JQ948479 JQ948810 JQ949140 JQ949470 JQ949800 JQ950130 CBS 115.14 Solanum lycopersicum, fruit Germany JQ948477 JQ948808 JQ949138 JQ949468 JQ949798 JQ950128 CBS 239.49 Unknown Unknown JQ948469 JQ948800 JQ949130 JQ949460 JQ949790 JQ950120 C. scovillei CBS 126529, PD 94/921-3, BBA 70349* Capsicum sp. Indonesia JQ948267 JQ948597 JQ948928 JQ949258 JQ949588 JQ949918 CBS 126530, PD 94/921-4 Capsicum sp. Indonesia JQ948268 JQ948598 JQ948929 JQ949259 JQ949589 JQ949919 CBS 120708, HKUCC 10893, Mj6 Capsicum annuum Thailand JQ948269 JQ948599 JQ948930 JQ949260 JQ949590 JQ949920 C. simmondsii CBS 294.67, DPI 13483 Carica papaya Australia JQ948277 JQ948607 JQ948938 JQ949268 JQ949598 JQ949928 CBS 122122, BRIP 28519* Carica papaya, fruit Australia JQ948276 JQ948606 JQ948937 JQ949267 JQ949597 JQ949927 CBS 126524, PD 89/582 Cyclamen sp., deformations and brown staining of stem Netherlands JQ948281 JQ948611 JQ948942 JQ949272 JQ949602 JQ949932 tip CBS 295.67, DPI 16518 Fragaria sp., fruit Australia JQ948278 JQ948608 JQ948939 JQ949269 JQ949599 JQ949929 IMI 345034, CPC 18884 Fragaria × ananassa, fruit Australia JQ948279 JQ948609 JQ948940 JQ949270 JQ949600 JQ949930 IMI 354381, CPC 18923 Fragaria × ananassa, fruit rot Australia JQ948280 JQ948610 JQ948941 JQ949271 JQ949601 JQ949931 IMI 313840, CPC 18875 Mangifera indica Australia JQ948284 JQ948614 JQ948945 JQ949275 JQ949605 JQ949935 CBS 111531, STE-U 2090 Protea cynaroides USA JQ948282 JQ948612 JQ948943 JQ949273 JQ949603 JQ949933 CBS 114494, STE-U 2964, STE-U 2088 Protea cynaroides USA JQ948283 JQ948613 JQ948944 JQ949274 JQ949604 JQ949934 C. sloanei IMI 364297, CPC 18929* Theobroma cacao, leaf Malaysia JQ948287 JQ948617 JQ948948 JQ949278 JQ949608 JQ949938 C. tamarilloi CBS 129814, T.A.6* Solanum betaceum, fruit, anthracnose Colombia JQ948184 JQ948514 JQ948845 JQ949175 JQ949505 JQ949835 CBS 129811, T.A.3 Solanum betaceum, fruit, anthracnose Colombia JQ948185 JQ948515 JQ948846 JQ949176 JQ949506 JQ949836 CBS 129813, T.A.5 Solanum betaceum, fruit, anthracnose Colombia JQ948187 JQ948517 JQ948848 JQ949178 JQ949508 JQ949838 CBS 129812, T.A.4 Solanum betaceum, fruit, anthracnose Colombia JQ948186 JQ948516 JQ948847 JQ949177 JQ949507 JQ949837 CBS 129954, Tom-21, RB017 Solanum betaceum Colombia JQ948188 JQ948518 JQ948849 JQ949179 JQ949509 JQ949839 CBS 129955, Tom-12, RB018 Solanum betaceum Colombia JQ948189 JQ948519 JQ948850 JQ949180 JQ949510 JQ949840 CBS 129956, Tom-9, RB112 Solanum betaceum Colombia JQ948190 JQ948520 JQ948851 JQ949181 JQ949511 JQ949841 Damm et al . 3–8.5 µm diam. Setae very few, medium brown, basal cell pale, smooth-walled, 1–2-septate, 45–85 µm long, base cylindrical, 3–4 µm diam, tip ± acute. Conidiophores hyaline to pale brown, smooth-walled, septate, branched, to 30 µm long. Conidiogenous cells hyaline, smooth-walled, cylindrical to ampulliform, 9–20 × 3.5– 5 µm, opening 1–1.5 µm diam, collarette 0.5–1 µm long, periclinal thickening distinct. Conidia hyaline, smooth-walled, aseptate, straight, cylindrical with one end round and one end slightly acute, (12.5–)15–18.5(–20.5) × (4–)4.5–5 µm, mean ± SD = 16.8 ± 1.7 × 4.7 ± 0.3 µm, L/W ratio = 3.6. Culture characteristics: Colonies on SNA flat with entire margin, hyaline to pale cinnamon, on filter paper, Anthriscus stem and medium partly covered with short floccose-felty white aerial mycelium and salmon, orange to olivaceous grey acervuli, reverse same colours, growth rate 20–21.5 mm in 7 d (32–33 mm in 10 d). Colonies on OA flat with entire margin; surface buff to honey, almost entirely covered with floccose-felty white to pale olivaceous grey aerial mycelium and olivaceous grey to salmon acervuli, reverse buff, pale olivaceous grey, grey olivaceous to iron-grey, growth rate 17.5–20 mm in 7 d (27.5–30 mm in 10 d). Conidia in mass salmon to orange. Material examined: New Zealand, Nelson, from bitter rot on fruit of Malus domestica, 1 Aug. 1987, P.R. Johnston, (CBS H-20725 holotype, culture ex-type CBS 128530 = ICMP 12921 = PRJ 1199.3). Notes: Bitter rot has been considered an economically signficant disease of apple for many years (Schrenk & Spaulding 1903b), and was initially ascribed to Gloeosporium fructigenum (Berkeley 1856). However, Berkeley’s type was examined by Vinnere (2004) and found to have falcate conidia, thus excluding it from the C. acutatum species complex. Currently, bitter rot is known to be caused primarily by fungi from the C. gloeosporioides species complex (González et al. 2006); that study focused on strains from the USA and Brazil, and we do not know whether their C. acutatum s. lat. strains are conspecific with C. acerbum. Those of Lee et al. (2007) from Korea are referable to C. acutatum clades 2 (C. nymphaeae and related species) and 3 (C. fioriniae), so the host certainly appears susceptible to a wide range of Colletotrichum pathogens. The ex-type strain of C. acerbum is the only strain we included in our study that represents C. acutatum group B as delineated by Lardner et al. (1999). It may be common on Malus in New Zealand, but Lardner et al. (1999) found that more strains from fruit rot of apple, as well as from feijoa and fig, belonged to group C and had similar RAPD banding patterns (Lardner et al. 1999). It is possible that their group C includes more than one species. The GAPDH sequence of strain PJ9 (= PRJ 819 in Lardner et al. 1999), which was isolated from apple in New Zealand and was sequenced by Guerber et al. (2003), is identical to that of CBS 128530, the ex- type strain of C. acerbum. Colletotrichum acerbum is distinguishable from C. rhombiforme and all other species in all gene sequences analysed except for CHS-1, and is most effectively distinguished with TUB2 and ITS. In morphological terms its conidia are longer and the appressoria are shorter and wider than those of C. rhombiforme. Based on our studies and blastn searches in GenBank, it seems that C. acerbum could be endemic to New Zealand. The closest match based on TUB2 sequence that we could find (with 99 % identity, 5 bp differences) was AJ748624 from isolate PT250 (= CBS 129953), derived from olive in Portugal (Talhinhas et al. 2005), which we assign to C. rhombiforme. The closest matches for the ITS Table 1. (Continued). Species Accession No. Host/Substrate Country GenBank No. ITS GAPDH CHS-1 HIS3 ACT TUB2 C. walleri CBS 125472, BMT(HL)19* Coffea sp., leaf tissue Vietnam JQ948275 JQ948605 JQ948936 JQ949266 JQ949596 JQ949926 Colletotrichum sp. CBS 129820, G5 Passiflora edulis , fruit, scab Colombia JQ948183 JQ948513 JQ948844 JQ949174 JQ949504 JQ949834 CBS 129821, G6 Passiflora edulis , fruit, scab Colombia JQ948182 JQ948512 JQ948843 JQ949173 JQ949503 JQ949833 CBS 129823, G8 Passiflora edulis , leaf, anthracnose Colombia JQ948192 JQ948522 JQ948853 JQ949183 JQ949513 JQ949843 IMI 384185, CPC 18937 Caryocar brasiliense Brazil JQ948191 JQ948521 JQ948852 JQ949182 JQ949512 JQ949842 CBS 101611 Fern Costa Rica JQ948196 JQ948526 JQ948857 JQ949187 JQ949517 JQ949847 CBS 129810, T.A.2 Solanum betaceum, fruit, anthracnose Colombia JQ948179 JQ948509 JQ948840 JQ949170 JQ949500 JQ949830 CBS: Culture collection of the Centraalbureau voor Schimmelcultures, Fungal Biodiversity Centre, Utrecht, The Netherlands; IMI: Culture collection of CABI Europe UK Centre, Egham, UK; MAFF: MAFF Genebank Project, Ministry of Agriculture, Forestry and Fisheries, Tsukuba, Japan; BRIP: Plant Pathology Herbarium, Department of Employment, Economic, Development and Innovation, Queensland, Australia; ICMP: International Collection of Microorganisms from Plants, Auckland, New Zealand; STE-U: Culture collection of the Department of Plant Pathology, University of Stellenbosch, South Africa; HKUCC: The University of Hong Kong Culture Collection, Hong Kong, China; PD: Plantenziektenkundige Dienst Wageningen, Nederland; * ex-holotype or ex-epitype cultures. The CotriC ollet hum aCtum a ut species complex Fig. 3. Colletotrichum acutatum (from ex-epitype strain CBS 112996). A–B. Conidiomata. C–I. Conidiophores. J–Q. Appressoria. R–S. Conidia. A, C–D, R. from Anthriscus stem. B, E–Q, S. from SNA. A–B. DM, C–S. DIC, Scale bars: A = 200 µm, B = 100 µm, C = 10 µm. Scale bar of C applies to C–S. sequence of C. acerbum (with 99 % identity, 3 bp differences), were to obovate, entire edge, sometimes undulate, (4–)5.5–9(–13) × (3–)4–6.5(–9.5) µm, mean ± SD = 7.3 ± 2.0 × 5.4 ± 1.2 µm, L/W with the ITS of C. phormii and C. salicis, which are all members of the same major clade. ratio = 1.3. Asexual morph on Anthriscus stem. Conidiomata acervular, conidiophores formed on a cushion of pale brown angular cells, Colletotrichum acutatum J.H. Simmonds, Queensland J. 2–7 µm diam. Setae not observed. Conidiophores hyaline, septate, agric. Anim. Sci. 25: 178A. 1968. Fig. 3. branched, smooth-walled, to 50 µm long. Conidiogenous cells ≡ Colletotrichum acutatum J.H. Simmonds, Queensland J. agric. Anim. Sci. 22: 458. 1965, nom. inval., Art. 37.1. hyaline, smooth-walled, cylindrical, 9–18 × 3–3.5 µm, opening 1–1.5 µm diam, collarette distinct, 0.5 µm long, periclinal thickening Sexual morph not observed. Asexual morph on SNA. Vegetative conspicuous. Conidia hyaline, smooth-walled, aseptate, straight, hyphae 1–5.5 µm diam, hyaline, smooth-walled, septate, fusiform to cylindrical, apex and base uniformly acute, (8.5–)12– branched. Chlamydospores not observed. Conidiomata absent, 16.5(–17.5) × (3–)3.5–4.5(–5) µm, mean ± SD = 14.3 ± 2.1 × 4.1 conidiophores formed directly on vegetative hyphae. Setae not ± 0.4 µm, L/W ratio = 3.5, conidia of strains CBS 112759, CBS observed. Conidiophores hyaline, smooth-walled, mostly simple, 370.73 and CBS 112979 differ in being cylindrical to clavate and in sometimes septate and branched, to 25 µm long. Conidiogenous having one round and one acute end, conidia of strain CBS 370.73 cells hyaline, smooth-walled, cylindrical to slightly inflated, often not are smaller, measuring (5–)6.5–11(–12.5) × (2–)2.5–3.5(–4.5) µm, clearly separated from subtending hyphae by a septum, 3.5–20 × mean ± SD = 8.8 ± 2.1 × 3.2 ± 0.5 µm, L/W ratio = 2.7. 2–3.5 µm, opening 1–1.5 µm diam, collarette distinct, 1–1.5 µm long, periclinal thickening conspicuous. Conidia hyaline, smooth- Culture characteristics: Colonies on SNA flat with entire margin, walled, aseptate, straight, cylindrical to fusiform with both ends hyaline with white aerial mycelium on Anthriscus stem and filter acute, (7.5–)11–14.5(–19) × 3.5–4(–4.5) µm, mean ± SD = 12.6 ± paper, reverse of filter paper partly pale ochreous; growth rate 1.8 × 3.9 ± 0.3 µm, L/W ratio = 3.2, conidia of strains CBS 112759, 21–24.5 mm in 7 d (30–36.5 mm in 10 d). Colonies on OA flat CBS 112979 and CBS 979.69 differ in being cylindrical to clavate with entire margin; surface buff, rosy buff, salmon to peach due to and having one round and one acute end, e.g., conidia of strain sporulation, with olivaceous sectors in the centre, partly covered by CBS 112759 are smaller, measuring (6.5–)8.5–12(–13) × (2.5–)3–4 white floccose aerial mycelium, reverse rosy buff to flesh, smoke µm, mean ± SD = 10.3 ± 1.9 × 3.4 ± 0.5 µm, L/W ratio = 3.1. grey to olivaceous grey in the centre; growth rate 20–25 mm in 7 d Appressoria solitary, medium brown, smooth-walled, ellipsoidal (31–33.5 mm in 10 d). Conidia in mass saffron to orange. www.studiesinmycology.org 55 Damm et al . Material examined: Australia, Queensland, Ormiston, Redlands Research Station, International Code of Nomenclature for Algae, Fungi and Plants from fruit rot of Carica papaya, 1 Oct. 1965, J.H. Simmonds (IMI 117617 = QDPI&F (ICN) as they are based on fungus/plant interactions rather than plant disease log book no. 16741B1 holotype, BRIP 4693, isotype of C. acutatum); single species, and formal ICN-compliant taxa cannot use formae Queensland, Brisbane, Ormiston, from fruit rot of Carica papaya, 5 Jul. 1965, J.H. speciales as basionyms for new combinations. Simmonds (deposited in CBS collection 2002 by P.W. Crous), (CBS-H 20723, epitype here designated, culture ex-epitype (and ex-paratype IMI 117620 of C. Colletotrichum acutatum f. sp. pinea (Dingley & Gilmour 1972) acutatum) CBS 112996 = ATCC 56816 = ICMP 1783 = STE-U 5292); New South was described for a malady of pines called terminal crook disease, Wales; Mount Annari, from Grevillea sp., 12 Oct. 1999, P.W. Crous, culture CBS with the fungus apparently causing malformation of growing tips. 111993 = STE-U 3037; Western Australia, Wanneroo, from Fragaria × ananassa, We have examined authentic cultures derived from Dingley & 8 Aug. 1988, R.M. Floyd, culture CBS 127602 = BRIP 52691a = WAC 5416; from seedling of Pinus radiata, collection date and collector unknown (isolated Apr. 1971, Gilmour’s work, which were also used by von Arx. Most of these deposited in CBS collection Sep. 1972 from Forest Research Institut Rotorua as C. cannot be distinguished in morphological or molecular terms acutatum f. sp. pineum), culture CBS 797.72. South Africa, from Leucadendron sp. from C. acutatum s. str., but strain CBS 436.77 (from Chile, not cv. Safari Sunset, collection date unknown, J.E. Taylor, culture CBS 112990 = STE-U from New Zealand as are the authentic cultures of C. acutatum 4448; from Aspalathus linearis, collection date unknown, S. Lamprecht, culture CBS 129915 = CPC 15512; Southern Cape, Kruisfontein, from Pinus radiata, collection f. sp. pinea), belongs to a quite different species outside of the C. date unknown, Lundquist, culture CBS 110735 = STE-U 163; Kruisfontein, from acutatum species complex (see C. pseudoacutatum). CBS 797.72 Pinus radiata, collection date unknown, Lundquist, culture CBS 112979 = STE-U appears to show evidence of hybrid origin and is not included in the 160; Eastern Cape, Langkloof, from Hakea sericea, collector unknown (deposited molecular analyses (see below). in CBS collection 2002 by P.W. Crous), culture CBS 112759 = STE-U 4470; from Hakea sericea, collection date unknown (deposited in CBS collection 2002 by P.W. Colletotrichum acutatum f. sp. hakeae (Lubbe et al. 2004) was Crous), K. Lubbe, culture CBS 112761 = STE-U 4461. New Zealand, Tokoroa, from introduced for an apparently strongly host-specific set of strains, Pinus radiata, unknown collection date and collector (deposited in CBS collection one of which was being used as a potential biological control Jan 1973 by J.M. Dingley), culture CBS 370.73 = NRCC 10088; Kenya, Yala, agent (Morris 1982, Gordon & Fourie 2011), but we have not from berry of Coffea arabica, collection date unknown, D.M. Masaba, culture IMI 319423 = CPC 18877; from Coffea arabica, unknown collection date and collector found any morphological differences and there are few sequence- (deposited in CBS collection Nov. 1969 by H. Vermeulen), culture CBS 979.69. based differences (1 bp difference in ITS, 2 bp differences in HIS3) between these and other C. acutatum s. str. strains. We Notes: Colletotrichum acutatum was described by Simmonds therefore do not feel confident to recognise this forma specialis (1965) from a range of different hosts from Australia. No type on that basis as a segregate species. Colletotrichum acutatum f. was designated, and the name was validated three years later sp. chromogenum was described by Baxter et al. (1983), based (Simmonds 1968) with designation of a holotype, IMI 117617 from on strains from olive referred to as Gloeosporium fructigenum f. Carica papaya, and paratypes from C. papaya (IMI 117618 - IMI sp. chromogenum by Gorter (1962), for strains producing pink to 117621), Capsicum frutescens (IMI 117622), and Delphinium sp. purple pigments in culture. Such pigment production is common (IMI 117623). throughout the C. acutatum complex (e.g. Polashock et al. 2009) Vinnere et al. (2002) sequenced the ITS region of the holotype and is especially prominent in C. acutatum s. str. (as their clade specimen (AF411700) and one paratype specimen IMI 117619 A5) according to Sreenivasaprasad & Talhinhas (2005). In fact the (AF411701) and found morphological and cultural differences only strain from olive in South Africa included in this study (CBS between Simmonds’s six holotype/paratype specimens of C. 127589) belongs to this species and could represent C. acutatum acutatum. There is no living ex-holotype culture available, but two f. sp. chromogenum. But whatever the case, the rank used is ex-paratype strains, one from Carica papaya (IMI 117620 = QDPI&F inappropriate for this purpose. plant disease log book no. 16633D = ATCC 56816 = CBS 112996 A variety of C. acutatum, described on Fiorinia externa (a scale = STE-U 5292) and one from Capsicum frutescens (IMI 117622 insect), C. acutatum var. fioriniae (Marcelino et al. 2008), was = QDPI&F plant disease log book no. 11711A = CBS 292.67, see recognised as the separate species C. fioriniae by Shivas & Tan C. brisbanense) and an ex-topotype strain from Carica papaya (2009) and is included below in this study. (QDPI&F plant disease log book no. 13483-0 = CBS 294.67, see A sexual morph was described for C. acutatum (Guerber & C. simmondsii) do exist in a living state. Correll 1997, 2001), based on mating compatible strains in the Than et al. (2008b) epitypified C. acutatum with a strain from laboratory. The cross designated as type of Glomerella acutata Carica papaya from the region in which the species was first was based on two cultures, ATCC 56816 and ATCC MYA-662. The collected (BRIP 28519 = CBS 122122). Not only was this action first of these is derived from one of Simmonds’ original Queensland inadvisable bearing in mind that living cultures from two paratypes collections from papaya, IMI 117620 (here designated as epitype still exist, it was regrettable as it was subsequently discovered of C. acutatum). There is ongoing confusion regarding the that their epitype was not conspecific with the type. Following provenance of this strain, however; Guerber & Correll (2001) and an ITS and TUB2 analysis of the clade, Shivas & Tan (2009) Than et al. (2008b) wrongly equated ATCC 56816 with IMI 117617, described C. acutatum sensu Than et al. (2008b) as a separate the holotype, and that congruence is recorded as such in the ATCC species, C. simmondsii. They did not designate a further epitype catalogue. The second strain ATCC MYA-662 was isolated from for C. acutatum, but bearing in mind that only the ITS region of apple in Louisiana, USA (Guerber & Correll 2001), and is here the holotype was sequenced, we feel that it is important to fix the assigned to C. fioriniae in clade 3. Fertile sexual morphs were also application of that species name with an appropriate epitype that produced by Guerber & Correll (2001) and Guerber et al. (2003) can be subject to multigene analysis. This has been done above, by mating a series of different strains, including crosses between with one of Simmond’s original paratypes chosen for this purpose. parents that are both assigned to C. fioriniae. None of the strains Colletotrichum acutatum s. str. causes diseases of a wide range tested was self-fertile. of unrelated plants, some of which are economically significant, The holotype of Glomerella acutata is therefore an interspecific including papaya (Carica papaya), strawberry (Fragaria × hybrid between C. acutatum and C. fioriniae. This might be construed ananassa), pine (Pinus spp.), Hakea spp. and rooibos (Aspalathus as strong evidence that these two taxa constitute a single biological linearis). Two of these are associated with recognition of formae species, and therefore that the species concepts used in this paper speciales. These are not accepted as a taxonomic rank in the are much too narrow. However, the parent strains of the holotype 56 The CotriC ollet hum aCtum a ut species complex originate from highly distant populations in geographical terms, and species in the C. acutatum species complex is highly variable and there are instances in other fungal groups (e.g. Neurospora) where overlapping. There is no strain from papaya in Brazil included in this non-sympatric populations lose post-mating reproductive isolation study, and there is no report of C. acutatum s. lat. from Brazil listed barriers (Turner et al. 2010, 2011). Further research on population in Farr & Rossman (2012). We have tried to draw a reasonable structures and mating-type barriers would be instructive. balance between respect for the rules of priority and the need for Colletotrichum acutatum has subsequently been reported to nomenclatural stability, and in this case we feel that Simmonds’ produce a sexual morph in nature, on Vaccinium corymbosum name should be conserved if such a synonymy is established. (highbush blueberry) in Norway (Talgø et al. 2007). Sequence- Colletotrichum acutatum is separated from other species based identification was apparently not carried out and so the by all genes. Closest matches in a blastn search with the TUB2 identity of this population remains uncertain, however the blueberry sequence of strain CBS 112996, with 100 % identity, were pathogen is usually C. fioriniae , which has a known sexual morph GU183307–GU183309 and GU183311–GU183314, from Boronia, (Marcelino et al. 2008). Its origin is also unknown; the crop is Anemone, Fragaria, Pistacia, Anemone, Olea, Ranunculus and not native to Norway and the fungus may have been introduced Mangifera in Australia (Shivas & Tan 2009), FJ788419 from from the USA along with planting material. The Glomerella sexual Simmonds’ specimen 16633D from Carica papaya in Australia morph described from Acer platanoides in Massachusetts, USA is (Weir & Johnston, unpubl. data), AY376546–AY376549 and homothallic (LoBuglio & Pfister 2008), and belongs to C. salicis, not AY376558–AY376568 from Pinus, Leucadendron and Carica C. acutatum s. str. Two strains from this research are included in (STE-U 5292 = CBS 112996) and Hakea (Lubbe et al. 2004), our study. Further discussion may be found in Cannon et al. (2012, AJ748627 and AJ748630 from Phlox and Statice (Talhinhas et al. this issue). 2005), HE573032 from Arbutus unedo (strawberry tree) (Polizzi et A further twist in the story may be provided by CBS 797.72; al. 2011) and with 99 % identity (1 or 2 bp difference) AY376550 this is one of the strains on which C. acutatum f. sp. pinea was and AY376545 from Protea and Leucospermum (Lubbe et al. 2004) based (Dingley & Gilmour 1972). Sequences of three of the six and AJ748618 from Olea (Talhinhas et al. 2005). Colletotrichum genes sampled (ACT, HIS3 and CHS-1) indicate affinities with C. acutatum s. str. can therefore be assumed to be a widespread acutatum (clade 4) but the other three (ITS, GAPDH and TUB2) species that causes disease symptoms on a wide range of plants. suggest that the strain belongs to C. fioriniae (clade 3). This was confirmed by repeating sequencing from a new subculture from Colletotrichum australe Damm, P.F. Cannon & Crous, sp. the CBS collection and after re-singlesporing of one of the single nov. MycoBank MB800495. Fig. 4. spore isolates. This too may be of hybrid origin. The phylogeny by Guerber et al. (2003) includes strains from Pinus in New Zealand in Etymology: derived from the localities of collection in the Southern both species (as groups J4 and C1). We do not know if they should Hemisphere. be assigned to C. fioriniae, or are hybrids as well. The widespread geographical range and economic importance Sexual morph not observed. Asexual morph on SNA. Vegetative of C. acutatum makes it likely that an earlier name exists for the hyphae 1–5 µm diam, hyaline, smooth-walled, septate, branched. species, probably listed as a synonym of C. gloeosporioides by von Chlamydospores not observed. Conidiomata absent, conidiophores Arx (1957). Walker et al. (1991) noted that C. xanthii (Halsted 1893) and setae formed directly on hyphae. Setae rarely observed, pale to is such a candidate based on the fusiform shape of conidia found medium brown, smooth-walled to finely verruculose, 1–3-septate, on the type material, but no authentic cultures exist and no other 30–90 µm long, base cylindrical to conical, 3.5–5.5 µm diam, strain from Xanthium with fusiform conidia was available to us. It tip ± roundish and bent and function as a conidiogenous locus. is therefore impossible to determine whether this species provides Conidiophores hyaline to pale brown, smooth-walled, simple or an earlier name for C. acutatum s. str., for another species within septate and branched, to 30 µm long. Conidiogenous cells hyaline the C. acutatum complex or belongs to the C. acutatum species to pale brown, smooth-walled, conical to ampulliform, 4.5–15 complex at all (see C. pseudoacutatum). × 2.5–5.5 µm, opening 0.5–1 µm diam, collarette 0.5–1.5 µm Apart from C. acutatum and C. simmondsii, there have been long, periclinal thickening visible. Conidia hyaline, smooth-walled, other Colletotrichum and Gloeosporium species described on aseptate, become septate with age, straight, cylindrical, with one Carica papaya, all from Brazil. Conidia of C. papayae Henn. end round and one end slightly acute to truncate, (10–)14.5–19.5(– described from branches and petioles of papaya in Sao Paulo, 25) × (3.5–)4–5(–6) µm, mean ± SD = 17.0 ± 2.4 × 4.4 ± 0.5 µm, are larger and differ in shape from C. acutatum s. str.; they are L/W ratio = 3.9. Appressoria single or in small groups, medium cylindrical, straight to curved, hyaline, and measure 12–20 × 5–7 brown, smooth-walled, outline mostly subglobose to elliptical, µm (Saccardo et al. 1931), while those of C. acutatum measure on sometimes clavate, the edge entire or undulate, sometimes slightly average 8.8–15.5 × 3.2–4.5 µm, depending on strain and medium. lobate, (5–)6–11(–14) × (4–)4.5–7(–8.5) µm, mean ± SD = 8.5 ± Gloeosporium papayae Henn., described from stems of papaya 2.6 × 5.8 ± 1.1 µm, L/W ratio = 1.5. in Uberaba, Minas Gerais, forms cylindrical-oblong to subclavate, Asexual morph on Anthriscus stem. Conidiomata acervular obtuse, straight, hyaline to pale yellowish conidia that measure where present, conidiophores and setae formed directly on hyphae 11–14 × 5–6 µm (Hennings 1895); conidia of C. acutatum are or on a cushion of pale brown angular cells. Setae pale to medium hyaline and broader. A presumed isotype in K(M) of G. papayae, brown, smooth-walled to finely verruculose, 2–7-septate, 40–130 “E. Ule n. 1947”, collected in June 1892, is actually a species of Phomopsis. Gloeosporium fructus-caricae Henn. forms conidia µm long, base cylindrical to conical, 3–5 µm diam, tip broadly that overlap in size with those of C. acutatum, however their shape rounded to somewhat acute, and may function as a conidiogenous is described as oblong-cylindrical with both ends rounded, while locus. Conidiophores hyaline to pale brown, smooth-walled, septate, little branched, to 50 µm long. Conidiogenous cells conidia of C. acutatum usually have both ends acute. Even if the hyaline to pale brown, smooth-walled, cylindrical to ampulliform, description matches completely with that of C. acutatum we could 8–19 × 3–5 µm, opening 1–2.5 µm diam, collarette 0.5–1 µm not be sure they are the same species; the morphology of most www.studiesinmycology.org 57 Damm et al . Fig. 4. Colletotrichum australe (from ex-holotype strain CBS 116478). A–B. Conidiomata. C. Seta. D–G. Conidiophores. H. Tip of seta. I. Basis of seta. J–K. Conidiophores. L–Q. Appressoria. R–S. Conidia. A, C–G, R. from Anthriscus stem. B, H–Q, S. from SNA. A–B. DM, C–S. DIC, Scale bars: A = 100 µm, F = 10 µm. Scale bar of A applies to A–B. Scale bar of F applies to C–S. long, periclinal thickening distinct. Conidia hyaline, smooth-walled, while those of C. australe are cylindrical. Additionally, appressoria aseptate, straight, cylindrical, sometimes slightly constricted in the of C. australe are shorter than those of C. phormii. Conidia of C. rhombiforme are shorter, while those of C. kinghornii are narrower. middle, with one end round and one end slightly acute to truncate, It is possible that Fusarium hakeae (Hennings 1898), described (16–)17–20(–22) × (4–)4.5–5(–5.5) µm, mean ± SD = 18.6 ± 1.6 from leaves of Hakea saligna from the Botanic Garden in Berlin, × 4.7 ± 0.4 µm, L/W ratio = 4.0, conidia of strain CBS 131325 Germany, is the same species as C. australe. The description is smaller, measuring (13.5–)15–17.5(–18) × (3.5–)4–5(–5.5) µm, short but largely corresponds with our species, but bearing in mind mean ± SD = 16.3 ± 1.1 × 4.4 ± 0.4 µm, L/W ratio = 3.7. that most Colletotrichum species show a lack of host specificity, there is no strong reason to equate the two taxa in the absence Culture characteristics: Colonies on SNA flat with entire margin, of sequenceable material of F. hakeae. Wollenweber (1916) hyaline to honey, filter paper straw to pale olivaceous grey, aerial transferred F. hakeae to Gloeosporium, and von Arx (1957, mycelium lacking, reverse same colours, growth rate 16–18 mm in 1970) included the name as a synonym of C. gloeosporioides. 7 d (28.5–30 mm in 10 d). Colonies on OA flat with entire margin; Bondarzeva-Monteverde et al. (1936) described a separate fungus surface pale luteous to amber, in the centre covered with floccose as Gloeosporium hakeae from greenhouses in St Petersburg; this white aerial mycelium, reverse pale luteous to salmon, growth rate was reported to have straight to curved conidia and is unlikely to 16–20 mm in 7 d (25–29.5 mm in 10 d). Conidia in mass salmon. be a synonym of Hennings’ fungus. Lubbe et al. (2004) published C.acutatum f. sp. hakeae for isolates that caused a distinctive Material examined: South Africa, Stellenbosch, university campus, from disease of Hakea in South Africa; these have shorter conidia than Trachycarpus fortunei, 2 Jan. 1998, J.E. Taylor, (CBS-H 20721 holotype, culture ex-type CBS 116478 = HKUCC2616). Australia, Western Australia, Alcoa, from those of C. australe and group in C. acutatum s. str. Colletotrichum Hakea sp., 12 Jul. 2011, W. Gams, culture CBS 131325. acutatum has been reported from Trachycarpus fortunei in Australia and Switzerland by Taylor & Hyde (2003); we do not know whether Notes: Colletotrichum australe belongs to the clade that includes these collections represent further records of C. australe. C. phormii, C. kinghornii, C. rhombiforme and C. acerbum. Setae Colletotrichum australe is separated from other species by all are better developed (in cultures on Anthriscus stem) and conidia gene sequences surveyed except for CHS-1, which is the same are larger than in most other species in the C. acutatum species as that of C. phormii, and most effectively separated by HIS3. The complex. Only C. phormii forms larger conidia, which are fusiform, closest match in a blastn search with the TUB2 sequence of strain 58 The CotriC ollet hum aCtum a ut species complex Fig. 5. Colletotrichum brisbanense (from ex-holotype strain CBS 292.67). A–B. Conidiomata. C–H. Conidiophores. I–N. Appressoria. O–P. Conidia. A, C–E, O. from Anthriscus stem. B, F–N, P. from SNA. A–B. DM, C–P. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–P. CBS 116478 (with 98 % identity, 8 and 9 bp differences) were µm long. Conidiogenous cells hyaline, smooth-walled, cylindrical to isolates PCF 459 (EU635504) from strawberry in Belgium (Debode slightly inflated, sometimes lacking a basal septum and continuous et al. 2009) and PT250 (= CBS 129953, see C. rhombiforme), and with the conidiophore, sometimes proliferating and extending to form AJ748624 from olive, Portugal (Talhinhas et al. 2005). We do not a new conidiogenous locus, discrete phialides measure 8.5–21 × 2.5– think that any of these sequences are derived from strains that 4 µm, opening 1–1.5 µm diam, collarette 1–1.5 µm long, periclinal are conspecific with C. australe. With the GAPDH sequence there thickening distinct. Conidia hyaline, smooth-walled, aseptate, was no closer match than 87 % identity. The closest matches with straight, cylindrical with both ends slightly acute or one end round ITS sequence, with 99 % sequence identity, include Glomerella and one end slightly acute, (12–)12–17.5(–25) × (3–) 3.5–4(–5) µm, cingulata BBA 70991 from Salix (AJ301952, Nirenberg et al. 2002) mean ± SD = 14.8 ± 2.8 × 3.8 ± 0.5 µm, L/W ratio = 3.9. Appressoria and Glomerella sp. strain MP3 from Acer platanoides (EU622052, single or in loose groups, pale brown, smooth-walled, mostly clavate, LoBuglio & Pfister 2008), which are both likely to be C. salicis. Other the edge entire to undulate, (5–)7.5–14.5(–18) × (2.5–)3.5–5(–6) µm, strains with 99 % ITS sequence homology include that deposited mean ± SD = 11.1 ± 3.4 × 4.3 ± 0.9 µm, L/W ratio = 2.6. as Fusarium phormii strain CBS 198.35 (DQ286144, Farr et al. Asexual morph on Anthriscus stem. Conidiomata possibly 2006) which we assign to C. kinghornii, and Ga. acutata PT715 acervular, but no basal cells observed. Setae not observed. from Olea europaea in Portugal (AM991135, Talhinhas et al. 2009). Conidiophores hyaline to pale brown, smooth-walled, septate, branched, to 30 µm long. Conidiogenous cells hyaline, smooth- Colletotrichum brisbanense Damm, P.F. Cannon & Crous, walled, cylindrical to ampulliform, sometimes proliferating and extending to form a new conidiogenous locus, sometimes sp. nov. MycoBank MB800497. Fig. 5. polyphialidic, 8.5–23 × 2.5–4.5 µm, opening 1–2 µm diam, Etymology: Named after Brisbane, the city in Queensland, Australia collarette 0.5–1 µm long, periclinal thickening distinct. Conidia where the species was collected. hyaline, smooth-walled, aseptate, straight, cylindrical with both ends slightly acute, (9.5–)12–15(–17) × (3–)3.5–4 µm, mean ± SD Sexual morph not observed. Asexual morph on SNA. Vegetative = 13.5 ± 1.4 × 3.9 ± 0.3 µm, L/W ratio = 3.5. hyphae 1–8 µm diam, hyaline, smooth-walled, septate, branched. Chlamydospores not observed. Conidiomata not developed, Culture characteristics: Colonies on SNA flat with entire margin, conidiophores formed directly on hyphae. Setae not observed. hyaline to pale cinnamon, on filter paper partly pale saffron, agar Conidiophores hyaline, smooth-walled, septate, branched, to 30 medium partly covered with very short white aerial mycelium, www.studiesinmycology.org 59 Damm et al . Fig. 6. Colletotrichum chrysanthemi (from strain CBS 126518). A–B. Conidiomata. C–H. Conidiophores. I–N. Appressoria. O–P. Conidia. A, C–E, O. from Anthriscus stem. B, F–N, P. from SNA. A–B. DM, C–P. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–P. reverse same colours; growth rate 18–20 mm in 7 d (26–29 mm in same strain generated by Shivas & Tan (2009); next closest was DQ454064 from isolate S6 from Fragaria in Thailand with 99 % 10 d). Colonies on OA flat with entire margin; surface buff, rosy buff to pale saffron, covered with short white aerial mycelium, reverse identity (four differences; Sang et al. 2011). With the GAPDH sequence there was no match with more than 95 % identity. The ITS same colours; growth rate 17.5–18.5 mm in 7 d (27.5–28.5 mm in sequence of strain CBS 292.67 matched 100 % with GU183315, a 10 d). Conidia in mass salmon. sequence of the same isolate generated by Shivas & Tan (2009). Material examined: Australia, Queensland, Brisbane, Eight Mile Plains, from fruit rot of Capsicum annuum, 14 Jul. 1955, J.H. Simmonds, (IMI 117622 holotype of C. Colletotrichum chrysanthemi (Hori) Sawada, Rep. Govt brisbanense (also paratype of C. acutatum), CBS H-20801 isotype, culture ex-type Res. Inst. Dep. Agric., Formosa 85: 81. 1943. Fig. 6. CBS 292.67 = BRIP 4684). ≡ Gloeosporium chrysanthemi Hori, in Takimoto, Jour. Hort. Japan 36(9): 27. 1924. Notes: The type and only confirmed strain of C. brisbanense was cited as one of the paratype strains of C. acutatum by Simmonds Sexual morph not observed. Asexual morph on SNA (CBS 126518). (1968), and assigned to C. simmondsii by Shivas & Tan (2009). Vegetative hyphae 1.5–9 µm diam, hyaline, smooth-walled, septate, Conidia and appressoria of C. brisbanense are larger overall branched. Chlamydospores not observed. Conidiomata absent, than those of C. simmondsii as accepted in this treatment. The conidiophores formed directly on hyphae. Setae not observed. two species are easily separable using all sequence data except Conidiophores hyaline to pale brown, smooth-walled, septate and for ITS, and most effectively with TUB2 and GAPDH sequences. branched, to 55 µm long. Conidiogenous cells hyaline, smooth- There is only one bp difference in CHS-1 sequence between C. walled, cylindrical to ampulliform, 7–15 × 3–4.5 µm, opening 1.5–2 brisbanense and C. indonesiense. There is a further species in µm diam, collarette distinct, 0.5–1 µm long, periclinal thickening clade 2 associated with Capsicum annuum, C. scovillei, possibly distinct. Conidia hyaline, smooth-walled, aseptate, straight, a species endemic to Southeast Asia. Colletotrichum brisbanense broadly ellipsoidal to ovoid, with both ends acute, rarely clavate can be separated easily from C. scovillei based on appressorium to cylindrical with one round end one acute end, (6–)7–9.5(–12) × measurements, as well as by most DNA data. See C. scovillei for (3–)4–5.5(–6) µm, mean ± SD = 8.3 ± 1.3 × 4.8 ± 0.6 µm, L/W ratio further information. = 1.7, conidia from aerial mycelium shorter, measuring (3.5–)4.5– A blastn search with the TUB2 sequence of strain CBS 292.67 9(–15) × 3–5(–6.5) µm, mean ± SD = 6.7 ± 2.3 × 4.1 ± 0.8 µm, resulted in a 100 % match with GU183275, the sequence of the L/W ratio = 1.6. Appressoria single, medium brown, smooth-walled, 60 The CotriC ollet hum aCtum a ut species complex subglobose, elliptical or irregular in outline, with entire, undulate or There are few additional reports of Colletotrichum on lobate margin, (5–)5.5–9.5(–11.3) × (3–)4.5–6.5(–7.5) µm, mean ± Carthamus, Chrysanthemum and Calendula. Sette et al. (1999) SD = 7.5 ± 1.8 × 5.4 ± 1.1 µm, L/W ratio = 1.4. report C. acutatum on Carthamus tinctorius in Korea; the fungus Asexual morph on Anthriscus stem (CBS 126518). Conidiomata formed strongly fusiform conidia (see fig. 2 in Sette et al. 1999), acervular, conidiophores formed on a cushion of angular cells and formed setae at least occasionally on host plant and PDA 3–8.5 µm diam. Setae not observed. Conidiophores hyaline to medium. Vichova et al. (2011) found C. simmondsii on Carthamus pale brown, smooth-walled, septate, branched, to 40 µm long. tinctorius in the Czech Republic. There is another species that Conidiogenous cells hyaline, smooth-walled, cylindrical, 7–16.5 × was also described on Chrysanthemum and Dahlia in Portugal, C. 3.5–4.5 µm, opening 1–2 µm diam, collarette distinct, 0.5–1 µm dahliae; this species however forms larger conidia with round ends, long, periclinal thickening distinct. Conidia hyaline, smooth-walled, measuring 16–19 × 5.3–7 µm (Costa & Sousa da Câmara 1953). aseptate, straight, subglobose, broadly ellipsoidal to oval, with both Colletotrichum chrysanthemi is separated from other species ends ± acute, (3.5–)6.5–10.5(–13.5) × (3.5–)4–5(–5.5) µm, mean by all diagnostic genes applied in this study except for ITS, best ± SD = 8.5 ± 1.8 × 4.5 ± 0.5 µm, L/W ratio = 1.9. with TUB2, GAPDH and HIS3, and its very short acute-ended conidia differ from those of other species of the C. acutatum species Culture characteristics (CBS 126518): Colonies on SNA flat with complex. The ITS sequence of strain CBS 126518 matches with entire margin, hyaline to pale honey, on filter paper, Anthriscus 100 % identity with AB042306 and AB042307 from isolates from stem and medium partly covered with floccose white aerial Carthamus and Chrysanthemum in Japan (Moriwaki J, Tsukiboshi mycelium, reverse hyaline to pale honey; growth rate 14–17.5 T, Sato T, Uematsu S, unpubl. data), and also with AJ749675 from mm in 7 d (23.5–27.5 mm in 10 d). Colonies on OA umbonate with isolates PD85/694 (= CBS 126519), sequenced by Talhinhas et entire margin; surface rosy buff to pale purplish grey, covered with al. (2005) and AY376508 Ga. acutata strain STE-U 5303 (= CBS woolly to floccose-felty white to pale grey aerial mycelium, reverse 112989, C. laticiphilum) from Hevea (Lubbe et al. 2004). Closest rosy buff, olivaceous grey to iron grey; growth rate 16–17.5 mm in match in a blastn search with the TUB2 sequence of strain CBS 7 d (27.5–28 mm in 10 d). Conidia in mass pale salmon. 126518 with 100 % identity was AJ748632 from isolate PD85/694 (= CBS 126519, included in this study), sequenced by Talhinhas Material examined: Netherlands, Emmeloord, from twisted stem of Carthamus et al. (2005). Closest matches with the GAPDH sequence with 95 sp., unknown collection date and collector, culture CBS 126518 = PD 84/520; from % identity (12 and 13 differences) were HM038336 from isolate vascular discoloration of Glebionis carinata, collection date and collector unknown, culture CBS 126519 = PD 85/694. China, Hong Kong, from leaf spot of Glebionis MFU09 0628 from Mangifera indica and HM038337 from isolate coronaria, (deposited in IMI 1994 by Wan-chi Ko as culture no. 1964), culture IMI MFU09 0624 from Ziziphus mauritiana, both from Laos (Phoulivong et al. 2010). Notes: Gloeosporium chrysanthemi was described by Hori Colletotrichum cosmi Damm, P.F. Cannon & Crous, sp. as causing severe anthracnose disease in Chrysanthemum nov. MycoBank MB800498. Fig. 7. coronarium (= Glebionis coronaria) in the Fukuoka prefecture in Japan (Takimoto 1924) and transferred to Colletotrichum by Sawada Etymology: Named after the host plant, Cosmos. (1943). A pathogen of another Asteraceae plant, Carthamus tinctorius, was described in Japan by Fukui as Marssonia carthami Sexual morph not observed. Asexual morph on SNA. Vegetative (Fukui 1916, see also Tanaka 1917). The fungus was transferred to hyphae 1–7.5 µm diam, hyaline, sometimes pale brown, smooth- Gloeosporium by Hori & Hemmi. walled, septate, branched. Chlamydospores not observed. Uematsu et al. (2012) re-examined authentic specimens of C. Conidiomata not developed, conidiophores formed directly on chrysanthemi collected by Takimoto in 1919 and of G. carthami hyphae. Setae not observed. Conidiophores hyaline to pale brown, collected by Hemmi in 1915 and sequenced the ITS1 and TUB2 smooth-walled, septate, branched, to 40 µm long. Conidiogenous regions of these specimens as well as of isolates from Carthamus, cells hyaline, smooth-walled, cylindrical, sometimes slightly inflated, Chrysanthemum and Calendula species from Japan. The resulting 9–17 × 2.5–3.5 µm, opening 1–1.5 µm diam, collarette 1 µm sequences place the two species in the C. acutatum species long, periclinal thickening visible. Conidia hyaline, smooth-walled, complex. While all specimens and strains had almost identical aseptate, straight, cylindrical to clavate with both ends slightly acute ITS sequences, there were two groups in the TUB2 phylogeny, or one end round, (7–)13–18.5(–19.5) × (3–)3.5–4.5 µm, mean ± SD placing most of the Calendula isolates with the authentic specimen = 15.8 ± 2.5 × 4.0 ± 0.4 µm, L/W ratio = 4.0. Appressoria very few, of Gm. carthami and the Chrysanthemum and Carthamus isolates mostly single, pale to medium brown, smooth-walled, subglobose, as well as two Calendula isolates with the authentic specimen of elliptical or clavate, the edge entire, (5–)5.5–8(–11.5) × (4–)4.5–5.5 Gm. chrysanthemi, suggesting the two species to be separate. µm, mean ± SD = 6.8 ± 1.2 × 4.9 ± 0.4 µm, L/W ratio = 1.4. In spite of this, the authors regard C. chrysanthemi as synonym Asexual morph on Anthriscus stem. Conidiomata either not of the older species G. carthami. Based on TUB2 sequences of developed, conidiophores formed directly on hyphae, or acervular, the authentic specimens (AB696992, AB696993) and some of conidiophores formed on pale brown, angular, basal cells, 3–9 µm the strains from Calendula (AB688785, AB688787), Carthamus diam. Setae not observed. Conidiophores hyaline to pale brown, (AB688807, AB688811) and Chrysanthemum (AB688791) included smooth-walled, septate, branched, to 40 µm long. Conidiogenous in our alignment (not shown), isolates studied here group with the Japanese isolates from Carthamus and Chrysanthemum and the cells hyaline to pale brown, smooth-walled, cylindrical, 9–24 × authentic specimen of Gm. chrysanthemi, and we therefore treat 3–3.5 µm, opening 1–1.5 µm diam, collarette 1–1.5 µm long, them here as C. chrysanthemi . The TUB2 sequences of the periclinal thickening conspicuous. Conidia hyaline, smooth-walled, Calendula isolates and the authentic material of Gm. carthami aseptate, straight, cylindrical to fusiform with both ends ± acute, appear to belong to a different clade that is not included in our (12–)14–16.5(–18) × (3.5–)4–4.5 µm, mean ± SD = 15.3 ± 1.4 × 4.0 ± 0.3 µm, L/W ratio = 3.8. study. www.studiesinmycology.org 61 Damm et al . Fig. 7. Colletotrichum cosmi (from ex-holotype strain CBS 853.73). A–B. Conidiomata. C–H. Conidiophores. I–N. Appressoria. O–P. Conidia. A, C–E, O. from Anthriscus stem. B, F–N, P. from SNA. A–B. DM, C–P. DIC, Scale bars: A = 200 µm, B = 100 µm, C = 10 µm. Scale bar of C applies to C–P. Culture characteristics: Colonies on SNA flat with entire margin, Two other species are reported from Cosmos bipinnatus in India, C. hyaline, buff to pale honey, on filter paper partly pale olivaceous truncatum (as C. capsici) associated with seeds and causing seed grey, the medium, filter paper and Anthriscus stem partly covered and seedling rot (Srivastava et al. 1981) and C. gloeosporioides with floccose-felty whitish to pale olivaceous grey aerial mycelium associated with leaves (Kumari et al. 1981). When strain CBS and orange acervuli, reverse of filter paper partly pale cinnamon, 853.73 was first accessed into CBS, von Arx identified it as C. pale olivaceous grey to olivaceous grey; growth rate 23–24 mm gloeosporioides, but with the remark “deviating by longer, slender in 7 d (33.5–34 mm in 10 d). Colonies on OA flat with entire conidia”. Molecular data do not support this identification; the strain margin; surface entirely covered with thin floccose-felty white to belongs to the C. acutatum complex, but it is possible that reports pale olivaceous grey aerial mycelium and orange acervuli, reverse of C. gloeosporioides refer to this species. vinaceous buff, purplish grey to fuscous black; growth rate 23–25 Colletotrichum cosmi is part of clade 2. It can be separated mm in 7 d (33.5–37.5 mm in 10 d). Conidia in mass orange. from other species by all gene sequences, but mostly with only 1 bp divergence. There are more sequence divergences in GAPDH Material examined: Netherlands, Wageningen, from seed of Cosmos sp., collection and HIS3; however, with these genes individually, the species sits date and collector unknown (deposited in CBS collection in Nov. 1973 by G.H. within the very variable C. nymphaeae clade. The closest match Boerema), (CBS H-20794 holotype, culture ex-type CBS 853.73 = PD 73/856). in a blastn search with the TUB2 sequence of strain CBS 853.73 (with 99 % identity, 4 bp differences) was GU246633 from isolate Notes: Kwon et al. (1999) report C. acutatum (s. lat.) to cause sunken R14 from Capsicum annuum from South Korea (Sang et al. 2011), brownish spots on stems, as well as symptoms on leaves, flowers while the closest match with the GAPDH sequence covering ± and floral axes of Cosmos bipinnatus in Korea. Morphological the full length sequence (with 98 % identity, 4 bp differences) was characters (conidia, appressoria) are similar to those of strain CBS HQ846724 from isolate OBP6 from an unknown plant, probably 853.73, except for setae, which our strain did not develop in our from India (P. Chowdappa, C.S. Chethana, S. Madhura, unpubl. standard culture conditions. It is therefore possible that the collection data). We do not consider that these data in isolation are sufficient from Korea represents C. cosmi. Colletotrichum acutatum (s. lat.) is also known as an anthracnose pathogen of flowers and flower buds evidence to identify these sequences as originating from C. cosmi. of Cosmos bipinnatus in Japan (Yaguchi et al. 1996). The shape of There are 22 sequences in GenBank that match the ITS sequence conidia and appressoria of the Japanese fungus are similar to our of strain CBS 853.73 with 99 % identity, all with 2 bp differences. strain, but the conidia are smaller, measuring 11–14 × 2.8–3.5 µm. 62 The CotriC ollet hum aCtum a ut species complex Fig. 8. Colletotrichum costaricense (from ex-holotype strain CBS 330.75). A–B. Conidiomata. C–H. Conidiophores. I–N. Appressoria. O–P. Conidia. A, C–D, O. from Anthriscus stem. B, E–N, P. from SNA. A–B. DM, C–P. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–P. septate, branched, to 40 µm long. Conidiogenous cells hyaline to Colletotrichum costaricense Damm, P.F. Cannon & Crous, pale brown, smooth-walled, cylindrical to ampulliform, 8–22 × 3–5 sp. nov. MycoBank MB800499. Fig. 8. µm, opening 1–1.5 µm diam, collarette 1–1.5 µm long, periclinal thickening distinct. Conidia hyaline, smooth-walled, aseptate, Etymology: Named after the country where it was collected, Costa straight, cylindrical with both ends acute, (12.5–)13.5–16(–18) × Rica. 3.5–4 µm, mean ± SD = 14.8 ± 1.4 × 3.8 ± 0.3 µm, L/W ratio = 3.9. Sexual morph not observed. Asexual morph on SNA. Vegetative Culture characteristics: Colonies on SNA flat with entire margin, hyphae 1–9.5 µm diam, hyaline, smooth-walled, septate, branched. hyaline to pale cinnamon, on Anthriscus stem partly olivaceous Chlamydospores not observed. Conidiomata not developed, grey to iron-grey, on filter paper pale olivaceous grey to olivaceous conidiophores formed directly on hyphae. Setae not observed. grey, with short or woolly white aerial mycelium and few salmon Conidiophores hyaline, smooth-walled, simple or septate and acervuli on filter paper and on Anthriscus stem, reverse of filter branched. Conidiogenous cells hyaline, smooth-walled, cylindrical to paper same colours; growth rate 19–22.5 mm in 7 d (31–34 mm in ampulliform, polyphialides observed, 4.5–24 × 2–3.5 µm, opening 10 d). Colonies on OA flat with entire margin; surface olivaceous 0.5–1.5 µm diam, collarette 0.5–1.5 µm long, periclinal thickening with pale olivaceous grey to olivaceous grey sectors, the sectors visible. Conidia hyaline, smooth-walled, aseptate, straight, cylindrical covered with short white aerial mycelium and salmon acervuli with both ends acute, (9–)11.5–18(–28) × (3–)3.5–4(–4.5) µm, mean or culture completely covered with short felty whitish aerial ± SD = 14.6 ± 3.1 × 3.7 ± 0.3 µm, L/W ratio = 4.0. Appressoria mycelium, reverse honey, olivaceous grey to iron-grey, growth sparse, single or in small groups, pale brown, smooth-walled, subglobose to elliptical, the edge entire to undulate, (4.5–)6–8.5(–10) rate 22–23 mm in 7 d (28.5–34.5 mm in 10 d). Conidia in mass salmon to saffron. × (3–)4–6(–6.5) µm, mean ± SD = 7.1 ± 1.2 × 4.9 ± 0.9 µm, L/W ratio = 1.4, appressoria of strain CBS 211.78 are medium brown. Material examined: Costa Rica, Meseta Central, from berry of Coffea arabica cv. Asexual morph on Anthriscus stem. Conidiomata not Typica, collection date and collector unknown (deposited in CBS collection Jun. 1975 developed, conidiophores and setae formed directly on hyphae. by D. Mulder, Wageningen), (CBS H-20811 holotype, culture ex-type CBS 330.75); Setae medium to dark brown, smooth-walled to finely verruculose, Turrialba, from twig of Coffea sp., collection date and collector unknown (deposited in 0–2-septate, 50–60 µm long, base cylindrical, 3.5–4.5 µm diam, the CBS collection Apr. 1978 by C. Bianchini), culture CBS 211.78 = IMI 309622. tip ± acute. Conidiophores hyaline to pale brown, smooth-walled, www.studiesinmycology.org 63 Damm et al . Notes: Von Arx (in litt.) identified the strain CBS 330.75 as C. occasionally observed, discrete phialides measuring 4–14.5 × acutatum but with the remark “deviating by lack of pigment and 2.5–4.5 µm, opening 1.5–2 µm diam, collarette 0.5–1.5 µm long, less fusiform conidia”. While the main causal agent of coffee berry periclinal thickening conspicuous. Conidia hyaline, smooth-walled, disease (CBD) is C. kahawae (Waller et al. 1993) that belongs aseptate, straight, cylindrical with both ends acute, (15.5–)17.5– 21(–27) × (3–)3.5–4.5 µm, mean ± SD = 19.2 ± 1.7 × 4.0 ± 0.3 to the C. gloeosporioides species complex (Weir et al. 2012, this µm, L/W ratio = 4.8. Appressoria single or in loose clusters, pale issue), strains from the C. acutatum aggregate are not frequently brown, smooth-walled, elliptical to clavate, entire edge (3.5–)5.5– encountered associated with coffee. Hindorf (1973) studied Colletotrichum populations from Coffea arabica in Kenya and 11.5(–15.5) × (2–)3.5–5.5(–6.5) µm, mean ± SD = 8.5 ± 3.2 × 4.6 illustrated conidia or ascospores of some strains diverging from ± 0.9 µm, L/W ratio = 1.8. each other in morphology and culture appearance, including a Asexual morph on Anthriscus stem. Conidiomata acervular, conidiophores formed on pale brown angular basal cells, 3–8 µm strain identified as C. acutatum and another as C. gloeosporioides diam. Setae not observed. Conidiophores hyaline to pale brown, with conidia some of which are ellipsoidal and acute-ended. One smooth-walled, septate, branched, to 40 µm long. Conidiogenous of the two strains from western Kenya that are assigned to C. cells hyaline, smooth-walled, cylindrical to fusiform with both acutatum s. str. is derived from a suspected disease symptom ends acute, 8–21 × 2–3.5 µm, opening 1–2 µm diam, collarette on a coffee berry from Kenya that did not cause CBD (Gielink 0.5–1 µm long, periclinal thickening conspicuous. Conidia hyaline, & Vermeulen, 1983). One of the endophytic strains from Coffea smooth-walled, aseptate, straight, cylindrical with both ends acute, robusta in Brazil studied by Sette et al. (2006) showing antimicrobial (15–)17–20(–21) × (3.5–)4–4.5 µm, mean ± SD = 18.6 ± 1.5 × 4.2 activity against Staphylococcus aureus belongs to the C. acutatum ± 0.2 µm, L/W ratio = 4.5. species complex; since only a short ITS sequence of this strain was generated (DQ123614), the species cannot be identified. Culture characteristics: Colonies on SNA flat with entire margin, Colletotrichum walleri (clade 2) is known from a single strain from hyaline to buff, on filter paper and Anthriscus stem partly covered coffee, from Vietnam. Colletotrichum costaricense is quite distinct with woolly to felty white to pale grey aerial mycelium and orange from either of these taxa based on molecular sequence data. acervuli, reverse hyaline to buff, under filter paper pale olivaceous Two Colletotrichum species have previously been described grey; growth 20 mm in 7 d (30 mm in 10 d). Colonies on OA flat to from leaves of Coffea sp. in Costa Rica, C. brachysporum and raised with entire margin; surface partly covered with woolly white C. coffeophilum. Conidia of the first are smaller than those of C. to pale olivaceous grey aerial mycelium and olivaceous grey to costaricense and have a different shape; they are subglobose- orange acervuli appearing in rings, reverse buff, pale olivaceous ovoid and measure 7–8 × 4–6 µm (Saccardo et al. 1931), while grey to olivaceous grey with orange sectors; growth 19–21 mm in 7 those of C. costaricense measure on average 14.6 × 3.7 µm or 14.8 d (27.5–31 mm in 10 d). Conidia in mass orange. × 3.8 µm depending on the medium. Conidia of C. coffeophilum are wider than those of C. costaricense, being ellipsoidal and straight Material examined: Dominica, Castle Comfort, from Cuscuta sp., 1986, C. Prior (IMI or slightly curved (navicular), and measuring 13–15 × 6–8 µm 304802 holotype, CBS H-20784 isotype, culture ex-type IMI 304802). (Saccardo et al. 1931). Colletotrichum costaricense may be differentiated from the other Notes: Colletotrichum cuscutae is known from a single strain, species accepted here by TUB2, GAPDH and ACT sequences, reported from Dominica. The multigene analysis indicates that and most effectively with TUB2. The ACT sequences of the two it occupies a single subclade within clade 1, quite distinct from strains differ by 2 bp, but have only 1 bp in common to separate the principal subclade of C. lupini. Its conidia are substantially them from C. lupini and some of the unnamed single strains. The longer than is typical for C. lupini (mean length 18.6 µm as closest match in a blastn search with the TUB2 sequence of strain opposed to 12 µm for C. lupini), though the length range for the CBS 330.75 with 99 % identity (3 bp differences) was FN611028 latter species is considerable. The appressoria of C. cuscutae from a Citrus sinensis isolate (Ramos et al. 2006), while the are narrower than those of C. lupini and also greater in length/ closest matches with the GAPDH sequence with 99 % identity (2 width ratio. differences) were EU647322 and EU647324 from leatherleaf fern Colletotrichum species have been reported previously isolates (MacKenzie et al. 2009). All isolates were from Florida, as parasitising Cuscuta species, which are themselves non- USA. The closest matches with the ITS sequence with 100 % photosynthetic parasites of other plants. Colletotrichum identity were FN566877 from isolate DPI from Citrus aurantifolia in destructivum was found to affect Cuscuta campestris parasitising Florida, USA (Ramos et al. 2006) and isolate c2 from Citrus sp. in alfalfa crops in NW USA (Leach 1958). A strain identified as C. Brazil (Giaretta et al. 2010). gloeosporioides f. sp. cuscutae was apparently used widely as a biological control agent “Lu Bao no. 1” of Cuscuta in China after Colletotrichum cuscutae Damm, P.F. Cannon & Crous, sp. its adoption in the 1960s (Zhang 1985, Gao & Gan 1992), but its nov. MycoBank MB800500. Fig. 9. current commercial status is unknown and it may no longer be in production (Watson et al. 2000). According to Watson et al. (2000) Etymology: Named after the host plant, Cuscuta. and Dinoor et al. (2009) the Lu Bao strain belongs to C. acutatum rather than C. gloeosporioides. However, no detailed morphological Sexual morph not observed. Asexual morph on SNA. Vegetative data are available and the identification as C. acutatum was made hyphae 1–5.5 µm diam, hyaline, smooth-walled, septate, branched. by means of primers that at that time were considered to be Chlamydospores not observed. Conidiomata not developed, species-specific for the two species that are both now recognised conidiophores formed directly on hyphae. Setae not observed. as species complexes. Conidiophores hyaline, smooth-walled, simple or septate and Guerber et al. (2003) studied isolates from Cuscuta in the USA branched, to 35 µm long. Conidiogenous cells hyaline, smooth- and China that belong to two different species, neither of which walled, cylindrical to ampulliform, often integrated, polyphialides is conspecific with C. cuscutae. Based on GAPDH sequences 64 The CotriC ollet hum aCtum a ut species complex Fig. 9. Colletotrichum cuscutae (from ex-holotype strain IMI 304802). A–B. Conidiomata. C–J. Conidiophores. K–P. Appressoria. Q–R. Conidia. A, C–E, Q. from Anthriscus stem. B, F–P, R. from SNA. A–B. DM, C–R. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–R. (Guerber et al. 2003), isolates FRC2 and FRC7 from dodder in Colletotrichum fioriniae (Marcelino & Gouli) R.G. Shivas & the USA are C. fioriniae , while strain 783 from China (apparently Y.P. Tan, Fungal Diversity 39: 117. 2009. Fig. 10. identical with strain Lu Bao no. 1) belongs to a subclade of clade Basionym: Colletotrichum acutatum var. fioriniae Marcelino & 2 that is not included in this study. Strain 783 was found to have Gouli, Mycologia 100: 362. 2008. a haplotype of MspI mtDNA identical to those of two Australian ≡ Glomerella fioriniae (Marcelino & Gouli) R.G. Shivas & Y.P. Tan, Fungal Diversity 39: 117. 2009. strains causing terminal crook disease of pine, and distinct from ≡ Glomerella acutata var. fioriniae Marcelino & Gouli, Mycologia 100: 362. those of other Cuscuta strains. In an attempt to compare endophytes of a Cuscuta parasite and its hosts in India, Suryanarayanan et al. (2000) isolated 44 fungal Sexual morph not observed. Asexual morph on SNA. Vegetative endophytes from Cuscuta reflexa, including C. gloeosporioides , hyphae 1.5–7.5 µm diam, hyaline to pale brown, smooth-walled, C. truncatum and a “Colletotrichum sp.” that was not further septate, branched. Chlamydospores not observed. Conidiomata characterised. None of the strains is included in this study, and conidiophores formed directly on hyphae. Setae not observed. there are no corresponding sequences available on GenBank. Conidiophores hyaline to pale brown, smooth-walled, septate, Colletotrichum cuscutae is separated from other species by all branched, up to 35 µm long. Conidiogenous cells hyaline to pale genes studied except for ITS, most effectively by TUB2 and ACT. brown, smooth-walled, cylindrical to ampulliform, sometimes lacking In blastn searches with the ITS, TUB2 and GAPDH sequences of a basal septum and continuous with the conidiophore, sometimes the ex-type strain IMI 304802, no sequence matched with 100 % covert with a mucous coating, discrete phialides measure 4–12 × homology. Closest matches with the TUB2 sequence (with 98 % 2.5–3.5 µm, opening 1–2 µm diam, collarette 1 µm long, periclinal identity, 8 bp differences) were FN611029 and FN611028 from thickening distinct. Conidia hyaline, smooth-walled, aseptate, Citrus aurantifolia and Citrus sinensis from Florida, USA (Ramos et straight, fusiform to cylindrical with both ends acute, (10–)13.5– al. 2006) and the closest matches with the GAPDH sequence (with 16.5(–19.5) × 4–5(–5.5) µm, mean ± SD = 15.0 ± 1.6 × 4.5 ± 0.3 98 % identity and 4 bp differences) were EU168905, EU647318 and µm, L/W ratio = 3.3 µm, conidia of strain CBS 129947 are smaller, EU647319 from sweet orange (Peres et al. 2008, MacKenzie et al. measuring (10.5–)12–15(–17) × 3.5–5(–6) µm, mean ± SD = 13.5 2009). In a blastn search with the ITS sequence a large number of strains were 99 % identical with that of strain IMI 304802 including ± 1.7 × 4.1 ± 0.8 µm, L/W ratio = 3.3 µm. Appressoria solitary or several ITS sequences from Key lime isolates, e.g. EU647307 and in loose groups, pale to medium brown, smooth-walled, ellipsoidal, clavate to irregular outline, entire edge or undulate, (4.5–)7–11.5(– EU647308 (MacKenzie et al. 2009). www.studiesinmycology.org 65 Damm et al . Fig. 10. Colletotrichum fioriniae (from ex-holotype strain CBS 128517). A–B. Conidiomata. C–L. Conidiophores. M–R. Appressoria. S–T. Conidia. A, C–G, S. from Anthriscus stem. B, H–R, T. from SNA. A–B. DM, C–T. DIC, Scale bars: A = 200 µm, B = 100 µm, C = 10 µm. Scale bar of C applies to C–T. Material examined: USA, New York, Ward Pound Ridge Reserve, on mummified 15.5) × (4–)4.5–7(–10.5) µm, mean ± SD = 9.2 ± 2.2 × 5.6 ± 1.2 adult Fiorinia externa (elongate hemlock scale, insect), 2005, J.A.P. Marcelino µm, L/W ratio = 1.6. and S. Gouli, culture ex-holotype of C. fioriniae CBS 128517 = EHS = ARSE Asexual morph on Anthriscus stem. Conidiomata forming a 10222; Michigan, from Vaccinium sp. (blueberry), collection date and collector cushion of pale brown, thick-walled, angular cells, 3–6.5 µm diam. unknown (isolated by A. Schilder), culture CBS 129916 = CPC 16823; Unknown Setae not observed. Conidiophores hyaline to pale brown, smooth- country (probably USA), from Rubus sp., collection date and collector unknown (deposited in CBS collection Apr. 1935 by K.J. Kadow as Glomerella rubicola), walled, septate, branched, up to 35 µm long. Conidiogenous cells culture CBS 200.35. Australia, Queensland, Mount Tamborine, from fruit rot of hyaline to pale brown, smooth-walled, cylindrical, 10–22 × 3–4 Persea americana, 4 Sep. 2002, K.G. Pegg, culture CBS 127599 = BRIP 29284a; µm, opening 1.5–2 µm diam, collarette 0.5–1 µm long, periclinal Queensland, Brisbane, from Persea americana, collection date and collector thickening distinct. Conidia hyaline, smooth-walled, aseptate, unknown (isolated J.H. Simmonds, No. 13120, 25 Jun 1958) culture CBS 293.67 = straight, fusiform to cylindrical with both ends acute, (12.5–)14– DPI 13120; Queensland, Yarwun, endophytic from stem of Mangifera indica, 16 Feb. 1994, G.I. Johnson, culture CBS 127601 = BRIP 28761a. Portugal, Lisbon, from 18.5(–24.5) × 4–5 µm, mean ± SD = 16.1 ± 2.2 × 4.4 ± 0.4 µm, Vitis vinifera, 2000, collector unknown, culture CBS 129947. L/W ratio = 3.6, conidia of CBS 200.35 differ in sometimes having one round and one slightly acute end, conidia of strain CBS 129947 Notes: Colletotrichum fioriniae is the only representative of clade are smaller, measuring (13–)14–16(–17) × (3.5–)4–4.5(–5) µm, 3, which is supported by all six genes individually (including mean ± SD = 15.0 ± 1.0 × 4.3 ± 0.4 µm, L/W ratio = 3.5 µm. ITS). The clade has been recognised as distinct within the C. acutatum species complex for some years now (Sreenivasaprasad Culture characteristics: Colonies on SNA filter paper, Anthriscus & Talhinhas 2005), and was accepted as a separate species by stem covered with orange acervuli, on filter paper covered with Shivas & Tan (2009). white to pale olivaceous grey aerial mycelium and partly with In the current study, a large number of strains (over 50) has salmon to orange acervuli, reverse filter paper with pale olivaceous been found to belong to this species. They were isolated from a grey to olivaceous grey patches and spots, growth rate 22.5–23 wide variety of host plants, primarily in the temperate zones. There mm in 7 d (32.5–34 mm in 10 d). Colonies on OA flat with entire is some evidence of heterogeneity within the species, as two margin; surface saffron with olivaceous spots (mottled), covered subclades are apparent in the phylogenetic analysis, but neither with salmon acervuli, aerial mycelium lacking, reverse salmon, pale vinaceous, olivaceous to purplish grey, growth rate 22–22.5 mm in bootstrap support nor Bayesian probability values are sufficiently 7 d (34–35 mm in 10 d). Conidia in mass salmon to orange high to justify their recognition at species level. Also, strains from the major hosts and countries appear throughout the clade. 66 The CotriC ollet hum aCtum a ut species complex The name C. fioriniae is based on C. acutatum var. fioriniae made. The name C. rubicola was cited on herbarium labels by Ellis (Marcelino et al. 2008), named for a series of strains isolated from & Everhart but only as an asexual name for Glomerella rubicola; an epizootic infection of the exotic scale insect Fiorinia externa in apparently it was never accompanied by a description. the New England region. Implication of Colletotrichum species as Colletotrichum fioriniae is separated from other species by all entomopathogens might be considered surprising. However, the gene sequences studied. The closest matches in a blastn search insects in question are sap-suckers and C. fioriniae was found with the TUB2 sequence of strain CBS 128517 with 100 % identity to occur widely as an endophyte (Marcelino et al. 2009), both in were AY376557 (from apple in the USA, strain STE-U 5287; Lubbe the host plant of the scale insect (Tsuga canadensis) and in a et al. 2004) and AJ748628 from Liriodendron tulipifera in the UK phylogenetically diverse set of associated plants. This appears (Talhinhas et al. 2005). With 99 % identity (and 1–3 bp differences) to represent a further case of mutualism between Colletotrichum a series of matches could be made, including AJ748610 and and its host plants, with endophytic strains acting as natural AJ748623 from olive in Portugal, AJ748626 from Nandina protectants against insect herbivory. A similar case was reported domestica and AJ748634 from Magnolia in the UK (Talhinhas et al. for a strain labelled C. gloeosporioides f. sp. ortheziidae (probably 2005). Further sequences with the same level of homology include belonging to C. nymphaeae, see notes there) parasitising the AJ311668 from Vitis vinifera (Talhinhas et al. 2002), EF593320– economically important citrus scale insect Orthezia praelonga in EF593326 from Fiorinia externa, EF593329 from blueberry and Brazil (Cesnik et al. 1996). Endophytic Colletotrichum strains have EF593330 tomato (all from the USA; Marcelino et al. 2008), been demonstrated to protect Theobroma cacao plants against GU183274 from Acacia acuminata, GU183273, GU183270, and Phytophthora pathogens (Arnold et al. 2003, Mejía et al. 2008, GU183268 from Persea americana, GU183267 Actinidia chinensis Rojas et al. 2010). and GU183269 from Mangifera indica (all from Australia; Shivas & Strains referred to as C. acutatum and identified here as C. Tan 2009), AB618092 from Apium graveolens var. dulce (celery) in fioriniae have been implicated in fruit rot of cranberry and blueberry Japan (Fujinaga et al. 2011) and AB273716 from grape in Japan throughout the northern USA and in British Columbia (MacKenzie (Nakaune & Nakano 2007). All of these are likely to represent strains et al. 2009, Polashock et al. 2009). of C. fioriniae, further emphasising its widespread distribution and In fruit-rot assays by Freeman & Shabi (1996), isolates from presumably also its wide host range as a pathogen. apple and peach (based on ITS sequence, probably identifiable as C. fioriniae ) produced lesions on many different fruits, “suggesting Colletotrichum godetiae Neerg., Friesia 4: 72. 1950. Fig. that isolates of this group have the ability to cross-infect fruit from multiple hosts”. All of the fruits tested in the study (almond, ≡ Colletotrichum godetiae Neerg., Aarsberetn. J. E. Ohlens Enkes apple, avocado, mango, nectarine) are host plants of C. fioriniae plantepatol. Lab. 1 April 1942–31 Marts 1943: 8. 1943, nom. inval., Art. (Guerber et al. 2003, Table 1). In pathogenicity tests MacKenzie et 36.1. = Colletotrichum clavatum Agosteo, Faedda & Cacciola, Fungal Diversity 50: al. (2009) showed that isolates from blueberry (= C. fioriniae) did 292. 2011. not cause lesions on strawberry leaves but caused anthracnose on strawberry fruits, though lesions were smaller than those caused Sexual morph not observed. Asexual morph on SNA. Vegetative by isolates from strawberry (= C. nymphaeae). MacKenzie et al. hyphae 1–7 µm diam, hyaline to pale brown, smooth-walled, (2009) concluded that therefore the probability of an epidemic on septate, branched. Chlamydospores not observed. Conidiomata strawberry in Florida caused by blueberry isolates is rather low, but absent, conidiophores formed directly on hyphae. Setae not added that the climate could also play a role; in Florida, ripe rot of observed. Conidiophores hyaline, smooth-walled, simple, to 14 blueberry fruits is predominantly caused by C. gloeosporioides (s. µm long. Conidiogenous cells hyaline, smooth-walled, cylindrical, lat.), while further north in temperate regions, it is most frequently often with only short necks, 4–14 × (1.5–)3–6 µm, opening 1.5–2 caused by C. acutatum (s. lat.) (Smith et al. 1996). According to our µm diam, collarette 0.5 µm long, periclinal thickening observed. study, both species occur on strawberry, but based on the number Conidia hyaline, smooth-walled, aseptate, straight, cylindrical of strains we have seen, C. fioriniae seems to be of rather minor to fusiform with both ends acute or one end round and one end importance compared to C. nymphaeae. slightly acute, (7–)10.5–14.5(–15.5) × (3.5–)4–5(–5.5) µm, mean Marcelino et al. (2008) found that strains of C. fioriniae could ± SD = 12.4 ± 2.0 × 4.3 ± 0.5 µm, L/W ratio = 2.9, strains CBS be crossed to form a sexual morph and that some appeared to be 127561, CBS 129917, CBS 193.32 and CBS 129951 differ in self-fertile, though it is not clear whether the self-fertile strains were forming cylindrical to clavate conidia with one round and one acute derived from single spores. We did not see sexual production in the end, conidia of strain CBS 862.70 are larger, measuring (8–)14– strains examined during the present study. 19(–24) × (4–)4.5–5(–5.5) µm, mean ± SD = 16.4 ± 2.4 × 4.9 An earlier name may exist for C. fioriniae , in Gnomoniopsis ± 0.4 µm, L/W ratio = 3.4. Appressoria solitary, medium brown, rubicola (Stoneman 1898), one of a group of five species (including smooth-walled, clavate to elliptical, the edge entire or undulate Ga. cingulata) on which the genus Glomerella was based (Schrenk (8–)9–12.5(–14.5) × (3–)4–5.5(–6) µm, mean ± SD = 10.7 ± 1.9 × & Spaulding 1903a, b). That species was described from diseased 4.7 ± 0.7 µm, L/W ratio = 2.3. leaves of Rubus strigosus in West Virginia. No cultures are Asexual morph on Anthriscus stem. Conidiomata absent, available and the description of the asexual morph is not detailed, conidiophores formed directly on hyphae in aerial mycelium (in but Marcelino et al. (2009) showed that C. fioriniae is widespread in the region and both taxa produce a sexual morph. Kadow (1935) strain CBS 125972 present as a cushion of angular to roundish ascribed a disease of raspberry from the same region to Ga. cells 4–10 µm diam). Setae not observed (in strain CBS rubicola, and a culture derived from his work (CBS 200.35) has 125972 very few setae present, medium brown, smooth-walled, been examined in the current study and confirmed as belonging to 2–3-septate, 70–110 µm long, base cylindrical, 4–5 µm diam, tip ± acute). Conidiophores hyaline, septate, branched, smooth-walled. C. fioriniae. Without sequence-based evidence from type material, Conidiogenous cells hyaline, smooth-walled, cylindrical, 9–20 × however, we are reluctant to adopt this earlier name. As far as we can tell, a combination into Colletotrichum has never formally been 3 µm, opening 1.5 µm diam, collarette < 0.5 µm long, periclinal www.studiesinmycology.org 67 Damm et al . Fig. 11. Colletotrichum godetiae (F–G, L–M, T–U from ex-holotype strain CBS 133.44. A–E, H–K, N–S from strain CBS 125972). A–B. Conidiomata. C. Tip of a seta. D. Basis of a seta. E–M. Conidiophores. N–S. Appressoria. T–U. Conidia. A, C–H, T. from Anthriscus stem. B, I–S, U. from SNA. A–B. DM, C–U. DIC, Scale bars: A = 100 µm, E = 10 µm. Scale bar of A applies to A–B. Scale bar of E applies to C–U. Fragaria × ananassa, collection date and collector unknown, culture CBS 125972 thickening visible. Conidia hyaline, smooth-walled, aseptate, = PD 85/456; near Meerssen, from fruit of Sambucus nigra, collection date and cylindrical to fusiform with both ends acute, (9.5–)10.5–15(–20.5) × collector unknown (deposited in CBS collection Oct. 1970), culture CBS 862.70. 4–5 µm, mean ± SD = 12.8 ± 2.3 × 4.5 ± 0.4 µm, L/W ratio = 2.8, South Africa, from Podocarpus sp., collection date unknown, A. Wood, culture CBS strain CBS 127561 differs in forming clavate conidia with one round 129911. Colombia, Cundinamarca, from fruit anthracnose of Solanum betaceum, 13 Aug. 2010, J. Molina, culture CBS 129809 = T.A.1; Cundinamarca, from fruit and one acute end and strains CBS 129917, CBS 193.32 and CBS anthracnose of Solanum betaceum, 13 Aug. 2010, J. Molina, culture CBS 129816 129911 in forming cylindrical to clavate conidia with one round and = T.A.8. Chile, Puerto Saavedra, from tip necrosis on twig of Ugni molinae, 1 Oct. one acute end, conidia of strain CBS 862.70 are larger, measuring 2008, A. Schilder, culture CBS 127561. Mexico, Montecillo, from Schinus molle, (12.5–)15.5–18(–19.5) × 4.5–5(5.5) µm, mean ± SD = 16.8 ± 1.4 unknown collection date, M. de Jesus Yarez-Morales, culture CBS 129917. USA, Arkansas, Fayetteville, from Aeschynomene virginica (but see notes), collection date × 4.9 ± 0.2 µm, L/W ratio = 3.4, conidia of strain CBS 129911 are and collector unknown (deposited in CBS collection Aug. 1972 by G.E. Templeton smaller, measuring (7–)9–13(–15.5) × (2.5–)3–4 µm, mean ± SD = as C. gloeosporioides f. sp. aeschynomenes), G.E. Templeton, culture CBS 796.72. 11.0 ± 2.0 × 3.5 ± 0.3 µm, L/W ratio = 3.1. Notes: Colletotrichum godetiae was described from seed of Clarkia Culture characteristics: Colonies on SNA flat with entire margin, (syn. Godetia) hybrida cv. Kelvedon Glory by Neergard (1943), hyaline, with little low white aerial mycelium, on Anthriscus stem and validated with a Latin description seven years later (Neergard growth rate 21–21.5 mm in 7 d (30.5–31.5 mm in 10 d). Colonies 1950). Colletotrichum godetiae corresponds to C. acutatum group on OA flat with entire margin; surface salmon to hazel, no aerial A4 as recognised by Sreenivasaprasad & Talhinhas (2005) and to mycelium, reverse salmon to vinaceous buff; growth rate 21–24 part of clade F as defined by Guerber et al. (2003). According to mm in 7 d (30–33.5 mm in 10 d). Conidia in mass not observed in Sreenivasaprasad & Talhinhas (2005), group A4 corresponds to strain CBS 133.44, but in strain CBS 125972 orange. group B from New Zealand (Lardner et al. 1999). However, the only C. acutatum group B strain from New Zealand that we have studied Material examined: Denmark, from seed of Clarkia (syn. Godetia) hybrida cv. Kelvedon Glory 463 C in seed disinfection experiment, 17 Jun. 1943, P. Neergaard, belongs to C. acerbum (A6-2). Faedda et al. (2011) described culture ex-holotype of C. godetiae CBS 133.44. Italy, Calabria, Rizziconi, from strains from group A4 that cause olive anthracnose in Italy as C. rotten fruit of Olea europaea, Oct. 1992, G.E. Agosteo and G. Magnano di San Lio, clavatum, not knowing that an older name for this species exists, culture ex-holotype of C. clavatum CBS 130251 = OL10 = IMI 398854. Greece, of which the ex-holotype culture is available in the CBS culture from Olea europaea, collection date and collector unknown (deposited in CBS collection Jan. 1932 by L. Petri), culture CBS 193.32. Netherlands, Tilburg, from collection. The ex-holo- and ex-paratype strains are included in this 68 The CotriC ollet hum aCtum a ut species complex study (Fig. 1). Von Arx (1957) regarded C. godetiae as a synonym Colletotrichum guajavae Damm, P.F. Cannon & Crous, sp. of Ga. cingulata. nov. MycoBank MB800501. Fig. 12. Colletotrichum godetiae also occurs on hosts such as Fragaria, Malus, and Prunus, mainly in Europe and the Near East, causing Etymology: Named after the host plant, Psidium guajava. fruit, leaf or stem (cane, twig) diseases. Most of the isolates of C. acutatum s. lat. from Rhododendron in Sweden and Latvia Sexual morph not observed. Asexual morph on SNA. Vegetative (Vinnere et al. 2002) belong to this species, based on ITS data. hyphae 1–6 µm diam, hyaline to pale brown, smooth-walled, One of their strains (S1) is included in Guerber et al. (2003); its septate, branched. Chlamydospores not observed. Conidiomata GAPDH sequence groups with C. godetiae, thus confirming this not developed, conidiophores formed directly on hyphae. Setae placement. Additionally, several strains from Latin America have not observed. Conidiophores hyaline to pale brown, smooth- been studied. These occupy a subclade that has comparitively high walled, septate, branched, to 30 µm long. Conidiogenous cells bootstrap support, but as the subclades cannot be separated using hyaline, smooth-walled, cylindrical, some polyphialides observed, any single gene of the set we have used, we amalgamate them into 7–19 × 3–4 µm, opening 1–1.5 µm diam, collarette 0.5–1 µm the one species. long, periclinal thickening visible. Conidia hyaline, smooth-walled, Faedda et al. (2011) named C. clavatum to highlight the shape aseptate, straight, cylindrical to fusiform with both ends slightly of the conidia in the constituent strains. However, conidia of the acute, (6–)10.5–16.5(–23.5) × (2.5–)3–4(–5) µm, mean ± SD = ex-type strain of C. godetiae, CBS 133.44, are rarely clavate and 13.4 ± 3.0 × 3.5 ± 0.5 µm, L/W ratio = 3.8. Appressoria formed mostly fusiform or short cylindrical. Additionally, conidia of CBS singly, medium brown, smooth-walled, subglobose or elliptical to 125972 from strawberry on SNA are uniformly fusiform, while those clavate, the outline entire, (4.5–)5–8(–10.5) × (3.5–)4.5–6(–6.5) of CBS 193.32 from olive are mainly clavate, and those of CBS µm, mean ± SD = 6.6 ± 1.4 × 5.2 ± 0.7 µm, L/W ratio = 1.3. 129911 from Podocarpus are fusiform on SNA and mainly clavate Asexual morph on Anthriscus stem. Conidiomata acervular, on Anthriscus stem. According to Vinnere et al. (2002) isolates conidiophores formed on pale brown, angular, basal cells 2.5–8 from Rhododendron in Sweden and Latvia also form mainly clavate µm diam. Setae medium brown, smooth-walled, 0–2-septate, 40– conidia. The conidial shape is therefore an unreliable character for 75 µm long, base cylindrical, sometimes inflated, 3–6 µm diam at species recognition and seems to depend on the host/origin of the the widest part, tip ± acute. Conidiophores hyaline to pale brown, isolate or the growth medium. smooth-walled, septate, branched, to 40 µm long. Conidiogenous One of the isolates we studied, CBS 796.72, was deposited cells hyaline, smooth-walled, cylindrical, sometimes extending in the CBS collection in August 1972 by G.E. Templeton as to form a new conidiogenous locus, 7–18 × 2–3.5 µm, opening C. gloeosporioides f. sp. aeschynomenes and would appear 1–1.5 µm diam, collarette 0.5–1.5 µm long, periclinal thickening to be an authentic strain of this forma specialis (Daniel et al. conspicuous. Conidia hyaline, smooth-walled, aseptate, straight, 1973). Colletotrichum gloeosporioides f. sp. aeschynomenes cylindrical to fusiform with both ends ± acute, (11–)13–16(–17) × caused an epidemic anthracnose disease of northern jointvetch (3–)3.5–4 µm, mean ± SD = 14.6 ± 1.7 × 3.8 ± 0.3 µm, L/W ratio (Aeschynomene virginica) in 1969 in Arkansas, USA and was in = 3.9. the following years successfully applied as a biological control agent against this weed. According to our multigene phylogeny, Culture characteristics: Colonies on SNA flat with entire margin, this isolate belongs to the C. godetiae clade. According to Daniel hyaline, buff to pale honey, on filter paper partly pale olivaceous et al. (1973) C. gloeosporioides f. sp. aeschynomenes is specific grey, on medium, filter paper and Anthriscus stem partly covered for Aeschynomene species, was considered to be more virulent with whitish to pale olivaceous grey floccose-felty aerial mycelium, to A. virginica than to A. indica and did not affect rice, soybeans, reverse of filter paper smoke grey to grey olivaceous; growth rate cotton or 12 other common crops tested. The fungus developed as 22–24 mm in 7 d (31.5–34 mm in 10 d). Colonies on OA flat with the weed biocontrol agent Collego (TeBeest 1988, Ditmore et al. entire margin; surface white, pale olivaceous grey to rosy buff, 2008) against A. virginica was also named as C. gloeosporioides covered with thin floccose-felty whitish to pale olivaceous grey f. sp. aeschynomenes, and is genetically distinct from C. godetiae. aerial mycelium, reverse rosy buff, grey olivaceous to olivaceous It belongs to the C. gloeosporioides species complex and is newly black; growth rate 24–26.5 mm in 7 d (35.5–37 mm in 10 d). described in this volume as C. aeschynomenes (Weir at al. 2012, Conidia in mass salmon. this issue). This is probably the reason for differences noted in the host range by TeBeest (1988). There is also some confusion about Material examined: India, Assam, Silchar, from fruit of Psidium guajava, collection the host plant. Aeschynomene virginica as a weed of soybean date and collector unknown (deposited in IMI 1991 by M. Das as isolate India No. 1), (IMI 350839 holotype, CBS H-20793 isotype, culture ex-type IMI 350839). and rice fields is actually misidentified A. indica, while the true A. virginica is rare and threatened and became a federally listed Notes: Anthracnose and fruit canker of guava are serious diseases threatened species in the United States in 1992 (www. wikipedia. org). in the Indian subcontinent, and according to Misra (2004) are caused Colletotrichum godetiae is separated from other species in the in part by C. psidii. However, the identity of the guava pathogen C. acutatum species complex by all genes except CHS-1, which in the sense of Misra is unclear as the conidia are described as has the same sequence as in C. johnstonii; TUB2, ACT and HIS3 sickle-shaped. Curzi (1927) described the conidia of C. psidii as separate the species best. With all genes, the interspecific variation cylindrical with both ends rounded, straight, sometimes slightly is high. Blastn searches with the TUB2 seqence of CBS 133.44 curved and measuring 12–15 × 3.5–4.5 µm. Based on study of resulted in 100 % identity with several GenBank accessions from an authentic strain from Psidium sp. from Italy, C. psidii belongs olive isolates studied by Talhinhas et al. (2005) and one (AJ409294) to the C. gloeosporioides species complex (Weir et al. 2012, this issue). A separate taxon, Glomerella psidii (apparently based on from a Fragaria isolate (Talhinhas et al. 2002), followed with 99 % Gloeosporium psidii), causing the “mummy disease” of guava, has identity by AJ409302 from a Ceanothus isolate in France (Talhinhas et al. 2002). These are all probably referable to C. godetiae. uncertain relationships. The sexual morph was formed on apple www.studiesinmycology.org 69 Damm et al . Fig. 12. Colletotrichum guajavae (from ex-holotype strain IMI 350839). A–B. Conidiomata. C. Seta. D–H. Conidiophores. I–N. Appressoria. O–P. Conidia. A, C–E, O. from Anthriscus stem. B, F–N, P. from SNA. A–B. DM, C–P. DIC, Scale bars: A = 100 µm, D = 10 µm. Scale bar of A applies to A–B. Scale bar of D applies to C–P. agar and resembled Glomerella. The Gloeosporium stage it links to belongs to clade J3 sensu Guerber et al. (2003) (= C. acutatum s. may well fall within the C. acutatum complex: Gm. psidii, described str.). Apart from C. acutatum s. lat. and C. psidii, Farr & Rossman from Psidium pomiferi (= Psidium guajava) in Mexico, forms (2012) list reports from Psidium for C. coccodes in Myanmar, C. ellipsoidal-ovoid conidia measuring 10–16 × 4–6 µm (Saccardo gloeosporioides in Brazil, China, Cuba, India, Mexico, Puerto Rico, 1906); its conidia are thus broader than those of C. guajavae. South Africa, USA, Virgin Islands and Mexico, and Colletotrichum Gloeosporium fructus-psidii was found on fruits of Psidium in Sao sp. in Brazil, Jamaica and Mexico; it is possible that some of these Paulo, Brazil, and was described as forming oblong, subfusoid to reports should be referred to C. guajavae. clavate, hyaline conidia, measuring 14–20 × 5–6 µm (Saccardo et Colletotrichum guajavae can be distinguished from other al. 1931). The shape of the conidia of that species points also at the species of clade 2 of the C. acutatum complex using TUB2, C. acutatum complex, however, there is no species in this complex GAPDH and ACT sequences, most effectively with GAPDH. With with conidia on average generally wider than 5 µm. Conidia of C. data from GAPDH alone the species sits within the very variable guajavae are substantially smaller, measuring on average 13.4 × C. nymphaeae cluster. With TUB2 and ACT there is only 1 bp 3.5 µm on SNA and 14.6 × 3.8 µm on Anthriscus stem. difference between C. guajavae and C. scovillei, while CHS- Peres et al. (2002) isolated C. acutatum (s. lat.) from a guava fruit 1 and HIS3 sequences are the same as those of C. scovillei. in Brazil. It caused lesions on guava fruits that were slightly larger Colletotrichum guajavae is not reliably distinguishable from these than those caused by a C. acutatum (s. lat.) isolate from strawberry. species using morphological characteristics. Blastn searches Based on the ITS sequences they generated, the isolates from guava with the GAPDH sequence of strain CBS 853.73 shows 100 % and strawberry from Brazil belong to the same major clade as C. identity with HM038337 from Colletotrichum sp. isolate MFU 09 guajavae; the ITS sequence is in fact identical to that of C. guajavae, 0624 from Ziziphus mauritiana (jujube) from Laos (Phoulivong et but also the same as a number of other species in this complex, al. 2010), and it is therefore probable that this strain also belongs making an identification to species level impossible without additional to C. guajavae. The closest match with the TUB2 sequence of information. Based on a phylogeny from combined GAPDH and GS strain CBS 853.73, with 100 % identity, was GU246633 from sequences in the study by Guerber et al. (2003), both strains belong isolate R14 from Capsicum annuum from South Korea (Sang et to clade D (= clade 2 in this study), but not to the same subclade. al. 2011). We identify that isolate as C. scovillei; the available The GAPDH sequence generated in Guerber et al. (2003) differs sequence does not include the region containing the single in 5 bp from that of C. guajavae ex-holotype strain IMI 350839. A nucleotide polymorphism that distinguishes TUB2 sequences of strain from guava from New Zealand, included in the same study, C. guajavae and C. scovillei. 70 The CotriC ollet hum aCtum a ut species complex Fig. 13. Colletotrichum indonesiense (from ex-holotype strain CBS 127551). A–B. Conidiomata. C–G. Conidiophores. H–M. Appressoria. N–O. Conidia. A, C–E, N. from Anthriscus stem. B, F–M, O. from SNA. A–B. DM, C–O. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–O. 1–1.5 µm long, periclinal thickening visible. Conidia hyaline, Colletotrichum indonesiense Damm, P.F. Cannon & Crous, smooth-walled, aseptate, straight, cylindrical to fusiform with both sp. nov. MycoBank MB800502. Fig. 13. ends acute, (10.5–)13–17.5(–19) × (3–)3.5–4 µm, mean ± SD = 15.4 ± 2.2 × 3.7 ± 0.2 µm, L/W ratio = 4.1. Etymology: Named after the country of origin, Indonesia. Culture characteristics: Colonies on SNA flat, partly raised with Sexual morph not observed. Asexual morph on SNA. Vegetative entire margin, hyaline, buff to pale honey, on medium, filter paper hyphae 1–7 µm diam, hyaline, smooth-walled, septate, branched. and Anthriscus stem partly covered with irregular white aerial Chlamydospores not observed. Conidiomata not developed, mycelium, Anthriscus stem partly covered with orange acervuli, conidiophores formed directly on hyphae. Setae not observed. reverse hyaline, white, buff to cinnamon, filter paper partly Conidiophores hyaline, smooth-walled, simple or septate and olivaceous grey; growth rate 18.5–20 mm in 7 d (30–31 mm in 10 branched, to 40 µm long. Conidiogenous cells hyaline, smooth- d). Colonies on OA flat, partly raised with entire margin; surface walled, cylindrical to ± inflated, 8–21 × 2–3.5 µm, opening 1–1.5 covered with irregular floccose to woolly white to olivaceous grey µm diam, collarette 1–1.5 µm long, periclinal thickening distinct. aerial mycelium and few orange acervuli, reverse buff, cinnamon to Conidia hyaline, smooth-walled, aseptate, straight, cylindrical with dark purplish grey; growth rate 22.5–24 mm in 7 d (32.5–34 mm in one end round and one end acute, (8–)10–14.5(–18) × (2.5–)3.5– 10 d). Conidia in mass orange. 4(–4.5) µm, mean ± SD = 12.3 ± 2.4 × 3.8 ± 0.3 µm, L/W ratio = 3.2. Appressoria single, pale to medium brown, smooth-walled, Material examined: Indonesia: Sumatra, Tele, from leaf spots developing after elliptical, to subglobose in outline, the edge entire, sometimes herbicide treatment of Eucalyptus sp., 1 Jan. 2008, M.J. Wingfield, (CBS H-20798 undulate, 5.5–9(–14.5) × (5–)5.5–7.5(–9) µm, mean ± SD = 7.5 ± holotype, culture ex-type CBS 127551 = CPC 14986). 1.8 × 6.3 ± 1.0 µm, L/W ratio = 1.2. Asexual morph on Anthriscus stem. Conidiomata acervular, Notes: Eucalyptus is not a well-known disease reservoir for conidiophores formed on pale brown, angular, basal cells 2.5–6 µm Colletotrichum species. Colletotrichum eucalypti was described diam. Setae not observed. Conidiophores hyaline to pale brown, from Brazil by Bitancourt (1927) and noted again by Viégas (1946) smooth-walled, septate, branched, to 60 µm long. Conidiogenous from the Campinas region, causing anthracnose of Eucalyptus cells hyaline to pale brown, smooth-walled, cylindrical, sometimes leaves. Viégas described the species as having conidia that are ± inflated, 9–25 × 2–4 µm, opening 1–1.5 µm diam, collarette elongate-fusiform to oblong and 10–20 × 3–5 µm in size; the www.studiesinmycology.org 71 Damm et al . description is reminiscent of the C. acutatum species complex, but type, but present in strain IMI 357027, medium brown, basal cell cultures are not available, we have not seen type material, and the sometimes pale brown, smooth-walled, 0–1-septate, 35–55 µm species was described from a different continent. long, base cylindric-conical, often constricted at septum, 3.5–4 There is a number of Gloeosporium species that were described µm diam, the tip ± acute. Conidiophores hyaline, smooth-walled, septate, branched. Conidiogenous cells hyaline smooth-walled, on Eucalyptus spp. in different countries, but none was described cylindrical, sometimes slightly inflated, sometimes lacking a basal in Asia, and most differ considerably from C. indonesiense. septum and continuous with the conidiophore, some polyphialides Gloeosporium eucalypti was described on E. corynocalyx in observed, discrete phialides measure 6–27 × 2.5–4 µm, opening Australia, and forms shorter conidia than C. indonesiense, 1–2 µm diam, collarette 1–1.5 µm long, periclinal thickening distinct. measuring 8–10 × 3–4 µm (Saccardo 1906) compared to those Conidia hyaline, smooth-walled, aseptate, straight, cylindrical to of C. indonesiense that average 12.3 × 3.8 µm and 15.4 × 3.7 fusiform with one end slightly acute and one end round or slightly µm on SNA and Anthriscus stem, respectively. Gloeosporium acute, (13.5–)14.5–19(–21.5) × (3.5–)4.5–5(–6) µm, mean ± SD eucalyptorum, described on leaves and twigs of Eucalyptus spp. = 16.7 ± 2.1 × 4.7 ± 0.4 µm, L/W ratio = 3.6. Appressoria sparse, in Italy, has larger conidia, measuring 18–26 × 5–6 µm. They have single or in loose groups, pale to medium brown, smooth-walled, a different shape, cylindrical to cylindric-clavate, straight to slightly elliptical to clavate or irregular, the outline undulate or entire, (6–) curved, with both ends obtuse (see Tavola VIII, fig. 5 in Turconi 8–11.5(–14) × (2–)4–7.5(–10.5) µm, mean ± SD = 9.6 ± 1.7 × 5.8 1924), while conidia of C. indonesiense are straight and cylindrical, ± 1.9 µm, L/W ratio = 1.7. with one acute end when formed on SNA and both ends acute Asexual morph on Anthriscus stem. Conidiomata acervular, when formed on Anthriscus stem. Gloeosporium capsularum was conidiophores formed on pale brown, angular, basal cells, 3.5–7.5 described on Eucalyptus sp. in California, USA; it has longer and µm diam. Setae not observed in type, but present in strain IMI narrower conidia, measuring 18–20 × 2.5 µm. They are straight 357027, medium brown, basal cell pale brown, smooth-walled, and cylindrical with both sides obtuse (Saccardo 1884). Conidia of 0–1-septate, 40–60 µm long, base cylindric-conical to slightly Gm. nigricans described from leaves of E. pauciflora in Australia inflated, 2.5–5 µm diam, the tip ± acute to ± roundish, sometimes are ovoid and wider than those of C. indonesiense, measuring 12 with a constriction. Conidiophores hyaline, smooth-walled, septate, × 7 µm (Cooke 1891). Gloeosporium ochrostictum from E. rostrata branched, to 60 µm long. Conidiogenous cells hyaline, smooth- in Australia has oblong-clavate, inaequilateral conidia measuring walled, cylindrical, 11–26 × 2.5–4 µm, opening 1–2 µm diam, 9–12 × 4–5 µm (Saccardo 1899); conidia of C. indonesiense collarette 1 µm long, periclinal thickening distinct. Conidia hyaline, are narrower and aequilateral. We have not examined authentic smooth-walled, aseptate, straight, cylindrical to fusiform with one material of any of these taxa, but bearing in mind that none have end slightly acute and one end round or slightly acute, (14.5–)15.5– associated cultures and that type material would be too old to yield 17(–18) × 4.5–5(–5.5) µm, mean ± SD = 16.3 ± 1.0 × 4.9 ± 0.3 µm, multigene sequences, we prefer to leave them in obscurity. L/W ratio = 3.3. There are Colletotrichum species in the C. boninense species complex known on Eucalyptus: C. boninense and C. karstii have Culture characteristics: Colonies on SNA flat with entire margin, both been found on Eucalyptus in South Africa, and C. karstii also hyaline; medium, filter paper and Anthriscus stem partly covered occurs on the related host genus Eugenia in Brazil (Damm et al. with thin floccose white to pale grey aerial mycelium and orange 2012, this issue). acervuli, reverse hyaline with orange to grey acervuli shining Colletotrichum indonesiense is separated from other species through; growth rate 23–24.5 mm in 7 d (36–37 mm in 10 d). by TUB2, ACT, GAPDH and CHS-1 sequences, and most Colonies on OA flat to raised, with entire margin; surface covered effectively with TUB2. With CHS-1 there is only one bp difference with floccose whitish to pale olivaceous grey aerial mycelium and from C. laticiphilum, and the HIS3 sequence is the same as that of orange acervuli, reverse rosy buff, olivaceous grey to iron-grey in that species. The closest match in a blastn search with the TUB2 the centre; growth rate 22.5–24.5 mm in 7 d (37.5–39 mm in 10 d). sequence of strain CBS 127551 with 99 % identity (6 differences) Conidia in mass orange. was GU246633 from isolate R14 from Capsicum annuum from South Korea (Sang et al. 2011; identified by us as C. scovillei). Material examined: New Zealand, AK, Auckland, from fruit rot of Solanum The closest match with the GAPDH sequence (with 97 % identity, 7 lycopersicum, 29 Feb. 1990, J.M. Dingley, (CBS H-20809 holotype, culture ex-type CBS 128532 = ICMP 12926 = PRJ 1139.3); Takaka, from fruit rot of Citrus sp., 1989, bp differences) is isolate OCC95 from an unspecified crop in India collector unknown (deposited in IMI 1993 by P.R. Johnston, No. 1125.5), culture IMI (HQ846719; P. Chowdappa, C.S. Chethana, S. Madhura, unpubl. 357027 = PRJ 1125.5. data). There are more than 40 ITS sequences in GenBank with 99 % identity (1 bp difference) to the ITS sequence of C. Notes: Colletotrichum johnstonii is part of clade 4 but has slightly indonesiense. longer conidia than those of C. godetiae, and can be separated from other species on the basis of ACT, HIS3, TUB2, and GAPDH Colletotrichum johnstonii Damm, P.F. Cannon & Crous, sequences. The gene that performs best as a differential test is sp. nov. MycoBank MB800503. Fig. 14. ACT. The GAPDH sequence is only 1 bp different from that of C. godetiae, while the CHS-1 sequences of both species are the Etymology: Named after Peter R. Johnston (Landcare Research), same. The two C. johnstonii strains from citrus and tomato and a a major contributor to recent improvements in Colletotrichum strain from pear that is newly described here as C. pyricola were systematics. included in C. acutatum group C by Lardner et al. (1999). Two of their tamarillo strains, also in Lardner’s group C, had near-identical Sexual morph not observed. Asexual morph on SNA. Vegetative RAPD banding patterns to that of the ex-type strain of C. johnstonii. hyphae 1–7 µm diam, hyaline, smooth-walled, septate, branched. There are two strains from citrus (PJ50 = PRJ 1125.5 and PJ49 = Chlamydospores not observed. Conidiomata not developed, PRJ 1124.5) and one from tamarillo (Pj18 = PRJ 979.9) from New conidiophores formed directly on hyphae. Setae not observed in Zealand included in the study of Guerber et al. (2003) that have the 72 The CotriC ollet hum aCtum a ut species complex Fig. 14. Colletotrichum johnstonii (A–B, D–G, I–R. from ex-holotype strain CBS 128532. C, H. from IMI 357027). A–B. Conidiomata. C, H. Setae. D–G, I–J. Conidiophores. K–P. Appressoria. Q–R. Conidia. A, C–G, Q. from Anthriscus stem. B, H–P, R. from SNA. A–B. DM, C–R. DIC, Scale bars: A = 100 µm, B = 200 µm, D = 10 µm. Scale bar of D applies to C–R. same GAPDH sequence, and these strains also were assigned to µm long. Conidiogenous cells hyaline, smooth-walled, cylindrical, to group C in Lardner et al. (1999). From the evidence we have to conical or ± inflated, 5.5–18 × 2–3.5 µm, opening 1–1.5 µm diam, date, C. johnstonii appears to be endemic to New Zealand, but is collarette 0.5–1.5, periclinal thickening visible. Conidia hyaline, not host-specific. smooth-walled, aseptate, straight, cylindrical to fusiform with one The closest matches from GenBank with the TUB2 sequence round and one truncate end, (11–)15.5–21(–22.5) × (3–)3.5–4(– of strain CBS 128532 with (98 % identity, 10 bp differences) were 4.5) µm, mean ± SD = 18.3 ± 2.9 × 3.8 ± 0.4 µm, L/W ratio = 4.9. AJ409294 from Fragaria in the UK (Talhinhas et al. 2002) as well Appressoria not observed. as AJ748609, AJ748612-AJ748614, AJ748619–AJ748622 and Asexual morph on Anthriscus stem. Conidiomata absent, AJ748625, isolates from olive (Talhinhas et al. 2005). We do not conidiophores formed directly on hyphae. Setae not observed. believe that any of these sequences represent further records of Conidiophores, hyaline, smooth-walled, septate, sometimes C. johnstonii. With the GAPDH sequence of strain CBS 128532, branched, up to 50 µm long. Conidiogenous cells, hyaline, smooth- there was no closer match than 88 % identity. The ITS sequence walled, cylindrical to clavate, 20–27 × 2.5–4 µm, opening 1–1.5 µm of strain CBS 128532 is identical to those of C. salicis, C. pyricola diam, collarette 1 µm, periclinal thickening visible. Conidia hyaline, and C. phormii. smooth-walled, aseptate, straight, cylindrical to fusiform with one round and one truncate end, (n = 18) measure (15–)16–20.5(–23) Colletotrichum kinghornii Damm, P.F. Cannon & Crous, × 3.5–4.5 µm, mean ± SD = 18.1 ± 2.3 × 4.0 ± 0.4 µm, L/W ratio = 4.6. sp. nov. MycoBank MB800504. Fig. 15. Etymology: Named after W.O. Kinghorn, who previously studied Culture characteristics: Colonies on SNA flat with entire margin, this fungus. hyaline, medium partly covert with very short white aerial mycelium, reverse same colours; 14.5–15.5 mm in 7 d (21–24 mm in 10 d). Sexual morph not observed. Asexual morph on SNA. Vegetative Colonies on OA flat with entire margin, white, pale olivaceous grey hyphae hyaline, smooth-walled, septate, branched, 1–6 µm diam. to greyish sepia, surface covert with thin, short floccose white aerial Chlamydospores not observed. Conidiomata absent, conidiophores mycelium, reverse white to pale olivaceous grey; 11–16.5 mm in 7 formed directly on hyphae. Setae not observed. Conidiophores d (16–24 mm in 10 d). Conidia in mass not observed. hyaline, smooth-walled, simple or septate and branched, up to 45 www.studiesinmycology.org 73 Damm et al . Fig. 15. Colletotrichum kinghornii (from ex-holotype strain CBS 198.35). A–J. Conidiophores. K–L. Conidia. H–K. from Anthriscus stem. A–G, L. from SNA. A–L. DIC, Scale bars: B = 10 µm. Scale bar of B applies to A–L. Material examined: UK, Scotland, from Phormium tenax, unknown collection date, Colletotrichum laticiphilum Damm, P.F. Cannon & Crous, N.L. Alcock (deposited in CBS collection Feb. 1935 by W.O. Kinghorn as Glomerella sp. nov. MycoBank MB800505. Fig. 16. phacidiomorpha), (CBS H-20909 holotype, culture ex-type CBS 198.35). Etymology: latex = Greek for milk, latex and -philus = Greek for Notes: Kinghorn (1936) worked on two strains isolated from loving; referring to the economically significant feature of the host Phormium from material collected in Scotland by N.L. Alcock. Both plant. of these were identified as C. phormii by Farr et al. (2006). One of these is confirmed as C. phormii in this study, but we have found Sexual morph not observed. Asexual morph on SNA. Vegetative the other (CBS 198.35) to be distinct in molecular terms. Kinghorn hyphae 1–7.5 µm diam, hyaline, smooth-walled, septate, named his material Glomerella phacidiomorpha, but Farr et al. branched. Chlamydospores not observed. Conidiomata not (2006) examined the type of that name and found it to be a species developed, conidiophores formed directly on hyphae. Setae of Phaeosphaeriopsis. not observed. Conidiophores hyaline, smooth-walled, simple or Colletotrichum kinghornii is one of the two species in the C. septate and branched. Conidiogenous cells hyaline, smooth- acutatum complex with the largest conidia; only those of C. phormii walled, ampulliform to conical, sometimes lacking a basal septum are bigger. However, strain CBS 198.35 hardly sporulates, and and continuous with the conidiophore, discrete phialides measuring the conidia measured were mostly formed in the aerial mycelium. 6.5–15 × 3–4.5 µm, opening 1–1.5 µm diam, collarette 0.5–1.5 µm According to the molecular analyses, strain CBS 198.35 must be long, periclinal thickening visible. Conidia hyaline, smooth-walled, considered separate at species rank from C. phormii, with several aseptate, straight, cylindrical with both ends ± acute or one end sequence differences in almost every gene, and a single bp round and one end slightly acute, (9.5–)13.5–19.5(–25.5) × (3–) difference in the ITS sequence (this was not detected in the Farr 3.5–4(–4.5) µm, mean ± SD = 16.6 ± 3.1 × 3.8 ± 0.4 µm, L/W ratio et al. study). Colletotrichum kinghornii is most effectively separated = 4.4, conidia of CBS 129827 smaller, measuring (5–)8–15(–18.5) from other species using HIS3. × (1.5–)2.5–4.5(–5.3) µm, mean ± SD = 11.5 ± 3.4 × 3.6 ± 0.9 µm, Closest match in blastn searches with the TUB2 sequence L/W ratio = 3.2. Appressoria single, medium brown, smooth-walled, of strain CBS 198.35 (with 98 % identity, 7 bp differences) was subglobose, elliptical to clavate, the edge entire or rarely slightly Glomerella acutata isolate PCF 459 (EU635504) from strawberry undulate, (5–)6.5–12(–16) × (4–)6–8(–8.5) µm, mean ± SD = 9.2 in Belgium (Debode et al. 2009) and with 98 % identity (8 bp ± 2.8 × 7.2 ± 1.0 µm, L/W ratio = 1.3, appressoria of CBS 129827 differences) isolate PT250 (= CBS 129953) AJ748624 from olive smaller, measuring (4–)5–7(–8) × (2.5–)3.5–5.5(–6) µm, mean ± in Portugal (see A6-1) (Talhinhas et al. 2005). This last strain SD = 6.0 ± 1.1 × 4.5 ± 0.8 µm, L/W ratio = 1.3. is assigned to C. rhombiforme in this study. With the GAPDH Asexual morph on Anthriscus stem. Conidiomata possibly sequence of strain CBS 198.35 there was no closer match from acervular, but no basal cells observed. Setae not observed. GenBank than with 86 % identity. Conidiophores hyaline to pale brown, smooth-walled, simple or septate and branched, to 25 µm long. Conidiogenous cells hyaline 74 The CotriC ollet hum aCtum a ut species complex Fig. 16. Colletotrichum laticiphilum (from ex-holotype strain CBS 112989). A–B. Conidiomata. C–H. Conidiophores. I–L. Appressoria. M–N. Conidia. A, C–E, M. from Anthriscus stem. B, F–L, N. from SNA. A–B. DM, C–N. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–N. to pale brown, smooth-walled, ampulliform to cylindrical, 9–15 × Jayasinghe and colleagues found that the majority of strains 3.5–5.5 µm, opening 1–1.5 µm diam, collarette 0.5–1 µm long, examined from Sri Lanka belonged to C. acutatum (s. lat.), and periclinal thickening visible. Conidia hyaline, smooth-walled, Saha et al. (2002) reported this species from India as well; it is likely aseptate, straight, cylindrical with one end round and one end that similar strains are widespread in the region. Saha et al. (2002) slightly acute, (10–)12–15(–19.5) × 4–5(–5.5) µm, mean ± SD = revealed that C. acutatum (s. lat.) causes the raised spot symptom, 13.6 ± 1.7 × 4.5 ± 0.3 µm, L/W ratio = 3.0. while C. gloeosporioides (s. lat.) causes both anthracnose and papery lesions on Hevea leaves in India. In a study from Sri Lanka, Culture characteristics: Colonies on SNA flat with entire margin, Thambugala & Deshappriya (2009) found that C. acutatum causes hyaline to pale honey, filter paper pale olivaceous grey; growth larger lesions and can act synergistically in combination with C. rate 22.5 mm in 7 d (33.5 mm in 10 d). Colonies on OA flat with gloeosporioides to cause CLD. Strain IMI 383015 is one of the entire margin; surface white, buff to pale isabelline, covered with strains causing the raised spots on Hevea leaves in India. It was short felty white aerial mycelium, reverse buff to honey; growth included in the study of Saha et al. (2002) and also in the study of rate 22.5–23 mm in 7 d (32.5–35 mm in 10 d). Conidia in mass Lubbe et al. (2004), who generated its ITS and TUB2 sequences. whitish. The TUB2 sequence of strain IMI 383015 (AY376556) was also included in the TUB2 phylogeny by Shivas & Tan (2009); the strain Material examined: India, Kerala, Kottayam, Rubber Research Institute campus, was identified there as C. simmonsii. from raised spots on leaf of Hevea brasiliensis, 1999, unknown collector, (CBS It is necessary to consider the possible conspecificity of C. H-20799 holotype, culture ex-type CBS 112989 = IMI 383015 = STE-U 5303 = laticiphilum with three previously described taxa, all published CG ). Colombia, Meta, Villavicencio, from leaf, anthracnose of Hevea brasiliensis, 14 Aug. 2010, O. Castro, culture CBS 129827 = CH2. by Petch in the same paper (Petch 1906) from collections made from Hevea in Sri Lanka. These were named as C. heveae, Notes: Colletotrichum leaf disease (CLD) has been considered to be Gloeosporium heveae [nomenclaturally unrelated to C. heveae] a major cause of declining yields of Hevea brasiliensis in Southeast and Gm. alborubrum. All three species were regarded as synonyms Asia (Brown & Soepena 1994, Jayasinghe et al. 1997, Saha et al. of C. gloeosporioides by von Arx (1957). 2002). The pathogen was at first routinely identified as C. heveae Colletotrichum heveae was described with very wide conidia, (Petch 1906) and then assumed to be C. gloeosporioides (s. lat.) measuring 18–24 × 7.5–8 µm (Petch 1906), larger than any of (Carpenter & Stevenson 1954, von Arx 1957). the species in the C. acutatum species complex, and possibly www.studiesinmycology.org 75 Damm et al . belonging to the C. crassipes group as accepted by Sutton (1980). Colletotrichum laticiphilum is separated from other species by No type details were given in the original description. There is its TUB2, GAPDH and CHS-1 sequences, and most differentially a probable type specimen of C. heveae in K(M), collected from with TUB2. With CHS-1 there is only one bp difference from C. leaves of Hevea (Petch 2228) on 7 Oct. 1905, presumably from Sri indonesiense, while the HIS3 sequence is the same as that of Lanka. It is fragmentary and also contains a fungus identified on that species. The closest match with the GAPDH sequence (with the label as Gloeosporium brunneum. According to Petch (1927), 99 % identity, 1 bp difference) was HQ846719 from an unnamed C. heveae causes an indeterminate leaf spot, and is perhaps plant, probably from India (P. Chowdappa, C.S. Chethana, S. an invader following mechanical damage; it was not considered Madhura, unpubl. data). The ITS sequence of strain CBS 112989 to be a significant disease of rubber at that time. No fungus matches 100 % with AB042306 and AB042307 from isolates from corresponding to the description of C. heveae was found on the Carthamus and Glebionis from Japan (J. Moriwaki, T. Tsukiboshi, type specimen, and a slide previously made from this material T. Sato, S. Uematsu, unpubl. data), with AJ749675 from isolate (IMI 80135) also does not contain this species. Glomerella PD85/694 (= CBS 126519, C. chrysanthemi), and with AB219024 phyllanthi (from the related plant Phyllanthus acidus) was initially from strawberry in Japan (Chung et al. 2006). regarded as the sexual morph of C. heveae (Pai 1970), but was later revealed to belong to the C. boninense species complex, Colletotrichum limetticola (R.E. Clausen) Damm, P.F. as was another species on Hevea, C. annellatum (Damm et al. Cannon & Crous, comb. nov. MycoBank MB455483. Fig. 17. 2012, this issue). Basionym: Gloeosporium limetticola [as Gm. limetticolum] R.E. The conidia of Gm. heveae are about the same size as those of Clausen, Phytopathology 2: 231. 1912. C. laticiphilum (12–17 × 3.5–5 µm); however the spores extrude in a pale brown mass, which would be unusual for a Colletotrichum. Sexual morph not observed. Asexual morph on leaf of Citrus Also the size range of the “basidia” (= conidiogenous cells) is given aurantifolia (BPI 394978). Conidiomata conidiophores formed on as 20–34 × 2 µm; corresponding structures of C. laticiphilum are a cushion of pale brown angular cells 3–6 µm diam. Setae not shorter and much wider. There is no material in K(M) identified observed. Conidiophores hyaline, smooth-walled, septate and as Gm. heveae. It is possible that the fungus identified as Gm. branched, up to 75 µm. Conidiogenous cells hyaline, smooth- brunneum in the type collection of C. heveae is actually Gm. walled, cylindrical, sometimes slightly inflated, 10–18 × 2.5–4 heveae, as Gm. brunneum is a completely unrelated fungus µm, opening 1–1.5 µm diam, collarette 0.5–1 µm long, periclinal originating from Populus leaves in the USA (Ellis & Everhart thickening visible, sometimes distinct. Conidia hyaline, smooth- 1889). Petch could have realised after writing the packet label, but walled, aseptate, straight, sometimes slightly flexuous, cylindrical before publication, that naming his fungus Gm. brunneum would with one end round and one end slightly acute to truncate, or both create a later homonym. Petch (1927) indicated that Gm. heveae ends slightly acute, (10–)12.5–17.5(–20) × (3.5–)4–4.5(–4.5) µm, was found only in one isolated instance in 1905, when it caused mean ± SD = 15.1 ± 2.4 × 4.1 ± 0.3 µm, L/W ratio = 3.7. Appressoria leaf fall in young nursery-grown plants and resulted in general few observed on specimen, pale to medium brown, smooth-walled, discoloration and death of the whole leaf blade. The disease was subglobose, ovoid to ellipsoidal outline, entire edge. successfully controlled by reducing exposure to shade. Synonymy Asexual morph on SNA (CBS 114.14). Vegetative hyphae of Gm. heveae with our fungus would not affect the naming of C. 1–8.5 µm diam, hyaline, smooth-walled, septate, branched. laticiphilum as a combination into Colletotrichum based on Gm. Chlamydospores not observed. Conidiomata not developed, heveae would be a later homonym of C. heveae. conidiophores formed directly on hyphae. Setae not observed. It seems possible that Gm. alborubrum might be referable Conidiophores hyaline, smooth-walled, simple or septate and to the species described here. According to Saha et al. (2002) a branched, up to 45 µm. Conidiogenous cells hyaline, smooth- symptom consisting of raised spots had been attributed to this walled, cylindrical to ampulliform, sometimes integrated (not species. The fungus was originally described from green stems of separated from fertile hyphae by a septum, polyphialides rarely Hevea brasiliensis, but Petch (1927) stated that it caused abnormal observed, 8.5–20 × 3–5.5 µm, opening 1–1.5 µm diam, collarette leaf fall and appeared to spread to green ends of the branches to 0.5–1 µm long, periclinal thickening visible, sometimes distinct. cause dieback. He thought that it might be a secondary invader Conidia hyaline, smooth-walled, aseptate, straight, sometimes following Phytophthora infection. These symptoms do not seem slightly curved, cylindrical to clavate with one end round and to correspond well with those described by Saha and colleagues. one end slightly acute to truncate, or both ends slightly acute, The conidia of Gm. alborubrum were measured as 15–20 × 3–4 sometimes slightly constricted in the middle, (9–)12–20.5(–29) × µm, and described as oblong with rounded ends, straight or slightly (3–)4–5(–6) µm, mean ± SD = 16.3 ± 4.2 × 4.5 ± 0.6 µm, L/W ratio curved, issuing in thick pink or white tendrils (Petch 1906). The = 3.6. Appressoria single or in loose groups, pale to medium brown, size is similar to C. laticiphilum; we also observed slightly curved smooth-walled, subglobose, ovoid to ellipsoidal outline, entire or conidia, especially in the isolate from Colombia (CBS 129827). The undulate edge (5–)6–8.5(–11) × (4–)4.5–6(–7) µm, mean ± SD = conidial shape of both C. laticiphilum isolates on Anthriscus stem 7.4 ± 1.3 × 5.3 ± 0.7 µm, L/W ratio = 1.4. is not fusiform, but cylindrical with one end round and one end Asexual morph on Anthriscus stem (CBS 114.14). Conidiomata only slightly acute. Therer are three specimens in K(M) identified conidiophores formed directly on hyphae or on a cushion of by Petch as belonging to Gm. alborubrum, but none can be type pale brown angular cells 3.5–6.5 µm diam. Setae not observed. material as they were all collected after publication of the name. Bearing in mind that definite type material of all three names Conidiophores hyaline, smooth-walled, septate, branched, to 80 is either missing or fragmentary and that none of the authentic µm long. Conidiogenous cells hyaline, smooth-walled, cylindrical material would be likely to yield good sequences, we think that it slightly inflated, 6–13 × 2.5–4.5 µm, opening 1–1.5 µm diam, collarette 0.5–1 µm long, periclinal thickening visible. Conidia is more practical to publish a new taxon rather than to epitypify or hyaline, smooth-walled, aseptate, straight, cylindrical, clavate, neotypify one of the earlier names with a specimen that we are not confident is conspecific with the type. cylindrical to fusiform with one end round and one end (often only 76 The CotriC ollet hum aCtum a ut species complex Fig. 17. Colletotrichum limetticola (from ex-epitype strain CBS 114.14). A–B. Conidiomata. C–K. Conidiophores. L–Q. Appressoria. R–S. Conidia. A, C–G, R. from Anthriscus stem. B, H–Q, S. from SNA. A–B. DM, C–S. DIC, Scale bars: A = 100 µm, F = 10 µm. Scale bar of A applies to A–B. Scale bar of F applies to C–S. slightly) acute or both ends acute, (12–)13–18(–24) × (3.5–)4–4.5(– another Cuban strain (from Santiago de las Vegas) caused broadly 5.5) µm, mean ± SD = 15.5 ± 2.3 × 4.3 ± 0.4 µm, L/W ratio = 3.6. similar symptoms on both sour lime and lemon (Citrus limon) trees. Clausen stated that a virulent form of wither tip occurred in Florida Culture characteristics: Colonies on SNA flat to low convex with also, but this author was unable to access diseased material to entire margin, hyaline, filter paper partly pale salmon to straw, partly compare with the Cuban pathogen. covered with felty white aerial mycelium, reverse hyaline to pale Type material of Gm. limetticola was deposited by Clausen in ochreous, filter paper partly straw; 18.5–20 mm in 7 d (26–30.5 mm the dried fungus collections at the University of California (UC) and in 10 d). Colonies on OA flat with entire margin; surface moist, white Washington DC (BPI). However, its identity (in particular its local to pale luteous, saffron towards the centre due to sporulation, aerial geographical origin, i.e. from Herradura or Santiago de las Vegas) mycelium lacking, reverse whitish, buff to rosy buff, 18–21.5 mm in was not specified in the original paper. The species was described 7 d (26–29 mm in 10 d). Conidia in mass salmon. [translated from the Latin] as occurring “in young leaves and stems of Citrus medica var. acida, acting as a pathogen naturally in Cuba, Material examined: Cuba, Herradura, inoculation experiment XV in Berkeley, and also artificially inoculated in greenhouses in California on Alameda Co., California, from twig of Citrus medica var. acida (= Citrus aurantifolia), leaves and stems of C. medica var. acida, C. limetta and C. limon)”. unknown collection date, (inoculated 30 Jan. 1912, photographed 20 Mar. 1912 by R.E. Clausen), Earle (UC 302386 lectotype [not seen], BPI 394978 isolectotype). The relevant accession at UC consists of a single packet (UC USA, Florida, from young twig of Citrus aurantifolia, collection date and collector 302386) containing three further packets. One is from Clausen’s unknown (deposited in CBS collection Feb. 1914 by R.E. Clausen as Gloeosporium Experiment XV and is marked “lime type”; another is from lemon limetticola), (CBS H-20910 epitype, here designated, culture ex-epitype CBS (Experiment XXVII) and Cuban lime material (presumably the 114.14). original diseased sample) and is marked “type material”. The lemon sample is definitely from a genetic source different from that Notes: Gloeosporium limetticola was described by Clausen (1912) of the lime collections, and, it was not marked as type material. The following pathogenicity trials in California on young sour lime (Citrus two lime samples may well be genetically identical and could be medica var. acida = Citrus aurantifolia, Key lime) trees inoculated with strains from sour lime from Cuba and with strains from orange, regarded collectively as the holotype, but on balance we feel that lemon, pomelo and tangerine from Cuba, California, and Florida. treating them as two syntypes is more reasonable. That conclusion The Cuban sour lime strain from Herradura consistently caused was also reached by Tavares et al. (1997), who designated the wither tip disease symptoms on tester plants from that species, and collection from Experiment XV in UC as lectotype of Gm. limetticola. www.studiesinmycology.org 77 Damm et al . Cultures from the type material have not been preserved. Chen et al. (2005) identified a gene (KLAP1 gene) that was required However, strain CBS 114.14 from Florida was deposited in the CBS for causing KLA, particularly for the infection of Key lime leaves, but collection in Feb. 1914 by R.E. Clausen, as Gm. limetticola. The not for the infection of flower petals. strain was not specified as being an ex-type strain, and we suppose Colletotrichum limetticola is distinguished from other species that it was one of the samples requested by Clausen from wither by TUB2, GAPDH and HIS3, most effectively with TUB2, which tip of lime in Florida. It is reasonable to consider the culture as is only 2 bp different from the sequence seen in CBS 129823 authentic material, and we therefore designate a dried subculture (Colletotrichum sp. from Passiflora in Colombia, occupying an as epitype for Gm. limetticola. unnamed subclade within Clade 1). The wither tip disease of Citrus aurantifolia is apparently identical with Key lime anthracnose (KLA), a specific disease of Colletotrichum lupini (Bondar) Damm, P.F. Cannon & leaves, twigs, flowers and fruits of Key lime (Citrus aurantifolia) and Crous, comb. nov. MycoBank MB800519. Fig. 18. has been well studied in recent years (Brown et al. 1996, Agostini Basionym: Gloeosporium lupini [as Gm. lupinus] Bondar, Boln et al. 1992, Timmer & Brown 2000, Peres et al. 2008, MacKenzie Agric., São Paulo 13: 427. 1912. et al. 2009). While the causal organism of KLA was identified as C. ≡ Colletotrichum lupini (Bondar) Nirenberg, Feiler & Hagedorn, Mycologia 94(2): 309. 2002, nom. inval. (Art. 33.3). gloeosporioides by Agostini et al. (1992), following von Arx (1957) ≡ Colletotrichum lupini var. setosum Nirenberg, Feiler & Hagedorn, who listed the fungus as a synonym of that taxon, Brown et al. Mycologia 94(2): 309. 2002, nom. inval. (Art. 43.1). (1996) assigned the fungus to C. acutatum based on ITS sequence data. According to Farr & Rossman (2012), Gm. limetticola has been Sexual morph not observed. Asexual morph on SNA. Vegetative reported from Citrus aurantifolia in Barbados, California, Cuba, Fiji, hyphae 1–6.5 µm diam, hyaline, smooth-walled, septate, Florida, Hawaii, India, Jamaica, Philippines and Tanzania. branched. Chlamydospores not observed. Conidiomata absent, Colletotrichum strains from anthracnose on leaves of Key lime in conidiophores formed directly on hyphae on the surface of Florida, USA (KLA-Anderson, HM-1, Ss) and MTR-KLA-A1 (Belize) the medium and in the aerial mycelium. Setae not observed. included in the study of Peres et al. (2008) and MacKenzie et al. Conidiophores hyaline, smooth-walled, simple or septate and (2009) have the same ITS and GAPDH sequences as strain CBS branched, rapidly degenerating. Conidiogenous cells hyaline, 114.14. Additionally, the ITS sequences of isolates DPI from Citrus smooth-walled, cylindrical, 2.5–20 × 1.5–2.5 µm, often integrated aurantifolia in Florida, USA (FN566877, Ramos et al. 2006) and c2 (not separated from fertile hyphae by a septum), opening 0.5 µm from Citrus sp. in Brazil (EU008878, Giaretta et al. 2010) match that diam, collarette 0.5 µm long, periclinal thickening visible. Conidia of CBS 144.14 with 100 % identity. Probable C. limetticola strains are hyaline, smooth-walled, aseptate, straight, rather variable in shape, also included in Guerber et al. (2003) as mtDNA RFLP haplotype J3; usually cylindrical to clavate with one end round and one end acute, the GAPDH sequences of two Key lime strains (MD33, MD15) are 9–15(–26.5) × (3–)3.5–4.5(–6) µm, mean ± SD = 12.0 ± 3.2 × 4.1 almost identical to that of CBS 114.14. The closest match with the ± 0.6 µm, L/W ratio = 2.9, conidia of strain CBS 109221 are slightly TUB2 sequence of strain CBS 114.14 with 100 % identity is GenBank larger, measuring 11.5–15.5(–19) × (3.5–)4–4.5(–5) µm, mean ± accession FN611029 from isolate DPI as well (Ramos et al. 2006). In SD = 13.5 ± 1.9 × 4.3 ± 0.4 µm, L/W ratio = 3.2. Appressoria single their study on Citrus in Portugal, Ramos et al. (2006) did not find any or in small dense clusters, medium brown, round to elliptical in C. acutatum s. lat.; C. gloeosporioides (s. lat.) seems to be the major outline with an undulate to lobate margin, (4–)6–12(–20.5) × (4.5–) anthracnose pathogen. 6–9(–11.5) µm, mean ± SD = 9.0 ± 2.8 × 7.4 ± 1.7 µm, L/W ratio According to MacKenzie et al. (2009), Key lime isolates differ = 1.2. Appressoria of strain CBS 109221 differ in being arranged significantly from isolates from flowers of postbloom fruit drop singly or in rows along hyphae and mostly having an entire margin (PFD) affecting sweet orange (Citrus sinensis) in Florida, USA (rarely undulate to lobate). (STF-FTP-10, OCO-ARC-4, ALB-IND-25). The differences are Asexual morph on Anthriscus stem. Conidiomata acervular, found in their ITS, GAPDH and GS sequences. Based on ITS conidiophores formed on a cushion of pale brown angular cells and GAPDH sequences of 69 PFD and KLA strains from different 3–6.5 µm diam. Setae not observed in the ex-neotype strain, countries (Belize, Brazil, Costa Rica, Dominican Republic, USA but in strain CBS 109221 where a few setae were observed. (Florida), Mexico), Peres et al. (2008) recognised the causal agents Conidiophores hyaline to pale brown, smooth-walled, septate, of the two citrus diseases as two distinct phylogenetic lineages of branched, to 30 µm long. Conidiogenous cells hyaline to pale C. acutatum with few or no sequence differences in both the ITS brown, smooth-walled, cylindrical, sometimes ± inflated, 7–15 and GAPDH genes. We did not include PFD isolates in our study, × 2.5–3.5 µm, opening 1–1.5 µm diam, collarette 0.5 µm long, but according to ITS and GAPDH sequences, PFD and KLA strains periclinal thickening distinct. Conidia hyaline, smooth-walled, are related to each other, but seem to belong to different species. aseptate, straight, cylindrical to clavate with one end round and Agostini et al. (1992) noticed morphological and cultural differences one end acute, (10–)12.5–16(–18.5) × (3–)3.5–4.5 µm, mean ± SD between PFD and KLA isolates: appressoria of PFD isolates were = 14.2 ± 1.7 × 4.0 ± 0.3 µm, L/W ratio = 3.6. clavate and deeply pigmented and those of KLA isolates round, smaller and less pigmented. Also, KLA strains grew slightly more slowly than PFD isolates. Culture characteristics: Colonies on SNA flat with entire margin, Pathogenicity tests by MacKenzie et al. (2009) had basically hyaline, on filter paper and on Anthriscus stem partly covered with the same results as those by Clausen (1912); only Colletotrichum short white to pale grey aerial mycelium, reverse of filter paper isolates from key lime caused leaf necrosis on key lime, while white to pale luteous; growth 15–21 mm in 7 d (25–31 mm in 10 d). isolates from PFD, strawberry (= C. nymphaeae, according to Colonies on OA flat with entire margin; surface covered with felty to this study), blueberry (= C. fioriniae , according to this study) and woolly white to pale olivaceous grey aerial mycelium, reverse buff to smoke grey; growth 15–19 mm in 7 d (24–27 mm in 10 d), strain leatherleaf fern did not. Key lime isolates caused necrosis of flowers CBS 466.76 grows faster 23.5–27.5 mm in 7 d (36–37.5 mm in 10 on Orlando tangelo flower clusters as well, but the percentage of affected flowers was lower than those inoculated with PFD isolates. d). Conidia in mass salmon. 78 The CotriC ollet hum aCtum a ut species complex Fig. 18. Colletotrichum lupini (from ex-neotype strain CBS 109225). A–B. Conidiomata. C–I. Conidiophores. J–O. Appressoria. P–Q. Conidia. A, C, P. from Anthriscus stem. B, D–O, Q. from SNA. A–B. Dissecting microscope (DM), C–Q. Differential interference contrast illumination (DIC), Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–Q. Material examined: Ukraine, from seed of Lupinus albus, unknown date, H.I. Nirenberg and colleagues indicated that the ITS sequences of the Nirenberg, culture ex-neotype of C. lupini, CBS 109225 = BBA 70884. Germany, two varieties differ in only one base. Our study, based on analysis of from Lupinus albus, unknown date, U. Feiler, culture ex-holotype of C. lupini var. six genes, showed few other bp differences, blurring the distinction setosum, CBS 109221 = BBA 70352. between the two varieties. The name C. lupini var. setosum was also invalidly published (Art. 43.1). As the species name C. lupini Notes: Two studies on the causal agent of lupin anthracnose was invalid itself at the time, and as we do not accept the variety as published in 2002 arrived at different results: while Talhinhas et a distinct taxon, we do not validate the name here. al. (2002) regarded the causal agent of lupin anthracnose as C. According to Nirenberg et al. (2002), a typical feature of C. acutatum, Nirenberg et al. (2002) concluded that the causal isolates lupini is the conidial morphology, with spores having one end belonged to a separate species, C. lupini. Nirenberg and her pointed and one rounded. We also observed this feature clearly colleagues based this new name on Gloeosporium lupini (Bondar when the fungus was growing on Anthriscus stem. However, the 1912), but their combination is invalid because the basionym was conidia of the ex-neotype strain observed in this study on SNA are not cited correctly according to the ICBN. We therefore validate from simple or branched conidiophores at the agar surface and the combination here. Nirenberg et al. (2002) designated a dried from the aerial mycelium rather than from conidiomata, because the culture derived from BBA 70884 (= CBS 109225) as a neotype strain no longer produces defined acervuli on this medium. Conidia of Gm. lupini, since no type material was designated by Bondar from aerial mycelium are ± cylindrical, sometimes with both ends (1912); this action is nomenclaturally correct. rounded. They are very variable in size (Nirenberg et al. 2002). Nirenberg et al. (2002) additionally described a variety of the lupin Colletotrichum lupini was originally described from Lupinus pathogen, C. lupini var. setosum. They noted few morphological and albus in the São Paulo region of Brazil, presumably introduced physiological differences between the two varieties: strains of var. to South America along with its host plant, which is native to the lupini were observed to produce more conidia than var. setosum in the aerial mycelium, as well as to grow slightly slower on PDA and Mediterranean region (Kurlovich 2002). The only isolates from to have a lower optimum growth temperature. In addition, var. lupini South and Central America (Bolivia and Costa Rica) included in isolates usually formed concentric growth rings in culture, while var. our study have sequences identical to that of the ex-neotype strain setosum did not. The authors rarely observed setae in var. lupini, of C. lupini. The same is true for the strains studied from Europe but these were regularly seen in var. setosum. In our study, the and elsewhere. The species now appears to have no restriction to particular continents or climatic zones. ex-holotype strain of C. lupini var. setosum formed a few setae. www.studiesinmycology.org 79 Damm et al . Fig. 19. Colletotrichum melonis (from ex-holotype strain CBS 159.84). A–B. Conidiomata. C–H. Conidiophores. I–N. Appressoria. O–P. Conidia. A, C–E, O. from Anthriscus stem. B, F–N, P. from SNA. A–B. DM, C–P. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–P. Colletotrichum lupini is an economically significant pathogen Colletotrichum melonis Damm, P.F. Cannon & Crous, sp. of lupin crops worldwide, and there is substantial interest in nov. MycoBank MB800506. Fig. 19. breeding resistant host cultivars (e.g. Adhikari et al. 2011). While C. lupini shows a clear host preference based on the strains we Etymology: Named after host plant, Cucumis melo. have examined, a few cultures were derived from hosts other than lupins, namely from Manihot, Camellia and Cinnamomum. Sexual morph not observed. Asexual morph on SNA. Vegetative Sreenivasaprasad & Talhinhas (2005) also listed Urtica dioica hyphae 1–6.5 µm diam, hyaline, smooth-walled, septate, branched. as a host. A study by Nirenberg & Gerlach (2000) showed that Chlamydospores not observed. Conidiomata not developed, a strain of C. lupini var. setosum was able to infect Bergenia in conidiophores formed directly from vegetative hyphae. Setae not greenhouse tests. Pathogenicity tests by Sreenivasaprasad & observed. Conidiophores hyaline, smooth-walled, septate, branched, Talhinhas (2005) also failed to show host specificity of C. acutatum degenerating rapidly. Conidiogenous cells hyaline, smooth-walled, strains from lupins (= C. lupini), though Lardner et al. (1999) found cylindrical to ampulliform, 7–19 × 2.5–4 µm, opening 1–1.5 µm that the strains they placed in C. acutatum Group D (now known to diam, collarette 1–1.5 µm long, periclinal thickening visible. Conidia belong to C. lupini) did not infect pine seedlings in the manner of C. hyaline, smooth-walled, aseptate, straight, some slightly curved, acutatum f. sp. pineum (now regarded as C. acutatum s. str.). The cylindrical with one end round and one end slightly acute to round, strain from Camellia in the UK (IMI 351261) was deposited 1992 in rarely both ends acute, (7–)9–16.5(–23.5) × (3–)3.5–4.5(–5) µm, IMI by R. Cook and is most likely one of the avirulent C. acutatum mean ± SD = 12.8 ± 3.6 × 3.9 ± 0.4 µm, L/W ratio = 3.3 µm, L/W strains reported from ornamental Camellia species by Dickens and ratio = 3.7. Appressoria formed singly, medium brown, smooth- Cook (1989). walled, subglobose, elliptical or clavate, the edge entire, rarely Our phylogeny clearly supports C. lupini as a distinct species slightly undulate, (4.5–)6–11(–13.5) × (3.5–)4.5–6.5(–7.5) µm, mean within the C. acutatum species complex. Colletotrichum lupini is ± SD = 8.3 ± 2.4 × 5.5 ± 1.0 µm, L/W ratio = 1.5. separated from other species by all genes included, except for ACT, Asexual morph on Anthriscus stem. Conidiomata acervular, with TUB2 providing the best differential test. conidiophores formed on pale brown angular basal cells, 3–7 µm diam. Setae not observed. Conidiophores hyaline to pale brown, smooth-walled, septate, branched, to 50 µm long. Conidiogenous cells hyaline, smooth-walled, cylindrical to ampulliform, sometimes 80 The CotriC ollet hum aCtum a ut species complex Fig. 20. Colletotrichum nymphaea (from ex-epitype strain CBS 515.78). A–B. Conidiomata. C–G. Conidiophores. H–M. Appressoria. N–O. Conidia. A, C–D, N. from Anthriscus stem. B, E–M, O. from SNA. A–B. DM, C–O. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–O. polyphialidic, 10–20 × 3–4.5 µm, opening 1–2 µm diam, collarette The pathogenicity of C. melonis is not known. This appears to 0.5–1(–1.5) µm long, periclinal thickening visible, sometimes be the first report of a Colletotrichum species from the C. acutatum distinct. Conidia hyaline, smooth-walled, aseptate, straight, species complex as an associate of cucurbits. There are various cylindrical with one end round and one end slightly acute to round, reports of disease caused by members of the C. boninense and (9–)12–17(–20) × (3.5–)4–4.5(–5) µm, mean ± SD = 14.5 ± 2.3 × C. gloeosporioides clades, but the principal cucurbit pathogens 4.2 ± 0.3 µm, L/W ratio = 3.5. appear to be Glomerella magna and C. orbiculare (von Arx & van der Velden 1961, Jenkins & Winstead 1964, Du et al. 2005, Hyde Culture characteristics: Colonies on SNA flat with entire margin, et al. 2009, Cannon et al. 2012, this issue). hyaline to pale honey, on filter paper and Anthriscus stem partly Colletotrichum melonis is separated from other species by covered with floccose-felty white aerial mycelium, reverse same GAPDH, ACT and HIS3 sequences, with GAPDH performing best as a colours; growth 20.5–21.5 mm in 7 d (27.5–32 mm in 10 d). Colonies differential gene, while the TUB2 sequence is the same as that of strain on OA flat with entire margin; surface buff, honey to saffron, partly IMI 384185 (unnamed strain in clade 1). Closest matches in blastn covered with floccose-felty white aerial mycelium and saffron to search with the GAPDH sequence of strain CBS 159.84 (with 97 % isabelline acervuli, reverse buff, honey to rosy buff; growth 22–24 identity, 6 bp differences) were EU168905, EU647318 and EU647319 mm in 7 d (34–34.5 mm in 10 d). Conidia in mass saffron. from sweet orange (Peres et al. 2008, MacKenzie et al. 2009), while the closest published matches with the TUB2 sequence (with 99 % Material examined: Brazil, from peel of fruit of Cucumis melo, unknown collector identity, 4 bp differences) were FN611029 and FN611028 from Citrus and collection date (isolated by H.A. van der Aa, No. 9014 and deposited in CBS aurantifolia and Citrus sinensis from USA, Florida (Ramos et al. 2006). collection 1 Mar. 1984), (CBS H-20785 holotype, culture ex-type CBS 159.84). The ITS sequence matched 100 % with EU008864–EU008866 from Malus domestica in Brazil (Giaretta et al. 2010). Notes: Colletotrichum melonis belongs to clade 1 of the C. acutatum species complex but occupies a distinct subclade that Colletotrichum nymphaeae (Pass.) Aa, Netherlands J. Pl. is supported by multiple genes. The sole strain that we are aware of has appressoria with a significantly larger length/width ratio than Pathol., Supplement 1 84: 110. 1978. Fig. 20. those of C. lupini (mean L/W = 1.5 versus 1.2), the most frequently Basionym: Ascochyta nymphaeae Pass., in Rabenh., Fungi encountered species of clade 1. These appressoria form singly Europaei edn 2: 2251 (1876, in sched.); Hedwigia 16: 120. rather than in clusters. 1877. www.studiesinmycology.org 81 Damm et al . = Colletotrichum mahoniae Fabric., Atti Imp. Regia Accad. Rovereto, ser. 3, date and collector unknown (deposited in CBS collection Jun. 1951 by R. Ciferri), 6: 139. 1950. culture CBS 173.51; Rome, from Fragaria x ananassa, cv. Idea, collection date and collector unknown (send to Plantenziektenkundige Dienst Wageningen by L Corazza), culture CBS 126372 = PD 93/1666A. South Africa Western Cape, Sexual morph not observed. Asexual morph on SNA. Vegetative Stellenbosch, Elsenberg Farm, from Protea magnifica , 1 Apr. 2001, K. Lubbe, hyphae 1.5–5 µm diam, hyaline, smooth-walled, septate, branched. culture CBS 112992 = STE-U 4452. Spain, from fruit lesions of Fragaria sp., Mar. Chlamydospores not observed. Conidiomata absent, conidiophores 2002, H.A. van der Aa, culture CBS 112202. formed directly on hyphae. Setae not observed. Conidiophores hyaline to pale brown, smooth-walled, septate and branched, to Notes: Colletotrichum nymphaeae was described in detail in 60 µm long. Conidiogenous cells hyaline to pale brown, smooth- morphological and pathological terms by van der Aa (1978). Its walled, cylindrical, 10.5–20 × 2–4 µm, opening 1 µm diam, basionym Ascochyta nymphaeae was first validly published in 1876 collarette distinct, 1–1.5 µm long, periclinal thickening distinct. in Rabenhorst’s Fungi Europaei edn nova, exsiccatum no. 2251 Conidia hyaline, smooth-walled, aseptate, straight, cylindrical to (Stevenson 1971), and the label data was published in the journal cylindric-clavate with one end round and one end rounded to ± Hedwigia in the following year. The name A. nymphaeae was acute, (10–)14–18.5(–19.5) × (3–)4–5.5(–6) µm, mean ± SD = ascribed to Passerini on the exsiccatum label as an unpublished herbarium name. Individuals of this exsiccatum can therefore be 16.1 ± 2.3 × 4.9 ± 0.7 µm, L/W ratio = 3.3. Strain CBS 526.77 has regarded as type material, but it is not clear where the holotype smaller conidia, measuring (8.5–)9–13(–16) × (3–)3–4.5(–5) µm, resides. We interpret individuals of Fungi Europaei no. 2251 as mean ± SD = 11.0 ± 2.0 × 3.8 ± 0.6 µm, L/W ratio = 2.9, while isotypes, and select one of the three examples in Kew, K(M) 176820 conidia of strain CBS 112202 differ in being cylindrical to fusiform (labelled as purchased 1/1886) as lectotype of A. nymphaeae. We with both ends acute. Appressoria single, medium brown, smooth- also designate an epitype with a living culture from the material walled, elliptical, clavate or irregular in outline, entire, undulate to lobate margin, (4.5–)6–11(–15) × (3–)4.5–6.5(–8) µm, mean ± SD studied by van der Aa. = 8.7 ± 2.5 × 5.5 ± 1.0 µm, L/W ratio = 1.6. Van der Aa (1978) investigated possible synonyms of C. Asexual morph on Anthriscus stem. Conidiomata absent, nymphaeae, finding that Ramularia nymphaeae (syn. Ovularia nymphaeae) was conspecific with that species. Gloeosporium conidiophores formed directly on hyphae. Setae not observed. nymphaearum (Allescher 1895) is the type of the genus Ovulariella Conidiophores hyaline to pale brown, smooth-walled, septate, (considered as a nom. nud. by von Arx (1970) but with an indirect branched, to 60 µm long. Conidiogenous cells hyaline to pale reference to a description in the original publication). Von Arx brown, smooth-walled, ± cylindrical, sometimes polyphialidic, considered it to be a later synonym of Ramularia nymphaeae, and 12–30 × 2.5–3.5 µm, opening 0.5 µm diam, collarette distinct, 0.5 van der Aa (1978) confirmed the synonymy. To our knowledge, µm long, periclinal thickening distinct. Conidia hyaline, smooth- there are no living cultures derived from authentic material of either walled, aseptate, straight, cylindrical to cylindric-clavate with one of these taxa. We have no reason to doubt van der Aa’s synonymy, end round and one end rounded to ± acute, (12.5–)14–18.5(–22.5) but we have not examined type material and there is no strong × (4–)4.5–5.5(–6) µm, mean ± SD = 16.3 ± 2.1 × 4.8 ± 0.5 µm, reason to designate epitypes. L/W ratio = 3.4. Strain CBS 526.77 has wider conidia, measuring We have examined a culture from Mahonia aquifolia from (9.5–)13.5–19(–21.5) × (3.5–)5–6(–6.5) µm, mean ± SD = 16.1 ± Italy, which was sent to CBS by R. Ciferri as C. mahoniae the 2.7 × 5.6 ± 0.7 µm, L/W ratio = 2.9, while conidia of strain 173.51 year after the species had been described, and this could have are smaller, measuring (7.5–)10–14.5(–16) × (3–)3.5–4.5 µm, been derived from the type of C. mahoniae, but we do not have mean ± SD = 12.3 ± 2.0 × 3.9 ± 0.4 µm, L/W ratio = 3.2, conidia enough information to be sure. Another species from Mahonia, of most of the isolates studied differ in shape from the ex-epitype Gloeosporium japonicum (Hemmi 1920), was described as having strain, being cylindrical to fusiform with both ends acute, e.g. CBS wider conidia (10–18 × 5–7 µm) with a different shape (ellipsoidal, 173.51 and CBS 112202. short-cylindrical or ovoidal, both ends rounded). However, Hemmi mentioned that conidia in culture have very variable size and Culture characteristics: Colonies on SNA flat with entire margin, shape, measuring 9–20 × 3.6–6 µm in size. We have not located hyaline with low white aerial mycelium on filter paper and Anthriscus authentic material for this taxon, but even if it were conspecific with stem, on filter paper partly pale olivaceous grey on both sides; growth C. nymphaeae its name would not have priority. Von Arx (1957) rate 16.5 mm in 7 d (20 mm in 10 d); some strains grow faster, e.g. considered Gm. japonicum to be a synonym of C. gloeosporioides. CBS 126382 25–26 mm in 7 d (35–37 mm in 10 d). Colonies on OA Another possible synonym of C. nymphaeae is C. nymphaeicola flat with entire margin; surface isabelline, cinnamon to honey, white (Kelkar 1972, as C. “nymphicola”). Judging from the description at the margin, aerial mycelium lacking, reverse greyish sepia to buff; and illustration this is certainly a species of Colletotrichum, but the growth rate 14.5 mm in 7 d (20 mm in 10 d); some other strains conidia were claimed to be oblong and to measure 5–15 × 1.5–3 grow faster, e.g. CBS 126382 23.5–29 mm in 7 d (37.5–40 mm in µm. This wide variation in size makes it impossible to attempt a 10 d). Colony surface of strains CBS 516.78 and CBS 526.77 is dark placement in any species as currently circumscribed. The type olivaceous to iron-grey. Conidia in mass pale salmon. was reputedly deposited in HCIO but apparently no cultures were Material examined: Italy, Parma, in horto botanico, from leaf of Nymphaea alba, obtained. Gloeosporium nymphaeae (Hemmi & Kawase 1954) summer 1875, G. Passerini, in Rabenhorst, Fungi Europaei exsiccati edn 2: 2251 causes symptoms similar to those of C. nymphaeae, but setae were (holotype not selected by the original author and location uncertain; K(M) 176820 found to be present. These were not seen in C. nymphaeae either by isotype, here designated as lectotype; K(M) 99741 isolectotype; CBS H-00769 ourselves or by van der Aa (1978). The conidia of Gm. nymphaeae isolectotype). Netherlands, Oude Waal near Nijmegen, Gem. Ubbergen, from leaf spots of Nymphaea alba, 7 Aug. 1978, G. van der Velde, (CBS H-20787 were described as rounded at both ends, 9–17 × 3–6 µm. We have epitype, here designated, culture ex-epitype CBS 515.78 = van der Aa No. 6573); not been able to locate type material or living cultures of this fungus. Kortenhoefse Plassen from leaf of Nymphaea alba, collection date and collector A further species of Colletotrichum associated with waterlilies, unknown (isolated Aug. 1977 by H.A. van der Aa), culture CBS 526.77; from curl C. nupharicola, was described by Johnson et al. (1997). This disease of Anemone coronaria De Caen, collection date and collector unknown, species appears to have substantially longer and wider conidia CBS 126382 = PD 79/648. Italy, Rome, from leaf of Mahonia aquifolium, collection 82 The CotriC ollet hum aCtum a ut species complex Fig. 21. Colletotrichum orchidophilum (A–M, S–T from ex-holotype strain CBS 632.80. N–R from IMI 305357). A–B. Conidiomata. C. Setae. D–F. Conidiophores. H. Tip of seta. I. Basis of seta. J–M. Conidiophores. N–R. Appressoria. S–T. Conidia. A, C–F, S. from Anthriscus stem. B, H–R, T. from SNA. A–B. DM, C–T. DIC, Scale bars: A = 100 µm, D = 10 µm. Scale bar of A applies to A–B. Scale bar of D applies to C–T. than C. nymphaeae with mean widths of individual strains ranging the search yielded AJ748605, AJ748607, AJ748608, AJ748611, between 6.5 and 7.5 µm (the figures are difficult to interpret and AJ748615 from olive; AM992148, AM992147 probably also from the overall range of conidial size in the discription surprising). It has olive; AJ748633 from Photinia (Talhinhas et al. 2005, 2009); and been found to belong within the C. gloeosporioides complex (Weir GQ369612 from a strain identified as C. caudatum (Chen H, et al. 2012, this issue). Feng Y and Hyde KD, unpubl. data). With 99 % identity reflecting In pathogenicity tests MacKenzie et al. (2009) showed that 2 bp differences, we got EF593327 and EF593328 from strains Colletotrichum isolates from petiole, fruit and crown of strawberry ARSEF4360 and EMA26, respectively, from Orthezia praelonga in with anthracnose from Florida, USA (based on ITS and GAPDH: Brazil (Marcelino et al. 2008). These two strains were identified as C. nymphaeae) caused anthracnose on strawberry fruits. Lesions C. gloeosporioides f. sp. ortheziidae and have entomopathogenic were larger than those caused by isolates from blueberry (based on activity to the scale insect Orthezia praelonga. They are apparently ITS and GAPDH: C. fioriniae ). These differences in virulence should being used effectively as a biological control agent against this be attributed to the different species the pathogens belong to rather insect in Brazil (Cesnik et al. 1996, Cesnik & Ferraz 2000). Several than to the different host plants; both species occur on strawberries, of these strains listed above are included in this study. but based on the number of strains in this study, C. nymphaeae seems to be the more important strawberry anthracnose pathogen Colletotrichum orchidophilum Damm, P.F. Cannon & within the C. acutatum species complex. Crous, sp. nov. MycoBank MB800507. Fig. 21. Colletotrichum nymphaeae is well separated from other species with TUB2, but not in its ITS. With all other genes the intraspecific Etymology: Named for the host plants from which the species is variability is very high. The closest matches (100 % identity) in a known, all of which belong to the Orchidaceae. blastn search using the TUB2 sequence of the ex-epitype strain were AB618090 from Apium in Japan (Fujinaga et al. 2011); AY376551– Sexual morph not observed. Asexual morph on SNA. Vegetative AY376555 from Protea (Lubbe et al. 2004); AJ409296, AJ314716, hyphae 1.5–7 µm diam, hyaline to pale brown, smooth-walled, AJ314718 from Fragaria in USA, Portugal and Australia; AJ314722, AJ409300, AJ748636 from Lupinus and Anemone (Talhinhas et al. septate, branched. Chlamydospores not observed. Conidiomata 2002, 2005); and DQ454063, DQ454064 from Fragaria in Thailand not developed, conidiophores and setae formed directly on hyphae. (Than et al. 2008a). With 99 % identity reflecting 1 bp difference, Setae abundant, medium brown, basal cell often paler, smooth- www.studiesinmycology.org 83 Damm et al . walled, 1–2-septate, 40–80 µm long, base cylindrical, 2–4.5 µm Notes: Diagnostic features for C. orchidophilum include its very diam, tip somewhat acute. Conidiophores pale to medium brown, narrow (usually 3–3.5 µm wide) cylindrical conidia, abundantly septate, branched, smooth-walled, to 60 µm long. Conidiogenous formed setae and dark brown, uniformly shaped, pyriform to cells hyaline to medium brown, usually smooth-walled, but some spathulate appressoria. Colletotrichum orchidophilum is basal to warted conidiogenous cells observed, cylindrical with a slime the C. acutatum species complex (fig. 1 in Cannon et al. 2012, this sheath, 7–18 × 2.5–5 µm, opening 1–1.5 µm diam, collarette issue) and therefore used as outgroup in the phylogeny of the C. 0.5 µm long, periclinal thickening conspicuous. Conidia hyaline, acutatum complex (Fig. 1). The species is associated with a range smooth-walled, aseptate, straight, cylindrical with one end round of genera in the Orchidaceae. According to blastn searches with ITS sequences, C. orchidophilum has possibly also been found and one end somewhat acute, (10.5–)11.5–14(–16.5) × (2–)3– on other orchids and in other countries: on Cycnoches aureum in 3.5(–4) µm, mean ± SD = 12.7 ± 1.1 × 3.1 ± 0.3 µm, L/W ratio = Panama (DQ286148, Farr et al. 2006), on Pleione sp. (AJ301980, 4.1, conidia of strain CBS 631.80 are larger, measuring (13–)13.5– Nirenberg et al. 2002) and as an endophyte of Dendrobium nobile 17.5(–19) × 2.5–3.5 µm, mean ± SD = 15.4 ± 2.1 × 3.0 ± 0.3 µm, in China (FJ042519, Yuan et al. 2009). As far as we can tell, C. L/W ratio = 5.1. Appressoria not observed in type, but present in orchidophilum is restricted to the Orchidaceae. strain IMI 305357, single or in periodic intervals along hyphae, dark The description of C. cinctum provided by Stoneman (1898), brown, smooth-walled, elliptical, pyriform or spathulate, (5.5–)7.5– with its narrow conidia and abundant setae, seems similar to that 15.5(–20.5) × (4.5–)5.5–8.5(–12) µm, mean ± SD = 11.6 ± 3.9 × of the strains we have identified as C. orchidophilum, and her 7.0 ± 1.6 µm, L/W ratio = 1.6, appressoria of strain CBS 631.80 strain originated from the same habitat and geographical region smaller, measuring (4.5–)5.5–11(–18) × (4–)4.5–6(–7) µm, mean as Berkeley & Curtis’s fungus Gloeosporium cinctum (Berkeley ± SD = 8.2 ± 2.8 × 5.2 ± 0.8 µm, L/W ratio = 1.6. In SNA cultures 1874). Stoneman referred to the binomial C. cinctum but only of strains IMI 305357 and CBS 119291 no setae were observed. in synonymy with the sexual morph Gnomoniopsis cincta (= Asexual morph on Anthriscus stem. Conidiomata acervular, Glomerella cincta), and it is therefore invalidly published. The conidiophores and setae formed directly on hyphae or on pale connection between Gloeosporium cinctum and Gnomoniopsis brown basal cells 3–6 µm diam. Setae abundant, dark brown, cincta does seem to be doubtful; Stoneman referred to the basal cell often paler, smooth-walled, 0–2-septate, 40–70 µm long, Colletotrichum morph “found associated with a pycnidial stage base cylindrical to conical, sometimes inflated, 3–6.5 µm wide, tip and also a minute pyrenomycetous form”. The former was somewhat acute, setae of strain CBS 631.80 only up to 40 µm long, not described (and is presumably a co-coloniser rather than with a round tip or functioning as conidiogenous cells. Conidiophores genetically linked), and the latter was described as having spores pale brown, septate, branched, to 40 µm long. Conidiogenous cells measuring only 6–7 × 2–3 µm – much smaller than typical hyaline to pale brown, smooth-walled, cylindrical, 7–16 × 3–5 µm, Glomerella ascospores. This contrasts with the Gnomoniopsis opening 1.5–2 µm diam, collarette 0.5–1 µm long, distinct, periclinal morph described by Stoneman from old cultures of the asexual thickening conspicuous. Conidia hyaline, smooth-walled, aseptate, morph, which had ascospores measuring 15–20 × 3 µm; we straight, cylindrical with one end round and one end somewhat acute, interpret this as the true sexual morph. We have not seen a (11.5–)12.5–14(–15.5) × (2.5–)3–3.5(–4) µm, mean ± SD = 13.2 ± sexual morph associated with C. orchidophilum, and we think it 0.9 × 3.3 ± 0.3 µm, L/W ratio = 4.0. is more likely that Stoneman’s fungus (and that of Berkeley & Curtis) belong to the C. gloeosporioides species complex. Culture characteristics: Colonies on SNA flat with entire margin, Colletotrichum orchidophilum differs from C. orchidearum hyaline, aerial mycelium lacking, medium, filter paper and on in forming much narrower conidia; those of the type of C. Anthriscus stem partly covered with acervuli appearing as tiny orchidearum forma eriae measure (13.5–)15.5–19.5 × 5–6 µm, black spots, which are also visible from the reverse side; growth mean ± SD = 17.2 ± 1.6 × 5.6 ± 0.3 µm, L/W ratio = 3.1, n = 20, rate 17.5–22.5 mm in 7 d (32.5–36 mm in 10 d). Colonies on OA flat and those of forma physosiphonis measure (14–)16–18.5 × 5–6 with entire margin; surface olivaceous to grey olivaceous, covered µm, mean ± SD = 17.2 ± 1.1 × 5.5 ± 0.3 µm, L/W ratio = 3.1, with black or salmon acervuli, aerial mycelium lacking, reverse n = 20. Colletotrichum orchidearum was described by Allescher olivaceous to olivaceous grey; growth rate 18–26 mm in 7 d (30– (1902) from three diseased orchid plants in the glasshouses of 37.5 mm in 10 d). Conidia in mass salmon. Colonies of isolate IMI the Munich botanic garden. Each of the collections was given a 309357 differ in forming felty white to olivaceous buff or grey aerial separate name at forma rank, as listed above, and while no forma mycelium on OA and Anthriscus stem. orchidearum was listed, that name automatically comes into existence on description of the other forms (Art. 26). The species Material examined: USA, Hawaii, Oahu, Manoa, from Dendrobium sp., unknown collection date and collector (deposited in CBS collection Oct. 1980 by M. Aragaki, account included a description of the overall taxon, and compared isolated 1978 as No. 826), (CBS H-20718 holotype, culture ex-type CBS 632.80); it with C. macrosporum, another species from orchids described Hawaii, Kona, from × Ascocenda sp., unknown collection date and collector (deposited by Saccardo (1896) from a Brazilian collection. That species was in CBS collection Oct. 1980 by M. Aragaki, isolated 1978 as No. 828), culture CBS found by Saccardo to have substantially larger conidia than those 631.80. UK, from Phalaenopsis sp., unknown collection date and collector, culture IMI 305357. Panama, APHIS interception Miami 223820, from Cycnoches aureum, of C. orchidearum (measurements of 28–32 × 8–10 µm were collection date unknown (isolated 11 Apr. 2003 by M.E. Palm), D. Begley, culture given), and its affinities are currently unknown. One of the forms CBS 119291 = MEP1545. Germany, Munich, glasshouses of Botanical Garden, on introduced by Allescher, forma cymbidii, is invalidly published as dead and dying leaves of Eria javanica (syn. E. stellata), April 1895, J.E. Weiss (M- no description was given. 0140831 syntype of C. orchidearum (named as forma eriae) and lectotype of C. orchidearum, here designated); Munich, glasshouses of Botanical Garden, on both There are three dried specimens in the Allescher collections sides of dying leaves of Cymbidium aloifolium (syn. C. pendulum), Apr. 1895, J.E. in M, all gathered by Dr J.E. Weiss in April 1895, which clearly Weiss (M-0140830 syntype of C. orchidearum (named as C. orchidearum forma constitute type material; M-0140830 named as C. orchidearum cymbidii)); Munich, glasshouses of Botanical Garden, on dead and dying leaves of forma cymbidii from Cymbidium aloifolium (syn. C. pendulum), Stelis emarginata (syn. Physosiphon loddigesii), April 1895, J.E. Weiss (M-0140832 syntype of C. orchidearum (named as forma physosiphonis)). M-0140831 named as forma eriae from Eria javanica (syn. E. stellata), and M-0140832 named as forma physosiphonis from 84 The CotriC ollet hum aCtum a ut species complex Fig. 22. Colletotrichum paxtonii (from ex-holotype strain IMI 165753). A–B. Conidiomata. C–F. Conidiophores. G–K. Appressoria. L–M. Conidia. A, C–D, L. from Anthriscus stem. B, E–K, M. from SNA. A–B. DM, C–M. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–M. Stelis emarginata (syn. Physosiphon loddigesii). The collection on Colletotrichum paxtonii Damm, P.F. Cannon & Crous, sp. Cymbidium appears to be effete, and while a few of the conidiomata nov. MycoBank MB800508. Fig. 22. contained setae, no conidia or conidiogenous cells were seen. This may be why C. orchidearum forma cymbidii was not described in Etymology: Named after Sir Joseph Paxton, gardener to William th the original publication. It is necessary to designate one of these Spencer Cavendish, 6 Duke of Devonshire, who first brought the authentic collections as lectotype of C. orchidearum in order to fix Cavendish banana into cultivation. the application of that name, and we therefore choose M-0140831 for this purpose as M-0140830 is effete and M-0140832 is rather Sexual morph not observed. Asexual morph on SNA. Vegetative depauperate. That has the effect that C. orchidearum forma hyphae 1–8 µm diam, hyaline to pale brown, smooth-walled, eriae becomes an obligate synonym of C. orchidearum forma septate, branched. Chlamydospores not observed. Conidiomata orchidearum. There are no significant morphological differences not developed, conidiophores formed directly on hyphae. Setae between the material from Eria and that from Physosiphon. The not observed. Conidiophores hyaline, smooth-walled, septate, conidiomata of the invalid forma cymbidii are substantially larger branched, to 30 µm long. Conidiogenous cells hyaline, smooth- than those of the two validly published forms, and the host plant walled, cylindrical to ± inflated, 5–10 × 2–4 µm, opening 1–1.5 material is strongly blackened in their immediate vicinity. We are µm diam, collarette 1–1.5 µm long, periclinal thickening distinct. unable to establish the significance of this distinction; it may be Conidia hyaline, smooth-walled, aseptate, straight, cylindrical host- rather than fungus-related. with one end round and one end slightly acute both ends slightly Yang et al. (2011) reviewed species of Colletotrichum from acute, (5–)10.5–15.5(–19.5) × (2.5–)3.5–4(–4.5) µm, mean ± SD orchids in south-western China. They identified one clade as C. = 13.0 ± 2.6 × 3.7 ± 0.3 µm, L/W ratio = 3.5. Appressoria single orchidearum, and their Chinese strain does seem to have close or in loose groups, medium brown, smooth-walled, subglobose, similarities with the type of that species. None of the species elliptical or clavate, the edge undulate or entire, (5–)6–11.5(–16.5) treated in Yang et al. (2011) belong to the C. acutatum complex. × (3.5–)5.5–7.5(–8.5) µm, mean ± SD = 8.8 ± 2.7 × 6.5 ± 1.1 µm, L/W ratio = 1.4, strain CBS 502.97 forms smaller appressoria, measuring (3.5–)4.5–7.5(–10.5) × (3–)3.5–5(–5.5) µm, mean ± SD = 6.0 ± 1.7 × 4.2 ± 0.7 µm, L/W ratio = 1.4. Asexual morph on Anthriscus stem. Conidiomata acervular, conidiophores formed on pale brown, angular, basal cells 3.5–7.5 www.studiesinmycology.org 85 Damm et al . µm diam. Setae not observed. Conidiophores hyaline to pale brown, × 4 µm. It was collected from ripe bananas in Brisbane, Australia smooth-walled, septate, branched, to 30 µm long. Conidiogenous (Cooke 1887). Apart from the rounded ends of the conidia, the cells hyaline, smooth-walled, cylindrical, 7–19 × 2–3 µm, opening fungus has features that tend to place it in the C. acutatum complex. 1–1.5 µm diam, collarette 1–1.5 µm long, periclinal thickening Glomerella musarum was described from Musa paradisiaca in Sri distinct. Conidia hyaline, smooth-walled, aseptate, straight, Lanka and was observed to be associated with Gm. musarum and cylindrical to fusiform with both ends ± acute, sometimes one end other fungi (Petch 1917). We could not locate the type material round, (6.5–)12–15.5(–17) × (3–)3.5–4 µm, mean ± SD = 13.7 ± of either of these species to confirm their taxonomic positions. 1.8 × 3.8 ± 0.3 µm, L/W ratio = 3.6. Gloeosporium musarum var. importatum, described in 1910 on fruits of Musa sapinea in Germany, has conidia larger than those Culture characteristics: Colonies on SNA flat to raised with entire of C. paxtonii, measuring 9–24 × 5–7 µm (Saccardo 1913). margin, hyaline, on filter paper partly pale olivaceous grey, on Gloeosporium lagenaria var. musarum was published without medium, filter paper and Anthriscus stem partly covered with thin, any morphological information; the paper merely stated that this floccose white to pale olivaceous grey aerial mycelium and orange fungus did not differ from the forms found on Cucurbitaceae (Ellis acervuli, reverse hyaline to pale cinnamon, filter paper partly pale & Everhart 1889). The lack of description means that the name olivaceous grey; 23–24.5 mm in 7 d (34–36.5 mm in 10 d). Colonies is invalidly published. Gloeosporium lagenaria var. lagenaria again on OA flat with entire margin; surface covered with floccose rosy has conidia larger than those of C. paxtonii, measuring 16–18 × buff to pale olivaceous grey aerial mycelium and orange acervuli, 5–6 µm. It is widely believed to be a synonym of C. orbiculare reverse pale vinaceous, hazel, olivaceous grey to iron grey; growth (Cannon et al. 2012, this issue). rate 22.5–23 mm in 7 d (33.5–35.5 mm in 10 d). Conidia in mass Colletotrichum paxtonii is separated from other species by orange. TUB2 and GAPDH, with TUB2 performing best as a diagnostic sequence. With the GAPDH sequence there is only one bp Material examined: St. Lucia, from Musa sp., 1972, P. Griffee (IMI 165753 holotype, difference from C. sloanei, while ACT, HIS3 and CHS-1 sequences CBS H-20797 isotype, culture ex-type IMI 165753). Unknown country (West are the same as C. simmondsii. The closest matches in a blastn Indies), from Musa nana, unknown collection date (deposited in CBS collection Feb. 1997 by J.A. Bailey), P. Spencer-Phillips, CBS 502.97 = LARS 58 [sterile on receipt search with the TUB2 sequence of strain IMI 165753 (with 99 % at CBS, judging from information in Sherriff et al. (1994) these two strains originate identity, 2 bp differences) were AJ748635 from isolate PD 89/582 from the same isolate]. (= CBS 126524, C. simmondsii) from Cyclamen in the Netherlands (Talhinhas et al. 2005), EU635505 from isolate DAR 32068 (as Notes: The most prominent species of Colletotrichum associated A9 from Whitelaw-Weckert et al. 2007) from Fragaria in Australia with Musa species is C. musae, a central species in one of the (Debode et al. 2009), EF143968 from isolate BRIP 4704a from major clades of the C. gloeosporioides species complex (Weir et Fragaria in Australia (Than et al. 2008a) and FJ907443 from al. 2012, this issue). It was recently epitypified with a strain from isolate BRIP 28519 (ex-holotype culture of C. simmondsii) from Florida (Su et al. 2011). One of the strains (CBS 502.97 = LARS 58) Carica papaya in Australia (Prihastuti et al. 2009). With the GAPDH that we have examined of C. paxtonii was first studied by Sherriff et sequence of strain IMI 165753 there are no closer matches than al. (1994) using the misapplied name C. musae; however, Johnston 97 % identity covering ± the full of the length sequence. Since the & Jones (1997) confirmed that it was a member of the C. acutatum ITS sequence of C. paxtonii strain IMI 165753 is the same as that complex. Colletotrichum paxtonii does not appear to produce setae of several other Colletotrichum spp., there is a long list of 100 % at all, while C. musae rarely does so, and this may have led to matching sequences in GenBank. These sequences, however, are confusion between the two species in the past. all from isolates with hosts other than Musa. There are no records of C. acutatum (s. lat.) on Musa in Farr & Rossman (2012); however, some other species have been Colletotrichum phormii (Henn.) D.F. Farr & Rossman, described on Musa spp. Colletotrichum cavendishii was described Mycol. Res. 110(12): 1403. 2006. Fig. 23. by Petrak (1925) with “elongated oblong, ellipsoid, oblong or Basionym: Fusarium phormii Henn., Verh. bot. Ver. Prov. Brandenb. ovate, almost cylindrical” conidia that measure 10–19 × 4.5–7 µm. 40: 175. 1898. [1899]. This certainly suggests that Petrak’s species belongs to the C. ≡ Gloeosporium phormii (Henn.) Wollenw., Fus. Auto Delin. no. 498. 1916, acutatum species complex and it could provide an earlier name non Sacc. 1915. for C. paxtonii, but its conidia are described as substantially wider = Gloeosporium phormii Sacc., Nuovo Giorn. Bot. Ital. n.s. 22: 67. 1915. than those of that the latter species - conidia in the C. acutatum = Cryptosporium rhodocyclum Mont. ex Almeida & Souza da Camara, Bol. Soc. Brot. 25: 190. 1909. species complex are rarely wider than 5 µm (Table 2). No cultures ≡ Gloeosporidium rhodocyclum (Mont. ex Almeida & Souza da Camara) are available to allow evaluation of the synonymy. Höhn., Annls mycol. 18(1/3): 92. 1920. Another species on banana was described by Sawada (1959), ≡ Colletotrichum rhodocyclum (Mont. ex Almeida & Souza da Camara) C. liukiuensis, on leaves of Musa liukiuensis in Taiwan. The conidia Petr., Annls mycol. 25(3/4): 251. 1927. = Physalospora phormii J. Schröt., in Cohn, Krypt.-Fl. Schlesien (Breslau) of this species are described as ellipsoid or oblong-ellipsoid with 3.2(3): 347. 1894. rounded ends, measuring 12–14 × 4.8–5.5 µm. The fungus forms ≡ Hypostegium phormii (J. Schröt.) Theiss., Verh. zool.-bot. Ges. Wien dark brown 1–2-septate setae, which seem to be prominent, 66: 384. 1916. because they were included in the sketchy drawing (Pl. II: 30-31 ≡ Glomerella phormii (J. Schröt.) D.F. Farr & Rossman, Mycol. Res. 110(12): 1403. 2006. of the publication) Sawada provided. This drawing showed a seta present as well as conidia with broadly rounded ends. Together with the width of the conidia, these characters exclude the name Sexual morph not observed. Asexual morph on SNA. Vegetative of this fungus from contention as an earlier synonym of C. paxtonii. hyphae 1–5 µm diam, hyaline, smooth-walled, septate, branched. Additional species on Musa have been described in Chlamydospores not observed. Conidiomata absent, conidiophores formed directly on hyphae. Setae not observed. Conidiophores Gloeosporium. Gloeosporium musarum Cooke & Massee has hyaline to very pale brown, smooth-walled to finely verruculose, elongate-ellipsoidal conidia with both ends rounded, measuring 12 86 The CotriC ollet hum aCtum a ut species complex Fig. 23. Colletotrichum phormii (from ex-epitype strain CBS 118194). A–B. Conidiomata. C. Seta. D–G. Conidiophores. H–L. Appressoria. M–N. Conidia. A, C–D, M. from Anthriscus stem. B, E–L, N. from SNA. A–B. DM, C–N. DIC, Scale bars: A = 100 µm, D = 10 µm. Scale bar of A applies to A–B. Scale bar of D applies to C–N. simple or septate and branched, to 40 µm in length. Conidiogenous conidia of most other strains are slightly broader and those of strain CBS 118191 are additionally shorter than conidia of the ex-epitype cells hyaline to pale brown, smooth-walled to finely verruculose, strain, measuring (14–)18.5–22(–24) × (4–)4.5–5(–5.5) µm, mean cylindrical, elongate ampulliform to ampulliform, 7.5–16.5 × 2.2– ± SD = 20.3 ± 1.9 × 4.9 ± 0.4 µm, L/W ratio = 4.1. 4.5 µm, opening 1–1.5 µm diam, collarette 1–2 µm long, periclinal thickening visible. Conidia hyaline, smooth-walled or verruculose, aseptate, straight, cylindrical to fusiform with both ends acute or Culture characteristics: Colonies on SNA flat with entire margin, one end round and one end acute, (17–)20–26(–35.5) × 4–5(–6.5) hyaline with felty white aerial mycelium on Anthriscus stem and µm, mean ± SD = 23.0 ± 3.2 × 4.6 ± 0.6 µm, L/W ratio = 5.1. filter paper, filter paper on both sides partially olivaceous to pale Appressoria single or in loose groups, medium to dark brown, olivaceous grey; growth rate 15–19 mm in 7 d (27.5–32.5 mm in outline mostly oblong to irregular, the edge entire or undulate, 10 d). Colonies on OA flat with entire margin; surface buff, with olivaceous to grey olivaceous sectors, and roundish olivaceous rarely lobate, (4–)8.5–20.5(–32) × (2.5–)4–6(–8) µm, mean ± SD grey structures embedded in the medium, surface partly covered = 14.5 ± 6.2 × 5.1 ± 1.0 µm, L/W ratio = 2.9, appressoria of strain with floccose-felty white to pale olivaceous grey aerial mycelium, CBS 102054 are shorter, measuring (5.5–)8–13(–14.5) × 5–6.5(–8) reverse buff with pale to dark olivaceous grey sectors; growth rate µm, mean ± SD = 10.4 ± 2.4 × 5.8 ± 0.8 µm, L/W ratio = 1.8. 15–21 mm in 7 d (27.5–33.5 mm in 10 d). Conidia in mass salmon. Asexual morph on Anthriscus stem. Conidiomata acervular, conidiophores and setae formed on a cushion of pale brown Material examined: Germany, Berlin, Botanical garden, Kalthaus, from Phormium roundish to angular cells, 2.5–10 µm diam. Setae few, hyaline to tenax, Apr. 1889, P. Hennings, (B 70 0005220 holotype of Fusarium phormii [not medium brown, smooth-walled, 0–1-septate, 25–70 µm long, base seen]); APHIS interception Port Orlando 007160, from Phormium sp., 6 Nov. 2000, cylindrical, to 5 µm diam, tip ± roundish to ± acute. Conidiophores W. Sheta, (CBS-H 20720 epitype, here designated, culture ex-epitype CBS 118194 = AR 3546). New Zealand, Auckland, Blockhouse Bay, from leaf spot of Phormium pale brown, smooth-walled, septate, branched, to 50 µm sp., Jun. 1999, C.F. Hill, culture CBS 102054; from leaf of Phormium sp., APHIS long. Conidiogenous cells pale brown, smooth-walled, usually interception Los Angeles, California 134866, 1 May 1997, M.A. Abdelshife, culture cylindrical, sometimes elongate ampulliform to ampulliform , 8–25 CBS 118197 = AR 3389; APHIS interception Los Angeles, California 105828), from × 2.5–3.5(–5.5) µm, opening 1–1.5 µm diam, collarette 1 µm leaf of Phormium sp., 4 May 1993, N. Suzuki, culture CBS 118201 = MEP 1334; from Phormium tenax, unknown collection date and collector (deposited in CBS 1 long, periclinal thickening visible. Conidia hyaline, smooth-walled, Aug. 198), culture CBS 483.82. South Africa, from leaf of Phormium sp., APHIS aseptate, straight, cylindrical to fusiform with both ends acute, interception Miami, Florida, 223143, 26 Feb. 2002, H. Ruiz, culture CBS 118191 (14–)20–24.5(–25.5) × 4–4.5(–5) µm (one conidium measured 47 = AR 3787. Netherlands, from leaf of Phormium sp., unknown collection date and collector, culture CBS 124953. × 5 µm), mean ± SD = 22.3 ± 2.3 × 4.3 ± 0.2 µm, L/W ratio = 5.2, www.studiesinmycology.org 87 Damm et al . Table 2. Conidia measurements of Colletotrichum strains studied. Species Accession No. Conidia on SNA Conidia on Anthriscus stem 2 2 length × width (µm) length × width (µm) L/W ratio length × width (µm) length × width (µm) L/W ratio mean ± stdev mean ± stdev C. acerbum CBS 128530* 15.5–20.5(–29) × (4–)4.5–5 17.9 ± 2.4 × 4.7 ± 0.2 3.8 (12.5–)15–18.5(–20.5) × (4–)4.5–5 16.8 ± 1.7 × 4.7 ± 0.3 3.6 C. acutatum CBS 112996* (7.5–)11–14.5(–19) × 3.5–4(–4.5) 12.6 ± 1.8 × 3.9 ± 0.3 3.2 (8.5–)12–16.5(–17.5) × (3–)3.5–4.5(–5) 14.3 ± 2.1 × 4.1 ± 0.4 3.5 CBS 111993 (10.5–)12–16(–20) × (3–)3.5–4.5(–5) 14.0 ± 1.8 × 4.0 ± 0.5 3.5 (12.5–)14–17(–18) × (3.5–)4–4.5(–5) 15.5 ± 1.3 × 4.2 ± 0.3 3.7 CBS 127602 (8–)11.5–14.5(–15) × (2.5–)3.5–4 13.0 ± 1.5 × 3.8 ± 0.4 3.5 (8–)12.5–18.5(–22) × 4–4.5 15.5 ± 2.9 × 4.2 ± 0.3 3.7 CBS 112990 (8.5–)12.5–15.5(–17.5) × (2.5–)4–5 14.1 ± 1.6 × 4.3 ± 0.5 3.3 (8.5–)11.5–15.5(–17) × (3.5–)4–4.5(–5) 13.5 ± 1.8 × 4.2 ± 0.3 3.2 CBS 129915 (7–)12–15.5(–16.5) × (3.5–)4–4.5(–5) 13.8 ± 1.9 × 4.1 ± 0.3 3.3 (6.5–)11–14.5(–15.5) × (3.5–)4–4.5(–5) 12.8 ± 2.0 × 4.3 ± 0.3 2.9 CBS 112759 (6.5–)8.5–12(–13) × (2.5–)3–4 10.3 ± 1.9 × 3.4 ± 0.5 3.1 (8–)11–15(–19) × (3–)4–5 12.9 ± 1.9 × 4.5 ± 0.4 2.9 CBS 112761 (7.5–)10–15.5(–20.5) × (3–)3.5–4.5(–6) 12.7 ± 2.7 × 4.1 ± 0.5 3.1 CBS 370.73 (5–)6.5–11(–12.5) × (2–)2.5–3.5(–4.5) 8.8 ± 2.1 × 3.2 ± 0.5 2.7 CBS 797.72 (6–)8.5–13(–18) × 3.5–4.5(–5) 10.8 ± 2.3 × 4.0 ± 0.3 2.7 (5.5–)10–14(–15.5) × (3–)4–5 12.0 ± 2.2 × 4.4 ± 0.5 2.7 CBS 110735 (7.5–)11–16.5(–21) × (3–)3.5–4(–4.5) 13.7 ± 2.5 × 3.8 ± 0.4 3.6 (12.5–)14–17(–17.5) × (3.5–)4–4.5(–5) 15.5 ± 1.5 × 4.4 ± 0.3 3.5 CBS 112979 (7.5–)9–13(–15) × (2–)3–3.5(–4) 11 ± 2.0 × 3.3 ± 0.4 3.3 (9–)10.5–15.5(–16.5) × (3–)3.5–4.5(–5) 13.1 ± 2.4 × 4.2 ± 0.5 3.1 CBS 979.69 (5–)8.5–14.5(–16.5) × (2.5–)3–4(–4.5) 11.5 ± 3.1 × 3.5 ± 0.4 3.3 (12–)13–15.5(–17) × (3.5–)4–4.5(–5) 14.1 ± 1.3 × 4.1 ± 0.3 3.4 IMI 319423 (8–)11.5–14.5(–16) × (3–)3.5–4.5 13.2 ± 1.5 × 4.0 ± 0.3 3.3 (7.5–)11.5–15.5(–19.5) × (3–)3.5–4.5 13.6 ± 2.0 × 4.0 ± 0.4 3.4 C. australe CBS 116478* (10–)14.5–19.5(–25) × (3.5–)4–5(–6) 17.0 ± 2.4 × 4.4 ± 0.5 3.9 (16–)17–20(–22) × (4–)4.5–5(–5.5) 18.6 ± 1.6 × 4.7 ± 0.4 4.0 CBS 131320 (14–)15–19(–26) × (3.5–)4–5(–5.5) 17.0 ± 2.0 × 4.5 ± 0.3 3.8 (13.5–)15–17.5(–18) × (3.5–)4–5(–5.5) 16.3 ± 1.1 × 4.4 ± 0.4 3.7 C. brisbanense CBS 292.67* (12–)12–17.5(–25) × (3–)3.5–4(–5) 14.8 ± 2.8 × 3.8 ± 0.5 3.9 (9.5–)12–15(–17) × (3–)3.5–4 13.5 ± 1.4 × 3.9 ± 0.3 3.5 C. chrysanthemi CBS 126518 (6–)7–9.5(–12) × (3–)4–5.5(–6) 8.3 ± 1.3 × 4.8 ± 0.6 1.7 (3.5–)6.5–10.5(–13.5) × (3.5–)4–5(–5.5) 8.5 ± 1.8 × 4.5 ± 0.5 1.9 CBS 126518 (3.5–)4.5–9(–15) × 3–5(–6.5) 6.7 ± 2.3 × 4.1 ± 0.8 1.6 CBS 126519 (4–)5–10(–14) × (3–)3.5–5(–6) 7.4 ± 2.6 × 4.1 ± 0.6 1.8 (6.5–)8–10.5(–14.5) × (3–)4–5(–5.5) 9.2 ± 1.4 × 4.5 ± 0.4 2.0 IMI 364540 (4.5–)6.5–13(–26) × (3–)3.5–5(–11) 9.8 ± 3.2 × 4.3 ± 0.9 2.3 (5–)6.5–12.5(–21) × (2–)3.5–5(–6) 9.4 ± 2.9 × 4.3 ± 0.7 2.2 C. cosmi CBS 853.73* (7–)13–18.5(–19.5) × (3–)3.5–4.5 15.8 ± 2.5 × 4.0 ± 0.4 4.0 (12–)14–16.5(–18) × (3.5–)4–4.5 15.3 ± 1.4 × 4.0 ± 0.3 3.8 C. costaricense CBS 330.75* (9–)11.5–18(–28) × (3–)3.5–4(–4.5) 14.6 ± 3.1 × 3.7 ± 0.3 4.0 12.5–)13.5–16(–18) × 3.5–4 14.8 ± 1.4 × 3.8 ± 0.3 3.9 CBS 211.78 (11.5–)12–16(–20) × (3.5–)4–4.5 13.9 ± 1.9 × 4.3 ± 0.2 3.2 (12–)14–16.5(18.5) × (3.5–)4–4.5 15.2 ± 1.4 × 4.2 ± 0.2 3.6 C. cuscutae IMI 304802* (15.5–)17.5–21(–22.5) × (3–)3.5–4.5 19.2 ± 1.7 × 4.0 ± 0.3 4.8 (15–)17–20(–21) × (3.5–)4–4.5 18.6 ± 1.5 × 4.2 ± 0.2 4.5 C. fioriniae CBS 128517* (10–)13.5–16.5(–19.5) × 4–5(–5.5) 15.0 ± 1.6 × 4.5 ± 0.3 3.3 (12.5–)14–18.5(–24.5) × 4–5 16.1 ± 2.2 × 4.4 ± 0.4 3.6 CBS 200.35 (8–)10.5–17.5(–30.5) × 3.5–5(–6.5) 14.1 ± 3.4 × 4.3 ± 0.6 3.3 (9–)12.5–17.5(–23) × (3.5–)4–5 15.0 ± 2.3 × 4.4 ± 0.4 3.4 CBS 127599 (7.5–)12–16.5(–17) × (2.5–)4–5(–5.5) 14.4 ± 2.4 × 4.5 ± 0.6 3.2 (10.5–)13.5–17(–17.5) × (3.5–)4–5 15.1 ± 1.7 × 4.4 ± 0.4 3.4 CBS 129916 (6.5–)11.5–16 × (3–)3.5–4.5(–5) 13.8 ± 2.2 × 3.9 ± 0.4 3.5 (10–)13–16.5(–18) × (4–)4.5–5(–5.5) 14.8 ± 1.7 × 4.7 ± 0.3 3.2 CBS 127601 (4.5–)10.5–18(–20) × (3.5–)4–5(–5.5) 14.2 ± 4.0 × 4.5 ± 0.4 3.2 (7–)13.5–18.5(–19) × (3.5–)4–4.5(–5) 15.9 ± 2.3 × 4.4 ± 0.4 3.6 CBS 129947 (10.5–)12–15(–17) × 3.5–5(–6) 13.5 ± 1.7 × 4.1 ± 0.8 3.3 (13–)14–16(–17) × (3.5–)4–4.5(–5) 15.0 ± 1.0 × 4.3 ± 0.4 3.5 CBS 293.67 (8.5–)12.5–16(–17.5) × (3–)3.5–4.5(–5) 14.4 ± 1.7 × 4.0 ± 0.5 3.6 (13–)14–16.5(–18) × (4–)4.5–5(–5.5) 15.2 ± 1.3 × 4.7 ± 0.3 3.2 C. godetiae CBS 133.44* (7–)10.5–14.5(–15.5) × (3.5–)4–5(–5.5) 12.4 ± 2.0 × 4.3 ± 0.5 2.9 (9.5–)10.5–15(–20.5) × 4–5 12.8 ± 2.3 × 4.5 ± 0.4 2.8 CBS 125972 (5.5–)12–16.5(–17) × (3.5–)4–4.5(–5) 14.2 ± 2.2 × 4.3 ± 0.4 3.3 (13.5–)14–16(–17) × (4–)4.5–5 15.1 ± 0.9 × 4.7 ± 0.3 3.2 The CotriC ollet hum aCtum a ut species complex www.studiesinmycology.org Table 2. (Continued). Species Accession No. Conidia on SNA Conidia on Anthriscus stem 2 2 length × width (µm) length × width (µm) L/W ratio length × width (µm) length × width (µm) L/W ratio mean ± stdev mean ± stdev C. godetiae CBS 193.32 (8–)11.5–15(–19.5) × (2.5–)3.5–4.5(–5) 13.2 ± 1.9 × 4.2 ± 0.5 3.1 (6.5–)9.5–14(–15.5) × (3–)3.5–4.5(–5.5) 11.8 ± 2.2 × 4.1 ± 0.6 2.9 CBS 129911 (10.5–)12.5–15.5(–17.5) × (3–)4–5(–6.5) 13.9 ± 1.4 × 4.5 ± 0.6 3.1 (7–)9–13(–15.5) × (2.5–)3–4 11.0 ± 2.0 × 3.5 ± 0.3 3.1 CBS 862.70 (8–)14–19(–24) × (4–)4.5–5(–5.5) 16.4 ± 2.4 × 4.9 ± 0.4 3.4 (12.5–)15.5–18(–19.5) × 4.5–5(5.5) 16.8 ± 1.4 × 4.9 ± 0.2 3.4 CBS 129809 (10.5–)13.5–17(–22.5) × (3.5–)4–5(–5.5) 15.3 ± 1.9 × 4.4 ± 0.3 3.4 (14–)14–17.5(–23) × 4–4.5(–5) 15.8 ± 1.6 × 4.4 ± 0.3 3.6 CBS 129816 (13–)13.5–16.5(–20.5) × 4–4.5(–5) 15.1 ± 1.4 × 4.4 ± 0.3 3.4 (13–)14–16(–17.5) × 4.5–5 15.1 ± 1.1 × 4.7 ± 0.2 3.2 CBS 127561 (12.5–)14–15.5(–16.5) × 4.5–5(–5.5) 14.7 ± 0.9 × 4.9 ± 0.3 3.0 (11.5–)13.5–17.5(–20) × (4–)4.5–5.5 15.5 ± 1.8 × 5.0 ± 0.4 3.1 CBS 129917 (8–)10–15(–18.5) × 3–4.5(–5.5) 12.5 ± 2.3 × 3.8 ± 0.6 3.3 (9.5–)13–16(–17) × (4–)4.5–5.5(–6) 14.6 ± 1.5 × 4.9 ± 0.5 3.0 C. guajavae IMI 350839* (6–)10.5–16.5(–23.5) × (2.5–)3–4(–5) 13.4 ± 3.0 × 3.5 ± 0.5 3.8 (11–)13–16(–17) × (3–)3.5–4 14.6 ± 1.7 × 3.8 ± 0.3 3.9 C. indonesiense CBS 127551* (8–)10–14.5(–18) × (2.5–)3.5–4(–4.5) 12.3 ± 2.4 × 3.8 ± 0.3 3.2 (10.5–)13–17.5(–19) × (3–)3.5–4 15.4 ± 2.2 × 3.7 ± 0.2 4.1 C. johnstonii CBS 128532* (13.5–)14.5–19(–21.5) × (3.5–)4.5–5(–6) 16.7 ± 2.1 × 4.7 ± 0.4 3.6 (14.5–)15.5–17(–18) × 4.5–5(–5.5) 16.3 ± 1.0 × 4.9 ± 0.3 3.3 IMI 357027 (13–)14.5–17(–19) × (4–)4.5–5(–5.5) 15.6 ± 1.3 × 4.7 ± 0.3 3.3 (8.5–)14.5–17.5(–19) × (3–)4–5 15.9 ± 1.6 × 4.6 ± 0.4 3.8 C. kinghornii CBS 198.35* (11–)15.5–21(–22.5) × (3–)3.5–4(–4.5) 18.3 ± 2.9 × 3.8 ± 0.4 4.9 (15–)16–20.5(–23) × 3.5–4.5 18.1 ± 2.3 × 4.0 ± 0.4 4.6 C. laticiphilum CBS 112989* (9.5–)13.5–19.5(–25.5) × (3–)3.5–4(–4.5) 16.6 ± 3.1 × 3.8 ± 0.4 4.4 (10–)12–15(–19.5) × 4–5(–5.5) 13.6 ± 1.7 × 4.5 ± 0.3 3.0 CBS 129827 (5–)8–15(–18.5) × (1.5–)2.5–4.5(–5.3) 11.5 ± 3.4 × 3.6 ± 0.9 3.2 (10–)12.5–17.5(–20) × 4–4.5(–5) 15.1 ± 2.5 × 4.4 ± 0.3 3.4 C. limetticola CBS 114.14* (9–)12–20.5(–29) × (3–)4–5(–6) 16.3 ± 4.2 × 4.5 ± 0.6 3.6 (12–)13–18(–24) × (3.5–)4–4.5(–5.5) 15.5 ± 2.3 × 4.3 ± 0.4 3.6 C. lupini CBS 109225* 9–15(–26.5) × (3–)3.5–4.5(–6) 12.0 ± 3.2 × 4.1 ± 0.6 2.9 (10–)12.5–16(–18.5) × (3–)3.5–4.5 14.2 ± 1.7 × 4.0 ± 0.3 3.6 IMI 375715 (7.5–)9.5–16(–25) × 3.5–5(–6.5) 12.8 ± 3.3 × 4.3 ± 0.6 3.0 (10–)11.5–15(–17) × (3.5–)4–4.5(–5) 13.3 ± 1.8 × 4.2 ± 0.3 3.1 CBS 109221 11.5–15.5(–19) × (3.5–)4–4.5(–5) 13.5 ± 1.9 × 4.3 ±0 .4 3.2 (11.5–)13.5–16.5(–18.5) × (3.5–)4–4.5 15.0 ± 1.5 × 4.3 ± 0.3 3.5 C. melonis CBS 159.84* (7–)9–16.5(–23.5) × (3–)3.5–4.5(–5) 12.8 ± 3.6 × 3.9 ± 0.4 3.3 (9–)12–17(–20) × (3.5–)4–4.5(–5) 14.5 ± 2.3 × 4.2 ± 0.3 3.5 C. nymphaeae CBS 173.51 (6–)9.5–13.5(–15) × (2–)3–4.5 11.5 ± 1.8 × 3.7 ± 0.5 3.1 (7.5–)10–14.5(–16) × (3–)3.5–4.5 12.3 ± 2.0 × 3.9 ± 0.4 3.2 CBS 112992 (5.5–)8–14.5(–20.5) × (2.5–)3–4(–4.5) 11.2 ± 3.4 × 3.5 ± 0.5 3.2 (7.5–)11–16(–20) × (2.5–)3.5–4(–4.5) 13.6 ± 2.7 × 3.8 ± 0.4 3.6 CBS 126372 (9.5–)13–17.5(–21.5) × (2.5–)3.5–4.5(–5.5) 15.3 ± 2.4 × 3.9 ± 0.7 3.9 (12.5–)13.5–17(–18.5) × (3.5–)4–4.5 15.3 ± 1.7 × 4.2 ± 0.3 3.7 CBS 112202 (10–)14–17(–18.5) × (3–)4–4.5 15.7 ± 1.6 × 4.1 ± 0.3 3.8 (12–)13.5–17.5(–19.5) × (3.5–)4(–4.5) 15.5 ± 1.8 × 4.0 ± 0.2 3.9 CBS 126382 (3–)7.5–14(–17.5) × 3–4(–5) 10.8 ± 3.4 × 3.6 ± 0.5 3.0 (11–)12.5–16(–18) × (3–)3.5–4.5 14.4 ± 1.8 × 4.0 ± 0.3 3.6 CBS 515.78* (10–)14–18.5(–19.5) × (3–)4–5.5(–6) 16.1 ± 2.3 × 4.9 ± 0.7 3.3 (12.5–)14–18.5(–22.5) × (4–)4.5–5.5(–6) 16.3 ± 2.1 × 4.8 ± 0.5 3.4 CBS 526.77 (8.5–)9–13(–16) × (3–)3–4.5(–5) 11.0 ± 2.0 × 3.8 ± 0.6 2.9 (9.5–)13.5–19(–21.5) × (3.5–)5–6(–6.5) 16.1 ± 2.7 × 5.6 ± 0.7 2.9 C. orchidophilum CBS 632.80* (10.5–)11.5–14(–16.5) × (2–)3–3.5(–4) 12.7 ± 1.1 × 3.1 ± 0.3 4.1 (11.5–)12.5–14(–15.5) × (2.5–)3–3.5(–4) 13.2 ± 0.9 × 3.3 ± 0.3 4.0 IMI 305357 (8.5–)11.5–17(–25) × (1.5–)2.5–4(–4.5) 14.2 ± 2.7 × 3.3 ± 0.6 4.4 (10–)12–14.5(–15) × 3–3.5(–4) 13.3 ± 1.0 × 3.5 ± 0.3 3.8 CBS 119291 (13.5–)14–15.5(–16) × 3–3.5(–4) 14.8 ± 0.7 × 3.3 ± 0.3 4.5 (10.5–)11.5–13.5(–14.5) × 3–4 12.7 ± 1.0 × 3.5 ± 0.3 3.6 CBS 631.80 (13–)13.5–17.5(–19) × 2.5–3.5 15.4 ± 2.1 × 3.0 ± 0.3 5.1 (10.5–)11.5–13.5(–14.5) × (3–)3.5–4 12.4 ± 0.9 × 3.6 ± 0.3 3.4 C. paxtonii IMI 165753* (5–)10.5–15.5(–19.5) × (2.5–)3.5–4(–4.5) 13.0 ± 2.6 × 3.7 ± 0.3 3.5 (6.5–)12–15.5(–17) × (3–)3.5–4 13.7 ± 1.8 × 3.8 ± 0.3 3.6 C. phormii CBS 118194* (17–)20–26(–35.5) × 4–5(–6.5) 23.0 ± 3.2 × 4.6 ± 0.6 5.1 (14–)20–24.5(–25.5) × 4–4.5(–5) 22.3 ± 2.3 × 4.3 ± 0.2 5.2 CBS 102054 (180.5–)20–24(–29) × (4–)4.5–5(–5.5) 22.1 ± 2.1 × 4.8 ± 0.4 4.6 (19–)20.5–24(–25) × (4–)4.5–5.5 22.2 ± 1.6 × 4.9 ± 0.4 4.5 CBS 118197 19.5–25(–33.4) × (3.5–)4–5(–6) 22.3 ± 2.6 × 4.5 ± 0.4 5.0 21.5–26(–30) × (4–)4.5–5(–6) 23.7 ± 2.1 × 4.9 ± 0.4 4.9 Damm et al . Table 2. (Continued). Species Accession No. Conidia on SNA Conidia on Anthriscus stem 2 2 length × width (µm) length × width (µm) L/W ratio length × width (µm) length × width (µm) L/W ratio mean ± stdev mean ± stdev C. phormii CBS 118201 (21–)21.5–24(–24.5) × 4–4.5 22.9 ± 1.2 × 4.4 ± 0.3 5.2 (20–)20.5–23.5(–25) × 4.5–5(–5.5) 21.9 ± 1.4 × 4.8 ± 0.2 4.5 CBS 118191 (18–)18.5–30(–39.5) × (3–)3.5–4.5(–5) 24.1 ± 5.5 × 4.2 ± 0.3 5.7 (14–)18.5–22(–24) × (4–)4.5–5(–5.5) 20.3 ± 1.9 × 4.9 ± 0.4 4.1 CBS 124953 (13.5–)18–26.5(–28) × 4–4.5(–5) 22.3 ± 4.2 × 4.4 ± 0.3 5.0 (20.5–)21–23(–23.5) × 4.5–5 22.0 ± 1.2 × 4.9 ± 0.2 4.5 CBS 483.82 (18–)19–28(–33.5) × 4–5(–6.5) 23.3 ± 4.5 × 4.5 ± 0.6 5.2 (19–)20–22(–23) × 4.5–5(–5.5) 20.9 ± 1.0 × 4.7 ± 0.3 4.4 C. pseudoacutatum CBS 436.77* (9.5–)11.5–13.5(–14.5) × 3.5–4 12.7 ± 1.1 × 3.8 ± 0.2 3.4 (9.5–)11.5–13.5(–14.5) × 3.5–4 15.0 ± 1.2 × 4.2 ± 0.3 3.5 C. pyricola CBS 128531* (10–)14.5–18.5(–24) × (3.5–)4.5–5(–5.5) 16.7 ± 2.1 × 4.7 ± 0.4 3.5 (9.5–)14–17(–18.5) × (4–)4.5–5(–5.5) 15.4 ± 1.6 × 4.8 ± 0.4 3.2 C. rhombiforme CBS 129953* (12–)12.5–17(–24) × (4–)4.5–5.5(–6) 14.7 ± 2.1 × 5.0 ± 0.7 2.9 (7.5–)10.5–17.5(–21) × (3.5–)4–5.5(–6) 14.1 ± 3.5 × 4.8 ± 0.6 2.9 C. salicis CBS 607.94* (8.5–)10.5–15.5(–19.5) × (3.5–)3–4.5(–5) 13.0 ± 2.4 × 4.0 ± 0.5 3.2 (14.5–)16–18.5(–20) × (4–)4.5–5(–5.5) 17.1 ± 1.3 × 4.9 ± 0.3 3.5 CBS 115.14 (9–)10.5–15(–17) × 2.5–3.5(–4) 12.7 ± 2.3 × 3.1 ± 0.5 4.1 (9.5–)11.5–16(–18.5) × (2.5–)3–4(–4.5) 14.0 ± 2.3 × 3.3 ± 0.4 4.2 CBS 465.83 (7.5–)9.5–15.5(–22) × 3–3.5(–4.5) 12.4 ± 3.1 × 3.3 ± 0.4 3.8 not observed C. scovillei CBS 126529* (10.5–)12.5–15(–16.5) × (3–)3.5–4(–4.5) 13.7 ± 1.3 × 3.8 ± 0.3 3.6 (9–)14.5–18(–19.5) × 3.5–4.5 16.0 ± 1.8 × 4.0 ± 0.3 4.0 CBS 120708 (11.5–)12.5–14.5(–15) × 3–3.5 13.5 ± 0.8 × 3.3 ± 0.2 4.1 (12.5–)13–16(–18) × (3–)3.5–4 14.6 ± 1.4 × 3.6 ± 0.3 4.1 C. simmondsii CBS 122122* (4.5–)6.5–10(–11.5) × (2–)2.5–3.5(–4) 8.1 ± 1.7 × 2.9 ± 0.4 2.7 (6–)7–10(–12.5) × (2–)2.5–3.5(–4.5) 8.4 ± 1.5 × 3.0 ± 0.5 2.8 CBS 294.67 (6–)10.5–14(–16.5) × 3.5–4.5(–5.5) 12.3 ± 1.8 × 4.0 ± 0.4 3.0 (11–)12–14.5(–15.5) × (3–)4–4.5(–5) 13.3 ± 1.2 × 4.1 ± 0.4 3.2 CBS 114494 (6–)9.5–14.5(–15.5) × (2.5–)3–4(–4.5) 12.1 ± 2.7 × 3.6 ± 0.5 3.3 (10–)13–17(–18) × (3–)3.5–4.5(–5) 14.9 ± 1.9 × 3.8 ± 0.4 3.9 IMI 354381 (8.5–)11–15(–16) × (3.5–)4–4.5 13.0 ± 1.8 × 4.2 ± 0.2 3.1 (12–)13.5–17(–19) × (3.5–)4–4.5(–5) 15.4 ± 1.7 × 4.2 ± 0.3 3.7 C. sloanei IMI364297* (8.5–)12–17(–22) × (3–)3.5–4(–4.5) 14.4 ± 2.5 × 3.7 ± 0.3 3.9 (9–)11.5–15.5(–19.5) × (3–)3.5–4(–4.5) 13.4 ± 1.8 × 3.9 ± 0.3 3.5 C. tamarilloi CBS 129814* (8.5–)11.5–14.5(–15) × (2.5–)3–4(–4.5) 13.0 ± 1.4 × 3.5 ± 0.4 3.7 (10.5–)12–16(–22) × (3–)3.5–4.5(–5) 14.0 ± 1.9 × 4.0 ± 0.4 3.5 CBS 129811 (9.5–)12–15.5(–19.5) × (3–)3.5–4(–4.5) 13.7 ± 1.6 × 3.7 ± 0.3 3.7 (12.5–)13.5–16.5(–17.5) × (3–)3.5–4 15.1 ± 1.4 × 3.8 ± 0.3 4.0 CBS 129955 (10.5–)11.5–14.5(–17.5) × 3–4(–5) 13.2 ± 1.5 × 3.6 ± 0.4 3.6 (11.5–)13.5–17(–18.5) × 3.5–4(–4.5) 15.3 ± 1.7 × 3.8 ± 0.3 4.0 C. walleri CBS 125472* (6–10.5)15.5–(–19.5) × (3–)3.5–4.5(–5.5) 13.0 ± 2.7 × 4.0 ± 0.5 3.3 (10.5–)12–16(–18.5) × 3.5–4(–4.5) 13.9 ± 1.8 × 4.0 ± 0.3 3.5 Colletotrichum sp. CBS 129821 (9–)12–14.5(–15.5) × (3–)3.5–4.5(–5.5) 13.2 ± 1.4 × 4.0 ± 0.5 3.3 (10–)13–17(–20) × 3.5–4(–4.5) 14.9 ± 2.0 × 4.0 ± 0.2 3.8 CBS 129820 (9.5–)11–15(–19.5) × (2.5–)3.5–4(–4.5) 13.1 ± 1.9 × 3.7 ± 0.4 3.5 (9.5–)12–14.5(–16) × (3–)4–4.5 13.3 ± 1.3 × 4.0 ± 0.2 3.3 CBS 129823 (7–)10.5–15.5(–18) × (2.5–)3–4(–4.5) 13.1 ± 2.3 × 3.5 ± 0.6 3.7 (9–)12–15.5(–17) × (2.5–)3.5–4(–4.5) 14.0 ± 1.8 × 3.8 ± 0.4 3.7 IMI 384185 (9–)12–14(–14.5) × (2.5–)3–4(–4.5) 12.3 ± 1.5 × 3.6 ± 0.4 3.4 (6–)10–16.5(–19.5) × (3–)3.5–4.5(–6) 13.5 ± 3.2 × 4.0 ± 0.6 3.4 CBS 101611 (13–)15–19(–22) × (3.5–)4–5(–5.5) 16.9 ± 2.0 × 4.5 ± 0.4 3.7 (14–)16.5–20(–23.5) × (4–)4.5–5(–5.5) 18.3 ± 1.8 × 4.6 ± 0.3 4.0 CBS 129810 (12.5–)13–17(–23.5) × (2.5–)3.5–4(–4.5) 15.1 ± 2.1 × 3.9 ± 0.3 3.9 (7.5–)9.5–12.5(–15) × 2.5–3.5(–4) 10.8 ± 1.5 × 2.9 ± 0.5 3.7 *ex-type strain aerial mycelium (min–)min-stdev–max-stdev(–max) The CotriC ollet hum aCtum a ut species complex Notes: The synonymy given for this species follows Farr et al. Colletotrichum pseudoacutatum Damm, P.F. Cannon & (2006), and this work should be consulted for details. Fusarium Crous, sp. nov. MycoBank MB800509. Fig. 24. phormii was described by Hennings (1898) on leaves of Phormium tenax in the Botanical Garden in Berlin, Germany, as forming Etymology: Named refers to the morphology that is similar to C. sporodochia with oblong-cylindrical to fusoid, straight to slightly acutatum, which is not closely related. curved, multiguttulate, hyaline conidia, measuring 18–25 × 4–6 µm. Hennings (1898) found this fungus together with Physalospora Sexual morph not observed. Asexual morph on SNA. Vegetative phormii, and assumed the two belonged together. Fusarium phormii hyphae 1–5 µm diam, hyaline to pale brown, smooth-walled, is formed on the leaf surface, while the perithecia of P. phormii septate, branched. Chlamydospores not observed. Conidiomata appear on the undersurface. Kinghorn (1936) observed structures acervular, conidiophores and setae formed on a cushion of pale considered to be the sexual morph of C. phormii on leaves of brown angular cells 3–8 µm diam. Setae rare (only one found), Phormium plants but not in culture, as did von Arx (in litt.). We have medium brown, smooth-walled, 2-septate, 57 µm long, base found, however, that Kinghorn was looking at two species; part cylindrical, constricted at basal septum, 4 µm diam, tip somewhat of this material belongs to a species that is named in the present round. Conidiophores hyaline to pale brown, smooth-walled, publication as C. kinghornii. The sexual morph, originally named septate, branched, to 50 µm long. Conidiogenous cells hyaline, as Physalospora phormii, was originally found by Schröter (1894) smooth-walled, cylindrical, often ± bent or partly inflated, 9–22 × on dead leaves of Phormium tenax in Breslau, Germany (today: 2–3.5 µm, opening 1 µm diam, collarette distinct, 0.5–1 µm long, Wrocław, Poland). periclinal thickening conspicuous. Conidia hyaline, smooth-walled, The sexual morph was not observed in our study. Farr et aseptate, straight, fusiform to cylindrical with both ends acute, al. (2006) gave the following description: “Ascomata on upper (9.5–)11.5–13.5(–14.5) × 3.5–4 µm, mean ± SD = 12.7 ± 1.1 × 3.8 and lower surface of leaves in large, elliptical, discoloured areas ± 0.2 µm, L/W ratio = 3.4. Appressoria in loose groups to dense similar to those bearing acervuli, with or without a narrow, black clusters, pale brown, verruculose, irregular shape, (3–)5.5–18.5(– margin, subepidermal, sometimes partially erumpent, solitary, 25) × (2.5–)3.5–7(–9.5) µm, mean ± SD = 12.0 ± 6.3 × 5.1 ± 1.7 scattered to crowded or aggregated, black, shiny when exposed, µm, L/W ratio = 2.3. globose to ellipsoid, flattened. Ascomatal walls of thin-walled, Asexual morph on Anthriscus stem. Conidiomata acervular, brown cells, 9–15 µm diam. Paraphyses sparse, inflated, hyaline. conidiophores and setae formed on a cushion of pale brown Asci unitunicate, narrowly clavate with a rounded apex and short angular cells 4–10 µm diam. Setae abundant, medium brown, stipe, 56–70 × 15–20 µm, with an indistinct apical ring in immature basal cell often paler, smooth-walled, 65–130 µm long, mostly with asci, 8-spored, obliquely seriate. Ascospores hyaline, non-septate, one septum close to the base, (0–)1(–2)-septate, base cylindrical ellipsoidal, 15–22 × 4.5–6 µm.” to conical, often ± bent, often looking like an outgrowth or like Von Arx (1957) regarded Gloeosporium phormii as a synonym beginning to branch, 3–5 µm wide, tip somewhat acute to slightly of C. gloeosporioides. However in the phylogeny of Farr et al. roundish. Conidiophores hyaline, septate, branched, smooth- (2006), strains of this species cluster with C. acutatum and C. lupini. walled, to 30 µm long. Conidiogenous cells hyaline, smooth- Morphological and cultural differences revealed C. phormii as a walled, cylindrical to elongate ampulliform, 5.5–17 × 2.5–4(–5) µm, distinct lineage. We have confirmed this in our study. Colletotrichum opening 1 µm diam, collarette distinct, 0.5–1 µm long, periclinal phormii can be distinguished from the closely related C. salicis (and thickening visible, sometimes conspicuous. Conidia hyaline, indeed from all other species in the C. acutatum complex) by its smooth-walled, aseptate, straight, fusiform to cylindrical with both elongate, large conidia and large appressoria (Tables 2, 3). The ends acute, (9.5–)11.5–13.5(–14.5) × 3.5–4 µm, mean ± SD = 15.0 species appears to be host-specific to Phormium spp. Recently, ± 1.2 × 4.2 ± 0.3 µm, L/W ratio = 3.5. Takeuchi & Hori (2006) reported C. gloeosporioides from Phormium in Japan. However, based on dimensions of conidia (10–16.5 × Culture characteristics: Colonies on SNA flat with undulate to lobate 4–6 µm) and appressoria (7–17 × 4–11.5 µm) and the shape of margin, hyaline, pale honey in the centre, aerial mycelium lacking, the conidia – cylindrical with broadly rounded ends – (fig. 3 of that filter paper grey and mottled, on Anthriscus stem partly covered paper), the fungus seems to be a species in the C. gloeosporioides with salmon to apricot acervuli; growth rate 13.5–17.5 mm in 7 d complex rather than one of the two C. acutatum complex members (23–26 mm in 10 d). Colonies on OA flat with undulate to lobate from Phormium treated in this study. margin; surface buff, sectors isabelline mottled and covered with Colletotrichum phormii is separated from other species by salmon to apricot acervuli, aerial mycelium lacking, reverse salmon TUB2, GAPDH, HIS3 and ACT sequences, and most effectively and mottled olivaceous grey, centre iron-grey; growth rate 15–21 with HIS3. The CHS-1 sequence is the same as that of C. australe. mm in 13.5–21 mm in 7 d (21–27.5 mm in 10 d). Conidia in mass The closest matches in a blastn search with the TUB2 sequence of salmon to apricot. strain CBS 118194 (with 99 % identity, 4 bp differences) was Ga. Material examined: Chile, Valdivia, San Patricio forest nursery of the Corporación acutata isolate PCF 459 (EU635504) from strawberry in Belgium Nacional Forestal near San José de la Mariquina, from seedlings of Pinus radiata, (Debode et al. 2009) and with 99 % identity (5 bp differences), between Dec 1976 and Feb 1977, unknown collector (isolated and deposited in isolate PT250 (= CBS 129953) AJ748624 from olive, Portugal CBS collection Aug. 1977 by H. Peredo López), (CBS H-20729 holotype, culture (Talhinhas et al. 2005), which is here referred to C. rhombiforme. ex-holotype CBS 436.77). With the GAPDH sequence of strain CBS 118194 there was no match closer than 89 % identity. The closest matches in a blastn Notes: Peredo et al. (1979) reported a disease of Pinus radiata search with the ITS sequence with 100 % identity were the same seedlings in a nursery in Chile. The seedlings bent leaders in a GenBank accessions as those obtained in blastn searches of C. similar manner to the “terminal crook” disease in New Zealand salicis, C. pyricola and C. johnstonii. (Dingley & Gilmor 1972) and the affected part of the stem became pinkish. The disease resulted in small seedlings with a thick stem, www.studiesinmycology.org 91 Damm et al . Table 3. Appressoria measurements of Colletotrichum strains studied. Species Accession No. Appressoria on SNA length × width (µm) length × width (µm) L/W ratio mean ± stdev C. acerbum CBS 128530* (8–)9–14(–16.5) × (4–)5–7.5(–9.5) 11.3 ± 2.4 × 6.2 ± 1.2 1.8 C. acutatum CBS 112996* (4–)5.5–9(–13) × (3–)4–6.5(–9.5) 7.3 ± 2.0 × 5.4 ± 1.2 1.3 CBS 111993 (3–)5–8.5(–10.5) × (2–)4–6(–7) 6.7 ± 1.8 × 4.9 ± 1.0 1.4 CBS 112759 (4–)5–7.5(–10) × (3.5–)4–6(–8) 6.3 ± 1.1 × 5.0 ± 1.0 1.3 IMI 319423 (5.5–)6–13(–19.5) × (4–)5–6(–7.5) 9.5 ± 3.6 × 5.5 ± 0.7 1.7 C. australe CBS 116478* (5–)6–11(–14) × (4–)4.5–7(–8.5) 8.5 ± 2.6 × 5.8 ± 1.1 1.5 CBS 131320 (5–)7–10(–11) × (4.5–)5–7(–9) 8.6 ± 1.6 × 6.1 ± 1.1 1.4 C. brisbanense CBS 292.67* (5–)7.5–14.5(–18) × (2.5–)3.5–5(–6) 11.1 ± 3.4 × 4.3 ± 0.9 2.6 C. chrysanthemi CBS 126518 (5–)5.5–9.5(–11.5) × (3–)4.5–6.5(–7.5) 7.5 ± 1.8 × 5.4 ± 1.1 1.4 IMI 364540 (5.5–)6–10(–14) × (4.5–)5–6.5(–7.5) 7.8 ± 2.0 × 5.5 ± 0.8 1.4 C. cosmi CBS 853.73* (5–)5.5–8(–11.5) × (4–)4.5–5.5 6.8 ± 1.2 × 4.9 ± 0.4 1.4 C. costaricense CBS 330.75* (4.5–)6–8.5(–10) × (3–)4–6(–6.5) 7.1 ± 1.2 × 4.9 ± 0.9 1.4 CBS 211.78 (4–)5.5–9(–11) × (3–)4–6(–6.5) 7.3 ± 1.8 × 4.9 ± 1.2 1.5 C. cuscutae IMI 304802* (3.5–)5.5–11.5(–15.5) × (2–)3.5–5.5(–6.5) 8.5 ± 3.2 × 4.6 ± 0.9 1.8 C. fioriniae CBS 128517* (4.5–)7–11.5(–15.5) × (4–)4.5–7(–10.5) 9.2 ± 2.2 × 5.6 ± 1.2 1.6 CBS 200.35 (6–)7.5–10.5(–12) × (4–)5–7(–9) 8.8 ± 1.5 × 6.0 ± 1.0 1.5 CBS 129916 (5–)5.5–11.5(–18) × (4–)4.5–6.5(–8) 8.5 ± 3.1 × 5.4 ± 0.8 1.6 C. godetiae CBS 133.44* (8–)9–12.5(–14.5) × (3–)4–5.5(–6) 10.7 ± 1.9 × 4.7 ± 0.7 2.3 CBS 125972 (6–)8–13(–17) × (3.5–)5–6.5(–7) 10.3 ± 2.4 × 5.8 ± 0.7 1.8 CBS 129911 (6–)7–10.5(–14.5) × (4.5–)5–7(–9) 9.0 ± 1.7 × 6.1 ± 1.0 1.5 CBS 862.70 (4–)5.5–12.5(–17.5) × (3.5–)4–6(–8) 9.0 ± 3.4 × 5.1 ± 1.2 1.8 CBS 129809 (6–)7.5–12(–15) × (4–)5–8(–11.5) 9.6 ± 2.2 × 6.5 ± 1.5 1.5 CBS 127561 (6–)7–12(–16.5) × 4–6(–6.5) 9.4 ± 2.5 × 5.0 ± 0.9 1.9 C. guajavae IMI 350839* (4.5–)5–8(–10.5) × (3.5–)4.5–6(–6.5) 6.6 ± 1.4 × 5.2 ± 0.7 1.3 C. indonesiense CBS 127551* 5.5–9(–14.5) × (5–)5.5–7.5(–9) 7.5 ± 1.8 × 6.3 ± 1.0 1.2 C. johnstonii CBS 128532* (6–)8–11.5(–14) × (2–)4–7.5(–10.5) 9.6 ± 1.7 × 5.8 ± 1.9 1.7 IMI 357027 (4.5–)6.5–10.5(–14) × (3–)4–7(–9.5) 8.4 ± 1.9 × 5.4 ± 1.6 1.6 C. laticiphilum CBS 112989* (5–)6.5–12(–16) × (4–)6–8(–8.5) 9.2 ± 2.8 × 7.2 ± 1.0 1.3 CBS 129827 (4–)5–7(–8) × (2.5–)3.5–5.5(–6) 6.0 ± 1.1 × 4.5 ± 0.8 1.3 C. limetticola CBS 114.14* (5–)6–8.5(–11) × (4–)4.5–6(–7) 7.4 ± 1.3 × 5.3 ± 0.7 1.4 C. lupini CBS 109225* (4–)6–12(–20.5) × (4.5–)6–9(–11.5) 9.0 ± 2.8 × 7.4 ± 1.7 1.2 CBS 109221 (4.5–)5.5–11.5(–19.5) × (3.5–)5–7.5(–8.5) 8.6 ± 3.0 × 6.2 ± 1.1 1.4 C. melonis CBS 159.84* (4.5–)6–11(–13.5) × (3.5–)4.5–6.5(–7.5) 8.3 ± 2.4 × 5.5 ± 1.0 1.5 C. nymphaeae CBS 173.51 (4–)5.5–11(–17) × (3–)4–6.5(–9) 8.2 ± 2.7 × 5.2 ± 1.3 1.6 CBS 112992 (4.5–)6–11(–16.5) × (4–)4.5–6(–7.7) 8.5 ± 2.3 × 5.2 ± 0.9 1.6 CBS 112202 (5–)6.5–10(–13.5) × (4–)5–6.5(–8) 8.2 ± 1.9 × 5.8 ± 0.8 1.4 CBS 126382 (5.5–)5.5–10(–17.5) × (3.5–)4.5–6.5(–9) 7.8 ± 2.4 × 5.5 ± 1.1 1.4 CBS 515.78* (4.5–)6–11(–15) × (3–)4.5–6.5(–8) 8.7 ± 2.5 × 5.5 ± 1.0 1.6 CBS 526.77 (4.5–)6–9(–12) × (3.5–)4.5–6.5(–7.5) 7.4 ± 1.6 × 5.6 ± 1.1 1.3 C. orchidophilum IMI 305357 (5.5–)7.5–15.5(–20.5) × (4.5–)5.5–8.5(–12) 11.6 ± 3.9 × 7.0 ± 1.6 1.6 CBS 631.80 (4.5–)5.5–11(–18) × (4–)4.5–6(–7) 8.2 ± 2.8 × 5.2 ± 0.8 1.6 C. paxtonii IMI 165753* (5–)6–11.5(–16.5) × (3.5–)5.5–7.5(–8.5) 8.8 ± 2.7 × 6.5 ± 1.1 1.4 CBS 502.97 (3.5–)4.5–7.5(–10.5) × (3–)3.5–5(–5.5) 6.0 ± 1.7 × 4.2 ± 0.7 1.4 C. phormii CBS 118194* (4–)8.5–20.5(–32) × (2.5–)4–6(–8) 14.5 ± 6.2 × 5.1 ± 1.0 2.9 CBS 102054 (5.5–)8–13(–14.5) × 5–6.5(–8) 10.4 ± 2.4 × 5.8 ± 0.8 1.8 C. pseudoacutatum CBS 436.77* (3–)5.5–18.5(–25) × (2.5–)3.5–7(–9.5) 12.0 ± 6.3 × 5.1 ± 1.7 2.3 C. pyricola CBS 128531* (4.5–)6–16(–22) × (3.5–)4.5–7(–8.5) 11.1 ± 5.1 × 5.7 ± 1.2 2.0 C. rhombiforme CBS 129953* (5.5–)8–13(–17.5) × (4.5–)6–8(–9.5) 10.6 ± 2.4 × 7.0 ± 1.1 1.5 C. salicis CBS 607.94* (6–)8–15(–19.5) × (5–)6.5–8.5(–9.5) 11.5 ± 3.5 × 7.6 ± 1.0 1.5 CBS 115.14 (3.5–)6.5–12(–16.5) × (3–)4–5.5(–7.5) 9.3 ± 2.7 × 4.9 ± 0.9 1.9 92 The CotriC ollet hum aCtum a ut species complex Table 3. (Continued). Species Accession No. Appressoria on SNA length × width (µm) length × width (µm) L/W ratio mean ± stdev C. salicis CBS 465.83 (7–)8–14(–18) × (5–)5.5–8(–11) 11.1 ± 2.9 × 6.9 ± 1.3 1.6 C. scovillei CBS 126529* (3.5–)5–7.5(–10.5) × (3.5–)5–6.5(–7) 6.3 ± 1.2 × 5.6 ± 0.8 1.1 CBS 120708 (4.5–)6.5–9(–10.5) × (4.5–)6–7.5(–7.5) 7.7 ± 1.2 × 6.7 ± 0.7 1.2 C. simmondsii CBS 122122* (4.5–)6–9.5(–11.5) × (3.5–)4–6.5(–9.5) 7.8 ± 1.9 × 5.3 ± 1.1 1.5 CBS 294.67 (6–)6.5–10(–14) × (4.5–)5–7(–8.5) 8.3 ± 1.8 × 6.0 ± 0.8 1.4 CBS 114494 (4–)5.5–9.5(–12.5) × (3–)4–6(–8) 7.5 ± 1.8 × 5.0 ± 1.1 1.5 C. sloanei IMI 364297* (4–)5–11(–17.5) × (4–)4.5–6.5(–8) 8.0 ± 3.0 × 5.4 ± 0.9 1.5 C. tamarilloi CBS 129814* (4–)5–10.5(–16) × (3.5–)4.5–6.5(–8) 7.8 ± 2.6 × 5.5 ± 0.9 1.4 CBS 129811 (4–)5–10(–15) × (3.5–)4.5–6(–7) 7.5 ± 2.4 × 5.2 ± 0.9 1.5 C. walleri CBS 125472* (4.5–)5.5–12.5(–18.5) × (3.5–)4.5–7.5(–10.5) 9.0 ± 3.3 × 5.9 ± 1.4 1.5 Colletotrichum sp. CBS 129821 (5.5–)6.5–9(–11) × (4.5–)5.5–7.5(–8.5) 7.9 ± 1.3 × 6.5 ± 0.9 1.2 CBS 129820 (6.5–)8.5–11.5(–13.5) × (5–)6–8.5(–10.5) 10.0 ± 1.6 × 7.2 ± 1.2 1.4 CBS 129823 (5–)5.5–10.5(–15.5) × (3.5–)4.5–6.5(–8) 7.9 ± 2.4 × 5.4 ± 1.1 1.5 IMI 384185 (4.5–)5.5–9.5(–12.5) × (4.5–)5–7(–8) 7.6 ± 2.1 × 6.0 ± 0.8 1.3 CBS 101611 (5.5–)6.5–10(–14) × (5–)6–8(–8.5) 8.2 ± 1.8 × 6.8 ± 1.0 1.2 CBS 129810 (6–)6.5–9(–10.5) × (5.5–)6–7(–7.5) 7.8 ± 1.1 × 6.3 ± 0.6 1.2 * ex-type strain (min–)min-stdev–max-stdev(–max) Fig. 24. Colletotrichum pseudoacutatum (from ex-holotype strain CBS 436.77). A–B. Conidiomata. C. Tips of setae. D. basis of seta. E. Conidiophores. F. Seta. G. Conidiophores. H–M. Appressoria. N–O. Conidia. A, C–E, N. from Anthriscus stem. B, F–M, O. from SNA. A–B. DM, C–O. DIC, Scale bars: A = 100 µm, B = 200 µm, E = 10 µm. Scale bar of E applies to C–O. www.studiesinmycology.org 93 Damm et al . Fig. 25. Colletotrichum pyricola (from ex-holotype strain CBS 128531). A–B. Conidiomata. C–K. Conidiophores. L–Q. Appressoria. R–S. Conidia. A, C–F, R. from Anthriscus stem. B, G–Q, S. from SNA. A–B. DM, C–S. DIC, Scale bars: A = 200 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–S. restricted terminal growth and increased growth of lateral shoots. 183087 (EU400145, probably C. coccodes, Chen YY, Conner R, Babcock C, Penner W, unpubl. data) and BBA 71369 from Pleione Two strains with differing colony characteristics were isolated and were used in pathogenicity tests on 4-month-old seedlings of Pinus (AJ301980, probably C. orchidophilum, Nirenberg et al. 2002). radiata; 11.5 % of the seedlings inoculated with the salmon orange The closest matches with the TUB2 sequence showed only 82 % culture and 92 % of the seedlings with the grey culture showed identity, including C. trichellum strains HKUCC 10378, CBS 217.64 and CBS 118198 (GQ849447, Yang et al. 2009, GU228106, the symptoms. The two strains were sent to CBS, and both were GU228107, Damm et al. 2009). There is no match over the whole identified as C. acutatum f. pineum by von Arx, presumably because span of the GAPDH sequence of this species. of the identity of the host plant and some of their morphological features, especially the conidia with acute ends typical for C. In morphological terms, C. pseudoacutatum mainly differs from species in the C. acutatum complex by the formation of pale brown, acutatum. One of the strains was kept in the CBS collection as verruculose, irregular shaped appressoria, and also by the more CBS 436.77; unfortunately we can only suppose it was the salmon abundant formation of setae. orange culture. Strain CBS 436.77 turns out not to be closely related to C. acutatum f. pineum, which belongs to C. acutatum s. str. (Fig. 1). Colletotrichum pyricola Damm, P.F. Cannon & Crous, sp. Colletotrichum pseudoacutatum is at best basal to the C. acutatum nov. MycoBank MB800510. Fig. 25. species complex and forms a sister group to a clade containing the C. acutatum complex and C. orchidophilum (fig. 2 in Cannon et al. Etymology: Named after the host plant Pyrus communis. 2012, this issue). The closest matches in a blastn search on the ITS sequence of strain CBS 436.77 (with only 94 % identity) are Sexual morph not observed. Asexual morph on SNA. Vegetative unidentified Colletotrichum isolates, e.g. from Podocarpaceae in hyphae 1–8 µm diam, hyaline, smooth-walled, septate, branched. New Zealand (Joshee et al. 2009), plus several C. coccodes strains Chlamydospores not observed. Conidiomata not developed, including the ex-epitype strain CBS 164.49 (HM171678, Liu et al. conidiophores formed directly on hyphae. Setae not observed. 2011), C. trichellum strains MEP1535 (= CBS 118198, DQ286152, Conidiophores hyaline, smooth-walled, septate, branched. Farr et al. 2006) and DAOM 188792 (= CBS 125343, EU400142, Conidiogenous cells hyaline smooth-walled, cylindrical, 9–25 × wrongly identified as C. dematium, Chen YY, Conner R, Babcock 2.5–3.5 µm, opening 1–1.5 µm diam, collarette 1–1.5 µm long, C, Penner W, unpubl. data) and “C. gloeosporioides” strains DAOM periclinal thickening visible. Conidia hyaline, smooth-walled, 94 The CotriC ollet hum aCtum a ut species complex aseptate, straight, fusiform to cylindrical with one end slightly acute Colletotrichum rhombiforme Damm, P.F. Cannon & Crous, and one end round or slightly acute, (10–)14.5–18.5(–24) × (3.5–) sp. nov. MycoBank MB800511. Fig. 26. 4.5–5(–5.5) µm, mean ± SD = 16.7 ± 2.1 × 4.7 ± 0.4 µm, L/W ratio = 3.5. Appressoria single or in small dense clusters, pale brown, Etymology: Named after the shape of the ascospores, which can smooth-walled, ellipsoidal, clavate to cylindrical, the edge entire or be rhomboidal. undulate, (4.5–)6–16(–22) × (3.5–)4.5–7(–8.5) µm, mean ± SD = 11.1 ± 5.1 × 5.7 ± 1.2 µm, L/W ratio = 2.0. Sexual morph developed on Anthriscus stem. Ascomata globose Asexual morph on Anthriscus stem. Conidiomata acervular, to subglobose, pale brown, 300–400 × 400–500 µm, glabrous, conidiophores formed on pale brown, angular, basal cells 3–7 ostiolate. Peridium 8–14 µm thick, composed of pale to medium µm diam. Setae not observed. Conidiophores hyaline, smooth- brown flattened angular cells, 6–16 µm diam. Ascogenous hyphae walled, septate, branched, to 40 µm long. Conidiogenous cells hyaline, smooth-walled, delicate. Interascal tissue composed of hyaline, smooth-walled, cylindrical, 11–20 × 3–4 µm, opening paraphyses, hyaline, septate, branched at the base, 35–80 × 3–5 1.5–2 µm diam, collarette 0.5–2 µm long, periclinal thickening µm, widest part at the base, tips round. Asci cylindrical, 55–73 distinct. Conidia hyaline, smooth-walled, aseptate, straight, × 9–11 µm, 8-spored. Ascospores arranged uni-to bi-seriately, fusiform to cylindrical with both ends acute, (9.5–)14–17(–18.5) aseptate, hyaline, smooth-walled, oval, fusiform, or rhomboidal, × (4–)4.5–5(–5.5) µm, mean ± SD = 15.4 ± 1.6 × 4.8 ± 0.4 µm, one end ± acute and one end round or both ends round, sometimes L/W ratio = 3.2. slightly curved, (11–)12.5–16(–17) × 4–)4.5–6(–7.5) µm, mean ± SD = 14.1 ± 1.6 × 5.2 ± 0.8 µm, L/W ratio = 2.7. Culture characteristics: Colonies on SNA flat with entire margin, Asexual morph on SNA. Vegetative hyphae 1–8 µm diam, hyaline, on medium, filter paper and Anthriscus stem partly covered hyaline to pale brown, smooth-walled, septate, branched. with thin floccose white to pale grey aerial mycelium and orange Chlamydospores not observed. Conidiomata absent, conidiophores acervuli, reverse hyaline with orange to grey acervuli shining formed directly on hyphae. Setae not observed. Conidiophores through; growth rate 24–25 mm in 7 d (35–37 mm in 10 d). Colonies hyaline to pale brown, smooth-walled, septate and branched, to on OA flat to raised with entire margin; surface partly covered with 50 µm long. Conidiogenous cells hyaline to pale brown, smooth- floccose to woolly whitish to pale olivaceous grey aerial mycelium walled, cylindrical to ampulliform, often lacking a basal septum and orange acervuli mainly appearing in growth rings, reverse buff, and continuous with the conidiophore, discrete phialides measure olivaceous buff to grey olivaceous with olivaceous grey to iron 4–13 × 3–5 µm, opening 1–2 µm diam, collarette distinct, 1–2 µm grey rings; growth rate 21.5–22.5 mm in 7 d (35–37.5 mm in 10 d). long, periclinal thickening distinct. Conidia hyaline, smooth-walled, Conidia in mass orange. aseptate, straight cylindrical with one end round and one end slightly acute or both ends round, (12–)12.5–17(–24) × (4–)4.5– Material examined: New Zealand, WO, Waikato, from fruit rot of Pyrus communis, 5.5(–6) µm, mean ± SD = 14.7 ± 2.1 × 5.0 ± 0.7µm, L/W ratio = 1 Jun. 1988, unknown collector (deposited in ICMP collection by P.R. Johnston), 2.9. Appressoria single or in loose groups, medium to dark brown, (CBS H-20810 holotype, culture ex-type CBS 128531 = ICMP 12924 = PRJ 977.1). smooth-walled, the outline mostly clavate, elliptical or ovate, the edge entire or undulate, rarely lobate, (5.5–)8–13(–17.5) × (4.5–) Notes: This is a third species within clade 4, not clearly distinct 6–8(–9.5) µm, mean ± SD = 10.6 ± 2.4 × 7.0 ± 1.1 µm, L/W ratio from C. johnstonii using morphological or cultural characteristics = 1.5. but with unique ACT, TUB2, CHS-1, GAPDH and HIS3 sequences. Asexual morph on Anthriscus stem. Conidiomata acervular, The ITS sequence of C. pyricola is identical with those of C. salicis, conidiophores formed on a cushion of pale brown angular cells C. johnstonii and C. phormii. 4–9 µm diam. Setae very few, pale brown, smooth-walled, As with C. johnstonii, C. pyricola appears to be endemic to New 3–4-septate, 50–80 µm long, base cylindrical, 3–3.5 µm diam, tip Zealand, but more data are needed to confirm its distribution. Strain ± rounded or ending with a conidiogenous locus. Conidiophores CBS 128531 (= PRJ 977.1) is the only strain of this species available pale brown, smooth-walled, septate, branched, to 40 µm long. to us and was included in C. acutatum group C by Johnston & Jones Conidiogenous cells pale brown, smooth-walled, cylindrical, (1997) and Lardner et al. (1999) and in group F2 by Guerber et al. (2003). In the combined GS and GAPDH phylogeny in Guerber sometimes polyphialides, 12–28 × 2–3.5 µm, opening 1–2 µm et al. (2003), there is a second strain grouping with C. pyricola diam, collarette 0.5–1.5 µm long, periclinal thickening distinct. Conidia hyaline, smooth-walled, aseptate, straight, very variable in that they assigned as the only representative of their F5 group. shape, cylindrical, clavate, ellipsoidal or limoniform with one end This strain (PRJ 823) however belongs to group B in Lardner et al. round and one end slightly acute to truncate, (7.5–)10.5–17.5(–21) (1999), with a completely different RAPD banding pattern. × (3.5–)4–5.5(–6) µm, mean ± SD = 14.1 ± 3.5 × 4.8 ± 0.6 µm, In contrast to apple, for which Colletotrichum species are listed as major pathogens causing bitter rot (González et al. 2006), pear L/W ratio = 2.9. trees seem to be rarely affected by anthracnose. Colletotrichum piri Noack was actually described from apple (listed as Pyrus malus, Culture characteristics: Colonies on SNA flat with entire margin, hyaline to pale cinnamon, on filter paper, Anthriscus stem and a synonym of Malus pumila) in Brazil, rather than from pear as its medium covered with short floccose-felty pale olivaceous grey name suggests. The closest match in a blastn search with the TUB2 sequence aerial mycelium, on Anthriscus stem covered with pale grey to black of strain CBS 128531 (with 98 % identity, 10 bp differences) were structures, reverse medium hyaline to pale cinnamon, filter paper AJ409294 isolate 90 from Fragaria in the UK (Talhinhas et al. 2002) pale cinnamon to olivaceous grey, growth rate 20–22.5 mm in 7 d as well as AJ748609, AJ748612–AJ748614, AJ748619–AJ748622, (32.5–37.5 mm in 10 d). Colonies on OA flat with entire margin; AJ748625 from olive isolates (Talhinhas et al. 2005). With the surface honey, pale olivaceous grey, grey olivaceous to olivaceous, GAPDH sequence there was no closer match than 89 % identity. almost entirely covered with floccose-felty pale olivaceous grey aerial mycelium, reverse pale olivaceous grey, grey olivaceous www.studiesinmycology.org 95 Damm et al . Fig. 26. Colletotrichum rhombiforme (from ex-holotype strain CBS 129953). A–B. Conidiomata. C–H. Conidiophores. I–M. Appressoria. N–O. Conidia. P. Ascomata. Q. Peridium in cross section. R. Outer surface of peridium. S. Ascospores. T. Paraphyses. U–W, Y. Asci. X. Apical region of ascus. A, C–E, N, P–Y. from Anthriscus stem. B, F–M, O. from SNA. A–B. DM, C–Y. DIC, Scale bars: A = 200 µm, B, P = 100 µm, C, Q = 10 µm. Scale bar of C applies to C–O. Scale bar of Q applies to Q–Y. 96 The CotriC ollet hum aCtum a ut species complex to iron grey, growth rate 19–21 mm in 7 d (29–32.5 mm in 10 d). CBS 131322, the other isolate of C. rhombiforme included in this Conidia in mass whitish to pale salmon. study) (Robideau et al. 2008). Material examined: Portugal, Mirandela, Torre de D. Chama, from anthracnose on Colletotrichum salicis (Fuckel) Damm, P.F. Cannon & fruit of Olea europaea, Dec. 2003, P. Talhinhas (CBS H-20724 holotype, culture Crous, comb. nov. MycoBank MB800518. Fig. 27. ex-type CBS 129953 = PT250). USA, Washington, Long Beach, from Vaccinium macrocarpon, 1993, Carris, culture CBS 131322 = DAOM 233523. Basionym: Sphaeria salicis Fuckel, Jahrb. nass. Ver. Naturk. 23– 24: 115. 1870. ≡ Sphaeria salicis Auersw., in Fuckel, Fungi Rhen. no. 913, in sched. Notes: Talhinhas et al. (2005, 2009, 2011) found a diverse range of 1864, nom. nud. C. acutatum isolates from olive fruit with anthracnose symptoms in ≡ Physalospora salicis (Fuckel) Sacc., Syll. fung. (Abellini) 1: 439. 1882. Portugal. One of these strains, PT250 (=CBS 129953) was found ≡ Physosporella salicis (Fuckel) Höhn., Annls mycol. 16: 58. 1918. to be significantly divergent from other groups within C. acutatum ≡ Anisostomula salicis (Fuckel) Petr., Hedwigia 65: 198. 1925. ≡ Plectosphaera salicis (Fuckel) Arx & E. Müll., Beitr. Kryptfl. Schweiz 11 based on ITS and beta-tubulin sequences, and was placed in the (no. 1): 204. 1954. new clade A6. Talhinhas’s olive strain here forms the type of C. ≡ Glomerella salicis (Fuckel) L. Holm, in Holm & Ryman, Thunbergia 30: rhombiforme. A second strain that we identified as C. rhombiforme 6. 2000. = Phyllachora amenti Rostr., Skr. Christiana Vidensk.-Selsk. Forhandl. 9: 5. and included here was isolated from Vaccinium macrocarpon (American cranberry) in the USA, and was studied by Robideau ≡ Haplothecium amenti (Rostr.) Theiss. & Syd., Annls Mycol. 13: 615. et al. (2008). Further representatives of this clade are likely to be some of those isolated from Rhododendron in Sweden and Latvia ≡ Glomerella amenti (Rostr.) Arx & E. Müll., Beitr. Kryptfl. Schweiz 11 (no. 1): 197. 1954. (strains S2, L3, L4, L5, L6) by Vinnere et al. (2002) that were = Glomerella lycopersici F. Krüger, Arbeiten Kaiserl. Biol. Anst. Land- Forstw. reported to belong to clade A6 by Sreenivasaprasad & Talhinhas 9: 308. 1913. (2005) based on ITS sequencing. Since ITS does not distinguish ≡ Gloeosporium lycopersici F. Krüger, Arbeiten Kaiserl. Biol. Anst. Land- between all species, sequences of additional genes would be Forstw. 9: 308. 1913. ≡ Colletotrichum kruegerianum Vassiljevsky, Fungi Imperfecti Parasitici 2: necessary to confirm this placement. 321. 1950 [non C. lycopersici Chester 1891]. A variety of Glomerella rufomaculans, Ga. rufomaculans var. = Physalospora miyabeana Fukushi, Annls phytopath. Soc. Japan 1 (no. 4): vaccinii Shear was described from leaves of Vaccinium macrocarpon 7. 1921. in New Jersey, USA with conidia and ascospores that agree in ≡ Glomerella miyabeana (Fukushi) Arx, Phytopath. Z. 29: 448. 1957. size with C. rhombiforme. Its conidia were described as oblong- cylindric, subclavate, sometimes slightly curved (Shear 1907). Sexual morph developed on Anthriscus stem. Ascomata globose The variety was wrongly listed as Ga. fructigena var. vaccinii in to pyriform, ostiolate, medium brown, darker towards the ostiole, Sylloge Fungorum (Saccardo & Trotter 1913); MycoBank and Index 150–200 × 185–250 µm. Peridium 10–15 µm thick, composed Fungorum list this taxon as separate species, Ga. rufomaculans- of pale to medium brown flattened angular cells 5–15 µm diam. vaccinii Shear, MycoBank also as Ga. rufomaculansvaccinii Ascogenous hyphae hyaline, smooth-walled, delicate. Interascal (orthographic variant) and additionally as Ga. fructigena var. tissue composed of paraphyses, hyaline, septate, 30–80 × 2–3.5 vaccinii. However a strain (CBS 124.22) deposited 1922 in the CBS µm, widest part at the base, tips round. Asci cylindrical, 55–88 collection by L.C. Shear as Ga. rufomaculans var. vaccinii is lacking × 8–12 µm, 8-spored. Ascospores arranged uni- to biseriately, host information and belongs to the C. gloeosporioides complex aseptate, hyaline, smooth-walled, ovoid, fusiform, cigar-shaped (Weir et al. 2012, this issue). or cylindrical, one end acute and one end obtuse or both ends Colletotrichum rhombiforme is closely related to C. acerbum, C. obtuse, sometimes very slightly curved, (12.5–)13–15(–17) × australe, C. kinghornii and C. phormii, which together form a sister (4.5–)5–6(–6.5) µm, mean ± SD = 14.1 ± 1.1 × 5.4 ± 0.5 µm, clade to C. salicis. In this study, only strains of C. rhombiforme and L/W ratio = 2.6. C. salicis formed sexual morphs in culture. The ascospores of the Asexual morph on SNA. Vegetative hyphae 1–8 µm diam, two species have the same size, but differ in shape. Additionally, hyaline to pale brown, smooth-walled, septate, branched. conidia of C. salicis formed on SNA are smaller than those of C. Chlamydospores not observed. Conidiomata absent, rhombiforme, and conidia of C. rhombiforme formed on Anthriscus conidiophores formed directly on hyphae. Setae not observed. stem are sometimes ellipsoidal or limoniform while those of C. Conidiophores hyaline, smooth-walled, simple or septate salicis are uniformly cylindrical. and branched. Conidiogenous cells hyaline, smooth-walled, Colletotrichum rhombiforme is separated from other species by cylindrical to elongate ampulliform, sometimes intercalary (necks all sequences studied except the CHS-1 sequence, which is the not separated from hyphae by a septum), 5–20 × 2–3.5 µm, same as that of C. acerbum. It can best be identified with TUB2 opening 1–1.5 µm diam, collarette 0.5–1 µm long, periclinal and ITS. The closest match in a blastn search with the TUB2 thickening visible. Conidia hyaline, smooth-walled, aseptate, sequence of CBS 129953 with 100 % identity was AJ748624, straight, cylindrical to clavate with one end round and one end ± the sequence generated from the same isolate by Talhinhas et acute to truncate, (8.5–)10.5–15.5(–19.5) × (3.5–)3–4.5(–5) µm, al. (2005), all other isolates showed ≤ 97 % sequence identity. mean ± SD = 13.0 ± 2.4 × 4.0 ± 0.5 µm, L/W ratio = 3.2, conidia With the GAPDH sequence there was no closer match than 88 of strains CBS 115.14 and CBS 465.83 narrower, measuring (9–) % identity. Closest matches with the ITS sequence (with 100 % 10.5–15(–17) × 2.5–3.5(–4) µm, mean ± SD = 12.7 ± 2.3 × 3.1 identity) were AJ749700 from isolate PT250 (= CBS 129953) ± 0.5 µm, L/W ratio = 4.1 and (7.5–)9.5–15.5(–22) × 3–3.5(–4.5) (Talhinhas et al. 2005), AF411704, AF411706, AF411707 and µm, mean ± SD = 12.4 ± 3.1 × 3.3 ± 0.4 µm, L/W ratio = 3.8. AF411719 from Rhododendron isolates L3, L5, L6, S2 from Latvia Appressoria single or in small groups, medium brown, outline and Sweden (Vinnere et al. 2002) and with 99 % identity (1 bp mostly clavate, elliptical or ovate, the edge entire or undulate, difference) AF411705 from Rhododendron isolate L4 (Vinnere et rarely lobate, (6–)8–15(–19.5) × (5–)6.5–8.5(–9.5) µm, mean ± SD = 11.5 ± 3.5 × 7.6 ± 1.0 µm, L/W ratio = 1.5. al. 2002) and EF672241 from Vaccinium isolate DAOM 233253 (= www.studiesinmycology.org 97 Damm et al . Fig. 27. Colletotrichum salicis (from ex-epitype strain CBS 607.94). A–B. Conidiomata. C–H. Conidiophores. I–N. Appressoria. O–P. Conidia. Q–R. Ascomata. S. Peridium in cross section. T. Outer surface of peridium. U. Ascospores. V. Paraphyses. W–Y. Asci. A, C–D, O, Q–Y. from Anthriscus stem. B, E–N, P. from SNA. A–B, Q. DM, C–P, R–Y. DIC, Scale bars: A, Q, R = 100 µm, C, S = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–P. Scale bar of S applies to S–Y. 98 The CotriC ollet hum aCtum a ut species complex Asexual morph on Anthriscus stem. Conidiomata acervular, amenti with filiform septate conidia, 35–45 × 1 µm in size, formed in only formed after ca. 14 d, the conidiophores, formed on a cushion pycnidia. This is most likely to be an accompanying species rather of pale brown angular cells, 3.5–8.5 µm diam. Setae not observed. than a genetically linked morph. It may be Septoria didyma. Conidiophores hyaline, smooth-walled, simple or septate and Physalospora miyabeana was described from Salix purpurea branched, to 30 µm long. Conidiogenous cells hyaline, smooth- var. angustifolia in Japan by Fukushi (1921), and combined into walled, cylindrical, 11–18 × 2.5–4 µm, opening 1–2 µm diam, Glomerella by von Arx (1957) as Glomerella miyabeana. The collarette 0.5 µm long, periclinal thickening visible. Conidia hyaline, pathology of this fungus was described in detail by Nattrass smooth-walled, aseptate, straight, cylindrical with one end round (1928) based on British collections from Salix viminalis. He noted and one end slightly acute to truncate, (14.5–)16–18.5(–20) × that the species showed similarities to Physalospora salicis. He (4–)4.5–5(–5.5) µm, mean ± SD = 17.1 ± 1.3 × 4.9 ± 0.3 µm, identified his collections as P. miyabeana due to the presence of L/W ratio = 3.5, conidia of strain CBS 115.14 smaller, measuring a Gloeosporium (i.e. Colletotrichum) asexual morph as noted by (9.5–)11.5–16(–18.5) × (2.5–)3–4(–4.5) µm, mean ± SD = 14.0 ± Fukushi (1921), and considered that the species was more closely related to Glomerella than to Physalospora. Further information on 2.3 × 3.3 ± 0.4 µm, L/W ratio = 4.2. pathology has been contributed by Butin (1960). Glomerella lycopersici was described from a mummified fruit of Culture characteristics: Colonies on SNA flat with entire margin, Solanum lycopersicum (= Lycopersicon esculentum) in Germany. hyaline, filter paper rose to iron-grey, with felty to woolly, white The ex-syntype strain CBS 115.14 hardly sporulates and did not to olivaceous grey aerial mycelium on Anthriscus stem and filter form a sexual morph in culture, but molecular data confirm the paper, reverse same colours; growth rate 18–24 mm in 7 d (32.5– synonymy. The ascospore measurements (15–17.3 × 5.8–6.9 µm) 36 mm in 10 d). Colonies on OA flat with entire margin; surface in the original description by Krüger (1913) differ somewhat from pale amber, ochraceous to apricot, almost entirely covered by felty our measurements, and those of conidia differ even more (20–22 × to floccose-felty, white, pale luteous to very pale olivaceous aerial 4.7–6.9 µm) from our own; the discrepancy could be due to the use mycelium, reverse rosy buff, ochraceous, cinnamon to buff; growth of different growth media. However, the shapes of the ascospores rate 21–27 mm in 7 d (34–37.5 mm in 10 d). Conidia in mass pale (one side often nearly straight and one side convex or irregularly salmon. biconvex) and of the conidia (often clavate) correspond to those of Material examined: Germany, Hessen, near Oestrich (Hostrichia), on dry branches strain CBS 607.94. A further synonym may be Guignardia salicina of Salix fragilis, collection date and collector unknown (Fuckel, Fungi Rhenani no. (syn. Physalospora salicina, Glomerella salicina), but we have 913 (G holotype [not seen], K(M) isotype of Sphaeria salicis). Netherlands, Z.- not been able to source the original description or examine type Flevoland, Salix forest near Blocq van Kuffeler, from leaf spot of Salix sp., 11 Sep. material. 1994, H.A. van der Aa, (CBS H-20730 epitype of Sphaeria salicis, here designated, culture ex-epitype CBS 607.94). Sweden, Uppland, Uppsala, Bondkyrka parish, Colletotrichum lucidae was described on living leaves Salix Nåsten forest, between Lurbo bridge and Predikstolen cliff, 22 Jun. 1946, S. lucida in Wisconsin, USA by Greene (1956). It forms obtuse Lundell (Fungi exsiccati Suecici, praesertim Upsalienses no. 3613a; K(M) 85441), cylindrical conidia (13–19 × 4–6.5 µm) and 1–2-septate setae stated by L. Holm to “agree perfectly” with the type of Sphaeria salicis. Germany, (50–65 × 4–5 µm). It might also be a synonym of C. salicis. Greene Berlin, Dahlem, from fruit of Solanum lycopersicum, collection date and collector unknown (deposited in CBS collection Feb. 1914 by F. Krüger), culture ex-syntype (1964) also found the species a few years later on S. pyrifolia. The of Glomerella lycopersici CBS 115.14. Japan, Sapporo, on stems of Salix purpurea, strains we studied did not form setae, but if C. lucidae is conspecific, 20 Oct. 1920, Fukushi (K(M) 110218), authentic and possible type material of it will just be a later synonym of C. salicis. Physalospora miyabeana, sent to Kew via R.M. Nattrass. USA, Ithaca, New York Johnston & Jones (1997) found that C. salicis (as Ga. State College of Agriculture, in office, Plant Sci. Bldg, Cornell Univ., from anthracnose and dieback of Araucaria excelsa, 22 Apr. 1983, J. E. Carol, culture CBS 465.83. miyabeana) had a close genetic affinity to C. acutatum. Vinnere (2004) regarded Ga. miyabeana as the sexual morph of one of the Notes: Colletotrichum salicis is unusual among Colletotrichum biological groups within C. acutatum s. lat., and suggested that species in the prominence of sexual structures relative to asexual it should be recognised as a separate species. This is confirmed structures; it is one of the few species to produce fertile ascomata by our study. Colletotrichum salicis forms a sister clade to a clade in culture. The ascomata are not infrequently encountered on dead formed by C. phormii, C. rhombiforme, C. acerbum, C. australe and and dying, weakly lignified tissues including young stems, bracts C. kinghornii. and flower/fruit stalks of Salix species. A lack of distinctive features Fruit-inhabiting strains of C. salicis (as Ga. miyabeana) are has caused this species to be described as new several times. known to be homothallic (Johnston & Jones 1997), and those Colletotrichum salicis was first described as Sphaeria salicis by from Acer platanoides in USA (which also belong here), were Fuckel (1870), based on an exsiccatum in his series Fungi Rhenani also determined as homothallic by LoBuglio & Pfister (2008). In issued in 1864. Its label ascribed the species name to Auerswald, this study, only strains of C. salicis and C. rhombiforme formed but no description was provided and Auerswald was not credited sexual morphs in culture. The ascospores of the two species are with the name when it was subsequently validly published. the same size, but differ in shape. Conidia of C. salicis formed on Sphaeria salicis has been transferred to a range of different SNA are smaller than those of C. rhombiforme, and those formed sexual morph genera. In 1954, it was moved to the rather confused on Anthriscus stem are uniformly cylindrical, with no ellipsoidal genus Plectosphaera (von Arx & Müller 1954, Cannon 1991) and or limoniform conidia as found in C. rhombiforme. Other closely later, in 2000, to Glomerella (Holm & Ryman 2000). related species i.e. C. acerbum, C. australe, C. kinghornii and C. Phyllachora amenti was described from Salix reticulata in phormii form conidia on SNA, measuring on average 17.9 × 4.7 Dovre, Norway by Rostrup (1891). Von Arx & Müller (1954) µm, 17 × 4.4 µm and 18.3 × 3.8 µm and 23 × 4.6 µm respectively, transferred the species to Glomerella (apparently not noticing the that are larger than those of C. salicis, measuring 13.0 × 4.0 µm. similarities with Plectosphaera salicis). We have not seen Rostrup’s According to our study, C. salicis is not restricted to a single type, but his description and that of von Arx & Müller are highly host genus but seems to have a preference for woody hosts (Acer, reminiscent of C. salicis and we are confident of the synonymy. Araucaria, Malus, Populus, Pyrus and especially Salix). According Rostrup also described a putative asexual morph of Phyllachora to Farr & Rossman (2012), Glomerella amenti has been recorded www.studiesinmycology.org 99 Damm et al . Fig. 28. Colletotrichum scovillei (from ex-holotype strain CBS 126529). A–B. Conidiomata. C–E. Conidiophores. F–K. Appressoria. L–M. Conidia. A, C, L. from Anthriscus stem. B, D–K, M. from SNA. A–B. DM, C–M. DIC, Scale bars: A = 200 µm, B = 100 µm, C = 10 µm. Scale bar of C applies to C–M. on Salix polaris and S. reticulata in Norway (Holm & Holm 1994) strawberry in Belgium (Debode et al. 2009). With the GAPDH sequence of CBS 607.94 no match closer than 87 % identity and Ga. miyabeana was recorded on Salix amygdaloides, S. babylonica, S. daphnoides, S. fragilis, S. gooddingii, S. lasiolepis, was found. In blastn searches with the ITS sequence, numerous S. × alba-matsudana, Fragaria × ananassa, Malus domestica and matches with 100 % identity were found, some of which we know to Pyrus pyrifolia in New Zealand (Pennycook 1989, Guerber et al. belong to distinct species. 2003, Gadgil 2005) on Salix sp. in Poland (Mulenko et al. 2008) and UK (Dennis 1986) and on Acer truncatum in China (Sun et Colletotrichum scovillei Damm, P.F. Cannon & Crous, sp. al. 2011). The species is also reported from leaf lesions of Salix nov. MycoBank MB800512. Fig. 28. fragilis, S. alba var. vitellina, S. cinerea in Australia (Cunnington et al. 2007). Johnston & Jones (1997) suggested that Ga. miyabeana Etymology: Named after Wilbur Lincoln Scoville (1865–1942) who which causes the distinctive disease “twig canker” on Salix spp., devised the Scoville scale for measuring the “hotness” of chilli only occurs on fruits (strawberry, apple, nashi, tomato) as an peppers, the host plant of this species. opportunistic secondary invader, becoming infected from willow trees that, in New Zealand, are commonly used as orchard shelter Sexual morph not observed. Asexual morph on SNA. Vegetative belts. Cunnington et al. (2007) therefore tested the pathogenicity of hyphae 1–5.5 µm diam, hyaline to pale brown, smooth-walled, strains from Salix spp. in Australia on apple and nashi fruits. They septate, branched. Chlamydospores not observed. Conidiomata were shown to be positive for pathogenicity but less aggressive absent, acervuli not developed, conidiophores formed directly than a different C. acutatum s. lat. strain that originated from an on hyphae. Setae not observed. Conidiophores hyaline to pale apple fruit. All Colletotrichum strains from Salix spp. in the CBS brown, smooth-walled to verruculose, septate, branched, to 50 collection belong to the former species. µm long. Conidiogenous cells hyaline smooth-walled, cylindrical Colletotrichum salicis is separated from other species by all to slightly inflated, 8–18 × 3–4 µm, opening 1–2 µm diam, genes, except for ITS; it forms a well-supported clade (bootstrap collarette 1–1.5(–2) µm long, periclinal thickening conspicuous. support 98–99 %) with little sequence variation in HIS3, TUB2, Conidia hyaline, smooth-walled, aseptate, straight, cylindrical to GAPDH and ACT. The closest match in a blastn search with clavate with one end round and one end ± acute, (10.5–)12.5– the TUB2 sequence of CBS 607.94 (with 97 % identity, 13 bp 15(–16.5) × (3–)3.5–4(–4.5) µm, mean ± SD = 13.7 ± 1.3 × differences) was Ga. acutata isolate PCF 459 (EU635504) from 3.8 ± 0.3 µm, L/W ratio = 3.6, conidia of strain CBS 120708 100 The CotriC ollet hum aCtum a ut species complex narrower, measuring (11.5–) 12.5–14.5(–15) × 3–3.5 µm, mean occuring also on other host plants (Damm et al. 2012, this issue). ± SD = 13.5 ± 0.8 × 3.3 ± 0.2 µm, L/W ratio = 4.1. Appressoria There are several reports of C. coccodes, inclusive of its synonym C. single or in loose groups, medium to dark brown, smooth-walled, atramentarium and of C. nigrum, on Capsicum in different countries subglobose, ovoid to ellipsoidal, the outline entire, sometimes (Farr & Rossman 2012). These species do not belong to the C. undulate, (3.5–)5–7.5(–10.5) × (3.5–)5–6.5(–7) µm, mean ± SD acutatum complex. Colletotrichum coccodes is more closely related = 6.3 ± 1.2 × 5.6 ± 0.8 µm, L/W ratio = 1.1. to some of the curved-spored species (fig. 1 in Cannon et al. 2012, Asexual morph on Anthriscus stem. Conidiomata acervular, this issue). The identity of C. nigrum has not been studied recently, conidiophores formed on pale brown, angular, basal cells 3–8.5 µm and it is most probably either a further synonym of C. coccodes or diam. Setae not observed in strain CBS 126529, however in strain a member of the C. gloeosporioides complex. Another species on CBS 120708 medium brown, smooth-walled, 1–2-septate, 40–60 Capsicum annuum from Australia belonging to the C. acutatum µm long, base cylindrical to inflated, 3.5–8 µm diam, rounded. species complex, C. brisbanense, is described above. Apart from Conidiophores hyaline to pale brown, smooth-walled, septate, earlier reports of the strains included in this study, C. acutatum (s. branched, to 30 µm long. Conidiogenous cells hyaline to pale lat.) has also been reported on Capsicum in Bulgaria (Jelev et al. brown, smooth-walled, cylindrical, 9–23 × 2.5–3.5 µm, opening 2008), India (Kaur & Singh 1990), Korea (Cho & Shin 2004) and 1.5–2 µm diam, collarette 1 µm long, periclinal thickening distinct. Taiwan (Liao et al. 2012). Conidia hyaline, smooth-walled, aseptate, straight, cylindrical to The closest match in a blastn search with the GAPDH sequence fusiform with both ends slightly acute or one end round, (9–)14.5– of strain CBS 126529 (with 100 % identity) was HM038335 from 18(–19.5) × 3.5–4.5 µm, mean ± SD = 16.0 ± 1.8 × 4.0 ± 0.3 µm, Colletotrichum sp. isolate MFU 090619 from Capsicum annuum L/W ratio = 4.0, conidia of strain CBS 120708 smaller, measuring (chilli) from Laos (Phoulivong et al. 2010). Among the closest (12.5–)13–16(–18) × (3–)3.5–4 µm, mean ± SD = 14.6 ± 1.4 × 3.6 matches with the TUB2 sequence were 100 % identity matches ± 0.3 µm, L/W ratio = 4.1. with DQ454059–DQ454060 from Capsicum annuum isolates obtained in Thailand (Than et al. 2008a). One of these isolates is Culture characteristics: Colonies on SNA flat with entire margin, included in this study. Another 100 % match was with GU246633 hyaline, on filter paper pale olivaceous grey, on medium, filter from isolate R14 from Capsicum annuum in South Korea (Sang paper and Anthriscus stem partly covered with floccose whitish to et al. 2011). All of these strains are likely to belong to C. scovillei. pale olivaceous grey aerial mycelium and on Anthriscus stem with Based on the GAPDH sequence of strain LLB17, C. scovillei also few orange acervuli, reverse hyaline, rosy buff to greyish sepia, on occurs on Capsicum annuum in Taiwan (as part of group D3 in filter paper and Anthriscus stem partly fuscous black; growth rate Guerber et al. 2003). 22–22.5 mm in 7 d (33.5–35 mm in 10 d). Colonies on OA flat with entire margin; surface covered with short floccose whitish to pale Colletotrichum simmondsii R.G. Shivas & Y.P. Tan, Fungal olivaceous grey aerial mycelium, margin rosy buff, reverse rosy Diversity 39: 119. 2009. Fig. 29. buff, olivaceous grey to iron grey in the centre; growth rate19–20 mm in 7 d (33–35 mm in 10 d). Conidia in mass salmon. Sexual morph not observed. Asexual morph on SNA. Vegetative hyphae 1–5 µm diam, hyaline, smooth-walled, septate, branched. Material examined: Indonesia, from Capsicum sp., collection date and collector Chlamydospores not observed. Conidiomata absent, conidiophores unknown, (CBS H-20792 holotype, culture ex-type CBS 126529 = BBA 70349 = PD formed directly on hyphae on the surface of the medium and in 94/921-3). Thailand, Chiang Mai, Sansai, from anthracnose on fruit of Capsicum annuum (chilli), 2005, P.P. Than, culture CBS 120708 = HKUCC 10893. the aerial mycelium. Setae not observed. Conidiophores hyaline, smooth-walled, rather irregular in form, sometimes septate. Notes: Colletotrichum scovillei belongs to clade 2 of the C. acutatum Conidiogenous cells formed singly or in clusters of 2–3 apically species complex, and can be separated from other species by or as lateral branches of conidiophores, hyaline, smooth-walled, TUB2, GAPDH and ACT sequences, (with GAPDH being most cylindrical, thread-like, 7–23 × 1–2.2 µm, opening 0.5 µm diam, clearly differential), while CHS-1 and HIS3 sequences are the collarette sometimes visible, < 0.5 µm long, periclinal thickening same as those of C. guajavae. The conidia are slightly longer not observed, conidiogenous cells of other strains differ, e.g. than is typical for C. simmondsii and C. nymphaeae, with a larger conidiophores of CBS 294.67 are cylindrical, sometimes slightly length/width ratio. However, those characters are variable within inflated and usually wider than the ex-type strain, measuring the clade, and sequence data are required to distinguish between 4.5–18 × 1.5–4 µm, opening 1–1.5 µm diam, collarette 0.5–1 µm the constituent taxa on a reliable basis. long, periclinal thickening visible. Conidia hyaline, smooth-walled, The ex-type strain was included in the study of Nirenberg et aseptate, straight, cylindrical with one end round and one end acute or both ends acute, (4.5–)6.5–10(–11.5) × (2–)2.5–3.5(–4) al. (2002) as C. acutatum, and one of the strains studied (CBS 120708) was included in a paper on Colletotrichum diseases of chilli µm, mean ± SD = 8.1 ± 1.7 × 2.9 ± 0.4 µm, L/W ratio = 2.7, conidia in Thailand (Than et al. 2008a), in which ITS and TUB2 sequences of other strains differ in shape and size from the ex-type strain, e.g. were generated. The strain was identified there as C. acutatum, conidia of CBS 294.67 are cylindrical to fusiform with both ends a representative of one of two clades of that species complex acute and measure (6–)10.5–14(–16.5) × 3.5–4.5(–5.5) µm, mean associated with chilli. In drop inoculation tests, strains from that clade ± SD = 12.3 ± 1.8 × 4.0 ± 0.4 µm, L/W ratio = 3. Appressoria in loose groups or dense clusters of 2–6, medium brown, round, were found to cause typical anthracnose symptoms on chilli fruits. Two other species (or species complexes) were reported to cause elliptical to clavate in outline, the margine entire to undulate, (4.5–) disease of chilli by Than et al. (2008a), with isolates identified also as 6–9.5(–11.5) × (3.5–)4–6.5(–9.5) µm, mean ± SD = 7.8 ± 1.9 × 5.3 C. gloeosporioides and C. capsici. The latter taxon was found to be a ± 1.1 µm, L/W ratio = 1.5. synonym of C. truncatum by Damm et al. (2009). Other Colletotrichum Asexual morph on Anthriscus stem. Conidiomata not species were also reported from the C. boninese species complex, observed, conidiophores formed on aerial hyphae only. Setae not observed in the ex-type strain, but few setae observed in namely C. novae-zelandiae and C. karstii in New Zealand, both www.studiesinmycology.org 101 Damm et al . Fig. 29. Colletotrichum simmondsii (A–K, R-S from strain CBS 294.67. L–Q from ex-holotype strain CBS 122122). A–B. Conidiomata. C. Seta. D–K. Conidiophores. L–Q. Appressoria. R–S. Conidia. A, C–F, R. from Anthriscus stem. B, G–Q, S. from SNA. A–B. DM, C–S. DIC, Scale bars: A = 200 µm, B = 100 µm, D = 10 µm. Scale bar of D applies to C–S. strain CBS 294.67, medium brown, smooth-walled, 0–1-septate, surface covered with felty white aerial mycelium, becoming pale 20–40 µm long, base 2–3 µm diam, cylindrical, tip ± acute. olivaceous grey towards the centre, margin white or rosy buff, Conidiophores hyaline, smooth-walled, septate, branched, to 65 reverse dark olivaceous grey or salmon and purplish to iron-grey µm long. Conidiogenous cells hyaline, smooth-walled, cylindrical, towards the margin, growth 10–16 mm in 7 d (14–24 mm in 10 d), thred-like, 19–30 × 1 µm, opening 0.5 µm diam, collarette < 0.5 other strains differ from the type strain by growing faster, e.g. CBS µm long, periclinal thickening not observed, conidiogenous cells 294.67 grows 21–27 mm in 7 d (32.5–40 mm in 10 d). Conidia in of other strains differ, e.g. conidiophores of CBS 294.67 are mass not observed in the ex-type strain, those of other strains are cylindrical to slightly inflated and usually wider than the ex-type salmon-orange. strain, measuring 5–18 × 2.5–4.5 µm, opening 1–1.5 µm diam, collarette 0.5–1 µm long, periclinal thickening visible. Conidia Material examined: Australia, Queensland, Yandina, from fruit anthracnose of of Carica papaya, May 1987, L.M. Coates, culture ex-holotype CBS 122122 = BRIP hyaline, smooth-walled, aseptate, straight, cylindrical to fusiform 28519 = BCC 28680 = HKUCC 10928 = ICMP 17298 = KACC 43258; Queensland, with both ends acute or one end round and one end acute, (6–)7– Brisbane, Ormiston, from fruit rot of Carica papaya, 1959, J.H. Simmonds, culture 10(–12.5) × (2–)2.5–3.5(–4.5) µm, mean ± SD = 8.4 ± 1.5 × 3.0 ex-topotype of C. acutatum CBS 294.67 = BRIP 11084; Queensland, Brisbane, ± 0.5 µm, L/W ratio = 2.8, conidia of other strains differ in shape Nambour, from fruit rot of Fragaria × ananassa, 30 Mar. 1965, J.H. Simmonds, (according to BRIP database: K.G. Pegg), culture CBS 295.67 = BRIP 11086; and size from the ex-type strain, e.g. conidia of CBS 294.67 are Western Australia, Wanneroo, from rotting fruit of Fragaria × ananassa, collection cylindrical to fusiform with both ends acute and (11–)12–14.5(– date and collector unknown (deposited in IMI in 1992 by R.M. Floyd, Western 15.5) × (3–)4–4.5(–5) µm, mean ± SD = 13.3 ± 1.2 × 4.1 ± 0.4 Australia Department of Agriculture, Australia, No. WA 2768), culture IMI 354381 = µm, L/W ratio = 3.2. CPC 18923. USA, Hawaii, from Protea cynaroides, 8 Dec. 1998, P.W. Crous & M.E. Palm, culture CBS 114494 = STE-U 2964 = STE-U 2088. Culture characteristics: Colonies on SNA flat with entire margin, hyaline to to pale isabelline, on filter paper and on Anthriscus stem Notes: Colletotrichum simmondsii was described by Shivas & partly covered with short white to pale grey felty aerial mycelium, Tan (2009) to accommodate strains of the C. acutatum aggregate reverse of filter paper white to olivaceous grey, growth 10–16 assigned to group A2 by Sreenivasaprasad & Talhinhas (2005). The mm in 7 d (16–26 mm in 10 d), other strains differ from the type type of C. simmondsii was erroneously designated as an epitype strain by growing faster, e.g. CBS 294.67 grows 20.5–31 mm in of C. acutatum (i.e. s.str.) by Than et al. (2008b), before Shivas 7 d (34–40 mm in 10 d). Colonies on OA flat with entire margin; & Tan (2009) recognised that the two taxa are not conspecific. In 102 The CotriC ollet hum aCtum a ut species complex this paper C. simmondsii is accepted in a more restricted sense. Colletotrichum sloanei Damm, P.F. Cannon & Crous, sp. According to the TUB2 phylogeny in Shivas & Tan (2009, see fig. nov. MycoBank MB800515. Fig. 30. 2 of that paper), C. simmondsii includes strain BRIP 4684 from Capsicum, here identified as C. brisbanense, and sequences from Etymology: Named after Sir Hans Sloane (1660–1753), physician GenBank belonging to strains of C. laticiphilum (AY376556) and C. and noted natural history collector. His specimens formed a major nymphaeae (AY376551, AJ748607), as well as some strains from part of the original collections of the Natural History Museum in Litchi and Persea that could represent further segregate species of London, his Jamaican material of the host plant became Linnaeus’s the C. acutatum species complex. type of Theobroma cacao, and his recipe for a milk chocolate drink Conidial measurements of the type of C. simmondsii by was commercialised by the Cadbury brothers (Natural History Shivas & Tan (2009) are considerably larger (10–16 × 3.5–4.5 Museum, 2011). µm) than ours. It is possible that this discrepancy could be due to the different growth medium that they used (PDA) or the age of Sexual morph not observed. Asexual morph on SNA. Vegetative the culture. Measurements of all other strains studied in culture, hyphae 1–8.5 µm diam, hyaline to pale brown, smooth-walled, including strain CBS 294.67, also from papaya in Australia, more septate, branched. Chlamydospores not observed. Conidiomata closely approximate to the measurements for C. simmondsii given not developed, conidiophores formed directly on hyphae. Setae not by Shivas & Tan (2009). observed. Conidiophores hyaline to pale brown, smooth-walled, The ex-holotype strain (CBS 122122) of C. simmondsii has simple or septate and branched. Conidiogenous cells hyaline to pale restricted growth; all other isolates studied are much faster growing, brown, smooth-walled, cylindrical to conical, sometimes lacking a especially CBS 294.67 on OA. Than et al. (2008b) also remarked basal septum and continuous with the conidiophore, polyphialides on the slow growth rate of CBS 122122 (as BRIP 28519), giving also sometimes observed, discrete phialides measuring 8–24 × measurements of 2.3–2.6 mm (presumably per day). CBS 111531 2–3.5 µm, opening 1 µm diam, collarette 1–1.5 µm long, periclinal also differs, showing buff to olivaceous pigmentation on OA, and thickening visible. Conidia hyaline, smooth-walled, aseptate, straight, cylindrical to clavate with one end round and one end ± white aerial mycelium. acute, sometimes both ends ± acute, (8.5–)12–17(–22) × (3–)3.5– Pigments produced in PDA cultures may differ among species 4(–4.5) µm, mean 14.4 ± SD = 3.7 ± 2.5 × ± 0.3 µm, L/W ratio = in the C. acutatum complex. According to Shivas & Tan (2009) the 3.9. Appressoria single or in loose groups, medium brown, smooth- reverse of C. acutatum cultures are intensely carmine-red without walled, elliptical, subglobose to clavate in outline, entire, the edge flecking, while those of C. fioriniae pale pink with flecking. Reverses undulate or lobate, (4–)5–11(–17.5) × (4–)4.5–6.5(–8) µm, mean ± in C. simmondsii appear pale orange or yellow, without flecking. SD = 8.0 ± 3.0 × 5.4 ± 0.9 µm, L/W ratio = 1.5. We did not use PDA as a diagnostic growth medium, so a direct Asexual morph on Anthriscus stem. Conidiomata either not comparison cannot be made among studies, but we did not observe developed, conidiophores formed directly on hyphae or formed on substantial differences in colony reverse colours in OA cultures. a cushion of pale brown, angular, basal cells 2.5–6 µm diam. Setae It appears that culture pigmentation may change with extended not observed. Conidiophores hyaline to pale brown, smooth-walled, storage or subculturing, and we would be cautious about using septate, branched, to 40 µm long. Conidiogenous cells hyaline, these characters as diagnostic tools. In a study on C. acutatum smooth-walled, cylindrical to ± inflated, 9–18 × 2.5–4 µm, opening s. lat. from grape in Australia, Whitelaw-Weckert et al. (2007) 1–1.5 µm diam, collarette 1–1.5 µm long, periclinal thickening established a further molecular group beyond those recognised by distinct. Conidia hyaline, smooth-walled, aseptate, straight, Sreenivasaprasad & Talhinhas (2005), designated as A9. We have fusiform to cylindrical with both ends acute, (9–)11.5–15.5(–19.5) not examined their cultures, and the TUB2 sequences generated × (3–)3.5–4(–4.5) µm, mean ± SD = 13.4 ± 1.8 × 3.9 ± 0.3 µm, in Whitelaw-Weckert et al. (2007) are from a different region of L/W ratio = 3.5. the gene and could therefore not be compared with our TUB2 sequence data, but we suspect that their strains may be referable Culture characteristics: Colonies on SNA flat with entire margin, to C. simmondsii. The TUB2 sequence of the ex-type strain of C. hyaline buff to pale honey, on filter paper and Anthriscus stem simmondsii, CBS 122122, is identical with that of strain DAR32068 partly pale olivaceous grey to olivaceous grey, the medium, filter (group A9 in Whitelaw-Weckert et al. 2007) from strawberry in paper and Anthriscus stem partly covered with thin white aerial Australia as sequenced by Debode et al. (2009, EU635505), which mycelium, reverse same colours; growth rate 21–24 mm in 7 d supports this hypothesis. (31–34 mm in 10 d). Colonies on OA flat with entire margin; surface Colletotrichum simmondsii is separable from other species iron-grey to black with a buff margin, partly covered with thin felty by GAPDH and TUB2 sequencing, with TUB2 more strongly white aerial mycelium and orange acervuli arranged in a few rings diagnostic, while ACT, HIS3 and CHS-1 sequences are the same at the margin, reverse olivaceous grey with a buff margin; growth as those of C. paxtonii. A blastn search with the TUB2 sequence of rate 21–22.5 mm in 7 d (31–32.5 mm in 10 d). Conidia in mass CBS 122122 resulted in 100 % matches with a number of different salmon to orange. sequences, including some from the main clade of C. simmondsii seen in the phylogeny of Shivas & Tan (2009, see fig. 2 of that Material examined: Malaysia, Borneo, Sabah, Tuaran, from leaf of Theobroma paper), HE573031 from strain ITEM 13492 from Arbutus unedo cacao, 1994, A.R. Rossman and C.L. Bong, (IMI 364297 holotype, CBS H-20796 in Italy (Polizzi et al. 2011), AJ748635 from strain PD 89/582 (= isotype, culture ex-type IMI 364297). CBS 126524) from Cyclamen sp. Netherlands (Talhinhas et al. 2005), and FJ907443 from strain BRIP 28519 (= CBS 122122, ex- Notes: A representative of the C. acutatum species complex does holotype) as generated by Prihastuti et al. (2009). not previously appear to have been associated with Theobroma cacao. Three species from the C. gloeosporioides species complex, C. ignotum, C. theobromicola and C. tropicale were recognised as endophytes of T. cacao by Rojas et al. (2010). Two of these www.studiesinmycology.org 103 Damm et al . Fig. 30. Colletotrichum sloanei (from ex-holotype strain IMI 364297). A–B. Conidiomata. C–J. Conidiophores. K–P. Appressoria. Q–R. Conidia. A, C–E, Q. from Anthriscus stem. B, F–P, R. from SNA. A–B. DM, C–R. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–R. species were considered to have potential to protect host plants setae described for these two species is reminiscent of species in from Phytophthora diseases. All have been reviewed by Weir et al. the C. gloeosporioides complex. (2012, this issue). Colletotrichum theobromae forms oblong, straight conidia Further Colletotrichum species have been described from with obtuse ends, measuring 9–12 × 3–5 µm, and dark-brown, pluriseptate, acute setae measuring 60–75 × 3 µm (Saccardo T. cacao, including C. brachytrichum from leaves of T. cacao in Trinidad. This species has conidia that are ovoid-cylindrical with 1906). It was found on fruits of T. cacao in Cameroon, and also does an attenuated base and a round apex, measuring 10–13.5 × not agree in character with C. sloanei. Gloeosporium theobromicola 3–3.7 µm; it produces sparse setae that are dark brown, aseptate, [as “theobromicolum”], from fruits of T. cacao in Brazil, forms slightly flexuous and 40 × 3.5 µm, as well as conidiogenous cells conidia that are hyaline, fusoid and 6–9 × 2–2.5 µm, (Saccardo et measuring 4 × 2 µm (Saccardo 1906). In contrast, C. sloanei forms al. 1931). These are considerably smaller than those of C. sloanei. larger conidia averaging 14.4 × 3.7 µm on SNA and 13.4 × 3.9 µm This organism may not be a species of Colletotrichum. on Anthriscus stem. No setae were found in cultures of C. sloanei None of the species previously described on T. cacao originates (though these may only form on host material) and its conidiogenous from Asia, and all known species from other parts of the world differ cells are much longer than those of C. brachytrichum. from C. sloanei. Rojas et al. (2010) noted several unidentified taxa Colletotrichum cradwickii, described from branches of T. amongst their collections from T. cacao from Panama, but based cacao in Jamaica, forms conidia that are hyaline (red in mass), on ITS sequence data, none of them belongs to the C. acutatum species complex. They also isolated C. gloeosporioides s. lat. and elongate, constricted in the middle, and 14–17 × 5 µm, with setae that are straight, rigid, acute, 2–3-septate, purplish and 70–100 a strain belonging to the C. boninense species complex (CBS × 4–6 µm in size (Saccardo & Trotter 1913). Colletotrichum 124951); the latter was identified as C. karstii by Damm et al. luxificum was collected from branches, buds and fruits of T. (2012, this issue). cacao in Surinam and Demerara (now Guyana). It formed ovoid- Colletotrichum sloanei may be separated from other species oblong conidia, sometimes slightly constricted in the centre, by TUB2, ACT, GAPDH and HIS3 sequences. It is most easily with both sides rounded, smooth, and 13–19 × 4–5 µm. Setae distinguished with TUB2, HIS3 and ACT. With GAPDH there is only were formed that were described as 2–4-septate, 50–120 × 3.5– one bp difference from C. paxtonii, while the CHS-1 sequence is 4.5 µm (Saccardo & Trotter 1913). Although the larger size is the same as that of C. walleri. Closest matches in a blastn search discrepant, the constriction of the conidia and the formation of with the TUB2 sequence of strain IMI 364297 (with 99 % identity, 104 The CotriC ollet hum aCtum a ut species complex Fig. 31. Colletotrichum tamarilloi (from ex-holotype strain CBS 129814). A–B. Conidiomata. C–J. Conidiophores. K–P. Appressoria. Q–R. Conidia. A, C–E, Q. from Anthriscus stem. B, F–P, R. from SNA. A–B. DM, C–R. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–R. 2 or 3 bp differences) were GU183300, GU183299 and GU183295 discrete phialides measure 8–18 × 2.5–3.5 µm, opening 1–1.5 from C. simmondsii strains from Litchi chinensis in Australia µm diam, collarette distinct, 1–1.5 µm long, periclinal thickening (Shivas & Tan 2009). There are no strains from Litchi included conspicuous. Conidia hyaline, smooth-walled, aseptate, straight, in our analyses, but according to the TUB2 tree in Shivas & Tan cylindrical to fusiform with both ends acute, sometimes clavate with (2009), they probably belong to C. simmondsii s. str. The closest one round and one acute end, (8.5–)11.5–14.5(–15) × (2.5–)3–4(– match with the GAPDH sequence of strain IMI 364297 covering 4.5) µm, mean ± SD = 13.0 ± 1.4 × 3.5 ± 0.4 µm, L/W ratio = 3.7. ± the full length sequence (with 98 % identity, 6 bp differences) Appressoria single, medium brown, smooth-walled, subglobose, was HQ846719 from an unnamed plant, probably from India elliptical or clavate, the edge entire, rarely slightly undulate, (4–)5– (Chowdappa P, Chethana CS, Madhura S, unpubl. data). Closest 10.5(–16) × (3.5–)4.5–6.5(–8) µm, mean ± SD = 7.8 ± 2.6 × 5.5 ± matches with the ITS sequence (with 99 % identity, 1 bp difference) 0.9 µm, L/W ratio = 1.4. were 25 sequences, that are not listed here. Asexual morph on Anthriscus stem. Conidiomata acervular, conidiophores formed on thick-walled, pale brown, angular, basal Colletotrichum tamarilloi Damm, P.F. Cannon & Crous, sp. cells 4–8 µm diam. Setae not observed. Conidiophores hyaline to pale brown, smooth-walled, septate, branched, to 50 µm long. nov. MycoBank MB800516. Fig. 31. Conidiogenous cells hyaline, smooth-walled, cylindrical, sometimes polyphialidic, 10–21 × 2–4 µm, opening 1–1.5 µm diam, collarette Etymology: Named after the host plant tamarillo (Solanum distinct, 1–2 µm long, periclinal thickening conspicuous. Conidia betaceum). hyaline, smooth-walled, aseptate, straight, cylindrical to fusiform Sexual morph not observed (structures that are possibly immature with both ends acute, (10.5–)12–16(–22) × (3–)3.5–4.5(–5) µm, mean ± SD = 14.0 ± 1.9 × 4.0 ± 0.4 µm, L/W ratio = 3.5. Conidia ascomata were seen on Anthriscus stem). Asexual morph on of CBS 129955 and CBS 129811 differ in having slightly longer SNA. Vegetative hyphae 1–5.5 µm diam, hyaline to pale brown, conidia, measuring (11.5–)13.5–17(–18.5) × 3.5–4(–4.5) µm, mean smooth-walled, septate, branched. Chlamydospores not observed. Conidiomata not developed, conidiophores formed directly on ± SD = 15.3 ± 1.7 × 3.8 ± 0.3 µm, L/W ratio = 4.0. hyphae. Setae not observed. Conidiophores hyaline, smooth- walled, septate, branched, to 30 µm long. Conidiogenous cells Culture characteristics: Colonies on SNA flat with entire margin, hyaline to pale honey, on filter paper partly pale olivaceous grey hyaline smooth-walled, cylindrical to ± inflated, often integrated, www.studiesinmycology.org 105 Damm et al . to olivaceous grey, filter paper Anthriscus stem and medium partly Andes. They formed two different subgroups within C. acutatum covered with felty white aerial mycelium (and salmon acervuli), based on ITS sequence data. The isolates from lupins were reverse same colours; growth rate 17.5–21.5 mm in 7 d (28.5–31.5 pathogenic to tamarillo and vice versa, but lupin and tamarillo mm in 10 d). Colonies on OA flat with entire margin; surface honey, isolates were each more virulent to their own hosts. ITS sequence isabelline to olivaceous, almost entirely covered by felty white to of the ex-type strain of C. tamarilloi, CBS 129814, matched with pale olivaceous grey aerial mycelium, reverse buff, olivaceous, 100 % identity with JN543070 from isolate Tam7 from tamarillo, as pale olivaceous grey, olivaceous grey to iron-grey, growth rate well as JN543066 from isolate Lup28 from L. mutabilis in Ecuador 16–18 mm in 7 d (26–29 mm in 10 d). Conidia in mass salmon. (Falconi et al. 2012). The closest TUB2 blastn matches for CBS 129814 (with 99 Material examined: Colombia, Cundinamarca, from fruit anthracnose of Solanum % identity, 4 bp differences) were FN611029 and FN611028 from betaceum, 13 Aug. 2010, J. Molina, (CBS H-20726 holotype, culture ex-type CBS isolates DPI and CS-1 from Citrus aurantifolia and Citrus sinensis 129814 = T.A.6); Cundinamarca, from anthracnose on a fruit of Solanum betaceum, from USA, Florida (Ramos et al. 2006). The closest GAPDH 13 Aug. 2010, J. Molina, culture CBS 129811 = T.A.3; Antioquia, Santa Rosa, from a matches (with 97 % identity) were EU647323 from leatherleaf fern flower of Solanum betaceum, 1998, collector unknown, CBS H-20728, culture CBS 129955 = Tom-12. and EU168905, EU647318 and EU647319 from sweet orange isolates, all from Florida, USA (Peres et al. 2008, MacKenzie et Notes: Afanador-Kafuri et al. (2003) identified several strains from al. 2009). tamarillo in Colombia as C. acutatum, three of which are included in this study. Sreenivasaprasad & Talhinhas (2005) recognised these Colletotrichum walleri Damm, P.F. Cannon & Crous, sp. strains as a separate molecular group, A8, closely related to A1 (C. nov. MycoBank MB800517. Fig. 32. lupini). Colletotrichum tamarilloi can be separated from other species Etymology: Named after J.M. Waller, tropical pathologist extra- using CHS-1, HIS3, TUB2 and GAPDH sequences, most effectively ordinaire and a key worker on the most important Colletotrichum with GAPDH, and forms a uniform cluster even with six genes (Fig. pathogen of coffee. 1). Afanador-Kafuri et al. (2003) observed uniformity of banding patterns with apPCR, RAPD-PCR and A+T-rich DNA analyses of Sexual morph not observed. Asexual morph on SNA. Vegetative the strains they studied. They speculated that selection for clonality hyphae 1–6 µm diam, hyaline, smooth-walled, septate, branched. and homogeneity had occurred among the isolates, all of which Chlamydospores not observed. Conidiomata not developed, were collected in one region in Colombia where only one cultivar conidiophores formed directly on hyphae. Setae not observed. of the host was cultivated. Conidia of C. tamarilloi are uniformly Conidiophores hyaline, smooth-walled, septate, branched, to 70 fusiform on SNA, and almost so on Anthriscus stem, while C. lupini µm long. Conidiogenous cells hyaline, smooth-walled, cylindrical to forms conidia that are usually clavate on SNA and cylindrical on ampulliform, 10–14 × 3–4 µm, opening 1–1.5 µm diam, collarette the stems. Additionally, we found that appressoria of C. lupini have 0.5–1 µm long, periclinal thickening distinct. Conidia hyaline, an undulate to lobate margin, while those of C. tamarilloi have an smooth-walled, aseptate, straight, cylindrical to fusiform with both entire or rarely slightly undulate edge. ends slightly acute or one end round, (6–10.5)15.5–(–19.5) × This species is only known on Solanum betaceum in Colombia. (3–)3.5–4.5(–5.5) µm, mean ± SD = 13.0 ± 2.7 × 4.0 ± 0.5 µm, There are no previously described species associated with this L/W ratio = 3.3. Appressoria single, medium brown, smooth-walled, host. Three Colletotrichum species are reported from tamarillo in elliptical, clavate, sometimes irregularly shaped, the edge entire or the USDA fungal databases (Farr & Rossman 2012): C. acutatum undulate, (4.5–)5.5–12.5(–18.5) × (3.5–)4.5–7.5(–10.5) µm, mean (Guerber et al. 2003, Gadgil 2005) and C. gloeosporioides (Gadgil ± SD = 9.0 ± 3.3 × 5.9 ± 1.4 µm, L/W ratio = 1.5. 2005) in New Zealand and C. simmondsii in Australia (Shivas & Tan Asexual morph on Anthriscus stem. Conidiomata either not 2009). None of these species/groups is identical with C. tamarilloi. developed, conidiophores formed directly on hyphae, or acervular, While C. lupini and C. tamarilloi form well-supported clusters, there conidiophores formed on pale brown, angular, basal cells 3.5–7 µm are several additional species and unnamed strains from various diam. Setae not observed. Conidiophores hyaline to pale brown, hosts in Central and South America, as well as in Florida that are smooth-walled, septate, branched, to 70 µm long. Conidiogenous closely related to C. lupini and C. tamarilloi. One of these is from cells hyaline to pale brown, smooth-walled, cylindrical, 12–23 tamarillo in the same locality in Colombia (CBS 129810). × 2.5–3 µm, opening 1–1.5 µm diam, collarette 0.5–1 µm long, A recently reported anthracnose pathogen of tamarillo in periclinal thickening visible to distinct. Conidia hyaline, smooth- the USA (Jones & Perez 2012) probably belongs to C. fioriniae walled, aseptate, straight, sometimes slightly curved, cylindrical to according to its ITS sequence (JN863589). The Colletotrichum fusiform with both ends ± acute or one end round, (10.5–)12–16(– strains available to us from tamarillo in Colombia and New Zealand 18.5) × 3.5–4(–4.5) µm, mean ± SD = 13.9 ± 1.8 × 4.0 ± 0.3 µm, belong to C. godetiae, C. tamarilloi and an unnamed strain related L/W ratio = 3.5. to C. tamarilloi (this study), as well as C. boninense, C. constrictum and C. karstii belonging to the C. boninense species complex Culture characteristics: Colonies on SNA flat with entire margin, (Damm et al. 2012, this issue). Yearsley et al. (1988) report C. hyaline, filter paper pale olivaceous grey, medium, filter paper and acutatum (s. lat.) infections of tamarillo in New Zealand; however Anthriscus stem covert with fely white aerial mycelium, reverse none of our tamarillo strains isolated from New Zealand belongs same colours; 21–24 mm in 7 d (31–34 mm in 10 d). Colonies on to the C. acutatum group. The strains from this host included in OA flat with entire margin; surface covert with felty or short floccose Guerber et al. (2003) and assigned to group F2 formed a clade with white to pale olivaceous grey aerial mycelium, reverse olivaceous strains described as C. johnstonii in this study. We did not find any grey to iron grey, olivaceous in the centre and white towards the species on tamarillo occurring in both Colombia and New Zealand. margin; 20–26 mm in 7 d (30.5–37.5 mm in 10 d). Conidia in mass Falconi & van Heusden (2011) studied Colletotrichum isolates salmon. collected from Lupinus mutabilis and tamarillo in the Ecuadorian 106 The CotriC ollet hum aCtum a ut species complex Fig. 32. Colletotrichum walleri (from ex-holotype strain CBS 125472). A–B. Conidiomata. C–H. Conidiophores. I–N. Appressoria. O–P. Conidia. A, C–E, O. from Anthriscus stem. B, F–N, P. from SNA. A–B. DM, C–P. DIC, Scale bars: A = 100 µm, C = 10 µm. Scale bar of A applies to A–B. Scale bar of C applies to C–P. Material examined: Vietnam, Buon Ma Thuot-Dak Lac, from leaf tissue of Coffea sequences, while sequences of other genes differ by only one bp arabica, unknown collection date, H. Nguyen, (CBS H-20795 holotype, culture ex- from those of other species. The CHS-1 sequence is the same as type CBS 125472 = BMT(HL)19). that of C. sloanei. The closest TUB2 blastn match for CBS 125472 (with 99 % identity, 5 bp differences) was GU246633 from isolate Notes: Species of the C. gloeosporioides species complex are R14 from Capsicum annuum from South Korea (Sang et al. 2011). well-known as pathogens of Coffea, especially the African coffee The closest GAPDH match for a sequence covering ± the full berry disease pathogen C. kahawae (Waller et al. 1993). Additional gene length (with 98 % identity, 4 bp differences) was HQ846724 Coffea-associated components of this species complex from from isolate OBP6 from an unnamed plant, probably from India Vietnam and Thailand have been studied by Nguyen et al. (2009) (Chowdappa P, Chethana CS, Madhura S, unpubl. data). The only and Prihastuti et al. (2009); see Weir et al. (2012, this issue) for 100 % match with the ITS sequence was FJ968601, the sequence further review. of the same isolate previously sequenced by Nguyen et al. (2009). Masaba & Waller (1992) commented that strains identified as C. acutatum may cause minor disease of ripening coffee berries. Kenny et al. (2006) and Nguyen et al. (2010) respectively isolated, DISCUSSION in Papua New Guinea and Vietnam, taxa in this species complex from coffee leaves, twigs and fruits. None of the Vietnamese Colletotrichum acutatum (in the broad sense) was originally isolates could infect undamaged coffee berries (Nguyen et al. distinguished using morphological characteristics. The primary 2010). One of the C. acutatum cultures studied by Nguyen et al. diagnostic feature was given as the possession of fusiform conidia (BMT(HL)19) was sent to CBS and a dried sample of this strain is with acute ends (Simmonds 1965). More detailed research has here designated as holotype of C. walleri. In this study, this is the only coffee isolate from Asia, while six other isolates from coffee, however shown that this characteristic is not absolute; while most originating from Africa and Central America, belong to three other strains of species within the C. acutatum complex have at least a species within the C. acutatum species complex (C. fioriniae , C. proportion of conidia with at least one acute end, it is common to acutatum s. str. and C. costaricense). Two of these strains were find significant variation in conidial shape within species and even included in the study by Waller et al. (1993). within individual strains. Conidia that are more or less cylindrical Colletotrichum walleri is separated from other species by are frequently encountered. The variation may have multiple almost all genes. It is most easily distinguished using HIS3 and ITS causes; in some circumstances it seems that secondary conidia www.studiesinmycology.org 107 Damm et al . are formed directly from the germ tube of a germinating primary and TUB2 DNA sequences), each of which was recognised here conidium, and these are smaller and more irregular in form than as comprising one or more separate species. These authors listed those from which they are derived (Buddie et al. 1999). Additionally, previously described groups that corresponded to their own groups, older strains, especially if they have been frequently subcultured, including the seven groups recognised by Lardner et al. (1999), A, may have conidia that are more variable in appearance than those B, C, D, E, Ga. miyabeana and C. acutatum f. pineum. The Lardner derived from recent stock. Nirenberg et al. (2002) observed that et al. groups were mainly distinguished by morphology, partial LSU shapes differed among conidia formed in acervuli and in the aerial sequences and RAPD banding patterns. Some of the strains from mycelium. The variation in conidial shape has led to species within Lardner et al. (1999) are included in the present study and we found the C. acutatum complex being incorrectly placed into synonymy that only some of them corresponded with the groups adopted by with other Colletotrichum species, primarily C. gloeosporioides Sreenivasaprasad & Talhinhas (2005). Colletotrichum acutatum – a legacy of the revision of the genus by von Arx (1957). His group A from Lardner et al. (1999) was regarded as corresponding work marked a new era in the understanding of Colletotrichum to group A5, but in our study, three of the four included strains of systematics (Cannon et al. 2012, this issue), but many of the C. acutatum group A – ICMP 1701, ICMP 12923 and ICMP 17991 synonymies proposed were inaccurate. – belonged to C. fioriniae (= group A3) and only one, ICMP 17992, In this study we found many species that had been considered belonged to C. acutatum (= group A5). At the same time, the three as synonyms of C. gloeosporioides by von Arx (1957) actually strains of C. acutatum group C, which was supposed to correspond belong to the C. acutatum species complex, including C. mahoniae, to Sreenivasaprasad & Talhinhas group A3, were shown to belong C. godetiae, Gm. phormii, Gm. lycopersici, and Gm. limetticola. to C. johnstonii, in the case of ICMP 12926 and IMI 357027, and Glomerella miyabeana, here treated as a synonym of the older C. to C. pyricola in the case of ICMP 12924. Colletotrichum acutatum salicis, was regarded as a forma specialis of Ga. cingulata by von group B was listed as corresponding to group A4, but the only strain Arx (1957). Species treated as synonyms of C. gloeosporioides by included here, ICMP 12921, is now the ex-type of C. acerbum. von Arx (1957) have also been found in the C. boninense species ICMP strains regarded as Ga. miyabeana, that is ICMP 12954– complex (Damm et al. 2012, this issue). There were 39 strains 12957, were confirmed here as C. salicis (= Ga. miyabeana). Our included in this study that had previously been identified as C. phylogenetic tree (see Fig. 1) attempts to portray the groupings of gloeosporioides or Ga. cingulata, based on morphology. These some of these earlier studies, mapped on to our own phylogeny. strains in fact belong to 14 species in or closely related to the C. This illustrates the problems encountered when one compares acutatum species complex, including C. acutatum, C. australe, C. groups established by different studies using different criteria for cosmi, C. costaricense, C. fioriniae, C. godetiae, C. limetticola, C. characterisation. lupini, C. melonis, C. nymphaeae, C. phormii, C. rhombiforme, C. Differences in pathogenicity of strains from different hosts have salicis and C. orchidophilum. been observed in several studies. Some fruit diseases caused Not all species of Colletotrichum with acute-ended conidia by the C. acutatum complex have been shown to be caused by belong to the C. acutatum complex. There are species with falcate distinct phylogenetic lineages (Peres et al. 2008), and strawberry conidia that belong to the C. graminicola species complex (Crouch fruit rot in particular was rarely found to be caused by isolates from et al. 2009). Also outside the C. acutatum complex are species heterogeneous hosts (Mackenzie et al. 2009). Cross-infection from herbaceous hosts with more or less curved conidia; these potential was tested by, to give a few examples, Bernstein et al. were previously regarded as C. dematium (Damm et al. 2009). In (1995), Freeman and Shabi (1996), Freeman et al. (2001b) and addition, the newly described C. pseudoacutatum forms straight Mackenzie et al. (2007). Cross-infection may occur in the field as conidia with acute ends but appears not to belong to the C. acutatum well as in the laboratory (Afanador-Kafuri et al. 2003). Freeman et species complex (Cannon et al. 2012, this issue). Conidial shape is al. (2001a) found that C. acutatum from strawberry is able to cause therefore not a uniform feature of the C. acutatum species complex. lesions on various fruits, both when the fruits are wounded and Bearing in mind the frequency with which strains from the C. when they are intact. In vitro infection studies by Whitelaw-Weckert acutatum species complex are encountered and their pathogenicity et al. (2007) revealed low host specificity among isolates that can to a wide range of crop plants, it would be surprising if earlier be assigned here to C. acutatum, C. simmondsii and C. fioriniae. names for C. acutatum did not exist. Walker et al. (1991) found The lack of perceived host specificity in the C. acutatum complex that C. xanthii (Halsted 1893) was synonymous with C. acutatum probably has multiple causes, but much of the difficulty rests with based on morphological criteria, but no authentic sequences are poor identification practice in pathology studies. Many investigations available and it is not clear at present in which clade this species even now avoid the inclusion of sequence-based evidence, or only fits. There was no interest at the time amongst Colletotrichum use ITS sequences, and only a few deposit adequate voucher researchers to replace the name C. acutatum, and now the name material. This means that name use is much less rigorous than is so widely used that a name change would be unlikely to gain it should be, leading to misleading results and poor comparability recognition. Other older taxa have been recognised as belonging to between studies. That said, it has to be acknowledged that many, if the C. acutatum complex, but as close relatives rather than formal not most of the species we now recognise via multigene analyses synonyms. Colletotrichum lupini was found to be an independent appear not to be restricted to particular plants. taxon within the C. acutatum complex by Nirenberg et al. (2002), One factor making interpretation of pathogenicity data difficult rather than belonging to the C. gloeosporioides aggregate as may be incomplete or misleading information on pathology for the assumed by Yang & Sweetingham (1998) and Elmer et al. (2001). strains we have studied. The stated plant/fungus association does Farr et al. (2006) found C. phormii (based on Fusarium phormii, not necessarily involve a pathogenic relationship: strains could be Hennings 1898) to be closely related to C. acutatum and stated isolated as benign endophytes or as secondary pathogens. There is that older reports of C. gloeosporioides as pathogens of Phormium much further work needed on the mechanisms of pathogenicity and could actually refer to C. phormii as well. on evolution at the population level, but it does appear that many Sreenivasaprasad & Talhinhas (2005) distinguished eight Colletotrichum species are unusually successful in overcoming distinct molecular groups within C. acutatum, A1–A8 (based on ITS multiple host barriers. 108 The CotriC ollet hum aCtum a ut species complex There is limited evidence of restricted geographical range complex. Speciation has taken place much more prolifically than for some of the species we accept here. For most species, the has been suspected so far. It seems likely that the C. acutatum number of strains available is too small to allow us to draw definite species complex is still evolving rapidly. The emergence of new conclusions. For example, except for C. lupini, all isolates of species is doubtless encouraged by the opportunities for mixing clade 1 (some of which are not recognised as separate species) of gene pools that are provided by modern global agricultural appear to have an origin restricted to Central and South America practices combined with imperfect phytosanitary regulation. and the southern USA. The globalisation of agriculture has in all probability led to frequent unrecognised introductions to new regions. The baseline information we have on native versus exotic ACKNOWLEDGEMENTS taxa is inadequate to allow introductions to be mapped. However, some of the apparently specific host-fungus connections could be We thank the curators and staff of the CABI and CBS culture collections as well as Dr Peter Johnston and Dr Bevan Weir (Landcare Research, Auckland, New supported further by tracing more strains from the respective hosts Zealand), Prof. dr Lilliana M. Hoyos-Carvajal (Faculty of Agronomy, Plant Health in future blastn searches, e.g. for C. scovillei and C. limetticola. Laboratory, Universidad Nacional de Colombia, Bogotá, Colombia), Dr Pedro Colletotrichum acutatum has been regarded as a pathogen of Talhinhas (Centro de Investigação das Ferrugens do Cafeeiro – IICT, Oeiras, countless host plant species, and also as occurring everywhere. Portugal), Riccardo Baroncelli (Warwick HRI, University of Warwick, UK), Prof. dr Lisa Vaillancourt (Department of Plant Pathology, University of Kentucky, USA), Sreenivasaprasad & Talhinhas (2005) discovered that C. acutatum Prof. dr María de Jesús Yáñez-Morales (Instituto de Fitosanidad, Colegio de group A5, here accepted as C. acutatum s. str., occurs only on certain Postgraduados, Montecillo, Mexico), Prof. dr Annemiek C. Schilder (Department hosts, mostly in the southern hemisphere. This study confirms that C. of Plant Pathology, Michigan State University, USA), Dr Sandra Lamprecht acutatum s. str. does in fact have multiple hosts, but the known host (Soilborne Plant Diseases Unit, Agricultural Research Council, Stellenbosch, South Africa), Y.P. Tan and Dr Roger G. Shivas (Plant Biosecurity Science, spectrum is much smaller than previously accepted. Ecosciences Precinct, Dutton Park, Queensland 4102, Australia), Dr Alan Wood Some host plants appear to be particularly susceptible to (Plant Protection Research Institute, Agricultural Research Council, Stellenbosch, infection by multiple Colletotrichum taxa. Occurrence of species on South Africa), Dr Carolyn Babcock (curator of the Canadian Collection of Fungal strawberry has been particularly well researched due to the former Cultures, Agriculture and Agri-Food Canada, Ottawa, Ontario, Canada), Dr Richard A. Humber (curator of the ARS Collection of Entomopathogenic Fungal status of C. acutatum as a regulated quarantine pathogen. We Cultures, USDA-ARS, Ithaca, NY, USA), Dr Stanley Freeman (Department of have found that strains from this host belong to six different clades Plant Pathology and Weed Research, The Volcani Center, Bet Dagan, Israel), Dr within the C. acutatum species complex, namely C. simmondsii Charles Lane (The Food and Environment Research Agency, Sand Hutton, York, (three strains from Australia), C. nymphaeae (38 strains, mostly UK), Hans de Gruyter (Plant Protection Service and National Reference Centre, from Europe and the USA), C. fioriniae (seven strains from New Wageningen, The Netherlands), Dr Ellis T.M. Meekes (Naktuinbouw, Research & Development, Roelofarendsveen, The Netherlands), Dr Jan Dijksterhuis (CBS- Zealand, UK and USA), C. godetiae (10 strains, all from Europe), C. KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands), Dr Katherine F. acutatum s. str. (one strain from Australia) and C. salicis (four strains LoBuglio (Harvard University Herbaria, Cambridge, Massachusetts, USA), Dr Lizel from New Zealand). In a study by MacKenzie et al. (2009), strains Mostert (Department of Plant Pathology, University of Stellenbosch, South Africa) from strawberry were shown to be more aggressive to strawberry and Dr Françoise Munot (Mycothèque de l’Université catholique de Louvain, Unité de Microbiologie, Louvain-la-Neuve, Belgique) for kindly supplying isolates for this than strains from Vaccinium. Based on TUB2 sequences generated study. We kindly thank the curators of the fungaria at the Royal Botanic Gardens by those authors, the strains from strawberry were assigned to in Kew, UK, at the US National Fungus Collections, Beltsville, Maryland, USA, of C. nymphaeae, and the strains from Vaccinium to C. fioriniae. the Botanic Garden and Botanical Museum Berlin-Dahlem, Freie Universität Berlin, Possibly the reason for apparent differences in pathogenicity, lie Berlin, Germany and of the Botanische Staatssammlung München (M), Germany for providing access to historical type specimens. This research was supported by not in the different hosts, but in the fact that the strains studied the Dutch Ministry of Agriculture, Nature and Food Quality through an endowment belong to different species. To our knowledge, C. acutatum s. str. of the FES programme “Versterking infrastructuur Plantgezondheid”. has rarely been found in Europe, and then mostly on ornamental plants. 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The Colletotrichum acutatum species complex

Studies in Mycology , Volume 73 (1) – Aug 22, 2012

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