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Evolution of within-colony distribution patterns of birds in response to habitat structure

Evolution of within-colony distribution patterns of birds in response to habitat structure Behav Ecol Sociobiol (2014) 68:851–859 DOI 10.1007/s00265-014-1697-8 ORIGINAL PAPER Evolution of within-colony distribution patterns of birds in response to habitat structure Piotr Minias Received: 10 December 2013 /Revised: 14 February 2014 /Accepted: 17 February 2014 /Published online: 4 March 2014 The Author(s) 2014. This article is published with open access at Springerlink.com . . . Abstract It has long been suggested that habitat structure Keywords Birds Ciconiiformes Coloniality Comparative . . affects how colonial birds are distributed within their nesting analysis Distribution Habitat structure aggregations, but this hypothesis has never been formally tested. The aim of this study was to test for a correlated evolution between habitat heterogeneity and within-colony Introduction distributions of Ciconiiformes by using Pagel’s general meth- od of comparative analysis for discrete variables. The analysis According to classic theoretical predictions on resource ac- indicated that central-periphery gradients of distribution quisition in animals, individuals should be distributed in en- (high-quality individuals occupying central nesting vironments so as to maximise their fitness. If there are no locations) prevail in species breeding in homogeneous habi- competitive asymmetries between conspecifics, the habitat tats. These were mainly ground-nesting larids and should be occupied proportionally to the available resources spheniscids, where clear central-periphery patterns were re- under the assumptions of the ideal free distribution model of corded in ca. 80 % of the taxa. Since homogeneous habitats Fretwell and Lucas (1970), which implies that the density of provide little variation in the physical quality of nest sites, individuals should increase along with the increasing quality central nesting locations should be largely preferred because of the habitat patch. However, in natural populations of ani- they give better protection against predators by means of more mals, individuals only rarely gain equal access to resources, as efficient predator detection and deterrence. By contrast, they notably differ in their competitive abilities. Conforming central-periphery gradients tended to be disrupted in hetero- to the empirical evidence on competitive asymmetries within geneous habitats, where 75 % of colonial Ciconiiform species populations, a model of ideal despotic distribution was pro- showed uniform patterns of distribution. Under this model of posed, assuming that dominant individuals have capacities to distribution, edge nest sites of high physical quality confer secure the best available territories and to relegate conspecifics higher fitness benefits in comparison to low-quality central of lower phenotypic quality to less attractive habitats (Fretwell sites, and thus, high-quality pairs are likely to choose nest sites 1972). irrespectively of their within-colony location. Breeding in Although there is abundant empirical evidence for ideal homogeneous habitats and uniform distribution patterns were despotic distributions in territorial birds (Andrén 1990;Ens identified as probable ancestral states in Ciconiiformes, but et al. 1995;Møller 1995; Petit and Petit 1996), information on there was a significant transition rate from uniform to central- the patterns of distribution in colonial species are much more periphery distributions in species occupying homogeneous scarce. Distribution patterns of colonial birds are typically habitats. considered on at least three different levels: (1) distribution of colonies in the available environment; (2) distribution of individuals among colonies; and (3) distribution of individuals within colonies. Large-scale patterns of colony distribution as Communicated by C. R. Brown well as distribution of individuals among the colonies located P. Minias (*) in the habitat patches of different quality have both recently Department of Teacher Training and Biodiversity Studies, University received increasing attention (Brown and Rannala 1995). It of Łódź, Banacha 1/3, 90-237 Łódź, Poland has been demonstrated that the foundation of new colonies in e-mail: pminias@biol.uni.lodz.pl 852 Behav Ecol Sociobiol (2014) 68:851–859 several avian species follows a despotic model (Serrano and sites of good physical quality considerably exceeds benefits Tella 2007;Oro 2008) and that individuals of low phenotypic associated with the central nesting position, then high-quality quality (expressed by young age or poor physical quality) may pairs may choose the best available nesting sites independent- be excluded from colonies that are located in the best habitat ly of their location in a colony (Velando and Freire 2001). patches (Rendón et al. 2001). Under such circumstances, the central-periphery patterns By contrast, much less empirical data has been collected on could be disrupted and pairs of varying quality could be the distribution of individuals within their breeding colonies. distributed more or less uniformly among the central and Despite this relative scarcity of information, it seems safe to peripheral zones of colonies. distinguish two major components of nesting site attractive- Although the effects of habitat heterogeneity on the within- ness that may have important fitness consequences for colo- colony patterns of distribution in birds have long been nially breeding species and that, consequently, are likely to hypothesised, most of the empirical evidence has only been determine within-colony distribution patterns. The first of the circumstantial and the suggested relationship has never been components is associated with the within-colony location of supported by a formal analysis. The aim of this study was to nest sites, as it is generally accepted that the centres of colo- test for evolutionary correlations between the structure of nies offer the highest benefits in terms of fitness (Coulson breeding habitat and within-colony distributions in 1968; Aebischer and Coulson 1990). It has been commonly Ciconiiformes (sensu Sibley and Ahlquist 1990), a phyloge- reported that pairs nesting in the centres are likely to achieve netic group with the highest prevalence of coloniality among higher breeding success due to decreased predation-related birds (Siegel-Causey and Kharitonov 1990). According to the losses of eggs and chicks (Götmark and Andersson 1984; theoretical predictions, I expected that birds nesting in homo- Yorio and Quintana 1997; Minias and Kaczmarek 2013), thus geneous habitats should form colonies according to the indicating that colonies may act as selfish herds against pre- central-periphery model of distribution, whereas in heteroge- dation (Brown and Brown 2001). The mechanisms explaining neous habitats, the central-periphery gradients should be lower susceptibility of central pairs to predation may include disrupted (uniform model of distribution). more efficient detection and deterrence of predators in the central parts of colonies. Central nests are also likely to be less accessible to predators, although this may largely depend on the type of predator (Brunton 1997). However, in general, Methods there is large empirical support that colonial birds dilute the risk of predation (Brown and Brown 2001) and that central For the purpose of the analysis, I collected data from the nesting sites are by far the most efficiently protected sites literature for 34 colonial species of Ciconiiformes grouped against predators. Although the breeding success of centrally into nine families (Table 1). Each species was assigned a nesting pairs may be decreased due to density-dependent prevailing model of within-colony distribution: central- intraspecific interactions (Jovani and Grimm 2008; periphery or uniform. The central-periphery model was Ashbrook et al. 2010) and parasitic rates (Tella 2002), many assigned when all studied reproductive parameters or parental studies have demonstrated higher reproductive output in col- quality traits declined from the centre of the colony towards ony centres in comparison to the edges (Patterson 1965; the peripheries. In contrast, the uniform model corresponded Gochfeld 1980; Becker 1995; Vergara and Aguirre 2006). to a situation in which the central-periphery gradients were For this reason individuals of higher quality are likely to disrupted, at least with respect to some of the studied traits or occupy the best central sites and to relegate individuals of in some of the studied colonies. With such an approach, the lower quality to less attractive edge sites. Assuming such a distribution patterns could be coded binarily, with central- despotic mechanism of colony formation, one would expect a periphery distributions denoted as 0 and distributions in which central-periphery pattern of distribution where the phenotypic central-periphery gradients were disrupted (uniform models) quality of breeding birds declines from the centre towards the denoted as 1. Heterogeneity of the breeding habitat was also edges of a colony (Coulson 1968). treated as a categorical variable with two states. Bare ground The physical quality of nesting sites may be considered as and mats of floating vegetation were identified as homoge- the second major component of their attractiveness for colo- neous habitats, as these provide none or negligible variation in nial birds. If the habitat is heterogeneous on a small spatial the physical quality of nesting sites and all nests are more or scale, considerable variation in the physical quality of nesting less equally vulnerable to predators or adverse weather con- sites within colonies is expected. Under this assumption, nest ditions (denoted as 0). All of the other habitats that may sites of high quality would be likely to provide much more provide moderate or considerable variation in the physical effective protection against predators or adverse weather con- quality of nesting sites were considered to be heterogeneous ditions and thus would promote higher reproductive success. habitats (denoted as 1). This category mostly included rocky It has been suggested that if the fitness benefits of nesting in habitats (cliff ledges, rocky slopes and islets, rock crevices, Behav Ecol Sociobiol (2014) 68:851–859 853 Table 1 Patterns of within-colony distribution and nesting habitat of colonial Ciconiiform species Species Distribution Habitat Parameters Authors Spheniscidae Aptenodytes patagonicus U Ground BD (C-P) Côté 2000 BD, RS (C-P) Bried and Jouventin 2001 AS, RS (U) Decamps et al. 2009 Eudyptes chrysocome C-P Ground RS Hull et al. 2004 Spheniscus magellanicus C-P Ground CS, S, RS Gochfeld 1980 S, RS Frere et al. 1992 Pygoscelis antarcticus C-P Ground AM Mínguez et al. 2001 BD Barbosa et al. 1997 Pygoscelis adeliae C-P Ground RS Taylor 1962 CS, RS Tenaza 1971 BD, CS Spurr 1975 CS, S Davis and McCaffrey 1986 Procellaridae Thalassarche melanophris C-P Ground RS Forster and Phillips 2009 Pelecanidae Pelecanus occidentalis C-P Ground AA, CS, RS Blus and Keahey 1978 Ciconiidae Ciconia ciconia C-P Trees AA, RS Vergara and Aguirre 2006 Ardeidae Nycticorax nycticorax U Trees CS (U); RS (C-P) Uzun 2009 Bubulcus ibis U Trees S (C-P) Siegfried 1972 HS (U) Ranglack et al. 1991 CS (U) Samraoui et al. 2007 Ardea cinerea U Trees RS Van Vessem and Draulans 1986 Egretta garzetta U Trees CS (U); RS (C-P) Uzun and Kopij 2010 Phalacrocoracidae Phalacrocorax atriceps URocks AA Shaw 1985 RS Svagelj and Quintana 2011 Phalacrocorax aristotelis U Rocks RS Velando and Freire 2001 Phalacrocorax pelagicus U Cliff BD, AA Siegel-Causey and Hunt 1986 Phalacrocorax carbo U Trees RS (U) Grieco 1994 BD (C-P) Andrews and Day 1999 BD, RS (C-P); Minias et al. 2012a CS (U) BD, CC, RS, S (C-P); CS (U) Minias and Kaczmarek 2013 Phalacrocorax auritus C-P Trees BD Léger and McNeil 1987 Sulidae Morus capensis C-P Ground AA, RS Staverees et al. 2008 Morus serrator U Ground BD, AA (C-P) Gibbs et al. 2000 AA (U) Pyk et al. 2008 Sula variegata U Rocks BD Duffy 1983 Sula leucogaster U Rocks RS Ospina-Alvarez 2008 Accipitridae Pandion haliaetus C-P Trees RS Hagan and Walters 1990 Laridae Hydroprogne caspia C-P Ground BD, RS Antolos et al. 2006 Sternula antillarum U Ground HS, S, RS Brunton 1997 Thalasseus maximus C-P Ground BD, S Buckley and Buckley 1977 854 Behav Ecol Sociobiol (2014) 68:851–859 Table 1 (continued) Species Distribution Habitat Parameters Authors Chlidonias hybridus C-P Floating vegetation CS Minias et al. 2011 CGR Minias et al. 2012b S Minias et al. 2013 Sterna dougallii C-P Ground BD Ramos 2002 Sterna hirundo C-P Ground BD, S, RS Becker 1995 Chroicocephalus ridibundus C-P Ground RS Patterson 1965 Rissa tridactyla U Cliff AS (C-P) Coulson and Wooller 1976 RS (U) Wooller and Coulson 1977 S (C-P); RS (U) Regehr et al. 1998 AS (C-P) Aebischer and Coulson 1990 Larus atricilla C-P Ground BD, CS, S, RS Montevecchi 1978 Larus delawarensis U Ground AA (C-P) Ludwig 1974 HS, S, RS (C-P) Dexheimer and Southern 1974 AA (C-P) Ryder 1975 BD, CS, HS, RS (U) Ryder and Ryder 1981 BD, AA (C-P) Haymes and Blokpoel 1980 Larus californicus C-P Ground RS, AA Pugasek and Diem 1983 Larus argentatus C-P Ground BD Burger and Shisler 1980 Central-periphery (C-P) and uniform (U) patterns were assigned to within-colony distributions of the following traits: BD breeding date, CS clutch size, HS hatching success, RS reproductive success, S brood survival, CGR chick growth rates, CC chick condition, AS adult survival, AA adult age, AM adult morphology. If different, the patterns of distribution were indicated in parentheses separately for each reported reproductive/quality trait or for each studied colony hollows and burrows) and vegetated habitats (woodlands and 1994), and it has been demonstrated that it does not bias the shrubs). results qualitatively (Møller et al. 1998;Nunn 1999). Since data from different species are not independent due To test for a correlated evolution between breeding habitat to their shared ancestral states, it is widely acknowledged that structure and within-colony distribution patterns, I used comparative analyses must control for the phylogeny. I based Pagel’s discrete variable method (1994) which uses the my phylogenetic tree on the classification of Sibley and continuous-time Markov model in order to characterise evo- Ahlquist (1990). This phylogeny is uniquely available for lutionary changes in selected pairs of variables along each the entire order of Ciconiiformes, and for this reason, it was branch of the phylogenetic tree. The method compares the fit used to branch the families of my tree (Fig. 1). Although the of two different models assuming an either independent or phylogeny of Sibley and Ahlquist (1990) was once considered dependent (the rate of change of one trait depends on the controversial (Sheldon and Gill 1996), it is now assumed as background state of the other) evolution of traits. The models quite robust for phylogenetic analyses in birds (reviewed in were fitted using maximum likelihood and compared using Mooers and Cotgreave 1994), and hence, it has been broadly the likelihood ratio (LR) statistic, which is expressed as LR=2 used in comparative studies (Cézilly et al. 2000;Dubois and (logL −logL ), where L is the likelihood of the model (D) (I) (D) Cézilly 2002;Garamszegietal. 2005; Olson et al. 2008), that allows the traits to evolve in a correlated fashion and L is (I) including those on avian coloniality (Rolland et al. 1998; the likelihood of the independent model. The LR statistic is Varela et al. 2007). In order to branch the genera and species, asymptotically distributed as χ with four degrees of freedom I used five phylogenies based on both molecular and morpho- for this test (Pagel 1997). logical data (Sheldon 1987; Kennedy et al. 2000;Thomas The discrete variables method was also used to estimate the et al. 2004; Bertelli and Giannini 2005; Smith 2010). Since ordering and direction of the evolutionary changes of the two different approaches were used to construct the above phy- analysed variables (so-called temporal order tests). For this logenies, I decided not to control for branch lengths, which purpose, one needs to fit reduced models in which a certain followed from other comparative studies (Dubois et al. 1998; rate of evolutionary transition q is excluded a priori (set to 0). ij Rolland et al. 1998; Cézilly et al. 2000; Varela et al. 2007). The constrained seven-parameter models are then compared Setting equal branch lengths is considered conservative (Pagel to the full eight-parameter model which tests the hypotheses Behav Ecol Sociobiol (2014) 68:851–859 855 Fig. 1 Phylogenetic tree of 34 colonial species from nine Ciconiiformes families involved in the study whether the specified transition rates differ significantly from proportion was found between the number of species that zero. The tests are asymptotically distributed as χ with one exhibited central-periphery distribution within colonies and degree of freedom (Pagel 1994). In this manner, the evolution those in which central-periphery gradients were disrupted (56 between the ancestral states and the derived states of both vs. 44 %, Table 1). There was a clear tendency for species selected variables may be traced. For root reconstruction of breeding in homogeneous habitats to be distributed central- ancestral states, I used the maximum-likelihood reconstruc- peripherally within the colonies (Fig. 2). The log-likelihood of tion method of Pagel (1999). All analyses were performed the model of independent evolution was estimated at L = with BayesTraits (Pagel and Meade 2008). −36.10 and was significantly lower in comparison to the likelihood of the dependent model L =−30.18 (χ =11.83, df=4, P=0.019). Such results support the hypothesis of a Results correlated evolution between preferences for heterogeneous breeding habitats and uniform patterns of within-colony Among the 34 taxa used for the analysis, there were 20 species distribution. that nested in homogeneous habitats (59 %) and 14 that chose Breeding in homogeneous habitats and uniform distribu- heterogeneous habitats for breeding (41 %). A similar tion of pairs within colonies were identified as ancestral states 856 Behav Ecol Sociobiol (2014) 68:851–859 mechanisms which may explain lower predation rates at these locations include: (1) restricted accessibility for predators (Siegel-Causey and Hunt 1981); (2) more efficient communal defence (Elliot 1985); (3) more efficient detection of predators (Roberts 1996); and (4) lower probability of being depredated due to the dilution effect (Murphy and Schauer 1996). By contrast, heterogeneous habitats were found to disrupt the central-periphery patterns of distribution within colonies. In habitats of moderate or high heterogeneity, edge nest sites of high physical quality are likely to confer higher fitness benefits in comparison to low-quality central sites. Thus, high-quality pairs are expected to choose nest sites irrespectively of their within-colony location, and thus, they Low High are expected to be uniformly distributed among the central and Habitat heterogeneity peripheral zones of colonies. Central-periphery distributions Fig. 2 Number of species exhibiting central-periphery (grey area)and uniform (white area) patterns of within-colony distribution with respect to were found to be disrupted in nearly 75 % of colonial the heterogeneity of breeding habitat Ciconiiformes species that nested in heterogeneous habitats. It seems that uniform patterns of distribution are especially with a probability of 94.8 %. I found a significant rate of common in birds that establish colonies on cliffs or in other transition from uniform to central-periphery distribution in rocky habitats, including various Phalacrocoracidae and species that bred in homogeneous habitats (χ =4.54, df=1, Sulidae species. Nesting sites such as crevices under fallen P=0.033). I also found a significant rate of reversed transi- rocks, open ground caves and open ledges on cliffs usually tions, i.e. from central-periphery to uniform patterns of distri- show great variation in their physical quality and attractive- bution (χ =7.50, df=1, P=0.006). The rate of evolution from ness for birds; for example, a clear preference for sites with breeding in homogeneous to heterogeneous habitats with no more lateral and overhead cover, with better drainage and with change in the background state of uniform distribution pattern better visibility has been demonstrated for the European Shag was not significant (χ =1.14, df=1, P=0.29), but it cannot be Phalacrocorax aristotelis (Velando and Freire 2003). Such excluded that this could have resulted from the low power of physical characteristics of nesting sites have been shown to the test. All the other transition rates were also non-significant provide more effective protection against predators and to (all P>0.05). prevent broods from flooding, unfavourable atmospheric con- ditions and intra-specific inference, which greatly affected the hatching success of Shags (Velando and Freire 2003). The Discussion distribution of birds within the same colony of Shags did not conform to the assumptions of the central-periphery model, as This study was the first to formally demonstrate a link be- individuals of different quality were distributed despotically tween within-colony distribution patterns in birds and the among the sites of varying physical quality (Velando and structure of preferred nesting habitat by using comparative Freire 2001, 2003). analysis. It was shown that as much as 85 % of colonial Disruptions in the central-periphery patterns of distribution Ciconiiformes species which breed in homogeneous habitats were also recorded in several waterbird species associated tend to show clear central-periphery patterns of distribution with woodland habitats; although, this kind of environment within their colonies and that these are mostly ground-nesting is expected to provide only moderate variation in the physical species from the Spheniscidae and Laridae families. In gener- quality of nesting sites, most commonly expressed by varia- al, bare-ground habitats, such as sandy islands or dunes, tion in tree height and canopy structure. In several tree-nesting provide no apparent variation in the physical quality of the colonial avian species, tree height was identified as an impor- nesting sites. Under such conditions, each nest site is likely to tant predictor of reproductive success and was suggested to be equally exposed to predation and inclement weather. determine accessibility of nests to ground and tree-dwelling Consequently, nest-site selection patterns should evolve to- predators (Post 1990; Childress and Bennun 2000). The wards choosing an appropriate location within the colony, breeding success of the Scarlet Ibis Eudocimus ruber corre- where pressure coming from predators will be minimised. lated positively with nest cover by overhanging branches Assuming that all nest sites are physically similar, the highest (Olmos 2003), and the study on Cattle Egrets Bubulcus ibis fitness benefits are expected to be acquired via nesting in the indicated higher fledging success in pairs nesting close to the central parts of colonies (Coulson 1968). As colony centres trunks of trees (Si Bachir et al. 2008). However, in some cases, the fitness benefits that were associated with nesting in the are usually associated with higher nesting densities, the No of species Behav Ecol Sociobiol (2014) 68:851–859 857 Cézilly F, Dubois F, Pagel M (2000) Is mate fidelity related to site sites of high physical quality could be acquired via mecha- fidelity? A comparative analysis in Ciconiiformes. Anim Behav nisms not related to anti-predatory protection; for example, in 59:1143–1152 the tree-nesting subspecies of Great Cormorant Childress RB, Bennun LA (2000) Nest size and location in relation to Phalacrocorax carbo sinensis, the physical quality of nesting reproductive success and breeding timing of tree-nesting Great Cormorants. Waterbirds 23:500–505 sites (tree height) determined the probability of nest collapse Côté SD (2000) Aggressiveness in King Penguins in relation to repro- before the conclusion of breeding activities (Minias and ductive status and territory location. Anim Behav 59:813–821 Kaczmarek 2013). Coulson JC (1968) Differences in the quality of birds nesting in the center and on the edges of a colony. Nature 217:478–479 Coulson JC, Wooller RD (1976) Differential survival rates among breed- Acknowledgments I appreciate the comments and discussion by Jerzy ing Kittiwake gulls Rissa tridactyla.J Anim Ecol 45:205–213 Bańbura and Krzysztof Kaczmarek. I also wish to thank the Associate Davis LS, McCaffrey FT (1986) Survival analysis of eggs and chicks of Editor, Charles R. Brown, and an anonymous reviewer for their construc- Adélie Penguins (Pygoscelis adeliae). Auk 103:379–388 tive suggestions. Decamps S, Le Bohec C, Le Mahoy Y, Gendner J-P, Gauthier-Clerc M (2009) Relating demographic performance to breeding-site location Open Access This article is distributed under the terms of the Creative in the King Penguin. 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Waterbirds 32:357–359 414–418 Uzun A, Kopij G (2010) Effect of the colony edge on the clutch size and Wooller RD, Coulson JC (1977) Factors affecting the age of first breeding fledging success in the Little Egrets Egretta garzetta (L.). Pol J Ecol in the Kittiwake Rissa tridactyla. Ibis 119:339–349 58:393–396 YorioP,QuintanaF(1997) PredationbyKelpGulls Larus Van Vessem J, Draulans D (1986) The adaptive significance of colonial dominicanus at a mixed species colony of Royal Terns Sterna breeding in the Grey Heron Ardea cinerea: inter- and intra-colony maxima and Cayenne Terns Sterna eurygnatha in Patagonia. Ibis variability in breeding success. Ornis Scand 17:356–362 139:536–541 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral Ecology and Sociobiology Pubmed Central

Evolution of within-colony distribution patterns of birds in response to habitat structure

Behavioral Ecology and Sociobiology , Volume 68 (5) – Mar 4, 2014

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Abstract

Behav Ecol Sociobiol (2014) 68:851–859 DOI 10.1007/s00265-014-1697-8 ORIGINAL PAPER Evolution of within-colony distribution patterns of birds in response to habitat structure Piotr Minias Received: 10 December 2013 /Revised: 14 February 2014 /Accepted: 17 February 2014 /Published online: 4 March 2014 The Author(s) 2014. This article is published with open access at Springerlink.com . . . Abstract It has long been suggested that habitat structure Keywords Birds Ciconiiformes Coloniality Comparative . . affects how colonial birds are distributed within their nesting analysis Distribution Habitat structure aggregations, but this hypothesis has never been formally tested. The aim of this study was to test for a correlated evolution between habitat heterogeneity and within-colony Introduction distributions of Ciconiiformes by using Pagel’s general meth- od of comparative analysis for discrete variables. The analysis According to classic theoretical predictions on resource ac- indicated that central-periphery gradients of distribution quisition in animals, individuals should be distributed in en- (high-quality individuals occupying central nesting vironments so as to maximise their fitness. If there are no locations) prevail in species breeding in homogeneous habi- competitive asymmetries between conspecifics, the habitat tats. These were mainly ground-nesting larids and should be occupied proportionally to the available resources spheniscids, where clear central-periphery patterns were re- under the assumptions of the ideal free distribution model of corded in ca. 80 % of the taxa. Since homogeneous habitats Fretwell and Lucas (1970), which implies that the density of provide little variation in the physical quality of nest sites, individuals should increase along with the increasing quality central nesting locations should be largely preferred because of the habitat patch. However, in natural populations of ani- they give better protection against predators by means of more mals, individuals only rarely gain equal access to resources, as efficient predator detection and deterrence. By contrast, they notably differ in their competitive abilities. Conforming central-periphery gradients tended to be disrupted in hetero- to the empirical evidence on competitive asymmetries within geneous habitats, where 75 % of colonial Ciconiiform species populations, a model of ideal despotic distribution was pro- showed uniform patterns of distribution. Under this model of posed, assuming that dominant individuals have capacities to distribution, edge nest sites of high physical quality confer secure the best available territories and to relegate conspecifics higher fitness benefits in comparison to low-quality central of lower phenotypic quality to less attractive habitats (Fretwell sites, and thus, high-quality pairs are likely to choose nest sites 1972). irrespectively of their within-colony location. Breeding in Although there is abundant empirical evidence for ideal homogeneous habitats and uniform distribution patterns were despotic distributions in territorial birds (Andrén 1990;Ens identified as probable ancestral states in Ciconiiformes, but et al. 1995;Møller 1995; Petit and Petit 1996), information on there was a significant transition rate from uniform to central- the patterns of distribution in colonial species are much more periphery distributions in species occupying homogeneous scarce. Distribution patterns of colonial birds are typically habitats. considered on at least three different levels: (1) distribution of colonies in the available environment; (2) distribution of individuals among colonies; and (3) distribution of individuals within colonies. Large-scale patterns of colony distribution as Communicated by C. R. Brown well as distribution of individuals among the colonies located P. Minias (*) in the habitat patches of different quality have both recently Department of Teacher Training and Biodiversity Studies, University received increasing attention (Brown and Rannala 1995). It of Łódź, Banacha 1/3, 90-237 Łódź, Poland has been demonstrated that the foundation of new colonies in e-mail: pminias@biol.uni.lodz.pl 852 Behav Ecol Sociobiol (2014) 68:851–859 several avian species follows a despotic model (Serrano and sites of good physical quality considerably exceeds benefits Tella 2007;Oro 2008) and that individuals of low phenotypic associated with the central nesting position, then high-quality quality (expressed by young age or poor physical quality) may pairs may choose the best available nesting sites independent- be excluded from colonies that are located in the best habitat ly of their location in a colony (Velando and Freire 2001). patches (Rendón et al. 2001). Under such circumstances, the central-periphery patterns By contrast, much less empirical data has been collected on could be disrupted and pairs of varying quality could be the distribution of individuals within their breeding colonies. distributed more or less uniformly among the central and Despite this relative scarcity of information, it seems safe to peripheral zones of colonies. distinguish two major components of nesting site attractive- Although the effects of habitat heterogeneity on the within- ness that may have important fitness consequences for colo- colony patterns of distribution in birds have long been nially breeding species and that, consequently, are likely to hypothesised, most of the empirical evidence has only been determine within-colony distribution patterns. The first of the circumstantial and the suggested relationship has never been components is associated with the within-colony location of supported by a formal analysis. The aim of this study was to nest sites, as it is generally accepted that the centres of colo- test for evolutionary correlations between the structure of nies offer the highest benefits in terms of fitness (Coulson breeding habitat and within-colony distributions in 1968; Aebischer and Coulson 1990). It has been commonly Ciconiiformes (sensu Sibley and Ahlquist 1990), a phyloge- reported that pairs nesting in the centres are likely to achieve netic group with the highest prevalence of coloniality among higher breeding success due to decreased predation-related birds (Siegel-Causey and Kharitonov 1990). According to the losses of eggs and chicks (Götmark and Andersson 1984; theoretical predictions, I expected that birds nesting in homo- Yorio and Quintana 1997; Minias and Kaczmarek 2013), thus geneous habitats should form colonies according to the indicating that colonies may act as selfish herds against pre- central-periphery model of distribution, whereas in heteroge- dation (Brown and Brown 2001). The mechanisms explaining neous habitats, the central-periphery gradients should be lower susceptibility of central pairs to predation may include disrupted (uniform model of distribution). more efficient detection and deterrence of predators in the central parts of colonies. Central nests are also likely to be less accessible to predators, although this may largely depend on the type of predator (Brunton 1997). However, in general, Methods there is large empirical support that colonial birds dilute the risk of predation (Brown and Brown 2001) and that central For the purpose of the analysis, I collected data from the nesting sites are by far the most efficiently protected sites literature for 34 colonial species of Ciconiiformes grouped against predators. Although the breeding success of centrally into nine families (Table 1). Each species was assigned a nesting pairs may be decreased due to density-dependent prevailing model of within-colony distribution: central- intraspecific interactions (Jovani and Grimm 2008; periphery or uniform. The central-periphery model was Ashbrook et al. 2010) and parasitic rates (Tella 2002), many assigned when all studied reproductive parameters or parental studies have demonstrated higher reproductive output in col- quality traits declined from the centre of the colony towards ony centres in comparison to the edges (Patterson 1965; the peripheries. In contrast, the uniform model corresponded Gochfeld 1980; Becker 1995; Vergara and Aguirre 2006). to a situation in which the central-periphery gradients were For this reason individuals of higher quality are likely to disrupted, at least with respect to some of the studied traits or occupy the best central sites and to relegate individuals of in some of the studied colonies. With such an approach, the lower quality to less attractive edge sites. Assuming such a distribution patterns could be coded binarily, with central- despotic mechanism of colony formation, one would expect a periphery distributions denoted as 0 and distributions in which central-periphery pattern of distribution where the phenotypic central-periphery gradients were disrupted (uniform models) quality of breeding birds declines from the centre towards the denoted as 1. Heterogeneity of the breeding habitat was also edges of a colony (Coulson 1968). treated as a categorical variable with two states. Bare ground The physical quality of nesting sites may be considered as and mats of floating vegetation were identified as homoge- the second major component of their attractiveness for colo- neous habitats, as these provide none or negligible variation in nial birds. If the habitat is heterogeneous on a small spatial the physical quality of nesting sites and all nests are more or scale, considerable variation in the physical quality of nesting less equally vulnerable to predators or adverse weather con- sites within colonies is expected. Under this assumption, nest ditions (denoted as 0). All of the other habitats that may sites of high quality would be likely to provide much more provide moderate or considerable variation in the physical effective protection against predators or adverse weather con- quality of nesting sites were considered to be heterogeneous ditions and thus would promote higher reproductive success. habitats (denoted as 1). This category mostly included rocky It has been suggested that if the fitness benefits of nesting in habitats (cliff ledges, rocky slopes and islets, rock crevices, Behav Ecol Sociobiol (2014) 68:851–859 853 Table 1 Patterns of within-colony distribution and nesting habitat of colonial Ciconiiform species Species Distribution Habitat Parameters Authors Spheniscidae Aptenodytes patagonicus U Ground BD (C-P) Côté 2000 BD, RS (C-P) Bried and Jouventin 2001 AS, RS (U) Decamps et al. 2009 Eudyptes chrysocome C-P Ground RS Hull et al. 2004 Spheniscus magellanicus C-P Ground CS, S, RS Gochfeld 1980 S, RS Frere et al. 1992 Pygoscelis antarcticus C-P Ground AM Mínguez et al. 2001 BD Barbosa et al. 1997 Pygoscelis adeliae C-P Ground RS Taylor 1962 CS, RS Tenaza 1971 BD, CS Spurr 1975 CS, S Davis and McCaffrey 1986 Procellaridae Thalassarche melanophris C-P Ground RS Forster and Phillips 2009 Pelecanidae Pelecanus occidentalis C-P Ground AA, CS, RS Blus and Keahey 1978 Ciconiidae Ciconia ciconia C-P Trees AA, RS Vergara and Aguirre 2006 Ardeidae Nycticorax nycticorax U Trees CS (U); RS (C-P) Uzun 2009 Bubulcus ibis U Trees S (C-P) Siegfried 1972 HS (U) Ranglack et al. 1991 CS (U) Samraoui et al. 2007 Ardea cinerea U Trees RS Van Vessem and Draulans 1986 Egretta garzetta U Trees CS (U); RS (C-P) Uzun and Kopij 2010 Phalacrocoracidae Phalacrocorax atriceps URocks AA Shaw 1985 RS Svagelj and Quintana 2011 Phalacrocorax aristotelis U Rocks RS Velando and Freire 2001 Phalacrocorax pelagicus U Cliff BD, AA Siegel-Causey and Hunt 1986 Phalacrocorax carbo U Trees RS (U) Grieco 1994 BD (C-P) Andrews and Day 1999 BD, RS (C-P); Minias et al. 2012a CS (U) BD, CC, RS, S (C-P); CS (U) Minias and Kaczmarek 2013 Phalacrocorax auritus C-P Trees BD Léger and McNeil 1987 Sulidae Morus capensis C-P Ground AA, RS Staverees et al. 2008 Morus serrator U Ground BD, AA (C-P) Gibbs et al. 2000 AA (U) Pyk et al. 2008 Sula variegata U Rocks BD Duffy 1983 Sula leucogaster U Rocks RS Ospina-Alvarez 2008 Accipitridae Pandion haliaetus C-P Trees RS Hagan and Walters 1990 Laridae Hydroprogne caspia C-P Ground BD, RS Antolos et al. 2006 Sternula antillarum U Ground HS, S, RS Brunton 1997 Thalasseus maximus C-P Ground BD, S Buckley and Buckley 1977 854 Behav Ecol Sociobiol (2014) 68:851–859 Table 1 (continued) Species Distribution Habitat Parameters Authors Chlidonias hybridus C-P Floating vegetation CS Minias et al. 2011 CGR Minias et al. 2012b S Minias et al. 2013 Sterna dougallii C-P Ground BD Ramos 2002 Sterna hirundo C-P Ground BD, S, RS Becker 1995 Chroicocephalus ridibundus C-P Ground RS Patterson 1965 Rissa tridactyla U Cliff AS (C-P) Coulson and Wooller 1976 RS (U) Wooller and Coulson 1977 S (C-P); RS (U) Regehr et al. 1998 AS (C-P) Aebischer and Coulson 1990 Larus atricilla C-P Ground BD, CS, S, RS Montevecchi 1978 Larus delawarensis U Ground AA (C-P) Ludwig 1974 HS, S, RS (C-P) Dexheimer and Southern 1974 AA (C-P) Ryder 1975 BD, CS, HS, RS (U) Ryder and Ryder 1981 BD, AA (C-P) Haymes and Blokpoel 1980 Larus californicus C-P Ground RS, AA Pugasek and Diem 1983 Larus argentatus C-P Ground BD Burger and Shisler 1980 Central-periphery (C-P) and uniform (U) patterns were assigned to within-colony distributions of the following traits: BD breeding date, CS clutch size, HS hatching success, RS reproductive success, S brood survival, CGR chick growth rates, CC chick condition, AS adult survival, AA adult age, AM adult morphology. If different, the patterns of distribution were indicated in parentheses separately for each reported reproductive/quality trait or for each studied colony hollows and burrows) and vegetated habitats (woodlands and 1994), and it has been demonstrated that it does not bias the shrubs). results qualitatively (Møller et al. 1998;Nunn 1999). Since data from different species are not independent due To test for a correlated evolution between breeding habitat to their shared ancestral states, it is widely acknowledged that structure and within-colony distribution patterns, I used comparative analyses must control for the phylogeny. I based Pagel’s discrete variable method (1994) which uses the my phylogenetic tree on the classification of Sibley and continuous-time Markov model in order to characterise evo- Ahlquist (1990). This phylogeny is uniquely available for lutionary changes in selected pairs of variables along each the entire order of Ciconiiformes, and for this reason, it was branch of the phylogenetic tree. The method compares the fit used to branch the families of my tree (Fig. 1). Although the of two different models assuming an either independent or phylogeny of Sibley and Ahlquist (1990) was once considered dependent (the rate of change of one trait depends on the controversial (Sheldon and Gill 1996), it is now assumed as background state of the other) evolution of traits. The models quite robust for phylogenetic analyses in birds (reviewed in were fitted using maximum likelihood and compared using Mooers and Cotgreave 1994), and hence, it has been broadly the likelihood ratio (LR) statistic, which is expressed as LR=2 used in comparative studies (Cézilly et al. 2000;Dubois and (logL −logL ), where L is the likelihood of the model (D) (I) (D) Cézilly 2002;Garamszegietal. 2005; Olson et al. 2008), that allows the traits to evolve in a correlated fashion and L is (I) including those on avian coloniality (Rolland et al. 1998; the likelihood of the independent model. The LR statistic is Varela et al. 2007). In order to branch the genera and species, asymptotically distributed as χ with four degrees of freedom I used five phylogenies based on both molecular and morpho- for this test (Pagel 1997). logical data (Sheldon 1987; Kennedy et al. 2000;Thomas The discrete variables method was also used to estimate the et al. 2004; Bertelli and Giannini 2005; Smith 2010). Since ordering and direction of the evolutionary changes of the two different approaches were used to construct the above phy- analysed variables (so-called temporal order tests). For this logenies, I decided not to control for branch lengths, which purpose, one needs to fit reduced models in which a certain followed from other comparative studies (Dubois et al. 1998; rate of evolutionary transition q is excluded a priori (set to 0). ij Rolland et al. 1998; Cézilly et al. 2000; Varela et al. 2007). The constrained seven-parameter models are then compared Setting equal branch lengths is considered conservative (Pagel to the full eight-parameter model which tests the hypotheses Behav Ecol Sociobiol (2014) 68:851–859 855 Fig. 1 Phylogenetic tree of 34 colonial species from nine Ciconiiformes families involved in the study whether the specified transition rates differ significantly from proportion was found between the number of species that zero. The tests are asymptotically distributed as χ with one exhibited central-periphery distribution within colonies and degree of freedom (Pagel 1994). In this manner, the evolution those in which central-periphery gradients were disrupted (56 between the ancestral states and the derived states of both vs. 44 %, Table 1). There was a clear tendency for species selected variables may be traced. For root reconstruction of breeding in homogeneous habitats to be distributed central- ancestral states, I used the maximum-likelihood reconstruc- peripherally within the colonies (Fig. 2). The log-likelihood of tion method of Pagel (1999). All analyses were performed the model of independent evolution was estimated at L = with BayesTraits (Pagel and Meade 2008). −36.10 and was significantly lower in comparison to the likelihood of the dependent model L =−30.18 (χ =11.83, df=4, P=0.019). Such results support the hypothesis of a Results correlated evolution between preferences for heterogeneous breeding habitats and uniform patterns of within-colony Among the 34 taxa used for the analysis, there were 20 species distribution. that nested in homogeneous habitats (59 %) and 14 that chose Breeding in homogeneous habitats and uniform distribu- heterogeneous habitats for breeding (41 %). A similar tion of pairs within colonies were identified as ancestral states 856 Behav Ecol Sociobiol (2014) 68:851–859 mechanisms which may explain lower predation rates at these locations include: (1) restricted accessibility for predators (Siegel-Causey and Hunt 1981); (2) more efficient communal defence (Elliot 1985); (3) more efficient detection of predators (Roberts 1996); and (4) lower probability of being depredated due to the dilution effect (Murphy and Schauer 1996). By contrast, heterogeneous habitats were found to disrupt the central-periphery patterns of distribution within colonies. In habitats of moderate or high heterogeneity, edge nest sites of high physical quality are likely to confer higher fitness benefits in comparison to low-quality central sites. Thus, high-quality pairs are expected to choose nest sites irrespectively of their within-colony location, and thus, they Low High are expected to be uniformly distributed among the central and Habitat heterogeneity peripheral zones of colonies. Central-periphery distributions Fig. 2 Number of species exhibiting central-periphery (grey area)and uniform (white area) patterns of within-colony distribution with respect to were found to be disrupted in nearly 75 % of colonial the heterogeneity of breeding habitat Ciconiiformes species that nested in heterogeneous habitats. It seems that uniform patterns of distribution are especially with a probability of 94.8 %. I found a significant rate of common in birds that establish colonies on cliffs or in other transition from uniform to central-periphery distribution in rocky habitats, including various Phalacrocoracidae and species that bred in homogeneous habitats (χ =4.54, df=1, Sulidae species. Nesting sites such as crevices under fallen P=0.033). I also found a significant rate of reversed transi- rocks, open ground caves and open ledges on cliffs usually tions, i.e. from central-periphery to uniform patterns of distri- show great variation in their physical quality and attractive- bution (χ =7.50, df=1, P=0.006). The rate of evolution from ness for birds; for example, a clear preference for sites with breeding in homogeneous to heterogeneous habitats with no more lateral and overhead cover, with better drainage and with change in the background state of uniform distribution pattern better visibility has been demonstrated for the European Shag was not significant (χ =1.14, df=1, P=0.29), but it cannot be Phalacrocorax aristotelis (Velando and Freire 2003). Such excluded that this could have resulted from the low power of physical characteristics of nesting sites have been shown to the test. All the other transition rates were also non-significant provide more effective protection against predators and to (all P>0.05). prevent broods from flooding, unfavourable atmospheric con- ditions and intra-specific inference, which greatly affected the hatching success of Shags (Velando and Freire 2003). The Discussion distribution of birds within the same colony of Shags did not conform to the assumptions of the central-periphery model, as This study was the first to formally demonstrate a link be- individuals of different quality were distributed despotically tween within-colony distribution patterns in birds and the among the sites of varying physical quality (Velando and structure of preferred nesting habitat by using comparative Freire 2001, 2003). analysis. It was shown that as much as 85 % of colonial Disruptions in the central-periphery patterns of distribution Ciconiiformes species which breed in homogeneous habitats were also recorded in several waterbird species associated tend to show clear central-periphery patterns of distribution with woodland habitats; although, this kind of environment within their colonies and that these are mostly ground-nesting is expected to provide only moderate variation in the physical species from the Spheniscidae and Laridae families. In gener- quality of nesting sites, most commonly expressed by varia- al, bare-ground habitats, such as sandy islands or dunes, tion in tree height and canopy structure. In several tree-nesting provide no apparent variation in the physical quality of the colonial avian species, tree height was identified as an impor- nesting sites. Under such conditions, each nest site is likely to tant predictor of reproductive success and was suggested to be equally exposed to predation and inclement weather. determine accessibility of nests to ground and tree-dwelling Consequently, nest-site selection patterns should evolve to- predators (Post 1990; Childress and Bennun 2000). The wards choosing an appropriate location within the colony, breeding success of the Scarlet Ibis Eudocimus ruber corre- where pressure coming from predators will be minimised. lated positively with nest cover by overhanging branches Assuming that all nest sites are physically similar, the highest (Olmos 2003), and the study on Cattle Egrets Bubulcus ibis fitness benefits are expected to be acquired via nesting in the indicated higher fledging success in pairs nesting close to the central parts of colonies (Coulson 1968). As colony centres trunks of trees (Si Bachir et al. 2008). However, in some cases, the fitness benefits that were associated with nesting in the are usually associated with higher nesting densities, the No of species Behav Ecol Sociobiol (2014) 68:851–859 857 Cézilly F, Dubois F, Pagel M (2000) Is mate fidelity related to site sites of high physical quality could be acquired via mecha- fidelity? A comparative analysis in Ciconiiformes. Anim Behav nisms not related to anti-predatory protection; for example, in 59:1143–1152 the tree-nesting subspecies of Great Cormorant Childress RB, Bennun LA (2000) Nest size and location in relation to Phalacrocorax carbo sinensis, the physical quality of nesting reproductive success and breeding timing of tree-nesting Great Cormorants. Waterbirds 23:500–505 sites (tree height) determined the probability of nest collapse Côté SD (2000) Aggressiveness in King Penguins in relation to repro- before the conclusion of breeding activities (Minias and ductive status and territory location. 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Published: Mar 4, 2014

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