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Patterns of fish distribution in tropical rock pools at Príncipe Island, Gulf of Guinea Patterns of fish distribution in tropical rock pools at Príncipe Island, Gulf of Guinea
Azevedo e Silva, J; Almeida, AJ; Cravo, M; Pais, MP; Santos, Y; Paula, J
2022-10-02 00:00:00
African Journal of Marine Science 2022, 44(4): 353–366 Copyright © NISC (Pty) Ltd Printed in South Africa — All rights reserved AFRICAN JOURNAL OF MARINE SCIENCE ISSN 1814-232X EISSN 1814-2338 https://doi.org/10.2989/1814232X.2022.2143423 Patterns of fish distribution in tropical rock pools at Príncipe Island, Gulf of Guinea 1 1,2 1 1,3 4 1,3 J Azevedo e Silva * , AJ Almeida , M Cravo , MP Pais , Y Santos and J Paula Animal Biology Department, Faculty of Sciences, University of Lisbon, Lisbon, Portugal Laboratório Marítimo da Guia (Cascais), Environmental Sciences Centre [MARE], Animal Biology Department, Faculty of Sciences, University of Lisbon, Lisbon, Portugal MARE – Marine and Environmental Sciences Centre/ARNET – Aquatic Research Network, Animal Biology Department, Faculty of Sciences, University of Lisbon, Lisbon, Portugal Fundação Príncipe, Santo António, São Tomé e Príncipe * Corresponding author, e-mail: jfazsilva@gmail.com Little is known about the ichthyofauna from intertidal rock pools of the west coast of Africa, especially in the Gulf of Guinea. Rock pools are characteristic habitats of the intertidal zone of structurally complex rocky shores, adding important niche space to coastal fish species. In this study, rock pools of three similar rocky shores of Príncipe Island were sampled to describe the composition, abundance and distribution of fish assemblages and their relation to parameters of pool structure (volume, depth), water mass (temperature, salinity and pH) and biology (algal and coral cover, and biological species richness). A total of 18 fish species and one leptocephalus larva of unknown species, representing 13 families, were observed during sampling. In decreasing order, the five-most-abundant species were the goby Bathygobius burtoni, night sergeant Abudefduf taurus, West African rockhopper Entomacrodus cadenati, sailfin blenny Microlipophrys velifer and Biafra doctorfish Prionurus biafraensis, which together represented 81% of the total number of fish recorded during this study. The four-most-abundant species also proved to be the better adapted to the range of conditions found in rock pools. Overall, larger rock pools with minimal biological cover and higher salinity were found to support higher fish abundance and species richness. Most species individually preferred rock pools with larger volumes, but some presented a degree of habitat specificity, such as the absence or presence of biological cover. Species that were more-active swimmers preferred deeper pools. Keywords: behavioural ecology, eastern tropical Atlantic, fish assemblage, habitat specificity, intertidal zone, rock pool characteristics, rocky shores, São Tomé and Príncipe Online supplementary material: The Supplementary Information, available at https://doi.org/10.2989/1814232X.2022.2143423, contains plots of water parameters (temperature, pH and salinity) as a function of the volume of each rock pool on the three sampled shores. Introduction Owing to their accessibility, intertidal zones have been (Tuya et al. 2018). Previous studies on the marine fishes of one of the most intensively studied marine environments São Tomé and Príncipe have focused mainly on the open across the globe, and many of these studies have included and coastal sea, and recently on mangrove ecosystems ichthyofauna. However, tropical rock pools have received (Herrero-Barrencua et al. 2017; Cravo et al. 2021). little attention (Gibson 1982; Mahon and Mahon 1994; Afonso et al. (1999) and Wirtz et al. (2007) documented Martins et al. 2007), particularly on the west coast of Africa limited sightings of fish in intertidal rocky pools, but with and adjacent islands (Zander et al. 1999). In this region, no detailed information. Of these, it is known that the fish families such as Clinidae, Tripterygiidae and Blenniidae blenniids West African rockhopper Entomacrodus cadenati, were the most commonly reported in intertidal habitats in sailfin blenny Microlipophrys velifer, horseface blenny past studies (Wirtz 1980; John and Lawson 1991; Zander Ophioblennius atlanticus and molly miller Scartella cristata are et al. 1999), but recent work, particularly focusing on whole resident species of the intertidal zone and widely distributed assemblages, is non-existent and very little is known about along the west coast of Africa (Zander et al. 1999). intertidal fishes of other families. Therefore, there is a lack Apart from the intrinsic scientific interest of intertidal of scientific knowledge on intertidal fishes of the eastern fishes and their physiological behaviour, the intertidal tropical Atlantic, and particularly of the Gulf of Guinea. and adjacent subtidal zones are also nursery areas for Although the marine ichthyofauna of the Gulf of Guinea numerous fish species that eventually recruit to coastal is one of the least-studied in the world, marine fish in São fisheries (Gibson 1999a). Any degradation and drastic Tomé and Príncipe have recently attracted scientific interest modification of such areas, therefore, have consequences African Journal of Marine Science is co-published by NISC (Pty) Ltd and Informa UK Limited (trading as Taylor & Francis Group) 354 Azevedo e Silva, Almeida, Cravo, Pais, Santos and Paula for both the economy and quality of life of many coastal and offshore habitats as they mature (Norton and Cook 1999; island countries (Gibson 1999a), such as São Tomé and White and Brown 2013). A third group, transients, usually Príncipe, where small-scale coastal fisheries are crucial to comprise a small fraction of the species in rock pools domestic trade and as coastal food-suppliers (Horemans (Mahon and Mahon 1994), occupying them on only certain et al. 1994; Abreu 2013; Tous 2015). Global climate occasions to forage or by accident, when trapped at low tide change, in particular ocean warming, puts further pressure (Horn et al. 1999; Griffiths 2003; White et al. 2015). on the environmental conditions of rocky shores and their Throughout the tidal cycle, intertidal fishes need to find biological communities (Horn et al. 1999). Projections and occupy a favourable rock pool during emersion time to of climate change in São Tomé and Príncipe show an increase their chance of survival. Thus, many behavioural increase in temperature that could exceed 3 °C by the patterns of fishes found in rock pools can be interpreted middle of the 21st century, as well as a heavier precipitation as adaptations for protecting either the individual or its rate (Chou et al. 2020). Impacts of increased temperature offspring from unfavourable conditions during low tide on biological communities in tropical waters are expected (Gibson 1986). Consequently, the different gradients of to be significant because the species are stenothermic, and biotic and abiotic factors can produce consistent patterns hence increases in water temperature can drive changes in the structure, distribution and abundance of fish above their lethal limit (Raffaelli and Hawkins 1999). Rock assemblages (Gibson 1982; Norton and Cook 1999; Zander pools constitute good models for assessing these impacts et al. 1999). Thus, an important part of the study of intertidal (Vinagre et al. 2018). fishes is to find the relationships between their distribution, Rock pools are characteristic habitats found in the physiology and behaviour and the environmental variables intertidal zone of rocky shores, adding important niche of the rock pools (Gibson 1999b). space to coastal habitats (Firth et al. 2014). During low In this study, we investigated rock pool fish assemblages tide, water is retained in holes and depressions that serve at Príncipe Island, in the eastern tropical Atlantic, with as refugia for many invertebrates and fishes (Zander the objective of describing the species composition et al. 1999; Martins et al. 2007). This renders rock pools as and abundance in relation to abiotic and biotic factors. microhabitats that attract a high diversity and abundance We aimed to: (i) determine the importance of rock pool of various organisms (White et al. 2015). Nonetheless, dimensions (depth, surface area and volume), within-pool rock pool organisms are subject to stressful environmental water conditions (temperature, salinity and pH), and algal, conditions during the low-water tidal period. When isolated coral and total biological community cover in controlling from the sea, rock pools become prone to large and rapid fish assemblage structure; (ii) assess the variables that fluctuations in the physicochemical properties of the water, contributed most to the abundance of each species; and such as temperature, salinity, oxygen concentration, (iii) describe species distribution depending on the water carbon dioxide concentration and pH (Huggett and Griffiths properties. 1986; Horn et al. 1999; Martins et al. 2007). Additionally, We defined a priori our hypotheses as: (1) environmental rock pools exist in numerous shapes and volumes, are variables drive fish assemblage structure; (2) fish species randomly distributed along the vertical and horizontal assemblages differ among sites; (3) environmental gradients of rocky shores, and are highly variable over variables drive species richness; and (4) environmental time (i.e. tidally, diurnally and with seasonally induced variables drive species abundance. fluctuations) and space (from geographic to local scales) (Martins et al. 2007; White et al. 2015). They also become Materials and methods more exposed to marine and terrestrial predators, such as fishes, octopuses and birds, compared with in the subtidal Ethical statement environment (Gibson 1986; White et al. 2015; Vinagre Ethical review and approval were not required for the et al. 2018). Consequently, several fish species have animal study since there are currently no institutional ethical developed behavioural, physiological and morphological guidelines in São Tomé and Príncipe, but only common- adaptations to better endure the extreme environmental sense practices. The work was conducted entirely in the fluctuations of these habitats (Zander et al. 1999). field at São Tomé and Príncipe under the jurisdiction and Many coastal fishes use rock pools at some point in approval of the Príncipe Biosphere Reserve and did not their life cycle to forage, take refuge from predators or involve animal experimentation or compromised animal as nursery areas (Horn et al. 1999), and thus rock pools welfare. The census of fish populations in this study represent a key habitat for supporting coastal fish species consisted of direct observations. On rare occasions, to diversity (White et al. 2015). Such fishes can be grouped ensure better identification, specimens were captured, into three categories based on how they use rock pools and photographed and returned alive and undamaged to the the proportion of their life cycle spent within them (Mahon environment with extreme care, following best practices. and Mahon 1994; Griffiths 2003; White et al. 2015), namely residents or primary residents, secondary residents and Study sites and rock pool sampling transients. Residents spend almost their entire juvenile and Sampling took place on Príncipe Island (part of São Tomé adult lives in the intertidal zone. They are generally small, and Príncipe), a small oceanic island of volcanic formation benthic fishes that are physiologically, morphologically and located in the Gulf of Guinea (Figure 1). The island is part behaviourally adapted for intertidal life (White and Brown of the eastern tropical Atlantic, which is characterised by 2013). Secondary residents use the intertidal primarily as a heavy and seasonal rainfall that is sufficient to reduce nursery area, after which they migrate into the subtidal and considerably the surface salinity levels to 30, increasing African Journal of Marine Science 2022, 44(4): 353–366 355 7°24′ N Bom-Bom Nigeria AFRICA Ponta Marmita BIGHT OF BENIN ATLANTIC OCEAN 1°40′ N Praia Uba 4° N Bioko Cameroon GULF OF GUINEA BIGHT OF BONNY Santo António 2° N Equatorial Príncipe Guinea São Tomé PRÍNCIPE ISLAND 0° Gabon ATLANTIC 1°36′ N OCEAN Annobón 2° S 5° E 7° E 9° E 5 km Figure 1: Location of the three rocky shore sampling sites at Príncipe Island: Bom-Bom Islet, Ponta Marmita and Praia Uba turbidity over extensive areas, particularly around the coralline alga Lithophyllum incrustans and the white mouths of the Niger and Congo rivers, but also affecting encrusting zoanthid Palythoa caribaeorum on the freely more-distant islands such as Príncipe Island (Reid 2011). draining open rock surface, followed by its replacement by The island has an equatorial humid tropical climate that black lichen Verrucaria sp. and hooded oyster Saccostrea can be divided into four seasons which alternate between cucullata, which defined the upper limit of the eulittoral. wetter and drier periods, with an average annual rainfall of Sampling was performed only close to peak low tide so ~2 000–3 000 mm (NBSAP II 2015; Chou et al. 2020). The that splashes from waves would not influence the water rainy seasons include the two main precipitation peaks, with conditions of the rock pools. Pools with freshwater drainage the highest occurring between October and November and from land or pools connected to other adjacent pools were a secondary peak around April and May (Chou et al. 2020). avoided to ensure relatively uniform conditions. Therefore, These are interspersed by the dry seasons, with the more only saltwater rock pools isolated during emersion were pronounced one (termed gravana) occurring between sampled. Salinity, temperature and pH were registered in June and September, and the lesser dry season between each pool using a YSI Multi 350i handheld meter. January and March (Chou et al. 2020; Cravo et al. 2021). To determine the area of the rock pools, a scaled Tidal ranges are relatively small at Príncipe Island, with a photograph was taken from directly above each pool, as maximum of 1.9 m during extreme spring tides (0.2–2.1 m from parallel to the pool surface (i.e. horizontally) as possible. hydrographic zero) and 0.4 m during neap tides (1.0–1.4 m Rock pools were only considered if they fitted into the full from hydrographic zero) (Instituto Hidrográfico 2019). frame of the camera (GoPro Hero7 Black in linear mode). Sampling occurred at three locations, Bom-Bom Islet, The area was then calculated using ImageJ software. Ponta Marmita and Praia Uba, located on the north coast of To calculate the water volume, the average depth was Príncipe Island (Gulf of Guinea) (Figure 1). These locations calculated from 10 random depth measures. Maximum were chosen for their similar geomorphological conditions depth was also recorded. and exposure to the sea, extensive rocky shores, numerous rock pools and relative ease of access. Fish and biological community sampling A total of 20 permanent rock pools were sampled at An absence of obstructions such as large macroalgae with each of the three locations between January and February considerable canopy meant that fish were clearly visible in 2020. Only rock pools in the eulittoral zone (mid-zone) were the rock pools, and thus direct observations were deemed sampled to allow comparison between the different rocky adequate to census the fish populations (Gibson 1999b). shores. The lower limit of the eulittoral zone was delimited Sampling consisted of first identifying the visible fish species by a noticeable and abrupt absence of the encrusting in the rock pool and their respective abundance, with minimal 356 Azevedo e Silva, Almeida, Cravo, Pais, Santos and Paula disturbance so the fish would not hide in crevices. Besides above the combined effect of all the covariates selected ichthyofauna, the different macroalgae and animal species using the BEST routine. One-way analysis of variance other than fish in the pools were quantified simply in terms of (ANOVA) was also used to compare the mean species presence or absence by visually identifying the species. The richness and total abundance among sampling locations. percentage cover of macroalgae and coral was recorded and The effect of rock pool environmental variables (excluding estimated by eye for the whole rock pool to the nearest 10%. pH and temperature) on the abundance of individual species If necessary, boulders were occasionally moved to account was analysed using multiple linear regressions with stepwise for possible hidden fish and other organisms. To ensure variable selection. These post hoc regressions were correct species identification, the bottom, ledges and holes conducted only for species that occurred in more than three of the rock pool were filmed using a waterproof camera, for pools and were represented by more than 10 individuals. later examination. All analyses were performed using the software Observations in the field were carried out by trained PRIMER-E 6.1.11, PERMANOVA+ 1.0.1 and IBM SPSS observers. Species identifications were confirmed in situ, Statistics 26.0. on recorded videos and in the laboratory using existing taxonomic references for the region (i.e. Afonso et al. 1999; Results Wirtz et al. 2007; Carpenter and De Angelis 2016a, 2016b; Vasco-Rodrigues et al. 2018). The taxonomy is according to Fish assemblages Nelson (2006). A total of 746 fish from 18 species and a leptocephalus of an unknown species, together representing 13 families, Data treatment were observed during sampling in the three study Draftsman plots using Pearson correlations were made locations (Table 1). In decreasing order, the five-most- between the environmental variables to determine highly abundant species were the goby Bathygobius burtoni, correlated pairs (p > 0.9) to eliminate any possible redundant night sergeant Abudefduf taurus, E. cadenati, M. velifer variables. The remaining variables were average depth and Biafra doctorfish Prionurus biafraensis, which together (cm), volume (l), pH, salinity, water temperature (°C), represented 81% of the total number of fish recorded during coral cover (%), macroalgae cover (%), total biological this study. cover (%), macroalgae species richness and metazoan Sampled fish abundance and composition varied between species richness. These variables were normalised, and the three locations (Figure 2). Some species appeared in a resemblance matrix was constructed using Euclidean all three locations, such as A. taurus, Guinean damselfish distances. Rock pool variables were then compared among Microspathodon frontatus, Cape Verde gregory Stegastes the three study sites using principal coordinates analysis imbricatus, E. cadenati, M. velifer, L. nuchipinnis, B. burtoni (PCoA). and P. biafraensis (Figure 2). Other species were found in Fish assemblage data were log-transformed, and only two locations, like the silverside Atherina lopeziana a resemblance matrix was constructed using the found at Bom-Bom and Praia Uba, and spotted soapfish zero-adjusted Bray–Curtis similarity coefficient. This was Rypticus subbifrenatus, sergeant major Abudefduf done to generate the distance matrix among samples saxatilis and Monrovia doctorfish Acanthurus monroviae because the sampled rock pools did not have all species in found at Bom-Bom and Ponta Marmita (Figure 2). Lastly, common (Clarke et al. 2006). Rock pool fish assemblages some were found at only one rocky shore site: cardinal were also compared among the three study sites using fish Apogon imberbis, crevalle jack Caranx hippos and PCoA. In this PCoA of the fish data, the vectors of the orangespotted filefish Cantherhines pullus were found environmental variables that were correlated as >0.3 and in Bom-Bom, and the leptocephalus (Anguilliformes the main fish species that were correlated as >0.4 were non-determined [nd]), pebbletooth moray Echidna peli, Niger overlapped for comparison. hind Cephalopholis nigri and Newton’s wrasse Thalassoma Based on the resemblance matrix of fish samples, newtoni in Ponta Marmita (Figure 2). a distance-based linear model (DISTLM) was used in Sampled rock pools were occupied predominantly by combination with a distance-based redundancy analysis resident fishes, which represented 64% of total individuals (dbRDA) for visualising the results (Anderson et al. but only 16% of total species (Table 1). In contrast, 2008), to identify which of the environmental variables secondary residents represented 34% of total individuals accounted for the most significant part of the variation in but 58% of total species (Table 1). Finally, transient fishes fish assemblage composition, while also assessing the represented only 2% of total abundance but 26% of total relationship of all variables individually with marginal tests. species (Table 1). The selection criterion and procedure were, respectively, Ten additional species were sighted during field the Akaike information criterion for small sample sizes observations outside the sampling period in the eulittoral zone (AICc) and the BEST routine, which selects the best of the same rocky shores and at similar shore sites around possible model. The resulting variables of the DISTLM the island, adding five more families (Table 2). These were model were used in a permutational multivariate analysis the honeycomb moray Muraena melanotis, round sardinella of variance (PERMANOVA) as covariates in the order Sardinella cf. aurita, white mullet Mugil curema, rock hind of the proportion of squared differences (Prop.) in the Epinephelus adscensionis, grey snapper Lutjanus griseus, marginal tests. The sequential (Type I) sum of squares blacktail picarel Spicara nigricauda, West African hawkfish (SS) was used, with Location as the last fixed factor. This Cirrhitus atlanticus, Hypleurochilus aequipinnis, O. atlanticus allowed for the evaluation of the effect of location over and and S. cristata. African Journal of Marine Science 2022, 44(4): 353–366 357 Table 1: Fish species documented in 60 rock pools from three locations at Príncipe Island: Bom-Bom Islet (BB), Ponta Marmita (PM) and Praia Uba (PU). R = resident; SR = secondary resident; T = transient Local common Residency Rock pool Family Species No. observed Location name status ID no. Anguilliformes nd Leptocephalus larva – T 1 PM 32 Muraenidae Echidna peli (Kaup, 1856) Moreia-salpicada SR 1 PM 32 Atherinidae Atherina lopeziana (Rossignol – T 12 BB, PU 6, 60 and Blache, 1961) Serranidae Rypticus subbifrenatus Peixe-sabão SR 2 BB, PM 16, 32 (Bloch and Schneider, 1801) Epinephelidae Cephalopholis nigri Cota-uê T 1 PM 30 (Günther, 1859) Apogonidae Apogon imberbis Cardinal T 1 BB 10 (Linnaeus, 1758) Carangidae Caranx hippos (Linnaeus, Corcovado SR 3 BB 17, 19 1766) Pomacentridae Abudefduf saxatilis Txim-txim SR 29 BB, PM 15, 32 (Linnaeus, 1758) Pomacentridae Abudefduf taurus (Müller and Txim-txim-preto SR 129 BB, PM, PU 5, 6, 8, 9, 11, 15, Troschel, 1848) 17, 18, 19, 23, 28, 31, 32, 33, 34, 36, 39, 44, 45, 46, 48, 49, 50, 58, 59 Pomacentridae Microspathodon frontatus Txim-txim SR 27 BB, PM, PU 5, 6, 15, 19, 28, Emery, 1970 29, 60 Pomacentridae Stegastes imbricatus Jenyns, Txim-txim SR 39 BB, PM, PU 5, 6, 9, 15, 17, 18, 1840 19, 27, 28, 29, 31, 34, 50, 60 Labridae Thalassoma newtoni Dodongo SR 1 PM 29 (Osório, 1891) Blenniidae Entomacrodus cadenati – R 97 BB, PM, PU 1, 2, 3, 4, 5, 6, 8, Springer, 1967 9, 11, 12, 15, 18, 23, 28, 29, 31, 35, 37, 41, 42, 43, 45, 46, 50, 51, 52, 53, 54, 56, 57, 58, 59, 60 Blenniidae Microlipophrys velifer – R 86 BB, PM, PU 4, 10, 16, 17, 19, (Norman, 1935) 20, 21, 23, 24, 28, 29, 31, 32, 36, 38, 39, 40, 41, 42, 43, 45, 49, 51, 52, 53, 55, 57, 58, 59 Labrisomidae Labrisomus nuchipinnis – SR 20 BB, PM, PU 6, 9, 11, 12, 17, (Quoy and Gaimard, 1824) 19, 35, 37, 49, 56, 60 Gobiidae Bathygobius burtoni Xarroco/Batu R 245 BB, PM, PU 5, 6, 7, 8, 9, 10, (O’Shaughnessy, 1875) 11, 15, 16, 17, 18, 19, 20, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 42, 44, 45, 46, 47, 48, 50, 51, 57, 59, 60 Acanthuridae Acanthurus monroviae Lâmina SR 3 BB, PM 5, 15, 32 Steindachner, 1876 Acanthuridae Prionurus biafraensis (Blache Cabo-verde SR 48 BB, PM, PU 15, 17, 19, 28, 29, and Rossignol, 1962) 30, 32, 36, 45, 49, 56, 60 Monacanthidae Cantherhines pullus Peixe-asno-magro T 1 BB 5 (Ranzani, 1842) 358 Azevedo e Silva, Almeida, Cravo, Pais, Santos and Paula 6.5 Bom-Bom Ponta Marmita Praia Uba 6.0 5.5 5.0 4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 SPECIES Figure 2: Average number of fish per rock pool of each species observed in rock pools of the eulittoral zone of three locations at Príncipe Island: Bom-Bom, Ponta Marmita and Praia Uba. Error bars represent SE. For full species names see Table 1 Table 2: Additional fish species observed outside the sampling period in rock pools of the eulittoral zone of several rocky shores around Príncipe Island. R = resident; SR = secondary resident T = transient Family Species Local common name Residency status Muraenidae Muraena melanotis (Kaup, 1859) Moreia-mapinta SR Clupeidae Sardinella cf. aurita (Valenciennes, 1847) Sardinha/Longo T Mugilidae Mugil curema (Valenciennes, 1836) Tainha SR Epinephelidae Epinephelus adscensionis (Osbeck, 1765) Garoupa SR Lutjanidae Lutjanus griseus (Duméril, 1861) Corvina SR Sparidae Spicara nigricauda (Norman, 1931) – T Cirrhitidae Cirrhitus atlanticus Osório, 1893 Cazebudo SR Blenniidae Hypleurochilus aequipinnis (Günther, 1861) – R Blenniidae Ophioblennius atlanticus (Valenciennes, 1836) – SR Blenniidae Scartella cristata (Linnaeus, 1758) – R Relationship between rock pool characteristics and fish oyster Striostrea denticulate and mussel Mytilus sp., assemblages but these rarely exceeded 10% cover. In terms of mobile Sixty permanent rock pools were sampled, having a range organisms, the most frequent and abundant were the of area (0.08–~8 m²), volume (9.8–~3 180 l), and depth rock-boring urchin Echinometra lucunter, a hermit crab (10–75 cm). The physicochemical properties of the water (Diogenidae nd), and the sea snail Nerita senegalensis. in the rock pools (temperature, pH and salinity) fluctuated Crabs of the family Grapsidae and other small crabs, sea more in smaller volumes and oscillated somewhat less as slugs of the genus Dolabrifera, and a limpet Fissurella sp. volume increased (Supplementary Figure S1). were also common, but not as abundant. Algal cover varied from 0% to 90% and was mainly The PCoA of the fish data (Figure 3a) shows the composed of encrusting coralline pink macroalgae, with overlap of rock pools from the three locations and how some other small red and brown macroalgae present. Coral environmental variables can explain the distribution of cover likewise varied from 0% to 90% and predominantly pools in the multivariate space. Macroalgal, coral and comprised the zoanthid P. caribaeorum. Other sessile total percentage cover appear to be indirectly correlated organisms that were somewhat abundant included with the abundance and richness of species in most sponges, anemones, tubeworms (Serpullidae nd), the rock pools, except for some pools that coincided with a Leptocephalus E. peli A. lopeziana R. subbifrenatus C. nigri A. imberbis C. hippos M. frontatus A. taurus A. saxatilis S. imbricatus T. newtoni E. cadenati M. velifer L. nuchipinnis B. burtoni A. monroviae P. biafraensis C. pullus NUMBER OF FISH African Journal of Marine Science 2022, 44(4): 353–366 359 Transform: Log(X+1) Normalise Resemblance: S17 Bray–Curtis similarity (+d) Resemblance: D1 Euclidean distance (a) (b) Ecaden Simbri Volume Mfront 2 Volume Lnuchi Average depth Salinity Average depth Pbiafr Ataurus Algae species Metazoan species Metazoan species Total % cover % coral % algae Bburto Algae species Temperature Mvelif Salinity % algae pH Location −2 % coral Bom-Bom −20 Ponta Marmita Total % cover Praia Uba −4 −40 −4 −2 0 2 4 6 −60 −40 −20 0 20 40 PCO1 (38.6% of total variation) PCO1 (25% of total variation) Figure 3: (a) Principal coordinates ordination (PCoA) plot based on zero-adjusted Bray–Curtis dissimilarities of the species composition matrix. Environmental biotic and abiotic vectors inside the circle represent their effect on fish assemblages, and the fish species vectors show in which pools these species tended to be found. (b) PCoA based on Euclidean distances of normalised environmental variables in rock pools at three locations at Príncipe Island. Vectors represent the effect on the characteristics of the rock pools; the longer the line, the more influential is the variable. The name codes for fish species correspond to the following: Ataurus – Abudefduf taurus; Mfront – Microspathodon frontatus; Simbri – Stegastes imbricatus; Ecaden – Entomacrodus cadenati; Mvelif – Microlipophrys velifer; Lnuchi – Labrisomus nuchipinnis; Bburto – Bathygobius burtoni; Pbiafr – Prionurus biafraensis greater correlation with the presence of the two blenniids, showed that the effect of location did not contribute to E. cadenati and M. velifer. This indicates that these explain additional variation (p = 0.160), accounting for only species prefer rock pools with greater biological cover. The 4% of the variation in the analysis (Location SS/Total SS) remaining species were more closely correlated with rock (Table 4). Furthermore, according to the ANOVA analysis, pools with greater volume and depth and more metazoan there were no significant differences among the three study species present. Both M. velifer and B. burtoni appear to be locations in species richness (F = 0.392, p = 0.677) and moderately tolerant to more saline pools. total abundance (F = 0.348, p = 0.707). Overall, the PCoA of the environmental variables data The dbRDA, using only the three variables selected by (Figure 3b) shows only a slight clumping of pools from the the DISTLM (Figure 4), accounted for 32.8% of the total same location, with a considerable overall mix of rock pools variation in the data, of which 89.1% could be explained by from different locations. However, salinity appears to be the first two axes. Rock pools with more fish tended to be more closely correlated with rock pools from Ponta Marmita. positioned farther to the left in the ordination plot and those This can be explained primarily by the fact that these rock with less fish more to the right. There were a few pools pools were sampled on two consecutive days when there with large numbers of fish that were somewhat smaller in was low precipitation and high solar radiation, conditions volume and had a high total percentage cover (i.e. rock which characterise the peak of the dry season. pools nos. 6, 28, 29). These pools grouped towards the According to the DISTLM, the variation in the fish bottom right corner of the ordination plot (Figure 4). Pools assemblages was better explained by the combination of with smaller volumes closely grouped along a strong three environmental variables: volume, total biological gradient, parallel to the vectors of total % cover and salinity community percentage cover and salinity, in descending (Figure 4). order of most influential (Table 3). Of these significant The values at which the highest species richness and variables, volume and salinity had a more positive influence abundance were observed (Figure 5) were, respectively, at on fish assemblage, whereas the total percentage cover maximum depths of 35 cm and 65 cm; salinities of 32.4 and had a more negative one. Of the remaining variables, the 31.9; temperatures of 31.2 ºC and 31.6 ºC; and pH values average depth, pH, coral percentage cover and macroalgae of 7.996 and 7.964. percentage cover also had a significant impact on fish The observed patterns of distribution of the richness assemblage (Table 3). The presence of other metazoans and abundance of fish species are suggested to be linked was marginally significant. to their physiological tolerances (White et al. 2015). Given The PERMANOVA with the resulting variables of the best their distribution along the different gradients, the species DISTLM model, and with location as the last fixed factor, that showed the greatest flexibility regarding available PCO2 (25.4% of total variation) PCO2 (21.5% of total variation) 360 Azevedo e Silva, Almeida, Cravo, Pais, Santos and Paula Table 3: The influence of rock pool environmental variables on the variation in fish assemblages at Príncipe Island, as revealed by the distance-based linear model (DISTLM) analysis. The best predictive model (with the lowest Akaike information criterion for small sample sizes [AICc]) achieved when testing all possible combinations (BEST routine) was composed of three variables: volume, salinity and total % cover (shown in bold font), and it explained 32.8% of the variance. Prop. = proportion of squared differences; RSS = root sum squared; SS = sum of squares Marginal tests Variable SS (trace) Pseudo-F p-value Prop. (1) Average depth 8 378.6 6.5381 0.002 0.10455 (2) Volume 12 565.0 10.412 0.001 0.15678 (3) pH 2 995.6 2.1745 0.042 0.037379 (4) Salinity 5 077.0 3.7875 0.007 0.063349 (5) Temperature 929.0 0.65674 0.615 0.011592 (6) % Coral 5 147.3 3.8435 0.007 0.064226 (7) % Macroalgae 4 275.2 3.1557 0.022 0.053345 (8) Total % cover 11 426 9.3117 0.001 0.14257 (9) Algae species 2 847.1 2.0627 0.091 0.035525 (10) Metazoan species 3 282.2 2.3914 0.057 0.040954 Overall best solution – AICc R² RSS No. of variables Selections 405.09 0.32814 53 845 3 2; 4; 8 Table 4: Assessment of the effect of location over and above the combined effect of all the covariants selected by the BEST routine using a distance-based linear model (DISTLM) analysis (volume, total % cover, salinity). These were introduced in a permutational multivariate analysis of variance (PERMANOVA) in order of the proportion of squared differences (Prop.) on the DISTLM marginal tests, using a sequential (Type I) sum of squares (SS). MS = mean squares PERMANOVA table of results Unique Variable df SS MS Pseudo-F p-value perms Volume 1 12 565 12 565 12.838 0.001 999 Total % cover 1 10 526 10 526 10.755 0.001 998 Salinity 1 3 206.7 3 206.7 3.2765 0.014 998 Location 2 2 952.7 1 476.3 1.5085 0.16 999 Res 52 50 892 978.7 Total 57 80 143 vertical space and fluctuations in physicochemical Discussion properties were the residents B. burtoni, E. cadenati and M. velifer and the secondary resident A. taurus, which were Fish assemblage composition and abundance seemed the four-most-abundant species. to be influenced mostly by the volume of rock pools, total The stepwise regression analysis was restricted to coverage by flora and fauna, and water salinity. Rock the eight species for which there were sufficient data pools with larger volumes generally supported a higher (Table 5). The presence of A. taurus, M. frontatus and abundance and richness of fish species. The volume of a S. imbricatus was higher in rock pools with larger volumes. tidepool is often a good predictor of the number of fish Entomacrodus cadenati was more significantly correlated it contains (Prochazka and Griffiths 1992; Mahon and with pools with higher macroalgae cover and the presence Mahon 1994; Gibson 1999b), as larger volumes allow for of other organisms. A presence model was not produced more space (and thus more biomass) and also decrease for M. velifer since no variables could significantly predict its the fluctuation of the physicochemical properties of the abundance. Labrisomus nuchipinnis was found more often water (temperature, salinity, pH and oxygen saturation) in pools with larger volumes and more total cover of the throughout tidal and diurnal cycles and variations in bottom by the biological community. Bathygobius burtoni climate conditions (Raffaelli and Hawkins 1999). This and P. biafraensis were more significantly correlated with provides more-stable conditions that a higher number rock pools with larger volumes and minimal biological cover. of fish species can tolerate. This becomes particularly These results can also be observed in the PCoA of fish important in rock pools of tropical rocky shores, as extreme assemblages (Figure 3a). exposure to the heat and sun during the drier seasons can African Journal of Marine Science 2022, 44(4): 353–366 361 36 16 Transform: Log(X+1) 32 37 Resemblance: S17 Bray–Curtis similarity (+d) 38 7 33 10 41 0 53 17 42 59 58 6 12 43 Salinity 28 −20 −40 Location Volume Bom-Bom Total % cover Ponta Marmita Praia Uba −60 −60 −40 −20 0 20 40 dbRDA1 (60.5% of fitted, 19.9% of total variation) Figure 4: Distance-based redundancy analysis (dbRDA) ordination plot of the best DISTLM model based on the species composition matrix using zero-adjusted Bray–Curtis dissimilarities, displaying the relationship between rock pool variables that best explain the variation of fish assemblages among pools at three locations at Príncipe Island. Numbers refer to the ID no. of each rock pool. Vectors represent the correlation of variables with both axes cause dangerous rises in water temperatures (Vinagre oxygen in the water (Martin and Bridges 1999; Raffaelli et al. 2018), and both rainfall, which is heavy in the region and Hawkins 1999), which in turn depend largely on the (Herrero-Barrencua et al. 2017; Chou et al. 2020), and conjunction of the tidal and diurnal cycles at emersion freshwater runoff can considerably decrease the salinity of time, and the presence of animals and plants (Truchot rock pools (Evans et al. 1999; Raffaelli and Hawkins 1999). and Duhamel-Jouve 1980). During the day, pools with The average salinity in rock pools was somewhat coral and macroalgae produce oxygen which overrides lower than expected for the dry season, despite the carbon dioxide released from respiration, and hence the rising temperatures during the day that could lead to high water becomes alkaline during emersion time (Truchot and evaporation in the pools (Evans et al. 1999). This may be Duhamel-Jouve 1980; Martin and Bridges 1999; Raffaelli due to the salinity of the surrounding sea being reduced by and Hawkins 1999), as was observed in this study. At night the influence of the plume of the Congo and Niger rivers during emersion, the pH decreases as more carbon dioxide throughout the Gulf of Guinea at this time of year (Measey is solubilised and there is no oxygen production, rendering et al. 2007; Reid 2011). Any salinity variation in pools with the pools more acidic (Truchot and Duhamel-Jouve similar volumes was most likely caused by local weather 1980; Raffaelli and Hawkins 1999). Thus, rock pools with conditions, such as occasional rainfall before the sampling relatively more macroalgae and/or coral cover will be more period. Across the recorded salinity range, rock pools with susceptible to large and rapid fluctuations in oxygen and higher salinity offered a better environment for marine carbon dioxide, and consequently will have very variable animals and attracted more fishes, although some fish pH values. This occurs especially in small and shallow species showed tolerance to lower salinities. However, the pools that can change by several pH units over the course recorded salinity range is only representative of the weaker of a few hours (Bridges 1993a, 1993b; Martin and Bridges dry season in which this study took place. Thus, it is likely 1999). Thus, only the fish species that are well-adapted that salinity may play a more critical role in determining for respiratory stress are capable of surviving in such fish assemblage variations throughout the seasons (Horn pools, and these tend to be mostly residents and juveniles et al. 1999). of secondary residents. Additionally, oxygen consumption The amount of biological cover on the bottoms of the by residents can exacerbate aquatic hypoxia in tidepools, pools was the second-most-influential variable and it especially in the absence of algae by day, or at night in tended to be negatively correlated to fish composition pools with numerous plants and animals (Truchot and and abundance, especially in smaller-volume pools. It Duhamel-Jouve 1980; Martin and Bridges 1999; Richards possibly reflects the effect on the pH of the water, as pH 2011). Hypoxic conditions further reduce the possibility is affected by the amounts of dissolved carbon dioxide and of other fish species settling. In contrast, large rock pools dbRDA2 (28.5% of fitted, 9.4% of total variation) 362 Azevedo e Silva, Almeida, Cravo, Pais, Santos and Paula SPECIES Maximum no. species 10 Scale (n ) Maximum no. fishes 29 20 7.5 7.7 7.9 8.1 8.3 Figure 5: Distribution of fish species abundance and richness along the observed variation of depth, salinity, temperature and pH in rock pools at Príncipe Island. The lines across the plots represent the value at which the maximum numbers of fish and species were found. For full species names see Table 1 Leptocephalus E. peli A. lopeziana R. subbifrenatus C. nigri A. imberbis C. hippos M. frontatus A. taurus A. saxatilis S. imbricatus T. newtoni E. cadenati M. velifer L. nuchipinnis B. burtoni A. monroviae P. biafraensis C. pullus pH TEMPERATURE (ºC) DEPTH (cm) SALINITY African Journal of Marine Science 2022, 44(4): 353–366 363 Table 5: Relationship between rock pool characteristics and abundance of individual fish species (stepwise regression results) at Príncipe Island. Variables are listed in order of addition in the forward-selection model. Only rock pool characteristics that had a significant effect on fish abundance are displayed Species Variables R² F p-value Abudefduf taurus Volume 0.377 35.032 <0.0001 Microspathodon frontatus Volume 0.204 14.876 0.0003 Stegastes imbricatus Volume 0.388 36.762 <0.0001 Entomacrodus cadenati % Algae 0.110 7.177 0.0100 Other metazoans 0.188 5.442 0.0230 Microlipophrys velifer No variables were entered into the equation Labrisomus nuchipinnis Volume 0.431 45.671 <0.0001 Total % cover 0.506 7.606 0.0078 Bathygobius burtoni Total % cover 0.361 32.704 <0.0001 Volume 0.537 21.686 <0.0001 Prionurus biafraensis Volume 0.132 8.847 0.0043 Total % cover 0.224 6.736 0.0120 are less susceptible to these changes and will have less and secondary residents A. taurus and P. biafraensis were polarised pH values (Raffaelli and Hawkins 1999). Even the most abundant in the eulittoral zone. However, field those that had 80% or more of total biological cover still observations suggest that pools positioned higher in the presented high fish abundance. tidal profile were more often occupied by these species, The location effect was not considered as one of the particularly A. taurus and B. burtoni. Pools lower on the main causes of the differences in fish assemblages. This shore were characterised by noticeably higher species makes sense given that the three rocky shores are similar richness and a more equitable proportion of residents, in geomorphology, exposure and orientation to the sea, and secondary residents and transients, likely because of the have a negligible geographic distance between them. more stable water conditions. The age structure of fish Depth had a considerable effect on the abundance and assemblages is also affected by the vertical position of richness of fish species found in rock pools, being the pools, as some studies have observed that smaller fishes third-most-influential variable for fish assemblages in this are generally more abundant higher up in the intertidal zone study (Table 3). In terms of water conditions, deeper pools (Zander et al. 1999), demonstrating greater tolerance to offer more protection from the heat and sun and allow extreme physicochemical changes. Although no individual the formation of a vertical salinity gradient under rainfall, size measurements were taken in this study, the field allowing fish to shelter at the bottom in higher salinity. observations and underwater video footage provided a In addition, deeper rock pools allow freer movement general qualitative perception of fish sizes. In the eulittoral, of fishes that are more active swimmers or that form residents appeared both as juveniles and adults, whereas schools (Lawson et al. 1999), and offer more protection secondary residents and transients were predominantly from predatory birds, which were frequently seen around and distinctively juveniles, with occasional occurrences the pools preying on trapped fish. These included four of subadults and adults of damselfishes, L. nuchipinnis, species of herons, western reef heron Egretta gularis, little C. atlanticus and moray eels, for example. Pools higher egret E. garzetta, cattle egret Bubulcus ibis and striated on the shore were occupied largely by juveniles, with the heron Butorides striatus, as well as the endemic Príncipe exception of B. burtoni. Rock pools lower on the shore kingfisher Corythornis nais. contained adult residents and noticeably more subadults The structural complexity of the rock pools was not and adults of secondary residents and transients, but still documented during sampling, but structures like rock with an apparent dominance of juveniles. This suggests ledges, caves, crevasses and loose rocks were seen that the rocky shores of Príncipe Island act as a nursery sheltering fish in some rock pools. The presence of area for a number of species, including some with local some of these structures appears to be very important commercial interest, such as S. aurita, R. subbifrenatus, in determining the abundance and choice of habitat of C. nigri, E. adscensionis, C. hippos, S. nigricauda, intertidal fish, which may be linked to predator avoidance A. saxatilis, S. imbricatus, A. monroviae, P. biafraensis behaviour (White et al. 2015). The greater the complexity, and C. pullus (Horemans et al. 1994; Afonso et al. 1999; the greater the availability of cover for fish to hide. Based Direção das Pescas 2015; Tous 2015). Lutjanus griseus on field observations in this study of fish behaviour and the is also commercially exploited elsewhere (Anderson 2002; regular occurrence of predatory birds around rock pools, it Frédou and Ferreira 2005) but has not been recorded in the is likely that structural complexity also plays an important local markets of São Tomé and Príncipe. role in determining fish preference of rock pools on the Six out of the eight species with sufficient data for the island, a hypothesis that requires further study. regression analysis were more likely to be found in rock The vertical position of a rock pool on the rocky shore is pools with larger volumes (i.e. A. taurus, M. frontatus, also known to affect fish community composition (Zander S. imbricatus, L. nuchipinnis, B. burtoni and P. biafraensis). et al. 1999). Residents E. cadenati, M. velifer and B. burtoni Even though these species occupied a variety of pool 364 Azevedo e Silva, Almeida, Cravo, Pais, Santos and Paula environments, including small and shallow ones, the larger in both the intertidal and sublittoral. Although A. taurus was pools are more stable and provide continuously favourable not correlated with coral percentage cover in this study, conditions. Entomacrodus cadenati and M. velifer were, several individuals were regularly sighted in lower intertidal apparently, equally likely to be found in smaller and larger rock pools completely covered with the yellow coral, as volumes. This can be related to the utilisation of different in shallow coastal waters. Eulittoral rock pools covered habitats during different stages of their development as their in coral may develop harsh water conditions, which could size increases (White et al. 2015). explain the absence of correlation with coral percentage In addition to the above eight fish species, the other cover in this study. species observed in rock pools sampled in this study Overall, given the geographic and climate setting of were either secondary residents (E. peli, R. subbifrenatus, Príncipe Island, fish assemblages tend to prefer rock C. hippos, A. saxatilis, T. newtoni and A. monroviae) pools with larger volumes, reduced presence of biological or transients (the leptocephalus, A. lopeziana, C. nigri, cover and higher salinity. However, other within-pool Apogon imberbis and C. pullus). These occurred in low characteristics that were not sampled may also influence abundance and were mostly found in larger and deeper fish presence, in particular the availability of cover (i.e. pools, possibly because they are mostly temporary or rock ledges, caves, and loose rocks) which is likely to be accidental inhabitants of the intertidal zone. They were representative of a preferred habitat (White et al. 2015). found in a narrow range of temperature, salinity and pH Primary and secondary resident species contributed values, in comparison to residents and the more-abundant the most to the fish assemblage structure in our study, secondary residents, suggesting that these species that but the extent to which they do so is likely to vary vertically thrive in open waters are more sensitive to fluctuations in on the shore and seasonally owing to variations in rock pool water conditions. Furthermore, some of these species are conditions (Gibson and Yoshiyama 1999; Zander et al. 1999). pelagic and more-active swimmers (C. hippos, A. saxatilis, Fish distribution may also change seasonally with the arrival T. newtoni, A. monroviae, A. lopeziana), and many of them of juveniles following the breeding season (White et al. 2015) are gregarious, which creates large demands for space and the migration of secondary residents to lower zones on (Lawson et al. 1999; White et al. 2015). Various species, the shore as they grow bigger (Norton and Cook 1999). including P. biafraensis and A. taurus, were often seen The conspicuously small size of many residents, but shoaling within pools, maybe as a mechanism of defence especially secondary residents and transients, indicates against predators. that these rocky shores play a role as a nursery area for Predation by birds is a frequent cause of death in the rock many coastal fish species of Príncipe Island. Future studies pools of Príncipe Island. For primary and secondary resident should focus on the structural complexity of rock pools to fish species that spend a significant part of their life in tide assess the effect of certain structures on fish species pools, predator avoidance is essential to ensure survival. abundance and composition. In addition, seasonal and Two strategies are the use of cryptic colouration and cryptic vertical distribution patterns should be assessed in more behaviour (Gibson 1982). Fish species reliant on colouration detail, also taking into account the size/age structure of fish may choose rock pools in which they can best camouflage populations, to better understand the use of rock pools as themselves. In addition to B. burtoni and P. biafraensis fish nursery grounds throughout the year. being more abundant in larger pools, they were also more Acknowledgements — The authors thank the staff of the Fundação likely to be found in pools with more bare rock, possibly Príncipe and the Príncipe Biosphere Reserve for their support and suitable for camouflage. Their cryptic colouration (Miller help during the various phases of the field and laboratory work at 2016; Rocha 2016) blended well with the rocky black and Príncipe Island. The authors also thank Dr Diana Boaventura and grey bottom. They also displayed cryptic behaviour. When Dr Francisco Andrade for critically reading and commenting on the approached by observers, these fishes often remained still, manuscript. This study was part of the research project COBIO-NET, especially B. burtoni. Juveniles of P. biafraensis sometimes funded by the Aga Khan Foundation and the Fundação para lay sideways against the rock and even adjusted their colour a Ciência e a Tecnologia IP, Portugal (FCT). The study was also slightly between lighter and darker shades. supported by the FCT through the strategic project UIDB/04292/2020 Entomacrodus cadenati, M. velifer and L. nuchipinnis also awarded to MARE and through project LA/P/0069/2020 granted to the ARNET Associate Laboratory. MPP was funded by FCT/FCUL present cryptic colouration (Williams and Springer 2016a, through researcher contract DL57/2016/CP1479/CT0020. 2016b), and in our study these fish were seen changing between darker and lighter colour patterns, allowing them to camouflage themselves against a wide range of surroundings ORCID (rocks, coral, oysters, coralline and other macroalgae, and Armando J Almeida: https://orcid.org/0000-0002-5221-3791 sandy bottoms). Both E. cadenati and L. nuchipinnis were, in João Azevedo e Silva: https://orcid.org/0000-0003-0820-2195 fact, significantly more likely to be found in pools with some Mariana Cravo: https://orcid.org/0000-0003-0022-4648 cover of macroalgae, coral or both. The presence of M. velifer Miguel Pessanha Pais: https://orcid.org/0000-0003-4282-9995 was not correlated with any type of environment since it was José Paula: https://orcid.org/0000-0001-8409-0821 seen in rock pools of all descriptions. Other species also have cryptic colouration in relation to a variety of backgrounds found in rock pools. Abudefduf References taurus, which is yellowish with five vertical brown bars Abreu AD. 2013. Príncipe Island’s Biosphere Reserve (Democratic (Edwards 2016), is camouflaged against surfaces covered Republic of São Tomé and Príncipe): a living laboratory for by the yellow coral P. caribaeorum, which is very common African Journal of Marine Science 2022, 44(4): 353–366 365 sustainable development. 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