Damselfishes play a major functional role in shallow tropical to temperate reef communities (Ceccarelli, 2001). Numerically dominant in different reef zones and habitats (Ceccarelli et al., 2001; Ceccarelli, 2007; Eurich et al., 2018), they present high trophic versatility, from herbivores to invertivores, but many species are considered omnivores (Feitosa et al., 2012; Frédérich, Parmentier, 2016; Eurich et al., 2019). These relatively small fishes take part in multiple energy pathways within reef food webs (Cowan et al., 2016; Pratchett et al., 2016), while exhibiting high site fidelity (Gardiner, Jones, 2005). Multiple species are known to hold territories and by doing so, they enhance algal productivity and overall diversity of benthic algae and associated cryptofauna within large reef habitats (Ferreira et al., 1998; Cleveland, Montgomery, 2003; Hamilton, Dill, 2003; Irving, Witman, 2009; Casey et al., 2014).
Territories are generally presented with abundant turf algae forming a complex, nominally the epilithic algae matrix (EAM), a substrate rich in algae and associated invertebrates and microbiota (e.g., meiofauna, bacteria, detritus) (Ferreira et al., 1998; Ceccarelli, 2007; Casey et al., 2014; Hata, Ceccarelli, 2016). Not surprisingly, these species are among the most aggressive reef fishes (Fontoura et al., 2020), fiercely defending their territories, while affecting the foraging behavior patterns of other species (Francini-Filho et al., 2010). At the same time, the EAM is a major substrate used as primary food source for a diverse set of other reef fishes and invertebrates (Wilson, Bellwood, 1997; Wilson et al., 2003). The degree of habitat modification exerted is, however, highly variable. The level of aggressive behavior displayed, feeding pressure, territory size and weeding intensity may change within species, life phase and at different spatial scales (Hata et al., 2002, 2010; Hata, Kato, 2002, 2004; Ceccarelli, 2007; Feitosa et al., 2012).
As for other species with high site fidelity, habitat selection during recruitment of damselfishes is considered one of the most important driving forces for adult distribution (Munday et al., 1997; Gutiérrez, 1998). However, post-settlement processes (i.e., predation, competition, and migration) are likewise critical, affecting patterns of their distribution at different spatial and temporal scales (Jones, 1991; Carr, Hixon, 1995; Feitosa, Ferreira, 2015). The use of space in territorial reef fish can, therefore, be determined by synergistic factors, such as the availability of preferred microhabitats (Holbrook et al., 2000), abundance of predators (Hixon, Beets, 1993; Almany, 2004), intra- and interspecific competition (Sweatman, 1985; Tolimieri, 1998; Bay et al., 2001) and swimming limitations in high-energy environments (Denny, 2005).
Although damselfishes show clearly structured distribution patterns according to habitat characteristics, spatial distribution patterns of reef fishes can be highly variable on the scale of tens to thousands of meters (Williams, 1982; Meekan et al., 1995; Holbrook et al., 2000; Emslie et al., 2012). At local scales, the relationships of fish composition and abundance were correlated with depth gradients (Green, 1996; Richardson, 1999; Medeiros et al., 2010), exposure (Russ, 1984; Williams, 1991; Gust, 2002; Depczynski, Bellwood, 2005; Floeter et al., 2007) and live coral cover (Bouchon-Navaro, Bouchon, 1989). Large-scale studies have examined the major limiting factors for species distribution, such as temperature (Floeter et al., 2005) and habitat connectivity (Mora, Robertson, 2005). However, for species with extensive distribution ranges, such as several species of damselfishes, the influence of major drivers to their local abundance and distribution has been comparatively poorly investigated (but see Emslie et al., 2012, 2019).
The Brazilian coast extends over 8,000 km of the southwestern Atlantic plus oceanic islands, while reef fishes are distributed along a gradient from tropical to subtropical reefs (Pinheiro et al., 2018). Coral reefs dominate from north to central tropical coast, while subtropical rocky reefs are the main features southwards (Ferreira et al., 2004; Pinheiro et al., 2018). Although considered relatively poor in diversity when compared to the Caribbean and Pacific (Cooper et al., 2009; Tang et al., 2021), Stegastes species are one of the most conspicuous and abundant component of reef fish communities in Brazil (Ferreira et al., 2004; Floeter et al., 2005; Morais et al., 2017; Araújo et al., 2020). Three territorial damselfish species from the genus Stegastes occur along nearshore reefs (Ferreira et al., 2004), while other three endemic species inhabit the oceanic islands (Pinheiro et al., 2018).
Such wide latitudinal distribution and high abundance of damselfishes offer an opportunity to examine driving factors shaping habitat use and relationships between sympatric species along their geographical range in the southwestern Atlantic, both within and among regions of the Brazilian coast. So far, many macro-ecological studies have considered the Brazilian coast an ideal gradient model for reef fish (Ferreira et al., 2004; Floeter et al., 2005; Barneche et al., 2009; Liedke et al., 2016; Morais et al., 2017; Longo et al., 2019) and benthic communities (Aued et al., 2018), but although large patterns of damselfish demography along the coast had been demonstrated, no study has been done to compare abundance patterns at a reef zonation scale. It is critical to understand the dynamics of damselfish assemblages, since they act as habitat modifiers (Ferreira et al., 1998). They occur in high numbers, virtually on the entire Brazilian coast (Ferreira et al., 2004), thus being an important functional group in reef ecosystems.
From tropical to subtropical reefs along the southwestern Atlantic, different habitat features and demographic drivers are expected to influence the spatial distribution and abundance of site-attached fish species. We analyzed patterns of abundance and distribution of three conspicuous territorial damselfishes comparatively in shallow tropical (within depths of 1–7 m) and subtropical reefs (within 1–11 m) of the Brazilian coast. Specifically, we pose these questions: (i) what are the major determinants for Stegastes spp. distribution within different shallow reef habitats? (ii) Are there particular requirements for different life stages (i.e., juveniles vs. adults)? (iii) Are these factors consistent across spatial scales studied (e.g., systems, habitats)?
Material and methods
Study species. The dusky damselfish, Stegastes fuscus (Cuvier, 1830), the cocoa damselfish, Stegastes variabilis (Castelnau, 1855) and the yellowtip damselfish, Stegastes pictus (Castelnau, 1855) are endemic to and widely distributed in the Brazilian Province (Ferreira et al., 2004; Pinheiro et al., 2018; Araújo et al., 2020). The dusky damselfish is one of the most abundant fish on shallow Brazilian coastal reef systems (Ferreira et al., 1998; Menegatti et al., 2003; Osório et al., 2006). Its distribution ranges from Ceará (03°34’5 S 38°24’W), to Santa Catarina (27°36’S 48°23’W). The cocoa damselfish is less conspicuous, but also occurring all along the coast, from Parcel Manoel Luis (00°52’S 44°15’W) to Santa Catarina. The yellowtip damselfish occurs all along the coast and some of the oceanic islands (Pinheiro et al., 2018). Stegastes fuscus and S. variabilis are territorial farming herbivorous (Ferreira et al., 1998; Feitosa et al., 2012), whereas S. pictus is an invertivorous species, feeding either on benthos or on the water column when plankton is abundant (Floeter et al., 2007; authors’ pers. obs.).
Study area and sampling design. Sites studied comprised the tropical fringing reefs of Tamandaré in the northeastern coast of Brazil and the subtropical rocky reefs of Arraial do Cabo in the southeastern coast. These two locations are International Long-term Ecological Program Sites in Brazil: the ILTER Site 18 (PELD-TAMS) and the ILTER Site 22 (RECA) (Muelbert et al., 2019).
The tropical fringing reefs of Tamandaré in the State of Pernambuco (08º44’S 35º05’W) are located in the upper limit of the Marine Protected Area APA Costa dos Corais, which extends 135 km along the northeastern coast of Brazil. Coral reefs are composed of three main reef lines parallel to the coast (Maida, Ferreira, 1997). Stegastes territories are widespread along shallow water reef lines, occupying reef surfaces (up to 2 m deep), where benthic cover in their surroundings is mainly composed of thick articulated calcareous algae (Jania spp. and Halimeda opuntia), and other macroalgae (Feitosa et al., 2012). The zoanthid Palythoa caribaeorum and sparse colonies of the fire-coral Millepora alcicornis are also important components of benthic coverage. The area has a tropical climate with an established regime of rainy (May to September) and dry (October to May) seasons that reach minimum and maximum water temperatures of 26 ºC and 30 ºC, respectively (Maida, Ferreira, 1997).
The subtropical rocky reefs of Arraial do Cabo in the state of Rio de Janeiro (22°59’S 42°00’W) was established as a Marine Extractive Reserve (RESEX Mar Arraial do Cabo) since 1997, a type of sustainable use conservation unit. The rocky shores formed by granite boulders reach 20–30 m of extension from the surface to the interface with the sand flats, with maximum depths of 15 m during high tides. Stegastes territories have dense algal mats 1–3 cm high that are usually dominated by the articulated calcareous algae, Jania spp. and Amphiroa sp. Within territories, these algae alternate with colonies of the fire coral M. alcicornis and the zoanthid P. caribaeorum (Ferreira et al., 1998). The mean water temperature in the study sites is approximately 22 ºC year round, reaching an averaged maximum of 25 ºC (Ferreira et al., 2001) and a minimum of 18 ºC, indicating that this region is under the influence of coastal upwelling during the summer/spring periods (Valentin, 1984). The reefs studied, however, are sporadically affected by cold waters and typically only in the deeper portions (Ferreira et al., 1998).
The distribution of the damselfishes S. fuscus, S. variabilis and S. pictus within systems were examined between December 2009 and February 2010, the summer season at both latitudes. Given the inherent structural differences of distinct reef formations, the sampling was adjusted to examine effects of exposure to wave surge in each habitat. In coral reefs of Tamandaré exposure was assessed in the two reef lines further away from the shoreline and at different sections. In the second line, the back reef was characterized as sheltered and the fore reef as exposed. In the third line, both back and fore reefs of deeper reefs (up to 7 m) were characterized as sheltered, due to lower wave surge effects observed. The selected reefs were large enough to separate second and third reef lines by at least 700 meters, and several small sites were sampled in two portions of the reef complex, 2 km apart from each other, allowing distance enough for site independence among samples (Figs. 1A,B). To assess exposure in Arraial do Cabo, two continuous rocky reefs were selected, subject to distinct intensities of wave surge, i.e., exposed and sheltered rocky shores, where three sites at least 700 meters apart from each other were determined (Figs. 1C–E). Also, each site comprised an area wide enough to ensure spatial independence among samples, observing the territorial nature of damselfishes studied (which holds territories of 1–2 m2, Ferreira et al., 1998; Osório et al., 2006; Medeiros et al., 2010). The sites chosen within each reef system presented the same orientation to the coast, so that levels of exposure to wave surge were comparable. Sampling was done at a continuous range of depth from 1 to 11 m, which represent depths where the majority of damselfish can be found.
FIGURE 1 | Map of studied tropical and subtropical reef systems in the Brazilian coast (South America) with respective reef profiles. 1. Fringing coral reefs (tropical system); 2. Rocky reefs (subtropical system). A. Overview of sites sampled in Tamandaré tropical reefs; B. Reef profiles indicating the positioning of sheltered and exposed tropical reefs; C. Overview of sites sampled in Arraial do Cabo subtropical reefs; D. Reef profile at exposed reefs; E. Reef profile at sheltered reefs. EX = Exposed sites; SH = Sheltered sites.
Fish surveys. Replicated 10 x 2 m belt transects were laid with an overall total of 180 transects (90 for each system). Samples were collected along a measuring tape laid on the reef surface, which was always placed at least 20 m away from another transect and sampled on the same day for each site and depth to avoid pseudo-replication. The visual census started after a 3 min period to allow fish to acclimate to the diver’s presence. To avoid edge effects, if an individual was not within a given transect, but at least 50% of its territory was inside the transect boundaries, the fish was still included in the counts. Fish were counted and grouped into life stages (juveniles and adults). While individual fish length was visually estimated, the conspicuous coloration of juveniles was the decisive factor in assigning fish into each life stage. It is important to note that length was slightly different for the studied reef systems (i.e., subtropical fish attain larger size ranges within stages; LCTC and collaborators, work in progress), as well as the distinct coloration patterns of adult S. variabilis between the two systems (Souza et al., 2011) (Fig. 2).
FIGURE 2 | Color patterns of damselfishes studied in their juvenile and adult life phases. A. Stegastes fuscus juvenile; B. S. fuscus adult; C. Stegastes variabilis juvenile; D. S. variabilis adult (in subtropical reefs); E. S. variabilis adult (in tropical reefs); F. Stegastes pictus juvenile; G. S. pictus adult. Image credits to A Bertoncini (A, C, D, F and G) and JLL Feitosa (B and E).
Benthic communities and reef complexity. In both reef systems, the benthic cover was estimated using 40 x 40 cm photoquadrats, taken at each 2 m of the transect used for fish censuses, distributed along the transect from 0 to 10 m (6 samples per transect; totaling 1080 photos). The images were later processed in CPCe 3.5 Software (Kohler, Gill, 2006), where 30 points were overlaid on each image, and organisms underneath were identified and classified in functional groups. The major functional groups defined were: massive corals (Siderastrea stellata, Montastraea cavernosa, Mussismilia hartii, Mussismilia hispida, Porites astreoides), branching corals (Millepora spp.), zoanthids (P. caribaeorum, Zoanthus spp.), erect macroalgae (mainly from the genera Sargassum, Caulerpa, Codium, Gracilaria, Dictyota, Dictyopteris), crustose calcareous algae, articulated calcareous algae (Jania spp., Amphiroa sp., H. opuntia), filamentous algae (Gelidium sp., Ceramium sp., Bryopsis sp.), urchins (Echinometra lucunter, Lytechinus variegatus), non-biotic substrate (sand, bare rock, rubble) and other organisms (sponges, ascidians, barnacles). Reef structural complexity was characterized by two metrics: number of holes per size class and rugosity. Quantity and diameters of holes were estimated on photoquadrats, measured in CPCe, and later categorized in size classes by maximum diameter (< 5 cm, 5–10 cm, and > 10 cm). Rugosity was measured in situ, using a modified chain-link method from Luckhurst, Luckhurst (1978), where a chain was laid along the entire transect line. The rugosity index was obtained from the relationship of the chain length divided by the length of the transect line (i.e., 10 m), which was used as the linear distance.
Data analyses. Species densities were compared between systems using the non-parametric Mann-Whitney tests, performed at each life stage (see Tab. S1). To characterize the diversity of microhabitats observed within both reef systems, variables associated with benthic cover and reef complexity were analyzed through a Principal Components Analysis, performed after standardization of variables per sample. These variables were then reduced into groups (PC scores), and later included in the predictive models for distribution of damselfishes, as described below. This analysis was performed in Primer-e 6 software (Clarke, Warwick, 2001).
To determine the most important factors describing distribution in damselfishes, a generalized linear mixed model (GLMM) was performed for each species and life phase, considered separately for each reef system (Tabs. S2). As S. pictus was only detected in one system and did not have enough individuals to enable analysis by separate life stages, data on juvenile and adult densities were pooled and nine models were fitted. We explored the data for each species and determined that a negative binomial distribution was the most adequate for most of the damselfish species, except for S. fuscus adults, which in both reef systems showed a better fit with Gaussian distribution. Five factors were used for fitting the model: exposure (considered as a categorical predictor, with exposed and sheltered sites as levels), depth (continuous variable), and the PC Axes (1, 2 and 3), obtained in the aforementioned PCA analysis, which represented proxies for microhabitat features. Such an approach allowed condensing 14 microhabitat parameters analyzed into three, avoiding oversaturated models, while considering the effects of the major differences in microhabitat. Prior to model fitting, these variables were tested for collinearity using a logistic regression model with all variables. We also examined the variance inflation factor (VIF) for each variable, considering VIF > 2 as a threshold to determine collinearity, following Graham (2003), and all variables were independent. GLMMs were computed using the ‘glmmadmb’ function of the ‘glmmADMB’ package available in R (Skaug et al., 2016). This analysis accounts for zero-inflation, an attribute observed for damselfish data. Spatial variation between samples under the same exposure regime (within exposed or within sheltered sites) was considered as a random effect variable. The backward stepwise removal of non-significant terms from the full model, based on log-likelihood ratio tests was applied for model selection (Zuur et al., 2009), also considering models with lowest value of Akaike information criterion (AIC) (Burnham, Anderson, 2004) (see Tabs. S3). All data in the manuscript can be made available upon request to the corresponding author.
More than 3500 damselfish were counted during this study: ~1500 individuals were observed in subtropical reefs and ~2000 in tropical coral reefs. Stegastes fuscus was the most abundant species in both systems, corresponding to ~88% of total damselfish abundance (73% adults, 15% juveniles), followed by S. variabilis, which accounted for 9% of the fish counted (5% adults, 4% juveniles). Slightly less than a hundred individuals of Stegastes pictus were observed (~3% of the total damselfish abundance), all of them recorded in subtropical reefs. No Stegastes pictus were counted in most censuses, but at some sheltered subtropical sites they reached densities of up to 15 individuals/20 m², indicating a specificity of their distribution to some sites only (Fig. 3). A few settlers were occasionally observed outside of our sampling area in tropical reefs (n = 2), indicating that this species has no established populations on the studied shallow reefs of Tamandaré.
FIGURE 3 | Densities of the three damselfish (adults and juveniles) species between tropical and subtropical reefs of the Brazilian coast. Box-plots show the median (line) and quartiles distributions. *Significant differences in Mann-Whitney tests; ns = non-significant differences; NA = no tests were applicable.
In both tropical and subtropical systems, benthic cover was a major feature for sample segregation and evidence of habitat selection by damselfish at the local scale. The first three PCA axes explained together 84.5% of variation (PC 1 = 38.7%, PC 2 = 27.8% and PC 3 = 18.0%). The main factors responsible for variation between samples in PC 1 were zoanthids (negatively) and articulated calcareous algae; in PC 2 were macroalgae (negatively) and articulated calcareous algae and; in PC 3 branching corals, articulated calcareous algae (negatively) and crustose calcareous algae were the most distinctive features (Fig. 4). Despite the fact that mean rugosity in tropical reefs had higher values than in subtropical reefs (mean ± standard deviation: 1.62 ± 0.2 vs. 1.56 ± 0.2), and higher frequency of holes of different sizes (5.26 ± 2.8 vs. 1.58 ± 1.9), complexity predictors had a minor contribution for explaining the variation among samples. In general, most of the samples were distributed around articulated calcareous algae dominance in both tropical and subtropical reefs. Samples dominated by macroalgae were almost exclusively observed in the tropical system, whereas higher coverage of zoanthids and branching corals/crustose calcareous algae were more frequent in subtropical reefs (Fig. 4).
FIGURE 4 | Principal Component Analysis of benthic cover and habitat predictors. For viewing purposes, vectors for variables with low scores (< 0.100 on axis displayed on each plot) were omitted from graphs. Variable contribution to each PC axis is presented on the table. Macroalgae (macal), articulated calcareous algae (artic), filamentous algae (filam) zoanthids (zoa), branching corals (branch), crustose calcareous algae (crust).
The selected predictors of damselfishes abundances are summarized in Figure 5. Adults of S. fuscus in both systems were highly associated with habitats dominated by articulated calcareous algae (positive relationship with PC2), the dominant species within turfs, but negatively associated with erect macroalgae-dominated habitats. Stegastes fuscus also showed some association with zoanthid-dominated habitats (according to the negative relationship with PC1, in the subtropical system only), which occur at the same depths as turf algae. Similarly, adults of S. variabilis had a negative relationship with PC1, indicating a weak association with articulated calcareous algae and/or a preference for zoanthid-dominated habitats. Conversely, juveniles were associated with habitats dominated by macroalgae, and were the only group with a negative relationship with PC2. Although PC3 contributed to almost 20% of sample variation, none of the species/life phase showed any relationship with the variables pertaining to this axis, so branching corals and crustose algae seem to have little contribution to damselfish distribution in both systems. These benthic groups, although often nearby, are rarely within territorial boundaries of studied damselfishes.
When compared to wave exposure and depth, benthic cover had a lesser explanation power and contributed to finer-scale local changes in damselfish distribution (Fig. 5). Wave exposure was the variable that most contributed to explain damselfish abundances in both systems, composing the models for all species but S. fuscus juveniles in the subtropical region. This life phase of S. fuscus had a distribution that was less consistently predicted by the variables considered herein. Depth was also a significant variable in determining damselfish distribution, and it was selected among five of the nine models fitted (Fig. 5). Although not a good predictor for S. fuscus abundance, in subtropical reefs, S. variabilis — regardless of the life phase — inhabited shallower areas, whereas S. pictus was almost exclusively found in deeper waters (mainly > 7 m). In the tropical system, the juveniles of S. fuscus and adult S. variabilis were exclusively observed in shallower habitats. Stegastes fuscus was more abundant on sheltered sites and this pattern was particularly evident for the subtropical system, where a two to three-fold greater numbers were observed. Adult S. variabilis, although observed in much lower densities, had comparatively higher densities in the subtropical reefs and in more exposed sites (Fig. 5).
FIGURE 5 | Predictors of damselfish densities on subtropical and tropical reefs. GLM coefficients are standardized for the selected factors. PC1–3 are axes extracted from Principal Component Analysis (Fig. 4), representing benthic cover and reef complexity characteristics. Values for non-significant predictors are presented in gray. Error bars denote standard error of coefficients.
This study investigated the distribution patterns of territorial damselfish assemblages, as well as the associated benthic communities comparatively in tropical and subtropical reef systems approximately 2,200 km apart along the Brazilian coast. These systems are very distinct due to their origin (non-biogenic and biogenic), morphology (rocky reefs and fringing reefs), and latitude (subtropical and tropical), and yet, patterns of distribution of damselfishes inhabiting both systems show similar responses to environmental drivers. Exposure to wave surge and depth were the most important predictors influencing patterns of abundance of these species within both systems. Reef complexity, although important to explain general patterns of richness and abundance in reef fish assemblages (McCormick, 1994; Chabanet et al., 1997; Friedlander, Parrish, 1998; Medeiros et al., 2011), did not play a major role influencing the distribution of damselfishes at the scales of reefs analyzed. Benthic cover accounted only for fine-scale changes in local abundance of different life phases for each species.
Stegastes fuscus was by far the most abundant territorial damselfish in all habitats analyzed regardless of the environmental conditions present. Previous studies along the Brazilian coast corroborate such dominance (Ferreira et al., 2004; Floeter et al., 2005, Longo et al., 2014). Stegastes variabilis and S. pictus occurred at much lower densities than S. fuscus. Stegastes pictus was not detected in shallow tropical habitats studied, where reefs closer to the coastline occur continuously for more than 2 km (Figs. 1A,B). Stegastes pictus is known to occur more frequently in deeper reefs (18–25 m), far from the shore (Floeter et al., 2007; Soares et al., 2018). In contrast, the subtropical rocky shores, with relatively short and steep/vertical relief from shallow to deeper rocky-sandy interface habitats (ca. 10 m deep and average 25 m in length), provided substrate for a well established population of S. pictus (Ferreira et al., 2001).
Exposure to wave surge was a reliable explanatory variable in our models, as previously reported to influence abundance patterns of pomacentrids in both the southeastern (Floeter et al., 2007) and northeastern Brazilian coast (Medeiros et al., 2010). In subtropical reefs, sheltered habitats sustained higher densities of adult S. fuscus, in comparison to adult S. variabilis densities, which is more abundant in exposed sites. Such an effect was detected in the tropical system, but at a much lesser extent, as the exposure to wave surge is attenuated by the barrier reef system. Swimming performance limitations are known to influence the majority of the ecological activities of coral reef fishes including settlement, foraging and reproduction from relatively small to large spatial scales (Kawamata, 1998; Fulton et al., 2001; Fisher, Bellwood, 2003; Blake, 2004; Denny, 2005; Fisher, 2005; Fulton, Bellwood, 2004, 2005). Many studies on reef fish ecomorphology had shown overall distribution patterns explained as a result of adaptations to distinct swimming and feeding modes (Fulton et al., 2001; Bellwood et al., 2002; Johansen, Jones, 2011). For instance, S. fuscus and S. variabilis are both herbivorous species, and very similar in morphology (Araújo et al., 2003; Medeiros et al., 2010; Feitosa et al., 2012). By contrast, S. pictus is smaller than its herbivorous counterparts, with a more pronounced forked caudal fin, which allows it to explore both benthic substrate and the water column, feeding upon both benthic and planktonic invertebrates (Floeter et al., 2007). This morphological adaptation and feeding plasticity also allow this small damselfish to inhabit a diversity of deeper and offshore habitats where water flow and currents provide rich sources of plankton (Pinheiro et al., 2018).
In addition to exposure, depth was also a good predictor of abundance of these damselfishes. As depth increases, environmental conditions, such as light intensity and water motion decline, affecting algal photosynthetic rate and nutrient uptake (Hay, 1981). Following this trend, S. fuscus and S. variabilis, thrive in shallow habitats where primary production peaks and diversity and biomass of preferred filamentous algae is augmented (Ferreira et al., 1998). Their territorial and feeding behaviors increase the likelihood of competition between them. However, S. fuscus is relatively large and more aggressive (Medeiros et al., 2010), hence its dominance.
Benthic communities were variable overall, but seemed to be more stable in sheltered sites, which may be associated with S. fuscus preference for these habitats. It is worth noting that dominant taxa in benthic communities often changed in distribution at the same scales as the damselfish studied here (i.e., latitude, wave exposure and depth), as had been previously described elsewhere (Connolly et al., 2003; Adjeroud et al., 2007; Bongaerts et al., 2013) and more recently, in the Brazilian coast (Aued et al., 2018). The major difference in benthic communities when comparing the more exposed reefs of both systems was the large contribution of macroalgae in the tropics and zoanthids and branching corals (milleporids) in the subtropics. It is generally accepted that the environmental gradients created by the interaction of exposure and depth are linked to both physical (temperature, light, currents) and biological (habitat and food availability) features, thus likely influencing the settlement and survival of damselfishes and benthic organisms (Meekan et al., 2003; Bergenius et al., 2005; McCormick, Hoey, 2006; Sponaugle et al., 2006).
More often than not, the heterogeneity created by such environmental gradients allow multiple species to coexist (Fulton, Bellwood, 2005; Brokovich et al., 2008; Jankowski et al., 2015). In a more diverse community of cohabiting damselfishes, species may develop a high degree of substratum specificity (Waldner, Robertson, 1980; Robertson 1984; Precht et al., 2010; Chaves et al., 2012). For instance, live coral is a major driver of damselfish distribution in many reef systems (Munday et al., 2008; Wilson et al., 2008; Chaves et al., 2012; McCormick, 2012; Garcia-Herrera et al., 2017; MacDonald et al., 2018). In the systems studied herein, the less-diverse damselfish assemblages may lead to lower substrate specificity by species. This is largely supported by our results, where exposure and depth were the most prevalent predictors of damselfish abundance in both tropical and subtropical reef systems.
Additional evidence of this lower substrate specificity is the lack of association of younger individuals to the proxies used for reef structural complexity (i.e., frequency/size of holes and rugosity). It is safe to assume that early life stages are usually under higher mortality rates, along with a high degree of intraspecific competition with adults; a plausible explanation for low numbers of early stage individuals encountered. Damselfishes are known to spawn year-round (e.g., S. fuscus; Souza et al., 2007) and a high degree of self-recruitment is observed for this group (Jones et al., 1999; Christie et al., 2010; Berumen et al., 2012). Additionally, age studies have demonstrated a moderate lifespan for S. fuscus (15–17 years), with accumulation of several adult cohorts on the same reef (Schwamborn, Ferreira, 2002; LCTC and collaborators, work in progress). Not surprisingly, juveniles of all species (but S. variabilis in the tropics) somewhat shared similar habitat relationships with adults of their species. Nonetheless, high quality refuges, as a means of predator avoidance are still relevant for younger and/or smaller individuals (Hixon, Beets, 1993; Carr, Hixon, 1995; Figueira et al., 2008; Komyakova et al., 2013; Quadros et al., 2019).
As much as our results show congruence with previously reported drivers of damselfish distribution, Brazilian reefs hold particularities associated with a low diversity system. Size actually matters, as S. fuscus largely dominate damselfish assemblages in varied habitats, while other species attain higher densities in peripheral, less-preferred sites. This scenario clearly indicated how important interspecific competition shapes damselfish assemblages along the Brazilian coast, where the large species, S. fuscus dominates shallow and more productive habitats to establish territories. This pattern is prevalent all along the Brazilian coast from tropical to subtropical reefs (Ferreira et al., 2004; Pinheiro et al., 2018). Parcel de Manuel Luiz, a mid-shore reef in the north coast of Brazil, is the only reef system known where S. variabilis is the dominant damselfish (Cordeiro et al., 2021).
Turfs are the dominant component in tropical and subtropical reefs in the Brazilian Province (Aued et al., 2018). The synergistic effects of warming oceans, increasing coral bleaching, eutrophication and overfishing (Bellwood et al., 2004; Pratchett et al., 2011; Hughes et al., 2017; Hughes et al., 2018) are leading coral reefs towards phase-shifts, where turf algae prevail. In most reef systems of the Brazilian coast, turf communities are largely dominated by articulated calcareous algae (e.g., Jania spp., Amphiroa spp.) (Ferreira et al., 1998). These algae form a thick turf matrix, composed by the epilithic algal community. This matrix is very productive and provide primordial substrate to epiphytes (i.e., red filamentous and diatoms), which are comparatively more nutritious than algal communities in the surroundings, and comprise the bulk of S. fuscus and S. variabilis diets (Ferreira et al., 1998; Feitosa et al., 2012). A scenario of homogenization of benthic features can be detrimental to the functional diversity of reef communities, but in effect, may benefit damselfishes, such as S. fuscus. However, in the Mediterranean and Australia, “bad turfs” with high percentage of innutritious sediment had been indicated as an undesirable habitat condition for herbivorous fishes (Airoldi, 1998; Tebbett et al., 2018), even for these territorial fish exhibiting high tolerance to variable environmental conditions (Feitosa et al., 2012; Eurich et al., 2019).
The forecast scenarios of sea level rise and increased sedimentation on coral reefs (Morgan et al., 2020), as well as changes in oceanographic conditions such as prevalence of strong winds and more hydrodynamic environments (Saunders et al., 2014), may also directly affect the distribution of these species, and consequently, influence their role under adverse conditions. Only by continuously monitoring and conducting experiments, we will understand how these fishes will persist in shallow, ever-changing reef systems of the Brazilian coast and reefs worldwide.
Many thanks to the staff of Centro de Pesquisa e Extensão Pesqueira do Nordeste (CEPENE) in Tamandaré and ICMBio (RESEX Mar AC) for providing facilities and local support. Special thanks to Andreza Pacheco, Felipe Ribeiro, Renata Mazzei, Diego Medeiros, Simone Marques and Pedro Pereira for field support. I also thank Allan Souza, Francisco Barros, Paulo Santos, Caroline Feitosa, Liz McGinty for revision and contributions in earlier drafts of this manuscript. Photo credits in Fig. 2 (A, C, D, F and G) to Áthila Bertoncini through the projects Meros do Brasil and Ilhas do Rio. The financial support for this work was provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) as a PhD scholarship and PADI Project Aware awarded to LCTC during the period of study. CELF and BPF are continuously supported by a CNPq research grant.
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 Departamento de Zoologia, Universidade Federal de Pernambuco, Av. Professor Moraes Rego s/n, Cidade Universitária, 50670-420 Recife, PE, Brazil. (JLLF) firstname.lastname@example.org, (TFX) email@example.com.
 Tropical Conservation Consortium, 10413 Southwest 40th Avenue, 97219 Portland, OR, USA.
Laís de Carvalho Teixeira Chaves: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Writing-original draft, Writing-review and editing.
João Lucas Leão Feitosa: Formal analysis, Methodology, Visualization, Writing-review and editing.
Túlio Freire Xavier: Writing-review and editing.
Beatrice Padovani Ferreira: Conceptualization, Funding acquisition, Methodology, Supervision, Writing-original draft, Writing-review and editing.
Carlos E. L. Ferreira: Conceptualization, Methodology, Supervision, Writing-original draft, Writing-review and editing.
The authors declare no competing interests.
How to cite this article
Chaves LCT, Feitosa JLL, Xavier TF, Ferreira BP, Ferreira CEL. Drivers of damselfishes distribution patterns in the southwestern Atlantic: tropical and subtropical reefs compared. Neotrop Ichthyol. 2021; 19(4):e210010. https://doi.org/10.1590/1982-0224-2021-0010
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Diversity and Distributions Published by SBI
Accepted June 23, 2021 by Fernando Gibran
Submitted January 11, 2021
Epub December 10, 2021