Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison

Aim To investigate how reef fish trophic structure responds to latitudinal changes, using a simple model: the extensive Brazilian coast. Location Six Brazilian tropical and subtropical coral and rocky coastal reefs, and the oceanic island of Atol das Rocas, between latitudes 0° and 27° S. Methods Underwater visual census data collected by the authors (five locations) or obtained from the literature (two locations) were used to estimate the relative abundance of 123 fish species belonging to 33 reef‐associated families. Cryptic species were excluded from the analysis. Fishes were grouped in eight trophic categories: roving herbivores, territorial herbivores, mobile invertebrate feeders, sessile invertebrate feeders, omnivores, planktivores, piscivores and carnivores. After a series of detailed predictions based on phylogeny, physiological constraints and anthropogenic impacts was established, the community trophic structure was analysed along a latitudinal gradient and among coastal, mid‐shore and oceanic sites. Results The trophic structure of Brazilian reef fish assemblages clearly changed with latitude. Roving herbivores such as scarids and acanthurids were proportionally more abundant at low latitudes. The browsing herbivores kyphosids followed an opposite latitudinal pattern. The parrotfish genus Sparisoma, more plastic in its feeding habits than Scarus, presented wider distribution. The relative abundance of territorial herbivores did not decrease towards higher latitudes. Mobile invertebrate feeders were the most important (in low latitudes) or the second most important trophic guild (in high latitudes) at all coastal sites. Sessile invertebrate feeders did not show any clear latitudinal trend, despite an expected increase in abundance towards low latitudes. Omnivores dominated high latitude reefs (27° S) and planktivores the oceanic island Atol das Rocas. Piscivores and carnivores were proportionally better represented in high latitudes. Main conclusions Latitudinal patterns seem to be influenced by phylogeny, physiological constraints (mainly related to temperature), and also by anthropogenic impacts. Grazing scarids and acanthurids are largely restricted to tropical reefs and show an abrupt decline beyond 23° S. This does not reflect the amount of algae present, but probably temperature‐dependent physiological constraints. Other herbivores seem to overcome this through symbiotic microbial digestive processes (kyphosids), manipulating the structure of algal turfs or increasing animal protein from within the territory (pomacentrids). Omnivores dominate the southern sites Arraial do Cabo and Arvoredo, being more adapted to environment constraints related to seasonal and/or stochastic shifts. Large carnivores (including piscivores) extend farther into high‐latitude habitats, apparently not constrained by thermal thresholds that limit the herbivores. Overfishing and/or ornamental harvesting certainly has been modifying local fish communities, but could not be detected properly at the large‐scale patterns found in this study. The data presented put in evidence for the first time how reef fish trophic structure behave in the extensive south‐western Atlantic latitudinal gradient.     

Reef fish structure and distribution in a south-western Atlantic Ocean tropical island

The community structure of the reef fish fauna of Trindade Island, a volcanic oceanic island located 1160 km off the coast of Brazil, is described based on intensive visual censuses. Seventy-six species were encountered in 252 censuses, with mean ± S.E. of 99 ± 3 individuals and 15.7 ± 0.3 species 40 m(-2) transect. The average fish biomass, calculated from length-class estimation, was 22.1 kg 40 m(-2) transect. The species contributing most to biomass were, in decreasing order, Melichthys niger, Cephalopholis fulva, Kyphosus spp., Holocentrus adscensionis, Sparisoma amplum, Sparisoma axillare, Acanthurus bahianus and Epinephelus adscensionis. Carnivorous fishes were the largest trophic group in terms of biomass, followed by omnivores and roving herbivores. The two predominant types of reef habitat, fringing reefs built by coralline algae and rocky reefs made of volcanic boulders, showed significant differences in the biomass and the abundance of the trophic guilds. Within each habitat type, significant differences in species richness, density and biomass were detected among crest, slope and interface zones. Although similar in overall species composition to coastal reefs in Brazil, the fish fauna of Trindade Island shares certain characteristics, such as a high abundance of planktivores, with other Brazilian oceanic islands. Despite comparatively high fish biomass, including the macro-carnivorous species habitually targeted by fisheries, signs of overfishing were evident. These findings highlight the urgency for a conservation initiative for this isolated, unique and vulnerable reef system.     

Reef Fishes at All Trophic Levels Respond Positively to Effective Marine Protected Areas

Marine Protected Areas (MPAs) offer a unique opportunity to test the assumption that fishing pressure affects some trophic groups more than others. Removal of larger predators through fishing is often suggested to have positive flow-on effects for some lower trophic groups, in which case protection from fishing should result in suppression of lower trophic groups as predator populations recover. We tested this by assessing differences in the trophic structure of reef fish communities associated with 79 MPAs and open-access sites worldwide, using a standardised quantitative dataset on reef fish community structure. The biomass of all major trophic groups (higher carnivores, benthic carnivores, planktivores and herbivores) was significantly greater (by 40% - 200%) in effective no-take MPAs relative to fished open-access areas. This effect was most pronounced for individuals in large size classes, but with no size class of any trophic group showing signs of depressed biomass in MPAs, as predicted from higher predator abundance. Thus, greater biomass in effective MPAs implies that exploitation on shallow rocky and coral reefs negatively affects biomass of all fish trophic groups and size classes. These direct effects of fishing on trophic structure appear stronger than any top down effects on lower trophic levels that would be imposed by intact predator populations. We propose that exploitation affects fish assemblages at all trophic levels, and that local ecosystem function is generally modified by fishing.     

Comparison of remote video and diver's direct observations to quantify reef fishes feeding on benthos in coral and rocky reefs

This study compared remote underwater video and traditional direct diver observations to assess reef fish feeding impact on benthos across multiple functional groups within different trophic categories (e.g. herbivores, zoobenthivores and omnivores) and in two distinct reef systems: a subtropical rocky reef and a tropical coral reef. The two techniques were roughly equivalent, both detecting the species with higher feeding impact and recording similar bite rates, suggesting that reef fish feeding behaviour at the study areas are not strongly affected by the diver's presence.     

The role of the reef flat in coral reef trophodynamics: Past,present, and future

The reef flat is one of the largest and most distinctive habitats on coral reefs, yet its role in reef trophodynamics is poorly understood. Evolutionary evidence suggests that reef flat colonization by grazing fishes was a major innovation that permitted the exploitation of new space and trophic resources. However, the reef flat is hydrodynamically challenging, subject to high predation risks and covered with sediments that inhibit feeding by grazers. To explore these opposing influences, we examine the Great Barrier Reef (GBR) as a model system. We focus on grazing herbivores that directly access algal primary productivity in the epilithic algal matrix (EAM). By assessing abundance, biomass, and potential fish productivity, we explore the potential of the reef flat to support key ecosystem processes and its ability to maintain fisheries yields. On the GBR, the reef flat is, by far, the most important habitat for turf‐grazing fishes, supporting an estimated 79% of individuals and 58% of the total biomass of grazing surgeonfishes, parrotfishes, and rabbitfishes. Approximately 59% of all (reef‐wide) turf algal productivity is removed by reef flat grazers. The flat also supports approximately 75% of all grazer biomass growth. Our results highlight the evolutionary and ecological benefits of occupying shallow‐water habitats (permitting a ninefold population increase). The acquisition of key locomotor and feeding traits has enabled fishes to access the trophic benefits of the reef flat, outweighing the costs imposed by water movement, predation, and sediments. Benthic assemblages on reefs in the future may increasingly resemble those seen on reef flats today, with low coral cover, limited topographic complexity, and extensive EAM. Reef flat grazing fishes may therefore play an increasingly important role in key ecosystem processes and in sustaining future fisheries yields.     

Seasonally changing habitat use patterns among roving herbivorous fishes in the southern Red Sea: the role of temperature and algal community structure

Coral reefs are characterized by intense herbivory. Spatial patterns in herbivory—particularly along the depth gradient—influence the distribution and abundance of algae. Depth gradients in herbivorous reef fishes are generally assumed to be temporally stable, but this assumption has rarely been questioned. Here, we use underwater visual census and herbivore exclusion experiments to study the community composition and temporal patterns in habitat use by roving herbivorous fishes in an environment characterized by profound seasonal changes in algal biomass and distribution and extreme summer temperatures. Among the 18 species of roving herbivores recorded, parrotfishes were dominant in species richness and biomass, while regional endemic species represented 77 % of the total biomass. During most of the year, roving herbivores aggregate in the shallow reef zones and their biomass declines with depth. The herbivore community on the reef flat is distinct from that in deeper zones. The former is characterized by Siganus rivulatus, Acanthurus gahhm and Hipposcarus harid, while the deeper reef zones are characterized by S. ferrugineus, Chlorurus sordidus and Ctenochaetus striatus. In summer, the distinct community structures among reef zones are lost as reef flat herbivores tend to exploit deeper reef zones and some reef crest species venture on to the reef flat. This summer change in herbivore distribution is also reflected in reduced turf biomass and increased yield to herbivores in the deeper reef zones. Habitat use is related to the feeding mode such that browsers dominate the reef flat and scrapers the reef crest, while the seasonal changes correspond to changes in availability of targeted algal resources. These seasonal changes appear to be driven by the extreme temperatures in summer, reaching 36 °C on the shallow reef flat.     

High macroalgal cover and low coral recruitment undermines the potential resilience of the world's southernmost coral reef assemblages

Coral reefs are under increasing pressure from anthropogenic and climate-induced stressors. The ability of reefs to reassemble and regenerate after disturbances (i.e., resilience) is largely dependent on the capacity of herbivores to prevent macroalgal expansion, and the replenishment of coral populations through larval recruitment. Currently there is a paucity of this information for higher latitude, subtropical reefs. To assess the potential resilience of the benthic reef assemblages of Lord Howe Island (31°32'S, 159°04'E), the worlds' southernmost coral reef, we quantified the benthic composition, densities of juvenile corals (as a proxy for coral recruitment), and herbivorous fish communities. Despite some variation among habitats and sites, benthic communities were dominated by live scleractinian corals (mean cover 37.4%) and fleshy macroalgae (20.9%). Live coral cover was higher than in most other subtropical reefs and directly comparable to lower latitude tropical reefs. Juvenile coral densities (0.8 ind.m(-2)), however, were 5-200 times lower than those reported for tropical reefs. Overall, macroalgal cover was negatively related to the cover of live coral and the density of juvenile corals, but displayed no relationship with herbivorous fish biomass. The biomass of herbivorous fishes was relatively low (204 kg.ha(-1)), and in marked contrast to tropical reefs was dominated by macroalgal browsing species (84.1%) with relatively few grazing species. Despite their extremely low biomass, grazing fishes were positively related to both the density of juvenile corals and the cover of bare substrata, suggesting that they may enhance the recruitment of corals through the provision of suitable settlement sites. Although Lord Howe Islands' reefs are currently coral-dominated, the high macroalgal cover, coupled with limited coral recruitment and low coral growth rates suggest these reefs may be extremely susceptible to future disturbances.     

Scaling metabolism from individuals to reef‐fish communities at broad spatial scales

Fishes contribute substantially to energy and nutrient fluxes in reef ecosystems, but quantifying these roles is challenging. Here, we do so by synthesising a large compilation of fish metabolic‐rate data with a comprehensive database on reef‐fish community abundance and biomass. Individual‐level analyses support predictions of Metabolic Theory after accounting for significant family‐level variation, and indicate that some tropical reef fishes may already be experiencing thermal regimes at or near their temperature optima. Community‐level analyses indicate that total estimated respiratory fluxes of reef‐fish communities increase on average ~2‐fold from 22 to 28 °C. Comparisons of estimated fluxes among trophic groups highlight striking differences in resource use by communities in different regions, perhaps partly reflecting distinct evolutionary histories, and support the hypothesis that piscivores receive substantial energy subsidies from outside reefs. Our study demonstrates one approach to synthesising individual‐ and community‐level data to establish broad‐scale trends in contributions of biota to ecosystem dynamics.     

Spatial patterns of fish standing biomass across Brazilian reefs

A large fish‐count dataset from the Brazilian province was used to describe spatial patterns in standing biomass and test if total biomass, taxonomic and functional trophic structure vary across nested spatial scales. Taxonomic and functional structure varied more among localities and sites than among regions. Total biomass was generally higher at oceanic islands and remote or protected localities along the coast. Lower level carnivores comprised a large part of the biomass at almost all localities (mean of 44%), zooplanktivores never attained more than 14% and omnivores were more representative of subtropical reefs and oceanic islands (up to 66% of total biomass). Small and large herbivores and detritivores varied greatly in their contribution to total biomass, with no clear geographical patterns. Macrocarnivores comprised less than 12% of the biomass anywhere, except for two remote localities. Top predators, such as sharks and very large groupers, were rare and restricted to a few reefs, suggesting that their ecological function might have already been lost in many Brazilian reefs.     

Coral reef mesopredators switch prey,shortening food chains,in response to habitat degradation

Diet specificity is likely to be the key predictor of a predator's vulnerability to changing habitat and prey conditions. Understanding the degree to which predatory coral reef fishes adjust or maintain prey choice, in response to declines in coral cover and changes in prey availability, is critical for predicting how they may respond to reef habitat degradation. Here, we use stable isotope analyses to characterize the trophic structure of predator–prey interactions on coral reefs of the Keppel Island Group on the southern Great Barrier Reef, Australia. These reefs, previously typified by exceptionally high coral cover, have recently lost much of their coral cover due to coral bleaching and frequent inundation by sediment‐laden, freshwater flood plumes associated with increased rainfall patterns. Long‐term monitoring of these reefs demonstrates that, as coral cover declined, there has been a decrease in prey biomass, and a shift in dominant prey species from pelagic plankton‐feeding damselfishes to territorial benthic algal‐feeding damselfishes, resulting in differences in the principal carbon pathways in the food web. Using isotopes, we tested whether this changing prey availability could be detected in the diet of a mesopredator (coral grouper, Plectropomus maculatus). The δ¹³C signature in grouper tissue in the Keppel Islands shifted from a more pelagic to a more benthic signal, demonstrating a change in carbon sources aligning with the change in prey availability due to habitat degradation. Grouper with a more benthic carbon signature were also feeding at a lower trophic level, indicating a shortening in food chains. Further, we found a decline in the coral grouper population accompanying a decrease in total available prey biomass. Thus, while the ability to adapt diets could ameliorate the short‐term impacts of habitat degradation on mesopredators, long‐term effects may negatively impact mesopredator populations and alter the trophic structure of coral reef food webs.     

Life history trait divergence among populations of a non‐palatable species reveals strong non‐trophic indirect effects of an abundant herbivore

When large herbivores exert selection on their prey plant species, co‐occurring, non‐prey species may experience selection through non‐trophic indirect effects. Such selection is likely common where herbivores are overabundant. Yet, empirical studies of non‐trophic indirect effects as drivers of non‐prey trait evolution are lacking. Here we test for adaptive shifts in life history traits in an unpalatable species, Arisaema triphyllum, a common forest perennial that is unique because it exhibits size‐dependent sex switching. We collected A. triphyllum from six sites that experience a gradient in abiotic stress caused by deer browse pressure on prey plant species that generate indirect effects. We grew A. triphyllum from these sites in a common garden for five years to evaluate life history predictions linking strong indirect effects and abiotic stress to changes in life history traits: flowering onset size threshold, female flowering size threshold, relative growth rate (RGR), biomass allocation, and asexual reproduction. Despite observed differences among phenotypes in the field, expression of flowering onset size threshold, biomass allocation, and asexual reproduction did not differ among the six populations in the garden, indicating common plastic responses. In contrast, A. triphyllum collected from sites experiencing the two highest deer impacts exhibited smaller female flowering size thresholds and the highest RGR. Responses in these traits support the predictions of adaptive divergence in response to indirect effects. Our results reinforce the idea that non‐trophic indirect effects of large herbivores can elicit evolutionary responses in some traits of non‐prey species. In general, life history traits of unpalatable species may be cryptically adapting to stressful indirect effects where large herbivores are overabundant.     

Reef fish community structure of the Fernando de Noronha Archipelago (Equatorial Western Atlantic): the influence of exposure and benthic composition

We studied the reef fish assemblage of eight reefs within the oceanic archipelago of Fernando de Noronha, off northeastern Brazil. In a total of 91 belt transects (20 × 2 m) we recorded 60 species from 28 families. The 25 most abundant species accounted for about 98% of all fish recorded in this study and most of these species are widely distributed in the Western Atlantic. The majority of fish counted were planktivores (37.0%), followed by mobile invertebrate feeders (28.5%), territorial herbivores (11.3%), roving herbivores (10.5%), omnivores (7.1%), macrocarnivores (6.5%) and sessile invertebrate feeders (0.03%). In terms of biomass, roving herbivores were the most representative (41.8%), followed by mobile invertebrate feeders (19.9%), macrocarnivores (14.3%), omnivores (14.0%), piscivores (8.3%), planktivores (1.4%), territorial herbivores (0.3%), and sessile invertebrate feeders (0.03%). Overall, density and biomass of fishes were positively correlated with coral cover and depth, and negatively correlated with wave exposure. These relationships are probably a response to the habitat complexity provided by the higher coral cover in deeper reefs (>10 m) of the archipelago or to the lower water turbulence below 10 m deep. Carnivores and mobile invertebrate feeders were mainly influenced by depth and non-consolidated substratum, planktivores and omnivores by wave exposure and herbivores by algal cover. Although our results suggest that habitat characteristics may play a role in determining the distribution of some fish species, we also found several habitat generalists, suggesting that the community is dominated by versatile species.     

西沙群岛礁栖鱼类物种多样性及其食性特征

通过新的方法(即潜水调查法)调查了西沙群岛浅水区的礁栖鱼类, 并从食性角度分析鱼类群落特征及其对水质环境变化的响应。2006年5-6月, 对西沙群岛6个岛礁(东岛、永兴岛、羚羊礁、金银岛、华光礁和中建岛)共10个站位的礁栖鱼类种类、数量和长度进行了调查, 结合公开资料(FishBase等)确定鱼类食性。共记录到29科71属119种鱼, 其中50种是新记录。至此, 西沙群岛的鱼类总记录已达到717种。从不同站位来看, 永兴岛西的种类数量和Shannon-Wiener多样性指数均最高。多数鱼种分布范围狭小。摄食浮游动物和底栖无脊椎动物的鱼类是优势类群, 而草食性、杂食性和食物链顶端食性的鱼类数量和生物量较低, 反映出西沙群岛珊瑚礁生态系统整体上健康稳定。永兴岛的杂食性鱼类的数量比例和生物量比例均高于其他岛礁, 反映出鱼类群落已对水体富营养化产生响应。     

Does Herbivorous Fish Protection Really Improve Coral Reef Resilience? A Case Study from New Caledonia (South Pacific)

Parts of coral reefs from New Caledonia (South Pacific) were registered at the UNESCO World Heritage list in 2008. Management strategies aiming at preserving the exceptional ecological value of these reefs in the context of climate change are currently being considered. This study evaluates the appropriateness of an exclusive fishing ban of herbivorous fish as a strategy to enhance coral reef resilience to hurricanes and bleaching in the UNESCO-registered areas of New Caledonia. A two-phase approach was developed: 1) coral, macroalgal, and herbivorous fish communities were examined in four biotopes from 14 reefs submitted to different fishing pressures in New Caledonia, and 2) results from these analyses were challenged in the context of a global synthesis of the relationship between herbivorous fish protection, coral recovery and relative macroalgal development after hurricanes and bleaching. Analyses of New Caledonia data indicated that 1) current fishing pressure only slightly affected herbivorous fish communities in the country, and 2) coral and macroalgal covers remained unrelated, and macroalgal cover was not related to the biomass, density or diversity of macroalgae feeders, whatever the biotope or level of fishing pressure considered. At a global scale, we found no relationship between reef protection status, coral recovery and relative macroalgal development after major climatic events. These results suggest that an exclusive protection of herbivorous fish in New Caledonia is unlikely to improve coral reef resilience to large-scale climatic disturbances, especially in the lightly fished UNESCO-registered areas. More efforts towards the survey and regulation of major chronic stress factors such as mining are rather recommended. In the most heavily fished areas of the country, carnivorous fish and large targeted herbivores may however be monitored as part of a precautionary approach.     

Human activities as a driver of spatial variation in the trophic structure of fish communities on Pacific coral reefs

Anthropogenic activities such as land‐use change, pollution and fishing impact the trophic structure of coral reef fishes, which can influence ecosystem health and function. Although these impacts may be ubiquitous, they are not consistent across the tropical Pacific Ocean. Using an extensive database of fish biomass sampled using underwater visual transects on coral reefs, we modelled the impact of human activities on food webs at Pacific‐wide and regional (1,000s–10,000s km) scales. We found significantly lower biomass of sharks and carnivores, where there were higher densities of human populations (hereafter referred to as human activity); however, these patterns were not spatially consistent as there were significant differences in the trophic structures of fishes among biogeographic regions. Additionally, we found significant changes in the benthic structure of reef environments, notably a decline in coral cover where there was more human activity. Direct human impacts were the strongest in the upper part of the food web, where we found that in a majority of the Pacific, the biomass of reef sharks and carnivores were significantly and negatively associated with human activity. Finally, although human‐induced stressors varied in strength and significance throughout the coral reef food web across the Pacific, socioeconomic variables explained more variation in reef fish trophic structure than habitat variables in a majority of the biogeographic regions. Notably, economic development (measured as GDP per capita) did not guarantee healthy reef ecosystems (high coral cover and greater fish biomass). Our results indicate that human activities are significantly shaping patterns of trophic structure of reef fishes in a spatially nonuniform manner across the Pacific Ocean, by altering processes that organize communities in both “top‐down” (fishing of predators) and “bottom‐up” (degradation of benthic communities) contexts.     

Tropical herbivores provide resilience to a climate‐mediated phase shift on temperate reefs

Climate‐mediated changes to biotic interactions have the potential to fundamentally alter global ecosystems. However, the capacity for novel interactions to drive or maintain transitions in ecosystem states remains unresolved. We examined temperate reefs that recently underwent complete seaweed canopy loss and tested whether a concurrent increase in tropical herbivores could be maintaining the current canopy‐free state. Turf‐grazing herbivorous fishes increased in biomass and diversity, and displayed feeding rates comparable to global coral reefs. Canopy‐browsing herbivores displayed high (~ 10 000 g 100 m^?2) and stable biomass between 2006 and 2013. Tropical browsers had the highest abundance in 2013 and displayed feeding rates approximately three times higher than previously observed on coral reefs. These observations suggest that tropical herbivores are maintaining previously kelp‐dominated temperate reefs in an alternate canopy‐free state by grazing turfs and preventing kelp reestablishment. This remarkable ecosystem highlights the sensitivity of biotic interactions and ecosystem stability to warming and extreme disturbance events.     

Geographic variation in reef-fish assemblages along the Brazilian coast

The species composition of reef‐fish assemblages from nine Brazilian major coastal sites and four oceanic islands are compared. Canonical correspondence analysis (CCA) was utilized to identify groups of sites based on similarity of composition, and to correlate environmental trends with such groups. Five distinct groups of sites were recognized: (1) the South and South‐eastern coastal reefs (from Guarapari Islands to Santa Catarina, the southernmost Brazilian reefs); (2) the North‐eastern coast (extending from the Manuel Luis Reefs to Abrolhos Archipelago); (3) Trindade Island; (4) Fernando de Noronha and Atol das Rocas; and (5) St Paul’s Rocks. Water temperature, coral richness, distance from mainland, primary production and shelf width strongly correlated with the diversity and composition of the reef sites.     

The influence of multiple factors upon reef fish abundance and species richness in a tropical coral complex

The present study was conducted on Tamandaré reefs, northeast Brazil and aimed to analyse the importance of different factors (e.g. tourism activity, fishing activity, coral abundance and algal abundance) on reef fish abundance and species richness. Two distinct reef areas (A ver o mar and Caieiras) with different levels of influence were studied. A total of 8239 reef fish individuals were registered, including 59 species. Site 1 (A ver o mar) presented higher reef fish abundance and richness, with dominance of roving herbivores (29.9 %) and mobile invertebrate feeders (28.7 %). In contrast, at Site 2 (Caieiras) territorial herbivores (40.9 %) predominated, followed by mobile invertebrate feeders (24.6 %). Concerning the benthic community, at Site 1 macroalgae were recorded as the main category (49.3 %); however, Site 2 was dominated by calcareous algae (36.0 %). The most important variable explaining more than 90 % of variance on reef fish abundance and species richness was macroalgae abundance, followed by fishing activity. Phase shifts on coral reefs are evident, resulting in the replacement of coral by macroalgae and greatly influencing reef fish communities. In this context, it is important to understand the burden of the factors that affect reef fish communities and, therefore, influence the extinction vulnerability of coral reef fishes.