Shelters and their use by fishes on fringing coral reefs

Coral reef fish density and species richness are often higher at sites with more structural complexity. This association may be due to greater availability of shelters, but surprisingly little is known about the size and density of shelters and their use by coral reef fishes. We quantified shelter availability and use by fishes for the first time on a Caribbean coral reef by counting all holes and overhangs with a minimum entrance diameter ≥3 cm in 30 quadrats (25 m(2)) on two fringing reefs in Barbados. Shelter size was highly variable, ranging from 42 cm(3) to over 4,000,000 cm(3), with many more small than large shelters. On average, there were 3.8 shelters m(-2), with a median volume of 1,200 cm(3) and a total volume of 52,000 cm(3) m(-2). The number of fish per occupied shelter ranged from 1 to 35 individual fishes belonging to 66 species, with a median of 1. The proportion of shelters occupied and the number of occupants increased strongly with shelter size. Shelter density and total volume increased with substrate complexity, and this relationship varied among reef zones. The density of shelter-using fish was much more strongly predicted by shelter density and median size than by substrate complexity and increased linearly with shelter density, indicating that shelter availability is a limiting resource for some coral reef fishes. The results demonstrate the importance of large shelters for fish density and support the hypothesis that structural complexity is associated with fish abundance, at least in part, due to its association with shelter availability. This information can help identify critical habitat for coral reef fishes, predict the effects of reductions in structural complexity of natural reefs and improve the design of artificial reefs.     

The non-linear relationship between body size and function in parrotfishes

Parrotfishes are a group of herbivores that play an important functional role in structuring benthic communities on coral reefs. Increasingly, these fish are being targeted by fishermen, and resultant declines in biomass and abundance may have severe consequences for the dynamics and regeneration of coral reefs. However, the impact of overfishing extends beyond declining fish stocks. It can also lead to demographic changes within species populations where mean body size is reduced. The effect of reduced mean body size on population dynamics is well described in literature but virtually no information exists on how this may influence important ecological functions. The study investigated how one important function, scraping (i.e., the capacity to remove algae and open up bare substratum for coral larval settlement), by three common species of parrotfishes (Scarus niger, Chlorurus sordidus, and Chlorurus strongylocephalus) on coral reefs at Zanzibar (Tanzania) was influenced by the size of individual fishes. There was a non-linear relationship between body size and scraping function for all species examined, and impact through scraping was also found to increase markedly when fish reached a size of 15–20 cm. Thus, coral reefs which have a high abundance and biomass of parrotfish may nonetheless be functionally impaired if dominated by small-sized individuals. Reductions in mean body size within parrotfish populations could, therefore, have functional impacts on coral reefs that previously have been overlooked.     

Importance of live coral habitat for reef fishes

Live corals are the key habitat forming organisms on coral reefs, contributing to both biological and physical structure. Understanding the importance of corals for reef fishes is, however, restricted to a few key families of fishes, whereas it is likely that a vast number of fish species will be adversely affected by the loss of live corals. This study used data from published literature together with independent field based surveys to quantify the range of reef fish species that use live coral habitats. A total of 320 species from 39 families use live coral habitats, accounting for approximately 8 % of all reef fishes. Many of the fishes reported to use live corals are from the families Pomacentridae (68 spp.) and Gobiidae (44 spp.) and most (66 %) are either planktivores or omnivores. 126 species of fish associate with corals as juveniles, although many of these fishes have no apparent affiliation with coral as adults, suggesting an ontogenetic shift in coral reliance. Collectively, reef fishes have been reported to use at least 93 species of coral, mainly from the genus Acropora and Porities and associate predominantly with branching growth forms. Some fish associate with a single coral species, whilst others can be found on more than 20 different species of coral indicating there is considerable variation in habitat specialisation among coral associated fish species. The large number of fishes that rely on coral highlights that habitat degradation and coral loss will have significant consequences for biodiversity and productivity of reef fish assemblages.     

The role of turtles as coral reef macroherbivores

Herbivory is widely accepted as a vital function on coral reefs. To date, the majority of studies examining herbivory in coral reef environments have focused on the roles of fishes and/or urchins, with relatively few studies considering the potential role of macroherbivores in reef processes. Here, we introduce evidence that highlights the potential role of marine turtles as herbivores on coral reefs. While conducting experimental habitat manipulations to assess the roles of herbivorous reef fishes we observed green turtles (Chelonia mydas) and hawksbill turtles (Eretmochelys imbricata) showing responses that were remarkably similar to those of herbivorous fishes. Reducing the sediment load of the epilithic algal matrix on a coral reef resulted in a forty-fold increase in grazing by green turtles. Hawksbill turtles were also observed to browse transplanted thalli of the macroalga Sargassum swartzii in a coral reef environment. These responses not only show strong parallels to herbivorous reef fishes, but also highlight that marine turtles actively, and intentionally, remove algae from coral reefs. When considering the size and potential historical abundance of marine turtles we suggest that these potentially valuable herbivores may have been lost from many coral reefs before their true importance was understood.     

Interactions between coral restoration and fish assemblages: implications for reef management

Corals create complex reef structures that provide both habitat and food for many fish species. Because of numerous natural and anthropogenic threats, many coral reefs are currently being degraded, endangering the fish assemblages they support. Coral reef restoration, an active ecological management tool, may help reverse some of the current trends in reef degradation through the transplantation of stony corals. Although restoration techniques have been extensively reviewed in relation to coral survival, our understanding of the effects of adding live coral cover and complexity on fishes is in its infancy with a lack of scientifically validated research. This study reviews the limited data on reef restoration and fish assemblages, and complements this with the more extensive understanding of complex interactions between natural reefs and fishes and how this might inform restoration efforts. It also discusses which key fish species or functional groups may promote, facilitate or inhibit restoration efforts and, in turn, how restoration efforts can be optimised to enhance coral fish assemblages. By highlighting critical knowledge gaps in relation to fishes and restoration interactions, the study aims to stimulate research into the role of reef fishes in restoration projects. A greater understanding of the functional roles of reef fishes would also help inform whether restoration projects can return fish assemblages to their natural compositions or whether alternative species compositions develop, and over what timeframe. Although alleviation of local and global reef stressors remains a priority, reef restoration is an important tool; an increased understanding of the interactions between replanted corals and the fishes they support is critical for ensuring its success for people and nature.     

Speciation in coral-reef fishes

Covering <0·1% of the ocean’s surface, coral reefs harbour about one‐third of all marine fishes or c. 5000 species. Allopatry (geographic isolation) is believed to be the primary mode of speciation, yet few biogeographic barriers exist between reefs, and most reef fishes have a pelagic larval stage capable of extensive dispersal. Under these circumstances, why are there so many species of reef fishes? Since most biogeographic barriers in the oceans are either spatially or temporally permeable on a relatively short time frame, the requirement of isolation during allopatric speciation is hard to satisfy. Evidence from empirical and theoretical studies, the biological characteristics of coral reefs, and a reanalysis of biogeographic barriers indicate that sympatric speciation is possible but not common at small spatial scales and that parapatric speciation is a common (and probably the prevalent) mode of diversification in coral‐reef fishes. Regardless of the speciation mode, previous hypotheses of accelerated diversification in the Pleistocene due to sea level fluctuations are not supported by phylogenetic analyses. Recent developments in the area of comparative genomics can fuel a new revolution in the way marine speciation is studied.     

Habitat associations of juvenile fish at Ningaloo Reef, Western Australia: the importance of coral and algae

Habitat specificity plays a pivotal role in forming community patterns in coral reef fishes, yet considerable uncertainty remains as to the extent of this selectivity, particularly among newly settled recruits. Here we quantified habitat specificity of juvenile coral reef fish at three ecological levels; algal meadows vs. coral reefs, live vs. dead coral and among different coral morphologies. In total, 6979 individuals from 11 families and 56 species were censused along Ningaloo Reef, Western Australia. Juvenile fishes exhibited divergence in habitat use and specialization among species and at all study scales. Despite the close proximity of coral reef and algal meadows (10's of metres) 25 species were unique to coral reef habitats, and seven to algal meadows. Of the seven unique to algal meadows, several species are known to occupy coral reef habitat as adults, suggesting possible ontogenetic shifts in habitat use. Selectivity between live and dead coral was found to be species-specific. In particular, juvenile scarids were found predominantly on the skeletons of dead coral whereas many damsel and butterfly fishes were closely associated with live coral habitat. Among the coral dependent species, coral morphology played a key role in juvenile distribution. Corymbose corals supported a disproportionate number of coral species and individuals relative to their availability, whereas less complex shapes (i.e. massive & encrusting) were rarely used by juvenile fish. Habitat specialisation by juvenile species of ecological and fisheries importance, for a variety of habitat types, argues strongly for the careful conservation and management of multiple habitat types within marine parks, and indicates that the current emphasis on planning conservation using representative habitat areas is warranted. Furthermore, the close association of many juvenile fish with corals susceptible to climate change related disturbances suggests that identifying and protecting reefs resilient to this should be a conservation priority.     

Caribbean reefs of the Anthropocene: Variance in ecosystem metrics indicates bright spots on coral depauperate reefs

Dramatic coral loss has significantly altered many Caribbean reefs, with potentially important consequences for the ecological functions and ecosystem services provided by reef systems. Many studies examine coral loss and its causes—and often presume a universal decline of ecosystem services with coral loss—rather than evaluating the range of possible outcomes for a diversity of ecosystem functions and services at reefs varying in coral cover. We evaluate 10 key ecosystem metrics, relating to a variety of different reef ecosystem functions and services, on 328 Caribbean reefs varying in coral cover. We focus on the range and variability of these metrics rather than on mean responses. In contrast to a prevailing paradigm, we document high variability for a variety of metrics, and for many the range of outcomes is not related to coral cover. We find numerous “bright spots,” where herbivorous fish biomass, density of large fishes, fishery value, and/or fish species richness are high, despite low coral cover. Although it remains critical to protect and restore corals, understanding variability in ecosystem metrics among low‐coral reefs can facilitate the maintenance of reefs with sustained functions and services as we work to restore degraded systems. This framework can be applied to other ecosystems in the Anthropocene to better understand variance in ecosystem service outcomes and identify where and why bright spots exist.     

Size-structural shifts reveal intensity of exploitation in coral reef fisheries

Fisheries exploitation represents a considerable threat to coral reef fish resources because even modest levels of extraction can alter ecological dynamics via shifts of stock size, species composition, and size-structure of the fish assemblage. Although species occupying higher trophic groups are known to suffer the majority of exploitative effects, changes in composition among lower trophic groups may be major, though are not frequently explored. Using size-based biomass spectrum analysis, we investigate the effects of fishing on the size-structure of coral reef fish assemblages spanning four geopolitical regions and determine if patterns of exploitation vary across trophic groups. Our analyses reveal striking evidence for the variety of effects fisheries exploitation can have on coral reef fish assemblages. When examining biomass spectra across the entire fish assemblage we found consistent evidence of size-specific exploitation, in which large-bodied individuals experience disproportionate reductions. The pattern was paralleled by and likely driven by, strongly size-specific reductions among top predators. In contrast, evidence of exploitation patterns was variable among lower trophic groups, in many cases including evidence of reductions across all size classes. The breadth of size classes and trophic groups that showed evidence of exploitation related positively to local human population density and diversity of fishing methods employed. Our findings highlight the complexity of coral reef fisheries and that the effects of exploitation on coral reefs can be realized throughout the entire fish assemblage, across multiple trophic groups and not solely restricted to large-bodied top-predators. Size-specific changes among fishes of lower trophic groups likely lead to altered ecological functioning of heavily exploited coral reefs. Together these findings reinforce the value of taking a multi-trophic group approach to monitoring and managing coral reef fisheries.     

Maintenance of fish diversity on disturbed coral reefs

Habitat perturbations play a major role in shaping community structure; however, the elements of disturbance-related habitat change that affect diversity are not always apparent. This study examined the effects of habitat disturbances on species richness of coral reef fish assemblages using annual surveys of habitat and 210 fish species from 10 reefs on the Great Barrier Reef (GBR). Over a period of 11 years, major disturbances, including localised outbreaks of crown-of-thorns sea star (Acanthaster planci), severe storms or coral bleaching, resulted in coral decline of 46–96% in all the 10 reefs. Despite declines in coral cover, structural complexity of the reef framework was retained on five and species richness of coral reef fishes maintained on nine of the disturbed reefs. Extensive loss of coral resulted in localised declines of highly specialised coral-dependent species, but this loss of diversity was more than compensated for by increases in the number of species that feed on the epilithic algal matrix (EAM). A unimodal relationship between areal coral cover and species richness indicated species richness was greatest at approximately 20% coral cover declining by 3–4 species (6–8% of average richness) at higher and lower coral cover. Results revealed that declines in coral cover on reefs may have limited short-term impact on the diversity of coral reef fishes, though there may be fundamental changes in the community structure of fishes.     

Predators reduce abundance and species richness of coral reef fish recruits via non-selective predation

Predators have important effects on coral reef fish populations, but their effects on community structure have only recently been investigated and are not yet well understood. Here, the effect of predation on the diversity and abundance of young coral reef fishes was experimentally examined in Moorea, French Polynesia. Effects of predators were quantified by monitoring recruitment of fishes onto standardized patch reefs in predator-exclosure cages or uncaged reefs. At the end of the 54-day experiment, recruits were 74% less abundant on reefs exposed to predators than on caged ones, and species richness was 42% lower on reefs exposed to predators. Effects of predators varied somewhat among families, however, rarefaction analysis indicated that predators foraged non-selectively among species. These results indicate that predation can alter diversity of reef fish communities by indiscriminately reducing the abundance of fishes soon after settlement, thereby reducing the number of species present on reefs.     

Reef Fishes in Biodiversity Hotspots Are at Greatest Risk from Loss of Coral Species

Coral reef ecosystems are under a variety of threats from global change and anthropogenic disturbances that are reducing the number and type of coral species on reefs. Coral reefs support upwards of one third of all marine species of fish, so the loss of coral habitat may have substantial consequences to local fish diversity. We posit that the effects of habitat degradation will be most severe in coral regions with highest biodiversity of fishes due to greater specialization by fishes for particular coral habitats. Our novel approach to this important but untested hypothesis was to conduct the same field experiment at three geographic locations across the Indo-Pacific biodiversity gradient (Papua New Guinea; Great Barrier Reef, Australia; French Polynesia). Specifically, we experimentally explored whether the response of local fish communities to identical changes in diversity of habitat-providing corals was independent of the size of the regional species pool of fishes. We found that the proportional reduction (sensitivity) in fish biodiversity to loss of coral diversity was greater for regions with larger background species pools, reflecting variation in the degree of habitat specialization of fishes across the Indo-Pacific diversity gradient. This result implies that habitat-associated fish in diversity hotspots are at greater risk of local extinction to a given loss of habitat diversity compared to regions with lower species richness. This mechanism, related to the positive relationship between habitat specialization and regional biodiversity, and the elevated extinction risk this poses for biodiversity hotspots, may apply to species in other types of ecosystems.     

Predation Risk,Resource Quality,and Reef Structural Complexity Shape Territoriality in a Coral Reef Herbivore

For many species securing territories is important for feeding and reproduction. Factors such as competition, habitat availability, and male characteristics can influence an individual’s ability to establish and maintain a territory. The risk of predation can have an important influence on feeding and reproduction; however, few have studied its effect on territoriality. We investigated territoriality in a haremic, polygynous species of coral reef herbivore, Sparisoma aurofrenatum (redband parrotfish), across eight reefs in the Florida Keys National Marine Sanctuary that were either protected or unprotected from fishing of piscivorous fishes. We examined how territory size and quality varied with reef protection status, competition, predation risk, and male size. We then determined how territory size and quality influenced harem size and female size to understand the effect of territoriality on reproductive potential. We found that protected reefs trended towards having more large predatory fishes and that territories there were smaller but had greater algal nutritional quality relative to unprotected reefs. Our data suggest that even though males in protected sites have smaller territories, which support fewer females, they may improve their reproductive potential by choosing nutritionally rich areas, which support larger females. Thus, reef protection appears to shape the trade-off that herbivorous fishes make between territory size and quality. Furthermore, we provide evidence that males in unprotected sites, which are generally less complex than protected sites, choose territories with higher structural complexity, suggesting the importance of this type of habitat for feeding and reproduction in S. aurofrenatum. Our work argues that the loss of corals and the resulting decline in structural complexity, as well as management efforts to protect reefs, could alter the territory dynamics and reproductive potential of important herbivorous fish species.     

Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae)

Habitat shifts are implicated as the cause of many vertebrate radiations, yet relatively few empirical studies quantify patterns of diversification following colonization of new habitats in fishes. The pufferfishes (family Tetraodon‐tidae) occur in several habitats, including coral reefs and freshwater, which are thought to provide ecological opportunity for adaptive radiation, and thus provide a unique system for testing the hypothesis that shifts to new habitats alter diversification rates. To test this hypothesis, we sequenced eight genes for 96 species of pufferfishes and closely related porcupine fishes, and added 19 species from sequences available in GenBank. We time‐calibrated the molecular phylogeny using three fossils, and performed several comparative analyses to test whether colonization of novel habitats led to shifts in the rate of speciation and body size evolution, central predictions of clades experiencing ecological adaptive radiation. Colonization of freshwater is associated with lower rates of cladogenesis in pufferfishes, although these lineages also exhibit accelerated rates of body size evolution. Increased rates of cladogenesis are associated with transitions to coral reefs, but reef lineages surprisingly exhibit significantly lower rates of body size evolution. These results suggest that ecological opportunity afforded by novel habitats may be limited for pufferfishes due to competition with other species, constraints relating to pufferfish life history and trophic ecology, and other factors.     

Cross-shelf variation in the role of parrotfishes on the Great Barrier Reef

Herbivorous fishes are a key functional group on coral reefs. These fishes are central to the capacity of reefs to resist phase shifts and regenerate after disturbance. Despite this importance few studies have quantified the direct impact of these fishes on coral reefs. In this study the roles of parrotfishes, a ubiquitous group of herbivorous fishes, were examined on reefs in the northern Great Barrier Reef. The distribution of 24 species of parrotfish was quantified on three reefs in each of three cross-shelf regions. Functional roles (grazing, erosion, coral predation and sediment reworking) were calculated as the product of fish density, bite area or volume, bite rate, and the proportion of bites taken from various substrata. Inner-shelf reefs supported high densities but low biomass of parrotfishes, with high rates of grazing and sediment reworking. In contrast, outer-shelf reefs were characterised by low densities and high biomass of parrotfish, with high rates of erosion and coral predation. Mid-shelf reefs displayed moderate levels of all roles examined. The majority of this variation in functional roles was attributable to just two species. Despite being rare, Bolbometopon muricatum, the largest parrotfish species, accounted for 87.5% of the erosion and 99.5% of the coral predation on outer-shelf reefs. B. muricatum displayed little evidence of selectivity of feeding, with most substrata being consumed in proportion to their availability. In contrast, the high density of Scarus rivulatus accounted for over 70% of the total grazing and sediment reworking on inner-shelf reefs. This marked variation in the roles of parrotfishes across the continental shelf suggests that each shelf system is shaped by fundamentally different processes. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Marine Reserves Enhance the Recovery of Corals on Caribbean Reefs

The fisheries and biodiversity benefits of marine reserves are widely recognised but there is mounting interest in exploiting the importance of herbivorous fishes as a tool to help ecosystems recover from climate change impacts. This approach might be particularly suitable for coral reefs, which are acutely threatened by climate change, yet the trophic cascades generated by reserves are strong enough that they might theoretically enhance the rate of coral recovery after disturbance. However, evidence for reserves facilitating coral recovery has been lacking. Here we investigate whether reductions in macroalgal cover, caused by recovery of herbivorous parrotfishes within a reserve, have resulted in a faster rate of coral recovery than in areas subject to fishing. Surveys of ten sites inside and outside a Bahamian marine reserve over a 2.5-year period demonstrated that increases in coral cover, including adjustments for the initial size-distribution of corals, were significantly higher at reserve sites than those in non-reserve sites. Furthermore, macroalgal cover was significantly negatively correlated with the change in total coral cover over time. Recovery rates of individual species were generally consistent with small-scale manipulations on coral-macroalgal interactions, but also revealed differences that demonstrate the difficulties of translating experiments across spatial scales. Size-frequency data indicated that species which were particularly affected by high abundances of macroalgae outside the reserve had a population bottleneck restricting the supply of smaller corals to larger size classes. Importantly, because coral cover increased from a heavily degraded state, and recovery from such states has not previously been described, similar or better outcomes should be expected for many reefs in the region. Reducing herbivore exploitation as part of an ecosystem-based management strategy for coral reefs appears to be justified.     

Coral reefs promote the evolution of morphological diversity and ecological novelty in labrid fishes

Although coral reefs are renowned biodiversity hotspots it is not known whether they also promote the evolution of exceptional ecomorphological diversity. We investigated this question by analysing a large functional morphological dataset of trophic characters within Labridae, a highly diverse group of fishes. Using an analysis that accounts for species relationships, the time available for diversification and model uncertainty we show that coral reef species have evolved functional morphological diversity twice as fast as non-reef species. In addition, coral reef species occupy 68.6% more trophic morphospace than non-reef species. Our results suggest that coral reef habitats promote the evolution of both trophic novelty and morphological diversity within fishes. Thus, the preservation of coral reefs is necessary, not only to safeguard current biological diversity but also to conserve the underlying mechanisms that can produce functional diversity in future.     

The influence of coral reef benthic condition on associated fish assemblages

Accumulative disturbances can erode a coral reef's resilience, often leading to replacement of scleractinian corals by macroalgae or other non-coral organisms. These degraded reef systems have been mostly described based on changes in the composition of the reef benthos, and there is little understanding of how such changes are influenced by, and in turn influence, other components of the reef ecosystem. This study investigated the spatial variation in benthic communities on fringing reefs around the inner Seychelles islands. Specifically, relationships between benthic composition and the underlying substrata, as well as the associated fish assemblages were assessed. High variability in benthic composition was found among reefs, with a gradient from high coral cover (up to 58%) and high structural complexity to high macroalgae cover (up to 95%) and low structural complexity at the extremes. This gradient was associated with declining species richness of fishes, reduced diversity of fish functional groups, and lower abundance of corallivorous fishes. There were no reciprocal increases in herbivorous fish abundances, and relationships with other fish functional groups and total fish abundance were weak. Reefs grouping at the extremes of complex coral habitats or low-complexity macroalgal habitats displayed markedly different fish communities, with only two species of benthic invertebrate feeding fishes in greater abundance in the macroalgal habitat. These results have negative implications for the continuation of many coral reef ecosystem processes and services if more reefs shift to extreme degraded conditions dominated by macroalgae.     

Climate-driven coral reorganisation influences aggressive behaviour in juvenile coral-reef fishes

Globally, habitat degradation is altering the abundance and diversity of species in a variety of ecosystems. This study aimed to determine how habitat degradation, in terms of changing coral composition under climate change, affected abundance, species richness and aggressive behaviour of juveniles of three damselfishes (Pomacentrus moluccensis, P. amboinensis and Dischistodus perspicillatus, in order of decreasing reliance on coral). Patch reefs were constructed to simulate two types of reefs: present-day reefs that are vulnerable to climate-induced coral bleaching, and reefs with more bleaching-robust coral taxa, thereby simulating the likely future of coral reefs under a warming climate. Fish communities were allowed to establish naturally on the reefs during the summer recruitment period. Climate-robust reefs had lower total species richness of coral-reef fishes than climate-vulnerable reefs, but total fish abundance was not significantly different between reef types (pooled across all species and life-history stages). The nature of aggressive interactions, measured as the number of aggressive chases, varied according to coral composition; on climate-robust reefs, juveniles used the substratum less often to avoid aggression from competitors, and interspecific aggression became relatively more frequent than intraspecific aggression for juveniles of the coral-obligate P. moluccensis. This study highlights the importance of coral composition as a determinant of behaviour and diversity of coral-reef fishes.