Cleaner fish drives local fish diversity on coral reefs

Coral reefs are one of the most diverse habitats in the world, yet our understanding of the processes affecting their biodiversity is limited. At the local scale, cleaner fish are thought to have a disproportionate effect, in relation to their abundance and size, on the activity of many other fish species, but confirmation of this species' effect on local fish diversity has proved elusive. The cleaner fish Labroides dimidiatus has major effects on fish activity patterns and may indirectly affect fish demography through the removal of large numbers of parasites. Here we show that small reefs where L. dimidiatus had been experimentally excluded for 18 months had half the species diversity of fish and one-fourth the abundance of individuals. Only fish that move among reefs, however, were affected. These fish include large species that themselves can affect other reef organisms. In contrast, the distribution of resident fish was not affected by cleaner fish. Thus, many fish appear to choose reefs based on the presence of cleaner fish. Our findings indicate that a single small and not very abundant fish has a strong influence on the movement patterns, habitat choice, activity, and local diversity and abundance of a wide variety of reef fish species.     

Configuration of small patch reefs and population abundance of a resident reef fish in a complex coral reef landscape

Habitat use by the resident coral reef anemonefish, Amphiprion frenatus, was examined in the complex coral reef landscape of Shiraho Reef, Ishigaki Island, Okinawa, Japan, using an enlarged color aerial photograph processed using image analysis software as an accurate field map. The anemonefish inhabit assemblages of the host sea anemone, Entacmaea quadricolor (clonal type), which inhabit various patch reefs in the back reef moat. We located all patch reefs inhabited by the host in the map based on snorkel observations: 297 anemonefish were found in 93 host assemblages in the study site of 2.9 ha. These patch reefs could be recognized by the reef colors, including the shadows (blackish color) in the photograph. Using image analysis software, the colors of the patch reefs were chosen and pixels with the same color values were regarded as potential habitat patches for the fish (PHPs). PHPs were 3D patch reefs (>0.5 m in height). Total areas (TA) and total perimeters (TP) of PHPs were measured in nine quadrats in the digitized aerial photograph. Host abundance and anemonefish abundance in a quadrat showed stronger correlations with the product of TA and TP of PHPs than TA alone. A site with numerous large 3D patch reefs (≥0.75 m² in situ) can be a better habitat for the fish than other sites consisting of several huge 3D patch reefs of the same total area. The methodology applied here may be useful for assessing the quality of habitats for small resident animals in shallow subtidal reefs.     

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.     

Recruitment and the structure of assemblages of fish on coral reefs

Much recent research has focused on the question of the high species richness and population densities of fish inhabiting coral reefs. Both density-dependent (post-recruitment) and density-independent (pre-recruitment) processes have been implicated in the regulation of these assemblages. These processes may operate at a variety of spatial and temporal scales. Here we review recent progress and point to some of the key questions for future research.     

Ecological structure of assemblages of coral reef fishes on isolated patch reefs

A 9-year study of the structure of assemblages of fish on 20 coral patch reefs, based on 20 non-manipulative censuses, revealed a total of 141 species from 34 families, although 40 species accounted for over 95% of sightings of fish. The average patch reef was 8.5 m² in surface area, and supported 125 fish of 20 species at a census. All reefs showed at least a two-fold variation among censuses in total numbers of fish present, and 12 showed ten-fold variations. There was also substantial variation in the composition and relative abundances of species present on each patch reef, such that censuses of a single patch reef were on average about 50% different from each other in percent similarity of species composition (Czekanowski's index). Species differed substantially in the degree to which their numbers varied from census to census, and in the degree to which their dispersion among patch reefs was modified from census to census. We characterize the 40 most common species with respect to these attributes. The variations in assemblage structure cannot be attributed to responses of fish to a changing physical structure of patch reefs, nor to the comings and goings of numerous rare species. Our results support and extend earlier reports on this study, which have stressed the lack of persistant structure for assemblages on these patch reefs. While reef fishes clearly have microhabitat preferences which are expressed at settlement, the variations in microhabitat offered by the patch reefs are insufficient to segregate many species of fish by patch reef. Instead, at the scale of single patch reefs, and, to a degree, at the larger scale of the 20 patch reefs, most of the 141 species of fish are distributed without regard to differences in habitat structure among reefs, and patterns of distribution change over time. Implications for general understanding of assemblage dynamics for fish over more extensive patches of reef habitat are considered.     

Relationships between structural complexity,coral traits,and reef fish assemblages

With the ongoing loss of coral cover and the associated flattening of reef architecture, understanding the links between coral habitat and reef fishes is of critical importance. Here, we investigate whether considering coral traits and functional diversity provides new insights into the relationship between structural complexity and reef fish communities, and whether coral traits and community composition can predict structural complexity. Across 157 sites in Seychelles, Maldives, the Chagos Archipelago, and Australia’s Great Barrier Reef, we find that structural complexity and reef zone are the strongest and most consistent predictors of reef fish abundance, biomass, species richness, and trophic structure. However, coral traits, diversity, and life histories provided additional predictive power for models of reef fish assemblages, and were key drivers of structural complexity. Our findings highlight that reef complexity relies on living corals—with different traits and life histories—continuing to build carbonate skeletons, and that these nuanced relationships between coral assemblages and habitat complexity can affect the structure of reef fish assemblages. Seascape-level estimates of structural complexity are rapid and cost effective with important implications for the structure and function of fish assemblages, and should be incorporated into monitoring programs.     

Wave energy and swimming performance shape coral reef fish assemblages

Physical factors often have an overriding influence on the distribution patterns of organisms, and can ultimately shape the long-term structure of communities. Although distribution patterns in sessile marine organisms have frequently been attributed to functional characteristics interacting with wave-induced water motion, similar evidence for mobile organisms is lacking. Links between fin morphology and swimming performance were examined in three diverse coral reef fish families from two major evolutionary lineages. Among-habitat variation in morphology and performance was directly compared with quantitative values of wave-induced water motion from seven coral reef habitats of different depth and wave exposure on the Great Barrier Reef. Fin morphology was strongly correlated with both field and experimental swimming speeds in all three families. The range of observed swimming speeds coincided closely with the magnitude of water velocities commonly found on coral reefs. Distribution patterns in all three families displayed highly congruent relationships between fin morphology and wave-induced water motion. Our findings indicate a general functional relationship between fin morphology and swimming performance in labriform-swimming fishes, and provide quantitative evidence that wave energy may directly influence the assemblage structure of coral reef fishes through interactions with morphology and swimming performance.     

Species-specific habitat distribution of coral reef fish assemblages in relation to habitat characteristics in an Okinawan coral reef

We determined the species-specific habitat associations of coral reef fishes and environmental characteristics in an Okinawan coral reef in Japan. We focused on three families (Pomacentridae, Gobiidae and Labridae) and attempted to determine differences in habitat utilization. We selected six sites along the coast of Amitori Bay, from the entrance to the innermost part, in order to cover a wide range of habitat characteristics (exposed habitat, semi-exposed habitat and sheltered habitat). The species diversity of coral assemblages was greater at the exposed and semi-exposed habitats, whereas branching coral mostly covered the sheltered habitat. The environmental factors that determine the species-specific spatial association in fishes differed among families. Both biological characteristics (coral morphology and coral species diversity) and physical characteristics (water depth and wave exposure) affected the spatial association of pomacentrids and gobiids. In contrast, physical characteristics such as substrate complexity and water depth affected the species-specific spatial association of labrid species. Further study is needed to determine the ecological factors that regulate the species-specific habitat preference in Okinawan coral reefs.     

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.     

Coral bleaching, reef fish community phase shifts and the resilience of coral reefs

The 1998 global coral bleaching event was the largest recorded historical disturbance of coral reefs and resulted in extensive habitat loss. Annual censuses of reef fish community structure over a 12-year period spanning the bleaching event revealed a marked phase shift from a prebleach to postbleach assemblage. Surprisingly, we found that the bleaching event had no detectable effect on the abundance, diversity or species richness of a local cryptobenthic reef fish community. Furthermore, there is no evidence of regeneration even after 5–35 generations of these short-lived species. These results have significant implications for our understanding of the response of coral reef ecosystems to global warming and highlight the importance of selecting appropriate criteria for evaluating reef resilience.     

Simple ecological trade-offs give rise to emergent cross-ecosystem distributions of a coral reef fish

Ecosystems are intricately linked by the flow of organisms across their boundaries, and such connectivity can be essential to the structure and function of the linked ecosystems. For example, many coral reef fish populations are maintained by the movement of individuals from spatially segregated juvenile habitats (i.e., nurseries, such as mangroves and seagrass beds) to areas preferred by adults. It is presumed that nursery habitats provide for faster growth (higher food availability) and/or low predation risk for juveniles, but empirical data supporting this hypothesis is surprisingly lacking for coral reef fishes. Here, we investigate potential mechanisms (growth, predation risk, and reproductive investment) that give rise to the distribution patterns of a common Caribbean reef fish species, Haemulon flavolineatum (French grunt). Adults were primarily found on coral reefs, whereas juvenile fish only occurred in non-reef habitats. Contrary to our initial expectations, analysis of length-at-age revealed that growth rates were highest on coral reefs and not within nursery habitats. Survival rates in tethering trials were 0% for small juvenile fish transplanted to coral reefs and 24-47% in the nurseries. As fish grew, survival rates on coral reefs approached those in non-reef habitats (56 vs. 77-100%, respectively). As such, predation seems to be the primary factor driving across-ecosystem distributions of this fish, and thus the primary reason why mangrove and seagrass habitats function as nursery habitat. Identifying the mechanisms that lead to such distributions is critical to develop appropriate conservation initiatives, identify essential fish habitat, and predict impacts associated with environmental change.     

Precision and accuracy of visual census technique for fish assemblages on coral patch reefs

Synopsis A visual census technique is described in which the results of three separate enumerations of fish at a site are combined to produce a best estimate of the fish fauna present. Its precision and accuracy are examined, and compared to those of censuses obtained by modifications of the technique. Visual censuses can display high repeatability, but they seldom (if ever) completely sample the fish present at a site. Accuracy varies with technique used. In our tests, the preferred method yielded 82% of species and 75% of individuals known to be present and potentially censurable at the time the observations were made. Visual censuses are of comparable accuracy to ichthyocide collections of unenclosed sites, but the two methods sample different components of the total fish fauna. It is important when using visual censuses to remember that their accuracy is not 100%.     

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.     

Facilitation in Caribbean coral reefs: high densities of staghorn coral foster greater coral condition and reef fish composition

Recovery of the threatened staghorn coral (Acropora cervicornis) is posited to play a key role in Caribbean reef resilience. At four Caribbean locations (including one restored and three extant populations), we quantified characteristics of contemporary staghorn coral across increasing conspecific densities, and investigated a hypothesis of facilitation between staghorn coral and reef fishes. High staghorn densities in the Dry Tortugas exhibited significantly less partial mortality, higher branch growth, and supported greater fish abundances compared to lower densities within the same population. In contrast, partial mortality, branch growth, and fish community composition did not vary with staghorn density at the three other study locations where staghorn densities were lower overall. This suggests that density-dependent effects between the coral and fish community may only manifest at high staghorn densities. We then evaluated one facilitative mechanism for such density-dependence, whereby abundant fishes sheltering in dense staghorn aggregations deliver nutrients back to the coral, fueling faster coral growth, thereby creating more fish habitat. Indeed, dense staghorn aggregations within the Dry Tortugas exhibited significantly higher growth rates, tissue nitrogen, and zooxanthellae densities than sparse aggregations. Similarly, higher tissue nitrogen was induced in a macroalgae bioassay outplanted into the same dense and sparse aggregations, confirming greater bioavailability of nutrients at high staghorn densities. Our findings inform staghorn restoration efforts, suggesting that the most effective targets may be higher coral densities than previously thought. These coral-dense aggregations may reap the benefits of positive facilitation between the staghorn and fish community, favoring the growth and survivorship of this threatened species.     

Impact of cyclones on hard coral and metapopulation structure,connectivity and genetic diversity of coral reef fish

Cyclones have one of the greatest effects on the biodiversity of coral reefs and the associated species. But it is unknown how stochastic alterations in habitat structure influence metapopulation structure, connectivity and genetic diversity. From 1993 to 2018, the reefs of the Capricorn Bunker Reef group in the southern part of the Great Barrier Reef were impacted by three tropical cyclones including cyclone Hamish (2009, category 5). This resulted in substantial loss of live habitat-forming coral and coral reef fish communities. Within 6–8 years after cyclones had devastated, live hard corals recovered by 50–60%. We show the relationship between hard coral cover and the abundance of the neon damselfish (Pomacentrus coelestis), the first fish colonizing destroyed reefs. We present the first long-term (2008–2015 years corresponding to 16–24 generations of P. coelestis) population genetic study to understand the impact of cyclones on the meta-population structure, connectivity and genetic diversity of the neon damselfish. After the cyclone, we observed the largest change in the genetic structure at reef populations compared to other years. Simultaneously, allelic richness of genetic microsatellite markers dropped indicating a great loss of genetic diversity, which increased again in subsequent years. Over years, metapopulation dynamics were characterized by high connectivity among fish populations associated with the Capricorn Bunker reefs (2200 km²); however, despite high exchange, genetic patchiness was observed with annual strong genetic divergence between populations among reefs. Some broad similarities in the genetic structure in 2015 could be explained by dispersal from a source reef and the related expansion of local populations. This study has shown that alternating cyclone-driven changes and subsequent recovery phases of coral habitat can greatly influence patterns of reef fish connectivity. The frequency of disturbances determines abundance of fish and genetic diversity within species.

     

Size-spectra as indicators of the effects of fishing on coral reef fish assemblages

The data requirements and resources needed to develop multispecies indicators of fishing impacts are often lacking and this is particularly true for coral reef fisheries. Size-spectra, relationships between abundance and body-size class, regardless of taxonomy, can be calculated from simple sizeabundance data. Both the slope and the mid-point height of the relationship can be compared at different fishing intensities. Here, we develop size-spectra for reef fish assemblages using body size- abundance data collected by underwater visual census in each of ten fishing grounds across a known gradient of fishing intensity in the Kadavu Island group, Fiji. Slopes of the size-spectra became steeper (F_9,69=3.20, p<0.01) and the height declined (F_9,69=15.78, p<0.001) with increasing fishing intensity. Regressions of numbers of individuals per size class across grounds were negative for all size classes, although the slope was almost zero for the smallest size class. Response to exploitation of each size class category was greatest for larger fish. Steepening of the slope with increasing fishing intensity largely resulted from reductions in the relative abundance of large fish and not from the ecological release of small fish following depletion of their predators. The slope and height of the size-spectrum appear to be good indicators of fishing effects on reef fish assemblages.     

Relationships among map resolution, fish assemblages, and habitat variables in a coral reef ecosystem

Benthic maps are broad-scale characterizations that lack the detailed environmental attributes which have been the focus of most prior empirical studies linking reef fish and habitat. We used multivariate analyses to quantify correlations among fish assemblages, local habitat variables, and reef types depicted in benthic maps. Benthic maps of a study system in the U.S. Virgin Islands with high (100 m² minimum mapping unit) and low (4,048 m² minimum mapping unit) spatial resolution, respectively, were evaluated. Benthic maps depicted six reef types and two shelf positions (lagoon vs. shelf). Fish assemblages and local environmental variables were quantified at random sites throughout the landscape by diver surveys. Multivariate ordination based on either fish assemblages or environmental data did not result in well-separated groups of sites. Mapped reef types were not associated with distinct values of either local environmental variables or fish assemblages. Reef types exhibited substantial overlap in ordination plots based on benthic characteristics with groupings based on fish assemblages showing even greater overlap. Ordination patterns involving reef type were largely the same for both low- and high-resolution maps. In contrast, sites showed clear groups for lagoon and shelf in ordinations based on both environmental variables and fish assemblage composition, respectively. These results suggest that knowledge of the overall fish assemblage or fine-scale environmental characteristics could not be used to predict reef type depicted in benthic maps or vice versa. In contrast, reef zone could be used to predict fish assemblage or fine-scale environmental variables and vice versa.