Historical and contemporary determinants of global phylogenetic structure in tropical reef fish faunas

Identifying the main determinants of tropical marine biodiversity is essential for devising appropriate conservation measures mitigating the ongoing degradation of coral reef habitats. Based on a gridded distribution database and phylogenetic information, we compared the phylogenetic structure of assemblages for three tropical reef fish families (Labridae: wrasses, Pomacentridae: damselfishes and Chaetodontidae: butterflyfishes) using the net relatedness (NRI) and nearest taxon (NTI) indices. We then related these indices to contemporary and historical environmental conditions of coral reefs using spatial regression analyses. Higher levels of phylogenetic clustering were found for fish assemblages in the Indo‐Australian Archipelago (IAA), and more particularly when considering the NTI index. The phylogenetic structure of the Pomacentridae, and to a lower extent of the Chaeotodontidae and Labridae, was primarily associated with the location of refugia during the Quaternary period. Phylogenetic clustering in the IAA may partly result from vicariance events associated with coral reef fragmentation during the glacial periods of the Quaternary. Variation in the patterns among fish families further suggest that dispersal abilities may have interacted with past habitat availability in shaping the phylogenetic structure of tropical reef fish assemblages.     

Evolutionary patterns in tropical marine reef fish feeding

The majority of tropical reef fishes are acanthopterygians. Most of them are percomorphs and thus are likely monophyletic. In accordance to modern systematics, the primitive types among the latter are large-mouthed suction feeders. Species from advanced families often have biting oral jaws with a reduced number and complexly shaped teeth. Mouth sizes decrease from the primitive towards the advanced reef fishes when ranked according to increasing family numbers (Nelson 1984). To create a functional resource axis, Randall's (1967) and Hobson's (1974) data on tropical reef fish feeding were re-interpreted by ranking food items from mobile to sessile prey. The primitive paracantho pterygian and acanthopterygian reef fishes are large-mouthed, suction-feeding predators on mobile prey. Most of the advanced, small-mouthed species are browsers and grazers, but often feed on mobile prey too. Obligatory specialists (monophagous and unable to switch) seem to be relatively rare among modern reef fishes. The trends stated above indicate a wealth of parallel developments in many advanced families of reef fishes towards small, often biting oral jaws. This parallelism may be the result of comparable regimes of selection pressures in reefs and of the need for newly evolved species to establish themselves within the already existing guilds.     

Predators favour mimicry in a tropical reef fish

Batesian mimicry evolves when the 'umbrella' of protection provided by resemblance to a conspicuous unpalatable model species is sufficient to overcome increased predation risk associated with greater conspicuousness. However, the shape and extent of this umbrella, that is, how the level of protection provided by mimicry changes with degree of resemblance between model and mimic, is poorly known. We investigated the response of wild predatory fishes to plastic replicas of a model-mimic species pair of tropical reef fishes, Canthigaster valentini (a toxic pufferfish, the model) and Paraluteres prionurus (the putative mimic), and additional replicas with progressively lower degrees of resemblance to the mimic species. Our results reveal a relatively broad region of protection, indicated by a reduced approach rate by piscivorous fishes, surrounding the colour pattern of the model species. Protection increased with increasing resemblance. By contrast, the response of non-piscivorous fishes was unrelated to degree of resemblance of replicas to the model. Our results suggest that piscivorous fishes on the reef are educated regarding the toxicity of C. valentini, and that avoidance of fish having the pufferfish colour pattern has generated selection favouring mimetic resemblance by the palatable P. prionurus. The relatively broad protective umbrella has probably facilitated the initial evolution of resemblance in the palatable prey species despite the potential hazards of greater conspicuousness.     

Determinants of reef fish assemblages in tropical Oceanic islands

Diversity patterns are determined by biogeographic, energetic, and anthropogenic factors, yet few studies have combined them into a large‐scale framework in order to decouple and compare their relative effects on fish faunas. Using an empirical dataset derived from 1527 underwater visual censuses (UVC) at 18 oceanic islands (five different marine provinces), we determined the relative influence of such factors on reef fish species richness, functional dispersion, density and biomass estimated from each UVC unit. Species richness presented low variation but was high at large island sites. High functional dispersion, density, and biomass were found at islands with large local species pool and distance from nearest reef. Primary productivity positively affected fish richness, density and biomass confirming that more productive areas support larger populations, and higher biomass and richness on oceanic islands. Islands densely populated by humans had lower fish species richness and biomass reflecting anthropogenic effects. Species richness, functional dispersion, and biomass were positively related to distance from the mainland. Overall, species richness and fish density were mainly influenced by biogeographical and energetic factors, whereas functional dispersion and biomass were strongly influenced by anthropogenic factors. Our results extend previous hypotheses for different assemblage metrics estimated from empirical data and confirm the negative impact of humans on fish assemblages, highlighting the need for conservation of oceanic islands.     

Global patterns and predictors of tropical reef fish species richness

In the marine realm, the tropics host an extraordinary diversity of taxa but the drivers underlying the global distribution of marine organisms are still under scrutiny and we still lack an accurate global predictive model. Using a spatial database for 6336 tropical reef fishes, we attempted to predict species richness according to geometric, biogeographical and environmental explanatory variables. In particular, we aimed to evaluate and disentangle the predictive performances of temperature, habitat area, connectivity, mid‐domain effect and biogeographical region on reef fish species richness. We used boosted regression trees, a flexible machine‐learning technique, to build our predictive model and structural equation modeling to test for potential ‘mediation effects’ among predictors. Our model proved to be accurate, explaining 80% of the total deviance in fish richness using a cross‐validated procedure. Coral reef area and biogeographical region were the primary predictors of reef fish species richness, followed by coast length, connectivity, mid‐domain effect and sea surface temperature, with interactions between the region and other predictors. Important indirect effects of water temperature on reef fish richness, mediated by coral reef area, were also identified. The relationship between environmental predictors and species richness varied markedly among biogeographical regions. Our analysis revealed that a few easily accessible variables can accurately predict reef fish species richness. They also highlight concerns regarding ongoing environmental declines, with region‐specific responses to variation in environmental conditions predicting a variable response to anthropogenic impacts.     

Phylogenetic perspectives on reef fish functional traits

Functional traits have been fundamental to the evolution and diversification of entire fish lineages on coral reefs. Yet their relationship with the processes promoting speciation, extinction and the filtering of local species pools remains unclear. We review the current literature exploring the evolution of diet, body size, water column use and geographic range size in reef‐associated fishes. Using published and new data, we mapped functional traits on to published phylogenetic trees to uncover evolutionary patterns that have led to the current functional diversity of fishes on coral reefs. When examining reconstructed patterns for diet and feeding mode, we found examples of independent transitions to planktivory across different reef fish families. Such transitions and associated morphological alterations may represent cases in which ecological opportunity for the exploitation of different resources drives speciation and adaptation. In terms of body size, reconstructions showed that both large and small sizes appear multiple times within clades of mid‐sized fishes and that extreme body sizes have arisen mostly in the last 10 million years (Myr). The reconstruction of range size revealed many cases of disparate range sizes among sister species. Such range size disparity highlights potential vicariant processes through isolation in peripheral locations. When accounting for peripheral speciation processes in sister pairs, we found a significant relationship between labrid range size and lineage age. The diversity and evolution of traits within lineages is influenced by trait–environment interactions as well as by species and trait–trait interactions, where the presence of a given trait may trigger the development of related traits or behaviours. Our effort to assess the evolution of functional diversity across reef fish clades adds to the burgeoning research focusing on the evolutionary and ecological roles of functional traits. We argue that the combination of a phylogenetic and a functional approach will improve the understanding of the mechanisms of species assembly in extraordinarily rich coral reef communities.     

Habitats as surrogates of taxonomic and functional fish assemblages in coral reef ecosystems: a critical analysis of factors driving effectiveness

Species check-lists are helpful to establish Marine Protected Areas (MPAs) and protect local richness, endemicity, rarity, and biodiversity in general. However, such exhaustive taxonomic lists (i.e., true surrogate of biodiversity) require extensive and expensive censuses, and the use of estimator surrogates (e.g., habitats) is an appealing alternative. In truth, surrogate effectiveness appears from the literature highly variable both in marine and terrestrial ecosystems, making it difficult to provide practical recommendations for managers. Here, we evaluate how the biodiversity reference data set and its inherent bias can influence effectiveness. Specifically, we defined habitats by geomorphology, rugosity, and benthic cover and architecture criteria, and mapped them with satellite images for a New-Caledonian site. Fish taxonomic and functional lists were elaborated from Underwater Visual Censuses, stratified according to geomorphology and exposure. We then tested if MPA networks designed to maximize habitat richness, diversity and rarity could also effectively maximize fish richness, diversity, and rarity. Effectiveness appeared highly sensitive to the fish census design itself, in relation to the type of habitat map used and the scale of analysis. Spatial distribution of habitats (estimator surrogate's distribution), quantity and location of fish census stations (target surrogate's sampling), and random processes in the MPA design all affected effectiveness to the point that one small change in the data set could lead to opposite conclusions. We suggest that previous conclusions on surrogacy effectiveness, either positive or negative, marine or terrestrial, should be considered with caution, except in instances where very dense data sets were used without pseudo-replication. Although this does not rule out the validity of using surrogates of species lists for conservation planning, the critical joint examination of both target and estimator surrogates is needed for every case study.     

Comparing patterns of taxonomic,functional and phylogenetic diversity in reef coral communities

Coral Reefs - Biodiversity defines the variety of living organisms on this planet and is often quantified by the total number of species. However, species richness is insufficient in accounting for...     

Habitat amount drives the functional diversity and nestedness of anuran communities in an Atlantic Forest fragmented landscape

Natural environments disturbed by human activities can suffer from species extinctions, but some can still harbor high taxonomic diversity. However, disturbances may have impacts beyond the species level, if the species lost represent unique functions in the ecosystem. In this study, we evaluated to what extent the amount of habitat can determine the functional diversity and nestedness of amphibian communities in an Atlantic Forest fragmented landscape in Brazil, and if there is a threshold of habitat amount beyond which there is severe loss of functional diversity. As species responses may depend on their habitat type, we performed the analyses for three different sets of species: all species, forest‐dependent species, and generalist species. We also evaluated the relative importance of turnover and nestedness components to total functional dissimilarity among sites. Habitat amount affected functional diversity of frogs, especially for forest‐dependent species where a linear reduction was detected. The functional dissimilarity among sites was mostly explained by the nestedness component. The reduction of functional diversity was mediated by an ordered loss of traits, leading to a functionally nested metacommunity. These sensitive traits were closely related to habits and reproductive modes that depend on rivers and streams. The maintenance of functional diversity of frogs in fragmented landscapes must rely on the conservation of both terrestrial and aquatic environments, as some species and their traits can disappear from remnants of native vegetation lacking some specific habitats (e.g. streams). Abstract in Portuguese is available with online material.     

Diversification and functional evolution of reef fish feeding guilds

A core eco‐evolutionary aim is to better understand the factors driving the diversification of functions in ecosystems. Using phylogenetic, trophic, and functional information, we tested whether trophic habits (i.e. feeding guilds) affect lineage and functional diversification in two major radiations of reef fishes. Our results from wrasses (Labridae) and damselfishes (Pomacentridae) do not fully support the ‘dead‐end’ hypothesis that specialisation leads to reduce speciation rates because the tempo of lineage diversification did not substantially vary among guilds in both fish families. Our findings also demonstrate a tight relationship between trophic habits and functional roles held by fish in reef ecosystems, which is not associated with a variation in the tempo of functional diversification among guilds. By illustrating the pivotal importance of the generalist feeding strategy during the evolutionary history of reef fishes, our study emphasises the role of this feeding guild as a reservoir for future diversity.     

Herbivory drives large‐scale spatial variation in reef fish trophic interactions

Trophic interactions play a critical role in the structure and function of ecosystems. Given the widespread loss of biodiversity due to anthropogenic activities, understanding how trophic interactions respond to natural gradients (e.g., abiotic conditions, species richness) through large‐scale comparisons can provide a broader understanding of their importance in changing ecosystems and support informed conservation actions. We explored large‐scale variation in reef fish trophic interactions, encompassing tropical and subtropical reefs with different abiotic conditions and trophic structure of reef fish community. Reef fish feeding pressure on the benthos was determined combining bite rates on the substrate and the individual biomass per unit of time and area, using video recordings in three sites between latitudes 17°S and 27°S on the Brazilian Coast. Total feeding pressure decreased 10‐fold and the composition of functional groups and species shifted from the northern to the southernmost sites. Both patterns were driven by the decline in the feeding pressure of roving herbivores, particularly scrapers, while the feeding pressure of invertebrate feeders and omnivores remained similar. The differential contribution to the feeding pressure across trophic categories, with roving herbivores being more important in the northernmost and southeastern reefs, determined changes in the intensity and composition of fish feeding pressure on the benthos among sites. It also determined the distribution of trophic interactions across different trophic categories, altering the evenness of interactions. Feeding pressure was more evenly distributed at the southernmost than in the southeastern and northernmost sites, where it was dominated by few herbivores. Species and functional groups that performed higher feeding pressure than predicted by their biomass were identified as critical for their potential to remove benthic biomass. Fishing pressure unlikely drove the large‐scale pattern; however, it affected the contribution of some groups on a local scale (e.g., large‐bodied parrotfish) highlighting the need to incorporate critical functions into conservation strategies.     

Isolation of Clostridium botulinum from tropical fish

Electroporation was used to facilitate transformation of Listeria species with plasmid DNA. Optimal conditions for transformation of L. monocytogenes were a field strength of 8.5 kV/cm, 200 Ohms resistance, 25 microF capacitor with a time constant of 5 ms. With these conditions, 3.9 x 10(6) transformants/micrograms DNA were obtained. Under the same conditions, L. innocua and L. ivanovii exhibited a frequency of transformation similar to that of L. monocytogenes but a somewhat lower level was obtained with L. seeligeri.     

Predator density and the functional responses of coral reef fish

Predation is a key process driving coral reef fish population dynamics, with higher per capita prey mortality rates on reefs with more predators. Reef predators often forage together, and at high densities, they may either cooperate or antagonize one another, thereby causing prey mortality rates to be substantially higher or lower than one would expect if predators did not interact. However, we have a limited mechanistic understanding of how prey mortality rates change with predator densities. We re-analyzed a previously published observational dataset to investigate how the foraging response of the coney grouper (Cephalopholis fulva) feeding on the bluehead wrasse (Thalassoma bifasciatum) changed with shifts in predator and prey densities. Using a model-selection approach, we found that per-predator feeding rates were most consistent with a functional response that declines as predator density increases, suggesting either antagonistic interactions among predators or a shared antipredator behavioral response by the prey. Our findings suggest that variation in predator density (natural or anthropogenic) may have substantial consequences for coral reef fish population dynamics.     

Freshwater fish functional and taxonomic diversity above and below Niagara Falls

The Niagara River, which connects two Great Lakes (Erie and Ontario) and forms a border between Canada and the United States, has experienced decades of abiotic and biotic disturbance as well as long-term restoration efforts. Given the iconic riverscape and importance as a binational fisheries resource, a biodiversity assessment of the mainstem Niagara River fish assemblage is overdue. Here, fish assemblage and habitat data from a standardized boat electrofishing program of the Niagara River were combined with species trait data related to substrate associations, diet preferences, reproductive strategies, and body size to quantify biodiversity patterns among river sections (sites above and below Niagara Falls), seasons (spring, summer, fall), and years (2015–2017). Sixty-five species were captured representing a variety of trait combinations. Significant differences in functional dispersion and divergence (i.e., functional diversity) were observed between river sections, seasons, and (or) years. The fish community captured in the lower river in spring 2015 had both the highest average functional dispersion (2.08?±?0.32 SD) and divergence (0.88?±?0.04 SD) compared to the other seasonal sampling efforts, but relatively few fishes were captured (n?=?686). Although non-native fishes represented a small portion of the catch over the 3 years (8.6% of catch), the seasonal presence (spring and fall) of mostly introduced large-bodied salmonids expanded functional trait space in the lower river during these periods. The importance of rare species on functional diversity metrics suggests further insight on local species detection probabilities is needed to understand if differences in functional diversity reflect ecological patterns or are driven by sampling design.

     

Rock structure drives the taxonomic and functional diversity of endolithic microbial communities in extreme environments

Endolithic (rock-dwelling) microbial communities are ubiquitous in hyper-arid deserts around the world and the last resort for life under extreme aridity. These communities are excellent models to explore biotic and abiotic drivers of diversity because they are of low complexity. Using high-throughput amplicon and metagenome sequencing, combined with X-ray computed tomography, we investigated how water availability and substrate architecture modulated the taxonomic and functional composition of gypsum endolithic communities in the Atacama Desert, Chile. We found that communities inhabiting gypsum rocks with a more fragmented substrate architecture had higher taxonomic and functional diversity, despite having less water available. This effect was tightly linked with community connectedness and likely the result of niche differentiation. Gypsum communities were functionally similar, yet adapted to their unique micro-habitats by modulating their carbon and energy acquisition strategies and their growth modalities. Reconstructed population genomes showed that these endolithic microbial populations encoded potential pathways for anoxygenic phototrophy and atmospheric hydrogen oxidation as supplemental energy sources.     

Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish

Determining the capacity of organisms to acclimate and adapt to increased temperatures is key to understand how populations and communities will respond to global warming. Although there is evidence that elevated water temperature affects metabolism, growth and condition of tropical marine fish, it is unknown whether they have the potential to acclimate, given adequate time. We reared the tropical reef fish Acanthochromis polyacanthus through its entire life cycle at present day and elevated (+1.5 and+3.0 °C) water temperatures to test its ability to thermally acclimate to ocean temperatures predicted to occur over the next 50–100 years. Fish reared at 3.0 °C greater than the present day average reduced their resting oxygen consumption (RMR) during summer compared with fish reared at present day temperatures and tested at the elevated temperature. The reduction in RMR of up to 69 mg O₂ kg^?1 h^?1 in acclimated fish could represent a significant benefit to daily energy expenditure. In contrast, there was no acclimation to summer temperatures exhibited by fish reared at 1.5 °C above present day temperatures. Fish acclimated to +3.0 °C were smaller and in poorer condition than fish reared at present day temperatures, suggesting that even with acclimation there will be significant consequences for future populations of tropical fishes caused by global warming.     

Influence of depth on sex-specific energy allocation patterns in a tropical reef fish

The effect of depth on the distribution and sex-specific energy allocation patterns of a common coral reef fish, Chrysiptera rollandi (Pomacentridae), was investigated using depth-stratified collections over a broad depth range (5–39 m) and a translocation experiment. C. rollandi consistently selected rubble habitats at each depth, however abundance patterns did not reflect the availability of the preferred microhabitat suggesting a preference for depth as well as microhabitat. Reproductive investment (gonado-somatic index), energy stores (liver cell density and hepatocyte vacuolation), and overall body condition (hepato-somatic index and Fulton’s K) of female fish varied significantly among depths and among the three reefs sampled. Male conspecifics displayed no variation between depth or reef. Depth influenced growth dynamics, with faster initial growth rates and smaller mean asymptotic lengths with decreasing depth. In female fish, relative gonad weight and overall body condition (Fulton’s K and hepato-somatic index) were generally higher in shallower depths (≤10 m). Hepatic lipid storage was highest at the deepest sites sampled on each reef, whereas hepatic glycogen stores tended to decrease with depth. Depth was found to influence energy allocation dynamics in C. rollandi. While it is unclear what processes directly influenced the depth-related patterns in energy allocation, this study shows that individuals across a broad depth gradient are not all in the same physiological state and may contribute differentially to the population reproductive output. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.