Many ways to build an angler: diversity of feeding morphologies in a deep-sea evolutionary radiation.

Almost nothing is known about the diets of bathypelagic fishes, but functional morphology can provide useful tools to infer ecology. Here we quantify variation in jaw and tooth morphologies across anglerfishes (Lophiiformes), a clade spanning shallow and deep-sea habitats. Deep-sea ceratioid anglerfishes are considered dietary generalists due to the necessity of opportunistic feeding in the food-limited bathypelagic zone. We found unexpected diversity in the trophic morphologies of ceratioid anglerfishes. Ceratioid jaws span a functional continuum ranging from species with numerous stout teeth, a relatively slow but forceful bite, and high jaw protrusibility at one end (characteristics shared with benthic anglerfishes) to species with long fang-like teeth, a fast but weak bite and low jaw protrusibility at the other end (including a unique 'wolftrap' phenotype). Our finding of high morphological diversity seems to be at odds with ecological generality, reminiscent of Liem's paradox (morphological specialization allowing organisms to have broader niches). Another possible explanation is that diverse ceratioid functional morphologies may yield similar trophic success (many-to-one mapping of morphology to diet), allowing diversity to arise through neutral evolutionary processes. Our results highlight that there are many ways to be a successful predator in the deep sea.

Redescription of Conniella apterygia Allen and its reassignment in the genus Cirrhilabrus Temminck and Schlegel (Teleostei: Labridae), with comments on cirrhilabrin pelvic morphology.

Conniella apterygia is redescribed from re-examination of the holotype, two paratypes, and six additional specimens. The genus is closely allied to Cirrhilabrus, sharing similarities in general morphological and meristic details, but is separated from Cirrhilabrus and most other labrid fishes in lacking pelvic fins and a pelvic girdle. Recent molecular phylogenetic studies have provided strong evidence for the deep nesting of Conniella within Cirrhilabrus, contradicting its generic validity and suggesting that the loss of pelvic elements is autapomorphic. Consequently, the species is redescribed and assigned to the genus Cirrhilabrus, as Cirrhilabrus apterygia new combination. The pelvic morphologies of related cirrhilabrin labrids are discussed, and a new synapomorphy is identified for Paracheilinus.

Collapsing ecosystem functions on an inshore coral reef.

Ecosystem functions underpin productivity and key services to humans, such as food provision. However, as the severity of environmental stressors intensifies, it is becoming increasingly unclear if, and to what extent, critical functions and services can be sustained. This issue is epitomised on coral reefs, an ecosystem at the forefront of environmental transitions. We provide a functional profile of a coral reef ecosystem, linking time-series data to quantified processes. The data reveal a prolonged collapse of ecosystem functions in this previously resilient system. The results suggest that sediment accumulation in algal turfs has led to a decline in resource yields to herbivorous fishes and a decrease in fish-based ecosystem functions, including a collapse of both fish biomass and productivity. Unfortunately, at present, algal turf sediment accumulation is rarely monitored nor managed in coral reef systems. Our examination of functions through time highlights the value of directly assessing functions, their potential vulnerability, and the capacity of algal turf sediments to overwhelm productive high-diversity coral reef ecosystems.

Algal turf sediments limit the spatial extent of function delivery on coral reefs.

The presence of key organisms is frequently associated with the delivery of specific ecosystem functions. Areas with such organisms are therefore often considered to have greater levels of these functions. While this assumption has been the backbone of coral reef ecosystem-based management approaches for decades, we currently have only a limited understanding of how fish presence equates to function on coral reefs and whether this relationship is susceptible to stressors. To assess the capacity of a stressor to shape function delivery we used a multi-scale approach ranging from tens of kilometres across the continental shelf of Australia's Great Barrier Reef, down to centimetres within a reef habitat. At each scale, we quantified the spatial extent of a model function (detritivory) by a coral reef surgeonfish (Ctenochaetus striatus) and its potential to be shaped by sediments. At broad spatial scales, C. striatus presence was correlated strongly with algal turf sediment loads, while at smaller spatial scales, function delivery appears to be constrained by algal turf sediment distributions. In all cases, sediment loads above ~250-500 g m-2 were associated with a marked decrease in fish abundance or feeding activity, suggesting that a common ecological threshold lies within this range. Our results reveal a complex functional dynamic between proximate agents of function delivery (fish) and the ultimate drivers of function delivery (sediments), which emphasizes: a) weaknesses in the assumed links between fish presence and function, and b) the multi-scale capacity of algal turf sediments to shape reef processes. Unless direct extractive activities (e.g. fishing) are the main driver of function loss on coral reefs, managing to conserve fish abundance is unlikely to yield the desired outcomes. It only addresses one potential driver. Instead, management of both the agents that deliver functions (e.g. fishes), and the drivers that modify functions (e.g. sediments), is needed.

Response to Comment on "Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning".

Allgeier and Cline suggest that our model overestimates the contributions of cryptobenthic fishes to coral reef functioning. However, their 20-year model ignores the basic biological limits of population growth. If incorporated, cryptobenthic contributions to consumed fish biomass remain high (20 to 70%). Disturbance cycles and uncertainties surrounding the fate of large fishes on decadal scales further demonstrate the important role of cryptobenthic fishes.

Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning.

How coral reefs survive as oases of life in low-productivity oceans has puzzled scientists for centuries. The answer may lie in internal nutrient cycling and/or input from the pelagic zone. Integrating meta-analysis, field data, and population modeling, we show that the ocean's smallest vertebrates, cryptobenthic reef fishes, promote internal reef fish biomass production through extensive larval supply from the pelagic environment. Specifically, cryptobenthics account for two-thirds of reef fish larvae in the near-reef pelagic zone despite limited adult reproductive outputs. This overwhelming abundance of cryptobenthic larvae fuels reef trophodynamics via rapid growth and extreme mortality, producing almost 60% of consumed reef fish biomass. Although cryptobenthics are often overlooked, their distinctive demographic dynamics may make them a cornerstone of ecosystem functioning on modern coral reefs.

Algal turf sediments across the Great Barrier Reef: Putting coastal reefs in perspective.

Sediments trapped within algal turfs play a key role in mediating ecosystem processes on reefs. Despite this ecological importance, our understanding of turf-bound sediments on coastal reefs is limited, even though such reefs are heavily exposed to terrestrial sediments. We compared algal turf sediment loads, composition and grain size distributions among coastal reefs along the Great Barrier Reef (GBR) and compared these to turf-bound sediments on reefs across the GBR. Algal turf sediment loads on coastal reefs were on average 9.4 times higher than offshore reefs (range 2.2-16.1 times). Among coastal reefs there was marked variability in the loads (797.87-3681.78 g m-2), composition (organics 1.0-8.9%; silicates 27.4-93.0%) and grain size of sediments. Our data highlight the potential variability in physical and ecological factors that control sediment dynamics on coastal reefs, including proximity to rivers, and reveal that turfs on coastal reefs are heavily influenced by sediments.

The hidden half: ecology and evolution of cryptobenthic fishes on coral reefs.

Teleost fishes are the most diverse group of vertebrates on Earth. On tropical coral reefs, their species richness exceeds 6000 species; one tenth of total vertebrate biodiversity. A large proportion of this diversity is composed of cryptobenthic reef fishes (CRFs): bottom-dwelling, morphologically or behaviourally cryptic species typically less than 50 mm in length. Yet, despite their diversity and abundance, these fishes are both poorly defined and understood. Herein we provide a new quantitative definition and synthesise current knowledge on the diversity, distribution and life history of CRFs. First, we use size distributions within families to define 17 core CRF families as characterised by the high prevalence (>10%) of small-bodied species (<50 mm). This stands in strong contrast to 42 families of large reef fishes, in which virtually no small-bodied species have evolved. We posit that small body size has allowed CRFs to diversify at extremely high rates, primarily by allowing for fine partitioning of microhabitats and facilitation of allopatric reproductive isolation; yet, we are far from understanding and documenting the biodiversity of CRFs. Using rates of description since 1758, we predict that approximately 30 new species of cryptobenthic species will be described per year until 2050 (approximately twice the annual rate compared to large fishes). Furthermore, we predict that by the year 2031, more than half of the described coral reef fish biodiversity will consist of CRFs. These fishes are the 'hidden half' of vertebrate biodiversity on coral reefs. Notably, global geographic coverage and spatial resolution of quantitative data on CRF communities is uniformly poor, which further emphasises the remarkable reservoir of biodiversity that is yet to be discovered. Although small body size may have enabled extensive diversification within CRF families, small size also comes with a suite of ecological challenges that affect fishes' capacities to feed, survive and reproduce; we identify a range of life-history adaptations that have enabled CRFs to overcome these limitations. In turn, these adaptations bestow a unique socio-ecological role on CRFs, which includes a key role in coral reef trophodynamics by cycling trophic energy provided by microscopic prey to larger consumers. Although small in body size, the ecology and evolutionary history of CRFs may make them a critical component of coral-reef food webs; yet our review also shows that these fishes are highly susceptible to a variety of anthropogenic disturbances. Understanding the consequences of these changes for CRFs and coral reef ecosystems will require us to shed more light on this frequently overlooked but highly diverse and abundant guild of coral reef fishes.

A functional evaluation of feeding in the surgeonfish Ctenochaetus striatus: the role of soft tissues.

Ctenochaetus striatus is one of the most abundant surgeonfishes on Indo-Pacific coral reefs, yet the functional role and feeding ecology of this species remain unclear. This species is reported to possess a rigid structure in its palate that is used for scraping, but some authors have reported that this element is comprised of soft tissue. To resolve the nature and role of this structure in the feeding ecology of C. striatus we examined evidence from anatomical observations, scanning electron microscopy, histology, X-ray micro-computed tomography scanning, high-speed video and field observations. We found that C. striatus from the Great Barrier Reef possess a retention plate (RP) on their palates immediately posterior to the premaxillary teeth which is soft, covered in a thin veneer of keratin with a papillate surface. This RP appears to be used during feeding, but does not appear to be responsible for the removal of material, which is achieved primarily by a fast closure of the lower jaw. We infer that the RP acts primarily as a 'dustpan', in a 'dustpan and brush' feeding mechanism, to facilitate the collection of particulate material from algal turfs.

Cryptobenthic reef fishes.

Christopher Goatley and Simon Bran introduce the 'hidden' small fishes found on coral reefs.

Algal Turf Sediments and Sediment Production by Parrotfishes across the Continental Shelf of the Northern Great Barrier Reef.

Sediments are found in the epilithic algal matrix (EAM) of all coral reefs and play important roles in ecological processes. Although we have some understanding of patterns of EAM sediments across individual reefs, our knowledge of patterns across broader spatial scales is limited. We used an underwater vacuum sampler to quantify patterns in two of the most ecologically relevant factors of EAM sediments across the Great Barrier Reef: total load and grain size distribution. We compare these patterns with rates of sediment production and reworking by parrotfishes to gain insights into the potential contribution of parrotfishes to EAM sediments. Inner-shelf reef EAMs had the highest sediment loads with a mean of 864.1 g m-2, compared to 126.8 g m-2 and 287.4 g m-2 on mid- and outer-shelf reefs, respectively. High sediment loads were expected on inner-shelf reefs due to their proximity to the mainland, however, terrigenous siliceous sediments only accounted for 13-24% of total mass. On inner-shelf reef crests parrotfishes would take three months to produce the equivalent mass of sediment found in the EAM. On the outer-shelf it would take just three days, suggesting that inner-shelf EAMs are characterised by low rates of sediment turnover. By contrast, on-reef sediment production by parrotfishes is high on outer-shelf crests. However, exposure to oceanic swells means that much of this production is likely to be lost. Hydrodynamic activity also appears to structure sediment patterns at within-reef scales, with coarser sediments (> 250 µm) typifying exposed reef crest EAMs, and finer sediments (< 250 µm) typifying sheltered back-reef EAMs. As both the load and grain size of EAM sediments mediate a number of important ecological processes on coral reefs, the observed sediment gradients are likely to play a key role in the structure and function of the associated coral reef communities.

The Effects of Algal Turf Sediments and Organic Loads on Feeding by Coral Reef Surgeonfishes.

Herbivorous and detritivorous fishes interact closely with the epilithic algal matrix (EAM) on coral reefs. While sediment and organic detrital loads within the EAM might influence this interaction, the responses of functionally distinct fishes to changing sediment and organic loads have not been investigated. Aquarium based feeding trials were performed to assess how different sediment and organic loads affected feeding by the highly abundant surgeonfishes, Ctenochaetus striatus, a detritivore, and Acanthurus nigrofuscus, a herbivore. C. striatus were highly sensitive to even small increases in sediment loads (of just 75 g m-2), displaying a significant decline in feeding rates as sediment loads increased. Although C. striatus is a specialised detritivore, changing organic loads had no effect and suggests that selection of feeding surfaces is primarily mediated by total sediment loads rather than organic loads. By contrast, A. nigrofuscus displayed no changes to its feeding behaviour regardless of sediment or organic load. These findings highlight the complex, species-specific way that sediments may mediate key ecological processes on coral reefs.

The evolution of fishes and corals on reefs: form, function and interdependence.

Coral reefs are renowned for their spectacular biodiversity and the close links between fishes and corals. Despite extensive fossil records and common biogeographic histories, the evolution of these two key groups has rarely been considered together. We therefore examine recent advances in molecular phylogenetics and palaeoecology, and place the evolution of fishes and corals in a functional context. In critically reviewing the available fossil and phylogenetic evidence, we reveal a marked congruence in the evolution of the two groups. Despite one group consisting of swimming vertebrates and the other colonial symbiotic invertebrates, fishes and corals have remarkably similar evolutionary histories. In the Paleocene and Eocene [66-34 million years ago (Ma)] most modern fish and coral families were present, and both were represented by a wide range of functional morphotypes. However, there is little evidence of diversification at this time. By contrast, in the Oligocene and Miocene (34-5.3 Ma), both groups exhibited rapid lineage diversification. There is also evidence of increasing reef area, occupation of new habitats, increasing coral cover, and potentially, increasing fish abundance. Functionally, the Oligocene-Miocene is marked by the appearance of new fish and coral taxa associated with high-turnover fast-growth ecosystems and the colonization of reef flats. It is in this period that the functional characteristics of modern coral reefs were established. Most species, however, only arose in the last 5.3 million years (Myr; Plio-Pleistocene), with the average age of fish species being 5.3 Myr, and corals just 1.9 Myr. While these species are genetically distinct, phenotypic differences are often limited to variation in colour or minor morphological features. This suggests that the rapid increase in biodiversity during the last 5.3 Myr was not matched by changes in ecosystem function. For reef fishes, colour appears to be central to recent diversification. However, the presence of pigment patterns in the Eocene suggests that colour may not have driven recent diversification. Furthermore, the lack of functional changes in fishes or corals over the last 5 Myr raises questions over the role and importance of biodiversity in shaping the future of coral reefs.

Fine sediments suppress detritivory on coral reefs.

Increasing sediment inputs are recognised as an important factor leading to coral reef degradation. However, the role of sediments in ecological processes is poorly understood. This study used paired-choice trials to quantify the effects of sediment grain size and chemical composition on feeding by the abundant detritivorous reef fish, Ctenochaetus striatus. The size of sediments from algal turfs were also compared to those ingested by reef-dwelling C. striatus. Algal turfs containing coarser sediments were preferred by C. striatus, while sediment composition (reefal carbonates vs. riverine silicates) had little effect. On the reef, C. striatus ingested finer sediments than those present in algal turfs. C. striatus appears to prefer algal turfs with coarser sediments as this facilitates ingestion of fine detrital particles, while finer sediments prevent selective feeding on detritus. These findings suggest that fine sediments from terrestrial runoff or dredging may be detrimental to feeding by detritivorous species.

Composition and temporal stability of turf sediments on inner-shelf coral reefs.

Elevated sediment loads within the epilithic algal matrix (EAM) of coral reefs can increase coral mortality and inhibit herbivory. Yet the composition, distribution and temporal variability of EAM sediment loads are poorly known, especially on inshore reefs. This study quantified EAM sediment loads (including organic particulates) and algal length across the reef profile of two bays at Orpheus Island (inner-shelf Great Barrier Reef) over a six month period. We examined the total sediment mass, organic load, carbonate and silicate content, and the particle sizes of EAM sediments. Throughout the study period, all EAM sediment variables exhibited marked variation among reef zones. However, EAM sediment loads and algal length were consistent between bays and over time, despite major seasonal variation in climate including a severe tropical cyclone. This study provides a comprehensive description of EAM sediments on inshore reefs and highlights the exceptional temporal stability of EAM sediments on coral reefs.

The Rise of Jaw Protrusion in Spiny-Rayed Fishes Closes the Gap on Elusive Prey.

Jaw protrusion is one of the most important innovations in vertebrate feeding over the last 400 million years [1, 2]. Protrusion enables a fish to rapidly decrease the distance between itself and its prey [2, 3]. We assessed the evolution and functional implications of jaw protrusion in teleost fish assemblages from shallow coastal seas since the Cretaceous. By examining extant teleost fishes, we identified a robust morphological predictor of jaw protrusion that enabled us to predict the extent of jaw protrusion in fossil fishes. Our analyses revealed increases in both average and maximum jaw protrusion over the last 100 million years, with a progressive increase in the potential impact of fish predation on elusive prey. Over this period, the increase in jaw protrusion was initially driven by a taxonomic restructuring of fish assemblages, with an increase in the proportion of spiny-rayed fishes (Acanthomorpha), followed by an increase in the extent of protrusion within this clade. By increasing the ability of fishes to catch elusive prey [2, 4], jaw protrusion is likely to have fundamentally changed the nature of predator-prey interactions and may have contributed to the success of the spiny-rayed fishes, the dominant fish clade in modern oceans [5].

Evolution of long-toothed fishes and the changing nature of fish-benthos interactions on coral reefs.

Interactions between fishes and the benthos have shaped the development of marine ecosystems since at least the early Mesozoic. Here, using the morphology of fish teeth as an indicator of feeding abilities, we quantify changes over the last 240 million years of reef fish evolution. Fossil and extant coral reef fish assemblages reveal exceptional stasis in tooth design over time, with one notable exception, a distinct long-toothed form. Arising only in the last 40 million years, these long-toothed fishes have bypassed the invertebrate link in the food chain, feeding directly on benthic particulate material. With the appearance of elongated teeth, these specialized detritivores have moved from eating invertebrates to eating the food of invertebrates. Over evolutionary time, fishes have slid back down the food chain.

Ecological consequences of sediment on high-energy coral reefs.

Sediments are widely accepted as a threat to coral reefs but our understanding of their ecological impacts is limited. Evidence has suggested that benthic sediments bound within the epilithic algal matrix (EAM) suppress reef fish herbivory, a key ecological process maintaining reef resilience. An experimental combination of caging and sediment addition treatments were used to investigate the effects of sediment pulses on herbivory and EAMs and to determine whether sediment addition could trigger a positive-feedback loop, leading to deep, sediment-rich turfs. A 1-week pulsed sediment addition resulted in rapid increases in algal turf length with effects comparable to those seen in herbivore exclusion cages. Contrary to the hypothesised positive-feedback mechanism, benthic sediment loads returned to natural levels within 3 weeks, however, the EAM turfs remained almost 60% longer for at least 3 months. While reduced herbivore density is widely understood to be a major threat to reefs, we show that acute disturbances to reef sediments elicit similar ecological responses in the EAM. With reefs increasingly threatened by both reductions in herbivore biomass and altered sediment fluxes, the development of longer turfs may become more common on coral reefs.

Sediment suppresses herbivory across a coral reef depth gradient.

Sediments are a ubiquitous feature of all coral reefs, yet our understanding of how they affect complex ecological processes on coral reefs is limited. Sediment in algal turfs has been shown to suppress herbivory by coral reef fishes on high-sediment, low-herbivory reef flats. Here, we investigate the role of sediment in suppressing herbivory across a depth gradient (reef base, crest and flat) by observing fish feeding following benthic sediment reductions. We found that sediment suppresses herbivory across all reef zones. Even slight reductions on the reef crest, which has 35 times less sediment than the reef flat, resulted in over 1800 more herbivore bites (h(-1) m(-2)). The Acanthuridae (surgeonfishes) were responsible for over 80 per cent of all bites observed, and on the reef crest and flat took over 1500 more bites (h(-1) m(-2)) when sediment load was reduced. These findings highlight the role of natural sediment loads in shaping coral reef herbivory and suggest that changes in benthic sediment loads could directly impair reef resilience.

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.