An evaluation of a double-tailed deformity in a coral-reef surgeonfish Acanthurus nigrofuscus (Acanthuridae) using micro-computed tomography.

X-ray micro-computed tomography scans were used to examine the caudal-fin structure of an unusual double-tailed deformity in an adult brown surgeonfish Acanthurus nigrofuscus from the Great Barrier Reef. In both this case and in a similar double-tailed deformity in a juvenile Tomini surgeonfish Ctenochaetus tominiensis from the Philippines, the caudal fin was duplicated along the dorsoventral axis. Detailed examination of the A. nigrofuscus specimen revealed that the deformity was associated with duplication and reflection of the hypural plates and the posterior vertebrae, yet the fish survived to adulthood, indicating that the effects of duplication on survival may be limited.

Global marine protected areas do not secure the evolutionary history of tropical corals and fishes.

Although coral reefs support the largest concentrations of marine biodiversity worldwide, the extent to which the global system of marine-protected areas (MPAs) represents individual species and the breadth of evolutionary history across the Tree of Life has never been quantified. Here we show that only 5.7% of scleractinian coral species and 21.7% of labrid fish species reach the minimum protection target of 10% of their geographic ranges within MPAs. We also estimate that the current global MPA system secures only 1.7% of the Tree of Life for corals, and 17.6% for fishes. Regionally, the Atlantic and Eastern Pacific show the greatest deficit of protection for corals while for fishes this deficit is located primarily in the Western Indian Ocean and in the Central Pacific. Our results call for a global coordinated expansion of current conservation efforts to fully secure the Tree of Life on coral reefs.

Fifty million years of herbivory on coral reefs: fossils, fish and functional innovations.

The evolution of ecological processes on coral reefs was examined based on Eocene fossil fishes from Monte Bolca, Italy and extant species from the Great Barrier Reef, Australia. Using ecologically relevant morphological metrics, we investigated the evolution of herbivory in surgeonfishes (Acanthuridae) and rabbitfishes (Siganidae). Eocene and Recent surgeonfishes showed remarkable similarities, with grazers, browsers and even specialized, long-snouted forms having Eocene analogues. These long-snouted Eocene species were probably pair-forming, crevice-feeding forms like their Recent counterparts. Although Eocene surgeonfishes likely played a critical role as herbivores during the origins of modern coral reefs, they lacked the novel morphologies seen in modern Acanthurus and Siganus (including eyes positioned high above their low-set mouths). Today, these forms dominate coral reefs in both abundance and species richness and are associated with feeding on shallow, exposed algal turfs. The radiation of these new forms, and their expansion into new habitats in the Oligocene-Miocene, reflects the second phase in the development of fish herbivory on coral reefs that is closely associated with the exploitation of highly productive short algal turfs.

The ontogeny of home ranges: evidence from coral reef fishes.

The concept of home ranges is fundamental to ecology. Numerous studies have quantified how home ranges scale with body size across taxa. However, these relationships are not always applicable intraspecifically. Here, we describe how the home range of an important group of reef fish, the parrotfishes, scales with body mass. With masses spanning five orders of magnitude, from the early postsettlement stage through to adulthood, we find no evidence of a response to predation risk, dietary shifts or sex change on home range expansion rates. Instead, we document a distinct ontogenetic shift in home range expansion with sexual maturity. Juvenile parrotfishes displayed rapid home range growth until reaching approximately 100-150 mm length. Thereafter, the relationship between home range and mass broke down. This shift reflected changes in colour patterns, social status and reproductive behaviour associated with the transition to adult stages. While there is a clear relationship between body mass and home ranges among adult individuals of different species, it does not appear to be applicable to size changes within species. Ontogenetic changes in parrotfishes do not follow expected mass-area scaling relationships.

Pair formation in the herbivorous rabbitfish Siganus doliatus.

This study investigated the basis of pair formation in the abundant herbivorous rabbitfish Siganus doliatus on Orpheus Island, Great Barrier Reef. Pair formation was the most common social system in S. doliatus, with 67.4% of all individuals occurring in pairs. Pairs were stable (i.e. individuals remained with the same partner throughout the study) and pair members were found within 5 m of each other 82.9% of the time. Of the examined pairs, 25% were homosexual resulting in a proportion of heterosexual pairs (75%) that was significantly lower than expected if pairs were formed solely for reproductive reasons. Therefore, although reproduction appears to be the main driver of pair formation in S. doliatus, other factors are likely to influence this behaviour. The high density of individuals on the reef crest (5.7 ± 0 .9 individuals 200 m(-2); mean ± s.e.) and extensively overlapping home ranges of pairs indicated that the defence of territories plays no role in pair formation. Instead, it appears that pair formation in S. doliatus is driven, in part, by other, non-reproductive, ecological factors. It is suggested that pair formation allows for increased vigilance against predation and enables S. doliatus to execute a novel feeding behaviour.

Coral reefs as drivers of cladogenesis: expanding coral reefs, cryptic extinction events, and the development of biodiversity hotspots.

Diversification rates within four conspicuous coral reef fish families (Labridae, Chaetodontidae, Pomacentridae and Apogonidae) were estimated using Bayesian inference. Lineage through time plots revealed a possible late Eocene/early Oligocene cryptic extinction event coinciding with the collapse of the ancestral Tethyan/Arabian hotspot. Rates of diversification analysis revealed elevated cladogenesis in all families in the Oligocene/Miocene. Throughout the Miocene, lineages with a high percentage of coral reef-associated taxa display significantly higher net diversification rates than expected. The development of a complex mosaic of reef habitats in the Indo-Australian Archipelago (IAA) during the Oligocene/Miocene appears to have been a significant driver of cladogenesis. Patterns of diversification suggest that coral reefs acted as a refuge from high extinction, as reef taxa are able to sustain diversification at high extinction rates. The IAA appears to support both cladogenesis and survival in associated lineages, laying the foundation for the recent IAA marine biodiversity hotspot.

Evolutionary history of the butterflyfishes (f: Chaetodontidae) and the rise of coral feeding fishes.

Of the 5000 fish species on coral reefs, corals dominate the diet of just 41 species. Most (61%) belong to a single family, the butterflyfishes (Chaetodontidae). We examine the evolutionary origins of chaetodontid corallivory using a new molecular phylogeny incorporating all 11 genera. A 1759-bp sequence of nuclear (S7I1 and ETS2) and mitochondrial (cytochrome b) data yielded a fully resolved tree with strong support for all major nodes. A chronogram, constructed using Bayesian inference with multiple parametric priors, and recent ecological data reveal that corallivory has arisen at least five times over a period of 12 Ma, from 15.7 to 3 Ma. A move onto coral reefs in the Miocene foreshadowed rapid cladogenesis within Chaetodon and the origins of corallivory, coinciding with a global reorganization of coral reefs and the expansion of fast-growing corals. This historical association underpins the sensitivity of specific butterflyfish clades to global coral decline.

Crucial knowledge gaps in current understanding of climate change impacts on coral reef fishes.

Expert opinion was canvassed to identify crucial knowledge gaps in current understanding of climate change impacts on coral reef fishes. Scientists that had published three or more papers on the effects of climate and environmental factors on reef fishes were invited to submit five questions that, if addressed, would improve our understanding of climate change effects on coral reef fishes. Thirty-three scientists provided 155 questions, and 32 scientists scored these questions in terms of: (i) identifying a knowledge gap, (ii) achievability, (iii) applicability to a broad spectrum of species and reef habitats, and (iv) priority. Forty-two per cent of the questions related to habitat associations and community dynamics of fish, reflecting the established effects and immediate concern relating to climate-induced coral loss and habitat degradation. However, there were also questions on fish demographics, physiology, behaviour and management, all of which could be potentially affected by climate change. Irrespective of their individual expertise and background, scientists scored questions from different topics similarly, suggesting limited bias and recognition of a need for greater interdisciplinary and collaborative research. Presented here are the 53 highest-scoring unique questions. These questions should act as a guide for future research, providing a basis for better assessment and management of climate change impacts on coral reefs and associated fish communities.

Hopping hotspots: global shifts in marine biodiversity.

Hotspots of high species diversity are a prominent feature of modern global biodiversity patterns. Fossil and molecular evidence is starting to reveal the history of these hotspots. There have been at least three marine biodiversity hotspots during the past 50 million years. They have moved across almost half the globe, with their timing and locations coinciding with major tectonic events. The birth and death of successive hotspots highlights the link between environmental change and biodiversity patterns. The antiquity of the taxa in the modern Indo-Australian Archipelago hotspot emphasizes the role of pre-Pleistocene events in shaping modern diversity patterns.

Functional versatility supports coral reef biodiversity.

We explore the role of specialization in supporting species coexistence in high-diversity ecosystems. Using a novel ordination-based method to quantify specialist and generalist feeding structures and diets we examined the relationship between morphology and diet in 120 wrasses and parrotfishes from the Great Barrier Reef. We find that wrasses, despite their morphological diversity, exhibit weak links between morphology and diet and that specialist morphologies do not necessarily equate to specialized diets. The dominant pattern shows extensive overlap in morphology (functional morphospace occupation) among trophic groups; fish with a given morphology may have a number of feeding modes. Such trophic versatility may lay the foundation for both the origins and maintenance of high biodiversity on coral reefs.

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.

Confronting the coral reef crisis.

The worldwide decline of coral reefs calls for an urgent reassessment of current management practices. Confronting large-scale crises requires a major scaling-up of management efforts based on an improved understanding of the ecological processes that underlie reef resilience. Managing for improved resilience, incorporating the role of human activity in shaping ecosystems, provides a basis for coping with uncertainty, future changes and ecological surprises. Here we review the ecological roles of critical functional groups (for both corals and reef fishes) that are fundamental to understanding resilience and avoiding phase shifts from coral dominance to less desirable, degraded ecosystems. We identify striking biogeographic differences in the species richness and composition of functional groups, which highlight the vulnerability of Caribbean reef ecosystems. These findings have profound implications for restoration of degraded reefs, management of fisheries, and the focus on marine protected areas and biodiversity hotspots as priorities for conservation.

Climate change, human impacts, and the resilience of coral reefs.

The diversity, frequency, and scale of human impacts on coral reefs are increasing to the extent that reefs are threatened globally. Projected increases in carbon dioxide and temperature over the next 50 years exceed the conditions under which coral reefs have flourished over the past half-million years. However, reefs will change rather than disappear entirely, with some species already showing far greater tolerance to climate change and coral bleaching than others. International integration of management strategies that support reef resilience need to be vigorously implemented, and complemented by strong policy decisions to reduce the rate of global warming.

Evolutionary history of the parrotfishes: biogeography, ecomorphology, and comparative diversity.

The family Scaridae comprises about 90 species of herbivorous coral reef, rock reef, and seagrass fishes. Parrotfishes are important agents of marine bioerosion who rework the substrate with their beaklike oral jaws. Many scarid populations are characterized by complex social systems including highly differentiated sexual stages, territoriality, and the defense of harems. Here, we test a hypothesis of relationships among parrotfish genera derived from nearly 2 kb of nuclear and mitochondrial DNA sequence. The DNA tree is different than a phylogeny based on comparative morphology and leads to important reinterpretations of scarid evolution. The molecular data suggest a split among seagrass and coral reef associated genera with nearly 80% of all species in the coral reef clade. Our phylogenetic results imply an East Tethyan origin of the family and the recurrent evolution of excavating and scraping feeding modes. It is likely that ecomorphological differences played a significant role in the initial divergence of major scarid lineages, but that variation in color and breeding behavior has triggered subsequent diversification. We present a two-phase model of parrotfish evolution to explain patterns of comparative diversity. Finally, we discuss the application of this model to other adaptively radiating clades.

Modulation of prey capture kinematics in the cheeklined wrasse Oxycheilinus digrammus (Teleostei: Labridae).

The ability to modulate prey capture behaviors is of interest to organismal biologists as it suggests that predators can perceive features of the prey and select suitable behaviors from an available repertoire to successfully capture the item. Thus, behavior may be as important a trait as morphology in determining an organism's diet. Using high-speed video, we measured prey capture kinematics in three cheeklined wrasse, Oxycheilinus digrammus. We studied the effects of three experimental prey treatments: live fish, dead prawn suspended in the water column, and dead prawn pieces anchored to the substrate in a clip. Live prey elicited significantly more rapid strikes than dead prey suspended in the water column, and the head of the predator was expanded to significantly larger maxima. These changes in prey capture kinematics suggest the generation of more inertial suction. With greater expansion of the head, more water can be accelerated into the buccal cavity. The attached prey treatment elicited strikes as rapid as those on live prey. We suggest that the kinematics of rapid strikes on attached prey are indicative of attempts to use suction to detach the prey item. More rapid expansion of the buccal or mouth cavity should lead to higher velocities of water entering the mouth and therefore to enhanced suction. Further modulation in response to the attached prey item, such as clipping or wrenching behaviors, was not observed. J. Exp. Zool. 290:88-100, 2001.

Regional-scale assembly rules and biodiversity of coral reefs.

Tropical reef fishes and corals exhibit highly predictable patterns of taxonomic composition across the Indian and Pacific Oceans. Despite steep longitudinal and latitudinal gradients in total species richness, the composition of these key taxa is constrained within a remarkably narrow range of values. Regional-scale variation in reef biodiversity is best explained by large-scale patterns in the availability of shallow-water habitat. Once habitat area is accounted for, there is surprisingly little residual effect of latitude or longitude. Low-diversity regions are most vulnerable to human impacts such as global warming, underscoring the urgent need for integrated management at multinational scales.

Evolution and mechanics of long jaws in butterflyfishes (family Chaetodontidae).

We analyzed the functional morphology and evolution of the long jaws found in several butterflyfishes. We used a conservative reanalysis of an existing morphological dataset to generate a phylogeny that guided our selection of seven short- and long-jawed taxa in which to investigate the functional anatomy of the head and jaws: Chaetodon xanthurus, Prognathodes falcifer (formerly Chaetodon falcifer), Chelmon rostratus, Heniochus acuminatus, Johnrandallia nigrirostris, Forcipiger flavissimus, and F. longirostris. We used manipulations of fresh, preserved, and cleared and stained specimens to develop mechanical diagrams of how the jaws might be protruded or depressed. Species differed based on the number of joints within the suspensorium. We used high-speed video analysis of five of the seven species (C. xanthurus, Chel. rostratus, H. acuminatus, F. flavissimus, and F. longirostris) to test our predictions based on the mechanical diagrams: two suspensorial joints should facilitate purely anteriorly directed protrusion of the lower jaw, one joint should allow less anterior protrusion and result in more depression of the lower jaw, and no joints in the suspensorium should constrain the lower jaw to simple ventral rotation around the jaw joint, as seen in generalized perciform fishes. We found that the longest-jawed species, F. longirostris, was able to protrude its jaws in a predominantly anterior direction and further than any other species. This was achieved with little input from cranial elevation, the principal input for other known lower jaw protruders, and is hypothesized to be facilitated by separate modifications to the sternohyoideus mechanism and to the adductor arcus palatini muscle. In F. longirostris the adductor arcus palatini muscle has fibers oriented anteroposteriorly rather than medial-laterally, as seen in most other perciforms and in the other butterflyfish studied. These fibers are oriented such that they could rotate the ventral portion of the quadrate anteriorly, thus projecting the lower jaw anteriorly. The intermediate species lack modification of the adductor arcus palatini and do not protrude their jaws as far (in the case of F. flavissimus) or in a purely anterior fashion (in the case of Chel. rostratus). The short-jawed species both exhibit only ventral rotation of the lower jaw, despite the fact that H. acuminatus is closely related to Forcipiger.

Prey capture in long-jawed butterflyfishes (Chaetodontidae): the functional basis of novel feeding habits.

Several species of butterflyfishes (Chaetodontidae) possess extremely elongate jaws, and feed mostly by probing the benthos and biting off pieces of attached invertebrates. In contrast, Forcipiger longirostris, the longest-jawed chaetodontid, exhibits a novel pattern of prey use, feeding almost exclusively on small caridean shrimp, a mobile and highly elusive prey type that lives within the structure of coral reefs. We explored the functional basis of this novel pattern of prey use by comparing prey capture kinematics in this and four other butterflyfish species, including two other species that possess elongate jaws. High speed video recordings of feeding events on live adult brine shrimp were analyzed from individuals of five species: Forcipiger longirostris, F. flavissimus, Chelmon rostratus, Heniochus acuminatus, and Chaetodon xanthurus. We focused on a comparison among species of the relative contribution of "suction", measured as the amount of movement of the prey toward the predator's mouth, and "ram", measured as the distance moved by the predator toward the prey during the strike. All five species utilized a combination of suction and ram while feeding on brine shrimp. The contribution of suction did not differ significantly among species. However, F. longirostris exhibited a ram contribution to the strike that was more than twice that seen in any of the other species, permitting this species to initiate strikes from the greatest initial predator-prey distance. F. longirostris is known to possess a major structural novelty in the feeding mechanism that permits anterior movement of the entire jaw apparatus. The ability of this species to feed successfully on elusive prey appears to be related to exceptional jaw protrusion, resulting in greater use of ram during prey capture. This ability to protrude long, slender jaws toward the prey may allow it to move the jaws without detection within close enough proximity of the prey to then permit the effective use of suction. The use of extensive ram in this manner by small-mouthed fishes may be more widespread than previously thought.