New insights into global patterns of ocean temperature anomalies: implications for coral reef health and management

Aim Coral reefs are widely considered to be particularly vulnerable to changes in ocean temperatures, yet we understand little about the broad‐scale spatio‐temporal patterns that may cause coral mortality from bleaching and disease. Our study aimed to characterize these ocean temperature patterns at biologically relevant scales. Location Global, with a focus on coral reefs. Methods We created a 4‐km resolution, 21‐year global ocean temperature anomaly (deviations from long‐term means) database to quantify the spatial and temporal characteristics of temperature anomalies related to both coral bleaching and disease. Then we tested how patterns varied in several key metrics of disturbance severity, including anomaly frequency, magnitude, duration and size. Results Our analyses found both global variation in temperature anomalies and fine‐grained spatial variability in the frequency, duration and magnitude of temperature anomalies. However, we discovered that even during major climatic events with strong spatial signatures, like the El Niño–Southern Oscillation, areas that had high numbers of anomalies varied between years. In addition, we found that 48% of bleaching‐related anomalies and 44% of disease‐related anomalies were less than 50 km², much smaller than the resolution of most models used to forecast climate changes. Main conclusions The fine‐scale variability in temperature anomalies has several key implications for understanding spatial patterns in coral bleaching‐ and disease‐related anomalies as well as for designing protected areas to conserve coral reefs in a changing climate. Spatial heterogeneity in temperature anomalies suggests that certain reefs could be targeted for protection because they exhibit differences in thermal stress. However, temporal variability in anomalies could complicate efforts to protect reefs, because high anomalies in one year are not necessarily predictive of future patterns of stress. Together, our results suggest that temperature anomalies related to coral bleaching and disease are likely to be highly heterogeneous and could produce more localized impacts of climate change.     

Differential uses of coral reef habitats by a poorly-known cryptic fish predator

This study used otolith microchemistry to evaluate whether the moray eel Gymnothorax chilospilus uses different habitats throughout its life (mainly juvenile and adult phases). Of the most informative trace elements within otoliths (the twelve isotopes ²³Na, ²⁵Mg, ⁴³Ca, ⁵⁵Mn, ⁵⁹Co, ⁶⁰Ni, ⁶³Cu, ⁶⁶Zn, ⁸⁶Sr, ¹¹¹Cd, ¹³⁸Ba and ²⁰⁸Pb) only three ratios of Ca (Na:Ca, Sr:Ca and Ba:Ca) were informative and therefore used in a multivariate regression-tree analysis. Using a multivariate partitioning, three main phases were described from profiles, including the larval life phase (leptocephali), the intermediate phase (longest section between the larval life phase and the terminal phase) and the terminal phase (final section i.e., the most recent months preceding the death of fish). According to concentrations of the three ratios to Ca, G. chilospilus can be separated into three groups during their larval life stage (very different in Sr and Na), four groups during the intermediate phase (few differences in Sr and Na) and three groups during the terminal phase (differences in Sr), illustrating that G. chilospilus inhabit different habitats during these three phases. Our results showed that the leptocephali encountered different oceanic water masses with fluctuating Sr:Ca ratios during the early larval phase. During the intermediate phase (main part of their life-span), they lived in lagoonal waters such as fringing reefs or reef flats of lagoonal islets, characterized by a lower Sr:Ca ratio. During the latter part of their life, approximately one third of G. chilospilus encountered more oceanic waters close to or at barrier reefs, suggesting possible movements of these fish along a coast-to-ocean gradient.     

Habitat degradation disrupts neophobia in juvenile coral reef fish

Habitat degradation not only disrupts habitat‐forming species, but alters the sensory landscape within which most species must balance behavioural activities against predation risk. Rapidly developing a cautious behavioural phenotype, a condition known as neophobia, is advantageous when entering a novel risky habitat. Many aquatic organisms rely on damage‐released conspecific cues (i.e. alarm cues) as an indicator of impending danger and use them to assess general risk and develop neophobia. This study tested whether settlement‐stage damselfish associated with degraded coral reef habitats were able to use alarm cues as an indicator of risk and, in turn, develop a neophobic response at the end of their larval phase. Our results indicate that fish in live coral habitats that were exposed to alarm cues developed neophobia, and, in situ, were found to be more cautious, more closely associated with their coral shelters and survived four‐times better than non‐neophobic control fish. In contrast, fish that settled onto degraded coral habitats did not exhibit neophobia and consequently suffered much greater mortality on the reef, regardless of their history of exposure to alarm cues. Our results show that habitat degradation alters the efficacy of alarm cues with phenotypic and survival consequences for newly settled recruits.     

Interactions between herbivorous fish guilds and their influence on algal succession on a coastal coral reef

Herbivory is an important mechanism affecting algal succession, particularly on coral reefs where the relationship between algae and corals is largely controlled by herbivores. However, different functional groups of herbivores may have contrasting effects on succession, which may explain different trajectories of coral reef recovery after disturbance. Here, the effects of different herbivore groups (roving herbivores = foragers and territorial damselfish = farmers) were isolated by a multi-factorial experiment carried out on a coastal coral reef with high macroalgal cover, high farmer densities and relatively low forager abundance. The effects of foragers and farmers were distinguished by monitoring algal succession on settlement tiles placed inside and outside exclusion cages, with orthogonal treatments established inside and outside damselfish territories (with appropriate cage controls). Within 12 months, algal assemblages on ungrazed tiles inside exclusion cages proceeded rapidly from fine filamentous turfs, to corticated algae, to tough erect (e.g. Amphiroa spp.) and foliose (e.g. Peyssonnellidae) calcified algae. Farmers had a dramatic impact on succession, essentially arresting the development of the algal community at a point where it was dominated by palatable filamentous algae of the genus Polysiphonia. Fleshy macroalgae such as Sargassum spp. were excluded from farmer territories. In contrast, foragers did not suppress fleshy macroalgae, but rather, appeared to decelerate succession and promote a relatively diverse assemblage. In contrast to forager-dominated reefs, farmer territories did not appear to function solely as forager exclusion areas or promote algal diversity as a result of intermediate grazing pressure. The relatively strong effects of farmers observed here may represent a future scenario for coral reefs that are increasingly subject to overfishing of large grazing fishes.     

Structure of Caribbean coral reef communities across a large gradient of fish biomass

The collapse of Caribbean coral reefs has been attributed in part to historic overfishing, but whether fish assemblages can recover and how such recovery might affect the benthic reef community has not been tested across appropriate scales. We surveyed the biomass of reef communities across a range in fish abundance from 14 to 593 g m⁻², a gradient exceeding that of any previously reported for coral reefs. Increased fish biomass was correlated with an increased proportion of apex predators, which were abundant only inside large marine reserves. Increased herbivorous fish biomass was correlated with a decrease in fleshy algal biomass but corals have not yet recovered.     

Microbial utilization of coral mucus in long term in situ incubation over a coral reef

The purpose of this study was to assess degradation and utilization of the mucus produced by 3 coral reef Anthozoa (Sarcophyton, Fungia and Acropora) by microorganisms. This was achieved by carrying out long term in situ incubations at Nouméa lagoon (New Caledonia).The microbial population including bacterial and eukaryotic cells was monitored by cell counts, cultures of mucus degraders, and by estimation of microbial activity from the pool of adenylates and enzymatic activity. In addition the chemical composition (C and N) of the mucus was monitored and its morphological features were observed by scanning electron microscope (SEM).Only slight differences were found between the 3 types of mucus studied. On the whole, they follow the same pattern of change. After a short bacterial growth phase (4 days), a bloom of eukaryotes (Flagellates, Ciliates and Diatoms) was observed. This eukaryote population remained constant for at least 10 days. A similar pattern has been described in the breakdown of detritus of plant origin.Several observations suggest that bacteria utilize only certain components of mucus, the most widely used being proteins, triglycerides and wax esters; these latter two compounds are known to be the dissolved photosynthetic products released by zooxanthellae during mucus secretion. Neither bacteria nor eukaryotes completely degrade the mucus web even after 21 days of incubation. The likelihood that mucus excretion is a defensive reaction against physical and chemical stresses might explain why mucus is a poor, or even inhibiting medium for the bacterial degraders isolated from the mucus itself.     

Food availability affects growth in a coral reef fish

Summary Pomacentrus amboinensis is common on small patch reefs within One Tree Lagoon (Great Barrier Reef), where it preferentially settles onto deep reefs. A preliminary experiment, in which juveniles were transplanted to identical reef structures at two sites, within two depth strata, indicated that juvenile growth and survivorship were better in deeper water. The hypothesis that this difference was due to food availability was tested by a supplemental feeding experiment, carried out at another two randomly chosen sites, within the same two depth strata. Fish were fed each day over a one month period, during which no mortality was observed. The growth rates of juveniles were markedly higher on all food-supplemented reefs, when compared to controls. Growth differed between depth strata, but there was no interaction between the food x depth factors, which would have suggested a greater effect of food supplementation in either habitat. Thus, although the difference between depths cannot be attributed to food availability, the results have a more general significance. Food appears to be a limiting resource (in terms of growth) in both the marginal shallow habitat, and the more suitable deeper habitat.     

Aggressive mimicry in a coral reef fish: The prey's view

Since all forms of mimicry are based on perceptual deception, the sensory ecology of the intended receiver is of paramount importance to test the necessary precondition for mimicry to occur, that is, model‐mimic misidentification, and to gain insight in the origin and evolutionary trajectory of the signals. Here we test the potential for aggressive mimicry by a group of coral reef fishes, the color polymorphic Hypoplectrus hamlets, from the point of view of their most common prey, small epibenthic gobies and mysid shrimp. We build visual models based on the visual pigments and spatial resolution of the prey, the underwater light spectrum and color reflectances of putative models and their hamlet mimics. Our results are consistent with one mimic‐model relationship between the butter hamlet H. unicolor and its model the butterflyfish Chaetodon capistratus but do not support a second proposed mimic‐model pair between the black hamlet H. nigricans and the dusky damselfish Stegastes adustus. We discuss our results in the context of color morphs divergence in the Hypoplectrus species radiation and suggest that aggressive mimicry in H. unicolor might have originated in the context of protective (Batesian) mimicry by the hamlet from its fish predators rather than aggressive mimicry driven by its prey.     

Traits,landmarks and outlines: Three congruent sides of a tale on coral reef fish morphology

Quantifying the morphology of organisms remains fundamental in ecology given the form‐function relationship. Morphology is quantifiable in traits, landmarks, and outlines, and the choice of approach may influence ecological conclusions to an unknown extent. Here, we apply these three approaches to 111 individual coral reef fish of 40 species common in Micronesia. We investigate the major dimensions of morphological variability among individuals, families, and predefined feeding functional groups. We find that although the approaches are complementary, they coincide in capturing elongation as the main dimension of variability. Furthermore, the choice of approach led to different interpretations regarding the degree of morphological differentiation among taxonomic and feeding functional groups. We also use each morphology dataset to compute community‐scale morphological diversity on Palauan reefs and investigate how the choice of dataset affects the detection of differences among sites and wave exposure levels. The exact ranking of sites from highest to lowest morphological diversity was sensitive to the approach used, but not the broad spatial pattern of morphological diversity. Conclusions regarding the effect of wave exposure on morphological diversity were robust to the approach used. Biodiversity hotspots (e.g., areas of exceptionally high diversity and/or endemism) are considered important conservation targets but their location may depend on the biodiversity metric used. In the same vein, our results caution against labelling particular sites as morphological diversity hotspots when metrics consider only a single aspect of morphology.     

Habitat type and complexity drive fish assemblages in a tropical seascape

Inshore marine seascapes support a diversity of interconnected habitats and are an important focus for biodiversity conservation. This study examines the importance of habitat attributes to fish assemblages across a mosaic of inshore habitats: coral reefs, rocky reefs, macroalgae beds and sand/rubble beds. Fishes and benthic habitats were surveyed at 34 sites around continental islands of the central Great Barrier Reef using baited remote underwater video stations (BRUVS). Species richness was influenced foremost by habitat type and also by structural complexity within habitat types. The most speciose assemblages occurred in coral and rocky reef habitats with high structural complexity, provided by the presence of coral bommies/overhangs, boulders and rock crevices. Nonetheless, macroalgae and sand/rubble beds also supported unique species, and therefore contributed to the overall richness of fish assemblages in the seascape. Most trophic groups had positive associations with complexity, which was the most important predictor for abundance of piscivorous fishes and mobile planktivores. There was significant differentiation of fish assemblages among habitats, with the notable exception of coral and rocky reefs. Species assemblages overlapped substantially between coral and rocky reefs, which had 60% common species, despite coral cover being lower on rocky reefs. This suggests that, for many species, rocky and coral substrates can provide equivalent habitat structure, emphasizing the importance of complexity in providing habitat refuges, and highlighting the contribution of rocky reefs to habitat provision within tropical seascapes. The results of this study support an emerging recognition of the collective value of habitat mosaics in inshore marine ecosystems.     

Coral microbialite environment in a Middle Miocene reef of Hungary

The presence of microbial crusts (microbialites) is reported here for the first time from a Middle Miocene (Badenian) coral reef in Hungary. The succession of initiation and development of the microbial crusts is described in relation to the reef architecture. The main features of the palaeoenvironment are discussed, with focus on the associated invertebrate faunas, mostly corals, molluscs, bryozoans, and crabs. We conclude that the microbial crusts developed under normal marine conditions and were a significant contributor to reef framework development, including its strengthening through calcification of the microbial organisms. Microbialites are anticipated in other Early and Middle Miocene coral reef occurrences of the Mediterranean–Paratethys realm, and to date may have simply escaped positive recognition.     

Character release following extinction in a Caribbean reef coral species complex

Abstract The Pleistocene extinction of the widespread organ‐pipe Montastraea coral had measurable morphological and ecological effects on surviving lineages of the Montastraea“annularis” species complex. Extinction of the organ‐pipe Montastraea occurred after more than 500,000 years of dominance in the shallow‐water reef habitat of Barbados. Extinction resulted in a morphological shift of the columnar Montastraea lineage from thick to thin columns in modern reef environments. Pleistocene colonies of the columnar morphotype sympatric with organ‐pipe Montastraea showed greater column widths than those in allopatry. We subjected our data to a number of criteria for interpreting the morphological shift as character release following lifting of competitive pressure after extinction. The morphological differences do not appear to be due either to chance or to physical properties of the marine environment. Differential local extinction and recolonization of four members of the species complex did not occur on Barbados, so that the species coexisted and appear to have coevolved between more than 600,000 and 82,000 years ago. The morphological shift is related to coral growth form and growth rate, and thus reflects the acquisition of a primary resource in corals‐light. Character release occurred at the same oceanic Caribbean island (Barbados) where environments have fluctuated with similar variance throughout the period of coexistence. Not only has competition among living members of the Montastraea“annularis” species complex been convincingly demonstrated, but trends in relative abundance among fossil members of the species complex strongly suggest that a competitive hierarchy was operating during their Pleistocene coexistence on Barbados. We also observed an ecological analogue to character release on another Caribbean island, Curaçao. The distribution and abundance of living columnarM. annularis s.s. and massive M. faveolata from the leeward reef crest in Curaçao is greater now than in the Pleistocene, when organ‐pipe Montastraea dominated this shallow‐water reef habitat. Extinction of the faster growing, shallow‐water organ‐pipe Montastraea resulted in higher abundance of the columnar Montastraea lineage in shallow‐water habitats, where it shifted its morphology to one adapted to high light levels. The species extinction released surviving lineages from a competitive network that had resulted in lower rank abundance in the Pleistocene community and enhanced abundance of both columnar M. annularis s.s. and M. faveolata in modern communities. Full validation of our interpretation of character release must await experiments that demonstrate whether phenotypic differences between populations have a genetic basis. However, we believe the results of this study point to the important, yet heretofore neglected, role that biological interactions have played in the evolution of closely related reef coral species.     

Factors influencing spatial distribution of fish communities on a fringing reef at Mauritius, S.W. Indian Ocean

This paper analyses the spatial patterns of fish communities on a narrow fringing reef of Mauritius and identifies some controlling factors. Canonical Correspondence Analysis revealed that the location in the reef ecosystem, the living coral coverage, and the proximity to a dredged area were the major factors controlling the distribution and abundance of fish species. Two distinct communities were observed across the fringing reef, representing a land-ocean gradient. The low diversity of fish species, and also of invertebrates such as corals, molluscs, and echinoderms is probably a consequence of the narrowness of the fringing reef and of anthropogenic impacts, notably the high pollution by nutrients.     

Positive indirect effects in a coral reef fish community

Indirect effects occur when two species interact through one or more intermediate species. Theoretical studies indicate that indirect interactions between two prey types that share common predators can be positive, neutral or negative. We document a positive indirect interaction between different types of prey fish on coral reefs in Australia. A high abundance of one type of prey fish (cardinalfishes: Apogonidae) resulted in higher recruitment, abundance and species richness of other prey fish. Our evidence indicates that these effects were not due to differential settlement but were instead due to differential post-settlement predation. We hypothesize that resident piscivores altered their foraging behaviour by concentrating on highly abundant cardinal-fish when they were present, leaving recruits of other species relatively unmolested. Indirect effects were evident within 48 h of settlement and persisted throughout the 42-day experiment, highlighting the importance of early post-settlement processes in these communities.     

Facultative mimicry: cues for colour change and colour accuracy in a coral reef fish

Mimetic species evolve colours and body patterns to closely resemble poisonous species and thus avoid predation (Batesian mimicry), or resemble beneficial or harmless species in order to approach and attack prey (aggressive mimicry). Facultative mimicry, the ability to switch between mimic and non-mimic colours at will, is uncommon in the animal kingdom, but has been shown in a cephalopod, and recently in a marine fish, the bluestriped fangblenny Plagiotremus rhinorhynchos, an aggressive mimic of the juvenile cleaner fish Labroides dimidiatus. Here we demonstrate for the first time that fangblennies adopted mimic colours in the presence of juvenile cleaner fish; however, this only occurred in smaller individuals. Field data indicated that when juvenile cleaner fish were abundant, the proportion of mimic to non-mimic fangblennies was greater, suggesting that fangblennies adopt their mimic disguise depending on the availability of cleaner fish. Finally, measurements of spectral reflectance suggest that not only do mimic fangblennies accurately resemble the colour of their cleaner fish models but also mimic other species of fish that they associate with. This study provides insights into the cues that control this remarkable facultative mimicry system and qualitatively measures its accuracy.     

Anticipative management for coral reef ecosystem services in the 21st century

Under projections of global climate change and other stressors, significant changes in the ecology, structure and function of coral reefs are predicted. Current management strategies tend to look to the past to set goals, focusing on halting declines and restoring baseline conditions. Here, we explore a complementary approach to decision making that is based on the anticipation of future changes in ecosystem state, function and services. Reviewing the existing literature and utilizing a scenario planning approach, we explore how the structure of coral reef communities might change in the future in response to global climate change and overfishing. We incorporate uncertainties in our predictions by considering heterogeneity in reef types in relation to structural complexity and primary productivity. We examine 14 ecosystem services provided by reefs, and rate their sensitivity to a range of future scenarios and management options. Our predictions suggest that the efficacy of management is highly dependent on biophysical characteristics and reef state. Reserves are currently widely used and are predicted to remain effective for reefs with high structural complexity. However, when complexity is lost, maximizing service provision requires a broader portfolio of management approaches, including the provision of artificial complexity, coral restoration, fish aggregation devices and herbivore management. Increased use of such management tools will require capacity building and technique refinement and we therefore conclude that diversification of our management toolbox should be considered urgently to prepare for the challenges of managing reefs into the 21st century.     

Eleven polymorphic microsatellite loci in a coral reef fish,Pterapogon kauderni

We describe the isolation and characterization of 11 polymorphic tetranucleotide microsatellite loci from a male mouthbrooding coral reef fish, the Banggai cardinalfish Pterapogon kauderni. In a sample of 37 fish from a natural population, polymorphism at these loci ranged from two to 15 alleles, with expected heterozygosities ranging from 0.107 to 0.928, enabling high‐resolution genetic studies of this coral reef fish.     

Elevated carbon dioxide affects behavioural lateralization in a coral reef fish

Elevated carbon dioxide (CO(2)) has recently been shown to affect chemosensory and auditory behaviour, and activity levels of larval reef fishes, increasing their risk of predation. However, the mechanisms underlying these changes are unknown. Behavioural lateralization is an expression of brain functional asymmetries, and thus provides a unique test of the hypothesis that elevated CO(2) affects brain function in larval fishes. We tested the effect of near-future CO(2) concentrations (880 μatm) on behavioural lateralization in the reef fish, Neopomacentrus azysron. Individuals exposed to current-day or elevated CO(2) were observed in a detour test where they made repeated decisions about turning left or right. No preference for right or left turns was observed at the population level. However, individual control fish turned either left or right with greater frequency than expected by chance. Exposure to elevated-CO(2) disrupted individual lateralization, with values that were not different from a random expectation. These results provide compelling evidence that elevated CO(2) directly affects brain function in larval fishes. Given that lateralization enhances performance in a number of cognitive tasks and anti-predator behaviours, it is possible that a loss of lateralization could increase the vulnerability of larval fishes to predation in a future high-CO(2) ocean.     

Distributional characteristics in fractionation of phosphorus in a coral reef sedimentary environment

Abstract

This paper focuses on the distribution of an important micronutrient element, phosphorus in the various coral reef sedimentary environments of the Lakshadweep Archipelago, in the Indian Ocean. One of the salient features observed is the high concentration of organic and residual phosphorous compared to inorganic phosphorous. This is particularly evident at stations characterised by higher total phosphorous concentrations. The concentrations of total phosphorous decrease with depth because of the upward migration of phosphate produced by mineralization of organic phosphorous and also as a result of the reduction of iron oxides to which phosphate is adsorbed. Among the inorganic forms, the major contribution towards total phosphorous pool was from calcium bound phosphorous. Sedimentary pH was not found to be a decisive factor in the distributional features of phosphorous forms in the surficial stations as well as in the core profile. In this study, organic carbon displayed co-variability with silty clay or fine sandy texture of the sediment. In most of the stations, organic carbon showed poor co-variance with organic and residual phosphorous form. This shows that major contribution towards organic and residual phosphorous form is from the residual fraction comprising biologically resistant or non-available phosphorous form composed of refractory materials.