Behaviourally Mediated Phenotypic Selection in a Disturbed Coral Reef Environment

Natural and anthropogenic disturbances are leading to changes in the nature of many habitats globally, and the magnitude and frequency of these perturbations are predicted to increase under climate change. Globally coral reefs are one of the most vulnerable ecosystems to climate change. Fishes often show relatively rapid declines in abundance when corals become stressed and die, but the processes responsible are largely unknown. This study explored the mechanism by which coral bleaching may influence the levels and selective nature of mortality on a juvenile damselfish, Pomacentrus amboinensis, which associates with hard coral. Recently settled fish had a low propensity to migrate small distances (40 cm) between habitat patches, even when densities were elevated to their natural maximum. Intraspecific interactions and space use differ among three habitats: live hard coral, bleached coral and dead algal-covered coral. Large fish pushed smaller fish further from the shelter of bleached and dead coral thereby exposing smaller fish to higher mortality than experienced on healthy coral. Small recruits suffered higher mortality than large recruits on bleached and dead coral. Mortality was not size selective on live coral. Survival was 3 times as high on live coral as on either bleached or dead coral. Subtle behavioural interactions between fish and their habitats influence the fundamental link between life history stages, the distribution of phenotypic traits in the local population and potentially the evolution of life history strategies.     

Predictive Modeling of Coral Disease Distribution within a Reef System

Diseases often display complex and distinct associations with their environment due to differences in etiology, modes of transmission between hosts, and the shifting balance between pathogen virulence and host resistance. Statistical modeling has been underutilized in coral disease research to explore the spatial patterns that result from this triad of interactions. We tested the hypotheses that: 1) coral diseases show distinct associations with multiple environmental factors, 2) incorporating interactions (synergistic collinearities) among environmental variables is important when predicting coral disease spatial patterns, and 3) modeling overall coral disease prevalence (the prevalence of multiple diseases as a single proportion value) will increase predictive error relative to modeling the same diseases independently. Four coral diseases: Porites growth anomalies (PorGA), Porites tissue loss (PorTL), Porites trematodiasis (PorTrem), and Montipora white syndrome (MWS), and their interactions with 17 predictor variables were modeled using boosted regression trees (BRT) within a reef system in Hawaii. Each disease showed distinct associations with the predictors. Environmental predictors showing the strongest overall associations with the coral diseases were both biotic and abiotic. PorGA was optimally predicted by a negative association with turbidity, PorTL and MWS by declines in butterflyfish and juvenile parrotfish abundance respectively, and PorTrem by a modal relationship with Porites host cover. Incorporating interactions among predictor variables contributed to the predictive power of our models, particularly for PorTrem. Combining diseases (using overall disease prevalence as the model response), led to an average six-fold increase in cross-validation predictive deviance over modeling the diseases individually. We therefore recommend coral diseases to be modeled separately, unless known to have etiologies that respond in a similar manner to particular environmental conditions. Predictive statistical modeling can help to increase our understanding of coral disease ecology worldwide.     

Larval Settlement: The Role of Surface Topography for Sessile Coral Reef Invertebrates

For sessile marine invertebrates with complex life cycles, habitat choice is directed by the larval phase. Defining which habitat-linked cues are implicated in sessile invertebrate larval settlement has largely concentrated on chemical cues which are thought to signal optimal habitat. There has been less effort establishing physical settlement cues, including the role of surface microtopography. This laboratory based study tested whether surface microtopography alone (without chemical cues) plays an important contributing role in the settlement of larvae of coral reef sessile invertebrates. We measured settlement to tiles, engineered with surface microtopography (holes) that closely matched the sizes (width) of larvae of a range of corals and sponges, in addition to surfaces with holes that were markedly larger than larvae. Larvae from two species of scleractinian corals (Acropora millepora and Ctenactis crassa) and three species of coral reef sponges (Luffariella variabilis, Carteriospongia foliascens and Ircinia sp.,) were used in experiments. L. variabilis, A. millepora and C. crassa showed markedly higher settlement to surface microtopography that closely matched their larval width. C. foliascens and Ircinia sp., showed no specificity to surface microtopography, settling just as often to microtopography as to flat surfaces. The findings of this study question the sole reliance on chemical based larval settlement cues, previously established for some coral and sponge species, and demonstrate that specific physical cues (surface complexity) can also play an important role in larval settlement of coral reef sessile invertebrates.     

Budget of Primary Production and Dinitrogen Fixation in a Highly Seasonal Red Sea Coral Reef

Biological dinitrogen (N₂) fixation (diazotrophy, BNF) relieves marine primary producers of nitrogen (N) limitation in a large part of the world oceans. N concentrations are particularly low in tropical regions where coral reefs are located, and N is therefore a key limiting nutrient for these productive ecosystems. In this context, the importance of diazotrophy for reef productivity is still not resolved, with studies up to now lacking organismal and seasonal resolution. Here, we present a budget of gross primary production (GPP) and BNF for a highly seasonal Red Sea fringing reef, based on ecophysiological and benthic cover measurements combined with geospatial analyses. Benthic GPP varied from 215 to 262 mmol C m^?2 reef d^?1, with hard corals making the largest contribution (41–76%). Diazotrophy was omnipresent in space and time, and benthic BNF varied from 0.16 to 0.92 mmol N m^?2 reef d^?1. Planktonic GPP and BNF rates were respectively approximately 60- and 20-fold lower than those of the benthos, emphasizing the importance of the benthic compartment in reef biogeochemical cycling. BNF showed higher sensitivity to seasonality than GPP, implying greater climatic control on reef BNF. Up to about 20% of net reef primary production could be supported by BNF during summer, suggesting a strong biogeochemical coupling between diazotrophy and the reef carbon cycle.     

Ecological Physiology of a Coral Pathogen and the Coral Reef Environment

Laboratory studies on the ecological physiology of a coral pathogen were carried out to investigate growth potential in terms of environmental factors that may control coral diseases on reefs. The disease chosen for this study, white plague type II, is considered to be one of the major diseases of Caribbean scleractinian corals, affecting a wide range of coral hosts and causing rapid and widespread tissue loss. It is caused by a single pathogen, the bacterium Aurantimonas coralicida. A series of laboratory experiments using a pure culture of the pathogen was carried out to examine the roles of temperature, pH, and O₂ concentration on growth rate. Results revealed optimal growth between 30 and 35°C, and between pH values of 6 and 8. There was a distinctive synergistic relationship between pH and temperature. Increasing temperature from 25 to 35°C expanded the range of pH tolerance from a minimum of 6.0 down to 5.0. O₂ concentration directly affected growth rate, which increased with increasing O₂. The combined effects of increasing O₂ and increasing temperature resulted in a synergistic effect of more rapid growth. These laboratory results are discussed in terms of the coral host and the range of the environmental factors that occur on coral reefs. We conclude that changing environmental conditions in the reef environment, in particular observed increases in water temperature, may be promoting coral diseases by allowing coral pathogens to expand their ecological niches. In the case of the white plague type II pathogen, elevated temperature would allow A. coralicida to colonize the low pH environment of the coral surface mucopolysaccharide layer as an initial stage of infection. The synergistic effect between temperature and oxygen concentration appeared to be less environmentally relevant for this coral pathogen.     

Pleistocene Perspectives on Coral Reef Community Structure

Composition and zonation of coral reef communities are unstableon the scale of human lifetimes, but stable on average overthousands to hundreds of thousands of years. Traditional small-scaleecological studies can miss community patterns which are obscuredby the noise of short-term change. Tests for stability requiremonitoring of populations over many generations—milleniafor long-lived corals and forest trees. The only recourse isthe fossil record.     

Pelagic Subsidies Underpin Fish Productivity on a Degraded Coral Reef

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Age-Related Shifts in Bacterial Diversity in a Reef Coral

This study investigated the relationship between microbial communities in differently sized colonies of the massive coral Coelastrea aspera at Phuket, Thailand where colony size could be used as a proxy for age. Results indicated significant differences between the bacterial diversity (ANOSIM, R = 0.76, p = 0.001) of differently sized colonies from the same intertidal reef habitat. Juvenile and small colonies (<6cm mean diam) harboured a lower bacterial richness than medium (~10cm mean diam) and large colonies (>28 cm mean diam). Bacterial diversity increased in a step-wise pattern from juveniles<small<medium colonies, which was then followed by a slight decrease in the two largest size classes. These changes appear to resemble a successional process which occurs over time, similar to that observed in the ageing human gut. Furthermore, the dominant bacterial ribotypes present in the tissues of medium and large sized colonies of C. aspera, (such as Halomicronema, an Oscillospira and an unidentified cyanobacterium) were also the dominant ribotypes found within the endolithic algal band of the coral skeleton; a result providing some support for the hypothesis that the endolithic algae of corals may directly influence the bacterial community present in coral tissues.     

Sporadic Disturbances in Fluctuating Coral Reef Environments: El Nino and Coral Reef Development in the Eastern Pacific

The disastrous effects of the intense 1982–83 El Niño-SouthernOscillation (ENSO) bring new insight into the long-term developmentof eastern Pacific coral reefs. The 1988–83 ENSO sea surfacewarming event caused extensive reef coral bleaching (loss ofsymbiotic zooxanthellae), resulting in up to 70–95% coralmortality on reefs in Costa Rica, Panama, Colombia and Ecuador.In the Galapagos Islands (Ecuador), most coral reefs experienced>95% coral mortality. Also, several coral species experiencedextreme reductions in population size, and local and regionalextinctions. The El Niño event spawned secondary disturbances,such as increased predation and bioerosion, that continue toimpact reef-building corals. The death of Pocillopora colonieswith their crustacean guards eliminated coral barriers now allowingthe corallivore Acanthaster planci access to formerly protectedcoral prey. Sea urchins and other organisms eroded disturbedcorals at rates that exceed carbonate production, potentiallyresulting in the elimination of existing reef buildups. In otherreefbuilding regions following extensive, catastrophic coralmortality, rapid recovery often occurs through the growth ofsurviving corals, recruitment of new corals from nearby sourcepopulations, and survival of consolidated reef surfaces. Inthe eastern Pacific, however, the return of upwelling conditionsand the survival of coral predators and bioeroders hamper coralreef recovery by reducing recruitment success and eroding coralreef substrates. Thus, coral reef growth that occurs betweendisturbance events is not conserved. Repeated El Niñodisturbances, which have occurred throughout the recent geologichistory of the eastern Pacific, prevent coral communities fromincreasing in diversity and limit the development and persistenceof significant reef features. The poor development of easternPacific coral reefs throughout Holocene and perhaps much ofPleistocene time may result from recurrent thermal disturbancesof the intensity of the 1982–83 El Niño event.     

Sex, Symbiosis and Coral Reef Communities

SYNOPSIS. Questions about how today's corals and coral reefswill fare in a future that holds not only increasing directanthropogenic impacts, but also global change, cannot be satisfactorilyanswered if we do not understand the relations of corals andreef systems to today's environmental conditions. This paperdiscusses four aspects of modern reef biology: coral reproduction,coral population biology, the coral-zooxanthella symbiosis,and reef community ecology. Conclusions of this survey of currentknowledge are that complexities of cnidarian reproductive biology,and our rudimentary knowledge of reproductive patterns in reefcnidarians, make forecasting based on current knowledge uncertainat best; new discoveries about the coral algal symbiotic systemsuggest a possible mode of adjustment to environmental changethat warrants a strong research effort; coral communities ofthe future may well be unlike what we are familiar with today;and these new assemblages will be shaped by the interactionof novel environmental conditions and the characteristics ofindividual reef species.     

Anthropogenic Stressors,Inter-Specific Competition and ENSO Effects on a Mauritian Coral Reef

Much of the western Indian Ocean suffered widespread loss of live coral in 1998 and interest is now focussed on the indirect effects of this coral loss on other components of the ecosystem, in particular fishes. However, it is just as important to identify changes in fish assemblages at locations that did not suffer coral mortality to understand local versus regional drivers. We surveyed benthic and fish communities on a reef flat in Mauritius five times between 1994 and 2005. The design allowed for comparison through time, along the coast and between inshore and offshore reef locations. The benthic community demonstrates a clear trend along the coast, likely in response to a dredged water ski lane, but little change through time. Branching Acropora colonies dominate much of the live coral and best explain patterns in the fish assemblage (P < 0.01). Few changes in overall fish species richness through time were identified, and observed changes were within fishery target families rather than species reliant on live coral. Departure from expected levels of taxonomic distinctness suggests degradation in the community associated with the dredged ski lane. Non-metric multi-dimensional scaling of the fish assemblage demonstrates a similar pattern to that seen in the benthos; greater differences along the coast (Global R = 0.34) than through time (Global R = 0.17) and no trend between reef positions. SIMPER analysis identified two species of Stegastes as the main drivers of trends in the MDS plot and the most dominant of these, S. lividus, appears to be reducing species richness of the remaining fish community. The study highlights Mauritius as a regional refugia of thermally-sensitive corals and specialised fish, suggesting a need for careful management.     

Impact of Herbivore Identity on Algal Succession and Coral Growth on a Caribbean Reef

Background

Herbivory is an important top-down force on coral reefs that regulates macroalgal abundance, mediates competitive interactions between macroalgae and corals, and provides resilience following disturbances such as hurricanes and coral bleaching. However, reductions in herbivore diversity and abundance via disease or over-fishing may harm corals directly and may indirectly increase coral susceptibility to other disturbances.

Methodology and Principal Findings

In two experiments over two years, we enclosed equivalent densities and masses of either single-species or mixed-species of herbivorous fishes in replicate, 4 m² cages at a depth of 17 m on a reef in the Florida Keys, USA to evaluate the effects of herbivore identity and species richness on colonization and development of macroalgal communities and the cascading effects of algae on coral growth. In Year 1, we used the redband parrotfish (Sparisoma aurofrenatum) and the ocean surgeonfish (Acanthurus bahianus); in Year 2, we used the redband parrotfish and the princess parrotfish (Scarus taeniopterus). On new substrates, rapid grazing by ocean surgeonfish and princess parrotfish kept communities in an early successional stage dominated by short, filamentous algae and crustose coralline algae that did not suppress coral growth. In contrast, feeding by redband parrotfish allowed an accumulation of tall filaments and later successional macroalgae that suppressed coral growth. These patterns contrast with patterns from established communities not undergoing primary succession; on established substrates redband parrotfish significantly reduced upright macroalgal cover while ocean surgeonfish and princess parrotfish allowed significant increases in late successional macroalgae.

Significance

This study further highlights the importance of biodiversity in affecting ecosystem function in that different species of herbivorous fishes had very different impacts on reef communities depending on the developmental stage of the community. The species-specific effects of herbivorous fishes suggest that a species-rich herbivore fauna can be critical in providing the resilience that reefs need for recovery from common disturbances such as coral bleaching and storm damage.     

Vulnerability of Coral Reef Fisheries to a Loss of Structural Complexity

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Sun Compass Orientation Helps Coral Reef Fish Larvae Return to Their Natal Reef

Reef fish sustain populations on isolated reefs and show genetic diversity between nearby reefs even though larvae of many species are swept away from the natal site during pelagic dispersal. Retention or recruitment to natal reefs requires orientation capabilities that enable larvae to find their way. Although olfactory and acoustically based orientation has been implicated in homing when larvae are in the reef’s vicinity, it is still unclear how they cope with greater distances. Here we show evidence for a sun compass mechanism that can bring the larvae to the vicinity of their natal reef. In a circular arena, pre-settlement larvae and early settlers (<24 hours) of the cardinal fish, Ostorhinchus doederleini, showed a strong SSE directional swimming response, which most likely has evolved to compensate for the locally prevailing large scale NNW current drift. When fish were clock-shifted 6 hours, they changed their orientation by ca. 180° as predicted by the tropical sun curve at One Tree Island, i.e. they used a time-compensated sun compass. Furthermore, the fish oriented most consistently at times of the day when the sun azimuth is easy to determine. Microsatellite markers showed that the larvae that had just arrived at One Tree Island genetically belonged to either the local reef population or to Fitzroy Reef located 12 kilometers to the SSE. The use of a sun compass adds a missing long-distance link to the hierarchy of other sensory abilities that can direct larvae to the region of origin, including their natal reef. Predominant local recruitment, in turn, can contribute to genetic isolation and potential speciation.     

Coral Reef Habitat Response to Climate Change Scenarios

Coral reef ecosystems are threatened by both climate change and direct anthropogenic stress. Climate change will alter the physico-chemical environment that reefs currently occupy, leaving only limited regions that are conducive to reef habitation. Identifying these regions early may aid conservation efforts and inform decisions to transplant particular coral species or groups. Here a species distribution model (Maxent) is used to describe habitat suitable for coral reef growth. Two climate change scenarios (RCP4.5, RCP8.5) from the National Center for Atmospheric Research’s Community Earth System Model were used with Maxent to determine environmental suitability for corals (order Scleractinia). Environmental input variables best at representing the limits of suitable reef growth regions were isolated using a principal component analysis. Climate-driven changes in suitable habitat depend strongly on the unique region of reefs used to train Maxent. Increased global habitat loss was predicted in both climate projections through the 21^st century. A maximum habitat loss of 43% by 2100 was predicted in RCP4.5 and 82% in RCP8.5. When the model is trained solely with environmental data from the Caribbean/Atlantic, 83% of global habitat was lost by 2100 for RCP4.5 and 88% was lost for RCP8.5. Similarly, global runs trained only with Pacific Ocean reefs estimated that 60% of suitable habitat would be lost by 2100 in RCP4.5 and 90% in RCP8.5. When Maxent was trained solely with Indian Ocean reefs, suitable habitat worldwide increased by 38% in RCP4.5 by 2100 and 28% in RCP8.5 by 2050. Global habitat loss by 2100 was just 10% for RCP8.5. This projection suggests that shallow tropical sites in the Indian Ocean basin experience conditions today that are most similar to future projections of worldwide conditions. Indian Ocean reefs may thus be ideal candidate regions from which to select the best strands of coral for potential re-seeding efforts.