Differential bleaching susceptibility among coral taxa and colony sizes, relative to bleaching severity across Australia's Great Barrier Reef and Coral Sea Marine Parks.

Climate-induced coral bleaching represents the foremost threat to coral assemblages globally, however bleaching susceptibility varies among and within coral taxa. We compared bleaching susceptibility among 10 coral morpho-taxa and two colony size classes relative to reef-scale bleaching severity at 33 reefs across the Great Barrier Reef and Coral Sea Marine Parks in February-March 2020. Colony size and bleaching severity caused the hierarchy of bleaching susceptibility among taxa to change considerably. Notably, massive Porites shifted from being among the least likely taxa to exhibit bleaching, to among the most susceptible as overall bleaching severity increased. Juvenile corals (≤5 cm diameter) were generally more resistant to bleaching, except for Montipora and Pocillopora colonies, which were more likely to bleach than adults (>5 cm). These findings suggest that colony size and reef-scale bleaching severity are important determinants of bleaching susceptibility among taxa and provide insights into possible shifts in the structure of coral assemblages caused by bleaching events.

Effects of habitat fragmentation on the recruitment and early post-settlement survival of coral reef fishes.

The combined effects of global climate change and local anthropogenic stressors are leading to increasing loss and fragmentation of habitats. On coral reefs, habitat loss has been shown to influence the abundance and composition of associated fish assemblages, yet few studies have considered how habitat fragmentation may influence reef fish populations and assemblages. Herein, we compared survival, growth and recruitment of reef fish among experimental patches composed of six similar sized colonies of finely branching Pocillopora spp. but with different degrees of fragmentation: coral colonies were clumped (unfragmented), divided into two groups (low fragmentation), three groups (moderate fragmentation) or six groups (high fragmentation). Thirty settlement-stage Pomacentrus amboinensis were tagged, released onto each of the experimental patches, and their survival monitored daily for 11 days. Abundance and species richness of all reef fishes that subsequently recruited to the patches were also recorded, and used to analyse recruitment and community composition. There were no detectable differences among fragmentation treatments in the abundance or composition of reef fish assemblages that recruited to the patches, however, fragmentation influenced the survivorship of P. amboinensis. Highest survival of P. amboinensis was recorded on the unfragmented patches (61%.11 days-1) and highly fragmented habitat patches (54%.11 days-1) and lowest survival on low and moderate fragmentation treatments (47% and 48%.11 days-1, respectively). This suggests that there may be multiple competing processes that moderate mortality (e.g., predation) in unfragmented versus highly fragmented habitats, with moderate levels of habitat fragmentation having the greatest influence on the early post-settlement survival of corsal reef fish.

Homing behaviour by destructive crown-of-thorns starfish is triggered by local availability of coral prey.

Corallivorous crown-of-thorns starfishes (Acanthaster spp.) can decimate coral assemblages on Indo-Pacific coral reefs during population outbreaks. While initial drivers of population irruptions leading to outbreaks remain largely unknown, subsequent dispersal of outbreaks appears coincident with depletion of coral prey. Here, we used in situ time-lapse photography to characterize movement of the Pacific crown-of-thorns starfish (Acanthaster cf. solaris) in the northern and southern Great Barrier Reef in 2015, during the fourth recorded population outbreak of the starfish, but prior to widespread coral bleaching. Daily tracking of 58 individuals over a total of 1117 h revealed all starfish to move a minimum of 0.52 m, with around half of all tracked starfish showing negligible daily displacement (less than 1 m day-1), ranging up to a maximum of 19 m day-1. Movement was primarily nocturnal and daily displacement varied spatially with variation in local availability of Acropora spp., which is the preferred coral prey. Two distinct behavioural modes emerged: (i) homing movement, whereby tracked paths (as tested against a random-walk-model) involved short displacement distances following distinct 'outward' movement to Acropora prey (typically displaying 'feeding scars') and 'homebound' movement to nearby shelter; versus (ii) roaming movement, whereby individuals showed directional movement beyond initial tracking positions without return. Logistic modelling revealed more than half of all tracked starfish demonstrated homing when local abundance (percentage cover) of preferred Acropora coral prey was greater than 33%. Our results reveal facultative homing by Acanthaster with the prey-dependent behavioural switch to roaming forays providing a mechanism explaining localized aggregations and diffusion of these population irruptions as prey is locally depleted.

Damselfishes alleviate the impacts of sediments on host corals.

Mutualisms play a critical role in ecological communities; however, the importance and prevalence of mutualistic associations can be modified by external stressors. On coral reefs, elevated sediment deposition can be a major stressor reducing the health of corals and reef resilience. Here, we investigated the influence of severe sedimentation on the mutualistic relationship between small damselfishes (Pomacentrus moluccensis and Dascyllus aruanus) and their coral host (Pocillopora damicornis). In an aquarium experiment, corals were exposed to sedimentation rates of approximately 100 mg cm-2 d-1, with and without fishes present, to test whether: (i) fishes influence the accumulation of sediments on coral hosts, and (ii) fishes moderate partial colony mortality and/or coral tissue condition. Colonies with fishes accumulated much less sediment compared with colonies without fishes, and this effect was strongest for colonies with D. aruanus (fivefold less sediment than controls) as opposed to P. moluccensis (twofold less sediment than controls). Colonies with symbiont fishes also had up to 10-fold less sediment-induced partial mortality, as well as higher chlorophyll and protein concentrations. These results demonstrate that fish mutualisms vary in the strength of their benefits, and indicate that some mutualistic or facilitative interactions might become more important for species health and resilience at high-stress levels.

Changes in the population and community structure of corals during recent disturbances (February 2016-October 2017) on Maldivian coral reefs.

Climate change is the greatest threat to coral reef ecosystems. In particular, increasing ocean temperatures are causing severe and widespread coral bleaching, contributing to extensive coral loss and degradation of coral reef habitats globally. Effects of coral bleaching are not however, equally apportioned among different corals, leading to shifts in population and community structure. This study explored variation in bleaching susceptibility and mortality associated with the 2016 severe mass bleaching in the Central Maldives Archipelago. Five dominant coral taxa (tabular Acropora, Acropora humilis, Acropora muricata, Pocillopora and massive Porites) were surveyed in February 2016 and October 2017 to test for changes in abundance and size structure. Substantial taxonomic differences in rates of mortality were observed; the most severely affected taxa, Acropora, were virtually extirpated during the course of this study, whereas some other taxa (most notably, massive Porites) were relatively unaffected. However, even the least affected corals exhibited marked changes in population structure. In February 2016 (prior to recent mass-bleaching), size-frequency distributions of all coral taxa were dominated by larger size classes with over-centralized, peaked distributions (negatively skewed with positive kurtosis) reflecting a mature population structure. In October 2017, after the bleaching, coral populations were dominated by smaller and medium size classes, reflecting high levels of mortality and injury among larger coral colonies. Pronounced changes in coral populations and communities in the Maldives, caused by coral bleaching and other disturbances (outbreaks of crown-of-thorns starfish and sedimentation), will constrain recovery capacity, further compounding upon recent coral loss.

Coral-dwelling fish moderate bleaching susceptibility of coral hosts.

Global environmental change has the potential to disrupt well established species interactions, with impacts on nutrient cycling and ecosystem function. On coral reefs, fish living within the branches of coral colonies can promote coral performance, and it has been hypothesized that the enhanced water flow and nutrients provided by fish to corals could ameliorate coral bleaching. The aim of this study was to evaluate the influence of small, aggregating damselfish on the health of their host corals (physiology, recovery, and survival) before, during, and after a thermal-bleaching event. When comparing coral colonies with and without fish, those with resident fish exhibited higher Symbiodinium densities and chlorophyll in both field and experimentally-induced bleaching conditions, and higher protein concentrations in field colonies. Additionally, colonies with damselfish in aquaria exhibited both higher photosynthetic efficiency (FV/FM) during bleaching stress and post-bleaching recovery, compared to uninhabited colonies. These results demonstrate that symbiotic damselfishes, and the services they provide, translate into measureable impacts on coral tissue, and can influence coral bleaching susceptibility/resilience and recovery. By mediating how external abiotic stressors influence coral colony health, damselfish can affect the functional responses of these interspecific interactions in a warming ocean.

Predation scars may influence host susceptibility to pathogens: evaluating the role of corallivores as vectors of coral disease.

Infectious diseases not regulated by host density, such as vector-borne diseases, have the potential to drive population declines and extinctions. Here we test the vector potential of the snail Drupella sp. and butterflyfish Chaetodon plebeius for two coral diseases, black band (BBD) and brown band (BrB) disease. Drupella transmitted BrB to healthy corals in 40% of cases immediately following feeding on infected corals, and even in 12% of cases 12 and 24 hours following feeding. However, Drupella was unable to transmit BBD in either transmission treatment. In a field experiment testing the vector potential of naturally-occurring fish assemblages, equivalent numbers of caged and uncaged coral fragments became infected with either BrB, BBD or skeletal eroding band, indicating that corallivorous fish were unlikely to have caused transmission. In aquaria, C. plebeius did not transmit either BBD or BrB, even following extended feeding on both infected and healthy nubbins. A literature review confirmed only four known coral disease vectors, all invertebrates, corroborating our conclusion that polyp-feeding fishes are unlikely to be vectors of coral diseases. This potentially because polyp-feeding fishes produce shallow lesions, not allowing pathogens to invade coral tissues. In contrast, corallivorous invertebrates that create deeper feeding scars increase pathogens transmission.

Coral recovery in the central Maldives archipelago since the last major mass-bleaching, in 1998.

Increasing frequency and severity of disturbances is causing global degradation of coral reef ecosystems. This study examined temporal changes in live coral cover and coral composition in the central Maldives from 1997 to 2016, encompassing two bleaching events, a tsunami, and an outbreak of Acanthaster planci. We also examined the contemporary size structure for five dominant coral taxa (tabular Acropora, Acropora muricata, Acropora humilis, Pocillopora spp, and massive Porites). Total coral cover increased throughout the study period, with marked increases following the 1998 mass-bleaching. The relative abundance of key genera has changed through time, where Acropora and Pocillopora (which are highly susceptible to bleaching) were under-represented following 1998 mass-bleaching but increased until outbreaks of A. planci in 2015. The contemporary size-structure for all coral taxa was dominated by larger colonies with peaked distributions suggesting that recent disturbances had a disproportionate impact on smaller colonies, or that recruitment is currently limited. This may suggest that coral resilience has been compromised by recent disturbances, and further bleaching (expected in 2016) could lead to highly protracted recovery times. We showed that Maldivian reefs recovered following the 1998 mass-bleaching event, but it took up to a decade, and ongoing disturbances may be eroding reef resilience.

Large predatory coral trout species unlikely to meet increasing energetic demands in a warming ocean.

Increased ocean temperature due to climate change is raising metabolic demands and energy requirements of marine ectotherms. If productivity of marine systems and fisheries are to persist, individual species must compensate for this demand through increasing energy acquisition or decreasing energy expenditure. Here we reveal that the most important coral reef fishery species in the Indo-west Pacific, the large predatory coral trout Plectropomus leopardus (Serranidae), can behaviourally adjust food intake to maintain body-condition under elevated temperatures, and acclimate over time to consume larger meals. However, these increased energetic demands are unlikely to be met by adequate production at lower trophic levels, as smaller prey species are often the first to decline in response to climate-induced loss of live coral and structural complexity. Consequently, ubiquitous increases in energy consumption due to climate change will increase top-down competition for a dwindling biomass of prey, potentially distorting entire food webs and associated fisheries.

Small-scale environmental variation influences whether coral-dwelling fish promote or impede coral growth.

Mutualistic symbioses are ubiquitous in nature and facilitate high biodiversity and productivity of ecosystems by enhancing the efficiency of energy and nutrient use within ecological communities. For example, small groups of fish that inhabit coral colonies in reef ecosystems potentially enhance coral growth through defense from coral predators, aeration of coral tissue and nutrient provisioning. This study examines whether the prevalence and consequences of fish-coral interactions vary among sites with different environmental conditions in a coral reef lagoon, using the humbug damselfish Dascyllus aruanus and its preferred coral host Pocillopora damicornis as a study system. Using a field experiment, we tested the site-specific effects of D. aruanus on coral growth, and show that the cost-benefit ratio for corals hosting fish varies with local environmental variation. Results of this study also demonstrate that fish prefer to inhabit coral colonies with particular branch-spacing characteristics, and that the local abundance of D. aruanus influences the proportion of coral colonies within a site that are occupied by fish rather than increasing the number of fish per colony. We also show that corals consistently benefit from hosting D. aruanus via defense from predation by corallivorous butterflyfish, regardless of local environmental conditions. These findings highlight the need to consider the potential for multiple scale- and state-dependent interaction effects when examining the ecology of fish-coral associations. We suggest that fluctuating cost-benefit ratios for species interactions may contribute to the maintenance of different colony phenotypes within coral populations.

The effects of coral bleaching on settlement preferences and growth of juvenile butterflyfishes.

Coral bleaching and associated mortality is an increasingly prominent threat to coral reef ecosystems. Although the effects of bleaching-induced coral mortality on reef fishes have been well demonstrated, corals can remain bleached for several weeks prior to recovery or death and little is known about how bleaching affects resident fishes during this time period. This study compared growth rates of two species of juvenile butterflyfishes (Chaetodon aureofasciatus and Chaetodon lunulatus) that were restricted to feeding upon either bleached or healthy coral tissue of Acropora spathulata or Pocillopora damicornis. Coral condition (bleached vs. unbleached) had no significant effects on changes in total length or weight over a 23-day period. Likewise, in a habitat choice experiment, juvenile butterflyfishes did not discriminate between healthy and bleached corals, but actively avoided using recently dead colonies. These results indicate that juvenile coral-feeding fishes are relatively robust to short term effects of bleaching events, provided that the corals do recover.

Increasing ocean temperatures reduce activity patterns of a large commercially important coral reef fish.

Large-bodied fish are critical for sustaining coral reef fisheries, but little is known about the vulnerability of these fish to global warming. This study examined the effects of elevated temperatures on the movement and activity patterns of the common coral trout Plectropomus leopardus (Serranidae), which is an important fishery species in tropical Australia and throughout the Indo West-Pacific. Adult fish were collected from two locations on Australia's Great Barrier Reef (23°S and 14°S) and maintained at one of four temperatures (24, 27, 30, 33 °C). Following >4 weeks acclimation, the spontaneous swimming speeds and activity patterns of individuals were recorded over a period of 12 days. At 24-27 °C, spontaneous swimming speeds of common coral trout were 0.43-0.45 body lengths per second (bls(-1)), but dropped sharply to 0.29 bls(-1) at 30 °C and 0.25 bls(-1) at 33 °C. Concurrently, individuals spent 9.3-10.6% of their time resting motionless on the bottom at 24-27 °C, but this behaviour increased to 14.0% at 30 °C and 20.0% of the time at 33 °C (mean ± SE). The impact of temperature was greatest for smaller individuals (<45 cm TL), showing significant changes to swimming speeds across every temperature tested, while medium (45-55 cm TL) and large individuals (>55 cm TL) were first affected by 30 °C and 33 °C, respectively. Importantly, there was some indication that populations can adapt to elevated temperature if presented with adequate time, as the high-latitude population decreased significantly in swimming speeds at both 30 °C and 33 °C, while the low-latitude population only showed significant reductions at 33 °C. Given that movement and activity patterns of large mobile species are directly related to prey encounter rates, ability to capture prey and avoid predators, any reductions in activity patterns are likely to reduce overall foraging and energy intake, limit the energy available for growth and reproduction, and affect the fitness and survival of individuals and populations.

From cooperation to combat: adverse effect of thermal stress in a symbiotic coral-crustacean community.

Although mutualisms are ubiquitous in nature, our understanding of the potential impacts of climate change on these important ecological interactions is deficient. Here, we report on a thermal stress-related shift from cooperation to antagonism between members of a mutualistic coral-dwelling community. Increased mortality of coral-defending crustacean symbionts Trapezia cymodoce (coral crab) and Alpheus lottini (snapping shrimp) was observed in response to experimentally elevated temperatures and reduced coral-host (Pocillopora damicornis) condition. However, strong differential numerical effects occurred among crustaceans as a function of species and sex, with shrimp (75%), and female crabs (55%), exhibiting the fastest and greatest declines in numbers. These declines were due to forceful eviction from the coral-host by male crabs. Furthermore, surviving female crabs were impacted by a dramatic decline (85%) in egg production, which could have deleterious consequences for population sustainability. Our results suggest that elevated temperature switches the fundamental nature of this interaction from cooperation to competition, leading to asymmetrical effects on species and/or sexes. Our study illustrates the importance of evaluating not only individual responses to climate change, but also potentially fragile interactions within and among susceptible species.

Specialist corallivores dominate butterflyfish assemblages in coral-dominated reef habitats.

This study examined the dietary habits and functional composition of butterflyfishes in the Chagos Archipelago, central Indian Ocean. Eighteen species of butterflyfishes were recorded in Chagos, including six obligate corallivores (Chaetodon bennetti, Chaetodon guttatissimus, Chaetodon meyeri, Chaetodon trifascialis, Chaetodon trifasciatus and Chaetodon zanzibarensis), five facultative corallivores (Chaetodon auriga, Chaetodon falcula, Chaetodon interruptus, Chaetodon kleinii and Chaetodon madagaskariensis), two non-corallivores (Chaetodon lunula and Chaetodon xanthocephalus) and a further five species (Chaetodon citrinellus, Chaetodon lineolatus, Heimitaurichthys zoster, Heniochus monoceros and Forcipiger flavissimus), for which local dietary habits were not studied. There were marked differences in the abundance of butterflyfishes among sites and between reef zones, mostly associated with variation in abundance of scleractinian corals. Obligate coral-feeding species (mostly C. trifascialis) dominated across all sites. This study suggests that coral feeding and high levels of dietary specialization contribute to high population-level fitness among coral reef butterflyfishes. Despite being more vulnerable to habitat disturbances and coral loss, it appears likely that specialist coral-feeding butterflyfishes are also much more resilient to occasional disturbances, and therefore dominate in a wide range of coral reef habitats.

Background mortality rates for recovering populations of Acropora cytherea in the Chagos Archipelago, central Indian Ocean.

This study quantified background rates of mortality for Acropora cytherea in the Chagos Archipelago. Despite low levels of anthropogenic disturbance, 27.5% (149/541) of A. cytherea colonies exhibited some level of partial mortality, and 9.0% (49/541) of colonies had recent injuries. A total of 15.3% of the overall surface area of physically intact A. cytherea colonies was dead. Observed mortality was partly attributable to overtopping and/or self-shading among colonies. There were also low-densities of Acanthaster planci apparent at some study sites. However, most of the recent mortality recorded was associated with isolated infestations of the coral crab, Cymo melanodactylus. A. cytherea is a relatively fast growing coral and these levels of mortality may be biologically unimportant. However, few studies have measured background rates of coral mortality, especially in the absence of direct human disturbances. These data are important for assessing the impacts of increasing disturbances, especially in projecting likely recovery.

Interspecific transmission and recovery of TCBS-induced disease between Acanthaster planci and Linckia guildingi.

The susceptibility of the coral-feeding crown-of-thorns starfish Acanthaster planci to disease may provide an avenue with which to effectively control population outbreaks that have caused severe and widespread coral loss in the Indo-Pacific. Injecting thiosulfate-citrate-bile-sucrose (TCBS) agar into A. planci tissues induced a disease characterized by dermal lesions, loss of skin turgor, collapsed spines, and accumulation of mucus on spine tips. Moreover, the symptoms (and presumably the agent) of this disease would spread rapidly intraspecifically, but interspecific transmission (to other species of echinoderms) is yet to be examined. Vibrio rotiferianus, which was previously reported as a pathogen isolated from lesions of experimentally infected A. planci, was also recovered from Linckia guildingi lesions after several days of direct contact with diseased A. planci, demonstrating disease transmission. However, all L. guildingi fully recovered after 31 ± 16 d. Further studies are in progress to understand the ecology of Vibrio infection in A. planci and the potential transmission risk to corals, fishes, and other echinoderms to evaluate whether injections of TCBS could be a viable tool for controlling A. planci outbreaks.

Effects of habitat modification on coastal fish assemblages.

The purpose of this study was to assess the influence of anthropogenic modification of coastal habitats on fish assemblages in Taiwan, comparing the abundance, species richness and taxonomic composition of fishes on natural v. artificial habitats. While there was no significant variation in the abundance or richness of fishes between natural and artificial habitats, the species composition of fishes in artificial habitats was significantly different from that of natural habitats. Natural reefs were characterized by greater abundance of Stethojulis spp. (Labridae), Abudefduf spp. (Pomacentridae) and Thalassoma spp. (Labridae), whereas anthropogenic habitats were dominated by Parupeneus indicus (Mullidae), Pempheris oualensis (Pempheridae) and Parapriacanthus ransonneti (Pempheridae). In general, it appears that specialist reef-associated species are being replaced with fishes that are much more generalist in their habitat-use. The loss of natural coastal habitats may threaten some species that cannot live in anthropogenically altered habitats, though the overall abundance and diversity of coastal fishes was not significantly different between natural and artificial habitats in Taiwan.

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.

Habitat degradation and fishing effects on the size structure of coral reef fish communities.

Overfishing and habitat degradation through climate change pose the greatest threats to sustainability of marine resources on coral reefs. We examined how changes in fishing pressure and benthic habitat composition influenced the size spectra of island-scale reef fish communities in Lau, Fiji. Between 2000 and 2006 fishing pressure declined in the Lau Islands due to declining human populations and reduced demand for fresh fish. At the same time, coral cover declined and fine-scale architectural complexity eroded due to coral bleaching and outbreaks of crown-of-thorns starfish, Acanthaster planci. We examined the size distribution of reef fish communities using size spectra analysis, the linearized relationship between abundance and body size class. Spatial variation in fishing pressure accounted for 31% of the variation in the slope of the size spectra in 2000, higher fishing pressure being associated with a steeper slope, which is indicative of fewer large-bodied fish and/or more small-bodied fish. Conversely, in 2006 spatial variation in habitat explained 53% of the variation in the size spectra slopes, and the relationship with fishing pressure was much weaker (approximately 12% of variation) than in 2000. Reduced cover of corals and lower structural complexity was associated with less steep size spectra slopes, primarily due to reduced abundance of fish < 20 cm. Habitat degradation will compound effects of fishing on coral reefs as increased fishing reduces large-bodied target species, while habitat loss results in fewer small-bodied juveniles and prey that replenish stocks and provide dietary resources for predatory target species. Effective management of reef resources therefore depends on both reducing fishing pressure and maintaining processes that encourage rapid recovery of coral habitat.

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.