Andrew S. Hoey

Global warming and recurrent mass bleaching of corals

During 2015–2016, record temperatures triggered a pan-tropical episode of coral bleaching, the third global-scale event since mass bleaching was first documented in the 1980s. Here we examine how and why the severity of recurrent major bleaching events has varied at multiple scales, using aerial and underwater surveys of Australian reefs combined with satellite-derived sea surface temperatures. The distinctive geographic footprints of recurrent bleaching on the Great Barrier Reef in 1998, 2002 and 2016 were determined by the spatial pattern of sea temperatures in each year. Water quality and fishing pressure had minimal effect on the unprecedented bleaching in 2016, suggesting that local protection of reefs affords little or no resistance to extreme heat. Similarly, past exposure to bleaching in 1998 and 2002 did not lessen the severity of bleaching in 2016. Consequently, immediate global action to curb future warming is essential to secure a future for coral reefs.

Sleeping Functional Group Drives Coral-Reef Recovery

The worlds coral reefs are in decline, with many exhibiting a phase shift from coral to macroalgal dominance . This change is often associated with habitat loss and overharvesting of herbivorous fishes, particularly parrotfishes and surgeonfishes . The challenge is to reverse this decline and enhance the resilience of coral-reef ecosystems . We demonstrate, by using a large-scale experimentally induced phase shift, that the rapid reversal from a macroalgal-dominated to a coral- and epilithic algal-dominated state was not a result of herbivory by parrotfishes or surgeonfishes. Surprisingly, phase-shift reversal was primarily driven by a single batfish species (Platax pinnatus), a fish previously regarded as an invertebrate feeder. The 43 herbivorous fishes in the local fauna played only a minor role, suggesting that biodiversity may not offer the protection we hoped for in complex ecosystems. Our findings highlight the dangers faced by coral reefs and other threatened complex ecosystems: Species or functional groups that prevent phase shifts may not be able to reverse phase shifts once they occur. Nevertheless, reversal is possible. The critical issue is to identify and protect those groups that underpin the resilience and regeneration of complex ecosystems.

Cross-shelf variation in the role of parrotfishes on the Great Barrier Reef

Herbivorous fishes are a key functional group on coral reefs. These fishes are central to the capacity of reefs to resist phase shifts and regenerate after disturbance. Despite this importance few studies have quantified the direct impact of these fishes on coral reefs. In this study the roles of parrotfishes, a ubiquitous group of herbivorous fishes, were examined on reefs in the northern Great Barrier Reef. The distribution of 24 species of parrotfish was quantified on three reefs in each of three cross-shelf regions. Functional roles (grazing, erosion, coral predation and sediment reworking) were calculated as the product of fish density, bite area or volume, bite rate, and the proportion of bites taken from various substrata. Inner-shelf reefs supported high densities but low biomass of parrotfishes, with high rates of grazing and sediment reworking. In contrast, outer-shelf reefs were characterised by low densities and high biomass of parrotfish, with high rates of erosion and coral predation. Mid-shelf reefs displayed moderate levels of all roles examined. The majority of this variation in functional roles was attributable to just two species. Despite being rare, Bolbometopon muricatum, the largest parrotfish species, accounted for 87.5% of the erosion and 99.5% of the coral predation on outer-shelf reefs. B. muricatum displayed little evidence of selectivity of feeding, with most substrata being consumed in proportion to their availability. In contrast, the high density of Scarus rivulatus accounted for over 70% of the total grazing and sediment reworking on inner-shelf reefs. This marked variation in the roles of parrotfishes across the continental shelf suggests that each shelf system is shaped by fundamentally different processes.

Limited functional redundancy in a high diversity system: single species dominates key ecological process on coral reefs

Herbivory is a key process structuring plant communities in both terrestrial and aquatic ecosystems, with variation in herbivory often being related to shifts between alternate states. On coral reefs, regional reductions in herbivores have underpinned shifts from coral to dominance by leathery macroalgae. These shifts appear difficult to reverse as these macroalgae are unpalatable to the majority of herbivores, and the macroalgae suppress the recruitment and growth of corals. The removal of macroalgae is, therefore, viewed as a key ecological process on coral reefs. On the Great Barrier Reef, Sargassum is a dominant macroalgal species following experimentally induced coral–macroalgal phase-shifts. We, therefore, used Sargassum assays and remote video cameras to directly quantify the species responsible for removing macroalgae across a range of coral reef habitats on Lizard Island, northern Great Barrier Reef. Despite supporting over 50 herbivorous fish species and six macroalgal browsing species, the video footage revealed that a single species, Naso unicornis, was almost solely responsible for the removal of Sargassum biomass across all habitats. Of the 42,246 bites taken from the Sargassum across all habitats, N. unicornis accounted for 89.8% (37,982) of the total bites, and 94.6% of the total mass standardized bites. This limited redundancy, both within and across local scales, underscores the need to assess the functional roles of individual species. Management and conservation strategies may need to look beyond the preservation of species diversity and focus on the maintenance of ecological processes and the protection of key species in critical functional groups.

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.

Suppression of herbivory by macroalgal density: a critical feedback on coral reefs?

Coral reefs globally are in decline, with some reefs undergoing phase shifts from coral-dominance to degraded states dominated by large fleshy macroalgae. These shifts have been underpinned by the overharvesting of herbivorous fishes and represent a fundamental change in the physical structure of these reefs. Although the physical structure provided by corals is regarded as a key feature that facilitates herbivore activity, the influence of the physical structure of macroalgal stands is largely unknown. Using transplanted Sargassum, the largest coral reef macroalga, we created habitat patches of predetermined macroalgal density (0.25-6.23 kg m(-2)). Remote video cameras revealed both grazing and browsing fishes avoided high density patches, preferring relatively open areas with low macroalgal cover. This behaviour may provide a positive feedback leading to the growth and persistence of macroalgal stands; increasing the stability of phase shifts to macroalgae.

Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs.

Around the globe, coral reefs and other marine ecosystems are increasingly overfished. Conventionally, studies of fishing impacts have focused on the population size and dynamics of targeted stocks rather than the broader ecosystem-wide effects of harvesting. Using parrotfishes as an example, we show how coral reef fish populations respond to escalating fishing pressure across the Indian and Pacific Oceans. Based on these fish abundance data, we infer the potential impact on four key functional roles performed by parrotfishes. Rates of bioerosion and coral predation are highly sensitive to human activity, whereas grazing and sediment removal are resilient to fishing. Our results offer new insights into the vulnerability and resilience of coral reefs to the ever-growing human footprint. The depletion of fishes causes differential decline of key ecosystem functions, radically changing the dynamics of coral reefs and setting the stage for future ecological surprises.

Consumer diversity interacts with prey defenses to drive ecosystem function.

Prey traits linking consumer diversity to ecosystem function remain poorly understood. On tropical coral reefs, herbivores promote coral dominance by suppressing competing macroalgae, but the roles of herbivore identity and diversity, macroalgal defenses, and their interactions in affecting reef resilience and function are unclear. We studied adjacent pairs of no-take marine reserves and fished areas on reefs in Fiji and found that protected reefs supported 7-17x greater biomass, 2-3x higher species richness of herbivorous fishes, and 3-11x more live coral cover than did fished reefs. In contrast, macroalgae were 27-61x more abundant and 3-4x more species-rich on fished reefs. When we transplanted seven common macroalgae from fished reefs into reserves they were rapidly consumed, suggesting that rates of herbivory (ecosystem functioning) differed inside vs. outside reserves. We then video-recorded feeding activity on the same seven macroalgae when transplanted into reserves, and assessed the functional redundancy vs. complementarity of herbivorous fishes consuming these macroalgae. Of 29 species of larger herbivorous fishes on these reefs, only four species accounted for 97% of macroalgal consumption. Two unicornfish consumed a range of brown macroalgae, a parrotfish consumed multiple red algae, and a rabbitfish consumed a green alga, with almost no diet overlap among these groups. The two most chemically rich, allelopathic algae were each consumed by a single, but different, fish species. This striking complementarity resulted from herbivore species differing in their tolerances to macroalgal chemical and structural defenses. A model of assemblage diet breadth based on our feeding observations predicted that high browser diversity would be required for effective control of macroalgae on Fijian reefs. In support of this model, we observed strong negative relationships between herbivore diversity and macroalgal abundance and diversity across the six study reefs. Our findings indicate that the total diet breadth of the herbivore community and the probability of all macroalgae being removed from reefs by herbivores increases with increasing herbivore diversity, but that a few critical species drive this relationship. Therefore, interactions between algal defenses and herbivore tolerances create an essential role for consumer diversity in the functioning and resilience of coral reefs.

Bright spots among the world’s coral reefs

Ongoing declines in the structure and function of the world’s coral reefs require novel approaches to sustain these ecosystems and the millions of people who depend on them. A presently unexplored approach that draws on theory and practice in human health and rural development is to systematically identify and learn from the ‘outliers’—places where ecosystems are substantially better (‘bright spots’) or worse (‘dark spots’) than expected, given the environmental conditions and socioeconomic drivers they are exposed to. Here we compile data from more than 2,500 reefs worldwide and develop a Bayesian hierarchical model to generate expectations of how standing stocks of reef fish biomass are related to 18 socioeconomic drivers and environmental conditions. We identify 15 bright spots and 35 dark spots among our global survey of coral reefs, defined as sites that have biomass levels more than two standard deviations from expectations. Importantly, bright spots are not simply comprised of remote areas with low fishing pressure; they include localities where human populations and use of ecosystem resources is high, potentially providing insights into how communities have successfully confronted strong drivers of change. Conversely, dark spots are not necessarily the sites with the lowest absolute biomass and even include some remote, uninhabited locations often considered near pristine. We surveyed local experts about social, institutional, and environmental conditions at these sites to reveal that bright spots are characterized by strong sociocultural institutions such as customary taboos and marine tenure, high levels of local engagement in management, high dependence on marine resources, and beneficial environmental conditions such as deep-water refuges. Alternatively, dark spots are characterized by intensive capture and storage technology and a recent history of environmental shocks. Our results suggest that investments in strengthening fisheries governance, particularly aspects such as participation and property rights, could facilitate innovative conservation actions that help communities defy expectations of global reef degradation.

Prevention of Hypertension in DOCA-Salt Rats by an Inhibitor of Soluble Epoxide Hydrolase

Cyclooxygenase and lipoxygenase metabolism of arachidonic acid produces compounds important in cardiovascular diovascular control. Further, arachidonic acid can be metabolised by cytochrome p450 to produce epoxyeicosatrienoic acids (EETs). These derivatives are inactivated by soluble epoxide hydrolase (sEH). The potential role of these EETs in hypertension and cardiac remodelling has been determined using the selective sEH inhibitor, N-adamantyl-N′-dodecylurea (ADU), in deoxycorticosterone acetate (DOCA)-salt hypertensive rats. Experiments were performed on male Wistar rats following uninephrectomy alone (UNX rats) or uninephrectomy with administration of DOCA (25 mg every fourth day subcutaneously) and 1% NaCl in drinking water (DOCA-salt rats). ADU (10 mg/kg/d subcutaneously) was administered for 2wk starting 2wk after surgery. Cardiovascular structure and function were determined using organ wet weights, histological analysis of collagen and inflammation, isolated heart and thoracic aortic ring preparation, and electrophysiological measurements. DOCA-salt hypertensive rats developed hypertension, hypertrophy, perivascular and interstitial fibrosis, endothelial dysfunction, and prolongation of the cardiac action potential duration within 4 wk. Administration of ADU prevented the further increase in systolic blood pressure and left-ventricular wet weight and normalized endothelial function. ADU treatment did not change inflammatory cell infiltration, collagen deposition, or cardiac action potential duration. EETs may be involved in the development of hypertension and endothelial dysfunction in DOCA-salt rats, but not in excessive collagen deposition or electrophysiological abnormalities.