Yves-Marie Bozec

Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp

Significance Most studies of the impact of global warming focus on the direct physiological impacts of climate change. However, global warming is shifting the distribution of many species and leading to novel interactions between previously separated species that have the potential to transform entire ecological communities. This study shows that an increase in the proportion of warmwater species (“tropicalization”) as oceans warm is increasing fish herbivory in kelp forests, contributing to their decline and subsequent persistence in alternate “kelp-free” states. These tropical and subtropical herbivores are increasingly impacting temperate algal communities worldwide, posing a significant threat to the long-term stability of these iconic ecosystems and the valuable services they provide. Some of the most profound effects of climate change on ecological communities are due to alterations in species interactions rather than direct physiological effects of changing environmental conditions. Empirical evidence of historical changes in species interactions within climate-impacted communities is, however, rare and difficult to obtain. Here, we demonstrate the recent disappearance of key habitat-forming kelp forests from a warming tropical–temperate transition zone in eastern Australia. Using a 10-y video dataset encompassing a 0.6 °C warming period, we show how herbivory increased as kelp gradually declined and then disappeared. Concurrently, fish communities from sites where kelp was originally abundant but subsequently disappeared became increasingly dominated by tropical herbivores. Feeding assays identified two key tropical/subtropical herbivores that consumed transplanted kelp within hours at these sites. There was also a distinct increase in the abundance of fishes that consume epilithic algae, and much higher bite rates by this group at sites without kelp, suggesting a key role for these fishes in maintaining reefs in kelp-free states by removing kelp recruits. Changes in kelp abundance showed no direct relationship to seawater temperatures over the decade and were also unrelated to other measured abiotic factors (nutrients and storms). Our results show that warming-mediated increases in fish herbivory pose a significant threat to kelp-dominated ecosystems in Australia and, potentially, globally.

The Ecological Role of Sharks on Coral Reefs.

Sharks are considered the apex predator of coral reefs, but the consequences of their global depletion are uncertain. Here we explore the ecological roles of sharks on coral reefs and, conversely, the importance of reefs for sharks. We find that most reef-associated shark species do not act as apex predators but instead function as mesopredators along with a diverse group of reef fish. While sharks perform important direct and indirect ecological roles, the evidence to support hypothesised shark-driven trophic cascades that benefit corals is weak and equivocal. Coral reefs provide some functional benefits to sharks, but sharks do not appear to favour healthier reef environments. Restoring populations of sharks is important and can yet deliver ecological surprise.

Synergistic impacts of global warming on the resilience of coral reefs

Recent epizootics have removed important functional species from Caribbean coral reefs and left communities vulnerable to alternative attractors. Global warming will impact reefs further through two mechanisms. A chronic mechanism reduces coral calcification, which can result in depressed somatic growth. An acute mechanism, coral bleaching, causes extreme mortality when sea temperatures become anomalously high. We ask how these two mechanisms interact in driving future reef state (coral cover) and resilience (the probability of a reef remaining within a coral attractor). We find that acute mechanisms have the greatest impact overall, but the nature of the interaction with chronic stress depends on the metric considered. Chronic and acute stress act additively on reef state but form a strong synergy when influencing resilience by intensifying a regime shift. Chronic stress increases the size of the algal basin of attraction (at the expense of the coral basin), whereas coral bleaching pushes the system closer to the algal attractor. Resilience can change faster—and earlier—than a change in reef state. Therefore, we caution against basing management solely on measures of reef state because a loss of resilience can go unnoticed for many years and then become disproportionately more difficult to restore.

Tradeoffs between fisheries harvest and the resilience of coral reefs

Significance Fisheries management must avoid adverse impacts on the ecosystem. Doing so can be challenging in highly complex systems, particularly if the target species serves an important ecosystem function. Caribbean coral reefs provide a classic example in which herbivorous parrotfish are both an important fishery and key driver of ecosystem resilience. We developed and tested a multispecies fisheries model of parrotfish and linked it to a coral reef ecosystem experiencing climate change. We found that corals can remain resilient if less than 10% of the fishable parrotfish biomass is harvested and a minimum size of 30 cm is implemented. To our knowledge, this work is the first attempt to identify harvest levels that have little adverse effect on corals. Many countries are legally obliged to embrace ecosystem-based approaches to fisheries management. Reductions in bycatch and physical habitat damage are now commonplace, but mitigating more sophisticated impacts associated with the ecological functions of target fisheries species are in their infancy. Here we model the impacts of a parrotfish fishery on the future state and resilience of Caribbean coral reefs, enabling us to view the tradeoff between harvest and ecosystem health. We find that the implementation of a simple and enforceable size restriction of >30 cm provides a win:win outcome in the short term, delivering both ecological and fisheries benefits and leading to increased yield and greater coral recovery rate for a given harvest rate. However, maintaining resilient coral reefs even until 2030 requires the addition of harvest limitations (<10% of virgin fishable biomass) to cope with a changing climate and induced coral disturbances, even in reefs that are relatively healthy today. Managing parrotfish is not a panacea for protecting coral reefs but can play a role in sustaining the health of reefs and high-quality habitat for reef fisheries.

Characterizing the ecological trade‐offs throughout the early ontogeny of coral recruitment

Drivers of recruitment in sessile marine organisms are often poorly understood, due to the rapidly changing requirements experienced during early ontogeny. The complex suite of physical, biological, and ecological interactions beginning at larval settlement involves a series of trade-offs that influence recruitment success. For example, while cryptic settlement within complex microhabitats is a commonly observed phenomenon in sessile marine organisms, it is unclear whether trade-offs between competition in cryptic refuges and predation on exposed surfaces leads to higher recruitment.To explore the trade-offs during the early ontogeny of scleractinian corals, we combined field observations with laboratory and field experiments to develop a mechanistic understanding of coral recruitment success. Multiple experiments conducted over 15 months in Palau (Micronesia) allowed a mechanistic approach to study the individual factors involved in recruitment: settlement behavior, growth, competition, and predation, as functions of microhabitat and ontogeny. We finally developed and tested a predictive recruitment model with the broader aim of testing whether our empirical insights explained patterns of coral recruitment and quantifying the relative importance of each trade-off.Coral settlement was higher in crevices than exposed microhabitats, but post-settlement bottlenecks differed markedly in the presence (uncaged) and absence (caged) of predators. Incidental predation by herbivores on exposed surfaces at early post-settlement (<3 mm) stages and targeted predation by corallivores at late post-settlement (3–10 mm) stages exceeded competition in crevices as major drivers of mortality. In contrast, when fish were excluded, competition with macroalgae and heterotrophic invertebrates intensified mortality, particularly in crevices. As a result, post-settlement trade-offs were reversed, and recruitment was more than twofold higher on exposed surfaces than crevices. Once post-settlement bottlenecks were overcome, survival was higher on exposed surfaces regardless of fish exclusion. However, maximum recruitment occurred in crevices of uncaged treatments, being ninefold higher than caged treatments. Overall, we characterize recruitment success throughout the earliest life-history stages of corals and uncover some intriguing trade-offs between growth, competition and predation, highlighting how these change and even reverse during ontogeny and under alternate disturbance regimes.

Multiple Stressors and the Functioning of Coral Reefs

Coral reefs provide critical services to coastal communities, and these services rely on ecosystem functions threatened by stressors. By summarizing the threats to the functioning of reefs from fishing, climate change, and decreasing water quality, we highlight that these stressors have multiple, conflicting effects on functionally similar groups of species and their interactions, and that the overall effects are often uncertain because of a lack of data or variability among taxa. The direct effects of stressors on links among functional groups, such as predator-prey interactions, are particularly uncertain. Using qualitative modeling, we demonstrate that this uncertainty of stressor impacts on functional groups (whether they are positive, negative, or neutral) can have significant effects on models of ecosystem stability, and reducing uncertainty is vital for understanding changes to reef functioning. This review also provides guidance for future models of reef functioning, which should include interactions among functional groups and the cumulative effect of stressors.

A coral-algal phase shift in Mesoamerica not driven by changes in herbivorous fish abundance

Coral-algal phase shifts in which coral cover declines to low levels and is replaced by algae have often been documented on coral reefs worldwide. This has motivated coral reef management responses that include restriction and regulation of fishing, e.g. herbivorous fish species. However, there is evidence that eutrophication and sedimentation can be at least as important as a reduction in herbivory in causing phase shifts. These threats arise from coastal development leading to increased nutrient and sediment loads, which stimulate algal growth and negatively impact corals respectively. Here, we first present results of a dynamic process-based model demonstrating that in addition to overharvesting of herbivorous fish, bottom-up processes have the potential to precipitate coral-algal phase shifts on Mesoamerican reefs. We then provide an empirical example that exemplifies this on coral reefs off Mahahual in Mexico, where a shift from coral to algal dominance occurred over 14 years, during which there was little change in herbivore biomass but considerable development of tourist infrastructure. Our results indicate that coastal development can compromise the resilience of coral reefs and that watershed and coastal zone management together with the maintenance of functional levels of fish herbivory are critical for the persistence of coral reefs in Mesoamerica.

Use of timed automata and model-checking to explore scenarios on ecosystem models

The interest to build ecosystem models is well acknowledged in order to improve the understanding of the sophisticated linkages between humans and natural species embedded within variable local and global environmental contexts. It is especially true when a complex temporal evolution intervenes as in population regulations. Ecological modellers usually resort to numerical models supported by accurate data and extensive knowledge on biological processes. Unfortunately, the task becomes more difficult to model ecosystems with limited data and knowledge. Qualitative models may be more suitable for designing data-poor systems in a decision-aid context. We propose a new qualitative approach for ecosystem modelling based on timed automata (TA) formalism combined with a high-level query language for exploring scenarios. TA rely on a discrete-event system formalism to reproduce the temporal dynamics of a system. Combined with model-checking techniques, TA enable the exploration of system properties in response to a wide range of scenarios based on a temporal logic. Our applicative case concerns the evolution of different fish biomass along time according to fishing policies, especially when exogenous environmental issues may also be considered. We have developed this approach to model a simplified marine ecosystem subject to different fishing policies. Using predefined query patterns, we show that TA and model-checking are relevant tools to query timed properties of a fishery system in response to different management options. This modelling approach may be especially useful for fostering better discussion among all stakeholders involved in fisheries management.

Asymmetric competition prevents the outbreak of an opportunistic species after coral reef degradation

Disturbance releases space and allows the growth of opportunistic species, excluded by the old stands, with a potential to alter community dynamics. In coral reefs, abundances of fast-growing, and disturbance-tolerant sponges are expected to increase and dominate as space becomes available following acute coral mortality events. Yet, an increase in abundance of these opportunistic species has been reported in only a few studies, suggesting certain mechanisms may be acting to regulate sponge populations. To gain insights into mechanisms of population control, we simulated the dynamics of the common reef-excavating sponge Cliona tenuis in the Caribbean using an individual-based model. An orthogonal hypothesis testing approach was used, where four candidate mechanisms—algal competition, stock-recruitment limitation, whole and partial mortality—were incorporated sequentially into the model and the results were tested against independent field observations taken over a decade in Belize, Central America. We found that releasing space after coral mortality can promote C. tenuis outbreaks, but such outbreaks can be curtailed by macroalgal competition. The asymmetrical competitive superiority of macroalgae, given by their capacity to pre-empt space and outcompete with the sponge in a size-dependant fashion, supports their capacity to steal the opportunity from other opportunists. While multiple system stages can be expected in coral reefs following intense perturbation macroalgae may prevent the growth of other space-occupiers, such as bioeroding sponges, under low grazing pressure.

Reassessing shark-driven trophic cascades on coral reefs: a reply to Ruppert et al

In our recent review of the ecological roles of sharks on coral reefs [1], we concluded that the evidence to support hypothesised shark-driven trophic cascades on coral reefs was weak and equivocal. In their response to our review, Ruppert et al. [2] assert that a major issue with our approach was that we primarily reviewed evidence from correlative observational studies to reach this conclusion. This is incorrect, because our conclusion is based upon multiple lines of evidence, including observational studies, food-web models, dietary and stable isotope analysis, trophic position, habitat use, and behavioural evidence [1].