Variation in body size drives spatial and temporal variation in lobster-urchin interaction strength.

How strongly predators and prey interact is both notoriously context dependent and difficult to measure. Yet across taxa, interaction strength is strongly related to predator size, prey size and prey density, suggesting that general cross-taxonomic relationships could be used to predict how strongly individual species interact. Here, we ask how accurately do general size-scaling relationships predict variation in interaction strength between specific species that vary in size and density across space and time? To address this question, we quantified the size and density dependence of the functional response of the California spiny lobster Panulirus interruptus, foraging on a key ecosystem engineer, the purple sea urchin Strongylocentrotus purpuratus, in experimental mesocosms. Based on these results, we then estimated variation in lobster-urchin interaction strength across five sites and 9 years of observational data. Finally, we compared our experimental estimates to predictions based on general size-scaling relationships from the literature. Our results reveal that predator and prey body size has the greatest effect on interaction strength when prey abundance is high. Due to consistently high urchin densities in the field, our simulations suggest that body size-relative to density-accounted for up to 87% of the spatio-temporal variation in interaction strength. However, general size-scaling relationships failed to predict the magnitude of interactions between lobster and urchin; even the best prediction from the literature was, on average, an order of magnitude (+18.7×) different than our experimental predictions. Harvest and climate change are driving reductions in the average body size of many marine species. Anticipating how reductions in body size will alter species interactions is critical to managing marine systems in an ecosystem context. Our results highlight the extent to which differences in size-frequency distributions can drive dramatic variation in the strength of interactions across narrow spatial and temporal scales. Furthermore, our work suggests that species-specific estimates for the scaling of interaction strength with body size, rather than general size-scaling relationships, are necessary to quantitatively predict how reductions in body size will alter interaction strengths.

Avoiding critical thresholds through effective monitoring.

A major challenge in sustainability science is identifying targets that maximize ecosystem benefits to humanity while minimizing the risk of crossing critical system thresholds. One critical threshold is the biomass at which populations become so depleted that their population growth rates become negative-depensation. Here, we evaluate how the value of monitoring information increases as a natural resource spends more time near the critical threshold. This benefit emerges because higher monitoring precision promotes higher yield and a greater capacity to recover from overharvest. We show that precautionary buffers that trigger increased monitoring precision as resource levels decline may offer a way to minimize monitoring costs and maximize profits. In a world of finite resources, improving our understanding of the trade-off between precision in estimates of population status and the costs of mismanagement will benefit stakeholders that shoulder the burden of these economic and social costs.

Remoteness does not enhance coral reef resilience.

Remote coral reefs are thought to be more resilient to climate change due to their isolation from local stressors like fishing and pollution. We tested this hypothesis by measuring the relationship between local human influence and coral community resilience. Surprisingly, we found no relationship between human influence and resistance to disturbance and some evidence that areas with greater human development may recover from disturbance faster than their more isolated counterparts. Our results suggest remote coral reefs are imperiled by climate change, like so many other geographically isolated ecosystems, and are unlikely to serve as effective biodiversity arks. Only drastic and rapid cuts in greenhouse gas emissions will ensure coral survival. Our results also indicate that some reefs close to large human populations were relatively resilient. Focusing research and conservation resources on these more accessible locations has the potential to provide new insights and maximize conservation outcomes.

Fertilization by coral-dwelling fish promotes coral growth but can exacerbate bleaching response.

Many corals form close associations with a diverse assortment of coral-dwelling fishes and other fauna. As coral reefs around the world are increasingly threatened by mass bleaching events, it is important to understand how these biotic interactions influence corals' susceptibility to bleaching. We used dynamic energy budget modeling to explore how nitrogen excreted by coral-dwelling fish affects the physiological performance of host corals. In our model, fish presence influenced the functioning of the coral-Symbiodiniaceae symbiosis by altering nitrogen availability, and the magnitude and sign of these effects depended on environmental conditions. Although our model predicted that fish-derived nitrogen can promote coral growth, the relationship between fish presence and coral tolerance of photo-oxidative stress was non-linear. Fish excretions supported denser symbiont populations that provided protection from incident light through self-shading. However, these symbionts also used more of their photosynthetic products for their own growth, rather than sharing with the coral host, putting the coral holobiont at a higher risk of becoming carbon-limited and bleaching. The balance between the benefits of increased symbiont shading and costs of reduced carbon sharing depended on environmental conditions. Thus, while there were some scenarios under which fish presence increased corals' tolerance of light stress, fish could also exacerbate bleaching and slow or prevent subsequent recovery. We discuss how the contrast between the potentially harmful effects of fish predicted by our model and results of empirical studies may relate to key model assumptions that warrant further investigation. Overall, this study provides a foundation for future work on how coral-associated fauna influence the bioenergetics of their host corals, which in turn has implications for how these corals respond to bleaching-inducing stressors.

Ecological impacts of human-induced animal behaviour change.

A growing body of literature has documented myriad effects of human activities on animal behaviour, yet the ultimate ecological consequences of these behavioural shifts remain largely uninvestigated. While it is understood that, in the absence of humans, variation in animal behaviour can have cascading effects on species interactions, community structure and ecosystem function, we know little about whether the type or magnitude of human-induced behavioural shifts translate into detectable ecological change. Here we synthesise empirical literature and theory to create a novel framework for examining the range of behaviourally mediated pathways through which human activities may affect different ecosystem functions. We highlight the few empirical studies that show the potential realisation of some of these pathways, but also identify numerous factors that can dampen or prevent ultimate ecosystem consequences. Without a deeper understanding of these pathways, we risk wasting valuable resources on mitigating behavioural effects with little ecological relevance, or conversely mismanaging situations in which behavioural effects do drive ecosystem change. The framework presented here can be used to anticipate the nature and likelihood of ecological outcomes and prioritise management among widespread human-induced behavioural shifts, while also suggesting key priorities for future research linking humans, animal behaviour and ecology.

Predation and landscape characteristics independently affect reef fish community organization.

Trophic island biogeography theory predicts that the effects of predators on prey diversity are context dependent in heterogeneous landscapes. Specifically, models predict that the positive effect of habitat area on prey diversity should decline in the presence of predators, and that predators should modify the partitioning of alpha and beta diversity across patchy landscapes. However, experimental tests of the predicted context dependency in top-down control remain limited. Using a factorial field experiment we quantify the effects of a focal predatory fish species (grouper) and habitat characteristics (patch size, fragmentation) on the partitioning of diversity and assembly of coral reef fish communities. We found independent effects of groupers and patch characteristics on prey communities. Groupers reduced prey abundance by 50% and gamma diversity by 45%, with a disproportionate removal of rare species relative to common species (64% and 36% reduction, respectively; an oddity effect). Further, there was a 77% reduction in beta diversity. Null model analysis demonstrated that groupers increased the importance of stochastic community assembly relative to patches without groupers. With regard to patch size, larger patches contained more fishes, but a doubling of patch size led to a modest (36%) increase in prey abundance. Patch size had no effect on prey diversity; however, fragmented patches had 50% higher species richness and modified species composition relative to unfragmented patches. Our findings suggest two different pathways (i.e., habitat or predator shifts) by which natural and/or anthropogenic processes can drive variation in fish biodiversity and community assembly.

How fishes and invertebrates impact coral resilience.

Increasingly intense and frequent ocean heatwaves are causing widespread coral mortality. These heatwaves are just one of the many stressors - among for instance ocean acidification, nutrient pollution and destructive fishing practices - that have caused widespread decline of coral reefs over the past century. This destruction of reefs threatens the remarkable biodiversity of organisms that depend upon coral reefs. However, recent research suggests that many of the fishes and invertebrates that inhabit coral reefs may play an underappreciated role in influencing the resistance and recovery of corals to stressors, especially those caused by global climate change such as ocean heatwaves. Unraveling the threads that link these coral inhabitants to the corals' response to stressors has the potential to weave a more comprehensive model of resilience that integrates the plight of coral reefs with the breathtaking diversity of life they host. Here, we aim to elucidate the critical roles that coral-associated fishes and invertebrates play in mediating coral resilience to environmental stressors. By integrating recent research findings, we aim to showcase how these often-overlooked organisms influence coral resilience in the face of climate change.

Coral guard crabs.

Adrian Stier and Craig Osenberg introduce Trapeziid crabs, which live in close symbiosis with corals.

Predator density and timing of arrival affect reef fish community assembly.

Most empirical studies of predation use simple experimental approaches to quantify the effects of predators on prey (e.g., using constant densities of predators, such as ambient vs. zero). However, predator densities vary in time, and these effects may not be well represented by studies that use constant predator densities. Although studies have independently examined the importance of predator density, temporal variability, and timing of arrival (i.e., early or late relative to prey), the relative contribution of these different predator regimes on prey abundance, diversity, and composition remains poorly understood. The hawkfish (Paracirrhites arcatus), a carnivorous coral reef fish, exhibits substantial variability in patch occupancy, density, and timing of arrival to natural reefs. Our field experiments demonstrated that effects of hawkfish on prey abundance depended on both hawkfish density and the timing of their arrival, but not on variability in hawkfish density. Relative to treatments without hawkfish, hawkfish presence reduced prey abundance by 50%. This effect increased with a doubling of hawkfish density (an additional 33% reduction), and when hawkfish arrived later during community development (a 34% reduction). Hawkfish did not affect within-patch diversity (species richness), but they increased between-patch diversity (beta) based on species incidence (22%), and caused shifts in species composition. Our results suggest that the timing of predator arrival can be as important as predator density in modifying prey abundance and community composition.

Material legacies can degrade resilience: Structure-retaining disturbances promote regime shifts on coral reefs.

Standing dead structures of habitat-forming organisms (e.g., dead trees, coral skeletons, oyster shells) killed by a disturbance are material legacies that can affect ecosystem recovery processes. Many ecosystems are subject to different types of disturbance that either remove biogenic structures or leave them intact. Here we used a mathematical model to quantify how the resilience of coral reef ecosystems may be differentially affected following structure-removing and structure-retaining disturbance events, focusing in particular on the potential for regime shifts from coral to macroalgae. We found that dead coral skeletons could substantially diminish coral resilience if they provided macroalgae refuge from herbivory, a key feedback associated with the recovery of coral populations. Our model shows that the material legacy of dead skeletons broadens the range of herbivore biomass over which coral and macroalgae states are bistable. Hence, material legacies can alter resilience by modifying the underlying relationship between a system driver (herbivory) and a state variable (coral cover).

Emergent effects of multiple predators on prey survival: the importance of depletion and the functional response.

The combined effects of multiple predators often cannot be predicted from their independent effects. Emergent multiple predator effects (MPEs) include risk enhancement, where combined predators kill more prey than predicted by their individual effects, and risk reduction, where fewer prey are killed than predicted. Current methods for detecting MPEs are biased because they assume linear functional responses and/or no prey depletion. As a result, past studies overestimated the occurrence of risk enhancement for additive designs, and tended to overestimate the occurrence of risk reduction for substitutive designs. Characterising the predators' functional responses and accounting for prey depletion reduces biases in detection, estimation, interpretation and generalisation of the emergent effects of predator diversity on prey survival. These findings have implications beyond MPE's and should be considered in all studies aimed at understanding how multiple factors combine when demographic rates are density dependent.

Multiple defender effects: synergistic coral defense by mutualist crustaceans.

The majority of our understanding of mutualisms comes from studies of pairwise interactions. However, many hosts support mutualist guilds, and interactions among mutualists make the prediction of aggregate effects difficult. Here, we apply a factorial experiment to interactions of 'guard' crustaceans that defend their coral host from seastar predators. Predation was reduced by the presence of mutualists (15% reduction in predation frequency and 45% in volume of coral consumed). The frequency of attacks with both mutualists was lower than with a single species, but it did not differ significantly from the expected frequency of independent effects. In contrast, the combined defensive efficacy of both mutualist species reduced the volume of coral tissue lost by 73%, significantly more than the 38% reduction expected from independent defensive efforts, suggesting the existence of a cooperative synergy in defensive behaviors of 'guard' crustaceans. These emergent 'multiple defender effects' are statistically and ecologically analogous to the emergent concept of 'multiple predator effects' known from the predation literature.

Detrital supply suppresses deforestation to maintain healthy kelp forest ecosystems.

Herbivores can reach extraordinary abundances in many ecosystems. When herbivore abundance is high, heavy grazing can severely defoliate primary producers and, in some cases, even drive ecosystem to undergo regime shifts from a high productivity state to a denuded, low productivity state. While the phenomenon of herbivore-driven regime shifts is well documented, we only partially understand the mechanisms underlying these events. Here, we combine herbivory experiments with 21 years of long-term monitoring data of kelp forest ecosystems to test the hypothesis that herbivores drive regime shifts when herbivory exceeds primary production. To test this hypothesis, we quantified how the foraging habits of an important group of marine herbivores-sea urchins-change with increases in sea urchin biomass and trigger regime shifts to a foundation species, giant kelp (Macrocystis pyrifera). Using experiments, we quantified how the grazing capacity of urchins increases as urchin biomass increases, then we combined these estimates of urchin grazing capacity with estimates of kelp production to predict when and where urchin grazing capacity exceeded kelp production. When grazing capacity exceeded kelp production, sea urchins caused a 50-fold reduction in giant kelp biomass. Our findings support the hypothesis that the balance between herbivory and production underlies herbivore-driven regime shifts in Southern California kelp forests and provides insight into when and where urchins are likely to force regime shifts in kelp forest ecosystems.

Glimmers of hope in large carnivore recoveries.

In the face of an accelerating extinction crisis, scientists must draw insights from successful conservation interventions to uncover promising strategies for reversing broader declines. Here, we synthesize cases of recovery from a list of 362 species of large carnivores, ecologically important species that function as terminal consumers in many ecological contexts. Large carnivores represent critical conservation targets that have experienced historical declines as a result of direct exploitation and habitat loss. We examine taxonomic and geographic variation in current extinction risk and recovery indices, identify conservation actions associated with positive outcomes, and reveal anthropogenic threats linked to ongoing declines. We find that fewer than 10% of global large carnivore populations are increasing, and only 12 species (3.3%) have experienced genuine improvement in extinction risk, mostly limited to recoveries among marine mammals. Recovery is associated with species legislation enacted at national and international levels, and with management of direct exploitation. Conversely, ongoing declines are robustly linked to threats that include habitat modification and human conflict. Applying lessons from cases of large carnivore recovery will be crucial for restoring intact ecosystems and maintaining the services they provide to humans.

Evidence that spillover from Marine Protected Areas benefits the spiny lobster (Panulirus interruptus) fishery in southern California.

Marine Protected Areas (MPAs) are designed to enhance biodiversity and ecosystem services. Some MPAs are also established to benefit fisheries through increased egg and larval production, or the spillover of mobile juveniles and adults. Whether spillover influences fishery landings depend on the population status and movement patterns of target species both inside and outside of MPAs, as well as the status of the fishery and behavior of the fleet. We tested whether an increase in the lobster population inside two newly established MPAs influenced local catch, fishing effort, and catch-per-unit-effort (CPUE) within the sustainable California spiny lobster fishery. We found greater build-up of lobsters within MPAs relative to unprotected areas, and greater increases in fishing effort and total lobster catch, but not CPUE, in fishing zones containing MPAs vs. those without MPAs. Our results show that a 35% reduction in fishing area resulting from MPA designation was compensated for by a 225% increase in total catch after 6-years, thus indicating at a local scale that the trade-off of fishing ground for no-fishing zones benefitted the fishery.

Variation in disturbance to a foundation species structures the dynamics of a benthic reef community.

Disturbance and foundation species can both have strong impacts on ecosystem structure and function, but studies of their interacting effects are hindered by the long life spans and slow growth of most foundation species. Here, we investigated the extent to which foundation species may mediate the impacts of disturbance on ecological communities, using the kelp forest ecosystem as a study system. Giant kelp (Macrocystis pyrifera) grows rapidly and experiences wave disturbance from winter storms. We developed and analyzed a model of the effects of variable storm regimes on giant kelp population dynamics and of the cascading effects on kelp-mediated competition between benthic community members in kelp forests. Simulations of severe storm regimes resulted in a greater abundance of understory macroalgae and a lower abundance of sessile invertebrates than did milder regimes. Both the cascading effects of periodic loss of giant kelp as well as the degree to which storms directly impacted the benthos (in the form of scouring) influenced the outcome of competition between benthic community members. The model's qualitative predictions were consistent with empirical data from a 20-yr time series of community dynamics, suggesting that interannual variability in disturbance that affects giant kelp abundance can have strong consequences for benthic community structure. Our findings point to the value of long-term studies in elucidating the interacting effects of disturbance and foundation species.

Propagule redirection: habitat availability reduces colonization and increases recruitment in reef fishes.

Increased habitat availability or quality can alter production of habitat-dependent organisms in two contrasting ways: (1) by enhancing input of new colonists to the new sites (the Field-of-Dreams Hypothesis); and (2) by drawing colonists away from existing sites (the Propagule Redirection Hypothesis), and thus reducing the deleterious effects of density. We conducted a field experiment on coral reef fishes in Moorea, French Polynesia, to quantify how differing levels of habitat availability (controlling for quality) increased and/or redirected colonizing larval fish. Focal reefs without neighboring reefs received two to four times more settlers than reefs with adjacent habitat, demonstrating that increased habitat redirected larval fish. At the scale of the entire reef array, total colonization increased 1.3-fold in response to a sixfold increase in reef area (and a 2.75-fold increase in adjusted habitat availability). Thus, propagules were both increased and redirected, a result midway between the Field-of-Dreams and Propagule Redirection Hypotheses. A recruitment model using our data and field estimates of density-dependent recruitment predicts that habitat addition increases recruitment primarily by ameliorating the negative effects of competition at existing sites rather than increasing colonization at the new sites per se. Understanding long-term implications of these effects depends upon the interplay among habitat dynamics, population connectivity, colonization dynamics, and density dependence.

Synthesizing mechanisms of density dependence in reef fishes: behavior, habitat configuration, and observational scale.

Coral and rocky reef fish populations are widely used as model systems for the experimental exploration of density-dependent vital rates, but patterns of density-dependent mortality in these systems are not yet fully understood. In particular, the paradigm for strong, directly density-dependent (DDD) postsettlement mortality stands in contrast to recent evidence for inversely density-dependent (IDD) mortality. We review the processes responsible for DDD and IDD per capita mortality in reef fishes, noting that the pattern observed depends on predator and prey behavior, the spatial configuration of the reef habitat, and the spatial and temporal scales of observation. Specifically, predators tend to produce DDD prey mortality at their characteristic spatial scale of foraging, but prey mortality is IDD at smaller spatial scales due to attack-abatement effects (e.g., risk dilution). As a result, DDD mortality may be more common than IDD mortality on patch reefs, which tend to constrain predator foraging to the same scale as prey aggregation, eliminating attack-abatement effects. Additionally, adjacent groups of prey on continuous reefs may share a subset of refuges, increasing per capita refuge availability and relaxing DDD mortality relative to prey on patch reefs, where the patch edge could prevent such refuge sharing. These hypotheses lead to a synthetic framework to predict expected mortality patterns for a variety of scenarios. For nonsocial, nonaggregating species and species that aggregate in order to take advantage of spatially clumped refuges, IDD mortality is possible but likely superseded by DDD refuge competition, especially on patch reefs. By contrast, for species that aggregate socially, mortality should be IDD at the scale of individual aggregations but DDD at larger scales. The results of nearly all prior reef fish studies fit within this framework, although additional work is needed to test many of the predicted outcomes. This synthesis reconciles some apparent contradictions in the recent reef fish literature and suggests the importance of accounting for the scale-sensitive details of predator and prey behavior in any study system.

The vermetid gastropod Dendropoma maximum reduces coral growth and survival.

Coral reefs are one of the most diverse systems on the planet; yet, only a small fraction of coral reef species have attracted scientific study. Here, we document strong deleterious effects of an often overlooked species-the vermetid gastropod, Dendropoma maximum-on growth and survival of reef-building corals. Our surveys of vermetids on Moorea (French Polynesia) revealed a negative correlation between the density of vermetids and the per cent cover of live coral. Furthermore, the incidence of flattened coral growth forms was associated with the presence of vermetids. We transplanted and followed the fates of focal colonies of four species of corals on natural reefs where we also manipulated presence/absence of vermetids. Vermetids reduced skeletal growth of focal corals by up to 81 per cent and survival by up to 52 per cent. Susceptibility to vermetids varied among coral species, suggesting that vermetids could shift coral community composition. Our work highlights the potential importance of a poorly studied gastropod to coral dynamics.