Adrian C. Stier

The value of estuarine and coastal ecosystem services

The global decline in estuarine and coastal ecosystems (ECEs) is affecting a number of critical benefits, or ecosystem services. We review the main ecological services across a variety of ECEs, including marshes, mangroves, nearshore coral reefs, seagrass beds, and sand beaches and dunes. Where possible, we indicate estimates of the key economic values arising from these services, and discuss how the natural variability of ECEs impacts their benefits, the synergistic relationships of ECEs across seascapes, and management implications. Although reliable valuation estimates are beginning to emerge for the key services of some ECEs, such as coral reefs, salt marshes, and mangroves, many of the important benefits of seagrass beds and sand dunes and beaches have not been assessed properly. Even for coral reefs, marshes, and mangroves, important ecological services have yet to be valued reliably, such as cross-ecosystem nutrient transfer (coral reefs), erosion control (marshes), and pollution control (mangroves). An important issue for valuing certain ECE services, such as coastal protection and habitat–fishery linkages, is that the ecological functions underlying these services vary spatially and temporally. Allowing for the connectivity between ECE habitats also may have important implications for assessing the ecological functions underlying key ecosystems services, such coastal protection, control of erosion, and habitat–fishery linkages. Finally, we conclude by suggesting an action plan for protecting and/or enhancing the immediate and longer-term values of ECE services. Because the connectivity of ECEs across land–sea gradients also influences the provision of certain ecosystem services, management of the entire seascape will be necessary to preserve such synergistic effects. Other key elements of an action plan include further ecological and economic collaborative research on valuing ECE services, improving institutional and legal frameworks for management, controlling and regulating destructive economic activities, and developing ecological restoration options.

Order of arrival affects competition in two reef fishes

Many communities experience repeated periods of colonization due to seasonally regenerating habitats or pulsed arrival of young-of-year. When an individuals persistence in a community depends upon the strength of competitive interactions, changes in the timing of arrival relative to the arrival of a competitor can modify competitive strength and, ultimately, establishment in the community. We investigated whether the strength of intracohort competitive interactions between recent settlers of the reef fishes Thalassoma hardwicke and T. quinquevittatum are dependent on the sequence and temporal separation of their arrival into communities. To achieve this, we manipulated the sequence and timing of arrival of each species onto experimental patch reefs by simulating settlement pulses and monitoring survival and aggressive interactions. Both species survived best in the absence of competitors, but when competitors were present, they did best when they arrived at the same time. Survival declined as each species entered the community progressively later than its competitor and as aggression by its competitor increased. Intraspecific effects of resident T. hardwicke were similar to interspecific effects. This study shows that the strength of competition depends not only on the identity of competitors, but also on the sequence and timing of their interactions, suggesting that when examining interaction strengths, it is important to identify temporal variability in the direction and magnitude of their effects. Furthermore, our findings provide empirical evidence for the importance of competitive lotteries in the maintenance of species diversity in demographically open marine systems.

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.

Guard crabs alleviate deleterious effects of vermetid snails on a branching coral

Stony corals provide important structural habitat for microbes, invertebrates, and fishes, which in some cases has led to the evolution of beneficial interactions that may protect corals from environmental factors such as thermal stress, nutrient limitation, competitors, or predators. For example, guard crabs (Trapezia spp.) protect corals (Pocillopora sp.) from attacks by crown-of-thorn seastar and sedimentation. Here, a field experiment demonstrates that guard crabs (Trapezia serenei) also ameliorate the strong negative effects of the giant vermetid (Dendropoma maximum) on growth of Pocillopora. This experiment highlights the importance of this crab-coral mutualism: guard crabs facilitate the growth of corals in stressful environments (e.g., where vermetids are abundant), thereby preserving the ecological goods and services (e.g., food and shelter) that these corals may provide to other reef-associated species.

The influence of fundamental traits on mechanisms controlling appendage regeneration

One of the most compelling questions in evolutionary biology is why some animals can regenerate injured structures while others cannot. Appendage regeneration appears to be common when viewed across the metazoan phylogeny, yet this ability has been lost in many taxa to varying degrees. Within species, the capacity for regeneration also can vary ontogenetically among individuals. Here we argue that appendage regeneration along the secondary body axis may be constrained by fundamental traits such as body size, aging, life stage, and growth pattern. Studies of the molecular mechanisms affecting regeneration have been conducted primarily with small organisms at early life stages. Such investigations disregard the dramatic shifts in morphology and physiology that organisms undergo as they age, grow, and mature. To help explain interspecific and intraspecific constraints on regeneration, we link particular fundamental traits to specific molecular mechanisms that control regeneration. We present a new synthesis for how these fundamental traits may affect the molecular mechanisms of regeneration at the tissue, cellular, and genomic levels of biological organization. Future studies that explore regeneration in organisms across a broad phylogenetic scale, and within an ontogenetic framework, will help elucidate the proximate mechanisms that modulate regeneration and may reveal new biomedical applications for use in regenerative medicine.

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.

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.

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.

Experimentally induced metamorphosis in axolotls reduces regenerative rate and fidelity

Abstract While most tetrapods are unable to regenerate severed body parts, amphibians display a remarkable ability to regenerate an array of structures. Frogs can regenerate appendages as larva, but they lose this ability around metamorphosis. In contrast, salamanders regenerate appendages as larva, juveniles, and adults. However, the extent to which fundamental traits (e.g., metamorphosis, body size, aging, etc.) restrict regenerative ability remains contentious. Here we utilize the ability of normally paedomorphic adult axolotls (Ambystoma mexicanum) to undergo induced metamorphosis by thyroxine exposure to test how metamorphosis and body size affects regeneration in age‐matched paedomorphic and metamorphic individuals. We show that body size does not affect regeneration in adult axolotls, but metamorphosis causes a twofold reduction in regeneration rate, and lead to carpal and digit malformations. Furthermore, we find evidence that metamorphic blastemal cells may take longer to traverse the cell cycle and display a lower proliferative rate. This study identifies the axolotl as a powerful system to study how metamorphosis restricts regeneration independently of developmental stage, body size, and age; and more broadly how metamorphosis affects tissue‐specific changes.

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.