Thomas C. Adam

Herbivory, Connectivity, and Ecosystem Resilience: Response of a Coral Reef to a Large-Scale Perturbation

Coral reefs world-wide are threatened by escalating local and global impacts, and some impacted reefs have shifted from coral dominance to a state dominated by macroalgae. Therefore, there is a growing need to understand the processes that affect the capacity of these ecosystems to return to coral dominance following disturbances, including those that prevent the establishment of persistent stands of macroalgae. Unlike many reefs in the Caribbean, over the last several decades, reefs around the Indo-Pacific island of Moorea, French Polynesia have consistently returned to coral dominance following major perturbations without shifting to a macroalgae-dominated state. Here, we present evidence of a rapid increase in populations of herbivorous fishes following the most recent perturbation, and show that grazing by these herbivores has prevented the establishment of macroalgae following near complete loss of coral on offshore reefs. Importantly, we found the positive response of herbivorous fishes to increased benthic primary productivity associated with coral loss was driven largely by parrotfishes that initially recruit to stable nursery habitat within the lagoons before moving to offshore reefs later in life. These results underscore the importance of connectivity between the lagoon and offshore reefs for preventing the establishment of macroalgae following disturbances, and indicate that protecting nearshore nursery habitat of herbivorous fishes is critical for maintaining reef resilience.

Resource partitioning along multiple niche axes drives functional diversity in parrotfishes on Caribbean coral reefs

The recent loss of key consumers to exploitation and habitat degradation has significantly altered community dynamics and ecosystem function across many ecosystems worldwide. Predicting the impacts of consumer losses requires knowing the level of functional diversity that exists within a consumer assemblage. In this study, we document functional diversity among nine species of parrotfishes on Caribbean coral reefs. Parrotfishes are key herbivores that facilitate the maintenance and recovery of coral-dominated reefs by controlling algae and provisioning space for the recruitment of corals. We observed large functional differences among two genera of parrotfishes that were driven by differences in diet. Fishes in the genus Scarus targeted filamentous algal turf assemblages, crustose coralline algae, and endolithic algae and avoided macroalgae, while fishes in the genus Sparisoma preferentially targeted macroalgae. However, species with similar diets were dissimilar in other attributes, including the habitats they frequented, the types of substrate they fed from, and the spatial scale at which they foraged. These differences indicate that species that appear to be functionally redundant when looking at diet alone exhibit high levels of complementarity when we consider multiple functional traits. By identifying key functional differences among parrotfishes, we provide critical information needed to manage parrotfishes to enhance the resilience of coral-dominated reefs and reverse phase shifts on algal-dominated reefs throughout the wider Caribbean. Further, our study provides a framework for predicting the impacts of consumer losses in other species rich ecosystems.

How will coral reef fish communities respond to climate-driven disturbances? Insight from landscape-scale perturbations

Global climate change is rapidly altering disturbance regimes in many ecosystems including coral reefs, yet the long-term impacts of these changes on ecosystem structure and function are difficult to predict. A major ecosystem service provided by coral reefs is the provisioning of physical habitat for other organisms, and consequently, many of the effects of climate change on coral reefs will be mediated by their impacts on habitat structure. Therefore, there is an urgent need to understand the independent and combined effects of coral mortality and loss of physical habitat on reef-associated biota. Here, we use a unique series of events affecting the coral reefs around the Pacific island of Moorea, French Polynesia to differentiate between the impacts of coral mortality and the degradation of physical habitat on the structure of reef fish communities. We found that, by removing large amounts of physical habitat, a tropical cyclone had larger impacts on reef fish communities than an outbreak of coral-eating sea stars that caused widespread coral mortality but left the physical structure intact. In addition, the impacts of declining structural complexity on reef fish assemblages accelerated as structure became increasingly rare. Structure provided by dead coral colonies can take up to decades to erode following coral mortality, and, consequently, our results suggest that predictions based on short-term studies are likely to grossly underestimate the long-term impacts of coral decline on reef fish communities.

Ecology and Evolution Affect Network Structure in an Intimate Marine Mutualism

Elucidating patterns and causes of interaction among mutualistic species is a major focus of ecology, and recent meta-analyses of terrestrial networks show that network-level reciprocal specialization tends to be higher in intimate mutualisms than in nonintimate mutualisms. It is largely unknown, however, whether this pattern holds for and what factors affect specialization in marine mutualisms. Here we present the first analysis of network specialization () for marine mutualistic networks. Specialization among eight Indo-Pacific networks of obligate mutualistic gobies and shrimps was indistinguishable from that among comparably intimate terrestrial mutualisms (ants-myrmecophytes) and higher than that among nonintimate ones (seed dispersers). Specialization was affected by variability in habitat use for both gobies and shrimps and by phylogenetic history for shrimps. Habitat use was phylogenetically conserved among shrimp, and thus effects of shrimp phylogeny on partner choice were mediated in part by habitat. By contrast, habitat use and pairing patterns in gobies were not related to phylogenetic history. This asymmetry appears to result from evolutionary constraints on partner use in shrimps and convergence among distantly related gobies to utilize burrows provided by multiple shrimp species. Results indicate that the evolution of mutualism is affected by life-history characteristics that transcend environments and that different factors constrain interactions in disparate ecosystems.

Competition encourages cooperation: client fish receive higher-quality service when cleaner fish compete

Partner choice is likely to be an important mechanism for the maintenance of cooperation in many mutualisms, and cleaner mutualisms among fish have been a model system for testing predictions of partner choice theories. Fish seeking to be cleaned (clients) face two potential problems: cleaners may cheat them by feeding on tissue or mucous, and they may have to wait for service from a cleaner. Previous work on interactions between the bluestreak cleaner wrasse, Labroides dimidiatus, and its clients indicates that cleaners provide higher-quality service to species that have the option of switching partners. These results have been interpreted as evidence that partner choice leads cleaners to behave cooperatively; however, alternative explanations exist for these between-species patterns. Here I focus on interactions between the bluestreak cleaner wrasse and a single client species that varies in its ability to switch partners to test the prediction that clients receive higher-quality service when cleaners have to compete for access to them. The results indicate that cleaners give ornate butterflyfish, Chaetodon ornatissimus, priority of access to their services when these clients can switch partners; however, ornate butterflyfish are not cheated less often when they have access to multiple cleaner stations, and they frequently respond to cheating by aggressively chasing cleaners. In combination with previous work, these results indicate that partner choice influences cooperative interactions between bluestreak cleaner wrasse and their clients, but that some clients with the ability to switch partners may use other strategies (i.e. punishment) to limit cheating by cleaners.

High-quality habitat and facilitation ameliorate competitive effects of prior residents on new settlers

Many species disperse during their lifetime. Two factors that can affect the performance of individuals following dispersal are the presence of conspecifics and intrinsic habitat quality at the settlement site. Detecting the influence of these factors can be difficult for at least two reasons: (1) the outcomes of interactions with conspecifics are often variable including both competition and facilitation, and (2) selection of high quality habitats often leads to positive covariance between habitat quality and density. In this study, I investigate positive and negative effects of resident blue streak cleaner wrasse (Labroides dimidiatus) on the growth and survival of recently settled conspecifics while accounting for habitat quality. Juvenile L. dimidiatus settle near adult conspecifics, but likely have to compete with resident adults for access to food. However, field experiments indicate that settlers have access to more resources at occupied sites, and as a result, grow faster despite evidence for competition with residents. This result is a direct consequence of two factors: (1) resident conspecifics facilitate settlers by attracting client fish, and (2) resident conspecifics are strongly associated with high quality habitat. These results highlight the need to simultaneously consider habitat quality and competitive and facilitative interactions between conspecifics when making inferences about ecological processes from spatial patterns of individual performance.

Coral Reef Resilience, Tipping Points and the Strength of Herbivory

Coral reefs increasingly are undergoing transitions from coral to macroalgal dominance. Although the functional roles of reef herbivores in controlling algae are becoming better understood, identifying possible tipping points in the herbivory-macroalgae relationships has remained a challenge. Assessment of where any coral reef ecosystem lies in relation to the coral-to-macroalgae tipping point is fundamental to understanding resilience properties, forecasting state shifts, and developing effective management practices. We conducted a multi-year field experiment in Moorea, French Polynesia to estimate these properties. While we found a sharp herbivory threshold where macroalgae escape control, ambient levels of herbivory by reef fishes were well above that needed to prevent proliferation of macroalgae. These findings are consistent with previously observed high resilience of the fore reef in Moorea. Our approach can identify vulnerable coral reef systems in urgent need of management action to both forestall shifts to macroalgae and preserve properties essential for resilience.

Recruitment Drives Spatial Variation in Recovery Rates of Resilient Coral Reefs

Tropical reefs often undergo acute disturbances that result in landscape-scale loss of coral. Due to increasing threats to coral reefs from climate change and anthropogenic perturbations, it is critical to understand mechanisms that drive recovery of these ecosystems. We explored this issue on the fore reef of Moorea, French Polynesia, following a crown-of-thorns seastar outbreak and cyclone that dramatically reduced cover of coral. During the five-years following the disturbances, the rate of re-establishment of coral cover differed systematically around the triangular-shaped island; coral cover returned most rapidly at sites where the least amount of live coral remained after the disturbances. Although sites differed greatly in the rate of return of coral, all showed at least some evidence of re-assembly to their pre-disturbance community structure in terms of relative abundance of coral taxa and other benthic space holders. The primary driver of spatial variation in recovery was recruitment of sexually-produced corals; subsequent growth and survivorship were less important in shaping the spatial pattern. Our findings suggest that, although the coral community has been resilient, some areas are unlikely to attain the coral cover and taxonomic structure they had prior to the most recent disturbances before the advent of another landscape-scale perturbation.

Phylogeny and character evolution in the Indo-Pacific genus Ctenogobiops (Gobiiformes: Gobiidae)

Ctenogobiops is a genus of Indo-Pacific gobies that form obligate, mutualistic associations with shrimp in the genus Alpheus. This study provides a molecular phylogenetic analysis of eight Ctenogobiops species: C. aurocingulus, C. crocineus, C. feroculus, C. formosa, C. maculosus, C. mitodes, C. tangaroai, and C. tongaensis. We recover two clades within the genus, one consisting of C. feroculus and C. aurocingulus, the second including the remaining species arrayed as follows: (C. tongaensis (C. mitodes (C. formosa (C. maculosus (C. crocineus, C. tangaroai))))). Recovery of C. maculosus and C. crocineus as distinct taxa suggests that these species are not synonymous, although sampling in this study is limited. Species of Ctenogobiops are morphologically very similar to each other, with generally consistent meristic character states present throughout the genus. Recognition of species is based primarily on slight variations in color pattern, shape of the dorsal fin, and size of the gill opening. Comparison of our specimens of C. mitodes with accounts of C. pomastictus confirms that color pattern variations and lateral scale counts are more reliable indicators of species identity than relative dorsal fin spine length, particularly for smaller specimens. We evaluate the distribution of morphological characters in the context of the new phylogenetic hypothesis, and provide a summary of distinguishing characters for Ctenogobiops species. In this case, as in other instances of diverse reef-dwelling fish taxa, molecular data are ideal for inferring phylogenetic relationships, whereas morphological data remain the most expedient way to identify species.

The importance of individual and species-level traits for trophic niches among herbivorous coral reef fishes

Resolving how species compete and coexist within ecological communities represents a long-standing challenge in ecology. Research efforts have focused on two predominant mechanisms of species coexistence: complementarity and redundancy. But findings also support an alternative hypothesis that within-species variation may be critical for coexistence. Our study focuses on nine closely related and ecologically similar coral reef fish species to test the importance of individual- versus species-level traits in determining the size of dietary, foraging substrate, and behavioural interaction niches. Specifically, we asked: (i) what level of biological organization best describes individual-level niches? and (ii) how are herbivore community niches partitioned among species, and are niche widths driven by species- or individual-level traits? Dietary and foraging substrate niche widths were best described by species identity, but no level of taxonomy explained behavioural interactions. All three niches were dominated by only a few species, contrasting expectations of niche complementarity. Species- and individual-level traits strongly drove foraging substrate and behavioural niches, respectively, whereas the dietary niche was described by both. Our findings underscored the importance of species-level traits for community-level niches, but highlight that individual-level trait variation within a select few species may be a key driver of the overall size of niches.