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The unique traits of large animals often allow them to fulfill functional roles in ecosystems that small animals cannot. However, large animals are also at greater risk from human activities. Thus, it is critical to understand how losing large animals impacts ecosystem function. In the oceans, selective fishing for large animals alters the demographics and size structure of numerous species. While the community-wide impacts of losing large animals are a major theme in terrestrial research, the ecological consequences of removing large animals from marine ecosystems remain understudied. Here, we combine survey data from 282 sites across the Caribbean with a field experiment to investigate how altering the size structure of parrotfish populations impacts coral reef communities. We show that Caribbean-wide, parrotfish populations are skewed toward smaller individuals, with fishes <11 cm in length comprising nearly 70% of the population in the most heavily fished locations vs. ~25% at minimally fished sites. Despite these differences in size structure, sites had similar overall parrotfish biomass. As a result, algal cover was unrelated to parrotfish biomass and instead, was negatively correlated with the density of large parrotfishes. To mechanistically explore how large parrotfishes shape benthic communities, we manipulated fishes' access to the benthos to create three distinct fish communities with different size structure. We found that excluding large or large and medium-sized parrotfishes did not alter overall parrotfish grazing rates but caused respective 4- and 10-fold increases in algal biomass. Unexpectedly, branching corals benefited from excluding large parrotfishes whereas the growth of mounding coral species was impaired. Similarly, removing large parrotfishes led to unexpected increases in coral recruitment that were absent when both large and medium bodied fishes were excluded. Our data highlight the unique roles of large parrotfishes in driving benthic dynamics on coral reefs and suggests that diversity of size is an important component of how herbivore diversity impacts ecosystem function on reefs. This study adds to a growing body of literature revealing the ecological ramifications of removing large animals from ecosystems and sheds new light on how fishing down the size structure of parrotfish populations alters functional diversity to reshape benthic reef communities.

Tropical reef fishes are widely regarded as being perhaps the most morphologically diverse vertebrate assemblage on earth, yet much remains to be discovered about the scope and patterns of this diversity. We created a morphospace of 2,939 species spanning 56 families of tropical Indo-Pacific reef fishes and established the primary axes of body shape variation, the phylogenetic consistency of these patterns, and whether dominant patterns of shape change can be accomplished by diverse underlying changes. Principal component analysis showed a major axis of shape variation that contrasts deep-bodied species with slender, elongate forms. Furthermore, using custom methods to compare the elongation vector (axis that maximizes elongation deformation) and the main vector of shape variation (first principal component) for each family in the morphospace, we showed that two thirds of the families diversify along an axis of body elongation. Finally, a comparative analysis using a principal coordinate analysis based on the angles among first principal component vectors of each family shape showed that families accomplish changes in elongation with a wide range of underlying modifications. Some groups such as Pomacentridae and Lethrinidae undergo decreases in body depth with proportional increases in all body regions, while other families show disproportionate changes in the length of the head (e.g., Labridae), the trunk or caudal region in all combinations (e.g., Pempheridae and Pinguipedidae). In conclusion, we found that evolutionary changes in body shape along an axis of elongation dominates diversification in reef fishes. Changes in shape on this axis are thought to have immediate implications for swimming performance, defense from gape limited predators, suction feeding performance and access to some highly specialized habitats. The morphological modifications that underlie changes in elongation are highly diverse, suggesting a role for a range of developmental processes and functional consequences.

It has become almost paradigmatic in the coral reef literature that fishing-induced reductions of parrotfish abundance cause benthic phase shifts from coral to macroalgal dominance. This study examined the alternatives of top-down control of the benthos by parrotfish density and bottom-up control of parrotfish density by the benthos at four Philippine islands in a long-term (7.5–30 years) “natural experiment”. No-take marine reserves (NTMRs) demonstrated that fishing reduced parrotfish density significantly at two islands (Sumilon, Mantigue), but not significantly at two other islands (Apo, Selinog). There was no evidence that cover of hard coral decreased, nor macroalgal cover increased, in fished areas relative to NTMRs, no evidence that parrotfish density affected hard coral cover significantly, and thus no evidence of top-down, fishing-induced benthic phase shifts at all four islands. There was, however, compelling evidence that benthos (cover of dead substrata and hard coral) exerted strong bottom-up control on parrotfish density. This bottom-up control was demonstrated most clearly by major environmental disturbances (e.g. typhoons, coral bleaching) that changed benthic habitat and, subsequently, parrotfish density. As hard coral cover declined (and cover of dead substratum increased), parrotfish density increased and vice versa. This response occurred in both major parrotfish feeding guilds (scrapers and excavators). This long-term study on heavily fished coral reefs suggests that the benthos drives the parrotfish, not the other way around. The paradigm of fishing-induced benthic phase shifts may not apply to all coral reefs at all times. Multiple drivers of benthic change on coral reefs should always be considered.

Phase shifts from hard coral to macroalgae have led to the formulation of a top-down herbivory paradigm, whose assumption is that a reduction in herbivory is the primary driver of these changes. Caribbean parrotfish from Scarus and Sparisoma genera are usually known as main reef herbivorous. Yet, they are a diverse group of organisms that perform multiple functions, including the bioerosion of reef structures. Generalizing functions at the group level likely explains why the direct effects of parrotfish on macroalgae regulation are not always evident. In this study, we tested the hypothesis that parrotfish potential functions are strongly linked to the habitat’s benthic characteristics. Furthermore, we expect that the parrotfish bioerosion potential will be highly sensitive to changes in benthic conditions, while herbivory will be more robust. We conducted in situ benthic and parrotfish surveys across the diverse reefscape of the remote Alacranes Reef, the most extensive system in the Gulf of Mexico. Both bioerosion and herbivory potential were highest in the most complex and structured sites, while only macroalgae removal was high in deep low-coral cover sites dominated by fleshy macroalgae. Interestingly, both functions were highly diminished in shallow and reticulated inner reefs dominated by turf algae and cyanobacteria, suggesting that even the herbivory function can be depleted under unfavorable benthic conditions. Our findings highlight the need to reconsider parrotfish management strategies to account for the specific roles of different species and consider reciprocal benthic-fish interactions.

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.

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 7-17× greater biomass, 2-3× higher species richness of herbivorous fishes, and 3-11× more live coral cover than did fished reefs. In contrast, macroalgae were 27-61× more abundant and 3-4× 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.

Human activities and land-use drivers combine in complex ways to affect coral reef health and, in turn, the diversity and abundance of reef fauna. Here we examine the impacts of different marine protected area (MPA) types, and various human and habitat drivers, on resource fish functional groups (i.e., total fish, herbivore, grazer, scraper, and browser biomass) along the 180 km west coast of Hawaii Island. Across survey years from 2008 to 2018, we observed an overall decrease in total fish biomass of 45%, with similar decreases in biomass seen across most fish functional groups. MPAs that prohibited a combination of lay nets, aquarium collection, and spear fishing were most effective in maintaining and/or increasing fish biomass across all functional groups. We also found that pollution, fishing, and habitat drivers all contributed to changes in total fish biomass, where the most negative impact was nitrogen input from land-based sewage disposal. Fish biomass relationships with our study drivers depended on fish functional grouping. For surgeonfish (grazers), changes in biomass linked most strongly to changes in reef rugosity. For parrotfish (scrapers), biomass was better explained by changes in commercial catch where current commercial fishing levels are negatively affecting scraper populations. Our observations suggest that regional management of multiple factors, including habitat, pollution, and fisheries, will benefit resource fish biomass off Hawaii Island.

A fundamental goal in ecology is to understand the role of consumers in top-down (TD) and bottom-up (BU) processes that affect the functioning of ecosystems. Consumers ingest organic matter and excrete inorganic nutrients, and individual roles are influenced by body size and functional identity. Our study quantifies how alterations to herbivore assemblages affect both TD and BU processes on coral reefs in the South Pacific. We collected empirical data on consumption and nutrient excretion rates from 300 individual herbivorous fishes belonging to five functional groups. Individual-level traits were then scaled to a 13-year time series of fish populations from reefs that have either shifted to algal dominance or remained in the coral state. Large excavating parrotfishes and other herbivores on reefs in the coral state contributed 43% more herbivory and excreted nutrients at a higher ratio of N:P than herbivores on algal-dominated reefs; both processes may benefit coral health. Algal-dominated reefs experienced 56% higher rates of detritivory by large detritivorous fishes that remove detritus from algal surfaces, a process that may facilitate algal dominance. By scaling individual-level traits to population time series, our study provides a framework to quantify how changes to consumer assemblages impact both TD and BU processes across ecosystems undergoing change. Identifying the unique roles of consumers in processes that maintain and reinforce ecosystem states is the key to predicting the importance of shifts in diverse consumer assemblages.

Environmental stress impedes predation and herbivory by limiting the ability of animals to search for and consume prey. We tested the contingency of this relationship on consumer traits and specifically hypothesized that herbivore mobility relative to the return time of limiting environmental stress would predict consumer effects. We examined how wave-induced water motion affects marine communities via herbivory by highly mobile (fish) vs. slow-moving (pencil urchin) consumers at two wave-sheltered and two wave-exposed rocky subtidal locations in the Galapagos Islands. The exposed locations experienced 99th percentile flow speeds that were 2–5 times greater than sheltered locations, with mean flow speeds >33 cm/s vs. <16 cm/s, 2–7 times higher standing macroalgal cover and 2–3 times lower cover of crustose coralline algae than the sheltered locations. As predicted by the environmental stress hypothesis (ESH), there was a negative relationship between mean flow speed and urchin abundance and herbivory rates on Ulva spp. algal feeding assays. In contrast, the biomass of surgeonfishes (Acanthuridae) and parrotfishes (Labridae: Scarinae) was positively correlated with mean flow speed. Ulva assays were consumed at equal rates by fish at exposed and sheltered locations, indicating continued herbivory even when flow speeds surpassed maximum reported swimming speeds at a rate of 1–2 times per minute. Modeled variation in fish species richness revealed minimal effects of diversity on herbivory rates at flow speeds <40 cm/s, when all species were capable of foraging, and above 120 cm/s, when no species could forage, while increasing diversity maximized herbivory rates at flow speeds of 40–120 cm/s. Two-month herbivore exclusion experiments during warm and cool seasons revealed that macroalgal biomass was positively correlated with flow speed. Fish limited macroalgal development by 65–91% at one exposed location but not the second and by 70% at the two sheltered locations. In contrast, pencil urchins did not affect algal communities at either exposed location, but reduced macroalgae by 87% relative to controls at both sheltered locations. We propose an extension of the ESH that is contingent upon mobility to explain species-specific changes in feeding rates and consumer effects on benthic communities across environmental gradients.

Continuing coral-reef degradation in the western Atlantic is resulting in loss of ecological and geologic functions of reefs. With the goal of assisting resource managers and stewards of reefs in setting and measuring progress toward realistic goals for coral-reef conservation and restoration, we examined reef degradation in this region from a geological perspective. The importance of ecosystem services provided by coral reefs—as breakwaters that dissipate wave energy and protect shorelines and as providers of habitat for innumerable species—cannot be overstated. However, the few coral species responsible for reef building in the western Atlantic during the last approximately 1.5 million years are not thriving in the 21st century. These species are highly sensitive to abrupt temperature extremes, prone to disease infection, and have low sexual reproductive potential. Their vulnerability and the low functional redundancy of branching corals have led to the low resilience of western Atlantic reef ecosystems. The decrease in live coral cover over the last 50 years highlights the need for study of relict (senescent) reefs, which, from the perspective of coastline protection and habitat structure, may be just as important to conserve as the living coral veneer. Research is needed to characterize the geological processes of bioerosion, reef cementation, and sediment transport as they relate to modern-day changes in reef elevation. For example, although parrotfish remove nuisance macroalgae, possibly promoting coral recruitment, they will not save Atlantic reefs from geological degradation. In fact, these fish are quickly nibbling away significant quantities of Holocene reef framework. The question of how different biota covering dead reefs affect framework resistance to biological and physical erosion needs to be addressed. Monitoring and managing reefs with respect to physical resilience, in addition to ecological resilience, could optimize the expenditure of resources in conserving Atlantic reefs and the services they provide. La degradación continua de los arrecifes de coral en el Atlántico oeste está resultando en la pérdida de las funciones ecológicas y geológicas de los arrecifes. Con el objetivo de asistir a los administradores de los recursos y de los arrecifes en el establecimiento y medida del progreso hacia metas realistas para la conservación y restauración de los arrecifes de coral, examinamos la degradación de los arrecifes en esta región desde una perspectiva geológica. La importancia de los servicios ambientales proporcionados por los arrecifes de coral - como rompeolas que disipan la fuerza de las olas y protegen las líneas de costa y como proveedores de hábitat para innumerables especies - no puede ser exagerada. Sin embargo, las pocas especies de coral responsables de la construcción de arrecifes en el Atlántico oeste durante aproximadamente los últimos 1.5 millones de años no están prosperando en el siglo XXI. Estas especies son altamente sensibles a los extremos abruptos de temperatura, propensas a las enfermedades infecciosas y tienen un potencial bajo de reproducción sexual. Su vulnerabilidad y la baja redundancia funcional de los corales que forman ramas han llevado a la baja resiliencia de los ecosistemas arrecifales del Atlántico oeste. La disminución en la cobertura de coral vivo en los últimos 50 años resalta la necesidad de estudios sobre los arrecifes relictos (senescentes), los cuales desde la perspectiva de la protección de la línea costera y la estructura del hábitat, pueden ser igual de importantes de conservar que la capa de corales vivientes. Se necesitan investigaciones para caracterizar los procesos geológicos de bioerosión, cementación de arrecifes y transporte de sedimentos conforme se relacionan a los cambios contemporáneos en la elevación de los arrecifes. Por ejemplo, aunque el pez loro (familia Scaridae) remueva macroalgas pesadas, lo que posiblemente promueva el reclutamiento de coral, no va a salvar a los arrecifes del Atlántico de la degradación geológica. De hecho, estos peces están mordisqueando rápidamente cantidades significativas de marco de trabajo sobre arrecifes del Holoceno. La pregunta de cómo la biota diferente que cubre los arrecifes muertos afecta al marco de trabajo sobre resistencia a la erosión física y biológica necesita ser atendida. El monitoreo y el manejo de los arrecifes con respecto a la resiliencia física, además de la resiliencia ecológica, podrían optimizar el gasto de los recursos para la conservación de los arrecifes del Atlántico y los servicios que proporcionan.