Seagrass production around artificial reefs is resistant to human stressors.

Primary production underpins most ecosystem services, including carbon sequestration and fisheries. Artificial reefs (ARs) are widely used for fisheries management. Research has shown that a mechanism by which ARs in seagrass beds can support fisheries and carbon sequestration is through increasing primary production via fertilization from aggregating fish excretion. Seagrass beds are heavily affected by anthropogenic nutrient input and fishing that reduces nutrient input by consumers. The effect of these stressors is difficult to predict because impacts of simultaneous stressors are typically non-additive. We used a long-term experiment to identify the mechanisms by which simultaneous impacts of sewage enrichment and fishing alter seagrass production around ARs across non-orthogonal gradients in human-dominated and relatively unimpacted regions in Haiti and The Bahamas. Merging trait-based measures of seagrass and seagrass ecosystem processes, we found that ARs consistently enhanced per capita seagrass production and maintained ecosystem-scale production despite drastic shifts in controls on production from human stressors. Importantly, we also show that coupled human stressors on seagrass production around ARs were additive, contrasting expectations. These findings are encouraging for conservation because they indicate that seagrass ecosystems are highly resistant to coupled human stressors and that ARs promote ecosystem services even in human-dominated ecosystems.

The natural capital of seagrass beds in the Caribbean: evaluating their ecosystem services and blue carbon trade potential.

Seagrass beds provide tremendous services to society, including the storage of carbon, with important implications for climate change mitigation. Prioritizing conservation of this valuable natural capital is of global significance, and including seagrass beds in global carbon markets through projects that minimize loss, increase area or restore degraded areas represents a mechanism towards this end. Using newly available Caribbean seagrass distribution data, we estimated carbon storage in the region and calculated economic valuations of total ecosystem services and carbon storage. We estimated the 88 170 km2 of seagrass in the Caribbean stores 1337.8 (360.5-2335.0, minimum and maximum estimates, respectively) Tg carbon. The value of these seagrass ecosystems in terms of total ecosystem services and carbon alone was estimated to be $255 billion yr-1 and $88.3 billion, respectively, highlighting their potential monetary importance for the region. Our results show that Caribbean seagrass beds are globally substantial pools of carbon, and our findings underscore the importance of such evaluation schemes to promote urgently needed conservation of these highly threatened and globally important ecosystems.

Mechanistic support for increased primary production around artificial reefs.

Understanding factors controlling primary production is fundamental for the protection, management, and restoration of ecosystems. Tropical seagrass ecosystems are among the most productive ecosystems worldwide, yielding tremendous services for society. Yet they are also among the most impaired from anthropogenic stressors, prompting calls for ecosystem-based restoration approaches. Artificial reefs (ARs) are commonly applied in coastal marine ecosystems to rebuild failing fisheries and have recently gained attention for their potential to promote carbon sequestration. Nutrient hotspots formed via excretion from aggregating fishes have been empirically shown to enhance local primary production around ARs in seagrass systems. Yet, if and how increased local production affects primary production at ecosystem scale remains unclear, and empirical tests are challenging. We used a spatially explicit individual-based simulation model that combined a data-rich single-nutrient primary production model for seagrass and bioenergetics models for fish to test how aggregating fish on ARs affect seagrass primary production at patch and ecosystem scales. Specifically, we tested how the aggregation of fish alters (i) ecosystem seagrass primary production at varying fish densities and levels of ambient nutrient availability and (ii) the spatial distribution of seagrass primary production. Comparing model ecosystems with equivalent nutrient levels, we found that when fish aggregate around ARs, ecosystem-scale primary production is enhanced synergistically. This synergistic increase in production was caused by nonlinear dynamics associated with nutrient uptake and biomass allocation that enhances aboveground primary production more than belowground production. Seagrass production increased near the AR and decreased in areas away from the AR, despite marginal reductions in seagrass biomass at the ecosystem level. Our simulation's findings that ARs can increase ecosystem production provide novel support for ARs in seagrass ecosystems as an effective means to promote (i) fishery restoration (increased primary production can increase energy input to the food web) and (ii) carbon sequestration, via higher rates of primary production. Although our model represents a simplified, closed seagrass system without complex trophic interactions, it nonetheless provides an important first step in quantifying ecosystem-level implications of ARs as a tool for ecological restoration.

Rewiring coral: Anthropogenic nutrients shift diverse coral-symbiont nutrient and carbon interactions toward symbiotic algal dominance.

Improving coral reef conservation requires heightened understanding of the mechanisms by which coral cope with changing environmental conditions to maintain optimal health. We used a long-term (10 month) in situ experiment with two phylogenetically diverse scleractinians (Acropora palmata and Porites porites) to test how coral-symbiotic algal interactions changed under real-world conditions that were a priori expected to be beneficial (fish-mediated nutrients) and to be harmful, but non-lethal, for coral (fish + anthropogenic nutrients). Analyzing nine response variables of nutrient stoichiometry and stable isotopes per coral fragment, we found that nutrients from fish positively affected coral growth, and moderate doses of anthropogenic nutrients had no additional effects. While growing, coral maintained homeostasis in their nutrient pools, showing tolerance to the different nutrient regimes. Nonetheless, structural equation models revealed more nuanced relationships, showing that anthropogenic nutrients reduced the diversity of coral-symbiotic algal interactions and caused nutrient and carbon flow to be dominated by the symbiont. Our findings show that nutrient and carbon pathways are fundamentally "rewired" under anthropogenic nutrient regimes in ways that could increase corals' susceptibility to further stressors. We hypothesize that our experiment captured coral in a previously unrecognized transition state between mutualism and antagonism. These findings highlight a notable parallel between how anthropogenic nutrients promote symbiont dominance with the holobiont, and how they promote macroalgal dominance at the coral reef scale. Our findings suggest more realistic experimental conditions, including studies across gradients of anthropogenic nutrient enrichment as well as the incorporation of varied nutrient and energy pathways, may facilitate conservation efforts to mitigate coral loss.

Anthropogenic versus fish-derived nutrient effects on seagrass community structure and function.

Humans are altering nutrient dynamics through myriad pathways globally. Concurrent with the addition of nutrients via municipal, industrial, and agricultural sources, widespread consumer exploitation is changing consumer-mediated nutrient dynamics drastically. Thus, altered nutrient dynamics can occur through changes in the supply of multiple nutrients, as well as through changes in the sources of these nutrients. Seagrass ecosystems are heavily impacted by human activities, with highly altered nutrient dynamics from multiple causes. We simulate scenarios of altered nutrient supply and ratios, nitrogen:phosphorus (N:P), from two nutrient sources in seagrass ecosystems: anthropogenic fertilizer and fish excretion. In doing so we tested expectations rooted in ecological theory that suggest the importance of resource dynamics for predicting primary producer dynamics. Ecosystem functions were strongly altered by artificial fertilizer (e.g., seagrass growth increased by as much as 140%), whereas plant/algae community structure was most affected by fish-mediated nutrients or the interaction of both treatments (e.g., evenness increased by ~140% under conditions of low fish nutrients and high anthropogenic nutrients). Interactions between the nutrient sources were found for only two of six response variables, and the ratio of nutrient supply was the best predictor for only one response. These findings show that seagrass structure and function are well predicted by supply of a single nutrient (either N or P). Importantly, no single nutrient best explained the majority of responses-measures of community structure were best explained by the primary limiting nutrient to this system (P), whereas measures of growth and density of the dominant producer in the system were best explained by N. Thus, while our findings support aspects of theoretical expectations, the complexity of producer community responses belies broad generalities, underscoring the need to manage for multiple simultaneous nutrients in these imperiled coastal ecosystems.

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.

Animal pee in the sea: consumer-mediated nutrient dynamics in the world's changing oceans.

Humans have drastically altered the abundance of animals in marine ecosystems via exploitation. Reduced abundance can destabilize food webs, leading to cascading indirect effects that dramatically reorganize community structure and shift ecosystem function. However, the additional implications of these top-down changes for biogeochemical cycles via consumer-mediated nutrient dynamics (CND) are often overlooked in marine systems, particularly in coastal areas. Here, we review research that underscores the importance of this bottom-up control at local, regional, and global scales in coastal marine ecosystems, and the potential implications of anthropogenic change to fundamentally alter these processes. We focus attention on the two primary ways consumers affect nutrient dynamics, with emphasis on implications for the nutrient capacity of ecosystems: (1) the storage and retention of nutrients in biomass, and (2) the supply of nutrients via excretion and egestion. Nutrient storage in consumer biomass may be especially important in many marine ecosystems because consumers, as opposed to producers, often dominate organismal biomass. As for nutrient supply, we emphasize how consumers enhance primary production through both press and pulse dynamics. Looking forward, we explore the importance of CDN for improving theory (e.g., ecological stoichiometry, metabolic theory, and biodiversity-ecosystem function relationships), all in the context of global environmental change. Increasing research focus on CND will likely transform our perspectives on how consumers affect the functioning of marine ecosystems.

Consistent nutrient storage and supply mediated by diverse fish communities in coral reef ecosystems.

Corals thrive in low nutrient environments and the conservation of these globally imperiled ecosystems is largely dependent on mitigating the effects of anthropogenic nutrient enrichment. However, to better understand the implications of anthropogenic nutrients requires a heightened understanding of baseline nutrient dynamics within these ecosystems. Here, we provide a novel perspective on coral reef nutrient dynamics by examining the role of fish communities in the supply and storage of nitrogen (N) and phosphorus (P). We quantified fish-mediated nutrient storage and supply for 144 species and modeled these data onto 172 fish communities (71 729 individual fish), in four types of coral reefs, as well as seagrass and mangrove ecosystems, throughout the Northern Antilles. Fish communities supplied and stored large quantities of nutrients, with rates varying among ecosystem types. The size structure and diversity of the fish communities best predicted N and P supply and storage and N : P supply, suggesting that alterations to fish communities (e.g., overfishing) will have important implications for nutrient dynamics in these systems. The stoichiometric ratio (N : P) for storage in fish mass (~8 : 1) and supply (~20 : 1) was notably consistent across the four coral reef types (but not seagrass or mangrove ecosystems). Published nutrient enrichment studies on corals show that deviations from this N : P supply ratio may be associated with poor coral fitness, providing qualitative support for the hypothesis that corals and their symbionts may be adapted to specific ratios of nutrient supply. Consumer nutrient stoichiometry provides a baseline from which to better understand nutrient dynamics in coral reef and other coastal ecosystems, information that is greatly needed if we are to implement more effective measures to ensure the future health of the world's oceans.

Consumers regulate nutrient limitation regimes and primary production in seagrass ecosystems.

Consumer-mediated nutrient supply is increasingly recognized as an important functional process in many ecosystems. Yet, experimentation at relevant spatial and temporal scales is needed to fully integrate this bottom-up pathway into ecosystem models. Artificial reefs provide a unique approach to explore the importance of consumer nutrient supply for ecosystem function in coastal marine environments. We used bioenergetics models to estimate community-level nutrient supply by fishes, and relevant measures of primary production, to test the hypothesis that consumers, via excretion of nutrients, can enhance primary production and alter nutrient limitation regimes for two dominant primary producer groups (seagrass and benthic microalgae) around artificial reefs. Both producer groups demonstrated marked increases in production, as well as shifts in nutrient limitation regimes, with increased fish-derived nutrient supply. Individuals from the two dominant functional feeding groups (herbivores and mesopredators) supplied nutrients at divergent rates and ratios from one another, underscoring the importance of community structure for nutrient supply to primary producers. Our findings demonstrate that consumers, through an underappreciated bottom-up mechanism in marine environments, can alter nutrient limitation regimes and primary production, thereby fundamentally affecting the way these ecosystems function.

Thresholds of ecosystem response to nutrient enrichment from fish aggregations.

Biogeochemical hotspots can be driven by aggregations of animals, via excretion, that provide a concentrated source of limiting nutrients for primary producers. In a subtropical seagrass ecosystem, we characterized thresholds of ecological change associated with such hotspots surrounding artificial reef habitats. We deployed reefs of three sizes to aggregate fishes at different densities (and thus different levels of nutrient supply via excretion) and examined seagrass characteristics that reflect ecosystem processes. Responses varied as a function of reef size, with higher fish densities (on larger reefs) associated with more distinct ecological thresholds. For example, adjacent to larger reefs, the percentage of P content (%P) of seagrass (Thalassia testudinum) blades was significantly higher than background concentrations; fish densities on smaller reefs were insufficient to support sharp transitions in %P. Blade height was the only variable characterized by thresholds adjacent to smaller reefs, but lower fish densities (and hence, nutrient input) on smaller reefs were not sufficient for luxury nutrient storage by seagrass. Identifying such complexities in ecological thresholds is crucial for characterizing the extent to which biogeochemical hotspots may influence ecosystem function at a landscape scale.

Water column contributions to coral reef productivity: overcoming challenges of context dependence.

Coral reefs are declining at an unprecedented rate. Effective management and conservation initiatives necessitate improved understanding of the drivers of production because the high rates found in these ecosystems are the foundation of the many services they provide. The water column is the nexus of coral reef ecosystem dynamics, and functions as the interface through which essentially all energy and nutrients are transferred to fuel both new and recycled production. Substantial research has described many aspects of water column dynamics, often focusing on specific components because water column dynamics are highly spatially and temporally context dependent. Although necessary, a cost of this approach is that these dynamics are often not well linked to the broader ecosystem or across systems. To help overcome the challenge of context dependence, we provide a comprehensive review of this literature, and synthesise it through the perspective of ecosystem ecology. Specifically, we provide a framework to organise the drivers of temporal and spatial variation in production dynamics, structured around five primary state factors. These state factors are used to deconstruct the environmental contexts in which three water column sub-food webs mediate 'new' and 'recycled' production. We then highlight critical pathways by which global change drivers are altering coral reefs via the water column. We end by discussing four key knowledge gaps hindering understanding of the role of the water column for mediating coral reef production, and how overcoming these could improve conservation and management strategies. Throughout, we identify areas of extensive research and those where studies remain lacking and provide a database of 84 published studies. Improved integration of water column dynamics into models of coral reef ecosystem function is imperative to achieve the understanding of ecosystem production necessary to develop effective conservation and management strategies needed to stem global coral loss.

Fish community structure and dynamics are insufficient to mediate coral resilience.

Coral reefs are being impacted by myriad stressors leading to drastic changes to their structure and function. Fishes play essential roles in driving ecosystem processes on coral reefs but the extent to which these processes are emergent at temporal or ecosystem scales or otherwise masked by other drivers (for example, climatic events and crown-of-thorns starfish outbreaks) is poorly understood. Using time series data on fish community composition and coral and macroalgae percentage cover between 2006 and 2017 from 57 sites around Mo'orea, Polynesia, we found that fish community diversity predicts temporal stability in fish biomass but did not translate to temporal stability of coral cover. Furthermore, we found limited evidence of directional influence of fish on coral dynamics at temporal and ecosystem scales and no evidence that fish mediate coral recovery rate from disturbance. Our findings suggest that coral reef fisheries management will benefit from maintaining fish diversity but that this level of management is unlikely to strongly mediate coral loss or recovery over time.

Biological trade-offs underpin coral reef ecosystem functioning.

Human impact increasingly alters global ecosystems, often reducing biodiversity and disrupting the provision of essential ecosystem services to humanity. Therefore, preserving ecosystem functioning is a critical challenge of the twenty-first century. Coral reefs are declining worldwide due to the pervasive effects of climate change and intensive fishing, and although research on coral reef ecosystem functioning has gained momentum, most studies rely on simplified proxies, such as fish biomass. This lack of quantitative assessments of multiple process-based ecosystem functions hinders local and regional conservation efforts. Here we combine global coral reef fish community surveys and bioenergetic models to quantify five key ecosystem functions mediated by coral reef fishes. We show that functions exhibit critical trade-offs driven by varying community structures, such that no community can maximize all functions. Furthermore, functions are locally dominated by few species, but the identity of dominant species substantially varies at the global scale. In fact, half of the 1,110 species in our dataset are functionally dominant in at least one location. Our results reinforce the need for a nuanced, locally tailored approach to coral reef conservation that considers multiple ecological functions beyond the effect of standing stock biomass.

Marine fisheries declines viewed upside down: human impacts on consumer-driven nutrient recycling.

We quantified how two human impacts (overfishing and habitat fragmentation) in nearshore marine ecosystems may affect ecosystem function by altering the role of fish as nutrient vectors. We empirically quantified size-specific excretion rates of one of the most abundant fishes (gray snapper, Lutjanus griseus) in The Bahamas and combined these with surveys of fish abundance to estimate population-level excretion rates. The study was conducted across gradients of two human disturbances: overfishing and ecosystem fragmentation (estuaries bisected by roads), to evaluate how each could result in reduced population-level nutrient cycling by consumers. Mean estimated N and P excretion rates for gray snapper populations were on average 456% and 541% higher, respectively, in unfished sites. Ecosystem fragmentation resulted in significant reductions of recycling rates by snapper, with degree of creek fragmentation explaining 86% and 72% of the variance in estimated excretion for dissolved N and P, respectively. Additionally, we used nutrient limitation assays and primary producer nutrient content to provide a simple example of how marine fishery declines may affect primary production. This study provides an initial step toward integrating marine fishery declines and consumer-driven nutrient recycling to more fully understand the implications of human impacts in marine ecosystems.

Effects of habitat heterogeneity at multiple spatial scales on fish community assembly.

Habitat variability at multiple spatial scales may affect community structure within a given habitat patch, even within seemingly homogenous landscapes. In this context, we tested the importance of habitat variables at two spatial scales (patch and landscape) in driving fish community assembly using experimental artificial reefs constructed across a gradient of seagrass cover in a coastal bay of The Bahamas. We found that species richness and benthic fish abundance increased over time, but eventually reached an asymptote. The correlation between habitat variables and community structure strengthened over time, suggesting deterministic processes were detectable in community assembly. Abundance of benthic fishes, as well as overall community structure, were predicted by both patch- and landscape-scale variables, with the cover of seagrass at the landscape-scale emerging as the most important explanatory variable. Results of this study indicate that landscape features can drive differences in community assembly even within a general habitat type (i.e., within seagrass beds). A primary implication of this finding is that human activities driving changes in seagrass cover may cause significant shifts in faunal community structure well before complete losses of seagrass habitat.

Nutrient stoichiometry of fishes and invertebrates in coastal marine Caribbean ecosystems.

The importance of animals for mediating ecosystem processes has long been recognized by ecologists. Traditionally, consumer-mediated dynamics have been considered through consumptive pathways such as predation and herbivory. Yet, consumers also play critical roles in mediating "bottom-up" pathways associated with nutrient dynamics. Foundational research demonstrated the importance of these dynamics in terrestrial, freshwater, and pelagic marine ecosystems, and introduced novel perspectives on the role of animals such as wildebeest, lacustrine fishes, and zooplankton, respectively, for providing an important source of nutrients that limit primary production. This research inspired a substantial body of research on the importance of consumer-mediated nutrient dynamics for ecosystem function. Despite this, only recently have ecologists begun to extend this line of thinking toward coastal marine ecosystems. The data presented herein is a comprehensive study of consumer nutrient dynamics from invertebrates and fishes that live in subtropical and tropical Caribbean coastal marine waters, including mangroves, seagrass beds, and coral reefs. This data set represents the largest, to my knowledge, published nutrient stoichiometry data set from a single system, including estimates of excretion rates (n = 900 individuals total; n = 667 individual fish, size range 0.14-2,597 g [2-107 cm]; n = 233 invertebrates, size range 0.04-487 g), and somatic nutrient content analyses (n = 658 individuals total, n = 494 vertebrates, n = 164 invertebrates). These data also include δ13 C and δ15 N stable isotopes of whole body, body mass (wet mass), taxonomic identification to class-level, and functional group classification. These data have been used to test basic ecological theory, to scale individual-level processes to coral reef, mangrove, and seagrass ecosystems, and to understand the role of human impacts for mitigating consumer-mediated nutrient dynamics. While these findings have helped improve our understanding of nutrient dynamics in tropical coastal ecosystems, these data offer a wealth of additional promise for advancing ecological theory and applied science in tropical marine ecosystems and beyond. Users are free to use and analyze the data. Attribution should be given to this presentation of the data.

Phylogenetic conservatism drives nutrient dynamics of coral reef fishes.

The relative importance of evolutionary history and ecology for traits that drive ecosystem processes is poorly understood. Consumers are essential drivers of nutrient cycling on coral reefs, and thus ecosystem productivity. We use nine consumer "chemical traits" associated with nutrient cycling, collected from 1,572 individual coral reef fishes (178 species spanning 41 families) in two biogeographic regions, the Caribbean and Polynesia, to quantify the relative importance of phylogenetic history and ecological context as drivers of chemical trait variation on coral reefs. We find: (1) phylogenetic relatedness is the best predictor of all chemical traits, substantially outweighing the importance of ecological factors thought to be key drivers of these traits, (2) phylogenetic conservatism in chemical traits is greater in the Caribbean than Polynesia, where our data suggests that ecological forces have a greater influence on chemical trait variation, and (3) differences in chemical traits between regions can be explained by differences in nutrient limitation associated with the geologic context of our study locations. Our study provides multiple lines of evidence that phylogeny is a critical determinant of contemporary nutrient dynamics on coral reefs. More broadly our findings highlight the utility of evolutionary history to improve prediction in ecosystem ecology.

Taxonomic identity best explains variation in body nutrient stoichiometry in a diverse marine animal community.

Animal-mediated nutrient dynamics are critical processes in ecosystems. Previous research has found animal-mediated nutrient supply (excretion) to be highly predictable based on allometric scaling, but similar efforts to find universal predictive relationships for an organism's body nutrient content have been inconclusive. We use a large dataset from a diverse tropical marine community to test three frameworks for predicting body nutrient content. We show that body nutrient content does not follow allometric scaling laws and that it is not well explained by trophic status. Instead, we find strong support for taxonomic identity (particularly at the family level) as a predictor of body nutrient content, indicating that evolutionary history plays a crucial role in determining an organism's composition. We further find that nutrients are "stoichiometrically linked" (e.g., %C predicts %N), but that the direction of these relationships does not always conform to expectations, especially for invertebrates. Our findings demonstrate that taxonomic identity, not trophic status or body size, is the best baseline from which to predict organismal body nutrient content.

Individual behavior drives ecosystem function and the impacts of harvest.

Current approaches for biodiversity conservation and management focus on sustaining high levels of diversity among species to maintain ecosystem function. We show that the diversity among individuals within a single population drives function at the ecosystem scale. Specifically, nutrient supply from individual fish differs from the population average >80% of the time, and accounting for this individual variation nearly doubles estimates of nutrients supplied to the ecosystem. We test how management (i.e., selective harvest regimes) can alter ecosystem function and find that strategies targeting more active individuals reduce nutrient supply to the ecosystem up to 69%, a greater effect than body size-selective or nonselective harvest. Findings show that movement behavior at the scale of the individual can have crucial repercussions for the functioning of an entire ecosystem, proving an important challenge to the species-centric definition of biodiversity if the conservation and management of ecosystem function is a primary goal.

Comment on "Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning".

Brandl et al (Reports, 21 June 2019, p. 1189) report that cryptobenthic fishes underpin coral reef ecosystem function by contributing ~60% of "consumed fish" biomass and ~20% of production. These results are artifacts of their simulation. Using their data and model, we show that cryptobenthic species contribute less than 4% to fish production, calling into question the extent to which they contribute to the high productivity of coral reefs.