Fish feces reveal diverse nutrient sources for coral reefs.

Consumers mediate nutrient cycling through excretion and egestion across most ecosystems. In nutrient-poor tropical waters such as coral reefs, nutrient cycling is critical for maintaining productivity. While the cycling of fish-derived inorganic nutrients via excretion has been extensively investigated, the role of egestion for nutrient cycling has remained poorly explored. We sampled the fecal contents of 570 individual fishes across 40 species, representing six dominant trophic guilds of coral reef fishes in Moorea, French Polynesia. We measured fecal macro- (proteins, carbohydrates, lipids) and micro- (calcium, copper, iron, magnesium, manganese, zinc) nutrients and compared the fecal nutrient quantity and quality across trophic guilds, taxa, and body size. Macro- and micronutrient concentrations in fish feces varied markedly across species. Genera and trophic guild best predicted fecal nutrient concentrations. In addition, nutrient composition in feces was unique among species within both trophic guilds (herbivores and corallivores) and genera (Acanthurus and Chaetodon). Particularly, certain coral reef fishes (e.g., Thalassoma hardwicke, Chromis xanthura, Chaetodon pelewensis and Acanthurus pyroferus) harbored relatively high concentrations of micronutrients (e.g., Mn, Mg, Zn and Fe, respectively) that are known to contribute to ocean productivity and positively impact coral physiological performances. Given the nutrient-rich profiles across reef fish feces, conserving holistic reef fish communities ensures the availability of nutritional pools on coral reefs. We therefore suggest that better integration of consumer egestion dynamics into food web models and ecosystem-scale processes will facilitate an improved understanding of coral reef functioning.

Nutrient loading alters the performance of key nutrient exchange mutualisms.

Nutrient exchange mutualisms between phototrophs and heterotrophs, such as plants and mycorrhizal fungi or symbiotic algae and corals, underpin the functioning of many ecosystems. These relationships structure communities, promote biodiversity and help maintain food security. Nutrient loading may destabilise these mutualisms by altering the costs and benefits each partner incurs from interacting. Using meta-analyses, we show a near ubiquitous decoupling in mutualism performance across terrestrial and marine environments in which phototrophs benefit from enrichment at the expense of their heterotrophic partners. Importantly, heterotroph identity, their dependence on phototroph-derived C and the type of nutrient enrichment (e.g. nitrogen vs. phosphorus) mediated the responses of different mutualisms to enrichment. Nutrient-driven changes in mutualism performance may alter community organisation and ecosystem processes and increase costs of food production. Consequently, the decoupling of nutrient exchange mutualisms via alterations of the world's nitrogen and phosphorus cycles may represent an emerging threat of global change.

Fish-derived nutrient hotspots shape coral reef benthic communities.

Animal-derived nutrients play an important role in structuring nutrient regimes within and between ecosystems. When animals undergo repetitive, aggregating behavior through time, they can create nutrient hotspots where rates of biogeochemical activity are higher than those found in the surrounding environment. In turn, these hotspots can influence ecosystem processes and community structure. We examined the potential for reef fishes from the family Haemulidae (grunts) to create nutrient hotspots and the potential impact of these hotspots on reef communities. To do so, we tracked the schooling locations of diurnally migrating grunts, which shelter at reef sites during the day but forage off reef each night, and measured the impact of these fish schools on benthic communities. We found that grunt schools showed a high degree of site fidelity, repeatedly returning to the same coral heads. These aggregations created nutrient hotspots around coral heads where nitrogen and phosphorus delivery was roughly 10 and 7 times the respective rates of delivery to structurally similar sites that lacked schools of these fishes. In turn, grazing rates of herbivorous fishes at grunt-derived hotspots were approximately 3 times those of sites where grunts were rare. These differences in nutrient delivery and grazing led to distinct benthic communities with higher cover of crustose coralline algae and less total algal abundance at grunt aggregation sites. Importantly, coral growth was roughly 1.5 times greater at grunt hotspots, likely due to the important nutrient subsidy. Our results suggest that schooling reef fish and their nutrient subsidies play an important role in mediating community structure on coral reefs and that overfishing may have important negative consequences on ecosystem functions. As such, management strategies must consider mesopredatory fishes in addition to current protection often offered to herbivores and top-tier predators. Furthermore, our results suggest that restoration strategies may benefit from focusing on providing structure for aggregating fishes on reefs with low topographic complexity or focusing the restoration of nursery raised corals around existing nutrient hotspots.

Context-dependent effects of nutrient loading on the coral-algal mutualism.

Human-mediated increases in nutrient availability alter patterns of primary production, impact species diversity, and threaten ecosystem function. Nutrients can also alter community structure by disrupting the relationships between nutrient-sharing mutualists that form the foundation of communities. Given their oligotrophic nature and the dependence of reef-building corals on symbiotic relationships, coral reefs may be particularly vulnerable to excess nutrients. However, individual studies suggest complex, even contradictory, relationships among nutrient availability, coral physiology, and coral growth. Here, we used meta-analysis to establish general patterns of the impact of nitrogen (N) and phosphorus (P) on coral growth and photobiology. Overall, we found that over a wide range of concentrations, N reduced coral calcification 11%, on average, but enhanced metrics of coral photobiology, such as photosynthetic rate. In contrast, P enrichment increased average calcification rates by 9%, likely through direct impacts on the calcification process, but minimally impacted coral photobiology. There were few synergistic impacts of combined N and P on corals, as the nutrients impact corals via different pathways. Additionally, the response of corals to increasing nutrient availability was context dependent, varying with coral taxa and morphology, enrichment source, and nutrient identity. For example, naturally occurring enrichment from fish excretion increased coral growth, while human-mediated enrichment tended to decrease coral growth. Understanding the nuances of the relationship between nutrients and corals may allow for more targeted remediation strategies and suggest how other global change drivers such as overfishing and climate change will shape how nutrient availability impacts corals.

Differing nutritional constraints of consumers across ecosystems.

Stoichiometric mismatches between resources and consumers may drive a number of important ecological interactions, such as predation and herbivory. Such mismatches in nitrogen (N) or phosphorus (P) content between resources and consumers have furthered our understanding of consumer behavior and growth patterns in aquatic systems. However, stoichiometric data for multiple consumers from the same community are lacking in terrestrial systems. Here, we present the results of a study designed to characterize nutritional constraints within a terrestrial arthropod community. In order to place our results in a broader context, we compared our data on resource-consumer stoichiometry to those of stream and lake ecosystems. We found that N and P varied among trophic levels, and that high N:P content of herbivores suggests that herbivores might experience strong N-limitation. However, incredibly low P-content of plant foliage leads to potential P-limitation in herbivores that is nearly as strong as potential N-limitation. Moreover, arthropod predators may also be strongly P-limited. In fact, potential nutrient limitation of terrestrial herbivores in our study is similar to nutrient limitation from streams and lakes, suggesting that similar nutritional constraints may be operating across all three study systems. Importantly, our data suggest that consumers in lakes experience a trade-off between N- and P-limitation, while terrestrial consumers experience simultaneous strengthening or weakening of N- and P-limitation. We suggest that P may be overlooked as an important limiting nutrient in terrestrial ecosystems.

Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching.

Nutrient loading is one of the strongest drivers of marine habitat degradation. Yet, the link between nutrients and disease epizootics in marine organisms is often tenuous and supported only by correlative data. Here, we present experimental evidence that chronic nutrient exposure leads to increases in both disease prevalence and severity and coral bleaching in scleractinian corals, the major habitat-forming organisms in tropical reefs. Over 3 years, from June 2009 to June 2012, we continuously exposed areas of a coral reef to elevated levels of nitrogen and phosphorus. At the termination of the enrichment, we surveyed over 1200 scleractinian corals for signs of disease or bleaching. Siderastrea siderea corals within enrichment plots had a twofold increase in both the prevalence and severity of disease compared with corals in unenriched control plots. In addition, elevated nutrient loading increased coral bleaching; Agaricia spp. of corals exposed to nutrients suffered a 3.5-fold increase in bleaching frequency relative to control corals, providing empirical support for a hypothesized link between nutrient loading and bleaching-induced coral declines. However, 1 year later, after nutrient enrichment had been terminated for 10 months, there were no differences in coral disease or coral bleaching prevalence between the previously enriched and control treatments. Given that our experimental enrichments were well within the ranges of ambient nutrient concentrations found on many degraded reefs worldwide, these data provide strong empirical support to the idea that coastal nutrient loading is one of the major factors contributing to the increasing levels of both coral disease and coral bleaching. Yet, these data also suggest that simple improvements to water quality may be an effective way to mitigate some coral disease epizootics and the corresponding loss of coral cover in the future.

Nutrient supply from fishes facilitates macroalgae and suppresses corals in a Caribbean coral reef ecosystem.

On coral reefs, fishes can facilitate coral growth via nutrient excretion; however, as coral abundance declines, these nutrients may help facilitate increases in macroalgae. By combining surveys of reef communities with bioenergetics modeling, we showed that fish excretion supplied 25 times more nitrogen to forereefs in the Florida Keys, USA, than all other biotic and abiotic sources combined. One apparent result was a positive relationship between fish excretion and macroalgal cover on these reefs. Herbivore biomass also showed a negative relationship with macroalgal cover, suggesting strong interactions of top-down and bottom-up forcing. Nutrient supply by fishes also showed a negative correlation with juvenile coral density, likely mediated by competition between macroalgae and corals, suggesting that fish excretion may hinder coral recovery following large-scale coral loss. Thus, the impact of nutrient supply by fishes may be context-dependent and reinforce either coral-dominant or coral-depauperate reef communities depending on initial community states.