Spatial subsidies drive sweet spots of tropical marine biomass production

Spatial subsidies increase local productivity and boost consumer abundance beyond the limits imposed by local resources. In marine ecosystems, deeper water and open ocean subsidies promote animal aggregations and enhance biomass that is critical for human harvesting. However, the scale of this phenomenon in tropical marine systems remains unknown. Here, we integrate a detailed assessment of biomass production in 3 key locations, spanning a major biodiversity and abundance gradient, with an ocean-scale dataset of fish counts to predict the extent and magnitude of plankton subsidies to fishes on coral reefs. We show that planktivorous fish-mediated spatial subsidies are widespread across the Indian and Pacific oceans and drive local spikes in biomass production that can lead to extreme productivity, up to 30 kg ha⁻¹ day⁻¹. Plankton subsidies form the basis of productivity “sweet spots” where planktivores provide more than 50% of the total fish production, more than all other trophic groups combined. These sweet spots operate at regional, site, and smaller local scales. By harvesting oceanic productivity, planktivores bypass spatial constraints imposed by local primary productivity, creating “oases” of tropical fish biomass that are accessible to humans.

How do tropical oceans sustain high productivity and intense coastal fisheries despite occurring in nutrient-poor oceans? This study shows that spatial subsidies dramatically increase local coral reef productivity across the globe, producing localized ‘sweet-spots’ of concentrated, exceptionally high productivity.     

Human,Oceanographic and Habitat Drivers of Central and Western Pacific Coral Reef Fish Assemblages

Coral reefs around US- and US-affiliated Pacific islands and atolls span wide oceanographic gradients and levels of human impact. Here we examine the relative influence of these factors on coral reef fish biomass, using data from a consistent large-scale ecosystem monitoring program conducted by scientific divers over the course of >2,000 hours of underwater observation at 1,934 sites, across ~40 islands and atolls. Consistent with previous smaller-scale studies, our results show sharp declines in reef fish biomass at relatively low human population density, followed by more gradual declines as human population density increased further. Adjusting for other factors, the highest levels of oceanic productivity among our study locations were associated with more than double the biomass of reef fishes (including ~4 times the biomass of planktivores and piscivores) compared to islands with lowest oceanic productivity. Our results emphasize that coral reef areas do not all have equal ability to sustain large reef fish stocks, and that what is natural varies significantly amongst locations. Comparisons of biomass estimates derived from visual surveys with predicted biomass in the absence of humans indicated that total reef fish biomass was depleted by 61% to 69% at populated islands in the Mariana Archipelago; by 20% to 78% in the Main Hawaiian islands; and by 21% to 56% in American Samoa.     

Non‐reef habitats in a tropical seascape affect density and biomass of fishes on coral reefs

Nonreef habitats such as mangroves, seagrass, and macroalgal beds are important for foraging, spawning, and as nursery habitat for some coral reef fishes. The spatial configuration of nonreef habitats adjacent to coral reefs can therefore have a substantial influence on the distribution and composition of reef fish. We investigate how different habitats in a tropical seascape in the Philippines influence the presence, density, and biomass of coral reef fishes to understand the relative importance of different habitats across various spatial scales. A detailed seascape map generated from satellite imagery was combined with field surveys of fish and benthic habitat on coral reefs. We then compared the relative importance of local reef (within coral reef) and adjacent habitat (habitats in the surrounding seascape) variables for coral reef fishes. Overall, adjacent habitat variables were as important as local reef variables in explaining reef fish density and biomass, despite being fewer in number in final models. For adult and juvenile wrasses (Labridae), and juveniles of some parrotfish taxa (Chlorurus), adjacent habitat was more important in explaining fish density and biomass. Notably, wrasses were positively influenced by the amount of sand and macroalgae in the adjacent seascape. Adjacent habitat metrics with the highest relative importance were sand (positive), macroalgae (positive), and mangrove habitats (negative), and fish responses to these metrics were consistent across fish groups evaluated. The 500‐m spatial scale was selected most often in models for seascape variables. Local coral reef variables with the greatest importance were percent cover of live coral (positive), sand (negative), and macroalgae (mixed). Incorporating spatial metrics that describe the surrounding seascape will capture more holistic patterns of fish–habitat relationships on reefs. This is important in regions where protection of reef fish habitat is an integral part of fisheries management but where protection of nonreef habitats is often overlooked.     

Human exploitation shapes productivity–biomass relationships on coral reefs

Coral reef fisheries support the livelihoods of millions of people in tropical countries, despite large‐scale depletion of fish biomass. While human adaptability can help to explain the resistance of fisheries to biomass depletion, compensatory ecological mechanisms may also be involved. If this is the case, high productivity should coexist with low biomass under relatively high exploitation. Here we integrate large spatial scale empirical data analysis and a theory‐driven modelling approach to unveil the effects of human exploitation on reef fish productivity–biomass relationships. We show that differences in how productivity and biomass respond to overexploitation can decouple their relationship. As size‐selective exploitation depletes fish biomass, it triggers increased production per unit biomass, averting immediate productivity collapse in both the modelling and the empirical systems. This ‘buffering productivity’ exposes the danger of assuming resource production–biomass equivalence, but may help to explain why some biomass‐depleted fish assemblages still provide ecosystem goods under continued global fishing exploitation.     

How accessible are coral reefs to people? A global assessment based on travel time

The depletion of natural resources has become a major issue in many parts of the world, with the most accessible resources being most at risk. In the terrestrial realm, resource depletion has classically been related to accessibility through road networks. In contrast, in the marine realm, the impact on living resources is often framed into the Malthusian theory of human density around ecosystems. Here, we develop a new framework to estimate the accessibility of global coral reefs using potential travel time from the nearest human settlement or market. We show that 58% of coral reefs are located < 30 min from the nearest human settlement. We use a case study from New Caledonia to demonstrate that travel time from the market is a strong predictor of fish biomass on coral reefs. We also highlight a relative deficit of protection on coral reef areas near people, with disproportional protection on reefs far from people. This suggests that conservation efforts are targeting low‐conflict reefs or places that may already be receiving de facto protection due to their isolation. Our global assessment of accessibility in the marine realm is a critical step to better understand the interplay between humans and resources.     

Caribbean reefs of the Anthropocene: Variance in ecosystem metrics indicates bright spots on coral depauperate reefs

Dramatic coral loss has significantly altered many Caribbean reefs, with potentially important consequences for the ecological functions and ecosystem services provided by reef systems. Many studies examine coral loss and its causes—and often presume a universal decline of ecosystem services with coral loss—rather than evaluating the range of possible outcomes for a diversity of ecosystem functions and services at reefs varying in coral cover. We evaluate 10 key ecosystem metrics, relating to a variety of different reef ecosystem functions and services, on 328 Caribbean reefs varying in coral cover. We focus on the range and variability of these metrics rather than on mean responses. In contrast to a prevailing paradigm, we document high variability for a variety of metrics, and for many the range of outcomes is not related to coral cover. We find numerous “bright spots,” where herbivorous fish biomass, density of large fishes, fishery value, and/or fish species richness are high, despite low coral cover. Although it remains critical to protect and restore corals, understanding variability in ecosystem metrics among low‐coral reefs can facilitate the maintenance of reefs with sustained functions and services as we work to restore degraded systems. This framework can be applied to other ecosystems in the Anthropocene to better understand variance in ecosystem service outcomes and identify where and why bright spots exist.     

Coral–algal phase shifts alter fish communities and reduce fisheries production

Anthropogenic stress has been shown to reduce coral coverage in ecosystems all over the world. A phase shift towards an algae‐dominated system may accompany coral loss. In this case, the composition of the reef‐associated fish assemblage will change and human communities relying on reef fisheries for income and food security may be negatively impacted. We present a case study based on the Raja Ampat Archipelago in Eastern Indonesia. Using a dynamic food web model, we simulate the loss of coral reefs with accompanied transition towards an algae‐dominated state and quantify the likely change in fish populations and fisheries productivity. One set of simulations represents extreme scenarios, including 100% loss of coral. In this experiment, ecosystem changes are driven by coral loss itself and a degree of habitat dependency by reef fish is assumed. An alternative simulation is presented without assumed habitat dependency, where changes to the ecosystem are driven by historical observations of reef fish communities when coral is lost. The coral–algal phase shift results in reduced biodiversity and ecosystem maturity. Relative increases in the biomass of small‐bodied fish species mean higher productivity on reefs overall, but much reduced landings of traditionally targeted species.     

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.     

Extinction rate, historical population structure and ecological role of the Caribbean monk seal

The productivity and biomass of pristine coral reef ecosystems is poorly understood, particularly in the Caribbean where communities have been impacted by overfishing and multiple other stressors over centuries. Using historical data on the spatial distribution and abundance of the extinct Caribbean monk seal (Monachus tropicalis), this study reconstructs the population size, structure and ecological role of this once common predator within coral reef communities, and provides evidence that historical reefs supported biomasses of fishes and invertebrates up to six times greater than those found on typical modern Caribbean reefs. An estimated 233,000-338,000 monk seals were distributed among 13 colonies across the Caribbean. The biomass of reef fishes and invertebrates required to support historical seal populations was 732-1018 gm(-2) of reefs, which exceeds that found on any Caribbean reef today and is comparable with those measured in remote Pacific reefs. Quantitative estimates of historically dense monk seal colonies and their consumption rates on pristine reefs provide concrete data on the magnitude of decline in animal biomass on Caribbean coral reefs. Realistic reconstruction of these past ecosystems is critical to understanding the profound and long-lasting effect of human hunting on the functioning of coral reef ecosystems.     

Parasites of coral reef fish larvae: its role in the pelagic larval stage

The pelagic larval stage is a critical component of the life cycle of most coral reef fishes, but the adaptive significance of this stage remains controversial. One hypothesis is that migrating through the pelagic environment reduces the risk a larval fish has of being parasitised. Most organisms interact with parasites, often with significant, detrimental consequences for the hosts. However, little is known about the parasites that larval fish have upon settlement, and the factors that affect the levels of parasitism. At settlement, coral reef fishes vary greatly in size and age (pelagic larval duration), which may influence the degree of parasitism. We identified and quantified the parasites of pre-settlement larvae from 44 species of coral reef fishes from the Great Barrier Reef and explored their relationship with host size and age at settlement, and phylogeny. Overall, less than 50% of the larval fishes were infected with parasites, and over 99% of these were endoparasites. A Bayesian phylogenetic regression was used to analyse host-parasite (presence and intensity) associations. The analysis showed parasite presence was not significantly related to fish size, and parasite intensity was not significantly related to fish age. A phylogenetic signal was detected for both parasite presence and intensity, indicating that, overall, closely related fish species were likely to have more similar susceptibility to parasites and similar levels of parasitism when compared to more distantly related species. The low prevalence of infection with any parasite type and the striking rarity of ectoparasites is consistent with the ‘parasite avoidance hypothesis’, which proposes that the pelagic phase of coral reef fishes results in reduced levels of parasitism.

     

Life history patterns shape energy allocation among fishes on coral reefs

Although critically important, the link between animal life histories and ecosystem energetics is seldom explored. In the pursuit of ecological simplification, ecosystem properties are typically described by models based on static counts, where organisms are aggregated into trophic- or size-based groups. Consequently, output is often based on an assumption that larger group biomass equals greater energetic contribution. Here, we modelled the individual growth of over 58,000 fishes from 74 genera within a coral reef ecosystem to investigate the role and importance of taxon-specific life histories to the division, spatial distribution and relative contribution of biomass production within 14 coral reef fish families. Rank changes among families in standing biomass to biomass production indicated that small cryptic families (e.g. Gobiidae and Blenniidae) exhibit collective growth potentials equal to or exceeding those of many other common families composed of individuals with body-sizes 1–3 orders of magnitude larger. Remaining at high risk of predation throughout their lives as a consequence of their small size, these cryptic fishes also provide a constant food resource and supply of reproductive energy to coral reefs throughout the year. Enhanced further by the strength and diversity of their trophic relationships within food webs, the highly productive nature of these small cryptic fishes suggests they make a substantial contribution to the flow of energy in coral reef ecosystems via predatory pathways. It appears that life histories leave a strong imprint on ecosystem energy fluxes and illustrate the importance of incorporating taxon-specific features when assigning values to key ecosystem processes. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Fishing degrades size structure of coral reef fish communities

Fishing pressure on coral reef ecosystems has been frequently linked to reductions of large fishes and reef fish biomass. Associated impacts on overall community structure are, however, less clear. In size‐structured aquatic ecosystems, fishing impacts are commonly quantified using size spectra, which describe the distribution of individual body sizes within a community. We examined the size spectra and biomass of coral reef fish communities at 38 US‐affiliated Pacific islands that ranged in human presence from near pristine to human population centers. Size spectra ‘steepened’ steadily with increasing human population and proximity to market due to a reduction in the relative biomass of large fishes and an increase in the dominance of small fishes. Reef fish biomass was substantially lower on inhabited islands than uninhabited ones, even at inhabited islands with the lowest levels of human presence. We found that on populated islands size spectra exponents decreased (analogous to size spectra steepening) linearly with declining biomass, whereas on uninhabited islands there was no relationship. Size spectra were steeper in regions of low sea surface temperature but were insensitive to variation in other environmental and geomorphic covariates. In contrast, reef fish biomass was highly sensitive to oceanographic conditions, being influenced by both oceanic productivity and sea surface temperature. Our results suggest that community size structure may be a more robust indicator than fish biomass to increasing human presence and that size spectra are reliable indicators of exploitation impacts across regions of different fish community compositions, environmental drivers, and fisheries types. Size‐based approaches that link directly to functional properties of fish communities, and are relatively insensitive to abiotic variation across biogeographic regions, offer great potential for developing our understanding of fishing impacts in coral reef ecosystems.     

Interpreting coral reef monitoring data: A guide for improved management decisions

Coral reef monitoring programmes exist in all regions of the world, recording reef attributes such as coral cover, fish biomass and macroalgal cover. Given the cost of such monitoring programs, and the degraded state of many of the world’s reefs, understanding how reef monitoring data can be used to shape management decisions for coral reefs is a high priority. However, there is no general guide to understanding the ecological implications of the data in a format that can trigger a management response. We attempt to provide such a guide for interpreting the temporal trends in 41 coral reef monitoring attributes, recorded by seven of the largest reef monitoring programmes. We show that only a small subset of these attributes is required to identify the stressors that have impacted a reef (i.e. provide a diagnosis), as well as to estimate the likely recovery potential (prognosis). Two of the most useful indicators, turf algal canopy height and coral colony growth rate are not commonly measured, and we strongly recommend their inclusion in reef monitoring. The diagnosis and prognosis system that we have developed may help guide management actions and provides a foundation for further development as biological and ecological insights continue to grow.     

Understanding the Spatio-Temporal Response of Coral Reef Fish Communities to Natural Disturbances: Insights from Beta-Diversity Decomposition

Understanding how communities respond to natural disturbances is fundamental to assess the mechanisms of ecosystem resistance and resilience. However, ecosystem responses to natural disturbances are rarely monitored both through space and time, while the factors promoting ecosystem stability act at various temporal and spatial scales. Hence, assessing both the spatial and temporal variations in species composition is important to comprehensively explore the effects of natural disturbances. Here, we suggest a framework to better scrutinize the mechanisms underlying community responses to disturbances through both time and space. Our analytical approach is based on beta diversity decomposition into two components, replacement and biomass difference. We illustrate this approach using a 9-year monitoring of coral reef fish communities off Moorea Island (French Polynesia), which encompassed two severe natural disturbances: a crown-of-thorns starfish outbreak and a hurricane. These disturbances triggered a fast logistic decline in coral cover, which suffered a 90% decrease on all reefs. However, we found that the coral reef fish composition remained largely stable through time and space whereas compensatory changes in biomass among species were responsible for most of the temporal fluctuations, as outlined by the overall high contribution of the replacement component to total beta diversity. This suggests that, despite the severity of the two disturbances, fish communities exhibited high resistance and the ability to reorganize their compositions to maintain the same level of total community biomass as before the disturbances. We further investigated the spatial congruence of this pattern and showed that temporal dynamics involved different species across sites; yet, herbivores controlling the proliferation of algae that compete with coral communities were consistently favored. These results suggest that compensatory changes in biomass among species and spatial heterogeneity in species responses can provide further insurance against natural disturbances in coral reef ecosystems by promoting high levels of key species (herbivores). They can also allow the ecosystem to recover more quickly.     

Relationships between structural complexity,coral traits,and reef fish assemblages

With the ongoing loss of coral cover and the associated flattening of reef architecture, understanding the links between coral habitat and reef fishes is of critical importance. Here, we investigate whether considering coral traits and functional diversity provides new insights into the relationship between structural complexity and reef fish communities, and whether coral traits and community composition can predict structural complexity. Across 157 sites in Seychelles, Maldives, the Chagos Archipelago, and Australia’s Great Barrier Reef, we find that structural complexity and reef zone are the strongest and most consistent predictors of reef fish abundance, biomass, species richness, and trophic structure. However, coral traits, diversity, and life histories provided additional predictive power for models of reef fish assemblages, and were key drivers of structural complexity. Our findings highlight that reef complexity relies on living corals—with different traits and life histories—continuing to build carbonate skeletons, and that these nuanced relationships between coral assemblages and habitat complexity can affect the structure of reef fish assemblages. Seascape-level estimates of structural complexity are rapid and cost effective with important implications for the structure and function of fish assemblages, and should be incorporated into monitoring programs.     

Ontogenetic habitat shifts in fusiliers (Lutjanidae): evidence from Caesio cuning at Lizard Island,Great Barrier Reef

Planktivorous reef-associated fishes provide a significant nutrient input to the reef, linking pelagic and reef environments. Highly mobile and relatively large body-sized fusiliers (Lutjanidae) often dominate reef fish biomass, but their role in ecosystem processes is poorly understood. We therefore combined fish counts and behavioural observations at Lizard Island, Great Barrier Reef, to investigate: (1) the spatial distribution and biology of fusiliers on a lagoonal coral reef system, and (2) how does fusilier behaviour and size distribution change from exposed to sheltered locations. We found higher abundances of large-sized fusiliers (≥ 20 cm total length) on exposed reef sites. Sheltered sites had almost exclusively small individuals (< 20 cm total length). We interpret this pattern as indicative of an ontogenetic habitat shift. This shift was estimated to occur at about 11.15 cm total length; the size at which the likelihood of an individual being in exposed or sheltered locations was equal. The age corresponding to this length was 1.01 years, based on a von Bertalanffy growth model using size-at-age data from otolith rings of Caesio cuning, the most abundant fusilier species in this location. This suggested that the shift in distribution occurred prior to the onset of sexual maturity. This apparent ontogenetic shift to more exposed habitats with increasing size, especially in C. cuning, was also associated with a distinct behavioural profile: larger fish at the exposed sites travelled further off reef, occupied deeper habitats, and formed larger schools compared to smaller individuals. This study provides the first evidence of seascape-scale ontogenetic habitat shifts in a planktivorous reef fish, providing a foundation for future detailed analyses of the ecological roles of fusiliers.

     

Recruitment of coral reef fishes along a cross-shelf gradient in the Red Sea peaks outside the hottest season

Knowledge on the early life history, ecology, and biology of marine species is crucial for future projections of the resilience of coral reef ecosystems and for adequate management strategies. A fundamental component of population dynamics is the recruitment of new individuals, and in some marine populations, this may be a limiting factor. Recruitment peaks of coral reef fishes commonly occur during the warmer months of the year in many subtropical and temperate locations worldwide. In the Red Sea, very little is known about the influence of temperature on reproductive patterns of coral reef fishes and studies on recruitment are missing. The Red Sea is one of the hottest and most isolated tropical seas in the world. We hypothesized that sea surface temperatures (SSTs) during the Red Sea’s hottest season may exceed the optimum for successful recruitment of some coral reef fishes, which therefore has to occur during other, cooler seasons, unlike recruitment among coral reef ecosystems around the world. We identified taxa among fish recruits by matching mitochondrial DNA sequences (using COI, commonly known as “barcoding”) and assessed potential biological and environmental drivers of recruitment. We studied three reefs located along a cross-shelf gradient for 12 consecutive months in the central Red Sea to capture seasonal changes in biotic and abiotic parameters along this gradient. Our results indicated that recruitment peaks did not occur during the hottest SSTs for most taxa, especially at the hottest inshore and mid-shelf reefs, and identified fish recruitment to be mainly and strongly correlated with the biomass of planktonic invertebrates. Moreover, temporal patterns of fish recruitment differed within and among taxonomic families among the reefs.

     

Relative Importance of Coral Cover,Habitat Complexity and Diversity in Determining the Structure of Reef Fish Communities

The structure of coral reef habitat has a pronounced influence on the diversity, composition and abundance of reef-associated fishes. However, the particular features of the habitat that are most critical are not always known. Coral habitats can vary in many characteristics, notably live coral cover, topographic complexity and coral diversity, but the relative effects of these habitat characteristics are often not distinguished. Here, we investigate the strength of the relationships between these habitat features and local fish diversity, abundance and community structure in the lagoon of Lizard Island, Great Barrier Reef. In a spatial comparison using sixty-six 2m² quadrats, fish species richness, total abundance and community structure were examined in relation to a wide range of habitat variables, including topographic complexity, habitat diversity, coral diversity, coral species richness, hard coral cover, branching coral cover and the cover of corymbose corals. Fish species richness and total abundance were strongly associated with coral species richness and cover, but only weakly associated with topographic complexity. Regression tree analysis showed that coral species richness accounted for most of the variation in fish species richness (63.6%), while hard coral cover explained more variation in total fish abundance (17.4%), than any other variable. In contrast, topographic complexity accounted for little spatial variation in reef fish assemblages. In degrading coral reef environments, the potential effects of loss of coral cover and topographic complexity are often emphasized, but these findings suggest that reduced coral biodiversity may ultimately have an equal, or greater, impact on reef-associated fish communities.     

Post-larval French grunts (Haemulon flavolineatum) distinguish between seagrass, mangrove and coral reef water: Implications for recognition of potential nursery habitats

Environmental cues like sound, magnetic field, oceanic currents, water chemistry or habitat structure are believed to play an important role in the orientation of reef fish towards their settlement habitat. Some species of coral reef fish are known to use seagrass beds and mangroves as juvenile habitats. Once oceanic larvae of these fish have located a coral reef from the open ocean, they still have to find embayments or lagoons harbouring these juvenile habitats. The sensory mechanisms that are used for this are still unknown. In the present study, experiments were conducted to investigate if recruits of the French grunt (Haemulon flavolineatum) respond to habitat differences in water type, as mangrove/seagrass water may differ in biotic and abiotic compounds from coral reef water. Our results show that post-larvae of a reef fish that is highly associated with mangroves and seagrass beds during its juvenile life stage, choose significantly more often for water from mangroves and seagrass beds than for water from the coral reef. These results provide a more detailed insight in the mechanisms that play a role in the detection of these juvenile habitats.