Species eradication for ecosystem restoration.

Many of the world's ecosystems are under unprecedented stress as human pressures have escalated to be a dominant driver of ecosystem composition and condition. Direct impacts such as agriculture, extraction, and development are impacting vast swathes of land and ocean, while the effects of human-caused climate change are felt even in the most remote parts of marine and terrestrial wildernesses. These impacts are resulting in changes ranging from ecosystem collapse or replacement to novel mixes of species due to temperature-driven range shifts. While reducing human pressures is paramount for the future viability of vulnerable ecosystems, much attention is now also focused on whether degraded areas can be restored. Indeed, the UN has declared 2021-2030 the Decade on Ecosystem Restoration, which aims to "prevent, halt and reverse the degradation of ecosystems on every continent and in every ocean".

Quantifying energy and nutrient fluxes in coral reef food webs.

The movement of energy and nutrients through ecological communities represents the biological 'pulse' underpinning ecosystem functioning and services. However, energy and nutrient fluxes are inherently difficult to observe, particularly in high-diversity systems such as coral reefs. We review advances in the quantification of fluxes in coral reef fishes, focusing on four key frameworks: demographic modelling, bioenergetics, micronutrients, and compound-specific stable isotope analysis (CSIA). Each framework can be integrated with underwater surveys, enabling researchers to scale organismal processes to ecosystem properties. This has revealed how small fish support biomass turnover, pelagic subsidies sustain fisheries, and fisheries benefit human health. Combining frameworks, closing data gaps, and expansion to other aquatic ecosystems can advance understanding of how fishes contribute to ecosystem functions and services.

Seabirds boost coral reef resilience.

Global climate change threatens tropical coral reefs, yet local management can influence resilience. While increasing anthropogenic nutrients reduce coral resistance and recovery, it is unknown how the loss, or restoration, of natural nutrient flows affects reef recovery. Here, we test how natural seabird-derived nutrient subsidies, which are threatened by invasive rats, influence the mechanisms and patterns of reef recovery following an extreme marine heatwave using multiyear field experiments, repeated surveys, and Bayesian modeling. Corals transplanted from rat to seabird islands quickly assimilated seabird-derived nutrients, fully acclimating to new nutrient conditions within 3 years. Increased seabird-derived nutrients, in turn, caused a doubling of coral growth rates both within individuals and across entire reefs. Seabirds were also associated with faster recovery time of Acropora coral cover (<4 years) and more dynamic recovery trajectories of entire benthic communities. We conclude that restoring seabird populations and associated nutrient pathways may foster greater coral reef resilience through enhanced growth and recovery rates of corals.

Reef-building corals farm and feed on their photosynthetic symbionts.

Coral reefs are highly diverse ecosystems that thrive in nutrient-poor waters, a phenomenon frequently referred to as the Darwin paradox1. The energy demand of coral animal hosts can often be fully met by the excess production of carbon-rich photosynthates by their algal symbionts2,3. However, the understanding of mechanisms that enable corals to acquire the vital nutrients nitrogen and phosphorus from their symbionts is incomplete4-9. Here we show, through a series of long-term experiments, that the uptake of dissolved inorganic nitrogen and phosphorus by the symbionts alone is sufficient to sustain rapid coral growth. Next, considering the nitrogen and phosphorus budgets of host and symbionts, we identify that these nutrients are gathered through symbiont 'farming' and are translocated to the host by digestion of excess symbiont cells. Finally, we use a large-scale natural experiment in which seabirds fertilize some reefs but not others, to show that the efficient utilization of dissolved inorganic nutrients by symbiotic corals established in our laboratory experiments has the potential to enhance coral growth in the wild at the ecosystem level. Feeding on symbionts enables coral animals to tap into an important nutrient pool and helps to explain the evolutionary and ecological success of symbiotic corals in nutrient-limited waters.

Macroalgae exhibit diverse responses to human disturbances on coral reefs.

Scientists and managers rely on indicator taxa such as coral and macroalgal cover to evaluate the effects of human disturbance on coral reefs, often assuming a universally positive relationship between local human disturbance and macroalgae. Despite evidence that macroalgae respond to local stressors in diverse ways, there have been few efforts to evaluate relationships between specific macroalgae taxa and local human-driven disturbance. Using genus-level monitoring data from 1205 sites in the Indian and Pacific Oceans, we assess whether macroalgae percent cover correlates with local human disturbance while accounting for factors that could obscure or confound relationships. Assessing macroalgae at genus level revealed that no genera were positively correlated with all human disturbance metrics. Instead, we found relationships between the division or genera of algae and specific human disturbances that were not detectable when pooling taxa into a single functional category, which is common to many analyses. The convention to use percent cover of macroalgae as an indication of local human disturbance therefore likely obscures signatures of local anthropogenic threats to reefs. Our limited understanding of relationships between human disturbance, macroalgae taxa, and their responses to human disturbances impedes the ability to diagnose and respond appropriately to these threats.

Terrestrial invasive species alter marine vertebrate behaviour.

Human-induced environmental changes, such as the introduction of invasive species, are driving declines in the movement of nutrients across ecosystems with negative consequences for ecosystem function. Declines in nutrient inputs could thus have knock-on effects at higher trophic levels and broader ecological scales, yet these interconnections remain relatively unknown. Here we show that a terrestrial invasive species (black rats, Rattus rattus) disrupts a nutrient pathway provided by seabirds, ultimately altering the territorial behaviour of coral reef fish. In a replicated ecosystem-scale natural experiment, we found that reef fish territories were larger and the time invested in aggression lower on reefs adjacent to rat-infested islands compared with rat-free islands. This response reflected changes in the economic defendability of lower-quality resources, with reef fish obtaining less nutritional gain per unit foraging effort adjacent to rat-infested islands with low seabird populations. These results provide a novel insight into how the disruption of nutrient flows by invasive species can affect variation in territorial behaviour. Rat eradication as a conservation strategy therefore has the potential to restore species interactions via territoriality, which can scale up to influence populations and communities at higher ecological levels.

Seabird diversity and biomass enhance cross-ecosystem nutrient subsidies.

Mobile consumers are key vectors of cross-ecosystem nutrients, yet have experienced population declines which threaten their ability to fill this role. Despite their importance and vulnerability, there is little information on how consumer biodiversity, in addition to biomass, influences the magnitude of nutrient subsidies. Here, we show that both biomass and diversity of seabirds enhanced the provisioning of nutrients across tropical islands and coral reefs, but their relative influence varied across systems. Seabird biomass was particularly important for terrestrial and near-shore subsidies and enhancing fish biomass, while seabird diversity was associated with nutrient subsidies further offshore. The positive effects of diversity were likely driven by high functional complementarity among seabird species in traits related to nutrient storage and provisioning. However, introduced rats and non-native vegetation reduced seabird biomass and diversity, with rats having a stronger effect on biomass and vegetation having a stronger effect on diversity. Accordingly, the restoration of cross-ecosystem nutrient flows provided by seabirds will likely be most successful when both stressors are removed, thus protecting both high biomass and diversity. Recognizing the importance of mobile consumer diversity and biomass, and their underlying drivers, is a necessary step to conserving these species and the ecosystem functions they provide.

Natural nutrient subsidies alter demographic rates in a functionally important coral-reef fish.

By improving resource quality, cross-ecosystem nutrient subsidies may boost demographic rates of consumers in recipient ecosystems, which in turn can affect population and community dynamics. However, empirical studies on how nutrient subsidies simultaneously affect multiple demographic rates are lacking, in part because humans have disrupted the majority of these natural flows. Here, we compare the demographics of a sex-changing parrotfish (Chlorurus sordidus) between reefs where cross-ecosystem nutrients provided by seabirds are available versus nearby reefs where invasive, predatory rats have removed seabird populations. For this functionally important species, we found evidence for a trade-off between investing in growth and fecundity, with parrotfish around rat-free islands with many seabirds exhibiting 35% faster growth, but 21% lower size-based fecundity, than those around rat-infested islands with few seabirds. Although there were no concurrent differences in population-level density or biomass, overall mean body size was 16% larger around rat-free islands. Because the functional significance of parrotfish as grazers and bioeroders increases non-linearly with size, the increased growth rates and body sizes around rat-free islands likely contributes to higher ecosystem function on coral reefs that receive natural nutrient subsidies. More broadly, these results demonstrate additional benefits, and potential trade-offs, of restoring natural nutrient pathways for recipient ecosystems.

Rat eradication restores nutrient subsidies from seabirds across terrestrial and marine ecosystems.

Biological invasions pose a threat to nearly every ecosystem worldwide.1,2 Although eradication programs can successfully eliminate invasive species and enhance native biodiversity, especially on islands,3 the effects of eradication on cross-ecosystem processes are unknown. On islands where rats were never introduced, seabirds transfer nutrients from pelagic to terrestrial and nearshore marine habitats, which in turn enhance the productivity, biomass, and functioning of recipient ecosystems.4-6 Here, we test whether rat eradication restores seabird populations, their nutrient subsidies, and some of their associated benefits for ecosystem function to tropical islands and adjacent coral reefs. By comparing islands with different rat invasion histories, we found a clear hierarchy whereby seabird biomass, seabird-driven nitrogen inputs, and the incorporation of seabird-derived nutrients into terrestrial and marine food chains were highest on islands where rats were never introduced, intermediate on islands where rats were eradicated 4-16 years earlier, and lowest on islands with invasive rats still present. Seabird-derived nutrients diminished from land to sea and with increasing distance to rat-eradicated islands, but extended at least 300 m from shore. Although rat eradication enhanced seabird-derived nutrients in soil, leaves, marine algae, and herbivorous reef fish, reef fish growth was similar around rat-eradicated and rat-infested islands. Given that the loss of nutrient subsidies is of global concern,7 that removal of invasive species restores previously lost nutrient pathways over relatively short timescales is promising. However, the full return of cross-ecosystem nutrient subsidies and all of their associated demographic benefits may take multiple decades.

Biodiversity increases ecosystem functions despite multiple stressors on coral reefs.

Positive relationships between biodiversity and ecosystem functioning (BEF) highlight the importance of conserving biodiversity to maintain key ecosystem functions and associated services. Although natural systems are rapidly losing biodiversity due to numerous human-caused stressors, our understanding of how multiple stressors influence BEF relationships comes largely from small, experimental studies. Here, using remote assemblages of coral reef fishes, we demonstrate strong, non-saturating relationships of biodiversity with two ecosystem functions: biomass and productivity. These positive relationships were robust both to an extreme heatwave that triggered coral bleaching and to invasive rats which disrupt nutrient subsidies from native seabirds. Despite having only minor effects on BEF relationships, both stressors still decreased ecosystem functioning via other pathways. The extreme heatwave reduced biodiversity, which, due to the strong BEF relationships, ultimately diminished both ecosystem functions. Conversely, the loss of cross-system nutrient subsidies directly decreased biomass. These results demonstrate multiple ways by which human-caused stressors can reduce ecosystem functioning, despite robust BEF relationships, in natural high-diversity assemblages.

Climatic and local stressor interactions threaten tropical forests and coral reefs.

Tropical forests and coral reefs host a disproportionately large share of global biodiversity and provide ecosystem functions and services used by millions of people. Yet, ongoing climate change is leading to an increase in frequency and magnitude of extreme climatic events in the tropics, which, in combination with other local human disturbances, is leading to unprecedented negative ecological consequences for tropical forests and coral reefs. Here, we provide an overview of how and where climate extremes are affecting the most biodiverse ecosystems on Earth and summarize how interactions between global, regional and local stressors are affecting tropical forest and coral reef systems through impacts on biodiversity and ecosystem resilience. We also discuss some key challenges and opportunities to promote mitigation and adaptation to a changing climate at local and global scales. This article is part of the theme issue 'Climate change and ecosystems: threats, opportunities and solutions'.

Synchronous biological feedbacks in parrotfishes associated with pantropical coral bleaching.

Biological feedbacks generated through patterns of disturbance are vital for sustaining ecosystem states. Recent ocean warming and thermal anomalies have caused pantropical episodes of coral bleaching, which has led to widespread coral mortality and a range of subsequent effects on coral reef communities. Although the response of many reef-associated fishes to major disturbance events on coral reefs is negative (e.g., reduced abundance and condition), parrotfishes show strong feedbacks after disturbance to living reef structure manifesting as increases in abundance. However, the mechanisms underlying this response are poorly understood. Using biochronological reconstructions of annual otolith (ear stone) growth from two ocean basins, we tested whether parrotfish growth was enhanced following bleaching-related coral mortality, thus providing an organismal mechanism for demographic changes in populations. Both major feeding guilds of parrotfishes (scrapers and excavators) exhibited enhanced growth of individuals after bleaching that was decoupled from expected thermal performance, a pattern that was not evident in other reef fish taxa from the same environment. These results provide evidence for a more nuanced ecological feedback system-one where disturbance plays a key role in mediating parrotfish-benthos interactions. By influencing the biology of assemblages, disturbance can thereby stimulate change in parrotfish grazing intensity and ultimately reef geomorphology over time. This feedback cycle operated historically at within-reef scales; however, our results demonstrate that the scale, magnitude, and severity of recent thermal events are entraining the biological responses of disparate communities to respond in synchrony. This may fundamentally alter feedbacks in the relationships between parrotfishes and reef systems.

Seabird nutrient subsidies alter patterns of algal abundance and fish biomass on coral reefs following a bleaching event.

Cross-ecosystem nutrient subsidies play a key role in the structure and dynamics of recipient communities, but human activities are disrupting these links. Because nutrient subsidies may also enhance community stability, the effects of losing these inputs may be exacerbated in the face of increasing climate-related disturbances. Nutrients from seabirds nesting on oceanic islands enhance the productivity and functioning of adjacent coral reefs, but it is unknown whether these subsidies affect the response of coral reefs to mass bleaching events or whether the benefits of these nutrients persist following bleaching. To answer these questions, we surveyed benthic organisms and fishes around islands with seabirds and nearby islands without seabirds due to the presence of invasive rats. Surveys were conducted in the Chagos Archipelago, Indian Ocean, immediately before the 2015-2016 mass bleaching event and, in 2018, two years following the bleaching event. Regardless of the presence of seabirds, relative coral cover declined by 32%. However, there was a post-bleaching shift in benthic community structure around islands with seabirds, which did not occur around islands with invasive rats, characterized by increases in two types of calcareous algae (crustose coralline algae [CCA] and Halimeda spp.). All feeding groups of fishes were positively affected by seabirds, but only herbivores and piscivores were unaffected by the bleaching event and sustained the greatest difference in biomass between islands with seabirds versus those with invasive rats. By contrast, corallivores and planktivores, both of which are coral-dependent, experienced the greatest losses following bleaching. Even though seabird nutrients did not enhance community-wide resistance to bleaching, they may still promote recovery of these reefs through their positive influence on CCA and herbivorous fishes. More broadly, the maintenance of nutrient subsidies, via strategies including eradication of invasive predators, may be important in shaping the response of ecological communities to global climate change.

Predator effects on reef fish settlement depend on predator origin and recruit density.

During major life-history transitions, animals often experience high mortality rates due to predation, making predator avoidance particularly advantageous during these times. There is mixed evidence from a limited number of studies, however, regarding how predator presence influences settlement of coral-reef fishes and it is unknown how other potentially mediating factors, including predator origin (native vs. nonnative) or interactions among conspecific recruits, mediate the non-consumptive effects of predators on reef fish settlement. During a field experiment in the Caribbean, approximately 52% fewer mahogany snapper (Lutjanus mahogoni) recruited to reefs with a native predator (graysby grouper, Cephalopholis cruentata) than to predator-free control reefs and reefs with an invasive predator (red lionfish, Pterois volitans) regardless of predator diet. These results suggest that snapper recruits do not recognize nonnative lionfish as a threat. However, these effects depended on the density of conspecific recruits, with evidence that competition may limit the response of snapper to even native predators at the highest recruit densities. In contrast, there was no effect of predator presence or conspecific density on the recruitment of bicolor damselfish (Stegastes partitus). These context-dependent responses of coral-reef fishes to predators during settlement may influence individual survival and shape subsequent population and community dynamics.

Central-place foraging and ecological effects of an invasive predator across multiple habitats.

Cross-habitat foraging movements of predators can have widespread implications for predator and prey populations, community structure, nutrient transfer, and ecosystem function. Although central-place foraging models and other aspects of optimal foraging theory focus on individual predator behavior, they also provide useful frameworks for understanding the effects of predators on prey populations across multiple habitats. However, few studies have examined both the foraging behavior and ecological effects of nonnative predators across multiple habitats, and none has tested whether nonnative predators deplete prey in a manner predicted by these foraging models. I conducted behavioral observations of invasive lionfish (Pterois volitans) to determine whether they exhibit foraging movements similar to other central-place consumers. Then, I used a manipulative field experiment to test whether their effects on prey populations are consistent with three qualitative predictions from optimal foraging models. Specifically, I predicted that the effects of invasive lionfish on native prey will (1) occur at central sites first and then in surrounding habitats, (2) decrease with increasing distance away from their shelter site, and (3) extend to greater distances when prey patches are spaced closer together. Approximately 40% of lionfish exhibited short-term crepuscular foraging movements into surrounding habitats from the coral patch reefs where they shelter during daylight hours. Over the course of 7 weeks, lionfish depleted native fish populations on the coral patch reefs where they reside, and subsequently on small structures in the surrounding habitat. However, their effects did not decrease with increasing distance from the central shelter site and the influence of patch spacing was opposite the prediction. Instead, lionfish always had the greatest effects in areas with the highest prey densities. The differences between the predicted and observed effects of lionfish foraging are likely due to different constraints faced by invasive predators compared to native predators, namely that lionfish do not face increased predation risk with increased movement away from shelter sites. By foraging at greater distances from patch reefs than native predators, lionfish eliminated a spatial refuge from predation used by juveniles of many commercially and ecologically important reef fishes.

Patterns and Variation in Benthic Biodiversity in a Large Marine Ecosystem.

While there is a persistent inverse relationship between latitude and species diversity across many taxa and ecosystems, deviations from this norm offer an opportunity to understand the conditions that contribute to large-scale diversity patterns. Marine systems, in particular, provide such an opportunity, as marine diversity does not always follow a strict latitudinal gradient, perhaps because several hypothesized drivers of the latitudinal diversity gradient are uncorrelated in marine systems. We used a large scale public monitoring dataset collected over an eight year period to examine benthic marine faunal biodiversity patterns for the continental shelf (55-183 m depth) and slope habitats (184-1280 m depth) off the US West Coast (47°20'N-32°40'N). We specifically asked whether marine biodiversity followed a strict latitudinal gradient, and if these latitudinal patterns varied across depth, in different benthic substrates, and over ecological time scales. Further, we subdivided our study area into three smaller regions to test whether coast-wide patterns of biodiversity held at regional scales, where local oceanographic processes tend to influence community structure and function. Overall, we found complex patterns of biodiversity on both the coast-wide and regional scales that differed by taxonomic group. Importantly, marine biodiversity was not always highest at low latitudes. We found that latitude, depth, substrate, and year were all important descriptors of fish and invertebrate diversity. Invertebrate richness and taxonomic diversity were highest at high latitudes and in deeper waters. Fish richness also increased with latitude, but exhibited a hump-shaped relationship with depth, increasing with depth up to the continental shelf break, ~200 m depth, and then decreasing in deeper waters. We found relationships between fish taxonomic and functional diversity and latitude, depth, substrate, and time at the regional scale, but not at the coast-wide scale, suggesting that coast-wide patterns can obscure important correlates at smaller scales. Our study provides insight into complex diversity patterns of the deep water soft substrate benthic ecosystems off the US West Coast.

Evaluating Temporal Consistency in Marine Biodiversity Hotspots.

With the ongoing crisis of biodiversity loss and limited resources for conservation, the concept of biodiversity hotspots has been useful in determining conservation priority areas. However, there has been limited research into how temporal variability in biodiversity may influence conservation area prioritization. To address this information gap, we present an approach to evaluate the temporal consistency of biodiversity hotspots in large marine ecosystems. Using a large scale, public monitoring dataset collected over an eight year period off the US Pacific Coast, we developed a methodological approach for avoiding biases associated with hotspot delineation. We aggregated benthic fish species data from research trawls and calculated mean hotspot thresholds for fish species richness and Shannon's diversity indices over the eight year dataset. We used a spatial frequency distribution method to assign hotspot designations to the grid cells annually. We found no areas containing consistently high biodiversity through the entire study period based on the mean thresholds, and no grid cell was designated as a hotspot for greater than 50% of the time-series. To test if our approach was sensitive to sampling effort and the geographic extent of the survey, we followed a similar routine for the northern region of the survey area. Our finding of low consistency in benthic fish biodiversity hotspots over time was upheld, regardless of biodiversity metric used, whether thresholds were calculated per year or across all years, or the spatial extent for which we calculated thresholds and identified hotspots. Our results suggest that static measures of benthic fish biodiversity off the US West Coast are insufficient for identification of hotspots and that long-term data are required to appropriately identify patterns of high temporal variability in biodiversity for these highly mobile taxa. Given that ecological communities are responding to a changing climate and other environmental perturbations, our work highlights the need for scientists and conservation managers to consider both spatial and temporal dynamics when designating biodiversity hotspots.

Density-dependent growth in invasive Lionfish (Pterois volitans).

Direct demographic density dependence is necessary for population regulation and is a central concept in ecology, yet has not been studied in many invasive species, including any invasive marine fish. The red lionfish (Pterois volitans) is an invasive predatory marine fish that is undergoing exponential population growth throughout the tropical western Atlantic. Invasive lionfish threaten coral-reef ecosystems, but there is currently no evidence of any natural population control. Therefore, a manipulative field experiment was conducted to test for density dependence in lionfish. Juvenile lionfish densities were adjusted on small reefs and several demographic rates (growth, recruitment, immigration, and loss) were measured throughout an 8-week period. Invasive lionfish exhibited direct density dependence in individual growth rates, as lionfish grew slower at higher densities throughout the study. Individual growth in length declined linearly with increasing lionfish density, while growth in mass declined exponentially with increasing density. There was no evidence, however, for density dependence in recruitment, immigration, or loss (mortality plus emigration) of invasive lionfish. The observed density-dependent growth rates may have implications for which native species are susceptible to lionfish predation, as the size and type of prey that lionfish consume is directly related to their body size. The absence of density-dependent loss, however, contrasts with many native coral-reef fish species and suggests that for the foreseeable future manual removals may be the only effective local control of this invasion.