Consumer diversity interacts with prey defenses to drive ecosystem function.
TL;DR: The findings indicate that the total diet breadth of the herbivore community and the probability of all macroalgae being removed from reefs by herbivores increases with increasing Herbivore diversity, but that a few critical species drive this relationship.
Abstract: Prey traits linking consumer diversity to ecosystem function remain poorly understood. On tropical coral reefs, herbivores promote coral dominance by suppressing competing macroalgae, but the roles of herbivore identity and diversity, macroalgal defenses, and their interactions in affecting reef resilience and function are unclear. We studied adjacent pairs of no-take marine reserves and fished areas on reefs in Fiji and found that protected reefs supported 7–17× greater biomass, 2–3× higher species richness of herbivorous fishes, and 3–11× more live coral cover than did fished reefs. In contrast, macroalgae were 27–61× more abundant and 3–4× more species-rich on fished reefs. When we transplanted seven common macroalgae from fished reefs into reserves they were rapidly consumed, suggesting that rates of herbivory (ecosystem functioning) differed inside vs. outside reserves.
We then video-recorded feeding activity on the same seven macroalgae when transplanted into reserves, and assessed the functional redundancy vs. complementarity of herbivorous fishes consuming these macroalgae. Of 29 species of larger herbivorous fishes on these reefs, only four species accounted for 97% of macroalgal consumption. Two unicornfish consumed a range of brown macroalgae, a parrotfish consumed multiple red algae, and a rabbitfish consumed a green alga, with almost no diet overlap among these groups. The two most chemically rich, allelopathic algae were each consumed by a single, but different, fish species. This striking complementarity resulted from herbivore species differing in their tolerances to macroalgal chemical and structural defenses.
A model of assemblage diet breadth based on our feeding observations predicted that high browser diversity would be required for effective control of macroalgae on Fijian reefs. In support of this model, we observed strong negative relationships between herbivore diversity and macroalgal abundance and diversity across the six study reefs. Our findings indicate that the total diet breadth of the herbivore community and the probability of all macroalgae being removed from reefs by herbivores increases with increasing herbivore diversity, but that a few critical species drive this relationship. Therefore, interactions between algal defenses and herbivore tolerances create an essential role for consumer diversity in the functioning and resilience of coral reefs.
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University of Western Australia1, Curtin University2, Commonwealth Scientific and Industrial Research Organisation3, Australian Institute of Marine Science4, Australian Museum5, Australian National University6, Marine Biological Association of the United Kingdom7, University of Canterbury8, University of Las Palmas de Gran Canaria9
TL;DR: It is shown that extreme warming of a temperate kelp forest off Australia resulted not only in its collapse, but also in a shift in community composition that brought about an increase in herbivorous tropical fishes that prevent the reestablishment of kelp.
Abstract: Ecosystem reconfigurations arising from climate-driven changes in species distributions are expected to have profound ecological, social, and economic implications. Here we reveal a rapid climate-driven regime shift of Australian temperate reef communities, which lost their defining kelp forests and became dominated by persistent seaweed turfs. After decades of ocean warming, extreme marine heat waves forced a 100-kilometer range contraction of extensive kelp forests and saw temperate species replaced by seaweeds, invertebrates, corals, and fishes characteristic of subtropical and tropical waters. This community-wide tropicalization fundamentally altered key ecological processes, suppressing the recovery of kelp forests.
856 citations
University of New South Wales1, Georgia Institute of Technology2, Spanish National Research Council3, University of South Alabama4, University of Technology, Sydney5, New South Wales Department of Primary Industries6, University of Sydney7, University of Western Australia8, Macquarie University9, University of Queensland10, Kōchi University11, Marine Biological Association of the United Kingdom12, Oregon State University13
TL;DR: It is argued that this phase shift is facilitated by poleward-flowing boundary currents that are creating ocean warming hotspots around the globe, enabling the range expansion of tropical species and increasing their grazing rates in temperate areas.
Abstract: Climate-driven changes in biotic interactions can profoundly alter ecological communities, particularly when they impact foundation species. In marine systems, changes in herbivory and the consequent loss of dominant habitat forming species can result in dramatic community phase shifts, such as from coral to macroalgal dominance when tropical fish herbivory decreases, and from algal forests to ‘barrens’ when temperate urchin grazing increases. Here, we propose a novel phase-shift away from macroalgal dominance caused by tropical herbivores extending their range into temperate regions. We argue that this phase shift is facilitated by poleward-flowing boundary currents that are creating ocean warming hotspots around the globe, enabling the range expansion of tropical species and increasing their grazing rates in temperate areas. Overgrazing of temperate macroalgae by tropical herbivorous fishes has already occurred in Japan and the Mediterranean. Emerging evidence suggests similar phenomena are occurring in other temperate regions, with increasing occurrence of tropical fishes on temperate reefs.
721 citations
TL;DR: Although conditions governing regime shift or recovery dynamics were diverse, pre-disturbance quantification of simple factors such as structural complexity and water depth accurately predicted ecosystem trajectories, foreshadow the likely divergent but predictable outcomes for reef ecosystems in response to climate change.
Abstract: Climate-induced coral bleaching is among the greatest current threats to coral reefs, causing widespread loss of live coral cover1. Conditions under which reefs bounce back from bleaching events or shift from coral to algal dominance are unknown, making it difficult to predict and plan for differing reef responses under climate change2. Here we document and predict long-term reef responses to a major climate-induced coral bleaching event that caused unprecedented region-wide mortality of Indo-Pacific corals. Following loss of >90% live coral cover, 12 of 21 reefs recovered towards pre-disturbance live coral states, while nine reefs underwent regime shifts to fleshy macroalgae. Functional diversity of associated reef fish communities shifted substantially following bleaching, returning towards pre-disturbance structure on recovering reefs, while becoming progressively altered on regime shifting reefs. We identified threshold values for a range of factors that accurately predicted ecosystem response to the bleaching event. Recovery was favoured when reefs were structurally complex and in deeper water, when density of juvenile corals and herbivorous fishes was relatively high and when nutrient loads were low. Whether reefs were inside no-take marine reserves had no bearing on ecosystem trajectory. Although conditions governing regime shift or recovery dynamics were diverse, pre-disturbance quantification of simple factors such as structural complexity and water depth accurately predicted ecosystem trajectories. These findings foreshadow the likely divergent but predictable outcomes for reef ecosystems in response to climate change, thus guiding improved management and adaptation.
589 citations
TL;DR: An increase in the proportion of warmwater species (“tropicalization”) as oceans warm is increasing fish herbivory in kelp forests, contributing to their decline and subsequent persistence in alternate “kelp-free” states, and posing a significant threat to kelp-dominated ecosystems in Australia and globally.
Abstract: Some of the most profound effects of climate change on ecological communities are due to alterations in species interactions rather than direct physiological effects of changing environmental conditions. Empirical evidence of historical changes in species interactions within climate-impacted communities is, however, rare and difficult to obtain. Here, we demonstrate the recent disappearance of key habitat-forming kelp forests from a warming tropical-temperate transition zone in eastern Australia. Using a 10-y video dataset encompassing a 0.6 °C warming period, we show how herbivory increased as kelp gradually declined and then disappeared. Concurrently, fish communities from sites where kelp was originally abundant but subsequently disappeared became increasingly dominated by tropical herbivores. Feeding assays identified two key tropical/subtropical herbivores that consumed transplanted kelp within hours at these sites. There was also a distinct increase in the abundance of fishes that consume epilithic algae, and much higher bite rates by this group at sites without kelp, suggesting a key role for these fishes in maintaining reefs in kelp-free states by removing kelp recruits. Changes in kelp abundance showed no direct relationship to seawater temperatures over the decade and were also unrelated to other measured abiotic factors (nutrients and storms). Our results show that warming-mediated increases in fish herbivory pose a significant threat to kelp-dominated ecosystems in Australia and, potentially, globally.
307 citations
Cites result from "Consumer diversity interacts with p..."
...Although such synergistic effects of warming remain to be confirmed, these findings are consistent with a growing body of literature that shows how the full suppression of large seaweeds on reefs is mediated by increases in herbivore functional diversity and feeding complementarity among herbivores (18, 21, 27)....
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TL;DR: The results demonstrate that crucial ecosystem functions can be maintained through a range of fisheries restrictions, allowing coral reef managers to develop recovery plans that meet conservation and livelihood objectives in areas where marine reserves are not socially or politically feasible solutions.
Abstract: Continuing degradation of coral reef ecosystems has generated substantial interest in how management can support reef resilience(1,2). Fishing is the primary source of diminished reef function globally(3-5), leading to widespread calls for additional marine reserves to recover fish biomass and restore key ecosystem functions(6). Yet there are no established baselines for determining when these conservation objectives have been met or whether alternative management strategies provide similar ecosystem benefits. Here we establish empirical conservation benchmarks and fish biomass recovery timelines against which coral reefs can be assessed and managed by studying the recovery potential of more than 800 coral reefs along an exploitation gradient. We show that resident reef fish biomass in the absence of fishing (B-0) averages similar to 1,000 kg ha(-1), and that the vast majority (83%) of fished reefs are missing more than half their expected biomass, with severe consequences for key ecosystem functions such as predation. Given protection from fishing, reef fish biomass has the potential to recover within 35 years on average and less than 60 years when heavily depleted. Notably, alternative fisheries restrictions are largely (64%) successful at maintaining biomass above 50% of B-0, sustaining key functions such as herbivory. Our results demonstrate that crucial ecosystem functions can be maintained through a range of fisheries restrictions, allowing coral reef managers to develop recovery plans that meet conservation and livelihood objectives in areas where marine reserves are not socially or politically feasible solutions.
267 citations
References
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Book•
03 Feb 1984
TL;DR: This paper presents the results of a series of experiments conducted in farmers' fields in the Czech Republic over a period of three years to investigate the effects of agricultural pesticides on animal welfare and human health.
Abstract: Elements of Experimentation. Single-Factor Experiments. Two-Factor Experiments. Three-or More-Factor Experiments. Comparison Between Treatment Means. Analysis of Multiobservation Data. Problem Data. Analysis of Data from a Series of Experiments. Regression and Correlation Analysis. Covariance Analysis. Chi-Square Test. Soil Heterogeneity. Competition Effects. Mechanical Errors. Sampling in Experimental Plots. Experiments in Farmers' Fields. Presentation of Experimental Results. Appendices. Index.
13,377 citations
Book•
21 Mar 2002TL;DR: An essential textbook for any student or researcher in biology needing to design experiments, sample programs or analyse the resulting data is as discussed by the authors, covering both classical and Bayesian philosophies, before advancing to the analysis of linear and generalized linear models Topics covered include linear and logistic regression, simple and complex ANOVA models (for factorial, nested, block, split-plot and repeated measures and covariance designs), and log-linear models Multivariate techniques, including classification and ordination, are then introduced.
Abstract: An essential textbook for any student or researcher in biology needing to design experiments, sample programs or analyse the resulting data The text begins with a revision of estimation and hypothesis testing methods, covering both classical and Bayesian philosophies, before advancing to the analysis of linear and generalized linear models Topics covered include linear and logistic regression, simple and complex ANOVA models (for factorial, nested, block, split-plot and repeated measures and covariance designs), and log-linear models Multivariate techniques, including classification and ordination, are then introduced Special emphasis is placed on checking assumptions, exploratory data analysis and presentation of results The main analyses are illustrated with many examples from published papers and there is an extensive reference list to both the statistical and biological literature The book is supported by a website that provides all data sets, questions for each chapter and links to software
9,509 citations
Dalhousie University1, University of Wyoming2, Plymouth Marine Laboratory3, Stockholm University4, Royal Swedish Academy of Sciences5, University of California, Santa Barbara6, Scripps Institution of Oceanography7, Smithsonian Tropical Research Institute8, Stanford University9, University of California, Davis10, University of British Columbia11
TL;DR: The authors analyzed local experiments, long-term regional time series, and global fisheries data to test how biodiversity loss affects marine ecosystem services across temporal and spatial scales, concluding that marine biodiversity loss is increasingly impairing the ocean's capacity to provide food, maintain water quality, and recover from perturbations.
Abstract: Human-dominated marine ecosystems are experiencing accelerating loss of populations and species, with largely unknown consequences. We analyzed local experiments, long-term regional time series, and global fisheries data to test how biodiversity loss affects marine ecosystem services across temporal and spatial scales. Overall, rates of resource collapse increased and recovery potential, stability, and water quality decreased exponentially with declining diversity. Restoration of biodiversity, in contrast, increased productivity fourfold and decreased variability by 21%, on average. We conclude that marine biodiversity loss is increasingly impairing the ocean's capacity to provide food, maintain water quality, and recover from perturbations. Yet available data suggest that at this point, these trends are still reversible.
3,672 citations
"Consumer diversity interacts with p..." refers background in this paper
...Biodiversity promotes the function, stability, and productivity of ecosystems, as well as the services they provide to human societies (Balvanera et al. 2006, Cardinale et al. 2006, Worm et al. 2006)....
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University of California, Santa Cruz1, Duke University2, University of California, Berkeley3, University of Montana4, University of Cape Town5, University of Wisconsin-Madison6, University of Washington7, University of Florida8, Scripps Institution of Oceanography9, University of Missouri–St. Louis10, Finnmark University College11, University of Turku12, Stony Brook University13, Oregon State University14, Wageningen University and Research Centre15, University of California, Davis16, University of British Columbia17, University of Oulu18, Swedish University of Agricultural Sciences19
TL;DR: This empirical work supports long-standing theory about the role of top-down forcing in ecosystems but also highlights the unanticipated impacts of trophic cascades on processes as diverse as the dynamics of disease, wildfire, carbon sequestration, invasive species, and biogeochemical cycles.
Abstract: Until recently, large apex consumers were ubiquitous across the globe and had been for millions of years. The loss of these animals may be humankind's most pervasive influence on nature. Although such losses are widely viewed as an ethical and aesthetic problem, recent research reveals extensive cascading effects of their disappearance in marine, terrestrial, and freshwater ecosystems worldwide. This empirical work supports long-standing theory about the role of top-down forcing in ecosystems but also highlights the unanticipated impacts of trophic cascades on processes as diverse as the dynamics of disease, wildfire, carbon sequestration, invasive species, and biogeochemical cycles. These findings emphasize the urgent need for interdisciplinary research to forecast the effects of trophic downgrading on process, function, and resilience in global ecosystems.
3,130 citations
"Consumer diversity interacts with p..." refers background in this paper
...Consumers often have cascading effects on the structure and function of terrestrial, aquatic, and marine ecosystems (Pace et al. 1999, Estes et al. 2011)....
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...Our findings have worrisome conservation implications, because critical ecosystem processes may rapidly deteriorate when only one, or a few, key consumers are locally extirpated (Estes et al. 2011, O’Gorman et al. 2011, Bellwood et al. 2012)....
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...Consumers impact ecosystem function through topdown forcing (Ives et al. 2005, Duffy et al. 2007, Estes et al. 2011), and consumers are likely more vulnerable to localized extinction than primary producers (Duffy 2003), yet our understanding of how consumer diversity affects real-world ecosystems…...
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TL;DR: The ecological roles of critical functional groups (for both corals and reef fishes) that are fundamental to understanding resilience and avoiding phase shifts from coral dominance to less desirable, degraded ecosystems are reviewed.
Abstract: The worldwide decline of coral reefs calls for an urgent reassessment of current management practices. Confronting large-scale crises requires a major scaling-up of management efforts based on an improved understanding of the ecological processes that underlie reef resilience. Managing for improved resilience, incorporating the role of human activity in shaping ecosystems, provides a basis for coping with uncertainty, future changes and ecological surprises. Here we review the ecological roles of critical functional groups (for both corals and reef fishes) that are fundamental to understanding resilience and avoiding phase shifts from coral dominance to less desirable, degraded ecosystems. We identify striking biogeographic differences in the species richness and composition of functional groups, which highlight the vulnerability of Caribbean reef ecosystems. These findings have profound implications for restoration of degraded reefs, management of fisheries, and the focus on marine protected areas and biodiversity hotspots as priorities for conservation.
3,032 citations