Out of shape: Ocean acidification simplifies coral reef architecture and reshuffles fish assemblages.

Climate change stressors are progressively simplifying biogenic habitats in the terrestrial and marine realms, and consequently altering the structure of associated species communities. Here, we used a volcanic CO2 seep in Papua New Guinea to test in situ if altered reef architecture due to ocean acidification reshuffles associated fish assemblages. We observed replacement of branching corals by massive corals at the seep, with simplified coral architectural complexity driving abundance declines between 60% and 86% for an assemblage of damselfishes associated with branching corals. An experimental test of habitat preference for a focal species indicated that acidification does not directly affect habitat selection behaviour, with changes in habitat structural complexity consequently appearing to be the stronger driver of assemblage reshuffling. Habitat health affected anti-predator behaviour, with P. moluccensis becoming less bold on dead branching corals relative to live branching corals, irrespective of ocean acidification. We conclude that coral reef fish assemblages are likely to be more sensitive to changes in habitat structure induced by increasing pCO2 than any direct effects on behaviour, indicating that changes in coral architecture and live cover may act as important mediators of reef fish community structures in a future ocean.

Ecological landscape explains aquifers microbial structure.

Aquifers have significant social, economic, and ecological importance. They supply 30 % of the freshwater for human consumption worldwide, including agricultural and industrial use. Despite aquifers' importance, the relationships between aquifer categories and their inhabiting microbial communities are still unknown. Characterizing variations within microbial communities' function and taxonomy structure at different aquifers could give a panoramic view of patterns that may enable the detection and prediction of environmental impact caused by multiple sources. Using publicly available shotgun metagenomic datasets, we examined whether soil properties, land use, and climate variables would have a more significant influence on the taxonomy and functional structure of the microbial communities than the ecological landscapes of the aquifer (i.e., Karst, Porous, Saline, Geyser, and Porous Contaminated). We found that these categories are stronger predictors of microbial communities' structure than geographical localization. In addition, our results show that microbial richness and dominance patterns are the opposite of those found in multicellular life, where extreme habitats harbour richer functional and taxonomic microbial communities. We found that low-abundant and recently described candidate taxa, such as the chemolithoautotrophic genus Candidatus Altiarcheum and the Candidate phylum Parcubacteria, are the main contributors to aquifer microbial communities' dissimilarities. Genes related to gram-negative bacteria proteins, cell wall structures, and phage activity were the primary contributors to aquifer microbial communities' dissimilarities among the aquifers' ecological landscapes. The results reported in the present study highlight the utility of using ecological landscapes for investigating aquifer microbial communities. In addition, we suggest that functions played by recently described and low abundant bacterial groups need further investigation once they might affect water quality, geochemical cycles, and the effects of anthropogenic disturbances such as pollution and climatic events on aquifers.

Behavioural generalism could facilitate coexistence of tropical and temperate fishes under climate change.

Coral-reef fishes are shifting their distributions poleward in response to human-mediated ocean warming; yet, the consequences for recipient temperate fish communities remain poorly understood. Behavioural modification is often the first response of species to environmental change, but we know little about how this might shape the ongoing colonisation by tropical fishes of temperate-latitude ecosystems under climate change. In a global hotspot of ocean warming (southeast Australia), we quantified 14 behavioural traits of invading tropical and local co-occurring temperate fishes at 10 sites across a 730 km latitudinal gradient as a proxy of species behavioural niche space in different climate ranges (subtropical, warm-temperate and cold-temperate). We found that tropical fishes (four species) modified their behavioural niches as well as increased their overall behavioural niche breadth in their novel temperate ranges where temperate species predominate, but maintained a moderate to high niche segregation with native temperate species across latitudinal range position. Temperate species (three co-occurring species) also modified their niches, but in contrast to tropical species, experienced an increased niche breadth towards subtropical ranges. Alterations to feeding and shoaling behaviours contributed most to niche modifications in tropical and temperate species, while behaviours related to alertness and escape from potential threats contributed least. We here show that at warmer and colder range edges where community structures are being reshuffled due to climate change, behavioural generalism and niche modification are potential mechanisms adopted by tropical range extenders and native temperate fishes to adjust to novel species interactions under climate change.

Positive species interactions strengthen in a high-CO2 ocean.

Negative interactions among species are a major force shaping natural communities and are predicted to strengthen as climate change intensifies. Similarly, positive interactions are anticipated to intensify and could buffer the consequences of climate-driven disturbances. We used in situ experiments at volcanic CO2 vents within a temperate rocky reef to show that ocean acidification can drive community reorganization through indirect and direct positive pathways. A keystone species, the algal-farming damselfish Parma alboscapularis, enhanced primary productivity through its weeding of algae whose productivity was also boosted by elevated CO2. The accelerated primary productivity was associated with increased densities of primary consumers (herbivorous invertebrates), which indirectly supported increased secondary consumers densities (predatory fish) (i.e. strengthening of bottom-up fuelling). However, this keystone species also reduced predatory fish densities through behavioural interference, releasing invertebrate prey from predation pressure and enabling a further boost in prey densities (i.e. weakening of top-down control). We uncover a novel mechanism where a keystone herbivore mediates bottom-up and top-down processes simultaneously to boost populations of a coexisting herbivore, resulting in altered food web interactions and predator populations under future ocean acidification.

Ocean acidification boosts reproduction in fish via indirect effects.

Ocean acidification affects species populations and biodiversity through direct negative effects on physiology and behaviour. The indirect effects of elevated CO2 are less well known and can sometimes be counterintuitive. Reproduction lies at the crux of species population replenishment, but we do not know how ocean acidification affects reproduction in the wild. Here, we use natural CO2 vents at a temperate rocky reef and show that even though ocean acidification acts as a direct stressor, it can indirectly increase energy budgets of fish to stimulate reproduction at no cost to physiological homeostasis. Female fish maintained energy levels by compensation: They reduced activity (foraging and aggression) to increase reproduction. In male fish, increased reproductive investment was linked to increased energy intake as mediated by intensified foraging on more abundant prey. Greater biomass of prey at the vents was linked to greater biomass of algae, as mediated by a fertilisation effect of elevated CO2 on primary production. Additionally, the abundance and aggression of paternal carers were elevated at the CO2 vents, which may further boost reproductive success. These positive indirect effects of elevated CO2 were only observed for the species of fish that was generalistic and competitively dominant, but not for 3 species of subordinate and more specialised fishes. Hence, species that capitalise on future resource enrichment can accelerate their reproduction and increase their populations, thereby altering species communities in a future ocean.

Trophic pyramids reorganize when food web architecture fails to adjust to ocean change.

As human activities intensify, the structures of ecosystems and their food webs often reorganize. Through the study of mesocosms harboring a diverse benthic coastal community, we reveal that food web architecture can be inflexible under ocean warming and acidification and unable to compensate for the decline or proliferation of taxa. Key stabilizing processes, including functional redundancy, trophic compensation, and species substitution, were largely absent under future climate conditions. A trophic pyramid emerged in which biomass expanded at the base and top but contracted in the center. This structure may characterize a transitionary state before collapse into shortened, bottom-heavy food webs that characterize ecosystems subject to persistent abiotic stress. We show that where food web architecture lacks adjustability, the adaptive capacity of ecosystems to global change is weak and ecosystem degradation likely.

Functional loss in herbivores drives runaway expansion of weedy algae in a near-future ocean.

The ability of a community to absorb environmental change without undergoing structural modification is a hallmark of ecological resistance. The recognition that species interactions can stabilize community processes has led to the idea that the effects of climate change may be less than what most considerations currently allow. We tested whether herbivory can compensate for the expansion of weedy algae triggered by CO2 enrichment and warming. Using a six-month mesocosm experiment, we show that increasing per capita herbivory by gastropods absorbs the boosted effects of CO2 enrichment on algal production in temperate systems of weak to moderate herbivory. However, under the combined effects of acidification and warming this compensatory effect was eroded by reducing the diversity, density and biomass of herbivores. This loss of functionality combined with boosted primary productivity drove a fourfold expansion of weedy algal species. Our results demonstrate capacity to buffer ecosystems against CO2 enrichment, but loss of this capacity through ocean warming either in isolation or combined with CO2, driving significant algal turf expansion. Identifying compensatory processes and the circumstances under which they prevail could potentially help manage the impacts of ocean warming and acidification, which are further amplified by local disturbances such as habitat loss and herbivore over-exploitation.

CO2 emissions boost the benefits of crop production by farming damselfish.

Farming is a technique employed by both humans and animals to enhance crop yields, allowing their populations to increase beyond the natural carrying capacity of the environment. Using volcanic CO2 vents, we investigate how a species of herbivorous fish (the black scalyfin Parma alboscapularis) may use increasing anthropogenic CO2 emissions to enhance its crop yields. We found that these farming fish can take advantage of this resource enrichment, to grow crops within smaller territories and increase the capacity of the environment to support more densely packed fish populations.

Boosted nutritional quality of food by CO2 enrichment fails to offset energy demand of herbivores under ocean warming, causing energy depletion and mortality.

The CO2-boosted trophic transfer from primary producers to herbivores has been increasingly discovered at natural CO2 vents and in laboratory experiments. Despite the emerging knowledge of this boosting effect, we do not know the extent to which it may be enhanced or dampened by ocean warming. We investigated whether ocean acidification and warming enhance the nutritional quality (C:N ratio) and energy content of turf algae, which is speculated to drive higher feeding rate, greater energy budget and eventually faster growth of herbivores. This proposal was tested by observing the physiological (feeding rate, respiration rate and energy budget) and demographic responses (growth and survival) of a common grazing gastropod (Phasianella australis) to ocean acidification and warming in a 6-month mesocosm experiment. Whilst we observed the boosting effect of ocean acidification and warming in isolation on the energy budget of herbivores by either increasing feeding rate on the more nutritious algae or increasing energy gain per feeding effort, their growth and survival were reduced by the sublethal thermal stress under ocean warming, especially when both climate change stressors were combined. This reduced growth and survival occurred as a consequence of depleted energy reserves, suggesting that the boosting effect via trophic transfer might not sufficiently compensate for the increased energy demand imposed by ocean warming. In circumstances where ocean acidification and warming create an energy demand on herbivores that outweighs the energy enhancement of their food (i.e. primary producers), the performance of herbivores to control their blooming resources likely deteriorates and thus runaway primary production ensues.

Species Interactions Drive Fish Biodiversity Loss in a High-CO2 World.

Accelerating climate change is eroding the functioning and stability of ecosystems by weakening the interactions among species that stabilize biological communities against change [1]. A key challenge to forecasting the future of ecosystems centers on how to extrapolate results from short-term, single-species studies to community-level responses that are mediated by key mechanisms such as competition, resource availability (bottom-up control), and predation (top-down control) [2]. We used CO2 vents as potential analogs of ocean acidification combined with in situ experiments to test current predictions of fish biodiversity loss and community change due to elevated CO2 [3] and to elucidate the potential mechanisms that drive such change. We show that high risk-taking behavior and competitive strength, combined with resource enrichment and collapse of predator populations, fostered already common species, enabling them to double their populations under acidified conditions. However, the release of these competitive dominants from predator control led to suppression of less common and subordinate competitors that did not benefit from resource enrichment and reduced predation. As a result, local biodiversity was lost and novel fish community compositions were created under elevated CO2. Our study identifies the species interactions most affected by ocean acidification, revealing potential sources of natural selection. We also reveal how diminished predator abundances can have cascading effects on local species diversity, mediated by complex species interactions. Reduced overfishing of predators could therefore act as a key action to stall diversity loss and ecosystem change in a high-CO2 world. VIDEO ABSTRACT.

Boosted food web productivity through ocean acidification collapses under warming.

Future climate is forecast to drive bottom-up (resource driven) and top-down (consumer driven) change to food web dynamics and community structure. Yet, our predictive understanding of these changes is hampered by an over-reliance on simplified laboratory systems centred on single trophic levels. Using a large mesocosm experiment, we reveal how future ocean acidification and warming modify trophic linkages across a three-level food web: that is, primary (algae), secondary (herbivorous invertebrates) and tertiary (predatory fish) producers. Both elevated CO2 and elevated temperature boosted primary production. Under elevated CO2 , the enhanced bottom-up forcing propagated through all trophic levels. Elevated temperature, however, negated the benefits of elevated CO2 by stalling secondary production. This imbalance caused secondary producer populations to decline as elevated temperature drove predators to consume their prey more rapidly in the face of higher metabolic demand. Our findings demonstrate how anthropogenic CO2 can function as a resource that boosts productivity throughout food webs, and how warming can reverse this effect by acting as a stressor to trophic interactions. Understanding the shifting balance between the propagation of resource enrichment and its consumption across trophic levels provides a predictive understanding of future dynamics of stability and collapse in food webs and fisheries production.

Dynamics of coral reef benthic assemblages of the Abrolhos Bank, eastern Brazil: inferences on natural and anthropogenic drivers.

The Abrolhos Bank (eastern Brazil) encompasses the largest and richest coral reefs of the South Atlantic. Coral reef benthic assemblages of the region were monitored from 2003 to 2008. Two habitats (pinnacles' tops and walls) were sampled per site with 3-10 sites sampled within different reef areas. Different methodologies were applied in two distinct sampling periods: 2003-2005 and 2006-2008. Spatial coverage and taxonomic resolution were lower in the former than in the latter period. Benthic assemblages differed markedly in the smallest spatial scale, with greater differences recorded between habitats. Management regimes and biomass of fish functional groups (roving and territorial herbivores) had minor influences on benthic assemblages. These results suggest that local environmental factors such as light, depth and substrate inclination exert a stronger influence on the structure of benthic assemblages than protection from fishing. Reef walls of unprotected coastal reefs showed highest coral cover values, with a major contribution of Montastraea cavernosa (a sediment resistant species that may benefit from low light levels). An overall negative relationship between fleshy macroalgae and slow-growing reef-building organisms (i.e. scleractinians and crustose calcareous algae) was recorded, suggesting competition between these organisms. The opposite trend (i.e. positive relationships) was recorded for turf algae and the two reef-building organisms, suggesting beneficial interactions and/or co-occurrence mediated by unexplored factors. Turf algae cover increased across the region between 2006 and 2008, while scleractinian cover showed no change. The need of a continued and standardized monitoring program, aimed at understanding drivers of change in community patterns, as well as to subsidize sound adaptive conservation and management measures, is highlighted.

Live coral predation by parrotfishes (Perciformes: Scaridae) in the Abrolhos Bank, eastern Brazil, with comments on the classification of species into functional groups

Parrotfishes (Perciformes: Scaridae) represent a critical functional group on coral reefs because their intense herbivory activity helps in avoiding coral overgrowth by algae. Although feeding preferentially on algae and detritus, some parrotfish species also consume live corals, leading to detrimental effects that may offset the benefits of removing competitive seaweeds. Parrotfish species differ markedly in terms of jaw morphology, foraging activity and extent of substratum excavation, and are typically divided into three functional groups: browsers, scrapers and excavators. The recognition of species within each functional group helps to understand their relative effects in terms of bioerosion, coral fitness and survival, habitat alteration and ecosystem dynamics. Here we report on live coral predation by the Brazilian endemic parrotfishes Scarus trispinosus and Sparisoma amplum in the largest coral reefs of the South Atlantic (Abrolhos Bank, eastern Brazil) and comment on their classification into functional groups based on direct behavioral observations. Scarus trispinosus and Sp. amplum allocated 0.8 percent and 8.1 percent of their bites to live corals respectively. Sparisoma amplum fed at lower rates, took shorter feeding forays and larger bites than Sc. trispinosus. Bite rates and foray size were negatively correlated to body size for Sc. trispinosus, but not for Sp. amplum. Our results indicate that Sp. amplum may be primarily recognized as an excavating species, as well as the most specialized parrotfish coral predator in Brazil, while Sc. trispinosus may be recognized as a scraper or excavator depending on its body size. This functional classification corresponds to the classification used for the putative sister taxa of Sc. trispinosus (Sc. coeruleus) and the sister taxa of Sp. amplum (Sp. viride) in the Caribbean, indicating that these two congeneric species pairs play similar ecological roles in different geographic regions.

Os budiões (Perciformes: Scaridae) representam um grupo funcional crítico em recifes de corais uma vez que a intensa atividade de herbivoria que desempenham ajuda a evitar a exclusão de corais por algas. Apesar de alimentarem-se preferencialmente de algas e detrito, algumas espécies de budiões também consomem corais vivos, causando efeitos negativos aos corais, os quais podem superar os benefícios decorrentes da remoção de algas. As espécies de budiões diferem acentuadamente em sua morfologia bucal, atividade de forrageio e potencial de escavação do substrato, sendo tipicamente divididas em três grupos funcionais: podadores, raspadores e escavadores. O reconhecimento das espécies nesses grupos funcionais ajuda a entender seus efeitos relativos em termos de bioerosão, condição e sobrevivência de corais, alteração do hábitat e dinâmica do ecossistema. No presente estudo nós registramos a predação de corais vivos pelos budiões endêmicos do Brasil Scarus trispinosus e Sparisoma amplum no maior complexo coralíneo do Atlântico Sul (Banco dos Abrolhos, leste do Brasil) e comentamos sobre a classificação dessas espécies em grupos funcionais com base em observações comportamentais. Scarus trispinosus e Sp. amplum alocaram 0.8 por cento e 8.1 por cento de suas mordidas a corais vivos respectivamente. Sparisoma amplum apresentou menores taxas alimentares, menor número de mordidas em seqüência e maior tamanho de mordidas que Sc. trispinosus. A taxa de mordidas e o número de mordidas em seqüência correlacionaram-se negativamente com o tamanho corporal para Sc. trispinosus, mas não para Sp. amplum. Nossos resultados indicam que Sp. amplum pode ser reconhecida como uma espécie primariamente escavadora, além do mais especializado budião predador de corais no Brasil, ao passo que Sc. trispinosus pode ser reconhecida como uma espécie raspadora ou escavadora, dependendo de seu tamanho corporal. Essa classificação funcional é similar àquela aplicada a suposta...