Corallivory in the Anthropocene: Interactive Effects of Anthropogenic Stressors and Corallivory on Coral Reefs

Corallivory is the predation of coral mucus, tissue, and skeleton by fishes and invertebrates, and a source of chronic stress for many reef-building coral species. Corallivores often prey on corals repeatedly, and this predation induces wounds that require extensive cellular resources to heal. The effects of corallivory on coral growth, reproduction, and community dynamics are well-documented, and often result in reduced growth rates and fitness. Given the degree of anthropogenic pressures that threaten coral reefs, it is now imperative to focus on understanding how corallivory interacts with anthropogenic forces to alter coral health and community dynamics. For example, coral bleaching events that stem from global climate change often reduce preferred corals species for many corallivorous fishes. These reductions in preferred prey may result in declines in populations of more specialized corallivores while more generalist corallivores may increase. Corallivory may also make corals more susceptible to thermal stress and exacerbate bleaching. At local scales, overfishing depletes corallivorous fish stocks, reducing fish corallivory and bioerosion, whilst removing invertivorous fishes and allowing population increases in invertebrate corallivores (e.g., urchins, Drupella spp.). Interactive effects of local stressors, such as overfishing and nutrient pollution, can alter the effect of corallivory by increasing coral-algal competition and destabilizing the coral microbiome, subsequently leading to coral disease and mortality. Here, we synthesize recent literature of how global climate change and local stressors affect corallivore populations and shape the patterns and effect of corallivory. Our review indicates that the combined effects of corallivory and anthropogenic pressures may be underappreciated and that these interactions often drive changes in coral reefs on scales from ecosystems to microbes. Understanding the ecology of coral reefs in the Anthropocene will require an increased focus on how anthropogenic forcing alters biotic interactions, such as corallivory, and the resulting cascading effects on corals and reef ecosystems

Cross-domain interactions confer stability to benthic biofilms in proglacial streams

Cross-domain interactions are an integral part of the success of biofilms in natural environments but remain poorly understood. Here, we describe cross-domain interactions in stream biofilms draining proglacial floodplains in the Swiss Alps. These streams, as a consequence of the retreat of glaciers, are characterised by multiple environmental gradients and perturbations (e.g., changes in channel geomorphology, discharge) that depend on the time since deglaciation. We evaluate co-occurrence of bacteria and eukaryotic communities along streams and show that key community members have disproportionate effects on the stability of community networks. The topology of the networks, here quantified as the arrangement of the constituent nodes formed by specific taxa, was independent of stream type and their apparent environmental stability. However, network stability against fragmentation was higher in the streams draining proglacial terrain that was more recently deglaciated. We find that bacteria, eukaryotic photoautotrophs, and fungi are central to the stability of these networks, which fragment upon the removal of both pro- and eukaryotic taxa. Key taxa are not always abundant, suggesting an underlying functional component to their contributions. Thus, we show that there is a key role played by individual taxa in determining microbial community stability of glacier-fed streams

The microbiome of cryospheric ecosystems.

peer reviewedThe melting of the cryosphere is among the most conspicuous consequences of climate change, with impacts on microbial life and related biogeochemistry. However, we are missing a systematic understanding of microbiome structure and function across cryospheric ecosystems. Here, we present a global inventory of the microbiome from snow, ice, permafrost soils, and both coastal and freshwater ecosystems under glacier influence. Combining phylogenetic and taxonomic approaches, we find that these cryospheric ecosystems, despite their particularities, share a microbiome with representatives across the bacterial tree of life and apparent signatures of early and constrained radiation. In addition, we use metagenomic analyses to define the genetic repertoire of cryospheric bacteria. Our work provides a reference resource for future studies on climate change microbiology

Cross-domain interactions confer stability to benthic biofilms in proglacial streams

Cross-domain interactions are an integral part of the success of biofilms in natural environments but remain poorly understood. Here, we describe cross-domain interactions in stream biofilms draining proglacial floodplains in the Swiss Alps. These streams, as a consequence of the retreat of glaciers, are characterised by multiple environmental gradients and perturbations (e.g., changes in channel geomorphology, discharge) that depend on the time since deglaciation. We evaluate co-occurrence of bacteria and eukaryotic communities along streams and show that key community members have disproportionate effects on the stability of community networks. The topology of the networks, here quantified as the arrangement of the constituent nodes formed by specific taxa, was independent of stream type and their apparent environmental stability. However, network stability against fragmentation was higher in the streams draining proglacial terrain that was more recently deglaciated. We find that bacteria, eukaryotic photoautotrophs, and fungi are central to the stability of these networks, which fragment upon the removal of both pro- and eukaryotic taxa. Key taxa are not always abundant, suggesting an underlying functional component to their contributions. Thus, we show that there is a key role played by individual taxa in determining microbial community stability of glacier-fed streams

Cross-domain interactions induce community stability to benthic biofilms in proglacial streams

AbstractCross-domain interactions are an integral part of the success of complex biofilms in natural environments. Here, we report on cross-domain interactions in biofilms of streams draining proglacial floodplains in the Swiss Alps. These streams, as a consequence of the retreat of glaciers, are characterized by multiple environmental gradients and stability that depend on the time since deglaciation. We estimate co-occurrence of prokaryotic and eukaryotic communities along this gradient and show that key community members have disproportionate effects on the stability of co-occurrence networks. The topology of the networks was similar independent of environmental gradients and stability. However, network stability was higher in the streams draining proglacial terrain that was more recently deglaciated. We find that both pro- and eukaryotes are central to the stability of these networks, which fragment upon the removal of both pro- and eukaryotic taxa. These ‘keyplayers’ are not always abundant, suggesting an underlying functional component to their contributions. Thus, we show that there is a key role played by individual taxa in determining microbial community stability of glacier-fed streams

Natural experiments and long-term monitoring are critical to understand and predict marine host-microbe ecology and evolution

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Leray, M., Wilkins, L. G. E., Apprill, A., Bik, H. M., Clever, F., Connolly, S. R., De Leon, M. E., Duffy, J. E., Ezzat, L., Gignoux-Wolfsohn, S., Herre, E. A., Kaye, J. Z., Kline, D. I., Kueneman, J. G., McCormick, M. K., McMillan, W. O., O’Dea, A., Pereira, T. J., Petersen, J. M., Petticord, D. F., Torchin, M. E., Thurber, R. V., Videvall, E., Wcislo, W. T., Yuen, B., Eisen, J. A. . Natural experiments and long-term monitoring are critical to understand and predict marine host-microbe ecology and evolution. Plos Biology, 19(8), (2021): e3001322, https://doi.org/10.1371/journal.pbio.3001322.Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host’s physiological capacities; however, the identity and functional role(s) of key members of the microbiome (“core microbiome”) in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems’ capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts’ plastic and adaptive responses to environmental change requires (i) recognizing that individual host–microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions.Financial support for the workshop was provided by grant GBMF5603 (https://doi.org/10.37807/GBMF5603) from the Gordon and Betty Moore Foundation (W.T. Wcislo, J.A. Eisen, co-PIs), and additional funding from the Smithsonian Tropical Research Institute and the Office of the Provost of the Smithsonian Institution (W.T. Wcislo, J.P. Meganigal, and R.C. Fleischer, co-PIs). JP was supported by a WWTF VRG Grant and the ERC Starting Grant 'EvoLucin'. LGEW has received funding from the European Union’s Framework Programme for Research and Innovation Horizon 2020 (2014-2020) under the Marie Sklodowska-Curie Grant Agreement No. 101025649. AO was supported by the Sistema Nacional de Investigadores (SENACYT, Panamá). A. Apprill was supported by NSF award OCE-1938147. D.I. Kline, M. Leray, S.R. Connolly, and M.E. Torchin were supported by a Rohr Family Foundation grant for the Rohr Reef Resilience Project, for which this is contribution #2. This is contribution #85 from the Smithsonian’s MarineGEO and Tennenbaum Marine Observatories Network.

Glacier shrinkage will accelerate downstream decomposition of organic matter and alters microbiome structure and function.

peer reviewedThe shrinking of glaciers is among the most iconic consequences of climate change. Despite this, the downstream consequences for ecosystem processes and related microbiome structure and function remain poorly understood. Here, using a space-for-time substitution approach across 101 glacier-fed streams (GFSs) from six major regions worldwide, we investigated how glacier shrinkage is likely to impact the organic matter (OM) decomposition rates of benthic biofilms. To do this, we measured the activities of five common extracellular enzymes and estimated decomposition rates by using enzyme allocation equations based on stoichiometry. We found decomposition rates to average 0.0129 (% d-1 ), and that decreases in glacier influence (estimated by percent glacier catchment coverage, turbidity, and a glacier index) accelerates decomposition rates. To explore mechanisms behind these relationships, we further compared decomposition rates with biofilm and stream water characteristics. We found that chlorophyll-a, temperature, and stream water N:P together explained 61% of the variability in decomposition. Algal biomass, which is also increasing with glacier shrinkage, showed a particularly strong relationship with decomposition, likely indicating their importance in contributing labile organic compounds to these carbon-poor habitats. We also found high relative abundances of chytrid fungi in GFS sediments, which putatively parasitize these algae, promoting decomposition through a fungal shunt. Exploring the biofilm microbiome, we then sought to identify bacterial phylogenetic clades significantly associated with decomposition, and found numerous positively (e.g., Saprospiraceae) and negatively (e.g., Nitrospira) related clades. Lastly, using metagenomics, we found evidence of different bacterial classes possessing different proportions of EEA-encoding genes, potentially informing some of the microbial associations with decomposition rates. Our results, therefore, present new mechanistic insights into OM decomposition in GFSs by demonstrating that an algal-based "green food web" is likely to increase in importance in the future and will promote important biogeochemical shifts in these streams as glaciers vanish

The effects of nutrient availability on the physiological response of tropical reef corals in the contexte of climate change

Les coraux constructeurs de récifs se développent généralement dans des eaux oligotrophes (i.e. : faibles concentrations en azote et phosphore (N, P)). Cette limitation se voit accentuée avec le réchauffement climatique. Cependant, aux abords des côtes, l'eutrophisation des eaux entraîne un excès de sels nutritifs, pouvant provoquer la rupture de l'association corail-dinoflagellés. Les buts principaux de cette thèse ont été d'évaluer: 1) l'utilisation de l'azote et du phosphore inorganique par les coraux dans diverses conditions environnementales; 2) l'effet d'une limitation ou d'un enrichissement en azote et/ou phosphore sur la physiologie corallienne. Les résultats ont montré que la forme et la source de N n'ont pas les mêmes effets sur la physiologie des coraux et que cet effet dépend également de la disponibilité en P. Sous faibles concentrations de P, un enrichissement en NH4+ stimule le métabolisme et maintient l'association symbiotique en période de stress. Au contraire, un excès de NO3- affecte négativement les processus de photosynthèse et de calcification, entrainant un blanchissement. Ces effets sont exacerbés en présence de matière organique particulaire, mais estompés en présence de phosphore. En effet, les résultats ont montré une très grande dépendance entre la présence en P et la santé corallienne. Ainsi, en période de stress thermique, les coraux ont la capacité d'augmenter leur taux d'absorption de phosphore. Ces travaux apportent des éclaircissements sur les relations existant entre la disponibilité en sels nutritifs et l'équilibre nutritionnel au sein de la symbiose, et devraient permettre d'affiner les stratégies de gestions des écosystèmes récifaux.Reef building corals are usually thriving in oligotrophic areas, characterized by low concentrations in inorganic nutrients, such as nitrogen and phosphorus. More, nutrient starvation is known to increase with global warming. However, along the urban coasts, water eutrophication induces nutrient excess, which could lead to the breakdown of the coraldinoflagellate symbiosis. The major aims of this thesis were to assess: 1) the use and uptake capacities of inorganic nitrogen and phosphorus by tropical corals according to environmental parameters; 2) the effects of nutrient limitation or enrichments in nitrogen and/or phosphorus on reef coral physiology. Results showed that corals response differed according to the chemical form, source of nitrogen and to the availability of phosphorus in the reef environment. In the presence of low phosphorus concentrations, ammonium supplementation enhanced coral metabolism and allowed coral colonies to overcome thermal stress. Conversely, nitrate enrichments negatively impacted photosynthesis and calcification processes, increasing coral bleaching susceptibility. These deleterious effects were enhanced when combined with organic matter supplementation, but repressed with addition of phosphorus. Indeed, results highlighted the tight relationship existing between phosphorus availability and coral health. During thermal stress, corals were able to increase their phosphorus uptake, this latter nutrient being essential for the holobiont metabolism. These outcomes shed a light into how marine symbioses cope with eutrophication, which is urgently required to refine risk management strategies

Effets de la disponibilité en sels nutritifs sur la réponse physiologique des coraux tropicaux dans le contexte du changement climatique

Reef building corals are usually thriving in oligotrophic areas, characterized by low concentrations in inorganic nutrients, such as nitrogen and phosphorus. More, nutrient starvation is known to increase with global warming. However, along the urban coasts, water eutrophication induces nutrient excess, which could lead to the breakdown of the coraldinoflagellate symbiosis. The major aims of this thesis were to assess: 1) the use and uptake capacities of inorganic nitrogen and phosphorus by tropical corals according to environmental parameters; 2) the effects of nutrient limitation or enrichments in nitrogen and/or phosphorus on reef coral physiology. Results showed that corals response differed according to the chemical form, source of nitrogen and to the availability of phosphorus in the reef environment. In the presence of low phosphorus concentrations, ammonium supplementation enhanced coral metabolism and allowed coral colonies to overcome thermal stress. Conversely, nitrate enrichments negatively impacted photosynthesis and calcification processes, increasing coral bleaching susceptibility. These deleterious effects were enhanced when combined with organic matter supplementation, but repressed with addition of phosphorus. Indeed, results highlighted the tight relationship existing between phosphorus availability and coral health. During thermal stress, corals were able to increase their phosphorus uptake, this latter nutrient being essential for the holobiont metabolism. These outcomes shed a light into how marine symbioses cope with eutrophication, which is urgently required to refine risk management strategies.Les coraux constructeurs de récifs se développent généralement dans des eaux oligotrophes (i.e. : faibles concentrations en azote et phosphore (N, P)). Cette limitation se voit accentuée avec le réchauffement climatique. Cependant, aux abords des côtes, l'eutrophisation des eaux entraîne un excès de sels nutritifs, pouvant provoquer la rupture de l'association corail-dinoflagellés. Les buts principaux de cette thèse ont été d'évaluer: 1) l'utilisation de l'azote et du phosphore inorganique par les coraux dans diverses conditions environnementales; 2) l'effet d'une limitation ou d'un enrichissement en azote et/ou phosphore sur la physiologie corallienne. Les résultats ont montré que la forme et la source de N n'ont pas les mêmes effets sur la physiologie des coraux et que cet effet dépend également de la disponibilité en P. Sous faibles concentrations de P, un enrichissement en NH4+ stimule le métabolisme et maintient l'association symbiotique en période de stress. Au contraire, un excès de NO3- affecte négativement les processus de photosynthèse et de calcification, entrainant un blanchissement. Ces effets sont exacerbés en présence de matière organique particulaire, mais estompés en présence de phosphore. En effet, les résultats ont montré une très grande dépendance entre la présence en P et la santé corallienne. Ainsi, en période de stress thermique, les coraux ont la capacité d'augmenter leur taux d'absorption de phosphore. Ces travaux apportent des éclaircissements sur les relations existant entre la disponibilité en sels nutritifs et l'équilibre nutritionnel au sein de la symbiose, et devraient permettre d'affiner les stratégies de gestions des écosystèmes récifaux