Direct and Interactive Effects of Enemies and Mutualists on Plant Performance: A Meta-Analysis

Plants engage in multiple, simultaneous interactions with other species; some (enemies) reduce and others (mutualists) enhance plant performance. Moreover, effects of different species may not be independent of one another; for example, enemies may compete, reducing their negative impact on a plant. The magnitudes of positive and negative effects, as well as the frequency of interactive effects and whether they tend to enhance or depress plant performance, have never been comprehensively assessed across the many published studies on plant–enemy and plant–mutualist interactions. We performed a meta-analysis of experiments in which two enemies, two mutualists, or an enemy and a mutualist were manipulated factorially. Specifically, we performed a factorial meta-analysis using the log response ratio. We found that the magnitude of (negative) enemy effects was greater than that of (positive) mutualist effects in isolation, but in the presence of other species, the two effects were of comparable magnitude. Hence studies evaluating single-species effects of mutualists may underestimate the true effects found in natural settings, where multiple interactions are the norm and indirect effects are possible. Enemies did not on average influence the effects on plant performance of other enemies, nor did mutualists influence the effects of mutualists. However, these averages mask significant and large, but positive or negative, interactions in individual studies. In contrast, mutualists ameliorated the negative effects of enemies in a manner that benefited plants; this overall effect was driven by interactions between pathogens and belowground mutualists (bacteria and mycorrhizal fungi). The high frequency of significant interactive effects suggests a widespread potential for diffuse rather than pairwise coevolutionary interactions between plants and their enemies and mutualists. Pollinators and mycorrhizal fungi enhanced plant performance more than did bacterial mutualists. In the greenhouse (but not the field), pathogens reduced plant performance more than did herbivores, pathogens were more damaging to herbaceous than to woody plants, and herbivores were more damaging to crop than to non-crop plants (suggesting evolutionary change in plants or herbivores following crop domestication). We discuss how observed differences in effect size might be confounded with methodological differences among studies

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.

INVASIVESNET towards an International Association for Open Knowledge on Invasive Alien Species

In a world where invasive alien species (IAS) are recognised as one of the major threats to biodiversity, leading scientists from five continents have come together to propose the concept of developing an international association for open knowledge and open data on IAS—termed “INVASIVESNET”. This new association will facilitate greater understanding and improved management of invasive alien species (IAS) and biological invasions globally, by developing a sustainable network of networks for effective knowledge exchange. In addition to their inclusion in the CBD Strategic Plan for Biodiversity, the increasing ecological, social, cultural and economic impacts associated with IAS have driven the development of multiple legal instruments and policies. This increases the need for greater co-ordination, co-operation, and information exchange among scientists, management, the community of practice and the public. INVASIVESNET will be formed by linking new and existing networks of interested stakeholders including international and national expert working groups and initiatives, individual scientists, database managers, thematic open access journals, environmental agencies, practitioners, managers, industry, non-government organisations, citizens and educational bodies. The association will develop technical tools and cyberinfrastructure for the collection, management and dissemination of data and information on IAS; create an effective communication platform for global stakeholders; and promote coordination and collaboration through international meetings, workshops, education, training and outreach. To date, the sustainability of many strategic national and international initiatives on IAS have unfortunately been hampered by time-limited grants or funding cycles. Recognising that IAS initiatives need to be globally coordinated and ongoing, we aim to develop a sustainable knowledge sharing association to connect the outputs of IAS research and to inform the consequential management and societal challenges arising from IAS introductions. INVASIVESNET will provide a dynamic and enduring network of networks to ensure the continuity of connections among the IAS community of practice, science and management

Effects of Parasites on the Impact of Exotic Marine Species

Human activities, particularly shipping and transport, have introduced many exotic species worldwide. Although the effects of most introductions are undetectable, certain species have dramatic ecological and economic impacts. After habitat destruction, invasive species are the largest key threats to biodiversity. The only certainty about invasive species is that they will continue to emerge as an environmental problem. Despite heightened awareness about the threat of invasions to natural ecosystems, we still have a poor understanding of the mechanisms responsible for invasion success. A prominent, but untested, hypothesis explaining the success of introduced species is that they are relatively free of the effects of natural enemies. Most notably, they may be subject to fewer parasites in their introduced range compared to their native range. For my dissertation research I developed a theoretical framework to model invasion success. I also evaluated the effects of parasites on the invasion success and impacts of three exotic marine and estuarine species, a crab, a snail and a fish. Finally, to determine the generality of this hypothesis, in a meta-analysis, I examined parasite presence and prevalence in host species from a broad range of taxa, including molluscs, crustaceans, fishes, birds, mammals, amphibians and reptiles over a wide range of ecologies from terrestrial, freshwater and marine systems.Some parasites of exotic hosts were introduced from the native range to the introduced range, and some native parasites colonized introduced hosts. Still, introduced populations of invasive species were substantially and significantly less parasitized compared to native populations, both in terms of parasite species richness and prevalence. Evidence from native green crab populations suggests that some parasites can significantly decrease both size of individuals and biomass of populations. Taken together, the loss of native parasites and the limitation of local parasites to become established in exotic hosts may explain why some invasive species are such successful invaders and cause significant ecological impacts

Effects of Parasites on the Impact of Exotic Marine Species

Human activities, particularly shipping and transport, have introduced many exotic species worldwide. Although the effects of most introductions are undetectable, certain species have dramatic ecological and economic impacts. After habitat destruction, invasive species are the largest key threats to biodiversity. The only certainty about invasive species is that they will continue to emerge as an environmental problem. Despite heightened awareness about the threat of invasions to natural ecosystems, we still have a poor understanding of the mechanisms responsible for invasion success. A prominent, but untested, hypothesis explaining the success of introduced species is that they are relatively free of the effects of natural enemies. Most notably, they may be subject to fewer parasites in their introduced range compared to their native range. For my dissertation research I developed a theoretical framework to model invasion success. I also evaluated the effects of parasites on the invasion success and impacts of three exotic marine and estuarine species, a crab, a snail and a fish. Finally, to determine the generality of this hypothesis, in a meta-analysis, I examined parasite presence and prevalence in host species from a broad range of taxa, including molluscs, crustaceans, fishes, birds, mammals, amphibians and reptiles over a wide range of ecologies from terrestrial, freshwater and marine systems.Some parasites of exotic hosts were introduced from the native range to the introduced range, and some native parasites colonized introduced hosts. Still, introduced populations of invasive species were substantially and significantly less parasitized compared to native populations, both in terms of parasite species richness and prevalence. Evidence from native green crab populations suggests that some parasites can significantly decrease both size of individuals and biomass of populations. Taken together, the loss of native parasites and the limitation of local parasites to become established in exotic hosts may explain why some invasive species are such successful invaders and cause significant ecological impacts