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      Parasitism and host behavior in the context of a changing environment: The Holocene record of the commercially important bivalve Chamelea gallina, northern Italy

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          Abstract

          Rapid warming and sea-level rise are predicted to be major driving forces in shaping coastal ecosystems and their services in the next century. Though forecasts of the multiple and complex effects of temperature and sea-level rise on ecological interactions suggest negative impacts on parasite diversity, the effect of long term climate change on parasite dynamics is complex and unresolved. Digenean trematodes are complex life cycle parasites that can induce characteristic traces on their bivalve hosts and hold potential to infer parasite host-dynamics through time and space. Previous work has demonstrated a consistent association between sea level rise and increasing prevalence of trematode traces, but a number of fundamental questions remain unanswered about this paleoecological proxy. Here we examine the relationships of host size, shape, and functional morphology with parasite prevalence and abundance, how parasites are distributed across hosts, and how all of these relationships vary through time, using the bivalve Chamelea gallina from a Holocene shallow marine succession in the Po coastal plain. Trematode prevalence increased and decreased in association with the transition from a wave-influenced estuarine system to a wave-dominated deltaic setting. Prevalence and abundance of trematode pits are associated with large host body size, reflecting ontogenetic accumulation of parasites, but temporal trends in median host size do not explain prevalence trends. Ongoing work will test the roles of temperature, salinity, and nutrient availability on trematode parasitism. Parasitized bivalves in one sample were shallower burrowers than their non-parasitized counterparts, suggesting that hosts of trematodes can be more susceptible to their predators, though the effect is ephemeral. Like in living parasite-host systems, trematode-induced malformations are strongly aggregated among hosts, wherein most host individuals harbor very few parasites while a few hosts have many. We interpret trace aggregation to support the assumption that traces are a reliable proxy for trematode parasitism in the fossil record.

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          The impacts of climate change in coastal marine systems.

          Anthropogenically induced global climate change has profound implications for marine ecosystems and the economic and social systems that depend upon them. The relationship between temperature and individual performance is reasonably well understood, and much climate-related research has focused on potential shifts in distribution and abundance driven directly by temperature. However, recent work has revealed that both abiotic changes and biological responses in the ocean will be substantially more complex. For example, changes in ocean chemistry may be more important than changes in temperature for the performance and survival of many organisms. Ocean circulation, which drives larval transport, will also change, with important consequences for population dynamics. Furthermore, climatic impacts on one or a few 'leverage species' may result in sweeping community-level changes. Finally, synergistic effects between climate and other anthropogenic variables, particularly fishing pressure, will likely exacerbate climate-induced changes. Efforts to manage and conserve living marine systems in the face of climate change will require improvements to the existing predictive framework. Key directions for future research include identifying key demographic transitions that influence population dynamics, predicting changes in the community-level impacts of ecologically dominant species, incorporating populations' ability to evolve (adapt), and understanding the scales over which climate will change and living systems will respond.
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            The Split-Apply-Combine Strategy for Data Analysis

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              Is a healthy ecosystem one that is rich in parasites?

              Historically, the role of parasites in ecosystem functioning has been considered trivial because a cursory examination reveals that their relative biomass is low compared with that of other trophic groups. However there is increasing evidence that parasite-mediated effects could be significant: they shape host population dynamics, alter interspecific competition, influence energy flow and appear to be important drivers of biodiversity. Indeed they influence a range of ecosystem functions and have a major effect on the structure of some food webs. Here, we consider the bottom-up and top-down processes of how parasitism influences ecosystem functioning and show that there is evidence that parasites are important for biodiversity and production; thus, we consider a healthy system to be one that is rich in parasite species.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                1 April 2021
                2021
                : 16
                : 4
                : e0247790
                Affiliations
                [1 ] Department of Geological Sciences, University of Missouri, Columbia, Missouri, United States of America
                [2 ] Dipartimento di Scienze Biologiche, Geologiche e Ambientali, University of Bologna, Bologna, Italy
                University of California, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0001-9955-8853
                Article
                PONE-D-20-38744
                10.1371/journal.pone.0247790
                8016236
                33793588
                30ff74d7-852b-48df-bfaa-c925b0122dcf
                © 2021 Huntley, Scarponi

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 9 December 2020
                : 12 February 2021
                Page count
                Figures: 6, Tables: 2, Pages: 21
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000160, Division of Earth Sciences;
                Award ID: 1650745
                Award Recipient :
                Funded by: Alexander von Humboldt-Stiftung (DE)
                Award Recipient :
                Funded by: Institute of Advanced Studies, University of Bologna
                Award Recipient :
                Funded by: University of Missouri, Faculty Research Leave
                Award Recipient :
                Institute for Advanced Studies, University of Bologna (JWH) http://www.isa.unibo.it/en, Alexander von Humboldt Stiftung (JWH) https://www.humboldt-foundation.de/en/, MU Faculty Research Leave (JWH) https://missouri.edu/, NSF CAREER EAR-1650745 (JWH) https://www.nsf.gov/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Trematodes
                Biology and Life Sciences
                Zoology
                Animals
                Invertebrates
                Helminths
                Trematodes
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Flatworms
                Trematodes
                Biology and Life Sciences
                Zoology
                Animals
                Invertebrates
                Flatworms
                Trematodes
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Molluscs
                Bivalves
                Biology and Life Sciences
                Zoology
                Animals
                Invertebrates
                Molluscs
                Bivalves
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Parasitic Life Cycles
                Biology and Life Sciences
                Parasitology
                Parasitic Life Cycles
                Biology and Life Sciences
                Species Interactions
                Parasitism
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Earth Sciences
                Geology
                Geologic Time
                Cenozoic Era
                Quaternary Period
                Holocene Epoch
                Biology and Life Sciences
                Physiology
                Physiological Parameters
                Biology and Life Sciences
                Paleontology
                Fossils
                Fossil Record
                Earth Sciences
                Paleontology
                Fossils
                Fossil Record
                Custom metadata
                The minimal data set for our manuscript and all relevant R script are included in the Supporting information files.

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