Environment and shipping drive environmental DNA beta-diversity among commercial ports

Jose Andrés^{1

2}, Paul Czechowski^{1

3

4}, Erin Grey^{5

6}, Mandana Saebi⁷, Kara Andres^{1

2}, Christopher Brown⁸, Nitesh Chawla⁷, James J Corbett⁹, Rein Brys¹⁰, Phillip Cassey¹¹, Nancy Correa^{12

13}, Marty R Deveney¹⁴, Scott P Egan¹⁵, Joshua P Fisher¹⁶, Rian Vanden Hooff¹⁷, Charles R Knapp¹⁸, Sandric Chee Yew Leong¹⁹, Brian J Neilson²⁰, Esteban M Paolucci²¹, Michael E Pfrender²², Meredith R Pochardt²³, Thomas A A Prowse¹¹, Steven S Rumrill²⁴, Chris Scianni^{25

26}, Francisco Sylvester²⁷, Mario N Tamburri²⁸, Thomas W Therriault²⁹, Darren C J Yeo^{30

31}, David M Lodge^{1

2}

Affiliations

¹ Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York, USA.
² Cornell Atkinson Center for Sustainability, Cornell University, Ithaca, New York, USA.
³ Department of Anatomy, University of Otago, Dunedin, New Zealand.
⁴ Helmholtz Institute for Metabolic, Obesity and Vascular Research, Leipzig, Germany.
⁵ School of Biology and Ecology and Maine Center for Genetics in the Environment, University of Maine, Orono, Maine, USA.
⁶ Division of Science, Mathematics and Technology, Governors State University, University Park, Illinois, USA.
⁷ Center for Network and Data Science (CNDS), University of Notre Dame, Notre Dame, Indiana, USA.
⁸ Golden Bear Research Center, California State University Maritime Academy, Vallejo, California, USA.
⁹ College of Earth, Ocean, and Environment, University of Delaware, Newark, Delaware, USA.
¹⁰ Research Institute for Nature and Forest, Geraardsbergen, Belgium.
¹¹ School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia.
¹² Servicio de Hidrografía Naval (Ministerio de Defensa), Buenos Aires, Argentina.
¹³ Escuela de Ciencias del Mar, Sede Educativa Universitaria, Facultad de la Armada, UNDEF, Buenos Aires, Argentina.
¹⁴ SARDI Aquatic Science and Marine Innovation SA, South Australian Research and Development Institute, West Beach, South Australia, Australia.
¹⁵ Department of BioSciences, Rice University, Houston, Texas, USA.
¹⁶ United States Fish and Wildlife Service, Pacific Islands Fish and Wildlife Office, Honolulu, Hawaii, USA.
¹⁷ Oregon Department of Environmental Quality, Portland, Oregon, USA.
¹⁸ Daniel P. Haerther Center for Conservation and Research, Chicago, Illinois, USA.
¹⁹ St. John's Island National Marine Laboratory, Tropical Marine Science Institute, National University of Singapore, Singapore, Singapore.
²⁰ State of Hawaii Division of Aquatic Resources, Honolulu, Hawaii, USA.
²¹ Museo Argentino de Ciencias Naturales "Bernardino Rivadavia"-CONICET, Buenos Aires, Argentina.
²² Department of Biological Sciences and Environmental Change Initiative, University of Notre Dame, Notre Dame, Indiana, USA.
²³ M. Rose Consulting, Haines, Alaska, USA.
²⁴ Marine Resources Program, Oregon Department of Fish and Wildlife, Newport, Oregon, USA.
²⁵ California State Lands Commission, Marine Invasive Species Program, Long Beach, California, USA.
²⁶ Instituto para el Estudio de la Biodiversidad de Invertebrados, Facultad de Ciencias Naturales, Universidad Nacional de Salta, Salta, Argentina.
²⁷ Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Salta, Argentina.
²⁸ Chesapeake Biological Laboratory, University of Maryland Center for Environmental Science, Solomons, Maryland, USA.
²⁹ Fisheries and Oceans Canada, Pacific Biological Station, Nanaimo, British Columbia, Canada.
³⁰ Department of Biological Sciences, National University of Singapore, Singapore, Singapore.
³¹ Lee Kong Chian Natural History Museum, National University of Singapore, Singapore, Singapore.

PMID: 36799015
DOI: 10.1111/mec.16888

Environment and shipping drive environmental DNA beta-diversity among commercial ports

Jose Andrés et al. Mol Ecol. 2023 Dec.

. 2023 Dec;32(23):6696-6709.

doi: 10.1111/mec.16888. Epub 2023 Mar 28.

Authors

Affiliations

¹ Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York, USA.
² Cornell Atkinson Center for Sustainability, Cornell University, Ithaca, New York, USA.
³ Department of Anatomy, University of Otago, Dunedin, New Zealand.
⁴ Helmholtz Institute for Metabolic, Obesity and Vascular Research, Leipzig, Germany.
⁵ School of Biology and Ecology and Maine Center for Genetics in the Environment, University of Maine, Orono, Maine, USA.
⁶ Division of Science, Mathematics and Technology, Governors State University, University Park, Illinois, USA.
⁷ Center for Network and Data Science (CNDS), University of Notre Dame, Notre Dame, Indiana, USA.
⁸ Golden Bear Research Center, California State University Maritime Academy, Vallejo, California, USA.
⁹ College of Earth, Ocean, and Environment, University of Delaware, Newark, Delaware, USA.
¹⁰ Research Institute for Nature and Forest, Geraardsbergen, Belgium.
¹¹ School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia.
¹² Servicio de Hidrografía Naval (Ministerio de Defensa), Buenos Aires, Argentina.
¹³ Escuela de Ciencias del Mar, Sede Educativa Universitaria, Facultad de la Armada, UNDEF, Buenos Aires, Argentina.
¹⁴ SARDI Aquatic Science and Marine Innovation SA, South Australian Research and Development Institute, West Beach, South Australia, Australia.
¹⁵ Department of BioSciences, Rice University, Houston, Texas, USA.
¹⁶ United States Fish and Wildlife Service, Pacific Islands Fish and Wildlife Office, Honolulu, Hawaii, USA.
¹⁷ Oregon Department of Environmental Quality, Portland, Oregon, USA.
¹⁸ Daniel P. Haerther Center for Conservation and Research, Chicago, Illinois, USA.
¹⁹ St. John's Island National Marine Laboratory, Tropical Marine Science Institute, National University of Singapore, Singapore, Singapore.
²⁰ State of Hawaii Division of Aquatic Resources, Honolulu, Hawaii, USA.
²¹ Museo Argentino de Ciencias Naturales "Bernardino Rivadavia"-CONICET, Buenos Aires, Argentina.
²² Department of Biological Sciences and Environmental Change Initiative, University of Notre Dame, Notre Dame, Indiana, USA.
²³ M. Rose Consulting, Haines, Alaska, USA.
²⁴ Marine Resources Program, Oregon Department of Fish and Wildlife, Newport, Oregon, USA.
²⁵ California State Lands Commission, Marine Invasive Species Program, Long Beach, California, USA.
²⁶ Instituto para el Estudio de la Biodiversidad de Invertebrados, Facultad de Ciencias Naturales, Universidad Nacional de Salta, Salta, Argentina.
²⁷ Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Salta, Argentina.
²⁸ Chesapeake Biological Laboratory, University of Maryland Center for Environmental Science, Solomons, Maryland, USA.
²⁹ Fisheries and Oceans Canada, Pacific Biological Station, Nanaimo, British Columbia, Canada.
³⁰ Department of Biological Sciences, National University of Singapore, Singapore, Singapore.
³¹ Lee Kong Chian Natural History Museum, National University of Singapore, Singapore, Singapore.

PMID: 36799015
DOI: 10.1111/mec.16888

Abstract

The spread of nonindigenous species by shipping is a large and growing global problem that harms coastal ecosystems and economies and may blur coastal biogeographical patterns. This study coupled eukaryotic environmental DNA (eDNA) metabarcoding with dissimilarity regression to test the hypothesis that ship-borne species spread homogenizes port communities. We first collected and metabarcoded water samples from ports in Europe, Asia, Australia and the Americas. We then calculated community dissimilarities between port pairs and tested for effects of environmental dissimilarity, biogeographical region and four alternative measures of ship-borne species transport risk. We predicted that higher shipping between ports would decrease community dissimilarity, that the effect of shipping would be small compared to that of environment dissimilarity and shared biogeography, and that more complex shipping risk metrics (which account for ballast water and stepping-stone spread) would perform better. Consistent with our hypotheses, community dissimilarities increased significantly with environmental dissimilarity and, to a lesser extent, decreased with ship-borne species transport risks, particularly if the ports had similar environments and stepping-stone risks were considered. Unexpectedly, we found no clear effect of shared biogeography, and that risk metrics incorporating estimates of ballast discharge did not offer more explanatory power than simpler traffic-based risks. Overall, we found that shipping homogenizes eukaryotic communities between ports in predictable ways, which could inform improvements in invasive species policy and management. We demonstrated the usefulness of eDNA metabarcoding and dissimilarity regression for disentangling the drivers of large-scale biodiversity patterns. We conclude by outlining logistical considerations and recommendations for future studies using this approach.

Keywords: 18S; dissimilarity analysis; eDNA; metabarcoding; ports; shipping.

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References

REFERENCES

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Environment and shipping drive environmental DNA beta-diversity among commercial ports

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Environment and shipping drive environmental DNA beta-diversity among commercial ports

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