Gimme shelter: Seven new leech species call freshwater mussels home

The frequent presence of leeches with a hidden lifestyle in the mantle cavity of freshwater mussels has been recorded since the second half of the 19th century. Yet this was, until now, regarded as an accidental phenomenon. Recent research not only reveals seven mussel-associated leech species new to science, but also shows that their association evolved over millions of years.

The diverse ecological group of leeches were found inside more than 3,000 freshwater mussels collected (by numerous collaborators) from East Asia, Southeast Asia, India and Nepal, Africa and North America between 2002 and 2018. Arthur Bogan, Research Curator of Mollusks for the North Carolina Museum of Natural Sciences, was part of the massive collecting effort and focused his search on parts of eastern Russia (Vladivostok area), Japan and Myanmar.

The study’s novel data reveals that at least two groups of mussel-associated leech species could be considered obligate inhabitants of the mantle cavity of freshwater mussels, meaning they cannot complete their lifecycle without exploiting their host. How did this come about? According to lead author Ivan N. Bolotov of the Federal Center for Integrated Arctic Research of the Russian Academy of Sciences, “It has been suggested that the primary selective pressure driving the evolution of parental care in leeches may have been predation on leech eggs and juvenile stages. From this point of view, [this lifestyle] could be considered a progressive evolutionary trait in brooding behavior helping to protect juvenile stages from predators.

“To estimate divergence times for mussel-associated leech clades, we calculated the first fossil-calibrated global phylogeny of leeches using a fossil leech cocoon from mid-Triassic lacustrine deposits in Antarctica as a calibration. It was found that leeches are slowly evolving animals as several other ‘living fossil’ taxa, for example freshwater mussels, coelacanths, anthozoans, sturgeons and puddle fishes. The reliable mutation rates obtained by us are of great importance to future evolutionary studies of these worms.”

The study also showed that even these leech species are not permanent residents. Molecular studies of the digestive system content of the adult mussel-associated leeches indicate that they leave their mussel hosts periodically to obtain blood of freshwater fishes. Probably, adult leeches need to use one or several higher-calorie fish blood meals instead of nutritionally sparse mussel haemolymph (body fluids of invertebrates) to ensure the successful development of eggs and complete their life cycle. While larvae and juvenile mussel-associated leeches could feed on mucus and body fluids of freshwater mussels.

Such a two-host feeding behavior, when fish blood meals are needed at the final stage of the lifecycle just before leech reproduction, appears to be a successful adaptation to a freshwater environment, in which availability of vertebrate blood is limited, and many leech species are forced to use nutrient-poor haemolymph as the primary feeding source.

The discovery of this mussel-leech association has wider ranging importance because freshwater mussels are one of the most imperiled animal groups worldwide, revealing the fastest rates of extinction. Habitat degradation, river pollution and climate change are the primary causes of global decline. However, biological threats for freshwater mussels are still poorly known.

The findings were published in Scientific Reports in November.

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Note to Editors: The study abstract follows.

“Freshwater mussels house a diverse mussel-associated leech assemblage”

Published: Nov. 11, 2019, Scientific Reports

DOI: 10.1038/s41598-019-52688-3

Abstract: Freshwater mussels (Unionida) are one of the most imperiled animal groups worldwide, revealing the fastest rates of extinction. Habitat degradation, river pollution and climate change are the primary causes of global decline. However, biological threats for freshwater mussels are still poorly known. Here, we describe a diverse ecological group of leeches (Hirudinea: Glossiphoniidae) inhabiting the mantle cavity of freshwater mussels. So far, examples of mussel-associated leech species are recorded from East Asia, Southeast Asia, India and Nepal, Africa, and North America. This group comprises a dozen glossiphoniid species with a hidden lifestyle inside the mantle cavity of their hosts largely overlooked by researchers. We show that the association with freshwater mussels evolved independently in three leech clades, i.e. Batracobdelloides, Hemiclepsis, and Placobdella, at least since the Miocene. Seven mussel-associated leech species and two additional free-living taxa are described here as new to science

Authors

Ivan N. Bolotov 1,2,3*, Anna L. Klass 1, Alexander V. Kondakov 1,2,3, Ilya V. Vikhrev 1,2,3, Yulia V. Bespalaya 1,2,3, Mikhail Yu Gofarov 1,2, Boris Yu Filippov 1,2, Arthur E. Bogan 4, Manuel Lopes-Lima 5,6,7, Zau Lunn 8, Nyein Chan 8, Olga V. Aksenova 1,2,3, Gennady A. Dvoryankin 2, Yulia E. Chapurina 1,2, Sang Ki Kim 9, Yulia S. Kolosova 1,2, Ekaterina S. Konopleva 1,2, Jin Hee Lee 10, Alexander A. Makhrov 3,11, Dmitry M. Palatov 11,12, Elena M. Sayenko 13, Vitaly M. Spitsyn 1,2, Svetlana E. Sokolova 2, Alena A. Tomilova 2, Than Win 14, Natalia A. Zubrii 1,2 & Maxim V. Vinarski 3

1 Northern Arctic Federal University, Arkhangelsk, Russia. 2 Federal Center for Integrated Arctic Research, Russian Academy of Sciences, Arkhangelsk, Russia. 3 Laboratory of Macroecology & Biogeography of Invertebrates, Saint Petersburg State University, Saint Petersburg, Russia. 4 Research Laboratory, North Carolina Museum of Natural Sciences, Raleigh, North Carolina, United States of America. 5 CIBIO/InBIO – Research Center in Biodiversity and Genetic Resources, University of Porto, Campus Agrário de Vairão, Vairão, Portugal. 6 CIIMAR/CIMAR – Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Terminal de Cruzeiros do Porto de Leixões, Matosinhos, Portugal. 7 SSC/IUCN – Mollusc Specialist Group, Species Survival Commission, International Union for Conservation of Nature, Cambridge, United Kingdom. 8 Fauna & Flora International – Myanmar Program, Yangon, Myanmar. 9 Nakdonggang National Institute of Biological Resources, Gyeongsangbuk-do, Korea. 10 Daegu Science High School, Daegu, Korea. 11 A. N. Severtzov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia. 12 Lomonosov Moscow State University, Moscow, Russia. 13 Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the Russian Academy of Sciences, Vladivostok, Russia. 1 4Department of Zoology, Hpa-An University, Hpa-An, Kayin State, Myanmar.

Funding / Acknowledgements

The Russian Ministry of Science and Higher Education partly funded the fieldworks in South Korea and East Africa (I.V.V. and M.Y.G.) under project No. AAAA-A18-118012390161-9. The National Geographic Society partly funded the leech collecting in Myanmar (A.E.B., M.L.L., I.N.B., I.V.V., Z.L., and N.C.) under project No. NGS-274R-18. The Russian Ministry of Science and Higher Education supported the molecular analyses of the leech samples under project No. 6.2343.2017/4.6. Species-level identification of the freshwater mussel samples by I.N.B., Y.V.B., E.S.K. and I.V.V. was supported by the Ministry of Science and Higher Education of Russia, the Ministry of Europe and Foreign Affairs of France (MEAE), and the Ministry of Higher Education, Research and Innovation of France (MESRI) under project No. 05.616.21.0114 of the Hubert Curien Partnership (PHC) for the Franco-Russian Cooperation for Science and Technology (PHC Kolmogorov 2019). Sampling of free-living leech specimens throughout Northern Eurasia (M.V.V., I.N.B., Y.V.B., I.V.V., and A.V.K.) was supported by the Russian Science Foundation under research grant No. 19-14-00066. M.L.-L. was funded by FCT – Foundation for Science and Technology under grant No. SFRH/BD/115728/2016. I.N.B. was supported by the Russian Foundation for Basic Research under grant No. 18-44-292001_r_mk. A.V.K. and M.Y.G. were funded by the Russian Foundation for Basic Research under grant 17-45-290066_r_a. I.V.V. and E.S.K. were funded by the Russian Foundation for Basic Research under grant No. 18-34-20033_mol_a_ved and by the President of Russia Grants Council under grant No. MK-4723.2018.4. The Nakdonggang National Institute of Biological Resources supported S.K.K. under reserach project No. NNIBR-2019-01101. The Northern Arctic Federal University covered the article processing charge. We are grateful to the late Dr. Tony Whitten (Fauna & Flora International – Asia-Pacific, UK), Mr. Frank Momberg (Director for Program Development and Asia-Pacific Program Director of Fauna & Flora International, UK), Mr. Mark Grindley (Country Director of Fauna & Flora International – Myanmar Program, Myanmar), and the staff of the Department of Fisheries of the Ministry of Agriculture, Livestock and Irrigation of Myanmar for their great help during this study. Special thanks go to Ms. Jamie M. Smith (collection manager of NCSM Mollusk collection, USA) for her assistance with freshwater mussels from Japan and to Dr. Bronwyn Williams (curator of Non-Molluscan Invertebrates, NCSM, USA) for access to the leeches from freshwater mussels housed in her collection. Our research in Myanmar has been performed under the survey permission No. 5/6000/LFR(210/2018) dated on 23 January 2018 issued by the Ministry of Agriculture, Livestock and Irrigation of Myanmar and the export permission No. NWCD/ CITES/9/5666/2018 dated on 28 June 2018 issued by the Forest Department of the Ministry of Environmental Conservation and Forestry of Myanmar.