Freshwater mussels house a diverse mussel-associated leech assemblage

Ivan N Bolotov,Than Win,Sang Ki Kim,Jin Hee Lee,Dmitry M Palatov,Alena A Tomilova,А А Махров ,Vitaly M Spitsyn,Zau Lunn,B Yu Filippov ,Mikhail Yu Gofarov ,Ilya V Vikhrev,Olga V Aksenova,Arthur E Bogan,Elena M Sayenko,Yulia S Kolosova,G A Dvoryankin ,Natalia A Zubrii,Yulia V Bespalaya,Ekaterina S Konopleva,Anna L Klass,Svetlana E Sokolova,Manuel Lopes‐Lima ,Nyein Chan,Yulia Chapurina ,Alexander V Kondakov,Maxim V Vinarski

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 life style 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.

Highlights

Parasites and symbionts of freshwater mussels (Unionida) are poorly known[1,2] representing an overlooked threat to this imperiled taxonomic group[3]
We found that leeches are commonly encountered within the mantle cavity of freshwater mussels in East Asia, Southeast Asia, and East Africa (Fig. 1 and Table 1)
The mussel-associated leeches collected in East Africa (Albert Nile Basin, Uganda) belong to a single species largely corresponding to the nominal taxon Batracobdelloides tricarinatus

Summary

Introduction

Parasites and symbionts of freshwater mussels (Unionida) are poorly known[1,2] representing an overlooked threat to this imperiled taxonomic group[3]. Batracobdella kasmiana, an East Asian species, was found to be a possible obligate inhabitant of the mantle cavity of large freshwater mussels having a broad range covering Japan, the southern areas of the Russian Far East, continental China, and Taiwan[15,16,17,18,19,20,21]. Batracobdelloides tricarinatus was recorded from the mantle cavity of freshwater mussels (Unionidae and Iridinidae) in Africa[26,27], but this association was regarded as incidental, because this leech species did not share any indication of feeding on mussels, even in prolonged starvation[26]. Batracobdella kasmiana and Batracobdelloides reticulatus seem to be the two possible obligate inhabitants of the mantle cavity of freshwater mussels known to date, while B. tricarinatus from Africa and the two Placobdella species from North America were considered occasional visitors of such unusual habitats. We consider mussel-associated leech species that can complete their life cycle in open environments besides the mantle cavity of freshwater mussels, using freshwater fishes and other taxa as hosts, but were repeatedly found as mussel mantle cavity inhabitants

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Conclusion