Not that many leech species after all: Myzobdella lugubris and Myzobdella patzcuarensis (Annelida: Hirudinida) are the same species

Syst Parasitol (2024) 101:38 https://doi.org/10.1007/s11230-024-10160-5 Not that many leech species after all: Myzobdella lugubris and Myzobdella patzcuarensis (Annelida: Hirudinida) are the same species Gerardo Torres‑Carrera Yanet Velázquez‑Urrieta · · Ana Santacruz Received: 25 January 2024 / Accepted: 29 March 2024 / Published online: 3 May 2024 © The Author(s) 2024 Abstract The genus Myzobdella groups five species of leeches parasites of fishes mainly of freshwater but with tolerance to brackish waters. Native distribution of these species includes the New World from North to South America. Myzobdella lugubris Leidy, 1851, the type species of the genus, was briefly described based on specimens from the USA, but subsequently their morphology, known distribution and host range were expanded; however, less is known about the other four species of the genus. As part of a survey focusing on characterizing the diversity of leeches from Mexico, specimens of Myzobdella patzcuarensis (Caballero, 1940), from the type locality of the species were included for the first time in a phylogenetic study. In addition, specimens assigned to Myzobdella from the southeast of Mexico as well as from Nicaragua, were also included. In the resulting phylogenetic tree, our newly generated G. Torres‑Carrera (*) · Y. Velázquez‑Urrieta Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, 04510 Mexico, Mexico e-mail: G. Torres‑Carrera · Y. Velázquez‑Urrieta · A. Santacruz Laboratorio de Helmintología, Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, 04510 Mexico, Mexico Present Address: A. Santacruz Stowers Institute for Medical Research, Kansas City, MO, USA sequences were found nested in the same clade that M. lugubris; with unresolved relationships and relatively low genetic divergence, suggesting conspecificity. In addition, the internal morphology of the specimens of Myzobdella from Mexico is consistent with the description of M. lugubris. Our morphological examination reveals high degrees of variability in the external pigmentation of the specimens. Based on our results we formally synonymize M. patzcuarensis under M. lugubris. Introduction Piscicolidae Johnston 1865 (Annelida: Hirudinida) is a family of parasitic leeches mainly associated with fishes, with about 170 described species around the world, two-thirds of which are marine species (Magalhães et al., 2021). Investigation about the systematics of this group is scarce in comparison with their freshwater counterparts, and the classification within the family remains unresolved (Williams & Burreson, 2006). Historically, three subfamilies were recognized: Platybdellinae Epshtein 1970, Piscicolinae Johnston 1865 and Pontobdellinae Llewellyn 1966. These subfamilies were proposed in the basis on the absence or presence of a single, or two pairs of pulsatile vesicles, respectively. So far, only members of Pontobdellinae have been recovered as a monophyletic group in phylogenetic studies (Williams & Burreson, 2006; Utevsky & Utevsky, 2018). Vol.: (0123456789) 13 38 Page 2 of 11 The genus Myzobdella was erected by Leidy, 1851 based on the study of specimens found attached to crabs of the genus Callinectes Stimpson (Decapoda: Portunidae) from an undefined locality, but must likely from Philadelphia, USA. The description of M. lugubris, the type species of the genus, is brief and provides no information about its geographic distribution or the designation of the holotype or paratypes; however, it was thought to be a brackish species (Leidy & Cassin, 1850). Meyer (1940) recognized the genus Illinobdella to include four freshwater fish-leech species from North America: Illinobdella alba Meyer, 1940, I. elongata Meyer, 1940, I. moorei Meyer, 1940 and I. richardsonii Meyer, 1940 and differentiated the new species from M. lugubris based on their habitat and host association, since all Illinobdella species are typically found in freshwater environments parasitizing fishes. In the same year, a morphologically similar species was described in Mexico: Illinobdella patzcuarensis; parasite of the charal fish Chirostoma estor Jordan (Teleostei: Atherinopsidae) from Patzcuaro Lake, Michoacán. Further studies on Myzobdella lugubris have established that this species has a broad geographic distribution along USA and Canada, dwelling brackish and freshwater habitats, and interestingly, able to parasitize both crustaceans and fish (see Moore, 1946; Hutton & Sogandares-Bernal, 1959; Klemm, 1972; Daniels & Sawyer, 1975). Sawyer et al. (1975) and Daniels & Sawyer (1975) found that neither habitat nor host preference are reliable features for the separation of species of Illinobdella and M. lugubris. Also, such studies found no differences in internal and external anatomical traits between species, therefore all Illinobdella species from USA were transferred to Myzobdella and synonymized with Myzobdella lugubris, with the notable exception of M. patzcuarensis. Currently, in addition to M. lugubris and M. patzcuarensis, three species are considered valid within the genus: Myzobdella reducta (=Piscicolaria reducta Meyer, 1940), from USA and Myzobdella uruguayensis Mañé-Garzón and Montero, 1977 and Myzobdella platensis (Cordero, 1933) from South America (Uruguay, Argentina and Brazil). Previous phylogenetic analysis of Piscicolidae included only M. lugubris and M. reducta (Williams & Burreson, 2006), showing low genetic variation between both species; hence, Saglam et al. (2018) suggested that both specimens Vol:. (1234567890) 13 Syst Parasitol (2024) 101:38 might belong to M. lugubris, so the remaining species are unrepresented. Records of Myzobdella lugubris have been reported in Hawaii and Italy (Williams & Burreson, 2006; Liuzzo et al., 2018), where they were likely accidentally introduced (Lages et al., 2021). More recently, Myzobdella sp. was also reported in Nicaragua, parasitizing freshwater cichlids (Santacruz et al., 2022). Myzobdella species are important for the economy due to the damage they may cause to fish (Appy & Cone, 1982; Faisal et al., 2011; Volonterio et al., 2004) and crab hosts (Severino-Rodrigues & de Almeida-Duarte, 2020; Zara et al., 2009); and due their potentially role as vectors of blood parasites (Faisal & Schulz, 2009). As part of a survey to characterize the morphologic and genetic diversity of fish leeches from Mexico, we collected samples of M. patzcuarensis from its type locality (Lake Patzcauro, Mexico) and additional specimens from the states of Veracruz, Yucatán, Quintana Roo, Mexico and from Nicaragua lake, Nicaragua. Materials and methods Sample collection Fish specimens of Vieja sp. were recollected in January–February 2019, and November 2021 in Escondida lagoon, Los Tuxtlas, Veracruz, Mexico (18° 35′ 25″ N, 95° 05′ 23″ W). Fish specimens were captured using cast net and transported alive to the laboratory. Fish were examined for leeches attached to (...truncated)