A checklist of helminth parasites of Elasmobranchii in Mexico

Abstract A comprehensive and updated summary of the literature and unpublished records contained in scientific collections on the helminth parasites of the elasmobranchs from Mexico is herein presented for the first time. At present, the helminth fauna associated with Elasmobranchii recorded in Mexico is composed of 132 (110 named species and 22 not assigned to species), which belong to 70 genera included in 27 families (plus 4 incertae sedis families of cestodes). These data represent 7.2% of the worldwide species richness. Platyhelminthes is the most widely represented, with 128 taxa: 94 of cestodes, 22 of monogeneans and 12 of trematodes; Nematoda and Annelida: Hirudinea are represented by only 2 taxa each. These records come from 54 localities, pertaining to 15 states; Baja California Sur (17 sampled localities) and Baja California (10), are the states with the highest species richness: 72 and 54 species, respectively. Up to now, 48 elasmobranch species have been recorded as hosts of helminths in Mexico; so, approximately 82% of sharks and 67% of rays distributed in Mexican waters lack helminthological studies. The present list provides the host, distribution (with geographical coordinates), site of infection, accession number in scientific collections, and references for the parasites. A host-parasite list is also provided.


Introduction
According to Eschmeyer and Fong (2015), 1338 species of elasmobranchs have been described worldwide (768 rays and 570 sharks). However, Naylor et al. (2012), based on the fact that since 2005 more than 130 new species have been described, considered that more species remain to be discovered. According to these authors, this increase is a result of reassessment of geographic variation; some of the increase represents recognition of subtle morphological variants among congeneric forms that nevertheless exhibit substantial molecular sequence divergence (cryptic species). In Mexico, this group is represented by 204 known species (95 rays and 109 sharks) (Del Moral-Flores and Pérez-Ponce de León 2013) ( Table 1); this richness constitutes 15% of the living species in the world. Nonetheless, most of the species recorded in Mexican waters also have been found in international waters, and many of them are cosmopolitan (Espinoza-Pérez et al. 2004).
Elasmobranchs (sharks, skates and rays) are host to a great variety of parasites in nature, particularly helminths. Up to now, more than 1500 helminth species have been recorded in association with these hosts worldwide; cestodes represent the most diverse group, with approximately 1133 species, followed by monogeneans with 226, nematodes with 83, digeneans with 50-60, leeches with 23, and aspidogastreans with 2 ). In addition, 4 species of acanthocephalans have been found only in elasmobranchs (Weaver and Smales 2014). In Mexico, the first record of a helminth parasitizing an elasmobranch was made by Caballero y Caballero (1945), who described the digenean Staphylorchis pacifica (=Petalodistomum pacificum) from the body cavity of an undetermined shark in the Pacific slope of this country. Since then, a great amount of information has been generated, most of it in the last 2 decades, particularly in the Gulf of California. The main goal of this checklist is to compile and discuss all these data and to establish some patterns of richness, geographical distribution and host spectrum.

Methods
This checklist contains information updated until December, 2015, and comes from two different sources: 1) retrospective bibliographical search, using different databases such as CAB Abstracts, Biological Abstracts, and Zoological Record; 2) Search in databases of national [Colección Nacional de Helmintos (CNHE), Instituto de Biología, UNAM, Mexico City, Mexico] and international [Harold W. Manter Laboratory of Parasitology (HWML), University of Nebraska-Lincoln, USA; National Museum of Natural History (USNM), Smithsonian Institution, Washington, D.C., USA, formerly United States National Parasite Collection (USNPC), Beltsville, Maryland, USA] parasite collections.
The checklist is divided into two sections; the first includes a parasite-host list, presented in phylogenetic order, starting with the phylum Platyhelminthes (Trematoda, Monogenoidea and Cestoda), and followed by the phyla Nematoda and Annelida (Hirudinea). Each phylum contains families, genera, and species in alphabetical order. The nomenclature and classification for each metazoan group is based on the following references: Trematoda (Gibson et al. 2002;Jones et al. 2005;Bray et al. 2008), Monogenoidea (Boeger and Kritsky 1993), Cestoda (Caira et al. 2014b), Nematoda (Anderson et al. 1974(Anderson et al. -1983Gibbons 2010), and Hirudinea (Sawyer 1986;Davies 1991). The information for each helminth species includes species name, authority, and site of infection. We use "NA" when some data are not available in the original source. Next, we present species distributions, referring to states of the Mexican Republic (in caps) where the record was made as well as the specific locality name, followed by the species of host and the bibliographic references related to records. For specimens deposited in a collection, acronyms are as follows: entific names of the species of helminths are listed in alphabetical order, indicating in parentheses the parasite group to which they belong. The scientific names of elasmobranchs were updated following Froese and Pauly (2014); higher levels of classification follow Del Moral-Flores and Pérez-Ponce de León (2013).

Results
To date, 48 species of elasmobranchs (20 sharks and 28 rays) have been recorded as host of 132 taxa of helminths (110 named species and 22 not assigned to species); these parasite species belong to 70 genera included in 27 families (plus 4 families of cestodes that are incertae sedis  Winter 1959). Specimens in collections. CNHE (921, 1069CNHE (921, , 1111CNHE (921, , 1585. Notes. The original description of this species was made under the name Petalodistomum pacificum (Caballero y Caballero 1945); later, this species was transferred to Nagmia by Markell (1953). This act was accepted by Sogandares-Bernal (1959) and Curran et al. (2009) but rejected by Caballero y Caballero et al. (1956) and Winter (1959). Lamothe-Argumedo (1969) erected Winteria to accommodate this species, but this genus was considered a synonym of Nagmia (Curran et al. 2009). Pigulevski (1953 divided the genus Petalodistomum in 2 subgenera, including the species of Petalodistomum described by Caballero y Caballero (1945) in Petalodistomum (Petalodistomum). Currently, this trematode species is accepted as Staphylorchis pacifica (see Campbell 2008).
Notes. Specimens from Ciudad del Carmen were identified as Heterocotyle aetobatis Hargis, but this species was considered a synonym of Decacotyle floridana by Chisholm and Whittington (1998 Notes. This material was recorded as Quadritestis almehensis n. gen., n. sp., but its description was not published, so that name is a nomen nudum.

No specimens in collections.
Paraorygmatobothrium sp.

Notes. This species was described as Calliobothrium evani and recently transferred to
Symcallio by Bernot et al. (2015). Type host of S. evani was determined by Caira (1985) as "unidentified shark of the family Carcharhinidae"; its accurate specific identity was established by Nasin et al. (1997).

Discussion
To date, 132 helminth taxa (110 named species and 22 taxa not assigned to species) have been reported as parasites of elasmobranch species in Mexico. Seventy-three of these taxa are represented by holotypes from Mexican waters. All of these taxa have been collected in the adult stage (132). Thus, the richness of helminth species parasitizing elasmobranchs distributed in Mexican waters represents 7.2% of the worldwide species richness for this group (see Caira et al. 2012).
The 132 taxa parasitize 48 taxa of elasmobranchs (4 of them not assigned to species), within 15 families; Myliobatidae (8 species) and Urotrygonidae (6) being the families with the highest number of species sampled, due to the fact that100% and 60% respectively of the species of these two families recorded in Mexico, have been studied for helminths. In addition, helminths have been reported from 9 of the 12 orders of elasmobranchs in Mexican waters; no records are available for Squaliformes, Orectolobiformes (Selachii) or Rhinobatiformes (Batoidea). Fifteen of the 23 families of sharks have not been reported as hosts of helminths, as well as half of the families of rays. From the 204 known species of elasmobranchs recorded in Mexican waters, only 26% of them have been studied for helminths; thus, only 18.3% and 32.6% of shark and ray species, respectively, have been examined for, and found to host, helminths (Table 1). This value is similar to that found by Randhawa and Poulin (2010), who established that only 317 species (26%) of this globally distributed group of hosts have been examined for intestinal parasites (specifically tapeworms).
The species of elasmobranchs with the higher parasite species richness are Urolophus halleri (with 19 taxa), Dasyatis longa (14) and Dasyatis brevis (13). However, 8 shark and 9 ray species have been recorded only once as hosting helminths. In total, Batoidea is parasitized by 109 taxa of helminths and Selachii by 52, of which 56% and 61%, respectively, are cestode species. The mean value of species harbored by a host is 2.8 for sharks and 3.8 for rays; these traits are in accordance with the findings reported by Randhawa and Poulin (2010), who noted that, on average, batoids harbor significantly more species of tapeworms than sharks.
Anaporrhutum euzeti and Probolitrema richardii (Trematoda) are the species with the broadest host spectrum; the former species is associated with 11 species of rays These numbers correspond with the position of localities on Figure 1. from three localities, and the latter has been found in 7 species of rays and one shark from three localities. Higher host specificity was shown by cestodes; 62 of the 76 nominal species of this group were specialists for a particular species of elasmobranch. These results are in accordance with Caira and Jensen (2014) who noted that the majority of tapeworm species are extremely host-specific, exhibiting species-specific (i.e., oioxenous) associations with their hosts. However, more conclusive results can be obtained only by increasing the sampling of this group of vertebrates on both coasts of Mexico, through comprehensive studies in which complete necropsies of elasmobranchs are conducted, avoiding partial analysis of a particular site of infection or organ system, which is a common trait of the research in this field according to Caira et al. (2012). Dendromonocotyle octodiscus had the widest geographic distribution, being found in 7 localities; this monogenean is followed by Echinobothrium fautleyae, Anthocephalum michaeli and Staphylorchis pacifica, which are distributed in 5 localities each, as well as Symcallio evani and Calicotyle urobati, recorded in 4 locations each. Acanthobothrium is the most specious genus, as it is represented by 14 species parasitizing 6 species of elasmobranchs.
Along with the increase in the number of species described worldwide, the number of helminth species parasitizing sharks and rays recorded in Mexico has increased in the past 2 decades, after slow growth from 1945, when Caballero y Caballero (1945) described the first species associated with this group of hosts (Staphylorchis pacifica). Between 1945 and 1994, only 20 species were reported in this group of hosts in the country. From 1995 to the present, this number increased more than 400%, rising to 107 species (Figure 2). According to Caira and Jensen (2014), approximately 250 species were erected over the past 2 decades; 36 of them were collected from elasmobranchs inhabiting Mexican waters.
The helminthological record of elasmobranchs distributed in Mexico is asymmetrically constituted in terms of the helminth groups represented, the hosts studied and the geographical distribution of the sampling sites. Cestodes are the most widely represented group, with 76 named species and 18 not assigned to species. The main reasons that explain this asymmetry can be summarized in two points: 1) the great diversity of cestodes associated with elasmobranchs, as nine of the 19 orders included in this Class infect this group of hosts, and eight are even exclusive parasites of them (Caira et al. 2014b); cestodes are by far the most diverse group of metazoan parasites of elasmobranchs, representing more than half of the described species for this host group ; 2) the particular interest of a research team lead by Janine N. Caira from the University of Connecticut to inventory the fauna of tapeworm parasites of sharks and rays distributed in the Gulf of California, through the project "A systematic survey of the metazoan parasites of elasmobranchs from the Sea of Cortez" between 1993 and 1994. As a result of this project, more than 45 species of cestode were recorded in this area of Mexico, 36 of which were described as new species. The most intensively studied host group is Batoidea, with 32% of the species in the country harboring at least 1 species of helminth; on the other hand, only 18% of the species of sharks caught in Mexico have been reported as hosting helminths. To determine if this could represent a bias in sampling and not a reflection of the real richness of the helminths in the different groups of hosts, more sampling efforts are necessary. Likewise, the specific richness of helminths is concentrated in two states, i.e., Baja California Sur (69 helminth species reported to date) and Baja California (54), both located in the Gulf of California, up to now, the most intensively sampled region of Mexico.
In spite of the great amount of information generated in the last 20 years, new records of the helminth fauna of Elasmobranchii in Mexico remain scarce and fragmentary. To date, 81.7% of sharks and 67.4% of rays distributed in Mexican waters lack helminthological studies. Completing the helminthological inventory for this group of vertebrates is a major challenge, as recent estimates establish the number of species to be described associated with these hosts at approximately 3600, considering only the tapeworms (Randhawa and Poulin 2010). Only through efforts such as the one conducted by Caira and collaborators in the Gulf of California will a comprehensive understanding of these host-parasite associations be achieved.