Parasite 25, 53 (2018) Ó J.F. Espínola-Novelo et al., published by EDP Sciences, 2018 https://doi.org/10.1051/parasite/2018054 Available online at: www.parasite-journal.org RESEARCH ARTICLE OPEN ACCESS Metazoan parasite communities of two deep-sea elasmobranchs: the southern lanternshark, Etmopterus granulosus, and the largenose catshark, Apristurus nasutus, in the Southeastern Pacific Ocean Juan F. Espínola-Novelo1, Rubén Escribano2,3, and Marcelo E. Oliva3,4,* 1 Programa de Doctorado en Ciencias Aplicadas, mención Sistemas Marinos Costeros, Universidad de Antofagasta, P.O. Box 179, Antofagasta, Chile 2 Departamento Oceanografía, Universidad de Concepción, P.O. Box 160-C, Concepción, Chile 3 Millennium Institute of Oceanography (IMO), Universidad de Concepción, P.O. Box 160-C, Concepción, Chile 4 Instituto de Ciencias Naturales Alexander von Humboldt, Universidad de Antofagasta, P.O. Box 170, Antofagasta, Chile Received 3 April 2018, Accepted 29 October 2018, Published online 20 November 2018 Abstract – Two deep-sea shark species were obtained as by-catch of the local fishery of the Patagonian toothfish, Dissostichus eleginoides, at depths ranging from 1000 to 2200 m off central and northern Chile. A total of 19 parasite taxa were found in 133 specimens of the southern lanternshark, Etmopterus granulosus,(n = 120) and largenose catshark, Apristurus nasutus, (n = 13). Fourteen taxa (four Monogenea, one Digenea, four Cestoda, one Nematoda, two Copepoda, one Annelida and one Thecostraca) were found in E. granulosus, whereas five taxa (one Monogenea, two Cestoda and two Nematoda) were found in A. nasutus. Representatives of Cestoda showed higher values of preva- lence and a greater intensity of infection; this pattern is consistent with reports for elasmobranchs, but the monoge- nean richness was higher than that previously reported for related deep-sea sharks. Regarding E. granulosus,a positive and significant correlation between host length and abundance was found for six (four ectoparasites, one mesoparasite, and one endoparasite) of the 14 taxa recorded, but prevalence was significantly correlated with host length only for the monogenean Asthenocotyle sp. Although the sample size for A. nasutus was limited, we compared richness, abundance, diversity and evenness at the infracommunity and component community levels. All of these variables were higher for E. granulosus, but at the infracommunity level, abundance was higher for A. nasutus. All the parasite taxa (except two) represent new host and geographical records. Key words: Deep-sea sharks, metazoan parasites, biodiversity, Southeastern Pacific Ocean. Résumé – Communautés des parasites métazoaires de deux élasmobranches de mer profonde, Etmopterus granulosus et Apristurus nasutus, dans le sud-est de l’océan Pacifique. Deux espèces de requins des grands fonds ont été obtenues comme prises accessoires de la pêcherie locale de Légine australe, Dissostichus eleginoides, à des profondeurs allant de 1000 à 2200 m, au large du centre et du nord du Chili. Au total, 19 taxons de parasites ont été trouvés dans 133 spécimens du Sagre long nez Etmopterus granulosus (n = 120) et du Holbiche cyrano Apristurus nasutus (n = 13). Quatorze taxons (quatre Monogenea, un Digenea, quatre Cestoda, un Nematoda, deux Copepoda, un Annelida et un Thecostraca) ont été trouvés chez E. granulosus, tandis que cinq taxons (un Monogenea, deux Cestoda et deux Nematoda) ont été trouvés chez A. nasutus. Les représentants des Cestoda ont montré des valeurs de prévalence plus élevées et une plus grande intensité d’infection; ce schéma concorde bien avec ce qui a été rapporté pour les élasmobranches, mais la richesse des Monogenea était supérieure à celle précédemment rapportée pour les requins de profondeur apparentés. En ce qui concerne E. granulosus, une corrélation positive et significative entre la longueur de l’hôte et l’abondance a été constatée pour six des 14 taxons répertoriés (quatre ectoparasites, un mésoparasite et un endoparasite), mais la prévalence était significativement corrélée à la longueur de l’hôte uniquement pour le Monogène Asthenocotyle sp. Bien que la taille de l’échantillon d’A. nasutus soit limitée, nous avons comparé la richesse, l’abondance, la diversité et la régularité aux niveaux infracommunautaire et communautaire. Toutes ces variables étaient plus élevées pour E. granulosus, mais au niveau infracommunautaire, l’abondance était supérieure pour A. nasutus. Tous les taxons parasites, à l’exception de deux, représentent de nouvelles mentions géographiques et de nouveaux hôtes. *Corresponding author: [email protected] This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 2 J.F. Espínola-Novelo et al.: Parasite 2018, 25,53 Introduction Materials and methods The deep-sea (>200 m depth) is the habitat for 10–15% of A total of 133 specimens (E. granulosus =120, the global ichthyofauna [29, 30]. Despite its limited primary A. nasutus = 13) of deep-sea sharks were obtained during production, important marine resources inhabit this environ- 2015–2017 (see Supplementary material) from the by-catch ment [3]; consequently, as coastal fisheries have collapsed, the of the local fishery of the Patagonian toothfish (D. eleginoides) deep-sea region may offer new resources [41]. Accordingly, along the northern (22°160S70°380W–23°260S70°430W) and we need not only clear and adequate knowledge of these poten- central (35°50S–72°530W) Chilean coasts at depths ranging tial new resources but also a sound understanding of the biodi- from1000to2200m(Fig. 1) using a deep-sea longline. The versity of these ecosystems [3, 29]. Parasites are an important sharks were captured, stored in bags and immediately frozen component of any ecosystem, not only because of the number (À18 °C) on board and transported to the laboratory for para- of species (which is higher than the number of free-living spe- sitological analyses. cies) but also because of the role they play in the trophic web After thawing, the sharks were measured (total length to the [16, 31]. Deep-sea fish parasites have often been neglected, nearest 1.0 cm), dissected and examined for metazoan parasites although they are an essential part of marine biodiversity (both ectoparasites and endoparasites). Parasites were recorded [29]. Moreover, through the study of parasites, it is possible by species and abundance for each shark, fixed in AFA (alcohol: to obtain information about their hosts, such as their diet, migra- formalin: acetic acid), and then preserved in 70% alcohol. tory movements and population structures, and the biodiversity Nematoda were cleared with Amann lactophenol. Digenea, and human impacts in the ecosystems where they coexist [34, Monogenea and Cestoda were stained (acetic carmine) and 56, 59]. Consequently, parasites can provide crucial clues about cleared with clove oil (Sigma-Aldrich) and then mounted in the features of the ecosystems inhabited by their hosts. Eukitt medium (O. Kindler GmbH, Germany) [42]. Copepoda Knowledge of the parasite fauna harboured by deep-sea and Thecostraca were stored in ethanol (70%) and dissected fishes is available for less than 10% of the ichthyofauna that for taxonomic purposes. Parasites were identified to the lowest inhabit these ecosystems [29, 30]. This is due to the economic taxonomic level possible. The prevalence and mean intensity of and logistical difficulties in accessing the hosts that inhabit infection were calculated [8]. these ecosystems in comparison with fishes of commercial The quantitative analysis was carried out at the infracom- importance or those that inhabit coastal areas [30]; an alterna- munity and community component levels. For the infracommu- tive is to study hosts from the by-catch of deep-sea commercial nity level, we calculated the richness (number of parasite species. Knowledge regarding the parasites of sharks is scarce species per examined host), abundance (number of parasite [9], and it is even scarcer for the species that inhabit the deep- individuals per examined host) and diversity (Brillouin index) sea. Of the 509 species of sharks known to date, no fewer than using PRIMER v6, parasite species accumulation curves were 250 are considered deep-sea species [58]. Parasitological stud- constructedusingthe‘‘vegan’’packageinRfreeware[44]. ies of species that inhabit these ecosystems focus on the taxo- The Berger-Parker dominance index was calculated as the num- nomic description of some species or new host records, but few ber of individuals of the most abundant parasite species divided include the analysis of the parasite community [14, 15, 25, 28]. by the total number of parasites in a given fish host as indicated For the Southeastern Pacific Ocean (SEPO herein and after), by Dallarés et al. [14]. The descriptors Shannon, Simpson and the same scenario is evident. Of the 68 shark species that have Inverse Simpson diversity index were calculated at the commu- been reported, at least 33 are considered deep-sea sharks [17]. nity component level using the ‘‘vegan’’ package in R freeware. Only five studies have been carried out on the parasites of Because the sample size for A. nasutus was small, the charac- deep-sea sharks for the SEPO [11, 23, 32, 53, 54]. These teristics were described but not compared, as 38% of the spec- papers focus on the taxonomic description