Metazoan parasites of deep-sea fishes from the South Eastern Pacific: Exploring the role of ecology and host phylogeny

Author’s Accepted Manuscript METAZOAN PARASITES OF DEEP-SEA FISHES FROM THE SOUTH EASTERN PACIFIC: EXPLORING THE ROLE OF ECOLOGY AND HOST PHYLOGENY Luis A. Ñacari, Marcelo E. Oliva www.elsevier.com

PII: DOI: Reference:

S0967-0637(16)30053-X http://dx.doi.org/10.1016/j.dsr.2016.06.002 DSRI2644

To appear in: Deep-Sea Research Part I Received date: 11 February 2016 Revised date: 8 June 2016 Accepted date: 14 June 2016 Cite this article as: Luis A. Ñacari and Marcelo E. Oliva, METAZOAN PARASITES OF DEEP-SEA FISHES FROM THE SOUTH EASTERN PACIFIC: EXPLORING THE ROLE OF ECOLOGY AND HOST P H Y L O G E N Y , Deep-Sea Research Part I, http://dx.doi.org/10.1016/j.dsr.2016.06.002 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

METAZOAN PARASITES OF DEEP-SEA FISHES FROM THE SOUTH EASTERN PACIFIC: EXPLORING THE ROLE OF ECOLOGY AND HOST PHYLOGENY Luis A. Ñacaria,b*, Marcelo E. Olivab,c a

Magister Ecology Aquatic Systems, Universidad de Antofagasta, Angamos 601,

Antofagasta Chile b c

Millenniun Institute of Oceanography, Universidad de Concepción, Concepción, Chile

Instituto Ciencias Naturales Alexander von Humboldt, Universidad de Antofagasta,

Angamos 601, Antofagasta, Chile

[email protected] [email protected]

*

Corresponding author. Tel.: 56 55 2637404.

Abstract We studied the parasite fauna of five deep-sea fish species (> 1000 m depth), Three members of Macrouridae (Macrourus holotrachys, Coryphaenoides ariommus and Coelorhynchus sp.), the Morid Antimora rostrata and the Synaphobranchidae Diaptobranchus capensis caught as by-catch of the Patagonian toothfish (Dissotichus eleginoides) from central and northern Chile at depths between 1000 and 2000 m. The parasite fauna of M. holotrachys was the most diverse, with 32 species (The higher reported for Macrourus spp.) and the lower occur in the basketwork eel D. capensis (one species). Trophically transmitted parasites, mainly Digenea and Nematoda explain 59.1% of the total number of species obtained (44 species) and the 81.1% of the 1020 specimens collected. 1

Similarity analysis based on prevalence as well as a Correspondence analysis shows that higher similitude in parasite fauna occurs in members of Macrouridae. The importance of diet and phylogeny is discussed as forces behind the characteristics of the endoparasite and ectoparasite communities found in the studied fish species.

Keyword: deep-sea fish, metazoan parasites, diversity, South Eastern Pacific

1. Introduction As noted by Klimpel et al. (2006), the oceans are the largest ecosystems on earth. More than two-thirds of the world’s surface is covered by seawater, to an average depth of 3,800 m. Waters between the depths of 200–1,000 m (Mesopelagic) are characterized by diffuse light and scarce nutrient conditions, whereas waters between the depths of 1,000–4,000 m (Bathipelagic) are completely dark and characterized by food shortage (Castro and Huber, 1997). Jointly, these layers represent the largest area of the deep sea (Bray et al., 1999). According to Froese and Pauly (2015), there are approximately 33,200 species of fish worldwide, of which perhaps 10–15% inhabit the deep sea (Klimpel et al., 2006). Given that approximately 1,030 fish species are found in the waters off of the coast of Chile (Pequeño, 1989; Kong and Melendez 1991), and following Klimpel et al. (2006) proportional estimates, then 100–150 of these Chilean fish species are deep-sea inhabitants. The Atacama Trench (20°–30° S), which runs along the Pacific coast of South America, is the deepest trench in the South Pacific Ocean, extending to a depth of more than 8,000 m (Danovaro, et al., 2002; Gambi, et al., 2003). Because of its great depths, information concerning species diversity in this trench is scarce; Kong and Melendez (1991) identified 67 teleost fish species caught at depths of 350–1100 m between the latitudes of 18°19’ S to 2

38°30’ S. Only four articles (Rodríguez and George-Nascimento, 1996; Oliva et al., 2008; Pardo-Gandarillas et al., 2008; and Salinas et al., 2008) have been published in the scientific literature about the parasite fauna of deep-sea fishes (> 300 m) that inhabit the waters of the Southeastern Pacific,. The study of the parasites of deep-sea fishes began with Manter (1934), who analyzed 721 specimens of teleost fish collected from Dry Tortugas (Florida), and Noble et al. (1973), who studied the parasites of Macrourus rupestris collected from Korsfjorden (Norway). Additional studies in the North Atlantic have been conducted by Wilhelm et al., (2008); Kellermanns, et al., (2009) and Klimpel et al., (2006; 2008; 2010), among others. Parasite assemblages of deep-sea fishes collected from the Antarctic Ocean have been studied by Walter et al. (2002), whereas Brickle et al. (2005); Dallarés et al. (2014); Mateu et al. (2015) and Constenla et al. (2015) analyzed the parasite fauna of Mediterranean deep-sea fishes. Klimpel et al. (2009) presented a comprehensive list of metazoan parasites of deepsea fishes (> 200 m). The evolutionary history and ecology of the host species influences the composition of its parasite communities (Poulin, 1995; Chavéz et al., 2012). Over the course of their evolutionary history, hosts can lose and acquire new parasite species through the evolution of native parasites, or they may acquire new parasite species from other hosts (Poulin and Rohde, 1997). Brook (1980) noted that studies of parasite communities that fail to account for phylogeny may provide inaccurate results and obscure the real relationship between host ecology and parasite richness (Poulin and Rohde, 1997). Moreover, Chavez et al. (2012) noted that few studies have simultaneously evaluated the determinant roles played by ecological and

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phylogenetic factors in parasite community formation, and those that have evaluated determinant roles show contradictory results. With regard to the parasites of deep-sea fishes, Campbell et al. (1980) suggested that the parasite community of Macrouridae exhibits a high degree of similarity as a consequence of a similar diet. It is clear that ecology influences the characteristics of the parasite community of a given host in addition to host phylogeny but in different ways (Morand et al. 2002). Janovy et al. (1992), for instance, demonstrated that ecological variables have a strong influence on parasite population structure (i.e., quantitative characteristics such as prevalence, abundance and intensity), whereas the evolutionary history of the host species should only affect the evolutionary processes of their parasites. Although many studies suggest the importance of host phylogeny, few have integrated this information into parasite-community analyses (Poulin, 1995; Morand et al., 2000). The importance of ecological and phylogenetic factors, when analyzed simultaneously, have been explored by Bush et al. (1990); Poulin (1996, 2010); Muñoz et al., (2006); and Chávez et al., (2010), among a handful of others, but to our knowledge, no study has applied such an approach to deep-sea fish species. Our primary goal here is to identify the metazoan parasites of five deep-sea host fish species in the southeastern Pacific and to examine the relative influence of ecology and host phylogeny in determining parasite composition.

2. Materials and Methods 2.1. Sampling area and parasite collection A total of 87 deep-sea fish specimens were obtained over the period of February–March 2015 and in October 2015 from the by-catch of artisanal fisheries and from a mark– recapture experiment of the Patagonian toothfish (Dissostichus eleginoides Smitt, 1898) in 4

northern (22°16’S 70°38’W – 23°26’S 70°43’W) and central (35° 5´S – 72°53´W) Chile at depths ranging between 1,000–2,200 m. (Figure 1) using a deep-sea longline. Fish specimens belonged to 5 species: bigeye grenadier (Macrourus holotrachys Günther, 1878; n = 30), Humboldt grenadier (Coryphaenoides ariommus Gilbert & Thompson, 1916; n = 7), Coelorhynchus sp. (n = 3), blue Antimora (Antimora rostrata Günther, 1878; n = 39) and basketwork eel (Diastobranchus capensis Barnard, 1923; n = 8). Size, weight, order and Family of the fish species are given in Table 1. Fish were immediately frozen (–18°C) aboard the fishing vessels and transported to the laboratory for parasitological analyses. After thawing, fish were measured (total length to nearest cm), weighed, dissected and examined for metazoan parasites (both ectoparasites and endoparasites). Parasites were recorded by species and abundance for each fish, fixed in AFA (alcohol:formalin:acetic acid), and then preserved in 70° alcohol. Nematoda and Acanthocephala were cleared with Amann lactophenol. Digenea, Monogenea and Cestoda were stained (Acetic Carmin) and cleared with Oil of Clove® (Sigma-Aldrich, Madagascar), then mounted in Eukitt® (O. Kindler GmBH, Germany).

2.2. Data analysis Parasites were identified to the lowest taxonomic level possible. The prevalence and mean intensity of infection were calculated based on procedures described by Bush et al. (1997). Cluster analyses (based on the Bray–Curtis similarity index and simple linkage algorithm) were used to determine whether endoparasitic composition (prevalence and intensity of infection) was similar among hosts. Correspondence analyses were then employed to assess host–parasite associations; only parasites with a prevalence ≥ 10% were included in this analysis. Due to the absence of copepods in four of the five analyzed hosts, and as all 5

monogeneans were specific to a single host species, multivariate analyses were performed only for endoparasites. All multivariate analyses were performed using Statistica 10.0 software (StatSoft Inc., Tulsa, Oklahoma, USA).

3. Results 3.1 Biodiversity A total of 1,020 individual specimens belonging to 44 taxa of metazoan parasites were obtained from the examined hosts; of these, 14 taxa were ectoparasites, and 30 taxa were endoparasites. Higher parasite richness was found in M. holotrachys, which harbored 32 taxa, followed by Coryphaenoides ariommus, Antimora rostrata, Coelorhynchus sp. and Diastobranchus capensis, with 15, 8, 5 and 1 taxa, respectively. (Table 2). Due to the low sample size for some species (Table 2), identification to species level was not always possible.

3.1.2 Copepoda Copepoda accounted for 11.4% of the recorded species, all of which were found in the gills, the gill arch or on the body surface of M. holotrachys. Although the absence of males of Clavella sp. in our samples precludes specific identification, an analysis of the female morphology suggests a possible new species (R. Castro pers. comm.)

3.1.3 Monogenea Monogeneans were the second most common parasites, accounting for 20.5% of the species identified. With the exception of a species of Capsalidae, all of the monogeneans found were members of the Diclidophoridae. According to Klimpel et al. (2009), 56.5% of the 6

monogenean subclass Oligonchoinea in deep-sea fishes are representative of this Family. M. holotrachys harbored 4 species, whereas both Coelorhynchus sp. and D. capensis were devoid of monogenean.

3.1.4 Digenea Digenea belonging to five families were the most abundant parasites, accounting for 40.9% of the total number of species. As a rule, all Digenea were found in the stomach and intestines, with the exception of Gonocerca haedrichi, which was found in the urinary bladder of the three macrourids, and an unidentified species found in the gonads of M. holotrachys and C. ariommus. M. holotrachys harbored 13 (72.2%) Digenea species, followed by C. ariommus with seven species. As a whole, members of the Macrouridae were parasitized by 17 species of Digenea, which corresponds to 94.4% of the species of this group now found. The basketwork eel D. capensis was the only species devoid of Digenea.

3.1.5 Cestoda Parabothriocephalus sp. (Pseudophyllidae) was the only adult cestode and was found in the intestine and pyloric caeca of M. holotrachys. Two additional Cestoda, the larval stage of a Trypanorhynchidae and Hepatoxylum sp. were found in the celomic cavity of M. holotrachys, C. ariommus and A. rostrata. Cestoda represent 6.8% of the parasite richness.

3.1.6 Nematoda Nematoda were well represented, accounting for 18.2% of the total number of parasite species. Nematoda were most abundant in M. holotrachys (75% of the species), and all 7

Nematoda identified were found in the three members of the Macrouridae. The anisakids Hysterothylacium sp. (both larval and adult stages) and Anisakis sp. were the most abundant nematodes found. D. capensis was parasitized only by Anisakis sp.

3.1.7 Acanthocephala One species belonging to the genus Echinorhynchus (Echinorhynchidae) was found in the intestine of M. holotrachys, representing 2.3% of the total number of species.

3.2 Multivariate analysis 3.2.1 Cluster analysis Cluster analysis based on prevalence of infection (Fig. 2) shows two main clades, the first one grouping members of Macrouridae and the second encompassing A. rostrata and D. capensis. Similitude between the two clades was 25%. In the first clade, the higher similitude occurs between Coelorhynchus sp. and M. holotrachy (42%), with the similitude between both species and C. ariommus at 32%. Similitude between A. rostrata and D. capensis was 41.6% Cluster analyses based on mean intensity of infection (Fig. 3) generate a different picture than prevalence, with higher similitude occurring between A. rostrata and Coelorhynchus sp. (41.0%). This clade exhibits a similitude of 5.5% with M. holotrachys. D. capensis joins the clade with a similitude of 23.6%, and finally C. ariommus has a similitude of 23% with the main clade.

3.2.2 Correspondence analysis

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Correspondence analysis based on prevalence of infection (Fig. 4) shows significant differences in the composition of the endoparasite fauna among analyzed hosts (x2 = 1580.7, df = 88, P < 0.001); 69.2% of the variance was explained by the first and second dimension (36.2% and 33.0%, respectively). Many parasites were associated with Macrourus holotrachys, C. ariommus and Coelorhynchus sp. Common species were Glomerricirrus macrouri, Gonocerca physidis, Gonocerca haechidri, Gonocerca sp. and Cystidicolidae gen sp1. M. holotrachys are strongly associated to Gibsonia hastata, Hemiuridae gen sp3, Parabothriocephalus sp., Hepatoxylum sp., Echinorynchus sp., Cystidicolidae gen sp2 and Nematoda gen sp1. The non-macrourid A. rostrata and D. capensis appear to be associated with Anisakis sp. and Digenea gen sp3. Correspondence analysis of mean intensity of infection also revealed significant differences among analyzed hosts (x2 = 150.9, df = 88, P < 0.001), with 72.3% of the variance explained by the first and second dimension (38.8% and 33.5%, respectively) (Fig. 5).

4. Discussion 4.1 Biodiversity Information about the metazoan parasites of the marine fishes of Chile is scarce, with no more than 70 of the approximately 1,020 known species having been studied (Muñoz and Olmos 2008), which includes both quantitative and qualitative descriptions. The near-total absence of research on the parasites of deep-sea fish represents an important gap in our knowledge of the biodiversity and structure of deep-sea communities. Four articles refer to the parasites of deep-sea fish of the southeastern Pacific: Rodriguez and GeorgeNascimento (1996) and Oliva et al., (2008), which discuss how the parasites of the Patagonian toothfish Dissostichus eleginoides can be used as biological tags for stock 9

identification in central and southern Chile (36°–48° 50’S) at depths of approximately 1000 m; Salinas et al. (2008), who analyzed the metazoan parasite fauna of the thumb grenadier Nezumia pulchella from central northern Chile (24°–33° S) caught at depths of no more than 380 m; and Pardo-Gandarillas et al. (2008), who studied the parasite fauna of two deep-sea fish species from the Juan Fernandez Archipelago caught at depths of approximately 1000 m. As such, this is the first study of the parasites of deep-sea fish (> 1000 m) associated with the Atacama Trench in the southeastern Pacific. With the exception of Antimora rostrata and C. ariommus, the fish species included in this study represent new recordings for northern Chile, as do all of parasitic species, with the exceptions of larval forms that exhibit low specificity and have a wide geographical distribution, such as larvae of Anisakis and Hysterothylacium. M. holotrachys is distributed along the southern coast of South America (both Atlantic and Pacific coasts), with the most northerly record reported by Ruiz and Oyarzún (1993), who found this fish in Talcahuano, central Chile (ca 37°S). Of the host species, M. holotrachys harbored the higher parasite diversity (32 of the 44 metazoan species recorded) and was the only species found to be parasitized by members of the Copepoda, including the mesoparasite L. szidati, which heretofore has been found only on Macrourus spp. (Walter et al. 2002; Gordeev, 2015) with a circumpolar distribution, suggesting a high specificity for this mesoparasite. This is the most northerly record for this species. C. radiatus have been observed only for members of Macrourus and Coryphaenoides (Klimpel et al. 2009). Monogenea were also well represented in M. holotrachys, harboring four species. Members of Digenea were the most dominant group, with 13 species; of those, G. haedrichi has been found in Macrourus spp. and Coryphaenoides spp. (Klimpel et al. 2009), and Gibsonia hastata has been identified as a parasite of two species of Macrourus (M. carinatus and M. 10

holotrachys) by Gaevskaya and Rodjuck (1988) and Zdzitowiecki and Cielecka (1998). The only other species of the genus, G. borealis, was described from Macrourus berglax by Campbell (1992), suggesting a high degree of host specificity for this parasite. Profundivermis intercalarius has been reported to parasitize Macrourus spp. and Coryphaenoides spp. (Klimpel et al. 2009). All the other parasite species are known to have a wide host range. Digenea are common parasites of Macrourus spp., with the proportion of recorded species ranging from 28.6% to 41.2% (See Supplementary Material); this host species was found to carry the most Digenea. Only three species of Cestoda – adult Parabothriocephalus sp., and larval Hepatoxylon sp. and Trypanorhyncha gen. sp. – were found in M. holotrachys. As noted by Kuchta et al. (2008), this genus includes four species, two of which have been reported to parasitize Macrourus spp., including M. holotrachys in the Weddell Sea of Antarctica. Larval Cestoda are common parasites in marine fish and exhibit low host specificity. Nematoda were also well represented, for which M. holotrachys showed the highest richness. Four species were larval forms. Nematoda (both larval and adult stages) are common parasites of Macrourus spp., representing between 19–38% of the parasitic species found in members of this genus of fish (see Supplementary Material). As a general rule, adult Acanthocephala are not well represented in deep-sea fishes, and here, we only found Echinorhynchus sp. in specimens of M. holotrachys. E. longiproboscis has been reported for M. holotrachys in the Falkland Islands (Gaevskaya and Rodjuck 1988). Although our sample size is relatively small (n = 30), the number of metazoan species is higher than for others members of Macrourus regardless of sample size; Walter et al. (2002), for instance, reported 21 parasite species for M. whitsoni from a sample of 386 11

specimens, and Zubchenko (1981) reported 18 species from 30 specimens of M. berglax. Our results indicated that specimens of M. holotrachys caught in sub-Antarctic waters have a more diverse parasite assemblage than do their sub-Antarctic counterparts (Supplementary Material). Coryphaenoides ariommus, which is found from northern Peru to southern Chile (4°10´ S – 38°08’ S) at depths of 590–1,860 m (Kong and Melendez, 1991), was found to harbor the second most diverse parasite fauna. Among the monogeneans, only one species belonged to the Diclidophoridae and Reimerocotyle spp. are parasites of Myctophid (Rohde and Wlilliams 1987). Capsalidae gen sp. exhibits a very peculiar globular posthaptor resembling these of Encotyllabinae hamuli, but larval hooks are absent. Of the seven digenean species found in this host, three were specific to this fish whereas the remainder occur on other Macrouridae. The larval Tripanorhyncha gen sp, was the only Cestoda found in this host. Two of the four species of Nematoda also found in this host (Anisakis sp. and Hysterothylacium sp.) were also found on other hosts. Acanthocephala were not found in this fish. Members of Coryphaenoides also harbor a rich diversity of parasites, ranging from 8 to 29 metazoan species (Supplementary Material), with Digenea and Nematoda composing the majority. Despite the small sample size, 15 parasite species were identified. As for M. holotrachys, Digenea represent the most diverse parasite group, with C. ariommus exhibiting the highest proportion of Digenea (46.7%) infection among the members of this genus (Supplementary Material). There are at least 100 different species within the genus Coelorhynchus, and as such, the genus has a worldwide distribution in tropical and temperate seas. Few species are found near the Antarctic Convergence, however; those that do occur generally at depths of 33– 12

2,220 m but typically inhabit depths between 150–800 m (Cohen et al. 1990). Three species of this genus – C. chilensis, C. fasciatus and C. aconcagua – have been recorded in the deep waters off the Chilean coast (Kong and Meléndez, 1991). Parasitological data are available for at least 15 species of this genus, but parasite richness is low when compared with other macrourid, with the number of species ranging between 1–15 (Supplementary Material). C. chilensis is one of the few deep-sea fish species in the southeastern Pacific for which parasites have been assessed; Pardo-Gandarillas et al. (2008) identified six parasite species in a sample of 12 fish specimens collected from the Juan Fernández Archipelago. Here, we identified five species of parasites (four Digenea and one Nematoda) in the three fish specimens of this species. As for other members of Coelorhynchus, the bulk of the parasite fauna are Digenea and Nematoda, and all the parasites were shared with other hosts (Supplementary Material). According to Kulka et al. (2003), the morid Antimora rostrata is one of the most abundant fish species of the deep sea, having been reported to occur in high densities in both the Atlantic and Pacific Ocean at depths between 400–3000 m (Wenner and Musick, 1977). Parasitological data for A. rostrata is scarce, however; Campbell et al. (1980), in an analysis of 622 specimens of A. rostrata collected from the New York Bight, identified 21 metazoan species, and based on the estimates of Klimpel et al. (2009). the total number of parasite species for this fish may be as high as 32. A. rostrata was the most abundant host in our sample (39 specimens), but the species displayed a low level of parasitic richness with only eight species, four of which were Digenea (Supplementary material). Our findings are consistent with Campbell et al. (1980), who stated that more than 50% of the parasite fauna of fish species that are generalized predators, such as A. rostrata, are comprised of digenetic trematodes. 13

Diastobranchus capensis (Synaphobranchidae) has a circumpolar distribution in the southern Pacific and Atlantic Oceans (Castle, 1986). This species was found to harbor just one species, the nematode Anisakis sp., but with high prevalence (62.5%) and a mean intensity of 1.4. The only reported metazoan parasite of D. capensis is an unidentified Diclidophoroidea (Rohde and Williams, 1987).

4.2 Exploring phylogenetic and ecological relationships The studied area is characterized by Antarctic Intermediate waters (Llanillo et al. 2012), which may explain the presence of fish species more typical of sub-Antarctic waters in northern Chile, along with their parasites. Parasites of deep-sea fish are important, but often overlooked, components of all marine environments and an integral component of deep-sea ecosystems (Klimpel et al., 2001; 2006). This is the first study to examine the relationship between ecology and phylogeny as a determinant of the parasite richness of deep-sea fish (> 1000 m) in the southeastern Pacific Ocean. Numerous studies have evaluated the importance of ecological factors (i.e., diet, depth, habitat, etc.) as driving forces of the community structure of fish parasites (e.g., González et al., 2001; Muñoz, 2006; Mateu et al., 2014; Constenla et al., 2015), but research exploring the links between ecology and phylogeny in determining parasite richness are scarce (e.g., Poulin & Rohde, 1997; Morand et al., 2000; Muñoz et al., 2006; Chávez et al., 2012). The structure of endoparasitic communities is highly influenced by the diet of the host (generalist versus specialist predators), by ontogenetic changes in the diet, and by prey availability (intermediate hosts) (Poulin, 1995), as well as by habitat, host behavior 14

(migratory versus sedentary, schooling versus non-schooling) and host density. Environmental factors, such as depth and water temperature, also influence community structure (Poulin, 1995; Oliva et al, 2004; Gonzalez and Oliva, 2006). All members of Macrouridae (Macrourus holotrachys, Coelorhynchus sp. and Coryphaenoides ariommus) displayed a high degree of similarity in the endoparasites they support. Consequently, trophic patterns, specifically a broad diet (Laptikhovsky, 2005, Chávez et al. 2012) but not phylogenetic factors, would be the best predictors of endoparasitic richness. As stated by Campbell et al. (1980), the endoparasitic fauna of a given host species is a good proxy of the role of the host within the food web; for example, the level of parasite richness can act as an indicator of host feeding behavior, whereas the presence of trophically transmitted parasites at adult or larval stages can provide information about the role the host plays in the food web (George-Nascimento, 1987). As it is, very little is known about the life cycles of deep-sea fish, but parasitological data can give us clues about the diet of the hosts. For instance, the presence of adult digenean on multiple hosts, such as G. macrouri, G. haedrichi, D. varicus, as well as the larval nematodes Anisakis sp. and Hysterothylacium sp., strongly suggest that the intermediate hosts for those parasites are part of the diet of the fish species in which the parasites were found. Specifically, large similarities in the endoparasitic communities among the members of the Macrouridae suggest that these fish have a similar diet, but the presence of highly specific parasites, such as G. hastata and P. intercalarius suggest a phylogenetic (coevolutionary) relationship between the host and those parasites. At the same time, Klimpel et al. (2010) reported that parasites in meso- and bathy-pelagic fish in the Mid-Atlantic Ridge exhibited low host specificity, thus there was no distinct pattern of host–parasite coevolution. Moreover, Chávez et al. (2012) demonstrated that closely-related gadiform 15

species (Merlucccius gayi and M. australis) do not have a similar parasite fauna, but a higher correlation of parasite fauna does occur between members of different suborders (Micromesistus australis and M. magallanicus), suggesting that diet and not phylogeny dictates the observed patterns. Differences in the parasite community of the most closelyrelated species (M. gayi and M. australis) may be due to latitudinal and bathymetric segregation. Likewise, differences between the parasite assemblages of the three members of the Family Macrouridae and A. rostrata (Moridae) could be attributed to their use of different habitats, as M. holotrachys, C. ariommus and Coelorhynchus sp. are bathydemersal fish whereas A. rostrata is bathypelagic (Froese and Pauly, 2015), in line with Klimpel et al. (2006), who demonstrated that parasite diversity was higher for demersal deep-sea fish than for bathypelagic species. Similarities in the parasitic fauna between the gadiform A. rostrata and the anguilliform D. capensis must be treated with caution because of the small sample size for the latter species and the meanness of their parasite fauna. For ectoparasites, all monogenean and copepod parasites were taken from a single host species, suggesting a high degree of host specificity. Morand et al. (2002) suggested that the phylogeny of the host influences the pattern of monogenean richness; for instance, three of the four species of Macrouricotyle are parasites of Macrourus spp. (Mamaev and Lyadov, 1975; Campbell et al., 1982; Suriano and Martorelli, 1984), whereas the fourth parasitizes the related Coryphaenoides (Walter et al. 2002). Similarly, the two known species of Cyclocotyloides are parasites of Macrourus spp. and Coryphaenoides spp. (Mamaev and Lyadov, 1975; Zubchenko, 1975; Kritsky and Klimpel, 2007).

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The copepod parasite Lophoura szidati is found only in Macrourus spp. (Gordeev, 2015), and C. radiatus have been found in Macrourus and Coryphaenoides (Klimpel et al. 2006; Palm and Klimpel, 2008). Our results suggest that host diet and habitat are the main determinants of the richness of endoparasites, but phylogenetic relationships cannot be ignored, as indicated by the presence of highly specific Digenea, such as G. hastata and P. intercalarius. On the other hand, host phylogeny plays a large role in determining ectoparastic richness.

Acknowledgements We appreciate the kind support of the crew of the fishing boat “Doña Bella” and its Captain Mr. Danny Manso. Partially funded by FIP 2014-03 (National Fund for Fisheries) and FONDECYT (National Fund for Science and Technology) 1140173

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Poulin, R., 2010. Decay of similarity with host phylogenetic distance in parasite faunas. Parasitology 137, 733–741. doi:10.1017/S0031182009991491 Poulin, R., Rohde, K., 1997. Comparing the richness of metazoan ectoparasite communities of marine fishes: controlling for host phylogeny. Oecologia 110, 278–283. doi:10.1007/s004420050160 Rodriguez, L., George-Nascimento, M., 1996. La fauna de parásitos metazoos del bacalao de profundidad Dissostichus eleginoides Smitt, 1898 (Pisces: Nototheniidae) en Chile central: aspectos taxonómicos, ecológicos y zoogeográficos. Rev. Chil. Hist. Nat. 69, 21– 33. Rohde, K., Williams, A., 1987. Taxonomy of monogeneans of deep sea fishes in southeastern Australia. Syst. Parasitol. 10, 45–71. doi:10.1007/BF00009101 Ruiz, V.H., Oyarzún, C., 1993. Presencia de Macrourus holotrachys en Chile. Gayana, Zool. 57, 57–59. Salinas, X., González, M.T., Acuña, E., 2008. Metazoan parasites of the thumb grenadier Nezumia pulchella, from the south-eastern Pacific, off Chile, and their use for discrimination of host populations. J. Fish. Biol. 73, 683–691. doi:10.1111/j.10958649.2008.01967.x Suriano, D.M., Martorelli, S.R., 1984. Monogeneos parasitos de peces pertenecientes al orden gadiformes de la plataforma del mar argentino.. Rev. Mus. La Plata, Secc. Zool. 13, 195–210. Walter, T., Palm, H., Piepiorka, S., Rückert, S., 2002. Parasites of the Antarctic rattail Macrourus whitsoni (Regan, 1913) (Macrouridae, Gadiformes). Polar Biol. 25, 633–640. doi:10.1007/s00300-002-0407-6

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Legend of Figures Figure 1. Stars indicated the approximate position of localities where samples of deep sea fishes were caught. A = Northern Chile (by catch samples as well mark-recapture experiment), B = (mark-recapture experiment). Figure 2. Cluster analyses based on prevalence of infection of endoparasite fauna of five species of deep-sea fishes. Code for host species as in Table 1. Figure 3. Cluster analyses based on intensity of infection of endoparasite fauna of five species of deep-sea fishes. Code for host species as in Table 1. Figure 4. Correspondence analysis based on prevalence of infection. Code for parásite species 1= Glomericirrus macrouri; 2 = Hemiuridae gen sp.2; 3 = Hemiuridae gen sp.3; 4 = 25

Derogenes varicus; 5 = Gonocerca phycidis; 6 = Gonocerca haedrichi; 7 = Gonocerca sp.; 8 = Gibsonia hastata; 9 = Paralepidapedon sp.; 10 = Steringophorus sp.; 11= Digenea gen sp1; 12 = Digenea gen sp.3; 13 = Echinorhynchus sp.; 14 = Parabotriocephalus sp.; 15 = Trypanorhyncha gen sp.; 16 = Hepatoxylum sp.; 17 = Anisakis sp.; 18 = Hysterothylacium sp.; 19 = Cystidicolidae gen sp.1; 20 = Cystidicolidae gen sp.2; 21= Cucullanidae gen sp.; 22 = Nematoda gen sp.1; 23 = Nematoda gen sp.2. Code for host species as in Table 1. Figure 5. Correspondence analysis based on intensity of infection. Code for host species and parasite species as in fig. 4.

Table1. Mean (X) and standard deviation (S.D.) for total length of five species of deep-sea fishes from Chile. Code for species:Mho = Macrourus holotrachys, Cor = Coryphaenoides ariommus, Coe = Coelorhynchus sp., Aro = Antimora rostrata,; Dia = Diastobranchus capensis. Habitat according to www.fishbase.org Total length (cm)

Body weight (g)

X ± S.D.

X ± S.D.

Mho

54.9 ± 8.53

Cor

40.0 ± 5.63

269.9 ± 99.67

Coe

54.4 ± 12.77

Aro Dia

Order

1136.5 ± 530.12 Gadiformes

Family

Habitat

Macrouridae

Bathydemersal

Gadiformes

Macrouridae

Bathydemersal

736 ± 518.52

Gadiformes

Macrouridae

Bathydemersal

49.9 ± 8.99

964 ± 669.91

Gadiformes

Moridae

Bathypelagic

60.4 ± 8.20

334.1 ± 109.16

26

Anguilliformes Synaphobranchidae Bathydemersal

Table 2. Prevalence (P) and Mean Intensity (MI) of infection of metazoan parasites found in five species of deep sea fishes from Chile. a = Adult; l = Larval stage, j = Juvenile. Fish Code as in Table 1 Species

Mho

Cor

Coe

Aro

Dia

Host number

n=30

n=7

n=3

n=39

n=8

M P

Site of infection

MI

P

I

M P

I

M P

I

COPEPODA Chondracanthodes

50.

radiatus (a) Chondracanthidae

Gills

0

gen

sp. (j)

10. Gills

0 53.

Clavella sp. (a)

Gills

3 10.

2.5 1.0 4.1 1.0

Clavellominus sp. (a)

Gills

Lophoura szidati (a)

Body surface

3.3 1.0

Gills

6.7 1.0

0

MONOGENEA Diclidophora sp. (a)

16. Macruricotyle sp. (a)

Gills

Choricotyle sp. (a)

Gills

7

1.2

3.3 1.0 10.

Cyclocotyloides sp.1 (a) Gills

0

1.0 2.6

Cyclocotyloides sp.2 (a) Gills

2. 0

42. 1. Diclidophoropsis sp (a)

9

Gills

Diclidophoridae gen. sp. (a)

7 2.6

Gills 27

1. 0

M P

I

14. 1. Reimerocotyle sp (a)

Gills

3

0

28. 4. Capsalidae gen sp. (a)

Gills

6

5

DIGENEA Glomericirrus macrouri

33. 3

33. 1.

1.4

(a)

Intestine

Genolinea sp. (a)

Intestine

6.7 1.0

Hemiuridae gen sp.1 (a) Intestine

6.7 1.0

3

0

2.6

1. 0

14. 1. Hemiuridae gen sp.2 (a) Intestine

3 16.

Hemiuridae gen sp.3 (a) Intestine

7 20.

Derogenes varicus (a)

Stomach

0 33.

Gonocerca phycidis (a)

Stomach

3

Ureter and urinary Gonocerca haedrichi (a) bladder Gonocerca sp. (a)

3

Stomach

16. Gibsonia hastata (a)

Intestine

7

Profundivermis intercalarius (a)

1.2 1.7

14. 2. 3

0 33. 5.

2.9

3.3 3.0 23.

0

2.9

3

0

28. 2. 33. 1. 6

0

3

0

71. 2. 33. 4. 12. 4. 4

8

3

0

8

2

8.4

3.3 1.0

Intestine

14. 1. Paralepidapedon sp.

Intestine

3

Lepocreadidae gen sp. (a) Bathycreadium sp. (a)

0

3.3 1.0

Intestine

2.6

Intestine 28

1. 0

28. 2. Steringophorus sp. (a)

Intestine

6 20.

Digenea gen sp. 1 (a)

Ovary

Digenea gen sp. 2 (a)

Intestine

0

2.7

0

28. 1. 6

0

3.3 1.0 10. 1.

Digenea gen sp. 3 (a)

Intestine

3

3

ACANTHOCEPHALA 10. Echinorhynchus sp (a)

0

Intestine

4.3

CESTODA Parabothriocephalus

Pyloric

sp.(a)

intestine

gut

and 10. 0

Trypanorhyncha gen sp. (l)

16. Visceral cavity

7 26.

Hepatoxylum sp. (l)

Visceral cavity

7

1.3 1.2

42. 1. 9

15. 1.

7

4

0

2.3

NEMATODA 33. Anisakis sp. (l) Hysterothylacium

Visceral cavity sp. Visceral

cavity

(l,a)

intestine

Contracaecum sp. (l)

Visceral cavity

3 7

5

3

0

3.3 2.0 26.

Intestine

7

Cystidicolidae gen sp. 2 (a)

13. Intestine

3

33. 4.

3.0

3

2.0 42. 2.

Cucullanidae gen sp. (a) Intestine

9 26.

Nematoda gen sp. 1 (l)

2

e 76. 17. 14. 1.

Cystidicolidae gen sp. 1 (a)

28. 1. 62. 1.

8.6 14. 1. 3 0

Intestine

7 29

5.4

7

0

9

5

4

28. 1. Nematoda gen sp. 2 (l)

Intestine

6

5

Highlights ·

First study regarding deep sea fish parasites from the South Eastern Pacific.

· ·

Four Macrouridae (Gadiformes) one Synaphobranchidae (Anguilliformes) species studied. Higher diversity found in Macrourus holotrachys (32 species).

· ·

Lower diversity found in Diastobranchus capensis (1 species). Ectoparasites showed higher host specificity than endoparasites.

Graphical abstract

30

31