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Parasites of two deep-sea fish Coelorynchus chilensis (Pisces: Macrouridae) and Notacanthus sexspinis (Pisces: Notacanthidae) from Juan Fernández Archipelago, Chile M. Cecilia Pardo-Gandarillas*‡, Karen González†, Christian M. Ibáñez* and Mario George-Nascimento† *Instituto de Ecología y Biodiversidad, Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile. †Departamento de Ecología Costera, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile. ‡Corresponding author, e-mail: [email protected]

This study gives a first qualitative and quantitative record of the parasitic infracommunities in two deep-sea fish species inhabiting the locality of the Juan Fernández Archipelago, Chile. In December of 2002 a total of 12 individuals of Coelorynchus chilensis and 35 Notacanthus sexspinis was obtained as by-catch of a shrimp Haliporoides diomedeae fishery at around 1000 m depth. The majority of the individuals of both species were infected at least by one parasitic taxon. Forty-five parasites were collected from C. chilensis including larval cestodes, Hepatoxylon trichiuri, Grillotia sp., larval nematodes Anisakis sp., adult digeneans Dinosoma sp., Brachyphallus sp., copepods Protochondia cf longicauda and myxozoa Myxidium sp. Twenty-two parasitic individuals were collected from N. sexspinis belonging to adult digeneans Lecithochirium sp., and Accacladium sp. (without eggs, immature), larval cestodes Hepatoxylon trichiuri, larval nematodes Anisakis sp. and myxozoa Ceratomyxa sp. Most of the parasites showed a low prevalence and abundance in both host species, except for Myxidium sp., Ceratomyxa sp., Dinosoma sp. and Brachyphallus sp. The parasites Hepatoxylon trichiuri and Anisakis sp. were the only shared taxa. These infracommunities are low in richness, diversity and abundance compared to shallow water fish–parasites communities. Nevertheless the numeric properties of infracommunities are not reliable due to sample size. Given the additional difficulties with reliable sampling of deep-sea fish, these results should not have too much significance attributed to them. The relevance of this study is simply the recognition of parasites that infect the deep-sea fish of the families Macrouridae and Notacanthidae in the southern hemisphere.

INTRODUCTION Parasitological studies carried out in fish that inhabit the deep-sea are scarce (Mauchline & Gordon, 1984; Bray, 2004), compared to studies on species from shallow coastal to shelf regions, or that are commercially important. The main obstacle is the difficult access to deep-sea organisms, and very expensive research expeditions are needed (Meléndez & Kong, 2000). Furthermore, only few captured species are available for parasitological examination, since parasitologists compete with scientists from other disciplines that study the same biological material. Studies on parasites of several deep-sea fish species report that 5–37% were infected by Digenea, 6–18% by Nematoda, 13% by Monogenea, 19–25% by Cestoda, and 2–21% by Acanthocephala (Campbell et al., 1980; Zubchenko, 1981; Houston & Haedrich, 1986; Gartner & Zwerner, 1989). Almost all of these studies have been carried out in the northern hemisphere and confirm that Digenea are the most frequent parasites of deep sea fish, between 200 and 4000 m in depth (Bray, 2004). Most parasitological studies on deep-sea fish concern records and description of new species (Harris & Dronen, 1999; Blend et al., 2000; Blend et al., 2004, Kuchta & Scholz, 2004), quantitative characteristics of the parasites (Rodríguez & George-Nascimento, 1996), related parasite–host sex (González et al., 2001), geographical distribution (Bray, 2004), variations of the parasite communities in a bathymetric gradient (Campbell et al., 1980), and host ontogeny (Campbell et al., 1980; Rodríguez & George-Nascimento, 1996; González et al., 2001). In order to contribute to the information on the deep-sea fish parasitism, the objectives of this study were to identify and quantify characteristics of the parasite infracommunities of Coelorynchus chilensis Gilbert & Thompson, 1916 and Notacanthus sexspinis Richardson, 1846, two deep-water fish species inhabitants of the southern hemisphere, near to the Juan Fernández Archipelago. Both bathypelagic species are found at depths between 200 and 1500 m (Sulak, 1986; Cohen et al., 1990). The distribution range of Coelorynchus chilensis is from Peru (06º26'S) to central Chile (38º08'S) (Cohen et al., 1990) and the Notacanthus sexspinis distribution range is the south-east and south-west Atlantic, eastern Indian Ocean and the south-east and south-west Pacific (Sulak, 1986). Nevertheless, information about the biology and ecology of these species is scarce, and therefore this study is a contribution to the knowledge of these fish from the Southern Ocean.



M.C. Pardo-Gandarillas et al.

Parasites of two deep-sea fish

MATERIALS AND METHODS

Table 1. Infection site (IS), prevalence (P), confidence interval (CI) and abundance (A) for each parasite taxon found in two deep-sea fish.

In December 2002, in the proximity of the Juan Fernández Archipelago, Chile, a total of Notacanthus sexspinis Coelorynchus chilensis 12 individuals of Coelorynchus chilensis and 35 Notacanthus sexspinis were obtained as byIS P (%) CI 95% A (mean) P (%) CI 95% A (mean) catch of the shrimp Haliporoides diomedeae (Faxon, 1893) fishery at a depth of around Myxozoa Ceratomyxa sp. gb 88.6 40–60*** 1000 m. The total body length (TL cm) of the Myxidium sp. sb 75.0 33.3–58.3*** fish was measured, and the total presence of Digenea ecto- and endoparasites was determined on Dinosoma sp. i, s 34.3 42.9–62.9 1.0 each individual without stomach eversion, Accacladium sp. immature* i, s 5.7 2.9–5.7 0.1 according to the method described by PardoLecithochirium sp. i, s 8.3 8.3–16.7 0.2 Gandarillas et al. (2004). Quantification and Brachyphallus sp. i, s 8.3 8.3–8.3 0.1 taxonomic identification of the parasites were Cestoda carried out according to Zdzitowiecki (1997) Hepatoxylon trichiuri** i 2.9 2.9–2.9 0.03 8.3 16.7–41.7*** 0.4 and Gibson (2002a,b) for digeneans, Schmidt Grillotia sp.** s 8.3 8.3–8.3 0.1 (1970) for cestode larvae, Yamaguti (1961) and Nematoda Anisakis sp.** i, s 8.6 11.4–20.0*** 0.2 33.3 33.3–66.7 0.8 Anderson (2000) for nematode larvae, Villalba & Fernández (1985) for copepod, and Shul’man Copepoda Protochondia cf longicauda g 8.3 8.3–8.3 0.1 (1988) for the myxozoans. Quantitative descriptors such as prevalence **, Larval stage; *, without eggs; ***, outside the confidence interval; gb, gall bladder; sb, swimming bladder; i, intestine; and abundance for each parasitic taxon were s, stomach; g, gills. calculated. In addition, for each infracommunity (community of parasite infrapopulations in a single host; Bush et al., 1997), the calculated descriptors were richness (number of parasitic taxa per host; see Holmes & Price, 1986), total prevalence (percentage hosts infected), and abundance (total number of parasite specimens in each infracommunity; Margolis et al., 1982).At the same time, diversity (calculated using the Brillouin index; Magurran, 1988), and evenness (to show how equally abundant the parasitic taxon are; Magurran, 1988) were calculated. In order to evaluate the effect of the low samples size (Gregory & Blackburn, 1991), the 95% confidence interval was calculated for all infracommunity descriptors (Sokal & Rohlf, 1995), for the total prevalence and for each parasitic taxon with a bootstrap procedure with 1000 iterations using PAST Statistics Software (Hammer et al., 2001).

RESULTS In Notacanthus sexspinis (N=35 specimens), a total of 22 parasite individuals were found belonging to adult digeneans Lecithochirium sp. Lühe, 1901, immature digeneans (without eggs) Accacladium sp. Odhner, 1928, larval cestodes Hepatoxylon trichiuri (Holten, 1802), larval nematode Anisakis sp. Dujardin, 1845 and the myxozoan Ceratomyxa sp. Thélohan, 1892. The 12 Coelorynchus chilensis contained forty-five parasites belonging to the larval cestodes H. trichiuri and Grillotia sp. Guiart, 1927, the larval nematode Anisakis sp., adult digeneans Dinosoma sp. Manter, 1934 and Brachyphallus sp. Odhner, 1905, the copepod Protochondia cf longicauda Ho, 1970, and the myxozoan Myxidium sp. Bütschli, 1882 (see Table 1). All specimens of C. chilensis examined and 97.1% of N. sexspinis were infected at least by one parasitic taxon (Table 2). The parasites Ceratomyxa sp., Myxidium sp., Dinosoma sp. and Anisakis sp. showed the highest prevalence in the gall bladder, swimming bladder, stomach and intestine of their host, respectively (Table 1). The species Accacladium sp., Lecithochirium sp., H. trichiuri, Grillotia sp. and Protochondia cf longicauda showed less than 10% prevalence in the stomach, intestine and gills of their host, respectively (Table 1). The abundance of each metazoan parasite was very Table 2. Quantitative descriptor of the parasite infracommunities of two deep-sea fish. Mean (m), standard low in both hosts (Table 1). deviation (SD), confidence interval (CI). Infracommunities were depauperate Notacanthus sexspinis Coelorynchus chilensis having low richness and abundance, with a similar diversity index, but not equally Descriptors % m SD CI 95% % m SD CI 95% abundant parasitic taxa (Table 2). Regarding 1.26 2.24 1.24 to –0.27* 1.67 2.19 2.29 to –0.19* the composition of parasites, they had a low Abundance Diversity 0.07 0.08 0.03 to –0.02* 0.07 0.10 0.03 to –0.02* similarity, only H. trichiuri and Anisakis sp. in Evenness 0.41 0.48 0.19 to –0.13* 0.37 0.47 0.31 to –0.20* larval stages were present in both host species Richness 1.44 0.50 0.29 to –0.04* 1.50 0.67 0.29 to –0.04* (Table1). These species are parasites in larval Total prevalence 97.1 61.80–85.3* 100 58.3–91.70* stages and are found in the majority of the fish species in the south-eastern Pacific. *, outside confidence interval. JMBA2 - Biodiversity Records Published on-line

Parasites of two deep-sea fish

M.C. Pardo-Gandarillas et al.



Nevertheless, the small sample sizes of both hosts (N<50), are not statistically reliable, because it generated an effect of overestimation or underestimation of the numeric property of infracommunity analysed, reflected in a low or absence probability of being calculated within the intervals of confidence (Tables 1 & 2).

DISCUSSION This study is the first report on the parasite infracommunities of Coelorynchus chilensis and Notacanthus sexspinis from the southern hemisphere in the proximity of Juan Fernández Archipelago, Chile. Campbell et al. (1980) suggested that the diversity of the digeneans is relatively low at the deep-sea, although the prevalence and abundance can be high. In this case, we found that the prevalence and abundance of these metazoan parasites were low in both host species. Nevertheless, these results should not be given too much significance due to the small sample size. Additionally, due to this problem, we did not have sufficient individuals of any digeneans to identify them to species level (Table 1).We can say that the digeneans found in this study belong to families recorded in different fish orders which present a similar bathymetric distribution (Bray, 2004). Notacanthus sexspinis and C. chilensis are definitive hosts of the three digeneans found, and the only Accacladium sp. specimen was found without eggs within the uterus (immature). Small specimens (12 to 15 cm TL) of C. chilensis were infected only by Myxidium sp., while large individuals (30 to 44 cm TL) were also infected with metazoan parasites. Notacanthus sexspinis was parasitized in the whole body size range of the examined individuals by Ceratomyxa sp. and metazoan parasites (40 to 57 cm TL). Myxozoan parasites are common in deep-sea fish (Moser & Noble, 1976; Threlfall & Khan, 1990). In our case, we found remains of polychaetes of the family Chaetopteridae in the stomachs of N. sexspinis, which could be the eventual intermediate or paratenic hosts of the myxozoans parasites (Kent et al., 2001). The species H. trichiuri, Grillotia sp. and Anisakis sp. have a wide host occurrence at larval stage (George-Nascimento, 1987). Adult individuals of the genus Hepatoxylon and Grillotia have been found to infect several elasmobranch species (Schmidt, 1970; Keeney & Campbell, 2001), and Anisakis, large marine mammals (Delyamure, 1968). The copepod Protochondia cf longicauda found in this study is one of the three species that compose the Chondracanthidae family (Østergaard, 2003).The most common parasite family in the deep-sea is Chondracanthidae within the order Poecilostomatoida, which is frequently reported in the oral-branchial cavity of deep-demersal fish (Boxshall, 1998; Østergaard, 2003), especially the Macrouridae family (Boxshall, 1998). Protochondria longicauda have been found in Hippoglossina bollmanni from Perú and Hippoglossina macrops in Chile (Villalba & Fernández, 1985, González et al., 2001). But other species of Protochondria (i.e. P. alaeiopis and P. neopercis) are found in fish that are systematically apart from the Pleuronectidae family (Villalba & Fernández, 1985). Few families of parasitic copepods have successfully colonized deep-demersal fish, and the taxa exhibit a wide range of levels of host specificity (Boxshall, 1998). The infracommunities exhibited low levels of richness, abundance, diversity and evenness between host species. Nevertheless, in this study like others that present aditional difficulty with reliable sampling of deep-sea fishes (Merrett et al., 1991), these results should not have too much significance attributed to the numeric properties of infracommunities (Table 2). Even so, the fact that the sample sizes are small, it is highly likely that the results on numerical descriptors of infracommunities would not change too much with larger samples, except for further taxonomic records, as they are typical figures of deep-sea and small fish species. On the other hand, the recognition of parasites that infect the deep-sea fishes of the family Macrouridae and Notacanthidae in the southern hemisphere, already with this is relevance in this study. We are grateful to Dr Karin Lorhmann (Universidad Católica del Norte, Chile) and Claudio González (Universidad de Chile) for help with the English.

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