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Metazoan parasites of the stomach of Dissostichus eleginoides Smitt 1898 (Pisces: Notothenidae) from southern Chile: A tool for stock discrimination?
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Fisheries Research 91 (2008) 119–122
Metazoan parasites of the stomach of Dissostichus eleginoides Smitt 1898 (Pisces: Notothenidae) from southern Chile: A tool for stock discrimination? M.E. Oliva a,∗ , I. Fern´andez b , C. Oyarz´un c , C. Murillo c a
Instituto de Investigaciones Oceanol´ogicas, FAREMAR, Universidad de Antofagasta, P.O. Box 170, Antofagasta, Chile Facultad de Ciencias Biol´ogicas, Departamento de Microbiolog´ıa, Universidad de Concepci´on, P.O. Box 160-C, Concepci´on, Chile c Facultad de Ciencias Naturales y Oceanogr´ aficas, Departamento de Oceanograf´ıa, Universidad de Concepci´on, P.O. Box 160-C, Concepci´on, Chile b
Received 25 August 2007; received in revised form 4 November 2007; accepted 5 November 2007
Abstract The taxonomic composition of the metazoan parasites found in the stomach of 629 specimens of the “Patagonian toothfish” Dissostichus eleginoides Smitt, 1898, from two localities in southern Chile (Lebu 36◦ 00 S; Quell´on 48◦ 49 S), is recorded. More than 58,000 parasite specimens belonging to 9 taxa were registered. Adult worms were represented by the hemiurids Gonocerca phycidis Manter 1925, Lecithochirium genypteri Luhe 1905, Brachyphallus crenatus (Rudolphi 1802), and Derogenes varicus (Muller 1784) and the nematode Hysterothylacium sp. Ward & Magath 1917. Larval forms of anisakid nematodes, an acanthocephalan (Corynosoma sp.), a trypanorhynch cestode (Hepatoxylon trichiuri (Holten 1802)) and an unidentified pseudophyllidean cestode were also obtained. Parasitological evidence, based on univariate and multivariate analysis, does not support either the existence of discrete stocks, migratory movements between areas or seasonality in pattern of infection. © 2007 Elsevier B.V. All rights reserved. Keywords: Tooth fish; Parasites; Chile; Stocks discrimination; Migration; Seasonality
1. Introduction According to Brickle et al. (2005) the notothenid Dissostichus eleginoides Smitt 1898 (Patagonian toothfish) is widely distributed in the Southern Ocean. Its distribution probably extends as far north as Uruguay on the Atlantic, and Peru on the Pacific coast of South America (Oyarz´un and Campos, 1987; Eastman, 1993; Chirichigno, 1998). This fish supports an important fishery in Chile, with landings reaching more than 17,000 t in 1995 (SERNAP, 2000). The Chilean fishing regulations assume that there is a single stock of Patagonian toothfish along the Chilean coast and this situation also applies for other important fish species (Valdivia et al., 2007). As stated by MacKenzie and Abaunza (2005), any study of the dynamics of an exploited population of fish should begin with the determination of its biological identity, in relation to neighbouring populations of the same species. Specifically the clear identity of the stock is a prerequisite for efficient management of the resource. There is evidence that D. eleginoides is not a panmictic population along its distri-
∗
Corresponding author. Tel.: +56 55 637404; fax: +56 55 637804. E-mail address: [email protected] (M.E. Oliva).
0165-7836/$ – see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.fishres.2007.11.012
bution. Stock structure, but also migratory movements between feeding and spawning areas, have been suggested using different tools (Shaw et al., 2004; Ashford et al., 2005; Laptikhovsky et al., 2006), at least for South Atlantic populations. The use of parasites as biological tags is one of the natural methods for stock discrimination. This approach has been successfully used in population studies to distinguish stocks (Moser, 1991) and migratory movements (Oliva, 2001) of fish. The present work lists the metazoan parasites found in the stomach of 629 specimens of D. eleginoides, discusses differences in their occurrence from two localities in southern Chile, and evaluates the possibility of using parasites as biological tags for stock identification. 2. Materials and methods Fishes (n = 629) were obtained from November 2001 to October 2002 from two fishing grounds in southern Chile: from 37◦ S to 39◦ S (landing port Lebu, n = 269) and 45◦ S to 51◦ S (landing port Quellon, Chiloe Island, n = 360) (Fig. 1) with a seasonal periodicity. Fishes were measured (nearest cm) and sexed on board local fishing vessels, and the stomach of each specimen was separated, stored and frozen (−18 ◦ C) until examination in the laboratory. After defrosting, each stomach was examined
120
M.E. Oliva et al. / Fisheries Research 91 (2008) 119–122 Table 1 Dissostichus eleginoides in southern Chile Locality and season
n
Mean size (S.D.)
Range
Quellon Spring Quellon Summer Quellon Autumn Quellon Winter Lebu Spring Lebu Summer Lebu Autumn Lebu Winter
90 90 90 90 90 60 60 59
80.9 (9.4) 100.9 (15.2) 101.2 (22.3) 93.9 (10.8) 86.3 (16.2) 74.3 (16.4) 91.2 (24.0) 81.2 (15.2)
60.0–117.0 72.0–135.0 67.0–161.0 76.0–134.0 59.0–130.0 42.8–136.5 61.4–151.0 50.1–122.5
Sample size (n) for each locality and season. Mean size (in cm) and standard deviation in parentheses.
analyses were performed to evaluate the characteristics of the infections at population and community levels. The significance of the differences in mean intensity and prevalence of infection for each parasite species was tested with an ANOVA previous log(n + 1) transformation of intensity data (due to non-normality of parasite count) and the likelihood “G” test, respectively. A multivariate discriminant analysis, using the landing ports and seasonality as grouping variables, was run in order to evaluate if parasites can be a good predictor of both, geographical origin of the samples and seasonality. Because many specimens of the toothfish harboured a large number of Anisakis sp., quantification for these species was difficult, so fishes harbouring more than 100 specimens were adjusted to an infection intensity of 100. Following Oliva (2001), Anisakis sp. were not identified to species level but were considered as a single taxon because the identification of these nematodes can be time-consuming, even more so when there were more than 30,000 individuals. Additionally, the taxonomy of Anisakis is confused and several sibling species have been described. The discovery of sibling species of Anisakis from the same host species (Scomber japonicus) and locality (Madeira Islands) (Pontes et al., 2005) where at least five species were identified justifies this decision. Statistical analyses followed Zar (1996) and SYSTAT® was used as the statistical programme.
Fig. 1. Approximate position of the fishing ground and associated landing port. A = northern fishing ground landing in Lebu (L), B = southern fishing ground landing in Quell´on (Q).
for metazoan parasites, including those encysted in or outside the stomach wall. Parasites were treated according to traditional techniques in parasitology. Reference material was deposited in the Laboratorio de Parasitolog´ıa, Departamento de Microbiolog´ıa de la Facultad de Ciencias Biol´ogicas de la Universidad de Concepci´on (Accession number on request). Population descriptors (prevalence and intensity) were calculated according to Bush et al. (1997). Univariate and multivariate
Table 2 Prevalence (Prev) and mean intensity of infection (MI) for the metazoan parasites of D. eleginoides from two localities in southern Chile Species
Locality and season QSp
Gp Dv Lg Bc Hsp An Pse Ht Cs
QSu
QAu
QWi
LSp
LSu
LAu
LWi
Prev
MI
Prev
MI
Prev
MI
Prev
MI
Prev
MI
Prev
MI
Prev
MI
Prev
MI
43.3 61.1 75.6 66.7 15.6 100 13.3 77.8 38.9
6.0 12.5 22.4 22.8 1.0 62 1.2 2.1 3.0
63.3 63.3 77.8 84.4 7.8 100 7.8 68.9 48.9
4.7 12.7 21.1 17.0 1.0 64.3 1.1 2.6 2.9
58.9 64.4 75.6 71.1 15.6 100 12.2 72.2 43.3
4.7 11.6 21.0 20.1 1.1 57 1.3 2.3 3.2
48.9 61.1 65.6 66.7 14.4 100 16.7 68.9 40.0
5.5 12.0 24.3 23.0 1.2 47.1 1.1 2.4 2.8
48.9 63.3 80.0 54.4 22.2 100 8.9 78.9 37.8
5.7 13.6 25.4 29.6 1.4 31.6 1.0 2.3 2.3
48.3 66.7 66.7 80.0 26.7 100 13.3 75.0 43.3
4.7 8.7 25.1 19.0 2.1 38.9 1.0 2.4 2.6
46.7 65.0 63.3 83.3 10.0 100 13.3 85.0 48.3
6.6 9.5 24.0 16.3 1.3 48.2 1.0 2.1 2.7
57.6 67.8 59.3 67.8 6.8 100 13.6 74.6 40.7
3.6 9.1 24.8 23.2 1.3 26.2 1.0 2.4 2.5
Codes for locality and season: QSp = Quellon Spring; QSu = Quellon Summer; QAu = Quellon Autumn; QWi = Quellon Winter; LSp = Lebu Spring; LSu = Lebu Summer; LAu = Lebu Autumn; LWi = Lebu Winter. Code for parasites: Gp = Gonocerca phycidis; Dv = Derogenes varicus; Lg = Lecithochirium genypteri; Bc = Brachyphallus crenatus; Hsp. = Hysterothylacium sp.; An = Anisakis sp.; Pse = larval Pseudophyllidea; Ht = Hepatoxylon trichiuri; Cs = Corynosoma sp.
M.E. Oliva et al. / Fisheries Research 91 (2008) 119–122 Table 3 Classification matrix Locality and Season LWi
LAu
LSp
LWi LAu LSp LSu QWi QAu QSp QSu
15 21 22 14 26 16 10 10
10 9 13 8 12 19 15 18
23 10 21 16 23 20 22 12
Total
134
104
147
LSu
QWi
QAu
QSp
QSu
% correct
2 4 16 9 5 7 9 3
2 4 2 5 2 5 4 2
2 1 3 0 8 0 9 8
3 4 7 5 10 11 9 21
2 7 6 3 4 12 12 16
25 15 23 15 2 0 10 18
55
26
31
70
62
13
Code for ports and season as in Table 2.
3. Results More than 58,000 specimens of metazoan parasites were obtained from 629 specimens of D. eleginoides. All the fish were parasitized with at least one species of metazoan parasite (range 1–9, mean = 5 species), and intensity of infection ranged from 6 to 619 (mean 93.1) parasite individuals. Table 1 shows the numbers and lengths of fish in seasonal samples from both localities. Fishes from the southern locality were (both males and females) significantly larger than those from Lebu (F(1,451) = 29.89; P 0.001). For both localities, the mean size of fishes differed significantly between seasons. Fish caught in spring (Quellon) and summer (Lebu) were the smallest. Table 2 shows the metazoan parasites and their population descriptors for each locality. ANOVAs and the “G” test demonstrated that both mean intensity and prevalence of infection, do not differ significantly for each species between localities (P > 0.38 in all cases), except for Anisakis sp. with mean intensity higher in Quellon than Lebu. Because there were no statistically significant relationships between fish size and intensity of infection for all the studied parasites, counts were not adjusted for host length and the analyses were performed on the whole sample rather than those of similar size or host age group (Oliva and Sanchez, 2005). A multivariate discriminant analysis, demonstrated the absence of significant differences at regional (interlocalities) and temporal scale (seasonality) (Wilk’s lambda 0.87, P = 0.272), with a very low level of correct assignation. Correct assignations varied from 0% (Quellon Autumn) to 25% (Lebu Winter). On average, only 13% of the fishes were correctly assigned to their locality and season (Table 3). 4. Discussion The importance of the “Patagonian toothfish” fishery as an economic activity began in the early 1990s with the decline of other resources like the Austral hake Merluccius australis (Hutton, 1872) and the kingclip Genypterus blacodes (Forster, 1801) in Chilean waters (Laptikhovsky and Brickle, 2005). Instead the economic importance focused on this resource, published information about important aspects of its biology and
121
fishery is scarce. Metazoan parasites of D. eleginoides from central Chile were studied by Rodriguez and George-Nascimento (1996). The metazoan parasites now recorded in the stomach of the “Patagonian toothfish” agree well with those stomach parasites recorded previously in central Chile, with the exception of the larval Pseudophyllidea not registered by Rodriguez and George-Nascimento (1996), and the digenean Ellytrophalloides oatesi, found by Brickle et al. (2005), but not by Rodriguez and George-Nascimento (1996) or in this study. Oliva (2001) found this species in Macruronus magellanicus L¨onnberg, 1907 from southern and central Chile; with prevalences of 52.9% and 23.8%, respectively, values that are higher than the 2.78% reported by Brickle et al. (2005) for juveniles from Shag Rocks but similar to those found at South Georgia (33.33%), suggesting that this species can be a parasite proper of adult D. eleginoides. As suggested by Brickle et al. (2005) the presence of both larval and adult forms of parasites can be considered as a mark of an intermediate level in the food web for D. eleginoides. The circumporal distribution of D. eleginoides and its distribution along the Pacific and Atlantic coast of South America, at least as far north as 18◦ S in the Pacific and 34◦ S in the Atlantic (Chirichigno, 1998; Brickle et al., 2005), strongly support the hypothesis of more than one population or stock of this species. This hypothesis is supported by genetic studies such as those by Smith and McVeagh (2000) who stated that geographically isolated populations around sub Antarctic islands and seamounts are genetically different, and represent separate stocks. Shaw et al. (2004) demonstrated that the Antarctic Polar Front and the deep-water around the Southern Ocean has been an effective barrier to genetic exchange. Ashford et al. (2005) demonstrated that otolith elemental signature can be a good tool to identify the geographical origin of D. eleginoides in the Southern Ocean. Elemental signature differs significantly from fish caught in the vicinity of the Falkland Islands and from off Southern Chile (Chiloe). Migratory movement has been proposed by Laptikhovsky et al. (2006), who suggested that Patagonian toothfish in the Falkland Island show two different kinds of migrations: an ontogenic migration from shelf waters into bathyal waters where adults live, and a seasonal adult migration between feeding and reproductive areas, covering distances >1000 km. Our samples were obtained from two localities separated by ca. 13◦ latitude (app. 1400 km). Univariate analyses demonstrated the absence of significant differences in prevalence and mean intensity of infection for both, long lived (encysted larval parasites) and short lived parasites such as digenetic trematodes. Parasites that remain for a long time in the host, like larval anisakids, larval Acanthocephala (Corynosoma sp.) and larval Cestoda (H. trichiuri) can give important clues about migratory movements of the fish host, as suggested by Oliva (2001), for the merluccid M. magellanicus. Migratory movements of D. eleginoides are not supported by parasitological evidence; at least along the Chilean coast, and the low levels of correct assignation in multivariate analyses are an adequate argument to reject the hypothesis of more than one stock of D. eleginoides in southern Chile.
122
M.E. Oliva et al. / Fisheries Research 91 (2008) 119–122
Acknowledgments Partial results of the GRANTT FIP 2001-16 (Fisheries Research Fund, Chile) to CO. The authors thank Dr. Ken Mackenzie (Zoological Department, University of Aberdeen) for comments and suggestions on an early draft of this paper. References Ashford, J., Jones, C.M., Hofmann, E., Everson, I., Moreno, C., Duhamel, G., Williams, R., 2005. Can otoliths elemental signatures record the capture site of Patagonian toothfish (Dissostichus eleginoides), a fully marine fish in the Southern Ocean. Can. J. Fish. Aquat. Sci. 62, 2832–2840, doi:10.1139/F05191. Brickle, P., MacKenzie, K., Pike, A., 2005. Parasites of the Patagonian toothfish, Dissostichus eleginoides Smitt 1898, in different parts of the Subantarctic. Polar Biol. 28, 663–671, doi:10.1007/s00300-005-0737-2. Bush, A., Lafferty, K., Lotz, J., Shostak, A., 1997. Parasitology meets ecology on its own term: Margolis et al. revisited. J. Parasitol. 83, 575–583. Chirichigno, N., 1998. Clave para identificar los peces marinos del Per´u. (Segunda edici´on revisada y actualizada). Instituto del Mar del Peru. ed. Especial. 496 pp. Eastman, J.T., 1993. Antarctic Fish Biology: Evolution in a Unique Environment. Academic Press, San Diego. Laptikhovsky, V., Brickle, P., 2005. The Patagonian toothfish fishery in Falkland Islands’ waters. Fish. Res. 74, 11–23, doi:10.1016/j.fishres.2005.04.006. Laptikhovsky, V., Arkhipkin, A., Brickle, P., 2006. Distribution and reproduction of the Patagonian toothfish Dissostichus eleginoides Smitt around the Falkland Islands. J. Fish Biol. 68, 849–861, doi:10.1111/j.10958649.2006.00973.x. MacKenzie, K., Abaunza, P., 2005. Parasites as biological tags. In: Cadrin, S.X., Friedland, K.D., Waldman, J.R. (Eds.), Stock Identification Methods.
Applications in Fisheries Science. Elsevier Academic Press, San Diego, pp. 211–226. Moser, M., 1991. Parasites as biological tags. Parasitol. Today 7, 182–185. Oliva, M.E., 2001. Metazoan parasites of Macruronus magellanicus from southern Chile as biological tags. J. Fish Biol. 58, 1617–1622., doi:10.1006/jfb.2001.1569. Oliva, M.E., Sanchez, M., 2005. Metazoan parasites and commensals of the Northern Chilean scallop Argopecten purpuratus (Lamarck 1819) as tools for stock identification. Fish. Res. 71, 71–75, doi:10.1016/j.fishres.2004.07.009. Oyarz´un, C., Campos, P., 1987. Dissostichus eleginoides Smitt 1898 Consideraciones sobre su determinaci´on taxon´omica e implicancias biogeogr´aficas (Pisces, Perciformes Nototheniidae). Rev. Biol. Mar. (Valpara´ıso) 23, 173–192. Pontes, T., D’Amelio, S., Costa, G., Paggi, L., 2005. Molecular characterization of larval anisakid nematodes from marine fishes of Madeira by a PCR-based approach, with evidence for a new species. J. Parasitol. 91, 1430–1434. Rodriguez, L., George-Nascimento, M., 1996. La fauna de parasitos metazoos del bacalao de profundidad Dissostichus eleginoides Smitt, 1898 (Pisces: Nototheniidae) en Chile central: aspectos taxon´omicos, ecol´ogicos y zoogeogr´aficos. Rev. Chil. Hist. Nat. 69, 21–33. SERNAP, 2000. Anuario Estad´ıstico de Pesca. Servicio Nacional de Pesca. Ministerio de Econom´ıa, Fomento y Reconstrucci´on, Chile. 195 pp. (available at www.sernapesca.cl). Shaw, P.W., Arkhipkin, P.W., Al- Khairulla, H., 2004. Genetic structuring of Patagonian toothfish populations in the Southwest Atlantic Ocean: the effect of the Antarctic Polar Front and deep-water troughs as barriers to genetic exchange. Mol. Ecol. 13, 3293–3303, doi:10.1111/j.1365294X.2004.02327.x. Smith, P., McVeagh, M., 2000. Allozyme and microsatellite DNA markers of toothfish population structure in the Southern Ocean. J. Fish Biol. 57 (Suppl. A), 72–83, doi:10.1006/jfbi.2000.1612. Valdivia, I.M., Chavez, R.A., Oliva, M.E., 2007. Metazoan parasites of Engraulis ringens as tools for stock discrimination along the Chilean coast. J. Fish Biol. 70, 1504–1511, doi:10.1111/j.1095-8649.2007.01429.x. Zar, J.H., 1996. Biostatistical Analysis, 3rd ed. Prentice-Hall, New Jersey.
Fisheries Research 91 (2008) 119–122
Metazoan parasites of the stomach of Dissostichus eleginoides Smitt 1898 (Pisces: Notothenidae) from southern Chile: A tool for stock discrimination? M.E. Oliva a,∗ , I. Fern´andez b , C. Oyarz´un c , C. Murillo c a
Instituto de Investigaciones Oceanol´ogicas, FAREMAR, Universidad de Antofagasta, P.O. Box 170, Antofagasta, Chile Facultad de Ciencias Biol´ogicas, Departamento de Microbiolog´ıa, Universidad de Concepci´on, P.O. Box 160-C, Concepci´on, Chile c Facultad de Ciencias Naturales y Oceanogr´ aficas, Departamento de Oceanograf´ıa, Universidad de Concepci´on, P.O. Box 160-C, Concepci´on, Chile b
Received 25 August 2007; received in revised form 4 November 2007; accepted 5 November 2007
Abstract The taxonomic composition of the metazoan parasites found in the stomach of 629 specimens of the “Patagonian toothfish” Dissostichus eleginoides Smitt, 1898, from two localities in southern Chile (Lebu 36◦ 00 S; Quell´on 48◦ 49 S), is recorded. More than 58,000 parasite specimens belonging to 9 taxa were registered. Adult worms were represented by the hemiurids Gonocerca phycidis Manter 1925, Lecithochirium genypteri Luhe 1905, Brachyphallus crenatus (Rudolphi 1802), and Derogenes varicus (Muller 1784) and the nematode Hysterothylacium sp. Ward & Magath 1917. Larval forms of anisakid nematodes, an acanthocephalan (Corynosoma sp.), a trypanorhynch cestode (Hepatoxylon trichiuri (Holten 1802)) and an unidentified pseudophyllidean cestode were also obtained. Parasitological evidence, based on univariate and multivariate analysis, does not support either the existence of discrete stocks, migratory movements between areas or seasonality in pattern of infection. © 2007 Elsevier B.V. All rights reserved. Keywords: Tooth fish; Parasites; Chile; Stocks discrimination; Migration; Seasonality
1. Introduction According to Brickle et al. (2005) the notothenid Dissostichus eleginoides Smitt 1898 (Patagonian toothfish) is widely distributed in the Southern Ocean. Its distribution probably extends as far north as Uruguay on the Atlantic, and Peru on the Pacific coast of South America (Oyarz´un and Campos, 1987; Eastman, 1993; Chirichigno, 1998). This fish supports an important fishery in Chile, with landings reaching more than 17,000 t in 1995 (SERNAP, 2000). The Chilean fishing regulations assume that there is a single stock of Patagonian toothfish along the Chilean coast and this situation also applies for other important fish species (Valdivia et al., 2007). As stated by MacKenzie and Abaunza (2005), any study of the dynamics of an exploited population of fish should begin with the determination of its biological identity, in relation to neighbouring populations of the same species. Specifically the clear identity of the stock is a prerequisite for efficient management of the resource. There is evidence that D. eleginoides is not a panmictic population along its distri-
∗
Corresponding author. Tel.: +56 55 637404; fax: +56 55 637804. E-mail address: [email protected] (M.E. Oliva).
0165-7836/$ – see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.fishres.2007.11.012
bution. Stock structure, but also migratory movements between feeding and spawning areas, have been suggested using different tools (Shaw et al., 2004; Ashford et al., 2005; Laptikhovsky et al., 2006), at least for South Atlantic populations. The use of parasites as biological tags is one of the natural methods for stock discrimination. This approach has been successfully used in population studies to distinguish stocks (Moser, 1991) and migratory movements (Oliva, 2001) of fish. The present work lists the metazoan parasites found in the stomach of 629 specimens of D. eleginoides, discusses differences in their occurrence from two localities in southern Chile, and evaluates the possibility of using parasites as biological tags for stock identification. 2. Materials and methods Fishes (n = 629) were obtained from November 2001 to October 2002 from two fishing grounds in southern Chile: from 37◦ S to 39◦ S (landing port Lebu, n = 269) and 45◦ S to 51◦ S (landing port Quellon, Chiloe Island, n = 360) (Fig. 1) with a seasonal periodicity. Fishes were measured (nearest cm) and sexed on board local fishing vessels, and the stomach of each specimen was separated, stored and frozen (−18 ◦ C) until examination in the laboratory. After defrosting, each stomach was examined
120
M.E. Oliva et al. / Fisheries Research 91 (2008) 119–122 Table 1 Dissostichus eleginoides in southern Chile Locality and season
n
Mean size (S.D.)
Range
Quellon Spring Quellon Summer Quellon Autumn Quellon Winter Lebu Spring Lebu Summer Lebu Autumn Lebu Winter
90 90 90 90 90 60 60 59
80.9 (9.4) 100.9 (15.2) 101.2 (22.3) 93.9 (10.8) 86.3 (16.2) 74.3 (16.4) 91.2 (24.0) 81.2 (15.2)
60.0–117.0 72.0–135.0 67.0–161.0 76.0–134.0 59.0–130.0 42.8–136.5 61.4–151.0 50.1–122.5
Sample size (n) for each locality and season. Mean size (in cm) and standard deviation in parentheses.
analyses were performed to evaluate the characteristics of the infections at population and community levels. The significance of the differences in mean intensity and prevalence of infection for each parasite species was tested with an ANOVA previous log(n + 1) transformation of intensity data (due to non-normality of parasite count) and the likelihood “G” test, respectively. A multivariate discriminant analysis, using the landing ports and seasonality as grouping variables, was run in order to evaluate if parasites can be a good predictor of both, geographical origin of the samples and seasonality. Because many specimens of the toothfish harboured a large number of Anisakis sp., quantification for these species was difficult, so fishes harbouring more than 100 specimens were adjusted to an infection intensity of 100. Following Oliva (2001), Anisakis sp. were not identified to species level but were considered as a single taxon because the identification of these nematodes can be time-consuming, even more so when there were more than 30,000 individuals. Additionally, the taxonomy of Anisakis is confused and several sibling species have been described. The discovery of sibling species of Anisakis from the same host species (Scomber japonicus) and locality (Madeira Islands) (Pontes et al., 2005) where at least five species were identified justifies this decision. Statistical analyses followed Zar (1996) and SYSTAT® was used as the statistical programme.
Fig. 1. Approximate position of the fishing ground and associated landing port. A = northern fishing ground landing in Lebu (L), B = southern fishing ground landing in Quell´on (Q).
for metazoan parasites, including those encysted in or outside the stomach wall. Parasites were treated according to traditional techniques in parasitology. Reference material was deposited in the Laboratorio de Parasitolog´ıa, Departamento de Microbiolog´ıa de la Facultad de Ciencias Biol´ogicas de la Universidad de Concepci´on (Accession number on request). Population descriptors (prevalence and intensity) were calculated according to Bush et al. (1997). Univariate and multivariate
Table 2 Prevalence (Prev) and mean intensity of infection (MI) for the metazoan parasites of D. eleginoides from two localities in southern Chile Species
Locality and season QSp
Gp Dv Lg Bc Hsp An Pse Ht Cs
QSu
QAu
QWi
LSp
LSu
LAu
LWi
Prev
MI
Prev
MI
Prev
MI
Prev
MI
Prev
MI
Prev
MI
Prev
MI
Prev
MI
43.3 61.1 75.6 66.7 15.6 100 13.3 77.8 38.9
6.0 12.5 22.4 22.8 1.0 62 1.2 2.1 3.0
63.3 63.3 77.8 84.4 7.8 100 7.8 68.9 48.9
4.7 12.7 21.1 17.0 1.0 64.3 1.1 2.6 2.9
58.9 64.4 75.6 71.1 15.6 100 12.2 72.2 43.3
4.7 11.6 21.0 20.1 1.1 57 1.3 2.3 3.2
48.9 61.1 65.6 66.7 14.4 100 16.7 68.9 40.0
5.5 12.0 24.3 23.0 1.2 47.1 1.1 2.4 2.8
48.9 63.3 80.0 54.4 22.2 100 8.9 78.9 37.8
5.7 13.6 25.4 29.6 1.4 31.6 1.0 2.3 2.3
48.3 66.7 66.7 80.0 26.7 100 13.3 75.0 43.3
4.7 8.7 25.1 19.0 2.1 38.9 1.0 2.4 2.6
46.7 65.0 63.3 83.3 10.0 100 13.3 85.0 48.3
6.6 9.5 24.0 16.3 1.3 48.2 1.0 2.1 2.7
57.6 67.8 59.3 67.8 6.8 100 13.6 74.6 40.7
3.6 9.1 24.8 23.2 1.3 26.2 1.0 2.4 2.5
Codes for locality and season: QSp = Quellon Spring; QSu = Quellon Summer; QAu = Quellon Autumn; QWi = Quellon Winter; LSp = Lebu Spring; LSu = Lebu Summer; LAu = Lebu Autumn; LWi = Lebu Winter. Code for parasites: Gp = Gonocerca phycidis; Dv = Derogenes varicus; Lg = Lecithochirium genypteri; Bc = Brachyphallus crenatus; Hsp. = Hysterothylacium sp.; An = Anisakis sp.; Pse = larval Pseudophyllidea; Ht = Hepatoxylon trichiuri; Cs = Corynosoma sp.
M.E. Oliva et al. / Fisheries Research 91 (2008) 119–122 Table 3 Classification matrix Locality and Season LWi
LAu
LSp
LWi LAu LSp LSu QWi QAu QSp QSu
15 21 22 14 26 16 10 10
10 9 13 8 12 19 15 18
23 10 21 16 23 20 22 12
Total
134
104
147
LSu
QWi
QAu
QSp
QSu
% correct
2 4 16 9 5 7 9 3
2 4 2 5 2 5 4 2
2 1 3 0 8 0 9 8
3 4 7 5 10 11 9 21
2 7 6 3 4 12 12 16
25 15 23 15 2 0 10 18
55
26
31
70
62
13
Code for ports and season as in Table 2.
3. Results More than 58,000 specimens of metazoan parasites were obtained from 629 specimens of D. eleginoides. All the fish were parasitized with at least one species of metazoan parasite (range 1–9, mean = 5 species), and intensity of infection ranged from 6 to 619 (mean 93.1) parasite individuals. Table 1 shows the numbers and lengths of fish in seasonal samples from both localities. Fishes from the southern locality were (both males and females) significantly larger than those from Lebu (F(1,451) = 29.89; P 0.001). For both localities, the mean size of fishes differed significantly between seasons. Fish caught in spring (Quellon) and summer (Lebu) were the smallest. Table 2 shows the metazoan parasites and their population descriptors for each locality. ANOVAs and the “G” test demonstrated that both mean intensity and prevalence of infection, do not differ significantly for each species between localities (P > 0.38 in all cases), except for Anisakis sp. with mean intensity higher in Quellon than Lebu. Because there were no statistically significant relationships between fish size and intensity of infection for all the studied parasites, counts were not adjusted for host length and the analyses were performed on the whole sample rather than those of similar size or host age group (Oliva and Sanchez, 2005). A multivariate discriminant analysis, demonstrated the absence of significant differences at regional (interlocalities) and temporal scale (seasonality) (Wilk’s lambda 0.87, P = 0.272), with a very low level of correct assignation. Correct assignations varied from 0% (Quellon Autumn) to 25% (Lebu Winter). On average, only 13% of the fishes were correctly assigned to their locality and season (Table 3). 4. Discussion The importance of the “Patagonian toothfish” fishery as an economic activity began in the early 1990s with the decline of other resources like the Austral hake Merluccius australis (Hutton, 1872) and the kingclip Genypterus blacodes (Forster, 1801) in Chilean waters (Laptikhovsky and Brickle, 2005). Instead the economic importance focused on this resource, published information about important aspects of its biology and
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fishery is scarce. Metazoan parasites of D. eleginoides from central Chile were studied by Rodriguez and George-Nascimento (1996). The metazoan parasites now recorded in the stomach of the “Patagonian toothfish” agree well with those stomach parasites recorded previously in central Chile, with the exception of the larval Pseudophyllidea not registered by Rodriguez and George-Nascimento (1996), and the digenean Ellytrophalloides oatesi, found by Brickle et al. (2005), but not by Rodriguez and George-Nascimento (1996) or in this study. Oliva (2001) found this species in Macruronus magellanicus L¨onnberg, 1907 from southern and central Chile; with prevalences of 52.9% and 23.8%, respectively, values that are higher than the 2.78% reported by Brickle et al. (2005) for juveniles from Shag Rocks but similar to those found at South Georgia (33.33%), suggesting that this species can be a parasite proper of adult D. eleginoides. As suggested by Brickle et al. (2005) the presence of both larval and adult forms of parasites can be considered as a mark of an intermediate level in the food web for D. eleginoides. The circumporal distribution of D. eleginoides and its distribution along the Pacific and Atlantic coast of South America, at least as far north as 18◦ S in the Pacific and 34◦ S in the Atlantic (Chirichigno, 1998; Brickle et al., 2005), strongly support the hypothesis of more than one population or stock of this species. This hypothesis is supported by genetic studies such as those by Smith and McVeagh (2000) who stated that geographically isolated populations around sub Antarctic islands and seamounts are genetically different, and represent separate stocks. Shaw et al. (2004) demonstrated that the Antarctic Polar Front and the deep-water around the Southern Ocean has been an effective barrier to genetic exchange. Ashford et al. (2005) demonstrated that otolith elemental signature can be a good tool to identify the geographical origin of D. eleginoides in the Southern Ocean. Elemental signature differs significantly from fish caught in the vicinity of the Falkland Islands and from off Southern Chile (Chiloe). Migratory movement has been proposed by Laptikhovsky et al. (2006), who suggested that Patagonian toothfish in the Falkland Island show two different kinds of migrations: an ontogenic migration from shelf waters into bathyal waters where adults live, and a seasonal adult migration between feeding and reproductive areas, covering distances >1000 km. Our samples were obtained from two localities separated by ca. 13◦ latitude (app. 1400 km). Univariate analyses demonstrated the absence of significant differences in prevalence and mean intensity of infection for both, long lived (encysted larval parasites) and short lived parasites such as digenetic trematodes. Parasites that remain for a long time in the host, like larval anisakids, larval Acanthocephala (Corynosoma sp.) and larval Cestoda (H. trichiuri) can give important clues about migratory movements of the fish host, as suggested by Oliva (2001), for the merluccid M. magellanicus. Migratory movements of D. eleginoides are not supported by parasitological evidence; at least along the Chilean coast, and the low levels of correct assignation in multivariate analyses are an adequate argument to reject the hypothesis of more than one stock of D. eleginoides in southern Chile.
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