Anisakinae nematodes in two commercial marine fish from the East Pacific of Baja California, México

Size: px

Start display at page:

Download "Anisakinae nematodes in two commercial marine fish from the East Pacific of Baja California, México"

Rosanna Walters
6 years ago
Views:

Anisakinae nematodes in two commercial marine fish from the East Pacific of Baja California, México By M.A, Rodríguez-Santiago* J.A, Rosales-Casián and M.I.

and the ocean whitefish Caulolatilus princeps, collected in coastal waters of San Quintin, Baja California, México. Anisakis sp.

1 Anisakinae nematodes in two commercial marine fish from the East Pacific of Baja California, México By M.A, Rodríguez-Santiago* J.A, Rosales-Casián and M.I. Grano- Maldonado Abstract This study documents temporal changes in abundance and prevalence of larval anisakid nematodes in two commercially important fish; the vermilion rockfish Sebastes miniatus, and the ocean whitefish Caulolatilus princeps, collected in coastal waters of San Quintin, Baja California, México. Anisakis sp., Hysterothylacium aduncum and Pseudoterranova decipiens (Anisakidae) were found in S. miniatus, while H. aduncum and P. decipiens were present in C. princeps. The vermilion rockfish constitutes a new host for H. aduncum; C. princeps is a new host for Anisakis sp. and H. aduncum. San Quintin constitutes a new geographic locality for Anisakis sp. and H. aduncum. Hysterothylacium aduncum was the most abundant parasite (S. miniatus =37; C. princeps =15.5), and Anisakis sp. was the most prevalent species (S. miniatus =91.8%; C. princeps =95%). The nematode abundance increased in summer in both S. miniatus and C. princeps. Both species were highly infected with nematode larval stages of Anisakis sp, P. decipiens, and H. aduncum (S. miniatus: 10,323 specimens, C. princeps: 2,575 specimens). These fish constitute one of the most important ground fish resources for recreational and commercial fisheries in Baja California (Mexico) and California (USA), and make up a substantial part of the regional seafood cuisine. Except for Anisakis sp. 1, the others anisakid species appear to show less organ specificity because they were found in almost all internal organs; their importance as a potential of human infection cannot be excluded due to possible migration to muscle, and fish should be gutted soon after capture to avoid worm migration into flesh. *Corresponding Author marodriguez@conacyt.mx Pacific Science, vol. 70, no. 2 December 16, 2015 (Early view)

2 Introduction In the northwestern coasts of Mexico, the ocean whitefish, Caulolatilus princeps Jenyns, 1842 (Malacanthidae), and the vermillion rockfish, Sebastes miniatus Jordan and Gilbert 1880 (Scorpaenidae) are two high-valued fish species that are caught year-round by both coastal commercial and recreational fishing (Rosales-Casián and Gonzalez-Camacho 2003, Rodriguez- Santiago and Rosales-Casián 2008). The vermillion rockfish is found from Prince William Sound, south Alaska to central Baja California, and inhabits rocky reefs, kelp forests and sea canyons at depths of m, but occurs most commonly at m (O Connell et al. 1992, Love et al. 2002). The ocean whitefish inhabits rocky reefs from 10 to 150 m depth (Hammann and Rosales-Casián 1990) and its distribution extends from Vancouver Isle in British Columbia (Canada) to Peru, including the Galapagos Islands (Dooley 1978). The vermillion rockfish represents a potential intermediate host for many parasites; it is a prey for final hosts such as the California sea lion (Lowry et al. 1991). In spite of their high economic importance, there are not enough studies focused on the nematode parasites in S. miniatus and C. princeps in Baja California. Helminthological studies in wild animals are important because they lead to a better understand of the behavioral links between host and parasite in nature, and when wild animals are hunted or fished, it is necessary to consider possible risks for human consumption. The present study is focused on nematodes of the family Anisakidae, which are one of the most common parasites of marine organisms, from crustaceans, fishes, and cephalopods to marine mammals (Navone et al. 1998, Purivirojkul 2009). The occurrence of anisakid larvae in these organisms is of great importance for human health (Eguia et al. 2003, Gomez et al. 2004, Rodríguez-Santiago and Rosales-Casián 2011), as well as for economic (Inoue et al. 2000) and ecological reasons (Klimpel et al. 2004, Podolska et al. 2006, Klimpel et al. 2007, Rodríguez- 2

3 Santiago et al. 2014, Rodríguez-Santiago et al. 2015). Infection in humans by these parasites (anisakiasis) usually occurs by ingesting raw marine fish and invertebrates infested with the third-stage larvae (Anderson 1992, Szostakowksa et al. 2002, Doupé et al. 2003). This disease is characterized by acute stomach infections, allergic reactions or anaphylaxis. Information about nematodes in commercially important fish species from the Mexican Pacific coasts is scarce. The present study identifies the larval anisakid nematodes of S. miniatus and C. princeps, from the coasts of San Quintin, Baja California, Mexico. We also provide information on the changes in the prevalence and abundance of parasites with respect to time, and its relations with the host size, weight, and seawater temperature. Materials and Methods The two fish species were sampled bimonthly from February to December Individuals were obtained from the sport-fishing catches of six sites located in the outer coast of San Quintin bay, Baja California, México (between: "N "W "N "W) (Figure 1). San Quintín bay is located 310 km south of the California border (USA) (Figure 1), and six kilometers to El Molino Viejo (Old Mill), the departure and arrival site of the fishing boats. The commercial and the sport fishery targets many pelagic and bottomliving fish species (Rosales-Casián and Gonzalez-Camacho 2003, Rodríguez-Santiago and Rosales-Casián 2011) from the surface to 150 m depth, and as far as 50 km from Punta Entrada, a rocky point outside of the bay. <<Figure 1 near here>> A total of 91 specimens of C. princeps and 210 specimens of S. miniatus were analyzed. The specimens were measured (total length, TL) using a measurement board with divisions to millimeter, and weighed (g) with a digital balance Accu-Lab (6 kg ± 1 g). The surface seawater 3

4 temperatures during 2005 (ºC) were obtained from the boat captains report at arriving. Temperatures at m depth were obtained from station of the IMECOCAL program (Lat N, Long W), located close to Isla San Martin (García-Córdova et al. 2005). Fish specimens were dissected, and their organs stored in plastic bags on ice. In laboratory, internal organs (gills, liver, spleen, intestine, pyloric cecum, heart, gonads, digestive tract) were examined under a stereoscopic microscope (LEICA-DMBL 10), and all parasites were removed. Helminths were fixed and preserved following Rodríguez-Santiago et al. (2014). Nematodes were fixed in Berl s liquid, preserved in ethyl alcohol (70 %), cleared with a solution of phenol ethanol (Lent s solution), and mounted with glycerin-gelatin. Identification of parasites was carried out using morphological data and identification keys (Anderson et al. 2009, Gibbson 2010). The parasitological material was deposited in the Ecology Fisheries Laboratory of the Center for Scientific Research Higher Education of Ensenada, Baja California (CICESE), México. Data analysis Species richness, prevalence (% P), and parasite abundance (parasite number/host) were determined according to Bush et al. (1997). Due to non-normality and heteroscedasticity of data, a non-parametric analysis of Kruskal-Wallis was used to determine differences in the parasite abundance of each species with respect to time. Fisher s Least Significant Difference LSD was used as a post-hoc test. A Mann-Whitney U test was used to assess significant differences in parasite prevalence between the two species of host fish. Spearman rank correlations were used to assess relationships between the parasite abundance and the host size, weight, and seawater temperature (ºC). 4

5 Results The examined specimens of C. princeps ranged from 370 to 510 mm of total length and those of S. miniatus from 280 to 610 mm. In C. princeps, a total of 2,575 larval of Anisakis sp. 1 and Hysterothylacium aduncum (Rudolphi, 1802) were found. Anisakis sp.1 Dujardin, 1845 was found in the mesentery only, whereas H. aduncum was found in mesentery, stomach, and intestine cecum (Table 1). In S. miniatus, a total of 10,323 individuals of Anisakis sp. 2, H. aduncum and Pseudterranova decipiens (Krabbe, 1878) were found. In both fish hosts, the anisakid species showed the highest overall prevalence, followed by H. aduncum (Table 1). <<Table 1 near here>> In C. princeps, prevalence of Anisakis sp. 1 ranged between 72% and 100%, and for S. miniatus the Anisakis sp. 2 ranged between 82.8% and 100% (Figure 2). These two species of Anisakis showed high prevalences during almost all the year with a slight decrease in winter. The prevalence of H. aduncum showed a similar tendency in both fish species, with relatively high values from February to June, followed by a slight decrease between October and December (Figure 2a, c). When comparing the prevalence values of H. aduncum in both hosts and between Anisakis sp. 1 and Anisakis sp. 2, no significant differences were found (Mann-Whitney U tests, p > 0.05). In the case of P. decipiens, it was present from April to August, only, with a prevalence range from 4.8% to 7.1% (Figure 2d). <<Figure 2 near here>> On the other hand, the most abundant nematode species in both fish species was H. aduncum (Table 1). This species was most abundant in June in both hosts (S. miniatus = 48.4 ± 10.2 SE ind/host; C. princeps = 24.7 ± 4.1 ind/host) and less abundant in April for S. miniatus (15.6 ± 2.7 ind/host) and December for C. princeps (7.9 ± 2.7 ind/host). In both host fish, Anisakis sp. and Hysterothylacium showed a similar tendency, as the highest abundance occurred 5

6 in June and the lowest between February and December (Figure 2a). Significant monthly changes were found in the abundance of Anisakis sp. 1 (KW, H = 21.1, p < 0.01), Anisakis sp. 2 (KW, H = 23.5, p < 0.01) and H. aduncum (KW, H = 21.1, p < 0.01). Prevalence did not change significantly with size and weight of hosts or with surface seawater temperature (Table 1). The highest abundance of nematodes occurred in summer months (between June and August) when surface water temperature reaches the highest values (Figure 3), and the lower abundance in winter (December to February) when water temperature decreases. A low but significant and positive correlation (r = 0.15, p < 0.05) was found between abundance of H. aduncum and weight of S. miniatus. <<Figure 3 near here>> Discussion Larvae of Anisakis sp. and Hysterothylacium aduncum have been recorded from most of the pelagic and demersal fishes studied in the Mexican Pacific coasts, (Laffon-Leal et al. 2000). In the present study, the vermilion rockfish (S. miniatus) constitutes a new fish host for H. aduncum. The ocean whitefish (C. princeps), is registered as new host for Anisakis sp. and H. aduncum. The San Quintín coast constitutes a new geographic locality for all these parasite species. These nematode species appear to show less organ specificity as they were found in almost all internal organs. The percentage of S. miniatus specimens infected by Anisakis larvae was relatively high (prevalence = 91.8%) compared with other congeneric fish species (Sebastes capensis, %) (Dominguez-Ortega et al. 2001). Rhode (1993) considered that an important latitudinal effect with respect to metazoan species richness and prevalence is found, suggesting that they increase towards low latitudes close to the equator. Also, Scott (1982) indicated that parasite species 6

7 richness is higher in hosts with extensive latitudinal distributions, however in the present study, a low species richness but with high prevalence for the two species of host fish was found. Although the parasite abundance in S. miniatus and C. princeps showed some seasonality, it was not related to length, weight, or water temperature during our study period; possibly, a seasonality effect could be due to fish migration. A positive correlation (r = 0.15, p < 0.05) was found only between abundance of H. aduncum and weight of S. miniatus, indicating that larger individuals of this fish had a higher abundance of this parasite species. Also, the variation in the parasite abundances can be due to the availability of prey, a change in feeding spots, or the arrival of more parasitized species during winter. Few studies about Anisakis sp. have been conducted in the region, Ferre (2001) attributed the high prevalence of third larval stage of anisakids in fish to an ichthyophagous diet. The genus Anisakis has a cosmopolitan distribution, although is more abundant in temperate and polar environments (Anderson 1984, Grabda 1991, Dick and Choudhury 1995). Anisakis larvae usually do not harm the fish because these are intermediaries or paratenic hosts, although the larvae migrate to the flesh from the intestine or stomach (Williams 1994). The anisakids found in this study were similar to the third stage larvae of A. simplex, however, future genetic analysis will be necessary to separate species of Anisakis sp. to confirm their identity at species level. This study determined that fish caught commercially near San Quintin Bay are infected with larval anisakids, which pose a potential hazards to human health. The anisakid nematode larvae found in the mesentery (digestive tract) can migrate to the muscle, and this migration may occur sometime after the fish has been caught. After liberation from the capsule, motility of anisakid larvae was observed after 16 h of cooling in the viscera of Sphyraena barracuda (Laffon-Leal et al. 2000). Therefore, fish should be gutted as soon as they was caught to avoid 7

8 migration of worms into flesh. Additional studies should be carried out in situ to evaluate if other commercial or recreational fish species are heavy infected with these nematodes. Acknowledgements Amparo Rodriguez-Santiago thanks to CONACYT for the scholarship awarded to her Doctoral program. Thanks to Gorgonio Ruiz (UABC Ensenada), Sharon Herzka and Ernestina Castro (CICESE Ensenada), and Emma Fajer (CIAD Unidad Mazatlán) for their help and laboratory facilities. This study was funded by two CICESE projects headed by Jorge A. Rosales-Casián: internal project "Analysis of the recreative and sport fishing catches from San Quintin, B.C., Mexico", and the UC MEXUS external project "Baseline study of the nearshore non-reef fishes of Bahía de Los Ángeles, B. C., Mexico, prior to proposed development". 8

9 Table 1. Nematode infections in Caulolatilus princeps and Sebastes miniatus from the coast of San Quintín, Baja California, México. Total number of nematodes per taxa (TNP), prevalence (%P), mean abundance (MA ± SE) of nematodes. Localization (L) in host body; G = gills, IC = intestinal cecum, S = stomach, I = intestine, M = mesentery, CC = coelomic cavity, Stw = stomach wall. HOST FISH SPECIES PARASITE SPECIES L TNP % P MA Caulolatilus princeps (n = 91) Anisakis sp. 1 M 1, ± ± 2.5 Hysterothylacium aduncum 1 M, S, I, IC 1, ± ± 3.1 Sebastes miniatus (n = 210) Anisakis sp. 2 CC, Stw, I, M 3, ± ± 3.9 Hysterothylacium aduncum 2 M, S, I 6, ± ± 18.0 Pseudoterranova decipiens S, M, I, IC ± ± 0.2 9

10 Figure 1. Location of the sport fishing area on coast of San Quintín, Baja California, México. 10

11 Figure 2. Prevalence and mean abundance (MA ± SE) of nematodes in Caulolatilus princeps (a, b), and Sebastes miniatus (c, d) from the coast of San Quintín, Baja California, México. 11

12 Figure 3. Nematode abundance over time in Sebastes miniatus and Caulolatilus princeps and the surface seawater temperature off the coast of San Quintín, Baja California, México 12

13 Literature Cited Anderson R. C The origins of zooparasitic nematodes. Can. J. Zool. 62: , ed Nematode parasites of vertebrates. Their development transmission. C. A. B. International, Cambridge. ---, A. G. Chabanaud, and S. Willmott, eds Keys to the nematode parasites of vertebrates: Archival volume. C. A. B. International, New York. Bush, A., K. Lafferty, J. Lotz, and A. Shostak Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 83: Castillo-Sánchez, E., Rosales-Casián, J. A., and G. Pérez-Ponce De León Helmintos parásitos de (Osteichthyes: Paralichthydae) en el estero de Punta Banda, bahía de Todos Santos y bahía de San Quintín, Baja California, México. Cienc. Mar. 24: Dick, I., and A. Choudhury, eds Fish diseases disorders. Protozoan Metazoan infection. Department of Zoology, University of Guelph, Ontario. Domínguez-Ortega, J., A. Alonso-Llamazares, L. Rodríguez, M. Chamorro, T. Robledo, J. M. Bartolomé, and C. Martínez Cócera Anaphylaxis due to hypersensitivity to Anisakis simplex. Int. Arch. Allergy Immunol. 125: Dooley, J. K Systematics biology of the tilefishes (Perciformes: Branchisoterigidae and Malacanthidae) with description of two new species. NOAA Tech. Rep. NMFS Circ. 411: Doupé, R. G., G. J. Ridge, and A. J. Lymbery Visible implant fluorescent elastomer tags as pedigree markers for applied aquaculture: an evaluation using black bream Acanthopagrus butcheri. Aquacult. Res. 34:

14 Eguia, A., J. M. Aguirre, M. A. Echevarria, R. Martinez-Conde, and J. Ponton Gingivostomatitis after eating fish parasitized by Anisakis simplex: a case report. Oral Surg. Oral Med. Oral Patho. Oral Radio. Endod. 96: Ferre, I Anisakiosis y otras zoonosis parasitarias transmitidas por consumo de pescado. Rev. Aquatic. 14:1-21. Grabda, J., ed Marine fish Parasitology: An outline. U. C. H. Publishers, New York. Hammann, M. G., and J. A. Rosales-Casián Taxonomía y estructura de la comunidad de peces del Estero de Punta Banda y Bahía de Todos Santos, B. C., México. Pages in J. Rosa-Vélez and F. González-Farías, eds. Temas de Oceanografía Biológica en México, Universidad Autónoma de Baja California, Ensenada. Inoue, K., S. I. Oshima, T. Hirata, and I. Kimura Possibility of anisakid larvae infection in farmed salmon. Fish Sci. 66: Klimpel, S., E. Kellermanns, H. W. Palm, and F. Moravec Zoogeography of fish parasites of the pearlside (Maurolicus muelleri), with genetic evidence of Anisakis simplex (s.s.) from the Mid-Atlantic Ridge. Mar. Biol. 52: Klimpel, S., H. W. Palm, S. Ruckert, and U. Piatkowski The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea). Parasitol. Res. 94:1 9. Laffon-Leal, S. M., Vidal-Martinez, V. M., and G. A rjona-torres Cebiche A potential source of human anisakiasis in México?. J. Helminthol. 74: Love, M. S., E. Caselle, and L. Snook Fish assemblages around seven oil platforms in the Santa Barbara Channel area. Fish. Bull. 98: , and M. Moser A checklist of parasites of California, Oregon and Washington marine and estuarine fishes. NOAA Tech. Rep. NMFS SSRF

15 ---, M. Yoklavich, and L. Thorsteinson The rockfishes of the Northeast Pacific. University of California Press, Los Angeles. Lowry, M., B. Stewart, C. Heath, and P. Yochem Seasonal and annual variability in the diet of California sea lions Zalophus californianus at San Nicolas Island, California, Fish. Bull. 89: Navone, G. T., N. H. Sardella, and J. T. Timi Larvae and adults of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda: Anisakidae) in fishes and crustaceans in the South West Atlantic. Parasite 5: O connell, V. A., D. A. Gordon, A. Hoffmann, and K. Hepler Northern range extension of the vermilion rockfish (Sebastes miniatus). Calif. Dept. Fish Game. 78:173. Pérez-Ponce De León, G., L. García Prieto, and C. Rosas Villa Helmintofauna de Opisthonema libertate y Harengula thrissina (Osteichthyes: Clupeidae) de la bahía de Chamela, Jalisco, México. Rev. Biol. Trop. 48(4): Podolska, M., J. Horbowy, and M. Wyszynski Discrimination of Baltic herring populations with respect to Anisakis simplex larva infection. J. Fish Biol. 68: Purivirojkul, W An investigation of larval ascaridoid nematodes in some marine fish from the Gulf of Thailand. Kasetsart J. Nat. Sci. 43: Rhode, K., ed Ecology of marine parasites: an introduction to marine parasitology. University of Queensland Press, Armidale. Rodríguez-Santiago, M. A., and J. A. Rosales-Casián Abundance and size composition of vermilion rockfish, Sebastes miniatus (Jordan Gilbert 1880), from sport fishing catches of San Quintín, Ensenada, Baja California, México. Bull. South. Calif. Acad. Sci. 107:

16 ---, J. A. Rosales-Casián, and M. I. Grano-Maldonado Dynamics of a parasite assemblage of the vermilion rockfish Sebastes miniatus from northwestern Baja California, Mexico. Helgol. Mar. Res. 68: , S. Gómez, J. A. Rosales-Casián, and M.I. Grano-Maldonado Parasitic Copepods of the vermilion rockfish Sebastes miniatus (Pisces: Scorpaenidae) from inshore waters of Baja California (Eastern Pacific). Neotrop. Helminthol. 9(1):1-12. Rosales-Casián, J. A., and J. R. González-Camacho Abundance and importance of fish species from the artisanal fishery on the Pacific coast of northern Baja California. Bull. South. Calif. Acad. Sci. 102: Roubal, F. R Observations on the seasonal occurrence of two species of transversotrematid Digenea parasitising the sparid fish Acanthopagrus australis in Moreton Bay, eastern Australia. Folia Parasitol. 45: Scott, J. S Digenean parasite communities in flatfishes of the Scotland shelf and Southern Gulf of St. Lawrence. Can. J. Zool. 60: Sekerak, A. D., and H. P. Arai Some metazoan parasites of rockfishes of the genus Sebastes from the northeastern Pacific Ocean. Syesis 10: Siri-Chiesa, M., and P. Moctezuma-Hernández., eds La pesca de Baja California. Universidad Autónoma de Baja California, Ensenada. Szostakowska, B., P. Myjak, and J. Kur Identification of anisakid nematodes from the southern Baltic Sea using PCR-based methods. Mol. Cell. Probes. 16: Van Thiel, P. H Anisakiasis. Parasitology 52: Williams H. A. J., ed Parasitic worms of fishes. Taylor Francis, London. Yamaguti, S., ed Systema Helminthum. III. The Nematodes of vertebrates. Interscience Publishers, New York. 16

Scomberomorus Commerson, a New Paratenic Host of Contracaecum sp. and Anisakis sp. (Nematoda: Anisakidae) from Persian Gulf

World Journal of Fish and Marine Sciences 5 (3): 310-314, 2013 ISSN 2078-4589 IDOSI Publications, 2013 DOI: 10.5829/idosi.wjfms.2013.05.03.71232 Scomberomorus Commerson, a New Paratenic Host of Contracaecum