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Helminth parasites of the oceanic horse mackerel Trachurus picturatus Bowdich 1825 (Pisces: Carangidae) from Madeira Island, Atlantic Ocean, Portugal

Published online by Cambridge University Press:  30 August 2011

G. Costa ,
E. Melo-Moreira  and
M.A.A. Pinheiro de Carvalho
G. Costa*
Affiliation:
Estação de Biologia Marinha do Funchal, Universidade da Madeira, Promenade Orla Marítima do Funchal, 9000-107Funchal, Portugal ISOPlexis, Universidade da Madeira, Campus da Penteada, 9000-390Funchal, Portugal
E. Melo-Moreira
Affiliation:
Estação de Biologia Marinha do Funchal, Universidade da Madeira, Promenade Orla Marítima do Funchal, 9000-107Funchal, Portugal
M.A.A. Pinheiro de Carvalho
Affiliation:
ISOPlexis, Universidade da Madeira, Campus da Penteada, 9000-390Funchal, Portugal
*
*Fax: +351291766339 E-mail: gcosta@uma.pt
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Abstract

The helminth parasite fauna of the oceanic horse mackerel Trachurus picturatus Bowdich 1825, caught off the Madeira Islands was composed of six different taxa. Prevalence and abundance of larval Anisakis sp. (Nematoda: Anisakidae) and Nybelinia lingualis (Trypanorhyncha: Tentaculariidae), the most common parasite taxa, were 24.3%, 0.9 and 37.9%, 0.7, respectively. Bolbosoma vasculosum (Acanthocephala: Polymorphidae) and the monogeneans Heteraxinoides atlanticus (Monogenea: Heteraxinidae) and Pseudaxine trachuri (Monogenea: Gastrocotylidae) were comparatively rare. The depauperate helminth fauna of the oceanic horse mackerel at Madeira compared to other geographical regions of the north-eastern Atlantic, namely the Azores banks and the West African coast, may be attributed to the paucity of nutrients off oceanic islands and to a low density of the fish population.

Type
Research Papers
Information
Journal of Helminthology , Volume 86 , Issue 3 , September 2012 , pp. 368 - 372
Copyright
Copyright © Cambridge University Press 2011

Introduction

The oceanic horse mackerel Trachurus picturatus Bowdich 1825 (Pisces: Carangidae) is distributed throughout the north-eastern Atlantic, the eastern central Atlantic, Mediterranean and Black Sea, generally confined to the neritic zones and island shelves, banks and seamounts (Smith-Vaniz, Reference Smith-Vaniz, Whitehead, Bauchot, Hureau, Nielsen and Tortonese1986). Its vertical distribution reaches a depth of 370 m. Feeding is mainly on crustaceans and planktonic copepods, but fish and cephalopods are also of importance in their diet (Gaevskaya & Kovaleva, Reference Gaevskaya and Kovaleva1985; Smith-Vaniz, Reference Smith-Vaniz, Whitehead, Bauchot, Hureau, Nielsen and Tortonese1986; Jesus, Reference Jesus1992). Extensive parasitological surveys were done by Gaevskaya & Kovaleva (Reference Gaevskaya and Kovaleva1980, Reference Gaevskaya and Kovaleva1985) from the Azores banks and Western Sahara Atlantic region, which reported the occurrence of several helminth species and the myxosporean Kudoa nova Najdenova, 1975. These authors found variations in prevalence of several of the parasite species between the regions sampled. Parasites have often proved to be good markers of fish populations (MacKenzie, Reference MacKenzie1990; George-Nascimento & Arancibia, Reference George-Nascimento and Arancibia1992; MacKenzie et al., Reference MacKenzie, Campbell, Mattiucci, Ramos, Pinto and Abaunza2008). To implement the principles of the use of parasites as biological indicators of fish populations recommended by MacKenzie (Reference MacKenzie1987) and MacKenzie & Abaunza (Reference MacKenzie and Abaunza1998), we need to have a detailed account of the parasites infecting a given fish species in the study area(s). The aim of this paper was to assess the parasitism of T. picturatus off Madeira Island, and to compare its parasite composition with those of T. picturatus from other Atlantic regions, in view of suggesting suitable parasites for use as biological indicators of population units.

Materials and methods

Samples of T. picturatus (n = 103) caught at Madeira Island, Atlantic Ocean (32°22′20″N and 16°16′30″W), obtained from purse seining catches in January and February 2005, were purchased at the Fish Landing Auction in the city of Funchal, Madeira Island. In order to examine fresh fish, subsamples of ten fish were obtained and brought to the laboratory at the Marine Biological Station of Funchal, until the total sample number was reached. The total sample consisted of fish ranging in length from 18 to 35 cm (mean ± standard deviation: 22.1 ± 1.9 cm) and in weight from 49.2 to 314.7 g (92.8 ± 27.7 g). All fish were measured in centimetres (cm) and weighed in grams (g). Gills were removed and examined under a binocular microscope for monogeneans and crustaceans. The body cavity was exposed and viscera removed and placed in Petri dishes. Stomachs and intestines were cut into small portions and examined for the presence of cestodes, nematodes, digeneans and acanthocephalans. Body cavities were also examined for parasites. All helminths recovered were fixed in 70% ethanol, cleared in glycerin or lactophenol, and identified according to the relevant literature (Berland, Reference Berland1961; Yamaguti, Reference Yamaguti1963; Khalil et al., Reference Khalil, Jones and Bray1994; Amin, Reference Amin1998). Prevalence and abundance descriptors were calculated according to Bush et al. (Reference Bush, Lafferty, Lotz and Shostak1997). The significance of the relationships between prevalence or abundance of infection and fish length were studied with univariate ANOVA and Spearman's correlation coefficient, using the statistical package SPSS 11.0 (SPSS Inc., Chicago, Illinois, USA). The calculation of the variance/mean ratio (s 2/x), index of dispersion (D) of Poulin (Reference Poulin1993) and confidence limits of prevalence and abundance of infection were done using the program QP 3.0 (Rozsá et al., Reference Rozsá, Reiczigel and Majoros2000).

Results

Two monogenean species were found in the gills of three fish, one with a single specimen of Heteraxinoides atlanticus (Gaevskaya & Kovaleva, 1979) (Monogenea: Heteraxinidae) and two other fish with one specimen each of Pseudaxine trachuri (Parona & Perugia, 1890) (Monogenea: Gastrocotylidae). Two juveniles of the acanthocephalan Bolbosoma vasculosum (Rudolphi, 1819) Porta, 1908 (Acanthocephala: Polymorphidae); 94 L3 larvae of Anisakis sp. type I (Nematoda: Anisakidae) and 75 postlarvae of Nybelinia lingualis Cuvier, 1817 (Trypanorhyncha: Tentaculariidae) were recovered from the 103 fish examined (table 1). One unidentified digenean was found in the visceral cavity of one fish. The two helminth parasites with higher prevalence were the larval Anisakis sp. and the postlarvae of N. lingualis. Table 1 summarizes the results of prevalence, intensity and abundance of the helminth parasites in T. picturatus, whereas table 2 shows the prevalence of Anisakis sp. and N. lingualis in different fish length classes. Estimations of the aggregation indices, variance/mean ratio (s 2/x) and index of discrepancy (D) for Anisakis sp. and N. lingualis suggested that the distribution of Anisakis sp. was overdispersed (χ2 = 25.5, df = 7, P = 0.05, s 2/x = 35.1; D = 0.9), whereas N. lingualis seemed to be randomly distributed (χ2 = 8.2, df = 3, P = 0.05, s 2/x = 1.7, D = 0.7). The relationships between fish length and abundance of Anisakis sp. and N. lingualis were significant at the 0.01 and 0.05 levels (r s = 0.3, P = 0.000; and r s= 0.2, P = 0.04, respectively). Prevalence of N. lingualis increased significantly with fish length (F = 4.5, df = 1, P = 0.04), with mean length of infected fish of 22.6 cm (n = 39) and mean length of uninfected fish of 21.8 cm (n = 64). Similarly, a positive significant relationship was found between prevalence of Anisakis sp. and fish length (F = 12.8, df = 1, P = 0.001), with mean length of infected fish of 23.2 cm (n = 25) against 21.8 cm (n = 78) for the uninfected fish.

Table 1 Prevalence, mean intensity and mean abundance of helminth parasites found infecting 103 Trachurus picturatus from Madeira Island, examined in January and February 2005.

Table 2 Prevalence of Anisakis sp. and Nybelinia lingualis found in 103 Trachurus picturatus from Madeira Island, according to fish length.

Discussion

The helminth parasite fauna of the oceanic horse mackerel, T. picturatus from Madeira Island (present results) was less rich in terms of species than that of the same fish species found in the Azores banks (Meteor and Irving banks), as well as from the West African coast, with only six taxa found in the present study against 17 in the Azores banks, and 15 off the West African coast (Gaevskaya & Kovaleva, Reference Gaevskaya and Kovaleva1980, Reference Gaevskaya and Kovaleva1985) (see table 3). In particular, the digenean fauna was very depauperated in the present survey, with only a single individual of an unidentified digenean recovered. Monogeneans, which were abundant on the gills of T. picturatus from the Azores banks and West African coast, were rare in Madeira, with only three individuals – H. atlanticus (1) and P. trachuri (2) – recovered from the gill filaments of T. picturatus in the present survey. The rarity of the occurrence of these monogeneans during the sampling period could be related to a seasonal effect. Cestodes were restricted to postlarvae of N. lingualis and acanthocephalans to cystacanths of B. vasculosum. Rhadinorhynchus cadenati, a typical acanthocephalan of Trachurus spp. (Gaevskaya & Kovaleva, Reference Gaevskaya and Kovaleva1985; George-Nascimento, Reference George-Nascimento2000; MacKenzie et al., Reference MacKenzie, Campbell, Mattiucci, Ramos, Pinto and Abaunza2008), was not found in the present survey. These results are consistent with those found in a previous survey of 304 T. picturatus in Madeira Island (Gonçalves, Reference Gonçalves1996).

Table 3 Prevalence of helminth parasites recovered from Trachurus picturatus from Madeira Island (present results), Azores banks and Western Sahara (West African Coast) (Gaevskaya & Kovaleva, Reference Gaevskaya and Kovaleva1985). The fish examined from Meteor bank, Irving bank and Western Sahara were 14–25 cm, 34–43 cm and 25–30 cm in length, respectively. When the parasite is present but prevalence was not found it is indicated with ‘Yes’.

According to Arkhipov & Mamedov (Reference Arkhipov and Mamedov1998), the Azores banks, Meteor and Irving, are rich in nutrients, where increased concentrations of phyto- and zooplankton occur. These regions are attractive to planktophagous fish such as T. picturatus and Scomber colias. Being regions of high plankton concentration, the conditions are met for a high availability of intermediate hosts of digeneans, nematodes and acanthocephalans, thus the potential for infections of fish is expected to be higher (Marcogliese, Reference Marcogliese1995, Reference Marcogliese2002). Additionally these regions have intense mixing due to the ocean currents (Arkhipov & Mamedov, Reference Arkhipov and Mamedov1998), providing, for example, a higher probability for eggs of monogeneans to find new hosts to infect. Accordingly, a higher prevalence of monogeneans, as well as of other helminth parasites requiring zooplanktonic intermediate hosts, were found in T. picturatus from those areas compared to Madeira Island (Gaevskaya & Kovaleva, Reference Gaevskaya and Kovaleva1985; present results). Similarly, the West African coast, a shelf region with a higher input of nutrients, compared with the oceanic region of Madeira Island, supports possibly more intermediate hosts, thus enhancing the transmission success of a larger number of parasite species (Gaevskaya & Kovaleva, Reference Gaevskaya and Kovaleva1985; Marcogliese, Reference Marcogliese2002).

Although the influence of nutrients in the water could be a plausible hypothesis, differences in parasite richness between Madeira Island and the Azores seamounts could also be related to sample size and fish length. George-Nascimento (Reference George-Nascimento2000), in his survey of parasites of another carangid species Trachurus symmetricus murphyi, found many fish infected with only one parasite taxon or uninfected (70% of the fish uninfected, sample size = 1831 fish). This means that perhaps by increasing the sample size, more parasite taxa could be found in T. picturatus. Is fish length an important factor? In our study we found significant positive differences in the abundance of Anisakis sp. and N. lingualis with fish length. Additionally, prevalence seemed to have a relationship with length, as fish shorter than 20 cm were not infected with Anisakis sp. and had lower values of prevalence of N. lingualis (see table 2), a trend already observed in a previous survey of parasites of T. picturatus (Gonçalves, Reference Gonçalves1996). The diet of this fish species is known to vary with fish length (Gaevskaya & Kovaleva, Reference Gaevskaya and Kovaleva1985); fish less than 25 cm long feed predominantly on copepods, suitable for transmission of Scolex pleuronectis and hemiuroid digeneans, whereas fish longer than 25 cm prefer cephalopods, which transmit anisakid nematodes and N. lingualis. Thus size seemed to be an important factor for intensity of infection and perhaps for parasite species richness, as evidenced by other authors (Rohde et al., Reference Rohde, Hayward and Heap1995; Brickle et al., Reference Brickle, Pompert and Poulding2002; Poulin & Morand, Reference Poulin and Morand2004).

Parasite species richness may be related to a number of other factors, such as host diet, host population density and differences in habitat characteristics (Poulin & Morand, Reference Poulin and Morand2004). Looking at the landings statistics for T. picturatus in Madeira Island, it appeared that a sharp decrease occurred from 1985 to 2005, from more than 1500 tons to roughly 400 tons from 1996 to date (data from the Fisheries Department of Funchal, unpublished). Thus, a lower population density of this fish species could lead to decreased parasite species richness. Unfortunately, no data on the occurrence of parasites prior to 1996 were available for T. picturatus from Madeira Island. The observed differences in prevalence and intensity of helminth parasites could also suggest that T. picturatus forms local, self-reproducing populations, as already assumed by Gaevskaya & Kovaleva (Reference Gaevskaya and Kovaleva1985).

Comparing the helminth parasite fauna of T. picturatus from Madeira Island with that found in the Azores banks and West of Africa, the following conclusions can be drawn (see table 3). Species characteristic of the genus Trachurus, such as Diplectanotrema trachuri Kovaljova, 1970, Cemocotyle trachuri Dillon & Hargis, 1965, Rhadinorhynchus cadenati Golvan & Houin, 1964, and Lernanthropus trachuri Brian, 1903 (Gaevskaya & Kovaleva, Reference Gaevskaya and Kovaleva1985), were absent in the present study. The generalist species B. vasculosum was only found in Madeira, whereas the generalists N. lingualis and Anisakis sp., were common to other Atlantic regions. It is possible that the monogeneans P. trachuri (with prevalence 80% in the shelf region, 33.3 and 0% in oceanic seamounts, present in Madeira), and Gastrocotyle trachuri (with prevalence 93.3% in the shelf region, and 66.7 and 0% in oceanic seamounts), as well as the trypanorhynch N. lingualis (with prevalence 93.3 and 20% in oceanic seamounts, 37.9% in the oceanic island of Madeira, 0% in the shelf region), could be useful as biological tags in future studies of ecological population structuring of this fish species. Moreover, the high prevalence of the above-mentioned monogeneans in the Azores banks indicate a higher population density of T. picturatus in the seamounts in comparison with Madeira Island, as expected (Stocks & Hart, Reference Stocks, Hart, Pitcher, Morato, Morato, Hart, Clark, Haggan and Santos2007).

Acknowledgements

This work was partially supported by the Portuguese Foundation for Science and Technology (FCT) Pluriannual Programs.

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Figure 0

Table 1 Prevalence, mean intensity and mean abundance of helminth parasites found infecting 103 Trachurus picturatus from Madeira Island, examined in January and February 2005.

Figure 1

Table 2 Prevalence of Anisakis sp. and Nybelinia lingualis found in 103 Trachurus picturatus from Madeira Island, according to fish length.

Figure 2

Table 3 Prevalence of helminth parasites recovered from Trachurus picturatus from Madeira Island (present results), Azores banks and Western Sahara (West African Coast) (Gaevskaya & Kovaleva, 1985). The fish examined from Meteor bank, Irving bank and Western Sahara were 14–25 cm, 34–43 cm and 25–30 cm in length, respectively. When the parasite is present but prevalence was not found it is indicated with ‘Yes’.