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Metazoan parasites in the head region of the bullet tuna Auxisrochei (Osteichthyes: Scombridae) from the western Mediterranean Sea

Published online by Cambridge University Press:  12 September 2014

S. Mele ,
S. Saber ,
M.J. Gómez-Vives ,
G. Garippa ,
F. Alemany ,
D. Macías  and
P. Merella
S. Mele*
Affiliation:
Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, via Vienna 2, 07100Sassari, Italy
S. Saber
Affiliation:
Departamento de Biología Animal, Universidad de Málaga, Campus de Teatinos s/n, 29071Málaga, Spain
M.J. Gómez-Vives
Affiliation:
Centro Oceanográfico de Málaga, Instituto Español de Oceanografía, Puerto Pesquero s/n, 29640Fuengirola, Spain
G. Garippa
Affiliation:
Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, via Vienna 2, 07100Sassari, Italy
F. Alemany
Affiliation:
Centre Oceanogràfic de les Balears, Instituto Español de Oceanografía, Moll de Ponent s/n, 07015Palma, Spain
D. Macías
Affiliation:
Centro Oceanográfico de Málaga, Instituto Español de Oceanografía, Puerto Pesquero s/n, 29640Fuengirola, Spain
P. Merella
Affiliation:
Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, via Vienna 2, 07100Sassari, Italy
*
*Fax: 0039 079 229 464 E-mail: smele@uniss.it
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Abstract

The head region of 72 bullet tuna Auxis rochei from the western Mediterranean Sea (south-east Spain and the Strait of Gibraltar) was examined for parasites. Seven metazoan species were found in the fish from south-east Spain: three monogeneans, two trematodes and two copepods, whereas only three species were isolated in the fish from the Strait of Gibraltar. A comparison of the levels of infection of the parasites according to fish size in south-east Spain showed that the prevalence of Didymozoon auxis and the mean abundance of Allopseudaxine macrova were higher in the larger hosts (range of fork length = 38–44 cm) than in the smaller ones (33–37 cm). A comparison of the parasite infections according to geographical region showed that the mean abundances of Nematobothriinae gen. sp. and Caligus bonito were higher in fish from south-east Spain than in those from the Strait of Gibraltar. A comparison of the parasite fauna of A. rochei from the Mediterranean Sea with the published data on Auxis spp. from the Atlantic, Indian and Pacific Oceans revealed the closest similarity between the Mediterranean A. rochei and the Atlantic A. thazard.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 6 , November 2015 , pp. 734 - 739
Copyright
Copyright © Cambridge University Press 2014 

Introduction

The bullet tuna Auxis rochei (Risso, 1810) (Osteichthyes: Scombridae) is a pelagic fish distributed in tropical and subtropical areas, including the Mediterranean Sea (Uchida, Reference Uchida1981). The limits of its distribution are not well known, mainly because this species is often confused with its congener, the frigate tuna Auxis thazard (Lacepède, 1800), another cosmopolitan fish (Di Natale et al., Reference Di Natale, Srour, Hattour, Keskin, Idrissi and Orsi Relini2009). In fact, the systematics of the genus Auxis is still controversial: some authors consider the species synonymous (Collignon, Reference Collignon1961; Nair et al., Reference Nair, Virabhadra Rao and Dorairaj1970), while others recognize the existence of two distinct species (Yesaki & Arce, Reference Yesaki and Arce1991; Collette & Aadland, Reference Collette and Aadland1996). Although at present the latter hypothesis is the one considered valid (Catanese et al., Reference Catanese, Infante and Manchado2008), recent genetic and morphometric studies showed that A. rochei is the only species distributed in the Mediterranean Sea and in the adjacent areas of the Atlantic Ocean (Orsi Relini et al., Reference Orsi Relini, Palandri, Garibaldi, Lanteri, Cilli, Ferrara and Tinti2008), suggesting that some occurrences of this species from this area could have been misidentified as A. thazard, even in scientific papers (Orsi Relini et al., Reference Orsi Relini, Palandri, Garibaldi, Lanteri and Tinti2009).

Auxis rochei, which is the most abundant tuna in the Mediterranean Sea, represents an important component of the food web (Mostarda et al., Reference Mostarda, Campo, Castriota, Esposito, Scarabello and Andaloro2007) and is exploited by artisanal fisheries, representing 39% of the total tuna landings in the Mediterranean area (9829 t in 2010; FAO, 2011). The migrations of A. rochei in the Atlantic Ocean have rarely been studied; Grudtsev (Reference Grudtsev1992) suggested that it may undertake a trophic migration along the north-west coast of Africa, and Richards & Simmons (Reference Richards and Simmons1971) suggested that spawning took place south of the Islands of Cape Verde. In addition, little is known about its life cycle and migrations in the Mediterranean Sea. Tortonese (Reference Tortonese1963) and Reglero et al. (Reference Reglero, Ciannelli, Álvarez-Berastegui, Balbín, López-Jurado and Alemany2012) reported that A. rochei performs local migrations around the spawning areas in the neritic habitat of the mainland and islands, whereas Sabatés & Recasens (Reference Sabatés and Recasens2001) proposed a spawning migration from the Atlantic Ocean to the western Mediterranean Sea.

Parasites are useful tags to investigate the biology, ecology, migration and population structure of marine organisms (MacKenzie & Abaunza, Reference MacKenzie, Abaunza, Cadrin, Kerr and Mariani2014), and they have also been used successfully to clarify taxonomic relationships between hosts (Whittington, Reference Whittington and Rohde2005). Although the parasites of the head region of representatives of the genus Auxis have been studied in several areas of the world, the confusion in the systematics of A. rochei and A. thazard makes specific information on their parasite fauna perplexing, e.g. in the Atlantic Ocean and Mediterranean Sea records of several parasites assigned to unidentified Auxis sp. (Dollfus, Reference Dollfus1926; Palombi, Reference Palombi1949; Cressey & Cressey, Reference Cressey and Cressey1980) could refer to A. rochei. The aim of this study is to describe the metazoan parasites of the head of A. rochei from the western Mediterranean Sea.

Materials and methods

Collection and examination of fish

A total of 63 A. rochei (32 males and 31 females) caught in the traditional trap fishery of La Azohía (37°32’59”N, 1°10’44”W, south-east Spain, western Mediterranean Sea), were examined for parasites: 21 specimens were collected in May 2008 and 42 in May 2011. An additional group of nine specimens of bullet tuna (six males and three females), caught in the traditional trap fishery of Tarifa (36°00’59”N, 5°37’44”W, Strait of Gibraltar) in May 2008, were examined for comparative purposes. For each individual fish, the fork length to the nearest centimetre was recorded (FL = 33–44 cm).

The heads of fish were excised, stored individually in plastic bags and frozen at − 20°C. Subsequently the samples were defrosted and examined for parasites according to Mele et al. (Reference Mele, Macías, Gómez, Garippa, Alemany and Merella2012). The following literature was used for species identification: for monogeneans, Palombi (Reference Palombi1949), Fuentes Zambrano (Reference Fuentes Zambrano1997), Mogrovejo & Santos (Reference Mogrovejo and Santos2002) and Mogrovejo et al. (Reference Mogrovejo, Lent and Santos2004); for didymozoids, Skrjabin (Reference Skrjabin1955), Yamaguti (Reference Yamaguti1970) and Pozdnyakov & Gibson (Reference Pozdnyakov, Gibson, Bray, Gibson and Jones2008); for copepods, Vervoort (Reference Vervoort1962, Reference Vervoort1965), Cressey & Cressey (Reference Cressey and Cressey1980), Boxshall & Halsey (Reference Boxshall and Halsey2004) and Lin & Ho (Reference Lin and Ho2006).

Data analysis

The prevalence of infection and mean abundance of each parasite species were calculated according to Bush et al. (Reference Bush, Lafferty, Lotz and Shostak1997). Confidence intervals of prevalence and mean abundance were assessed with the Sterne's exact method and the bias-corrected and accelerated Efron–Tibshirani bootstrap, respectively, using the free software Quantitative Parasitology 3.0 (Reiczigel & Rózsa, Reference Reiczigel and Rózsa2005).

Possible correlations between abundance of infection and host size were evaluated using the Spearman rank correlation coefficient, and its significance tested using the R-software (‘spearman’ method, ‘cor.test’ function, ‘stats’ library of the R-software; R Development Core Team, 2014). Levels of infection of each parasite species were calculated for each of two size groups: (1) FL 33–37 cm; (2) FL 38–44 cm. Samples from south-east Spain comprised four groups according to sampling year and host size: group (1) and (2) of 2008 (n= 11 and 22, respectively) and 2011 (n= 10 and 20, respectively). Samples from the Strait of Gibraltar of 2008 belonged only to the host size group (2) (n= 9). Differences between the parasite infections of the five host groups and between host sexes were evaluated using the Fisher exact test for prevalence and the Welsh bootstrap t-test for mean abundance (Reiczigel & Rózsa, Reference Reiczigel and Rózsa2005).

Published and new data on the parasites of the head region of Auxis spp. worldwide were used to assess the dissimilarity between the parasite faunas of the head region of the bullet and frigate tunas from four geographical regions: A. thazard from the Atlantic Ocean (data from Vervoort, Reference Vervoort1965; Fuentes Zambrano, Reference Fuentes Zambrano1997; Mogrovejo et al., 2004; Chisholm & Whittington, Reference Chisholm and Whittington2007), A. thazard from the Indian Ocean (data from Silas, Reference Silas1962; Mogrovejo et al., 2004; Chisholm & Whittington, Reference Chisholm and Whittington2007), A. thazard from the Pacific Ocean (data from Silas, Reference Silas1962; Yamaguti, Reference Yamaguti1970; Mogrovejo et al. 2004; Chisholm & Whittington, Reference Chisholm and Whittington2007) and A. rochei from the Mediterranean Sea (present results). Parasite fauna dissimilarity was evaluated with the Marczewski–Steinhaus distance (‘cc’ method, ‘betadiver’ function, ‘vegan’ library of the R-software) and the Bray–Curtis index (‘–1’ method, ‘betadiver’ function, ‘vegan’ library of the R-software) (Culurgioni et al., Reference Culurgioni, Mele, Merella, Addis, Figus, Cau, Karakulak and Garippa2014; Mele et al., Reference Mele, Pennino, Piras, Bellido, Garippa and Merella2014).

Results and discussion

This study is the first description of the parasite fauna of the head region of A. rochei from the western Mediterranean Sea. A total of seven parasite species were found in and on the hosts from south-east Spain, with 72% being adult didymozoids belonging to two species, Didymozoon auxis Taschenberg, 1879 and Nematobothriinae gen. sp. (table 1). Up to 21% were monogeneans, including Allopseudaxine macrova (Uchida, Reference Uchida1981), Churavera triangula (Mamaev, 1967) and Hexostoma auxisi Palombi, 1943. The remaining 7% comprised two copepod species, Caligus bonito Wilson, 1905 and Unicolax mycterobius (Vervoort, Reference Vervoort1965). Unidentified post-larval stages of didymozoids were found in the gill arch tissues. Only three parasite species were detected in A. rochei from the Strait of Gibraltar: D. auxis (86.7% of all specimens), A. macrova (6.7%) and U. mycterobius (6.6%). Only D. auxis and H. auxisi have been reported previously in Auxis sp. from the Mediterranean Sea (Dollfus, Reference Dollfus1926; Palombi, Reference Palombi1949).

Table 1 Prevalence (%), mean abundance (MA), 95% confidence intervals (CI) and microhabitat of the metazoan parasites in the head region of Auxis rochei from south-east Spain and the Strait of Gibraltar.

FL, fork length; na, no data given; * and ∧  level of significant differences between pairs of samples given as P≤ 0.05.

The unidentified Nematobothriinae gen. sp. has never been described before, therefore it could be a specific parasite of A. rochei in the Mediterranean Sea, although the lack of previous records of this parasite could also be due to the difficulty of detection in the retrobulbar fat tissue. The other parasites have been reported in a wide range of hosts and regions: the congener A. thazard was found to harbour C. triangula in the Atlantic and Pacific Oceans and H. auxisi in the Atlantic Ocean only (Mogrovejo et al., 2004); A. macrova infects several tunas, such as A. thazard, Euthynnus spp., Thunnus albacares and Katsuwonus pelamis, from the three oceans (Bussiéras & Baudin-Laurencin, Reference Bussiéras and Baudin-Laurencin1973; Rohde et al., Reference Rohde, Roubal and Hewitt1980; Gibson et al., Reference Gibson, Bray and Harris2005; Alves & Luque, Reference Alves and Luque2006); C. bonito infects pelagic fish from the Mediterranean Sea (Coryphaena hippurus and K. pelamis; Carbonell et al., Reference Carbonell, Massutí, Castro and García1999; Mele et al., Reference Mele, Macías, Gómez, Garippa, Alemany and Merella2012), the north-west Atlantic Ocean (Thunnus thynnus) and the tropical areas of the Atlantic, Indian and Pacific Oceans (Euthynnus spp., K. pelamis and Sarda spp.; Cressey & Cressey, Reference Cressey and Cressey1980; Öktener & Trilles, Reference Öktener and Trilles2009). In the Mediterranean Sea A. macrova seems to be restricted to A. rochei, since this monogenean was not found in 156 Euthynnus alletteratus and 35 K. pelamis caught within the same sampling programme (Mele, Reference Mele2013). The cross-infection of A. macrova among the Mediterranean tuna could be limited by the different life history and habitat of hosts (Reglero et al., Reference Reglero, Ciannelli, Álvarez-Berastegui, Balbín, López-Jurado and Alemany2012; Rodríguez et al., Reference Rodríguez, Álvarez, López-Jurado, García, Balbin, Álvarez-Berastegui, Torres and Alemany2013).

No significant differences in prevalence and mean abundance were found (P>0.05) between host sexes and years of sampling; therefore the data from south-east Spain were pooled across sex and years, and the hosts from south-east Spain were only divided according to host size (table 1). The highest prevalence was that of D. auxis in host size group (2) (71% in the samples from south-east Spain and 78% in those from the Strait of Gibraltar), being twice that in host size group (1) (33% in the samples from south-east Spain). Significant differences between the mean abundance of three parasites were found: A. macrova had higher mean abundance in host size group (2) from south-east Spain than in host size group (1); Nematobothriinae gen. sp. had higher mean abundance in both host groups from south-east Spain than in that from the Strait of Gibraltar; and C. bonito had higher mean abundance in the host size group (2) from the south-east Spain than in that from the Strait of Gibraltar (table 1). The higher prevalence of D. auxis and the higher mean abundance of A. macrova in the larger A. rochei than in the smaller ones could be due to the different origin of the fish. However, considering that D. auxis infects the definitive host through the food web, these differences could also indicate a change of the diet with size. In fact large fish (>35 cm) can feed on fast-swimming prey including juvenile and adult fish and cephalopods (Mostarda et al., Reference Mostarda, Campo, Castriota, Esposito, Scarabello and Andaloro2007), which are among the intermediate hosts of didymozoids (Felizardo et al., Reference Felizardo, Justo, Knoff, Fonseca, Pinto and Gomes2011). The difference of the mean abundance of Nematobothriinae gen. sp. and C. bonito according to geographical region could also be influenced by the small number of hosts sampled from the Strait of Gibraltar. The level of infection of Nematobothriinae gen. sp. did not change with host size (table 1). Considering that its geographical range is limited to the Mediterranean Sea and that the host cannot lose this tissue parasite with migration, the occurrence of Nematobothriinae gen. sp. only in the Mediterranean A. rochei could indicate that this host population is separated from that of Auxis spp. from other areas. However, the presence of this parasite could go unnoticed in routine parasitological analysis.

A negative relationship between the abundance of U. mycterobius and the host size (–0.27, P= 0.003) was found. This fact could be due to the increased distance between the narine walls in the larger hosts, which will not offer an ideal microhabitat for the parasite to live, wedged in the nasal cavities (Cressey & Cressey, Reference Cressey and Cressey1980).

The parasite fauna of A. thazard from the Atlantic and Pacific Oceans has the highest richness, with nine and eight species, respectively. The poorest is the parasite fauna of A. thazard from the Indian Ocean, with only six species, although this could be due to the scarcity of parasitological studies on this fish from this area. The parasite fauna of A. rochei from the Mediterranean Sea showed the closest similarity with that of A. thazard from the Atlantic Ocean, while the other groups were largely dissimilar (fig. 1). Considering the current debate on host taxonomy and identification, the affinity between the parasite assemblages of the Mediterranean A. rochei and the Atlantic A. thazard could be compatible with the existence of a unique Auxis species throughout the Atlantic Ocean and the Mediterranean Sea (Orsi Relini et al., Reference Orsi Relini, Palandri, Garibaldi, Lanteri and Tinti2009).

Fig. 1 Cluster dendrograms (group-average linkage) of the parasites of the head of Auxis rochei from the western Mediterranean Sea (Ar-Med), and of A. thazard from the Atlantic Ocean (At-Atl), Indian Ocean (At-Ind) and Pacific Ocean (At-Pac), using Marczewski–Steinhaus (A) and Bray–Curtis (B) dissimilarity measures based on the presence/absence data with the cophenetic correlation coefficients having a similar value of 0.89. Sources: Silas (Reference Silas1962), Vervoort (Reference Vervoort1965), Yamaguti (Reference Yamaguti1970), Cressey & Cressey (Reference Cressey and Cressey1980), Murugesh & Madhavi (Reference Murugesh and Madhavi1995), Fuentes Zambrano (Reference Fuentes Zambrano1997), Mogrovejo et al. (2004), Chisholm & Whittington (Reference Chisholm and Whittington2007) and present results.

Acknowledgements

We wish to express our gratitude to the technicians of the laboratory of Mazarrón of the IEO Centro Oceanográfico de Murcia, Spain, to Enrique Majuelos for the assistance during the sampling in Tarifa, and to Rod A. Bray for the revision of the English style and grammar of the manuscript.

Financial support

This work was supported by the Spanish project grants (GPM-3, GPM-4, PARATUN AGL2010-20 892 and EC Data Collection Framework n. 199/2008) and the Regione Autonoma della Sardegna grant (S.M., Master and Back 2012-2013 PRR-MAB-A2013-17 605).

Conflict of interest

None.

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Figure 0

Table 1 Prevalence (%), mean abundance (MA), 95% confidence intervals (CI) and microhabitat of the metazoan parasites in the head region of Auxis rochei from south-east Spain and the Strait of Gibraltar.

Figure 1

Fig. 1 Cluster dendrograms (group-average linkage) of the parasites of the head of Auxis rochei from the western Mediterranean Sea (Ar-Med), and of A. thazard from the Atlantic Ocean (At-Atl), Indian Ocean (At-Ind) and Pacific Ocean (At-Pac), using Marczewski–Steinhaus (A) and Bray–Curtis (B) dissimilarity measures based on the presence/absence data with the cophenetic correlation coefficients having a similar value of 0.89. Sources: Silas (1962), Vervoort (1965), Yamaguti (1970), Cressey & Cressey (1980), Murugesh & Madhavi (1995), Fuentes Zambrano (1997), Mogrovejo et al. (2004), Chisholm & Whittington (2007) and present results.