Size and number of monogenean species

Six monogenean species, Pseudokuhnia minor, Kuhnia scombri, K. sprostonae, K. scombercolias, Grubea cochlear and G. australis have been reported to date from the gills and pseudobranchs of scombrid fishes (see Rohde & Watson, Reference Rohde and Watson1985a, Reference Rohde and Watsonb; Rohde Reference Rohde1986, Reference Rohde1989a, Reference Rohdeb). Considerable variability has been found in both body and hamuli length in specimens of the same species collected from different geographical areas and from different hosts (Rohde & Watson, Reference Rohde and Watson1985a, Reference Rohde and Watsonb). Values obtained for total body length and size of the large hamuli for Pseudokuhnia minor in Madeiran samples were close to those obtained for the same fish species from South African Atlantic waters (mean length = 1.72 and 1.56 mm respectively; hamuli 42  μm mean length and 38–42  μm respectively). On the other hand specimens from the Mediterranean and Spanish Atlantic coastal waters, were smaller (mean length 1.12 mm) (Rohde & Watson, Reference Rohde and Watson1985a). The total body length of K. scombri from Madeira was closer to measurements obtained for South African samples of this species (3.18 and 2.87 mm respectively), when compared with values for Mediterranean (1.1–2.4 mm) and south Atlantic waters of Brazil (1.49–3.44 mm) (Rohde & Watson, Reference Rohde and Watson1985b). Kuhnia scombercolias collected from Madeira also showed a larger body size (1.6–2.64 mm) and slightly larger hamuli (37.5–67.5 μm), while in specimens from Ecuador and Brazil the size of hamuli varied between 36 and 55 μm. The three species P. minor, K. scombri and K. scombercolias recovered from Madeiran waters, in summary, are more closely related to South African specimens than to those from Mediterranean and south-western Atlantic waters, in terms of body length and hamuli size, thus confirming the existence of geographical variation in these parameters.

Prevalence, abundance and intensity of infection

The most common monogenean species found on the gills of S. japonicus was P. minor reaching a maximum prevalence of 98.7% (n = 151). Kuhnia scombri and K. scombercolias also showed relatively high prevalences (43.7 and 39.1% respectively in sample 1), whereas Grubea cochlear and K. sprostonae were rarely observed (see table 2). The prevalence of K. scombri in other regions of the Atlantic differed considerably, with high values being obtained for the Northeast Atlantic (60–75% in S. scombrus; Somdal & Schram, Reference Somdal and Schram1992) and off continental Portugal (73.9% in S. japonicus; Rego, Reference Rego1985). Contrasting with those high prevalences, only 1.1% of chub mackerel from Argentinean waters were infected with K. scombri (Cremonte & Sardella, Reference Cremonte and Sardella1997), 11% in Brazilian waters (Alves et al., Reference Alves, Luque and Abdallah2003) and 6.6% in North Pacific waters (Pozdnyakov & Vasilenko, Reference Pozdnyakov and Vasilenko1994). These data suggest that this parasite is better adapted to colder temperate waters of the North Atlantic, with Madeira serving as an intermediate region between the colder temperate waters of the North Atlantic and the south Atlantic waters. Of course there are other factors that can mask the differences in prevalence, as for example fish size, although in the present study no correlation between prevalence and fish size was observed. Furthermore, the lengths of chub mackerel examined by Alves et al. (Reference Alves, Luque and Abdallah2003) were similar to those examined in Madeira (20–32 cm). Likewise, the mean length of fish collected from the Skagerrak (North Atlantic) was 30 cm, and prevalence with K. scombri ranged from 76 to 100% (Somdal & Schram, Reference Somdal and Schram1992). Kuhnia sprostonae which, according to Rohde & Watson (Reference Rohde and Watson1985b), is characterized by having a wide geographical distribution, encompassing Pacific waters of Australia, south Atlantic waters of Brazil, coastal waters of Ecuador and the North Sea, was not recovered by Alves et al. (Reference Alves, Luque and Abdallah2003) in coastal waters of Brazil, nor from Argentinean waters by Cremonte & Sardella (Reference Cremonte and Sardella1997). Although present in Madeira, this species was extremely rare (present work). On the other hand K. scombercolias, which is morphologically similar to K. sprostonae, but with a smaller total body and hamuli length (see Rohde & Watson, Reference Rohde and Watson1985b; Rohde, Reference Rohde1989b), was a relatively frequent species in Madeira (39.1%) and in the South Atlantic waters of Brazil (46%, Alves et al., Reference Alves, Luque and Abdallah2003). This monogenean was not recovered from North Atlantic and Argentinean waters. It may be better adapted to warmer waters, being replaced in colder waters by K. sprostonae (found in Helgoland, Plymouth, Madeira, southern Australia; while K. scombercolias found in Ecuador, northern New South Wales, Australia, Perth, Western Australia, São Paulo, Brazil and Madeira). Pseudokuhnia minor, the monogenean with the highest prevalence, intensity and abundance in Madeiran waters (present work) was surprisingly not found by previous authors in Atlantic waters off Portugal (Rego, Reference Rego1985; Rego et al., Reference Rego, Carvalho-Varela, Mendonça and Afonso-Roque1985) and the southwestern Atlantic (Cremonte & Sardella, Reference Cremonte and Sardella1997; Alves et al., Reference Alves, Luque and Abdallah2003). Nevertheless Rohde & Watson (Reference Rohde and Watson1985a) studied this monogenean from South African Atlantic waters, Mediterranean and Atlantic waters of Spain, although they did not consider prevalence and intensity. Therefore it is not possible to compare the frequency of occurrence of this monogenean in different geographical regions where it is present, in order to reach more accurate conclusions about the links of those regions and the distribution of this parasite. Apparently P. minor has a more restricted distribution, with preference for warmer waters (Madeira, present work; New South Wales in Hayward et al., Reference Hayward, Perera and Rohde1998). Finally, Grubea cochlear was rare in both S. japonicus and S. scombrus, with low prevalences ranging from 3.3% in Madeira, 6% and 18% in Brazilian waters (Rego & Santos, Reference Rego and Santos1983; Alves et al., Reference Alves, Luque and Abdallah2003), while it occurred in S. scombrus with a prevalence of 2.5% in Portuguese waters (Rego et al., Reference Rego, Carvalho-Varela, Mendonça and Afonso-Roque1985) and 3.4% in the Mediterranean (Parukhin et al., Reference Parukhin, Naidenova, Nikolaeva and Vodjanichky1971). Grubea cochlear differs significantly from the other species by its larger size (up to 10 mm in length). The low number of individuals of G. cochlear both in the present study (five individuals) and elsewhere (see Rohde, Reference Rohde1986) do not allow conclusive statements about the geographical variation of the species, although the species has been recovered from S. scombrus and S. japonicus from the Atlantic Ocean, Mediterranean and Indo-Pacific waters (Rego & Santos, Reference Rego and Santos1983; Rohde, Reference Rohde1986; Somdal & Schram, Reference Somdal and Schram1992; Alves et al., Reference Alves, Luque and Abdallah2003).

The mean abundance of K. scombri was higher in Madeiran waters (0.98–1.17) and at the austral region (0.14–2.25) (Rohde & Watson, Reference Rohde and Watson1985b) whereas in Brazil and Argentinean waters lower values were obtained (0.2 and 0.01 respectively) (Cremonte & Sardella, Reference Cremonte and Sardella1997; Alves et al., Reference Alves, Luque and Abdallah2003). The mean abundance of K. scombercolias was higher in Brazil (3.7) followed by Madeiran waters (0.20–0.71) and the austral region (0.39–1.20) (Alves et al., Reference Alves, Luque and Abdallah2003; present work). The mean abundance of P. minor reached 13.72–24.47 in Madeiran waters, and from 1.29 to 6.13 at the austral region. Taking into account that P. minor is much smaller than K. scombri and K. scombercolias, its high intensities could also mean that this species adopted a strategy of closeness to other members of the species, for defence purposes or cooperative feeding (see Bush et al., Reference Bush, Fernández, Esch and Seed2001). An increase in parasite numbers for P. minor from November to August observed in Madeiran waters, may be due to parasite reproduction occurring on the fish host when the water temperature rises. However, this assumption would need an experimental study in order to fully comprehend the life cycle of this monogenean.

In a study of the monogenean Gyrodactylus turnbulli of guppies, Poecilia reticulata, Scott (Reference Scott1987) concluded that parasites became more aggregated as their numbers increased, due to direct reproduction of parasites on individual fish. Furthermore, according to this author, the best indicator of the degree of aggregation is the s ²/x ratio. In our case this ratio was higher for P. minor and increased in the summer (14.16, see table 5). For K. scombri, relatively high values of the s ²/x ratio were obtained (see table 5) indicating that at least for these two species, the parasites were aggregated.

The prevalence and abundance of the four monogeneans, Pseudokuhnia minor, K. scombri, K. scombercolias and K. sprostonae from the scombrid Scomber australasicus in New South Wales showed similar trends to values obtained at Madeira (Hayward et al., Reference Hayward, Perera and Rohde1998). Consequently, for fish of the same length range, the highest prevalence and intensity was found for P. minor (58.7–78.2%; 1.56–6.13), followed by K. scombercolias (38.1–59%; 0.87–1.15), K. scombri (34.4–74.5%; 0.49–2.25) and K. sprostonae with the lowest values (1.6–5.5%; 0.03–0.05). A positive association found in the intensities of P. minor and K. scombri in the present work may have several explanations (Hayward et al., Reference Hayward, Perera and Rohde1998). One possible explanation could be an increase in susceptibility to infection, once one of the parasites settles on the host gills or one species could establish the microhabitat for the second species.

The occurrence of monogeneans in Scomber japonicus at Madeira, with the disparity of degrees of prevalence and intensity, may lead to the conclusion that Madeiran waters represent an interesting mixing point for the monogeneans, with species more frequent in colder waters, such as K. sprostonae, species characteristic of warmer waters, such as K. scombercolias, and species with wide geographical distributions such as K. scombri. Pseudokuhnia minor, which seems to be more host-specific, having been recorded from S. japonicus and S. australasicus only, apparently has a preference for warmer waters, with higher intensities occurring when the water temperature rises (present study). Further studies on the influence of temperature in the abundance of P. minor are in progress in order to test this assumption. Its presence in South African and Madeiran samples in S. japonicus may indicate a relationship between host populations in these areas, in contrast to its absence from Brazilian populations.