Pathogens, Vol. 11, Pages 1432: Anisakis Infection in the Spotted Flounder Citharus linguatula (Pleuronectiformes: Citharidae) Caught in the Gulf of Cadiz (Area FAO 27-ICES IXa) Appears to Negatively Affect Fish Growth

1. IntroductionAnisakidosis or anisakiasis is infection by anisakid larvae, acquired through consumption of fish or cephalopods infected with viable third-stage larvae (L3). Anisakidae are a family of parasitic nematodes with a complex life cycle that includes some species which can accidentally infect humans, mostly of the genus Anisakis and, less commonly, of the genus Pseudoterranova [1]. These genera involve crustaceans, cephalopods, and marine fish as intermediate/paratenic hosts and marine mammals as definitive hosts. Rarely, the genera Contracaecum (C. osculatum) and Hysterothylacium (H. aduncum) (this now family Raphidascarididae) have been implicated in human infection [1]. Citharus linguatula (Linnaeus, 1758) (spotted flounder) is a marine flatfish of the order Pleuronectiformes and family Citharidae found along the entire eastern Atlantic coast to 23° S, as well as throughout the Mediterranean as far as the Black Sea. It is a demersal fish, with adults inhabiting soft bottoms from the shoreline to about 300 m depth, although rarely caught at depths greater than 200 m [2]. They feed on small fish and crustaceans [3]. Although it does not have the commercial value of other flatfish of the same size, such as the common sole (Solea solea), its lower price (approximately one-third of that of the common sole in our geographical area) makes it attractive to the consumer. In Andalusia (southern Spain), more than half a million kg of spotted flounder were marketed in the period of 2020 to 2021 [4].

It is a fish that has been little studied as a host of anisakids, but its significant consumption makes it necessary to clarify whether it can pose a risk to human health. For this purpose, the fish available in the fish markets of a city in southern Spain were taken as a reference. Moreover, from a biological and commercial point of view, it would be useful to know if this fish is affected by the presence of the parasite. For this purpose, Fulton’s condition factor and the exponent b of the potential equation relating fish length and weight were calculated. The study shows the modification of growth type in fish parasitized with Anisakis even when parasite intensity is low.

4. DiscussionParasitic nematodes of spotted flounder (C. linguatula) have been little studied, and only a few papers record ascaridoids, such as those belonging to the genera Anisakis (A. simplex s.s. and A. pegreffii), Hysterothylacium (H. aduncum and H. fabri), and some larvae of Contracaecum sp., mainly in waters of the Iberian Peninsula [30,31,32,33,34], but also in the Adriatic Sea [35,36]. Both Hysterothylacium and Anisakis larvae have been detected in this work. The prevalence is similar in both cases (Table 1), but only two fish were found to be parasitized by larvae of both genera, so the prevalence by ascaridoids is almost the sum of the two taxa detected (Table 1). The same is true for the mean abundance.The spotted flounder is a marine flatfish inhabiting soft bottom habitats up to 300 m deep. Throughout its life, it feeds mainly on crustaceans, cephalopods, and fish from its area of influence, which may vary throughout its development. Among the crustaceans, caridean decapods and mysids are the most commonly consumed [37,38], although Belghyti et al. [39] reported a reduction in the consumption of polychaetes, cephalopods, and amphipods, with age associated with an increase in consumption of decapods and molluscs. However, they also reported many other complementary prey, among which copepods, the main first intermediate hosts of Hysterothylacium together with some hyperid amphipods [40], are not frequent. It can thus be suggested that C. linguatula is probably infected by this nematode via paratenic hosts that are predators of copepods; for example, crustaceans such as mysids, decapods, and amphipods, in addition to small fish [11]. This wide variety of spotted flounder prey, which can be hosts for Hysterothylacium, could explain the absence of significant differences associated with the size/age of the fish (Table 3), although there is a trend towards an increase in the epidemiological parameters, probably related to a cumulative effect of parasites in the fish with the consumption of infected prey (Table 3, Figure 4). On the other hand, euphausiids, the main first intermediate hosts of Anisakis, are considered complementary prey which are consumed mainly from 2 years of age onwards [39]. This could explain the significantly higher prevalence and mean abundance of Anisakis in longer/older fish (Table 3, Figure 4).On the other hand, although no significant variations in the condition factor associated with parasitism were detected (Table 2), a modification in the growth of fish infected by Anisakis larvae was observed. This is a change from positive allometric growth in the uninfected fish to negative allometric growth in infected fish (Figure 1 and Figure 2). This trend becomes significant (p = 0.01) when comparing the growth of infected and uninfected fish ≥15.5 cm (size of the smallest fish infected with Anisakis; approximate age 2–2.5 years [28,29]).Although the decrease in fish condition factor associated with high parasite intensity [41,42] that could lead to growth impairment is known [43], to our knowledge this is the first time that significant impairment of fish growth by Anisakis infection at such a low intensity (MI = 1.4, Table 1), without significant modification of the CF, has been reported. However, a significant reduction in CF was observed only in fish ≥17 cm infected with Anisakis (pFigure 4) and mean intensity (MI = 1.83). The condition factor is known to be affected by numerous factors, including the age and/or maturity of the fish (see Figure 3), the season, and the energy availability of the fish [44,45,46,47]. This is of vital economic importance for the fishing industry since, if confirmed in other fish of commercial interest, production yields, whether in commercial fisheries or in fish farming, can be reduced by even mild infections with Anisakis. This has already been shown in fish farms with higher intensities of this nematode (MI = 6.56 [48]). Although unknown factors cannot be ruled out in these changes in the growth of Anisakis-parasitized fish, the fact that they are from the same area and caught within a short period of time leads to the assumption that all fish have been subjected to the same or similar conditions, which makes a cause–effect relationship quite plausible, i.e., that the growth of the fish has been affected by Anisakis infection.However, contrary to what might be expected from previous data, we have observed that parasitized fish have a significantly greater length and weight than uninfected fish (Table 2), as we have previously detected in other fish species parasitized with Anisakis [15,16]. This could be explained by the cumulative nature of these infections since, once the weakest fish are eliminated by predation and/or death, the strongest (and/or those with a lower parasite load) are selected and will attain a greater age, presumably presenting a higher resistance to infection due to having a more robust/mature immune system that allows the parasite and the host to coexist [1,44,45,49,50,51,52,53,54].Finally, the molecular identification of Anisakis larvae showed the majority presence of A. pegreffii (68.75%) together with A. simplex s.s. (18.75%) and larvae with recombinant genotype between the two (12.50%). Although most of the coasts of the Iberian Peninsula are sympatric areas for these Anisakis species, the majority presence of A. pegreffii is common in the Gulf of Cadiz, decreasing in proportion as we move northward along the Atlantic coast of the Iberian Peninsula [55,56].

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