Parasites as biological tags in the south-western Atlantic Ocean

At present only seven studies involving the use of parasites as biological tags in the south-western Atlantic have been published, two of them aimed at discriminating stocks of non-fish hosts, the dolphin Pontoporia blainvillei (Aznar et al., Reference Aznar, Raga, Corcuera and Monzón1995) and the shortfin squid, Illex argentinus (González & Kroeck, Reference González and Kroeck2000).

The rest of the studies have been carried out on fish of commercial importance, the first two suggesting the potential of parasites to be used as biological tags for the discrimination of both the Argentine hake Merluccius hubbsi and the New Zealand hake M. australis in the waters around the Malvinas (Falkland) Islands, southern Chile and Argentina (MacKenzie & Longshaw, Reference MacKenzie and Longshaw1995) and of the mackerel Scomber japonicus in two zones of the Argentine Sea (Mar del Plata, 37–38°S, and El Rincón, 39–41°S) (Cremonte & Sardella, Reference Cremonte and Sardella1997).

The first study using parasites for the delineation of fish populations was carried out on a sample of 671 specimens of Argentine anchovy Engraulis anchoita (see Timi, Reference Timi2003). The use of biological tags allowed the identification of four stocks of this species in the south-west Atlantic, south of 34°S, one composed of autumn samples (35–37°S) and three of spring samples. Among the latter, a Patagonian group (43–46°S) was clearly separated from a Bonaerense group, which was divided into two groups: North Bonaerense (34–40°S) and South Bonaerense (40–43°S). The biological tags identified as markers for populations of anchovies in this region agreed, in general, with those groups indicated as suitable biological tags for other pelagic and planktophagous fish species (MacKenzie, Reference MacKenzie1983). Some of them are specific for anchovies and others are very common parasites of many fish species; among spring samples Pseudanthocotyloides heterocotyle, Lecithochirium microstomum, Parahemiurus merus, Scolex polymorphus and Corynosoma australe were characteristic of the northern region, whereas Cardiocephaloides sp., Anisakis simplex, Contracaecum sp. and Hysterothylacium aduncum were more prevalent in southern waters.

The second study was carried out on 344 specimens of Argentine hake M. hubbsi, by testing previous hypotheses based on ichthyological studies on the existence of four hake populations in this zone (Sardella & Timi, Reference Sardella and Timi2004). Fish were caught in the Argentine–Uruguayan Common Fishing Zone (35°30′–38°S/53°30′–56°W), San Matías Gulf (46°30′S, 66°30′W), San Jorge Gulf (46°30′S, 66°30′W) and Patagonian Shelf (45°50′–47°10′S, 60°20′–63°10′W). Despite no differences being found between the two most southern samples, the use of biological tags allowed the identification of three stocks of hake in the south-west Atlantic. Univariate analysis on both parasite populations and infracommunity descriptors, as well as a multivariate discriminant analysis, allowed the identification of one stock composed of hake from the Argentine–Uruguayan Common Fishing Zone, a second stock of fish from San Matías Gulf and a third comprising samples from both San Jorge Gulf and the Patagonian Shelf. Northern samples were characterized by low values of prevalence for most parasite species, with the exception of Corynosoma australe and Grillotia sp. 1. Among Patagonian hake, Anisakis simplex showed similar values of prevalence in all zones, while fish from San Matías Gulf were characterized by Kudoa rosenbuschi, Grillotia sp. 1 and Contracaecum sp.

More recently Timi et al. (Reference Timi, Luque and Sardella2005), in a study on a larger geographic scale, identified two stocks of striped weakfish Cynoscion guatucupa, in the south-west Atlantic. A total of 297 fish were caught in Brazil, Uruguay and Argentina; univariate analysis on parasite populations, as well as multivariate discriminant analysis, calculated for juvenile and adult fish separately, allowed the identification of one stock from Argentina and Uruguay and another from Brazil. Southern samples were characterized by a higher prevalence and abundance of larval endohelminths, whereas in the northern stock, gastrointestinal and ectoparasitic species were common. Discriminant analyses on parasite infracommunities of Brazilian fish showed notable differences between juvenile and adult hosts; no such trend was observed in fish from Argentina and Uruguay, despite differences between juveniles and adults at population level. Again, the species C. australe and A. simplex were identified among the suitable biological tags.

Reasons for the success of the method in the south-western Atlantic

A common feature of all previous studies, even those not designed to discriminate stocks, is a successful finding of differences among the compared fish groups. The question arises: why is the discrimination of fish populations in this region so easy by using biological tags? The answer is to be found in the basis of the method.

The biological tags method is ultimately based on the geographical distribution of parasites. The geographical distance between conspecific host populations is no doubt a key determinant of the likelihood that exchanges of parasite species occur between these populations (Poulin & Morand, Reference Poulin and Morand1999). Therefore, the underlying assumption of this method is that hosts can become infected only when they are within the endemic area of a parasite (that geographical region in which the conditions are suitable for transmission). For parasites with direct life cycles the endemic area is mainly determined by environmental conditions, whereas for parasites with indirect life cycles, an additional requirement is that suitable hosts for all the developmental stages must be present (MacKenzie & Abaunza, Reference MacKenzie and Abaunza1998).

The distribution patterns of marine parasites, in particular, are mainly determined by temperature–salinity profiles and their association with specific masses of water (Esch & Fernández, Reference Esch and Fernández1993).

The marine environment in the Atlantic continental shelf of South America shows a structural complexity governed by the dynamics of different masses of water. Water circulation in the south-west Atlantic is characterized by the Brazil Current (warm and saline water) flowing southwards along the continental margin, and the Malvinas (Falklands) Current (cold, low-salinity subantarctic water) flowing northwards at the edge of the Argentine shelf (Martos, Reference Martos1989). Both currents meet on the continental slope near 38°S, creating a strong frontal zone, which marks the division between subtropical and subantarctic waters. The Malvinas (Falklands) Current dominates adjacent shelf waters, producing a latitudinal gradient of temperature which decreases southwards, whereas at the northern limit of the Argentine sea, the effect of the warm Brazil Current is marked (Martos, Reference Martos1989; Bakun & Parrish, Reference Bakun and Parrish1991). The discharge of the De La Plata river strongly influences the oceanographic conditions at the north of the Argentine Sea by reducing salinity, mainly north of 38°S (Guerrero & Piola, Reference Guerrero, Piola and Boschi1997).

As a consequence of the gradient in environmental conditions, the distribution of zooplankton and definitive hosts is also influenced. For example, in the Argentine Sea, zooplankters may be assigned to three water masses – coastal at the north to Península Valdes, middle shelf, and outer shelf, influenced by the Malvinas (Falklands) current waters – each one with its characteristic specific composition (Ramírez et al., Reference Ramírez, Mianzán, Santos and Viñas1989). This distribution pattern determines that in each zone fish have a different diet (in quantity and composition), which is reflected in variations in diet specificity and changes in prey size (mainly due to the presence of euphausiids and hyperiids) as both latitude and distance from the coast increase for anchovies (Angelescu, Reference Angelescu1982), and an increase in consumption of crustaceans by hakes in those zones where availability of zooplankton is higher (Prenski & Angelescu, 1993).

Timi (Reference Timi2003) tested the possible influence of oceanographic conditions on the distribution of parasites by using as a model the Argentine anchovy, a widely distributed fish on the continental shelf. The sampling scheme covered the south-west Atlantic shelf from 34°S (Uruguayan coasts) to 46°S (San Jorge Gulf, Patagonia), and parasite populations and communities were analysed in relation to latitude, as an indirect measurement of the gradient in environmental conditions characteristic of the region. Ordination of infracommunities in a correspondence analysis based on parasite abundances in individual fish showed a gradual displacement of fish through the first axis, which accounted for most of the variance of the data. An indirect gradient analysis (a correlation between fish scores and latitude at which fish were caught) showed that the position of each fish in the bidimensional space was significantly related to latitude, when it was used as an explanatory variable. Therefore infracommunities followed a latitudinal pattern in the space determined by the axes.

At component community level, prevalence of parasite species showed a similar pattern. At both infracommunity and component community levels, the superimposition of the species scores indicated that some parasites behaved differently from the average pattern at some sites and their presence was related to given zones; for example C. australe was directly related to northern samples, whereas A. simplex was associated with southern samples.

Therefore, there are unquestionable latitudinal gradients in the distribution of parasite assemblages of anchovies. This is a consequence of the effect of environmental conditions on the distribution of individual parasite species. Indeed, it was found that prevalence and mean abundance of many parasites varied functionally with latitude; the values of the coefficients of determination showed that a high proportion of the variation of these parameters is explained by this variable.

Rohde & Heap (Reference Rohde and Heap1998) concluded that water temperature, rather than latitudinal gradients, affects the spatial distribution of parasite communities. Therefore, temperature, as a measurement of energy input, is a good predictor of latitudinal gradients in species richness and diversity (Rohde, Reference Rohde1992, Reference Rohde1999), so the great influence of latitude on populations and communities of parasites of E. anchoita could be due mainly to the thermal gradient, characteristic of the study area (Bakun & Parrish, Reference Bakun and Parrish1991; Hoffmann et al., Reference Hoffmann, Núñez, Piccolo and Boschi1997).

Perspectives for the use of biological tags in the south-western Atlantic

It is clear from previous studies that the three host species share a group of suitable biological tags, comprising species with extremely low specificity, given their presence in almost all the host species studied in the area, among which A. simplex and C. australe are conspicuous examples (see Timi et al., Reference Timi, Sardella and Navone2001; Sardella et al., Reference Sardella, Mattiucci, Timi, Bastida, Rodriguez and Nascetti2005).

More importantly, independent of variations of parasite burdens among host species due to differential habits, diet, size, etc., of fish, this group of parasites displays the same latitudinal pattern in all hosts. Indeed, their distribution patterns can be reinforced by trophic relationships among host species. In fact, anchovy is the main prey of both M. hubbsi (Prenski & Angelescu, 1993) and Cynoscion guatucupa (Cordo, Reference Cordo1986), among many other species of predators (Angelescu, Reference Angelescu1982), and it can transmit larval stages of species that involve paratenic hosts in their life cycles (for example anisakid nematodes).

Therefore, on the basis of existing information it can be predicted that these few species should be enough for discriminating populations of other fish species in further studies.

This prediction becomes realistic only if predictability in parasite burdens can be found. Unfortunately, there are no long-term studies on temporal repeatability in population attributes of fish parasites in the south-western Atlantic. However, some evidence does support this postulate. Timi & Poulin (Reference Timi and Poulin2003) showed that, despite finding no repeatability of parasite community structure across samples of E. anchoita, parasite species of 16 component communities from four host populations, sampled in a period of 3 years, occurred as a nested subset pattern. In other words, species in depauperate component communities, irrespective of host size, geographical origin and year of capture, were non-random subsets of the species that occurred in progressively richer assemblages, indicating that there are some general, large-scale processes structuring parasite communities at the level of host species. Timi et al. (2005) analysed specimens of C. guatucupa taken at Argentinean coasts, which were caught over a long period of time (>10 years) overlapping the dates of capture of weakfish from both Uruguay and Brazil. Both similarity and multivariate analyses showed that Argentinean fish were similar to Uruguayan fish, caught in a single catch, whereas they were more homogeneous in terms of parasite community structure than Brazilian weakfish, caught during a 1-year period. Therefore, differences in sampling periods seem to have no marked effects on the parasite community structure.

Concluding remarks

Water circulation on the continental shelf in the south-western Atlantic Ocean determines a characteristic thermal gradient, which in turn influences the latitudinal distribution of parasites, allowing the identification of stock units of fish hosts.

Given the broad latitudinal distribution of most fish species in the region (see Cousseau & Perrotta, Reference Cousseau and Perrotta1998) and the presence of a group of parasite species suitable as biological tags with low specificity (they are common in all, or most, host species studied), involving paratenic hosts in their life cycles, with marked variations in their latitudinal distribution and temporal predictability of their populations, the use of parasites as biological tags in the region will be a successful tool to be applied in future studies, not only for delineation of host populations, but also for the identification of harvest locations.