Parasites as bioindicators
The very low dissimilarity of infracommunities between sites, as indicated by the global R from ANOSIM, and by the lack of significant differences in species richness, diversity index, and dominance index between conserved and degraded sites, suggest that the ecological conditions (e.g. mangrove coverage) at those sampling sites were not reflected in the structure of the parasite infracomunities of P. velifera. It was probably due to the fact that stress-induced decreases in one species can be countered by increases in another [12]. Even so, the site under restoration showed a significantly lower diversity of parasites, which suggests that restoration efforts have not improved the ecological conditions, at least not to be comparable with the conserved site. According to Marcogliese [7], perturbations in ecosystem structure and function that affect food web topology may also affect parasite transmission, which impacts upon parasite species abundance and composition. It is a very complex issue given the difficulty of determining the particular mechanisms driving differences in parasite community dynamics (e.g. [24]). Nonetheless, it has been observed that ecological disturbance has a negative impact on parasite diversity. For instance, Krause et al. [8] observed that fish Etheostoma nigrum from polluted sites had significantly lower numbers of parasite individuals and species richness than fish from reference sites.
At population level, given that prevalence and intensity of ectoparasite species E. aff. cerastes and Argulus sp. were practically similar between sites, it could be assumed that water quality did no changed through the study area. The exception was the significantly lower prevalence of Ergasilus aff. ceraste in the site under restoration, which could be indicating (to some extent) poorer water quality than in the other sampling sites and, therefore, poor progress in the successful restoration of Bahamitas after 5 years. We got this conjecture considering the fact that ectoparasites are in direct contact with their environment and poor water quality may reduce their vitality or increase their mortality [9, 12]. The prevalence of Argulus sp. was also lower in the site under restoration than in the conserved, but the difference was not significant.
Likewise, the significantly lower prevalence and intensity of C. formosanus in the under restoration and degraded sites may indicate more unfavorable ecological conditions than in the conserved site, where the infection levels of C. formosanus were significantly higher. This parasite requires three host species (snail, fish, and fish-eating birds) to complete their life cycle. We conjecture that the scarce vegetation bordering the under restoration and degraded sites provoked a decrease in abundance of the final bird host which resulted in a decrease of C. formosanus population. When Huspeni and Lafferty [13] evaluated a saltmarsh restoration project, they observed that the prevalence of trematodes of snails (Cerithidea californica) increased in restored sites, which was attributed to an increased bird presence. Aguirre-Macedo et al. [14] observed that the populations of trematodes of snails (Cerithidea pliculosa) decreased after a hurricane, but then started to increase and in 6 years reached parameters similar to those before the hurricane, indicating the ecosystem recovery. Taglioretti et al. [24] showed that the susceptibility of fish-trematode systems to variations in both biotic and abiotic stressors makes them a promising tool for detecting disturbances in aquatic ecosystems. Therefore, trematodes are seen as promising effect indicators so that prevalence is inversely related to the degree of disturbance of aquatic ecosystems [9, 24].
Nonetheless, the use of C. formosanus as bioindicator has to be taken with caution since it is an invasive trematode, which was introduced to Mexico in 1979 with its intermediate snail host (Melanoides tuberculata) and was able to disperse through a variety of fresh- or brackish-water fish in different regions of the country, reaching extraordinarily high infection levels [25]. The snail M. tuberculata has already been reported from the Terminos Lagoon [26], possibly at high abundance since this successful invasive species may be more tolerant to abiotic stressors than native species [27]. This possible high abundance of the first intermediate host plus its low preference for a particular fish host species could account for the high proliferation of C. formosanus.
As mentioned initially, our fish samples were not originally collected for parasitological analysis. Therefore, one shortcoming of this study is the lack of a proper study design, including perhaps more contrasting or distant sampling sites, replication of sites, and examination of freshly sacrificed fish, since preservation prior to dissection results in incomplete quantitative and qualitative data [28]. This situation could have influenced that our parasitological data did not show useful information to provide a confident diagnosis related to ecosystem health. However, in the particular case of the restoration project, the low abundance of trematodes and crustaceans may suggest that strategies of restoration should be improved to achieve better results.
New host-parasite records
Four out of six parasite species herein reported are helminths. According to previous studies, P. velifera is the potential host of at least 11 helminth species: Contracaecum sp., Atrophecaecum astorquii, Stunkardiella minima, Clinostomum complanatum, Saccocoelioides sogandaresi, Ascocotyle tenuicollis, A. megalocephala, A. diminuta, A. macrostoma, A. nana, and Proterodiplostomidae gen. sp. [29,30,31,32]. These records are from freshwater habitats so that their absence in brackish water of the Terminos Lagoon is not surprising. However, except for Contracaecum sp., the parasites we found in P. velifera have not been previously recorded in this fish. The presence of these parasites may be explained by the ecological characteristics of the Terminos Lagoon, which is influenced by both marine and freshwater ecosystems that favor biodiversity, particularly in the interlinked mangrove-seagrass habitat where the highest number of trophic levels may be observed [33].
To the best of our knowledge, the present study represents the first record of a species of Gyrodactylus on P. velifera. According to García-Vásquez et al. [34], 19 species of Gyrodactylus are known to infect poeciliid fishes but P. velifera does not appear in the list. There are approximately 450 species of Gyrodactylus for which delimitation currently requires not only morphometrics but also molecular analyses, a task beyond the scope of the present research. Recently, García-Vásquez et al. [35] pointed out that poeciliids could contribute to the spread of Gyrodactylus cichlidarum, which is a serious pathogen for tilapia. Thus, a more precise identification of the species found in P. velifera is necessary.
Other interesting findings in this study were the parasitic crustaceans; however, a detailed taxonomic study for the correct species designation is needed. Species of Argulus and Ergasilus are typically found on brackishwater fish; however, they have not previously been reported from P. velifera. Ergasilus is a polyphyletic genus that includes approximately 180 nominal species whose delimitation may be confused because of insufficient detail in some older published descriptions [36, 37]. The species of Argulus found in the present study morphologically resembles A. elongatus and A. izintwala, which are distinguished from congeners by their elongated body and a carapace covering only the base of the first pair of legs [38]. We suspect that our specimens represent a new species but a deeper taxonomic study is required.