First assessment of the metazoan parasite community of the Argentine menhaden Brevoortia pectinata (Jenyns, 1842) (Clupeiformes: Alosidae) off Rio de Janeiro, southeastern BrazilAbstract
Brevoortia pectinata is important for the fish industry and crucial for the ecology of South Atlantic marine environments. Despite this importance, the structure of the parasite community of B. pectinata has never been investigated. We evaluated for the first time the parasite community structure from a population of B. pectinata, off the State of Rio de Janeiro, Brazil, and the factors influencing it. One hundred fish were bought from local fisherman at Sepetiba Bay (22°57’44”S; 43°52’28”W). Detailed parasitological examination revealed that all fish were parasitized by at least one parasite. We found 14 parasite taxa: 3 monogeneans, 4 copepods, 1 isopod, 3 digenetics and 3 nematode larvae. Presence of both adult and larvae indicated that B. pectinata occupies an intermediate trophic level, acting as definitive and intermediate / paratenic host. The community had low diversity and was dominated by the monogeneans Mazocraeoides georgei and Kuhnia sp., whereas the endoparasites were less prevalent and abundant. Fish schools and host specificity seem to be important for ectoparasite infestation, and host diet influenced the infection by trophic-transmitted endoparasites. Fish sex and body length exerted weak influence in the parasite community structure, which was depauperate and non-interactive.
Key words
Alosidae; Brazil; ecology; marine fish; Neotropical region; parasite community
INTRODUCTION
The Brazilian Atlantic coast has 8,500 km of extension, including bays and lagoons that are rich environments for fish establishment and development (Araújo et al. 1998). The Sepetiba Bay is in the State of Rio de Janeiro and is considered an important aquatic ecosystem with a rich ichthyofauna (Isaac et al. 2006). Such a diverse ichthyofauna makes Sepetiba Bay an area of intense artisanal and industrial fishing exploitation (Costa 2020, Verba et al. 2020).
Popularly known as menhadens, fishes of the genus Brevoortia are migratory and commonly found in estuarine coastal waters, where juveniles develop and form large schools (Nelson et al. 2016, Wang et al. 2022). Currently, seven nominal species of Brevoortia are known, in which B. aurea (Spix & Agassiz 1829) and B. pectinata (Jenyns, 1842) occur in the South Atlantic (Froese & Pauly 2024). The Argentine menhaden B. pectinata feeds mainly on plankton and is found from the coast of Rio de Janeiro, Brazil to that of Bahía Blanca, Argentina (Sanchez 1989, Froese & Pauly 2024). This species is both economically and ecologically important, since it is widely explored by the fishing industry (Lorenzo et al. 2015, Biolé et al. 2020) as well as is preyed upon several organisms of higher trophic levels (Prisco et al. 2001, Norbis & Galli 2004, Cazorla & Forte 2005, De Wysiecki et al. 2018).
In the South Atlantic, studies on the ecological aspects of metazoan parasites of Brevoortia spp. are scarce. In addition to Tavares et al. (2004) who studied the fauna of parasites from B. aurea at the State of Rio de Janeiro, Brazil, in a more ecological manner, there have been a few taxonomic reports of monogeneans infesting B. aurea (Kohn & Santos 1988, Kohn & Cohen 1998) also in Brazil, and crustaceans infesting B. tyrannus (Latrobe, 1802) in other countries (Kroger & Guthrie 1972, Trilles 2007). The parasite community structure of B. pectinata has never been accessed, and the monogenean Mazocraeoides argentinensis Suriano, 1979 found at Mar del Plata, Argentina (Suriano 1981), represents the only parasite reported in this host. Therefore, the aim of the present study was to evaluate, for the first time, the community structure of metazoan parasites of B. pectinata from Spetiba Bay, State of Rio de Janeiro, Brazil.
MATERIALS AND METHODS
Fish sampling and analysis of parasites
From December 2022 to February 2023, 100 specimens of B. pectinata (total length: 27.4 ± 3.6 [20.0–33.5] cm; weight 218.2 ± 78.1 [81.0–375.0] g) captured in Spetiba Bay (22°57’44”S; 43°52’28”W), State of Rio de Janeiro, southeastern Brazil, were bought directly from local fisherman. Fish taxonomic identification was according to Figueiredo & Menezes (1978), and nomenclature and classification updated following Froese & Pauly (2024). Most fish were analyzed fresh, but some were maintained frozen at -20°C, prior to examination.
All internal organs (esophagus, stomach, large and small intestine, mesentery, heart, liver, gonads, gallbladder and musculature), nostrils, gills, eyes, opercula, body cavity and surface, were individually analyzed for parasites, using a stereomicroscope. The metazoan parasites were collected and processed according to standard parasitological techniques (Eiras et al. 2006). The taxonomic identification of parasites followed specific literature pertinent to each taxon. Helminth vouchers were deposited in the Coleção Helmintológica do Instituto Oswaldo Cruz (acronym CHIOC), and crustaceans were deposited in the Coleção do Museu de Zoologia da Universidade de São Paulo (acronym MZUSP), both located in Brazil.
Evaluation of parasite community structure and statistical analyzes
To evaluate the parasite community structure, we considered prevalence and mean abundance as population descriptors, according to Bush et al. (1997). Diversity measured by Brillouin index (HB), frequency of dominance (percentage of infracommunities in which a parasite species was dominant) and relative dominance (number of specimens of the most abundant species / total number of parasites in the infracommunity), were used as community descriptors (Rohde et al. 1995, Magurran 2004). The index of dispersion (ID; variance/mean ratio of parasite abundance) and the discrepancy index (D; which ranges from 0 = fully random or uniform to 1 = fully aggregated) were used to evaluate the distribution of parasite species within the host population (Poulin 1993).
We tested if body length was different between male and female fish, using the Mann-Whitney test (Zar 2010). The correlation between host body length and abundance of each parasite species or HB was tested using Spearman correlation (Zar 2010). Differences in parasite prevalence between male and female hosts were evaluated using Fisher’s exact test (Zar 2010). Differences in abundance of each parasite species and HB between male and female hosts were evaluated using the Mann-Whitney test (Zar 2010).
For testing possible interspecific interactions of parasites, we considered taxa that co-occurred in the same site of infestation or infection. In this sense, two types of generalized linear models were adjusted, Poisson and logistic regression for parasite abundance and prevalence, respectively (Dohoo et al. 2003). We considered as response variable the abundance or prevalence of the most dominant species and as explanatory variables those of the remaining species. The models were set with and without interaction among the explanatory variables, and the best-fit model was chosen based on the Akaike information criteria, using the stepwise method in both directions (Harrell 2001). The odds ratios (OR) for the explanatory variables of the best-fit models were calculated to evaluate their relationship with the response variable, in which 0 < OR < 1 indicates negative association, OR = 1 indicates absence of association and OR > 1 indicates positive association (Dohoo et al. 2003). Moreover, the 95% confidence intervals (CI) for the odds ratios were estimated, and if 1 was within the range, the association between the variables was considered invalid.
Only the parasite taxa with prevalence ≥ 10% were considered in the statistical analyzes, to avoid statistical bias due to low sample size (Bush et al. 1997, Zar 2010). We used only non-parametric inferential statistics because the data distribution was not normal, even after transformation, and p ≤ 0.05 was considered for rejection of the null hypothesis (Zar 2010). Analyzes were run using the software Quantitative Parasitology (Reiczigel et al. 2019) and RStudio (RStudio Team 2020).
RESULTS
A total of 14 parasite taxa were collected in the 100 B. pectinata analyzed (Table I). All hosts were parasitized by at least one taxon of parasite. There were three digeneans, three monogeneans, three nematodes in larval stage (L3), four copepods and one isopod (Table I). Monogeneans were the most prevalent and abundant parasites and, except by the copepod Nothobomolochus cresseyi Timi & Sardella, 1997, the other taxa showed prevalences lower than 15% and mean abundances lower than one (Table I). Such a situation was also reflected by frequency of dominance and relative dominance, in which the monogeneans Mazocraeoides georgei Price, 1936 and Kuhnia sp. were the most dominant, followed by N. cresseyi that was dominant in only 3% of the infracommunities (Table II). Only eight parasite taxa showed sufficient prevalence and abundance to calculate dispersion and discrepancy indices (Table III). These were mostly aggregated within the host population, except for M. georgiei, Kuhnia sp. and N. cresseyi that tended to show a uniform distribution (Table III). The mean HB of the parasite component community was 0.77 ± 0.31 (0.10–1.51).
Values of variance to mean ratio of parasite abundance (ID) and index of Discrepancy (D) of eight metazoan parasites of Brevoortia pectinata from the Sepetiba Bay, State of Rio de Janeiro, Brazil.
Frequency of dominance and mean relative dominance of metazoan parasites of Brevoortia pectinata from the Sepetiba Bay, State of Rio de Janeiro, Brazil.
Deposition number (DN), prevalence (P), mean abundance ± standard deviation (MA±SD), and site of infection / infestation (SI) of metazoan parasites of Brevoortia pectinata from the Sepetiba Bay, State of Rio de Janeiro, Brazil.
Female fish were slightly bigger than males in that total body length were 28.4 ± 3.5 (n = 47) and 26.6 ± 3.5 (n = 53), respectively. Such a difference was statistically significant (U = 1617.5; p = 0.014). However, HB was not different between male and female hosts (U = 1414; p = 0.24) and not correlated with fish body length (p = 0.65). The abundances of the digenean Myosaccium ecaude Montgomery, 1957 and of the nematode Contracaecum sp. were positively correlated with the host total length (rs = 0.203, p = 0.042 and rs = 0.224, p = 0.024, respectively). The only difference regarding the parasitism between male and female hosts was in the prevalence of Contracaecum sp., which was higher in females (23.4%) than in males (5.7%) (X2 = 5.12; p = 0.01).
We observed concurrent infestations by Cribromazocraes travassosi Santos & Kohn, 1992, Kuhnia sp., M. georgei and N. cresseyi. Since M. grorgei was by far the most dominant species, it was considered as response variable in the Poisson and regression models. The stepwise method indicated similar models for both Poisson and logistic regressions. The best-fit model included all explanatory variables with and without interactions. No interspecific interaction was observed using prevalence, since logistic regression indicated no significant relationship among the variables (p values were higher than 0.8). Considering the parasite abundance, there was a positive association between M. georgei and Kuhnia sp. (p < 0.001; OR = 1.03; CI = 1.02–1.04), and the association was negative when the abundances of C. travassosi, Kuhnia sp. and N. cresseyi were put in interaction (p = 0.02; OR = 0.98; CI = 0.97–0.99).
Concurrent infections possible to test were observed between M. ecaude and Parahemiurus merus (Linton, 1910) that co-occurred in the intestine, and between the unidentified digenetic and Contracaecum sp. that were present in the mesenteries. Since these models included only two variables each, their order of insertion would not change the results and there was no need for the stepwise method. The prevalence of M. ecaude and P. merus had a positive association (p = 0.04; OR = 5.08; CI = 1.07–24.11), but their abundances were not associated (p = 0.42). In the co-infections by the unidentified digenean and Contracaecum sp., there was no association between the prevalences or the abundances (p > 0.24).
DISCUSSION
Since this is the first work investigating the parasite community of B. pectinata, the genera Anisakis, Contracaecum, Hysterothylacium, Kuhnia and the species Caligus itacurusnesis Luque & Cezar, 2000, C. travassosi, M. georgei, M. ecaude, Neobomolochus elongatus Cressey, 1981, N. cresseyi, Parashiinoa bakeri (Cressey & Cressey, 1986), P. merus and Olencira praegustator (Latrobe, 1802) represent new parasite records for this host.
The parasite community of B. pectinata studied here was dominated by ectoparasites, especially monogeneans. A similar pattern was observed for the parasite fauna of B. aurea from the State of Rio de Janeiro (Tavares et al. 2004). Such dominance by ectoparasites on these hosts may be related to their occurrence in large schools, and to the fact that ectoparasites have short and direct life cycles, which favor their transmission (Mackenzie & Abaunza 1998, da Silva et al. 2022). Similar results have been observed in parasite communities from fish other than Clupeiformes, but that also form schools, off Rio de Janeiro (Cezar & Luque 1999, Paschoal et al. 2023). Moreover, the parasite community of B. pectinata was composed of both larvae (represented exclusively by nematodes) and adults, suggesting that this fish occupy an intermediate trophic level in the local trophic chain and, consequently, exert important ecological role in this ecosystem.
Ectoparasites commonly are more host specific than endoparasites (Poulin 1992). In the present study, it is plausible to assume that the monogenean M. georgei is more specific to species of Brevoortia. In addition to the present observations, this parasite has been reported in other species of Brevoortia with high prevalence and abundance (Kohn & Santos 1988, Tavares et al. 2004). Since the monogenean Kuhnia sp. could not be identified to species level, it is not prudent to discuss about its host specificity, even though it was the second most dominant species. Regarding the crustacean ectoparasites, although N. cresseyi was dominant in only 3% of the present infracommunities, it showed high prevalence and abundance when compared with infestations on other clupeiform fish, off Rio de Janeiro (Moreira et al. 2015, Benicio et al. 2022). Such an observation may indicate greater host specificity of N. cresseyi for B. pectinata rather than for other clupeiform fishes. In fact, the attachment structures of ectoparasites normally are adapted to their site of infestation on host, which may vary biometrically according to the fish species (see Kabata 1979, Oliveira et al. 2022).
Most parasites tend to have an aggregated distribution within their host populations (Crofton 1971, Shaw & Dobson 1995, Poulin 2007). However, prevalent, abundant and dominant parasites may have more uniform distribution, since they are both quantitatively and qualitatively present in a host population. This pattern was observed in the present study, in which the most dominant parasites represented by M. georgei, Kuhnia sp. and N. cresseyi were evenly distributed in B. pectinata population, whereas the other parasite taxa that showed much lower prevalence and abundance, were more aggregated. It should be mentioned that Morrill et al. (2022), using prediction models in a meta-analysis, found a negative association between abundance and aggregation for ectoparasites, but not for endoparasites. Furthermore, these authors observed that the factor species was the most predictive of parasite aggregation, which is interesting since life history is crucial for the parasite to reach its host.
It is important to highlight that, as stated by Poulin (1993), the D is more efficient for measuring parasite distribution among host population than the ID, which was originally proposed for evaluating the distribution of free-living organisms in the environment. This could be clearly observed in the present results (see Table III), in which ID was highly affected by high values of parasite abundance, and its variations were not proportional to D values. In fact, parasite prevalence has no direct effect in ID (since it is based only on abundance), whereas it is implicit in D representing an important advantage of this index when dealing with parasites (see Poulin 1993 for more details).
According to the data compilation by Luque et al. (2017), parasite richness and diversity are higher for freshwater fish in South America. These authors suggested that geographic isolation and the uneven research efforts towards freshwater environments are responsible for such a pattern. In fact, previous studies with sample sizes such as the present one indicate that parasite diversity in clupeiform fish off Rio de Janeiro tend to be low, in which the mean HB values have been lower than one (Tavares et al. 2005, Moreira et al. 2015, Chaves & Paschoal 2020, Benício et al. 2022, da Silva et al. 2022). However, the diversity of the present parasite community was the highest among those of other sympatric clupleiforms (Tavares et al. 2005, Moreira et al. 2015, Chaves & Paschoal 2020, Benício et al. 2022, da Silva et al. 2022). What specifically contributes to the diversity observed here cannot be accessed, but host specificity by ecoparasites, fish schooling, and diet that is linked to endoparasite transmission, certainly are important factors related to this diversity.
The influence of sex and body length on the structure of parasite communities from clupeiform fish seem to be stochastic, in some host species it is observed (Tavares et al. 2005) whereas in others it is not, or the influence is weak (Tavares et al. 2004, Moreira et al. 2015, Chaves & Paschoal 2020, Benício et al. 2022, da Silva et al. 2022). Here, we observed that although females were larger than males, the only sexual difference was in the prevalence of Contracaecum sp., which was higher in females. Moreover, host body length correlated only with the abundances of the trophic-transmitted endoparasites Contracaecum sp. and M. ecaude. Therefore, it is plausible to assume that larger fish, with a consequent greater energy requirement, consume more food, being more exposed to larval parasites that are frequently available in the intermediate host populations, as may be the case of Contracaecum sp. and M. ecaude.
Holmes (1990) in his pioneering work searching for patterns and processes that structure the parasite communities in marine fish, suggested that interactions between species are weak. It seems to be confirmed by the present results and by previous findings for other Clupeiformes, since there was little interference regarding the presence or absence of different species sharing the same guild, in a same host individual (see also Moreira et al. 2015, Chaves & Paschoal 2020, Benício et al. 2022). However, two important points should be highlighted. First, Holmes (1990) considered only gastrointestinal helminths, thus all endoparasites. Second, in some cases, it was possible to observe positive associations between the abundances of M. georgei and Kuhnia sp. in co-infestations, and between the presence of M. ecaude and P. merus in co-infections. Positive association between abundances of the endoparasites Rhiphidocotyle sp. and Hysterothylacium sp. was also reported in the clupeiform Cetengraulis edentulus (Cuvier, 1829) (Benício et al. 2022). These observations may seem contradictory to Holmes (1990) suggestion, but they are not. Such positive associations can be easily explained by the exposure of the host to interspecific parasites with similar infection / infestation routes, which are also similarly abundant, frequent and have equal probabilities of finding their host. These factors are more plausible than direct interspecific interactions between parasites, favoring their abundance or prevalence mutually. The values of OR close to 1.00 and broad CI observed here statistically reinforce the evidence that species interaction was weak in the present study.
Interestingly, in the model including interaction of all ectoparasites that occurred in co-infestations, there was a negative association among parasite abundances. In this case, direct interference among these parasites cannot be discarded, or perhaps host’s ability to withstand parasite infestation becomes saturated at some point, resulting in a decline in parasite abundance. Despite some indications of interactions between species, the present parasite community seems to be genuinely more isolationist than interactive, following Holmes (1990) conception.
Although B. pectinata represents a valuable economic resource, largely explored in the food trade, as well as has important ecological role in the marine ecosystems, acting as both predator and prey (De Wysiecki et al. 2018, Biolé et al. 2020), the parasite fauna of this fish remained poorly understood so far. Such a situation turns clear with basis on the present results, in which 13 taxa are reported parasitizing B. pectinata for the first time, highlighting the importance of our work. Moreover, this first ecological evaluation of the parasite community structure of B. pectinata, revealed some features that seem to be common in parasite communities of clupeiform fishes, which are: low overall diversity, high dominance by a few species (normally ectoparasites), ectoparasites with higher host specificity than endoparasites, non-interactive species, and marked influence of host diet and schooling behavior (Tavares et al. 2005, Moreira et al. 2015, Chaves & Paschoal 2020, Benício et al. 2022, da Silva et al. 2022). Finally, it should be mentioned that the presence of third-stage larvae of Anisakis sp. in those fish used for food, as is the case of B. pectinata, needs especial attention, since this parasite form has been associated with a globally neglected zoonosis (Adroher-Auroux & Benítez-Rodríguez 2020).
Acknowledgements
Luana Benicio was supported by Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior (CAPES, Financial Code 001), Brazil. Fabiano Paschoal was supported by Programa de Apoio Técnico às Atividades de Ensino, de Pesquisa e de Extensão (PROATEC-2022). Felipe B. Pereira was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Universal 404083/2021-8).
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