Occurrence of Neoechinorhynchus curemai (Acanthocephala: Neoechinorhynchidae) in Prochilodus nigricans (Characiformes: Prochilodontidae), in southwestern Amazon

Lucena Rocha Virgilio lurunita@gmail.com

Universidade Federal do Acre, Brasil

Universidade Federal do Acre, Brasil

Fabricia da Silva Lima

Universidade Federal do Acre, Brasil

Luciano Negreiros

Instituto Federal do Acre, Brasil

Ricardo Massato Takemoto

Universidade Estadual de Maringá, Brasil

Luís Marcelo Aranha Camargo

Universidade de São Paulo, Brasil

Dionatas Ulises de Oliveira Meneguetti

Universidade Federal do Acre, Brasil

Universidade Federal do Acre, Brasil

Esta obra está bajo una Licencia Creative Commons Atribución 4.0 Internacional.

Acanthocephala endoparasites parasitize a wide diversity of terrestrial organisms and aquatic vertebrates (Galaktionov & Atrashkevich, 2015; Saini et al., 2018), in which more than half of the known species are found in wild and farmed fish (Nickol, 2006). These parasites are characterized by the presence of a proboscis with hooks used to pierce and adhere to the host’s intestinal wall (Near, Garey, & Nadler, 1998), and do not have digestive tubes, in this sense they absorb nutrients from their hosts directly from the integument (Valladão, Gallani, Jerônimo, & Seixas, 2020). The life cycle of acanthocephala is indirect and is related to their host’s food chain, including vertebrates as definitive hosts and invertebrates (Insecta, Myriapoda and Crustacea) as intermediate hosts (Martins, Moraes, Fujimoto, Onaka, & Quintana, 2001; Santos, Gibson, Tavares, & Luque, 2008; Belo et al., 2013).

Acanthocephala species of the genus Neoechinorhynchus can cause damage to their hosts, because they attach to the intestine through a spiny proboscis (Nickol, 2006) causing changes in the growth and weight gain of fish, in addition to pathologies such as acanthocephalosis (Melo, Rodrigues, Giese, Gardner, & Santos, 2014; Valladão et al., 2020). There are many reports of the effects of parasitism by Neoechinorhynchus on commercial fish, such as Colossoma macropomum (Jerônimo et al., 2017; Matos, Oliveira, Gomes, & Silva, 2017; Chagas et al., 2019), Prochilodus lineatus (Martins et al., 2001) and Plagioscion squamosissimus (Melo et al., 2014), where the authors describe significant changes, such as desquamation of the intestinal epithelium, hyperplasia, goblet cell hypertrophy and submucosal inflammatory reaction around the point of proboscis attachment. Pathogenesis of parasitic infection is based on the depth of penetration of the proboscis and the intensity of the parasite, that is, the number of parasites inside the host intestine (Taraschewski, 2000). However, when these infestations in fish are low or moderate, no damage has been reported in relation to host growth and development, where some hosts of acanthocephala are usually asymptomatic, especially when the parasites are attached only on the epithelial mucosa (Melo et al., 2014).

Neoechinorhynchus curemai Noronha, 1973 depends on ostracod species as an intermediate host and completes its life cycle in fish species, such as Prochilodus scrofa, P. lineatus Valenciennes, 1837 (Noronha, 1984; Martins et al., 2001), and Mugil curema Valenciennes, 1836 (Fortes, Mattos, & Oliveira, 2000). However, susceptible fish can get infected by eating parasitized fish or invertebrates (Lassiere & Crompton, 1988). Prochilodus fish are among the most abundant and widespread freshwater species in South American rivers (Sivasundar, Bermingham, & Ortí, 2001). In the case of Prochilodus nigricans Spix & Agassiz, 1829, popularly known as curimatã, it has migratory behavior and is extensively exploited in fishing and aquaculture in the Brazilian Amazon (Gonçalves & Batista, 2008). This fish species has low fat and high protein content with high nutritional value (Machado & Foresti, 2009). It was recorded as the definitive host of the acanthocephalan N. curemai for the first time in Amazonian lakes (Arévalo, Morey, & Malta, 2018). Nevertheless, information on the influence of the infection by this acanthocephala on this fish species is scarce, with reports on the relationship of this parasite with its host in other species of Prochilodus, such as P. lineatus (Martins et al., 2001; Belo et al., 2013).

Thus, considering the commercial importance of P. nigricans and the influence of the parasite-host relationship, where some parasites can cause damage to the host growth and development, the present study aimed to evaluate the occurrence of N. curemai in P. nigricans and the parasite-host relationship in three rivers (Juruá, Crôa and Môa) in southwestern Amazon.

The study was carried out in the municipality of Cruzeiro do Sul, state of Acre, Brazil, at a latitude of 07°37’52’’ S and longitude of 72°40’12’’ W (Figure 1). We selected three sampling sites in the Juruá River (7°40'34.1" S 72°39'39.5" W), located in an urbanized area with a high flow of boats, Crôa River (7°71'48.30" S 72°53'34.98" W), a preserved area dedicated to ecotourism, and the Môa River (7°37'18" S 72°47'47" W), a preserved area highly visited by fishermen.

Figure 1. Location of sampling sites of Prochilodus nigricans in southwestern Amazon.

Fish were caught (authorization from the Brazilian Institute of the Environment and Renewable Natural Resources 59642-2/2019) between June and September 2019, using 12 gillnets. Nets were set up in the early afternoon, remaining exposed for 24 hours. Fish were collected every four hours, in which samples were taken during the morning, afternoon, and evening. The captured individuals of P. nigricans were weighed, measured, and subjected to necropsy. The gastrointestinal tract and viscera were examined under a stereomicroscope to search for N. curemai individuals.

Collection, fixation, preservation, and preparation of parasites for identification followed the recommendations of Eiras, Takemoto, & Pavanelli (2006). Parasites were identified according to Schmidt & Hugghins (1973), and the ecological terms used were adopted from those recommended by Rohde, Hayward, & Heap (1995) and Bush, Lafferty, Lotz, & Shostak (1997).

We caught a total of 87 specimens of P. nigricans (31 in the Crôa River, 25 in the Juruá River, and 31 in the Môa River). Fish had an average weight of 72.7± 35.4 g and an average length of 15.7 ± 35.6 cm (Figure 2 and Table 1).

Figure 2. A. Neoechinorhynchus curemai, B. Neoechinorhynchus curemai when removed from the intestine, C. Anterior region with proboscis, D. Prochilodus nigricans.

Table 1. Parasitological indices for Prochilodus nigricans parasitized with Neoechinorhynchus curemai in Môa, Crôa, and Juruá rivers of the upper Juruá River, state of Acre (Brazil).

*p < 0.05.

We found a total of 178 specimens of N. curemai, with a total prevalence of (P = 58.62%); the highest parasite intensity was observed in fish from the Môa River (N = 123) and the lowest in the Juruá River (N = 10). There was a significant difference in parasite intensity in P. nigricans collected between the three rivers (Kruskal-Wallis H = 18.8; p < 0.001), in which fish from the Juruá River were significantly different for the others, by showing the lowest intensity of parasitism (Dunn’s p < 0.005). The prevalence, mean intensity, and mean abundance were higher in the Môa River and the lowest in the Juruá River. The intensity of infection ranged from one to 11 parasites per fish, with a higher infestation in specimens from the Môa and Crôa rivers (Table 1).

Regarding the length-weight relationship, the b-value did not differ statistically from three for fish species in the three rivers, nor between parasitized and non-parasitized species and the growth was considered isometric (p < 0.05) (Table 2). In the case of the relative condition factor, there was no difference between the sites (ANOVA F = 1.2; p = 0.09) or between the parasitized and non-parasitized specimens (t = 2.31; p = 0.08) in the standard value (K = 1.00).

We found no correlation between parasite intensity and condition factor (rs = -0.34, p = 0.11) and between parasite intensity and fish length (rs = -0.34; p = 0.23) in the Juruá River. The same results were observed for the Môa (Ka rs = 0.25; p = 0.25, Length rs = 0.10; p = 13) and Crôa rivers (Ka rs = 0.24; Length p = 0.44).

Table 2. Mean ± SD and range of total length and body weight parameters, length-weight relationship (LWR) and allometric condition factor for samples of Prochilodus nigricans collected in the rivers of the upper Juruá River, state of Acre Brazil.

*p < 0.001.

Neoechinorhynchus curemai occurred in more than half of the fish population in the environments and was the only endoparasite found in these fish. Previous studies have reported the occurrence of this acanthocephalan species parasitizing mainly P. lineatus (Martins et al., 2001; Lizama, Takemoto, & Pavanelli, 2006; Santos et al., 2008). Moreover, this species of endoparasite was also recorded for the first time in P. nigricans in floodplain lakes of the Solimões River (Arévalo et al., 2018), expanding the number of known hosts for this species.

The prevalence and intensity of N. curemai in P. nigricans varied between environments, where the tributaries of Crôa and Môa Rivers showed a higher prevalence, mean intensity, and mean abundance of parasites than the Juruá River. This difference may be related to the predominance of intermediate hosts, parasitized by the acanthocephalan larvae in the sampled environments. In general, ostracods are intermediate hosts for Neoechinorhynchus species (DeMont & Corkum, 1982; Lourenço et al., 2017), and since P. nigricans feeds on debris and zoobenthos (Silva & Stewart, 2017), they may have ingested ostracods and become the definitive host of this acanthocephalan species. The Juruá River shows a higher rate of environmental degradation in comparison to its tributaries, caused by deforestation, construction of urban centers, and pollution (Silva & Ribeiro, 2004). This may have influenced the decline of ostracods, resulting in a lower intensity of parasitism in the definitive host. Other studies also reported this host-parasite relationship in contaminated environments (Kussat, 1969; Overstreet & Howse, 1977; Vidal-Martinez & Wunderlich, 2017). Interference in water chemistry by pollution can limit the distribution of invertebrates that act as intermediate hosts for fish parasites, often explaining the variability in parasitism levels between different habitats (Poulin, 1992).

The infection of N. curemai in P. nigricans did not affect the health of these hosts since the length-weight relationship, both of parasitized and non-parasitized fish, showed proportional allometric growth and indicated a good condition factor. The condition factor and length-weight relationship of fish are quantitative indicators of fish health (Marinho et al., 2013; Abba, Abdulhamid, Omenesa, and Mudassir, 2018). Thus, the occurrence of acanthocephalans did not interfere with the growth and development of these individuals, which may be associated with the low intensity of these endoparasites in the fish intestine.

On the contrary to what occurs with fish species from environments changed by humans that showed an increase in the intensity of Neoechinorhynchus, these parasites negatively influenced the condition factor and length of fish (Jerônimo et al., 2017; Lourenço et al., 2018; Chagas et al., 2019). According to Malta, Gomes, Andrade, & Varella, (2001), a large infestation by Acanthocephala can occur in culture systems and negatively influence the development of hosts. These conditions can cause changes in the external morphology of fish, where parasitized individuals grow less than non-parasitized individuals. That is, these systems can induce disproportionate growth of ostracods and increase parasitic infection by acanthocephalans (Merritt & Pratt, 1964; DeMont & Corkum, 1982). On the other hand, in natural environments not disturbed by human activities, the prevalence and infection by Neoechinorhynchus occurs moderately in host species, such as N. paraguayensis Machado 1954 in Geophagus brasiliensis Quoy & Gaimard, 1824 (Nickol & Padilha, 1979), N. macronucleatus Machado Filho, 1954 in Hoplias malabaricus Bloch 1794 (Fabio, 1983), N. pimelodi in Pimelodus maculatus Lacépède, 1803 (Brasil-Sato & Pavanelli, 1999), and N. curemai in Prochilodus lineatus (Fortes et al., 2000; Ranzani-Paiva, Silva-Souza, Pavanelli, & Takemoto, 2000). Then, we can suggest that environmental changes can influence the infection of parasites in their hosts.

Thus, the present study showed that the infection by N. curemai in P. nigricans, varied among the natural environments of the Amazon, where urban sites in the Juruá River presented low prevalence and average abundance of acanthocephalans, and an increase in preserved rivers, such as Môa and Crôa Rivers, which may suggest that N. curemai may prefer more preserved environments. Nevertheless, studies relating data on the degree of environmental preservation of aquatic environments with the occurrence of the population of N. curemai are very important for future studies of biological indicators. In addition, the present study showed that when N. curemai occurs at low intensity in the intestine of fish, it does not seem to influence the growth and development of their hosts. However, further studies involving seasonality and the relationship between abiotic and biotic factors are encouraged to help understand these processes related to the parasite-host relationship of these species.

The present study showed that when N. curemai occurs at low intensity in the intestine of fish, it does not seem to influence the growth and development of their hosts. However, further studies involving seasonality and the relationship between abiotic and biotic factors are encouraged to help understand these processes related to the parasite-host relationship of these species.

We would like to thank the Animal Biology Laboratory of the Federal University of Acre- Campus Floresta, the Ichthyoparasitology Laboratory of the State University of Maringá and Capes and CnPq for financially supporting the project.