Ecology of parasites of Metynnis lippincottianus (Characiformes: Serrasalmidae) from the eastern Amazon region, Macapa, State of Amapa, Brazil/Ecologia parasitaria de Metynnis lippincottianus (Characiformes: Serrasalmidae) da regiao da Amazonia oriental, Macapa, Estado do Amapa, Brasil.
Parasites are recognized as important components of ecosystems specially when considering the dynamics of food web (MORLEY, 2012). Consequently, there has been increased research of these components in fish species of diverse ecosystems (LACERDA et al., 2012; RAKAUSKAS; BLAZEVTCTUS, 2009; ROHDE et al., 1995; TAKEMOTO et al., 2009). Parasites can use intermediary and definite hosts via trophic web, which allows them to infect the fish species, but most parasite species show a high specificity to their hosts. Thus, the knowledge of parasites infecting fish is of particular interest not only regarding the host health, but also considering the relationship between parasite and host within the aquatic environment (LACERDA et al., 2012; MORETRA et al., 2009, 2010; NEVES et al., 2013; RAKAUSKAS; BLAZEVICIUS, 2009; TAKEMOTO et al., 2009; YAMADA et al., 2012).
Parasites can cause alterations in population dynamics and behavior of their hosts. Parasites influence the competition capacity in the predator-prey relationship. They can hinder the ability to swim, influencing the mating choice, sexual behavior and corporeal health of the host fish (GOMIERO et al., 2012). This study concerns the parasite relationship of the freshwater fish, Metynnis lippincottianus Cope, 1870 (Serrasalmidae), also commonly known as pacu CD. It is native to South America and found in French Guyana and Brazil distributed through the Amazon Basin, rivers of French Guyana (JEGU, 2003), Parana river (FROESE; PAULY, 2013; MOREIRA et al., 2009; YAMADA et al., 2012) and Tocantins river (SANTOS et al., 2004). M. lippincottianus is primarily herbivore, feeding on vegetable sources, seeds and phytoplanktonic algae, but occasionally consumes arthropods and debris (FROESE; PAULY, 2013; SANTOS et al., 2004), thus occupying the second trophic level of the food chain. This pelagic fish inhabits along the shores of rivers and lakes (FROESE; PAULY, 2013; MOREIRA et al., 2010; SANTOS et al., 2004) and measures at a maximum of 20 cm in length becoming sexually mature when it reaches 10 cm in length (SANTOS et al., 2004). Commercially, it is more valuable as an ornamental fish, but it is important species in the diet of riverine populations (MOREIRA et al., 2009; YAMADA et al., 2012).
In the Parana river basin (Brazil), M. lippincottianus has been parasitized by Dadayius pacupeva, Procamallanus (Spirocamallanus) inopnatus, Contracaecum larvae, Raphidascaris mahnerti and Spinoxyuris oxydoras (MOREIRA et al., 2009; TAKEMOTO et al., 2009; MOREIRA et al., 2010; YAMADA et al., 2012). Even though this characid occurs in other hydrographic basins, such as the Amazon Basin, no study has been conducted on its parasites in the region, or any research has not been performed on the ectoparasites harbored by this fish. Therefore, this study evaluated the ecological aspects of parasites and the parasite-host relationship in M. lippincottianus of a tributary from the Amazonas river, in Northern Brazil.
Material and methods
Study area, fishes and parasite sampling
The Igarape Fortaleza basin (Figure 1), located in the county of Macapa in the State of Amapa (eastern Amazon region) is a tributary of the Amazon river and has a main canal and a floodplain.
In the period from August to December of 2011, 80 specimens of M. lippincottianus were captured in the Fortaleza Igarape basin (Figure 1), and analyzed for parasites. Fish were captured using nets with a 20-25 mm web (License ICMBio: 23276-1) placed into isothermal box with ice and taken to the Sanity Laboratory of Aquatic Organisms from Embrapa Amapa for parasitological analyses.
It exhibits unique characteristics: it is strongly influenced by the high pluviosity rates of the Amazon region and the diary strong tides of the Amazon delta (TAKYAMA et al., 2004), which create an ideal environment for fish inhabiting and feeding.
Collection and analysis of parasites
The captured fish where weighed (g) and measured for total length (cm). Each specimen was analyzed macroscopically and the observations were taken of the body surface, mouth, eyes, operculum, and gills. The gills were removed for ectoparasites collection while the gastro-intestinal tract was removed and examined for endoparasites collection. The parasites were collected, fixed, counted and stained using the method of Eiras et al. (2006). The ecological terms adopted follow the previous recommendations of Rohde et al. (1995) and Bush et al. (1997).
The index of Brillouin (HB), species richness, evenness index (E) and Berger-Parker dominance (d) were calculated for each infracommunity of parasites using the software Diversity (Pisces Conservation Ltda, UK). The index of dispersion (ID) and the index of discrepancy (D) were calculated using the software Quantitative Parasitology 3.0. All calculations were used to detect the distribution pattern of the infracommunities of parasites (ROZSA et al., 2000) for species with prevalence >10%. ID significance was tested using the statistic d according to (LUDWIG; REYNOLDS, 1988) for each infracommunity.
The Pearson coefficient (r) was employed to test the relationship of total host length with prevalence of parasite infection and compared with previous studies on angular transformation of prevalence data (sine-arc [square root of x]), after which the samples of hosts were separated into five length classes. The Pearson coefficient of correlation (r) was employed to investigate a possible correlation of HB between the prevalence of parasite infestation and the host length of in the sample collection (ZAR, 2010).
Body weight data (g) and total length (cm) were used for calculating the relative condition factor (Kn) of the sampled fish (LE-CREN, 1951), and then compared with the norm (Kn = 1.0) using the t-test. The Pearson coefficient (r) was also used to determine possible correlations in the abundance of parasites versus fish length, body weight, and Kn of the hosts (ZAR, 2010).
During three fish collections the pH (6.6 [+ or -] 0.2), temperature (31.0 [+ or -] 0.3[degrees]C) and dissolved oxygen levels (2.0 [+ or -] 0.4 mg [L.sup.-1]) were determined by using digital device for each purpose.
80 specimens of M. lippincottianus with a total length of 7.1 [+ or -] 0.8 cm and weight of 12.1 [+ or -] 3.6 g were collected, 98.7% of the samples collected were infected with one or more species of parasites. Parasites were identified as Ichthyophthirius multifiliis Fouquet, 1876 (Ciliophora); Anacanthorus jegui Van Every and Kritsky, 1992 (Dactylogyridae); Dadayius pacupeva Lacerda et al. 2003 (Cladorchiidae), encapsulated metacercariae of Digenea gen. sp.; Procamallanus (Spirocamallanus) inopinatus Travassos et al. 1928, Procamallanus (Spirocamallanus) sp. (Camallanidae); Spinoxyuris oxydoras Petter, 1994 (Pharyngodonidae); Contracaecum Railliet & Henry, 1912 (Anisakidae), Dolops longicauda Heller, 1857 (Argulidae) and Glossiphoniidae gen. sp. (Hirudinea). Ichthyophthirius multifiliis was the dominant species, while nematode species were the most prevalent endoparasites (Table 1).
The mean richness of species was 4.9 [+ or -] 1.3 per host, with predominance of parasites in parasitized individuals from 4 to 6 species (Figure 2). The mean diversity (HB) was 0.96 [+ or -] 0.32), evenness (E) index was 0.48 [+ or -] 0.15 and dominance (d) index was 0.55 [+ or -] 0.18. The HB did not show a significant correlation (r = 0.17, p = 0.12) between parasite prevalence and total length of hosts.
Most of parasites species in M. lippincottianus showed aggregate distribution pattern, which is typical of parasites of freshwater fish. However, I. multifiliis and P. (S.) inopinatus showed a higher index of discrepancy (Table 2) indicating a greater level of parasitic aggregation
The relative condition factor (Kn) for M. lippincottianus (Kn = 1.000 [+ or -] 0.092, t = 0.023, p = 0.982) did not vary from the standard values of Kn, which indicates that the parasite infection did not harm the host's body condition. The prevalence of parasite infection showed negative correlation (r = -0.701, p = <0.0001) with the length of host indicating the higher prevalence of parasites in smaller hosts. However, there was a positive correlation in the abundance of I. multifiliis and S. oxydoras when weight and Kn of the fish were compared, as well as the abundance of D. pacupeva with Kn relative condition factor. In contrast, the abundance of Contracaecum sp. larvae showed a negative correlation when compared with the length of the hosts (Table 3).
Specimens of M. lippincottianus captured during the dry season in the Amazon showed the highest diversity of parasites (HB = 0.962 [+ or -] 0.32). Parasite samples were composed of one Protozoa, one Monogenoidea, two Digenea, four Nematoda, one Crustacea, and one Hirudinea. Ichthyophthirius multifiliis, A. jegui, D. pacupeva, metacercariae of Digenea, P. (S.) inopinatus, Procamallauns (S.) sp., S. oxydoras and Contracaecum larvae showed a distribution pattern of aggregation. Aggregate dispersion for D. pacupeva, S. oxydoras, P. (S.) inopinatus, Contracaecum sp. and Raphidascaris (Sprentascaris) mahnerti infesting M. lippincottianus in the upper Parana river basin was also reported, where D. pacupeva and S. oxydoras were the dominant parasites with HB = 0.337 (MOREIRA et al., 2009). Such a distribution pattern could be related to a parasite strategy for survival, genetic and immunity heterogeneity of the hosts, environmental conditions (KNUDSEN et al., 2004; MOREIRA et al., 2009; NEVES et al., 2013) and the host's survival mechanism (KNUDSEN et al., 2004; NEVES et al., 2013).
Out of the parasites reported for M. lippincottianus from the Parana river basin that were captured in different seasons of the year (MOREIRA et al., 2009, 2010; YAMADA et al., 2012), only R. (S.) mahnerti was not found in the present study. On the other hand, ectoparasites were not found in the gills (I. multifiliis, A. jegui, metacercariae of digeneas, D. longicauda and hirudineas), which were not studied for this host from the Parana river basin. Diferences in richness and diversity of parasites for a host that inhabits different geographic regions could be associated with its ecology (size, age, heterogeneity of diet, and behavior), as well as the environmental factors, in particular, the physical and chemical parameters, the presence of intermediary hosts in the location, and seasonal differences (LACERDA et al., 2012; MOREIRA et al., 2009; NEVES et al., 2013; RAKAUSKAS; BLAZEVICIUS, 2009; SILVA et al., 2011; YAMADA et al., 2012), besides host density.
Ichthyophthirius multifiliis is a dominant parasite species infecting the pelagic fish, M. lippincottianus that showed higher levels of infection than those reported for the bentonic fish, Oxydoras niger of the Solimoes river (SILVA et al., 2011). This ciliate fish parasite is common in natural habitats as well as in farmed fish (RAISSY et al., 2010; RAKAUSKAS; BLAZEVICIUS, 2009; WURTSBAUGH; TAPIA, 1998). However, the infection is higher in fish raised in tanks. This is due to horizontal transmission of this parasite, which causes lesions on the gills and cutaneous surfaces, thus hindering respiration of the host and facilitating the entrance of bacteria (RAISSY et al., 2010). However, epizooty caused by I. multifiliis also occurs in natural populations (RAISSY et al., 2010; WURTSBAUGH; TAPIA, 1998), but this occurrence has not been documented in wild fish in Brazil.
On the gills of M. lippincottianus captured along the tributaries of the Amazon river in the State of Amapa, high levels of infection by A. jegui were found. This is a species of monogenoidean originally described parasitizing another characid that inhabits the Amazonas River tributaries, S. rhombeus (VAN EVERY; KRITSKY, 1992). Monogenoideans are parasites with high specifity when compared with other taxa of helminths (SILVA et al., 2011; TAKEMOTO et al., 2009). For M. lippincottianus captured in any other location there is no record of A. jegui. Therefore, this is the first record of A. jegui for this host, in addition it has expanded its presence for the eastern Amazon region.
Leeches species of Glossiphoniidae family were observed on the gills of M. lippincottianus in low levels of infection, which is similar to the results described for R. rutilus from different ecosystems (RAKAUSKAS; BLAZEVICIUS, 2009). Glossiphoniidae are common parasites infecting freshwater fish worldwide, but they can occur in high density in some species of hosts (SKET; TRONTELJ, 2008). However, among freshwater fish inhabiting the Brazilian rivers and lakes, the species of the genera Helobdella and Mymyzobdella have been more common (TAKEMOTO et al., 2009).
Dolops longicauda occurred in low levels of infection on the gills of M. lippincottianus. This argulid is distributed in fish throughout Uruguay, Argentina, and Brazil (States of Mato Grosso, Sao Paulo, Parana, Rio Grande do Sul, and Amazonas) (MALTA, 1998). However, this study is the first one to relate the occurrence of D. longicauda in M. lippincottianus, and also expand the occurrence of this parasite species for the eastern Amazon region.
In M. lippincottianus of the eastern Amazon, low levels of infection by Digenea metacercarie were observed on the gills, and D. pacupeva metacercarie were collected in the intestine. However, these levels of infection by D. pacupeva were lesser than those described for this same host from the Parana River basin (MOREIRA et al., 2009; YAMADA et al., 2012), which was probably due to a lower ingestion of the infective stages of this digenean. Differences in the abundance of D. pacupeva in M. lippincottianus were also reported by Moreira et al. (2009). Yamada et al. (2012) mentioned that ontogenetic alterations in the diet or habitat will make M. lippincottianus more susceptible to infections by D. pacupeva, a parasite that accumulates in the intestine. The species within Trematoda needs mollusks as first intermediate hosts (MOREIRA et al., 2009; MORLEY, 2012), and fish such as M. lippincottianus are the definite host of D. pacupeva. Although the main role of cercariae of these parasites, which are components of zooplankton (meroplankton), being to find and infect the target host; secondarily, they play an important role in the trophic web of aquatic environments. When they migrate in the water column searching for target hosts, they also become a food source for fish (MORLEY, 2012), including M. lippincottianus, a pelagic host, which showed high level of infection by D. pacupeva.
Metynnis lippincottianus is a omnivorous fish that feeds on aquatic plants, phytoplanktonic algae, and at times will eat microcrustaceans, and detritus (FROESE; PAULY, 2013; SANTOS et al., 2004), but along the Igarape Fortaleza basin it was found that this fish is a frequent predator of microcrustaceans and other invertebrates. Consequently, it became infected by four species of nematodes: P. (S.) inopinatus, Procamallauns (S.) sp., S. oxydoras and Contracaecum sp. S. oxydoras was the predominant nematode; similar to that described for this same host from Parana river basin (MOREIRA et al., 2009; YAMADA et al., 2012). On the other hand, the hosts of the present study showed higher levels of P. (S.) inopinatus, Procamallauns (S.) inopinatus and Contracaecum larvae, which have low parasitic specificity (MORAVEC, 1998; MOREIRA et al., 2009). Chironomids are intermediate hosts of P. (S.) inopinatus while microcrustaceans are intermediate hosts of Contracaecum sp. (MOREIRA et al., 2009). Even though S. oxydoras is a nematode with a direct life cycle, it uses Oxydoras kneri (MORAVEC, 1998) and M. lippincottianus to reach its adult stage.
The Kn values of M. lippincottianus indicated that the body condition of the hosts was not affected by high infection of ectoparasites and endoparasites. The abundance of I. multifiliis, D. pacupeva and S. oxydoras was higher in fish with better relative conditions. Similarly, for M. lippincottianus from Parana River basin was reported that the largest fish were infected by D. pacupeva and S. oxydoras and showed higher Kn values (MOREIRA et al., 2010). Larger hosts support a higher degree of infection by these parasites because such parasites are not pathogenic and cause little harm to their host. On the other hand, more pathogenic and abundant parasites may reduce the condition factor of hosts (LACERDA et al., 2012). This is because they have minor chance of reacting to the infections when their immunological system does not aptly respond to the parasite infection.
The total length (5.0-10.0 cm) of M. lippincottianus (juveniles and sub-adults), which may be an expression of their age, showed negative correlation with abundance of Contracaecum larvae and Kn, indicating that larger and older individuals ingested a smaller quantity of food containing infective stages of these nematodes. Only host body weight showed a positive correlation with abundance of I. multifiliis and S. oxydoras, which indicates that larger-sized hosts accumulate higher quantities of these parasites. For this same host in the Parana river basin, positive correlation was found between total length and abundance of Contracaecum sp., D. pacupeva and S. oxydoras (YAMADA et al., 2012), whose fish examined had from 1.4-13.4 cm in total length and were at all stages of its life cycle (fingerlings, juveniles, and adults). However, such discrepancies may have been caused by differences in ecosystems and variations in size (age) of the hosts that were examined in both studies.
Metynis lippincottianus, a pelagic fish, showed diversity of ectoparasites and endoparasites. If one considers that this freshwater fish spends a greater part of its life cycle in areas with vegetation, it may be feeding on microcrustaceans and possibly, on cercariae of D. pacupeva and ostracods mollusks, which are constant items of their diet. Due to low parasites diversity, the HB was not correlated with the length of the hosts, which indicates little ontogenic variation in the diet of this host in its juvenile and sub-adult stages. Our results indicated that juveniles and sub-adults M. lippincottianus are omnivore fish during these phases of its life cycle. This study records the first occurrence of I. multifiliis in M. lippincottianus, and expands the occurrence of D. pacupeva and S. oxydoras for the Amazon region.
Received on January 21, 2013.
Accepted on August 21, 2013.
This study was undertaken in accordance with the principles adopted by the Brazilian College for Animal Experimentation (Cobea). Marcos Tavares-Dias was supported by a Research fellowship from Conselho Nacional de Pesquisa e Desenvolvimento Tecnologico (CNPq), Brazil.
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Maria Danielle Figueiredo Guimaraes Hoshino (1) and Marcos Tavares-Dias (1,2) *
(1) Programa de Pos-graduacao em Biodiversidade Tropical, Universidade Federal do Amapa, Macapa Amapa, Brazil. (2) Laboratorio de Aquicultura e Pesca, Embrapa Amapa, Rod. Juscelino Kubitschek, km 5, 2600, 68903-419, Macapa, Amapa, Brazil. * Author for correspondence. E-mail: firstname.lastname@example.org
Table 1. Parasites of M. lippincottianus (n = 80) from the Igarape Fortaleza basin, eastern Amazon, Brazil. MI: Mean intensity, MA: Mean abundance, TNP: Total Number of Parasites, SD: Standard deviation, RD: Relative dominance SI: Site of infection. Parasites Prevalence MI [+ or -] SD (Range) (%) Ectoparasites Ichthyophthirius 45.0 132.5 [+ or -] 157.2 (6-1133) multifiliis Dolops longicauda 1.2 1.0 [+ or -] 0.1 Anacanthorus jegui 95.0 19.1 [+ or -] 21.7 (1-138) Digenea gen. sp. 77.5 11.1 [+ or -] 10.2 (1-60) (metacercariae) Hirudinea gen. sp. 6.2 1.00 [+ or -] 0.2 Endoparasites Dadayius pacupeva 82.5 11.0 [+ or -] 14.6 (1-77) (adults) Dadayius pacupeva 22.5 9.3 [+ or -] 7.5 (2-60) (metacercariae) Procamallanus 36.2 6.1 [+ or -] 5.0 (1-32) (Spirocamallanus) inopinatus Procamallanus 8.7 1.6 [+ or -] 0.5 (1-4) (Spirocamallanus) sp. Spinoxyuris oxydoras 65.0 12.5[+ or -] 17.9 (1-95) Contracaecum sp. 68.7 2.3 [+ or -] 2.2 (1-15) (larvae) Parasites MA TNP RD SI Ectoparasites Ichthyophthirius 59.6 4.770 0.5437 Gills multifiliis Dolops longicauda 0.01 1 0.0001 Gills Anacanthorus jegui 18.1 1.450 0.1653 Gills Digenea gen. sp. 8.6 686 0.0782 Gills (metacercariae) Hirudinea gen. sp. 0.06 5 0.0006 Gills Endoparasites Dadayius pacupeva 9.1 727 0.0829 Intestine (adults) Dadayius pacupeva 2.1 168 0.0191 Intestine (metacercariae) Procamallanus 2.2 176 0.0201 Intestine (Spirocamallanus) inopinatus Procamallanus 0.1 11 0.0013 Intestine (Spirocamallanus) sp. Spinoxyuris oxydoras 8.1 652 0.0743 Intestine Contracaecum sp. 1.6 128 0.0146 Intestine (larvae) Table 2. Dispersion Index (ID), discrepancy Index (D) and statistic d for the parasites infracommunities of Metynnis lippincottianus from the Igarape Fortaleza basin, eastern Amazon, Brazil. Parasites ID d D Ichthyophthirius multifiliis 6.294 19.01 0.705 Anacanthorus jegui 4.218 13.28 0.374 Digenea gen. sp. (metacercariae) 4.761 14.89 0.478 Procamallanus (S.) inopinatus 4.278 13.46 0.764 Spinoxyuris oxydoras 4.573 14.34 0.590 Contracaecum sp. (larvae) 1.682 3.77 0.537 Dadayius pacupeva 4.283 13.48 0.486 Table 3. Pearson coefficient (r) of correlation for parasite abundance compared with total length (cm), body weight (g), and relative condition factor (Kn) for Metynnis lippincottianus of the Igarape Fortaleza basin, eastern Amazon, Brazil. Length (cm) Weight: (g) Parasites r p r p Ichthyophthirius mukfdiis 0.063 0.580 0.250 0.025 Anacanthorus jegui -0.063 0.559 -0.116 0.304 Digenea gen. sp. (metacercariae) -0.066 0.559 -0.080 0.479 Procamallanus (S.) inopinatus -0.159 0.158 -0.055 0.628 Spinoxyuris oxydoras -0.006 0.957 0.249 0.026 Contracaecum sp. (larvae) -0.253 0.023 -0.132 0.240 Dadayius pacupeva 0.007 0.947 0.169 0.132 Kn r p Parasites 0.253 0.023 Ichthyophthirius mukfdiis -0.078 0.493 Anacanthorus jegui -0.097 0.389 Digenea gen. sp. (metacercariae) 0.110 0.332 Procamallanus (S.) inopinatus 0.327 0.003 Spinoxyuris oxydoras 0.073 0.518 Contracaecum sp. (larvae) 0.230 0.040 Dadayius pacupeva Figure 2. Species richness in parasites infracommunity of M. lippinconttianus from the Igarape Fortaleza basin, eastern Amazon, Brazil. 0 1 1 0 2 2 3 5 4 25 5 17 6 24 7 5 8 1 9 0 10 0 Species richness Note: Table made from bar graph.