Acessibilidade / Reportar erro

Ecology and diversity of metazoan parasites infecting Geophagus altifrons (Cichliformes: Cichlidae) from the Amazon River system in northern Brazil

Ecologia e diversidade de parasitos metazoários infectando Geophagus altifrons (Cichliformes: Cichlidae) do sistema do Rio Amazonas no norte do Brasil

Abstract

The aim of this study was to investigate the ecology and diversity of community and infracommunities of metazoan parasites Geophagus altifrons (Heckel, 1840) in Rio Jari, in the state of Amapá, in the eastern Amazon region. From the total of 31 fish examined, 90.3% were parasitized by one or more species, collecting a total number of 806 parasites. The parasites species identified were: Sciadicleithrum geophagi, Posthodiplostomum sp., Procamallanus (Spirocamallanus) inopinatus, Raphidascaris (Sprentacaris) sp., Genarchella genarchella, Gorytocephalus spectabilis and Ergasilus xinguensis. Most of the parasites showed an aggregate dispersion pattern. Brillouin diversity index, uniformity and species richness of parasites were low. The component community of parasites was constituted by ectoparasites and endoparasites, but with a predominance of ectoparasites. The body size of hosts had a low effect on the parasites infracommunities. This first eco-epidemiological study for G. altifrons reports these parasites in a host, for the first time, with the exception of S. geophagi and E. xinguensis.

Keywords:
Freshwater fish; aggregation; helminth; infection

Resumo

O objetivo deste estudo foi investigar a ecologia e a diversidade da comunidade e infracomunidades de parasitos metazoários em Geophagus altifrons (Heckel, 1840), do Rio Jari, estado do Amapá, na região da Amazônia oriental. De um total de 31 peixes examinados, 90,3% estavam parasitados por uma ou mais espécies e 806 parasitos foram coletados. As espécies de parasitos identificadas foram: Sciadicleithrum geophagi, Posthodiplostomum sp., Procamallanus (Spirocamallanus) inopinatus, Raphidascaris (Sprentacaris) sp., Genarchella genarchella, Gorytocephalus spectabilis e Ergasilus xinguensis. A maioria dos parasitos apresentaram dispersão agregada. Foi baixo o índice de diversidade de Brillouin, uniformidade e riqueza de espécies de parasitos. A comunidade componente de parasitos foi constituída por ectoparasitos e endoparasitos, mas com predominância de ectoparasitos. O tamanho corporal dos hospedeiros teve baixo efeito sobre as infracomunidades dos parasitos. Este primeiro estudo ecoepidemiológico para G. altifrons registra pela primeira vez estes parasitos para este hospedeiro, exceto S. geophagi e E. xinguensis.

Palavras-chave:
Peixe de água doce; agregação; helminto; infecção

Introduction

Species of Cichlidae are fish with innumerous species distributed particularly in fresh and brackish waters from the Central and South America and Africa; however, some species were introduced in other regions. Geophagus altifrons (Heckel, 1840), an ornamental cichlid from the Amazon River basin in Brazil with sedentary habits, is a benthopelagic and omnivorous fish that feeds on large-bodied benthonic organisms, terrestrial and aquatic insects, crustaceans and fish, algae, detritus, macrophytes, fruits and seeds, depending on the seasonal period. This fish that inhabits lakes and rivers have a maximum length of 27 cm, and its first maturation occurs with 15-17 cm (Soares et al., 2011Soares MGM, Costa EL, Siqueira-Souza FK, Anjos HDB, Yamamoto KC, Freitas CEC. Peixes de lagos do médio Rio Solimões. Manaus: Reggo Edições; 2011.; Hawlitschek et al., 2013Hawlitschek O, Yamamoto KC, Carvalho-Neto FGMR. Diet composition of fish assemblage of lake Tupé, Amazonas, Brazil. Rev Colombiana Cienc Anim 2013; 5(2): 313-326. http://dx.doi.org/10.24188/recia.v5.n2.2013.296.
http://dx.doi.org/10.24188/recia.v5.n2.2...
; Camargo et al., 2015Camargo M, Giarrizzo T, Isaac VJ. Population and biological parameters of selected fish species from the middle Xingu River, Amazon basin. Braz J Biol 2015;75(3 Suppl 1): 112-124. http://dx.doi.org/10.1590/1519-6984.01914BM. PMid:26691084.
http://dx.doi.org/10.1590/1519-6984.0191...
; Dary et al., 2017Dary EP, Ferreira E, Zuanon J, Röpke CP. Diet and trophic structure of the fish assemblage in the mid-course of the Teles Pires River, Tapajós River basin, Brazil. Neotrop Ichthyol 2017; 15(4): e160173. http://dx.doi.org/10.1590/1982-0224-20160173.
http://dx.doi.org/10.1590/1982-0224-2016...
; Froese & Pauly, 2021Froese R, Pauly D. FishBase. Version (8/2021) [online]. USA: FishBase; 2021 [cited 2021 Oct 15]. Available from: www.fishbase.org
www.fishbase.org...
).

For G. altifrons, Ergasilus xinguensis (Taborda, Paschoal & Luque, 2016Taborda NL, Paschoal F, Luque LJ. A new species of Ergasilus (Copepoda: Ergasilidae) from Geophagus altifrons and G. argyrostictus (Perciformes: Cichlidae) in the Brazilian Amazon. Acta Parasitol 2016; 61(3): 549-555. http://dx.doi.org/10.1515/ap-2016-0073. PMid:27447219.
http://dx.doi.org/10.1515/ap-2016-0073...
) and Sciadicleithrum geophagi (Kritsky, Thatcher & Boeger, 1989) (Paschoal et al., 2016Paschoal F, Scholz T, Tavares-Dias M, Luque JL. Dactylogyrids (Monogenea) parasitic on cichlids from northern Brazil, with description of two new species of Sciadicleithrum and new host and geographical records. Acta Parasitol 2016; 61(1): 158-164. http://dx.doi.org/10.1515/ap-2016-0021. PMid:26751887.
http://dx.doi.org/10.1515/ap-2016-0021...
), are the only two species that have been described, due to the paucity of studies carried out. Despite their economic importance in the Amazon, studies focusing on the parasite fauna of G. altifrons have been not performed; hence, the ecology and diversity of parasites remain unknown. This species is not on the Red List of Threatened Species. Therefore, further studies on the ecology and diversity of the parasite in wild G. altifrons populations are need.

In wild fish populations, communities and infracommunities of parasites are the result of repeated additions and losses of parasite species during evolutionary history. Developing over time, the ecological and biological characteristics of hosts and parasites determine host colonization, consequently influencing parasite community richness and diversity (Poulin, 2004Poulin R. Parasite species richness in New Zealand fishes: a grossly underestimated component of biodiversity? Divers Distrib 2004; 10(1): 31-37. http://dx.doi.org/10.1111/j.1472-4642.2004.00053.x.
http://dx.doi.org/10.1111/j.1472-4642.20...
; Hoshino et al., 2014Hoshino MDFG, Hoshino EM, Tavares-Dias M. First study on parasites of Hemibrycon surinamensis (Characidae), a host from the eastern Amazon region. Rev Bras Parasitol Vet 2014; 23(3): 343-347. http://dx.doi.org/10.1590/S1984-29612014069. PMid:25271454.
http://dx.doi.org/10.1590/S1984-29612014...
; Oliveira et al., 2017Oliveira MSB, Corrêa LL, Castro LA, Brito LS, Tavares-Dias M. Metazoan parasites of Geophagus proximus, a Cichlidae fish from the eastern Amazon (Brazil). Nat Resour 2017; 8(3): 268-277. http://dx.doi.org/10.4236/nr.2017.83015.
http://dx.doi.org/10.4236/nr.2017.83015...
; Tavares-Dias et al., 2017aTavares-Dias M, Oliveira MSB, Gonçalves RA, Neves LR. Parasitic diversity of a wild Satanoperca jurupari population, an ornamental cichlid in the Brazilian Amazon. Acta Amazon 2017a; 47(2): 155-162. http://dx.doi.org/10.1590/1809-4392201602514.
http://dx.doi.org/10.1590/1809-439220160...
, bTavares-Dias M, Gonçalves RA, Oliveira MSB, Neves LR. Ecological aspects of the parasites in Cichlasoma bimaculatum (Cichlidae), ornamental fish from the Brazilian Amazon. Acta Biol Colomb 2017b; 22(2): 53. http://dx.doi.org/10.15446/abc.v22n2.60015.
http://dx.doi.org/10.15446/abc.v22n2.600...
). The study of the factors influencing host-parasite interactions in wild fish populations has been gaining the interest of ecologists and parasitologists, resulting in an increase in the number of studies on this subject in the last decades.

Host age, size, diet, habitat, behavior, distribution and geographical range have been recognized as some of the factors influencing richness and diversity of parasite communities in wild fish populations (Poulin, 2004Poulin R. Parasite species richness in New Zealand fishes: a grossly underestimated component of biodiversity? Divers Distrib 2004; 10(1): 31-37. http://dx.doi.org/10.1111/j.1472-4642.2004.00053.x.
http://dx.doi.org/10.1111/j.1472-4642.20...
; Lagrue et al., 2011Lagrue C, Kelly DW, Hicks A, Poulin R. Factors influencing infection patterns of trophically transmitted parasites among a fish community: host diet, host-parasite compatibility or both? J Fish Biol 2011; 79(2): 466-485. https://doi.org/10.1111/j.1095-8649.2011.03041.x.
https://doi.org/10.1111/j.1095-8649.2011...
; Hoshino et al., 2014Hoshino MDFG, Hoshino EM, Tavares-Dias M. First study on parasites of Hemibrycon surinamensis (Characidae), a host from the eastern Amazon region. Rev Bras Parasitol Vet 2014; 23(3): 343-347. http://dx.doi.org/10.1590/S1984-29612014069. PMid:25271454.
http://dx.doi.org/10.1590/S1984-29612014...
; Oliveira et al., 2017Oliveira MSB, Corrêa LL, Castro LA, Brito LS, Tavares-Dias M. Metazoan parasites of Geophagus proximus, a Cichlidae fish from the eastern Amazon (Brazil). Nat Resour 2017; 8(3): 268-277. http://dx.doi.org/10.4236/nr.2017.83015.
http://dx.doi.org/10.4236/nr.2017.83015...
; Tavares-Dias et al., 2017 a, bTavares-Dias M, Gonçalves RA, Oliveira MSB, Neves LR. Ecological aspects of the parasites in Cichlasoma bimaculatum (Cichlidae), ornamental fish from the Brazilian Amazon. Acta Biol Colomb 2017b; 22(2): 53. http://dx.doi.org/10.15446/abc.v22n2.60015.
http://dx.doi.org/10.15446/abc.v22n2.600...
; Pelegrini et al., 2021Pelegrini LS, Vieira DHM, Leite LAR, Gião T, Azevedo RK, Abdallah VD. Parasite diversity of Hoplosternum littorale from the Tietê-Batalha River basin, southeastern Brazil. Bol Inst Pesca 2021; 47: e650. http://dx.doi.org/10.20950/1678-2305/bip.2021.47.e650.
http://dx.doi.org/10.20950/1678-2305/bip...
). Therefore, since the factors controlling infection levels, richness and diversity of parasite communities are diverse and can likely can vary spatially in wild fish populations, such factors need to be analyzed for different fish species, including G. altifrons. The aim of this study was to investigate the ecology and diversity of community and infracommunities of metazoan parasites in G. altifrons of a tributary from the Amazon River system in northern Brazil.

Material and Methods

Sampling area and fish collection

Thirty-one specimens of G. altifrons (16.9 ± 2.7 cm and 108.6 ± 49.9 g) were collected in the Jari River basin, Jarilândia community, in the municipality of Vitória do Jari, Amapá state, Brazil (Figure 1), for parasitological analysis. Fish were captured using gill nets with 20 to 40 mm mesh.

Figure 1
Collection site of Geophagus altifrons in Jari River, State of Amapá, northern Brazil.

The present study was carried out according to the recommendations and guidelines of the Brazilian College of Animal Experimentation (COBEA) and with authorization from the Ethics Committee on the Use of Animals of Embrapa Amapá (Protocol No 014 - CEUA/CPAFAP).

Parasite collection and analysis procedures

Fish were weighed (g) and measured in total length (cm) and then necropsied for parasitological analysis. The mouth, operculum, gills, viscera and gastrointestinal tract were examined in each fish to collection of ectoparasites and endoparasites, using a stereomicroscope. The collection, fixation, conservation, counting and preparation of the parasites for identification followed the recommendations of Eiras et al. (2006)Eiras JC, Takemoto RM, Pavanelli GC. Métodos de estudos e técnicas laboratóriais em parasitologia de peixes. Maringá: Eduem; 2006.. Parasites were identified according to Moravec (1998)Moravec F. Nematodes of freshwater fishes of the Neotropical region. Prague: Academia; 1998. and Thatcher (2006)Thatcher VE. Amazon fish parasites. Sofia: Pensoft Publishers; 2006. and also in specialized papers

The ecological terms used were those recommended by Bush et al. (1997)Bush AO, Lafferty KD, Lotz JM, Shostak W. Parasitology meets ecology on its own terms: margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
http://dx.doi.org/10.2307/3284227...
. Brillouin diversity index (HB), evenness (E) and species richness (Magurran, 2004Magurran A. Measuring biological diversity. Oxford: Blackwell Publishing; 2004.) and dominance frequency (Rohde et al., 1995Rohde K, Hayward C, Heap M. Aspects of the ecology of metazoan ectoparasites of marine fishes. Int J Parasitol 1995; 25(8): 945-970. https://doi.org/10.1016/0020-7519(95)00015-T.
https://doi.org/10.1016/0020-7519(95)000...
) were calculated to evaluate the community component of parasites using Diversity software (Pisces Conservation Ltd, UK). The dispersion index (ID) and discrepancy index (D) were calculated using the Quantitative Parasitology 3.0 software to detect the distribution pattern of parasite infracommunities (Rózsa et al., 2000Rózsa L, Reiczigel J, Majoros G. Quantifying parasites in samples of hosts. J Parasitol 2000; 86(2): 228-232. http://dx.doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2. PMid:10780537.
http://dx.doi.org/10.1645/0022-3395(2000...
) for species with a prevalence >10%. The significance of the ID was calculated using the d-statistic with Quantitative Parasitology 3.0 software, as well as the Poulin discrepancy index (D) (Ludwig et al., 1988Ludwig JA, Quartet L, Reynolds JF, Reynolds JS. Statistical ecology: a primer in methods and computing. New York: John Wiley & Sons; 1988.). Spearman's correlation coefficient (rs) was used to investigate possible correlations of body length and weight of host with the richness of parasite species, Brillouin diversity index and parasite abundance (Zar, 2010Zar JH. Biostatistical analysis. New Jersey: Prentice-Hall; 2010.).

Results

In G. altifrons, a total of 806 parasites were collected such as S. geophagi, Posthodiplostomum sp., Procamallanus (Spirocamallanus) inopinatus (Travassos, Artigas & Pereira, 1928), Raphidascaris (Sprentacaris) sp., Genarchella genarchella (Travassos, Artigas & Pereira, 1928), Gorytocephalus spectabilis (Machado-Filho, 1956) and E. xinguensis (Table 1).

Table 1
Metazoan parasites in Geophagus altifrons from the Amazon River system in northern Brazil.

Parasites showed an aggregate dispersion, except G. genarchella and G. spectabilis that showed a random dispersion (Table 2). From the total of 31 examined fish, prevalence of 90.3% was recorded, and the Brillouin diversity index showed that evenness and species richness were low (Table 3).

Table 2
Index of dispersion (ID), d-statistical (d) and discrepancy index (D) of parasite infracommunities in Geophagus altifrons from the Amazon River system in northern Brazil.
Table 3
Component community of metazoan parasites in in Geophagus altifrons from the Amazon River system in northern Brazil.

There was a predominance of parasites infected by 2 to 4 species (Figure 2).

Figure 2
Species richness of metazoan parasites in Geophagus altifrons from the Amazon River system in northern Brazil.

There was no significant correlation of the Brillouin diversity index (rs = 0.19, p = 0.29) and species richness (rs = 0.18, p= 0.31) with the length of hosts.

The abundance of S. geophagi (rs = 0.34, p = 0.06), abundance of Posthodiplostomum sp. (rs =0.08, p = 0.65), abundance of Raphidascaris (Sprentacaris) sp. (rs = 0.17, p = 0.36), abundance of G. spectabilis (rs = -0.03, p= 0.85) and abundance of G. genarchella (rs = -0.006, p = 0.97) showed no correlation with host length. The abundance of E. xinguensis (rs = 0.38, p = 0.03) presented a week positive correlation with the length of hosts, as well as the abundance of P. (S.) inopinatus (rs = 0.52, p = 0.002). The abundance of G. spectabilis (rs = -0.07, p= 0.70), abundance of S. geophagi (rs = 0.27, p = 0.15), abundance of Posthodiplostomum sp. (rs = 0.12, p = 0.53) and abundance of Raphidascaris (Sprentacaris) sp. (rs = 0.17, p = 0.37) showed no correlation with the host weight. The abundance of E. xinguensis (rs = 0.43, p = 0.01) and P. (S.) inopinatus (rs = 0.51, p= 0.003) presented a week positive correlation with the host weight.

Discussion

Wild fish populations act as hosts for various taxa of parasites with varied life cycle strategies. Hence, the diversity and richness of parasite species depends on the host species and other factors related to the host and environment such as parasite life cycle, feeding habits and the reproductive stage of the host fish. Furthermore, they depend on the presence of intermediate hosts in the environment (Tavares-Dias et al., 2017aTavares-Dias M, Oliveira MSB, Gonçalves RA, Neves LR. Parasitic diversity of a wild Satanoperca jurupari population, an ornamental cichlid in the Brazilian Amazon. Acta Amazon 2017a; 47(2): 155-162. http://dx.doi.org/10.1590/1809-4392201602514.
http://dx.doi.org/10.1590/1809-439220160...
, bTavares-Dias M, Gonçalves RA, Oliveira MSB, Neves LR. Ecological aspects of the parasites in Cichlasoma bimaculatum (Cichlidae), ornamental fish from the Brazilian Amazon. Acta Biol Colomb 2017b; 22(2): 53. http://dx.doi.org/10.15446/abc.v22n2.60015.
http://dx.doi.org/10.15446/abc.v22n2.600...
; Hoshino et al., 2014Hoshino MDFG, Hoshino EM, Tavares-Dias M. First study on parasites of Hemibrycon surinamensis (Characidae), a host from the eastern Amazon region. Rev Bras Parasitol Vet 2014; 23(3): 343-347. http://dx.doi.org/10.1590/S1984-29612014069. PMid:25271454.
http://dx.doi.org/10.1590/S1984-29612014...
; Pelegrini et al., 2021Pelegrini LS, Vieira DHM, Leite LAR, Gião T, Azevedo RK, Abdallah VD. Parasite diversity of Hoplosternum littorale from the Tietê-Batalha River basin, southeastern Brazil. Bol Inst Pesca 2021; 47: e650. http://dx.doi.org/10.20950/1678-2305/bip.2021.47.e650.
http://dx.doi.org/10.20950/1678-2305/bip...
). In G. altifrons from Jari River, the community of metazoan parasites was composed by seven species, those being: Monogenea, two Digenea, two Nematoda, one Acanthocephala and one Crustacea; parasites with aggregate or random dispersion pattern. The community of metazoan parasites in Satanoperca jurupari (Heckel, 1840) from Igarapé Fortaleza River was composed of eight species, those being: Monogenea, three Digenea, one Nematoda, one Acanthocephala and two Crustacea; all parasites with an aggregate dispersion (Tavares-Dias et al., 2017aTavares-Dias M, Oliveira MSB, Gonçalves RA, Neves LR. Parasitic diversity of a wild Satanoperca jurupari population, an ornamental cichlid in the Brazilian Amazon. Acta Amazon 2017a; 47(2): 155-162. http://dx.doi.org/10.1590/1809-4392201602514.
http://dx.doi.org/10.1590/1809-439220160...
). However, in Cichlasoma bimaculatum (Linnaeus, 1758) from the Igarapé Fortaleza River, the parasite community was composed of only three species, those being: one Monogenea, one Digenea and one Nematoda; parasites with aggregated dispersion (Tavares-Dias et al., 2017bTavares-Dias M, Gonçalves RA, Oliveira MSB, Neves LR. Ecological aspects of the parasites in Cichlasoma bimaculatum (Cichlidae), ornamental fish from the Brazilian Amazon. Acta Biol Colomb 2017b; 22(2): 53. http://dx.doi.org/10.15446/abc.v22n2.60015.
http://dx.doi.org/10.15446/abc.v22n2.600...
). Therefore, such differences in the composition of the diversity and species richness of parasites are attributed to differences in host fish species, environment, age, size, diet, behavior, and distribution and geographical range.

Monogenea are common ectoparasites in freshwater fish populations from different ecosystems and their level of infection depends on environmental quality and habitat type (Ferreira-Sobrinho & Tavares-Dias, 2016Ferreira-Sobrinho A, Tavares-Dias M. A study on monogenean parasites from the gills of some cichlids (Pisces: Cichlidae) from the Brazilian Amazon. Rev Mex Biodivers 2016; 87(3): 1002-1009. http://dx.doi.org/10.1016/j.rmb.2016.06.010.
http://dx.doi.org/10.1016/j.rmb.2016.06....
; Tavares-Dias et al., 2017bTavares-Dias M, Gonçalves RA, Oliveira MSB, Neves LR. Ecological aspects of the parasites in Cichlasoma bimaculatum (Cichlidae), ornamental fish from the Brazilian Amazon. Acta Biol Colomb 2017b; 22(2): 53. http://dx.doi.org/10.15446/abc.v22n2.60015.
http://dx.doi.org/10.15446/abc.v22n2.600...
). In the gills of G. altifrons the levels of infection by S. geophagi were lower than in Geophagus camopiensis (Pellegrin, 1903) (Ferreira-Sobrinho & Tavares-Dias, 2016Ferreira-Sobrinho A, Tavares-Dias M. A study on monogenean parasites from the gills of some cichlids (Pisces: Cichlidae) from the Brazilian Amazon. Rev Mex Biodivers 2016; 87(3): 1002-1009. http://dx.doi.org/10.1016/j.rmb.2016.06.010.
http://dx.doi.org/10.1016/j.rmb.2016.06....
). In the gills of G. altifrons there was also an infection by metacercariae of Posthodiplostomum sp., a digenean parasite that can be found in several freshwater fish around world (Tavares-Dias et al., 2017bTavares-Dias M, Gonçalves RA, Oliveira MSB, Neves LR. Ecological aspects of the parasites in Cichlasoma bimaculatum (Cichlidae), ornamental fish from the Brazilian Amazon. Acta Biol Colomb 2017b; 22(2): 53. http://dx.doi.org/10.15446/abc.v22n2.60015.
http://dx.doi.org/10.15446/abc.v22n2.600...
). The life cycle of the Posthodiplostomum species involves two intermediate hosts, those being a fish species and a mollusk species, and a definitive host, which is a fish-eating bird (Ritossa et al., 2013Ritossa L, Flores VR, Viozzi G. Life cycle stages of a Posthodiplostomum species (Digenea: Diplostomidae) in Patagonia, Argentina. J Parasitol 2013; 99(5): 777-780. http://dx.doi.org/10.1645/12-170.1. PMid:23628085.
http://dx.doi.org/10.1645/12-170.1...
; Tavares-Dias et al., 2017bTavares-Dias M, Gonçalves RA, Oliveira MSB, Neves LR. Ecological aspects of the parasites in Cichlasoma bimaculatum (Cichlidae), ornamental fish from the Brazilian Amazon. Acta Biol Colomb 2017b; 22(2): 53. http://dx.doi.org/10.15446/abc.v22n2.60015.
http://dx.doi.org/10.15446/abc.v22n2.600...
). Therefore, G. altifrons is an intermediate host for metacercariae of Posthodiplostomum sp.

Genarchella genarchella occurred at low levels of infection in the intestine of G. altifrons from Jari River as reported for Hemibrycon surinamensis (Gery, 1962) from Igarapé Fortaleza River (Hoshino et al., 2014Hoshino MDFG, Hoshino EM, Tavares-Dias M. First study on parasites of Hemibrycon surinamensis (Characidae), a host from the eastern Amazon region. Rev Bras Parasitol Vet 2014; 23(3): 343-347. http://dx.doi.org/10.1590/S1984-29612014069. PMid:25271454.
http://dx.doi.org/10.1590/S1984-29612014...
). This species of digenean has mollusk species and smaller fish as intermediate hosts, and large Characiformes and Siluriformes as definitive hosts (Martorelli, 1989Martorelli SR. Estudios parasitologicos en biotopos lenticos de la República Argentina. V. Desarollo del ciclo biologico monoxeno de la metacercaria progenetica de Genarchella genarchella Travassos, 1928 (Digenea, Hemiuridae) parasita de Littoridina parchappei (Mollusca, Hidrobiidae). Rev Mus Cienc Nat Zool 1989; 14(157): 109-117.; Lefebvre & Poulin, 2005Lefebvre F, Poulin R. Progenesis in digenean trematodes: a taxonomic and synthetic overview of species reproducing in their second intermediate hosts. Parasitology 2005; 130(6): 587-605. http://dx.doi.org/10.1017/S0031182004007103.
http://dx.doi.org/10.1017/S0031182004007...
). Therefore, G. altifrons was infected by this digenean through ingestion of infected mollusks or by direct contact with cercariae of G. genarchella in the environment.

Procamallanus (S.) inopinatus occurred at low levels of infection in G. altifrons. This nematode species, usually frequent in wild fish populations in Brazil, has fish as definitive hosts and in general has low levels of prevalence, intensity and abundance due to its complex life cycle (Neves et al., 2020Neves LR, Silva LMA, Florentino AC, Tavares-Dias M. Distribution patterns of Procamallanus (Spirocamallanus) inopinatus (Nematoda: Camallanidae) and its interactions with freshwater fish in Brazil. Rev Bras Parasitol Vet 2020; 29(4): e012820. http://dx.doi.org/10.1590/s1984-29612020092. PMid:33295383.
http://dx.doi.org/10.1590/s1984-29612020...
). The abundance of P. (S.) inopinatus increased with the weight and length of the hosts. It can be assumed that larger host fish are ingesting more infective stages of this nematode than smaller hosts. In addition, in G. altifrons of the Jari River, larvae of Raphidascaris (Sprentacaris) sp. are at infection levels lower than those reported for Geophagus proximus (Castelnau, 1855) found in the Tapajós River (PA) (Oliveira et al., 2017Oliveira MSB, Corrêa LL, Castro LA, Brito LS, Tavares-Dias M. Metazoan parasites of Geophagus proximus, a Cichlidae fish from the eastern Amazon (Brazil). Nat Resour 2017; 8(3): 268-277. http://dx.doi.org/10.4236/nr.2017.83015.
http://dx.doi.org/10.4236/nr.2017.83015...
). Species of Raphidascaris (Sprentacaris) have cladocerans as first intermediate hosts, smaller fish as secondary hosts and predatory fish as definitive hosts (Moravec, 1970Moravec F. On the life history of the nematode Raphidascaris acus (Bloch, 1779) in the natural environment of the River Bystřice, Czechoslovakia. J Fish Biol 1970; 2(4): 313-322. http://dx.doi.org/10.1111/j.1095-8649.1970.tb03290.x.
http://dx.doi.org/10.1111/j.1095-8649.19...
, 1998Moravec F. Nematodes of freshwater fishes of the Neotropical region. Prague: Academia; 1998.). Gorytocephalus spectabilis, occurred at low levels of infection in G. altifrons, which is a definitive host for this acanthocephalan, with unknown life cycle.

Ergasilidae is one of the largest families of order Cyclopoida, and most species are found in freshwater fish. Just adult females have parasites in the gills, fins and nasal cavities of fish species (Taborda et al., 2016Taborda NL, Paschoal F, Luque LJ. A new species of Ergasilus (Copepoda: Ergasilidae) from Geophagus altifrons and G. argyrostictus (Perciformes: Cichlidae) in the Brazilian Amazon. Acta Parasitol 2016; 61(3): 549-555. http://dx.doi.org/10.1515/ap-2016-0073. PMid:27447219.
http://dx.doi.org/10.1515/ap-2016-0073...
). Ergasilus xinguensis occurred at high levels of infestation in the gills of G. altifrons from the Jari River when compared to those reported for Geophagus argyrostictus (Kullander, 1991) and G. altifrons from Rio Xingu, in the state of Pará (Taborda et al., 2016Taborda NL, Paschoal F, Luque LJ. A new species of Ergasilus (Copepoda: Ergasilidae) from Geophagus altifrons and G. argyrostictus (Perciformes: Cichlidae) in the Brazilian Amazon. Acta Parasitol 2016; 61(3): 549-555. http://dx.doi.org/10.1515/ap-2016-0073. PMid:27447219.
http://dx.doi.org/10.1515/ap-2016-0073...
). This is the second report of E. xinguensis for G. altifrons. Furthermore, abundance of E. xinguensis increased with the weight and length of hosts.

In conclusion, the component community of parasites in G. altifrons was composed by ecto- and endoparasite species with aggregate dispersion, but with a predominance of ectoparasites. This omnivorous fish occupies a lower position in the food web and is consumed by other larger fish species and fish-eating birds in the environment. The body size of hosts had a low influence on the parasites infracommunities. This first eco-epidemiological study of G. altifrons records, for the first time, these parasites for this host, except for S. geophagi and E. xinguensis.

References

  • Bush AO, Lafferty KD, Lotz JM, Shostak W. Parasitology meets ecology on its own terms: margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227 PMid:9267395.
    » http://dx.doi.org/10.2307/3284227
  • Camargo M, Giarrizzo T, Isaac VJ. Population and biological parameters of selected fish species from the middle Xingu River, Amazon basin. Braz J Biol 2015;75(3 Suppl 1): 112-124. http://dx.doi.org/10.1590/1519-6984.01914BM PMid:26691084.
    » http://dx.doi.org/10.1590/1519-6984.01914BM
  • Dary EP, Ferreira E, Zuanon J, Röpke CP. Diet and trophic structure of the fish assemblage in the mid-course of the Teles Pires River, Tapajós River basin, Brazil. Neotrop Ichthyol 2017; 15(4): e160173. http://dx.doi.org/10.1590/1982-0224-20160173
    » http://dx.doi.org/10.1590/1982-0224-20160173
  • Eiras JC, Takemoto RM, Pavanelli GC. Métodos de estudos e técnicas laboratóriais em parasitologia de peixes Maringá: Eduem; 2006.
  • Ferreira-Sobrinho A, Tavares-Dias M. A study on monogenean parasites from the gills of some cichlids (Pisces: Cichlidae) from the Brazilian Amazon. Rev Mex Biodivers 2016; 87(3): 1002-1009. http://dx.doi.org/10.1016/j.rmb.2016.06.010
    » http://dx.doi.org/10.1016/j.rmb.2016.06.010
  • Froese R, Pauly D. FishBase. Version (8/2021) [online]. USA: FishBase; 2021 [cited 2021 Oct 15]. Available from: www.fishbase.org
    » www.fishbase.org
  • Hawlitschek O, Yamamoto KC, Carvalho-Neto FGMR. Diet composition of fish assemblage of lake Tupé, Amazonas, Brazil. Rev Colombiana Cienc Anim 2013; 5(2): 313-326. http://dx.doi.org/10.24188/recia.v5.n2.2013.296
    » http://dx.doi.org/10.24188/recia.v5.n2.2013.296
  • Hoshino MDFG, Hoshino EM, Tavares-Dias M. First study on parasites of Hemibrycon surinamensis (Characidae), a host from the eastern Amazon region. Rev Bras Parasitol Vet 2014; 23(3): 343-347. http://dx.doi.org/10.1590/S1984-29612014069 PMid:25271454.
    » http://dx.doi.org/10.1590/S1984-29612014069
  • Lagrue C, Kelly DW, Hicks A, Poulin R. Factors influencing infection patterns of trophically transmitted parasites among a fish community: host diet, host-parasite compatibility or both? J Fish Biol 2011; 79(2): 466-485. https://doi.org/10.1111/j.1095-8649.2011.03041.x
    » https://doi.org/10.1111/j.1095-8649.2011.03041.x
  • Lefebvre F, Poulin R. Progenesis in digenean trematodes: a taxonomic and synthetic overview of species reproducing in their second intermediate hosts. Parasitology 2005; 130(6): 587-605. http://dx.doi.org/10.1017/S0031182004007103
    » http://dx.doi.org/10.1017/S0031182004007103
  • Ludwig JA, Quartet L, Reynolds JF, Reynolds JS. Statistical ecology: a primer in methods and computing New York: John Wiley & Sons; 1988.
  • Magurran A. Measuring biological diversity Oxford: Blackwell Publishing; 2004.
  • Martorelli SR. Estudios parasitologicos en biotopos lenticos de la República Argentina. V. Desarollo del ciclo biologico monoxeno de la metacercaria progenetica de Genarchella genarchella Travassos, 1928 (Digenea, Hemiuridae) parasita de Littoridina parchappei (Mollusca, Hidrobiidae). Rev Mus Cienc Nat Zool 1989; 14(157): 109-117.
  • Moravec F. On the life history of the nematode Raphidascaris acus (Bloch, 1779) in the natural environment of the River Bystřice, Czechoslovakia. J Fish Biol 1970; 2(4): 313-322. http://dx.doi.org/10.1111/j.1095-8649.1970.tb03290.x
    » http://dx.doi.org/10.1111/j.1095-8649.1970.tb03290.x
  • Moravec F. Nematodes of freshwater fishes of the Neotropical region Prague: Academia; 1998.
  • Neves LR, Silva LMA, Florentino AC, Tavares-Dias M. Distribution patterns of Procamallanus (Spirocamallanus) inopinatus (Nematoda: Camallanidae) and its interactions with freshwater fish in Brazil. Rev Bras Parasitol Vet 2020; 29(4): e012820. http://dx.doi.org/10.1590/s1984-29612020092 PMid:33295383.
    » http://dx.doi.org/10.1590/s1984-29612020092
  • Oliveira MSB, Corrêa LL, Castro LA, Brito LS, Tavares-Dias M. Metazoan parasites of Geophagus proximus, a Cichlidae fish from the eastern Amazon (Brazil). Nat Resour 2017; 8(3): 268-277. http://dx.doi.org/10.4236/nr.2017.83015
    » http://dx.doi.org/10.4236/nr.2017.83015
  • Paschoal F, Scholz T, Tavares-Dias M, Luque JL. Dactylogyrids (Monogenea) parasitic on cichlids from northern Brazil, with description of two new species of Sciadicleithrum and new host and geographical records. Acta Parasitol 2016; 61(1): 158-164. http://dx.doi.org/10.1515/ap-2016-0021 PMid:26751887.
    » http://dx.doi.org/10.1515/ap-2016-0021
  • Pelegrini LS, Vieira DHM, Leite LAR, Gião T, Azevedo RK, Abdallah VD. Parasite diversity of Hoplosternum littorale from the Tietê-Batalha River basin, southeastern Brazil. Bol Inst Pesca 2021; 47: e650. http://dx.doi.org/10.20950/1678-2305/bip.2021.47.e650
    » http://dx.doi.org/10.20950/1678-2305/bip.2021.47.e650
  • Poulin R. Parasite species richness in New Zealand fishes: a grossly underestimated component of biodiversity? Divers Distrib 2004; 10(1): 31-37. http://dx.doi.org/10.1111/j.1472-4642.2004.00053.x
    » http://dx.doi.org/10.1111/j.1472-4642.2004.00053.x
  • Ritossa L, Flores VR, Viozzi G. Life cycle stages of a Posthodiplostomum species (Digenea: Diplostomidae) in Patagonia, Argentina. J Parasitol 2013; 99(5): 777-780. http://dx.doi.org/10.1645/12-170.1 PMid:23628085.
    » http://dx.doi.org/10.1645/12-170.1
  • Rohde K, Hayward C, Heap M. Aspects of the ecology of metazoan ectoparasites of marine fishes. Int J Parasitol 1995; 25(8): 945-970. https://doi.org/10.1016/0020-7519(95)00015-T
    » https://doi.org/10.1016/0020-7519(95)00015-T
  • Rózsa L, Reiczigel J, Majoros G. Quantifying parasites in samples of hosts. J Parasitol 2000; 86(2): 228-232. http://dx.doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2 PMid:10780537.
    » http://dx.doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2
  • Soares MGM, Costa EL, Siqueira-Souza FK, Anjos HDB, Yamamoto KC, Freitas CEC. Peixes de lagos do médio Rio Solimões Manaus: Reggo Edições; 2011.
  • Taborda NL, Paschoal F, Luque LJ. A new species of Ergasilus (Copepoda: Ergasilidae) from Geophagus altifrons and G. argyrostictus (Perciformes: Cichlidae) in the Brazilian Amazon. Acta Parasitol 2016; 61(3): 549-555. http://dx.doi.org/10.1515/ap-2016-0073 PMid:27447219.
    » http://dx.doi.org/10.1515/ap-2016-0073
  • Tavares-Dias M, Oliveira MSB, Gonçalves RA, Neves LR. Parasitic diversity of a wild Satanoperca jurupari population, an ornamental cichlid in the Brazilian Amazon. Acta Amazon 2017a; 47(2): 155-162. http://dx.doi.org/10.1590/1809-4392201602514
    » http://dx.doi.org/10.1590/1809-4392201602514
  • Tavares-Dias M, Gonçalves RA, Oliveira MSB, Neves LR. Ecological aspects of the parasites in Cichlasoma bimaculatum (Cichlidae), ornamental fish from the Brazilian Amazon. Acta Biol Colomb 2017b; 22(2): 53. http://dx.doi.org/10.15446/abc.v22n2.60015
    » http://dx.doi.org/10.15446/abc.v22n2.60015
  • Thatcher VE. Amazon fish parasites Sofia: Pensoft Publishers; 2006.
  • Zar JH. Biostatistical analysis New Jersey: Prentice-Hall; 2010.

Publication Dates

  • Publication in this collection
    14 Mar 2022
  • Date of issue
    2022

History

  • Received
    03 Nov 2021
  • Accepted
    17 Feb 2022
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
E-mail: cbpv_rbpv.fcav@unesp.br