Diversity of metazoan parasites in fish Triportheus angulatus and Triportheus auritus living in sympatry in the Brazilian Amazon

Diversidade de parasitos metazoários em peixes Triportheus angulatus e Triportheus auritus vivendo em simpatria na Amazônia brasileira

Abstract

The aim of this study was to compare the diversity and community structure of metazoan parasites in sympatric populations of Triportheus angulatus and Triportheus auritus in the Jari River basin, in the eastern Brazilian Amazon. All the specimens of T. angulatus and T. auritus examined were infected by Anacanthorus furculus, Anacanthorus pithophallus, Digenea gen. sp., Procamallanus (Spirocamallanus) inopinatus, Rhabdochona acuminata, Contracaecum sp., Ergasilus sp. and Acarina gen. sp. These parasites displayed aggregated or random dispersion. The parasite community in T. angulatus and T. auritus presented a similarity of 78%. The diversity indice and richness of parasite species were greater in T. auritus and there were differences in levels of host parasite infection for some infracommunities. Phyllodistomum spatula occurred only in T. angulatus, while metacercariae of Clinostomum marginatum and Digenea gen. sp.2 occurred only in T. auritus. The species richness of the parasites was influenced by host size, as well as the abundance of some parasite infracommunities. This is the first report of these parasites for T. angulatus and T. auritus, except for P. (S.) inopinatus and Contracaecum sp. for T. angulatus.

Keywords:
Amazon; community; fish; helminth; parasites; similarity

Resumo

O objetivo deste estudo foi comparar a diversidade e comunidade de parasitos metazoários em populações simpátricas de Triportheus angulatus e Triportheus auritus da bacia do Rio Jari, na Amazônia oriental brasileira. Todos os espécimes de T. angulatus e T. auritus examinados estavam infectados por Anacanthorus furculus, Anacanthorus pithophallus, Digenea gen. sp., Procamallanus (Spirocamallanus) inopinatus, Rhabdochona acuminata, Contracaecum sp., Ergasilus sp. e Acarina gen. sp. Esses parasitos apresentaram dispersão agregada ou randômica. A comunidade de parasitos em T. angulatus e T. auritus apresentou uma similaridade de 78%. A diversidade e riqueza de espécies de parasitos foram maiores em T. auritus e houve diferenças nos níveis de infecção parasitária entre os hospedeiros para algumas infracomunidades. Phyllodistomum spatula ocorreu somente em T. angulatus, enquanto metacercárias de Clinostomum marginatum e Digenea gen. sp.2 ocorreram somente em T. auritus. A riqueza de espécies de parasitos foi influenciada pelo tamanho dos hospedeiros, bem como pela abundância de algumas infracomunidades de parasitos. Este é o primeiro relato desses parasitos para T. angulatus e T. auritus, exceto P. (S.) inopinatus e Contracaecum sp. para T. angulatus.

Palavras-chave:
Amazônia; comunidade; peixe; helminto; parasito; similaridade

Introduction

The Jari River basin is located in the division between the south of the state of Amapá and the north of the state of Pará, in the north of Brazil. Its source is found in the Serra do Tumucumaque mountain range on the border between Brazil and French Guiana, and it is approximately 800 km long, with its mouth on the Amazon River to the south of the state of Amapá. It has a clear water basin system, and the region is comprised of tropical rainforest (EPE, 2010). There is the presence of anthropic action in the south of the basin, where the original forest was replaced by agricultural activities and silvicultural explorations (Cunha & Cunha, 2010; Abreu & Cunha, 2015). In addition, the region has a great diversity of birds, zooplankton and several other invertebrates that form part of the diet of fish, and which can be hosts for different species of fish parasites.

Triportheus are freshwater fish of the Triportheidae family and Characiformes order, which contains 19 valid species (Froese & Pauly, 2021), including Triportheus angulatus (Spix & Agassiz, 1829) and Triportheus auritus (Valenciennes, 1850). Triportheus angulatus is distributed in the Amazon and Essequibo River basins, while T. auritus is more widely distributed, and is found in the Amazon, Essequibo, Tocantins, and Araguaia river basins, and on the Ilha de Trindade (Trindade Island) (Lima et al., 2003; Lasso & Sánchez-Duarte, 2011; Malabarba, 2004; Froese & Pauly, 2021). Both species are benthopelagic and have omnivorous feeding habits, feeding mainly on insects, fruits, seeds, fragments of fish, plankton and crustaceans (Almeida, 1984; Yamamoto et al., 2004; Lasso & Sánchez-Duarte, 2011; Sá-Oliveira et al., 2014; Rojas et al., 2016; Froese & Pauly, 2021). In general, the reproduction of these fish occurs in the rainy season, when there are lateral migrations to floodplain areas (Santos et al., 1984; Soares et al., 2011; Lasso & Sánchez-Duarte, 2011; Araújo et al., 2012), a favorable environment for fish larvae feeding. As such, in general, T. angulatus and T. auritus are caught in schools in rivers and flooded forests (Lasso & Sánchez-Duarte, 2011; Sá-Oliveira et al., 2014). Triportheus angulatus and T. auritus (Ponte et al., 2016; Goulding et al., 2018) are consumed in the Amazon basin, and are species whose biology has been little studied, notably their parasite diversity and communities.

In wild fish populations, studies on parasite fauna are important not only for understanding diversity, biogeography and population distribution, but also parasite-host-environment interactions (Tavares-Dias et al., 2014; Oliveira et al., 2016; Moreira et al., 2017; Baia et al., 2018). In several species of fish in the Amazon Basin, an ecosystem that serves as a habitat for a number of parasite species, parasite community and infracommunities are yet to be studied, and include species of hosts living in the same environment (sympatry), which tend to have similar parasite communities and infracommunities (Muñoz et al., 2006; Oliveira et al., 2016; Hoshino et al., 2016; Santos-Bustos et al., 2018). However, the community and infracommunities of parasites of sympatric populations of T. angulatus and T. auritus have not yet been investigated. As such, the aim of the present study was to compare the diversity and community structure of metazoan parasites of T. angulatus and T. auritus living in sympatry in the Jari River basin, in the eastern Brazilian Amazon.

Material and Methods

Study area and collection of fishes

Twice monthly, from January to July 2020, T. angulatus and T. auritus were collected in river and stream bank areas and lowland regions of the lower Jari River, close to the Jarilândia District, in the municipal region of Vitória do Jari, in the state of Amapá, Brazil (Figure 1). Fish were collected using reeds, hand lines, nets and gillnets with 25 mm and 30 mm meshes.

Figure 1
Collection site of Triportheus angulatus and Triportheus auritus in lower Jari River, in Amazon River system (Brazil).

The collection of fish was authorized by the Brazilian Ministry of the Environment (SISBio No 73550-1). This study was developed in accordance with the principles adopted by the Brazilian College of Animal Experimentation (COBEA) and was conducted under authorization from the Ethics Committee for Animal Use of Embrapa Amapá (Protocol No 014/2018).

Parasite collection and analysis procedures

Each fish was weighed (g) and measured (standard length, cm), before being necropsied for parasitological analysis. The body surface, opercula, gastrointestinal tract and viscera were examined at the collection site, while the gills were fixed in heated 5% formalin (60-70 ºC) and analyzed at the Embrapa Amapá Aquaculture and Fisheries Laboratory, Macapá (Brazil). The mouth, gills, opercula and fins were examined to check for the presence of ectoparasites and the viscera and gastrointestinal tract for the presence of endoparasites. The collection, fixation, conservation and preparation of the parasites for identification followed previous recommendations (Eiras et al., 2006). The ecological terms used were those recommended by Bush et al. (1997).

Statistical analyses

The normality and homoscedasticity of the data were evaluated using the Shapiro-Wilk and Bartlett tests, respectively. The Brillouin index (HB), Uniformity, Berger-Parker dominance index, species richness (Magurran, 2004) and frequency of dominance, that is, the percentage of infracommunities in which a given parasite species is numerically dominant (Rohde et al., 1995), were calculated to assess the parasite component community using Diversity software (Pisces Conservation Ltd, UK). For comparison of prevalence between T. angulatus and T. auritus the chi-square test (χ²) was used, followed by Yates’s correction. The mean intensity, mean abundance, species richness, diversity index, evenness and Berger-Parker dominance between both hosts were compared with the Mann–Whitney (U) test (Zar, 2010).

The dispersion index (DI) and discrepancy index (D) of Poulin were calculated using the Quantitative Parasitology 3.0 software package, to detect the distribution patterns of the parasite infracommunities (Rózsa et al., 2000) for species with prevalence >10%. The significance of the DI, for each infracommunity, was tested using the d-statistic test (Ludwig & Reynolds, 1988).

Using the R software package (R Core Team, 2020), Non-metric Multidimensional Scaling (NMDS) was performed to order the parasite abundance data from the similarity matrix generated through the Bray-Curtis quantitative index. To test the differences between the parasite component communities of T. angulatus and T. auritus, the ANOSIM test was used with 999 permutations using the Jaccard (J) similarity index (presence/absence of species), and Bray-Curtis dissimilarity index (B) (abundance). The Similarity Percentage test (SIMPER) was used to detect the contribution of each parasite species in the sampling.

The body weight (W) and the total length (L) data were used to calculate the relative condition factor (Kn) of the host fish, as well as the length–weight relationship (W = aL^b) after the logarithmic transformation of the length (L) and weight (W) and subsequent adjustment of two straight lines, thereby obtaining lny = ln a + b ln L (Le Cren, 1951).

The Spearman correlation coefficient (rs) was used to determine possible correlations of the abundance of parasites with the length, weight and Kn of hosts, as well as of hosts length with the species richness and HB.

Results

All specimens of T. angulatus and T. auritus examined (100%) were infected with one or more species of parasites, and a total of 2,410 parasites were collected. Both the hosts were parasitized by Anacanthorus furculus (Kritsky, Boeger & Van Every, 1992), Anacanthorus pithophallus (Kritsky, Boeger & Van Every, 1992), Digenea gen. sp.1; Procamallanus (Spirocamallanus) inopinatus (Travassos, Artigas & Pereira, 1928), Rhabdochona acuminata (Molin, 1860), Contracaecum sp., Ergasilus sp. e Acarina gen.sp. However, Phyllodistomum spatula (Odhner, 1902) occurred only in T. angulatus, while the metacercariae of Clinostomum marginatum (Rudolphi, 1819) and Digenea gen. sp.2 occurred only in T. auritus. However, in both hosts, the monogeneans A. furculus and A. pithophallus were dominant (Table 1).

Table 1
Parasites in Triportheus spp. from lower Jari River, in Brazilian Amazon.

	Triportheus angulatus (n = 30)									Triportheus auritus (n = 34)
Parasite species	P (%)	MI	MA	TNP	FD (%)	SI			P (%)		MI	MA	TNP	FD (%)	SI
Anacanthorus furculus and Anacanthorus pithophallus	96.7	37.4±41.8	36.2±41.7	1085	77.1	Gills			97.1		16.9±17.2	16.4±17.5	558	55.7	Gills
Digenea gen. sp.1 (metacercariae)	20.0	1.8±0.5	0.4±0.9	11	0.8	Gills			23.53		1.3±0.3	0.3±0.6	10	1.0	Gills
Phyllodistomum spatula (metacercariae)	30.0	6.6±2.1	2.0±5.5	59	4.2	Swim bladder			-		-	-	-	-	-
Digenea gen. sp.2 (metacercariae)	3.33	1.0±0.2	0.0	1	0.07	Liver			-		-	-	-	-	-
Clinostomum marginatum (metacercariae)	-	-	-	-	-	-			5.88		1.5±0.2	0.1±0.4	3	0.3	Muscle
Digenea gen. sp.2 (metacercariae)	-	-	-	-	-	-			17.65		1.0±0.1	0.2±0.4	6	2.1	Intestine
Procamallanus (S.) inopinatus	53.3	1.9± 0.8	1.0±1.1	31	2.2	Pyloric caeca			44.12		1.7±0.8	0.7±1.0	25	2.5	Pyloric caeca
Procamallanus (S.) inopinatus	20.0	2.2±0.7	0.4±1.5	13	0.9	Intestine			38.24		1.8±1.1	0.7±1.3	24	2.4	Intestine
Rhabdochona acuminata	3.33	108.0±1.1	3.6±19.7	108	7.7	Caecum pyloric			8.82		2.7±0.7	0.2±0.9	8	0.8	Caecum pyloric
Rhabdochona acuminata	3.33	37.0±2.1	1.2±6.8	37	2.6	Intestine			23.53		31.0±14.1	7.3±19.1	248	24.7	Intestine
Contracaecum sp. (larvae)	43.3	2.6±0.8	1.1±2.4	34	2.4	Abdominal cavity			41.18		3.1±2.0	1.3±3.0	44	4.4	Abdominal cavity
Ergasilus sp.	6.7	1.5±0.6	0.1±0.4	3	0.2	Gills			58.82		2.8±1.2	1.6±2.2	55	5.5	Gills
Acarina gen. sp	26.7	3.3±1.3	0.9±2.2	26	1.8	Gills			17.65		3.5±0.8	0.6±1.8	21	2.1	Gills

• Abbreviations: P, prevalence; MI, mean intensity; MA, mean abundance; TNP, total number of parasites; SI, site of infection. FD: Frequency of dominance, SI: Site of infection, n = Sampling number

Anacanthorus furculus and A. pithophallus, R. acuminata, Ergasilus sp. and Acarina gen. sp. exhibited aggregate dispersion, while Digenea gen. sp.1 and Digenea gen. sp.2, P. spatula, P. (S.) inopinatus and Contracaecum sp. presented random dispersion (Table 2).

Table 2
Dispersion index (DI), d-statistic (d) and discrepancy index (D) for infracommunities of parasites in Triportheus spp. from Iower Jari River, in Brazilian Amazon.

Hosts		Triportheus angulatus				Triportheus auritus
Parasite species		ID	d	D		ID	d	D
Anacanthorus furculus and Anacanthorus pithophallus		2.270	3.289	0.343		2.100	3.587	0.351
Digenea gen. sp.1		1.410	0.858	0.806		0.990	-0.102	0.765
Digenea gen. sp.2		-	-	-		0.850	-0.673	0.800
Phyllodistomum spatula		1.650	1.597	0.746		-	-	-
Procamallanus (S.) inopinatus		1.100	-0.198	0.491		1.110	0.370	0.451
Rhabdochona acuminata		-	-	-		2.950	5.768	0.815
Contracaecum sp.		1.590	1.418	0.669		1.510	1.798	0.669
Ergasilus sp.		-	-	-		5.290	10.500	0.438
Acarina gen. sp.		2.030	2.665	0.785		2.380	4.348	0.846

The prevalence of A. furculus and A. pithophallus was similar (χ² = 0.008, p = 0.529) for T. auritus and T. angulatus, however the average abundance (U = 327.0, p = 0.014) and average intensity (U = 293.5, p = 0.001) were higher in T. angulatus. The prevalence (χ² = 0.116, p = 0.969), mean abundance (U = 500.5, p = 0.898) and mean intensity (U = 15.5, p = 0.272) of Digenea gen. sp.1 were similar in both hosts. The prevalence (χ² = 0.542, p = 0.627), mean abundance (U = 439, p = 0.339) and mean intensity (U = 96.0, p = 0.343) of P. (S.) inopinatus were similar in intestine of both hosts. The prevalence (χ² = 2.539, p = 0.187), mean abundance (U = 413.5, p = 0.194) and mean intensity (U = 35.5, p = 0.759) of P. (S.) inopinatus were similar in pyloric caeca of both hosts. In the pyloric caeca, the prevalence (χ² = 0.820, p = 0.698) and mean abundance (U = 483.5, p = 0.721) of R. acuminata were similar in both hosts. In the intestine, the prevalence (χ² = 5.379, p = 0.05) of R. acuminata was higher in T. auritus than in T. angulatus, while the mean abundance (U = 483.5, p = 0.0.721) was similar for both hosts. The prevalence (χ² = 0.597, p = 0.595), mean abundance (U = 509.0, p = 0.989) and mean intensity (U = 81.0, p = 0.627) of Contracaecum sp. were similar in both hosts. The prevalence (χ² = 19.219, p = 0.0001) and mean abundance (U = 237.5, p = 0.0002) of Ergasilus sp. were higher in T. auritus than T. angulatus. The prevalence (χ² = 0.759, p = 0.570), mean abundance (U = 466.0, p = 0.553) and mean intensity (U = 22.0, p = 0.796) of acari were similar in both hosts.

The component community of T. angulatus and T. auritus was similar and was composed of a similar presence of ectoparasites and endoparasites (Table 3). In T. angulatus, there was a predominance of hosts infected by 2 to 4 parasite species, while in T. auritus there was a predominance of hosts infected by 3 to 4 parasite species (Figure 2).

Table 3
Component community of parasites in Triportheus spp. from lower Jari River, in Brazilian Amazon.

Characteristics	Triportheus angulatus	Triportheus auritus
Examined fish number	30	34
Body length (cm)	15.2 ± 2.0	14.3± 2.4
Weigth (g)	68.3 ± 22.2	38.3 ± 30.4
Prevalence (%) of parasites	100	100
Total number of parasites	1408	1002
Ectoparasite species	5	5
Percentage of ectoparasites	79.9	64.3
Endoparasite species	5	5
Percentage of endoparasites	20.1	35.7
Endoparasite species (adults)	5	6
Endoparasite species (larvae)	4	3

Figure 2
Species richness of parasites in Triportheus angulatus and Triportheus auritus from lower Jari River, in Brazilian Amazon.

Berger-Parker dominance was greater (p<0.05) in T. angulatus, while the Brillouin diversity index, equitability and richness of the parasite species were greater (p<0.001) in T. auritus (Figure 3).

Figure 3
Descriptors of diversity for communities of parasites in Triportheus angulatus and Triportheus auritus from lower Jari River, in Brazilian Amazon (Box plots represent medians, interquartile ranges (25-75%), minimum–maximum ranges and outliers). Different letters indicate differences between descriptor parameters.

The NMDS did not reveal differences in parasite abundance between T. angulatus and T. auritus, with a stress value of 0.022 (Figure 4). The similarity of the component communities of the host populations exhibited qualitative similarity, according to the Jaccard index (J = 0.78) and quantitative dissimilarity according to Bray-Curtis index homogeneity (B = 0.69). ANOSIM did not detect any difference between sites but detected a difference between the parasite communities (R_Jaccard = 0.169, p = 0.0001; R_Bray-Curtis = 0.049; p = 0.033). SIMPER showed that the monogeneans (60.1%) and R. acuminata (15.2%) contributed most to these differences.

Figure 4
Non-metric multidimensional scaling ordination (NMDS) of abundance of parasites in Triportheus angulatus and Triportheus auritus from lower Jari River, in Brazilian Amazon.

In T. angulatus, Brillouin diversity did not reveal a correlation (r_s = -0.235, p = 0.210) with host length, but the richness of the parasite species correlated negatively (r_s = -0.436, 0.016) with host length. In T. auritus, Brillouin diversity revealed no correlation (r_s = -0.312, p = 0.072) with host length, but the richness of the parasite species correlated positively (r_s = 0.335, p = 0.053) with host length. In addition, some parasite infracommunities showed a correlation with the length, weight and Kn of the hosts (Table 4).

Table 4
Spearman correlation coefficient (rs) of the abundance of parasites with the total length, body weight and condition factor (Kn) of Triportheus spp. from lower Jari River, in Brazilian Amazon.

Hosts	Triportheus angulatus							Triportheus auritus
	Length		Weight		Kn			Length		Weight		Kn
Parasite species	rs	p	rs	p	rs	p		rs	p	rs	p	rs	p
Anacanthorus furculus and Anacanthorus pithophallus	-0.349	0.050	-0.21	0.241	0.336	0.069		0.328	0.050	0.340	0.048	0.003	0.984
Digenea gen. sp.1	-0.161	0.395	-0.369	0.044	-0.505	0.004		-0.307	0.077	-0.375	0.029	-0.126	0.476
Digenea gen. sp. 2	-	-	-	-	-	-		-0.119	0.501	-0.193	0.273	-0.162	0.358
Phyllodistomum spatula	-0.044	0.818	0.129	0.496	0.184	0.329		-	-	-	-	-	-
Procamallanus (S.) inopinatus	-0.387	0.034	-0.221	0.240	0.315	0.089		0.448	0.008	0.358	0.037	-0.022	0.9
Rhabdochona acuminata	-	-	-	-	-	-		0.015	0.933	0.094	0.594	-0.043	0.808
Contracaecum sp.	0.130	0.492	0.035	0.854	-0.129	0.494		0.164	0.353	0.097	0.583	0.100	0.572
Ergasilus sp.	-	-	-	-	-	-		0.374	0.029	0.301	0.083	-0.045	0.799
Acarina gen. sp	-0.334	0.071	-0.478	0.007	-0.194	0.303		0.016	0.928	-0.087	0.624	-0.214	0.223

• P= p-values

Discussion

Parasite communities in sympatric hosts with similar ecology and which are phylogenetically related tend to be structured in a similar manner (Muñoz et al., 2006; Oliveira et al., 2016; Hoshino et al., 2016; Santos-Bustos et al., 2018), especially when the diets of these hosts overlap in the environment. The similar component communities of T. angulatus and T. auritus parasites from the lower Rio Jari was composed of Monogenea, Digenea, Nematoda, Crustacea and Acarina, with a predominance of A. furculus and A. pithophallus monogeneans, parasites with simple, direct life cycles (Kohn et al., 2016). ANOSIM revealed that the abundance of parasites was similar in T. angulatus and T. auritus, as both hosts had a qualitative similarity of 78%. The NMDS analysis revealed a slight difference between the parasite community of T. angulatus and T. auritus, caused by the abundance of A. furculus, A. pithophallus and R. acuminata. This can occur due to parasite abundance, which can vary depending on the birth rate and mortality, ability to migrate between hosts, competition, or detachment from the host by mechanical action and/or the physiological responses of the host (Anderson & Gordon, 1982; Von Zuben, 1997; Luque et al., 2013).

In wild fish populations, quantitative and qualitative descriptive patterns are found among parasite communities (Magurran, 2004; Oliveira et al., 2016; Hoshino et al., 2016). In T. angulatus and T. auritus from the lower Rio Jari, we observed that the ecto and endoparasite communities were similar. However, the diversity and richness of parasite species were higher in T. auritus. The prevalence of R. acuminata was higher in T. auritus than in T. angulatus. The prevalence and abundance of Ergasilus sp. were higher in T. auritus. In addition, P. spatula occurred only in T. angulatus, while C. marginatum occurred only in T. auritus. Such differences may be related to the different contacts of these hosts with the infectious forms of the parasites in the environment, possibly associated with food, as fish need to explore different locations to feed, thus increasing the possibility of parasitic infection (Luque et al., 2004; Santos-Bustos et al., 2018).

In T. angulatus and T. auritus, infection by A. furculus and A. pithophallus, R. acuminata, Ergasilus sp. and Acarina gen. sp. presented aggregate dispersion. However, Digenea gen. sp.1 and Digenea gen. sp.2, P. spatula, P. (S.) inopinatus and Contracaecum sp. showed random dispersion. The aggregate dispersion pattern is common in fish populations and is caused by several factors associated with the host and the environment (Rohde et al., 1995; Neves et al., 2013; Oliveira et al., 2016; Hoshino et al., 2016). Random dispersion has generally been attributed to those species of pathogenic parasites which have little opportunity to colonize hosts (Guidelli et al., 2003).

In wild fish populations, the body size of hosts has been identified as a significant predictor of parasite burden (Poulin, 2004; Poulin & Leung, 2011; Paraguassú & Luque, 2007; Baia et al., 2018). Several studies on fish populations have shown that the abundance of parasites increases or decreases according to the age or size of the host fish (Poulin, 2004; Paraguassú & Luque, 2007; Gonçalves et al., 2018; Baia et al., 2018). However, any correlation between the body size of the fish and the burden of the parasites using it as an intermediate host should be positive, as large hosts are unlikely to serve as prey. In T. angulatus, the abundance of A. furculus, Ergasilus sp., A. pithophallus and P. (S.) inopinatus correlated negatively with the length of the hosts. The abundance of Digenea gen. sp.1 and Acarina gen. sp. correlated negatively with body weight. However, the abundance of A. furculus, A. pithophallus and P. (S.) inopinatus in T. auritus correlated positively with the size of the hosts.

To conclude, we showed that the parasite community of T. angulatus and T. auritus were characterized by a low abundance of helminths, low species richness, low diversity and evenness, with a predominance of ectoparasite species. There was similarity between the metazoan parasite community of T. angulatus and T. auritus, but with differences in a few infracommunities, diversity and richness of parasites. Moreover, host size was a factor that influenced the diversity and species richness of parasites. Triportheus angulatus and T. auritus are intermediate hosts for metacercariae of the digeneas and larvae of Contracaecum sp., and definitive hosts for P. (S.) inopinatus and R. acuminata. This was the first study on parasites of T. auritus and T. angulatus from the Jari River.

Acknowledgements

We would like to thank Mr. João Pena de Oliveira for his assistance in collecting the fish. This study received financial support from the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq) through a productivity grant to Tavares-Dias, M (Process number 303013/2015-0) and, Coordination for the Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, CAPES, Brazil) under the financial code 001, PROAP/CAPES resource, and granting the doctoral scholarship to Oliveira, MSB (Process number 88882.430002/2019-01) and Borges, WF (Process number 88887.484708/2020-00).

• How to cite: Borges WF, Oliveira MSB, Tavares-Dias M. Diversity of metazoan parasites in fish Triportheus angulatus and Triportheus auritus living in sympatry in the Brazilian Amazon. Braz J Vet Parasitol 2021; 30(3): e008221. https://doi.org/10.1590/S1984-29612021064

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Publication Dates

• Publication in this collection
  06 Aug 2021
• Date of issue
  2021

History

• Received
  03 May 2021
• Accepted
  15 June 2021