Metazoan endoparasites of Acestrorhynchus lacustris (Actinopterygii: Acestrorhynchidae) from lagoons bordering the upper and middle São Francisco river basin, Brazil

Metazoários endoparasitos de Acestrorhynchus lacustris (Actinopterygii: Acestrorhynchidae) de lagoas marginais da bacia do alto e médio rio São Francisco, Brasil

Abstract

The endoparasitic fauna of Acestrorhynchus lacustris from eight marginal lagoons of the upper and middle São Francisco river basin, Brazil, is recorded here for the first time. For this, a total of 106 specimens of A. lacustris were collected. Eighteen helminth species were found. The taxa recorded were phylum Platyhelminthes: one metacercaria of Clinostomum sp. (Trematoda: Clinostomidae) and plerocercoid larvae of unidentified species (Eucestoda: Proteocephalidae gen. sp.); phylum Acanthocephala: juvenile of Quadrigyrus sp.; and phylum Nematoda: larvae of Brevimulticaecum sp., Contracaecum sp. Type1_, Contracaecum sp. Type2, Hysterothylacium sp., Gnathostoma sp., Spiroxys sp., juvenile and adult specimens of Freitascapillaria sp., Paracapillaria piscicola, Capillariidae gen. sp., Procamallanus (Spirocamallanus) hilarii, Procamallanus (S.) inopinatus, Procamallanus (S.) saofranciscencis, Travassosnema travassosi paranaensis, Cystidicoloides fischeri and Spinitectus rodolphiheringi. Proteocephalidae gen. sp., Contracaecum sp. Type1 and Travassosnema t. paranaensis were present in all eight lagoons with high parasitic indexes. Proteocephalidae gen. sp., Brevimulticaecum sp., Gnathostoma sp., Freitascapillaria sp., P. piscicola, Capillariidae gen. sp., Procamallanus (S.) hilarii, C. fischeri and S. rodolphiheringi are new records for A. lacustris. The known geographical distribution of Gnathostoma sp., Freitascapillaria sp., P. piscicola, Capillariidae gen. sp., Procamallanus (S.) hilarii and Travassosnema t. paranaensis has now been extended to the São Francisco river basin.

Keywords:
Anisakidae; Capillariidae; Digenea; Gnathostomatidae; Lagoon environment parasitology; Proteocephalidae

Resumo

A fauna endoparasitária de Acestrorhynchus lacustris de oito lagoas marginais da bacia do alto e médio rio São Francisco, Brasil, foi registrada pela primeira vez. Para isso, um total de 106 espécimes de A. lacustris foi coletado. Dezoito espécies de helmintos foram encontradas. Os táxons relacionados foram do Filo Platyhelminthes: uma metacercária de Clinostomum sp. (Trematoda: Clinostomidae); larvas plerocercoides de espécie não identificada (Eucestoda: Proteocephalidae gen. sp.); Filo Acanthocephala: juvenil de Quadrigyrus sp.; e Filo Nematoda: larvas de Brevimulticaecum sp., Contracaecum sp. Tipo1_, Contracaecum sp. Tipo2, Hysterothylacium sp., Gnathostoma sp., Spiroxys sp.; juvenis e adultos de Freitascapillaria sp., Paracapillaria piscicola, Capillariidae gen. sp., Procamallanus (Spirocamallanus) hilarii, Procamallanus (S.) inopinatus, Procamallanus (S.) saofranciscencis, Travassosnema travassosi paranaensis, Cystidicoloides fischeri e Spinitectus rodolphiheringi. Proteocephalidae gen. sp., Contracaecum sp. Tipo1 e Travassosnema t. paranaensis foram compartilhadas entre todas as oito lagoas com altos índices parasitários. Proteocephalidae gen. sp., Brevimulticaecum sp., Gnathostoma sp., Freitascapillaria sp., P. piscicola, Capillariidae gen. sp., Procamallanus (S.) hilarii, C. fischeri e S. rodolphiheringi são novos registros para A. lacustris. Gnathostoma sp., Freitascapillaria sp., P. piscicola, Capillariidae gen. sp., Procamallanus (S.) hilarii e Travassosnema t. paranaensis têm sua distribuição geográfica estendida para a bacia do rio São Francisco.

Palavras-Chave:
Anisakidae; Capillariidae; Digenea; Gnathostomatidae; parasitologia de ambiente lagunar; Proteocephalidae

Introduction

The hydrographic basin of the São Francisco river is the largest in Brazil, and traditionally it is divided into four segments: upper (from the Serra da Canastra source to Pirapora, in the state of Minas Gerais), middle (from Pirapora to Remanso, in the state of Bahia, which is the longest stretch), sub-middle (from Remanso to Paulo Afonso, both in the state of Bahia) and lower (from Paulo Afonso, in the state of Bahia to its mouth between the states of Sergipe and Alagoas, with marine influence) (Planvasf, 1989). Its ichthyofauna is diverse, with socioenvironmental importance, especially for fishing (Godinho & Godinho, 2003).

The monotypic genus Acestrorhynchus Eigenmann and Kennedy, 1903 (Acestrorhynchidae: Acestrorhynchinae), comprises fourteen valid species of endemic South American fish. Among these, Acestrorhynchus britskii Menezes, 1969, endemic of São Francisco river basin cited as Least Concern (LC) in Red List of threatened species (ICMBio, 2021); and Acestrorhynchus lacustris (Lütken, 1875) is native to the São Francisco and upper Paraná river basins (Froese & Pauly, 2021). The fish of this subfamily live in lake, lagoon or river pool environments (Britski et al., 1988). They have an elongated and compressed body and a mouth provided with caniniform conical teeth and are therefore popularly known as “peixe-cachorro” (“dogfish”) (Britski et al., 1999).

Studies involving the eating habits of A. lacustris in the Tibagi river (Bennemann et al., 2000) and Itaipu reservoir (Hahn et al., 2000), both in the state of Paraná, have classified this fish species as preferentially piscivorous. In the hydrographic basin of the São Francisco river, studies by Gomes & Verani (2003) in the Três Marias reservoir (upper river), Pompeu & Godinho (2003) in marginal lagoons of the middle river, Luz et al. (2009) in Curralinho lagoon of the sub-middle river and Rocha et al. (2011) in the Sobradinho reservoir (between the middle and sub-middle stretches) considered the eating habits of A. lacustris and its congener A.britskii, to be exclusively piscivorous, and occasionally attributed the presence of items such as plant tissue, insects and shrimps in their diets to accidental ingestion.

Brasil-Sato (2003) compiled a list of fish parasites from the São Francisco river basin and recorded the nematodes Contracaecum sp., Hysterothylacium sp. (indicated as Heterotyphlum sp.), Travassosnema travassosi Costa, Moreira & Oliveira, 1991, and Procamallanus (Spirocamallanus) saofranciscencis (Moreira, Oliveira & Costa, 1994), as endoparasites of A. lacustris. Costa et al. (2011) added the first record of Rhabdochona (Rhabdochona) acuminata (Molin, 1860) in this fish species from the Três Marias reservoir, on the upper São Francisco river.

The aim of the current study was to register the metazoan endoparasites of A. lacustris specimens collected in eight lagoons bordering the upper and middle São Francisco river and expand the knowledge of freshwater fish parasitology in this important Brazilian river basin.

Materials and Methods

A total of 106 specimens of A. lacustris from eight marginal lagoons in the São Francisco river basin were provided for parasitological analysis by the management team of the project “Revitalization of the marginal lagoons of upper-middle São Francisco river basin, Minas Gerais, Brazil”. This project was conducted in cooperation between the Brazilian Institute for the Environment and Renewable Natural Resources (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, IBAMA) and the Development Company for the São Francisco and Parnaíba Valleys (Companhia de Desenvolvimento dos Vales do São Francisco e do Parnaíba, CODEVASF).

Among these fish, 56 were collected from five lagoons (Batatas, Feia, Piranhas, Porcos and Silva Campos) in the upper São Francisco river basin and 50 came from three lagoons (Curral de Varas, Grande and Mocambo) in the middle São Francisco river basin (Tables 1, 2 and Figures 1-2). The software QGIS 3.14.16 with GRASS 7.8.3 was used to obtain maps (Figures 1-2). The fish were fixed in 3% formalin, marked with biometric data and the lagoon name (on tags) and individually packaged inside plastic bags. They were then sent to the Parasite Ecology and Biology Laboratory (Laboratório de Biologia e Ecologia de Parasitos, LABEPAR) of the Federal Rural University of Rio de Janeiro (Universidade Federal Rural do Rio de Janeiro, UFRRJ), Seropédica, state of Rio de Janeiro, Brazil, for examination.

Table 1
Localities from which Acestrorhynchus lacustris was collected, from lagoons in the upper and middle São Francisco river basin, states of Minas Gerais (MG) and Bahia (BA), Brazil.

Localities (lagoons)	Coordinates	Municipality	Riverside bank
Upper
Porcos	19º59’31” S - 45º36’04” O	Lagoa da Prata/MG	Right
Batatas	19º59’09” S - 45º35’24” O	Lagoa da Prata/MG	Right
Feia	19º57’54” S - 45º34’22” O	Lagoa da Prata/MG	Right
Piranhas	19º48’09” S - 45º29’01” O	Moema/MG	Right
Silva Campos	18º58’18” S - 45º05’54” O	Pompéu/MG	Right
Middle
Grande	15º30’27” S - 44º17’04” O	Pedras de Maria Cruz/MG	Right
Curral de Varas	15º03’09” S - 44º02’00” O	Itacarambi/MG	Left
Mocambo	14º19’40” S - 43º43’37” O	Malhada/BA	Right

Table 2
Numbers and sizes of Acestrorhynchus lacustris collected from lagoons bordering the São Francisco river basin: total number – N; number of females – NF; number of males – NM; mean total length – MTL; and respective size ranges.

Collection localities (lagoons)	Collection period	N	NF	NM	MTL	Range
Upper
Porcos	September/2016	6	3	3	16.3	14.0 – 19.0
Batatas	September/2018	27	6	21	18.0	15.5 – 23.0
Feia	June/2011	7	6	1	24.8	23.0 – 29.0
Piranhas	June/2011	13	11	2	17.7	15.0 – 20.0
Silva Campos	October/2016	3	3	-	25.3	22.0 – 28.0
Middle
Grande	November/2008	12	7	5	20.4	16.0 – 26.0
Curral de Varas	October/2007	15	10	5	19.7	15.5 – 25.0
Mocambo	October/2007	23	13	10	20.8	15.0 – 26.0

Figure 1
Collection areas (lagoons) for Acestrorhynchus lacustris in the region of the upper São Francisco river basin, state of Minas Gerais (MG), Brazil.

Figure 2
Collection areas (lagoons) for Acestrorhynchus lacustris in the region of the middle São Francisco river basin, states of Minas Gerais (MG) and Bahia (BA), Brazil.

The procedure for fixing and preparing temporary or permanent slides of parasite specimens followed standardized methodology (Amato et al., 1991). To identify and classify the taxa, the following references were consulted: Kanev et al. (2002) for digenean metacercariae; Chervy (2002) and Chambrier et al. (2017) for eucestode plerocercoids; Amin (1987) for juvenile specimens of Acanthocephala; and Moravec (1998) for larvae, juveniles and adults of Nematoda.

Voucher specimens of parasites of A. lacustris were deposited in the Helminthological Collection of the Oswaldo Cruz Institute (Coleção Helmintológica do Instituto Oswaldo Cruz, CHIOC), state of Rio de Janeiro, RJ, Brazil, in accordance with the numbering presented in the results section (Table 3). The fish voucher specimen was deposited in the Zoological Museum of the University of São Paulo (Museu de Zoologia da Universidade de São Paulo, MZUSP), State of São Paulo, SP, Brazil, under the number 105.886.

Table 3
Occurrence of endoparasite species, deposition numbers of voucher specimens in CHIOC (Coleção Helmintológica do Instituto Oswaldo Cruz), their parasite indexes (prevalence - P; mean intensity - MI; mean abundance - MA; standard deviation - SD) and infection sites (abdominal cavity - AC; stomach - S; intestine - I; intestinal cecum - IC; liver - L), in Acestrorhynchus lacustris from lagoons bordering the upper and middle São Francisco river, states of Minas Gerais (MG) and Bahia (BA), Brazil.

Endoparasites species		CHIOC	Indexes			Site	Localities (lagoons)
			P (%)	MI ± SD	MA ± SD
Platyhelminthes (Larvae)
	Clinostomidae
	Clinostomum sp. (metacercaria)	39106	8.00	1.00	0.08 ± 0.29	AC	Grande	Middle
	Proteocephalidae
	Proteocephalidae gen. sp. (plerocercoids)	.	100	101.70 ± 75.48	101.70 ± 75.48	AC; IC	Porcos	Upper
		.	22.00	20.83 ± 12.86	4.63 ± 10.09	AC; IC	Batatas	Upper
		.	100	224.30 ± 149.87	224.30 ± 149.87	AC; IC	Feia	Upper
		39123	77.0	420.00 ± 221.16	323.10 ± 265.72	AC; IC	Piranhas	Upper
		.	33.00	10.00	3.33 ± 5.77	AC; IC	Silva Campos	Upper
		.	100	281.70 ± 137.70	281.70 ± 137.70	AC; IC	Grande	Middle
		39122	100	858.60 ± 699.94	858.60 ± 699.94	AC; IC	Curral de Varas	Middle
		39124	87.00	187.00 ± 135.03	162.61 ± 141.04	AC; IC	Mocambo	Middle
Acanthocephala (Juveniles)
	Quadrigyridae
	Quadrigyrus sp.	.	4.00	1.00	0.04 ± 0.19	AC	Batatas	Upper
Nematoda (Larvae)
	Acanthocheilidae
	Brevimulticaecum sp.	39107	4.00	1.00	0.04 ± 0.21	AC	Mocambo	Middle
	Anisakidae
	Contracaecum sp. Type1	39150	33.00	15.50 ± 13.44	5.17 ± 10.01	AC	Porcos	Upper
		39152	85.00	5.43 ± 4.91	4.63 ± 4.95	AC	Batatas	Upper
		39151	100	14.57 ± 24.76	14.57 ± 24.76	AC	Feia	Upper
		39145	100	11.69 ± 6.13	11.69 ± 6.13	AC	Piranhas	Upper
		39146	100	8.33 ± 6.66	8.33 ± 6.66	AC	Silva Campos	Upper
		39149	67.00	1.75 ± 0.71	1.17 ± 1.03	AC	Grande	Middle
		39147	53.00	1.63 ± 1.06	0.87 ± 1.13	AC	Curral de Varas	Middle
		39148	87.00	15.00 ± 17.31	13.04 ± 16.90	AC; IC; L	Mocambo	Middle
	Contracaecum sp. Type2	39143	4.00	1.00	0.04 ± 0.19	AC	Batatas	Upper
		39144	14.00	1.00	0.14 ± 0.38	AC	Feia	Upper
		39141	8.00	1.00	0.08 ± 0.28	AC	Piranhas	Upper
		39140	33.00	1.00	0.33 ± 0.58	AC	Silva Campos	Upper
		30139	17.00	1.00	0.17 ± 0.39	AC	Grande	Middle
		39142	7.00	1.00	0.07 ± 0.26	AC	Curral de Varas	Middle
	Hysterothylacium sp.	39128	44.00	3.92 ± 4.58	1.74 ± 3.58	AC	Batatas	Upper
		.	14.00	3.00	0.43 ± 1.13	AC	Feia	Upper
		39126	33.00	1.00	0.33 ± 0.58	AC	Silva Campos	Upper
		39127	20.00	1.33 ± 0.58	0.27 ± 0.59	AC; S	Curral de Varas	Middle
		39125	9.00%	2.50 ± 2.12	0.22 ± 0.85	AC	Mocambo	Middle
	Gnathostomatidae
	Gnathostoma sp.	39108	7.00	1.00	0.07 ± 0.26	S	Curral de Varas	Middle
	Spiroxys sp.	39130	59.00	2.56 ± 2.19	1.52 ± 2.10	AC	Batatas	Upper
		39129	33.00	3.00	1.00 ± 1.73	AC	Silva Campos	Upper
		39132	7.00	1.00	0.07 ± 0.26	AC	Curral de Varas	Middle
		39131	39.00	2.56 ± 2.24	1.00 ± 1.86	AC; IC	Mocambo	Middle
Nematoda (juvenile/adult)
	Capillariidae
	Freitascapillaria sp.	39109	14.00	1.00	0.14 ± 0.38	AC	Feia	Upper
	Paracapillaria piscicola	39110	14.00	2.00	0.29 ± 0.76	AC	Feia	Upper
	Capillariidae gen. sp.	39111; 39112	29.00	1.00	0.29 ± 0.49	S; AC	Feia	Upper
	Camallanidae
	Procamallanus (Spirocamallanus) hilarii	39117; 39118	26.00	2.00 ± 0.82	0.52 ± 0.98	S; I; IC	Batatas	Upper
	Procamallanus (S.) inopinatus	39138	4.00	1.00	0.04 ± 0.19	I	Batatas	Upper
		.	14.00	1.00	0.14 ± 0.38	I	Feia	Upper
		39133; 39134	33.00	2.00	0.67 ± 1.15	I	Silva Campos	Upper
		39137	17.00	2.00 ± 1.41	0.33 ± 0.89	IC	Grande	Middle
		39136	13.00	1.50 ± 0.71	0.20 ± 0.56	I	Curral de Varas	Middle
		39135	4.00	1.00	0.04 ± 0.21	IC	Mocambo	Middle
	Procamallanus (S.) saofranciscencis	39115	8.00	3.00	0.25 ± 0.87	I	Grande	Middle
		39116	22.00	2.00 ± 1.00	0.43 ± 0.95	I; IC	Mocambo	Middle
	Guyanemidae
	Travassosnema travassosi paranaensis	39155	100	10.17 ± 6.88	10.17 ± 6.88	AC	Porcos	Upper
		39161	74.00	5.25 ± 2.84	3.89 ± 3.38	AC	Batatas	Upper
		39158a; 39158b	100	9.86 ± 11.99	9.86 ± 11.99	AC	Feia	Upper
		39156	92.00	11.33 ± 7.08	10.46 ± 7.47	AC	Piranhas	Upper
		39153	100	3.33 ± 1.53	3.33 ± 1.53	AC	Silva Campos	Upper
		39154a; 39154b	92.00	3.82 ± 2.60	3.50 ± 2.71	AC	Grande	Middle
		39159; 39160	80.00	6.17 ± 6.26	4.93 ± 6.11	AC	Curral de Varas	Middle
		39157	52.00	5.17 ± 4.34	2.70 ± 4.05	AC; IC	Mocambo	Middle
	Cystidicolidae
	Cystidicoloides fischeri	39121	7.00	7.00 ± 1.41	0.52 ± 1.89	AC	Batatas	Upper
		39120	29.00	3.00 ± 1.41	0.86 ± 1.57	AC; IC	Feia	Upper
		39119	9.00	1.00	0.09 ± 0.29	IC; AC	Mocambo	Middle
	Spinitectus rodolphiheringi	39113; 39114	67.00	2.50 ± 0.71	1.67 ± 1.53	AC; S	Silva Campos	Upper

The ecological descriptors used were in accordance with Bush et al. (1997). Statistical tests were only applied to the parasite species that showed parasite prevalence higher than 10% (Bush et al., 1990). The software GraphPad Prism 9.2.0 was used to calculate these indexes. The frequency of dominance, the shared frequency of dominance and the mean relative dominance of each parasite species were calculated as described by Rohde et al. (1995). The ratio between the mean parasite variance and abundance (dispersion index, DI) was calculated for each parasite species to determinate its distribution pattern. The significance of the distribution was tested using the statistical d-test (d > 1.96) (Ludwig & Reynolds, 1988).

Student’s t test was used to check for possible differences in the total length of hosts, in relation to their sex. Pearson’s correlation coefficient (r) was used to assess the correlation between parasite prevalence and the hosts’ size classes, as estimated using Sturges’s formula (Sturges, 1926). Spearman’s correlation coefficient by ranks (rs) was used to evaluate possible correlations between the host’s total length and abundance. The chi-square test with Yate’s correction (x² Yates) and Fisher's exact test (F(p)) were used to determine the influence of sex on the prevalence of parasites. The Mann-Whitney test (U) was used to assess possible differences in abundance, in relation to the hosts’ sex. These tests were applied only to species from two helminthic communities (Batatas and Mocambo lagoons), from which more than twenty fish specimens were examined. The statistical significance level adopted was p < 0.05 (Zar, 1996).

Results

In total, eighteen species of helminthic endoparasites in parasite communities of A. lacustris from these eight marginal lagoons were identified. Two taxa in the phylum Platyhelminthes were identified: one metacercaria of Clinostomum sp. (Trematoda: Clinostomidae) and plerocercoid larvae of Eucestoda (Proteocephalidae gen. sp.); one taxon of the phylum Acanthocephala: Quadrigyridae - Quadrigyrus sp.; and fifteen taxa of the phylum Nematoda: Acanthocheilidae - Brevimulticaecum sp.; Anisakidae – Contracaecum sp. Type1 larvae of Moravec, Kohn & Fernandes, 1993, Contracaecum sp. Type2 larvae of Moravec, Kohn & Fernandes, 1993, and Hysterothylacium sp.; Gnathostomatidae – Gnathostoma sp., and Spiroxys sp.; Capillariidae – Freitascapillaria sp., Paracapillaria piscicola (Travassos, Artigas & Pereira, 1928) and unidentified species of Capillariidae gen. sp.; Camallanidae – Procamallanus (Spirocamallanus) hilarii Vaz & Pereira, 1934, Procamallanus (Spirocamallanus) inopinatus Travassos, Artigas & Pereira, 1928, and Procamallanus (S.) saofranciscencis; Guyanemidae – Travassosnema travassosi paranaensis Moravec, Kohn & Fernandes, 1993; and Cystidicolidae – Cystidicoloides fischeri (Travassos, Artigas & Pereira, 1928) and Spinitectus rodolphiheringi Vaz & Pereira, 1934.

Fourteen species of helminths were found in five lagoons in the upper São Francisco river basin and twelve species in three lagoons in the middle São Francisco river basin. The parasite indexes, sites and stages of parasite species development recorded in A. lacustris per lagoon and its location in the upper or middle São Francisco river basin are listed in Table 3.

Among the larval endoparasites identified (Table 3), Proteocephalidae gen. sp. and Contracaecum sp. Type1 occurred in eight lagoons with high parasite indexes (prevalence reaching 100% in four and three communities, respectively) with high abundance values, compared with the other species of community parasites found. These two species were followed by Contracaecum sp. Type2, Hysterothylacium sp. and Spiroxys sp., which occurred in six, five and four lagoons, respectively, with prevalence usually higher than 10%. Clinostomum sp., Quadrigyrus sp. Brevimulticaecum sp. and Gnathostoma sp. were found parasitizing a single specimen of A. lacustris from the Grande, Mocambo and Curral de Varas lagoons (which are all in the middle São Francisco river basin), respectively, with prevalence below 10% and average abundance below 1.0.

Among the juvenile and adult endohelminths represented by nematodes (Table 3), Travassosnema t. paranaensis stands out. This occurred in eight lagoons, in which the minimum prevalence registered was greater than 50% (reaching 100% of the fish in three lagoons in the upper São Francisco river basin), with a minimum abundance of 2.7 specimens per infected fish. This species was followed by Procamallanus (S.) inopinatus, which was recorded in six lagoons, with prevalence greater than 10% in four of them. Cystidicoloides fischeri occurred in the communities of three lagoons: two in the upper and one in the middle São Francisco river basin; and Procamallanus (S.) saofranciscencis occurred in two lagoons in the middle São Francisco river basin. For each of these, prevalence above 10% was found in a single lagoon, in the upper and middle São Francisco river basin, respectively.

Among these eighteen species that were components of the parasite communities of “peixes-cachorros” from São Francisco river lagoons, six (Quadrigyrus sp., Freitascapillaria sp., P. piscicola, Capillariidae gen. sp., Procamallanus (S.) hilarii and S. rodolphiheringi) and three (Clinostomum sp., Brevimulticaecum sp., and Gnathostoma sp.) helminth species were exclusive to the upper and middle São Francisco river basin, respectively. The other nine species occurred in lagoons in both stretches of the basin.

Seven species were shared between two helminth communities in the largest sampling of A. lacustris from the upper (Batatas lagoon) and middle (Mocambo lagoon) São Francisco river basin: four species with prevalence above 10% (Proteocephalidae gen. sp., Contracaecum sp. Type1, Spiroxys sp. and Travassosnema t. paranaensis); one species, Hysterothylacium sp., with prevalence below 10% in Mocambo lagoon; and two species, Procamallanus (S.) inopinatus and C. fischeri, with prevalence below 10% in both lagoons (Table 3).

The most dominant species in the upper São Francisco river basin were Proteocephalidae gen. sp. in the Piranhas (dominance frequency value = 10), Feia (7) and Porcos (6) lagoons; Travassosnema t. paranaensis in Batatas lagoon (9); and Contracaecum sp. Type1 in Silva Campos lagoon (2). Proteocephalidae gen. sp. was also the most dominant taxon in the three lagoons in the middle São Francisco river basin, with dominance frequency values of 20 in Mocambo, 15 in Curral de Varas and 12 in Grande. All species that had a significant statistical d-test result showed aggregated distribution (Table 4).

Table 4
Dominance frequency, shared dominance frequency, average relative dominance (standard deviation - SD), dispersion index with distribution pattern (< 1.00 - aggregated; > 1.00 - uniform; = 1.00 - random) and statistical d-test, regarding Acestrorhynchus lacustris collected from marginal lagoons in the upper and middle São Francisco river basin, states of Minas Gerais (MG) and Bahia (BA), Brazil.

Endoparasites species		Dominance Frequency	Shared Dominance Frequency	Average Relative Dominance ± SD	Dispersion Index			Localities (lagoons)
					Value	Distribution	Statistical d-test
Platyhelminthes (Larvae)
	Proteocephalidae
	Proteocephalidae gen. sp. (plerocercoids)	6	0	0.878 ± 0.063	56.03	Aggregated	20.67*	Porcos	Upper
		5	0	0.134 ± 0.270	21.98	Aggregated	26.67*	Batatas	Upper
		7	0	0.850 ± 0.146	100.15	Aggregated	31.35*	Feia	Upper
		10	0	0.715 ± 0.411	218.54	Aggregated	99.46*	Piranhas	Upper
		0	0	0.104 ± 0.180	10.00	Aggregated	4.59*	Silva Campos	Upper
		12	0	0.976 ± 0.018	67.32	Aggregated	33.90*	Grande	Middle
		15	0	0.985 ± 0.014	570.59	Aggregated	121.20*	Curral de Varas	Middle
		20	0	0.789 ± 0.322	122.34	Aggregated	66.81*	Mocambo	Middle
Nematoda (Larvae)
	Anisakidae
	Contracaecum sp. Type1	0	0	0.027 ± 0.042	19.39	Aggregated	10.92*	Porcos	Upper
		7	2	0.338 ± 0.313	5.30	Aggregated	9.46*	Batatas	Upper
		0	0	0.044 ± 0.047	42.07	Aggregated	19.15*	Feia	Upper
		0	0	0.089 ± 0.143	3.21	Aggregated	3.99*	Piranhas	Upper
		2	0	0.408 ± 0.096	5.32	Aggregated	2.88*	Silva Campos	Upper
		0	0	0.007 ± 0.009	0.91	Uniform	0.11	Grande	Middle
		0	0	0.002 ± 0.003	1.46	Aggregated	1.20	Curral de Varas	Middle
		2	0	0.138 ± 0262	21.90	Aggregated	24.48*	Mocambo	Middle
	Contracaecum sp. Type2	0	0	0.000 ± 0.001	1.00	Random	0.15	Feia	Upper
		0	0	0.010 ± 0.018	1.00	Random	0.27	Silva Campos	Upper
		0	0	0.000 ± 0.001	0.91	Uniform	0.11	Grande	Middle
	Hysterothylacium sp.	2	0	0.044 ± 0.077	7.36	Aggregated	12.42*	Batatas	Upper
		0	0	0.001 ± 0.003	3.00	Aggregated	2.68*	Feia	Upper
		0	0	0.026 ± 0.44	1.00	Random	0.27	Silva Campos	Upper
		0	0	0.001 ± 0.001	1.32	Aggregated	0.89	Curral de Varas	Middle
	Gnathostomatidae
	Spiroxys sp.	2	0	0.121 ± 0.201	2.91	Aggregated	5.15*	Batatas	Upper
		0	0	0.031 ± 0.054	3.00	Aggregated	1.73	Silva Campos	Upper
		0	0	0.006 ± 0.011	3.45	Aggregated	5.77*	Mocambo	Middle
Nematoda (juvenile/adult)
	Capillariidae
	Freitascapillaria sp.	0	0	0.002 ± 0.004	1.00	Random	0.15	Feia	Upper
	Paracapillaria piscicola	0	0	0.002 ± 0.004	2.00	Aggregated	1.58	Feia	Upper
	Capillariidae gen. sp.	0	0	0.001 ± 0.002	0.83	Uniform	0.15	Feia	Upper
	Camallanidae
	Procamallanus (Spirocamallanus) hilarii	0	0	0.030 ± 0.076	1.84	Aggregated	2.63*	Batatas	Upper
	Procamallanus (S.) inopinatus	0	0	0.001 ± 0.002	1.00	Random	0.15	Feia	Upper
		0	0	0.056 ± 0.096	2.00	Aggregated	1.10	Silva Campos	Upper
		0	0	0.002 ± 0.004	2.36	Aggregated	2.63*	Grande	Middle
		0	0	0.001 ± 0.002	1.57	Aggregated	1.44	Curral de Varas	Middle
	Procamallanus (S.) saofranciscencis	0	0	0.004 ± 0.012	2.05	Aggregated	2.95*	Mocambo	Middle
	Guyanemidae
	Travassosnema travassosi paranaensis	0	0	0.095 ± 0.036	4.66	Aggregated	3.83*	Porcos	Upper
		9	2	0.326 ± 0.277	2.93	Aggregated	5.21*	Batatas	Upper
		0	0	0.097 ± 0.146	14.59	Aggregated	9.91*	Feia	Upper
		3	0	0.119 ± 0.218	5.33	Aggregated	6.52*	Piranhas	Upper
		1	0	0.232 ± 0.162	0.70	Uniform	0.06	Silva Campos	Upper
		0	0	0.015 ± 0.012	2.10	Aggregated	2.22*	Grande	Middle
		0	0	0.012 ± 0.012	7.57	Aggregated	9.36*	Curral de Varas	Middle
		0	0	0.020 ± 0.029	6.09	Aggregated	9.81*	Mocambo	Middle
	Cystidicolidae
	Cystidicoloides fischeri	0	0	0.002 ± 0.004	2.89	Aggregated	2.57*	Feia	Upper
	Spinitectus rodolphiheringi	0	0	0.132 ± 0.119	1.40	Aggregated	0.63	Silva Campos	Upper

• ^*
  significance value > 1.96

Female fish specimens were larger than males in three lagoons: Batatas (t = 4.385; p = 0.001), Grande (t = 2.899; p = 0.015) and Mocambo (t = 3.297; p = 0.003). In the other lagoons, although females were also larger than males, this difference was not significant (Porcos: t = 0.730; p = 0.498; Feia: t = 0.104; p = 0.921; Piranhas: t = 0.357; p = 0.728; Curral de Varas: t = 2.016; p = 0.063). In Silva Campos lagoon only females were collected.

Contracaecum Type1 was more abundant in larger fish (rs = 0.669; p = 0.001) and in female fish (U = 19.00; p = 0.003) from Mocambo lagoon. Hysterothylacium sp. was more abundant in smaller fish (rs = -0.459; p = 0.016) from Batatas lagoon, without sex correlation. The parasite indexes recorded for the other parasite species analyzed in the current study were not influenced by the host’s total length and sex (Table 5).

Table 5
Analysis on parasite indices, regarding possible influence of total length (r = Pearson's correlation coefficient; rs = Spearman rank correlation coefficient) and sex (X² = chi-square with Yates correction; F(p) = Fisher’s exact test; and U = Mann-Whitney U test), on Acestrorhynchus lacustris collected from the upper (Batatas lagoon, state of Minas Gerais, MG) and middle (Mocambo lagoon, state of Bahia, BA) São Francisco river basin, Brazil.

Endoparasites species		Total length				Sex					Localities (lagoons)
		Prevalence		Abundance		Prevalence			Abundance
		r	p	rs	p	X2	P	F (p)	U	p
Platyhelminthes (Larvae)
	Proteocephalidae
	Proteocephalidae gen. sp. (plerocercoids)	-0.473	0.343	-0.288	0.145	0.003	0.095	>0.999	52.50	0.358	Batatas	Upper
		-0.354	0.492	-0.256	0.239	0.145	0.704	>0.999	46.00	0.247	Mocambo	Middle
Nematoda (Larvae)
	Anisakidae
	Contracaecum sp. Type1	0.401	0.430	0.158	0.430	0.018	0.895	>0.999	48.50	0.410	Batatas	Upper
		0.282	0.589	0.669	0.001*	2.230	0.135	0.069	19.00	0.003*	Mocambo	Middle
	Hysterothylacium sp.	-0.774	0.071	-0.460	0.016*	1.181	0.277	0.182	36.50	0.105	Batatas	Upper
	Gnathostomatidae
	Spiroxys sp.	-0.556	0.252	-0.033	0.869	0.003	0.958	0.662	59.00	0.837	Batatas	Upper
		-0.676	0.140	-0.346	0.106	0.006	0.940	>0.999	64.50	>0.999	Mocambo	Middle
Nematoda (juvenile/adult)
	Camallanidae
	Procamallanus (Spirocamallanus) hilarii	-0.545	0.296	-0.068	0.738	0.003	0.953	>0.999	53.00	0.411	Batatas	Upper
	Procamallanus (S.) saofranciscencis	-0.353	0.493	-0.026	0.905	0.472	0.492	0.339	51.50	0.254	Mocambo	Middle
	Guyanemidae
	Travassosnema travassosi paranaensis	-0.056	0.916	-0.006	0.977	0.220	0.639	0.633	56.60	0.717	Batatas	Upper
		-0.071	0.894	0.328	0.127	0.365	0.546	0.414	50.00	0.337	Mocambo	Middle

• ^*
  significant values (significance level p < 0.05).

The richness of the parasite communities of A. lacustris in these eight lagoons was based on a minimum of three species (Proteocephalidae gen. sp., Contracaecum sp. Type1 and Travassosnema t. paranaensis), which were shared among all communities. In the lagoons of the upper São Francisco river basin, the parasite richness of A. lacustris ranged from three to ten species of helminths. The parasite communities from the Batatas and Feia lagoons in the upper São Francisco river basin presented the greatest richness (ten species each), while Silva Campos lagoon had eight species, Piranhas had four species and Porcos had the smallest number of species recorded (three species). Among the lagoons of the middle São Francisco river basin, the highest richness occurred in the parasite community of A. lacustris from Mocambo lagoon (nine species), followed by Curral de Varas Lagoon (eight species) and Grande Lagoon (seven species).

Discussion

The diet of A. lacustris in this study consisted mainly of fish, thus reinforcing the previous reports regarding the piscivorous habit of acestrorhynchid fish in the São Francisco river basin (Gomes & Verani, 2003; Pompeu & Godinho, 2003; Luz et al., 2009; Rocha et al., 2011). Bell & Burt (1991) mentioned that piscivorous fish shelter more endoparasite species than do non-piscivorous fish, because their diet includes smaller species of fish (foragers), which had previously become infected. Smaller fish acted as intermediate or paratenic hosts for parasite groups, especially nematodes in the upper São Francisco river basin (Costa et al., 2011; Albuquerque et al., 2016).

In the present study, as expected, A. lacustris was a piscivorous predator that acted as the definitive host of nine parasite species (Freitascapillaria sp., P. piscicola, Capillariidae gen. sp., Procamallanus (S.) hilarii, Procamallanus (S.) inopinatus, Procamallanus (S.) saofranciscencis, Travassosnema t. paranaensis, C. fischeri and S. rodolphiheringi). However, the parasite community of A. lacustris also included nine helminth species (50%) in the larval stage, some of them with high indexes (abundance and prevalence). This highlights the importance of A. lacustris as an intermediate or paratenic host too.

Piscivorous fish parasitized by helminth larvae can be preyed upon by large vertebrates (birds, mammals and reptiles) that live in or visit the lagoons. This increases the availability of the respective definitive hosts for these helminths and the opportunity that these helminths have for reaching them. However, the invasive parasitic niches (autonomously, or through intermediate or paratenic hosts) need to overlap with the hosts’ niches, for infection to occur (Rolbiecki, 2006). The occurrence of parasite species in the larval stage, proportional to adults and juveniles, is also indicative of this overlap in the lagoon environment.

Dobson & Roberts (1994) confirm earlier studies that suggest that increasing degrees of aggregation are crucial in allowing several species of parasites to coexist in the same species of hosts. In this study, the species Proteocephalidae gen. sp., Contracaecum sp. Type1, Hysterothylacium sp., Spiroxys sp., Procamallanus (S.) hilarii, Procamallanus (S.) inopinatus, Procamallanus (S.) saofranciscencis, Travassosnema t. paranaensis and C. fischeri whose statistical d-tests were significant, showed the typical pattern of aggregated distribution. This tends to increase the stability in the parasite-host relationship to achieve the parasites’ reproductive success, because the higher the level of aggregation of the parasites, the lower the rates of pathogenicity and mortality of the hosts induced by the parasites (Zuben, 1997).

Mature specimens of proteocephalids have been recorded in the following top-of-chain predatory fish species in the upper São Francisco river: Characiformes – Salminus brasiliensis (Cuvier, 1816) (= Salminus franciscanus Lima & Britski, 2007) (Brasil-Sato, 2003); Siluriformes – Pseudoplatystoma corruscans (Spix & Agassiz, 1829) (Brasil-Sato, 2003); and Perciformes – Cichla kelberi Kullander & Ferreira, 2006 (Santos-Clapp & Brasil-Sato, 2014). Plerocercoids have been reported in many fish species in the upper São Francisco river: Characiformes - Prochilodus argenteus Spix & Agassiz, 1829 (Monteiro et al., 2009), P. piraya (Santos-Clapp et al., 2022, in press), Salminus hilarii Valenciennes, 1850 (Duarte et al., 2016) and Tetragonopterus chalceus Spix & Agassiz, 1829 and Triportheus guentheri (Garman, 1890) (Albuquerque et al., 2016); and Siluriformes - Pimelodus maculatus Lacepède, 1803 (Brasil-Sato, 2003) and Pimelodus pohli Ribeiro & Lucena, 2006 (Sabas & Brasil-Sato, 2014). In A. lacustris, which is an expert predator, only the larvae of these proteocephalids formed part of their parasite community, but with elevated indexes, and these were dominant in the communities of six out of these eight lagoons sampled in the upper and middle São Francisco river.

Larval specimens of Rhabdochona (R.) acuminata and Rhabdochona sp. have been registered in the abdominal cavity of some species of fish from the upper São Francisco river (Brasil-Sato, 2003; Brasil-Sato & Santos, 2005; Costa et al., 2011; Santos-Clapp & Brasil-Sato, 2014; Albuquerque et al., 2016). This indicates that this nematode species is not host-specific at this development stage. Occurrence of adult specimens of Rhabdochona (R.) acuminata in A. britskii and A. lacustris from the Três Marias reservoir, in the upper São Francisco river, was registered by Costa et al. (2011) and their absence from the A. lacustris specimens from the lagoons of the present study is indicative that the richness estimated for these lagoon parasite communities may be even higher than what was found in this study. The absence of juvenile or adult nematode specimens may have been due to the small numbers of definitive hosts collected in some lagoons (i.e. Porcos, Feia and Silva Campos), or because the foraging fish in the lagoons were not infected with rhabdochonid larvae at the time of sampling these fish.

In addition to the descriptions and records in the upper São Francisco river, endohelminths parasitizing A. lacustris have also been found in other localities: T. travassosi (Nematoda) in the Tibagi river, state of Paraná (Silva-Souza & Saraiva, 2002); Clinostomum sp. and Rhipidocotyle gibsoni Kohn & Fernandes, 1994 (Digenea), Quadrigyrus torquatus Van Cleave, 1920 (Acanthocephala) and Contracaecum sp. Type1, Contracaecum sp. Type2, Contracaecum sp., Eustrongylides sp. and Procamallanus sp. (Nematoda) in marginal lagoons of the upper Paraná river (Carvalho et al., 2003); Philometridae gen. sp. (Nematoda) (Takemoto et al., 2009); Philonema sp. “A” of Buhrnheim, 1976, and Procamallanus (S.) saofranciscencis (Nematoda) (Eiras et al., 2010); and Austrodiplostomum compactum (Lutz, 1928) (Digenea), Cestoda fam. gen. sp. and Onchoproteocephalidea gen. sp. (Lehun et al., 2020) on the floodplain of the upper Paraná river, which is another natural basin for this host.

Silva-Junior et al. (2011) registered parasitism by Anisakidae larvae in specimens of A. lacustris collected in an environmental protection area of the Curiaú river, Macapá, state of Amapá, along with the representatives of this family (Contracaecum spp. and Hysterothylacium sp.) and Gnathostomatidae (Gnathostoma sp.) that were also collected in the “peixes-cachorros” of the present study. These deserve attention due to the potential zoonotic risk. In the Peixe river, state of São Paulo, Abdallah et al. (2012) recorded Contracaecum sp., Dioctophyme renale (Goeze, 1782), Philometroides caudata Moravec, Scholz & Vivas-Rodríguez, 1995, Procamallanus (S.) inopinatus, Procamallanus (S.) neocaballeroi (Caballero-Deloya, 1977) and Procamallanus (S.) saofranciscencis; while Camargo et al. (2015) registered Ascocotyle sp., Diplostomidae gen. sp. and Sphincterodiplostomum musculosum Dubois, 1936 (Digenea) and Contracaecum sp., P. caudata, Procamallanus (S.) inopinatus and Procamallanus (S.) saofranciscencis (Nematoda). In the Batalha river, state of São Paulo, the following were recorded: A. compactum, Bellumcorpus major Kohn, 1962, R. santanaensis and Rhipidocotyle gibsoni Kohn & Fernandes, 1994 (Digenea) and Capillariidae gen. sp., Contracaecum sp., Goezia brasiliensis Moravec, Kohn & Fernandes, 1994, Guyanema raphiodoni Moravec, Kohn & Fernandes, 1993, T. travassosi, P. caudata, Spiroxys contortus (Rudolphi, 1819), Heliconema sp. and Procamallanus (S.) inopinatus (Nematoda) (Pedro et al., 2016a); Rhipidocotyle santanaensis Lunaschi, 2004 (Digenea) (Pedro et al., 2016b); and Contracaecum sp. as a bioindicator of metal pollution (Leite et al., 2017).

The parasite records relating to A. lacustris mostly include nematode species (larval and adult specimens), followed by digeneans. In the present study, the helminthic community included elevated presence of nematodes (richness and abundance), but regarding digeneans, only one specimen of Clinostomum sp. was collected, from the abdominal cavity of A. lacustris from Grande lagoon. This result, with absence of adult specimens of Digenea and Eucestoda in the parasite community of A. lacustris, reflects the possibility that the food items available, which formed the prey of A. lacustris, did not include gastropod molluscs or aquatic invertebrates as intermediate hosts in the evolutionary cycles of these parasites. It may even reflect a possibility that infective forms of these species evolve to use definitive hosts other than “peixes-cachorros” (e.g., Proteocephalidae gen. sp.).

The highest number of helminth species (ten species) was found in the parasite communities of Batatas and Feia lagoons (upper São Francisco river basin), in which the richness of the infracommunities ranged from one to six species among the twenty-seven infected fish and from three to six species among the seven infected fish, respectively. Another community that stood out was Silva Campos lagoon (upper São Francisco river basin), with eight species of parasites in only three infected fish, in which the infracommunity richness ranged from four to five parasite species per host. In two lagoons, Feia and Silva Campos, the number of fish examined was low (seven and three fish, respectively) and the fish were larger than those in the other lagoons (average total length = 24.8 and 25.3 cm, respectively). The parasite community of A. lacustris from Mocambo lagoon (middle São Francisco river basin) showed the highest richness of the parasite infracommunity (one to seven helminth species per fish) and presented nine helminth species.

The parasite communities of A. lacustris from these lagoons in the upper and middle São Francisco river are structured by constant species that are shared with high parasite indexes. Travassosnema travassosi is a species whose adult specimens are well correlated with acestrorhynchid hosts (Cypriniformes): in the São Francisco river, state of Minas Gerais (Costa et al., 1991); in the Tibagi river, state of Paraná (Silva-Souza & Saraiva, 2002); and in the Batalha river, state of São Paulo (Pedro et al., 2016a).

In addition, it was possible to detect rare species (e.g., Brevimulticaecum sp. and Gnathostoma sp.) in the communities from the lagoons along the basin, even with the sampling limitation presented in this study. Batatas and Feia (upper São Francisco river lagoons) and Mocambo (middle São Francisco river lagoon) showed the highest richness of the parasite communities of A. lacustris. Because of the inherent characteristics of the locations of the Feia and Mocambo lagoons, they receive less input of water from the São Francisco river basin. Thus, water inflow to them is rarer than to the other lagoons. This regional characteristic, together with the lower water input, alters the density of the populations of organisms that survive in its environment and consequently the composition of the parasite fauna and its indexes. Feia lagoon not only had the largest number of species registered (ten), but also had the largest number of adult helminth species (six). As all organisms involved in the cycles of these parasites had long periods of exposure to them in the same area, transmission of some species of parasites was favored. Interaction with and predation of smaller fish by the “peixes-cachorros” must have facilitated occurrence of the rare parasite species detected in this lagoon, such as the three capillariid nematode species found (juveniles and adults), which had never been found in fish from the upper São Francisco river. These rare species contributed to the increase in parasite richness. The presence of juvenile and adult helminth species in the communities of these lagoons also suggest that dynamism of accumulation of parasites exists, with ongoing infections and reinfections. This would be dependent on the life cycles of the parasites (in many cases unknown), the trophic mechanisms and the particularities of the lagoons, which need to be studied in greater detail.

These lagoons have been recognized for their importance as fundamental “nurseries” for reproduction of many fish species (Sato & Godinho, 2003), including the foraging fish that A. lacustris feeds on (Pompeu & Godinho, 2003). They are complex ecosystems for which investigation of parasitism assists in understanding the supporting biotic interactions that exist in them.

Conclusions

This was the first study on the parasites of A. lacustris in the São Francisco river and was a pioneer regarding studies on fish parasites from lagoons in this hydrographic basin. The composition of the parasite community of these piscivorous fish, collected from eight lagoons in the upper and middle São Francisco river basin, comprised eighteen species of helminths (of seven families, including Anisakidae and Gnathostomatidae, which are important due to the zoonotic risk that they pose), from heteroxenous cycles that were established through predation of intermediate hosts by A. lacustris. There was a minimum of three shared species (Proteocephalidae gen. sp., Contracaecum sp. Type1 and Travassosnema t. paranaensis) between the parasite communities in these lagoons, which all had high parasite indexes. The correlation between adult Travassosnema t. paranaensis helminths and acestrorhynchids can be highlighted.

Nine parasite species were recorded for the first time in A. lacustris: Proteocephalidae gen. sp., Brevimulticaecum sp., Gnathostoma sp., Freitascapillaria sp., P. piscicola, Capillariidae gen. sp., Procamallanus (S.) hilarii, C. fischeri and S. rodolphiheringi. The geographical distribution of six nematode species: three capillariid species, Gnathostoma sp., and Procamallanus (S.) hilarii (with low parasite indexes) and Travassosnema t. paranaensis, was expanded to the São Francisco river basin through the present study.

The parasite community of A. lacustris from lagoons bordering the upper and middle São Francisco river basin reflects occurrences of many biological interactions and several parasites’ life cycles. The lagoons of this important Brazilian hydrographic basin maintain part of the biodiversity of the Cerrado biome, and efforts are needed to expand the knowledge about them. Based on the current survey, it can be estimated that the parasite richness of A. lacustris from the lagoons of the upper and middle São Francisco river basin is even higher than what was recorded in this study.

Acknowledgements

The authors are grateful to Dr Yoshimi Sato (1st CIT/CODEVASF, Três Marias, MG) and Dr Mario Tallarico de Miranda (IBAMA, MG) for material support; to Dr Marcelo Knoff, and Dr Osvaldo Takeshi Oyakawa, the curators of the Coleção Helmintológica do Instituto Oswaldo Cruz (CHIOC, RJ), and Museu de Zoologia da Universidade de São Paulo (MZUSP, SP) for deposition of parasites and fish voucher specimens, respectively. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 (RD – Doctoral Scholarship).

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Publication Dates

• Publication in this collection
  20 Apr 2022
• Date of issue
  2022

History

• Received
  10 Jan 2022
• Accepted
  22 Mar 2022