Isopod parasites of Pygocentrus piraya (Characiformes: Serrasalmidae) in the lower São Francisco River, Brazil

Abstract

Isopods of the suborder Cymothoida include ectoparasite species that cause physical damage and affect the development of the host by feeding on blood and tissues. On fishes, these parasites attach themselves to the skin, fins, gills, and oral cavity using claws on articulated legs. The ability to remain hidden in cavities even after the fish is caught enables isopods to be transported to new areas along with the host, making these parasites potential co-invaders. Understanding the role and environmental impact of parasites is essential, although research on parasitism in the context of biological invasions lags in comparison to general research on such invasions. Previous records indicate only two species of parasitic isopods in the São Francisco River basin. However, the present study reports the first record of two other species (Braga patagonica and Braga nasuta) on Pygocentrus piraya and in the basin itself. This demonstrates a lack of knowledge regarding fish parasites in the region, despite the presence of other parasites. Collaborations with research groups conducting fish sampling in the basin can contribute to expanding knowledge on these parasites and the training of human resources in fish parasitology. The present study provides important information on the presence of unidentified parasitic isopods on fishes in the São Francisco River basin, underscoring the need for further studies and expanding the geographic distribution of these parasites, as well as the host list for these isopods.

Keywords:
Braga; Cymothoidae; ectoparasites; Neotropical region; freshwater fishes

INTRODUCTION

Isopods of the family Cymothoidae Leach, 1814 correspond to a group of obligate ectoparasitic crustaceans currently represented by 40 genera and 380 species (Smit et al., 2014). These parasites usually occur on marine and freshwater fishes and are associated with the gill cavity (sometimes several specimens simultaneously), mouth, body surface, fins, and even holes in tissues of the host (Thatcher, 2006; Smit et al., 2014). They feed on blood, mucus, and epithelial tissues by attaching to the body of the host with the claws and using parts of the oral apparatus. This behavior can cause physical damage and compromise host health (Thatcher, 2006). In addition, these parasites are protandrous hermaphrodites, in which males become females (Costa and Chellappa, 2010; Eiras et al., 2010; Fadel et al., 2020).

The greatest diversity of Cymothoidae occurs in the tropics, with a well-documented distribution of marine parasites (Searle and Richardson, 1905; Brusca, 1981; Bruce, 1897; Kensley and Schotte, 1989; Silva and Souza-Filho, 2017; Ravichandran et al., 2019; Alves et al., 2019; Purivirojkul and Songsuk, 2020; Ribeiro et al., 2021). However, studies on these parasites in freshwater ecosystems are incipient and usually involve the description of species and new records (Smit et al., 2014; Tavares-Dias et al., 2014; Virgilio et al., 2020). In Brazil, filling gaps in knowledge is a key point for understanding distribution patterns of isopod species in freshwater environments, as the country has the largest hydrographic network in the world and is one of the most important countries in terms of freshwater fish diversity (Dagosta and de Pinna, 2019).

Among freshwater parasitic isopods in Brazil, the genus Braga Schioedte and Meinert, 1881 has eight valid species (Thatcher et al. 2009), most of which are associated with the tongue, gills, and body surface of the host. Species of the genus Braga are characterized by a symmetrical body, anterior region slightly immersed in pereonite 1, all prehensile pereopods with robust claw-shaped dactyls, a wider than long pleotelson, and multilaminate pleopods 2-5 (Thatcher, 2006; Thatcher et al., 2009). Although this is a well-studied group, gaps in knowledge remain regarding the distribution of this genus in Brazilian watersheds. The aim of the present study is to report, for the first time, the occurrence of two species of Braga, Braga patagonica Schioedte and Meinert, 1884 and Braga nasuta Schioedte and Meinert, 1881, on the freshwater piranha Pygocentrus piraya (Cuvier), expanding the geographic distribution of isopods in Brazilian freshwater environments.

MATERIAL AND METHODS

Parasitized individuals of P. piraya were sampled in two environments in the lower São Francisco River (Fig. 1). Sampling in the lotic section was conducted in the main channel of the river (10°13’2.25’’S 36°46’1.67’’W; 10°10’51.50’’S 36°50’37.20’’W), with pH 7.64 ( 0.09, electrical conductivity 85.9 ( 0.4 (S cm^-1, total dissolved solids 56.0 ( 0.01 mg L^-1, and dissolved oxygen 7.48 ( 0.43 mg L^-1. The abiotic variables were different in the location corresponding to Lagoa da Marituba (10°18’17.47’’S 36°23’43.16’’W) and reflected the lentic environment, with slightly acidic pH (6.83 ( 0.05) likely due to the presence of humic acids and the decomposition of organic matter, which may contribute to higher values of electrical conductivity (226.4 ( 0.1 (S cm^-1) total dissolved solids (114.9 ( 0.1 mg L^-1) and lower concentrations of dissolved oxygen (2.55 ( 0.05 mg L^-1).

Figure 1.
Location of the São Francisco River basin (SFB) in Brazil, with details of records of Braga nasuta and Braga patagonica found parasitizing Pygocentrus piraya in the lower portion of the river.

Fishes were collected between 2022 and 2023, using gill nets set up at dusk and removed at dawn, with an average deployment time of 14h. The individuals were removed from the net and transported to the laboratory for biometry. Total length (TL), standard length (SL), and body weight (BW) were measured. Ectoparasites were macroscopically located and removed from the hosts using fine-tipped tweezers, placed into Petri dishes, and cleaned with jets of water. Representative specimens of taxa were deposited in the Zoological Collection of Universidade Federal de Sergipe (CZUFS), São Cristóvão, Sergipe, Brazil.

Isopods were identified through morphological comparisons obtained from the scientific literature (Thatcher, 1995; 2006; Tavares-Dias et al., 2014; Narciso et al., 2019) combined with observations of the body, morphological attributes of the appendages, and other taxonomic structures. The specimens were then illustrated using a mixed technique with colored pencils, colored brush pens, and India ink, based on Alves et al. (2022). The figure boards were assembled and treated using the Paint and GIMP version 2.10.34 software.

Ecological descriptors of isopod parasites were calculated based on Bush et al. (1997): prevalence (P), intensity (I), mean intensity (Im), and mean abundance (Am).

SYSTEMATICS

Nine individuals of P. piraya were collected, three of which were parasitized. Five were collected at 10°13’2.25”S 36°46’1.67”W, one of which was parasitized; two were collected at 10°10’51.50”S 36°50’37.20”W, one of which was parasitized; two were collected at 10°18’17.47”S 36°23’43.16”W, and one was parasitized. The parasitized fish measured 20.5 cm (± 2.12) in length and weighed 171g (± 113.71). The isopods were identified as belonging to the genus Braga Schioedte and Meinert, 1881. The diagnoses of the genus and species are as follows:

Order Isopoda Latreille, 1816

Suborder Cymothoida Wägele, 1989

Superfamily Cymothooidea Leach, 1814

Family Cymothoidae Leach, 1814

Genus Braga Schioedte and Meinert, 1881

Diagnosis (male and female): Body longer than wide, symmetrical. Cephalon not immersed in pereonite 1; forehead obtuse; antennal bases well separated. Pereonite 1 larger than pereonite 7; compact coxal plates, not extending posteriorly to the respective pereonites. Relatively long pereopods with 7^th pair longer than others, all ending in stout prehensile, claw-shaped dactyls. Mandible subrectangular, without cutting or incisor process. Pleon slightly immersed in pereonite 7; pleonites usually with lateral projections; pleopods multilaminate - pleopod 1 bilaminate, 2 quadrilaminate, 3-5 trilaminate. Pleotelson keelless shield-shaped; uropods short with endopods shorter than exopods.

Braga patagonica Schioedte and Meinert, 1884

(Fig. 2)

Material examined. 2 females and 2 males (catalogue number: CZUFS CRU-00373).

Supplementary description. Females (Fig. 2A ): oval body; light milky color. Cephalon triangular, anterior long and rounded; scattered and discrete chromatophores; relatively small eyes. Antennule with 7 articles and antenna with 8 articles (Fig. 2D , E). Pereon broad, being longest and widest at pereonite 5. Pleon narrow. Pleotelson prominent, wider than long. Pleopod 1 bilaminate, 2 quadrilaminate, 3-5 trilaminate; exopod longer than endopod. Uropod shorter than pleotelson.

Males (Fig. 2B , C). Smaller than females. Milky brownish coloration, with chromatophores forming patterned dotted dark brown pigmentation arranged at lateral and posterior ends of pereonites and in central strip extending from anterior to posterior region. Head with well-developed eyes. Antennule with 7 articles. Antenna bases well separated, with 8 articles. Seen from side, body practically straight, with subtle depression in pereonite 5.

Figure 2.
Braga patagonica (CZUFS CRU-00373) detected on Pygocentrus piraya. A, Female habitus in dorsal view; B, C, male, habitus in dorsal and lateral views, respectively, scale: 1 mm; D, E, antennule and antenna, respectively, scale: 0.5 mm.

Host/site of infection. Pygocentrus piraya, body surface.

Place of registration. Main channel of the São Francisco River between the municipalities of Porto Real do Colégio (state of Alagoas) and Propriá (state of Sergipe).

Ecological descriptors. P = 22.22%; Im = 2.00; Am = 0.44 ± 1.01

Braga nasuta Schioedte and Meinert, 1881

(Fig. 3)

Material examined. One male collected (catalogue number: CZUFS CRU-00374).

Figure 3.
Braga nasuta (CZUFS CRU-00374) detected on Pygocentrus piraya; A, B, Male, habitus in dorsal and lateral views, respectively, scale: 1 mm; C, D, antennule and antenna, respectively, arrows point to the basal article, scale: 0.5 mm; E, pleopods 1-5 (2-5 are multilaminate), scale: 0.5 mm.

Supplementary description. Male: Yellowish coloration with chromatophores forming a patterned dotted dark pigmentation in distinct longitudinal bands along the body (Fig. 3A ). Laterally, body curved, with concave shape (Fig. 3B ); compact coxal plates not extending beyond pereonites. Cephalon anteriorly truncated, with well-developed eyes. Antennule with 7 articles. Antennal bases well separated, with 8 articles (Fig. 3C , D). Pereopods ending in prehensile dactyls (hooks); some chromatophores also found on some pereopods; pereopod 7 with shorter dactyl than others. Pleotelson triangular, ending in small point. Pleopods short (Fig. 3E ), rounded. Pleopod 1 bilaminate, 2 quadrilaminate, 3-5 trilaminate; uropod extending beyond apex of pleotelson, with exopod slightly longer than endopod. Male appendix flattened, tapering; small lateral and near medial peduncular lobes on all pleopods; anterior accessory gill lamellae present on pleopods 2-5.

Host/site of infection. Pygocentrus piraya, body surface.

Place of registration. Lagoa da Marituba, municipality of Penedo (state of Alagoas).

Ecological descriptors. P = 11.1%; Im = 1.00; Am = 0.11 ± 0.33.

DISCUSSION

The studied specimens of B. patagonica and B. nasuta had similar morphologies to specimens reported by Thatcher (1995; 2006), Tavares-Dias et al. (2014), and Narciso et al. (2019). Although pigmentation is not a taxonomic characteristic, the difference in pigmentation between males and females is notable. According to Trilles (1991), this difference in pigmentation is related to the habitat occupied by isopods. Specimens that parasitize the buccal or branchial cavity, preferably occupied by females, are whitish or weakly pigmented. In contrast, species that parasitize the surface of the host, preferentially occupied by males, have more intense or stronger pigmentation.

The findings of the present study expand the distribution of the genus Braga and contribute to biogeographical knowledge of the species. The ability to parasitize species from different taxonomic groups attests to the low specificity, as past records indicate parasitized fishes from different families of Characiformes, Siluriformes, Cichliformes, and Osteoglossiformes, such as Arapaima gigas (Schinz) (Tab. 1). This fact seems very opportune because of the great diversity of fishes in the Neotropical region (Dagosta and de Pinna, 2019), which may be directly associated with the wide geographical distribution of the parasites.

Table 1.
Occurrence records of Braga patagonica and Braga nasuta in Brazilian hydrographic basins.

Parasite	Host	Order/Family	Hydrographic basin	Reference
Braga patagonica	Pygocentrus nattereri Kner	Characiformes/Serrasalmidae	Tocantins basin	Carvalho et al. (2004)
	Colossoma macropomum (Cuvier)	Characiformes/Serrasalmidae	Amazon, High São Francisco, Paraná and Southeast Atlantic basins	Luque et al. (2013)
	Hoplias malabaricus (Bloch)	Characiformes/Erythrinidae
	Salminus hilarii (Valenciennes)	Characiformes/Erythrinidae
	Colossoma macropomum	Characiformes/Serrasalmidae	Amazon basin	Tavares-Dias et al. (2014)
	Pygogentrus nattereri	Characiformes/Serrasalmidae
	Mylossoma duriventre (Cuvier)	Characiformes/Serrasalmidae
	Serrasalmus rhombeus (Linnaeus)	Characiformes/Serrasalmidae
	Brycon amazonicus (Spix and Agassiz)	Characiformes/Bryconidae
	Hydrolycus scomberoides (Cuvier)	Characiformes/Cynodontidae
	Chaetobranchopsis orbicularis (Steindachner)	Cichliformes/Cichlidae
	Oreochromis niloticus (Linnaeus)	Cichliformes/Cichlidae	Amazon basin	Bittencourt et al. (2014)
	Colossoma macropomum	Characiformes/Serrasalmidae	Pisciculture	Dias et al. (2015)
	Peprilus paru (Linnaeus)	Scombriformes/Stromateidae	Amazon basin	das Chagas et al. (2015)
	Acestrorhynchus falcatus (Bloch)	Characiformes/Acestrorhynchidae	Amazon basin	Hoshino et al. (2016)
	Curimata incompta Vari	Characiformes/Curimatidae	Amazon basin	Neves et al. (2016)
	Odontesthes bonariensis (Valenciennes)	Atheriniformes/Atherinopsidae	Guaíba, Mirim-São Gonçalo and Southeast Atlantic basins	Huanto (2017)
	Serrasalmus altispinis Merckx, Jégu and Santos	Characiformes/Serrasalmidae	Amazon basin	Oliveira et al. (2017)
	Chaetobranchus flavescens Heckel	Cichliformes/Cichlidae	Amazon basin	Tavares-Dias et al. (2018)
	Pellona castelnaeana Valenciennes	Clupeiformes/Pristigateridae	Amazon basin	Souza (2018)
	Pygocentrus nattereri (Kner)	Characiformes/Serrasalmidae	Amazon basin	Souza et al. (2018)
	Serrasalmus elongatus (Kner)	Characiformes/Serrasalmidae
	Brycon amazonicus (Spix and Agassiz)	Characiformes/Bryconidae
	Triportheus albus Cope	Characiformes/Triportheidae
	Mylesinus sp.	Characiformes/Serrasalmidae
	Colossoma macropomum	Characiformes/Serrasalmidae	Amazon basin	Gonçalves et al. (2018)
	Leporinus fasciatus (Bloch)	Characiformes/Anostomidae	Amazon basin	Neves and Tavares-Dias (2019)
	Propimelodus eigenmanni (Van der Stigchel)	Siluriformes/Pimelodidae
	Phractocephalus hemioliopterusBloch and Schneider	Siluriformes/Pimelodidae	Amazon basin	Oliveira et al. (2019)
	Pimelodella humeralisSlobodian, Akama and Dutra	Siluriformes/Heptapteridae	Amazon basin	Virgilio et al. (2020)
	Hoplias malabaricus	Characiformes/Erythrinidae	Western Northeast Atlantic Basin	Ribeiro and Mugnai (2020)
	Serrasalmus sp.	Characiformes/Serrasalmidae
Braga nasuta	Hypostomus sp.	Siluriformes/Loricariidae	Amazon High São Francisco Paraná and Southeast Atlantic basins	Luque et al. (2013)
	Arapaima gigas (Schinz)	Osteoglossiformes/Arapaimidae	Pisciculture	Jesus et al. (2017)
	Hyphessobrycon eques (Steindachner)	Characiformes/Characidae	Paraná basin	Narciso et al. (2019)
	Serrasalmus sp.	Characiformes/Serrasalmidae	Western Northeast Atlantic Basin	Ribeiro and Mugnai (2020)

Isopods of the suborder Cymothoida are ectoparasites that can cause physical harm and affect the development of the host, feeding on blood and tissues when attached to the integument, fins, gills, and oral cavity by claws at the ends of their articulated legs (Izdebska and Rolbiecki, 2010). Owing to their fixation method and the possibility of remaining hidden (e.g., oral and gill cavities) even after the fish has been caught, these parasites can be transported to new areas along with the host. In the context of biological invasions, this is an important factor to consider, as they can be co-invaders and benefit from the lack of host specificity to continue their cycle in other species in the receiving river basin (Lymbery et al., 2014). Poulin (2017) stated that research on parasitism in the context of biological invasions is not keeping pace with research on biological invasions in general and it is crucial to reverse this situation, as understanding the role and environmental impact of parasites is fundamental.

Previous studies have indicated the presence of only two species of isopods in the São Francisco River basin: Braga fluviatilis Richardson, 1911 on P. piraya and Amphira branchialis Thatcher, 1993 on the serrasalmid Pygocentrus nattereri Kner (Santos, 2008; Vital et al., 2011). However, B. patagonica and B. nasuta have not previously been reported, even in large studies. Although parasitic intensity was low, the presence of adult females of B. patagonica with a developed marsupium on P. piraya suggests that this fish is a suitable host for parasitism. Thus, the information presented in this study corresponds to the first record of these isopods on P. piraya and for the São Francisco River basin. This indicates that there is still a lack of knowledge regarding the study of fish parasites in the river basin, as previous records show the occurrence of other parasites (e.g., Nematoda, Cestoidea, and Eupentasomida) (Santos et al., 2009; Santos-Clapp et al., 2022; Duarte et al., 2022). Collaborations between research groups that carry out sampling of fishes throughout the basin can contribute to the expansion of knowledge on these organisms as well as the training of human resources in fish parasitology.

This study provides important information about the presence of previously unidentified isopod parasites on fishes of the São Francisco River basin, underscoring the need for further studies in this area. Low levels of infection were observed on P. piraya, represented by only one specimen of B. nasuta. The isopod B. patagonica had a higher infection rate compared to B. nasuta on P. piraya. The occurrence of these isopods in the lower São Francisco River in northeastern Brazil expands the geographic distribution of these two species and places P. piraya in the list of hosts for these two ectoparasites.

ACKNOWLEDGMENTS

The authors thank Universidade Federal de Sergipe, Companhia de Desenvolvimento dos Vales do São Francisco e Parnaíba and Instituto de Meio Ambiente de Alagoas for support. We also thank Instituto Chico Mendes de Conservação da Biodiversidade and Instituto de Meio Ambiente de Alagoas for the collection permits FAPEAL (Process number APQ2022021000055).

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• Zoobank:

  http://zoobank.org/urn:lsid:zoobank.org:pub:5ECC3D20-B88B-4D36-9123-5DA8C375B35F

ADDITIONAL INFORMATION AND DECLARATIONS

• Consent for publication

  All authors declare that they have reviewed the content of the manuscript and gave their consent to submit the document

• Data availability

  All study data are included in the article

• Funding and grant disclosures

  We also thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq #461008/2014-9) and Fundação de Amparo à Pesquisa do Estado de Alagoas (FAPEAL #APQ2022021000055) for funding. MFGB received a research grant from CNPq (312779/2021-6)

• Study association

  This study was developed in collaboration between the Laboratório de Estudos em Genética de Doenças Infecciosas e Parasitárias, situado and the Laboratório de Ictiologia (both located at the Universidade Federal de Sergipe), the Universidade Federal de Alagoas and the Companhia de Desenvolvimento dos Vales do São Francisco e Parnaíba (CODEVASF)

• Study permits

  Instituto Chico Mendes de Conservação da Biodiversidade (#45700-1, #45700-2); Instituto de Meio Ambiente de Alagoas (IMA#2023.20031249053)

Edited by

Editor-in-chief:

Christopher Tudge

Associate Editor:

Brenda Doti

Data availability

All study data are included in the article

Publication Dates

• Publication in this collection
  08 July 2024
• Date of issue
  2024

History

• Received
  08 Nov 2023
• Accepted
  04 Jan 2024