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Ectoparasite crustaceans of ten fish species from the upper Araguari River in northern Brazil

Abstract

Fish parasites are an important part of aquatic biodiversity and knowing these species and their interactions with their hosts helps in monitoring the aquatic biota. The present study investigated the ectoparasite crustacean fauna of ten fish species from the upper Araguari River, in the state of Amapá, northern Brazil. A total of 508 fish were collected and analyzed from July to November 2014, of which 82.6% (109) were parasitized by one or more crustacean ectoparasite species. In the ten host fish species, a total of 308 ectoparasite specimens were collected, from 12 taxa, such as Argulus multicolor Stekhoven, 1937, Argulus spinulosus Silva, 1980, Argulus sp.1, Argulus sp.2, Argulus sp.3, Dipteropeltis sp., Dipteropeltis hirundo Calman, 1912, Dolops bidentata Bouvier, 1899, Dolops striata Bouvier, 1899 (Argulidae), Braga fluviatilis Richardson, 1911, Braga amapaensis Thatcher, 1996 (Cymothoidae) and Excorallana berbicensis Boone, 1918 (Corallanidae). Higher levels of prevalence and abundance were recorded for Hoplias aimara (Valenciennes, 1847) and Tometes trilobatus Valenciennes, 1850, respectively. These ectoparasites were found in the fins, integument, mouth, and anus of the host fish. Argulus sp.2 and D. bidentata were the most abundant parasites (65.1%), and had the highest species richness. This study registered 36 novel host-parasite interactions, and thus represents a new record for all host species here examined.

Key words
Branchiura; isopoda; freshwater fish; infestation; parasites

INTRODUCTION

The state of Amapá has two great basins, the Amazon River basin system and the North Atlantic Ocean basin, which have high levels of connectivity through lakes, rivers channels and floodplains, with singular physical and chemical parameters pivotal for the maintenance of the fish community (Hoorn 1994HOORN C. 1994. An environmental reconstruction of the palaeo-Amazon River system (Middle-Late Miocene, NW Amazonia). Palaeogeogr Palaeoclimatol Palaeoecol 112: 187-238., Latrubesse et al. 2010LATRUBESSE EM, COZZUOL M, SILVA-CAMINHA SAF, RIGSBY CA, ASSY ML & JARAMILL C. 2010. The Late Miocene paleogeography of the Amazon Basin and the evolution of the Amazon River system. Earth Sci Rev 99: 99-124., Cavalcanti et al. 2013CAVALCANTI AC, CUNHA HFA & PINHEIRO LAR. 2013. Modelagem e simulaçao do escoamento e sispersão azonais de agentes passivos no Rio Araguari AP: Cenários para o AHE Ferreira Gomes-I- Amapá/Brasil. RBRH – Rev Bras Recur Hídricos 18: 67-85., Hurd et al. 2016HURD LE, SOUSA RGC, SIQUEIRA-SOUZA FK, COOPER GJ, KAHN JR & FREITAS CEC. 2016. Amazon floodplain fish communities : Habitat connectivity and conservation in a rapidly deteriorating environment. Biol Conserv 195: 118-127., Santos et al. 2018SANTOS ES, LOPES PPP, PEREIRA HH, PEREIRA HHS, NASCIMENTO OO, RENNIE CD, STERNBERG LSLO & CUNHA AC. 2018. The impact of channel capture on estuarine hydro-morphodynamics and water quality in the Amazon delta. Sci Total Environ 624: 887-899.). The Araguari River basin is the main basin in the state of Amapá, and acts as an estuarine drainage network between the Amazon River and North Atlantic Ocean, with an area of 38,000 km2. The river rises from its headwaters in the Serra do Tumucumaque Mountains of the Guiana Shields, and discharges into the Atlantic Ocean throughout the Amazon delta. Along its course, it crosses the Amapá National Forest, the Amapá State Forest, the Lago Piratuba (Piratuba Lake) Biological Reserve (REBio), the municipalities of Porto Grande and Ferreira Gomes, includes three hydropower plants (Coaracy Nunes, Ferreira Gomes and Cachoeira Caldeirão), and drains almost all of its water volume into the Amazon River and a small portion into the Atlantic Ocean (Santos et al. 2018SANTOS ES, LOPES PPP, PEREIRA HH, PEREIRA HHS, NASCIMENTO OO, RENNIE CD, STERNBERG LSLO & CUNHA AC. 2018. The impact of channel capture on estuarine hydro-morphodynamics and water quality in the Amazon delta. Sci Total Environ 624: 887-899.). Moreover, is characterized by rocky outcrops and small waterfalls, precluding its navigation, which is restricted to small boats used by the riverine population in their daily activities.

Anthropogenic factors, such as the building of hydroelectrical dams in the Araguari River basin, have caused long-term alterations to the course flow and water quality, binding the natural patterns of this aquatic ecosystem, as well as the native vegetation cover, river discharge, turbidity and oxygen level of water, and the submersion of microhabitats, resulting in changes in ecosystems, which can lead to alterations in the diversity and complex network of parasite-host interaction (Fearnside 2001FEARNSIDE PM. 2001. Environmental impacts of Brazil’s Tucuruí Dam: Unlearned lessons forh hydroelectric development in amazonia. Environ Manag 27: 377-396., Thatcher 2006THATCHER VE. 2006. Amazon fish parasites. 2nd ed, Sofia: Pensoft Publishers, 508 p., Morley 2007MORLEY NJ. 2007. Anthropogenic effects of reservoir construction on the parasite fauna of aquatic wildlife. Ecohealth 4: 374-383., Cavalcanti et al. 2013CAVALCANTI AC, CUNHA HFA & PINHEIRO LAR. 2013. Modelagem e simulaçao do escoamento e sispersão azonais de agentes passivos no Rio Araguari AP: Cenários para o AHE Ferreira Gomes-I- Amapá/Brasil. RBRH – Rev Bras Recur Hídricos 18: 67-85., Santos et al. 2014SANTOS ES, CUNHA AC & CUNHA EDS. 2014. Análise Espaço-sazonal da Qualidade da Água na Zona Flúvio-Marinha do Rio Araguari-Amazônia Oriental-Brasil. Rev Bras Rec Hidric 19(3): 215-226., 2018, Sá-Oliveira et al. 2015SÁ-OLIVEIRA JC, HAWES JE, ISAAC-NAHUM VJ & PERES CA. 2015. Upstream and downstream responses of fish assemblages to an eastern Amazonian hydroelectric dam. Freshwater Biol 60: 2037-2050.). Among parasites of fish, crustacean species comprise three main taxa: Branchiura, Copepoda, and Isopoda. In general, these parasitic crustaceans have been reported on all the external body surfaces of the host fish, i.e., the integument, opercula, fins, eyes, oral cavity, gills, and/or anus (Thatcher 2006THATCHER VE. 2006. Amazon fish parasites. 2nd ed, Sofia: Pensoft Publishers, 508 p., Lima et al. 2013LIMA JTAX, COSTA E FS, NASCIMENTO WS & CHELLAPPA S. 2013. Tendências evolutivas do parasito isópodo Livoneca redmanni Leach, 1818 (Crustacea, Isopoda, Cymothoidae) em duas espécies de peixes marinhos do Rio Grande do Norte, Brasil. Biota Amaz 3(1): 66-73., Gentil-Vasconcelos & Tavares-Dias 2015GENTIL-VASCONCELOS HC & TAVARES-DIAS M. 2015. First study on infestation of Excorallana berbicensis (Isopoda: Corallanidae) on six fishes in a reservoir in Brazilian Amazon during dry and rainy seasons. Lat Am J Aquat Res 43(5): 936-943., 2016, Oliveira et al. 2019). Fish are important hosts in the biological cycle of crustacean ectoparasites (Tavares-Dias et al. 2015TAVARES-DIAS M, DIAS-JÚNIOR MBF, FLORENTINO AC, SILVA LMA & CUNHA AC. 2015. Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Braz J Vet Parasitol 24(2): 136-147., Oliveira et al. 2017OLIVEIRA MSB, CORRÊA LL, FERREIRA DO, NEVES LR & TAVARES-DIAS M. 2017. Records of new localities and hosts for crustacean parasites in fish from the eastern Amazon in northern Brazil. J Paras Dis 41(2): 565-570.). Parasitic crustaceans are widely distributed in freshwater watersheds, and often affect host biology and fitness, playing a crucial role in the regulation of the fish community (Alberto et al. 2009ALBERTO RMF, MACIEL PC & ARAÚJO PB. 2009. Infestation by the freshwater cymothoid Artystone trysibia Schioedte (Crustacea, Isopoda): Parasite and host behaviour. J Nat Hist 43: 47-56., Tavares-Dias et al. 2014TAVARES-DIAS M, ARAÚJO CSO, BARROS MS & VIANA GM. 2014. New Hosts and distribution records of Braga patagonica, a parasite Cymothoidae of fishes from the Amazon. Braz J Aquat Sci Technol 18: 91-97.).

Few studies on parasite crustaceans of fish in the Araguari River basin have been carried out. Those that have, in a reservoir area of the Coaracy Nunes hydropower plant, reported the occurrence of Excorallana berbicensis Boone, 1918; Argulus chicomendesi Malta & Varella, 2000 and Ergasilus turucuyus Malta & Varella, 1996 in Psectrogaster falcata Eigenmann & Eigenmann, 1889 (Curimatidae); Ageneiosus ucayalensis Castelnau, 1855 (Auchenipteridae); Acestrorhynchus falcirostris Cuvier, 1819 (Acestrorhynchidae); Hemiodus unimaculatus Bloch, 1794 (Hemiodontidae); Serrasalmus gibbus Castelnau, 1855 (Serrasalmidae) and Geophagus proximus Castelnau, 1855 (Cichlidae) (Gentil-Vasconcelos & Tavares-Dias 2015GENTIL-VASCONCELOS HC & TAVARES-DIAS M. 2015. First study on infestation of Excorallana berbicensis (Isopoda: Corallanidae) on six fishes in a reservoir in Brazilian Amazon during dry and rainy seasons. Lat Am J Aquat Res 43(5): 936-943., Gentil-Vasconcelos & Tavares-Dias 2016GENTIL-VASCONCELOS HC & TAVARES-DIAS M. 2016. Host-parasite interaction between crustaceans of six fish species from the Brazilian Amazon. Acta Sci Biol Sci 38(1): 113-123.). However, no other study has been carried out of fish in the Araguari River basin, despite the importance of knowledge about the diversity of parasitic crustaceans in host fish. Thus, the aim of the present study was to investigate parasite crustaceans in ten fish species from the Araguari River, in the state of Amapá, northern Brazil.

MATERIALS AND METHODS

Fish and collection site

The fish were collected in the upper stretch of the Araguari River, between the municipalities of Serra do Navio and Ferreira, in the state of Amapá, in northern Brazil, at geographic coordinates 1°4’26.11”N 51°59’1.94”W; 1°7’16.50”N 51°58’59.64”W; 1°12’43.59”N 52°0’8.70”W; 1°13’50.97”N 51°59’59.53”W; 1°16’52.75”N 51°59’47.51”W and 1°18’8.54”N 51°58’52.28”W (Figure 1). The fish were collected in July and November 2014. For fish collection, gill nets of different measures and hook lines were used. Afterwards, the weight (g) and total length (cm) were measured for each fish.

Figure 1
Geographic location of fish collection sites in the upper Araguari River, in the state of Amapá, northern Brazil.

Collection procedures and analysis of parasites

Immediately after capture, each fish was transferred to a tray and the sites of infection, such as the mouth, gills, opercula, tegument, fins, and anus were analyzed to verify the presence of ectoparasite crustaceans. The crustaceans collected were then fixed in ethyl alcohol (70%) for 24 hours and preserved in ethyl alcohol (70%) with glycerin (10%). Parasites were clarified for analysis of morphological structures using potassium hydroxide 5%, as recommended by Oliveira et al. (2021)OLIVEIRA MSB, CORRÊA LL, ADRIANO EA & TAVARES-DIAS M. 2021. Integrative taxonomy of a new species of Therodamas (Ergasilidae) infecting the Amazonian freshwater fish Leporinus fasciatus (Anostomidae). Parasitol Res 120(9): 3137-3147.. Small parasites (Branchiura) were clarified whole and mounted on temporary slides containing glycerin for morphological visualization. Larger parasites (Isopoda) were dissected and parts of taxonomic interest were clarified in potassium hydroxide 5% and temporary slides were mounted. The parasites identification was carried out according to Van Name (1925)VAN NAME BWG. 1925. The isopods of Kartabo. Bartica district, British Guiana. Zoologica 5: 461-503., Lemos de Castro (1959)LEMOS DE CASTRO A. 1959. Sobre as espécies sul-americanas do gênero Braga Schioedte et Meinert, 1881 (Isopoda: Cymothoidae). Arch Mus Nac Rio de Janeiro 59: 69-77., Silva (1980)SILVA NMM. 1980. Argulus spinulosus sp. n. (Branchiura, Argulidae), em peixes de água doce do Rio Grande do Sul, Brasil. Iheringia, Série Zoologia (56): 15-23., Malta (1982)MALTA JCO. 1982. Os argulídeos (Crustacea: Branchiura) da Amazônia Brasileira. Aspectos da ecologia de Dolops discoidalis Bouvier, 1899 e Dolops bidentata Bouvier, 1899. (1). Acta Amaz 12(3): 521-528., Lemos de Castro (1985)LEMOS DE CASTRO A. 1985. Branchiura. In: Schaden R (Ed), Manual de Identificação de Invertebrados Límnicos do Brasil, Brasília: CNPq/MCT, BR, p. 1-23., Lemos de Castro & Loyola-Silva (1985)LEMOS DE CASTRO A & LOYOLA-SILVA J. 1985. Isopoda. In: Schaden R (Ed), Manual de Identificação de Invertebrados Límnicos do Brasil, Brasília: CNPq/MCT, p. 1-20. and Thatcher (2006)THATCHER VE. 2006. Amazon fish parasites. 2nd ed, Sofia: Pensoft Publishers, 508 p.. The parasitological descriptors of prevalence, mean abundance and mean intensity were measured as recommended by Bush et al. (1997)BUSH AO, LAFFERTY KD, LOTZ JM & SHOSTAK AW. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83(4): 575-583.. Abundance data were subjected to normality analysis using the Shapiro-Wilk test from the “RVAideMemoire” package (Herve 2023HERVE M. 2023. RVAideMemoire: Testing and plotting procedures for biostatistics. R package version 0.9-82-2[online] 2023 [cited 2023 Jul 18]. Available from: https://CRAN.R-project.org/package=RVAideMemoire.
https://CRAN.R-project.org/package=RVAid...
), which showed a non-normal distribution. Spearman’s correlation was used to assess the influence of fish length and weight on parasite abundance, using the tidyverse package (Wickham et al. 2019WICKHAM H ET AL. 2019. Welcome to the Tidyverse. J Open Source Softw 4(43): 1686.) in R software (R Core Team 2021). For this analysis, we considered three scenarios: (1) Isopoda abundance; (2) abundance of Branchiura and (3) the sum of the abundance of Isopoda and Branchiura, in order to evaluate the behavior of the results.

Ethics statement

Fish collection was authorized by ICMBio (Nº 42203-1), and the procedures involving animals were approved by the Ethics Committee on Animal Use of the Fish Biology Laboratory of the Federal University of Amapá (UNIFAP) approved the procedures involving animals (Protocol number 47757715.5.0000.0003).

RESULTS

A total of 558 specimens of fish distributed in 26 species were collected and analyzed (Table I). Of these, only 109 fish of 10 species were parasitized by crustacean ectoparasites (Tables I and II). Overall, 11.9% of Acestrorhynchus microlepis (Jardine, 1841), 14.7% of Ageneiosus inermis (Linnaeus, 1766), 4.6% of Boulengerella cuvieri, 3.7% of Charax sp., 14.7% of H. aimara, 6.4% of M. asterias, 9.2% of M. ternetzi, 8.2% of P. rhomboidalis, 11.0% of S. rhombeus and 15.6% of T. trilobatus were infested by one or more species of parasite crustaceans. Of the 109 fish specimens examined, 82.6% (n = 90) were infested by Argulus multicolor Stekhoven, 1937; Argulus spinulosus Silva, 1980; Argulus sp.1; Argulus sp.2; Argulus sp.3; Dolops bidentata Bouvier, 1899; Dolops striata Bouvier, 1899; Dipteropeltis hirundo Calman, 1912; Dipteropeltis sp. (Argulidae), Braga fluviatilis Richardson, 1911; Braga amapaensis Thatcher, 1996 (Cymothoidae) and E. berbicensis (Corallanidae). A total of 36 host-parasite associations were recorded. High prevalence, mean intensity and mean abundance values were reported for D. bidentata and E. berbicensis (Table I).

Table I
Fish species parasitized and not parasitized by Branchiura and Isopoda, collected from the upper Araguari River, Amapá, Brazil. N = Number of fish collected.
Table II
Ectoparasite crustaceans of ten fish species collected in the upper Araguari River, in eastern Amazon, northern Brazil. P (%): Prevalence, MA: Mean abundance, MI: Mean intensity, TNP: Total number of parasites.

Argulidae presented the highest abundance and species richness (Figure 2). Among the host species, A. microlepis presented the highest species richness of the parasite crustaceans, followed by H. aimara (Figure 3).

Figure 2
Total number of parasitic crustaceans collected from ten fish species from the upper Araguari River, in eastern Amazon, northern Brazil, according to parasite family.
Figure 3
Parasite species richness in ten fish species from the upper Araguari River, in the eastern Amazon, northern Brazil.

There was positive correlation of branchiuran abundance with length and weight of the hosts (Figure 4). However, there was no correlation of isopod abundance with weight and length (Figure 5). There was also positive correlation of branchiuran + isopod with length and weight of the hosts (Figure 6).

Figure 4
Spearman correlation to evaluate the relationship between Branchiura abundance and host length and weight.
Figure 5
Spearman correlation to evaluate the relationship between Isopoda abundance and host length and weight.
Figure 6
Spearman correlation to evaluate the relationship between Branchiura + Isopoda abundance and host length and weight.

DISCUSSION

Studies surveying the fauna of parasitic crustaceans and description of new species have revealed a richness of parasite crustaceans in the Amazon biome (Oliveira et al. 2017OLIVEIRA MSB, CORRÊA LL, FERREIRA DO, NEVES LR & TAVARES-DIAS M. 2017. Records of new localities and hosts for crustacean parasites in fish from the eastern Amazon in northern Brazil. J Paras Dis 41(2): 565-570., Gaboardi et al. 2023GABOARDI LM, REEVES LE, MOREY GAM, STANTON DL & CARNEY RM. 2023. A new species of the fish louse genus Dipteropeltis Calman, 1912 (Crustacea: Branchiura) from Peru. Zootaxa 5315(2): 101-121.). On the body surfaces of ten host fish species from the Araguari River we found ten species of Argulidae and three species of Isopoda, thus contributing 36 new records of host-parasite interactions. However, on the body surfaces of six fish species from an Araguari River reservoir, one species of Isopoda and two species of Argulidae have been reported (Vasconcelos & Tavares-Dias 2015).

Low (A. microlepis, A. inermis, B. cuvieri, M. asterias and S. rhombeus) to moderate (H. aimara and T. trilobatus) infestation of E. berbicensis occurred, with this parasite the most frequently occurring in the host fish studied herein. In the region of the present study, this species of isopod was previously reported in A. falcirostris, H. unimaculatus, P. falcata and S. gibbus, A. ucayalensis and G. proximus, with low infestation levels (Vasconcelos & Tavares-Dias 2016). Therefore, this parasite has no host specificity. Excorallana species are temporary parasites found in cryptic habitats and eventually parasitize fish species when emerging from these habitats to feed (Delaney 1989DELANEY PM. 1989. Phylogeny and Biogeography of the Marine Isopod Family Corallanidae (Crustacea, Isopoda, Flabellifera). LACM 409: 1-75.). Hence, it is believed that E. berbicensis is found in host fish when it performs vertical migrations in the water column (Gentil-Vasconcelos & Tavares-Dias 2015GENTIL-VASCONCELOS HC & TAVARES-DIAS M. 2015. First study on infestation of Excorallana berbicensis (Isopoda: Corallanidae) on six fishes in a reservoir in Brazilian Amazon during dry and rainy seasons. Lat Am J Aquat Res 43(5): 936-943.).

Cymothoidae species are obligate parasites from freshwater, brackish and marine teleost and chondrichthyan fish (Smit et al. 2014SMIT NJ, BRUCE NL & HADFIELD KA. 2014. Global diversity of fish parasitic isopod crustaceans of the family Cymothoidae. Int J Parasitol Parasites Wildl 3(2): 188-197.) and possess 46 genera and 386 valid species (WoRMS 2023WORMS. 2023. World Register of Marine Species. http://www.marinespecies.org (accessed 27 September 2023).
http://www.marinespecies.org...
). Thatcher (1996)THATCHER VE. 1996. Braga amapaensis n. sp. (Isopoda: Cymothoidae) a mouth cavity parasite of the Amazonian fish, Acestrorhynchus guyanensis Menezes, with a redefinition of the genus Braga. Amaz Oecologia Reg Syst Fluminis Amaz 14(1/2): 121-129. described B. amapaensis in A. microlepis from the state of Amapá; however, since then, no record of this parasite species has been carried out, until now. Therefore, this second report of B. amapaensis shows a high prevalence and low abundance and represents the first study on parasitic infestation, which was similar to that reported for other Cymothoidae species (Oda et al. 2015ODA FH, GRAÇA RJ, TENCATT LFC, TAVARES LER, FROEHLICH O & TAKEMOTO RM. 2015. The poorly known Riggia acuticaudata (Crustacea: Isopoda) parasitizing Ancistrus sp. (Siluriformes: Loricariidae) from the Paraguay River Basin, Brazil, with comments on its reproductive biology. Comp Parasitol 82(1): 25-28., Tavares-Dias et al. 2015TAVARES-DIAS M, DIAS-JÚNIOR MBF, FLORENTINO AC, SILVA LMA & CUNHA AC. 2015. Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Braz J Vet Parasitol 24(2): 136-147., Oliveira et al. 2017OLIVEIRA MSB, CORRÊA LL, FERREIRA DO, NEVES LR & TAVARES-DIAS M. 2017. Records of new localities and hosts for crustacean parasites in fish from the eastern Amazon in northern Brazil. J Paras Dis 41(2): 565-570.). Therefore, it seems that B. amapaensis has a high host specificity, emphasizing the need for further studies to elucidate this issue. Moreover, we found low infestation of B. fluviatilis on the body surface of M. ternetzi, M. asterias, S. rhombeus and Charax sp., but with a higher prevalence in M. ternetzi. Low infestation by B. fluviatilis has been reported for Leporinus friderici Bloch, 1794 from the Jari River basin, in the state of Amapá (Oliveira et al. 2017OLIVEIRA MSB, CORRÊA LL, FERREIRA DO, NEVES LR & TAVARES-DIAS M. 2017. Records of new localities and hosts for crustacean parasites in fish from the eastern Amazon in northern Brazil. J Paras Dis 41(2): 565-570.). B. fluviatilis has been also reported for Pimelodidae gen. sp.; Serrasalmus spilopleura Kner, 1858 (Hamann 1998HAMANN MI. 1998. Aspectos ecológicos de la relácion parasitaria entre juveniles de Braga fluviatilis Richardson, 1911 (Crustacea, Cymothoidae) y Serrasalmus spilopleura Kner, 1860 (Pisces, Characidae) en poblaciones naturales del Nordeste Argentino. Physis 55: 15-22.), Loricariichthys anus Valenciennes, 1835, Salminus brasiliensis Cuvier, 1816 (Lemos de Castro 1959LEMOS DE CASTRO A. 1959. Sobre as espécies sul-americanas do gênero Braga Schioedte et Meinert, 1881 (Isopoda: Cymothoidae). Arch Mus Nac Rio de Janeiro 59: 69-77.), C. temensis (Brasil-Lima & Barros 1998BRASIL-LIMA IM & BARROS CML. 1998. Malacostraca - Peracarida. Freshwater Isopoda. Flabellifera and Asellota. In: Young PS (Ed), Catalogue of Crustacea of Brazil. Rio de Janeiro: Museu Nacional, p. 645-651.), Cichlasoma sp., Hypostomus sp., Salminus spp. and Sorubim lima Bloch & Schneider, 1801 (Thatcher 2006THATCHER VE. 2006. Amazon fish parasites. 2nd ed, Sofia: Pensoft Publishers, 508 p.). However, this was the first report of B. fluviatilis for M. ternetzi, M. asterias, S. rhombeus and Charax sp.

Argulidae is the richest and most abundant taxon of parasitic crustaceans, and this may be associated to the lifestyle of these ectoparasite crustaceans. This pattern has also been reported in previous studies in fish from central Amazon (Malta 1984MALTA JCO. 1984. Os peixes de um lago de várzea da Amazônia Central (Lago Janauacá, Rio Solimões) e suas relações com os crustáceos ectoparasitas (Branchiura: Argulidae). Acta Amaz 14: 355-372.) and eastern Amazon (Oliveira et al. 2017OLIVEIRA MSB, CORRÊA LL, FERREIRA DO, NEVES LR & TAVARES-DIAS M. 2017. Records of new localities and hosts for crustacean parasites in fish from the eastern Amazon in northern Brazil. J Paras Dis 41(2): 565-570., Neves & Tavares-Dias 2019NEVES LR & TAVARES-DIAS M. 2019. Low levels of crustacean parasite infestation in fish species from the Matapi River in the state of Amapá, Brazil. Braz J Vet Parasitol 28(3): 493-498.). Among argulids, low to moderate infestations by D. bidentata occurred on the body surface of A. microlepis, B. cuvieri, Charax sp., H. aimara, M. asterias, M. ternetzi, P. rhomboidalis, S. rhombeus and T. trilobatus, all new hosts for this argulid species. Dolops bidentata is known to parasitize the body surface of Anostomidae, Serrasalmidae, Prochilodontidae and Cichlidae fish species (Malta 1982MALTA JCO. 1982. Os argulídeos (Crustacea: Branchiura) da Amazônia Brasileira. Aspectos da ecologia de Dolops discoidalis Bouvier, 1899 e Dolops bidentata Bouvier, 1899. (1). Acta Amaz 12(3): 521-528., Luque et al. 2013LUQUE JL, VIEIRA FM, TAKEMOTO RM, PAVANELLI GC & EIRAS JC. 2013. Checklist of Crustacea parasitizing fishes from Brazil. Check List 9(6): 1449-1470.). Therefore, D. bidentata has no host-specificity, as well as other fish lice species found herein. Moreover, D. striata occurred only in A. microlepis, H. aimara and Hoplias aimara, and had a low infestation level. This argulid species has also been reported infesting other species of fish with this same pattern of infestation on the body surface, due to lack of host-specificity (Malta & Varella 1983MALTA JCO & VARELLA A. 1983. Os argulíddeos (Crustacea: Branchiura) da Amazônia brasileira 3. Aspectos da ecologia de Dolops striata Bouvier, 1899 e Dolops carvalhoi Castro, 1949. Acta Amaz 13: 299-306., Malta 1984MALTA JCO. 1984. Os peixes de um lago de várzea da Amazônia Central (Lago Janauacá, Rio Solimões) e suas relações com os crustáceos ectoparasitas (Branchiura: Argulidae). Acta Amaz 14: 355-372., Luque et al. 2013LUQUE JL, VIEIRA FM, TAKEMOTO RM, PAVANELLI GC & EIRAS JC. 2013. Checklist of Crustacea parasitizing fishes from Brazil. Check List 9(6): 1449-1470., Pereira et al. 2017). Argulus sp. infested only A. microlepis and B. cuvieri, while Argulus sp.2 infested A. microlepis, Charax sp., A. inermis and H. aimara, and Argulus sp.3 infested only M. asterias.

The Dipteropeltis genus has only three valid species, and is found exclusively in Neotropical region, namely, Dipteropeltis campanaformis Neethling, Malta & Avenant-Oldewage (Neethling et al. 2014NEETHLING LAM, MALTA JCO & AVENANT-OLDEWAGE A. 2014. Additional morphological information on Dipteropeltis hirundo Calman, 1912, and a description of Dipteropeltis campanaformis n. sp. (Crustacea: Branchiura) from two characiform benthopelagic fish hosts from two Northern rivers of the Brazilian Amazon. Zootaxa 3755(2): 179-193.), Dipteropeltis longicaudatus Gaboardi, Reeves, Morey, Stanton & Carney, 2023 (Gaboardi et al. 2023GABOARDI LM, REEVES LE, MOREY GAM, STANTON DL & CARNEY RM. 2023. A new species of the fish louse genus Dipteropeltis Calman, 1912 (Crustacea: Branchiura) from Peru. Zootaxa 5315(2): 101-121.) and D. hirundo (Calman, 1912). Dipteropeltis hirundo occurred only in Charax sp. and with low infestation and was a new host for parasite species. A new species of Dipteropeltis sp. (which will be described in another study) was found infesting H. aimara, T. trilobatus and M. ternetzi. Low infestation levels of D. hirundo have also been reported for Acestrorhynchus sp.; Astyanax fasciatus Cuvier, 1819; Brycon melanopterus Cope, 1872; Luciopimelodus pati Valenciennes, 1835; Mylossoma aureum Spix & Agassiz, 1829; S. brasiliensis; Salminus franciscanus Lima & Britski, 2007 and Pygocentrus piraya Cuvier 1819, which were the only host fish known for this argulid species (Lemos de Castro 1985LEMOS DE CASTRO A. 1985. Branchiura. In: Schaden R (Ed), Manual de Identificação de Invertebrados Límnicos do Brasil, Brasília: CNPq/MCT, BR, p. 1-23., Luque et al. 2013LUQUE JL, VIEIRA FM, TAKEMOTO RM, PAVANELLI GC & EIRAS JC. 2013. Checklist of Crustacea parasitizing fishes from Brazil. Check List 9(6): 1449-1470.). Carvalho 1941CARVALHO JP. 1941. Sobre Dipteropeltis hirundo Calman, Crustáceo (Branchiura) parasito de peixes d’água doce. Bol Fac Filos Ciênc Let Univ São Paulo Zool 5(5): 265-277. reports D. hirundo in two species of lambarí, the yellowtail (Tetragonopterus aureus) and the redtail (Tetragonopterus rutilus). However, Tetragonopterus aureus was possibly misnamed by this author, and based on reclassifications of the group, it is possible that the hosts mentioned are actually Astyanax lacustris (yellow-tailed lambari) and Astyanax rutilus (red-tailed lambari). Therefore, the present study enlarged the host fish species for D. hirundo.

Aspects inherent to the host, such as size and weight, are important variables that explain part of the abundance of parasites in host fish population (Poulin 2007POULIN R. 2007. Evolutionary Ecology of Parasites. 2nd ed. New Jersey: Princeton University Press, 465 p., Poulin & Leung 2011POULIN R & LEUNG TLF. 2011. Body size, trophic level, and the use of fish as transmission routes by parasites. Oecologia 166(3): 731-738., Baia et al. 2018BAIA RRJ, FLORENTINO AC, SILVA LMA & TAVARES-DIAS M. 2018. Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region. Acta Parasitol 63(2): 304-316.). Our results clearly show this, since there was a positive correlation between the abundance of crustacean ectoparasites and the length and weight of the host fish. Therefore, fish size plays an important role in the abundance of parasites in a host population, and as the fish grows, either in length and/or weight, it becomes a potential target for the colonization of new crustacean parasites. This is probably because larger fish have a greater surface area to establish a larger population of these ectoparasites. We observe positive correlation between the abundance of branchiurans and the size host fish, similar correlation was reported for ectoparasites in Amazonian fish (Baia et al. 2018BAIA RRJ, FLORENTINO AC, SILVA LMA & TAVARES-DIAS M. 2018. Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region. Acta Parasitol 63(2): 304-316.).

In conclusion, 308 parasite crustaceans were found on the body surfaces of the ten host fish species examined, being argulids the richest taxa in the community of these ectoparasites. Furthermore, most fish examined had a low abundance of ectoparasites, except for A. microlepis and H. aimara, which were the most parasitized hosts. Lastly, the present study reports new hosts for parasite crustacean species.

ACKNOWLEDGMENTS

The Fundação de Amparo à Pesquisa do Amapá (FAPEAP) for its financial support under the project Monitoramento da Atividade Pesqueira no Médio Rio Araguari (Process number 004/2013 and 005/2014). The authors thank Conservação Internacional do Brazil (CI), Walmart Brazil and the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), for their support under the Biology and Ethnoecology of Ichthyofauna in the Amapá National Forest (FLONA) project. To the Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (CNPq), for the productivity grant to Tavares-Dias, M. (Grant 303013/2015-0) and the Financiadora de Estudos e Projetos (FINEP) (Grant 0117005600). To the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for granting a doctoral scholarship to Oliveira, MSB (Process number 88882.430002/2019-01), to the Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (CNPq) for granting a master degree scholarship to Esteves-Silva, PH. The authors thank Msc. Raissa Alves Gonçalves for the immense contribution during field activities on the Araguari River.

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Publication Dates

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

History

  • Received
    5 Dec 2023
  • Accepted
    4 Mar 2024
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