Este trabajo describe los metazoarios parásitos de Acestrorhynchus falcatus (Bloch, 1794) (Characiformes: Acestrorhynchidae) capturados en lagos inundables de la Amazonía brasileña. Los lagos estudiados fueron: Baixio, Preto, São Tomé, Ananá, Araçá y Maracá, localizados entre las ciudades de Manaus y Coari en la Amazonía Central. Sesenta y seis A. falcatus fueron colectados y examinados en marzo, junio, septiembre y diciembre de 2013. Fueron encontrados 263 especímenes de parásitos pertenecientes a 11 especies. Del total de parásitos, 166 especímenes (63,12%) fueron endoparásitos y 97 especímenes (36,88%) ectoparásitos. Siete especies son citadas por primera vez: Quadrigyrus torquatus Van Cleave, 1920 (Acanthocephala); Anisakis sp. (Nematoda), Pseudoproleptus sp. (Nematoda); Travasosnema travassosi paranaensis Costa, Moreira & Oliveira, 1991 (Nematoda); Amplexibranchius bryconis Thatcher & Paredes, 1985 (Copepoda); Acusicola pellonidis Thatcher & Boeger, 1983 (Copepoda) y Argulus amazonicus Malta & Silva, 1986 (Brachiura). Acestrorhynchus falcatus tiene una posición intermediaria en la red trófica de los lagos estudiados, siendo un hospedero intermediario, paraténico y definitivo de diferentes especies de parásitos

de Oliveira Malta, José Celso

Murrieta Morey, Germán Augusto

Spanish

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 ISSN Versión impresa 2218-6425    ISSN Versión Electrónica 1995-1043Neotropical Helminthology, 2018, 12(2), jul-dic:147-152.ORIGINAL ARTICLE / ARTÍCULO ORIGINALMETAZOAN PARASITES OF ACESTRORHYNCHUS FALCATUS (CHARACIFORMES: ACESTRORHYNCHIDAE) FROM FLOODPLAIN LAKES OF THE BRAZILIAN AMAZONMETAZOARIOS PARÁSITOS DE ACESTRORHYNCHUS FALCATUS (CHARACIFORMES: ACESTRORHYNCHIDAE) COLECTADOS EN LAGOS INUNDABLES DE LA AMAZONÍA BRASILEÑA1Instituto de Investigaciones de la Amazonía Peruana. Centro de Investigaciones Fernando Alcántara (CIFAB - IIAP). Laboratorio de Parasitología y Sanidad Acuícola. Carretera Iquitos-Nauta, Km. 4.5, San Juan Bautista, Iquitos – Perú.2Instituto Nacional de Pesquisas da Amazônia (INPA, Manaus, Brasil). Av. André Araújo, 2936 – Petrópolis, Manaus, Amazonas, Brasil 69067-375. Programa de Pós-graduação em Biología de Água Doce e Pesca Interior-BADPI*Corresponding author: E-mail: germantiss1106@gmail.com1,* 2Germán Augusto Murrieta Morey  & José Celso de Oliveira MaltaABSTRACTKeywords: Acestrorhynchus falcatus – Amazonia – ectoparasites – endoparasites – fish – host This work describes the metazoan parasites of Acestrorhynchus falcatus (Bloch, 1794) (Characiformes: Acestrorhynchidae) caught in floodplain lakes of the Brazilian Amazon. The studied lakes were: Baixio, Preto, São Tomé, Ananá, Araçá and Maracá, located between the cities of Manaus and Coari in Central Amazonia. Sixty-six specimens of A. falcatus were collected and examined in March, June, September, and December 2013. A total of 263 specimens of parasites belonging to 11 species were found. These included 166 endoparasitic specimens (63.12%) and 97 ectoparasitic specimens (36.88%). Seven species are reported for the first time: Quadrigyrus torquatus Van Cleave, 1920 (Acanthocephala); Anisakis sp. (Nematoda), Pseudoproleptus sp. (Nematoda); Travasosnema travassosi paranaensis Costa, Moreira & Oliveira, 1991 (Nematoda); Amplexibranchius bryconis Thatcher & Paredes, 1985 (Copepoda); Acusicola pellonidis Thatcher & Boeger, 1983 (Copepoda) and Argulus amazonicus Malta & Silva, 1986 (Brachiura). Acestrorhynchus falcatus has an intermediate position in the trophic web of the studied floodplain lakes, being intermediate, paratenic and definitive host of different parasite species.Neotropical Helminthology 147Volume12,Number2(jul-dec2018)ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)Lima-PerúVersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043Species of Acestrorhynchus are benthopelagic fish, exclusively of freshwater that are distributed in rivers and lakes of South America. Eleven species occur in the Amazonas and Orinoco River basins, and in rivers of Guianas. Two species are restricted to the River São Francisco in the River Paraná. One species occurs in the River Paraná, Uruguay and Paraguay River basins (Toledo-Piza, 2007; Pretti et al., 2009).Acestrorhynchus falcatus occurs in the Amazonas and Orinoco River basins and in rivers of Suriname and French Guyana. This species can be differentiated from other Acestrorhynchus by presenting a humeral spot next to the operculum and next to the caudal fin. It can reach 30 cm of length, is sedentary, diurnal and piscivorous, but younger specimens can also feed on crustaceans (Soares et al., 2008; Pretti et al., 2009).There are few studies on the fauna of parasites of A. falcatus. In the Amazon Region, there are non-studies concerning to parasites of this fish species. Thus, the present study pretends to identify the metazoan parasites of A. falcatus collected in floodplain lakes of the Brazilian Amazon. Sixty-six A. falcatus (Figure 1) with mean 17.82 ± 2.33 cm standard length and mean 86.45 ± 43.54 g weight were collected between March and December 2013 from six floodplain lakes of the Brazilian Amazon: Lake Baixio (03°17'27, 2''S/ 60°04'29,6''W) at the city of Iranduba, Lake Preto (03°21'17, 1''S/ 60°37'28,6''W) at Manacapurú; Lake Ananá (03°53'54,8''S/ 61°40'18,4''W) at Anori; Lake Araçá (S03°45' 04,3" S/ 62°21' 25,9" W) at Codajás and Lake Maracá (03°50'32,8''S/ 62°34'32,4''W) at Coari and Lake São Tomé (03°49' 39,0"S/ 61°25' 24,6" W).Fish were caught using 100 mm between adjacent nodes-meshed, 20 m long x 2 m high gillnets. Posteriorly the fishes were quickly immersed in 75 -1mg clove oil·L  solution and euthanized (CONCEA, 2013). In the field, fishes were measured and weighed. The gills, operculum and fins were examined for the presence of ectoparasites. Gills and nostrils were removed and preserved in 5% formalin; the gastrointestinal tract was preserved in 70% ethanol for posterior analyses at the laboratory of Fish Parasitology (LPP) in the National Institute of Amazonian Research (INPA).148Neotropical Helminthology, 2018, 12(2), jul-dicRESUMENPalabras clave: Acestrorhynchus falcatus – Amazonia – ectoparásitos – endoparásitos – hospedero – pecesEste trabajo describe los metazoarios parásitos de Acestrorhynchus falcatus (Bloch, 1794) (Characiformes: Acestrorhynchidae) capturados en lagos inundables de la Amazonía brasileña. Los lagos estudiados fueron: Baixio, Preto, São Tomé, Ananá, Araçá y Maracá, localizados entre las ciudades de Manaus y Coari en la Amazonía Central. Sesenta y seis A. falcatus fueron colectados y examinados en marzo, junio, septiembre y diciembre de 2013. Fueron encontrados 263 especímenes de parásitos pertenecientes a 11 especies. Del total de parásitos, 166 especímenes (63,12%) fueron endoparásitos y 97 especímenes (36,88%) ectoparásitos. Siete especies son citadas por primera vez: Quadrigyrus torquatus Van Cleave, 1920 (Acanthocephala); Anisakis sp. (Nematoda), Pseudoproleptus sp. (Nematoda); Travasosnema travassosi paranaensis Costa, Moreira & Oliveira, 1991 (Nematoda); Amplexibranchius bryconis Thatcher & Paredes, 1985 (Copepoda); Acusicola pellonidis Thatcher & Boeger, 1983 (Copepoda) y Argulus amazonicus Malta & Silva, 1986 (Brachiura). Acestrorhynchus falcatus tiene una posición intermediaria en la red trófica de los lagos estudiados, siendo un hospedero intermediario, paraténico y definitivo de diferentes especies de parásitos.Murrieta Morey & Oliveira MaltaINTRODUCTION MATERIAL AND METHODSAt the laboratory, the parasites found were processed according to Amato et al. (1991).  Specimens were studied using a light microscope Zeiss Axioscope 2. Voucher specimens were deposited at the invertebrate collection of the National Institute of Amazon Research (INPA), Manaus, Brazil. The ecological terminology applied to parasites followed Bush et al. (1997). A number of 263 specimens of parasites belonging to 11 species were found parasitizing A. falcatus (Table 1). From the total number of parasites, 166 specimens (63.12%) were endoparasites and 97 specimens (36.88%) were ectoparasites. Seven parasites species were in the stage of adult and the other were immatures. The highest prevalence was for Diaphorocleidus sp. (32.14%), the highest mean intensity was for Anisakidae larvae (Table 1).149RESULTSNeotropical Helminthology, 2018, 12(2), jul-dicTable 1. Metazoan parasites in Acestrorhynchus falcatus  (Bloch, 1794) from oodplain lakes of the Brazilian Amazon. P% = prevalence, N = number of parasites, I = intensity of infection, mI = mean intensity, mA = mean abundance.Parasites Accession No P% N I mI mAMONOGENOIDEA             Diaphorocleidus sp. INPA - 643 32.14 80 1-15 4.44 ± 3.91 1.42 ± 3.03 DIGENEA             Clinostomum marginatum INPA - 690 7.14 8 1-3 2 ± 0.70 0.14 ± 0.54 ACANTOCEPHALA             Quadrigyrus torquatus INPA - 55 7.14 8 1-2 2,00 0.14 ± 0.51 NEMATODA             Anisakis sp. INPA - 87 5.36 30 1-3 10 ± 5.62 0.53 ± 2.37 Pseudoproleptus sp. INPA - 88 19.64 6 1-5 0.54 ± 0.81 0.10 ± 0.48 Procamallanus (Spirocamallanus) inopinatus INPA - 89 8.93 19 1-16 3.8 ± 1.21 0.33 ± 0.86 Travassosnema travassosi paranaensis  INPA - 90 3.57 6 2 3,00 0.10 ± 0.44 Larvas Anisakidae INPA - 91 25.00 89 1-23 6.35 ± 6.89 1.58 ± 4.37 COPEPODA             Amplexibranchius bryconis INPA - 2339 10.71 11 1-3 1.83 ± 1.11 0.19 ± 0.68 Acusicola pellonidis INPA - 2340 7.14 5 1-2 1.25 ± 0.43 0.08 ± 0.33 BRANCHIURA             Argulus amazonicus INPA - 2341 1.79 1 1 1,00 0,02 DISCUSSIONSpecies of Diaphorocleidus were found in Characidae species: Bryconops affinis (Günther, 1864), Astyanax bimaculatus (Linnaeus, 1758), Hemigrammus microstomus Durbin, 1918 and Gymnocorymbus ternetzi (Boulenger, 1895) (Jogunoori et al., 2004). For Acestrorhynchidae Diaphorocleidus sp. was found in Acestrorhynchus lacustris (Lütken, 1875) from São Paulo (Camargo et al., 2015), in A. falcirostris Cuvier, 1818 and A. falcatus from Amapá (Hoshino et al., 2016). In the present study, Diaphorocleidus sp. was found parasitizing A. falcatus, representing the first occurrence of a Diaphorocleidus species in the Brazilian Amazon.Clinostomum marginatum (Rudolphi, 1819) was cited in A. falcirostris and A. falcatus collected in Amapá, Brazil (Hoshino et al., 2016). In Brazilian floodplain lakes C. marginatum was found parasitizing different organs of A. falcirostris (Dumbo, 2014). In the present study, metacercariae of C. marginatum were found in the gills and intestine of A. falcatus. Metazoan parasites of Serrasalmus altispinis150For A. falcatus, the acanthocephalans Palliolisentis polyonca Schmidt & Hugghins, 1973 (Thatcher, 2006) and Neoechinorhynchus pterodoridis Thatcher, 1981 (Hoshino et al., 2016) were found parasitizing the intestine. For species of A c e s t ro rh y n c h u s ,  t h e  a c a n t h o c e p h a l a n Quadrigyrus torquatus Van Cleave, 1920 was cited parasitizing A. lacustris (Carvalho et al., 2003) and A. falcirostris (Dumbo, 2014). In the present study Q. torquatus was found in the intestine of A. falcatus, being the first record of this parasite in this fish species. Additionally, the number of known host for this acanthocephalan is expanded to a new host.In floodplain lakes of the Brazilian Amazon, A n i s a k i s  s p . ,  P.  ( S . )  i n o p i n a t u s  a n d Pseudoproleptus sp. were found in Pygocentrus nattereri Kner, 1858 (Morais, 2011); Anisakis sp. and P. (S.) inopinatus in C. monoculus (Santana, 2013);  Anisakis  sp. ,  P. (S.)  inopinatus , Pseudoproleptus sp.  and Travassosnema travassosi paranaensi in A. falcirostris (Dumbo, 2014) and P. (S.) inopinatus and Pseudoproleptus sp. in Astronotus ocellatus (Agassiz, 1831) (Attroch, 2016). In the present study all these nematodes were found parasitizing different organs of A. falcatus. The only species specific for Acestrorhynchus is T. travassosi paranaensi that was found in A. lacustris (Moravec et al., 1993). In the present study, Anisakis sp., Pseudoproleptus sp. and T. travassosi paranaensis are cited for the first time in A. falcatus.The feeding habits of fish are the main factor that determines the composition of endoparasite species, because they are transmitted through the trophic web in predator-prey relationships (Marcogliese, 2002). In the present study additionally to the adult and immature nematodes quote above, numerous Anisakidae larvae were found. In this way, A. falcatus has an intermediate position in the trophic web of the studied floodplain lakes, being intermediate, paratenic and definitive host of different endoparasites.For Acestrorhynchus the copepod parasite species known are: Ergasilus turucuyus Malta & Varella, 1996 from A. falcatus, A. falcirostris and A. microlepis (Shomburgk, 1841) (Malta & Varella, 1996); E. turucuyus, Amplexibranchius bryconis, Acusicola pellonidis and Miracetyma piraya Malta, 1993 from A. falcirostris (Dumbo, 2014). In the present study, A. bryconis and A. pellonidis are cited for the first time in A. falcatus.For Acestrorhynchus, Dolops bidentata Bouvier, 1899,  D. geayi  Bouvier,  1897,  Argulus chicomendesi Malta & Varella, 2000 and A. amazonicus Malta & Silva, 1986 are cited parasitizing A. falcirostris (Matta & Silva, 1986; Dumbo, 2014). In the present study, A. amazonicus Figure 1. Lateral view of Acestrorhynchus falcatus (Bloch, 1794) captured in oodplain lakes of the Brazilian Amazon Neotropical Helminthology, 2018, 12(2), jul-dic Murrieta Morey & Oliveira Malta151was found in A. falcatus, representing the first occurrence of this parasite in this fish species.GAMM received a scholarship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES (Brazil).ACKNOWLEDGEMENTSAmato, JFR, Boeger, WA & Amato, SB. 1991. Protocolos para laboratório coleta e processamento de parasitas do pescado. Imprensa Universitária, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brasil. 81 pp.Atroch, FMPB. 2016. Metazoários parasitos de Astronotus ocellatus (Agassiz, 1831) e Astronotus crassipinnis (Heckel, 1840) (Perciformes: Cichlidae) em lagos de várzea na Amazônia, Amazonas, Brasil. Tese de Mestrado, INPA, Manaus, Brasil. 92 pp.Bush, AO, Lafferty, KD, Lotz, JM & Shostak, AW. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of parasitology, vol. 83, pp. 575-583.Camargo, A, Pedro, NHO, Pelegrini, LS, de Azevedo, RK, da Silva & RJ, Abdallah, VD. 2015. Parasites of Acestrorhynchus lacustris (Lütken, 1875) (Characiformes: Acestrorhynchidae) collected from the Peixe River, southeast Brazil. Acta Scientiarum. Biological Sciences, vol. 37, pp. 231-237.CONCEA, 2013. Diretrizes da Prática de Eutanásia do Conselho Nacional de Controle de Experimentação Animal - CONCEA .  Ministério da Ciência,  Tecnologia e Inovação, Brasília, DF. 54 pp.Dumbo, JC. 2014. Espécies de metazoários parasitos de Acestrorhynchus falcirostris ( C u v i e r,  1 8 1 9 )  ( C h a r a c i f o r m e s :  Acestrorhynchidae) de lagos de várzea da Amazônia Central. Tese de Mestrado, BIBLIOGRAPHIC REFERENCESINPA, Manaus. 150 pp.Hoshino, MD, Neves, LR & Tavares-Dias, M. 2016. Parasite communities of the predatory fish, Acestrorhynchus falcatus and Acestrorhynchus falcirostris, living in sympatry in Brazilian Amazon. Revista Brasileira de Parasitologia Veterinária, vol. 25, pp. 207-216. Jogunoori, W, Kritsky, DC & Venkatanarasaiah, J. 2004. Neotropical Monogenoidea. 46. Three new species from the gills of introduced aquarium fishes in India, the proposal  of  Heterotylus  ng.  and Diaphorocleidus ng., and the reassignment of some previously described species of Urocleidoides Mizelle & Price, 1964 (Polyonchoinea:  Dactylogyridae) .  Systematic Parasitology, vol. 58, pp. 115-124.Malta, JCO & Silva, EM. 1986. Argulus amazonicus n. sp. crustáceo parasito de p e i x e s  d a  A m a z ô n i a  B r a s i l e i r a  (Branchiura: Argulidae), Amazoniana, vol. 9, pp. 485-492.Malta, JCO & Varella, AΜΒ. 1996. Ergasilus turucuyus sp. n. (Copepoda: Ergasilidae) from the gills of Acestrorhynchus falcatus (Bloch, 1794) e A. falcirostris (Cuvier, 1819) (Characiformes: Characidae) from Brazilian Amazon. Acta Amazonica, vol. 26, pp. 69-76.Marcogliese, DJ. 2002. Food webs and the transmission of parasites to marine fish. Parasitology, vol. 124, pp. 83-99.Morais, AM. 2011. Biodiversidade de parasitos da piranha vermelha Pygocentrus nattereri ( K n e r,  1 8 5 8 )  ( C h a r a c i f o r m e s ;  Serrasalmidae) e sua avaliação como bioindicadores na Amazônia Central. Tese de Doutorado, Instituto Nacional de Pesquisas da Amazônia,  Manaus,  Amazonas. 234 pp.Moravec, F, Kohn, A & Fernandes, BM. 1993. Nematode parasites of fishes of the Paraná River, Brazil. Part 2. Seuratoidea, Ascaridoidea, Habronematoidea and Acuarioidea. Folia Parasitologica, vol. 40, pp. 115-115.Pretti, VQ, Calcagnotto, D, Toledo-Piza, M &  Almeida-Toledo, LF. 2009. Phylogeny of the neotropical genus Acestrorhynchus (Ostariophysi:Characiformes) based on Neotropical Helminthology, 2018, 12(2), jul-dic Metazoan parasites of Serrasalmus altispinis152nuclear and mitochondrial gene sequences and morphology: A total evidence approach. Molecular phylogenetics and evolution, vol. 52, pp. 312-320.Santana HP. 2014. A fauna parasitária de Cichla monoculus (Spix & Agassiz, 1831) (Perciformes: Cichlidae) de lagos de várzea da Amazônia Central, Brasil. Tese de Mestrado, INPA, Manaus. 65 pp.Soares, MG, Costa, EL, Siqueira-Souza, FK, Dos Anjos, HD, Yamamoto, KC & Freitas, CE. 2008. Peixes de lagos do médio rio Solimões. 2ª ed. Instituto Piatam, Manaus. 176 pp.Thatcher, VE. 2006. Amazon Fish Parasites. ndPensoft Publishers, 2  ed. Sofia-Moscoow, 508 pp.Toledo-Piza, M. 2007. Phylogenetic relationship a m o n g  A c e s t r o r h y n c h u s  s p e c i e s  ( O s t a r i o p h y s i :  C h a r a c i f o r m e s :  Acestrorhynchidae). Zoological Journal of the Linnean Society, vol. 151, pp. 691-757..Received August 8, 2018.Accepted October 5, 2018.Neotropical Helminthology, 2018, 12(2), jul-dic Murrieta Morey & Oliveira Malta

METAZOARIOS PARÁSITOS DE ACESTRORHYNCHUS FALCATUS (CHARACIFORMES: ACESTRORHYNCHIDAE) COLECTADOS EN LAGOS INUNDABLES DE LA AMAZONÍA BRASILEÑA

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METAZOARIOS PARÁSITOS DE ACESTRORHYNCHUS FALCATUS (CHARACIFORMES: ACESTRORHYNCHIDAE) COLECTADOS EN LAGOS INUNDABLES DE LA AMAZONÍA BRASILEÑA

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