Este trabajo describe la fauna parasitaria de Serrasalmus altispinis Merckx, Jégu y Santos, 2000 provenientes de lagos inundables de la Amazonía brasileña. Todas las especies identificadas representan los primeros registros para este hospedero. 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 S. altispinis fueron colectados y examinados durante cuatro expediciones en Marzo, Junio, Septiembre y Diciembre del 2013. Fueron identificadas 36 especies pertenecientes a Monogenoidea, Digenea, Nematoda, Copepoda, Branchiura e Isopoda. Los índices parasitológicos obtenidos en este estudio indican que la comunidad de endoparásitos de S. altispinis es caracterizada por baja prevalencia, bajo número de individuos y bajo número de especies. En contraste, los ectoparásitos presentan alta prevalencia y un alto número de individuos y especies

de Oliveira Malta, José Celso

Murrieta Morey, Germán Augusto

Spanish

LAReferencia - Red Federada de Repositorios Institucionales de Publicaciones Científicas Latinoamericanas

 ISSN Versión impresa 2218-6425    ISSN Versión Electrónica 1995-1043Neotropical Helminthology, 2018, 12(2), jul-dic:141-146.ORIGINAL ARTICLE / ARTÍCULO ORIGINALMETAZOAN PARASITES OF SERRASALMUS ALTISPINIS (SERRASALMIDAE) FROM FLOODPLAIN LAKES OF THE BRAZILIAN AMAZONMETAZOÁRIOS PARÁSITOS DE SERRASALMUS ALTISPINIS (SERRASALMIDAE) DE 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: Amazon – ectoparasites – endoparasites – parasitological indices – piranha – Serrasalmus altispinisThis work describes the parasitic fauna of Serrasalmus altispinis Merckx, Jégu and Santos, 2000 caught in floodplain lakes of the Brazilian Amazon. All parasite species reported represent first records for this host. The studied lakes were: Baixio, Preto, São Tomé, Ananá, Araçá and Maracá, located between the cities of Manaus and Coari in Central Amazonia. Sixty S. altispinis were collected and examined in March, June, September, and December 2013. Thirty-six species belonging to Monogenoidea, Digenea, Nematoda, Copepoda, Branchiura and Isopoda were identified. Parasitological indices obtained in this study indicate that the community of endoparasites of S. altispinis is characterized by low prevalence, low number of individuals and low number of species. In contrast, ectoparasites presented higher prevalence and higher number of individuals and species.Neotropical Helminthology 141Volume12,Number2(jul-dec2018)ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)Lima-PerúVersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043RESUMENPalabras clave: Amazonas – ectoparásitos – endoparásitos – índices parasitarios – piraña – Serrasalmus altispinisEste trabajo describe la fauna parasitaria de Serrasalmus altispinis Merckx, Jégu y Santos, 2000 provenientes de lagos inundables de la Amazonía brasileña. Todas las especies identificadas representan los primeros registros para este hospedero. 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 S. altispinis fueron colectados y examinados durante cuatro expediciones en Marzo, Junio, Septiembre y Diciembre del 2013. Fueron identificadas 36 especies pertenecientes a Monogenoidea, Digenea, Nematoda, Copepoda, Branchiura e Isopoda. Los índices parasitológicos obtenidos en este estudio indican que la comunidad de endoparásitos de S. altispinis es caracterizada por baja prevalencia, bajo número de individuos y bajo número de especies. En contraste, los ectoparásitos presentan alta prevalencia y un alto número de individuos y especies.142Neotropical Helminthology, 2018, 12(2), jul-dicINTRODUCTION the Purus River (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 mg clove oil L  solution and euthanized -1·(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 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), Manaus, Brazil.At 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).  All specimens of S. altispinis were parasitized by at least one parasite species. There were found 1,122 specimens of parasites. We identified 36 species, 23 belonging to Monogenoidea, 1 to Digenea, 5 to Nematoda, 4 to Copepoda, 1 to Branchiura and 2 to Isopoda (Table 1).The highest prevalence of infection was 50% for Anacanthorus jegui Van Every & Kritsky, 1992, the highest mean intensity and mean abundance of infection was found for Amplexibranchius bryconis Thatcher & Paredes, 1995 (Table 1).In this study S. altispinis was parasitized by 23 species of Monogenoidea from eight genera. Species allocated in five of these genera are specific of Serrasalmidae namely: Amphithecium; Within Serralsamidae, Serrasalmus altispinis Merckx, Jégu & Santos, 2000, commonly known as “piranha seca” can reach 19 cm and inhabits lakes of white water rivers, being usually captured near to the aquatic vegetation and in flooded forest (Claro-Jr., 2003). According to Claro-Jr. (2003) S. altispinis feeds on scales and fins of fishes and can also swallow small fishes and invertebrates.Taxonomic studies that discover new species, new host and geographical occurrences represent enormous contribution to the knowledge of the biodiversity of a determinate area and constitute a base for other studies in parasitological ecology, environmental impacts, biotic integrity and conservation of ecosystems (Luque & Poulin, 2007). Studies on parasite communities and diversity in fish from the Amazon increase the knowledge of the richness and diversity in this ecosystem.For S. altispinis there is still scarce information on their parasitic fauna. The only records for this species are cited by Oliveira et al. (2017) who found the crustaceans Braga patagonica Schiodte & Meinert, 1884 on the mouth and Argulus nattereri Heller, 1857 on the integument of specimens collected in the state of Amapá, Brazil. The parasitic fauna of S. altispinis has been poorly studied. Thus, the objective of the present study was to identify the metazoan parasite fauna of S. altispinis collected in different floodplain lakes from the Brazilian Amazon.Between March and December 2013, 60 S. altispinis (Figure 1) were caught in  six floodplain lakes of the Solimões River: Lake Baixio (03°17'27, 2''S/ 60°04'29,6''W) at the city of I randuba,  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 at the Murrieta Morey & Oliveira MaltaMATERIAL AND METHODSRESULTSDISCUSSION143Parasites Accession No P% N mI mA MONOGENOIDEA     Amphithecium diclonophallum Kritsky, Boeger & Jégu, 1997 INPA 622 11.67 12 1.71 ± 1.49 0.20 Amphithecium falcatum Boeger & Kritsky, 1988 INPA 623 36.67 71 3.22 ± 3 1.18 Anacanthorus amazonicus Kritsky & Boeger 1995 INPA 624 13.33 21 2.62 ± 4.20 0.35 Anacanthorus cintus Van Every & Kritsky, 1992 INPA 625 3.33 4 2 ± 1.41 0.07 Anacanthorus cladophallus Van Every & Kritsky, 1992 INPA 626 1.67 1 1 0.02 Anacanthorus crytocaulus Van Every & Kritsky, 1992 INPA 627 3.33 2 1 0.03 Anacanthorus gravihamulatus Van Every & Kritsky, 1992 INPA 628 3.33 2 1 0.03 Anacanthorus jegui Van Every & Kritsky, 1992 INPA 629 50.00 104 3.46 ± 2.99 1.73 Anacanthorus lepyrophallus Kritsky, Boeger & Van Every 1992 INPA 630 21.67 45 3.46 ± 4.99 0.75 Anacanthorus mesocondylus Van Every & Kritsky, 1992 INPA 631 30.00 34 1.88 ± 2.80 0.57 Anacanthorus peryphallus Kritsky, Boeger & Van Every 1992 INPA 632 21.67 21 1.61 ± 0.76 0.35 Anacanthorus prodigiosus Van Every & Kritsky, 1992 INPA 633 15.00 12 1.33 ± 0.70 0.20 Anacanthorus sciponophallus Van Every & Kritsky, 1992 INPA 634 33.33 44 2.2 ± 1.63 0.73 Anacanthorus serrasalmi Van Every & Kritsky, 1992 INPA 635 5.00 4 1.33 ±  0.57 0.07 Ancanthorus sp. INPA 636 36.67 68 3.04 ± 1.60 1.13 Calpidothecium crescentis Mizelle & Price, 1965 INPA 635 1.67 1 1 0.02 Enallothecium aegidatum Kritsky, Boeger & Jégu, 1998 INPA 636 26.67 54 3.31 ± 1.92 0.90 Myramothecium whittingtoni Kritsky, Boeger & Jégu, 1996 INPA 637 3.33 2 1 0.03 Notothecium cyphophallum Kritsky, Boeger & Jegú, 1998  INPA 638 28.33 71 4.17 ± 5.99 1.18 Notothecium deleastoideum Kritsky, Boeger & Jegú, 1998  INPA 639 38.33 149 6.43 ± 6.05 2.48 Notozothecium euzeti Kritsky, Boeger & Jegú, 1996  INPA 640 1.67 1 1 0.02 Notozothecium minor Boeger & Kritsky, 1988  INPA 641 20.00 16 1.33 ± 0.77 0.27 Rhinoxenus piranhus Kritsky, Boeger & Thatcher, 1988  INPA 642 35.00 78 3.71 ± 4.05 1.30 DIGENEA      Clinostomum marginatum (Rudolphi, 1819) INPA 689 a -b 16.67 22 2.2 ± 3.15 0.37 NEMATODA     Procamallanus (Spirocamallanus) inopinatus  Travassos, Artigas & Pereira, 1928 INPA 79, 80 55.00 48 1.45 ± 1 0.8 Anisakis sp. INPA 77, 78 11.67 13 1.86 ± 1.9 0.21 Contracaecum sp. INPA 83 1.67 2 2 0.03 Pseudoproleptus sp. INPA 82 3.33 6 3 0.1 Philometra nattereri Cárdenas, Moravec, Fernándes & Morais 2011 INPA 81 1.67 1 1 ± 2.82 0.01 COPEPODA     Amplexibranchius bryconis Thatcher & Paredes, 1995 INPA 2236 35.00 163 7.8 ± 2.82 2.72 Ergasilus jaraquensis Thatcher & Robertson, 1982 INPA 2235 17.00 10 1 ± 0.5 0.17 Gamidactylus jaraquensis Thatcher & Boeger, 1984 INPA 2234 17.00 22 2.2 ± 1.5 0.4 Rhinergasilus piranhus Boeger & Thatcher, 1988 INPA 2233 1.67 1 1 0.02 BRANCHIURA     Argulus chicomendesi Malta & Varella, 2000 INPA 2231 1.67 1 1 4.4 ISOPODA     Amphira branchialis Thatcher, 1993 INPA 2229 11.67 14 2 0.23 Vanamea symetrica (Van Name, 1925) INPA 2230 1.67 1 1 0.02Table 1. Metazoan parasites in Serrasalmus altispinis Merckx, Jégu and Santos, 2000 from Brazilian Amazon floodplain lakes. P% = prevalence, N = number of parasites, mI = mean intensity, mA = mean abundance.Metazoan parasites of Serrasalmus altispinisNeotropical Helminthology, 2018, 12(2), jul-dic144Figure 1. Lateral view of Serrasalmus altispinis Merckx, Jégu and Santos, 2000 captured in floodplain lakes of the Brazilian Amazon.Calpidothecium; Enallothecium; Myramothecium and Notothecium. Three genera are not host specific namely: Anacanthorus, which also parasitizes fish species of Characidae and Curimatidae, Notozothecium that is also found in Cynodontidae and Rhinoxenus that parasitizes Charac idae  (Braga  et  a l . ,  2014) .  Al l  monogenoideans recorded in the present study are first records for S. altispinis.In floodplain lakes from the Brazilian Amazon, Clinostomum marginatum was recorded infecting the gills of Cichla monoculus Spix & Agassiz, 1831 (Paredio, 2014), in the musculature of Pygocentrus nattereri Kner, 1858 (Morais, 2011), and in gills, eyes, intestine and liver of Acestrorhynchus falcirostris (Cuvier, 1819) (Dumbo, 2014). In the present study, C. marginatum is cited for the first time parasitizing S. altispinis. This parasite is capable to parasitize different organs of several fish species in floodplain lakes of the Brazilian Amazon.In floodplain lakes of the Brazilian Amazon, Anisakis sp., Pseudoproleptus sp. and P. (S.) inopinatus were found parasitizing the intestine, stomach and liver of P. nattereri (Morais, 2011) and A. falcirostris (Dumbo, 2014). Morais (2011) cited Philometra nattereri parasitizing the eyes of P. nattereri. Dumbo (2014) found Contracaecum sp. parasitizing the intestine and stomach of A. falcirostris. In the present study, all these nematodes are cited for the first time in S. altispinis, expanding the number of known hosts for these parasites.Amplexibranchius bryconis was cited for the first time in Brazil parasitizing the gills of Potamorhina latior (Spix & Agassiz, 1829) captured in floodplain lakes of the Brazilian Amazon (Morey et al., 2015). The second record was reported in A. falcirostris captured in the same lakes (Dumbo, 2014). In the present study, this copepod species is cited for the third time in Brazil, parasitizing a new host, representing the first record for S. altispinis.Ergasilus jaraquensis was found for the first time parasitizing the gills of Semaprochilodus insignis (Jardine, 1841) collected in the River Solimões (Thatcher & Robertson, 1982). In floodplain lakes of the Brazilian Amazon, E. jaraquensis was cited parasitizing P. latior (Morey et al., 2015). In the Neotropical Helminthology, 2018, 12(2), jul-dic Murrieta Morey & Oliveira MaltaAmato, 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.Bellay, S, Oliveira, EF, Almeida-Neto, M, Lima Junior, DP, Takemoto, RM & Luque, JL. 2013. Developmental stages of parasites influences the structure of fish-parasite networks. PLoS ONE, vol. 8, pp. 1-6.Braga, MP, Araújo, SB & Boeger, WA. 2014. Patterns of interaction between Neotropical f reshwater  f i shes  and  the ir  g i l l  Monogenoidea (Pla tyhelminthes) .  Parasitology research, vol. 113, pp. 481-490.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.Claro Jr, LH. 2003. A influência da floresta alagada na es trutura tróf ica de  comunidades de peixes em lagos de várzea da Amazônia Central. Tesis de mestrado. INPA-UFAM, Manaus, 61 pp.Carvalho, LN, Arruda, R & Del-Claro, K. 2004. Host-parasite interactions between the piranha P. nattereri (Characiformes: Characidae) and isopods and branchiurans (Crustacea) in the rio Araguaia basin, Brazil. Neotropical Ichthyology, vol. 2, pp. 93-98.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, INPA, Manaus, 150 pp.Lacerda, ACF, Takemoto, RM, Lizama, M & Pavanelli, GC. 2008. Copépodes parasitos de fossas nasais de cinco espécies de peixes (Characiformes) da planície de inundação 145present study, S. altispinis is cited as a new host for this parasite species.In floodplain lakes of the Brazilian Amazon, Rhinergasilus piranhus was found in the nostrils of P. nattereri (Morais, 2011). According to Varella & Malta (1995), R. piranhus is usually found together with Gamidactylus jaraquensis. These two copepods were also collected in the nostrils of different fish species from the River Paraná (Lacerda et al., 2008). In the present study, R. piranhus and G. jaraquensis were found in the nostrils of S. altispinis, being new records for this fish.The branchiuran Argulus chicomendesi was found parasitizing the body surface of P. nattereri collected in floodplain lakes of the Brazilian Amazon (Morais, 2011). In the present study, only one specimen of A. chicomendesi was found in S. altispinis. However, it represents the first record of this parasite in this host; it may also be considered as an accidental infestation.For Serrasalmidae, the isopod Anphira branchialis was cited parasitizing P. nattereri (Thatcher, 1993; Carvalho et al., 2004; Vital et al., 2011; Morais, 2011; Tavares-Dias et al., 2015), Serrasalmus spilopleura Kner, 1858 Serrasalmus sp. (Thatcher, 1993; Tavares-Dias et al., 2015). Vanamea symetrica was cited parasitizing S. elongatus Kner, 1858, S. rhombeus (Linnaeus, 1766), S. spilopleura and Serrasalmus sp. (Thatcher, 1993). In the present study, these two isopods are cited for the first time in S. altispinis.The presence of parasites in larval stage indicates that a fish species is a prey with an intermediate position in the food chain and is an intermediate or paratenic host of one or more parasite species (Bellay et al., 2013, Poulin & Leung 2011). In the present study two endoparasite species were found in adult stage and four were found in larval stage, indicating that S. altispinis is a definitive host of P. (S.) inopinatus and Philometra nattereri Cardenas, Movarec, Fernandes & Morais, 2012 and intermediate or paratenic host of C. marginatum, A n i s a k i s  s p ,  C o n t r a c a e c u m  s p  a n d  Pseudoproleptus sp. This fish occupies an intermediate position in the food web, feeding on other organisms and being predated by other vertebrates.BIBLIOGRAPHIC REFERENCESMetazoan parasites of Serrasalmus altispinisNeotropical Helminthology, 2018, 12(2), jul-dic146do alto rio Paraná, Paraná, Brasil. Acta Scientiarum, vol. 29, pp. 429-435.Luque, JL & Poulin, R. 2007. Metazoan parasite species richness in Neotropical fishes: hotspots and the geography of biodiversity. Parasitology, vol. 134, pp. 865-878.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, INPA, Manaus, 234 PP.Morey, GAM, Moreira, ADC & Malta, JCO. 2015. As espécies de Copepoda (Crustacea: Ergasilidae) parasitas dos filamentos branquiais de Potamorhina latior (Spix & A g a s s i z ,  1 8 2 9 )  ( C h a r a c i f o r m e s :  Curimatidae) de lagos de várzea da Amazônia  Centra l ,  Bras i l .  Fol ia  Amazónica, vol. 24, pp. 103-108.Oliveira, 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. Journal of Parasitic Diseases, vol. 41, pp. 565-570.Paredio, HS. 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.Poulin, R & Leung, TLF. 2011. Body size, trophic level, and the use of fish as transmission routes by parasites. Oecologia, vol. 166, pp. 731-738.Tavares-Dias, M, Dias-Júnior, MBF, Florentino, AC, Silva, LMA & Cunha, ACD. 2015. Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Revista Brasileira de Parasitologia Veterinária, vol. 24, pp. 136-147.Thatcher, VE & Robertson, BA. 1982. Parasitic crustaceans of fishes from the Brazilian Amazon. 3. Erasilus jaraquensis, n. sp.(Copepoda: Cyclopoidea) from the gills of Semaprochilodus insignis (Schomburgk). Revista brasileira de biologia, vol. 42, pp. 515-519.Thatcher, VE. 1993. Vanamea gen, nov. for Livoneca symmetrica Van Name, 1925, (Crustacea, Isopoda, Cymothoidae) and a redescription of the species based on specimens from Brazilian piranhas. Acta Amazonica, vol. 23, pp. 287-296.Varella, A & Malta, JCO. 1995. Gamidactylus h o p l i u s  s p .  n . ( C o p e p o d a ,  Poecilostomatoida, Vaigamidae) from nasal fossae of Hoplias maiabaricus (Bloch, 1794) (Characiformes, Erythrynidae) from the Brazilian Amazon. Acta Amazonica, vol. 25, pp. 281-288.Vital, JF, Varella, AMB, Porto, DB & Malta, JCO. 2011.  Sazonalidade da fauna de metazoários de Pygocentrus nattereri (Kner, 1858) no lago Piranha (Amazonas, Brasil) e a avaliação de seu potencial como indicadora da saúde do ambiente. Biota Neotropical, vol. 11, pp. 199-204.Received August 9, 2018.Accepted October 5, 2018.Neotropical Helminthology, 2018, 12(2), jul-dic Murrieta Morey & Oliveira Malta

METAZOÁRIOS PARÁSITOS DE SERRASALMUS ALTISPINIS (SERRASALMIDAE) DE LAGOS INUNDABLES DE LA AMAZONÍA BRASILEÑA

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METAZOÁRIOS PARÁSITOS DE SERRASALMUS ALTISPINIS (SERRASALMIDAE) DE LAGOS INUNDABLES DE LA AMAZONÍA BRASILEÑA

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