Argulus elongatus (Branchiura, Argulidae) in fish in the upper São Francisco river, Brazil

Argulus elongatus (Branchiura, Argulidae) de peixes do alto rio São Francisco, Brasil

Rayane Duarte Maria de Fátima Cancella de Almeida-Berto Caroline Ferreira Calvario Michelle Daniele dos Santos-Clapp Marilia de Carvalho Brasil-Sato About the authors

Abstract

Among 164 fish from the upper São Francisco river, caught in the Três Marias reservoir (18º 12’ 59” S; 45º 17’ 34” W) or downstream from this reservoir (18º 12’ 32” S; 45º 15’ 41” W) in 2007, 2008, 2016 and 2017, four specimens of Argulus elongatus Heller, 1857 were found, one specimen per fish, in the following host species: Brycon orthotaenia Günther (two fish parasitized out of 38 examined) and Salminus hilarii Valenciennes (one fish parasitized out of 45 examined) (both in Bryconidae); and Metynnis lippincottianus (Cope) (one fish parasitized out of 81 examined) (Serrasalmidae). This opportunistic ectoparasite deserves attention even in the case of low infestation in fish in a natural water system. This is the first record of a branchiuran species in B.orthotaenia; the host list of A.elongatus is extended through addition of the three fish species examined in this study, and the known Brazilian geographical distribution of this argulid is enlarged to the São Francisco river basin.

Keywords:
Fish ectoparasite; fish lice; Brycon orthotaenia; Salminus hilarii; Metynnis lippincottianus

Resumo

De 164 peixes do alto rio São Francisco, capturados no Reservatório de Três Marias (18º 12’ 59” S; 45º 17’ 34” O) ou à jusante dele (18º 12’ 32” S; 45º 15’ 41” O), em 2007, 2008, 2016 e 2017, quatro espécimes de Argulus elongatus Heller, 1857 foram encontrados, sendo um branquiúro por peixe nas seguintes espécies de hospedeiros: Brycon orthotaenia Günther (dois peixes parasitados de 38 peixes examinados), Salminus hilarii Valenciennes (um peixe parasitado de 45 examinados) – ambos Bryconidae, e Metynnis lippincottianus (Cope) (um peixe parasitado de 81 examinados) - Serrasalmidae. Esse ectoparasito oportunista merece atenção, mesmo no caso de infestações baixas em peixes de ambientes hídricos naturais. Esse é o primeiro registro de Branchiura em B.orthotaenia. A lista de hospedeiros de A. elongatus é ampliada com a adição das três espécies de peixes examinadas neste estudo. A distribuição geográfica conhecida desse argulídeo no Brasil, é ampliada para a bacia do rio São Francisco.

Palavras-chave:
Ectoparasitos de peixes; piolhos de peixe; Brycon orthotaenia; Salminus hilarii; Metynnis lippincottianus

The basin of the São Francisco river is the largest hydrographic basin in Brazilian territory. Its ichthyofauna is diverse, with socioenvironmental importance, especially for fishing (Godinho & Godinho, 2003Godinho AL, Godinho HP. Breve visão do São Francisco. In: Godinho HP, Godinho AL. Águas, peixes e pescadores do São Francisco das Minas Gerais. Belo Horizonte: PUC Minas; 2003. p. 15-24.). Several groups of parasites have been recorded in fish from the Três Marias reservoir, on the upper São Francisco river, including Branchiura (Brasil-Sato, 2003Brasil-Sato MC. Parasitos de peixes da bacia do São Francisco. In: Godinho HP, Godinho AL. Águas, peixes e pescadores do São Francisco das Minas Gerais. Belo Horizonte: PUC Minas; 2003. p. 149-165.).

Branchiura is a group of crustaceans that usually parasitizes both freshwater and saltwater fish and is recognized by fishermen and fish farmers as ‘fish lice’ (Lemos de Castro, 1985Lemos de Castro A. Branchiura. In: Schaden R. Manual de identificação de invertebrados límnicos do Brasil. Brasília: CNPq/MCT; 1985. p. 1-23.; Thatcher, 2006Thatcher VE. Amazon fish parasites. 2nd ed. Sofia, Moscow: Pensoft Publishers, 2006.). They parasitize the surface of the body, fins, buccal cavity and gills of fish and can occasionally parasitize amphibians, reptiles and some invertebrates (Ringuelet, 1943Ringuelet R. Revisión de los Argúlidos Argentinos (Crustácea. Branchiura) con el catálago de las especies neotropicales. Rev Museo de La Plata 1943; 3(19): 43-100.; Poly, 2008Poly WJ. Global diversity of fishlice (Crustacea: Branchiura: Argulidae) in freshwater. Hydrobiologia 2008; 595(1): 209-212. http://dx.doi.org/10.1007/s10750-007-9015-3.
http://dx.doi.org/10.1007/s10750-007-901...
). Argulidae is the only family in Branchiura and it comprises four genera: Argulus Müller, 1785, Chonopeltis Thiele, 1900, Dipteropeltis Calman, 1912, and Dolops Audouin, 1837. This family has the highest diversity of genera and species occurring in the Afrotropical and Neotropical regions, in comparison with other biogeographical areas of the world: Nearctic, Oriental, Palearctic, Australasia with Pacific Ocean islands and Antarctica (Poly, 2008Poly WJ. Global diversity of fishlice (Crustacea: Branchiura: Argulidae) in freshwater. Hydrobiologia 2008; 595(1): 209-212. http://dx.doi.org/10.1007/s10750-007-9015-3.
http://dx.doi.org/10.1007/s10750-007-901...
).

Reports of injuries to fish caused by argulids have included blood and tissue consumption at the puncture site; fungal infections at the puncture site; and transmission of viral and bacterial diseases (Thatcher, 2006Thatcher VE. Amazon fish parasites. 2nd ed. Sofia, Moscow: Pensoft Publishers, 2006.; Poly, 2008Poly WJ. Global diversity of fishlice (Crustacea: Branchiura: Argulidae) in freshwater. Hydrobiologia 2008; 595(1): 209-212. http://dx.doi.org/10.1007/s10750-007-9015-3.
http://dx.doi.org/10.1007/s10750-007-901...
; Woo & Buchmann, 2012Woo PT, Buchmann K. Fish parasites: pathobiology and protection. London: CABI; 2012. http://dx.doi.org/10.1079/9781845938062.0000.
http://dx.doi.org/10.1079/9781845938062....
). These reports highlight the importance of reporting occurrences of these ectoparasites, even when they are uncommon in the fish communities of natural water systems.

In 2007, 2008, 2016 and 2017, a total of 164 fish specimens were caught by artisanal fishermen in the upper São Francisco river, state of Minas Gerais, Brazil. Among these, 139 fish were caught in the Três Marias reservoir (18º 12’ 59” S; 45º 17’ 34” W), consisting of 13 specimens of B. orthotaenia Günther, 1864 (in 2008) and 45 of S. hilarii Valenciennes, 1850 (33 fish in 2007, and 12 in 2016) (both in Bryconidae); and 81 of M. lippincottianus (Cope, 1870) (67 in 2016, and 14 in 2017) (Serrasalmidae). The other 25 fish (B.orthotaenia, in 2016) were caught in the São Francisco river (18º 12’ 32” S; 45º 15’ 41” W), downstream from the Três Marias dam.

The fish caught in 2007 and 2008 were individually fixed in bottles filled with 3% formalin and those caught in 2016 and 2017 were individually packaged in plastic bags and frozen. These fish were transported from the Três Marias Integrated Center for Fishery and Aquiculture Resources (Centro Integrado de Recursos Pesqueiros e Aquicultura de Três Marias; 1st CIT), state of Minas Gerais, Brazil, which belongs to the Development Company of the São Francisco and Parnaíba Valleys (Companhia de Desenvolvimento dos Vales do São Francisco e Parnaíba; CODEVASF), to the Parasite Biology and Ecology Laboratory of the Federal Rural University of Rio de Janeiro (Universidade Federal Rural do Rio de Janeiro), Seropédica, state of Rio de Janeiro, southeastern Brazil, for parasitological analysis. The mean total body length and respective minimum and maximum values of each fish were recorded: B. orthotaenia: 34.1 (23.0-50.0 cm); S. hilarii: 26.7 (19.5-41.0 cm); and M. lippincottianus: 14.0 (9.0-19.0 cm).

The fish classification followed Reis et al. (2003)Reis RE, Kullander SO, Ferraris CJ. Check list of the freshwater fishes of South and Central America. Porto Alegre: EDIPUCRS; 2003. and Froese & Pauly (2019)Froese R, Pauly D, editors. 2019. Fishbase. World Wide Web eletronic publication. Version (02/2019) [online] [cited 2019 Jun 28]. Available from: http://www.fishbase.org/search.php
http://www.fishbase.org/search.php...
; the voucher specimens were deposited in the Zoology Museum of the University of São Paulo (MZUSP): B. orthotaenia (95166) and M. lippincottianus (95160). The classification of family and genus levels of the branchiurans followed Lemos de Castro (1985)Lemos de Castro A. Branchiura. In: Schaden R. Manual de identificação de invertebrados límnicos do Brasil. Brasília: CNPq/MCT; 1985. p. 1-23. and Thatcher (2006)Thatcher VE. Amazon fish parasites. 2nd ed. Sofia, Moscow: Pensoft Publishers, 2006.; and the argulid species were identified in accordance with Thiele (1904)Thiele J. Beiträge zur Morphologie der Arguliden. In: Zoologisches Museum in Berlin. Mitteilungen aus dem Zoologischen Museum, Berlin (4th ed.). Berlin: R. Friedländer & Sohn, 1904. v. 2, p. 1-51. Mit 4 Tafeln (6-9).. The ectoparasite specimens were mounted on temporary slides using Amann’s lactophenol for morphological evaluation and to make photomicrographs using an Olympus BX41 light microscope. Voucher specimens of the parasitic argulids were deposited in liquid medium (70 ºGL ethanol) in the Crustacea Collection of the National Institute for Amazon Research (Instituto Nacional de Pesquisas da Amazônia; INPA): 2501 (B. orthotaenia), 2503 (S. hilarii) and 2502 (M. lippincottianus). The ecological parameters of prevalence (P), mean intensity (MI) and mean abundance (MA) were determined as described by Bush et al. (1997)Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
http://dx.doi.org/10.2307/3284227...
.

A total of four specimens of crustaceans were identified as Argulus elongatus Heller, 1857 (Figure 1), which is located in Maxillopoda, Branchiura, Arguloida, Argulidae, were found on the body surface of four fish: two ectoparasites (one in each) in two specimens of B. orthotaenia from the São Francisco river in October 2016, out of 38 examined (P = 5.3%, MI = 1.0, MA = 0.05); one ectoparasite in one of S. hilarii from the Três Marias reservoir in October 2016, out of 45 examined (P = 2.2%, MI = 1.0, MA = 0.02); and one ectoparasite in one of M. lippincottianus from the Três Marias reservoir in July 2017, out of 81 examined (P = 1.2%, MI = 1.0, MA = 0.01).

Figure 1
A-E: Argulus elongatus Heller, 1857, found on Salminus hilarii Valenciennes, 1850, from the Três Marias reservoir, on the upper São Francisco river, state of Minas Gerais, Brazil. Female adult specimen clarified with Amann's lactophenol: Photo A (ventral overview) - AN: antennae, BA: bilobed abdomen, scale = 1 mm; Photo B (dorsal overview) - CE: compound eyes, LE: legs, SP: spermathecae, scale = 1 mm; Photo C (first maxilla) – 1st M: first maxilla, detail of the chitinous support rods of suction cups, scale = 50 μm; Photo D (second maxilla) - 2nd M: second maxilla, arrows indicate maxillary teeth, *indicates partial respiratory area (as shown in Photo E), scale = 200 μm; Photo E (region near the first maxilla) - RA: partial respiratory area, *indicates same region as in Photo D, scale = 50 μm.

Argulus elongatus is considered to be a generalist parasite, and was recorded with low prevalence in the three host species in the current study. Nonspecificity is inherent among argulid species. Hence, specimens of a particular species can be found in several species of fishes and, conversely, a single fish can be parasitized by different species of argulids. In addition, these branchiurans can easily move from one point to another on the host, and they are able to swim swiftly through the thoracic appendages. These characteristics help in understanding the diversity of fish species that they can parasitize (Lemos de Castro, 1985Lemos de Castro A. Branchiura. In: Schaden R. Manual de identificação de invertebrados límnicos do Brasil. Brasília: CNPq/MCT; 1985. p. 1-23.).

This opportunistic ectoparasite deserves attention because it can cause several types of injury to its hosts through spoliation and trauma in the tissues. The severity of injuries depends on the intensity of infestation, such that numerous lesions are often sites that allow secondary infections. These parasites can have a serious impact on farmed fish, mainly because these fish are concentrated in small areas or held under semi-confinement, but may also affect fish from natural water systems (Kabata, 1970Kabata Z. Diseases of fishes: crustacea as enemies of fishes. Jersey City, USA: TFH; 1970.; Thatcher, 2006Thatcher VE. Amazon fish parasites. 2nd ed. Sofia, Moscow: Pensoft Publishers, 2006.; Poly, 2008Poly WJ. Global diversity of fishlice (Crustacea: Branchiura: Argulidae) in freshwater. Hydrobiologia 2008; 595(1): 209-212. http://dx.doi.org/10.1007/s10750-007-9015-3.
http://dx.doi.org/10.1007/s10750-007-901...
).

In the São Francisco river, Brasil-Sato (2003)Brasil-Sato MC. Parasitos de peixes da bacia do São Francisco. In: Godinho HP, Godinho AL. Águas, peixes e pescadores do São Francisco das Minas Gerais. Belo Horizonte: PUC Minas; 2003. p. 149-165. cited a finding of the argulid Argulus multicolor Stekhoven, 1937, in Salminus brasiliensis (Cuvier, 1816) [= S. franciscanus Lima & Britski, 2007], with the indexes P = 2.8%, MI = 7.0 and MA = 0.2, which was reported in: Tavares, R.O. & Brasil-Sato, M.C. Parasitos de brânquias de Salminus brasiliensis (Cuvier, 1817) (Osteichthyes, Characidae) do Rio São Francisco, MG, Brasil. Annals of “XI Jornada de Iniciação Científica da UFRRJ”, v. 11, n. 1, p. 355-356, 2001. Edur: Seropédica, RJ, ISSN 1518-5680. Brasil-Sato (2003)Brasil-Sato MC. Parasitos de peixes da bacia do São Francisco. In: Godinho HP, Godinho AL. Águas, peixes e pescadores do São Francisco das Minas Gerais. Belo Horizonte: PUC Minas; 2003. p. 149-165. also reported an occurrence of Dolops sp. in Hoplias lacerdae Miranda-Ribeiro, 1908 [= H. intermedius (Günther, 1864)], from a record made in 1994 by Narcisa Imaculada Brant Moreira in her master’s dissertation in the Institute of Biological Sciences of the Federal University of Minas Gerais (Universidade Federal de Minas Gerais), state of Minas Gerais, Brazil.

Among the hosts analyzed in the present study, S. hilarii and M. lippincottianus are known to have geographical distribution outside of the São Francisco river (Shibatta & Garavello, 1993Shibatta OA, Garavello JC. Estudo da variação geográfica em Salminus hilarii Valenciennes, 1849, das bacias do Alto Paraná e São Francisco, através da análise morfométrica multivariada em componentes principais. Naturalia (Sao Jose Rio Preto) 1993; 18: 109-116.; Sato & Sampaio, 2006Sato Y, Sampaio EV. A ictiofauna do Reservatório de Três Marias, Rio São Francisco, Minas Gerais. Belo Horizonte: FUNDEP-UFMG/ SECTESMG; 2006.). Salminus hilarii was recorded as a host in Brazil for Argulus paulensis Wilson, 1924, according to Thatcher (2006)Thatcher VE. Amazon fish parasites. 2nd ed. Sofia, Moscow: Pensoft Publishers, 2006.; while M.lippincottianus in the Igarapé Fortaleza basin, a tributary of the Amazon river, in Macapá, state of Amapá, was recorded as a host for the argulid Dolops longicauda Heller, 1857 (Hoshino & Tavares-Dias, 2014Hoshino MDFG, Tavares-Dias M. Ecologia parasitária de Metynnis lippincottianus (Characiformes: Serrasalmidae) da região da Amazônia oriental, Macapá, Estado do Amapá, Brasil. Acta Sci Biol Sci 2014; 36(2): 249-255. http://dx.doi.org/10.4025/actascibiolsci.v36i2.19876.
http://dx.doi.org/10.4025/actascibiolsci...
).

Argulus elongatus was described by Heller in 1857 from a female specimen that was very poorly preserved in the zoological collection of the Natural History Museum of Vienna (Naturhistorischen Museum Wiener), in Austria (Thiele, 1904Thiele J. Beiträge zur Morphologie der Arguliden. In: Zoologisches Museum in Berlin. Mitteilungen aus dem Zoologischen Museum, Berlin (4th ed.). Berlin: R. Friedländer & Sohn, 1904. v. 2, p. 1-51. Mit 4 Tafeln (6-9).), which originated from an unidentified host in Brazil (Thiele, 1904Thiele J. Beiträge zur Morphologie der Arguliden. In: Zoologisches Museum in Berlin. Mitteilungen aus dem Zoologischen Museum, Berlin (4th ed.). Berlin: R. Friedländer & Sohn, 1904. v. 2, p. 1-51. Mit 4 Tafeln (6-9).; Moreira, 1913Moreira C. Historia natural: zoologia, crustaceos. Comissão de Linhas Telegraphicas Estratégicas de Matto-Grosso ao Amazonas. 1913. 21 p. Anexo 5.). This type specimen was reexamined and illustrated (Thiele, 1904Thiele J. Beiträge zur Morphologie der Arguliden. In: Zoologisches Museum in Berlin. Mitteilungen aus dem Zoologischen Museum, Berlin (4th ed.). Berlin: R. Friedländer & Sohn, 1904. v. 2, p. 1-51. Mit 4 Tafeln (6-9).). In Brazil, A. elongatus among other branchiurans species, was recorded in Pygocentrus nattereri Kner, 1858, Serrasalmus marginatus Valenciennes, 1837, and Serrasalmus spilopleura Kner, 1858. These are all serrasalmid fish living in the Miranda river basin of the Pantanal wetland, state of Mato Grosso do Sul (Carvalho et al., 2003Carvalho LN, Del-Claro K, Takemoto RM. Host–parasite interaction between branchiurans (Crustacea: Argulidae) and piranhas (Osteichthyes: Serrasalminae) in the Pantanal wetland of Brazil. Environ Biol Fishes 2003; 67(3): 289-296. http://dx.doi.org/10.1023/A:1025899925545.
http://dx.doi.org/10.1023/A:102589992554...
). Recently, A. elongatus was recorded in Leporinus fasciatus (Bloch, 1794) [Anostomidae] and P. nattereri from the Matapi River, state of Amapá (Neves & Tavares-Dias, 2019Neves LR, Tavares-Dias M. from the Matapi River in the state of Amapá, Brazil. Rev Bras Parasitol Vet 2019; 28(3): 493-498. http://dx.doi.org/10.1590/s1984-29612019006. PMid:31188939.
http://dx.doi.org/10.1590/s1984-29612019...
).

Now, through the present study, one endemic species, B. orthotaenia, and one nonendemic species, S. hilarii (both in Bryconidae), and one introduced fish species, M.lippincottianus (Serrasalmidae), are also added as known hosts for A. elongatus in the São Francisco river basin. It is noteworthy that, over the years, not as many records of A.elongatus have been published as have been for its congeners. Therefore, a more detailed description of this ectoparasite is required, considering its hosts and its geographical distribution. As contributions to this, the present study adds three species of fish to the host list of A. elongatus, and the São Francisco river basin is added to the known geographical distribution of this ectoparasite species in Brazil.

Acknowledgements

The authors are grateful to Dr Yoshimi Sato and Dr Edson Vieira Sampaio (1stCIT/CODEVASF) for material and logistical support; to Dr Célio Magalhães, the curator of the Crustacea Collection, INPA, for deposition of voucher specimens. This study was financed in part (Master’s scholarships R Duarte and a Scientific Initiation scholarships CF Calvario) by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001; and by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the granting of Master’s scholarships (MFC Almeida-Berto), and for financial support (Basic Parasitology Edict 2012).

  • How to cite: Duarte R, Almeida-Berto MFC, Calvario CF, Santos-Clapp MD, Brasil-Sato MC. Argulus elongatus (Branchiura, Argulidae) in fish in the upper São Francisco river, Brazil. Braz J Vet Parasitol 2020; 29(2): e016119. https://doi.org/10.1590/S1984-29612020010

References

  • Brasil-Sato MC. Parasitos de peixes da bacia do São Francisco. In: Godinho HP, Godinho AL. Águas, peixes e pescadores do São Francisco das Minas Gerais Belo Horizonte: PUC Minas; 2003. p. 149-165.
  • Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227 PMid:9267395.
    » http://dx.doi.org/10.2307/3284227
  • Carvalho LN, Del-Claro K, Takemoto RM. Host–parasite interaction between branchiurans (Crustacea: Argulidae) and piranhas (Osteichthyes: Serrasalminae) in the Pantanal wetland of Brazil. Environ Biol Fishes 2003; 67(3): 289-296. http://dx.doi.org/10.1023/A:1025899925545
    » http://dx.doi.org/10.1023/A:1025899925545
  • Froese R, Pauly D, editors. 2019. Fishbase. World Wide Web eletronic publication. Version (02/2019) [online] [cited 2019 Jun 28]. Available from: http://www.fishbase.org/search.php
    » http://www.fishbase.org/search.php
  • Godinho AL, Godinho HP. Breve visão do São Francisco. In: Godinho HP, Godinho AL. Águas, peixes e pescadores do São Francisco das Minas Gerais Belo Horizonte: PUC Minas; 2003. p. 15-24.
  • Hoshino MDFG, Tavares-Dias M. Ecologia parasitária de Metynnis lippincottianus (Characiformes: Serrasalmidae) da região da Amazônia oriental, Macapá, Estado do Amapá, Brasil. Acta Sci Biol Sci 2014; 36(2): 249-255. http://dx.doi.org/10.4025/actascibiolsci.v36i2.19876
    » http://dx.doi.org/10.4025/actascibiolsci.v36i2.19876
  • Kabata Z. Diseases of fishes: crustacea as enemies of fishes. Jersey City, USA: TFH; 1970.
  • Lemos de Castro A. Branchiura. In: Schaden R. Manual de identificação de invertebrados límnicos do Brasil Brasília: CNPq/MCT; 1985. p. 1-23.
  • Moreira C. Historia natural: zoologia, crustaceos. Comissão de Linhas Telegraphicas Estratégicas de Matto-Grosso ao Amazonas 1913. 21 p. Anexo 5.
  • Neves LR, Tavares-Dias M. from the Matapi River in the state of Amapá, Brazil. Rev Bras Parasitol Vet 2019; 28(3): 493-498. http://dx.doi.org/10.1590/s1984-29612019006 PMid:31188939.
    » http://dx.doi.org/10.1590/s1984-29612019006
  • Poly WJ. Global diversity of fishlice (Crustacea: Branchiura: Argulidae) in freshwater. Hydrobiologia 2008; 595(1): 209-212. http://dx.doi.org/10.1007/s10750-007-9015-3
    » http://dx.doi.org/10.1007/s10750-007-9015-3
  • Reis RE, Kullander SO, Ferraris CJ. Check list of the freshwater fishes of South and Central America. Porto Alegre: EDIPUCRS; 2003.
  • Ringuelet R. Revisión de los Argúlidos Argentinos (Crustácea. Branchiura) con el catálago de las especies neotropicales. Rev Museo de La Plata 1943; 3(19): 43-100.
  • Sato Y, Sampaio EV. A ictiofauna do Reservatório de Três Marias, Rio São Francisco, Minas Gerais. Belo Horizonte: FUNDEP-UFMG/ SECTESMG; 2006.
  • Shibatta OA, Garavello JC. Estudo da variação geográfica em Salminus hilarii Valenciennes, 1849, das bacias do Alto Paraná e São Francisco, através da análise morfométrica multivariada em componentes principais. Naturalia (Sao Jose Rio Preto) 1993; 18: 109-116.
  • Thatcher VE. Amazon fish parasites. 2nd ed. Sofia, Moscow: Pensoft Publishers, 2006.
  • Thiele J. Beiträge zur Morphologie der Arguliden In: Zoologisches Museum in Berlin. Mitteilungen aus dem Zoologischen Museum, Berlin (4th ed.). Berlin: R. Friedländer & Sohn, 1904. v. 2, p. 1-51. Mit 4 Tafeln (6-9).
  • Woo PT, Buchmann K. Fish parasites: pathobiology and protection. London: CABI; 2012. http://dx.doi.org/10.1079/9781845938062.0000
    » http://dx.doi.org/10.1079/9781845938062.0000

Publication Dates

  • Publication in this collection
    18 May 2020
  • Date of issue
    2020

History

  • Received
    09 Sept 2019
  • Accepted
    04 Feb 2020
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