Occurrence of Clavellisa ilishae (Copepoda: Lernaeopodidae) parasitizing herrings (Actinopterygii: Clupeidae) in Brazil

Ocorrência de Clavellisa ilishae (Copepoda: Lernaeopodidae) parasitando sardinhas (Actinopterygii: Clupeidae) no Brasil

Juliana Moreira Fabiano Paschoal Anderson Dias Cezar José Luis Luque About the authors

Abstracts

The lernaeopodids are highly specialized copepods which are widely distributed worldwide. In this paper the first record of Clavellisa ilishae Pillai, 1962 in the Neotropical region is documented parasitizing Sardinella brasiliensis from coastal zone of Rio de Janeiro, Brasil.

Sardinella brasiliensis ; ectoparasites; Clavellisa ilishae ; Neotropical region


Os lerneopodídeos são copépodes altamente especializados que estão amplamente distribuídos no mundo. Neste estudo é documentado o primeiro registro de Clavellisa ilishae Pillai, 1962 na região Neotropical, parasitando Sardinella brasiliensis do litoral do Rio de Janeiro, Brasil.

Sardinella brasiliensis ; ectoparasitos; Clavellisa ilishae ; região Neotropical


Parasitic copepods are common on marine fish, and there is a vast literature describing their taxonomy and the records on several hosts (BOXSHALL; HALSEY, 2004Boxshall GA, Halsey SH. An introduction to copepod diversity. London: The Ray Society; 2004.). In the Neotropics, copepods are the second largest parasite group in marine fishes and the third largest group in the freshwater hosts (LUQUE; POULIN, 2007Luque JL, Poulin R. Metazoan parasite species richness in Neotropical fishes: hotspots and the geography of biodiversity. Parasitology 2007; 134(6): 865-878. PMid:17291392. http://dx.doi.org/10.1017/S0031182007002272
http://dx.doi.org/10.1017/S0031182007002...
). However, there are few records of parasitic copepods on clupeid fishes in this region, essentially due to lack of parasitological studies of these hosts (LUQUE; TAVARES, 2007Luque JL, Tavares LER. Checklist of Copepoda associated with fishes from Brazil. Zootaxa 2007; 1579: 1-39.).

Sardinella brasiliensis (Steindachner, 1879) is a small pelagic fish, belonging to family Clupeidae, which form large schools, and according to Whitehead (1985) is distributed from Gulf of Mexico, Caribbean, West Indies southward to Brazil and northern Uruguay, but according to Figueiredo and Menezes (1978)Figueiredo JL, Menezes NA. Manual de Peixes marinhos do sudeste do Brasil. II Teleostei (1). São Paulo: Museu de Zoologia da USP; 1978. the distribution of S. brasiliensis is restricted to southwest Atlantic, more specifically from Rio de Janeiro to south Brazil. The Brazilian sardinella is the commercially most important fish on the southeastern Brazilian coast and is used as fresh food, canned, or processed as fishmeal for animal feed, and supports the most important fishery, with total annual catches around 150.000 t (ROSSI-WONGTSCHOWSKI et al., 2003Rossi-Wongtschowski CLDB, Clemmensen C, UeberschÄr B, Dias JF. Larval condition and growth of Sardinella brasiliensis (Steindachner, 1879): preliminary results from laboratory studies. Sci Mar 2003; 67(1): 13-23.; TEODORO et al., 2007Teodoro AJ, Andrade ECB, Mano SB. Avaliação da utilização de embalagem em atmosfera modificada sobre a conservação de sardinhas (Sardinella brasiliensis). Ciênc Tecnol Aliment 2007; 27(1): 158-161. http://dx.doi.org/10.1590/S0101-20612007000100028
http://dx.doi.org/10.1590/S0101-20612007...
).

Lernaeopodidae is a large and diverse family of highly specialized parasitic copepods, currently comprising 48 genera including Clavellisa Wilson, 1915, which consists of 12 nominal species (GURNEY, 1947Gurney R. Some notes on parasitic Copepoda. J Mar Biol Assoc United Kingdom 1947; 27(1): 133-137. http://dx.doi.org/10.1017/S0025315400014132
http://dx.doi.org/10.1017/S0025315400014...
; BOXSHALL; HALSEY, 2004Boxshall GA, Halsey SH. An introduction to copepod diversity. London: The Ray Society; 2004.). Members of Clavellisa genus are host specific, and many species have been found associated with clupeiform fishes, particularly from Indian waters (RUBEC; HOGANS, 1987Rubec LA, Hogans WE. Redescription of Clavellisa cordata Wilson, 1915 (Copepoda: Lernaeopodidae) from anadromous clupeids in eastern Canada. Can J Zool 1987; 65(6): 1559-1563. http://dx.doi.org/10.1139/z87-241
http://dx.doi.org/10.1139/z87-241...
; EL-RASHIDY; BOXSHALL, 2010El-Rashidy H, Boxshall GA. Parasitic copepods on immigrant and native clupeid fishes caught in Egyptian coastal waters off Alexandria. Syst Parasitol 2010; 76(1): 19-38. PMid:20401576. http://dx.doi.org/10.1007/s11230-010-9230-6
http://dx.doi.org/10.1007/s11230-010-923...
).

One hundred specimens of Sardinella brasiliensis, collected from coastal zone of the State of Rio de Janeiro, Brazil (21-23°S, 41-45°W) were necropsied between march 2010 and august 2011, to study their biodiversity of metazoan parasites. Four specimens were parasitized by Clavellisa ilishae (Figure 1), indicating a prevalence of 4%. After collection, the copepods were fixed and preserved in ethanol (70% GL) and were clarified with lactic acid for identification. The taxonomic determination of the parasites was in accordance with the diagnosis proposed by El-Rashidy and Boxshall (2010)El-Rashidy H, Boxshall GA. Parasitic copepods on immigrant and native clupeid fishes caught in Egyptian coastal waters off Alexandria. Syst Parasitol 2010; 76(1): 19-38. PMid:20401576. http://dx.doi.org/10.1007/s11230-010-9230-6
http://dx.doi.org/10.1007/s11230-010-923...
. Were collected a total of eleven specimens of C. ilishae, with a mean intensity of 2.75, all attached to the gills, and all copepods were sexually mature females. Specimens of C. ilishae (three females) were deposited in the Crustacea Collection of the National Museum, Rio de Janeiro (MNRJ No 23421).

Figure 1.
Clavellisa ilishaePillai, 1962Pillai NK. Copepods parasitic on South Indian fishes: Families Lernaeopodidae and Naobranchidae. Journal of the Marine Biological Association of India 1962; 4: 58-94., female. a) Habitus; b) habitus (DIC electron micrograph); c) anal laminae; d) maxillae attached to bulla.

The body of a lernaeopodid female has the maxillae fused to an anchoring structure known as a bulla, which is attached to the host (PIASECKI et al., 2004Piasecki W, Goodwin AE, Eiras JC, Nowak BF. Importance of copepoda in freshwater aquaculture. Zool Studies 2004; 43(2): 193-205.). We identified C. ilishae from the shape of the trunk, broader than long and laterally rounded, the elongate cephalothorax, details of oral appendages and its short maxillary arms, and by the presence of small caudal rami, flanking the anal laminae, on the posterior margin of the trunk, reported, until the present moment, only on this species. The dimensions of the present specimens are comparable with those given by Pillai (1962)Pillai NK. Copepods parasitic on South Indian fishes: Families Lernaeopodidae and Naobranchidae. Journal of the Marine Biological Association of India 1962; 4: 58-94., Kensley and Grindley (1973)Kensley B, Grindley JR. South African parasitic Copepoda. Ann S Afr Mus 1973; 62: 69-130. and by El-Rashidy and Boxshall (2010)El-Rashidy H, Boxshall GA. Parasitic copepods on immigrant and native clupeid fishes caught in Egyptian coastal waters off Alexandria. Syst Parasitol 2010; 76(1): 19-38. PMid:20401576. http://dx.doi.org/10.1007/s11230-010-9230-6
http://dx.doi.org/10.1007/s11230-010-923...
(Table 1).

Table 1.
Comparison of measures of Clavellisa ilishae Pillai, 1962Pillai NK. Copepods parasitic on South Indian fishes: Families Lernaeopodidae and Naobranchidae. Journal of the Marine Biological Association of India 1962; 4: 58-94..

Clavellisa ilishae was originally described by Pillai (1962)Pillai NK. Copepods parasitic on South Indian fishes: Families Lernaeopodidae and Naobranchidae. Journal of the Marine Biological Association of India 1962; 4: 58-94. and since its description this species has only been recorded parasitizing clupeiform hosts (Ilisha filigera, I. melastoma, Tenualosa ilisha, Sardinops sagax and Sardinella aurita) (KABATA, 1979Kabata Z. Parasitic Copepoda of British fishes. Ray Society, London, U.K; 1979.; PILLAI, 1985Pillai NK. The Fauna of India: Copepod parasites of marine fishes. Calcutta: Zoological Survey of India; 1985.; KENSLEY; GRINDLEY, 1973Kensley B, Grindley JR. South African parasitic Copepoda. Ann S Afr Mus 1973; 62: 69-130.; EL-RASHIDY; BOXSHALL, 2010El-Rashidy H, Boxshall GA. Parasitic copepods on immigrant and native clupeid fishes caught in Egyptian coastal waters off Alexandria. Syst Parasitol 2010; 76(1): 19-38. PMid:20401576. http://dx.doi.org/10.1007/s11230-010-9230-6
http://dx.doi.org/10.1007/s11230-010-923...
). The presence of this copepod in S. brasiliensis corroborates with the theory of host specificity on the genus by clupeiform fishes proposed by El-Rashidy and Boxshall (2010)El-Rashidy H, Boxshall GA. Parasitic copepods on immigrant and native clupeid fishes caught in Egyptian coastal waters off Alexandria. Syst Parasitol 2010; 76(1): 19-38. PMid:20401576. http://dx.doi.org/10.1007/s11230-010-9230-6
http://dx.doi.org/10.1007/s11230-010-923...
, which recorded C. ilishae parasitizing the Round sardinella Sardinella aurita in Egypt. Probably the dissemination of C. ilishae in the Neotropics occurred through the S. aurita, that is widely distributed in this region, inhabiting the continental shelves of the western Atlantic from Massachusetts (USA) throughout the Gulf of Mexico and Caribbean Sea to Rio de Janeiro (Brazil) and the eastern Atlantic at the African coasts, South Africa, and also on Mediterranean and Black Sea (FISCHER, 1978Fischer W. FAO species indentification sheets for fishery purposes. Western Central Atlantic (Fishing Area 31), Vol II. Rome: FAO; 1978.; WHITEHEAD, 1985).

There are no records of parasitic copepods on S. brasiliensis, indeed there are few records of parasitic copepods in clupeid fishes at the Brazilian waters. Montú (1980)Montú M. Parasite copepods of southern Brazilian fishes. I. Ergasilus euripedesi n.sp. (Copepoda: Cyclopoidea). Iheringia, Série Zoologia 1980; 56: 53-62. described the species Gauchergasilus (= Ergasilus) euripedesi parasitizing Brevoortia pectinata. Amado and Rocha (1996)Amado MAP, Rocha CEF. New species of parasitic copepods of the genus Acusicola (Poecilostomatoida: Ergasilidae) from gill filaments of coastal and freshwater Brazilian fishes, and proposition of Acusicola rogeri n. sp. for A. tenax sensu Cressey & Collette (1970). Hydrobiologia 1996; 324(3): 183-193. http://dx.doi.org/10.1007/BF00016390
http://dx.doi.org/10.1007/BF00016390...
described the species Acusicola brasiliensis parasitizing the gill filaments of Lile piquitinga and Opisthonema oglinum.

Lernaeopodids may affect their hosts through pathological effects, sometimes causing slight inflammation where the bulla is inserted into the host, but most damage is caused by the rasping action of the mandibles (FRYER, 1982Fryer G. The parasitic copepoda and Branchiura of British freshwater fishes: A handbook and key. Freshwater Biological Association Scientific Publications; 1982.). The habit to form schools can favor the transmission of some parasites with direct life cycle, such as copepods and monogeneans. Thereby, a massive infestation could seriously damage the host and lead to large economic losses in commercially important fishes as Brazilian sardinella.

References

  • Amado MAP, Rocha CEF. New species of parasitic copepods of the genus Acusicola (Poecilostomatoida: Ergasilidae) from gill filaments of coastal and freshwater Brazilian fishes, and proposition of Acusicola rogeri n. sp. for A. tenax sensu Cressey & Collette (1970). Hydrobiologia 1996; 324(3): 183-193. http://dx.doi.org/10.1007/BF00016390
    » http://dx.doi.org/10.1007/BF00016390
  • Boxshall GA, Halsey SH. An introduction to copepod diversity. London: The Ray Society; 2004.
  • El-Rashidy H, Boxshall GA. Parasitic copepods on immigrant and native clupeid fishes caught in Egyptian coastal waters off Alexandria. Syst Parasitol 2010; 76(1): 19-38. PMid:20401576. http://dx.doi.org/10.1007/s11230-010-9230-6
    » http://dx.doi.org/10.1007/s11230-010-9230-6
  • Figueiredo JL, Menezes NA. Manual de Peixes marinhos do sudeste do Brasil. II Teleostei (1). São Paulo: Museu de Zoologia da USP; 1978.
  • Fischer W. FAO species indentification sheets for fishery purposes. Western Central Atlantic (Fishing Area 31), Vol II. Rome: FAO; 1978.
  • Fryer G. The parasitic copepoda and Branchiura of British freshwater fishes: A handbook and key. Freshwater Biological Association Scientific Publications; 1982.
  • Gurney R. Some notes on parasitic Copepoda. J Mar Biol Assoc United Kingdom 1947; 27(1): 133-137. http://dx.doi.org/10.1017/S0025315400014132
    » http://dx.doi.org/10.1017/S0025315400014132
  • Kabata Z. Parasitic Copepoda of British fishes. Ray Society, London, U.K; 1979.
  • Kensley B, Grindley JR. South African parasitic Copepoda. Ann S Afr Mus 1973; 62: 69-130.
  • Luque JL, Poulin R. Metazoan parasite species richness in Neotropical fishes: hotspots and the geography of biodiversity. Parasitology 2007; 134(6): 865-878. PMid:17291392. http://dx.doi.org/10.1017/S0031182007002272
    » http://dx.doi.org/10.1017/S0031182007002272
  • Luque JL, Tavares LER. Checklist of Copepoda associated with fishes from Brazil. Zootaxa 2007; 1579: 1-39.
  • Montú M. Parasite copepods of southern Brazilian fishes. I. Ergasilus euripedesi n.sp. (Copepoda: Cyclopoidea). Iheringia, Série Zoologia 1980; 56: 53-62.
  • Piasecki W, Goodwin AE, Eiras JC, Nowak BF. Importance of copepoda in freshwater aquaculture. Zool Studies 2004; 43(2): 193-205.
  • Pillai NK. Copepods parasitic on South Indian fishes: Families Lernaeopodidae and Naobranchidae. Journal of the Marine Biological Association of India 1962; 4: 58-94.
  • Pillai NK. The Fauna of India: Copepod parasites of marine fishes. Calcutta: Zoological Survey of India; 1985.
  • Rossi-Wongtschowski CLDB, Clemmensen C, UeberschÄr B, Dias JF. Larval condition and growth of Sardinella brasiliensis (Steindachner, 1879): preliminary results from laboratory studies. Sci Mar 2003; 67(1): 13-23.
  • Rubec LA, Hogans WE. Redescription of Clavellisa cordata Wilson, 1915 (Copepoda: Lernaeopodidae) from anadromous clupeids in eastern Canada. Can J Zool 1987; 65(6): 1559-1563. http://dx.doi.org/10.1139/z87-241
    » http://dx.doi.org/10.1139/z87-241
  • Teodoro AJ, Andrade ECB, Mano SB. Avaliação da utilização de embalagem em atmosfera modificada sobre a conservação de sardinhas (Sardinella brasiliensis). Ciênc Tecnol Aliment 2007; 27(1): 158-161. http://dx.doi.org/10.1590/S0101-20612007000100028
    » http://dx.doi.org/10.1590/S0101-20612007000100028
  • Whitehead PJP. Clupeoid fishes of the world (suborder Clupeioidei). An annotated and illustrated catalogue of the herring, sardines, pilchards, sprats, shads, anchovies and wolfherrings. Part 1: Chirocentridae, Clupidae and Pristigasteridae. FAO; 1985. FAO Fisheries Synopsis n. 125

Publication Dates

  • Publication in this collection
    Oct-Dec 2013

History

  • Received
    15 July 2013
  • Accepted
    28 Aug 2013
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