Folia Parasitologica, vol. 62 (2015)

Folia Parasitologica 62:029 (2015) | 10.14411/fp.2015.029

Parasite richness in fish larvae from the nearshore waters of central and northern Chile

Gabriela Muñoz1, Mauricio F. Landaeta2, Pamela Palacios-Fuentes2, Zambra López3, María Teresa González3
1 Laboratorio de Parasitología Marina, Facultad de Ciencias del Mar y de Recursos Naturales, Universidad de Valparaíso, Valparaíso, Chile;
2 Laboratorio de Ictioplancton (LABITI), Facultad de Ciencias del Mar y de Recursos Naturales, Universidad de Valparaíso, Valparaíso, Chile;
3 Instituto de Ciencias Naturales 'Alexander von Humboldt', Facultad de Ciencias del Mar y Recursos Biológicos, Universidad de Antofagasta, Antofagasta, Chile

In the present study, we determine the presence of parasites in fish larvae collected from nearshore waters along the northern and central coast of Chile. The parasites were identified to the lowest possible taxonomic level based on morphological and molecular analyses. The fish sample was composed of 5 574 fish larvae. Of these, 3% harboured only larval ectoparasitic copepods whereas no endoparasites were found in the 1 141 fish evaluated for this group of parasites. The parasitic copepods collected were initially classified as 'morphotypes' according to differences in morphological characteristics. They were then analysed using molecular techniques based on the 28S and COI genes. Seven morphotypes of parasitic copepods (mostly at chalimus stages) were recognised: two of the morphotypes belonged to Pennellidae Burmeister, 1835, three to Caligidae Burmeister, 1835 and two were not identified. Only five morphotypes of copepods were analysed using molecular sequences, which confirmed the existence of six species: two pennellids of the genus Trifur Wilson, 1917 and two caligids of the genus Caligus Müller, 1785, plus two additional species that were morphologically different from these taxa. The pennellids were present in several fish species, being generally more prevalent than the caligids, in both the central and northern localities of Chile. Multispecies infections in larval fish were infrequent (< 1%). We conclude that fish larvae were rich in parasites, considering that these hosts exhibited small body sizes and were very young. We suggest that fish larvae could play a role, as intermediate hosts, in the life cycle of the parasitic copepods found.

Keywords: copepods, Pennellidae, Caligidae, fish larva assemblage, intertidal fish

Received: August 8, 2014; Accepted: February 16, 2015; Published online: June 2, 2015


References

  1. Anderson G., Dale W. 1981: Probopyrus pandalicola (Packard) (Isopoda: Epicaridae): morphology and development of larvae in culture. Crustaceana 41: 143-161. Go to original source...
  2. Anstensrud M., Schram T.A. 1988: Host and site selection by larval stages and adults of the parasitic copepod Lernaeenicus sprattae (Sowerby) (Copepoda, Pennellidae) in the Oslofjord. Hydrobiologia 47: 587-595. Go to original source...
  3. Atria G. 1977: Lista de copépodos asociados a organismos marinos en Chile (Caligoidea, Lerneapoidea, Cyclopoida). Not. Mens. Mus. Nac. Hist. Nat. 21: 2-7.
  4. Balbontín F., Llanos A., Valenzuela V. 1997: Sobreposición trófica e incidencia alimentaria en larvas de peces de Chile central. Rev. Chil. Hist. Nat. 70: 381-390.
  5. Balbontín F., Pérez R. 1979: Modalidad de postura, huevos y estados larvales de Hypsoblennius sordidus (Bennett) en la Bahía de Valparaíso (Blenniidae: Perciformes). Rev. Biol. Mar. 16: 311-318.
  6. Balbuena J.A., Karlsbakk E., Kvensenth A.M., Saksvik M., Nylund A. 2000: Growth and emigration of the third-stage larvae of Hysterotylacium aduncum (Nematoda: Anisakidae) in larval herring Clupea harengus. J. Parasitol. 86: 1271-1275. Go to original source... Go to PubMed...
  7. Bourque J.-F., Dibson J.J., Ryan D.A.J., Marcogliese D.J. 2006: Cestode parasitism as a regulator of early life-history survival in an estuary population of rainbow smelt Osmerus mordax. Mar. Ecol. Prog. Ser. 314: 295-307. Go to original source...
  8. Boxshall G. 2005: Copepoda (copepods). In: K. Rohde (Ed.), Marine Biology. CSIRO Publishing, Collingwood, pp. 123-138.
  9. Brooker A.J., Shinn A.P., Bron J.E. 2007: A review of the biology of the parasitic copepod Lernaeocera branchialis (L., 1767) (Copepoda: Pennellidae). Adv. Parasitol. 65: 297-341. Go to original source... Go to PubMed...
  10. Castro R., Baeza H. 1986: Premetamorphosis stages of two pennellids (Copepoda, Siphonostomatoida) from their definitive hosts. Crustaceana 50: 166-175. Go to original source...
  11. Contreras J.E., Landaeta M.F., Plaza G., Ojeda F.P., Bustos C.A. 2013: The contrasting hatching patterns and larval growth of two sympatric clingfishes inferred by otolith microstructure analysis. Mar. Freshwater Res. 64: 157-167. Go to original source...
  12. Cribb T.H., Pichelin S., Dufour V., Bray R.A., Chauvet C., Faliex E., Galzin R., Lo C.M., Lo-Yat A., Morand S., Rigby M.C., Sasal P. 2000: Parasites of recruiting coral fish reef larvae in New Caledonia. Int. J. Parasitol. 30: 1445-1451. Go to original source... Go to PubMed...
  13. Felley S.M., Vecchione M.L., Hare S.G.F. 1987: Incidence of ectoparasitic copepods on ichthyoplankton. Copeia 3: 778-782. Go to original source... Go to PubMed...
  14. Filatov D.A. 2002: Proseq: software for preparation and evolutionary analysis of DNA sequence datasets. Mol. Ecol. Notes 2: 621-624. Go to original source...
  15. Flores K., George-Nascimento M. 2009: Las infracomunidades de parásitos de dos especies de Scartichthys (Pisces: Blenniidae) en localidades cercanas del norte de Chile. Rev. Chil. Hist. Nat. 82: 63-71. Go to original source...
  16. Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. 1994: DNA primers for amplification of mitochondrial cytochrome c-oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotech. 3: 294-299. Go to PubMed...
  17. George-Nascimento M. 1996: Populations and assemblages of parasites in hake, Merluccius gayi, from southeastern Pacific Ocean: stock implications. J. Fish. Biol. 48: 557-568. Go to original source...
  18. George-Nascimento M., Muñoz G., Marquet A.P., Poulin R. 2004: Testing the energetic equivalence rule with helminth endoparasites of vertebrates. Ecol. Lett. 7: 527-531. Go to original source...
  19. González L. 1998: The life cycle of Hysterothylacium aduncum (Nematoda: Anisakidae) in Chilean marine farms. Aquaculture 162: 173-186. Go to original source...
  20. González L., Carvajal J. 2003: Life cycle of Caligus rogercresseyi (Copepoda: Caligidae) parasite of Chilean reared salmonids. Aquaculture 220: 101-117. Go to original source...
  21. Hebert P., Penton E., Burns J., Janzen D., Hallwachs W. 2004: Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc. Natl. Acad. Sci. U. S. A. 101: 14812-14817. Go to original source... Go to PubMed...
  22. Henriquez V., González M.T. 2014: Patterns of variation in parasite component communities and infracommunities of a littoral fish species from the northern coast of Chile. J. Helminthol. 88: 89-96. Go to original source... Go to PubMed...
  23. Herrera G. 1984: Parasitismo de juveniles de copépodos caligoideos sobre larvas de peces de la Bahía Coliumo (36 32'S; 75 57'W), Chile. Biol. Pesq. 13: 31-38. Go to PubMed...
  24. Herrera G. 1990: Incidence of anchovy (Engraulis ringens) larvae parasitized by caligid developmental stages. Bull. Mar. Sci. 47: 571-575.
  25. Herrera G.A., Llanos-Rivera A., Landaeta M.F. 2007: Larvae of the sand stargazer Sindoscopus australis and notes on the development of Dactyloscopidae (Perciformes: Blennioidei). Zootaxa 1401: 63-68. Go to original source...
  26. Ismail N., Ohtsuka S., Venmathi-Maran B.A., Tasumi S., Zaleha K., Yamashita H. 2013: Complete life cycle of a pennellid Peniculus minuticaudae Shiino, 1956 (Copepoda: Siphonostomatoida) infecting cultured threadsail filefish, Stephanolepis cirrhifer. Parasite 20: 42. Go to original source... Go to PubMed...
  27. Kabata Z. 1979: Parasitic Copepoda of British Fishes. The Ray Society, London, 468 pp.
  28. Lacerda A.C.F., Santin M., Takemoto R.M., Pavanelli G.C., Bialetzki A., Tavernari F.C. 2009: Helminths parasitizing larval fish from Pantanal, Brazil. J. Helminthol. 83: 51-55. Go to original source... Go to PubMed...
  29. Landaeta M.F., Martínez R., Bustos C.A., Castro L.R. 2013: Distribution of microplankton and fish larvae related to sharp clines in a Patagonian fjord. Rev. Biol. Mar. Oceanogr. 48: 401-407. Go to original source...
  30. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. 2007: Clustal W and Clustal X version 2.0. Bioinformatics 3: 2947-2948. Go to original source... Go to PubMed...
  31. MacKenzie K. 1974: Immature digeneans from the alimentary tract of larval and juvenile pelagic stages of haddock, Melanogrammus aeglefinus (L.). J. Fish Biol. 6: 103-106. Go to original source...
  32. Madinabeitia I., Nagasawa K. 2011: Chalimus stages of Caligus latigenitalis (Copepoda: Caligidae) parasitic on blackhead seabream from Japanese waters, with discussion of terminology used for developmental stages of caligids. J. Parasitol. 97: 221-236. Go to original source... Go to PubMed...
  33. Morais-Falavigna D.L., Machado Velho L.F., Pavanelli G.C. 2003: Proteocephalidean larvae (Cestoda) in naturally infected cyclopid copepods of the Upper Paraná River Floodplain, Brazil. Mem. Inst. Oswaldo Cruz 98: 69-72. Go to original source... Go to PubMed...
  34. Morales-Serna F.N., Hernández-Inda Z.L., Gómez S., Pérez-Ponce de León G. 2013: Redescription of Caligus serratus Shiino, 1965 (Copepoda: Caligidae) parasitic on eleven fish species from Chamela Bay in the Mexican Pacific. Acta Parasitol. 58: 367-375. Go to original source... Go to PubMed...
  35. Moyano M., Rodríguez J. M., Hernández-León S. 2009: Larval fish abundance and distribution during the late winter bloomoff Gran Canaria Island, Canary Islands. Fish. Oceanogr. 18: 51-61. Go to original source...
  36. Muñoz G. 2014: Parasite communities in the clingfish Gobiesox marmoratus from central Chile. Acta Parasitol. 59: 108-114. Go to PubMed...
  37. Muñoz G., Castro R. 2012: Comunidades de parásitos eumetazoos de peces labrisómidos de Chile central. Rev. Biol. Mar. Oceanogr. 47: 565-571. Go to original source...
  38. Muñoz G., Delorme N. 2011: Variaciones temporales de las comunidades de parásitos de peces intermareales de Chile central: hospedadores residentes vs temporales. Rev. Biol. Mar. Oceanogr. 46: 313-327. Go to original source...
  39. Muñoz G., Olmos V. 2007: Revisión bibliográfica de especies ectoparásitas y hospedadoras de sistemas acuáticos de Chile. Rev. Biol. Mar. Oceanogr. 42: 89-148.
  40. Muñoz G., Valdebenito V., George-Nascimento M. 2002: La dieta y la fauna de parásitos metazoos del torito Bovichthys chilensis Regan 1914 (Pisces: Bovichthydae) en la costa de Chile centro-sur: variaciones geográficas y ontogenéticas. Rev. Chil. Hist. Nat. 75: 661-671.
  41. Nei M., Kumar S. 2000: Molecular Evolution and Phylogenetics. Oxford University Press, London, 333 pp.
  42. Nielson J.D., Perry R.I., Scott J.S., Valerio P. 1987: Interactions of caligid ectoparasites and juvenile gadids on Georges Bank. Mar. Ecol. Prog. Ser. 39: 221-232. Go to original source...
  43. Ochoa-Muñoz M.J., Valenzuela C.P., Toledo S., Bustos C.A., Landaeta M.F. 2013: Feeding of a larval clinid fish in a microtidal estuary from southern Chile. Rev. Biol. Mar. Oceanogr. 48: 45-57. Go to original source...
  44. Oines O., Heuch P.A. 2005: Identification of sea louse species of the genus Caligus using mtDNA. J. Mar. Biol. Assoc. U. K. 85: 73-79. Go to original source...
  45. Oines O., Schram T. 2008: Intra- or inter-specific difference in genotypes of Caligus elongatus Nordmann 1832? Acta Parasitol. 53: 93-105.
  46. Palacios-Fuentes P., Landaeta M.F., Muñoz G., Plaza G., Ojeda F.P. 2012: The effects of a parasitic copepod on the recent larval growth of a fish inhabiting rocky coasts. Parasitol. Res. 111: 1661-1671. Go to original source... Go to PubMed...
  47. Pardo-Gandarillas M.C., Garcías F., George-Nascimento M. 2004: La dieta y la fauna de endoparásitos del pejesapo Gobiesox marmoratus Jenyns, 1842 (Pisces: Gobiesocidae) en el litoral de Chile están conectadas pero no correlacionadas. Rev. Chil. Hist. Nat. 77: 627-637. Go to original source...
  48. Pérez R. 1979: Desarrollo postembrionario de Tripterygion chilensis Cancino 1955, en la Bahía de Valparaíso (Tripterygiidae: Perciformes). Rev. Biol. Mar. 16: 319-329.
  49. Pérez R.1981: Desarrollo embrionario y larval de los pejesapos Sicyases sanguineus y Gobiesox marmoratus en la Bahía de Valparaíso, Chile, con notas sobre su reproducción (Gobiesocidae: Pisces). Inves. Mar. 9: 1-24.
  50. Plaza G., Landaeta M.F., Espinoza C.V., Ojeda F.P. 2013: Daily growth patterns of six species of young-of-the-year of Chilean intertidal fishes. J. Mar. Biol. Assoc. U. K. 93: 389-395. Go to original source... Go to PubMed...
  51. Posada D., Crandall K.A. 1998: Modeltest: testing the model of DNA substitution. Bioinformatics 1: 817-818. Go to original source... Go to PubMed...
  52. Radulovici A., Archambault P., Dufresne F. 2010: DNA barcoding for marine biodiversity: moving fast forward? Diversity 2: 450-472. Go to original source...
  53. Riscala-Madi R.; Tiduko-Ueta M., Ferraz-Frezza T., Müller M.I., Bazan-Simionatto K. 2011: Copépodos Notodiaptomus sp. Kiefer (Crustacea, Calanoida) naturalmente infectados com metacestódeos no reservatório do Juqueri, São Paulo, Brasil. Biota Neotrop. 11: 179-182. Go to original source...
  54. Rosenthal H. 1967: Parasites in larvae of the herring (Clupea harengus L.) fed with wild plankton. Mar. Biol. 1: 10-15. Go to original source...
  55. Rusinek O.T., Bakina M.P., Nikolskii A.V. 1996: Natural infection of the calanoid crustacean Epischura baicalensis by procercoids of Proteocephalus sp. in Listvenichnyi Bay, Lake Baikal. J. Helminthol. 70: 237-247. Go to original source...
  56. Sirois P., Dobson J.J. 2000: Influence of turbidity, food density and parasites on the ingestion and growth of larval rainbow smelt Osmerus mordax. Mar. Ecol. Prog. Ser. 193: 167-179. Go to original source...
  57. Skovgaard A., Bahlool Q.M.S., Munk P., Bege T., Buchmann K. 2011: Infection of North Sea cod, Gadus morhua L., larvae with the parasitic nematode Hysterothylacium aduncum Rudolphi. J. Plankton Res. 33: 1311-1316. Go to original source...
  58. Song Y., Wang G.T., Yao W.J., Gao Q., Nie P. 2008: Phylogeny of freshwater parasitic copepods in the Ergasilidae (Copepoda: Poecilostomatoida) based on 18S and 28S rDNA sequences. Parasitol. Res. 102: 299-306. Go to original source... Go to PubMed...
  59. Sutherland K., Strydom N.A., Wooldridge T.H. 2012: Composition, abundance, distribution and seasonality of larval fishes in the Sundays Estuary, South Africa. Afr. Zool. 47: 229-244. Go to original source...
  60. Swofford D.L. 2001: PAUP: Phylogenetic Analysis Using Parsimony (*and other methods). ver. 4.0b8. Sinauer, Sunderland, M.A.
  61. Tamura K., Nei M. 1993: Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10: 512-526. Go to PubMed...
  62. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013: MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 30: 2725-2729. Go to original source... Go to PubMed...
  63. Venmathi-Maran B.A., Moon S.Y., Ohtsuka S., Oh S-Y., Soh H.Y., Myoung J-G., Iglikowska A., Boxshall G.A. 2013: The caligid life cycle: new evidence from Lepeophtheirus elegans reconciles the cycles of Caligus and Lepeophtheirus (Copepoda: Caligidae). Parasite 20: 15. Go to original source... Go to PubMed...