Parasitology Research

, Volume 115, Issue 9, pp 3657–3661 | Cite as

A case of complete loss of gill parasites in the invasive cichlid Oreochromis mossambicus

  • Cyril FirmatEmail author
  • Paul Alibert
  • Guillaume Mutin
  • Michèle Losseau
  • Antoine Pariselle
  • Pierre Sasal
Short Communication


This study investigates the recent evolution of a rich parasite community associated with one of the world’s most invasive species, the cichlid fish Oreochromis mossambicus. Populations from the species’ native range (Mozambique) are compared to a population from New Caledonia (Wester Pacific), an island where the species was introduced in 1954. The results support the complete local extinction of the gill parasite community in the course of the invasion process. Up to six gill parasite species per locality were documented in the O. mossambicus native range, and previous surveys consistently reported at least one parasite species introduced along African cichlid species established out of Africa. The absence of parasites in New Caledonia is therefore exceptional. This can be attributed to local factors, such as a strong initial population bottleneck, the likely absence of multiple host introductions, and the frequent occurrence of brackish watersheds that might enhance the probability for natural deparasitation.


Ancyrocephalidae Biological invasion Enemy release Monogenea Tilapia 



F. Pariela (Banhine National Park, Mozambique) provided sampling authorization (no. 0002/2009). We thank the Banhine National Park team, A. Losseau, C. Flouhr (Hytec), J.-L. Justine (MNHN), D. Lecchini (IRD), C. Poellabauer (Erbio), C. and L. Hester, A. and A. Guillas to have provided assistance for fieldwork. Sampling authorizations in New Caledonia were delivered by the Province Nord (no. 60912-2869-2009/JCC) and Province Sud (no. 11262-2009/ARR/DENV). This study is was funded by a BQR no. 2009 BQRl 01-4, and Region Bourgogne PARI no. 079. Early versions of this work benefited from the comments from T. Rigaud (Biogéosciences), U. K Schliewen (ZSM), J. Claude, and J.-F. Agnèse (ISE-M) and one anonymous reviewer.

Supplementary material

436_2016_5168_MOESM1_ESM.doc (430 kb)
ESM 1 (DOC 429 kb)


  1. Benejam L, Alcaraz C, Sasal P, Simon-Levert G, García-Berthou E (2009) Life history and parasites of the invasive mosquitofish (Gambusia holbrooki) along a latitudinal gradient. Biol Invasions 11:2265–2277. doi: 10.1007/s10530-008-9413-0 CrossRefGoogle Scholar
  2. Blakeslee AMH, Fowler AE (2012) Aquatic introductions and genetic founder effects: how do parasites compare to hosts? In: Caliskan M (ed) Genetic Diversity I. InTech, p 315–336Google Scholar
  3. Britton JR (2013) Introduced parasites in food webs: new species, shifting structures? Trends Ecol Evol 28:93–99. doi: 10.1016/j.tree.2012.08.020 CrossRefPubMedGoogle Scholar
  4. Canonico GC, Arthington A, McCrary JK, Thieme ML (2005) The effects of introduced tilapias on native biodiversity. Aquat Conserv-Mar Freshw Ecosyst 15:463–483. doi: 10.1002/aqc.699 CrossRefGoogle Scholar
  5. Cone DK, Arthur JR, Bondad-Reantaso MG (1995) Description of two new species of Gyrodactylus von Nordmann, 1832 (Monogenea) from cultured Nile Tilapia, Tilapia nilotica (Cichlidae), in the Philippines. J Helminthol Soc Wash 62:6–9Google Scholar
  6. D’Amato ME, Esterhuyse MM, van der Waal BCW, Brink D, Volckaert FAM (2007) Hybridization and phylogeography of the Mozambique tilapia Oreochromis mossambicus in southern Africa evidenced by mitochondrial and microsatellite DNA genotyping. Conserv Genet 8:475–488. doi: 10.1007/s10592-006-9186-x
  7. Firmat C (2011) Hybridization and population bottlenecks induced by human activity: population genetics, morphometrics and parasitology in the invaded and invasive tilapia Oreochromis mossambicus (Teleostei, Cichlidae). Unpublished PhD manuscript, University of BurgundyGoogle Scholar
  8. Firmat C, Alibert P (2011) One more alien freshwater fish species in New Caledonia: the three-spot gourami Trichogaster trichopterus (Teleostei: Osphronemidae) Belg J Zool 141:90–92Google Scholar
  9. Firmat C, Alibert P, Losseau M, Baroiller J-F, Schliewen UK (2013) Successive invasion-mediated interspecific hybridizations and population structure in the endangered cichlid Oreochromis mossambicus. PLoS ONE 8:e63880. doi: 10.1371/journal.pone.0063880 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Firmat C, Schliewen UK, Losseau M, Alibert P (2012) Body shape differentiation at global and local geographic scales in the invasive cichlid Oreochromis mossambicus. Biol J Linn Soc 105:369–381. doi: 10.1111/j.1095-8312.2011.01802.x
  11. Froese R, Pauly D (2011) FishBase. World Wide Web electronic publication (
  12. Gaither MR, Aeby G, Vignon M, Meguro Y, Rigby M, Runyon C, Toonen RJ, Wood CL, Bowen BW (2013) An invasive fish and the time-lagged spread of its parasite across the Hawaiian Archipelago. PLoS ONE 8:e56940. doi: 10.1371/journal.pone.0056940
  13. Global Invasive Species Database (2009) Oreochromis mossambicus. www.issgorg Accessed Nov 2015.
  14. Hadiroseyani Y, Harti LS, Nuryati DS (2009) Control of ectoparasiticmonogenean infestation on GIFT tilapia (Oreochromis sp.) using salt addition. J Akua Indo 8:31–38Google Scholar
  15. Jimenez-Garcia MI, Vidal-Martinez VM, Lopez-Jimenez S (2001) Monogeneans in introduced and native cichlids in Mexico: evidence for transfer. J Parasitol 87:907–909. doi: 10.1645/0022-3395(2001)087 PubMedGoogle Scholar
  16. Lafferty KD, Torchin ME, Kuris AM (2010) The geography of host and parasite invasions. In: Morand S, Krasnov BR (eds) The biogeography of host-parasite interactions. Oxford University Press, New York, pp 191–203Google Scholar
  17. Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460. doi: 10.1126/science.3420403 CrossRefPubMedGoogle Scholar
  18. Madanire-Moyo GN, Matla MM, Olivier PAS, Luus-Powell WJ (2011) Population dynamics and spatial distribution of monogeneans on the gills of Oreochromis mossambicus (Peters, 1852) from two lakes of the Limpopo River System. S Afr J Helminthol 85:146–152. doi: 10.1017/s0022149x10000301 CrossRefGoogle Scholar
  19. Maneepitakusanti W, Nagasawa K (2012) Monogeneans of Cichlidogyrus Paperna, 1960 (Dactylogyridae), gill parasites of tilapias, from Okinawa Prefecture, Japan. Biogeography 14:111–119Google Scholar
  20. Marquet G, Keith P, Vigneux E (2003) Atlas des poissons et des crustacés d’eau douce de Nouvelle-Calédonie vol 58. Partimoines Naturels, ParisGoogle Scholar
  21. Mendoza-Franco E, Vidal-Martínez V, Cruz-Quintana Y, León F (2006) Monogeneans on native and introduced freshwater fishes from Cuba with the description of a new species of Salsuginus Beverley-Burton, 1984 from Limia vittata (Poeciliidae). Syst Parasitol 64:181–190. doi: 10.1007/s11230-006-9030-1 CrossRefPubMedGoogle Scholar
  22. Olivier PAS, Luus-Powell WJ, Saayman JE (2009) Report on some monogenean and clinostomid infestations of freshwater fish and waterbird hosts in Middle Letaba Dam, Limpopo Province. S Afr Onderst J Veter Res 76:187–199Google Scholar
  23. Pariselle A, Euzet L (2009) Systematic revision of dactylogyridean parasites (Monogenea) from cichlid fishes in Africa, the Levant and Madagascar. Zoosystema 31:849–898. doi: 10.5252/z2009n4a6 CrossRefGoogle Scholar
  24. Paterson RA, Townsend CR, Tompkins DM, Poulin R (2012) Ecological determinants of parasite acquisition by exotic fish species. Oikos 121:1889–1895. doi: 10.1111/j.1600-0706.2012.20143.x CrossRefGoogle Scholar
  25. R Development Core Team (2013) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria ISBN 3-900051-07-0. URL
  26. Rakotofiringa SL (1986) Les Monogènes parasites de Poissons continentaux et marins de Madagascar (Taxonomie - Spécificité - Affinités). MontpellierGoogle Scholar
  27. Roche DG, Leung B, Franco EFM, Torchin ME (2010) Higher parasite richness, abundance and impact in native versus introduced cichlid fishes. Int J Parasitol 40:1525–1530. doi: 10.1016/j.ijpara.2010.05.007 CrossRefPubMedGoogle Scholar
  28. Sara JR, Smit WJ, Erasmus LJC, Ramalepe TP, Mogashoa ME, Raphahlelo ME, Theron J, Luus-Powell WJ (2013) Ecological status of Hout River Dam, Limpopo province, South Africa, using fish condition and health assessment index protocols: a preliminary investigation. Afr J Aquat Sci 39:35–43. doi: 10.2989/16085914.2013.848181 CrossRefGoogle Scholar
  29. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630. doi: 10.1038/nature01346 CrossRefPubMedGoogle Scholar
  30. Van Steenberge M, Pariselle A, Huyse T, Volckaert FAM, Snoeks J, Vanhove MPM (2015) Morphology, molecules, and monogenean parasites: an example of an integrative approach to cichlid biodiversity. PLoS One 10:e0124474. doi: 10.1371/journal.pone.0124474 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Vignon M, Sasal P, Galzin R (2009) Host introduction and parasites: a case study on the parasite community of the peacock grouper Cephalopholis argus (Serranidae) in the Hawaiian Islands. Parasitol Res 104:775–782. doi: 10.1007/s00436-008-1254-3
  32. Webb AC (2003) The ecology of invasions of non-indigeneous freshwater fish in north Queensland. PhD thesis, James Cook UniversityGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Cyril Firmat
    • 1
    • 2
    • 3
    Email author
  • Paul Alibert
    • 3
  • Guillaume Mutin
    • 3
  • Michèle Losseau
    • 4
  • Antoine Pariselle
    • 5
  • Pierre Sasal
    • 6
  1. 1.UMR 1202 BIOGECOUniversity of Bordeaux-INRACestasFrance
  2. 2.Department of Biology, Centre for Biodiversity DynamicsNorwegian University of Science and Technology (NTNU)TrondheimNorway
  3. 3.UMR CNRS 5561 Biogéosciences - Université de BourgogneDijonFrance
  4. 4.Polana Caniço AMaputoMozambique
  5. 5.IRD (ex-ORSTOM)/ISE-M, UR226/UMR5554YaoundéCameroon
  6. 6.Laboratoire d’Excellence CORAIL, USR 3278 CNRS-EPHE-UPVD CRIOBEMooreaFrench Polynesia

Personalised recommendations