Hostname: page-component-7479d7b7d-qs9v7 Total loading time: 0 Render date: 2024-07-12T10:24:59.949Z Has data issue: false hasContentIssue false
  • English
  • Français

Ligula intestinalis (Cestoda: Diphyllobothriidae) in Kenya: a field investigation into host specificity and behavioural alterations

Published online by Cambridge University Press:  23 July 2009

J. R. BRITTON ,
M. C. JACKSON  and
D. M. HARPER
J. R. BRITTON*
Affiliation:
Centre for Conservation Ecology & Environmental Change, School of Conservation Sciences, Bournemouth University, Poole, Dorset BH12 5BB, UK
M. C. JACKSON
Affiliation:
School of Biological & Chemical Sciences, Queen Mary, University of London, Mile End Rd, London E1 4NS, UK
D. M. HARPER
Affiliation:
Department of Biology, University of Leicester, University Road, Leicester LE1 7RH, UK
*
*Corresponding author: Centre for Conservation Ecology, School of Conservation Sciences, Bournemouth University, Poole, Dorset, BH12 5BB, UK. Tel: +44 (0)120 2965384. E-mail: Rbritton@bournemouth.ac.uk.
Get access Rights & Permissions [Opens in a new window]

Summary

Within the distribution of Ligula intestinalis, a tapeworm affecting freshwater fishes, there are genetically distinct and well-separated phylogenetic clusters. East Africa is represented by a single monophyletic clade which is understudied compared with Euro-Mediterranean clades. The present field investigation in the Lake Baringo and Naivasha catchments, Kenya, revealed that this L. intestinalis clade was highly host-specific, present in only 2 of 12 fishes examined; Barbus paludinosus in Naivasha and Barbus lineomaculatus in Baringo. In infected fish, cestodes comprised up to 20% of body weight. Only 1 parasite was recorded per fish, a contrast to infected fishes in Europe where mixed infections are commonplace. In B. lineomaculatus in Baringo, only fish of greater than 64 mm in length were parasitized. The highest parasite prevalence was recorded in fish of 70–77 mm in length, and reduced for lengths of 78–84 mm. Parasitized fish were significantly associated with a particular type of habitat, occurring most frequently in shallow littoral areas, and being absent from open water and rocky shore habitats. Uninfected fish were present in all habitats. This relationship between spatial occupancy and parasite prevalence is suggested to arise from behavioural alterations induced by the parasite that promotes completion of the parasite life cycle.

Keywords

parasite prevalenceBarbus lineomaculatusBarbus paludinosusLigula intestinalis
Type
Research Article
Information
Parasitology , Volume 136 , Issue 11 , September 2009 , pp. 1367 - 1373
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arme, C. and Owen, R. W. (1968). Occurrence and pathology of Ligula intestinalis infections in British fish. Journal of Parasitology 54, 272–280.CrossRefGoogle Scholar
Barnard, C. J. and Behnke, J. M. (1990). Parasitism and Host Behaviour. Taylor and Francis, London, UK.CrossRefGoogle Scholar
Bean, C. W. and Kirkwood, R. C. (1997). First record of Ligula intestinalis from stone loach. Journal of Fish Biology 50, 455–456.Google Scholar
Bean, C. W. and Winfield, I. J. (1992). Influences of the tapeworm Ligula intestinalis (L.) on the spatial distributions of juvenile roach Rutilus rutilus (L.) and gudgeon Gobio gobio (L.) in Lough Neagh, Northern Ireland. Netherlands Journal of Zoology 42, 416–429.Google Scholar
Bouzid, W., Stefka, J., Hypsa, V., Lek, S., Scholz, T., Legal, L., Hassine, O. K. B. and Loot, G. (2008). Geography and host specificity: Two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae). International Journal for Parasitology 38, 1465–1479.Google Scholar
Britton, J. R. and Harper, D. M. (2006 a). Assessing the true status of Labeo cylindricus in Lake Baringo, Kenya. African Journal of Aquatic Science 30, 203–205.Google Scholar
Britton, J. R., Ng'eno, J. B. K., Lugonzo, J. and Harper, D. (2006 b). Can an introduced, non-indigenous species save the fisheries of Lakes Baringo and Naivasha, Kenya? In Proceedings of the XI World Lake Conference, Nairobi, Kenya, Vol. II. (ed. Odata, E. O., Olago, D. O., Ochola, W., Ntiba, M., Wandiga, S., Gichuki, N. and Oyieke, H.), pp. 568–572. ILEC: Tokyo, Japan.Google Scholar
Britton, J. R., Boar, R. R., Grey, J., Foster, J., Lugonzo, J. and Harper, D. (2007). From introduction to fishery dominance: the initial impacts of the invasive carp Cyprinus carpio in Lake Naivasha, Kenya, 1999 to 2006. Journal of Fish Biology 71 (Suppl. D), 239–257.Google Scholar
Britton, J. R. and Harper, D. M. (2008). Juvenile growth of two tilapia species in Lakes Naivasha and Baringo, Kenya. Ecology of Freshwater Fish 17, 481–488.CrossRefGoogle Scholar
Chapman, A., Hobbs, R. P., Morgan, D. L. and Gill, H. S. (2006). Helminth parasitism of Galaxias maculatus (Jenyns 1842) in southwestern Australia. Ecology of Freshwater Fish 15, 559–564.CrossRefGoogle Scholar
Cowx, I. G., Rollins, D. and Tumwebaze, R. (2008). Effect of Ligula intestinalis on the reproductive capacity of Rastrineobola argentea in Lake Victoria. Journal of Fish Biology 73, 2249–2260.CrossRefGoogle Scholar
Dejen, E., Sibbing, F. A. and Vijverberg, J. (2003). The reproductive biology of two ‘small barbs’ (Barbus humilis and Barbus tanapelagius) in Lake Tana, Ethiopia. Netherlands Journal of Zoology 52, 281–299.Google Scholar
Dejen, E., Vijverberg, J. and Sibbing, F. A. (2006). Spatial and temporal variation of cestode infection and its effects on two small barbs (Barbus humilis and Barbus tanapelagius) in Lake Tana, Ethiopia. Hydrobiologia 566, 109–117.CrossRefGoogle Scholar
Fisher, P. and Eckmann, R. (1997). Spatial distribution of littoral fish species in a large European lake, Lake Constance, Germany. Archiv für Hydrobiologie 140, 91–116.CrossRefGoogle Scholar
Giles, N. (1983). Behavioural effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the three-spined stickleback Gasterosteus aculeatus L. Animal Behaviour 31, 1192–1194.CrossRefGoogle Scholar
Giles, N. (1987). A comparison of the behavioural responses of parasitised and non-parasitised threespined sticklebacks, Gasterosteus aculeatus L., to progressive hypoxia. Journal of Fish Biology 30, 631–638.CrossRefGoogle Scholar
Gandon, S. and Michalakis, Y. (2002). Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology 15, 451–462.Google Scholar
Godin, J.-G. J. and Sproul, C. D. (1988). Risk taking in parasitised sticklebacks under threat of predation: effects of energetic need and food availability. Canadian Journal of Zoology 66, 2360–2367.CrossRefGoogle Scholar
Greischar, M. A. and Koskella, B. (2007). A synthesis of experimental work on parasite local adaptation. Ecology Letters, 10, 418–434.CrossRefGoogle ScholarPubMed
Groves, K. L. and Shields, B. A. (2001). Observations on the plerocercoid stage of the tapeworm Ligula in three species of fish from the lower crooked river of central Oregon. Journal of Aquatic Animal Health 13, 285–289.Google Scholar
Guégan, J.-F. and Kennedy, C. R. (1996). Parasite richness/Sampling effort/Host range: the fancy three-piece jigsaw Puzzle. Parasitology Today 12, 367–370.CrossRefGoogle ScholarPubMed
Harris, M. T. and Wheeler, A. (1974). Ligula infection of bleak Alburnus alburnus (L.) in the tidal Thames. Journal of Fish Biology 6, 181–188.CrossRefGoogle Scholar
Hickley, P., Muchiri, M., Boar, R. R., Britton, J. R., Adams, C., Gichuru, N. and Harper, D. (2004). Habitat degradation and subsequent fishery collapse in Lakes Naivasha and Baringo, Kenya. Ecohydrology & Hydrobiology 5, 503–517.Google Scholar
Hickley, P., North, E., Muchiri, S. M. and Harper, D. M. (1994). The diet of largemouth bass, Micropterus salmoides, in Lake Naivasha, Kenya. Journal of Fish Biology 44, 607–619.CrossRefGoogle Scholar
Kennedy, C. R. and Burrough, R. J. (1981). The establishment and subsequent history of a population of Ligula intestinalis in roach Rutilus rutilus. Journal of Fish Biology 19, 105–126.CrossRefGoogle Scholar
Lester, R. J. G. (1971). The influence of Schistocephalus plerocercoids on the respiration of Gasterosteus and a possible resulting effect on the behaviour of the fish. Canadian Journal of Zoology 49, 361–366.Google Scholar
Loot, G., Brosse, S., Lek, S. and Guegan, J. F. (2001 a). Behaviour of roach (Rutilus rutilus L.) altered by Ligula intestinalis (Cestoda: Pseudophyllidea): a field demonstration. Freshwater Biology 46, 1219–1227.Google Scholar
Loot, G., Francisco, P., Santoul, F., Lek, S. and Guegan, J. F. (2001 b). The three hosts of the Ligula intestinalis (Cestoda) life cycle in Lavernose-Lacasse gravel pit, France. Archiv für Hydrobiologie 152, 511–525.Google Scholar
Loot, G., Poulin, R., Lek, S. and Guegan, J.-F. (2002). The differential effects of Ligula intestinalis (L.) plerocercoids on host growth in three natural populations of roach, Rutilus rutilus (L.). Ecology of Freshwater Fish 11, 168–177.CrossRefGoogle Scholar
Marshall, J. and Cowx, I. G. (2003). Will the explosion of Ligula intestinalis in Rastrineobola argentea lead to another shift in the fisheries of Lake Victoria? In Interactions Between Fish and Birds: Implications for Management (ed. Cowx, I. G.), pp. 244–258. Blackwell Science Publications, Oxford, UK.CrossRefGoogle Scholar
Milinski, M. (1990). Parasites and host decision-making. In Parasitism and Host Behaviour (ed. Barnard, C. J. and Behnke, J. M.), pp. 95–116. Taylor and Francis, London, UK.Google Scholar
Museth, J. (2001). Effects of Ligula intestinalis on habitat use, predation risk and catchability in European minnows. Journal of Fish Biology 59, 1070–1080.Google Scholar
Orr, T. S. C. (1966). Spawning behaviour of Rudd, Scardinius erythrophthalmus infested with plerocercoids of Ligula intestinalis. Nature, London 12, 736.CrossRefGoogle Scholar
Pascoe, D. and Mattey, D. (1977). Dietary stress in parasitised and non-parasitised Gasterosteus aculeatus L. Zeitschrift für Parasitenkunde 51, 179–186.Google Scholar
Persson, L. and Eklov, P. (1995). Prey refuges affecting interactions between piscivorous perch and juvenile perch and roach. Ecology 76, 70–81.CrossRefGoogle Scholar
Poulin, R. (1998). Evolutionary Ecology of Parasites: from Individuals to Communities. Chapman and Hall, London, UK.Google Scholar
Sweeting, R. A. (1976). Studies on Ligula intestinalis. Effects on a roach population in gravel pit. Journal of Fish Biology 9, 515–522.Google Scholar
Taylor, M. J. and Hoole, D. (1989). Ligula Intestinalis (L.) (Cestoda: Pseudophyllidea): plerocercoid-induced changes in the spleen and pronephros of roach, Rutilus rutilus (L.), and gudgeon, Gobio gobio (L.). Journal of Fish Biology 34, 583–597.CrossRefGoogle Scholar
Wilson, R. S. (1971). The decline of a roach Rutilus rutilus (L.) population in Chew Valley Lake. Journal of Fish Biology 3, 129–137.CrossRefGoogle Scholar