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

  • J. R. BRITTON (a1), M. C. JACKSON (a2) and D. M. HARPER (a3)
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.

Copyright
Corresponding author
*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.
References
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Arme, C. and Owen, R. W. (1968). Occurrence and pathology of Ligula intestinalis infections in British fish. Journal of Parasitology 54, 272280.
Barnard, C. J. and Behnke, J. M. (1990). Parasitism and Host Behaviour. Taylor and Francis, London, UK.
Bean, C. W. and Kirkwood, R. C. (1997). First record of Ligula intestinalis from stone loach. Journal of Fish Biology 50, 455456.
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, 416429.
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, 14651479.
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, 203205.
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. 568572. ILEC: Tokyo, Japan.
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), 239257.
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, 481488.
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, 559564.
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, 22492260.
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, 281299.
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, 109117.
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.
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, 11921194.
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, 631638.
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, 451462.
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, 23602367.
Greischar, M. A. and Koskella, B. (2007). A synthesis of experimental work on parasite local adaptation. Ecology Letters, 10, 418434.
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, 285289.
Guégan, J.-F. and Kennedy, C. R. (1996). Parasite richness/Sampling effort/Host range: the fancy three-piece jigsaw Puzzle. Parasitology Today 12, 367370.
Harris, M. T. and Wheeler, A. (1974). Ligula infection of bleak Alburnus alburnus (L.) in the tidal Thames. Journal of Fish Biology 6, 181188.
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, 503517.
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, 607619.
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, 105126.
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, 361366.
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, 12191227.
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, 511525.
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, 168177.
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. 244258. Blackwell Science Publications, Oxford, UK.
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.
Museth, J. (2001). Effects of Ligula intestinalis on habitat use, predation risk and catchability in European minnows. Journal of Fish Biology 59, 10701080.
Orr, T. S. C. (1966). Spawning behaviour of Rudd, Scardinius erythrophthalmus infested with plerocercoids of Ligula intestinalis. Nature, London 12, 736.
Pascoe, D. and Mattey, D. (1977). Dietary stress in parasitised and non-parasitised Gasterosteus aculeatus L. Zeitschrift für Parasitenkunde 51, 179186.
Persson, L. and Eklov, P. (1995). Prey refuges affecting interactions between piscivorous perch and juvenile perch and roach. Ecology 76, 7081.
Poulin, R. (1998). Evolutionary Ecology of Parasites: from Individuals to Communities. Chapman and Hall, London, UK.
Sweeting, R. A. (1976). Studies on Ligula intestinalis. Effects on a roach population in gravel pit. Journal of Fish Biology 9, 515522.
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, 583597.
Wilson, R. S. (1971). The decline of a roach Rutilus rutilus (L.) population in Chew Valley Lake. Journal of Fish Biology 3, 129137.
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Parasitology
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