Skip to main content Accessibility help
Hostname: page-component-59b7f5684b-8dvf2 Total loading time: 0.386 Render date: 2022-10-03T12:54:01.497Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "displayNetworkTab": true, "displayNetworkMapGraph": true, "useSa": true } hasContentIssue true

Spatial and temporal distribution of Ligula intestinalis (Cestoda: Diphyllobothriidea) in usipa (Engraulicypris sardella) (Pisces: Cyprinidae) in Lake Nyasa

Published online by Cambridge University Press:  18 August 2017

N.P. Gabagambi*
University of Bergen, Department of Biology, Post Box 7803, N-5020 Bergen, Norway
A. Skorping
University of Bergen, Department of Biology, Post Box 7803, N-5020 Bergen, Norway


Engraulicypris sardella is an endemic and economically important cyprinid species in Lake Nyasa/Malawi which has recently been infected by the tapeworm Ligula intestinalis. This parasite is known to induce severe pathological and behavioural effects on other cyprinids, including castration, followed by a collapse of infected populations. As a first step to understanding the dynamics between this parasite and E. sardella, we studied the spatial and temporal variation in prevalence over a period of 1 year. Overall prevalence was about 15%, but we observed a consistently higher prevalence in the littoral compared to the pelagic zone. Fish in the upper water levels showed the highest prevalence, with a marked decline with increasing water depth down to 150 m. The proportion of infected fish varied over time, with a significantly higher prevalence in the rainy season. In a huge lake like the Nyasa, with a surface area of 29,000 km2 and a maximum depth of 785 m, the transmission success of the parasite appears to show large variations in time and space. We suggest that these conditions could lead the parasite to become persistent within the lake, rather than the typical epidemic situation as observed in smaller bodies of water.

Research Paper
Copyright © Cambridge University Press 2017 

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.)


Allison, E., Irvine, K., Thompson, A. & Ngatunga, B. (1996) Diets and food consumption rates of pelagic fish in Lake Malawi, Africa. Freshwater Biology 35, 489515.CrossRefGoogle Scholar
Barbour, C.D. & Brown, J.H. (1974) Fish species diversity in lakes. The American Naturalist 108, 473489.CrossRefGoogle Scholar
Bean, C.W. & 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.CrossRefGoogle Scholar
Bootsma, H.A. & Hecky, R.E. (1993) Conservation of the African Great-Lakes – limnological perspective. Conservation Biology 7, 644656.CrossRefGoogle Scholar
Britton, J.R., Jackson, M.C. & Harper, D.M. (2009) Ligula intestinalis (Cestoda: Diphyllobothriidae) in Kenya: a field investigation into host specificity and behavioural alterations. Parasitology 136, 13671373.CrossRefGoogle ScholarPubMed
Brown, S., Loot, G., Grenfell, B. & Guégan, J. (2001) Host manipulation by Ligula intestinalis: accident or adaptation? Parasitology 123, 519529.CrossRefGoogle ScholarPubMed
Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Cowx, I.G., Rollins, D. & Tumwebaze, R. (2008) Effect of Ligula intestinalis on the reproductive capacity of Rastrineobola argentea in Lake Victoria. Journal of Fish Biology 73, 22492260.CrossRefGoogle Scholar
Degnbol, P. (1982) Food habits of larval Engraulicypris sardella in Lake Malawi: diurnal feeding pattern and comparison of size groups. FAO Fishery Expansion Project, Malawi; Biological studies on the pelagic ecosystem of Lake Malawi. Technical Report 1, pp. 5767. Rome, FAO.Google Scholar
Dejen, E., Vijverberg, J. & Sibbing, F.A. (2006) Spatial and temporal variation of cestode infection and its effects on two small Barbs (Barbus humilis and B. tanapelagius) in Lake Tana, Ethiopia. Hydrobiologia 556, 109117.CrossRefGoogle Scholar
Dianne, L., Perrot-Minnot, M.J., Bauer, A., Gaillard, M., Léger, E. & Rigaud, T. (2011) Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution 65, 26922698.CrossRefGoogle ScholarPubMed
Dobben, W.v. (1952) The food of the cormorant in the Netherlands. Ardea 40, 163.Google Scholar
Dubinina, M.N. (1980) Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR. New Delhi, Amerind Publishing.Google Scholar
Eccles, D.H. (1992) FAO species identification sheets for fishery purposes. Field guide to the freshwater fishes of Tanzania. UNDP Project URT/87/016. Rome, FAO.Google Scholar
Gopko, M., Mikheev, V.N. & Taskinen, J. (2015) Changes in host behaviour caused by immature larvae of the eye fluke: evidence supporting the predation suppression hypothesis. Behavioral Ecology and Sociobiology 69, 17231730.CrossRefGoogle Scholar
Gurevitch, J. & Padilla, D.K. (2004) Are invasive species a major cause of extinctions? Trends in Ecology & Evolution 19, 470474.CrossRefGoogle Scholar
Hafer, N. & Milinski, M. (2015) When parasites disagree: evidence for parasite-induced sabotage of host manipulation. Evolution 69, 611620.CrossRefGoogle ScholarPubMed
Hafer, N. & Milinski, M. (2016) Inter- and intraspecific conflicts between parasites over host manipulation. Proceedings of the Royal Society of London, Biological Sciences 283, 20152870.CrossRefGoogle ScholarPubMed
Kennedy, C., Shears, P. & Shears, J. (2001) Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years. Parasitology 123, 257269.CrossRefGoogle ScholarPubMed
Kennedy, C.R. (1974) A checklist of British and Irish freshwater fish parasites with notes on their distribution. Journal of Fish Biology 6, 613644.CrossRefGoogle Scholar
Kihedu, K., Mlay, M., Mwambungu, J. & Ngatunga, B. (2001) Drifting long line, a potential fishing method for the northern part of Lake Nyasa/Malawi/Niassa. Lake Malawi Fisheries Management Symposium, Lilongwe, Malawi, 4-9 June.Google Scholar
Lester, R. (1971) The influence of Schistocephalus plerocercoids on the respiration of Gasterosteus and a possible resulting effect on the behavior of the fish. Canadian Journal of Zoology 49, 361366.CrossRefGoogle Scholar
Linn, I. & Campbell, K. (1992) Interactions between white-breasted cormorants Phalacrocorax carbo (Aves: Phalacrocoracidae) and the fisheries of Lake Malawi. Journal of Applied Ecology 29, 619634.CrossRefGoogle Scholar
LNBWB (Lake Nyasa Basin Water Board). (2013) Lake Nyasa basin water board; basin annual hydrological report Nov. 2012–Dec. 2013. Ministry of Water, United Republic of Tanzania.Google Scholar
Loot, G., Brosse, S., Lek, S. & Guegan, J.F. (2001a) Behaviour of roach (Rutilus rutilus L.) altered by Ligula intestinalis (Cestoda : Pseudophyllidea): a field demonstration. Freshwater Biology 46, 12191227.CrossRefGoogle Scholar
Loot, G., Francisco, P., Santoul, F., Lek, S. & Guégan, J.-F. (2001b) The three hosts of the Ligula intestinalis (Cestoda) life cycle in Lavernose-Lacasse gravel pit, France. Archiv für Hydrobiologie 152, 511525.CrossRefGoogle Scholar
Lovell, S.J., Stone, S.F. & Fernandez, L. (2006) The economic impacts of aquatic invasive species: a review of the literature. Agricultural and Resource Economics Review 35, 195208.CrossRefGoogle Scholar
Lymbery, A.J., Morine, M., Kanani, H.G., Beatty, S.J. & Morgan, D.L. (2014) Co-invaders: the effects of alien parasites on native hosts. International Journal for Parasitology: Parasites and Wildlife 3, 171177.Google ScholarPubMed
Maguza-Tembo, F., Palsson, O. & Msiska, O. (2009) Growth and exploitation of Engraulicypris sardella in the light attraction fishery of southern Lake Malawi. Malawi Journal of Aquaculture and Fisheries (MJAF) 6, 612.Google Scholar
Marshall, J. & Cowx, I. (2003) Will the explosion of Ligula intestinalis in Rastrineobola argentea lead to another shift in the fisheries of Lake Victoria. pp. 244258 in Cowx, I.G. (Ed.) Interactions between fish and birds: Implications for management. Oxford, UK, Blackwell Science.Google Scholar
Mikheev, V.N., Pasternak, A.F., Taskinen, J. & Valtonen, E. (2010) Parasite-induced aggression and impaired contest ability in a fish host. Parasites & Vectors 3, 17.CrossRefGoogle Scholar
Milinski, M. (1990) Parasites and host decision-making. pp. 95116 in Barnad, C.J. & Behnke, J.M. (Eds) Parasitism and host behaviour. London, Taylor & Francis.Google Scholar
Moore, J. (2013) An overview of parasite-induced behavioral alterations – and some lessons from bats. Journal of Experimental Biology 216, 1117.CrossRefGoogle ScholarPubMed
Msafiri, A., Kwendwa, K., Nestory, P.G. & Alistidia, M. (2014) Assessment of the effects of plerocercoid larvae of Ligula intestinalis (Cestoda) on Engraulicypris sardella (Cyprinidae) from northern Lake Nyasa/Malawi/Niasa. Aquatic Ecosystem Health & Management 17, 9096.CrossRefGoogle Scholar
Museth, J. (2001) Effects of Ligula intestinalis on habitat use, predation risk and catchability in European minnows. Journal of Fish Biology 59, 10701080.CrossRefGoogle Scholar
Mwambungu, J., Ngatunga, B.P., Kihedu, K.J. & Mlay, M.K.L. (1996) Development of longline fishery in the Tanzania coast of Lake Nyasa. Tanzania Fisheries Research Institute Bulletin 1996, 112.Google Scholar
Ngupula, G.W., Ezekiel, C.N., Kimirei, I.A., Mboni, E. & Kashindye, B.B. (2012) Physical and chemical characteristics of the Tanzanian inshore and offshore waters of Lake Victoria in 2005–2008. African Journal of Aquatic Science 37, 339345.CrossRefGoogle Scholar
Pejchar, L. & Mooney, H.A. (2009) Invasive species, ecosystem services and human well-being. Trends in Ecology & Evolution 24, 497504.CrossRefGoogle ScholarPubMed
Poulin, R. (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Advances in the Study of Behavior 41, 151186.CrossRefGoogle Scholar
Rufli, H. & Van Lissa, J. (1982) Age and growth of Engraulicypris sardella in Lake Malawi. Biological studies on the pelagic ecosystem of Lake Malawi. FAO Technical Report 1, pp. 85–97. Rome, FAO.Google Scholar
Rusuwa, B., Ngochera, M. & Maruyama, A. (2014) Ligula intestinalis (Cestoda: Pseudophyllidea) infection of Engraulicypris sardella (Pisces: Cyprinidae) in Lake Malawi. Malawi Journal of Science and Technology 10, 814.Google Scholar
Stefka, J., Hypsa, V. & Scholz, T. (2009) Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda). Molecular Ecology 18, 11871206.CrossRefGoogle Scholar
Sweeting, R. (1976) Studies on Ligula intestinalis (L.) effects on a roach population in a gravel pit. Journal of Fish Biology 9, 515522.CrossRefGoogle Scholar
Sweeting, R. (1977) Studies on Ligula intestinalis. Some aspects of the pathology in the second intermediate host. Journal of Fish Biology 10, 4350.CrossRefGoogle Scholar
Taraschewski, H. (2006) Hosts and parasites as aliens. Journal of Helminthology 80, 99128.CrossRefGoogle ScholarPubMed
Thompson, A. (1996) Early life history of Engraulicypris sardella (Cyprinidae) in Lake Malawi. Journal of Plankton Research 18, 13491368.CrossRefGoogle Scholar
Vanacker, M., Masson, G. & Beisel, J.N. (2012) Host switch and infestation by Ligula intestinalis L. in a silver bream (Blicca bjoerkna L.) population. Parasitology 139, 406417.CrossRefGoogle Scholar
Vollmer, M.K., Bootsma, H.A., Hecky, R.E., Patterson, G., Halfman, J.D., Edmond, J.M., Eccles, D.H. & Weiss, R.F. (2005) Deep-water warming trend in Lake Malawi, East Africa. Limnology and Oceanography 50, 727732.CrossRefGoogle Scholar
Wilson, R. (1971) The decline of a roach Rutilus rutilus (L.) population in Chew Valley Lake. Journal of Fish Biology 3, 129137.CrossRefGoogle Scholar
Wyatt, R.J. & Kennedy, C.R. (1988) The effects of a change in the growth-rate of roach, Rutilus rutilus (L), on the biology of the fish tapeworm Ligula intestinalis (L). Journal of Fish Biology 33, 4557.CrossRefGoogle Scholar
Zhokhov, A.E. & Pugacheva, M.N. (2012) Distribution and occurrence of Ligula intestinalis (L.) plerocercoids (Cestoda, Ligulidae) in the fishes of Lake Tana, Ethiopia. Inland Water Biology 5, 293298.CrossRefGoogle Scholar
Cited by

Save article to Kindle

To save this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the or variations. ‘’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Spatial and temporal distribution of Ligula intestinalis (Cestoda: Diphyllobothriidea) in usipa (Engraulicypris sardella) (Pisces: Cyprinidae) in Lake Nyasa
Available formats

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

Spatial and temporal distribution of Ligula intestinalis (Cestoda: Diphyllobothriidea) in usipa (Engraulicypris sardella) (Pisces: Cyprinidae) in Lake Nyasa
Available formats

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

Spatial and temporal distribution of Ligula intestinalis (Cestoda: Diphyllobothriidea) in usipa (Engraulicypris sardella) (Pisces: Cyprinidae) in Lake Nyasa
Available formats

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *