Skip to main content
SpringerLink
Log in

Dynamics and effects of Ligula intestinalis (L.) infection in the native fish Barbus callensis Valenciennes, 1842 in Algeria

  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

The dynamics of the emergence, duration, and decline phases in epizootic cycles are well known for humans and some crops, but they are poorly understood for host–parasite systems in the wild. Parasites may be particularly insidious as they are often introduced unintentionally, simultaneously with their hosts, and later transferred to species in the new location. Here we investigate the epizootic dynamics of the tapeworm Ligula intestinalis in the Hamiz reservoir, Algeria, and explore its effects on the cyprinid fish Barbus callensis. Regular sampling was conducted from October 2005 to February 2008 with intermittent surveys carried out until 2010. Five percent of the 566 specimens of B. callensis that were caught were infected, with the maximum number of parasites found in spring. There was no obvious difference in weight between uninfected fish and infected ones, and infection did not affect fish condition. However, infected fish were significantly longer than uninfected fish and had inhibited gonad development. The proportion of infected fish caught was significantly higher in year 1 and by the second winter, infection collapsed to zero. The Ligula infection thus appeared to have minimal ecological effects and be of a temporary nature, thus exhibiting an epizootic cycle. Taken together, our data indicates that this infection declined or even failed during our study period. Failure may be due to the specific genetic strain of Ligula, but invasive carp may also have been influential in both the introduction and subsequent decline of this parasite.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Avibase 2014. The World Bird Database (24 June 2003) https://doi.org/avibase.bsc-eoc.org

    Google Scholar 

  • Barber I., Daniel Hoare D., Krause J. 2000. Effects of parasites on fish behaviour: a review and evolutionary perspective. Reviews in Fish Biology and Fisheries, 10, 131–165

    Article  Google Scholar 

  • Barson M., Marshall B.E. 2003. The occurrence of the tapeworm, Ligula intestinalis (L.), in Barbus paludinosus from a small dam in Zimbabwe. African Journal of Aquatic Science, 28, 75–78

    Article  Google Scholar 

  • Bouzid-Lamine W. 2008. Genetic structure of Ligula intestinalis (Cestoda: Diphyllobothriidea), a parasite of freshwater fish. PhD Thesis, University of Toulouse III — Paul Sabatier, France, pp. 162. (In French)

    Google Scholar 

  • Bouzid W., Štefka J., Bahri-Sfar L., Peter Beerli P., Loot G., Lek S., Haddaoui N., Hypša V., Tomáš Scholz T., Dkhil-Abbes T., Meddour R., Ben Hassine O.K. 2013. Pathways of cryptic invasion in a fish parasite traced using coalescent analysis and epidemiological survey. Biological Invasions, 15, 1907–1923. DOI: 10.1007/s10530-013-0418-y

    Article  Google Scholar 

  • Bouzid W., Stefka J., Hypsa V., Lek S., Scholz T., Legal L., Ben Hassine O.K., 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 (12), 1465–1479. DOI: 10.1016/j.ijpara.2008.03.008

    Article  CAS  Google Scholar 

  • Britton J.R., Pegg J. 2011. Ecology of European Barbel Barbus Barbus: Implications for River, Fishery, and Conservation Management. Reviews in Fisheries Science, 19, 321–330. DOI: 10.1080/10641262.2011.599886

    Article  Google 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, 1367–1373. DOI: 10.1017/S003118200999059X

    Article  CAS  Google Scholar 

  • Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. 1997. Parasitology meets Ecology on its own Terms: Margolis et al. Revised. Journal of Parasitology, 83, 575–583. DOI: 10.2307/3284227

    Article  CAS  Google Scholar 

  • Carter V., Pierce R., Dufour S., Arme C., Hoole D. 2005. The tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea) inhibits LH expression and puberty in its teleost host, Rutilus rutilus. Society for Reproduction and Fertility, 130, 939–945. DOI:10.1530/rep.1.00742

    Article  CAS  Google Scholar 

  • Cherghou S., Khodari M., Yaâkoubi F., Benadid M., Badri A. 2002. Contribution to the study of the diet of barbel, Barbus barbus callensis (Valenciennes, 1842) of a stream of the Middle Atlas (Morocco): wadi Boufekrane. Revue des sciences de l’eau, 15, 153–163. (In French)

    Article  Google Scholar 

  • Crivelli A.J. 1992. Are introduced species the right answer to the declining inland fisheries within the Mediterranean region? World Fisheries Congress, Abstract Bulletin, 143

    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, 109–117. DOI: 10.1007/s10750-005-1187-0

    Article  Google Scholar 

  • Dubinina M.N. 1980. Tapeworms, (Cestoda, Ligulidae) of the Fauna of the U.S.S.R. US Department of Commerce National Technical Information Service Springfield, USA, pp. vii + 320

    Google Scholar 

  • Dumont H.J. 1979. Limnologie van Sahara en Sahel. D Sci Thesis, University of Ghent, Belgium, pp. 557

    Google Scholar 

  • Dunn A.M., Torchin M.E., Hatcher M.J., Kotanen P.M., Blumenthal D.M., Byers J.E., Coon Courtney A.C., Frankel V.M., Holt R.D., Hufbauer R.A., Kanarek A.R., Schierenbeck K.A., Wolfe L.M., Perkins S.E. 2012. Indirect effects of parasites in invasions. Functional Ecology, 26, 1262–1274. DOI:10.1111/j.1365-2435.2012.02041.x

    Article  Google Scholar 

  • Dussart B. 1967. Copepods inland waters of Western Europe. I: calanoid and harpacticoid]. N. Boubée et Cie (eds.), Paris, pp. 1–500 (In French)

  • Dussart B. 1969. Copepods inland waters of Western Europe. II: Cyclopoids and biology. N. Boubée et Cie (eds.), Paris, 1–292 pp. (In French)

  • Ergonul M.B., Altindag A. 2005. The effects of Ligula intestinalis plerocercoids on the growth features of Tench, Tinca tinca. Turkish Journal of Veterinary and Animal Sciences, 29, 1337–1341

    Google Scholar 

  • Froese R., Pauly D. 2014. Fishbase. World Wide Web electronic publication. (version 06/2014). https://doi.org/www.fishbase.org

    Google Scholar 

  • García N., Cuttelod A., Abdul Malak D. (ed) 2010. The Status and Distribution of Freshwater Biodiversity in Northern Africa. Gland, Switzerland, Cambridge, UK, and Malaga, Spain: IUCN ISBN: 978-2-8317-1271-0, pp. 141

    Google Scholar 

  • Georgiev B.B., Angelov A., Vasileva G.P., Sánchez M.I., Hortas F., Mutafchiev Y., Pankov P., Green A.J. 2014. Larval helminths in the invasive American brine shrimp Artemia franciscana throughout its annual cycle. Acta Parasitologica, 59, 000–000. DOI: 10.2478/s11686-014-0255-x

  • Heins D.C., Baker J.A., Green D.M. 2011. Processes influencing the duration and decline of epizootics in Schistocephalus solidus. Journal of Parasitology 97, 371–376. DOI: 10.1645/GE-2699.1

    Article  Google Scholar 

  • Hoole D., Carter V., Dufour S. 2010. Ligula intestinalis (Cestoda: Pseudophyllidea): an ideal fish-metazoan parasite model? Parasitology, 137, 425–438. DOI:10.1017/S0031182010000107

    Article  CAS  Google Scholar 

  • IUCN 2014. The IUCN Red List of Threatened Species. Version 3.2014. https://doi.org/www.iucnredlist.org

    Google Scholar 

  • Jobling S., Tyler C.R. 2003. Endocrine disruption, parasites and pollutants in wild freshwater fish. Parasitology, 126, S103–S107 DOI: 10.1017/S0031182003003652

    Article  CAS  Google Scholar 

  • Kennedy C.R. 1993. Introductions, spread and colonization of new localities by fish helminth and crustacean parasites in the British Isles: A perspective ans appraisal. Journal of Fish Biology, 43, 287–301

    Article  Google Scholar 

  • Kennedy C.R., Burrough R.J. 1981. The establishment and subsequent history of a population of Ligula intestinalis in roach Rutilus rutilus (L.), Journal of Fish Biology, 19, 105–126. DOI: 10.1111/j.1095-8649.1981.tb05815.x

    Article  Google Scholar 

  • Kennedy C.R., Shears P.C., Shears J.A. 2001. Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years. Parasitology, 123, 257–269. DOI: 10.1017/S0031182001008538

    Article  CAS  Google Scholar 

  • Korkmaz A.S., Zencir O. 2009. Annual dynamics of tapeworm, Ligula intestinalis parasitism in Tench (Tinca tinca) from Beysehir Lake, Turkey. Journal of Animal and Veterinary Advances, 8, 1790–1793

    Google Scholar 

  • Kraïem M.M. 1994. Systematics, biogeography and bio- ecology of Barbus callensis Valenciennes, 1842 (fish, Cyprinidae) in Tunisia. PhD Thesis, Biol. Fac. Sci., Tunisia, pp. 227 (In French)

    Google Scholar 

  • Kraïem M.M. 1996. The diet of Barbus callensis (Cyprinidae) in Northern Tunisia. Cybium, 20, 75–85

    Google Scholar 

  • Kroupova H., Trubiroha A., Wuertz S., Frank S.N., Sures B., Kloas W. 2012. Nutritional status and gene expression along the somatotropic axis in roach (Rutilus rutilus) infected with the tapeworm Ligula intestinalis. General and Comparative Endocrinology, 177, 270–277. DOI: 10.1016/j.ygcen.2012. 04.007

    Article  CAS  Google Scholar 

  • Lafferty K.D., Torchin M.E., Kuris A.M. 2010. The geography of host and parasite invasions Pages 191–202 in S. Morand and B. Krasnow, eds. The Geography of Host-Parasite Interactions. Oxford University Press, Oxford, U.K.

    Google Scholar 

  • Lévêque C., Daget J. 1984. Cyprinidae. In: CLOFFA 1: Check List of the Freshwater Fishes of Africa (Dajet J., Gosse J.P. & Thys van den Audenaerde D.F.E.), Orstom & Tervuren: MRAC (eds.), Paris, pp. 410

    Google Scholar 

  • Loot G., Francisco P., Santoul F., Lek S., Guegan J.F. 2001. The three hosts of the Ligula intestinalis (Cestoda) life cycle in Lavernose-Lacasse gravel pit, France. Archiv fur Hydrobiologie, 152, 511–525

    Article  Google Scholar 

  • Loot G., Aulagnier S., Lek S., Thomas F., Guegan J.F. 2002. Experimental demonstration of a behavioural modification in a cyprinid fish, Rutilus rutilus (L.), induced by a parasite, Ligula intestinalis (L.). Canadian Journal of Zoology, 80, 738–744

    Article  Google Scholar 

  • Margolis L., Esch G.W., Holmes J.C., Kuris A.M., Schad G.A. 1982. The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). Journal of Parasitology, 68, 131–133

    Article  Google Scholar 

  • 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, 90–96. DOI: 10.1080/14634988.2014.875444A

    Article  Google Scholar 

  • Nash R.D.M., Valencia A.H., Geffen A.J. 2006. The origin of Fulton’s condition factor- setting the record straight. Fisheries, 31, 236–238

    Google Scholar 

  • Ould Rouis S., Ould Rouis A., Micha J.C., Arab A. 2012. Reproductive biology of the Cyprinidae, Barbus callensis in an Algerian Dam. Tropicultura, 30, 88–93. (In French)

    Google Scholar 

  • Parsa Khanghah A., Mojazi Amiri B., Sharifpour I., Jalali jafari B., Motalebi A.A. 2011. Gonad tissue changes of Chalcalburnus mossulensis (Heckel, 1843) infected by Ligula intestinalis (cestoda). Iranian Journal of Fisheries Sciences, 10, 85–94

    Google Scholar 

  • Piasecki W., Goodwin A.E., Eiras J.C., Nowak B.F. 2004. Importance of Copepoda in freshwater aquaculture. Zoological Studies, 43, 193–205

    Google Scholar 

  • Pyšek P., Richardson D.M. 2010. Invasive Species, Environmental Change and Management, and Health. Annu. Rev. Environ. Resour., 35, 25–55. DOI: 10.1146/annurev-environ-033009-095548

    Article  Google Scholar 

  • Quinnell R.J., Grafen A., Woolhouse M.E.J. 1995. Changes in parasite aggregation with age: a discrete infection model. Parasitology, 111, 635–644

    Article  Google Scholar 

  • Reiczigel J., Rózsa L. 2005. Quantitative Parasitology 3.0. Budapest, Hungary. Distributed by the authors

    Google Scholar 

  • Richardson D.M., Pyšek P., Rejmánek M., Barbour M.G., Dane Panetta F., West C.J. 2000. Naturalization and Invasion of Alien Plants: Concepts and Definitions. Diversity and Distributions, 6, 93–107

    Article  Google Scholar 

  • Samraoui B., Samraoui F. 2008. An ornithological survey of Algerian wetlands: Important bird areas, Ramsar sites and threatened species. Wildfowl, 58, 71–96

    Google Scholar 

  • Samraoui F., Alfarhan A.H., Al-Rasheid K.A.S., Samraoui B. 2011. An appraisal of the status and distribution of waterbirds of Algeria: indicators of global changes? Ardeola, 58, 137–163

    Article  Google Scholar 

  • Simberloff D., Rejmánek M. 2010. Encyclopedia of Biological Invasions University of California Press, pp. 792

    Google Scholar 

  • Simberloff D., Martin J.L., Genovesi P., Maris V., Wardle D.A., Aronson J., Courchamp F., Galil B., Garcıà-Berthou E., Pascal M., Pyšek P., Sousa R., Tabacchi E., Vilà M. 2013. Impacts of biological invasions: what’s what and the way forward. Trends in Ecology & Evolution, Ce Press, 28, 58–66. DOI: 10.1016/j.tree.2012.07.013

    Google Scholar 

  • Sitjà-Bobadilla A. 2008. Living off a fish: A trade-off between parasites and the immune system. Fish & Shellfish Immunology, 25, 358–372. DOI: 10.1016/j.fsi.2008.03.018

    Article  CAS  Google Scholar 

  • Sitjà-Bobadilla A. 2009. Can Myxosporean parasites compromise fish and amphibian reproduction? Proc. R. Soc. B., 276, 2861–2870. DOI: 10.1098/rspb.2009.0368

    Article  Google Scholar 

  • Trubiroha A., Kroupova H., Frank S.N., Sures B., Kloas W. 2010. Inhibition of gametogenesis by the cestode Ligula intestinalis in roach (Rutilus rutilus) is attenuated under laboratory conditions. Parasitology, 138, 648–659. DOI: 10.1017/S0031182010001514

    Article  CAS  Google Scholar 

  • Turgut E., Develi N., Yeşilayer N., Buhan E. 2011. Seasonal Occurrence of Ligula intestinalis infection in Cyprinids from Almus Dam Lake, Turkey. Kahramanmaras Sutcu Imam University Journal of Natural Sciences, 14, 9–11

    Google Scholar 

  • Urdeş L., Hangan M. 2013. The Epidemiology of Ligula intestinalis (Phylum Platyhelminthes) within the Cyprinid Populations Inhabiting the Danubian Delta Area. Animal Science and Biotechnologies, 46, 273–276

    Google Scholar 

  • Vulpe V. 2002. Parasitic invasions on fish stocks of N-E area from Moldavia. Revista Scientia Parasitologica, 3, 144–149

    Google Scholar 

  • Yen Nhi T.T., Mohd Shazili N.A., Shaharom-Harrison F. 2013. Use of cestodes as indicator of heavy metal pollution. Experimental Parasitology, 133, 75–79. DOI: 10.1016/j.exppara.2012.10.014

    Article  CAS  Google 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, 293–298. DOI: 10.1134/S1995082912020162

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Biological Sciences (FSB), Department of Ecology and Environment, Laboratory of Dynamic and Biodiversity, University of Science and Technology Houari Boumediene (USTHB) BP 32, El Alia Bab-Ezzouar, 16111, Algiers, Algeria

    Sonia Ould Rouis, Abdelhalim Ould Rouis & Abdeslem Arab

  2. Department of Biology, Limnology Section, Ghent University, Ledeganckstraat 35, Ghent, B-9000, Belgium

    Henri J. Dumont

  3. South African Institute for Aquatic Biodiversity, Grahamstown, 6139, South Africa

    Kit Magellan

  4. Department of Ecology and Institute of Hydrobiology, Jinan University, Guangzhou, 510632, China

    Henri J. Dumont

Authors
  1. Sonia Ould Rouis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abdelhalim Ould Rouis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Henri J. Dumont
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kit Magellan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abdeslem Arab
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sonia Ould Rouis.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rouis, S.O., Rouis, A.O., Dumont, H.J. et al. Dynamics and effects of Ligula intestinalis (L.) infection in the native fish Barbus callensis Valenciennes, 1842 in Algeria. Acta Parasit. 61, 307–318 (2016). https://doi.org/10.1515/ap-2016-0041

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1515/ap-2016-0041

Keywords

Search

Navigation