Abstract
Freshwater ecosystems are often impacted by biological invasions, including the introduction of exotic parasites capable of infecting native species. Here, we report the occurrence of the introduced tapeworm Ligula sp. from common bully, Gobiomorphus cotidianus, and quinnat salmon, Oncorhynchus tshawytscha, in Lake Hawea, South Island, New Zealand. This parasite has a complex life cycle, reaching its adult stage in fish-eating birds. Worms recovered from the body cavity of fish hosts reached huge sizes (60–300 mm long); however, their low prevalence in fish populations suggests that infections are rare or localised. Molecular analysis (internal transcribed spacer (ITS)1 and ITS2 sequences) confirms that these specimens belong to the genus Ligula and suggests tentative routes of invasion into New Zealand. Monitoring the spread of this parasite is important, as it can impact fish populations and also, when infection levels are high, those of piscivorous birds.
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References
Arme C (1968) Effects of the plerocercoid larva of a pseudophyllidean cestode, Ligula intestinalis, on the pituitary gland and gonads of its host. Biol Bull 134(1):15–25. https://doi.org/10.2307/1539963
Arme C (1997) Ligula intestinalis: interactions with the pituitary-gonadal axis of its fish host. J Helminthol 71(02):83–84. https://doi.org/10.1017/S0022149X00015728
Barus V, Prokes M (1994) Parasite load of Ligula intestinalis plerocercoids in adult silver bream, Blicca bjoerkna. Helminthologia 31:91–94
Bouzid W, Stefka J, Hypsa V, Lek S, Scholz T, Legal L, Kalthoum O, Hassine B, Loot G (2008) Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae). Int J Parasitol 38(12):1465–1479. https://doi.org/10.1016/j.ijpara.2008.03.008
Britton JR, Jackson MC, Harper DM (2009) Ligula intestinalis (Cestoda: Diphyllobothriidae) in Kenya: a field investigation into host specificity and behavioural alterations. Parasitology 136(11):1367–1373. https://doi.org/10.1017/S003118200999059X
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. Reproduction 130(6):939–945. https://doi.org/10.1530/rep.1.00742
Chapman A, Hobbs RP, Morgan DL, Gill HS (2006) Helminth parasitism of Galaxias maculatus (Jenyns 1842) in southwestern Australia. Ecol Freshwat Fish 15(4):559–564. https://doi.org/10.1111/j.1600-0633.2006.00198.x
Cowx IG, Rollins D, Tumwebaze R (2008) Effect of Ligula intestinalis on the reproductive capacity of Rastrineobola argentea in Lake Victoria. J Fish Biol 73(9):2249–2260. https://doi.org/10.1111/j.1095-8649.2008.02058.x
Dove ADM, Fletcher AS (2000) The distribution of the introduced tapeworm Bothriocephalus acheilognathi in Australian freshwater fishes. J Helminthol 74(2):121–127
Dubinina MN (1966) Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR. Nauka Publishers, Moscow.
Dunn AM (2009) Parasites and biological invasions. Adv Parasitol 68:161–184. https://doi.org/10.1016/S0065-308X(08)00607-6
Grosholz ED (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17(1):22–27. https://doi.org/10.1016/S0169-5347(01)02358-8
Hare T (1945) Tapeworm in freshwater fish. British Med J 1(4392):347. https://doi.org/10.1136/bmj.1.4392.347-b
Hoole D, Carter V, Dufour S (2010) Ligula intestinalis (Cestoda: Pseudophyllidea): an ideal fish-metazoan parasite model? Parasitology 137(03):425–438. https://doi.org/10.1017/S0031182010000107
Jensen LA, Snoyink RJ (2005) The distribution and numbers of Australasian crested grebe (kamana) in New Zealand, January 2004. Notornis 52:34–42
Kennedy CR, Shears PC, Shears JA (2001) Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years. Parasitology 123(Pt 3):257–269
Logan FJ, Horák A, Štefka J, Aydogdu A, Scholz T (2004) The phylogeny of diphyllobothriid tapeworms (Cestoda: Pseudophyllidea) based on ITS-2 rDNA sequences. Parasitol Res 94(1):10–15. https://doi.org/10.1007/s00436-004-1164-y
Loot G, Brosse S, Lek S, Guégan J-F (2001) Behaviour of roach (Rutilus rutilus) altered by Ligula intestinalis (Cestoda: Pseudophyllidea): a field demonstration. Freshwat Biol 46(9):1219–1227. https://doi.org/10.1046/j.1365-2427.2001.00733.x
Loot G, Poulin R, Lek S, Guégan J-F (2002) The differential effects of Ligula intestinalis (L.) plerocercoids on host growth in three natural populations of roach, Rutilus rutilus (L.) Ecol Freshwat Fish 11(3):168–177. https://doi.org/10.1034/j.1600-0633.2002.00006.x
Luo H, Nie P, Yao W, Wang G, Gao Q (2003) Is the genus Digramma synonymous to the genus Ligula (Cestoda: Pseudophyllidea)? Parasitol Res 89(5):419–421. https://doi.org/10.1007/s00436-002-0802-5
Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Frontiers Ecol Environ 6(9):485–492. https://doi.org/10.1890/070064
Morgan DL (2003) Distribution and biology of Galaxias truttaceus (Galaxiidae) in south-western Australia, including first evidence of parasitism of fishes in Western Australia by Ligula intestinalis (Cestoda). Environ Biol Fish 66(2):155–167. https://doi.org/10.1023/A:1023645506913
O’Donnell, CFJ (2013) Australasian crested grebe. In: New Zealand birds online (ed. by Miskelly CM); [cited 2016 Dec 12]. Available from: http://www.nzbirdsonline.org.nz/
Olson P, Littlewood DTJ, Griffiths D, Kennedy C, Arme C (2002) Evidence for the co-existence of separate strains or species of Ligula in Lough Neagh, Northern Ireland. J Helminthol 76(2):171–174. https://doi.org/10.1079/JOH2001101
Pérez-Ponce de León G, Lagunas-Calvo O, Garcia-Prieto L, Briosio-Aguilar R, Aguilar-Aguilar R (2017) Update on the distribution of the co-invasive Schyzocotyle acheilognathi (= Bothriocephalus acheilognathi), the Asian fish tapeworm, in freshwater fishes of Mexico. J Helminthol. https://doi.org/10.1017/S0022149X17000438
Perrings C, Dehnen-Schmutz K, Touza J, Williamson M (2005) How to manage biological invasions under globalization. Trends Ecol Evol 20(5):212–215. https://doi.org/10.1016/j.tree.2005.02.011
Pleijel F, Jondelius U, Norlinder E, Nygren A, Oxelman B, Schander C, Sundberg P, Thollesson M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol Phyl Evol 48(1):369–371. https://doi.org/10.1016/j.ympev.2008.03.024
Poulin R, Paterson RA, Townsend CR, Tompkins DM, Kelly DW (2011) Biological invasions and the dynamics of endemic diseases in freshwater ecosystems. Freshwat Biol 56(4):676–688. https://doi.org/10.1111/j.1365-2427.2010.02425.x
Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19(7):385–390. https://doi.org/10.1016/j.tree.2004.05.002
Ruiz DM, Rawlings TK, Dobbs FC, Drake LA, Mullady T, Huq A, Colwell RR (2000) Global spread of microorganisms by ships. Nature 408(6808):49–50. https://doi.org/10.1038/35040695
Štefka J, Gilleard J, Grillo V, Hypša V (2007) Isolation and characterization of microsatellite loci in the tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea). Mol Ecol Notes 7(5):794–796. https://doi.org/10.1111/j.1471-8286.2007.01704.x
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729. https://doi.org/10.1093/molbev/mst197
Taraschewski H (2006) Hosts and parasites as aliens. J Helminthol 80(2):99–128. https://doi.org/10.1079/JOH2006364
Weekes PJ, Penlington B (1986) First records of Ligula intestinalis (Cestoda) in rainbow trout, Salmo gairdneri, and common bully, Gobiomorphus cotidianus, in New Zealand. J Fish Biol 28(2):183–190. https://doi.org/10.1111/j.1095-8649.1986.tb05156.x
Werle E, Schneider C, Renner M, Völker M, Fiehn W (1994) Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Res 22(20):4354–4355. https://doi.org/10.1093/nar/22.20.4354
Acknowledgements
We thank Matthias Galipaud and Ken Miller for technical assistance, as well as the following Fish & Game New Zealand staff members for logistical support: Morgan Trotter from the Dunedin office and Paul van Klink for the Cromwell office.
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Sampling and examination of bullies were carried out with permission from the University of Otago Animal Ethics Committee (permit ET 22/16).
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Lagrue, C., Presswell, B., Dunckley, N. et al. The invasive cestode parasite Ligula from salmonids and bullies on the South Island, New Zealand. Parasitol Res 117, 151–156 (2018). https://doi.org/10.1007/s00436-017-5684-7
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DOI: https://doi.org/10.1007/s00436-017-5684-7