Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-20T00:36:07.453Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of chewing lice (Phthiraptera: Philopteridae) as intermediate hosts in the transmission of Hymenolepis microps (Cestoda: Cyclophyllidea) from the willow ptarmigan Lagopus lagopus (Aves: Tetraonidae)

Published online by Cambridge University Press:  06 March 2017

D. Pistone ,
M. Lindgren ,
P. Holmstad ,
N.K. Ellingsen ,
H. Kongshaug ,
F. Nilsen  and
A. Skorping
D. Pistone
Affiliation:
Fish Diseases Research Group, Department of Biology, University of Bergen, PO Box 7803-5020, Bergen, Norway
M. Lindgren
Affiliation:
Department of Biology, University of Bergen, PO Box 7803, N-5006 Bergen, Norway
P. Holmstad
Affiliation:
Department of Biology, University of Bergen, PO Box 7803, N-5006 Bergen, Norway
N.K. Ellingsen
Affiliation:
Department of Biology, University of Bergen, PO Box 7803, N-5006 Bergen, Norway
H. Kongshaug
Affiliation:
SLCR-Sea Lice Research Center, Department of Biology, University of Bergen, Thormøhlensgt. 55, 5008 Bergen, Norway
F. Nilsen
Affiliation:
SLCR-Sea Lice Research Center, Department of Biology, University of Bergen, Thormøhlensgt. 55, 5008 Bergen, Norway
A. Skorping*
Affiliation:
Department of Biology, University of Bergen, PO Box 7803, N-5006 Bergen, Norway
*
*E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The cestode Hymenolepis microps is an intestinal parasite of tetraonid birds, including the willow ptarmigan (Lagopus lagopus). This parasite is able to maintain a high prevalence and intensity throughout the year, even in a subarctic environment in bird populations with relatively low host densities, indicating effective transmission routes. Willow ptarmigan consume mainly vegetal material and active consumption of invertebrates is confined to the first two or three weeks of life. Ptarmigan are infected by different species of ectoparasites, of which two species of feather lice, Lagopoecus affinis and Goniodes lagopi, are the most abundant. In this study, we explored the hypothesis that feather lice may be suitable intermediate hosts for H. microps. We applied histological techniques and light microscopy to investigate lice for the presence of larval cestode stages (cysticercoids). We found 12 cysticercoid-like structures inside chewing lice collected on L. lagopus hosts harbouring H. microps. In addition, a polymerase chain reaction (PCR) screening of Ischnocera lice DNA, targeting the 18S rRNA gene of the cestode, showed positive results for two different short fragments of the 18S rRNA gene of H. microps which were sequenced from lice collected on birds. Both independent lines of evidence support the hypothesis that Ischnocera lice might be suitable intermediate hosts in the life cycle of H. microps in L. lagopus.

Type
Research Papers
Information
Journal of Helminthology , Volume 92 , Issue 1 , January 2018 , pp. 49 - 55
Copyright
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.)

References

Andreassen, J., Ito, A., Ito, M., Nakao, M. & Nakaya, K. (2004) Hymenolepis microstoma: direct life cycle in immunodeficient mice. Journal of Helminthology 78, 1–5.Google Scholar
Bartlett, C.M. (1993) Lice (Amblycera and Ischnocera) as vectors of Eulimdana spp. (Nematoda: Filarioidea) in charadriiform birds and the necessity of short reproductive periods in adult worms. Journal of Parasitology 79, 85–91.Google Scholar
Case, A.A. & Ackert, J.E. (1940) New intermediate hosts of fowl cestodes. Transactions of the Kansas Academy of Science 43, 393–396.Google Scholar
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.CrossRefGoogle ScholarPubMed
Clayton, D.H. (1991) Coevolution of avian grooming and ectoparasites avoidance. pp. 258–289 in Loye, J.E. & Zuk, M. (Eds) Bird–parasite interactions. Oxford, Oxford University Press.Google Scholar
Conn, D.B. (1985) Life cycle and postembryonic development of Oochoristica anolis (Cyclophyllidea: Linstowiidae). Journal of Parasitology 71, 10–16.CrossRefGoogle ScholarPubMed
Cramp, S. & Simmons, K.E.L. (1980) Handbook of the birds of Europe the Middle East and North Africa. The birds of the Western Palearctic. Vol. 2. Oxford, Oxford University Press.Google Scholar
Darolova, A., Hoi, H., Kristofik, J. & Hoi, C. (2001) Horizontal and vertical ectoparasite transmission of three species of Mallophaga, and individual variation in European bee-eaters (Merops apiaster). Journal of Parasitology 87, 256–262.Google Scholar
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.Google Scholar
de Juana, E. (1994) Tetraonidae (grouse). pp. 376–410 in del Hoyo, J., Elliott, A. & Sargatol, J. (Eds) Handbook of the birds of the world. Vol. 2. Barcelona, Lynx Edicions.Google Scholar
Delahay, R.J. (1999) Cestodiasis in the red grouse in Scotland. Journal of Wildlife Diseases 35, 250–258.CrossRefGoogle ScholarPubMed
Dick, T.A. & Burt, M.D.B. (1970) The life cycle and seasonal variation of Davainea tetraoensis Fuhrmann 1919, a cestode parasite of ruffed grouse, Bonasa umbellus (L.). Canadian Journal of Zoology 49, 109–119.Google Scholar
Erikstad, K.E. & Spidsø, T.K. (1982) The influence of weather on food intake, insect prey selection and feeding behaviour in willow grouse chicks in Northern Norway. Ornis Scandinavica 13, 176–182.Google Scholar
Haukisalmi, V., Konyaev, S., Lavikainen, A., Isomursu, M. & Nakao, M. (2016) Description and life-cycle of Taenia lynciscapreoli sp. n. (Cestoda, Cyclophyllidea). ZooKeys 584, 1–23.Google Scholar
Heicher, D.S. & Gallati, W.W. (1978) Three new hosts for the cysticercoid of Hymenolepis diminuta . The Ohio Journal of Science 78, 149–151.Google Scholar
Hillgarth, N. (1996) Ectoparasite transfer during mating in ring-necked pheasants Phasanius colchicus . Journal of Avian Biology 27, 260–262.Google Scholar
Holmstad, P.R. & Skorping, A. (1998) Covariation of parasite intensities in willow ptarmigan, Lagopus lagopus L. Canadian Journal of Zoology 76, 1581–1588.Google Scholar
Holmstad, P.R., Holstad, Ø., Karbøl, G., Revhaug, J.O., Schei, E., Vandvik, V. & Skorping, A. (2004) Parasite tags in ecological studies of terrestrial hosts: a study on ptarmigan (Lagopus spp.) dispersal. Ornis Fennica 81, 128–136.Google Scholar
Holmstad, P.R., Hudson, P.J., Vandvik, V., & Skorping, A. (2005a) Can parasites synchronise the population fluctuations of sympatric tetraonids? – examining some minimum conditions. Oikos 109, 429–434.Google Scholar
Holmstad, P.R., Hudson, V. & Skorping, A. (2005b) The influence of a parasite community on the dynamics of a host population: a longitudinal study on willow ptarmigan and their parasites. Oikos 111, 377–391.Google Scholar
Holmstad, P.R., Jensen, K.H. & Skorping, A. (2008) Ectoparasite intensities are correlated with endoparasite infection loads in willow ptarmigan. Oikos 117, 515–520.Google Scholar
Huus, J. (1928) Darmparasiten des norwegiscen Moorschneehuhns (Lagopus lagopus L.). Nematoden und cestoden. Bergens Museums Årbok, Naturvidenskapelig rekke 3, 1–49.Google Scholar
Mackiewicz, J. (1988) Cestode transmission patterns. International Journal of Parasitology 74, 66–71.Google Scholar
Marshall, A.G. (1967) The cat flea, Ctenocephalides felis felis (Bouché, 1835) as an intermediate host for cestodes. Parasitology 57, 419–430.CrossRefGoogle ScholarPubMed
Marshall, A.G. (1981) The ecology of ectoparasitic insects. London, Academic Press.Google Scholar
Møller, A.P. & Rózsa, L. (2005) Parasite biodiversity and host defenses: chewing lice and immune response of their avian hosts. Oecologia 142, 169–176.Google Scholar
Nakao, M., Lavikainen, A., Iwaki, T., Haukisalmi, V., Konyaev, S., Oku, Y., Okamoto, M. & Ito, A. (2013) Molecular phylogeny of the genus Taenia (Cestoda: Taeniidae): proposals for the resurrection of Hydatigera Lamarck, 1816 and the creation of a new genus Versteria . International Journal for Parasitology 43, 427–437.Google Scholar
Padgett, K.A. & Boyce, W.M. (2005) Ants as first intermediate hosts of Mesocestoides on San Miguel Island, USA. Journal of Helminthology 79, 67–73.Google Scholar
Reid, W.M. (1991) Cestodes and trematodes. pp. 764–778 in Calnek, B.W. (Ed.) Diseases of poultry. 9th edn. Ames, Iowa, Iowa State University Press.Google Scholar
Ronquist, F. & Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Schei, E., Holmstad, P.R. & Skorping, A. (2005) Seasonal infection patterns in willow grouse (Lagopus lagopus L.) do not support the presence of parasite-induced winter losses. Ornis Fennica 82, 137–146.Google Scholar
Scholz, T., Bray, R.A., Kuchta, R. & Řepová, R. (2004) Larvae of gryporhynchid cestodes (Cyclophyllidea) from fish: a review. Folia Parasitologica 51, 131–152.Google Scholar
Shostak, A.W. (2014) Hymenolepis diminuta infections in tenebrionid beetles as a model system for ecological interactions between helminth parasites and terrestrial intermediate hosts: a review and meta-analysis. Journal of Parasitology 100, 46–58.CrossRefGoogle Scholar
Smirnova, L.V. & Kontrimavichus, V.L. (1977) Collembola as intermediate hosts of cestodes of Muridae in Chukotka. Doklady Akademii Nauk SSSR 236, 771–772.Google Scholar
Spidsø, T.K. (1980) Food selection by willow grouse Lagopus lagopus chicks in Northern Norway. Ornis Scandinavica 11, 99–105.Google Scholar
Steen, J.B. (1994) Ryper. Oslo, Gyldendal Norsk Forlag.Google Scholar
Stock, T.M. & Hunt, L.E. (1989) Site specificity of three species of lice, Mallophaga, on the willow ptarmigan, Lagopus lagopus, from Chilkat Pass, British Columbia. The Canadian Field-Naturalist 103, 584–588.Google Scholar
Thomas, V.G. (1994) Winter diet and intestinal proportions of rock and willow ptarmigan and sharp-tailed grouse in Ontario. Canadian Journal of Zoology 62, 2258–2263.Google Scholar
Valkounova, J. (1983) Morphology of cysticercoid of the tapeworm Coronacanthus integer (Hamann, 1891) (Hymenolepididae). Folia Parasitologica 30, 243–247.Google Scholar
Voge, M. (1964) Development of Hymenolepis microstoma (Cestoda: Cyclophyllidea) in the intermediate host Tribolium confusum . Journal of Parasitology 50, 77–80.Google Scholar
Voge, M. & Heyneman, D. (1957) Development of Hymenolepis nana and Hymenolepis diminuta (Cestoda: Hymenolepididae) in the intermediate host Tribolium confusum . University of California Publications in Zoology 59, 549–580.Google Scholar
Wahl, E. (1967) Etude parasito-écologique des petits mammifères (Insectivores et Rongeurs) du Val de l'Allondon (Genève). Revue Suisse de Zoologie 74, 129–188.Google Scholar
Weiss, L.M., Zhu, X., Cali, A., Tanowitz, H.B. & Wittner, M. (1994) Utility of microsporidian rRNA in diagnosis and phylogeny: a review. Folia Parasitologica 41, 81–90.Google Scholar
Wissler, K. & Halvorsen, O. (1977) Helminths from willow grouse (Lagopus lagopus) in two localities in North Norway. Journal of Wildlife Diseases 13, 409–413.CrossRefGoogle ScholarPubMed
Supplementary material: File

Pistone supplementary material

Table S1

Download Pistone supplementary material(File)
File 99.8 KB