Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-06-05T17:07:38.527Z Has data issue: false hasContentIssue false
  • English
  • Français

Sex ratio variation in gastrointestinal nematodes of Svalbard reindeer; density dependence and implications for estimates of species composition

Published online by Cambridge University Press:  13 December 2004

A. STIEN ,
M. DALLIMER ,
R. J. IRVINE ,
O. HALVORSEN ,
R. LANGVATN ,
S. D. ALBON  and
J. F. DALLAS
A. STIEN
Affiliation:
Department of Biology, University of Tromsø, N-9037 Tromsø, Norway
M. DALLIMER
Affiliation:
NERC Molecular Genetics in Ecology Initiative, School of Biological Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
R. J. IRVINE
Affiliation:
Centre for Ecology and Hydrology, Banchory Research Station, Glassel, Hill of Brathens, Banchory, Aberdeenshire, AB31 4BW, UK
O. HALVORSEN
Affiliation:
Zoological Museum, University of Oslo, Sarsgate. 1, N-0562 Oslo, Norway
R. LANGVATN
Affiliation:
University Courses in Svalbard (UNIS), Longyearbyen, N-9170, Norway Norwegian Institute for Nature Research (NINA), Tunasletta-2, Trondheim, N-7040, Norway
S. D. ALBON
Affiliation:
The Macaulay Institute, Craigiebuckler, Aberdeen AB15 8QH, UK
J. F. DALLAS
Affiliation:
NERC Molecular Genetics in Ecology Initiative, School of Biological Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen AB24 2TZ, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

Estimates of the intensity and abundance of species provide essential data for ecological, evolutionary and epidemiological studies of gastrointestinal nematode communities. These estimates are typically derived from the species composition of adult males when only males have readily scorable species-specific morphological traits. Such estimation assumes that all species in the community have the same adult sex ratio. We evaluated this assumption for the trichostrongyle nematodes Ostertagia gruehneri and Marshallagia marshalli in infracommunities in Svalbard reindeer by identifying to species adult females using a polymerase chain reaction assay. The proportion of males was found to be slightly higher in O. gruehneri than in M. marshalli. Evidence for seasonal variation and density dependence in the adult sex ratio was only found for O. gruehneri. Possible demographic mechanisms for such sex ratio variation are discussed, and stochastic models that generate density-dependent sex ratios proposed. Sex ratio variation caused substantial bias in some male-based estimates of intensity of infection, while substantial and consistent bias in estimates of abundances was only evident in late winter samples. Our results suggest that estimating sex ratios can be particularly important in individual host level studies of nematode species of low abundance.

Keywords

Rangifer tarandusparasitedemographic modelsMCMC methodsWinBUGS
Type
Research Article
Information
Parasitology , Volume 130 , Issue 1 , January 2005 , pp. 99 - 107
Copyright
© 2004 Cambridge University Press

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

REFERENCES

ALBON, S. D., STIEN, A., IRVINE, R. J., LANGVATN, R., ROPSTAD, E. & HALVORSEN, O. ( 2002). The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London, B 269, 1625–1632.CrossRefGoogle Scholar
ANDERSON, R. M. & MICHEL, J. F. ( 1977). Density-dependent survival in populations of Ostertagia ostertagi. International Journal for Parasitology 7, 321–329.CrossRefGoogle Scholar
BASANEZ, M. G., MARSHALL, C., CARABIN, N., GYORKOS, T. & JOSEPH, L. ( 2004). Bayesian statistics for parasitologists. Trends in Parasitology 20, 85–91.CrossRefGoogle Scholar
BORGSTEEDE, F. H. M. & HENDRIKS, J. ( 1979). Experimental infections with Cooperia oncophora (Railliet, 1918) in calves: results of single infections with two graded dose levels of larvae. Parasitology 78, 331–342.CrossRefGoogle Scholar
BROOKS, S. P. & GELMAN, A. ( 1998). General methods for monitoring convergence of iterative simulations. Journal of Computational and Graphical Statistics 7, 434–455.Google Scholar
BYE, K. & HALVORSEN, O. ( 1983). Abomasal nematodes of the Svalbard reindeer (Rangifer tarandus platyrhynchus Vrolik). Journal of Wildlife Diseases 19, 101–105.CrossRefGoogle Scholar
CROFTON, H. D. & WHITLOCK, J. H. ( 1969). Changes in sex ratio in Haemonchus contortus cayugensis. The Cornell Veterinarian 57, 388–392.Google Scholar
DALLAS, J. F., IRVINE, R. J. & HALVORSEN, O. ( 2000 a). DNA evidence that Ostertagia gruehneri and Ostertagia arctica (Nematoda: Ostertagiinnae) in reindeer from Norway and Svalbard are conspecific. International Journal for Parasitology 30, 655–658.Google Scholar
DALLAS, J. F., IRVINE, R. J. & HALVORSEN, O. ( 2001). DNA evidence that Marshallagia marshalli Ransom, 1907 and M. occidentalis Ransom, 1907 (Nematoda: Ostertagiinae) from Svalbard reindeer are conspecific. Systematic Parasitology 50, 101–103.Google Scholar
DALLAS, J. F., IRVINE, R. J., HALVORSEN, O. & ALBON, S. D. ( 2000 b). Identification by polymerase chain reaction (PCR) of Marshallagia marshalli and Ostertagia gruehneri from Svalbard reindeer. International Journal for Parasitology 30, 863–866.Google Scholar
DRÓZDZ, J. ( 1965). Studies in helminths and helminthiases in Cervidae. Part I: Revision of the subfamily Ostertagiinae Sarwar, 1956 and an attempt to explain the phylogenesis of its representatives. Acta Parasitologica Polonica 13, 445–481.Google Scholar
GIBBONS, L. M. & KHALIL, L. F. ( 1983). Morphology of the genital cone in the nematode family Trichostrongylidae and its value as taxonomic character. In Concepts in Nematode Systematics (ed. Stone, A. R., Platt, H. M. & Khalil, L. F.), pp. 261–271. Academic Press, London.
GILKS, W. R., RICHARDSON, S. & SPIEGELHALTER, D. J. ( 1996). Markov Chain Monte Carlo in Practice. Chapman and Hall/CRC, London.
HALVORSEN, O. & BYE, K. ( 1999). Parasites, biodiversity, and population dynamics in an ecosystem in the High Arctic. Veterinary Parasitology 84, 205–227.CrossRefGoogle Scholar
HALVORSEN, O., STIEN, A., IRVINE, J., LANGVATN, R. & ALBON, S. ( 1999). Evidence for continued transmission of parasitic nematodes in reindeer during the Arctic winter. International Journal for Parasitology 29, 567–579.CrossRefGoogle Scholar
HARWOOD, J. & STOKES, K. ( 2003). Coping with uncertainty in ecological advice: lessons from fisheries. Trends in Ecology and Evolution 18, 617–622.CrossRefGoogle Scholar
HAUKISALMI, V., HENTTONEN, H. & VIKMAN, P. ( 1996). Variability of sex ratio, mating probability and egg production in an intestinal nematode in its fluctuating host population. International Journal for Parasitology 26, 755–764.CrossRefGoogle Scholar
HUDSON, P. J. & DOBSON, A. P. ( 1995). Macroparasites: observed patterns. In Ecology of Infectious Diseases in Natural Populations (ed. Grenfell, B. T. & Dobson, A. P.), pp. 144–176. Cambridge University Press, Cambridge.CrossRef
IRVINE, R. J. ( 2000). Use of moxidectin treatment in the investigation of abomasal nematodiasis in wild reindeer (Rangifer tarandus platyrhynchus). Veterinary Record 147, 570–573.CrossRefGoogle Scholar
IRVINE, R. J., STIEN, A., HALVORSEN, O., LANGVATN, R. & ALBON, S. D. ( 2000). Life-history strategies and population dynamics of abomasal nematodes in Svalbard reindeer (Rangifer tarandus platyrhynchus). Parasitology 120, 297–311.CrossRefGoogle Scholar
IRVINE, R. J., STIEN, A., DALLAS, J. F., HALVORSEN, O., LANGVATN, R. & ALBON, S. D. ( 2001). Contrasting regulation of fecundity in two abomasal nematodes of Svalbard reindeer (Rangifer tarandus platyrhynchus). Parasitology 122, 673–681.CrossRefGoogle Scholar
KAO, R. R., LEATHWICK, D. M., ROBERTS, M. G. & SUTHERLAND, I. A. ( 2000). Nematode parasites of sheep: a survey of epidemiological parameters and their application in a simple model. Parasitology 121, 85–103.CrossRefGoogle Scholar
LICHTENFELS, J. R. ( 1983). The synlophe and species determination in Trichostrongyloidea. In Concepts in Nematode Systematics (ed. Stone, A. R., Platt, H. M. & Khalil, L. F.), pp. 273–291. Academic Press, London.
LICHTENFELS, J. R. & PILITT, P. A. ( 1989). Cuticular ridge pattern of Marshallagia marshalli and Ostertagia occidentalis (Nematoda: Trichostrongyloidea) parasitic in ruminants in North America. Proceedings of the Helminthological Society of Washington 56, 173–182.Google Scholar
LICHTENFELS, J. R., PILITT, P. A. & FRUETEL, M. ( 1990). Cuticular ridge pattern in Ostertagia gruehneri and Ostertagia arctica (Nematoda: Trichostrongyloidea) from caribou, Rangifer tarandus. Journal of the Helminthological Society of Washington 57, 61–68.Google Scholar
LUNN, D. J., THOMAS, A., BEST, N. & SPIEGELHALTER, D. ( 2000). WinBUGS – A Bayesian modelling framework: concepts, structure, and extensibility. Statistics and Computing 10, 325–337.CrossRefGoogle Scholar
MAY, R. M. & WOOLHOUSE, M. E. J. ( 1993). Biased sex-ratios and parasite mating probabilities. Parasitology 107, 283–295.CrossRefGoogle Scholar
McKEAND, J. B. ( 1998). Molecular diagnosis of parasitic nematodes. Parasitology 117, S87–S96.Google Scholar
POULIN, R. ( 1997 a). Covariation of sexual size dimorphism and adult sex ratio in parasitic nematodes. Biological Journal of the Linnean Society 62, 567–580.Google Scholar
POULIN, R. ( 1997 b). Population abundance and sex ratio in dioecious helminth parasites. Oecologia 111, 375–380.Google Scholar
PUGLIESE, A., ROSÀ, R. & DAMAGGIO, M. L. ( 1998). Analysis of a model for macroparasitic infections with variable aggregation and clumped infections. Journal of Mathematical Biology 36, 419–447.Google Scholar
SINGHVI, A. & JOHNSON, S. ( 1976). Numbers, sex-ratio and length of Rictularia jodhpurensis, a nematode parasite of house rat, Rattus rattus, in relation to weight of host and season. Zoologischer Anzeiger 200, 417–425.Google Scholar
STIEN, A., HALVORSEN, O. & LEINAAS, H. P. ( 1996). Density-dependent sex ratio in Echinomermella matsi (Nematoda), a parasite of the sea urchin Strongylocentrotus droebachiensis. Parasitology 112, 105–112.CrossRefGoogle Scholar
STIEN, A., IRVINE, R. J., LANGVATN, R., ALBON, S. D. & HALVORSEN, O. ( 2002 a). The population dynamics of Ostertagia gruehneri in reindeer: a model for the seasonal and intensity dependent variation in nematode fecundity. International Journal for Parasitology 32, 991–996.Google Scholar
STIEN, A., IRVINE, R. J., ROPSTAD, E., HALVORSEN, O., LANGVATN, R. & ALBON, S. D. ( 2002 b). The impact of gastrointestinal nematodes on wild reindeer: experimental and cross-sectional studies. Journal of Animal Ecology 71, 937–945.Google Scholar
VAN DER WAL, R., IRVINE, J., STIEN, A., SHEPHERD, N. & ALBON, S. D. ( 2000). Faecal avoidance and the risk of infection by nematodes in a natural population of reindeer. Oecologia 124, 19–25.CrossRefGoogle Scholar
VENABLES, W. N. & RIPLEY, B. D. ( 1999). Modern Applied Statistics with S-Plus, 3rd Edn. Springer Verlag, New York.
ZARLENGA, D. S. & HIGGINS, J. ( 2001). PCR as a diagnostic and quantitative technique in veterinary parasitology. Veterinary Parasitology 101, 215–230.CrossRefGoogle Scholar