Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Long-term effects of immunocontraception on wild boar fertility, physiology and behaviour

Giovanna Massei A D , Dave P. Cowan A , Julia Coats A , Fiona Bellamy A , Roger Quy A , Stéphane Pietravalle A , Matthew Brash B and Lowell A. Miller C

A Food and Environment Research Agency, Sand Hutton, York, YO26 5 LE, UK.

B ARKVETS, Givendale House, Givendale, Pocklington, YO42 ITT, UK.

C USDA APHIS National Wildlife Research Center, 4101 Laporte Avenue, Fort Collins, CO 80521, USA.

D Corresponding author. Email: giovanna.massei@fera.gsi.gov.uk

Wildlife Research 39(5) 378-385 http://dx.doi.org/10.1071/WR11196
Submitted: 29 November 2011  Accepted: 13 April 2012   Published: 28 May 2012

Abstract

Context: Fertility control appears as a publicly acceptable alternative to lethal methods for limiting population growth in wildlife. Recently developed single-dose immunocontraceptive vaccines have induced infertility in several mammals. However, the potential side-effects and the long-term effectiveness of these contraceptives have been poorly investigated.

Aims: We tested the long-term effectiveness and potential side-effects of the single-dose gonadotrophin-releasing hormone (GnRH) vaccine GonaCon™ on captive female wild boar.

Methods: We carried out two sequential trials: Trial 1 (n = 6 GonaCon™-treated and 6 control wild boar) and Trial 2 which started two years later and replicated Trial 1. We assessed the effectiveness of GonaCon™ to cause infertility by measuring GnRH antibody titres, by monitoring the oestrous cycle through the concentration of faecal progesterone and by recording the sows’ reproductive output in the 4–6 years following treatment. We evaluated the potential side-effects by monitoring behaviour, bodyweight and haematological and biochemical variables.

Key results: GnRH-antibody titres decreased with time but were still detectable in all females six years after vaccination with a single dose of GonaCon™. In Trial 1 none of the treated females gave birth in the six years after vaccination. In Trial 2, progesterone indicated that two of the six treated females were cycling. One of the cycling treated females gave birth one year after vaccination; the other five, including the second cycling sow, did not reproduce in the four years following vaccination. We found no differences in bodyweight, haematology, biochemistry and behaviour and no obvious sign of injection site reaction.

Conclusions: GonaCon™ can suppress reproduction in wild boar with no long-term effects on behaviour and physiology. Therefore, GonaCon™ can be regarded as an effective and safe contraceptive for this species.

Implications: The lack of evidence of adverse effects and the longevity of effect of GonaCon™ suggest that this contraceptive could be now tested in field trials and in contexts where culling of overabundant populations of wild boar is unfeasible, illegal or unacceptable. These instances include urban areas, parks, and management of diseases where culling might cause social perturbation and result in increased disease transmission rates.


References

Barr, J. J. F., Lurz, P. W. W., Shirley, M. D. F., and Rushton, S. P. (2002). Evaluation of immunocontraception as a publicly acceptable form of vertebrate pest species control: the introduced grey squirrel in Britain as an example. Environmental Management 30, 342–351.
Evaluation of immunocontraception as a publicly acceptable form of vertebrate pest species control: the introduced grey squirrel in Britain as an example.CrossRef | open url image1

Barrette, C., and Vandal, D. (1986). Social rank dominance, antler size and access to food in snow-bound wild woodland caribou Rangifer tarandus caribou. Behaviour 97, 118–145.
Social rank dominance, antler size and access to food in snow-bound wild woodland caribou Rangifer tarandus caribou.CrossRef | open url image1

Bradford, J. B., and Hobbs, N. T. (2008). Regulating overabundant ungulate populations: an example for elk in Rocky Mountain National Park, Colorado. Journal of Environmental Management 86, 520–528.
Regulating overabundant ungulate populations: an example for elk in Rocky Mountain National Park, Colorado.CrossRef | open url image1

Buehler, D. M., Versteegh, M. A., Matson, K. D., and Tielemanet, B. I. (2011). One problem, many solutions: simple statistical approaches help unravel the complexity of the immune system in an ecological context. PLoS ONE 64, e185992. open url image1

Caley, P., and Ramsey, D. (2001). Estimating disease transmission in wildlife, with emphasis on leptospirosis and bovine tuberculosis in possums, and effects of fertility control. Journal of Applied Ecology 38, 1362–1370.
Estimating disease transmission in wildlife, with emphasis on leptospirosis and bovine tuberculosis in possums, and effects of fertility control.CrossRef | open url image1

Carroll, M. J., Singer, A., Smith, G. C., Cowan, D. P., and Massei, G. (2010). The use of immunocontraception to improve rabies eradication in urban dog populations. Wildlife Research 37, 676–687.
The use of immunocontraception to improve rabies eradication in urban dog populations.CrossRef | open url image1

Conover, M. R. (2007). America’s first feral hog war. Human-Wildlife Conflicts 1, 129–131. open url image1

Crawford, J., Boulet, M., and Drea, C. M. (2011). Smelling wrong: hormonal contraception in lemurs alters critical female odour cues. Proceedings. Biological Sciences 278, 122–130.
Smelling wrong: hormonal contraception in lemurs alters critical female odour cues.CrossRef | 1:CAS:528:DC%2BC3MXmt1Glurc%3D&md5=9c6b71c145a6df187458366eacbe88ecCAS | open url image1

Curtis, P. D., Richmond, M. E., Miller, L. A., and Quimby, F. W. (2008). Physiological effects of gonadotropin-releasing hormone immunocontraception on white-tailed deer. Human-Wildlife Conflicts 2, 68–79. open url image1

Deigert, F. A., Duncan, A. E., Frank, K. M., Lyda, R. O., and Kirkpatrick, J. F. (2003). Immunocontraception of captive exotic species. III. Contraception and population management of fallow deer (Cervus dama). Zoo Biology 22, 261–268.
Immunocontraception of captive exotic species. III. Contraception and population management of fallow deer (Cervus dama).CrossRef | open url image1

Delsink, A. K., Van Altena, J. J., Grobler, D., Bertschinger, H., Kirkpatrick, J. F., and Slotow, R. (2006). Regulation of a small discrete African elephant population through immunocontraception in the Makalali Conservancy, Limpopo, South Africa. South African Journal of Science 102, 403–405. open url image1

Delves, P. J. (2002). Antifertility vaccines. Trends in Immunology 23, 213–219.
Antifertility vaccines.CrossRef | 1:CAS:528:DC%2BD38XitlGhs7c%3D&md5=2c438e25364cb7b63d5b1f1a76615e8cCAS | open url image1

Demas, G. E., Zysling, D. A., Beechler, B. R., Muehlenbein, M. P., and French, S. S. (2011). Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. Journal of Animal Ecology 80, 710–730.
Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts.CrossRef | open url image1

Engeman, R. M., Smith, H. T., Severson, R., Severson, M. A., Woolard, J., Shwift, S., Constantin, B. U., and Griffin, D. (2004). Damage reduction estimates and benefit–cost ratios for feral swine control from the last remnant of a basin marsh system in Florida. Environmental Conservation 31, 207–211.
Damage reduction estimates and benefit–cost ratios for feral swine control from the last remnant of a basin marsh system in Florida.CrossRef | open url image1

Fagerstone, K.A., Coffey, M. A., Curtis, P. D., Dolbeer, R. A., Killian, G. J., Miller L. A., and Wilmot, L. M. (2002).Wildlife fertility control. The Wildlife Society Technical Review 02–2.

Fagerstone, K. A., Miller, L. A., Killian, G. J., and Yoder, C. A. (2010). Review of issues concerning the use of reproductive inhibitors, with particular emphasis on resolving human–wildlife conflicts in North America. Integrative Zoology 5, 15–30.
Review of issues concerning the use of reproductive inhibitors, with particular emphasis on resolving human–wildlife conflicts in North America.CrossRef | open url image1

Gionfriddo, J. P., Eisemann, J. D., Sullivan, K. J., Healey, R. S., Miller, L. A., Fagerstone, K. A., Engeman, R. M., and Yoder, C. A. (2009). Field test of a single-injection gonadotrophin-releasing hormone immunocontraceptive vaccine in female white-tailed deer. Wildlife Research 36, 177–184.
Field test of a single-injection gonadotrophin-releasing hormone immunocontraceptive vaccine in female white-tailed deer.CrossRef | 1:CAS:528:DC%2BD1MXksVOnsLk%3D&md5=ea98678b7656090e0a4b25e26385eefeCAS | open url image1

Gionfriddo, J. P., Denicola, A. J., Miller, L. A., and Fagerstone, K. A. (2011). Health effects of GnRH immunocontraception of wild white-tailed deer in New Jersey. Wildlife Society Bulletin 35, 149–160.
Health effects of GnRH immunocontraception of wild white-tailed deer in New Jersey.CrossRef | open url image1

Gray, M. E., Thain, D. S., Cameron, E. Z., and Miller, L. A. (2010). Multi-year fertility reduction in free-roaming feral horses with single-injection immunocontraceptive formulations. Wildlife Research 37, 475–481.
Multi-year fertility reduction in free-roaming feral horses with single-injection immunocontraceptive formulations.CrossRef | 1:CAS:528:DC%2BC3cXhsVCht7%2FI&md5=7a9e58d696ead043f2580f60c224b6c0CAS | open url image1

Harrison, A., Newey, S., Gilbert, L., Haydon, D. T., and Thirgood, S. (2010). Culling wildlife hosts to control disease: mountain hares, red grouse and louping ill virus. Journal of Applied Ecology 47, 926–930.
Culling wildlife hosts to control disease: mountain hares, red grouse and louping ill virus.CrossRef | open url image1

Hobbs, N. T., Bowden, D. C., and Baker, D. L. (2000). Effects of fertility control on populations of ungulates: general, stage-structured models. Journal of Wildlife Management 64, 473–491.
Effects of fertility control on populations of ungulates: general, stage-structured models.CrossRef | open url image1

Hone, J. (2002). Feral hogs in Namadgi National Park, Australia: dynamics, impacts and management. Biological Conservation 105, 231–242.
Feral hogs in Namadgi National Park, Australia: dynamics, impacts and management.CrossRef | open url image1

Killian, G. J., Miller, L. A., Rhyan, J. C., and Doten, H. (2006a). Immunocontraception of Florida feral swine with a single-dose GnRH vaccine. American Journal of Reproductive Immunology 55, 378–384.
Immunocontraception of Florida feral swine with a single-dose GnRH vaccine.CrossRef | 1:CAS:528:DC%2BD28Xltlehtr4%3D&md5=6bfed944c7dfc64d383e48980714fcdaCAS | open url image1

Killian, G., Eisemann, J. D., Wagner, D., and Werner, J., Shaw, D., Engeman, R., and Miller, L. A. (2006b). Safety and toxicity evaluation of GonaCon immunocontraceptive vaccine in white-tailed deer. In ‘Proceedings of the 22nd Vertebrate Pest Conference’. (Eds R. M. Timm and J. M. O’Brien.) pp. 82–87. (University of California: Davis, CA.)

Killian, G., Thain, D. S., Diehl, N., Rhyan, J., and Miller, L. (2008a). Four-year contraception rates of mares treated with single-injection porcine zona pellucid and GnRH vaccines and intrauterine devices. Wildlife Research 35, 531–539.
Four-year contraception rates of mares treated with single-injection porcine zona pellucid and GnRH vaccines and intrauterine devices.CrossRef | 1:CAS:528:DC%2BD1cXht1KrtLjJ&md5=fa1d7c86b179efd890d41028b465ba53CAS | open url image1

Killian, G., Wagner, D. C., Fagerstone, K., and Miller, L. (2008b). Long-term efficacy and reproductive behaviour associated with Gonacon™ use in white-tailed deer (Odocoileus virginianus). In ‘Proceedings of the 23rd Vertebrate Pest Conference’. (Eds R. M. Timm and M. B. Madon.) pp. 240–243. (University of California: Davis, CA.)

Killian, G., Kreeger, T. J., Rhyan, J., Fagerstone, K., and Miller, L. (2009). Observations on the use of Gonacon™ in captive female elk (Cervus elaphus). Journal of Wildlife Diseases 45, 184–188. open url image1

Kirkpatrick, J. F., and Turner, A. (2007). Immunocontraception and increased longevity in equids. Zoo Biology 26, 237–244.
Immunocontraception and increased longevity in equids.CrossRef | open url image1

Kirkpatrick, J. F., Lyda, R. O., and Frank, K. M. (2011). Contraceptive vaccines for wildlife: a review. American Journal of Reproductive Immunology 66, 40–50.
Contraceptive vaccines for wildlife: a review.CrossRef | open url image1

Levy, J. K. (2011). Contraceptive vaccines for the humane control of community cat populations. American Journal of Reproductive Immunology 66, 63–70.
Contraceptive vaccines for the humane control of community cat populations.CrossRef | open url image1

Levy, J. K., Friary, J. A., Miller, L. A., Crawford, P. C., Tucker, S. J., and Fagerstone, K. A. (2011). Long-term fertility control in female cats with GonaCon™, a GnRH immunocontraceptive. Theriogenology 76, 1517–1525.
Long-term fertility control in female cats with GonaCon™, a GnRH immunocontraceptive.CrossRef | 1:CAS:528:DC%2BC3MXht12isbnF&md5=014114b167111151d3a83f60c7014a79CAS | open url image1

Long, D. B., Campbell, T. A., and Massei, G. (2010). Evaluation of feral swine-specific feeder systems. Rangelands 32, 8–13.
Evaluation of feral swine-specific feeder systems.CrossRef | open url image1

Massei, G. (in press). Fertility control in dogs. In ‘Dogs, Zoonoses and Public Health’. (Eds C. N. L. Macpherson, F. X. Meslin and A. I. Wandeler.) (CABI Publishing: Oxford.)

Massei, G., and Genov, P. (2004). The environmental impact of wild boar. Galemys 16, 135–145. open url image1

Massei, G., Cowan, D. P., Coats, J., Gladwell, F., Lane, J. E., and Miller, L. A. (2008). Effect of the GnRH vaccine GonaCon™ on the fertility, physiology and behaviour of wild boar. Wildlife Research 35, 540–547.
Effect of the GnRH vaccine GonaCon™ on the fertility, physiology and behaviour of wild boar.CrossRef | 1:CAS:528:DC%2BD1cXht1KrtLjP&md5=c48f31ad4821063c95103f6e79a39a8dCAS | open url image1

Massei, G., Quy, R., Gurney, J., and Cowan, D. P. (2010a). Can translocations be used to manage human–wildlife conflicts? Wildlife Research 37, 428–439.
Can translocations be used to manage human–wildlife conflicts?CrossRef | open url image1

Massei, G., Coats, J., Quy, R., Storer, K., and Cowan, D. P. (2010b). The BOS (Boar-Operated-System): a novel method to deliver baits to wild boar. Journal of Wildlife Management 74, 333–336.
The BOS (Boar-Operated-System): a novel method to deliver baits to wild boar.CrossRef | open url image1

Massei, G., Roy, S., and Bunting, R. (2011). Too many hogs? A review of methods to mitigate impact by wild boar and feral pigs. Human-Wildlife Interactions 5, 79–99. open url image1

McDonald, R. A., Delahay, R. J., Carter, S. P., Smith, G. C., and Cheeseman, C. L. (2008). Perturbing implications of wildlife ecology for disease control. Trends in Ecology & Evolution 23, 53–56.
Perturbing implications of wildlife ecology for disease control.CrossRef | open url image1

McLaughlin, E. A., and Aitken, R. J. (2010). Is there a role for immunocontraception? Molecular and Cellular Endocrinologyl. ePub.

Merrill, J. A., Cooch, E. G., and Curtis, P. D. (2003). Time to reduction: factors influencing management efficacy in sterilizing overabundant white-tailed deer. Journal of Wildlife Management 67, 267–279.
Time to reduction: factors influencing management efficacy in sterilizing overabundant white-tailed deer.CrossRef | open url image1

Messmer, T. A. (2009). Human–wildlife conflicts: emerging challenges and opportunities. Human–Wildlife Conflicts 3, 10–17. open url image1

Miller, L. A., Johns, B. E., and Killian, G. J. (2000). Immunocontraception of white-tailed deer with GnRH vaccine. American Journal of Reproductive Immunology 44, 266–274.
Immunocontraception of white-tailed deer with GnRH vaccine.CrossRef | 1:STN:280:DC%2BD3M7lt1Gnug%3D%3D&md5=57d0705243e3852e925133cdb321caf3CAS | open url image1

Miller, L. A., Rhyan, J. C., and Drew, M. (2004). Contraception of bison by GnRH vaccine: a possible means of decreasing transmission of brucellosis in bison. Journal of Wildlife Diseases 40, 725–730.
| 1:CAS:528:DC%2BD2MXhsV2ht74%3D&md5=95bb807b2bd5bcb7e556a52bd8a32b20CAS | open url image1

Miller, L. A., Fagerstone, K. A., Kemp, J., and Killian, G. J. (2008a). Immune mechanisms and characterization of injection site reactions involved in the multi-year contraceptive effect of the GonaCon™ vaccine. In ‘Proceedings of the 23rd Vertebrate Pest Conference’. (Eds R. M. Timm and M. B. Madon.) pp. 244–249. (University of California: Davis, CA.)

Miller, L. A., Gionfriddo, J. P., Fagerstone, K. A., Rhyan, J. C., and Killian, G. J. (2008b). The single-shot GnRH immunocontraceptive vaccine (GonaCon™) in white-tailed deer: comparison of several GnRH preparations. American Journal of Reproductive Immunology 60, 214–223.
The single-shot GnRH immunocontraceptive vaccine (GonaCon™) in white-tailed deer: comparison of several GnRH preparations.CrossRef | 1:CAS:528:DC%2BD1cXhtFKrsbzP&md5=a9c8f181a31a2002f6e58c71d6d85e06CAS | open url image1

Miller, L. A., Fagerstone, K. A., Wagner, D. C., and Killian, G. J. (2009). Factors contributing to the success of a single-shot, multiyear PZP immunocontraceptive vaccine for white-tailed deer. Human-Wildlife Conflicts 31, 103–115. open url image1

Nash, P. B., James, D. K., Hui, L., and Miller, L. A. (2004). Fertility control of California ground squirrels using GnRH immunocontraception. In ‘Proceedings of the 21st Vertebrate Pest Conference’. (Eds R. M. Timm and W. P. Gorenzel.) pp. 274–278. (University of California: Davis, CA.)

Payne, R. W. (2003). ‘Genstat 7.1 Numerical Algorithms Group.’ (VSN International: Oxford.)

Ramsey, D. (2007). Effect of fertility control on behavior and disease transmission of brush-tailed possum. Journal of Wildlife Management 71, 109–116.
Effect of fertility control on behavior and disease transmission of brush-tailed possum.CrossRef | open url image1

Ramsey, D., Spencer, N., Caley, P., Efford, M., Hansen, K., Lam, M., and Cooper, D. (2002). The effect of population density on contact rates between male and female brushtail possums Trichosurus vulpecula and the implications for transmission of bovine tuberculosis. Journal of Applied Ecology 39, 806–818.
The effect of population density on contact rates between male and female brushtail possums Trichosurus vulpecula and the implications for transmission of bovine tuberculosis.CrossRef | open url image1

Rutberg, A. T., and Naugle, R. E. (2008). Population-level effects of immunocontraception in white-tailed deer. Wildlife Research 35, 494–501.
Population-level effects of immunocontraception in white-tailed deer.CrossRef | 1:CAS:528:DC%2BD1cXht1KrtLnM&md5=9405801a6d489a1b488f0eb573ef7941CAS | open url image1

Saunders, G., McIlroy, J., Berghout, M., Kay, B., Gifford, E., Perry, R., and Van De Ven, R. (2002). The effects of induced sterility on the territorial behaviour and survival of foxes. Journal of Applied Ecology 39, 56–66.
The effects of induced sterility on the territorial behaviour and survival of foxes.CrossRef | open url image1

Smith, G. C., and Cheeseman, C. L. (2002). The control of diseases in wildlife populations: culling, vaccine and fertility control. Ecological Modelling 150, 45–53.
The control of diseases in wildlife populations: culling, vaccine and fertility control.CrossRef | open url image1

Thornton, C., and Quinn, M. S. (2009). Coexisting with cougars: public perceptions, attitudes, and awareness of cougars on the urban–rural fringe of Calgary, Alberta, Canada. Human–Wildlife Conflicts 3, 10–17. open url image1

Waddell, R. B., Osborn, D. A., Warren, R. J., Griffin, J. C., and Kesler, D. J. (2001). Prostaglandin F-2 alpha-mediated fertility control in captive white-tailed deer. Wildlife Society Bulletin 29, 1067–1074. open url image1

White, P. C. L., and Ward, A. I. (2010). Interdisciplinary approaches for the management of existing and emerging human–wildlife conflicts. Wildlife Research 37, 623–629.
Interdisciplinary approaches for the management of existing and emerging human–wildlife conflicts.CrossRef | open url image1

Yoder, C. A., and Miller, L. A. (2011). Effect of GonaCon™ vaccine on black-tailed prairie dogs: immune response and health effects. Vaccine 29, 233–239.
Effect of GonaCon™ vaccine on black-tailed prairie dogs: immune response and health effects.CrossRef | open url image1



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