Immunocontraception of mammalian wildlife: ecological and immunogenetic issues

in Reproduction
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  • 1 Australian and New Zealand Conservation Laboratories, School of Biological, Earth and Environmental Sciences, The University of New South Wales, Sydney, New South Wales 2052, Australia

Correspondence should be addressed to D W Cooper; Email: des.cooper@unsw.edu.au

Immunocontraception involves stimulating immune responses against gametes or reproductive hormones thus preventing conception. The method is being developed for the humane control of pest and overabundant populations of mammalian wildlife. This paper examines three fundamental issues associated with its use: (1) the difficulties of obtaining responses to self-antigens, (2) the likely evolution of genetically based non-response to immunocontraceptive agents, and (3) the possible changes in the array of pathogens possessed by the target species after generations of immunocontraception. Our review of the literature demonstrates that the barriers to an effective immunocontraceptive are at present very basic. Should they be overcome, the effects of immunocontraception on the immunogenetic constitution of wildlife populations through the selection for non-responders must be examined. We suggest that the attempt to use the animal’s own immune system to modulate reproduction may be incompatible with the basic biological function of protection against infectious disease. Research programs on mammalian immunocontraception should involve measurement of the heritability of non-response and an assessment of the likely change in the response of the contracepted population to possible pathogens.

Abstract

Immunocontraception involves stimulating immune responses against gametes or reproductive hormones thus preventing conception. The method is being developed for the humane control of pest and overabundant populations of mammalian wildlife. This paper examines three fundamental issues associated with its use: (1) the difficulties of obtaining responses to self-antigens, (2) the likely evolution of genetically based non-response to immunocontraceptive agents, and (3) the possible changes in the array of pathogens possessed by the target species after generations of immunocontraception. Our review of the literature demonstrates that the barriers to an effective immunocontraceptive are at present very basic. Should they be overcome, the effects of immunocontraception on the immunogenetic constitution of wildlife populations through the selection for non-responders must be examined. We suggest that the attempt to use the animal’s own immune system to modulate reproduction may be incompatible with the basic biological function of protection against infectious disease. Research programs on mammalian immunocontraception should involve measurement of the heritability of non-response and an assessment of the likely change in the response of the contracepted population to possible pathogens.

Introduction

The regulation of human and animal population numbers constitutes a difficult and largely unsolved contemporary problem. In the developed world, steroid contraceptives for humans are both widely used and efficacious. Elsewhere they are too costly. The development of less expensive methods is considered necessary (Aitken et al. 1993). One such method is immunocontraception, i.e. the vaccination against sperm, eggs, or reproductive hormones to prevent either fertilization or the production of gametes. Attempts to design human immunocontraception have a long history (Joshi 1973, Stevens 1975, Basten 1988, Gupta & Talwar 1994). The targets include sperm antigens, oocyte antigens, especially zona pellucida proteins (PZP), gonadotropin riboflavin carrier protein, gonadotropins and gonadotropin releasing hormones (Delves et al. 2002). The most advanced method involves immunization against human chorionic gonadotropin, in reality a method of very early pregnancy termination (Baird 2000). It now seems likely that problems associated with autoimmune disease and variability of response will prevent any widespread use of immunocontraception in humans in the foreseeable future (Rao 2001, Aitken 2002). Women’s health advocates have objected to all forms of immunocontraception because of perceived health risks and the potential for political abuse of the vaccine (Richter 1994). Human male immunocontraceptives have received much less attention and do not appear to be feasible in the near future (Delves et al. 2002).

Immunocontraceptives for wild animals have a different objective than those for humans. Their main aim is to check population growth rather than to contracept particular individuals. If some animals are irreversibly sterilized so much the better whereas such an effect in human medicine would be ethically most undesirable. Immunocontraceptives for animals are ostensibly humane and could potentially be used on the large scale required for wildlife population regulation. Research progress to date has been reviewed in Tyndale-Biscoe (1991, 1994), Barber & Fayrer-Hosken (2000), Barlow (2000), and Cooper & Herbert (2001). Three fundamental questions remain to be addressed: (1) Can sufficiently strong immune responses be provoked against the antigens (immunogens) of gametes or reproductive hormones to cause contraception in a proportion of animals large enough for effective population management? (2) How rapidly will variation in these responses lead to the evolution of failure to respond to the immunocontraceptive agent? (3) What will be the ecological consequences of the likely changes to the immunogenetic constitution of the population as a result of selection for non-responders? In particular, will the endemic pathogens of the species change? There is considerable information which allows us to answer at least in part the first two questions. The third is of fundamental importance but even a preliminary answer is not possible at present.

Target species

Population control of native and exotic mammals is generally justified by environmental degradation, competition with and predation on native wildlife, conflicts with humans over food production, potential spread of pathogenic infectious diseases and the possibility of population crashes of over-abundant fauna or of wildlife populations near urban areas. Although still in its infancy, immunocontraception is regarded as being more humane than the traditional methods of wildlife population control, such as shooting, trapping, poisoning, or pathogenic agents and its use has strong support from influential animal welfare agencies worldwide (Oogjes 1997, Grandy & Rutberg 2002). Table 1 lists mammalian species for which immunocontraception is being investigated and for which the method could be applied. In all these species, there are at present no completely efficacious, cost-effective, or socially acceptable methods for population regulation available.

Immune responses to self-antigens

Responses to self-antigens are unusual and mainly weak. This constitutes a major barrier to the development of an immunocontraceptive. Table 2 summarizes data on attempts to induce immunocontraception using a variety of antigens in 14 mammalian species. The data in Table 2 show that in most cases a significant proportion of the population is not contracepted by administration of the immunocontraceptive antigen. The reason for this could be either genetic or environmental. In either case it indicates that a fraction of the population will continue to breed despite the administration of the contraceptive. In most cases, there is likely to be at least in part genetic causes underlying lack of response. If so, the genes for lack of response will be selected for and in a comparatively small number of generations most of the population will be non-responsive. This implies that the immunocontraceptive can be useful for only a short period of time.

All studies summarized in Table 2 involve the use of some kind of adjuvant, i.e. a substance or array of substances designed to enhance the immune response. There are no reports of successful immunocontraception without some form of adjuvant. Moreover, most immunizations were boosted at least once (see Table 2). The need for multiple injections and the dependence upon adjuvant to achieve the necessary level of response renders the whole approach impractical at present. The most commonly used adjuvant, Freund’s Adjuvant, also induces a range of undesirable side effects and its use is being challenged on animal welfare grounds (Leenaars et al. 1994, 1998). There is at present no feasible or acceptable method of promoting responses to self-antigens sufficient to cause immunocontraception.

Jackson et al.(2001) attempted to overcome the problem of lack of immune response to self-antigens in the absence of adjuvant by inserting the cytokine interleukin-4 into mousepox virus with the intention of increasing the humoral response. The virus was then inserted into the mice with the unwelcome outcome that the mice all died very quickly. This work caused alarm because of the possibility that this technology could lead to a method for simple conversion of relatively innocuous viruses into lethal ones, which could be used in biological warfare (Finkel 2001).

Another possible problem with virus-vectored immunocontraception is the potential for the horizontal transfer of the immunocontraceptive gene into viruses affecting other species (Becker 2000). While it may be possible to create genetically modified organisms without adverse effects on the target animals, the effects they might have on related species they come in contact with make any use of this approach questionable.

Variation in response and genetic change

Variation in response to biocontrol agents is a widespread phenomenon. This variation has frequently led to evolution of a degree of resistance so that the agent is no longer useful. The evolution of resistance to insecticides has been reviewed by McKenzie (1996). He draws a distinction between biocontrol agents with responses within the phenotypic range and those with responses outside the phenotypic range of the target species. An agent which initially kills all members of the target species is acting outside the normal phenotypical range, while one which kills onlya fraction of the population is acting within the normal phenotypical range. He points out that when resistance appears in the former case it is frequently monogenic, while in the latter case a number of different genetic regions are involved, i.e. it is probably multi-factorial. The basic genetic parameter to be estimated in either case is heritability, i.e. the extent to which genetic variation is controlled by genetic as opposed to environmental factors. The relative fertility of the immunocontracepted animals in Table 2 is >10% in 27 out of the 32 data sets. A proportion of non-responders is characteristic of most species. Only three species (Tammar wallaby, Fallow deer and Norway rat) out of 14 had no non-responders (Table 2). Following McKenzie’s (1996) argument, this implies that non-response is likely to be multi-factorial in genetic terms. There are no data which will allow estimates of the heritability of non-response to immunocontraception in any of the species in Table 2. We are unable to predict the rate at which this characteristic will increase in any one of these populations under the selective influence of immunocontraception. However, some idea of the likely change per generation given the initial frequency of non-responders can be found using Falconer’s (1965) model for threshold characters (Table 3). Reproduction is a good example of a threshold character; it is an all-or-none attribute which can be affected by a variety of underlying genetic and environmental factors. If heritabilities are high, rapid selection occurs. This is shown by the high percentage of non-responders that occur within one generation (Table 3).

A limited place for immunocontraception in wildlife management could be in species with long generation times. Genetic changes in them, if they occur, will take decades. Claims have been made for the potential efficacy of immunocontraception for African elephants (Fayrer-Hosken et al. 2000, Delsink et al. 2002), although this view has been challenged on demographic grounds (Pimm & van Aarde 2001). Long-term studies on immunocontraception in wild horses report 78–94.2% contraceptive efficacy (Kirkpatrick et al. 1995, Turner et al. 1997, 2002, Turner & Kirkpatrick 2002).

Zoo animals are convenient for immunocontraception studies of wild species, because of their long-term accessibility, although the small numbers usually available make controls hard to find. This is illustrated by an investigation involving 27 females from 10 felid species. Immunization with PZP and Freund’s Complete Adjuvant gave several kinds of adverse reaction but no convincing evidence of an effect upon fertility (Harrenstien et al. 2004).

Delves & Roitt (2005) review attempts to immunocontracept mammals and conclude that GnRH is the most promising target, because of its evolutionary conserved sequence.

Immunogenetic issues

Infectious diseases are assumed to be one of the main classes of selective forces which act upon genes controlling immune responses (Klein et al. 1993). Immunocontraceptive agents also have the potential to influence the genetic constitution of a population with respect to the ability to mount immune responses. The two are similar in that pathogens which cause plagues and immunocontraceptive agents are both capable of exerting very strong selective pressure with the potential for rapid genetic change. However, they differ in two important respects. First, most pathogens are cellular and antigenically more complex than most immunocontraceptive agents, which consist of one or a few proteins and in some cases associated carbohydrate. Second, they have opposite directions of selection; resistance to a pathogen involves a positive response, whereas resistance to an immunocontraceptive involves non-response. The consequences of this kind of selection imposed by an immunocontraceptive agent require study. It seems likely that it will alter the immunogenetic constitution of the target species. The existence of genes governing response to pathogens is well documented in humans for malaria (Hill 2001), tuberculosis (Blackwell 1998, Bellamy 2003), and HIV (McNicholl & Cuenco 1999, Carrington & O’Brien 2003). Relevant examples are found in New Zealand Red Deer in which susceptibility to tuberculosis has high heritability (Mackintosh et al. 2000) and in the NRAMP1 association with the human response to leishmaniasis (Bucheton et al. 2003). The complexities of the co-evolution of pathogens and hosts and its biomedical significance are beginning to be unraveled (Woolhouse et al. 2002). Both experimental (Lively & Dybdahl 2000) and theoretical analyses (e.g. Nowak & May 1994) point to the inherent difficulties of prediction of the course of these interactions. Prediction and detection of the ecopathological consequences of the use of immunocontraception of wild animals will also be made difficult by the spread of emerging infectious diseases as a result of human activity (Daszak et al. 2000).

The effect of immunocontraception upon genetic diversity could be significant. There is the possibility that restriction of breeding to a small group of animals which are closely related will result in localized inbreeding. This will be especially likely if their capacity to resist the immunocontraceptive is the result of shared uncommon genotype. Acevedo-Whitehouse et al.(2003) have shown that in California sea lions, inbreeding is associated with a wide range of diseases. They suggest that inbred individuals could act disproportionally as reservoirs of infectious agents.

Selection based upon immune responses could be on one of two parts of the genome: the MHC (major histocompatability complex) region which governs responses to specific immunogens, or other genes, e.g. NRAMP which govern the functioning of the immune system in general (Bellamy 1999). The tightly linked MHC genes and the resultant linkage disequilibrium mean that selection on one gene will result in changes in gene frequencies at other loci. This could either raise or lower susceptibility to other pathogens. Understanding of the non-MHC genetic component of variability of the immune response is much less advanced than for the MHC component. This understanding is needed to attempt any predictions concerning immunocontraception-based selection.

Experimental approaches to this question have until now been very difficult. The existence of genetic maps of some wild animals (e.g. Tammar wallaby (Zenger et al. 2002)) may now allow a genomic approach, in which whole genome DNA typing may allow the identification of changes in gene frequency which accompany the application of immunocontraception or a pathogen, through comparing treated and control populations. A concomitant survey of pathogens in the two groups may identify susceptibility regions, whose existence could be further tested in lab-based investigation. The genome would thus be assayed for these genes, and test the extent to which the same genes are involved in responses to different pathogens and to immunocontraception.

A good model system to address these questions is wildlife tuberculosis which is of economic significance in several countries, e.g. Britain (Delahay et al. 2002), New Zealand (Buddle et al. 2002), and the United States (Palmer et al. 2002). Considerable information on the genetic control of response to mycobacterial antigens is available (North & Medina 1998, Kramnik et al. 2000, Bellamy 2003). The possibility of obtaining results relevant to human mycobacterial susceptibility may also encourage use of this system.

We conclude that attempting to use the immunological system to modulate reproduction could be incompatible with the basic biological function of resisting pathogens. We have not discussed some of the practical issues. For example, all fertility control methods have the problem of delivery of the control agent. Highly valued animals must be treated without harming them. When this is the case, fertility control methods with fewer concomitant problems, such as surgical sterilization or the use of steroids or gonadotropin-based hormones, would be competitive with immunocontraception (Cooper & Herbert 2001).

Table 1

Immunocontraception: target species and justification for fertility control.

SpeciesLocationManagement issuesPopulation control needsReferences
K-selected species
    KoalaAustralia; local overpopulationsHabitat degradation; likely destruction of own habitat; highly regarded speciesControl methods with public acceptanceMartin & Handasyde (1999)
    African elephantSouthern AfricaHabitat degradation; public safety and health concerns; highly regarded speciesControl methods with public acceptanceHanks (2001)
    Wild horseUSA, AustraliaHabitat degradation; conflicts with livestock, timber and mining industry interests (USA); highly regarded speciesControl methods with public acceptanceBerger (1986), Dobbie et al.(1993), Furbish & Albano (1994)
    White-tailed deerUSAHabitat degradation; public safety and health concerns; high frequencies of deer-vehicle collisions; crop and garden damageControl methods with public acceptanceMcShea et al.(1997), Warren (1997)
    Feral donkey/BurroUSA, Australia, AfricaHabitat degradation; public safety and health concerns; highly regarded speciesBroad-scale control over large, remote and inaccessible areas (Australia)McCool (1981), Berger (1986), Freeland & Choquenot (1990)
    Brushtail possumNew Zealand; major introduced pest speciesHabitat degradation (New Zealand); public, livestock and wildlife health concerns; reservoir for bovine tuberculosisBroad-scale control over large, often inaccessible, areas (New Zealand). Alternative to poison baits (1080)Montague (2000)
    MacropodsAustraliaPublic, livestock and wildlife health concerns; high frequencies of kangaroo-vehicle collisions; highly regarded speciesControl methods with public acceptanceDawson (1995), Pople & Grigg (1999)
    European red foxAustralia; major introduced pest speciesPredation on native wildlife (Australia); public, livestock and wildlife health concernsControl over continental area (Australia). Alternative to poison baits (1080)Saunders et al.(1995)
    PinnipedsWorldwidePossible contribution to the depletion of fish stocksContraception suggested as humane alternative to cullingButterworth et al.(1988), Brown et al.(1996), Mohn & Bowen (1996)
    Feral catWorldwide; major introduced pest species in AustraliaPredation on native wildlife (Australia); public and wildlife health concernsControl over continental area (Australia) Alternative to poison baits (1080)Newsome (1991),Bomford et al.(1996), Mahlow & Slater (1996)
    Feral dogWorldwidePublic and livestock safety and health concerns; predation on native wildlife (Australia)Control methods with public acceptanceFleming et al.(2001), Sabeta et al.(2003)
    Feral pigWorldwide; major introduced pest species in AustraliaHabitat degradation; damage to economic resources; public, live- stock and wildlife health concernsControl methods with public acceptanceChoquenot et al.(1996)
    BadgerUKPublic, livestock and wildlife health concerns; reservoir for bovine tuberculosisControl methods with public acceptanceKrebs et al.(1998), Donnelly et al.(2003)
    Grey squirrelUK; introduced speciesHabitat degradation; threat to the native Red squirrelControl methods with public acceptanceMoore et al.(1997)
r-selected species
    European rabbitWorldwide; major vertebrate pest species in AustraliaHabitat degradation; major cost to agriculture; public, livestock and wildlife health concernsBroad-scale control over large areasLawson (1995), Williamset al.(1995)
    RodentsWorldwideMajor damage to economic resources, incl. crops, pastures, stored grain, livestock, buildings and infrastructure; public, livestock and wildlife health concernsBroad-scale control over large areas. Species-specific alternatives to rodenticidesCaughley et al.(1998), Chambers et al.(1999), Seamark (2001)
Table 2

Relative fertility of immunocontracepted females in 14 mammalian species.

SpeciesImmunogenAdjuvantNo. of immunizationsReproductive performance (control, treated)Statistical significanceaReduction in relative fertility (%)bReference
Investigations have been conducted on approximately 70 species. This table includes only true experiments, i.e. studies with an immunized group compared with a control group.
aThe P values are those given in the references cited.
bRelative fertility is defined as the mean no. of offspring for females in the vaccinated group divided by the same figure for the control group (i.e. unimmunized females).
BaboonLDH-C4+ promiscuous epitopeCGP11637 emulsified w. Squalene:Arlacel - (4:1)3Offspring/females 10/13, 4/14P < 0.0262O’Hern et al.(1997)
Brushtail possumWhole spermFreund’s complete (FCA), Freund’s incomplete (FIA) in boosters3Offspring/females 12/16, 2/16P < 0.00183Duckworth et al.(1998)
Tammar wallabyPorcine ZPFCA, FIA in boosters5Offspring/females 4/6, 0/6P < 0.05 (n = 6)100Kitchener et al.(2002)
African elephant
    First schedulePorcine ZPAdjuvant used, type not given3Offspring/females 16/18, 8/18P = 0.00550Fayrer-Hosken et al.(2000)
    Second schedulePorcine ZPAdjuvant not mentioned2Offspring/females 2/10 (no true control)P = 0.00177Fayrer-Hosken et al.(2000)
Wild horsePorcine ZPFCA, FIA in boosters3–4Pregnancy rate 3/6, 1/14Not stated85Kirkpatrick et al.(1991)
White-tailed deer
    First schedulePorcine ZPFCA, FIA in booster2Fawns/doe years 30/16, 4/16P < 0.000187Miller et al. (2000a)
    Second scheduleRC55FCA, FIA in booster2Fawns/doe years 30/16, 19/14P < 0.0528Miller et al. (2000a)
    Third scheduleRC75aFCA, FIA in booster2Fawns/doe years 30/16, 11/8P < 0.0127Miller et al. (2000a)
    Fourth scheduleCombined antigensFCA, FIA in booster2Fawns/doe years 30/16, 16/8P>0.050Miller et al. (2000a)
White-tailed deerKLH-GnRHFCA, FIA in boosters2–4Fawns/doe years 35/19, 5/24P < 0.0189Miller et al. (2000b)
White-tailed deerPorcine ZPFCA, FIA in boosters2–3Fawns/doe years 35/19, 25/57P < 0.0176Miller et al. (2000c)
White-tailed deer
    First scheduleGnRHFCA, FIA in boosters3Fawns/doe years 110/90, 36/118P < 0.000575Curtis et al.(2002)
    Second schedulePorcine ZPFCA, FIA in boosters3Fawns/doe years 72/56, 10/60P < 0.000587Curtis et al.(2002)
Fallow deerSpayVacFCA1Pregnancy rate 322/334, 0/22P < 0.0001100Fraker et al.(2002)
BurroPorcine ZPFCA, FIA in boosters2–3Offspring/females 6/11, 1/16P < 0.0588Turner et al.(1996)
Grey sealSIZP (SpayVac)FCA1Pups/female 2.76, 0.22P < 0.00192Brown et al.(1996, 1997)
Tule elkPorcine ZPFCA, FIA in boosters3–4Calves/cow years 53/91, 5/104Not stated91Shideler et al.(2002)
CatPorcine ZPFCA, FIA in boosters5Pregnancy rate 2/2, 1/5Not stated50Ivanova et al.(1995)
Cat
    First scheduleSpayVacFCA1Mean litter size 5.2, 4.5P = 0.885913Gorman et al.(2002)
    Second scheduleSpayVacAlum1Mean litter size 5.2, 4.4P = 0.885915Gorman et al.(2002)
European rabbitMyxoma vectored ZPBFCA, FIA in boosters3Mean litter size 7.4, 7.0Not stated5Kerr et al.(1999)
Norway rat
    First scheduleMZPP/KLHFCA, FIA in boosters3Pregnancy rate 7/8, 4/8P>0.0540Miller et al.(1997)
    Second scheduleGnRH/KLHFCA, FIA in boosters3Pregnancy rate 7/8, 0/8P < 0.004100Miller et al.(1997)
Wild mouseKLH-mZP3FCA, FIA in boosters5Pregnancy rate 8/15, 7/30P = 0.04656Hardy et al. (2002b)
BALB/c mouse
    First schedule (71–81 days)Murine rFA-1FCA, FIA in boosters4Mean litter size 8.9, 3.2P < 0.000164Naz & Zhu (1998)
    Second schedule (283 days)Murine rFA-1FCA, FIA in boosters4Mean litter size 8.6, 9P>0.050Naz & Zhu (1998)
BALB/c mouse
    First schedulesp56FLAGFCA, FIA in boosters6Offspring/females 55/14, 12/5P = 001739Hardy & Mobbs (1999)
    Second schedulesp56FLAGFCA, FIA in boosters4Offspring/females 55/14, 19/5Not stated3Hardy & Mobbs (1999)
BALB/c mouse
    First scheduleMBP-polyepitope AFCA, FIA in boosters4Mean litter size 5.2, 3.3Not stated37Hardy et al. (2002a)
    Second scheduleMBP-polyepitope BFCA, FIA in boosters4Mean litter size 5.2, 2.1P < 0.0560Hardy et al. (2002a)
    Third schedule6XHis-polyepitope AFCA, FIA in boosters4Mean litter size 6.5, 6.3Not stated3Hardy et al. (2002a)
Table 3

Predicted proportion of non-responder daughters after one generation of selection by immunocontraception of mothers given various heritabilities (after Falconer 1965).

Heritability (%)
Non-responder mothers (%)100806050
The prediction has been arrived at by entering the table in Falconer (1965) which relates heritability for a threshold trait to incidences in parent and offspring. The response to selection (predicted percentage of non-responders) obtained has been halved because selection is being carried out on one sex.
51511108
1023191615

Received 21 May 2006
 First decision 22 June 2006
 Revised manuscript received 30 July 2006
 Accepted 10 October 2006

We acknowledge helpful comments from John Aitken, Tony Basten, Kathy Belov, David Briscoe, Bryce Buddle, Margaret Carrington, Charles Daugherty, Dick Frankham, Cathy Herbert, John McKenzie, Bill Sherwin, Jim Shields, Roger Short, and Kyall Zenger. Our research on population control in koalas and kangaroos is supported by the Australian Research Council grant LPO560344. The authors declare that there is no conflict of interest that would prejudice the impartiality of this scientific work.

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    • Export Citation
  • Grandy JW & Rutberg AT 2002 An animal welfare view of wildlife contraception. Reproduction (Cambridge, England) Supplement 60 1–7.

  • Gupta SK & Talwar GP 1994 Contraceptive vaccines. Advances in Contraceptive Delivery Systems 10 255–265.

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  • Fleming PL, Corbett L, Harden R & Thomson P 2001 Managing the Impacts of Dingoes and Other Wild Dogs, Canberra: Bureau of Rural Sciences.

  • Fraker MA, Brown RG, Gaunt GE, Kerr JA & Pohajdak B 2002 Long-lasting, single-dose immunocontraception of feral fallow deer in British Columbia. Journal of Wildlife Management 66 1141–1147.

    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
  • Furbish CE & Albano M 1994 Selective herbivory and plant community structure in a mid-Atlantic salt marsh. Ecology 75 1015–1022.

  • Gorman SF, Levy JK, Hampton AL, Collante WR, Harris AL & Brown RG 2002 Evaluation of a porcine zona pellucida vaccine for the immunocontraception of domestic kittens (Felis catus). Theriogenology 58 135–149.

    • Search Google Scholar
    • Export Citation
  • Grandy JW & Rutberg AT 2002 An animal welfare view of wildlife contraception. Reproduction (Cambridge, England) Supplement 60 1–7.

  • Gupta SK & Talwar GP 1994 Contraceptive vaccines. Advances in Contraceptive Delivery Systems 10 255–265.

  • Hanks J 2001 Conservation strategies for Africa’s large mammals. Reproduction, Fertility, and Development 13 459–468.

  • Hardy CM & Mobbs KJ 1999 Expression of recombinant mouse sperm protein sp56 and assessment of its potential for use as an antigen in an immunocontraceptive vaccine. Molecular Reproduction and Development 52 216–224.

    • Search Google Scholar
    • Export Citation
  • Hardy CM, Pekin J & ten Have JF 2002a Mouse-specific immunocontraceptive polyepitope vaccines. Reproduction (Cambridge, England) Supplement 60 19–30.

    • Search Google Scholar
    • Export Citation
  • Hardy CM, ten Have JF, Mobbs KJ & Hinds LA 2002b Assessment of the immunocontraceptive effect of a zona pellucida 3 peptide antigen in wild mice. Reproduction, Fertility, and Development 14 151–155.

    • Search Google Scholar
    • Export Citation
  • Harrenstien LA, Munson L, Chassy LM, Liu IK & Kirkpatrick JF 2004 Effects of porcine zona pellucida immunocontraceptives in zoo felids. Journal of Zoo and Wildlife Medicine 35 271–279.

    • Search Google Scholar
    • Export Citation
  • Hill AV 2001 The genomics and genetics of human infectious disease susceptibility. Annual Review of Genomics and Human Genetics 2 373–400.

    • Search Google Scholar
    • Export Citation
  • Ivanova M, Petrov M, Klissourska D & Mollova M 1995 Contraceptive potential of procine zona pellucida in cats. Theriogenology 43 969–981.

    • Search Google Scholar
    • Export Citation
  • Jackson RJ, Ramsay AJ, Christensen CD, Beaton S, Hall DF & Ramshaw IA 2001 Expression of mouse interleukin-4 by a recombinant ectromelia virus suppresses cytolytic lymphocyte responses and overcomes genetic resistance to mousepox. Journal of Virology 75 1205–1210.

    • Search Google Scholar
    • Export Citation
  • Joshi SH 1973 An immunological approach to fertility control. American Journal of Pharmacy 145 22–26.

  • Kerr PJ, Jackson RJ, Robinson AJ, Swan J, Silvers L, French N, Clarke H, Hall DF & Holland MK 1999 Infertility in female rabbits (Oryctolagus cuniculus) alloimmunized with the rabbit zona pellucida protein ZPB either as a purified recombinant protein or expressed by recombinant myxoma virus. Biology of Reproduction 61 606–613.

    • Search Google Scholar
    • Export Citation
  • Kirkpatrick JF, Liu IKM, Turner JW & Bernoco M 1991 Antigen recognition in feral mares previously immunized with porcine zonae pellucidae. Journal of Reproduction and Fertility. Supplement 44 321–325.

    • Search Google Scholar
    • Export Citation
  • Kirkpatrick JF, Naugle R, Liu IKM & Turner JW 1995 Effects of Seven Consecutive Years of Porcine Zonae Pellucidae Contraception on Ovarian Function in Feral Mares, Biology of Reproduction Monograph Series. vol 1, pp 411–413 (Equine Reproduction VI).

    • Search Google Scholar
    • Export Citation
  • Kitchener AL, Edds LM, Molinia FC & Kay DJ 2002 Porcine zonae pellucidae immunization of tammar wallabies (Macropus eugenii): fertility and immune responses. Reproduction, Fertility, and Development 14 215–223.

    • Search Google Scholar
    • Export Citation
  • Klein J, Satta Y, O’HUigin C & Takahata N 1993 The molecular descent of the major histocompatibility complex. Annual Review of Immunology 11 269–295.

    • Search Google Scholar
    • Export Citation
  • Kramnik I, Dietrich WF, Demant P & Bloom BR 2000 Genetic control of resistance to experimental infection with virulent Mycobacterium tuberculosis. PNAS 97 8560–8565.

    • Search Google Scholar
    • Export Citation
  • Krebs JR, Anderson RM, Clutton-Brock T, Donnelly CA, Frost S, Morrison WI, Woodroffe R & Young D 1998 Badgers and bovine TB: conflicts between conservation and health. Science 279 817–818.

    • Search Google Scholar
    • Export Citation
  • Lawson M 1995 Rabbit virus threatens ecology after leaping the fence. Nature 378 531.

  • Leenaars PP, Hendriksen CF, Angulo AF, Koedam MA & Claassen E 1994 Evaluation of several adjuvants as alternatives to the use of Freund’s adjuvant in rabbits. Veterinary Immunology and Immunopathology 40 225–241.

    • Search Google Scholar
    • Export Citation
  • Leenaars PP, Koedam MA, Wester PW, Baumans V, Claassen E & Hendriksen CF 1998 Assessment of side effects induced by injection of different adjuvant/antigen combinations in rabbits and mice. Laboratory Animals 32 387–406.

    • Search Google Scholar
    • Export Citation
  • Lively CM & Dybdahl MF 2000 Parasite adaptation to locally common host genotypes. Nature 405 679–681.

  • Mackintosh CG, Qureshi T, Waldrup K, Labes RE, Dodds KG & Griffin JF 2000 Genetic resistance to experimental infection with Mycobacterium bovis in red deer (Cervus elaphus). Infection and Immunity 68 1620–1625.

    • Search Google Scholar
    • Export Citation
  • Mahlow JC & Slater MR 1996 Current issues in the control of stray and feral cats. Journal of the American Veterinary Medical Association 209 2016–2020.

    • Search Google Scholar
    • Export Citation
  • Martin R & Handasyde K 1999 The Koala: Natural History, Conservation and Management, Sydney: University of New South Wales Press Ltd.

  • McCool CJ 1981 Feral Donkeys in the Northern Territory: Report to the Feral Animals Committee of a Working Party on the Feral Donkey Problem, Darwin: Department of Primary Production.

  • McKenzie JA 1996 Ecological and Evolutionary Aspects of Insecticide Resistance, Texas, USA: Academic Press/R.G. Landes.

  • McNicholl JM & Cuenco KT 1999 Host genes and infectious diseases. HIV, other pathogens, and a public health perspective. American Journal of Preventive Medicine 16 141–154.

    • Search Google Scholar
    • Export Citation
  • McShea WJ, Underwood HB & Rappole JH 1997 The Science of Overabundance: Deer Ecology and Population Management, Washington, D.C.: Smithsonian Institution Press.

  • Miller LA, Johns BE, Elias DJ & Crane KA 1997 Comparative efficacy of two immunocontraceptive vaccines. Vaccine 15 1858–1862.

  • Miller LA, Johns BE & Killian GJ 2000a Immunocontraception of white-tailed deer using native and recombinant zona pellucida vaccines. Animal Reproduction Science 63 187–195.

    • Search Google Scholar
    • Export Citation
  • Miller LA, Johns BE & Killian GJ 2000b Immunocontraception of white-tailed deer with GnRH vaccine. American Journal of Reproductive Immunology 44 266–274.

    • Search Google Scholar
    • Export Citation
  • Miller LA, Johns BE & Killian GJ 2000c Long-term effects of PZP immunization on reproduction in white-tailed deer. Vaccine 18 568–574.

  • Mohn R & Bowen WD 1996 Grey seal predation on the Eastern Scotian Shelf: modeling the impact on Atlantic cod. Canadian Journal of Fisheries and Aquatic Sciences 53 2722–2738.

    • Search Google Scholar
    • Export Citation
  • Montague TLe 2000 The Brushtail Possum: Biology, Impact and Management of an Introduced Marsupial, Lincoln, NZ: Manaaki Whenua Press.

  • Moore HD, Jenkins NM & Wong C 1997 Immunocontraception in rodents: a review of the development of a sperm-based immuno-contraceptive vaccine for the grey squirrel (Sciurus carolinensis). Reproduction, Fertility, and Development 9 125–129.

    • Search Google Scholar
    • Export Citation
  • Naz RK & Zhu X 1998 Recombinant fertilization antigen-1 causes a contraceptive effect in actively immunized mice. Biology of Reproduction 59 1095–1100.

    • Search Google Scholar
    • Export Citation
  • Newsome AE 1991 Feral cats: an overview. In The Impact of Cats on Native Wildlife, Ed. C Potter. Canberra: Australian National Parks and Wildlife Service.

  • North RJ & Medina E 1998 How important is Nramp1 in tuberculosis?. Trends in Microbiology 6 441–443.

  • Nowak MA & May RM 1994 Superinfection and the evolution of parasite virulence. Proceedings of the Royal Society of London. Series B 255 81–89.

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