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209
Chapter 10
Novel Management Methods:
Immunocontraception and Other
Fertility Control Tools
Giovanna Massei, Dave Cowan and Douglas Eckery
Impacts of overabundant ungulate populations on human activities and conserva-
tion include crop and forestry losses, collisions with vehicles, disease transmis-
sion, nuisance behaviour, damage to infrastructures, predation on livestock and
native species, and reduction of biodiversity on plant and animal communities
(e.g. Curtis et al., 2002; Massei et al., 2011; Reimoser and Putman, 2011; Ferroglio
et al., 2011; Langbein et al., 2011).
Current trends in human population growth and landscape development indicate
that human–ungulate confl icts in Europe, as well as in the United States, are likely
to increase in parallel with increased expansion in numbers and range of many
of these species (Rutberg and Naugle, 2008; Brainerd and Kaltenborn, 2010;
Gionfriddo et al., 2011a). Many of these confl icts have been traditionally managed
by lethal methods. However, current trends in distribution and numbers of wild
boar, feral pigs and deer in Europe and in the United States (e.g. Saez-Royuela
and Telleria, 1986; Waithman et al., 1999; Ward, 2005; Apollonio et al., 2010)
suggest that recreational hunting is not suffi cient to control ungulate densities.
In addition, ethical considerations regarding humane treatment of animals are
increasingly shaping public attitudes towards acceptable methods of mitigating
human – wildlife confl icts and lethal control is often opposed (Beringer et al.,
2002; Wilson, 2003; Barfi eld et al., 2006; McShea, 2012).
Public antipathy towards lethal methods increasingly constrains the options
available for ungulate management, particularly in urban and suburban areas
and in protected areas where culling is often opposed on ethical, legal or safety
grounds (Kirkpatrick et al., 2011; Boulanger et al., 2012; Rutberg et al., 2013).
Consequently, interest in non-lethal methods, such as translocation or fertility
control, has increased (Fagerstone et al., 2010).
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210 Massei, Cowan and Eckery
Reviews of translocations of problem wildlife as a mechanism for reducing
human – ungulate confl icts concluded that this method may cause signifi cant
stress, increase mortality and traffi c accidents, is relatively expensive and has the
potential to spread diseases and pathogens (Daszak et al., 2000; Corn and Nettles,
2001; Conover, 2002; Beringer et al., 2002; Massei et al., 2010a). Examples of
translocations of pathogens and hosts include the spread of bovine brucellosis and
bovine tuberculosis following the translocation of bison (Bison bison) in Canada
(Nishi et al., 2006), the potential spread and dissemination of diseases such as the
Aujeszky’s disease virus following the translocation of wild boar between hunt-
ing estates in Spain (Ruiz-Fons et al., 2008) and warble and nostril fl ies spread to
conspecifi cs by caribou (Rangifer tarandus) after translocation of animals from
Norway to Greenland (in Kock et al., 2010).
Fertility control is often advocated as a safe, humane alternative to culling for
managing overabundant wildlife (Fagerstone et al., 2010; M.C. Laughlin and
Aitken, 2011; Kirkpatrick et al., 2011). Early attempts to use fertility control to
manage ungulates failed for reasons that included toxicity of the drugs used, trans-
fer of these drugs to the food chain, manufacturing costs and the fact that repeated
applications of contraceptives were required to induce long-term infertility (Gray
and Cameron, 2010; Kirkpatrick et al., 2011). In the last two decades, a reawak-
ened interest in alternatives to surgical sterilization for companion animals and
livestock has led to the development of novel fertility control agents (Herbert and
Trigg, 2005; Naz et al., 2005; Massei et al., 2010b). In parallel, several fertility
control agents have emerged for wildlife applications.
In this chapter we provide a comprehensive, critical overview of fertility control
to mitigate human–ungulate confl icts. In particular, we discuss the availability and
use of fertility control agents in ungulates, we review delivery methods for these
agents, we provide a synthesis of the conclusions of empirical and theoretical stud-
ies of fertility control applied to populations and we offer suggestions to guide
decisions regarding the suitability of fertility control to mitigate human–ungulate
confl icts.
10.1 Fertility inhibitors for ungulates
10.1.1 Fertility control and reproduction
Chemical fertility control can be achieved through contraception or sterilization.
Contraception prevents the birth of offspring but maintains fertility, whilst steri-
lization renders animals infertile (Kutzler and Wood, 2006). In mammals, the
series of events that leads to ovulation and spermatogenesis begins in the brain,
where gonadotropin-releasing hormone (GnRH) is produced in the hypothala-
mus. GnRH is transported through small blood vessels to the anterior pituitary
gland, where it binds to GnRH receptors to stimulate the release of the pituitary
gonadotropins, LH (luteinizing hormone) and FSH (follicle-stimulating hor-
mone) (Figure 10.1).
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Novel Management Methods 211
These gonadotropins in turn stimulate the synthesis and secretion of sex hor-
mones such as oestrogen, progesterone, and testosterone which are responsible for
ovulation, spermatogenesis and sexual behaviour. The reproductive cycle and the
production of eggs and sperm can be disrupted by administration of substances
that interfere with the hypothalamic–pituitary–gonadal axis by blocking the syn-
thesis, release or actions of hormones produced by the hypothalamus, the pituitary
gland, or the testes and ovary. In females, a further target for contraception is the
zona pellucida (ZP), a protein coat that surrounds the ovulated egg and allows
species-specifi c sperm recognition and fertilization. In males, sterilization can also
be achieved by chemicals that cause testicular sclerosis and permanent sterility
(Crawford et al., 2011). The following section presents a brief overview of fertility
control agents commercially available or widely tested on ungulates. Taking into
account fi eld applications, the review includes only those drugs that induce infer-
tility for at least 6–12 months following administration of a single dose.
The majority of the fertility inhibitors reported in the literature target females,
although some are effective for both genders and a few have been specifi cally
developed for males. In many ungulate species the mating system is promiscuous,
thus requiring extremely high levels of male sterility for fertility control to have
any effect at the population level. For instance, in feral horses (Equus caballus)
breeding still occurred even when 100 per cent of the dominant harem stallions
were sterilized (Turner and Kirkpatrick, 1991; Garrott and Siniff, 1992). In addi-
tion, some contraceptives may affect secondary sexual characteristics such as antler
development (see later sections) and their use is not recommended for male deer.
Figure 10.1 Schematic illustration of the fertility axis in male and female mammals.
GnRH
LH FSH
Progesterone
Estrogen
Testosterone
Hypothalamus
Pituitary
Ovary Testis
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212 Massei, Cowan and Eckery
A fertility control agent suitable for fi eld applications should ideally have the
following characteristics (Turner and Kirkpatrick, 1991; Fagerstone et al., 2002;
Massei and Miller, 2013):
1. Nil or acceptable side effects on the target animal’s physiology, behaviour and
welfare, including no interference with pre-existing pregnancy or lactation
2. Effective for at least one reproductive season when delivered through a single,
injectable dose or implant or when administered in one or multiple oral doses
3. Render all or the majority of treated animals infertile
4. Inhibit female reproduction but ideally prevent reproduction in both sexes
5. Relatively inexpensive to produce and deliver
6. No effect on any food chain
7. Species specifi city
8. Stability under a wide range of fi eld conditions.
Although none of the fertility control agents currently available meet all the
above features, several exhibit many of these characteristics.
10.1.2 Hormonal contraceptives
Synthetic progestins such as norgestomet, melengestrol acetate (MGA), megestrol
acetate (MA) and levonorgestrel have been widely used in zoo animals, livestock
and wildlife. By binding to progesterone receptors, synthetic progestins disrupt
ovulation and egg implantation in females and impair spermatogenesis in males
(Asa and Porton, 2005). For instance, norgestomet, administered to white-tailed and
black-tailed deer, caused infertility in 92–100 per cent of the females for at least one
year (Jacobsen et al., 1995; DeNicola et al., 1997). These drugs may cause abortion,
although this effect depends on progestin type, species, dose and time of administra-
tion during pregnancy (Waddell et al., 2001; Asa and Porton, 2005). MGA did not
affect pregnancy in several ungulate species, but delayed or prevented parturition in
treated white-tailed deer (Plotka and Seal, 1989; Asa and Porton, 2005). Progestin
implants, with an estimated duration of effi cacy of ≥2 years, have been widely used
for suppression or synchronisation of oestrus in cattle and they have been employed
as contraceptives in zoos for about 20 years. MA implants induced infertility in
female mountain goats for at least 5 years, with reproduction recorded in 10 per cent
treated goats against 68 per cent untreated controls (Hoffman and Wright, 1990).
Implants containing different concentrations of steriods such as ethinyloestra-
diol (EE), and progesterone (P) have been successful in preventing pregnancy in
feral mares. Suppression of ovulation appeared to be inversely related to the con-
centration of EE used in the implant. The percentage of animals ovulating after
2 years was 12–20 per cent for groups that had received a combination of P and
EE or the highest dose of EE respectively, against 100 per cent for control mares;
pregnancy rate for the same groups was 0 per cent for both P+EE and EE and
100 per cent for control females. All animals that were pregnant at the time of
contraceptive treatment delivered normal foals. The results demonstrated effective
contraception of feral mares for up to 36 months without compromising pregnancy
(Plotka et al., 1992).
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Novel Management Methods 213
Another group of hormones widely used as contraceptives are the gonadotropin-
releasing hormone (GnRH) agonists: these are synthetic peptides that mimic GnRH
and stimulate the production and release of FSH and LH. Chronic administration of
these drugs (e.g. >4 weeks) results in a downregulation of the pituitary gland and sup-
pression of the secretion of FSH and LH. However, immediately following admin-
istration, a ‘fl are up’ effect often occurs that can stimulate oestrus in females and
cause temporary enhancement of testosterone and semen production in males (Pat-
ton et al., 2007). As agonists have a higher affi nity for and do not quickly dissociate
from the GnRH receptors, the ‘fl are up’ is followed by prolonged oestrus inhibition
and infertility (Gobello, 2007) as long as the drug is present. The effectiveness of
GnRH agonists depends on type of agonist, release system, dose rate and duration
of treatment (Gobello, 2007; Patton et al., 2007). The side-effects are equivalent to
gonad removal but are reversible; however, GnRH agonists may cause abortion and
thus their application to free-living ungulates is limited to those species that have a
well-defi ned, relatively short breeding season (Asa and Porton, 2005).
Sustained-release subcutaneous implants containing GnRH agonists have been
tested successfully in several livestock and wildlife species. For instance, implants
of the GnRH agonist deslorelin (Suprelorin©) have been used to inhibit reproduc-
tion for 1–2 years in cattle and in several other wildlife species (e.g. D’Occhio
et al., 2002; Herbert and Trigg, 2005; Eymann et al., 2007). Another GnRH
agonist, leuprolide, administered in biodegradable implants was found effective
at preventing pregnancy for one breeding season in 100 per cent of female elk
(wapiti) and mule deer with no effects on behaviour, body condition, haematology
and blood chemistry (Baker et al., 2002, 2004; Conner et al., 2007). Regardless of
proven effi cacy, the use of hormonal contraceptives on free-ranging ungulates is
still controversial because of potential welfare effects on pregnancy, environmen-
tal impact and possible transfer to consumers through the food chain (Kirkpatrick
et al., 1996; De Nicola et al., 2000).
10.1.3 Immunocontraceptive vaccines
Most studies of fertility control applications in free-ranging ungulates have
focussed on immunocontraceptive vaccines. These vaccines stimulate the immune
system to produce antibodies to proteins or hormones essential for reproduction
(Miller and Killian, 2002), thus rendering animals contracepted or infertile. To
achieve long-term infertility, adjuvants are used, which are chemicals, large mol-
ecules or entire cells of killed pathogens, that enhance the immune response to a
vaccine (Fraker et al., 2002). Using liposome-based formulations has also been
shown to increase the immune response of some immunocontraceptive vaccines
(Fraker and Brown, 2011). The effectiveness, duration and side effects of immu-
nocontraceptive vaccines can vary with species, sex, age, individual differences in
immunocompetence, as well as the active component of the vaccine, its formula-
tion, delivery system and the dose and type of adjuvant (Miller et al., 2008a, 2009;
Holland et al., 2009; Kirkpatrick et al., 2011). The most studied immunocontra-
ceptives in ungulates are zona pellucida- and GnRH-based vaccines (Table 10.1).
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214 Massei, Cowan and Eckery
Table 10.1 Effectiveness of single-dose immunocontraceptive vaccines to cause infertility in ungulate species in captivity and fi eld trials. The
effectiveness is expressed as proportion of infertile females in the control (C) and treatment (T) groups in the years following administration of
the vaccine.
Species Type of
study
Vaccine type, adjuvant
type and vaccine dose
% infertile females References
White-tailed deer
Odocoileus virginianus
Captive GonaCon and AdjuVac
various formulations
T GonaCon-KLH = 100% 60% 50% 50% 25%
T GonaCon-Blue = 100% 100% 80% 80% 80%
Miller et al. (2008a)
White-tailed deer Field GonaCon-KLH and
AdjuVac
T = 67% 43%
C = 8% 17%
Gionfriddo et al.
(2011a)
White-tailed deer Field GonaCon-KLH and
AdjuVac
T = 88% 47%
C = 15% 0%
Gionfriddo et al.
(2009)
White-tailed deer Field PZP (SpayVac) and
AdjuVac
T = 100% 100%
C = 22%
Locke et al. (2007)
White-tailed deer Field PZP and AdjuVac T = 100%
C = 22%
Hernandez et al.
(2006)
White-tailed deer Captive PZP and SpayVac, with
AdjuVac or Alum
SpayVac-AdjuVac: 100% 100% 100% 80% 80%
IVT-PZP-AdjuVac: 100% 80% 80% 80% 80%
SpayVac-Alum: 80%
NWRC-PZP-AdjuVac: 80% 0%
(200 µg)
NWRC-PZP-AdjuVac: 100% 20% 20% 20% 0%
(500 µg);
C = 0%
Miller et al. (2009)
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Novel Management Methods 215
Elk
Cervus elaphus
Captive GonaCon-B and
AdjuVac
T = 90% 75% 50% 25%
C = 0% 0% 0% 14%
Powers et al. (2011)
Elk Captive GonaCon-KLH and
AdjuVac
GonaCon-KLH (1000 µg) = 92% 90% 100%
GonaCon-KLH (2000 µ g) = 90% 100% 100%
C = 27% 25% 0%
Killian et al. (2009)
Bison
Bison bison
Captive GonaCon-KLH and
AdjuVac
T = 100%
C = 0%
Miller et al. (2004)
Wild boar
Sus scrofa
Captive GonaCon-KLH and
AdjuVac
T = 92 % infertile for at least 4-6 years
C = 0%
Massei et al. (2008)
Massei et al. (2012)
Fallow deer
Dama dama
Field PZP (SpayVac) and
FCA
T = 100% 100% 100%
C = 4% 3% 4%
Fraker et al. (2002)
Feral horse
(Equus caballus)
Captive GonaCon-KLH and
AdjuVac
T = 93% 64% 57% 43%
C = 25% 25% 12% 0%
Killian et al. (2008)
Feral horse Field GonaCon-B and
AdjuVac
T = 61% 58% 69%
C = 40% 31% 14%
Gray et al. (2010)
Feral horse Captive PZP (SpayVac) and
AdjuVac
T = 100% 83% 83% 83%
C = 25% 25% 12% 0%
Killian et al. (2008)
Feral horse Field PZP with FCA and
QS-21 T = 95% 85% 68% 54%
C = 47% 42% 49% 48%
Turner et al. (2007)
Feral horse Field PZP and AdjuVac T= 63% 50% 56%
C= 40% 31% 14%
Gray et al. (2010)
Gray et al. (2011)
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216 Massei, Cowan and Eckery
The zona pellucida (ZP) that surrounds an ovulated egg is composed of four
types of proteins, named ZP1, ZP2, ZP3 and ZP4, each with different functions
in mediating structure and species-specifi c sperm recognition and binding. Dif-
ferences in these proteins among mammals are partly responsible for the variable
results obtained when using a particular ZP vaccine on different species (Kitchener
et al., 2009; Gupta and Bansal, 2010). For instance, porcine ZP (PZP) immunocon-
traceptive vaccines, derived from ZP isolated from pig ovaries inhibit fertilisation
in many wildlife species including ungulates (Table 10.1) but not rodents, cats
and wild pigs (Fagerstone et al., 2002; Kirkpatrick et al., 2009, 2011). Likewise,
differences in the results of studies using ZP-based vaccines may refl ect different
formulations of native, purifi ed or recombinant ZP vaccines and different methods
of extraction of PZP from pig ovaries (Miller et al., 2009; Kirkpatrick et al., 2011;
Bechert et al., 2013).
Early immunocontraceptive vaccines had to be delivered as a primer injection
followed by a booster, which made fi eld applications impractical (Putman, 1997).
Initial vaccine formulations also used Freund’s complete adjuvant (FCA). Some
constituents of this adjuvant, namely mycobacteria (Mycobacterium tuberculosis)
and mineral oil, were found responsible for granulomas (thickened tissue fi lled
with fl uid) at injection sites, for false-positive results in TB skin tests in deer treated
with these vaccines and for potential carcinogenicity to consumers of treated ani-
mals (Kirkpatrick et al., 2011). Signifi cant progress has been made through the
development of a novel adjuvant (AdjuVacTM, National Wildlife Research Center,
United States), containing inactivated Mycobacterium avium and based on a modi-
fi ed version of the Johne’s disease vaccine.
Injectable ZP-based immunocontraceptives have been employed extensively to
reduce fertility in zoo ungulates, in free-living deer, feral horses and elephants
(Table 10.1). In particular, the combination of AdjuVac and PZP-vaccine made
ungulates infertile for several years after a single dose (Table 10.1). In some spe-
cies, such as white-tailed deer, some ZP vaccines may cause pathologies such as
infl ammation of the ovary (Curtis et al., 2007) but in others, such as wild horses,
no ovarian damage was observed after 3 years of treatment (Patton et al., 2007).
Following injection of ZP-based immunocontraceptives, injection site reactions
such as granulomas are common, whilst the occurrence of draining abscesses is
around 1 per cent in various species (Gray et al., 2010; Kirkpatrick et al., 2009).
As ZP-based immunocontraceptives inhibit fertilisation but not ovulation, animals
treated with these vaccines tend to have multiple infertile oestrus cycles which
may lead to extended breeding seasons, increased movements and potential late
births (Miller et al., 2000; Curtis et al., 2007; Nuñez et al., 2009, 2010; reviewed in
Kirkpatrick et al., 2009, 2011). Multiple infertile oestrus cycles following treatment
with PZP vaccine were observed in white-tailed deer, wapiti and horses (Heilmann
et al., 1998; Killian and Miller, 2001; Curtis et al., 2002; Ransom et al., 2013).
Other studies suggested that treatment with ZP vaccines did not affect behav-
iour and body condition of mares (Ransom et al., 2010; Kirkpatrick et al., 2011),
white-tailed deer (Hernandez et al., 2006) and wapiti (Heilmann et al., 1998).
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Novel Management Methods 217
However, an extension of the breeding season in deer treated with PZP vaccine
resulted in increased energy expenditure by males (Curtis et al., 2002). PZP vac-
cines were found safe to administer to pregnant or lactating females (Kirkpatrick
and Turner, 2002; Patton et al., 2007) and had no long-term effect on health of
white tailed deer (Miller et al., 2001). In 2012, an injectable PZP-based vaccine,
ZonaStat-H, was registered by the US Humane Society and approved by the US
Environment Protection Agency (EPA) as a contraceptive for population control
of wild and feral horses and feral donkeys.
Vaccines based on gonadotropin-releasing hormone (GnRH) generate antibod-
ies towards GnRH, thus preventing the hormonal cascade that leads to ovulation
and sperm production. Several multi-dose GnRH-based immunocontraceptive vac-
cines, developed for use in livestock are unsuitable for wildlife due to the diffi -
culty of recapturing individuals to administer booster doses and to their relatively
short-term (a few months) effectiveness (reviewed in Naz et al., 2005; McLaughlin
and Aitken, 2010). Single-dose injectable GnRH-based vaccines, specifi cally for-
mulated for wildlife applications, offer better prospects for managing ungulates.
Among these vaccines, the most studied is GonaconTM, currently registered in the
United States by the EPA as an immunocontraceptive for white-tailed deer, feral
horses and feral donkeys. GonaconTM consists of a synthetic GnRH coupled to a
mollusc protein (Miller et al., 2008b).
Formulated as an injectable, single-dose immunocontraceptive, GonaconTM
caused infertility for several years in males and females of several ungulates (e.g.
Miller et al., 2000; Killian et al., 2008; Massei et al., 2008; Gray et al., 2010; Massei
et al., 2012) (Table 10.1). As GonaconTM interferes with steroid production, treated
females do not exhibit oestrus behaviour. Male deer treated with GonaConTM also
showed a complete lack of sexual activity and reduced testicle size, but they also
exhibited abnormal antler development (Miller et al., 2000, 2009; Fagerstone
et al., 2008). The lack of sexual activity, in species where this behaviour might
increase human – wildlife confl icts such as deer collisions with vehicles during
the rut, could be advantageous, although the effect on antler development suggests
GonaConTM should not be used on male deer. Similar to ZP-based contraceptives,
antibodies to GnRH decrease with time and fertility may be restored in the years
after treatment unless animals are administered booster vaccinations (Miller et al.,
2008b; Massei et al., 2012).
The main side effect of GonaconTM is the formation of a granuloma or a ster-
ile abscess at the injection site; the severity and incidence of injection site reac-
tions vary with species. In white-tailed deer, injection-site granulomas and sterile
abscesses occurred in the deep hind-limb musculature of >85 per cent of treated
animals, although no evidence of limping or impaired mobility was observed in
these deer during a 2-year study (Gionfriddo et al., 2011b). These reactions are
typical responses to injection of adjuvanted vaccines formulated as water-in-oil
emulsions (Miller et al., 2009). On the other hand, GonaConTM had no adverse effects
on major organs, body condition, fat deposits or blood chemistry in wild boar,
white-tailed deer and wapiti (Massei et al., 2008, 2012; Gionfriddo et al., 2009,
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218 Massei, Cowan and Eckery
2011b). When given to pregnant bison and elk, GonaConTM did not affect pregnancy
(Miller et al., 2004; Powers et al., 2011). Other studies found that GonaConTM did
not induce infertility and did not prevent sexual development when administered
to 3–4-month-old white-tailed deer (Miller et al., 2008a; Gionfriddo et al., 2011a).
Like ZP-based vaccines, GnRH vaccines are broken down if ingested, thus they do
not pose risks to predators or human consumers.
10.2 Delivery methods
Although a fertility control agent should be ideally species specifi c, this is rarely
the case and specifi city must be achieved through the delivery method. At present,
fertility control agents that induce at least 1 year of infertility are administered by
direct injection following capture, by implant or are delivered remotely through
biobullets and syringe-darts (see below). Subcutaneous implants that release con-
traceptive agents into the body over a sustained period of time have been success-
fully employed to induce infertility for 1–5 years in a variety of wildlife species
(e.g. Plotka and Seal, 1989; Nave et al., 2002; Coulson et al., 2008; Lohr et al.,
2009). However, steroid implants have the potential for transferring active ingre-
dients to predators and scavengers.
Biobullets are biodegradable projectiles used for remote administration of
veterinary products (DeNicola et al., 2000). Syringe-darts, routinely employed
to anaesthetise wild animals, have also been used to administer contraceptives
to large ungulates at ranges of ≤40 m (Rudolph et al., 2000; Aune et al., 2002;
Delsink et al., 2006). The advantages of remote administration of contraceptives
to ungulates are that delivery can be targeted to specifi c individuals (unlike oral
delivery), and that this method minimises the welfare and economic costs of trap-
ping (Kreeger, 1997). Potential disadvantages of these delivery systems include
the inability to identify successfully vaccinated animals, cost, dose regulation and
incomplete intra-muscular injection (De Nicola et al., 1997; Kreeger, 1997; Aune
et al., 2002). The inability to identify previously vaccinated animals is important
because these animals can receive multiple doses: whilst this is not expected to
have welfare costs, it certainly reduces the effi ciency of any fertility control pro-
gramme. Another approach to a single-dose, multiple-year immunocontraceptive
is to mimic the effects of booster injections by incorporating the vaccine into con-
trolled-released polymers formulated as injectable pellets. This approach was suc-
cessfully tested with wild horses by using simultaneous intramuscular injection of
1-, 3- and 12-month pellets to provide in vivo delivery of booster doses of the PZP
vaccine (Turner et al., 2007; Rutberg et al., 2013).
Injectable forms of fertility control vaccines have been shown to effectively
block fertility in a number of species. However, to be of further practical use
in wildlife management, more effi cient means of delivery are required. There
is great interest in the development of mucosal (e.g. oral or intranasal) vac-
cines in human pharmaceuticals (reviewed in Woodrow et. al., 2012) and this
will aid in efforts towards wildlife applications where some research has already
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Novel Management Methods 219
been conducted (Cui et al., 2010). Once developed, oral fertility control agents
are likely to be less expensive to administer than injectable forms, in part, because
capture and handling of animals will not be necessary for the delivery of these
contraceptives. However, unlike injectable vaccines, oral fertility control agents
will likely require repeated applications to cause infertility (Cross et al., 2011).
As oral forms of fertility control might also affect non-target animals, species
specifi city could be achieved through targeted delivery methods. One example
is the BOS (Boar-Operated System) developed as a specifi c delivery system for
wild boar and feral pigs (Massei et al., 2012c; Long et al., 2010; Campbell et al.,
2011) (Figure 10.2).
Immunocontraceptive vaccines delivered through genetically modifi ed, self-
sustaining infectious vectors have been developed in Australia. Criticism of this
approach involved concerns regarding irreversibility, the diffi culty of controlling
the vectors once released, possible mutations of the vectors that could affect non-
target species and possible development of resistance (Barlow, 2000; Williams,
Figure 10.2 Free-living wild boar feeding on maize-based baits from a Boar-Operated
System (BOS). The metal cone slides along the pole and fully encloses the base onto which
the baits are placed. Several studies found that free-living wild boar and wild pigs fed regu-
larly from the BOS and that the device successfully prevented bait uptake by non-target
species. The BOS can be used to deliver vaccines, contraceptives or other pharmaceuticals
employed to manage overabundant populations of wild suids.
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220 Massei, Cowan and Eckery
2002). In New Zealand genetically modifi ed transmissible organisms, such as
species-specifi c nematode parasites, have been explored to deliver contraceptives,
although no data are available for ungulates (McDowell et al., 2006; Cowan et al.,
2008; Cross et al., 2011).
10.3 Fertility control and population responses
Most recent fi eld studies on fertility control have used immunocontraceptives,
whilst modelling studies have focussed on generic contraceptives of different lev-
els and duration of induced infertility (Table 10.2). Comparing the relative merits
of fertility and lethal control to manage overabundant populations, recent research
suggests that large, long-lived species are easier to manage with fertility control
than smaller, shorter-lived ones because a lower proportion of the population must
be targeted each year (Hone, 1999), particularly if lifelong contraceptives are
employed (Hobbs et al., 2000).
Modelling the impact of fertility control versus culling for a geographically
closed population of white-tailed deer, Merrill et al. (2003) concluded that, for
instance, to achieve a 60 per cent reduction over 4 years, culling should remove
40 per cent of available fertile females each year. To maintain this level of reduc-
tion, only 13 per cent of the available females should be sterilised every year.
Based on this model, the authors suggest that an effective management strategy
to control overabundant urban deer populations would require two steps. The fi rst
step will reduce the population to a given level: to achieve this, culling would
be more effi cient than sterilisation. The second step will maintain the population
at a set level and sterilisation will become more effi cient as the number of steri-
lised females increases (Hobbs et al., 2000). However, in long-lived species and in
populations characterised by slow turnover, the benefi ts of using fertility control
to decrease population size will only accrue in the long term (Twigg et al., 2000;
Kirkpatrick and Turner, 2008; Cowan and Massei, 2008).
The effects of fertility control on population dynamics also depend on species-
specifi c social and reproductive behaviours, on the type of contraceptive used and
on its mode of action, as well as on whether a population is isolated or open. There
is general consensus that fertility control is most effective for managing relatively
small (50–200 animals) isolated populations of ungulates (Rudolph et al., 2000;
Kirkpatrick and Turner, 2008). Avoiding disruption of behaviour is crucial, as
fertility-control-induced changes in immigration and emigration might prevent
fertility control achieving the required reduction in population growth (e.g. Davis
and Pech, 2002; Merril et al., 2006).
On the other hand, using fertility control methods that inhibit normal sex-
ual behaviour can potentially reduce disease transmission by decreasing con-
tact rates between individuals (Caley and Ramsey, 2001; Ramsey, 2007). For
instance, a reduction of reproductive behaviour would result in decreased trans-
mission of venereal diseases such as pseudorabies and brucellosis (Miller et al.,
2004; Killian et al., 2006). In this context, methods that prevent ovulation are
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Novel Management Methods 221
likely to be more successful at decreasing disease transmission than those that
only block fertilisation. When only fertilisation is blocked, females of many
ungulate species will continue to ovulate, thus attracting males (Putman, 1997;
Miller et al., 2000; Curtis et al., 2007; Nuñez et al., 2009, 2010). This may have
signifi cant effects on prolonging the duration of the rut, enhancing and extend-
ing the period of male–male competition (and thus increasing risk of injury or
male exhaustion).
The factors affecting emigration and immigration in ungulate populations
managed through fertility control have received little attention. For instance, a
reduction in population density due to fertility control might increase immigra-
tion rate, thus negating the benefi ts of using non-lethal population management.
On the other hand, fertility control might also encourage emigration, particu-
larly of males looking for mating opportunities outside their normal home range.
As female white-tailed deer in urban and suburban areas have relatively small
home range size and high site fi delity (Grund et al., 2002), it is possible to
hypothesise that fertility control will not affect the movements of these animals.
Other studies found that ZP-based immunocontraceptives did not affect spatial
behaviour in white-tailed deer and feral horses (Hernandez et al., 2006; Ransom
et al., 2010).
Density-dependent regulation of population should also be taken into account:
Merrill et al. (2003) suggested that if density-dependence was occurring, it would
increase the effectiveness of sterilisation as the reproductive removal (but not the
physical removal) of part of the population would intensify density-dependent
feedback. Clearly, this is an area where more fi eld studies are warranted to assess
the effects of fertility control on emigration, immigration, recruitment and mortal-
ity in ungulate populations with different life-history traits.
Fertility control has been associated with increased survival and improved health
condition, probably due to the reduced expenditure of energy normally required
for reproduction. For example, sterilization-induced increases in survival and total
food consumption in feral Soay rams caused an increase in both animal density
and impact on the plant community (Jewell, 1986). Similarly, as immunocontra-
ceptives can signifi cantly extend lifespan and improve body condition (Turner and
Kirkpatrick, 2002; Kirkpatrick and Turner, 2007; Gionfriddo et al., 2011b), the
impact of increased survival on population dynamics must be taken into account
when using fertility control to manage ungulate populations.
Fertility control in ungulates has been used to decrease population size or
growth, reduce vertical or horizontal transmission of diseases or reduce impacts
of local populations on human activities (Table 10.2). The relative merits of
fertility control and culling have been much debated, with advocates of the two
methods often holding opposite, irreconcilable positions (Kirkpatrick, 2007;
Curtis et al., 2008; Fagerstone et al., 2010). Modelling studies concluded that
in several instances the outcome of the two methods in reducing population size
or disease transmission depends on the defi nition of ‘effi ciency’. If effi ciency is
defi ned in terms of the time taken to achieve the desired effect, then culling is
Chapter 10.indd 221Chapter 10.indd 221 6/28/2014 11:57:48 AM6/28/2014 11:57:48 AM
222 Massei, Cowan and Eckery
Table 10.2 Examples of empirical and theoretical applications of fertility control (FC) at population level in wildlife and in feral ungulate
populations.
Aim Species Trial Method Results and conclusions Reference
Evaluate impact of FC
on population size
White-tailed deer
Odocoileus
virginianus
Field PZP vaccine FC feasible to maintain small (<200)
suburban deer populations at
30–70% of carrying capacity
Rudolph et al.
(2000)
White-tailed deer Field PZP vaccine FC induced a 7.9% population decline
in a suburban deer population
Rutberg et al.
(2004)
White-tailed deer Field and
model
PZP vaccine FC caused a 27–58% % decline in
population size in the 5–10 years
following treatment of females
Rutberg and Naugle
(2008)
Wild horse
(Equus
caballus)
Field PZP vaccine The effort required to achieve zero
population growth decreased, as
95, 83, 84, 59 and 52% of all adult
mares were treated in the fi rst
5 years FC increased longevity and
improved body condition
Turner and
Kirkpatrick
(2002)
Wild horse Field PZP vaccine FC prevented population growth
within 2 years; by year 11, the
population had declined by 22.8%.
FC also increased longevity of mares
Kirkpatrick and
Turner (2008)
Wild horse Model PZP vaccine FC can be used to reduce population
size to the target number in 5–8 years
Ballou et al. (2008)
Elephant
Loxodonta
africana
Field PZP vaccine FC prevented population growth Delsink (2006)
Chapter 10.indd 222Chapter 10.indd 222 6/28/2014 11:57:48 AM6/28/2014 11:57:48 AM
Novel Management Methods 223
Elephant Model Immuno-
contraception
‘Rotational’ FC can be used to increase
calving interval, slow population
growth rate and alter age structure
Druce et al. (2011)
Wildlife Model Generic
contraception
FC was more effective than culling in
reducing population size for medium
and large-size animals
Zhang (2000)
White-tailed deer Model Generic
contraceptive
FC was more effi cient than culling
in reducing population size pro-
vided >50% females are maintained
infertile
Hobbs et al. (2000)
Wapiti Cervus
elaphus
Model Yearlong vs.
lifelong
contraceptive
FC using lifetime contraceptives was
more effi cient than any other popula-
tion control option
Bradford and
Hobbs (2008)
Evaluate impact of
removal and FC on
population size
Feral horse Model Generic
contraception
Compared to removal, FC resulted
in smaller, less fl uctuating popula-
tion size
Gross (2000)
Evaluate factors affect-
ing time to reduce a
population through FC
White-tailed deer Model Permanent
sterilisazion
FC could reduce a population by
30–60% in 4–10 years if 25–50% of
fertile females were sterilised every
year
Merrill et al. (2003)
Evaluate effects of
immigration, stochas-
ticity and variation
in capture process on
FC to manage popu-
lation size
White-tailed deer Model Permanent
sterilisazion
FC was unlikely to reduce the size of
an open population. In a closed popu-
lation, permanent sterilisation could
reduce population size if 30–45%
deer were captured each year
Merrill et al. (2006)
Chapter 10.indd 223Chapter 10.indd 223 6/28/2014 11:57:48 AM6/28/2014 11:57:48 AM
224 Massei, Cowan and Eckery
always the most effi cient solution (Bradford and Hobbs, 2008). Conversely, if
effi ciency is defi ned as the proportion of the population to be targeted, fertility
control can be regarded as potentially more effi cient than culling (Hobbs et al.,
2000; Merrill et al., 2003). By defi ning effi ciency as the proportion of the popu-
lation that must be treated, the time and costs required are deliberately ignored
(Merrill et al., 2003). In this scenario, modelling suggests that fertility control
agents that render animals infertile for many years are likely to be more effi cient
than culling, provided that the fertility status of the treated animals is known,
for instance, through ear-tags that identify animals previously treated with con-
traceptives.
Other advantages of fertility control over culling include:
1. Compared to fertility control, culling is more likely to cause social perturbation,
increased contact rates and hence increased likelihood of disease transmission
(e.g. Ramsey et al., 2006; Carter et al., 2007)
2. Animals in improved body condition, following treatment with contraceptives,
might be less susceptible to disease and also mount a better immune response
to disease vaccines
3. Infertile animals remain in the population, thus maintaining density-dependent
feedback to recruitment and survival (Zhang, 2000)
4. A growing recognition that fertility control in conjunction with disease vaccina-
tion can be as effective as culling to manage disease transmission (Smith and
Cheeseman, 2002).
As animals vaccinated against a disease reproduce, new susceptible indi-
viduals enter the population and dilute the level of herd immunity provided by
disease vaccination; combining disease vaccination and fertility control, to prevent
the recruitment of new susceptibles can thus reduce the effort required to eliminate
the disease (Smith and Wilkinson, 2003; Carroll et al., 2010).
In some instances, fertility control might be required to reduce or halt popula-
tion growth rather than to decrease population size. Exploring options to manage
a small, isolated population of African elephants, Druce et al. (2011) suggested
that using reversible immunocontraceptives on an individual rotational basis would
increase inter-calving intervals, stabilise population structure and lower population
growth to a predetermined rate.
Some authors have hypothesised that the use of immunocontraceptive vaccines
to manage wildlife could result in the evolution of resistance through selection for
individuals that remain fertile because of low or no response to vaccination (e.g.
Gross, 2000; Magiafoglu et al., 2003; Cooper and Larsen, 2006; Holland et al.,
2009). These authors argue that when females only are treated with immunocon-
traceptives, resistance might evolve if the response to the vaccine is specifi c for
this gender and could be inherited through the maternal line. No studies have so
far demonstrated such effects although unresponsiveness to immunocontraceptive
vaccines was found to have a genetic component in brushtail possums (Holland
et al., 2009).
Chapter 10.indd 224Chapter 10.indd 224 6/28/2014 11:57:48 AM6/28/2014 11:57:48 AM
Novel Management Methods 225
10.4 Can fertility control mitigate
human–ungulate confl icts?
Human–ungulate confl icts often demand immediate solutions. Stakeholders have
a signifi cant impact on management options but often hold opposite opinions.
For instance, animal welfare groups tend to advocate fertility control to manage
these confl icts (Curtis et al., 2008), whilst many hunting groups oppose the use of
fertility control because of concerns that this method will replace sport hunting
(Kirkpatrick, 2007; Fagerstone et al., 2010).
The studies carried out so far indicate that if fertility control is the sole method
employed to manage overabundant populations, a substantial initial effort is
required (Rudolph et al., 2000; Walter et al., 2002; Merrill et al., 2003, 2006). In
addition, changes in survival and immigration can reduce population-level effi cacy
of fertility control (Ransom et al., 2013). However, as the proportion of infertile
females increases, this effort will decline and remain constant once the desired
density has been achieved. Successful examples are the marked reduction in sub-
urban white-tailed deer obtained over a 10-year timescale (Rutberg and Naugle,
2004, 2008), the zero-population growth of an isolated population of elephants
achieved within 2 years (Delsink et al., 2006) and of an island population of wild
horses obtained within 2 years (Kirkpatrick and Turner, 2008). For closed popula-
tions, Merril et al. (2006) suggested that, at least in white-tailed deer, contraception
of 30–45 per cent of the animals would decrease population size after 2–3 years
and that a population reduction of 60 per cent would be achieved in 10 years.
Depending on how urgent the resolution of the confl ict is, fertility control can
be used alone or once the population size has been reduced through other methods
(Barlow, 1997; Hobbs et al., 2000). When fertility control is chosen to mitigate
human – ungulate confl icts, a number of issues should be considered before fi eld
applications are implemented. These issues cover humaneness, effi cacy, feasibil-
ity, cost, timeframe and sustainability as well as alternative methods for population
control. As humaneness is one of the primary public concerns regarding any type
of wildlife management, defi ning this term is crucial to obtaining and maintain-
ing public support in relation to specifi c, well-defi ned objectives. For instance,
humaneness can be defi ned as (1) the level of stress experienced by treated ani-
mals, (2) the severity and type of side effects, (3) the proportion of animals likely
to experience negative side effects following treatment with a contraceptive, (4)
the proportion of animals that will suffer from capture, handling and anaesthesia
associated with administering the contraceptives, or (5) a combination of all these
defi nitions.
When lethal control is illegal, unacceptable or unfeasible, fertility control might
be the only option available for managing overabundant populations of ungulates.
In these instances, key issues to be discussed at the planning stage include assessing
the overall proportion of the population that must be rendered infertile to mitigate
the confl ict, estimating the relative effort and time required to achieve the target
population size and evaluating the feasibility of fi eld application of contraceptives
Chapter 10.indd 225Chapter 10.indd 225 6/28/2014 11:57:48 AM6/28/2014 11:57:48 AM
226 Massei, Cowan and Eckery
(Hobbs et al., 2000; Bradford and Hobbs, 2008). This feasibility in turn is likely
to depend on factors such as animal density, approachability of individual ani-
mals, access to private and public land, and effi cacy of the contraceptive treatment
(Rudolph et al., 2000; Walter et al., 2002; Rutberg and Naugle, 2008; Boulanger
et al., 2012). In the early planning stages, modelling the impact of fertility con-
trol on population dynamics can assist determining whether the application of this
method will meet specifi c management goals (e.g. Jacob et al., 2008).
The economic cost of reducing ungulate population growth through fertility
control agents that require capture and handling of the animals is expected to be
high. For instance, Rutberg (2005) estimated that the cost of rendering infertile
a medium-to-large size individual mammal varied between US$25 and US$500.
Delsink et al. (2007) calculated that in 2005 the average cost of managing ele-
phants through aerial vaccination with immunocontraceptives was US$98–110 per
animal, inclusive of darts, vaccine, helicopter and veterinary assistance. Walter
et al. (2002) reported that the cost of trapping and injecting 30 white-tailed
deer with immunocontraceptives for 2 years (with a spring capture and vaccina-
tion followed by two boosters in autumn of year 1 and year 2) was US$1128/deer.
Labour accounted for 64 per cent of the total cost and equipment, supplies, lodg-
ing and travel accounted for the remaining 36 per cent of the total cost. However,
after the initial year, the cost per deer dropped to US$270 (Walter et al., 2002).
Boulanger et al. (2012) found that the cost of capture, handling and administering
contraceptives to white-tailed deer in various studies was about US$1,000 but that
75 per cent of this cost was due to drugs, including anaesthetics, and a veterinar-
ian’s time. It is conceivable that costs would drop signifi cantly if immunocon-
traceptives were delivered by trained staff (i.e. by wildlife managers instead of
veterinarians) and ungulate capture was organised with the assistance of volun-
teers donating their time and skills to the project. Hobbs et al. (2000) suggested
that fertility control of deer will only be cost-effective, compared to culling, where
professionals are employed to cull deer instead of recreational hunters.
Identifying who should bear the costs of population management might raise
awareness of the economics of available options amongst stakeholders and add a
different perspective to ungulate management. This awareness would be further
enhanced if the full costs, including negative environmental and welfare conse-
quences, associated with each option are included.
In addition to the practical challenges of using fertility control on ungulate
populations, regulatory and legal requirements for fi eld applications of contracep-
tives must be met. For products that have not been registered in a country, trials
can often be carried out under experimental permits and on a case-by-case basis
(Humphrys and Lapidge, 2008).
In summary, this review highlighted that safe, effective contraceptives are now
available allowing fi eld applications aimed at reducing population growth in ungu-
lates. Although many challenges still exist, we believe the next decade will witness
a large number of fi eld studies carried out to manage ungulate populations through
fertility control. We recommend that, for each context, the use of fertility control,
Chapter 10.indd 226Chapter 10.indd 226 6/28/2014 11:57:48 AM6/28/2014 11:57:48 AM
Novel Management Methods 227
alone or in conjunction with other methods, is evaluated and compared with alter-
native options for population control. Only then can the costs and benefi ts of dif-
ferent methods be fully established and the optimum options selected to mitigate
the confl icts between human interests and ungulate populations.
Acknowledgements
The authors would like to thank Alastair Ward for reading the manuscript and
providing comments and suggestions.
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