Journal of Applied
© 2001 British
Blackwell Science Ltd
Estimating disease transmission in wildlife, with emphasis
on leptospirosis and bovine tuberculosis in possums, and
effects of fertility control
PETER CALEY*† and DAVE RAMSEY*‡
*Landcare Research and ‡Marsupial Cooperative Research Centre at Landcare Research, Private Bag 11052,
Palmerston North 5301, New Zealand; and †Applied Ecology Group, University of Canberra, ACT 2601, Australia
1. We present methods for estimating disease transmission coefficients in wildlife, using
Leptospira interrogans infection (a bacterial disease transmitted predominantly during
social contacts) in brushtail possums Trichosurus vulpecula as a model system.
2. Using data from a field experiment conducted on a naturally infected possum
population, we estimated disease transmission coefficients assuming either ‘density-
dependent’ or ‘frequency-dependent’ transmission.
3. A model-selection approach determined that density-dependent transmission was
the most appropriate form of the transmission of L. interrogans infection in brushtail
4. We used the chosen model of transmission to examine experimentally the effect of
tubally ligating female brushtail possums on the epidemiology of L. interrogans. The
estimated transmission coefficient was 28% higher (P = 0·16) in populations subject to
tubal ligation, raising the possibility that fertility control of this type may increase dis-
ease transmission rates.
5. Altering mating behaviour through fertility control may have the potential to control
diseases such as bovine tuberculosis in brushtail possums, although the potential of
fertility control techniques to change disease transmission coefficients and disease
epidemiology requires further investigation. This would require models that exam-
ine the combined effects of fertility control on population dynamics, social behaviour
and disease transmission coefficients simultaneously.
Key-words: epidemiology, Leptospira interrogans, modelling, Mycobacterium bovis,
Journal of Applied Ecology (2001) 38, 1362–1370
Based on the projections of host–pathogen models,
reducing susceptible host abundance is often proposed
as a strategy for eradicating diseases from wildlife
populations, such as Mycobacterium bovis (Karlson &
Lessel) infection (bovine tuberculosis) in brushtail
possums Trichosurus vulpecula (Kerr) (Barlow 1991b,
1996; Roberts 1996) and badgers Meles meles (L.)
(White & Harris 1995), and Brucella abortus infection
(brucellosis) in bison Bison bison (L.) (Dobson &
Meagher 1996). Indeed, reducing the population den-
sity of animals is one of the most frequently attempted
management strategies for controlling disease in wild
animals (Wobeser 1994). This logically follows from
the paradigm of threshold density for the establish-
ment and persistence of disease (Kermack & McKen-
drick 1927; Anderson & May 1979; May & Anderson
1979) and the implicit assumption underlying this par-
adigm that disease transmission scales positively with
abundance. However, the projections of these host–
pathogen models are greatly affected by the way in
which transmission between infected and susceptible
hosts is modelled (McCallum, Barlow & Hone 2001).
Estimating disease transmission coefficients is con-
sidered to be a very difficult parameter estimation
problem (Anderson & May 1991) and remains a great
challenge in field ecology today (McCallum, Barlow &
Hone 2001). Disease transmission coefficients are
model-dependent, and an important issue is the form
of the model for the scaling between host population
density and parasite transmission rate (McCallum,
Correspondence: P. Caley, Landcare Research, Private Bag
11052, Palmerston North 5301, New Zealand (fax + 64 6355
9230; e-mail email@example.com).
© 2001 British
Journal of Applied
Barlow & Hone 2001; Grenfell & Bolker 1998 and ref-
erences therein). Resolving this issue can be considered
a model-selection problem for which Akaike’s infor-
mation criterion (AIC) provides an approach for
choosing between competing models of transmission
(Burnham & Anderson 1998), providing data sets exist.
Studies that estimate transmission coefficients for
diseases of free-living vertebrates, let alone estimate
the effect of management on disease transmission, are
uncommon in both the laboratory (Bouma, De Jong &
Kimman 1995) and the field (Hone, Pech & Yip 1992;
Swinton et al. 1997; Begon et al. 1999). A result of this
is a general paucity of data on transmission rates (De
Leo & Dobson 1996).
Reducing susceptible host abundance and/or popu-
lation density may be achieved by a variety of means,
such as lethal control, vaccination or reducing fertility
(fertility control). Fertility control has been proposed
as an alternative non-lethal tactic for reducing the
abundance of species such as brushtail possums (Bar-
low 1996; Cowan 1996; Barlow, Kean & Briggs 1997)
and badgers (Swinton et al. 1997; Tuyttens & Macdon-
ald 1998) below the threshold for disease (M. bovis)
persistence. Here, fertility control is broadly defined as
a reduction in the birth rate that should decrease the
rate of population increase, assuming no compensa-
tory change occurs in the death rate (Hone 1992). The
possibility that population control may cause a change
in transmission coefficients through effects on social
behaviour is receiving increasing theoretical interest.
For example, social perturbation arising from lethal
control of badgers may act to promote transmission of
M. bovis (Swinton et al. 1997). In contrast, Tuyttens &
Macdonald (1998) considered that fertility control
(sterilization) of badgers could reduce vertical trans-
mission of M. bovis, and transmission of M. bovis
during mating through changed behaviour.
Endemic M. bovis infection in New Zealand possum
populations is the single biggest threat to the nation’s
livestock industry, with M. bovis-infected possums
occurring over about 24% of the land mass (Coleman &
Caley 2000). The presence of this wildlife reservoir of
M. bovis infection has hampered efforts at controlling
the disease in livestock (O’Neil & Pharo 1995; Coleman
& Caley 2000), similar to the problem encountered in
England (Zuckerman 1981) and Ireland (OMairtin
et al. 1998a,b) arising from M. bovis-infected badgers.
While reducing abundance by non-selective culling is
presently the primary strategy for controlling M. bovis
infection in brushtail possum populations in New Zea-
land (Barlow 1991b; Caley et al. 1999), fertility control
is being pursued as an alternative method of reducing
abundance (Cowan 1996, 2000). Methods of fertility
control that block fertilization, such as immunocontra-
ception, may leave the endocrine system intact. Thus
sterile but hormonally competent females may have
an increased frequency of mating contacts due to an
increased frequency of oestrus, as observed in white-
tailed deer Odoicoileus virginianus (Miller) (McShea
et al. 1997) and elk Cervus elaphus (Bailey) (Heilmann
et al. 1998) subjected to this type of contraception.
This prediction is supported for brushtail possums by a
field trial by Ji, Clout & Sarre (2000). Whilst increased
frequency of mating could enhance the transmission
of a hypothetical transmissible biocontrol vector in
brushtail possums (Barlow 1994), it could possibly also
increase the transmission coefficient of M. bovis, thus
negating some of the benefits of reduced abundance
resulting from fertility control. Alternatively, methods
of fertility control that target endocrine control of
reproduction may result in behavioural changes, in-
cluding inhibition of mating behaviour. For brushtail
possums this could mean reduced sexual contacts and
possibly also reduced agonistic contacts, which would
be associated with a reduction in disease transmission.
Clearly, altered behaviour arising from fertility control
techniques potentially may help or hinder disease man-
agement in wildlife, although little attention has been
given to altering high risk behaviour of wildlife to
reduce disease transmission. This is in contrast to the
management of disease in humans, where behaviour
modification (e.g. changing sexual habits in the case of
sexually transmitted diseases) is one of the most com-
monly used methods of management of public health
(Anderson & May 1991; Morris 1996).
In this paper, we present methods for estimating
disease transmission coefficients in wildlife, using
Leptospira interrogans serovar balcanica (Kmety &
Dikken 1993) (hereafter L. balcanica) infection in
brushtail possums as a model system. We compared
two models of transmission (density-dependent and
frequency-dependent) and used the selected best
model to estimate from a field experiment the effect of
behavioural changes induced by fertility control (here
tubally ligating female possums) on the transmission of
disease. We then examined the theoretical implications
of attempting to use fertility control to manage M. bovis
infection in brushtail possums.
Materials and methods
The ability of a pathogen to establish and persist in
animal populations is largely determined by the basic
reproductive rate of the disease (Ro). This is defined as
the expected number of secondary infections caused in
an entirely susceptible population by a typical infected
host. By definition, if Ro is greater than or equal to
unity the disease will establish and, conversely, if Ro is
less than unity the disease will fail to establish (Ander-
son & May 1991). We use a simplified version of the
compartment model for a directly transmitted disease,
as presented by Anderson & May (1979), to illustrate
the possible effects of fertility control relative to that of
culling and vaccination. We choose a model with hor-
izontal transmission, a negligible latent period and no
P. Caley &
© 2001 British
Journal of Applied
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Received 18 September 2000; revision received 16 August 2001