Spatial perturbation caused by a badger (Meles meles)

culling operation: implications for the function of

territoriality and the control of bovine tuberculosis

(Mycobacterium bovis)

F. A. M. TUYTTENS*, R. J. DELAHAY{ , D. W. MACDONALD*,

C. L. CHEESEMAN{ , B. LONG* and C. A. DONNELLY{*Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, South Parks Road,

Oxford OX1 3PS; {Central Science Laboratory, Sand Hutton, York YO4 1LW; {Wellcome Trust Centre for

the Epidemiology of Infectious Disease, Department of Zoology, University of Oxford, South Parks Road,

Oxford OX1 3PS, UK

Summary

1. The spatial organization of a badger population (North Nibley) is described

before and after it was subjected to a UK Ministry of Agriculture, Fisheries and

Food badger removal operation (BRO) intended to control bovine tuberculosis.

Comparison is made with an undisturbed badger population (Woodchester Park).

2. The Woodchester Park population was organized in group territories with

clearly de®ned boundaries that remained stable during the 3 years of study (1995±

97). In North Nibley, however, the badgers' spatial organization was severely per-

turbed in the ®rst year and, to a lesser extent, also in the second year after the

BRO, with badgers using latrines further away from their setts. This resulted in

enlarged social group ranges that were di�cult to de®ne and overlapped consider-

ably.

3. The disturbance was observed in the removal groups, those immediately adja-

cent, as well as those at a distance of one or two social groups from the removal

area, with an unexpected indication that the latter groups may have been the most

a�ected.

4. The apparent increase in the size of the group ranges in North Nibley was likely

to have been caused by an increased proportion of badgers making extra-group

excursions in the aftermath of the BRO.

5. Initial recolonization was almost exclusively by females.

6. Although such perturbation might be expected to facilitate disease transmission

between badger social groups, there was no evidence that any infectious animals

had survived the BRO. However, there were further cattle breakdowns in the area.

7. The behaviour of badgers after the BRO also provided an opportunity to test

predictions made by competing hypotheses about the main determinants of the

badger's socio-spatial behaviour.

Key-words: bait-marking, disease control, infanticide, radio-tracking, spatial orga-

nization.

Journal of Animal Ecology (2000) 69, 815±828

Introduction

The dynamics of infectious diseases can be in¯u-

enced by the spatial organization of the host. For

example, it has been hypothesized that culling foxes

may be counter-productive for rabies control by

Correspondence: Frank Tuyttens, Department of

Mechanization, Labour, Buildings, Animal Welfare and

Environmental Protection, Van Gansberghelaan 115, 9820

Merelbeke, Belgium., E-mail:: dvl@clo.fgov.be, Fax:� 32

(0)92722801, Tel.:� 32 (0)92722768,

Journal of Animal

Ecology 2000,

69, 815±828

# 2000 British

Ecological Society

creating a vacuum e�ect, drawing in foxes from

other areas or otherwise increasing contact rates

(Macdonald 1995). In this paper we investigate

whether badger (Meles meles Linnaeus) culling

operations in the UK may result in similarly unfa-

vourable consequences for the control of bovine

tuberculosis (TB).

Considerable circumstantial evidence suggests

that the badger is a wildlife reservoir of Mycobacter-

ium bovis (the causative agent of bovine TB). Trans-

mission of infection from this wildlife reservoir to

cattle is believed to be at least partly responsible for

the failure to eradicate TB from British cattle herds,

particularly in the south-west of the country where

badger density is highest (Krebs et al. 1997).

Between 1975 and 1997, the UK Ministry of Agri-

culture, Fisheries and Food (MAFF) implemented a

series of strategies for culling badgers in areas where

they were thought to be responsible for infection in

cattle. However, despite these `Badger Removal

Operations' (BROs), the proportion of cattle herds

with infected animals in south-west England is

higher now than before the onset of culling (Krebs

et al. 1997). This raised the question of whether

BROs might be counter-productive for the control

of the disease. Several authors have suggested that

the perturbation of an otherwise stable social struc-

ture caused by culling operations could facilitate the

spread of disease (Overend 1980; Tuyttens & Mac-

donald 1998, 2000). Furthermore, computer simula-

tions support this as a theoretical possibility (White

& Harris 1995; Swinton et al. 1997).

In order to understand the potential mechanism

for the perturbation e�ect, it is necessary to elabo-

rate brie¯y on the relationship between TB epide-

miology and the socio-spatial organization of

badgers. The most likely route of transmission of

M. bovis from badger to cattle is when cattle come

into contact with urine, faeces and sputum of infec-

tious badgers, although direct contact resulting in

inhalation or ingestion of bacteria cannot be ruled

out (Krebs et al. 1997). Badgers are most likely to

become infected via the respiratory route and, to a

lesser extent, from bite wounds (Cheeseman, Wile-

smith & Stuart 1989; Fagan 1993). In undisturbed,

medium-to-high density populations, badgers live in

mixed-sex groups of up to 35 animals that defend a

communal range (`territory'), which typically

includes several setts. These setts provide ideal con-

ditions for the spread of respiratory infections (Gal-

lagher, Muirhead & Burn 1976; Higgins, Kung &

Or 1985). Territorial boundaries between social

groups are marked by `latrines' (clusters of dung

pits), overlap little and may remain stable for many

years. This stable spatial organization combined

with the relatively low rate of dispersal may mitigate

against disease transmission between social groups.

This is consistent with the observation that in such

undisturbed populations infections of M. bovis

appear highly localized and concentrated within par-

ticular territories (Cheeseman et al. 1988). BROs

could o�er enhanced opportunities for disease trans-

fer if perturbation of this stable social structure

increased rates of contact between individuals and/

or the likelihood of successful disease transmission

during such contacts.

Movement between social groups was identi®ed

as a potential factor in disease spread in badger

populations in a study by Rogers et al. (1998) which

showed an increase in the incidence of new TB cases

in the years following high inter-group movement

rates. This illustrates that the study of badger spatial

organization is of crucial importance to understand

the transmission patterns of M. bovis infection.

However, apart from reports by Cheeseman et al.

(1993) and O'Corry-Crowe et al. (1993, 1996), the

socio-spatial behaviour and dynamics of TB within

disturbed badger populations are poorly under-

stood.

An understanding of the major determinants of

space-use in badgers would greatly enhance our abil-

ity to predict the consequences of removal opera-

tions. However, there is little consensus among

researchers about how and why a stable socio-spa-

tial organization should have evolved in high density

undisturbed badger populations (Woodro�e & Mac-

donald 1993). Several hypotheses have been sug-

gested and can be tested insofar as they make

speci®c predictions about how badgers should

respond to the removal of adjacent groups. Hence,

BROs provide an opportunity to improve our

understanding of the badger's socio-spatial organi-

zation which, in turn, could help with the formula-

tion of more optimal disease control strategies.

The Resource Dispersion Hypothesis (RDH)

states that badger social groups can develop where

resources are dispersed such that the smallest eco-

nomically defensible territory to supply year-round

needs for a pair of badgers can also sustain addi-

tional animals at no net cost to the original pair

(Kruuk 1978; Carr & Macdonald 1986). The Passive

Range Exclusion (PRE) hypothesis (Stewart, Ander-

son & Macdonald 1997) suggests that the amount of

faeces at boundary latrines signals the extent of

food depletion in neighbouring territories and,

therefore, indicates the potential gains (or losses) of

entering. The RDH predicts that badgers will gener-

ally not expand their ranges in response to the

removal of adjacent badgers, whereas according to

the PRE they may (conditional upon su�cient food

depletion within their own territory).

Non-food based hypotheses have also been sug-

gested. Roper, Shepherdson & Davies (1986) argued

that territorial behaviour is primarily related to the

defence of oestrous females by resident males. This

theory predicts that male badgers would not be

motivated to immigrate into the range of removed

groups unless some reproductively mature females

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Journal of Animal

Ecology, 69,

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had survived the culling. The main resource to be

defended could also be the sett (Doncaster & Woo-

dro�e 1993; Roper 1993), which could be related to

the deterrence of infanticide (Wol� 1993). The

infanticide deterrence hypothesis would predict

reproductively suppressed females to be the ®rst

recolonizers of vacated setts.

In this paper we describe the spatial organization

of a badger population before and after it was sub-

jected to a BRO, compared to that of a nearby,

undisturbed badger population. The aims of this

work are two-fold: (1) to investigate whether the

spatial consequences of this BRO are consistent

with the hypothesis of perturbation-induced disease

spread, and (2) to gain insight into the factors that

determine socio-spatial behaviour in badgers. We

argue that understanding badger society and the

transmission of disease within it are inseparable

topics.

Methods

STUDY AREAS AND TRAPPING

PROCEDURES

In January 1995 intradermal skin testing of cattle

identi®ed several TB positive cattle on a farm near

North Nibley in Gloucestershire, south-west Eng-

land. Badgers were identi®ed as the likely source of

infection by the State Veterinary Service and conse-

quently MAFF undertook a BRO in September

1995. The details of this BRO have been described

by Tuyttens et al. (in press). Badgers were live-

trapped in a 6�5-km2 plot (the `Trial Area') around

the index farm. Their TB-status was tested by

ELISA for four consecutive days (the `Live-Test

Week'). For up to 6 weeks, MAFF then attempted

to cage-trap, and shoot all badgers from eight setts

from which one or more ELISA-positive badgers

had been identi®ed during the Live Test Week. A

second BRO took place in the study area in June

1996, but its impact on population demography was

negligible as only two badgers were killed (Tuyttens

et al. 2000).

A 16�5-km2 study area was established around the

®rst breakdown farm in March 1995. This allowed

for the collection of data before, during and after

the BRO. Badger control had operated in the study

area in the past, so the population could not be con-

sidered as undisturbed prior to the present BRO.

These data were compared with data from the

undisturbed badger population at nearby (� 8 km)

Woodchester Park. This high-density population has

been studied since 1976 and has not been subjected

to any substantial form of human persecution, since

the 1980s. Methods of data collection were standar-

dized at the two sites.

We restrict analyses to data collected during 1995,

1996 and 1997. The ®eldwork consisted of mark-

recapture, bait-marking and radio-tracking. At

Woodchester Park live-trapping in cage-traps posi-

tioned near active setts took place during two conse-

cutive days in `spring' (May±July), `summer' (July±

September), `autumn' (September±December), and

`winter' (December±February). Data collected dur-

ing the latter trapping were ignored because there

was no winter trapping at North Nibley. The 1995

summer trapping at North Nibley was replaced by

the BRO, but otherwise trapping and sampling pro-

cedures were similar to those at Woodchester Park

(Tuyttens et al. 1999). Trapped badgers were anaes-

thetized, marked with a tattoo on initial capture,

weighed, sexed and aged (if year of birth was

known). Captured badgers were tested with an indir-

ect ELISA-test for antibodies to M. bovis (Goodger

et al. 1994), and by culture of the organisms from

faeces, urine, tracheal aspirate and pus from wounds

(Pritchard et al. 1986). However, the diagnostic

power of both tests is limited. The prevalence of

infection (percentage of badgers sampled that were

positive to the ELISA-test) was calculated before

and after the BRO within and outside the Trial

Area in North Nibley, and compared with the

Woodchester Park population.

Social group size was calculated as the number of

di�erent badgers trapped within the range of the

group during any of the three annual trapping occa-

sions, divided by the total capture probability for

that year (see Tuyttens et al. 1999).

SOCIAL GROUP RANGES

Bait-marking in early spring was used to delineate

social group ranges (Kruuk 1978). This technique

involves putting down bait consisting of a mixture

of peanuts, golden syrup and indigestible plastic

chips at each active major badger sett in the study

areas for 2±3weeks. Each sett was given a di�erent

colour of plastic chips. The study areas were then

searched for badger latrines. From the colour of the

markers in the faeces it could be deduced which

latrines were used by badgers from which sett(s).

Setts were de®ned to belong to the same social

group if the overlap between the minimum convex

polygons (MCP) drawn around the 95% outermost

latrines used by badgers from the di�erent setts

exceeded 50% in both ways. The area included in

the 95% MCP drawn around the latrines used by

any of the setts belonging to the same group, was

then de®ned as the social group range (Delahay

et al., in press). In Nibley three types of social group

were de®ned: groups that were removed during the

BRO (`removal groups'), groups that bordered

removal groups (`neighbouring groups'), and groups

that were separated from removal groups by at least

one social group (`other groups').

Ranges V (ITE, Wareham, Dorset) was used to

calculate the size and percentage overlap of social

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group ranges, and the distances from the setts where

bait was put down to every latrine in which corre-

sponding colour markers had been found. The mean

sett-latrine distance was calculated for each social

group each year. The e�ect of the BRO on sett-

latrine distances and group range areas were investi-

gated using an analysis of variance with nested

social group e�ects (SAS 1996) at two levels of

detail. First, we tested whether the pattern of annual

variation in sett-latrine distances or range areas dif-

fered between study sites. Secondly, we tested

whether this annual variation within North Nibley

was consistent in the three types of group.

INDIVIDUAL HOME RANGES

During 1995 in North Nibley adult badgers were

radio-tracked at night just before (June±August),

during (September) and immediately after (October)

the BRO. In the following two years, radio-tracking

took place during the same three periods of the

year. In 1997, however, there was an additional

radio-tracking period in March coinciding with the

period when bait was being put down for the bait-

marking trial. No badgers were radio-tracked at

night in Woodchester Park, with the exception of

September 1996. In all cases, badgers were radio-

tracked on foot with Mariner receivers and three-

element antennae (Mariner Radar, Lowestoft, Suf-

folk). To aid observation at night, a small lumines-

cent `beta-light' (Saunders & Roe, Hayes,

Middlesex) was attached to the radio-collars (Bio-

track, Wareham, Dorset). Each radio-tracker fol-

lowed a focal badger from the time it emerged from

the sett until it returned, while additional ®xes for

other badgers were collected opportunistically. Only

Fig. 1. Badger social group ranges for (a) Woodchester Park and (b) North Nibley from 1995 to 1997. Boundaries of social

group ranges are estimated as 95% minimum convex polygons drawn around the latrines used by each group of badgers as

revealed by annual bait-marking in spring. The groups and setts that were removed during the BRO in September 1995 in

North Nibley are in bold. Badgers from the sett BB were also removed but their range was not known in 1995. Key: (a) A,

West; B, Larch; C, Cedar; D, Beech; E, Arthurs; F, Jacks; G, Fieldfarm; H, Junction; I, Septic tank; J, Hedge; K, Yew; L,

Top; M, Honeywell; N, Colepark; O, Wychelm; P, Kennel; Q, Peglars; R, Colliers Wood; S, Old Oak; T, Nettle; U,

Atcombe West; V, Atcombe Corner; W, Parkmill; X, Woodfarm; Y, Windsoredge; Z, Inchbrook; AA, Woodrush. (b) A,

Piers Court; B, Maggs; C, Yercombe; D, Ammonite; E, Fortune; F, Holts; G, Helicopter; H, Middle Wick; I, Boisley

Wood; J, Footpath; K, Maitlands; L, Villa; M, Park Bank; N, Peninsula; O, Warend; P. Nuclear; Q, Millend; R, Ruby's; S,

Quarry; T, Sharncli�e; U, Monument; V, Lay-by; W, Brackenbury; X, Waterley; Y, Steep bank; Z, Spuncombe; AA, Wes-

tridge; BB, New Sett; CC, Garlic; DD, Drakestone.

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direct observations of beta-lights were used as ®xes,

because the magnitude of error of triangulated ®xes

was sometimes unacceptable (>20m). Fixes were

marked on a map every 15min when possible, or

more frequently if the animal moved substantially.

Home ranges were calculated only if at least 60

®xes, each being 1 h apart (to ensure su�cient tem-

poral range), had been collected per animal per per-

iod. We checked that the size of the majority of

home ranges had reached an asymptote at this cut-

o� point. Home ranges were estimated as 95%

MCPs (arithmetic mean as focal site) using Ranges

V.

Generalized linear models (GLM), ®tted using

generalized estimating equations, were used to test

for an association between various variables and

home range size (log-transformed). Standard covari-

ates included in all models were (if available): sex,

year, radio tracking period and type of group.

Adjusting for these covariates we tested for the

e�ects of age (`yearling' or `older' if this was

known), TB-status (`positive' if the animal had a

positive ELISA or culture test in the trapping occa-

sion just before the relevant radio-tracking period, if

not `negative'), study area and the March radio-

tracking period as compared to the other periods in

1997. In order to investigate the short-term conse-

quences of the BRO in North Nibley we tested for

an e�ect of period and the period*type of group

interaction on home-range size using the same

model, but restricted to 1995 data only. In order to

investigate the long-term consequences of the BRO

we tested for an e�ect of year and the year*type of

group interaction on the June±August home ranges.

The proportion of home ranges that included

focal setts belonging to more than one social group

was compared between radio-tracking periods. A

focal sett was de®ned as any main, annexe or sub-

sidiary sett (sensu Wilson, Harris & Mclaren 1997)

Fig. 1. Continued.

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that had been considered to be su�ciently active to

be included in the bait-marking trial that year.

Results

SOCIAL GROUP RANGES

For the 3 years of study, a core of 21 social groups

was identi®ed at North Nibley and of 23 groups at

Woodchester Park, occupying 13�4 km2 and 8 km2

of the respective study areas (Fig. 1). During the

BRO in North Nibley 27 badgers were killed. The

eight setts that had been trapped during this BRO

belonged to six social groups. Eleven social groups

were identi®ed as direct neighbours to the removal

groups, and ®ve social groups were separated from

them by at least one social group.

Mean sett-latrine distances were greater at North

Nibley than at Woodchester Park (Fig. 2a). This dif-

ference was most pronounced in 1996, the ®rst year

after the BRO. Furthermore, at Woodchester Park

the mean sett-latrine distance remained constant

during the 3 years of study, whereas at North Nib-

ley it increased by 35% from 1995 to 1996 and then

decreased by 10% the following year. This year*-

study site interaction was statistically signi®cant

(F2,84� 4�97, P� 0�009). Figure 2(b) shows that var-

iations in group range size between years also dif-

fered across study sites (year*study area: F2,84�4�55, P� 0�013). At Woodchester Park the mean

group range remained roughly constant in size dur-

ing the 3 years of study, whereas at North Nibley it

increased in size by 68% between 1995 and 1996. In

Fig. 2. Mean (� SE) (a) badger sett±latrine distances (b)

size of social group ranges, and (c) percentage overlap

between social group ranges in Woodchester Park (WP)

and North Nibley (NN) during 1995±97.

Fig. 3. Comparison of the mean (�SE) (a) badger sett±

latrine distances and (b) size of social group ranges for

three types of group at North Nibley: Removed � groups

that were removed during the BRO in September 1995,

Neighbour � groups adjacent to removal groups and

Other � other groups further away from the removal

groups.

820Spatial

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the spring of 1997 the mean group range size had

decreased by 37% of the 1996 mean size. As a con-

sequence of this increase in range size following the

BRO in North Nibley, percentage overlap between

all pairs of group ranges also peaked in 1996 (Fig.

2c).

Figure 3 shows that the peaks in sett-latrine dis-

tance and group range size at North Nibley in 1996

were predominantly due to the other groups, rather

than the removal groups or their direct neighbours.

Indeed, the ranges of the ®ve other groups had con-

sistently and considerably increased in size from

1995 to 1996. The mean range of the neighbouring

groups had also increased in size, but to a far lesser

extent and with two exceptions (Villa and Sharn-

cli�e). Amongst the ®ve removal groups (excluding

New Sett) the pattern was even less consistent. The

range of three groups had decreased in size between

1995 and 1996, while the range of one group (Wes-

tridge) was unaltered, and that of another (Park

Bank) had increased 3±4-fold (Fig. 1). It might be

signi®cant that a female cub and an adult male (and

cub) survived the BRO in Westridge and Park

Bank, respectively, whereas we had no evidence that

any badgers survived the culling in the other

removal groups. This year*group type interaction

was statistically signi®cant for group range areas

(F4,36� 2�81, P� 0�040), but not for sett-latrine dis-

tances (F4,36� 1�2, P� 0�327).The neighbouring groups (with the exception of

Quarry) could be classi®ed as `invaders' (Footpath,

Ruby, Waterley, Monument and Lay-by) or `non-

invaders' (Nuclear, Spuncombe, Villa, Sharncli�e

and Brackenbury) according to whether or not they

had expanded their range by 1996 to incorporate

part of the vacated habitat of the removal groups.

Four of the ®ve groups classi®ed as invaders, but

only one of the ®ve non-invader groups, had at least

one badger that was known from trapping or radio-

tracking (Fig. 4) to have made extra-group excur-

sions into the range of one of the removal groups.

The majority of these badgers (7/10) were females.

One of the male invaders (A131) stayed within the

range of the removal group for a maximum period

of 4 months only, while the fate of another male

invader (A147) was not known because it has never

been captured afterwards. The third male invader

(B39) moved into the sett of a removal group only

once it had been recolonized by a sow.

INDIVIDUAL HOME RANGES

Radio-tracking allowed us to evaluate whether the

increase in the size of the social group ranges after

the BRO at North Nibley was caused by individual

members of these groups having either enlarged

short-term home ranges or less contiguous home

ranges.

There was considerable individual variation in the

size of the home ranges of male (11±211 ha) and

female (1±100 ha) badgers (Fig. 4). Home ranges of

badgers at North Nibley also varied in size by sea-

son and year (Fig. 5), being signi®cantly smaller in

1997 than in 1995 (z�ÿ 3�311, P<0�001) and in

October compared to June±August (z�ÿ 3�609, P<0�001). Male badgers had signi®cantly larger

home ranges than female badgers (z�ÿ 2�022, P�0�043). Badgers from removal groups had signi®-

cantly smaller home ranges than badgers from

groups that did not border the removal groups (z�3�504, P<0�001). However, home range size did

not di�er signi®cantly between badgers from the

removal groups and neighbouring groups (z� 1�406,P� 0�16). Variations in home range size were not

signi®cantly related to group size (z�ÿ 1�116, P�0�265), age (yearling versus older badgers: z� 0�978,P� 0�328) or TB-status (z�ÿ 0�327, P� 0�744).However, relationships with TB-status should be

interpreted with caution because only four radio-

collared badgers were identi®ed as TB-positive dur-

ing the study. Figure 5 shows that at North Nibley

in 1997 badger home range sizes did not di�er

between March and any of the other radio-tracking

periods (June±August: z� 1�542, P� 0�123; Septem-

ber: z� 1�045, P� 0�296; October: z� 1�241, P�0�215).

Figure 6 shows that badgers had signi®cantly

smaller home ranges at Woodchester Park than at

North Nibley during September 1996 (z�ÿ 3�854,P<0�001). The BRO at North Nibley was not fol-

lowed by an increase in mean home range size. On

the contrary, Fig. 5(a) shows that the average size of

the adult female ranges in 1995 were larger just

before (June±August) than during (September) or

immediately after (October) the BRO. The sample

size was too small to detect such a pattern for males

(Fig. 5b), but the single male (54A) that had been

radio-tracked during all three periods in 1995 also

ranged furthest prior to the BRO. The June±August

home ranges at Nibley decreased signi®cantly in size

from 1995 to 1996 (z�ÿ 2�193, P� 0�028). This

year di�erence was not caused by badgers from

removal groups or neighbouring groups, but by bad-

gers from groups further away. Combining home

ranges of badgers from removal and neighbouring

groups (which did not di�er), the year*group type

interaction approached statistical signi®cance (z�1�734, P� 0�083).

Only 15% of the home ranges before the BRO

included focal setts from at least two di�erent social

groups (Fig. 7). In the same radio-tracking period of

the following year, this percentage had doubled. The

home ranges of six out of 12 males (50%), but only

®ve out of 18 females (28%), included focal setts

from at least two di�erent social groups during at

least one of the radio-tracking periods after the

BRO at North Nibley (Fig. 4). The home ranges of

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Fig.4.Homeranges

(95%

minim

um

convex

polygons)

ofbadgersradio-tracked

inNorthNibleyduringJune±August

(period1),

September

(period2)andOctober

(period3)in

1995±97.Homerange

boundaries

ofpositivelyidenti®ed

yearlingsare

dashed.

822Spatial

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all but one (B18) of these ®ve sows included habitat/

setts that had been cleared during the BRO. How-

ever, only one (B39) of the six males had expanded

its range to include that of a removal group (which

by then had already been recolonized by a female).

TB PREVALENCE

Before the BRO, the percentage of trapped badgers

that were positive to the ELISA-test was higher

inside the trial area of the BRO at North Nibley

(19±29%) than outside (8%) and also higher than at

Woodchester Park (4%) (Fig. 8). The high preva-

lence of ELISA-positive badgers inside the trial area

was reduced to very low levels immediately after the

BRO. Nearly 40% (10/27) of badgers that were

killed during the BRO were found to be infected

with M. bovis by post-mortem examination and tis-

sue culture. After the BRO the TB prevalence at

North Nibley remained very low until the end of

our study in 1997. Only three ELISA-positive bad-

gers (and no culture-positives) were found after the

BRO in the entire North Nibley study area. This

contrasts with Woodchester Park where the disease

prevalence more than doubled between 1995 and

1997. It should be noted that only a positive culture

test, constitutes any evidence of infectious status.

The ELISA test cannot exclude false positives and

also detects badgers that are infected but not (yet)

infectious (Clifton-Hadley, Sayers & Stock 1995).

Discussion

The present study shows severe disruption of the

spatial organization of the North Nibley badger

population following the removal of six of its central

social groups during a BRO. In the ®rst and to a les-

Fig. 5. Mean (� SE) size of home ranges of (a) male, (b)

female and (c) all badgers radio-tracked in North Nibley

during March 1997 and during June-August, September

and October in 1995±97. Sample sizes are above error bars.

Fig. 6. Comparison of the mean (�SE) home range size of

male and female badgers radio-tracked in North Nibley

and Woodchester Park during September 1996. Sample

sizes are above error bars.

Fig. 7. Percentage (� SE) of home ranges that include

focal setts of more than one di�erent social group in North

Nibley during each radio-tracking period between 1995

and 1997.

823F. Tuyttens

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ser extent in the second year post-removal, badgers

defecated in latrines further away from their setts,

and as a result our estimates (from bait-marking) of

group range size increased signi®cantly. Conse-

quently, there was also more overlap between social

group ranges, to the extent that boundaries between

groups were largely indistinguishable and the popu-

lation could no longer be considered territorial. This

contrasted sharply with the territorial organization

of the undisturbed population at Woodchester Park

where boundaries between social groups were dis-

tinct, overlapped little and had remained relatively

stable over the 3 years of study. Our observation

that the spatial disruption of social group ranges

was not restricted to groups removed during the

BRO, di�ers from the report by Cheeseman et al.

(1993). They found that the spatial organization of

neighbouring groups was una�ected by the complete

removal of 11 social groups in the Woodchester

Park study area during the late 1970s. In the present

study, however, spatial disruption was observed not

only in surrounding groups, but even appeared most

severe in groups further away.

The present study also provided some evidence

that the e�ect of the BRO on removal groups varied

with the number, age and sex of the survivors.

Groups that had apparently been completely

removed (and then recolonized) had smaller ranges,

whereas the range of the one removal group from

which we have evidence that a male adult and cub

had survived, had substantially increased in size.

Furthermore, the range of a removal group from

which evidence suggested that only a female cub

(A67) had survived, remained unchanged. However,

shortly after the BRO this survivor moved around

in the study area to an unprecedented degree, being

recorded within the ranges of at least six di�erent

social groups as a yearling and often staying in out-

lier setts.

Radio-tracking results revealed that, 1 year after

the BRO, badgers at North Nibley had larger home

ranges than at Woodchester Park. However, radio

tracking provided no evidence that the overall

increase in the size of the social group ranges,

derived from bait-marking at North Nibley, was due

to individual members of these groups having

enlarged short-term home ranges in the aftermath of

the BRO. On the contrary, home ranges were on

average smaller in the short term after the BRO

than before. The radio-tracking trial in March 1997

(coinciding with the bait-marking trial) revealed that

home ranges at this time did not di�er from those

observed during radio tracking later in the year. It is

therefore unlikely that the apparent discrepancy

between bait-marking and radio-tracking results was

due to the two techniques being conducted at di�er-

ent times of the year. The increase in the social

group range size after the BRO was most likely due

to an increased proportion of badgers making excur-

sions beyond previous range boundaries. Males

were more likely than females to use setts from at

least two di�erent social groups in the aftermath of

the BRO. However, the home ranges of these males

very rarely included setts that had been removed

during the BRO, whereas the opposite was true for

females.

IMPLICATIONS FOR THE EVOLUTION OF

THE BADGER'S SOCIO-SPATIAL

ORGANIZATION

The value of opportunistic or experimental removal

studies to test assumptions and predictions of

hypotheses about the formation of territoriality in

many species, including the badger, has long been

recognized (Beletsky & Orians 1987; Roper & LuÈ ps

1993; Stamps 1994). For example, the view that bad-

gers are `contractors' (Kruuk & Macdonald 1985)

has been supported on the basis that partial

removals cause alterations in boundary con®gura-

tions, but not in territory size (O'Corry-Crowe et al.

1993) and that complete removals do not result in

the extension of neighbouring territories (Cheese-

man et al. 1993). These studies support the RDH,

which predicts that badgers will on average not

attempt to enlarge their territories when given the

opportunity. Woodro�e & Macdonald (1992), how-

ever, commented that when the population studied

by Cheeseman et al. (1993) was recovering, groups

formed before territories, whereas the RDH assumes

that territories are chosen and then ®lled with

groups. In contrast, the PRE hypothesis predicts

that territorial boundaries will only be established

once the density of badgers in an area is su�cient to

create a gradient of food depletion from the centre

Fig. 8. Percentage (�SE) of live-trapped badgers with a

positive result on the ELISA-test inside and outside the

trial area of the BRO at North Nibley (NN) and at Wood-

chester Park (WP), between 1995 and 1997.

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to the periphery of the group range and is therefore

consistent with groups forming before territories.

Roper & LuÈ ps (1993) reported that two adjacent

badger social groups encompassed the range of

another group from which all males had suddenly

died while the range of two other adjacent groups

had not changed. They argued that the observed

spatial disruption was more consistent with mates,

rather than food being the major determinant of

space-use in badgers. The present study illustrates

further complexity. Whereas characteristics of the

removal operation in the present study were similar

to that investigated by Cheeseman et al. (1993) the

response of the adjacent groups resembled more the

observations of Roper & LuÈ ps (1993): half the

neighbouring groups enlarged their ranges post-

removal to include parts of the cleared area, while

the remainder did not. However, most ranges had

reverted back to their pre-removal sizes by 1997, so

the RDH was not critically challenged because it

allows for badgers to recon®gure their ranges due to

the availability of vacated patches, as long as they

do not strive for long-term expansion. Neither did

the observed trends seriously challenge the PRE

hypothesis, which predicts that badgers may make

feeding excursions into a vacated neighbouring terri-

tory depending on the degree of food depletion

within their own range (which unfortunately was

not known).

If the determinants of space-use were similar for

male and female badgers, then no di�erences would

be expected between the sexes in the pattern of reco-

lonization of vacated habitat. However, in the pre-

sent study recolonization was primarily by females,

whereas boars did not seem attracted to the vacated

habitat. However, if only females remain in a group

(Roper & LuÈ ps 1993) or once a removal group

range has been recolonized by a female (e.g. badger

B39 in this study), neighbouring males might

become more motivated to move in. These observa-

tions suggest that the availability of mates is a more

important determinant of movement for male bad-

gers than for female badgers. Hypotheses based

purely on the defence of food or setts cannot explain

the observed reluctance of male badgers to recolo-

nize vacated habitats where food and unexploited

den sites may be abundant. Any functional explana-

tion for socio-spatial behaviour in badgers should

take into account such fundamental di�erences

between the sexes.

The cub-defence hypothesis, which invokes the

protection of young from infanticide as an explana-

tion of the badger's socio-spatial organization, is

one of the few theories that accommodates di�er-

ences between the sexes. The hypothesis remains

untested for badgers, but Wol� (1993, 1997) states

that it is likely to apply to many carnivores with

altricial non-mobile young that are reared in a bur-

row. Competition for reproductive opportunities

amongst females has been well documented in bad-

gers (Woodro�e & Macdonald 1995) and infanticide

is a likely contributor to the high pre-emergence cub

mortality (Kruuk 1989; LuÈ ps & Roper 1990). The

defence of young could occur through the defence

of a sett and may also be related to the maintenance

of a territory to provide exclusive access to food and

deter potentially infanticidal intruders (Wol� 1993).

The importance of cub defence is consistent with the

reported di�erences in the use of hinterland versus

boundary latrines between the sexes and between

seasons (Roper et al. 1993; Stewart 1997). All

females that were observed to disperse into vacated

habitat in the present study were old cubs or young

adults, and none showed signs of having lactated on

an earlier occasion (Tuyttens et al., 2000).

The most intriguing ®nding of this study is that

the ranges of social groups furthest away from the

removal groups increased most in size following the

BRO. It is di�cult to invoke a mechanism that may

have resulted in these groups being a�ected more by

the BRO than those immediately adjacent. None of

the functional hypotheses to explain badger's socio-

spatial organization discussed in this paper, are

entirely consistent with the observations. It is, how-

ever, interesting to note that these groups were

located in that part of the study site where there was

least woodland. Woodland is important to badgers

for the supply of food when the availability of earth-

worms on pasture, and of edible crops on arable

land is low. Woodland also o�ers shelter, protection

and suitable conditions for setts. It is possible, there-

fore, that badgers from these groups changed the

con®guration of their ranges to incorporate more

woodland when the opportunity arose.

IMPLICATIONS FOR THE CONTROL OF M.

BOVIS

The rate at which animals acquire a directly trans-

mitted infection depends on the rate of encounters

between susceptible and infectious animals (CR) and

on the probability that the infection is transmitted

when contact occurs (PI). The e�ectiveness of dis-

ease control by population reduction depends on

how both components change with population den-

sity. The relationships between host density and CR,

and between host density and PI may be susceptible

to socio-spatial perturbations induced by control

strategies (Tuyttens & Macdonald 1998). Tuyttens

et al. 2000 discuss the e�ect of disturbances of the

behaviour, age/sex structure, and the nutritional and

reproductive status of badgers caused by a BRO on

the relationship between badger density and PI.

Here, we concentrate on the relationship between

density and CR.

The disruption of spatial organization, increased

sett-latrine distances, enlargement of social group

ranges and increased range overlap revealed by our

825F. Tuyttens

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bait-marking study, suggest that reducing the den-

sity of badger populations is likely to result in less

than proportional reductions in between group CR.

The spatial scale of such disruption is not known

and presumably depends on the scale of the removal

operation. The present study suggests, however, that

the demographic and epidemiological consequences

of BROs may extend spatially far wider than pre-

viously thought. Although the perturbation e�ect

caused by the culling operation studied by Cheese-

man et al. (1993) was restricted to the removal

groups only, it lasted for several years. In contrast,

the spatial disturbance caused by the BRO in North

Nibley seemed largely (but not totally) limited to the

®rst year post-BRO. These di�erences in the spatial

and temporal extent of the perturbation caused by

the BROs at Woodchester Park and at North Nibley

may be related to the fact that at the former badger

social groups were completely removed, whereas at

North Nibley a small number of animals were

known to have survived. The consequences of BROs

may also vary according to characteristics of the

surrounding badger population (e.g. density, social

stability).

Mark±recapture (Tuyttens et al. 2000) and radio-

telemetry results have con®rmed this increase of

extra-group movements post-BRO. Several compu-

ter models have indicated that such perturbations

have the potential to neutralize or counteract the

e�ect of disease control strategies (White & Harris

1995; Swinton et al. 1997). Radio-tracking revealed,

however, that the potential for increased inter-group

did not apply to the entire badger population (as

may have been wrongly suggested by bait-marking).

Not all members of a social group utilize the entire

group range as determined from bait-marking. In

fact, the home range of only 37% (11/30) of adult

badgers in North Nibley included focal setts from at

least two di�erent social groups during at least one

radio-tracking period after the BRO.

Despite the observed socio-spatial perturbation,

the prevalence of TB in the North Nibley badger

population was substantially reduced by the BRO

and remained at very low levels until the end of

1997. One explanation is that the type of socio-spa-

tial perturbation caused by BROs does not facilitate

disease transmission. This interpretation, however,

disagrees not only with our current (albeit patchy)

understanding about the route and mode of disease

transmission among badgers, but also with the ®nd-

ing that movements between social groups of bad-

gers is strongly related with the TB incidence the

following year (Rogers et al. 1998). We therefore

propose as an alternative hypothesis, that the epide-

miological consequences of perturbation may not

have been revealed in the present study because

there was no evidence that any infectious badgers

survived the culling operations or moved into the

study area afterwards. However, there are consider-

able practical problems involved in the implementa-

tion of a BRO (Tuyttens et al., in press) and it is

not known to what extent the apparent success

reported here is representative of other such opera-

tions. Consequently, the increased potential for

direct and indirect contacts between badgers of dif-

ferent social groups following population reductions

may still have contributed to the failure of BROs to

halt the rising incidence of TB in British cattle.

Although the prevalence of TB in the Nibley bad-

ger population was seemingly reduced to negligible

levels by the BRO, further infections in cattle were

reported at the index farm and an adjacent farm in

the subsequent 3 years. This is, however, consistent

with several explanations including a source other

than the resident badgers, persistence of M. bovis

contamination in the local environment or failure to

detect the presence of infection in the badger popu-

lation due to incomplete trapping success or incor-

rect diagnosis of TB-status.

To conclude, the BRO at North Nibley caused

perturbation of the spatial organization of the bad-

ger population. Although the nature of the observed

perturbation was of the type that would be expected

to enhance disease transmission between social

groups, its impact on the e�ectiveness of disease

control strategies based on badger culling remains

unclear.

Acknowledgements

We are grateful to P. Mallinson, L. Rogers, P. Spy-

vee, D. Handoll, J. Howard, L. Barron, M. Wal-

dram and the many volunteers who have helped

with ®eldwork. We thank A. Roddam, P. Johnson

and S. Langton for help with statistical analyses,

VLA for testing the TB-status of the badgers that

we trapped, and the landowners in both study areas

for allowing us access to their land. Thanks also to

F. Matthews, H. Kruuk, P. Stewart and T. Roper,

and two anonymous referees for comments on ear-

lier drafts. The badger studies at Woodchester Park

and North Nibley are funded by MAFF. CAD

thanks the Wellcome Trust for support.

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Ecology, 69,

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