Directory UMM :Data Elmu:jurnal:A:Applied Animal Behaviour Science:Vol66.Issue4.2000:
Applied Animal Behaviour Science 66 Ž2000. 323–333
www.elsevier.comrlocaterapplanim
Cereal aversion in behaviourally resistant house
mice in Birmingham, UK
R.E. Humphries
a,1
, R.M. Sibly
a,)
, A.P. Meehan
b
a
Department of Biochemistry and Physiology, School of Animal and Microbial Sciences,
UniÕersity of Reading, P.O. Box 228, Whiteknights, Reading RG6 6AJ, UK
b
Research and DeÕelopment DiÕision, Rentokil Initial, Felcourt, East Grinstead, West Sussex RH19 2JY, UK
Accepted 26 August 1999
Abstract
In 1986, house mice in a small defined area of inner Birmingham were reported as not taking a
variety of rodenticides from bait containers, a phenomenon labelled ‘behavioural resistance’. This
study investigated behavioural resistance by comparing the food preferences of West Midlands
behaviourally resistant ŽWMBR. mice with those of normal ŽBC. mice. Nine bait boxes each
containing one of nine different foods Žcheese, chicken, tuna fish, peanut butter, canary seed, Cat
stars, wheat, PCD ŽMOD. pellets and Non-tox. were introduced to 12 WMBR and seven BC sites
ŽExperiment 1.. The experiment was repeated in the laboratory with six pens of WMBR and six of
BC mice ŽExperiment 2., and to investigate whether the preferences had a genetic basis the
offspring were similarly assayed ŽExperiment 3.. In each experiment the consumption of each
food was measured over 7 days and the droppings around the bait boxes were counted to assess
mouse activity. Food neophobia was noted in some populations of BC mice. Tested in the wild
and in the laboratory WMBR mice showed an aversion to foods containing cereals, as did their
offspring. These results, with other lines of evidence, strongly suggest that cereal aversion in
WMBR mice has a physiologicalrgenetic basis. Since cereal aversion allows WMBR mice to
survive cereal-based rodenticidal baits, we conclude that WMBR mice have genetically based
behaviours that allow them to survive poisoning regimes that kill other strains. q 2000 Elsevier
Science B.V. All rights reserved.
Keywords: House mouse; Food preferences; Neophobia; Behavioural resistance; Bait avoidance
)
Corresponding author. Tel.: q44-118-931-8461; fax: q44-118-931-0180; e-mail: r.m.sibly@reading.ac.uk
Now at: Faculty of Veterinary Science, University of Liverpool, Veterinary Teaching Hospital, Leahurst,
Neston, CH64 7TE, UK.
1
0168-1591r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved.
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R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
1. Introduction
In 1986, pest control operatives reported that house mice Ž Mus domesticus. in
localised inner-city areas of London and Birmingham in the UK had stopped taking a
variety of rodenticide baits from bait containers ŽHumphries et al., 1992.. Bait avoidance
was identified in the field wherever house mice continually avoided taking both acute
rodenticides Žrapid mortality, single-dose poisons, such as Alphachloralose. and chronic
rodenticides Ždelayed mortality, multiple-dose poisons, such as Bromadiolone.. The
continued existence of the mice was established from fresh droppings, catches on
sticky-boards, damage to goods and structures, the presence of tracks and active
burrows, andror sightings of live and dead mice. This phenomenon was labelled
‘behavioural resistance’, although there was initially no evidence that the behaviour was
inherited.
Throughout initial attempts to catch West Midlands behaviourally resistant ŽWMBR.
mice for the experiments reported here, no mice were captured in live-capture traps
baited with cereals ŽHumphries et al., 1992., which at the time was surprising since
house mice generally prefer cereals to non-cereal foods ŽSouthern, 1954; Rowe et al.,
1974.. In urban environments however, mice can obtain much of their food from
garbage ŽSchein and Orgain, 1953; personal observation., and some trapping success
was achieved when traps were baited with either tuna fish or chicken ŽHumphries et al.,
1992, 1996..
Here, we investigate the food preferences and aversions of WMBR mice in the field
ŽExperiment 1. and in the laboratory ŽExperiment 2. using a ‘cafeteria’ experimental
design in which nine foods were presented simultaneously. ‘Non-tox’ Ža cerealroil mix.
was included as one of the test foods because it had been extensively used as a bait base
by Rentokil throughout Birmingham city centre for 9 years prior to the experiment. In
Experiment 3, the offspring of the wild-caught mice were assayed to test whether the
WMBR food aversions are genetic or learnt. To provide a comparison with normal mice,
seven nearby populations ŽBC mice. were investigated at sites where cereal-based baits
were readily taken. Note was taken of any initial aversions to novel foods Žneophobias.
since these are of special interest in rodent control.
2. Materials and methods
2.1. Experiment 1
Twelve WMBR and seven BC study sites showing signs of recent mouse activity
were selected in November 1990. The WMBR sites had been reported by pest control
operatives as sites at which mice had stopped taking rodenticide baits from bait
containers, and comprised shops, restaurants, banks or offices which are 0.02–0.8 km
apart in Birmingham city centre. The BC sites were chosen as containing representative
mouse populations at convenient sites reasonably close to Birmingham, these were farms
2–28 km apart in Berkshire. Any existing bait boxes and other containers with
R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
325
rodenticides were removed, disposable latex gloves being worn whenever food or
droppings were handled. A 5 = 1 m area adjacent to a wall containing droppings but not
food sources was selected at each site. On the first day of the experiment Žday 0.
droppings were removed from these areas and nine cardboard mouse bait boxes
Ž10 = 4 = 4 cm. were placed against the 5-m length of wall at intervals of 50 cm. Each
bait box contained 4 g of one of the first nine foods listed in Table 1. All foods were
crushed, chopped up or minced in a food processor into pieces less than 0.3 g to
minimise hoarding. Foods removed from the boxes in the previous 24 h were recorded
on days 1, 2, and 7. Evaporation was allowed for by recording the weight losses from
boxes to which mice could not gain access. Each container was topped up daily with
fresh food so that 4 g of each food was available to the mice, and the number of
droppings in the experimental areas was counted. In one of the BC sites takes on some
days were near maximal so that food preferences could not be established, and this site
was therefore not included in the analysis. Food consumption and dropping counts were
comparable at the remaining WMBR and BC sites.
2.2. Experiments 2 and 3
Six male and six female WMBR mice were live-trapped from eight shops, restaurants
and offices in Birmingham city centre, and the same numbers of BC mice were
live-trapped from six farms in Berkshire. The substantial problems encountered in
trapping and maintaining the WMBR mice are described by Humphries et al. Ž1992;
1996.. No site contributed more than three mice, and if two mice came from the same
site they were kept as a pair. All animals weighed over 14 g, were sexually mature but
not pregnant, and had hind-foot lengths of at least 16 mm on capture, and WMBR and
BC mice did not differ in body weight. The mice were kept in large cages Ž55 = 39 = 19
cm. or pens Žas below. in the period between trapping and the start of the experiments
Žmean time s 14 days, no difference between WMBR and BC pairs of mice. and fed on
tuna fish and PCD ŽMOD. pellets ŽTable 1.. Pens were made of sheet aluminium
Ž185 = 185 = 90 cm. and contained two wooden mouse boxes Ž30 = 24 = 12 cm. filled
with paper wool as bedding ŽFig. 1.. At the front of the pens there were two metal food
trays Ž26 = 16 = 2.5 cm., each placed on a piece of wood in order to prevent sawdust
being scattered into the trays and to enable any spillage of food to be easily collected
and recorded. Vitamin K1 enriched water from a standard chick drinker Žmade of glass
and plastic. was available ad libitum. Three pieces of white Melamine-coated chipboard
Žeach measuring 180 = 30 = 1.75 cm. were pushed firmly against the back and two side
walls of the pens. All the pens were floored with approximately 5 cm of sawdust firmly
patted down in order that any burying or hoarding of food in the sawdust could be easily
detected.
In Experiment 2, a male and a female were placed in each of 12 pens on day 0,
WMBR pens being paired with BC pens on the basis of date of capture. The pens may
seem very large, but we had only limited success in keeping WMBR mice in smaller
enclosures. To control the food eaten in the week prior to testing for preferences, the
mice were fed 20 g of a standard mouse diet, EPA ŽTable 1. daily. The EPA was ground
326
Food
Variety
% Crude
protein
% Fat
or oil
%
Moisture
%
Carbohydrate
Energy value
Žkcalr100 g.
% Cereal
Žcornrgrain.
Food type
Cheese
Chicken
Tuna fish
Peanut butter
Canary seed
Cat stars
Wheat
PCD MOD
Non-tox
EPA
English cheddar
boneless breast, oven-cooked
tinned, in vegetable oil
crunchy
Phalaris canariensis
tuna-flavoured, dried cat food
whole grain
pelleted rodent maintenance diet
cerealroil bait base used by Rentokil
rodent maintenance diet
26.0
21.0
28.0
24.0
13.7
30.0
10.5
19.3
4.1
y
33.5
16.0
17.5
52.0
3.5
8.5
2.0
2.8
55.8
low oil
37.0
63.5
54.6
1.1
14.3
10.0
13.5
trace
6.5
low
trace
0
1.0
13.0
58.5
38.0
72.4
60.9
30.3
high
406
142
289
613
241
350
329
361
y
y
0
0
0
0
100
high
100
72.5
41
95
dairy product
meat
fish
ground nuts
cereal
cereal
cereal
cereal
fats and cereal
cereal
R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
Table 1
The nutritional composition and cereal content of the 10 experimental foods, of which the first nine were presented in bait boxes. After McCance and Widdowson
Ž1991., with additional information supplied by food manufacturers. y indicates information not available
R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
327
Fig. 1. Experimental design showing layout of bait boxes in Experiments 2 and 3. Each box contained 4 g of
one of the first nine foods in Table 1.
down to reduce hoarding, and placed in the two metal food trays at the front of the pens
ŽFig. 1.. The 24-h consumption was recorded on days 1, 2, 3, 6 and 7. At the end of the
seventh day all droppings were removed from the back half of the pens and nine bait
boxes containing foods were introduced into them as in Experiment 1, except that the
between-box spacing was reduced and the side walls were used as well as the back wall
ŽFig. 1.. Food order in the bait boxes was randomised but the same order was used for
paired WMBR and BC pens. To allow for seasonal variations in day length the boxes
were introduced 1 h before sunset. The bait boxes were provisioned daily at 0900–1000
h and food consumption was recorded and droppings counted as in Experiment 1. After
14 days, the mice were caught and weighed, and any hoarded food was weighed.
Experiment 3 followed the experimental protocol of Experiment 2 using mature
offspring from the first and second litters of the mice used in Experiment 2. The mice
used in Experiment 2 were maintained in the pens on a diet consisting of all 10 foods.
The offspring were born in the pens and kept in them until separated from their parents
at weaning Ž20–21 days old. and matured in large cages Ž55 = 39 = 19 cm. where they
continued to be fed on the 10-food diet until they were tested. Water enriched with
vitamin K1 from a standard drinker was available ad libitum. The mice used in
Experiment 3 were 5–7 months old when tested, females were not pregnant, and there
was no significant difference in body weight between the WMBR and BC mice. One
pen of BC mice did not eat from the bait boxes on any study day, and it and the
associated WMBR pen were therefore not included in the analysis. All statistical testing
used the Mann–Whitney test with n1 s 12 and n 2 s 6 in Experiment 1, n1 s n 2 s 6 in
Experiment 2 and n1 s n 2 s 5 in Experiment 3, except where otherwise stated.
328
R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
3. Results
3.1. EPA consumption before the introduction of the bait boxes in Experiments 2 and 3
It was not possible to assess natural feeding in Experiment 1 before the introduction
of the bait boxes. However, in the laboratory, in Experiment 2, only the cereal-based
diet EPA was available in the week prior to bait box introduction, and during this time
the wild-caught WMBR mice took consistently less EPA than BC mice ŽFig. 2A.. BC
mice ate less on day 1 than on day 2 ŽWilcoxon test, W s 21.0, n s 6, p s 0.036. but
thereafter consistent amounts day to day. The pattern of EPA consumption by the
offspring of the wild-caught mice in Experiment 3, was similar to that of their parents
ŽFig. 2B..
3.2. Food preferences and aÕersions
Food consumption on days 1, 2 and 7 after bait box introduction is shown for each
experiment in Fig. 3. When the nine foods were introduced to wild mice in their natural
environments in Experiment 1, WMBR mice took consistently more cheese, chicken and
tuna fish than BC mice, and the amounts taken were close to the maximum available, 4
g ŽFig. 3, top row.. Only small amounts of the other foods were taken by WMBR mice
and Non-tox was completely avoided in 11 of the 12 WMBR sites, not even tooth marks
being observed. By contrast, BC mice showed no clear preferences.
A similar pattern was seen when the nine foods were introduced to wild mice in the
laboratory in Experiment 2 ŽFig. 3, middle row.. The WMBR mice again took
consistently more cheese, chicken and tuna fish, and Non-tox was completely avoided
by four of the six pairs of WMBR mice. By contrast, BC mice took relatively small
amounts of the nine foods in bait boxes on day 1, but EPA was taken in large amounts.
By day 7, however, BC mice were taking some of all of the foods.
The pattern of food consumption of the offspring ŽFig. 3, bottom row. developed so
that by day 7 they were similar to those of their parents, except that WMBR offspring
ate more PCD and Non-tox than their parents. WMBR offspring showed no clear
preference for any particular food type on day 1, though they avoided canary seed and
wheat.
The total daily consumption of all foods before and after bait box introduction is
shown in Fig. 2. When the bait boxes were introduced total food consumption by wild
WMBR mice increased dramatically ŽWilcoxon test comparing consumption on the days
before and after bait box introduction, W s 21.0, n s 6, p s 0.036., and thereafter they
took significantly more food than BC mice on most days. Their offspring showed a
similar pattern, though less marked ŽFig. 2B.. There was no significant difference in
Fig. 2. Total food consumption Žgrpair of mice. before and after bait box introduction by ŽA. wild WMBR
and BC mice in the laboratory ŽExperiment 2., and ŽB. their offspring ŽExperiment 3.. Stars indicate
Mann–Whitney test p-values for differences between WMBR and BC mice: U p- 0.05, UU p- 0.01. Bars
indicate standard errors of the means.
R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
329
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R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
Fig. 3. Consumption of the foods presented in the preference tests. Within each panel the amount taken by
WMBR mice is shown on the left Ždark bars., and that by BC mice on the right Žlight bars.. The panels in the
top row refer to Experiment 1, those in the middle and bottom rows to Experiments 2 and 3. Columns of
panels refer to days 1, 2 and 7. Units are grsite in Experiment 1, grpen in Experiments 2 and 3. Stars indicate
Mann–Whitney test p-values for differences between WMBR and BC sites: U p- 0.05, UU p- 0.01, UUU p0.001. Bars indicate standard errors of the means.
total consumption over the 14 days of the experiment between pairs of WMBR mice and
BC mice in either experiment. The amount of food found hoarded by WMBR and BC
mice at the end of Experiments 2 and 3 was small, averaging 1.0 grpair of mice.
4. Discussion
4.1. Food preferences and aÕersions
Strong and persistent preferences of WMBR mice for cheese, chicken and tuna fish
and aversions to cereals Žcanary seed and wheat. and cereal-based foods ŽCat stars, PCD
and Non-tox. were evident in the preference tests in all three experiments ŽFig. 3., and
cereal aversion was seen in the pre-bait box week of Experiments 2 and 3, when, offered
only the cereal-based food EPA, WMBR mice ate substantially less than BC mice ŽFig.
2. and lost weight. Although there were minor nutritional differences between the foods,
the only consistent feature of those to which WMBR mice were averse was that they
contained cereal ŽTable 1.. Cereals and cereal-based foods were not completely avoided,
R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
331
but when they were taken the cereal content of the diet was low. Thus, for instance,
some PCD and Non-tox were taken by WMBR mice in Experiment 3 ŽFig. 3., but the
cereal content of these foods is lower than that of the other cereal-based foods. The
WMBR mice food aversions are in marked contrast to the usual preferences of wild and
laboratory house mice, i.e., cereals, shown here by the BC mice ŽSouthern, 1954; Rowe
et al., 1974; Meehan, 1984..
When the bait boxes with foods were introduced in Experiments 2 and 3, the food
consumption by WMBR mice increased markedly ŽFig. 2.. Presumably, when they were
offered foods they liked they took large amounts to compensate for the earlier period
when they had eaten less. This compensation was such that over the 14 days of the
experiments WMBR and BC mice did not differ in total consumption.
4.2. Genetics and ontogeny of cereal aÕersion
The similarity between parents and offspring in cereal aversion in Experiments 2 and
3 ŽFig. 3. raises the question as to whether cereal aversion in WMBR mice has a genetic
basis or is learnt. Foetalrpre-natal learning is established in rodents ŽSmotherman, 1982;
Hepper, 1988, 1991., as is learning between birth and weaning ŽGalef and Henderson,
1972; Galef and Sherry, 1973; Bronstein and Crockett, 1976; Duveau and Godinot,
1988.. However, following on from the experiments reported here Maczka Ž1993. ŽMSc
thesis. and Rout Ž1994. ŽMSc thesis. showed that the cereal aversion of our WMBR
mice persisted through several generations. In an undergraduate project, Taylor et al.
Ž1996. investigated the physiological basis of the cereal aversion by comparing caecum
mass and duodenal a-amylase activity in WMBR and BC mice. The results suggested
that low a-amylase activity in WMBR mice caused ingested carbohydrate to bypass
normal digestion and reach the caecum, causing caecal enlargement. Associated symptoms could cause WMBR mice to select a low-carbohydrate diet, and hence avoid
cereals and other carbohydrate-rich foods. The genetics of cereal aversion have been
investigated by crossing WMBR mice with a laboratory strain of mice, and then
backcrossing the heterozygotes with the parental strains ŽHolmes, C., 1995, undergraduate project.. The results suggested a multi-locus basis for cereal aversion in WMBR
mice. Taking together these various lines of evidence, we conclude that cereal aversion
in WMBR mice does have a physiologicalrgenetic basis. Since the trait allows WMBR
mice to survive cereal-based rodenticidal baits, it seems that WMBR mice are truly
‘behaviourally resistant’, possessing genetically based behaviours that allow them to
survive poisoning regimes that kill other strains.
There was no suggestion that bait boxes were avoided by WMBR mice since they
readily took large amounts of food from bait boxes if they contained foods that they
liked. However, it is interesting that in Experiment 1 WMBR mice completely avoided
the bait base Non-tox in 11 of 12 sites. Since WMBR mice took some Non-tox in
Experiment 3 ŽFig. 3. they were not innately completely averse to it, so the mice in
Experiment 1 presumably learnt to avoid it by associating it with the Non-tox-based
rodenticides Betalard and Bromard then widely used in WMBR sites. Implications of
these results for rodent control are discussed by Humphries et al. Ž1996..
332
R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
Fig. 4. Total food consumption Žgrsite. from the nine bait boxes on study days at WMBR and BC sites in
Experiment 1. Bars indicate standard errors of the means.
4.3. Food neophobia
House mice are generally regarded as inquisitive animals showing little neophobia,
i.e., initial avoidance of novel stimuli in familiar environments ŽSouthern, 1954; Wolfe,
1969; Meehan, 1984. although there are some reports of neophobia in both laboratory
and wild mice ŽMisslin, 1982; Misslin and Ropartz, 1981; Kronenberger and Medioni,
´
1985; Brigham and Sibly, in press.. WMBR mice took large amounts of food from the
bait boxes from day 1 in all three experiments, and so, by definition, showed no
evidence of neophobia. There was however, between-site variation in the initial responses to the bait boxes of mice in the six BC sites in Experiment 1. Whereas the mice
in three BC sites took food from the bait boxes from day 1, mice in the other three BC
sites took nothing from bait boxes on day 1, though they did feed from them later, and
the average daily consumption from BC bait boxes increased with time ŽWilcoxon test
comparing days 1 and 3, W s 21.0, n s 6, p s 0.036, Fig. 4.. Similar results were
obtained in Experiments 2 and 3. The average daily consumption of EPA by BC mice
increased between days 1 and 2, before the introduction of the bait boxes ŽFig. 2., and
on days 1 and 2 after bait box introduction BC mice continued eating EPA rather than
the foods in the bait boxes ŽFig. 3.. Again, there was variation between pens in the BC
mice’s initial responses. In Experiment 2, two pairs of BC mice took large amounts of
food from the bait boxes on day 1 Ž7.5 and 9.6 g., but three pairs took no food at all Žfor
further details of all three experiments, see Humphries, 1994.. In all replicates dropping
counts showed activity around the bait boxes from day 1, and since some of the foods
have a strong smell, it is likely that the mice were aware of the boxes. We conclude that
some but not all populations of BC mice were neophobic to new foods.
Acknowledgements
We would like to express our sincere thanks to all the Rentokil service technicians,
shop assistants, restaurant staff and farmers that we have met for helping us capture
these somewhat elusive mice. Many thanks are due to Dr. Dave Cowan, Dr. Pete Smith,
Professor Robert Smith and James Gallagher for their helpful advice during this project.
R.E.H. was supported by a CASE studentship funded by the Science and Engineering
Research Council and Rentokil.
R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
333
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www.elsevier.comrlocaterapplanim
Cereal aversion in behaviourally resistant house
mice in Birmingham, UK
R.E. Humphries
a,1
, R.M. Sibly
a,)
, A.P. Meehan
b
a
Department of Biochemistry and Physiology, School of Animal and Microbial Sciences,
UniÕersity of Reading, P.O. Box 228, Whiteknights, Reading RG6 6AJ, UK
b
Research and DeÕelopment DiÕision, Rentokil Initial, Felcourt, East Grinstead, West Sussex RH19 2JY, UK
Accepted 26 August 1999
Abstract
In 1986, house mice in a small defined area of inner Birmingham were reported as not taking a
variety of rodenticides from bait containers, a phenomenon labelled ‘behavioural resistance’. This
study investigated behavioural resistance by comparing the food preferences of West Midlands
behaviourally resistant ŽWMBR. mice with those of normal ŽBC. mice. Nine bait boxes each
containing one of nine different foods Žcheese, chicken, tuna fish, peanut butter, canary seed, Cat
stars, wheat, PCD ŽMOD. pellets and Non-tox. were introduced to 12 WMBR and seven BC sites
ŽExperiment 1.. The experiment was repeated in the laboratory with six pens of WMBR and six of
BC mice ŽExperiment 2., and to investigate whether the preferences had a genetic basis the
offspring were similarly assayed ŽExperiment 3.. In each experiment the consumption of each
food was measured over 7 days and the droppings around the bait boxes were counted to assess
mouse activity. Food neophobia was noted in some populations of BC mice. Tested in the wild
and in the laboratory WMBR mice showed an aversion to foods containing cereals, as did their
offspring. These results, with other lines of evidence, strongly suggest that cereal aversion in
WMBR mice has a physiologicalrgenetic basis. Since cereal aversion allows WMBR mice to
survive cereal-based rodenticidal baits, we conclude that WMBR mice have genetically based
behaviours that allow them to survive poisoning regimes that kill other strains. q 2000 Elsevier
Science B.V. All rights reserved.
Keywords: House mouse; Food preferences; Neophobia; Behavioural resistance; Bait avoidance
)
Corresponding author. Tel.: q44-118-931-8461; fax: q44-118-931-0180; e-mail: r.m.sibly@reading.ac.uk
Now at: Faculty of Veterinary Science, University of Liverpool, Veterinary Teaching Hospital, Leahurst,
Neston, CH64 7TE, UK.
1
0168-1591r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 8 - 1 5 9 1 Ž 9 9 . 0 0 0 9 6 - 9
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R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
1. Introduction
In 1986, pest control operatives reported that house mice Ž Mus domesticus. in
localised inner-city areas of London and Birmingham in the UK had stopped taking a
variety of rodenticide baits from bait containers ŽHumphries et al., 1992.. Bait avoidance
was identified in the field wherever house mice continually avoided taking both acute
rodenticides Žrapid mortality, single-dose poisons, such as Alphachloralose. and chronic
rodenticides Ždelayed mortality, multiple-dose poisons, such as Bromadiolone.. The
continued existence of the mice was established from fresh droppings, catches on
sticky-boards, damage to goods and structures, the presence of tracks and active
burrows, andror sightings of live and dead mice. This phenomenon was labelled
‘behavioural resistance’, although there was initially no evidence that the behaviour was
inherited.
Throughout initial attempts to catch West Midlands behaviourally resistant ŽWMBR.
mice for the experiments reported here, no mice were captured in live-capture traps
baited with cereals ŽHumphries et al., 1992., which at the time was surprising since
house mice generally prefer cereals to non-cereal foods ŽSouthern, 1954; Rowe et al.,
1974.. In urban environments however, mice can obtain much of their food from
garbage ŽSchein and Orgain, 1953; personal observation., and some trapping success
was achieved when traps were baited with either tuna fish or chicken ŽHumphries et al.,
1992, 1996..
Here, we investigate the food preferences and aversions of WMBR mice in the field
ŽExperiment 1. and in the laboratory ŽExperiment 2. using a ‘cafeteria’ experimental
design in which nine foods were presented simultaneously. ‘Non-tox’ Ža cerealroil mix.
was included as one of the test foods because it had been extensively used as a bait base
by Rentokil throughout Birmingham city centre for 9 years prior to the experiment. In
Experiment 3, the offspring of the wild-caught mice were assayed to test whether the
WMBR food aversions are genetic or learnt. To provide a comparison with normal mice,
seven nearby populations ŽBC mice. were investigated at sites where cereal-based baits
were readily taken. Note was taken of any initial aversions to novel foods Žneophobias.
since these are of special interest in rodent control.
2. Materials and methods
2.1. Experiment 1
Twelve WMBR and seven BC study sites showing signs of recent mouse activity
were selected in November 1990. The WMBR sites had been reported by pest control
operatives as sites at which mice had stopped taking rodenticide baits from bait
containers, and comprised shops, restaurants, banks or offices which are 0.02–0.8 km
apart in Birmingham city centre. The BC sites were chosen as containing representative
mouse populations at convenient sites reasonably close to Birmingham, these were farms
2–28 km apart in Berkshire. Any existing bait boxes and other containers with
R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
325
rodenticides were removed, disposable latex gloves being worn whenever food or
droppings were handled. A 5 = 1 m area adjacent to a wall containing droppings but not
food sources was selected at each site. On the first day of the experiment Žday 0.
droppings were removed from these areas and nine cardboard mouse bait boxes
Ž10 = 4 = 4 cm. were placed against the 5-m length of wall at intervals of 50 cm. Each
bait box contained 4 g of one of the first nine foods listed in Table 1. All foods were
crushed, chopped up or minced in a food processor into pieces less than 0.3 g to
minimise hoarding. Foods removed from the boxes in the previous 24 h were recorded
on days 1, 2, and 7. Evaporation was allowed for by recording the weight losses from
boxes to which mice could not gain access. Each container was topped up daily with
fresh food so that 4 g of each food was available to the mice, and the number of
droppings in the experimental areas was counted. In one of the BC sites takes on some
days were near maximal so that food preferences could not be established, and this site
was therefore not included in the analysis. Food consumption and dropping counts were
comparable at the remaining WMBR and BC sites.
2.2. Experiments 2 and 3
Six male and six female WMBR mice were live-trapped from eight shops, restaurants
and offices in Birmingham city centre, and the same numbers of BC mice were
live-trapped from six farms in Berkshire. The substantial problems encountered in
trapping and maintaining the WMBR mice are described by Humphries et al. Ž1992;
1996.. No site contributed more than three mice, and if two mice came from the same
site they were kept as a pair. All animals weighed over 14 g, were sexually mature but
not pregnant, and had hind-foot lengths of at least 16 mm on capture, and WMBR and
BC mice did not differ in body weight. The mice were kept in large cages Ž55 = 39 = 19
cm. or pens Žas below. in the period between trapping and the start of the experiments
Žmean time s 14 days, no difference between WMBR and BC pairs of mice. and fed on
tuna fish and PCD ŽMOD. pellets ŽTable 1.. Pens were made of sheet aluminium
Ž185 = 185 = 90 cm. and contained two wooden mouse boxes Ž30 = 24 = 12 cm. filled
with paper wool as bedding ŽFig. 1.. At the front of the pens there were two metal food
trays Ž26 = 16 = 2.5 cm., each placed on a piece of wood in order to prevent sawdust
being scattered into the trays and to enable any spillage of food to be easily collected
and recorded. Vitamin K1 enriched water from a standard chick drinker Žmade of glass
and plastic. was available ad libitum. Three pieces of white Melamine-coated chipboard
Žeach measuring 180 = 30 = 1.75 cm. were pushed firmly against the back and two side
walls of the pens. All the pens were floored with approximately 5 cm of sawdust firmly
patted down in order that any burying or hoarding of food in the sawdust could be easily
detected.
In Experiment 2, a male and a female were placed in each of 12 pens on day 0,
WMBR pens being paired with BC pens on the basis of date of capture. The pens may
seem very large, but we had only limited success in keeping WMBR mice in smaller
enclosures. To control the food eaten in the week prior to testing for preferences, the
mice were fed 20 g of a standard mouse diet, EPA ŽTable 1. daily. The EPA was ground
326
Food
Variety
% Crude
protein
% Fat
or oil
%
Moisture
%
Carbohydrate
Energy value
Žkcalr100 g.
% Cereal
Žcornrgrain.
Food type
Cheese
Chicken
Tuna fish
Peanut butter
Canary seed
Cat stars
Wheat
PCD MOD
Non-tox
EPA
English cheddar
boneless breast, oven-cooked
tinned, in vegetable oil
crunchy
Phalaris canariensis
tuna-flavoured, dried cat food
whole grain
pelleted rodent maintenance diet
cerealroil bait base used by Rentokil
rodent maintenance diet
26.0
21.0
28.0
24.0
13.7
30.0
10.5
19.3
4.1
y
33.5
16.0
17.5
52.0
3.5
8.5
2.0
2.8
55.8
low oil
37.0
63.5
54.6
1.1
14.3
10.0
13.5
trace
6.5
low
trace
0
1.0
13.0
58.5
38.0
72.4
60.9
30.3
high
406
142
289
613
241
350
329
361
y
y
0
0
0
0
100
high
100
72.5
41
95
dairy product
meat
fish
ground nuts
cereal
cereal
cereal
cereal
fats and cereal
cereal
R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
Table 1
The nutritional composition and cereal content of the 10 experimental foods, of which the first nine were presented in bait boxes. After McCance and Widdowson
Ž1991., with additional information supplied by food manufacturers. y indicates information not available
R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
327
Fig. 1. Experimental design showing layout of bait boxes in Experiments 2 and 3. Each box contained 4 g of
one of the first nine foods in Table 1.
down to reduce hoarding, and placed in the two metal food trays at the front of the pens
ŽFig. 1.. The 24-h consumption was recorded on days 1, 2, 3, 6 and 7. At the end of the
seventh day all droppings were removed from the back half of the pens and nine bait
boxes containing foods were introduced into them as in Experiment 1, except that the
between-box spacing was reduced and the side walls were used as well as the back wall
ŽFig. 1.. Food order in the bait boxes was randomised but the same order was used for
paired WMBR and BC pens. To allow for seasonal variations in day length the boxes
were introduced 1 h before sunset. The bait boxes were provisioned daily at 0900–1000
h and food consumption was recorded and droppings counted as in Experiment 1. After
14 days, the mice were caught and weighed, and any hoarded food was weighed.
Experiment 3 followed the experimental protocol of Experiment 2 using mature
offspring from the first and second litters of the mice used in Experiment 2. The mice
used in Experiment 2 were maintained in the pens on a diet consisting of all 10 foods.
The offspring were born in the pens and kept in them until separated from their parents
at weaning Ž20–21 days old. and matured in large cages Ž55 = 39 = 19 cm. where they
continued to be fed on the 10-food diet until they were tested. Water enriched with
vitamin K1 from a standard drinker was available ad libitum. The mice used in
Experiment 3 were 5–7 months old when tested, females were not pregnant, and there
was no significant difference in body weight between the WMBR and BC mice. One
pen of BC mice did not eat from the bait boxes on any study day, and it and the
associated WMBR pen were therefore not included in the analysis. All statistical testing
used the Mann–Whitney test with n1 s 12 and n 2 s 6 in Experiment 1, n1 s n 2 s 6 in
Experiment 2 and n1 s n 2 s 5 in Experiment 3, except where otherwise stated.
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3. Results
3.1. EPA consumption before the introduction of the bait boxes in Experiments 2 and 3
It was not possible to assess natural feeding in Experiment 1 before the introduction
of the bait boxes. However, in the laboratory, in Experiment 2, only the cereal-based
diet EPA was available in the week prior to bait box introduction, and during this time
the wild-caught WMBR mice took consistently less EPA than BC mice ŽFig. 2A.. BC
mice ate less on day 1 than on day 2 ŽWilcoxon test, W s 21.0, n s 6, p s 0.036. but
thereafter consistent amounts day to day. The pattern of EPA consumption by the
offspring of the wild-caught mice in Experiment 3, was similar to that of their parents
ŽFig. 2B..
3.2. Food preferences and aÕersions
Food consumption on days 1, 2 and 7 after bait box introduction is shown for each
experiment in Fig. 3. When the nine foods were introduced to wild mice in their natural
environments in Experiment 1, WMBR mice took consistently more cheese, chicken and
tuna fish than BC mice, and the amounts taken were close to the maximum available, 4
g ŽFig. 3, top row.. Only small amounts of the other foods were taken by WMBR mice
and Non-tox was completely avoided in 11 of the 12 WMBR sites, not even tooth marks
being observed. By contrast, BC mice showed no clear preferences.
A similar pattern was seen when the nine foods were introduced to wild mice in the
laboratory in Experiment 2 ŽFig. 3, middle row.. The WMBR mice again took
consistently more cheese, chicken and tuna fish, and Non-tox was completely avoided
by four of the six pairs of WMBR mice. By contrast, BC mice took relatively small
amounts of the nine foods in bait boxes on day 1, but EPA was taken in large amounts.
By day 7, however, BC mice were taking some of all of the foods.
The pattern of food consumption of the offspring ŽFig. 3, bottom row. developed so
that by day 7 they were similar to those of their parents, except that WMBR offspring
ate more PCD and Non-tox than their parents. WMBR offspring showed no clear
preference for any particular food type on day 1, though they avoided canary seed and
wheat.
The total daily consumption of all foods before and after bait box introduction is
shown in Fig. 2. When the bait boxes were introduced total food consumption by wild
WMBR mice increased dramatically ŽWilcoxon test comparing consumption on the days
before and after bait box introduction, W s 21.0, n s 6, p s 0.036., and thereafter they
took significantly more food than BC mice on most days. Their offspring showed a
similar pattern, though less marked ŽFig. 2B.. There was no significant difference in
Fig. 2. Total food consumption Žgrpair of mice. before and after bait box introduction by ŽA. wild WMBR
and BC mice in the laboratory ŽExperiment 2., and ŽB. their offspring ŽExperiment 3.. Stars indicate
Mann–Whitney test p-values for differences between WMBR and BC mice: U p- 0.05, UU p- 0.01. Bars
indicate standard errors of the means.
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329
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R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
Fig. 3. Consumption of the foods presented in the preference tests. Within each panel the amount taken by
WMBR mice is shown on the left Ždark bars., and that by BC mice on the right Žlight bars.. The panels in the
top row refer to Experiment 1, those in the middle and bottom rows to Experiments 2 and 3. Columns of
panels refer to days 1, 2 and 7. Units are grsite in Experiment 1, grpen in Experiments 2 and 3. Stars indicate
Mann–Whitney test p-values for differences between WMBR and BC sites: U p- 0.05, UU p- 0.01, UUU p0.001. Bars indicate standard errors of the means.
total consumption over the 14 days of the experiment between pairs of WMBR mice and
BC mice in either experiment. The amount of food found hoarded by WMBR and BC
mice at the end of Experiments 2 and 3 was small, averaging 1.0 grpair of mice.
4. Discussion
4.1. Food preferences and aÕersions
Strong and persistent preferences of WMBR mice for cheese, chicken and tuna fish
and aversions to cereals Žcanary seed and wheat. and cereal-based foods ŽCat stars, PCD
and Non-tox. were evident in the preference tests in all three experiments ŽFig. 3., and
cereal aversion was seen in the pre-bait box week of Experiments 2 and 3, when, offered
only the cereal-based food EPA, WMBR mice ate substantially less than BC mice ŽFig.
2. and lost weight. Although there were minor nutritional differences between the foods,
the only consistent feature of those to which WMBR mice were averse was that they
contained cereal ŽTable 1.. Cereals and cereal-based foods were not completely avoided,
R.E. Humphries et al.r Applied Animal BehaÕiour Science 66 (2000) 323–333
331
but when they were taken the cereal content of the diet was low. Thus, for instance,
some PCD and Non-tox were taken by WMBR mice in Experiment 3 ŽFig. 3., but the
cereal content of these foods is lower than that of the other cereal-based foods. The
WMBR mice food aversions are in marked contrast to the usual preferences of wild and
laboratory house mice, i.e., cereals, shown here by the BC mice ŽSouthern, 1954; Rowe
et al., 1974; Meehan, 1984..
When the bait boxes with foods were introduced in Experiments 2 and 3, the food
consumption by WMBR mice increased markedly ŽFig. 2.. Presumably, when they were
offered foods they liked they took large amounts to compensate for the earlier period
when they had eaten less. This compensation was such that over the 14 days of the
experiments WMBR and BC mice did not differ in total consumption.
4.2. Genetics and ontogeny of cereal aÕersion
The similarity between parents and offspring in cereal aversion in Experiments 2 and
3 ŽFig. 3. raises the question as to whether cereal aversion in WMBR mice has a genetic
basis or is learnt. Foetalrpre-natal learning is established in rodents ŽSmotherman, 1982;
Hepper, 1988, 1991., as is learning between birth and weaning ŽGalef and Henderson,
1972; Galef and Sherry, 1973; Bronstein and Crockett, 1976; Duveau and Godinot,
1988.. However, following on from the experiments reported here Maczka Ž1993. ŽMSc
thesis. and Rout Ž1994. ŽMSc thesis. showed that the cereal aversion of our WMBR
mice persisted through several generations. In an undergraduate project, Taylor et al.
Ž1996. investigated the physiological basis of the cereal aversion by comparing caecum
mass and duodenal a-amylase activity in WMBR and BC mice. The results suggested
that low a-amylase activity in WMBR mice caused ingested carbohydrate to bypass
normal digestion and reach the caecum, causing caecal enlargement. Associated symptoms could cause WMBR mice to select a low-carbohydrate diet, and hence avoid
cereals and other carbohydrate-rich foods. The genetics of cereal aversion have been
investigated by crossing WMBR mice with a laboratory strain of mice, and then
backcrossing the heterozygotes with the parental strains ŽHolmes, C., 1995, undergraduate project.. The results suggested a multi-locus basis for cereal aversion in WMBR
mice. Taking together these various lines of evidence, we conclude that cereal aversion
in WMBR mice does have a physiologicalrgenetic basis. Since the trait allows WMBR
mice to survive cereal-based rodenticidal baits, it seems that WMBR mice are truly
‘behaviourally resistant’, possessing genetically based behaviours that allow them to
survive poisoning regimes that kill other strains.
There was no suggestion that bait boxes were avoided by WMBR mice since they
readily took large amounts of food from bait boxes if they contained foods that they
liked. However, it is interesting that in Experiment 1 WMBR mice completely avoided
the bait base Non-tox in 11 of 12 sites. Since WMBR mice took some Non-tox in
Experiment 3 ŽFig. 3. they were not innately completely averse to it, so the mice in
Experiment 1 presumably learnt to avoid it by associating it with the Non-tox-based
rodenticides Betalard and Bromard then widely used in WMBR sites. Implications of
these results for rodent control are discussed by Humphries et al. Ž1996..
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Fig. 4. Total food consumption Žgrsite. from the nine bait boxes on study days at WMBR and BC sites in
Experiment 1. Bars indicate standard errors of the means.
4.3. Food neophobia
House mice are generally regarded as inquisitive animals showing little neophobia,
i.e., initial avoidance of novel stimuli in familiar environments ŽSouthern, 1954; Wolfe,
1969; Meehan, 1984. although there are some reports of neophobia in both laboratory
and wild mice ŽMisslin, 1982; Misslin and Ropartz, 1981; Kronenberger and Medioni,
´
1985; Brigham and Sibly, in press.. WMBR mice took large amounts of food from the
bait boxes from day 1 in all three experiments, and so, by definition, showed no
evidence of neophobia. There was however, between-site variation in the initial responses to the bait boxes of mice in the six BC sites in Experiment 1. Whereas the mice
in three BC sites took food from the bait boxes from day 1, mice in the other three BC
sites took nothing from bait boxes on day 1, though they did feed from them later, and
the average daily consumption from BC bait boxes increased with time ŽWilcoxon test
comparing days 1 and 3, W s 21.0, n s 6, p s 0.036, Fig. 4.. Similar results were
obtained in Experiments 2 and 3. The average daily consumption of EPA by BC mice
increased between days 1 and 2, before the introduction of the bait boxes ŽFig. 2., and
on days 1 and 2 after bait box introduction BC mice continued eating EPA rather than
the foods in the bait boxes ŽFig. 3.. Again, there was variation between pens in the BC
mice’s initial responses. In Experiment 2, two pairs of BC mice took large amounts of
food from the bait boxes on day 1 Ž7.5 and 9.6 g., but three pairs took no food at all Žfor
further details of all three experiments, see Humphries, 1994.. In all replicates dropping
counts showed activity around the bait boxes from day 1, and since some of the foods
have a strong smell, it is likely that the mice were aware of the boxes. We conclude that
some but not all populations of BC mice were neophobic to new foods.
Acknowledgements
We would like to express our sincere thanks to all the Rentokil service technicians,
shop assistants, restaurant staff and farmers that we have met for helping us capture
these somewhat elusive mice. Many thanks are due to Dr. Dave Cowan, Dr. Pete Smith,
Professor Robert Smith and James Gallagher for their helpful advice during this project.
R.E.H. was supported by a CASE studentship funded by the Science and Engineering
Research Council and Rentokil.
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