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Maternal influences on food preferences in weanling mice
Behavioural Processes, 19 (1989) 155-166 Elsevier
155
MATERNAL INFLUENCES ON FOOD PREFERENCES IN WE.~NLING MICE M=u_s d0mesticu s PAOLA VALSECCHI, MARISA MAINARDI. ANDREA SGOIFO AND ANTONIO TATICCHI IstJtuto di Zoologia. Universit~ degli Studi di Parma, via delle Scienze 43100 Parma, Italy
( Accepted
26 May 1989 )
ABSTRACT Valsecchi. P.. Mainardi. M.. Ssoifo. A. a n d Taticchi. A. 1989. Matern al i n f l u e n c e s on food preferences in w e a n l i n g mice Mus d o m e s t i c u s . Behav. Process., 19:155-166. This s t u d y has been d e s i g n e d to e v a l u a t e t h e role of s o c k ~_ (maternaD i n f l u e n c e s on t h e d e v e l o p m e n t of f e e d i n g b e h a v i o u r in mice. A l a r g e e n c l o s u r e , allowing d i r e c t o b s e r v a t i o n , was d i v i d e d in to t h r e e s e p a r a t e a r e a s : a c e n t r a l a r e a for t h e n e s t a nd two s i d e f e e d i n g a r e a s a t o p p o s i t e e n d s . In one th e y o u n g could feed with t h e i r mother, in t h e o t h e r one t h e y o u n g had to feed on t h e i r own. Thre e d i f f e r e n t g r o u p s were s t u d i e d : one had the same food in the two f e e d i n g a r e a s ; t h e s e c o n d had a l e s s p a l a t a b l e food in th e m o t h e r f e e d i n g area: t h e t h i r d had two d i f f e r e n t k i n d s of food with similar p a l a t a b i l i t y in th e feed i n g a r e a s . The d e v e l o p m e n t of i n f a n t s ' b e h a v i o u r e x p r e s s e d as: a) o r d e r of exit from t h e ne st ; b) f i r s t d i r e c t i o n t a k e n on l e a v i n g t h e n est: c) f i r s t food consumed: dl f r e q u e n c y of c o n t a c t s with m o t h e r o r p u p food, was e l e c t r o n i c a l l y r e c o r d e 4 and a n a l y s e d . The r e s u l t s c l e a r l y show t h a t w e a n l i n g mice s t r o n g l y p r e f e r to follow t h e i r m o t h e r a t h e r f e e d i n g s i t e s e v e n when th e m o t h e r ' s food is los=; p a l a t a b l e t h a n t h e i r ~wn. F u r t h e r m o r e i n f a n t s of one g r o u p , in a followin~ b i n a r y choice t e s t . p r e f e r r e d to e a t t h e food t h e y e x p e r i e n c e d in t h e mum's f e e d i n g a r e a i n s t e a d of w h a t t h e y e x p e r i e n c e d in t h e i r ~wn f e e d i n g area. The f i t n e s s of s u c h b e h a v i o u r in more n a t u r a l s i t u a t i o n s is d i s c u s s e d . KEY WgRDS: Food preferences, ,~oeial i n f l u e n c e s , mice
INTRODUCTION The mechanisms involved in social transmission of food preferences are well understood, particularly in rodents. Weanling rats know neither the identity nor the
location
accumulated
of
t h e ir
experience,
dietary
needs,
probably
whereas
during
adults
exploration
of of
the their
colony
have
home-range
(Galef, 1977l. Galef and co-workers have identified the mechanisms of tra ns fer of dietary information from adults to wear, ling offspring. Factors such as smell and taste of the mother's milk (Galef & Clark, feeding grounds
~Calef & Clark, 1971;
1972}, adults' physical
Galef & Henderson,
1972),
presence on and
residual
o l f a c t o r y stimuli d e p o s i t e d by a d u l t s on food s o u r c e s (Calef & Neiber. 1976) mc~v a f f e c t y o u n g r a t s ' f u t u r e food choices.
0376-6357/89/$03.50
© 1989 Elsevier Science Publishers B.V. (Biomedical Division)
156
Since t h e y a r e social animals, l i v i n g in a colony b u r r o w s y s t e m from which they
e m e r g e to f o r a g e
logical to
expect
in t he
that
there
surrounding may
be
e n v i r o n m e n t (Calhoun,
exchanges
of
in fo rmatio n
1962).
it is
among
adult
members of t h e same coiony a b o u t t h e n a t u r e an d location of food. It has in fa c t been shown
t h a t an a d u l t a n i m a l ' s choice b e t w e e n
two d i f f e r e n t
d i e t s is a f f e c t e d by social i n t e r a c t i o n with a n o t h e r a d u l t p r e v i o u s l y fed on one of t he two d i e t s (Ca!of & Wingmore, 1983: P o s a d a s - A n d r e w s & Roper, 1983; S t r u p p & L e v i t s k y . 1984). Olfactory
signs
from
interaction between the s e c ond
a ni ma l ' s
an
animal fed
on
two animals (i.e. nose
increased
preference
for
(Galef & Stein, 1985). On t h e o t h e r h a n d
a
a
certain
to nose) food
food,
together
with
lie at t h e b a s i s of t h e
already
eaten
by
the
first
it has been shown t h a t a h u n g r y r a t
may, in a familiar e n v i r o n m e n t , follow a n o t h e r r a t ' s t r a c e s in o r d e r to find food (Galef
et
transmit
al.,
1987).
It
to a n o t h e r
toxicosis (Galef
does
a
et
not,
however,
conditioned
aversion
al..
1983).
For
a
more
seem possible for
a
for
foodstuff
detailed
one
animal
to
caused
a
which
a n a l y s i s of
this
complex
phenomenon, s e e t h e two r e v i e w s p u b l i s h e d by Galef (1977 and 19R8). A l t h o u g h a c o n s i d e r a b l e amount is b e h a v i o u r in r a t s . social s p e c i e s
known
about
these aspects
of f e e d i n g
t h e same c a n n o t be said for mice. Mice a r e also a s t r o n g l y
with e c o - e t h o l o g i c a l f e a t u r e s
which make n o n - g e n e t i c m e c h a n i s m s
of i nforma t i o n t r a n s m i s s i o n l i k e l y (Mainardi & Mainardi 1988). It
is
known
that
early
experience
p r e f e r e n c e s (Mainardi e t al.. 1976), preferences
in t h e same
with
certain
foodstuff
affects
food
r~ot all t h e s u b s t a n c e s h o w e v e r a f f e c t t h e s e
way. I t has
been
shown
(Mainardi e t al.. 1982) t h a t
e x p e r i e n c e a t w e a n i n g with g e n t i a n e x t r a c t does not a l t e r t h e a t t i t u d e of a d u l t mice
towards
this
smell,
whereas
early
experience
with
heptanoic
acid,
an
u n p l e a s a n t s t i m u l u s , may r e d u c e a v e r s i o n in a d u l t s (Mainardi e t al, 1985), A recent study
has
d e m o n s t r a t e d t h a t w e a n i n g animals will e a t an u n p l e a s a n t ,
but not t o t a l l y r e j e c t e d f o o d s t u f f such as fennel seeds, i f t h e y have had e a r l y e x p e r i e n c e with it. Moreover p u p s a r e l i k e l y to r e c o g n i z e t h e s t i m u l u s d i e t from t he m o t h e r ' s milk, a nd will s e l e c t for it in a s u b s e q u e n t b i n a r y food choice t e s t (Mainardi e t el., in p r e s s ) . In all t h e s e e x p e r i m e n t s , a l i m e n t a r y e x p e r i e n c e v~a~ imposed on t h e animal, either
by
mother's
means milk, On
of
a direct
the
allowed to choose its
experience
contrary,
in
the
with
a partita}far
following
experiment
own a l i m e n t a r y e x p e r i e n c e , sin ce
diet, the
we w ere
or
v ia
the
animal was i n t e r e s t e d in
e v a l u a t i n g t h e e x t e n t to which social b o n d s with t h e m o t h e r a f f e c t food choice. In
fact,
cnnsidering
t he
eco-ethological
features
of
the
species
under
i n v e s t i g a t i o n , y o u n g mic~ a r e l i kely to be i n f l u e n c e d by t h e m o t h e r ' s ~ r e s e n c e at l e a s t till t h e y a r e complctely wea ~ed.
157
The
experiment
was
first solid meal, the pups or to This
feed
alone
situation
set
in a n o t h e r
was
up
in a c o m p l e x a r t i f i c i a l
enclost~re.
were allowed to follow their mother to her feeding
reinforced
areas. The pups* behaviour
area
using
in t h e s e
to which
different situations
diets
the in
mother the
hcd
For
their
feeding area no access.
different
feeding
was record,~d and then analyzed.
MATERIALS
W e constructed enclosures allowing direct observation o~" the litters (see Pig I). The enclosures consisted of black PVC rectangular boxes 30 x 120 x I',.5 cm. A maze was built inside the box using removable partitions which s~bdivided it into three separate areas: a central area for the nest and two side areas at opl.,osite ends, provided with food and water.
HUH FEEDING AREA I
I bi~ hoi¢~
f Tm~ll hulct ¢
z
F i g 1. R o u g h p l a n o f e x p e r i m e n t a l e n c l o s u r e (120 x 30 x 14.5 c m ). T h e e ~ a c t m e a s u r e m e n t s o f t h v h o l e s z n d f e e d i n g t r a y s a r e g i v e n ",~ t;,e t e x t . A n i m a l s e n t e r MUM f e e d i n g area t h r o u g h big holes ( m o t h e r and p u p s ) and PUP f e e d i n g area t h r o u g h small holes ( p u p s o n l y ) .
Each f e e d i n g area had 6 food c u p s (6 × 9 x ? cm ) c o n s i s t i n g of a f r o n t t r a y c o n t a i n i n g t h e food and a t r a y b e h i n d to collect spillage (Fig 2). The c e n t r a l area (20 x 30 cm) was d i v i d e d i n t o t w o l i v i n g ~paces, one f o r t h e nest and the o~her as an entrance corridor to the two feeding areas. The partition c l o s i ~ g o f f t h e f i r s t f e e d i n g a r e a h a d 2 h o l e s (30 mm in d i a m e t e r ) in it, l a r g e e n o u g h f o r b o t h t h e f e m a l e a n d tl~e y o u n g t o p a s s t h r o u g h , T h e p a r t i t i o n c l o s i n g o f f t h e s e c o n d f e e d i n g a r e a , h a d 3 h o l e s (16 m ~ in d i a m e t e r ) , b i g e n o u g h o n l y f o r ~he y o u n g , b u t n o t f o r t h e i r m v t h e r t o p a s s . Thus we obtained two separate feeding areas, one where the mother could f e e d w i t h h e r y o u n g , h e r e a f t e r r e ~ . e r r e d t o a s MUM a r e a , a n d o n e w h e r e t h e young had to feed on their own, hereafter referred to as PUP area. Each f e e d i n g c u p a l l o w e d t w o a n i m a l s t o f e e d a t a t i m e so a s n o t t o c r e a t e c o m p e t i t i o n for food.
158
o
1,5
cm
3
f
Ir ( I
F~g 2. Diaqram of food c up u s e d in t h e e x p e r i m e n t : t r a y in f r o n t for food powder, t r a y b e h i n d to e n s u r e s p i l l a g e c o n t r o l . H e a s u r e m e n t s a r e g i v e n in t h e text. The e x p e r i m e n t was b a s e d on t h e u s e of 3 d i f f e r e n t d i e t s : commercial, f e n n e l a nd j u n i p e r diet. The commercial d i e t c o n s i s t e d of l a b o r a t o r y p o w d e r e d chow for mice (Hil Horini). F en n el an d j u n i p e r d i e t w e r e o b t a i n e d in o u r l a b o r a t o r y mixing 3% and 1.5% g r o u n d f e n n e l s e e d s (FEN d i e t ! an d 2) o r 2.5% g r o u n d j u n i p e r b e r r i e s (JUN diet) to t h e commercial diet. From p r e v i o u s o b s e r v a t i o n s we kne w t h a t n e i t h e r f e n n e l n o r junipeL- a r e v e r y p a l a t a b l e to mice. SUBJECTS AND PROCEDURE T w e n t y - f o u r p r e g n a n t fem~.le Swiss mice ( C h a r l e s River Italia) w e r e i s o l a t e d be fore d e l i v e r y in b r e e d i n g boxes w ith food lHil Horini) an d w a t e r ad lib.. They we re k e p t t h e r e ~ f t e r d e l i v e r y u n t i l p u p s w e r e ~ d a y s old, On d a y 5 a f t e r b i r t h e a c h l i t t e r was limited to I0 i n d i v i d u a l s . On d ay 14 a r a n d o m l y c h o s e n male and female p u p from eaci~ !.~tter '~ere m a r k e d so t h e y could be r e c o g n i z e d a t s i g h t by a d i f f e r e n t c o l o u r e d blotch at t h e bottom e n d of t h e i r b a c k s a n d u s e d as focal animals ( s e e p r o c e d u r ? by L e h n e r ' s , 1919l. I t was t h u s p o s s i b l e to d i s t i n g u i s h t h e two focal animals e v e n wh en t h e y w e r e p a r t i a l l y immers ed in t h e f e e d i n g c u p s . H o t h e r s w e r e r a n d o m l y a s s i g n e d to 3 d i f f e r e n t g r o u p s a c c o r d i n g to t h e following scheme. COHH GROUP FEN GROUP MIX GROUP HlX FEN
: : : :
commercial d i e t i n both f e e d i n g a r e a s (MUM and PUP). f e n n e l d i e t l (3%) in HU~ a r e a and c o m e r c i a l d i e t in PUP a r e a . s u b d i v i d e d i n t o two c a t e g o r i e s fenn,,:l d i e t 2 (1.5%~ in HUM a r e a and j u n i p e r d i e t i n PUP a r e a .
HIX JUN
: juPiper
diet
i n HUH a r e a and f e n n e l d i e t
2 (1.5%)
i n PUP a r e a .
In t h e mix g r o u p we u s e d 1.5% F en n el d i e t in o r d e r to c o u n t e r b a l a n c e p o s s i b l e p r e f e r e n c e s for t h e f e nnel o r t h e j u n i p e r diet, s i n c e t h e y a p p e a r to be more or l e s s e q u a l l y u n p a l a t a b l e .
159
We u s e d t h e s e d i f f e r e n t g r o u p s to co mp are t h e f e e d i n g b e h a v i o u r s of t h e y o u n g whe n t h e food in t h e PUP a r e a was : a) t h e same as of t h e m o t h e r ' s (COHH q r o u p ) ; bl more p a l a t a b l e t h a n t h e m o t h e r ' s (FEN g r o u p ) ; c) simply d i f f e r e l t fro:~= ~h~ m o t h e r ' s ( H I ; ( g r o u p ) . On Day 14 e a c h female was t r a n s f e r r e d t o g e t h e r with h e r l i t t e r to one of t h e t e r r i t o r i e s d e s c r i b e d a b o v e a n d k e p t t h e r e for 10 d a y s . All c u p s in HUM and PUP a r e a s w e r e filled e v e r y d ay w ith f r e s h food. O b s e r v a t i o n and d i r e c t r e c o r d i n g of focal a n i m a l s ' b e h a v i o u r w e r e c a r r i e d o u t for 7 c o n s e c u t i v e day s , from da y 18 to 24. Th,a 24 l i t t e r s (in e a c h l i t t e r N=IO) w e r e o b s e r v e d e v e r y day for 20 m i n u t e s c o n s e c u t i v e l y a nd an e l e c t r o n i c c o u n t e r r e c o r d e d t h e b e h a v i o u r a l p a r a m e t e r s of t h e focal animals d e s c r i b e d below. The e v e n i n g b e f o r e each e x p e r i m e n t a l s e s s i o n , m o t h e r s a nd p u p s w e r e c o n f i n e d lo t h e c e n t r a l a r e a of t h e t e r r i t o r y a nd had no a c c e s s to food for 12 h o u r s . During t h i s time t h e y had only a piece of a p p l e a nd w a t e r. Next m o r n i n g t h e e x p e r i m e n t e r o p e n e d t h e p a r t i t i o n s i nt o MUM and PUP f e e d i n g a r e a s an d r e c o r d e d t h e following behaviours: a) b) c) d)
o r d e r of e x i t from t h e n e s t b e t w e e n m o t h e r an d focal animals; f i r s t d i r e c t i o n (MUM or PUP a r e a ) t a k e n on l e a v i n g t h e n e s t by focal animals: f i r s t food c o n s u m e d by focal animals; focal a ni ma l s ' f r e q u e n c y of c o n t a c t with HUM an d PUP foods.
On da y 25 all p u p s (2 focals p l u s t h e i r 8 s i b l i n g s ) in t h e MIX g r o u p were g i v e n a b i n a r y food choice t e s t , in o r d e r to e v a l u a t e t h e i r b e h a v i o u r when faced with a c hoi c e a f t e r s e v e n d a y s of e x p e r i e n c e . At t h a t time p u p s a r e fu lly weaned a c c o r d i n g to Konig a n d Markl (1987). This t e s t was o r g a n i z e d for t h i s g r o u p o n l y s i n c e t h e two f o o d s t u f f s w e r e l e s s oz- m~re e q u a l l y u n p a l a t a b l e (informal o b s e r v a t i o n s s how e d t h a t n a i v e mice c o n s u m e d a b o u t 45 of 1.5% of fen n el d i et and 55 of 2.5% j u n i p e r d i e t d u r i n g a b i n a r y ch o ice t e s t ) . The a p p a r a t u s for t h e t e s t c o n s i s t e d in t r a n s p a r e n t p l e x i g l a s boxes 25 x 38 × 15 cm c o n t a i n i n g two food c u p s i d e n t i c a l to U,,,se u s e d in t h e e n c l o s u r e ( se e fig 2). Thus it was p o s s i b l e to m e a s u r e c o n s u m p t i o n a c c u r a t e l y . One of t h e two food c u p s c o n t a i n e d j u n i p e r , an d t h e o t h e r f e n n e l diet. In t h e b i n a r y choice t e s t , t h e animal was pl a c e d in one of t h e s e boxes a f t e r a c c u r a t e l y m e a s u r i n g and w e i g h i n g t h e food c u p s to 0.0! g. Mice w e r e remo v ed from t h e boxes 24 h o u r s l a t e r a nd food c u p s w e r e r e - w e i g h e d , to s ee how much of t h e two feed s had been e a t e n by e a c h animal. Te s t boxes w e r e also p r o v i d e d with w a t e r ad lib an d c<~tton-wool ~or the nest, The data basis f o r statistical analysis comprises series of binary responses given by each focal animal during the seven days of observation, In order to have a general idea of the behaviour recorded throughout the entire period, the da i l y r e s p o n s e s of each focal animal w e r e a d d e d up for p a r a m e t e r s b, c and d. In t h i s way t h e i nf or m a t i on o f f e r e d b y e a c h focal anim,~l is t h e n u m b e r of times t h e animal made one or o t h e r choice in t h e week of o b s e r v a t i o n . Wilcoxon t e s t was u s e d for t h e s t a t i s t i c a l a n a l y s i s . These d a t a ~re b i n a r y a n d c l a s s i f i c a t o r y and t h u s e x c l u d e t h e a p p l i c a t i o n of S t u d e n t ' s t tes~: in f a c t each animal c h o o s i n g b e t w e e n HUM o r PUP a r e a s a n d foods " s e " v e s as his own c o n t r o l " . As reported in Siegel (1956) the Wilcoxon matched-pairs signed-ranked test "gives more weight to a pair which shows a large diffe=-ence between the two conditions than to a pair which shows a ~mall difference". These characteristics make this one of the more suitable te~t for the analysis of behavioral responses such as those considered in this research.
160
RESULTS The
two
categories
in
the
they
MIX
GROUP
considered
together;
preference
f o r FEN o r JUN d i e t . O b v i o u s l y
for each category). the
mother's
groups a)
The parameters
Order
allowed
The
presence
of exit access
from
to
focal animal's
affected
analyzed
were:
the
nest:
was
the
al, m o s t
MIX
in t h i s
the
FEN
and
MIX
to counterbalance
directly
strongly
food,
(i.e.
w e r e in f a c t c r e a t e d
group
recorded pups
first
animal
always
the
slight
N= 24 {12 f o c a l a n i m a l s behavio,~r
feeding
showed
behaviour
to leave mother
JULY) w e r e
possible
the
in
nest,
every
that
in
all 3
on
being
experimental
g r o u p . CORM GROUP: 34 exits o u t of 42; FEN GROUP: 35 o u t of 42; MIX GROUP: 80 o u t of 84. This f a c t may have c r e a t e d a t r a i l i n g b) F i r s t
direction
taken
situation for the young.
on le~=ving t h e nest. D u r i n g
the period
c o n s i d e r e d (18-24 days of age) focal animals could t a k e ~ PUP
area:
their
daily
choice
Wilcoxon t e s t in
t h e way
t h a t focal
of all
pups
greatly preferred
was
desrribed
three
recorded, in
added
t h e method
of observation
f i r s t d i r e c t i o n MUM o r
up
and
sectio==.
compared
This
using
a n a l y s i s shows
experimental g r o u p {CORM, FEN and MIX g r o u p s )
to follow t h e i r m o t h e r o r to j o i n h e r in MUM area ~Table I. A).
Table I. The data r e p o r t e d in t h e t a b l e are s t a t i s t i c a l v a l u e s (T) o b t a i n e d u s i n g Wilcoxon's test. The c o n t e n t s of p a r t A are r e f e r r e d to n u m b e r of times each focal animal choose MUM o r PUP f e e d i n g area on f i r s t d a i l y e x i t from t h e nest. Part B is r e f e r r e d to f i r s t food c o n t a c t e d b y each focal animal d o r i n g t h e seven days of observation and part C to frequency of contact with M U M food in the same period. { C O M M = commercial group; FEN= fennel group; MIX= mixed group.)
GROUP
N
T value
COMH
1~
11.0
FEN
12
9.0
0.01
NIX
24
15.5
< O.OOi
COMM
12
8.5
0.01
FEN
12
2.5
0.004
~IX
24
8.0
< 0.001
COHN
12
0.0
= 0,002
FEN
12
8.0
= 0.01
Hl×
24
37.0
P
(
=
0.025
0.004
161
Furthermore for
the
the evolution
three
percentage
of this
experimental
behaviour
is s h o w n
and
every
groups
of focal animals choosing
for
in Fig day
3 which reports,
of
observation,
the
the HUH area as the first direction.
loo -
\
9O
-
a COMM m FEN MIX
.
~
7O
~ 6o ~ ~o ~
4o
L~. 3o ~
2o
0 1
2DAYS3OF
4 5 0 OBSERVATION
Fig 3. P e r c e n t a g e o f f o c a l a n l m a I z c h o o s i n 9 H U H s i d e a s f i r s t d i r e c t i o n d u r i n g t h e s e v e n d a y s o f o b s e r v a t i o n . (COHH- c o m m e r c i a l g r o u p ; FEN = f e n n e l g r o u p ; HI}(= m i x e d g r o u p . ) c) F i r s t food consumed. As f o r the p r e v i o u s D a r a ~ e t e r the 4ata w e r e analyzed as the total number o f choice.
Wilcoxon's
s i g n i f i c a n t both
times each focal animal s~!ected MUM o r PUP foo4 as f i r s t
test
shows
that
the
preference
for
HUH
food
was
when PUP and HUH foods w e r e the same (COHH g r o u p )
highly as well
as when t h e y were d i f f e r e n t (FEN and HI× g r o u p ) (Table *. B). Fig 4 r e p o r t s the p e r c e n t a g e o f pups selecting HUH food as f i r s t
choice d u r i n g
the seven days o f
observation. d) F r e q u e n c y o f c o n t a c t comparing
w i t h HUH and PUP food: the analysis was c a r r i e d out
f o r each focal animal the total number of contacts w i t h HUH food to
the total number
of contacts
observation.
analysis
only
went
prefer
The to
HUH
it ( T a b l e
contacts for every
with
food
I, C). In
HUH
food
with PUP
using a~ t h e i r
~ddition over
d a y of o b s e r v a t i o n
food recorded
Wilcoxon's test
the
first the
choice data
(see
were
total number
( F i g 5).
during
clearly
the seven
indicates
point
c)
considered
of contacts
but as with
days
tha'. pups
of not
continued
to
percentages
of
the
two foods
162
11o lOC
L~
_~ "~o ~
ao
~
70
~
6o
~
40-
~
20-
~
10-
COMM FEN
A
MIX
~so 3o-
2
.3 DAYS
4 .5 OF" O B S E R V A T I O N
6
7
Fig 4. P e r c e n t a g e of focal a n i m a l s s e l e c t i n g MUM food a s f i r s t c h o i c e d u r i n g t h e s e v e n d a y s of o b s e r v a t i o n . ~qOMM= c o m m e r c i a l g r o u p ; FEN= f e n n e l g r o u p ; MIX= mixed g r o u p . )
11o 1oo
~
®.-...
9o
COMM FEN
•
~..1q •
::I::
7o
~
6o
~-
§
5o
~
3O
MIX
4O
100
I
'> ,, "DAYS ~OF
4 5 OBSERVATION
6
7
Fig 5. P e r c e n t a g e of c o n t a c t s of f o c a l a n i m a l s w i t h MUM food o v e r t h e n u m b e r of food c o n t a c t s r e c o r d e d d u r i n g t h e s e v e n d a y s of o b s e r v a t i o n . (COMM= c o m m e r c i a l g r o u p ; FEN: f e n n e l g r o u p ; MIX= mixed g r o u p . )
total
163
Results
obtained
Student's
t
animal
the
as
percenta.ge
consumed d u r i n g
category
analysis
binary
food
choice
the
mother's
in Fig
that
a t e 60.51% o f t h e
old. therefore
already
young
didn't
show such
revealed
to
a
be
better
diet
eaten
animals
a~lalyzed
using
out
of
the
total
food
c a t e g o r i e s M~× FEN and
mothe'r's diet. (n=55,
t = 5.36,
than
t,~,e H!~
FEN
A n i m a l s o f MIX JUN
f o o d e v e n if t h e y a r e
P<0.001). T h e
youngs
(n=57, t = - 0 A 3 , n .S } fennel
to
t h e a n i m a l s o f t h e MIX
i.e. j u n i p e r .
for mother's
a preference stimulus
belong~.ng
die','. Le. f e n n e l , a n d
preference
weaned
category
were
6.
indicates
showed a strong
test
T h e d a t ~ w e r e coY2ected f o r e a c h
Mean v a l u e s o f t h e d i f f e r e n t
a t e 49.07% o i t h e m o t h e r ' s
JUN c a t e g o r y category
the of
t i m te:;t.
MIX JUN a r e r e p o r t e d The
from
f o r o n e s a m p l e (nulI. h y p o t h e s i s ) .
o n e in i n d u c t a g
Juniper a
25 d a y s
o f MiX FEN tast~ has
preferehce
in
t h e s e ar, i m a l s . ~oo N
9o
70 ~z
N=57 L=-0.48 n s
N=55 t=5.36 p<0.001
6o
~
5o
~o
4o
~ ~o 2O Z o
MIx FeN
~qtx
durJ
Fig 6. M e a n p e r c e P t ~ ' g e ( a n d s t a n d a r d e r r o r ) o f m o t h e r ' s d i e t e a t e n b y all p u p s ( f o c a l a n d t h e i r s i b l i n g s ) of MiX FEN a n d MiX JUN c a t e g o r i e s d u r i n g t h e b i n a r y c h o i c e t e s t . S t a t i s t i c a l v a l u e s a r e g i v e n in t h e f i g u r e .
164
GENERAL DISCUSSION
The s t a r t i n g h y p o t h e s i s of t h i s s t u d y was t h a t p u p s will follow t h e m o t h e r to
feeding
sites
and
there
learn
mother's
food
c h a r a c t e r i s t i c s . Not much
is
known a b o u t t h e o r i g i n a nd d e v e l o p m e n t of food p r e f e r e n c e s in mice, e x c e p t t h a t e a r l y e x p e r i e n c e with p a r t i c u l a r s u b s t a n c e s can b r i n g a b o u t forms of l e a r n i n g in l a b o r a t o r y mice (Mainardi e t al. 1976, 1982, .~985). Galef a nd
Clark (1971)
following a d u l t s " c a r a v a n i n g " has
to t h e been
mouse (Crowcroft,
maintain that
feeding sites.
youn9
rats
Th~s b e h a v i o u r ,
l e a r n w h a t is known
as
s afe by
"trailing" or
o b s e r v e d in a va~dety of s p e c i e s of animals: t h e h o u s e
1966); s h r e w s
(Crowcroft,
1957); m e e r k a t s (Ewer,
1968); wild
and d o m e s t i c a t e d r a t s (Calhoun, 1962). For t e s t i n g o u r h y p o t h e s i s
was c r e a t e d a s i t u a t i o n in which m o t h e r s an d
l i t t e r we re p u t i nt o a t e r r i t o r y with s e p a r a t e s o u r c e s of t h e same food (COHM g r o u p ) . We f u r t h e r r e i n f o r c e d t h i s s i t u a t i o n by: l) p u t t i n g an u n p a l a t a b l e f e nne l d i e t in t h e a r e a to which both m o t h e r a n d p u p s had a c c e s s , w h e r e a s we p u t t h e more p a l a t a b l e commercial d i e t in t h e t h a t a r e a only t h e p u p s could r e a c h (FEN g r o u p ) ; 2) u s i n g d i f f e r e n t u n p a l a t a b l e d i e t s for MUM a n d PUP a r e a s (MIX g r o u p ) . R e sul t s from t h e COMM g r o u p s h o w ed t h a t once t h e m o t h e r l e f t t h e n es t . he r y o u n g p r e f e r r e d
t h e a r e a in h e r company. They could e i t h e r s t a y ~n,~ oat
t h e r e , or go off to t h e o t h e r a rea,
w h e r e t h e food was e q u a l l y a p p e t i s i n g . Yet
mouse p u p s c h o s e for t h e i r f i r s t food t h a t e a t e n by t h e m o t h e r a n d continu~.d to p r e f e r it for s e v e r a l d a y s . The d e v e l o p m e n t of f e e d i n g p r e f e r e n c e s in t h e t h r e e different
groups
is
very
s i milar
day. P u p s
with
the
preference
fo r
in t h e FEN an d MIX g r o u p s
mother's
food
d e c r e a s i n g slow da y
by
also p r e f e r r e d
t h e i r m o t h e r ' s food
a nd c o n t i n u e d to do so u n t i l d ay 22 o r 23. Up u n t i l t h i s
a ge p u p s made few attemp'~s to g e t away from t h e i r m o t h e r s an d e a t t h e food on t h e o t h e r side. It is w o r t h notin~ t h a t t h i s w,~ also t r u e
when t h e food on t h e m o t h e r ' s
si de was l e s s appetizi~lg t h a n t he o t h e r . This means t h a t mice p u p s ' b e h a v i o u r is s t r o n g l y i n f l u e n c e d by
the mother's presence:
t he occasion to l e a r n t h e i d e n t i t y an d
s t a y i n g close to h e r
they have
location of food. Moreover, it has been
o b s e r v e d in o t h e r animals, s u c h as c a t s , t h a t t h e y o u n g e a t w h a t t h e i r m o t h e r e a t s . e v e n if it is an u n u s u a l food for t h e s p e c i e s ( b a n a n a s an d p o t a t o e s ) an d more s u i t a b l e food (meat) may be a v a i l a b l e (Wyrwicka, 1978). C o n s i d e r i n g t h e r e s u l t s of t h e b i n a r y choice t e s t , we can note ~.hat at d ay 25 (when rJups a r e fully weaned) th~:y m a i n t a i n t h e p r e f e r e n c e for m o t h e r ' s food in t h e c;,se s he had be e n fed on j u n 3 p e r diet. The same is not t r u e ~.Jhen m o t h e r had be~n fed on f e n n e l diet, e v e n
if als o in t h i s c a s e t h e p u p s
achieve the
165
chance level (50%). The difference between the two groups is proI~ably due to t h e fa c t t h a t j u n i p e r m i g h t be a littl~ more p a l a t a b l e flav o u r, an d a c c o r d i n g to Galef's (19??) s t a t o m e n t , for s t a b l e fc~,d p r e f e r e n c e s to be e s t a b l i s h e d in r a t s ,
the food
must
be
highly
palatable,
if
the
preference
socially
transmitted
concerns an unpalatable food, as in this case. the animal that has acquired this preference
is
prepared
to
abandon
it
when
faced
with
a
more
palatable
alte~ native. The r e s u l t s of this experiment h i g h l i g h t the fact that interactions between adults and weanlings are to be found in mice as well. I f we imagine a natural situation in which a weanling animal starts to explore its external environment, it is l i k e l y to follow i t s m o t h e r or o t h e r a d u l t s of t h e colony d u r i n g t h e i r fora.qing t r i p s . In o r d e r to s u r v i v e , a y o u n g o m n i v o r o u s animal m u s t s e l e c t a n u t r i t i o n a l l y adequate
diet
from
the
myriad
of
nutritional
and
non-nutritional
or
toxic
s u b s t a n c e s p r e s e n t in i t s e n v i r o n m e n t : following a d u l t memb ers of t h e colony as far
as
the
behaviour.
food Thus
sources, young
having
animals
the
can
chance feed
on
to l e a r n , "safe"
is
a
foods,
truly at
adaptive
l e a s t at
the
beginning. This experiment therefore, r e p r e s e n t s f o r this species a f i r s t step towards u n d e r s t a n d i n g the importance of the interaction between simple stimuli (taste and smell) and social contexts. On the o t h e r hand the social organization of the species (Crowcroft, cosmopolitan,
capable
of
1955 and 1966), rapid
environmental changes (Berry,
together
adaptation
to
with the even
quite
fact that it is considerable
1981) makes it a species p a r t i c u l a r l y
suited f o r
the s t u d y of mechanisms u n d e r l y i n g non-genetic transmission of in(ormation. Acknowledgements: The authors thank d r B.C. Ga|ef, j r . (HcHaste~ Un iv ersity. Canada) f o r his comments on this manuscript, d r P. Henozzi ( U n i v e r s i t y of Parma, Italy) f o r statistical suggestions and Hrs V. Vascelli f o r h~r technical assistance. This paper has been supported by Italian H.P.I. and C.N.R. granLs. REFERENCES CathoLic, J.B. 1962. The ecology and sociology of the norway rat. Bethesda. Haryla.~d: United States Department of Health, Education and Welfare. Crowcroft. P. 1955. Social organization in wild mouse colonies. Br. J. Anita. Beh,~;'.. 3: 36. Crowcroft, P. 1957. The life of the shrew. London: Hax Reinhardt. Crowcroft, 1". 1966. Hice all over. London: A.T. Fowlis and Co. Etver. RF. 1968. Ethology of ma¢.~mals. London: Plenum Pro~s. Galef. B.C j r . 1977. Hechanisms f o r the social transmission of acquired food preferences ~'rom adult to weanling rats. In: L.M. Baker, H.~. Best af)d H. Domjan (eds), L ~ r n i n g mechanisms in food selection. Baylor University Press, pp. 1~3-148. Galef, B.G. j i . 1988. Commu~,ication of information concerning distant diets J~= a social, central-place foraging species: Rat tus norveflicus. In: T.R. Zentall and B.G. Galef (Eds), Social learning - Psychological and Biological perspectives. Lawrence Erlbaum associates, Hillsdale, New Jersey, pp. 119-138.
166
Galef, B.G. j r . and Clark, M.H. 1971. Social factors in the poison avoidance ana feeding behaviour of wild and domesticated r a t pups. J. Cornp. Psychol., 75: 341-357. Galef, B.G. j r . a n d H e n d e r s o n , P.W. 1072. M o t h e r ' s milk: a d e t e r m i n a n t of f e e d i n g p r e f e r e n c e s of w e a n l i n g r a t p u p s . J. Comp. Physiol. Psychol., 78: 213-219. Ga]ef, B.G. j r . a nd Clark, M.M. 1972. M o t h e r ' s an d a d u l t p r e s e n c e : two f a c t o r s d e t e r m i n i n g i n i t i a l d i e t a r y s e l e c t i o n by w e a n l i n g r a t s . J. Comp. Physiol. Psychol., 2: 220-225. Galef, 5.C. j r . and Heiber, L. 1976. Role of r e s i d u a l o l f a c t o r y c u e s in t h e d e t e r m i n i n g of f e e d i n g d i e t selec'~iou a n d e x p l o r a t i o n p a t t e r n s of d o mes tic r~ts. J. Comp. Physiol. Psych., 90: 7:~7-739. Galef, B.G. jr. and Wigmore. S.W. 1983. Transfer of in~'ormation concerning distant foods: a laboratory investigation of tile "information - centre" hypothesis. Anirn. Beha:'., 3 h 748-758. Galef, B.G. jr., Wigrnore, S.W. and Kennet, D.J. 1983. A failure to fiad socially mediated taste aversion learning in N o r w a y rats (R~ nor ye£icusL J. cornp.
Psych., 97: 358-363. Galef, B.G. j r . a n d Stein, M. 1985. D e m o n s t r a t o r i n f l u e n c e on o b s e r v e r diet p r e f e r e n c e : a n a l y s i s of c r i t i c a l social i n t e r a c t i o n s an d o l f a c t o r y s i g n a l s . Anita. L e a r n i n g a nd Behavior, 13: 31-38. Galef, B,G. j r . , M i s c h i n g e r , A. a nd Malenfant, S.A. 1987, H u n g r y r a t ' s following of c o n s p e c i f i c s to food d e p e n d s on t h e d i e t s e a t e n by p o t e n t i a l l e a d e r s . Anim. Behav., 35: 1234-1239. Konig, B, a nd Harkt, H. 1987. M atern al c a r e in h o u se .;ice. I. The w e a n i n g s t r a t e g y as a m . a n s for p a r e n t a l m a n i p u l a t i o n of o f f s p r i n g q u a l i t y . Behav. Ecol. Sociobiol., 20: 1-9. Leh;!er, P.N. 1979. Handbook of e t h o l o g i c a l meth o d s. Garland, New York an d Londra, pp. 114-117. Mainardi, M., P a r m i g i a n i , S., Csermely, D. an d P=-squali, A. 1976. Food p r e f e r e n c e s in mice: an a n a l y s i s u s i n g wheat, rice, chrysz~lis flo u r a n d commercial food p e l l e t s . Acc. Naz. Lincei, 61: 635-640. H a i n a r d i , H., P a s q u a l i , A., S a c c h e t t i , D. an d Damon, A. 1982. Food p r e f e r e n c e s in mice: an a n a l y s i s u s i n g Ge n t j a n a lute_a_ e x t r a c t an d e n a n t h i c acid. Acc. Naz. Lincei, 72: 37-42. MainardL H., Pasqua!':, A. - ~nd P a s q u a l e , E. 1985. Food ch o ice in Mu_s mus_culus: e f f e c t s of e x p e r i e n c e on a v e r s i o n to an u n p l e a s a n t f l a v o u r . Biol. Behav., 10: 67-74. Mainardi, D. a nd Mainardi, M. 1988. C u l t u r e an d g e n e t i c s in t h e h o u s e mouse. In: T.R. Zentall and B . G . Galef, j r . (edsl, Social learning-Psychological and biological perspectives. Lawrence Erlbaum Associates, Hillsdale, New Jersey, pp, 239-252. H a i n a r d i , M., Poll, M. and Valsecchi. P. O n t o g e n y of d i e t a r y s e l e c t i o n hi w e a n i n g mice: e f f e c t s of e a r l y e x p e r i e n c e an d m o t h e r ' s milk. Biol. Behav., in p r e s s . P o s a d a s - A n d r e w s , A. and Roper, T.,I. 1983. ~ocial t r a n s m i s s i o n of food p r e f e r e n c e s in a d u l t r a t s . Anim. Behav., 31: 265-271. Siegel, S. 1956. N o n p a r a m e t r i c sta~isti=~ for t h e b e h a v i o r a l s c i e n c e . Hc-Graw Hill ,qook Company, New York. S t r u p p , B.J. a n d L e v i t s k y , D.A. 1984. Social t r a n s m i s s i o n of [ood p r e f e r e n c e s in a d u l t Hooded r a t s ( R a t t u s nol:vg~icus u r s L J. cornp. Ps y ch ., 98: 257-266. Wyrwicka, W. 1978, Imitation of moti~er's i n a p p r o p r i a t e food p r e f e r e n c e in w e a n l i n g k i t t e n s . Pay. J. Biol. 3ci., 13: 55-?2.
155
MATERNAL INFLUENCES ON FOOD PREFERENCES IN WE.~NLING MICE M=u_s d0mesticu s PAOLA VALSECCHI, MARISA MAINARDI. ANDREA SGOIFO AND ANTONIO TATICCHI IstJtuto di Zoologia. Universit~ degli Studi di Parma, via delle Scienze 43100 Parma, Italy
( Accepted
26 May 1989 )
ABSTRACT Valsecchi. P.. Mainardi. M.. Ssoifo. A. a n d Taticchi. A. 1989. Matern al i n f l u e n c e s on food preferences in w e a n l i n g mice Mus d o m e s t i c u s . Behav. Process., 19:155-166. This s t u d y has been d e s i g n e d to e v a l u a t e t h e role of s o c k ~_ (maternaD i n f l u e n c e s on t h e d e v e l o p m e n t of f e e d i n g b e h a v i o u r in mice. A l a r g e e n c l o s u r e , allowing d i r e c t o b s e r v a t i o n , was d i v i d e d in to t h r e e s e p a r a t e a r e a s : a c e n t r a l a r e a for t h e n e s t a nd two s i d e f e e d i n g a r e a s a t o p p o s i t e e n d s . In one th e y o u n g could feed with t h e i r mother, in t h e o t h e r one t h e y o u n g had to feed on t h e i r own. Thre e d i f f e r e n t g r o u p s were s t u d i e d : one had the same food in the two f e e d i n g a r e a s ; t h e s e c o n d had a l e s s p a l a t a b l e food in th e m o t h e r f e e d i n g area: t h e t h i r d had two d i f f e r e n t k i n d s of food with similar p a l a t a b i l i t y in th e feed i n g a r e a s . The d e v e l o p m e n t of i n f a n t s ' b e h a v i o u r e x p r e s s e d as: a) o r d e r of exit from t h e ne st ; b) f i r s t d i r e c t i o n t a k e n on l e a v i n g t h e n est: c) f i r s t food consumed: dl f r e q u e n c y of c o n t a c t s with m o t h e r o r p u p food, was e l e c t r o n i c a l l y r e c o r d e 4 and a n a l y s e d . The r e s u l t s c l e a r l y show t h a t w e a n l i n g mice s t r o n g l y p r e f e r to follow t h e i r m o t h e r a t h e r f e e d i n g s i t e s e v e n when th e m o t h e r ' s food is los=; p a l a t a b l e t h a n t h e i r ~wn. F u r t h e r m o r e i n f a n t s of one g r o u p , in a followin~ b i n a r y choice t e s t . p r e f e r r e d to e a t t h e food t h e y e x p e r i e n c e d in t h e mum's f e e d i n g a r e a i n s t e a d of w h a t t h e y e x p e r i e n c e d in t h e i r ~wn f e e d i n g area. The f i t n e s s of s u c h b e h a v i o u r in more n a t u r a l s i t u a t i o n s is d i s c u s s e d . KEY WgRDS: Food preferences, ,~oeial i n f l u e n c e s , mice
INTRODUCTION The mechanisms involved in social transmission of food preferences are well understood, particularly in rodents. Weanling rats know neither the identity nor the
location
accumulated
of
t h e ir
experience,
dietary
needs,
probably
whereas
during
adults
exploration
of of
the their
colony
have
home-range
(Galef, 1977l. Galef and co-workers have identified the mechanisms of tra ns fer of dietary information from adults to wear, ling offspring. Factors such as smell and taste of the mother's milk (Galef & Clark, feeding grounds
~Calef & Clark, 1971;
1972}, adults' physical
Galef & Henderson,
1972),
presence on and
residual
o l f a c t o r y stimuli d e p o s i t e d by a d u l t s on food s o u r c e s (Calef & Neiber. 1976) mc~v a f f e c t y o u n g r a t s ' f u t u r e food choices.
0376-6357/89/$03.50
© 1989 Elsevier Science Publishers B.V. (Biomedical Division)
156
Since t h e y a r e social animals, l i v i n g in a colony b u r r o w s y s t e m from which they
e m e r g e to f o r a g e
logical to
expect
in t he
that
there
surrounding may
be
e n v i r o n m e n t (Calhoun,
exchanges
of
in fo rmatio n
1962).
it is
among
adult
members of t h e same coiony a b o u t t h e n a t u r e an d location of food. It has in fa c t been shown
t h a t an a d u l t a n i m a l ' s choice b e t w e e n
two d i f f e r e n t
d i e t s is a f f e c t e d by social i n t e r a c t i o n with a n o t h e r a d u l t p r e v i o u s l y fed on one of t he two d i e t s (Ca!of & Wingmore, 1983: P o s a d a s - A n d r e w s & Roper, 1983; S t r u p p & L e v i t s k y . 1984). Olfactory
signs
from
interaction between the s e c ond
a ni ma l ' s
an
animal fed
on
two animals (i.e. nose
increased
preference
for
(Galef & Stein, 1985). On t h e o t h e r h a n d
a
a
certain
to nose) food
food,
together
with
lie at t h e b a s i s of t h e
already
eaten
by
the
first
it has been shown t h a t a h u n g r y r a t
may, in a familiar e n v i r o n m e n t , follow a n o t h e r r a t ' s t r a c e s in o r d e r to find food (Galef
et
transmit
al.,
1987).
It
to a n o t h e r
toxicosis (Galef
does
a
et
not,
however,
conditioned
aversion
al..
1983).
For
a
more
seem possible for
a
for
foodstuff
detailed
one
animal
to
caused
a
which
a n a l y s i s of
this
complex
phenomenon, s e e t h e two r e v i e w s p u b l i s h e d by Galef (1977 and 19R8). A l t h o u g h a c o n s i d e r a b l e amount is b e h a v i o u r in r a t s . social s p e c i e s
known
about
these aspects
of f e e d i n g
t h e same c a n n o t be said for mice. Mice a r e also a s t r o n g l y
with e c o - e t h o l o g i c a l f e a t u r e s
which make n o n - g e n e t i c m e c h a n i s m s
of i nforma t i o n t r a n s m i s s i o n l i k e l y (Mainardi & Mainardi 1988). It
is
known
that
early
experience
p r e f e r e n c e s (Mainardi e t al.. 1976), preferences
in t h e same
with
certain
foodstuff
affects
food
r~ot all t h e s u b s t a n c e s h o w e v e r a f f e c t t h e s e
way. I t has
been
shown
(Mainardi e t al.. 1982) t h a t
e x p e r i e n c e a t w e a n i n g with g e n t i a n e x t r a c t does not a l t e r t h e a t t i t u d e of a d u l t mice
towards
this
smell,
whereas
early
experience
with
heptanoic
acid,
an
u n p l e a s a n t s t i m u l u s , may r e d u c e a v e r s i o n in a d u l t s (Mainardi e t al, 1985), A recent study
has
d e m o n s t r a t e d t h a t w e a n i n g animals will e a t an u n p l e a s a n t ,
but not t o t a l l y r e j e c t e d f o o d s t u f f such as fennel seeds, i f t h e y have had e a r l y e x p e r i e n c e with it. Moreover p u p s a r e l i k e l y to r e c o g n i z e t h e s t i m u l u s d i e t from t he m o t h e r ' s milk, a nd will s e l e c t for it in a s u b s e q u e n t b i n a r y food choice t e s t (Mainardi e t el., in p r e s s ) . In all t h e s e e x p e r i m e n t s , a l i m e n t a r y e x p e r i e n c e v~a~ imposed on t h e animal, either
by
mother's
means milk, On
of
a direct
the
allowed to choose its
experience
contrary,
in
the
with
a partita}far
following
experiment
own a l i m e n t a r y e x p e r i e n c e , sin ce
diet, the
we w ere
or
v ia
the
animal was i n t e r e s t e d in
e v a l u a t i n g t h e e x t e n t to which social b o n d s with t h e m o t h e r a f f e c t food choice. In
fact,
cnnsidering
t he
eco-ethological
features
of
the
species
under
i n v e s t i g a t i o n , y o u n g mic~ a r e l i kely to be i n f l u e n c e d by t h e m o t h e r ' s ~ r e s e n c e at l e a s t till t h e y a r e complctely wea ~ed.
157
The
experiment
was
first solid meal, the pups or to This
feed
alone
situation
set
in a n o t h e r
was
up
in a c o m p l e x a r t i f i c i a l
enclost~re.
were allowed to follow their mother to her feeding
reinforced
areas. The pups* behaviour
area
using
in t h e s e
to which
different situations
diets
the in
mother the
hcd
For
their
feeding area no access.
different
feeding
was record,~d and then analyzed.
MATERIALS
W e constructed enclosures allowing direct observation o~" the litters (see Pig I). The enclosures consisted of black PVC rectangular boxes 30 x 120 x I',.5 cm. A maze was built inside the box using removable partitions which s~bdivided it into three separate areas: a central area for the nest and two side areas at opl.,osite ends, provided with food and water.
HUH FEEDING AREA I
I bi~ hoi¢~
f Tm~ll hulct ¢
z
F i g 1. R o u g h p l a n o f e x p e r i m e n t a l e n c l o s u r e (120 x 30 x 14.5 c m ). T h e e ~ a c t m e a s u r e m e n t s o f t h v h o l e s z n d f e e d i n g t r a y s a r e g i v e n ",~ t;,e t e x t . A n i m a l s e n t e r MUM f e e d i n g area t h r o u g h big holes ( m o t h e r and p u p s ) and PUP f e e d i n g area t h r o u g h small holes ( p u p s o n l y ) .
Each f e e d i n g area had 6 food c u p s (6 × 9 x ? cm ) c o n s i s t i n g of a f r o n t t r a y c o n t a i n i n g t h e food and a t r a y b e h i n d to collect spillage (Fig 2). The c e n t r a l area (20 x 30 cm) was d i v i d e d i n t o t w o l i v i n g ~paces, one f o r t h e nest and the o~her as an entrance corridor to the two feeding areas. The partition c l o s i ~ g o f f t h e f i r s t f e e d i n g a r e a h a d 2 h o l e s (30 mm in d i a m e t e r ) in it, l a r g e e n o u g h f o r b o t h t h e f e m a l e a n d tl~e y o u n g t o p a s s t h r o u g h , T h e p a r t i t i o n c l o s i n g o f f t h e s e c o n d f e e d i n g a r e a , h a d 3 h o l e s (16 m ~ in d i a m e t e r ) , b i g e n o u g h o n l y f o r ~he y o u n g , b u t n o t f o r t h e i r m v t h e r t o p a s s . Thus we obtained two separate feeding areas, one where the mother could f e e d w i t h h e r y o u n g , h e r e a f t e r r e ~ . e r r e d t o a s MUM a r e a , a n d o n e w h e r e t h e young had to feed on their own, hereafter referred to as PUP area. Each f e e d i n g c u p a l l o w e d t w o a n i m a l s t o f e e d a t a t i m e so a s n o t t o c r e a t e c o m p e t i t i o n for food.
158
o
1,5
cm
3
f
Ir ( I
F~g 2. Diaqram of food c up u s e d in t h e e x p e r i m e n t : t r a y in f r o n t for food powder, t r a y b e h i n d to e n s u r e s p i l l a g e c o n t r o l . H e a s u r e m e n t s a r e g i v e n in t h e text. The e x p e r i m e n t was b a s e d on t h e u s e of 3 d i f f e r e n t d i e t s : commercial, f e n n e l a nd j u n i p e r diet. The commercial d i e t c o n s i s t e d of l a b o r a t o r y p o w d e r e d chow for mice (Hil Horini). F en n el an d j u n i p e r d i e t w e r e o b t a i n e d in o u r l a b o r a t o r y mixing 3% and 1.5% g r o u n d f e n n e l s e e d s (FEN d i e t ! an d 2) o r 2.5% g r o u n d j u n i p e r b e r r i e s (JUN diet) to t h e commercial diet. From p r e v i o u s o b s e r v a t i o n s we kne w t h a t n e i t h e r f e n n e l n o r junipeL- a r e v e r y p a l a t a b l e to mice. SUBJECTS AND PROCEDURE T w e n t y - f o u r p r e g n a n t fem~.le Swiss mice ( C h a r l e s River Italia) w e r e i s o l a t e d be fore d e l i v e r y in b r e e d i n g boxes w ith food lHil Horini) an d w a t e r ad lib.. They we re k e p t t h e r e ~ f t e r d e l i v e r y u n t i l p u p s w e r e ~ d a y s old, On d a y 5 a f t e r b i r t h e a c h l i t t e r was limited to I0 i n d i v i d u a l s . On d ay 14 a r a n d o m l y c h o s e n male and female p u p from eaci~ !.~tter '~ere m a r k e d so t h e y could be r e c o g n i z e d a t s i g h t by a d i f f e r e n t c o l o u r e d blotch at t h e bottom e n d of t h e i r b a c k s a n d u s e d as focal animals ( s e e p r o c e d u r ? by L e h n e r ' s , 1919l. I t was t h u s p o s s i b l e to d i s t i n g u i s h t h e two focal animals e v e n wh en t h e y w e r e p a r t i a l l y immers ed in t h e f e e d i n g c u p s . H o t h e r s w e r e r a n d o m l y a s s i g n e d to 3 d i f f e r e n t g r o u p s a c c o r d i n g to t h e following scheme. COHH GROUP FEN GROUP MIX GROUP HlX FEN
: : : :
commercial d i e t i n both f e e d i n g a r e a s (MUM and PUP). f e n n e l d i e t l (3%) in HU~ a r e a and c o m e r c i a l d i e t in PUP a r e a . s u b d i v i d e d i n t o two c a t e g o r i e s fenn,,:l d i e t 2 (1.5%~ in HUM a r e a and j u n i p e r d i e t i n PUP a r e a .
HIX JUN
: juPiper
diet
i n HUH a r e a and f e n n e l d i e t
2 (1.5%)
i n PUP a r e a .
In t h e mix g r o u p we u s e d 1.5% F en n el d i e t in o r d e r to c o u n t e r b a l a n c e p o s s i b l e p r e f e r e n c e s for t h e f e nnel o r t h e j u n i p e r diet, s i n c e t h e y a p p e a r to be more or l e s s e q u a l l y u n p a l a t a b l e .
159
We u s e d t h e s e d i f f e r e n t g r o u p s to co mp are t h e f e e d i n g b e h a v i o u r s of t h e y o u n g whe n t h e food in t h e PUP a r e a was : a) t h e same as of t h e m o t h e r ' s (COHH q r o u p ) ; bl more p a l a t a b l e t h a n t h e m o t h e r ' s (FEN g r o u p ) ; c) simply d i f f e r e l t fro:~= ~h~ m o t h e r ' s ( H I ; ( g r o u p ) . On Day 14 e a c h female was t r a n s f e r r e d t o g e t h e r with h e r l i t t e r to one of t h e t e r r i t o r i e s d e s c r i b e d a b o v e a n d k e p t t h e r e for 10 d a y s . All c u p s in HUM and PUP a r e a s w e r e filled e v e r y d ay w ith f r e s h food. O b s e r v a t i o n and d i r e c t r e c o r d i n g of focal a n i m a l s ' b e h a v i o u r w e r e c a r r i e d o u t for 7 c o n s e c u t i v e day s , from da y 18 to 24. Th,a 24 l i t t e r s (in e a c h l i t t e r N=IO) w e r e o b s e r v e d e v e r y day for 20 m i n u t e s c o n s e c u t i v e l y a nd an e l e c t r o n i c c o u n t e r r e c o r d e d t h e b e h a v i o u r a l p a r a m e t e r s of t h e focal animals d e s c r i b e d below. The e v e n i n g b e f o r e each e x p e r i m e n t a l s e s s i o n , m o t h e r s a nd p u p s w e r e c o n f i n e d lo t h e c e n t r a l a r e a of t h e t e r r i t o r y a nd had no a c c e s s to food for 12 h o u r s . During t h i s time t h e y had only a piece of a p p l e a nd w a t e r. Next m o r n i n g t h e e x p e r i m e n t e r o p e n e d t h e p a r t i t i o n s i nt o MUM and PUP f e e d i n g a r e a s an d r e c o r d e d t h e following behaviours: a) b) c) d)
o r d e r of e x i t from t h e n e s t b e t w e e n m o t h e r an d focal animals; f i r s t d i r e c t i o n (MUM or PUP a r e a ) t a k e n on l e a v i n g t h e n e s t by focal animals: f i r s t food c o n s u m e d by focal animals; focal a ni ma l s ' f r e q u e n c y of c o n t a c t with HUM an d PUP foods.
On da y 25 all p u p s (2 focals p l u s t h e i r 8 s i b l i n g s ) in t h e MIX g r o u p were g i v e n a b i n a r y food choice t e s t , in o r d e r to e v a l u a t e t h e i r b e h a v i o u r when faced with a c hoi c e a f t e r s e v e n d a y s of e x p e r i e n c e . At t h a t time p u p s a r e fu lly weaned a c c o r d i n g to Konig a n d Markl (1987). This t e s t was o r g a n i z e d for t h i s g r o u p o n l y s i n c e t h e two f o o d s t u f f s w e r e l e s s oz- m~re e q u a l l y u n p a l a t a b l e (informal o b s e r v a t i o n s s how e d t h a t n a i v e mice c o n s u m e d a b o u t 45 of 1.5% of fen n el d i et and 55 of 2.5% j u n i p e r d i e t d u r i n g a b i n a r y ch o ice t e s t ) . The a p p a r a t u s for t h e t e s t c o n s i s t e d in t r a n s p a r e n t p l e x i g l a s boxes 25 x 38 × 15 cm c o n t a i n i n g two food c u p s i d e n t i c a l to U,,,se u s e d in t h e e n c l o s u r e ( se e fig 2). Thus it was p o s s i b l e to m e a s u r e c o n s u m p t i o n a c c u r a t e l y . One of t h e two food c u p s c o n t a i n e d j u n i p e r , an d t h e o t h e r f e n n e l diet. In t h e b i n a r y choice t e s t , t h e animal was pl a c e d in one of t h e s e boxes a f t e r a c c u r a t e l y m e a s u r i n g and w e i g h i n g t h e food c u p s to 0.0! g. Mice w e r e remo v ed from t h e boxes 24 h o u r s l a t e r a nd food c u p s w e r e r e - w e i g h e d , to s ee how much of t h e two feed s had been e a t e n by e a c h animal. Te s t boxes w e r e also p r o v i d e d with w a t e r ad lib an d c<~tton-wool ~or the nest, The data basis f o r statistical analysis comprises series of binary responses given by each focal animal during the seven days of observation, In order to have a general idea of the behaviour recorded throughout the entire period, the da i l y r e s p o n s e s of each focal animal w e r e a d d e d up for p a r a m e t e r s b, c and d. In t h i s way t h e i nf or m a t i on o f f e r e d b y e a c h focal anim,~l is t h e n u m b e r of times t h e animal made one or o t h e r choice in t h e week of o b s e r v a t i o n . Wilcoxon t e s t was u s e d for t h e s t a t i s t i c a l a n a l y s i s . These d a t a ~re b i n a r y a n d c l a s s i f i c a t o r y and t h u s e x c l u d e t h e a p p l i c a t i o n of S t u d e n t ' s t tes~: in f a c t each animal c h o o s i n g b e t w e e n HUM o r PUP a r e a s a n d foods " s e " v e s as his own c o n t r o l " . As reported in Siegel (1956) the Wilcoxon matched-pairs signed-ranked test "gives more weight to a pair which shows a large diffe=-ence between the two conditions than to a pair which shows a ~mall difference". These characteristics make this one of the more suitable te~t for the analysis of behavioral responses such as those considered in this research.
160
RESULTS The
two
categories
in
the
they
MIX
GROUP
considered
together;
preference
f o r FEN o r JUN d i e t . O b v i o u s l y
for each category). the
mother's
groups a)
The parameters
Order
allowed
The
presence
of exit access
from
to
focal animal's
affected
analyzed
were:
the
nest:
was
the
al, m o s t
MIX
in t h i s
the
FEN
and
MIX
to counterbalance
directly
strongly
food,
(i.e.
w e r e in f a c t c r e a t e d
group
recorded pups
first
animal
always
the
slight
N= 24 {12 f o c a l a n i m a l s behavio,~r
feeding
showed
behaviour
to leave mother
JULY) w e r e
possible
the
in
nest,
every
that
in
all 3
on
being
experimental
g r o u p . CORM GROUP: 34 exits o u t of 42; FEN GROUP: 35 o u t of 42; MIX GROUP: 80 o u t of 84. This f a c t may have c r e a t e d a t r a i l i n g b) F i r s t
direction
taken
situation for the young.
on le~=ving t h e nest. D u r i n g
the period
c o n s i d e r e d (18-24 days of age) focal animals could t a k e ~ PUP
area:
their
daily
choice
Wilcoxon t e s t in
t h e way
t h a t focal
of all
pups
greatly preferred
was
desrribed
three
recorded, in
added
t h e method
of observation
f i r s t d i r e c t i o n MUM o r
up
and
sectio==.
compared
This
using
a n a l y s i s shows
experimental g r o u p {CORM, FEN and MIX g r o u p s )
to follow t h e i r m o t h e r o r to j o i n h e r in MUM area ~Table I. A).
Table I. The data r e p o r t e d in t h e t a b l e are s t a t i s t i c a l v a l u e s (T) o b t a i n e d u s i n g Wilcoxon's test. The c o n t e n t s of p a r t A are r e f e r r e d to n u m b e r of times each focal animal choose MUM o r PUP f e e d i n g area on f i r s t d a i l y e x i t from t h e nest. Part B is r e f e r r e d to f i r s t food c o n t a c t e d b y each focal animal d o r i n g t h e seven days of observation and part C to frequency of contact with M U M food in the same period. { C O M M = commercial group; FEN= fennel group; MIX= mixed group.)
GROUP
N
T value
COMH
1~
11.0
FEN
12
9.0
0.01
NIX
24
15.5
< O.OOi
COMM
12
8.5
0.01
FEN
12
2.5
0.004
~IX
24
8.0
< 0.001
COHN
12
0.0
= 0,002
FEN
12
8.0
= 0.01
Hl×
24
37.0
P
(
=
0.025
0.004
161
Furthermore for
the
the evolution
three
percentage
of this
experimental
behaviour
is s h o w n
and
every
groups
of focal animals choosing
for
in Fig day
3 which reports,
of
observation,
the
the HUH area as the first direction.
loo -
\
9O
-
a COMM m FEN MIX
.
~
7O
~ 6o ~ ~o ~
4o
L~. 3o ~
2o
0 1
2DAYS3OF
4 5 0 OBSERVATION
Fig 3. P e r c e n t a g e o f f o c a l a n l m a I z c h o o s i n 9 H U H s i d e a s f i r s t d i r e c t i o n d u r i n g t h e s e v e n d a y s o f o b s e r v a t i o n . (COHH- c o m m e r c i a l g r o u p ; FEN = f e n n e l g r o u p ; HI}(= m i x e d g r o u p . ) c) F i r s t food consumed. As f o r the p r e v i o u s D a r a ~ e t e r the 4ata w e r e analyzed as the total number o f choice.
Wilcoxon's
s i g n i f i c a n t both
times each focal animal s~!ected MUM o r PUP foo4 as f i r s t
test
shows
that
the
preference
for
HUH
food
was
when PUP and HUH foods w e r e the same (COHH g r o u p )
highly as well
as when t h e y were d i f f e r e n t (FEN and HI× g r o u p ) (Table *. B). Fig 4 r e p o r t s the p e r c e n t a g e o f pups selecting HUH food as f i r s t
choice d u r i n g
the seven days o f
observation. d) F r e q u e n c y o f c o n t a c t comparing
w i t h HUH and PUP food: the analysis was c a r r i e d out
f o r each focal animal the total number of contacts w i t h HUH food to
the total number
of contacts
observation.
analysis
only
went
prefer
The to
HUH
it ( T a b l e
contacts for every
with
food
I, C). In
HUH
food
with PUP
using a~ t h e i r
~ddition over
d a y of o b s e r v a t i o n
food recorded
Wilcoxon's test
the
first the
choice data
(see
were
total number
( F i g 5).
during
clearly
the seven
indicates
point
c)
considered
of contacts
but as with
days
tha'. pups
of not
continued
to
percentages
of
the
two foods
162
11o lOC
L~
_~ "~o ~
ao
~
70
~
6o
~
40-
~
20-
~
10-
COMM FEN
A
MIX
~so 3o-
2
.3 DAYS
4 .5 OF" O B S E R V A T I O N
6
7
Fig 4. P e r c e n t a g e of focal a n i m a l s s e l e c t i n g MUM food a s f i r s t c h o i c e d u r i n g t h e s e v e n d a y s of o b s e r v a t i o n . ~qOMM= c o m m e r c i a l g r o u p ; FEN= f e n n e l g r o u p ; MIX= mixed g r o u p . )
11o 1oo
~
®.-...
9o
COMM FEN
•
~..1q •
::I::
7o
~
6o
~-
§
5o
~
3O
MIX
4O
100
I
'> ,, "DAYS ~OF
4 5 OBSERVATION
6
7
Fig 5. P e r c e n t a g e of c o n t a c t s of f o c a l a n i m a l s w i t h MUM food o v e r t h e n u m b e r of food c o n t a c t s r e c o r d e d d u r i n g t h e s e v e n d a y s of o b s e r v a t i o n . (COMM= c o m m e r c i a l g r o u p ; FEN: f e n n e l g r o u p ; MIX= mixed g r o u p . )
total
163
Results
obtained
Student's
t
animal
the
as
percenta.ge
consumed d u r i n g
category
analysis
binary
food
choice
the
mother's
in Fig
that
a t e 60.51% o f t h e
old. therefore
already
young
didn't
show such
revealed
to
a
be
better
diet
eaten
animals
a~lalyzed
using
out
of
the
total
food
c a t e g o r i e s M~× FEN and
mothe'r's diet. (n=55,
t = 5.36,
than
t,~,e H!~
FEN
A n i m a l s o f MIX JUN
f o o d e v e n if t h e y a r e
P<0.001). T h e
youngs
(n=57, t = - 0 A 3 , n .S } fennel
to
t h e a n i m a l s o f t h e MIX
i.e. j u n i p e r .
for mother's
a preference stimulus
belong~.ng
die','. Le. f e n n e l , a n d
preference
weaned
category
were
6.
indicates
showed a strong
test
T h e d a t ~ w e r e coY2ected f o r e a c h
Mean v a l u e s o f t h e d i f f e r e n t
a t e 49.07% o i t h e m o t h e r ' s
JUN c a t e g o r y category
the of
t i m te:;t.
MIX JUN a r e r e p o r t e d The
from
f o r o n e s a m p l e (nulI. h y p o t h e s i s ) .
o n e in i n d u c t a g
Juniper a
25 d a y s
o f MiX FEN tast~ has
preferehce
in
t h e s e ar, i m a l s . ~oo N
9o
70 ~z
N=57 L=-0.48 n s
N=55 t=5.36 p<0.001
6o
~
5o
~o
4o
~ ~o 2O Z o
MIx FeN
~qtx
durJ
Fig 6. M e a n p e r c e P t ~ ' g e ( a n d s t a n d a r d e r r o r ) o f m o t h e r ' s d i e t e a t e n b y all p u p s ( f o c a l a n d t h e i r s i b l i n g s ) of MiX FEN a n d MiX JUN c a t e g o r i e s d u r i n g t h e b i n a r y c h o i c e t e s t . S t a t i s t i c a l v a l u e s a r e g i v e n in t h e f i g u r e .
164
GENERAL DISCUSSION
The s t a r t i n g h y p o t h e s i s of t h i s s t u d y was t h a t p u p s will follow t h e m o t h e r to
feeding
sites
and
there
learn
mother's
food
c h a r a c t e r i s t i c s . Not much
is
known a b o u t t h e o r i g i n a nd d e v e l o p m e n t of food p r e f e r e n c e s in mice, e x c e p t t h a t e a r l y e x p e r i e n c e with p a r t i c u l a r s u b s t a n c e s can b r i n g a b o u t forms of l e a r n i n g in l a b o r a t o r y mice (Mainardi e t al. 1976, 1982, .~985). Galef a nd
Clark (1971)
following a d u l t s " c a r a v a n i n g " has
to t h e been
mouse (Crowcroft,
maintain that
feeding sites.
youn9
rats
Th~s b e h a v i o u r ,
l e a r n w h a t is known
as
s afe by
"trailing" or
o b s e r v e d in a va~dety of s p e c i e s of animals: t h e h o u s e
1966); s h r e w s
(Crowcroft,
1957); m e e r k a t s (Ewer,
1968); wild
and d o m e s t i c a t e d r a t s (Calhoun, 1962). For t e s t i n g o u r h y p o t h e s i s
was c r e a t e d a s i t u a t i o n in which m o t h e r s an d
l i t t e r we re p u t i nt o a t e r r i t o r y with s e p a r a t e s o u r c e s of t h e same food (COHM g r o u p ) . We f u r t h e r r e i n f o r c e d t h i s s i t u a t i o n by: l) p u t t i n g an u n p a l a t a b l e f e nne l d i e t in t h e a r e a to which both m o t h e r a n d p u p s had a c c e s s , w h e r e a s we p u t t h e more p a l a t a b l e commercial d i e t in t h e t h a t a r e a only t h e p u p s could r e a c h (FEN g r o u p ) ; 2) u s i n g d i f f e r e n t u n p a l a t a b l e d i e t s for MUM a n d PUP a r e a s (MIX g r o u p ) . R e sul t s from t h e COMM g r o u p s h o w ed t h a t once t h e m o t h e r l e f t t h e n es t . he r y o u n g p r e f e r r e d
t h e a r e a in h e r company. They could e i t h e r s t a y ~n,~ oat
t h e r e , or go off to t h e o t h e r a rea,
w h e r e t h e food was e q u a l l y a p p e t i s i n g . Yet
mouse p u p s c h o s e for t h e i r f i r s t food t h a t e a t e n by t h e m o t h e r a n d continu~.d to p r e f e r it for s e v e r a l d a y s . The d e v e l o p m e n t of f e e d i n g p r e f e r e n c e s in t h e t h r e e different
groups
is
very
s i milar
day. P u p s
with
the
preference
fo r
in t h e FEN an d MIX g r o u p s
mother's
food
d e c r e a s i n g slow da y
by
also p r e f e r r e d
t h e i r m o t h e r ' s food
a nd c o n t i n u e d to do so u n t i l d ay 22 o r 23. Up u n t i l t h i s
a ge p u p s made few attemp'~s to g e t away from t h e i r m o t h e r s an d e a t t h e food on t h e o t h e r side. It is w o r t h notin~ t h a t t h i s w,~ also t r u e
when t h e food on t h e m o t h e r ' s
si de was l e s s appetizi~lg t h a n t he o t h e r . This means t h a t mice p u p s ' b e h a v i o u r is s t r o n g l y i n f l u e n c e d by
the mother's presence:
t he occasion to l e a r n t h e i d e n t i t y an d
s t a y i n g close to h e r
they have
location of food. Moreover, it has been
o b s e r v e d in o t h e r animals, s u c h as c a t s , t h a t t h e y o u n g e a t w h a t t h e i r m o t h e r e a t s . e v e n if it is an u n u s u a l food for t h e s p e c i e s ( b a n a n a s an d p o t a t o e s ) an d more s u i t a b l e food (meat) may be a v a i l a b l e (Wyrwicka, 1978). C o n s i d e r i n g t h e r e s u l t s of t h e b i n a r y choice t e s t , we can note ~.hat at d ay 25 (when rJups a r e fully weaned) th~:y m a i n t a i n t h e p r e f e r e n c e for m o t h e r ' s food in t h e c;,se s he had be e n fed on j u n 3 p e r diet. The same is not t r u e ~.Jhen m o t h e r had be~n fed on f e n n e l diet, e v e n
if als o in t h i s c a s e t h e p u p s
achieve the
165
chance level (50%). The difference between the two groups is proI~ably due to t h e fa c t t h a t j u n i p e r m i g h t be a littl~ more p a l a t a b l e flav o u r, an d a c c o r d i n g to Galef's (19??) s t a t o m e n t , for s t a b l e fc~,d p r e f e r e n c e s to be e s t a b l i s h e d in r a t s ,
the food
must
be
highly
palatable,
if
the
preference
socially
transmitted
concerns an unpalatable food, as in this case. the animal that has acquired this preference
is
prepared
to
abandon
it
when
faced
with
a
more
palatable
alte~ native. The r e s u l t s of this experiment h i g h l i g h t the fact that interactions between adults and weanlings are to be found in mice as well. I f we imagine a natural situation in which a weanling animal starts to explore its external environment, it is l i k e l y to follow i t s m o t h e r or o t h e r a d u l t s of t h e colony d u r i n g t h e i r fora.qing t r i p s . In o r d e r to s u r v i v e , a y o u n g o m n i v o r o u s animal m u s t s e l e c t a n u t r i t i o n a l l y adequate
diet
from
the
myriad
of
nutritional
and
non-nutritional
or
toxic
s u b s t a n c e s p r e s e n t in i t s e n v i r o n m e n t : following a d u l t memb ers of t h e colony as far
as
the
behaviour.
food Thus
sources, young
having
animals
the
can
chance feed
on
to l e a r n , "safe"
is
a
foods,
truly at
adaptive
l e a s t at
the
beginning. This experiment therefore, r e p r e s e n t s f o r this species a f i r s t step towards u n d e r s t a n d i n g the importance of the interaction between simple stimuli (taste and smell) and social contexts. On the o t h e r hand the social organization of the species (Crowcroft, cosmopolitan,
capable
of
1955 and 1966), rapid
environmental changes (Berry,
together
adaptation
to
with the even
quite
fact that it is considerable
1981) makes it a species p a r t i c u l a r l y
suited f o r
the s t u d y of mechanisms u n d e r l y i n g non-genetic transmission of in(ormation. Acknowledgements: The authors thank d r B.C. Ga|ef, j r . (HcHaste~ Un iv ersity. Canada) f o r his comments on this manuscript, d r P. Henozzi ( U n i v e r s i t y of Parma, Italy) f o r statistical suggestions and Hrs V. Vascelli f o r h~r technical assistance. This paper has been supported by Italian H.P.I. and C.N.R. granLs. REFERENCES CathoLic, J.B. 1962. The ecology and sociology of the norway rat. Bethesda. Haryla.~d: United States Department of Health, Education and Welfare. Crowcroft. P. 1955. Social organization in wild mouse colonies. Br. J. Anita. Beh,~;'.. 3: 36. Crowcroft, P. 1957. The life of the shrew. London: Hax Reinhardt. Crowcroft, 1". 1966. Hice all over. London: A.T. Fowlis and Co. Etver. RF. 1968. Ethology of ma¢.~mals. London: Plenum Pro~s. Galef. B.C j r . 1977. Hechanisms f o r the social transmission of acquired food preferences ~'rom adult to weanling rats. In: L.M. Baker, H.~. Best af)d H. Domjan (eds), L ~ r n i n g mechanisms in food selection. Baylor University Press, pp. 1~3-148. Galef, B.G. j i . 1988. Commu~,ication of information concerning distant diets J~= a social, central-place foraging species: Rat tus norveflicus. In: T.R. Zentall and B.G. Galef (Eds), Social learning - Psychological and Biological perspectives. Lawrence Erlbaum associates, Hillsdale, New Jersey, pp. 119-138.
166
Galef, B.G. j r . and Clark, M.H. 1971. Social factors in the poison avoidance ana feeding behaviour of wild and domesticated r a t pups. J. Cornp. Psychol., 75: 341-357. Galef, B.G. j r . a n d H e n d e r s o n , P.W. 1072. M o t h e r ' s milk: a d e t e r m i n a n t of f e e d i n g p r e f e r e n c e s of w e a n l i n g r a t p u p s . J. Comp. Physiol. Psychol., 78: 213-219. Ga]ef, B.G. j r . a nd Clark, M.M. 1972. M o t h e r ' s an d a d u l t p r e s e n c e : two f a c t o r s d e t e r m i n i n g i n i t i a l d i e t a r y s e l e c t i o n by w e a n l i n g r a t s . J. Comp. Physiol. Psychol., 2: 220-225. Galef, 5.C. j r . and Heiber, L. 1976. Role of r e s i d u a l o l f a c t o r y c u e s in t h e d e t e r m i n i n g of f e e d i n g d i e t selec'~iou a n d e x p l o r a t i o n p a t t e r n s of d o mes tic r~ts. J. Comp. Physiol. Psych., 90: 7:~7-739. Galef, B.G. jr. and Wigmore. S.W. 1983. Transfer of in~'ormation concerning distant foods: a laboratory investigation of tile "information - centre" hypothesis. Anirn. Beha:'., 3 h 748-758. Galef, B.G. jr., Wigrnore, S.W. and Kennet, D.J. 1983. A failure to fiad socially mediated taste aversion learning in N o r w a y rats (R~ nor ye£icusL J. cornp.
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