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Journal of Comparative and Physiological Psychology
1979, Vol. 93, No.2, 295--305
Investigation of the Functions of Coprophagy
in Juvenile Rats
Bennett G. Galef, Jr.
McMaster University, Hamilton, Canada
A series of experiments were undertaken to examine possible functions of the
ingestion of maternal anal excreta by juvenile rats. No strong support was
found for hypotheses suggesting (a) that maternal excreta serves as a major
transition diet from mother's milk to solid food, (b) that ingestion of maternal
excreta influences pup diet selection at weaning, or (c) that ingestion of mater-
nal excreta is a necessary condition for inoculation of pups with enteric bacte-
ria. Some support was found for the hypothesis that maternal excreta can
serve as a short-term emergency food supply for rat pups after weaning. It is
proposed that pup ingestion of maternal anal excreta may not be a functional-
ly meaningful unit of behavior in preweaning rats. Allocoprophagy may be
one facet of a broader pattern of oral exploration in which functional signifi-
cance resides.
During the 17-day period when newborn
rats are totally dependent on their dam's
milk for sustenance (Babicky, Parizek, Os-
tadalova, & Kolar, 1973), they mouth and
possibly ingest samples of most of the solid
objects with which they come in contact.
Under standard laboratory maintenance
conditions the anal excreta of the dam are
one of the substances samples of which are
frequently contacted, chewed, and appar-
ently swallowed by juvenile rats. Although
there are reports in the literature of mouth-
ing and chewing of maternal excreta by the
young of numerous mammalian species
(Ewer, 1968, p. 274), including the rat (see,
e.g., Bolles & Woods, 1964). Leon (1974)
was, to my knowledge, both the first to re-
port stomach content analyses indicating
that rat pups actually ingest maternal ex-
creta and the first to consider systematically
This research was supported by National Research
Council of Canada Grant AP-307 and a McMaster
University Research Board grant to the author. I would
like to thank Rod Pelchat, Carol Edwards, Sheelagh
Kemp, Pat Muskus, Merry Kaner, and Sue Johns for
their technical assistance, and Evelyn Thoman for re-
minding me that Experiment 5 needed to be done. The
comments of J. R. Alberts and M. M. Clark on earlier
drafts of the manuscript are gratefully acknowledged.
Requests for reprints should be sent to Bennett G.
Galef, Jr., Department of Psychology, McMaster Uni-
versity, Hamilton, Ontario, Canada L8S 4Kl.
possible functions of coprophagy in the
growth and development of young rats.
Leon suggested four possible functions of
ingestion of maternal excreta by rat pups:
(a) Ingestion of maternal excreta may inoc-
ulate young rats with maternal enteric bac-
teria which facilitate digestion of solid food
at weaning (Ewer, 1968, p. 274). (b) Ma-
ternal excreta may be utilized by weanlings
as a "baby food," an important transition
diet from mother's milk to solid foods, as
seems to be the case in koala (Minchin, cited
in Gewalt, 1972, p. 125). (c) Excreta de-
posited in or near the nest site may serve as
an emergency food supply which can sustain
weanlings in the absence of their dam. (d)
Ingestion of maternal excreta may serve to
familiarize pups with the flavor of maternal
diet and direct pups to their mother's diet at
weaning (Galef, 1977; Galef & Henderson,
1972).
Although the role of autocoprophagy (the
ingestion by an organism of its own excreta)
in the maintenance of intestinal flora and the
prevention of vitamin deficiencies in rats has
been an area of active inquiry (see, e.g.,
Barnes, 1962; Gustafsson & Fitzgerald,
1960), little information is available on the
significance of allocoprophagy (the ingestion
of the excreta of conspecifics). Hence, the
adequacy of the Leon (1974) hypotheses to
account for the phenomenon of allocopro-
Copyright 1979 by the American Psychological Association, Inc. 0021-9940/79/9302-0295$00.75
295
296
phagy in
question.
juvenile rats remains open to
BENNETT G. GALEF, JR.
Experiment 1
In the present experiment systematic
observation ofthe behavior of infant rats was
undertaken to establish the age of initiation
and the relative frequency of occurrence of
mouthing and chewing episodes directed
toward the various solid objects present in
the environment. The collection of such
des~riptiv~ dB:ta is a necessary first step in
the mvestigatIOn of hypotheses concerning
the functions of allocoprophagy. If, for ex-
ample, rat pups began to chew on solid food
prior to initiating ingestion of maternal ex-
creta, it would be difficult to maintain that
allocoprophagy is a transitional stage be-
tween nursing and ingestion of more usual
foods. Similarly, temporal precedence of
ingestion of 801id food over coprophagy
wouid render difficult the maintename of
hypo(be8es propoaing that pups use adult
ex~ as a supplementary diet when their
dams Me absent. Thus, a descriptive study
of the time of onset of ingestion of the vari-
ous solids available in the environment is a
necessary pfeCUrsor to any analytic investi-
lati0D5.
Method
Subjects. Subjects were eight recently parturient
female Long-Evans rats obtained from Canadian
Breedin« Farms (St. CQnatant, Quebec), and their lit-
ters, cldled to ei(ht pups/titter on the day of birth.
Proudure. Each mother and litter was establiahed
in
~
38 X 31 X 17 em polycarbonate cace the ftoor of
which was covered with wood chips (Beua-<:hip,
N~tem Products Corp., Warrensburg, New York)
and IIftD ad lib access to food (Purina Laboratory Chow
pellets) and w~ter. The eight litters were kept in a
soun~-att~nuatm? room on a 12:12 hr light/dark cycle.
IllummatlOn durmg the dark period was provided by
two 40- W red light bulbs suspended above the cages.
Eac~ of the eight litters was observed for .5 hr/day
durmg each of the !ight and dark portions of the cycle,
t~e observer recordmg every object mouthed by all eight
htter members.
Results
.
The results of Experiment 1 are presented
m Figure 1, which indicates the percentage
of observation periods during which one or
more members of each of the eight litters was
seeI? to mouth various objects in its cage
durmg 2 hr of observation on two consecu-
tive days. As is clear from examination of
the figures, prior to weaning, pups regularly
mouth everything available in the environ-
meJ?t-themselves, wood chips, other pups,
their dam, food pellets, mother's fecal pel-
lets, mother's cecotrophe; pup fecal pellets,
and objects not reported in the figures (i.e.,
water spouts, cage walls, etc.). These de-
scriptive categories are obviously somewhat
arbitrary in that while chewing on a wood
chip, its own foot, or its mother's tail, a pup
may actually be tasting fecal material, urine,
or cecotrophe. Further, the fact that pups
mouth an object gives no indication of
whether or not it is ingested.
In spite of their limitations, the present
observations do indicate, for example, that
~a) the range of objects mouthed by pups
m~reases with increasin~ age, (b) there is a
faIr degree of consistency in the ages at
100
Z
Q
Ii
80
~ 60
~
40
f :
~
100
--0--
SAwDuST
--9--
DRY FECES
-+-
wET FECES
-~- Pt.MI* PELLETS
(!)
z
~
~
100
---0-
PlPFECES ~ ... Ir"''''~--'''
~
80
=--:-==~s ~
~
60
~
:J
40
a.
it
20
ex>
u.
o
i
,
I
,
o
% 101"
'2/'3
141,5
'7,7 '8/'920/21 22/23
24
o.e
DAYSPOST-PARTUM
Figure 1. Percentage of eight pup litters in which
mouthin~ of various objects was observed during four
consecutive .5-hr observation periods.
FUNCTIONS OF COPROPHAGY
which different items are first introduced by
pups into their mouths (Day 1, nipples of
mother and fur of mother's ventral surface;
Days 9-11, own feet, fur of other pups, and
substrate material; Days 13-15, feces of
mother, nonventral surface of mother, and
food pellets; Days 17-21, mother's ceco-
trophe, water, and pup feces), and (c) once
mouthing of a class of objects begins it con-
tinues through the weaning period.
Discussion
The results of Experiment 1, though not
conclusive because of the difficulty of de-
termining by visual inspection whether or
not chewed samples are ingested, suggest
that ingestion of maternal excreta, particu-
larly dried fecal pellets, is an extremely
common pattern of behavior in laboratory-
maintained juvenile rats. The data, though
not sufficient to exclude any ofthe hypoth-
eses briefly described above, cast serious
doubt on interpretations of maternal fecal or
cecal material as an important transition diet
from mother's milk to solid food. Pups did
not reliably initiate chewing on maternal
excreta prior to chewing on Purina pellets,
in spite of the fact that the former objects
were far more common on the floor of the
cage than the latter.
It is, however, clear that decisive tests of
hypothesized functions of allocoprophagy
require determination of the substances ac-
tually ingested by pups of various ages.
Experiment 2 provides relevant data.
Experiment 2
To determine the substances actually in-
gested by rat pups of various ages, I directly
examined their stomach contents. The re-
sults of a series of pilot studies revealed that
pups 10 days of age were not sufficiently
mature to ingest solid foods. When 10-
day-old pups were force-fed a mash con-
sisting either of ground Purina chow and
water or ground dried excreta (deposited by
a lactating female rat) and water, it was not
possible to reliably discriminate excreta from
chow in the stomachs of pups. However,
lactating female rats fed a diet of powdered
Purina Laboratory Chow adulterated with
297
.2% by weight alcohol-soluble eosin (Telle,
1966) produced a bright orange anal excreta
(both feces and cecotrophe) which, when
dried, ground, sieved, and force-fed to pups,
was readily discriminable from powdered
Purina chow in pup stomachs. In blind ex-
periments, as little as .01 g of ground, dyed
powdered feces could be reliably detected in
pup stomachs as long as 5 hr after force-
feeding.
To determine the age of onset of ingestion
by pups of both solid food and excreta, it was
necessary to design an apparatus in which
mothers ate eosin-dyed food at a location
inaccessible to pups and pups had access to
undyed food at a site inaccessible to their
dam. Although the procedure described
below was sufficient for this purpose, it has
certain inevitable disadvantages which I
consider in discussing the results of the
present experiment.
Method
Subjects. One-hundred twenty Long- Evans rat pups
from 15 litters, culled to eight pups/litter at birth, served
as subjects.
Apparatus. A few days prior to parturition each
female was established in a .9 X .9 X .9 menclosure like
that illustrated schematically in Figure 2. The enclo-
sure was divided by a barrier, the height of which (12 in.;
30 cm) was such as to permit an adult rat, but not a ju-
venile, to cross from one side of the cage to the other.
The juveniles were invariably delivered and maintained
on the side containing a .3 X .3 X .15 m nest box, water
bottle, and pup feeder. The pup feeder was a small box
mounted on the cage wall with an entrance hole (1 in.
I
I
I
EOSIN DYED PURINA
IPOWDER
I
I
PUP FEEDER
(PlJRfNA POWDER)
Figure 2. Enclosure for feeding dams eosin-dyed food
separate from their young and young undyed food
separate from their mothers (Experiments 2 and 3).
100
(.!)
z
2
80
~2
0
U
(/)
60
I
~~40
~(/)
u.
0
::J:
20
0
298
BENNETI' G. GALEF, ,JR.
[2.54 em] in diameter) sufficiently large to permit ready
access by pups but too small for the mother to enter.
The floor of the pup feeder was kept covered with
powdered Purina chow. Daily inspection of the feeder
revealed no disturbance of the food surface until pup
footprints were found on it.
Food for the dam (powdered Purina Laboratory
Chow, adulterated 2% by weight with alcohol-soluble
eosin) was available ad lib on the far side of the barrier.
Daily inspection of the enclosure revealed no transport
of the bright orange food from one side of the enclosure
to the other. Review of periodic time-lapse videotapes
of the enclosure revealed no instance of a pup crossing
the barrier.
Procedure. Each of six dams and litters were left
undisturbed in one of six enclosures until the pups were
11 days of age. On Day 11 and every 2 days thereafter,
two pups were taken from each litter and sacrificed, and
their stomach contents were examined for the presence
of food particles and orange maternal excreta. The
remaining nine litters were treated identically to the
first six except that sacrifice of litter members was ini-
tiated on Day 19.
Results
Pups 11 or 13 days of age invariably had
stomachs containing a pure white milk curd
of rubbery consistency which could be re-
moved intact from the stomach. As can be
seen in Figure 3, no particulate matter was
f(nVt~ i.Qthe stoma~h.s of either 11- or 13-
daX<;~~ though"th~ turds from the stom-
achs of the latter animals invariably exhib-
--+-- FECES
-
...
- FOOD
~ FECES (NO FOOD GROUP)
ited a uniform very pale orange color, which
I attributed to leakage of the eosin dye into
maternal milk during the later stages of
lactation for two reasons. First, if one pup
in a litter had a pale orange stomach curd, all
pups in that litter did, and, second, these
curds contained no particulate matter at
all.
Orange particles began to appear in the
stomachs of pups at 15 days of age and were
detectable thereafter in the stomachs of
many animals. Although the present
method did not provide a means of quanti-
fying the amount of maternal excreta in-
gested by pups, the amounts found in pup
stomachs throughout the study were in-
variably small. Comparison with the
stomach contents of pups force-fed known
amounts of ground, eosin-dyed feces indi-
cated that voluntary feces intake rarely ex-
ceeded .1 g.
Greenish food particles (undyed Purina
chow) were first detected in small quantities
on Day 17, were invariable present in mod-
erate or large quantity on Day 21, and vir-
tually filled the stomach on Day 23.
In summary, our results indicated that
pups initiated ingestion of excreta prior to
feeding on Purina chow but that they in-
II
13
DAYS POST - PARTUM
r----
I
I
I
I
I
I
I
I
I
I
/
I
I
I
I
I
I
I
I
I
-"
~-
15 17
19
21
23
Fi#ure .5. Percentage of pup stomachs observed to contain particles of Purina chow or maternai excreta
as a function of pup age (Experiments 2 and 3).
FUNCTIONS OF COPROPHAGY
299
gested very little of the former material and
increasing amounts of the latter.
Discussion
The results of the present experiment do
not provide support for the suggestion that
in the rat, mothers' excreta serve as a major
transition diet from milk to solid food. We
could find no case in which a significant
portion of a pup's stomach contents con-
sisted of maternal excreta.
The data do offer limited support for the
hypothesis that ingestion of maternal ex-
creta is necessary to inoculate juveniles with
enteric bacteria which facilitate digestion of
solid food. Small quantities of excreta were
observed in the stomachs of many pups in
the absence of particles of Purina chow, but
Purina chow was rarely observed in the ab-
sence of feces prior to Day 21 when the pups
had weaned. These observations are con-
sistent with the hypothesis that ingestion of
small quantities of excreta precedes inges-
tion of solid food and that such ingestion of
maternal excreta may be a necessary condi-
tion for the transmission of specific enteric
bacteria to juveniles, facilitating their in-
gestion of solid food. It should, however, be
kept in mind that the relative age of onset of
allocoprophagy and ingestion of solid food
found in the present experiment may well be
specific to the experimental situation em-
ployed. My co-workers and I (Galef, 1971;
Galef & Clark, 1972) hav03previously found
that age of onset of weaning in rats is af-
fected by such variables as distance from the
nest to the feeding site and the presence or
absence of conspecifics at the feeding site.
In the present experiment, pups and dam
were prevented from exploiting a common
food source, and one would expect an arti-
factual delay in the weaning of the pups to
solid food.
In addition, there are several reasons for
questioning the necessity of explicit inges-
tion of maternal excreta for the development
of a functional gastrointestinal flora in the
rat. First, even pups reared artificially
(without any direct contact with conspecifics
or their excreta) exhibit normal growth fol-
lowing weaning to standard laboratory diets
(Hall, 1975; Thoman & Arnold, 1968). AI-
though it is impossible, in the absence of
bacteriological examination of the gut flora
of weaned, artificially reared pups, to know
if such animals have a normal enteric popu-
lation, they certainly possess an intestinal
flora both acquired without direct contact
with conspecifics or their excreta and ade-
quate for normal growth in some environ-
ments.
Second, available evidence strongly
suggests that although most of the organisms
colonizing the alimentary tract of the neo-
nate probably derive from the anal excreta
of the dam (Smith, 1965a), active ingestion
of feces is not a necessary condition for pup
inoculation with a normal bacterial flora.
The infant rat, sterile at birth, has a rich
bacterial flora as early as 24 hr following
birth, when the pup is insufficiently mature
to locate and chew maternal feces. Strep-
tococci, lactobacilli, and E. coli are all
present in the gastrointestinal tract of young
rats within 72 hr of birth (Raibaud, Dickin-
son, Sacquet, Charlier, & Mocquot, 1966;
Smith, 1965a). Bacteriodes and Clostridi-
um welchii are, respectively, first observed
in the rat gut between Day 4 and Day 10 and
at 18 days neonatally and might enter the
gut as the result of allocoprophagy by.pups.
However, the fact that both Bacteroides and
C. welchii invade the gut of a number of
other altricial species (e.g., man and cat) on
the day of birth (Smith & Crabb, 1961)
suggests that these bacteria may also be
transmitted from dam to young without ex-
plicit ingestion of excreta by the infant. The
fact that C. welchii are not found in the ex-
creta of the dam (Smith, 1965a) and that the
ability of C. welchii to successfully colonize
the rat alimentary tract is largely dependent
on the diet of the host (Smith, 1965b)
suggests that the appearance of C. welchii in
the gut is the result of weaning from moth-
er's milk to solid food on Day 18 and not pup
ingestion of anal excreta. The evidence re-
garding the role of allocoprophagy in pup
inoculation with Bacteroides is less clear, but
the fact that some infant rats are colonized
by Bacteroides as early as Day 4 (Smith,
1965a) again suggests that explicit copro-
phagy is not a critical factor in inoculation.
In general, the literature does not provide
strong support for the view that allocopro-
300 BENNE'IT G. GALEF, JR.
phagy functions to inoculate young rats with Experiment 3, lacking access to s.olid fo.od
maternal enteric bacteria. rations, invariably had stomachs fIlled wIth
orange particles.
Experiment 3
In discussing the results of Experiment 2
with Leon, it became clear that the data
which he collected on the ingestion of ma-
ternal excreta by weaning rat pups was at
variance with our own. Leon (1974) found
substantial quantities of maternal excreta in
the guts of 93% of the 20-day-old pups he
examined, whereas I found only traces of
maternal excreta in less than 80% of the pups
I examined at the same age (Day 21 in my
system). Consideration of differences be-
tween Leon's experimental design and my
own revealed that although they were very
similar there was a major difference in the
access to food provided pups. In Leon's
study, pups had no possible source of food
other than maternal milk or excreta, whereas
in Experiment 2 above they could ingest
milk, maternal excreta, or Purina chow.
If the failure of pups in Experiment 2 to
ingest large quantities of maternal excreta
resulted from the availability of other solid
food then one would expect pups to ingest
larg~ quantities of mat~rnal excreta if no
other foods were available to them. The
present experiment, which examines th~
possibility, bears directly on the hypothesIs
that maternal excreta may serve as an
emergency food ration for weanlings.
Method
Subjects. Subjects were eight litters of Long-Evans
rat pups born in the McMaster colony and culIed to
eight pups/litter on the day of birth.
Procedure. The procedure was identical to that of
Experiment 2 except no food was present in the pup
feeder and sacrifice of pups was initiated in half of the
litters at Day 13 and in half at Day 23.
Results
As can be seen in Figure 3, pups without
food available initiated ingestion of maternal
excreta at about the same time as those with
food available. Stomach content analyses
revealed small quantities of orange granules
in the stomachs of a steadily increasing
proportion of pups on Days 13, 15, and 17.
However, on Day 21 and thereafter, pups in
Discussion
The results of the present experiment
strongly suggest that rat pups make us~ of
maternal excreta as an emergency ratIOn
when mother's milk ceases to be a source of
adequate nutrition and no other food .is
available to them. If, as was the case In
Experiment 2, adequate foo~ is available in
the vicinity of the nest, pups mgest that food
in preference to maternal excreta. These
data support the hypothesis that maternal
excreta is available to the young as an
emergency ration in the event that no f?Od
is to be found in the environment at the tIme
of compulsory weaning.
Experiment 4
The results of Experiments 1 and 2 indi-
cate that pups initiate ingestion of maternal
excreta well before weaning occurs. The
results of Experiment 2 further indicate that
so long as mother's milk or regular food is
available to pups in adequate quantity, they
ingest only small quantities of maternal ex-
creta. In the present experiment, I exam-
ined the effects of removal of the dam and
food on the ingestion of maternal excreta by
pups of various ages to determine the .r~ge
of ages at which pups are capable of utl.hzu!,g
maternal excreta as an emergency ratIOn m
the absence of alternative rations.
Method
Subjects. Subjects were 18 litters of Long-Evans rat
pups, culIed to eight pups!Iitter on the day of birth.
Procedure. Six litters of pups were examined at each
ofthree ages (Days 16, 19, and 23) to determine the ef-
fects of both maternal and food deprivation on ingestion
of maternal excreta. Each litter of pups was randomly
divided into two groups of four pups/group, and each
group was placed together in a polycarbonate cage (37
X 31 X 17 cm) with wood chip bedding and a water
source. Pups assigned to the Excreta condition were
given very large rations of fresh maternal excreta (both
feces and cecotrophe) at the time they were removed
from their dam and every 12 hr thereafter. Pups in the
Deprivation condition were treated identically to t~ose
in the Excreta condition except that they were not gIven
access to maternal excreta. Each pup was weighed at
FUNCTIONS OF COPROPHAGY
301
the time of removal from its dam, and 24 and 48 hr
thereafter. To assure independence of groups, I treated
the mean weight loss of each group of four pups as a
single data point in calculating means and standard
errors.
Results and Discussion
The main results of Experiment 4 are
presented in Figure 4 which shows the mean
weight loss of pups in Excreta and Depriva-
tion conditions following 24 and 48 hr of
isolation from their dam. As is clear from
examination of the figure, weight loss over a
48-hr period, but not a 24-hr one, was sig-
nificantly reduced in 19- and 22-day-old
pups by the presence of maternal excreta in
their cages. The presence of maternal ex-
creta had no comparable effect on pups 16
days of age at the onset of testing. Thus,
pups of postweaning age are able to utilize
maternal excreta as an emergency food
supplement in the absence both of their dam
and of other rations, but pups of preweaning
age are not.
Of course, the fact that young rats ingest
maternal excreta in the absence of their more
usual sources of nutrition does not mean that
8
.-....
0")
-
6
5
2
7
4
3
such coprophagy provides a meaningful
source of nutrients. However, in an exper-
iment in which the longevity of seven 22-
day-old rat pups left in a clean cage with ad
lib water was compared with that of seven of
their littermates left in cages provisioned
with maternal excreta and water, it was
found that although all pups succumbed
within 24 hr of one another, the latter ani-
mals lived significantly longer than the for-
mer (Mann-Whitney U = 1,P < .001), which
indicates that mothers' excreta is a partially
adequate diet.
Although allocoprophagy may postpone
death, its long-term value is not clear. The
situation in which the pups in the present
experiment were examined is, of course, far
removed from that experienced in the nat-
ural environment. In particular, the pups
in our study were prevented from dispersing
from a location in which the only available
food was inadequate for long-term survival.
It might be argued that following prolonged
absence of the dam, weanling pups in a nest
site lacking food would be better advised to
disperse from the nest site in search of ade-
quate rations than to remain in the natal site
48hr
24hr
DEPRIVATION
GROUP
EXCRETA
GROUP
16 19 22
AGE AT ONSET OF TESTING(DAYS)
Fiuure 4. Mean weight loss by pups following 24 and 48 hr of isolation from the dam, in the presence
or absence of maternal excreta.
302 BENNETI' G. GALEF, JR.
feeding on an inadequate diet. Humans lost
in the wilderness are advised not to linger in
locl;lls in which inadequate food is available
in that further movement is necessary and
the greater the period of subsistence on an
inadequate diet the less the energy reserves
available for further exploration (Angier,
1962, p. 52). By analogy, the utilization by
rat pups of maternal excreta as an emergency
ration, while providing some short-term
benefit, might not, in the long run, be a use-
ful strategy for weanling pups in the absence
of both their dam and conventional foods.
Experiment 5
The final hypothesis to be examined
suggests that the ingestion of maternal ex-
creta by pups serves as a mechanism for the
transmission of food preferences from a dam
to her offspring. The results of studies in a
number of laboratories (Bronstein, Levine,
& Marcus, 1975; Capretta & Rawls, 1974;
Galef & Clark, 1972; Galef & Henderson,
1972) indicate that at weaning, rat pups ex-
hibit enhanced intake of the diet of their
dam, and it i~ possible that allocoprophagy
by the pups function to introduce the young
to undigested particles of diet in the excreta
of their dam. In a series of studies under-
taken to determine the means by which pups
become familiar with their mother's diet,
Henderson and I (1972) found evidence of
flavor cues in mothers' milk (see also Galef
& Sherry, 1973) but found no evidence that
pup ingestion of feces played a role in the
transmission of food preferences from
mother to young.
The results of studies published after
Henderson and I completed our work (Leon,
1974) suggest that our experiments may not
have been an adequate test of the hypothesis
that maternal excreta is utilized by pups to
determine their food choice at weaning
(Galef, 1977). Leon presented data indi-
cating the following: (a) Lactating female
rats deposit two types of anal excreta, feces
and cecotrophe, and virgin female rats re-
ingest the latter and deposit only the former.
(b) Feces is less attractive to rat pups of
weaning age than cecotrophe. (c) Some
maternal diets, among them one of the diets
Henderson and I used, do not permit syn-
thesis of attractive cecotrophe by lactating
females of some strains (Galef & Heiber,
1976), and (d) food-deprived lactating fe-
males exhibit reduced cecotrophe deposi-
tion. All four of these findings cast some
doubt on the adequacy of the experiments
Henderson and I carried out to test the hy-
pothesis that flavor cues in maternal excreta
influence pup diet choice at weaning. The
present experiment was undertaken to cor-
rect the methodological deficiencies of Galef
and Henderson (1972).
Method.
Subjects. Subjects were 16 pregnant Long-Evans
rats obtained from Canadian Breeding Farms. Eight
females and their litters, culled to six pups!litter on the
day of birth, were assigned to experimental groups, and
eight were used as sources of excreta.
Maintenance apparatus. Each female assigned to
serve as an experimental animal was placed in a stan-
dard plastic laboratory cage (37 X 31 X 17 em) with ad
lib access to water. Each female assigned to serve as a
source of excreta was placed in a modified standard
laboratory cage like that depicted in overhead schematic
in Figure 5 and was maintained on ad lib food and water.
A modified laboratory cage containing a source animal
and her litter was suspended above each standard lab-
oratory cage containing an experimental animal and her
litter. Two thirds of the bottom of each modified cage
was removed and replaced with hardware cloth (1.2 X
2.5 em) to permit excreta to fall to the cage below it.
The hardware-cloth-floored section of each source fe-
male's cage was separated from the remaining one third
of her cage by a sealed transparent partition. Entrance
to the third of the cage behind the partition was through
a single 5-cm-diam. hole. A nesting area of aluminum
sheet metal (10 X 10 X 17 em) and a food source were
located behind the partition.
Testing apparatus. The apparatus used to deter-
mine the food preferences of individual pups, described
5O!RCE
FEMALE AND UTTER
WIRE MESH
Figure 5. Overhead schematic view of the modified
standard laboratory cage containing a source-group
female and litter in Experiment 4. (This cage was
suspended directly above a standard laboratory cage
containing an experimental group female and litter.)
100
0
80
Q
x
~G
60
UIJ)
1J)n.
n.......
......+
~40
0>
Z
«
w
~20
FUNCTIONS OF COPROPHAGY
30~
in detail in Galef and Henderson (1972), consisted of a
plastic dish (22 cm in diameter, 6.6 cm deep) with two
detachable food cups mounted 1800 apart on its exte-
rior. Water was available throughout testing in a
shallow bowl placed in the center of the apparatus.
Intake of diet from each food cup was determined by
weighing.
Procedure. Three to four days prior to parturition,
each female was assigned one of two maintenance diets
and was given ad lib access to either powdered Purina
Laboratory Chow (Diet P) or a powdered diet whose
main constituents were potato starch and casein (Diet
PSC).l Both diets are known to allow dams to syn-
thesize cecotrophe highly attractive to young rats (Leon,
1974). On the day of parturition each female was as-
signed to either an experimental or a source cage. To
ensure that pups born to experimental females ingested
solid food for the first time when tested for theirJood
preference in the test apparatus, each experimental
female was fed for 3 hr/day (9-10 a.m., 3-4 p.m., 10-11
p.m.) in a cage separate from her young on the diet on
which she had been maintained prior to parturition.
Each female serving as a source of excreta was paired
with an experimental female whose time of parturition
was within 24 hr of her own and was provided ad lib
access in her home cage to the diet on which she had
been maintained prior to parturition.
Pups in experimental litters were reared in one Of
three conditions: (a) Both their dam and the dam
overhead were eating Purina Laboratory Chow (P/P),
(b) both darns were eating the potato-starch-casein diet
(PSC/PSC), or (c) the dam overhead was eating Purina
Laboratory Chow while the dam of experimental pups
was eating the potato-starch-casein diet (P/PSC).
Cages containing source females were examined daily
and were cleaned if any spillage was detected in the
feeding area. Source mothers invariably kept their
young in the nesting area and kept the area behind the
partition relatively free of anal excreta, more than 90%
of which fell to the cage below.
Testing was initiated when experimental pups were
21 days of age. Each experimental pup was placed in-
dividually in a test apparatus and was offered the choice
of Diet P and Diet PSC. Intake of each diet was de-
termined 3, 6, 12, and 24 hr follo~g placement of a pup
in the test apparatus.
Results and Discussion
I expected on the basis of previous work
that pups in Groups PIP and PSCIPSC
would exhibit a preference for the diet of
their dam and the source female living above
them. As can be seen in Figure 6, which ip-
dicates the amount of Diet PSC ingested by
pups in Groups PIP and PSCIPSC as a per-
centage of total intake, my expectations were
confirmed. Pups exposed to females eating
Diet PSC ingested a considerably greater
percentage of that diet during the test period
than did pups exposed to females eating
Diet P.
-0-
(PSC)/(PSC) (3 LITTERS)
-tJ-
(PJI(P) (2 UTTERS)
-Q- (P)/(PSC) (3 LITTERS)
0-3
3-6
HOURS OF TESTING
Figure 6. Amount of Diet PSC eaten by experimental
group pups during 24-hr testing as a percentage of total
intake. '
I expected that if pups were influenced in
their choice of diet at weaning by maternal
excreta, then pups in Group P IPSC, which
were exposed to the excreta of a lactating
female eating Diet P during ontogeny, would
exhibit less of a preference for Diet PSC
during testing than pups in Group PSCIPSC
which lacked such exposure. As can also be
seen in Figure 6, pups in Group P IPSC did
not exhibit any effect of exposure to the ex-
creta of source females eating Diet P. The
feeding preference of pups in Group P IPSC
was not different from that of pups in Group
PSCIPSC.
The results of the present experiment
confirm those found previously (Galef &
Henderson, 1972) and do not offer support
for hypotheses implicating exposure to ma-
ternal excreta in the determination of pup
feeding preferences at weaning. It might, of
course, be argued that the reason why pups
in Group P IPSC failed to exhibit any effect
of exposure to the excreta of females eating
Diet P is that pups in Group P IPSC did not
ingest any of the excreta from the female
eating Diet P and therefore the present ex-
1
Diet PSC was compounded (in g/kg) of 584.5
g
of
potato starch, 211 g of casein, 104.5
g of cellulose, 50.0
g of corn oil, 40.0 g of salt mix VSP XIV, and 10.0 g of
Vitamin Fortification Mix.
304 BENNETT G. GALEF, JR.
periment does not adequately test the hy- orally explore their environment and, per-
pothesis. It should be kept in mind that the haps, learn the adequacy of various sub-
question addressed in the present experi- stances as dietary constituents before serious
ment was not whether pups could utilize weaning begins. In support of the latter
information in maternal excreta ifforced to view, the data presented in Figure 1 indicate
do so but rather whether they would utilize that sawdust is the substance first and most
such information if allowed to do so. The frequently mouthed by pups 8 to 19 days of
results of the present experiment suggest age. Perhaps sawdust chewing is in itself
that the answer to the latter question is functional, perhaps not. Similarly, alloco-
negative, but they provide no evidence prophagy by young rats may be a functional
bearing on the former. unit of behavior, or it may be one aspect of
a broader pattern of oral exploration in
which functional significance resides. The
present studies fail to provide strong evi-
dence supporting the former view.
General Discussion
The results of the present series of ex-
periments are in a sense disappointing. The
hypotheses under study concerning the
function of allocoprophagy in young rats
seemed at the outset readily testable and
likely to be confirmed. However, the ex-
periments and literature review presented
above offer support only for the view that
ingestion of mothers' excreta may serveas a
short-term emergency diet when weaned
pups are starving and no other food is
available. Such data does little to explain
the frequent gnawing of maternal feces to be
observed in 12. to 18-day-old pups which are
both adequately maintained by their dams
and have access to an adequate diet of solid
food.
There seem to me to remain two possible
classes of answer to the question of the
function of allocoprophagy in preweaning
rats. First, future studies may reveal some
as yet unknown benefits accruing to pups
from the ingestion of their dam's excreta. In
particular, it is possible that bacteriological
investigations, beyond the capacity of our
laboratory to perform, might reveal an im-
poverished intestinal flora in rats reared
without access to maternal excreta, which
would leave pups vulnerable to diets defi-
cient in specific vitamins (Barnes, 1962).
Alternatively, it is possible that the question
What is the function of allocoprophagy in
weanling rats? is unanswerable in that form.
Nibbling on and ingestion of maternal ex-
creta by young rats may not be the appro-
priate unit of behavior in which to seek
functional significance. It is possible that
allocoprophagy may simply be one expres-
sion of a general tendency of young rats to
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