ISSN 0889-3667
IJCPB 7(1)1-43(1994)
IISICIP
INTERNATIONAL JOURNAL OF
COMPARATIVE
PSYCHOLOGY
Published by
The International Society
for
Comparative Psychology
VOLUME?, NUMBER 1
EDITOR
Robert N. Hughes
Dept. of Psychology
University of Canterbury, PB 4800
Christchurch, New Zealand
ASSOCIATE EDITOR
Nancy K. Innis
Dept. of Psychology
University of Western Ontario
London, Ontario, N6A 5C2 Canada
MANAGING EDITOR
Sally A. McFadden
Dept. of Psychology
The University of Newcastle
Newcastle, NSW 2308 Australia
EDITORIAL ADVISORY BOARD
Ruben Ardila
University of Columbia
Apartado 88754
Bogota Colombia S.A.
M. Balakrishnan
University of Kerala
Kariavattom 695581
Trivandrum, India
Abelardo Brenes
University of Costa Rica
San Jose, Costa Rica
David Croft
University of NSW
PO Box 1, Kensington NSW
2033, Australia
J.D. Delius
Allgemeine Psychologie
Universitat Konstanz
D-78434 Konstanz 1
Germany
Gary Greenberg
Dept. of Psychology
Wichita State University
Wichita, Kansas
67260-0034 USA
S. Koref-Santibanez
Museum f. Naturkunde
43 Invalidenstras.se
Berlin 104, Germany
Kiyoko Murofushi
Ritsumeikan University
56-1 Toujin-kita machi
Kyoto City, 603 Japan
Anthony Nijssen
Universitiet Van
Amsterdam
Post bus 20218
Amsterdam, HE 1000
The Netherlands
Marco Poli
University of Milan
Via Francesco Sforza 23
Milan, 20122 Italy
J. Martin Ramirez
Universidad Complutense
Madrid
Enrique Larreta 10
Madrid, 28036 Spain
A.F. Semiokhina
Moscow State University
Moscow, 119899 Rus.sia
L.C. Simbayi
Dept. of Psychology
University of Port Elizabeth
PO Box 1600
Port Elizabeth 6000
Republic of South Africa
Joseph Terkel
Dept. of Zoology
University of Tel Aviv
Ramat Aviv
Tel Aviv 69978 Israel
Ethel Tobach
American Mu.seum of
Natural History
Central Park West at 79th St
New York, New York
10024-5192 USA
Charles W. Tolman
University of Victoria
P.O. Box 1700
Victoria British Columbia
Canada V8W 2Y2
D.F. Ventura
Instituto de Psicologia
University de Sao Paulo
Cx. Postal, Sao Paulo
Brazil SP
Jiao Shao
Dept. of Psychology
Peking University
Beijing 100871 China
INTERNATIONAL JOURNAL
OF COMPARATIVE PSYCHOLOGY
Volume 7, Number 1, 1994
ARTICLES
Flavour-Meal Size Conditioning in the Rat (Rattus norvegicus):
Failure to Confirm Some Earlier Findings 1
Leickness Chisamu Simbayi
Light Mediation of Circadian Predatory Behavior in the
Young Alligator 27
Jack A. Palmer and Linda K. Palmer
Portia labiata, a Cannibalistic Jumping Spider,
Discriminates Between Own and Foreign Eggsacs 38
Robert J. Clark and Robert R. Jackson
INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY is sponsored
by the International Society for Comparative Psychology, an affiliate of the International
Union of Psychological Sciences. In consonance with the goals and activities of the
Society, it publishes reports of studies in the evolution and development of behavior of
all species; on the use of the comparative method for the understanding of behavioral
processes; and the examination of the adequacy of psychological and evolutionary
theories. It accepts articles that deal with historical and contemporary relationships
between humans and other animals; that elucidate problems of ecological and behavioral
processes in resource management; that explicate fundamental concepts about human
evolution; and that present research results and develop theories about the development
and evolution of behavior. Articles on the contemporary and historical organization of
knowledge about comparative psychology; promoting public education on the evolution
and development of behavior; and about the training of students in comparative
psychology are also invited. Book reviews; letters discussing published articles with
replies by authors; notices of new books, journals, meetings and competitions or other
matters of interest to the readers will be published at the discretion of the editors. The
Editor, Associate Editor and Managing Editor are elected by the Operations Committee
of the Society. The Editorial Advisory Board is appointed by the Editors and the
Operations Committee.
MANUSCRIPTS should be submitted in triplicate to Robert Hughes, Editor. See inside
back cover for style requirements.
SUBSCRIPTION inquiries and subscription orders to institutions and individuals who
are not Society members should be addressed to International Society for Comparative
Psychology, P.O. Box 1897, Lawrence, KS 66044-8897, USA, Telephone 913-843-1221,
or Fax 913-843-1274. Subscription inquiries and subscription orders for Society
members should be addressed to Sally McFadden, Managing Editor (E-mail address:
McFadden@psychology.newcastle.edu.au or Fax 61 49 216980).
Subscription rates:
Volume 7, 1994 (4 issues) $95.00 (outside the U.S., $110.00). Members of the
International Society for Comparative Psychology receive their yearly subscription as
part of their membership dues. For membership information see back pages.
INDEXED OR ABSTRACTED IN: Psychological Abstracts.
PHOTOCOPYING: Authorizations to photocopy items for internal and personal use
of specified clients is granted by the International Society for Comparative Psychology
for users registered with the Copyright Clearance Center (CCC) Transactional Reporting
Service, provided that the flat fee of $6.50 per copy per article (no additional per-page
fees) is paid directly to CCC, 27 Congress St., Salem, MA 01970. For those
organizations which have been granted a photocopy license by CCC, a separate system
of payment has been arranged. The fee code for users of the Transactional Reporting
Service is: 0889-3667/9 1/$6.50.
COPYRIGHT 1994 by the International Society for Comparative Psychology.
Published quarterly.
ISSN 0889-3667 IJCPE8 7( 1 ) 1 -43( 1 994)
International Journal of Comparative Psychology, Vol. 7, No. 1, 1994
FLAVOUR-MEAL SIZE CONDITIONING IN THE
RAT (RATTUS NORVEGICUS): FAILURE TO
CONFIRM SOME EARLIER FINDINGS
Leickness Chisamu Simbayi
University of Port Elizabeth
ABSTRACT: A series of experiments was carried out in order to explore further the
possibility that hungry rats, both mature and weanling, might learn to associate flavours
with different sizes of meals made from the same diet. The general procedure used
involved providing rats with either a large meal (e.g. 5 gm). usually consisting of wet
mash with an added flavour such as anise, or a small meal (e.g. 1 gm) of the same diet
with a second flavour such as vanilla added, on alternate days. Following a number of
such discrimination training days, subjects were given a two-jar extinction choice test
to assess their relative preferences for the two flavours. It was originally anticipated that
rats would come to prefer the flavour associated with the larger meal (i.e., conditioned
appetite), because the larger meal provided more calories. However, this result was
never obtained. When a significant preference was acquired, this was for the flavour of
the small meal instead, (i.e. conditioned satiety). The conditioned effects not only
extinguished very rapidly but were also rather elusive at times. It is thought that the
observed conditioned satiety effects were probably due to flavour-calorie rather than
flavour-flavour associations.
A central theme in a number of current theories of food intake
control is the idea that omnivores such as rats or human beings regulate
their food intake on a short-term basis, that is, within a meal, by
associating the caloric consequences of ingestion with the flavour of
foods (e.g., Booth, 1985; Deutsch, 1987; Le Magnen, 1987). This
phenomenon which is known as conditioned satiety is considered to be
very important because it means that the omnivores do not necessarily
have to wait until they have actually experienced the delayed results of
digestion, namely, calories, before they terminate feeding. They can
instead simply rely on their previous experience with familiar flavours
Address correspondence to Leickness Simbayi. Psychology Department, University
of Port Elizabeth, P.O. Box 1600, Port Elizabeth 6000, South Africa.
© 1994 International Society for Comparative Psychology 1
2 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
as cues for satiety. Accordingly, inability to make such associations may
be responsible for inducing some pressing human problems such as
obesity (Booth & Mather, 1978), alcoholism (Deems, Getting, Sherman
& Garcia, 1986) and drug withdrawal problems (Le Magnen,
Marfaing-Jallat & Miceli, 1980).
A complementary process known as conditioned appetite which also
involves learning about flavour-food relationships has been implicated
as a food selection mechanism on a more long term basis whereby
omnivores choose their food after learning about the caloric values of
different foods (Bolles, 1983; Bolles, Hay ward & Crandall, 1981;
Hay ward, 1983; Mehiel & Bolles, 1984; Rozin, 1977). It is thought that
rats are perhaps adept at learning about both of these types of
conditioned preferences in much the same way as they acquire
conditioned taste aversion (CTA) learning or bait shyness. In contrast
to the very considerable and unequivocal evidence for CTA learning in
rats which has been accumulated over the past three decades or so of
research (see Riley & Tuck, 1985), evidence for positive conditioned
flavour preferences, which include both conditioned satiety and
conditioned appetite, is relatively less strong and unconvincing. This
seems rather surprising in view of the fact that the idea of the
involvement of such learning mechanisms in the regulation of feeding
behaviour was originally proposed as early as 1955 by Le Magnen (see
Le Magnen, 1969).
Although there is mounting evidence in support of the idea that rats
are capable of learning about positive flavour preferences (e.g., Boakes
& Lubart, 1988; Boakes, Rossi- Amaud & Garcia-Hoz, 1987; Capaldi,
Campbell, Sheffer & Bradford, 1987; Simbayi, 1987; Simbayi, Boakes
& Burton, 1986) most of the evidence demonstrated conditioned appetite
rather than conditioned satiety. It is interesting to note here that most
of these studies had employed fluids such as glucose, saccharin and
ethanol rather than solid food as reinforcers. In contrast, a relatively
small number of studies have also demonstrated conditioned flavour
preferences using solid food in other animals such as humans (e.g.,
Booth, Lee & McAleavey, 1976; Booth, Mather & Fuller, 1982) and
chicks (e.g., see Capretta, 1961; Hogan, 1977, 1980). These studies
could be considered more informative about conditioned preferences than
those that used fluids as reinforcers, because most of the food of
omnivores is in solid rather than liquid form.
The fact that the experimental demonstration of conditioned satiety
has proved to be rather elusive has been hitherto acknowledged by Smith
and Gibbs (1979). According to them, only two studies, one by Booth
(1972) and the other by Booth and Davis (1973), had successfully
LEICKNESS C. SIMBAYI 3
demonstrated conditioned satiety learning in rats. In his initial study,
Booth (1972) found evidence for the ability of flavours to elicit
conditioned satiety in rats. In this research, flavours were paired with
high or low calorie diets during training and presented to the rats one at
a time. During testing, when the two flavours were presented one at a
time in isocaloric diets, the "low calorie" flavour was preferred more
than the "high calorie" flavour. However, in a two stimulus preference
test in which the flavours were presented simultaneously in isocaloric
diets, the high-calorie flavour was preferred more than the low calorie
flavour. This latter result demonstrated conditioned appetite. Similar
findings have also been reported by Booth and Davis (1973). However,
similar studies carried out by Bolles et al. (1981) and Hay ward (1983)
were only able to demonstrate conditioned appetite but not conditioned
satiety. Perhaps even more interesting was Hayward's findings which
also showed that young rats were capable of more diverse learning than
adult rats.
The experiments reported in the present paper were undertaken in an
attempt to explore further the positive conditioned flavour preference
effects reported by Booth (1972), Bolles et al. (1981) and Hay ward
(1983) using wet solid food as a reinforcer. To test the validity of
Haywood's (1983) developmental finding, conditioned flavour
preferences were investigated in adult rats in Experiments 1, 2 and 4,
and in rat pups in Experiment 3.
EXPERIMENT 1
This experiment was a partial replication of experiments carried out
by Bolles et al. (1981), except for the following changes:
a) The ratio of meal sizes was increased to 5:1 instead of 2:1. It was
hoped that the ratio increment would serve to make the meal sizes
more easily discriminable.
b) To prevent rats from learning to anticipate or predict specific
flavours during each subsequent training day, semi random
presentations of flavour-meal size correlations replaced the
alternating presentations every other day adopted by Bolles et al
(1981).
c) Control groups were added for which supplementary food (wet mash
of standard laboratory chow) was made available 15 min after the
4 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
presentation of small meals. These control groups were somewhat
similar to the Oral Group used in Bolles et al.'s (1981) Experiment
4 and were meant to equate the total caloric consequences of both
meal sizes and thereby controlling for any possible confounding
effects of differential hunger.
Basically, rats were given experience with two meal sizes of the
same diet, each of which was marked by a distinctive flavour (anise oil
or vanilla). Thus, the two distinctive flavours were correlated with the
same pattern of oral cues and caloric density but different caloric
consequences: that is, large meals yielded more calories than smaller
ones. The conditioning of flavour preferences was assessed by the
degree to which the animals tracked the flavours in an extinction choice
test when they were no longer correlated with meal size.
METHOD
Animals
Twenty male hooded Lister rats were obtained from Sussex University's
Laboratory of Experimental psychology breeding colony. They had been
used previously in a food neophobia experiment but had no experience
with either the reinforcer or flavours used in the present experiment.
The rats were fed for only 2 h each day beginning at 1500 hrs and were
food deprived for the rest of the day except for 30 - 60 mins beginning
at 1000 hrs each morning when training or testing was conducted. More
importantly, the animals also had some previous experience with feeding
from jars and their mean consumption time for 5 gm of wet unflavoured
mash was about 5 min. The average age and weight of the rats at the
beginning of the experiment were 100 days and 250 gm respectively.
Materials
The experimental flavours, which were added to the chow diets,
were made by adding 0.5 ml anise oil (Sigma London Chemical
Company Limited, Poole, Dorset, England) and 2.0 ml vanilla (E.F.
Langdale Ltd., New Addington, Surrey, England) extracts to 100 ml
water. These flavour concentrations were chosen following a titration
experiment which tested for sensitivity of rats to flavours relying on food
neophobia as the dependent variable. Both the conditioning and testing
diets consisted entirely of standard laboratory chow (Spratt's Expanded
LEICKNESS C. SIMBAYI 5
Rodent Diet, Spiller's Limited, Newmarket, Suffolk, England) to which
some water was added and yielded about 2 cal/gm.
All conditioning and testing was carried out in the animals' home
cages where both the conditioning and testing diets were presented in
feeding jars with holes in the lids large enough for the rats to insert their
heads in order to reach the food. During testing the jars were attached
in pairs to prevent rats from altering the position of each jar relative to
the other. In addition, the pairing arrangement also made it possible to
effectively counterbalance for any positional biases.
Experimental design
A 2 X 2 factorial design was used with large meal flavours (anise vs.
vanilla) and supplementation (whether or not the animal had received
supplementary food on small meal days during conditioning) as factors.
The experiment had two major phases during which conditions were
reversed. For each subject the treatments in each phase were identical
except that the relation between flavour and meal size was reversed.
Each phase consisted of two 8-day conditioning cycles, each of which
were followed by a single test day. Finally, a 5-day interval separated
the two phases during which no flavours were presented and the same
food deprivation schedule as used in the actual experiment was also
maintained.
Procedure
Conditioning involved presenting flavour-meal size correlations for
blocks of 8 days in semi random order, that is, a total of 4 days with
each flavour. The animals were randomly assigned to four equal groups
(n = 5) namely. Groups V, VS, A and AS. Groups V and VS were
presented with a large meal (5 gm) flavoured with 2.0 % vanilla on
some days and a small meal (1 gm) flavoured with 0.5 % anise oil on
other days. On the other hand. Groups A and AS were both presented
with a large meal (5 gm) flavoured with 0.5 % anise oil on some days
and a small meal (1 gm) flavoured with 2.0 % vanilla on the other days.
However, in addition, Groups VS and AS also received a supplement of
4 gm of unflavoured plain chow (also in wet mash form) 15 min after
consuming the small meals. On any given conditioning day, all the
animals received the same flavour: for example, on a typical 'vanilla
day', Group V and VS received large vanilla flavoured meals, while
Groups A and AS received small vanilla flavoured meals, and only
Group AS received the 4 gm of supplementary food after 15 min. The
6 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
flavoured meals used for conditioning were presented at 1 000 hr while
maintenance food was presented for 2 h beginning at 1500 hr.
Testing was done using a two jar extinction choice paradigm which
involved comparing the consumption of two diets presented
simultaneously in equal amounts in two feeding jars. Each jar contained
20 gm of either anise or vanilla flavoured food in wet mash form.
Testing lasted for only 10 min beginning at 1000 hr on each test day.
The positions of test foods were counterbalanced for each pair of
animals to minimise any positional biases. The first test was done on
Day 9 (Phase 1) after which the conditioning cycle was repeated for
another 8 days. Then, another choice test followed on Day 23 (Phase 2).
In order to further demonstrate the consistency and resilience of the
phenomenon under investigation, the above procedure was repeated
exactly except that the flavours were reversed during Phase 2 as
mentioned earlier. A 5-day interval was allowed to reduce the chances
of rats confusing flavour-meal size pairings used in Phase 1 . However,
no tests were carried out to ascertain whether or not preferences had
remained unchanged during the intervening period. Thus, during Phase
2 Groups V and VS were presented with anise-flavoured large meals on
some days and vanilla-flavoured small meals on other days while Groups
A and AS were presented with vanilla-flavoured large meals on some
days and anise-flavoured small meals on other days. Note that these
flavour meal size correlations are exactly the opposite to treatments
given in Phase 1. In addition. Groups VS and AS were retained as
controls as in Phase 1, and they both received supplements of 4 gm of
unflavoured plain mash 15 min after the presentation of food on 'small
meal' days. However, as in Phase I, Groups V and A did not receive
any supplementary food on their small meal days.
Relative preferences for anise-flavoured food in the extinction choice
tests which followed each 8 day training cycle were calculated in terms
of percentages of total food consumption by each subject during each
test as follows:
intake of anise
intake of both anise and vanilla
Preference for anise (%) = 100 ^
Data analysis
Data obtained during each of the two phases of the experiment were
initially assessed using separate three way analyse of variance (ANOVA)
with repeated measures, comprising large meal flavour (anise versus
vanilla), supplementation (supplement versus no supplement) and test
LEICKNESS C. SIMBAYI 7
session (Test 1 versus Test 2) as factors. In order to determine how
flavour preferences shifted after each 8 day training cycle, data obtained
during each of the two test sessions in each phase were also separately
assessed using two way ANOVAs with large meal flavour and
supplementation as factors.
RESULTS
During conditioning, all animals ate all of the portions of food given
to them every day. The data obtained from the extinction choice tests
carried out at the end of each of the four 8 day training cycles in
Experiment 1 are illustrated in Figure 1 . This figure shows that although
all groups highly preferred vanilla compared with anise in all choice
tests (as revealed by low anise preferences ranging from 2 % to 35 %),
quite clear group differences could still be seen.
PHASE 1
2 1
TEST SESSIONS
PHASE 2
- GROUP V -t- GROUP VS -X- GROUP A "■- GROUP AS
Figure 1. Mean preferences (%) for anise flavour during the two-jar extinction choice
tests in Experiment 1 (n = 5). Note: Flavour-meal size pairings were reversed during
Phase 2.
8 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
The ANOVAS performed on data obtained during each of the two
phases of the experiment revealed a significant main effect of large meal
flavour during Phase 1 only, F(3,16) = 5.69, p < 0.01. As can be clearly
seen in Figure 1, this indicates that both Groups V and VS consumed
significantly more anise-flavoured food than Groups A and AS during
Phase 1 . However, there were no such major flavour preference shifts
observed during Phase 2 following reversal training, although the
direction of the small preference shifts that had occurred was similar to
that observed during Phase 1.
A two way ANOVA of data obtained during Test 1 of Phase 1
revealed reliable main effects of both large meal flavour and
supplementation, F(l, 16) = 8.17 and 5.32, p < 0.01 and 0.05,
respectively. However, there was no significant interaction between the
two factors. As can also be clearly seen in Figure 1, supplementation of
meals significantly reduced the magnitude of flavour preference shifts
during Test 1 . Another two way ANOVA of data obtained during Test
2 of Phase 1 revealed a significant main effect of large meal flavour
only, F(l,16) = 5.32, p < 0.05. Similar statistical analyse of data
obtained during each of the two tests in Phase 2 of the experiment failed
to reveal any significant main effects or interactions.
DISCUSSION
Three main findings emerged from Experiment 1 . Firstly, adult rats
learned to prefer a particular flavour when it was previously correlated
with small meals more than when the same flavour was correlated with
larger ones. Secondly, supplementation of small meals initially slightly
reduced the preferences for the flavour previously paired with the small
meal, but had no effect on the preferences afterwards. Even though the
rats had clearly a positive preference for vanilla and what appeared to be
an unconditioned aversion to anise, it was also clear from the data that
the flavour tracking effect was quite consistent throughout the
experiment. Thirdly, although reverse flavour-meal size pairings reduced
the preferences to non significance, they were still in the direction
determined by meal sizes.
Although the first finding appears to be consistent with Booth's
(1972; conditioned satiety findings, the extinction testing procedure
which was used in the present experiment was different from that
utilised by Booth. For instance. Booth's testing procedure involved
presenting the two test flavours one at a time whereas in the present
experiment the testing procedure involved simultaneous (or side by side)
LEICKNESS C. SIMBAYI 9
presentation of the two test flavours. However, the same finding clearly
contradicts reports by Bolles et al. (1981) and Hay ward (1983) that adult
rats can not learn taste preferences based on differing caloric outcome.
The second finding appears to be entirely consistent with those of
Booth and Davis (1973) and Booth et al. (1982) who found that although
the latter supplements failed to condition meal size per se, they did
actually manage to condition flavour preferences. Finally, the third
finding could be explained in terms of either overshadowing or proactive
interference (or inhibition) of the subsequent learning during Phase 2 by
learning which took place earlier during Phase 1.
EXPERIMENT 2
One criticism of the conditioned satiety hypothesis, namely that the
animal will prefer the flavour not associated with satiety, is that it might
instead avoid the flavour with a prolonged exposure due to an acquired
aversion. In order to rule out this possibility, in Experiment 2 flavours
were presented for an equal amount of time but were followed or
preceded by different sized supplements. Therefore, for one half of the
subjects, one flavour was followed by 4 gm while a second flavour was
followed by 1 gm of plain mash. Hence, this procedure controlled both
for flavour exposure time and for the disturbance factor involved when
supplements are given after the presentation of flavour cues. Another
important issue concerns the extent to which the relationship between the
flavour cue and the caloric supplement could also be important, since
cues presented at meal onset may have a different value compared with
those at the end of the meal. In order to investigate this issue flavour
cues were preceded by supplements for the remaining half of the
experimental subjects. This allowed comparisons to be made to examine
the extent to which conditioned satiety depended upon the relative
temporal positions of flavour cues and supplements.
METHOD
Animals and materials
The subjects consisted of 24 male hooded Lister rats obtained from
the same breeding colony as in the previous experiment. They were
aged about 160 days and weighed 325 - 480 gm at the beginning of the
experiment. The rats had previously been used in another flavour
10 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
conditioning experiment employing the Holman (1975) procedure using
delayed reinforcement (Simbayi, 1987), but had no experience with the
solid reinforcer, the two flavours (i.e., vanilla and anise) and the
conditioning procedure used in this experiment. The subjects were
allowed about 4 weeks of ad libitum feeding prior to being given another
2 weeks to adjust to new housing conditions and a new feeding schedule
similar to that used in Experiment 1 . In addition, they were allowed 6
days to accommodate to feeding on wet chow from feeding jars placed
inside their individual cages before the actual experiment began.
All the materials used were similar to those used in Experiment 1 .
Procedure
The rats were housed, watered, fed and tested exactly as in
Experiment 1. However, some major changes were made during
training. Discrimination training commenced at the same time of day as
in Experiment 1 and flavours were also presented in a semi-random
order for 8 days. The subjects were randomly divided into four groups
(n = 6), namely. Groups VS, AS, SV and SA. Groups VS and AS
received flavoured mash initially before supplements of plain mash were
presented whereas supplements of plain mash preceded the presentation
of flavoured mash in Groups S V and S A. All four groups received 1 gm
of either vanilla or anise flavoured mash, each flavour separately for a
total of 4 days. On any particular conditioning day, all groups received
only one of the two flavours which served as the conditioned stimuli.
Group VS received 4 gm of plain mash 2 min after the presentation of
1 gm of vanilla flavoured mash on some days and only 1 gm of plain
mash also 2 min after the presentation of 1 gm of anise flavoured mash
on other days. Groups AS received a similar treatment to Group VS,
except that flavour-meal size contingencies were reversed, that is, 4 gm
of plain mash 2 min after the presentation of 1 gm of anise flavoured
mash on some days and 1 gm of plain mash also 2 min after the
presentation of 1 gm of vanilla flavoured mash on other days. However,
Groups SV and SA were presented with the same flavour-meal size
pairings, as Groups VS and AS respectively, except that the order of the
presentation of the flavoured and plain mash were reversed. Therefore,
Group SV received 4 gm of plain mash 5 min before the presentation of
1 gm of vanilla flavoured mash on some days and also 1 gm of plain
mash 2 min before the presentation of 1 gm of anise flavoured mash on
the other days. Similarly, Group SA received the same treatment as
Group SV, except that the flavour-meal size pairing was reversed, that
is, 4 gm of plain mash was presented 5 min before the presentation of
LEICKNESS C. SIMBAYI 11
1 gm of anise flavoured mash on some days and 1 gm of plain mash 2
min before the presentation of 1 gm of vanilla flavoured mash on other
days. The 2-min and 5-min intervals were introduced to enable the
animals to eat all of the initial plain and flavoured mash respectively
before additional food was presented. This procedure was adopted to
prevent mixing of flavoured and unflavoured food and a possible
reduction of the potency of the conditioned stimuli due to dilution.
Testing for changes in preferences of either anise- or vanilla-
flavoured mash was performed using two jar extinction choice tests on
2 consecutive days and lasted for 10 min on each day as in Experiment
1 . Rats were simultaneously presented with 30 gm of vanilla flavoured
mash and 30 gm of anise flavoured mash in separate jars. Both Tests
1 and 2 were held under conditions of food deprivation similar to those
employed during conditioning.
RESULTS
All animals consumed their food portions on all training days. The
results obtained from the choice tests carried out at the end of the single
8-day training cycle are shown in Figure 2. During Test 1, both Groups
VS and SV which had prior exposure to large vanilla-flavoured meals
and small anise-flavoured meals had higher preferences for anise-
flavoured mash than Groups AS and SA which had been exposed to
large anise-flavoured meals and small vanilla- flavoured meals. There
was a similar pattern of group preferences during Test 2. During both
Tests 1 and 2, Groups VS and AS (which had received cues before
supplements) had higher preferences for anise-flavoured mash than
Groups SV and SA, which had received flavour cues after the meal
supplements.
A two way ANOVA of data obtained during Test 1 revealed
significant main effects for both large meal flavour and the timing of the
supplement, Fs (1, 20) = 10.43 and 6.22, ps < 0.01 and 0.05,
respectively. However, there was no significant interaction between the
two factors. The former main effect indicates that Groups VS and SV
had significantly higher preferences for anise-flavoured mash than
Groups AS and SA, whereas the latter one shows that flavour cues were
more effective as conditioned stimuli during conditioning when they
were presented at meal onset as in Groups VS and AV than at meal
offset as in Groups SV and SA. When data obtained during Test 2 was
also statistically assessed, neither the main effects nor the interaction
between the two factors were found to be significant.
12
INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
TEST 1
TEST 2
TEST SESSION
GROUP VS E] GROUP AS D GROUP SV ^ GROUP SA
Figure 2. Mean preferences (%) for anise flavour during the two-jar extinction choice
tests in Experiment 2 (n = 6). Bars represent standard errors.
DISCUSSION
Three main findings emerged from Experiment 2. Firstly, it
confirmed the finding in Experiment 1 that adult rats are capable of
learning about flavour-meal size associations. Even when flavour-
exposure time was controlled, the rats learned to prefer a flavour
previously associated with a small meal better than when the same
flavour was paired with a large meal. Secondly, flavour-meal size
effects were stronger when flavour cues were presented at meal onset
than at meal offset. Thirdly, the conditioned effects extinguished very
rapidly.
The finding that conditioned satiety effects could still emerge when
flavour exposure time was controlled provides further evidence that
satiety associated with the ingestion of large meals has no positive
reinforcement properties. Similar conclusions have been arrived at by
Van Vort and Smith (1983). The present finding also weakens the
LEICKNESS C. SIMBAYI 13
argument that conditioned flavour preferences observed in Experiment
1 were due to an acquired aversion towards prolonged flavour exposure
which was associated with large meals during conditioning.
The second finding that flavour cues were presented at meal onset
rather than at meal offset suggested that the cues may be more salient
and less interfered with at the former than at the latter stage. The
presentation of flavour cues following supplements was still effective in
conditioning satiety but it reduced the effects considerably. It is possible
that when supplements preceded flavour cues, they interfered with the
learning of the discrimination between the two flavours and the
appropriate satiety signals derived from the two meal sizes. The result
of such interference was probably some weakening of the effects of the
conditioning.
An alternative explanation would be that the rats became satiated
after consuming the supplements and perceived the appropriate satiety
signals immediately afterwards before the flavour cues were even
presented and perceived. Therefore, it would appear from the present
data that the strength of any flavour-meal size conditioning is stronger
when the flavour cues precede supplements than vice versa. This finding
appears to contradict the findings reported by Booth and Davis (1973)
in rats and Booth et al. (1982) in humans, where the later supplements
failed to condition meal size per se and conditioned only flavour
preferences at most. The third finding that the conditioned satiety effects
were weak and extinguished rapidly was surprising when compared with
the extreme persistency of the other types of flavour conditioning based
phenomena (see Capaldi, Myers, Campbell & Sheffer, 1983; Logue,
1979; Revusky, 1974; although see Simbayi, 1987). The effects had
disappeared as early as the second test day after an 8-day conditioning
cycle during which each flavour-meal size pairing was presented four
times only. Perhaps, the effects could have been more persistent and
more resistant or less susceptible to extinction with additional
conditioning.
EXPERIMENT 3
Both previous experiments demonstrated flavour-meal size
conditioning in adult rats. The aim of Experiment 3 was to test
Hay ward's (1983) claim that rat pups are apparently capable of more
diverse learning than adult rats. As indicated earlier, Hayward showed
that rat pups, but not adult rats, could acquire a conditioned taste
preference for a flavour paired with a diet that provides more calories
14 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
than another diet of equal caloric density. In particular in her
Experiment 3, she obtained stronger conditioning of caloric effects with
rat pups when a 4 cal/gm novel diet represented the major part of the
animal's daily caloric intake for just 4 conditioning days. The pups were
given unlimited access to 20 gm of the 4 cal/gm diet on one day, and
three quarters of the previous day's consumption on alternate days. In
order to control for differential hunger experienced on days when rats
had inadequate food, the food supply of half of the animals was topped
up with laboratory chow 8 h after presentation of the novel diet. Thus,
the present experiment was meant to confirm such caloric effects by
using a procedure almost identical to that employed by Hayward except
for the following four minor changes which were made. Firstly, rats
were first familiarised with the diets to reduce neophobia. Secondly, on
small days the rats received only half of the amounts of food they
received on large meal days to make the meal sizes more easily
discriminable but, as indicated above, their training diets were also
supplemented by laboratory chow pellets. Thirdly, the duration of
testing was extended to cover a period of up to 24 h with intervals at 30
min and 4 h instead of only after 30-min and 3-h intervals as per
Hayward (1983). This allowed monitoring of intake rates for a period
longer than a meal which in turn made it possible for one to distinguish
between aversions taking place early and throughout the meal as opposed
to those taking place later. This in turn made it possible to distinguish
between conditioned aversion and conditioned satiety respectively.
Finally, in order to facilitate comparisons with other experiments
reported in the present paper, conditioning lasted for 8 days instead of
only 4 as in Hayward's study.
METHOD
Animals
Twenty four male naive Lister rat pups, 24 - 28 days old and
weighing 46-91 gm at the beginning of the experiment, were used.
The rat pups were weaned at the age of 2 1 days old and reared in colony
cages (4-6 animals per cage). They had ad libitum access to dry
laboratory chow pellets (Scientific Foods, Croydon, England) and tap
water for 3 - 7 days before the experiment commenced. Following
selection and assignment to groups, the weanling rats were housed
individually in wire cages in a cage rack in an experimental room and
had ad libitum access to water throughout the experiment.
LEICKNESS C. SIMBAYI 15
Materials
The recipe for the novel diet used was identical to that utilised by
Hayward as the high calorie food. It consisted of 50% dextrin (Sigma),
15% calcium carbonate (chalk, East Anglia Chemicals), 2.5% mineral oil
(liquid paraffin, British Drug Houses, now M. W. Scientific, Ltd., Poole,
Dorset, England), 7.5% ordinary (domestic) vegetable cooking oil and
25% lactic casein (Sigma). The diet provided approximately 4 cal/gm.
Either vanilla or anise extract was added to the diets separately in the
following proportions: for vanilla, 10 ml of flavour was added to 100 gm
of the diet mixture; for anise, 0.50 ml of flavour was dissolved in 20 ml
of water and also added to 100 gm of the diet mixture.
Procedure
The rats were assigned randomly to four groups (n = 6), namely.
Groups R-A, R-V, Ad-A, and Ad-V, with R and Ad standing for
restricted and ad libitum conditions respectively, as explained below.
Groups R-A and R-V represented Groups A and V in Experiment 1 in
the present study whereas Groups Ad-A and Ad-V represented Group 2
(the chow group) in Experiment 3 reported by Hayward (1983). On
familiarisation days, all the weanling rats were exposed to the
unflavoured novel 4 cal/gm diet. First, all groups received 40 gm
overnight. Then, Groups R-A and R-V received only 5 gm while
Groups Ad-A and Ad-V continued to receive unrestricted access to 40
gm for every 24 h beginning at 1200 hrs for the next 3 consecutive days.
On conditioning days, Groups R-A received anise flavour in 5 gm
of the novel 4 cal/gm diet on some days and vanilla flavour in 1 gm of
the same diet on other days. The flavour-meal size pairing was reversed
for Group R-V. Group Ad-A received anise flavour in 20 gm of the
novel 4 cal/gm diet on some days and vanilla flavour in 10 gm of the
same diet on other days. Similarly, the flavour-meal size pairing was
reversed for Group Ad-V. Therefore, for all rats, the two flavours were
correlated with the same pattern of oral cues but differing caloric
consequences (i.e., 20 vs. 4 calories for Groups R-A and R-V and 80 vs.
40 calories for Groups Ad-A and Ad-V, both respectively). Altogether,
rats in Groups Ad-A and Ad-V experienced 4 days with sufficient food
(i.e., large meals) and another 4 days with an inadequate amount of food
(i.e., small meals). In order to avoid the problem of differential hunger
on days of inadequate food, the food supply was supplemented by 5
pellets of dry laboratory chow (weighing approximately 10 gm and
containing 40 calories) 5 h after the presentation of the training diet.
16 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
For both Groups R-A and R-V, laboratory chow was removed 2.5 h
prior to the presentation of the novel diet and returned 5 h afterwards.
The remaining rats in both Groups Ad-A and Ad-V received no
additional food except only as specified above, that is, on small meal
days. Flavours were also presented in semi-random order as in previous
experiments.
All groups were given an extinction choice test between the anise
and vanilla flavoured diets on Day 9. Two jars of the 4 cal/gm food
were presented simultaneously, and consumption was recorded at the end
of 30 min, 4 h and 24 h for all four groups. As in previous experiments,
preferences for anise-flavoured food were calculated as percentages of
total food intake.
Data analysis
The data were first assessed using a three way repeated measures
ANOVA with the following factors: duration of exposure to the training
diet (restricted vs. ad libitum), the large meal flavour (anise vs. vanilla)
and cumulative test intervals (30 min vs. 4 h vs. 24 h). Follow up
limited pair-wise comparisons between groups trained under similar
conditions of exposure to the training diets at each test interval were also
carried out using independent t tests.
RESULTS AND DISCUSSION
All animals completely consumed their food portions on all training
days. Figure 3 outlines the results obtained during the three cumulative
intervals of the extinction choice test held on Day 9. It shows that the
two groups which had received vanilla flavour paired with the larger
meal during training (i.e., Groups R-V and Ad-V) generally had higher
preferences for anise than the other two groups (i.e., Groups R-A and
Ad-A) which had received anise paired with the larger meal during
training. This effect was particularly marked after 24 h than after both
the 30 min and 4 h cumulative intervals of the extinction choice test.
The repeated measures ANOVA failed to reveal any significant main
effects (all ps > 0.05). However, the interaction between all three factors
was significant, F(2,40) = 5.82, p < 0.01. Additional between-group
comparisons also revealed a highly significant difference between
Groups Ad-A and Ad-V after 24 h of testing only, / (10, one tailed) =
5.07, p < 0.001 (see Figure 3). This shows that the rat pups were clearly
capable of learning to associate a taste with the size of the meal under
LEICKNESS C. SIMBAYI
17
30 MIN
4 HOURS
TEST INTERVAL
24 HOURS
GROUP R-A E] GROUP R-V D GROUP Ad-A ^ GROUP Ad-V
Figure 3. Mean preferences (%) for anise flavour during the two-jar extinction choice
tests in Experiment 2 (n = 6). Bars represent standard errors.
the ad libitum feeding conditions, whereas they were not able to do so
under restricted feeding conditions. Even more interesting was the fact
that flavour preference shifts were most pronounced after 24 h of testing
than earlier. This finding suggests that the flavour-meal size
conditioning effects observed in these experiments might be attributed
to satiety rather than aversions, because if the latter were involved,
flavour preference shifts would have been observed throughout the test
period. In particular, they would have commenced at the beginning of
the test period rather than later, as occurred in the present experiment.
The results are consistent with Booth's (1972) conditioned satiety ideas
but they clearly contradict Hayward's (1983) findings. It is important to
note here that the present experiment used a procedure similar to
Hayward's except that the meal sizes and one flavour were different.
However, her findings generally supported a conditioned appetite
hypothesis whereby only young rats learned to prefer a taste which was
previously associated with larger meal sizes or more calorific diets.
18 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
EXPERIMENT 4
As both the training and testing procedures employed in Experiment
3 did differ somewhat from those employed in both earlier experiments
(i.e., Experiments 1 and 2), it is not only difficult but also rather unfair
to make direct comparisons between their respective findings. Clearly,
the best way to achieve such a goal would be to replicate Experiment 3
using naive adult rats. This was the aim of Experiment 4. According
to Hay ward (1983), an adult rat no longer attends to post-ingestional
feedback since it is rarely hungry and therefore is not capable of learning
conditioned taste preferences based on differing caloric outcome.
Therefore, Experiment 4 investigated whether naive adult rats could be
as responsive as naive young rats to flavours paired with differing
caloric outcome when novel diets provided either only a small proportion
or most of the rats' daily caloric needs.
METHOD
Animals
Twenty four naive male hooded Lister rats 81 - 126 days-old and
weighing 245 - 420 gm at the start of the experiment were used.
Materials and Procedure
The materials and procedure were the same as for Experiment 3
except for the following three minor changes: both Groups R-A and R-
V were allowed 25 gm of supplementary solid laboratory chow pellets
at 17.00 hrs each day; during familiarisation, both Groups Ad-A and
Ad-V received 30 gm of unflavoured and novel high calorie diet instead
of 20 gm only as in Experiment 3; during training, both Groups Ad-A
and Ad-V received 30 gm of the novel diet with no supplements on
large meal days and 15 gm of the novel diet plus another 15 gm
supplement of solid laboratory chow pellets on small meal days. All the
changes were made to compensate for the larger size of animals used in
the present experiment compared to those used in Experiment 3.
RESULTS AND DISCUSSION
All animals completely consumed their food portions on all training
LEICKNESS C. SIMBAYI
19
30 MIN
4 HOURS
TEST INTERVAL
24 HOURS
GROUP R-A E] GROUP R-V DgROUP Ad-A ^ GROUP Ad-V
Figure 4. Mean preferences (%) for anise flavour during the two-jar extinction choice
test in Experiment 3 (n = 6). Bars represent standard errors.
days. The results obtained during the three interval of the extinction
choice test held on Day 9 are displayed in Figure 4. They show that
Group Ad-V generally had higher preferences for anise flavour than
Group Ad-A, whereas no such differences are evident between Groups
R-A and R-V.
When the data were assessed using a three way repeated measures
ANOVA as for Experiment 3, neither the main effects nor interactions
were significant. However, additional between-group comparisons of
anise preferences indicated that Group Ad-A had a significantly higher
preference than Group Ad-V after the 4 h test interval only, / (10, one
tailed) = 2.20, p < 0.05. Thus, these mature rats were also able to learn
about flavour-meal size associations under ad libitum but not restricted
feeding conditions, as did the weanling ones in Experiment 3. It is
rather difficult to explain why adult rats appeared to learn conditioned
satiety only when flavour-meal size pairings were presented on an ad
libitum basis (30 gm vs. 15 gm) but not when access was restricted to
20 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
much smaller amounts (5 gm vs. 1 gm). Perhaps, in the latter condition
adult rats simply ignored post-ingestional feedback of the small snacks
with a novel flavour and concentrated mostly on the bigger
supplementary meals from which most of their daily caloric requirements
were derived. Such a view is consistent with that of Bolles et al. (1981)
and Hay ward (1983) who used this fact to argue why adult rats should
fail to learn to associate a flavour with a diet that provides more calories
under such conditions. Nevertheless, the fact that, like weanling rats,
adults can acquire flavour-meal size effects, appears to contradict these
authors' findings. Another interesting aspect of the present results is that
preference shifts in those groups which displayed them were most
evident only after 4 h of testing. This differs from Experiment 3 where
preference shifts were most notable in the groups concerned after 24 h
of testing. Although the reasons for this disparity are unclear at present,
one possibility is that older rats may experience the onset of satiety
much sooner than younger ones. Nevertheless, this issue needs to be
investigated further. Experiment 4, therefore, has shown that adult rats
appear to learn to make flavour-meal size associations just as well as
weanling rats especially when the diet provides for most of the animals
daily caloric needs.
GENERAL DISCUSSION
The present research showed that both weanling and mature rats are
capable of learning to associate a flavour with the size of a meal. In
particular, these findings demonstrated flavour-meal size conditioning
effects whereby an animal learns to prefer a flavour not associated with
a larger meal. It is however important to note here that, as Capaldi and
Myers (1982) and Davidson-Codjoe and Holman (1982) have pointed
out, the preferences demonstrated in experiments of this sort are relative,
rather than absolute. The data really do not distinguish a preference for
the flavour consumed when rats received the small meal from an
aversion for the flavour consumed when they received the large meal.
Furthermore, as Capaldi et al. (1983) also pointed out, the word
"preference" is usually intended as a neutral term accommodating either
a learned aversion for the flavour associated with the large meal, learned
liking for the flavour associated with the small meal, or both.
As the present results are consistent with Booth's (1972) and Booth
and Davis' (1973) findings, a phenomenon very similar to Booth's
conditioned satiety may be implicated. Conditioned satiety involves an
increment in the size of the feeding bout on the dilute nutrient (or, small
LEICKNESS C. SIMBAYI 21
meal, few calories, etc.) more than on the more concentrated nutrient (or
large meal, many calories, etc.) after several pairs of presentations. This
takes place in order to compensate for calories depending on the nature
of the concentrated diet. Booth suggested that such conditioning of
satiety may be important in the control of food intake only under
conditions which are put on the timing of meals, that is, under high food
deprivation schedules. Perhaps, different mechanisms are involved under
normal ad libitum feeding conditions. This might explain why stronger
evidence of conditioned satiety learning was obtained under restricted
feeding conditions in both Experiments 1 and 2 in the present study than
was the case under ad libitum feeding conditions in both Experiments 3
and 4. Nevertheless, the present findings clearly demonstrated the
existence of an acquired oral and/or olfactory sensory control of the
satiation process just as Booth's conditioned satiety study did. The
present findings are also in agreement with those of Le Magnen (1985)
and Deutsch (1982).
The present findings suggest that oral qualities of a familiar food
may enable a mammal to react in anticipation of that food's caloric value
or the duration of its satiating effect. According to such a view, animals
stop eating at an appropriate stage even though absorption has barely
started or possibly has not even started at all as in the case of a rapid
feeder such as a dog. However, our findings clearly contradict
Hay ward's (1983) findings which generally demonstrated conditioned
appetite in weanling rats but not in adults. Apart from strain differences,
it is unclear at present why our results contradict Hayward's.
One hypothesis which explains the present findings is that the
flavour tracking may be due to an acquired difference in the
development of feeding inhibition during meals. This is because there
were no differences in basal acceptability since both meals consisted of
the same diet, except for flavours which were added to them. This view
is consistent with that of Booth (1972). The higher preference for the
flavour which had been paired with a small meal demonstrated in the
present study could be attributed to a difference in the speed of onset of
the suppression of intake in the later stages of the meal. This might
suggest that an acquired oral and/or olfactory factor contributed to the
development of the satiety which ended the meal to which the flavour
previously associated with the large meal was added. When faced with
a choice between flavour cues previously associated with large and small
meals during conditioning, a satiety signal switched off eating
immediately after the animal had perceived that the flavour was
previously correlated with a large meal which was too satiating.
However, there was no such satiety signal forthcoming from flavour
22 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
correlated with less satiating small meals and consequently, rats
consumed significantly more food with a flavour which was previously
associated with a small, less satiating meal. Hence, satiety had no
positive reinforcing effects and might have been aversive. As was
mentioned earlier, such a conclusion is consistent with that of Van Vort
and Smith's (1983) who found that satiety had no positive reinforcing
effects on flavour preferences at all whilst using sham feeding techniques
and a similar flavour tracking procedure.
An alternative explanation is that when rats were exposed to flavours
correlated with large meals, they developed slightly stronger aversions
to them than when exposed to flavours correlated with small meals.
However, since Experiments 2-4 controlled for the amount of flavour
exposure, this hypothesis is highly improbable. Furthermore, the mere
fact that all groups in Experiment 1 ate in excess of 60% vanilla-
flavoured food during choice tests further weakens this argument.
The conditioning of flavour preferences based on meal size
demonstrated in the present research does not in any way contradict Le
Magnen's (1969) findings of conditioned appetite at all. Conditioned
discriminative (also referred to as selective or differential) appetite
induced during conditioning causes a rat to eat more of the reinforced,
and hence beneficial food, and less of the non reinforced food in the
final choice test. As Bolles et al. (1981) pointed out, conditioned satiety
and conditioned appetite merely represent complementary aspects of
intake regulation. Whereas the phenomenon proposed by Le Magnen
(which Bolles et al. later failed to demonstrate) was basically concerned
with food selection through learning about the caloric potential of
different foods, the phenomenon demonstrated in the present study more
likely operates after the selection of the diet offering optimum caloric
consequences has been completed. Hence, the animal learns to eat less
of that diet on a day-after-day basis under conditions in which
constraints are put on the timing of meals.
According to Capaldi et al. (1987), shifts in preferences such as
those demonstrated in the present study can be viewed within either a
classical conditioning or an instrumental learning paradigm. In a
classical conditioning framework, the flavours are the conditioned stimuli
(CSs) and they are being associated with some unconditioned stimulus
(US) that is produced by consumption of meals of different sizes made
from the same diet. In an instrumental learning paradigm, the flavours
are the discriminatory stimuli (SDs) signalling the reinforcement
produced by the instrumental response of consuming meals of different
sizes. The important question therefore concerns what is the US or
reinforcer in either paradigm.
LEICKNESS C. SIMBAYI 23
One of the best candidates for the US or reinforcer in the type of
learning demonstrated in the present study is the post-ingestive
consequences of ingesting meals such as calories. Supporting evidence
for flavour-calorie learning in rats has been reported elsewhere (e.g.,
Capaldi et al., 1987; Deems et al., 1986; Hayward, 1983; Holman, 1975;
Mehiel and Bolles, 1984; Sherman, Hickis, Rice, Rusiniak & Garcia,
1983). Another possible candidate for the US or reinforcer is some oral
stimulus such as flavour (or taste). However, this is very unlikely
because the different sized meals in each experiment in the present study
consisted of exactly the same diet, which meant that the flavour of the
food contained in the two meals was identical. Thus, the flavour-meal
size conditioning effects demonstrated in the present research were most
probably the result of flavour-calorie rather than flavour-flavour
associations.
Finally, it must be noted here that although only four experiments
are reported in the present paper, six additional experiments were also
carried out which consistently failed to yield any significant effects.
However, preferences were mainly in the direction which is predicted by
the conditioned satiety hypothesis, that is, the small meal flavour was
relatively more preferred. These findings also suggest that the
flavour-meal size conditioning effect definitely occurs but we have not
yet been able to identify all the conditions which enable consistently
reliable effects.
In conclusion, both mature and weanling rats appear to be capable
of learning about flavour-meal size associations. In particular, they
acquired conditioned satiety, albeit very weakly, rather than conditioned
appetite as previously demonstrated by both Bolles et al. (1981) and
Hayward (1983) in their similar studies. These conditioned satiety
effects, which are most probably due to flavour-calorie rather than
flavour-flavour (or tastes) associations, are also distinctly elusive.
ACKNOWLEDGEMENTS
This research was carried out in the Laboratory of Experimental
Psychology at the University of Sussex, Brighton, England, U.K., as part
of a D. Phil, project. It was partially financed by a U.K. Medical
Research grant to Dr. M.J. Burton and also by a University of Zambia
Staff Development Fellowship to the author. The author wishes to
acknowledge, with deep gratitude, the immense help received during the
study from Drs. Burton and R. A. Boakes, both of the Laboratory of
Experimental Psychology at Sussex University at the time, who jointly
24 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
served as supervisors for this project. Their constant encouragement
throughout his sojourn at Sussex University is especially appreciated.
The author would also like to thank Sara Hill, Tracey Gummet,
Annabele Poate and Mark Allen for helping carry out Experiment 2 as
part of their undergraduate research project under his supervision and
also Dr Christopher J. Rainey for his assistance with running some of the
experiments. Finally, the comments and suggestions of two anonymous
reviewers are greatly appreciated.
REFERENCES
Boakes, R.A., & Lubart, T. (1988). Enhanced preference for a flavour following reversed
flavour-glucose pairing. Quarterly Journal of Experimental Psychology, B40, 49-62.
Boakes, R.A., Rossi-Arnaud, C, & Garcia-Hoz, V. (1987). Early experience and
reinforcer quality in delayed flavour- food learning in the rat. Appetite, 9, 191-206.
Bolles, R.C. (1983). A "mixed" model of taste preference. In R.L. Mellgren (Ed.),
Advances in Psychology (Vol. 3): Animal cognition and animal behavior.
Amsterdam: North-Holland.
Bolles, R.C, Hayward, L., & Crandall, C (1981). Conditioned taste preferences based
on caloric density. Journal of Experimental Psychology: Animal Behavior
Processes, 7, 59-69.
Booth. D.A. (1972). Conditioned satiety in the rat. Journal of Comparative and
Physiological Psychology, 81, 457-47 1 .
Booth, D.A. (1985). Food-conditioned eating preferences and aversions with
interoceptive elements: Conditioned appetites and satieties. In N.S. Braveman & P.
Bronstein (Eds.), Experimental assessments and clinical applications of conditioned
food aversions. Annals of the N.Y. Academy of Science, 443, 22-41.
Booth, D.A., & Davis, J.D. (1973). Gastrointestional factors in the acquisition of oral
sensory control of satiation. Physiology and Behavior, 11, 23-29.
Booth, D.A., & Mather, P. (1978). Prototype model of human feeding growth and
obesity. In D.A. Booth (Ed.), Hunger models. New York: Academic Press.
Booth, D.A., Lee, M., & Aleavey, C. (1976). Acquired sensory control of satiation in
man. British Journal of Psychology, 67, 137-147.
Booth, D.A., Mather, P. & Fuller, J. (1982). Starch content of ordinary foods
associatively conditions human appetite and satiation, indexed by intake and eating
pleasantness of starch-paired flavours. Appetite, 3, 16-184.
Booth, D.A., Stoloff, R., & Nicholls, J. (1974). Dietary flavour acceptance in infant rats
established by association with effects of nutrient composition. Physiological
Psychology, 2, 313-319.
Capaldi, E.D., & Myers, D.E. (1982). Taste preferences as a function of food deprivation
during original taste exposure. Animal Learning and Behavior, 10, 21 1-219.
Capaldi, E.D., Campbell, D.H., Sheffer, J.D., & Bradford, J. P. (1987). Conditioned
flavour preferences based on delayed caloric consequences. Journal of Experimental
Psychology: Animal Behavior Processes, 13, 150-155.
Capaldi, E.D., Myers, D.E., Campbell, D.H., & Sheffer, J.D. (1983). Conditioned flavour
preferences based on hunger level during original flavour exposure. Animal
LEICKNESS C. SIMBAYI 25
Learning and Behavior, J], 107-115.
Capretta, P.J. (1961). An experimental modification of food preferences in chickens.
Journal of Comparative and Physiological Psychology, 54, 238-242.
Crawford, D., & Baker, T.B. (1982). Alcohol dependence and taste-mediated learning
in the rat. Pharmacology, Biochemistry and Behavior, 16, 253-261.
Davidson-Codjoe, M., & Holman, E.W. (1982). The effect of non-nutritive satiation on
the learning of a flavour preference by rats. Animal Learning and Behavior, 10,
220-222.
Deems, D.A., Getting, R.L., Sherman, J.E., & Garcia, J. (1986). Hungry, but not thirsty,
rats prefer flavours paired with ethanol. Physiology and Behavior, 36, 141-144.
Deutsch, J. A. (1982). Controversies in food intake. In B.C. Hoebel & D. Novin (Eds.),
The neural basis of feeding and reward. Brunswick, Maine, U.S.A.: Haer Institute
of Electrophysiological Research.
Deutsch, J.A. (1983). Dietary control and the stomach. In G.A. Kerkut, & J.W. Phillips
(Eds.), Progress in neurobiology. (Vol. 20) Oxford: Pergamon Press.
Deutsch, J.A. (1987). Signals determining meal size. In R.A. Boakes, D.A. Popplewell,
& M.J. Burton (Eds.), Eating habits. Chichester: John Wiley.
Deutsch, J.A., & Gonzalez, M.F. (1980). Gastric nutrient content signals satiety.
Behavioral and Neural Biology, 30, 113-116.
Deutsch, J. A., & Walton, N.Y. (1977). A rat alcoholism model in a free choice situation.
Behavioral Biology, 19, 349-360
Deutsch, J.A., Gonzalez, M.F., & Young, M.G. (1980). Two factors control meal size.
Brain Research Bulletin, 5(4), 55-58.
Fanselow, M.S., & Berk, J. (1982). Flavour-flavour associations induce hedonic shifts
in taste preferences. Animal Learning and Behavior, 10, 223-228.
Hay ward, L. (1983). The role and postingestional cues in the conditioning of taste
preferences based on differing caloric density and caloric outcome in weanling and
mature rats. Animal Learning and Behavior, 11, 325-331.
Hogan, J.A. (1977). The ontogeny of food preferences in chicks and other animals. In
L.M. Barker, M.R. Best., & M. Domjan (Eds.), Learning mechanisms in food
selection. Waco, Texas: Baylor University Press.
Hogan, J.A. (1980). Homeostasis and behavior. In F.M. Toates, & R.R. Halliday (Eds.),
Analysis of motivational processes. London: Academic Press.
Holman, E.W. (1975). Immediate and delayed reinforcers for flavour preferences in rats.
Learning and Motivation, 6, 9 1 - 1 00.
Le Magnen, J. (1969). Peripheral and systemic actions of food in the caloric regulation
of intake. Annals of the N.Y. Academy of Science, 57, 1 126-1 156.
Le Magnen, J. (1971). Advances in studies on the physiological control and regulation
of food intake. In E. Steller, & J.M. Spraque (Eds.), Progress in physiological
psychology (Vol. 4). New York: Academic Press.
Le Magnen, J. (1985). Hunger. Cambridge, U.K.: Cambridge University Press.
Le Magnen, J. (1987). Palatability: Concept, terminology and mechanisms. In R.A.
Boakes, D.A. Popplewell, & M.J. Burton (Eds.), Eating habits. Chichester: John
Wiley.
Le Magnen, J., Marfaing-Jallat, P., & Miceli, D. (1980). A bioassay of
ethanol-dependence in rats. Pharmacology, Biochemistry and Behavior, 12,
707-709.
Logue, A.W. (1979). Taste aversion and the generality of laws of learning. Psychological
Bulletin, 86, 276-296.
26 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
Marfaing-Jallat, P., & Le Magnen, J. (1979). Ethanol-induced taste aversion in
ethanol-dependent and normal rats. Behavioral and Neural Biology, 26, 106-114.
Mehiel, R., & Bolles, R.C. (1984). Learned flavour preferences based on caloric
outcome. Animal Learning and Behavior, 12, 421-427.
Revusky, S.H. (1967). Hunger level during food consumption: Effects on subsequent
preference. Psychonomic Science, 7, 109-110.
Revusky, S.H. (1968). Effects of thirst level during consumption of flavoured water on
subsequent preference. Journal of Comparative and Physiological Psychology, 66,
111-119.
Revusky, S.H. (1974). Retention of learned increase in the preference for flavoured
solution. Behavioral Biology, 11, 121-1254.
Riley, A.L., & Tuck, D.L. (1985). Conditioned taste aversions: A bibliography. In N.S.
Braveman, & P. Bronstein (Eds.), Experimental assessments and clinical
applications of conditioned food aversions. Annals of the N.Y. Academy of Science,
443, 381-437.
Rozin, P. (1977). The significance of learning mechanisms in food selection: Some
biology, psychology and sociology of science. In L.M. Barker, M.R. Best, and M.
Domjan (Eds.), Learning mechanisms in food selection. Waco, Texas: Baylot
University Press.
Sherman, J.E., Hickis, C.F., Rice, A.G., Rusianik, K.W., & Garcia, J. (1983). Preferences
and aversions for stimuli paired with ethanol in hungry rats. Animal Learning and
Behavior, 77, 101-106.
Simbayi, L.C. (1987). Immediate and delayed flavour-calorie learning. Can rats do it?
International Journal of Comparative Psychology, 1, 58-77.
Simbayi, L.C, Boakes, R.A., & Burton, M.J (1986). Can rats learn to associate a flavour
with the delayed delivery of food? Appetite, 7, 41-53.
Smith, G.P., & Gibbs, J. (1979). Postprandial satiety. In J.M. Sprague, & A.N. Epstein
(Eds.), Progress in psychobiology and physiological psychology (vol. 8). New York:
Academic Press.
Van Vort, W., & Smith, G.P. (1983). The relationships between the positive reinforcing
and satiating effects of a meal in the rat. Physiology and Behavior, 30, 279-284.
Internationa! Journal of Comparative Psychology, Vol. 7, No. 1, 1994
LIGHT MEDIATION OF CIRCADIAN
PREDATORY BEHAVIOR IN THE YOUNG
ALLIGATOR
Jack A. Palmer
Linda K. Palmer
Northeast Louisiana University
ABSTRACT: Minnow predation by 10 young American alligators (Alligator
mississippiensis) was systematically measured during four daily time periods under
four different conditions of lighting in order to investigate a circadian rhythm of
predatory behavior. The four daily time periods were night (1:00 a.m. -7.00 a.m.),
morning (7.00 a.m.- 1:00 p.m.), afternoon (1:00 p.m.-7:00 p.m.), and evening (7:00
p.m. -1:00 a.m.). Each of the following lighting conditions had a duration of 4 weeks:
continuous complete darkness (DD); continuous artificial illumination (LL); naturally
varying Ught-dark conditions (natural LD); and reversed light-dark conditions with
artificial lights on at sunset and off at sunrise (reversed LD). Predatory behavior (i.e.,
the number of prey fish consumed wholly or partially during each test session) varied
significantly as a function of the interaction between time period and lighting
condition. Under natural LD, the mean number of prey killed during night sessions
was significantly higher than either morning or afternoon sessions. Under reversed
LD, the pattern of predation reversed from that exhibited under normal Ughting, with
both morning and afternoon predation significantly higher than either evening or
night. Under conditions of continuous illumination (LL and DD) the natural LD
circadian pattern persisted for over 1 week with significantly higher predation rates
during the night periods as compared to the morning and afternoon periods. The
gradual transition of predation pattern in response to manipulations of the light-dark
cycle suggests that the circadian rhythm of alligator predadon is dependent upon
light-dark variation for entrainment.
INTRODUCTION
The adult American alligator {Alligator mississippiensis) has been
described as an opportunistic scavenger as well as an active predator
Address correspondence to Jack A. Palmer, Department of Psychology,
Northeast Louisiana University, Monroe, LA 71209, USA.
© 1994 International Society for Comparative Psychology 27
28 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
(Mcllhenny, 1976; Pooley, 1989; Weldon, Swenson, Olson, &
Brinkmeier, 1990). Hatchling alligators eat insects, small crustaceans,
and small fish (Coulson & Hernandez, 1983), whereas adult alligators
prey upon frogs, snakes, birds, muskrats, nutria, and larger mammals
(Mcllhenny, 1976; Pooley, 1989; Ross & Magnusson, 1989; Scott &
Weldon, 1990). The alligator is generally considered a nocturnal
species with most of its feeding behavior and general activity taking
place during the night (Lang, 1976; Mcllhenny, 1976; Murphy, 1981;
Pooley, 1989). Alligator predatory behavior appears to follow a
circadian rhythm, but this has not been systematically investigated and
reported.
In almost all vertebrates, endogenous circadian rhythms regulate
temporally certain types of behavior (e.g., sleep) and bodily functions
(e.g., hormone secretions, Aschoff, 1989). The rhythm itself is often
entrained or synchronized by environmental cues such as daily cycles
of light-dark and temperature change (Aschoff, 1989; Griffiths, 1986).
These environmental cues that set the timing of circadian behavior are
referred to as zeitgebers (Aschoff, 1989). Aschoff reports that the
most powerful of all zeitgebers is a light-dark cycle. In the absence
of zeitgebers (e.g., an environment of continuous darkness), circadian
rhythms are free-running and self-sustaining. The free-running
rhythm may cycle every 24 hours, be slightly longer, or slightly
shorter.
In lower vertebrates, light mediates circadian rhythm via the
photosensitive pineal gland. Although alligators lack pineal glands,
studies have indicated that some circadian rhythms in alligators are
controlled or mediated by light cycles. Circadian rhythm of young
alligator motor activity was documented by Kavaliers and Ralph
(1980). Lang (1976) found that movement between land and water in
juvenile alligators varied as a function of circadian rhythm cued by
light-dark cycles. A study by Murphy (1981) indicated the existence
of an endogenous clock synchronized by the circadian light-dark cycle
which enabled young alligators to use solar compass orientation.
Kavaliers (1980) demonstrated that extraretinal responses to light
pulses varied according to circadian phase. Moreover, photoperiod
manipulation indicated exogenous entrainment of the extraretinal
responses by light-dark cycles. In light of the alligators' lack of a
pineal gland, Kavaliers and Ralph (1981) argued that overall
organization of circadian rhythm and period length depends on a
complex interaction of retinal inputs, extraretinal inputs, and other
neural areas.
This study sought to determine if alligator predation was subject
JACK PALMER AND LINDA PALMER
29
to circadian rhymicity. Minnow predation (i.e., number of minnows
wholly or partially consumed) by young alligators was systematically
measured during four daily time periods under different conditions of
lighting. It was hypothesized that predation rates would peak during
the dark periods of 24-hour natural and reversed light-dark cycles, and
that an endogenous circadian rhythm would persist under continuous
illumination. It was predicated that the circadian fluctuation could be
altered by manipulating the light-dark cycle, thus supporting
dependence upon light-dark alternation as a zeitgeber. A gradual
transition of predation pattern in response to light-dark cycle
manipulations would indicate entrainment by a light-dark zeitgeber.
TABLE 1
Subject Size After the Study Compared with Number of Prey
Captured During 6-Hr Sessions
Subject Size
Number of Prey
Captured
Range
Mean
Subject
Length
Weight
SD
1
46.0
304.0
0-9
1.89
2.28
2
46.5
285.5
0-10
2.77
2.94
3
42.5
215.0
0-10
2.57
2.97
4
42.5
203.5
0-10
2.36
2.78
5
41.9
208.5
0-10
2.28
2.84
6
38.5
176.5
0-9
2.16
2.37
7
39.0
164.0
0-6
1.59
1.84
8
44.0
228.5
0-10
2.71
2.94
9
37.0
148.5
0-5
1.65
1.73
10
38.0
151.5
0-10
2.08
2.48
METHOD
Subjects
Ten 1990 hatchling alligators {Alligator mississippiensis), 27 to 29
cm in length and weighing 56 to 80 gm, were obtained from the
Rockefeller Wildlife Refuge, Grand Chenier, Louisiana when they
30 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
were approximately 1 month of age. (Age is approximate because
exact date of hatching is not known). Testing began when subjects
were approximately 6 months old and continued until subjects were
approximately 14 months old. At the completion of testing, subjects
ranged from 37 to 46 cm in length and 148.5 to 304 gm in weight
(Table 1). Individual subjects were identified by removing a specific
tail scute.
Maintenance
When not being tested, all 10 alligators were maintained in a
home pool measuring 45.72 cm deep and 2.44 m in diameter. Ten
cm of water covered the bottom, and a 60.96 cm diameter gravel-
surfaced concrete "island" was situated near the center of the pool.
The pool was retained in a heated- enclosed garage with windows
facing north and east. Air temperature ranged from 21 to 28°C with
an average of 25°C. Water temperature ranged from 20 to 27°C with
an average of 24°C. The pool was drained and filled with fresh water
as necessary (usually once each week).
Food included two species of live minnows (Notropis cornutus
and Cyprinus Idas idus) and Burris Alligator Feed. Alligators were
permitted to obtain live prey (minnows) beginning when they were 2
months old. Once testing began, live prey was available only in the
testing arenas during test sessions. Burris Alligator Feed was
provided ad libitum in the home pool.
Live minnows were obtained as needed (about every 2 weeks)
from local bait shops and fish supply outlets. They were maintained
in a plastic barrel, 55.88 cm in diameter and 71.12 cm high, filled
with water. Aeration was furnished by an electric Second Nature
Whisper 400 aquarium pump. Water and air temperature were the
same as that for the alligators. The minnows were fed an adequate
amount of Wardley Tropical Flakes fish food every evening.
Apparatus
Each test arena consisted of a plexiglass tray 45.72 cm x 25.4 cm
X 12.7 cm high with a grill-type metal lid that allowed air circulation
but prevented escape. Each arena was filled with 7.62 cm of water.
The test arenas were located in the same room as the alligator home
pool. Water temperature was the same as that in the home pool.
JACK PALMER AND LINDA PALMER 31
Procedure
All subjects were tested under all conditions. A two-factor (4 x
4) within-subjects experimental design was used, with one factor
(daily time period) nested within the other factor (lighting condition).
The four lighting conditions were continuous complete darkness
(DD), continuous artificial illumination (LL), naturally varying light-
dark (natural LD), and reversed light-dark with artificial light on at
sunset and off at sunrise (reversed LD). Each lighting condition was
maintained for 4 weeks, and each followed a 2-week period of natural
lighting to control for carryover effects. (Kavaliers and Ralph [1980]
demonstrated that, following light manipulation, 10 days of natural
light were sufficient to restore normal circadian rhythmicity of
alligator motor activity).
Artificial illumination was provided by a Power-Glo 40-watt full
spectrum fluorescent lamp. When necessary to shut out natural light,
the windows were covered with black shades taped tightly against the
walls so that no light could enter.
A total of 640 predation test sessions of 6-hour duration were
conducted (160 test sessions per lighting condition). Predation test
sessions were alternated randomly among four time periods: night
(1:00 a.m.-7:00 a.m.), morning (7:00 a.m.- 1:00 p.m.), afternoon (1:00
p.m. -7:00 p.m.), and evening (7:00 p.m.- 1:00 a.m.). No time period
was repeated until the other three had been used. All four time
periods were tested each week.
Because movement between land and water has been
demonstrated to follow a circadian pattern itself (Lang, 1976),
alligators and prey animals were placed in test arenas to control for
this possible confound. Each test session was conducted as follows:
ten minnows, five specimens each of Notropis cornutus and Cyprinus
idus idus, were moved with a net by the investigator from their home
barrel to a test arena at the beginning of the designated 6-hr time
period. An alligator was then carried by the investigator by hand
from its home pool to the test arena. A grill-type metal lid was then
placed on the test arena. During the 6-hr test session, the animals
were not disturbed. At the end of the session, the number of prey
killed (i.e., number of minnows missing or partially consumed) was
recorded. The alligator and remaining minnows (if any) were then
returned to their respective homes. The water in the test arena was
emptied and replaced with fresh water after each test session.
32
RESULTS
INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
The dependent variable, number of minnows consumed wholly or
partially, was analyzed with a repeated measures analysis of variance
(ANOVA), in which time period and lighting condition were
independent variables (both repeating) with time periods nested within
lighting conditions. Predatory behavior varied significantly as a
function of the interaction between time period and lighting condition,
F(9,270) = 15.79, /?<.001. Mean prey killed for each time period
within each lighting condition are reported in Table 2.
TABLE 2
Means and Standard Deviations of Prey Killed During Time
Periods Under Different Lighting Conditions
Time Periods
Lighting Conditions
Night
Morning
Afternoon
Evening
Continuous Dark
Mean
0.393
0.260
0.065
0.203
SD
(0.507)
(0.404)
(0.227)
(0.377)
Continuous Light
Mean
2.775
2.975
2.800
2.350
SD
(2.769)
(3.109)
(2.757)
(2.107)
Natural Light
Mean
2.700
1.300
1.250
2.075
SD
(2.221)
(1.488)
(1.256)
(1.542)
Light Reversal
Mean
2.600
4.500
4.600
1.750
SD
(1.646)
(2.491)
(3.177)
(1.932)
Figure 1 compares the predation patterns that occurred under
natural LD and reversed LD cycles. Tukey HSD multiple
comparisons showed that under natural LD the mean number of prey
killed at night was significantly higher than either morning (p<.0\) or
afternoon (p<.0\). Although mean number of prey killed was higher
during evening than either morning or afternoon, the differences were
JACK PALMER AND LINDA PALMER 33
40 -1
5 30
0)
0)
^ 20
o
u
10
Natural LD
Reversed LD
' I 1 I I
Afternoon Evening Night Morning
Figure 1. Circadian predatory behavior patterns under lighting conditions
natural and reversed LD.
not significant. Kill rates for evening and night sessions did not differ
significantly from each other. Morning and afternoon kill rates also
did not differ significantly from each other.
Under reversed LD conditions, the pattern of predation reversed
from that exhibited under natural LD. Tukey HSD multiple
comparisons revealed that morning predation was significantly higher
than either night (p<.00\) or evening predation (p<.00l). Afternoon
predation was also significantly higher than either night (p<.00\) or
evening predation (p<.00\). The reversed LD condition produced no
significant differences between morning and afternoon predation.
However, night predation was significantly higher than evening
predation (p<.05).
Under DD, night predation was significantly higher than afternoon
predation (p<.01). Under LL, no significant differences were found
among the time periods.
The data for the initial week under each of the two constant
conditions, LL and DD, were examined to see to what degree the
natural LD pattern persisted. Figure 2 illustrates that the natural
predation pattern did persist during the first week of LL and DD with
predation rates peaking during night periods. Tukey HSD multiple
comparisons determined the following significant differences. Under
DD, night predation was significantly higher than after noon (p<.Q5)
34
INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
Afternoon Evening Night Morning
Figure 2. Circadian rhythm of predation during the first week of LL, DD, and
natural LD conditions.
predation. Under LL, night predation was significantly higher than
morning (jx.Ol), afternoon (p<.0\), and evening (p<.05) predation.
Table 1 displays the mean number of prey killed by each subject.
Predation rates of the 10 subjects were analyzed with a one-way
ANOVA to determine if predation differed among subjects. No
significant differences were found.
DISCUSSION
Alligators as young as 2 months of age are capable of capturing
very active prey. The evidence accrued in this study suggests that
predatory behavior in the young alligator varies as a function of light-
mediated circadian rhythm. Light plays a critical role, as predation
during dark periods was significantly higher than during light periods,
whether lighting conditions were natural or reversed. Predation rates
during natural and reversed LD climaxed during the second
contiguous time period of darkness (i.e., night period of natural LD
and afternoon period of reversed LD). This suggests that, in the wild,
predatory behavior of the young alligator reaches a peak during the
hours before dawn, declines sharply after daybreak, remains low
throughout the day, and then rises steadily after nightfall. Such an
JACK PALMER AND LINDA PALMER 35
activity cycle is similar to the circadian rhythms of alligator motor
activity found in other research (Kavaliers, 1980; Kavaliers & Ralph,
1980, 1981; Lang, 1976).
Aschoff (1989) describes circadian rhythms as "self-sustaining
oscillations", and the test for such persistence is a recording of the
activity under continuous non-varying illumination. Under DD, a
predation pattern similar to natural LD persisted (i.e., night predation
was significantly higher than afternoon), although predation was
relatively suppressed during all time periods (see Table 2).
Examination of predation rates of the first week under conditions of
LL and DD showed that a general pattern of circadian rhythm, similar
to the natural LD pattern, persisted. During the second week of LL,
the pattern became arhythmic. This is in accord with Kavaliers and
Ralph's (1980) study where the free-running circadian rhythm of
alligator motor activity became arhythmic after 10-15 days of LL.
The suppression of predation during DD may have been due to
melatonin, a hormone that increases during periods of darkness
(Galluscio, 1990) and appears to regulate cycles of sleep and activity
in many animals (Wurtman & Lieberman, 1987). Melatonin is
present in the blood of alligators (Gern, Owens, Ralph, & Roth,
1978), but its exact role is not known. In birds, the increase in
melatonin appears to cause a decrease in activity and in body
temperature (Binkley, 1979). Although alligators are poikilotherms,
an increase in melatonin due to continuous darkness may suppress
predatory behavior.
Figure 3 provides further evidence of an endogenous circadian
rhythm of predatory behavior. If the temporal occurrence of the
young alligator's predatory behavior was solely under light stimulus
control with no endogenous circadian rhythm, then an abrupt change
in predatory behavior should occur immediately following light
reversal. However, Figure 3 demonstrates a gradual transition of
predation pattern in response to reversed LD, more indicative of a
circadian rhythm being reprogrammed by the zeitgeber than behavior
cued directly by light. Alligator predation follows a circadian rhythm
and appears to be dependent upon light-dark variation for entrainment.
As an ancient species that has evolved in latitudes subject to
seasonal shifts in photoperiod, the alligator is an excellent subject for
the study of endogenous circadian clocks that are fine tuned by
environmental cues (eg., light-dark, temperature variations). Whether
there is one circadian clock or a number of subordinate circadian
clocks each kept in synchronization with the others by natural
36
INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
0)
en
40 n
30 -
20-
10
Afternoon Evening Night Morning
Figure 3. Transition of circadian predatory pattern from natural LD (solid triangles)
to the first week (open circles) and fourth week (open triangles) of reversed LD.
zeitgebers can only be determined by extensive research. Amphibious
behavior, solar compass time compensation, photoreceptor sensitivity,
motor activity, and predatory behavior all may be controlled by one
"master" circadian clock, or each behavior may have its own
independent circadian clock. Conversely, all of the above behaviors
may reflect variations symptomatic of the animals' activity cycles. To
resolve these issues, it would be necessary to measure continuously
and concurrently all of these behaviors under controlled laboratory
conditions. By manipulating light and temperature cues, it may be
possible to produce desynchronization of the behaviors from each
other thereby demonstrating subordinate circadian clocks for some or
all of these behaviors.
ACKNOWLEDGEMENTS
Grateful acknowledgement is due to Ted Joanen and the
Rockefeller Wildlife Refuge, Grand Chenier, LA for supplying the
alligators for this research. Special acknowledgement is due to Dr
Ethel Tobach, Dr Ernest G Maples and two anonymous reviewers for
their valuable comments.
JACK PALMER AND LINDA PALMER 37
REFERENCES
Aschoff, J. (1989). Temporal orientation: Circadian clocks in animals and humans.
Animal Behavior, 37, 881-896.
Binkley, S. (1979). A timekeeping enzyme in the pineal gland. Scientific American,
240, 66-71.
Coulson, R.A., & Hernandez, T. (1983). Alligator metabolism: Studies on chemical
reactions in vivo. New York: Maxwell House.
Galluscio, E.H. (1990). Biological psychology. New York: Macmillan Publishing
Co.
Gem, W.A., Owens, D.W., Ralph, C.L., & Roth, J.J. (1978). Plasma melatonin from
extra-pineal sites. American Zoologist, 18, 557.
Griffiths, R.A. (1986). Natural environmental cues and circadian rhythms of
behaviour: A perspective. Chronobiology-Intemational, 3, 247-253.
Kavaliers, M. (1980). Circadian rhythm of extraretinal photosensitivity in hatchling
alligators, Alligator mississippiensis. Photochemistry and Photobiology, 32, 67-
70.
Kavaliers, M., & Ralph, C.L. (1980). Circadian organization of an animal lacking a
pineal organ; the young alligator. Alligator mississippiensis. Journal of
Comparative Physiology 139, 287-292.
Kavaliers, M., & Ralph, C.L. (1981). Encephalic photoreceptor involvement in the
entrainment and control of circadian activity of young American alligators.
Physiology and Behavior, 26, 413-418.
Lang, J.W. (1976). Amphibious behavior of Alligator mississippiensis: Roles of a
circadian rhythm and light. Science, 191, 575-577.
Mcllhenny, E.A. (1976). The alligator's life history. Society for the Study of
Amphibians and Reptiles. (Original work published 1935).
Murphy, P. (1981). Celestial compass orientation in juvenile American alligators
{Alligator mississippiensis). Copeia, 3, 638-645.
Pooley, A.C. (1989). Food and feeding habits. In C.A. Ross (Ed.), Crocodiles and
alligators (pp. 76-91). New York: Facts on File, Inc.
Ross, C.A., & Magnusson, W.E. (1989). Living crocodilians. In C.A. Ross (Ed.),
Crocodiles and alligators (pp. 58-73). New York: Facts on File, Inc.
Scott, T.P., & Weldon, P.J. (1990). Chemoreception in the feeding behavior of adult
American alligators. Alligator mississippiensis. Animal Behavior, 39, 398-405.
Weldon, P.J., Swenson, D.J.. Olson, J.K., & Brinkmeier, W.G. (1990). The American
alligator detects food chemicals in aquatic and terrestrial environments.
Ethology, 85, 191-198.
Wurtman, R.J., & Lieberman, H. (1987). Melatonin secretion as a mediator of
circadian variations in sleep and sleepiness. Integrative Psychiatry, 5, 13-14.
International Journal of Comparative Psychology, Vol. 7, No. 1, 1994
PORTIA LABIATA, A CANNIBALISTIC JUMPING
SPIDER, DISCRIMINATES BETWEEN
OWN AND FOREIGN EGGSACS
Robert J. Clark
Robert R. Jackson
University of Canterbury
ABSTRACT: Eggsac recognition was investigated in Portia labiata, a jumping spider
(Salticidae) that routinely feeds on the eggs of conspecifics, but does not normally feed
on its own eggs. In laboratory experiments, we demonstrate that P. labiata females can
discriminate between their own and foreign eggsacs. The cues by which these
discriminations are made are discussed.
INTRODUCTION
Various types of parental care are known in spiders, including
guarding eggs against predators (Eberhard, 1974; Kessler & Fokkinga,
1973; Pollard, 1984; Fink, 1986, 1987; Willey & Adler, 1989), providing
food for young (N0rgaard, 1956; Bristowe, 1958; Kullmann, 1972;
Shear, 1970) and opening the eggsac to allow emergence of spiderlings
(Whitcomb & Eason, 1967). Generally, if a female that does not have
eggs is offered eggs of a conspecific, she will reject, and sometimes eat,
them (Bonnet, 1940; Palmgren, 1944; but see N0rgaard, 1956; Pollard,
1984). Yet females do not normally eat their own eggs.
In vertebrates, the stimuli by which females recognize their own
offspring have been well studied (Fletcher & Michener, 1987), but the
stimuli by which female spiders discriminate between their own eggs and
those of conspecifics have received little attention. Previous studies
suggest that eggsac discrimination by spiders is mediated by one or more
of four cues (Kraft, 1982): (1) tactile cues based on the physical
Address correspondence to Robert J. Clark, Department of Zoology, University of
Canterbury, Christchurch, New Zealand.
38 © 1994 International Society for Comparative Psychology
ROBERT CLARK AND ROBERT JACKSON 39
characteristics of the eggsac; (2) chemical cues associated with the
eggsac's silk; (3) chemical cues associated with the spider's web; (4) cues
based on the geographic location of the eggsac, the web or both.
Portia is a web-building jumping spider that specializes in preying
on other spiders, including conspecifics (Jackson, 1992). Portia females
enter the webs of conspecifics, where they attack or sometimes kill the
resident female, then eat any eggsacs that are left behind (Jackson &
Blest, 1982; Jackson & Hallas, 1986). Upon encountering eggsacs,
Portia females open them by chewing and tugging with their chelicerae,
then using their front pair of legs to rake the eggs forward into their
mouths (Jackson & Blest, 1982).
Portia females have never been observed eating their own eggs. Yet
females leave, then return to their webs during the incubation period
(Jackson & Blest, 1982). Also, incubating Portia females in nature have
been observed to eat eggs of conspecifics (Jackson & Blest, 1982;
Jackson, unpubl. data). This suggests that P. labiata females have
evolved an ability to recognize their own eggs or web. We investigated
this hypothesis using a representative species, P. labiata, from Sri Lanka.
MATERIALS AND METHODS
Standard maintenance procedures were used, as described elsewhere
(Jackson & Hallas, 1986). Tests were carried out in cages with
removable glass sides (Fig lA). An internal metal frame was positioned
inside each cage (Fig IB). Spiders attached their webs to the metal
frame instead of to the glass, enabling the cages to be opened without
damaging webs.
All females used in tests were randomly selected from the laboratory
stock. Though a given female was used in more than one (maximum of
two tests) test, no eggsac-female pair was used more than once. Also, no
eggsac was used more than once, except for instances in which it had
previously been paired with its parent. All eggsacs used in tests were of
approximately (maximum difference of 3 days) matching age.
Before each test, the parent spider (test spiders and spiders that
provided foreign eggsacs and webs) was deprived of contact with its
eggsac and web for a 2-h period. After the 2-h period, the test female
was placed in a cage containing one of the following treatments: (1) the
test female's own eggsac in the test female's own web; (2) the eggsac
and web of another conspecific female ('foreign eggsac in foreign web');
(3) the test female's eggsac in another conspecific female's web ('own
eggsac in foreign web'); (4) the eggsac of another conspecific in the test
40
INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
B
Figure 1. Cage (30 cm x 30 cm x 30 cm) used in testing Portia labiata for eggsac
recognition. A: Wooden outer frame with sliding glass sides, one of which is shown
partially raised. Prey were introduced through the four holes (plugged with corks) on top
of the cage. B: Inner metal frame that is slightly smaller than the inside dimensions of
outer cage. Inner frame is shown separately for clarity, but is normally positioned inside
the outer wooden frame.
female's web ('foreign eggsac in own web'). The test consisted of leaving
the test female in the cage for one week, during which time the eggsac
was checked daily for evidence of having been fed upon.
Treatments 3 and 4 were obtained each time by taking a pair of
incubating females' webs and trading the eggsacs: eggsac of female 1
placed in web of female 2 as close as possible to previous location of
eggsac of female 2, and likewise for eggsac of female 2 placed in web
of female 1 .
RESULTS
Eggsacs encountered by test females in their own webs were treated
differently depending on whether they belonged to the test female or
another conspecific female (x^=47.62, N= 59): test females in their own
webs resumed guarding their own eggsac in 19 out of 20 tests, and ate
the foreign eggsac in only 6 out of 12 tests.
Test females in foreign webs resumed guarding their own eggsacs
ROBERT CLARK AND ROBERT JACKSON 41
in 13 out of 14 tests and ate the eggsacs in 12 out of 13 tests. Eggsacs
which the test female did not resume guarding were invariably eaten.
DISCUSSION
Evidently, P. labiata females can discriminate between their own
eggsac and a foreign eggsac. In the present study, females usually
guarded their own eggs and ate foreign eggs. How widespread eggsac
recognition abilities may be in salticids is unknown because species
other than P. labiata have not yet been studied. However, an ability to
recognize their own eggs may be especially advantageous in Portia
because this is a genus of salticids known to feed frequently on eggs of
other spiders, including conspecifics.
This study raises questions about the cues by which P. labiata
distinguishes between its own and foreign eggsacs. In some vertebrates,
cues from the geographic locations of the eggs are known to be
important (Colgan, 1983). However, for P. labiata, cues other than
location must be of primary importance. In our tests, when females' own
eggsacs were placed in foreign webs, they were not placed in a location
comparable to their original positions in the parent webs but, instead, as
close as possible to the previous location of the foreign eggsac.
Therefore, if the location of the eggsac in the web was the most
important cue for eggsac recognition, then test females would have been
expected often to eat their own eggsacs. However, test females usually
guarded their own eggsacs, instead of eating them, regardless of whether
they were in foreign webs or the females' own webs. Probably, in P.
labiata, eggsac discrimination is based primarily on chemical cues.
However, it is interesting that, when we placed foreign eggsacs in
the webs of test females, the test females accepted (i.e., did not eat) the
foreign eggsac half the time. Yet, when test females encountered foreign
eggsacs in foreign webs, they usually ate them. This suggests that cues
from the female's own web are important in addition to cues from her
eggsac. It is probably unlikely in nature for a female to encounter
foreign eggs in her own web and, therefore, it might be advantageous for
females to be reluctant to eat eggsacs encountered in their own webs,
despite dissenting chemical cues.
42 INTERNATIONAL JOURNAL OF COMPARATIVE PSYCHOLOGY
ACKNOWLEDGEMENTS
We thank Andrew McLachlan, Mary Whitehouse and Philip Taylor
for useful comments on the manuscript and Tracey Robinson for her
invaluable help in the preparation of the manuscript. Financial support
was provided by grants from the National Geographic Society (3226-85)
and the U.S. -New Zealand Cooperative Program of the National Science
Foundation (BNS 8657078). Import permits were provided by the New
Zealand Ministry of Agriculture and Fisheries.
REFERENCES
Bonnet P. (1940). L'instinct maternal des araignees a I'epreuve de I'experimentation.
Bulletin Societe d'Histoire Naturelle Toulouse, 81, 185-250.
Bristowe, W.S. (1958). The World of Spiders. London: Collins.
Colgan, P. (1983). Comparative social recognition. New York: John Wiley & Sons.
Eberhard, W.G. (1974). Maternal behaviour in a South American Lyssomanes. Bulletin
of the British Arachnological Society, i, 51.
Farley, C, & Shear, W.A. (1973). Observations on the courtship behaviour of Lycosa
carolinensis. Bulletin of the British Arachnological Society, 2, 153-158.
Fink, L.S. (1986). Costs and benefits of maternal behaviour in the green lynx spider
{Oxyo^xdois., Puecitia viridans). Animal Behaviour, 34, 1051-1060.
Fink, L.S. (1987). Green lynx spider egg sacs: source of mortality and the function of
female guarding (Araneae, Oxyopidae). Journal of Arachnology, 15, 231-239.
Fletcher, D.J.C., & Michener, CD. (1987). Kin recognition in animals. Chichester: John
Wiley & Sons.
Jackson, R.R. (1992). Eight-legged tricksters: spiders that specialize at catching other
spiders. BioScience, 42, 590-598.
Jackson, R.R., & Blest, A.D. (1982). The biology of Portia fimbriata, a web building
jumping spider (Araneae, Salticidae) from Queensland: utilization of webs and
predatory versatility. Journal of Zoology, 196, 255-292.
Jackson, R.R., & Hallas S.E.A. (1986). Comparative biology of Portia africana, Portia
albimana, Portia fimbriata, Portia labiata, Portia schultzi, araneophagic jumping
spiders (Araneae, Salticidae): utilisation of webs, predatory versatility and
intraspecific interactions. New Zealand Journal of Zoology, 13, 423-489.
Kessler, A., & Fokkinga. A. (1973). Hymenopterous parasites in eggsacs of spiders of
the genus Pardosa (Araneida, Lycosidae). Tijdschrift voor Entomologie, 116, 43-
61.
Kraft, B. (1982). The significance and complexity of communication in spiders. In P.N.
Witt & J.S. Rovner (Eds.), Spider communication: mechanisms and ecological
significance. Princeton: Princeton University Press.
Kullman, E.J. (1972). Evolution of .social behavior in spiders (Araneae: Eresidae and
Theriididae). American Zoologist, 12, 419-426.
N0rgaard E. (1956). Environment and behavior ot'Theridion saxatile. Oikos, 7, 159-162.
Palmgren, P. (1944). Uber die brutpfleginstincthandlung der wolfspinnen. Societas
Scientiarum fennica-Commentationes Biologicae, 9, 1-19.
ROBERT CLARK AND ROBERT JACKSON 43
Pollard S.D. (1984). Egg guarding by Clubiona cambridgei (Araneae, Clubionidae)
against conspecific predators. Journal of Arachnology, ]], 323-326.
Shear W.A. (1970). The evolution of social phenomena in spiders. Bulletin of the British
Arachnological Society, 1, 65-76.
Whitcomb W.H., Eason R. (1967). Life history and predatory importance of the striped
lynx spider (Araneida, Oxyopidae). Proceedings of the Arkansas Academy of
Science, 21, 49-58.
Willey, M.B., & Adler P.H. (1989). Biology of Peucitia viridans (Aranae, Oxyopidae)
in South Carolina, with special reference to predation and maternal care. Journal
of Arachnology, 17, 275-284.
The International Society for Comparative Psychology
Announces its Seventh International Conference
July 4-8, 1994 at the University of Sao Paulo, Brazil
Registration and program information may be obtained from:
Cesar Ades
ISCP Local Organizing Committee
Dept. Experimental Psychology
Av. Prof. Mello Moraes 1721
Sao Paulo 05508-900 BRAZIL
Fax: 81 38895
E-mail: cades@fox.cce.usp.br
To obtain the following publications, write to Ethel Tobach, American
Museum of Natural History, Central Park West at 79th Street, New
York, NY 10024-5192, USA (bitnet: etthc@cunyvm; Fax: 212 769
5233).
ISCP PUBLICATIONS:
Historical Perspectives and Contemporary Status of Comparative
Psychology
Advances in Comparative Psychology
Volume 1: The Comparative Psychology of Natural Resource
Management: Costa Rica
Volume 2: Australian People and Animals in Today's Dreamtime
AVAILABLE FOR MAILING COST ONLY:
Experimental Studies of Elementary Reasoning: Evolutionary,
Physiological and Genetic Aspects of Behavior by L. V. Krushinsky,
late Chair of Higher Nervous Activity in the Biological Faculty of
Moscow State University (1990).
INTERNATIONAL SOCIETY FOR
COMPARATIVE PSYCHOLOGY
AN AFFILIATE OF THE INTERNATIONAL UNION OF PSYCHOLOGICAL SCIENCES
1994 MEMBERSHIP APPLICATION FORM
I I New Member I I Renewing Member I I
(Must complete entire form)
Renewing Member
(Complete sections A&B)
Change of Address
(Complete section A)
Al.
APPLICANT DETAILS
LAST
FIRST OTHER INITIAL DEGREE(S)
DEPARTMENT
E-MAIL ADDRESS
INSTITUTION
STREET
CITY
STATE ZIP
(I'OUNtRY
TELEPHONE (Include International Codes)
( ) ( )
DAYTIME FAX
A2. AREA OF INTEREST
NEW MEMBERS
Please ensure that your
application is endorsed by
a current ISCP non-student
member;
MaME of endorser (Please print)
SIGNATURE OF ENDORSER
STUDENT MEMBERS
For continuing student
members and new student
applicants:
SUPERVISORS NAME (Please
prim)
SUPERVISORS SIGNATURE
COURSE OF STUDY
B. MEMBERSHIP CATEGORY
All categories include subscription to the International Journal of Comparative Psychology
LJ Professional Individual interested in the teaching, theoretical development and
experimental investigation of comparative psychology
n New Member Entry Level $30
LJ Renewing Member $50
I I Retiree Professional member who retires or is without financial support. . . . $30
I — I Family Two members who have the same mailing address and require only
one subscription to the International Journal of Comparative Psychology .... $50
LJ Student Individual enrolled at an institution of higher learning in a
scientific field related to comparative psychology $30
PAYMENT INFORMATION
The 1994 membership year is January 1 to December 31, 1994. We only accept
payment in U.S. dollars drawn on U.S. banks. Please make cheques payable to
the International Society for Comparative Psychology and send to:
Dr S.A. McFadden, ISCP Secretary/Treasurer
Departnnent of Psychology • The Univ. of Newcastle • NSW 2308 • AUSTRALIA
Fax +61 (49) 216980 • E-Mail: McFadclen@psychology.newcastle.edu.au
Instructions to Authors
All manuscripts are reviewed by two readers other than the Editors. Authors
should send three copies of their manuscripts to either their National Editor or
to the Editor (Hughes). One diskette copy saved in ASCII format or as a
standard word processor file, will subsequently need to be submitted to the
Editor once the manuscript is accepted for publication. Indicate clearly on the
diskette the author(s) name, file format and program version number. (Alternate
arrangements may be possible for those authors who are unable to provide a
diskette copy).
The manuscript should have a cover page with the full title, the author(s)
name(s) and address(es) and should indicate the person with whom the Journal
may correspond. If the author(s) has(ve) an electronic mail address or fax
number, these should be given in a covering letter accompanying the
manuscript. The abstract should be on a separate page. All articles are
published in English; the author(s) should also submit an abstract in their
language if it does not require non-Roman type. Author(s) are responsible for
the accuracy of the non-English abstract. Acknowledgements should appear on
a separate page and carry the title of the article and the author(s) name(s). If
the author(s) prefer(s) anonymity in the review process, this should be stated in
a covering letter and the manuscript, abstracts, and illustrative material should
carry only the title of the article. The cover sheet and acknowledgements will
not be sent to the reviewers in this instance.
GENERAL REQUIREMENTS: Logical organization is essential. While
headings help to structure the content, titles and headings within the manuscript
should be as short as possible. Tables and figures should not be redundant.
Illustrative material should be self-explanatory and used sparingly. Tables and
figures must be in camera-ready condition and include separate captions. Only
items cited in manuscripts should be listed as references. Page numbers must
be provided for direct quotations. Footnotes should not be used except in
special circumstances and with permission of the Editor.
MANUSCRIPTS should be double-spaced, the original on white bond paper,
with margins of 3 cm on all four edges and approximately 26 lines to the page.
Manuscripts longer than 20 typed pages (not counting figures, tables, and
references) will only be considered in unusual circumstances. The style manual
of the American Psychological Association (3rd Edition, 1983) is to be
followed. If the manual is not available, authors may write to the Editor
(Hughes) for a style sheet. Manuscripts which do not meet the style
requirements will be returned for retyping.
REFERENCES should be listed on a separate page and referred to in the text
by author(s) and year of publication as in the Publication Manual of the
American Psychological Association.
International Society for Comparative Psychology
Live Music Archive
Librivox Free Audio
Metropolitan Museum
Cleveland Museum of Art
Internet Arcade
Console Living Room
Books to Borrow
Open Library
TV News
Understanding 9/11