Individual sibling recognition in experimental broods of common tern chicks
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ANIMAL BEHAVIOUR, 1999, 58, 375–381
Article No. anbe.1999.1135, available online at http://www.idealibrary.com on
Individual sibling recognition in experimental broods of
common tern chicks
BRIAN G. PALESTIS & JOANNA BURGER
Department of Ecology, Evolution and Natural Resources, Rutgers University
(Received 14 January 1999; initial acceptance 23 February 1999;
final acceptance 30 March 1999; MS. number: A8224R)
Studies of kin recognition in birds have usually examined parent–offspring recognition, while studies of
sibling recognition are relatively rare. Using choice experiments, we studied the development of sibling
recognition among common tern, Sterna hirundo, chicks and tested the cues used for recognition. We
collected newly hatched common tern chicks and raised them in a laboratory in 10 artificial broods of
three. Chicks showed a significant preference for broodmates (‘siblings’) over familiar nonsiblings
(nonsiblings from neighbouring broods) when first tested at 4 days posthatching, earlier than previously
reported. Preferential approach to siblings was most common in broods with low levels of intrabrood
aggression. Responsiveness of test chicks was highest when test chicks and stimulus chicks could both see
and hear each other and lowest when they could only hear each other. Sibling-biased approach did not
depend on stimulus and test chicks seeing each other, only on test chicks seeing (and probably hearing)
stimulus chicks. Surprisingly, no preference was shown for siblings over strange nonsiblings, suggesting
that a preference for siblings may involve learning the identity of not only siblings, but also of chicks
from neighbouring broods.
1999 The Association for the Study of Animal Behaviour
Kin recognition has been a major focus of behavioural discriminate between nestmates and non-nestmates in
research during the past two decades, and the ability to the laboratory, and between recorded sibling and non-
discriminate kin from nonkin has been demonstrated in sibling begging calls in the field. Tern chicks are highly
many species of mammals, birds, anuran amphibians, variable in appearance, particularly in down coloration
social insects, colonial invertebrates and others (Fletcher (Buckley & Buckley 1970), and this variation may be used
& Michener 1987; Pfennig & Sherman 1995). Discrimi- by parents to recognize offspring (Shugart 1990). Multiple
nation of kin from nonkin can be important in determin- cues and sensory modalities are often used in recognition
ing the distribution of positive and negative interactions (Colgan 1983; Halpin 1991). It is therefore possible that
among members of social groups. However, avian kin visual cues also play a role in common tern sibling
recognition studies have focused largely on parent– recognition. Burger et al. (1988), although originally
offspring recognition, and thus studies of recognition of demonstrating discrimination among chicks that could
siblings or other collateral kin by birds are relatively rare both see and hear each other, only tested the importance
(reviews in Evans 1980; Beecher 1988; Halpin 1991). of auditory cues.
Tests for sibling discrimination among the Laridae Sibling recognition in colonial birds may help chicks to
(gulls and terns) have consistently demonstrated its locate their own nests quickly, thus avoiding aggression
presence (Evans 1970; Noseworthy & Lien 1976; Burger from unrelated adults and avoiding missed opportunities
et al. 1988; Pierotti et al. 1988; Burger 1998). Preferences for parental feeding, in an environment where many
for siblings are learned, as is typical of avian kin recog- nests (and thus broods) are found within a small area
nition (Beecher 1988), thus chicks appear to treat nest- (Evans 1970; Noseworthy & Lien 1976; Beecher &
mates as siblings regardless of actual relatedness (Burger Beecher 1983; unpublished data). Sibling recognition,
et al. 1988; Pierotti et al. 1988). Burger et al. (1988) therefore, should develop before the age at which young
demonstrated that common tern, Sterna hirundo, chicks begin wandering from the nest (Evans 1970; Beecher &
Beecher 1983; see also Holmes & Sherman 1982). In
Correspondence: B. G. Palestis, Rutgers University, Department of ground-nesting species, like the common tern, the poten-
Ecology, Evolution and Natural Resources, Nelson Biological Labs, tial for wandering into a neighbouring territory is high,
604 Allison Road, Piscataway, NJ 08854-8082, U.S.A. (email: and thus this proposed benefit of sibling discrimination
palestis@eden.rutgers.edu). should be particularly important. We have demonstrated
0003–3472/99/080375+07 $30.00/0 375 1999 The Association for the Study of Animal Behaviour376 ANIMAL BEHAVIOUR, 58, 2
(unpublished data) that 4-day-old common tern chicks in We placed the cages containing the chicks in a chick
the field are better able to locate their natal nests when brooder set to 30C for the first week of captivity. After
siblings are present in the nest than when chicks have no the first week, we kept chicks warm with space heaters.
siblings or when siblings have been temporarily removed, Each cage contained paper bedding, which we changed
moved to a neighbouring nest, or replaced by a non- daily, and was always adjacent to the same neighbouring
sibling. Other proposed benefits of sibling discrimination cages. Chicks could both see and hear chicks in neigh-
among larid chicks include prevention of adoption of bouring broods (typically two or three broods), but could
unrelated chicks (Holley 1988; but see Pierotti et al. not see chicks in the remaining broods, separated at first
1988), avoidance of aggression from nonsiblings (Burger by the shelves of the brooder and later by cardboard
1998; Burger et al. 1988), maintenance of cohesive family barriers.
groups for efficient provisioning of food (Evans 1970, We fed the chicks five times per day by hand, with bait
1980), and approach to sibling begging calls to maximize fish species (Fundulus spp. and Menidia menidia) that are a
food intake (Burger et al. 1988). These proposed benefits part of the natural diet of tern chicks. We weighed the
of sibling recognition also suggest that discrimination is chicks periodically, and most grew throughout the study.
adaptive at an early age. However, Burger et al. (1988) Any chicks that stopped growing or were in poor con-
found no evidence for sibling discrimination in common dition were separated from their broods, and we no longer
terns at 8 or 9 days of age, when chicks are already highly used them as either test chicks or stimulus chicks in the
mobile, but did demonstrate sibling discrimination experiments outlined below. We aborted additional
among 12-day-old chicks. experiments when several chicks developed a thiamine
In this study we confirm that common tern chicks (vitamin B1) deficiency. Supplementation of the diet with
learn the identity of their nestmates (‘siblings’) and crushed vitamin B1 tablets prevented further cases, and
preferentially approach nestmates over non-nestmates, led to the rapid recovery of some affected chicks (B. G.
and we demonstrate that this preference develops earlier Palestis, J. Burger & M. Gochfeld, unpublished data). On
than previously reported by Burger et al. (1988). We also 23 July 1997 we killed all surviving chicks under the
demonstrate the importance of visual cues in sibling supervision of a veterinarian (R. Harris). We felt that any
recognition indirectly, by comparing approach responses chicks raised without exposure to adult terns and released
when chicks can both see and hear each other to into the wild would have died of starvation, because tern
approach responses when only auditory cues are avail- fledglings must learn how to fish (LeCroy 1972) and
able. Kin recognition studies usually fail to control for probably require feeding from their parents even after
behavioural cues (Gamboa et al. 1991), but the behaviour fledging (Ashmole & Tovar 1968; Burger 1980).
of larid chicks may be of overriding importance in The Rutgers University Institutional Review Board for
discrimination by parents (Halpin 1991). We test the the Use and Care of Animals approved the rearing and
importance of behavioural, nonvocal interactions among experimental protocol (amendment to protocol 86-016),
chicks in sibling discrimination with the use of one-way and chicks were collected under the appropriate state and
mirrors. Furthermore, we compare discrimination among federal permits (PRT 674091).
familiar and unfamiliar individuals to discrimination
among familiar individuals (true individual recognition).
Experiment 1: Visual and Auditory Contact
We also test whether preferences exist for particular
individuals within a brood, as occurs among budgerigar, The first experiment tested whether chicks could dis-
Melopsittacus undulatus, chicks (Stamps et al. 1990). criminate siblings from nonsiblings when test and stimu-
Finally, we compare approach responses among broods lus chicks could both see and hear each other. Choice
with varying levels of within-brood competitive tests began when chicks were 4 days old, and had
aggression. therefore been with their siblings for only 3 days. We
placed test chicks in the middle of a rectangular box
METHODS (99.140.6 cm) inside an inverted cup. We placed stimu-
lus chicks (one sibling and one nonsibling) in separate,
We collected 30 newly hatched common tern chicks from transparent mouse cages 56 cm apart, behind cardboard
30 different nests, spread over three colonies in Barnegat dividers. Test chicks and stimulus chicks could hear each
Bay, New Jersey, on 7 July 1997. All chicks were less than other and frequently called, but could not see each other
1 day old, but were no longer wet from hatching. In until removal of the cardboard dividers. We did not place
the laboratory, we weighed and banded the chicks, and siblings consistently on the left or right side of the arena,
placed them in clear plastic mouse cages in groups of to control for any direction preferences. All nonsiblings
three, the natural brood size. Because we did not remove were familiar nonsiblings (i.e. chicks from neighbouring
more than one chick from a given nest, to avoid adversely broods). We hid from view and, after allowing 30 s for
affecting the productivity of the colonies, broodmates habituation, removed the cup and the cardboard dividers
were not true siblings. However, broodmates were raised remotely. We recorded latency to first movement, any
together from less than 1 day posthatching, and were position changes, any calling by test or stimulus chicks
mostly first-hatched chicks with no experience with their and the time the test chick spent in each of four equal
true siblings other than exposure to prenatal vocaliz- sections of the arena (0–14 cm from sibling’s cage,
ations (Saino & Fasola 1996). We will refer to laboratory 14–28 cm from sibling’s cage, 14–28 cm from non-
broodmates as ‘siblings’ throughout this paper. sibling’s cage, and 0–14 cm from the nonsibling’s cage).PALESTIS & BURGER: SIBLING RECOGNITION 377
We ended each trial when the test chick had been greater Observations of Intrabrood Aggression
than 14 cm away from either cage for 2 consecutive min
(scored as unresponsive) or stayed within 14 cm from In addition to the choice experiments described above,
either cage for 2 consecutive min (scored as choice made we also observed aggression among siblings within each
for sibling or nonsibling). A trial also ended if the test brood. During feeding, we usually separated siblings from
chick walked back and forth between the two stimulus each other to minimize aggression and to facilitate
chicks repeatedly for 3 min without making a choice unbiased feeding of all three chicks. During one feeding
(scored as ambivalent). We also calculated the proportion session per day, however, siblings were not separated and
of time the test chick spent in each of the four parts of the observations of aggression were recorded. We recorded
arena. the number of pecks and bites directed towards siblings
We used each 4-day-old chick as a test chick once, for 1 min before feeding and 1 min after feeding. If a
resulting in 30 total trials. We repeated this experiment chick grabbed another chick’s leg or wing without letting
on the following day, using each chick as a test chick go, then the two chicks were briefly separated. No injuries
again, but with a different combination of sibling and resulted from this aggressive behaviour. If a chick was
familiar nonsibling stimulus chicks. We analysed the removed from a brood due to poor condition or lack of
data for each day separately, to avoid pooling non- growth, then observations of aggression were no longer
independent data (repeated observations on the same made on that brood, to eliminate differences due to
individuals), a common error in kin recognition studies brood size.
(Gamboa et al. 1991). Data from the two trials were only
combined when comparing preferences among broods, RESULTS
but were averaged to give only one data point per brood
(N=10), thus decreasing statistical power. We followed Sibling discrimination was already present when chicks
the same experimental protocol when the chicks were 10 were first tested at 4 days of age, with both auditory and
days old, but used unfamiliar nonsiblings instead of visual contact among stimulus and test chicks. Signifi-
familiar nonsiblings. cantly more test chicks chose siblings than familiar non-
siblings at this age (Table 1). These chicks also spent
significantly more time in the section of the test arena
Experiment 2: No Visual Cues closest to their siblings than in the section closest to
To examine the importance of visual cues indirectly, we familiar nonsiblings (Fig. 1; Wilcoxon signed-ranks test,
prevented test and stimulus chicks from seeing each sample sizes given in Table 1: Z=3.03, P378 ANIMAL BEHAVIOUR, 58, 2
Table 1. Results of common tern sibling versus nonsibling (familiar, strange) choice tests with auditory and visual
contact among test and stimulus chicks, no visual contact among chicks and unidirectional visual contact
Auditory/visual contact No visual contact One-way mirror
Familiar Familiar Strange Familiar Familiar Familiar Familiar
Age (days) 4 5 10 8 12 7 11
Test chick
Chose sibling* 16 14 6 5 5 11 7
Chose nonsibling 4 7 6 3 2 2 2
Ambivalent 1 3 4 2 2 1 0
Unresponsive 9 6 7 15 12 16 13
Total 30 30 23 25 21 30 22
Probability† 0.005 0.055 0.226 0.219 0.164 0.01 0.07
(0.01) (0.117) (0.122) (0.246) (0.246) (0.022) (0.07)
*We considered a choice to be made when the test chick spent 2 consecutive min in the end (one-fourth of arena
area) of the test arena nearest a stimulus chick. Unresponsive chicks remained in the centre of the test arena for
2 consecutive min, and ambivalent chicks walked back and forth between siblings and nonsiblings for 3 min
without making a clear choice.
†Binomial probabilities, comparing choice of sibling versus choice of nonsibling. The number in parentheses is the
binomial probability if sibling choice is compared to responsive chicks that did not choose their sibling (i.e. chicks
that chose nonsiblings plus ambivalent chicks).
Test chicks spent a significantly larger proportion of (Fig. 2). There was no trend for test chicks that had been
time near siblings than near nonsiblings in both trials used previously as stimulus chicks on a given day to be
(Fig. 1; age 7 days: Z=2.95, PPALESTIS & BURGER: SIBLING RECOGNITION 379
0·7 0·8
0·7
0·6
0·5
Responsiveness
Time near sibling
0·5 0·5
0·4
0·4 0·3
0·2
0·3
0·1
0·2 0
2 4 6 8 10 12 14
Age (days) –0·1
1·5 2 2·5 3 3·5 4 4·5 5 5·5 6
Figure 2. The mean±SE responsiveness of test chicks equals the Prefeeding aggression/min
proportion of time spent near the sibling plus the proportion of
time spent near the nonsibling. h: Auditory/visual contact, includes Figure 3. Mean±SE proportion of time members of each common
treatments with familiar (ages 4 and 5 days) and strange nonsiblings tern brood spent in the section of the test arena nearest their sib-
(10 days) and choice among siblings (6 and 9 days); ◆: no visual lings in relation to mean intrabrood, prefeeding aggression/min.
contact; j: one-way mirror. Y= −0.10X+0.76.
see and hear each other, and mean responsiveness was chicks can recognize their siblings at this age. This is also
relatively high in both trials (Fig. 2). the age at which common tern chicks first discriminate
There was significantly more within-brood aggression between the calls of their parents and those of other
in the minute before feeding than in the minute after adults (Stevenson et al. 1970). Four-day-old common tern
feeding (paired t test: t9 =6.86, P380 ANIMAL BEHAVIOUR, 58, 2
them from seeing neighbouring broods, and the arrange- in the frequency of competitive aggression successfully
ment of broods was randomly changed daily so that the predicts much of the variation among broods in the
identity of neighbours was constantly changing. If sibling proportion of time spent near siblings in the choice tests.
discrimination does indeed involve comparing familiar That chicks in highly aggressive broods are less likely to
nestmates to familiar neighbours, then the rearing proto- approach their siblings than chicks in less aggressive
col of Burger et al. (1988), which was intended to reduce broods may suggest an adaptive response by chicks to
familiarity with neighbours, may have actually led to avoid aggressive siblings. Failure to approach a sibling
discrimination developing late. The lack of a preference and/or a nonsibling in a choice test may not always be
for siblings over strangers needs replication, particularly evidence of a recognition error, but instead may reflect
because this experiment was performed on a different day accurate recognition and avoidance of the sibling. Dis-
than the trials using familiar nonsiblings, and thus used crimination of kin is expected to be context dependent,
test chicks of a different age. and therefore recognition ‘errors’ are also to be expected
We have also demonstrated the importance of visual (Blaustein & Porter 1990; Sherman et al. 1997). However,
cues in common tern sibling discrimination. Burger et al. the behaviour of the test chicks suggested that siblings or
(1988) demonstrated that common tern chicks could nonsiblings were approached, not that one chick was
recognize their siblings based on playback of begging calls avoided. This hypothesis could be tested experimentally
alone. We found no evidence here for discrimination by using only one stimulus chick at a time. It is also
when test chicks could not see stimulus chicks, but, possible that sibling recognition simply did not develop
although calls were present in all visual isolation trials, fully in all of the broods, resulting in high levels of
the calls were not necessarily begging calls and calling aggression in these broods. This nonadaptive hypothesis
was often infrequent. We found chicks to be more is suggested by the fact that the levels of aggression
responsive, and thus more likely to approach siblings, observed in these artificial broods is much higher than is
when they had full auditory and visual contact with observed in the field.
stimulus chicks than when they could only hear stimulus Sibling recognition can have important ecological
chicks. This comparison is complicated by differences in consequences in colonial, ground-nesting birds. We have
the age of the chicks, but responsiveness of test chicks demonstrated that sibling recognition in common terns
when stimulus and test chicks could both see and hear develops early enough for it to benefit chicks when they
each other was relatively high at all ages tested (4, 5, 6, 9 become mobile, and that more than one sensory
and 10 days), while responsiveness of test chicks visually modality is used in discrimination of siblings from non-
isolated from stimulus chicks was very low at both ages siblings. Whether discrimination requires comparison
tested (8 and 12 days) (see Fig. 2). That auditory and among familiar individuals should be tested rigorously, as
visual cues combined are more effective than auditory should the effect of age and relative age on interactions
cues alone has been demonstrated previously for parent– among siblings.
offspring recognition in razorbills, Alca torda (Ingold
1973) and ring-billed gulls, Larus delawarensis (Conover
et al. 1980), and for approach responses towards other Acknowledgments
chicks in ring-billed gulls (Evans 1970). Whether visual The authors thank H. John-Alder, T. McGuire, J.
cues alone can allow sibling recognition among common Spendelow, R. Trivers and the referees for comments on
tern chicks has not been demonstrated. However, in the the manuscript, and M. Gochfeld and R. Harris for advice
auditory and visual contact experiments described here, on the care of chicks. B.G.P. is supported by a Marion
there were six cases in which neither stimulus chick Johnson Fellowship and a teaching assistantship from
called, and, in all three cases when the test chick made a Rutgers University, and J.B. is supported by the Penn
choice, the chick chose its sibling. Foundation through the Trust for Public Lands, CRESP
In the trials using one-way mirrors to separate test and (Department of Energy, AI DE-FC01-95EW55084) and
stimulus chicks, we demonstrated that nonvocal behav- NIEHS (ESO 5022).
ioural interactions among chicks, although important
in maintaining responsiveness, are not necessary for
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