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Local enhancement and seed choice in the juvenile canary, Serinus canarius
Anim.
Behav., 1995, 50, 793-800
Local enhancementand seedchoicein the juvenilecanary, Serinus canarius J. C. CADIEU*, *Laboratoire tLaboratoire
d’Ethologie de Biologie
et de Psychologie Quantitative,
N. CADIEU*
& J. LAUGAt
Animale, URA 1837 CNRS, Universit& Paul Sabatier, Toulouse UMR 9964 CNRS, UniversitC Paul Sabatier, Toulouse
(Received 9 November 1993; initial acceptance 16 February 1994, final acceptance 13 January 1995; MS. number: 4522)
Abstract. The influence of the presence and feeding behaviour of the father on the behaviour of young
canarieswas examined. The naive offspring had accesssimultaneously to canary seedor oat seedsin the sameplace as did the parent, who either did or did not have accessto seeds(canary seeds,oats or hemp). In the absence of an adult, the juveniles took, husked and ate few seeds. The presence of the father increasedthe picking up, husking and ingestion of seedsby the juveniles, who also tended to feed in the sameplace as the parent (local enhancement). The choice of seed was also influenced by the parent’s tehaviour as the young birds picked up more oat seedswhen these seedswere available to the father. Thiswas not observed for canary seeds,which tended to be selected spontaneously by the young birds. Theamounts of canary seedsand oats husked and ingested by the juveniles did not only depend on seed choice.Manipulation of canary seed by the father facilitated its husking by the juvenile, whereas manipulation of oats by the father had no facilitatory effect on the use of this seed by the young birds. Overall,the effects of social facilitation tended to favour ingestion of seedsspontaneously selected by theoffspring. 0 1995The Association for the Study of Animal Fkhaviour Preculturaland social transmission is known to occur in numerous non-human vertebrates, includingmammals, fish and birds (Pallaud 1984; Galef1988; Suboski 1989a; Suboski & Templeton 1989).Although transmission may derive from imitation of experienced conspecifics (NortonGriffiths 1966; Will et al. 1974; Palameta & Lefebvre 1985) simpler processes may also be involved such as social facilitation and local enhancement(Turner 1964; Clayton 1978; Senar & Metcalfe 1988) as well as the use of excretory markers(Laland & Plotkin 1991) or vestiges of certainactivities (Sherry & Galef 1984). In birds, local enhancement is thought to accountfor the transmission of knowledge from an experienced to a naive bird, especially with respectto recognition of edible objects (Thorpe 1956;Suboski 1989a). This process may also be involved during the more complex learning involved in the acquisition of a new technique (Palameta & Lefebvre 1985). Thorpe (1956) definedlocal enhancement as ‘a particular case of Correspondence: N. Cadieu, Laboratoire d’Ethologie et de Psychologie Animale, URA 1837 CNRA, UniversitC PaulSabatier, 118 route de Narbonne. 31062 Toulouse Ctiex, France. 0003-3472/95/090793 +08 $12.00/O
social facilitation during which the attention of the subject is oriented towards a specific object or environmental zone’. This definition, however, does not take account of the tendency of two conspecifics to aggregate, which may also favour social or precultural transmission (Cadieu 1985; Zentall 1988). Furthermore, although birds tend to peck food in the same place as a conspecific, they are able to learn tasks, that cannot be accounted for by simple indication of an environmental cue or by observation of a purely spatial procedure. Thus naive pigeons, Columba livia, can learn by observation of an experienced conspecific to discriminate between a reinforced and a nonreinforced stimulus (Biederman & Vanyan 1988; Zentall 1988); out of two stimuli, hatchling chicks, Gallus gallus domesticus, preferentially peck the stimulus indicated by a pecking arrow (Hogan 1973; Suboski 1989b); ducks, Cairina moschata and Anas platyrhynchos, and red-winged blackbirds, Agelaius phoeniceus, avoid a food item associated with a noxious stimulus purely from observation of a conspecific (miipfer 1957; Mason & Reidinger 1982); and pigeons can learn by observation to pierce a membrane (Palameta & Lefebvre 1985).
C 1995 The Association for the Study of Animal Behaviour 793
794
Animal
Behaviour,
In passerines, feeding traditions have been observed in field studies, especially in tits (Fisher & Hinde 1949; Hinde & Fisher 1951) and finches (Peterson 1961; Newton 1967). Numerous studies have been devoted to the feeding choices of finches, which feed mainly on seeds. They husk the seeds and eat the kernels. The choice of seed has been related to both beak shape and profitability of the food source (Kear 1962; Newton 1967; Ghick 1985; Greig-Smith & Cracker 1986; Greig-Smith 1987; Diaz 1989). In a previous study, we observed social transmission of seed preferences in the canary (Cadieu 1985). This transmission occurred more readily if the young birds were allowed to feed close to their parents, from which they could pick up environmental cues. In the present study we investigated (1) how much the presence of an experienced bird and local enhancement affected the young birds’ preference; (2) whether the young birds could discriminate food sources indicated by the experienced bird; and whether subsequent seed choice was affected by observation of the experienced bird; and (3) whether observation of the feeding behaviour of the experienced bird facilitated husking and ingestion of seed by the young birds.
50, 3
into two parts (left and right), one containing naked oats, the other canary seeds.Half the birds had oats in the left compartment and the other half oats in the right compartment. The juveniles also had ad libitum accessto mash from another trough facing the transparent partition. The adult had no accessto mash. Five experimental situations each with 16 juveniles were tested. (1) No father: without the father, juvenile with free choice of oats and canary seeds. (2) Father/no seeds:with the father but the latter had no accessto any seeds. This situation was designed to examine the effect of the presence of the parent on the food choice of the offspring. (3) Father/hemp seeds: with the father who had accessto hemp seedsfrom a trough hung from the transparent partition backing onto the equivalent trough in the juvenile’s side of the cage. In thk situation, by consuming seeds the father could draw attention to an environmental cue, which might shape the juvenile to eat seeds,but withou serving as a model for the type of seed to eat, sina hemp was not available to the juvenile. (4) Father1 canary seeds:as for the previous situation except with canary seeds instead of hemp. (5) Father/ oats: with the father who had accessto oats. This and the Father/canary seeds situation provided information on the role of the parental model on METHODS the offspring’s food choice during local enhan@ment. The birds were observed for 1 h in each We studied 80 juvenile canaries, which were 28 situation. days old at the time of the experiments. The birds We noted the following. were reared by their parents in cages measur(1) We recorded for. the father the latency to ing 60 x 30 x 35 cm. The parents had access to pick up the first seed, the time taken to consume various types of seed (oats, canary seeds, hemp), the seedsand the total number of seeds manip* greens and mash during the brooding and rearing lated to seewhether the father reacted equally to period. When the young fledged at around 18 days the three types of seed. (2) The effects of the presence of the parent and after hatching, the seedswere removed, and both adults and juveniles had accessto just greens and local enhancement were investigated by recording mash. The juveniles thus did not learn how to the duration of immobility of the juveniles, to husk and eat seeds. They were maintained at see whether the father reduces fear (cf. Tolman 25 5 1°C on a 15:9 h 1ight:dark cycle. 1965), the number of pecks in the mash, the At 28 days of age one juvenile per brood was latency to pick up the first seed,and the number of selected at random and placed in its rearing cage seeds taken, husked and ingested. The juveniles’ either alone or with its father. The cage was consumption of mash should fall in the presence divided into two compartments by a vertical of the father eating seeds, while their seed Plexiglas partition to separate the father and consumption should rise correspondingly. offspring. The juvenile and the adult had accessto (3) To determine the influence of parental water from drinking troughs on the sides of the behaviour on the choice and proportions of seeds cage facing the Plexiglas partition. In the middle used by the juveniles we calculated the ratios of the partition and opposite the perch, the of the numbers of canary seeds to the total juvenile had access to a feeding trough divided number of seeds taken, husked and ingested (as
Cadieu et al.: Local enhancement
percentages). To determine the spontaneous preferenceof the juvenile for canary seedsor oats, we comparedthe percentage of canary seeds taken againstthe chance level (50%) in the situations Father/no seeds and Father/hemp seeds. This wasalso calculated for the percentages of canary seeds husked and ingested. We thus examined the influenceof which seed the parent ate, on the percentageof canary seeds taken, husked and eaten. (4) To find out whether the parental influence wasrestricted to the choice of a particular seed type,or whether it facilitated subsequent use of thisseedby the young birds (oats or canary seeds), wedetermined whether the proportion of seeds husked(over the number of seedstaken) and the proportion of seedsingested (over the number of seedshusked) was increased when the father manipulatedthis type of seed. We used Meddis’ non-parametric methods to test a priori directions of differences between treatments (Meddis 1984). Percentages were comparedto a chance value (50%) according to Schwartz(1963).
RESULTS
and choice
795
absence of the father the median duration of immobility was 2544 min versus 10.00, 8.74, 14.59 and 9.52 min for Father/no seeds, Father/hemp seeds, Father/canary seeds and Father/oats, respectively. The juveniles consumed less mash in the presence of the father, the decrease being greatest when seedswere available to the parent (Meddis’ specific test: ~~2.94, df=4, PcO.01; medians=236, 111.5, 58, 35.5 and 77 pecks in mash, respectively, for No father, Father/no seeds, Father/hemp seeds, Father/canary seedsand Father/oats). The latency to pick up the first seed by the juvenile was longer in the No father situation (median = 53.16 min) than in Father/no seeds (median=13.20) and was shortest in the other three situations (medians=9.67, 5.27 and 4.67 for Father/hemp seeds, Father/canary seeds and Father/oats, respectively; Meddis’ specific test: z=4.08, df=4, P
Father’sReaction to the Seed Types Our results support the hypothesis that the father reacted equally to the three types of seed. There were no significant differences between the three situations of availability (Fatherlhemp seeds,Father/canary seeds and Father/oats) for thethree parameters measured: latency to pick up thefirst seed (Meddis’ non-specific test: H=0.03, df=2, NS, with median latencies of 5, 5 and 8 s respectivelyfor Father/hemp seeds,Father/canary seeds and Father/oats); duration of feeding (medians=21.57, 23.32 and 19.05 min, Meddis’ non-specifictest: H=0.34, df=2, NS); number of seedsmanipulated (medians=258.5, 330.5 and 286.5, Meddis’ non specific test: H=3.72, df=2, NS).
Presenceof Father and Local Enhancement The juvenile’s period of immobility was shorter in the presence of the parent supporting the hypothesisthat its presence reduces fear (Meddis’ specific test: 2~3.25, df=4, PcO.01). In the
Copying of Seed Choice Comparisons were carried out for the four situations in which the father was present as very few seeds were consumed in the absence of the parent. There was no significant difference between the numbers of seedspicked up, husked and ingested between the right and left sidesof the feeding trough. Thus 1156 seedsout of 2400 were taken from the right hand side (x2= 3.23, df= 1, NS), 149 husked seeds out of 326 came from the right hand side (x2=2.40, df= 1, NS) and 97 seeds out of 219 ingested came from the right hand side (x2=2.85,
df=l,
NS).
Of the seeds the juveniles picked up in the Father/no seeds situation, the percentage of canary seeds (x& s~=65.89 f 6.84%, N= 14) significantly exceeded 50% (tz2.3, P
Animal Behaviour, 50. 3
196 651
husked and ingested by the juveniles should be higher in the Father/canary seedssituation than in the Father/no seeds and Father/hemp seeds situations. (2) If oats are available to the father, the relevant proportions of canary seeds should be lower in the Father/oats situation than in the Father/no seeds and Father/hemp seeds situations. Figure 2 shows the results. When canary seedwas available to the father there was no effect on the proportion of canary seeds picked up (Meddis’ specific test: z= 1.29, df=2, NS) but a greater proportion was husked (z=2.91, df=2, P
-I
T
Cc)
Seed Use Facilitation T
I
8 7 6 5 4 3 2
1 0
NO Father/ Father/ Father/ Father/ father no seeds izey! canary oats seeds Figure 1. The median number ( f one quartile) of seeds (a) taken, (b) huskedor (c) eaten by juvenile canaries when no father waspresentin the next compartmentor when the father waspresentbut without accessto seeds, with accessto hemp, with accessto canaryseedsor with accessto oats. NS,and x& s~=55.63 f 10.32, N= 12; t=0.54, NS, respectively), nor for the amount of canary seeds ingested (x& s~=44.07 * 11.18%, N=ll; t=0.37, NS, and x~!~s~=45.56& 11.38%, N=ll; t=0.5, NS, respectively). If the father servesas a model for the juveniles as to the type of seed to use, the following should be observed. (1) If canary seed is available to the father, the proportions of canary seedspicked up,
after Seed Choice
The father’s presence may also affect how the seeds are used after they have been chosen. The following hypotheses were examined. (1) If canary seedwas available to the father, the proportion of canary seedshusked with respect to the number of canary seeds picked up should be higher in the Father/canary seedsthan in the other situations. This hypothesis was supported by the results (Meddis’ specific test: zz3.09, df=3, P~0.01; Fig. 3a), a higher proportion of canary seeds being husked in the Father/canary seeds situation. (2) Similarly, the proportion of canary seedsingested with respect to the number of canary seedshusked should be higher in the Father/canary seedsthan in the other situations. The results, however, did not support this hypothesis (z= - 0.7, df=3, NS; Fig. 3b), there being no increasein the proportion of canary seeds ingested in the Father/canary seedssituation. We also examined the following hypotheses.(1) If oats were available to the father, the proportion of oats husked with respect to the number of oat seeds picked up should be higher in the Father/ oats than in the other situations. (2) The proportion of oats ingested with respect to the number of oat seedshusked should be higher in the Father/ oats than in the other situations. Both hypotheses were rejected (Meddis’ test: z=1.38 and 1.41.
Cadieu et al.: Local enhancement 90 t
80 70 60 50 40 30 20
60 I
(a)
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and choice
I ‘r
797
(a)
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t 40 30 1
1 T
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-
O-
*
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-
0 I Father/ no seeds
100 c (c)
90 80 70 60 50 40 30 20
~ -
10 O- nl Father/ no seeds
1
90t 80 70 60 50 40 30 20
l!l
Father/ is:
Father/ canary seeds
Father/ oats
Figure 3. The median number (f one quartile) of canary seeds (a) husked over the number of canary seeds taken, (b) eaten over the number of canary seeds husked, by juvenile canaries when the father was present but without accessto seeds, with accessto hemp, with access to canary seeds or with access to oats. DISCUSSION
Figure 2. The median percentage ( f one quartile) of canary seeds (a) taken, (b) husked or (c) eaten by juvenile canaries when the father was present but without access to seeds, with access to hemp, with access to canary seeds or with access to oats.
Our results show the importance of interactions between juveniles and adults on the first contact with seeds after the juveniles fledge. The presence of a conspecific, local enhancement and consumption of a type of seed by a tutor all influenced the juvenile’s feeding behaviour. The mere presence of the parent led to a social facilitation effect (Zajonc 1965), as the latency to
df=3, NS for hypotheses 1 and 2, respectively; Fig. 4); the proportions of oats husked and ingested werenot higher in the Father/oats situation. Use of oats by the father thus had no facilitatory influenceon husking and ingestion of this type of seedbv the iuveniles.
pick up the first seed was reduced and the numbers of seeds picked up, husked and ingested by the juveniles were increased in the presence of the father (Fig. 1). The paternal presence also attenuated the fear of the young birds (Tolman 1965) with a general increase in activity. The effects of local enhancement (Thorpe 1956) were observed when the parent consumed seeds,
Father/ kz
Father/ canary seeds
Father/ oats
Animal
798
Behaviour,
50, 3
place of manipulation in line with that observedin the cat, Felis catus, by Adler (1955). Our results 50 are comparable to the findings of Biederman & Vanyan (1988) and Zentall (1988) for learning by 40 1 observation of a discrimination task in pigeons which can distinguish accurately the stimulus 30 pecked by a conspecific. Our findings are also in agreement with those of Hogan (1973) and 20 Suboski (1989b) on newly hatched chicks, which can discriminate between two stimuli of which one T is indicated by a pecking arrow; although the chick cannot reach the stimulus attached to the it tends to peck the stimulus indicated byit. 1 arrow z 100 The proportions of seeds husked and ingested ii4 90 were influenced by the parent’s behaviour (Fig. 2). although apparently not entirely because of the 80 initial choice behaviour. With respect to the con. 70 trol situations (Father/hemp seedsand Father/no 60 seeds), observation of the father manipulating 50 oats had no effect on husking or ingestioa 40 although it altered the number of oat seedspicked 30 up by the young birds. On the other hand, when 20 the adult manipulated canary seeds,more of thir 10 type of seed was husked and ingested by the 0 juveniles. More detailed analysis of the fate of the Father/ Father/ Father/ Father/ no seeds oats seedspicked up and then husked by the juveniles canary ::3i seeds (Figs 3 and 4) showed the influence of the parental Figure 4. The median number ( f one quartile) of oat model on the stages of seed use by the juvenile. seeds (a) husked over the number of oat seeds taken, (b) Husking of canary seed by the juveniles was eaten over the number of oat seeds husked, by juvenile enhanced by observation of the parent manipulat. canaries when the father was present but without access ing this type, but not other types of seed. Obser. to seeds, with access to hemp, with access to canary vation of manipulation of oats did not, however. seeds or with access to oats. favour husking of this type of seed. We failed to observe any specific effect of consumption of a irrespective of whether they were of the same type particular type of seed by the parent on its inges. as that available to the juveniles. There was a tion by the juveniles. Although the juveniles reduction in the latency to pick up the first seed, ingested more canary seed when it was available an increase in activity of the juvenile towards to the parent, this was due to juveniles preferen. seeds (Fig. 1) and a reduction in consumption of tially husking this type of seed. The parental mash. influence is thus not limited to local enhancemenl The influence of the parent on the juvenile and discrimination of the seed type, but can also altered the choice of seedstaken by the latter (Fig. induce the appearance of similar behaviour in the 2), particularly when oats were available to the juveniles: in this casethe husking of canary seeds. parent; the proportion of oat seeds picked up by Nevertheless, young birds husk and ingest the the juveniles was then increased relative to the seedsavailable even in the absence of a parental situations Father/hemp seeds and Father/no model. The behavioural features induced by the seeds. We were unable to show a facilitation of parental feeding behaviour are thus indicators picking up of canary seeds by the parent as the of social facilitation in the sense of co-action young birds tended to prefer this type of seed (Clayton 1978). Local enhancement appears here anyway. to be a particular form of social facilitation in Our results in the canary thus point to a distinc- which conspecifics carry out the same activity tion between the object to manipulate and the in the same place (Galef 1988; Suboski 1989a). 60
1 (a)
.2
T
I
Cadieu
et al.:
Local
enhancement
However, we found that the social facilitation induced by observation of a parent facilitated husking of seeds that the offspring tended to take preferentially, in this case canary seeds (Fig. 2). Observation of the activity of the parents thus favours husking of small seeds, which are known to be preferred by young finches (Kear 1962). Our results indicate that birds in a group tend to display similar feeding behaviour, as has been observed in field studies (Templeton & Giraldeau 1990). The tendency of the young to consume the sameseeds as the adults may favour social transmission (Galef 1988) of food preferences. Other work has pointed to a role of observation and ingestion of seeds in the processes leading to seed recognition after the young are separated from the adults. Local enhancement followed by consumption of food indicated by a conspecific is generally regarded as an important process in the transmission of food preferences in birds, although ingestion may not always be required (Suboski 1989a).
and
Greig-Smith, P. W. 1987. Persistence in foraging: when do bullfinches abandon unurofitable seeds?Behaviour, 103, 203-216.
Greig-Smith, P. W. & Cracker, D. R. 1986. Mechanisms of food size selection by bullfinches Pyrrhula pyrrhula L. feeding on sunflower seeds. Anim. Behav., 34, 843-859.
Hinde, R. A. & Fisher, J. 1951. Further observations on the opening of milk bottles by birds. Br. Birds, 44, 392-396.
Hogan, J. A. 1973. How young chicks learn to recognize fond. In: Constraints on Learning (Ed. by R. A. Hinde & J. Stevenson-Hinde). on. 119-139. New York: Academic Press. Kear, J. 1962. Food selection in finches with special reference to interspecific differences. Proc. zool. Sot. Lond.,
138, 163-204.
Klopfer, P. H. 1957. An experiment on empathic learning in ducks. Am. Nat., 91, 6143. Laland, K. N. & Plotkin, H. C. 1991. Excretory deposits surrounding food sites facilitate social learning of food preference in Norway rats. Anim. Behav., 41, 997-1006. Mason, J. R. & Reidinger, R. F., Jr. 1982. Observational learning of food aversions in red-winged black-bird Agelaius
ACKNOWLEGMENTS We are very grateful to A. Turner for her invaluable advice, constructive comments and linguistic help. We also thank R. Gorse for his technical
assistance.
Adler, H. E. 1955. Some factors of observational learning in cats. Psychologia, Kyoto, 86, 159-177. Biederman, G. B. & Vanyan, M. 1988. Observational learning in pigeons: the function of quality of observed performance in simultaneous discrimination. Motiv.,
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Cadieu,J. C. 1985. Mise en evidence du role du modtle parental dans les processus d’autonomisation des jeunes passeraux: etude chez Serinus canarius. Actes 19th int. ethol.
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Clayton, D. A. 1978. Socially facilitated Q. Rev. Biol.,
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Meddis, R. 1984. Statistic Using Ranks. Oxford: Blackwell. Newton, I. 1967. The adaptive radiation and feeding ecology of some British finches. Ibis, 109, 33-98. Norton-Griffiths, M. 1966. Some ecological aspects of the feeding behaviour of the oystercatcher Haematopus ostralegus on the edible mussel Mytilus edulis. Ibis, 109,412A23.
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Fisher, J. & Hinde, R. A. 1949. The opening of milk bottles by birds. Br. Birds, 42, 347-357. Galef, B.G., Jr. 1988. Imitation in animals: history, definition and interpretation of data from the psychological laboratory. In: Social Learning: Psychological and Biological Perspectives (Ed. by T. R. Zentall & B. G. Galef, Jr), pp. 3-29. Hillsdale, New Jersey: Lawrence Erlbaum. Gliick, E. E. 1985. Seed preference and energy intake of goldfinches Carduelis carduelis in the breeding season. Ibis, 127, 421429.
Palameta, B. & Lefebvre, L. 1985. The social transmission of a food-finding technique in pigeons: what is learned. Anim. Behav., 33, 892-896. Pallaud, B. 1984. Hypotheses on mechanisms underlying observational learning in animals: imitation. Behav. Proc., 9, 381-394. Peterson, M. 1961. The nature and spread of Daphne eating in the greenfinch, and the spread of some other habits. Anim. Behav., 9, 114. Schwartz, D. 1963. Methodes Statistiques a I’lJsage des Medecins et des Biologistes. Paris: Flammarion. Senar, J. C. & Metcalfe, N. B. 1988. Differential use of local enhancement for finding food by resident and transient siskins. Anim. Behav., 36, 1549-1550. Sherry, D. F. & Galef, B. G. 1984. Cultural transmission without imitation: milk bottle opening by birds. Anim. Behav.,
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the operant conditioning of albino rats. Anim. Behav., 22, 66467 1. Zajonc, R. B. 1965. Social facilitation. Science, 149, 2699274. Zentall, R. 1988. Experimentally manipulated imitative behaviour in rats and pigeons. In: Social Learning. Psychological and Biological Perspectives (Ed. by T. R. Zentall & B. G. Galef, Jr), pp. 191-206. Hillsdale, New Jersey: Lawrence Erlbaum.
Behav., 1995, 50, 793-800
Local enhancementand seedchoicein the juvenilecanary, Serinus canarius J. C. CADIEU*, *Laboratoire tLaboratoire
d’Ethologie de Biologie
et de Psychologie Quantitative,
N. CADIEU*
& J. LAUGAt
Animale, URA 1837 CNRS, Universit& Paul Sabatier, Toulouse UMR 9964 CNRS, UniversitC Paul Sabatier, Toulouse
(Received 9 November 1993; initial acceptance 16 February 1994, final acceptance 13 January 1995; MS. number: 4522)
Abstract. The influence of the presence and feeding behaviour of the father on the behaviour of young
canarieswas examined. The naive offspring had accesssimultaneously to canary seedor oat seedsin the sameplace as did the parent, who either did or did not have accessto seeds(canary seeds,oats or hemp). In the absence of an adult, the juveniles took, husked and ate few seeds. The presence of the father increasedthe picking up, husking and ingestion of seedsby the juveniles, who also tended to feed in the sameplace as the parent (local enhancement). The choice of seed was also influenced by the parent’s tehaviour as the young birds picked up more oat seedswhen these seedswere available to the father. Thiswas not observed for canary seeds,which tended to be selected spontaneously by the young birds. Theamounts of canary seedsand oats husked and ingested by the juveniles did not only depend on seed choice.Manipulation of canary seed by the father facilitated its husking by the juvenile, whereas manipulation of oats by the father had no facilitatory effect on the use of this seed by the young birds. Overall,the effects of social facilitation tended to favour ingestion of seedsspontaneously selected by theoffspring. 0 1995The Association for the Study of Animal Fkhaviour Preculturaland social transmission is known to occur in numerous non-human vertebrates, includingmammals, fish and birds (Pallaud 1984; Galef1988; Suboski 1989a; Suboski & Templeton 1989).Although transmission may derive from imitation of experienced conspecifics (NortonGriffiths 1966; Will et al. 1974; Palameta & Lefebvre 1985) simpler processes may also be involved such as social facilitation and local enhancement(Turner 1964; Clayton 1978; Senar & Metcalfe 1988) as well as the use of excretory markers(Laland & Plotkin 1991) or vestiges of certainactivities (Sherry & Galef 1984). In birds, local enhancement is thought to accountfor the transmission of knowledge from an experienced to a naive bird, especially with respectto recognition of edible objects (Thorpe 1956;Suboski 1989a). This process may also be involved during the more complex learning involved in the acquisition of a new technique (Palameta & Lefebvre 1985). Thorpe (1956) definedlocal enhancement as ‘a particular case of Correspondence: N. Cadieu, Laboratoire d’Ethologie et de Psychologie Animale, URA 1837 CNRA, UniversitC PaulSabatier, 118 route de Narbonne. 31062 Toulouse Ctiex, France. 0003-3472/95/090793 +08 $12.00/O
social facilitation during which the attention of the subject is oriented towards a specific object or environmental zone’. This definition, however, does not take account of the tendency of two conspecifics to aggregate, which may also favour social or precultural transmission (Cadieu 1985; Zentall 1988). Furthermore, although birds tend to peck food in the same place as a conspecific, they are able to learn tasks, that cannot be accounted for by simple indication of an environmental cue or by observation of a purely spatial procedure. Thus naive pigeons, Columba livia, can learn by observation of an experienced conspecific to discriminate between a reinforced and a nonreinforced stimulus (Biederman & Vanyan 1988; Zentall 1988); out of two stimuli, hatchling chicks, Gallus gallus domesticus, preferentially peck the stimulus indicated by a pecking arrow (Hogan 1973; Suboski 1989b); ducks, Cairina moschata and Anas platyrhynchos, and red-winged blackbirds, Agelaius phoeniceus, avoid a food item associated with a noxious stimulus purely from observation of a conspecific (miipfer 1957; Mason & Reidinger 1982); and pigeons can learn by observation to pierce a membrane (Palameta & Lefebvre 1985).
C 1995 The Association for the Study of Animal Behaviour 793
794
Animal
Behaviour,
In passerines, feeding traditions have been observed in field studies, especially in tits (Fisher & Hinde 1949; Hinde & Fisher 1951) and finches (Peterson 1961; Newton 1967). Numerous studies have been devoted to the feeding choices of finches, which feed mainly on seeds. They husk the seeds and eat the kernels. The choice of seed has been related to both beak shape and profitability of the food source (Kear 1962; Newton 1967; Ghick 1985; Greig-Smith & Cracker 1986; Greig-Smith 1987; Diaz 1989). In a previous study, we observed social transmission of seed preferences in the canary (Cadieu 1985). This transmission occurred more readily if the young birds were allowed to feed close to their parents, from which they could pick up environmental cues. In the present study we investigated (1) how much the presence of an experienced bird and local enhancement affected the young birds’ preference; (2) whether the young birds could discriminate food sources indicated by the experienced bird; and whether subsequent seed choice was affected by observation of the experienced bird; and (3) whether observation of the feeding behaviour of the experienced bird facilitated husking and ingestion of seed by the young birds.
50, 3
into two parts (left and right), one containing naked oats, the other canary seeds.Half the birds had oats in the left compartment and the other half oats in the right compartment. The juveniles also had ad libitum accessto mash from another trough facing the transparent partition. The adult had no accessto mash. Five experimental situations each with 16 juveniles were tested. (1) No father: without the father, juvenile with free choice of oats and canary seeds. (2) Father/no seeds:with the father but the latter had no accessto any seeds. This situation was designed to examine the effect of the presence of the parent on the food choice of the offspring. (3) Father/hemp seeds: with the father who had accessto hemp seedsfrom a trough hung from the transparent partition backing onto the equivalent trough in the juvenile’s side of the cage. In thk situation, by consuming seeds the father could draw attention to an environmental cue, which might shape the juvenile to eat seeds,but withou serving as a model for the type of seed to eat, sina hemp was not available to the juvenile. (4) Father1 canary seeds:as for the previous situation except with canary seeds instead of hemp. (5) Father/ oats: with the father who had accessto oats. This and the Father/canary seeds situation provided information on the role of the parental model on METHODS the offspring’s food choice during local enhan@ment. The birds were observed for 1 h in each We studied 80 juvenile canaries, which were 28 situation. days old at the time of the experiments. The birds We noted the following. were reared by their parents in cages measur(1) We recorded for. the father the latency to ing 60 x 30 x 35 cm. The parents had access to pick up the first seed, the time taken to consume various types of seed (oats, canary seeds, hemp), the seedsand the total number of seeds manip* greens and mash during the brooding and rearing lated to seewhether the father reacted equally to period. When the young fledged at around 18 days the three types of seed. (2) The effects of the presence of the parent and after hatching, the seedswere removed, and both adults and juveniles had accessto just greens and local enhancement were investigated by recording mash. The juveniles thus did not learn how to the duration of immobility of the juveniles, to husk and eat seeds. They were maintained at see whether the father reduces fear (cf. Tolman 25 5 1°C on a 15:9 h 1ight:dark cycle. 1965), the number of pecks in the mash, the At 28 days of age one juvenile per brood was latency to pick up the first seed,and the number of selected at random and placed in its rearing cage seeds taken, husked and ingested. The juveniles’ either alone or with its father. The cage was consumption of mash should fall in the presence divided into two compartments by a vertical of the father eating seeds, while their seed Plexiglas partition to separate the father and consumption should rise correspondingly. offspring. The juvenile and the adult had accessto (3) To determine the influence of parental water from drinking troughs on the sides of the behaviour on the choice and proportions of seeds cage facing the Plexiglas partition. In the middle used by the juveniles we calculated the ratios of the partition and opposite the perch, the of the numbers of canary seeds to the total juvenile had access to a feeding trough divided number of seeds taken, husked and ingested (as
Cadieu et al.: Local enhancement
percentages). To determine the spontaneous preferenceof the juvenile for canary seedsor oats, we comparedthe percentage of canary seeds taken againstthe chance level (50%) in the situations Father/no seeds and Father/hemp seeds. This wasalso calculated for the percentages of canary seeds husked and ingested. We thus examined the influenceof which seed the parent ate, on the percentageof canary seeds taken, husked and eaten. (4) To find out whether the parental influence wasrestricted to the choice of a particular seed type,or whether it facilitated subsequent use of thisseedby the young birds (oats or canary seeds), wedetermined whether the proportion of seeds husked(over the number of seedstaken) and the proportion of seedsingested (over the number of seedshusked) was increased when the father manipulatedthis type of seed. We used Meddis’ non-parametric methods to test a priori directions of differences between treatments (Meddis 1984). Percentages were comparedto a chance value (50%) according to Schwartz(1963).
RESULTS
and choice
795
absence of the father the median duration of immobility was 2544 min versus 10.00, 8.74, 14.59 and 9.52 min for Father/no seeds, Father/hemp seeds, Father/canary seeds and Father/oats, respectively. The juveniles consumed less mash in the presence of the father, the decrease being greatest when seedswere available to the parent (Meddis’ specific test: ~~2.94, df=4, PcO.01; medians=236, 111.5, 58, 35.5 and 77 pecks in mash, respectively, for No father, Father/no seeds, Father/hemp seeds, Father/canary seedsand Father/oats). The latency to pick up the first seed by the juvenile was longer in the No father situation (median = 53.16 min) than in Father/no seeds (median=13.20) and was shortest in the other three situations (medians=9.67, 5.27 and 4.67 for Father/hemp seeds, Father/canary seeds and Father/oats, respectively; Meddis’ specific test: z=4.08, df=4, P
Father’sReaction to the Seed Types Our results support the hypothesis that the father reacted equally to the three types of seed. There were no significant differences between the three situations of availability (Fatherlhemp seeds,Father/canary seeds and Father/oats) for thethree parameters measured: latency to pick up thefirst seed (Meddis’ non-specific test: H=0.03, df=2, NS, with median latencies of 5, 5 and 8 s respectivelyfor Father/hemp seeds,Father/canary seeds and Father/oats); duration of feeding (medians=21.57, 23.32 and 19.05 min, Meddis’ non-specifictest: H=0.34, df=2, NS); number of seedsmanipulated (medians=258.5, 330.5 and 286.5, Meddis’ non specific test: H=3.72, df=2, NS).
Presenceof Father and Local Enhancement The juvenile’s period of immobility was shorter in the presence of the parent supporting the hypothesisthat its presence reduces fear (Meddis’ specific test: 2~3.25, df=4, PcO.01). In the
Copying of Seed Choice Comparisons were carried out for the four situations in which the father was present as very few seeds were consumed in the absence of the parent. There was no significant difference between the numbers of seedspicked up, husked and ingested between the right and left sidesof the feeding trough. Thus 1156 seedsout of 2400 were taken from the right hand side (x2= 3.23, df= 1, NS), 149 husked seeds out of 326 came from the right hand side (x2=2.40, df= 1, NS) and 97 seeds out of 219 ingested came from the right hand side (x2=2.85,
df=l,
NS).
Of the seeds the juveniles picked up in the Father/no seeds situation, the percentage of canary seeds (x& s~=65.89 f 6.84%, N= 14) significantly exceeded 50% (tz2.3, P
Animal Behaviour, 50. 3
196 651
husked and ingested by the juveniles should be higher in the Father/canary seedssituation than in the Father/no seeds and Father/hemp seeds situations. (2) If oats are available to the father, the relevant proportions of canary seeds should be lower in the Father/oats situation than in the Father/no seeds and Father/hemp seeds situations. Figure 2 shows the results. When canary seedwas available to the father there was no effect on the proportion of canary seeds picked up (Meddis’ specific test: z= 1.29, df=2, NS) but a greater proportion was husked (z=2.91, df=2, P
-I
T
Cc)
Seed Use Facilitation T
I
8 7 6 5 4 3 2
1 0
NO Father/ Father/ Father/ Father/ father no seeds izey! canary oats seeds Figure 1. The median number ( f one quartile) of seeds (a) taken, (b) huskedor (c) eaten by juvenile canaries when no father waspresentin the next compartmentor when the father waspresentbut without accessto seeds, with accessto hemp, with accessto canaryseedsor with accessto oats. NS,and x& s~=55.63 f 10.32, N= 12; t=0.54, NS, respectively), nor for the amount of canary seeds ingested (x& s~=44.07 * 11.18%, N=ll; t=0.37, NS, and x~!~s~=45.56& 11.38%, N=ll; t=0.5, NS, respectively). If the father servesas a model for the juveniles as to the type of seed to use, the following should be observed. (1) If canary seed is available to the father, the proportions of canary seedspicked up,
after Seed Choice
The father’s presence may also affect how the seeds are used after they have been chosen. The following hypotheses were examined. (1) If canary seedwas available to the father, the proportion of canary seedshusked with respect to the number of canary seeds picked up should be higher in the Father/canary seedsthan in the other situations. This hypothesis was supported by the results (Meddis’ specific test: zz3.09, df=3, P~0.01; Fig. 3a), a higher proportion of canary seeds being husked in the Father/canary seeds situation. (2) Similarly, the proportion of canary seedsingested with respect to the number of canary seedshusked should be higher in the Father/canary seedsthan in the other situations. The results, however, did not support this hypothesis (z= - 0.7, df=3, NS; Fig. 3b), there being no increasein the proportion of canary seeds ingested in the Father/canary seedssituation. We also examined the following hypotheses.(1) If oats were available to the father, the proportion of oats husked with respect to the number of oat seeds picked up should be higher in the Father/ oats than in the other situations. (2) The proportion of oats ingested with respect to the number of oat seedshusked should be higher in the Father/ oats than in the other situations. Both hypotheses were rejected (Meddis’ test: z=1.38 and 1.41.
Cadieu et al.: Local enhancement 90 t
80 70 60 50 40 30 20
60 I
(a)
-
and choice
I ‘r
797
(a)
50
t 40 30 1
1 T
10 -
-
O-
*
10
-
0 I Father/ no seeds
100 c (c)
90 80 70 60 50 40 30 20
~ -
10 O- nl Father/ no seeds
1
90t 80 70 60 50 40 30 20
l!l
Father/ is:
Father/ canary seeds
Father/ oats
Figure 3. The median number (f one quartile) of canary seeds (a) husked over the number of canary seeds taken, (b) eaten over the number of canary seeds husked, by juvenile canaries when the father was present but without accessto seeds, with accessto hemp, with access to canary seeds or with access to oats. DISCUSSION
Figure 2. The median percentage ( f one quartile) of canary seeds (a) taken, (b) husked or (c) eaten by juvenile canaries when the father was present but without access to seeds, with access to hemp, with access to canary seeds or with access to oats.
Our results show the importance of interactions between juveniles and adults on the first contact with seeds after the juveniles fledge. The presence of a conspecific, local enhancement and consumption of a type of seed by a tutor all influenced the juvenile’s feeding behaviour. The mere presence of the parent led to a social facilitation effect (Zajonc 1965), as the latency to
df=3, NS for hypotheses 1 and 2, respectively; Fig. 4); the proportions of oats husked and ingested werenot higher in the Father/oats situation. Use of oats by the father thus had no facilitatory influenceon husking and ingestion of this type of seedbv the iuveniles.
pick up the first seed was reduced and the numbers of seeds picked up, husked and ingested by the juveniles were increased in the presence of the father (Fig. 1). The paternal presence also attenuated the fear of the young birds (Tolman 1965) with a general increase in activity. The effects of local enhancement (Thorpe 1956) were observed when the parent consumed seeds,
Father/ kz
Father/ canary seeds
Father/ oats
Animal
798
Behaviour,
50, 3
place of manipulation in line with that observedin the cat, Felis catus, by Adler (1955). Our results 50 are comparable to the findings of Biederman & Vanyan (1988) and Zentall (1988) for learning by 40 1 observation of a discrimination task in pigeons which can distinguish accurately the stimulus 30 pecked by a conspecific. Our findings are also in agreement with those of Hogan (1973) and 20 Suboski (1989b) on newly hatched chicks, which can discriminate between two stimuli of which one T is indicated by a pecking arrow; although the chick cannot reach the stimulus attached to the it tends to peck the stimulus indicated byit. 1 arrow z 100 The proportions of seeds husked and ingested ii4 90 were influenced by the parent’s behaviour (Fig. 2). although apparently not entirely because of the 80 initial choice behaviour. With respect to the con. 70 trol situations (Father/hemp seedsand Father/no 60 seeds), observation of the father manipulating 50 oats had no effect on husking or ingestioa 40 although it altered the number of oat seedspicked 30 up by the young birds. On the other hand, when 20 the adult manipulated canary seeds,more of thir 10 type of seed was husked and ingested by the 0 juveniles. More detailed analysis of the fate of the Father/ Father/ Father/ Father/ no seeds oats seedspicked up and then husked by the juveniles canary ::3i seeds (Figs 3 and 4) showed the influence of the parental Figure 4. The median number ( f one quartile) of oat model on the stages of seed use by the juvenile. seeds (a) husked over the number of oat seeds taken, (b) Husking of canary seed by the juveniles was eaten over the number of oat seeds husked, by juvenile enhanced by observation of the parent manipulat. canaries when the father was present but without access ing this type, but not other types of seed. Obser. to seeds, with access to hemp, with access to canary vation of manipulation of oats did not, however. seeds or with access to oats. favour husking of this type of seed. We failed to observe any specific effect of consumption of a irrespective of whether they were of the same type particular type of seed by the parent on its inges. as that available to the juveniles. There was a tion by the juveniles. Although the juveniles reduction in the latency to pick up the first seed, ingested more canary seed when it was available an increase in activity of the juvenile towards to the parent, this was due to juveniles preferen. seeds (Fig. 1) and a reduction in consumption of tially husking this type of seed. The parental mash. influence is thus not limited to local enhancemenl The influence of the parent on the juvenile and discrimination of the seed type, but can also altered the choice of seedstaken by the latter (Fig. induce the appearance of similar behaviour in the 2), particularly when oats were available to the juveniles: in this casethe husking of canary seeds. parent; the proportion of oat seeds picked up by Nevertheless, young birds husk and ingest the the juveniles was then increased relative to the seedsavailable even in the absence of a parental situations Father/hemp seeds and Father/no model. The behavioural features induced by the seeds. We were unable to show a facilitation of parental feeding behaviour are thus indicators picking up of canary seeds by the parent as the of social facilitation in the sense of co-action young birds tended to prefer this type of seed (Clayton 1978). Local enhancement appears here anyway. to be a particular form of social facilitation in Our results in the canary thus point to a distinc- which conspecifics carry out the same activity tion between the object to manipulate and the in the same place (Galef 1988; Suboski 1989a). 60
1 (a)
.2
T
I
Cadieu
et al.:
Local
enhancement
However, we found that the social facilitation induced by observation of a parent facilitated husking of seeds that the offspring tended to take preferentially, in this case canary seeds (Fig. 2). Observation of the activity of the parents thus favours husking of small seeds, which are known to be preferred by young finches (Kear 1962). Our results indicate that birds in a group tend to display similar feeding behaviour, as has been observed in field studies (Templeton & Giraldeau 1990). The tendency of the young to consume the sameseeds as the adults may favour social transmission (Galef 1988) of food preferences. Other work has pointed to a role of observation and ingestion of seeds in the processes leading to seed recognition after the young are separated from the adults. Local enhancement followed by consumption of food indicated by a conspecific is generally regarded as an important process in the transmission of food preferences in birds, although ingestion may not always be required (Suboski 1989a).
and
Greig-Smith, P. W. 1987. Persistence in foraging: when do bullfinches abandon unurofitable seeds?Behaviour, 103, 203-216.
Greig-Smith, P. W. & Cracker, D. R. 1986. Mechanisms of food size selection by bullfinches Pyrrhula pyrrhula L. feeding on sunflower seeds. Anim. Behav., 34, 843-859.
Hinde, R. A. & Fisher, J. 1951. Further observations on the opening of milk bottles by birds. Br. Birds, 44, 392-396.
Hogan, J. A. 1973. How young chicks learn to recognize fond. In: Constraints on Learning (Ed. by R. A. Hinde & J. Stevenson-Hinde). on. 119-139. New York: Academic Press. Kear, J. 1962. Food selection in finches with special reference to interspecific differences. Proc. zool. Sot. Lond.,
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Klopfer, P. H. 1957. An experiment on empathic learning in ducks. Am. Nat., 91, 6143. Laland, K. N. & Plotkin, H. C. 1991. Excretory deposits surrounding food sites facilitate social learning of food preference in Norway rats. Anim. Behav., 41, 997-1006. Mason, J. R. & Reidinger, R. F., Jr. 1982. Observational learning of food aversions in red-winged black-bird Agelaius
ACKNOWLEGMENTS We are very grateful to A. Turner for her invaluable advice, constructive comments and linguistic help. We also thank R. Gorse for his technical
assistance.
Adler, H. E. 1955. Some factors of observational learning in cats. Psychologia, Kyoto, 86, 159-177. Biederman, G. B. & Vanyan, M. 1988. Observational learning in pigeons: the function of quality of observed performance in simultaneous discrimination. Motiv.,
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