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Behav Ecol. 2011 Jul-Aug; 22(4): 745–754.
Published online Apr 29, 2011. doi:  10.1093/beheco/arr055
PMCID: PMC3117902
Progressive parenting behavior in wild golden lion tamarins
Lisa G. Rapaportcorresponding author
Department of Biological Sciences, 132 Long Hall, Clemson University, Clemson, SC 29612, USA
corresponding authorCorresponding author.
Address correspondence to L.G. Rapaport. E-mail: lrapapo/at/clemson.edu.
Received November 17, 2010; Revised March 22, 2011; Accepted March 27, 2011.
Young primates in the family Callitrichidae (the marmosets and tamarins) receive extensive and relatively prolonged care from adults. Of particular note, callitrichid young are routinely provisioned until well after weaning by parents and helpers, which is in stark contrast to typical juvenile primates, who must acquire most of their food independently once they are weaned. Adults of some callitrichid species produce a specialized vocalization that encourages immature group members to take proffered food from the caller. Here, I report that wild adult golden lion tamarins (Leontopithecus rosalia) not only used this food-offering call to encourage young, mobile offspring to approach and take captured prey from them, but as the young began to spend significant time foraging for themselves and to acquire prey by independent means, the frequency of these vocalizations in the context of food transfer declined. Adults then began to use food-offering calls in a novel context: to direct juveniles to foraging sites that contained hidden prey that the adults had found but not captured. During the period of these most frequent adult-directed prey captures, the independent prey-capture success rates of juveniles improved. Thus, adults modified their provisioning behavior in a progressive developmentally sensitive manner that may have facilitated learning how to find food. I hypothesize that as a result of these demonstrations by adults, juveniles either may be encouraged to continue foraging despite low return rates or to learn the properties of productive prey-foraging substrates in a complex environment.
Keywords: golden lion tamarin, infant development, parenting behavior, prey foraging, provisioning, teaching
Young primates in the family Callitrichidae (the marmosets and tamarins) receive extensive and relatively prolonged care from adults. Callitrichids are cooperative breeders: that is, species in which individuals other than the parents play a significant role in caring for the young (Solomon and French 1997; Burkart et al. 2009). As such, all or most of a group's adults participate in caretaking, which includes substantial provisioning of infants and weaned juveniles, tolerance of young at feeding sites, as well as carrying infants and acting as sentinels for predators (Garber et al. 1984; Terborgh and Goldizen 1985; Caine 1993; Schiel and Huber 2006). Among noncooperatively breeding primates, in contrast, juveniles typically must acquire most of their food independently once they are weaned and receive little food or foraging assistance from others (Rapaport and Brown 2008). Variable forms of care, extending past the age of weaning or fledging, have been reported in a wide range of cooperatively breeding species and may be characteristic of this type of breeding system (Doolan and MacDonald 1999; Langen 2000; Clutton-Brock et al. 2002; Ridley and Raihani 2007).
Details of caretaking behavior in callitrichids are known from decades of studies on captive and wild groups (reviewed in Tardif et al. 1993; Brown et al. 2005; Rapaport and Brown 2008). In terms of feeding assistance, provisioning rates in tamarins peak during weaning and shortly thereafter (when immatures are 3–5 months old), but food transfer to young may continue throughout the first year of life or even longer (Ferrari 1987; Tardif et al. 2002; Rapaport and Ruiz-Miranda 2006). Due to their communal caretaking system, nonmothers provision as frequently as do mothers, and in some cases, more frequently (Brown et al. 2004). Food transfers for the most part are initiated by the young, but adults of some species, including the golden lion tamarin, also produce a specialized vocalization that encourages immature group members to approach and take proffered food from the caller (Feistner and Price 1991; Ruiz-Miranda et al. 1999; Roush and Snowdon 2001; Joyce and Snowdon 2007). Callitrichids are the only primates known to use acoustically and contextually distinct food-offering calls to provision their young. What is not well understood, however, is the degree to which adult caretaking activities track the skills of developing young. For example, a prior report of wild golden lion tamarins in the same population as that under study in the present account described 3 instances in which adults employed the food-offering call, not to facilitate transfer but to direct their young to find hidden prey that the adults had found but not captured (Rapaport and Ruiz-Miranda 2002). These observations raise the possibility that the function of the vocalizations may vary according to the developmental stage of recipient young in much the same way that pied babblers (Turdoides bicolor) vary the context of their purr call, first using it to facilitate food transfer to nestlings and later to recruit fledglings to profitable foraging sites (Radford and Ridley 2006; Raihani and Ridley 2007).
The foraging methods used by lion tamarins to obtain prey may require time and practice to master. As is true of all callitrichids, lion tamarins search for and catch visible prey such as lizards and insects from vegetation surfaces (Rapaport LG, personal observation). However, lion tamarins specialize in the capture of embedded prey; they frequently forage by reaching into crevices and holes with their elongated hands and fingers in the search for hidden insects, spiders, and tree frogs (Rosenberger 1992). Tree knotholes, bromeliads, dried palm leaf-sheaths, broken branch tips, vine tangles, and accumulations of leaf litter and detritus are all common substrates for manipulative foraging (Dietz et al. 1997; Rylands 1993; Rapaport LG, personal observation). Within a group's territory, the number of potential locations in which prey may be found is so large and constantly changing that there may be little benefit for a lion tamarin to remember the identity of any specific site that has yielded unseen prey. Moreover, the young mature rapidly and disperse from their natal territory as early as 12 months of age (Baker 1991), thereby limiting the value of any prior locational knowledge. Developing the skills to forage effectively for prey within such a complex system thus may favor social learning (Galef and Giraldeau 2001) and, potentially, a predisposition by adults to provide foraging assistance to inexperienced young.
The goal of this study was to examine the relationship between the ontogeny of juvenile prey-foraging behavior and the food-related caretaking behavior of adults. That is, do adults vary their caretaking behavior in a progressive, developmentally sensitive manner such that the foraging assistance provided tracks the skill or information deficits of recipient young? To examine this question I first describe the ontogeny of prey foraging by delineating age-related changes in juvenile foraging effort and foraging success. Second, I investigate the developmental time course of provisioning and food-offering vocalizations to juveniles. In order to clarify the functions of food-offering vocalizations during ontogeny, I examine a behavior I hereby term adult-directed prey capture, that is, instances in which adults use food-offering calls to draw attention to hidden prey that the callers have found but not extracted. Does this behavior, previously observed only 3 times, occur throughout the population? Does the context in which adults employ the food-offering call (i.e., to offer food-in-hand vs. to alert young to prey that the young must find and capture) vary in such a way so as to provide the young with age-specific experience? If so, the contexts in which food-offering calls are given are predicted to vary according to juvenile age-related foraging ability: the frequency of food-offering calls uttered in the context of prey transfer will peak before the young begin to spend significant time foraging for prey, whereas calls given in the context of adult-directed prey capture will peak when juvenile prey-foraging effort is high but their prey-foraging success is low.
Finally, I test the predictions set out by Caro and Hauser (1992) regarding teaching. In other words, does the evidence support the supposition that the tamarins are teaching their young where to search for prey? Social learning is widespread among nonhuman animals but, unlike teaching, tends to be limited to those mechanisms in which the onus is on the inexperienced individual to gather information without assistance from the knowledgeable model (Heyes 1994). Although relatively rare, teaching has been reported in a wide range of species, from ants (Temnothorax albipennis: Franks and Richardson 2006) to orcas (Orcinus orca: Boran and Heimlich 1999; see Hoppitt et al. 2008; Thornton and Raihani 2008, for reviews). Although most studies are largely anecdotal in nature, teaching appears to be overrepresented among solitary hunters of large or dangerous prey, such as felids, and among cooperative breeders (Rapaport 2006; Burkart et al. 2009). The presence of teaching in the first group can be explained because natural selection will favor social learning when independent learning entails great difficulty or risk, for example, the risk of injury to an inexperienced hunter by its prey (Caro and Hauser 1992; Thornton and Raihani 2008). Burkart and van Schaik (2010) posit that cooperative breeders are preadapted to teach because they exhibit a high motivation to assist others, a psychological predisposition that is driven by the cooperative infant care system. Cooperatively breeding primates, for instance, regularly take turns with other group members during caretaking activities and also tend to be exceptionally tolerant and attentive to others in a variety of contexts. Such social tolerance and cooperativeness should favor social learning. Even more, this spontaneous prosociality means that not only do adults often take an active role in assisting naive individuals but that cooperative breeders may be unusually sensitive to the information or skill deficits of the young, thereby setting the stage for the possibility of teaching (Burkart et al. 2009; Burkart and van Schaik 2010). Thus, marmosets and tamarins are excellent candidates in which to study social learning and teaching behavior because they are at once cooperative breeders and solitary hunters of relatively large prey.
Study site and subjects
I conducted observations from January 2000 through October 2003 on 8 groups of wild golden lion tamarins living in the União Biological Reserve, Brazil: a 3126 ha mosaic of primary, late- and early-stage secondary Brazilian Atlantic coastal rainforest, Eucalyptus plantations, small feral banana groves, and narrow grassy strips. The reserve's golden lion tamarin population originated from 6 wild family groups that had been translocated into the reserve from various isolated forest remnants in 1994–1997 (Kierulff and Rylands 2003). Six of the study groups had one or 2 adults who had been translocated in this way but all other individuals had been born in the União Reserve.
Six groups were studied longitudinally: spanning the period when focal immatures were about 12–56 weeks of age (Supplementary Material). Two of these groups were studied again, but for shorter periods, as were 2 additional groups (average study duration for these 4 groups: 15.75 weeks). Adult provisioning of young in captive lion tamarins peaks at approximately 12 weeks of age (Tardif et al. 2002), but the young still receive about 90% of their solid food from adults at 16 weeks of age (Hoage 1982). Thus, observations were planned so as to include the period of maximum provisioning.
Immature study subjects are considered to be juveniles, and individuals 57–112 weeks of age are considered to be subadults (Rapaport 2006). In this paper, “adults” refers to both subadults and adults except where subadult is specified. Immatures in the longitudinally studied groups had been weaned, or nearly so, when formal observations on them began. Three singleton juveniles were studied in one group (Bauen [BA]); each of the other groups had one pair of twin immatures (Supplementary Material). Groups were usually captured twice per year, at which time group members were marked with hair dye for individual identification and at least one individual per group was fitted with a radio transmitter collar. Food supplementation by humans (i.e., bananas) was provided only at trapping platforms during trapping attempts.
Data collection
On a given observation day, data collection was focused on either subadults and adults or juveniles. Data collection sessions lasted 20 min and focal individuals were determined according to a preset, rotating order throughout the day. Observations typically were carried out 0630–1430, with number of sessions ranging from 1 to 20 per day. I used either focal instantaneous sampling with a 120-s interval or continuous sampling in conjunction with all occurrences sampling (Martin and Bateson 1993). The continuous sampling method was discontinued 3 months into the first year of the study (having been used on only the Luiza Brunet and Funil groups). Data were collected in teams of 2, and observers other than the author were trained for a minimum of 2 months prior to independent data collection. Interobserver agreement was assessed and recalibrated through comparison of simultaneously collected data, discussion of behavioral definitions during regular meetings, and while collecting data with the author in the field at frequent intervals.
All occurrences of food transfers (part or all of a food item changes possession), food-offering calls (a distinctive staccato vocalization, also termed food-transfer call, that may be given by a food possessor in the presence of immatures; Brown and Mack 1978; Ruiz-Miranda et al. 1999), and independent prey captures involving a focal animal were recorded. I calculated the percentage of time juveniles spent foraging for prey (i.e., actively engaged in visual or manipulative search for animal prey) from the instantaneous sampling method. Adult-directed prey captures by immatures (see RESULTS for full description of the behavior) were recorded on an ad libitum basis.
Data analyses
A total of 1330.32 focal contact hours was collected on 13 juveniles, an average of 102.33 h per juvenile. These data were used to calculate rates. Additionally, 860.20 focal contact hours were collected on 34 adults: 8 mothers, 11 potential fathers, and 15 helpers (i.e., individuals >56 week of age living in the group in which they were born). Instances of adult-directed prey capture were gleaned from the total data set, which included 20 immatures (Supplementary Material).
Analyses use individual means. To investigate the effects of age on rates of provisioning, food-offering calls, and independent prey capture, I pooled data for each focal individual in 4 age categories: 09–20, 21–32, 33–44, and 45–56 weeks. The data regarding prey transfer have been presented in a previous publication in a slightly different manner (i.e., averaged over 3 age-blocks instead of 4: Rapaport 2006) and are reanalyzed here in order to elucidate developmental changes in provisioned versus independent prey acquisition. I calculated rates (i.e., food transfers received, food-offering vocalizations given to juveniles during interactions in which adults had prey in hand, and independent prey capture) by estimating time spent visible from the simultaneously collected focal instantaneous and continuous samples. Rates therefore represent the frequency of a given behavior exhibited by a juvenile or received by a juvenile divided by the estimated number of hours spent visible, for a given period. The rates at which food-offering calls were recorded were probably underestimated because it is unlikely that observers heard all these low-amplitude vocalizations, which were produced by adults who were often several meters away from a given focal immature at the beginning of a food-transfer interaction. Nonetheless, it is doubtful that underestimation was age biased. I used linear mixed models incorporating repeated measures to investigate the effects of age category on behavior. Additionally, group and individual within group were considered random effects in the model. To account for correlation between measurements taken on the same individual over time, a first-order autoregressive correlation structure was used. Heterogeneity of variance across ages was evaluated against equal variances across ages using Akaike Information Criteria (AIC); the heterogeneous variance structure was adopted as it yielded the smallest AIC in all analyses. Analyses were conducted in SAS. All tests are 2-tailed and significance level set at P < 0.05.
Reliable rates could not be assessed for adult-directed prey capture; because tamarins often foraged for prey out of sight of each other, it is unlikely that all adult-directed prey-foraging interactions were seen by observers who were watching juveniles. If an observer was focusing on a juvenile, an adult tamarin could call to a juvenile yet the observer might never know if the adult had just found, but not retrieved, a hidden prey item unless the adult had been fortuitously nearby and unobscured by vegetation. I excluded from the dataset any instance in which a juvenile approached an adult, engaged in manipulative foraging near the adult, and did or did not extract prey but in which the adult's prior behavior was not directly observed. In this way, I have conservatively eliminated all questionable interactions from consideration.
Independent foraging
Prey foraging was not a skill that was quickly mastered by the juvenile golden lion tamarins in my study. The youngest age at which a tamarin was observed to capture prey from its own independent foraging activity was at 13 weeks (mean for immatures for whom observations began by 12 weeks of age: 17 weeks, range: 13–23, n = 7). When they were between 9- and 20-week old, juveniles spent an average of 10.93 ± 0.025% of visible observation time searching for prey but only captured an average of one prey item every 5 h. I performed a linear mixed-model analysis of variance incorporating repeated measures on percentage of visible time juveniles spent foraging with age category as the main effect and with group and individual within group as random effects. I found a significant effect of age category (F3,33 = 17.57, P < 0.0001). Time spent foraging was significantly less during first age category (9–20 weeks) compared with the other 3 age categories according to post hoc tests (t-test for differences of least-square means, degrees of freedom [df] = 33, age category 1 vs. 2, 3, and 4, P < 0.05; age categories 2 vs. 3 and 4; and 3 vs. 4, P ≥ 0.05; Table 1). In other words, juveniles spent little time foraging when they were 09–20 weeks old, but throughout the rest of development, prey-foraging time remained essentially constant, at about 20% of visible observation time. Foraging time was greatest in the last 2 age categories compared with the second age category, but not significantly so (Figure 1a).
Table 1
Table 1
Effects of juvenile age on juvenile foraging behavior and on adult caretaking behavior
Figure 1
Figure 1
Development of prey acquisition. (a) Percentage of time spent foraging by juveniles as a function of age category. Juveniles spent significantly less time foraging when in the first age category than in any of the other age categories. (b) Rates per hour (more ...)
Rates of independent prey capture per hour did not follow the same pattern as prey-foraging effort. Independent prey capture did vary as a function of age category (F3,21 = 20.14, P < 0.0001) but post hoc tests indicated a significant difference between the ages of 21–32 weeks and 33–44 weeks (t-test for differences of least-square means, df = 21, age category 1 vs. 3 and 4; and 2 vs. 3 and 4, P < 0.05; age categories 1 vs. 2 and category 3 vs. 4, P ≥ 0.05; Table 1). Rates of independent prey capture tended to increase gradually until as the young tamarins approached 1 year of age, they were capturing on average more than one prey item per hour (45–56 weeks age category, 1.20 ± 0.21 items/h; Figure 1b). Prey-capture rate per hour of visible observation time would not necessarily take into account effort expended in prey foraging, especially since time spent foraging varied during development. I therefore also analyzed prey-capture rates after controlling for search time (i.e., number of prey captures divided by number of intervals spent foraging for prey). This measure of foraging efficiency varied as a function of age category (F3,21 = 16.62, P < 0.0001), and post hoc tests showed the same pattern as did prey foraging rate per hour of visible observation; that is, there was a significant increase between the second and third age categories (t-test for differences of least-square means, df = 21, age category 1 vs. 3 and 4 and category 2 vs. 3 and 4, P ≤ 0.05; age categories 1 vs. 2 and category 3 vs. 4, P ≥ 0.05; Table 1). In other words, when juveniles were 21–32-week old, they spent a significant amount of their time foraging for prey, but with a low rate of success. It was not until the subsequent age category that juveniles achieved a significant improvement.
Because independent prey-capture rates increased later in development than did prey-foraging effort, there was a substantial lag between increased effort and improvement in prey-capture success. This and the slow improvement in prey-capture success indicate that it takes time and practice for an immature golden lion tamarin to learn to forage for prey effectively.
Food transfer
The prey that juveniles receive from adult group-members supplements prey captured independently. Therefore, not surprisingly, the rates at which weaned young received prey items from adults decreased as a function of juvenile age (F3,32 = 25.92, P < 0.0001; see also Rapaport 2006). Post hoc tests revealed that rates remained high during the first 2 age categories (age-category 1 vs. 2: t-test, df = 32, P ≥ 0.05; Table 1) and then declined steadily (all other comparisons, P < 0.05; Figure 1c). Food-transfer rates dropped most steeply between age-categories 2 and 3; juveniles received 0.68 ± 0.07 items per hour when 21–32 week of age but just 0.15 ± 0.04 items per hour when 33–44 week of age. This is the same period in which juveniles showed a striking improvement in independent prey capture.
These results point to a marked shift in juvenile food-acquisition strategies, especially between 21–32 and 33–44 weeks of age. Foraging comprised a significant percentage of the juvenile time budget after the first age category. Despite an increase in prey-foraging effort, juveniles continued to receive most of their prey food items from parents and adult helpers throughout the first 2 age categories (09–32 weeks inclusive) and acquired little prey through their own independent foraging efforts. This situation was reversed in the third and fourth age categories (33–56 weeks inclusive); that is, food transfer of prey by adults to immatures became infrequent, whereas the rate with which juveniles captured their own prey increased so that juveniles in the last 2 age categories obtained most of their prey from independent foraging (Figure 1).
Food-offering calls
I found that the golden lion tamarins in my study varied their calling behavior as their group's young matured. I performed a linear mixed-model analysis of variance incorporating repeated measures on the rate at which adults emitted food-offering calls during all prey-transfer interactions (i.e., regardless of whether the outcome was successful transfer or not) and found a significant effect of juvenile age category (F3,32 = 4.92, P < 0.0064; Figure 2). Adults used food-offering calls to attract their group's offspring to take prey-in-hand most frequently when the young were 21–32 weeks of age (mean rate: 0.112 ± 0.024 calls/h). Post hoc tests revealed a significant decrease between the ages of 21–32 and 33–44 weeks (t-tests, df = 32, age category 2 vs. 3 and 2 vs. 4, P < 0.05; all other comparisons P ≥ 0.05; Table 1).
Figure 2
Figure 2
Food-offering calls from adults to juveniles as a function of juvenile age category. Circles: mean rates (±standard error of the mean) at which juveniles received calls from adults in the context of prey transfer interactions, whether transfer (more ...)
Adults not only used food-offering calls to encourage young to take food that the caller had captured. Starting at about 20 weeks of age, adults began to use the call in a new context: to alert juveniles to productive prey-foraging sites. During the study's first year, we had observed 3 instances in which an adult initiated extractive foraging, stopped without having captured prey, and then emitted a food-offering call. The juvenile who approached in response to the call began to forage immediately in the same place where the adult had just been foraging and found the prey within seconds. The adult either left as soon as the juvenile found the item or stayed but, either way, allowed the juvenile to eat the prey without further interaction (Rapaport and Ruiz-Miranda 2002). To that initial report, 12 other similar events are now added (Table 2). During these events, the targeted substrates varied but the food item was always concealed within vegetation. Adults directed juveniles to find items within the following substrates: knothole in a branch (7 instances), curled dead leaf (2), broken end of a branch (3), crevice in twisted vines (2), and thick tangle of dead vines, small leaves, and twigs (1).
Table 2
Table 2
Adult-directed foraging: group name, identity of individuals involved in the interaction, description of food item extracted by the juvenile, and substrate in which the manipulative foraging occurred
In all but 2 cases, the juveniles found prey, which was most often arthropods but also included tree frogs (Table 2). In one of the exceptions, a subadult male helper of the Mais Um (MA) group gave a food-offering call after having briefly foraged in a knothole and found and eaten a small (≤1.0 cm in length) prey item. The male's 40-week-old brother approached in response to the call and foraged in the knothole but did not extract anything. Both individuals then left the area. The other exception was the only event to involve nonprey. In this instance, the breeding female of the BA group was holding and eating the relatively large fruit of a Eugenia robustovenosa tree when she emitted a food-offering call, but the group's 21-week-old juvenile did not approach to take the fruit from her hand. She then reached down and placed the fruit in a crevice of twisted vines. This was the only time that an individual did not let a fruit just drop when finished with it. The female emitted another food-offering call, at which point her juvenile daughter approached and foraged by inserting her fingers into the vine crevices around the fruit but neither the juvenile nor her mother extracted it. The remaining adult-directed foraging events were striking with regard to the speed with which juveniles extracted prey. It was far more typical for juveniles to engage in extensive manipulative foraging, in substrate after substrate, and without success. For instance, when juveniles approached and foraged on a substrate where another individual was foraging or had been foraging within the past 15 s, but in which food-offering calls were not heard, the juveniles did not often capture prey; the proportion of these juvenile-initiated social foraging bouts that resulted in successful prey capture was only 3.33% (n = 13 juveniles; range: 0.00–8.90%).
Individuals in 7 of the 8 different study groups participated in the 15 unambiguous adult-directed foraging events (Table 2). Mothers, putative fathers (i.e., non-natal adult males of a group; genetic paternity was not determined), and male helpers were seen to call their group's juveniles to vegetation substrates where prey could be found. Adult-directed foraging events were distributed among 6 different mothers (8 events), 4 putative fathers (4 events), and 2 male helpers (3 events). Ten different juveniles, 4 females and 6 males, were involved in these adult-directed events.
Most instances occurred when the juveniles were in the 2 middle age categories. Five events were observed when immatures were in age-category 2 and 8 events when they were in age-category 3. The youngest juvenile to be so directed to a substrate containing prey was 20 weeks of age and the oldest was 45 weeks of age (Table 2). Although the total number of observation days varied among juvenile age categories (an observation day being defined as that in which >2 focals were completed; repeated measures analysis of variance F = 4.324; df = 3; P = 0.012; range: 97–170 days), the only significant post hoc comparison was between the first age category and the second (9–20 vs. 21–32 weeks: t-test, t = −3.568, df = 10, P < 0.05), suggesting that the drop in number of adult-directed prey captures seen between the juvenile age-category 3 and 4 was not simply due to disparity in observation time.
The emerging picture is of a progressive change in the function of food-offering calls as juveniles mature. Around the age of weaning and for several weeks thereafter, food-offering vocalizations were given routinely to encourage the young to take captured prey from the caller (see also Ruiz-Miranda et al. 1999; Rapaport 2006). At 20 weeks of age, an adult was first seen to use the call to direct a juvenile to a substrate where a prey item was located and then allow the juvenile to find and eat it. By the time juveniles were 33–44 weeks of age, adults rarely called with prey in hand. At this stage, use of the call to direct young to capture their own prey was at peak frequency. Age-category 2 (21–32 weeks of age) thus can be viewed as a transitional phase in which food-offering calls were habitually emitted in both contexts (Figure 2).
I found that prey-capture skills develop slowly in golden lion tamarins. Prey-foraging success remained very low until my young study subjects were more than 7.5 month old, and their prey-foraging effort was still on the rise at that age. Young common marmosets (Callithrix jacchus), in contrast, have mastered most prey-capture techniques by 3 months of age and attain adult proficiency in all prey-foraging behaviors by the time they are 5 months old (Schiel et al. 2010). Unlike lion tamarins, common marmosets rely on visual methods to detect prey: in addition to stalking and pouncing on exposed prey, they often look under leaves to find hidden insects but tend not to use manipulative foraging to extract embedded prey (Schiel et al. 2010). Thus, I hypothesize that it is the lion tamarin's manipulative-foraging specialization that requires an exceptionally long time to master.
The rates at which adults provisioned juveniles were found to mirror rates of independent prey capture by juveniles. That is, prey-transfer to juveniles declined in concert with an improvement in juvenile prey-capture success. What is more, the rates by which adults encouraged prey transfer with food-offering vocalizations even rose slightly during the second age category, at which time juveniles had increased their prey-foraging effort but had not yet achieved an improvement in prey-foraging success. These results demonstrate the willingness of adults to provision until juveniles are able to effectively feed by independent means.
The adult golden lion tamarins varied the context in which they uttered food-offering calls in a developmentally sensitive manner, as hypothesized. Adults used food-offering calls most frequently to encourage transfer of adult-captured prey at a time when juvenile prey-capture success was low but when juveniles were not yet spending maximal effort foraging for prey. Once juveniles began to increase their prey-foraging effort but before their prey-capture rates had increased, adults began to use the calls in a context that promoted successful prey foraging. Calling by adults to encourage prey capture by juveniles was pervasive in the population but it occurred infrequently. By the time the juveniles were in the last age category, at around 1 year of age, the percentage of time they spent prey foraging had leveled off, prey-foraging success had peaked, and adult food-offering calls in both contexts had all but disappeared. Thus, adults seemed to alter their food-related caretaking behavior according to juvenile foraging ability. However, my data do not distinguish between the possibilities that adults are sensitive to juvenile foraging ability or simply to juvenile age. Thus, adults may use juvenile age as the proximate cue to adjust their provisioning behavior, as is the case in meerkats (Suricata suricatta: Thornton and McAuliffe 2006). Wild adult meerkats first provision young pups with dead and disabled scorpions, then provision older pups with live scorpions, stingers intact. Thornton and McAuliffe (2006) have shown experimentally that it is pup age, rather than individual pup foraging proficiency, that determines whether a pup will receive a live or a dead scorpion. Furthermore, experiments suggest that adult callitrichids may use juvenile age as the determinant of provisioning rates. For instance, Saito et al. (2008) found that captive common marmoset parents were more generous to younger offspring, even though the food in their experiment was presented in a bowl and thus readily obtainable to all, regardless of age.
In addition to this study, adult-directed foraging assistance has been described in 2 laboratory studies in which young callitrichids were encouraged to solve a novel foraging task by a knowledgeable parent (Humle and Snowdon 2008; Dell'Mour et al. 2009). By contrast, reports of adults altering their behavior to assist foraging young are virtually nonexistent for our closest relatives, the nonhuman apes. Neither wild orangutans (Pongo pygmaeus wurmbii: Jaeggi et al. 2010) nor gorillas (Gorilla gorilla: Nowell and Fletcher 2006) as yet have been observed to provide active foraging assistance to their young. Only 2 instances have been seen in wild chimpanzees (Pan troglodytes), the most well studied of the apes. In each of these cases, a female West African chimpanzee demonstrated to her offspring how to crack open palm nuts with stones (Boesch 1991). What is more, Boesch (1991) reported many instances in which female chimpanzees either left stones and nuts in the vicinity of their offspring or passively allowed their young to take stones and nuts from them.
Is this teaching?
Are the golden lion tamarins in this study population teaching their young? Caro and Hauser (1992) provided an operational definition, which stipulates that to be considered teaching, a behavior must satisfy 4 criteria: 1) a knowledgeable individual A alters its behavior only in the presence of an inexperienced individual B, 2) A incurs a cost or at least no immediate benefit, 3) the demonstrator's action encourages or punishes B or provides B with appropriate experience, and 4) as a result, B either learns more quickly or efficiently or acquires knowledge that it might not otherwise learn. This definition circumvents the prickly stipulation that the demonstrator, or tutor, understand the pupils' level of skill or knowledge. Accordingly, teaching can occur when a tutor actively modifies its behavior such that learning by an inexperienced pupil is encouraged, whether we understand the tutor's intentions or not. In the following paragraphs, I assess the 4 criteria as they relate to the golden lion tamarins' behavior.
The first criterion by Caro and Hauser is assessed by excluding the possibility that tamarin food-offering calls are given regardless of the presence of immatures. Previous studies have demonstrated that food-offering calls are made only in the presence of young and can be categorized unequivocally as parental and alloparental behaviors (Feistner and Price 1991; Joyce and Snowdon 2007). In my study population, almost exclusively it was immatures, not adults, who responded to the calls (93/94 calls). In the single instance in which an adult responded to a call, the food-possessor did not relinquish the prey it had captured (Rapaport and Brown 2008). Juveniles, in contrast, did not emit food-offering calls. All the main study groups contained immature group members while under observation, but ad libitum observations were conducted for brief periods on 2 additional groups that did not have immatures. One, comprised 4 adults, was observed for 8 all-day follows; the other consisted of 3 adults and was observed for 11 days (≥6 h group-contact time per day). Food-offering calls were never heard in these adult-only groups nor were any events observed that could be construed as adult-directed prey capture. What is more, adults in the main study groups varied their calling behavior in developmentally appropriate ways. Importantly, adults used the vocalization to call attention to productive prey-foraging sites only when juveniles were at the developmental stage in which they were often foraging for prey, but their prey-capture success rates were either low or increasing; that is, when the young were inexperienced. The behavior was extinguished when the young were effectively foraging for prey on their own. Thus, the first criterion of Caro and Hauser (1992) is met.
The second criterion by Caro and Hauser (1992) stipulates that tutors sustain cost or gain no immediate benefit from their actions. Food-offering vocalizations may cause a caller to incur a cost because prey that could have been eaten by the caller ends up in the hands of another individual. Helpers hypothetically may gain immediate benefit for their generosity in the form of increased tolerance from breeding group members, as has been suggested for other infant-caretaking behaviors (Clutton-Brock et al. 2000; Sánchez et al. 2002; Ginther and Snowdon 2009) although this supposition has not been tested.
Adults attract juveniles to them when they call with prey-in-hand and as a result food transfer is facilitated. Calling to offer captured prey in general, therefore, is an efficient means to supplement juvenile nutrition and must be excluded as teaching according to the second criterion of Caro and Hauser (1992). However, experimental evidence suggests that food transfer, in addition to serving as an efficient means to supplement nutrition, also may act to inform young callitrichids about diet. Young tamarins (Leontopithecus rosalia: Rapaport 1999; Saguinus oedipus: Joyce and Snowdon 2004) and common marmosets (Vitale and Queyras 1997; Voelkl et al. 2006) are more likely to receive novel foods from adults than foods with which they are familiar (but see Brown et al. 2005). Young common marmosets are responsible for any information gained because they beg more for novel foods (Brown et al. 2005; Voelkl et al. 2006). Immature tamarins, on the other hand, beg indiscriminately, whereas adults more readily relinquish acceptable food items that are novel to the immatures (Rapaport 1999; Joyce and Snowdon 2004). By varying their provisioning behavior depending on the novelty of the item, tamarin adults may increase the likelihood that naive immatures will learn to identify appropriate foods. It is not yet known whether immatures do, in fact, learn to incorporate novel foods in their diet from provisioning interactions.
Are adult-directed prey captures an efficient means by which to augment juvenile feeding and do adults therefore benefit from these interactions? During prey transfers accompanied by food-offering calls and during adult-directed prey captures, the adult typically engages in manipulative foraging, locates a prey item, gives a food-offering call, and waits for a juvenile to approach. The salient differences between the 2 types of interactions are the identity of the individual who captures the prey item and the greater time lag between initial prey detection and extraction in adult-directed prey captures. When an adult finds a prey item but does not capture it and instead calls and waits for a juvenile to search for it, the adult runs the risk that the prey will escape or that the juvenile will not find it, as may have occurred in the incidence between brothers of the MA group. If capture outcomes of immatures are less likely than those of adults, even after prey has been located for the juveniles, then immediate nutritional benefits to juveniles would be optimized if the adults were to catch the prey immediately and offer it to them. On the other hand, if juveniles do not experience higher rates of nondetection or prey escape once they have been alerted to the presence of the item, adults might obtain small energetic savings by allowing the juveniles to sustain the cost of prey extraction. Determination of the comparative rates at which common prey species escape detection and capture by wild-born golden lion tamarin adults and juveniles would help to delineate the costs or benefits to adult-directed prey captures. If juveniles were found to experience higher failure rates, then the second criterion by Caro and Hauser (1992) would be satisfied. In the long-term, though, both parents and related helpers will benefit if these behaviors function to reduce the period of provisioning and/or increase offspring survival (Thornton and Raihani 2008).
The golden lion tamarins' adult-directed prey capture behavior satisfies the third criterion of Caro and Hauser (1992); that is, the behavior encourages age-appropriate experience. Around the age of weaning, when young golden lion tamarins spend little time attempting to find prey, adults regularly provision them with captured prey, often calling to promote transfer. As the young begin to spend more time foraging for prey but their return-rates remain at a nadir, adults begin to habitually, if infrequently, direct them to substrates where they can forage with immediate reward. By offering the juveniles an opportunity to succeed, adult-directed foraging may act to condition the young to keep trying in the face of high failure rates. Between the second and third age category, juvenile foraging-success rates increase dramatically. It is during this same period that adults most often provide juveniles with opportunities to experience productive foraging. Thus, adults progressively modify their food-calling behavior in a manner appropriate to the skill development of their young.
The rise in the rate at which juveniles captured prey independently concomitant with adult-directed prey capture suggests that the experience the adults provide may accelerate the development of the young tamarins' foraging skills. If adults are providing food-related information, what is it specifically that juveniles may be learning? Juveniles may learn from these interactions what kinds of prey are appropriate to eat but this possibility was not addressed in my study. In wild meerkats, adults hasten the development of their pups' prey-capture abilities by providing them with progressively more challenging prey-handling opportunities. As a result of experience, the pups learn at a younger age to dispatch dangerous prey (Thornton and McAuliffe 2006). It is unlikely, though, that adult-directed foraging instructs juvenile tamarins in prey-handling techniques. In all the adult-directed foraging events in which prey was extracted, the prey was removed quickly and then immediately killed and eaten. In contrast to calls made during adult-directed prey capture, however, food-offering calls made in the context of food transfer may function to enhance prey-handling proficiency. Adults with prey in hand more frequently used food-offering vocalizations to encourage juveniles to approach and take the item when the prey was alive than when it was dead, especially when juveniles were reluctant to take the item (Rapaport 2006).
The adult wild golden lion tamarins could be offering information to their young about prey-foraging substrate properties. Adult cotton-top tamarins (S. oedipus) helped their offspring to solve a novel laboratory foraging task by partially solving the task in the presence of the pupil, exposing the hidden food, and allowing the youngster to remove it from the apparatus. Parents not only offered this active assistance but they showed sensitivity to individual juvenile foraging proficiency, as they refused more begs as soon as the juveniles had solved the foraging task. As in the meerkat study (Thornton and McAuliffe 2006), the naive young tamarins appeared to learn more quickly due to adult encouragement (Humle and Snowdon 2008). My study does not provide evidence that young tamarins do indeed learn as a consequence of responding to food-offering calls by adults. The use of playbacks of adult food-offering calls at foraging sites that have been experimentally supplied with hidden food could help to unequivocally determine whether naive wild golden lion tamarins learn to find prey more quickly or efficiently as a direct result of adult demonstration and whether the behavior serves to focus the young on appropriate substrates, thus satisfying the fourth criterion of Caro and Hauser (1992).
Unlike pied babblers, who frequently (about 0.6 times per hour) used calls to recruit their fledglings to profitable foraging patches (Radford and Ridley 2006), the tamarins only rarely called their young to forage for hidden food. I eliminated many questionable events from consideration because the adult's behavior before the interaction had not been observed. Even if most of those deleted interactions were, in fact, adult-directed prey captures, the behavior still would have been quite rare. Adult-directed prey captures might be predicted to occur at a higher frequency if these events are important for the development of competent prey-foraging behavior (Thornton and Raihani 2008). If, on the other hand, the function of these interactions is to encourage poor foragers, the events need not occur often but instead should be directed to particularly slow learners or to less diligent foragers. Of course, this would require adults to somehow track the proficiencies of individual pupils rather than merely to adjust their behavior with juvenile age. For the demonstrations to be effective, a juvenile would be expected to experience an increase in prey-foraging return rate or at the very least an increase in prey-foraging effort on similar substrates, following an adult-directed prey-capture event. Further observational and experimental studies, designed to assess juvenile behavior before and after adult-directed foraging, could resolve these issues.
Caro and Hauser (1992) divided teaching into 2 categories: “opportunity teaching” in which the demonstrator puts the pupil in “a situation conducive to acquiring a new skill or knowledge” and “coaching” in which the demonstrator “directly alters the behavior of a pupil by encouragement or punishment” (p. 166). Coaching requires that the demonstrator actively mold the pupil's behavior, whereas in opportunity teaching, the demonstrator simply creates an environment that facilitates learning by the pupil as a result of the pupil's own behavior. The tamarins in my study did not actively change their pupils' behavior in the same way that captive gorilla mothers can be said to coach their offspring when they physically alter their infant's movements to encourage increasingly independent locomotion (Gorilla gorilla: Whiten 1999). However, the adult tamarins' food-offering calls do encourage juveniles to approach a situation in which productive-substrate properties may be learned. Extractive foraging for prey requires a lion tamarin to choose a foraging substrate with limited information regarding the probability of success. Furthermore, once a prey source has been depleted it may not provide prey again because favored prey species typically occur as solitary items and because the substrate may have been destroyed in the course of foraging, as often occurs when tamarins forage on dead and dying vegetation. Thus, a foraging tamarin's challenge is to generalize from a previous productive food site to a new one.
In conclusion, I found that the function of food-offering calls changes as the young develop. When immatures are very young and spend little time foraging, the calls are most frequently used to facilitate the transfer of food from the hands of the caller. Experimental evidence suggests that immatures may learn to identify appropriate food items from these interactions (Rapaport 1999). Thus, through food transfer, the young tamarins may be encouraged to learn a fact: this is good food to eat. The calls also potentially have a training function as they encourage immatures to handle live prey (Rapaport 2006). Later in development, when adults call the young to productive foraging sites, they may be providing information that can help the young to solve a more general problem: what does a productive foraging site look like? This, according to Thornton and Raihani (2008) can be termed “progressive teaching” as it encourages the development of general foraging skills, allowing the young tamarins to learn to forage competently. If it can be shown that juvenile golden lion tamarins do learn to forage for prey more effectively or at a younger age as a result of adult-directed foraging, they will join the ranks of the few species known to teach their young (Hoppitt et al. 2008; Thornton and Raihani 2008).
FUNDING
National Institute of Mental Health at the National Institutes of Health(MH59175); Pittsburgh Zoo Conservation Fund.
Supplementary Material
Lay Summary
Supplementary Data
Acknowledgments
P. Gerard of Clemson University provided statistical advice and assistance. Brazilian employees and my Biosc 491 students at Clemson University are acknowledged for their contribution to data collection and analysis. I thank the Translocation Team of the Golden Lion Tamarin Association, run by Paula Procópio de Oliveira and Maria Cécilia Kierulff, for their help and cooperation. I would like to warmly acknowledge IBAMA, the Golden Lion Tamarin Association, CNPq, Carlos Ruiz-Miranda, the late Devra Kleiman, and Jane Lancaster for logistical assistance and Sarah Hrdy, and 3 anonymous reviewers for valuable comments that improved the manuscript. This research adhered to University of New Mexico Main Campus Animal Care and Use Committee guidelines (Protocol #9801) and to all relevant Brazilian laws, regulations, and guidelines. The paper is dedicated to Devra Kleiman, whose untiring efforts have kept the golden lion tamarin from near-certain extinction.
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