Social learning of food preferences by white-tailed ptarmigan chicks

ANIMAL BEHAVIOUR, 2005, 70, 305–310 doi:10.1016/j.anbehav.2004.10.022

Social learning of food preferences by white-tailed ptarmigan chicks TR AC I AL LEN & J ENN IF ER A . C LAR KE

Department of Biology, University of Northern Colorado (Received 10 February 2004; initial acceptance 30 March 2004; final acceptance 18 October 2004; published online 23 May 2005; MS. number: 8004R)

The social-learning function of a food call is to share information about resources with conspecifics. Field studies on the social learning of food and parent–offspring interactions regarding food in a natural environment are rare. Our aims in a 2-year study in the Rocky Mountain National Park, U.S.A., were to monitor white-tailed ptarmigan, Lagopus leucurus, hens’ food calls, a vocalizing and tidbitting display, to determine whether the hens selected foraging areas based on food availability and whether chicks learned about important food resources from hen food calls. Our findings indicate that the white-tailed ptarmigan hen’s food call is a form of cultural transmission in which information regarding available food is disseminated from hens to chicks. Hens chose foraging patches where certain plant species were abundant and called their chicks to these foods, which dominated their diet. Chick consumption mirrored the calling rates of hens and as a result chicks ate high-protein foods, which are critical for chick growth and development. The results suggest that white-tailed ptarmigan hens’ food calls may function to enhance survival of juvenile ptarmigan. Ó 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Empirical studies suggest that social learning affects the food choice of juvenile birds (Stokes 1971; Sherry 1977; Moffatt & Hogan 1992; Fritz et al. 2000; Midford et al. 2000). Naı¨ve individuals that learn from skilled conspecifics benefit by reducing their costs associated with learning (Laland et al. 1993, 1996; Avital & Jablonka 1994; Galef 1995; Giraldeau & Caraco 2000). Observers can learn novel behaviours faster and more thoroughly by observing a trained demonstrator than without exposure to a trained individual (Heyes et al. 1992; Nicol & Pope 1992). Individuals that learn behaviours from others can experience lower error rates than those that learn on their own (Boyd & Richerson 1985). Reducing the learning curve is critical for juveniles when mortality is linked to inefficient foraging abilities (e.g. in birds, Lack 1954; Perrins 1980; Sullivan 1989). The social-learning function of a food call is to share information about food resources with conspecifics. Social learning through food-related calls has been widely documented in gallinaceous birds, primarily for courtship (Marler et al. 1986a, b; Evans & Marler 1994; Nicol & Pope

Correspondence and present address: T. Allen, Department of Zoology, University of Otago, Dunedin, New Zealand (email: rkymtnptarmigan@ yahoo.com). J. A. Clarke is at the Department of Biology, University of Northern Colorado, Greeley, CO 80639, U.S.A. 0003–3472/04/$30.00/0

1994, 1999; Van Kampen 1994; Evans & Evans 1999) and parental care (Stokes 1971; Sherry 1977; Moffatt & Hogan 1992). Laboratory experiments emphasizing horizontal transmission of information dominate the research, whereas field studies on the social learning of food (Lefebvre & Bouchard 2003) and on parent–offspring interactions regarding food are rare. We investigated food calls transmitting food information vertically from hen to chick in a natural population of white-tailed ptarmigan, Lagopus leucurus, North America’s only alpine grouse. Social learning plays an important role in the development of this species. The alpine tundra environment is physically challenging: the breeding season is short, with extreme wind, intense ultraviolet light and severe cold (Martin 2001). Seasonal flowering in the alpine zone is under tight environmental regulation controlled by the exogenous cues of photoperiod and temperature (Korner 1999). Ptarmigan breed during the flowering season; chicks are born precocial, self-feed, and have a short time to discriminate between foods available before the onset of winter. In the Sierra Nevada Mountains of California, U.S.A., one of us (Clarke 2001) documented white-tailed ptarmigan hens calling their chicks to plants and chicks responding by rushing to the indicated plant and feeding. Clark & Mangel (1986) referred to the chick’s response as the ‘milkshake effect’ because individuals will accelerate their

305 Ó 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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feeding rate to increase their share of a limited resource. A white-tailed ptarmigan hen’s food call is a vocalizing and tidbitting display (pecking down at a food substrate), which stimulates chicks to join the hen in consuming the preferred food resource. Gallinaceous chicks have an unlearned predisposition to peck at foods (Suboski & Bartashunas 1984); however, the hen’s food call encourages chicks to focus their pecks at specific plants. The objectives of our study were to monitor the foraging behaviour of white-tailed ptarmigan broods to determine whether the hens selected foraging areas based on food availability and whether chicks learned about important food resources from the hen’s food calls.

foraging plot the distance and direction of the 1-m2 paired-control plot was randomly generated (up to 20 m). Plants in forage and paired-control plots were identified to generic level using Weber & Wittman (2001). A major component of summer diet for ptarmigan, forbs (May & Braun 1972), were classified to species level. We compared the relative percentage cover of plant species in forage plots with the relative percentage cover in paired-control plots to determine whether food patch selection was based on the presence or absence of certain foods. Percentages of food available within forage plots were also compared with percentages in the chicks’ diet to determine whether their diet reflected food abundance.

METHODS

Subjects

Nutritional Analyses

We observed white-tailed ptarmigan broods for 2 years (15 July–15 August, 2002–2003) in the alpine tundra accessible by car on Trail Ridge Road in Rocky Mountain National Park, U.S.A. (elevation 3400–3658 m). Broods were found on windy, sloped talus typically 1–3 days after the chicks hatched. We used a chick distress call played on a hand-held recorder (Braun et al. 1973) to detect broods, because adult ptarmigan are cryptic and their plumage blends in with the environment (Lewis 1904; Giesen et al. 1980; Schmidt 1988). Broods were observed R 2 m away and were monitored only when the hen appeared comfortable with our presence. We were able to distinguish between broods by specific locations, number of chicks, presence or absence of bands, and age of chicks. The study was conducted with permission of the Rocky Mountain National Park.

Samples (10 g) of each plant eaten were collected with tweezers or manicure scissors, weighed and then placed in a plant press. They were oven dried at 55  C for 12 h. To determine macronutritional content of consumed plants, we conducted proximate analyses measuring the amount of crude protein (Kjeldahl), soluble carbohydrate (ADG, lignin), insoluble carbohydrate (fibre) and lipid (diethyl ether extract), crude fibre, ash and nitrogen-free extract (Fonnesbeck 1977; Van Soest 1981; Perry 1984; Robbins 1993). These tests were done at Weld Laboratories, Greeley, Colorado, U.S.A. We focused primarily on protein, because it is the most important macronutrient for chick growth and development (Robbins 1993).

Statistical Analyses Data Collection We collected data three times a day (0630–0830, 1000– 1200 and 1300–1500 hours) at four locations. Observational sessions began only when the hen started to forage. The observer monitored the hen’s foraging behaviour and the closest chick/s to her and maintained visual contact with the hen at all time by using a hand-held tape recorder to record data. Foods consumed by hens and chicks were recorded once each minute; and hen food calls were recorded continuously. A foraging session ended when the hen moved away from the centre of the foraging area and each session lasted 10–20 min. At the completion of each observational session, a 1-m2 plot centred on the location of the foraging hen was marked with a flag and roped off. We measured the plant species composition within the plot shortly after a foraging session ended, when the hen and her chicks moved away from the foraging area. Ptarmigan spent most of their foraging time pecking at food and eating a few very small bites of each plant (each bite ! 0.25 cm), which allowed for post hoc assessment of plant species availability in foraging plots (T. Allen, personal observation). Relative ground cover within the plot was classified into categories including forbs, grasses, sedges, bare ground and rock. For each

We compared plant species availability in the forage and control-paired plots with the 1-m2 plot as the unit of measurement. Each time a plant was present in one of the two types of plots, we measured its percentage composition within the plot and compared it with the other plot to see whether the plots differed. Paired t tests were used to compare means of individual plant species in pairedcontrol and forage plots to determine whether hens were selective about foraging location. Paired t tests were also used to compare means of plants in the chicks’ diet with their availability within the forage plot to determine whether chicks consumed foods in proportion to their relative availability. We used a bivariate regression analysis to determine the amount of variation in the chicks’ diet that could be explained by the hen’s food calls and a one-factor ANOVA to compare the mean differences of food-calling rates between hens that called more or less to determine whether calling rates were dependent upon the calling frequency of the hen. Protein comparison was conducted by running a one-factor ANOVA and comparing percentages of food calls for high-protein versus low-protein foods. Carex jonesii had the median protein value and was included in both groups for statistical analyses.

ALLEN & CLARKE: SOCIAL LEARNING IN PTARMIGAN

RESULTS

Foraging Area Selectivity Over the 2-year study we observed 12 hens in 95 foraging sessions. The distribution of foraging bouts per hen was relatively normal (XGSEZ6:00G2:67 bouts=hen). Ptarmigan ate a variety of foods, with hens consuming 75% (12/16 foods) of the same foods as chicks (Fig. 1). Hens appeared to select foraging patches, as several plants were significantly more abundant in forage plots than in paired-control plots. In particular, two plants, Salix reticulata (dwarf alpine willow) and Bistorta vivipara (alpine bistort), comprised more than half of the ptarmigan diet and were significantly more available in forage plots (paired t test: S. reticulata: t94 Z 6.01, P ! 0.0001; B. vivipara: t94 Z 3.36, P Z 0.0005; Fig. 2a). A further comparison of the chicks’ diet with the relative abundance within forage plots indicated a significantly strong preference for S. reticulata and B. vivipara (S. reticulata: t94 Z 6.01, P ! 0.0001; B. vivipara: t94 Z 3.36, P Z 0.0005) as chicks consumed large percentages of each compared with their limited availability (Fig. 2b).

Hen Food calls

Nutrition Hens gave a significantly greater percentage of food calls to high-protein foods (one-way ANOVA: F1,6 Z 7.004, P Z 0.038; Table 2). High-protein foods were T. dasyphyllum, S. reticulata, and B. vivipara and low-protein foods were A. rossi, S. umbellata and G. algida.

DISCUSSION Herbivores eat a diverse diet to meet their nutritional requirements (Hartmann 1991) and this variety was reflected in the food calls of hens. Hens selectively chose foraging patches where certain species were abundant and called their chicks to these foods, which dominated their diet. In particular, more than half of the hen’s food calls were to S. reticulata and B. vivipara, which not only

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Observed hens uttered 47 food calls (XGSEZ3:83G2:85 food calls/hen). The timing of the hen’s food calls during a foraging session was sporadic. Chicks responded to 91.5% of the food calls, but response rates to calls might have been low than normal because lightning and thunder on the mountains caused hens’ calls to be inaudible in four of the 47 calls. Chicks responded immediately to food calls by switching to the specific plant indicated by the call (T. Allen, personal observation). In 31.9% of the calls (15/47), hens called chicks to foods other than those the chicks were eating at the time. In 59.6% (28/47) of the calls, chicks were already foraging on the same plant species indicated in the hen’s food call but

not the individual plant. Chicks switched to the individual plant signalled by the hen’s food call. Hens called their chicks to grit twice. The influence of the hen’s food call was evident, as 94% of the chicks’ diet comprised foods associated with the hen’s food calls (Table 1) and percentages of foods consumed by chicks mirrored percentages of the hen’s calls to foods (Fig. 3). Hens called most often (57.0% of calls) to foods that chicks consumed most, S. reticulata and B. vivipara. Of the variance in the chick diet 70.9% could be explained by the hen’s food calls (bivariate regression: r2 Z 0.709, P Z 0.002; Fig. 3). The foraging bouts/hen data were bimodally distributed because hens either called a lot (O5 calls/hen) or a little (!3 calls/hen). There was a significant difference in the number of calls between the two groups, low-calling (N Z 7) and high-calling hens (N Z 5; one-way ANOVA: F1,10 Z 20.75, P Z 0.001). High-calling hens made significantly more food calls to S. reticula (F1,10 Z 6.50, P Z 0.029) and B. vivipara (F1,10 Z 6.86, P Z 0.036).

Plant species

Figure 1. Plant species consumed by white-tailed ptarmigan hens and their chicks in Rocky Mountain National Park in 2002 and 2003. ACO Z Acomastylis rossii, BIB Z Bistorta bistortoides, BIV Z Bistorta vivipara, CAR Z Carex jonesii, CLA Z Claytonia lanceolata, GEN Z Gentianodes algida, JUN Z Juncus spp., MOSP Z moss spores, OXY Z Oxyria digyna, POA Z Poa spp., POT Z Potentilla nivea, SAL Z Salix reticulata, SIL Z Silene acaulis, STE Z Stellaria umbellata, TRD Z Trifolium dasyphyllum and TRN Z Trifolium nanum.

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Figure 2. Percentage of plant species (a) in forage and in paired-control plots and (b) in the chicks’ diet and in forage. *Significant difference in average amount detected through a paired t test. ACO Z Acomastylis rossii, BIB Z Bistorta bistortoides, BIV Z Bistorta vivipara, CAR Z Carex jonesii, CLA Z Claytonia lanceolata, GEN Z Gentianodes algida, JUN Z Juncus spp., MOSP Z moss spores, OXY Z Oxyria digyna, POA Z Poa spp., POT Z Potentilla nivea, SAL Z Salix reticulata, SIL Z Silene acaulis, STE Z Stellaria umbellata, TRD Z Trifolium dasyplyllum and TRN Z Trifolium nanum.

mirrored calling rates of the hens but were also highprotein foods, which are critical for chick growth and development (Robbins 1993). The ecological circumstances faced by white-tailed ptarmigan include factors such as a truncated breeding

Table 1. Percentage of foods consumed by chicks that were or were not associated with the hen’s food calls Food call foods Plant species

Nonfood call foods % Diet

Plant species

% Diet

Salix reticulata Bistorta vivipara Moss spores Trifolium dasyphyllum Acomastylis rossii Carex jonesii Gentianodes algida Stellaria umbellata Claytonia lanceolata Juncus spp. Oxyria digyna

38.3 21.5 7.5 5.6 5.6 4.7 3.7 2.8 1.8 1.8 0.9

Trifolium nanum Bistorta bistortoides Poa spp. Potentilla nivea Silene acaulis

1.8 0.9 0.9 0.9 0.9

Total percentage

94.2

5.4

season, ephemeral foraging areas, and limited time for chicks to develop efficient foraging skills. The latter seems especially important because inefficient foraging skills have been linked to juvenile bird mortality (Lack 1954; Perrins 1980; Sullivan 1989). This social transmission of food call information has been shown to increase chick foraging efficiency (Valone 1989). Research by Stokes (1971), Sherry (1977) and Moffatt & Hogan (1992) confirmed a similar vertical transmission of information in Burmese red junglefowl, Gallus gallus spadiceus, by documenting hens attracting chicks to food through vocalizations in laboratory studies. Although empirical laboratory experiments are vital for our understanding of social learning, Lefebvre & Palameta (1988) cautioned that socially learned behaviour demonstrated in a laboratory experiment may not diffuse into a wild population. Field studies of vocal communication in white-tailed ptarmigan enhance our understanding of vertical transmission of food resource information in avian species. The hen’s food call appears to function as a mechanism for transmitting foraging information within natural populations of whitetailed ptarmigan. This finding increases our limited knowledge of nonimitative social-learning mechanisms (Coussi-Korbell & Fragaszy 1995; Fragaszy & Visalberghi 1996; Galef 1996; Fritz et al. 2000).

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ALLEN & CLARKE: SOCIAL LEARNING IN PTARMIGAN

Plant species Figure 3. Bivariate regression comparing percentages of the hen’s food calls to certain foods with percentages of the same foods in the chicks’ diet. ACO Z Acomastylis rossii, BIV Z Bistorta vivipara, CAR Z Carex jonesii, CLA Z Claytonia lanceolata, GEN Z Gentianodes algida, JUN Z Juncus spp., MOSP Z moss spores, OXY Z Oxyria digyna, SAL Z Salix reticulata, STE Z Stellaria umbellata and TRD Z Trifolium dasyphyllum.

Moffatt & Hogan (1992) demonstrated the influence of the food calls of Burmese red junglefowl by using taperecorded calls of hens giving calls to both high-quality (mealworms) and low-quality (crumbs) food. Initially, chicks responded faster to calls to high-quality food. However, with continued reinforcement of the call to the low-quality food, chicks responded equally to both calls. Food calls influenced selection and quality of the chicks’ diet, showing the magnitude of social learning in the context of juvenile foraging. The white-tailed ptarmigan hen’s food call had similar compelling effects as it regulated chick diet and quality. For example, although chicks appeared to be unable to see what food a hen was eating (chicks frequently foraged on rocky-sloped areas behind rocks and facing away from hens), they still heard the food calls of the hens and responded to them. Over time, as hens stopped calling and mature chicks foraged further from the hen, the chicks continued to consume highprotein foods (e.g. S. reticulata). A potential evolutionary consequence is, as chicks become adults, they retain this knowledge and transfer it to the next generation through the hen’s food call, which has the potential for aiding chick survivorship.

Table 2. Protein content of foods eaten by white-tailed ptarmigan chicks as a total percentage of the hen’s food calls associated with each food Plant species Trifolium dasyphyllum Salix reticulata Bistorta vivipara Carex jonesii Acomastylis rossii Stellaria umbellata Gentianodes algida

Protein (mg/g)

% Food call

310 220 210 170 150 140 95

4.3 40.0 17.0 8.5 2.2 8.5 4.2

Values shown are medians. Moss spores, Juncus seed heads, Oxyria digyna and Claytonia lanceolata were too scarce to collect sufficient for protein analyses.

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