Zoo Biology 857-65 (1989)

Effect of Food Preparation on Feeding Behavior of Lion-Tai led Macaques Amy Smith, D.G. Lindburg, and S. Vehrencamp

Biology Department, University of California, San Diego (AS., S. K), and Center for Reproduction of Endangered Species, Zoological Society of San Diego (0. G. L.), San Diego

Ten group-living lion-tailed macaques (Mucacu silenus), accustomed to receiving fruits and vegetable items of the diet in chopped form, were given these same foods in whole form to compare reactions to the non-nutritional properties of food. Contrary to common belief, the access of individuals to the different food items was not equalized through chopping into bite-sized morsels. Mean dietary diversity actually increased with presentation of whole foods, as did time spent feeding and total amount of food consumed. The widespread practice of chopping of food for captive primates has little to commend it in light of these findings.

Key words: Mucuca silenus, diet, colony management

INTRODUCTION

A common practice in the feeding of naturalistic diets to captive primates is to present items such as fruits and vegetables in chopped form. This practice stems from the belief that competition between individuals leads to unequal access to the more preferred foods when offered whole. Unequal distribution in turn incurs nutritional deficiencies for subordinate individuals.

Studies of wild troops indicate that primates as a rule spend a major portion of each day in foraging [Jolly, 19721, and that diets are highly europhagic [Clutton- Brock, 19771, offering marked variation in the tasks of food harvesting and process- ing. In addition, studies of food choice point to the importance of organoleptic qualities (i.e., attributes which are stimulating to the sense organs) [Lang, 19701 which affect food intake and which are altered by human processing. Although nutritional concerns have taken priority in captive provisioning, the feeding styles of animals under natural conditions implicate the non-nutritional properties of food as important to psychological, and perhaps to oral, health. Approaches which enrich the

Received for publication March 8, 1988; accepted June 1, 1988. Address reprint requests to D.G. Lindburg, Center for Reproduction of Endangered Species, San Diego Zoo, P.O. Box 551, San Diego, CA 921 12.

0 1989 Alan R. Liss, Inc.

58 Smith et al.

captive feeding process may therefore outweigh disadvantages incurred from unequal distribution of food items, and obviate the need for human processing.

To this end a study was devised which would investigate the effects of food preparation on feeding behavior in a captive colony of lion-tailed macaques (Macaca silenus). In the wild, lion-tails are known to feed on a wide variety of fruits, leaves, seeds, flowers, etc. [Green and Minkowski, 19771, and it is reasonable to assume that the parts and quantities of individual food items consumed vary with time and place, as has been shown for other macaques (e.g., M . mulatta) [Lindburg, 19761. While the range of selection criteria and processing tasks thus employed in the wild far exceeds anything possible under the simplified dietary regimes of captivity, it was hypothe- sized that the feeding of unchopped foods would increase feeding time but would reduce diversity of intake due to competition for the most preferred food items.

MATERIALS AND METHODS Enclosures

The animals were housed in two off-exhibit cages, each measuring 5.4 X 3.6 X 4.0 m, and connected by an access-controlled tunnel at the Primate Research Pad of the San Diego Zoo. The first cage contained numerous branches, ramps for climbing, a nestbox, an exercise wheel, and chains for swinging. The floor of the cage was covered with straw. Generally, the tunnel was left open and the macaques were allowed access to the second cage which differed from the first only in that it contained no exercise wheel and the concrete floor was free of straw. During observation, the animals were placed within the second cage, with the tunnel closed, before they were given their morning browse. The bare concrete floor granted the observer maximum visibility of food, and the confinement of the animals to one cage allowed for maximum between-animal competition.

Subjects Ten of the 12 members of a lion-tailed macaque group served as subjects. This

group originated with 3-5 founders of unknown provenance, acquired by a European zoo in 1963 and 1965. In 1983, the entire colony was acquired by the San Diego Zoo. Recruitment was by birth only, except for the adult male, which was added to the group 3 months before the study began. Two group members were excluded from observations. A male approaching 3 years of age, having cerebral palsy, was hand-fed by staff and was unable to climb up and through the tunnel to the observational side of the enclosure. The 12th individual was a clinging infant, not yet capable of taking solid food. The ranks assigned in Table 1 were based on pretest determination of winners and losers in contests over food and other resources.

Daily Diets The animals were fed commercial chow (15 biscuits per animal) at 7:OO A . M . ,

and browse (branches of Syzygium paniculatum and Hibiscus rosa-sinensis) at 1O:OO A.M. Then, just prior to the actual observation period, they received “greens” (described in Table 2). Since the amount of greens consumed could affect the quantity of study food an animal ate, their consumption was carefully monitored. When the group was no longer eating or handling the “greens,” the study food, consisting of fruits and vegetables (see Table 3 for description) was fed. Except for some pretest

Macaque Feeding Behavior 59

TABLE 1. Composition of the study population

Animal Sex Rank Age (years) Comment

Celie F I c. 23 Postmenopausal; no known offspring in group Linda F 2 c. 14 Gave birth during study Stephanie F 3 1.5 Daughter of Linda Ginger F 4 C. 10 Suspected sister of Linda; no offspring Bonnie F 5 C. 9 Lactating, mother of Henri Amir M 6 6 Introduced as breeder 3 months before study began Kim0 M 7 2.8 Son of Marge Lenore F 8 c. 10 Apparently nulliparous Marge F 9 c . 23 Postmenopausal, mother of Kim0 Mrs. C F 10 c. 21 Very small, with scoliosis; separated from group at night for

urine collection Kim M - 2.8 Son of Bonnie; has cerebral palsy; excluded from

observations Henri M - 0.08 Suckling infant, excluded from observations because of age

TABLE 2. Description of “greens” fed each day prior to study food

Amount placed in cage

Green beans 3 11.3 each Spinach 1 root stalk 33 .O/stalk Kale 1 stalk 55.7lstalk

0.5 stalk 76.6/stalk Celery

Average weight Food type per individual (gs)

TABLE 3. Description of study foods

Average weight Food type Amount fed (gs) No. of bites

Broccoli 2 stalks 260.751stalk 52istalk Papaya 1 445.00 each 32 each Bananas 5 191.58 each 11 each Grapes 40 3.19 each 1 each Carrots 2 175.67 each 18 each Yams 2 233.29 each 50 each Apples 3 189.08 each 40 each Oranges 3 186.17 each 20 each

feeding sessions, these items had been fed in chopped form from the time the group was acquired in 1983. In addition to the daily diet, once or twice a week the group received a cup of mealworms, scattered throughout their cage, or two onions. These were fed only on days that the macaques were not observed.

Food Preparation

Test foods were presented whole or chopped on alternate days. On chopped days, the number of pieces/slices of each food type was counted. By knowing the number of pieces and the average weight of each food type (Table 3), the amount consumed by an individual could be determined. For example, if one carrot was cut into 60 slices of which the animal consumed three, it could be said that the animal ate

60 Smith et al.

(3/60) (175.67) = 8.78 g of carrot. The technique was applied similarly to all food types.

On whole food days the food was served uncut, except for bananas that were served in halves. Since the mean number of bites required to consume a whole food item had been established in pretest feeding sessions (Table 3), it was possible to measure the amount in grams of whole food consumed by counting bites instead of slices. Bite counts were not required for bananas and grapes, as any whole portion of these handled was also immediately consumed. As shown in Table 3, papayas and oranges contained few bites relative to their size. This occurred because these fruits are soft and pulled from the skin, and large bites were easily handled by the macaques’ mouths.

Like macaques in the wild [Lindburg, 19711, captive subjects will engage in preconsumptive food preparation. Obvious examples are the peeling and dividing of foods such as oranges and bananas. However, in this study the outside fibers were pulled from broccoli stalks, grape peels were removed in the mouth and expelled, papaya peel was left uneaten and carrots, yams and apples were “peeled” by biting off the outside edges. Only those bites actually consumed were taken into account when calculating dietary intake.

Food Presentation Since the group had been moved to the cage without straw before their morning

browse, they were correctly positioned for the study. A keeper or an experienced volunteer fed the whole or chopped foods, accomplished by tossing and thus scattering the food through a ground-level cage opening. This was the standard method of food presentation for the group, and no changes were made for either the whole or chopped presentations. All test feedings were performed at routine meal times, and the cages of animals were fed in the usual order, to avoid stressing the animals by altering their routine.

Observation The experiment was conducted between September 15 and November 15, 1986.

Feeding data were collected by one observer (author A.S.) between 9:OO and 11:OO A . M . , using a focal animal method. The observation period began upon food presentation and ended when the focal subject had finished its initial feeding. An “initial feeding” was defined as the period of time in which an animal ate continu- ously. This period ended when the animal had not gathered new food or chewed stored food for 5 minutes. The time that it took for the group to complete its initial feeding was recorded daily and, like that of the focal animal, ended when no individuals had taken food for five minutes. Each focal animal was observed on 2 consecutive days and was served a chopped version of the food on 1 day and whole food the next, creating a set of paired samples. The order of testing was randomly determined. After each of the ten animals was observed in this way once, the process was repeated, reaching a total of 40 days of observation.

RESULTS Feeding Duration

Using the data from duration of “initial feedings” as defined above, the group spent significantly more time in feeding when food was presented whole than when

Macaque Feeding Behavior 61

TABLE 4. Diversity indices for each individual under both food preparation types*

Individual Whole diversity index Chopped diversity index

Celie ,543 ,147 ,303 ,320

Linda ,241 .436 ,502 ,373

,761 ,660 Ginger .67 1 ,396

,370 ,589 Bonnie .488 ,453

,484 ,349 Amir ,124 ,440

.679 ,699 Kimo ,595 .610

,721 ,542 Lenore ,551 ,625

,673 .303 Marge .668 ,565

.522 . 592 Mrs. C ,462 ,461

,471 ,231

Stephanie .529 ,439

*Higher values indicate greater dietary diversity.

presented in chopped form (paired t-test, 2-tailed, t = -3.36, P = .003). In effect, this difference resulted from the food being parcelled into bite-size units by the animals instead of by their keepers.

Feeding Diversity and Rank The Shannon index of heterogeneity [Pielou, 19751 was employed to detect

diversity in the animals’ diets as influenced by the two preparation types. This index (as applied here) varies from a value of zero for individuals whose diet on a given day consisted entirely of one food type to relatively higher values for individuals who ate portions of each of the eight food types. Diversity indices for the ten subjects in both iterations of testing are shown in Table 4.

To analyze the effect of rank (the independent variable) on dietary diversity (the dependent variable), both ranks and diversity indices were treated as continuous variables. A polynomial regression was applied to the data, using a stepwise regression procedure. It was concluded that two different second-degree polynomials (quadratic equations) fit the whole and chopped diversity data. The regression lines show (Fig. 1) that diversity for both whole and chopped forms of presentation decreased at both the dominant and subordinate ends of the hierarchy.

Each regression is significant as determined by F-tests (chopped: F = 4.131, df = 2,17, P = .034; whole: F = 3.614, df = 2,17, P = .049). This result indicates that the relationship between diversity and rank is substantial, but curvilin- ear. This conclusion is further supported by the adjusted R-squared values (.248, .216), indicating that 25% of the variation in chopped food diversity and 22% of that in whole food diversity can be explained by differences in rank.

Finally, a comparison of diversity indices revealed a difference in central

62 Smith et al.

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=n H

a

z .5.

.4.

I _

p .3.

.2.

m- Whole y = -278 + . 1 0 9 X - . 0 0 9 X 2 p=.0492 0 ------ Chopped y = -166 + - 1 2 4 ~ - .01sf2 p=.0345

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0 - 1 , . , , , , , . I . , , , . , , , , , , , ,

lndiuidual Rank

Fig. 1. chopped food types.

Second-order polynomial regression models fit to diversity of consumption for whole and

tendency between whole and chopped food indices (Wilcoxon signed-ranks test, 2-tailed, P = .043). In fact, the groups’ diet is more diverse when fed whole food (mean = S48, s = .142) than when food is presented in chopped form (mean = .461, s = ,148).

Amount of Food Consumed In order to assess the effects of preparation type (whole or chopped), food type

(eight varieties), and individuals (ten) on food consumption by weight, a three-factor ANOVA was performed. The results of the test, using these three categorical predictor variables and the continuous outcome variable, are presented in Table 5. The test result showed a significant difference in mean weight consumed for different individuals, preparation types, food types, and the interaction of individual and food type. This implies that individuals were unique in the amount of food they consumed, that certain food types were generally consumed in greater amounts than others, but that the differences in weights of food items consumed were not the same for all individuals (i.e., the group consumes relatively more bananas by weight than any other food type, but bananas are not included in the diet of Mrs. “(2”). It is noteworthy that these conclusions are unaffected by food preparation method.

For the purpose of this study, the interesting aspect of the ANOVA results is that the average weight of food consumed differed between preparation types. Inspection of the data reveals that the average macaque consumed more food when it was served whole (395 g) than when presented in chopped form (306 g).

DISCUSSION

The results of this study indicate that achieving complete equity of diet in group-living macaques by chopping foods is unlikely. The eight foods used in this

Macaque Feeding Behavior 63

TABLE 5. Relationships among individuals, food types, and preparation types, in affecting food consumption

~

Source Sum of squares DF F-ratio Prob.

Preparation types (N = 2) 9,810.10 1 4.46 ,036 Food types (N = 8) 226,569.06 7 14.73 .ooo Individuals (N = 10) 168,756.24 9 8.53 ,000

Individuals X food 602,024.11 63 4.35 .ooo Individuals X preparation 23,850.24 9 1.21 ,295

Preparation X food 23,209.42 7 1.51 ,168 Individuals X preparation X food 106,755.86 63 .77 ,881 Residual 351,645.42 160

study were represented in varying proportions in the diets of the ten individuals either because of group-imposed hierarchical relationships or individual preferences. Indi- viduals in the highest ranks may eat different food types than subordinates because they acquire and hoard those items that are generally preferred. Bananas and grapes, for example, were always ardently consumed within the first few minutes after presentation. During this preliminary period subordinate individuals held back, while the centrally ranked animals snatched food items at risk of aggression from the dominants. As undesirable as this scenario may be to those hoping for equity of diet between individuals, it should be noted that the type of preparation does not affect these competitive interactions.

The foregoing observational and statistical conclusions establish the somewhat lower dietary diversity for individuals at opposite ends of the status hierarchy. While dominant individuals eat only the generally preferred foods and the subordinates eat what is left over, the centrally ranked individuals are able to obtain some of the preferred foods and finish their feedings with the leftovers, explaining their higher diversity scores. As noted earlier, the purpose behind chopping the animals’ food is to provide high intra-individual dietary diversity, especially for the low-ranking animals. However, the ANOVA results show that chopping food into bite-sized morsels does not remedy the situation. Both ends of the hierarchy have low diversity scores, regardless of preparation type.

For the group as a whole, mean dietary diversity was increased when the macaques were provided with unprocessed food. This result is quite the opposite of what would have been expected if chopped food had truly created more diversity in food intake.

The ANOVA’s indication that individual macaques consume dissimilar amounts of food is not surprising, since each animal undoubtedly has a distinct metabolism and level of activity. However, preparation also affects the mean amount eaten in that whole foods caused the animals to consume more in their initial feeding. This finding is more difficult to interpret. Perhaps whole food was a novelty that stimulated increased consumption, despite that it had been served during preliminary testing and that the present study lasted 8 weeks. If novelty is a factor, the amount of whole food consumed should eventually decrease to that of chopped food. Another possibility is that whole food naturally increases a hoarding propensity, although this has not been documented. Finally, in the analysis of the time data, it was found that more time was allocated to the initial feeding of whole food than to that of chopped. Again, novelty is a possibility, as are the different requirements for handling whole food. The latter

64 Smith et al.

is plausible due to the macaques’ aforementioned practice of peeling food items and the need to process food into ingestable portions. Then again, since they are eating more food when presented whole, consumption would logically require more time.

The preparation/food type interaction extends what is known about the main effect of food-that although the macaques eat different amounts of each food type, the differences are the same for both preparation types. Similarly, the preparation- /individual interaction supplements the main effect of individuals by indicating that although they consume different amounts of food, that dissimilarity holds true for both preparation types. Also, the preparation/individual/food type interaction imparts the information that although individuals vary in the types of food they eat, those differences are not affected by its preparation.

The discovery that rank differences and/or personal preferences will affect individual consumption in captive primate groups is not new. However, it is instruc- tive to note that the food preparation regimes which have been prescribed to alleviate these inequalities may fall short of achieving their objective. Where “naturalistic” foods are the sole or primary food source, it appears likely therefore that the nutritional health of some group members could be imperiled.

While the dietary idiosyncracies of individuals in this study were unaffected by food preparation, the feeding of unchopped food did have three consequences-an increase in the amount consumed during initial feedings, an increase in feeding time, and an increase in the mean dietary diversity of individuals. Given the observations on europhagy and time spent foraging which characterize primates in the wild, the latter two findings suggest that the feeding of whole foods has more to commend it than merely a savings in human labor, viz., that it fosters conditions which more closely mimic those in nature and which are therefore more likely to contribute to psychological well-being.

CONCLUSIONS

1 . The presentation of “naturalistic” foods in chopped form failed in its intended objective of achieving dietary equity among group members. Dominant individuals had priority of access to preferred foods whether presented whole or chopped.

2. Diversity in foods consumed was lowest for individuals at both the dominant and subordinate ends of the status hierarchy, regardless of preparation type. However, mean diversity indices of all individuals were higher when food was presented whole.

3. Quantity of food consumed was higher on the average when food was presented whole.

4. Total time spent feeding was greater, as a result of increased consumption and processing requirements, when whole foods were offered.

ACKNOWLEDGMENTS We thank the animal technician staff of the Center for Reproduction of Endan-

gered Species for its cooperation during the study, and Dr. A. Susan Clarke for comments on the manuscript. Manuscript preparation was by Sharon Dinwiddie. This is a publication of the Behavior Unit of the Center for Reproduction of Endangered Species.

Macaque Feeding Behavior 65

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