Final Thesis - Ronald Billy George Jildmalm
Food preferences in relation to nutrient composition in captive white-handed gibbons, Hylobates lar
The aim of the present study was to assess the occurrence of spontaneous food preferences in captive white-handed gibbons and to analyse whether these preferences correlate with nutrient composition. By using a two-alternative choice test three male Hylobates lar were repeatedly presented with all possible binary combinations of 10 types of food that are part of their diet in captivity. I found that with 36 out of 45 possible binary combinations the animals displayed a statistically significant preference for one of the alternatives. The gibbons exhibited the following rank-order of preference: grape > banana > fig > apple > pear > cantaloupe melon > carrot > tomato > cucumber > avocado. Correlational analysis showed a highly significant positive correlation between this food preference ranking and the total carbohydrate, fructose and glucose contents of the foods (P < 0.01). These results suggest that white-handed gibbons are selective feeders with regard to the source of metabolic energy as neither the content of total energy nor the contents of protein or lipids significantly correlated with the displayed food preference ranking. These findings are in agreement with the dietary habits observed in free-ranging animals of this species.
Most species of animals are highly selective about what they eat and spend a considerable proportion of their time and energy on searching for preferred foods (Hughes, 1993). This is also true for non-human primates (Thorington 1970, Waterman 1984). It is commonly agreed that the selective food choice that primates display is caused by two principal factors: the nutritional and/or toxic content of a particular food source (Freeland & Janzen 1974, Glander 1982, Ungar 1995, Simmen et al. 1999) and its relative spatial and temporal availability (Leighton 1993, Laska 2001, Stevenson 2003). Several other factors such as body size, gut morphology and taste perception have also been demonstrated to affect an animal’s choice of food (Hladik 1978, Glander 1982, Waterman 1984, Richard 1985, Martinez del Rio & Restrepo 1993, Ungar 1995, Visalberghi et al. 2003) but can generally be regarded as adaptations to the two previously mentioned principal factors (Laska 2001).
Several studies reported that food selection of non-human primates correlates negatively with the contents of toxic and/or digestion inhibitory secondary plant compounds (Waterman 1984, Glander 1982, Simmen et al. 1999), while only a few studies, in contrast, have been able to show a positive correlation between food selection and the content of any given nutrient (Martinez del Rio & Restrepo 1993, Laska et al 2000, Laska 2001, Visalberghi et al. 2003). This lack of positive correlations between nutritional content and food selection can possibly be explained by the complex chemical composition of plant foods and the trade-offs that primates have to make in order to gain sufficient amounts of required nutrients, while at the same time they try to minimize ingestion of potentially harmful plant secondary compounds (Glander 1982, Howe & Westley 1988).
A possible approach to study the relationship between nutritional content and the food preferences of non-human primates is to present them with binary choices of food items that contain very small and therefore presumably negligible amounts of secondary plant compounds (Laska et al. 2000). Laska et al. (2000) proposed that cultivated fruits could be used for this purpose. By repeatedly presenting captive spider monkeys with all possible binary combinations of 10 cultivated foods, Laska et al. (2000) were able to show a positive correlation between the food preferences displayed by this species and the content of total energy in the foods used. Additional studies that employed the same approach found that captive squirrel monkeys (Laska 2001), capuchin monkeys (Visalberghi 2003) and pacas (Laska 2003), like the spider monkeys, display food preferences that are highly significantly correlated with the total energy content, while pigtail macaques (Laska 2001), on the other hand, were found to prefer foods with high contents of total carbohydrates. The authors speculate that differences in the degree of frugivory might account for the fact that some primate species seem to be opportunistic with regard to their preferred source of metabolic energy whereas others are not.
The fact that white-handed gibbons, like pigtailed macaques, include a high proportion of sugar rich fruits in their natural diet and show clear preferences towards ripe fruits, which typically have the highest content of soluble sugars (Bollard 1970, Simmen et al. 1999), suggests that the total carbohydrate content in foods might be an important determinant of food choice for this species too (Carpenter 1940, Raemaekers 1978, Jolly 1985, Richard 1985, Ungar 1995, Ungar 1996). Furthermore, the findings that white-handed gibbons primarily meet their water requirement by consuming fleshy fruits and immature leaves, and only rarely drink from open water sources, suggest that also the content of water may be an important factor that determines their food preferences (Carpenter 1940, Raemaekers 1978).
The aim of the present study was therefore to assess the occurrence of spontaneous food preferences in captive white-handed gibbons by presenting them with all possible binary combinations of 10 cultivated fruits and to analyse whether these preferences correlate with the abundance of macro- or micronutrients in these food items.
Testing was carried out using one sub-adult and two juvenile male white-handed gibbons, Hylobates lar, of twelve, seven and five years of age, respectively. All animals were born and kept at Kolmårdens Zoological Park , Kolmården , Sweden , and descended from the same breeding couple. The gibbons were housed in two enclosures of 177 and 215m3, respectively, joined together by a corridor wherein two 10m3 test rooms were situated. The corridor was sealed by doors at both ends to allow for temporary separation of the animals. From the enclosure in which the two juveniles where kept, the animals had to move through the corridor to get to the test rooms, while the animals in the other enclosure could move directly into the test rooms through a sliding door in the adjacent wall. All animals were trained to enter the test rooms voluntarily and were completely accustomed to the procedure. The subjects were maintained on a 14:10 h light/dark cycle at 20- 22°C . The gibbons were fed commercial monkey chow and water ad libitum. Fresh fruits and vegetables were available to the gibbons ad libitum between 16:00 and 20:00 h and then removed over night.
Food preferences were assessed using a two-alternative choice test. The animals were presented with pairs of food items, and their choice behaviour, i.e., which of the two food items is consumed first, was recorded. Animals were tested singly in order to avoid competition or disturbance by conspecifics affecting a monkey’s choice behaviour.
The gibbons were separated for three sessions each day, at approximately 09:00, 12:00 and 15:00 h. The specific times were set in order to account for possible diurnal changes in food choice. During the sessions the gibbons approached a wooden shelf of 90 x 46 cm , mounted on the wall of the test room, chose one of a pair of simultaneously presented food items and then retreated, so the rejected food item could be removed. All foods were cut into cubes with the sides measuring 1 cm to avoid choice behaviour based on size differences of the food items. Sessions consisted of 20 pairwise presentations and the position of the food items (e.g., grape presented left and carrot presented right) was pseudorandomized in order to counterbalance possible side preferences. Schedules for all sessions were generated with the optimization software AMPL/CPLEX to assure optimal spreading of all 45 possible binary combinations of 10 types of food over the sessions and days. Each pair of food items was presented to an animal for a total of 12 times and care was taken to never present a food item that had been part of the previous pair.
The following types of food were employed: apple (Malus sylvestris), avocado (Persea gratissima), banana (Musa paradisiaca), cantaloupe melon (Cucumis melo cantalupensis), carrot (Daucus carota), cucumber (Cucumis sativus), fig (Ficus carica), grape (Vitis vinifera), pear (Pyrus communis) and tomato (Lycopersicum esculentum). The rationale for choosing these types of food was (a) that all of them are part of the animals’ diet in captivity and thus familiar to the gibbons and (b) that data for the contents of macro- and micronutrients in these types of food were available, allowing me to analyze correlations between food preferences and nutrient contents (Souci et al. 1989, Food Standards Agency 2002). In an attempt to minimize the inevitable intraspecific variation in nutrient composition, care was taken to always present food items of a given type with the same degree of ripeness.
A total of 1620 choices (45 binary combinations x 12 presentations per animal x 3 animals) were recorded, and food preference rankings were established using four different criteria.
Foods of a given type that were consumed first by an individual animal in the majority of presentations with a given binary combination (i.e., in at least 7 out of 12 presentations), were assigned 1 point and the alternative 0. If an animal chose both alternatives in a given binary combination equally often, both types of food were assigned 0.5 points each. The theoretical maximum score for any type of food with this criterion is 9 (9 combinations x 1 animal).
This criterion adopts the same assignment of points to preferred food items as for criterion 1, although, here, the points for all three animals were collapsed. Thus, the theoretical maximum score for any type of food with this criterion is 27 (9 combinations x 3 animals).
The sum total of choices for each of the 10 types of food across all binary combinations was built for each individual animal. The theoretical maximum score for any type of food with this criterion is 108 (9 combinations x 12 presentations per animal x 1 animals).
This criterion adopts the same procedure of building the sum total of choices as for criterion 3, although, here, the data for all three animals were collapsed. Thus, the theoretical maximum score for any type of food with this criterion is 324 (9 combinations x 12 presentations per animal x 3 animals).
Additionally, two-tailed binomial tests using the sum total of choices for each member of a given binary combination were performed to assess significant preferences both at the individual level, criterion 3, and at the group level, criterion 4, (P < 0.01).
Preliminary analysis revealed that the food preference rankings obtained with the four criteria showed significant correlations with each other (Spearman rs ≥ .93, P < 0.01 for all four criteria), i.e., they were very similar, though not identical (cf. Table 2); thus, for further analyses, only the rankings obtained with criterion 4 were used.
Correlations between the food preference rankings and the contents of nutrients were evaluated by calculating Spearman rank-order correlation coefficients rs, which were compared for significance with a list of critical values for two-tailed binomial tests.
Food preference rankings were separately constructed for 09:00, 12:00 and 15:00 h sessions and rankings were compared with each other and checked for correlations using Spearman rank-order correlation coefficients.
Table 1 summarizes the choice behaviour of the gibbons in the food preference tests, i.e., the number of choices made by the gibbons in favour of each member of a given pair of foods. With 36 out of 45 possible binary combinations, the animals displayed a statistically significant preference for one of the options (two-tailed binomial test, P < 0.01). Grapes, figs and bananas were clearly the most preferred food items and were significantly preferred over all other options (P < 0.01 for all 21 combinations). The attractiveness of grapes, figs and bananas is further displayed by the fact that 82.4 to 89.2 percent of all possible choices were in favour of these three food items (Table 2). Avocado was clearly the least preferred food and was never preferred over an alternative. Consequently, only 0.3 percent of all choices made, and hence the lowest percentage of all options, were in favour of this type of food.
Table 2 illustrates the food preference rankings derived from the gibbons’ choice behaviour according to the four criteria. Calculations of Spearman rank order correlation coefficients revealed that the rankings obtained with all four criteria were highly significantly correlated with each other (rs ≥ .93, P < 0.01 for all six combinations), i.e., they were very similar, though not identical. Comparisons of the preference rankings derived from criteria 1 and 3 show that the individual gibbons displayed highly similar patterns of preference (Spearman rs ≥ .93, P < 0.01). Thus, the rank order of preference obtained with all four criteria applies to the gibbons both as a group and as individuals.
The food preference rankings derived from the 09:00, 12:00 and 15:00 h sessions showed close to perfect correlations with each other (Spearman rs ≥ 0,96 , P < 0.01), i.e., they were similar though not identical (Table 3). The fact that the gibbons’ choice behaviour was almost identical during the three sessions indicates that the animals’ food preferences were stable across the day.
Table 4 summarizes the Spearman rank-order correlation statistics between food preference ranking and the nutritional content of the foods. The food preference ranking was highly significantly correlated with total carbohydrate content, and with the contents of fructose and glucose. The content of sucrose, on the other hand, did not show a significant correlation with the food preference ranking. The total energy content as well as the content of lipids and protein also failed to significantly correlate with the food preference ranking. Thus, the animals clearly preferred to consume foods high in glucose and fructose but did not significantly prefer foods that are high in other energy sources such as lipids and protein. Additionally, correlations between the food preference ranking and the content of water, dietary fibre, acids and vitamins also failed to show statistical significance. This was also true for all minerals except selenium which significantly correlated with the food preference ranking.
The results of the present study demonstrate that the food preference ranking of captive white-handed gibbons is highly significantly correlated with the contents of fructose, glucose and total carbohydrates of the food items used. Additionally, the animals’ food preferences were found to be stable across the day and representative for both individual gibbons as well as for the group as a whole.
It is important to recognize that several variables may influence an animal’s choice of food (Laska 2001, Stevenson 2003), and therefore it seems appropriate to consider whether methodological reasons might account for the observed food preferences. When faced with a situation in which to choose and consume one of two, or more, differently sized food items, nonhuman primates such as rhesus monkeys (Fay et al. 1953), chimpanzees, white-handed gibbons, and orangutans usually go for the largest piece available (Menzel 1960, Menzel & Davenport 1962, Draper & Menzel 1965, Menzel & Draper 1965). To eliminate a possible bias due to this factor, care was taken to always present the gibbons with food items of equal size.
The composition of nutrients in fruits changes with their stage of maturity (Bollard 1970, Simmen et al. 1999), and thus not surprisingly, ripeness of fruits has been shown to affect food choice behaviour in primates (Redford 1984, Richard 1985, Ungar 1995). In an attempt to limit potential effects of fruit maturation on choice behaviour, a given type of food was always presented with the same degree of ripeness.
Differences in palatability and/or novelty of food items might also affect an animal’s choice behaviour (Visalberghi et al. 1998, Laska 2001, Visalberghi et al. 2002, Visalberghi et al. 2003). To control for these factors, all foods presented to the gibbons were selected from the diet that the animals were regularly fed and were hence familiar with and palatable to the animals.
Additionally, monkey’s food choice behaviour can be affected by social context (Visalberghi et al. 1998). Thus, all animals were tested separately to avoid disturbances and/or competition between conspecifics from influencing an individual’s food choice behaviour.
In the wild, white-handed gibbons (Raemaekers 1978), as well as several other primates (Thorington 1970, Whitten 1982), have been shown to vary both quantity and type of consumed food with the time of day. To eliminate possible bias from diurnal variation in diet, the twelve presentations of a given binary combination were spread as evenly as possible over 09:00, 12:00 and 15:00 sessions.
Finally, it is well known that side preferences may affect an animal’s choice behaviour, and this was controlled for by pseudorandomizing positions of food items.
The feeding regimen employed in this study was adjusted so that neither ravenous hunger nor satiety was likely to affect the individual gibbons’ food choice behaviour.
Thus, it is likely that the observed food preferences indeed reflect the gibbons’ ability to choose between food items on the basis of perceived differences in nutritional content.
The finding that the gibbons displayed food preferences that were highly significantly correlated with total carbohydrate content, but not with total energy content, suggests that these lesser apes are selective feeders with regard to energy gain. This supposition is supported by findings that wild gibbons include a considerable proportion (59 to 87%) of sugar rich fruits in their diet and that they demonstrate clear preferences towards ripe fruits (85%) (Carpenter 1940, Raemaekers 1978, Jolly 1985, Richard 1985, Ungar 1995, Ungar 1996), which typically have the highest content of sugars (Bollard 1970, Richard 1985, Simmen et al. 1999).
The fact that the content of glucose and fructose significantly correlated with the gibbons’ food preference ranking, while the content of sucrose did not, is surprising. It has been demonstrated that humans as well as squirrel monkeys are unable to discriminate between the taste of sucrose, fructose and glucose when their relative concentrations are adjusted (Breslin et al. 1994, Breslin et al. 1996, Laska 1997). This indicates that these three sugars are experienced as having the same taste quality. Assuming that white-handed gibbons, like humans and squirrel monkeys, are unable to discriminate between the taste quality of sucrose, fructose and glucose, there has to be an alternative explanation for the obtained results. One such explanation could be the selection of foods presented to the animals. In the majority of ripe fruits the sugar composition is predominated by the content of sucrose (Simmen & Sabatier 1996). However, this is not the case with grapes (Souci et al. 1989, Food Standards Agency 2002), in which the ratio between sucrose and fructose and sucrose and glucose in both cases is 0.06, i.e., the content of sucrose is much lower than both the content of fructose and glucose. The fact that grapes are ranked as the most preferred food, and that they have a low content of sucrose compared to most other foods tested, inevitably affects the correlation between sucrose and the food preference ranking displayed by the gibbons. Therefore, the content of sucrose highly significantly correlated with the animals’ food preference rankings when grapes were removed from the statistical calculation while, at the same time, all other correlations stayed more or less the same. This suggests that the lack of a significant correlation between the animals’ food preference ranking and the content of sucrose might indeed be the result of the fruits selected by the experimenter.
5.2.3 Protein and lipids
The lack of a significant correlation between the gibbons’ food preference ranking and the content of proteins and lipids could possibly be explained by the fact that the present experiment only considered and tested preferences for fruits and vegetables. These foods are generally poor sources of proteins and lipids (Souci et al. 1989, Simmen & Sabatier 1996, Waterman 1984, Food Standards Agency 2002) and several free-ranging frugivorous primates therefore frequently supplement their diet with leaves and/or insects (Raemaekers 1984, Richard 1985, Oftedal 1991). Leaves contain levels of protein that are on average five times as high as those normally found in fruits and therefore constitute an excellent source of this macronutrient (Waterman 1984). Insects are likewise good sources of high quality protein but may additionally supply high levels of lipids (Ramos-Elorduy et al. 1997, Banjo et al. 2006), which is a macronutrient that most leaves selected by monkeys are short in (Simmen & Sabatier 1996).
Several field studies have shown that white-handed gibbons often include both these sources of protein in their diet, although their relative proportions, 3 to 34 percent and 3 to 24 percent of total time spent feeding on leaves and insects respectively, differ with the location and/or the method used to collect data (Carpenter 1940, Raemaekers 1977, MacKinnon & MacKinnon 1978, Raemaekers 1978, Ungar 1995, Palombit 1997). The percentage of insects, however, may, according to Redford et al. (1984) be underestimated in the reported diets of several primates. They suggest that a significant percentage of the observed behaviours scored as fruit eating may in fact result in significant and intentional ingestion of invertebrates. This could also be the case for white-handed gibbons given that almost half of their fruit consumption consists of figs (Ungar 1995), which according to Janzen (1979) at some times of the year become filled to the capacity with coleopteran and diptera larvae. In view of the fact that leaves and insects constitute a considerable proportion of the diet, and together provide sources of protein and lipids that generally are several times higher than those found in fruits, it may make sense that the gibbons did not choose fruit or vegetables based on the content of protein or lipids. This was even the case despite the fact that one of the foods used in the present study – avocado – contains an untypically high proportion of lipids.
The finding that the gibbons displayed food preference rankings that were not significantly correlated with the content of any micronutrient, except selenium, suggests that these lesser apes are not selective feeders with regard to minerals or vitamins.
Wild plant parts and insects have been demonstrated to contain moderate to high levels of several micronutrients, and given that gibbons include a wide variety of foods in their diet, they should easily be able to reach optimal levels of required minerals and vitamins (Nagy and Milton 1979, Ramos-Elorduy et al. 1997, Milton 1999, Milton 2003, Banjo et al. 2006). As nonhuman primates are very similar to humans in physiology, and therefore presumably subjected to similar micronutrient requirements (Portman 1970), this supposition is supported by findings that several primate species ingest levels of micronutrients that are far higher than those recommended for humans (Milton, 2003). Milton (2003) suggests that this high intake of micronutrients might not be necessary but rather unavoidable due their highly plant-based diet. In view of these facts it seems very unlikely that white-handed gibbons would need to prefer foods with high contents of micronutrients, and would therefore benefit more by preferring foods that are high in other, less plentiful nutrients. It is therefore a bit difficult to explain why the gibbons’ food preference rankings significantly correlated with the content of selenium. The most probable explanation for this finding, though, is that it is a “false positive”, i.e., that the content of selenium just happens to significantly correlate with food preferences due to the choice of foods presented to the gibbons. The fact that the content of selenium significantly positively correlated with the total carbohydrate, fructose and glucose content of the food items supports this supposition.
Somewhat surprisingly, the results of the present study showed that the food preferences displayed by the gibbons were not significantly correlated with the content of water. Given that white-handed gibbons primarily meet their water requirement by consuming fleshy fruits and immature leaves, and only rarely drink from open water sources, a positive correlation might have been expected (Carpenter 1940, Raemaekers 1978). However, plant foods that are high in water content are typically low in carbohydrate content as well as in content of other forms of metabolic energy such as proteins or lipids (Souci et al. 1989, Food Standards Agency 2002). For example, cucumber and tomato, two of the least preferred types of food in this study, have the highest water content but, at the same time, they have the lowest carbohydrate content of all options tested (Souci et al. 1989, Food Standards Agency 2002). Thus, the white-handed gibbons may trade-off the content of water for total carbohydrate content of potential food items. An alternative explanation could be that the water content of fruits and immature leaves, which generally exceeds 80 percent of the wet weight (Waterman 1984), would supply primates with an abundance of water, which has been suggested by Nagy and Milton (1979). If this is the case, then gibbons would likely be able to meet their water requirement while foraging for foods high in other, less abundant nutrients. Thus is seems plausible that white-handed gibbons do not need to prefer foods with high contents of water but rather select their food based on the content of carbohydrates.
By employing the same method, and with few exceptions, using the same types of foods as the ones used in the present study, Laska (2001) showed that the food preferences displayed by pigtail macaques significantly correlated with the total carbohydrate content of the food items. In line with the findings for the white-handed gibbons tested here, the pigtail macaques’ preference for food items was not significantly correlated with the contents of total energy, lipids or proteins. In contrast to Hylobates lar and Macaca nemestrina, though, the food preferences of several other species like spider monkeys (Laska et al. 2000), squirrel monkeys (Laska 2001), capuchin monkeys (Visalberghi 2003) and pacas (Laska et al. 2003), have been shown to significantly correlate with the total energy content of food items, independent of the source of metabolic energy.
Laska and co-workers (2000, 2001, 2003) have speculated that differences in the degree of frugivory might account for the fact that some primate species seem to be opportunistic with regard to their preferred source of metabolic energy whereas others are not, but so far the data are inconclusive and further research with other species is therefore needed in order to prove or disprove this hypothesis.
An alternative explanation that could possibly account for the contrast between the species and their respective preferences for different sources of metabolic energy is competition for food by sympatric animals. In order to minimize competition and to be able to survive and reproduce in large communities of different species, animals have to find their own specific food niche (Mackinnon & MacKinnon 1980). In view of the fact that most primates (Harding 1981), as well as several other mammals and birds (Payne 1980), at least partially include fruit in their diet, it is reasonable to assume that there is a considerable competition for this food resource. It might therefore make sense that frugivorous species may display different preferences for food items and the respective nutrients that they contain.
The results of the present study provide evidence that captive white-handed gibbons display marked food preferences when repeatedly presented with all possible binary combinations of 10 cultivated fruits and vegetables. Correlational analyses revealed that the white-handed gibbons are selective feeders that prefer to meet their daily energy requirements by consuming foods with a high content of total carbohydrates. This finding is in agreement with their dietary habits in the wild, as white-handed gibbons include a considerable proportion of sugar rich fruits in their diet and display clear preferences towards ripe fruits which typically contain the highest contents of soluble carbohydrates.
It has been speculated that differences in the degree of frugivory might account for the fact that some primate species seem to be opportunistic with regard to their preferred source of metabolic energy whereas others are not, but so far the species data is contradictive and additional studies with other species that display dissimilar degrees of frugivory are therefore required in order to prove or disprove this hypothesis.
I would like to thank my supervisor Matthias Laska for the amount of energy and engagement that he has put into this work. I would also like to thank Mats Amundin as well as the carpenters and gibbon caretakers at Kolmården zoological park for all their help. Finally, I would like to thank Åsa Holm for her help in constructing the computer program that allowed me to optimize the day to day schedules that I used during the experiment.
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Last updated: 05/07/08