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Home , Agile gibbon, Hoolock gibbon, Siamang, Western hoolock gibbon

Wild ’ Diet A Literature Review Gabriella Skollar

Gibbons are one of the most threatened globally (Melfi, 2013), primarily due to loss of their forest habitat due to crop cultivation, , hunting for bushmeat and for the wildlife trade. Currently, there are 20 recognized species, including the newly described Skywalker (Hoolock tianxing) (Fan et al. 2017), making them the most diverse of all . The species are grouped into 4 genera, separated largely by differences in karyotype. (Cunningham, 2009)

Gibbons are arboreal and live and forage for food in the upper forest canopy. When feeding on small terminal branches, gibbons use quadrumanous climbing and a variety of seated and suspensory feeding postures. When they travel, they move through the canopy by brachiating. Their travel paths reflect detailed knowledge of the territory and its food sources (Brockelman et al. 2014).

Gibbons spend 50–70 percent of feeding time consuming fruits, including figs ( spp.) (Raemaekers 1979, Gittins 1982, Chivers 1984, Srikosamatara 1984, Ungar 1995, Palombit 1997, McConkey et al. 2002, Bartlett 2009). Although ripe fruits are the major food type in their diet, they also consume smaller percentages of young leaves, shoots, flowers, and insects. Fruit sources vary in size from vines and understory trees to large canopy trees with superabundant crops. (Suwanvecho, 2017).

Their average home range is 40 ha (approximately 100 acres), and their territory makes up about 80 percent of it. (Bartlett, 2007). If there is a drop in food availability, gibbons can adapt by increasing their day range, increasing foraging time, or increasing their territory size. Gibbons are important seed dispersers. They play an important role in forest regeneration and are essential for the healthy forest ecosystem. (Bach, 2018)

Avery K. Twitchell-Heyne, in her 2016 literature review of 34 studies from the last five decades on wild gibbons feeding ecology, found significant differences between the four genera. According to her paper, gibbons spend on average 24% and 36% of their feeding time eating figs and non-fig fruits (60% total fruit), followed by 28% leaves, 6% flowers, and 6% . The four genera had significant differences in their habitat, including amount of annual rainfall, latitude, altitude, territory, and forest size, which was reflected in differences in their diet composition, in the amount of all fruit and leaf consumption, and plant food diversity. The genus spent the highest amount of time eating leaves, 44% of total feeding time, followed by the 31%. Hoolock and Nomascus together had the most extreme habitat, the highest altitudes and latitudes, the least rainfall, and the most fragmentation and the greatest variation in diet composition. (Twichell-Heyne, 2016, Guan, et al. 2017)

As preferred food items become increasingly scarce, gibbons alter their diet by including greater amounts of lower-quality items, such as leaves, often labeled as fallback foods. Some species are able to maintain high rates of fruit in the diet by making increased use of keystone foods (Gilbert 1980). Keystone plant resources represent a special class of fallback food that Terborgh (1986) defines as any reliable food item that plays a prominent role “in sustaining frugivores through periods of general food scarcity”. Gibbons often rely on figs as fallback food. (Clink, 2017)

Gibbons’ diet tends to change to season to season. During the dry season (November – April) there is less fruit available and many species of gibbons adjust to this change by an increase in leaf consumption and a decrease in fruit consumption. Their activity also changes; in the dry season the gibbons spend more time eating overall and less time on other activities compared to the wet season (May – October). Fruit consumption usually peaks during the wet season. (Frechette, 2017)

Gibbons’ habitat also changes annually. Usually, trees do not have two heavy- fruiting years in a row. Gibbons have to develop a knowledge of their habitat, where their preferred and less-preferred fruit are available. As the forest changes seasonally and annually the “gibbons’ menu” seems to be “reshuffled” every year. (Suwanvecho, 2017)

Leaf consumption also increases as the forest became fragmented, as well as time spent on foraging and feeding. Western hoolock gibbons’ fruit consumption was ranging from 34-71% of total feeding time in different months. In January they consumed 63% leaves and only 37% fruits. (Borah, 2017)

Leaves were the main dietary item for northern white-cheeked gibbons in Laos throughout the year (53-85% of monthly diet), but gibbons increased their fruit consumption whenever fruit was most abundant in the forest. (Ruppell, 2013)

In habitats where smaller gibbons and co-occur in and , the larger siamangs rely more on young leaves than do the smaller lar gibbons, which eat more fruit (1997, Palombit). The siamangs also have smaller day ranges (1 km or less) and smaller home ranges (18–50 ha) than the smaller gibbons.

Different species of gibbons can adapt differently to mountainous and northern habitat. During the coldest months (December to February), there are no figs and non-fig fruits available for eastern hoolock gibbons living in higher elevation. When fruits were not available, hoolock gibbons shifted to a diet mainly of leaves and they increased feeding time. When fruit was more available, hoolock gibbons also spent more time feeding on insects and less time feeding on leaves. Insect feeding has been widely reported in different gibbon populations as an alternative source of protein. (Fan, et al. 2012)

For a group of blackcrested gibbon (Nomascus concolor) also found in high elevation, fruit consumption varied from 0.3 to 82.7%; figs from 0 to 68.2%; tree leaves and buds from 1.5 to 83.3%; vine leaves and buds from 3.1 to 61.9%; and epiphyte leaves from 0 to 22.2% of the proportion of their diet. (Fan, et all. 2008)

Javan gibbons in higher elevation habitats have substantially larger home ranges than lowland populations, despite a broad similarity in their activity budgets and diets. (Kim, 2011)

Many also eat flowers, but flowers are not generally regarded as making an important contribution to primate energy budgets. There have been reports of gibbons and siamangs relying on flowers both as a fallback food and as preferred food items. Siamangs at Way Canguk spent 12% of feeding time eating flowers from October 2000 to August 2002, and in 1 month flower-feeding time exceeded 40% of total feeding time. Flower-feeding time was highest in months when non-fig fruit- feeding time was lowest, and a switch from heavy reliance on fruit to substantial flower consumption was associated with a shift in activity patterns toward reduced energy expenditure, which is consistent with the interpretation that flowers may function as a fallback food for Way Canguk siamangs. (Lappan, 2009).

In Central Kalimantan, the diet of two groups of hybrid gibbons was mostly influenced by the availability of flowers. When flowers were most abundant the gibbons increased their consumption, and they also ate more figs and young leaves to satiate their hunger and seek a dietary bulk from more easily available food. (Mcconkey, 2003)

In Sabangu, Indonesia, gibbons also ate a higher percentage of flowers during the dry season, more than availability would have suggested, it was a preferred food. (Cheyne, 2010).

In summary, gibbons are frugivores but they can adapt to some extent to various climate and geographic variables, seasonal changes and human-induced changes such as deforestation and forest fragmentations, by switching to other food sources, when preferred fruits are not available. How these changes affect the population and the individual gibbons’ health still need to be answered. Frugivorous primates may suffer weight loss, increased mortality, or impaired reproduction in years when the diversity of fruits is low. Does it affect their sex ratio? Are they more prone to diseases? How is the gibbons’ body score living in extreme habitat compare to gibbons living in less extreme habitat? I feel this is where people working daily with captive gibbons could contribute their knowledge in gibbon care to field studies and perhaps participate in them.

Primates known as frugivorous species in the wild are often provided a fruit-based diet in captivity. Most cultivated fruits available in the supermarkets are grown for human consumption, and selectively breed and cultivated to appeal to human taste. These fruits are high in sugars, particularly sucrose, low in fiber and are poorer sources of protein and vitamins and minerals than their wild relatives. (Milton 2000). Generally, captive diet doesn’t take into account the seasonal changes in the foods gibbons experience in the wild. The different nutrition, high carbs food, and less time foraging can cause gibbons to become overweight, develop diabetes, heart disease, intestinal problems, etc.

A study on the gastrointestinal microbiota of northern white-cheeked gibbons found that captive gibbons’ microbiotas were colonized by human-associated gut bacterial genera Bacteroides and Prevotella. Captivity may humanize captive primates microbiome. They also found significant differences between the two groups of gibbons living in different captive conditions. The group with a more diverse diet (17 different types of food) had more diverse gut microbiotas compare to the group with a less diverse diet (9 types of food). (Jia, et al. 2018)

More study is needed to understand how gut microbiotas changes in response to specific changes in the diet, and how it can affect the health of gibbons and other primates.

Captive diets should resemble wild diets in terms of nutritional composition. Certain vegetables more closely resemble wild fruits in their nutritional composition than commercially available fruits and are a better choice than some sugary fruit for captive gibbons. (Schwitzer, 2008)

There have been only a few studies on the nutritional composition of wild gibbon diets.

A preliminary analysis suggests that very hard foods are avoided, as are foods high in tannins e.g. seeds. (Cheyne, 2010)

During low fruit periods, gibbons often eat a higher diversity of fruit, probably a strategy to cope with secondary compounds found in lesspreferred fruit sources such as toxins, or digestion inhibitors. When fruit sources are abundant, the gibbons are more likely to able to obtain preferred fruit sources than in times of scarcity. The same true for leaves, gibbons increase their diet diversity when they eat more leaves possibly to cope with toxins or digestion inhibitor accumulation associated with feeding on a limited number of leaf species. (Fan, 2012)

A study on Javan gibbon nutrition revealed the nutrition content of the food items they generally eat. Flowers and ripe fruits contained the most carbohydrate. Young leaves were the highest in water content, ash and crude protein. Crude fiber content was the highest in ripe fruits. They also ate a small amount of unripe fruit, which was highest in fat content compared to other food sources. (Octaviani, 2018)

A group of northern yellow-cheeked gibbon in Cambodia had similar dietary intake, researchers found that ripe fruits were not just the highest in sugar content, they also had more fat than other food items. Young leaves and flowers were highest in protein content. Flowers are also an important source of calcium and phosphorus.

Mature leaves were high in water and low in fiber compare to young leaves and that made them a more valuable item during the dry season. (Hon, et al. 2017)

A third study on Cao Vit gibbons in China also confirmed that fruits and figs are a high-quality food source for gibbons and contain the most sugar. Cao Vit gibbons prefer fruits in early morning and in later afternoon (Ma, et al. 2014). Leaves and buds provided important protein sources for these gibbons as well as minerals. Flowers are important fallback food and they provide high protein and high carbs at the same time. (Fan, 2016)

Studies on wild gibbons’ diet can also benefit captive care. As we gain more information about what gibbons eat in the wild, we can also continue to improve husbandry practices, optimized their diet, provide a more stimulating environment, and more exercise. As we go forward it would be interesting and beneficial to develop a study and a survey on diet of captive gibbons and how it affects their development, group dynamics, general health, sex ratio, and their gastrointestinal microbiota.

“It was a sprawling Ficus that soared over a hundred feet in the air, and high overhead was a family of gibbons moving through the distant branches. Certainly, it was a climactic moment, but even though I felt a burst of exhilaration, it was quickly followed by a sense of alarm. I was shocked by how hard it was to see the animals, which compared to their surroundings looked more like squirrels than apes, and I began to wonder how I was ever going to follow them for a full day, let alone simultaneously collect behavioral data. An even bigger surprise, as I later wrote in my diary, was how difficult it was to see the fruit the gibbons had apparently come to the tree to eat. I suppose I had expected fruit the size of supermarket produces dangling from every branch. Instead, I could barely distinguish the nickel and dime- sized fruit from the branches themselves. This predicament was no small matter because the topic I had come to Khao Yai to study was the feeding behavior of these highly frugivorous primates.” Thad Q. Bartlett, From the Preface of The Gibbons of Khao Yai – Seasonal Variation in Behavior and Ecology

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