1 Introduction

Zoo animal nutrition is an important topic that originated from domestic animal nutrition [1, 2]. Food presentation and preparation are two aspects of the nutrition of zoo animals that have recently gained research interest, and these factors can induce behavioural change in animals [3,4,5,6,7]. Animals have the chance to better thrive within captivity if they can consume a natural array of nutrients [8] being presented naturally [9]. After all, providing welfare and wellbeing are accepted aims of the modern-day zoo [10,11,12], and promoting good welfare can aid the reproductive success of endangered animals and the ex-situ conservation output of zoos [9].

1.1 Why study food presentation in zoos?

Wild animals do not have access to chopped food, and yet chopping is popular in zoos [13,14,15]. So why chop? Anecdotally, it is suggested that animals gain benefit by having access to more food variety during chopped food condition [7] and there may be reduced food aggression because of this [4]. However, many papers suggest that whole foods are more beneficial for animals, and actually reduce aggression [6], increase the variety of feeding behaviours such as food manipulation [14], increase feeding times [16], and result in less food desiccation [17] and bacterial contamination, and a decrease in keeper preparation time [5].

1.2 Chopping food slashes nutritional quality

The nutritional quality of food changes once chopped. In fruits and vegetables, the respiration rate (production of carbon dioxide) increases after cutting or damaging [18], which correlates to a reduction in weight, in the form of water, and therefore a loss of soluble nutrients [19]. This is supported by Hodges and Toivonen [20] who also state that the browning of cut or damaged fruits increases ethylene production. These factors can also affect the palatability of food items, with changes in sweetness and texture [18, 20] impacting how an item tastes. Ethylene, for example, is a key compound in the ripening of fruits and is present in high concentrations when the fruit is overripe or damaged [21,22,23], suggesting that when fruits are chopped, the process of desiccation is accelerated and the time available to store these items is therefore limited. Within the zoo environment, this may not be the most practical way to prepare animal diets. Fridges can aid in the preservation of foodstuffs [19] courtesy of protection from negative environmental effects such as temperature [14] and humidity [23]. Chopped fruits also showcase higher sugar content courtesy of the breakdown of starches, altering the nutritional content of the food item [3].

Aside from the nutritional effects chopping food may have, there is also a risk of contamination from the utensils used during preparation [24]. Blunt utensils can increase the rate of desiccation, with greater damage to the cell walls of the food item, equalling higher water and nutrient loss [3, 19]. It is also worth noting that various food presentation techniques within zoos, such as scattering feed into outside areas [25], can also increase the chances of microbial contamination, with particular concern attributing itself to smaller chopped pieces, courtesy of having a larger surface area [3, 14].

Finally, chopping food can also have an impact on keeper times. James et al. [14] found a significant increase in time taken to prepare chopped food diets, with keepers spending 91% more time on chopped diets versus whole diets. Therefore, the provision of whole food diets may allow keepers to re-allocate their time into other activities. Overall, there are some potentially negative effects to chopping food, such as desiccation, microbial contamination, and long preparation times, however, the factors which affect these may be mitigated by utilising appropriate storage facilities, better preparation methods, or avoiding certain environmental conditions.

1.3 Food presentation affects behaviour, too

Primates appear frequently in the food presentation literature [6], likely as a result of frugivorous diets [26]. These primate studies have shown varying results. research identified that whole food diets resulted in less aggression, more sociality, and natural behaviours in a group of Barbary macaques (Macaca sylvanus [15]), while Plowman et al. [5] found no reasons to suggest whole food would increase aggression in a study with Sulawesi crested macaques (Macaca nigra) and tapirs (Tapirus terrestris). Holistically, it appears that whole food often decreases aggression, as subordinate individuals have time to move away from their conspecifics to process the larger items rather than compete over an immobile food resource [6]. Similarly, Welsh et al. [16] found a significant increase in ‘carrying’ behaviour in ring-tailed lemurs (Lemur catta) during whole food presentation. An alternative study showed that aggression reduced by 38% in a group of Rhesus macaques (Macaca mulatta) when the group were given larger items that required more manipulation, such as whole corn husks and celery [27]. Ultimately, whole food is a natural form of food presentation, [9] and the movement of animals away from a shared food area carrying a large food item appears to reduce aggression, as the animals are no longer in the same location whilst eating.

Other primate studies have shown conflicting results, with both Mathy and Isbell [4] and Waasdorp et al. [7] finding that aggression increased in Rhesus macaques and white-naped mangabeys (Cercocebus lunulatus), respectively, when provided whole foods. Both studies focused on large groups of primates, with Mathy and Isbell [4] providing a limited number of food items to a large group of macaques. This method potentially increased aggression due to the large number of animals competing for them. The study by Waasdorp et al. [7] did not state how much food was provided, and some questions could be raised by the placement of feeding sites, with no consideration of biological relevance of the feeding areas due to the proximity to visitors, who have been shown to affect animal behaviour [28, 29]. Deeper investigations into food particle size effects should be considered, especially considering the impact of scatter feeding and the use of chopped food in enrichment items. There is a need for more studies that investigate food presentation effects for singly-housed, group-housed and pair-housed animals, as this is likely to affect how animals respond to food presentation. There appears to be limited information on the effects of food presentation on single-housed animals, and studies instead tend to focus on pairs and especially groups of animals. Future studies should investigate how food presentation differentially affects the behaviour of pairs or groups so as to gain a clearer understanding of potential impacts.

Other taxa are beginning to be represented within food presentation literature, with a blue and gold macaw (Ara ararauna) study by James et al. [14] finding significantly more activity, more podomanipulation, and allofeeding when whole food was given. Rozek et al. [30] found that orange-winged Amazon parrots (Amazona amazonica) preferred larger pellets through choice-preference trials and spent significantly longer gnawing when providing with oversized pellets, showing that natural presentation styles can potentially provide enrichment opportunities.

The order Carnivora have been recently represented in food presentation studies with a study on ring-tailed coatis (Nasua nasua), which also found a decrease in aggression and an increase in food manipulation behaviours during whole food provision [6]. Aside from the herbivorous portion of some carnivore diets, it has also been advised that carnivores are fed whole prey (in the form of carcasses) as it can be a more cognitively stimulating and natural method of feeding [9], allowing a wider range of feeding behaviours and potentially improving dental health [31]. The use of carcasses also has benefits in terms of group dynamics and social behaviours, for carnivores that naturally hunt and feed in a group, such as lions (Panthera leo) by resolving social discrepancies and therefore reducing aggression [31]. This is because the animals must convene over the carcass and therefore can establish an order of feeding; the establishment of relationships during these events can reduce future conflicts.. While mammals are traditionally well represented in zoos [32, 33], with an apparent research bias towards them [34], there is room for further food presentation research within this group. Not all carnivorans feature frequently in field of food presentation, and viverrids appear to feature especially rarely [35, 36].

The binturong (Arctictis binturong) is the largest member of the civet family [36,37,38,39,40]. This species is native across southeast Asia and southern China [38, 40]. Binturongs are predominantly arboreal [39], and they inhabit areas of primary and secondary lowland forests, and forest/grassland mosaics [40]. With a 30% decline of their original population [41], the binturong is Vulnerable on the International Union for Conservation of Nature (IUCN) red list [36, 41]. Plantations are particularly troublesome, as while binturongs show some tolerance to degraded forest [40], plantations provide few natural food sources; binturongs display almost complete frugivory in the wild [36, 42]. Within their diet, they show a strong dependency on trees in the Ficus genus, using the fruits, figs, as their main food source [36]. Nakabayashi and Ahamad [39] found that fig trees made up 87.5% of feeding sites for binturongs, across 13 species of fig. This dependence suggests that binturongs are important seed-dispersing ecosystem engineers [36, 41], highlighting their conservation concern. Their ability as seed dispersers is partly down to their physiology, with short gastrointestinal tracts [43] leading to inefficient digestion of plant material [38, 39]. The binturong dental structure is typically carnivore, with large canines and carnassial teeth adapted for shearing meat [44, 45], leading to the assumption that food items are poorly processed before being swallowed [37]. The rest of their diet is predominantly protein-based, with carrion, fish, and birds often consumed [41]. Binturongs are usually solitary in the wild, and are apparently not territorial, with other territories overlapping by around 35% in some cases [37]. Despite being a potential conservation priority for zoos worldwide [46, 47], binturongs are seemingly understudied [38], leaving a large niche for scientific study. Their lifestyle is quite unknown, with some sources stating they are diurnal, crepuscular, nocturnal, or cathemeral [39,40,41, 48, 49]. Therefore, ex-situ zoo research can provide an invaluable source of information that can hopefully contribute to a better understanding of this species.

1.4 Zoo food presentation: the bintu-wrong way

Studying how different stimuli in an animal’s environment affects them, and which they prefer, is valuable information for an animal collection [50]. Food preference research allows keepers to implement diet changes more successfully by knowing what their animals prefer [51]. Alternatively, it provides opportunities for investigate feeding ecology, and selective feeding [52]. For binturongs, this is important, as most captive diets incorporate lower portions of fruit, and higher portions of starchy vegetables compared to their natural diet (A. Bourgeois, personal communication, February 16, 2024).

Interestingly, the whole food debate may turn up some interesting results with binturongs, due to their main natural food source being figs. While the nutritional and microbial effects of chopping food will still apply, it will be interesting to assess if binturongs show behavioural differences with larger whole food items and whether those differences will apply to wild individuals. Ultimately, adding food presentation research in a feliform carnivoran to current literature can help fill in the knowledge gap in this area, as well as kick starting further research of binturongs in captive environments. The aim of this study was therefore to investigate the impact of food particle size on binturong behaviour and overall food preference, whilst also investigating keeper time required to prepare diets.

2 Methods

2.1 Study subjects and location

This study was conducted using two (1.1) binturongs (Table 1, [53]) housed at Beale Wildlife Park, Pangbourne, United Kingdom, with observations lasting from June to November 2023. Overall, 60 h of behavioural data were collected per individual, totalling 120 h by the end of the study. This project was granted ethical approval from University Centre Sparsholt ethics committee. Behavioural data were collected by one student researcher, with keeper time data collected with the assistance of a keeper from Beale Park.

Table 1 Study subjects
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The two binturongs were housed together in an open-topped, grassy enclosure (239.26 m2), both with constant access to a heated indoor area (25.22 m2). The outdoor area contained a series of platforms at approximately 1.5 m height, which were connected with firehose and branches, allowing the animals to climb. Several small shrubs were also available within the exhibit. The indoor exhibit consisted of a large, heated room, with wooden ledges for sitting and straw-filled beds, with sawdust as a substrate for the floor. The layout of the enclosure provided no ‘off-show’ area, with all indoor and outdoor areas visible. On busier days, a binturong keeper talk would be held at 1500 h by the enclosure, with occasional visitor experiences also taking place around the middle of the day. Prior to the study, multiple keepers were responsible for the husbandry of the animals, although they were not present in equal numbers. Husbandry was completed between 0800 and 0900 h, with two feeds, am and pm, being scattered on raised platforms in the enclosure at 0900 h and 1600 h every day. For normal husbandry, the diets consisted of both chopped and whole fruits and vegetables to a weight of 1200 g for both the animals (600 g each). Prior to this study, whole food items were occasionally given as dietary enrichment. A meat portion of their diet, a choice between omnivore pellet, chicken eggs, quail, or chicks, was given whole with their afternoon feed.

2.2 Food presentation

The specific food items fed at any given meal differed on a daily basis, as per the diet sheet of Beale Wildlife Park. As a result, the specific food items fed during each observation differed: the food items offered can be seen in Appendix Table 5. While additional information on specific food preferences was collected, the main focus of this study was on the effect of food size. The food was presented in three sizes (hereafter referred to as “food size”): whole, chopped, and very chopped. Very chopped food was cut into 1 cm3 pieces, while chopped food was cut into 4 cm3 pieces. Whole food items were left whole (or if exceptionally large, such as a melon, they were halved. While there was therefore some variance in the size of individual whole food items, they were larger than the chopped foods. Food was provided at three feeding times: 0900 h, 1200 h, and 1500 h, and food size was varied using a Latin square design, so that all food sizes were represented equally during all feeding times by the end of the study [54]. Food was weighed and split evenly between feeds and scattered around the enclosure, on raised platforms as per normal husbandry.

Aside from the diet, food preparation time was also measured in minutes and seconds. This process was completed by one Beale Park keeper to ensure reliability, and only involved the time taken to cut, weigh, and place the diet into a suitable dish. Post-feeding, diet remains were collected and re-weighed to establish how much had been consumed. Weather conditions were also recorded for each feeding session through World Weather Online [55], namely the temperature, current weather, and humidity, date and time.

To record results, an ethogram was developed for binturongs (Table 2). Binturong state behaviours (long-duration behaviours) were observed using instantaneous focal sampling at 1-min intervals for one-hour sessions starting with each scheduled feed. Event behaviours (short duration behaviours) were recorded using continuous focal sampling [54]. Food preferences were also recorded during observations, with the first three items of food consumed per binturong also being recorded, and later compiled into a table showing the times the food item was chosen versus the number of times it appeared in the diet. A pilot study was conducted a week before the study to develop the ethogram and test study methodology. One observer (AJV) conducted all behavioural observations, following ethogram development and behavioural observation training.

Table 2 Binturong ethogram
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2.3 Data analysis

Data were compiled into an Excel™ 2016 spreadsheet and were analysed using Minitab version 21.1. For the keeper preparation times, data were analysed using a Kruskal–Wallis test, with Mann Whitney post hoc tests. Behavioural data were analysed using a series of general linear mixed effects models (GLMM), with a Poisson distribution applied. State behavioural data were converted into percentages for analysis, whereas event behaviours were treated as a rate per individual per hour. For these tests, the response was set as the behaviour, with food size and individual set as fixed factors, and date and temperature inputted as random factors.

3 Results

3.1 State behaviour

Food size was a predictor of behaviour change for only one state behaviour: feeding, which occurred for significantly longer periods when very chopped food was provided (T(3) = 12.59, P < 0.001) (Fig. 1; Table 3). There was a much greater number of differences between the two individuals, with significantly more resting (T(3) = 6.937, P < 0.001), grooming (T(3) = − 0.246, P = 0.015) and less locomotion (T(3) = 2.64, P = 0.008) and stationary behaviour (T(3) = 2.172, P = 0.033) identified for the male.

Fig. 1
figure 1

Activity budget for binturong when provided with whole, chopped, or very chopped food, mean ± standard deviation. a Activity budget for Rosie and b Ted. * indicates P > 0.05, ** indicates P < 0.01, *** indicates P < 0.001

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Table 3 Outputs of GLMMs on the effect of food size (whole, chopped or very chopped) and individual on behaviour
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3.2 Event behaviour

For event behaviours, the whole food significantly increased levels of food manipulation (T(3) = 8.63, P < 0.001), locomotion with food (T(3) = 0.458, P < 0.001) and reduced vocalisations (T(3) = 2.126, P = 0.023) (Table 4; Fig. 2), but not the other behaviours. Individual was a predictor of dropping, grabbing and scent marking, with scent marking (T(3) = − 2/579, P = 0.011) occurring significantly more often and grabbing (T(3) = 2.263, P = 0.027) and dropping (T(3) = 2.132, P = 0.036) occurring significantly less often for the male.

Table 4 Outputs of GLMMs on the effect of food size (whole, chopped or very chopped) and individual for event behaviours
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Fig. 2
figure 2

Event behaviour graph for binturong when provided with whole, chopped, or very chopped food, mean ± standard deviation. a Graph for Rosie and b Ted. * indicates P > 0.05, ** indicates P < 0.01, *** indicates P < 0.001

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3.3 Keeper preparation time

The number of seconds taken to prepare food by keepers was assessed for all three conditions: the time taken to prepare whole, chopped and very chopped food was 42, 146 and 293 s, respectively. On average, over 251 s of time was saved when whole food was prepared in comparison to very chopped feeds (Fig. 3). There was a statistically significant difference between the three conditions (H(2) = 88.23, P < 0.001). Post hoc analysis revealed a significant difference between the chopped and whole (W(40) = 2320, P < 0.001), chopped and very chopped (W(40) = 1036, P < 0.001) and very chopped and whole conditions (W(40) = 820, P < 0.001).

Fig. 3
figure 3

Average amount of time taken to prepare diets for binturong for the whole, chopped and very chopped condition mean (± standard deviation). * indicates P > 0.05, ** indicates P < 0.01, *** indicates P < 0.001

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3.4 Food preference

Data collected on food preference were organised into a table (see Appendix) for visual representation, showing the number of times a food item was eaten either first, second, or third, and how often it was present in the diet. It should be noted that only chopped food data were used. Fruits (bar beetroot once) were picked first and second over 50% of the time in both animals.

4 Discussion

Overall, only the state behaviour of feeding was decreased when whole foods were provided. Most significant findings were instead a result of individual differences or the recorded extraneous variables (temperature and date). In event behaviours, however, both food manipulation and locomotion with food showcased significant differences between whole food and very chopped foods. Vocalisation was also significantly different between whole versus very chopped condition and chopped versus very chopped condition. Considerable time was saved during whole food condition keeper preparation too. Given the keeper input and nutritional damage caused by chopping, whole food may be a viable strategy for feeding binturong.

4.1 State behaviour

State behaviours were minimally affected, although the time spent feeding was significantly different between whole and very chopped condition (P = 0.011), with feeding time increasing the smaller the food was chopped. There were small differences in resting behaviour, with both binturongs resting the most during chopped food and resting the least during very chopped food (Figs. 2 and 3), although overall the behaviours in the activity budgets remained similar between the different food conditions, suggesting that they were minimally affected by the different food presentation. Autogrooming, feeding, foraging, resting, and stationary behaviours were significantly affected by other recorded variables such as date and temperature.

Finding longer feeding times during very chopped condition seemingly contradicts previous findings of longer feeding times during whole condition [5], however, this finding has been supported by previous research showing that Barbary macaques spent longer picking out particular parts of a chopped food diet, taking longer to consume items during feeding times [56]. It appears this argument is valid for binturongs, as during observations, they would often knock smaller pieces of food off the feeding areas into long grass, leading to longer consumption times. It may also be possible that the studies definition of ‘foraging’ behaviour was underutilised, due to poor visibility once the food items had fallen. It is also plausible that the results show only half of the story; often during whole food, the binturongs would locomote into an obscured tunnel with a large food item, preventing any visibility on feeding behaviour, eventually leading to a misrepresentation of how much feeding was observed.

Resting behaviour was one of the most frequently recorded behaviours, occupying 30–50% of the activity budget in both binturongs. In recorded literature, there is no definitive evidence of the activity patterns of binturongs [40], although a study conducted by Finch et al. [57] found a crepuscular activity pattern in zoo housed binturongs. However, it should be noted that captive binturong are normally fed during the daytime, and so are likely to be active during normal feeding times [46]. Further studies should aim to establish whether the time of day can influence binturong activity patterns or if other variables contributed to these differences, such as weather condition or visitor numbers.

4.2 Event behaviours

Whole food presentation significantly increased food manipulation, locomotion with food, and vocalisation behaviours during this study. Akin to the other studies, in particular the fellow carnivore study on ring-tailed coatis [6], food manipulation increased the larger the food item [14, 36, 58]. Food items were often transported to a different location, particularly if another binturong was close by, where they would then hold the food item using the front paws, and pull it apart with the mouth until a suitably sized item was eaten. Food manipulation can be enriching for zoo animals; Clark et al. [59] investigated this by recording whether ring-tailed lemurs used both hands during enrichment testing. Using two hands meant that the lemur’s posture was compromised compared to normal, with the idea being that if it was uncomfortable, the lemurs would not engage with the enrichment. The binturongs naturally stand on all four legs, however, whole food encouraged them to stand on their hind legs, or even hang from ledges using their prehensile tail [42, 60, 61] to manipulate their food items, potentially showing a motivation to manipulate.

Ironically, the size of the whole food provided in this study may not be akin to their natural diet. Nakabayashi and Ahmad [38] compiled a table of known food sources of radio-tagged wild binturongs and found that the largest food item was Glenniea philippinensis, with an average diameter of 84 mm. This itself was an outlier, with most figs (such as Ficus annulata and Ficus binnendijkii) being around 25 mm in diameter [39]. This is closer to the size of the chopped food in this study than it is to the whole, suggesting manipulation behaviour is perhaps not as present in the wild. While presenting food in the most natural way has been considered as best practice within zoos [9], finding ways which can help cognitively engage animals in captivity, even if unnatural, should not be ignored, and with the binturongs not being deterred by larger, harder to eat items, this is quite possibly an example of this. It is also worth noting that binturong dentition is poorly equipped to tackle large food items that require a lot of mastication, and it has been observed that they often swallow food items whole and relatively unprocessed [37]. This goes some way to explaining why there were significantly less manipulation behaviours with smaller food items.

Locomotion with food occurred more with whole foods [16]. In rodents these foods are cached for later consumption [58] and in coatis, individuals moved away from other conspecifics, potentially to prevent aggression [6]. In binturongs, there seems to be much the same trend, with the binturong locomoting with food significantly more frequently when food items were whole (P < 0.001). There was an overall trend showing the bigger the food, the more counts of locomotion with food. In nature, binturongs have large home ranges, ranging from 1.54 to 6.9 km2 [49, 62], that can overlap by 35% [37] which is something that cannot be replicated in captivity. This shows that some interaction between individuals can be expected, and there can be a level of tolerance for conspecifics sharing feeding areas. There have been anecdotal reports supporting this, stating that multiple binturongs have shared the same fruiting tree (L. Bodnar, personal communication, February 16, 2024). Because food availability is temporally limited compared to the wild, with the presence of fruiting trees present in the wild [36,37,38,39,40], it is understandable that locomotion with food takes place to protect high value items from competition [6].

However, while it could then be predicted that there might be more aggression during whole food condition because of the limited space in captivity, this was not the case. There were no food presentation-related significant differences in most aggressive behaviours (biting, grabbing, and lunging) nor any trends suggesting one food condition promoted any one of those behaviours more. There was, however, a significant increase in vocalisations between very chopped, whole, and chopped conditions. Vocalisation in binturongs is hard to define, as under observation it only seemed to happen as a result of interaction between both animals. For this study, it was perceived as an aggressive behaviour, as if any of the other three aggressive behaviours happened, it was preceded and then accompanied by bouts of vocalisation. Peters [63] classed binturong vocalisation as ‘geckering’, differing it from purring which is also found within the family Viverridae, with Abra [64] noting ‘non-aggressive’ vocalisations between binturongs during a breeding attempt; unfortunately there was no definition of the difference in vocalisations. If it is aggression-related, there is a case to suggest very chopped food can create more competition for food, maybe due to the pressure of finding high value items, and therefore more aggression.

4.3 Keeper time effects

Considerable time was saved when preparing whole food diets versus preparing chopped, or very chopped diets (P < 0.001). Saving keeper time is important, with Fidgett and Gardner [26] noting that other diet-related tasks, such as performing a food intake study, are time consuming. Being able to perform research tasks instead of ‘wasting’ time chopping up diets may be beneficial to staff wellbeing, with further learning and experience with their animals becoming more accessible, therefore aiding in their professional development [65, 66]. It can also add aspects of ethology and evidence-based husbandry to a daily routine [65], furthering the advancements of animal welfare and zookeeping in general. At Beale in particular, there was around five minutes saved between whole and very chopped preparations, and that is just considering binturong diets. Beale also have meerkats (Suricatta suricata), Brazilian cavies (Cavia aperea), and rock hyrax (Procavia capensis) which also have a produce portion of their diet. Cumulatively, at five minutes prep apiece, around 35 min of time is used on chopping food a week for a single species, resulting in roughly 30 h of chopping food per year per animal.

4.4 Future directions

Many taxonomic groups display active behaviours such as locomotion with food when given whole food items [14]. Davison et al. [58] and Shora et al. [6] found this in Azara’s agoutis (Dasyprocta azarae) and ring-tailed coatis, respectively. However, this may be worth researching further to explore how far back, evolutionarily speaking, this trend goes, with studies on more birds, reptiles, and amphibians needed to establish whether it is a hard-wired evolutionary behaviour in times of food scarcity or periods of more intense competition.

Fruit items are seemingly preferred in binturong, although future studies could establish if binturongs show a true preference for fruit or if they selectively choose their food items. Food preference can also help inform binturong welfare; Allam et al. [36] analysed binturong scats across Palawan, almost exclusively finding fruit material, bar one invertebrate in the family Coleoptera, suggesting it is more natural to feed binturongs this way in captivity, and it is perhaps the responsibility of keepers to alter binturong diets accordingly. However, the nutritional content of fruit in captivity is vastly different, with much higher carbohydrate content in the form of sugars, and lower fibre, which can lead to dental and physical health issues such as obesity and tooth decay [67,68,69]. Studies have found that fruit-free diets in primates are more beneficial, finding reduced abnormal behaviours [70] and more consistent faeces [69]. With these findings, it is understandable that animals previously fed a lot of fruit may have portions of their diet altered to accommodate more fibrous vegetables to keep calorie content lower and dietary fibre levels higher. However, in binturongs, their gastrointestinal tract is short as is in most carnivores [42], and their gut microbiome is far less specialised to breaking down fibrous and starchy foods compared to other animals with high fibre diets, such as western lowland gorillas (Gorilla gorilla gorilla, [43]). Combined with the fact they poorly masticate their food [41, 42] it may be worth studying the effects of fruit-based diets, similar to their natural ecology [71], and assessing if it is a more enriching or preferred diet. Behaviourally, it would be interesting to assess if presenting fruit-based diets change any aspect of their activity budget.

It must be mentioned that this study investigated only two individuals, one from each sex. Given this small sample size, the results cannot be extrapolated to all binturongs. Further studies using multiple zoo collections and a greater sample size could increase the generalisability of these findings. Future studies should also include the coding of a subset of behavioural observations by a second observer to assess reliability.

5 Conclusion

Food presentation minimally affected binturong behaviour, although locomotion with food and food manipulation both significantly increased during whole food. These behaviours could be considered more enriching and cognitive for the animals; therefore it may be worthwhile to offer whole food to captive binturongs. Whole food reduces preparation keeper time and reduces desiccation and microbial contamination risk. However, due to the frugivory in binturongs, any fruit-based diets must be evaluated on a regular basis to prevent any negative physiological or behavioural effects in these animals, such as obesity. There is scope for further studies on food presentation to establish if certain trends (locomotion with food and food manipulation) exist across Mammalia, and to assess whether whole foods will be beneficial to binturongs in captivity over a longer period of time, across many individuals and zoos.