Viruses detected on plants chewed by primates

New research has discovered a noninvasive way to test primates for viruses. Collaboration between UC Davis and Gorilla Doctors has shown that the plants mountain gorillas (Gorilla beringei beringei) and golden monkeys (Cercopithecus mitis kandti) consume and discard can be collected and analyzed to determine what viruses the animals have. Blood samples and oral and rectal swabs all require the researcher to anesthetize the animal, something that is not done with critically endangered mountain gorillas unless absolutely necessary.

Thus, this new noninvasive method will allow researchers to detect viruses simply by following the animals at a distance and collecting any bits of chewed bark, leaves, or fruit the individual discards. For this study, Smiley Evans and colleagues (2016) spent almost a year collecting these vegetation discards from 294 gorillas from 26 different family groups across the Volcanoes National Park, Bwindi Impenetrable Forest, and Mgahinga Gorilla Park.

The authors also looked at golden monkeys, collecting plant samples on three different dates in order to determine if their methods could be used on other primate species. Samples were collected from 18 individuals. For both species, researchers observed the animals, collected disregarded plant parts, and sampled from plants with visible bite marks and saliva.

It was possible to collect samples from nearly every individual in a family, including infants who may not consume the plants but still bite and chew them. DNA and RNA viruses were both successfully detected using this method with minimal disruption. Compared to other methods, Smiley Evans and colleagues were able to sample more individuals with less risk and little behavioral disruption. Using this method, the researcher easily knows the age of the sample because close behavioral observation is required.

Golden monkeys proved more challenging than mountain gorillas because they are arboreal and handle food less with their mouths when compared to mountain gorillas. However, it is still possible to collect samples, but researchers should prepare to collect fewer samples per visit.

This research is especially important for mountain gorillas because infectious diseases are one of the greatest threats to this species, and as wildlife increasingly comes into contact with humans, breakthroughs in disease ecology have the potential to positively impact these gentle giants. Roughly 60% of the remaining 880 mountain gorillas are habituated to humans (Gray et al., 2011; Robbins et al., 2011), meaning they encounter humans, whether tourists, researchers, or others, on a regular basis and are accustomed their presence.

Links of possible interest: 

IUCN mountain gorilla page

Gorilla Doctors

Mountain gorilla genome sequenced

Works cited:
Gray, M., Fawcett, K., Basabose, A., et al., (2011). Virunga Massif Mountain Gorilla Census 2010 Summary Report. International Gorilla Conservation Programme.

Robbins, M. M., Roy, J., Kato, R., Kabano, P., Basabose, A., Tibenda, E., ... & Gray, G. (2011). Bwindi Mountain Gorilla Census 2011-Summary of Results. Uganda Wildlife Authority, 28.

Smiley Evans, T., Gilardi, K. V., Barry, P. A., Dsebide, B. J., Kinani, J. F., Nizeyimana, F., ... & Mazet J. A. (2016). Detection of Viruses Using Disregarded Plants from Wild Mountain Gorillas and Golden Monkeys. American Journal of Primatology.

Cercopithecus monkeys opportunistically prey on bats

C. mitis, photo Diana Robinson

Two species of Cercopithecus monkeys in Kenya have been observed and documented feeding on bats when the opportunity presents itself. Tapanes and colleagues (2016) photographed and filmed this behavior in Blue monkeys, Cercopithecus mitis, and in one monkey which was a hybrid species of C. mitis and C. ascanius, the Red-tailed monkey. They report on thirteen observations of bat predation attempts over six and a half years at two sites, Gombe in Tanzania and the Kakamega Forest in Kenya). Of these thirteen attempts, eleven were successful. Surveying researchers of blue and red-tailed monkeys at other sites did not identify further instances of bat predation.

Although identifying the bats was challenging, Tapanes and colleagues determined that multiple species of bats were consumed. Researchers observed two instances where an individual grabbed a lone roosting bat and consumed it. In the other observations, the researchers did not witness the individual capturing the bat.

Unsurprisingly, the evidence suggests that bats are a preferred food item for Cercopithecus monkeys. In two of a successful predation event, other monkeys gathered around and observed the monkey feeding on the bat. Three instances were observed where some sort of aggressive display or behavior to either obtain or retain the bat, implying this food item is worth fighting over.

All observed instances of this behavior occurred in either forest edges or human-modified habitat, raising the question as to whether or not this behavior occurs naturally or is a product of habitat destruction and alteration due to human activities. It is possible that anthropogenic changes to the landscape have resulted in blue and red-tailed monkeys altering their feeding patterns and behaviors accordingly, with increased consumption of bats as a potential modification. Thirty-six years of data collection at Kakamega forest show that bat predation coincides with increased use of plantation forests that has occurred due to forest fragmentation and loss. Tapanes and colleagues (2016) also suggest that bat predation could be more widespread, but it is simply easier for researchers to observe this rare behavior within altered habitats. They do not think this reason is likely, stating that observation conditions were similar in both plantation forest and forest that is more natural.

Blue monkey feeding, photo Christoph Strässler

These findings have important implications for the transmission of zoonotic diseases, or diseases that can be transmitted from animals to humans. It has previously been hypothesized that primates contract diseases from bats when they consume fruit with an infected bat's saliva or feces (Dobson, 2005; Alexander et al., 2015; Rodhain, 2015). This latest study forces us to consider the fact that directly handling the bats themselves may be a method for disease transfer. As monkeys can transmit many diseases to humans, it is worth studying this phenomenon more, if possible.

Links of potential interest:
IUCN Redlist page for C. mitis
Primate zoonotic diseases
Which primate is likely the source of the next pandemic?
Ebola, primates, and bushmeat

Works cited:
Alexander, K. A., Sanderson, C. E., Marathe, M., Lewis, B. L., Rivers, C. M., Shaman, J., ... & Eubank, S. (2015). What factors might have led to the emergence of Ebola in West Africa?. PLoS Negl Trop Dis, 9(6), e0003652.
Dobson, A. P. (2005). What links bats to emerging infectious diseases?. Science, 310(5748), 628-629.
Rodhain, F. (2015). Chauves-souris et virus: des relations complexes. Bulletin de la Société de pathologie exotique, 108(4), 272-289.
Tapanes, E., Detwiler, K. M., & Cords, M. (2016). Bat Predation by Cercopithecus Monkeys: Implications for Zoonotic Disease Transmission. EcoHealth, 1-5.

What effect temporally and spatially complex fruits may have on chimp cognition

Photo credit Sergio Morchon

A recent study by Janmaat and colleagues (2016) details how fruits in chimpanzee habitat are spatially and temporally complex (see that post here). As Janmaat and colleagues stated, this complexity in diet has implications for chimpanzee intelligence.

Fruits are a preferred food. It's worth hunting down these high-energy food items. That said, fruits aren't always easy to find. It's a waste of energy to travel to a specific fruiting tree with the thought of consuming a high-energy meal if that tree isn't producing. Wasting energy wandering around a forest looking for fruits that don't exist definitely isn't adaptive, and it's not something we would expect to see in chimpanzees or in any other species. It's in a chimpanzee's best interest to know where a fruit tree is and whether or not it will be fruiting. This type of processing  takes a certain amount of knowledge and brain power. 

The ecological intelligence hypothesis suggests that primates consuming foods that are fleeting in their availability and scattered geographically would require larger ranges and the cognitive capability to forage optimally for those ephemeral and scattered foods (Milton and May, 1976; Milton, 1980; Milton, 1981; Milton, 1988). Being able to remember where these scattered foods are and when they are available would be advantageous for the primate.

Janmaat and colleagues (2016) found substantial variation between fruiting species in regards to the timing of fruit production, and the authors suggest that chimps would benefit from learning species-specific fruiting patterns to locate these foods. There was also significant variation within a species in the monthly percentage of fruiting trees across years and between forests. Rather than this knowledge being genetic or something all chimpanzees are born with, it is more likely that chimpanzees learn about synchronicity of fruiting.

In regards to remembering trees that produce large amounts of fruit, the authors used existing literature and their own observations of great variation in fruit tree production histories to hypothesize that chimpanzees use their ranging patterns to monitor trees that are likely to produce large crops of fruit. Chimps would need to store information on fruit production histories over many years, particularly for species that fruit every few years rather than every few months, providing further evidence of how chimpanzees use their brains and intelligence to survive in their environment.

The forests chimpanzees inhabit clearly provide challenges for our closest relatives in terms of finding their preferred foods, ripe fruits. However, these intelligent animals have the brain power needed to master this environment and the challenges forests present. Their intelligence not only helps them navigate living in a social group and managing complex relationships but it also allows them to navigate the complex ecology surrounding them.

Links of possible interest:
Chimpanzees and long term memory
NOVA's Ape Genius


Works cited:

Milton, K., & May, M. L. (1976). Body weight, diet and home range area in primates. Nature, 259(5543), 459-462.

Milton, K. (1980). The foraging strategy of howler monkeys: a study in primate economics. Columbia University Press.

Milton, K. (1981). Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development. American Anthropologist, 83(3), 534-548.

Milton K. 1988. Foraging behaviour and the evolution of primate intelligence. In: Byrne RW, Whiten A, editors. Machiavellian intelligence: social expertise and the evolution of intellect in monkeys, apes and humans. Oxford: Clarendon Press. p 285–305.

The spatial and temporal complexity of fruit species consumed by chimps

Chimpanzees live in a variety of environments, thus the types of food they consume vary accordingly. We wouldn't expect a chimpanzee troop living in Fongoli (a savanna) to consume the same foods as chimpanzees living in Gombe (a tropical forest).

That caveat aside, chimpanzees across habitats prefer fruits to other food types. We know this because fruits make up a greater proportion of their diet than would be expected given fruit availability (Hladik, 1977; Tutin et al., 1997; Conklin-Brittain et al., 1998; Wrangham et al., 1998; Doran-Sheehy et al., 2006). Fruits are high in energy and low in secondary compounds, or digestive inhibitors or toxins, such as tannins or lignin. (Remember that the fruits we see in a grocery store or at a food stand have been selectively bred to look and taste considerably different than most wild fruits). Interestingly, chimpanzees in Guinea-Bissau consume mainly wild fruits and flowers even when they are in close proximity to agricultural areas (Carvalho et al., 2015). Thus, it seems safe to conclude that fruits are high up on the desired menu.

Feeding on Ficus sur fruits, Photo credit: Alain Houle

A recent study by Janmaat and colleagues (2016) looked at three populations of chimpanzees in tropical lowland rainforest, lowland tropical moist forest, and a moist evergreen tropical forest to better understand how chimpanzees access energy-rich foods. They considered multiple food types that are high-energy: young leaves, unripe fruit, and ripe fruit. The authors also had a particular interest in large crops of ripe fruit. They described the probability of finding trees for each of the aforementioned, three food types and how predictable ripe fruit production is in each focal tree in regards to timing, frequency, and quantity of ripe fruit produced. 

 The authors found that individuals were more likely to encounter young leaves or unripe fruit than ripe fruit, confirming that fruits present more of a challenge than other food types. However, over half of all of the trees chimpanzees encountered over the course of this study were species of fruiting trees consumed by chimps. Thus, finding a tree species known to produce an edible fruit isn't a monumental challenge for these populations. The challenge lies in timing.  

There was considerable variation in the timing of fruit production within a population of a tree species. Within the same species, the length of fruit production varied: one individual may produce fruit for a few months over multiple years whereas another individual may fruit for many more months within the same period. There was also monthly variation in the size of fruit crops produced. Further variation within a species complicates matters for chimps even more, as they can't count on large crops of fruits in certain months, even within individual species.

Look for an upcoming post on the implications of finding ripe fruits in a complex environment. How might the ecology of chimpanzee habitat and their dietary choices affect their intelligence?

Links of potential interest:
Chimps understand and choose to cook
Female chimpanzees more likely to use tools when hunting than males
 

Works cited:

Carvalho, J. S., Vicente, L., & Marques, T. A. (2015). Chimpanzee (Pan troglodytes verus) Diet Composition and Food Availability in a Human-Modified Landscape at Lagoas de Cufada Natural Park, Guinea-Bissau. International Journal of Primatology, 36(4), 802-822. 

Conklin-Brittain, N. L., Wrangham, R. W., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. II. Macronutrients. International Journal of Primatology, 19(6), 971-998.

Doran-Sheehy, D. M., Shah, N. F., & Heimbauer, L. A. (2006). Sympatric western gorilla and mangabey diet: re-examination of ape and monkey foraging strategies. Cambridge Studies in Biological and Evolutionary Anthropology, 48, 49.

Hladik, C. M. (1977). Chimpanzees of Gabon and chimpanzees of Gombe: some comparative data on the diet. Primate Ecology: Studies of Feeding and Ranging behaviour in Lemurs, Monkeys, and Apes, 81-501.

Janmaat, K. R., Boesch, C., Byrne, R., Chapman, C. A., Bi, G., Zoro, B., ... & Polansky, L. (2016). Spatio‐temporal complexity of chimpanzee food: How cognitive adaptations can counteract the ephemeral nature of ripe fruit. American Journal of Primatology.

Tutin, C. E., Ham, R. M., White, L. J., & Harrison, M. J. (1997). The primate community of the Lopé Reserve, Gabon: diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology, 42(1), 1-24.

Wrangham, R. W., Conklin-Brittain, N. L., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. International Journal of Primatology, 19(6), 949-970.