Living for the City: Interview with Dr. Iván Soto-Calderón
Staff Writer, Luke Fannin
My fellow research assistants from this past summer will undoubtedly agree with me when I say that tamarins are incredibly flexible when it comes to their daily habits in the Amazon rainforest. Not only do they eat a wide variety of food items (including the occasional non-native banana or two), but they also have the fantastic ability to traverse the jungle landscape with ease, regardless of the often-obstructive vegetation in their paths. The same cannot be said for their fellow bipedal primates who follow on the ground. This ability to thrive in a diversity of landscapes- a term that has earned them the moniker of “generalist” has assuredly proven beneficial for these monkeys as the 21st century progresses. The study of ethnoprimatology has emerged as humans and non-human primates have begun to interact more frequently and to a greater extent; much of the research on urban living in primates has been done with macaques, a group of monkeys that has found great success in the transformed landscapes of Asia and frequently interacts with humans (see here for a great article on the health effects of tourist provisioning in Barbary macaques, and here for the behavior of Asian macaques and associations with humans). Many researchers have documented the survival of tamarin populations within urban city forest fragments that have replaced the natural jungle environment that these animals usually reside it. Although many of their other New World monkey relatives may be hard hit by the effects of habitat loss, for the tamarin, their dietary and locomotive versatility may give them an edge in these transformed landscapes – at least for the time being.
But, as any city dweller will probably agree, a city lifestyle certainly has the potential to leave its mark on the health of an individual. Do tamarins then display adverse health effects when they live in cities? A recent publication in the American Journal of Primatology by Iván Soto-Calderón and colleagues from the Universidad de Antioquia examined bodily, hematological, and parasitological evidence of how an urban environment may affect the health of free-ranging white-footed tamarins (Saguinus leucopus). This Columbian-native and endangered species was studied in the city of Medellín, as well as in four rural localities. Individuals were trapped and sedated, and the researchers collected body measurements, blood samples, and fecal samples. Samples were used to evaluate blood chemistry and parasite load (for both blood and intestinal parasites) for each animal. These data, along with measures of physical condition, were used to make comparisons of the health between tamarins living in the city of Medellín and those in more rural environments. Although behavioral follows were not done in this published study, Dr. Soto-Calderón commented that, from a behavioral standpoint, urban tamarins are very much more habituated to humans, but it seems that city-living has not really altered their normal behavioral routine: “The most obvious difference is responsiveness to humans. Whereas rural tamarins are quite elusive, urban tamarins are relatively well habituated to humans…We have actually taken advantage of this to do guided watching of these primates in urban environments.”
Regarding general health, while most of the urban white-footed tamarins were considered to be in “optimum” body condition, it was found that body mass and body mass indices (BMI) were higher in urban tamarins than their rural counterparts. Urban tamarins also had higher levels of cholesterol in their blood. Additionally, urban living tamarins in Medellín had consistent access to high caloric food from fruiting trees, supplemented by the availability of processed human foods with high levels of carbohydrates and fat. These food sources, coupled with low levels of activity due to the ability to find ready food sources with minimal travel time, have most likely resulted in a caloric surplus for these tamarins, leading to the declines in overall bodily health as described above. In order to actually follow these tamarins to see what they were eating, Soto-Calderón used radio-telemetry devices on one urban tamarin and followed its group for a year. “We also identified food items and time invested in their consumption,” reported Soto-Calderón. “Preliminary analyses show that 15% of their diets to correspond to human sources (banana, processed sugar, and flour items) and 85% to natural sources (leaves, fruit pulp, flowers and animal protein from invertebrates or small lizards. This agrees with previous reports for urban tamarins, whose diet is mostly based on plant sources, followed by a small fraction on animal sources. This is in the process of publication but we are already using this info in a no-feed campaign and educational activities that aim a reduction of human food in the tamarin diet.”
Concerning parasite loads and diversity, the authors report that of the ten types of parasites found in all white-footed tamarins studied, all were found in the rural dwelling tamarins, including Trypanosoma (a blood parasite) and 9 types of gastrointestinal parasites (Prosthenorchis, Strongyloides, and several others). In contrast, only two of the aforementioned parasites were found in the urban tamarins, Trypanosoma and Strongyloides. Rural tamarin populations also had a higher percentage of individuals actually infected with a parasite, as well as a higher number of unique parasite infections per individual. Although infected with a more substantial number of parasite species, the authors do note that the health of rural tamarins does not seem to be adversely affected by some of the parasites they carry, when compared to those individuals who possess the same parasite infections in a captive setting.
“When we say “captive animals” we generally mean smuggled wild animals,” reports Soto-Calderón in our interview. “In other words, both captive and wild animals have probably been exposed to parasites, including Prosthenorchis, in rural environments but their immune systems tend to decay once they are moved to captivity, which is thought to be associated to stress and nutritional imbalance.” So it seems that it may be the stress of captivity and a lack of a proper diet that causes these white-footed tamarins to potentially succumb to their parasite infections, not necessarily just having a parasite infection in the first place.
The authors point out that the fewer number of parasites in these urban dwellers can be attributed to several environmental causes, including habitat fragmentation preventing parasite spread, a lack of other potential mammalian parasite reservoirs, or a lack of secondary hosts for those parasites to undergo parts of their life cycles. However, the more significant diversity of parasite species in the rural white-footed tamarins may not necessarily be an adverse health risk, as pointed out by the undetected health effects of some parasite infections in these individuals. Maybe rural and urban white-footed tamarins are not as stressed induced or as nutritionally balanced as their captive counterparts and are therefore are not as pre-disposed to health risks from an infection.
Overall, the study provides a sobering report of some of the adverse effects that city living can have on even the most adaptable and flexible primates. As habitat destruction and human population growth continue to bring non-human primates into closer and more frequent contact with humans, understanding the health consequences of urbanization on primates may be beneficial to the development of meaningful conservation plans that attempt to minimize these effects. This is particularly relevant to critically endangered species, such as the white-footed tamarin. Additionally, this study highlights the importance of parasites in the evaluation of the health of an organism and its ecology, as parasite loads and composition can be beneficial in evaluating critical aspects of a species’ lifestyle, as well as its vulnerability to decline if their dynamics change.
- Soto‐Calderón, I. D., Acevedo‐Garcés, Y. A., Álvarez‐Cardona, J., Hernández‐Castro, C., & García‐Montoya, G. M. (2016). Physiological and parasitological implications of living in a city: the case of the white‐footed tamarin (Saguinus leucopus). American Journal of Primatology, 78(12), 1272-1281. http://onlinelibrary.wiley.com/doi/10.1002/ajp.22581/full
- Gordo, M., Calleia, F. O., Vasconcelos, S. A., Leite, J. J., & Ferrari, S. F. (2013). The challenges of survival in a concrete jungle: conservation of the pied tamarin (Saguinus bicolor) in the urban landscape of Manaus, Brazil. In Primates in Fragments(pp. 357-370). Springer New York. https://link.springer.com/chapter/10.1007/978-1-4614-8839-2_23
- Ashby, B., & King, K. C. (2017). Friendly foes: The evolution of host protection by a parasite. Evolution Letters, 1(4), 211-221. http://onlinelibrary.wiley.com/doi/10.1002/evl3.19/full
- Marcogliese, D. J., & Cone, D. K. (1997). Food webs: a plea for parasites. Trends in Ecology & Evolution, 12(8), 320-325. http://www.sciencedirect.com/science/article/pii/S016953479701080X
- Fuentes, A. (2006). Human culture and monkey behavior: assessing the contexts of potential pathogen transmission between macaques and humans. American Journal of Primatology, 68(9), 880-896. http://onlinelibrary.wiley.com/doi/10.1002/ajp.20295/full
- Maréchal, L., Semple, S., Majolo, B., &MacLarnon, A. (2016) Assessing the effects of tourist provisioning on the health of wild barbary macaques . PLoS ONE, 11(5), online. http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0155920