Changes in Activity Patterns and Intergroup Relationships After a Significant Mortality Event in Commensal Long- Tailed Macaques (Macaca Fascicularis) in Bali, Indonesia
Brotcorne, Fany; Fuentes, Agustin; Wandia, I Nengahet al.
2015 • In International Journal of Primatology, 36 (3), p. 548–566
Anthropogenic habitat; Bali Monkey Forest; Behavioral impact; Intergroup relationship; Significant mortality; Social dynamics
Abstract :
[en] Little is known regarding behavioral and social responses of free-ranging primates to demographic changes emerging from significant mortality events. Here, we report on the activity patterns and intergroup sociospatial relationships in a commensal population of long-tailed macaques (Macaca fascicularis) in Bali, Indonesia, that underwent a significant mortality event in summer 2012. During the period of interest,
we noted heightened mortality in three of the five social groups present in this population, with adult females and juveniles experiencing higher mortality rates than adult and subadult males. Limited diagnostic data regarding pathogen identification and a lack of any conclusive etiology of the deaths prevent our ascertainment of the agent(s) responsible for the observed mortality, but given the characteristics of the event we assume it was caused by a transmissible disease outbreak. Comparing the pre- and postmortality event periods, we found significant differences in activity patterns, including a decreased proportion of affiliation in adult females. This result is likely indicative of enhanced social instability induced by the high mortality of adult females that constitute the stable core of macaque social structure. A higher social tension between groups after the mortality event was indicated by more frequent and intense agonistic intergroup encounters. Intergroup conflict success was inversely proportional to the rate of mortality a group suffered. Our results illustrate how changes in demographic structure caused by significant mortality events may have substantial consequences on behavior and social dynamics in primate groups and at the level of a population.
Disciplines :
Zoology
Author, co-author :
Brotcorne, Fany ; Université de Liège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Fuentes, Agustin
Wandia, I Nengah
Beudels-Jamar, Roseline C.
Huynen, Marie-Claude ; Université de Liège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Language :
English
Title :
Changes in Activity Patterns and Intergroup Relationships After a Significant Mortality Event in Commensal Long- Tailed Macaques (Macaca Fascicularis) in Bali, Indonesia
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227–267.
Altmann, J., & Muruthi, P. (1988). Differences in daily life between semiprovisioned and wild-feeding baboons. American Journal of Primatology, 15, 213–221.
Beisner, B. A., Jackson, M. E., Cameron, A. N., & McCowan, B. (2011). Detecting instability in animal social networks: Genetic fragmentation is associated with social instability in rhesus macaques. PloS One, 6(1), e16365.
Bermejo, M., Rodríguez-Teijeiro, J. D., Illera, G., Barroso, A., Vilà, C., & Walsh, P. D. (2006). Ebola outbreak killed 5000 gorillas. Science, 314(5805), 1564.
Brotcorne, F., Wandia, I. N., Rompis, A. L. T., Soma, I. G., Suatha, I. K., & Huynen, M. C. (2011). Recent demographic and behavioral data of Macaca fascicularis at Padangtegal, Bali, Indonesia. In M. D. Gumert, A. Fuentes, & L. Jones-Engel (Eds.), Monkeys on the edge: Ecology and management of long-tailed macaques and their interface with humans (pp. 180–182). Cambridge, U.K.: Cambridge University Press.
Camperio Ciani, A. (1986). Intertroop agonistic behaviour of a feral rhesus macaque troop ranging in town and forest areas in India. Aggressive Behavior, 12, 433–439.
Capitanio, J. P. (2012). Social processes and disease in nonhuman primates: Introduction to the special section. American Journal of Primatology, 74(6), 491–496.
Chapman, C., Rothman, J. M., & Hodder, S. A. M. (2009). Can parasite infections be a selective force influencing primate group size ? A test with red colobus. In M. A. Huffman & C. Chapman (Eds.), Primate parasite ecology: The dymanics of study of host-parasite relationships (pp. 422–440). Cambridge, U.K.: Cambridge University Press.
Chapman, C. A., Gillespie, T. R., & Goldberg, T. L. (2005). Primates and the ecology of their infectious diseases: How will anthropogenic change affect host-pathogen interactions? Evolutionary Anthropology, 14, 134–144.
Cooper, M., Aureli, F., & Singh, M. (2004). Between-group encounters among bonnet macaques (Macaca radiata). Behavioral Ecology and Sociobiology, 56(3), 217–227.
Cords, M. (2012). The behavior, ecology, and social evolution of cercopithecine monkeys. In J. C. Mitani, J. Call, M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The evolution of primate societies (pp. 91–112). Chicago: University of Chicago Press.
Cowlishaw, G., & Dunbar, R. (2000). Primate conservation biology. Chicago: University of Chicago Press.
Dunbar, R. I. M. (1991). Functional significance of social grooming in primates. Folia Primatologica, 57, 121–131.
Engel, G., Hungerford, L. L., Jones-Engel, L., Travis, D., Eberle, R., Fuentes, A., et al. (2006). Risk assessment: A model for predicting cross-species transmission of simian foamy virus from macaques (M. fascicularis) to humans at a monkey temple in Bali, Indonesia. American Journal of Primatology, 68(9), 934–948.
Engel, G. A., Jones-Engel, L., Schillaci, M. S., Suaryana, K. G., Putra, A., Fuentes, A., et al. (2002). Human exposure to herpesvirus B-seropositive macaques, Bali, Indonesia. Emerging Infectious Diseases, 8(8), 789–795.
Fooden, J. (1995). Systematic review of southeast Asian longtail macaques, Macaca fascicularis, (Raffles, [1821]). Fieldiana Zoology (New Series), 81, 1–206.
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.
Fuentes, A. (2012). Ethnoprimatology and the anthropology of the human-primate interface. Annual Review of Anthropology, 41, 101–117.
Fuentes, A., & Gamerl, S. (2005). Disproportionate participation by age/sex classes in aggressive interactions between long-tailed macaques (Macaca fascicularis) and human tourists at Padangtegal Monkey Forest, Bali, Indonesia. American Journal of Primatology, 66(2), 197–204.
Fuentes, A., Rompis, A. L. T., Arta Putra, I. G. A., Watiniasih, N. L., Suatha, I. K., Soma, I. G., et al. (2011). Macaque behavior at the human-monkey interface: The activity and demography of semi-free ranging Macaca fascicularis at Padangtegal, Bali, Indonesia. In M. D. Gumert, A. Fuentes, & L. Jones-Engel (Eds.), Monkeys on the edge: Ecology and management of long-tailed macaques and their interface with humans (pp. 159–179). Cambridge, U.K.: Cambridge University Press.
Fuentes, A., Southern, M., & Suaryana, K. G. (2005). Monkey forests and human landscapes: Is extensive sympatry sustainable for Homo sapiens and Macaca fascicularis on Bali? In J. D. Patterson & J. Wallis (Eds.), Commensalism and conflict: The human-primate interface (Vol. 4, pp. 168–195). Norman, OK: American Society of Primatologists.
Genton, C., Pierre, A., Cristescu, R., Lévréro, F., Gatti, S., Pierre, J.-S., et al. (2014). How Ebola impacts social dynamics in gorillas: A multistate modelling approach. Journal of Animal Ecology. doi:10.1111/1365-2656.12268.
Gumert, M. D., Fuentes, A., & Jones-Engel, L. (2011). Monkeys on the edge: Ecology and management of long-tailed macaques and their interface with humans. Cambridge, U.K.: Cambridge University Press.
Hanamura, S., Kiyono, M., Lukasik-Braum, M., Mlengeya, T., Fujimoto, M., Nakamura, M., et al. (2008). Chimpanzee deaths at Mahale caused by a flu-like disease. Primates, 49, 77–80.
Hanya, G., Matsubara, M., Sugiura, H., Hayakawa, S., Goto, S., Tanaka, T., et al. (2004). Mass mortality of Japanese macaques in a western coastal forest of Yakushima. Ecological Research, 19, 179–188.
Harrison, M. E., Vogel, E. R., Morrogh-Bernard, H. C., & van Noordwijk, M. A. (2009). Methods for calculating activity budgets compared: A case study using orangutans. American Journal of Primatology, 71(4), 353–358.
Hussain, S., Ram, M. S., Kumar, A., Shivaji, S., & Umapathy, G. (2013). Human presence increases parasitic load in endangered lion-tailed macaques (Macaca silenus) in its fragmented rainforest habitats in Southern India. PloS One, 8(5), e63685.
Hutabarat, T. S. P. N., Putra, A. A. G., Widowati, N., & Heriyanto, A. (1999). Streptococcosis septikemik pada babi. In Manual standar metode diagnosa Laboratorium kesehatan hewan (pp. 185–188): Direktorat bina Kesehatan Hewan, Direktorat Jenderal Peternakan, Departemen Pertanian.
Isbell, L. A., & Young, T. P. (1993). Social and ecological influences on activity budgets of vervet monkeys, and their implications for group living. Behavioral Ecology and Sociobiology, 32(6), 377–385.
Jaman, M. F., & Huffman, M. A. (2013). The effect of urban and rural habitats and resource type on activity budgets of commensal rhesus macaques (Macaca mulatta) in Bangladesh. Primates, 54(1), 49–59.
Jones-Engel, L., Engel, G. A., Heidrich, J., Chalise, M., Poudel, N., Viscidi, R., et al. (2006). Temple monkeys and health implications of commensalism, Kathmandu, Nepal. Emerging Infectious Diseases, 12(6), 900–906.
Jones-Engel, L., Engel, G. A., Schillaci, M. A., Rompis, A., Putra, A., Suaryana, K. G., et al. (2005). Primate-to-human retroviral transmission in Asia. Emerging Infectious Diseases, 11(7), 1028–1035.
Jones-Engel, L., May, C. C., Engel, G. A., Steinkraus, K. A., Schillaci, M. A., Fuentes, A., et al. (2008). Diverse contexts of zoonotic transmission of simian foamy viruses in Asia. Emerging Infectious Diseases, 14(8), 1200–1208.
Kaburu, S. S. K., Inoue, S., & Newton-Fisher, N. E. (2013). Death of the alpha: Within-community lethal violence among chimpanzees of the Mahale Mountains National Park. American Journal of Primatology, 75(8), 789–797.
Karlsson, E. A., Engel, G. A., Feeroz, M. M., San, S., Rompis, A., Lee, B. P. Y. H., et al. (2012). Influenza virus infection in nonhuman primates. Emerging Infectious Diseases, 18(10), 1672–1675.
Kaur, T., Singh, J., Tong, S., Humhrey, C., Clevenger, D., Tan, W., et al. (2008). Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related Metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Moutains National Park, Western Tanzania. American Journal of Primatology, 70, 1–11.
Kurita, H., Sugiyama, Y., Ohsawa, H., Hamada, Y., & Watanabe, T. (2008). Changes in demographic parameters of Macaca fuscata at Takasakiyama in relation to decrease of provisioned foods. International Journal of Primatology, 29, 1189–1202.
Lane, K. (2011). Landscape dynamics: Genetic and parasitism in Balinese long-tailed macaques (Macaca fascicularis). Unpublished Ph.D. thesis, University of Notre Dame.
Lane, K., Holley, C., Hollocher, H., & Fuentes, A. (2011). The anthropogenic environment lessens the intensity and prevalence of gastrointestinal parasites in Balinese long-tailed macaques (Macaca fascicularis). Primates, 52(2), 117–128.
Lane, K., Lute, M., Rompis, A., Wandia, I. N., Arta Putra, I. G. A., Hollocher, H., et al. (2010). Pests, pestilence and people: The long-tailed macaque and its role in the cultural complexities of Bali. In S. Gursky-Doyen & J. Supriatna (Eds.), Indonesian primates (pp. 235–248). Developments in primatology: Progress and prospects. New York: Springer Science+Business Media.
Lane-deGraaf, K. E., Putra, I. G. A., Wandia, A., Rompis, I. N., Hollocher, A. H., & Fuentes, A. (2014). Human behavior and opportunities for parasite transmission in communities surrounding long-tailed macaque populations in Bali, Indonesia. American Journal of Primatology, 76(2), 159–167.
Leendertz, F. H., Pauli, G., Maetz-Rensing, K., Boardman, W., Nunn, C., Ellerbrok, H., et al. (2006). Pathogens as drivers of population declines: The importance of systematic monitoring in great apes and other threatened mammals. Biological Conservation, 131(2), 325–337.
Lehmann, J., Korstjens, A. H., & Dunbar, R. I. M. (2007). Group size, grooming and social cohesion in primates. Animal Behaviour, 74(6), 1617–1629.
Loudon, J. E., Howells, M. E., & Fuentes, A. (2006). The importance of integrative anthropology: A preliminary investigation employing primatological and cultural anthropological data collection methods in assessing human-monkey co-existence in Bali, Indonesia. Ecological and Environmental Anthropology, 2(1), 1–13.
MacIntosh, A. J. J., Jacobs, A., Garcia, C., Shimizu, K., Mouri, K., Huffman, M. A., et al. (2012). Monkeys in the middle: parasite transmission through the social network of a wild primate. PloS One, 7(12), e51144.
Mätz-Rensing, K., Winkelmann, J., Becker, T., Burckhardt, I., Van Der Linden, M., Köndgen, S., et al. (2009). Outbreak of Streptococcus equi subsp. zooepidemicus infection in a group of rhesus monkeys (Macaca mulatta). Journal of Medical Primatology, 38(5), 328–334.
McLennan, M., & Huffman, M. A. (2012). High frequency of leaf swallowing and its relationship to intestinal parasite expulsion in "village" chimpanzees at Bulindi, Uganda. American Journal of Primatology, 74, 642–650.
Nunn, C. L. (2012). Primate disease ecology in comparative and theoretical perspective. American Journal of Primatology, 74(6), 497–509.
Nunn, C. L., & Altizer, S. (2006). Infectious diseases in primates: Behavior, ecology and evolution. Oxford: Oxford University Press.
Pope, T. R. (1998). Effects of demographic change on group kin structure and gene dynamics of populations of red howling monkeys. Journal of Mammalogy, 79(3), 692–712.
Quinn, G., & Keough, M. (2002). Experimental designs and data analysis for biologists. Cambridge, U.K.: Cambridge University Press.
Core Team, R. (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Salasia, S. I. O., Teguh Wibawan, I. W., Pasaribu, F. H., Abdulmawjood, A., & Lämmler, C. (2004). Persistent occurrence of a single Streptococcus equi subsp. zooepidemicus clone in the pig and monkey population in Indonesia. Journal of Veterinary Science, 5(3), 263–265.
Sapolsky, R. M., & Share, L. J. (2004). A pacific culture among wild baboons: Its emergence and transmission. PLoS Biology, 2(4), 534–541.
Scarry, C. J. (2013). Between-group contest competition among tufted capuchin monkeys, Sapajus nigritus, and the role of male resource defence. Animal Behaviour, 85(5), 931–939.
Scarry, C. J., & Tujague, M. P. (2012). Consequences of lethal intragroup aggression and alpha male replacement on intergroup relations and home range use in tufted capuchin monkeys (Cebus apella nigritus). American Journal of Primatology, 74(9), 804–810.
Schino, G., Maestripieri, D., Scucchi, S., & Turillazzi, P. G. (1990). Social tension in familiar and unfamiliar pairs of long-tailed macaques. Behaviour, 113(3/4), 264–272.
Soedarmanto, I., Pasaribu, F. H., Wibawan, I. W. T., & Lammler, C. (1996). Identification and molecular characterization of serological group C Streptococci isolated from diseased pigs and monkeys in Indonesia. Journal of Clinical Microbiology, 34(9), 2201–2204.
Sokal, R., & Rohlf, F. (1995). Biometry. New York: W. H. Freeman.
Sugiura, H., Agetsuma, N., & Suzuki, S. (2002). Troop extinction and female fusion in wild Japanese macaques in Takushima. International Journal of Primatology, 23(1), 69–84.
Sugiura, H., Saito, C., Sato, S., Agetsuma, N., Takahashi, H., Tanaka, T., et al. (2000). Variation in intergroup encounters in two populations of Japanese macaques. International Journal of Primatology, 21(3), 519–535.
Thierry, B. (2007). Unity in diversity: Lessons from macaque societies. Evolutionary Anthropology: Issues, News, and Reviews, 16(6), 224–238.
van Noordwijk, M. A., & van Schaik, C. P. (1987). Competition among female long-tailed macaques, Macaca fascicularis. Animal Behaviour, 35(2), 577–589.
van Schaik, C., van Noordwijk, M., Warsono, B., & Sutriono, E. (1983). Party size and early detection of predators in Sumatran forest primates. Primates, 24(2), 211–221.
Wallis, J., & Lee, D. R. (1999). Primate conservation: The prevention of disease transmission. International Journal of Primatology, 20, 803–826.
Weaver, R., Entry, J. A., & Graves, A. (2005). Numbers of fecal streptococci and Escherichia coli in fresh and dry cattle, horse, and sheep manure. Canadian Journal of Microbiology, 51, 847–851.
Weyher, A. H., Ross, C., & Semple, S. (2006). Gastrointestinal parasites in crop raiding and wild foraging Papio anubis in Nigeria. International Journal of Primatology, 27, 1519–1534.
Wheatley, B. P. (1999). The sacred monkeys of Bali. Prospect Heights, IL: Waveland Press.
Worton, B. J. (1989). Kernel methods for estimating the utilization distribution in home-range studies. Ecology, 70(1), 164–168.
Young, T. P. (1994). Natural die-offs of large mammals: Implications for conservation. Conservation Biology, 8(2), 410–418.