CICASP | Center for International Collaboration and Advanced Studies in Primatology

Research

• Primate behavioral ecology
• Primate parasite/disease ecology and ecological immunology
• Parasite community structure and coinfection
• Fitness costs and health impacts of parasitism in natural populations
• Wildlife monitoring, health and conservation
• Biocomplexity - fractal analysis as an indicator of complexity loss or increased stereotypy in stress and disease

Infectious Disease Ecology

I have initiated a long-term project monitoring parasite infection dynamics in Japanese macaques (Macaca fuscata), with the aim of modeling interactions between primate and parasite population processes and the impacts of parasitism on primate health and behavior. Understanding these patterns and processes under natural conditions can help determine potential impacts of habitat alteration on primate populations, which is a constant concern in conservation of endangered species. One of my main interests is to determine host traits that contribute to heterogeneity in infection phenotypes across individuals. I am currently focusing on the importance of social structure in mediating both exposure and susceptibility to parasitic nematode infection, working with the populations of Japanese macaques on Koshima and Yakushima Islands, under naturalistic and field-experimental conditions. By disrupting the natural course of infection via anthelmintic treatment of target individuals, I hope to uncover mechanisms of reinfection and potential fitness benefits of parasite removal.

In a recent expansion of this project, I am now beginning a project in collaboration with the Sabah Wildlife Department, the Danau Girang Field Centre and Cardiff University, Universiti Malaysia Sabah and other researchers here at KUPRI to investigate ecological networks in parasite infection among Borneo's rich primate biodiversity. Since Japanese macaques are isolated from other nonhuman primates, within-species effects clearly dominate parasite transmission dynamics, at least for parasites with direct modes of transmission. In tropical areas, however, multiple related primate species typically live sympatrically, allowing for potential cross-infection by parasites. This means that not only specific host individuals but also specific host species may play a disproportionate role in the transmission dynamics of certain disease-causing or otherwise parasitic organisms, i.e. between-species effects. If host community assemblages can affect the transmission rates of generalist (shared) parasites, then the potential exists for other species to influence infection dynamics of focal species, such as primates and other wildlife of conservation concern, or humans, leading to indirect effects on their population viabilities. We aim to address such issues in a project aimed at: (1) developing robust parasite-specific molecular diagnostics to assess primate-parasite biodiversity; (2) determining the extent to which parasites are shared across primate hosts and whether parasites can determine host community structure; (3) assessing spillover of gastrointestinal parasites between nonhuman primates and humans, including domestic animals; and, (4) examining the relationship between habitat fragmentation and parasite biodiversity sensu environmental parasitology.

Fractal Complexity in Animal Behaviour

Perhaps because of the difficulties inherent in determining costs associated with parasite infection and other ecological challenges, I have also been investigating the utility of fractal analysis in health monitoring studies of wild animal behaviour. I am currently using various fractal methods, including detrended fluctuation analysis (DFA) and various other Hurst exponent estimators, as well as other tools that measure fractal dimension, to examine complexity in behavioural sequences - which are subtly more stereotypical with stress and disease. My previous research suggested a possible link between parasitic infection and complexity loss in Japanese macaques, and I am currently applying these fractal tools to other study systems, including further work with Japanese macaques and other primates in collaboration with the University of Veterinary and Pharmaceutical Sciences Brno, as well as penguins in collaboration with the IPHC-DEPE, CNRS-University of Strasbourg. In the latter case, using the novel merger of temporal fractal analysis applied to data collected via bio-logging (i.e. using animal-attached data recording devices) has shown that penguin dive sequences exhibit fractal properties across a number of scales and over long time periods, and that certain challenges such as increased physiological stress are associated with fractal complexity loss. We aim to use fractal tools to investigate through a comparative approach behavioral complexity in relation to both individual and environmental quality, and particularly with reference to issues surrounding climate change in the Antarctic region.

Background

• (2000) B. Sc. in Anthropology, Department of Anthropology, University of Calgary
• (2002) M. A. in Anthropology, Concentration: Primatology, Department of Anthropology, University of Calgary
• (2010) D. Sc. in Primatology, Graduate School of Sciences, Division of Biology, Primate Research Institute, Kyoto University

After receiving the MA degree from the University of Calgary, I moved to Japan and worked as an English teacher before returning to academia in 2007 to conduct doctoral studies at the Kyoto University Primate Research Institute. My dissertation, which was supervised by Dr. Michael Huffman, was entitled "Gastrointestinal helminth parasitism among Japanese macaques: patterns, processes and host responses". After completing my degree, I remained at the PRI as a post-doctoral research associate with CICASP but worked largely with Dr. Yan Ropert-Coudert at the CNRS-Strasbourg University supported by a JSPS researcher exchange grant to study complexity in seabird foraging behavior in relation to habitat characteristics and global change. I was awarded an assistant professorship with CICASP in April 2012, and was promoted to Associate Professor in April 2014 with affiliations to Kyoto University's Wildlife Research Center and its Leading Graduate Program in Primatology and Wildlife Science. In April 2017, I became tenured Associate Professor at PRI, with CICASP and the Department of Ecology and Social Behavior, through Kyot University's Institute for Liberal Arts and Sciences. To date, I have studied primates in one capacity or another in Central America, Africa, and Asia, but my current focus is on Asian primates and their gastrointestinal parasites. My research is and has been supported by grants-in-aid from the Japan Society for the Promotion of Science, as well as Kyoto University. Aside from primates, I also study seabird behaviour, and in particular patterns of behavioural complexity among various penguin species in relation to various ecological challenges and global change biology.

Selected Publications

updated December 2018

*these authors contributed equally to this work

• Frias L, Hasegawa H, Stark DJ, Salgado-Lynn M, Nathan KSS Senthilvel, Chua T, Goossens B, Okamoto M, MacIntosh AJJ (2018) A pinworm’s tale: the evolutionary history of Lemuricola (Protenterobius) nycticebi. Int J Parasitol: Parasites & Wildlife. DOI: 10.1016/j.ijppaw.2018.11.009
• Le Guen C, Kato A, Raymond B, Barbraud C, Beaulieu M, Bost, C-A, Delord K, MacIntosh AJJ, Meyer X, Raclot T, Sumner M, Takahashi A, Thiebot J-B, Ropert-Coudert Y (2018) Reproductive performance and foraging behaviour share a common sea-ice concentration optimum in Adélie penguins (Pygoscelis adeliae). Global Change Biol 24:5304–5317. DOI:10.1111/gcb.14377
• Romano V, Shen M, Pansanel J, MacIntosh AJJ, Sueur C (2018) Social transmission in networks: global efficiency peaks with intermediate levels of modularity. Behav Ecol Sociobiol 72:154
• Burgunder J, Petrzelkova KJ, Modry D, Kato A, MacIntosh AJJ (2018) Fractal measures in activity patterns: do gastrointestinal parasites affect the complexity of sheep behaviour? Appl Anim Behav Sci. DOI: 10.1016/j.applanim.2018.05.014
• Frias L, MacIntosh AJJ (In Press) Threatened Hosts, Threatened Parasites? Parasite Diversity and Distribution in Red-Listed Primates. In: A Behie et al. (eds) Primate Research and Conservation in the Anthropocene. Cambridge University Press
• Sarabian C, Belais R, MacIntosh AJJ (2018) Feeding decisions under contamination risk in bonobos. Phil Trans B. DOI: 10.1098/rstb.2017.0195
• Frias L, Stark DJ, Salgado Lynn M, Nathan SKSS, Goossens B, Okamoto M, MacIntosh AJJ (2018) Lurking in the dark: Cryptic Strongyloides in a Bornean slow loris. Int J Parasitol: Parasites & Wildlife. DOI: 10.1016/j.ijppaw.2018.03.003
• Sarabian C, Ngoubangoye B, MacIntosh AJJ (2017) Avoidance of biological contaminants through sight, smell and touch in chimpanzees. R Soc Open Sci 4:170968.
• Balasubramaniam KN, Beisner BA, Berman CM, De Marco A, Duboscq J, Koirala S, Majolo B, MacIntosh AJ, McFarland R, Molesti S, Ogawa H, Petit O, Schino G, Sosa S, Sueur C, Thierry B, de Waal FBM, and McCowan B (2017) The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure. Am J Primatol DOI:10.1002/ajp.22727.
• Duboscq J, Romano V, Sueur C, MacIntosh AJJ (2017) One step at a time in investigating relationships between self-directed behaviours and parasitological, social and environmental variables. R Soc Open Sci 4:170461
• Meyer X, MacIntosh AJJ, Chiaradia A, Kato A, Mattern T, Sueur C, Ropert-Coudert Y (Accepted) Shallow divers, deep waters, and the rise of behavioural stochasticity. Marine Biology 164:149
• Burgunder J, Hashiomto C, Modry D, Kalousova B, Petrzelkova K, MacIntosh AJJ (2017) Complexity in behavioural organisation and strongylid infection among wild chimpanzees. Animal Behaviour 129:257-268
• Duboscq J, Romano V, Sueur C, MacIntosh AJJ (2016) Scratch that itch: revisiting links between self-directed behaviour and parasitological, social and environmental factors in a free-ranging primate. Royal Society Open Science
• Rigaill L, MacIntosh AJJ, Higham JP, Winters S, Shimizu K, Mouri K, Suzumura T, Furuichi T, Garcia C (2016) Testing for links between face color and age, dominance status, parity, weight, and intestinal nematode infection in a sample of female Japanese macaques. Primates 58:83-91
• Duboscq J, Romano V, MacIntosh A, Sueur C (2016) Social information transmission in animals: Lessons from studies of diffusion. Frontiers in Psychology 7: 1147
• Romano V, Duboscq J, Sueur C, MacIntosh AJJ (2016) Modelling infection transmission in primate networks to predict centrality-based risk. Am J Primatol 78:767–779
• Duboscq J, Romano V, Sueur C, MacIntosh AJJ (2016) Network centrality and seasonality interact to predict lice load in a social primate. Sci Rep 6:22095
• Sarabian C, MacIntosh AJJ (2015) Hygienic tendencies correlate with low geohelminth infection in free-ranging macaques. Biology Letters 11:20150757
• MacIntosh AJJ (2015) At the edge of chaos – error tolerance and the maintenance of Levy statistics in animal movement: Comment on “Liberating Lévy walk research from the shackles of optimal foraging” by A.M. Reynolds. Physics of Life Reviews. doi:10.1016/j.plrev.2015.07.010
• Reynolds AM, Ropert-Coudert Y, Kato A, Chiaradia A, MacIntosh AJJ (2015) A priority-based queuing process explanation for scale-free foraging behaviours. Animal Behaviour 108:67-71
• Meyer X*, MacIntosh AJJ*, Kato A, Chiaradia A, Ropert-Coudert Y (2015) Hydrodynamic handicaps and organizational complexity in the foraging behavior 2 of two free-ranging penguin species. Animal Biotelemetry 3:25
• Rigaill LR, MacIntosh AJJ, Higham JP, Winters S, Shimizu K, Mouri K, Furuichi T, Garcia C (2015) Multimodal advertisement of pregnancy in free-ranging female Japanese macaques (Macaca fuscata). PLoS ONE 10(8): e0135127
• Ropert-Coudert Y, Kato A, Meyer X, Pellé M, MacIntosh AJJ, Angelier F, Chastel O, Widmann M, Arthur B, Raymond B, Raclot T (2015) A complete breeding failure in an Adélie penguin colony correlates with unusual, extreme environmental events. Ecography 38:111-113
• Pasquaretta C, Levé M, Claidière N, van de Waal E, Whiten A, MacIntosh AJJ, Pelé M, Borgeaud C, Brosnan S, Crofoot M, Fedigan L, Fichtel C, Hopper L, Mareno MC, Petit O, Schnoell AV, di Sorrentino EP, Thierry B, Tiddi B, Sueur C (2014) Social networks in primates: smart and tolerant species have more efficient networks. Scientific Reports 4:7600
• MacIntosh AJJ (2014) The fractal primate: interdisciplinary science and the math behind the monkey. Primate Research 30:95-119
• MacIntosh AJJ (2014) Ecology and epidemiology of nematode infection in Japanese macaques: building an empirical model. Primate Research 30:23-51
• Cottin M*, MacIntosh AJJ*, Kato A, Takahashi A, Debin M, Raclot T, Ropert-Coudert Y (2014) Corticosterone administration leads to a transient alteration of foraging behaviour and complexity in a diving seabird. Marine Ecology Progress Series 496:249-262
• MacIntosh AJJ*, Pelletier L*, Chiaradia A, Kato A, Ropert-Coudert Y (2013) Temporal fractals in seabird foraging behaviour: diving through the scales of time. Scientific Reports 3:1884
• Sueur C, MacIntosh AJJ, Jacobs AT, Watanabe K, Petit O (2013) Predicting leadership using nutrient requirements and dominance rank of group members. Behavioral Ecology and Sociobiology 67:457-470
• MacIntosh AJJ, Jacobs A, Garcia C, Shimizu K, Mouri K, Huffman MA, Hernandez AD (2012) Monkeys in the middle: parasite transmission through the social network of a wild primate. PLoS one 7:e51144
• MacIntosh AJJ, Huffman MA, Nishiwaki K, Nishiwaki-Miyabe T (2012) Urological screening of wild Japanese macaques: trends in nutrition and health. International Journal of Primatology 33:460-478
• MacIntosh AJJ, Alados CL, Huffman MA (2011) Fractal analysis of behaviour in a wild primate: behavioural complexity in health and disease. Journal of the Royal Society Interface 8:1497-1509
• MacIntosh AJJ, Hernandez AD, Huffman MA (2010) Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates 51:353-364
• MacIntosh AJJ, Huffman MA (2010) Towards understanding the role of diet in host-parasite interactions: the case for Japanese macaques. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Springer, pp. 323–344
• Hernandez AD, MacIntosh AJJ, Huffman MA (2009) Primate parasite ecology: patterns and predictions from an on-going study of Japanese macaques. In: Huffman MA, Chapman CA (eds) Primate parasite ecology: the dynamics of host-parasite relationships. Cambridge University Press, pp. 387–401
• MacIntosh AJJ, Sicotte P (2009) Vigilance in ursine black and white colobus monkeys (Colobus vellerosus): an examination of the effects of conspecific threat and predation. American Journal of Primatology 71:919-927
• Sicotte P, MacIntosh AJ (2004) Inter-group encounters and male incursions in Colobus vellerosus in Central Ghana. Behaviour 141(5):533-553

Students Supervised

Current Graduate Students

Zhihong Xu, section of Social Systems Evolution. 1st year master's student (2018~). Project Title: Comparative look at the transmission of parasites in macaque social and spatial networks. *Previously an undergraduate intern with me at KUPRI (2016~2017) from Sun Yat Sen University, China. 

Kenneth Keuk, pre-PhD research student (2019~). *previously a Master's student from the University of Strasbourg who conducted his Master's research with me at KUPRI (2016). Project Title: Social networks, social style, and the dynamics of parasite infection

Surdensteeve Peter, Institute of Tropical Biology and Conservation. 1st year Master's student (2018~). Project Title: The diversity and distribution of parasitic protozoa in primates of the lower Kinabatangan Flood Plain

Cecile Sarabian, section of Social Systems Evolution. 4th year doctoral student. Project Title: The Origins of Hygiene: Infection-risk Avoidance in Papionini and Hominidae. *Formerly 2nd year master's internship student (2014) from the University of Strasbourg and 1st year master's internship student (2012-2013) from Rennes 1 University.

Liesbeth Frias, section of Cellular and Molecular Biology. 4th year doctoral student. Project Title: Host-Parasite Systems Dynamics in Human-Modified Habitats (since 2014).

Current Postdoctoral Fellows

Valeria Romano de Paula, Currently a JSPS postdoc at PRI. Formerly a student at the: 1. Institut Pluridisciplinaire Hubert Curien - IPHC, Département Ecologie, Physiologie et Ethologie - DEPE, University of Strasbourg. 3rd year doctoral student; 2. Kyoto University Wildlife Research Center. Japan Society for the Promotion of Science (JSPS) Short-term Doctoral Fellow. Graduated 2017! Project Title: Primate Social Networks as a Trade-off between Information and Disease Transmission  (2013~2017).

Barbora Kubenova (photo coming soon),  Primate Research Institute. Japan Society for the Promotion of Science (JSPS) Standard Postdoctoral Fellow. Project Title: Infant handling and social integration of infants and juveniles in wild Japanese macaques (2017~2019).

Marie Sigaud (photo coming soon), Primate Research Institute. Japan Society for the Promotion of Science (JSPS) Standard Postdoctoral Fellow. Project Title: Measuring fitness costs of habitat degradation in an endangered primate (2018~2020).

Alumni

Julie Duboscq. (2013-2018) Formerly a (1) Postdoctoral Fellow at the Primate Research Institute with the Japan Society for the Promotion of Science (JSPS) Short-term (2016~2017) and Standard (2017~2019) programs. Project Title: Connecting the dots: linking host behavior to parasite transmission and infection risk

Xavier Meyer (2013~2018). Formerly a (1) research associate at PRI (2017-2018); (2) student (2013~2016) at the Institut Pluridisciplinaire Hubert Curien - IPHC, Département Ecologie, Physiologie et Ethologie - DEPE, University of Strasbourg. Graduated 2016! Project Title: Does complexity in behavioral organization allow seabirds to adapt to changes in their environment?

Jade Burgunder. (2013~2018) PhD student at Masaryk University, Department of Botany and Zoology. Graduated 2018!  Project Title: Complexity in Behavioral Organization: a novel approach to assessing clinical outcomes of parasitic diseases 

Elodie Thomas. (2013) Previously a Master's internship student from the University of Strasbourg who conducted her Master's research with me at KUPRI. Project Title: Influence of nematode parasites on stress of Koshima macaques (Macaca fuscata)

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