CICASP | Center for International Collaboration and Advanced Studies in Primatology

Research

The work being done in my lab broadly interfaces behavioral ecology and parasitism, with the ultimate aim of better understanding the evolutionary relationships between animal hosts and the parasites that depend on them. I am a behavioral ecologist by training and at heart, but like any modern scientific undertaking, our work covers many fields, including behavioral ecology and ethology, cognition, parasitology, ecological immunology and infectious disease ecology and epidemiology. To accomplish our research aims, we integrate field and lab work with computational methods that delve into network analyses, fractals and chaos.

Research Keywords

• Behavioral ecology
• 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
• one health; ecohealth; coupled human and natural systems
• Biocomplexity - fractal analysis as an indicator of complexity loss or increased stereotypy in stress and disease

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.

Current Projects

Parasites as a Selective Force in Primate Social Systems Evolution

The idea that parasites pose a selection pressure in the evolution of free-living species is not new, nor is the idea that parasites might factor into the evolution of host social systems. In his famous essay appearing in the Annual Reviews of Ecology and Systematics, Richard Alexander (1974) wrote that there may be no universal benefits to group living, but there are universal costs, one of which being the heightened risk of infectious disease. Later, William Freeland (1976, Biotropica; 1979, Ecology) suggested that primate groups act as biological islands of infection (colonization) for parasites, and thereby brought the concepts of island biogeography into the study of host-parasite ecology. Flash forward a few decades and, while there is no shortage of studies now attempting to link sociality with infectious disease, we still lack concrete evidence in most cases demonstrating a role for parasites in host social systems evolution. That said, compelling studies now appear regularly in this field of research, for example in relation to organizational immunity - a form of behavioral immunity whereby elements of the social structure exist to protect individuals from exposure to infection - and the role of social networks in disease or parasite transmission.

It is from this context that work in my lab has sprung. With students and collaborators, we have begun trying to examine links between social structure and parasitism, mainly using primates as a model system. Empirical aspects of this work rely on field data describing the social netwroks of primates and variation in parasitism across individuals. Theoretical aspects of the work involve simulation and/or agent-based modeling - themselves drawing on empirical networks and infectious disaese dynamics - to predict the spread of infection through groups and how this might change under varying conditions of social structure and the environment. Long-term work with Japanese macaques and their gastrointestinal helminth parasites provides a useful platform for this research, which has recently been combined with deworming experiements in a free-living population to better undertstand the impacts of infection on host individuals and populations. 

Primates and Parasites of Sabah as Indicators of a Transitioning Ecosystem (P²ARASITE)

The main purpose of this project is to investigate ecological networks involving parasites and Borneo's rich primate biodiversity in an area subjected to ongoing anthropogenic change. Unlike the case for Japanese macaques, which are isolated from other nonhuman primates and thus within-species effects dominate parasite transmission dynamics, primates in tropical areas typically share their habitats with multiple related species, allowing for potential between-species effects in parasitism and likely involving 'apparent competition'; i.e. competition between primate species for 'enemy-free space'. Our search for 'superspreaders' among specific host individuals in Japanese macaque and other primate groups here expands to a search for specific host species that may play disproportionate roles in the transmission dynamics of certain disease-causing or otherwise parasitic organisms. 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. Throw in large-scale land conversion and the ever-shrinking habitats for wildlife everywhere, and we have a recipe for which the end-product has yet to be determined. Although challenging, it is actually critical to view parasitism from such a complex, community perspective. The ultimate aims here will be to carry this work into the one health paradigm, where environmental, wildlife and public health are treated as mart of the same, dynamic system.

To accomplish our aims, we are using a diverse set of methods that include field work and sampling, traditional and molecular parasitology, social, ecological and spatial data analysis and modeling, as well as comparative literature surveys to gain a broader perspective. To date, our major focus has been on gastrointestinal parasites. Such environmentally-transmitted parasites have the potential to spread into new regions and new hosts as landscapes are altered, making them important target species to consider. In addition, they are perhaps more amenable to sampling than other parasitic organisms, particularly when working in sensitive areas with endangered host species.

Aims in a nutshell

• develop robust parasite-specific molecular diagnostics to assess primate-parasite biodiversity
• determine the extent to which parasites are shared across primate hosts and whether parasites can determine host community structure
• assess spillover of gastrointestinal parasites between nonhuman primates and humans, including domestic animals
• examine the relationship between habitat fragmentation and parasite biodiversity sensu environmental parasitology. 

Collaborating institutions

• Danau Girang Field Centre and Cardiff University
• Sabah Wildlife Department
• Universiti Malaysia Sabah
• Kinabatangan Orang-utan Conservation Programme (HUTAN)

Selected Publications

Google Scholar Page

Selected Publication List [updated June 2021]

• Sarabian C, Belais R, MacIntosh AJJ (2021) Avoidance of contaminated food correlates with low protozoan infection in bonobos. Front Ecol Evol 9:651159
• Frias L, Hasegawa H, Chua TH, Sipangkui S, Stark D, Salgado-Lyn M, Goossens B, Keuk K, Okamoto M, MacIntosh AJJ (2021) Parasite community structure in sympatric Bornean primates. Int J Parasitol DOI: 10.1016/j.ijpara.2021.03.003
• Gomez-Melara JL, Acosta-Naranjo R, MacIntosh AJJ, Maulany RI, Ngakan PO, Amici F (2021) Dominance style predicts differences in food retrieval strategies. Sci Rep 11:2726
• Amici F, Widdig A, MacIntosh AJJ, Beltrán Francés V, Castellano-Navarro A, Lopez Caicoya, Karimullah K, Maulany RI, Ngakan PO, Hamzah AS, Majolo B (2020) Dominance style only partially predicts differences in neophobia and social tolerance over food in four macaque species. Sci Rep 10: 22069
• Beltrán Francés V, Castellano-Navarro A, Maulany RI, Ngakan PO, MacIntosh AJJ, Llorente M, Amici F (2020) Play behavior in immature moor macaques (Macaca maura) and Japanese macaques (Macaca fuscata). Amer J Primatol 82(10):e23192. DOI: 10.1002/ajp.23192
• Romano V, MacIntosh AJJ, Sueur C (2020) Stemming the flow: information, infection, and social evolution. Trends in Ecology and Evolution DOI: 10.1016/j.tree.2020.07.004
• Meyer X, MacIntosh AJJ, Chiaradia A, Kato A, Ramirez F, Sueur C, Ropert-Coudert Y (Accepted) Oceanic thermal structure mediates dive sequences in a foraging seabird. Ecol and Evol DOI: 10.1002/ece3.6393
• Sarabian C, Ngoubangoye B, MacIntosh AJJ (2020) Divergent strategies in faeces avoidance between two cercopithecoid primates. R Soc Open Sci 7: 191861
• Frias L, MacIntosh AJJ (2020) Global Diversity and Distribution of Soil-Transmitted Helminths in Monkeys. In: S Knauf & L Jones-Engel (eds) Neglected Diseases in Monkeys - From the Monkey-Human Interface to One Health. Springer Nature
• Balasubramaniam KN, Sueur C, Huffman MA, MacIntosh AJJ (2019) Primate Infectious Disease Ecology: Insights and Future Directions at the Human-Macaque Interface. In: J-H Li et al. (eds) The Behavioral Ecology of the Tibetan Macaque
• Frias L, Stark DJ, Salgado Lynn M, Nathan S, Goossens B, Okamoto M, MacIntosh AJJ (2019) Molecular characterization of nodule worm in a community of Bornean primates. Ecology and Evolution 9:3937-3945
• Poirotte C*, Sarabian C*, Ngoubangoye B, MacIntosh AJJ, Charpentier M (2019) Faecal avoidance differs across sexes but not with nematode infection-risk in mandrills. Anim Behav 149:97-106
• 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. 205:44-53
• Frias L, MacIntosh AJJ (2019) 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. 373: 20170195
• 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. 7:141-146
• 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 80(1):e22727
• 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 14:105–107
• 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

Press

On parasite avoidance, hygiene and 'disgust'

Students Supervised

Current Graduate Students

Katherine Majewski, section of Social Systems Evolution. DSc student (2021~). Project Title: Impact on small carnivore community and infectious disease dynamics on Yakushima Island resulting from the introduction of non-native raccoon dogs (Nyctereues procyonoides)

Zhihong Xu, section of Social Systems Evolution. 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 and MEXT Scholar (2019~present). *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

Abdullah Langgeng, pre-master's research student and MEXT scholar (2019~present). Project Title: Does hot spring bathing behavior affect the parasites and gut microbiome of Japanese macaques?

Current Postdoctoral Fellows

Cecile Sarabian, JSPS Postdoctoral Fellow (2019~present). Formerly a PhD student in the 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.

Alumni

Marie Sigaud, 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 (2018~2021).

Surdensteeve Peter, Institute of Tropical Biology and Conservation. Master's student (2018~2020). Project Title: The diversity and distribution of parasitic protozoa in primates of the lower Kinabatangan Flood Plain

Barbora Kubenova. (2017~2019)  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

Liesbeth Frias (2014~2019), section of Cellular and Molecular Biology. 4th year doctoral student. Project Title: Host-Parasite Systems Dynamics in Human-Modified Habitats

Valeria Romano de Paula. (2013~2019) Formerly a JSPS postdoc at PRI (2017~2019) and cosupervised 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).

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)

Contact