Primate and parasite community assemblages as indicators of a transitioning environment

• Project/Area Number: 16H06181
• Research Category: Grant-in-Aid for Young Scientists (A)
• Allocation Type: Single-year Grants
• Research Field: Physical anthropology
• Research Institution: Kyoto University
• Principal Investigator: MacIntosh Andrew 京都大学, 霊長類研究所, 准教授 (30623136)
• Project Period (FY): 2016-04-01 – 2020-03-31
• Project Status: Completed (Fiscal Year 2019)
• Budget Amount: ¥21,060,000 (Direct Cost: ¥16,200,000、Indirect Cost: ¥4,860,000); Fiscal Year 2019: ¥1,820,000 (Direct Cost: ¥1,400,000、Indirect Cost: ¥420,000); Fiscal Year 2018: ¥4,940,000 (Direct Cost: ¥3,800,000、Indirect Cost: ¥1,140,000); Fiscal Year 2017: ¥4,940,000 (Direct Cost: ¥3,800,000、Indirect Cost: ¥1,140,000); Fiscal Year 2016: ¥9,360,000 (Direct Cost: ¥7,200,000、Indirect Cost: ¥2,160,000)
• Keywords: Primatology / Infectious Disease / Parasitology / Conservation / Biodiversity / Ecology / parasitology / community ecology / host-parasite ecology / epidemiology / conservation / Epidemiology / primatology / ecology / Conservation Ecology / Wildlife Epidemiology / Community Ecology

Outline of Final Research Achievements

This research characterized primate and parasite communities in the Kinabatangan region of Sabah, Malaysian Borneo. Results fill a key knowledge gap about parasites infecting primates in Southeast Asia, which has historically been under studied despite being a biodiverse region with high degrees of human disturbance of natural areas and thus high risk of disease emergence.

Combining primate censuses with sampling and analysis of primate feces across a fragmented landscape, this study demonstrates that habitat disturbance can both enhance and reduce the risk of parasite infection in the community, largely depending on parasite traits like its mode of transmission and whether or not it can infect multiple host species. This study also found evidence of potentially pathogenic and even zoonotic parasites in the community, so future work will need to investigate these in greater detail to better assess risks to primate conservation and public health.

Academic Significance and Societal Importance of the Research Achievements

Parasites are everywhere in nature, and can increase the risk of extinction in endangered animals or "spill over" into human populations. Parasitism is thus a conservation and public health concern, so understanding how human disturbance of nature influences wildlife parasites is clearly important.

Research Products

• [Journal Article] irst description of male worms of Enterobius (Colobenterobius) serratus (Nematoda: Oxyuridae), the pinworm parasite of proboscis monkeys. (2020)
  • Author(s): Hasegawa H, Frias l, Peter S, Hasan NH, Stark DJ, Lynn MS, Sipangkui S, Goossens B, Matsuura K, Okamoto M, MacIntosh AJJ.
  • Journal Title: Zootaxa Volume: 4722(3) Issue: 3 Pages: 187-294
  • DOI: 10.11646/zootaxa.4722.3.6
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Antiprotozoal and antihelminthic properties of plants ingested by wild Japanese macaques (Macaca fuscata yakui) in Yakushima Island (2020)
  • Author(s): Tasdemir D, MacIntosh AJJ, Stergiou P, Kaiser M, Mansour N, Bickle Q, Huffman MA
  • Journal Title: Journal of Ethnopharmacology Volume: 247 Pages: 112270-112270
  • DOI: 10.1016/j.jep.2019.112270
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Divergent strategies in faeces avoidance between two cercopithecoid primates (2020)
  • Author(s): Sarabian C, Ngoubangoye B, MacIntosh AJJ
  • Journal Title: Royal Society Open Science Volume: 7 Issue: 3 Pages: 191861-191861
  • DOI: 10.1098/rsos.191861
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Primate Infectious Disease Ecology: Insights and Future Directions at the Human-Macaque Interface (2020)
  • Author(s): Balasubramaniam KN, Sueur C, Huffman MA, MacIntosh AJJ
  • Journal Title: The Behavioral Ecology of the Tibetan Macaque Volume: 1 Pages: 249-284
  • DOI: 10.1007/978-3-030-27920-2_13
  • ISBN: 9783030279196, 9783030279202
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Global Diversity and Distribution of Soil-Transmitted Helminths in Monkeys (2020)
  • Author(s): Frias L, MacIntosh AJJ
  • Journal Title: Neglected Diseases in Monkeys - From the Monkey-Human Interface to One Health Volume: 1
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Hematological and blood chemistry values in captive Japanese macaques (Macaca fuscata fuscata) (2019)
  • Author(s): Takako Miyabe-Nishiwaki Andrew J. J. MacIntosh Akihisa Kaneko Mayumi Morimoto Juri Suzuki Hirofumi Akari Munehiro Okamoto
  • Journal Title: Journal of Medical Primatology Volume: 48 (6) Issue: 6 Pages: 338-350
  • DOI: 10.1111/jmp.12434
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Primate Infectious Disease Ecology: Insights and Future Directions at the Human-Macaque Interface (2019)
  • Author(s): Balasubramaniam KN, Sueur C, Huffman MA, MacIntosh AJJ
  • Journal Title: The Behavioral Ecology of the Tibetan Macaque Volume: in press
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Global Diversity and Distribution of Soil-Transmitted Helminths in Monkeys (2019)
  • Author(s): Frias L, MacIntosh AJJ
  • Journal Title: Neglected Diseases in Monkeys - From the Monkey-Human Interface to One Health Volume: in press
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Social Behavior and Infectious Disease (2019)
  • Author(s): Duboscq J, Romano V, MacIntosh AJJ
  • Journal Title: Encyclopedia of Animal Behavior, 2nd edition Volume: 4 Pages: 790-800
  • Int'l Joint Research
• [Journal Article] Threatened Hosts, Threatened Parasites? Parasite Diversity and Distribution in Red-Listed Primates (2019)
  • Author(s): Frias L, MacIntosh AJJ
  • Journal Title: Primate Research and Conservation in the Anthropocene Volume: 1 Pages: 141-164
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Parasites of gibbons (2019)
  • Author(s): 5.MacIntosh AJ, Frias L
  • Journal Title: Parasites of apes: an atlas of coproscopic diagnostics Volume: 1
  • Int'l Joint Research
• [Journal Article] Molecular characterization of nodule worm in a community of Bornean primates (2019)
  • Author(s): 1.Frias L, Stark DJ, Salgado Lynn M, Nathan S, Goossens B, Okamoto M, MacIntosh AJJ
  • Journal Title: Ecology and Evolution Volume: 9 Issue: 7 Pages: 3937-3945
  • DOI: 10.1002/ece3.5022
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] A pinworm’s tale: the evolutionary history of Lemuricola (Protenterobius) nycticebi (2019)
  • Author(s): 3.Frias L, Hasegawa H, Stark DJ, Salgado-Lynn M, Nathan KSS Senthilvel, Chua T, Goossens B, Okamoto M, MacIntosh AJJ
  • Journal Title: International Journal for Parasitology: Parasites and Wildlife Volume: 8 Pages: 25-32
  • DOI: 10.1016/j.ijppaw.2018.11.009
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Lurking in the dark: Cryptic Strongyloides in a Bornean slow loris (2018)
  • Author(s): Frias Liesbeth、Stark Danica J.、Lynn Milena Salgado、Nathan Senthilvel KSS.、Goossens Benoit、Okamoto Munehiro、MacIntosh Andrew J.J.
  • Journal Title: International Journal for Parasitology: Parasites and Wildlife Volume: 7 Issue: 2 Pages: 141-146
  • DOI: 10.1016/j.ijppaw.2018.03.003
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure. (2018)
  • Author(s): Balasubramaniam, K. N., Beisner, B. A., Berman, C. M., de Marco, A., Duboscq, J., Koirala, S., Majolo, B., MacIntosh, A. J. J., McFarland, R., Molesti, S., Ogawa, H., Petit, O., Schino, G., Sosa, S., Sueur, C., Thierry, B., de Waal, F. B. M, & McCowan, B. J.
  • Journal Title: American Journal of Primatology Volume: 80(1) Issue: 1
  • DOI: 10.1002/ajp.22727
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Complexity in behavioural organization and strongylid infection among wild chimpanzees (2017)
  • Author(s): Burgunder J.、Paf?o B.、Petr?elkov? K.J.、Modr? D.、Hashimoto C.、MacIntosh A.J.J.
  • Journal Title: Animal Behaviour Volume: 129 Pages: 257-268
  • DOI: 10.1016/j.anbehav.2017.06.002
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] One step at a time in investigating relationships between self-directed behaviours and parasitological, social and environmental variables (2017)
  • Author(s): Duboscq Julie、Romano Val?ria、Sueur C?dric、MacIntosh Andrew J. J.
  • Journal Title: Royal Society Open Science Volume: 4 Issue: 8 Pages: 170461-170461
  • DOI: 10.1098/rsos.170461
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Shallow divers, deep waters and the rise of behavioural stochasticity (2017)
  • Author(s): Meyer Xavier、MacIntosh Andrew J. J.、Chiaradia Andre、Kato Akiko、Mattern Thomas、Sueur C?dric、Ropert-Coudert Yan
  • Journal Title: Marine Biology Volume: 164 Issue: 6 Pages: 149-149
  • DOI: 10.1007/s00227-017-3177-y
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Avoidance of biological contaminants through sight, smell and touch in chimpanzees (2017)
  • Author(s): Sarabian Cecile、Ngoubangoye Barthelemy、MacIntosh Andrew J. J.
  • Journal Title: Royal Society Open Science Volume: 4 Issue: 11 Pages: 170968-170968
  • DOI: 10.1098/rsos.170968
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Coevolution of Hosts and Parasites (2017)
  • Author(s): MacIntosh AJJ, Frias L
  • Journal Title: The Encyclopedia of Primatology Volume: 1 Pages: 1-8
  • DOI: 10.1002/9781119179313.wbprim0395
  • Int'l Joint Research
• [Journal Article] Pathogen (2017)
  • Author(s): MacIntosh AJJ
  • Journal Title: The Encyclopedia of Primatology Volume: 1 Pages: 1-3
  • DOI: 10.1002/9781119179313.wbprim0106
  • Int'l Joint Research
• [Journal Article] Social information transmission in animals: Lessons from studies of diffusion (2016)
  • Author(s): Duboscq J, Romano V, MacIntosh A, Sueur C
  • Journal Title: Frontiers in Psychology Volume: 7 Pages: 1147-1147
  • DOI: 10.3389/fpsyg.2016.01147
  • NAID: 120005980814
  • Peer Reviewed / Open Access / Int'l Joint Research / Acknowledgement Compliant
• [Journal Article] Testing for links between face color and age, dominance status, parity, weight, and intestinal nematode infection in a sample of female Japanese macaques (2016)
  • Author(s): Rigaill L, MacIntosh AJJ, Higham JP, Winters S, Shimizu K, Mouri K, Suzumura T, Furuichi T, Garcia C
  • Journal Title: Primates Volume: 58 Issue: 1 Pages: 83-91
  • DOI: 10.1007/s10329-016-0575-6
  • Peer Reviewed / Int'l Joint Research / Acknowledgement Compliant
• [Journal Article] Scratch that itch: revisiting links between self-directed behaviour and parasitological, social and environmental factors in a free-ranging primate. (2016)
  • Author(s): Duboscq J, Romano V, Sueur C, MacIntosh AJJ
  • Journal Title: Royal Society Open Science Volume: 3 Issue: 11 Pages: 160571-160571
  • DOI: 10.1098/rsos.160571
  • NAID: 120005973377
  • Peer Reviewed / Open Access / Int'l Joint Research / Acknowledgement Compliant
• [Presentation] Prevalence of cryptosporidium and giardia infection in long tailed macaques and proboscis monkeys in the lower Kinabatangan floodplain (2019)
  • Author(s): Surdensteeve Peter, Noor Haliza Hasan, Liesbeth Frias, Andrew J. J MacIntosh
  • Organizer: The 11th International Symposium on Primatology and Wildlife Science
  • Int'l Joint Research
• [Presentation] Behavioral ecology and epidemiology of gastrointestinal parasitism in primates: patterns, processes and host responses (2019)
  • Author(s): Andrew MacIntosh
  • Organizer: Czech Academy of Science
  • Invited
• [Presentation] Monkeys in the middle: towards organisational immunity in primate societies (2017)
  • Author(s): MacIntosh AJJ, Romano V, Duboscq J, Sueur C
  • Organizer: Royal Society Scientific Meeting on the Evolution of parasite and pathogen avoidance
  • Int'l Joint Research / Invited
• [Presentation] Monkeys in the middle: sociality and parasitism in a primate-helminth model system (2017)
  • Author(s): MacIntosh AJJ
  • Organizer: Primatology and Evolutionary Anthropology Young Scholars Forum, Sun Yat Sen University
  • Invited
• [Presentation] Parasites and primate social systems evolution (2017)
  • Author(s): MacIntosh AJJ
  • Organizer: SoHaPi Workshop, German Primate Center
  • Invited
• [Presentation] From the darkness: cryptic diversity of Strongyloides in a community of Bornean primates (2017)
  • Author(s): Frias L, Okamoto M, MacIntosh AJJ
  • Organizer: 66th Annual International Conference of the Wildlife Disease Association
  • Int'l Joint Research
• [Presentation] Modeling the evolution of social structure: from individual decisions to group-living trade-offs (2017)
  • Author(s): Romano V., Puga-Gonzalez I., Sueur C., MacIntosh AJJ
  • Organizer: XI. Göttinger Freilandtage - Social complexity: patterns, processes and evolution
  • Int'l Joint Research
• [Presentation] How do you choose your friends? – The trade-off between information and pathogen transmission (2017)
  • Author(s): Romano V., MacIntosh AJJ, Sueur C
  • Organizer: Seminar on Ecology and Natural Resources. UENF
  • Invited
• [Presentation] Connecting the dots: linking host behaviour to parasite transmission and infection risk (2017)
  • Author(s): Duboscq J. & MacIntosh A
  • Organizer: 7th meeting of the European Federation for Primatology
  • Int'l Joint Research / Invited
• [Presentation] Infection patterns of simian foamy virus in macaques (2017)
  • Author(s): Duboscq, J., Okamoto, M., & MacIntosh, A
  • Organizer: 7th meeting of the European Federation for Primatology
  • Int'l Joint Research
• [Presentation] Infection patterns of simian foamy virus in macaques (2017)
  • Author(s): Duboscq, J., Okamoto, M., & MacIntosh, A
  • Organizer: meeting of the French Society of the Study of Animal Behaviour
  • Int'l Joint Research
• [Presentation] Diving into complexity: exploring fractality in seabird foraging behavior (2016)
  • Author(s): MacIntosh AJJ, Meyer X, Kato A, Ropert-Coudert Y
  • Organizer: The Seventh Symposium on Polar Science
  • Place of Presentation: National Institute of Polar Research, Tachikawa, Japan
  • Year and Date: 2016-11-29
  • Int'l Joint Research / Invited
• [Presentation] Parasite sharing as a preliminary indicator of multispecies connectivity (2016)
  • Author(s): Frias L, Okamoto M, MacIntosh A
  • Organizer: 12th Conference of the European Wildlife Disease Association
  • Place of Presentation: Berlin, Germany
  • Year and Date: 2016-08-27
  • Int'l Joint Research
• [Presentation] Towards a primate parasite community ecology: parasite sharing in sympatric Bornean primates (2016)
  • Author(s): Frias L, Okamoto M, MacIntosh A
  • Organizer: The 26th Congress of the International Primatological Society
  • Place of Presentation: Chicago, USA
  • Year and Date: 2016-08-21
  • Int'l Joint Research
• [Presentation] A primate's sense of cleanliness: perspectives from Papionini and Hominini (2016)
  • Author(s): Sarabian C, MacIntosh AJJ
  • Organizer: The 26th Congress of the International Primatological Society
  • Place of Presentation: Chicago, USA
  • Year and Date: 2016-08-21
  • Int'l Joint Research
• [Presentation] Parasites as a selective force in primate social systems evolution: perspectives from an empirical model (2016)
  • Author(s): MacIntosh AJJ, Sarabian C, Duboscq J, Romano V, Kaneko A, Okamoto M, Suzumura T
  • Organizer: The 26th Congress of the International Primatological Society
  • Place of Presentation: Chicago, USA
  • Year and Date: 2016-08-21
  • Int'l Joint Research
• [Presentation] Helminth parasites as potential regulators of Japanese macaque population dynamics (2016)
  • Author(s): MacIntosh AJJ, Sarabian C, Duboscq J, Romano V, Kaneko A, Okamoto M, Suzumura T
  • Organizer: The 26th Congress of the International Primatological Society
  • Place of Presentation: Chicago, USA
  • Year and Date: 2016-08-21
  • Int'l Joint Research
• [Presentation] Behavioral Organization and Parasites in Japanese Macaques (Macaca fuscata) on Koshima Island (2016)
  • Author(s): Finn K, MacIntosh A
  • Organizer: The 26th Congress of the International Primatological Society
  • Place of Presentation: Chicago, USA
  • Year and Date: 2016-08-21
  • Int'l Joint Research
• [Presentation] Chaotic choice dynamics buffer chimpanzees and orangutans against exploitation by a computer algorithm in a solitary matching pennies task (2016)
  • Author(s): Martin C, MacIntosh AJJ
  • Organizer: The 26th Congress of the International Primatological Society
  • Place of Presentation: Chicago, USA
  • Year and Date: 2016-08-21
  • Int'l Joint Research
• [Presentation] Revulsion in chimpanzees: health maintenance through avoidance of biological contaminants (2016)
  • Author(s): Sarabian C, MacIntosh AJJ
  • Organizer: Chimpanzees in Context, 'Understanding Chimpanzees' Symposium Series
  • Place of Presentation: Chicago, USA
  • Year and Date: 2016-08-18
  • Int'l Joint Research
• [Presentation] Testing disgust in non-human primates (2016)
  • Author(s): Sarabian C, MacIntosh AJJ
  • Organizer: The 31st International Congress of Psychology
  • Place of Presentation: Yokohama, Japan
  • Year and Date: 2016-07-24
  • Int'l Joint Research
• [Presentation] Gastrointestinal parasite sharing in multi-host primate communities (2016)
  • Author(s): Frias L, Okamoto M, MacIntosh A
  • Organizer: 13th International Conference on Molecular Epidemiology and Evolutionary Genetics of Infectious Diseases
  • Place of Presentation: Antwerp, Belgium
  • Year and Date: 2016-05-11
  • Int'l Joint Research
• [Presentation] Project l'AMMER: Adelie Penguins as Monitors of the Marine Environment (2016)
  • Author(s): MacIntosh AJJ
  • Organizer: National Institute of Ecology Seminar Series
  • Place of Presentation: National Institute of Ecology, South Korea
  • Invited
• [Presentation] The Wormy World of Primates: Vignettes from an Empirical Model System in Japan (2016)
  • Author(s): MacIntosh AJJ
  • Organizer: National Institute of Ecology Seminar Series
  • Place of Presentation: National Institute of Ecology, South Korea
  • Invited
• [Remarks] MacIntosh Lab | Research
  • URL: https://www.macintoshlab.com/hosts-parasites-ecosystems
• [Remarks] Academic Website for Andrew MacIntosh
  • URL: http://www.cicasp.pri.kyoto-u.ac.jp/people/andrew-macintosh
• [Remarks] The PrimateCast
  • URL: http://theprimatecast.com/
• [Remarks] The PrimateCast
  • URL: http://www.theprimatecast.com