Journal of Insect Behavior

, Volume 25, Issue 4, pp 352–361 | Cite as

Parasites and Dung Beetles as Ecosystem Engineers in a Forest Ecosystem

  • Broox G. V. BozeEmail author
  • Alexander D. Hernandez
  • Michael A. Huffman
  • Janice Moore


Dung beetles serve as the intermediate host for Streptopharagus pigmentatus, a nematode parasite that infects an old world primate, the Japanese Macaque (Macaca fuscata). This study compares the behaviors of infected and uninfected beetles in both transmission dynamics and the ecological role of the parasite. The results suggest that parasitism does not alter the beetle’s use of shelter or choice of substrate on Yakushima Island, Japan. However, infected beetles consume significantly less feces. Dung beetles remove the majority of fecal material in this forest ecosystem, eliminating breeding grounds for many insect pests and burying nutrients that are essential for plant health. Thus, the nematode parasite S. pigmentatus, by altering its host’s behavior, changes the availability of fecal resources to both plant and animal communities and should therefore be classified as an ecosystem engineer.


Dung beetle nematode behavioral modification ecosystem engineer Yakushima 



Financial support for this study was provided the National Science Foundation and Japanese Society for the Promotion of Science’s East Asia and Pacific Summer Institute. The National Science Foundation also provided funding for Broox Boze through the Alliance for Graduate Education and the Professoriate program.


  1. Bryan RP (1973) The effects of dung beetle activity on numbers of parasitic gastrointestinal helminth larvae recovered from pasture samples. Aust J Agric Res 24(1):161–168CrossRefGoogle Scholar
  2. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology in its own terms: Margolis et al. revisited. Journal of Parasitology 83(4):575–583Google Scholar
  3. De Oca EM (1998) Invasion of Mexico by two dung beetles previously introduced into the United States. Stud Neotrop Fauna Environ 33(1):37–45CrossRefGoogle Scholar
  4. Estrada A, Anzures AD, Coates-Estrada R (1999) Tropical rain forest fragmentation, howler monkeys (Alouatta palliate), and dung beetles at Los Tuxtlas, Mexico. Am J Primatol 48(4):253–262PubMedCrossRefGoogle Scholar
  5. Fincher GT (1981) The potential value of dung beetles in pasture ecosystems. J Ga Entomol Soc 16(1):316–333Google Scholar
  6. Gotoh S (2000) Regional differences in the infection of wild Japanese macaques by gastrointestinal Helminth parasites. Primates 41(3):291–298CrossRefGoogle Scholar
  7. Halffter G, Matthews EG (1966) The natural history of dung beetles of the subfamily Scarabaeinae (Coleoptera: Scarabaeidae). Folia Entomologia Mexico 12–14:312Google Scholar
  8. Hanksi I, Cambefort Y (1991) Dung beetle ecology. Princeton University Press, PrincetonGoogle Scholar
  9. Hernandez AD, Sukhdeo MVK (2008) Parasite effects on isopod feeding rates can alter the host’s functional role in a natural stream ecosystem. Int J Parasitol 33:683–690CrossRefGoogle Scholar
  10. Hernandez AD, MacIntosh AJ, Huffman MA (2009) Primate parasite ecology: patterns and predictions from an on-going study of Japanese macaques. Cam S Bio Evol Anthr 57:387–401Google Scholar
  11. Jones CG (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957CrossRefGoogle Scholar
  12. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Okios 69(3):373–386CrossRefGoogle Scholar
  13. Kanda N, Yokota T, Shibata E, Sato H (2005) Diversity of dung-beetle community in declining subalpine forest caused by increasing deer population. Ecol Res 20(2):135–141CrossRefGoogle Scholar
  14. Lafferty KD, Allesina S, Arim M, Briggs CJ, DeLeo G, Dobson A, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546PubMedCrossRefGoogle Scholar
  15. Lafferty KD, Dobson A P, Kuris Armand M (2006) Parasite dominate food web links. Proceedings of the National Academy of Sciences of the United States of America 103:11211–11216Google Scholar
  16. Lefevre T, Lebarbenchon C, Gauthier-Clerc M, Misse D, Poulin R, Thomas F (2009) The ecological significance of manipulative parasites. Trends Ecol Evol 24(1):41–48PubMedCrossRefGoogle Scholar
  17. Losey JE, Vaughn M (2006) The economic value of ecological services provided by insects. BioScience 56(4):311–323CrossRefGoogle Scholar
  18. Machida M, Araki J, Koyama T, Kumada M, Horii Y, Imada I, Takasaka M, Honjo S, Matsubayashi K, Tiba T (1978) The life cycle of Streptopharagus pigmentatus (Nematoda, Spiruroidea) from the Japanese monkey. Bull Nat Sci Mus, Series A (Zoology) 4(1):1–9Google Scholar
  19. MacIntosh AJJ, Hernandez AD, Huffman MA (2010) Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese Macaques. Primates 51:353–364PubMedCrossRefGoogle Scholar
  20. MacIntosh AJJ, Alados CL, Huffman MA (2011) Fractal analysis of behavior in a wild primate: behavioural complexity in health and disease. J R Soc Interface. doi: 10.1098/rsif.2011.0049
  21. Moore J (2002) Parasites and the behavior of animals. In: May R, Murray P (eds) Oxford series in ecology and evolution. Oxford University Press, OxfordGoogle Scholar
  22. Nichols E, Spector S, Louzada J, Larsen T, Amezquita S, Favila ME, The Scarabaeinae Research Network (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biol Conserv 141:1461–1474CrossRefGoogle Scholar
  23. Sasayama K, Nakamura K, Kurohihi I (1984) Diurnal prevalence and seasonal change of dung beetles: relationships to weather elements. J Jpn Soc Grassl Sci 29(4):362–367Google Scholar
  24. Slade EM, Mann DJ, Villanueva JF, Lewis OT (2007) Experimental evidence for the effects of dung beetle functional group richness and composition on ecosystem function in a tropical forest. J Anim Ecol 76(6):1094–104PubMedCrossRefGoogle Scholar
  25. Tarnaud L, Yamagiwa J (2008) Age-dependent patterns of intensive observation on elders by free-ranging juvenile Japanese macaques (Macaca fuscata yakui) within foraging context on Yakushima. Am J Primatol 70:1103–1113PubMedCrossRefGoogle Scholar
  26. Thomas F, Poulin R, de Meeus T, Fuegan JF, Renaud F (1999) Parasites and ecosystem engineering: what roles could they play? Oikos 84(1):167–171CrossRefGoogle Scholar
  27. Thomas F, Adamo S, Moore J (2005) Parasitic manipulation: where are we and where should we go? Behav Process 68:185–199CrossRefGoogle Scholar
  28. Thompson RM, Mouritsen KN, Poulin R (2005) Importance of parasites and their life cycle characteristics in determining the structure of a large marine food web. Journal of Animal Ecology 74(1):77–85Google Scholar
  29. Yamagiwa J, Hill DA (1998) Intraspecific variation in the social organization of Japanese macaques: past and present scope of field studies in natural habitats. Primates 39(3):257–273CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Broox G. V. Boze
    • 1
    Email author
  • Alexander D. Hernandez
    • 2
    • 3
  • Michael A. Huffman
    • 2
  • Janice Moore
    • 1
  1. 1.Department of BiologyColorado State UniversityFort CollinsUSA
  2. 2.Department of Ecology and Social Behavior, Primate Research InstituteKyoto UniversityInuyamaJapan
  3. 3.Center for Infectious Disease DynamicsThe Pennsylvania State UniversityUniversity ParkUSA

Personalised recommendations