Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection

BMC Ecology

Volumn 11, Issue , 2011, Pages

  Hughes, David P ^a,b   Andersen, Sandra B ^b   Hywel Jones, Nigel L ^c   Himaman, Winanda ^d   Billen, Johan ^e   Boomsma, Jacobus J ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^d DEPARTMENT OF NATIONAL PARKS   (Thailand)

^e UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Ants; Behavioral manipulation; Convergent evolution; Extended phenotype; Fungi; Parasites

Indexed keywords

ANT; CONVERGENT EVOLUTION; FUNGAL DISEASE; GENOME; HISTOLOGY; MORPHOLOGY; MORTALITY; PARASITIC DISEASE; PHENOTYPE; STEREOTYPIC BEHAVIOR;

CAMPONOTUS LEONARDI; FORMICIDAE; FUNGI;

ANIMAL; ANIMAL BEHAVIOR; ANT; ARTICLE; HOST PARASITE INTERACTION; HYPOCREALES; MICROBIOLOGY; MYCOSIS; PATHOPHYSIOLOGY; PHYSIOLOGY; THAILAND;

ANIMALS; ANTS; BEHAVIOR, ANIMAL; HOST-PARASITE INTERACTIONS; HYPOCREALES; MYCOSES; THAILAND;

EID: 79955678351     PISSN: None     EISSN: 14726785     Source Type: Journal    
DOI: 10.1186/1472-6785-11-13     Document Type: Article

References (34)

1. Moore J. Parasites and the behavior of animals. 2002, Oxford: Oxford University Press.
2. Lafferty K, Kuris AM. Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology 2009, 25(12):564-572. 10.1016/j.pt.2009.09.003, 19800291.
3. Poulin R. Progenesis and reduced virulence as an alternative transmission strategy in a parasitic trematode. Parasitology 2001, 123:623-630.
4. Lefevre T, Adamo SA, Biron DG, Misse D, Hughes D, Thomas F. Invasion of the Body Snatchers: the diversity and evolution of manipulative strategies in host-parasite interactions. Advances in Parasitology 2009, 68:45-83.
5. Dawkins R. The extended phenotype. 1982, Oxford: W.H. Freeman.
6. Rogers ME, Bates PE. Leishmania manipulation of sand fly feeding behavior results in enhanced transmission. Plos Pathogens 2007, 3(6):e91. 10.1371/journal.ppat.0030091, 1904410, 17604451.
7. Eberhard WG. Spider manipulation by a wasp larva. Nature 2000, 406(6793):255-256. 10.1038/35018636, 10917517.
8. Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, et al. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 2008, 454(7203):515-518. 10.1038/nature06970, 18650923.
9. Thomas F, Adamo S, Moore J. Parasitic manipulation: where are we and where should we go?. Behavioural Processes 2005, 68(3):185-199. 10.1016/j.beproc.2004.06.010, 15792688.
10. Hughes DP, Kronauer DJC, Boomsma JJ. Extended Phenotype: Nematodes turn ants into bird-dispersed fruits. Current Biology 2008, R294-295.
11. Poulin R. The evolution of parasite manipulation of host behavior: a theoretical analysis. Parasitology 1994, 109:S109-S118. 10.1017/S0031182000085127, 7854845.
12. Poulin R. Manipulation of host behaviour by parasites: a weakening paradigm?. Proceedings of the Royal Society of London Series B 2000, 267(1445):787-792. 10.1098/rspb.2000.1072, 1690597, 10819148.
13. Dawkins R. Parasites, desiderata lists and the paradox of the organism. Parasitology 1990, 100:S63-S73. 10.1017/S0031182000073029, 2235064.
14. Sanchez MI, Ponton F, Schmidt-Rhaesa A, Hughes DP, Misse D, Thomas F. Two steps to suicide in crickets harbouring hairworms. Animal Behaviour 2008, 76:1621-1624.
15. Evans HC. Entomogenous fungi in the tropical forest ecosystems: an appraisal. Ecological Entomology 1982, 7:47-60.
16. Evans HC, Samson RA. Cordyceps species and their anamorphs pathogenic on ants (Formicidae) in tropical forest ecosystems. II. The Camponotus (Formicinae) complex. Transactions of the British Mycolocical Society 1984, 82:127-150.
17. Van Pelt A. The occurrence of a Cordyceps on the ant Camponotus pennsylvanicus (De Geer) in the Highlands, N.C. region. Journal of the Tennesee Academy of Sciences 1958, 33(120-122).
18. Hughes DP, Evans HC, Hywel-Jones NL, Boomsma JJ, Armitage SAO. Novel fungal disease in complex leaf-cutting ant societies. Ecological Entomology 2009, 34(2):214-220.
19. Hölldobler B, Wilson EO. The ants. 1990, Cambridge, Mass.: Harvard University Press.
20. Andersen SB, Gerritsma S, Yusah KM, Mayntz D, Hywel-Jones NL, Billen J, Boomsma JJ, Hughes DP. The life of a dead ant: the expression of an adaptive extended phenotype. American Naturalist 2009, 174(3):424-433. 10.1086/603640, 19627240.
21. Kuris AM. Trophic interactions: similarity of parasitic castrators to parasitoids. Quarterly Review of Biology 1974, 49:129-148.
22. Evans HC, Samson RA. Cordyceps species and their anamorph pathogenic on ants (Formicidae) in tropical forest ecosystems. I. The Cephalotes (Myrmicinae) complex. Transactions of the British Mycolocical Society 1982, 79:431-453.
23. Pontoppidan M-B, Himaman W, Hywel-Jones NL, Boomsma JJ, Hughes DP. Graveyards on the move: the spatio-temporal distribution of dead Ophiocordyceps-infected ants. PLoS ONE 2009, 4(3):e4835. 10.1371/journal.pone.0004835, 2652714, 19279680.
24. Sanjuán T, Guillermo Henao L, Amat G. Distribución espacial de Cordyceps spp. (Ascomycotina: Clavicipitaceae) y su impacto sobre las hormigas en selvas del piedemonte amazónico de Colombia. Revista de Biologia Tropical 2001, 49(3-4):945-955.
25. Evans HC. Natural control of Arthropods with special reference to ants (Formicidae) by fungi in the tropical high forest of Ghana. The Journal of Applied Ecology 1974, 11(1):37-49.
26. Hughes DP. Parasitic manipulation: a social context. Behavioural Processes 2005, (3):263-266.
27. Hughes DP. The extended phenotype within the colony and how it obscures social communication. Sociobiology of Communication: an interdisciplinary perspective 2008, Oxford Oxford University Press, d'Ettorre P, Hughes DP.
28. Hughes DP, Pierce NE, Boomsma JJ. Social insect symbionts: evolution in homeostatic fortresses. Trends in Ecology & Evolution 2008, 23(12):672-677. 10.1016/j.tree.2008.07.011, 21630111.
29. Pearson K. The problem of the random walk. Nature 1905, 72:342-342.
30. Fawcett W. Description of Cordyceps llyodii in ants. Annals and Magazine of Natural History 1886, 5(XVIII):317.
31. Marikovsky PI. On some features of behaviour of the ants Formica rufa L. infected with fungous disease. Insectes Sociaux 1962, 9(173-179).
32. Blair JE. Fungi. 2009, Oxford Oxford University Press.
33. Manga-Gonzalez MY, Gonzalez-Lanza C, Cabanas E, Campo R. Contributions to and review of dicrocoeliosis, with special reference to the intermediate hosts of Dicrocoelium dendriticum. Parasitology 2001, 123:S91-S114.
34. Evans HC, Elliot SL, Hughes DP. Hidden diversity behind the Zombie-ant fungus Ophiocordyceps unilateralis: Four new species described from Carpenter ants in Minas Gerais, Brazil. PLoS ONE 2011, 6(3):e17024. 10.1371/journal.pone.0017024, 3047535, 21399679.