Innate olfactory preferences in dung beetles

Journal of Experimental Biology

Volumn 213, Issue 18, 2010, Pages 3177-3186

  Dormont, Laurent ^a   Jay Robert, Pierre ^b   Bessière, Jean Marie ^c   Rapior, Sylvie ^d   Lumaret, Jean Pierre ^b  

^a CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^b UNIVERSITÉ PAUL VALÉRY   (France)

^c INSTITUT CHARLES GERHARDT   (France)

^d UNIV MONTPELLIER   (France)

Author keywords

Agrilinus constans; Coprophagous; Dung; Larval diet; Olfaction

Indexed keywords

VOLATILE ORGANIC COMPOUND;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BEETLE; CATTLE; CHEMISTRY; COPROPHAGY; FECES; FOOD PREFERENCE; HORSE; LARVA; METABOLISM; ODOR; PHYSIOLOGY; SHEEP; SWINE;

ANIMALS; BEETLES; BEHAVIOR, ANIMAL; CATTLE; COPROPHAGIA; FECES; FOOD PREFERENCES; HORSES; LARVA; ODORS; SHEEP; SMELL; SWINE; VOLATILE ORGANIC COMPOUNDS;

AGRILINUS; BOS; COLEOPTERA; EQUIDAE; HEXAPODA; MAMMALIA; OVIS ARIES; SUS SCROFA;

EID: 77956363834     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.040964     Document Type: Article

References (58)

1. Aguiar, R. and Wink, M. (2005). Do naive ruminants degrade alkaloids in the rumen? J. Chem. Ecol. 31, 761-787.
2. Aii, T., Yonaga, M. and Tanaka, H. (1980). Changes in headspace volatiles of feed in the digestive tracts of cattle. Nippon S. Ochi Gakkaishi 26, 223-230.
3. Arnould, C., Malosse, C., Signoret, J.-P. and Descoins, C. (1998). Which chemical constituents from dog feces are involved in its food repellent effect in sheep? J. Chem. Ecol. 24, 559-575.
4. Barron, A. B. (2001). The life and death of Hopkins' host-selection principle. J. Insect Behav. 14, 725-737.
5. Barron, A. B. and Corbet, S. A. (1999). Preimaginal conditioning in Drosophila revisited. Anim. Behav. 58, 621-628.
6. Bazemore, R., Wysocki, C. J., Murray, S., Lawley, H. J. and Preti, G. (2000). Amelioration of odorous components in spent mushroom compost. J. Agric. Food Chem. 48, 3694-3697.
7. Bicudo, J. R., Schmidt, D. R., Powers, W., Zahn, J. A., Tengman, C. L., Clanton, C. J. and Jacobson, L. D. (2002). Odor and VOC emissions from swine manure storages. In Proceedings of the Water Environment Federation, Odors and Toxic Air Emissions 2002, pp. 123-135. Albuquerque: Water Environment Federation.
8. Chow, J. K., Akhtar, Y. and Isman, M. B. (2005). The effects of larval experience with a complex plant latex on subsequent feeding and oviposition by the cabbage looper moth: Trichoplusia ni (Lepidoptera: Noctuidae). Chemoecol. 15, 129-133.
9. Corbet, S. A. (1985). Insect chemosensory responses-a chemical legacy hypothesis. Ecol. Entomol. 10, 143-153.
10. Cunningham, J. P., Moore, C. J., Zalucki, M. P. and West, S. A. (2004). Learning, odour preference and flower foraging in moths. J. Exp. Biol. 207, 87-94.
11. Cunningham, J. P., Moore, C. J., Zalucki, M. P. and Cribb, B. W. (2006). Insect odour perception: recognition, of odour components by flower foraging moths. Proc. R. Soc. Lond. B. Biol. Sci. 273, 2035-2040.
12. Dormont, L. and Roques, A. (2001). Why are seed cones of Swiss stone pine (Pinus cembra) not attacked by the specialized pine cone weevil, Pissodes validirostris? A case of host selection vs host suitability. Entomol. Exp. Appl. 99, 157-163.
13. Dormont, L., Epinat, G. and Lumaret, J.-P. (2004). Trophic preferences mediated by olfactory cues in dung beetles colonizing cattle and horse dung. Environ. Entomol. 33, 370-377.
14. Dormont, L., Rapior, S., McKey, D. and Lumaret, J.-P. (2007). Influence of dung volatiles on the process of resource selection by coprophagous beetles. Chemoecol. 17, 23-30.
15. Du, Y. J., Poppy, G. M., Powell, W. and Wadhams, L. J. (1997). Chemically mediated associative learning in the host foraging behaviour of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae). J. Insect Behav. 10, 509-522.
16. Dukas, R. (2008). Evolutionary biology of insect learning. Annu. Rev. Entomol. 53, 145-160.
17. Fan, R. J., Anderson, P. and Hansson, B. S. (1997). Behavioural analysis of olfactory conditioning in the moth Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae). J. Exp. Biol. 200, 2969-2976.
18. Finn, J. and Giller, P. S. (2002). Experimental investigations of colonisation by North temperate dung beetles of different types of domestic herbivore dung. Appl. Soil Ecol. 20, 1-13.
19. Galante, E. and Cartagena, C. (1999). Comparison of Mediterranean dung beetles (Coleoptera: Scarabaeoidea) in cattle and rabbit dung. Environ. Entomol. 28, 420-424.
20. Gandolfi, M., Mattiacci, L. and Dorn, S. (2003). Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp. Proc. R. Soc. Lond. B. Biol. Sci. 270, 2623-2629.
21. Garner, C. E., Smith, S., de Lacy Costello, B., White, P., Spencer, R., Probert, C. S. J. and Ratcliffe, N. M. (2007). Volatile organic compounds from feces and their potential for diagnosis of gastrointestinal disease. FASEB J. 21, 1675-1688.
22. Gibernau, M., Macquart, D. and Przetak, G. (2004). Pollination in the genus Arum - a review. Aroideana 27, 148-166.
23. Giurfa, M. (2007). Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J. Comp. Physiol. A 193, 801-824.
24. Hanski, I. and Cambefort, Y. (1991). Dung Beetle Ecology. Princeton, NJ: Princeton University Press.
25. Hempel, H., Scheffczyk, A., Schallnaß, H.-J., Lumaret, J.-P., Alvinerie, M. and Römbke, J. (2006). Toxicity of four veterinary parasiticides on larvae of the dung beetle Aphodius constans in the laboratory. Environ. Toxicol. Chem. 25, 3155-3163.
26. Hirschberger, P. and Degro, H. N. (1996). Oviposition of the dung beetle Aphodius ater in relation to the abundance of yellow dungfly larvae (Scatophaga stercoraria). Ecol. Entomol. 21, 352-357.
27. Hobbs, P. J., Misselbrook, T. H. and Cumby, T. R. (1999). Production and emission of odours and gases from ageing pig waste. J. Agric. Eng. Res. 72, 291-298.
28. Inouchi, J., Shibuya, T. and Hatanaka, T. (1988). Food odor responses of single antennal olfactory cells in the Japanese dung beetle, Geotrupes auratus (Coleoptera: Geotrupidae). Appl. Entomol. Zool. 23, 167-174.
29. Jaenike, J. (1988). Effects of early adult experience on host-selection in insects: some experimental and theoretical results. J. Insect Behav. 1, 3-15.
30. Jørgensen, K., Stranden, M., Sandoz, J.-C., Menzel, R. and Mustaparta, H. (2007). Effects of two bitter substances on olfactory conditioning in the moth Heliothis virescens. J. Exp. Biol. 210, 2563-2573.
31. Kalinova, B., Podskalska, H., Ruzicka, J. and Hoskovec, M. (2009). Irresistible bouquet of death - or how are burying beetles (Coleoptera, Silphidae: Nicrophorus) attracted by carcasses. Naturwissenschafen 96, 889-899.
32. Kelber, A. (2002). Pattern discrimination in a hawkmoth: innate preferences, learning performance and ecology. Proc. R. Soc. Lond. B. Biol. Sci. 269, 2573-2577.
33. King, R. A., May, B. L., Davies, D. A. and Bird, A. R. (2009). Measurement of phenol and p-cresol in urine and feces using vacuum microdistillation and high-performance liquid chromatography. Anal. Biochem. 384, 27-33.
34. Kite, G. C. (1995). The floral odour of Arum maculatum. Biochem. Syst. Ecol. 23, 343-354.
35. Knudsen, J. T., Eriksson, R. and Gershenzon, J. (2006). Diversity and distribution of floral scent. Bot. Rev. 72, 1-120.
36. Lumaret, J.-P. (1975). Etude des conditions de ponte et de développement larvaire d'Aphodius (Agrilinus) constans Duft. (Coléoptère, Scarabaeidae) dans la nature et au laboratoire. Vie et Milieu 25, 267-282.
37. Lumaret, J.-P. (1990). Atlas des Scarab́ides Laparosticti de France. In Śries Inventaire de Faune et de Flore, fasc 1. F. Paris: Secŕtariat Faune-Flore/MNHN.
38. Lumaret, J.-P. and Iborra, O. (1996). Separation of trophic niches by dung beetles (Coleoptera: Scarabaeoidea) in overlapping habitats. Pedobiology 40, 392-404.
39. Lumaret, J.-P., Alvinerie, M., Hempel, H., Schallnab, H.-J., Claret, D. and Römbke, J. (2007). New screening test to predict the potential impact of ivermectincontamined cattle dung on dung beetles. Vet. Res. 38, 15-24.
40. Martin-Piera, F. and Lobo, J. M. (1996). A comparative discussion of the trophic preferences in dung beetle communities. Misc. Zool. 19, 13-31.
41. Monroe, L. S. (1985). Fecal analysis. In Bockus Gastroenterology, 4th edn, Vol.1 (ed. J. E. Berk), pp. 350-363. Philadelphia: W. B. Saunders Co.
42. Moore, J. G., Jessop, L. D. and Osborne, D. N. (1987). Gas-chromatographic and mass-spectrometric analysis of the odour of human feces. Gastroenterology 93, 1321-1329.
43. Murphey, R. M., Bahre, C. J., Penedo, M. C. and Webster, G. L. (1981). Foraging differences in cattle: fecal analysis of three racial categories in a harsh environment. Behav. Genet. 11, 385-394.
44. O'Neill, D. H. and Phillips, V. R. (1992). A review of the control of odour nuisance from livestock buildings. Part 3, properties of the odorous substances which have been identified in livestock wastes or in the air around them. J. Agric. Eng. Res. 53, 23-50.
45. Prins, R. A. (1977). Biochemical activities of gut microorganisms. In Microbial Ecology of the Gut (ed. R. T. J. Clarke and T. Bauchop), pp. 173-183. New York: Academic Press.
46. Raguso, R. A. and Willis, M. A. (2002). Synergy between visual and olfactory cues in nectar feeding by naive hawkmoths, Manduca sexta. Anim. Behav. 64, 685-695.
47. Rietdorf, K. and Steidle, J. L. M. (2002). Was Hopkins right? Influence of larval and early adult experience on the olfactory response in the granary weevil Sitophilus granarius (Coleoptera, Curculionidae). Physiol. Entomol. 27, 223-227.
48. Riffell, J. A., Alarcó n, R., Abrell, L., Davidowitz, G., Bronstein, J. L. and Hildebrand, J. G. (2008). Behavioral consequences of innate preferences and olfactory learning in hawkmoth-flower interactions. Proc. Natl. Acad. Sci. USA 105, 3404-3409.
49. Riveros, A. J. (2009). Olfactory learning and memory in the bumblebee Bombus occidentalis. Naturwissenschafen 96, 851-856.
50. Römbke, J., Hempel, H., Scheffczyk, A., Schallnass, H.-J., Alvinerie, M. and Lumaret, J.-P. (2007). Environmental risk assessment of veterinary pharmaceuticals: development of standard laboratory test with the dung beetle Aphodius constans. Chemosphere 70, 57-64.
51. Sato, H., Hirose, T., Kimura, T., Moriyama, Y. and Nakashima, Y. (2001). Analysis of malodorous volatile substances of human waste: feces and urine. J. Health Sci. 47, 483-490.
52. Schoonhoven, L. M., Jermey, T. and van Loon, J. A. (1998). Insect-Plant Biology: from Physiology to Evolution. London: Chapman and Hall.
53. Scott, M. P. (1998). The ecology and behavior of burying beetles. Annu. Rev. Entomol. 43, 595-618.
54. Smith, D., Spanel, P. and Jones, J. B. (2000). Analysis of volatile emissions from porcine faeces and urine using selected ion flow tube mass spectrometry. Biores. Technol. 75, 27-33.
55. Smith, M. A. and Cornell, H. V. (1979). Hopkins host-selection in Nasonia vitripennis and its implications for sympatric speciation. Anim. Behav. 27, 365-370.
56. Suarez, F. L., Springfield, J. and Levitt, M. D. (1998). Identification of gases responsible for the odour of human flatus and evaluation of a device purported to reduce this odour. Gut 43, 100-104.
57. Turlings, T. C. J., Wackers, F. L., Vet, L. E. M., Lewis, W. J. and Tumlinson, J. H. (1993). Learning of host-finding cues by hymenopterous parasitoids. In Insect Learning. Ecological and Evolutionary Perspectives (ed. D. R. Papaj and A. C. Lewis), pp. 51-78. New York: Chapman and Hall.
58. Wright, G. A., Mustard, J. A., Kottcamp, S. M. and Smith, B. H. (2007). Olfactory memory formation and the influence of reward pathway during appetitive learning by honey bees. J. Exp. Biol. 210, 4024-4033.