Microbes and animal olfactory communication: Where do we go from here?

BioEssays

Volumn 36, Issue 9, 2014, Pages 847-854

  Ezenwa, Vanessa O ^a   Williams, Allison E ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

Bacteria; Chemical signals; Microbes; Olfactory communication; Scent mark

Indexed keywords

ANIMAL COMMUNICATION; ARTICLE; HOST PATHOGEN INTERACTION; MICROORGANISM; NONHUMAN; ODOR; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TECHNOLOGY; WILD ANIMAL; ANAL SAC; ANIMAL; HUMAN; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; SCENT GLAND;

ANIMALIA;

PHEROMONE;

ANAL SACS; ANIMAL COMMUNICATION; ANIMALS; HUMANS; MICROBIOTA; ODORS; PHEROMONES; SCENT GLANDS;

EID: 84905906017     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201400016     Document Type: Article

References (84)

1. McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, et al. 2013. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110: 3229-36.
2. Clemente JC, Ursell LK, Parfrey LW, Knight R. 2012. The impact of the gut microbiota on human health: an integrative view. Cell 148: 1258-70.
3. Archie EA, Theis KR. 2011. Animal behaviour meets microbial ecology. Anim Behav 82: 425-36.
4. Ezenwa VO, Gerardo NM, Inouye DW, Medina M, et al. 2012. Animal behavior and the microbiome. Science 338: 198-9.
5. Albone ES, Eglinton G, Walker JM, Ware GC. 1974. The anal sac secretion of the red fox (Vulpes vulpes); its chemistry and microbiology. A comparison with the anal sac secretion of the lion (Panthera leo). Life Sci 14: 387-400.
6. Gorman M, Nedwell DB, Smith RM. 1974. An analysis of the contents of the anal scent pockets of Herpestes auropunctatus (Carnivora: Viverridae). J Zool 172: 389-99.
7. Gorman ML. 1976. A mechanism for individual recognition by odour in Herpestes auropunctatus (Carnivora: Viverridae). Anim Behav 24: 141-5.
8. Steiger S, Schmitt T, Schaefer HM. 2011. The origin and dynamic evolution of chemical information transfer. P Roy Soc Lond B Bio 278: 970-9.
9. Wyatt TD. 2014. Pheromones and Animal Behavior: Chemical Signals and Signature Mixes. New York, USA: Cambridge University Press.
10. Steiger S. 2012. New synthesis - visual and chemical ornaments: what researchers of different signal modalities can learn from each other. J Chem Ecol 38: 1.
11. Wyatt TD. 2003. Pheromones and Animal Behaviour: Communication by Smell and Taste. Cambridge, UK: Cambridge University Press.
12. Davis TS, Crippen TL, Hofstetter RW, Tomberlin JK. 2013. Microbial volatile emissions as insect semiochemicals. J Chem Ecol 39: 1-20.
13. Wyatt TD. 2009. Fifty years of pheromones. Nature 457: 262-3.
14. Douglas AE, Dobson AJ. 2013. New synthesis: animal communication mediated by microbes: fact or fantasy? J Chem Ecol 39: 1149.
15. Voigt CC, Caspers B, Speck S. 2009. Bats, bacteria, and bat smell: sex-specific diversity of microbes in a sexually selected scent organ. J Mammal 86: 745-59.
16. Hagey L, MacDonald E. 2003. Chemical cues identify gender and individuality in giant pandas (Ailuropoda melanoleuca). J Chem Ecol 29: 1479-88.
17. Sin YW, Buesching CD, Burke T, Macdonald DW. 2012. Molecular characterization of the microbial communities in the subcaudal gland secretion of the European badger (Meles meles). FEMS Microbiol Ecol 81: 648-59.
18. Zomer S, Dixon SJ, Xu Y, Jensen SP, et al. 2009. Consensus multivariate methods in gas chromatography mass spectrometry and denaturing gradient gel electrophoresis: MHC-congenic and other strains of mice can be classified according to the profiles of volatiles and microflora in their scent-marks. Analyst 134: 114-23.
19. Theis KR, Venkataraman A, Dycus JA, Koonter KD, et al. 2013. Symbiotic bacteria appear to mediate hyena social odors. Proc Natl Acad Sci USA 110: 19832-7.
20. Li Q, Korzan WJ, Ferrero DM, Chang RB, et al. 2013. Synchronous evolution of an odor biosynthesis pathway and behavioral response. Curr Biol 23: 11-20.
21. Dillon RJ, Vennard CT, Charnley AK. 2000. Pheromones: exploitation of gut bacteria in the locust. Nature 403: 851.
22. Dillon R, Vennard C, Charnley A. 2002. A note: gut bacteria produce components of a locust cohesion pheromone. J Appl Microbiol 92: 759-63.
23. Dillon RJ, Dillon VM. 2004. The gut bacteria of insects: nonpathogenic Interactions. Annu Rev Entomol 49: 71-92.
24. Brand J, Bracke J, Britton L, Markovetz A, et al. 1976. Bark beetle pheromones: production of verbenone by a mycangial fungus of Dendroctonus frontalis. J Chem Ecol 2: 195-9.
25. Brand J, Schultz J, Barras S, Edson L, et al. 1977. Bark-beetle pheromones. J Chem Ecol 3: 657-66.
26. Leufvén A, Bergström G, Falsen E. 1984. Interconversion of verbenols and verbenone by identified yeasts isolated from the spruce bark beetle Ips typographus. J Chem Ecol 10: 1349-61.
27. Hunt D, Borden J. 1990. Conversion of verbenols to verbenone by yeasts isolated from Dendroctonus ponderosae (Coleoptera: Scolytidae). J Chem Ecol 16: 1385-97.
28. Ruiz-Rodríguez M, Martínez-Bueno M, Martín-Vivaldi M, Valdivia E, et al. 2013. Bacteriocins with a broader antimicrobial spectrum prevail in enterococcal symbionts isolated from the hoopoe's uropygial gland. FEMS Microbiol Ecol 85: 495-502.
29. Soler JJ, Martín-Vivaldi M, Ruiz-Rodríguez M, Valdivia E, et al. 2008. Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Funct Ecol 22: 864-71.
30. Martín-Vivaldi M, Peña A, Peralta-Sánchez JM, Sánchez L, et al. 2010. Antimicrobial chemicals in hoopoe preen secretions are produced by symbiotic bacteria. Proc Biol Sci 277: 123-30.
31. Leclaire S, Merkling T, Raynaud C, Mulard H, et al. 2012. Semiochemical compounds of preen secretion reflect genetic make-up in a seabird species. Proc Biol Sci 279: 1185-93.
32. Zhang J-X, Wei W, Zhang J-H, Yang W-H. 2010. Uropygial gland-secreted alkanols contribute to olfactory sex signals in budgerigars. Chem Senses 35: 375-82.
33. Zhang Y-H, Du Y-F, Zhang J-X. 2013. Uropygial gland volatiles facilitate species recognition between two sympatric sibling bird species. Behav Ecol 24: 1271-8.
34. Ruiz-Rodríguez M, Valdivia E, Soler JJ, Martín-Vivaldi M, et al. 2009. Symbiotic bacteria living in the hoopoe's uropygial gland prevent feather degradation. J Exp Biol 212: 3621-6.
35. Hudson PJ, Dobson AP, Newborn D. 1998. Prevention of population cycles by parasite removal. Science 282: 2256-8.
36. Marzal A, De Lope F, Navarro C, Møller AP. 2005. Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142: 541-5.
37. Ezenwa VO, Etienne RS, Luikart G, Beja-Pereira A, et al. 2010. Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion in African buffalo. Am Nat 176: 613-24.
38. Goodwin TE, Broederdorf LJ, Burkert BA, Hirwa IH, et al. 2012. Chemical signals of elephant musth: temporal aspects of microbially-mediated modifications. J Chem Ecol 38: 81-7.
39. Robinson CJ, Bohannan BJ, Young VB. 2010. From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol R 74: 453-76.
40. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, et al. 2012. Diversity, stability and resilience of the human gut microbiota. Nature 489: 220-30.
41. Hooper D, Chapin 3rd F, Ewel J, Hector A, et al. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75: 3-35.
42. Allison SD, Martiny JB. 2008. Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA 105: 11512-9.
43. Nielsen U, Ayres E, Wall D, Bardgett R. 2011. Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity-function relationships. Eur J Soil Sci 62: 105-16.
44. Naeem S. 1998. Species redundancy and ecosystem reliability. Conserv Biol 12: 39-45.
45. Yachi S, Loreau M. 1999. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci USA 96: 1463-8.
46. Loreau M. 2010. Linking biodiversity and ecosystems: towards a unifying ecological theory. Philos T Roy Soc B 365: 49-60.
47. Ferrer M, Ruiz A, Lanza F, Haange SB, et al. 2013. Microbiota from the distal guts of lean and obese adolescents exhibit partial functional redundancy besides clear differences in community structure. Environ Microbiol 15: 211-26.
48. Burgener N, East M, Hofer H, Dehnhard M. 2008. Do Spotted Hyena Scent Marks Code for Clan Membership? Chemical Signals in Vertebrates 11. New York: Springer. p. 169-77.
49. Kruuk H, Gorman M, Leitch A. 1984. Scent-marking with the subcaudal gland by the European badger, Meles meles. Anim Behav 32: 899-907.
50. Buesching C, Stopka P, Macdonald D. 2003. The social function of allo-marking in the European badger (Meles meles). Behaviour 140: 965-80.
51. Koren O, Goodrich JK, Cullender TC, Spor A, et al. 2012. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150: 470-80.
52. Maynard Smith J, Harper D. 2003. Animal Signals. Oxford series in ecology and evolution. Oxford, UK: Oxford University Press.
53. Sharon G, Segal D, Ringo JM, Hefetz A, et al. 2010. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA 107: 20051-6.
54. Martín-Vivaldi M, Ruiz-Rodríguez M, José Soler J, Manuel Peralta-Sánchez J, et al. 2009. Seasonal, sexual and developmental differences in hoopoe Upupa epops preen gland morphology and secretions: evidence for a role of bacteria. J Avian Biol 40: 191-205.
55. van Dongen WF, White J, Brandl HB, Moodley Y, et al. 2013. Age-related differences in the cloacal microbiota of a wild bird species. BMC Ecol 13: 11.
56. Marino S, Baxter NT, Huffnagle GB, Petrosino JF, et al. 2014. Mathematical modeling of primary succession of murine intestinal microbiota. Proc Natl Acad Sci USA 111: 439-44.
57. Vandegrift KJ, Hudson PJ. 2009. Response to enrichment, type and timing: small mammals vary in their response to a springtime cicada but not a carbohydrate pulse. J Anim Ecol 78: 202-9.
58. Martínez-Padilla J, Pérez-Rodríguez L, Mougeot F, Ludwig S, et al. 2014. Intra-sexual competition alters the relationship between testosterone and ornament expression in a wild territorial bird. Horm Behav 65: 435-44.
59. Albone ES, Shirley SG. 1984. Mammalian Semiochemistry: The Investigation of Chemical Signals Between Mammals. Chichester: Wiley.
60. Albone ES, Perry GC. 1976. Anal sac secretion of the red fox, Vulpes vulpes; volatile fatty acids and diamines: implications for a fermentation hypothesis of chemical recognition. J Chem Ecol 2: 101-11.
61. Hepper PG. 1987. The discrimination of different degrees of relatedness in the rat: evidence for a genetic identifier? Anim Behav 35: 549-54.
62. Theis KR, Schmidt TM, Holekamp KE. 2012. Evidence for a bacterial mechanism for group-specific social odors among hyenas. Sci Rep 2: 615.
63. Leclaire S, Nielsen JF, Drea CM. 2014. Bacterial communities in meerkat anal scent secretions vary with host sex, age, and group membership. Behav Ecol, in press, doi: 10.1093/beheco/aru074.
64. Dzieciol M, Niżański W, Kozdrowski R, Ochota M, et al. 2013. The Influence of Experimentally Reduced Vaginal Flora in Oestrus Females on the Mating Behaviour of Male Domestic Dogs (Canis familiaris): Chemical Signals in Vertebrates 12. New York USA: Springer. p. 391-6.
65. Li G, Roze U, Locke DC. 1997. Warning odor of the North American porcupine (Erethizon dorsatum). J Chem Ecol 23: 2737-54.
66. Brown RE, Schellinck HM. 1992. Interactions among the MHC, diet and bacteria in the production of social odors in rodents. In Chemical Signals in Vertebrates 6. New York USA: Springer. p. 175-81.
67. Schellinck HM, Brown RE, Slotnick BM. 1991. Training rats to discriminate between the odors of individual conspecifics. Anim Learn Behav 19: 223-33.
68. Zechman JM, Martin IG, Wellington JL, Beauchamp GK. 1984. Perineal scent gland of wild and domestic cavies: bacterial activity and urine as sources of biologically significant odors. Physiol Behav 32: 269-74.
69. Svendsen GE, Jollick JD. 1978. Bacterial contents of the anal and castor glands of beaver (Castor canadensis). J Chem Ecol 4: 563-9.
70. Müller-Schwarze D, Heckman S. 1980. The social role of scent marking in beaver (Castor canadensis). J Chem Ecol 6: 81-95.
71. Sun L, Müller-Schwarze D. 1998. Anal gland secretion codes for family membership in the beaver. Behav Ecol Sociobiol 44: 199-208.
72. Sun L, Müller-Schwarze D. 1997. Sibling recognition in the beaver: a field test for phenotype matching. Anim Behav 54: 493-502.
73. Gassett J, Dasher K, Miller K, Osborn D, et al. 2000. White-tailed deer tarsal glands: sex and age-related variation in microbial flora. Mammalia 64: 371-8.
74. Alexy KJ, Gassett JW, Osborn DA, Miller KV, et al. 2003. Bacterial fauna of the tarsal tufts of white-tailed deer (Odocoileus virginianus). Am Midl Nat 149: 237-40.
75. Ungerfeld R, Silva L. 2005. The presence of normal vaginal flora is necessary for normal sexual attractiveness of estrous ewes. Appl Anim Behav Sci 93: 245-50.
76. Ziegler TE, Epple G, Snowdon CT, Porter TA, et al. 1993. Detection of the chemical signals of ovulation in the cotton-top tamarin, Saguinus oedipus. Anim Behav 45: 313-22.
77. MacDonald EA, Fernandez-Duque E, Evans S, Hagey LR. 2008. Sex, age, and family differences in the chemical composition of owl monkey (Aotus nancymaae) subcaudal scent secretions. Am J Primatol 70: 12-8.
78. Nordstrom KM, Belcher AM, Epple G, Greenfield KL, et al. 1989. Skin surface microflora of the saddle-back tamarin monkey, Saguinus fuscicollis. J Chem Ecol 15: 629-39.
79. Merritt G, Goodrich B, Hesterman E, Mykytowycz R. 1982. Microflora and volatile fatty acids present in inguinal pouches of the wild rabbit, Oryctolagus cuniculus, in Australia. J Chem Ecol 8: 1217-25.
80. Brand J, Bracke J, Markovetz A, Wood D, et al. 1975. Production of verbenol pheromone by a bacterium isolated from bark beetles. Nature 254: 136-7.
81. Hoyt C, Osborne G, Mulcock A. 1971. Production of an insect sex attractant by symbiotic bacteria. Nature 230: 472-3.
82. Chararas C, Riviere J, Ducauze C, Ruttledge D, et al. 1980. Bioconversion of a terpene compound under the action of a bacterium of the digestive tract of Phloeosinus armatus (Coleoptera, Scolytidae). CR Hebd Acad Sci 291: 299-302.
83. Lam K, Babor D, Duthie B, Babor E-M, et al. 2007. Proliferating bacterial symbionts on house fly eggs affect oviposition behaviour of adult flies. Anim Behav 74: 81-92.
84. Martín J, López P. 2006. Age-related variation in lipophilic chemical compounds from femoral gland secretions of male lizards Psammodromus algirus. Biochem System Ecol 34: 691-7.