Microbially Mediated Chemical Ecology of Animals: A Review of Its Role in Conspecific Communication, Parasitism and Predation
Abstract
:Simple Summary
Abstract
1. Introduction
2. Conspecific Chemical Communication Mediated by Bacterial Symbionts
3. Negative Effects of the Microbiome in Relation to Parasitism and Predation
4. Beneficial Effects of the Microbiome in Relation to Parasitism and Predation
5. Final Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- McFall-Ngai, M.; Hadfield, M.G.; Bosch, T.C.G.; Carey, H.V.; Domazet-Lošo, T.; Douglas, A.E.; Dubilier, N.; Eberl, G.; Fukami, T.; Gilbert, S.F.; et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 2013, 110, 3229–3236. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rosenbaum, M.; Knight, R.; Leibel, R.L. The gut microbiota in human energy homeostasis and obesity. Trends Endocrinol. Metab. 2015, 26, 493–501. [Google Scholar] [CrossRef] [Green Version]
- Clemente, J.C.; Ursell, L.K.; Parfrey, L.W.; Knight, R. The impact of the gut microbiota on human health: An integrative view. Cell 2012, 148, 1258–1270. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Douglas, A.E. The microbial dimension in insect nutritional ecology. Funct. Ecol. 2009, 23, 38–47. [Google Scholar] [CrossRef]
- Wang, J.; Chen, L.; Zhao, N.; Xu, X.; Zhu, B. Of genes and microbes: Solving the intricacies in host genomes. Protein Cell 2018, 5, 446–461. [Google Scholar] [CrossRef] [Green Version]
- Ezenwa, V.O.; Williams, A.E. Microbes and animal olfactory communication: Where do we go from here? BioEssays 2014, 36, 847–854. [Google Scholar] [CrossRef] [PubMed]
- Danchin, E.; Giraldeau, L.; Valone, T.J.; Wagner, R.H. Public information: From nosy neighbors to cultural evolution. Science 2004, 305, 487–491. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maynard-Smith, J.; Harper, D. Animal Signals; Oxford University Press: Oxford, UK, 2003. [Google Scholar]
- Dawkins, R.; Krebs, J. Animal signals: Information or manipulation? In Behavioral Ecology: An Evolutionary Approach; Blackwell: Oxford, UK, 1978; Volume 2, pp. 282–309. [Google Scholar]
- Searcy, W.A.; Nowicki, S. The Evolution of Animal Communication: Reliability and Deception in Signaling Systems; Princeton University Press: Princeton, NJ, USA, 2010. [Google Scholar]
- Zahavi, A.; Zahavi, A. The Handicap Principle: A Missing Piece of Darwin’s Puzzle; Oxford University Press: Oxford, UK, 1997. [Google Scholar]
- Wyatt, T.D. Pheromones and signature mixtures: Defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J. Comp. Physiol. A 2010, 196, 685–700. [Google Scholar] [CrossRef]
- Archie, E.A.; Theis, K.R. Animal behaviour meets microbial ecology. Anim. Behav. 2011, 82, 425–436. [Google Scholar] [CrossRef]
- Engl, T.; Kaltenpoth, M. Influence of microbial symbionts on insect pheromones. Nat. Prod. Rep. 2018, 35, 386–397. [Google Scholar] [CrossRef]
- Leclaire, S.; Jacob, S.; Greene, L.K.; Dubay, G.R.; Drea, C.M. Social odours covary with bacterial community in the anal secretions of wild meerkats. Sci. Rep. 2017, 7, 3240. [Google Scholar] [CrossRef] [PubMed]
- Theis, K.R.; Venkataraman, A.; Dycus, J.A.; Koonter, K.D.; Schmitt-Matzen, E.N.; Wagner, A.P.; Holekamp, K.E.; Schmidt, T.M. Symbiotic bacteria appear to mediate hyena social odors. Proc. Natl. Acad. Sci. USA 2013, 110, 19832–19837. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Whittaker, D.J.; Slowinski, S.P.; Greenberg, J.M.; Alian, O.; Winters, A.D.; Ahmad, M.M.; Burrell, M.J.E.; Soini, H.A.; Novotny, M.V.; Ketterson, E.D.; et al. Experimental evidence that symbiotic bacteria produce chemical cues in a songbird. J. Exp. Biol. 2019, 222. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Riley, M.A.; Wertz, J.E. Bacteriocines: Evolution, ecology, and application. Annu. Rev. Microbiol. 2002, 56, 117–137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Feldhaar, H. Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol. Entomol. 2011, 36, 533–543. [Google Scholar] [CrossRef]
- Sherwin, E.; Bordenstein, S.R.; Quinn, J.L.; Dinan, T.G.; Cryan, J.F. Microbiota and the social brain. Science 2019, 366. [Google Scholar] [CrossRef]
- Carthey, A.J.R.; Gillings, M.R.; Blumstein, D.T. The extended genotype: Microbially mediated olfactory communication. Trends Ecol. Evol. 2018, 33, 885–894. [Google Scholar] [CrossRef] [PubMed]
- Albone, E.S.; Eglinton, G.; Walker, J.M.; Ware, G.C. 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. 1974, 14, 387–400. [Google Scholar] [CrossRef]
- Albone, E.S.; Gosden, P.E.; Ware, G.C.; Macdonald, D.W.; Hough, N.G. Bacterial action and chemical signalling in the Red Fox (Vulpes vulpes) and other mammals. Bact. Action Chem. Signal. 1978, 67, 78–91. [Google Scholar]
- Archie, E.A.; Tung, J. Social behavior and the microbiome. Curr. Opin. Behav. Sci. 2015, 6, 28–34. [Google Scholar] [CrossRef] [Green Version]
- Maraci, Ö.; Engel, K.; Caspers, B.A. Olfactory communication via microbiota: What is known in birds? Genes 2018, 9, 387. [Google Scholar] [CrossRef] [Green Version]
- Sharon, G.; Segal, D.; Ringo, J.M.; Hefetz, A.; Zilber-Rosenberg, I.; Rosenberg, E. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 2010, 107, 20051–20056. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schmidtberg, H.; Shukla, S.P.; Halitschke, R.; Vogel, H.; Vilcinskas, A. Symbiont-mediated chemical defense in the invasive ladybird Harmonia axyridis. Ecol. Evol. 2019, 9, 1715–1729. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brunetti, A.E.; Lyra, M.L.; Melo, W.G.P.; Andrade, L.E.; Palacios-Rodríguez, P.; Prado, B.M.; Haddad, C.F.B.; Pupo, M.T.; Lopes, N.P. Symbiotic skin bacteria as a source for sex-specific scents in frogs. Proc. Natl. Acad. Sci. USA 2019, 116, 2124–2129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Law-Brown, J.; Meyers, P.R. Enterococcus phoeniculicola sp. nov., a novel member of the enterococci isolated from the uropygial gland of the Red-billed Woodhoopoe, Phoeniculus purpureus. Int. J. Syst. Evol. Microbiol. 2003, 53, 683–685. [Google Scholar] [CrossRef]
- Martín-Vivaldi, M.; Peña, A.; Peralta-Sánchez, J.M.; Sánchez, L.; Ananou, S.; Ruiz-Rodríguez, M.; Soler, J.J. Antimicrobial chemicals in hoopoe preen secretions are produced by symbiotic bacteria. Proc. R. Soc. B Biol. Sci. 2010, 277, 123–130. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bradbury, J.; Vehrencamp, S. Principles of Animal Communication, 2nd ed.; Sinauer Associates: Sunderland, UK, 2011. [Google Scholar]
- Lee, C.Y.; Peralta-Sánchez, J.M.; Martínez-Bueno, M.; Møller, A.P.; Rabelo-Ruiz, M.; Zamora-Muñoz, C.; Soler, J.J. The gut microbiota of brood parasite and host nestlings reared within the same environment: Disentangling genetic and environmental effects. ISME J. 2020, 14, 2691–2702. [Google Scholar] [CrossRef]
- Caro, S.P.; Balthazart, J.; Bonadonna, F. The perfume of reproduction in birds: Chemosignaling in avian social life. Horm. Behav. 2015, 68, 25–42. [Google Scholar] [CrossRef] [Green Version]
- Buxton, R.T.; Jones, I.L. An experimental study of social attraction in two species of storm-petrel by acoustic and olfactory cues. Condor 2012, 114, 733–743. [Google Scholar] [CrossRef]
- Krause, E.T.; Caspers, B.A. Are ofactory cues involved in nest recognition in two social species of Estrildid Finches? PLoS ONE 2012, 7, e36615. [Google Scholar] [CrossRef] [Green Version]
- Arteaga, L.; Bautista, A.; González, D.; Hudson, R. Smell, suck, survive: Chemical signals and suckling in the rabbit, cat, and dog. In Chemical Signals in Vertebrates; Springer: New York, NY, USA, 2013; ISBN 9781461459262. [Google Scholar]
- Logan, W.D.; Brunet, L.J.; Webb, W.R.; Cutforth, T.; Ngai, J.; Stowers, L. Learned recognition of maternal signature odors mediates the first suckling episode in mice. Curr. Biol. 2012, 22, 1998–2007. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Howard, J.C. H-2 and mating preferences. Nature 1977, 266, 406–408. [Google Scholar] [CrossRef]
- Leclaire, S.; Merkling, T.; Raynaud, C.; Giacinti, G.; Bessière, J.M.; Hatch, S.A.; Danchin, E. An individual and a sex odor signature in kittiwakes? Study of the semiochemical composition of preen secretion and preen down feathers. Naturwissenschaften 2011, 98, 615–624. [Google Scholar] [CrossRef]
- Harrison, X.A.; Cameron, S.J.S. Analytical approaches for microbiome research. Microbiomes Soils Plants Anim. 2020, 8–28. [Google Scholar] [CrossRef]
- Flórez, L.V.; Biedermann, P.H.W.; Engl, T.; Kaltenpoth, M. Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat. Prod. Rep. 2015, 32, 904–936. [Google Scholar] [CrossRef] [Green Version]
- McFall-Ngai, M.J. Unseen forces: The influence of bacteria on animal development. Dev. Biol. 2002, 242, 1–14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Parker, B.J.; Hrček, J.; McLean, A.H.C.; Brisson, J.A.; Charles, H. Intraspecific variation in symbiont density in an insect-microbe symbiosis. Mol. Ecol. 2021, 30, 1559–1569. [Google Scholar] [CrossRef]
- Gerardo, N.M.; Parker, B.J. Mechanisms of symbiont-conferred protection against natural enemies: An ecological and evolutionary framework. Curr. Opin. Insect Sci. 2014, 4, 8–14. [Google Scholar] [CrossRef]
- Douglas, A.E.; Werren, J.H. Holes in the hologenome: Why host-microbe symbioses are not holobionts. mBio 2016, 7, e02099-15. [Google Scholar] [CrossRef] [Green Version]
- Theis, K.R.; Dheilly, N.M.; Klassen, J.L.; Brucker, R.M.; Baines, J.F.; Bosch, T.C.G.; Cryan, J.F.; Gilbert, S.F.; Goodnight, C.J.; Lloyd, E.A.; et al. Getting the hologenome concept right: An eco-evolutionary framework for hosts and their microbiomes. mSystems 2016, 1, e00028-16. [Google Scholar] [CrossRef] [Green Version]
- Bordenstein, S.R.; Theis, K.R. Host biology in light of the microbiome: Ten principles of holobionts and hologenomes. PLoS Biol. 2015, 13, e1002226. [Google Scholar] [CrossRef] [Green Version]
- Carthey, A.J.R.; Blumstein, D.T.; Gallagher, R.V.; Tetu, S.G.; Gillings, M.R. Conserving the holobiont. Funct. Ecol. 2020, 34, 764–776. [Google Scholar] [CrossRef]
- Brooks, A.W.; Kohl, K.D.; Brucker, R.M.; van Opstal, E.J.; Bordenstein, S.R. Phylosymbiosis: Relationships and functional effects of microbial communities across host evolutionary history. PLoS Biol. 2016, 14, e2000225. [Google Scholar] [CrossRef] [PubMed]
- Suárez, J.; Stencel, A. A part-dependent account of biological individuality: Why holobionts are individuals and ecosystems simultaneously. Biol. Rev. 2020, 95, 1308–1324. [Google Scholar] [CrossRef] [PubMed]
- Suzuki, T.A.; Ley, R.E. The role of the microbiota in human genetic adaptation. Science 2020, 370, eaaz6827. [Google Scholar] [CrossRef]
- Campos-Cerdá, F.; Bohannan, B.J.M. The nidobiome: A framework for understanding microbiome assembly in neonates. Trends Ecol. Evol. 2020, 35, 573–582. [Google Scholar] [CrossRef]
- Soler, J.J.; Martín-Vivaldi, M.; Peralta-Sánchez, J.M.; Arco, L.; Juárez-García-Pelayo, N. Hoopoes color their eggs with antimicrobial uropygial secretions. Naturwissenschaften 2014, 101, 697–705. [Google Scholar] [CrossRef]
- Díaz-Lora, S.; Pérez-Contreras, T.; Azcárate-García, M.; Martínez Bueno, M.; Soler, J.J.; Martín-Vivaldi, M. Hoopoe Upupa epops male feeding effort is related to female cosmetic egg colouration. J. Avian Biol. 2020, 51, 1–14. [Google Scholar] [CrossRef]
- Ruiz-Rodríguez, M.; Soler, J.J.; Martín-Vivaldi, M.; Martín-Platero, A.M.; Méndez, M.; Peralta-Sánchez, J.M.; Ananou, S.; Valdivia, E.; Martínez-Bueno, M. Environmental factors shape the community of symbionts in the hoopoe uropygial gland more than genetic factors. Appl. Environ. Microbiol. 2014, 80, 6714–6723. [Google Scholar] [CrossRef] [Green Version]
- Martínez-García, Á.; Martín-Vivaldi, M.; Ruiz-Rodríguez, M.; Martínez-Bueno, M.; Arco, L.; Rodríguez-Ruano, S.M.; Peralta-Sánchez, J.M.; Soler, J.J. The microbiome of the uropygial secretion in hoopoes is shaped along the nesting phase. Microb. Ecol. 2016, 72, 252–261. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Olsson, M.J.; Lundström, J.N.; Kimball, B.A.; Gordon, A.R.; Karshikoff, B.; Hosseini, N.; Sorjonen, K.; Olgart Höglund, C.; Solares, C.; Soop, A.; et al. The scent of disease: Human body odor contains an early chemosensory cue of sickness. Psychol. Sci. 2014, 25, 817–823. [Google Scholar] [CrossRef] [PubMed]
- Behringer, D.C.; Butler, M.J.; Shields, J.D. Avoidance of disease by social lobsters. Nature 2006, 441, 421. [Google Scholar] [CrossRef] [PubMed]
- Boillat, M.; Challet, L.; Rossier, D.; Kan, C.; Carleton, A.; Rodriguez, I. The vomeronasal system mediates sick conspecific avoidance. Curr. Biol. 2015, 25, 251–255. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kavaliers, M.; Choleris, E.; Ågmo, A.; Braun, W.J.; Colwell, D.D.; Muglia, L.J.; Ogawa, S.; Pfaff, D.W. Inadvertent social information and the avoidance of parasitized male mice: A role for oxytocin. Proc. Natl. Acad. Sci. USA 2006, 103, 4293–4298. [Google Scholar] [CrossRef] [Green Version]
- Poirotte, C.; Massol, F.; Herbert, A.; Willaume, E.; Bomo, P.M.; Kappeler, P.M.; Charpentier, M.J.E. Mandrills use olfaction to socially avoid parasitized conspecifics. Sci. Adv. 2017, 3, e1601721. [Google Scholar] [CrossRef] [Green Version]
- Endler, J.A. Natural Selection in the Wild; Princeton University Press: Princeton, NJ, USA, 1986. [Google Scholar]
- Futuyma, D.J. Evolution; Sinauer & Associates. Inc.: Sunderland, MA, USA, 2005. [Google Scholar]
- Hamilton, W.D.; Zuk, M. Heritable true fitness and bright birds: A role for parasites? Science 1982, 218, 384–387. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ridley, M. Evolution Blackwell Scientific Publications; Oxford: Boston, MA, USA, 1993. [Google Scholar]
- Andersson, M. Sexual Selection; Princeton University Press: Princeton, NJ, USA, 1994. [Google Scholar]
- Grafen, A. Biological signals as handicaps. J. Theor. Biol. 1990, 144, 517–546. [Google Scholar] [CrossRef]
- Laidre, M.E.; Johnstone, R.A. Animal signals. Curr. Biol. 2013, 23, 829–833. [Google Scholar] [CrossRef] [Green Version]
- Zuk, M.; Kolluru, G.R. Exploitation of sexual signals by predators and parasitoids. Q. Rev. Biol. 1998, 73, 415–438. [Google Scholar] [CrossRef]
- Zuk, M.; Rotenberry, J.T.; Tinghitella, R.M. Silent night: Adaptive disappearance of a sexual signal in a parasitized population of field crickets. Biol. Lett. 2006, 2, 521–524. [Google Scholar] [CrossRef] [Green Version]
- Akre, K.L.; Farris, H.E.; Lea, A.M.; Page, R.A.; Ryan, M.J. Signal perception in frogs and bats and the evolution of mating signals. Science 2011, 333, 751–752. [Google Scholar] [CrossRef]
- Díez-Fernández, A.; Martínez-de la Puente, J.; Gangoso, L.; López, P.; Soriguer, R.; Martín, J.; Figuerola, J. Mosquitoes are attracted by the odour of Plasmodium-infected birds. Int. J. Parasitol. 2020, 50, 569–575. [Google Scholar] [CrossRef]
- Lacroix, R.; Mukabana, W.R.; Gouagna, L.C.; Koella, J.C. Malaria infection increases attractiveness of humans to mosquitoes. PLoS Biol. 2005, 3, e298. [Google Scholar] [CrossRef] [Green Version]
- Møller, A.P.; Peralta-Sánchez, J.M.; Nielsen, J.T.; López-Hernández, E.; Soler, J.J. Goshawk prey have more bacteria than non-prey. J. Anim. Ecol. 2012, 81, 403–410. [Google Scholar] [CrossRef]
- Nicholson, J.K.; Holmes, E.; Kinross, J.; Burcelin, R.; Gibson, G.; Jia, W.; Pettersson, S. Host-gut microbiota metabolic interactions. Science 2012, 336, 1262–1267. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hall, M.J.R. Trapping the flies that cause myiasis: Their responses to host-stimuli. Ann. Trop. Med. Parasitol. 1995, 89, 333–357. [Google Scholar] [CrossRef] [PubMed]
- Cozzarolo, C.S.; Glaizot, O.; Christe, P.; Pigeault, R. Enhanced attraction of arthropod vectors to infected vertebrates: A review of empirical evidence. Front. Ecol. Evol. 2020, 8, 296. [Google Scholar] [CrossRef]
- Moore, J. Parasites and the Behavior of Animals; Oxford Series in Ecology and Evolution: Oxford, UK, 2002. [Google Scholar]
- Poldy, J. Volatile cues influence host-choice in arthropod pests. Animals 2020, 10, 1984. [Google Scholar] [CrossRef]
- Ruiz-López, M.J. Mosquito behavior and vertebrate microbiota interaction: Implications for pathogen transmission. Front. Microbiol. 2020, 11, 3169. [Google Scholar] [CrossRef]
- Verhulst, N.O.; Takken, W.; Dicke, M.; Schraa, G.; Smallegange, R. Chemical ecology of interactions between human skin microbiota and mosquitoes. FEMS Microbiol. Ecol. 2010, 74, 1–9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Verhulst, N.O.; Qiu, Y.T.; Beijleveld, H.; Maliepaard, C.; Knights, D.; Schulz, S.; Berg-Lyons, D.; Lauber, C.L.; Verduijn, W.; Haasnoot, G.W.; et al. Composition of human skin microbiota affects attractiveness to malaria mosquitoes. PLoS ONE 2011, 6, e28991. [Google Scholar] [CrossRef]
- Verhulst, N.O.; Beijleveld, H.; Knols, B.G.; Takken, W.; Schraa, G.; Bouwmeester, H.J.; Smallegange, R.C. Cultured skin microbiota attracts malaria mosquitoes. Malar. J. 2009, 8, 302. [Google Scholar] [CrossRef] [Green Version]
- Busula, A.O.; Takken, W.; de Boer, J.G.; Mukabana, W.R.; Verhulst, N.O. Variation in host preferences of malaria mosquitoes is mediated by skin bacterial volatiles. Med. Vet. Entomol. 2017, 31, 320–326. [Google Scholar] [CrossRef] [PubMed]
- Logan, J.G.; Birkett, M.A.; Clark, S.J.; Powers, S.; Seal, N.J.; Wadhams, L.J.; Mordue, A.J.; Pickett, J.A. Identification of human-derived volatile chemicals that interfere with attraction of Aedes aegypti mosquitoes. J. Chem. Ecol. 2008, 34, 308–322. [Google Scholar] [CrossRef] [PubMed]
- Mansourian, S.; Corcoran, J.; Enjin, A.; Löfstedt, C.; Dacke, M.; Stensmyr, M.C. Fecal derived phenol induces egg laying aversion in drosophila. Curr. Biol. 2016, 26, 2762–2769. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jacob, S.; Parthuisot, N.; Vallat, A.; Ramon-Portugal, F.; Helfenstein, F.; Heeb, P. Microbiome affects egg carotenoid investment, nestling development and adult oxidative costs of reproduction in Great tits. Funct. Ecol. 2015, 29, 1048–1058. [Google Scholar] [CrossRef]
- Soler, J.J.; Ruiz-Castellano, C.; Figuerola, J.; Martín-Vivaldi, M.; Martínez-de la Puente, J.; Ruiz-Rodríguez, M.; Tomás, G. Telomere length and dynamics of spotless starling nestlings depend on nest-building materials used by parents. Anim. Behav. 2017, 126, 89–100. [Google Scholar] [CrossRef]
- Jacob, S.; Sallé, L.; Zinger, L.; Chaine, A.S.; Ducamp, C.; Boutault, L.; Russell, A.F.; Heeb, P. Chemical regulation of body feather microbiota in a wild bird. Mol. Ecol. 2018, 27, 1727–1738. [Google Scholar] [CrossRef]
- Azcárate-García, M.; Ruiz-Rodríguez, M.; Díaz-Lora, S.; Ruiz-Castellano, C.; Soler, J.J. Experimentally broken faecal sacs affect nest bacterial environment, development and survival of spotless starling nestlings. J. Avian Biol. 2019, 50, e02044. [Google Scholar] [CrossRef]
- Mazorra-Alonso, M.; Martín-Vivaldi, M.; Peralta-Sánchez, J.M.; Soler, J.J. Autoclaving nest-material remains influences the probability of ectoparasitism of nestling hoopoes (Upupa epops). Biology 2020, 9, 306. [Google Scholar] [CrossRef] [PubMed]
- Dubiec, A.; Góźdź, I.; Mazgajski, T.D. Green plant material in avian nests. Avian Biol. Res. 2013, 6, 133–146. [Google Scholar] [CrossRef]
- Ibáñez-Álamo, J.D.; Rubio, E.; Soler, J.J. Evolution of nestling faeces removal in avian phylogeny. Anim. Behav. 2017, 124, 1–5. [Google Scholar] [CrossRef]
- Ruiz-Castellano, C.; Ruiz-Rodríguez, M.; Tomás, G.; Soler, J.J. Antimicrobial activity of nest-lining feathers is enhanced by breeding activity in avian nests. FEMS Microbiol. Ecol. 2019, 95, fiz052. [Google Scholar] [CrossRef]
- Amo, L.; Galván, I.; Tomás, G.; Sanz, J.J. Predator odour recognition and avoidance in a songbird. Funct. Ecol. 2008, 22, 289–293. [Google Scholar] [CrossRef]
- Kats, L.B.; Dill, L.M. The scent of death: Chemosensory assessment of predation risk by prey animals. Ecoscience 1998, 5, 361–394. [Google Scholar] [CrossRef]
- Zidar, J.; Løvlie, H. Scent of the enemy: Behavioural responses to predator faecal odour in the fowl. Anim. Behav. 2012, 84, 547–554. [Google Scholar] [CrossRef]
- Temple, S.A. Do predators always capture substandard individuals disproportionately from prey populations? Ecology 1987, 68, 669–674. [Google Scholar] [CrossRef]
- Packer, C.; Holt, R.D.; Hudson, P.J.; Lafferty, K.D.; Dobson, A.P. Keeping the herds healthy and alert: Implications of predator control for infectious disease. Ecol. Lett. 2003, 6, 797–802. [Google Scholar] [CrossRef] [Green Version]
- Cabreiro, F.; Gems, D. Worms need microbes too: Microbiota, health and aging in Caenorhabditis elegans. EMBO Mol. Med. 2013, 5, 1300–1310. [Google Scholar] [CrossRef]
- van Veelen, H.P.J.; Falcão Salles, J.; Matson, K.D.; van der Velde, M.; Tieleman, B.I. Microbial environment shapes immune function and cloacal microbiota dynamics in zebra finches Taeniopygia guttata. Anim. Microbiome 2020, 2, 1–17. [Google Scholar] [CrossRef]
- Liew, W.P.-P.; Ong, J.-S.; Gan, C.-Y.; Yahaya, S.; Khoo, B.Y.; Liong, M.T. Gut Microbiome and Stress. In Beneficial Microorganisms in Medical and Health Applications. Microbiology Monographs; Liong, M.T., Ed.; Springer: Berlin/Heidelberg, Germany, 2015; pp. 223–255. ISBN 9783319232133. [Google Scholar]
- Noguera, J.C.; Aira, M.; Domínguez, J.; Animal, G.D.E.; De Vigo, U.; Cacti, T. Glucocorticoids modulate gastrointestinal microbiome in a wild bird. R. Soc. Open Sci. 2018, 5, 171743. [Google Scholar] [CrossRef] [Green Version]
- Liu, J.; Huang, S.; Li, G.; Zhao, J.; Lu, W.; Zhang, Z. High housing density increases stress hormone- or disease-associated fecal microbiota in male Brandt’s voles (Lasiopodomys brandtii). Horm. Behav. 2020, 126, 104838. [Google Scholar] [CrossRef]
- Farzi, A.; Fröhlich, E.E.; Holzer, P. Gut microbiota and the neuroendocrine system. Neurotherapeutics 2018, 15, 5–22. [Google Scholar] [CrossRef] [Green Version]
- Levin, E.R.; Hammes, S.R. Nuclear receptors outside the nucleus: Extranuclear signalling by steroid receptors. Nat. Rev. Mol. Cell Biol. 2016, 17, 783–797. [Google Scholar] [CrossRef] [Green Version]
- Mao, K.; Baptista, A.P.; Tamoutounour, S.; Zhuang, L.; Bouladoux, N.; Martins, A.J.; Huang, Y.; Gerner, M.Y.; Belkaid, Y.; Germain, R.N. Innate and adaptive lymphocytes sequentially shape the gut microbiota and lipid metabolism. Nature 2018, 554, 255–259. [Google Scholar] [CrossRef]
- Belkaid, Y.; Hand, T.W. Role of the microbiota in immunity and inflammation. Cell 2014, 157, 121–141. [Google Scholar] [CrossRef] [Green Version]
- Clark, L. The Nest Protection Hypothesis: The Adaptive Use of Plant Secondary Compounds by European Starlings; Oxford University Press: Oxford, UK, 1991. [Google Scholar]
- Clayton, D.H.; Wolfe, N.D. The adaptive significance of self-medication. Trends Ecol. Evol. 1993, 8, 60–63. [Google Scholar] [CrossRef]
- Lozano, G.A. Parasitic stress and self-medication in wild animals. Adv. Study Behav. 1998, 27, 291–317. [Google Scholar]
- De Roode, J.C.; Lefèvre, T.; Hunter, M.D. Self-Medication in Animals. Science 2013, 340, 150–152. [Google Scholar] [CrossRef]
- Tomás, G.; Zamora-Muñoz, C.; Martín-Vivaldi, M.; Barón, M.D.; Ruiz-Castellano, C.; Soler, J.J. Effects of chemical and auditory cues of Hoopoes (Upupa epops) in repellence and attraction of blood-feeding flies. Front. Ecol. Evol. 2020, 8, 579667. [Google Scholar] [CrossRef]
- Jacob, J.; Ziswiler, V. The Uropygial Gland; Famer, D.S., King, J.R., Parker, K.C., Eds.; Academic Press: New York, NY, USA, 1982; Volume VII, pp. 359–362. [Google Scholar]
- Møller, A.P.; Czirjak, G.Á.; Heeb, P. Feather micro-organisms and uropygial antimicrobial defences in a colonial passerine bird. Funct. Ecol. 2009, 23, 1097–1102. [Google Scholar] [CrossRef]
- Moreno-Rueda, G. Preen oil and bird fitness: A critical review of the evidence. Biol. Rev. 2017, 92, 2131–2143. [Google Scholar] [CrossRef]
- Ruiz-Rodríguez, M.; Valdivia, E.; Soler, J.J.; Martín-Vivaldi, M.; Martín-Platero, A.M.; Martínez-Bueno, M. Symbiotic bacteria living in the hoopoe’s uropygial gland prevent feather degradation. J. Exp. Biol. 2009, 212, 3621–3626. [Google Scholar] [CrossRef] [Green Version]
- Bailey, R.J.E.; Birkett, M.A.; Ingvarsdóttir, A.; Mordue, A.J.; Mordue, W.; O’Shea, B.; Pickett, J.A.; Wadhams, L.J. The role of semiochemicals in host location and non-host avoidance by salmon louse (Lepeophtheirus salmonis) copepodids. Can. J. Fish. Aquat. Sci. 2006, 63, 448–456. [Google Scholar] [CrossRef]
- Douglas, H.D.; Co, J.E.; Jones, T.H.; Conner, W.E. Interspecific differences in Aethia spp. auklet odorants and evidence for chemical defense against ectoparasites. J. Chem. Ecol. 2004, 30, 1921–1935. [Google Scholar] [CrossRef]
- Douglas, H.D.; Co, J.E.; Jones, T.H.; Conner, W.E.; Day, J.F. Chemical odorant of colonial seabird repels mosquitoes. J. Med. Entomol. 2005, 42, 647–651. [Google Scholar] [CrossRef]
- Logan, J.G.; Birkett, M.A. Semiochemicals for biting fly control: Their identification and exploitation. Pest Manag. Sci. 2007, 63, 647–657. [Google Scholar] [CrossRef] [Green Version]
- Reneerkens, J.; Piersma, T.; Sinninghe Damsté, J.S. Switch to diester preen waxes may reduce avian nest predation by mammalian predators using olfactory cues. J. Exp. Biol. 2005, 208, 4199–4202. [Google Scholar] [CrossRef] [Green Version]
- Lopanik, N.B. Chemical defensive symbioses in the marine environment. Funct. Ecol. 2014, 28, 328–340. [Google Scholar] [CrossRef]
- Molloy, E.; Hertweck, C. Antimicrobial discovery inspired by ecological interactions. Curr. Opin. Microbiol. 2017, 39, 121–127. [Google Scholar] [CrossRef]
- Torres, J.P.; Schmidt, E.W. The biosynthetic diversity of the animal world. J. Biol. Chem. 2019, 294, 17684–17692. [Google Scholar] [CrossRef] [Green Version]
- Xie, J.; Lan, Y.; Sun, C.; Shao, Y. Insect microbial symbionts as a novel source for biotechnology. World J. Microbiol. Biotechnol. 2019, 35, 25. [Google Scholar] [CrossRef]
- Moreira, L.A.; Iturbe-Ormaetxe, I.; Jeffery, J.A.; Lu, G.; Pyke, A.T.; Hedges, L.M.; Rocha, B.C.; Hall-Mendelin, S.; Day, A.; Riegler, M.; et al. A Wolbachia symbiont in Aedes aegypti limits infection with Dengue, Chikungunya, and Plasmodium. Cell 2009, 139, 1268–1278. [Google Scholar] [CrossRef] [Green Version]
- Jaenike, J.; Unckless, R.; Cockburn, S.N.; Boelio, L.M.; Perlman, S.J. Adaptation via symbiosis: Recent sepread of a Drosophila defensiva symbiont. Science 2010, 329, 212–215. [Google Scholar] [CrossRef] [PubMed]
- Xie, S.; Vilchez, I.; Mateos, M. Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS ONE 2010, 5, e12149. [Google Scholar] [CrossRef] [PubMed]
- Kaltenponh, M.; Gottler, W.; Herzner, G.; Strohm, E. Symbiotic bacteria protect wasp larvae from fungal infestation. Curr. Biol. 2005, 15, 475–479. [Google Scholar] [CrossRef] [Green Version]
- Currie, C.R.; Scottt, J.A.; Summerbell, R.C.; Malloch, D. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 1999, 398, 701–704. [Google Scholar] [CrossRef]
- Scott, J.J.; Chan, D.O.; Yuceer, M.; Klepzig, K.D.; Clardy, J.; Currie, C.R. Bacterial protection of beetle-fungus mutualism. Nature 2008, 452, 456–459. [Google Scholar] [CrossRef]
- Kellner, R.L.L. Stadium-specific transmission of endosymbionts needed for pederin biosynthesis in three species of Paederus rove beetles. Entomol. Exp. Appl. 2003, 107, 115–124. [Google Scholar] [CrossRef]
- Davis, T.S.; Crippen, T.L.; Hofstetter, R.W.; Tomberlin, J.K. Microbial volatile emissions as insect semiochemicals. J. Chem. Ecol. 2013, 39, 840–859. [Google Scholar] [CrossRef] [PubMed]
- Law-Brown, J. Chemical Defence in the Red-Billed Woodhoopoe, Phoeniculus Purpureus. Master’s Thesis, University of Cape Town, Cape Town, South Africa, 2001. [Google Scholar]
- Soler, J.J.; Martín-Vivaldi, M.; Ruiz-Rodríguez, M.; Valdivia, E.; Martín-Platero, A.M.; Martínez-Bueno, M.; Peralta-Sánchez, J.M.; Méndez, M. Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Funct. Ecol. 2008, 22, 864–871. [Google Scholar] [CrossRef] [Green Version]
- Ruiz-Rodríguez, M.; Martínez-Bueno, M.; Martín-Vivaldi, M.; Valdivia, E.; Soler, J.J. Bacteriocins with a broader antimicrobial spectrum prevail in enterococcal symbionts isolated from the hoopoe’s uropygial gland. FEMS Microbiol. Ecol. 2013, 85, 495–502. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martín-Platero, A.M.; Valdivia, E.; Ruíz-Rodríguez, M.; Soler, J.J.; Martín-Vivaldi, M.; Maqueda, M.; Martínez-Bueno, M. Characterization of antimicrobial substances produced by Enterococcus faecalis MRR 10-3, isolated from the uropygial gland of the hoopoe (Upupa epops). Appl. Environ. Microbiol. 2006, 72, 4245–4249. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Magallanes, S.; García-Longoria, L.; López-Calderón, C.; Reviriego, M.; de Lope, F.; Møller, A.P.; Marzal, A. Uropygial gland volume and malaria infection are related to survival in migratory house martins. J. Avian Biol. 2017, 48, 1355–1359. [Google Scholar] [CrossRef]
- Magallanes, S.; García-Longoria, L.; Muriel, J.; De Lope, F.; Marzal, A. Variation of uropygial gland volume and malaria infection between urban-rural environment in the house sparrow. Ecosistemas 2020, 29. [Google Scholar] [CrossRef]
- Magallanes, S.; Møller, A.P.; García-Longoria, L.; De Lope, F.; Marzal, A. Volume and antimicrobial activity of secretions of the uropygial gland are correlated with malaria infection in house sparrows. Parasites Vectors 2016, 9, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Bodawatta, K.H.; Schierbech, S.K.; Petersen, N.R.; Sam, K.; Bos, N.; Jønsson, K.A.; Poulsen, M. Great tit (Parus major) uropygial gland microbiomes and their potential defensive roles. Front. Microbiol. 2020, 11, 1735. [Google Scholar] [CrossRef]
- Chiale, M.C.; Montalti, D.; Flamini, M.A.; Barbeito, C.G. The uropygial gland of the southern caracara (Caracara plancus; Falconidae: Falconinae): Histological and histochemical aspects. Acta Zool. 2017, 98, 245–251. [Google Scholar] [CrossRef]
- Braun, M.S.; Zimmermann, S.; Danner, M.; Rashid, H.O.; Wink, M. Corynebacterium uropygiale sp. nov., isolated from the preen gland of turkeys (Meleagris gallopavo). Syst. Appl. Microbiol. 2016, 39, 88–92. [Google Scholar] [CrossRef] [PubMed]
- Schulte, B.A.; Goodwin, T.E.; Ferkin, M.H. Chemical Signals in Vertebrates, 13th ed.; Springer International Publishing: Heidelberg, Germany, 2016; ISBN 9781461459279. [Google Scholar]
- Stevens, M. Cheats and Deceits: How Animals and Plants Exploit and Mislead; Oxford University Press: New York, NY, USA, 2016. [Google Scholar]
- Wyatt, T.D. Pheromones and Animal Behavior: Chemical Signals and Signatures, 2nd ed.; Cambridge University Press: Cambridge, UK, 2014. [Google Scholar] [CrossRef] [Green Version]
- Santacroce, L.; Charitos, I.A.; Ballini, A.; Inchingolo, F.; Luperto, P.; De Nitto, E.; Topi, S. The human respiratory system and its microbiome at a glimpse. Biology 2020, 9, 318. [Google Scholar] [CrossRef]
- Conover, M.R. Predator-Prey Dynamics: The Role of Olfaction; CRC Press: Boca Raton, FL, USA, 2007. [Google Scholar]
- Hughes, N.K.; Price, C.J.; Banks, P.B. Predators are attracted to the olfactory signals of prey. PLoS ONE 2010, 5, e13114. [Google Scholar] [CrossRef] [Green Version]
- Takken, W.; Knols, B.G.J. Odor-mediated behavior of afrotropical malaria mosquitoes. Annu. Rev. Entomol. 1999, 44, 131–157. [Google Scholar] [CrossRef]
- Balenger, S.L.; Zuk, M. Testing the Hamilton-Zuk hypothesis: Past, present, and future. Integr. Comp. Biol. 2014, 54, 601–613. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Briskie, J.V.; Martin, P.R.; Martin, T.E. Nest predation and the evolution of nestling begging calls. Proc. R. Soc. B Biol. Sci. 1999, 266, 2153–2159. [Google Scholar] [CrossRef] [Green Version]
- McNair, C.M. Ectoparasites of medical and veterinary importance: Drug resistance and the need for alternative control methods. J. Pharm. Pharmacol. 2015, 67, 351–363. [Google Scholar] [CrossRef]
- Grisi, L.; Leite, R.C.; de Souza Martins, J.R.; Medeiros de Barros, A.T.; Andreotti, R.; Cançado, P.H.D.; Pérez de León, A.A.; Pereira, J.B.; Silva Villela, H. Reassessment of the potential economic impact of cattle parasites in Brazil. Rev. Bras. Parasitol. Vet. 2014, 23, 150–156. [Google Scholar] [CrossRef] [Green Version]
- Ravikumar, R.K.; Periyaveeturaman, C.; Selvaraju, D.; Kinhekar, A.S.; Dutta, L.; Kumar, V. Community oriented ectoparasite intervention system: Concepts for on-farm application of indigenous veterinary medication. Adv. Anim. Vet. Sci. 2016, 4, 9–19. [Google Scholar]
- Marangi, M.; Morelli, V.; Pati, S.; Camarda, A.; Cafiero, M.A.; Giangaspero, A. Acaricide residues in laying hens naturally infested by red mite Dermanyssus gallinae. PLoS ONE 2012, 7, e31795. [Google Scholar] [CrossRef] [Green Version]
- Lee, B.; Groth, P. Scabies: Transcutaneous Poisoning During Treatment. Pediatrics 1977, 59, 643. [Google Scholar]
- Pasay, C.; Walton, S.; Fischer, K.; Holt, D.; Mccarthy, J. PCR-based assay to survey for knockdown resistance to pyrethroid acaricides in human scabies mites (Sarcoptes scabiei var hominis). Am. J. Trop. Med. Hyg. 2006, 74, 649–657. [Google Scholar] [CrossRef]
- Gordon, J.R.; Goodman, M.H.; Potter, M.F.; Haynes, K.F. Population variation in and selection for resistance to pyrethroid-neonicotinoid insecticides in the bed bug. Sci. Rep. 2014, 4, 3836. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mazorra-Alonso, M.; Tomás, G.; Soler, J.J. Microbially Mediated Chemical Ecology of Animals: A Review of Its Role in Conspecific Communication, Parasitism and Predation. Biology 2021, 10, 274. https://doi.org/10.3390/biology10040274
Mazorra-Alonso M, Tomás G, Soler JJ. Microbially Mediated Chemical Ecology of Animals: A Review of Its Role in Conspecific Communication, Parasitism and Predation. Biology. 2021; 10(4):274. https://doi.org/10.3390/biology10040274
Chicago/Turabian StyleMazorra-Alonso, Mónica, Gustavo Tomás, and Juan José Soler. 2021. "Microbially Mediated Chemical Ecology of Animals: A Review of Its Role in Conspecific Communication, Parasitism and Predation" Biology 10, no. 4: 274. https://doi.org/10.3390/biology10040274
APA StyleMazorra-Alonso, M., Tomás, G., & Soler, J. J. (2021). Microbially Mediated Chemical Ecology of Animals: A Review of Its Role in Conspecific Communication, Parasitism and Predation. Biology, 10(4), 274. https://doi.org/10.3390/biology10040274