Understanding the Role of Semiochemicals on the Reproductive Behaviour of Cheetahs (Acinonyx jubatus)—A Review
Abstract
:Simple Summary
Abstract
1. Introduction
2. The Cheetah
2.1. Threats
2.2. Possible Reasons for Population Decline
2.3. Reproductive Characteristics
2.4. Reproductive Behaviour
3. The Physiology of Olfaction
3.1. The Main Versus the Vomeronasal (Accessory) Olfactory System
3.2. The Main Olfactory System
3.3. The Vomeronasal (Accessory) Olfactory System
3.4. The Link to Olfaction and Hormone Release
4. How Is Olfaction Linked to Reproduction?
4.1. The Effect of Pheromones on Behaviour
4.2. Captive Breeding
5. Semiochemicals
5.1. Complex vs. Single Compounds
5.2. Semiochemicals in Communication
5.3. Identification of Individuals through Semiochemicals
5.4. Semiochemicals in Cheetahs
5.5. Current Uses of Synthetic Scent to Influence Behaviour and Its Potential Use in Cheetahs
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Cheetah Outreach. Cheetah Information; 2018; Available online: http://www.cheetah.co.za/pdf/Cheetah%20Information.doc (accessed on 1 November 2021).
- Durant, S.; Mitchell, N.; Ipavec, A.; Groom, R. Acinonyx Jubatus. The IUCN Red List of Threatened Species 2015: E.T219A50649567. IUCN Red List Threat. Species 2015. Available online: https://www.iucnredlist.org/species/219/50649567 (accessed on 1 November 2021).
- Menotti-Raymond, M.; O’Brien, S.J. Dating the Genetic Bottleneck of the African Cheetah. Proc. Natl. Acad. Sci. USA 1993, 90, 3172–3176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- O’Brien, S.J.; Wildt, D.E.; Goldman, D.; Merril, C.R.; Bush, M. The Cheetah Is Depauperate in Genetic Variation. Science 1983, 221, 459–462. [Google Scholar] [CrossRef]
- Frankham, R. Genetics and Extinction. Biol. Conserv. 2005, 126, 131–140. [Google Scholar] [CrossRef]
- Koester, D.C. The Effect of Environment on the Reproductive Potential of Ex Situ Cheetahs (Acinonyx jubatus). Ph.D. Thesis, George Mason University, Fairfax, VA, USA, 2014. [Google Scholar]
- Silva, L.; Antunes, A. Vomeronasal Receptors in Vertebrates and the Evolution of Pheromone Detection. Ann. Rev. Anim. Biosci. 2017, 5, 353–370. [Google Scholar] [CrossRef] [Green Version]
- Wachter, B.; Thalwitzer, S.; Hofer, H.; Lonzer, J.; Hildebrandt, T.B.; Hermes, R. Reproductive History and Absence of Predators Are Important Determinants of Reproductive Fitness: The Cheetah Controversy Revisited. Conserv. Lett. 2011, 4, 47–54. [Google Scholar] [CrossRef]
- Wielebnowski, N.; Brown, J.L. Behavioral Correlates of Physiological Estrus in Cheetahs. Zoo Biol. 1998, 17, 193–209. [Google Scholar] [CrossRef]
- Carrel, J.E. Aphrodisiacs and Anaphrodisiacs: Better Loving through Chemistry. Stadler Genet. Symp. 1976, 8, 79–109. [Google Scholar]
- Soso, S.B. Chemical Constituency and Odor of Semiochemicals: Studying the Chemical Composition and Odor of Volatile Organic Compounds of Great Cat Marking Fluid in an Effort to Aid Tiger and Lion Conservation. Ph.D. Thesis, Iowa State University, Ames, IA, USA, 2016. [Google Scholar]
- Visser, R.R.C. Chemical Communication: Chemical Characterization of Volatile Constituents of Urine of the Southern African Cheetah (Acinonyx jubatus), Using Headspace Sampling and GC-MS. Ph.D. Thesis, Stellenbosch University, Stellenbosch, South Africa, 2002. [Google Scholar]
- Belanger, R.M.; Corkum, L.D. Review of Aquatic Sex Pheromones and Chemical Communication in Anurans. J. Herpetol. 2009, 43, 184–191. [Google Scholar] [CrossRef]
- Poddar-Sarkar, M. Mammalian Semiochemicals: Chemical and Behavioural Aspects with Special Reference to Tiger. Ph.D. Thesis, University of Calcutta, Kolkata, India, 1995. [Google Scholar]
- Brahmachary, R.L. Ecology and Chemistry of Mammalian Pheromones. Endeavour 1986, 10, 65–68. [Google Scholar] [CrossRef]
- Igbokwe, C.O. The Role of Main Olfactory and Vomeronasal Systmes in Animal Behaviour and Reproduction. Anim. Res. Int. 2009, 6, 1093–1101. [Google Scholar]
- Brown, J.L. Female Reproductive Cycles of Wild Female Felids. Anim. Reprod. Sci. 2011, 124, 155–162. [Google Scholar] [CrossRef]
- Caro, T.M.; Laurenson, M.K. Ecological and Genetic Factors in Conservation: A Cautionary Tale. Science 1994, 263, 485–487. [Google Scholar] [CrossRef]
- Soso, S.B.; Koziel, J.A. Analysis of Odorants in Marking Fluid of Siberian Tiger (Panthera Tigris Altaica) Using Simultaneous Sensory and Chemical Analysis with Headspace Solid-Phase Microextraction and Multidimensional Gas Chromatography-Mass Spectrometry-Olfactometry. Molecules 2016, 21, 834. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rostro-García, S.; Kamler, J.F.; Ash, E.; Clements, G.R.; Gibson, L.; Lynam, A.J.; McEwing, R.; Naing, H.; Paglia, S. Endangered Leopards: Range Collapse of the Indochinese Leopard (Panthera Pardus Delacouri) in Southeast Asia. Biol. Conserv. 2016, 201, 293–300. [Google Scholar] [CrossRef]
- Caro, T.M. Behavioral Solutions to Breeding Cheetahs in Captivity: Insights from the Wild. Zoo Biol. 1993, 12, 19–30. [Google Scholar] [CrossRef]
- Bertschinger, H.J.; Meltzer, D.G.A.; van Dyk, A. Captive Breeding of Cheetahs in South Africa—30 Years of Data from the de Wildt Cheetah and Wildlife Centre. Reprod. Domest. Anim. 2008, 43, 66–73. [Google Scholar] [CrossRef] [PubMed]
- Laurenson, M.K. High Juvenile Mortality in Cheetahs (Acinonyx Jubatus) and Its Consequences for Maternal Care. J. Zool. 1994, 234, 387–408. [Google Scholar] [CrossRef]
- Brown, J.L.; Wildt, D.E.; Wielebnowski, N.; Goodrowe, K.L.; Graham, L.H.; Wells, S.; Howard, J.G. Reproductive Activity in Captive Female Cheetahs (Acinonyx Jubatus) Assessed by Faecal Steroids. J. Reprod. Fertil. 1996, 106, 337–346. [Google Scholar] [CrossRef] [Green Version]
- Kleiman, D.G.; Eisenberg, J.F. Comparisons of Canid and Felid Social Systems from an Evolutionary Perspective. Anim. Behav. 1973, 21, 637–659. [Google Scholar] [CrossRef]
- Burger, B.V.; Visser, R.; Moses, A.; le Roux, M. Elemental Sulfur Identified in Urine of Cheetah, Acinonyx Jubatus. J. Chem. Ecol. 2006, 32, 1347–1352. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mills, M.G.L.; Mills, M.E.J. Cheetah Cub Survival Revisited: A Re-Evaluation of the Role of Predation, Especially by Lions, and Implications for Conservation. J. Zool. 2014, 292, 136–141. [Google Scholar] [CrossRef]
- Beekman, S.P.A.; Kemp, B.; Louwman, H.C.M.; Colenbrander, B. Analyses of Factors Influencing the Birth Weight and Neonatal Growth Rate of Cheetah (Acinonyx Jubatus) Cubs. Zoo Biol. 1999, 18, 129–139. [Google Scholar] [CrossRef]
- Laurenson, M.K. Early Maternal Behavior of Wild Cheetahs: Implications for Captive Husbandry. Zoo Biol. 1993, 12, 31–43. [Google Scholar] [CrossRef]
- Chimonyo, M.; Dzama, K.; Bhebhe, E. Genetic Determination of Mothering Ability and Piglet Growth in Indigenous Mukota Sows of Zimbabwe. Livest. Sci. 2008, 113, 74–80. [Google Scholar] [CrossRef]
- Grandinson, K. Genetic Background of Maternal Behaviour and Its Relation to Offspring Survival. Livest. Prod. Sci. 2005, 93, 43–50. [Google Scholar] [CrossRef]
- Gäde, S.; Bennewitz, J.; Kirchner, K.; Looft, H.; Knap, P.W.; Thaller, G.; Kalm, E. Genetic Parameters for Maternal Behaviour Traits in Sows. Livest. Sci. 2008, 114, 31–41. [Google Scholar] [CrossRef]
- Garrick, D.J. Maternal Effects on Growth in Beef Cattle. Proc. 8th Conf. Aust. Assoc. Anim. Breed. Genet. 1990, 11, 397–400. [Google Scholar]
- Lund, M.S.; Puonti, M.; Rydhmer, L.; Jensen, J. Relationship between Litter Size and Perinatal and Pre-Weaning Survival in Pigs. Anim. Sci. 2002, 74, 217–222. [Google Scholar] [CrossRef] [Green Version]
- Hill, W.G. Selective Breeding. In Encyclopedia of Genetics; Brenner, S., Miller, J.H., Eds.; Elsevier: Amsterdam, The Netherlands, 2001; pp. 1796–1799. [Google Scholar]
- Koester, D.C.; Freeman, E.W.; Brown, J.L.; Wildt, D.E.; Terrell, K.A.; Franklin, A.D.; Crosier, A.E. Motile Sperm Output by Male Cheetahs (Acinonyx Jubatus) Managed Ex Situ Is Influenced by Public Exposure and Number of Care-Givers. PLoS ONE 2015, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Terio, K.A.; Marker, L.; Overstrom, E.W.; Brown, J.L. Analysis of Ovarian and Adrenal Activity in Namibian Cheetahs. S. Afr. J. Wildl. Res. 2003, 33, 71–78. [Google Scholar]
- Baker, R. Husbandry Guidelines for the Tiger Panthera Tigris. West. Inst. Syd. 2006. Available online: http://nswfmpa.org/Husbandry%20Manuals/Published%20Manuals/Mammalia/Tiger.pdf (accessed on 1 November 2021).
- Ertuev, M.M.; Semenov, U.A. Behaviour Features of the Persian Leopard (Panthera Pardus Saxicolor) during Different Stages of the Estrous Cycle. Nat. Conserv. Res. 2016, 1, 59–69. [Google Scholar] [CrossRef] [Green Version]
- Holesh, J.E.; Bass, A.N.; Lord, M. Physiology, Ovulation. In StatPearls [Internet]; StatPearls Publishing: Treasure Island, FL, USA, 2020. [Google Scholar]
- Johnson, L.M.; Gay, V.L. Luteinizing Hormone in the Cat. II. Mating-Induced Secretion. Endocrinology 1981, 109, 247–252. [Google Scholar] [CrossRef] [PubMed]
- Wildt, D.E.; Seager, S.W.J.; Chakraborty, P.K. Effect of Copulatory Stimuli on Incidence of Ovulation and on Serum Luteinizing Hormone in the Cat. Endocrinology 1980, 107, 1212–1217. [Google Scholar] [CrossRef]
- Penfold, L.M.; Powell, D.; Traylor-Holzer, K.; Asa, C.S. “Use It or Lose It”: Characterization, Implications, and Mitigation of Female Infertility in Captive Wildlife. Zoo Biol. 2014, 33, 20–28. [Google Scholar] [CrossRef] [PubMed]
- Crosier, A.E.; Comizzoli, P.; Baker, T.; Davidson, A.; Munson, L.; Howard, J.G.; Marker, L.L.; Wildt, D.E. Increasing Age Influences Uterine Integrity, but Not Ovarian Function or Oocyte Quality, in the Cheetah (Acinonyx Jubatus). Biol. Reprod. 2011, 85, 243–253. [Google Scholar] [CrossRef] [Green Version]
- Munson, L.; Gardner, A.; Mason, R.J.; Chassy, L.M.; Seal, U.S. Endometrial Hyperplasia and Mineralization in Zoo Felids Treated with Melengestrol Acetate Contraceptives. Vet. Pathol. 2002, 39, 419–427. [Google Scholar] [CrossRef]
- Koester, D.C.; Wildt, D.E.; Brown, J.L.; Meeks, K.; Crosier, A.E. Public Exposure and Number of Conspecifics Have No Influence on Ovarian and Adrenal Activity in the Cheetah (Acinonyx Jubatus). Gen. Comp. Endocrinol. 2017, 243, 120–129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wildt, D.E.; Platz, C.C.; Seager, S.W.J.; Bush, M. Induction of Ovarian Activity in the Cheetah (Acinonyx jubatus). Biol. Reprod. 1981, 24, 217–222. [Google Scholar] [CrossRef] [Green Version]
- Sarri, K.J. Estrous behavior of the female cheetah (Acinonyx jubatus) and the male cheetah’s response to an estrous female. In International Cheetah Studbook 1991. (Sect. N-5); Marker-Kraus, L., Ed.; NOAHS Center, National Zoological Park, Smithsonian Institution: Washington, DC, USA, 1992; pp. 1–22. [Google Scholar]
- Sorenson, C. The cheetah (Acinonyx jubatus) in captivity: Descriptions of estrus and fecal steroid fluctuations activity patterns and solitary behavior. In International Cheetah Studbook 1993. (Sect. K-10); Marker-Kraus, L., Ed.; NOAHS Center, National Zoological Park, Smithsonian Institution: Washington, DC, USA, 1995; pp. 1–41. [Google Scholar]
- Everaert, I.; (Ann van Dyk Cheetah Centre, Pretoria, South Africa). Personal communication, 9 April 2019.
- Apps, P.J.; Weldon, P.J.; Kramer, M. Chemical Signals in Terrestrial Vertebrates: Search for Design Features. Nat. Prod. Rep. 2015, 32, 1131–1153. [Google Scholar] [CrossRef]
- Apps, P.J. Are Mammal Olfactory Signals Hiding Right under Our Noses? Naturwissenschaften 2013, 100, 1131–1153. [Google Scholar] [CrossRef] [PubMed]
- Salazar, I.; Sánchez-Quinteiro, P. A Detailed Morphological Study of the Vomeronasal Organ and the Accessory Olfactory Bulb of Cats. Microsc. Res. Tech. 2011, 74, 1109–1120. [Google Scholar] [CrossRef]
- Brahmachary, R.L.; Poddar-Sarkar, M. Fifty Years of Tiger Pheromone Research. Curr. Sci. 2015, 108, 2178–2185. [Google Scholar]
- Boehm, U.; Zou, Z.; Buck, L.B. Feedback Loops Link Odor and Pheromone Signaling with Reproduction. Cell 2005, 123, 683–695. [Google Scholar] [CrossRef] [Green Version]
- Zufall, F.; Leinders-Zufall, T. Mammalian Pheromone Sensing. Curr. Opin. Neurobiol. 2007, 17, 483–489. [Google Scholar] [CrossRef] [PubMed]
- Shepherd, G.M. Behaviour: Smells, Brains and Hormones. Nature 2006, 439, 149–151. [Google Scholar] [CrossRef] [PubMed]
- Ache, B.W.; Young, J.M. Olfaction: Diverse Species, Conserved Principles. Neuron 2005, 48, 417–430. [Google Scholar] [CrossRef] [Green Version]
- Liberles, S.D.; Buck, L.B. A Second Class of Chemosensory Receptors in the Olfactory Epithelium. Nature 2006, 442, 645–650. [Google Scholar] [CrossRef]
- Doving, K.B.; Trotier, D. Structure and Function of the Vomeronasal Organ. J. Exp. Biol. 1998, 201, 2913–2925. [Google Scholar] [CrossRef]
- Gilfillan, G.D.; Vitale, J.D.T.; McNutt, J.W.; McComb, K. Spontaneous Discrimination of Urine Odours in Wild African Lions, Panthera Leo. Anim. Behav. 2017, 126, 177–185. [Google Scholar] [CrossRef]
- Mellen, J.D. A Comparative Analysis of Scent-Marking, Social and Reproductive Behavior in 20 Species of Small Cats (Felis). Am. Zool. 1993, 33, 151–166. [Google Scholar] [CrossRef] [Green Version]
- Bland, K.P. Tom-Cat Odour and Other Pheromones in Feline Reproduction. Vet. Sci. Commun. 1979, 3, 125–136. [Google Scholar] [CrossRef]
- Verberne, G.; de Boer, J. Chemocommunication among Domestic Cats, Mediated by the Olfactory and Vomeronasal Senses: I. Chemocommunication. Z. Für Tierpsychol. 1976, 42, 86–109. [Google Scholar] [CrossRef]
- Ewer, R.F. The Carnivores; Cornell University Press: Ithaca, NY, USA, 1973. [Google Scholar]
- Firestein, S. How the Olfactory System Makes Sense of Scents. Nature 2001, 413, 211–218. [Google Scholar] [CrossRef] [PubMed]
- Soso, S.B.; Koziel, J.A. Characterizing the Scent and Chemical Composition of Panthera Leo Marking Fluid Using Solid-Phase Microextraction and Multidimensional Gas Chromatography-Mass Spectrometry-Olfactometry. Sci. Rep. 2017, 7, 5137. [Google Scholar] [CrossRef]
- Ferrero, D.M.; Lemon, J.K.; Fluegge, D.; Pashkovski, S.L.; Korzan, W.J.; Datta, S.R.; Spehr, M.; Fendt, M.; Liberles, S.D. Detection and Avoidance of a Carnivore Odor by Prey. Proc. Natl. Acad. Sci. USA 2011, 108, 11235–11240. [Google Scholar] [CrossRef] [Green Version]
- Brahmachary, R.L.; Dutta, J. On the Pheromones of Tigers: Experiments and Theory. Am. Nat. 1981, 118, 561–567. [Google Scholar] [CrossRef]
- Silva, A.R.; Moreira, N.; Pereira, A.F.; Peixoto, G.C.X.; Maia, K.M.; Campos, L.B.; Borges, A.A. Estrus cycle monitoring in wild mammals: Challenges and perspectives. In Theriogenology; 2017; p. 21. Available online: https://www.intechopen.com/books/5861 (accessed on 1 November 2021).
- Wielebnowski, N.C.; Ziegler, K.; Wildt, D.E.; Lukas, J.; Brown, J.L. Impact of Social Management on Reproductive, Adrenal and Behavioural Activity in the Cheetah (Acinonyx Jubatus). Anim. Conserv. 2002, 5, 291–301. [Google Scholar] [CrossRef] [Green Version]
- Mossotti, R.H. Female Reaction to Male Urine Scents as Potential Indicator of Mate Choice in Captive Cheetahs (Acinonyx Jubatus). Ph.D. Thesis, Southern Illinois University, Carbondale, IL, USA, 2010. [Google Scholar]
- Beekman, S.P.A.; de Wit, M.; Louwman, J.; Louwman, H. Breeding and Observations on the Behaviour of Cheetah Acinonyx Jubatus at Wassenaar Wildlife Breeding Centre. Int. Zoo Yearb. 1997, 35, 43–50. [Google Scholar] [CrossRef]
- Heuskin, S.; Verheggen, F.J.; Haubruge, E.; Wathelet, J.-P.; Lognay, G. The Use of Semiochemical Slow-Release Devices in Integrated Pest Management Strategies. Biotechnol. Agron. Soc. Et Environ. 2011, 15, 459–470. [Google Scholar]
- Poddar-Sarkar, M.; Brahmachary, R.L. Pheromones of tiger and other big cats. In Neurobiology of Chemical Communication; Mucignat-Caretta, C., Ed.; CRC Press; Taylor & Francis: Boca Raton, FL, USA, 2014; pp. 407–460. [Google Scholar]
- Cederlund, J. Behavioural Responses of Amur Tigers (Panthera Tigris Altaica) and African Lions (Panthera Leo) to Conspecific Urine and to a Component of Tiger Marking Fluid. Master’s Thesis, Linköping University, Linköping, Sverige, 2018. [Google Scholar]
- Rowe, C. Receiver Psychology and the Evolution of Multicomponent Signals. Anim. Behav. 1999, 58, 921–931. [Google Scholar] [CrossRef] [Green Version]
- Andersen, K.F.; Vulpius, T. Urinary Volatile Constituents of the Lion, Panthera Leo. Chem. Senses 1999, 24, 179–189. [Google Scholar] [CrossRef] [PubMed]
- Burger, B.V.; Viviers, M.Z.; Bekker, J.P.I.; le Roux, M.; Fish, N.; Fourie, W.B.; Weibchen, G. Chemical Characterization of Territorial Marking Fluid of Male Bengal Tiger, Panthera Tigris. J. Chem. Ecol. 2008, 34, 659. [Google Scholar] [CrossRef] [Green Version]
- Penn, D.J.; Oberzaucher, E.; Grammer, K.; Fischer, G.; Soini, H.A.; Wiesler, D.; Novotny, M.V.; Dixon, S.J.; Xu, Y.; Brereton, R.G. Individual and Gender Fingerprints in Human Body Odour. J. R. Soc. Interface 2007, 4, 331–340. [Google Scholar] [CrossRef]
- Kalmus, H. The Discrimination by the Nose of the Dog of Individual Human Odours and in Particular of the Odours of Twins. Br. J. Anim. Behav. 1955, 3, 25–31. [Google Scholar] [CrossRef]
- McLean, L.; Hurst, J.L.; Gaskell, C.J.; Lewis, J.C.M.; Beynon, R.J. Characterization of Cauxin in the Urine of Domestic and Big Cats. J. Chem. Ecol. 2007, 33, 1997–2009. [Google Scholar] [CrossRef]
- Martínez-Macipe, M.; Lafont-Lecuelle, C.; Manteca, X.; Pageat, P.; Cozzi, A. Evaluation of an Innovative Approach for Sensory Enrichment in Zoos: Semiochemical Stimulation for Captive Lions (Panthera Leo). Anim. Welf. 2015, 24, 455–461. [Google Scholar] [CrossRef]
- Starkenmann, C.; Niclass, Y.; Cayeux, I.; Brauchli, R.; Gagnon, A.C. Odorant Volatile Sulfur Compounds in Cat Urine: Occurrence of (+/−)-3,7-Dimethyloct-3-Sulfanyl-6-En-1-Ol and Its Cysteine Conjugate Precursor. Flavour Fragr. J. 2015, 30, 91–100. [Google Scholar] [CrossRef]
- Poddar-Sarkar, M.; Brahmachary, R.L. Putative Semiochemicals in the African Cheetah (Acinonyx Jubatus). J. Lipid Mediat. Cell Signal. 1997, 15, 285–287. [Google Scholar] [CrossRef]
- Poddar-Sarkar, M.; Brahmachary, R.L. Putative Chemical Signals of Leopard. Anim. Biol. 2004, 54, 255–259. [Google Scholar]
- Banks, G.R.; Buglass, A.J.; Waterhouse, J.S. Amines in the Marking Fluid and Anal Sac Secretion of the Tiger, Panthera Tigris. Z. Für Nat. C 1992, 47, 618–620. [Google Scholar] [CrossRef] [PubMed]
- Coombes, H.A.; Stockley, P.; Hurst, J.L. Female Chemical Signalling Underlying Reproduction in Mammals. J. Chem. Ecol. 2018, 44, 851–873. [Google Scholar] [CrossRef] [Green Version]
- Van Metter, J.E.; Harriger, M.D.; Bolen, R.H. Environmental Enrichment Utilizing Stimulus Objects for African Lions (Panthera Leo Leo) and Sumatran Tigers (Panthera Tigris Sumatrae). Bios 2008, 79, 7–16. [Google Scholar] [CrossRef]
- Dehnhard, M. Mammal Semiochemicals: Understanding Pheromones and Signature Mixtures for Better Zoo-Animal Husbandry and Conservation. Int. Zoo Yearb. 2011, 45, 55–79. [Google Scholar] [CrossRef]
- Yu, S.; Jiang, Z.; Zhu, H.; Li, C.; Zhang, E.; Zhang, J.; Harrington, C. Effects of Odors on Behaviors of Captive Amur Leopards Panthera Pardus Orientalis. Curr. Zool. 2009, 55, 20–27. [Google Scholar] [CrossRef]
- Thomas, P.; Balme, G.; Hunter, L.; McCabe-Parodi, J. Using Scent Attractants to Non-Invasively Collect Hair Samples from Cheetahs, Leopards and Lions. Anim. Keep. Forum 2005, 7, 342–384. [Google Scholar]
- Barja, I.; de Miguel, F.J. Chemical Communication in Large Carnivores: Urine-Marking Frequencies in Captive Tigers and Lions. Pol. J. Ecol. 2010, 58, 397–400. [Google Scholar]
- Heinrich, S.K.; Hofer, H.; Courtiol, A.; Melzheimer, J.; Dehnhard, M.; Czirják, G.A.; Wachter, B. Cheetahs Have a Stronger Constitutive Innate Immunity than Leopards. Sci. Rep. 2017, 7, 1–11. [Google Scholar] [CrossRef] [PubMed]
Chemical Compound | Cat | Lion | Cheetah | Leopard | Tiger | Other Animals | Behaviour |
---|---|---|---|---|---|---|---|
Octanal | MF/U c,d,e | U f,g | MF k | African wild dogs c | Immobility c,e | ||
1-Octanol | MF c,e | MF k,l | Foraging, Alarm recruitment, Sensory perception c,e | ||||
2,5-Dimethylpyrazine | MF c,e | MF l | African wild dogs, Wolf, House mouse, Tree shrew c,o,p | Fear, Freezing, Aggression, Lengthens oestrus cycle, Delays puberty in both sexes, Overmarking c,e,o,p | |||
2-Butanone | MF/U c,d,e | U f,g | MF l | Sexuality c,e | |||
2-Nonanone | MF c,e | U f,g | MF k,l | Sex attraction c,e | |||
2-Pentanone | MF/U c,d,e | U f,g | Reproduction, Concentration c,e | ||||
3-Methylbutanal | MF/U c,d,e | MF l | Attraction c,e | ||||
3-Methylcyclopentanone | MF c | U f,g | Badgers c | Seasonal reproduction c | |||
4-Heptanone | U d | U f,g | MF l | Red fox p | Overmarking p | ||
4-Methylphenol | MF c,e | MF l | Wild Iberian wolves, Horse c,q,p | Sexuality, Estrus, Oestrus, Diestrus, Sexual attraction c,e,q,p | |||
Acetaldehyde | MF c,e | MF i,j | MF m | Locomotion, Taste aversion, Anxiety c,e | |||
Acetic acid | MF c,e | MF h | MF i | MF m,j,k | African wild dogs c | Detector of estrus, copulation, Oestrus, Attraction, Flight c,e | |
Acetone | MF/U c,d,e | MF i,j | MF m,l | Locomotion, Sexuality, Irritation c,e | |||
Acetophenone | MF c,e | U f,g | MF k | African wild dogs, Fox c,p | Anti-attraction, Attraction, Responsiveness, Stimulates overmarking c,e, p | ||
Benzaldehyde | MF/U c,d,e | U f,g | MF k,l | African wild dogs c | Oviposition, Defensive, Aggression, Alarm recruitment, Affects sexual behaviour c,e, r | ||
Butyrolactone | MF c,e | Appetite, Vomiting, and Tremor Suppression, Estrus c,e | |||||
Cyclohexanone | MF c,e | U f,g | Asian elephant p | Attraction, Locomotion, Stimulation, Inhibition c,e,p | |||
Dimethyl disulfide | MF/U c,d,e | U f,g | MF l | Oviposition inhibition, Attraction, Sniffing c,e | |||
Dodecan-4-olide | MF k | Overmarking behaviour k | |||||
Dodecanal | MF c,e | African wild dogs c | Physiological responses c,e | ||||
Heptanal | MF/U c,d,e | MF k | Aggregation, Inhibited behavior, Excitation c,e | ||||
Indole | U a | MF c,e | MF l | African wild dogs, wild Iberian wolvs c | Sexuality, Age differentiation c,e,a | ||
Linalool | MF c,e | Alarm recruitment, Attraction c,e | |||||
Nonanal | MF/U c,d,e | U f,g | MF k,l | African wild dogs c | Sexual attraction c,e | ||
Phenol | MF c,e | U f,g | MF k,l | African wild dogs, wild Iberian wolves c | Estrus, Oestrus, Sexuality c,e | ||
Phenylacetic acid | MF k | Male Mongolian gerbil p | Overmarking p | ||||
Propanoic acid | MF k | Rat p | Signals estrus, Induces erections p | ||||
Squalene | MF k | Rat p | Attraction p | ||||
Trimethylamine | MF/U c,d,e | MF i | MF n,l | Mouse p | Species-specific attractant p | ||
Valeric acid | VS b | MF h | MF i | MF m,j,l | Attractiveness, Greatly affects behaviour (males and females), Estrus, Oestrus onset b |
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 (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tommasi, A.; Koziel, J.A.; Molotsi, A.H.; Esposito, G. Understanding the Role of Semiochemicals on the Reproductive Behaviour of Cheetahs (Acinonyx jubatus)—A Review. Animals 2021, 11, 3140. https://doi.org/10.3390/ani11113140
Tommasi A, Koziel JA, Molotsi AH, Esposito G. Understanding the Role of Semiochemicals on the Reproductive Behaviour of Cheetahs (Acinonyx jubatus)—A Review. Animals. 2021; 11(11):3140. https://doi.org/10.3390/ani11113140
Chicago/Turabian StyleTommasi, Alexia, Jacek A. Koziel, Annelin H. Molotsi, and Giulia Esposito. 2021. "Understanding the Role of Semiochemicals on the Reproductive Behaviour of Cheetahs (Acinonyx jubatus)—A Review" Animals 11, no. 11: 3140. https://doi.org/10.3390/ani11113140