Chemical Communication in Mammals

A Review

 

 

 

 

 

 

 

 

 

 

 

 

 

Felicity May

CSUCat@hotmail.com

Colorado State University

April 12, 2002

Abstract

Presented here is a summary of the current position on chemical communication in mammals.  This summary combines information of the anal sac secretions of the red fox, Vulpes vulpes, the lion, Panthera leo, the European badger, Meles meles, and the mink, Mustela vison, with the chemical signals of the ringed seal, Phoca hispida, the brown hyena, Hyaena brunnea, and the koala, Phascolarctos cinereus.  Discussed are the similarities and differences among chemical signals and how they are used.  The most notable of these being the use of putrescine (1,4-diaminobutane) in the lion, fox, and mink and the use of nitriles in koalas.  The chemicals from the mink were tested as deterrents for the mountain beaver.  The application of these signals to the fermentation hypothesis of chemical recognition is looked at in depth. 

 

Introduction

The way animals communicate has always been a curiosity of mankind.  This has been shown in the movies, with Dr. Dolittle and Tarzan, and in the scientific community, with the accumulation of papers published.  Visual and acoustic methods of communication have been long studied, but odor communication has only been seriously studied in the last 40 years.  Some believe that the role of olfaction in communication is, in evolutionary terms, a secondary development.  In the class of mammals, the olfactory sense is extremely sensitive and appears to be highly developed as shown in Figure 11.  The importance of these chemical signals has become evident in studies from around the globe.  Here I strive to bring together information on nine different mammals from around the globe in a comparison of the chemicals they use in communication.  Russian and English Mink, English badgers and red fox, American beavers, Norwegian seals, African hyena and Australian koalas are the mammals investigated. 

 

General use of chemical signals

There are two very general types of chemical signals: range markings, where a signal is emitted into the environment and may later be investigated in the absence of the signaler, or as signals emitted in the presence of the receiver, these include sex attractants, recognition signals and alarms signals.  There are four variables in the use of any chemical signal: the amount of material release, the concentration threshold necessary by the receiver, the diffusion coefficient of the molecules released, and the environment the signal is released into.  The different types of chemical signals need to possess different physical properties in order to function appropriately.  Therefore, it should be possible to map signals based on their physical properties.  For example, alarm signals should be highly volatile, so they do not remain in the environment too long.  Conversely, range marks should be relatively non-volatile and resist degradation so that they will persist after the signaler leaves.  A significant difference was found in the molecular weight for signals that were used in different social contexts, as shown in Table 1.2

 

Origin of the chemical signals

The animal body varies from species to species, but there are some similar scent organs that are common through out the kingdom.  Listed in Table 1 is a sample of scent glands that are used by a range of animals.  There is a broad range of glands, as shown in Table 2, but the most common is the anal gland, with only four of the 231 species of carnivore lacking them.  Most of the animals discussed here will use this type gland.  The anal sac consists of two organs, one on either side of the anus, which drain into ducts that may open either internally or externally to the anal orifice.  These organs serve as reservoirs for secretions of apocrine and sebaceous cells3.  They are also a moist, warm, and enclosed environment that supports an abundant microflora4.  The other two glands reviewed are the large sternal gland of the koala, Phascolarctos cinereus, and the facial gland of ringed seal, Phoca hispida.  For koalas and seals, the glands are isolated to the male of species.

 

Anal sac secretions

The red fox, Vulpes vulpes, is a solitary carnivore whose secretions have been studied in depth.  The anal glands of the red fox secrete a variety of fatty acids and sulfur compounds.  The concentration of these compounds varied from animal to animal, starting at about 6mM and ranging to 146mM.  The pH of the samples varied as well, from 6.5-9.4.  The most prominent compounds are putrescine (1,4-diaminobutane) and cadaverine (1,5-diaminopentane).  The fatty acids present in the sample were found in the odorless form and are acetic acid, propionic acid, n-butyric acid, isobutyric acid, isovaleric acid, and isocaproic acid.  Ammonia was the only other non fatty acid besides putrecine and cadaverine.  It has been reported that the anal sac secretions of the lion, Panthera leo, also contain putrecine and cadaverine.5

 

The European badger, Meles meles, is a social omnivore that lives in groups of four to twelve.  It has anal glands that are just internal to the anus and consists of both sebaceous and apocrine tissue.  The sacs produce a strong smelling orange-colored liquid.  For the twenty animals studied the scent profiles were very similar. The secretions contained no volatile fatty acids of low molecular weight, but did contain high molecular weight fatty acids of low volatility.  These acids consist of palmitic acid, stearic acid, oleic acid, linoleic acid, and eicosatrienoic acid.  The scent profile was also stable over time.  The secretions themselves did not depend on the size of the animal or whether the animal was male or female.  The secretions did change when different populations were compared6.  The location of the secretions in the environment supported the idea that they are used to identify different groups of animals.

 

The brown hyena, Hyaena brunnea, is a social scavenger that lives in multimale packs of 4 to 14.  The anal sac of this animal secretes two distinct, strong smelling substances.  A white substance produced by the sebaceous tissue of the anal sac contains mostly free lipid with a small amount of polysaccharides.  A black substance is produced by the aprocrin tissue, and contains mostly lipo-fuschin and polysaccharides, with aldehydes and acid mucopolysaccharides in smaller quantities.  Individual compounds within the secretions have not been identified, but the concentration differences between animals suggest that the secretions are used to identify individual animals.7

 

The American mink, Mustela vison, is a semiaquatic carnivore that is solitary throughout most of the year, only forming pairs in the breeding season.  The anal sac secretions of the mink are released in aggressive encounters.  The identified compounds in the secretion are 5-aminovaleric acid, putrescine, indole and 2-2-dimethylthietane (DMT)4,8.  Other compounds were shown to be trimethylamines and triethylamines.  The secretions from the mink were tested as a feeding repellant for the mountain beaver, Aplodontia rufa.  DMT was found not to be any form of repellent for the beaver.9

 

Other scent glands

The Australian koala, Phascolarctos cinereus, is an arboreal vegetarian, spending most of its time sleeping.  The sternal gland is located in the subcutaneous tissue of the male chest, and not found in females.  The males rub their chest on the trunks and branches of trees to mark their territory.  The yellow secretion turns the cream white fur of the chest a dirty brown to ginger color.  The secretion is a complex mixture containing predominantly fatty acids, aldehydes, ketones, sesquiterpines, and some nitriles and oximes.  A complete list is given in Table 3.  The most abundant nitrile in the secretion was identified as benzyl cyanide.  This compound was first identified in the chest gland secretion of the male African great bushbaby, Galago crassicaudarus.  Benzyl cyanide was not among the most abundant components in the entire solution, which were syn- and anti-phenylacetaldehyde oxime, acetic acid, 2-methylbutanoic acid, nonanal, aromadendrene, and C16 ketone.10

 

 The ringed seal, Phoca hispida, is an asocial animal. Adult seals are solitary except for loose feeding aggregations in the water in summer.  During the breeding season mature males secretes a substance from their face that has earned them the name ‘gasoline seal’ because of its foul smell.  The glands only produce the odor during the time when they are defending territory.  The most prominent components of the extract were found to be N-ethyl-N-methyl ethanamine, 3-methylbutan-1-thiol, dodecyl cyclohexane, pentylamino nonanol, and pentylamino undecanol.  DMT (2-2-dimethylthietane) and eicosatrienoic acid were also identified in the samples.11

 

Fermentation hypothesis of chemical recognition

This hypothesis was originally presented by ML Gorman in 1976.  The idea offers a possibility of how a group of animals can use their microflora as a means of group identification.  It is known that characteristically different volatile metabolite profiles are produced by different strains of microorganism incubated under standard condition.  This raises the idea that a group of animals in close contact can cross-infect each other with their microflora, until they all share a common assortment.  It has been proven that part of the anal sac secretion of the Indian mongoose originates with the microflora, as specific fatty acids are not produced in the presence of penicillin.  Problems with this idea arise when it is considered that the length of microbial incubation can affect the volatile profile.4  It has been shown that in the red fox the pH range for the anal sac secretions varies greatly (6.5-9.4) with in a social group.  It was also noted that the two sacs of the red fox are not emptied to the same extent with each secretion.  There is an obvious similarity in the compounds identified in the mink and the red fox.  There are at least six chemicals found in both animals.  The similarity of the secretions, the pH differences among animals of the same group, and the variability of the left or right sac secretions all combine as evidence against a fermentation hypothesis by microflora as a means of chemical recognition.6

 

Conclusions

The use of chemical signals is a widely studied process.  There is a great range of chemicals used as signals, yet there are also compounds that are common among different species of mammals.  The anal sac secretion can be used as alarm mechanism, for the solitary animal or territory marking, for the social animal.  Gorman’s fermentation hypothesis does offer a rather attractive theory for how a community of animals can recognize their group members, but lacks supporting evidence.  More work needs to be done in determining what microflora are actually present in the groups of animals and how they differ among different communities.  When that has been determined it will refute or support the theory.  At the moment, the chemical profiles of the secretions is known, and when those signals are used is known.  The purpose and the origin of the signals has yet to be determined.

Ref. 2
 
 

 


Figure 1: Sagittal section of a rabbit’s head showing the appearance of the right nasal cavity after removal from the septum.  Stripping denoted the extent of the olfactory epithelium1

 

Table 2

Review of species and type of glands present.2

 

Table 3:

Compounds identified in the sternal gland secretion of the koala.11

References

  1. Stoddart, DM. Mammalian Odours and Pheromones.  Southampton: The Camelot Press Ltd, 1976.
  2. Alberts, A.C. 1992. Constraints on the design of chemical communication systems in terrestrial vertebrates.  Am. Nat. 139:S62-S89.
  3. Brown, Richard and Macdonald, David, eds.  Social odours in mammals.  New York: Oxford University Press, 1985.
  4. Albone, E.S. Mammalian Semiochemistry: The investigation of chemical signals between mammals.  Chichester: John Wiley & Sons Ltd, 1984.
  5. Albone, E.S., Perry, G.C.  1975.  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.  2:101-111.
  6. Davis, JM., Lachno, DR., Roper, TJ. 1988. The anal gland secretion of the European Badger (Meles meles) and its role in social communication. J. Zool., Lond. 216:455-463.
  7. Mills, MGL., Gorman, ML., Mills, MEJ.  1980.  The scent marking behaviour of the brown hyaena Hyaena brunnea.  S.Afr. J. Zool. 15:240-248.
  8. Sokolov, V.E., Albone, E.S., et al. 1980.  Secretion and secretory tissues of the anal sac of the mink, Mustela vison.  J. Chem. Ecol. 6:805-825.
  9. Epple, G., Mason, J.R. et al.  1995. Feeding responses to predator-based repellents on the mountain beaver (Apolodontia rufa).  Ecol. Appl. 5:1163-1170.
  10. Salamon, M., Davies, N.W.  1998.  Identification and variation of volatile compounds in sternal gland secretions of male koalas (Phascolarctos cinereus). J. Chem. Ecol. 24:1659-1676.
  11. Ryg, M., Solberg, Y. et al.  1992. The scent of rutting male ringed seals (Phoca hispida).  J. Zool. Lond. 226:681-689.