Skip to main content
View expanded cover

Chemical Signals in Vertebrates 12 pp 171–184Cite as

Hemiterpenoids and Pyrazines in the Odoriferous Urine of the Maned Wolf (Chrysocyon brachyurus)

Abstract

Maned wolves (Chrysocyon brachyurus) are endemic to South America, monogamous, solitary, and threatened in the wild. Maned wolf urine has a pungent and powerful odour and is used for scent marking. There is evidence to suggest that the presence of a male may be required to initiate oestrus and/or ovulation, thus implying the presence of a primer pheromone. We have employed solid phase dynamic extraction (SPDE)/GC-MS to identify a number of volatile compounds in maned wolf urine. These include sulphur-containing hemiterpenoids which are predominantly responsible for the distinctive urinary odour, hemiterpenoid alcohols which are known bark beetle pheromones, and a variety of pyrazines, some of which are known to be insect pheromones. Hemiterpenoids are most likely biosynthesised via a shunt of the mevalonate pathway, while pyrazines are thought to be products of amino acid metabolism. The abundance of some of these compounds increases as the urine ages, perhaps providing a timed release of putative chemical signals.

Keywords

  • Volatile Organic Compound
  • Gray Wolf
  • Roasted Coffee
  • Isopentenyl Diphosphate
  • Isopentenyl Pyrophosphate

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

This is a preview of subscription content, access via your institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • DOI: 10.1007/978-1-4614-5927-9_13
  • Chapter length: 14 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   149.00
Price excludes VAT (USA)
  • ISBN: 978-1-4614-5927-9
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Softcover Book
USD   199.99
Price excludes VAT (USA)
Hardcover Book
USD   249.99
Price excludes VAT (USA)
Learn about institutional subscriptions
Fig. 13.1
Fig. 13.2
Fig. 13.3

References

  • Albone ES (1984) Mammalian semiochemistry. Wiley-Interscience, New York

    Google Scholar 

  • Albone ES, Gosden PE, Ware GC (1977) Bacteria as a source of chemical signals in mammals. In: Müller-Schwarze D, Mozell MM (eds) Chemical signals in vertebrates. Plenum Press, New York, pp 35–43

    CrossRef  Google Scholar 

  • Asa CS, Mech LD, Seal US (1984) The use of urine, feces, and anal-gland secretions in scent marking by a captive wolf (Canis lupus) pack. Anim Behav 33:1034–1036

    CrossRef  Google Scholar 

  • Bakke A, Frøyen P, Skattebøl L (1977) Field response to a new pheromonal compound isolated from Ips typographus. Naturwissenschaften 64:98–99

    CrossRef  CAS  Google Scholar 

  • Berg JM, Tymoczko JL, Stryer L, Gatto GJ Jr (2012) Biochemistry. W.H. Freeman, New York

    Google Scholar 

  • Bestelmeyer SV (2000) Solitary, reproductive and parental behaviors of maned wolves (Chrysocyon brachyurus). PhD Thesis, Colorado State University, Fort Collins, Colorado, USA

    Google Scholar 

  • Bovée KC, Bush M, Dietz J, Jezyk P, Segal S (1981) Cystinuria in the maned wolf of South America. Science 212:919–920

    PubMed  CrossRef  Google Scholar 

  • Boyer ML, Jemiolo B, Andreolini F, Wiesler D, Novotny M (1989) Urinary volatile profiles of pine vole, Microtus pinetorum, and their endocrine dependency. J Chem Ecol 15:649–662

    CrossRef  CAS  Google Scholar 

  • Brophy JJ (1989) Pyrazines obtained from insects: their source, identification, synthesis and function. In: Atta-ur-Rahman (ed) Studies in natural products chemistry, Vol. 5, structure elucidation (Part B). Elsevier, Amsterdam, p 221–293

    Google Scholar 

  • Burger BV, Pretorius PJ (1988) Mammalian pheromone studies, VI. Compounds from the preorbital gland of the blue duiker, Cephalophus monticola. Z Naturforsch 42c:1355–1357

    Google Scholar 

  • Burns CS, Heyerick A, De Keukeleire D, Forbes MDE (2001) Mechanism for formation of the lightstruck flavor in beer revealed by time-resolved electron paramagnetic resonance. J Chem Eur 7:4553–4561

    CrossRef  CAS  Google Scholar 

  • Cane DE (1999) Isoprenoid biosynthesis: overview. In: Barton D, Nakanishi K, Meth-Cohn O (eds) Comprehensive natural products chemistry, Vol. 2: isoprenoids including carotenoids and steroids. Elsevier, Amsterdam, pp 1–13

    CrossRef  Google Scholar 

  • Childs-Sanford SE (2005) The captive maned wolf (Chrysocyon brachyurus): nutritional considerations with emphasis on management of cystinuria. M.S. Thesis, University of Maryland, College Park, Maryland, USA

    Google Scholar 

  • Chuman T, Landolt PJ, Heath RR, Tumlinson JH (1987) Isolation, identification, and synthesis of male-produced sex pheromone of papaya fruit fly, Toxotrypana curvicauda Gerstaecker (Diptera: Tephritidae). J Chem Ecol 13:1979–1992

    CrossRef  CAS  Google Scholar 

  • DelBarco-Trillo J, Burkert BA, Goodwin TE, Drea CM (2011) Night and day: the comparative study of strepsirrhine primates reveals socioecological and phylogenetic patterns in olfactory signals. J Evol Biol 24:82–98

    PubMed  CrossRef  CAS  Google Scholar 

  • Dickschat JS, Wickel S, Bolten CJ, Nawrath T, Schulz S, Wittmann C (2010) Pyrazine biosynthesis in Corynebacterium glutamicum. Eur J Org Chem 2687–2695

    Google Scholar 

  • Dietz JM (1984) Ecology and social organization of the maned wolf (Chrysocyon brachyurus). Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Dietz JM (1985) Chrysocyon brachyurus. Mammal Spec 234:1–4

    CrossRef  Google Scholar 

  • Francke W (1991) Semiochemicals: mevalogenins in systems of chemical communication. In: Muller PM, Lamparsky D (eds) Perfumes: art, science and technology. Elsevier, London and New York, pp 61–99

    Google Scholar 

  • Francke W, Schulz S (1999) Pheromones. In: Barton D, Nakanishi K, Meth-Cohn O, Mori K (eds) Comprehensive natural products chemistry, Vol. 8: miscellaneous natural products including marine natural products, pheromones, plant hormones, and aspects of ecology. Elsevier, Amsterdam, pp 197–261

    Google Scholar 

  • Goodwin TE, Schulte BA (2009) Prospecting for mammalian chemical signals via solventless extraction techniques: an elephantine task. ChemoSense 11:9–15

    Google Scholar 

  • Goodwin TE, Rasmussen LEL, Schulte BA, Brown PA, Davis BL, Dill WM, Dowdy NC, Hicks AR, Morshedi RG, Mwanza D, Loizi H (2005) Chemical analysis of preovulatory female African elephant urine: a search for putative pheromones. In: Mason RT, LeMaster MP, Müller-Schwarze D (eds) Chemical signals in vertebrates 10. Springer Press, New York, pp 128–139

    CrossRef  Google Scholar 

  • Goodwin TE, Eggert MS, House SJ, Weddell ME, Schulte BA, Rasmussen LEL (2006) Insect pheromones and precursors in female African elephant urine. J Chem Ecol 32:1849–1853

    PubMed  CrossRef  CAS  Google Scholar 

  • Goodwin TE, Brown PA, Eggert MS, Evola MG, House SJ, Morshedi RG, Weddell ME, Chen CJ, Jackson SR, Aubut Y, Eggert J, Schulte BA, Rasmussen LEL (2007) Use of automated solid phase dynamic extraction (SPDE)/GC-MS and novel macros in the search for African elephant pheromones. In: Hurst J, Beynon R, Wyatt T, Roberts C (eds) Chemical signals in vertebrates 11. Springer Press, New York, pp 25–35

    Google Scholar 

  • Goodwin TE, Broederdorf LJ, Burkert BA, Hirwa HH, Mark DB, Waldrip ZJ, Kopper RA, Sutherland MV, Freeman EW, Hollister-Smith JA, Schulte BA (2012) Chemical signals of elephant musth: temporal aspects of microbially-mediated modifications. J Chem Ecol 38:81–87

    PubMed  CrossRef  CAS  Google Scholar 

  • Gros J, Nizet S, Collin S (2009) Hop allylic alcohols are precursors of sulfur-containing odorants in fresh beer. Acta Hortic 848:273–278

    CAS  Google Scholar 

  • Guilford T, Nicol C, Rothschild M, Moore BP (1987) The biological roles of pyrazines: evidence for a warning odour function. J Linn Soc 31:113–128

    CrossRef  Google Scholar 

  • Helsper JPFG, Bucking M, Muresan S, Blaas J, Wietsma WA (2006) Identification of the volatile component(s) causing the characteristic foxy odor in various cultivars of Fritillaria imperialis L. (Liliaceae). J Agric Food Chem 54:5087–5091

    PubMed  CrossRef  CAS  Google Scholar 

  • Holscher W, Vitzthum OG, Steinhart H (1992) Prenyl alcohol—source for odorants in roasted coffee. J Agric Food Chem 40:655–658

    CrossRef  CAS  Google Scholar 

  • Hughes MN, Centelles MN, Moore KP (2009) Making and working with hydrogen sulfide, the chemistry and generation of hydrogen sulfide in vitro and its measurement in vivo: a review. Free Radic Biol Med 47:1346–1353

    PubMed  CrossRef  CAS  Google Scholar 

  • Jácomo ATDA, Kashivakura CK, Ferro C, Furtado MM, Astete SP, Tôrres NM, Sollmann R, Silveira L (2009) Home range and spatial organization of maned wolves in the Brazilian grasslands. J Mammal 90:150–157

    CrossRef  Google Scholar 

  • Jemiolo B, Novotny M (1993) The long-term effect of a urinary chemosignal on reproductive fitness in female mice. Biol Reprod 48:926–929

    PubMed  CrossRef  CAS  Google Scholar 

  • Jorgensen JW, Novotny M, Carmack M, Copland GB, Wilson SR (1978) Chemical scent constituents in the urine of the red fox (Vulpes vulpes L.) during the winter season. Science 199:796–798

    CrossRef  Google Scholar 

  • Kelly DR (1996) When is a butterfly like an elephant? Chem Biol 3:595–602

    PubMed  CrossRef  CAS  Google Scholar 

  • Kleiman DG (2011) Canid mating system, social behavior, parental care and ontogeny: are they flexible? Behav Genet 41:803–809

    PubMed  CrossRef  Google Scholar 

  • Krohn S, Fletcher MT, Kitching W, Moore CJ, Drew RAI, Francke W (1992) Chemistry of fruit flies: glandular secretion of Bactrocera (Polistomimetes) visenda (Hardy). J Chem Ecol 18:2169–2176

    CrossRef  CAS  Google Scholar 

  • Lanne BS, Ivarsson P, Johnsson P, Bergström G, Wassgren A-B (1989) Biosynthesis of 2-methyl-3-buten-2-ol, a pheromone component of Ips typographus (Coleoptera: Scolytidae). Insect Biochem 19:163–167

    CrossRef  CAS  Google Scholar 

  • Mattoo A, Goldfarb DS (2008) Cystinuria Semin. Nephrology 28:181–191

    CAS  Google Scholar 

  • Moir M, Gallacher IM, Seaton JC, Suggett A (1980) Terpene methyl sulphides in the essential oil of hops. Chem Ind, London, pp 624–625

    Google Scholar 

  • Morgan ED (2009) Trail pheromones of ants. Physiol Entomol 34:1–17

    CrossRef  CAS  Google Scholar 

  • Mueller EG, Palenchar PM, Buck CJ (2001) The role of the cysteine residues of ThiI in the generation of 4-thiouridine in tRNA. J Biol Chem 276:33588–33595

    PubMed  CrossRef  CAS  Google Scholar 

  • Nawrath T, Dickschat JS, Kunze B, Schulz S (2010) The biosynthesis of branched dialkylpyrazines in myxobacteria. Chem Biodivers 7:2129–2144

    PubMed  CrossRef  CAS  Google Scholar 

  • Obata Y, Tanaka H (1965) Studies of the sunlight flavor of beer Part IX. Formation of prenylmercaptan from S-prenyl-L-cysteine by sunlight. Agric Biol Chem 29:104–107

    CrossRef  CAS  Google Scholar 

  • Rasmussen LEL (1998) Chemical communication: an integral part of functional Asian elephant (Elephas maximus) society. Ecoscience 5:410–426

    Google Scholar 

  • Raymer JH (1984) Investigation into the chemical nature of chemo-olfactory communication in the wolf (Canus lupus). PhD Thesis, Indiana University, Bloomington, Indiana, USA

    Google Scholar 

  • Raymer J, Wiesler D, Novotny M, Asa C, Seal US, Mech LD (1984) Volatile constituents of wolf (Canis lupus) urine as related to gender and season. Experiencia 40:707–709

    CrossRef  CAS  Google Scholar 

  • Raymer J, Wiesler D, Novotny M, Asa C, Seal US, Mech LD (1986) Chemical scent constituents in urine of wolf (Canis lupus) and their dependence on reproductive hormones. J Chem Ecol 12:297–314

    CrossRef  CAS  Google Scholar 

  • Rizzi GP (1988) Formation of pyrazines from acyloin precursors under mild conditions. J Agric Food Chem 36:349–352

    CrossRef  CAS  Google Scholar 

  • Rizzi GP (1995) Formation of sulfur-containing flavor compounds from allylic alcohol precursors. Dev Food Sci 37:289–302

    CrossRef  Google Scholar 

  • Rodden MD, Sorenson LG, Sherr A, Kleiman DG (1996) Use of behavioral measures to assess reproductive function in maned wolves (Chrysocyon brachyurus). Zoo Biol 15:565–585

    CrossRef  Google Scholar 

  • Rodden M, Rodrigues F, Bestelmeyer S (2004) Maned wolf (Chrysocyon brachyurus). In: Sillero-Zubiri C, Hoffman M, Macdonald DE (eds) Canids: foxes, wolves, jackals and dogs. Status survey and conservation action plan. IUCN/SSC Canid Specialist Group, Gland, Switzerland and Cambridge, UK, pp 38–43

    Google Scholar 

  • Roussel-UCLAF patent application (1966) Cyclic sulfones. Chem Abstr 64:15849h

    Google Scholar 

  • Schildknecht H, Birkner C, Krauß D (1981) Struktur und wirkung der musteliden-ökomone II. Erweiterte analyse des analbeutelsekretes des nerzes Mustela vison L. Chem Ztg 105:273–286

    CAS  Google Scholar 

  • Schultz TH, Flath RA, Stern DJ, Mon TR, Teranishi R, Kruse SM, Butler B, Howard WE (1988) Coyote estrous urine volatiles. J Chem Ecol 14:701–712

    CrossRef  CAS  Google Scholar 

  • Schwende FJ, Weisler D, Jorgensen JW, Carmack M, Novotny M (1986) Urinary volatile constituents of the house mouse, Mus musculus, and their endocrine dependency. J Chem Ecol 12:277–296

    CrossRef  CAS  Google Scholar 

  • Senger-Emonnot P, Rochard S, Pellegrin F, George G, Fernandez X, Lizzani-Cuvelier L (2006) Odour active aroma components of sea fig (Microcosmus sulcatus). Food Chem 97:465–471

    CrossRef  CAS  Google Scholar 

  • Seybold SJ, Vanderwel D (2003) Biosynthesis and endocrine regulation of pheromone production in the Coleoptera. In: Bloomquist G, Vogt R (eds) Insect pheromone biochemistry and molecular biology. Elsevier, Amsterdam, pp 137–200

    CrossRef  Google Scholar 

  • Sokolov VE, Albone ES, Flood PF, Heap PF, Kagan MZ, Vasilieva VS, Roznov VV, Zinkevich EP (1980) Secretion and secretory tissues of the anal sac of the mink, Mustela vison. J Chem Ecol 6:805–825

    CrossRef  CAS  Google Scholar 

  • Songsasen N, Rodden M, Brown JL, Wildt DE (2006) Patterns of fecal gonadal hormone metabolites in the maned wolf (Chrysocyon brachyurus). Theriogenology 66:1743–1750

    PubMed  CrossRef  CAS  Google Scholar 

  • Stoakley JT, Bakke A, Renwick JAA, Vité JP (1978) The aggregation pheromone of the larch bark beetle, Ips cembrae Heer. J Appl Entomol 86:174–176

    Google Scholar 

  • Teague B, Asiedu S, Moore PK (2002) The smooth muscle relaxant effect of hydrogen sulphide in vitro: evidence for a physiological role to control intestinal contractility. Br J Pharmacol 137:139–145

    PubMed  CrossRef  CAS  Google Scholar 

  • Toftegaards CL, Moore C, Bradley AJ (1999) Chemical characterization of urinary pheromones in brown antechinus, Antechinus stuartii. J Chem Ecol 25:527–535

    CrossRef  CAS  Google Scholar 

  • Vieth HJ, Koeniger N, Maschwitz U (1984) 2-Methyl-3-butene-2-ol, a major component of the alarm pheromone of the hornet Vespa crabro. Naturwissenschaften 71:328–329

    CrossRef  Google Scholar 

  • Wang R (2002) Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16:1792–1798

    PubMed  CrossRef  CAS  Google Scholar 

  • Wilson SR, Carmack M, Novotny M, Jorgenson JW, Whitten WK (1978) D3-Isopentyl methyl sulfide. A new terpenoid in the scent mark of the red fox (Vulpes vulpes). J Org Chem 43:4675–4676

    CrossRef  CAS  Google Scholar 

  • Wood WF, Walsh A, Seyjagat J, Weldon PJ (2005) Volatile compounds in shoulder gland secretions of male flying foxes, genus Pteropus (Pteropodidae, Chiroptera). Z Naturforsch C 60:779–784

    PubMed  CAS  Google Scholar 

  • Woolfson A, Rothschild M (1990) Speculating about pyrazines. Proc R Soc Lond B 242:113–119

    CrossRef  CAS  Google Scholar 

  • Woolhouse AD, Morgan DR (1995) An evaluation of repellents to suppress browsing by possums. J Chem Ecol 21:1571–1583

    CrossRef  CAS  Google Scholar 

  • Zhang JX, Soini HA, Bruce KE, Wiesler D, Woodley SK, Baum MJ, Novotny MV (2005) Putative chemosignals of the ferret (Mustela furo) associated with individual and gender recognition. Chem Senses 30:727–737

    PubMed  CrossRef  CAS  Google Scholar 

  • Zlatkis A, Bertsch W, Lichtenstein HA, Tishbee A, Shunbo F, Liebich HM, Coscia AM, Fleischer N (1973) Profile of volatile metabolites in urine by gas chromatography–mass spectrometry. Anal Chem 45:763–767

    PubMed  CrossRef  CAS  Google Scholar 

Download references

Acknowledgements

Urine samples were provided by the Center for Species Survival, Smithsonian Conservation Biology Institute, and the Little Rock Zoo. We thank Paul Caster of the Little Rock Zoo for assistance in urine collection. We are grateful for the hemiterpenoid and pyrazine samples that were provided by Joe Brophy, Doug Crump, Peter Schieberle, and Tony Woolhouse. TEG appreciates financial support provided by the Hendrix College Odyssey Program, Julia Mobley, and John and Laura Byrd. Funding was provided by the U.S. National Science Foundation for the GC-MS (NSF CRUI grant to T.E.G., Bruce Schulte, and the late L.E.L. Rasmussen, Award Nos. 02-17062, -17068 and -16862, respectively) and the NMR spectrometer (NSF MRI grant to Hendrix College, Award No. 1040470).

Author information

Authors and Affiliations

  1. Department of Chemistry, Hendrix College, Conway, AR, 72032, USA

    Thomas E. Goodwin, Laura J. Broederdorf, Blake A. Burkert, C. Joi Chen, Stephen R. Jackson, K. Bryan Keplinger, Margaret E. Rountree, Zach J. Waldrip, Margaret E. Weddell & Linda P. Desrochers

  2. Department of Reproductive Sciences, Center for Species Survival, Smithsonian Conservation Biology Institute, Front Royal, VA, 22630, USA

    Nucharin Songsasen

  3. Little Rock Zoo, Little Rock, AR, 72205, USA

    William K. Baker Jr.

  4. Panthera Research, Rockwall, TX, 75032, USA

    William K. Baker Jr.

  5. Business Unit Bioscience, Plant Research International, Wageningen, The Netherlands

    Johannes P. F. G. Helsper

Authors
  1. Thomas E. Goodwin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nucharin Songsasen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura J. Broederdorf
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Blake A. Burkert
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. Joi Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stephen R. Jackson
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. K. Bryan Keplinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Margaret E. Rountree
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zach J. Waldrip
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Margaret E. Weddell
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Linda P. Desrochers
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. William K. Baker Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Johannes P. F. G. Helsper
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas E. Goodwin .

Editor information

Editors and Affiliations

  1. , Department of Evolutionary Ecology, Leibniz Institute for Zoo and Wildlife R, Im Forschungsverbund Berlin e.V, Berlin, 10252, Berlin, Germany

    Marion L East

  2. , Department of Reproduction Biology, Leibniz Institute for Zoo and Wildlife R, Im Forschungsverbund Berlin e.V, Berlin, 10252, Germany

    Martin Dehnhard

Rights and permissions

Reprints and Permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Goodwin, T.E. et al. (2013). Hemiterpenoids and Pyrazines in the Odoriferous Urine of the Maned Wolf (Chrysocyon brachyurus). In: East, M., Dehnhard, M. (eds) Chemical Signals in Vertebrates 12. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5927-9_13

Download citation