Volatiles and Tannins in Pistacia lentiscus and Their Role in Browsing Behavior of Goats (Capra hircus)

  • 81 Accesses


Goat herding is an important tool in the ecologically sound management of Mediterranean shrublands and woodlands, although effective levels of woody biomass removal by the goats is neither guaranteed nor easy to predict. Preliminary observations indicated that one reason for this may be poor understanding of plant-herbivore interactions that operate intraspecifically at the local spatial scale. We asked, whether goats show intraspecific preferences among neighboring plants when foraging a small local population of Pistacia lentiscus, a dominant tall shrub. First, we characterized and quantified the profile of stored and emitted volatile organic compounds (VOCs) and the PEG-binding capacity of tannins (a proxy for protein binding capacity) in the foliage of P. lentiscus shrubs, sampled within an area of 0.9 ha. We then tested goat preference between pairs of these shrubs that differed in chemical composition. Almost all sampled P. lentiscus shrubs were allocated to one of two distinct VOC chemotypes: one dominated by germacrene D and limonene (designated chemotype L) and the other by germacrene D and α-pinene (chemotype P). In contrast, continuous moderate variability was found in the binding capacity of tannins in the foliage. Goats showed preference for shrubs of chemotype L over those of chemotype P, and their preference was negatively correlated with the binding capacity of tannins. Possible influences of VOCs on goat preference that may explain the observed patterns are discussed in the light of possible context-dependent interpretation of plant VOC signals by large mammalian herbivores.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5


  1. Adams RP (2001) Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy. Allured Publishing Corporation, Carol Stream

  2. Andrew RL, Peakall R, Wallis IR, Foley WJ (2007) Spatial distribution of defense chemicals and markers and the maintenance of chemical variation. Ecology 88:716–728

  3. Arviv A, Muklada H, Kigel J, Voet H, Glasser T, Dvash L, Ungar ED, Landau SY (2016) Targeted grazing of milk thistle (Silybum marianum) and Syrian thistle (Notobasis syriaca) by goats: preference following preconditioning, generational transfer, and toxicity. Appl Anim Behav Sci 179:53–59

  4. Baldwin IT (2010) Plant volatiles. Curr Biol 20:R392–R397

  5. Bar Massada A, Gabay O, Perevolotsky A, Carmel Y (2008) Quantifying the effect of grazing and shrub-clearing on small-scale spatial pattern of vegetation. Landsc Ecol 23:327–339

  6. Baraza E, Hódar JA, Zamora R (2009) Consequences of plant–chemical diversity for domestic goat food preference in Mediterranean forests. Acta Oecol 35:117–127

  7. Barra A, Coroneo V, Dessi S, Cabras P, Angioni A (2007) Characterization of the volatile constituents in the essential oil of Pistacia lentiscus L. from different origins and its antifungal and antioxidant activity. J Agric Food Chem 55:7093–7098

  8. Bartolomé J, Franch J, Plaixats J, Seligman NG (2000) Grazing alone is not enough to maintain landscape diversity in the Montseny biosphere reserve. Agric Ecosyst Environ 77:267–273

  9. Bedoya-Pérez MA, Isler I, Banks PB, McArthur C (2014) Roles of the volatile terpene, 1, 8-cineole, in plant–herbivore interactions: a foraging odor cue as well as a toxin? Oecologia 174:827–837

  10. Biquand S, Biquand-Guyot V (1992) The influence of peers, lineage and environment on food selection of the criollo goat (Capra hircus). Appl Anim Behav Sci 34:231–245

  11. Boelens MH, Jimenez R (1991) Chemical composition of the essential oils from the gum and from various parts of Pistacia lentiscus L.(mastic gum tree). Flav Frag J 6:271–275

  12. Carmel Y, Kadmon R (1999) Effects of grazing and topography on long-term vegetation changes in a Mediterranean ecosystem in Israel. Plant Ecol 145:243–254

  13. Castola V, Bighelli A, Casanova J (2000) Intraspecific chemical variability of the essential oil of Pistacia lentiscus L. from Corsica. Biochem Syst Ecol 28:79–88

  14. Castro M, Fernández Núñez E (2016) Seasonal grazing of goats and sheep on Mediterranean mountain rangelands of Northeast Portugal. Livestock Res Rural Dev 28:1–13

  15. Decandia M, Sitzia M, Cabiddu A, Kababya D, Molle G (2000) The use of polyethylene glycol to reduce the anti-nutritional effects of tannins in goats fed woody species. Small Rumin Res 38:157–164

  16. Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175

  17. Estell RE, Fredrickson EL, Tellez MR, Havstad KM, Shupe WL, Anderson DM, Remmenga MD (1998) Effects of volatile compounds on consumption of alfalfa pellets by sheep. J Anim Sci 76:228–233

  18. Estell RE, James DK, Fredrickson EL, Anderson DM (2013) Within-plant distribution of volatile compounds on the leaf surface of Flourensia cernua. Biochem Syst Ecol 48:144–150

  19. Estell RE, Utsumi SA, Cibils AF, Anderson DM (2014) Is differential use of Juniperus monosperma by small ruminants driven by terpenoid concentration? J Chem Ecol 40:285–293

  20. Garson GD (2017) Multilevel mixed modeling. Kindle edn. Statistical Associates Publishers, NC

  21. Glasser TA, Landau SY, Ungar ED, Perevolotsky A, Dvash L, Muklada H, Walker JW (2012) Foraging selectivity of three goat breeds in a Mediterranean shrubland. Small Rumin Res 102:7–12

  22. Goff SA, Klee HJ (2006) Plant volatile compounds: sensory cues for health and nutritional value? Science 311:815–819

  23. Henkin Z, Perevolotsky A, Rosenfeld A, Brosh A, Provenza F, Silanikove N (2009) The effect of polyethylene glycol on browsing behaviour of beef cattle in a tanniferous shrubby Mediterranean range. Livest Sci 126:245–251

  24. Hester AJ, Scogings PF, Trollope WS (2006) Long-term impacts of goat browsing on bush-clump dynamics in a semi-arid subtropical savanna. Plant Ecol 183:277–290

  25. Illius AW, Jessop NS (1995) Modeling metabolic costs of allelochemical ingestion by foraging herbivores. J Chem Ecol 21:693–719

  26. Izhaki I, Safriel UN (1985) Why do fleshy-fruit plants of the Mediterranean scrub intercept fall- but not spring-passage of seed-dispersing migratory birds? Oecologia 67:40–43

  27. Joch M, Cermak L, Hakl J, Hucko B, Duskova D, Marounek M (2016) In vitro screening of essential oil active compounds for manipulation of rumen fermentation and methane mitigation. Asian-Australas J Anim Sci 29:952–959

  28. Landau S, Dvash L, Decandia M, Cabiddu A, Shapiro F, Molle G, Silanikove N (2004) Determination of poly (ethylene glycol)-binding to browse foliage, as an assay of tannin, by near-infrared reflectance spectroscopy. J Agric Food Chem 52:638–642

  29. Landau S, Muklada H, Markovics A, Azaizeh H (2014) Traditional uses of Pistacia lentiscus in veterinary and human medicine. In: Yaniv Z, Dudai N (eds) Medicinal and aromatic plants of the middle-east. Springer, Netherlands, pp 163–180

  30. Langenheim JH (1994) Higher plant terpenoids: a phytocentric overview of their ecological roles. J Chem Ecol 20:1223–1280

  31. Lawler IR, Stapley J, Foley WJ, Eschler BM (1999) Ecological example of conditioned flavor aversion in plant–herbivore interactions: effect of terpenes of Eucalyptus leaves on feeding by common ringtail and brushtail possums. J Chem Ecol 25:401–415

  32. Levin SA (1992) The problem of pattern and scale in ecology. Ecology 73:1943–1967

  33. Lindborg R, Gordon LJ, Malinga R, Bengtsson J, Peterson G, Bommarco R, Deutsch L, Gren A, Smith HG (2017) How spatial scale shapes the generation and management of multiple ecosystem services. Ecosphere 8:e01741

  34. Liu ZL, Yu M, Li XM, Wan T, Chu SS (2011) Repellent activity of eight essential oils of Chinese medicinal herbs to Blattella germanica L. Rec Nat Prod 5:176–183

  35. Llorens-Molina JA, Vacas Gonzales S, Martinez JS (2015) Essential oil composition of leaves of Pistacia lentiscus L. growing wild in Valencia (Spain). Nat Volatiles Essent Oils 2:17–26

  36. Lussig G, Probo M, Hodge S, Lombardi G (2015) Plant species selection by goats foraging on montane semi-natural grasslands and grazable forestlands in the Italian Alps. Ital J Anim Sci 14:484–494

  37. Makkar HPS (2003) Effect and fate of tannins in ruminant animals, adaptation to tannins and strategies to overcome detrimental effects of feeding tannin-rich feeds. Small Rumin Res 49:241–256

  38. Markó G, Novák I, Bernáth J, Altbäcker V (2011) Both gas chromatography and an electronic nose reflect chemical polymorphism of juniper shrubs browsed or avoided by sheep. J Chem Ecol 37:705–713

  39. Massei G, Cotterill JV, Coats JC, Bryning G, Cowan DP (2007) Can Batesian mimicry help plants to deter herbivores? Pest Manag Sci 63:559–563

  40. Moore BD, Wallis IR, Palá-Paúl J, Brophy JJ, Willis RH, Foley WJ (2004) Antiherbivore chemistry of Eucalyptus — cues and deterrents for marsupial folivores. J Chem Ecol 30:1743–1769

  41. Nagy JG, Tengerdy RP (1968) Antibacterial action of essential oils of Artemisia as an ecological factor, II. Appl Microbiol 16:441–444

  42. Nahum S, Inbar M, Ne’eman G, Ben-Shlomo R (2008) Phenotypic plasticity and gene diversity in Pistacia lentiscus L. along environmental gradients in Israel. Tree Genet Genomes 4:777–785

  43. Papachristou TG, Dziba LE, Provenza FD (2005) Foraging ecology of goats and sheep on wooded rangelands. Small Rumin Res 59:141–156

  44. Perevolotsky A, Seligman NG (1998) Role of grazing in Mediterranean rangeland ecosystems. BioScience 48:1007–1017

  45. Provenza FD, Villalba JJ, Dziba LE, Atwood SB, Banner RE (2003) Linking herbivore experience, varied diets and plant biochemistry diversity. Small Rumin Res 49:257–274

  46. Raudenbush SW, Bryk AS (2002) Hierarchical linear models: applications and data analysis methods, 2nd edn. Sage, Los Angeles

  47. Rogosic J, Pfister JA, Provenza FD, Grbesa D (2006) Sheep and goat preference for and nutritional value of Mediterranean maquis shrubs. Small Rumin Res 64:169–179

  48. Said SA, Fernandez C, Greff S, Torre F, Derridj A, Gauquelin T, Mevy JP (2011) Inter-population variability of terpenoid composition in leaves of Pistacia lentiscus L. from Algeria: a chemoecological approach. Molecules 16:2646–2657

  49. Schmitt MH, Shuttleworth A, Ward D, Shrader AM (2018) African elephants use plant odours to make foraging decisions across multiple spatial scales. Anim Behav 141:17–27

  50. Selya AS, Rose JS, Dierker LC, Hedeker D, Mermelstein RJ (2012) A practical guide to calculating Cohen’s f 2, a measure of local effect size, from PROC MIXED. Front Psychol 3:111

  51. Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423

  52. Shmida A (1981) Mediterranean vegetation in California and Israel: similarities and differences. Israel J Bot 30:105–123

  53. Stutz RS, Banks PB, Proschogo N, McArthur C (2016) Follow your nose: leaf odour as an important foraging cue for mammalian herbivores. Oecologia 182:643–651

  54. Torrano L, Valderrábano J (2004) Impact of grazing on plant communities in forestry areas. Span J Agric Res 2:93–105

  55. Utsumi SA, Cibils AF, Estell RE, Soto-Navarro SA, van Leeuwen D (2009) Seasonal change in one seed juniper intake by sheep and goats in relation to dietary protein and plant secondary metabolites. Small Rumin Res 81:152–162

  56. Villalba JJ, Provenza FD, Olson KC (2006) Terpenes and carbohydrate source influence rumen fermentation, digestibility, intake and preference in sheep. J Anim Sci 84:2463–2473

  57. Zrira S, Elamrani A, Benjilali B (2003) Chemical composition of the essential oil of Pistacia lentiscus L. from Morocco—a seasonal variation. Flav Frag J 18:475–480

Download references


The authors are grateful to the Ramat Hanadiv Nature Park for hosting this research and partially funding the chemical analyses. The authors thank Avi Perevolotsky, Yan Landau, Alexander Weinstein, Hillary Voet, Levana Devash, Tania Masci, Ben Spitzer-Rimon, Uzi Ravid and Fred Provenza for their valuable help and advice.

Author information

Correspondence to Shilo Navon.

Ethics declarations

The preference experiments were approved by the Animal Experimentation Ethics Committee of the Israeli Agricultural Research Organization (ARO).

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic supplementary material


(DOCX 1.98 mb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Navon, S., Kigel, J., Dudai, N. et al. Volatiles and Tannins in Pistacia lentiscus and Their Role in Browsing Behavior of Goats (Capra hircus). J Chem Ecol 46, 99–113 (2020) doi:10.1007/s10886-019-01124-x

Download citation


  • Essential oil
  • Foraging
  • Mediterranean shrubland
  • Local spatial scale
  • Terpenes
  • Intraspecific