Skip to main content
Log in

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

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

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 via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

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

Similar content being viewed by others

References

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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

Download references

Acknowledgements

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

Authors and Affiliations

Authors

Corresponding author

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

ESM 1

(DOCX 1.98 mb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. 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). https://doi.org/10.1007/s10886-019-01124-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-019-01124-x

Keywords

Navigation