Skip to main content
Log in

Early physiological responses of Abies alba and Rubus fruticosus to ungulate herbivory

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

For the last 50 years, Chamois (Rupicapra rupicapra) population exponentially increased in the French Alps. This herbivore faces a food shortage in the winter; its diet mainly includes woody species (Abies alba Mill.) and brambles (Rubus fruticosus). The physiological response following simulated herbivory of these two plants was assessed. More precisely, the effects of leaf clipping and ungulate saliva application on the epidermal flavonoids and chlorophyll contents were considered as an induced structural response. The chlorophyll fluorescence (Fv/Fm) was also measured to provide information on the photosynthesis status as an induced functional response. The non-invasive techniques used in this experiment highlighted an induced response, emerging during the days following the simulated herbivory. R. fruticosus was drastically affected, photosynthesis was disturbed (decreased Fv/Fm) and mortality began on day 5 reaching 100 % less than 1 week later. Physiological parameters were also affected in A. alba (slight decrease of Fv/Fm and lower content of flavonoids), but this species recovered and survived no matter what the stressing treatment was. These results did not point out an efficient repulsive-induced response of A. alba and R. fruticosus to herbivory. The existence of constitutive defences such as prickles (R. fruticosus) or low-digestible tannins (A. alba) is no more efficient to escape from ungulates consumption. Nevertheless, in spite of the increase of the ungulates exponential demography, these two plants do not face rarefaction problem in the French Alps. Thus, survival of A. alba stands is probably linked to the recovery ability of saplings, when R. fruticosus stands maintain themselves thanks to the strong resprouting capacity of this species.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Babad G (1997) Etude des relations entre un peuplement animal et la végétation : impacts du Chamois, du Chevreuil et du Mouflon sur les peuplements forestiers dans la réserve nationale de faune sauvage et de chasse des Bauges (Savoie). Université de Savoie, Chambéry

    Google Scholar 

  • Bazely DR, Myers JH, Dasilva KB (1991) The response of numbers of bramble prickles to herbivory and depressed resource availability. Oikos 61(3):327–336. doi:10.2307/3545240

    Article  Google Scholar 

  • Bergman M (2002) Can saliva from moose, Alces alces, affect growth responses in the sallow, Salix caprea? Oikos 96(1):164–168. doi:10.1034/j.1600-0706.2002.960118.x

    Article  Google Scholar 

  • Bertolino S, di Montezemolo NC, Bassano B (2009) Food-niche relationships within a guild of alpine ungulates including an introduced species. J Zool 277(1):63–69. doi:10.1111/j.1469-7998.2008.00512.x

    Article  Google Scholar 

  • Bidel LPR, Meyer S, Goulas Y, Cadot Y, Cerovic ZG (2007) Responses of epidermal phenolic compounds to light acclimation: in vivo qualitative and quantitative assessment using chlorophyll fluorescence excitation spectra in leaves of three woody species. J Photochem Photobiol B 88(2–3):163–179. doi:10.1016/j.jphotobiol.2007.06.002

    Article  PubMed  CAS  Google Scholar 

  • Boissier J-M (2005) Guide d’interprétation des habitats naturels du massif des Bauges. Conservatoire Botanique National Alpin

  • Buricova L, Andjelkovic M, Cermakova A, Reblova Z, Jurcek O, Kolehmainen E, Verhe R, Kvasnicka F (2011) Antioxidant capacity and antioxidants of strawberry, blackberry, and raspberry leaves. Czechoslov J Food Sci 29(2):181–189

    CAS  Google Scholar 

  • Cartelat A, Cerovic ZG, Goulas Y, Meyer S, Lelarge C, Prioul JL, Barbottin A, Jeuffroy MH, Gate P, Agati G, Moya I (2005) Optically assessed contents of leaf polyphenolics and chlorophyll as indicators of nitrogen deficiency in wheat (Triticum aestivum L.). Field Crops Res 91(1):35–49. doi:10.1016/j.fcr.2004.05.002

    Article  Google Scholar 

  • Carter GA, Knapp AK (2001) Leaf optical properties in higher plants: linking spectral characteristics to stress and chlorophyll concentration. Am J Bot 88(4):677–684. doi:10.2307/2657068

    Article  PubMed  CAS  Google Scholar 

  • Castro H, Nabais C, Alados CL, Freitas H (2003) Effects of cessation of grazing on leaf-level photosynthesis of Periploca laevigata. Appl Veg Sci 6(2):255–260. doi:10.1658/1402-2001(2003)006[0255:eocogo]2.0.co;2

    Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103(4):551–560. doi:10.1093/aob/mcn125

    Article  PubMed  CAS  Google Scholar 

  • Chen YE, Yuan S, Du JB, Xu MY, Zhang ZW, Lin HH (2009) Phosphorylation of photosynthetic antenna protein CP29 and photosystem II structure changes in monocotyledonous plants under environmental stresses. Biochemistry 48(41):9757–9763. doi:10.1021/bi901308x

    Article  PubMed  CAS  Google Scholar 

  • Chiapusio G, Pellissier F (2001) Radiochemical techniques to quantify allelochemicals in plants. Handbook of plant ecophysiology techniques. Springer-Verlag, New York, pp 443–452

    Google Scholar 

  • Chiapusio G, Pellissier F, Gallet C (2004) Uptake and translocation of phytochemical 2-benzoxazolinone (BOA) in radish seeds and seedlings. J Exp Bot 55(402):1587–1592

    Article  PubMed  CAS  Google Scholar 

  • Corti R (2006) Inventaire des populations françaises d’ongulés de montagne. http://www.oncfs.gouv.fr/IMG/file/mammiferes/ongules/montagne/intro_conclusion_2006.pdf. Accessed 24 Nov 2012

  • Fornoni J (2011) Ecological and evolutionary implications of plant tolerance to herbivory. Funct Ecol 25(2):399–407. doi:10.1111/j.1365-2435.2010.01805.x

    Article  Google Scholar 

  • Gaillard JM, Loison A, Festa-Bianchet M, Yoccoz NG, Solberg E (2003) Ecological correlates of life span in populations of large herbivorous mammals. Popul Dev Rev 29:39–56

    Google Scholar 

  • Galvez DA, Tyree MT (2009) Impact of simulated herbivory on water relations of aspen (Populus tremuloides) seedlings: the role of new tissue in the hydraulic conductivity recovery cycle. Oecologia 161(4):665–671. doi:10.1007/s00442-009-1416-8

    Article  PubMed  Google Scholar 

  • Garrido E, Andraca-Gomez G, Fornoni J (2012) Local adaptation: simultaneously considering herbivores and their host plants. New Phytol 193(2):445–453. doi:10.1111/j.1469-8137.2011.03923.x

    Article  PubMed  Google Scholar 

  • Goulas Y, Cerovic ZG, Cartelat A, Moya I (2004) Dualex: a new instrument for field measurements of epidermal ultraviolet absorbance by chlorophyll fluorescence. Appl Opt 43(23):4488–4496. doi:10.1364/ao.43.004488

    Article  PubMed  CAS  Google Scholar 

  • Govindjee (1995) 63 years since Kautsky-chlorophyll-a fluorescence. Aust J Plant Physiol 22(2):131–160. doi:10.1071/pp9950131

    Article  CAS  Google Scholar 

  • Greenwood PL, Shutt DA (1992) Salivary and plasma-cortisol as an index of stress in goats. Aust Vet J 69(7):161–163. doi:10.1111/j.1751-0813.1992.tb07501.x

    Article  PubMed  CAS  Google Scholar 

  • Gudej J, Tomczyk M (2004) Determination of flavonoids, tannins and ellagic acid in leaves from Rubus L. species. Arch Pharm Res 27(11):1114–1119. doi:10.1007/bf02975114

    Article  PubMed  CAS  Google Scholar 

  • Gutbrodt B, Dorn S, Unsicker SB, Mody K (2012) Species-specific responses of herbivores to within-plant and environmentally mediated between-plant variability in plant chemistry. Chemoecology 22(2):101–111. doi:10.1007/s00049-012-0102-1

    Article  Google Scholar 

  • Häsler H, Senn J (2012) Ungulate browsing on European silver fir Abies alba: the role of occasions, food shortage and diet preferences. Wildl Biol 18(1):67–74. doi:10.2981/09-013

    Article  Google Scholar 

  • Häsler H, Senn J, Edwards PJ (2008) Light-dependent growth responses of young Abies alba to simulated ungulate browsing. Funct Ecol 22(1):48–57. doi:10.1111/j.1365-2435.2007.01346.x

    Google Scholar 

  • Heil M (2010) Plastic defence expression in plants. Evol Ecol 24(3):555–569. doi:10.1007/s10682-009-9348-7

    Article  Google Scholar 

  • Hochwender CG, Marquis RJ, Stowe KA (2000) The potential for and constraints on the evolution of compensatory ability in Asclepias syriaca. Oecologia 122(3):361–370. doi:10.1007/s004420050042

    Article  Google Scholar 

  • Karban R (2011) The ecology and evolution of induced resistance against herbivores. Funct Ecol 25(2):339–347. doi:10.1111/j.1365-2435.2010.01789.x

    Article  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis-the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349. doi:10.1146/annurev.pp.42.060191.001525

    Article  CAS  Google Scholar 

  • Liu J, Wang L, Wang D, Bonser SP, Sun F, Zhou YF, Gao Y, Teng X (2012) Plants can benefit from herbivory: stimulatory effects of sheep saliva on growth of leymus chinensis. Plos One 7(1):e29259. doi:10.1371/journal.pone.0029259

  • Louis J, Meyer S, Maunoury-Danger F, Fresneau C, Meudec E, Cerovic ZG (2009) Seasonal changes in optically assessed epidermal phenolic compounds and chlorophyll contents in leaves of sessile oak (Quercus petraea): towards signatures of phenological stage. Funct Plant Biol 36(8):732–741. doi:10.1071/fp09010

    Article  CAS  Google Scholar 

  • Martemyanov VV, Dubovskiy IM, Rantala MJ, Salminen JP, Belousova IA, Pavlushin SV, Bakhvalov SA, Glupov VV (2012) The effects of defoliation-induced delayed changes in silver birch foliar chemistry on gypsy moth fitness, immune response, and resistance to baculovirus infection. J Chem Ecol 38(3):295–305. doi:10.1007/s10886-012-0090-1

    Article  PubMed  CAS  Google Scholar 

  • Martz F, Jaakola L, Julkunen-Tiitto R, Stark S (2010) Phenolic composition and antioxidant capacity of bilberry (Vaccinium myrtillus) leaves in northern Europe following foliar development and along environmental gradients. J Chem Ecol 36(9):1017–1028. doi:10.1007/s10886-010-9836-9

    Article  PubMed  CAS  Google Scholar 

  • Maschinski J, Whitham TG (1989) The continuum of plant-responses to herbivory-the influence of plant-association, nutrient availability, and timing. Am Nat 134(1):1–19. doi:10.1086/284962

    Article  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51(345):659–668. doi:10.1093/jexbot/51.345.659

    Article  PubMed  CAS  Google Scholar 

  • McEwen BS, Stellar E (1993) Stress and the individual-mechanisms leading to disease. Arch Intern Med 153(18):2093–2101. doi:10.1001/archinte.153.18.2093

    Article  PubMed  CAS  Google Scholar 

  • MorenoCaselles J, PerezEspinosa A, PerezMurcia MD, Moral R, Gomez I (1997) Cobalt-induced stress in tomato plants: effect on yield, chlorophyll content, and nutrient evolution. J Plant Nutr 20(9):1231–1237. doi:10.1080/01904169709365330

    Article  CAS  Google Scholar 

  • Netto AT, Campostrini E, de Oliveira JG, Bressan-Smith RE (2005) Photosynthetic pigments, nitrogen, chlorophyll a fluorescence and SPAD-502 readings in coffee leaves. Sci Hortic 104(2):199–209. doi:10.1016/j.scienta.2004.08.013

    Article  Google Scholar 

  • O’Neill BF, Zangerl AR, Dermody O, Bilgin DD, Casteel CL, Zavala JA, DeLucia EH, Berenbaum MR (2010) Impact of elevated levels of atmospheric CO2 and herbivory on flavonoids of soybean (Glycine max Linnaeus). J Chem Ecol 36(1):35–45. doi:10.1007/s10886-009-9727-0

    Article  PubMed  Google Scholar 

  • Pellissier F, Souto XC (1999) Allelopathy in northern temperate and boreal semi-natural woodland. Crit Rev Plant Sci 18(5):637–652

    Article  Google Scholar 

  • Perrin PM, Mitchell FJG, Kelly DL (2011) Long-term deer exclusion in yew-wood and oakwood habitats in southwest Ireland: changes in ground flora and species diversity. For Ecol Manage 262(12):2328–2337. doi:10.1016/j.foreco.2011.08.028

    Article  Google Scholar 

  • Petzold J, Brownie C, Gould F (2009) Effect of Heliothis subflexa herbivory on fruit abscission by Physalis species: the roles of mechanical damage and chemical factors. Ecol Entomol 34(5):603–613. doi:10.1111/j.1365-2311.2009.01109.x

    Article  Google Scholar 

  • Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5(5):308–316. doi:10.1038/nchembio.164

    Article  PubMed  CAS  Google Scholar 

  • Redjadj C (2010) Etude inter- et intra-spécifique des variations spatio-temporelles de l’utilisation des ressources alimentaires au sein d’une communauté de grands herbivores de montagne. PhD thesis, Université de Grenoble, Grenoble

  • Redondo-Gomez S, Mancilla-Leyton JM, Mateos-Naranjo E, Cambrolle J, Martin-Vicente A (2010) Differential photosynthetic performance of three Mediterranean shrubs under grazing by domestic goats. Photosynthetica 48(3):348–354. doi:10.1007/s11099-010-0045-0

    Article  CAS  Google Scholar 

  • Robakowski P, Wyka T, Samardakiewicz S, Kierzkowski D (2004) Growth, photosynthesis, and needle structure of silver fir (Abies alba Mill.) seedlings under different canopies. For Ecol Manage 201(2–3):211–227. doi:10.1016/j.foreco.2004.06.029

    Article  Google Scholar 

  • Rutigliano FA, DeSanto AV, Berg B, Alfani A, Fioretto A (1996) Lignin decomposition in decaying leaves of Fagus sylvatica L and needles of Abies alba Mill. Soil Biol Biochem 28(1):101–106. doi:10.1016/0038-0717(95)00120-4

    Article  Google Scholar 

  • Salaj J, Kormutak A (1995) Structural changes in mesophyll celles of Abies alba Mill. during the autumn–spring period. Biologia 50(1):93–98

    Google Scholar 

  • Schales C, Gerlach H, Kosters J (1993) Investigations on the antibacterial effect of conifer needle oil on bateria isolated from the feces of captive capercaillies (Tetrao urogallus L., 1758). J Vet Med Ser B 40(6):381–390

    Article  CAS  Google Scholar 

  • Senn J, Suter W (2003) Ungulate browsing on silver fir (Abies alba) in the Swiss Alps: beliefs in search of supporting data. For Ecol Manage 181(1–2):151–164. doi:10.1016/s0378-1127(03)00129-4

    Article  Google Scholar 

  • Shemesh H, Ovadia O, Novoplansky A (2012) Prioritized contingencies: context-dependent regeneratory effects of grazer saliva. Plant Ecol 213(1):167–174. doi:10.1007/s11258-011-9968-1

    Article  Google Scholar 

  • Shimada T (2006) Salivary proteins as a defense against dietary tannins. J Chem Ecol 32(6):1149–1163. doi:10.1007/s10886-006-9077-0

    Article  PubMed  CAS  Google Scholar 

  • Slimestad R (2003) Flavonoids in buds and young needles of Picea, Pinus and Abies. Biochem Syst Ecol 31(11):1247–1255. doi:10.1016/s0305-1978(03)00018-8

    Article  CAS  Google Scholar 

  • Stevens MT, Kruger EL, Lindroth RL (2008) Variation in tolerance to herbivory is mediated by differences in biomass allocation in aspen. Funct Ecol 22(1):40–47. doi:10.1111/j.1365-2435.2007.01356.x

    Google Scholar 

  • Stolter C, Ball JP, Niemela P, Julkunen-Tiitto R (2010) Herbivores and variation in the composition of specific phenolics of boreal coniferous trees: a search for patterns. Chemoecology 20(4):229–242. doi:10.1007/s00049-010-0053-3

    Article  CAS  Google Scholar 

  • Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Annu Rev Ecol Syst 31:565–595. doi:10.1146/annurev.ecolsys.31.1.565

    Article  Google Scholar 

  • Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17(6):278–285. doi:10.1016/s0169-5347(02)02483-7

    Article  Google Scholar 

  • Thomson VP, Cunningham SA, Ball MC, Nicotra AB (2003) Compensation for herbivory by Cucumis sativus through increased photosynthetic capacity and efficiency. Oecologia 134(2):167–175. doi:10.1007/s00442-002-1102-6

    PubMed  Google Scholar 

  • Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Physiol Plant Mol Biol 40:19–38. doi:10.1146/annurev.pp.40.060189.000315

    Article  Google Scholar 

  • Valkama E, Koricheva J, Salminen JP, Helander M, Saloniemi I, Saikkonen K, Pihlaja K (2005) Leaf surface traits: overlooked determinants of birch resistance to herbivores and foliar micro-fungi? Trees-Struct Funct 19(2):191–197. doi:10.1007/s00468-004-0380-5

    Article  Google Scholar 

  • Vourc’h G, Martin JL, Duncan P, Escarre J, Clausen TP (2001) Defensive adaptations of Thuja plicata to ungulate browsing: a comparative study between mainland and island populations. Oecologia 126(1):84–93. doi:10.1007/s004420000491

    Article  Google Scholar 

Download references

Acknowledgments

The author is greatly indebted to Laurie Morales for her valuable help in PEA and Dualex measurements. Goat saliva was freely and abundantly provided by Maurice Michaud and sons, owners of the Grand-Champ goat farm (F-73170 Yenne). Thanks to Dr. Anne Loison (CNRS UMR 5553) and two anonymous reviewers for helpful comments concerning the manuscript and to Kate Desmurs whom corrected English.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to François Pellissier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pellissier, F. Early physiological responses of Abies alba and Rubus fruticosus to ungulate herbivory. Plant Ecol 214, 127–138 (2013). https://doi.org/10.1007/s11258-012-0151-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-012-0151-0

Keywords

Navigation