Skip to main content

Advertisement

Log in

Leaf compensatory growth as a tolerance strategy to resist herbivory in Pancratium sickenbergeri

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

We examined the effects of leaf herbivory by the dorcas gazelle, Gazella dorcas, on the compensatory growth of the geophyte Pancratium sickenbergeri (Amaryllidaceae) in the Negev desert, Israel. In three populations exposed to different levels of herbivory, we removed different amounts of photosynthetic leaf area from plants in five clipping treatments: 0, 25, 50%-dispersed over all leaves, 50%-entire area of half the leaves, 100%. The population with the lowest level of herbivory showed the lowest relative regrowth rate after clipping. In the population with a constantly high level of herbivory, plants in intermediate-clipping treatments overcompensated in leaf area after clipping. For all the populations, clipped plants produce more new leaves than unclipped plants. In the population with the highest level of herbivory, clipping treatments did not have a significant effect on the number of fruits per plant. In addition, we did not find a trade-off between investments in growth and reproduction in this population. Our results indicated that, in the desert lily, herbivores may select for plant mechanisms that compensate after damage as a tolerant strategy to maintain fitness.

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

Similar content being viewed by others

References

  • Avila-Sakar G, Leist LL, Stephenson AG (2003) Effects of the spatial pattern of leaf damage on growth and reproduction: nodes and branches. J Ecol 91:867–879

    Article  Google Scholar 

  • Avila-Sakar G, Stephenson AG (2006) Effects of the spatial pattern of leaf damage on growth and reproduction: whole plants. Int J Plant Sci 167:1021–1028

    Article  Google Scholar 

  • Belsky AJ (1986) Does herbivory benefit plants? A review of the evidence. Am Nat 127:870–892

    Article  Google Scholar 

  • Belsky AJ, Carson WP, Jensen CL, Fox GA (1993) Overcompensation by plants: herbivore optimization or red herring? Evol Ecol 7:109–121

    Article  Google Scholar 

  • Bold H, Alexopoulos CJ, Delevoryas T (1987) Morphology of plants and fungi. Harper & Row, New York

    Google Scholar 

  • Crawley MJ (1985) Reduction of oak fecundity by low density herbivore populations. Nature 314:163–164

    Article  Google Scholar 

  • Crawley MJ (1987) Benevolent herbivores? Trends Ecol Evol 2:167–168

    Article  Google Scholar 

  • Dafni A, Shmida A, Avishai M (1981) Leafless autumnal-flowering geophytes in the Mediterranean region—Phytogeographical, ecological and evolutionary aspects. Plant Syst Evol 137:181–193

    Article  Google Scholar 

  • Garrish RS, Lee TD (1989) Physiological integration in Cassia fasciculata Michx. inflorescence removal and defoliation experiments. Oecologia 81:279–284

    Google Scholar 

  • Hendrix SD (1988) Herbivory and its impact on plant reproduction. In: Lovett J, Lovett L (eds) Plant reproductive ecology: patterns and strategies. Oxford Univ. Press, Oxford, pp 246–263

    Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Inouye DW (1982) The consequences of herbivory: a mixed blessing for Jurines mollis (Asteraceae). Oikos 39:269–272

    Article  Google Scholar 

  • Jaremo J, Nilsson P, Tuomi J (1996) Plant compensatory growth: herbivory or competition? Oikos 77:238–247

    Article  Google Scholar 

  • Kulman HM (1971) Effects of insect defoliation on growth and mortality of trees. Annu Rev Entomol 16:289–324

    Article  Google Scholar 

  • Larcher W (1975) Physiological plant ecology. Springer-Verlag, Berlin

    Google Scholar 

  • Lawes MJ, Nanni RF (1993) The density, habitat use and social organization of the dorcas gazelles (Gazella dorcas) in the Makhtesh Ramon, Negev desert, Israel. J Arid Environ 24:177–196

    Article  Google Scholar 

  • Lee TD, Bazzaz FA (1980) Effects of defoliation and competition on growth and reproduction in the annual plant Abutilon theophrasti. J Ecol 68:813–821

    Article  Google Scholar 

  • Lowman MD (1982) Effects of different rates and methods of leaf area removal on rain forest seedlings of coachwood. Austr J Bot 30:477–483

    Article  Google Scholar 

  • Marquis RJ (1984) Leaf herbivores decrease fitness of a tropical plant. Science 226:537–539

    Article  PubMed  Google Scholar 

  • Marquis RJ (1992) A bite is a bite is a bite? Constraints on response to folivory in Piper arieianum (Piperaceae). Ecology 73:143–152

    Article  Google Scholar 

  • Marshall DL (1989) Integration of response to defoliation within plants of two species of Sesbania. Funct Ecol 3:207–214

    Article  Google Scholar 

  • Mauricio R, Bowers MD, Bazzaz FA (1993) Pattern of leaf damage affects fitness of the annual plant Raphanus sativus (Brassicaceae). Ecology 74:2066–2071

    Article  Google Scholar 

  • McNaughton SJ (1979a) Grazing as optimization process: grass-ungulate relationships in the Serengeti. Am Nat 113:691–703

    Article  Google Scholar 

  • McNaughton SJ (1979b) Grassland herbivore dynamics. In: Sinclair ARE, Norton-Griffiths M (eds) Serengeti: dynamics of an ecosystems. Chicago Univ. Press, Chicago, pp 46–81

    Google Scholar 

  • McNaughton SJ (1983) Compensatory plant growth as a response to herbivory. Oikos 40:329–336

    Article  Google Scholar 

  • McNaughton SJ (1986) On plants and herbivores. Am Nat 128:765–770

    Article  Google Scholar 

  • Noy-Meir I (1993) Compensating growth of grazed plants and its relevance to the use of rangelands. Ecol Appl 3:32–34

    Article  Google Scholar 

  • Owen DF (1980) How plants may benefit from the animals that eat them. Oikos 35:230–235

    Article  Google Scholar 

  • Owen DF, Wiegert RG (1976) Do consumers maximizes plant fitness? Oikos 27:488–492

    Article  Google Scholar 

  • Paige KN (1992) Overcompensation in response to mammalian herbivory: from mutualistic to antagonistic interaction. Ecology 73:2076–2085

    Article  Google Scholar 

  • Paige KN (1999) Regrowth following ungulate herbivory in Ipomopsis aggregata: geographic evidence for overcompensation. Oecologia 118:316–323

    Article  Google Scholar 

  • Paige KN, Whitham TG (1987) Overcompensation in response to mammalian herbivory: the advantage of being eaten. Am Nat 129:407–416

    Article  Google Scholar 

  • Painter EL, Belsky AJ (1993) Application of herbivore optimization theory to rangelands of the western United States. Ecol Appl 3:2–9

    Article  Google Scholar 

  • Price EAC, Hutchings MJ (1992) Studies of growth in the clonal herb Glechoma hederacea. II. The effects of selective defoliation. J Ecol 80:39–47

    Article  Google Scholar 

  • Ruiz N, Ward D, Saltz D (2002a) Crystals of calcium oxalate in leaves: constitutive or induced defense? Funct Ecol 16:99–105

    Article  Google Scholar 

  • Ruiz N, Ward D, Saltz D (2002b) Responses of Pancratium sickenbergeri to simulated bulb herbivory: combining defense and tolerance strategies. J Ecol 90:472–479

    Article  Google Scholar 

  • Ruiz N, Saltz D, Ward D (2006a) The effects of herbivory and resource variability on the production of a second inflorescence by the desert lily, Pancratium sickenbergeri. Plant Ecol 186:47–55

    Article  Google Scholar 

  • Ruiz N, Ward D, Saltz D (2006b) Population differentiation and the effects of herbivory and sand compaction on the subterranean growth of a desert lily. J Hered 97:409–416

    Article  Google Scholar 

  • Ruiz N, Saltz D, Ward D (2006c) Signal selection in a desert lily Pancratium sickenbergeri. Evol Ecol Res 8:1461–1474

    Google Scholar 

  • Saltz D, Ward D (2000) Responding to a three-pronged attack: desert lilies subject to herbivory by dorcas gazelles. Plant Ecol 148:127–138

    Article  Google Scholar 

  • Saltz D, Schmidt H, Rowen M, Karnieli A, Ward D, Schmidt I (1999) Assessing grazing impacts by remote sensing in hyper-arid environments. J Range Manage 52:500–507

    Article  Google Scholar 

  • Shea MM, Watson MA (1989) Patterns of leaf and flower removal: their effect on fruit growth in Chamaenerion angustifolium (fireweed). Amer J Bot 76:884–890

    Article  Google Scholar 

  • Tiffin P, Rausher MD (1999) Genetic constraints and selection acting on tolerance to herbivory in the common morning glory Ipomoea purpurea. Am Nat 154:700–716

    Article  PubMed  Google Scholar 

  • Tuomi J, Nilsson P, Astrom M (1994) Plant compensatory responses-bud dormancy as an adaptation to herbivory. Ecology 75:1429–1436

    Article  Google Scholar 

  • Vail SG (1992) Selection for overcompensatory plant responses to herbivory: a mechanism for the evolution of plant-herbivore mutualism. Am Nat 139:1–8

    Article  Google Scholar 

  • Van Der Heyden F, Stock WD (1996) Regrowth of a semiarid shrub following simulated browsing: the role of reserve carbon. Funct Ecol 10:647–653

    Article  Google Scholar 

  • Van Der Meijden E, Wijn M, Verkaar HJ (1988) Defence and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:355–363

    Article  Google Scholar 

  • Verkaar HJ (1988) Are defoliators beneficial for their host plant in terrestrial ecosystems—a review? Acta Bot Neerl 37:137–152

    CAS  Google Scholar 

  • Wandera JL, Richards JH, Muller RJ (1992) The relationship between relative growth rate, meristematic potential and compensatory growth of semiarid-land shrubs. Oecologia 90:391–398

    Article  Google Scholar 

  • Ward D, Olsvig-Whittaker L (1993) Plant species diversity at the junction of two desert biogeographic zones. Biodivers Lett 1:172–185

    Article  Google Scholar 

  • Ward D, Saltz D (1994) Foraging at different spatial scales: dorcas gazelles foraging for lilies in the Negev desert. Ecology 75:48–58

    Article  Google Scholar 

  • Ward D, Olsvig-Whittaker L, Lawes MJ (1993) Vegetation-environment relationships in a Negev desert erosion cirque. J Veg Sci 4:83–94

    Article  Google Scholar 

  • Ward D, Spiegel M, Saltz D (1997) Gazelle herbivory and interpopulation differences in calcium oxalate content of leaves of a desert lily. J Chem Ecol 23:333–346

    Article  CAS  Google Scholar 

  • Ward D, Saltz D, Olsvig-Whittaker L (2000) Distinguishing signal from noise: long-term studies of vegetation in Makhtesh Ramon erosion cirque, Negev desert, Israel. Plant Ecol 150:27–36

    Article  Google Scholar 

  • Watson MA, Casper BB (1984) Morphogenetic constraints on patterns of carbon distribution in plants. Ann Rev Ecol Syst 15:233–258

    Article  Google Scholar 

  • Wilkinson L (1997) Systat: the system for statistics. SYSTAT, Inc., Evanson, IL

    Google Scholar 

Download references

Acknowledgments

We thank Iris Musli, Ofrit Gilan, and Betina Berendock for assistance in the field. We thank the anonymous reviewers for their insights. This study was supported by the Israel Science Foundation. This is publication number 587 of the Mitrani Department for Desert Ecology.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Ward.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ruiz-R, N., Ward, D. & Saltz, D. Leaf compensatory growth as a tolerance strategy to resist herbivory in Pancratium sickenbergeri . Plant Ecol 198, 19–26 (2008). https://doi.org/10.1007/s11258-007-9381-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-007-9381-y

Keywords

Navigation