Skip to main content

Advertisement

SpringerLink
Log in

Fertility, Root Reserves and the Cost of Inducible Defenses in the Perennial Plant Solanum carolinense

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

Abstract

We examined the relationship between internal resources (root reserves), external resources (soil fertility), and allocation to defense vs. growth in the clonal, perennial herb Solanum carolinense. In a short-term (9 d) greenhouse experiment, plants were treated once with jasmonic acid (JA) to determine if polyphenols and glycoalkaloids were inducible by simulated herbivory. In a longer-term (4 wk) greenhouse experiment, we measured the cost, in terms of growth, of treatment with JA every 3 d, to determine if the induced response was due more to carbon limitation or nitrogen limitation. We manipulated the resources available to the plants by varying soil fertility and the size of root cuttings from which plants were grown, and assessed how different resource levels affected the growth and production of polyphenols and alkaloids under JA treatment or control conditions. In the short term, JA increased the concentration of polyphenols in both above- and belowground plant parts, as well as alkaloid concentrations in the roots. In the long term, the only significant secondary chemistry response to JA was an increased polyphenol concentration in above ground tissues. The total amount of polyphenols produced was the same for JA and control plants, indicating that the higher concentration was a result of the lower biomass of treated plants. In contrast, alkaloid concentrations in plants treated with JA for 4 wk did not differ from controls, but JA-treated plants contained lower total amounts of alkaloids in above ground tissues, as a result of decreased growth. Fertilizer level and root cutting size had effects on growth and the production of secondary compounds and influenced the cost of induction. Plants grown under high fertility had a greater reduction in growth in response to JA than plants grown under low fertility, indicating a greater trade-off between growth and defense for high fertility plants. Plants from larger root cuttings grew bigger without any reduction in the concentration of polyphenols and alkaloids. We demonstrated that the phenotype of S. carolinense was plastic in response to simulated herbivory, fertility level, and root cutting size, and that there was a significant growth cost to induction that varied with the environment and appears to be due in large part to the allocation of limited carbon reserves.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • F. Adler R. Karban (1994) ArticleTitleDefended fortress or moving targets? Another model of inducible defenses inspired by military metaphors Am. Nat. 144 813–832 Occurrence Handle10.1086/285708

    Article  Google Scholar 

  • A. A. Agrawal (1999) ArticleTitleBenefits and costs of induced plant defense for Lepidium virginicum (Brassicaceae) Ecology 81 1804–1813

    Google Scholar 

  • A. A. Agrawal J. K. Conner M. T. J. Johnson R. Wallsgrove (2002) ArticleTitleEcological genetics of an induced plant defense against herbivores: Additive genetic variance and costs of phenotypic plasticity Evolution 56 2206–2213 Occurrence Handle12487351

    PubMed  Google Scholar 

  • A. I. Al-Humaid (2003) ArticleTitleEffects of compound fertilization on growth and alkaloids of datura (Datura innoxia Mill.) plants J. Agric. Rural Dev. Trop. 104 151–165

    Google Scholar 

  • H. M. Appel (1993) ArticleTitleThe role of phenolics in ecological systems: The importance of oxidation J. Chem. Ecol. 19 1521–1552 Occurrence Handle10.1007/BF00984895

    Article  Google Scholar 

  • H. M. Appel H. L. Govenor M. D'Ascenzo E. Siska J. C. Schlultz (2001) ArticleTitleLimitations of Folin assays of foliar phenolics in ecological studies J. Chem. Ecol. 27 761–778 Occurrence Handle10.1023/A:1010306103643 Occurrence Handle11446299

    Article  PubMed  Google Scholar 

  • C. A. Armer R. E. Berry G. L. Reed S. J. Jepsen (2004) ArticleTitleColorado potato beetle control by application of the entomopathogenic nematode Heterorhabditis marelata and potato plant alkaloid manipulation Entomol. Exp. Appl. 11 47–58 Occurrence Handle10.1111/j.0013-8703.2004.00152.x

    Article  Google Scholar 

  • I. T. Baldwin (1988) ArticleTitleDamage-induced alkaloids in tobacco: Pot-bound plants are not inducible J. Chem. Ecol. 14 1113–1120 Occurrence Handle10.1007/BF01019339

    Article  Google Scholar 

  • I. T. Baldwin (1998) ArticleTitleJasmonate-induced responses are costly but benefit plants under attack in native population Proc. Natl. Acad. Sci. U.S.A. 95 8113–8118 Occurrence Handle10.1073/pnas.95.14.8113 Occurrence Handle9653149

    Article  PubMed  Google Scholar 

  • I. T. Baldwin W. Hamilton (2000) ArticleTitleJasmonate-induced response of Nicotiana sylvestris results in fitness costs due to impaired competitive ability for nitrogen J. Chem. Ecol. 26 915–952 Occurrence Handle10.1023/A:1005408208826

    Article  Google Scholar 

  • I. T. Baldwin C. L. Sims S. E. Kean (1990) ArticleTitleThe reproductive consequences associated with inducible alkaloid responses in wild tobacco Ecology 71 252–262

    Google Scholar 

  • I. T. Baldwin D. Gorham E. A. Schmelz C. Lewandowski G. Y. Lynds (1998) ArticleTitleAllocation of nitrogen to an inducible defense and seed production in Nicotiana attenuata Oecologia 115 541–552 Occurrence Handle10.1007/s004420050552

    Article  Google Scholar 

  • F. A. Bazzaz (1996) Plants in Changing Environments: Linking Physiological, Population, and Community Ecology Cambridge University Press Cambridge, UK

    Google Scholar 

  • J. Bergelson (1994) ArticleTitleThe effects of genotype and the environment on costs of resistance in lettuce Am. Nat. 143 349–359 Occurrence Handle10.1086/285607

    Article  Google Scholar 

  • J. Bergelson C. B. Purrington (1996) ArticleTitleSurveying patterns in the cost of resistance in plants Am. Nat. 148 536–558 Occurrence Handle10.1086/285938

    Article  Google Scholar 

  • J. Birner (1969) ArticleTitleDetermination of total steroid bases in Solanum species J. Pharm. Sci. 58 258–259 Occurrence Handle5779876

    PubMed  Google Scholar 

  • R. C. Bolser M. E. Hay (1998) ArticleTitleA field test of inducible resistance to specialist and generalist herbivores using the water lily Nuphar luteum Oecologia 116 143–153 Occurrence Handle10.1007/s004420050573

    Article  Google Scholar 

  • J. P. Bryant F. S. Chapin SuffixIII D. R. Klein (1983) ArticleTitleCarbon/nutrient balance of boreal plants in relation to vertebrate herbivory Oikos 40 357–368

    Google Scholar 

  • D. F. Cipollini J. Bergelson (2001) ArticleTitlePlant density and nutrient availability constrain constitutive and wound-induced expression of trypsin inhibitors in Brassica napus J. Chem. Ecol. 27 593–610 Occurrence Handle10.1023/A:1010384805014 Occurrence Handle11441448

    Article  PubMed  Google Scholar 

  • M. L. Cipollini D. J. Levey (1997) ArticleTitleAntifungal activity of Solanum fruit glycoalkaloids: implications for frugivory and seed dispersal Ecology 78 799–809

    Google Scholar 

  • D. F. Cipollini A. M. Redman (1999) ArticleTitleAge-dependent effects of jasmonic acid treatment and wind exposure on foliar oxidase activity and insect resistance in tomato J. Chem. Ecol. 25 271–281 Occurrence Handle10.1023/A:1020842712349

    Article  Google Scholar 

  • M. L. Cipollini L. Bohs K. Mink E. Paulk K. Boehning-Gaese (2001) Patterns of secondary compound within fleshy fruits: Ecology and phylogeny D. J. Levey W. R. Silva M. Galleti (Eds) Seed Dispersal and Frugivory: Ecology, Evolution and Conservation CABI Publishing Wallingford, Oxfordshire, UK 11–128

    Google Scholar 

  • M. L. Cipollini E. Paulk D. F. Cipollini (2002) ArticleTitleEffect of nitrogen and water treatment on leaf chemistry in horsenettle (Solanum carolinense), and relationship to herbivory by flea beetles (Epitrix spp.) and tobacco hornworm (Manduca sexta) J. Chem. Ecol. 28 2377–2398 Occurrence Handle10.1023/A:1021494315786 Occurrence Handle12564788

    Article  PubMed  Google Scholar 

  • M. L. Cipollini E. Paulk K. Mink K. Vaughn T. Fischer (2004) ArticleTitleDefense tradeoffs in fleshy fruits: effects of resource variation on growth, reproduction, and fruit secondary chemistry in Solanum carolinense J. Chem. Ecol. 30 1–17 Occurrence Handle10.1023/B:JOEC.0000013179.45661.68 Occurrence Handle15074654

    Article  PubMed  Google Scholar 

  • P. D. Coley J. P. Bryant F. S. Chapin SuffixIII (1985) ArticleTitleResource availability and plant antiherbivore defenses Science 230 895–899

    Google Scholar 

  • R. E. Cook (1985) Growth and development in clonal plant populations J. B. C. Jackson R. E. Cook (Eds) Population Biology and Evolution of Clonal Organisms Yale University Press New Haven, CT 259–296

    Google Scholar 

  • T. J. Witt ParticleDe A. Sih D. S. Wilson (1998) ArticleTitleCosts and limits of phenotypic plasticity Trends Ecol. Evol. 13 77–81 Occurrence Handle10.1016/S0169-5347(97)01274-3

    Article  Google Scholar 

  • O. Erickson (1993) ArticleTitleDynamics of genets in clonal plants Trends Ecol. Evol. 8 313–316 Occurrence Handle10.1016/0169-5347(93)90237-J

    Article  Google Scholar 

  • V. R. Franceschi T. Krekling E. Christiansen (2002) ArticleTitleApplication of methyl jasmonate on Picea abies (Pinaceae) stems induces defense-related responses in phloem and xylem Am. J. Bot. 89 578–586

    Google Scholar 

  • E. Gianoli H. M. Niemeyer (1997) ArticleTitleLack of costs of herbivory-induced defense in a wild wheat: integration of physiological and ecological approaches Oikos 80 269–275

    Google Scholar 

  • T. Givnish (1986) Economic of Biotic Interactions Cambridge University Press Cambridge, UK

    Google Scholar 

  • J. P. Grime (1979) Plant Strategies and Vegetative Processes Wiley Chichester, England

    Google Scholar 

  • A. E. Hagerman K. M. Klucher (1986) Tannin–protein interactions V. Cody E. Middelton J. Harborne (Eds) Plant Flavinoids in Biology and Medicine: Biochemical, Pharmacological and Structure Activity Relationships Alan R. Liss New York 67–76

    Google Scholar 

  • M. Heil (2002) ArticleTitleEcological costs of induced resistance Curr. Opin. Plant Biol. 5 1–6 Occurrence Handle10.1016/S1369-5266(02)00267-4

    Article  Google Scholar 

  • M. Heil I. T. Balwin (2002) ArticleTitleFitness cost of induced resistance: emerging experimental support for a slippery concept Trends Plant Sci. 27 61–67 Occurrence Handle10.1016/S1360-1385(01)02186-0

    Article  Google Scholar 

  • D. A. Herms W. J. Mattson (1992) ArticleTitleThe dilemma of plants: to grow or defend Q. Rev. Biol. 67 283–335 Occurrence Handle10.1086/417659

    Article  Google Scholar 

  • M. D. Hunter J. C. Schultz (1995) ArticleTitleFertilization mitigates chemical induction and herbivore responses within damaged oak trees Ecology 76 1226–1232

    Google Scholar 

  • J. Jokela P. Schmid-Hempel M. C. Rigby (2000) ArticleTitleDr. Pangloss restrained by the Red Queen—steps toward a unified defence theory Oikos 89 267–274 Occurrence Handle10.1034/j.1600-0706.2000.890207.x

    Article  Google Scholar 

  • R. Karban (1993) ArticleTitleCosts and benefits of induced resistance and plant density for a native shrub, Gossypium thurberi Ecology 74 9–19

    Google Scholar 

  • R. Karban I. T. Baldwin (1997) Induced Responses to Herbivory The University of Chicago Press Chicago, IL

    Google Scholar 

  • R. Karban A. A. Agrawal M. Mangel (1997) ArticleTitleThe benefits of induced defenses against herbivores Ecology 78 1351–1355

    Google Scholar 

  • D. J. Kliebenstein A. Figuth T. Mitchell-Olds (2002) ArticleTitleGenetic architecture of plastic methyl jasmonate responses in Arabidopsis thaliana Genetics 161 1685–1696 Occurrence Handle12196411

    PubMed  Google Scholar 

  • J. Koricheva (1999) ArticleTitleInterpreting phenotypic variation in plant allelochemistry: problems with the use of concentrations Oecologia 119 467–473 Occurrence Handle10.1007/s004420050809

    Article  Google Scholar 

  • J. Koricheva (2002) ArticleTitleThe carbon–nutrient balance hypothesis is dead; Long live the carbon–nutrient balance hypothesis? Oikos 98 537–539 Occurrence Handle10.1034/j.1600-0706.2002.980319.x

    Article  Google Scholar 

  • J. León E. Rojo J. J. Sánchez-Serrano (2001) ArticleTitleWound signaling in plants J. Exp. Bot. 52 1–9 Occurrence Handle10.1093/jexbot/52.354.1

    Article  Google Scholar 

  • J. Maschinski T. G. Whitham (1989) ArticleTitleThe continuum of plant responses to herbivory: the influence of plant association, nutrient availability and timing Am. Nat. 134 1–19 Occurrence Handle10.1086/284962

    Article  Google Scholar 

  • M. Marcel P. G. L. Klinkenhamer K. Vrieling E. Meiden ParticleVan Der (2002) ArticleTitleDiversity of pyrrolizidine akaloids in Sencio species does not affect the specialist herbivore Tyria jacobaeae Oecologia 133 541–550 Occurrence Handle10.1007/s00442-002-1074-6

    Article  Google Scholar 

  • J. P. Moore J. E. Taylor N. D. Paul J. B. Whittaker (2003) ArticleTitleReduced leaf expansion as a cost of systemic induced resistance to herbivory Funct. Ecol. 17 75–81 Occurrence Handle10.1046/j.1365-2435.2003.00708.x

    Article  Google Scholar 

  • J. P. Moore N. D. Paul J. B. Whittaker J. E. Taylor (2003) ArticleTitleExogenous jasmonic acid mimics herbivore-induced systemic increase in cell wall bound peroxidase activity and reduction in leaf expansion Funct. Ecol. 17 549–554 Occurrence Handle10.1046/j.1365-2435.2003.00767.x

    Article  Google Scholar 

  • C. A. Mullin A. Gonzolez Coloma C. Guiterrez M. Reina H. Eichenseer B. Hollister S. Chyb (1997) ArticleTitleAnitfeedant effects of some novel terpenoids on chrysomelidae beetles: comparisons with alkaloids on an alkaloid-adapted and non-adapted species J. Chem. Ecol. 23 1865–1866 Occurrence Handle10.1023/B:JOEC.0000006455.72602.3f

    Article  Google Scholar 

  • J. J. Pan J. S. Price (2002) ArticleTitleFitness and evolution in clonal plants: the impacts of clonal growth Evol. Ecol. 15 583–600 Occurrence Handle10.1023/A:1016065705539

    Article  Google Scholar 

  • A. M. Redman D. F. Cipollini J. C. Schultz (2001) ArticleTitleFitness costs of jasmonic acid-induced defense in tomato, Lycopersicum esculantum Oecologia 126 380–385 Occurrence Handle10.1007/s004420000522

    Article  Google Scholar 

  • R. A. Relyea (2002) ArticleTitleCost of phenotypic plasticity Am. Nat. 159 272–282 Occurrence Handle10.1086/338540

    Article  Google Scholar 

  • Rhode Island Agricultural Experimental Station. 1962. Life history studies as related to weed control in the Northeast, 3-Horsenettle. Bulletin of the University of Rhode Island Agricultural Experimental Station. University of Rhode Island, Kingston, RI.

  • W. R. Rice (1989) ArticleTitleAnalyzing tables of statistical tests Evolution 43 223–225

    Google Scholar 

  • D. R. Rudell J. P. Mattheis X. Fan J. K. Fellman (2002) ArticleTitleMethyl jasmonate enhances anthocyanin accumulation and modifies production of phenolics and pigments in ‘Fuji’ apples J. Am. Soc. Hortic. Sci. 127 435–441

    Google Scholar 

  • G. Sembdner B. Parthier (1993) ArticleTitleThe biochemistry and the physiological and molecular actions of jasmonates Annu. Rev. Plant Physiol. 44 569–589 Occurrence Handle10.1146/annurev.pp.44.060193.003033

    Article  Google Scholar 

  • D. H. Siemens S. H. Garner T. Mitchell-Olds R. M. Callaway (2002) ArticleTitleCost of defense in the context of plant competition: Brassica rapa may grow and defend Ecology 83 505–517

    Google Scholar 

  • B. P. Solomon (1983) ArticleTitleCompensatory production in Solanum carolinense following attack by a host-specific herbivore J. Ecol. 71 681–690

    Google Scholar 

  • N. Stamp (2003) ArticleTitleOut of the quagmire of plant defense hypotheses Q. Rev. Biol. 78 23–55 Occurrence Handle10.1086/367580 Occurrence Handle12661508

    Article  PubMed  Google Scholar 

  • S. Y. Strauss J. A. Rudgers J. A. Lau R. E. Irwin (2002) ArticleTitleDirect and ecological costs of resistance to herbivory Trends Ecol. Evol. 17 278–285 Occurrence Handle10.1016/S0169-5347(02)02483-7

    Article  Google Scholar 

  • D. R. Strong J. H. Lawton R. Southwood (1984) Insects on Plants: Community Patterns and Mechanisms Harvard University Press Cambridge, MA

    Google Scholar 

  • S. E. Sultan (1987) ArticleTitleEvolutionary implications of phenotypic plasticity in plants Oikos 70 212–222

    Google Scholar 

  • T. Swain J. L. Goldstein (1964) The quantitative analysis of phenolic compound J. B. Pridham (Eds) Methods in Polyphenol Chemistry Pergamon Press Oxford, England 131–145

    Google Scholar 

  • T. Swain W. E. Hillis (1959) ArticleTitleThe phenolic constituents of Prunus domestica: I. The quantitative analysis of phenolic constituents J. Sci. Food Agric. 10 63–68

    Google Scholar 

  • J. S. Thaler M. J. Stout R. Karban S. S. Duffy (1996) ArticleTitleExogenous jasmonates simulate insect wounding in tomato plants (Lycopersicum esculantum) in the laboratory and field J. Chem. Ecol. 22 1767–1781 Occurrence Handle10.1007/BF02028503

    Article  Google Scholar 

  • Tisdell, T. F. 1961. A life cycle study of horse nettle (Solanum carolinense). Ph.D. dissertation, Rutgers University, New Brunswick, NJ.

  • T. Tscharntke S. Thiessen R. Dolck W. Boland (2001) ArticleTitleHerbivory, induced resistance and interplant signal transfer in Alnus glutinosa Biochem. Syst. Ecol. 29 1025–1047 Occurrence Handle10.1016/S0305-1978(01)00048-5

    Article  Google Scholar 

  • S. Via R. Gomulkiewicz G. Dejong S. M. Scheiner C. D. Schlichting P. H. Tierneden ParticleVan (1995) ArticleTitleAdaptive phenotypic plasticity—consensus and controversy Trends Ecol. Evol. 10 212–217 Occurrence Handle10.1016/S0169-5347(00)89061-8

    Article  Google Scholar 

  • D. K. Wijesinghe D. F. Whigham (1997) ArticleTitleCosts of producing clonal offspring and the effects of plant size on population dynamic of the woodland herb Uvularia perfoliata (Liliaceae) J. Ecol. 85 907–919

    Google Scholar 

  • M. J. Wise C. F. Sacchi (1996) ArticleTitleImpact of two specialist insect herbivores of horse nettle, Solanum carolinense Oecologia 108 328–337

    Google Scholar 

  • Z. P. Zhang I. T. Baldwin (1997) ArticleTitleTransport of [2-14C]jasmonic acid from leaves to roots mimics wound-induced changes in endogenous jasmonic acid pools in Nicotiana sylvestris Planta 203 436–441 Occurrence Handle10.1007/s004250050211

    Article  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Toni Schaeffer for guidance in the greenhouse and in the lab, and to Eric Paulk for help with the GA analysis. Thanks are also due to Isabel Ashton, Adam Eher, and Elizabeth Leger for comments on an earlier draft of the manuscript. R.L.W. was supported by a National Science Foundation Root Biology Training Grant (NSF DBI 96002255) and supplies were provided by a National Science Foundation Long Term Research in Environmental Biology grant to J.C.S. (DEB-9974067).

Author information

Author notes

  1. Ramona Walls

    Present address: Department of Ecology and Evolution, Stony Brook University, 650 Life Sciences Building, Stony Brook, NY, 11794-5245, USA

Authors and Affiliations

  1. Chemical Ecology Lab, The Pennsylvania State University, University Park, PA, 16802, USA

    Ramona Walls, Heidi Appel & Jack Schultz

  2. Biology Department, Berry College, Mount Berry, GA, 30149, USA

    Martin Cipollini

Authors
  1. Ramona Walls
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heidi Appel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin Cipollini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jack Schultz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ramona Walls.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Walls, R., Appel, H., Cipollini, M. et al. Fertility, Root Reserves and the Cost of Inducible Defenses in the Perennial Plant Solanum carolinense. J Chem Ecol 31, 2263–2288 (2005). https://doi.org/10.1007/s10886-005-7101-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-005-7101-4

Key Words

Search

Navigation