Skip to main content
SpringerLink
Log in

How do plants balance multiple mutualists? Correlations among traits for attracting protective bodyguards and pollinators in cotton (Gossypium)

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Many species, both plants and animals, are simultaneously engaged in interactions with multiple mutualists. However, the extent to which separate traits that attract different mutualist guilds display negative or positive relationships remains largely unstudied. We asked whether correlations exist among extrafloral nectary traits to attract arthropod bodyguards and floral traits to attract pollinator mutualists. For 37 species in the cotton genus (Gossypium), we evaluated correlations among six extrafloral nectary traits and four floral traits in a common greenhouse environment, with and without correction for phylogenetic non-independence. Across Gossypium species, greater investment in extrafloral nectary traits was positively correlated with greater investment in floral traits. Positive correlations remained after accounting for the evolutionary history of the clade. Our results demonstrate that traits to maintain multiple mutualist guilds can be positively correlated across related species and build a more general understanding of the constraints on trait evolution in plants.

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

Similar content being viewed by others

References

  • Agrawal AA (2011) Current trends in the evolutionary ecology of plant defense. Funct Ecol 25:420–432

    Article  Google Scholar 

  • Agrawal A, Fishbein M (2006) Plant defense syndromes. Ecology 87:S132–S149

    Article  PubMed  Google Scholar 

  • Agrawal AA, Fishbein M, Halitschke R, Hastings AP, Rabosky DL, Rasmann S (2009a) Evidence for adaptive radiation from a phylogenetic study of plant defenses. Proc Natl Acad Sci USA 106:18067–18072

    Article  PubMed  CAS  Google Scholar 

  • Agrawal AA, Salminen JP, Fishbein M, Tiffin P (2009b) Phylogenetic trends in phenolic metabolism of milkweeds (Asclepias): evidence for escalation. Evolution 63:663–673

    Article  PubMed  CAS  Google Scholar 

  • Benitez-Vieyra S, Medina A, Glinos E, Cocucci A (2006) Pollinator-mediated selection on floral traits and size of floral display in Cyclopogon elatus, a sweat-bee pollinated orchid. Funct Ecol 20:948–957

    Article  Google Scholar 

  • Brody AK, Mitchell R (1997) Effects of experimental manipulation of inflorescence size on pollination and pre-dispersal seed predation in the hummingbird-pollinated plant Ipomopsis aggregata. Oecologia 110:86–93

    Article  Google Scholar 

  • Bronstein JL (1994) Our current understanding of mutualism. Q Rev Biol 69:31–51

    Article  Google Scholar 

  • Cahill JF, Elle E, Smith GR, Shore BH (2008) Disruption of a belowground mutualism alters interactions between plants and their floral visitors. Ecology 89:1791–1801

    Article  PubMed  Google Scholar 

  • Cavender-Bares J, Ackerly DD, Baum DA, Bazzaz FA (2004) Phylogenetic overdispersion in Floridian oak communities. Am Nat 163:823–843

    Article  PubMed  CAS  Google Scholar 

  • Chen ZJ et al (2007) Toward sequencing cotton (Gossypium) genomes. Plant Physiol 145:1303–1310

    Article  PubMed  CAS  Google Scholar 

  • Clark KR, Gorley RN (2007) Primer, version 6.1.10, user manual and tutorial. Primer-E, Plymouth

    Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Dejoode D, Wendel J (1992) Genetic diversity and origin of the Hawaiian Islands cotton, Gossypium tomentosum. Am J Bot 79:1311–1319

    Article  Google Scholar 

  • Eckstein RL, Karlsson PS, Weih M (1999) Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate-arctic regions. New Phytol 143:177–189

    Article  Google Scholar 

  • Felsenstein J (2008) Comparative methods with sampling error and within-species variation: contrasts revisited and revised. Am Nat 171:713–725

    Article  PubMed  Google Scholar 

  • Fritz RS, Morse DH (1981) Nectar parasitism of Asclepias syriaca by ants: effect on nectar levels, pollinia insertion, pollinaria removal and pod production. Oecologia 50:316–319

    Article  Google Scholar 

  • Fryxell P (1979) The natural history of the cotton tribe (Malvaceae, tribe Gossypieae). Texas A&M University Press, College Station

    Google Scholar 

  • Galen C, Geib JC (2007) Density-dependent effects of ants on selection for bumble bee pollination in Polemonium viscosum. Ecology 88:1202–1209

    Article  PubMed  Google Scholar 

  • Gange AC, Smith AK (2005) Arbuscular mycorrhizal fungi influence visitation rates of pollinating insects. Ecol Entomol 30:600–606

    Article  Google Scholar 

  • Gómez J, Bosch J, Perfectti F, Fernández J, Abdelaziz M, Camacho J (2008) Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators. Proc R Soc Lond Ser B Biol Sci 275:2241–2249

    Article  Google Scholar 

  • Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol Syst 34:425–453

    Article  Google Scholar 

  • Heil M, Fiala B, Baumann B, Linsenmair K (2000) Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Funct Ecol 14:749–757

    Article  Google Scholar 

  • Heil M, Rattke J, Boland W (2005) Postsecretory hydrolysis of nectar sucrose and specialization in ant/plant mutualism. Science 308:560–563

    Article  PubMed  CAS  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Hulshof CM, Swenson NG (2010) Variation in leaf functional trait values within and across individuals and species: an example from a Costa Rican dry forest. Funct Ecol 24:217–223

    Article  Google Scholar 

  • Ives AR, Midford PE, Garland T (2007) Within-species variation and measurement error in phylogenetic comparative methods. Syst Biol 56:252

    Article  PubMed  Google Scholar 

  • Klinkhamer P, de Jong T, de Bruyn G-J (1989) Plant size and pollinator visitation in Cynoglossum officinale. Oikos 54:201–204

    Article  Google Scholar 

  • Kubitzki K (ed) (2003) Flowering plants, dicotyledons, Malvales, Capparales and non-betalain Caryophyllales. Springer, Berlin

    Google Scholar 

  • Lach L (2007) A mutualism with a native membracid facilitates pollinator displacement by Argentine ants. Ecology 88:1994–2004

    Article  PubMed  Google Scholar 

  • Mack KML, Rudgers JA (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117:310–320

    Article  Google Scholar 

  • Mooney KA, Halitschke R, Kessler A, Agrawal AA (2010) Evolutionary trade-offs in plants mediate the strength of trophic cascades. Science 327:1642–1644

    Article  PubMed  CAS  Google Scholar 

  • Morris WF et al (2007) Direct and interactive effects of enemies and mutualists on plant performance: a meta-analysis. Ecology 88:1021–1029

    Article  PubMed  Google Scholar 

  • Motten AF, Stone JL (2000) Heritability of stigma position and the effect of stigma-anther separation on outcrossing in a predominantly self-fertilizing weed, Datura stramonium (Solanaceae). Am J Bot 87:339–347

    Article  PubMed  CAS  Google Scholar 

  • Ness JH (2006) A mutualism’s indirect costs: the most aggressive plant bodyguards also deter pollinators. Oikos 113:506–514

    Article  Google Scholar 

  • Omacini M, Eggers T, Bonkowski M, Gange AC, Jones TH (2006) Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct Ecol 20:226–232

    Article  Google Scholar 

  • Poorter L et al (2008) Are functional traits good predictors of demographic rates? Evidence from five Neotropical forests. Ecology 89:1908–1920

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rudgers JA (2004) Enemies of herbivores can shape plant traits: selection in a facultative ant-plant mutualism. Ecology 85:192–205

    Article  Google Scholar 

  • Rudgers JA, Gardener MC (2004) Extrafloral nectar as a resource mediating multispecies interactions. Ecology 85:1495–1502

    Article  Google Scholar 

  • Rudgers JA, Strauss SY (2004) A selection mosaic in the facultative mutualism between ants and wild cotton. Proc R Soc Lond Ser B Biol Sci 271:2481–2488

    Article  Google Scholar 

  • Rudgers JA, Strauss SY, Wendel JE (2004) Trade-offs among anti-herbivore resistance traits: insights from Gossypieae (Malvaceae). Am J Bot 91:871–880

    Article  PubMed  Google Scholar 

  • Rudgers JA, Savage AM, Rúa MA (2010) Geographic variation in a facultative mutualism: consequences for local arthropod composition and diversity. Oecologia 163:985–996

    Article  PubMed  Google Scholar 

  • Rutter MT, Rausher MD (2007) Natural selection on extrafloral nectar production in Chamaecrista fasciculata: the costs and benefits of a mutualism trait. Evolution 58:2657–2668

    Google Scholar 

  • Schatz B, Proffit M, Rakhi BV, Borges RM, Hossaert McKey M (2006) Complex interactions on fig trees: ants capturing parasitic wasps as possible indirect mutualists of the fig–fig wasp interaction. Oikos 113:344–352

    Article  Google Scholar 

  • Stachowicz JJ, Whitlatch RB (2005) Multiple mutualists provide complementary benefits to their seaweed host. Ecology 86:2418–2427

    Article  Google Scholar 

  • Waser N, Chittka L, Price M, Williams N, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060

    Article  Google Scholar 

  • Wendel JF, Cronn RC (2003) Polyploidy and the evolutionary history of cotton. Adv Agron 78:139–186

    Article  Google Scholar 

  • Wendel JF, Brubaker C, Seelanan T (2010) The origin and evolution of Gossypium. In: Stewart JM, Oosterhuis D, Heitholt JJ (eds) Physiology of cotton. Springer, The Netherlands

    Google Scholar 

  • Whitney KD, Rudgers JA (2009) Constraints on plant signals and rewards to multiple mutualists? Plant Signal Behav 4:1–4

    Article  Google Scholar 

  • Wright IJ et al (2007) Relationships among ecologically important dimensions of plant trait variation in seven Neotropical forests. Ann Bot 99:1003–1015

    Article  PubMed  Google Scholar 

  • Young H (2008) Selection on spur shape in Impatiens capensis. Oecologia 156:535–543

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank J. Frelichowski and J. Love for facilitating research at the USDA Southern Plains Agricultural Research Center. J. Wendel advised on construction of the Gossypium phylogeny for use in phylogenetically independent contrasts. L. Seifert, L. Albert, and R. Ross collected data in greenhouses. R. Anwar and A. Gorischek provided laboratory assistance. J.A.R. was supported by the Godwin Assistant Professorship at Rice University.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Rice University, 6100 Main Street, MS-170, Houston, TX, USA

    Scott A. Chamberlain & Jennifer A. Rudgers

Authors
  1. Scott A. Chamberlain
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jennifer A. Rudgers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Scott A. Chamberlain.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 157 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chamberlain, S.A., Rudgers, J.A. How do plants balance multiple mutualists? Correlations among traits for attracting protective bodyguards and pollinators in cotton (Gossypium). Evol Ecol 26, 65–77 (2012). https://doi.org/10.1007/s10682-011-9497-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-011-9497-3

Keywords

Search

Navigation