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Perspectives on allelopathic disruption of plant mutualisms: a framework for individual- and population-level fitness consequences

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Abstract

Mutualisms with mycorrhizal fungi, pollinators, and seed dispersers are critical for plant survival and reproduction. However, mutualism effectiveness is highly sensitive to disturbance by environmental stressors. Allelopathy is often overlooked, yet likely important, as a potential stress on plant mutualism function. Allelochemicals can affect plant mutualisms by either directly interfering with the plant’s ability to produce resources and rewards for its mutualistic partners or by directly or indirectly altering the non-plant mutualist’s behavior. Here we explore the potential effects of allelochemicals on plant mutualisms. Since allelochemicals can reduce plant growth and carbon acquisition, we suggest that allelopathy could directly diminish: (1) carbon provisioning to mycorrhizal fungi, (2) flower, pollen, and nectar production for pollinators, and (3) fruit attractiveness to seed dispersers. Similarly, allelochemicals that directly affect mycorrhizal fungi functioning can reduce the flow of soil resources to their plant partner. Further, volatile allelochemicals or uptake of allelochemicals from the soil by the plant could alter pollen/nectar or fruit attractiveness and indirectly influence pollinator and seed disperser behavior. Finally, we explore the extent to which plant-produced chemicals could have a direct or indirect positive effect on plant mutualisms. We end using these questions to frame future avenues of research that could help to move studies of allelopathy into the broader ecological context of mutualisms.

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References

  • Adler LS (2000) The ecological significance of toxic nectar. Oikos 91:409–420

    Article  Google Scholar 

  • Adler LS, Seifert MG, Wink M, Morse GE (2012) Reliance on pollinators predicts defensive chemistry across tobacco species. Ecol Lett. doi:10.1111/j.1461-0248.2012.01838.x

    Google Scholar 

  • Afzal B, Bajwa R, Javaid A (2000) Allelopathy and VA mycorrhizae VII: cultivation of Vigna radiata and Phaseolus vulgaris under allelopathy stress caused by Imperata cylindrica. Pak J Biol Sci 3:1926–1928

    Article  Google Scholar 

  • Agrawal AA, Ackerly DD, Adler F, Arnold AE, Cáceres C, Doak DF, Post E, Hudson PJ, Maron J, Mooney KA, Power M, Schemske D, Stachowicz J, Strauss S, Turner MG, Werner E (2007) Filling key gaps in population and community ecology. Front Ecol Environ 5:145–152

    Article  Google Scholar 

  • Aguilar-Chama A, Guevara R (2012) Mycorrhizal colonization does not affect tolerance to defoliation of an annual herb in different light availability and soil fertility treatments but increases flower size in light-rich environments. Oecologia 168:131–139

    Article  PubMed  Google Scholar 

  • Ashman T-L, Schoen DJ (1994) How long should flowers live? Nature 371:788–791

    Article  CAS  Google Scholar 

  • Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–957

    Article  PubMed  CAS  Google Scholar 

  • Bainard LD, Brown PD, Upadhyaya MK (2009) Inhibitory effect of tall hedge mustard (Sisymbrium loeselii) allelochemicals on rangeland plants and arbuscular mycorrhizal fungi. Weed Sci 57:386–393

    Article  CAS  Google Scholar 

  • Baker HG, Baker I (1982) Chemical constituents of nectar in relation to pollination mechanisms and phylogeny. In: Nitecki MH (ed) Biochemical aspects of evolutionary biology. University of Chicago Press, Chicago, pp 131–171

    Google Scholar 

  • Baker HG, Baker I (1986) The occurrence and significance of amino acids in floral nectar. Plant Syst Evol 151:175–186

    Article  CAS  Google Scholar 

  • Barney JN, Hay AG, Weston LA (2005) Isolation and characterization of allelopathic volatiles from mugwort (Artemisia vulgaris). J Chem Ecol 31:247–265

    Article  PubMed  CAS  Google Scholar 

  • Barto K, Friese C, Cipollini D (2010) Arbuscular mycorrhizal fungi protect a native plant from allelopathic effects of an invader. J Chem Ecol 36:351–360

    Article  PubMed  CAS  Google Scholar 

  • Barto EK, Antunes PM, Stinson K, Koch AM, Klironomos JN, Cipollini D (2011) Differences in arbuscular mycorrhizal fungal communities associated with sugar maple seedlings in and outside of invaded garlic mustard forest patches. Biol Invasions 13:2755–2762

    Article  Google Scholar 

  • Batlang U, Shushu DD (2007) Allelopathic activity of sunflower (Helianthus annuus L.) on growth and nodulation of Bambara groundnut (Vigna subterranean (L.) Verde.). J Agron 6:541–547

    Article  Google Scholar 

  • Becklin KM, Gamez G, Uelk B, Raguso R, Galen C (2011) Soil fungal effects on floral signals, rewards, and aboveground interactions in an alpine pollination web. Am J Bot 98:1299–1308

    Article  PubMed  Google Scholar 

  • Blair AC, Weston LA, Nissen SJ, Brunk GR, Hufbauer RA (2009) The importance of analytical techniques in allelopathy studies with the reported allelochemical catechin as an example. Biol Invasions 11:325–332

    Article  Google Scholar 

  • Boyd RS (2004) Ecology of hyperaccumulation. New Phytol 162:563–567

    Article  Google Scholar 

  • Boyd RS, Wall MA, Jaffré T (2006) Nickel levels in arthropods associated with Ni hyperaccumulator plants from an ultramafic site in New Caledonia. Insect Sci 13:271–277

    Article  CAS  Google Scholar 

  • Bradshaw HD Jr, Otto KG, Frewen BE, McKay JK, Schemske DW (1998) Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149:367–382

    PubMed  CAS  Google Scholar 

  • Bronstein JL (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217

    Article  PubMed  CAS  Google Scholar 

  • Brown PD, Morra MJ (1997) Control of soil-borne plant pests using glucosinolate-containing plants. Adv Agron 61:167–231

    Article  CAS  Google Scholar 

  • Brown PD, Morra MJ, McCaffrey JP, Auld DL, Williams L III (1991) Allelochemicals produced during glucosinolate degradation in soil. J Chem Ecol 17:2021–2034

    Article  CAS  Google Scholar 

  • Brundrett M, Kendrick B (1988) The mycorrhizal status, root anatomy, and phenology of plants in a sugar maple forest. Can J Bot 66:1153–1173

    Article  Google Scholar 

  • Buchholz R, Levey DJ (1990) The evolutionary triad of microbes, fruits, and seed dispersers: an experiment in fruit choice by cedar waxwings Bombycilla cedrorum. Oikos 59:200–204

    Article  Google Scholar 

  • Burke DJ (2008) Effects of Alliaria petiolata (garlic mustard; Brassicaceae) on mycorrhizal colonization and community structure in three herbaceous plants in a mixed deciduous forest. Am J Bot 95:1416–1425

    Article  PubMed  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 

  • Callaway RM, Ridenour W (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443

    Article  Google Scholar 

  • Callaway RM, Cipollini D, Barto K, Thelen GC, Hallett SG, Prati D, Stinson KA, Klironomos J (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043–1055

    Article  PubMed  Google Scholar 

  • Cantor A, Hale AN, Aaron J, Traw MB, Kalisz S (2011) Low allelochemical concentrations detected in garlic mustard-invaded forest soils inhibit fungal growth and AMF spore germination. Biol Invasions 13:3015–3025

    Article  Google Scholar 

  • Caswell H (2001) Matrix population models: construction, analysis and interpretation, 2nd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Chapin FS III, Schulze E-D, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447

    Article  Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Article  Google Scholar 

  • Chiapusio G, Pellisier F (2001) Methodological setup to study allelochemical translocation in radish seedlings. J Chem Ecol 27:1701–1712

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cipollini D, Gruner B (2007) Cyanide in the chemical arsenal of garlic mustard, Alliaria petiolata. J Chem Ecol 33:85–94

    Article  PubMed  CAS  Google Scholar 

  • Cipollini ML, Levey DJ (1997) Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. Am Nat 150:346–372

    Article  PubMed  CAS  Google Scholar 

  • Cipollini D, Rigsby CM, Barto EK (2012) Microbes as targets and mediators of allelopathy in plants. J Chem Ecol 38:714–727

    Article  PubMed  CAS  Google Scholar 

  • Clayton DH, Wolfe ND (1993) The adaptive significance of self-medication. Trends Ecol Evol 8:60–63

    Article  PubMed  CAS  Google Scholar 

  • Cnaani J, Thomson JD, Papaj DR (2006) Flower choice and learning in foraging bumblebees: effects of variation in nectar volume and concentration. Ethology 112:278–285

    Article  Google Scholar 

  • Corrêa A, Gurevitch J, Martins-Loução MA, Cruz C (2012) C allocation to the fungus is not a cost to the plant in ectomycorrhizae. Oikos 121:449–463

    Article  Google Scholar 

  • Coté J-F, Thibault J-R (1988) Allelopathic potential of raspberry foliar leachates on growth of ectomycorrhizal fungi associated with black spruce. Am J Bot 75:966–970

    Article  Google Scholar 

  • Czarnota MA, Paul RN, Dayan FE, Nimbal CI, Weston LA (2001) Mode of action, localization of production, chemical nature, and activity of sorgoleone: a potent PSII inhibitor in Sorghum spp. root exudates. Weed Technol 15:813–825

    Article  CAS  Google Scholar 

  • Darwin CR (1859) On the origin of species by means of natural selection or the preservation of favoured races in the struggle for life. John Murray, London

    Google Scholar 

  • Dayan FE, Howell J, Weidenhamer JD (2009) Dynamic root exudation of sorgoleone and its in planta mechanism of action. J Exp Bot 60:2107–2117

    Article  PubMed  CAS  Google Scholar 

  • de Kroon H, Plaisier A, van Groenendael J, Caswell H (1986) Elasticity: the relative contribution of demographic parameters to population growth rate. Ecology 67:1427–1431

    Article  Google Scholar 

  • de Vega C, Herrera CM (2012) Relationships among nectar-dwelling yeasts, flowers and ants: patterns and incidence on nectar traits. Oikos. doi:10.1111/j.1600-0706.2012.20295.x

    Google Scholar 

  • Duke SO, Dayan FE (2006) Modes of action of phytotoxins from plants. In: Reigosa MJ, Pedrol N, González L (eds) Allelopathy: a physiological process with ecological implications. Springer, Dordrecht, pp 511–536

    Google Scholar 

  • Ehlers BK, Olesen JM (1997) The fruit-wasp route to toxic nectar in Epipactis orchids? Flora 192:223–229

    Google Scholar 

  • Elmer WH, Pignatello JJ (2011) Effect of biochar amendments on mycorrhizal associations and fusarium crown and root rot of asparagus in replant soils. Plant Dis 95:960–966

    Article  Google Scholar 

  • Etterson JR, Galloway LF (2002) The influence of light on paternal plants in Campanula americana (Campanulaceae): pollen characteristics and offspring traits. Am J Bot 89:1899–1906

    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 

  • Gehring CA, Whitham TG (1994) Interactions between aboveground herbivores and the mycorrhizal mutualists of plants. Trends Ecol Evol 9:251–255

    Article  PubMed  CAS  Google Scholar 

  • Gimsing AL, Kirkegaard JA (2006) Glucosinolate and isothiocyanate concentration in soil following incorporation of Brassica biofumigants. Soil Biol Biochem 38:2255–2264

    Article  CAS  Google Scholar 

  • Gimsing AL, Kirkegaard JA (2009) Glucosinolates and biofumigation: fate of glucosinolates and their hydrolysis products in soil. Phytochem Rev 8:299–310

    Article  CAS  Google Scholar 

  • Giudici AM, Regente MC, de la Canal L (2000) A potent antifungal protein from Helianthus annuus flowers is a trypsin inhibitor. Plant Phys Biochem 38:881–888

    Article  CAS  Google Scholar 

  • Glinwood R, Ninkovic V, Petterson J, Ahmed E (2004) Barley exposed to aerial allelopathy from thistles (Cirsium spp.) becomes less acceptable to aphids. Ecol Entomol 29:188–195

    Article  Google Scholar 

  • Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 57:761–780

    Article  PubMed  CAS  Google Scholar 

  • Hachinohe M, Sunohara Y, Matsumoto H (2004) Absorption, translocation and metabolism of L-DOPA in barnyardgrass and lettuce: their involvement in species-selective phytotoxic action. Plant Growth Regul 43:237–243

    Article  CAS  Google Scholar 

  • Halbrendt JM (1996) Allelopathy in the management of plant-parasitic nematodes. J Nematol 28:8–14

    PubMed  CAS  Google Scholar 

  • Hale AN, Tonsor SJ, Kalisz S (2011) Testing the mutualism disruption hypothesis: physiological mechanisms for invasion of intact perennial plant communities. Ecosphere 2:110. doi:10.1890/ES11-00136.1

    Article  Google Scholar 

  • Haribal M, Renwick JAA (1998) Isovitexin 6″-O-β-d-glucopyranoside: a feeding deterrent to Pieris napi oleracea from Alliaria petiolata. Phytochemistry 47:1237–1240

    Article  CAS  Google Scholar 

  • Haribal M, Yang Z, Attygalle AB, Renwick JAA, Meinwald J (2001) A cyanoallyl glucoside from Alliaria petiolata as a feeding deterrent for larvae of Pieris napi oleracea. J Nat Prod 64:440–443

    Article  PubMed  CAS  Google Scholar 

  • Harms KE, Wright SJ, Calderón O, Hernández A, Herre EA (2000) Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404:493–495

    Article  PubMed  CAS  Google Scholar 

  • Hassiotis CN, Dina EI (2011) The effects of laurel (Laurus nobilis L.) on development of two mycorrhizal fungi. Int Biodeterior Biodegrad 65:628–634

    Article  CAS  Google Scholar 

  • Hejl AM, Koster KL (2004) Juglone disrupts root plasma membrane H+-ATPase activity and impairs water uptake, root respiration, and growth in soybean (Gycine max) and corn (Zea mays). J Chem Ecol 30:453–471

    Article  PubMed  CAS  Google Scholar 

  • Hejl AM, Einhellig FA, Rasmussen JA (1993) Effects of juglone of growth, photosynthesis, and respiration. J Chem Ecol 19:559–568

    Article  CAS  Google Scholar 

  • Herrera CM (1982) Defense of ripe fruit from its pests: its significance in relation to plant-disperser interactions. Am Nat 120:218–241

    Article  Google Scholar 

  • Herrera CM, García IM, Pérez R (2008) Invisible floral larcenies: microbial communities degrade floral nectar of bumble-bee pollinated plants. Ecology 89:2369–2376

    Article  PubMed  Google Scholar 

  • Hussain MI, Reigosa MJ (2011) Allelochemical stress inhibits growth, leaf water relations, PSII photochemistry, non-photochemical fluorescence quenching, and heat energy dissipation in three C3 perennial species. J Exp Bot 62:4533–4545

    Article  PubMed  CAS  Google Scholar 

  • Inderjit, Duke SO (2003) Ecophysiological aspects of allelopathy. Planta 217:529–539

    Article  PubMed  CAS  Google Scholar 

  • Inderjit, Wardle DA, Karban R, Callaway RM (2011a) The ecosystem and evolutionary contexts of allelopathy. Trends Ecol Evol 26:655–662

    Article  PubMed  CAS  Google Scholar 

  • Inderjit, Evans H, Crocoll C, Bajpai D, Kaur R, Feng Y-L, Silva C, Carreón JT, Valiente-Banuet A, Gershenzon J, Callaway RM (2011b) Volatile allelochemicals from leaf litter are associated with invasiveness of a neotropical weed in Asia. Ecology 92:316–324

    Article  PubMed  CAS  Google Scholar 

  • Jaffré T, Brooks RR, Lee J, Reeves RD (1976) Sebertia acuminate: a hyperaccumulator of nickel from New Caledonia. Science 193:579–580

    Article  PubMed  Google Scholar 

  • Jassbi AR, Zamanizadehnajari S, Baldwin IT (2010) Phytotoxic volatiles in the roots and shoots of Artemisia tridentata as detected by headspace solid-phase microextraction and gas chromatographic-mass spectrometry analysis. J Chem Ecol 36:1398–1407

    Article  PubMed  CAS  Google Scholar 

  • Javaid A (2008) Allelopathy in mycorrhizal symbiosis in the Poaceae family. Allelopath J 21:207–218

    Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585

    Article  Google Scholar 

  • Jordano P (2000) Fruits and frugivory. In: Fenner M (ed) Seeds: the ecology of regeneration in natural plant communities. CAB International, Wallingford, pp 125–166

    Chapter  Google Scholar 

  • Jordano P, Forget P-M, Lambert JE, Böhning-Gaese K, Traveset A, Wright SJ (2011) Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biol Lett 7:321–323

    Article  PubMed  Google Scholar 

  • Jose S, Gillespie AR (1998) Allelopathy in black walnut (Juglans nigra L.) alley cropping. II. Effects of juglone on hydroponically grown corn (Zea mays L.) and soybean (Glycine max L. Merr.) growth and physiology. Plant Soil 203:199–205

    Article  CAS  Google Scholar 

  • Kevan PG, Eisikowitch D, Fowle S, Thomas K (1988) Yeast-contaminated nectar and its effects on bee foraging. J Apic Res 27:26–29

    Google Scholar 

  • Kiers ET, van der Heijden MGA (2006) Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary cooperation. Ecology 87:1627–1636

    Article  PubMed  Google Scholar 

  • Kiers ET, Palmer TM, Ives AR, Bruno JF, Bronstein JL (2010) Mutualisms in a changing world: an evolutionary perspective. Ecol Lett 13:1459–1474

    Article  Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    Article  PubMed  CAS  Google Scholar 

  • Kluson RA (1995) Intercropping allelopathic crops with nitrogen-fixing legume crops. A tripartite legume symbiosis perspective. In: Inderjit, Dakshini KMM, Einhellig FA (eds) Allelopathy: organisms, processes, and applications. ACS Symposium Series No 582, American Chemical Society, Washington, DC, pp 193–210

  • Koide RT, Li M (1991) Mycorrhizal fungi and the nutrient ecology of three old field annual plant species. Oecologia 85:403–412

    Article  Google Scholar 

  • Kong CH, Hu F, Xu X (2002) Allelopathic potential and chemical constituents of volatiles from Ageratum conyzoides under stress. J Chem Ecol 28:1173–1182

    Article  PubMed  CAS  Google Scholar 

  • Kong CH, Li HB, Hu F, Xu XH, Wang P (2006) Allelochemicals released by rice roots and residues in soil. Plant Soil 288:47–56

    Article  CAS  Google Scholar 

  • Kong CH, Wang P, Zhao H, Xu XH, Zhu YD (2008) Impact of allelochemical exuded from allelopathic rice on soil microbial community. Soil Biol Biochem 40:1862–1869

    Article  CAS  Google Scholar 

  • Lankau RA (2011a) Resistance and recovery of soil microbial communities in the face of Alliaria petiolata invasions. New Phytol 189:536–548

    Article  PubMed  Google Scholar 

  • Lankau RA (2011b) Intraspecific variation in allelochemistry determines an invasive species’ impact on soil microbial communities. Oecologia 165:453–463

    Article  PubMed  Google Scholar 

  • Lankau RA (2012) Coevolution between invasive and native plants driven by chemical competition and soil biota. Proc Natl Acad Sci USA. doi:10.1073/pnas.1201343109

    PubMed  Google Scholar 

  • Lankau RA, Strauss SY (2007) Mutual feedbacks maintain both genetic and species diversity in a plant community. Science 317:1561–1563

    Article  PubMed  CAS  Google Scholar 

  • Lankau RA, Nuzzo V, Spyreas G, Davis AS (2009) Evolutionary limits ameliorate the negative impact of an invasive plant. Proc Natl Acad Sci USA 106:15362–15367

    Article  PubMed  CAS  Google Scholar 

  • Lankau RA, Wheeler E, Bennett AE, Strauss SY (2011) Plant–soil feedbacks contribute to an intransitive competitive network that promotes both genetic and species diversity. J Ecol 99:176–185

    Article  Google Scholar 

  • Levey DJ (2004) The evolutionary ecology of ethanol production and alcoholism. Integr Comp Biol 44:284–289

    Article  PubMed  CAS  Google Scholar 

  • Levey DJ, Tewksbury JJ, Izhaki I, Tsahar E, Haak DC (2007) Evolutionary ecology of secondary compounds in ripe fruit: case studies with capsaicin and emodin. In: Dennis AJ, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CAB International, Cambridge, pp 37–58

    Chapter  Google Scholar 

  • Loi RX, Solar MC, Weidenhamer JD (2008) Solid-phase microextraction method for in vivo measurement of allelochemical uptake. J Chem Ecol 34:70–75

    Article  PubMed  CAS  Google Scholar 

  • Macías FA, Torres A, Molinllo JMG, Varela RM, Castellano D (1996) Potential allelopathic sesquiterpene lactones from sunflower leaves. Phytochemistry 43:1205–1215

    Article  Google Scholar 

  • Macías FA, Fernández A, Varela RM, Molinillo JMG, Torres A, Alves PLCA (2006) Sesquiterpene lactones as allelochemicals. J Nat Prod 69:795–800

    Article  PubMed  CAS  Google Scholar 

  • Mallik AU, Zhu H (1995) Overcoming allelopathic growth inhibition by mycorrhizal inoculation.. In: Inderjit, Dakshini KMM, Einhellig FA (eds) Allelopathy: organisms, processes, and applications. ACS Symposium Series No 582, American Chemical Society, Washington, DC, pp 39–57

  • Manson JS, Otterstatter MC, Thomson JD (2010) Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia 162:81–89

    Article  PubMed  Google Scholar 

  • Meinhardt KA, Gehring CA (2012) Disrupting mycorrhizal mutualisms: a potential mechanism by which exotic tamarisk outcompetes native cottonwoods. Ecology 22:532–549

    Google Scholar 

  • Morra MJ, Kirkegaard JA (2002) Isothiocyanate release from soil-incorporated Brassica tissues. Soil Biol Biochem 34:1683–1690

    Article  CAS  Google Scholar 

  • Mummey DL, Rillig MC (2006) The invasive plant species Centaurea maculosa alters arbuscular mycorrhizal fungal communities in the field. Plant Soil 288:81–90

    Article  CAS  Google Scholar 

  • Mummey DL, Rillig MC, Holben WE (2005) Neighboring plant influences on arbuscular mycorrhizal fungal community composition as assessed by T-RFLP analysis. Plant Soil 271:83–90

    Article  CAS  Google Scholar 

  • National Research Council (2007) Status of pollinators in North America. National Academies Press, Washington DC

    Google Scholar 

  • Nilsson M-C, Högberg P, Zackrisson O, Fengyou W (1993) Allelopathic effects by Empetrum hermaphroditum on development and nitrogen uptake by roots and mycorrhizae of Pinus silvestris. Can J Bot 71:620–628

    Article  Google Scholar 

  • Ninkovic V, Glinwood R, Dahlin I (2009) Weed–barley interactions affect plant acceptance by aphids in laboratory and field experiments. Entomol Exp Appl 133:38–45

    Article  Google Scholar 

  • Onwubiko NC, Uguru MI, Ngwuta AA, Inyang ET, Nnajiemere OJ (2011) Floral biology of bambara groundnut [Vigna subterranean (L.) Verdc]. J Plant Breed Crop Sci 3:293–295

    Google Scholar 

  • Parker BJ, Barribeau SM, Laughton AM, de Roode JC, Gerardo NM (2011) Non-immunological defense in an evolutionary framework. Trends Ecol Evol 26:242–248

    Article  PubMed  Google Scholar 

  • Patterson DT (1981) Effects of allelopathic chemicals on growth and physiological responses of soybean (Glycine max). Weed Sci 29:53–59

    CAS  Google Scholar 

  • Pedersen CT, Safir GR, Siqueiro JO, Parent S (1991) Effect of phenolic compounds on asparagus mycorrhizae. Soil Biol Biochem 23:491–494

    Article  CAS  Google Scholar 

  • Pellisier F (1993) Allelopathic effect of phenolic acids from humic solutions on two spruce mycorrhizal fungi: Cenococcum graniforme and Laccaria laccata. J Chem Ecol 19:2105–2114

    Article  Google Scholar 

  • Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243

    Article  PubMed  CAS  Google Scholar 

  • Piotrowski JS, Morford SL, Rillig MC (2008) Inhibition of colonization by a native arbuscular mycorrhizal fungal community via Populus trichocarpa litter, litter extract, and soluble phenolic compounds. Soil Biol Biochem 40:709–717

    Article  CAS  Google Scholar 

  • Prats E, Galindo JC, Bazzalo ME, León A, Macías FA, Rubiales D, Jorrín JV (2007) Antifungal activity of a new phenolic compound from capitulum of a head rot-resistance sunflower genotype. J Chem Ecol 33:2245–2253

    Article  PubMed  CAS  Google Scholar 

  • Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569

    Article  Google Scholar 

  • Roberts KJ, Anderson RC (2001) Effect of garlic mustard [Alliaria petiolata (Beib. Cavara and Grande)] extracts on plants and arbuscular mycorrhizal (AM) fungi. Am Midl Nat 146:146–152

    Article  Google Scholar 

  • Robinson RK (1972) The production by roots of Calluna vulgaris of a factor inhibitory to growth of some mycorrhizal fungi. J Ecol 60:219–224

    Article  Google Scholar 

  • Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222:187–209

    Article  CAS  Google Scholar 

  • Sánchez-Moreiras AM, Oliveros-Bastidas A, Reigosa MJ (2010) Reduced photosynthetic activity is directly correlated with 2-(3H)-benzoxazolinone accumulation in lettuce leaves. J Chem Ecol 36:205–209

    Article  PubMed  CAS  Google Scholar 

  • Sanon A, Béguiristain T, Cébron A, Berthelin J, Ndoye I, Leyval C, Sylla S, Duponnois R (2009) Changes in soil diversity and global activities following invasions of the exotic invasive plant, Amaranthus viridis L., decrease the growth of native Sahelian Acacia species. FEMS Microbiol Ecol 70:118–131

    Article  PubMed  CAS  Google Scholar 

  • Sanon A, Béguiristain T, Cébron A, Berthelin J, Sylla S, Duponnois R (2012) Differences in nutrient availability and mycorrhizal infectivity in soils invaded by an exotic plant negatively influence the development of indigenous Acacia species. J Env Manag 95:S275–S279

    Article  CAS  Google Scholar 

  • Schaefer HM, Schaefer V (2007) The evolution of visual fruit signals: concepts and constraints. In: Dennis AJ, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CAB International, Cambridge, pp 59–77

    Chapter  Google Scholar 

  • Schemske D (1978) Evolution of reproductive characteristics in Impatiens (Balsaminaceae): the significance of cleistogamy and chasmogamy. Evolution 59:596–613

    Google Scholar 

  • Schreiner RP, Koide RT (1993) Antifungal compounds from the roots of mycotrophic and non-mycotrophic plant species. New Phytol 123:99–105

    Article  CAS  Google Scholar 

  • Singer MS, Mace KC, Bernays EA (2009) Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars. PLoS One 4(3):e4796. doi:10.1371/journal.pone.0004796

    Article  PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London

    Google Scholar 

  • Snow AA, Whigham DF (1989) Costs of flower and fruit production in Tipularia discolor (Orchidaceae). Ecology 70:1286–1293

    Article  Google Scholar 

  • Southwick EE (1984) Photosynthate allocation to floral nectar: a neglected energy investment. Ecology 65:1775–1779

    Article  CAS  Google Scholar 

  • Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos J (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:727–731

    Article  CAS  Google Scholar 

  • Stinson KA, Kaufman S, Durbin L, Lowenstein F (2007) Impacts of garlic mustard invasion on a forest understory community. Northeast Nat 14:73–88

    Article  Google Scholar 

  • Strauss SY, Siemens DH, Decher MB, Mitchell-Olds T (1999) Ecological costs of plant resistance to herbivores in the currency of pollination. Ecology 53:1105–1113

    Google Scholar 

  • Timbal J, Gelpe J, Garbaye J (1990) Preliminary study on the effect of Molinia caerulea on growth and mycorrhizal status of northern red oak (Quercus rubra) seedlings. Ann Sci For 47:643–649

    Article  Google Scholar 

  • Urgenson LS, Reichard SH, Halpern CB (2012) Multiple competitive mechanisms underlie the effects of a strong invader on early- to late-seral tree seedlings. J Ecol 100:1204–1215

    Google Scholar 

  • Valido A, Olesen JM (2007) The importance of lizards as frugivores and seed dispersers. In: Dennis AJ, Schupp EW, Green RJ, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CAB International, Cambridge, pp 124–147

    Chapter  Google Scholar 

  • Varga S, Kytöviita M-M (2010) Gender dimorphism and mycorrhizal symbiosis affect floral visitors and reproductive output in Geranium sylvaticum. Funct Ecol 24:750–758

    Article  Google Scholar 

  • Vaughn SF, Berhow MA (1999) Allelochemicals isolated from tissues of the invasive weed garlic mustard (Alliaria petiolata). J Chem Ecol 25:2495–2504

    Article  CAS  Google Scholar 

  • Vierheilig H, Bennett R, Kiddle G, Kaldorf M, Ludwig-Müller J (2000) Differences in glucosinolate patterns and arbuscular mycorrhizal status of glucosinolate-containing plant species. New Phytol 146:343–352

    Article  CAS  Google Scholar 

  • Vyvyan JR (2002) Allelochemicals as leads for new herbicides and agrochemicals. Tetrahedron 58:1631–1646

    Article  CAS  Google Scholar 

  • Wacker TL, Safir GR, Stephens CT (1990a) Effects of ferulic acid on Glomus fasciculatum and associated effects on phosphorus uptake and growth of asparagus (Asparagus officinalis L.). J Chem Ecol 16:901–909

    Article  CAS  Google Scholar 

  • Wacker TL, Safir GR, Stephenson SN (1990b) Evidence for succession of mycorrhizal fungi in Michigan asparagus fields. Acta Hortic 271:273–279

    Google Scholar 

  • Weston LA, Duke SO (2003) Weed and crop allelopathy. Crit Rev Plant Sci 22:367–389

    Article  CAS  Google Scholar 

  • Wiens F, Zitzmann A, Lachance M-A, Yegles M, Pragst F, Wurst FM, von Holst D, Guan SL, Spanagel R (2008) Chronic intake of fermented floral nectar by wild treeshrews. Proc Natl Acad Sci USA 105:10426–10431

    Article  PubMed  CAS  Google Scholar 

  • Wills C, Condit R, Foster RB, Hubbell SP (1997) Strong density- and diversity-related effects help to maintain tree species diversity in a neotropical forest. Proc Natl Acad Sci USA 94:1252–1257

    Article  PubMed  CAS  Google Scholar 

  • Wolfe BE, Husband BC, Klironomos JN (2005) Effects of a belowground mutualism on an aboveground mutualism. Ecol Lett 8:218–223

    Article  Google Scholar 

  • Wolfe BE, Rodgers VL, Stinson KA, Pringle A (2008) The invasive plant Alliaria petiolata (garlic mustard) inhibits ectomycorrhizal fungi in its introduced range. J Ecol 96:777–783

    Article  Google Scholar 

  • Wyatt R (1982) Inflorescence architecture: how flower number, arrangement, and phenology affect pollination and fruit-set. Am J Bot 69:585–594

    Article  Google Scholar 

  • Yamasaki SH, Fyles JW, Egger KN, Titus BD (1998) The effect of Kalmia angustifolia on the growth, nutrition, and ectomycorrhizal symbiont community of black spruce. For Ecol Manag 105:197–207

    Article  Google Scholar 

  • Yun KW, Choi SK (2002) Mycorrhizal colonization and plant growth affected by aquaeous extract of Artemisia princeps var. orientalis and two phenolic compounds. J Chem Ecol 28:353–362

    Article  PubMed  CAS  Google Scholar 

  • Yun KW, Maun A, Kim JH (2007) Effects of the aqueous extract from Artemisia campestris spp. caudata on mycorrhizal fungi colonization and growth of sand dune grasses. J Plant Biol 50:358–361

    Article  Google Scholar 

  • Zhang C, Tanabe K, Tamura F, Itai A, Wang S (2005) Partitioning of 13C-photosynthate from spur leaves during fruit growth of three Japanese pear (Pyrus pyrifolia) cultivars differing in maturation date. Ann Bot 95:685–693

    Article  PubMed  CAS  Google Scholar 

  • Zhang Q, Yao LJ, Yang RY, Yang XY, Tang JJ, Chen X (2007) Potential allelopathic effects of an invasive species Solidago canadensis on the mycorrhizae of native plant species. Allelopath J 20:71–78

    CAS  Google Scholar 

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Acknowledgments

This research was support by NSF award DEB 0958676 to SK, a Botany-in-Action Fellowship from Phipps Conservatory, and a Sigma-Xi Grants-in-Aid of Research to ANH. We thank RB Spigler, N Brouwer, and two anonymous reviewers for comments.

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Correspondence to Alison N. Hale.

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Hale, A.N., Kalisz, S. Perspectives on allelopathic disruption of plant mutualisms: a framework for individual- and population-level fitness consequences. Plant Ecol 213, 1991–2006 (2012). https://doi.org/10.1007/s11258-012-0128-z

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