Abstract
Many adult Lepidoptera nectar at flowers of plant species on which they also deposit their eggs. As a consequence, the same partner may act as both a pollinator and herbivore. How high are the costs associated with such herbivorous pollinators, relative to the potential benefits they confer? We addressed this question in the association between Datura wrightii (Solanaceae) and Manduca sexta (Sphingidae), which in southern Arizona, USA is both the plant’s most important pollinator (as adults) and most significant herbivore (as larvae). We manually inflicted two biologically relevant levels of artificial folivory (33% and 66% leaf removal) at two points during the growing season, to nearly 200 D. wrightii plants established in a common-garden outdoor plot. We recorded plant survival, growth, and several components of reproduction (bud, flower, and fruit production). We found no detectable effect of damage on plant growth rate, fruit set in the same or the following growing season, or plant volume or survival in the same or the following three seasons. These results suggest that D. wrightii may be highly tolerant of leaf consumption by the herbivorous offspring of its specialized, nectar-feeding pollinators. We argue that this mechanism would likely foster persistence of the pollination mutualism more effectively than would resistance to, or deterrence of, herbivores. Tolerance to the costs of mutualism is an underexplored phenomenon that could contribute to the stability of these interactions.
Similar content being viewed by others
References
Adler L, Bronstein J (2004) Attracting antagonists: does floral nectar increase leaf herbivory? Ecology 85:1519–1526
Ågren J, Schemske DW (1993) The cost of defense against herbivores: an experimental study of trichome production in Brassica rapa. Am Nat 141:338–350
Altermatt F, Pearse IS (2011) Similarity and specialization of the larval versus adult diet of European butterflies and moths. Am Nat 178:372–382
Antonovics J, Bergmann J, Hempel S, Verbruggen E, Veresoglou S, Rillig M (2015) The evolution of mutualism from reciprocal parasitism: more ecological clothes for the Prisoner’s Dilemma. Evol Ecol 29:627–641
Baldwin IT (1988) Short-term damage-induced increases in tobacco alkaloids protect plants. Oecologia 75:367–370
Baldwin IT (1990) Herbivory simulations in ecological research. Trends Ecol Evol 5:91–93
Barron-Gafford GA, Rascher U, Bronstein JL, Davidowitz G, Chaszar B, Huxman TE (2012) Herbivory of wild Manduca sexta causes fast down-regulation of photosynthetic efficiency in Datura wrightii: an early signaling cascade visualized by chlorophyll fluorescence. Photosynth Res 113:249–260
Bronstein JL (2001) The costs of mutualism. Am Zool 41:127–141
Bronstein JL, Huxman TE, Davidowitz G (2007) Plant-mediated effects linking herbivory and pollination. In: Ohgushi T, Craig TP, Price PW (eds) Plant mediation in indirect interaction webs. Cambridge University Press, Cambridge UK, pp 75–103
Bronstein JL, Huxman T, Horvath B, Farabee M, Davidowitz G (2009) Reproductive biology of Datura wrightii: the benefits of a herbivorous pollinator. Ann Bot 103:1435–1443
Bustos-Segura C, Fornoni J, Núñez-Farfán J (2014) Evolutionary changes in plant tolerance against herbivory through a resurrection experiment. J Evol Biol 27:488–498
Camargo ID, Tapia-López R, Núñez-Farfán J (2015) Ecotypic variation in growth responses to simulated herbivory: trade-off between maximum relative growth rate and tolerance to defoliation in an annual plant. AoB Plants 7:15
Carmona D, Fornoni J (2013) Herbivores can select for mixed defensive strategies in plants. New Phytol 197:576–585
Chapman RF, Simpson SJ, Douglas AE (2013) The insects: structure and function, 5th edn. Cambridge University Press, New York
Cisneros-Silva A, Castillo G, Chávez-Pesqueira M, Bello-Bedoy R, Camagro ID, Núñez-Farfán J (2017) Light limitation reduces tolerance to leaf damage in Datura stramonium. Evol Ecol Res 18:351–362
Dutton EM, Luo EY, Cembrowski AR, Shore JS, Frederickson ME (2016) Three's a crowd: trade-offs between attracting pollinators and ant bodyguards with nectar rewards in Turnera. Am Nat 188:38–51
Edwards DP (2009) The roles of tolerance in the evolution, maintenance and breakdown of mutualism. Naturwissenschaften 96:1137–1145
Elle E, van Dam NM, Hare JD (1999) Cost of glandular trichomes, a "resistance" character in Datura wrightii Regel (Solanaceae). Evolution 53:22–35
Engelbrecht L, Orban U, Heese W (1969) Leaf-miner caterpillars and cytokinins in green islands of autumn leaves. Nature 223:319–321
Fornoni J (2011) Ecological and evolutionary implications of plant tolerance to herbivory. Funct Ecol 25:399–407
Fornoni J, Nuñez-Farfán J (2000) Evolutionary ecology of Datura stramonium: genetic variation and costs for tolerance to defoliation. Evolution 54:789–797
Fornoni J, Valverde P, Nuñez-Farfán J (2004) Population variation in the cost and benefit of tolerance and resistance against herbivory in Datura stramonium. Evolution 56:1696–1704
Frederickson ME, Ravenscraft A, Miller GA, Hernández LMA, Booth G, Pierce NE (2012) The direct and ecological costs of an ant-plant symbiosis. Am Nat 179:768–778
Frost CJ, Hunter MD (2008) Herbivore-induced shifts in carbon and nitrogen allocation in red oak seedlings. New Phytol 178:835–845
Garrido E, Andraca-Gómez G, Fornoni J (2011) Local adaptation: simultaneously considering herbivores and their host plants. New Phyt 193:445–453
Glaum P, Kessler A (2017) Functional reduction in pollination through herbivore-induced pollinator limitation and its potential in mutualist communities. Nat Comm 8:article 2031
Hare JD (2010) Ontogeny and season constrain the production of herbivore- inducible plant volatiles in the field. J Chem Ecol 36:1363–1374
Harrison JF, Woods HA, Roberts SP (2012) Ecological and environmental physiology of insects. Oxford University Press, Oxford
Ida TY, Harder LD, Kudo G (2012) Effects of defoliation and shading on the physiological cost of reproduction in silky locoweed Oxytropis sericea. Ann Bot 109:237–246
Irwin RE, Adler LS, Brody AK (2004) The dual role of floral traits: pollinator attraction and plant defense. Ecology 85:1503–1511
Jacobsen DJ, Raguso RA (2018) Lingering effects of herbivory and plant defenses on pollinators. Curr Biol 28:R1164–R1173
Jiménez-Lobato V, Martínez-Borda E, Núñez-Farfán J, Valverde PL, Cruz LL, López-Velázquez A, Santos-Gally R, Arroyo J (2017) Changes in floral biology and inbreeding depression in native and invaded regions of Datura stramonium. Plant Biol 20:214–223
Kariñho-Betancourt E, Agrawal A, Halitschke R, Núñez-Farfán J (2015) Phylogenetic correlations among chemical and physical plant defenses change with ontogeny. New Phytol 206:796–806
Kato M, Kawakita A (eds) (2017) Obligate pollination mutualism. Ecological Research Monographs. Springer, Tokyo
Ke P-J, Nakazawa T (2018) Ontogenetic mutualism-antagonism coupling: perspectives on resilience of stage-structured communities. Oikos 127:353–363
Kearney T, Peebles R (1960) Arizona flora. University of California Press, Berkeley
Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions. Ecology 92:1769–1780
Kessler D, Kallenbach M, Diezel C, Rothe E, Murdock M, Baldwin IT (2015) How scent and nectar influence floral antagonists and mutualists. eLife 4:7641
Krug E, Proksch P (1993) Influence of dietary alkaloids on survival and growth of Spodoptera littoralis. Biochem Syst Ecol 21:749–756
Liu J, Wang L, Wang D, Bonser SP, Sung F, Zhou Y, Gao Y, Teng X (2012) Plants can benefit from herbivory: stimulatory effects of sheep saliva on growth of Leymus chinensis. PLoS ONE 7:e29259
Louca S, Ibanez S, Piau D, Després L (2012) Specialized nursery pollination mutualisms as evolutionary traps stabilized by antagonistic traits. J Theor Biol 296:65–83
Lucas-Barbosa D (2015) Integrating studies on plant-pollinator and plant-herbivore interactions. Trends Plant Sci 21:125–133
Lucas-Barbosa D, Sun P, Hakman A, van Beek TA, van Loon JJA, Dicke M (2016) Visual and odour cues: plant responses to pollination and herbivory affect the behaviour of flower visitors. Func Ecol 30:431–441
Malé P-JG, Leroy C, Dejean S, Quilichini A, Orivel J (2012) An ant symbiont directly and indirectly limits its host plant’s reproductive success. Evol Ecol 26:55–63
Marquis R (1992) Selective impact of herbivores. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. University of Chicago Press, Chicago, pp 301–325
Mauricio R, Bowers MD, Bazzaz FA (1993) Pattern of leaf damage affects fitness of the annual plant Raphanus sativus (Brassicaceae). Ecology 74:2066–2071
Mauricio R, Rausher MD, Burdick DS (1997) Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78:1301–1311
McCall AC, Richman S, Thomson E, Edgerton M, Jordan S, Bronstein JL (2018) Do honeybees act as pollinators or pollen thieves of Datura wrightii?. J Pollinat Ecol 24:164–171
McFadden MW (1968) Observations on feeding and movement of tobacco hornworm larvae. J Econ Entomol 61:352–356
Mesa JM, Scholes DR, Juvik JA, Paige KN (2017) Molecular constraints on resistance-tolerance tradeoffs. Ecology 98:2528–2537
Meyer GA (1998) Pattern of defoliation and its effect on photosynthesis and growth of goldenrod. Funct Ecol 12:270–279
Miles PW (1968) Studies on salivary physiology of plant-bugs: experimental induction of galls. J Insect Physiol 14:97–106
Morris WF, Vázquez DP, Chacoff NP (2010) Benefit and cost curves for typical pollination mutualisms. Ecology 91:1276–1285
Motten AF, Antonovics J (1992) Determinants of outcrossing rate in a predominantly self-fertilizing weed, Datura stramonium (Solanaceae). Am J Bot 79:419–427
Núñez-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Ann Rev Ecol Evol Syst 38:541–566
Offenberg J (2001) Balancing between mutualism and exploitation: the symbiotic interaction between Lasius ants and aphids. Behav Ecol Soc 49:304–310
Ohm JR, Miller TEX (2014) Balancing anti-herbivore benefits and anti-pollinator costs of defensive mutualists. Ecology 95:2924–2935
Oliver TH, Leather SR, Cook JM (2009) Tolerance traits and the stability of mutualism. Oikos 118:346–352
Parker AJ, Williams NM, Thomson JD (2016) Specialist pollinators deplete pollen in the spring ephemeral wildflower Claytonia virginica. Ecol Evol 6:5169–5177
Potter K, Bronstein JL, Davidowitz G (2012) Choice of oviposition sites by Manduca sexta and its consequences for egg and larval performance. Entomol Exp Appl 144:286–293
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. https://www.R-project.org/
Ramos SE, Schiestl FP (2019) Rapid plant evolution driven by the interaction of pollination and herbivory. Science 364:193–196
Revilla TA, Encinas-Viso F (2015) Dynamical transitions in a pollination–herbivory interaction: A conflict between mutualism and antagonism. PLoS ONE 10:e0017964
Rudgers JA, Miller TED, Ziegler SM, Cravel KD (2012) There are many ways to be a mutualist: endophytic fungus reduces plant survival but increases population growth. Ecology 93:565–574
Sasaki M, Riddiford LM (1984) Regulation of reproductive behaviour and egg maturation in the tobacco hawk moth, Manduca sexta. Physiol Entomol 9:315–327
Sawaya GM, Goldberg AS, Steele MA, Dalgleish HJ (2018) Environmental variation shifts the relationship between trees and scatterhoarders along the continuum from mutualism to antagonism. Integr Zool 13:319–330
Schiestl FP, Kirk H, Bigler L, Cozzolino A, Desurmont GA (2014) Herbivory and floral signaling: phenotypic plasticity and tradeoffs between reproduction and indirect defense. New Phytol 203:257–266
Smith GP, Johnson CA, Davidowitz G, Bronstein JL (2018) Linkages between nectaring and oviposition preferences of Manduca sexta on two co-blooming Datura species in the Sonoran Desert. Ecol Entomol 43:85–92
Stone JL, Motten AF (2002) Anther-stigma separation is associated with inbreeding depression in Datura stramonium, a predominantly self-fertilizing annual. Evolution 56:2187–2195
Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185
Theimer TC (2005) Rodent scatterhoaders as conditional mutualists. In: Forget PM, Lambert JE, Hulme PE, Wall SBV (eds) Seed fate. CAB International, Wallingford, pp 283–295
Throop HL (2005) Nitrogen deposition and herbivory affect biomass production and allocation in an annual plant. Oikos 111:91–100
Tiffin P (2000) Mechanisms of tolerance to herbivore damage: what do we know? Evol Ecol 14:523–536
Tiffin P, Inouye BD (2000) Measuring tolerance to herbivory: accuracy and precision of estimates made using natural versus imposed damage. Evolution 54:1024–1029
Valverde PL, Fornoni J, Nuñez-Farfán J (2003) Evolutionary ecology of Datura stramonium: equal plant fitness benefits of growth and resistance against herbivory. J Evol Biol 16:127–137
Valverde PL, Arroyo J, Nuñez-Farfán J, Castillo G, Calahorra A, Pérez-Barrales R, Tapia-Lopez R (2015) Natural selection on plant resistance to herbivores in the native and introduced range. AoB Plants 7:plv090
Villamil N, Boege K, Stone GN (2018) Ant-pollinator conflict results in pollinator deterrence but no nectar trade-offs. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01093
Wilson JK, Tseng AS, Potter KA, Davidowitz G, Hildebrand JG (2018) The effects of the alkaloid scopolamine on the performance and behavior of two caterpillar species. Arthopod-Plant Int 12:21–29
Wilson JK, Woods HA, Kessler A (2018b) High levels of abiotic noise in volatile organic compounds released by a desert perennial: implications for the evolution and ecology of airborne chemical communication. Oecologia 188:367–379
Wink M, Theile V (2002) Alkaloid tolerance in Manduca sexta and phylogenetically related Sphingids (Lepidoptera : Sphingidae). Chemoecology 12:29–46
Youngsteadt E, Irwin RE, Fowler A, Bertone MA, Giacomini SJ, Kunz M, Suiter D, Sorenson CE (2018) Venus flytrap rarely traps its pollinators. Am Nat 191:539–546
Zhou W, Kügler A, McGale E, Haverkamp A, Knaden M, Guo H, Beran F, Yon F, Li R, Lackus N, Köllner TG, Bing J, Schuman MC, Hansson BS, Kessler D, Baldwin IT, Xu S (2017) Tissue-specific emission of (E)-bergamotene helps resolve the dilemma when pollinators are also herbivores. Curr Biol 27:1336–1341
Acknowledgements
We thank Monica Edgerton, Skyler Jordan, Emily McCall, and Eric Thomson for field assistance, and the Bronstein lab, Jerome K. Wilson, Anurag Agrawal, J. Heiling, J. Nuñez-Farfán, J. Fornoni, and an anonymous reviewer for helpful suggestions on the analyses, text, and citations. A.M. gratefully acknowledges the University of Arizona for hosting him during the fieldwork and writing of this manuscript. This study was supported in part by NSF Grant IOS-1053318 to G.D.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Dagmar Voigt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
McCall, A.C., Davidowitz, G. & Bronstein, J.L. How high are the costs inflicted by an herbivorous pollinator?. Arthropod-Plant Interactions 14, 387–397 (2020). https://doi.org/10.1007/s11829-020-09745-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-020-09745-w