The ethics of theft: Reevaluating the impacts of floral larceny on plant reproductive success

doi:10.1016/j.pld.2024.12.004

Abstract

Abstract: Plants and their interaction partners offer unparalleled views of evolutionary ecology. Nectar larceny, entailing nectar extraction without pollinating, is thought to be an example of a harmful, antagonistic behavior, but the precise consequences of floral larceny on plant reproductive success remain contentious. We conducted a comprehensive meta-analysis of 153 studies across 120 plant species, using 14 moderators to assess the effects of floral larceny on plant reproductive success and examine the key moderators. We found that floral larceny negatively impacts flower traits, pollinator visitation, pollen deposition, and fruit set, while having a neutral effect on critical female fitness indicators, such as seed set and seed quality, as well as on male fitness. By altering pollinator behavior, floral larceny may reduce geitonogamy, potentially enhancing genetic diversity. Additionally, factors such as pollinator type, plant mating system, and pollen limitation were identified as key moderators of these effects. Our analysis reveals an ultimately neutral effect of floral larceny on plant reproductive success, with potential benefits in certain contexts. These findings suggest that floral larceny plays a complex and multifaceted role within plant-pollinator interactions, facilitating the evolutionary stability and coexistence of floral larcenists and host plants.

Key words: Floral larceny, Nectar robbing, Nectar thief, Plant-pollinator interactions, Plant reproductive success, Indirect effects

Jin-Ru Zhong, Xiao-Fang Jin, Michael C. Orr, Xiao-Qing Li, Yong-Deng He, Sheng-Wei Wang, Qing-Feng Wang, Chun-Feng Yang, Zhong-Ming Ye. The ethics of theft: Reevaluating the impacts of floral larceny on plant reproductive success[J]. Plant Diversity, 2025, 47(01): 148-158.

References

Bergamo, P.J., Sazima, M., 2018. Differential outcomes of nectar robbing on the reproductive success of a melittophilous and an ornithophilous species. Int. J. Plant Sci. 179, 192-197.
Burd, M., 1994. Bateman’s principle and plant reproduction: the role of pollen limitation in fruit and seed set. Bot. Rev. 60, 83-139.
Burkle, L.A., Irwin, R.E., Newman, D.A., 2007. Predicting the effects of nectar robbing on plant reproduction: implications of pollen limitation and plant mating system. Am. J. Bot. 94, 1935-1943.
Carbonari, V., Polatto, L.P., Junior, V.V.A., 2009. Evaluation of the impact on Pyrostegia venusta (Bignoniaceae) flowers due to nectar robbery by Apis mellifera (Hymenoptera, Apidae). Sociobiology 54, 373-382.
Cayenne Engel, E., Irwin, R.E., 2003. Linking pollinator visitation rate and pollen receipt. Am. J. Bot. 90, 1612-1618.
Chamberlain, S.A., Hovick, S.M., Dibble, C.J., et al., 2012. Does phylogeny matter? assessing the impact of phylogenetic information in ecological meta-analysis. Ecol. Lett. 15, 627-636.
Cronk, Q., Ojeda, I., 2008. Bird-pollinated flowers in an evolutionary and molecular context. J. Exp. Bot. 59, 715-727.
Darwin, C., 1877. The Effects of Cross and Self Fertilisation in the Vegetable Kingdom. John Murray, London.
Dedej, S., Delaplane, K., 2005. Net energetic advantage drives honey bees (Apis mellifera L.) to nectar larceny in Vaccinium ashei Reade. Behav. Ecol. Sociobiol. 57, 398-403.
Deng, X.B., Ren, P.Y., Li, Q.J., 2005. Nectar secretion patterns, floral visitor behavior and their impacts on fruit and seed sire of Alpinia blepharocalyx. Acta Phytoecol. Sin. 29, 274-280.
Duval, S., Tweedie, R., 2000. A nonparametric “trim and fill” method of accounting for publication bias in meta-analysis. J. Am. Stat. Assoc. 95, 89-98.
Egger, M., Davey Smith, G., Schneider, M., et al., 1997. Bias in meta-analysis detected by a simple, graphical test. BMJ (Clinical research ed.) 315, 629-634.
Fumero-Caban, J.J., Melendez-Ackerman, E.J., 2013. Effects of nectar robbing on pollinator behavior and plant reproductive success of Pitcairnia angustifolia (Bromeliaceae). Plant Species Biol. 28, 224-234.
Galen, C., 1983. The effects of nectar thieving ants on seedset in floral scent morphs of Polemonium viscosum. Oikos 41, 245-249.
Gass, C., Montgomerie, R., 1981. Hummingbird foraging behavior: decision-making and energy regulation. In: Kamil, A., Sargent, T. (Eds.). Foraging Behavior: Ecological, Ethological, and Psychological Approaches. Garland, New York, pp. 159-194.
Gonzalez-Browne, C., Murua, M.M., Navarro, L., et al., 2016. Does plant origin influence the fitness impact of flower damage? A meta-analysis. PLoS One 11, e0146437.
Hedges, L.V., Gurevitch, J., Curtis, P.S., 1999. The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150-1156.
Hothorn, T., Bretz, F., Westfall, P., 2008. Simultaneous inference in general parametric models. Biom. J. 50, 346-363.
Inouye, D.W., 1980. The terminology of floral larceny. Ecology 61, 1251-1253.
Irwin, R., Maloof, J., 2002. Variation in nectar robbing over time, space, and species. Oecologia 133, 525-533.
Irwin, R.E., 2003. Impact of nectar robbing on estimates of pollen flow: conceptual predictions and empirical outcomes. Ecology 84, 485-495.
Irwin, R.E., 2009. Realized tolerance to nectar robbing: compensation to floral enemies in Ipomopsis aggregata. Ann. Bot. 103, 1425-1433.
Irwin, R.E., Adler, L.S., Brody, A.K., 2004. The dual role of floral traits: pollinator attraction and plant defense. Ecology 85, 1503-1511.
Irwin, R.E., Brody, A.K., 1999. Nectar-robbing bumble bees reduce the fitness of Ipomopsis aggregata (Polemoniaceae). Ecology 80, 1703-1712.
Irwin, R.E., Brody, A.K., Waser, N.M., 2001. The impact of floral larceny on individuals, populations, and communities. Oecologia 129, 161-168.
Irwin, R.E., Bronstein, J.L., Manson, J.S., Richardson, L. 2010. Nectar robbing: ecological and evolutionary perspectives. Annu. Rev. Ecol. Evol. Syst. 41(1), 271-292.
Irwin, R.E., Galen, C., Rabenold, J.J., et al., 2008. Mechanisms of tolerance to floral larceny in two wildflower species. Ecology 89, 3093-3104.
Irwin, R.E., Howell, P., Galen, C., 2015. Quantifying direct vs. indirect effects of nectar robbers on male and female components of plant fitness. J. Ecol. 103, 1487-1497.
Jin, Y., Qian, H., 2023. U.PhyloMaker: An R package that can generate large phylogenetic trees for plants and animals. Plant Divers. 45, 347-352.
Knight, T.M., Steets, J.A., Vamosi, J.C., et al., 2005. Pollen limitation of plant reproduction: pattern and process. Annu. Rev. Ecol. Evol. Syst. 36, 467-497.
Koricheva, J., Gurevitch, J., Mengersen, K.L., 2013. Handbook of meta-analysis in ecology and evolution. Princeton University Press, Princeton.
Lajeunesse, M.J., 2016. Facilitating systematic reviews, data extraction and meta-analysis with the METAGEAR package for R. Methods Ecol. Evol. 7, 323-330.
Lara, C., Ornelas, J.F., 2002. Flower mites and nectar production in six hummingbird-pollinated plants with contrasting flower longevities. Can. J. Bot. 80, 1216-1229.
Maidana-Tuco, Y.N., Larrea-Alcazar, D.M., Pacheco, L.F., 2024. Nectar robbing effects on pollinators of a key nectar source plant (Tecoma fulva, Bignoniaceae) in a dry tropical Andean valley. Biotropica 56, e13319.
Maloof, J.E., 2001. The effects of a bumble bee nectar robber on plant reproductive success and pollinator behavior. Am. J. Bot. 88, 1960-1965.
Maloof, J.E., Inouye, D.W., 2000. Are nectar robbers cheaters or mutualists? Ecology 81, 2651-2661.
Navarro, L., 1999. Pollination ecology and effect of nectar removal in Macleania bullata (Ericaceae). Biotropica 31, 618-625.
Navarro, L., 2000. Pollination ecology of Anthyllis vulneraria subsp. vulgaris (Fabaceae): nectar robbers as pollinators. Am. J. Bot. 87, 980-985.
Navarro, L., 2001. Reproductive biology and effect of nectar robbing on fruit production in Macleania bullata (Ericaceae). Plant Ecol. 152, 59-65.
Newman, D.A., Thomson, J.D., 2005. Effects of nectar robbing on nectar dynamics and bumblebee foraging strategies in Linaria vulgaris (Scrophulariaceae). Oikos 110, 309-320.
Nunez-Farfan, J., Fornoni, J., Valverde, P.L., 2007. The evolution of resistance and tolerance to herbivores. Annu. Rev. Ecol. Evol. Syst. 38, 541-566.
Paradis, E., Claude, J., Strimmer, K., 2004. Ape: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290.
Pleasants, J.M., 1983. Nectar production patterns in Ipomopsis aggregata (Polemoniaceae). Am. J. Bot. 70, 1468-1475.
Pyke, G.H., 1991. What does it cost a plant to produce floral nectar? Nature 350, 58-59.
R Core Team, 2022. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Richman, S.K., Barker, J.L., Baek, M., et al., 2021. The sensory and cognitive ecology of nectar robbing. Front. Ecol. Evol. 9, 698137.
Richman, S.K., Irwin, R.E., Bosak, J.T., et al., 2018. Consequences of secondary nectar robbing for male components of plant reproduction. Am. J. Bot. 105, 943-949.
Rosenberg, M., 2005. The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59, 464-468.
Rosenthal, R., 1986. Meta-analytic procedures for social science research sage publications. Educ. Res. 15, 18-20.
Roubik, D., 1982. The ecological impact of nectar-robbing bees and pollinating hummingbirds on a tropical shrub. Ecology 63, 54-60.
Tang, B., Man, J., Lehmann, A., et al., 2023. Arbuscular mycorrhizal fungi benefit plants in response to major global change factors. Ecol. Lett. 26, 2087-2097.
Tuck, S.L., Winqvist, C., Mota, F., et al., 2014. Land-use intensity and the effects of organic farming on biodiversity: a hierarchical meta-analysis. J. Appl. Ecol. 51, 746-755.
Vico, G., Manzoni, S., Nkurunziza, L., et al., 2016. Trade-offs between seed output and life span-a quantitative comparison of traits between annual and perennial congeneric species. New Phytol. 209, 104-114.
Viechtbauer, W., 2010. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1-48.
Wan, X., Wang, W.Q., Liu, J.M., et al., 2014. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med. Res. Methodol. 14, 135.
Zhang, Y.W., Yu, Q., Zhao, J.M., et al., 2009. Differential effects of nectar robbing by the same bumble-bee species on three sympatric Corydalis species with varied mating systems. Ann. Bot. 104, 33-39.