Abstract
Losses of floral tissues to herbivory (florivory) can affect plant reproduction, population growth and structure, and community dynamics. Because carnivorous plants inhabit nutrient-poor environments and exhibit slow growth rates, losses to herbivory may be particularly costly. However, there has been no published study of florivory in carnivorous plants. We conducted a 2-year field study in Leon County, Texas USA, on the carnivorous Pale Pitcher Plant Sarracenia alata and its specialist herbivore Exyra semicrocea. We surveyed the proportions of flowers attacked and compared the mass of floral components (ovaries, anthers, petals, sepals, and style) between attacked and undamaged flowers. In 2017, a mean of 53% of flowers was attacked. The anther count and the masses of anthers, perianth (petals + sepals), and style were significantly lower in attacked flowers than in undamaged flowers, but ovary mass was not significantly affected. The total flower dry mass (without peduncle) of attacked flowers on the last collection date was 13.3% less than that of undamaged flowers, but this difference was not statistically significant. In 2018, a mean of 33% of flowers were attacked, with significant mass losses from all floral components, including ovaries. The total flower dry mass (without peduncle) of attacked flowers on the last collection date was significantly (48%) less than that of undamaged flowers. Herbivore population size, differences in emergence phenology of the host and/or herbivore, and differential defense of components may have contributed to differences between years in the proportion of flowers attacked and variation in the floral structures consumed.
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References
Adamec L (1997) Mineral nutrition of carnivorous plants: a review. Bot Rev 63:273–299
Atwater DZ, Butler JL, Ellison AM (2006) Spatial distribution and impacts of moth herbivory on Northern pitcher plants. Northeast Nat 13:43–56
Bauer U, Rembold K, Grafe TU (2016) Carnivorous Nepenthes pitcher plants are a rich food source for a diverse vertebrate community. J Nat Hist 50:483–495
Bodri MS, Gaspard AM (2006) The pollination biology of Sarracenia alata Wood (Sarraceniaceae) in Louisiana. Bartonia 63:1–9
Botto-Mahan C, Ramírez PA, Gloria OC, Medel R, Ojeda-Camacho M, González AV (2011) Floral herbivory affects female reproductive success and pollinator visitation in the perennial herb Alstroemeria ligtu (Alstroemeriaceae). Int J Plant Sci 172:1130–1136
Brewer JS (1999) Short-term effects of fire and competition on growth and plasticity of the yellow pitcher plant, Sarracenia alata (Sarraceniaceae). Am J Bot 86:1264–1271
Brewer JS (2001) A demographic analysis of fire-stimulated seedling establishment of Sarracenia alata (Sarraceniaceae). Am J Bot 88:1250–1257
Cardel YJ, Koptur S (2010) Effects of florivory on the pollination of flowers: an experimental field study with a perennial plant. Int J Plant Sci 171:283–292
Carmickle R, Horner JD (2019) Impact of the specialist herbivore Exyra semicrocea on the carnivorous plant Sarracenia alata: a field experiment testing the effects of tissue loss and diminished prey capture on plant growth. Plant Ecol 220:553–561
Carper AL, Adler LS, Irwin RE (2016) Effects of florivory on plant-pollinator interactions: implications for male and female components of plant reproduction. Am J Bot 103:1061–1070
Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant anti-herbivore defense. Science 230:895–899
Crawley MJ (1989) Insect herbivores and plant population dynamics. Annu Rev Entomol 34:531–564
Cross AT, Krueger TA, Gonella PM, Robinson AS, Fleischmann AS (2020) Conservation of carnivorous plants in the age of extinction. Glob Ecol Conserv 24:1–30
Ellison AM (2006) Nutrient limitation and stoichiometry of carnivorous plants. Plant Biol 8:740–747
Ellison AM, Adamec L (2011) Ecophysiological traits of terrestrial and aquatic carnivorous plants: are the costs and benefits the same? Oikos 120:1721–1731
Ellison AM, Gotelli NJ (2009) Energetics and the evolution of carnivorous plants—Darwin’s ‘most wonderful plants in the world.’ J Exp Bot 60:19–42
Ellison AM, Parker JN (2002) Seed dispersal and seedling establishment of Sarracenia purpurea (Sarraceniaceae). Am J Bot 89:1024–1026
Folkerts DR, Folkerts GW (1996) Aids for field identification of pitcher plant moths of the genus Exyra (Lepidoptera: Noctuidae). Entomol News 107:128–136
Gilbert KJ, Nitta JH, Talavera G, Pierce NE (2018) Keeping an eye on coloration: ecological correlates of the evolution of pitcher traits in the genus Nepenthes (Caryophyllales). Biol J Linn Soc 123:321–337
Givnish TJ, Burkhardt EL, Happel RE, Weintraub JD (1984) Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. Am Nat 124:479–497
Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194
Haack RA, Byler JW (1993) Insects and pathogens: regulators of forest ecosystems. J for 91(9):32–37
Heath JJ, Kessler A, Woebbe E, Cipollini D, Stireman JO III (2014) Exploring plant defense theory in tall goldenrod, Solidago altissima. New Phytol 202:1357–1370
Hendrix SD (1988) Herbivory and its impact on plant reproduction. In: Lovett Doust J, Lovett Doust L (eds) Plant reproductive ecology: patterns and strategies. Oxford University Press, New York, pp 246–263
Horner JD (2014) Phenology and pollinator-prey conflict in the carnivorous plant, Sarracenia alata. Am Midl Nat 171:153–156
Irwin RE, Warren PS, Carper AL, Adler LS (2014) Plant-animal interactions in suburban environments: implications for floral evolution. Oecologia 174:803–815
Jones FM (1907) Pitcher-plant insects—II. Entomol News 18:413–420
Jones FM (1921) Pitcher plants and their moths: The influence of insect-trapping plants on their insect associates. Nat Hist 21:296–316
Juniper BE, Robins RJ, Joel DM (1989) The carnivorous plants. Academic Press, London
Kirk WD, Ali M, Breadmore KN (1995) The effects of pollen beetles on the foraging behavior of honey bees. J Apic Res 34:15–22
Krupnick GA, Weis AE (1999) The Effect of floral herbivory on male and female reproductive success in Isomeris arborea. Ecology 80:135–149
Krupnick GA, Weis AE, Campbell DR (1999) The consequences of floral herbivory for pollinator service to Isomeris arborea. Ecology 80:125–134
Lamb T, Kalies EL (2020) An overview of lepidopteran herbivory on North American pitcher palnts (Sarracenia), with a novel observation of feeding on Sarracenia flava. J Lepid Soc 74:193–197
Leavitt H, Robertson IC (2006) Petal herbivory by chysomelid beetles (phyllotreta sp.) is detrimental to pollination and seed production in Lepidium papilliferum (Brassicaceae). Ecol Entomol 31:657–660
Lin L, Xu C (2020) Arcsine-based transformations for meta-analysis of proportions: pros, cons, and alternatives. Health Sci Rep. https://doi.org/10.1002/hsr2.178
Lloyd FE (1942) The carnivorous plants. Chronica Botanica, Waltham
Louda SM, Potvin MA (1995) Effect of inflorescence-feeding insects on the demography and lifetime fitness of a native plant. Ecology 76:229–245
McCall AC (2010) Does dose-dependent petal damage affect pollen limitation in an annual plant? Botany 88:601–605
McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 9:1351–1365
Møllers AP (1995) Bumblebee preference for symmetrical flowers. Proc Natl Acad Sci USA 92:2288–2292
Moon DC, Rossi A, Stokes K, Moon J (2008) Effects of the pitcher plant mining moth Exyra semicrocea on the hooded pitcher plant Sarracenia minor. Am Midl Nat 159:321–326
Moreira X, Castagneyrol B, Abdala-Roberts L, Traveset A (2019) A meta-analysis of herbivore effects on plant attractiveness to pollinators. Ecology. https://doi.org/10.1002/bes2.1556
Mothershead K, Marquis RJ (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81:30–40
Onodera H, Oguro M, Sakai S (2014) Effects of nutrient contents and defense compounds on herbivory in reproductive organs and leaves of Iris gracilipes. Plant Ecol 215:1025–1035
Osaki H, Tagawa K (2020) Life on a deadly trap: Buckleria paludum, a specialist herbivore of carnivorous sundew plants, licks mucilage from glands for defense. Entomol Sci 23:227–230
Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press, New York, pp 3–54
Ricci CA, Meier AJ, Meier OW, Philips TK (2017) Effects of Exyra ridingsii (Lepidoptera: Noctuidae) on Sarracenia flava (Nepenthales: Sarraceniaceae). Environ Entomol 46:1346–1350
Schmitz OJ (2008) Herbivory from individuals to ecosystems. Annu Rev Ecol Evol Syst 39:133–152
Schnell DE (1976) Carnivorous plants of the United States and Canada. John F. Blair, Winston-Salem
Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268
Stegemann T, Kruse LH, Bruett M, Ober D (2019) Specific distribution of pyrrolizidine alkaloids in floral parts of comfrey (Symphytum officinale) and its implications for flower ecology. J Chem Ecol 45:128–135
Stephens JD, Folkerts DR (2012) Life history aspects of Exyra semicrocea (pitcher plant moth) (Lepidoptera: Noctuidae). Southeast Nat 11:111–126
Teixido AL, Méndez M, Valladares F (2011) Flower size and longevity influence florivory in the large-flowered shrub Cistus ladanifer. Acta Oecologica 37:418–421
Tsuji K, Ohgushi T (2018) Florivory indirectly decreases the plant reproductive output through changes in pollinator attraction. Ecol Evol 8:2993–3001
Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10
Washitani I, Okayama Y, Sato K, Takahashi H, Ohgushi T (1996) Spatial variation in female fertility related to interactions with flower consumers and pathogens in a forest metapopulation of Primula sieboldii. Popul Ecol 2:249–256
Acknowledgements
The Texas Christian University Research and Creative Activities Fund provided funding for this research. ZMW was provided support by a grant from the Department of Biology Adkins Program. The authors thank R Carmickle and Dr. M Green for field assistance and the land owners for permission to work on their property. We thank Dr. Wes Nowlin at the Aquatic Ecology Lab at Texas State University for performing nutrient analyses. Three reviewers made helpful suggestions on an earlier draft of this manuscript.
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Winer, Z.M., Horner, J.D. Floral herbivory in the carnivorous plant, Sarracenia alata. Arthropod-Plant Interactions 16, 109–118 (2022). https://doi.org/10.1007/s11829-021-09880-y
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DOI: https://doi.org/10.1007/s11829-021-09880-y