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Floral herbivory in the carnivorous plant, Sarracenia alata

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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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Photographs by J. Horner

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References

  • Adamec L (1997) Mineral nutrition of carnivorous plants: a review. Bot Rev 63:273–299

    Google Scholar 

  • Atwater DZ, Butler JL, Ellison AM (2006) Spatial distribution and impacts of moth herbivory on Northern pitcher plants. Northeast Nat 13:43–56

    Google Scholar 

  • 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

    Google Scholar 

  • Bodri MS, Gaspard AM (2006) The pollination biology of Sarracenia alata Wood (Sarraceniaceae) in Louisiana. Bartonia 63:1–9

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Brewer JS (2001) A demographic analysis of fire-stimulated seedling establishment of Sarracenia alata (Sarraceniaceae). Am J Bot 88:1250–1257

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant anti-herbivore defense. Science 230:895–899

    CAS  PubMed  Google Scholar 

  • Crawley MJ (1989) Insect herbivores and plant population dynamics. Annu Rev Entomol 34:531–564

    Google Scholar 

  • 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

    Google Scholar 

  • Ellison AM (2006) Nutrient limitation and stoichiometry of carnivorous plants. Plant Biol 8:740–747

    CAS  PubMed  Google Scholar 

  • Ellison AM, Adamec L (2011) Ecophysiological traits of terrestrial and aquatic carnivorous plants: are the costs and benefits the same? Oikos 120:1721–1731

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ellison AM, Parker JN (2002) Seed dispersal and seedling establishment of Sarracenia purpurea (Sarraceniaceae). Am J Bot 89:1024–1026

    PubMed  Google Scholar 

  • Folkerts DR, Folkerts GW (1996) Aids for field identification of pitcher plant moths of the genus Exyra (Lepidoptera: Noctuidae). Entomol News 107:128–136

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Haack RA, Byler JW (1993) Insects and pathogens: regulators of forest ecosystems. J for 91(9):32–37

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Horner JD (2014) Phenology and pollinator-prey conflict in the carnivorous plant, Sarracenia alata. Am Midl Nat 171:153–156

    Google Scholar 

  • Irwin RE, Warren PS, Carper AL, Adler LS (2014) Plant-animal interactions in suburban environments: implications for floral evolution. Oecologia 174:803–815

    PubMed  Google Scholar 

  • Jones FM (1907) Pitcher-plant insects—II. Entomol News 18:413–420

    Google Scholar 

  • Jones FM (1921) Pitcher plants and their moths: The influence of insect-trapping plants on their insect associates. Nat Hist 21:296–316

    Google Scholar 

  • Juniper BE, Robins RJ, Joel DM (1989) The carnivorous plants. Academic Press, London

    Google Scholar 

  • 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

    Google Scholar 

  • Krupnick GA, Weis AE (1999) The Effect of floral herbivory on male and female reproductive success in Isomeris arborea. Ecology 80:135–149

    Google Scholar 

  • Krupnick GA, Weis AE, Campbell DR (1999) The consequences of floral herbivory for pollinator service to Isomeris arborea. Ecology 80:125–134

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Lloyd FE (1942) The carnivorous plants. Chronica Botanica, Waltham

    Google Scholar 

  • Louda SM, Potvin MA (1995) Effect of inflorescence-feeding insects on the demography and lifetime fitness of a native plant. Ecology 76:229–245

    Google Scholar 

  • McCall AC (2010) Does dose-dependent petal damage affect pollen limitation in an annual plant? Botany 88:601–605

    Google Scholar 

  • McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 9:1351–1365

    PubMed  Google Scholar 

  • Møllers AP (1995) Bumblebee preference for symmetrical flowers. Proc Natl Acad Sci USA 92:2288–2292

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Mothershead K, Marquis RJ (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81:30–40

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Schmitz OJ (2008) Herbivory from individuals to ecosystems. Annu Rev Ecol Evol Syst 39:133–152

    Google Scholar 

  • Schnell DE (1976) Carnivorous plants of the United States and Canada. John F. Blair, Winston-Salem

    Google Scholar 

  • Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Stephens JD, Folkerts DR (2012) Life history aspects of Exyra semicrocea (pitcher plant moth) (Lepidoptera: Noctuidae). Southeast Nat 11:111–126

    Google Scholar 

  • 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

    Google Scholar 

  • Tsuji K, Ohgushi T (2018) Florivory indirectly decreases the plant reproductive output through changes in pollinator attraction. Ecol Evol 8:2993–3001

    PubMed  PubMed Central  Google Scholar 

  • Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    PubMed  Google Scholar 

  • 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

    Google Scholar 

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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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Authors contributed equally to the design, field work, statistical analysis, and writing of the project. ZMW performed most of the laboratory analyses.

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Correspondence to John D. Horner.

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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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