Implications of enemy escape on chemically mediated interactions with mutualists: wild parsnip pollination in two hemispheres
DOI:
https://doi.org/10.26786/1920-7603(2013)6Abstract
When plant species invade new areas, they can escape from specialist enemies and thereby reduce investment in chemical defense. Enemy release may have other impacts on plant chemistry; in the absence of specialists, plants may be able to increase production of volatiles that enhance attractiveness to pollinators. In the United States (US), the introduced Eurasian wild parsnip, Pastinaca sativa, has long been subject to attack by an introduced coevolved florivore, Depressaria pastinacella, the parsnip webworm. In 2004, webworms were found for the first time attacking parsnips in New Zealand (NZ). Relative to US P. sativa, NZ P. sativa produces lower levels of defenses but higher levels of certain floral volatiles, suggesting that escape from its specialist florivore may have resulted in changes in volatile profiles to increase pollinator attraction.
In this study, we examined the influence of wild parsnip floral volatiles on pollinator attraction and seed production in NZ and the US. While many insect groups were observed on parsnip umbels, the percentage of flowers that set seed could significantly be predicted by the occurrence of large calyptrate flies and small syrphids in both localities. In the US, β-pinene, γ-terpinene, hexyl butyrate, octyl butyrate, germacrene D and an unknown monoterpene were all positively correlated with visitation by large calyptrates and small syrphids. In NZ, trans- ocimene, carene and octyl butyrate were positively correlated with visitation. Remarkably, most compounds positively associated with visitation are produced in significantly higher proportions in NZ flowers, suggesting that NZ flowers, in the absence of specialized florivores, may be chemically better constituted to attract pollinators.
References
Andersson S, Dobson H (2003) Behavioral foraging responses by the butterfly Heliconius melpomene to Lantana camara floral scent. Journal of Chemical Ecology 29: 2303-2318
Ashman TL, Bradburn M, Cole DH, Blaney BH, Raguso RA (2005) The scent of a male: The role of floral volatiles in pollination of a gender dimorphic plant. Ecology 86: 2099-2105
Baldwin IT, Preston C, Euler M, Gorham D (1997) Patterns and consequences of benzyl acetone floral emissions from Nicotiana attenuata plants. Journal of Chemical Ecology 23: 2327-2343
Bell CR (1971) Breeding systems and floral biology of the Umbelliferae or evidence for specialization in unspecialized flowers. In: Heywood V H (ed) The Biology and Chemistry of the Umbelliferae Supplement 1 to Botanical Journal of the Linnean Society 64: 93-108
Berenbaum MR (1981) Patterns of furanocoumarin production and insect herbivory in a population of wild parsnip (Pastinaca sativa L). Oecologia 49: 236-244
Borg-Karlson A, Valterová I, Nilsson LA (1993) Volatile compounds from flowers of six species in the family Apiaceae: Bouquets for different pollinators? Phytochemistry 35: 111-119
Carroll MJ, Berenbaum MR (2002) Behavioral responses of the parsnip webworm to host plant volatiles. Journal of Chemical Ecology 28: 2191-2201
Carroll MJ, Zangerl AR, Berenbaum MR (2000). Brief communication. Heritability estimates for octyl acetate and octyl butyrate in the mature fruit of the wild parsnip. Journal of Heredity 91: 68-71.
Dobson HEM (2006) Relationship between floral fragrance composition and type of pollinator In Pichersky NA, Dudareva E (eds) The Biology of Floral Scents ,CRC Press, Boca Raton, Florida pp 147 – 199
Dotterl S, Jurgens A, Seifert K et al. (2006) Nursery pollination by a moth in Silene latifolia: The role of odours in eliciting antennal and behavioural responses. New Phytologist 169: 707-718
Dotterl S, Jahreiss K, Umma Salma J et al. (2012) Temporal variation of flower scent in Silene otites (Caryophyllaceae): a species with a mixed pollination system. Botanical Journal of the Linnean Society 169: 447-460.
Feeny P (1977) Defensive ecology of the Cruciferae. Annals of the Missouri Botanical Garden 64: 221-234
Galen C, Kaczorowski R, Todd SL, Geib J, Raguso RA (2011) Dosage-dependent impacts of a floral volatile compound on pollinators, larcenists, and the potential for floral evolution. American Naturalist 177: 258-272
Janzen DH (1975) Behavior of Hymenaea courbaril when its predispersal agent is absent. Science 189: 145-147
Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: Incorporating the fundamental difference between specialist and generalist herbivores. Ecology Letters 8: 704-714
Jürgens A, Dötterl S, Meve U (2006) The chemical nature of fetid floral odours in stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae). New Phytologist 172: 452-468
Jürgens A, Dötterl S, Liede-Schumann S et al (2008) Chemical diversity of floral volatiles in Asclepiadoideae-Asclepiadeae (Apocynaceae). Biochemical Systematics and Ecology 36: 842-852
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17: 164-170
Kessler D, Baldwin IT (2011) Back to the past for pollination biology. Current Opinions in Plant Biology 14: 429-434
Kessler D, Gase K, Baldwin IT (2008) Field experiments with transformed plants reveal the sense of floral scents. Science 321: 1200-1202
Kessler D, Diezel C, Clark DG, Colquhoun TA, Baldwin IT (2012) Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends. Ecology Letters doi: 10.1111/ele.12038
Knudsen JT, Stahl B (1994) Floral odors in the Theophrastaceae. Biochemical Systematics and Ecology 22: 259-268
Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Botanical Review 72: 1-120
Knudsen JT, Tollsten L, Ervik F (2001) Flower scent and pollination in selected Neotropical palms. Plant Biology 3: 642-653
Liu H, Stiling P (2006) Testing the enemy release hypothesis: A review and meta-analysis. Biological Invasions 8: 1535-1545
Lohman D, Zangerl AR, Berenbaum MR (1996) Impact of floral herbivory by parsnip webworm (Oecophoridae: Depressaria pastinacella Duponchel) on pollination and fitness of wild parsnip (Apiaceae: Pastinaca sativa L). American Midland Naturalist 136: 407-412
Mao W, Zangerl AR, Berenbaum MR, Schuler MA (2008) Metabolism of myristicin by Depressaria pastinacella CYP6AB3v2 and inhibition by its metabolite. Insect Biochemistry and Molecular Biology 38: 645-651
Maron JL, Vilà M (2001) When do herbivores affect plant invasion? evidence for the natural enemies and biotic resistance hypotheses. Oikos 95: 361-373
R Development Core Team (2008) R: A language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria ISBN 3-900051-07-0, URL http://wwwR-projectorg
Raguso RA (2008) Wake up and smell the roses: The ecology and evolution of floral scent. Annual Review of Ecology and Evolution S 39: 549-569
Shuttleworth A, Johnson SD (2010) The missing stink: Sulphur compounds can mediate a shift between fly and wasp pollination systems. Proceedings of the Royal Society B-Biological Sciences 277: 2811-2819
Theis N (2006) Fragrance of Canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. Journal of Chemical Ecology 32: 917-927
Theis N and Adler LS (2012) Advertising to the enemy: enhanced floral fragrance increases beetle attraction and reduces plant reproduction. Ecology 93:430–435
Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annual Review of Ecology Evolution and Systematics 25: 443-466
Zangerl AR, Berenbaum MR (2009) Effects of florivory on floral volatile emissions and pollination success in the wild parsnip. Arthropod-Plant Interactions 3: 181-191
Zangerl AR, Stanley MC, Berenbaum MR (2008) Selection for chemical trait remixing in an invasive weed after reassociation with a coevolved specialist. Proceedings of the National Academy of Sciences 105: 4547-4552
Zangerl AR, Berenbaum MR (2005) Increase in toxicity of an invasive weed after reassociation with its coevolved herbivore. Proceedings of the National Academy of Sciences 102: 15529-15532
Zangerl AR, Berenbaum MR (1993) Plant chemistry, insect adaptations to plant chemistry, and host plant utilization patterns. Ecology 74: 47-54
Zangerl AR, Berenbaum MR (1990) Furanocoumarin induction in wild parsnip - genetics and populational variation. Ecology 71: 1933-1940
Zangerl AR, Arntz A, Berenbaum MR (1997) Physiological price of an induced chemical defense: Photosynthesis, respiration, biosynthesis, and growth. Oecologia 109: 433-441
Zangerl AR, Berenbaum MR, Nitao JK (1991) Parthenocarpic fruits in wild parsnip - decoy defense against a specialist herbivore. Evolutionary Ecology, 5, 136-145
Zuur AF, Ieno EN, Walker NJ, et al (2009) Mixed Effects Models and Extensions in Ecology with R. Springer, New York, NY, USA
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Copyright (c) 2014 Tania Jogesh, Arthur Zangerl, Margaret Stanley, May Berenbaum

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