Subscribe to RSS
DOI: 10.1055/s-2004-821236
Georg Thieme Verlag Stuttgart KG · New York
Herbivory Differentially Affects Male and Female Reproductive Traits of Cucumis sativus
Publication History
Publication Date:
17 September 2004 (online)
Abstract
Herbivory is an important selection pressure in the life history of plants. Most studies use seed or fruit production as an indication of plant fitness, but the impact of herbivory on male reproductive success is usually ignored. It is possible that plants compensate for resources lost to herbivory by shifting the allocation from seed production to pollen production and export, or vice versa. This study examined the impact of herbivory by Helix aspersa on both male and female reproductive traits of a monoecious plant, Cucumis sativus. The effects of herbivory on the relative allocation to male and female flowers were assessed through measurements of the number and size of flowers of both sexes, and the amount of pollinator visitation. We performed two glasshouse experiments; the first looked at the impact of three levels of pre-flowering herbivory, and the second looked at four levels of herbivory after the plants had started to flower. We found that herbivory during the flowering phase led to a significant increase in the number of plants without male flowers. As a consequence there was significantly less pollen export from this population, as estimated by movement of a pollen analog. The size of female flowers was reduced by severe herbivory, but there was no affect on pollen receipt by the female flowers of damaged plants. The decrease in allocation to male function after severe herbivory may be adaptive when male reproductive success is very unpredictable.
Key words
Pollination - plant-animal interactions - floral characteristics - reproductive allocation.
References
- 1 Agrawal A. A., Gorski P. M., Tallamy D. W.. Polymorphism in plant defence against herbivory: Constitutive and induced resistance in Cucumis sativus. . Journal of Chemical Ecology. (1999); 25 2285-2304
- 2 Allison T. D.. The influence of deer browsing on the reproductive biology of Canada yew (Taxus canadensis Marsh). 1. Direct effect on pollen, ovule and seed production. Oecologia. (1990); 83 523-529
- 3 Alward R. D., Joern A.. Plasticity and overcompensation in grass responses to herbivory. Oecologia. (1993); 95 358-364
- 4 Ashman T. L.. Pollinator selectivity and its implications for the evolution of dioecy and sexual dimorphism. Ecology. (2000); 81 2577-2591
- 5 Ashman T. L.. The role of herbivores in the evolution of separate sexes from hermaphroditism. Ecology. (2002); 83 1175-1184
- 6 Atsmon D., Galun E.. A morphogenetic study of staminate, pistillate and hermaphrodite flowers in Cucumis sativus. . Phytomorphology. (1960); 10 110-115
- 7 Bateman A. J.. Intra-sexual selection in Drosophila. . Heredity. (1948); 2 349-368
- 8 Bertin R. I.. Paternity and fruit production in trumpet creeper (Campsis radicans). . American Naturalist. (1982); 119 694-709
-
9 Bleakney M. M., Fleming C. C., Marks R. J..
Genetic and phenotypic variation in allopatric populations of Helix aspersa (Muller): A preliminary report. Henerson, I., ed. Slugs and Snails in World Agriculture. Guildford; The British Crop Protection Council (1989): 319-326 - 10 Burd M.. Bateman's principle and plant reproduction; the role of pollen limitation in fruit and seed set. Botanical Review. (1994); 60 83-139
- 11 Campbell D. R.. Experimental tests of sex-allocation theory in plants. Trends in Ecology and Evolution. (2000); 15 227-232
- 12 Campbell D. R., Halama K. J.. Resource and pollen limitations to lifetime seed production in a natural plant population. Ecology. (1993); 74 1043-1051
- 13 Campbell D. R., Waser N. M., Price M. V.. Mechanisms of hummingbird-mediated selection for flower width in Ipomopsis aggregata. . Ecology. (1996); 77 1463-1472
- 14 Connor J. K., Davis R., Rush S.. The effect of wild radish floral morphology on pollination efficiency by four taxa of pollinators. Oecologia. (1995); 104 234-245
- 15 Connor J. K., Rush S.. Effects of flower size and number on pollinator visitation to wild radish, Raphanus raphanistrum. . Oecologia. (1996); 105 509-516
- 16 Cunningham S. A.. Pollen supply limits fruit initiation by a rain forest understorey palm. Journal of Ecology. (1996); 84 185-194
- 17 Delph L. F., Johannsson M. H., Stephenson A. G.. How environmental factors affect pollen performance: ecological and evolutionary perspectives. Ecology. (1997); 78 1632-1639
- 18 Devlin B., Ellstrand N. C.. Male and female fertility variation in wild radish, a hermaphrodite. American Naturalist. (1990); 136 87-107
- 19 Dollin A. E., Dollin L. J., Sakagami S. F.. Australian stingless bees of the genus Trigona (Hymenoptera: Apidae). Invertebrate Taxonomy. (1997); 11 861-896
- 20 Frazee J. E., Marquis R. J.. Environmental contribution to floral trait variation in Chamaecrista fasciculata (Fabaceae, Caesalpinoideae). American Journal of Botany. (1994); 81 206-215
- 21 Godan D.. Pest Slugs and Snails. Berlin; Springer-Verlag (1983)
- 22 Gronemeyer P. A., Dilger B. J., Bouzat J. L., Paige K. N.. The effects of herbivory on paternal fitness in scarlet gilia - better moms also make better pops. American Naturalist. (1997); 150 592-602
- 23 Haig D., Westoby M.. On limits to seed production. American Naturalist. (1988); 131 757-759
- 24 Heard T. A.. Propagation of hives of Trigona carbonaria Smith (Hymenoptera: Apidae). Journal of the Australian Entomological Society. (1988); 27 303-304
- 25 Heard T. A.. Behaviour and pollinator efficiency of stingless bees on macadamia flowers. Journal of Apicultural Research. (1994); 33 191-198
- 26 Heard T. A.. The role of stingless bees in crop pollination. Annual Review of Entomology. (1999); 44 183-206
- 27 Hendrix S. D., Trapp E. J.. Plant-herbivore interactions: insect induced changes in host plant sex expression and fecundity. Oecologia. (1981); 49 119-122
- 28 Horovitz A.. Is the hermaphrodite flowering plant equisexual?. American Journal of Botany. (1978); 65 485-486
- 29 Johnson S. G., Delph L. F., Elderkin C. L.. The effect of petal size manipulation on pollen removal, seed set and insect visitor behaviour in Campanula americana. . Oecologia. (1995); 102 174-179
- 30 Juenger T., Bergelson J.. Pollen and resource limitation of compensation to herbivory in scarlet gilia, Ipomopsis aggregata. . Ecology. (1997); 78 1684-1695
- 31 Karban R., Strauss S. Y.. Effects of herbivores on growth and reproduction of their perennial host, Erigeron glaucus. . Ecology. (1993); 74 39-46
- 32 Lawrence W.. Resource and pollen limitation: plant size-dependent reproductive patterns in Physalis longifolia. . American Naturalist. (1993); 141 293-313
- 33 Lehtila K., Strauss S. Y.. Effects of foliar herbivory on male and female reproductive traits of wild radish, Raphanus raphanistrum. . Ecology. (1999); 80 116-124
- 34 Lehtila K., Syränen K.. Compensatory responses of two Melampyrum species after damage. Functional Ecology. (1995); 9 511-517
- 35 Lennartson T., Nilsson P., Tuomi J.. Induction of overcompensation in the field Gentian, Gentianella capestris. . Ecology. (1998); 79 1061-1072
- 36 Maschinski J., Whitham T. G.. The continuum of plant responses to herbivory: the influence of plant association, nutrient availability and timing. American Naturalist. (1989); 134 1-19
- 37 McCall C., Primack R. B.. Effects of pollen and nitrogen availability on reproduction in a woodland herb Lysimachia quadrifida. . Oecologia. (1985); 76 403-410
- 38 Mothershead K., Marquis R. J.. Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. . Ecology. (2000); 81 30-40
- 39 Mutikainen P., Delph L. F.. Effects of herbivory on male reproductive success in plants. Oikos. (1996); 75 353-358
- 40 Perl-Treves R., Kahana A., Rosenman N., Xiang Y., Silberstein L.. Expression of multiple AGAMOUS-like genes in male and female flowers of cucumber (Cucumis sativus). . Plant Cell Physiology. (1998); 39 701-710
- 41 Pilson D.. Herbivory and natural selection on flowering phenology in wild sunflower, Helianthus annuus. . Oecologia. (2000); 122 72-82
- 42 Quesada M., Bollman K., Stephenson A. G.. Leaf damage decreases pollen production and hinders pollen performance in Cucurbita texana. . Ecology. (1995); 76 437-443
- 43 Rodríguez-Roubles J. A., Meléndez E. J., Ackerman J. D.. Effects of display size, flowering phenology, and nectar availability on effective visitation frequency in Comparettia falcata (Orchidaceae). American Journal of Botany. (1992); 79 1009-1017
- 44 Scarré J. E., Lepart J., Sentuc J. J.. Effects of simulated herbivory in three old field Compsitae with different inflorescence architectures. Oecologia. (1996); 105 501-508
- 45 Schlichting C. D., Delesalle V. A.. Stressing the differences between male and female functions in hermaphroditic plants. Trends in Ecology and Evolution. (1997); 12 51-52
- 46 Schlichting C. D., Devlin B.. Male and female reproductive success in the hermaphroditic plant Phlox drummondii. . American Naturalist. (1989); 133 212-227
- 47 Snyder M. A.. Interactions between Albert's squirrel and Ponderosa pine: the relationship between selective herbivory and plant fitness. American Naturalist. (1993); 141 866-879
- 48 Strauss S. Y.. Direct, indirect and cumulative effects of three native herbivores on a shared host plant. Ecology. (1991); 72 543-558
- 49 Strauss S. Y., Armbruster W. S.. Linking herbivory and pollination - new perspectives on plant and animal ecology and evolution. Ecology. (1997); 78 1617-1618
- 50 Strauss S. Y., Conner J. K., Lehtila K. P.. Effects of foliar herbivory by insects on the fitness of Raphanus raphanistrum: damage can increase male fitness. American Naturalist. (2001); 158 496-504
- 51 Strauss S. Y., Conner J. K., Rush S. L.. Foliar herbivory affects floral characters and plant attractiveness to pollinators - implications for male and female plant fitness. American Naturalist. (1996); 147 1098-1107
- 52 Thomson J. D., Price M. V., Waser N. M., Stratton D. A.. Comparative studies of pollen and fluorescent dye transport by bumble bees visiting Erythronium grandiflorum. . Oecologia. (1986); 69 561-566
- 53 Thomson V. P., Cunningham S. A., Ball M. C., Nicotra A. B.. Compensation for herbivory by Cucumis sativus through increased photosynthetic capacity and efficiency. Oecologia. (2003); 134 167-175
- 54 Trivers R. L., Willard D. E.. Natural selection of parental ability to vary the sex-ratio of offspring. Science. (1973); 179 90-92
- 55 Vallius E., Salonen V.. Effects of defoliation on male and female reproductive tratis of a perennial orchid, Dactylorhiza maculata. . Functional Ecology. (2000); 14 668-674
- 56 Waser N. M., Price M. V.. A comparison of pollen and fluorescent dye carryover by natural pollinators of Ipomopsis aggregata (Polemoniaceae). Ecology. (1982); 63 1168-1172
- 57 Wilson P., Thomson J. D., Stanton M. L., Rigney L. P.. Beyond floral batemania: gender biases in selection for pollination success. American Naturalist. (1994); 143 283-296
- 58 Wise M. J., Sacchi C. F.. Impact of two specialist insect herbivores on reproduction of horse nettle, Solanum carolinense. . Oecologia. (1996); 108 328-337
- 59 Yin T., Quinn J. A.. Tests of a mechanistic model of one hormone regulating both sexes in Cucumis sativus (Cucurbitaceae). American Journal of Botany. (1995); 82 1537-1546
- 60 Young H. J., Stanton M. L.. Influences of floral variation on pollen removal and seed production in wild radish. Ecology. (1990); 71 536-547
V. P. Thomson
School of Botany and Zoology
Australian National University
Canberra, ACT, 0200
Australia
Email: vpthomson@hotmail.com
Section Editor: C. M. J. Pieterse