Abstract
The long-term persistence of obligate mutualisms (over 40 Mya in both fig/fig wasps and yucca/yucca moths) raises the question of how one species limits exploitation by the other species, even though there is selection pressure on individuals to maximize fitness. In the case of yuccas, moths serve as the plant's only pollinator, but eggs laid by the moths before pollination hatch into larvae that consume seeds. Previous studies have shown that flowers with high egg loads are more likely to abscise. This suggests that yucca flowers can select against moths that lay many eggs per flower through selective abscission of flowers; however, it is not known how yucca moths trigger floral abscission. We tested how the moth Tegeticula yuccasella triggers floral abscission during oviposition in Yucca filamentosa by examining the effects of ovipositor insertion and egg laying on ovule viability and floral abscission. Eggs are not laid at the site of ovipositor insertion: we used this separation to test whether wounded ovules were more closely associated with the ovipositor site or an egg's location. Using a tetrazolium stain to detect injured ovules, we determined whether the number of ovipositions affected the number of wounded ovules in naturally pollinated flowers. Two wounding experiments were used to test the effect of mechanical damage on the probability of floral abscission. The types of wounds in these experiments mimicked two types of oviposition—superficial oviposition in the ovary wall and oviposition into the locular cavity—that have been observed in species of Tegeticula. The effect of moth eggs on ovule viability was experimentally tested by culturing ovules in vitro, placing moth eggs on the ovules, and measuring changes in ovule viability with a tetrazolium stain. We found that ovules were physically wounded during natural oviposition. Ovules showed a visible wounding response in moth-pollinated flowers collected 7–12 h after oviposition. Exact location of wounded ovules relative to eggs and oviposition scars, as well as results from the artificial wounding experiments, showed that the moth ovipositor inflicts mechanical damage on the ovules. Significantly higher abscission rates were observed in artificially wounded flowers in which only 4–8% of the ovules were injured. Eggs did not affect ovule viability as measured by the tetrazolium stain. These results suggest that physical damage to ovules caused by ovipositing is sufficient to explain selective fruit abscission. Whether injury as a mechanism of selective abscission in yuccas is novel or a preadaptation will require further study.
Similar content being viewed by others
References
Addicott FT (1982) Abscission. University of California Press, Berkeley
Addicott JF (1986) Variation in the costs and benefits of mutualism: the interaction between yuccas and yucca moths. Oecologia 70:486–494
Addicott JF (1998) Regulation of mutualism between yuccas and yucca moths: population level processes. Oikos 81:119–129
Addicott JF, Bao T (1999) Limiting the costs of mutualism: multiple modes of interaction between yuccas and yucca moths. Proc R Soc Lond Ser B 266:197–202
Aker CL (1982) Regulation of flower, fruit and seed production by a monocarpic perennial, Yucca whipplei. J Ecol 70:357–372
Anderson AN (1989) Impact of insect predation on ovule survivorship in Eucalyptus baxteri. J Ecol 77:62–69
Binh LT, Muoi LT, Oanh HTK, Thang TD, Phong DT (1990) Rapid propagation of Agave by in vitro tissue culture. Plant Cell Tissue Organ Cult 23:67–70
Brody AK, Morita SI (2000) A positive association between oviposition and fruit set: female choice or manipulation? Oecologia 124:418–425
Bull JJ, Rice WR (1991) Distinguishing mechanisms for the evolution of cooperation. J Theor Biol 149:63–74
Chapman RF (1998) The insects: structure and function, 4th edn. Cambridge University Press, Cambridge
Connor RC (1995) The benefits of mutualism: a conceptual framework. Biol Rev 70:427–457
Cunningham SA (1997) Predator control of seed production by a rain forest understory palm. Oikos 79:282–290
Davies E (1987) Action potentials as multifunctional signals in plants: a unifying hypothesis to explain apparently disparate wound responses. Plant Cell Environ 10:623–631
Doorn WG van, Stead AD (1997) Abscission of flowers and floral parts. J Exp Bot 48:821–837
Fuller OS (1990) Factors affecting the balance of cooperation and conflict between the yucca moth, Tegeticula yuccasella, and its mutualist, Yucca glauca. Ph.D. dissertation, University of New Mexico, Albuquerque
Gleason HA, Cronquist A (1991) Manual of vascular plants of northeastern United States and adjacent Canada, 2nd edn. New York Botanical Garden, Bronx
Herre EA (1999) Laws governing species interactions? Encouragement and caution from figs and their associates. In: Keller L (ed) Levels of selection in evolution. Princeton University Press, Princeton, NJ, pp 209–237
Hori K (1992) Insect secretions and their effect on plant growth, with special reference to Hemipterans. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, Oxford, pp 157–170
Hori K, Torikura H, Kumagai M (1987) Histological and biochemical changes in the tissue of pumpkin fruit injured by Lygus disponsi Linnavuori (Hemiptera: Miridae). Appl Entomol Zool 232:259–265
Humphries SA, Addicott JF (2000) Regulation of the mutualism between yuccas and yucca moths: intrinsic and extrinsic factors affecting flower retention. Oikos 89:329–339
Huth CJ, Pellmyr O (1997) Non-random fruit retention in Yucca filamentosa: consequences for an obligate mutualism. Oikos 78:576–584
Huth CJ, Pellmyr O (1999) Yucca moth oviposition and pollination behavior is affected by past flower visitors: evidence for a host-marking pheromone. Oecologia 119:593–599
Huth CJ, Pellmyr O (2000) Pollen-mediated selective abortion in yuccas and its consequences for the plant-pollinator mutualism. Ecology 81:1100–1107
Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 2:465–492
Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Niwot
Keck CB (1934) Relation of oviposition punctures of the Mediterranean fruit fly to the premature dropping of citrus fruits. J Econ Entomol 28:908–914
King EE (1973) Endo-polymethylgalacturonase of boll weevil larvae, Anthonomus grandis: an initiator of cotton flower bud abscission. J Insect Physiol 19:2433–2437
King EE, Lane HC (1969) Abscission of cotton flower buds and petioles caused by protein from boll weevil larvae. Plant Physiol 44:903–906
Kingsolver RW (1984) Population biology of a mutualistic association: Yucca glauca and Tegeticula yuccasella. Ph.D. dissertation, University of Kansas, Lawrence
Levine E, Hall FR (1978) Pectinases and cellulases from plum curculio larvae: possible causes of apple and plum fruit abscission. Entomol Exp App 23:259–268
Meyer AJ, Weisenseel MH (1997) Wound-induced changes of membrane voltage, endogenous currents, and ion fluxes in primary roots of maize. Plant Physiol 114:989–998
Moore RP (1972) Effects of mechanical injuries on viability. In: Roberts EH (ed) Viability of seeds. Syracuse University Press, Chapman and Hall, UK pp 94–113
Murashige T (1974) Plant propagation through tissue cultures. Annu Rev Plant Physiol 25:135–66
Pellmyr O (1997) Pollinating seed eaters: why is active pollination so rare? Ecology 78:1655–1660
Pellmyr O (1999) Systematic revision of the yucca moths in the Tegeticula yuccasella complex (Lepidoptera: Prodoxidae) north of Mexico. Syst Entomol 24:1–28
Pellmyr O, Huth CJ (1994) Evolutionary stability of mutualism between yuccas and yucca moths. Nature 372:257–260
Pellmyr O, Leebens-Mack J (2000) Reversal of mutualism as a mechanism for adaptive radiation in yucca moths. Am Nat 156:S62–S76
Richter KS, Weis AE (1995) Differential abortion in the yucca. Nature 376:557–558
Riley CV (1873) On the oviposition of the yucca moth. Am Nat 7: 619–623
Riley CV (1892) Some interrelations of plants and insects. Proc Biol Soc Wash 7:81–104
Roberts LW (1951) Survey of factors responsible for reduction of 2,3,5-triphenyltetrazolium chloride in plant meristems. Science 113:692–693
Rodrigo J, Herrero M (1998) Influence of intraovular reserves on ovule fate in apricot (Prunus armeniaca L.). Sex Plant Reprod 11:86–93
Salisbury FB, Ross CW (1996) Plant physiology, 4th edn. Wadsworth, Belmont
Sallabanks R, Courtney SP (1992) Frugivory, seed predation, and insect-vertebrate interactions. Ann Rev Entomol 37:377–400
SPSS (1999) SPSS 10.0 syntax reference guide. SPSS Inc., Chicago
Stephenson AG (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annu Rev Ecol Syst 12:253–279
Sutherland S, Delph LF (1984) On the importance of male fitness in plants: patterns of fruit-set. Ecology 65:1093–1104
Trelease W (1902) The Yucceae. Mo Bot Garden 13th Annu Rep pp 27–133
Udovic D (1981) Determinants of fruit set in Yucca whipplei: reproductive expenditure vs. pollinator availability. Oecologia 48:389–399
Wilson RD, Addicott JF (1998) Regulation of mutualism between yuccas and yucca moths: is oviposition behavior responsive to selective abscission of flowers? Oikos 81:109–118
Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, Upper Saddle River
Acknowledgements
We thank Lindsey Elms for help with the artificial wounding experiments, Chad Huth for his advice in the early stages of this project, Holly Bonar and Michael Lacey for help with seed counting, and Kari Segraves and two anonymous reviewers for comments on an earlier version of this manuscript. This work was supported by NSF (DEB 95-09056) and a Natural Science Grant from Vanderbilt University to O. Pellmyr.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Marr, D.L., Pellmyr, O. Effect of pollinator-inflicted ovule damage on floral abscission in the yucca-yucca moth mutualism: the role of mechanical and chemical factors. Oecologia 136, 236–243 (2003). https://doi.org/10.1007/s00442-003-1279-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-003-1279-3