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Science 5 October 2007:
Vol. 318. no. 5847, p. 70
DOI: 10.1126/science.1145147
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Brevia

Odor-Mediated Push-Pull Pollination in Cycads

Irene Terry,1* Gimme H. Walter,2 Chris Moore,2 Robert Roemer,3 Craig Hull2

The reproductive organs of some plants self-heat, release scent, and attract pollinators. The relations among these processes are not well understood, especially in the more ancient, nonflowering gymnosperm lineages. We describe the influence of plant volatiles in an obligate pollination mutualism between an Australian Macrozamia cycad (a gymnosperm with male and female individuals) and its specialist thrips pollinator, Cycadothrips chadwicki. Pollen-laden thrips leave male cycad cones en masse during the daily thermogenic phase, when cone temperatures and volatile emissions increase dramatically and thrips are repelled. As thermogenesis declines, total volatile emissions diminish and cones attract thrips, resulting in pollination of female cones. Behavioral and electrophysiological tests on thrips reveal that variations in b-myrcene and ocimene emissions by male and female cones are sufficient to explain the observed sequential thrips' repellence (push) and attraction (pull). These dynamic interactions represent complex adaptations that enhance the likelihood of pollination and may reflect an intermediate state in the evolution of biotic pollination.

1 Department of Biology, University of Utah, Salt Lake City, UT 84112, USA.
2 The School of Integrative Biology, University of Queensland, Brisbane, QLD 4072, Australia.
3 Department of Mechanical Engineering, University of Utah, Salt Lake City, UT 84112, USA.

* To whom correspondence should be addressed. E-mail: terry{at}biology.utah.edu

Cycads are dioecious gymnosperms, with male and female individuals, of Permian origin. Cycads share obligate mutualisms with specialist insect pollinators, almost universally beetles (1). The known exception involves thrips of the genus Cycadothrips (1, 2), which participate in obligate pollination mutualisms with endemic Australian Macrozamia cycads. Cycadothrips are in a basal thysanopteran family, proposed as arising by at least the Cretaceous (3). Thrips are primarily found on male cones, which provide food (pollen) for adults and larvae (2, 4). During pollination, male and female Macrozamia lucida cones self-heat daily, up to 12°C above ambient temperatures between the hours of ~1100 and 1500, when nearly a millionfold increase in male volatile emissions occurs [females reach ~one-fifth that amount (4)]. In concert, adult Cycadothrips chadwicki leave male and female cones en masse (movie S1) (4), and larvae move to the exterior of their male cone habitat. Pollination is mediated by pollen-laden thrips that enter female cones.

We tested thrips' electrophysiological and behavioral responses to cone volatiles. A two-way choice between male sporophyll volatiles or air in a Y-tube olfactometer (5) demonstrated that thrips are attracted (or neutral) to sporophylls early in the day, repelled at midday, and attracted at later times (Fig. 1A). These phases parallel field results; cones retain (morning, low volatile emissions), repel (midday high emissions), and later attract (low emissions) thrips (4).


Figure 1 Fig. 1. Cycadothrips responses to M. lucida volatiles. (A) The % of insects going to sporophylls of four mid-pollination-stage male cones (M1 to M4) versus controls (Y-tube tests). Lines are quadratic fits to data from separate cones; fit parameters are not statistically different (5). (B and C) Male thrips physiologically respond [gas chromatography electroantennographic (EAG) detection, GCEAD] (B) to ß-myrcene (peak 1) from male cone volatiles and (C) to (E)-ß-ocimene (peak 3) and allo-ocimene (peak 4) but not to (Z)-ß-ocimene (peak 2) from ocimene standard. (D) The % of insects attracted to different concentrations of ß-myrcene standard versus controls (Y-tube tests). [View Larger Version of this Image (31K GIF file)]
 

Electrophysiological tests (5) with volatiles from cones and their specific chemical components revealed that Cycadothrips respond to three components (Fig. 1, B and C): ß-myrcene (>90% of total emissions during thermogenesis) and (E)-ß-ocimene (2%), which change postthermogenesis (4, 5), and allo-ocimene (~2%) (5). Y-tube tests at ecological concentrations of these chemicals (5) showed that ocimenes attract thrips (fig. S1), whereas ß-myrcene attracts thrips at low concentrations but repels them at higher levels (Fig. 1D). When control and high-concentration ß-myrcene vessels (5) were switched after thrips had entered the control arm, 77% moved directly into the new control arm. Most that remained died within 10 min, suggesting that by leaving cones thrips avoid toxic ß-myrcene levels.

These cone volatile changes sufficiently explain the diel thrips behavior observed in situ (4), although temperature and light may modulate their effects. We characterize this as a "push-pull" pollination strategy. Flowers are generally portrayed as only "pulling" pollinators via visual or odor cues. Some orchids, though, chemically repel pollinators after pollination (6). Driving thrips from male cones increases pollen-laden thrips attendance at female cones, which presumably attract by deceit because their volatile components match those of males (4). Parallel attraction to male cones allows thrips to accrue pollen for the next day's cycle. This obligate pollination mutualism stands out for its pushpull behavior and because it involves an ancient gymnosperm lineage and a basal thrips clade (2). Floral scent may have originally evolved to deter herbivores (7), and this system may represent a conserved early intermediary in the evolution of seed plant pollination.


References

  • 1. W. Tang, in Vistas in Palaeobotany and Plant Morphology, P. Srivastava, Ed. (UP Offset, Lucknow, India, 2004), pp. 383–394.
  • 2. I. Terry et al., Am. J. Bot. 92, 931 (2005).[Abstract/Free Full Text]
  • 3. D. Grimaldi, A. Shmakov, N. Fraser, J. Paleontol. 78, 941 (2004).[Abstract/Free Full Text]
  • 4. I. Terry et al., Plant Syst. Evol. 243, 233 (2004). [CrossRef]
  • 5. Materials and methods are available at Science Online.
  • 6. F. Schiestl, M. Ayasse, Oecologia 126, 531 (2001). [CrossRef] [Web of Science]
  • 7. O. Pellmyr, L. Thien, Taxon 35, 76 (1986). [CrossRef] [Web of Science]
  • 8. Studies partially supported by National Geographic Society. Thanks to R. Raguso, A. Najar, F. Adler, and anonymous reviewers.

Supporting Online Material

www.science.org/cgi/content/full/318/5847/70/DC1

Materials and Methods

Fig. S1

Movie S1

Received for publication 15 May 2007. Accepted for publication 27 August 2007.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Infrared radiation from hot cones on cool conifers attracts seed-feeding insects.
S. Takacs, H. Bottomley, I. Andreller, T. Zaradnik, J. Schwarz, R. Bennett, W. Strong, and G. Gries (2009)
Proc R Soc B 276, 649-655
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Pollination biology of basal angiosperms (ANITA grade).
L. B. Thien, P. Bernhardt, M. S. Devall, Z.-d. Chen, Y.-b. Luo, J.-H. Fan, L.-C. Yuan, and J. H. Williams (2009)
Am. J. Botany 96, 166-182
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Science. ISSN 0036-8075 (print), 1095-9203 (online)