Pollination by Sexual Deception in Australian
Terrestrial Orchids

Text and Photographs by Rod Peakall

Dr Rod Peakall
Professor
School of Botany and Zoology
Australian National University
Canberra 0200 ACT Australia
rod.peakall@anu.edu.au

All photographs are copyright to Rod Peakall 2007.

News Flash

This news feature appeared in Nature (22 February 2007)
Plant biology: The flower of seduction

An Introduction to Pollination in Australian Orchids


The Prasophyllum leek orchids are one of the few Australian terrestrial orchid genera
to provide the reward of nectar to their pollinators. Note the orchid pollen mass attached to the face of the pollinator.

The great majority of animal pollinated plants secure the services of their animal pollinators by providing food rewards such as nectar or pollen. However, orchids are exceptional in that perhaps as many as one third of the 30,000 or so species achieve pollination by deception. That is, they lure animal pollinators to the flower by false promises of food, but do not provide any. Most of these species are ‘food deceptive’ falsely advertising the presence of food by bright colors and sweet scents.



Cyanicula gemmata falsely advertises the promise of a food reward by its bright color, but does not provide any to the flower beetles that pollinate it.

In an even more intriguing group of orchids, pollination is achieved by sexual deception. In these cases, male insects are sexually attracted to the flower by a floral scent that imitates the olfactory cue or sex pheromone used by the pollinator species to attract a mate. Pollination occurs when pollinators attempt copulation (or so-called pseudocopulation) with the flower. The pollination syndrome of sexual deception is known from the terrestrial orchid genus Ophrys in Europe and at least 9 genera of ground orchids in Australia. Many of these flowers are inconspicuous dull colored, red, greens and browns with little or no detectable scent to humans, since bright floral colors and sweet floral odours are not needed to advertise the flower. Typically, pollination by sexual deception is highly specific and usually only involves one insect species (Schiest and Peakall 2002). Remarkably, in Australia several different kinds of male wasps as well as the males of one species of ant and a species of saw fly are sexually exploited by orchids.



A male Lissopimpla excelsa wasp with pollen it has just removed during pseudocopulation with the flower of Cryptostylis ovata.

The discovery of pollination by pseudocopulation was made independently on two continents in the early 1900’s. In 1916, Pouyanne reported his observations of pollination by pseudocopulation in a French journal, but his work lay largely unknown until his observations were confirmed and brought to light by Godfrey in 1925. In Australia, Edith Coleman, a prominent naturalist of her time, confirmed in a series of publications from 1927 to 1938 that pollination of Cryptostylis was achieved by male Lissopimpla excelsa (Casta) (formerly L. semipunctata) wasps during pseudocopulation with the flower. Her detailed observations and experimental approach generated considerable excitement and her Australian reports were reproduced in Transactions of the Entomological Society of London (1928), The Journal of Botany (1929) and Proceedings of the Royal Entomological Society of London (1938) (Schiestl, Peakall and Mant 2003, in press).

The study of pollination by sexual deception in Australia lay dormant until the 1970’s when Prof Warren Stoutamire from USA discovered that this pollination strategy was found in many additional Australia ground orchids. More recently the author and his co-workers have been studying various aspects of this truly intriguing pollination system. A list of scientific publications by the author on Australian orchids is provided below. A summary of this more recent work will be provided as this web site evolves.



Comparison of flightless female thynnine wasp, Zapilothynnus trilobatus and the orchid labellum of Drakaea glyptodon. The males of this wasp species are sexually attracted to the orchid first by a scent that probably mimics the female wasp pheromone, then at short range by the visual similarity of the orchid labellum.


The male thynnine wasp pollinator departing the flower of the green spider orchid Caladenia tentaculata after attempting to mate with the flower.

The following series of photographs show the pollination of the orchid Chiloglottis trapeziformis.



The sexually attracted male pollinator Neozeleboria cryptoides on the stem of the orchid Chiloglottis trapeziformis.


The male pollinator Neozeleboria cryptoides on the labellum of the orchid Chiloglottis trapeziformis prior to
attempted mating with the flower (pseudocopulation). During this process pollen removal will take place
.


The male pollinator Neozeleboria cryptoides on the labellum of the orchid Chiloglottis trapeziformis carrying pollen (pollinia) that was removed during attempted copulation (pseudocopulation) with a previous flower. The callus structures on the labellum mimic the flightless female of the wasp pollinator, although the mimicry is less apparent to human eyes than in Drakaea depicted above where there is striking resemblance of the orchid labellum and the flightless female wasp.


The male pollinator Neozeleboria cryptoides with a mass of pollen (pollinia) it has removed from
the orchid Chiloglottis trapeziformis during attempted copulation (pseudocopulation).
A visit to another flower will result in pollination – a service provided to the orchid at no cost to the flower.



A sexually attracted male pollinator Neozeleboria cryptoides with a mass of pollen (pollinia)
leaves the orchid Chiloglottis trapeziformis after depositing pollen from another flower on the stigma.



A sexually attracted male pollinator Neozeleboria cryptoides with a mass of pollen
(pollinia) resting on a closed flower of Chiloglottis trapeziformis that had been
pollinated several days earlier.

 

News Flash – The Chemistry of Sexual Deception in an Orchid-Wasp Pollination System

This story appeared in Science (October 17, 2003)

Schiestl, F.P., Peakall, R., Mant, J.M., Ibarra, F., Schulz, C., Franke, S and Francke, W. (2003) The chemistry of sexual deception in an orchid-wasp pollination system. Science 302, 437-438. Published October 17.



See below for more photographs and info on Sexual Deception in Australian Orchids

The Science paper abstract:
http://www.sciencemag.org/cgi/content/abstract/302/5644/437

Science magazine commentary on this story:
http://www.sciencemag.org/cgi/content/full/302/5644/372

The Why Files
Science behind the news commentary on this story:
Sexual Deception Play a mating game for keeps! http://whyfiles.org/shorties/139sex_deception/index.html

Radio media coverage of this story

The Science Show Radio National
http://www.abc.net.au/rn/science/ss/

This story featured as the lead story on the Science Show for the Saturday Oct 18. See also:
http://www.abc.net.au/rn/science/ss/stories/s967322.htm
You can also listen to this show online which includes an interview with the author. Online shows can be downloaded for up to 4 weeks after the show.

Australian National University Media Release
http://info.anu.edu.au/mac/Media/Media_Releases/_2003/_031017Orchids.asp

More about the top story in brief:

Pollination by sexual deception of male pollinators is known only in orchids from Australia and Europe.

These orchid flowers mimic the odour and appearance of female insects and pollination is achieved during mating attempts by the male.

This pollination is sometimes known as "pseudocopulation" meaning false mating, although attempted mating is not necessary for pollination in all species, hence we use the more general term of "sexual deception".

In Australia at least 100 species (perhaps has many as 300) in at least 9 orchid genera, are involved. Not only are male wasps of several kinds exploited, but also ants and sawflys.

Although some orchids look remarkably like female wasps (see photos below) we have known for a long time that the floral odor (although not detectable to human noses), rather than appearance is most important.

The exciting breakthrough we have described in our Science paper (Schiestl et al. 2003) is that a single compound, identical in the female and the orchid Chiloglottis trapeziformis, is sufficient to attract the male wasps.

This single compound is unique, representing a new class of compounds previously unknown to science.

This is also the first known case in orchids (and probably plants generally) where the orchids have evolved and copied an identical compound to that used by their pollinator as a sex pheromone.



A male Neozeleboria cryptoides that has been attracted to synthetic copy of the female pheromone
that as been dispensed on a bead. A single unique compound identical in the female and the orchid Chiloglottis trapeziformis is
sufficient to attract the male wasps. A proportion of males attracted to the bead even attempt to copulate with the structure.

Further Reading

Popular
Schiestl, F.P. and Peakall R. (2002) Floral odour and insect olfaction. New tricks to unlock secrets of orchid pollination. Orchids. 71, 906-915.

Selected Scientific Publications on Australian Orchids (to February 2007)
Flanagan, N.S., Peakall, R., Clements, M.A., and Otero, J.T. (2007) Molecular genetic diagnosis of the 'taxonomically difficult' Australian endangered orchid, Microtis angusii: An evaluation of the utility of DNA barcoding. Lankesterian a 7, In press.

Peakall, R. (2007) Orchid speciation - confronting the challenges.   Molecular Ecology , In press.   Invited News and Views Commentary

Flanagan, N.S., Peakall, R., Clements, M.A., Otero, J.T. (2007) Identification of the endangered Australian orchid Microtis angusii using allele-specific PCR assay.   Conservation Genetics, In press (DOI 10.1007/s0592-006-9198-6)

Flanagan, N.S., Peakall, R., Clements, M.A., Otero, J.T., (2006) Conservation of taxonomically difficult species: the case of the Australian orchid, Microtis angusii . Conservation Genetics 7, 847-859 (DOI 10.1007/s10592-006-91119-8.)

Flanagan, N.S., Ebert, D., Porter, C., Rossetto, M., and Peakall, R. (2006) Microsatellite markers for evolutionary studies in the sexually deceptive orchid genus Chiloglottis , Molecular Ecology Notes 6, 123-126 (DOI 10.1111/j.1471-8286.2005.001161.x)

Mant, J., Bower, C.C., Weston, P.H. and Peakall, R. (2005) Phylogeography of pollinator-specific sexually deceptive Chiloglottis taxa (Orchidaceae): evidence for sympatric divergence? Molecular Ecology 14, 3067-3076

Schiestl, F.P., and Peakall, R. (2005) Identical sex pheromones but differing behavioral responses in pollinators of two sexually deceptive orchids.   Functional Ecology, 19, 674-680.

Mant, J., Peakall, R., and Weston, P.H. (2005) Specific pollinator attraction and the diversification of sexually deceptive Chiloglottis (Orchidaceae). Plant Systematics and Evolution , 253, 185-200

Mant, J., Peakall, R., and Schiestl, F.P. (2005) Does selection on floral odor promote differentiation among populations and species of the sexually deceptive orchids, Ophrys.   Evolution 59, 1449-1463.

Peakall, R., and Schiestl, F.P. (2004) A mark-recapture study of male Colletes cunicularius bees: implications for pollination by sexual deception.   Behavioral Ecology and Sociobiology 56, 579-584.

Schiestl, F.P., Peakall, R. and Mant, J. (2004) Chemical communication in the sexually deceptive orchid genus Cryptostylis .   Botanical Journal of the Linnean Society 144, 199-205.

Schiestl, F.P., Peakall, R., Mant, J.M., Ibarra, F., Schulz, C., Franke, S and Francke, W. (2003) The chemistry of sexual deception in an orchid-wasp pollination system. Science 302, 437-438. Published October 17.

Schiestl, F.P., Peakall, R. and Mant, J. (2003) Chemical communication in the sexually deceptive orchid genus Cryptostylis. Botanical Journal of the Linnean Society (in press). Accepted Aug 28, 2003.

Mant, J.G., Schiestl, F.P., Peakall, R., and Weston, P.H. (2002) A phylogenetic study of pollinator conservatism among sexually deceptive orchids. Evolution 56, 888-898.

Peakall, R., Jones, L., Bower, C. C. and Mackey, B. G. (2002) Bioclimatic assessment of the geographic and climatic limits to hybridisation in a sexually deceptive orchid system. Australian Journal of Botany 50, 21-30.

Peakall, R., Bower, C. C., Logan, A. E., and Nicol H. I. (1997) Confirmation of the hybrid origin of Chiloglottis X pescottiana R. S. Rogers (Orchidaceae: Diurideae). 1. Genetic and morphometric analysis. Australian Journal of Botany 45, 839-855.

Peakall, R., and Beattie, A. J. (1996). Ecological and genetic consequences of pollination by sexual deception in the orchid Caladenia tentaculata. Evolution 50, 2207-2220.

Peakall, R. (1990) Responses of male Zaspilothynnus trilobatus wasps to females and the sexually deceptive orchid it pollinates. Functional Ecology 4, 159-167.

Peakall, R., Angus, C. J. and Beattie, A. J. (1990) The significance of ant and plant traits for ant pollination in Leporella fimbriata. Oecologia 84, 457-460.

Peakall, R. (1989a) The unique pollination of Leporella fimbriata (Orchidaceae) by pseudocopulating winged male ants Myrmecia urens (Formicidae). Plant Systematics and Evolution 167, 137-148.

Peakall, R., Beattie, A. J., and James, S. H. (1987) Pseudocopulation of an orchid by male ants: A test of two hypotheses accounting for the rarity of ant pollination. Oecologia 73, 522-524.

Full Publications List