Chemical Mimicry in Pollination

Elisa J. Bernklau
Entomology Dept.
Colorado State University
Fort Collins, CO 80523
The use of chemical signals may be the dominant form of communication in the insect world.а Many insects have evolved highly complex and specific chemical signals with 
which to communicate within their own species.а It is not surprising that other 
organisms have evolved the ability to exploit these communication systems in order 
to fulfill their own needs.а One method of exploitation involves mimicking the 
chemical signals used by insects.а In a system of chemical mimicry, a single 
compound or a mixture of compounds is produced by an organism to elicit a specific 
behavioral response by an organism of a different species.а 
Chemical mimicry, which is used by vertebrates, invertebrates, plants and fungi, can 
be divided into unique categories based on the outcome of the relationship.а These 
different classes include aggressive mimicry, reproductive mimicry, dispersal 
mimicry, group mimicry, and predator mimicry (Wiens 1978).а One of the most 
intriguing systems is the use of chemical mimicry by plants in order to attract 
insect pollinators.а 
Most pollination systems have evolved as mutualistic relationships in which both 
organisms are rewarded:а the insect obtaining pollen, nectar, waxes or scents from 
the flower and the plant achieving reproduction through the transfer of its pollen 
by the insect.а Chemical mimicry has evolved in insect/flower systems where no 
reward is received by the insect.а The plant, which is the sole benefactor, lures 
the insect to its flower by producing specific scents.а These odors may mimic insect 
pheromones, food sources, broodsites or prey odors.
Pollination mimicry has been studied in some detail and the literature contains 
several excellent reviews of the subject.а A 1978 review entitled Mimicry in Plantsа 
(Wiens 1978) includes a section on pollination mimicry in which Wiens briefly 
describes some different categories of chemical mimicry and gives a few examples of 
each.а A chapter entitled 'Chemical Mimicry' (Stowe 1988), in the book Chemical 
Mediation of Coevolution, contains a review of all known chemical mimicry systems.а 
In the section on pollination mimicry, Stowe cites numerous examples of pheromone 
and brood-site mimicry.а He summarizes the similarities in compounds (identified to 
date) produced by flowers and their insect pollinators and provides some possible 
explanations for differences that have been found between insect and plant-produced 
compounds.а He also suggests possible evolutionary patterns for various classes of 
chemical mimicry.а In a 1990 article, Borg-Karlson (1990) provides a comprehensive 
review of the relationships between orchids of the genus Ophrys and their insect 
pollinators.а In this review, Borg-Karlson describes the detailed chemical analyses 
and field studies conducted by herself and her associates.а She also discusses 
previous field work and chemical identifications carried out by other experts in the 
field (Bergstrom, Paulus, Kullenberg).а A 1994 review by Dettner (1994) provides 
examples of particular compounds that are produced by plants in different 
pollination systems and the specific insects that are effected by them.
Plant Mimicry of Insect Pheromones
Some form of mimicry is used by approximately 50% of orchid species to attract 
insects of specific taxa for pollination.а Visual mimicry of female insects by the 
flowers was believed to be the main factor in these relationships until 1961 when 
Kullenberg first suggested that chemical mimicry may also play a role (Kullenberg 
1961).а Researchers have since demonstrated this to be the case and the chemistry of 
many pollination mimicry systems is now known.а According to Borg-Karlson (1990), 
the most important studies on the Ophrys orchid/insect pollination systems are those 
compiled by Kullenberg (1973), Kullenberg et al. (1984), Warncke and Kullenberg 
(1984) and Paulus and Gack (1986).
In these systems, male insects are attracted by odors produced by the flowers 
(specifically by the labellum).а These odors excite the insects sexually and cause 
them to approach and investigate the flowers more closely.а In some instances, the 
males will go so far as to attempt to copulate with the flower.а This behavior, 
termed 'pseudocopulation', was first observed by Correvon and Pauyanne (Pouyanne 
1917; Correvon and Pouyanne 1923).а During the insect/flower interaction, pollinaria 
are inadvertently attached to the head or abdomen of the male insect who then 
pollinates the next flower that he visits (Borg-Karlson 1990).
The odors produced by these orchids are blends of several compounds that closely 
resemble different types of insect pheromones.а These include:а odors produced by 
eclosing females, sex attractants produced by virgin females, scents produced by 
mated females, male courtship pheromones, and male scent markers (Stowe 1988).а A 
flower species or variety may produce one specific type of odor or a combination of 
the different pheromones.
Visual and Tactile Cues
In addition to the chemical attractants, many of the orchid species use visual and 
tactile cues to dupe their pollinators.а The combination of visual, tactile and 
olfactory cues may mimic a female insect so well that the male is not able to 
distinguish the difference.а The pheromone odor cues serve to attract patrolling 
insects to the flowers from a distance.а Many of these compounds also stimulate the 
males sexually.а The visual stimuli then serve as close-range attractants that, in 
some cases, cause the sexually-stimulated males to actually alight on the flower.а 
Borg-Karlson (1986) noted that in some cases Andrena bees will not alight on the 
odor source without the proper visual cues.а However, the visual cues are not 
important for all hymenoptera species.а Tactile cues such as the firmness and 
smoothness of the labellum help to guide the male into a position that insures his 
contact with the pollinaria.
Examples of Pheromone Mimicry
All but one example of pheromone mimicry in plants occur in the family Orchidaceae.а 
At least 30 species of one genus (Ophrys) produce compounds in common with their 
insect pollinators.а While most of the insects involved are bees and wasps, a few 
plants depend upon beetles for pollination (Stowe 1988).а 
Because this phenomenon is so widespread in the orchid family, it has been 
extensively studied and many of the specific insect/orchid relationships have been 
defined.а For example, orchids of the genus Ophrys are pollinated by males of the 
hymenoptera families Andrenidae, Anthophoridae, Colletidae, Megachilidae, Sphecidae 
and Scoliidae and by two species of beetle (Elateridae and Scarabaeidae) (Borg-
Karlson 1990).а All Cryptostylis flowers attract Lissopimpla excelsa wasps 
(Ichneumonidae).а Wasps of the subfamily Thynninae are attracted to related orchids 
(Chiloglottis, Drakaea, Caladenia, Arthrochilus, Paracaleana, and Specula) (Stowe 
1988).а Calochilus attracts scoliid wasps, Caleana attracts pergid sawflies,Ophrys 
diurisа and O. galilaea attract male halictid bees (Halictus marginatus) (Borg-
Karlson et al. 1985), and Leporella fimbriata attracts male alate ants (Myrmecia 
sp.) (Stowe 1988).а Guiera senegalensis (Combretaceae), which is the only non-orchid 
plant known to mimic insect sex pheromones (Kullenberg 1961) attracts male sphecid 
wasps (Tachysphex).а A very complete listing of specific orchids and their 
pollinators was compiled by Kullenberg (1973; 1976; 1985).
Chemical Analysis
A review by Borg-Karlson (Borg-Karlson 1990) details the chemical analysis of Orchid 
volatiles and field studies of the insect-Ophrys relationships conducted by herself 
and her associates and by other researchers (Bergstrom, Paulus, Kullenberg).а 
Chemical analyses resulted in the identification of the main compounds produced by 
flowers in the Ophrysа genus as well as by Andrena, Eucera and Colletes bees.а In 
addition, these studies revealed similarities between the insects and their 
associated flowers and helped to determine the specific compounds responsible for 
the attraction in some of these systems.
A combination of techniques was used for extracting flower and insect specimens to 
insure the collection of compounds of both low and high volatility.а These methods 
included making sorption extracts using Porapak Q or Tenax GC, low temperature 
trapping with liquid nitrogen or carbon dioxide in ethanol, and extracting the 
flower and insect parts in hexane or methanol (Borg-Karlson 1990).а GC-MS was used 
to identify particular compounds. 
Bioassays and Field Studies
 After identifying the key components of the volatile blends, the effects of 
collected volatile samples as well as synthetic mixtures of those blends on the 
behavior of the insects were tested.а Field studies were conducted in the natural 
mating areas of the insects using a revised version of a bioassay that was 
originally developedа by Kullenberg (1961).а In the bioassays, they applied the test 
compounds to insect "dummies" which were constructed of black nylon velvet attached 
to an insect pin.а Physiological responses of the insects to key compounds were 
tested in the laboratory using an electroantennagram technique.
Compounds Isolated from Insects and Flowers
Using the techniques described above, Borg-Karlson detected approximately 100 
volatile compounds in the flower extracts (Borg-Karlson et al. 1985).а Of these, 
aliphatics and terpenoids were determined to be the main components.а The aliphatic 
compounds, including saturated hydrocarbons, aldehydes (octanal and nonanal), 1- and 
2-alcohols and esters, were always present in the largest quantities. аTerpenoids 
(geraniol, citronellol and E,E-farnesol) were always present as well, but the 
amounts varied greatly (Borg-Karlson 1990).а 
Compounds isolated from the mandibular glands of Andrena bees include aliphatics (1- 
and 2-alcohols, 2-ketones and esters) and terpenoids (geraniol, citronellol and 
farnesol).а Borg-Karlson separated the Andrena species into four distinct groups 
based upon the mixtures of these volatiles.а Oxygenated open chain mono- and 
sesquiterpenes (geranial and neral) and their alcohol derivatives were found to be 
the main constituents in the first group.а A second group of insects shares a 
mixture of geranial, neral, their alcohols, aliphatic alcohols and aldehydes.а A 
third group was found to produce mainly aliphatic alcohols, esters, and 2-ketones, 
along with smaller amounts of monoterpenes (geranial) and spiroacetals.а The fourth 
group of bees included only one species (Andrena squalida), which produces only a 
series of esters.а 
Compounds isolated from the Dufour's gland of Andrena bees include terpene esters 
and aliphatic esters (Borg-Karlson 1990).а 
Colletes bees contain linalool, geranial and neral in their mandibular gland 
secretions.а Cephalic secretions of the Eucera bees have only a few volatile 
compounds and these included alcohols, terpenoids and linalool (Borg-Karlson 1990).
Similarities Between Floral and Insect Volatiles
Many similarities were found in the chemicals produced by the flowers and by their 
pollinators.а In fact, several Ophrys sp. release compounds identical to those found 
in the mandibular and/or Dufour's glands of their pollinators.а Similarities are 
seen between Ophrys lutea and Ophrys fusciа and several species of Andrena bees, 
Ophrys arachnitiformes-araneiferae and bees of both the Andrena and Colletes genera, 
Ophrys insectifera and two digger wasps (Argogorytes mystaceus and A. fargei ) and 
Ophrys scolopax heldreichiiа and males of the bee species Tetralonia cressaа (Borg-
Karlson 1990).а Volatile compounds common to Andrena bees and Ophrys flowers 
include1-and 2-alcohols, 2-ketones, acetates, esters, geraniol, geranial, 
citronellol, citronellal, linalool, E,E-farnesol and farnesol esters.а Colletes bees 
and their flower hosts both produce geranial neral and linalool.а Eucera bees share 
geranial and linalool, benzaldehyde, 4-methyl phenol, 1,4-benzoquinone, methyl 
esters, ethyl esters and acetates with their flowers (Borg-Karlson 1990).а 
Behavioral Responses of Pollinators
Some of these compounds were found to be responsible for the attraction of male bees 
and wasps in the field tests.а The most important components in the Andrena-Fuscii-
Luteae and Arachnitiformes-Araneiferae attractions were concluded to be geraniol, 
E,E-farnesol and aliphatic 1-alcohols (Borg-Karlson 1990).а Andrena bees and digger 
wasps (Argogorytes spp. and Campsoscolia ciliata) showed the most vigorous responses 
to these compounds.а Borg-Karlson notes that in field tests these insects began to 
expose their genitalia before they even encountered the model dummies.а Males of 
Andrena squalida responded to odors of Ophrys splendida by eliciting a digging 
behavior that is common to sexually-stimulated bees.
In related studies it was found that some coleopteran pollinators are attracted to 
the alcohol compounds produced by some orchid species (Dettner and Liepert 1994).
Pollinator Specificity 
Taxonomy of Ophrys is currently based upon morphological characteristics.а Borg-
Karlson notes that this system is often confusing because consistent differences 
between species-subspecies, varieties, forms and hybrids can be very difficult to 
determine by morphology.а Kullenberg and Bergstrom (Kullenberg and Bergstrom 1976) 
have proposed that a taxonomic division based on pollination, insect attraction and 
chemical analysis of insect and flower volatiles might be more exact because the 
flower selection of particular insects to particular flower scents is fairly 
The exact degree of selectivity in these mimicry pollination systems is not yet 
clear (Borg-Karlson 1990).а The 'one-pollinator-one-Ophrys taxon' hypothesis is 
supported by field studies conducted so far.а Paulus and Gack (Paulus and Gack 1986) 
observed that four different forms of Ophrys fusca were pollinated by four different 
genera of hymenoptera.а In addition, Kullenberg proposed that Andrena bees can be 
divided into three categories based on their attraction to O. fusca and O. lutea 
(Kullenberg et al. 1985).а Some degree of specificity is also supported by the 
chemical similarities shown by Borg-Karlson's analysis.а However, other studies show 
that a variety of insects that are all of a particular 'physiological type' are 
attracted to Ophrysа flowers that are of a similar 'biochemical type' (Borg-Karlson 
1990).а For example, in Europe and Africa Andrena flavipesа pollinates several taxa 
of Ophrys fusci-luteaeа (Warncke and Kullenberg 1984).а 
Borg-Karlson (1990) points out that the odors emitted by Ophrysа flowers often 
include mixtures of compounds that are sure to attract more than one species of 
insect (at least within a particular genus).а The key components of the insect 
attraction that were identified by Borg-Karlson can be found in most Ophrysа 
species, but the amounts and proportions of these compounds vary greatly.а 
Quantitative differences may be partly responsible for the variation in attraction 
of different pollinators to Ophrys flowers.а Visual and tactile cues may also play 
an important part in the final selection of flowers by specific insects (Borg-
Karlson 1990).
Variation in Plant and Insect Odors
The large number of compounds involved in odor production as well as the variations 
that occur among individual plants make it difficult to determine the exact mixture 
produced by any one flower taxon.а Even though the chemical similarities have been 
determined and the behavioral effects of certain compounds have been demonstrated, 
it is still difficult to know exactly what is going on in the natural setting.а It 
is possible that the congruence between some insect and flower odors is actually 
much closer in nature than can be shown in the laboratory.а As pointed out by Stowe 
(1988), some compounds that are extracted and identified from the insects and/or 
flowers may never actually be released by the organism.а In addition, the mixtures 
of compounds that are released (especially by the flowers) may vary at different 
times of the day.а Important signal compounds that are produced in tiny amounts may 
be missed or overlooked during chemical identification.а Finally, variations in the 
volatile mixtures between individual plants may not be discerned when flowers are 
pooled into a single mix for extraction.а 
On the other hand, differences between the plant and insect odors in the natural 
setting may be greater than has been shown in the laboratory.а Extra compounds found 
in the plant odor blends that are not produced by the insects may greatly effect the 
overall odor and subsequent behavior of the insects.а Also, plant volatile blends 
may not include some compounds that are generated in the insect glands.а In 
addition, the ratios of individual compounds may vary between the insect and the 
plant.а Finally, the mixtures produced by the plants may change greatly throughout a 
24 hour period.а 
Broodsite or Food Mimicry
Some flowers mimic the odors of dung and/or carrion to attract insects (mostly 
beetles and flies) for pollination.а These systems are widespread in the plant 
kingdom and have been extensively reported on.а This type of relationship is found 
in ten plant families (Annonaceae, Araceae, Aristolochiaceae, Asclepiadaceae, 
Burmanniaceae, Hydnoraceae, Orchidaceae, Rafflesiaceae, Sterculiaceae, and 
Taccaceae) (Wiens 1978).
The odors produced by these flowers smell like decaying protein or feces and are 
very unpleasant to humans.а However, the scents are highly attractive to 
coprophilous beetles and flies that oviposit or feed at carrion or dung.а 
While the primary cues that the insects respond to are olfactory, secondary visual 
cues are produced by some plants.а For example, several species of Araceae have 
enlarged bracts, mottled purple petals and attenuated appendages.а With a 
combination of these features, the flower bears a striking resemblance to a mass of 
foraging flies (Wiens 1978).
Chemistry of Dung/Carrion Mimicry
Chemicals that are responsible for the carrion-like odors include ammonia, 
alkylamines, cadaverine and putrescine.а More fecal-like odors are also produced by 
skatole and indole (Dettner and Liepert 1994).а These odors are enhanced in some 
flowers (of the Araceae) by the production of heat and carbon dioxide.а Heat 
increases the production of volatile compounds and carbon dioxide, which is produced 
as a by-product of the heat production may increase the length of time that an 
insect remains at the flower (Dafni 1984).
In addition to mimicking attractive odors, many dung or carrion flowers have evolved 
elaborate traps that increase the likelihood of pollination.а In general, flies and 
beetles are not active pollinators and must be induced into having adequate contact 
with the reproductive structures of the flower (Wiens 1978).а To insure pollination, 
these plants mimic food or brood-site odors to attract the insects to the flowers 
and lure them inside.а Once inside, the pollinators are trapped in the flower for an 
extended period of time.а In most systems the insects are eventually released by the 
flower or allowed to escape, but in a few cases the insects are permanently trapped 
or even killed (Stowe 1988).
Mimicry of Decaying Fruit
In a similar mimicry system, flowers produce odors that resemble those of either 
fresh or decaying fruit.а The main pollinators in these cases are beetles and small 
flies.а Methylesters may play a role in this attraction as they are present in many 
fruit odors as well as in many flower scents (Stowe 1988), (Gottsberger 1977).а 
Prey Mimicry
Wiens (1978) reported on an unusual variation of reproductive mimicry in which 
plants attract parasite or predator pollinators by mimicking their prey (hosts).а In 
some cases, the insect is rewarded with nectar and in other cases there is no 
reward.а Occasionally, the insect is duped into laying its eggs in the flower.а 
Because the flower is not a true broodsite, the eggs either do not hatch or the 
hatchlings die for lack of proper food (Stowe 1988).а In these mimicry systems, the 
flower is sometimes pollinated when a parasite tries to sting what they think is 
their prey on the flower.а In other cases, the flowers lure their pollinators inside 
and use elaborate traps to contain the insects long enough to insure pollination.а 
Three genera of orchid (Ada, Brassia and Encyclia) are known to use this 
"pseudoparasitism" method of attracting pollinators.а In addition, two unrelated 
genera of orchids (Epipactis and Paphiopedilum) may mimic the compounds produced by 
aphids in order to attract female syrphid flies that normally lay their eggs near 
aphid infestations.а According to Stowe (1988), visual cues and nectar are also 
important in attracting the flies to the flowers.а Because the presence of aphid 
odors stimulates oviposition by the flies, it is likely that the plants are indeed 
mimicking the chemistry of aphids even though these examples have not been verified.а 
One species of orchid (Oberonia thwaitesii) that is pollinated by ants may also 
mimic aphid odors (Faegri and van der Pijl 1979). 
Cost/Benefit of Pollination Mimicry
One question that is often debated in the literature is whether or not pollinators 
are impaired by their participation in these systems where no reward is received for 
their pollination efforts.а In the systems involving mimicry of food or broodsite 
odors, the cost to the insects varies.а In some cases, a duped insect only loses 
some time while searching for food that is not there or while he is trapped inside a 
flower for an extended period.а The cost is much higher, however, when a female is 
fooled into laying her eggs on a false broodsite.а 
The costs and/or benefits to the pollinators in systems where plants mimic female 
insects are more difficult to determine.а Kullenberg (1985) and Burns-Balogh (1985) 
believe that the non-rewarding flowers may actually benefit their pollinators.а For 
example, the flowers serve to concentrate male insects in a suitable habitat where 
females are likely to be found.а In addition, the males who are sexually stimulated 
after their encounters with flowers may spend more time looking for females to mate 
On the other hand, Stowe (1988) argues that the non-rewarding mimics are harmful to 
their pollinators. Because the male insects lose time that would otherwise be spent 
seeking females, they ultimately achieve lower mating success.а He argues that there 
is much less profit in time spent visiting the flowers than in time spent in 
searching for females.а He believes that males who can discriminate between flowers 
and female insects will have the selective advantage.
However, these plants depend upon insects for pollination and it would not be to 
their ultimate advantage to out-compete female insects for the attention of the 
males.а As pointed out by Weins (1978) some of the plants in these systems produce 
flowers after male pollinators have become active but before the females emerge.а In 
this way, they are able to acheive pollination and still avoid competition with 
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