Gaskett - Orchid Pollination by Sexual Deception Pollinator Perspectives

Biol. Rev. (2011), 86, pp. 3375.
doi: 10.1111/j.1469-185X.2010.00134.x
33
Orchid pollination by sexual deception:

pollinator perspectives
A. C. Gaskett1,2
1 Department
2
of Biological Sciences, Macquarie University, NSW 2109, Australia

Present address: School of Biological Sciences, The University of Auckland, Private Bag 92019, Auckland 1142, New Zealand
(Received 29 August 2008; revised 25 February 2010; accepted 1 March 2010)
ABSTRACT
The extraordinary taxonomic and morphological diversity of orchids is accompanied by a remarkable range of
pollinators and pollination systems. Sexually deceptive orchids are adapted to attract specific male insects that are fooled
into attempting to mate with orchid flowers and inadvertently acting as pollinators. This review summarises current
knowledge, explores new hypotheses in the literature, and introduces some new approaches to understanding sexual
deception from the perspective of the duped pollinator. Four main topics are addressed: (1) global patterns in sexual
deception, (2) pollinator identities, mating systems and behaviours, (3) pollinator perception of orchid deceptive signals,
and (4) the evolutionary implications of pollinator responses to orchid deception, including potential costs imposed on
pollinators by orchids. A global list of known and putative sexually deceptive orchids and their pollinators is provided
and methods for incorporating pollinator perspectives into sexual deception research are provided and reviewed.
At present, almost all known sexually deceptive orchid taxa are from Australia or Europe. A few sexually deceptive
species and genera are reported for New Zealand and South Africa. In Central and Southern America, Asia, and the
Pacific many more species are likely to be identified in the future. Despite the great diversity of sexually deceptive orchid
genera in Australia, pollination rates reported in the literature are similar between Australian and European species.
The typical pollinator of a sexually deceptive orchid is a male insect of a species that is polygynous, monandrous,
haplodiploid, and solitary rather than social. Insect behaviours involved in the pollination of sexually deceptive orchids
include pre-copulatory gripping of flowers, brief entrapment, mating, and very rarely, ejaculation. Pollinator behaviour
varies within and among pollinator species.
Deception involving orchid mimicry of insect scent signals is becoming well understood for some species, but
visual and tactile signals such as colour, shape, and texture remain neglected. Experimental manipulations that test
for function, multi-signal interactions, and pollinator perception of these signals are required. Furthermore, other
forms of deception such as exploitation of pollinator sensory biases or mating preferences merit more comprehensive
investigation. Application of molecular techniques adapted from model plants and animals is likely to deliver new
insights into orchid signalling, and pollinator perception and behaviour.
There is little current evidence that sexual deception drives any species-level selection on pollinators. Pollinators do
learn to avoid deceptive orchids and their locations, but this is not necessarily a response specific to orchids. Even in
systems where evidence suggests that orchids do interfere with pollinator mating opportunities, considerable further
research is required to determine whether this is sufficient to impose selection on pollinators or generate antagonistic
coevolution or an arms race between orchids and their pollinators.
Botanists, taxonomists and chemical ecologists have made remarkable progress in the study of deceptive orchid
pollination. Further complementary investigations from entomology and behavioural ecology perspectives should
prove fascinating and engender a more complete understanding of the evolution and maintenance of such enigmatic
plant-animal interactions.
Key words: orchid, pollinator behaviour, mating behaviour, insects, floral scent, colour and shape, mimicry, sensory
biases, learning, evolution.
* Address for correspondence: E-mail: a.gaskett@auckland.ac.nz

Biological Reviews 86 (2011) 3375 2010 The Author. Biological Reviews 2010 Cambridge Philosophical Society
A. C. Gaskett
34
CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
II. Pollination by sexual deception . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
III. Pollinators of sexually deceptive orchids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Pollinator identities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Pollinator mating systems and traits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Exceptions to the general types of pollinators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
IV. Pollinator behaviours . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Pollinator behaviour and the origins of sexual deception . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Pollinator sexual behaviour with orchids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Sexual deception by Pterostylis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Within-species variation in pollinator behaviour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
V. Pollinator abundance and diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
VI. Orchid signals and pollinator perception . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Scent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Colour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Shape . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Multimodal signalling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
VII. Pollinator learning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
VIII. Costs of deception and orchid-pollinator coevolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
IX. Future directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
X. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
XI. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
XII. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
I. INTRODUCTION
Sexual deception is an extreme form of pollinator specialisation in which an orchid lures its pollinator with fraudulent sex
signals. Male insects fooled into sexual behaviour with orchid
flowers inadvertently collect or deliver the pollinia and do
not receive floral rewards such as nectar or pollen (Schiestl,
2005; Jersakova, Johnson & Kindlmann, 2006a). In specialist pollination systems, flowers are unconstrained by the
stabilising selection that limits generalist pollination systems
to floral forms suiting several pollinators (Cresswell, 1998;
2000). Instead, specialist flowers can evolve specific fitnessenhancing adaptations to their pollinator, e.g. corollas that
match pollinator tonguelength (Alexandersson & Johnson,
2002; Rodrguez-Girones & Santamara, 2007; Muchhala
& Thomson, 2009). Sexually deceptive orchids are highly
specialised and typically pollinator-specific, thus pollinator
preferences and pollinator-driven selection are likely to be
strongly directional and influence orchid floral features and
diversity (Peakall & Handel, 1993; Cozzolino & Widmer,
2005; Mant, Peakall & Schiestl, 2005d; Schiestl & Schluter,
2009). Investigation of how pollinators and their behaviours
might affect the evolution and maintenance of sexual deception by orchids provides new insights into this intriguing
subject.
Sexual deception relies on the pollinators sexual rather
than foraging behaviour, suggesting insect sexual behaviour
is crucial in driving the evolution of orchid features. Analysis
of the sexual behaviours stimulated by orchids and the natural mating systems of pollinators in the absence of orchids
could reveal which types of insects and behaviours permit and
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maintain deception. Furthermore, as sexual deception relies

upon exploiting pollinator sensory ecology, insect perception
of signals is fundamental for selection on orchid features.
Insects are capable of sophisticated learning, memory, and
cognition (Dukas, 2008), which are also likely to affect orchid
signals and the evolution of deception.
Recent reviews discuss the mechanisms of orchid
deception and the selective pressures on orchids influencing
the evolution of deception (Schiestl, 2005; Jersakova et al.,
2006a; Schaefer & Ruxton, 2009; Vereecken, 2009), and how
orchid ecology, pollination biology, genetics, mycorrhizal
associations, and environmental factors affect orchid
speciation (Tremblay, 1992; Vasquez, Ibisch & Gerkmann,
2003; Gravendeel et al., 2004; Cozzolino & Widmer, 2005;
Tremblay et al., 2005; Peakall, 2007; Schluter & Schiestl,
2008; Waterman & Bidartondo, 2008; Phillips et al., 2009a;
Schiestl & Schluter, 2009). Here, however, sexually deceptive
pollination is considered from the pollinator perspective.
This review summarises current knowledge, explores new
hypotheses in the literature, and introduces some new
approaches as to how pollinators and their mating systems, behaviour, sensory perception and diversity could
influence the evolution of sexual deception. Contemporary
and historic data are synthesised and evaluated from both
broadlyaccessible and lesser-known sources, and from experiments, comparative studies, and natural history observations.
The first part of this review concerns pollinators and their
behaviour during pollination. Pollinator identity and natural
mating systems are surveyed and broad patterns in pollinator
sexual behaviours during visits to different types of orchids
are identified. Evidence for sexual deception in the poorly
Orchid pollination by sexual deception

known Pterostylis complex is evaluated. The second and major
element of this review discusses orchid signals and the mechanisms of deception by considering how orchids mimic female
insects and exploit male insects sensory biases. Attempts to
analyse pollinator perception of orchid scent and colour signals are reviewed and topics for productive further research
are identified. The third section of this review addresses
the question of whether sexual deception could involve
avoidance learning by pollinators, corresponding selection
on pollinators by orchids, and consequently coevolution
between orchids and pollinators. I evaluate whether orchids
could impose costs on their pollinators at the individual,
population, or species level. Finally, I propose some future
directions promoting research into pollinator perspectives.
Reflecting current knowledge, this review focuses primarily on European and Australian orchid species. Species
from Central and Southern America, South Africa and New
Zealand have been the subjects of fewer studies and consequently, they are covered in less detail here. The taxonomy
of Australasian orchids is undergoing considerable revision
(see Hopper, 2009). I use the most commonly recognised
genera and species names, with reference to the Australian
Plant Names Index (Centre for Plant Biodiversity Research,
2008). Table 1 also provides the newer names for genera
from revisions by Jones (2006). European orchids are named
according to the International Plant Names Index (2008) and
Delforge (2005). European pollinator names are according
to Fauna Europaea (2004).
II. POLLINATION BY SEXUAL DECEPTION

Although an absence of floral rewards occurs at least
intermittently in species from almost all major angiosperm
groups, obligatory deception is most common amongst
orchids (Schiestl, 2005; Renner, 2006). Many orchid species
are food-deceptive in that they resemble rewarding flowers
but do not provide food rewards, and are pollinated by
female and male insects attempting to feed from the flowers
(Jersakova et al., 2006a). Sexual deception is less common
than food deception in the orchids, but has nonetheless
evolved multiple times in different lineages (Kores et al., 2001;
Cozzolino & Widmer, 2005). Currently, there are thought
to be 11 sexually deceptive genera in Australia: Arthrochilus,
Caladenia (including synonyms according to Jones (2006),
e.g. Arachnorchis and Jonesiopsis), Caleana, Calochilus, Chiloglottis
( including synonyms Myrmechila and Simpliglottis), Cryptostylis,
Drakaea, Leporella, Paracaleana (synonymous with Sullivania),
Pterostylis (including synonyms, e.g. Diplodium, Linguella,
Oligochaetochilus and Urochilus), and Spiculaea (see Table 1 for
species with known pollinators; Figs 1 and 2 for images).
In New Zealand, several of these genera are represented
by endemic species or occasional vagrants from Australia
(Caladenia, Caleana, Calochilus, Chiloglottis, Cryptostylis, and
Pterostylis; St George, 1999). However, conclusive pollinator
identifications and evidence of sexual deception amongst
New Zealand species is largely absent. Tentative pollinator
35
identifications for some potentially sexually deceptive New
Zealand species are listed in Table 1. The accepted number
of sexually deceptive genera in Australia is likely to change if
reports of sexual deception in Pterostylis cannot be confirmed
or if the proposed taxonomic splitting of Caladenia, Chiloglottis
and Pterostylis is upheld (Jones & Clements, 2003; Jones, 2006;
Hopper, 2009; see Section IV.3; seeTable 1 for synonyms).
In Europe, there is a diversity of food-deceptive orchid
genera, but sexual deception is restricted to the large
and well-studied genus Ophrys, and a single species of the
related and generally food-deceptive genus Orchis (Table 1;
Bino, Dafni & Meeuse, 1982; Widmer, Cozzolino & Dafni,
2001). Perhaps surprisingly, only two South African sexually
deceptive species are known, both from the well-studied and
generally rewarding or food-deceptive genus Disa (Table 1;
Steiner, Whitehead & Johnson, 1994; Johnson, Linder &
Steiner, 1998). Although no sexually deceptive orchids are
known for North America, sexual deception is confirmed
for species from eight South and Central American orchid
genera, and more cases are likely to be recognised in the
future (Table 1; Dodson, 1962; Dod, 1976; Calvo, 1990;
van der Cingel, 2001; Singer, 2002; Singer et al., 2004;
Blanco & Barboza, 2005; Ciotek et al., 2006). For example,
although only two Central American Lepanthes species are
listed in Table 1, this is a diverse and highly regionally
endemic neotropical genus and sexual deception is suspected
for many species (Vasquez et al., 2003; Blanco & Barboza,
2005; Schiestl, 2005). Similarly, there are approximately 15
potentially sexually deceptive Cryptostylis species distributed
throughout the Asia-Pacific region, but sexual deception
is confirmed for only the five species from Australia and
New Zealand (Jones, 2006; Table 1). Subantarctic sexual
deception is also a possibility; Chiloglottis and Pterostylis species
grow on New Zealands subantarctic islands (Meurk, Foggo
& Wilson, 1994; Molloy, 2002).
When data from food- and sexually deceptive orchids
are combined, pollination success is higher in southern
temperate regions (41.4%) than in the tropics (11.5%),
North America (19.5%) and Europe (27.7%; Neiland &
Wilcock, 1998). However, if the dataset includes only
sexually deceptive orchid species (Table 1), there is no
significant difference in the pollination rates of flowers
from southern temperate Australia and from Europe
(mean S.D; Australia: 18.4 11.4%, N = 21; Europe:
18.4 17.4%, N = 8; ANOVA F1,28 = 0.04, P = 0.95).
Insufficient data for sexually deceptive species elsewhere
prevents comparisons for these regions (see Table 1 for a
summary of the pollination rates reported in the literature).
III. POLLINATORS OF SEXUALLY DECEPTIVE

ORCHIDS
Sexually deceptive orchid species typically exploit one or
few specific pollinator species, (Table 1), and may have
different pollinators in different regions (e.g. Chiloglottis species; Bower & Brown, 2009). A single insect
Diseae
South Africa
Disa atricapilla (Harv. ex
Lindl.)
Disa bivalvata (L. f.)
T.Durand & Schinz.
Diurideae
Australia
Arthrochilus huntianus
(F.Muell.) Blaxell subsp.
huntianus (prev. Spiculaea
huntiana (F.Muell.)
Schltr.)
Arthrochilus irritabilis
F.Muell.
Arthrochilus latipes
D.L.Jones
Caladenia (syn. Arachnorchis)
amnicola D.L.Jones
Caladenia ampla (D.L.Jones)
G.N.Backh.
arenicola Hopper &
A.P.Br.
atrovespa D.L.Jones
Cymbidieae
Japan
Cymbidium pumilum Rolfe
Orchid
Arthrothynnus rufiabdominalis
Brown
Arthrothynnus sp.
Thynnoides gracilis
(Westwood)
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Thynnoides senilis (Erichson) Tiphiidae;
Hymenoptera
Phymatothynnus nr. nitidus 1 Tiphiidae;
Hymenoptera
Zaspilothynnus nigripes
Tiphiidae;
Guerin
Hymenoptera
Tiphiidae;
Hymenoptera
Arthrothynnus huntianus
Brown (not Rhagigaster
sp. as suggested by
Rotherham, 1967)
Apidae;
Hymenoptera
Sphecidae;
Hymenoptera
Pompilidae;
Hymenoptera
Apis cerana japonica

Fabricius
Pollinator
Family; Order
Primarily Podalonia
canescens (Dahlbom)
Hemipepsis hilaris Sm.,
H. capensis Fabricius
Growth form Pollinator
unconf.
9.9
36.4 (550 on
184 plants)
42.1 (482 on
116 plants)
Pollinator sexual % flowers

behaviour
pollinated (N )
% plants
pollinated (N )
Phillips et al. (2009a)
Brown et al. (1997); Phillips et al.

(2009a)*
Bower (2001a)
Bower (2001a)
Rotherham (1967); Bower

(2001a, f ); Mant et al. (2005c)
Steiner et al. (1994)
Steiner et al. (1994)
Sasaki et al. (1991)
Source
Table 1. Sexually deceptive orchid species and their pollinators. All pollinators are male, except where a female pollinator is specifically stated. A question mark (?) after
the pollinator name indicates a putative rather than confirmed pollinator. When data are reported from more than one study, symbols (*, , or ) correspond between the
data and citation. Pro. hybr. after a species name indicates it was described as an occaisional hybrid by Delforge (2005). For Growth form, E = epiphytic, T = terrestrial.
For Pollinator sexual behaviour stimulated by the orchid: 1 = pollinator copulates and ejaculates on the orchid, 2 = pollinator copulates with orchid, 3 = pollinator grips or
lifts hinged labellum, 4 = pollinator is briefly trapped and transfers pollinia on escape, unconf. = pollination is likely to involve sexual behaviour, but this is unconfirmed. %
flowers pollinated is the percentage of flowers that had pollinia collected and deposited, or set fruit. % plants pollinated is the percentage of flowering plants that had pollinia
collected and deposited, or set fruit. (N ) = number of flowers or plants reported in that study. Pollination rates labelled with more than one symbol are the average of data
from the correspondingly labelled source. Australian orchid species names are from the Australian Plant Names Index (Centre for Plant Biodiversity Research, 2008) and
Jones (2006). European orchid species names are according to the International Plant Names Index (2008) and Delforge (2005). Orchid families are according to van der
Cingel (2001) and Kores et al. (2001). European pollinator names are according to Fauna Europaea (2004)
36
A. C. Gaskett

concolor Fitzg.

clavula D.L.Jones
concinna (Rupp)
D.L.Jones &
M.A.Clem.
Caladenia aff. concinna

calcicola G.W.Carr
Callitrophila D.L.Jones
caudata Nicholls
clavigera A.Cunn. ex
Lindl.

behrii Schltdl.
branwhitei D.L.Jones
brownii Hopper & A.P.Br.
Caladenia (syn. Jonesiopsis)
cairnsiana F.Muell.

attingens Hopper &
A.P.Br. subsp. attingens
aurulenta (D.L.Jones)
R.J.Bates
australis G.W.Carr
Caladenia (syn. Drakonorchis)
barbarossa Rchb.f.
Thynnoides sp.* (Thynnoides
bidens (Saussure)
inaccurate, G. Brown
pers. comm.)
Tachynomyia sp.
Thynnoides sp.
Phymatothynnus nitidus
Sm.?* Phymatothynnus
victor Turner
Phymatothynnus nr. nitidus 1
Thynnine wasp
Thynnine wasp
Phymatothynnus monilicornis
(Sm.) complex*,
Lophocheilus anilitatus
(Sm.)
Lestricothynnus sp.
Thynnine wasp
Neozeleboria nr. volatile (Sm.)
Aeolothynnus generosus
(Turner)
(Sm.) complex
Zaspilothynnus sp.
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Thynnine wasp
Tiphiidae;
Hymenoptera
Macrothynnus sp.
3?
32.1
14 (782)
1.8*
19.9
C.C. Bower (unpublished data)
Bates (2009a)
Phillips et al. (2009a)*; Bates

(2009a)
Hopper & Brown (2001)
C. C. Bower (unpublished data)
Stoutamire (1974, 1983); Brown

et al. (1997)*; Phillips et al.
(2009a)
Bates (2009b)
Coleman (1930); Stoutamire

(1974, 1979, 1983); Brown
et al. (1997); Phillips et al.
(2009a)*
Dickson & Petit (2006)
Bates (2009a)

37

ferruginea Nicholls
filamentosa R.Br.
fitzgeraldii Rupp
formosa G.W.Carr

discoidea Lindl.
Caladenia dilatata var.
rhomboidiformis
E.Coleman
Caladenia douglasiorum
(D.L.Jones) G.N.Backh.
doutchiae O.H.Sarg.
exstans Hopper &
A.P.Br.
falcata (Nicholls)
M.A.Clem. & Hopper

crebra A.S.George
cruciformis D.L.Jones
cruscula Hopper &
A.P.Br.
decora Hopper & A.P.Br.
dilatata R.Br.

conferta D.L.Jones
corynephora A.S.George
Orchid
Table 1. (Cont.)
Thynnine wasp;
Lestricothynnus modestus
(Sm.)*
Campylothynnus assimilis
Sm. C. flavopictus (Sm.)
Thynnine wasp
Guerin
Thynnoides gracilis
(Westwood), Thynnoides
spp.
Phymatothynnus sp.
Zeleboria marginalis
(Westwood)* ,
Thynnoides sp. ,
(Thynnoides bidens*
inaccurate; G. Brown
pers. comm.)
Thynnine wasp
Chilothynnus trochanterinus
Brown
Thynnine wasp
Phymatothynnus nr.
pygidialis 1
Thynnine wasp*,
Phymatothynnus ?nitidus
Thynnoides sp.
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Ichneumonid sp.?
Tiphiidae;
Hymenoptera
Ichneumonidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Pollinator
Family; Order
Thynnine wasp
3?
14.4
8.3*
14.3

behaviour
pollinated (N )
% plants
pollinated (N )
Brown et al. (1997)*; Phillips et al.

(2009a)
Stoutamire (1983)*; Brown et al.

(1997)
Coleman (1930)
Stoutamire (1983); but see van

der Cingel (2001) for several
other sources)
Stoutamire (1983); Brown et al.

1997; van der Cingel (2001)*;
Phillips, et al. (2009)*
Brown et al. (1997)
Bates (2009a)
Source
38
A. C. Gaskett

lowanensis G.W.Carr
macrostylis Fitzg.
magniclavata Nicholls

fragrantissima D.L.Jones
& G.W.Carr
gardneri Hopper &
A.P.Br.
georgei Hopper &
A.P.Br.
gladiolata R.S.Rogers
hastata (Nicholls) Rupp
aff. heberleana Hopper &
A.P.Br.
huegelii Rchb.f.
incrassata Hopper &
A.P.Br.
infundibularis
A.S.George
insularis G.W.Carr
integra E.Coleman
leptoclavia D.L.Jones
lobata Fitzg.
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Zaspilothynnus sp.
Zaspilothynnus sp.
Zaspilothynnus sp.
Guerinius sp.? *, thynnine
wasp
(Sm.) complex
Thynnine wasp (Thynnoides
preissi & T. bidens
inaccurate; G. Brown
pers. comm.)
Tachynomyia sp.
Thynnine wasp
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Thynnine wasp
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Lophocheilus villosus Guerin
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Thynnine wasp
Tiphiidae;
Hymenoptera
Zaspilothynnus sp.
Thynnine wasp
Tiphiidae;
Hymenoptera
Phymatothynnus nr. pygidialis

2
7.3*
Bates (2009b)
(Stoutamire, 1983)
Stoutamire (1979, 1983); Brown

et al. (1997)
Stoutamire (1983)*; Brown et al.

(1997)
Bates (2009b)
Stoutamire (1983); Phillips et al.

(2009a)*
Bates (2009b)
Brown et al. (1997); S.D. Hopper

(unpublished data)
(Pritchard, 2007)
Bates (2009a)
Bates (2009b)

(unpublished data)

39

reticulata Fitzg
rhomboidiformis
(E.Coleman)
M.A.Clem. & Hopper
richardsiorum D.L.Jones
rigida R.S.Rogers
rileyi D.L.Jones

phaeoclavia D.L.Jones
procera Hopper & A.P.Br
pulchra Hopper &
A.P.Br. (prev. Caladenia
flaccida subsp. pulchra
Hopper & A.P.Br.)
radiata Nicholls

pachychila Hopper &
A.P.Br.
parva G.W.Carr
pectinata R.S.Rogers

montana G.W.Carr
multiclavia Rchb.f.
necrophylla D.L.Jones
Orchid
Table 1. (Cont.)
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Pollinator
Family; Order
Phymatothynnus aff. pygidialis Tiphiidae;

Hymenoptera
Phymatothynnus sp.
Tiphiidae;
Hymenoptera
Thynnoides new sp. R
Tiphiidae;
Brown
Hymenoptera
Thynnine wasp;
Tiphiidae;
Zaspilothynnus sp.*,
Hymenoptera
Catocheilus affinis
(Guerin)*
Tiphiidae;
Phymatothynnus nr. nitidus
Hymenoptera
1*, Phymatothynnus victor
Tiphiidae;
Guerin
Hymenoptera
Guerin?
Aeolothynnus sp. (as
Asthenothynnus sp.)
Zeleboria marginalis
(Westwood) (as
Z. marginatus);
Guerin*
Lophocheilus anilitatus (Sm.)
Thynnoides senilis (Erichson)
T
Thynnine wasp*;
Tachynomia sp.
Phymatothynnus sp.
2.5*

behaviour
pollinated (N )
% plants
pollinated (N )
Bates (2009a)
Bates (2009a)

(2009a)
Stoutamire (1983); Phillips et al.

(2009a)*

(unpublished data)
Bower (1992); Mant et al. (2005c);

Brown et al. (1997); Phillips et al.

(2009a)*
Brown et al. (1997) ; Hopper &

Brown (2001)*
(Stoutamire, 1983; Brown et al.

1997)
Bates (2009a)
Bower (2001b)
Source
40
A. C. Gaskett
Thynnoides mesopleuralis
Turner
Thynnine wasp
(Sm.)*, Phymatothynnus
monilicornis complex*,
Phymatothynnus sp. 14
Thynnine wasp
Thynnoides aff. gracilis
Thynnoides pugionatus
Guerin (sp. complex),
T. rufithorax Turner,
Thynnoides gracilis
(Westwood)
Thynnoides new sp.
D Brown
Macrothynnus sp.
Aeolothynnus generosus
(Turner)
Thynnine wasp
Phymatothynnus sp.
Caladenia aff. tentacula

tesselata D.L.Jones
thinicola Hopper &
A.P.Br
toxochila Tate
uliginosa A.S.George
valida (Nicholls)
M.A.Clem. &
D.L.Jones
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Phymatothynnus nitidus

stricta R.J.Bates
tensa G.W.Carr
tentaculata Schltdl.
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Thynnine wasp
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera

robinsonii G.W.Carr
roei Benth.
saxatilis (D.L.Jones)
R.J.Bates
septuosa D.L.Jones
speciosa Hopper &
A.P.Br.
stellata D.L.Jones
20.5
36.4 (1214)*
Bates (2009a)
Bates (2009b)
Bower (1992); Peakall & Beattie

(1996)*; Mant et al. (2005c);
Bates (2009a)
Bates (2009a)

(2009a)

(unpublished data)
Bates (2009a)
Stoutamire (1983); Brown et al.

(1997)
Bates (2009a)

41
Scoliidae;
Hymenoptera
Scoliidae;
Hymenoptera
Scoliidae;
Hymenoptera
Scoliidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Thynnine wasp
Lophyrotoma leachii (Kirby)*, Pergidae;
Pterygophorus sp. ,
Hymenoptera
L. cyanea (Leach)
Iswaroides armiger (Turner) Tiphiidae;
(prev. Thynnoturneria
Hymenoptera
armiger)
Scoliidae;
Hymenoptera
Thynnine wasp
Campsomeris sp.
Campsomeris tasmaniensis
Saussure
Scoliid wasp (also
self-pollinates)
Scoliid wasp (also
self-pollinates)
Scoliid wasp (also
self-pollinates)
Neozeleboria n.sp. 33 Brown
Chiloglottis aff. formicifera 2
Neozeleboria impatiens Sm.

N . aff. impatiens
Arthrothynnus latus Brown,
A. angustus Brown,
Neozeleboria nr sp. 25(A)*
Neozeleboria n.sp. 41 Brown Tiphiidae;
Hymenoptera
Neozeleboria n.sp. 45 Brown Tiphiidae;
Hymenoptera
Thynnine wasp
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Zaspilothynnus sp. nov. 5
Pollinator
Family; Order
Chiloglottis (syn. Myrmechila)

formicifera Fitzg.
Chiloglottis aff. formicifera 1
Calochilus cupreus
R.S.Rogers
Calochilus platychilus
D.L.Jones
Calochilus pruinosus
D.L.Jones
Chiloglottis anaticeps
D.L.Jones
Chiloglottis (syn. Simpliglottis)
chlorantha D.L.Jones
Chiloglottis diphylla R.Br.
Caleana (syn. Sullivania)

minor R.Br. (prev.
Paracaleana minor (R.Br.)
Blaxell)
Calochilus caeruleus
L.O.Williams (as
Calochilus holtzei
F.Muell.)
Calochilus campestris R.Br.

verrucosa G.W.Carr
villosissima (G.W.Carr)
D.L.Jones & M.A.Clem
wanosa A.S.George
woolcockiorum D.L.Jones
zephyra (D.L.Jones)
R.J.Bates
Caleana major R.Br.
Orchid
Table 1. (Cont.)

behaviour
pollinated (N )
% plants
pollinated (N )
Bower, (1992, 1996); Mant et al.

(2002, 2005c, d)
Mant et al. (2002, 2005c, d)
Mant et al. (2002); Mant et al.

(2005c, d)
Bower, (1996)*; Mant, et al.
(2005c)
Mant et al. (2005c)
Bates (2009a)
Bates (2009a)
Fordham (1946); Bower &

Branwhite (1993)
Bates (2009a)
Jones & Gray (1974); Bower

(2001d)
Bower (2001c)
Cady (1965)*; Bates (1989) ;

Bates (2009a)
Bates (2009a)
Brown et al. (1997)
Source
42
A. C. Gaskett

N .aff. impatiens
Neozeleboria tabulata Brown
Neozeleboria tabulata Brown
Thynnine wasp
Chiloglottis aff. pluricallata 2
Chiloglottis reflexa (Labill.)

Druce
Chiloglottis reflexa sensu stricta

(Tas.)
Chiloglottis seminuda
D.L.Jones
Chiloglottis (syn.
Sympliglottis) triceratops
D.L.Jones
Chiloglottis sphrynoides
D.L.Jones
Chiloglottis sylvestris
D.L.Jones &
M.A.Clem.
trapeziformis Fitzg.
Chilothynnus palachilus
Brown
Neozeleboria cryptoides Sm.,

Zaspilothynnus sp.
T
Neozeleboria carinicollis
Turner
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Neozeleboria nr impatiens 2
Neozeleboria nr monticola 1
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Eirone sp.
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Eirone leai Turner

grammata G.W.Carr
gunnii Lindl.
jeanesii D.L.Jones
Chiloglottis palachila
D.L.Jones &
M.A.Clem.
platyptera D.L.Jones
pluricallata D.L.Jones
Chiloglottis aff. pluricallata
(also referred to as
Chiloglottis bifaria
D.L.Jones m.s)
4*
58.5 (210)
58.5 (210)
Oakwood (1990)*; Mant et al.

(2002); Schiestl, (2004) ; Mant
et al. (2005c, d); Bates (2009a)
Bower & Brown (2009)
Mant et al. (2002, 2005c, d)
Bower (1992, 1996); Bower &

Brown (1997); Mant et al.
(2002, 2005c, d)
Mant et al. (2002, 2005c, d)
Bower (1996); Bower & Brown

(1997); Mant et al. (2002,
2005c, d)
Bower (1992, 1996); Mant et al.

2002, 2005c, d)
Bower (1992, 1996); Mant et al.
(2002, 2005a, c, d)
Mant et al. (2002, 2005a, c, d)
Mant et al. (2005c)
Stoutamire (1975)
Mant et al. (2002, 2005c)

43
Chiloglottis aff. valida 2
Cryptostylis erecta R.Br.
Cryptostylis hunteriana
Nicholls
Cryptostylis leptochila Benth.
Cryptostylis ovata R.Br.
Cryptostylis subulata (Labill.)

Rchb.f.
Drakaea concolor Hopper &

A.P.Br.
Drakaea confluens Hopper &

A.P.Br.
Chiloglottis aff. valida 1

turfosa D.L.Jones
valida D.L.Jones
Zaspilothynnus gilesi Turner

(as Hemithynnus gilesi)*,
thynnine wasp
Thynnine wasp
Neozeleboria aff. ursitatum

Brown, N .sp. Spotted,
N . aff. cryptoides 1, N. aff
cryptoides 2, N . sp.
(red/black), N . sp.
(small black)
Neozeleboria nr monticola 2
Tiphiidae;
Hymenoptera
Neozeleboria monticola
Tiphiidae;
Turner, N. nitidula
Hymenoptera
(Turner), N. cryptoides
Sm.
Neozeleboria nr. impatiens 1 Tiphiidae;
Hymenoptera
Neozeleboria nr. impatiens,
Tiphiidae;
Neozeleboria nr.
Hymenoptera
monticola 3
Lissopimpla excelsa (Costa)
Ichneumonidae;
Hymenoptera
Ichneumonidae;
Hymenoptera
Ichneumonidae;
(prev. L. semipunctata)
Hymenoptera
Ichneumonidae;
Hymenoptera
Ichneumonidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Thynnine wasp
Tiphiidae;
Hymenoptera

trullata D.L.Jones
truncata D.L.Jones &
M.A.Clem.
Neozeleboria proxima
(Turner)
Pollinator
Family; Order
Chiloglottis trilabra Fitzg.
Orchid
Table 1. (Cont.)
1?
35.0 (47)*
66.6 (154)*
25.4 (994)*
41.9 (121)*
70.4 (402)*
41 (86)*
% plants
pollinated (N )
12.0 (122)*
5.2 (1329)*
32.7 (2187)*
41 (86)*

behaviour
pollinated (N )
Hopper & Brown (2007);

Hopper (2009)
Gaskett & Herberstein (2006)*;

Gaskett et al. (2008)
Coleman (1930); A. C. Gaskett
(unpublished data)*
Schiestl et al. (2004)*; Gaskett &
Herberstein (2006) ; Gaskett
et al. (2008)
Brown et al. (1997)*; Hopper &
Brown, (2007) ; Hopper (2009)
Gaskett & Herberstein (2006)*;

Gaskett et al. (2008)
Nicholls (1938)

(2009)
(2009)
Bower (1992, 1996, 2006); Mant

et al. (2005c, d); Bower &
Brown (2009)
Mant et al. (2002, 2005c, d)
Bower (1992, 1996); Peakall &

Handel (1993)*; Bower &
Brown (1997); Mant et al.
(2002, 2005c, d)
Source
44
A. C. Gaskett
Diptera
Mycetophilidae;
Diptera
Zaspilothynnus sp.
Myrmecia urens Lower
Mycetophilid fly
Thynnine wasp
Erione sp.*, Labium sp.
Culex sp. female mosquito?
Mycetophilid fly
Fly
Fly
Fly
Mycomya sp.
T
T
Drakaea micrantha Hopper

& A.P.Br.
Drakaea thynniphila
A.S.George
Leporella fimbriata (Lindl.)
A.S.George
Oligochaetochilus lepidus
D.L.Jones
Paracaleana hortiorum
Hopper & A.P.Br.
Paracaleana (syn. Sullivania)
nigrita (J.Drumm. ex
Lindl.) Blaxell
Pterostylis acuminata R.Br.
Pterostylis arenicola
M.A.Clem. & J.Stewart
(syn. Oligochaetochilus
arenicolus)
Pterostylis aspera D.L.Jones
& M.A.Clem. (syn.
Diplodium asperum)
Pterostylis (syn.
Oligochaetochilus)
boormanii Rupp
Pterostylis cucullata subsp.
sylvicola D.L.Jones
Pterostylis curta R.Br.
Guerin, Z. dilatatus
spiculifera Turner
Thynnine wasp
Drakaea livida J.Drumm.

(as Drakaea elastica Lindl.
in Stoutamire, 1979)
Drakaea livida x confluens
Diptera
Diptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Formicidae;
Hymenoptera
Mycetophilidae,
Diptera
Tiphiidae,
Hymenoptera
Tiphiidae,
Ichneumonidae;
Hymenoptera
Culicidae; Diptera
Mycetophilidae,
Diptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Drakaea gracilis Hopper &

A.P.Br.
Tiphiidae;
Hymenoptera
Zaspilothynnus trilobatus
Turner*, Z. dilatatus
spiculifera Turner
Guerin* (Thynnoides
bidens inaccurate, G.
Brown pers. comm.),
Thynnoides elongata
Guerin
Drakaea glyptodon Fitzg.
unconf.
unconf.
unconf.
unconf.
unconf.
unconf.
unconf.
23.9 (1478)
20.7 (1203)
20.7 (1203)
Bernhardt (1995)
Bates (2009a)
Bates (2009a)
Bates (2009b)
Coleman (1934)
Bates (2009a)
Brown et al. (1997)* ; Hopper &

Brown (2006)*
Bates (2009b)
Bates (2009a)
Hopper & Brown (2007);

Hopper (2009)
Mant et al. (2005c); Hopper &
Brown (2007); Hopper (2009)
Peakall (1989)
Stoutamire (1974, 1979); Mant

et al. (2005c); Hopper & Brown
(2007); Hopper (2009)
Brown et al. (1997)
Stoutamire (1974)*; Peakall

(1990)*; Brown et al. (1997)* ;
Mant et al. (2005c)*
Brown et al. (1997)*; Bates
(2009b)

45
Pterostylis rufa R.Br. (syn

Oligochaetochilus rufus)
Pterostylis sanguinea
D.L.Jones &
M.A.Clem. (syn.
Urochilus sanguineus
(D.L.Jones &
M.A.Clem.) D.L.Jones
& M.A.Clem.)
Pterostylis (syn. Ranorchis)
sargentii C.R.P.Andrews
Pterostylis (syn. Diplodium)
scabra Lindl. (as
Pterostylis constricta
O.H.Sarg.)
Pterostylis (syn. Urochilus)
vittata Lindl.
Spiculaea ciliata Lindl.
Pterostylis psammophila
(D.L.Jones) R.J.Bates
(syn. Oligochaetochilus
psammophilus)
Pterostylis pusilla
R.S.Rogers (syn
Oligochaetochilus pusillus
(R.S.Rogers) Szlach.)
rogersii E.Coleman
Pterostylis falcata
R.S.Rogers
Pterostylis gibbosa R.Br. (syn.
Oligochaetochilus gibbosus)
Pterostylis lepida (syn.
Oligochaetochilus lepidus)
Pterostylis (syn. Linguella)
nana R.Br.
Pterostylis nutans R.Br.
Orchid
Table 1. (Cont.)
Diptera
Tiphiidae;
Hymenoptera
Fly
Fly
Gnat
Thynnoturneria sp.*,
Iswaroides sp.
Diptera
Diptera
Diptera
Gnat
Mycetophilidae;
Diptera
Diptera
Fungus gnat*, fly
Fungus gnat
Mycetophilidae;
Diptera
Mycetophilidae;
Diptera
Diptera
Fungus gnat
Fungus gnat
Fly
Mosquito-like fly
Mycetophilid fly
Heteropterna sp.
Mycetophilidae;
Diptera
Mycetophilidae,
Diptera
Diptera
Culex sp. female mosquito? Culicidae; Diptera
Pollinator
Family; Order
unconf.
unconf.
unconf.
unconf.
unconf.
unconf.
4?
unconf.
4?
unconf.
unconf.
4?
unconf.
12 (490)*

behaviour
pollinated (N )
25.9 (154)*
% plants
pollinated (N )
Brown et al. (1997)*; Alcock

(2000)*; Mant et al. (2005c)
Sargent (1909)
Brown et al. (1997)
Sargent (1909)
Beardsell & Bernhardt (1982)*;

Brown et al. (1997)
Brown et al. (1997)
Bates (2009b)
Beardsell & Bernhardt (1982)
Bates (2009a)
Hyett (1960)
Brown et al. (1997)
Taylor (1999)*; National Parks &

Wildlife Service (2002)*
Bates (2009a)
Coleman (1934)
Source
46
A. C. Gaskett
Tachinidae;
Diptera
Meliponinae;
Hymenoptera
Paragymnomma sp.
Plebeia droryana Friese
Tolumnia (prev. Oncidium)

henekenii (R.H.Schomb.
ex Lindl.)
Trichoceros antennifera (prev.
T. parviflora) (H. et B).
H.B.K.
Trigonidium obtusum Lindley
Tachinid fly
Centris sp.?
Telipogon sp.
Stellilabium sp.
Apidae;
Hymenoptera
Tachinidae;
Diptera
Tachinidae;
Diptera
Anthophoridae;
Hymenoptera
Nannotrigona testaceicornis
(Lep.), Scaptotrigona sp.
Tachinid fly
Sciaridae; Diptera
Bradysia floribunda Mohrig
E
E
South and Central

America
Mormolyca ringens (Lindl.)
Scoliidae;
Hymenoptera
Campsomeris bistrimacula
(Lep.)
Pterostylis trullifolia Hook.f.

(syn. Diplodium
trullifolium)
South America
Geoblasta pennicillata (Rchb.
f.) Hoehne ex Correa
Epidendreae
Central America
Lepanthes glicensteinii Luer
Lepanthes wendlandii
Reichb. f. (E)
Maxillarieae
Fungus gnat?
Aneura longipalpis Tonnoir

& Edwards?* Cerotelion
sp.?*, Fungus gnat
Fungus gnat
Pterostylis patens Colenso
Mycetophilidae,
Keratophilidae;
Diptera
Mycetophilidae;
Diptera
Zygomyia sp.
Ichneumonidae;
Hymenoptera
Mycetophilidae;
Diptera
Pterostylis graminea Hook.f.
Cryptostylis subulata (Labill.)

Rchb.f.
alobula (Hatch)
L.B.Moore
Pterostylis australis Hook.f.
New Zealand
2&4
unconf.
1?
?
unconf.
4?
4?
4?
4?
1?
41 (24)
11.6 (4232 on
200 plants)
52.2 (57)
<25%
41.6 (24)
2.8 (72)
52.2 (57)
41.6 (24)
2.8 (72)
Singer (2002)
Dodson (1962); van der Cingel

(2001)
Christensen (1994); van der

Cingel (2001)
Christensen (1994); van der
Cingel (2001)
Dod (1976)
Singer et al. (2004)
Blanco & Barboza (2005)

Calvo (1990)
Ciotek et al. (2006)
Cheeseman (1872, 1875)
Lehnebach et al. (2005)
E. Scanlen (unpublished data)
Lehnebach et al. (2005)*;

E. Scanlen (unpublished data)
Lehnebach et al. (2005)
Graham (1983)

47
Eucera nigrilabris Lep.

Eucera ( prev. Synhalonia)
rufa (=Tetralonia berlandi
Dusmet)
Andrenidae,
Colletes cunicularius (L.);
Megachilidae,
Andrena sabulosa subsp.
Colletidae;
trimmerana, Osmia
Hymenoptera
aurentula* (probably =
Osmia aurulenta Panzer)
Osmia bicolor (Schrank)
Megachilidae,
Andrenidae;
inaccurate according to
Hymenoptera
Paulus (2000), Andrena
lathyri Alfken , Andrena
combinata (Christ)
Colletes cunicularius (L.)
Colletidae;
Hymenoptera
Andrena fulvata Stoeckhert Andrenidae;
Hymenoptera
Ophrys apiformis Steud.
Ophrys aprilia Devillers &

Devillers-Tersch.
Ophrys apulica (O.Danesch
& E.Danesch)
O.Danesch &
E.Danesch
Ophrys arachnitiformis Gren.
& M.Philippe
Eucera sp.*, Eucera

punctulata Alfken?
Eucera barbiventris Perez
Ophrys archipelagi Golz &

H.R.Reinhard
Ophrys argentaria
Devillers-Tersch. &
Devillers
Osmia rufa (L.)
Colletes sp.
Ophrys araneola Rchb.
Andrena bimaculata (Kirby)
Ophrys africana G.Foelsche

& W.Foelsche
Ophrys alasiatica Kreutz,
Segers & H.Walraven
Ophrys algarvensis D.Tyteca,
Benito & M.Walravens
Ophrys annae
Devillers-Tersch. &
Devillers
Ophrys apifera Huds.
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrena paucisquama
Noskiewicz
Andrena flavipes Panzer
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Colletidae;
Hymenoptera
Megachilidae;
Hymenoptera
Ophrys aesculapii Renz
Anthophora orientalis
Morawitz
Eucera taurica Morawitz
Pollinator
Family; Order
Ophrys aegaea Kalteisen &

H.R.Reinhard
Ophrys aegirtica P.Delforge
Orchideae
Europe
Orchid
Table 1. (Cont.)

behaviour
pollinated (N )
% plants
pollinated (N )
Paulus & Gack (1990); Widmer

et al. (2000); Delforge (2005)
Delforge (2005)
Paulus & Gack (1990)*; Delforge

(2005) ; Schiestl & Vereecken
(2008)
Kullenberg (1961); Delforge

(2005)*
Paulus & Gack (1990); Delforge

(2005)
Delforge (2005)
Kullenberg & Bergstrom,

(1976b)*; Paulus (2000)
Paulus & Gack (1990)
Delforge (2005)
Paulus (2006)
Delforge (2005)
Stokl et al. (2005)
Delforge (2005)
Delforge (2005)
Delforge (2005); Paulus (2006)
Source
48
A. C. Gaskett
Chalicodoma sicula (Rossi)
Ophrys bilunulata Risso
Ophrys biscutella O.Danesch

& E.Danesch
Chalicodoma parietina
(Geoffr.), C. pyrenaica
(Lep.)
Chalicodoma sicula (Rossi)*,
C. benoisti Tkalcu
Anthophora retusa (L.)
Eucera euroa Tkalcu
(Geoffr.)
Andrena vetula Lep.?
Anthophora nigrocincta Lep.
Ophrys bertoloniiformis
O.Danesch &
E.Danesch
Ophrys biancae Macch.
Ophrys basilissa A.Alibertis

& H.R.Reinhard
Ophrys battandieri
E.G.Camus (pro. hybr.)
Ophrys benacensis (Reisigl.)
O.Danesch &
E.Danesch
Ophrys bertolonii Moretti
Andrena combinata (Christ)
(Geoffr.), C. pyrenaica
(Lep.)
Andrena hattorfiana
(Fabricius)
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Megachilidae;
Hymenoptera
Megachilidae;
Hymenoptera
Andrenidae;
Hymenoptera
Megachilidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Megachilidae;
Hymenoptera
Andrenidae;
Hymenoptera
Ophrys atlantica Munby
Andrena nigroaenea (Kirby)
Ophrys attica Boiss. &

Orph.
Ophrys aurelia P.Delforge,
Devillers-Tersch. &
Devillers
Ophrys aveyronensis
(J.J.Wood) H.Baumann
& Kunkele
Ophrys aymoninii (Breistr.)
Buttler
Ophrys balearica P.Delforge
Andrenidae;
Hymenoptera
Megachilidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Megachilidae;
Hymenoptera
Melecta albifrons subsp.

albovaria
(Geoffr.)
Eucera seminuda Brulle
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Anthophora plagiata (Illiger)
Ophrys argolica H.Fleischm.

ex Vierh.
Ophrys ariadnae H.F.Paulus
(as O. cretica subsp.
karpathensis E.Nelson*)
Ophrys arnoldii P.Delforge
Schiestl & Ayasse (2002);

Delforge (2005); Stokl et al.
(2005)
(2005)
Delforge (2005)

(2005)
Paulus (2000, 2006); Delforge

(2005)

(2005); Paulus (2006)
Delforge (2005)

(2005)
Delforge (2005)

(2005)

(2005); Paulus (2006)
(2005)
Delforge (2005)

(2005); Paulus (2006)
(2005)*

49
Ophrys crabronifera Sebast.

& Mauri
Ophrys creberrima Paulus (as
Ophrys fusca (small)?*)
Ophrys cinereophila Paulus &

Gack
Ophrys cornutula Paulus
Ophrys bornmuelleri
M.Schulze
Ophrys bucephala Golz &
H.R.Reinhard
Ophrys calocaerina
Devillers-Tersch. &
Devillers
Ophrys calypsus M.Hirth &
H.Spaethe
Ophrys candica Greuter,
Matthas & Risse
Ophrys celiensis (O.Danesch
& E.Danesch)
P.Delforge
Ophrys cerastes Devillers &
Devillers-Tersch. (as
Ophrys cornuta (small)?*)
Ophrys ceto P. Devillers,
Devillers-Tersch. &
P.Delforge
Ophrys chestermanii (J.J.
Wood) Golz &
H.R.Reinhard
Ophrys cilentana
Devillers-Tersch. &
Devillers
Ophrys cilicica Schltr.
Ophrys blitopertha Paulus &

Gack
Ophrys bombyliflora Link
Orchid
Table 1. (Cont.)
Andrena labialis (Kirby)?

Eucera dalmatica Lep.
Andrena creberrima Perez* ,

A. flavipes Panzer*
Sphecidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Argogorytes sp.
Eucera punctulata Alfken,

E. signifera
Anthophora plumipes (Pallas)
Andrenidae;
Hymenoptera
Andrena florentina Magretti
Apidae;
Hymenoptera
Bombus vestalis (Geoffr.)
Andrena cinereophila War.
Anthophoridae;
Hymenoptera
Eucera euroa Tkalcu?,

E. plumigera?
Anthophoridae;
Hymenoptera
Eucera puncticollis Mor.?
Anthophoridae;
Hymenoptera
Eucera hispana Lep.*,
Anthophoridae;
E. hispana Lep.
Hymenoptera
Eucera graeca Radoszkowski Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Eucera paulusi Tkalcu*,

E. penicillata Risch
Eucera curvitarsis Mocz.
Scarabaeidae;
Coleoptera
Anthophoridae;
Hymenoptera
Pollinator
Family; Order
Blitopertha lineolata (Fischer

von Waldheim)
Eucera oraniensis Lep. ,
E. algira Brulle ,
Eucera sp.

(2005)
Paulus & Gack (1990); Paulus

(2006)
Paulus (2001, 2009); Delforge
(2005)
Delforge (2005)
Delforge (2005)
Delforge (2005); Gogler et al.

(2009)
Delforge (2005)

(2005)
Delforge (2005)
2
2
Delforge (2005)
Kullenberg & Bergstrom (1976a,

b); Paulus & Gack (1990) ;
Neiland & Wilcock (1998)*;
Paulus (2000)
(2005)
(2005)
Delforge (2005)
Source
Paulus (2001); Delforge (2005)
% plants
pollinated (N )
2
21.3 (122 on 37
plants)*

behaviour
pollinated (N )
50
A. C. Gaskett
Anthophora plagiata (Illiger)

Eucera euroa Tkalcu
Chalicodoma albonotata
(Radoszkowski)
Anthophora atroalba Lep.
Tetralonia salicariae (Lep.)
Anthophora erschowi
Fedtschenko
Andrena morio Brulle
Eucera ( prev. Synhalonia)
Dusmet)*, inaccurate
according to (Delforge,
2005)
Ophrys dyris Maire
Ophrys elatior Gumpr. ex.

Paulus
Ophrys elegans (Renz)
H.Baumann & Kunkele
Ophrys eleonorae
Devillers-Tersch. &
Devillers
Ophrys episcopalis Poir (as
O. episcopalis (maxima))
(Geoffr.)
Chalicodoma manicata
(Giraud)
Eucera dimidiata Brulle
Ophrys flavicans Vis.
Ophrys flavomarginata (Renz)

H. Baumann &
Kunkele
Ophrys fleischmannii Hayek
Anthophora sicheli
Radoszkowski
Andrena fabrella Perez
Ophrys explanata (Lojac.)

P. Delforge
Ophrys fabrella Paulus &
Ayasse ex P. Delforge
Ophrys ferrum-equinum Desf.
Ophrys exaltata Ten.
Andrena vachali subsp.

creticola
Melecta tuberculata Lieftinck
Andrena merula War.?
Ophrys cretensis (Baumann

& Kunkele) Paulus
Ophrys cretica (Vierh.)
E.Nelson
Ophrys delphinensis
O.Danesch &
E.Danesch (pro hybr.)
Ophrys discors Bianca (syn.
O. todaris)
Ophrys drumana P.Delforge
Ophrys cressa Paulus
Anthophoridae;
Hymenoptera
Colletidae;
Hymenoptera
Megachilidae;
Hymenoptera
Andrenidae;
Hymenoptera
Megachilidae;
Hymenoptera
Megachilidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Apidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Megachilidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Apidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera

(2005)

(2001, 2009); Delforge (2005)
Delforge (2005)
Delforge (2005)

(2005); Mant et al. (2005b)
Delforge (2005)
Paulus & Gack (1990)*
Delforge (2005)

(2000); Delforge (2005)

(2005)
Delforge (2005)

(2005)
(2001); Delforge (2005)
(2005)
Delforge (2005)

51
Ophrys fusca (type II Sicily)
Ophrys fusca (type III Sicily)
Ophrys cf. fusca (Ophrys

sulcata Devillers &
Devillers-Tersch.)
Ophrys gackiae P.Delforge
Ophrys grigoriana
G.Kretzschmar &
H.Kretzschmar
Ophrys hebes (Kalopissis)
E.Willing & B.Willing
Ophrys gracilis (Buel &

Danesch) P.Englmaier
Ophrys grammica (B.Willing
& E.Willing)
Devillers-Tersch. &
Devillers (as O. herae*,
according to Paulus
(2006)
Ophrys grandiflora Ten.
Ophrys garganica E.Nelson

ex O.Danesch &
E.Danesch
Ophrys gazella
Devillers-Tersch. &
Devillers
Ophrys gottfriediana Renz
Ophrys fusca Link
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Eucera clypeata Erichson?

Andrena nigroaena (Kirby)
Eucera algira Brulle?

Xylocopa violacea (L.)
Andrena symphiti
Schmiedeknecht
Megachilidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Chalicodoma sp.
Andrenidae;
Hymenoptera
Andrena florentina Magretti? Andrenidae;

Hymenoptera
Andrena carbonaria (L.)
Andrenidae;
Hymenoptera
Eucera nigrescens Perez*, E. Anthophoridae;

longicornis (L.)*, Microdon
Hymenoptera
latifrons Loew*, M.
Scarabaeidae;
mutabilis (L.)*,
Coleoptera
Phyllopertha horticola (L.)
Andrena nigroaenea (Kirby), Andrenidae,
Colletidae;
Hymenoptera
Andrena thoracica Fabricius, Andrenidae;
A. florentina Magretti
Hymenoptera
Andrena sabulosa subsp.
Andrenidae;
trimerana
Hymenoptera
Andrena wilkella (Kirbyi)
Andrenidae;
Hymenoptera
Pollinator
Family; Order
Ophrys fuciflora
(F.W.Schmidt) Moench
Orchid
Table 1. (Cont.)
5.45 (463
plants)

behaviour
pollinated (N )
% plants
pollinated (N )

(2005)
Paulus (2006)
Delforge (2005)
Delforge (2005)*; Stokl et al.

(2005)*
Delforge (2005)
Paulus (2006)
Delforge (2005)
Delforge (2005)
Paulus (2000)
Paulus & Gack (1990); Schiestl &

Ayasse (2002); Delforge
(2005); Stokl et al. (2005)

b); Delforge (2005)*; Tyteca
et al. (2006) ; Vanderwoestijne
et al. (2009)
Source
52
A. C. Gaskett
Andrena thoracica (Fabricius)

Eucera cypria Alfken
Ophrys helios Kreutz
Ophrys herae M.Hirth &

H.Spaeth
Ophrys heterochila (Renz &
Taubenheim)
P.Delforge
Ophrys holoserica
(N.L.Burm.)
Ophrys integra (Moggr. &

Rchb.f.) Paulus & Gack
Ophrys iricolor Desf.
Ophrys laurensis Geniez &

Melki
Ophrys lesbis Golz &
H.R.Reinhard
Ophrys israelitica
H.Baumann & Kunkele
Ophrys kotschyi H.Fleischm.
& Soo
Ophrys lacaitae Lojac.
Ophrys insectifera L.
Andrena curiosa (Morawitz)
Eucera eucnemidea Dours
T
Andrena schulzi Strand
Melecta tuberculata Lieftinck
Argogorytes fargeii
(Shuckard), A. mystaceus
(L.), Anthobium minutum
F. (Staphylinidae)
Ophrys incubacea Bianca ex.

Tod.
Eucera &Tetralonia sp.*,

Eucera clypeata
Erichson , E. longicornis
(L.) , and rarely
Phyllopertha horticola (L.)
& Microdon sp.
Eucera (Synhalonia) cressa?
Ophrys helenae Renz
Eucera (prev. Synhalonia)

Dusmet) , Tetralonia
alternans ( Brulle)
Eucera longicornis (L.)?
Ophrys heldreichii Schltr.
Andrenidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Colletidae;
Hymenoptera
Andrenidae;
Hymenoptera
Sphecidae;
Hymenoptera,
Staphylinidae;
Coleoptera
Anthophoridae;
Hymenoptera,
Scarabaeidae;
Coleoptera
Syrphidae;
Diptera
Andrenidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Apidae;
Hymenoptera
15.1 (2775
plants)*

(2005)

(2001); Delforge (2005); Stokl
et al. (2007); Cortis et al. (2009)
Paulus & Gack (1990); Stokl et al.
(2005)
(2005)
(2005)
Delforge (2005)

(2000); Delforge (2005); Cortis
et al. (2009)
Darwin (1885)*; Wolff (1950)*;
Kullenberg (1961); Kullenberg
& Bergstrom (1976a, b) ;
Agren
& Borg-Karlson (1984);
Delforge (2005);
Vanderwoestijne et al. (2009)*
Paulus & Gack (1990)*; Paulus

(2000 , 2006 )

(2001); Delforge (2005)
Paulus (2006)
Delforge (2005)
Delforge (2005)
Paulus & Gack (1990) ; Delforge

(2005)*; Spaethe et al. (2007)*;
Streinzer et al. (2009)*

53
Ophrys marmorata
G.Foelsche &
W.Foelsche
Ophrys massiliensis Viglione
& Vela
Ophrys melitensis (Salk.)
Devillers-Tersch. &
Devillers
Ophrys lutea subsp. melena

Renz)
Ophrys lyciensis Paulus,
Gugel, D.Ruckbr. &
U.Ruckbr.
Ophrys mammosa Desf.
Ophrys lupercalis
Devillers-Tersch. &
Devillers
Ophrys lutea Cav.
Ophrys lucis (Kalteisen &

H.R.Reinhard) Paulus
& Gack
Ophrys lunulata Parl.
Ophrys lucana P.Delforge,

Devillers-Tersch. &
Devillers
Ophrys lucentina P.Delforge
Ophrys leucadica Renz (pro

hybr.)
Ophrys lojaconoi P.Delforge
Orchid
Table 1. (Cont.)
Megachilidae;
Hymenoptera
Colletidae,
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Osmia kohlii Ducke
Andrena cinerea Brulle ,

A. senecionis Perez ,
A. clypella Strand,
A. hasitata, A. nigroolivacea
Dours ?,
S. panurgimorpha
Mavromoustakis ,
A. humilis Imhoff ,
A. humilis subsp.
prunella*, A.cinerophila
War.
Andrena transitoria
Andrenidae;
Morawitz
Hymenoptera
Eucera graeca Radoszkowski Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Megachilidae;
Hymenoptera
Andrena wilkella (Kirby)

Andrena bicolor Fabricius
Andrena fuscosa Erichson
Andrenidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrena flavipes
A. Andrenidae;
creberrima Perez ?
Hymenoptera
Andrena ocreata (Christ)?
Andrenidae;
Hymenoptera
Andrena labialis (Kirby)
Andrenidae;
Hymenoptera
Panzer* ,
Pollinator
Family; Order
Andrena vulpecula
Kriechbaumer
Anthophora cf. mucida

behaviour
pollinated (N )
% plants
pollinated (N )
Delforge (2005)
Vereecken & Patiny (2006)

(2005)
Paulus,Gugel, Ruckbrodt &
Ruckbrodt (2001); Delforge
(2005)
(2005)
Delforge (2005)

b); Borg-Karlson & Tengo
(1986); Paulus & Gack (1990)*;
Bournerias & Prat (2005);
Delforge (2005)

(2005)
Delforge (2005)
Delforge (2005)
Delforge (2005)
Delforge (2005)
Paulus (2001)*; Delforge (2005)
Source
54
A. C. Gaskett
Andrenidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Colletidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Apidae;
Hymenoptera
Andrenidae;
Hymenoptera
Anthophoridae;
Hymenoptera

Anthophora sicheli
Radoszkowski
Colletes sp.
Eucera clypeata Erichson,
E. oraniensis Lep.?
Bombus vestalis (Geoffr.)
Ophrys panormitana var.

praecox (Corrias)
P.Delforge
Ophrys parvimaculata
(O.Danesch &
E.Danesch) Paulus &
Gack
Andrena thoracica
(Fabricius)* , A. florentina
Magretti*, A. sabulosa
(Scopoli) , A. sabulosa
subsp. trimerana*
Andrena thoracica
(Fabricius), A. nigroaenea
(Kirby)?
Eucera nigrescens Perez
Ophrys panattensis Scrugli,

Pessei & Cogoni (pro
hybr.)
Ophrys panormitana (Tod.)
Soo
Andrena orbitalis Morawitz
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Osmia rufa subsp. rufa
Ophrys pallida Raf.
Anthophora atroalba subsp.

atroalba
Andrena hypopolia
Smiedeknecht
Eucera graeca Radoszkowski
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Megachilidae;
Hymenoptera
Anthophora atroalba subsp.

agamoides, A. nigriceps
Mor.
Colletidae;
Hymenoptera
Ophrys omegaifera
H.Fleischm. (as O.
omegifera subsp. omegaifera
in Paulus & Gack 1990)
Ophrys omegaifera subsp.
dyris (Maire) Del Prete
Ophrys ortuabis M.P.Grasso
& Manca
Ophrys oxyrrhynchos Tod.
Ophrys normanii J.J.Wood

(pro hybr.)
Ophrys obaesa Lojac.
Ophrys montis-leonis
O.Danesch &
E.Danesch (pro hybr.)
Ophrys morio Paulus &
Kreutz
Ophrys morisii (Martelli)
G.Keller & Soo
Ophrys murbeckii
H.Fleischm.
Ophrys neglecta Parl.

(2005)
Delforge (2005)

(2005)

(2005)

(2006)
Delforge (2005)
Delforge (2005); Gogler et al.

(2009)
(2005)
(2005)
Delforge (2005)
Paulus (2006)
Delforge (2005)
Delforge (2005)

55
Andrena panurgimorpha
Mavromoustakis,
A. humilis Imhoff,
A. tadauchii
Gusenleitner, A. clypella
subsp. hasiata?
Eucera barbiventris Perez
Ophrys passionis var.

garganica (E.Nelson ex.
O.Danesch & E.
Danesch) P.Delforge
Ophrys phryganae
Devillers-Tersch. &
Devillers
Chalicodoma albonotata
(Radoszkoski)
Eucera longicornis (L.)*,
Eucera nigrescens Perez*,
E. interrupta Baer*,
E. (Hetereucera) elongatula
Vachal
Eucera clypeata Erichson
Andrena hesperia Sm.* ,
A. vulpecula
Kriechbaumer* ,
A. merula War. ,
A. taraxaci Giraud ,
A. bicolor Fabricius ?
Ophrys serotina H.Rolli ex

H.F. Paulus
Ophrys sicula Tineo (as O.
sicula (minor)*)
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Megachilidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Melecta sp.*, Anthophora

obscura , Eupavlovskia
obscura Friese , E.
funeraria Sm.?
Andrena sabulosa (Scopoli)
Anthophoridae;
Hymenoptera
Anthophora atriceps Perez
Ophrys sabulosa Paulus &

Gack ex P.Delforge
Ophrys saratoi E.G.Camus
(pro hybr.)
Ophrys scolopax Cav.
Anthophoridae;
Hymenoptera
Osmia mustelina
Gerstaecker
Ophrys promontorii
O.Danesch &
E.Danesch
Ophrys provincialis
(Baumann & Kunkele)
Paulus
Ophrys reinholdii Spruner
ex. Boiss.
Anthophoridae;
Hymenoptera
Megachilidae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Pollinator
Family; Order
Ophrys picta Link
Ophrys passionis Sennen
Andrena tomora War.
Ophrys parvula Paulus
Orchid
Table 1. (Cont.)

behaviour
pollinated (N )
% plants
pollinated (N )

(2001) ; Delforge (2005)
Paulus (2000)

b)*; Paulus & Gack (1990)*;
Delforge (2005)*; Vereecken
et al. (2007)
Delforge (2005)
Kullenberg & Bergstrom, (1976a,

b)*; Paulus & Gack (1990) ;
Paulus (2001) ; Delforge
(2005)
Delforge (2005)

(2005)
Delforge (2005)
Delforge (2005)
Delforge (2005)
Delforge (2005)
Paulus (2001): Delforge (2005)
Source
56
A. C. Gaskett
Andrena squalida Olivier

Xylocopa iris (Christ)
Ophrys splendida Golz &

H.R.Reinhard
Ophrys spruneri Nyman
Osmia tricornis Latreille

Andrena tibialis (Kirby)
Ophrys tenthredinifera Willd.
Eucera nigrilabris Lep.

E. dimidiata Brulle,
E. clypeata Erichson,
E. algira Brulle?
Andrena flavipes Panzer,

A. ovulata (Kirby),
A. wilkella (Kirby)
Eucera taurica Morawitz?
Sterictiphora furcata (Villers)
Ophrys subinsectifera
C.E.Hermos. &
J.Sabando
Ophrys sulcata
Devillers-Tersch. &
Devillers
Ophrys tardans O.Danesch
& E.Danesch (pro
hybr.)
Ophrys tarentina Golz &
H.R.Reinhard
Ophrys tarquinia P.Delforge
Andrena nigroaenea
(Kirby)* , A. barbilabris
(Kirby)*, A. thoracica
(Fabricius)*, A. cineraria
(L.)*, A. limata
Eversmann*
Ophrys sphegodes Mill.
Megachilidae;
Hymenoptera
Andrenidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Andrenidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Argidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Eucera notata Lep.
Dasyscolia ciliata (Fabricius)

(as Campsoscolia ciliata)
Dasyscolia ciliata subsp.
araratensis
Scoliidae;
Hymenoptera
Scoliidae;
Hymenoptera
Anthophoridae;
Hymenoptera
Andrenidae;
Hymenoptera
Xylocopa iris (Christ)
Ophrys speculum subsp.

orientalis (Paulus) Paulus
& Salkowski
Ophrys sphegifera Willd.
Ophrys sipontensis R.Lorenz

& Gembardt
Ophrys sitiaca Paulus,
C.Alibertis &
A.Alibertis
Ophrys speculum Link
55.5 (20 on 13
plants)*
0.03 (3000)
12.9 (963)*
17.04 (235
plants)
Paulus & Gack (1990); Neiland &

Wilcock (1998)*; Paulus
(2000) ; Bournerias & Prat
(2005); Delforge (2005)

(2005)
Delforge (2005)
Delforge (2005)
Delforge (2005)
Delpino (in Darwin (1885) as

O. aranifera Huds.) ; Paulus &
Gack (1990); Ayasse et al.
(1997)*; Neiland & Wilcock
(1998)*; Bournerias & Prat
(2005); Delforge (2005);
Vanderwoestjine et al. (2009)
(2005)
(2005)
Delforge (2005); Tyteca et al.
(2006)
Delforge (2005)

b); Ayasse et al. (2003)
Paulus (2009)
Paulus & Gack (1990); Widmer

et al. (2000)
(2005); Stokl et al. (2005)

57
Ophrys thriptiensis Paulus
Ophrys tommasinii Visiani
Ophrys transhyrcana
Czerniak.
Ophrys umbilicata Desf.
Ophrys vernixia Brot.
Ophrys villosa Desf. (various

forms)
Ophrys zonata
Devillers-Tersch. &
Devillers
Orchis galilaea (Bornmuller
et Schultze) Schlechter
Ophrys untchjii (M.Schulze)

P.Delforge
Ophrys urteae H.F.Paulus
Pollinator
Family; Order
Lassioglossum marginatum
Brulle (prev. Halictus
(Evylaeus) marginatus)
Halictidae;
Hymenoptera
Apidae;
Tetraloniella fulvescens
Hymenoptera
(Giraud) (prev.
Tetralonia f.)*, Eucera
fulvescens Giraud , Eucera
inulae , but reports of
Tetralonia ruficornis
(Fabricius) are
inaccurate .
Andrena bicolor Fabricius?
Andrenidae;
Hymenoptera
Andrena pandellei Perez
Andrenidae;
Hymenoptera
Andrena morio Brulle*,
Andrenidae;
A. fuscosa Erichson ?
Hymenoptera
Eucera gaullei Vachal,
Anthophoridae;
E. galilaea Tkalcu,
Hymenoptera
E. spatulata Gribodo,
E. seminuda Brulle,
Eucera penicillata Risch
Eucera clypeata Erichson
Anthophoridae;
Hymenoptera
Scarabaeidae;
Blitopertha nigripennis
Reitter
Coleoptera
Dasyscolia ciliata (Fabricius) Scoliidae;
(as Campsoscolia ciliata)
Hymenoptera
Anthophoridae;
Eucera dimidiata Brulle,
Hymenoptera
E. bidentata Perez,
E. nigrilabris Lep.
E. rufitarsis Friese,
E. curvitarsis Mocsary?
Andrenidae;
Hymenoptera
Ophrys tetraloniae
W.P.Teschner
Orchid
Table 1. (Cont.)
7.6 (475 on 105

plants)*
27.5 (2146 on
129 plants)*
Bino et al. (1982)*; Delforge

(2005)
Delforge (2005)
Paulus & Gack (1990); Neiland &

Wilcock (1998)*
Delforge (2005)
Paulus (2009)

(2005)
(2005) ; Paulus (2009)
Paulus (2000)
Delforge (2005)

(2000) ; Delforge (2005)
Source
Delforge (2005)
% plants
pollinated (N )

behaviour
pollinated (N )
58
A. C. Gaskett
Fig. 1. Sexually deceptive tongue orchids, Cryptostylis species,

are remarkably morphologically disparate, yet share a single
pollinator, males of the parasitoid wasp Lissopimpla excelsa
(Ichneumonidae). (A) Cryptostylis subulata, (B) C. leptochila, (C) C.
erecta, and (D) C. hunteriana labelled to show the large labellum
and reduced petals and sepals typical of this genus. C. erecta
image by Julia Cooke.
species may also pollinate more than one sexually deceptive

orchid species in different regions (see Table 1 for repeated
pollinator species). Avoidance of cross-pollination (prepollination or pre-zygotic isolation) is generally achieved
via differences in scent compounds or odour blends (e.g.
Mant et al., 2002; Schiestl & Ayasse, 2002). Less commonly,
hybridisation is prevented by differences in pollinator flight
and flowering times, floral height, or the location of pollinia
attachment on the pollinating insect (Schiestl & Peakall, 2005;
Paulus, 2006; Bower & Brown, 2009). Sympatric species of
sexually deceptive orchids rarely share a pollinator and correspondingly, post-pollination or post-zygotic isolation factors
are weak or uncommon (Scopece et al., 2007; Cozzolino &
Scopece, 2008). However, post-pollination isolation factors
have been suggested for two pairs of sympatric Ophrys species
from Sardinia: Ophrys chestermanii and O. normanii are genetically distinct, but similarly scented and share their pollinator,
male Bombus vestalis (Gogler et al., 2009), and Ophrys iricolor
and O. incubacea are natural hybrids that are also similarly
scented and share their pollinator, male Andrena morio (Cortis
59
Fig. 2. In many Australian orchid species, the labellum is

attached by a flexible hinge. When a pollinator grips the
labellum, he is flung into the stigma and pollinia. Examples of
orchids with hinged labellae are (A) Paracaleana nigrita (B) Drakaea
glyptodon, (C) Caleana major, and (D) Caladenia cairnsiana. In
Pterostylis species, the petals are folded into a hood and a
sensitive labellum can act as a trap door and detain pollinators
briefly within the hood. (E) Pterostylis (syn. Diplodium) grandiflorum.
Most photographs by Julia Cooke.
et al., 2009). Post-pollination isolation is also confirmed for

four Australian sexually deceptive Cryptostylis species that
are often sympatric and share their single pollinator (male
Lissopimpla excelsa; Ichneumonidae), but do not hybridise in
nature or when cross-pollinated by hand (Dacy, 1974; Jones,
1988; Backhouse & Jeanes, 1995). Cryptostylis species differ in
chromosome numbers, a common mechanism of incompatibility in food-deceptive orchid species (Dawson, Molloy &
Beuzenberg, 2007; Cozzolino & Scopece, 2008).
(1) Pollinator identities
Although some rewarding orchid species are pollinated by
birds (Singer & Sazima, 2000; Johnson & Brown, 2004;
Micheneau, Fournel & Pailler, 2006), no other vertebrates
such as rodents or bats are reported as orchid pollinators,
and only insects are involved in sexually deceptive pollination (Table 1). The typical pollinator of a sexually deceptive
orchid is male, an insect, and solitary rather than social
(Gaskett, Winnick & Herberstein, 2008; see Table 1 for
pollinator species, families and orders). The few reports
of female insects visiting orchids in potentially sexually
A. C. Gaskett
60
deceptive pollination systems require further substantiation.
For example, early reports of pollination of Pterostylis orchids
by female mosquitoes (Coleman, 1934; Table 1) are drawn
from a single observation and it is unclear whether pollination
involved any sexual behaviour.
Solitary and parasitoid wasps are the most common
pollinators of sexually deceptive orchids (Table 1). Such
specialised pollination by wasps is rare in almost all other
groups of flowering plants, except figs (Johnson, 2005). Thynnine, ichneumonid and scoliid wasps pollinate species from
most Australian sexually deceptive orchid genera, and sphecid and pompilid wasps pollinate both South African Disa
species (Table 1). European Ophrys species are predominantly
pollinated by solitary bees in the families Andrenidae, Colletidae, Megachilidae, and Apidae (but see Section III.3, and
families of pollinators listed in Table 1).
(2) Pollinator mating systems and traits
The mating systems of solitary wasps and bees have several
features that may facilitate or pre-adapt them to exploitation by sexually deceptive orchids. These features could
include: male attraction to airborne sex signals (allowing
signal mimicry and long-distance attraction by orchids),
intense male searching and vigilance for sex signals (encouraging rapid response to orchids), vigorous mating behaviour
(ensuring pollinia transfer between the orchid and pollinator), and polygyny (ensuring a pollinator visits more than one
orchid, permitting both pollinia collection and delivery). Correspondingly, male hymenoptera from solitary species are
typically strongly attracted to the airborne sex pheromones
of female conspecifics (Ridley, 1993; Godfray & Cook, 1997).
Male bees and wasps are also generally highly vigilant and
respond quickly to female pheromones. Female monandry
or first-male sperm precedence imposes strong selection on
these males to secure paternity by rapidly finding and mating
with virgin females (Alcock et al., 1978; Eickwort & Ginsberg,
1980; Tengo, Eriksson & Borg-Karlson, 1989; Hardy, 1994;
El Agoze, Poirie & Periquet, 1995; Paxton, 2005; Damiens &
Boivin, 2006). For example, the solitary bee Colletes cunicularius is the sole or major pollinator for at least six Ophrys species
(Table 1) and has many characteristics lending it to orchid
exploitation. Colletes cunicularius is relatively common, the
females are monandrous, attract mates with sex pheromones
and do not exhibit any courtship behaviour, and the males
are polygynous (Larsson, 1991). Consequently, there is considerable competition between male Colletes cunicularius to
detect virgin female pheromones quickly and to mate first
with many females (Cane & Tengo, 1988; Mant et al., 2005b).
Male thynnine wasps (family Tiphiidae, subfamily Thynninae), which are common pollinators of Australian sexually
deceptive orchids, have many similar mate-searching and
mating behaviours (Burrell, 1935; Alcock, 1981). Therefore,
orchids that mimic the sex pheromones of females of these
insect taxa benefit from the males rapid response to scent
and enthusiastic and somewhat indiscriminate mating.
Haplodiploid insects are surprisingly common pollinators of sexually deceptive orchids (Gaskett et al., 2008). Many
diploid insect orders that are diverse, abundant, and common

pollinators for rewarding orchids and other plants are either
conspicuously absent (Hemiptera, Lepidoptera, Orthoptera)
or scarce (Coleoptera, Diptera) in the pollination of sexually
deceptive orchids (see Tables 1 and 2 for pollinator types).
This may reflect current knowledge (for example, in the
future more dipteran pollinators of sexually deceptive Lepanthes species are likely to be discovered), but haplodiploidy
may also provide some advantageous features that facilitate
the maintenance of sexual deception. In haplodiploid insect
species, fertilised eggs become female offspring and unfertilised eggs become male offspring (King, 1987; Hardy, 1994;
Heimpel & de Boer, 2008). Therefore, female haplodiploid
insects deprived of matings (because male insects are mating
with orchids) can still reproduce, although all their offspring
must be sons. In this manner, haplodiploidy could moderate orchid interference in pollinator reproduction, and even
generate extra males to act as pollinators (Gaskett et al.,
2008). A further consequence of haplodiploidy is that selection imposed on male insects by orchids cannot be inherited
directly by their sons because any eggs fertilised by a males
sperm always become daughters. Selection on a male must
therefore always operate indirectly via his daughters and
then on her sons, effectively doubling the intergenerational
delay in any response to orchid exploitation. However, indirect selection in any solitary hymenoptera appears largely
unstudied and research into this topic using the pollinators of sexually deceptive orchids would make a significant
contribution to general understanding of haplodiploidy and
indirect selection.
(3) Exceptions to the general types of pollinators
Not all pollinators of sexually deceptive orchids are solitary, haplodiploid hymenoptera. For example male social
bees pollinate South American Trigonidium obtusum and Mormolyca ringens, and European Orchis galilea (Bino et al., 1982;
Singer, 2002; Singer et al., 2004). Male social ants pollinate
Australian Leporella fimbriata, however no social interactions
are observed between these males (Peakall, 1989). Diploid
flies (Diptera) pollinate Central American genera, and the
incidence of fly pollination is almost certain to increase as
further studies are undertaken on orchids from this region
(Calvo, 1990; Christensen, 1994; van der Cingel, 2001;
Blanco & Barboza, 2005). A hoverfly (Syrphidae; Diptera)
is an occasional pollinator of European Ophrys holoserica, a
species primarily pollinated by anthophorid bees (Table 1;
Paulus, 2006). Many Australian and New Zealand members of Pterostylis and synonymous genera are also potentially
pollinated by diploid diptera, principally flies and fungus
gnats (Christensen, 1994; Table 1). However, the extent of
sexual deception in Pterostylis is unclear (see Section IV.3).
Sexual deception of diploid beetle pollinators (Coleoptera)
is documented for Ophrys blithopertha, Ophrys fuciflora, and
Ophrys urteae, and is occasionally observed for Ophrys holoserica
(Delforge, 2005; Paulus, 2006; Tyteca, Rois & Vereecken,
2006; Paulus, 2009).
Watsonia densiflora s.l. Baker

(Iridaceae)
Zaluzianskya microsiphon (Kuntze)

K. Schum. (Scrophulariaceae)
Watsonia lepida N.E. Brown

(Iridaceae)
Disa nervosa Lindl.
Disa nivea H.P.Linder
Disa pulchra Sond.
Gompholobium huegelii Bentham

(Fabaceae)
Daviesia ulicifolia Andrews ssp.
ulicifolia, plus other related
legumes (Fabaceae)
Bellevalia flexuosa Boiss. (Liliaceae)
Campanula spp. (Campanulaceae)
Diuris maculata Smith
Orchideae
Orchis israelitica
H. Baumann & Dafni
Neottieae
Cephalanthera rubra
(L.) Rich.
Diurideae
Diuris aequalis Fitzg.
Tritoniopsis triticea (Burm. F.)

Goldbl. (Iridaceae) or Kniphofia
uvaria (L.) Hook
(Asphodelaceae)
Scabiosa columbaria L.
(Dipsacaceae)
Rewarding model
Disa ferruginea (Thunb.) Sw.
Diseae
Disa cephalotes Rchb.f. ssp.
cephalotes
Orchid species
Solitary bees
Chelostoma fuliginosum Panzer,
C. campanularum (Kirby)
(Megachilidae)
Solitary bees
Anthophora sp., Eucera clypeata
Erichson (Anthophoridae),
Bombylius sp. (Bombyliidae)
Male solitary bees Trichocolletes

venustus (Smith) (Colletidae)
Long-proboscid fly Prosoeca

ganglbaueri Lichtwardt
(Nemestrinidae)
Long-proboscid fly Philoliche
aethiopica (Thunberg)
(Tabanidae)
Long-proboscid fly Philoliche

aethiopica Thunberg
(Tabanidae)
Butterfly Meneris tulbaghia L.

(Nymphalidae)
Long-proboscid flies (Tabanidae,

Nemestrinidae)
Pollinator
8.5% fruits per flower

(N = 200)
with model sp. 48.6% of

flowers set fruit
(N = 692), without
model sp. 3.75%
(N = 428)
17% of flowers set fruit

(N = 122); 59% of
plants set fruit (N = 29)
15.7% fruit set per plant

(N = 17)
flowers: 13.9% pollinia

removed, 21.2%
pollinia deposited
(N = 37)
with model sp.: 69.5% of
flowers set fruit
(N = 600), without
model sp: 28%
(N = 852)
24.9% of flowers
pollinated (N = 95);
41.3% fruit set per
plant (N = 28)
92.5% of flowers set fruit
(N = 890)
Orchid mean Pollination success
Nilsson (1983)
Dafni & Ivri (1981); Galizia et al.

(2005)
Indsto et al. (2006)
Indsto et al. (2006)
Johnson (2000)
Anderson, Johnson & Carbutt

(2005)
Johnson & Morita (2006)
Johnson (1994)
Johnson et al. (2003)
Source
Table 2. Food-deceptive or unrewarding orchid species tested for similarity in colour with co-occurring plant species that do provide nectar rewards for their pollinators.
Pollination success for each orchid species is the average of values reported in the source. N = sum of sample sizes reported in source

61
A. C. Gaskett
62
IV. POLLINATOR BEHAVIOURS
(1) Pollinator behaviour and the origins of sexual
deception
Although pollination by sexual deception is confirmed only
for orchids, Kullenberg (1961) reported sexual behaviour by
a sphecid wasp on flowers of Guiera senegalensis Lam. (Combretaceae), and sexual deception is a compelling explanation
for the nectarless and insectiform flowers of Gilliesia graminea
Lindl. (Alliaceae; Rudall et al., 2002). These cases are yet
to be confirmed. Despite the prevalence of sexual deception amongst orchids, pollination involving some form of
insect sexual behaviour may actually precede the evolution
of orchids. Early floral scents that evolved initially to protect
plant reproductive organs from insect herbivory are likely to
have resembled the sex pheromones of other insects (Pellmyr
& Thien, 1986; Harrewijn, Minks & Mollema, 1994; Gang,
2005). Consequently, insects were likely to aggregate and
mate on the flowers and coincidentally function as pollinators. For many modern insect species, plant and floral scents
still enhance insect sex pheromone release and attractiveness
(for a review, see Reddy & Guerrero, 2004).
In orchids, phylogenetic comparisons suggest that sexual
deception evolved from food deception, which is common
amongst primitive, nectarless orchid groups, although some
of these orchids do provide pollen as a reward (Cozzolino
& Widmer, 2005). Surveying pollinator behaviour within
a genus could indicate how the transition between food
and sexual deception may occur, and whether elements of
both systems can coexist. For example, different species of
Australian Donkey orchids (genus Diuris) reward or deceive
foraging insects, and potentially, exploit aspects of pollinator
sexual behaviour. Diuris alba appears to be a rewarding
species; it provides nectar and has several pollinator species,
whereas Diuris aurea is food-deceptive and has several
pollinators (Indsto et al., 2007). Diuris pedunculata provides
nectar, but an early report suggests it is pollinated only by
male bees of Halictus lanuginosus, perhaps suggesting some sexbased pollination (Coleman, 1932). Another species, Diuris
maculata, has features associated with sexual deception, it lacks
nectar and is pollinated by male bees of Tricholetes venustus
(Indsto et al., 2006). However, detailed observations reveal
no sexual behaviour with orchid flowers (Indsto et al., 2006).
In the case of these last two species, Diuris pedunculata and
D. maculata, it seems likely that the orchids act as, or mimic,
both a foraging site and a rendezvous site for courting
males, although the lack of female visitors is inconsistent
with observations of other orchid species thought to mimic
rendezvous sites (Nilsson, 1983; Steiner, 1998; Jersakova
et al., 2006a). Other orchids proposed to employ aspects
of both pollinator foraging and sexual behaviour include
European Orchis galilaea (Bino et al., 1982) and Australian
Caladenia patersonii (Stoutamire, 1983), and possibly Japanese
Cymbidium pumilum (Sasaki et al., 1991). However, there is
scarce empirical evidence that any orchid species employs
both sexual and food deception (Faast et al., 2009). In
these putative cases, detailed observations are required to
confirm pollinator species and sex, and document any sexual

behaviour.
Phylogenetic analysis of Disa suggests multiple shifts
between pollinator types and gains and losses of nectar
rewards (Johnson et al., 1998). Similar phylogenetic analyses
tracing the evolution of sexual deception could be applied
to the Australian genus Caladenia, which has a diversity of
rewarding and food- and sexually deceptive pollination systems and considerable new data now available for analysis
(Stoutamire, 1983; Bates, 1984; Peakall & Beattie, 1996;
Hopper & Brown, 2004; Salzmann, Brown & Schiestl,
2006; Dixon & Tremblay, 2009; Dixon & Hopper, 2009;
Phillips et al., 2009a, b). Table 1 provides the known or putative pollinators for many sexually deceptive orchid species.
Lists of pollinators for food-deceptive and rewarding Caladenia species are available elsewhere (e.g. Brown et al., 1997;
Phillips et al., 2009a).
(2) Pollinator sexual behaviour with orchids
Sexually deceptive orchids elicit a range of sexual behaviours
from their pollinators. Pollinators of some orchid species do
indeed attempt to mate with the orchid, typically by grasping
the large central petal or labellum (Fig. 1; Kullenberg, 1961;
Paulus & Gack, 1990; Table 1). This copulatory behaviour
occurs for European Ophrys and Orchis species, Central American Lepanthes glicensteinii, South American Mormolyca ringens
and Geoblasta pennicillata, and Australian Calochilus campestris,
Leporella fimbriata, and Cryptostylis species (Coleman, 1928a,
1929, 1930; Fordham, 1946; Bino et al., 1982; Peakall, 1989;
Bower & Branwhite, 1993; Singer et al., 2004; Blanco &
Barboza, 2005; Ciotek et al., 2006). Pollination of Australian
Cryptostylis species even involves pollinator ejaculation. This
was first suspected by Coleman (1927, 1928a, b) whilst
observing pollinator behaviour on Cryptostylis leptochila, and
was recently confirmed using microscopy and sperm-staining
dye (Gaskett et al., 2008). Ejaculation during orchid pollination is also likely in Lepanthes glicenstenii because scanning
electron microscopy of flowers after pollinator visits revealed
putative spermatophores (Blanco & Barboza, 2005). There
is currently little evidence of pollinator ejaculation for any
other orchid species, but future studies are likely to generate
further examples, especially amongst lesser-known Lepanthes
and Cryptostylis species.
For most Australian sexually deceptive orchid species, successful pollination requires only pre-copulatory rather than
copulatory behaviour from the pollinator. When a male
insect grips or lifts the orchid labellum as if it was a female
insect, the labellum bends on a flexible hinge and presses the
duped insect into contact with the orchid stigma and pollinia
(Bower, 2001e; see Fig. 1D for orchid flower parts). This is
common for orchids from the diverse genera Caladenia and
Chiloglottis, the less speciose Arthrochilus, Caleana, Drakaea and
Paracaleana genera, and the single species from the genus Spiculaea (Fig. 2; Cady, 1965; Stoutamire, 1983; Peakall, 1990;
Peakall & Beattie, 1996; Alcock, 2000; Bower, 2001a, b, c,
e, f ; Jones et al., 2001; Hopper & Brown, 2006, 2007). In
some species, the sexual behaviour of the pollinator on the
63
orchid may trigger a floral trap. For example, pollinators

attempting copulation with Australian Duck orchids, e.g.
Caleana major (Fig. 2C) become briefly pinned upside-down
between an orchids hinged labellum and the column, which
bears the stigma and pollinia (Bower, 2001c). Male bees of
Plebeia droryana (Meliponinae) visiting South American Trigonidium obtusum (Maxillariinae) are also briefly trapped after
they attempt copulation with the sepals or petals and slip
on a waxy surface into a floral cavity (Singer, 2002). The
pollinator soon escapes via a hinged floral lip after brushing
past the stigma and pollinia.
1885; Sargent, 1909; Jones, 2001; Jones & Clements, 2003;

Lehnebach, Robertson & Hedderley, 2005). Although almost
all reported pollinators for Pterostylis spp. are male (Table 1),
confirming pollinator identity or sexual behaviour is challenging because pollination is rarely observed (see Table 1 for
pollination rates). There is some suggestion that the fungus
gnat pollinating Pterostylis gibbosa does attempt to mate with
the orchid labellum (National Parks and Wildlife Service,
2002), but much remains to be discovered about these enigmatic dipteran-orchid pollination relationships before sexual
deception can be substantiated.
(3) Sexual deception by Pterostylis
(4) Within-species variation in pollinator behaviour
Pterostylis and synonomous genera comprise a taxonomically

contentious complex of Australian and New Zealand terrestrial species (for proposed revisions and various names
see Table 1; Jones & Clements, 2003; Jones, 2006; Hopper,
2009). Many species in this group have a floral trap, although
entrapment does not appear to require copulatory behaviour
from the pollinator, unlike the traps described above for
Caleana and Trigonidium orchid species. When the potential
pollinator touches the sensitive labellum he is catapulted
into a curved hood formed by the dorsal sepal, and can
escape only via a narrow passage that forces contact with
the pollinia and stigma (Fig. 2E; Cheeseman, 1872; Sargent,
1909; Coleman, 1934; Christensen, 1994; Bernhardt, 1995).
Experiments suggest that labellae can be triggered up to three
times, and regain their position and sensitivity within 3h, or
longer in cool conditions (Sargent, 1909; Bernhardt, 1995).
It is important to note that the occurrence of sexual
deception in Pterostylis spp. is largely based on unpublished or
anecdotal evidence (often of considerable antiquity), and pollinator behaviour for most species in the group is completely
unstudied (Cheeseman, 1872; Thomson, 1878; Darwin,
Within a pollinator species, not all individuals that encounter

an orchid are fooled into actual pollination. Some individuals approach the orchid but then fly away without landing
or attempting sexual behaviour (Table 3). This variation
among individuals could be due to genetic differences in
learning ability (Dukas, 2008), or differing previous experience with orchids (Ayasse et al., 2000). However, prior
learning is not necessary to provoke this variability. When
orchids are experimentally moved within their pollinators
range to areas where they do not normally grow, pollinator
responses still vary even though all the insects attracted must
have no previous experience with sexually deceptive orchids
(Bower, 1996). There is probably individual variation in
insect sensory sensitivity or perception of orchid signals, and
in the quality or attractiveness of each orchid (Peakall, 1990).
Responses are also likely to be affected by spatial variation in
temperature and air currents, influencing the local dispersal
of orchid scent.
Data extracted from the literature suggest that the percentage of pollinators attracted and then actually fooled into
pollinating an orchid varies consistently among orchid species
Table 3. Percentages of insects fooled into pollinating some Australian sexually deceptive orchids after initial attraction. N = visits
observed. *Data combined & averaged from more than one study
% fooled
Orchid
Pollinator behaviour
Caladenia (syn. Arachnorchis) tentaculata

Chiloglottis diphylla
Chiloglottis (syn. Myrmechila) formicifera
Chiloglottis (syn. Myrmechila) platyptera
Chiloglottis (syn. Simpliglottis) pluricallata
Chiloglottis reflexa
Chiloglottis seminuda
Chiloglottis trilabra
Gripping hinged labellum

7.5
41.7
10.5
28.3
3.85
24.0
39.0
23.23
287
24
38
53
26
48
79
2897
Chiloglottis (syn. Simpliglottis) valida

Cryptostylis erecta

Copulation/ejaculation
13.0
90.99
46
111
Cryptostylis subulata
Copulation/ejaculation
92.73
55
Drakaea glyptodon
Leporella fimbriata
Spiculaea ciliata

Copulation
Copulation
21.9
60.0
44.0
618
55
50
Source
Peakall & Beattie (1996)
Bower (1996)
Bower (1996)
Bower (1996)
Bower (1996)
Bower (1996)
Bower (1996)
Peakall & Handel (1993);
Bower (1996)
Bower (1996)
Gaskett et al. (2008); A. C.
Gaskett (unpublished
data)
Gaskett et al. (2008); A. C.
Gaskett (unpublished
data)
Peakall (1990)
Peakall (1989)
Alcock (2000)
A. C. Gaskett
64
depending on the extent of pollinator sexual behaviour
elicited by each orchid (Table 3). If orchids are classified
according to the sexual behaviour stimulated from their pollinators, orchids causing more extreme behaviour have higher
pollination success (Gaskett et al., 2008). Analysis of data
presented in Tables 1 and 3 shows there is also a significant
correlation between the extent of pollinator sexual behaviour
and the percentage of attracted insects that are fooled into
pollination (partial correlation: 0.84, d.f. = 11, P < 0.001,
controlling for the number of pollinator visits observed).
Orchids stimulating the most extreme sexual behaviour are
the most likely to fool pollinators into making contact with
the orchid (Fig. 3), suggesting a strong fitness benefit for
orchids with persuasive mimicry and deceptive signalling. It
is worth noting that the data available in the literature may
overestimate pollinator response because it is impossible to
determine the number of insects that did detect an orchid,
but did not fly close enough to be counted by an observer.
V. POLLINATOR ABUNDANCE AND DIVERSITY

Insect abundance and diversity could be important factors
influencing the reproduction and fitness of sexually deceptive
orchids. Orchid pollination success can vary considerably
among years and determining lifetime success is difficult
given the potential longevity of individual plants and the
likelihood of vegetative or clonal reproduction (Neiland &
Wilcock, 1998; Tremblay et al., 2005). Although there are
some long-term demographic studies of sexually deceptive
orchids, actual pollination or seed set rates are not necessarily reported (e.g. Hutchings, 1987), and most long-term
Fig. 3. The relationship between the percentage of the insects

attracted to an orchid that are fooled into pollinating the flower
and the extent of pollinator sexual behaviour stimulated by the
orchid species.
studies focus on food-deceptive or rewarding orchid species

(e.g. Pfeifer, Heinrich & Jetschke, 2006; Zotz & Schmidt,
2006). When data for food and sexually deceptive orchids
are combined, the global averages calculated for the rates
of pollination or fruit set per flower are typically low and
approximately half that of rewarding or nectariferous species:
25% versus 52.9% (Neiland & Wilcock, 1998) or 20.7% versus 37.1% (Tremblay et al., 2005), respectively. In Australia,
sexually deceptive orchids have lower fruit-set per flower
than food-deceptive orchids (14% versus 36%; Phillips et al.,
2009a). Globally, the literature surveyed for Table 1 shows
that for sexually deceptive orchids, an average of 20.5
14.7% of all flowers (mean S.D., N = 35 species), or
alternatively, 37.5 20.9% of plants (N = 11 species), had
pollinia collected and deposited, or set fruit.
The poor pollination success of sexually deceptive orchids
is generally attributed to a lack of pollinators or pollinator
visits, rather than any limitation in resources such as water
or nutrients (Peakall, 1989; Calvo, 1993; Neiland & Wilcock,
1998; Schiestl, 2005; Tremblay et al., 2005; Zotz & Schmidt,
2006; Vandewoestijne et al., 2009). Pollinator limitation may
be a consequence of extreme specialisation to a single or very
few pollinator species. Specialist orchids may be vulnerable to
mismatches in pollinator emergence and flowering seasons,
which is likely to worsen due to climate change (Memmott
et al., 2007). Pollinator limitation may also be particularly
severe in sexually deceptive systems because of the likelihood
that insects attracted to an orchid will not make contact
or effect pollination, the variation in individual pollinator
responses, or the possibility of fooled pollinators avoiding
orchids or orchid locations after previous visits (see Sections
IV.2, IV.4 and VII). Thus, even if abundant pollinators are
available, they may not necessarily be coerced into orchid
visits.
Sexual deception typically involves a species-specific pollinator (Table 1), so the potential for speciation in sexually
deceptive orchids may be constrained by the diversity of
insects available to act as pollinators, and the potential for
speciation in an existing pollinator species. For example, the
radiations of the relatively diverse sexually deceptive genera
Chiloglottis and Caladenia are both accompanied by frequent
pollinator switching between closely related thynnine wasps
(Mant et al., 2002; Mant, Brown & Weston, 2005c; Bower
& Brown, 2009; Phillips et al., 2009a). Australian thynnine
wasps are diverse, and many of the 715 named species are
endemic (Naumann, 2000). Table 1 shows that at least 70
Australian thynnine species from 12 genera pollinate at least
150 sexually deceptive orchid species from seven genera, with
many more thynnines yet to be formally identified (Table 1).
This availability of diverse thynnines may have contributed to
the extraordinary diversification of the major (and largely sexually deceptive) subclades of Caladeniinae and Drakaeinae.
Caladeniinae includes the large genus Caladenia, of which the
sexually deceptive species are almost exclusively thynninepollinated, and Drakaeinae comprises a diverse radiation of
closely related thynnine-pollinated genera including Caleana,
Chiloglottis, Drakaea, and Paracaleana (Kores et al., 2001).

By contrast, all five Australian and New Zealand species
of Cryptostylis (subclade Cryptostylidinae) share a single pollinator, male Lissopimpla excelsa (family Ichneumonidae, subfamily Pimplinae; Coleman, 1928a, b, 1938; Graham, 1983;
Schiestl, Peakall & Mant, 2004; Gaskett et al., 2008). Australia
has only four Lissopimpla species and a relatively small ichneumonid fauna (Naumann, 2000). Therefore, any novel,
mutated, or hybrid forms of Cryptostylis that arise may be
unlikely to attract a new pollinator because so few Lissopimpla
species or Pimplinae are available in the environment. Interestingly, although Australia has several solitary bee species
from the families that are major pollinators for Ophrys species
in Europe, they are not involved in any sexually deceptive
pollination in Australia (Colletidae, Halictidae, Megachilidae
and Anthophoridae; Table 1; Naumann, 2000).
VI. ORCHID SIGNALS AND POLLINATOR

PERCEPTION
Although understanding of orchid scent and pheromone
mimicry is advancing rapidly, there is only meagre
information about other signals or cues involved in pollinator
deception. Scent is undoubtedly vital for long-range
pollinator attraction, but once a pollinator is nearby, visual
signals such as colour or shape must indicate the specific
source of the scent, and, crucially, coerce him into making
contact (Peakall & Beattie, 1996; Streinzer, Paulus & Spaethe,
2009). This would be particularly important for species that
occur in dense aggregations that generate a large scent plume
with multiple, indeterminate origins. It is often assumed or
speculated that shape and colour play a role in sexual
deception by orchids (e.g. Dodson et al., 1969; Bergstrom,
1978; Ayasse et al., 1997; Ascensao et al., 2005; Jersakova
et al., 2006a; Paulus, 2006; Salzmann et al., 2006; Schluter &
Schiestl, 2008). However, experimental tests for shape and
colour mimicry and manipulations of these signals require
considerably more attention before this can be confirmed.
(1) Scent
Early researchers swiftly recognised the importance of orchid
scent for attracting pollinators and stimulating pollinator
sexual behaviour (Coleman, 1928b, 1929; Kullenberg, 1956;
1961). In the field, pollinators approach orchid flowers with a
characteristic zig-zag flight path associated with chemoreception (Wallace, 1978; Stoutamire, 1979, 1983; Peakall, Beattie
& James, 1987; Peakall, 1989, 1990; Peakall & Beattie, 1996;
Paulus, 2006). Behavioural tests offering pollinators dissected
orchid flowers can be useful for determining where scent is
released in the flower (typically from the sepals, petals, and/or
labellum; Peakall, 1989; Peakall & Beattie, 1996).
Initially, behavioural studies confirmed that pollinators
could be attracted with extracts of sexually deceptive orchids
or synthetic mixtures of common compounds (Kullenberg,
1956, 1961). Subsequent chemical analyses tested for similarities in extracts or volatiles collected from orchids and the
65
females of their pollinator species using gas chromatography
and gas chromatography-mass spectrometry (GC, GC-MS;
Bergstrom, 1978; Borg-Karlson, 1987, 1990; Schiestl et al.,
1999; Flach et al., 2006). The most powerful studies combine
behavioural observations and assays with chemical analyses
and tests for pollinator perception of scents (Fig. 4). Pollinator
perception of orchid scent can be tested with calcium imaging of antennal lobe activity in the pollinator brain during
exposure to floral scents (Galizia et al., 2005), or much more
commonly, gas chromatography-electroantennography or
gas chromatography-electroantennal detection (GC-EAG or
GC-EAD; Schiestl, 2005). GC-EAD allows scent compounds
to be individually tested for their capacity to stimulate a pollinators antennal chemoreceptors. Whole live antennae of the
pollinator species have been tested with synthetic versions
of compounds identified in orchids (Agren

& Borg-Karlson,
1984; Schiestl et al., 1999), or more commonly, with extracts
of orchid labellae and/or females of the pollinator species
(Schiestl et al., 1999, 2000; Schiestl & Ayasse, 2002; Ayasse
et al., 2003; Mant et al., 2005b, d; Schiestl & Peakall, 2005;
Stokl et al., 2005, 2007; Vereecken & Schiestl, 2008; Gogler
et al., 2009). Not every electrophysiologically active compound necessarily elicits a behavioural response from the
pollinator, so behavioural assays must be performed (Schiestl
& Marion-Poll, 2002; Leal, 2005). The model example of
this procedure is the elegant and methodical identification,
synthesis, and field testing of the single novel compound
attracting pollinators to Chiloglottis trapeziformis, and the use of
this compound and analogs in further investigations of other
Chiloglottis species (Schiestl et al., 2003; Schiestl & Peakall,
2005; Poldy, Peakall & Barrow, 2008; Franke et al., 2009;
Fig. 4).
Application of GC-EAD could be enhanced by more
detailed reporting. Few studies reveal the total number of
trials performed, including those in which antennae failed to
make any response at all. It is also rare to report the magnitude or number of antennal responses required before a
compound can be considered electrophysiologically active.
For example, compounds could be considered electrophysiologically active when they provoke antennal responses in
at least half of the runs performed (Schiestl & Ayasse, 2002;
Stokl et al., 2007; Gogler et al., 2009). Ideally, studies should
report the number of trials performed, the proportion in
which antennae failed to respond, and the number and
magnitude of antennal responses obtained for each electrophysiologically active compound. The latter could be
addressed when publishing Tables of electrophysiologically
active compounds by adding a column that provides the
number of antennae responding to each compound and
the mean magnitude of the response. Since most statistical
tests assume independence of data, it is also important to
declare and control for antennae used in more than one
trial (e.g. Mant et al., 2005b) and when using both antennae
from one insect. Interestingly, the sensitivity and responsiveness of insect antennae (or conversely, the strength of
the orchid signal) may vary consistently with some biologically relevant factor such as the extent of pollinator sexual
A. C. Gaskett
66
Fig. 4. Research paths incorporating a pollinator perspective: assessing the role of pollinator behaviour and pollinator perception
of orchid signals in studies of pollination by sexual deception. GC, gas chromatography; GC-MS, gas chromatographymass spectrometry; GC-EAD, gas chromatography-electroantennodetection or gas chromatography-electroantennography; SEM,
scanning electron microscopy. 1 Bower & Brown (2009); 2 Peakall (1990); 3 Alcock (1981); 4 Schiestl et al. (1999); 5 Schiestl et al. (2003);
6
Gaskett & Herberstein (2010); 7 Schiestl (2004); 8 Zelditch et al. (2004); 9 Shipunov & Bateman (2005); 10 Kullenberg (1961); 11 Agren
12
13
14
15
16
et al. 1984; Galizia et al. (2005); Francke et al. (2009); Vereecken et al. (2007a); Ayasse et al. (2000); Wong et al. (2004);
17 Johnson et al. (1998); 18 Mondrag
on-Palomino & Theien (2009); 19 Fitzpatrick et al. (2005).
behaviour, or between major and minor pollinators for an

orchid species, suggesting interesting additional analyses that
would maximise the value of EAD-based research.
(2) Colour
Analyses of orchid colour from a human perspective are
largely redundant given the differences between human and
insect visual systems (Kelber, Vorobyev & Osorio, 2003).
Early studies by Kullenberg (1961) attempted to quantify
the colour of Ophrys species with spectral measurements and
comparisons with standard colour hues. Recently, studies
of food-deceptive pollination systems compare the spectral reflectance of food-deceptive orchids and co-occurring
rewarding species (Table 2). Some studies take the next step
and consider pollinator perception of colour by mapping
spectral reflectances of food-deceptive orchids into pollinator visual systems (Gumbert & Kunze, 2001; Galizia et al.,
2005; Indsto et al., 2006). Similar analyses for sexually deceptive species show that despite colour differences seen by
humans (Fig. 1), four Australian Cryptostylis orchid species
are all perceptually identical in colour to their pollinators
female conspecific when modelled into a hymenopteran
visual system (Gaskett & Herberstein, 2010). Analysis from
the pollinators visual perspective is crucial for understanding
pollinator-driven selection on orchid colour, but is hindered

by the lack of specific information about the visual systems of
most orchid pollinator species and disagreement about modelling methods (Chittka, 1992; Vorobyev & Brandt, 1997;
Kelber et al., 2003; Chittka & Kevan, 2005). Nonetheless,
any studies modelling orchids from the visual perspective of
the pollinator would be a significant contribution (Fig. 4).
A major difficulty when studying colour mimicry by
orchids is the potential to conflate mimicry and convergent evolution (see Johnson, Alexandersson & Linder, 2003;
Grim, 2005). If food-deceptive orchids (the putative mimic)
are compared with co-occurring rewarding flower species
(the models), it is likely their shared environmental conditions and pollinators would exert similar selective pressure
on many features including colour. This problem can be
avoided by investigating mimicry in sexually deceptive,
rather than food-deceptive, pollination systems. Sexually
deceptive orchids, the mimics, have an entirely different
ecology and physiology to their models, female insects. Consequently, similarities between the orchid and the female
insect can be more confidently attributed to mimicry rather
than to convergence in sexually deceptive systems.
Sexually deceptive orchids may also exploit pollinator sensory biases or perceptual weaknesses. Sensory biases evolve
when sensitivity to certain signals or cues provides fitness

benefits, e.g. quick detection of colours associated with food
or mates, or a preference for larger body size in mate
choice (Schaefer & Ruxton, 2009). Orchids that exploit
insect sensory biases can take advantage of their pollinators
innate attraction to certain signals such as wavelengths or
shapes (see also Section VI.3). The ornaments of sexually
deceptive Ophrys heldreichii orchids were thought to exploit
innate pollinator visual biases for pink wavelengths because
pollinators preferred flowers with intact natural pink ornaments (Spaethe, Moser & Paulus, 2007). However, a later
study established that pollinators found the orchid more
rapidly when researchers attached various coloured ornaments as long as they contrasted with the background,
suggesting a sensory bias for contrast rather than specific
colours (Streinzer et al., 2009). Yellow and ultraviolet (UV)
wavelengths may be more likely candidates for exploitation of innate insect preferences. Many insects are strongly
attracted to yellow or UV (Jonsson, Lindkvist & Anderson,
2005; Goulson et al., 2007; Lunau, 2007) and orchids often
have bright yellow pollinia visible to the pollinator or yellow
sepals or petals (e.g. Cryptostylis, Fig. 1; Gaskett & Herberstein,
2010; see Delforge (2005) for pictures of Ophyrs spp.). Bright
yellow spots on the labellum are known to attract pollinators
in the food-deceptive slipper orchid Paphiopedilum barbigerum
(Shi et al., 2009) and similar pollinator behaviour is reported
in other Paphiopedilum species (Banziger, 1996). Exploitation
of insect attraction to UV is also plausible (Paulus, 2006;
Gaskett & Herberstein, 2010). For example, bumps on the
labellae of Cryptostylis subulata and C. ovata reflect UV, identical
to the wings of their pollinators female conspecific (Gaskett
& Herberstein, 2010). However, UV-reflection is relatively
uncommon in rewarding flowers (Chittka et al., 1994), and is
correspondingly rare in food-deceptive orchids (e.g. Johnson,
2000; Johnson et al., 2003).
Intriguingly, many sexually deceptive orchids are predominantly green, red, or white, which are colours not easily
seen by hymenoptera (Gaskett & Herberstein, 2010; Figs 1
and 2; further images of Australian, European, and South
and Central American species see Blanco & Barboza, 2005;
Delforge, 2005; Jones, 2006; Singer et al., 2006). Green flowers may be difficult to distinguish from surrounding green
leaves, perhaps resembling background leaves or plants and
thus obscuring parts of the flower that may hinder mimicry
of female insect body shapes. Although white flowers appear
obvious to humans, they can be difficult for hymenoptera
to distinguish from the background (Chittka et al., 1994).
This is because white flowers, like background foliage, soil
and stones, cause approximately equal excitation of the
Blue, Green and UV receptors typical of most hymenoptera
(Chittka et al., 1994). Red floral colouration may act as
a cognitive sensory trap (Schaefer & Ruxton, 2009). Red
wavelengths are beyond the peak sensitivities of the Blue,
Green and UV receptors, and are therefore difficult for
hymenoptera to detect or differentiate between (Chittka
et al., 1994) and distinguish from the background (Spaethe,
Tautz & Chittka, 2001). Better modelling of pollinator perception of orchid colours requires characterisation of the
67
peak sensitivities of the visual receptors of common sexually
deceptive orchid pollinators such as Colletes cunicularius or
thynnines (e.g. Peitsch et al., 1992). More studies investigating and testing for exploitation of sensory biases and sensory
traps in sexual deception would be fascinating.
Finally, although within-species colour polymorphism
occurs in several food-deceptive orchid species (Gigord,
Macnair & Smithson, 2001; Koivisto, Vallius & Salonen,
2002; Salzmann & Schiestl, 2007), it is rare for sexually
deceptive species, exceptions include Caladenia behrii (Dickson
& Petit, 2006) and Ophrys arachnitiformis (Vereecken & Schiestl,
2009). The role of colour polymorphism is unclear. Most
studies with food-deceptive orchid species find no evidence
of frequency-dependent selection or pollinator preferences
for rare colour morphs (Koivisto et al., 2002; Aragon &
Ackerman, 2004; Pellegrino, Bellusci & Musacchio, 2005;
Dickson & Petit, 2006; Smithson et al., 2007; Tremblay
& Ackerman, 2007; Vereecken & Schiestl, 2009, but see
Gigord et al., 2001). Thus future studies of colour polymorphism in either sexual or food deception should consider
how colour morphs differ in several factors such as fitness,
post-pollination barriers, or seed viability, rather than just
pollinator preferences (e.g. Pellegrino et al., 2005; Jersakova,
Kindlmann & Renner, 2006b).
(3) Shape
The shape of an orchid is also likely to be an important visual
signal for sexual deception. After a pollinator has landed on
an orchid, he must be persuaded into attempting copulation.
This could be accomplished by close-range mimicry of the
dimensions and tactile qualities of the body of his female
conspecific. Comparison of the distribution and dimensions
of hairs on the surface of Ophrys spp. labellae and the specific female bees they mimic indicated considerable textural
congruence (Agren,
Kullenberg & Sensenbaugh, 1984). Several orchids feature notably insectiform labellae that might
mimic female insects, e.g. Drakaea, Paracaleana and Lepanthes
species and Geoblasta pennicillata, but others, including Cryptostylis erecta, Trigonidium obtusum and Pterostylis species do not
appear insect-like to the human viewer (Figs 1 and 2; Singer,
2002; Blanco & Barboza, 2005; Ciotek et al., 2006).
Close-range tactile cues may also determine pollinator
orientation on the orchid, which is imperative for effective
pollinia collection and transferral (Kullenberg, 1961;
Wallace, 1978). The surface cells on the labellae of Ophrys fusca
and O. lutea bear long trichomes that point towards the stigma
and these are likely to direct the pollinators genital claspers
towards the stigma and adjacent pollinia (Ascensao et al.,
2005). The hypothesis that trichomes function in pollinator
orientation could be tested by experimentally removing
trichomes or manipulating their arrangement and observing
pollinator orientation behaviour. In field experiments,
pollination and fruit-set would be expected to be lower
for orchids with experimentally removed trichomes than for
control orchids that had received a similar level of sham
damage, e.g. small cuts made on the reverse of the labellum.
A. C. Gaskett
68
Shape may also exploit pollinator sensory biases involved
in male mate-choice behaviour. Morphological comparisons
of flower size show that the labellae of Chiloglottis trapeziformis
orchids are consistently larger than the female insects they
mimic (Schiestl, 2004). These large flowers could represent
an irresistible super-stimulus that exploits the common male
insect preference for large female body size (Bonduriansky,
2001; Schiestl, 2004). However, in tests with model female
insects, the pollinator of Chiloglottis trapeziformis preferred
intermediate over both small and large models, indicating a
limit to male preference for large female body size (Schiestl,
2004). However, measurements were taken of the whole
labellum, rather than just the insectiform black, glossy calli
on the labellum of the orchid, which may be more relevant
for comparison (for drawings, see Bower, 1996; Mant et al.,
2005a; Mant, Peakall & Weston, 2005e). A comprehensive
multi-species study of the possible tactile function of these
calli in Chiloglottis species, the insectiform labellae of Drakaea
or Caleana species, or the whole labellae of Ophrys species,
would help clarify the role (if any) of shape mimicry in sexual
deception.
The literature suggests two alternative and as yet unstudied
hypotheses for the function of varying floral shape in sexual
deception. Firstly, variation in shape could impair pollinator learned avoidance in the same way that scent variation
hinders this process in Ophrys sphegodes and other unrewarding flowers (Ayasse et al., 2000; Raguso, 2004). Experiments
testing pollinator behaviour and learning using manipulated
floral shapes are required. Secondly, floral shape is undoubtedly important in the function of floral traps. Morphology is
likely to control both the location and duration of pollinator
contact, with strong consequences for pollinia transfer and
thus fitness. For example, when a pollinator grips the loosely
hinged labellum of Arthrochilus species, he is swiftly swung into
a pair of flanges that control his position against the stigma
and pollinia, then a second pair of curved flanges traps his
wings and prevents his escape until after pollinia transferral
has occurred (Bower, 2001a). Research into the evolution of
trap mechanisms could commence by testing how variation
in some morphological aspect of a floral trap interacts with
pollination success.
(4) Multimodal signalling
In his thesis, Kullenberg (1961) addressed the possibility
of multiple olfactory, visual and tactile stimuli in sexual
deception, but there are few contemporary tests in which
pollinators are offered models with simultaneous variations
in scent and colour and shape to determine signal functions
and the extent of signal duplication (Fig. 4; e.g. Vereecken &
Schiestl, 2009). Sexually deceptive orchids exploit their pollinators mate search and mate-choice signals. Mate choice
often involves assessment of multicomponent or multimodal
signals (Candolin, 2003; Papke, Kemp & Rutowski, 2007).
Therefore, orchids that produce multiple deceptive sex signals in chemical, visual and tactile modes could be extremely
compelling for their mate-searching potential pollinators.
Since the attractiveness of an orchid appears to provide
fitness benefits in terms of increased pollination success

(Fig. 3; Gaskett et al., 2008), there should be strong selection
for multimodal signalling.
Multicomponent signals can enhance detection in signalnoisy environments, or assist in species and mate recognition
(Partan & Marler, 1999; Candolin, 2003). Furthermore, each
signal mode could convey different information about the
emitter (Candolin, 2003). For orchids, scent and colour might
advertise the orchids location, whilst the size of the orchid
might suggest a female of high fecundity and mate quality.
Alternatively, each mode could elicit a different part of the
receivers response (Kullenberg, 1961). For orchids, scent
might attract over long distance, while shape and texture
cause precise orientation on the orchid, and stimulate copulation. A third explanation, the backup hypothesis, suggests
that each component reiterates or reinforces the same message (Partan & Marler, 1999; Candolin, 2003; Papke et al.,
2007). However, behavioural tests with Ophrys arachnitiformis
show that for this species, scent alone is sufficient for pollinator attraction, and that there is no signal reinforcement
between the scent and the natural green or white floral ornaments (Vereecken & Schiestl, 2009). Other candidates for
multi-signal manipulation are colourful and morphologically
ornate species for which the attractive scents are well studied,
e.g. Ophrys exaltata (Mant et al., 2005b; Vereecken & Schiestl,
2008), Ophrys fusca (Ascensao et al., 2005; Stokl et al., 2005),
Ophrys iricolor (Stokl et al., 2007), and Ophrys sphegodes (Schiestl
et al., 1999; Ayasse et al., 2000).
The functions and evolution of multiple signals can also be
studied by applying molecular data from model systems such
as Arabidopsis and Antirrhinum to orchids (Schluter & Schiestl,
2008; Mondragon-Palomino & Theien, 2009). The pollinator perspective could be incorporated by applying molecular
data on the expression of insect sexual behaviour, odorant receptor genes, the functions and pathways of olfactory
receptor neurons, and signal processing in the brain (e.g.
Fitzpatrick et al., 2005; Rutzler & Zwiebel, 2005; Bargmann,
2006; Hallem, Dahanukar & Carlson, 2006). There is also
considerable existing data on the molecular basis of insect
colour perception (e.g. the genes coding for visual pigments
such as opsin) which could be applied to the study of deceptive orchid colouration (Briscoe & Chittka, 2001; Kelber
et al., 2003; Spaethe & Briscoe, 2004).
VII. POLLINATOR LEARNING

In insects, learning and memory are common in all aspects of
life including sexual behaviour (Dukas, 2008). In the past, sexual deception was thought to activate only innate behaviour
with no scope for learning (Kullenberg & Bergstrom, 1976a;
Dafni, 1987). It is now widely accepted that deception stimulates pollinator learning and memory, and consequently,
changes in individual behaviour (Wong & Schiestl, 2002;
Schiestl, 2005; Jersakova et al., 2006a; Paulus, 2006; Spaethe
et al., 2007). After visiting a sexually deceptive orchid, a pollinator appears to become aversive to the location of the

deception. Unlike the pollinators of rewarding, nectariferous
flowers (Chittka, Thomson & Waser, 1999), sexually deceived
pollinators generally depart quickly and rarely visit multiple neighbouring orchids (Peakall, 1990; Peakall & Beattie,
1996; Peakall & Schiestl, 2004; but see Jones & Gray, 1974).
Fieldworkers frequently report that when an orchid flower is
artificially introduced into an area, pollinators arrive swiftly,
even within a minute for some species, but the rate of insect
attraction soon wanes, even when fresh orchids or real female
insects are subsequently placed in the same location (Peakall,
1990; Bower, 1996; Bower & Brown, 1997; Alcock, 2000;
Ayasse et al., 2000; Wong & Schiestl, 2002; Wong, Salzmann
& Schiestl, 2004). This is not because pollinator chemoreceptors have become desensitised or habituated to the orchid
scent because if the orchids are moved a few metres, they
typically attract pollinators again (Bates, 1977; Stoutamire,
1983; Peakall, 1990; Bower, 1996; Ayasse et al., 2000). In one
study, the pollinators of Ophrys sphegodes quickly learnt orchid
locations and the scents of individual flowers, and avoided
them when tested a few minutes later (Ayasse et al., 2000).
Post-deception aversion to orchids appears to involve two
forms of learning: spatial configuration, and recognition of
signals or sensory information (Dukas, 2008). It is unknown
how long these memories are retained and whether variation
in one or more of the signal modes impairs or assists in
memory acquisition. Another unknown component is the
influence of positive and negative reinforcement, i.e. if prior
matings with real female insects or orchids make a male
insect more or less likely to mate with a female insect or visit
an orchid in the future. Capacity for learning and memory
are heritable (Dukas, 2008), and this suggests several interesting hypotheses: is learned avoidance a specific response to
orchid deception, or a regular behavioural response to any
negative experience, such as attempting to mate with a dead
or heterospecific female? Does learned avoidance improve
pollinator fitness, and is this sufficient to drive selection at a
population or species level? Are nave insects outside orchid
ranges more likely to be fooled by an orchid than nave insects
in populations in long-term contact with orchids? Experimental assays involving pollinator learning require nave or
captive-bred male insects to ensure no previous experience
with orchids or real females. Almost all studies of sexual
deception employ wild-caught male insects, but Gogler et al.
(2009) used commercial colonies of Bombus terrestris to lure and
establish laboratory colonies of parasitic Bombus vestalis (the
pollinator of Sardinian Ophrys normanii and O. chestermanii) and
a similar technique could be used for other parasitoids that act
as pollinators for sexually deceptive orchids. There are few
experimental tests of learning in sexually deceived pollinators
so this is likely to be a very productive field for future research.
VIII. COSTS OF DECEPTION AND

ORCHID-POLLINATOR COEVOLUTION
Sexually deceptive orchids generally exert little influence on
the evolution of their pollinators (Schiestl, 2005; Jersakova
69
et al., 2006a). Pollinators of sexually deceptive orchids receive
no benefits from orchid visits and in most cases orchids are
also unlikely to impose any costs on their pollinator species.
Costs to the pollinator species are unlikely because not all
insects that encounter an orchid are fooled into acting as
pollinators (Table 3) and orchids are often rare or flower
sporadically, and do not grow in all areas in which their pollinating species is found (Kindlemann & Balounova, 2001;
Peakall et al., 2002; Bower & Brown, 2009). Therefore many
insects from a pollinating species may never or only rarely
encounter a sexually deceptive orchid. In this situation, at
species level the fitness benefits of responding swiftly to sexual
signals and securing many matings with real females may outweigh the disadvantages of occasional matings with orchids.
However, mating with orchids may have negative impacts
for individual pollinators. Pollinators can prefer orchids to
real females, prematurely end a copulation with a real female
to visit an orchid, or be unable to find real female mates
among false orchid signals (Coate, 1965; Wong & Schiestl,
2002; Schiestl, 2004; Vereecken & Schiestl, 2008). If sexual
deception involves pollinator ejaculation and sperm wastage,
it may even affect a males future mating opportunities.
Sperm production can be costly in many insect species,
limiting lifetime sperm production (Wedell, Gage & Parker,
2002). Even if sperm production is not costly, a male could
become temporarily sperm depleted during an orchid visit. If
he then soon encounters a real female, he may not be able to
copulate, or may transfer only seminal fluid without sperm,
as occurs in many solitary wasp species (King, 1987; Damiens
& Boivin, 2006). Although currently considered extremely
rare and proposed only for Cryptostylis and Lepanthes species
(Blanco & Barboza, 2005; Gaskett et al., 2008), pollinator
ejaculation has been studied in so few species that it may be
more common than currently believed.
Learned avoidance by pollinators after visiting sexually
deceptive orchids is well documented and could be an
evolved response to the costs imposed by the deception
(Peakall, 1990; Bower, 1996; Bower & Brown, 1997; Alcock,
2000; Ayasse et al., 2000; Wong & Schiestl, 2002; Wong et al.,
2004). If the costs of deception are strong enough to select
for pollinator avoidance of orchids, this in turn could select
for increasingly sophisticated and persuasive orchid signals,
ie. antagonistic coevolution or an arms race (Wong & Schiestl, 2002; Gaskett et al., 2008). However, there are currently
no data indicating whether these costs actually do impede
pollinator fitness sufficiently to drive coevolution and a large
study addressing pollinator mating behaviour and sperm use
and exploring the potential for individual and population
costs of exploitation by orchids is required.
At present, it is apparent that pollinators and their
behaviours, mating systems, diversity, and sensory perception could exert considerable selection on sexually deceptive
orchids and their signals. If sexual deception does negatively
impact the mating opportunities of individual pollinators,
there is no experimental evidence to show this is adequate to
impose selection on pollinators at the level of population or
A. C. Gaskett
70
species. Thus, antagonistic coevolution remains a tantalising
hypothesis for future research.
IX. FUTURE DIRECTIONS

(a) Fundamental natural history observations of pollinator
identity and sexual behaviour with poorly known
orchids are crucial for conservation and knowledge.
This is especially so for highly endemic and diverse
orchid regions such as Australia and Central and South
America, contentious taxa (e.g. Cymbidium pumilum and
Pterostylis), and species that may combine aspects of
both sexual and food deception (e.g. Orchis galilaea and
Caladenia patersonii).
(b) Investigating pollinator mating systems and the
consequences of haplodiploidy and indirect selection
offers new frameworks for researching sexual
deception, and more generally, hymenopteran
evolution and behavioural ecology.
(c) Future studies involving gas chromatographyelectroantennography (GC-EAG or GC-EAD) can be
enhanced by reporting factors such as the number
of trials, number of unresponsive antennae, and the
magnitude of responses observed, and considering
whether these factors vary consistently with pollinator
mating systems or behaviours.
(d) Although more studies of colour mimicry in
sexual deception are desirable, investigating how
orchids exploit pollinator visual biases and employ
sensory traps would make a more widely applicable
contribution to the field of deceptive signalling.
(e) Investigation of floral shape provides many new or
under-studied opportunities for research: mimicry,
exploitation of sensory biases, the effect of shape
variation on pollinator learning, and the evolution
of floral trap morphology.
(f) Current molecular studies of orchid signal expression
could be accompanied by research into the genetic
factors influencing pollinator perception of signals (e.g.
olfactory receptors and visual pigments) and pollinator
learning and memory.
(g) Future topics to address in pollinator learning include
the temporal longevity of memory, the functions of
multiple signal modes, and the influence of positive
and negative reinforcement.
(h) Costs imposed on pollinators by deception remain
unquantified and evidence for antagonistic coevolution
between orchids and their deceived pollinators merits
considerable attention.
X. CONCLUSIONS
(1) At present, sexually deceptive orchid genera have
been identified in Australia and New Zealand
(2)
(3)
(4)
(5)
(6)
(7)
(8)
(Arthrochilus, Caladenia, Caleana, Calochilus, Chiloglottis,

Cryptostylis, Drakaea, Leporella, Paracaleana, Spiculaea and
potentially Pterostylis), Europe (Ophrys, Orchis), South
Africa (Disa), Central and South America (Geoblasta,
Lepanthes, Mormolyca, Stellilabium, Telipogon, Trichoceros,
Trigonidium and potentially Tolumnia), and potentially
Japan (Cymbidium pumilum).
Sexually deceptive orchids are pollinated only by
male insects, which are typically from species that
are solitary rather than social and are haplodiploid,
monandrous, and polygynous.
There is considerable diversity in the behaviour of
sexually deceived pollinators among different orchid
species, and among different individuals of the pollinator species. Generally, pollination involves copulation
or simple gripping of the orchid. Ejaculation is rare.
In some cases, pollinators are trapped briefly.
Orchid speciation may be facilitated by high insect
diversity if this fuels pollinator shifts and provides new
pollinators for hybrids and mutants.
A literature survey reveals that for sexually deceptive
orchids, an average of 20.5 14.7% of all flowers
(mean S.D.; N = 35 species), or alternatively, 37.5
20.9% of plants (N = 11 species) had pollinia collected and deposited, or set fruit. Pollination rates per
flower are similar in Europe (18.4% 17.4, N = 8)
and temperate Australia (18.4 11.4%, N = 21).
Although scent mimicry is increasingly well studied,
visual and tactile mimicry require further attention, with emphasis on pollinator perception and
experimental manipulations involving multiple sensory modes. Alternative deceptive interactions such as
exploitation of pollinator sensory biases are also likely.
Observations suggest that pollinators commonly
exhibit learned avoidance of orchids or orchid locations.
Generally, even if orchids impose minor costs on
individual pollinators, these may be insufficient to
drive selection at a population or species level. Rare
examples of sexual deception provoking pollinator
ejaculation may exert considerable costs on the pollinator, but this is yet to be demonstrated empirically.
XI. ACKNOWLEDGEMENTS
I thank Marie Herberstein and Andy Beattie (Macquarie
University), Greg Holwell (University of Auckland) and
anonymous referees for their constructive, thorough, and
thoughtful comments on the manuscript. Colin Bower
(FloraSearch), Graham Brown (Museum and Art Gallery
of the Northern Territory), Stephen Hopper (Royal
Botanic Gardens, Kew) and Eric Scanlen and Ian St
George (New Zealand Native Orchid Group) provided
advice and unpublished data for the list of pollinators in
Table 1. Most photographs were kindly provided by Julia
Cooke (Macquarie University). This work was generously

supported by a Furniss Foundation/American Orchid
Society Fellowship.
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Biol. Rev. (2011), 86, pp. 3375.

Orchid pollination by sexual deception:

of Biological Sciences, Macquarie University, NSW 2109, Australia

(Received 29 August 2008; revised 25 February 2010; accepted 1 March 2010)

* Address for correspondence: E-mail: a.gaskett@auckland.ac.nz

maintain deception. Furthermore, as sexual deception relies

Orchid pollination by sexual deception

II. POLLINATION BY SEXUAL DECEPTION

III. POLLINATORS OF SEXUALLY DECEPTIVE

Apis cerana japonica

Growth form Pollinator

Pollinator sexual % flowers

Phillips et al. (2009a)

Brown et al. (1997); Phillips et al.

Phillips et al. (2009a)

Phillips et al. (2009a)

Rotherham (1967); Bower

Steiner et al. (1994)

Steiner et al. (1994)

Sasaki et al. (1991)

Caladenia (syn. Arachnorchis)

Caladenia (syn. Arachnorchis)

Caladenia (syn. Arachnorchis)

Caladenia (syn. Arachnorchis)

Caladenia (syn. Arachnorchis)

Neozeleboria nr. volatile (Sm.)

Phymatothynnus nr. nitidus 1

C.C. Bower (unpublished data)

Phillips et al. (2009a)

Phillips et al. (2009a)

Phillips et al. (2009a)*; Bates

Hopper & Brown (2001)

C. C. Bower (unpublished data)

Phillips et al. (2009a)

Stoutamire (1974, 1983); Brown

Phillips et al. (2009a)

Coleman (1930); Stoutamire

Phillips et al. (2009a)

Phillips et al. (2009a)

Orchid pollination by sexual deception

Caladenia (syn. Arachnorchis)

Caladenia (syn. Arachnorchis)

Caladenia (syn. Arachnorchis)

Caladenia (syn. Arachnorchis)

Phymatothynnus nr. nitidus 1

Growth form Pollinator

Pollinator sexual % flowers

Phillips et al. (2009a)

C.C. Bower (unpublished data)

Phillips et al. (2009a)

Phillips et al. (2009a)

Brown et al. (1997)*; Phillips et al.

Stoutamire (1983)*; Brown et al.

Phillips et al. (2009a)

Stoutamire (1983); but see van

Phillips et al. (2009a)

Hopper & Brown (2001)

Phillips et al. (2009a)

Stoutamire (1983); Brown et al.

Caladenia (syn. Arachnorchis)

Caladenia (syn. Arachnorchis)

Lophocheilus villosus Guerin

Phymatothynnus nr. pygidialis