Biol. Rev. (2011), 86, pp. 33–75.

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) 33–75 © 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; Jers´akov´a, 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; Rodríguez-Giron´es & Santamaría, 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 & Schl¨uter,
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 pollinator’s 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; Jers´akov´a 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; V´asquez, Ibisch & Gerkmann,
2003; Gravendeel et al., 2004; Cozzolino & Widmer, 2005;
Tremblay et al., 2005; Peakall, 2007; Schl¨uter & Schiestl,
2008; Waterman & Bidartondo, 2008; Phillips et al., 2009a;
Schiestl & Schl¨uter, 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

Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society

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
(Jers´akov´a 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 (V´asquez 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 Zealand’s 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

Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society

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.
Caladenia (syn. Arachnorchis)
arenicola Hopper &
A.P.Br.
Caladenia (syn. Arachnorchis)
atrovespa D.L.Jones

Cymbidieae
Japan
Cymbidium pumilum Rolfe

Orchid

Arthrothynnus rufiabdominalis
Brown
Arthrothynnus sp.

T

Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society

T

T

T

T

T

Thynnoides gracilis
(Westwood)

Tiphiidae;
Hymenoptera

Tiphiidae;
Hymenoptera
Tiphiidae;
Hymenoptera
Thynnoides senilis (Erichson) Tiphiidae;
Hymenoptera
Phymatothynnus nr. nitidus 1 Tiphiidae;
Hymenoptera
Zaspilothynnus nigripes
Tiphiidae;
Gu´erin
Hymenoptera

Tiphiidae;
Hymenoptera

Arthrothynnus huntianus
Brown (not Rhagigaster
sp. as suggested by
Rotherham, 1967)

T

T

Apidae;
Hymenoptera
Sphecidae;
Hymenoptera
Pompilidae;
Hymenoptera

Apis cerana japonica
Fabricius

Pollinator
Family; Order

Primarily Podalonia
canescens (Dahlbom)
Hemipepsis hilaris Sm.,
H. capensis Fabricius

T

E

Growth form Pollinator

3

3

3

3

3

3

3

2

2

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)*

Phillips et al. (2009a)

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

L. (1997)*.Bates Caladenia (syn.P. nitidus 1 Thynnine wasp Thynnine wasp Phymatothynnus monilicornis (Sm. Bates (2009a)† Hopper & Brown (2001) C. Hymenoptera Tiphiidae. Caladenia (syn. G. Bower (unpublished data) Phillips et al. Arachnorchis) behrii Schltdl.) complex*. Hymenoptera Tiphiidae.L.Muell. Caladenia (syn. concinna Caladenia (syn. Caladenia (syn.J. T Tiphiidae. Jonesiopsis) cairnsiana F.L. Brown pers. Brown et al.Jones Caladenia (syn.W.Carr Caladenia (syn. Stoutamire (1974. Hymenoptera Tiphiidae. Hymenoptera Thynnine wasp T Tiphiidae. T 3 3 3 3 3 3? 3 3 3 3 3 3 3 3 3 3 32. (2009a)* Dickson & Petit (2006) Phillips et al.Br.?* Phymatothynnus victor Turner† Phymatothynnus nr. T Thynnoides sp. Thynnoides sp.Carr Caladenia (syn.Br. 1983).A. Arachnorchis) caudata Nicholls Caladenia (syn. Hymenoptera Tiphiidae. nitidus 1 T T Tiphiidae.Clem. Hymenoptera Tiphiidae. Phillips et al. T T T T Thynnine wasp Neozeleboria nr. Hymenoptera Tiphiidae.) T T Aeolothynnus generosus (Turner) T T T T Phymatothynnus monilicornis (Sm. Hymenoptera Macrothynnus sp.Cunn.C.P. Arachnorchis) clavigera A. Arachnorchis) calcicola G.)† Lestricothynnus sp.) complex Zaspilothynnus sp.8* 19. Arachnorchis) brownii Hopper & A. C.f. Hymenoptera Tiphiidae.W. Hymenoptera Tiphiidae. Phymatothynnus nitidus Sm. subsp.L. Phillips et al.Jones & M.1† 14 (782) 1. Caladenia (syn.9 C. Brown et al.* (Thynnoides bidens (Saussure) inaccurate. (2009a)*. Arachnorchis) concolor Fitzg.L. (2009a) Phillips et al. attingens Caladenia (syn. Arachnorchis) concinna (Rupp) D.Jones Caladenia (syn. Arachnorchis) attingens Hopper & A. volatile (Sm. ex Lindl. (2009a) Orchid pollination by sexual deception 37 Biological Reviews 86 (2011) 33–75 © 2010 The Author. Hymenoptera Tiphiidae.Caladenia (syn. (2009a) Bates (2009a) Phillips et al. Lophocheilus anilitatus (Sm. (2009a)† Bates (2009b) Phillips et al. Hymenoptera Tiphiidae. Arachnorchis) Callitrophila D. Hymenoptera Tiphiidae. Biological Reviews © 2010 Cambridge Philosophical Society . (1997).Jones Caladenia (syn. Hymenoptera Tiphiidae. Arachnorchis) clavula D. 1979. Caladenia aff. 1983). Arachnorchis) aurulenta (D. Bower (unpublished data) Phillips et al. Arachnorchis) branwhitei D. (2009a) Stoutamire (1974. (2009a) Coleman (1930). Arachnorchis) australis G. Hymenoptera Tiphiidae. Drakonorchis) barbarossa Rchb. (2009a) Bates (2009a) Phillips et al. comm.Jones) R. Hymenoptera Phymatothynnus nr.) Tachynomyia sp. Caladenia (syn.

Arachnorchis) conferta D.3* 14. Hymenoptera Tiphiidae. (2009a)† Stoutamire (1983)*.Br. van der Cingel (2001)*. (2009a) Coleman (1930) Stoutamire (1983). (2009a) Phillips et al. but see van der Cingel (2001) for several other sources) Phillips et al. Hymenoptera Phymatothynnus nr. Hymenoptera Tiphiidae.Coleman Caladenia douglasiorum (D. (1997) Bates (2009a) Source 38 A.Biological Reviews 86 (2011) 33–75 © 2010 The Author. (Thynnoides bidens* inaccurate. Jonesiopsis) filamentosa R. (2009a) Stoutamire (1983). C. Hymenoptera Tiphiidae.P. (2009a) C.A. (2009a) Hopper & Brown (2001) Phillips et al. Phymatothynnus sp. & Hopper Caladenia (syn. (2009a) Phillips et al.S. Arachnorchis) ferruginea Nicholls Caladenia (syn.) Thynnine wasp. Phillips. (2009a) Phillips et al. Brown pers. Hymenoptera Tiphiidae. pygidialis 1 Thynnine wasp*. Arachnorchis) cruciformis D. Hymenoptera Tiphiidae.Backh. Arachnorchis) fitzgeraldii Rupp Caladenia (syn.Clem.)* Campylothynnus assimilis Sm.4 8.3 Pollinator sexual % flowers behaviour pollinated (N ) % plants pollinated (N ) Phillips et al. Gaskett . Biological Reviews © 2010 Cambridge Philosophical Society Caladenia (syn. Lestricothynnus modestus (Sm. (2009a) Brown et al. rhomboidiformis E.L. 1997.) Phymatothynnus nr. Arachnorchis) falcata (Nicholls) M.C. Thynnoides spp.Jones Caladenia (syn. Arachnorchis) dilatata R.N. Hymenoptera Pollinator Family.Sarg. Hymenoptera Tiphiidae. (Cont. flavopictus (Sm. G. Caladenia (syn. Hymenoptera Tiphiidae. Caladenia (syn.Br.P. comm. Hymenoptera Tiphiidae. Order T T T T Thynnine wasp T Growth form Pollinator 3 3 3 3 3 3 3 3 3? 3 3 3 3 3 3 3 3 14. C. (2009)* Brown et al. Brown et al.L. (1997)*.L. Caladenia (syn.George Caladenia (syn.) Thynnine wasp Chilothynnus trochanterinus Brown Thynnine wasp T T T T T Phymatothynnus nr. Caladenia (syn. T Tiphiidae. T T T T Zeleboria marginalis (Westwood)*† . Hymenoptera Tiphiidae. Jonesiopsis) doutchiae O. Phymatothynnus ?nitidus† Thynnoides sp. Hymenoptera Ichneumonidae. Hymenoptera Tiphiidae. Hymenoptera Ichneumonid sp. nitidus 1 T T Tiphiidae.Jones Caladenia (syn. Brown et al.W. Hymenoptera Tiphiidae. Caladenia (syn. Arachnorchis) discoidea Lindl. Hymenoptera Tiphiidae.George Orchid Table 1.? Tiphiidae. Arachnorchis) corynephora A.S. Caladenia (syn. Arachnorchis) exstans Hopper & A.† . (1997)† Phillips et al. Arachnorchis) crebra A. Hymenoptera Tiphiidae.Jones) G. Arachnorchis) cruscula Hopper & A. Bower (unpublished data) Phillips et al. Arachnorchis) decora Hopper & A. Phillips et al.Carr Caladenia (syn.H.Br. Thynnoides sp. Caladenia dilatata var.P.Br. et al.Br. nitidus 1 Thynnine wasp Zaspilothynnus nigripes Gu´erin Thynnoides gracilis (Westwood). Caladenia (syn. Arachnorchis) formosa G.

Hymenoptera Tiphiidae. Hymenoptera T Thynnine wasp T Tiphiidae.W. Zaspilothynnus sp. (1997) Stoutamire (1983)*. Caladenia (syn. Arachnorchis) georgei Hopper & A. Hymenoptera Tiphiidae. nitidus 1 Guerinius sp. S.Coleman Caladenia (syn. Arachnorchis) gladiolata R. Arachnorchis) gardneri Hopper & A. heberleana Hopper & A.Carr Caladenia (syn. Hopper (unpublished data) Phillips et al.W. Caladenia (syn. 1983). (1997). Arachnorchis) hastata (Nicholls) Rupp Caladenia (syn.Br. Hymenoptera T Phymatothynnus nr. (1997).Jones & G. Hymenoptera Lophocheilus villosus Gu´erin Tiphiidae.D.Jones Caladenia (syn.Rogers Caladenia (syn. (2009a)* Bates (2009b) Brown et al. Arachnorchis) huegelii Rchb.L. Arachnorchis) integra E. Hymenoptera Tiphiidae.Caladenia (syn. Arachnorchis) aff. Hymenoptera Zaspilothynnus sp.) Phymatothynnus nr. Caladenia (syn.P. bidens inaccurate. Brown et al.Br. Zaspilothynnus sp. (2009a) Bates (2009b) Stoutamire (1983). Arachnorchis) magniclavata Nicholls Caladenia (syn. Arachnorchis) leptoclavia D.P. 1983) Phillips et al.? *. Arachnorchis) fragrantissima D. (2009a) Stoutamire (1979.P. Phymatothynnus nr.3* Bates (2009b) (Stoutamire. Hymenoptera Tiphiidae. Hopper (unpublished data) (Pritchard.Carr Caladenia (syn. Hymenoptera Tiphiidae. (1997)† Phillips et al. Arachnorchis) macrostylis Fitzg. Jonesiopsis) incrassata Hopper & A. Caladenia (syn. S. comm.f. Hymenoptera Tiphiidae. Thynnine wasp T Tiphiidae. nitidus 1 Tachynomyia sp.L. (2009a) Phillips et al.Carr Caladenia (syn. G. Hymenoptera Tiphiidae.W.P.S.) complex Thynnine wasp (Thynnoides preissi & T.D. Caladenia (syn. Arachnorchis) lowanensis G. Hymenoptera Thynnine wasp T T Tiphiidae. Arachnorchis) insularis G. Tiphiidae. pygidialis 2 T 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 7. Brown et al. Hymenoptera Zaspilothynnus sp. Caladenia (syn. Hymenoptera Tiphiidae. Biological Reviews © 2010 Cambridge Philosophical Society . Thynnine wasp T T T T T T T T T Tiphiidae. Hymenoptera Tiphiidae. 2007) Bates (2009a) Bates (2009b) Brown et al. Arachnorchis) infundibularis A. (2009a) Orchid pollination by sexual deception 39 Biological Reviews 86 (2011) 33–75 © 2010 The Author.Br. Hymenoptera Tiphiidae. thynnine wasp † Phymatothynnus monilicornis (Sm. Brown pers.Br.George Caladenia (syn. Phillips et al.S. Arachnorchis) lobata Fitzg.

(1997). Jonesiopsis) pulchra Hopper & A.L. Arachnorchis) pectinata R. (2009a)*.Clem. (2009a) Phillips et al. Hymenoptera Tiphiidae.Caladenia (syn. Brown et al.L. Caladenia flaccida subsp. Phillips et al.Carr Caladenia (syn. Hymenoptera Tiphiidae. Jonesiopsis) pachychila Hopper & A. & Hopper Caladenia (syn. pulchra Hopper & A. 1997) Bates (2009a) Bower (2001b) Source 40 A. Arachnorchis) montana G.S. T Growth form Pollinator 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 2. Hymenoptera Tiphiidae. Order Phymatothynnus aff.Jones Caladenia (syn. (2009a) Stoutamire (1983).) T T Lophocheilus anilitatus (Sm. C.Carr Caladenia (syn. Hopper & Brown (2001)* (Stoutamire. Zaspilothynnus sp.) Caladenia (syn. Arachnorchis) reticulata Fitzg Caladenia (syn.S. Biological Reviews © 2010 Cambridge Philosophical Society T T T T T T T T Tiphiidae.W. Gaskett . Phillips et al.P. nitidus Hymenoptera 1*. Hymenoptera Tiphiidae. Zaspilothynnus nigripes Gu´erin* Lophocheilus anilitatus (Sm. T T Phymatothynnus sp.A. (prev.L. Bates (2009a)† Phillips et al. (1997)† . Arachnorchis) procera Hopper & A. marginatus). Arachnorchis) rhomboidiformis (E. (2009a) Brown et al. Caladenia (syn.Br Caladenia (syn. (2009a)* Phillips et al.) Zeleboria marginalis (Westwood) (as Z. Tiphiidae. S.*. pygidialis Tiphiidae.Jones Caladenia (syn. Mant et al. Phymatothynnus nr.) Biological Reviews 86 (2011) 33–75 © 2010 The Author. Hymenoptera Tiphiidae.L.5* Pollinator sexual % flowers behaviour pollinated (N ) % plants pollinated (N ) Phillips et al. Caladenia (syn. Hymenoptera Tiphiidae. Arachnorchis) radiata Nicholls Caladenia (syn. (as Asthenothynnus sp. Phymatothynnus victor † Zaspilothynnus nigripes Tiphiidae.Coleman) M. Arachnorchis) phaeoclavia D. (1997). Hymenoptera Catocheilus affinis (Gu´erin)* Tiphiidae.Br.Jones Orchid Table 1. Arachnorchis) rileyi D.Rogers Caladenia (syn.W. Arachnorchis) necrophylla D. (Cont. Hopper (unpublished data) Bower (1992). Hymenoptera Pollinator Family. Hymenoptera Tiphiidae.f. Phymatothynnus ?nitidus† Tachynomia sp.) T Thynnoides senilis (Erichson) T Thynnine wasp*. Brown Hymenoptera Thynnine wasp.P. 1983. (2009a) Bates (2009a) Bates (2009a) Phillips et al. Hymenoptera Phymatothynnus sp. Hymenoptera Tiphiidae.Br. Jonesiopsis) multiclavia Rchb. Tiphiidae. Arachnorchis) parva G.Rogers Caladenia (syn. ‘R’ Tiphiidae.P. Phillips et al. Arachnorchis) rigida R.Jones Caladenia (syn.D. (2009a) Brown et al.Br. (2005c).P. Arachnorchis) richardsiorum D. (2009a)* Brown et al. Hymenoptera Thynnoides new sp. Gu´erin Hymenoptera Zaspilothynnus nigripes Gu´erin? Aeolothynnus sp.

& D. (1997) Bates (2009a) Phillips et al.L. Arachnorchis) tesselata D. Aeolothynnus generosus (Turner) Thynnine wasp Phymatothynnus sp. Phymatothynnus monilicornis complex*.L.W. Hopper (unpublished data) Bates (2009a) Stoutamire (1983). Hymenoptera Tiphiidae. Hymenoptera Phymatothynnus nitidus T Caladenia (syn.L. (2005c). T T T T T T T T T T Caladenia aff. Arachnorchis) uliginosa A. Hymenoptera Tiphiidae.5 36.Br Caladenia (syn.Bates Caladenia (syn. Tiphiidae. T. (2009a) Phillips et al. gracilis Thynnoides pugionatus Gu´erin (sp. Hymenoptera Tiphiidae.George Caladenia (syn. (1997). Brown et al. Arachnorchis) valida (Nicholls) M.4 (1214)* Bates (2009a) Bates (2009b) Phillips et al. Hymenoptera Phymatothynnus nr.Bates Caladenia (syn. Hymenoptera Tiphiidae.D. Caladenia (syn. Hymenoptera Tiphiidae. Caladenia (syn. (2009a) C. (2009a) Orchid pollination by sexual deception 41 Biological Reviews 86 (2011) 33–75 © 2010 The Author.Carr Caladenia (syn. Arachnorchis) saxatilis (D.Jones Caladenia (syn.P.Jones T Tiphiidae. ‘D’ Brown Phymatothynnus nr. Mant et al.S.L. Arachnorchis) toxochila Tate Caladenia (syn. Arachnorchis) stellata D.Br. Hymenoptera Tiphiidae.Carr Caladenia (syn. Arachnorchis) thinicola Hopper & A.J. Hymenoptera Tiphiidae.Jones Caladenia (syn.W. tentacula Caladenia (syn. Hymenoptera Tiphiidae. Jonesiopsis) roei Benth. Biological Reviews © 2010 Cambridge Philosophical Society . Hymenoptera Thynnine wasp T T Tiphiidae.Jones 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 20. S. Bates (2009a)† Brown et al.L.)*. Arachnorchis) tensa G. Arachnorchis) tentaculata Schltdl. Hymenoptera Tiphiidae. 14† Thynnine wasp Thynnoides aff. Peakall & Beattie (1996)*. nitidus 1 T Caladenia (syn. Arachnorchis) septuosa D. Arachnorchis) robinsonii G. Arachnorchis) stricta R. rufithorax Turner. Hymenoptera Tiphiidae. Hymenoptera Tiphiidae.C. Phymatothynnus sp. Arachnorchis) speciosa Hopper & A. Bower (unpublished data) Bower (1992). (2009a) Phillips et al.Clem. Thynnoides gracilis (Westwood) Thynnoides new sp. Hymenoptera Tiphiidae.J. nitidus 1 Macrothynnus sp.Thynnoides mesopleuralis Turner Thynnine wasp Phymatothynnus monilicornis (Sm.Jones) R.P. (2009a)*.A. (2009a) Bates (2009a) Bates (2009a) Phillips et al. complex). Phillips et al.

Clem Caladenia (syn. d) Mant et al. Bower (unpublished data) Bower. (1996)*. 25(A)* Neozeleboria n.Jones & M. (2005c. N . (prev. (1997) Phillips et al.Williams (as Calochilus holtzei F. Arachnorchis) verrucosa G. Hymenoptera Tiphiidae.) 3 3 3 3 3 3 2 2 2 2 2 3 3 3 3 3 3 3 Pollinator sexual % flowers behaviour pollinated (N ) % plants pollinated (N ) C. Hymenoptera Tiphiidae. Myrmechila) formicifera Fitzg. Hymenoptera Thynnine wasp Campsomeris sp.Jones Caladenia (syn.Jones) R. Hymenoptera Scoliidae. d) Mant et al.Biological Reviews 86 (2011) 33–75 © 2010 The Author.) T Tiphiidae.L. Mant et al. Arachnorchis) villosissima (G. Bower & Branwhite (1993) Bates (2009a) Jones & Gray (1974).Br. aff.L.Br.L. Hymenoptera Tiphiidae. Simpliglottis) chlorantha D. (2009a) Phillips et al. Neozeleboria nr sp. A. Arachnorchis) zephyra (D. nov. Mant. Hopper & Brown (2006)‡ Bates (2009a) Bates (2009a) Brown et al. Chiloglottis aff. Biological Reviews © 2010 Cambridge Philosophical Society Scoliidae. 5 Pollinator Family. (2005c) Mant et al. Hymenoptera Zaspilothynnus sp. Jonesiopsis) wanosa A. (1992. Caladenia (syn. (2002. Hymenoptera Scoliidae.Br.L. Pterygophorus sp. (Cont.Jones Calochilus pruinosus D. 33 Brown T T T T T T T Chiloglottis aff.George Caladenia (syn.sp.Jones Chiloglottis anaticeps D.S. Paracaleana minor (R. Hymenoptera Tiphiidae. (prev. Hymenoptera Thynnine wasp Lophyrotoma leachii (Kirby)*.L. Hymenoptera Tiphiidae. impatiens Arthrothynnus latus Brown.Bates Caleana major R. Orchid Table 1. 1996).L.Jones Chiloglottis diphylla R. Hymenoptera Thynnine wasp Tiphiidae. Order T Growth form Pollinator Chiloglottis (syn.Muell. Hymenoptera Lophocheilus anilitatus (Sm. C. d) Bower.) Blaxell) Calochilus caeruleus L.† .A. et al. Hymenoptera Tiphiidae. (2002).sp. formicifera 2 T T T T T T T T Phymatothynnus ?nitidus T Neozeleboria impatiens Sm. Gaskett . Hymenoptera Scoliidae.Rogers Calochilus platychilus D. Campsomeris tasmaniensis Saussure Scoliid wasp (also self-pollinates) Scoliid wasp (also self-pollinates) Scoliid wasp (also self-pollinates) Neozeleboria n.Jones Chiloglottis (syn.Br. Mant et al.C.O. 2005c. Thynnoturneria Hymenoptera armiger) Scoliidae. Bates (1989)† . 2005c.L.W. 41 Brown Tiphiidae. Pergidae. formicifera 1 Calochilus cupreus R.sp. (2009a) Source 42 A.) Calochilus campestris R.Carr) D. angustus Brown. Arachnorchis) woolcockiorum D. 45 Brown Tiphiidae.W. (2002. Hymenoptera Tiphiidae. (2005c) Bates (2009a) Bates (2009a) Fordham (1946). Bower (2001d) Bower (2001c) Cady (1965)*.J. Hymenoptera L. Hymenoptera Neozeleboria n.Carr Caladenia (syn.Br. Caleana (syn.S. cyanea (Leach)‡ Iswaroides armiger (Turner) Tiphiidae. Sullivania) minor R.

Jones Chiloglottis aff.. (2002. Hymenoptera Tiphiidae. 40 Brown Neozeleboria impatiens Sm.L. 1996). 2005a.sp. pluricallata 2 Chiloglottis aff.sp.Clem.) Chiloglottis seminuda D.Jones Chiloglottis (syn. Myrmechila) platyptera D. (2002. Mant et al. d) Mant et al. Hymenoptera Tiphiidae.A.Jones Chiloglottis sphrynoides D. d). 1996).A.aff. Chiloglottis (syn.Jones Chiloglottis (syn. Bower & Brown (1997). Mant et al. Sympliglottis) triceratops D. Biological Reviews © 2010 Cambridge Philosophical Society . Hymenoptera Tiphiidae. Hymenoptera Eirone leai Turner T Chiloglottis (syn. Hymenoptera Tiphiidae. 2005c. Bower (unpublished data) Bower & Brown (2009) Bower & Brown (2009) Bower & Brown (2009) Bower (1992. Mant et al. (2002. d) C.L. Hymenoptera Tiphiidae.L.Neozeleboria n. 2005c.L. d) Bower (1996).Clem.sp. 2005c.L.) Druce Chiloglottis reflexa sensu stricta (Tas.L.L. Hymenoptera Tiphiidae.C. Schiestl. Hymenoptera Tiphiidae. c. Mant et al. Chiloglottis (syn.‡ T Neozeleboria carinicollis Turner Neozeleboria n. impatiens Neozeleboria tabulata Brown Neozeleboria tabulata Brown Thynnine wasp Neozeleboria n. (2004)† . Hymenoptera Tiphiidae.Jones Chiloglottis palachila D. Hymenoptera Tiphiidae. d) Mant et al. 1996). Hymenoptera Tiphiidae. 2002. T Tiphiidae. Bower & Brown (1997). 50 Brown T T Neozeleboria n. (2002. Simpliglottis) pluricallata D. Hymenoptera Tiphiidae.sp.Carr Chiloglottis (syn. Chiloglottis (syn. Hymenoptera Eirone sp. Hymenoptera Tiphiidae. pluricallata 3 Chiloglottis reflexa (Labill. 2005c. (2005c. d) Bower (1992. 29 Brown T T T T T T T T T Chiloglottis aff. (2005c) Bower & Brown (2009) Stoutamire (1975) Mant et al.5 (210)† Oakwood (1990)*.sp.W.Jones m. Hymenoptera Neozeleboria nr impatiens 2 T Neozeleboria nr monticola 1 Tiphiidae. (2002. c. Tiphiidae.L.Jones & M. 2005a. Bates (2009a)‡ Bower & Brown (2009) Mant et al. 30 Brown Neozeleboria impatiens Sm.L. N . 2005c. Mant et al. Simpliglottis) jeanesii D. pluricallata 1 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 4* 58. Chilothynnus palachilus Brown T Neozeleboria cryptoides Sm. Hymenoptera Tiphiidae. Simpliglottis) gunnii Lindl. d) Bower (1992. 3 Brown T Neozeleboria n. Hymenoptera Tiphiidae.Jones Chiloglottis sylvestris D. (2002. (2002). Zaspilothynnus sp. Myrmechila) trapeziformis Fitzg.Jones & M.s) Chiloglottis aff. 2005c) Orchid pollination by sexual deception 43 Biological Reviews 86 (2011) 33–75 © 2010 The Author. pluricallata (also referred to as Chiloglottis ‘bifaria’ D. d) Mant et al. (2002. Simpliglottis) grammata G.5 (210)† 58. Mant et al.

Hopper (2009) Gaskett & Herberstein (2006)*. Hymenoptera monticola 3 Lissopimpla excelsa (Costa) Ichneumonidae. N. Hymenoptera Tiphiidae. Hymenoptera Chiloglottis (syn. Hopper (2009) Gaskett & Herberstein (2006)*. Biological Reviews © 2010 Cambridge Philosophical Society Zaspilothynnus gilesi Turner (as Hemithynnus gilesi)*. C. aff cryptoides 2. d) C. L.) 3 3 1 1 1 1? 1 3 3 3 3 3 3 3 35. Simpliglottis) turfosa D. (2008)‡ Brown et al. (Cont. Mant et al.L. Simpliglottis) valida D.0 (122)* 5. Tiphiidae. N. Hymenoptera Lissopimpla excelsa (Costa) Ichneumonidae. A.f. Order T Growth form Pollinator Chiloglottis trilabra Fitzg. Neozeleboria nr. 2005c. Cryptostylis subulata (Labill.Jones & M.L. aff. thynnine wasp† Thynnine wasp Neozeleboria aff.P. Peakall & Handel (1993)*.2 (1329)*† 32.6 (154)*†‡ 25. Bower (unpublished data) Source 44 A. (prev.Br. Myrmechila) trullata D. Bower & Brown (1997). (red/black). (2002. Hymenoptera Tiphiidae. sp. impatiens 1 Tiphiidae. valida 1 Chiloglottis (syn. N.C. Myrmechila) truncata D. Gaskett et al. Hymenoptera Lissopimpla excelsa (Costa) Ichneumonidae. Gaskett (unpublished data)* Schiestl et al. cryptoides 1. (2008)† Nicholls (1938) Bower (2006).Jones Chiloglottis (syn. 1996. Hymenoptera T Tiphiidae. 1996). Gaskett & Herberstein (2006)† . (2002. ursitatum Brown.4 (994)*†‡ 41. T T Chiloglottis aff. (1997)*.) Rchb. Drakaea confluens Hopper & A. Gaskett . Gaskett et al.Clem.0 (47)* 66. Drakaea concolor Hopper & A. Bower & Brown (2009) Bower & Brown (2009) Mant et al.sp. Bower & Brown (2009) Bower (1992.7 (2187)*† 41 (86)* Pollinator sexual % flowers behaviour pollinated (N ) Hopper & Brown (2007). Cryptostylis ovata R. 2006). semipunctata) Hymenoptera Lissopimpla excelsa (Costa) Ichneumonidae. cryptoides Sm. N . d). nitidula Hymenoptera (Turner).Br. Neozeleboria proxima (Turner) Pollinator Family. Bower & Brown (2009) Bower (2006).A.9 (121)*† 70. Hopper & Brown. Cryptostylis hunteriana Nicholls Cryptostylis leptochila Benth. Turner.Br.4 (402)*† 41 (86)* % plants pollinated (N ) 12. d) Bower (1992. N . N .T T T T T T T T T Chiloglottis aff.Br. 2005c. (small black) Neozeleboria nr monticola 2 Tiphiidae. Orchid Table 1.P.L. Hymenoptera Lissopimpla excelsa (Costa) Ichneumonidae. Mant et al. (2007)† . Neozeleboria nr. (2008)† Coleman (1930). Spotted. Hymenoptera Tiphiidae. N .L. sp.Jones Chiloglottis (syn.Jones Biological Reviews 86 (2011) 33–75 © 2010 The Author. Hymenoptera Neozeleboria nr. valida 2 Cryptostylis erecta R. (2004)*. (2005c. impatiens. C. Hymenoptera Neozeleboria monticola Tiphiidae. Gaskett et al. Hymenoptera Thynnine wasp T Tiphiidae.

Br. Ichneumonidae. & J.) Blaxell Pterostylis acuminata R.Drumm.Clem.Drumm. (2005c).† Culex sp.P. unconf. G. unconf.) A. Thynnoides elongata† Zaspilothynnus nigripes Gu´erin T Drakaea glyptodon Fitzg. Brown pers. Zaspilothynnus nigripes Gu´erin.9 (1478) 20. (1997)*† . (2005c)* Brown et al.Stewart (syn. (2005c). Mant et al. Diptera Zaspilothynnus sp. Hymenoptera Tiphiidae. Brown et al. Hopper (2009) Mant et al. Pterostylis arenicola M.7 (1203) 20. 1979) Drakaea livida x confluens Diptera Diptera Tiphiidae. Hymenoptera T Drakaea gracilis Hopper & A. Oligochaetochilus) boormanii Rupp Pterostylis cucullata subsp.). Hymenoptera Mycetophilidae. Bates (2009b)† Orchid pollination by sexual deception 45 Biological Reviews 86 (2011) 33–75 © 2010 The Author. Hopper (2009) Peakall (1989) Stoutamire (1974. (as Drakaea elastica Lindl.George Leporella fimbriata (Lindl. Hymenoptera Zaspilothynnus trilobatus Turner*.L. Diptera Tiphiidae. Hymenoptera Culicidae. Hymenoptera Tiphiidae. in Stoutamire. Hopper & Brown (2007). ex Lindl.Clem. (syn.L. female mosquito? Mycetophilid fly Fly Fly Fly Mycomya sp.Jones & M. Sullivania) nigrita (J.*.Br. Hopper (2009) Brown et al.Jones Paracaleana hortiorum Hopper & A. Peakall (1990)*. Diplodium asperum) Pterostylis (syn. Hymenoptera Tiphiidae.Br. Mant et al. Biological Reviews © 2010 Cambridge Philosophical Society .Jones Pterostylis curta R. 3 3 unconf. unconf.P.A.L. Paracaleana (syn. dilatatus spiculifera Turner† Zaspilothynnus nigripes Gu´erin* (Thynnoides bidens inaccurate.S. 2 3 3 3 3 3 3 23. unconf. 1979). Myrmecia urens Lower Mycetophilid fly Thynnine wasp Erione sp. Labium sp.S.Diptera Mycetophilidae. comm. T T T T T T T T T T T T T Drakaea micrantha Hopper & A. Z.George Oligochaetochilus lepidus D. (1997)*.P. Hopper & Brown (2007). unconf. sylvicola D. Tiphiidae. (1997)*† .A.Br. Hymenoptera Formicidae. Hopper & Brown (2006)* Bates (2009b) Bates (2009a) Hopper & Brown (2007).Br. Diptera Tiphiidae. Diptera Mycetophilidae. Z. Drakaea thynniphila A.7 (1203) Bernhardt (1995) Bates (2009a) Bates (2009a) Bates (2009b) Coleman (1934) Bates (2009a) Brown et al. Hymenoptera Tiphiidae. (1997) Stoutamire (1974)*. dilatatus spiculifera Turner Thynnine wasp T Drakaea livida J. Oligochaetochilus arenicolus) Pterostylis aspera D. unconf.

Mant et al. National Parks & Wildlife Service (2002)* Bates (2009a) Coleman (1934) Source 46 A. Biological Reviews © 2010 Cambridge Philosophical Society T T Diptera Diptera Diptera Gnat T Mycetophilidae. Ranorchis) sargentii C.Clem.L. Hymenoptera Fly Fly Gnat Thynnoturneria sp. Diplodium) scabra Lindl.Clem. T Mycetophilidae.Jones & M. Urochilus sanguineus (D.Sarg.) D.A.P. unconf.Rogers Pterostylis gibbosa R.) Diptera Tiphiidae.Andrews Pterostylis (syn. Diptera Mycetophilidae. Spiculaea ciliata Lindl. Alcock (2000)*. Linguella) nana R.S.Rogers (syn Oligochaetochilus pusillus (R.R. (1997) Bates (2009b) Beardsell & Bernhardt (1982) Bates (2009a) Hyett (1960) Brown et al. fly† Fungus gnat T Mycetophilidae. unconf. Diptera Diptera T Fungus gnat Fungus gnat T T Fly T Mosquito-like fly Mycetophilid fly T T Heteropterna sp. (syn. unconf. Diptera Diptera Fungus gnat*.Pterostylis rufa R. (Cont. C. Brown et al.Clem.Bates (syn.Jones) R.9 (154)* % plants pollinated (N ) Brown et al. Diptera Pollinator Family. (1997)*.J.L. (syn Oligochaetochilus rufus) Pterostylis sanguinea D. (1997)† Brown et al.Br. (syn. Order T Growth form Pollinator 3 unconf.A.Coleman Pterostylis falcata R.*. Diptera Diptera Culex sp. unconf. Oligochaetochilus lepidus) Pterostylis (syn.S. Iswaroides sp. unconf.S.Jones & M.Br. 12 (490)* Pollinator sexual % flowers behaviour pollinated (N ) 25.) Pterostylis (syn. (as Pterostylis constricta O. Gaskett .) Pterostylis (syn. Diplodium) rogersii E. Urochilus) vittata Lindl.Rogers) Szlach. (1997) Sargent (1909) Beardsell & Bernhardt (1982)*.) Pterostylis (syn.L. Oligochaetochilus gibbosus) Pterostylis lepida (syn.Jones & M. 4? unconf.† T T Biological Reviews 86 (2011) 33–75 © 2010 The Author. (1997) Taylor (1999)*. female mosquito? Culicidae.Br. 4? unconf. (2005c)† Sargent (1909) Brown et al.A. Pterostylis nutans R. Orchid Table 1. Pterostylis psammophila (D.H. unconf. Oligochaetochilus psammophilus) Pterostylis pusilla R.L. 4? unconf. Diptera Mycetophilidae.Br.

T T Ichneumonidae.H. 1875) Lehnebach et al. et B). Apidae. ex Lindl.6 (4232 on 200 plants) 52. Diplodium) alobula (Hatch) L. Diptera Meliponinae. Scanlen (unpublished data) Lehnebach et al.B. Cryptostylis subulata (Labill.8 (72) 52. Trigonidium obtusum Lindley Tachinid fly Centris sp. T. H. Hymenoptera Tachinidae. Pterostylis (syn. (syn. Diptera Tachinidae.K.f. 2 2 2 1? ? 2 unconf. Fungus gnat† Fungus gnat T Pterostylis patens Colenso Mycetophilidae. Tachinid fly E E Sciaridae. (2004) Blanco & Barboza (2005) Calvo (1990) Ciotek et al. Oncidium) henekenii (R. van der Cingel (2001) Dod (1976) Singer et al. Scanlen (unpublished data)† Lehnebach et al.) Scoliidae.) T Pterostylis trullifolia Hook. Biological Reviews © 2010 Cambridge Philosophical Society .) Rchb.) Hoehne ex Correa Epidendreae Central America Lepanthes glicensteinii Luer Lepanthes wendlandii Reichb.? E Telipogon sp. f. Hymenoptera Mycetophilidae.f.?*. 4? 4? 4? 4? 1? 41 (24) 11.Tachinidae.2 (57) 41.Moore Pterostylis australis Hook. parviflora) (H. van der Cingel (2001) Christensen (1994).2 (57) <25% 41. Diptera Lissopimpla excelsa (Costa) T Pterostylis graminea Hook. (2005) E. (2006) Cheeseman (1872.Schomb. Hymenoptera Paragymnomma sp. Plebeia droryana Friese E E Tolumnia (prev.B. Keratophilidae.). Diptera Anthophoridae. f.f. Diplodium trullifolium) South America Geoblasta pennicillata (Rchb. Scaptotrigona sp.8 (72) Singer (2002) Dodson (1962). Hymenoptera Campsomeris bistrimacula (Lep. E. (2005)*.6 (24) 2.6 (24) 2.f. Diptera Bradysia floribunda Mohrig E E South and Central America Mormolyca ringens (Lindl. (2005) Graham (1983) Orchid pollination by sexual deception 47 Biological Reviews 86 (2011) 33–75 © 2010 The Author. Diptera Zygomyia sp. New Zealand 2&4 2 unconf. van der Cingel (2001) Christensen (1994). Diptera Mycetophilidae.) Trichoceros antennifera (prev. E E Stellilabium sp. (E) Maxillarieae Fungus gnat? T T Aneura longipalpis Tonnoir & Edwards?* Cerotelion sp. Hymenoptera Nannotrigona testaceicornis (Lep.

Tyteca.) Colletidae. Widmer et al. Segers & H. Biological Reviews © 2010 Cambridge Philosophical Society Eucera nigrilabris Lep. Andrena bimaculata (Kirby) T Ophrys africana G.). Eucera punctulata Alfken?† Eucera barbiventris P´erez T Ophrys archipelagi G¨olz & H. Colletidae. Hymenoptera Ophrys aesculapii Renz Anthophora orientalis Morawitz Eucera taurica Morawitz Pollinator Family.Philippe T T Eucera sp.Biological Reviews 86 (2011) 33–75 © 2010 The Author. (2005) Delforge (2005) Delforge (2005) Delforge (2005).Reinhard Ophrys aegirtica P. Hymenoptera Anthophoridae. Hymenoptera Andrenidae.) T T Colletes sp. Hymenoptera Anthophoridae. Delforge (2005)* Paulus & Gack (1990). (Cont. Hymenoptera Andrena paucisquama Noskiewicz Andrena flavipes Panzer T Anthophoridae.Danesch & E.Foelsche Ophrys alasiatica Kreutz. Megachilidae. C.Walraven Ophrys algarvensis D. Paulus (2000)† Paulus & Gack (1990) Delforge (2005) Paulus (2006) Delforge (2005) St¨okl et al.Danesch & E. T Ophrys araneola Rchb. Delforge (2005) Delforge (2005) Paulus & Gack (1990)*. Hymenoptera T T T T T Ophrys apiformis Steud. Paulus (2006) Source 48 A. & M.Danesch Ophrys arachnitiformis Gren. Hymenoptera Anthophoridae. Anthophoridae. Order T T Growth form Pollinator Ophrys aegaea Kalteisen & H. Andrenidae. Andrena lathyri Alfken† .Reinhard Ophrys argentaria Devillers-Tersch. (2000). Hymenoptera Megachilidae. Benito & M. trimmerana. Synhalonia) rufa (=Tetralonia berlandi Dusmet) Andrenidae. inaccurate according to Hymenoptera Paulus (2000). Ophrys aprilia Devillers & Devillers-Tersch. Colletes cunicularius (L. Delforge (2005)† . Hymenoptera Andrenidae. Andrena sabulosa subsp. Gaskett .*. Andrena combinata (Christ)‡ Colletes cunicularius (L.Foelsche & W.R. & Devillers Osmia rufa (L. Ophrys apulica (O. (1976b)*. Eucera ( prev. Delforge (2005) Delforge (2005) Kullenberg & Bergstr¨om.Danesch) O. Hymenoptera Andrenidae.R. & Devillers Ophrys apifera Huds.Delforge Orchideae Europe Orchid Table 1.) 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 Pollinator sexual % flowers behaviour pollinated (N ) % plants pollinated (N ) Paulus & Gack (1990).Walravens Ophrys annae Devillers-Tersch. Hymenoptera Andrena fulvata Stoeckhert Andrenidae. Hymenoptera Anthophoridae. Osmia Hymenoptera aurentula* (probably = Osmia aurulenta Panzer) Osmia bicolor (Schrank)∗ Megachilidae. Hymenoptera Colletidae. Schiestl & Vereecken (2008)‡ Kullenberg (1961).

Delforge (2005)† Paulus (2000. Paulus (2006) Paulus & Gack (1990).Danesch Ophrys biancae Macch. C.) Buttler Ophrys balearica P.Paulus (as O.Wood) H.) Eucera seminuda Brull´e Anthophoridae.J. Hymenoptera Andrenidae.) T T Andrena vetula Lep. Hymenoptera Megachilidae. pyrenaica (Lep.) Andrena hattorfiana (Fabricius) T Anthophoridae. Hymenoptera Megachilidae. Paulus (2006) Delforge (2005) Delforge (2005). Delforge (2005). Ophrys aurelia P.F. & Devillers Ophrys aveyronensis (J. Delforge (2005). Paulus (2006) Paulus & Gack (1990). Delforge (2005) Delforge (2005). Delforge (2005)* Orchid pollination by sexual deception 49 Biological Reviews 86 (2011) 33–75 © 2010 The Author.Delforge. Hymenoptera Andrenidae. Hymenoptera Anthophoridae. Devillers-Tersch. Hymenoptera Anthophoridae. albovaria T Chalicodoma parietina (Geoffr.Reinhard Ophrys battandieri E. Paulus (2006) Delforge (2005) Paulus & Gack (1990). karpathensis E. ex Vierh.Danesch & E.Fleischm.Danesch & E.Chalicodoma sicula (Rossi) T T T Ophrys bilunulata Risso Ophrys biscutella O. 2006). Delforge (2005) Delforge (2005) Paulus & Gack (1990)*.). T Ophrys bertoloniiformis O. Hymenoptera Andrenidae.) O.) Andrena flavipes Panzer Eucera euroa Tkalcu˚ Chalicodoma parietina (Geoffr. Hymenoptera Megachilidae.Baumann & K¨unkele Ophrys aymoninii (Breistr.) Ophrys benacensis (Reisigl. benoisti Tkalcu˚ † T Anthophora retusa (L. pyrenaica (Lep.) Chalicodoma sicula (Rossi)*. Delforge (2005) Paulus & Gack (1990).Alibertis & H. C. Paulus (2006) Paulus & Gack (1990). Hymenoptera Anthophora plagiata (Illiger) T Ophrys argolica H. Hymenoptera Andrenidae.Danesch Ophrys bertolonii Moretti Andrena combinata (Christ) T T Chalicodoma parietina (Geoffr. Delforge (2005).Delforge Andrenidae. Hymenoptera Megachilidae. Ophrys basilissa A. Biological Reviews © 2010 Cambridge Philosophical Society . Hymenoptera Megachilidae. Hymenoptera Melecta albifrons subsp. Hymenoptera Megachilidae.Danesch & E.Delforge 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 Schiestl & Ayasse (2002). Delforge (2005).R.). & Orph. hybr.G.Danesch Chalicodoma parietina (Geoffr.Nelson*) Ophrys arnoldii P. Delforge (2005) Delforge (2005) Paulus & Gack (1990). St¨okl et al. Hymenoptera Anthophoridae.Camus (pro. Hymenoptera Anthophoridae. Ophrys ariadnae H. cretica subsp. C. (2005) Paulus & Gack (1990). Hymenoptera T Ophrys atlantica Munby T Andrena nigroaenea (Kirby) T Ophrys attica Boiss. Delforge (2005) Paulus & Gack (1990).? T T Anthophora nigrocincta Lep.

Hymenoptera Bombus vestalis (Geoffr.Danesch) P. & P. Hymenoptera Eucera hispana Lep. Hymenoptera Pollinator Family. hispana Lep.? T T T T Anthophoridae. E. Wood) G¨olz & H. Gaskett . Paulus (2000)† Paulus & Gack (1990)*. & Devillers Ophrys calypsus M. Hymenoptera ˚ Eucera paulusi Tkalcu*. Biological Reviews © 2010 Cambridge Philosophical Society Ophrys crabronifera Sebast. Ophrys blitopertha Paulus & Gack Ophrys bombyliflora Link Orchid Table 1.*.Reinhard Ophrys calocaerina Devillers-Tersch.) T Andrena cinereophila War. Paulus & Gack (1990)† . E. T T Andrena creberrima P´erez*† . Hymenoptera Anthophoridae. Delforge (2005) Delforge (2005) 2 Source Paulus (2001). Matth¨as & Risse Ophrys celiensis (O.R. b). Eucera sp. Devillers-Tersch. penicillata Risch† Eucera curvitarsis Mocz. Hymenoptera Andrenidae.Delforge Ophrys cerastes Devillers & Devillers-Tersch. Delforge (2005) % plants pollinated (N ) 2 21. 2009). plumigera? T T Anthophoridae.Danesch & E. G¨ogler et al. flavipes Panzer* T T Sphecidae. & Devillers Ophrys cilicica Schltr. Paulus (2006) Paulus & Gack (1990). Hymenoptera Andrena florentina Magretti T T Apidae. Devillers.) Andrena labialis (Kirby)? Eucera dalmatica Lep.3 (122 on 37 plants)* Pollinator sexual % flowers behaviour pollinated (N ) 50 A. T T Scarabaeidae. E. Anthophoridae. E. algira Brull´e† .Delforge Ophrys chestermanii (J. E.J. & Mauri Ophrys creberrima Paulus (as Ophrys fusca (small)?*) Ophrys cinereophila Paulus & Gack Ophrys cornutula Paulus Ophrys bornmuelleri M.Spaethe Ophrys candica Greuter. Coleoptera Anthophoridae. (2009) Delforge (2005) Paulus & Gack (1990). Hymenoptera Anthophoridae. Hymenoptera Anthophoridae.Schulze Ophrys bucephala G¨olz & H. Hymenoptera Eucera puncticollis Mor. Hymenoptera ˚ Eucera euroa Tkalcu?.† .R. Hymenoptera Andrenidae. Delforge (2005)† Delforge (2005). Delforge (2005) Delforge (2005) 2 2 Paulus & Gack (1990) Delforge (2005) 2 2 2 2 2 Kullenberg & Bergstr¨om (1976a. Anthophoridae. Neiland & Wilcock (1998)*. Hymenoptera Anthophoridae. (Cont. Hymenoptera Argogorytes sp. Delforge (2005) Delforge (2005) Delforge (2005) Delforge (2005).Hirth & H.Reinhard Ophrys cilentana Devillers-Tersch. A. Order Blitopertha lineolata (Fischer von Waldheim) Eucera oraniensis Lep. (as Ophrys cornuta (small)?*) Ophrys ceto P.† Hymenoptera Eucera graeca Radoszkowski Anthophoridae. C. signifera Anthophora plumipes (Pallas) Andrenidae. Delforge (2005)† Paulus & Gack (1990). T Eucera punctulata Alfken. Hymenoptera Anthophoridae.∗ T Growth form Pollinator 2 2 2 2 2 2 2 2 Paulus & Gack (1990)*. Paulus (2006) Paulus (2001.Biological Reviews 86 (2011) 33–75 © 2010 The Author.

) Anthophora erschowi Fedtschenko Andrena morio Brull´e Eucera ( prev. inaccurate according to (Delforge. Paulus (2001. Hymenoptera Anthophoridae. Paulus (2001).) Ophrys discors Bianca (syn. Hymenoptera Andrenidae.Delforge T Ophrys cressa Paulus Anthophoridae. Hymenoptera Megachilidae.? Ophrys cretensis (Baumann & K¨unkele) Paulus Ophrys cretica (Vierh. creticola Melecta tuberculata Lieftinck T Andrena merula War. Delforge Ophrys fabrella Paulus & Ayasse ex P.Danesch (pro hybr. T Chalicodoma sicula (Rossi) T Ophrys exaltata Ten. Delforge (2005) Delforge (2005). Hymenoptera Anthophoridae. 2009).) E. Hymenoptera Megachilidae. Delforge (2005) Delforge (2005) Delforge (2005) Paulus & Gack (1990). Hymenoptera Apidae. Biological Reviews © 2010 Cambridge Philosophical Society . T Andrena vachali subsp. (2005b) Delforge (2005) Paulus & Gack (1990)* Delforge (2005) Paulus & Gack (1990). Hymenoptera Colletidae. Hymenoptera Anthophoridae.) P. Ophrys flavomarginata (Renz) H. Hymenoptera 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 Delforge (2005). Hymenoptera Megachilidae.) T T T T T T T T Ophrys dyris Maire Ophrys elatior Gumpr. todaris) Ophrys drumana P. Hymenoptera Anthophoridae. 2005) Colletes cunicularius (L.Baumann & K¨unkele Ophrys eleonorae Devillers-Tersch.Danesch & E. Hymenoptera Apidae. Hymenoptera Andrenidae. Paulus (2000). Delforge (2005) Delforge (2005) Paulus & Gack (1990). O. Delforge (2005) Paulus & Gack (1990). Hymenoptera Anthophoridae. Baumann & K¨unkele Ophrys fleischmannii Hayek Anthophora sicheli Radoszkowski Andrena fabrella P´erez T Ophrys explanata (Lojac. Synhalonia) rufa (=Tetralonia berlandi Dusmet)*. ex. & Devillers Ophrys episcopalis Poir (as O.Anthophora plagiata (Illiger) Eucera euroa Tkalcu˚ Chalicodoma albonotata (Radoszkowski) Anthophora atroalba Lep. Delforge (2005) Paulus & Gack (1990).) Chalicodoma manicata (Giraud) Eucera dimidiata Brull´e T T T T Ophrys flavicans Vis. Hymenoptera Andrenidae.Nelson Ophrys delphinensis O. Paulus (2006) Delforge (2005). Hymenoptera Megachilidae. Mant et al. Delforge (2005). Paulus (2006) Paulus & Gack (1990). Tetralonia salicariae (Lep. Delforge (2005) Paulus & Gack (1990). Hymenoptera Andrenidae. Delforge Ophrys ferrum-equinum Desf. Paulus (2006) Paulus & Gack (1990). Hymenoptera Anthophoridae. Delforge (2005) Delforge (2005) Orchid pollination by sexual deception 51 Biological Reviews 86 (2011) 33–75 © 2010 The Author. Paulus Ophrys elegans (Renz) H. episcopalis (maxima)∗) Chalicodoma parietina (Geoffr.

Willing & E.) 2 2 2 2 2 2 2 2 2 2 2 2 2 2 5.Kretzschmar Ophrys hebes (Kalopissis) E. Schiestl & Ayasse (2002). Hymenoptera Anthophoridae. longicornis (L. Hymenoptera Andrenidae. & Devillers Ophrys gottfriediana Renz T Ophrys fusca Link Anthophoridae. Colletes cunicularius (L. trimerana Hymenoptera Andrena wilkella (Kirbyi) Andrenidae. E. Ophrys garganica E. A.) Ophrys gackiae P. Delforge (2005). Biological Reviews © 2010 Cambridge Philosophical Society Ophrys grigoriana G.)*. Hymenoptera Anthophoridae. (2006)† .Englmaier Ophrys grammica (B. (2005)* Delforge (2005) Paulus (2006) Delforge (2005) Paulus & Gack (1990) Delforge (2005) Paulus (2000) Paulus & Gack (1990) Paulus & Gack (1990). Hymenoptera Chalicodoma sp. Hymenoptera Andrena flavipes Panzer Andrena florentina Magretti? Andrenidae.Willing Ophrys gracilis (B¨uel & Danesch) P. Andrenidae. T T Andrenidae. Hymenoptera Eucera nigrescens P´erez*. Order T T T T Growth form Pollinator Ophrys fuciflora (F. Coleoptera Phyllopertha horticola (L.Kretzschmar & H. Delforge (2005)*. Hymenoptera Andrena carbonaria (L.45 (463 plants)‡ Pollinator sexual % flowers behaviour pollinated (N ) % plants pollinated (N ) Paulus & Gack (1990). Anthophoridae. herae*. Gaskett .) Andrenidae. Hymenoptera Pollinator Family.) Andrena symphiti Schmiedeknecht T T T T Megachilidae. fusca (Ophrys sulcata Devillers & Devillers-Tersch.Danesch & E. Hymenoptera Eucera clypeata Erichson? Andrena nigroaena (Kirby) Eucera algira Brull´e? Xylocopa violacea (L.Schmidt) Moench Orchid Table 1. florentina Magretti Hymenoptera Andrena sabulosa subsp. C. according to Paulus (2006) Ophrys grandiflora Ten. & Devillers (as O.Nelson ex O. (2009)‡ Source 52 A.W. St¨okl et al. Microdon Hymenoptera latifrons Loew*. Andrenidae.Willing & B. Scarabaeidae. (2005) Paulus & Gack (1990) Kullenberg & Bergstr¨om (1976a. St¨okl et al.)† Andrena nigroaenea (Kirby).)*.) Colletidae. Andrenidae. Tyteca et al. (Cont.Delforge Biological Reviews 86 (2011) 33–75 © 2010 The Author.Danesch Ophrys gazella Devillers-Tersch. Hymenoptera Andrenidae. mutabilis (L. Vanderwoestijne et al.T T T Ophrys fusca (type II Sicily) Ophrys fusca (type III Sicily) Ophrys cf. b). M. Delforge (2005) Paulus (2006) Delforge (2005) Delforge (2005)*. Hymenoptera Andrena thoracica Fabricius.Willing) Devillers-Tersch.

Hymenoptera Andrenidae. Coleoptera Anthophoridae.) Andrena morio Brull´e T T Ophrys integra (Moggr. E. 2006‡ ) Paulus & Gack (1990). Coleoptera Syrphidae. Paulus (2001). Delforge (2005) Paulus (2006) Delforge (2005) Delforge (2005) Paulus & Gack (1990)† . Wolff (1950)*. Andrenidae. Kullenberg (1961). Delforge (2005) Paulus & Gack (1990). Hymenoptera Andrenidae. Hymenoptera Sphecidae. Delforge (2005). Kullenberg & Bergstr¨om (1976a. b)† . Delforge (2005).‡ Andrena morio Brull´e Eucera (Synhalonia) cressa? T Ophrys helenae Renz Eucera (prev. St¨okl et al. (2007). Hymenoptera Colletidae. Paulus (2000). Hymenoptera Anthophoridae. Eucera &Tetralonia sp. (2009)* Orchid pollination by sexual deception 53 Biological Reviews 86 (2011) 33–75 © 2010 The Author. Vanderwoestijne et al. Anthobium minutum F. Hymenoptera Andrenidae.L.) Paulus & Gack Ophrys iricolor Desf. Hymenoptera 2 2 2 2 2 2 2 2 2 2 2 2 2 2 15.Hirth & H. Cortis et al. Hymenoptera. mystaceus (L.*. Delforge (2005).)† . A. Delforge (2005) Paulus & Gack (1990). (2009) Darwin (1885)*.Andrena thoracica (Fabricius) Eucera cypria Alfken T T T Ophrys helios Kreutz Ophrys herae M. (2005) Paulus & Gack (1990). (2009) Paulus & Gack (1990). Staphylinidae. St¨okl et al. (2007)*. (2009)* Paulus & Gack (1990) Paulus & Gack (1990)*. longicornis (L. and rarely Phyllopertha horticola (L. Synhalonia) rufa (=Tetralonia berlandi Dusmet)∗† . Scarabaeidae.)? T Ophrys heldreichii Schltr.Fleischm. Hymenoptera. Colletes cunicularius (L. Hymenoptera Anthophoridae. Paulus (2000† . Hymenoptera Andrenidae.Burm.f. Hymenoptera Anthophoridae.1 (2775 plants)* Paulus & Gack (1990).) T Ophrys insectifera L. Spaethe et al. Diptera Andrenidae.). ˚ Agren & Borg-Karlson (1984). Tod. Delforge (2005) Delforge (2005) Paulus & Gack (1990).R. Tetralonia alternans ( Brull´e)† Eucera longicornis (L.Baumann & K¨unkele Ophrys kotschyi H. Biological Reviews © 2010 Cambridge Philosophical Society . & So´o Ophrys lacaitae Lojac. Hymenoptera Anthophoridae. (Staphylinidae)† T Ophrys incubacea Bianca ex. Hymenoptera Anthophoridae. Andrena curiosa (Morawitz) T Eucera eucnemidea Dours T Andrena schulzi Strand Melecta tuberculata Lieftinck T T Andrena flavipes Panzer T Argogorytes fargeii (Shuckard). Eucera clypeata Erichson† . Ophrys laurensis Geniez & Melki Ophrys lesbis G¨olz & H. Paulus (2001).Delforge Ophrys holoserica (N.Reinhard Ophrys israelitica H. Streinzer et al.Spaeth Ophrys heterochila (Renz & Taubenheim) P. & Rchb. Hymenoptera Apidae. Delforge (2005)*.)‡ & Microdon sp. Cortis et al.

Hymenoptera Megachilidae.Delforge. Hymenoptera T Andrenidae. S. Hymenoptera Osmia kohlii Ducke T T Andrena cinerea Brull´e† . A.R. senecionis P´erez† . Morawitz Hymenoptera Eucera graeca Radoszkowski Anthophoridae.R¨uckbr. & Devillers Ophrys lutea subsp. melena Renz) Ophrys lyciensis Paulus.Delforge Orchid Table 1. clypella Strand.cinerophila War.Delforge Ophrys leucadica Renz (pro hybr. Hymenoptera Andrenidae. (Cont. A. Devillers-Tersch. Ophrys lupercalis Devillers-Tersch.R¨uckbr. Pollinator Family. A. Gaskett . b). Delforge (2005) Delforge (2005) Delforge (2005). humilis subsp. Hymenoptera Andrena flavipes A.G¨ugel. Delforge (2005)† Source 54 A. Ophrys lucana P.) Devillers-Tersch. Order Andrena vulpecula Kriechbaumer Anthophora cf. Delforge (2005) Delforge (2005) Kullenberg & Bergstr¨om (1976a. R¨uckbrodt & R¨uckbrodt (2001).) Megachilidae. Paulus & Gack (1990)*. Delforge (2005) Paulus.Foelsche & W. Hymenoptera Anthophoridae. D. hasitata.Reinhard) Paulus & Gack Ophrys lunulata Parl.∗ Andrena transitoria Andrenidae. prunella*. Hymenoptera Andrenidae. & U. Delforge (2005) Paulus & Gack (1990). Delforge (2005)† Paulus & Gack (1990). Borg-Karlson & T¨engo (1986). Andrenidae. A. creberrima P´erez† ? Hymenoptera Andrena ocreata (Christ)? Andrenidae. A.) Ophrys lojaconoi P. Ophrys lucis (Kalteisen & H. nigroolivacea Dours† ?. Hymenoptera Panzer*† . Hymenoptera Andrenidae. Biological Reviews © 2010 Cambridge Philosophical Society Ophrys marmorata G. mucida T T T Growth form Pollinator 2 2 2 2 2 2 2 2 2 2 2 2 2 2 Pollinator sexual % flowers behaviour pollinated (N ) % plants pollinated (N ) Delforge (2005) Vereecken & Patiny (2006) Paulus & Gack (1990). G¨ugel. Hymenoptera Colletidae. C. A. & Devillers Ophrys lucentina P. humilis Imhoff∗ . Andrenidae. Hymenoptera Andrena wilkella (Kirby) Andrena bicolor Fabricius Chalicodoma sicula (Rossi) T T T T Andrena fuscosa Erichson T T Andrena nigroaenea (Kirby) T T Andrenidae. & Devillers Ophrys lutea Cav. Paulus (2006) Delforge (2005) Delforge (2005) Delforge (2005) Paulus (2001)*. panurgimorpha Mavromoustakis∗ . A. Bourn´erias & Prat (2005).Biological Reviews 86 (2011) 33–75 © 2010 The Author. Hymenoptera Andrena labialis (Kirby) Andrenidae. Ophrys mammosa Desf.Foelsche Ophrys massiliensis Viglione & V´ela Ophrys melitensis (Salk.

Wood (pro hybr. Hymenoptera Andrenidae. A.) Ophrys obaesa Lojac.Fleischm. Delforge (2005) Delforge (2005) Paulus & Gack (1990)*. Hymenoptera Andrenidae. Hymenoptera Osmia rufa subsp. omegifera subsp. Hymenoptera Anthophoridae. sabulosa (Scopoli)† . Hymenoptera Andrenidae. Hymenoptera Colletidae. Hymenoptera Megachilidae.Keller & So´o Ophrys murbeckii H.) Ophrys panormitana (Tod.Fleischm. Ophrys neglecta Parl.Danesch (pro hybr. T T T Colletidae. trimerana* Andrena thoracica (Fabricius). florentina Magretti*. Hymenoptera Andrenidae. nigroaenea (Kirby)? Eucera nigrescens P´erez T Ophrys panattensis Scrugli.Grasso & Manca Ophrys oxyrrhynchos Tod. dyris (Maire) Del Prete Ophrys ortuabis M.) Andrena flavipes Panzer T T T T T T Ophrys panormitana var. oraniensis Lep. nigriceps Mor. omegaifera in Paulus & Gack 1990) Ophrys omegaifera subsp. Hymenoptera Anthophoridae. Biological Reviews © 2010 Cambridge Philosophical Society . Pessei & Cogoni (pro hybr. G¨ogler et al. E. Paulus (2006) Paulus & Gack (1990) Paulus & Gack (1990). Ophrys normanii J.) Ophrys morio Paulus & Kreutz Ophrys morisii (Martelli) G. Delforge (2005) Paulus & Gack (1990). Hymenoptera Anthophoridae.Delforge Ophrys parvimaculata (O. rufa T Ophrys pallida Raf. Hymenoptera Apidae.Andrenidae.? Bombus vestalis (Geoffr. Hymenoptera Anthophoridae.P. A. (2009) Paulus & Gack (1990). Delforge (2005) Delforge (2005) Paulus (2006) Delforge (2005). Eucera clypeata Erichson. (as O. Paulus (2006) Delforge (2005) Delforge (2005). Hymenoptera Colletes cunicularius (L. sabulosa subsp. praecox (Corrias) P. atroalba Andrena hypopolia Smiedeknecht Eucera graeca Radoszkowski T T Anthophoridae.Danesch) Paulus & Gack Andrena thoracica (Fabricius)*† . Delforge (2005)† Paulus & Gack (1990). A. Delforge (2005) Delforge (2005). A. Hymenoptera Andrena morio Brull´e Anthophora sicheli Radoszkowski Colletes sp.Danesch & E. 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 Paulus & Gack (1990). Hymenoptera Anthophora atroalba subsp.) T Ophrys omegaifera H. Paulus (2006) Delforge (2005) Delforge (2005) Orchid pollination by sexual deception 55 Biological Reviews 86 (2011) 33–75 © 2010 The Author. Hymenoptera Andrenidae. Ophrys montis-leonis O. A. agamoides.) So´o T T Andrena orbitalis Morawitz Anthophoridae.Danesch & E.J. Anthophora atroalba subsp.

Hymenoptera Andrenidae. Hymenoptera Melecta sp. merula War. O. Eupavlovskia obscura Friese‡ . Gaskett . vulpecula Kriechbaumer*‡ .Danesch & E.) 2 2 2 2 2 2 2 2 2 2 2 2 2 Pollinator sexual % flowers behaviour pollinated (N ) % plants pollinated (N ) Paulus & Gack (1990)*.)*. A.Nelson ex.Andrena carbonaria (L. Hymenoptera Andrenidae. Order Ophrys picta Link Andrena carbonaria (L. Anthophoridae. (Hetereucera) elongatula Vachal† Eucera clypeata Erichson Andrena hesperia Sm. A. Hymenoptera Andrenidae. Hymenoptera Anthophora atriceps P´erez T Ophrys sabulosa Paulus & Gack ex P. Paulus (2001)‡ . Hymenoptera Andrenidae.*†‡ . E.*. tadauchii Gusenleitner.Danesch Ophrys provincialis (Baumann & K¨unkele) Paulus Ophrys reinholdii Spruner ex.‡ . Hymenoptera Megachilidae. T Growth form Pollinator Ophrys parvula Paulus Orchid Table 1. Hymenoptera Megachilidae. Anthophoridae. A. & Devillers Chalicodoma albonotata (Radoszkoski) Eucera longicornis (L.Camus (pro hybr. Boiss. Paulus Ophrys sicula Tineo (as O. taraxaci Giraud‡ .Delforge Ophrys phryganae Devillers-Tersch. A. (2007)† Delforge (2005) Kullenberg & Bergstr¨om. interrupta Baer*. sicula (minor)*) T T Anthophoridae. Eucera nigrescens P´erez*. Biological Reviews © 2010 Cambridge Philosophical Society T Ophrys serotina H. Delforge (2005) Delforge (2005) Delforge (2005) Delforge (2005) Delforge (2005) Paulus (2001): Delforge (2005) Source 56 A.) Ophrys scolopax Cav. garganica (E. C. b)*.) T Ophrys passionis Sennen Andrena tomora War. E. E. Hymenoptera Osmia mustelina Gerstaecker T Ophrys promontorii O. Paulus & Gack (1990)† .Rolli ex H. (Cont. Paulus & Gack (1990)*. humilis Imhoff. Paulus (2006) Paulus & Gack (1990). Hymenoptera T Andrenidae. bicolor Fabricius‡ ? T Biological Reviews 86 (2011) 33–75 © 2010 The Author.Danesch & E. clypella subsp. A. Vereecken et al. A. Danesch) P. hasiata? Eucera barbiventris P´erez T T Ophrys passionis var.?‡ Andrena sabulosa (Scopoli) T T Anthophoridae. Hymenoptera Anthophoridae.Delforge Ophrys saratoi E. funeraria Sm. (1976a. Hymenoptera Pollinator Family. Delforge (2005)‡ Delforge (2005) Delforge (2005). Delforge (2005)‡ Paulus (2000) Kullenberg & Bergstr¨om (1976a.) Andrena panurgimorpha Mavromoustakis. A. Hymenoptera Andrenidae.F. Delforge (2005)*. Paulus (2001)† . b)*. Anthophora obscura† .G.

Reinhard Ophrys tarquinia P. Hymenoptera Andrenidae. Bourn´erias & Prat (2005).Lorenz & Gembardt Ophrys sitiaca Paulus. (2003) Paulus (2009) Paulus & Gack (1990).04 (235 plants)† Paulus & Gack (1990). Hymenoptera Anthophoridae.03 (3000)‡ 12. A. A. Hymenoptera Anthophoridae. Tyteca et al.)*. Hymenoptera Argidae.Hermos. (2009)† Paulus & Gack (1990). E. Delforge (2005) Delforge (2005) Delforge (2005) Delforge (2005) Delpino (in Darwin (1885) as O. cineraria (L. Hymenoptera Scoliidae. & J. orientalis (Paulus) Paulus & Salkowski Ophrys sphegifera Willd. barbilabris (Kirby)*. A.R. Delforge (2005) Paulus & Gack (1990). E. limata Eversmann* T Ophrys sphegodes Mill. Ayasse et al. A. C.R. T Dasyscolia ciliata (Fabricius) (as Campsoscolia ciliata) Dasyscolia ciliata subsp.5 (20 on 13 plants)* 0.Alibertis & A. Delforge (2005). (2000) Paulus & Gack (1990). Paulus (2000)† . Hymenoptera Andrenidae. Hymenoptera Eucera notata Lep. Hymenoptera Xylocopa iris (Christ) T Ophrys speculum subsp. Neiland & Wilcock (1998)*.Delforge Andrena nigroaenea (Kirby)*† .Danesch (pro hybr. Eucera nigrilabris Lep. araratensis T T Scoliidae. Hymenoptera Andrenidae. dimidiata Brull´e. St¨okl et al.Danesch & E. Bourn´erias & Prat (2005). A. clypeata Erichson. & Devillers Ophrys tardans O. Widmer et al.Reinhard Ophrys spruneri Nyman Osmia tricornis Latreille Andrena tibialis (Kirby) T T T Ophrys tenthredinifera Willd.9 (963)* 17. A. (1997)*. Vanderwoestjine et al. aranifera Huds. Hymenoptera Andrena nigroaenea (Kirby) T Anthophoridae. (2005) Orchid pollination by sexual deception 57 Biological Reviews 86 (2011) 33–75 © 2010 The Author. Delforge (2005). Hymenoptera Andrenidae. wilkella (Kirby) Eucera taurica Morawitz? T T Sterictiphora furcata (Villers) T Ophrys subinsectifera C. Ophrys sipontensis R. (2006) Delforge (2005) Kullenberg & Bergstr¨om (1976a. ovulata (Kirby).Andrena squalida Olivier Xylocopa iris (Christ) T T Ophrys splendida G¨olz & H. thoracica (Fabricius)*.) Ophrys tarentina G¨olz & H. Delforge (2005) Paulus & Gack (1990). Hymenoptera Anthophoridae. Ayasse et al. Paulus & Gack (1990). Hymenoptera Andrenidae. Hymenoptera Anthophoridae.Sabando Ophrys sulcata Devillers-Tersch.)‡ . Megachilidae. Biological Reviews © 2010 Cambridge Philosophical Society . b). Neiland & Wilcock (1998)*. E. algira Brull´e? Andrena flavipes Panzer.E.Alibertis Ophrys speculum Link 2 2 2 2 2 2 2 2 2 2 2 2 2 2 55. Delforge (2005) Delforge (2005).

Delforge (2005)† Source Delforge (2005) % plants pollinated (N ) 2 2 2 2 2 2 Pollinator sexual % flowers behaviour pollinated (N ) 58 A. (various forms) Ophrys zonata Devillers-Tersch. A. Eucera penicillata Risch‡ Eucera clypeata Erichson Anthophoridae. rufitarsis Friese. Hymenoptera Andrena morio Brull´e*. C. Andrena bicolor Fabricius? Andrenidae. E. fuscosa Erichson† ? Hymenoptera Eucera gaullei Vachal.P.Teschner Orchid Table 1.) 2 2 2 2 7.5 (2146 on 129 plants)* Bino et al. E.Paulus T T Pollinator Family. Biological Reviews 86 (2011) 33–75 © 2010 The Author.T T T Ophrys thriptiensis Paulus Ophrys tommasinii Visiani Ophrys transhyrcana Czerniak. (as Campsoscolia ciliata) Hymenoptera Anthophoridae. but reports of Tetralonia ruficornis (Fabricius)∗ are inaccurate‡ . Neiland & Wilcock (1998)* Delforge (2005) Paulus (2009) 2 Paulus & Gack (1990)*. Ophrys umbilicata Desf. galilaea Tkalcu. & Devillers Orchis galilaea (Bornm¨uller et Schultze) Schlechter T T T Ophrys untchjii (M. Hymenoptera Apidae. Hymenoptera E. Ophrys villosa Desf. Biological Reviews © 2010 Cambridge Philosophical Society T T T Ophrys vernixia Brot. Hymenoptera Growth form Pollinator Ophrys tetraloniae W.Delforge Ophrys urteae H. E. spatulata Gribodo. Hymenoptera Andrena pandellei P´erez Andrenidae. bidentata P´erez. Tetraloniella fulvescens Hymenoptera (Giraud) (prev.F. Andrenidae. Hymenoptera E. curvitarsis Mocsary? Andrena flavipes Panzer Andrenidae. nigrilabris Lep. Eucera dimidiata Brull´e.6 (475 on 105 plants)* 27. Delforge (2005)† Paulus & Gack (1990)*. Tetralonia f. seminuda Brull´e. E.Schulze) P. Delforge (2005) Delforge (2005) Paulus & Gack (1990). (Cont. Blitopertha nigripennis Reitter Coleoptera Dasyscolia ciliata (Fabricius) Scoliidae. Paulus (2000)‡ . (1982)*. Anthophoridae. Order Lassioglossum marginatum Brull´e (prev. Halictus (Evylaeus) marginatus) Halictidae. Delforge (2005)† . Hymenoptera Scarabaeidae. Paulus (2009)‡ Paulus (2000) Delforge (2005) Paulus & Gack (1990)*. Eucera inulae† . Gaskett .)*. Eucera fulvescens Giraud† . ˚ E.

see Table 1 for pollinator species. normanii are genetically distinct. an insect. 2. 2009).. floral height.. 1. and solitary rather than social (Gaskett. post-pollination isolation factors have been suggested for two pairs of sympatric Ophrys species from Sardinia: Ophrys chestermanii and O. The few reports of female insects visiting orchids in potentially sexually Biological Reviews 86 (2011) 33–75 © 2010 The Author. but do not hybridise in nature or when cross-pollinated by hand (Dacy. no other vertebrates such as rodents or bats are reported as orchid pollinators. In many Australian orchid species. Most photographs by Julia Cooke. Biological Reviews © 2010 Cambridge Philosophical Society . are remarkably morphologically disparate. et al. 2002. Johnson & Brown. male Bombus vestalis (G¨ogler et al. incubacea are natural hybrids that are also similarly scented and share their pollinator. 1995). 2008). leptochila. Less commonly. Molloy & Beuzenberg. 2007. the labellum is attached by a flexible hinge. 2008). Examples of orchids with hinged labellae are (A) Paracaleana nigrita (B) Drakaea glyptodon. 2000. 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. (1) Pollinator identities Although some rewarding orchid species are pollinated by birds (Singer & Sazima. (C) C. Ichneumonidae). families and orders). 2008.Orchid pollination by sexual deception Fig. a common mechanism of incompatibility in food-deceptive orchid species (Dawson. Mant et al. 2009).. and (D) C. the petals are folded into a hood and a sensitive labellum can act as a trap door and detain pollinators briefly within the hood. 2006. and Ophrys iricolor and O. 1988. Avoidance of cross-pollination (prepollination or pre-zygotic isolation) is generally achieved via differences in scent compounds or odour blends (e. male Andrena morio (Cortis 59 Fig. he is flung into the stigma and pollinia. Micheneau. Schiestl & Ayasse. In Pterostylis species. yet share a single pollinator. However. Fournel & Pailler. (E) Pterostylis (syn. or the location of pollinia attachment on the pollinating insect (Schiestl & Peakall. When a pollinator grips the labellum. The typical pollinator of a sexually deceptive orchid is male. 1974. (A) Cryptostylis subulata. 2002). erecta image by Julia Cooke. hunteriana labelled to show the large labellum and reduced petals and sepals typical of this genus. Bower & Brown. post-pollination or post-zygotic isolation factors are weak or uncommon (Scopece et al. Winnick & Herberstein. hybridisation is prevented by differences in pollinator flight and flowering times. erecta. 2009). Sympatric species of sexually deceptive orchids rarely share a pollinator and correspondingly. Cozzolino & Scopece. (B) C. but similarly scented and share their pollinator. Cozzolino & Scopece. species may also pollinate more than one sexually deceptive orchid species in different regions (see Table 1 for repeated pollinator species). Cryptostylis species differ in chromosome numbers.g. Sexually deceptive tongue orchids. Jones. 2005. and (D) Caladenia cairnsiana. Cryptostylis species. C. and only insects are involved in sexually deceptive pollination (Table 1). Paulus. 2007. 2004. (C) Caleana major. males of the parasitoid wasp Lissopimpla excelsa (Ichneumonidae). Backhouse & Jeanes.. 2006). Diplodium) grandiflorum.

1978. 1934. Paulus. Mant et al. These features could include: male attraction to airborne sex signals (allowing signal mimicry and long-distance attraction by orchids). 2005. Hardy. although all their offspring must be sons. 2008). 2008). Diptera) in the pollination of sexually deceptive orchids (see Tables 1 and 2 for pollinator types). and the males are polygynous (Larsson. 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. 2001. but haplodiploidy may also provide some advantageous features that facilitate the maintenance of sexual deception. (3) Exceptions to the general types of pollinators Not all pollinators of sexually deceptive orchids are solitary.A. Gaskett 60 deceptive pollination systems require further substantiation. 1987. 1982. the females are monandrous. 1989. Paxton. haplodiploid hymenoptera. 1935. 1994. 2005). attract mates with sex pheromones and do not exhibit any courtship behaviour. Biological Reviews 86 (2011) 33–75 © 2010 The Author. For example male social bees pollinate South American Trigonidium obtusum and Mormolyca ringens. 2008).. This may reflect current knowledge (for example. Table 1). 1981). 1994. Therefore.3. 2005). however no social interactions are observed between these males (Peakall. a species primarily pollinated by anthophorid bees (Table 1. 2009). Orthoptera) or scarce (Coleoptera. Damiens & Boivin. haplodiploidy could moderate orchid interference in pollinator reproduction. 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. In this manner. there is considerable competition between male Colletes cunicularius to detect virgin female pheromones quickly and to mate first with many females (Cane & T¨engo. Many Australian and New Zealand members of Pterostylis and synonymous genera are also potentially pollinated by diploid diptera. 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. Christensen. Ophrys fuciflora. and Ophrys urteae. fertilised eggs become female offspring and unfertilised eggs become male offspring (King. 2002. 2005b). Lepidoptera. Poiri´e & P´eriquet. Heimpel & de Boer. Selection on a male must therefore always operate indirectly via his daughters and then on her sons. Consequently. For example. 2005. Diploid flies (Diptera) pollinate Central American genera. in the future more dipteran pollinators of sexually deceptive Lepanthes species are likely to be discovered). Male thynnine wasps (family Tiphiidae. A hoverfly (Syrphidae.. 2006). subfamily Thynninae). Hardy. 1991). Eriksson & Borg-Karlson. In haplodiploid insect species. Correspondingly. Many diploid insect orders that are diverse.. 1994. Therefore. 2006. Such specialised pollination by wasps is rare in almost all other groups of flowering plants. except figs (Johnson. 1995. 1990. and families of pollinators listed in Table 1). 1989). 2006. El Agoze. Teng¨o. However. abundant. 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. intense male searching and vigilance for sex signals (encouraging rapid response to orchids). principally flies and fungus gnats (Christensen. 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 male’s sperm always become daughters. Haplodiploid insects are surprisingly common pollinators of sexually deceptive orchids (Gaskett et al. Male social ants pollinate Australian Leporella fimbriata. the extent of sexual deception in Pterostylis is unclear (see Section IV. 2004). Table 1) are drawn from a single observation and it is unclear whether pollination involved any sexual behaviour. have many similar mate-searching and mating behaviours (Burrell. and European Orchis galilea (Bino et al. Tyteca. permitting both pollinia collection and delivery). Eickwort & Ginsberg. For example. van der Cingel. vigorous mating behaviour (ensuring pollinia transfer between the orchid and pollinator). Diptera) is an occasional pollinator of European Ophrys holoserica. and sphecid and pompilid wasps pollinate both South African Disa species (Table 1). female haplodiploid insects deprived of matings (because male insects are mating with orchids) can still reproduce. C. and polygyny (ensuring a pollinator visits more than one orchid. 1980. However. Godfray & Cook. and even generate extra males to act as pollinators (Gaskett et al. Colletes cunicularius is relatively common. 1997). Paulus. Male bees and wasps are also generally highly vigilant and respond quickly to female pheromones. Biological Reviews © 2010 Cambridge Philosophical Society . and Apidae (but see Section III. Sexual deception of diploid beetle pollinators (Coleoptera) is documented for Ophrys blithopertha. Paulus. Singer. European Ophrys species are predominantly pollinated by solitary bees in the families Andrenidae. (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. 1993. male hymenoptera from solitary species are typically strongly attracted to the airborne sex pheromones of female conspecifics (Ridley. effectively doubling the intergenerational delay in any response to orchid exploitation. and common pollinators for rewarding orchids and other plants are either conspicuously absent (Hemiptera. Alcock. ichneumonid and scoliid wasps pollinate species from most Australian sexually deceptive orchid genera.. early reports of pollination of Pterostylis orchids by female mosquitoes (Coleman. which are common pollinators of Australian sexually deceptive orchids. Solitary and parasitoid wasps are the most common pollinators of sexually deceptive orchids (Table 1).3).. 1994. and the incidence of fly pollination is almost certain to increase as further studies are undertaken on orchids from this region (Calvo. Singer et al. Megachilidae. Thynnine. 2006). Blanco & Barboza. and is occasionally observed for Ophrys holoserica (Delforge. Colletidae. Rois & Vereecken.. 1988.

(2003) Source Table 2. without model sp: 28% (N = 852) 24. 21. ulicifolia. N = sum of sample sizes reported in source Orchid pollination by sexual deception 61 Biological Reviews 86 (2011) 33–75 © 2010 The Author.6% of flowers set fruit (N = 692).) Goldbl.Linder Disa pulchra Sond. (Scrophulariaceae) Watsonia lepida N.5% of flowers set fruit (N = 890) Orchid mean Pollination success Nilsson (1983) Dafni & Ivri (1981). Food-deceptive or unrewarding orchid species tested for similarity in colour with co-occurring plant species that do provide nectar rewards for their pollinators. campanularum (Kirby) (Megachilidae) Solitary bees Anthophora sp. Diurideae Diuris aequalis Fitzg.) Hook (Asphodelaceae) Scabiosa columbaria L. Pollination success for each orchid species is the average of values reported in the source.: 69. without model sp. F.5% fruits per flower (N = 200) with model sp.9% pollinia removed.3% fruit set per plant (N = 28) 92.P.Watsonia densiflora s. C. (Campanulaceae) Diuris maculata Smith Orchideae Orchis israelitica H. Tritoniopsis triticea (Burm. Nemestrinidae) Pollinator 8.7% fruit set per plant (N = 17) flowers: 13. Biological Reviews © 2010 Cambridge Philosophical Society . 48. Disa nivea H. (Nymphalidae) Long-proboscid flies (Tabanidae. Schum.5% of flowers set fruit (N = 600).9% of flowers pollinated (N = 95).f. (Dipsacaceae) Rewarding model Disa ferruginea (Thunb.) Sw.E. Diseae Disa cephalotes Rchb. (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. (2006) Indsto et al. Baumann & Dafni Neottieae Cephalanthera rubra (L. 3. (Liliaceae) Campanula spp. (2005) Indsto et al. 59% of plants set fruit (N = 29) 15.2% pollinia deposited (N = 37) with model sp. cephalotes Orchid species Solitary bees Chelostoma fuliginosum Panzer. (Iridaceae) or Kniphofia uvaria (L. Brown (Iridaceae) Disa nervosa Lindl. Gompholobium huegelii Bentham (Fabaceae) Daviesia ulicifolia Andrews ssp. (2006) Johnson (2000) Anderson. plus other related legumes (Fabaceae) Bellevalia flexuosa Boiss.l.. Bombylius sp. Baker (Iridaceae) Zaluzianskya microsiphon (Kuntze) K. 41.) Rich. Galizia et al. Eucera clypeata Erichson (Anthophoridae). ssp.75% (N = 428) 17% of flowers set fruit (N = 122). Johnson & Carbutt (2005) Johnson & Morita (2006) Johnson (1994) Johnson et al.

although the lack of female visitors is inconsistent with observations of other orchid species thought to mimic rendezvous sites (Nilsson. but future studies are likely to generate further examples. 2001e. and document any sexual behaviour. 1993. 2005). Ciotek et al. which is common amongst primitive.. 1983). Drakaea and Paracaleana genera. and Australian Calochilus campestris. 1983. Kullenberg (1961) reported sexual behaviour by a sphecid wasp on flowers of Guiera senegalensis Lam. has features associated with sexual deception.. Dixon & Hopper. POLLINATOR BEHAVIOURS (1) Pollinator behaviour and the origins of sexual deception Although pollination by sexual deception is confirmed only for orchids. 1996. 1997. but an early report suggests it is pollinated only by male bees of Halictus lanuginosus. and was recently confirmed using microscopy and sperm-staining dye (Gaskett et al. b.. the labellum bends on a flexible hinge and presses the duped insect into contact with the orchid stigma and pollinia (Bower. b) whilst observing pollinator behaviour on Cryptostylis leptochila. Pollination of Australian Cryptostylis species even involves pollinator ejaculation. Jers´akov´a et al. When a male insect grips or lifts the orchid labellum as if it was a female insect. Stoutamire. Lists of pollinators for food-deceptive and rewarding Caladenia species are available elsewhere (e. Surveying pollinator behaviour within a genus could indicate how the transition between food and sexual deception may occur. Paulus & Gack. This copulatory behaviour occurs for European Ophrys and Orchis species. Ejaculation during orchid pollination is also likely in Lepanthes glicenstenii because scanning electron microscopy of flowers after pollinator visits revealed putative spermatophores (Blanco & Barboza. 1996. Similar phylogenetic analyses tracing the evolution of sexual deception could be applied to the Australian genus Caladenia. Diuris pedunculata provides nectar. Bates. Peakall & Beattie.A. Diuris pedunculata and D. and Cryptostylis species (Coleman. 2009a). Jones et al. and sexual deception is a compelling explanation for the nectarless and insectiform flowers of Gilliesia graminea Lindl. In these putative cases.. it seems likely that the orchids act as. the less speciose Arthrochilus. Leporella fimbriata.. 1983. 2005. Fordham. 1994. 2009). However.. 2006. especially amongst lesser-known Lepanthes and Cryptostylis species. 2001a.. Peakall. it lacks nectar and is pollinated by male bees of Tricholetes venustus (Indsto et al. Gaskett 62 IV. it provides nectar and has several pollinator species. In some species. 1928a. 2001. In orchids. For most Australian sexually deceptive orchid species. 2009. Harrewijn. Peakall & Beattie. 2009. 1929. Pollinators of some orchid species do indeed attempt to mate with the orchid. 1986. Caleana.. Phillips et al. Gang. Dixon & Tremblay. and whether elements of both systems can coexist. 2004. 2002). nectarless orchid groups.g. 2004. and possibly Japanese Cymbidium pumilum (Sasaki et al. 1946. and the single species from the genus Spiculaea (Fig. C. Phillips et al. Steiner. c. both a foraging site and a rendezvous site for courting males. e. 1961. These cases are yet to be confirmed. (Combretaceae). 2006). Peakall. typically by grasping the large central petal or labellum (Fig. 2006. This is common for orchids from the diverse genera Caladenia and Chiloglottis. 2009a. Hopper & Brown. different species of Australian Donkey orchids (genus Diuris) reward or deceive foraging insects. 1D for orchid flower parts). Central American Lepanthes glicensteinii. 2007). 2006a). 1930. Alcock. 2006). Table 1). detailed observations are required to confirm pollinator species and sex. 1989. Consequently. Brown & Schiestl. (Alliaceae. successful pollination requires only pre-copulatory rather than copulatory behaviour from the pollinator.. whereas Diuris aurea is food-deceptive and has several pollinators (Indsto et al.. and potentially. 1984. South American Mormolyca ringens and Geoblasta pennicillata. 1932). which has a diversity of rewarding and food. phylogenetic comparisons suggest that sexual deception evolved from food deception. 1998). 2006). This was first suspected by Coleman (1927. 1983. 2005). Another species. For example. Phylogenetic analysis of Disa suggests multiple shifts between pollinator types and gains and losses of nectar rewards (Johnson et al. 2008). pollination involving some form of insect sexual behaviour may actually precede the evolution of orchids. f . 1982. Salzmann. (2) Pollinator sexual behaviour with orchids Sexually deceptive orchids elicit a range of sexual behaviours from their pollinators. or mimic. However. Bino et al. perhaps suggesting some sexbased pollination (Coleman. 2. the sexual behaviour of the pollinator on the Biological Reviews 86 (2011) 33–75 © 2010 The Author. Hopper & Brown. b).. Despite the prevalence of sexual deception amongst orchids. 1998. 2007). 2000. insects were likely to aggregate and mate on the flowers and coincidentally function as pollinators.. Blanco & Barboza. 1991). Brown et al. 1965. 1.. 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. plant and floral scents still enhance insect sex pheromone release and attractiveness (for a review. Table 1 provides the known or putative pollinators for many sexually deceptive orchid species. Diuris alba appears to be a rewarding species. Bower & Branwhite. In the case of these last two species. Cady.and sexually deceptive pollination systems and considerable new data now available for analysis (Stoutamire. exploit aspects of pollinator sexual behaviour. see Reddy & Guerrero. 1928a. although some of these orchids do provide pollen as a reward (Cozzolino & Widmer. detailed observations reveal no sexual behaviour with orchid flowers (Indsto et al. maculata. Bower. 2005). 2004). Minks & Mollema. Diuris maculata. 1990. 1982) and Australian Caladenia patersonii (Stoutamire. Rudall et al.. Singer et al. There is currently little evidence of pollinator ejaculation for any other orchid species. Biological Reviews © 2010 Cambridge Philosophical Society .. Kullenberg.. For many modern insect species. Other orchids proposed to employ aspects of both pollinator foraging and sexual behaviour include European Orchis galilaea (Bino et al. there is scarce empirical evidence that any orchid species employs both sexual and food deception (Faast et al. 1990.. see Fig.

2001. 1994. It is important to note that the occurrence of sexual deception in Pterostylis spp. Simpliglottis) valida Cryptostylis erecta Gripping hinged labellum Copulation/ejaculation 13. When orchids are experimentally moved within their pollinator’s range to areas where they do not normally grow. Christensen. 2E. Percentages of insects fooled into pollinating some Australian sexually deceptive orchids after initial attraction.5 28. (2008). However. prior learning is not necessary to provoke this variability. Although almost all reported pollinators for Pterostylis spp. For example. pollinator responses still vary even though all the insects attracted must have no previous experience with sexually deceptive orchids (Bower. confirming pollinator identity or sexual behaviour is challenging because pollination is rarely observed (see Table 1 for pollination rates). Arachnorchis) tentaculata Chiloglottis diphylla Chiloglottis (syn.9 60. *Data combined & averaged from more than one study % fooled N Orchid Pollinator behaviour Caladenia (syn.3 3. Simpliglottis) pluricallata Chiloglottis reflexa Chiloglottis seminuda Chiloglottis trilabra Gripping hinged labellum Gripping hinged labellum Gripping hinged labellum Gripping hinged labellum Gripping hinged labellum Gripping hinged labellum Gripping hinged labellum Gripping hinged labellum 7.0 618 55 50 Source Peakall & Beattie (1996) Bower (1996) Bower (1996) Bower (1996) Bower (1996) Bower (1996) Bower (1996) Peakall & Handel (1993). A. although entrapment does not appear to require copulatory behaviour from the pollinator. Bernhardt. 1934.0 90. 1878. Gaskett (unpublished data) Gaskett et al. 2003. unlike the traps described above for Caleana and Trigonidium orchid species. and pollinator behaviour for most species in the group is completely unstudied (Cheeseman. 1909. (2008). 2009). Jones & Clements. A. Cheeseman. 2002). 1872. N = visits observed. or longer in cool conditions (Sargent. are male (Table 1). Sargent. Bernhardt. Responses are also likely to be affected by spatial variation in temperature and air currents. 2C) become briefly pinned upside-down between an orchid’s hinged labellum and the column.. 1995). or differing previous experience with orchids (Ayasse et al.73∗ 55∗ Drakaea glyptodon Leporella fimbriata Spiculaea ciliata Gripping hinged labellum Copulation Copulation 21. Myrmechila) formicifera Chiloglottis (syn. 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. Robertson & Hedderley. Caleana major (Fig. is largely based on unpublished or anecdotal evidence (often of considerable antiquity).23∗ 287 24 38 53 26 48 79 2897∗ Chiloglottis (syn. 2000). C. Experiments suggest that labellae can be triggered up to three times. 2001c). Hopper. and can escape only via a narrow passage that forces contact with the pollinia and stigma (Fig. influencing the local dispersal of orchid scent.0 39. and regain their position and sensitivity within 3h. When the potential pollinator touches the sensitive labellum he is catapulted into a curved hood formed by the dorsal sepal.85 24. 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. Myrmechila) platyptera Chiloglottis (syn.7 10. e. 1990). This variation among individuals could be due to genetic differences in learning ability (Dukas.g. 2002). but much remains to be discovered about these enigmatic dipteran-orchid pollination relationships before sexual deception can be substantiated. 1996). 1885. There is some suggestion that the fungus gnat pollinating Pterostylis gibbosa does attempt to mate with the orchid labellum (National Parks and Wildlife Service. Some individuals approach the orchid but then fly away without landing or attempting sexual behaviour (Table 3). 2003. not all individuals that encounter an orchid are fooled into actual pollination. which bears the stigma and pollinia (Bower.Orchid pollination by sexual deception 63 orchid may trigger a floral trap. The pollinator soon escapes via a hinged floral lip after brushing past the stigma and pollinia. 2005). 2006. Darwin. Sargent. C. 1995). 1909. Many species in this group have a floral trap.5 41.0 44. (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. 1872. 1909. Gaskett (unpublished data) Peakall (1990) Peakall (1989) Alcock (2000) Biological Reviews 86 (2011) 33–75 © 2010 The Author. Coleman.0 23. Within a pollinator species. Lehnebach. Thomson. Bower (1996) Bower (1996) Gaskett et al. Jones. There is probably individual variation in insect sensory sensitivity or perception of orchid signals. pollinators attempting copulation with Australian Duck orchids. 2008). Biological Reviews © 2010 Cambridge Philosophical Society . Jones & Clements.99∗ 46 111∗ Cryptostylis subulata Copulation/ejaculation 92. and in the quality or attractiveness of each orchid (Peakall. Jones.

. or set fruit. 1993. C. actual pollination or seed set rates are not necessarily reported (e. 2005). Phillips et al.A. Caladeniinae includes the large genus Caladenia. Drakaea. 37..1% (Tremblay et al. even if abundant pollinators are available. of which the sexually deceptive species are almost exclusively thynninepollinated. Heinrich & Jetschke. IV.. When data for food and sexually deceptive orchids are combined. 2000). Thus.9% of plants (N = 11 species).g... 3). 2005. 1987). Bower & Brown. V. 2006. the variation in individual pollinator responses. suggesting a strong fitness benefit for orchids with persuasive mimicry and deceptive signalling. 2006). 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. Mant.9% (Neiland & Wilcock.84. orchids causing more extreme behaviour have higher pollination success (Gaskett et al. 2009. 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. Zotz & Schmidt. Brown & Weston.5 ± 14. which is likely to worsen due to climate change (Memmott et al. with many more thynnines yet to be formally identified (Table 1). respectively. and most long-term Fig.. = 11. 2005. Phillips et al. The poor pollination success of sexually deceptive orchids is generally attributed to a lack of pollinators or pollinator visits. or alternatively. POLLINATOR ABUNDANCE AND DIVERSITY Insect abundance and diversity could be important factors influencing the reproduction and fitness of sexually deceptive orchids. 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.f. 1989. 1998. This availability of diverse thynnines may have contributed to the extraordinary diversification of the major (and largely sexually deceptive) subclades of Caladeniinae and Drakaeinae. 2009).5 ± 20. they may not necessarily be coerced into orchid visits. For example. the literature surveyed for Table 1 shows that for sexually deceptive orchids. so the potential for speciation in sexually deceptive orchids may be constrained by the diversity of insects available to act as pollinators. Table 1 shows that at least 70 Australian thynnine species from 12 genera pollinate at least 150 sexually deceptive orchid species from seven genera... and Paracaleana (Kores et al. 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.4 and VII). In Australia.2. Tremblay et al. P < 0. 2009a). 2005). 2006.7% versus 37. 2007). Pfeifer.001.. 2001). Specialist orchids may be vulnerable to mismatches in pollinator emergence and flowering seasons. 2005c. Biological Reviews 86 (2011) 33–75 © 2010 The Author. 2002.D. If orchids are classified according to the sexual behaviour stimulated from their pollinators. 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. Chiloglottis. Vandewoestijne et al.g. 1998) or 20. Australian thynnine wasps are diverse. 3. 1998. d. sexually deceptive orchids have lower fruit-set per flower than food-deceptive orchids (14% versus 36%. and many of the 715 named species are endemic (Naumann. 2009a). Orchids stimulating the most extreme sexual behaviour are the most likely to fool pollinators into making contact with the orchid (Fig. rather than any limitation in resources such as water or nutrients (Peakall. 2008).7% of all flowers (mean ± S. had pollinia collected and deposited. Globally. and Drakaeinae comprises a diverse radiation of closely related thynnine-pollinated genera including Caleana. Zotz & Schmidt.. Biological Reviews © 2010 Cambridge Philosophical Society . or the possibility of fooled pollinators avoiding orchids or orchid locations after previous visits (see Sections IV. Gaskett 64 depending on the extent of pollinator sexual behaviour elicited by each orchid (Table 3). Pollinator limitation may be a consequence of extreme specialisation to a single or very few pollinator species. Schiestl. Calvo. N = 35 species). but did not fly close enough to be counted by an observer. controlling for the number of pollinator visits observed). an average of 20. 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. Although there are some long-term demographic studies of sexually deceptive orchids.. Neiland & Wilcock. Hutchings. studies focus on food-deceptive or rewarding orchid species (e. and the potential for speciation in an existing pollinator species. Sexual deception typically involves a species-specific pollinator (Table 1). Tremblay et al. 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.

and/or labellum. Peakall. 1999). Borg-Karlson. synthesis. 2005). 2009. Gaskett et al. Schiestl & Peakall. Peakall. compounds could be considered electrophysiologically active when they provoke antennal responses in at least half of the runs performed (Schiestl & Ayasse. subfamily Pimplinae. or more commonly. all five Australian and New Zealand species of Cryptostylis (subclade Cryptostylidinae) share a single pollinator.. 1996. Schiestl. male Lissopimpla excelsa (family Ichneumonidae. 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. 2005. 2005b. Few studies reveal the total number of trials performed. Naumann. GC-EAD allows scent compounds to be individually tested for their capacity to stimulate a pollinator’s antennal chemoreceptors. 1928b. b. they are not involved in any sexually deceptive pollination in Australia (Colletidae. Leal. Peakall & Beattie. 2009). 2009). behavioural studies confirmed that pollinators could be attracted with extracts of sexually deceptive orchids or synthetic mixtures of common compounds (Kullenberg. 1997. Schiestl & Peakall.g.. Schiestl et al. indeterminate origins.. although Australia has several solitary bee species from the families that are major pollinators for Ophrys species in Europe. 1961).. 2005b) and when using both antennae from one insect. Peakall & Barrow. 2000). 2005. 2005).. 2005. 2008). 1990. VI. For example. 1956. visual signals such as colour or shape must indicate the specific source of the scent. Application of GC-EAD could be enhanced by more detailed reporting. Ideally. 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. Schiestl & Ayasse. 4). including those in which antennae failed to make any response at all. 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. Fig.. Biological Reviews © 2010 Cambridge Philosophical Society . 2007. Jers´akov´a et al. (1) Scent Early researchers swiftly recognised the importance of orchid scent for attracting pollinators and stimulating pollinator sexual behaviour (Coleman. Megachilidae and Anthophoridae. studies should report the number of trials performed. and the number and magnitude of antennal responses obtained for each electrophysiologically active compound. 2009). 1989. Since most statistical tests assume independence of data. 2006). 1984. G¨ogler et al. 2008. so behavioural assays must be performed (Schiestl & Marion-Poll. 1929. St¨okl et al. 2006. and. d. Whole live antennae of the pollinator species have been tested with synthetic versions ˚ of compounds identified in orchids (Agren & Borg-Karlson. Graham. Vereecken & Schiestl. This would be particularly important for species that occur in dense aggregations that generate a large scent plume with multiple. 1987. Paulus & Spaethe. any novel. the sensitivity and responsiveness of insect antennae (or conversely. Behavioural tests offering pollinators dissected orchid flowers can be useful for determining where scent is released in the flower (typically from the sepals.. Salzmann et al. but once a pollinator is nearby. 2004. 1956. 2008. Interestingly. 2005. Halictidae. 1996). 1999. Beattie & James.. St¨okl et al. It is often assumed or speculated that shape and colour play a role in sexual deception by orchids (e. 1978. 4). GC-MS. 1999. 1978. However. it is also important to declare and control for antennae used in more than one trial (e.. mutated. Franke et al.. 2008). Schiestl et al. 1938. Mant et al. Therefore. 2002. 1989. In the field. Schl¨uter & Schiestl. 2002. G¨ogler et al. 2003. Stoutamire.. Poldy.. Scent is undoubtedly vital for long-range pollinator attraction. The model example of this procedure is the elegant and methodical identification. and field testing of the single novel compound attracting pollinators to Chiloglottis trapeziformis. 2006a. 2003. 1987.. petals. 2006. 2000. 2006).. 1990. The most powerful studies combine behavioural observations and assays with chemical analyses and tests for pollinator perception of scents (Fig. Schiestl. 1979. Mant et al... Coleman. 1996. It is also rare to report the magnitude or number of antennal responses required before a compound can be considered ‘electrophysiologically active’. Peakall.. crucially. 2000). Paulus.Orchid pollination by sexual deception By contrast. Peakall & Beattie. Dodson et al. Table 1. Not every electrophysiologically active compound necessarily elicits a behavioural response from the pollinator. 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. and the use of this compound and analogs in further investigations of other Chiloglottis species (Schiestl et al. or much more commonly. Paulus.. experimental tests for shape and colour mimicry and manipulations of these signals require considerably more attention before this can be confirmed. 1983. Ayasse et al. there is only meagre information about other signals or cues involved in pollinator deception. gas chromatography-electroantennography or gas chromatography-electroantennal detection (GC-EAG or GC-EAD. 2007. Bergstr¨om. the strength of the orchid signal) may vary consistently with some biologically relevant factor such as the extent of pollinator sexual Biological Reviews 86 (2011) 33–75 © 2010 The Author. Ascens˜ao et al. Initially. Interestingly. 2005). the proportion in which antennae failed to respond.g. Kullenberg. Flach et al. ORCHID SIGNALS AND POLLINATOR PERCEPTION Although understanding of orchid scent and pheromone mimicry is advancing rapidly. 1961). Bergstr¨om. 2002. Australia has only four Lissopimpla species and a relatively small ichneumonid fauna (Naumann. Peakall & Mant. with extracts of orchid labellae and/or females of the pollinator species (Schiestl et al. 1969. Ayasse et al. 1983. coerce him into making contact (Peakall & Beattie. pollinators approach orchid flowers with a characteristic zig-zag flight path associated with chemoreception (Wallace.. 1978. Streinzer.. 1928a.

GC-MS. GC. Consequently. If food-deceptive orchids (the putative mimic) are compared with co-occurring rewarding flower species (the models). have an entirely different ecology and physiology to their models. 11 Agren 12 13 14 15 16 et al. Gaskett 66 Fig. gas chromatography-electroantennodetection or gas chromatography-electroantennography. 18 Mondrag´ on-Palomino & Theiβen (2009). 9 Shipunov & Bateman (2005). the mimics. 2005). Sexually deceptive orchids. Biological Reviews © 2010 Cambridge Philosophical Society . Vorobyev & Brandt. studies of food-deceptive pollination systems compare the spectral reflectance of food-deceptive orchids and co-occurring rewarding species (Table 2). Nonetheless. 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. similarities between the orchid and the female insect can be more confidently attributed to mimicry rather than to convergence in sexually deceptive systems. (2005). it is likely their shared environmental conditions and pollinators would exert similar selective pressure on many features including colour. 2003). (2005). 2006). (1999). GC-EAD. Vereecken et al. Francke et al.. (2004). pollination systems. Indsto et al.. but is hindered by the lack of specific information about the visual systems of most orchid pollinator species and disagreement about modelling methods (Chittka. 2005). 4 Schiestl et al. SEM. Grim. 2 Peakall (1990). gas chromatographymass spectrometry. Ayasse et al. Early studies by Kullenberg (1961) attempted to quantify the colour of Ophrys species with spectral measurements and comparisons with standard colour hues. (2009). four Australian Cryptostylis orchid species are all perceptually identical in colour to their pollinator’s female conspecific when modelled into a hymenopteran visual system (Gaskett & Herberstein. 2010). Galizia et al. (2000). 1997. 1). 7 Schiestl (2004). gas chromatography. any studies modelling orchids from the visual perspective of the pollinator would be a significant contribution (Fig. (2007a). 8 Zelditch et al. C. 1 Bower & Brown (2009). 2005. Similar analyses for sexually deceptive species show that despite colour differences seen by humans (Fig. 17 Johnson et al. Kelber et al. This problem can be avoided by investigating mimicry in sexually deceptive. (2) Colour Analyses of orchid colour from a human perspective are largely redundant given the differences between human and insect visual systems (Kelber. Sexually deceptive orchids may also exploit pollinator sensory biases or perceptual weaknesses. Recently. 1984. A major difficulty when studying colour mimicry by orchids is the potential to conflate mimicry and convergent evolution (see Johnson. 6 ˚´ Gaskett & Herberstein (2010). Alexandersson & Linder. 4. behaviour. 10 Kullenberg (1961). or between major and minor pollinators for an orchid species.. 2003. female insects. Analysis from the pollinator’s visual perspective is crucial for understanding pollinator-driven selection on orchid colour. (2004). 2001. (2003). Galizia et al. rather than food-deceptive. Vorobyev & Osorio. 19 Fitzpatrick et al. (1998). Chittka & Kevan. 4).A. 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. Wong et al. 2003. 3 Alcock (1981). 5 Schiestl et al. scanning electron microscopy. Sensory biases evolve when sensitivity to certain signals or cues provides fitness Biological Reviews 86 (2011) 33–75 © 2010 The Author. 1992. suggesting interesting additional analyses that would maximise the value of EAD-based research.

However. Orchids that exploit insect sensory biases can take advantage of their pollinator’s innate attraction to certain signals such as wavelengths or shapes (see also Section VI. e. Drakaea. Johnson et al. red. 1994). 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. UV-reflection is relatively uncommon in rewarding flowers (Chittka et al. Kindlmann & Renner. soil and stones.). Vallius & Salonen. 2009) and similar pollinator behaviour is reported in other Paphiopedilum species (B¨anziger. Dickson & Petit. 2001).. 2005.. Green and UV receptors. (3) Shape The shape of an orchid is also likely to be an important visual signal for sexual deception. 2006. Fig.. and are therefore difficult for hymenoptera to detect or differentiate between (Chittka et al. Green flowers may be difficult to distinguish from surrounding green leaves. Singer et al.. For example. 1. More studies investigating and testing for exploitation of sensory biases and sensory traps in sexual deception would be fascinating. small cuts made on the reverse of the labellum. 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. Gaskett & Herberstein.g. Several orchids feature notably insectiform labellae that might mimic female insects. or seed viability. it is rare for sexually deceptive species. After a pollinator has landed on an orchid. Singer. Bright yellow spots on the labellum are known to attract pollinators in the food-deceptive slipper orchid Paphiopedilum barbigerum (Shi et al. Salzmann & Schiestl. 2007. Cryptostylis. 2005. 2007). Biological Reviews © 2010 Cambridge Philosophical Society .. Red wavelengths are beyond the peak sensitivities of the Blue. Blanco & Barboza. 1994). Jones. Thus future studies of colour polymorphism in either sexual or food deception should consider how colour morphs differ in several factors such as fitness. Yellow and ultraviolet (UV) wavelengths may be more likely candidates for exploitation of innate insect preferences. 2004. post-pollination barriers. but others. 2005. Lunau. Tremblay & Ackerman. 2007.g. he must be persuaded into attempting copulation. labellae and the specific female bees they mimic indicated considerable textural ˚ congruence (Agren. 2009. Although white flowers appear obvious to humans. Aragon & Ackerman. further images of Australian. Figs 1 and 2. 2001.Orchid pollination by sexual deception benefits. including Cryptostylis erecta. 2006. Tautz & Chittka. Jers´akov´a. 2006) and Ophrys arachnitiformis (Vereecken & Schiestl. e. Exploitation of insect attraction to UV is also plausible (Paulus.. 2005. quick detection of colours associated with food or mates. but see Gigord et al. 2007). and South and Central American species see Blanco & Barboza. However.g. Most studies with food-deceptive orchid species find no evidence of frequency-dependent selection or pollinator preferences for rare colour morphs (Koivisto et al. Wallace.. Gaskett & Herberstein. lutea bear long trichomes that point towards the stigma and these are likely to direct the pollinator’s genital claspers towards the stigma and adjacent pollinia (Ascens˜ao et al.. identical to the wings of their pollinator’s female conspecific (Gaskett & Herberstein. Smithson et al. Close-range tactile cues may also determine pollinator orientation on the orchid. many sexually deceptive orchids are predominantly green. Pellegrino. 2010). Intriguingly.. or white. Trigonidium obtusum and Pterostylis species do not appear insect-like to the human viewer (Figs 1 and 2. which is imperative for effective pollinia collection and transferral (Kullenberg. 2009). 1992). 2010. perhaps resembling background leaves or plants and thus obscuring parts of the flower that may hinder mimicry of female insect body shapes. Finally. exceptions include Caladenia behrii (Dickson & Petit. see Delforge (2005) for pictures of Ophyrs spp. 2005).. 1994) and distinguish from the background (Spaethe. e. Macnair & Smithson. 2002. Many insects are strongly attracted to yellow or UV (J¨onsson. 2001).. European. 1994). although within-species colour polymorphism occurs in several food-deceptive orchid species (Gigord. Johnson. Koivisto. Delforge. cause approximately equal excitation of the Blue. This is because white flowers. Red floral colouration may act as a cognitive sensory trap (Schaefer & Ruxton. Goulson et al. The role of colour polymorphism is unclear.g.. bumps on the labellae of Cryptostylis subulata and C. 2006). 2006b). 2010. In field experiments. suggesting a sensory bias for contrast rather than specific colours (Streinzer et al. 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. they can be difficult for hymenoptera to distinguish from the background (Chittka et al.. Lindkvist & Anderson.3). 2010).g. 1961. 2005. 1996). The surface cells on the labellae of Ophrys fusca and O. or a preference for larger body size in mate choice (Schaefer & Ruxton. 2005. 2006.. which are colours not easily seen by hymenoptera (Gaskett & Herberstein. Green and UV receptors typical of most hymenoptera (Chittka et al. ovata reflect UV. 2009). 2002. Kullenberg & Sensenbaugh. 2009). Vereecken & Schiestl. Bellusci & Musacchio. Paracaleana and Lepanthes species and Geoblasta pennicillata. 2000. 1978). 2003). 2002.. Pellegrino et al. Peitsch et al. and is correspondingly rare in food-deceptive orchids (e.. 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. Ciotek et al. rather than just pollinator preferences (e.g. Comparison of the distribution and dimensions of hairs on the surface of Ophrys spp. This could be accomplished by close-range mimicry of the dimensions and tactile qualities of the body of his female conspecific. The hypothesis that trichomes function in pollinator orientation could be tested by experimentally removing trichomes or manipulating their arrangement and observing pollinator orientation behaviour. 1984). like background foliage. 2007. 2007) and orchids often have bright yellow pollinia visible to the pollinator or yellow sepals or petals (e.g. Moser & Paulus. 2006). Biological Reviews 86 (2011) 33–75 © 2010 The Author. 2009).

. orchids that produce multiple deceptive sex signals in chemical. 2001. These large flowers could represent an irresistible super-stimulus that exploits the common male insect preference for large female body size (Bonduriansky. R¨utzler & Zwiebel. Firstly. indicating a limit to male preference for large female body size (Schiestl. For orchids. 1976a. 2001a). Schiestl. the pollinator of Chiloglottis trapeziformis preferred intermediate over both small and large models. Candolin. Candolin. 2005a. Bargmann. 2007). Peakall & Weston. 2003). 1999. Raguso. then a second pair of curved flanges traps his wings and prevents his escape until after pollinia transferral has occurred (Bower. learning and memory are common in all aspects of life including sexual behaviour (Dukas. Ayasse et al. each signal mode could convey different information about the emitter (Candolin. visual and tactile modes could be extremely compelling for their mate-searching potential pollinators. rather than just the insectiform black. the functions and pathways of olfactory receptor neurons. Dahanukar & Carlson. Experiments testing pollinator behaviour and learning using manipulated floral shapes are required. The pollinator perspective could be incorporated by applying molecular data on the expression of insect sexual behaviour. 2006... e.. while shape and texture cause precise orientation on the orchid. St¨okl et al. Mant et al. However. VII. Mondrag´on-Palomino & Theißen. sexual deception was thought to activate only innate behaviour with no scope for learning (Kullenberg & Bergstr¨om. C. the backup hypothesis. 2006).. or assist in species and mate recognition (Partan & Marler. 2007). visual and tactile stimuli in sexual deception. and signal processing in the brain (e. 2005.. scent might attract over long distance. or the whole labellae of Ophrys species.A. Furthermore.g. 3. 2005. when a pollinator grips the loosely hinged labellum of Arthrochilus species. Ophrys fusca (Ascens˜ao et al. each mode could elicit a different part of the receiver’s response (Kullenberg.g. there should be strong selection for multimodal signalling. 2005b. 2004). 2004). the genes coding for visual pigments such as opsin) which could be applied to the study of deceptive orchid colouration (Briscoe & Chittka. 2004). and that there is no signal reinforcement between the scent and the natural green or white floral ornaments (Vereecken & Schiestl. Spaethe & Briscoe. A third explanation. suggests that each component reiterates or reinforces the same message (Partan & Marler. 2003). changes in individual behaviour (Wong & Schiestl. Vereecken & Schiestl. Mant. 2005. Mate choice often involves assessment of multicomponent or multimodal signals (Candolin. 2005. 2005). and Ophrys sphegodes (Schiestl et al. scent and colour might advertise the orchid’s location. 2008.g. 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. Ophrys exaltata (Mant et al. 2002.. Dafni.. 2005e). 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 (Schl¨uter & Schiestl. e. glossy calli on the labellum of the orchid. Therefore. Morphology is likely to control both the location and duration of pollinator contact. Kelber et al. 1999.. 1999. Secondly. Papke et al. Biological Reviews © 2010 Cambridge Philosophical Society . Schiestl. 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. Papke. he is swiftly swung into a pair of flanges that control his position against the stigma and pollinia. Since the attractiveness of an orchid appears to provide fitness benefits in terms of increased pollination success (Fig. 1987). Gaskett et al. 2004). Sexually deceptive orchids exploit their pollinators’ mate search and mate-choice signals. However. 2009).g. 2007). For example. Kemp & Rutowski. Alternatively. Gaskett 68 Shape may also exploit pollinator sensory biases involved in male mate-choice behaviour. 2003. (4) Multimodal signalling In his thesis. 2000. Vereecken & Schiestl. Hallem. Paulus... 2003.. 1996. 2009). 2001. 2003. The literature suggests two alternative and as yet unstudied hypotheses for the function of varying floral shape in sexual deception. the insectiform labellae of Drakaea or Caleana species. 2008). 2008). Multicomponent signals can enhance detection in signalnoisy environments. Fitzpatrick et al. measurements were taken of the whole labellum. 2004). odorant receptor genes. 2009). For orchids. would help clarify the role (if any) of shape mimicry in sexual deception. Jers´akov´a et al. A comprehensive multi-species study of the possible tactile function of these calli in Chiloglottis species. Other candidates for multi-signal manipulation are colourful and morphologically ornate species for which the attractive scents are well studied. floral shape is undoubtedly important in the function of floral traps. In the past. 1961). POLLINATOR LEARNING In insects. which may be more relevant for comparison (for drawings. scent alone is sufficient for pollinator attraction. However. Ophrys iricolor (St¨okl et al. behavioural tests with Ophrys arachnitiformis show that for this species. 2000). with strong consequences for pollinia transfer and thus fitness. 2007). in tests with model female insects. whilst the size of the orchid might suggest a female of high fecundity and mate quality. and stimulate copulation. It is now widely accepted that deception stimulates pollinator learning and memory. Kullenberg (1961) addressed the possibility of multiple olfactory. 4. After visiting a sexually deceptive orchid. a pollinator appears to become aversive to the location of the Biological Reviews 86 (2011) 33–75 © 2010 The Author. 2006a. 2008).. see Bower. 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.. and consequently. Spaethe et al. Morphological comparisons of flower size show that the labellae of Chiloglottis trapeziformis orchids are consistently larger than the female insects they mimic (Schiestl. 2006. There is also considerable existing data on the molecular basis of insect colour perception (e.

In this situation. or may transfer only seminal fluid without sperm. Bower. Capacity for learning and memory are heritable (Dukas. Ayasse et al. or a regular behavioural response to any negative experience. Although currently considered extremely rare and proposed only for Cryptostylis and Lepanthes species (Blanco & Barboza. 2004). At present. Ayasse et al. There are few experimental tests of learning in sexually deceived pollinators so this is likely to be a very productive field for future research. antagonistic coevolution or an arms race (Wong & Schiestl. and sensory perception could exert considerable selection on sexually deceptive orchids and their signals. Wong & Schiestl. Peakall & Schiestl. 1977. this in turn could select for increasingly sophisticated and persuasive orchid signals. 1990. limiting lifetime sperm production (Wedell. Gaskett et al. 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. 1987. Bower & Brown. Gage & Parker. 1983. If sexual deception involves pollinator ejaculation and sperm wastage. nectariferous flowers (Chittka. However. 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. pollinators arrive swiftly.. 2004. 1997. 1974). 2000). 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. However. 1990. 2004. but see Jones & Gray. (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. Peakall.. as occurs in many solitary wasp species (King. 2002. 2009). 2008). 2002). 1996. Thomson & Waser. prematurely end a copulation with a real female to visit an orchid.. Pollinators can prefer orchids to real females.. 2008). he may not be able to copulate.. Almost all studies of sexual deception employ wild-caught male insects. and do not grow in all areas in which their pollinating species is found (Kindlemann & Balounov´a. If sexual deception does negatively impact the mating opportunities of individual pollinators. 2002. 2005. Alcock. If the costs of deception are strong enough to select for pollinator avoidance of orchids. Unlike the pollinators of rewarding. Sperm production can be costly in many insect species. and is this sufficient to drive selection at a population or species level? Are na¨ıve insects outside orchid ranges more likely to be fooled by an orchid than na¨ıve insects in populations in long-term contact with orchids? Experimental assays involving pollinator learning require na¨ıve or captive-bred male insects to ensure no previous experience with orchids or real females. Damiens & Boivin. This is not because pollinator chemoreceptors have become desensitised or habituated to the orchid scent because if the orchids are moved a few metres. even within a minute for some species. 2000). 1996. the pollinators of Ophrys sphegodes quickly learnt orchid locations and the scents of individual flowers. they typically attract pollinators again (Bates. 2000. Bower. 2002. even when fresh orchids or real female insects are subsequently placed in the same location (Peakall. there is no experimental evidence to show this is adequate to impose selection on pollinators at the level of population or Biological Reviews 86 (2011) 33–75 © 2010 The Author. Wong & Schiestl.. 2008). 2008). Jers´akov´a 69 et al.. Wong et al. 1990. Peakall & Beattie. Gaskett et al. Wong & Schiestl. 2002. Wong. In one study. Post-deception aversion to orchids appears to involve two forms of learning: spatial configuration. 2006a). Ayasse et al. 2002. Stoutamire. Biological Reviews © 2010 Cambridge Philosophical Society . 2001. sexually deceived pollinators generally depart quickly and rarely visit multiple neighbouring orchids (Peakall. and this suggests several interesting hypotheses: is learned avoidance a specific response to orchid deception..Orchid pollination by sexual deception deception. Even if sperm production is not costly. 1990. 1965. mating systems. it is apparent that pollinators and their behaviours. it may even affect a male’s future mating opportunities. 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. 2000. chestermanii) and a similar technique could be used for other parasitoids that act as pollinators for sexually deceptive orchids. mating with orchids may have negative impacts for individual pollinators. 2005. but the rate of insect attraction soon wanes. Bower & Brown. Peakall et al. 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. i. 1999).e. or be unable to find real female mates among false orchid signals (Coate. If he then soon encounters a real female. Bower. a male could become temporarily sperm depleted during an orchid visit. 1996. 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. Another unknown component is the influence of positive and negative reinforcement. Schiestl. and recognition of signals or sensory information (Dukas. 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. ie. Salzmann & Schiestl. 1996. but G¨ogler et al. Therefore many insects from a pollinating species may never or only rarely encounter a sexually deceptive orchid. pollinator ejaculation has been studied in so few species that it may be more common than currently believed. 2004). Alcock. Fieldworkers frequently report that when an orchid flower is artificially introduced into an area. Vereecken & Schiestl. 1997. Bower & Brown. COSTS OF DECEPTION AND ORCHID-POLLINATOR COEVOLUTION Sexually deceptive orchids generally exert little influence on the evolution of their pollinators (Schiestl. 2006). VIII. and avoided them when tested a few minutes later (Ayasse et al. diversity. 2008). such as attempting to mate with a dead or heterospecific female? Does learned avoidance improve pollinator fitness. 2000.. 2000.

pollination involves copulation or simple gripping of the orchid. Stephen Hopper (Royal Botanic Gardens. Lepanthes. Mormolyca. an average of 20. Caleana. Orchis galilaea and Caladenia patersonii). C. (c) Future studies involving gas chromatographyelectroantennography (GC-EAG or GC-EAD) can be enhanced by reporting factors such as the number of trials.4% ± 17. sexually deceptive orchid genera have been identified in Australia and New Zealand (2) (3) (4) (5) (6) (7) (8) (Arthrochilus. In some cases. N = 21). and the influence of positive and negative reinforcement. antagonistic coevolution remains a tantalising hypothesis for future research. CONCLUSIONS (1) At present. Cryptostylis. ACKNOWLEDGEMENTS I thank Marie Herberstein and Andy Beattie (Macquarie University). which are typically from species that are solitary rather than social and are haplodiploid. (d) Although more studies of colour mimicry in sexual deception are desirable. Caladenia. Orchid speciation may be facilitated by high insect diversity if this fuels pollinator shifts and provides new pollinators for hybrids and mutants. 37. FUTURE DIRECTIONS (a) Fundamental natural history observations of pollinator identity and sexual behaviour with poorly known orchids are crucial for conservation and knowledge. Leporella. There is considerable diversity in the behaviour of sexually deceived pollinators among different orchid species. N = 8) and temperate Australia (18. even if orchids impose minor costs on individual pollinators. the functions of multiple signal modes. Central and South America (Geoblasta. N = 35 species).4. thorough. 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 1.4 ± 11. and more generally. Spiculaea and potentially Pterostylis). Europe (Ophrys. Alternative deceptive interactions such as exploitation of pollinator sensory biases are also likely. Trigonidium and potentially Tolumnia). contentious taxa (e. Stellilabium. This work was generously Biological Reviews 86 (2011) 33–75 © 2010 The Author. (b) Investigating pollinator mating systems and the consequences of haplodiploidy and indirect selection offers new frameworks for researching sexual deception. these may be insufficient to drive selection at a population or species level. and thoughtful comments on the manuscript.5 ± 14. A literature survey reveals that for sexually deceptive orchids. Rare examples of sexual deception provoking pollinator ejaculation may exert considerable costs on the pollinator. XI. exploitation of sensory biases. hymenopteran evolution and behavioural ecology. or set fruit. monandrous. (h) Costs imposed on pollinators by deception remain unquantified and evidence for antagonistic coevolution between orchids and their deceived pollinators merits considerable attention. X. Sexually deceptive orchids are pollinated only by male insects. and the magnitude of responses observed.g. Thus. Observations suggest that pollinators commonly exhibit learned avoidance of orchids or orchid locations.. Orchis). with emphasis on pollinator perception and experimental manipulations involving multiple sensory modes. Generally. Telipogon. olfactory receptors and visual pigments) and pollinator learning and memory. Greg Holwell (University of Auckland) and anonymous referees for their constructive. Pollination rates per flower are similar in Europe (18. Chiloglottis. pollinators are trapped briefly. Paracaleana. Most photographs were kindly provided by Julia Cooke (Macquarie University).5 ± 20.A. and potentially Japan (Cymbidium pumilum). Graham Brown (Museum and Art Gallery of the Northern Territory). (e) Investigation of floral shape provides many new or under-studied opportunities for research: mimicry. and the evolution of floral trap morphology. visual and tactile mimicry require further attention. Although scent mimicry is increasingly well studied. Generally.g. Calochilus. or alternatively. This is especially so for highly endemic and diverse orchid regions such as Australia and Central and South America. investigating how orchids exploit pollinator visual biases and employ sensory traps would make a more widely applicable contribution to the field of deceptive signalling. Drakaea. IX. number of unresponsive antennae.4%. and among different individuals of the pollinator species.D. Biological Reviews © 2010 Cambridge Philosophical Society .g. Colin Bower (FloraSearch). and considering whether these factors vary consistently with pollinator mating systems or behaviours. (f) Current molecular studies of orchid signal expression could be accompanied by research into the genetic factors influencing pollinator perception of signals (e. Ejaculation is rare. and polygynous. Cymbidium pumilum and Pterostylis).9% of plants (N = 11 species) had pollinia collected and deposited. and species that may combine aspects of both sexual and food deception (e.7% of all flowers (mean ± S. South Africa (Disa). Gaskett 70 species. but this is yet to be demonstrated empirically. (g) Future topics to address in pollinator learning include the temporal longevity of memory. the effect of shape variation on pollinator learning. Trichoceros.

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