Gaskett - Orchid Pollination by Sexual Deception Pollinator Perspectives (1)

Biol. Rev. (2011), 86, pp. 33–75. 33doi: 10.1111/j.1469-185X.2010.00134.x

Orchid pollination by sexual deception:pollinator perspectives

A. C. Gaskett1,2∗1 Department of Biological Sciences, Macquarie University, NSW 2109, Australia2 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 ofpollinators and pollination systems. Sexually deceptive orchids are adapted to attract specific male insects that are fooledinto attempting to mate with orchid flowers and inadvertently acting as pollinators. This review summarises currentknowledge, explores new hypotheses in the literature, and introduces some new approaches to understanding sexualdeception from the perspective of the duped pollinator. Four main topics are addressed: (1) global patterns in sexualdeception, (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 onpollinators by orchids. A global list of known and putative sexually deceptive orchids and their pollinators is providedand 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 deceptivespecies and genera are reported for New Zealand and South Africa. In Central and Southern America, Asia, and thePacific many more species are likely to be identified in the future. Despite the great diversity of sexually deceptive orchidgenera 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 orchidsinclude pre-copulatory gripping of flowers, brief entrapment, mating, and very rarely, ejaculation. Pollinator behaviourvaries within and among pollinator species.

Deception involving orchid mimicry of insect scent signals is becoming well understood for some species, butvisual and tactile signals such as colour, shape, and texture remain neglected. Experimental manipulations that testfor function, multi-signal interactions, and pollinator perception of these signals are required. Furthermore, otherforms of deception such as exploitation of pollinator sensory biases or mating preferences merit more comprehensiveinvestigation. Application of molecular techniques adapted from model plants and animals is likely to deliver newinsights into orchid signalling, and pollinator perception and behaviour.

There is little current evidence that sexual deception drives any species-level selection on pollinators. Pollinators dolearn to avoid deceptive orchids and their locations, but this is not necessarily a response specific to orchids. Even insystems where evidence suggests that orchids do interfere with pollinator mating opportunities, considerable furtherresearch is required to determine whether this is sufficient to impose selection on pollinators or generate antagonisticcoevolution or an arms race between orchids and their pollinators.

Botanists, taxonomists and chemical ecologists have made remarkable progress in the study of deceptive orchidpollination. Further complementary investigations from entomology and behavioural ecology perspectives shouldprove fascinating and engender a more complete understanding of the evolution and maintenance of such enigmaticplant-animal interactions.

Key words: orchid, pollinator behaviour, mating behaviour, insects, floral scent, colour and shape, mimicry, sensorybiases, learning, evolution.

* Address for correspondence: E-mail: [email protected]

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

34 A. C. Gaskett

CONTENTS

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34II. Pollination by sexual deception . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35

III. Pollinators of sexually deceptive orchids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35(1) Pollinator identities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59(2) Pollinator mating systems and traits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60(3) Exceptions to the general types of pollinators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60

IV. Pollinator behaviours . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62(1) Pollinator behaviour and the origins of sexual deception . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62(2) Pollinator sexual behaviour with orchids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62(3) Sexual deception by Pterostylis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63(4) Within-species variation in pollinator behaviour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63

V. Pollinator abundance and diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64VI. Orchid signals and pollinator perception . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65

(1) Scent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65(2) Colour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66(3) Shape . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67(4) Multimodal signalling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68

VII. Pollinator learning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68VIII. Costs of deception and orchid-pollinator coevolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69

IX. Future directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70X. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70

XI. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70XII. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71

I. INTRODUCTION

Sexual deception is an extreme form of pollinator specialisa-tion in which an orchid lures its pollinator with fraudulent sexsignals. Male insects fooled into sexual behaviour with orchidflowers inadvertently collect or deliver the pollinia and donot receive floral rewards such as nectar or pollen (Schiestl,2005; Jersakova, Johnson & Kindlmann, 2006a). In spe-cialist pollination systems, flowers are unconstrained by thestabilising selection that limits generalist pollination systemsto floral forms suiting several pollinators (Cresswell, 1998;2000). Instead, specialist flowers can evolve specific fitness-enhancing adaptations to their pollinator, e.g. corollas thatmatch pollinator tonguelength (Alexandersson & Johnson,2002; Rodríguez-Girones & Santamaría, 2007; Muchhala& Thomson, 2009). Sexually deceptive orchids are highlyspecialised and typically pollinator-specific, thus pollinatorpreferences and pollinator-driven selection are likely to bestrongly directional and influence orchid floral features anddiversity (Peakall & Handel, 1993; Cozzolino & Widmer,2005; Mant, Peakall & Schiestl, 2005d; Schiestl & Schluter,2009). Investigation of how pollinators and their behavioursmight affect the evolution and maintenance of sexual decep-tion by orchids provides new insights into this intriguingsubject.

Sexual deception relies on the pollinator’s sexual ratherthan foraging behaviour, suggesting insect sexual behaviouris crucial in driving the evolution of orchid features. Analysisof the sexual behaviours stimulated by orchids and the nat-ural mating systems of pollinators in the absence of orchidscould reveal which types of insects and behaviours permit and

maintain deception. Furthermore, as sexual deception reliesupon exploiting pollinator sensory ecology, insect perceptionof signals is fundamental for selection on orchid features.Insects are capable of sophisticated learning, memory, andcognition (Dukas, 2008), which are also likely to affect orchidsignals and the evolution of deception.

Recent reviews discuss the mechanisms of orchiddeception and the selective pressures on orchids influencingthe evolution of deception (Schiestl, 2005; Jersakova et al.,2006a; Schaefer & Ruxton, 2009; Vereecken, 2009), and howorchid ecology, pollination biology, genetics, mycorrhizalassociations, and environmental factors affect orchidspeciation (Tremblay, 1992; Vasquez, Ibisch & Gerkmann,2003; Gravendeel et al., 2004; Cozzolino & Widmer, 2005;Tremblay et al., 2005; Peakall, 2007; Schluter & Schiestl,2008; Waterman & Bidartondo, 2008; Phillips et al., 2009a;Schiestl & Schluter, 2009). Here, however, sexually deceptivepollination is considered from the pollinator perspective.

This review summarises current knowledge, explores newhypotheses in the literature, and introduces some newapproaches as to how pollinators and their mating sys-tems, behaviour, sensory perception and diversity couldinfluence the evolution of sexual deception. Contemporaryand historic data are synthesised and evaluated from bothbroadlyaccessible and lesser-known sources, and from experi-ments, comparative studies, and natural history observations.The first part of this review concerns pollinators and theirbehaviour during pollination. Pollinator identity and naturalmating systems are surveyed and broad patterns in pollinatorsexual behaviours during visits to different types of orchidsare identified. Evidence for sexual deception in the poorly


Orchid pollination by sexual deception 35

known Pterostylis complex is evaluated. The second and majorelement of this review discusses orchid signals and the mecha-nisms of deception by considering how orchids mimic femaleinsects and exploit male insects’ sensory biases. Attempts toanalyse pollinator perception of orchid scent and colour sig-nals are reviewed and topics for productive further researchare identified. The third section of this review addressesthe question of whether sexual deception could involveavoidance learning by pollinators, corresponding selectionon pollinators by orchids, and consequently coevolutionbetween orchids and pollinators. I evaluate whether orchidscould impose costs on their pollinators at the individual,population, or species level. Finally, I propose some futuredirections promoting research into pollinator perspectives.

Reflecting current knowledge, this review focuses pri-marily on European and Australian orchid species. Speciesfrom Central and Southern America, South Africa and NewZealand have been the subjects of fewer studies and conse-quently, they are covered in less detail here. The taxonomyof Australasian orchids is undergoing considerable revision(see Hopper, 2009). I use the most commonly recognisedgenera and species names, with reference to the AustralianPlant Names Index (Centre for Plant Biodiversity Research,2008). Table 1 also provides the newer names for generafrom revisions by Jones (2006). European orchids are namedaccording to the International Plant Names Index (2008) andDelforge (2005). European pollinator names are accordingto Fauna Europaea (2004).

II. POLLINATION BY SEXUAL DECEPTION

Although an absence of floral rewards occurs at leastintermittently in species from almost all major angiospermgroups, obligatory deception is most common amongstorchids (Schiestl, 2005; Renner, 2006). Many orchid speciesare ‘food-deceptive’ in that they resemble rewarding flowersbut do not provide food rewards, and are pollinated byfemale and male insects attempting to feed from the flowers(Jersakova et al., 2006a). Sexual deception is less commonthan food deception in the orchids, but has nonethelessevolved multiple times in different lineages (Kores et al., 2001;Cozzolino & Widmer, 2005). Currently, there are thoughtto 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 forspecies with known pollinators; Figs 1 and 2 for images).In New Zealand, several of these genera are representedby endemic species or occasional vagrants from Australia(Caladenia, Caleana, Calochilus, Chiloglottis, Cryptostylis, andPterostylis; St George, 1999). However, conclusive pollinatoridentifications and evidence of sexual deception amongstNew Zealand species is largely absent. Tentative pollinator

identifications for some potentially sexually deceptive NewZealand species are listed in Table 1. The accepted numberof sexually deceptive genera in Australia is likely to change ifreports of sexual deception in Pterostylis cannot be confirmedor 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 orchidgenera, but sexual deception is restricted to the largeand well-studied genus Ophrys, and a single species of therelated and generally food-deceptive genus Orchis (Table 1;Bino, Dafni & Meeuse, 1982; Widmer, Cozzolino & Dafni,2001). Perhaps surprisingly, only two South African sexuallydeceptive species are known, both from the well-studied andgenerally rewarding or food-deceptive genus Disa (Table 1;Steiner, Whitehead & Johnson, 1994; Johnson, Linder &Steiner, 1998). Although no sexually deceptive orchids areknown for North America, sexual deception is confirmedfor species from eight South and Central American orchidgenera, and more cases are likely to be recognised in thefuture (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 arelisted in Table 1, this is a diverse and highly regionallyendemic neotropical genus and sexual deception is suspectedfor many species (Vasquez et al., 2003; Blanco & Barboza,2005; Schiestl, 2005). Similarly, there are approximately 15potentially sexually deceptive Cryptostylis species distributedthroughout the Asia-Pacific region, but sexual deceptionis confirmed for only the five species from Australia andNew Zealand (Jones, 2006; Table 1). Subantarctic sexualdeception is also a possibility; Chiloglottis and Pterostylis speciesgrow on New Zealand’s subantarctic islands (Meurk, Foggo& Wilson, 1994; Molloy, 2002).

When data from food- and sexually deceptive orchidsare combined, pollination success is higher in southerntemperate 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 onlysexually deceptive orchid species (Table 1), there is nosignificant difference in the pollination rates of flowersfrom 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 elsewhereprevents comparisons for these regions (see Table 1 for asummary of the pollination rates reported in the literature).

III. POLLINATORS OF SEXUALLY DECEPTIVEORCHIDS

Sexually deceptive orchid species typically exploit one orfew specific pollinator species, (Table 1), and may havedifferent pollinators in different regions (e.g. Chiloglot-

tis species; Bower & Brown, 2009). A single insect


36 A. C. Gaskett

Tab

le1.

Sexu

ally

dece

ptiv

eor

chid

spec

ies

and

thei

rpo

llina

tors

.All

polli

nato

rsar

em

ale,

exce

ptw

here

afe

mal

epo

llina

tor

issp

ecifi

cally

stat

ed.A

ques

tion

mar

k(?

)afte

rth

epo

llina

tor

nam

ein

dica

tes

apu

tativ

era

ther

than

confi

rmed

polli

nato

r.W

hen

data

are

repo

rted

from

mor

eth

anon

est

udy,

sym

bols

(*,† ,o

r‡ )c

orre

spon

dbe

twee

nth

eda

taan

dci

tatio

n.‘P

ro.h

ybr.

’afte

ra

spec

ies

nam

ein

dica

tes

itw

asde

scri

bed

asan

occa

isio

nalh

ybri

dby

Del

forg

e(2

005)

.For

Gro

wth

form

,E=

epip

hytic

,T=

terr

estr

ial.

For

Polli

nato

rse

xual

beha

viou

rst

imul

ated

byth

eor

chid

:1=

polli

nato

rco

pula

tes

and

ejac

ulat

eson

the

orch

id,2

=po

llina

tor

copu

late

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chid

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polli

nato

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orlif

tshi

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polli

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brie

flytr

appe

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dtr

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nia

ones

cape

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=po

llina

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ely

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volv

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beha

viou

r,bu

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sis

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nfirm

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flow

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dis

the

perc

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geof

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had

polli

nia

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depo

site

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%pl

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rate

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ra3

Phill

ips

etal

.(20

09a)



Cal

aden

ia(sy

n.A

rach

norc

his)

atting

ens

Hop

per

&A

.P.B

r.su

bsp.

atting

ens

TM

acro

thyn

nus

sp.

Tip

hiid

ae;

Hym

enop

tera

319

.9Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.A

rach

norc

his)

auru

lent

a(D

.L.J

ones

)R

.J.B

ates

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3

Bat

es(2

009a

)

Cal

aden

ia(sy

n.A

rach

norc

his)

aust

ralis

G.W

.Car

rT

Phy

mat

othy

nnus

nr.n

itid

us1

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.D

rako

norc

his)

barb

aros

saR

chb.

f.T

Thy

nnoi

des

sp.*

(Thy

nnoi

des

bide

ns(S

auss

ure)

inac

cura

te,G

.Bro

wn

pers

.com

m.)

Tip

hiid

ae;

Hym

enop

tera

31.

8*C

olem

an(1

930)

;Sto

utam

ire

(197

4,19

79,1

983)

;Bro

wn

etal

.(19

97);

Phill

ips

etal

.(2

009a

)*C

alad

enia

(syn.

Ara

chno

rchi

s)be

hrii

Schl

tdl.

TT

achy

nom

yia

sp.

Tip

hiid

ae;

Hym

enop

tera

314

(782

)D

icks

on&

Petit

(200

6)

Cal

aden

ia(sy

n.A

rach

norc

his)

bran

whi

tei

D.L

.Jon

esT

Phy

mat

othy

nnus

mon

ilic

orni

s(S

m.)

com

plex

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.A

rach

norc

his)

brow

niiH

oppe

r&

A.P

.Br.

TZ

aspi

loth

ynnu

ssp

.T

iphi

idae

;H

ymen

opte

ra3

Bat

es(2

009b

)

Cal

aden

ia(sy

n.Jon

esio

psis

)ca

irns

iana

F.M

uell.

TT

hynn

oide

ssp

.P

hym

atot

hynn

usni

tidu

sSm

.?*

Phy

mat

othy

nnus

vict

orT

urne

r†

Tip

hiid

ae;

Hym

enop

tera

332

.1†

Stou

tam

ire

(197

4,19

83);

Bro

wn

etal

.(19

97)*

;Phi

llips

etal

.(2

009a

)†

Cal

aden

ia(sy

n.A

rach

norc

his)

calc

icol

aG

.W.C

arr

TP

hym

atot

hynn

usnr

.nitid

us1

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.A

rach

norc

his)

Cal

litr

ophi

laD

.L.J

ones

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3

C.C

.Bow

er(u

npub

lishe

dda

ta)

Cal

aden

ia(sy

n.A

rach

norc

his)

caud

ata

Nic

holls

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3?

Hop

per

&B

row

n(2

001)

Cal

aden

ia(sy

n.A

rach

norc

his)

clav

iger

aA

.Cun

n.ex

Lin

dl.

TP

hym

atot

hynn

usm

onilic

orni

s(S

m.)

com

plex

*,L

opho

chei

lus

anilitat

us(S

m.)†

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)*;

Bat

es(2

009a

)†

Cal

aden

ia(sy

n.A

rach

norc

his)

clav

ula

D.L

.Jon

esT

Les

tric

othy

nnus

sp.

Tip

hiid

ae;

Hym

enop

tera

3B

ates

(200

9a)

Cal

aden

ia(sy

n.A

rach

norc

his)

conc

inna

(Rup

p)D

.L.J

ones

&M

.A.C

lem

.

TA

eolo

thyn

nus

gene

rosu

s(T

urne

r)T

iphi

idae

;H

ymen

opte

ra3

Phill

ips

etal

.(20

09a)

Cal

aden

iaaf

f.co

ncin

naT

Neo

zele

bori

anr

.vol

atile

(Sm

.)T

iphi

idae

;H

ymen

opte

ra3

Phill

ips

etal

.(20

09a)

Cal

aden

ia(sy

n.A

rach

norc

his)

conc

olor

Fitz

g.T

Thy

nnin

ew

asp

Tip

hiid

ae;

Hym

enop

tera

3C

.C.B

ower

(unp

ublis

hed

data

)


38 A. C. GaskettT

able

1.(C

ont.)

Orc

hid

Gro

wth

form

Polli

nato

rPo

llina

tor

Fam

ily;O

rder

Polli

nato

rse

xual

beha

viou

r%

flow

ers

polli

nate

d(N

)%

plan

tspo

llina

ted

(N)

Sour

ce

Cal

aden

ia(sy

n.A

rach

norc

his)

conf

erta

D.L

.Jon

esT

Thy

nnin

ew

asp

Tip

hiid

ae;

Hym

enop

tera

3B

ates

(200

9a)

Cal

aden

ia(sy

n.A

rach

norc

his)

cory

neph

ora

A.S

.Geo

rge

TT

hynn

ine

was

p;L

estr

icot

hynn

usm

odes

tus

(Sm

.)*

Tip

hiid

ae;

Hym

enop

tera

3St

outa

mir

e(1

983)

;Bro

wn

etal

.19

97;v

ande

rC

inge

l(20

01)*

;Ph

illip

s,et

al.(

2009

)*C

alad

enia

(syn.

Ara

chno

rchi

s)cr

ebra

A.S

.Geo

rge

TC

ampy

loth

ynnu

sas

sim

ilis

Sm.C

.fla

vopi

ctus

(Sm

.)T

iphi

idae

;H

ymen

opte

ra3

Bro

wn

etal

.(19

97)

Cal

aden

ia(sy

n.A

rach

norc

his)

cruc

ifor

mis

D.L

.Jon

esT

Phy

mat

othy

nnus

nr.n

itid

us1

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.A

rach

norc

his)

crus

cula

Hop

per

&A

.P.B

r.

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3

Hop

per

&B

row

n(2

001)

Cal

aden

ia(sy

n.A

rach

norc

his)

deco

raH

oppe

r&

A.P

.Br.

TZ

aspi

loth

ynnu

sni

grip

esG

ueri

nT

iphi

idae

;H

ymen

opte

ra3

14.3

Phill

ips

etal

.(20

09a)

Cal

aden

ia(sy

n.A

rach

norc

his)

dila

tata

R.B

r.T

Thy

nnoi

des

grac

ilis

(Wes

twoo

d),T

hynn

oide

ssp

p.

Tip

hiid

ae;

Hym

enop

tera

3St

outa

mir

e(1

983)

;but

see

van

der

Cin

gel(

2001

)for

seve

ral

othe

rso

urce

s)C

alad

enia

(syn.

Ara

chno

rchi

s)di

scoi

dea

Lin

dl.

TP

hym

atot

hynn

ussp

.T

iphi

idae

;H

ymen

opte

ra3

Phill

ips

etal

.(20

09a)

Cal

aden

iadi

lata

tava

r.rh

ombo

idifor

mis

E.C

olem

an

TIc

hneu

mon

idsp

.?Ic

hneu

mon

idae

;H

ymen

opte

ra3?

Col

eman

(193

0)

Cal

aden

iado

ugla

sior

um(D

.L.J

ones

)G.N

.Bac

kh.

TP

hym

atot

hynn

usnr

.nitid

us1

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.Jon

esio

psis

)do

utch

iae

O.H

.Sar

g.T

Thy

nnin

ew

asp*

,P

hym

atot

hynn

us?n

itid

us†

Tip

hiid

ae;

Hym

enop

tera

3St

outa

mir

e(1

983)

*;B

row

net

al.

(199

7)†

Cal

aden

ia(sy

n.A

rach

norc

his)

exst

ans

Hop

per

&A

.P.B

r.

TT

hynn

oide

ssp

.T

iphi

idae

;H

ymen

opte

ra3

Phill

ips

etal

.(20

09a)

Cal

aden

ia(sy

n.A

rach

norc

his)

falc

ata

(Nic

holls

)M

.A.C

lem

.&H

oppe

r

TZ

eleb

oria

mar

gina

lis

(Wes

twoo

d)*† ,

Thy

nnoi

des

sp.† ,

(Thy

nnoi

des

bide

ns*

inac

cura

te;G

.Bro

wn

pers

.com

m.)

Tip

hiid

ae;

Hym

enop

tera

38.

3*B

row

net

al.(

1997

)*;P

hilli

pset

al.

(200

9a)†

Cal

aden

ia(sy

n.A

rach

norc

his)

ferr

ugin

eaN

icho

llsT

Thy

nnin

ew

asp

Tip

hiid

ae;

Hym

enop

tera

314

.4Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.Jon

esio

psis

)fil

amen

tosa

R.B

r.T

Chi

loth

ynnu

str

ocha

nter

inus

Bro

wn

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.A

rach

norc

his)

fitzg

eral

dii

Rup

pT

Thy

nnin

ew

asp

Tip

hiid

ae;

Hym

enop

tera

3C

.C.B

ower

(unp

ublis

hed

data

)

Cal

aden

ia(sy

n.A

rach

norc

his)

form

osa

G.W

.Car

rT

Phy

mat

othy

nnus

nr.

pygi

dial

is1

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)



Cal

aden

ia(sy

n.A

rach

norc

his)

frag

rant

issi

ma

D.L

.Jon

es&

G.W

.Car

r

TP

hym

atot

hynn

usnr

.pyg

idia

lis

2T

iphi

idae

;H

ymen

opte

ra3

Phill

ips

etal

.(20

09a)

Cal

aden

ia(sy

n.A

rach

norc

his)

gard

neri

Hop

per

&A

.P.B

r.

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3

Bro

wn

etal

.(19

97);

S.D

.Hop

per

(unp

ublis

hed

data

)

Cal

aden

ia(sy

n.A

rach

norc

his)

geor

gei

Hop

per

&A

.P.B

r.

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3

Bat

es(2

009b

)

Cal

aden

ia(sy

n.A

rach

norc

his)

glad

iola

taR

.S.R

oger

sT

Zas

pilo

thyn

nus

sp.

Tip

hiid

ae;

Hym

enop

tera

3B

ates

(200

9a)

Cal

aden

ia(sy

n.A

rach

norc

his)

hast

ata

(Nic

holls

)Rup

pT

Lop

hoch

eilu

svi

llos

usG

ueri

nT

iphi

idae

;H

ymen

opte

ra3

(Pri

tcha

rd,2

007)

Cal

aden

ia(sy

n.A

rach

norc

his)

aff.

hebe

rlea

naH

oppe

r&

A.P

.Br.

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3

Bro

wn

etal

.(19

97);

S.D

.Hop

per

(unp

ublis

hed

data

)

Cal

aden

ia(sy

n.A

rach

norc

his)

hueg

elii

Rch

b.f.

TZ

aspi

loth

ynnu

ssp

.T

iphi

idae

;H

ymen

opte

ra3

7.3*

Stou

tam

ire

(198

3);P

hilli

pset

al.

(200

9a)*

Cal

aden

ia(sy

n.Jon

esio

psis

)in

cras

sata

Hop

per

&A

.P.B

r.

TZ

aspi

loth

ynnu

ssp

.T

iphi

idae

;H

ymen

opte

ra3

Bat

es(2

009b

)

Cal

aden

ia(sy

n.A

rach

norc

his)

infu

ndib

ular

isA

.S.G

eorg

e

TZ

aspi

loth

ynnu

ssp

.T

iphi

idae

;H

ymen

opte

ra3

Bat

es(2

009b

)

Cal

aden

ia(sy

n.A

rach

norc

his)

insu

lari

sG

.W.C

arr

TP

hym

atot

hynn

usnr

.nitid

us1

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.A

rach

norc

his)

inte

gra

E.C

olem

anT

Gue

rini

ussp

.?*,

thyn

nine

was

p†

Tip

hiid

ae;

Hym

enop

tera

3St

outa

mir

e(1

983)

*;B

row

net

al.

(199

7)†

Cal

aden

ia(sy

n.A

rach

norc

his)

lept

ocla

via

D.L

.Jon

esT

Phy

mat

othy

nnus

mon

ilic

orni

s(S

m.)

com

plex

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.A

rach

norc

his)

loba

taFi

tzg.

TT

hynn

ine

was

p(T

hynn

oide

spr

eiss

i&

T.bi

dens

inac

cura

te;G

.Bro

wn

pers

.com

m.)

Tip

hiid

ae;

Hym

enop

tera

3St

outa

mir

e(1

979,

1983

);B

row

net

al.(

1997

)

Cal

aden

ia(sy

n.A

rach

norc

his)

low

anen

sis

G.W

.Car

rT

Phy

mat

othy

nnus

nr.n

itid

us1

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.A

rach

norc

his)

mac

rost

ylis

Fitz

g.T

Tac

hyno

myi

asp

.T

iphi

idae

;H

ymen

opte

ra3

(Sto

utam

ire,

1983

)

Cal

aden

ia(sy

n.A

rach

norc

his)

mag

nicl

avat

aN

icho

llsT

Thy

nnin

ew

asp

Tip

hiid

ae;

Hym

enop

tera

3B

ates

(200

9b)


40 A. C. GaskettT

able

1.(C

ont.)

Orc

hid

Gro

wth

form

Polli

nato

rPo

llina

tor

Fam

ily;O

rder

Polli

nato

rse

xual

beha

viou

r%

flow

ers

polli

nate

d(N

)%

plan

tspo

llina

ted

(N)

Sour

ce

Cal

aden

ia(sy

n.A

rach

norc

his)

mon

tana

G.W

.Car

rT

Phy

mat

othy

nnus

sp.

Tip

hiid

ae;

Hym

enop

tera

3B

ower

(200

1b)

Cal

aden

ia(sy

n.Jon

esio

psis

)m

ulticl

avia

Rch

b.f.

TT

achy

nom

iasp

.T

iphi

idae

;H

ymen

opte

ra3

(Sto

utam

ire,

1983

;Bro

wn

etal

.19

97)

Cal

aden

ia(sy

n.A

rach

norc

his)

necr

ophy

lla

D.L

.Jon

esT

Thy

nnoi

des

seni

lis

(Eri

chso

n)T

iphi

idae

;H

ymen

opte

ra

3B

ates

(200

9a)

Cal

aden

ia(sy

n.Jon

esio

psis

)pa

chyc

hila

Hop

per

&A

.P.B

r.

TT

hynn

ine

was

p*;

Phy

mat

othy

nnus

?nitid

us†

Tip

hiid

ae;

Hym

enop

tera

3B

row

net

al.(

1997

)† ;Hop

per

&B

row

n(2

001)

*

Cal

aden

ia(sy

n.A

rach

norc

his)

parv

aG

.W.C

arr

TL

opho

chei

lus

anilitat

us(S

m.)

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.A

rach

norc

his)

pect

inat

aR

.S.R

oger

sT

Zel

ebor

iam

argi

nalis

(Wes

twoo

d)(a

sZ

.m

argi

natu

s);Z

aspi

loth

ynnu

sni

grip

esG

ueri

n*

Tip

hiid

ae;

Hym

enop

tera

3B

row

net

al.(

1997

);Ph

illip

set

al.

(200

9a)*

Cal

aden

ia(sy

n.A

rach

norc

his)

phae

ocla

via

D.L

.Jon

esT

Lop

hoch

eilu

san

ilitat

us(S

m.)

Tip

hiid

ae;

Hym

enop

tera

3B

ower

(199

2);M

ante

tal

.(20

05c);

Phill

ips

etal

.(20

09a)

Cal

aden

ia(sy

n.A

rach

norc

his)

proc

era

Hop

per

&A

.P.B

rT

Zas

pilo

thyn

nus

nigr

ipes

Gue

rin?

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.Jon

esio

psis

)pu

lchr

aH

oppe

r&

A.P

.Br.

(pre

v.C

alad

enia

flacc

ida

subs

p.pu

lchr

aH

oppe

r&

A.P

.Br.

)

TA

eolo

thyn

nus

sp.(

asA

sthe

noth

ynnu

ssp

.)T

iphi

idae

;H

ymen

opte

ra3

Bro

wn

etal

.(19

97);

S.D

.Hop

per

(unp

ublis

hed

data

)

Cal

aden

ia(sy

n.A

rach

norc

his)

radi

ata

Nic

holls

TT

hynn

ine

was

p;Z

aspi

loth

ynnu

ssp

.*,

Cat

oche

ilus

affin

is(G

ueri

n)*

Tip

hiid

ae;

Hym

enop

tera

32.

5*St

outa

mir

e(1

983)

;Phi

llips

etal

.(2

009a

)*

Cal

aden

ia(sy

n.A

rach

norc

his)

reticu

lata

Fitz

gT

Phy

mat

othy

nnus

nr.n

itid

us1*

,Phy

mat

othy

nnus

vict

or†

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)*;

Bat

es(2

009a

)†

Cal

aden

ia(sy

n.A

rach

norc

his)

rhom

boid

ifor

mis

(E.C

olem

an)

M.A

.Cle

m.&

Hop

per

TZ

aspi

loth

ynnu

sni

grip

esG

ueri

nT

iphi

idae

;H

ymen

opte

ra3

Phill

ips

etal

.(20

09a)

Cal

aden

ia(sy

n.A

rach

norc

his)

rich

ards

ioru

mD

.L.J

ones

TP

hym

atot

hynn

usaf

f.py

gidi

alis

Tip

hiid

ae;

Hym

enop

tera

3B

ates

(200

9a)

Cal

aden

ia(sy

n.A

rach

norc

his)

rigi

daR

.S.R

oger

sT

Phy

mat

othy

nnus

sp.

Tip

hiid

ae;

Hym

enop

tera

3B

ates

(200

9a)

Cal

aden

ia(sy

n.A

rach

norc

his)

rile

yiD

.L.J

ones

TT

hynn

oide

sne

wsp

.‘R

’B

row

nT

iphi

idae

;H

ymen

opte

ra3

Phill

ips

etal

.(20

09a)



Cal

aden

ia(sy

n.A

rach

norc

his)

robi

nson

iiG

.W.C

arr

TP

hym

atot

hynn

usnr

.nitid

us1

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.Jon

esio

psis

)ro

eiB

enth

.T

Thy

nnin

ew

asp

Tip

hiid

ae;

Hym

enop

tera

3St

outa

mir

e(1

983)

;Bro

wn

etal

.(1

997)

Cal

aden

ia(sy

n.A

rach

norc

his)

saxa

tilis

(D.L

.Jon

es)

R.J

.Bat

es

TP

hym

atot

hynn

usni

tidu

sT

iphi

idae

;H

ymen

opte

ra3

Bat

es(2

009a

)

Cal

aden

ia(sy

n.A

rach

norc

his)

sept

uosa

D.L

.Jon

esT

Thy

nnoi

des

mes

ople

ural

isT

urne

rT

iphi

idae

;H

ymen

opte

ra3

Bat

es(2

009a

)

Cal

aden

ia(sy

n.A

rach

norc

his)

spec

iosa

Hop

per

&A

.P.B

r.

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3

Bro

wn

etal

.(19

97);

S.D

.Hop

per

(unp

ublis

hed

data

)

Cal

aden

ia(sy

n.A

rach

norc

his)

stel

lata

D.L

.Jon

esT

Phy

mat

othy

nnus

mon

ilic

orni

s(S

m.)*

,Phy

mat

othy

nnus

mon

ilic

orni

sco

mpl

ex*,

Phy

mat

othy

nnus

sp.1

4†

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)*;

Bat

es(2

009a

)†

Cal

aden

ia(sy

n.A

rach

norc

his)

stri

cta

R.J

.Bat

esT

Thy

nnin

ew

asp

Tip

hiid

ae;

Hym

enop

tera

3B

ates

(200

9a)

Cal

aden

ia(sy

n.A

rach

norc

his)

tens

aG

.W.C

arr

TT

hynn

oide

saf

f.gr

acilis

Tip

hiid

ae;

Hym

enop

tera

3B

ates

(200

9a)

Cal

aden

ia(sy

n.A

rach

norc

his)

tent

acul

ata

Schl

tdl.

TT

hynn

oide

spu

gion

atus

Gue

rin

(sp.c

ompl

ex),

T.ru

fitho

rax

Tur

ner,

Thy

nnoi

des

grac

ilis

(Wes

twoo

d)

Tip

hiid

ae;

Hym

enop

tera

336

.4(1

214)

*B

ower

(199

2);P

eaka

ll&

Bea

ttie

(199

6)*;

Man

tetal

.(20

05c);

Phill

ips

etal

.(20

09a)

Cal

aden

iaaf

f.te

ntac

ula

TT

hynn

oide

sne

wsp

.‘D

’Bro

wn

Tip

hiid

ae;

Hym

enop

tera

3C

.C.B

ower

(unp

ublis

hed

data

)

Cal

aden

ia(sy

n.A

rach

norc

his)

tess

elat

aD

.L.J

ones

TP

hym

atot

hynn

usnr

.nitid

us1

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.A

rach

norc

his)

thin

icol

aH

oppe

r&

A.P

.Br

TM

acro

thyn

nus

sp.

Tip

hiid

ae;

Hym

enop

tera

320

.5Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.A

rach

norc

his)

toxo

chila

Tat

eT

Aeo

loth

ynnu

sge

nero

sus

(Tur

ner)

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.A

rach

norc

his)

ulig

inos

aA

.S.G

eorg

eT

Thy

nnin

ew

asp

Tip

hiid

ae;

Hym

enop

tera

3B

ates

(200

9b)

Cal

aden

ia(sy

n.A

rach

norc

his)

valida

(Nic

holls

)M

.A.C

lem

.&D

.L.J

ones

TP

hym

atot

hynn

ussp

.T

iphi

idae

;H

ymen

opte

ra3

Bat

es(2

009a

)


42 A. C. GaskettT

able

1.(C

ont.)

Orc

hid

Gro

wth

form

Polli

nato

rPo

llina

tor

Fam

ily;O

rder

Polli

nato

rse

xual

beha

viou

r%

flow

ers

polli

nate

d(N

)%

plan

tspo

llina

ted

(N)

Sour

ce

Cal

aden

ia(sy

n.A

rach

norc

his)

verr

ucos

aG

.W.C

arr

TZ

aspi

loth

ynnu

ssp

.nov

.5T

iphi

idae

;H

ymen

opte

ra3

Phill

ips

etal

.(20

09a)

Cal

aden

ia(sy

n.A

rach

norc

his)

villos

issi

ma

(G.W

.Car

r)D

.L.J

ones

&M

.A.C

lem

TL

opho

chei

lus

anilitat

us(S

m.)

Tip

hiid

ae;

Hym

enop

tera

3Ph

illip

set

al.(

2009

a)

Cal

aden

ia(sy

n.Jon

esio

psis

)w

anos

aA

.S.G

eorg

eT

Phy

mat

othy

nnus

?nitid

usT

iphi

idae

;H

ymen

opte

ra3

Bro

wn

etal

.(19

97)

Cal

aden

ia(sy

n.A

rach

norc

his)

woo

lcoc

kior

umD

.L.J

ones

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3

Bat

es(2

009a

)

Cal

aden

ia(sy

n.A

rach

norc

his)

zeph

yra

(D.L

.Jon

es)

R.J

.Bat

es

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3

Bat

es(2

009a

)

Cal

eana

maj

orR

.Br.

TL

ophy

roto

ma

leac

hii

(Kir

by)*

,P

tery

goph

orus

sp.† ,

L.cy

anea

(Lea

ch)‡

Perg

idae

;H

ymen

opte

ra3

Cad

y(1

965)

*;B

ates

(198

9)† ;

Hop

per

&B

row

n(2

006)

‡

Cal

eana

(syn.

Sul

liva

nia)

min

orR

.Br.

(pre

v.P

arac

alea

nam

inor

(R.B

r.)

Bla

xell)

TIs

war

oide

sar

mig

er(T

urne

r)(p

rev.

Thy

nnot

urne

ria

arm

iger

)

Tip

hiid

ae;

Hym

enop

tera

3B

ower

(200

1c)

Cal

ochi

lus

caer

uleu

sL

.O.W

illia

ms

(as

Cal

ochi

lus

holtze

iF.

Mue

ll.)

TC

amps

omer

issp

.Sc

oliid

ae;

Hym

enop

tera

2Jo

nes

&G

ray

(197

4);B

ower

(200

1d)

Cal

ochi

lus

cam

pest

ris

R.B

r.T

Cam

psom

eris

tasm

anie

nsis

Saus

sure

Scol

iidae

;H

ymen

opte

ra2

Ford

ham

(194

6);B

ower

&B

ranw

hite

(199

3)C

aloc

hilu

scu

preu

sR

.S.R

oger

sT

Scol

iidw

asp

(also

self-

polli

nate

s)Sc

oliid

ae;

Hym

enop

tera

2B

ates

(200

9a)

Cal

ochi

lus

plat

ychi

lus

D.L

.Jon

esT

Scol

iidw

asp

(also

self-

polli

nate

s)Sc

oliid

ae;

Hym

enop

tera

2B

ates

(200

9a)

Cal

ochi

lus

prui

nosu

sD

.L.J

ones

TSc

oliid

was

p(a

lsose

lf-po

llina

tes)

Scol

iidae

;H

ymen

opte

ra2

Bat

es(2

009a

)

Chi

logl

ottis

anat

icep

sD

.L.J

ones

TN

eoze

lebo

ria

n.sp

.33

Bro

wn

Tip

hiid

ae;

Hym

enop

tera

3M

ante

tal

.(20

05c)

Chi

logl

ottis

(syn.

Sim

plig

lottis

)ch

lora

ntha

D.L

.Jon

esT

Neo

zele

bori

aim

patien

sSm

.N

.af

f.im

patien

sT

iphi

idae

;H

ymen

opte

ra3

Man

tetal

.(20

02);

Man

tetal

.(2

005c

,d)

Chi

logl

ottis

diph

ylla

R.B

r.T

Art

hrot

hynn

usla

tus

Bro

wn,

A.an

gust

usB

row

n,N

eoze

lebo

ria

nrsp

.25(

A)*

Tip

hiid

ae;

Hym

enop

tera

3B

ower

,(19

96)*

;Man

t,et

al.

(200

5c)

Chi

logl

ottis

(syn.

Myr

mec

hila

)fo

rmic

ifer

aFi

tzg.

TN

eoze

lebo

ria

n.sp

.41

Bro

wn

Tip

hiid

ae;

Hym

enop

tera

3B

ower

,(19

92,1

996)

;Man

tetal

.(2

002,

2005

c,d)

Chi

logl

ottis

aff.

form

icifer

a1

TN

eoze

lebo

ria

n.sp

.45

Bro

wn

Tip

hiid

ae;

Hym

enop

tera

3M

ante

tal

.(20

02,2

005c

,d)

Chi

logl

ottis

aff.

form

icifer

a2

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3

C.C

.Bow

er(u

npub

lishe

dda

ta)



Chi

logl

ottis

(syn.

Sim

plig

lottis

)gr

amm

ata

G.W

.Car

rT

Eir

one

leai

Tur

ner

Tip

hiid

ae;

Hym

enop

tera

3M

ante

tal

.(20

02,2

005c

)

Chi

logl

ottis

(syn.

Sim

plig

lottis

)gu

nnii

Lin

dl.

TE

iron

esp

.T

iphi

idae

;H

ymen

opte

ra3

Stou

tam

ire

(197

5)

Chi

logl

ottis

(syn.

Sim

plig

lottis

)je

anes

iiD

.L.J

ones

TN

eoze

lebo

ria

nrim

patien

s2

Tip

hiid

ae;

Hym

enop

tera

3B

ower

&B

row

n(2

009)

Chi

logl

ottis

pala

chila

D.L

.Jon

es&

M.A

.Cle

m.

TC

hilo

thyn

nus

pala

chilus

Bro

wn

Tip

hiid

ae;

Hym

enop

tera

3M

ante

tal

.(20

05c)

Chi

logl

ottis

(syn.

Myr

mec

hila

)pl

atyp

tera

D.L

.Jon

esT

Neo

zele

bori

an.

sp.4

0B

row

nT

iphi

idae

;H

ymen

opte

ra3

Bow

er(1

992,

1996

);M

ante

tal

.20

02,2

005c

,d)

Chi

logl

ottis

(syn.

Sim

plig

lottis

)pl

uric

alla

taD

.L.J

ones

TN

eoze

lebo

ria

impa

tien

sSm

.N

.aff.

impa

tien

sT

iphi

idae

;H

ymen

opte

ra3

Bow

er(1

992,

1996

);M

ante

tal

.(2

002,

2005

a,c,

d)

Chi

logl

ottis

aff.

plur

ical

lata

(also

refe

rred

toas

Chi

logl

ottis

‘bifar

ia’

D.L

.Jon

esm

.s)

TN

eoze

lebo

ria

tabu

lata

Bro

wn

Tip

hiid

ae;

Hym

enop

tera

3M

ante

tal

.(20

02,2

005a

,c,d

)

Chi

logl

ottis

aff.

plur

ical

lata

1T

Neo

zele

bori

ata

bula

taB

row

nT

iphi

idae

;H

ymen

opte

ra3

Bow

er&

Bro

wn

(200

9)

Chi

logl

ottis

aff.

plur

ical

lata

2T

Neo

zele

bori

anr

mon

tico

la1

Tip

hiid

ae;

Hym

enop

tera

3B

ower

&B

row

n(2

009)

Chi

logl

ottis

aff.

plur

ical

lata

3T

Neo

zele

bori

aim

patien

sSm

.T

iphi

idae

;H

ymen

opte

ra3

Bow

er&

Bro

wn

(200

9)

Chi

logl

ottis

refle

xa(L

abill

.)D

ruce

TN

eoze

lebo

ria

n.sp

.30

Bro

wn

Tip

hiid

ae;

Hym

enop

tera

3B

ower

(199

6);B

ower

&B

row

n(1

997)

;Man

tetal

.(20

02,

2005

c,d)

Chi

logl

ottis

refle

xase

nsu

stri

cta

(Tas

.)T

Thy

nnin

ew

asp

Tip

hiid

ae;

Hym

enop

tera

3C

.C.B

ower

(unp

ublis

hed

data

)

Chi

logl

ottis

sem

inud

aD

.L.J

ones

TN

eoze

lebo

ria

n.sp

.29

Bro

wn

Tip

hiid

ae;

Hym

enop

tera

3B

ower

(199

2,19

96);

Bow

er&

Bro

wn

(199

7);M

ante

tal

.(2

002,

2005

c,d)

Chi

logl

ottis

sphr

ynoi

des

D.L

.Jon

esT

Neo

zele

bori

an.

sp.3

Bro

wn

Tip

hiid

ae;

Hym

enop

tera

3M

ante

tal

.(20

02,2

005c

,d)

Chi

logl

ottis

sylv

estr

isD

.L.J

ones

&M

.A.C

lem

.

TN

eoze

lebo

ria

n.sp

.50

Bro

wn

Tip

hiid

ae;

Hym

enop

tera

3M

ante

tal

.(20

02,2

005c

,d)

Chi

logl

ottis

(syn.

Myr

mec

hila

)tr

apez

ifor

mis

Fitz

g.T

Neo

zele

bori

acr

ypto

ides

Sm.,

Zas

pilo

thyn

nus

sp.‡

Tip

hiid

ae;

Hym

enop

tera

34* 58

.5(2

10)†

58.5

(210

)†O

akw

ood

(199

0)*;

Man

tetal

.(2

002)

;Sch

iest

l,(2

004)

† ;Man

tet

al.(

2005

c,d);

Bat

es(2

009a

)‡

Chi

logl

ottis

(syn.

Sym

plig

lottis

)tri

cera

tops

D.L

.Jon

es

TN

eoze

lebo

ria

cari

nico

llis

Tur

ner

Tip

hiid

ae;

Hym

enop

tera

Bow

er&

Bro

wn

(200

9)


44 A. C. Gaskett

Tab

le1.

(Con

t.)

Orc

hid

Gro

wth

form

Polli

nato

rPo

llina

tor

Fam

ily;O

rder

Polli

nato

rse

xual

beha

viou

r%

flow

ers

polli

nate

d(N

)%

plan

tspo

llina

ted

(N)

Sour

ce

Chi

logl

ottis

trilab

raFi

tzg.

TN

eoze

lebo

ria

prox

ima

(Tur

ner)

Tip

hiid

ae;

Hym

enop

tera

341

(86)

*41

(86)

*B

ower

(199

2,19

96);

Peak

all&

Han

del(

1993

)*;B

ower

&B

row

n(1

997)

;Man

tetal

.(2

002,

2005

c,d)

Chi

logl

ottis

(syn.

Myr

mec

hila

)tr

ulla

taD

.L.J

ones

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3

C.C

.Bow

er(u

npub

lishe

dda

ta)

Chi

logl

ottis

(syn.

Myr

mec

hila

)tr

unca

taD

.L.J

ones

&M

.A.C

lem

.

TN

eoze

lebo

ria

aff.

ursi

tatu

mB

row

n,N

.sp.

Spot

ted,

N.

aff.

cryp

toid

es1,

N.af

fcr

ypto

ides

2,N

.sp

.(r

ed/b

lack

),N

.sp

.(sm

allb

lack

)

Tip

hiid

ae;

Hym

enop

tera

3M

ante

tal

.(20

02,2

005c

,d)

Chi

logl

ottis

(syn.

Sim

plig

lottis

)tu

rfos

aD

.L.J

ones

TN

eoze

lebo

ria

nrm

ontico

la2

Tip

hiid

ae;

Hym

enop

tera

3B

ower

&B

row

n(2

009)

Chi

logl

ottis

(syn.

Sim

plig

lottis

)va

lida

D.L

.Jon

esT

Neo

zele

bori

am

ontico

laT

urne

r,N

.ni

tidu

la(T

urne

r),N

.cr

ypto

ides

Sm.

Tip

hiid

ae;

Hym

enop

tera

3B

ower

(199

2,19

96,2

006)

;Man

tet

al.(

2005

c,d);

Bow

er&

Bro

wn

(200

9)

Chi

logl

ottis

aff.

valida

1T

Neo

zele

bori

anr

.im

patien

s1

Tip

hiid

ae;

Hym

enop

tera

3B

ower

(200

6);B

ower

&B

row

n(2

009)

Chi

logl

ottis

aff.

valida

2T

Neo

zele

bori

anr

.im

patien

s,N

eoze

lebo

ria

nr.

mon

tico

la3

Tip

hiid

ae;

Hym

enop

tera

3B

ower

(200

6);B

ower

&B

row

n(2

009)

Cry

ptos

tylis

erec

taR

.Br.

TL

isso

pim

pla

exce

lsa

(Cos

ta)

Ichn

eum

onid

ae;

Hym

enop

tera

132

.7(2

187)

*†70

.4(4

02)*

†G

aske

tt&

Her

bers

tein

(200

6)*;

Gas

kett

etal

.(20

08)†

Cry

ptos

tylis

hunt

eria

naN

icho

llsT

Lis

sopi

mpl

aex

cels

a(C

osta

)Ic

hneu

mon

idae

;H

ymen

opte

ra1?

Nic

holls

(193

8)

Cry

ptos

tylis

lept

ochi

laB

enth

.T

Lis

sopi

mpl

aex

cels

a(C

osta

)(p

rev.

L.s

emip

unct

ata)

Ichn

eum

onid

ae;

Hym

enop

tera

15.

2(1

329)

*†41

.9(1

21)*

†G

aske

tt&

Her

bers

tein

(200

6)*;

Gas

kett

etal

.(20

08)†

Cry

ptos

tylis

ovat

aR

.Br.

TL

isso

pim

pla

exce

lsa

(Cos

ta)

Ichn

eum

onid

ae;

Hym

enop

tera

112

.0(1

22)*

35.0

(47)

*C

olem

an(1

930)

;A.C

.Gas

kett

(unp

ublis

hed

data

)*C

rypt

osty

lis

subu

lata

(Lab

ill.)

Rch

b.f.

TL

isso

pim

pla

exce

lsa

(Cos

ta)

Ichn

eum

onid

ae;

Hym

enop

tera

125

.4(9

94)*

†‡66

.6(1

54)*

†‡Sc

hies

tlet

al.(

2004

)*;G

aske

tt&

Her

bers

tein

(200

6)† ;G

aske

ttet

al.(

2008

)‡

Dra

kaea

conc

olor

Hop

per

&A

.P.B

r.T

Zas

pilo

thyn

nus

gile

siT

urne

r(a

sH

emithy

nnus

gile

si)*

,th

ynni

new

asp†

Tip

hiid

ae;

Hym

enop

tera

3B

row

net

al.(

1997

)*;H

oppe

r&

Bro

wn,

(200

7)† ;H

oppe

r(2

009)

Dra

kaea

confl

uens

Hop

per

&A

.P.B

r.T

Thy

nnin

ew

asp

Tip

hiid

ae;

Hym

enop

tera

3H

oppe

r&

Bro

wn

(200

7);

Hop

per

(200

9)



Dra

kaea

glyp

todo

nFi

tzg.

TZ

aspi

loth

ynnu

str

ilob

atus

Tur

ner*

,Z.di

lata

tus

spic

ulifer

aT

urne

r†

Tip

hiid

ae;

Hym

enop

tera

320

.7(1

203)

20.7

(120

3)St

outa

mir

e(1

974)

*;Pe

akal

l(1

990)

*;B

row

net

al.(

1997

)*† ;

Man

tetal

.(20

05c)*

Dra

kaea

grac

ilis

Hop

per

&A

.P.B

r.T

Zas

pilo

thyn

nus

nigr

ipes

Gue

rin*

(Thy

nnoi

des

bide

nsin

accu

rate

,G.

Bro

wn

pers

.com

m.),

Thy

nnoi

des

elon

gata

†

Tip

hiid

ae;

Hym

enop

tera

3B

row

net

al.(

1997

)*;B

ates

(200

9b)†

Dra

kaea

livi

daJ.

Dru

mm

.(a

sD

raka

eael

astica

Lin

dl.

inSt

outa

mir

e,19

79)

TZ

aspi

loth

ynnu

sni

grip

esG

ueri

nT

iphi

idae

;H

ymen

opte

ra3

Stou

tam

ire

(197

4,19

79);

Man

tet

al.(

2005

c);H

oppe

r&

Bro

wn

(200

7);H

oppe

r(2

009)

Dra

kaea

livi

dax

confl

uens

TZ

aspi

loth

ynnu

sni

grip

esG

ueri

n,Z

.di

lata

tus

spic

ulifer

aT

urne

r

Tip

hiid

ae;

Hym

enop

tera

3B

row

net

al.(

1997

)

Dra

kaea

mic

rant

haH

oppe

r&

A.P

.Br.

TT

hynn

ine

was

pT

iphi

idae

;H

ymen

opte

ra3

Hop

per

&B

row

n(2

007)

;H

oppe

r(2

009)

Dra

kaea

thyn

niph

ila

A.S

.Geo

rge

TZ

aspi

loth

ynnu

ssp

.T

iphi

idae

;H

ymen

opte

ra3

Man

tetal

.(20

05c);

Hop

per

&B

row

n(2

007)

;Hop

per

(200

9)L

epor

ella

fimbr

iata

(Lin

dl.)

A.S

.Geo

rge

TM

yrm

ecia

uren

sL

ower

Form

icid

ae;

Hym

enop

tera

223

.9(1

478)

Peak

all(

1989

)

Oligo

chae

toch

ilus

lepi

dus

D.L

.Jon

esT

Myc

etop

hilid

flyM

ycet

ophi

lidae

,D

ipte

raun

conf

.B

ates

(200

9a)

Par

acal

eana

hort

ioru

mH

oppe

r&

A.P

.Br.

TT

hynn

ine

was

pT

iphi

idae

,H

ymen

opte

ra3

Bat

es(2

009b

)

Par

acal

eana

(syn.

Sul

liva

nia)

nigr

ita

(J.D

rum

m.e

xL

indl

.)B

laxe

ll

TE

rion

esp

.*,L

abiu

msp

.†T

iphi

idae

,Ic

hneu

mon

idae

;H

ymen

opte

ra

3B

row

net

al.(

1997

)*† ;H

oppe

r&

Bro

wn

(200

6)*

Pte

rost

ylis

acum

inat

aR

.Br.

TC

ulex

sp.f

emal

em

osqu

ito?

Cul

icid

ae;D

ipte

raun

conf

.C

olem

an(1

934)

Pte

rost

ylis

aren

icol

aM

.A.C

lem

.&J.

Stew

art

(syn.

Oligo

chae

toch

ilus

aren

icol

us)

TM

ycet

ophi

lidfly

Myc

etop

hilid

ae,

Dip

tera

unco

nf.

Bat

es(2

009a

)

Pte

rost

ylis

aspe

raD

.L.J

ones

&M

.A.C

lem

.(sy

n.D

iplo

dium

aspe

rum

)

TFl

yD

ipte

raun

conf

.B

ates

(200

9b)

Pte

rost

ylis

(syn.

Oligo

chae

toch

ilus

)bo

orm

anii

Rup

p

TFl

yD

ipte

raun

conf

.B

ates

(200

9a)

Pte

rost

ylis

cucu

llat

asu

bsp.

sylv

icol

aD

.L.J

ones

TFl

yD

ipte

raun

conf

.B

ates

(200

9a)

Pte

rost

ylis

curt

aR

.Br.

TM

ycom

yasp

.M

ycet

ophi

lidae

;D

ipte

raun

conf

.B

ernh

ardt

(199

5)


46 A. C. Gaskett

Tab

le1.

(Con

t.)

Orc

hid

Gro

wth

form

Polli

nato

rPo

llina

tor

Fam

ily;O

rder

Polli

nato

rse

xual

beha

viou

r%

flow

ers

polli

nate

d(N

)%

plan

tspo

llina

ted

(N)

Sour

ce

Pte

rost

ylis

falc

ata

R.S

.Rog

ers

TC

ulex

sp.f

emal

em

osqu

ito?

Cul

icid

ae;D

ipte

raun

conf

.C

olem

an(1

934)

Pte

rost

ylis

gibb

osa

R.B

r.(sy

n.O

ligo

chae

toch

ilus

gibb

osus

)T

Het

erop

tern

asp

.M

ycet

ophi

lidae

;D

ipte

ra4?

12(4

90)*

25.9

(154

)*T

aylo

r(1

999)

*;N

atio

nalP

arks

&W

ildlif

eSe

rvic

e(2

002)

*P

tero

styl

isle

pida

(syn.

Oligo

chae

toch

ilus

lepi

dus)

TM

ycet

ophi

lidfly

Myc

etop

hilid

ae,

Dip

tera

unco

nf.

Bat

es(2

009a

)

Pte

rost

ylis

(syn.

Lin

guel

la)

nana

R.B

r.T

Fly

Dip

tera

unco

nf.

Bro

wn

etal

.(19

97)

Pte

rost

ylis

nuta

nsR

.Br.

TFu

ngus

gnat

Myc

etop

hilid

ae;

Dip

tera

4?H

yett

(196

0)

Pte

rost

ylis

psam

mop

hila

(D.L

.Jon

es)R

.J.B

ates

(syn.

Oligo

chae

toch

ilus

psam

mop

hilu

s)

TM

osqu

ito-li

kefly

Dip

tera

unco

nf.

Bat

es(2

009a

)

Pte

rost

ylis

pusi

lla

R.S

.Rog

ers

(syn

Oligo

chae

toch

ilus

pusi

llus

(R.S

.Rog

ers)

Szla

ch.)

TFu

ngus

gnat

Myc

etop

hilid

ae;

Dip

tera

4?B

eard

sell

&B

ernh

ardt

(198

2)

Pte

rost

ylis

(syn.

Dip

lodi

um)

roge

rsii

E.C

olem

anT

Fung

usgn

atM

ycet

ophi

lidae

;D

ipte

ra

unco

nf.

Bat

es(2

009b

)

Pte

rost

ylis

rufa

R.B

r.(sy

nO

ligo

chae

toch

ilus

rufu

s)T

Fung

usgn

at*,

fly†

Dip

tera

unco

nf.

Bea

rdse

ll&

Ber

nhar

dt(1

982)

*;B

row

net

al.(

1997

)†

Pte

rost

ylis

sang

uine

aD

.L.J

ones

&M

.A.C

lem

.(sy

n.U

roch

ilus

sang

uine

us(D

.L.J

ones

&M

.A.C

lem

.)D

.L.J

ones

&M

.A.C

lem

.)

TG

nat

Dip

tera

unco

nf.

Bro

wn

etal

.(19

97)

Pte

rost

ylis

(syn.

Ran

orch

is)

sarg

entii

C.R

.P.A

ndre

ws

TFl

yD

ipte

raun

conf

.Sa

rgen

t(19

09)

Pte

rost

ylis

(syn.

Dip

lodi

um)

scab

raL

indl

.(as

Pte

rost

ylis

cons

tric

taO

.H.S

arg.

)

TFl

yD

ipte

raun

conf

.B

row

net

al.(

1997

)

Pte

rost

ylis

(syn.

Uro

chilus

)vi

ttat

aL

indl

.T

Gna

tD

ipte

raun

conf

.Sa

rgen

t(19

09)

Spi

cula

eaci

liat

aL

indl

.T

Thy

nnot

urne

ria

sp.*

,Is

war

oide

ssp

.†T

iphi

idae

;H

ymen

opte

ra3

Bro

wn

etal

.(19

97)*

;Alc

ock

(200

0)*;

Man

tetal

.(20

05c)†



New

Zea

lan

d

Cry

ptos

tylis

subu

lata

(Lab

ill.)

Rch

b.f.

TL

isso

pim

pla

exce

lsa

(Cos

ta)

Ichn

eum

onid

ae;

Hym

enop

tera

1?G

raha

m(1

983)

Pte

rost

ylis

(syn.

Dip

lodi

um)

alob

ula

(Hat

ch)

L.B

.Moo

re

TZ

ygom

yia

sp.

Myc

etop

hilid

ae;

Dip

tera

4?2.

8(7

2)2.

8(7

2)L

ehne

bach

etal

.(20

05)

Pte

rost

ylis

aust

ralis

Hoo

k.f.

TA

neur

alo

ngip

alpi

sT

onno

ir&

Edw

ards

?*C

erot

elio

nsp

.?*,

Fung

usgn

at†

Myc

etop

hilid

ae,

Ker

atop

hilid

ae;

Dip

tera

4?L

ehne

bach

etal

.(20

05)*

;E

.Sca

nlen

(unp

ublis

hed

data

)†

Pte

rost

ylis

gram

inea

Hoo

k.f.

TFu

ngus

gnat

Myc

etop

hilid

ae;

Dip

tera

4?E

.Sca

nlen

(unp

ublis

hed

data

)

Pte

rost

ylis

pate

nsC

olen

soT

Fung

usgn

at?

4?41

.6(2

4)41

.6(2

4)L

ehne

bach

etal

.(20

05)

Pte

rost

ylis

trul

lifo

lia

Hoo

k.f.

(syn.

Dip

lodi

umtr

ullifo

lium

)

Tun

conf

.<

25%

Che

esem

an(1

872,

1875

)

Sou

thA

mer

ica

Geo

blas

tape

nnic

illa

ta(R

chb.

f.)H

oehn

eex

Cor

rea

TC

amps

omer

isbi

stri

mac

ula

(Lep

.)Sc

oliid

ae;

Hym

enop

tera

252

.2(5

7)52

.2(5

7)C

iote

ket

al.(

2006

)

Ep

iden

dre

aeC

entr

alA

mer

ica

Lep

anth

esgl

icen

stei

nii

Lue

rE

Bra

dysi

aflo

ribu

nda

Moh

rig

Scia

rida

e;D

ipte

ra1?

41(2

4)B

lanc

o&

Bar

boza

(200

5)L

epan

thes

wen

dlan

dii

Rei

chb.

f.(E

)E

?11

.6(4

232

on20

0pl

ants

)C

alvo

(199

0)

Max

illa

riea

e

Sou

than

dC

entr

alA

mer

ica

E

Mor

mol

yca

ring

ens

(Lin

dl.)

EN

anno

trig

ona

test

acei

corn

is(L

ep.),

Sca

ptot

rigo

nasp

.A

pida

e;H

ymen

opte

ra2

Sing

eret

al.(

2004

)

Ste

llilab

ium

sp.

ET

achi

nid

flyT

achi

nida

e;D

ipte

ra2

Chr

iste

nsen

(199

4);v

ande

rC

inge

l(20

01)

Tel

ipog

onsp

.E

Tac

hini

dfly

Tac

hini

dae;

Dip

tera

2C

hris

tens

en(1

994)

;van

der

Cin

gel(

2001

)T

olum

nia

(pre

v.O

ncid

ium

)he

neke

nii

(R.H

.Sch

omb.

exL

indl

.)

EC

entr

issp

.?A

ntho

phor

idae

;H

ymen

opte

raun

conf

.D

od(1

976)

Tri

choc

eros

ante

nnifer

a(p

rev.

T.pa

rvifl

ora)

(H.e

tB).

H.B

.K.

EP

arag

ymno

mm

asp

.T

achi

nida

e;D

ipte

ra2

Dod

son

(196

2);v

ande

rC

inge

l(2

001)

Tri

goni

dium

obtu

sum

Lin

dley

EP

lebe

iadr

orya

naFr

iese

Mel

ipon

inae

;H

ymen

opte

ra2

&4

Sing

er(2

002)


48 A. C. GaskettT

able

1.(C

ont.)

Orc

hid

Gro

wth

form

Polli

nato

rPo

llina

tor

Fam

ily;O

rder

Polli

nato

rse

xual

beha

viou

r%

flow

ers

polli

nate

d(N

)%

plan

tspo

llina

ted

(N)

Sour

ce

Orc

hid

eae

Eu

rop

e

Oph

rys

aega

eaK

alte

isen

&H

.R.R

einh

ard

TA

ntho

phor

aor

ient

alis

Mor

awitz

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5);P

aulu

s(2

006)

Oph

rys

aegi

rtic

aP.

Del

forg

eT

Euc

era

taur

ica

Mor

awitz

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

aesc

ulap

iiR

enz

TA

ndre

napa

ucis

quam

aN

oski

ewic

zA

ndre

nida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

afri

cana

G.F

oelsc

he&

W.F

oelsc

heT

And

rena

flavi

pes

Panz

erA

ndre

nida

e;H

ymen

opte

ra2

Stok

letal

.(20

05)

Oph

rys

alas

iatica

Kre

utz,

Sege

rs&

H.W

alra

ven

TA

ndre

nabi

mac

ulat

a(K

irby

)A

ndre

nida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

alga

rven

sis

D.T

ytec

a,B

enito

&M

.Wal

rave

nsT

Col

lete

ssp

.C

olle

tidae

;H

ymen

opte

ra2

Paul

us(2

006)

Oph

rys

anna

eD

evill

ers-

Ter

sch.

&D

evill

ers

TO

smia

rufa

(L.)

Meg

achi

lidae

;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

apifer

aH

uds.

TE

ucer

asp

.*,E

ucer

apu

nctu

lata

Alfk

en?†

Ant

hoph

orid

ae;

Hym

enop

tera

2K

ulle

nber

g&

Ber

gstr

om,

(197

6b)*

;Pau

lus

(200

0)†

Oph

rys

apifor

mis

Steu

d.T

Euc

era

barb

iven

tris

Pere

zA

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

Oph

rys

apri

lia

Dev

iller

s&

Dev

iller

s-T

ersc

h.T

Euc

era

nigr

ilab

ris

Lep

.A

ntho

phor

idae

;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

apul

ica

(O.D

anes

ch&

E.D

anes

ch)

O.D

anes

ch&

E.D

anes

ch

TE

ucer

a(p

rev.

Syn

halo

nia)

rufa

(=T

etra

loni

abe

rlan

diD

usm

et)

Ant

hoph

orid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)

Oph

rys

arac

hnitifor

mis

Gre

n.&

M.P

hilip

peT

Col

lete

scu

nicu

lari

us(L

.);A

ndre

nasa

bulo

sasu

bsp.

trim

mer

ana,

Osm

iaau

rent

ula*

(pro

babl

y=

Osm

iaau

rule

nta

Panz

er)

And

reni

dae,

Meg

achi

lidae

,C

olle

tidae

;H

ymen

opte

ra

2K

ulle

nber

g(1

961)

;Del

forg

e(2

005)

*

Oph

rys

aran

eola

Rch

b.T

Osm

iabi

colo

r(S

chra

nk)∗

inac

cura

teac

cord

ing

toPa

ulus

(200

0),A

ndre

nala

thyr

iA

lfken

† ,And

rena

com

bina

ta(C

hris

t)‡

Meg

achi

lidae

,A

ndre

nida

e;H

ymen

opte

ra

2Pa

ulus

&G

ack

(199

0)*;

Del

forg

e(2

005)

† ;Sch

iest

l&V

eree

cken

(200

8)‡

Oph

rys

arch

ipel

agi

Gol

z&

H.R

.Rei

nhar

dT

Col

lete

scu

nicu

lari

us(L

.)C

olle

tidae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Wid

mer

etal

.(20

00);

Del

forg

e(2

005)

Oph

rys

arge

ntar

iaD

evill

ers-

Ter

sch.

&D

evill

ers

TA

ndre

nafu

lvat

aSt

oeck

hert

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)



Oph

rys

argo

lica

H.F

leis

chm

.ex

Vie

rh.

TA

ntho

phor

apl

agia

ta(I

llige

r)A

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

;Pau

lus

(200

6)O

phry

sar

iadn

aeH

.F.P

aulu

s(a

sO

.cr

etic

asu

bsp.

karp

athe

nsis

E.N

elso

n*)

TM

elec

taal

bifr

ons

subs

p.al

bova

ria

Ant

hoph

orid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)*

Oph

rys

arno

ldii

P.D

elfo

rge

TA

ndre

nani

groa

enea

(Kir

by)

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

atla

ntic

aM

unby

TC

halico

dom

apa

riet

ina

(Geo

ffr.)

Meg

achi

lidae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

;Pau

lus

(200

6)O

phry

sat

tica

Boi

ss.&

Orp

h.T

Euc

era

sem

inud

aB

rulle

Ant

hoph

orid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)O

phry

sau

relia

P.D

elfo

rge,

Dev

iller

s-T

ersc

h.&

Dev

iller

s

TC

halico

dom

apa

riet

ina

(Geo

ffr.),

C.py

rena

ica

(Lep

.)

Meg

achi

lidae

;H

ymen

opte

ra2

Del

forg

e(2

005)

;Pau

lus

(200

6)

Oph

rys

avey

rone

nsis

(J.J

.Woo

d)H

.Bau

man

n&

Kun

kele

TA

ndre

naha

ttor

fiana

(Fab

rici

us)

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)

Oph

rys

aym

onin

ii(B

reis

tr.)

But

tler

TA

ndre

naco

mbi

nata

(Chr

ist)

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)O

phry

sba

lear

ica

P.D

elfo

rge

TC

halico

dom

asi

cula

(Ros

si)

Meg

achi

lidae

;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

basi

liss

aA

.Alib

ertis

&H

.R.R

einh

ard

TA

ntho

phor

ani

groc

inct

aL

ep.

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5);P

aulu

s(2

006)

Oph

rys

battan

dier

iE

.G.C

amus

(pro

.hyb

r.)

TA

ndre

nave

tula

Lep

.?A

ndre

nida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

bena

cens

is(R

eisi

gl.)

O.D

anes

ch&

E.D

anes

ch

TC

halico

dom

apa

riet

ina

(Geo

ffr.)

Meg

achi

lidae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

;Pau

lus

(200

6)

Oph

rys

bert

olon

iiM

oret

tiT

Cha

lico

dom

apa

riet

ina

(Geo

ffr.),

C.py

rena

ica

(Lep

.)

Meg

achi

lidae

;H

ymen

opte

ra2

Paul

us(2

000,

2006

);D

elfo

rge

(200

5)

Oph

rys

bert

olon

iifo

rmis

O.D

anes

ch&

E.D

anes

ch

TC

halico

dom

asi

cula

(Ros

si)*

,C

.be

nois

tiT

kalc

u†M

egac

hilid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)*;

Del

forg

e(2

005)

†

Oph

rys

bian

cae

Mac

ch.

TE

ucer

aeu

roa

Tka

lcu

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

bilu

nula

taR

isso

TA

ndre

nafla

vipe

sPa

nzer

And

reni

dae;

Hym

enop

tera

2Sc

hies

tl&

Aya

sse

(200

2);

Del

forg

e(2

005)

;Sto

klet

al.

(200

5)O

phry

sbi

scut

ella

O.D

anes

ch&

E.D

anes

chT

Ant

hoph

ora

retu

sa(L

.)A

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)


50 A. C. GaskettT

able

1.(C

ont.)

Orc

hid

Gro

wth

form

Polli

nato

rPo

llina

tor

Fam

ily;O

rder

Polli

nato

rse

xual

beha

viou

r%

flow

ers

polli

nate

d(N

)%

plan

tspo

llina

ted

(N)

Sour

ce

Oph

rys

blitop

erth

aPa

ulus

&G

ack

TB

lito

pert

haline

olat

a(F

isch

ervo

nW

aldh

eim

)Sc

arab

aeid

ae;

Col

eopt

era

2Pa

ulus

(200

1);D

elfo

rge

(200

5)

Oph

rys

bom

byliflo

raL

ink

TE

ucer

aor

anie

nsis

Lep

.† ,E

.al

gira

Bru

lle† ,

Euc

era

sp.∗

Ant

hoph

orid

ae;

Hym

enop

tera

221

.3(1

22on

37pl

ants

)*K

ulle

nber

g&

Ber

gstr

om(1

976a

,b)

;Pau

lus

&G

ack

(199

0)† ;

Nei

land

&W

ilcoc

k(1

998)

*;Pa

ulus

(200

0)†

Oph

rys

born

mue

ller

iM

.Sch

ulze

TE

ucer

apa

ulus

iT

kalc

u*,

E.pe

nici

llat

aR

isch

†A

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

*;D

elfo

rge

(200

5)†

Oph

rys

buce

phal

aG

olz

&H

.R.R

einh

ard

TE

ucer

acu

rvitar

sis

Moc

z.A

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

Oph

rys

calo

caer

ina

Dev

iller

s-T

ersc

h.&

Dev

iller

s

TA

ndre

nala

bial

is(K

irby

)?A

ndre

nida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

caly

psus

M.H

irth

&H

.Spa

ethe

TE

ucer

ada

lmat

ica

Lep

.A

ntho

phor

idae

;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

cand

ica

Gre

uter

,M

atth

as&

Ris

seT

Euc

era

hisp

ana

Lep

.*,

E.hi

span

aL

ep.†

Ant

hoph

orid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)

Oph

rys

celien

sis

(O.D

anes

ch&

E.D

anes

ch)

P.D

elfo

rge

TE

ucer

agr

aeca

Rad

oszk

owsk

iA

ntho

phor

idae

;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

cera

stes

Dev

iller

s&

Dev

iller

s-T

ersc

h.(a

sO

phry

sco

rnut

a(sm

all)?

*)

TE

ucer

apu

nctico

llis

Mor

.?A

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

Oph

rys

ceto

P.D

evill

ers,

Dev

iller

s-T

ersc

h.&

P.D

elfo

rge

TE

ucer

aeu

roa

Tka

lcu?

,E

.pl

umig

era?

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

ches

term

anii

(J.J

.W

ood)

Gol

z&

H.R

.Rei

nhar

d

TB

ombu

sve

stal

is(G

eoffr

.)A

pida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

;Gog

ler

etal

.(2

009)

Oph

rys

cile

ntan

aD

evill

ers-

Ter

sch.

&D

evill

ers

TA

ndre

naflo

rent

ina

Mag

rett

iA

ndre

nida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

cilici

caSc

hltr

.T

Arg

ogor

ytes

sp.

Sphe

cida

e;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Pau

lus

(200

6)O

phry

sci

nere

ophi

laPa

ulus

&G

ack

TA

ndre

naci

nere

ophi

laW

ar.

Ant

hoph

orid

ae;

Hym

enop

tera

2Pa

ulus

(200

1,20

09);

Del

forg

e(2

005)

Oph

rys

corn

utul

aPa

ulus

TE

ucer

apu

nctu

lata

Alfk

en,

E.si

gnifer

aA

ntho

phor

idae

;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

crab

roni

fera

Seba

st.

&M

auri

TA

ntho

phor

apl

umip

es(P

alla

s)A

ntho

phor

idae

;H

ymen

opte

ra2

Del

forg

e(2

005)

;Pau

lus

(200

6)

Oph

rys

creb

erri

ma

Paul

us(a

sO

phry

sfu

sca

(smal

l)?*)

TA

ndre

nacr

eber

rim

aPe

rez*

† ,A

.fla

vipe

sPa

nzer

*A

ndre

nida

e;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

*;D

elfo

rge

(200

5)†



Oph

rys

cres

saPa

ulus

TA

ndre

nam

erul

aW

ar.?

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

cret

ensi

s(B

aum

ann

&K

unke

le)P

aulu

sT

And

rena

vach

ali

subs

p.cr

etic

ola

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)O

phry

scr

etic

a(V

ierh

.)E

.Nel

son

TM

elec

tatu

berc

ulat

aL

iefti

nck

Ant

hoph

orid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);P

aulu

s(2

001)

;Del

forg

e(2

005)

Oph

rys

delp

hine

nsis

O.D

anes

ch&

E.D

anes

ch(p

rohy

br.)

TA

ntho

phor

apl

agia

ta(I

llige

r)A

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

Oph

rys

disc

ors

Bia

nca

(syn.

O.to

dari

s)T

Euc

era

euro

aT

kalc

uA

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

Oph

rys

drum

ana

P.D

elfo

rge

TC

halico

dom

aal

bono

tata

(Rad

oszk

owsk

i)M

egac

hilid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

dyri

sM

aire

TA

ntho

phor

aat

roal

baL

ep.

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5);P

aulu

s(2

006)

Oph

rys

elat

ior

Gum

pr.e

x.Pa

ulus

TT

etra

loni

asa

lica

riae

(Lep

.)A

pida

e;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Pau

lus

(200

0);D

elfo

rge

(200

5)O

phry

sel

egan

s(R

enz)

H.B

aum

ann

&K

unke

leT

Ant

hoph

ora

ersc

how

iFe

dtsc

henk

oA

ntho

phor

idae

;H

ymen

opte

ra2

Del

forg

e(2

005)

;Pau

lus

(200

6)

Oph

rys

eleo

nora

eD

evill

ers-

Ter

sch.

&D

evill

ers

TA

ndre

nam

orio

Bru

lleA

ndre

nida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

epis

copa

lis

Poir

(as

O.ep

isco

palis

(max

ima)∗)

TE

ucer

a(p

rev.

Syn

halo

nia)

rufa

(=T

etra

loni

abe

rlan

diD

usm

et)*

,ina

ccur

ate

acco

rdin

gto

(Del

forg

e,20

05)

Api

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)*

Oph

rys

exal

tata

Ten

.T

Col

lete

scu

nicu

lari

us(L

.)C

olle

tidae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

;Man

tetal

.(20

05b)

Oph

rys

expl

anat

a(L

ojac

.)P.

Del

forg

eT

Cha

lico

dom

asi

cula

(Ros

si)

Meg

achi

lidae

;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

fabr

ella

Paul

us&

Aya

sse

exP.

Del

forg

eT

And

rena

fabr

ella

Pere

zA

ndre

nida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

ferr

um-e

quin

umD

esf.

TC

halico

dom

apa

riet

ina

(Geo

ffr.)

Meg

achi

lidae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Pau

lus

(200

1,20

09);

Del

forg

e(2

005)

Oph

rys

flavi

cans

Vis

.T

Cha

lico

dom

am

anic

ata

(Gir

aud)

Meg

achi

lidae

;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

flavo

mar

gina

ta(R

enz)

H.B

aum

ann

&K

unke

le

TE

ucer

adi

mid

iata

Bru

lleA

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

Oph

rys

fleis

chm

anni

iH

ayek

TA

ntho

phor

asi

chel

iR

ados

zkow

ski

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5);P

aulu

s(2

006)


52 A. C. Gaskett

Tab

le1.

(Con

t.)

Orc

hid

Gro

wth

form

Polli

nato

rPo

llina

tor

Fam

ily;O

rder

Polli

nato

rse

xual

beha

viou

r%

flow

ers

polli

nate

d(N

)%

plan

tspo

llina

ted

(N)

Sour

ce

Oph

rys

fuci

flora

(F.W

.Sch

mid

t)M

oenc

hT

Euc

era

nigr

esce

nsPe

rez*

,E.

long

icor

nis

(L.)*

,Mic

rodo

nla

tifr

ons

Loe

w*,

M.

mut

abilis

(L.)*

,P

hyllop

erth

aho

rtic

ola

(L.)†

Ant

hoph

orid

ae;

Hym

enop

tera

Scar

abae

idae

;C

oleo

pter

a

25.

45(4

63pl

ants

)‡K

ulle

nber

g&

Ber

gstr

om(1

976a

,b)

;Del

forg

e(2

005)

*;T

ytec

aet

al.(

2006

)† ;Van

derw

oest

ijne

etal

.(20

09)‡

Oph

rys

fusc

aL

ink

TA

ndre

nani

groa

enea

(Kir

by),

Col

lete

scu

nicu

lari

us(L

.)A

ndre

nida

e,C

olle

tidae

;H

ymen

opte

ra

2Pa

ulus

&G

ack

(199

0);S

chie

stl&

Aya

sse

(200

2);D

elfo

rge

(200

5);S

tokl

etal

.(20

05)

Oph

rys

fusc

a(ty

peII

Sici

ly)

TA

ndre

nath

orac

ica

Fabr

iciu

s,A

.flo

rent

ina

Mag

rett

iA

ndre

nida

e;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

Oph

rys

fusc

a(ty

peII

ISi

cily

)T

And

rena

sabu

losa

subs

p.tr

imer

ana

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)

Oph

rys

cf.f

usca

(Oph

rys

sulc

ata

Dev

iller

s&

Dev

iller

s-T

ersc

h.)

TA

ndre

naw

ilke

lla

(Kir

byi)

And

reni

dae;

Hym

enop

tera

2Pa

ulus

(200

0)

Oph

rys

gack

iae

P.D

elfo

rge

TA

ndre

naflo

rent

ina

Mag

rett

i?A

ndre

nida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

garg

anic

aE

.Nel

son

exO

.Dan

esch

&E

.Dan

esch

TA

ndre

naca

rbon

aria

(L.)

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)

Oph

rys

gaze

lla

Dev

iller

s-T

ersc

h.&

Dev

iller

s

TA

ndre

nafla

vipe

sPa

nzer

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

gottfr

iedi

ana

Ren

zT

Cha

lico

dom

asp

.M

egac

hilid

ae;

Hym

enop

tera

2Pa

ulus

(200

6)

Oph

rys

grac

ilis

(Bue

l&D

anes

ch)P

.Eng

lmai

erT

Euc

era

clyp

eata

Eri

chso

n?A

ntho

phor

idae

;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

gram

mic

a(B

.Will

ing

&E

.Will

ing)

Dev

iller

s-T

ersc

h.&

Dev

iller

s(a

sO

.he

rae*

,ac

cord

ing

toPa

ulus

(200

6)

TA

ndre

nani

groa

ena

(Kir

by)

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)*;

Stok

letal

.(2

005)

*

Oph

rys

gran

diflo

raT

en.

TE

ucer

aal

gira

Bru

lle?

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

grig

oria

naG

.Kre

tzsc

hmar

&H

.Kre

tzsc

hmar

TX

yloc

opa

viol

acea

(L.)

Ant

hoph

orid

ae;

Hym

enop

tera

2Pa

ulus

(200

6)

Oph

rys

hebe

s(K

alop

issi

s)E

.Will

ing

&B

.Will

ing

TA

ndre

nasy

mph

iti

Schm

iede

knec

htA

ndre

nida

e;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)



Oph

rys

held

reic

hii

Schl

tr.

TE

ucer

a(p

rev.

Syn

halo

nia)

rufa

(=T

etra

loni

abe

rlan

diD

usm

et)∗†

,Tet

ralo

nia

alte

rnan

s(B

rulle

)†

Api

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)† ;D

elfo

rge

(200

5)*;

Spae

the

etal

.(20

07)*

;St

rein

zer

etal

.(20

09)*

Oph

rys

hele

nae

Ren

zT

Euc

era

long

icor

nis

(L.)?

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

helios

Kre

utz

TE

ucer

a(S

ynha

loni

a)cr

essa

?A

ntho

phor

idae

;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

hera

eM

.Hir

th&

H.S

paet

hT

And

rena

thor

acic

a(F

abri

cius

)A

ndre

nida

e;H

ymen

opte

ra2

Paul

us(2

006)

Oph

rys

hete

roch

ila

(Ren

z&

Tau

benh

eim

)P.

Del

forg

e

TE

ucer

acy

pria

Alfk

enA

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Pau

lus

(200

1);D

elfo

rge

(200

5)

Oph

rys

holo

seri

ca(N

.L.B

urm

.)E

ucer

a&

Tet

ralo

nia

sp.*

,E

ucer

acl

ypea

taE

rich

son† ,E

.lo

ngic

orni

s(L

.)† ,and

rare

lyP

hyllop

erth

aho

rtic

ola

(L.)‡

&M

icro

don

sp.‡

Ant

hoph

orid

ae;

Hym

enop

tera

,Sc

arab

aeid

ae;

Col

eopt

era

Syrp

hida

e;D

ipte

ra

Paul

us&

Gac

k(1

990)

*;Pa

ulus

(200

0† ,200

6‡ )

Oph

rys

incu

bace

aB

ianc

aex

.T

od.

TA

ndre

nam

orio

Bru

lleA

ndre

nida

e;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Pau

lus

(200

0);D

elfo

rge

(200

5);C

ortis

etal

.(20

09)

Oph

rys

inse

ctifer

aL

.T

Arg

ogor

ytes

farg

eii

(Shu

ckar

d),A

.m

ysta

ceus

(L.),

Ant

hobi

umm

inut

umF.

(Sta

phyl

inid

ae)†

Sphe

cida

e;H

ymen

opte

ra,

Stap

hylin

idae

;C

oleo

pter

a

215

.1(2

775

plan

ts)*

Dar

win

(188

5)*;

Wol

ff(1

950)

*;K

ulle

nber

g(1

961)

;Kul

lenb

erg

&B

ergs

trom

(197

6a,b

)† ;A

gren

&B

org-

Kar

lson

(198

4);

Del

forg

e(2

005)

;V

ande

rwoe

stijn

eet

al.(

2009

)*O

phry

sin

tegr

a(M

oggr

.&R

chb.

f.)Pa

ulus

&G

ack

TC

olle

tes

cuni

cula

rius

(L.)

Col

letid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)

Oph

rys

iric

olor

Des

f.T

And

rena

mor

ioB

rulle

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);P

aulu

s(2

001)

;Del

forg

e(2

005)

;Sto

klet

al.(

2007

);C

ortis

etal

.(20

09)

Oph

rys

isra

elitic

aH

.Bau

man

n&

Kun

kele

TA

ndre

nafla

vipe

sPa

nzer

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);S

tokl

etal

.(2

005)

Oph

rys

kots

chyi

H.F

leis

chm

.&

Soo

TM

elec

tatu

berc

ulat

aL

iefti

nck

Ant

hoph

orid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)O

phry

sla

caitae

Loj

ac.

TE

ucer

aeu

cnem

idea

Dou

rsA

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

Oph

rys

laur

ensi

sG

enie

z&

Mel

kiT

And

rena

schu

lzi

Stra

ndA

ndre

nida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

lesb

isG

olz

&H

.R.R

einh

ard

TA

ndre

nacu

rios

a(M

oraw

itz)

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)


54 A. C. GaskettT

able

1.(C

ont.)

Orc

hid

Gro

wth

form

Polli

nato

rPo

llina

tor

Fam

ily;O

rder

Polli

nato

rse

xual

beha

viou

r%

flow

ers

polli

nate

d(N

)%

plan

tspo

llina

ted

(N)

Sour

ce

Oph

rys

leuc

adic

aR

enz

(pro

hybr

.)T

And

rena

flavi

pes

Panz

er*† ,A

.cr

eber

rim

aPe

rez† ?

And

reni

dae;

Hym

enop

tera

2Pa

ulus

(200

1)*;

Del

forg

e(2

005)

†

Oph

rys

loja

cono

iP.

Del

forg

eT

And

rena

ocre

ata

(Chr

ist)?

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

luca

naP.

Del

forg

e,D

evill

ers-

Ter

sch.

&D

evill

ers

TA

ndre

nala

bial

is(K

irby

)A

ndre

nida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

luce

ntin

aP.

Del

forg

eT

And

rena

vulp

ecul

aK

riec

hbau

mer

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

luci

s(K

alte

isen

&H

.R.R

einh

ard)

Paul

us&

Gac

k

TA

ntho

phor

acf

.m

ucid

aA

ntho

phor

idae

;H

ymen

opte

ra2

Del

forg

e(2

005)

;Pau

lus

(200

6)

Oph

rys

lunu

lata

Parl

.T

Osm

iako

hlii

Duc

keM

egac

hilid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)O

phry

slu

perc

alis

Dev

iller

s-T

ersc

h.&

Dev

iller

s

TA

ndre

nani

groa

enea

(Kir

by)

Col

letid

ae,

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

lute

aC

av.

TA

ndre

naci

nere

aB

rulle

† ,A

.se

neci

onis

Pere

z† ,A

.cl

ypel

laSt

rand

,A.

hasi

tata

,A

.ni

groo

liva

cea

Dou

rs† ?,

S.pa

nurg

imor

pha

Mav

rom

oust

akis

∗ ,A

.hu

milis

Imho

ff∗,

A.hu

milis

subs

p.pr

unel

la*,A

.cin

erop

hila

War

.∗

And

reni

dae;

Hym

enop

tera

2K

ulle

nber

g&

Ber

gstr

om(1

976a

,b)

;Bor

g-K

arlso

n&

Ten

go(1

986)

;Pau

lus&

Gac

k(1

990)

*;B

ourn

eria

s&

Prat

(200

5);

Del

forg

e(2

005)

†

Oph

rys

lute

asu

bsp.

mel

ena

Ren

z)T

And

rena

tran

sito

ria

Mor

awitz

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)O

phry

sly

cien

sis

Paul

us,

Gug

el,D

.Ruc

kbr.

&U

.Ruc

kbr.

TE

ucer

agr

aeca

Rad

oszk

owsk

iA

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us,G

ugel

,Ruc

kbro

dt&

Ruc

kbro

dt(2

001)

;Del

forg

e(2

005)

Oph

rys

mam

mos

aD

esf.

TA

ndre

nafu

scos

aE

rich

son

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)O

phry

sm

arm

orat

aG

.Foe

lsche

&W

.Foe

lsche

TA

ndre

naw

ilke

lla

(Kir

by)

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

mas

silien

sis

Vig

lione

&V

ela

TA

ndre

nabi

colo

rFa

bric

ius

And

reni

dae;

Hym

enop

tera

2V

eree

cken

&Pa

tiny

(200

6)

Oph

rys

mel

iten

sis

(Sal

k.)

Dev

iller

s-T

ersc

h.&

Dev

iller

s

TC

halico

dom

asi

cula

(Ros

si)

Meg

achi

lidae

;H

ymen

opte

ra2

Del

forg

e(2

005)



Oph

rys

mon

tis-

leon

isO

.Dan

esch

&E

.Dan

esch

(pro

hybr

.)

TC

olle

tes

cuni

cula

rius

(L.)

Col

letid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

mor

ioPa

ulus

&K

reut

zT

And

rena

mor

ioB

rulle

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

mor

isii

(Mar

telli

)G

.Kel

ler

&So

oT

Ant

hoph

ora

sich

eli

Rad

oszk

owsk

iA

ntho

phor

idae

;H

ymen

opte

ra2

Del

forg

e(2

005)

;Pau

lus

(200

6)

Oph

rys

mur

beck

iiH

.Fle

isch

m.

TC

olle

tes

sp.

Col

letid

ae;

Hym

enop

tera

2Pa

ulus

(200

6)

Oph

rys

negl

ecta

Parl

.T

Euc

era

clyp

eata

Eri

chso

n,E

.or

anie

nsis

Lep

.?A

ntho

phor

idae

;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

norm

anii

J.J.

Woo

d(p

rohy

br.)

TB

ombu

sve

stal

is(G

eoffr

.)A

pida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

;Gog

ler

etal

.(2

009)

Oph

rys

obae

saL

ojac

.T

And

rena

flavi

pes

Panz

erA

ndre

nida

e;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

Oph

rys

omeg

aife

raH

.Fle

isch

m.(

asO

.om

egifer

asu

bsp.

omeg

aife

rain

Paul

us&

Gac

k19

90)

TA

ntho

phor

aat

roal

basu

bsp.

agam

oide

s,A

.ni

gric

eps

Mor

.

Ant

hoph

orid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)

Oph

rys

omeg

aife

rasu

bsp.

dyri

s(M

aire

)Del

Pret

eT

Ant

hoph

ora

atro

alba

subs

p.at

roal

baA

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Pau

lus

(200

6)O

phry

sor

tuab

isM

.P.G

rass

o&

Man

caT

And

rena

hypo

polia

Smie

dekn

echt

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

oxyr

rhyn

chos

Tod

.T

Euc

era

grae

caR

ados

zkow

ski

Ant

hoph

orid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)

Oph

rys

pallid

aR

af.

TA

ndre

naor

bita

lis

Mor

awitz

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)O

phry

spa

natten

sis

Scru

gli,

Pess

ei&

Cog

oni(

pro

hybr

.)

TO

smia

rufa

subs

p.ru

faM

egac

hilid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5);P

aulu

s(2

006)

Oph

rys

pano

rmitan

a(T

od.)

Soo

TA

ndre

nath

orac

ica

(Fab

rici

us)*

† ,A.flo

rent

ina

Mag

rett

i*,A

.sa

bulo

sa(S

copo

li)† ,A

.sa

bulo

sasu

bsp.

trim

eran

a*

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)*;

Del

forg

e(2

005)

†

Oph

rys

pano

rmitan

ava

r.pr

aeco

x(C

orri

as)

P.D

elfo

rge

TA

ndre

nath

orac

ica

(Fab

rici

us),

A.ni

groa

enea

(Kir

by)?

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

parv

imac

ulat

a(O

.Dan

esch

&E

.Dan

esch

)Pau

lus

&G

ack

TE

ucer

ani

gres

cens

Pere

zA

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)


56 A. C. GaskettT

able

1.(C

ont.)

Orc

hid

Gro

wth

form

Polli

nato

rPo

llina

tor

Fam

ily;O

rder

Polli

nato

rse

xual

beha

viou

r%

flow

ers

polli

nate

d(N

)%

plan

tspo

llina

ted

(N)

Sour

ce

Oph

rys

parv

ula

Paul

usT

And

rena

tom

ora

War

.A

ndre

nida

e;H

ymen

opte

ra2

Paul

us(2

001)

:Del

forg

e(2

005)

Oph

rys

pass

ioni

sSe

nnen

TA

ndre

naca

rbon

aria

(L.)

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

pass

ioni

sva

r.ga

rgan

ica

(E.N

elso

nex

.O

.Dan

esch

&E

.D

anes

ch)P

.Del

forg

e

TA

ndre

naca

rbon

aria

(L.)

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

phry

gana

eD

evill

ers-

Ter

sch.

&D

evill

ers

TA

ndre

napa

nurg

imor

pha

Mav

rom

oust

akis

,A

.hu

milis

Imho

ff,A

.ta

dauc

hii

Gus

enle

itner

,A.cl

ypel

lasu

bsp.

hasi

ata?

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

pict

aL

ink

TE

ucer

aba

rbiv

entr

isPe

rez

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

prom

onto

rii

O.D

anes

ch&

E.D

anes

ch

TO

smia

mus

telina

Ger

stae

cker

Meg

achi

lidae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

Oph

rys

prov

inci

alis

(Bau

man

n&

Kun

kele

)Pa

ulus

TA

ntho

phor

aat

rice

psPe

rez

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5);P

aulu

s(2

006)

Oph

rys

rein

hold

iiSp

rune

rex

.Boi

ss.

TM

elec

tasp

.*,A

ntho

phor

aob

scur

a† ,Eup

avlo

vski

aob

scur

aFr

iese

‡ ,E.

fune

rari

aSm

.?‡

Ant

hoph

orid

ae;

Hym

enop

tera

2K

ulle

nber

g&

Ber

gstr

om,(

1976

a,b)

*;Pa

ulus

&G

ack

(199

0)† ;

Paul

us(2

001)

‡ ;Del

forg

e(2

005)

‡

Oph

rys

sabu

losa

Paul

us&

Gac

kex

P.D

elfo

rge

TA

ndre

nasa

bulo

sa(S

copo

li)A

ndre

nida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

sara

toi

E.G

.Cam

us(p

rohy

br.)

TC

halico

dom

aal

bono

tata

(Rad

oszk

oski

)M

egac

hilid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

scol

opax

Cav

.T

Euc

era

long

icor

nis

(L.)*

,E

ucer

ani

gres

cens

Pere

z*,

E.in

terr

upta

Bae

r*,

E.

(Het

ereu

cera

)elo

ngat

ula

Vac

hal†

Ant

hoph

orid

ae;

Hym

enop

tera

2K

ulle

nber

g&

Ber

gstr

om(1

976a

,b)

*;Pa

ulus

&G

ack

(199

0)*;

Del

forg

e(2

005)

*;V

eree

cken

etal

.(20

07)†

Oph

rys

sero

tina

H.R

olli

exH

.F.P

aulu

sT

Euc

era

clyp

eata

Eri

chso

nA

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us(2

000)

Oph

rys

sicu

laT

ineo

(as

O.

sicu

la(m

inor

)*)

TA

ndre

nahe

sper

iaSm

.*†‡

,A

.vu

lpec

ula

Kri

echb

aum

er*‡ ,

A.m

erul

aW

ar.‡ ,

A.ta

raxa

ciG

irau

d‡ ,A

.bi

colo

rFa

bric

ius‡ ?

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)*;

Paul

us(2

001)

† ;Del

forg

e(2

005)

‡



Oph

rys

sipo

nten

sis

R.L

oren

z&

Gem

bard

tT

Xyl

ocop

air

is(C

hris

t)A

ntho

phor

idae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Wid

mer

etal

.(20

00)

Oph

rys

sitiac

aPa

ulus

,C

.Alib

ertis

&A

.Alib

ertis

TA

ndre

nani

groa

enea

(Kir

by)

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5);S

tokl

etal

.(20

05)

Oph

rys

spec

ulum

Lin

kT

Das

ysco

lia

ciliat

a(F

abri

cius

)(a

sC

amps

osco

lia

ciliat

a)Sc

oliid

ae;

Hym

enop

tera

2K

ulle

nber

g&

Ber

gstr

om(1

976a

,b)

;Aya

sse

etal

.(20

03)

Oph

rys

spec

ulum

subs

p.or

ient

alis

(Pau

lus)

Paul

us&

Salk

owsk

i

TD

asys

colia

ciliat

asu

bsp.

arar

aten

sis

Scol

iidae

;H

ymen

opte

ra2

Paul

us(2

009)

Oph

rys

sphe

gife

raW

illd.

TE

ucer

ano

tata

Lep

.A

ntho

phor

idae

;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

sphe

gode

sM

ill.

TA

ndre

nani

groa

enea

(Kir

by)*

† ,A.ba

rbilab

ris

(Kir

by)*

,A.th

orac

ica

(Fab

rici

us)*

,A.ci

nera

ria

(L.)*

,A.lim

ata

Eve

rsm

ann*

And

reni

dae;

Hym

enop

tera

20.

03(3

000)

‡

12.9

(963

)*17

.04

(235

plan

ts)†

Del

pino

(inD

arw

in(1

885)

asO

.ar

anifer

aH

uds.

)‡ ;Pau

lus

&G

ack

(199

0);A

yass

eet

al.

(199

7)*;

Nei

land

&W

ilcoc

k(1

998)

*;B

ourn

eria

s&

Prat

(200

5);D

elfo

rge

(200

5);

Van

derw

oest

jine

etal

.(20

09)†

Oph

rys

sple

ndid

aG

olz

&H

.R.R

einh

ard

TA

ndre

nasq

ualida

Oliv

ier

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)O

phry

ssp

rune

riN

yman

TX

yloc

opa

iris

(Chr

ist)

Ant

hoph

orid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0);D

elfo

rge

(200

5)O

phry

ssu

bins

ectife

raC

.E.H

erm

os.&

J.Sa

band

o

TSte

rict

ipho

rafu

rcat

a(V

iller

s)A

rgid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5);T

ytec

aet

al.

(200

6)

Oph

rys

sulc

ata

Dev

iller

s-T

ersc

h.&

Dev

iller

s

TA

ndre

nafla

vipe

sPa

nzer

,A

.ov

ulat

a(K

irby

),A

.w

ilke

lla

(Kir

by)

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

tard

ans

O.D

anes

ch&

E.D

anes

ch(p

rohy

br.)

TE

ucer

ata

uric

aM

oraw

itz?

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

tare

ntin

aG

olz

&H

.R.R

einh

ard

TO

smia

tric

orni

sL

atre

ille

Meg

achi

lidae

;H

ymen

opte

ra2

Paul

us&

Gac

k(1

990)

;Del

forg

e(2

005)

Oph

rys

tarq

uini

aP.

Del

forg

eT

And

rena

tibi

alis

(Kir

by)

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

tent

hred

inifer

aW

illd.

TE

ucer

ani

grilab

ris

Lep

.E

.di

mid

iata

Bru

lle,

E.cl

ypea

taE

rich

son,

E.al

gira

Bru

lle?

Ant

hoph

orid

ae;

Hym

enop

tera

255

.5(2

0on

13pl

ants

)*Pa

ulus

&G

ack

(199

0);N

eila

nd&

Wilc

ock

(199

8)*;

Paul

us(2

000)

† ;Bou

rner

ias

&Pr

at(2

005)

;Del

forg

e(2

005)


58 A. C. Gaskett

Tab

le1.

(Con

t.)

Orc

hid

Gro

wth

form

Polli

nato

rPo

llina

tor

Fam

ily;O

rder

Polli

nato

rse

xual

beha

viou

r%

flow

ers

polli

nate

d(N

)%

plan

tspo

llina

ted

(N)

Sour

ce

Oph

rys

tetr

alon

iae

W.P

.Tes

chne

rT

Tet

ralo

niel

lafu

lves

cens

(Gir

aud)

(pre

v.T

etra

loni

af.)*

,E

ucer

afu

lves

cens

Gir

aud† ,E

ucer

ain

ulae

† ,but

repo

rtso

fT

etra

loni

aru

ficor

nis

(Fab

rici

us)∗

are

inac

cura

te‡ .

Api

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)*;

Paul

us(2

000)

‡ ;Del

forg

e(2

005)

†

Oph

rys

thri

ptie

nsis

Paul

usT

And

rena

bico

lor

Fabr

iciu

s?A

ndre

nida

e;H

ymen

opte

ra2

Del

forg

e(2

005)

Oph

rys

tom

mas

inii

Vis

iani

TA

ndre

napa

ndel

lei

Pere

zA

ndre

nida

e;H

ymen

opte

ra2

Paul

us(2

000)

Oph

rys

tran

shyr

cana

Cze

rnia

k.T

And

rena

mor

ioB

rulle

*,

A.fu

scos

aE

rich

son† ?

And

reni

dae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)*;

Del

forg

e(2

005)

†

Oph

rys

umbi

lica

taD

esf.

TE

ucer

aga

ulle

iV

acha

l,E

.ga

lila

eaT

kalc

u,E

.sp

atul

ata

Gri

bodo

,E

.se

min

uda

Bru

lle,

Euc

era

peni

cillat

aR

isch

‡

Ant

hoph

orid

ae;

Hym

enop

tera

2Pa

ulus

&G

ack

(199

0)*;

Del

forg

e(2

005)

† ;Pau

lus

(200

9)‡

Oph

rys

untc

hjii

(M.S

chul

ze)

P.D

elfo

rge

TE

ucer

acl

ypea

taE

rich

son

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

urte

aeH

.F.P

aulu

sT

Blito

pert

hani

grip

enni

sR

eitt

erSc

arab

aeid

ae;

Col

eopt

era

2Pa

ulus

(200

9)

Oph

rys

vern

ixia

Bro

t.T

Das

ysco

lia

ciliat

a(F

abri

cius

)(a

sC

amps

osco

lia

ciliat

a)Sc

oliid

ae;

Hym

enop

tera

27.

6(4

75on

105

plan

ts)*

Paul

us&

Gac

k(1

990)

;Nei

land

&W

ilcoc

k(1

998)

*O

phry

svi

llos

aD

esf.

(var

ious

form

s)T

Euc

era

dim

idia

taB

rulle

,E

.bi

dent

ata

Pere

z,E

.ni

grilab

ris

Lep

.E

.ru

fitar

sis

Frie

se,

E.cu

rvitar

sis

Moc

sary

?

Ant

hoph

orid

ae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Oph

rys

zona

taD

evill

ers-

Ter

sch.

&D

evill

ers

TA

ndre

nafla

vipe

sPa

nzer

And

reni

dae;

Hym

enop

tera

2D

elfo

rge

(200

5)

Orc

his

galila

ea(B

ornm

ulle

ret

Schu

ltze)

Schl

echt

erT

Las

siog

loss

umm

argi

natu

mB

rulle

(pre

v.H

alic

tus

(Evy

laeu

s)m

argi

natu

s)

Hal

ictid

ae;

Hym

enop

tera

227

.5(2

146

on12

9pl

ants

)*B

ino

etal

.(19

82)*

;Del

forg

e(2

005)



Fig. 1. Sexually deceptive tongue orchids, Cryptostylis species,are remarkably morphologically disparate, yet share a singlepollinator, males of the parasitoid wasp Lissopimpla excelsa(Ichneumonidae). (A) Cryptostylis subulata, (B) C. leptochila, (C) C.erecta, and (D) C. hunteriana labelled to show the large labellumand reduced petals and sepals typical of this genus. C. erectaimage by Julia Cooke.

species may also pollinate more than one sexually deceptiveorchid species in different regions (see Table 1 for repeatedpollinator species). Avoidance of cross-pollination (pre-pollination or pre-zygotic isolation) is generally achievedvia differences in scent compounds or odour blends (e.g.Mant et al., 2002; Schiestl & Ayasse, 2002). Less commonly,hybridisation is prevented by differences in pollinator flightand flowering times, floral height, or the location of polliniaattachment on the pollinating insect (Schiestl & Peakall, 2005;Paulus, 2006; Bower & Brown, 2009). Sympatric species ofsexually deceptive orchids rarely share a pollinator and corre-spondingly, post-pollination or post-zygotic isolation factorsare weak or uncommon (Scopece et al., 2007; Cozzolino &Scopece, 2008). However, post-pollination isolation factorshave been suggested for two pairs of sympatric Ophrys speciesfrom Sardinia: Ophrys chestermanii and O. normanii are geneti-cally distinct, but similarly scented and share their pollinator,male Bombus vestalis (Gogler et al., 2009), and Ophrys iricolor

and O. incubacea are natural hybrids that are also similarlyscented and share their pollinator, male Andrena morio (Cortis

Fig. 2. In many Australian orchid species, the labellum isattached by a flexible hinge. When a pollinator grips thelabellum, he is flung into the stigma and pollinia. Examples oforchids with hinged labellae are (A) Paracaleana nigrita (B) Drakaeaglyptodon, (C) Caleana major, and (D) Caladenia cairnsiana. InPterostylis species, the petals are folded into a hood and asensitive labellum can act as a trap door and detain pollinatorsbriefly within the hood. (E) Pterostylis (syn. Diplodium) grandiflorum.Most photographs by Julia Cooke.

et al., 2009). Post-pollination isolation is also confirmed forfour Australian sexually deceptive Cryptostylis species thatare often sympatric and share their single pollinator (maleLissopimpla excelsa; Ichneumonidae), but do not hybridise innature or when cross-pollinated by hand (Dacy, 1974; Jones,1988; Backhouse & Jeanes, 1995). Cryptostylis species differ inchromosome numbers, a common mechanism of incompat-ibility in food-deceptive orchid species (Dawson, Molloy &Beuzenberg, 2007; Cozzolino & Scopece, 2008).

(1) Pollinator identities

Although some rewarding orchid species are pollinated bybirds (Singer & Sazima, 2000; Johnson & Brown, 2004;Micheneau, Fournel & Pailler, 2006), no other vertebratessuch as rodents or bats are reported as orchid pollinators,and only insects are involved in sexually deceptive pollina-tion (Table 1). The typical pollinator of a sexually deceptiveorchid is male, an insect, and solitary rather than social(Gaskett, Winnick & Herberstein, 2008; see Table 1 forpollinator species, families and orders). The few reportsof female insects visiting orchids in potentially sexually


60 A. C. Gaskett

deceptive pollination systems require further substantiation.For example, early reports of pollination of Pterostylis orchidsby female mosquitoes (Coleman, 1934; Table 1) are drawnfrom a single observation and it is unclear whether pollinationinvolved any sexual behaviour.

Solitary and parasitoid wasps are the most commonpollinators of sexually deceptive orchids (Table 1). Suchspecialised pollination by wasps is rare in almost all othergroups of flowering plants, except figs (Johnson, 2005). Thyn-nine, ichneumonid and scoliid wasps pollinate species frommost Australian sexually deceptive orchid genera, and sphe-cid and pompilid wasps pollinate both South African Disa

species (Table 1). European Ophrys species are predominantlypollinated by solitary bees in the families Andrenidae, Col-letidae, Megachilidae, and Apidae (but see Section III.3, andfamilies of pollinators listed in Table 1).

(2) Pollinator mating systems and traits

The mating systems of solitary wasps and bees have severalfeatures that may facilitate or pre-adapt them to exploita-tion by sexually deceptive orchids. These features couldinclude: male attraction to airborne sex signals (allowingsignal mimicry and long-distance attraction by orchids),intense male searching and vigilance for sex signals (encour-aging rapid response to orchids), vigorous mating behaviour(ensuring pollinia transfer between the orchid and pollina-tor), and polygyny (ensuring a pollinator visits more than oneorchid, permitting both pollinia collection and delivery). Cor-respondingly, male hymenoptera from solitary species aretypically strongly attracted to the airborne sex pheromonesof female conspecifics (Ridley, 1993; Godfray & Cook, 1997).Male bees and wasps are also generally highly vigilant andrespond quickly to female pheromones. Female monandryor first-male sperm precedence imposes strong selection onthese males to secure paternity by rapidly finding and matingwith virgin females (Alcock et al., 1978; Eickwort & Ginsberg,1980; Tengo, Eriksson & Borg-Karlson, 1989; Hardy, 1994;El Agoze, Poirie & Periquet, 1995; Paxton, 2005; Damiens &Boivin, 2006). For example, the solitary bee Colletes cunicular-

ius is the sole or major pollinator for at least six Ophrys species(Table 1) and has many characteristics lending it to orchidexploitation. Colletes cunicularius is relatively common, thefemales are monandrous, attract mates with sex pheromonesand do not exhibit any courtship behaviour, and the malesare polygynous (Larsson, 1991). Consequently, there is con-siderable competition between male Colletes cunicularius todetect virgin female pheromones quickly and to mate firstwith many females (Cane & Tengo, 1988; Mant et al., 2005b).Male thynnine wasps (family Tiphiidae, subfamily Thynni-nae), which are common pollinators of Australian sexuallydeceptive orchids, have many similar mate-searching andmating behaviours (Burrell, 1935; Alcock, 1981). Therefore,orchids that mimic the sex pheromones of females of theseinsect taxa benefit from the males’ rapid response to scentand enthusiastic and somewhat indiscriminate mating.

Haplodiploid insects are surprisingly common pollina-tors of sexually deceptive orchids (Gaskett et al., 2008). Many

diploid insect orders that are diverse, abundant, and commonpollinators for rewarding orchids and other plants are eitherconspicuously absent (Hemiptera, Lepidoptera, Orthoptera)or scarce (Coleoptera, Diptera) in the pollination of sexuallydeceptive orchids (see Tables 1 and 2 for pollinator types).This may reflect current knowledge (for example, in thefuture more dipteran pollinators of sexually deceptive Lep-

anthes species are likely to be discovered), but haplodiploidymay also provide some advantageous features that facilitatethe maintenance of sexual deception. In haplodiploid insectspecies, fertilised eggs become female offspring and unfer-tilised eggs become male offspring (King, 1987; Hardy, 1994;Heimpel & de Boer, 2008). Therefore, female haplodiploidinsects deprived of matings (because male insects are matingwith orchids) can still reproduce, although all their offspringmust be sons. In this manner, haplodiploidy could moder-ate orchid interference in pollinator reproduction, and evengenerate extra males to act as pollinators (Gaskett et al.,2008). A further consequence of haplodiploidy is that selec-tion imposed on male insects by orchids cannot be inheriteddirectly by their sons because any eggs fertilised by a male’ssperm always become daughters. Selection on a male musttherefore always operate indirectly via his daughters andthen on her sons, effectively doubling the intergenerationaldelay in any response to orchid exploitation. However, indi-rect selection in any solitary hymenoptera appears largelyunstudied and research into this topic using the pollina-tors of sexually deceptive orchids would make a significantcontribution to general understanding of haplodiploidy andindirect selection.

(3) Exceptions to the general types of pollinators

Not all pollinators of sexually deceptive orchids are soli-tary, haplodiploid hymenoptera. For example male socialbees pollinate South American Trigonidium obtusum and Mor-

molyca ringens, and European Orchis galilea (Bino et al., 1982;Singer, 2002; Singer et al., 2004). Male social ants pollinateAustralian Leporella fimbriata, however no social interactionsare observed between these males (Peakall, 1989). Diploidflies (Diptera) pollinate Central American genera, and theincidence of fly pollination is almost certain to increase asfurther studies are undertaken on orchids from this region(Calvo, 1990; Christensen, 1994; van der Cingel, 2001;Blanco & Barboza, 2005). A hoverfly (Syrphidae; Diptera)is an occasional pollinator of European Ophrys holoserica, aspecies primarily pollinated by anthophorid bees (Table 1;Paulus, 2006). Many Australian and New Zealand mem-bers of Pterostylis and synonymous genera are also potentiallypollinated by diploid diptera, principally flies and fungusgnats (Christensen, 1994; Table 1). However, the extent ofsexual deception in Pterostylis is unclear (see Section IV.3).Sexual deception of diploid beetle pollinators (Coleoptera)is documented for Ophrys blithopertha, Ophrys fuciflora, andOphrys urteae, and is occasionally observed for Ophrys holoserica

(Delforge, 2005; Paulus, 2006; Tyteca, Rois & Vereecken,2006; Paulus, 2009).



Tab

le2.

Food

-dec

eptiv

eor

unre

war

ding

orch

idsp

ecie

ste

sted

for

sim

ilari

tyin

colo

urw

ithco

-occ

urri

ngpl

ant

spec

ies

that

dopr

ovid

ene

ctar

rew

ards

for

thei

rpo

llina

tors

.Po

llina

tion

succ

ess

for

each

orch

idsp

ecie

sis

the

aver

age

ofva

lues

repo

rted

inth

eso

urce

.N=

sum

ofsa

mpl

esi

zes

repo

rted

inso

urce

Orc

hid

spec

ies

Rew

ardi

ngm

odel

Polli

nato

rO

rchi

dm

ean

Polli

natio

nsu

cces

sSo

urce

Dis

eae

Dis

ace

phal

otes

Rch

b.f.

ssp.

ceph

alot

esSca

bios

aco

lum

bari

aL

.(D

ipsa

cace

ae)

Lon

g-pr

obos

cid

flies

(Tab

anid

ae,

Nem

estr

inid

ae)

flow

ers:

13.9

%po

llini

are

mov

ed,2

1.2%

polli

nia

depo

site

d(N

=37

)

John

son

etal

.(20

03)

Dis

afe

rrug

inea

(Thu

nb.)

Sw.

Tri

toni

opsi

str

itic

ea(B

urm

.F.)

Gol

dbl.

(Iri

dace

ae)o

rK

niph

ofia

uvar

ia(L

.)H

ook

(Asp

hode

lace

ae)

But

terfl

yM

ener

istu

lbag

hia

L.

(Nym

phal

idae

)w

ithm

odel

sp.:

69.5

%of

flow

ers

setf

ruit

(N=

600)

,with

out

mod

elsp

:28%

(N=

852)

John

son

(199

4)

Dis

ane

rvos

aL

indl

.W

atso

nia

dens

iflor

as.

l.B

aker

(Iri

dace

ae)

Lon

g-pr

obos

cid

flyP

hilo

lich

eae

thio

pica

Thu

nber

g(T

aban

idae

)

24.9

%of

flow

ers

polli

nate

d(N

=95

);41

.3%

frui

tset

per

plan

t(N

=28

)

John

son

&M

orita

(200

6)

Dis

ani

vea

H.P

.Lin

der

Zal

uzia

nsky

am

icro

siph

on(K

untz

e)K

.Sch

um.(

Scro

phul

aria

ceae

)L

ong-

prob

osci

dfly

Pro

soec

aga

nglb

auer

iL

icht

war

dt(N

emes

trin

idae

)

92.5

%of

flow

ers

setf

ruit

(N=

890)

And

erso

n,Jo

hnso

n&

Car

butt

(200

5)

Dis

apu

lchr

aSo

nd.

Wat

soni

ale

pida

N.E

.Bro

wn

(Iri

dace

ae)

Lon

g-pr

obos

cid

flyP

hilo

lich

eae

thio

pica

(Thu

nber

g)(T

aban

idae

)

15.7

%fr

uits

etpe

rpl

ant

(N=

17)

John

son

(200

0)

Diu

rid

eae

Diu

ris

aequ

alis

Fitz

g.G

omph

olob

ium

hueg

elii

Ben

tham

(Fab

acea

e)In

dsto

etal

.(20

06)

Diu

ris

mac

ulat

aSm

ithD

avie

sia

ulic

ifol

iaA

ndre

ws

ssp.

ulic

ifol

ia,pl

usot

her

rela

ted

legu

mes

(Fab

acea

e)

Mal

eso

litar

ybe

esT

rich

ocol

lete

sve

nust

us(S

mith

)(C

olle

tidae

)17

%of

flow

ers

setf

ruit

(N=

122)

;59%

ofpl

ants

setf

ruit

(N=

29)

Inds

toet

al.(

2006

)

Orc

hid

eae

Orc

his

isra

elitic

aH

.Bau

man

n&

Daf

niB

elle

valia

flexu

osa

Boi

ss.(

Lili

acea

e)So

litar

ybe

esA

ntho

phor

asp

.,E

ucer

acl

ypea

taE

rich

son

(Ant

hoph

orid

ae),

Bom

bylius

sp.(

Bom

bylii

dae)

with

mod

elsp

.48.

6%of

flow

ers

setf

ruit

(N=

692)

,with

out

mod

elsp

.3.7

5%(N

=42

8)

Daf

ni&

Ivri

(198

1);G

aliz

iaet

al.

(200

5)

Neo

ttie

aeC

epha

lant

hera

rubr

a(L

.)R

ich.

Cam

panu

lasp

p.(C

ampa

nula

ceae

)So

litar

ybe

esC

helo

stom

afu

ligi

nosu

mPa

nzer

,C

.ca

mpa

nula

rum

(Kir

by)

(Meg

achi

lidae

)

8.5%

frui

tspe

rflo

wer

(N=

200)

Nils

son

(198

3)


62 A. C. Gaskett

IV. POLLINATOR BEHAVIOURS

(1) Pollinator behaviour and the origins of sexualdeception

Although pollination by sexual deception is confirmed onlyfor orchids, Kullenberg (1961) reported sexual behaviour bya sphecid wasp on flowers of Guiera senegalensis Lam. (Com-bretaceae), and sexual deception is a compelling explanationfor the nectarless and insectiform flowers of Gilliesia graminea

Lindl. (Alliaceae; Rudall et al., 2002). These cases are yetto be confirmed. Despite the prevalence of sexual decep-tion amongst orchids, pollination involving some form ofinsect sexual behaviour may actually precede the evolutionof orchids. Early floral scents that evolved initially to protectplant reproductive organs from insect herbivory are likely tohave resembled the sex pheromones of other insects (Pellmyr& Thien, 1986; Harrewijn, Minks & Mollema, 1994; Gang,2005). Consequently, insects were likely to aggregate andmate on the flowers and coincidentally function as pollina-tors. For many modern insect species, plant and floral scentsstill enhance insect sex pheromone release and attractiveness(for a review, see Reddy & Guerrero, 2004).

In orchids, phylogenetic comparisons suggest that sexualdeception evolved from food deception, which is commonamongst primitive, nectarless orchid groups, although someof these orchids do provide pollen as a reward (Cozzolino& Widmer, 2005). Surveying pollinator behaviour withina genus could indicate how the transition between foodand sexual deception may occur, and whether elements ofboth systems can coexist. For example, different species ofAustralian Donkey orchids (genus Diuris) reward or deceiveforaging insects, and potentially, exploit aspects of pollinatorsexual behaviour. Diuris alba appears to be a rewardingspecies; it provides nectar and has several pollinator species,whereas Diuris aurea is food-deceptive and has severalpollinators (Indsto et al., 2007). Diuris pedunculata providesnectar, but an early report suggests it is pollinated only bymale bees of Halictus lanuginosus, perhaps suggesting some sex-based pollination (Coleman, 1932). Another species, Diuris

maculata, has features associated with sexual deception, it lacksnectar and is pollinated by male bees of Tricholetes venustus

(Indsto et al., 2006). However, detailed observations revealno sexual behaviour with orchid flowers (Indsto et al., 2006).In the case of these last two species, Diuris pedunculata andD. maculata, it seems likely that the orchids act as, or mimic,both a foraging site and a rendezvous site for courtingmales, although the lack of female visitors is inconsistentwith observations of other orchid species thought to mimicrendezvous sites (Nilsson, 1983; Steiner, 1998; Jersakovaet al., 2006a). Other orchids proposed to employ aspectsof both pollinator foraging and sexual behaviour includeEuropean Orchis galilaea (Bino et al., 1982) and AustralianCaladenia patersonii (Stoutamire, 1983), and possibly JapaneseCymbidium pumilum (Sasaki et al., 1991). However, there isscarce empirical evidence that any orchid species employsboth sexual and food deception (Faast et al., 2009). Inthese putative cases, detailed observations are required to

confirm pollinator species and sex, and document any sexualbehaviour.

Phylogenetic analysis of Disa suggests multiple shiftsbetween pollinator types and gains and losses of nectarrewards (Johnson et al., 1998). Similar phylogenetic analysestracing the evolution of sexual deception could be appliedto the Australian genus Caladenia, which has a diversity ofrewarding and food- and sexually deceptive pollination sys-tems and considerable new data now available for analysis(Stoutamire, 1983; Bates, 1984; Peakall & Beattie, 1996;Hopper & Brown, 2004; Salzmann, Brown & Schiestl,2006; Dixon & Tremblay, 2009; Dixon & Hopper, 2009;Phillips et al., 2009a, b). Table 1 provides the known or puta-tive pollinators for many sexually deceptive orchid species.Lists of pollinators for food-deceptive and rewarding Calade-

nia species are available elsewhere (e.g. Brown et al., 1997;Phillips et al., 2009a).

(2) Pollinator sexual behaviour with orchids

Sexually deceptive orchids elicit a range of sexual behavioursfrom their pollinators. Pollinators of some orchid species doindeed attempt to mate with the orchid, typically by graspingthe large central petal or labellum (Fig. 1; Kullenberg, 1961;Paulus & Gack, 1990; Table 1). This copulatory behaviouroccurs for European Ophrys and Orchis species, Central Amer-ican Lepanthes glicensteinii, South American Mormolyca ringens

and Geoblasta pennicillata, and Australian Calochilus campestris,

Leporella fimbriata, and Cryptostylis species (Coleman, 1928a,1929, 1930; Fordham, 1946; Bino et al., 1982; Peakall, 1989;Bower & Branwhite, 1993; Singer et al., 2004; Blanco &Barboza, 2005; Ciotek et al., 2006). Pollination of AustralianCryptostylis species even involves pollinator ejaculation. Thiswas first suspected by Coleman (1927, 1928a, b) whilstobserving pollinator behaviour on Cryptostylis leptochila, andwas recently confirmed using microscopy and sperm-stainingdye (Gaskett et al., 2008). Ejaculation during orchid pollina-tion is also likely in Lepanthes glicenstenii because scanningelectron microscopy of flowers after pollinator visits revealedputative spermatophores (Blanco & Barboza, 2005). Thereis currently little evidence of pollinator ejaculation for anyother orchid species, but future studies are likely to generatefurther examples, especially amongst lesser-known Lepanthes

and Cryptostylis species.For most Australian sexually deceptive orchid species, suc-

cessful pollination requires only pre-copulatory rather thancopulatory behaviour from the pollinator. When a maleinsect grips or lifts the orchid labellum as if it was a femaleinsect, the labellum bends on a flexible hinge and presses theduped insect into contact with the orchid stigma and pollinia(Bower, 2001e; see Fig. 1D for orchid flower parts). This iscommon for orchids from the diverse genera Caladenia andChiloglottis, the less speciose Arthrochilus, Caleana, Drakaea andParacaleana genera, and the single species from the genus Spic-

ulaea (Fig. 2; Cady, 1965; Stoutamire, 1983; Peakall, 1990;Peakall & Beattie, 1996; Alcock, 2000; Bower, 2001a, b, c,e, f ; Jones et al., 2001; Hopper & Brown, 2006, 2007). Insome species, the sexual behaviour of the pollinator on the



orchid may trigger a floral trap. For example, pollinatorsattempting copulation with Australian Duck orchids, e.g.Caleana major (Fig. 2C) become briefly pinned upside-downbetween an orchid’s hinged labellum and the column, whichbears the stigma and pollinia (Bower, 2001c). Male bees ofPlebeia droryana (Meliponinae) visiting South American Trigo-

nidium obtusum (Maxillariinae) are also briefly trapped afterthey attempt copulation with the sepals or petals and slipon a waxy surface into a floral cavity (Singer, 2002). Thepollinator soon escapes via a hinged floral lip after brushingpast the stigma and pollinia.

(3) Sexual deception by Pterostylis

Pterostylis and synonomous genera comprise a taxonomicallycontentious complex of Australian and New Zealand ter-restrial species (for proposed revisions and various namessee Table 1; Jones & Clements, 2003; Jones, 2006; Hopper,2009). Many species in this group have a floral trap, althoughentrapment does not appear to require copulatory behaviourfrom the pollinator, unlike the traps described above forCaleana and Trigonidium orchid species. When the potentialpollinator touches the sensitive labellum he is catapultedinto a curved hood formed by the dorsal sepal, and canescape only via a narrow passage that forces contact withthe pollinia and stigma (Fig. 2E; Cheeseman, 1872; Sargent,1909; Coleman, 1934; Christensen, 1994; Bernhardt, 1995).Experiments suggest that labellae can be triggered up to threetimes, and regain their position and sensitivity within 3h, orlonger in cool conditions (Sargent, 1909; Bernhardt, 1995).

It is important to note that the occurrence of sexualdeception in Pterostylis spp. is largely based on unpublished oranecdotal evidence (often of considerable antiquity), and pol-linator behaviour for most species in the group is completelyunstudied (Cheeseman, 1872; Thomson, 1878; Darwin,

1885; Sargent, 1909; Jones, 2001; Jones & Clements, 2003;Lehnebach, Robertson & Hedderley, 2005). Although almostall reported pollinators for Pterostylis spp. are male (Table 1),confirming pollinator identity or sexual behaviour is chal-lenging because pollination is rarely observed (see Table 1 forpollination rates). There is some suggestion that the fungusgnat pollinating Pterostylis gibbosa does attempt to mate withthe orchid labellum (National Parks and Wildlife Service,2002), but much remains to be discovered about these enig-matic dipteran-orchid pollination relationships before sexualdeception can be substantiated.

(4) Within-species variation in pollinator behaviour

Within a pollinator species, not all individuals that encounteran orchid are fooled into actual pollination. Some individ-uals approach the orchid but then fly away without landingor attempting sexual behaviour (Table 3). This variationamong individuals could be due to genetic differences inlearning ability (Dukas, 2008), or differing previous expe-rience with orchids (Ayasse et al., 2000). However, priorlearning is not necessary to provoke this variability. Whenorchids are experimentally moved within their pollinator’srange to areas where they do not normally grow, pollinatorresponses still vary even though all the insects attracted musthave no previous experience with sexually deceptive orchids(Bower, 1996). There is probably individual variation ininsect sensory sensitivity or perception of orchid signals, andin the quality or attractiveness of each orchid (Peakall, 1990).Responses are also likely to be affected by spatial variation intemperature and air currents, influencing the local dispersalof orchid scent.

Data extracted from the literature suggest that the per-centage of pollinators attracted and then actually fooled intopollinating an orchid varies consistently among orchid species

Table 3. Percentages of insects fooled into pollinating some Australian sexually deceptive orchids after initial attraction. N = visitsobserved. *Data combined & averaged from more than one study

Orchid Pollinator behaviour % fooled N Source

Caladenia (syn. Arachnorchis) tentaculata Gripping hinged labellum 7.5 287 Peakall & Beattie (1996)Chiloglottis diphylla Gripping hinged labellum 41.7 24 Bower (1996)Chiloglottis (syn. Myrmechila) formicifera Gripping hinged labellum 10.5 38 Bower (1996)Chiloglottis (syn. Myrmechila) platyptera Gripping hinged labellum 28.3 53 Bower (1996)Chiloglottis (syn. Simpliglottis) pluricallata Gripping hinged labellum 3.85 26 Bower (1996)Chiloglottis reflexa Gripping hinged labellum 24.0 48 Bower (1996)Chiloglottis seminuda Gripping hinged labellum 39.0 79 Bower (1996)Chiloglottis trilabra Gripping hinged labellum 23.23∗ 2897∗ Peakall & Handel (1993);

Bower (1996)Chiloglottis (syn. Simpliglottis) valida Gripping hinged labellum 13.0 46 Bower (1996)Cryptostylis erecta Copulation/ejaculation 90.99∗ 111∗ Gaskett et al. (2008); A. C.

Gaskett (unpublisheddata)

Cryptostylis subulata Copulation/ejaculation 92.73∗ 55∗ Gaskett et al. (2008); A. C.Gaskett (unpublisheddata)

Drakaea glyptodon Gripping hinged labellum 21.9 618 Peakall (1990)Leporella fimbriata Copulation 60.0 55 Peakall (1989)Spiculaea ciliata Copulation 44.0 50 Alcock (2000)


64 A. C. Gaskett

depending on the extent of pollinator sexual behaviourelicited by each orchid (Table 3). If orchids are classifiedaccording to the sexual behaviour stimulated from their polli-nators, orchids causing more extreme behaviour have higherpollination success (Gaskett et al., 2008). Analysis of datapresented in Tables 1 and 3 shows there is also a significantcorrelation between the extent of pollinator sexual behaviourand the percentage of attracted insects that are fooled intopollination (partial correlation: 0.84, d.f. = 11, P < 0.001,controlling for the number of pollinator visits observed).Orchids stimulating the most extreme sexual behaviour arethe most likely to fool pollinators into making contact withthe orchid (Fig. 3), suggesting a strong fitness benefit fororchids with persuasive mimicry and deceptive signalling. Itis worth noting that the data available in the literature mayoverestimate pollinator response because it is impossible todetermine the number of insects that did detect an orchid,but did not fly close enough to be counted by an observer.

V. POLLINATOR ABUNDANCE AND DIVERSITY

Insect abundance and diversity could be important factorsinfluencing the reproduction and fitness of sexually deceptiveorchids. Orchid pollination success can vary considerablyamong years and determining lifetime success is difficultgiven the potential longevity of individual plants and thelikelihood of vegetative or clonal reproduction (Neiland &Wilcock, 1998; Tremblay et al., 2005). Although there aresome long-term demographic studies of sexually deceptiveorchids, actual pollination or seed set rates are not neces-sarily reported (e.g. Hutchings, 1987), and most long-term

Fig. 3. The relationship between the percentage of the insectsattracted to an orchid that are fooled into pollinating the flowerand the extent of pollinator sexual behaviour stimulated by theorchid species.

studies focus on food-deceptive or rewarding orchid species(e.g. Pfeifer, Heinrich & Jetschke, 2006; Zotz & Schmidt,2006). When data for food and sexually deceptive orchidsare combined, the global averages calculated for the ratesof pollination or fruit set per flower are typically low andapproximately half that of rewarding or nectariferous species:25% versus 52.9% (Neiland & Wilcock, 1998) or 20.7% ver-

sus 37.1% (Tremblay et al., 2005), respectively. In Australia,sexually deceptive orchids have lower fruit-set per flowerthan food-deceptive orchids (14% versus 36%; Phillips et al.,2009a). Globally, the literature surveyed for Table 1 showsthat for sexually deceptive orchids, an average of 20.5 ±14.7% of all flowers (mean ± S.D., N = 35 species), oralternatively, 37.5 ± 20.9% of plants (N = 11 species), hadpollinia collected and deposited, or set fruit.

The poor pollination success of sexually deceptive orchidsis generally attributed to a lack of pollinators or pollinatorvisits, rather than any limitation in resources such as wateror nutrients (Peakall, 1989; Calvo, 1993; Neiland & Wilcock,1998; Schiestl, 2005; Tremblay et al., 2005; Zotz & Schmidt,2006; Vandewoestijne et al., 2009). Pollinator limitation maybe a consequence of extreme specialisation to a single or veryfew pollinator species. Specialist orchids may be vulnerable tomismatches in pollinator emergence and flowering seasons,which is likely to worsen due to climate change (Memmottet al., 2007). Pollinator limitation may also be particularlysevere in sexually deceptive systems because of the likelihoodthat insects attracted to an orchid will not make contactor effect pollination, the variation in individual pollinatorresponses, or the possibility of fooled pollinators avoidingorchids or orchid locations after previous visits (see SectionsIV.2, IV.4 and VII). Thus, even if abundant pollinators areavailable, they may not necessarily be coerced into orchidvisits.

Sexual deception typically involves a species-specific pol-linator (Table 1), so the potential for speciation in sexuallydeceptive orchids may be constrained by the diversity ofinsects available to act as pollinators, and the potential forspeciation in an existing pollinator species. For example, theradiations of the relatively diverse sexually deceptive generaChiloglottis and Caladenia are both accompanied by frequentpollinator switching between closely related thynnine wasps(Mant et al., 2002; Mant, Brown & Weston, 2005c; Bower& Brown, 2009; Phillips et al., 2009a). Australian thynninewasps are diverse, and many of the 715 named species areendemic (Naumann, 2000). Table 1 shows that at least 70Australian thynnine species from 12 genera pollinate at least150 sexually deceptive orchid species from seven genera, withmany more thynnines yet to be formally identified (Table 1).This availability of diverse thynnines may have contributed tothe extraordinary diversification of the major (and largely sex-ually deceptive) subclades of Caladeniinae and Drakaeinae.Caladeniinae includes the large genus Caladenia, of which thesexually deceptive species are almost exclusively thynnine-pollinated, and Drakaeinae comprises a diverse radiation ofclosely related thynnine-pollinated genera including Caleana,Chiloglottis, Drakaea, and Paracaleana (Kores et al., 2001).



By contrast, all five Australian and New Zealand speciesof Cryptostylis (subclade Cryptostylidinae) share a single pol-linator, male Lissopimpla excelsa (family Ichneumonidae, sub-family Pimplinae; Coleman, 1928a, b, 1938; Graham, 1983;Schiestl, Peakall & Mant, 2004; Gaskett et al., 2008). Australiahas only four Lissopimpla species and a relatively small ich-neumonid fauna (Naumann, 2000). Therefore, any novel,mutated, or hybrid forms of Cryptostylis that arise may beunlikely to attract a new pollinator because so few Lissopimpla

species or Pimplinae are available in the environment. Inter-estingly, although Australia has several solitary bee speciesfrom the families that are major pollinators for Ophrys speciesin Europe, they are not involved in any sexually deceptivepollination in Australia (Colletidae, Halictidae, Megachilidaeand Anthophoridae; Table 1; Naumann, 2000).

VI. ORCHID SIGNALS AND POLLINATORPERCEPTION

Although understanding of orchid scent and pheromonemimicry is advancing rapidly, there is only meagreinformation about other signals or cues involved in pollinatordeception. Scent is undoubtedly vital for long-rangepollinator attraction, but once a pollinator is nearby, visualsignals such as colour or shape must indicate the specificsource of the scent, and, crucially, coerce him into makingcontact (Peakall & Beattie, 1996; Streinzer, Paulus & Spaethe,2009). This would be particularly important for species thatoccur in dense aggregations that generate a large scent plumewith multiple, indeterminate origins. It is often assumed orspeculated that shape and colour play a role in sexualdeception by orchids (e.g. Dodson et al., 1969; Bergstrom,1978; Ayasse et al., 1997; Ascensao et al., 2005; Jersakovaet al., 2006a; Paulus, 2006; Salzmann et al., 2006; Schluter &Schiestl, 2008). However, experimental tests for shape andcolour mimicry and manipulations of these signals requireconsiderably more attention before this can be confirmed.

(1) Scent

Early researchers swiftly recognised the importance of orchidscent for attracting pollinators and stimulating pollinatorsexual behaviour (Coleman, 1928b, 1929; Kullenberg, 1956;1961). In the field, pollinators approach orchid flowers with acharacteristic zig-zag flight path associated with chemorecep-tion (Wallace, 1978; Stoutamire, 1979, 1983; Peakall, Beattie& James, 1987; Peakall, 1989, 1990; Peakall & Beattie, 1996;Paulus, 2006). Behavioural tests offering pollinators dissectedorchid flowers can be useful for determining where scent isreleased in the flower (typically from the sepals, petals, and/orlabellum; Peakall, 1989; Peakall & Beattie, 1996).

Initially, behavioural studies confirmed that pollinatorscould be attracted with extracts of sexually deceptive orchidsor synthetic mixtures of common compounds (Kullenberg,1956, 1961). Subsequent chemical analyses tested for simi-larities in extracts or volatiles collected from orchids and the

females of their pollinator species using gas chromatographyand gas chromatography-mass spectrometry (GC, GC-MS;Bergstrom, 1978; Borg-Karlson, 1987, 1990; Schiestl et al.,1999; Flach et al., 2006). The most powerful studies combinebehavioural observations and assays with chemical analysesand tests for pollinator perception of scents (Fig. 4). Pollinatorperception of orchid scent can be tested with calcium imag-ing of antennal lobe activity in the pollinator brain duringexposure to floral scents (Galizia et al., 2005), or much morecommonly, gas chromatography-electroantennography orgas chromatography-electroantennal detection (GC-EAG orGC-EAD; Schiestl, 2005). GC-EAD allows scent compoundsto be individually tested for their capacity to stimulate a polli-nator’s antennal chemoreceptors. Whole live antennae of thepollinator species have been tested with synthetic versionsof compounds identified in orchids (Agren & Borg-Karlson,1984; Schiestl et al., 1999), or more commonly, with extractsof orchid labellae and/or females of the pollinator species(Schiestl et al., 1999, 2000; Schiestl & Ayasse, 2002; Ayasseet al., 2003; Mant et al., 2005b, d; Schiestl & Peakall, 2005;Stokl et al., 2005, 2007; Vereecken & Schiestl, 2008; Gogleret al., 2009). Not every electrophysiologically active com-pound necessarily elicits a behavioural response from thepollinator, so behavioural assays must be performed (Schiestl& Marion-Poll, 2002; Leal, 2005). The model example ofthis procedure is the elegant and methodical identification,synthesis, and field testing of the single novel compoundattracting pollinators to Chiloglottis trapeziformis, and the use ofthis compound and analogs in further investigations of otherChiloglottis species (Schiestl et al., 2003; Schiestl & Peakall,2005; Poldy, Peakall & Barrow, 2008; Franke et al., 2009;Fig. 4).

Application of GC-EAD could be enhanced by moredetailed reporting. Few studies reveal the total number oftrials performed, including those in which antennae failed tomake any response at all. It is also rare to report the mag-nitude or number of antennal responses required before acompound can be considered ‘electrophysiologically active’.For example, compounds could be considered electrophys-iologically active when they provoke antennal responses inat least half of the runs performed (Schiestl & Ayasse, 2002;Stokl et al., 2007; Gogler et al., 2009). Ideally, studies shouldreport the number of trials performed, the proportion inwhich antennae failed to respond, and the number andmagnitude of antennal responses obtained for each elec-trophysiologically active compound. The latter could beaddressed when publishing Tables of electrophysiologicallyactive compounds by adding a column that provides thenumber of antennae responding to each compound andthe mean magnitude of the response. Since most statisticaltests assume independence of data, it is also important todeclare and control for antennae used in more than onetrial (e.g. Mant et al., 2005b) and when using both antennaefrom one insect. Interestingly, the sensitivity and respon-siveness of insect antennae (or conversely, the strength ofthe orchid signal) may vary consistently with some biologi-cally relevant factor such as the extent of pollinator sexual


66 A. C. Gaskett

Fig. 4. Research paths incorporating a pollinator perspective: assessing the role of pollinator behaviour and pollinator perceptionof orchid signals in studies of pollination by sexual deception. GC, gas chromatography; GC-MS, gas chromatography-mass spectrometry; GC-EAD, gas chromatography-electroantennodetection or gas chromatography-electroantennography; SEM,scanning electron microscopy. 1Bower & Brown (2009); 2Peakall (1990); 3Alcock (1981); 4Schiestl et al. (1999); 5Schiestl et al. (2003);6Gaskett & Herberstein (2010); 7Schiestl (2004); 8Zelditch et al. (2004); 9Shipunov & Bateman (2005); 10Kullenberg (1961); 11 ´Agrenet al. 1984; 12Galizia et al. (2005); 13Francke et al. (2009); 14Vereecken et al. (2007a); 15Ayasse et al. (2000); 16Wong et al. (2004);17Johnson et al. (1998); 18Mondragon-Palomino & Theiβen (2009); 19Fitzpatrick et al. (2005).

behaviour, or between major and minor pollinators for anorchid species, suggesting interesting additional analyses thatwould maximise the value of EAD-based research.

(2) Colour

Analyses of orchid colour from a human perspective arelargely redundant given the differences between human andinsect visual systems (Kelber, Vorobyev & Osorio, 2003).Early studies by Kullenberg (1961) attempted to quantifythe colour of Ophrys species with spectral measurements andcomparisons with standard colour hues. Recently, studiesof food-deceptive pollination systems compare the spec-tral reflectance of food-deceptive orchids and co-occurringrewarding species (Table 2). Some studies take the next stepand consider pollinator perception of colour by mappingspectral reflectances of food-deceptive orchids into pollina-tor visual systems (Gumbert & Kunze, 2001; Galizia et al.,2005; Indsto et al., 2006). Similar analyses for sexually decep-tive species show that despite colour differences seen byhumans (Fig. 1), four Australian Cryptostylis orchid speciesare all perceptually identical in colour to their pollinator’sfemale conspecific when modelled into a hymenopteranvisual system (Gaskett & Herberstein, 2010). Analysis fromthe pollinator’s visual perspective is crucial for understanding

pollinator-driven selection on orchid colour, but is hinderedby the lack of specific information about the visual systems ofmost orchid pollinator species and disagreement about mod-elling methods (Chittka, 1992; Vorobyev & Brandt, 1997;Kelber et al., 2003; Chittka & Kevan, 2005). Nonetheless,any studies modelling orchids from the visual perspective ofthe pollinator would be a significant contribution (Fig. 4).

A major difficulty when studying colour mimicry byorchids is the potential to conflate mimicry and conver-gent evolution (see Johnson, Alexandersson & Linder, 2003;Grim, 2005). If food-deceptive orchids (the putative mimic)are compared with co-occurring rewarding flower species(the models), it is likely their shared environmental condi-tions and pollinators would exert similar selective pressureon many features including colour. This problem can beavoided by investigating mimicry in sexually deceptive,rather than food-deceptive, pollination systems. Sexuallydeceptive orchids, the mimics, have an entirely differentecology and physiology to their models, female insects. Con-sequently, similarities between the orchid and the femaleinsect can be more confidently attributed to mimicry ratherthan to convergence in sexually deceptive systems.

Sexually deceptive orchids may also exploit pollinator sen-sory biases or perceptual weaknesses. Sensory biases evolvewhen sensitivity to certain signals or cues provides fitness



benefits, e.g. quick detection of colours associated with foodor mates, or a preference for larger body size in matechoice (Schaefer & Ruxton, 2009). Orchids that exploitinsect sensory biases can take advantage of their pollinator’sinnate attraction to certain signals such as wavelengths orshapes (see also Section VI.3). The ornaments of sexuallydeceptive Ophrys heldreichii orchids were thought to exploitinnate pollinator visual biases for pink wavelengths becausepollinators preferred flowers with intact natural pink orna-ments (Spaethe, Moser & Paulus, 2007). However, a laterstudy established that pollinators found the orchid morerapidly when researchers attached various coloured orna-ments as long as they contrasted with the background,suggesting a sensory bias for contrast rather than specificcolours (Streinzer et al., 2009). Yellow and ultraviolet (UV)wavelengths may be more likely candidates for exploita-tion of innate insect preferences. Many insects are stronglyattracted to yellow or UV (Jonsson, Lindkvist & Anderson,2005; Goulson et al., 2007; Lunau, 2007) and orchids oftenhave bright yellow pollinia visible to the pollinator or yellowsepals or petals (e.g. Cryptostylis, Fig. 1; Gaskett & Herberstein,2010; see Delforge (2005) for pictures of Ophyrs spp.). Brightyellow spots on the labellum are known to attract pollinatorsin the food-deceptive slipper orchid Paphiopedilum barbigerum

(Shi et al., 2009) and similar pollinator behaviour is reportedin other Paphiopedilum species (Banziger, 1996). Exploitationof insect attraction to UV is also plausible (Paulus, 2006;Gaskett & Herberstein, 2010). For example, bumps on thelabellae of Cryptostylis subulata and C. ovata reflect UV, identicalto the wings of their pollinator’s female conspecific (Gaskett& Herberstein, 2010). However, UV-reflection is relativelyuncommon in rewarding flowers (Chittka et al., 1994), and iscorrespondingly rare in food-deceptive orchids (e.g. Johnson,2000; Johnson et al., 2003).

Intriguingly, many sexually deceptive orchids are pre-dominantly green, red, or white, which are colours not easilyseen by hymenoptera (Gaskett & Herberstein, 2010; Figs 1and 2; further images of Australian, European, and Southand Central American species see Blanco & Barboza, 2005;Delforge, 2005; Jones, 2006; Singer et al., 2006). Green flow-ers may be difficult to distinguish from surrounding greenleaves, perhaps resembling background leaves or plants andthus obscuring parts of the flower that may hinder mimicryof female insect body shapes. Although white flowers appearobvious to humans, they can be difficult for hymenopterato distinguish from the background (Chittka et al., 1994).This is because white flowers, like background foliage, soiland stones, cause approximately equal excitation of theBlue, Green and UV receptors typical of most hymenoptera(Chittka et al., 1994). Red floral colouration may act asa cognitive sensory trap (Schaefer & Ruxton, 2009). Redwavelengths are beyond the peak sensitivities of the Blue,Green and UV receptors, and are therefore difficult forhymenoptera to detect or differentiate between (Chittkaet al., 1994) and distinguish from the background (Spaethe,Tautz & Chittka, 2001). Better modelling of pollinator per-ception of orchid colours requires characterisation of the

peak sensitivities of the visual receptors of common sexuallydeceptive orchid pollinators such as Colletes cunicularius orthynnines (e.g. Peitsch et al., 1992). More studies investigat-ing and testing for exploitation of sensory biases and sensorytraps in sexual deception would be fascinating.

Finally, although within-species colour polymorphismoccurs in several food-deceptive orchid species (Gigord,Macnair & Smithson, 2001; Koivisto, Vallius & Salonen,2002; Salzmann & Schiestl, 2007), it is rare for sexuallydeceptive species, exceptions include Caladenia behrii (Dickson& Petit, 2006) and Ophrys arachnitiformis (Vereecken & Schiestl,2009). The role of colour polymorphism is unclear. Moststudies with food-deceptive orchid species find no evidenceof frequency-dependent selection or pollinator preferencesfor rare colour morphs (Koivisto et al., 2002; Aragon &Ackerman, 2004; Pellegrino, Bellusci & Musacchio, 2005;Dickson & Petit, 2006; Smithson et al., 2007; Tremblay& Ackerman, 2007; Vereecken & Schiestl, 2009, but seeGigord et al., 2001). Thus future studies of colour polymor-phism in either sexual or food deception should considerhow colour morphs differ in several factors such as fitness,post-pollination barriers, or seed viability, rather than justpollinator preferences (e.g. Pellegrino et al., 2005; Jersakova,Kindlmann & Renner, 2006b).

(3) Shape

The shape of an orchid is also likely to be an important visualsignal for sexual deception. After a pollinator has landed onan orchid, he must be persuaded into attempting copulation.This could be accomplished by close-range mimicry of thedimensions and tactile qualities of the body of his femaleconspecific. Comparison of the distribution and dimensionsof hairs on the surface of Ophrys spp. labellae and the spe-cific female bees they mimic indicated considerable texturalcongruence (Agren, Kullenberg & Sensenbaugh, 1984). Sev-eral orchids feature notably insectiform labellae that mightmimic female insects, e.g. Drakaea, Paracaleana and Lepanthes

species and Geoblasta pennicillata, but others, including Cryp-

tostylis erecta, Trigonidium obtusum and Pterostylis species do notappear insect-like to the human viewer (Figs 1 and 2; Singer,2002; Blanco & Barboza, 2005; Ciotek et al., 2006).

Close-range tactile cues may also determine pollinatororientation on the orchid, which is imperative for effectivepollinia collection and transferral (Kullenberg, 1961;Wallace, 1978). The surface cells on the labellae of Ophrys fusca

and O. lutea bear long trichomes that point towards the stigmaand these are likely to direct the pollinator’s genital clasperstowards the stigma and adjacent pollinia (Ascensao et al.,2005). The hypothesis that trichomes function in pollinatororientation could be tested by experimentally removingtrichomes or manipulating their arrangement and observingpollinator orientation behaviour. In field experiments,pollination and fruit-set would be expected to be lowerfor orchids with experimentally removed trichomes than forcontrol orchids that had received a similar level of shamdamage, e.g. small cuts made on the reverse of the labellum.


68 A. C. Gaskett

Shape may also exploit pollinator sensory biases involvedin male mate-choice behaviour. Morphological comparisonsof flower size show that the labellae of Chiloglottis trapeziformis

orchids are consistently larger than the female insects theymimic (Schiestl, 2004). These large flowers could representan irresistible super-stimulus that exploits the common maleinsect preference for large female body size (Bonduriansky,2001; Schiestl, 2004). However, in tests with model femaleinsects, the pollinator of Chiloglottis trapeziformis preferredintermediate over both small and large models, indicating alimit to male preference for large female body size (Schiestl,2004). However, measurements were taken of the wholelabellum, rather than just the insectiform black, glossy callion the labellum of the orchid, which may be more relevantfor comparison (for drawings, see Bower, 1996; Mant et al.,2005a; Mant, Peakall & Weston, 2005e). A comprehensivemulti-species study of the possible tactile function of thesecalli in Chiloglottis species, the insectiform labellae of Drakaea

or Caleana species, or the whole labellae of Ophrys species,would help clarify the role (if any) of shape mimicry in sexualdeception.

The literature suggests two alternative and as yet unstudiedhypotheses for the function of varying floral shape in sexualdeception. Firstly, variation in shape could impair pollina-tor learned avoidance in the same way that scent variationhinders this process in Ophrys sphegodes and other unreward-ing flowers (Ayasse et al., 2000; Raguso, 2004). Experimentstesting pollinator behaviour and learning using manipulatedfloral shapes are required. Secondly, floral shape is undoubt-edly important in the function of floral traps. Morphology islikely to control both the location and duration of pollinatorcontact, with strong consequences for pollinia transfer andthus fitness. For example, when a pollinator grips the looselyhinged labellum of Arthrochilus species, he is swiftly swung intoa pair of flanges that control his position against the stigmaand pollinia, then a second pair of curved flanges traps hiswings and prevents his escape until after pollinia transferralhas occurred (Bower, 2001a). Research into the evolution oftrap mechanisms could commence by testing how variationin some morphological aspect of a floral trap interacts withpollination success.

(4) Multimodal signalling

In his thesis, Kullenberg (1961) addressed the possibilityof multiple olfactory, visual and tactile stimuli in sexualdeception, but there are few contemporary tests in whichpollinators are offered models with simultaneous variationsin scent and colour and shape to determine signal functionsand the extent of signal duplication (Fig. 4; e.g. Vereecken &Schiestl, 2009). Sexually deceptive orchids exploit their pol-linators’ mate search and mate-choice signals. Mate choiceoften involves assessment of multicomponent or multimodalsignals (Candolin, 2003; Papke, Kemp & Rutowski, 2007).Therefore, orchids that produce multiple deceptive sex sig-nals in chemical, visual and tactile modes could be extremelycompelling for their mate-searching potential pollinators.Since the attractiveness of an orchid appears to provide

fitness benefits in terms of increased pollination success(Fig. 3; Gaskett et al., 2008), there should be strong selectionfor multimodal signalling.

Multicomponent signals can enhance detection in signal-noisy environments, or assist in species and mate recognition(Partan & Marler, 1999; Candolin, 2003). Furthermore, eachsignal mode could convey different information about theemitter (Candolin, 2003). For orchids, scent and colour mightadvertise the orchid’s location, whilst the size of the orchidmight suggest a female of high fecundity and mate quality.Alternatively, each mode could elicit a different part of thereceiver’s response (Kullenberg, 1961). For orchids, scentmight attract over long distance, while shape and texturecause precise orientation on the orchid, and stimulate copu-lation. A third explanation, the backup hypothesis, suggeststhat each component reiterates or reinforces the same mes-sage (Partan & Marler, 1999; Candolin, 2003; Papke et al.,2007). However, behavioural tests with Ophrys arachnitiformis

show that for this species, scent alone is sufficient for polli-nator attraction, and that there is no signal reinforcementbetween the scent and the natural green or white floral orna-ments (Vereecken & Schiestl, 2009). Other candidates formulti-signal manipulation are colourful and morphologicallyornate species for which the attractive scents are well studied,e.g. Ophrys exaltata (Mant et al., 2005b; Vereecken & Schiestl,2008), Ophrys fusca (Ascensao et al., 2005; Stokl et al., 2005),Ophrys iricolor (Stokl et al., 2007), and Ophrys sphegodes (Schiestlet al., 1999; Ayasse et al., 2000).

The functions and evolution of multiple signals can also bestudied by applying molecular data from model systems suchas Arabidopsis and Antirrhinum to orchids (Schluter & Schiestl,2008; Mondragon-Palomino & Theißen, 2009). The pollina-tor perspective could be incorporated by applying moleculardata on the expression of insect sexual behaviour, odor-ant receptor genes, the functions and pathways of olfactoryreceptor neurons, and signal processing in the brain (e.g.Fitzpatrick et al., 2005; Rutzler & Zwiebel, 2005; Bargmann,2006; Hallem, Dahanukar & Carlson, 2006). There is alsoconsiderable existing data on the molecular basis of insectcolour perception (e.g. the genes coding for visual pigmentssuch as opsin) which could be applied to the study of decep-tive orchid colouration (Briscoe & Chittka, 2001; Kelberet al., 2003; Spaethe & Briscoe, 2004).

VII. POLLINATOR LEARNING

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



deception. Unlike the pollinators of rewarding, nectariferousflowers (Chittka, Thomson & Waser, 1999), sexually deceivedpollinators generally depart quickly and rarely visit multi-ple neighbouring orchids (Peakall, 1990; Peakall & Beattie,1996; Peakall & Schiestl, 2004; but see Jones & Gray, 1974).Fieldworkers frequently report that when an orchid flower isartificially introduced into an area, pollinators arrive swiftly,even within a minute for some species, but the rate of insectattraction soon wanes, even when fresh orchids or real femaleinsects are subsequently placed in the same location (Peakall,1990; Bower, 1996; Bower & Brown, 1997; Alcock, 2000;Ayasse et al., 2000; Wong & Schiestl, 2002; Wong, Salzmann& Schiestl, 2004). This is not because pollinator chemore-ceptors have become desensitised or habituated to the orchidscent because if the orchids are moved a few metres, theytypically attract pollinators again (Bates, 1977; Stoutamire,1983; Peakall, 1990; Bower, 1996; Ayasse et al., 2000). In onestudy, the pollinators of Ophrys sphegodes quickly learnt orchidlocations and the scents of individual flowers, and avoidedthem when tested a few minutes later (Ayasse et al., 2000).

Post-deception aversion to orchids appears to involve twoforms of learning: spatial configuration, and recognition ofsignals or sensory information (Dukas, 2008). It is unknownhow long these memories are retained and whether variationin one or more of the signal modes impairs or assists inmemory acquisition. Another unknown component is theinfluence of positive and negative reinforcement, i.e. if priormatings with real female insects or orchids make a maleinsect more or less likely to mate with a female insect or visitan orchid in the future. Capacity for learning and memoryare heritable (Dukas, 2008), and this suggests several inter-esting hypotheses: is learned avoidance a specific response toorchid deception, or a regular behavioural response to anynegative experience, such as attempting to mate with a deador heterospecific female? Does learned avoidance improvepollinator fitness, and is this sufficient to drive selection at apopulation or species level? Are naıve insects outside orchidranges more likely to be fooled by an orchid than naıve insectsin populations in long-term contact with orchids? Experi-mental assays involving pollinator learning require naıve orcaptive-bred male insects to ensure no previous experiencewith orchids or real females. Almost all studies of sexualdeception employ wild-caught male insects, but Gogler et al.(2009) used commercial colonies of Bombus terrestris to lure andestablish laboratory colonies of parasitic Bombus vestalis (thepollinator of Sardinian Ophrys normanii and O. chestermanii) anda similar technique could be used for other parasitoids that actas pollinators for sexually deceptive orchids. There are fewexperimental tests of learning in sexually deceived pollinatorsso this is likely to be a very productive field for future research.

VIII. COSTS OF DECEPTION ANDORCHID-POLLINATOR COEVOLUTION

Sexually deceptive orchids generally exert little influence onthe evolution of their pollinators (Schiestl, 2005; Jersakova

et al., 2006a). Pollinators of sexually deceptive orchids receiveno benefits from orchid visits and in most cases orchids arealso unlikely to impose any costs on their pollinator species.Costs to the pollinator species are unlikely because not allinsects that encounter an orchid are fooled into acting aspollinators (Table 3) and orchids are often rare or flowersporadically, and do not grow in all areas in which their pol-linating species is found (Kindlemann & Balounova, 2001;Peakall et al., 2002; Bower & Brown, 2009). Therefore manyinsects from a pollinating species may never or only rarelyencounter a sexually deceptive orchid. In this situation, atspecies level the fitness benefits of responding swiftly to sexualsignals and securing many matings with real females may out-weigh the disadvantages of occasional matings with orchids.

However, mating with orchids may have negative impactsfor individual pollinators. Pollinators can prefer orchids toreal females, prematurely end a copulation with a real femaleto visit an orchid, or be unable to find real female matesamong false orchid signals (Coate, 1965; Wong & Schiestl,2002; Schiestl, 2004; Vereecken & Schiestl, 2008). If sexualdeception involves pollinator ejaculation and sperm wastage,it may even affect a male’s future mating opportunities.Sperm production can be costly in many insect species,limiting lifetime sperm production (Wedell, Gage & Parker,2002). Even if sperm production is not costly, a male couldbecome temporarily sperm depleted during an orchid visit. Ifhe then soon encounters a real female, he may not be able tocopulate, or may transfer only seminal fluid without sperm,as occurs in many solitary wasp species (King, 1987; Damiens& Boivin, 2006). Although currently considered extremelyrare and proposed only for Cryptostylis and Lepanthes species(Blanco & Barboza, 2005; Gaskett et al., 2008), pollinatorejaculation has been studied in so few species that it may bemore common than currently believed.

Learned avoidance by pollinators after visiting sexuallydeceptive orchids is well documented and could be anevolved response to the costs imposed by the deception(Peakall, 1990; Bower, 1996; Bower & Brown, 1997; Alcock,2000; Ayasse et al., 2000; Wong & Schiestl, 2002; Wong et al.,2004). If the costs of deception are strong enough to selectfor pollinator avoidance of orchids, this in turn could selectfor increasingly sophisticated and persuasive orchid signals,ie. antagonistic coevolution or an arms race (Wong & Schi-estl, 2002; Gaskett et al., 2008). However, there are currentlyno data indicating whether these costs actually do impedepollinator fitness sufficiently to drive coevolution and a largestudy addressing pollinator mating behaviour and sperm useand exploring the potential for individual and populationcosts of exploitation by orchids is required.

At present, it is apparent that pollinators and theirbehaviours, mating systems, diversity, and sensory percep-tion could exert considerable selection on sexually deceptiveorchids and their signals. If sexual deception does negativelyimpact the mating opportunities of individual pollinators,there is no experimental evidence to show this is adequate toimpose selection on pollinators at the level of population or


70 A. C. Gaskett

species. Thus, antagonistic coevolution remains a tantalisinghypothesis for future research.

IX. FUTURE DIRECTIONS

(a) Fundamental natural history observations of pollinatoridentity and sexual behaviour with poorly knownorchids are crucial for conservation and knowledge.This is especially so for highly endemic and diverseorchid regions such as Australia and Central and SouthAmerica, contentious taxa (e.g. Cymbidium pumilum andPterostylis), and species that may combine aspects ofboth sexual and food deception (e.g. Orchis galilaea andCaladenia patersonii).

(b) Investigating pollinator mating systems and theconsequences of haplodiploidy and indirect selectionoffers new frameworks for researching sexualdeception, and more generally, hymenopteranevolution and behavioural ecology.

(c) Future studies involving gas chromatography-electroantennography (GC-EAG or GC-EAD) can beenhanced by reporting factors such as the numberof trials, number of unresponsive antennae, and themagnitude of responses observed, and consideringwhether these factors vary consistently with pollinatormating systems or behaviours.

(d) Although more studies of colour mimicry insexual deception are desirable, investigating howorchids exploit pollinator visual biases and employsensory traps would make a more widely applicablecontribution to the field of deceptive signalling.

(e) Investigation of floral shape provides many new orunder-studied opportunities for research: mimicry,exploitation of sensory biases, the effect of shapevariation on pollinator learning, and the evolutionof floral trap morphology.

(f) Current molecular studies of orchid signal expressioncould be accompanied by research into the geneticfactors influencing pollinator perception of signals (e.g.olfactory receptors and visual pigments) and pollinatorlearning and memory.

(g) Future topics to address in pollinator learning includethe temporal longevity of memory, the functions ofmultiple signal modes, and the influence of positiveand negative reinforcement.

(h) Costs imposed on pollinators by deception remainunquantified and evidence for antagonistic coevolutionbetween orchids and their deceived pollinators meritsconsiderable attention.

X. CONCLUSIONS

(1) At present, sexually deceptive orchid genera havebeen identified in Australia and New Zealand

(Arthrochilus, Caladenia, Caleana, Calochilus, Chiloglottis,Cryptostylis, Drakaea, Leporella, Paracaleana, Spiculaea andpotentially Pterostylis), Europe (Ophrys, Orchis), SouthAfrica (Disa), Central and South America (Geoblasta,Lepanthes, Mormolyca, Stellilabium, Telipogon, Trichoceros,Trigonidium and potentially Tolumnia), and potentiallyJapan (Cymbidium pumilum).

(2) Sexually deceptive orchids are pollinated only bymale insects, which are typically from species thatare solitary rather than social and are haplodiploid,monandrous, and polygynous.

(3) There is considerable diversity in the behaviour ofsexually deceived pollinators among different orchidspecies, and among different individuals of the pollina-tor species. Generally, pollination involves copulationor simple gripping of the orchid. Ejaculation is rare.In some cases, pollinators are trapped briefly.

(4) Orchid speciation may be facilitated by high insectdiversity if this fuels pollinator shifts and provides newpollinators for hybrids and mutants.

(5) A literature survey reveals that for sexually deceptiveorchids, an average of 20.5 ± 14.7% of all flowers(mean ± S.D.; N = 35 species), or alternatively, 37.5± 20.9% of plants (N = 11 species) had pollinia col-lected and deposited, or set fruit. Pollination rates perflower are similar in Europe (18.4% ± 17.4, N = 8)and temperate Australia (18.4 ± 11.4%, N = 21).

(6) Although scent mimicry is increasingly well studied,visual and tactile mimicry require further atten-tion, with emphasis on pollinator perception andexperimental manipulations involving multiple sen-sory modes. Alternative deceptive interactions such asexploitation of pollinator sensory biases are also likely.

(7) Observations suggest that pollinators commonlyexhibit learned avoidance of orchids or orchid loca-tions.

(8) Generally, even if orchids impose minor costs onindividual pollinators, these may be insufficient todrive selection at a population or species level. Rareexamples of sexual deception provoking pollinatorejaculation may exert considerable costs on the polli-nator, but this is yet to be demonstrated empirically.

XI. ACKNOWLEDGEMENTS

I thank Marie Herberstein and Andy Beattie (MacquarieUniversity), Greg Holwell (University of Auckland) andanonymous referees for their constructive, thorough, andthoughtful comments on the manuscript. Colin Bower(FloraSearch), Graham Brown (Museum and Art Galleryof the Northern Territory), Stephen Hopper (RoyalBotanic Gardens, Kew) and Eric Scanlen and Ian StGeorge (New Zealand Native Orchid Group) providedadvice and unpublished data for the list of pollinators inTable 1. Most photographs were kindly provided by JuliaCooke (Macquarie University). This work was generously



supported by a Furniss Foundation/American OrchidSociety Fellowship.

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