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
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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
sw
ithor
chid
,3=
polli
nato
rgr
ips
orlif
tshi
nged
labe
llum
,4=
polli
nato
ris
brie
flytr
appe
dan
dtr
ansf
ers
polli
nia
ones
cape
,unc
onf.
=po
llina
tion
islik
ely
toin
volv
ese
xual
beha
viou
r,bu
tthi
sis
unco
nfirm
ed.%
flow
ers
polli
nate
dis
the
perc
enta
geof
flow
ers
that
had
polli
nia
colle
cted
and
depo
site
d,or
setf
ruit.
%pl
ants
polli
nate
dis
the
perc
enta
geof
flow
erin
gpl
ants
that
had
polli
nia
colle
cted
and
depo
site
d,or
setf
ruit.
(N)=
num
ber
offlo
wer
sor
plan
tsre
port
edin
that
stud
y.Po
llina
tion
rate
sla
belle
dw
ithm
ore
than
one
sym
bola
reth
eav
erag
eof
data
from
the
corr
espo
ndin
gly
labe
lled
sour
ce.A
ustr
alia
nor
chid
spec
ies
nam
esar
efr
omth
eA
ustr
alia
nPl
ant
Nam
esIn
dex
(Cen
tre
for
Plan
tB
iodi
vers
ityR
esea
rch,
2008
)and
Jone
s(2
006)
.Eur
opea
nor
chid
spec
ies
nam
esar
eac
cord
ing
toth
eIn
tern
atio
nalP
lant
Nam
esIn
dex
(200
8)an
dD
elfo
rge
(200
5).O
rchi
dfa
mili
esar
eac
cord
ing
tova
nde
rC
inge
l(20
01)a
ndK
ores
etal
.(20
01).
Eur
opea
npo
llina
tor
nam
esar
eac
cord
ing
toFa
una
Eur
opae
a(2
004)
Orc
hid
Gro
wth
form
Polli
nato
rPo
llina
tor
Fam
ily;O
rder
Polli
nato
rse
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viou
r%
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d(N
)%
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tspo
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ted
(N)
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dium
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ilum
Rol
feE
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sce
rana
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nica
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iciu
sA
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e;H
ymen
opte
raun
conf
.Sa
saki
etal
.(19
91)
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eae
Sou
thA
fric
aD
isa
atri
capi
lla
(Har
v.ex
Lin
dl.)
TPr
imar
ilyP
odal
onia
cane
scen
s(D
ahlb
om)
Sphe
cida
e;H
ymen
opte
ra2
36.4
(550
on18
4pl
ants
)St
eine
ret
al.(
1994
)
Dis
abi
valv
ata
(L.f
.)T
.Dur
and
&Sc
hinz
.T
Hem
ipep
sis
hila
ris
Sm.,
H.ca
pens
isFa
bric
ius
Pom
pilid
ae;
Hym
enop
tera
242
.1(4
82on
116
plan
ts)
Stei
ner
etal
.(19
94)
Diu
rid
eae
Au
stra
lia
Art
hroc
hilu
shu
ntia
nus
(F.M
uell.
)Bla
xell
subs
p.hu
ntia
nus
(pre
v.Spi
cula
eahu
ntia
na(F
.Mue
ll.)
Schl
tr.)
TA
rthr
othy
nnus
hunt
ianu
sB
row
n(n
otR
hagi
gast
ersp
.as
sugg
este
dby
Rot
herh
am,1
967)
Tip
hiid
ae;
Hym
enop
tera
3R
othe
rham
(196
7);B
ower
(200
1a,
f);
Man
tetal
.(20
05c)
Art
hroc
hilu
sir
rita
bilis
F.M
uell.
TA
rthr
othy
nnus
rufia
bdom
inal
isB
row
nT
iphi
idae
;H
ymen
opte
ra3
Bow
er(2
001a
)
Art
hroc
hilu
sla
tipe
sD
.L.J
ones
TA
rthr
othy
nnus
sp.
Tip
hiid
ae;
Hym
enop
tera
3B
ower
(200
1a)
Cal
aden
ia(sy
n.A
rach
norc
his)
amni
cola
D.L
.Jon
esT
Thy
nnoi
des
seni
lis
(Eri
chso
n)T
iphi
idae
;H
ymen
opte
ra3
Phill
ips
etal
.(20
09a)
Cal
aden
iaam
pla
(D.L
.Jon
es)
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.A
rach
norc
his)
aren
icol
aH
oppe
r&
A.P
.Br.
TZ
aspi
loth
ynnu
sni
grip
esG
ueri
nT
iphi
idae
;H
ymen
opte
ra3
9.9∗
Bro
wn
etal
.(19
97);
Phill
ips
etal
.(2
009a
)*
Cal
aden
ia(sy
n.A
rach
norc
his)
atro
vesp
aD
.L.J
ones
TT
hynn
oide
sgr
acilis
(Wes
twoo
d)T
iphi
idae
;H
ymen
opte
ra3
Phill
ips
etal
.(20
09a)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 37
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
)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 39
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 41
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
)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 43
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 45
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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)†
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 47
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 49
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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)†
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 51
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 53
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 55
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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)
‡
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 57
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 59
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
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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).
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 61
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 63
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)
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
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).
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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
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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
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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.
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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
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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
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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
Biological Reviews 86 (2011) 33–75 © 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society
Orchid pollination by sexual deception 71
supported by a Furniss Foundation/American OrchidSociety Fellowship.
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