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Observations on the pollination of Ophrys fuciflora by pseudo- copulating males of Phyllopertha horticola in northern France

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Tyteca, D., Róis, A.S. & N.J. Vereecken (2006): Observations on the pollination of Ophrys fuciflora by pseudocopulating males of Phyllopertha horticola in northern France.-Jour. Eur. Orch. 38 (1): 203-214. Males of the coleopteran Phyllopertha horticola (L.) (Coleoptera, Scarabaeidae) have been observed pseudocopulating on Ophrys fuciflora (F.W. Schmidt) Moench (Orchidaceae) labella in a population from the Paris Tertiary Basin. Although these uncommon pollen vectors are not recognised as the most effective insect species in the pollination process, the males appeared to perform effective cross-pollination in both cephalic and abdominal positions. A somewhat erratic behaviour was noted as well, denoting high sexual excitation of males, during which they stretch their legs and squeeze the labellum. A discussion on the relativity of cephalic vs. abdominal position adopted in pseudocopulation among the various Ophrys species is also proposed. Zusammenfassung Tyteca, D., Róis, A.S. & N.J. Vereecken (2006): Observations on the pollination of Ophrys fuciflora by pseudocopulating males of Phyllopertha horticola in northern France.-Jour. Eur. Orch. 38 (1): 203-214. Männchen des Käfers Phyllopertha horticola (L.) (Coleoptera, Scarabaeidae) konnten bei Pseudokopulationen auf Lippen der Blüten von Ophrys fuciflora (F.W. Schmidt) Moench (Orchidaceae) im Gebiet des Pariser Tertiärbeckens beobachtet werden. Obwohl diese ungewöhnlichen Überträger von Pollen nicht als besonders effektive Bestäuber-Insekten angesehen werden, erwiesen sich
Journal Europäischer Orchideen 38(1):2006.203
Jour. Eur. Orch.
38 (1): 203 – 214. 2006.
Daniel Tyteca, Ana Sofia Róis and Nicolas J. Vereecken
Observations on the pollination of Ophrys fuciflora by pseudo-
copulating males of Phyllopertha horticola in northern France
Keywords
Orchidaceae; Ophrys fuciflora; Coleoptera; Phyllopertha horticola;
Pseudocopulation; Pollination; Sexual deceit.
Summary
Tyteca, D., Róis,A.S. & N.J. Vereecken (2006): Observations on the
pollination of Ophrys fuciflora by pseudocopulating males of Phyllopertha
horticola in northern France.-Jour. Eur. Orch. 38 (1): 203-214.
Males of the coleopteran Phyllopertha horticola (L.) (Coleoptera,
Scarabaeidae)have been observed pseudocopulating on Ophrys fuciflora (F.W.
Schmidt) Moench (Orchidaceae)labella in a population from the Paris Tertiary
Basin. Although these uncommon pollen vectors are not recognised as the most
effective insect species in the pollination process, the males appeared to
perform effective cross-pollination in both cephalic and abdominal positions. A
somewhat erratic behaviour was noted as well, denoting high sexual excitation
of males, during which they stretch their legs and squeeze the labellum. A
discussion on the relativity of cephalic vs. abdominal position adopted in
pseudocopulation among the various Ophrys species is also proposed.
Zusammenfassung
Tyteca, D., Róis,A.S. & N.J. Vereecken (2006): Observations on the
pollination of Ophrys fuciflora by pseudocopulating males of Phyllopertha
horticola in northern France.-Jour. Eur. Orch. 38 (1): 203-214.
Männchen des Käfers Phyllopertha horticola (L.) (Coleoptera, Scarabaeidae)
konnten bei Pseudokopulationen auf Lippen der Blüten von Ophrys fuciflora
(F.W. Schmidt) Moench (Orchidaceae) im Gebiet des Pariser Tertiärbeckens
beobachtet werden. Obwohl diese ungewöhnlichen Überträger von Pollen nicht
als besonders effektive Bestäuber-Insekten angesehen werden, erwiesen sich
204 Journal Europäischer Orchideen 38(1):2006.
diese Käfermännchen als wirksame Kreuzbestäuber sowohl in Kopf-als auch
Abdomenposition. Während Phasen hoher sexueller Erregung bewegten sich die
Männchen unregelmäßig auf der Lippe hin und her, streckten dabei ihre Beine
aus,umklammerten die Lippe und drückten sie so zusammen, daß diese
anschließend deutlich erkennbare Beschädigungen aufwies. Das Verhältnis von
Kopf-zu Abdomenpollination durch Pseudokopulationen auf den verschiedenen
Ophrys-Arten wird diskutiert.
Résumé
Tyteca, D., Róis,A.S. & N.J. Vereecken (2006): Observations sur la
pollinisation d’Ophrys fuciflora par pseudocopulation de mâles de
Phyllopertha horticola dans le nord de la France. .- Jour. Eur. Orch. 38 (x):
203-214.
Des mâles du coléoptère Phyllopertha horticola (L.) (Coleoptera,
Scarabaeidae) ont été observés en pseudocopulation sur des labelles d’Ophrys
fuciflora (F.W. Schmidt) Moench (Orchidaceae) dans une population du
Bassin Tertiaire Parisien. Bien que ces vecteurs inhabituels ne soient pas
reconnus comme l’espèce d’insecte la plus efficace dans le processus de
pollinisation, on a pu noter que celle-ci a été réalisée adéquatement, dans
chacune des deux positions céphalique et abdominale. Un comportement
quelque peu erratique a été également remarqué, traduisant une forte excitation
sexuelle des mâles, au cours duquel ceux-ci étirent leurs pattes et compriment le
labelle. On propose également une discussion sur la relativité de la position
céphalique ou abdominale adoptée lors de la pseudocopulation parmi les
différentes espèces d’Ophrys.
***
Introduction
The genus Ophrys L. is well known for its pollination mechanism through the
sexual deceit of male insects (e.g., KULLENBERG 1961; PAULUS & GACK 1990;
SCHIESTL et al. 1999; SCHIESTL 2005). Pollinator attraction in Ophrys is often
species-specific (i.e. each Ophrys species being pollinated by one or a few
insect species) and is mostly mediated by the emission of specific blends of
chemical compounds that mimic the female sex pheromones of insect species
(SCHIESTL et al. 1999, 2000; AYASSE et al. 2000, 2003; MANT et al. 2005).
Small deviations from a given compound mixture may, under certain
circumstances, promote the attraction of another insect species and through this,
Journal Europäischer Orchideen 38(1):2006.205
constitute an effective factor of sympatric speciation through pollinator shifts
(SCHIESTL & AYASSE 2002). This explains that the phenotypic variability among
and within Ophrys species is quite important, as witnessed by the ca. 250
morphospecies described over the genus distribution range (DELFORGE 2005).
Within the family Orchidaceae, the monophyletic genus Ophrys has been
traditionally divided into two sister sections, Pseudophrys and Euophrys (or
Ophrys sensu stricto), based on the position of the insect on the flower labellum
during pseudocopulation. Recent studies using molecular markers have provided
evidence for the paraphyly of the section Euophrys (cephalic
pseudocopulation), while confirming the monophyletic origin of the section
Pseudophrys (abdominal pseudocopulation) (SOLIVA et al. 2001; BATEMAN et
al. 2003; S. Vandewoestijne, pers. comm. 2005). This implies that the
plesiomorphic pollination mechanism in Ophrys would be through cephalic
position of the pollinator, the abdominal position being a derived condition (i.e.,
apomorphy)that appeared in a subgroup of Ophrys, namely the Pseudophrys.
This in turn calls for a revision of Ophrys systematics, as was already suggested
in some recent monographies (e.g., ALDASORO & SÁEZ 2005).
Although male hymenopterans are the most likely pollinators of Ophrys, other
insects are known to bring about pollination through the same process of sexual
deceit. Among these are dipterans and coleopterans, such as male scarabaeid
beetles (Phyllopertha horticola, Blithopertha lineolata, Hoplia farinosa) and
male hoverflies (Microdon mutabilis, M. latifrons, Merodon velox) (PAULUS
2005; REINHARD et al. 1991).
In this paper we report on observations on the pollination of Ophrys fuciflora
by pseudocopulating males of Phyllopertha horticola in a population from
northern France.
Observations
In the scope of a field research on the reproductive success of Ophrys species
(RÓIS et al. 2006), two of us (DT and ASR) have observed, at length, males of
Phyllopertha horticola pseudocopulating on flowers of Ophrys fuciflora, in a
population from the neighbourhood of the city of Laon, in northern France, on a
calcarous grassland at the border of the Paris Tertiary Basin. Some
characteristics of the population are given in Table 1.
Table 1: Characteristics of the population investigated.
206 Journal Europäischer Orchideen 38(1):2006.
Locality name,
municipality, department Saint-Thomas, Camp des Romains,
Ste-Erme Outre – et – Ramecourt, Aisne
Altitude 190 m
Slope, exposition 20°, S
Surface area ± 5 hectares
Status Private property, with management contract towards
conservation
Dates of observations 16th and 28th of May 2005
Biotope Open, pastured chalk grassland, with various orchids
Overview of
accompanying flora Euphorbia cyparissias, E. seguieriana, Globularia
bisnagarica, Blackstonia perfoliata, Linum
tenuifolium, L. catharticum, Orobanche sp., Briza
media,
Accompanying orchids Orchis purpurea, O. ustulata, Platanthera
chlorantha, Ophrys sphegodes, O. insectifera, O.
apifera, Gymnadenia conopsea, Himantoglossum
hircinum, Anacamptis pyramidalis, Epipactis
atrorubens
Number of O. fuciflora
individuals ± 150
At least three specimens of P. horticola were observed on the 16th of May 2005
and one more on the 28th of May 2005. The behaviour could be extensively
watched and several pictures have been taken, some of which are reproduced
herein (Figs. 1-4). Obvious sexual excitation was taking place and the male
insects were performing all kinds of strong disordered movements on the lips,
sometimes squeezing the latter and stretching their legs in such a way that after
pseudocopulation, the lips looked damaged, with cracks and scratches
witnessing extremely excited behaviour.
The males were seen in the “usual” (in the sense of the Euophrys section, see
above) cephalic position (Fig. 1), but much more astonishing, they were also
observed performing pollen transfer in the abdominal position (Figs. 2-4). In this
position as well as in the cephalic position, pollination appeared to be effective,
as shown by the succession of Figs. 2 to 4. Fig. 2 shows the insect in quite an
excited posture, Fig. 3 depicts the abdominal pseudo-copulation, while Fig. 4
shows the result with a pollinium stuck to the stigma of the Ophrys. Thus, not
only Phyllopertha horticola males could be corroborated as “confirmed
pollinators” of Ophrys fuciflora (sensu COX & KNOX 1986), but effective
pollination was also performed in both cephalic and abdominal positions.
Journal Europäischer Orchideen 38(1):2006.207
Discussion
As mentioned above, coleopterans can act as well as hymenopterans as Ophrys
pollinators, through the same process of pseudocopulation. It was shown
(BORG-KARLSON 1989) that the chemical compounds emitted by species from
the O. fuciflora (as well as O. tenthredinifera) complex trigger the same kind of
sexual attraction to Phyllopertha horticola males as to male hymenopterans.
Although the movements of the insects on the lip appear more erratic than what
is usually observed with hymenopterans, pseudocopulation appears to be
effective. Seemingly erratic movements were also observed with other insect
species, even hymenopterans, as is the case, e.g., for Sterictiphora furcata on
O. subinsectifera (HERMOSILLA et al. 1999; J.E. Arnold pers. comm.. 2005).
Phyllopertha horticola males have already been reported as visitorsand/or
pollinators of O. fuciflora, at least by PAULUS & GACK (1990, “in Central
Europe”), REINHARD et al. (1991), VAN DER CINGEL (1995), DUSAK & PERNOT
(2002), SOUCHE (2004), PAULUS (2005) and in BOURNÉRIAS (1998; observation
by R. ENGEL), but are not recognised as such by DELFORGE (2005). PAULUS &
GACK (1990) indicate this process as “less significant” with respect to
pollination efficiency. However, from our observation on only a few individuals,
we have notedthat pollinia had been taken up effectively and in the right
position (either on the head or on the tip of the abdomen Figs. 1-3), and
thereafter deposited on the stigma, in the “expected” way (from the abdominal
position Fig. 4). Although the global fecundation success of O. fuciflora was
found to be rather low in the population investigated compared to other
populations under study (RÓIS et al. 2006), the efficiency of the pollination
brought about by Phyllopertha horticola males could be demonstrated in spite
of the few pseudocopulations observed. In this location, we have not reported
any visit by the most frequently recognised pollinators of O. fuciflora, namely
male hymenopterans belonging to the genus Eucera (Anthophoridae)
(KULLENBERG et al. 1984).
In O. fuciflora, the sharing of confirmedpollinators belonging to distinct
insect orders (here, Coleoptera versus Hymenoptera) also raises the question of
sex pheromone similarity emitted by females of each pollinator species. Recent
studies on the chemical chemistry of the floral odour of Ophrys have provided
evidence for the qualitative (i.e. classes of odour compounds) and quantitative
(i.e. different ratios, yet identical chemicals) complexity of odour blends emitted
by individual flowers (see e.g. SCHIESTL et al. 1999; AYASSE et al. 2003; MANT
208 Journal Europäischer Orchideen 38(1):2006.
et al. 2005; SCHIESTL 2005 and references therein). This phenomenon may,
even within a given population, allow Ophrys flowers to be pollinated by males
belonging to distinct insect species if the set of floral biochemicals that triggers
sexual arousal in male insects differs from one species to another.Such a
scenario would also account for the distinct (yet closely-related) Andrena
species that have been shown to pollinate flowers of O. sphegodes in the same
region, namely Eastern France (see LORELLA et al. 2002). Consequently, we
hypothesize that Eucera females may emit a sex pheromone blend differing
from that of Phyllopertha horticola females, thereby preventing unsuccessful
interspecific mating attempts by the patrolling males of each species. Flowers of
O. fuciflora, on the other hand, may emit both classes of key odour compounds
for mate attraction, resulting in cross-attractiveness of the floral odour to each
pollinator species.
Further reports should be made on the behaviour of Phyllopertha horticola
males on the flower labellum of O. fuciflora. Although there was obvious sexual
excitation, with genitalia in extension (Fig. 2), there also tended to be some
“aggressive” attitude. Such a behaviour lasted quite a while, during which the
male stretched his legs and squeezed the lip, as if it were attempting to seize it
and expel it from the flower, which resulted in significant damage of the lip
(Fig. 4). Although cases of aggressive behaviour, in which males attempt to
extirpate “putative” male rivals from the flowers, have been noted for some
Ophrys species (O. regis-ferdinandii, O. grigoriana: PAULUS 2005), the
explanation of the behaviour of Phyllopertha horticola males is most likely to
be sought in sexual arousal.
A last comment will focus on the position adopted in the pseudocopulation
process. Ophrys fuciflora obviously belongs to the so-called Euophrys section,
where in principle only cephalic pseudocopulation takes place. Here however,
both cephalic and abdominal positions were observed and noted as effective,
although pollination effectiveness is often put into doubt, as e.g. by DUSAK &
PERNOT (2002) who illustrated abdominal uptake of O. fuciflora pollinia by
Phyllopertha. Whereas this is far from being frequent, alternative
pseudocopulatory positions have also been observed in pollinators of other
Ophrys species, also belonging to the Euophrys, such as is the case for O.
subinsectifera, visited by males of Sterictiphora furcata (Hymenoptera,
Argidae). In that process, the male insect gets the pollinia attached to its legs
after seemingly disordered movements on the lip and the flower, resulting,
however, in effective pollination of the flowers (J.E. Arnold, pers. comm.
2005). In conclusion we can note that the position of male insects on Ophrys
flowers may not be as clear-cut as usually indicated, which might tend to
Journal Europäischer Orchideen 38(1):2006.209
challenge somewhat the traditional distinction based solely on the position
during pseudocopulation; and indeed, hybrids between representatives of the
two commonly recognized Ophrys sections are not rare (e.g., DANESCH 1972;
TYTECA 1997; KRETZSCHMAR et al. 2002).
Acknowledgements
We gratefully acknowledge fruitful discussions with several colleagues, among
which Ana Caperta (Universidade Lusófona de Humanidades e Tecnologias,
and Insituto Superior de Agronomia, Lisboa) who initiated this collaboration
between two of us (DT and ASR), as well as Sofie Vandewoestijne and Michel
Baguette (Unit of Ecology and Biogeography, Université catholique de Louvain,
Louvain-la-Neuve). Thanks are due to J.E. Arnold (Manresa, Spain) for sharing
his observations with one of us (NJV).
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Figures (Colour table pag. 213)
2 4
1 3
Figs. 1-4. Pseudocopulation and other postures of Phyllopertha horticola
males on flowers of Ophrys fuciflora, St-Thomas (Aisne, France), 16 May
2005 (digital pictures D. Tyteca).
Fig. 1: Male removing pollinia in cephalic position.
Fig. 2: Male with a pollinium on its head, standing in lateral abdominal
position, with stretched legs and erected genitalia.
Fig. 3: Male pseudocopulating in abdominal position.
Fig. 4: Same as Fig. 3, after deposition of one pollinium on the stigma.
Journal Europäischer Orchideen 38(1):2006.213
214 Journal Europäischer Orchideen 38(1):2006.
Authors
Daniel Tyteca
Centre de recherche sur la Biodiversité
Unité d’Ecologie et de Biogéographie
Université catholique de Louvain
Place Croix du Sud, 4
B-1348 Louvain-la-Neuve (Belgium)
tyteca@ecol.ucl.ac.be
(corresponding author)
Ana Sofia Róis
Universidada Lusófona de Humanidades e Tecnologias
Av. do Campo Grande, 376
P-1749 - 024 Lisboa (Portugal)
rois.ana@gmail.com
Nicolas J. Vereecken
Behavioural and Evolutionary Ecology
Université Libre de Bruxelles
CP 160/12
Av. F.D. Roosevelt, 50
B-1050 Brussels (Belgium)
nicolas.vereecken@ulb.ac.be
... The latter is also occasionally pollinated by Coleopterans, e.g. Phyllopertha horticola (Tyteca et al. 2006). Although pollination events by species other than Hymenopterans are observed, they remain rare and are not likely to have any evolutionary significance (Paulus 2006). ...
... Only seven pseudocopulatory events by pollinating insects, in 2784 flowers from the 581 surveyed Ophrys Vandewoestijne, Ró is, Caperta, Baguette & Tyteca Effects of individual and population parameters on orchid reproduction plants, were observed during the 2005 field season. Three of these pseudocopulations were performed by Hymenopterans (two Argogorytes mystaceus on O. insectifera and one Eucera sp. on O. fuciflora), and the remaining four by a Coleopteran, namely Phyllopertha horticola on O. fuciflora (Tyteca et al. 2006). No pseudocopulatory events were observed during the 2006 field season (3664 flowers from 700 plants). ...
Article
Reproductive success (RS) in orchids in general, and in non-rewarding species specifically, is extremely low. RS is pollinator and pollination limited in food deceptive orchids, but this has rarely been studied in sexually deceptive orchid species. Here, we tested the effects of several individual (plant height, inflorescence size, nearest neighbour distance and flower position) and population (patch geometry, population density and size) parameters on RS in three sexually deceptive Ophrys (Orchidaceae) species. Inter-specific differences were observed in RS of flowers situated in the upper versus the lower part of the inflorescence, likely due to species-specific pollinator behaviour. For all three species examined, RS increased with increasing plant height, inflorescence size and nearest neighbour distance. RS generally increased with decreasing population density and increasing patch elongation. Given these results, we postulate that pollinator availability, rather than pollinator learning, is the most limiting factor in successful reproduction for sexually deceptive orchids. Our results also suggest that olfactory 'display' (i.e. versus optical display), in terms of inflorescence size (and co-varying plant height), plays a key role in individual RS of sexually deceptive orchids. In this regard, several hypotheses are suggested and discussed.
... 1C) near Sydney and n p 43 Melbourne, Australia, and recorded the percentage of flowering plants in which both pollen was removed and fruit capsules were formed. We also surveyed the literature for data on pollination rates, pollinator behavior, and pollinator identity for Cryptostylis and other sexually deceptive orchids worldwide (Wolff 1950; Bino et al. 1982; Stoutamire 1983; Peakall 1989 Peakall , 1990; Paulus and Gack 1990; Peakall and Handel 1993; Steiner et al. 1994; Bernhardt 1995; Peakall and Beattie 1996; Ayasse et al. 1997; Neiland and Wilcock 1998; Taylor 1999; Alcock 2000; Singer 2002; Wong and Schiestl 2002; Hopper and Brown 2004; Schiestl 2004; Schiestl et al. 2004; Singer et al. 2004; Blanco and Barboza 2005; Delforge 2005; Lehnebach et al. 2005; Mant et al. 2005b; Vereecken and Patiny 2005; Bower 2006; Ciotek et al. 2006; Dickson and Petit 2006; Gaskett and Herberstein 2006; Tyteca et al. 2006). ...
... Six out of 222 orchid species are pollinated by social ants or bees: Ophrys chestermanii, Ophrys normanii, Orchis galilea, Trigonidium obtusum, Leporella fimbriata, and Mormolyca ringens (Bino et al. 1982; Peakall 1989; Singer 2002; Singer et al. 2004; Delforge 2005). Diploid beetles pollinate Ophrys blitopertha and visit Ophrys fuciflora, but pollination in the latter is primarily by other haplodiploid solitary Hymenoptera (Paulus and Gack 1990; Delforge 2005; Tyteca et al. 2006). Diploid dipterans pollinate Pterostylis spp. ...
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... Other observations are more surprising: 1) The beetle Oedemera podagrariae was observed pollinating O. philippi. Although other beetles have been reported to visit and pollinate Ophrys plants, such as Blitopertha majuscula for O. urteae (Paulus 2018), Blitopertha lineolata for O. blithopertha (Paulus 2007) or Phyllopertha horticola for O. fuciflora (Tyteca et al. 2006;Paulus 2007), it is unclear whether those represent true cases of sexual deception or whether another mechanism causes pollinator attraction in these systems. 2) The bumblebee Bombus terrestris xanthopus was observed pollinating O. bombyliflora; it is the second bumblebee species observed pollinating Ophrys plants only (Gögler et al. 2009(Gögler et al. , 2011(Gögler et al. , 2015. ...
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... Since Pouyanne's milestone contributions to the field, pollination by sexual deceit has been further confirmed and reported from independent orchid lineages and on different continents, with extant representatives found across Australia (10 genera; Coleman 1928; Stoutamire 1975; Peakall et al. 1987; Jones 1988; Peakall 1990; Bower 1996), Central and South America (7 genera; van der Pijl and Dodson 1966; Dod 1976; Singer 2002; Singer et al. 2004; Blanco and Barboza 2005; Ciotek et al. 2006), South Africa (genus Disa Bergius (Orchidaceae); Steiner et al. 1994), and Europe (Delforge 2005; Schiestl 2005; Ayasse 2006; Jersáková et al. 2006). In all cases described so far, patrolling male insects (mostly solitary bees, but also solitary wasps and occasionally beetles; see Tyteca et al. 2006) attempt copulation, a phenomenon also termed ''pseudocopulation'', or a precopulatory courtship with the orchid flowers. The male insects sometimes display high levels of sexual stimulation on the flowers, erecting their genital capsule during convulsive movements, and rubbing it against areas on the flower lip where the density of hairs presumably adds to the initial olfactory stimulation (Agren et al. 1984 ; N.J. ...
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... Not only that, but a great number of these orchids also have wide geographic range across which no pollinator record is available. Consequently, two parasitic orchids might each have a single pollinator host, but detailed investigations across their geographic ranges and over the years sometimes reveal that these orchids are instead exploiting a broader range of insect hosts (see, e.g., Lorella et al. 2002 ; Tyteca et al. 2006 ; Vereecken and Patiny 2006 ; Bower 2006 ; Vereecken et al. 2007a) . The real range of hosts that can be exploited by a given parasite species is illustrated by Combes' (2001) " filters " concept (Fig. 4 ), which shows the mechanisms restricting the number of potential hosts. ...
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Sexually deceptive orchids attract male insects as pollinators by mimicking the reproductive signals emitted by the targeted females. Since this mimicry system involves the imitation of female mating signals of certain insects, and since mating signals, especially sex pheromones, generally act on a species-specific basis, theory holds that each sexually deceptive orchid is usually pollinated by only one or a few male insect species. While these orchids rely exclusively on their specialized pollinators for their own reproduction, the male insects derive no benefit from this interaction. In this chapter, I will argue that incorporating questions relevant to the field of animal-centered host–parasite interactions into investigations on the evolutionary ecology of orchid pollination by deception will provide important insights at both the proximate (or mechanistic) and at the ultimate (or evolutionary) levels.
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Internal transcribed spacer (ITS nuclear rDNA) data have been obtained from 190 terrestrial orchid species, encompassing all genera and the great majority of the widely recognized species of Orchidinae, a heterogeneous selection of species of Habenariinae, and single species of Satyriinae and Disinae (the latter serving as outgroup). The resulting parsimony-based phylogeny reveals 12 well-resolved clades within the Orchidinae, based on Anacamptis s.l., Serapias, Ophrys, Steveniella–Himantoglossum s.l. (including ‘Comperia’ and ‘Barlia’, most species being 2n = 36), Neotinea s.l., Traunsteinera–Chamorchis, Orchis s.s., Pseudorchis–Amerorchis–Galearis–Neolindleya–Platanthera s.l. (most 2n = 42), Dactylorhiza s.l., Gymnadenia s.l. (most 2n = 40, 80), Ponerorchis s.l.–Hemipilia s.l.–Amitostigma–Neottianthe, and Brachycorythis (most 2n = 42). Relationships are less clearly resolved among these 12 clades, as are those within Habenariinae; the subtribe appears either weakly supported as monophyletic or as paraphyletic under maximum parsimony, and the species-rich genus Habenaria is clearly highly polyphyletic. The triphyly of Orchis as previously delimited is confirmed, and the improved sampling allows further generic transfers to Anacamptis s.l. and Neotinea s.l. In addition, justifications are given for: (1) establishing Steveniella as the basally divergent member of an appreciably expanded Himantoglossum that incorporates the former genera ‘Barlia’ and ‘Comperia’, (2) reuniting ‘Piperia’ with a broadly defined Platanthera as section Piperia, necessitating ten new combinations, (3) broadening Ponerorchis to include Chusua, and Hemipilia to include single ‘orphan’ species of Ponerorchis and Habenaria, and (4) recognizing ‘Gymnadenia’camtschatica as the monotypic Neolindleya camtschatica within the Pseudorchis∼Platanthera clade. Few further generic transfers are likely in Orchidinae s.s., but they are anticipated among habenariid genera, on acquisition of additional morphological and molecular evidence; one probable outcome is expansion of Herminium. Species-level relationships are also satisfactorily resolved within most of the major clades of Orchidinae, with the notable exceptions of Serapias, the derived sections of Ophrys, Himantoglossum s.s., some sections within Dactylorhiza, the former genus ‘Nigritella’ (now tentatively placed within Gymnadenia s.l.), Hemipilia s.l., and possibly Ponerorchis s.s. Relationships among the 12 major clades broadly accord with bona fide records of intergeneric hybridization. Current evidence supports the recently recognized 2n = 36 clade; it also indicates a 2n = 40 clade that is further diagnosed by digitate root-tubers, and is derived relative to the recently recognized clade of exclusively Asian genera (Ponerorchis s.l.–Hemipilia s.l.–Amitostigma–Neottianthe). This in turn appears derived relative to the Afro-Asiatic Brachycorythis group; together, these two clades identify the plesiomorphic chromosome number as 2n = 42. If the African genus Stenogolottis is correctly placed as basally divergent within a monophyletic Habenariinae, the tribe Orchideae and subtribes Orchidinae and Habenariinae could all have originated in Africa, though in contrast the Asiatic focus of the basally divergent members of most major clades of Orchidinae suggests an Asiatic radiation of the subtribe. Morphological characters informally ‘mapped’ across the molecular phylogeny and showing appreciable levels of homoplasy include floral and vegetative pigmentation, flower shape, leaf posture, gynostemium features, and various pollinator attractants. Qualitative comparison of, and reciprocal illumination between, degrees of sequence and morphological divergence suggests a nested set of radiations of progressively decreasing phenotypic magnitude. Brief scenarios, both adaptive and non-adaptive, are outlined for specific evolutionary transitions. Recommendations are made for further species sampling, concentrating on Asian Orchidinae (together with the Afro-Asiatic Brachycorythis group) and both Asian and Southern Hemisphere Habenariinae, and adding plastid sequence data. Taxonomic changes listed are: Anacamptis robusta (T.Stephenson) R.M.Bateman, comb. nov., A. fragrans (Pollini) R.M.Bateman, comb. nov., A. picta (Loiseleur) R.M.Bateman, comb. nov., Neotinea commutata (Todari) R.M.Bateman, comb. nov., N. conica (Willdenow) R.M.Bateman, comb. nov., Platanthera elegans Lindley ssp. maritima (Rydberg) R.M.Bateman, comb. nov., P. elegans Lindley ssp. decurtata (R.Morgan & Glicenstein) R.M.Bateman, comb. nov., P. elongata (Rydberg) R.M.Bateman, comb. nov., P. michaelii (Greene) R.M.Bateman, comb. nov., P. leptopetala (Rydberg) R.M.Bateman, comb. nov., P. transversa (Suksdorf) R.M.Bateman, comb. nov., P. cooperi (S.Watson) R.M.Bateman, comb. nov., P. colemanii (R.Morgan & Glicenstein) R.M.Bateman, comb. nov., P. candida (R.Morgan & Ackerman) R.M.Bateman, comb. nov. and P. yadonii (R.Morgan & Ackerman) R.M.Bateman, comb. nov. © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society, 2003, 142, 1–40.
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We investigated the female-produced sex pheromone of the solitary bee Andrena nigroaenea and compared it with floral scent of the sexually deceptive orchid Ophrys sphegodes which is pollinated by Andrena nigroaenea males. We identified physiologically and behaviorally active compounds by gas chromatography with electroantennographic detection, gas chromatography-mass spectrometry, and behavioral tests in the field. Dummies scented with cuticle extracts of virgin females or of O. sphegodes labellum extracts elicited significantly more male reactions than odorless dummies. Therefore, copulation behavior eliciting semiochemicals are located on the surface of the females' cuticle and the surface of the flowers. Within bee and orchid samples, n-alkanes and n-alkenes, aldehydes, esters, all-trans-farnesol and all-trans-farnesyl hexanoate triggered electroantennographic responses in male antennae. Most of the alkanes and alkenes occurred in similar patterns both in the bees and orchids. O. sphegodes leaf extracts contained mostly the same compounds but in different proportions. In behavioral tests with synthetic compounds, blends of alkenes triggered significantly more approaches and pounces of the males whereas alkanes were not more attractive than odorless dummies. Since alkanes and alkenes together were most attractive, we conclude they constitute the bees' sex pheromone as well as the pseudocopulation-behavior releasing orchid-odor bouquet.
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Ophrys flowers mimic virgin females of their pollinators, and thereby attract males for pollination. Stimulated by scent, the males attempt to copulate with flower labella and thereby ensure pollination. Here, we show for the first time, to our knowledge, that pollinator attraction in sexually deceptive orchids may be based on a few specific chemical compounds. Ophrys speculum flowers produce many volatiles, including trace amounts of (omega-1)-hydroxy and (omega-1)-oxo acids, especially 9-hydroxydecanoic acid. These compounds, which are novel in plants, prove to be the major components of the female sex pheromone in the scoliid wasp Campsoscolia ciliata, and stimulate male copulatory behaviour in this pollinator species. The specificity of the signal depends primarily on the structure and enantiomeric composition of the oxygenated acids, which is the same in wasps and in the orchids. The overall composition of the blend differs significantly between the orchid and its pollinator and is of secondary importance. 9-Hydroxydecanoic acid is a rarely occurring compound that until now has been identified only in honeybees. Contrary to the standard hypothesis that Ophrys flowers produce only 'second-class attractivity compounds' and are neglected once the pollinator females are present, we show that flowers are more attractive to the males than are their own females.
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Male Colletes cunicularius bees pollinate the orchid, Ophrys exaltata, after being sexually deceived by the orchid's odor-mimicry of the female bee's sex pheromone. We detected biologically active volatiles of C. cunicularius by using gas chromatographic-electroantennographic detection (GC-EAD) with simultaneous flame ionization detection. After identification of the target compounds by coupled gas chromatography mass spectrometry (GC-MS), we performed behavioral tests using synthetic blends of the active components. We detected 22 EAD active compounds in cuticular extracts of C. cunicularius females. Blends of straight chain, odd-numbered alkanes and (Z)-7-alkenes with 21-29 carbon atoms constituted the major biologically active compounds. Alkenes were the key compounds releasing mating behavior, especially those with (Z)-7 unsaturation. Comparison of patterns of bee volatiles with those of O. exaltata subsp. archipelagi revealed that all EAD-active compounds were also found in extracts of orchid labella. Previous studies of the mating behavior in C. cunicularius showed linalool to be an important attractant for patrolling males. We confirmed this with synthetic linalool but found that it rarely elicited copulatory behavior, in accordance with previous studies. A blend of active cuticular compounds with linalool elicited both attraction and copulation behavior in patrolling males. Thus, linalool appears to function as a long-range attractant, whereas cuticular hydrocarbons are necessary for inducing short-range mating behavior.
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The orchid Ophrys sphegodes Miller is pollinated by sexually excited males of the solitary bee Andrena nigroaenea, which are lured to the flowers by visual cues and volatile semiochemicals. In O. sphegodes, visits by pollinators are rare. Because of this low frequency of pollination, one would expect the evolution of strategies that increase the chance that males will visit more than one flower on the same plant; this would increase the number of pollination events on a plant and therefore the number of seeds produced. Using gas chromatography-mass spectrometry (GC-MS) analyses, we identified more than 100 compounds in the odor bouquets of labellum extracts from O. sphegodes; 24 compounds were found to be biologically active in male olfactory receptors based on gas chromatography with electroantennographic detection (GC-EAD). Gas chromatography (GC) analyses of odors from individual flowers showed less intraspecific variation in the odor bouquets of the biologically active compounds as compared to nonactive compounds. This can be explained by a higher selective pressure on the pollinator-attracting communication signal. Furthermore, we found a characteristic variation in the GC-EAD active esters and aldehydes among flowers of different stem positions within an inflorescence and in the n-alkanes and n-alkenes among plants from different populations. In our behavioral field tests, we showed that male bees learn the odor bouquets of individual flowers during mating attempts and recognize them in later encounters. Bees thereby avoid trying to mate with flowers they have visited previously, but do not avoid other flowers either of a different or the same plant. By varying the relative proportions of saturated esters and aldehydes between flowers of different stem positions, we demonstrated that a plant may take advantage of the learning abilities of the pollinators and influence flower visitation behavior. Sixty-seven percent of the males that visited one flower in an inflorescence returned to visit a second flower of the same inflorescence. However, geitonogamy is prevented and the likelihood of cross-fertilization is enhanced by the time required for the pollinium deposited on the pollinator to complete its bending movement, which is necessary for pollination to occur. Cross-fertilization is furthermore enhanced by the high degree of odor variation between plants. This variation minimizes learned avoidance of the flowers and increases the likelihood that a given pollinator would visit several to many different plants within a population.
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We present a phylogenetic analysis of the major lineages of the sexually deceptive orchid genus Ophrys based on nuclear ribosomal (nr) DNA (internal transcribed spacer region) and noncoding chloroplast (cp) DNA (trnL-trnF region) sequences. Sequence divergence within and among major Ophrys lineages was low for both nrDNA and cpDNA sequences. Separate analyses resulted in similar but poorly resolved trees. An incongruence length difference test revealed that nrDNA and cpDNA data sets were not incongruent. A combined analysis resulted in a better-resolved phylogenetic hypothesis of relationships among the major Ophrys lineages. Our data strongly support a division of Ophrys into two groups. These groups do not correspond to the earlier proposed sections Euophrys and Pseudophrys and are thus in conflict with traditional classifications. Our results support a well-resolved monophyletic group that contains the geographically widespread O. bombyliflora, O. speculum, O. tenthredinifera, and the O. fusca-lutea lineage. Relationships in the other group are poorly resolved. Based on our observations that taxa with identical sequences at presumably rapidly evolving loci clearly differ in floral morphology, we hypothesize that the diversity in the genus Ophrys is the result of a recent radiation in this orchid lineage.