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EVOLUTION OF LONG-TONGUED HAWKMOTHS AND POLLINATION OF LONG-SPURRED ANGRAECUM ORCHIDS

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Since Darwin the extremely long tongues of tropical hawkmoths have been interpreted to be the result of a coevolutionary race with long nectar spurs of orchids. However, extremely long-proboscis hawkmoths are not restricted to the exploitation of highly specialized sphingophilous flowers. Due to their long tongues and a swing-hovering flight they avoid ambush predators such as huntsman spiders, which lurk among flowers. However, swing-hovering hinders full insertion of the proboscis into the long spurs of orchids. Some orchids prevent the moths from the swinging flight by forcing them to land on their protruding labellum. This is the case with Angraecum sesquipedale and Xanthopan morganii praedicta. Illegitimate visitors with tongues longer than the orchid spurs can exploit the nectar or even waste the pollinaria, thus exerting selection pressure towards spur elongation with the consequence of pollinator-shift from shorter- to longer-tongued moths.
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October 5, 2013 10:26 WOC Orchid 210mm x 297mm p0026 3rd Reading
EVOLUTION OF LONG-TONGUED HAWKMOTHS
AND POLLINATION OF LONG-SPURRED
ANGRAECUM ORCHIDS
Lutz Thilo WASSERTHAL
University of Erlangen-Nuremberg,
Staudtstrasse 5, 91058 Erlangen, Germany
ltwthal@biologie.uni-erlangen.de, Lutz.Thilo.Wasserthal@fau.de
Since Darwin the extremely long tongues of tropical hawkmoths have been interpreted to
be the result of a coevolutionary race with long nectar spurs of orchids. However, extremely
long-proboscis hawkmoths are not restricted to the exploitation of highly specialized sphin-
gophilous flowers. Due to their long tongues and a swing-hovering flight they avoid ambush
predators such as huntsman spiders, which lurk among flowers. However, swing-hovering
hinders full insertion of the proboscis into the long spurs of orchids. Some orchids prevent
the moths from the swinging flight by forcing them to land on their protruding labellum.
This is the case with Angraecum sesquipedale and Xanthopan morganii praedicta. Illegiti-
mate visitors with tongues longer than the orchid spurs can exploit the nectar or even waste
the pollinaria, thus exerting selection pressure towards spur elongation with the consequence
of pollinator-shift from shorter- to longer-tongued moths.
Introduction
After having inspected one specimen of the
long-spurred orchid Angraecum sesquipedale
Darwin (1862) predicted a pollinating moth with
a long proboscis, which could reach the nectar
hidden deeply in the spurs. This assumption
was supported by Wallace (1867). Rothschild
and Jordan in their revision of Sphingid moths
(1903) had a choice between two Malagasy hawk
moths with such long tongues, Xanthopan mor-
gani and Coelonia solani. They attributed the
“job” of pollinating the long-spurred Angrae-
cum sesquipedale to Xanthopan morgani and
called the endemic Malagasy race praedicta
with reference to Wallace’s prediction. Since
then, the extremely long tongues of hawkmoths
have been interpreted to be the result of a
coevolutionary race with long nectar spurs or
tubes of plants as suggested by Darwin and
Wallace. Fruit set in European Platanthera
orchids with long spurs was shown experimen-
tally to be higher in specimens with spurs
slightly longer than the moth’s tongue (Nilsson,
1988). There is, however, no evidence for the cor-
related nutritional dependence of the moths on
the orchids, which could exert a high selection
pressure on length increase of the moth’s tongue.
The extremely long-tongued hawkmoths from
Madagascar and the tropics of South America are
not restricted to an exploitation of highly special-
ized sphingophilous flowers. They also visit less
specialized flowers such as inflorescences of Lan-
tana camara or Clerodendron putre, Verbenaceae
(Wasserthal, 1993).
Flowers, Pollinating Moths
and Predatory Spiders
Extremely Long Tongues and
Swing-Hovering: Adaptations
for Predator Avoidance
With their long tongues and a swing-hovering
flight during visits to flowers the hawkmoths
280
Proceedings of the 20th World Orchid Conference, Singapore 2011, 280-284
October 5, 2013 10:26 WOC Orchid 210mm x 297mm p0026 3rd Reading
Evolution of Long-tongued Hawkmoths and Pollination of Long-spurred Angraecum Orchids 281
Fig. 1. A Cup ien niu s coccin eus spider changes from lurk (a) to attack position (b) without jumping at the hovering
Agrius cingulatus moth, which is swinging in front of an artificial blossom between position (a) and (b). From Wasserthal
(2001).
avoid predators such as huntsman spiders, which
produce no webs but locate and catch their prey in
vegetation (Wasserthal, 1993, 1996). They sense
the wing vibrations of the moths from distances
of up to 3 m. The long tongues allow the moths
to maintain a safe distance from most flowers
they visit and the swing-hovering prevents the
predators from targeting the moths and finding
the proper moment for an attack (Wasserthal,
2001; Fig. 1). Swinging flight and long tongues
are assumed to be very old traits. Hunting spi-
ders existed as far back as the Carboniferous
(Kittel, 1910). When hawkmoths appeared on
the evolutionary stage they were confronted with
predators such as hunting spiders and evolved
their long tongues. The long-spurred orchids thus
profited from the availability of diverse pre-
adapted moths with different tongue lengths.
They recruited for the transfer of pollinaria
species with tongues best fitted to their actual
spur length.
The hypothesis that extremely long tongues
evolved as an adaptation to predators was coun-
tered with the argument that hunting spiders were
not observed in the wild to capture large hawk-
moths (Nilsson, 1989). However, these interac-
tions occur in the dark. Also, most flowers are
in the canopy of the rainforest, where there is
little chance of observing them. Our confronta-
tion experiments with diverse hawkmoths species
in the field and greenhouse cages with Mala-
gasy spiders of the family Sparassidae and Costa
Rican Ctenid spiders showed that they target and
approach the shivering or hovering moths at night
(Wasserthal,1998). Moreover, the longest tongued
hawkmoth species occur in the new world trop-
ics with sphingophilous flowers in plant families
other than orchids. Some sphingophilous flowers
are suspended in a manner, which allows the
moths to swing-hover together with the blossom
while their proboscises are fully inserted into the
nectar tubes.
How is Angraecum Sesquipedale
Pollinated Despite the Impediment
of Swing-Hovering?
It was hypothesized that the swing-hovering
hawkmoths are incapable of inserting their
tongues deeply enough into the spurs of Angrae-
cum orchids to obtain nectar and remove the
pollinaria, which become attached to the proper
(basal) area of the proboscis. To test this
hypothesis the visits of Xanthopan morganii to
A. sesquipedale were observed and documented
with infrared videos in southeastern Madagas-
car in 1992. As Xanthopan proved to be rare
in that area, we introduced two captured indi-
viduals into a large flight tent installed in the
field above flowering A. sesquipedale. The cap-
tured male moth already carried at its tongue
a viscidium and nectar remnants from the wild.
This was the first proof of the pollinator role of
Xanthopan for A. sesquipedale. In the flight tent
the male and a female repeatedly visited the flow-
ers. Both stopped the initial swing-hovering when
they established leg-contact with the protruding
labellum and thus fully inserted the tongue into
the spur. They removed the pollinaria and trans-
ferred them later to other blossoms (Wasserthal,
1997 and Fig. 2).
A similar interaction exists between Angrae-
cum sororium, which also has a protruding
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282 L. T. Wasserthal
Fig. 2. Xanthopan morganii praedicta, first photographic documentation for it as the pollinator of Angraecum
sesquipedale. (a) Tongue insertion, (b) Landing on the protruding labellum (c) Backwards and upwards flight with polli-
naria on the tongue base. From Wasserthal (1997).
labellum and the swing-hovering Coelonia solani.
One moth species of this guild (Panogena
lingens) never swing-hovers. This is why they
can pollinate orchids with upright rather than
protruding labella like Angraecum arachnites
or species with intermediately long or narrow
spurs like A. compactum and A. teretifolium,
which are not pollinated by related species with
swing-hovering flight. This confirms observations
by Nilsson et al., (1985, 1987) who detected
pollinaria of these and other species on dif-
ferent sites on the basal tongue of Panogena
lingens. Moths with tongues longer than the
spurs can become illegitimate visitors and exploit
the nectar without transferring pollinaria, which
may even be wasted. This exerts selection pres-
sure towards spur elongation with the conse-
quence of pollinator-shift from shorter tongued
moths to longer tongued ones (Wasserthal,
1997; Fig. 3).
Angraecum longicalcar — Lack
of a Landing Platform as an
Obstacle to Successful
Pollination
Angraecum longicalcar is another extremely long-
spurred orchid (up to 32 cm in length), which
can have as many as 10 blossoms per panicle.
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Evolution of Long-tongued Hawkmoths and Pollination of Long-spurred Angraecum Orchids 283
Fig. 3. Comparison of the “coevolution” model of Darwin 1862 (a) and the “pollinator shift” model (b) in orchid
spur evolution. (a) Evolutionary race between increasing spur length and increasing tongue length. (b) Recruitment of
generalist feeders with preadapted tongues of different lengths as pollinators by long-spurred angraecoid orchids and their
successive substitution. When spur enlargement driven by the primary visitor, exceeds a certain diameter, the flower can
be exploited by a longer-tongued illegitimate visitor (asterisk): Such a situation has been represented by the interaction of
X. morganii and C. solani with Angraecum compactum (Wasserthal, 1997). When the spurs have reached a length longer
than the extremely long tongues of the moths, these become the regular pollinators. When the spur of the flower reaches
a size which places the nectar column out of reach for the primary pollinator, the flower may still be pollinated by this
species but it now acts as a deceptive blossom. Black: orchid pollinator; grey: non-pollinating orchid visitor; white: moth
incapable of exploiting the orchid. From Wasserthal (1997).
Fig. 4. (a) Two Xanthopan morganii praedicta swing-hovering in front of Angraecum longicalcar without an attempt
to fully introduce extended tongues into the spur. The moths did not obtain access to the nectar column and did not
remove the pollinaria. (b) An unusual not spontaneously swing-hovering female Coelonia solani removed and transferred
the pollinaria at the base of the proboscis (arrowhead). This is the first documentation of a successful visit to Angraecum
longicalcar by an extremely long-tongued hawkmoth.
October 5, 2013 10:26 WOC Orchid 210mm x 297mm p0026 3rd Reading
284 L. T. Wasserthal
It has an upright labellum, not appropriate for
landing. This Malagasy endemic orchid has van-
ished from its natural habitat. We obtained plants
from Marcel Lecoufle in Paris in 1994 and culti-
vated them until now. In addition, we bred all
relevant long-tongued hawkmoths species in our
Erlangen greenhouse in a subtropical climate. We
synchronized the eclosion of the moths with the
flowering season of the orchids between 1995 and
2009. In confrontation experiments with 21 Xan-
thopan morganii praedicta all proved to be unable
to introduce their tongues deeply enough into the
spurs to obtain nectar because the labellum is
upright and the blossom structure is such that
the moth could not land. Thus the moths swing-
hovered and moved restlessly from blossom to
blossom without a chance of coming close enough
to obtain nectar, which is in the distal half of
the spurs (Fig. 4a). The other Malagasy Sphingid
with an extremely long tongue, Coelonia solani,
was also confronted with this orchid and one indi-
vidual of seven with a tongue length of 19 cm
removed and transferred the pollinaria (Fig. 4b).
It was an individual which was exceptional in
not exhibiting spontaneous swing-hovering. All
19 tested Panogena lingens were not capable
of obtaining nectar, as their tongues (maximum
length between 7.4 and 11.5 cm) were too short
to reach it. None of the moths removed the polli-
naria, although they inserted the tongue fully into
the spur. Perhaps the dimension and proportions
of this orchid are too large for the slender tongue
of Panogena.
The observed interactions of angraecoid
orchids with sphingid moths confirm Darwin’s
hypothesis that these flowers are dependent on
moths with correspondingly long proboscises for
their pollination. These moths “pay” for the nec-
tar reward with impaired mobility. Long tongues
and the swing-hovering behavior are pre-adapted
to avoid predator attacks. The orchids take
advantage of the extremely long-tongued and big
moths, which consume large volumes of nectar
due the high energy demands of their powerful
flight.
Acknowledgements
This investigation was supported by DFG
(Wa 158/4). I thank Prof. J. Arditti, University
of California, Irvine, for linguistic editing.
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Supplementary resource (1)

Article
Full-text available
Since DARWIN the extremely long tongues of tropical hawk moths have been interpreted to be the result of a coevolutionary race with long nectar spurs of orchids. However, extremely long-proboscis hawkmoths are not restricted to the exploitation of highly specialized sphingophilous flowers. Due to their long tongues and a swing-hovering flight they avoid ambush predators such as huntsman spiders, which lurk among flowers. However, swing-hovering hinders full insertion of the proboscis into the long spurs of orchids. Some orchids prevent the moths from the swinging flight by forcing them to land on their protruding labellum. This is the case with Angraecum sesquipedale and Xanthopan morganii praedicta. Illegitimate visitors with tongues longer than the orchid spurs can exploit the nectar or even waste the pollinaria, thus exerting selection pressure towards spur elongation with the consequence of pollinator-shift from shorter- to longer-tongued moths.
Article
Full-text available
Abstract: The pollination process of the extremely lang-spurred orchids Angraecum sesquipedale and A. sororium is described and documented here for the first time. The pollinaria and viscidia Ioad was examined in moths captured in central and south Madagascar. Visits to orchids by hawkmoths were rarely observed in the field and were therefore systematically recorded in !arge flight tents using a night-vision video technique and fla shlight photography. Angraecum sesquipedale in Fort Dauphin is pollinated by Xanthopan morgoni proedieta and A. sororium on Mt. Angavokely by Coelonia solani. By combining a deep nectar spur of extraordinary length with a protruding labellum functioning as a landing platform, these orchids overcome the moth's Stereotypie swing-hovering flight thus enabling full Insertion of the long tongue. Angroecum compaetum in Foret d'Ambohitantely is pollinated by both the shorter and longertongued forms of Ponogeno lingens which never swing-hover but is also exploited by X. morgani and C. solani with wastage of pollinaria. The duration of tongue Insertion, nectar exploitation and tongue withdrawal were analyzed: legitimate and illegitimate visito rs differ in their time budget and approach to the flower. Nectar volume, nectar Ievei and sugar concentration of A. sesquipeda/e and A. sororium were compared with the nectar requirements of the pollinating hawkmoths. The evolution of very long spurs in these orchids is likely to have involved a series of pollinator shifts. The orchids adapted to different hawkmoth species with increasingly long tongues which primarily evolved to avoid predator attacks during vis its to less specialized flowers. This "pollinator s hift" model modifies the dassical "coevolutionary race" model. The relevance of the taxon Angroecum bosseri Senghas is questioned.
Book
In this investigation of orchids, first published in 1862, Darwin expands on a point made in On the Origin of Species that he felt required further explanation, namely that he believes it to be 'a universal law of nature that organic beings require an occasional cross with another individual'. Darwin explains the method by which orchids are fertilised by insects, and argues that the intricate structure of their flowers evolved to favour cross pollination because of its advantages to the species. The book is written in Darwin's usual precise and elegant style, accessible despite its intricate detail. It includes a brief explanation of botanical terms and is illustrated with 34 woodcuts.
Article
Studies on hawkmoth pollination in a primary forest in central Madagascar indicated that at least five of six flowering, long-spurred angraecoid species exploited the same hawkmoth, Panogena lingens. as a pollen vector. Several other long-tongued hawkmoth species were present, but no evidence was found that they participated in orchid pollination. The pollinaria of Angraecum arachnites, A. compactum, Neobathiea grandidierana, and Jumellea teretifolia were deposited on the basal portion of the proboscis. The latter three species utilized the same dorsal portion of the proboscis, whereas attachment by A. arachnites was ventral. The pollinaria of Aerangis fuscata were deposited on the frons and palps. Hawkmoths frequently carried mixed loads, but at least ethological and mechanical mechanisms seemed to restrict interspecific pollination. The P. lingens-angraecoid orchid relationship may have reached a specialized state before progenitors of other long-tongued Sphingidae colonized or evolved in central Madagascar.
Article
Some plants have evolved flowers of extraordinary depth, a phenomenon which puzzled Darwin1. Darwin suggested that the evolution of deep flowers could be a response to a kind of 'race' with pollinating insects: the length of the tongues of pollinating insects could increase as a result of a general size increase, or because it increased their nectar foraging efficiency. As this occurred, plants with relatively shallow flowers could be disadvantaged since pollen transfer, which is effected by physical contact between the pollinator and the anthers or stigma of the plant, could be reduced when the insect tongue is long relative to flower depth. This could lead to the evolution of increasing flower depth which in turn could drive the evolution of a further increase in insect tongue length. Various predictions of Darwin's proposal were tested here for orchid species with deep flowers that are pollinated by moths. It was found that insects do indeed insert their probosces no further than necessary to obtain nectar; that an experimental reduction in flower depth reduces both the male and female components of fitness; and that in natural populations there is a correlation between flower depth and female fitness measured by fruit set. These results all support Darwin's hypothesis to explain the evolution of flower depth.
Article
Anthecological relations between a long-spurred angraecoid orchid and pollinating Sphingidae are documented for the first time. In a primary forest on the Central Plateau of Madagascar Angraecum arachnites Schltr. was found to be pollinated by and adapted to a single species of hawk-moth, Panogena lingens (Butler), despite abundance of many concurrent Sphingidae of which several were also long-tongued. Furthermore, P. lingens was dimorphic in the length and breadth of its proboscis and only the morph with the longest and most slender proboscis was recorded to pollinate A. arachnites. Exclusive and precise adaptation to the latter morph of P. lingens existed in floral morphology and probably in other characteristics such as flowering phenology and chemical signalling. Several concurrently flowering orchid species were sharing P. lingens as a pollinator resource. The monophily in A. arachnites is interpreted as a result of a refined long-term specialization developed within an archaic evolutionary relationship in a relatively stable environment. The extraordinary number and diversity of long-spurred Orchidaceae in Madagascar appears to be a direct coevolutionary consequence of an Old-World-unique diversity of long-tongued archaic Sphingidae that has persisted in this isolated land.
Anpassungen bei Sphingiden zur Vermeidung von Spinnen-und Fledermaus- Attacken
  • L T Wasserthal
Wasserthal, L.T. (2001). Anpassungen bei Sphingiden zur Vermeidung von Spinnen-und Fledermaus- Attacken. Verhandlungen Westdeutscher Entomologentag Düsseldorf 2000: 13–30.