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Pollination biology of Aristolochia grandiflora (Aristolochiaceae) in Veracruz, Mexico

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Abstract

The flowers of Aristolochia grandiflora are sapromyiophilous trap blossoms that deceive their visitors with optical and olfactory promise of hidden protein-rich substrate. The most effective pollinators are large Diptera, mostly Calliphoridae, which become trapped in the protogynous flowers on the first day of anthesis. Although the flowers are protogynous and subsequently release pollen, a variety of floral changes occur that discourage further insect visitation after pollination and allow the pollinators to escape on the second day of anthesis. On the first day of anthesis the flowers' strong carrion odor and color gradients draw pollinators toward the receptive gynostemium deep within the flower. Constricting floral tubes with trichomes oriented toward the gynostemium aid in capturing and holding the insects. On the next day, the flowers change to male phase and pollen is deposited on the pollinator. Flower structure and function then change to release the pollen-dusted pollinator. To aid in pollinator release, the floral odor disappears, color cues change, hairs relax, and the constricting areas of the tube are opened. Pollination appears to be a two-day process for any given flower with floral senescence by the third day. Floral visitors do oviposit in the flowers, but we suggest that this is not relevant to pollination. Comparisons are made with other Aristolochiaceae.
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Pollination Biology of Aristolochia grandiflora (Aristolochiaceae) in Veracruz, Mexico
Author(s): K. S. Burgess, J. Singfield, V. Melendez and P. G. Kevan
Source:
Annals of the Missouri Botanical Garden,
Vol. 91, No. 2 (Jul., 2004), pp. 346-356
Published by: Missouri Botanical Garden Press
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1 We thank Robert Bye, Director of the Botanic Garden, UNAM, Edelmira Linares (UNAM), Carlos Vergara, Biology
and Chemistry, Universidad de Las Americas, Puebla, Mexico, and Delfino Alvaro Campos Villanueva at the Estacion
de Biologfa Tropical "Los Tuxtlas," Instituto de Biologfa, UNAM, for his interest and help with the project. We also
thank Pablo Manrque-Saide (FMVZ) for help with insect identification, and Ian Smith at the University of Guelph
Imaging Facility, College of Biological Sciences, for help with the figures. Some funds were made available through a
grant from the Natural Sciences and Engineering Research Council of Canada to P.G.K.
2 Botany Department, University of Guelph, Guelph, Ontario, Canada N1G 2W1. burgessk@uoguelph.ca.
3 Departamento de Ecologfa, FMVZ, Universidad Autonoma de Yucatan, C.P. 97000, Apdo. Postal 4-116, Itzimna
Merida, Mexico. virmelen@tunku.uady.mx.
4 Department of Environmental Biology, University of Guelph, Guelph, Ontario, Canada N1G 2W1. pkevan@
uoguelph.ca.
ANN . MISSOURI BOT. GARD. 91: 346-356. 2004.
K. S. Burgess72 J. Singfield72
E Melendez73 and P. G. Kevan4
ABSTRACT
The flowers of Aristolochia grandiJ]ora are sapromyiophilous trap blossoms that deceive their visitors with optical
and olfactory promise of hidden protein-rich substrate. The most effective pollinators are large Diptera, mostly Calli-
phoridae, which become trapped in the protogynous flowers on the first day of anthesis. Although the flowers are
protogynous and subsequently release pollen, a variety of floral changes occur that discourage further insect visitation
after pollination and allow the pollinators to escape on the second day of anthesis. On the first (lay of anthesis the
flowers' strong carrion odor and color gradients draw pollinators toward the receptive gynostemium deep within the
flower. Constricting floral tubes with trichomes oriented toward the gynostemium aid in capturing and holding the
insects. On the next day, the flowers change to male phase and pollen is deposited on the pollinator. Flower structure
and function then change to release the pollen-dusted pollinator. To aid in pollinator release, the floral odor disappears,
color cues change, hairs relax, and the constricting areas of the tube are opened. Pollination appears to be a two-day
process for any given flower with floral senescence by the third day. Floral visitors do oviposit in the flowers, but we
suggest that this is not relevant to pollination. Comparisons are made with other Aristolochiaceav.
Key words: Aristolochia grandiJ]ora, Aristolochiaceae, brood site provision, Calliphoridae, Diptera, insect interac-
tions, Phoridae, pollination biology, protogyny, sapromyiophily, Staphylinidae.
There are many examples of how plants eleceive
their pollinators to ensure pollination events (Dafni,
1984; Proctor et al., 1996). In some of the more
elaborate examples, the plant benefits from such
interactions by securing the transport of its pollen,
whereas the pollinator does not benefit. This is es-
pecially true for the Orchidaceae (containing the
majority of species pollinated by deceit), as most
insects will not eat pollinaria (Faegri & van der
Pijl, 1979). However, in many examples of floral
deceit some reward, including false pollen (e.g.,
Melastomataceae) and shelter (e.g., Araceae), are
provided. Brood site mimicry, especially by scents
and sometimes appearances of carrion, dung, and
fungi, is well known in fly pollination through sap-
romyophily (Vogel, 1990; Larson et al., 2001) (or
sapromyiophily of Proctor et al., 1996) and its
equivalent involving beetles, saprocantharophily
(Bernhardt, 2000). Although Faegri and van der
Pijl (1979) combined the characteristic s of both fly
and beetle pollination by such deceit under the
syndrome of sapromyiophily, characteristics of this
syndrome include: more or less radial floral parts
with depth; lantern-shaped floral parts with filiform
appendages; dull floral colors (dark brown/purple/
green) often checkered with dark spots; odor resem-
bling that of decaying protein; the presence of os-
mophores (scent glands); the absence of nectar
guides, nectar, or other primary resources (Faegri
& van der Pijl, 1979; Vogel, 1990; Proctor et al.,
1996). These features can be found in flowers of
Asclepiadaceae, Araceae, Orchidaceae, Aristolo-
chiaceae, Sterculiaceae, Rafflesiaceae, Hydnora-
ceae, Taccaceae, and Burmanniaceae. Sapromyi-
ophily can occur with or without some form of
imprisonment (trap or semi-trap blossoms) of the
insect by the flower (Proctor et al., 1996; Faegri &
van der Pijl, 1979).
POLLINATION BIOLOGY OF
ARISTOLOCHIA
GRANDIFLORA
(ARISTOLOCHIACEAE) IN
VERACRUZ MEXICO1
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Volume 91, Number 2
2004 Burgess et al. 347
Pollination Biology of Aristolochia grandiflora
The Aristolochiaceae comprise six genera: Aris-
tolochia L., Asarum L., Saruma Oliv., Euglypha R.
Chodat & E. Hassl., Holostylis Rchb., and Thottea
Rottb. (Pfeifer, 1960; Gonzalez, 1994). All are pol-
linated by deceiving their pollinators (although
some species may self-pollinate; Burke, 1890;
Petch, 1924; Hou, 1983), and some may or may not
trap their pollinator. For example, the genus Asa-
rum secures pollination by deceit but without im-
prisonment, as in A. caudatum Lindl., which at-
tracts mostly mycophilous Diptera. In this case the
flies, during oviposition within the flower, acquire
pollen, but the larvae perish (Vogel, 1978a, 1978b).
A genus that imprisons its pollinators is Aristolo-
chia, comprising most of the 450 species within the
family (Pfeifer, 1960, 1970; Gonzalez, 1994). Like
many trap and semi-trap blossoms, Aristolochia has
protogynous flowers. During the female phase floral
visitors, pollinators or otherwise, are trapped within
the flower to facilitate pollen deposition on the stig-
ma. After pollination, visitors remain trapped with-
in the flower until pollen is shed over them during
the male phase of anthesis. After pollen release,
the flower opens to allow pollinators to escape and
carry pollen to another flower in female phase
(Proctor et al., 1996). Although the general mech-
anism of pollination in Aristolochiaceae is under-
stood from studies on various species such as A.
bracteolata Lam., A. clematitis L., A. Iittoralis D.
Parodi, A. pilosa Kunth, A. grandiflora Sw., A. Ia-
biata Willd., A. Iinderi A. Berger, A. cordifolia
Glaz., A. sipho L'Her., A. tricaudata Lem., A. fim-
briata Cham. & Schltdl., A. macroura Gomes, A.
glaucescens Kunth, A. goldieana Hook. f., and A.
arborea Linden (Sprengel, 1793; Hildebrand, 1867,
1870; Delpino, 1873; Muller, 1873, 1883; Cooke,
1882; Correns, 1891, 1892; Ule, 1898a, 1898b,
1898c, 1898d, 1899, 1900; Knuth, 1909; Kirchner,
1911; Cammerloher, 1923; Carr, 1924; Petch,
1924; Knoll, 1956; Brantjes, 1980; Faegri & van
der Pijl, 1979; Hou, 1983; Hilje, 1984; Hime &
Costa, 1985; Wolda & Sabrosky, 1986; Razzak et
al., 1992; Hall & Brown, 1993; Proctor et al.,
1996), detailed studies on the pollination biology
are scarce (see Cammerloher, 1923; Hilje, 1984;
Hall & Brown, 1993), and there are few compara-
tive studies between species (Brantjes, 1980; Sakai,
2002b).
One of the more complex examples of sapromyi-
ophily is found in Aristolochia grandiflora Swartz,
which produces one of the largest flowers of the
Neotropical flora, and the largest in the Aristolo-
chiaceae (ca. 35 cm diam.) (Knuth, 1909; Gonzalez,
1994). There are only two studies that attempt to
explore the pollination biology of this species. Cam-
merloher (1923) studied its floral mechanisms at
the Botanic Gardens in Bogor, Java, and Hilje
(1984) worked mostly on the phenology of a natural
population in Costa Rica. Although Cammerloher
(1923) studied cultivated plants outside the natural
Neotropical range of A. grandiflora, both authors
described the pollination system of A. grandiflora
as consistent with the syndrome of sapromyiophily
with long-term imprisonment of the pollinators.
However, these studies contrast in the type of pol-
linators and insect visitors observed in two dispa-
rate populations, namely those native to Java and
Costa Rica, respectively. Because neither study
provides a detailed assessment of the insect inter-
actions and floral phenology of A. grandiflora, and
because there is only sparse information on A.
grandiflora in its native range, the results of further
detailed observations contribute greatly to our un-
derstanding of the pollination biology of this spe-
cies.
The goal of our research is to describe the pol-
lination biology of Aristolochia grandiflora growing
in its native habitat from a garden in Los Tuxlas,
Veracruz, Mexico. In this study we address the fol-
lowing objectives:
1. Determination of the mechanisms of sapro-
myiophily for long-term imprisonment in A.
grandiflora.
2. Assessment of the diversity and visitation
rates of floral visitors to flowers of A. gran-
diflora.
3. Determination of whether flowers of A. gran-
diflora provide brood sites for flower visitors.
MATERIALS AND METHODS
This study took place 1 km from La Estacion de
Biologia Tropical de los Tuxtlas, in the lowland
coastal rain forest of Veracruz, southeastern Mexico
(28 Apr.-9 May 1997). Aristolochia grandiflora is
known to be native to the area and flowers through-
out the year (Ibarra Manriquez & Sinaca Colin,
1987; Hilje, 1984) and was found growing as a
woody liana among cultivated vegetation in an open
habitat. Fifteen separate flowers of A. grandiflora
were used to make observations on floral structure
and insect interactions.
In order to describe the mechanisms of sapro-
myiophily for long-term imprisonment (Objective
1), floral structures important to the pollination pro-
cess of this species were measured on one-, two-,
and three-day-old flowers (N = 8). These include
overall condition of the flower, sexual stage of the
gynostemium, color of various floral structures, and
the presence/absence of odor. Herbarium speci-
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348 Annals of the
Missouri Botanical Garden
mens were made of floral dissections and deposited
at the Herbarium of the Universidad Nacional Au-
tonoma de Mexico in Mexico City.
To address Objectives 2 and 3, insect interac-
tions were observed across all 15 flowers prior to,
during, and after anthesis. In order to observe in-
sect visitation, insects were counted visiting, enter-
ing, and leaving flowers on the first and second day
of anthesis. Eight flowers were covered with mesh
bags to capture all insect visitors to the flower.
Flowers were then cut after the first, second, and
third day of anthesis based on insect interactions
with the flowers (i.e., fly entry and release). Two
flowers were bagged prior to anthesis as controls.
For example, Day 1: Three flowers bagged and cut
for dissection after one day of fly entry (end of the
first day of anthesis); Day 2: Three flowers bagged
after one day of fly entry and cut for dissection at
the end of the second day of anthesis; Day 3: Two
flowers bagged after one day of fly entry and cut
for dissection at the end of the third day of anthesis.
Bagged flowers were then taken to the field sta-
tion at Los Tuxtlas for longitudinal dissection, ob-
servation, preservation, and photography. To count
and identify (1) the insects contained within the
flower and (2) the insects released from the flower
but trapped within the mesh bags, bagged flowers
were fumigated in sealed plastic bags with ethyl
acetate to kill all floral visitors. Upon floral dissec-
tion, all floral visitors trapped within the flowers or
bags were collected and preserved in 70% ethanol.
Insects were not examined microscopically for pol-
len, although visual observations were made. A
sub-sample of each of the insect families was taken
to the Entomological Collection of the Autonomous
University of Yucatan in Merida for identification.
OBSERVATIONS AND RESULTS
MECHANISMS OF SAPROMYIOPHILY FOR LONG-TERM
IMPRISONMENT
Aristolochia grandiflora flowering patterns at our
site are consistent with continual flowering systems
of tropical lianas whereby relatively few flowers per
plant are at anthesis at the same time (Hilje, 1984;
Proctor et al., 1996). As in our study plants, such
flowering patterns are indicative of limited self-pol-
lination by geitonogamy. Flowers of A. grandiflora
at our site also had functional and structural mech-
anisms consistent with those used to describe this
species in the literature (Cammerloher, 1923; Hilje,
1984; Pfeifer, 1966). The flower (Fig. 1) has a uni-
seriate perianth, which includes a long filiform ap-
pendix (ap); the main perianth or limb (li); the fau-
ces (fa) or opening of the flower; the entrance or
ov
ut -li
fa
sy
tu' an
Figure 1. Morphological terminology of Aristolochia
grandiJ]ora floral structures: annulus (an), appendix (ap),
bracteole (br), fauces (fa), gynostemium (gy), limb (li), ova-
ry (ov), syrinx (sy), tube (tu), utricle (ut). (Re-drawn from
Gonzalez, 1994.)
annulus (an); a trichome-lined tube (tu) connected
to the syrinx (sy), which opens into the inner cham-
ber of the flower, the utricle (ut); male and female
organs are located at the top of the utricle collec-
tively called a gynostemium (gy); and the inferior
ovary (ov) is subtended by a bracteole (br). General
observations on floral odor revealed that A. gran-
diflora flowers one day prior to and during the first
day of anthesis had a strong carrion scent, which
disappeared by the second day.
Additional changes in overall floral form oc-
curred during anthesis. As seen in Figure 2, the
length measurements made between the utricle and
the tube increased as the flower switched from fe-
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Volume 91, Number 2
2004 Burgess et al. 349
Pollination Biology of Aristolochia grandiflora
A
Figure 2. Relaxation of Aristolochia grandiJ)ora floral structure to allow for insect departure on the second day of
anthesis. A. The angle between these floral structures increased to 60 degrees on the second day of anthesis. B.
The angle between the floral tube and utricle wall prior to pollination on the first day of anthesis is approximately 28
degrees.
male to male phase (an increase in angle from 28
to 60 degrees). Table 1 details changes in floral
form, structure, and color over the first three days
of anthesis. Observations are based on floral dis-
sections made on one-, two-, and three-day-old
flowers. The first day of anthesis, starting shortly
after dawn, showed vibrant coloration of all struc-
tural components as the female phase of the gy-
nostemium progressed. Most of the flower's struc-
tural components (annulus, tube, syrinx, and
utricle) had erect trichomes and all had intact tis-
sue. As the gynostemium switched from female to
male phase on day 2 of anthesis, a general deteri-
oration of the structural components of the flower
initiated. As seen in Table 1, the tissue of both the
syrinx and the utricle started to degrade, and the
trichomes of all structures flattened. The limb also
began to deteriorate and fold in at this stage, and
discoloration of various structures started. By the
third day of anthesis, the limb completely folded
in, trichomes were mostly absent from all floral
structures, and the tissues of all structures had
started to decay and brown.
INSECT INTERACTIONS (VISITATION AND BROOD SITE
PROVISION)
General observations of floral visitors to five Aris-
tolochia grandifora flowers revealed that on the
day prior to the opening of the limb on the first day
of anthesis, large (ca. 5 mm) Diptera (Calliphori-
dae) were observed congregating along the limb
edge and on the appendix. Shortly after dawn on
the first day of anthesis the carrion-like odor in-
creased in intensity. Insect visitation was observed
to peak between 9:30 and 10:30 A.M. Approxi-
mately 200 insects were observed to be entering
each flower during peak visitation with activity
dwindling to 13 insects between 11:30 A.M. and 12:
00 noon. Even though visitation (the total number
of insects entering a flower) dropped dramatically
by noon, flowers remained open until the next day,
potentially receiving more visitors, although this
was not observed. A more detailed observation of
floral visitation on the first day of anthesis showed
that of those insects immediately identifiable to the
researchers in the field, Coleoptera (ca. 7 mm) and
small (ca. 2 mm) Diptera (Phoridae) were the pri-
mary visitors in the early morning, whereas large
(ca. 5 mm) Diptera (Calliphoridae, Sepsidae, Mus-
cidae, and Heleomyzidae) were only found to visit
mid-morning, although Phoridae visitation contin-
ued throughout (Fig. 3).
Upon dissection of the flowers at the end of the
first day of anthesis the average number of insects
per flower was 454 (Table 2). Although most insects
were Diptera: Phoridae (269) (ca. 2 mm) and Co-
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Floral structure Day I Day 2 Day 3
Limb
350 Annals of the
Missouri Botanical Garden
Table 1. Floral structures important to the pollination process of Aristolochia grandiflora measured on eight flowers
at the end of the first, second, and third day of anthesis. Measurements include overall status of the structure, status
of trichomes on the structure (+
brown; P = purple; W = white). flattened), and notes on structure color (B beige; B1 = black; Br
erecl;
folding on guidelines
absent
checkered (P/W)
folded/decaying
absent
P/Br
Status
Trichomes erect/flattened
Color
Annulus
Status
Trichomes erect/flattened
Color
Tube
Status
Trichomes erect/flattened
Color
.
Syrlnx
Status
Trichomes erect/flattened
Color
Utricle
Status
Trichomes erect/flattened
Color
Gynostemium
Stigma lobes
Status
Color
Anther
Status
Color
rigid and open
absent
checkered (P/W)
soft deeaying
P/P;r
rigid
+
P/B1 plw
rigid
+
P to W
soft
+l-
P to Br/W
decay starting
de( aying
Br
det aying
Br
rigid
+
W Br
rigid
+
spotted (W/P)
decay starting
Br
stigma not receptive
Br
det aying
Br
stigma re(eptive
B decaying
Br
anthers closed
B anthers dehisced
Br decaying
Br
leoptera: Staphylinidae (144) (ca. 7 mm), a number
of large (ca. 5 mm) Diptera were found within the
flowers, namely; Calliphoridae (13), Sepsidae (7),
Muscidae (16), and Heleomyzidae (4). No insects
were found in the mesh bags outside the flower at
the end of the first day of anthesis.
On the second day after anthesis, release of large
(ca. 5 mm) flies (Calliphoridae, Sepsidae, Muscidae,
and Heleomyzidae) by relaxed angle of the perianth
tube and fiattening of trichomes (Fig. 2; Table 1)
occurred between 8:00 A.M. and 9:00 A.M. This was
followed by the release of smaller (ca. 2 mm) flies
(Phoridae). Large (ca. 5 mm) flies (Calliphoridae,
Sepsidae, Muscidae, and Heleomyzidae) were ob-
served to leave the flower with large clumps of pollen
on their back. Upon dissection of the flowers at the
end of the second day of anthesis most insect taxa
initially found within the one-day-old flowers were
now inside the mesh bags but absent from the flower
interior. These included all adult Diptera (Calli-
phoridae (9), Muscidae (4), and Heleomyzidae (1),
and most notably the Phoridae (366)) (Table 2).
Probably most notable was the presence of large
numbers of Staphylinidae still within an average
flower (218) and the occurrence of approximately
1000 Phoridae larvae on the utricle wall.
Dissections of bagged flowers cut after the third
day of anthesis revealed that almost all the insects
that were in the flower at the second day of anthesis
were now only found outside the flower within the
mesh bags (Table 2). These included Phoridiae (29)
and the Staphylinidae (203). There was also a large
number of Phoridae larvae found within three-day-
old flowers (approximately 400), although numbers
decreased from two-day-old flowers by more than
50% (Table 2).
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Volume 91, Number 2
2004 Burgess et al. 351
Pollination Biology of Aristolochia grandiflora
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as a percentage of total insect visitation for each census period.
DISCUSSION
POLLINATION AND MECHANISMS OF
SAPROMYIOPHILY FOR LONG-TERM IMPRISONMENT
Although self-pollination has been suggested for
some Aristolochia species (Burek, 1890, 1892a,
1892b, 1892c, 1894) our observations on A. gran-
diflora suggest that this is most unlikely. Our re-
sults indicate that pollination in A. grandiflora is
consistent with the syndrome of sapromyiophily in
odor, color, and floral structure (Table 1) and ap-
pears to be a two-day process. The protogynous
flowers last only three days, but are attractive to
pollinating insects (Diptera and Coleoptera) only on
the first day of anthesis, which is when they are
most odoriferous and in the pistillate phase, al-
though a large number of insects are attracted by
odor to the general vicinity of even the pre-anthesal
flower. After pollination on the first day, anthers
release pollen onto insects trapped within the utri-
cle. On the second day of anthesis, pollen-laden
insects escape after the flower goes through various
changes in form and loses its scent. Mimetic color
and floral structures appear to entice visitors into
the depth of the perianth once odor has brought
them to congregate in the general area (Faegri &
van der Pijl, 1979; Dafni, 1984). Upon opening
(Fig. 1), the large radial, funnel-shaped limb dis-
played a blotchy pattern of purple and white with
blotchy purple guide-lines leading to the dark cen-
tral cavity of the tube entrance or annulus (see
Cammerloher, 1923; Hilje, 1984). Once the insect
visitors have proceeded past the annulus, our ob-
servations from floral dissection suggest that insects
are directed to the utricle (site of pollination)
through a combination of floral structure (shape of
tube and trichome orientation) and color changes
(Table 1). The floral tube has grades in color from
a dark purple near the annulus to the brighter,
translucent utricle. Presumably, flies phototactical-
ly orient themselves to the light color of the utricle
as suggested by Hilje (1984) and Cammerloher
(1923). Within the flower there are two sites (Fig.
1) that act as filters for insect size selection (see
Hilje, 1984; Brantjes, 1980). Between the perianth
tube and the limb (annulus), and between the tube
and the utricle (syrinx) are constricted areas cov-
ered with stiff trichomes pointing in toward the utri-
cle that allow visitor movement in only one direc-
tion, as seems general for the genus (Knuth, 1909;
Cammerloher, 1923; Hilje, 1984; Hall & Brown,
1993) (also see Table 1).
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Table 2. Insects found
inside the flowers or within mesh bags containing the flowers
of Aristolochia grandiJYora. Dissections were performed on eight flowers cut at: (1) the first
day of anthesis (Day 1: three flowers bagged and cut after one full day of fly entry); (2) the end of the second day of anthesis (Day 2: three flowers
bagged after one full day of fly
entry and cut after fly release); and (3) the end of the third day of anthesis (Day 3: two
flowers bagged after one full day of fly entry and cut one day after fly release). Taxonomic
keys used were McAlpine
et al. (1981-1987), Curran (1934), and Dear (1985).
Day 1 dissection Day 2 dissection Day
3 dissection
Average/ Location Average/ Location Average/ Location
Order Family Genus flower found flower found flower found
Diptera Calliphoridae Cochiomyia 13 flower 9 bag 2 bag
Chloroprocta
Diptera Sepsidae Nemopoda 7 flower 0 0
Diptera Muscidae 16 flower 4 bag 0
Diptera Heleomyzidae Cinderella 4 flower 1 bag 0
Diptera Phoridae Spinophora 269 flower 366 bag 29 bag
Pericyclocera 4 flower
Diplonerva
Dorniphora
Diptera Empididae Boreodronia 1 flower 0 0
Hymenoptera Formicidae 0 0 59 bag
Coleoptera Staphylinidae 144 flower 218 flower 203 bag
4 flower
Coleoptera Nitintulidae 0 flower 1 bag 0
Homoptera Cicadellidae 0 flower 1 bag 0
Diptera Phoridae ° flower 916 flower 396 flower
Larvae
Total (excluding larvae) 454 flower 218 flower 8 flower
382 bag 293 bag
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Volume 91, Number 2
2004 Burgess et al. 353
Pollination Biology of Aristolochia grandiflora
The transition from pistillate to staminate phase
is indicated by changes in floral odor, color, and
structure (Table 1). The switch is reported to be
physiologically triggered by the direct deposition of
pollen onto the stigmatic surface of pistillate flow-
ers (Pfeifer, 1966). Although limited to two flowers,
our bagged controls to which insects had no access
and thus pollen cannot have been deposited on the
stigmas, showed changes as in open-pollinated
flowers. We noted that in the staminate phase the
overall structure of the flower appears to relax at
the beginning of the second day of anthesis (Table
1; Fig. 2). The tube is no longer appressed to the
utricle as the angle increases between these two
floral structures. Hilje (1984) also noted an in-
crease in the diameter of the restriction between
the utricle and the tube at this stage in Aristolochia
grandifora (Fig. 1). Presumably this relaxation of
the flower allows escape of the entrapped insects,
now bearing newly deposited pollen loads from the
dehiscence of anthers as observed in this study on
the morning of the second day of anthesis. Contrib-
uting to the release of insects were changes in the
trichomes (Table 1) throughout the tube and utricle
that become either flattened or brittle, and lose uni-
directional orientation (also noted by Knuth, 1909;
Pfeifer, 1966) (Table 1). At the same time, probably
contributing to insect release is the darkening of
the utricle from translucent white of the first day of
anthesis to brown in the second, which would re-
duce phototactic orientation (Table 1).
By the third day of anthesis the flower decays
rapidly (Table 1). In general, floral senescence oc-
curs and the calyx is either autodigested or falls
(Knuth, 1909; Pfeifer, 1966). We did not observe
persistent calyxes on fruits present at our site, al-
though fallen flowers had withered and dried quick-
ly (within two days: casual observations) in the sun.
The suite of characters (morphological, odor, and
phenological) we describe occurs with sapromyi-
ophily and allows for precise timing of events as-
sociated with successful pollination. The process
depends on the long-term (ca. 1 day) imprisonment
of the insect visitors. The exact timing of entry and
exit of visitors to any Aristolochia species has not
been recorded hitherto, but our observations
showed a peak entry of insects around 10:00 A.M.
On the first day of anthesis, and exiting around 8:
30 the next morning.
INSECT INTERACTIONS (FLORAL XTISITATION AND
POTENTIAL POLLINATORS)
According to Brantjes (1980) some Aristolochia
species are specialized to capture specific fly spe-
cies or sizes, whereas many others capture a wide
variety of organisms that may not be effective pol-
linators. Thus, the potential pollinators of any Aris-
tolochia species are selected by floral size (as sug-
gested by the review in Knuth, 1909) and the
nature of the trap mechanism. Therefore, by mea-
suring the visitor's thorax height and the distance
between floral structures that act as filters, non-
pollinators may be distinguished from potential pol-
linators (Brantjes, 1980). Petch (1924) conducted
studies on the native small-flowered species A.
indica L. and A. bracteata Retz in Sri Lanka and
found that both were visited by a single insect spe-
cies of Ceratopogon (Diptera: Ceratopogonidae).
However, we demonstrated a wide range of Diptera,
Coleoptera, Homoptera, and Hymenoptera impris-
oned in the utricle of A. grandiflora (Table 2).
Our study agrees with previous studies on the
pollination biology of Aristolochia that Diptera, es-
pecially Phoridae, Muscidae, and Calliphoridae,
are the predominant pollinators (Table 2). Although
high numbers of Staphylinidae were present in our
flower dissections, there is no evidence for beetle
pollination in our study. Bernhardt (2000) would
interpret A. grandifora as a generalist system in-
corporating both beetles and flies given that the
species belongs to a genus of basal angiosperms.
Because our study does not exceed the third day of
anthesis, it is plausible that beetles may yet emerge
with viable pollen from rotting flowers. However,
studies consistently report that pollen is carried on
the backs of Dipteran thoraces (Delpino, 1873;
Knuth, 1909; Hilje, 1984; Brantjes, 1980; Hall &
Brown, 1993), indicating that the flies walk on the
utricle wall and have pollen deposited from the gy-
nostemium (Correns, 1891; Knuth, 1909). We found
most fly visitors to A. grandifora were small Phor-
idae, but based on our visual observations large
Calliphoridae and Muscidae were the flies that car-
ried pollen (Table 2). Although Phoridae visitation
was high, we suggest that the Phoridae are not ef-
fective pollinators for this species. Hilje (1984) also
found that the most abundant visitors to A. gran-
difora flowers were Phoridae, but noted that it was
unlikely they were the pollinators because they car-
ried relatively little pollen. He, too, indicated in-
stead larger flies of the families Otitidae and Mus-
cidae. In Java, Cammerloher (1923) indicated that
the pollinators of A. grandifora were large Calli-
phoridae even though he found the principal visi-
tors to be smaller Anthomyidae. The specific dif-
ference between our results and the two previous
studies may reflect differences in geographic loca-
tion, time of year, the availability and diversity of
pollinators, or combinations thereof. Cammerloher
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354 Annals of the
Missouri Botanical Garden
(1923) studies were conducted outside the native
habitat of A. grandifZora, and Hilje (1984) did not
document floral changes and phenology to the level
of detail that we provide.
INSECT INTERACTIONS (PRO\TISION OF REWARDS:
BROOD SITES, MATES, FOOD, PREY)
We found a large community of Phoridae larvae
living on the utricle wall of flowers of Aristolochia
grandiffora indicating oviposition by visiting in-
sects (Table 2). Little is known about provision of
brood sites within the Aristolochiaceae. Asarum
caudatum provides a site for oviposition, but larvae
die (Proctor et al., 1996). Some investigators of
Aristolochia, including those studying A. grandiffo-
ra, who found larvae of Phoridae, Muscidae, and
Drosophilidae within the flowers have shown that
the utricle wall acts as a brood site (Hall & Brown,
1993; Hilje, 1984), but again without larval surviv-
al. Wolda and Sabrosky (1986) studied flies asso-
ciated with the flowers of A. pilosa in Panama and
found no evidence of oviposition. They also noted
that no males were ever reported inside the flowers.
Three studies of different Aristolochia species in
Panama have shown female-biased trapping (Wolda
& Sabrosky, 1986; Carr, 1924; Hime & Costa,
1985), but for A. Iittoralis in Florida, the bias is
mainly to males, presumably attracted by a female
sex pheromone mimic (Hall & Brown, 1993). For
A. grandifZora, insect visitors of both sexes have
been shown (Cammerloher, 1923; Hilje, 1984), in-
dicating that co-habitational sequestration may pro-
mote mating.
It has been suggested that some Aristolochia spe-
cies may provide food rewards to visitors (Knuth,
1909); these include nectar, e.g., A. clematitis, and
mucilaginous stigmatic exudates (Hilje, 1984; Wol-
da & Sabrosky, 1986) although nectaries were not
found in our study species. Whether or not there is
a benefit for the pollinator for its services to the
plant is incompletely known, and rewards may vary
from species to species of Aristolochia and polli-
nator. Within the utricle lives a diverse community
of Coleoptera, Diptera, and Hymenoptera that may
show interesting predator/prey interactions (Hilje,
1984) (Table 2). The flower attracts many predators
to the utricle, possibly in search of protein-rich lar-
vae (Hilje, 1984). The primary predators for both
Hilje (1984) and our study were Staphylinidae (Co-
leoptera). The fact that Staphylinidae did not es-
cape from A. grandifZora flowers until the third day
of anthesis (Table 2) suggests that they may obtain
some benefit, possibly prey, from remaining Phori-
dae larvae. A greater than 50% decrease in larval
counts within day 3 flowers as compared to that of
day 2 also suggests the possibility of predation by
Staphylinidae (Table 2). However, in A. grandifZora
Petch (1924) suggested that a toxic chemical stored
in the utricle wall protects developing maggots from
predation.
CONCLUSIONS
Aristolochia grandiffora is a short-lived flower (3
days) of a continual blooming tropical liana. Its
suite of characters, including form and color of the
perianth, odor (its production and cessation there-
of), floral movements (including trichomes and the
perianth as a whole) with aging, and definitive pro-
togyny, place the flower within the syndrome of sap-
romyiophilous trap blossoms (Faegri & van der Pijl,
1979). We suggest that the most effective pollina-
tors are the large (ca. 5 mm) Diptera (Calliphoridae,
Muscidae, Sepsidae, Heleomyzidae). Although we
did not quantify our observations, they were seen
exiting our study flowers with visible dustings of
pollen on their bodies. The flowers also attract and
trap large numbers of small beetles (Staphylinidae)
and small Diptera (Phoridae); however, we cannot
assess the role of Phoridae and Staphylinidae as
pollinators. Although brood site provision can at-
tract pollinators to the flowers of some Aristolochia
species (Disney & Sakai, 2001; Sakai, 2002a,
2002b), we cannot conclude this from our study.
The large Diptera (Calliphoridae, Muscidae, Sep-
sidae) have larval developments that are typically
more than a week (Smith, 1986), and much longer
than the life of the flower, where the falling flowers
of A. grandifZora in our study were withered and
dried within two days. The small Diptera (Phoridae)
may be able to mature on rotting flowers provided
they remain moist for long enough (e.g., at least a
week (Disney, 1983, 1989)). The flowers do not ap-
pear to provide nectar and we did not determine if
the flies ingested pollen, but those families we
found are not noted for pollenivory, except for pos-
sibly some Muscidae (Larson et al., 2001). Thus,
we do not invoke mutualism between the flies and
the flowers, but rather attraction by deceit (Dafni,
1984). Results from our floral dissections and ob-
servations indicate a reduction in Phoridae larvae
in the presence of large numbers of Staphylinidae
beetles. Based on our observations, it is possible
that the beetles found within A. grandif ora flowers
(e.g., Staphylinidae) may be predatory and feed on
Dipteran eggs and larvae deposited in the flowers,
but this idea remains to be tested.
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Volume 91, Number 2
2004 Burgess et al
Pollination Biology of Aristolochia grandiflora
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Annals of the
Missouri Botanical Garden
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... Flowers of many Aristolochia species are adapted in structure and colour to sapromyophily (carrion-fly pollination). The floral features of sapromyophily can be identified as follows: the brightly coloured inner side of perianth and the discrete (or dim) colouring of the outer side (dark brown, purple, or green); a perianth with a window area; the presence of osmophores (odorous glands); the missing nectar paths and nectar; etc. (Faegri & van der Pijl 1979;Vogel 1990;Proctor et al. 1996;Burgess et al. 2004). Aristolochia species have peculiar, protogynous flowers which can temporarily trap their pollinators, small dipteran insects from different families (Wolda & Sabrosky 1986;Razzak et al. 1992;Sakai 2002;Burgess et al. 2004;Murugan et al. 2006;Trujillo & Sérsic 2006;Valdivia & Niemeyer 2007;Rulik et al. 2008;Berjano et al. 2009;Hipólito et al. 2012;Stotz & Gianoli 2013;Oelschlägel et al. 2015Oelschlägel et al. , 2016Aliscioni et al. 2017;Martin et al. 2017). ...
... The floral features of sapromyophily can be identified as follows: the brightly coloured inner side of perianth and the discrete (or dim) colouring of the outer side (dark brown, purple, or green); a perianth with a window area; the presence of osmophores (odorous glands); the missing nectar paths and nectar; etc. (Faegri & van der Pijl 1979;Vogel 1990;Proctor et al. 1996;Burgess et al. 2004). Aristolochia species have peculiar, protogynous flowers which can temporarily trap their pollinators, small dipteran insects from different families (Wolda & Sabrosky 1986;Razzak et al. 1992;Sakai 2002;Burgess et al. 2004;Murugan et al. 2006;Trujillo & Sérsic 2006;Valdivia & Niemeyer 2007;Rulik et al. 2008;Berjano et al. 2009;Hipólito et al. 2012;Stotz & Gianoli 2013;Oelschlägel et al. 2015Oelschlägel et al. , 2016Aliscioni et al. 2017;Martin et al. 2017). These flowers attract flies primarily by their specific scent (Vogel 1990) and by mimicking sex-specific pheromones (Wolda & Sabrosky 1986) or the same scent components that insects (chloropids) use to find their food sources (Oelschlägel et al. 2015). ...
... According to our study, the flowers mainly open in the first half of the day (08:00-12:00) (Nakonechnaya et al. 2014). Most saprophagous flies and beetles are attracted to flowers by the specific smell that is especially strong in the first hours after flower opening (Burgess et al. 2004;Berjano et al. 2011). It is possible that flowers of A. manshuriensis can also attract insects by smell, but this assumption requires further study. ...
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Background and aims – Interactions of insects with trap flowers of Aristolochia manshuriensis, a relic woody liana with fragmented natural populations from south-eastern Russia, were studied. Pollination experiments were conducted to identify the causes of the poor fruit set in this plant.Material and methods – The study was carried out at two ex situ sites within the natural range of A. manshuriensis in the suburban zone of the city of Vladivostok (Russia). The floral morphology was examined to verify how it may affect the process of pollination in this species. To test for a probability of self-pollination, randomly selected flowers at the female phase of anthesis (day 1 of limb opening) were hand-pollinated with pollen from the same plant. The daily insect visitation was studied. The pollen limitation coefficient and the number of visitors to the flowers were determined. To identify insects that lay eggs on the flowers, the insects were reared from eggs collected from fallen flowers. Both caught and reared insects were identified.Key results – The floral morphology and the colour pattern of A. manshuriensis are adapted to temporarily trap insects of a certain size. The hand-pollination experiment showed that flowers of this plant are capable of self-pollination by geitonogamy and require a pollinator for successful pollination. The positive value (2.64) for the pollen limitation coefficient indicates a higher fruit set after hand-pollination compared to the control without pollination. The number of visitors to the flowers was low (0.17 visitors per flower per day). Insects from three orders were observed on the flowers: Diptera (up to 90.9%), Coleoptera (8.3%), and Hymenoptera (0.8%). Four species of flies (Scaptomyza pallida, Drosophila transversa (Drosophilidae), Botanophila fugax, and Botanophila sp. 1 (Anthomyiidae)) are capable of transferring up to 2500–4000 pollen grains on their bodies and can be considered as pollinators of A. manshuriensis. Data of the rearing experiment indicate that flies of the families Drosophilidae (S. pallida, D. transversa), Chloropidae (Elachiptera tuberculifera, E. sibirica, and Conioscinella divitis), and Anthomyiidae (B. fugax, B. sp. 1) use A. manshuriensis flowers to lay eggs. Beetles were also collected from the flowers, but they were probably not involved in pollination, because no pollen grains were observed on them during our study.Conclusions – Pollinators of A. manshuriensis include mainly Diptera that lay eggs on the flowers. The poor fruit set (2%) in A. manshuriensis is associated with pollen limitation due to the lack of pollinators, as the number of visitors to flowers was extremely low. This may be due to the fact that the flowers of this species are highly specialized on insects of a certain size for pollination.
... Uno de los hábitats más utilizado por este grupo de insectos son las flores e inflorescencias; se han citado como visitantes florales de plantas en familias como Cactaceae (Navarrete-Heredia et al. 2002), Ebenaceae, Magnoliaceae, Monimiaceae, Myristicaceae (Bernhardt 2000), Zingiberaceae (López- García et al. 2011), Heliconiaceae (Frank y Barrera 2010), Aristolochiaceae (Burguess et al. 2004), Araceae (García-Robledo et al. 2004) Annonaceae (Gottsberger 1999) y Arecaceae (Núñez 2014). ...
... Las especies de palmas están dentro de las principales familias de plantas donde hay evidencia de asociación con especies de Staphylinidae (Bernal y Ervik 1996, Núñez 2014) con interacciones como la depredación (Navarrete-Heredia et al. 2002, Burguess et al. 2004, Frank y Barrera 2010), la saprófagia (Sanabria et al. 2008) y relaciones mutualistas como la polinización (Seres y Ramírez 1995, Bernal y Ervik 1996, Gibernau et al. 1999, Gottsberger 1999, Bernhardt 2000, Navarrete-Heredia et al. 2002, Ollerton 2006, siendo esta un intercambio de recursos o servicios (Ollerton 2006). ...
... Los valores de similitud obtenidos tanto con el dendrograma como con el análisis de similitud (ANOSIM) indican especificidad de morfoespecies de Staphylinidae con las inflorescencias de las diferentes especies de palmas donde fueron registradas (Figura 3). En el establecimiento de la especificidad se debe principalmente a los recursos ofrecidos, pues la visita de los insectos a las inflorescencias, está relacionada con la oferta de sitios de cópula, desarrollo de su ciclo de vida y alimentación (Navarrete-Heredia et al. 2002, Amat 2007, cumpliendo así, funciones como la polinización (Seres y Ramírez 1995, Bernal y Ervik 1996, Gibernau et al. 1999, Gottsberger 1999, Bernhardt 2000, Navarrete-Heredia et al. 2002, la depredación (Navarrte-Heredia et al. 2002, Burguess et al. 2004, Frank y Barrera 2010, y la saprofagia (Sanabria et al. 2008). En el presente estudio, y a juzgar por su gran abundancia, Athetini sp.1 actúa posiblemente como polinizador pese a ser también polinívoro (Bernhardt 2000, Sanabria et al. 2008; en este caso el consumo de polen puede ser una interacción positiva para la planta porque mediante este mutualismo facultativo, las palmas se benefician de los servicios de la polinización por parte de las especies de Staphylinidae, a pesar de que cierta parte del polen sea consumido (Strauss 1997) La alta riqueza y especificidad de especies de Staphylinidae que interactúan con Phytelephas tenuicaulis es una posible evidencia de adaptaciones morfológicas y fenológicas, así como de las recompensas ofrecidas a los visitantes florales (Knudsen et al. 2001). ...
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Palm inflorescences are associated with a large number of mainly coleopteran insects, but so far there are no previous studies evaluating the association with visiting Staphylinidae species. Objective: We register the species richness, abundance, the association and specificity of staphylinids in inflorescences of wild palms of the Colombian Pacific. Methodology: Visiting insects of 27 palms were collected in the departments of Chocó, Valle del Cauca and Nariño. Non-parametric ICE, Jacknife 2, Chao 2 and Bootstrap richness estimators were used. The specificity was determined through the analysis of interaction networks, using similarity indexes of Jaccard and ANOSIM. Results: Of the 27 palms species sampled, only 18 were visited by staphylinids and 48 morph species were collected. The most abundant subfamily was Aleocharinae (23 morphospecies). The abundance found was between 1 and 21.956 individuals. Athetini sp.1 recorded the highest abundance (16.068 individuals). Bootstrap estimated 63 morph species; however, no estimator was below the 48-morph species observed. The interactions recorded were 68 out of 864 possible and the network connectivity was 7.8%. Conclusion: The Jaccard and ANOSIM test indicated low similarity in the preference of each species of Staphylinidae indicating high specificity and strong association between this coleopteran and the Colombian Pacific palms.
... The chemical ecology of brood-site deception is best understood in fly-pollinated systems involving the mimicry of dung (oligosulfides) or carrion (cresol and indole; Jürgens et al. 2013;Urru et al. 2011), with recent studies elucidating brood-site mimicry of rotting fruit, sap or yeasts nurtured by these substrates (small aliphatic alcohols and esters; Martos et al. 2015;Stökl et al. 2010). Brood-site deceptive flowers or inflorescences often take the form of kettle traps, to which duped insects are attracted by volatile compounds, and within which they are held captive as a mechanism for ensuring pollen placement or transfer (Bernhardt 2000, Burgess et al. 2004;Chartier et al. 2014;Heiduk et al. 2015). Furthermore, many brood-site deceptive plants are thermogenic, presumably because heat is an important cue attracting flies to dead or decaying substrates (Angioy et al. 2004;Schiestl 2017). ...
... Furthermore, many brood-site deceptive plants are thermogenic, presumably because heat is an important cue attracting flies to dead or decaying substrates (Angioy et al. 2004;Schiestl 2017). Interestingly, neither floral chambers (Meve and Liede 1994) nor heat (Burgess et al. 2004) are necessary to persuade female flies to oviposit into broodsite deceptive flowers. ...
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The attention of the global pollination community has been drawn to food safety and other ecosystem services provided by pollinators, in light of decline in social bee populations. Despite intensified research on bees, recent studies have revealed important contributions of flies to pollination success, reproductive isolation and floral diversification. Diptera is a highly diverse insect order, comprising over 125,000 described species in 110 families and representing a broad spectrum of ecological niches beyond the well-known agricultural pests and blood-feeding vectors of human and animal diseases. Flies are most appreciated as generalized pollinators in alpine habitats (anthomyiids and tachinids) and as specialized pollinators in brood-site deceptive plants that mimic fungi (drosophilids), feces (muscids) or carrion (sarcophagids and calliphorids). Syrphid and bombyliid flies visit many of the same flowers as bees and butterflies do, but with different impacts on plant fitness. Guilds of South African plants have evolved specialized relationships with long-tongued nemestrinid and tabanid flies, thanks to geographic isolation and climatic stability. Studies in Japan highlight the evolution of another plant guild, pollinated by sciarid and mycetophilid fungus gnats, whereas Zygothrica flies (Drosophilidae) pollinate mushroom-like Dracula orchids in Andean cloud forests.
... Several orders of Insecta were recorded as floral visitors of Aristolochia, as Coleoptera, Diptera, Hemiptera, Hymenoptera, and Orthoptera (Valdivia et al. 2007). Burgess et al. (2004) pointed out that Phoridae and Staphylinidae, Diptera and Coleoptera respectively, were the most common visitors of Aristolochia grandiflora Sw. At least 39 families of Diptera were recorded in Aristolochia, but only some groups are known to carry pollen loads and act as pollinators. ...
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Xanthaciura (Diptera, Tephritidae) is a Neotropical genus of Tephritinae compose of 17 species. Currently, to Brazil are recorded eight valid species names. The members of the Tephritinae are marked by their interaction with Asteraceae, as females lay eggs in these plants, where the larvae posteriorly feed and develop on various parts of the plant as capitulum, stem, and bud. Aristolochia is the largest genus of Aristolochiaceae, currently comprising approximately 525 species widely distributed throughout the tropics. There are 92 registered species in Brazil, widely spread in all ecoregions. Several orders of insects were recorded as floral visitors of Aristolochia flowers, as Coleoptera,
... Although Sciaridae, and to a lesser extent Sphaeroceridae, were frequently found in the flowers of A. microstoma, they were not classified as pollinators. The occurrence of significant numbers of non-pollinating Diptera families is not unusual in Aristolochia, since several species attract and trap different Diptera, with only a subset of taxa actually pollinating them (e.g., Cammerloher, 1933;Brantjes, 1980;Hilje, 1984;Burgess et al., 2004;Berjano et al., 2009). The spectrum of flower visitors of A. microstoma is remarkably similar to that of A. pallida (Rulik et al., 2008), another Mediteranean species. ...
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Deceptive flowers decoy pollinators by advertising a reward, which finally is not provided. Numerous deceptive plants are pollinated by Diptera, but the attractive cues and deceptive strategies are only identified in a few cases. A typical fly-deceptive plant genus is Aristolochia , which evolved sophisticated trap flowers to temporarily capture pollinators. Though rarely demonstrated by experimental approaches, Aristolochia species are believed to chemically mimic brood sites, food sources for adult flies, or utilize sexual deception. Indeed, for most species, studies on scent composition and attractive signals are lacking. In this study, we focused on Aristolochia microstoma , a peculiar Greek endemic with flowers that are presented at ground level in the leaf litter or between rocks and are characterized by a unique morphology. We analyzed flower visitor and pollinator spectra and identified the floral scent composition using dynamic headspace and gas chromatography coupled to mass spectrometry (GC/MS). Female and male phorid flies (Phoridae) are the exclusive pollinators, although the flowers are also frequently visited by Sciaridae, as well as typical ground-dwelling arthropods, such as Collembola and arachnids. The carrion-like floral scent mainly consists of the oligosulphide dimethyldisulfide and the nitrogen-bearing compound 2,5-dimethylpyrazine. These compounds together are known to be released from decomposing insects, and thus, we conclude that pollinators are likely deceived by chemical imitation of invertebrate carrion, a deceptive strategy not described from another plant species so far.
... Por último, cabe destacar que algunas especies son consideradas polinizadoras, ya que son fuertemente atraídas por flores que emiten componentes volátiles similares a los de la materia orgánica en descomposición (Burgess et al., 2004;Moré et al., 2018). ...
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Dentro de los dípteros caliptrados (Diptera: Calyptratae), Oestroidea es uno de los clados más relevantes y diversificados en cuanto a sus variados modos de vida y los distintos papeles ecosistémicos que cumplen sus especies. Calliphoridae y Sarcophagidae, dos familias pertenecientes a este grupo, incluyen especies asociadas tanto con ecosistemas forestales y vegetaciones abiertas, como así también a ambientes rurales y urbanos, presentando una notable variabilidad en la estructura de sus comunidades según el grado de intervención antrópica que presenten los ambientes. La mayoría de sus representantes son sarcosaprófagos, se alimentan de materia orgánica animal en estado de descomposición, lo que permite el reciclado y la incorporación de los nutrientes al suelo y al agua. Ambas familias cuentan con especies de importancia médica y veterinaria y, además, tienen destacada relevancia en el ámbito de la entomología forense. El objetivo de esta tesis fue evaluar la diversidad y describir la estructura y dinámica temporal de las comunidades de dípteros de las familias Calliphoridae y Sarcophagidae presentes en áreas naturales y ambientes disturbados por acción del hombre en la ecorregión del Chaco Oriental. En este estudio se incluye un inventario actualizado de las Calliphoridae y Sarcophagidae registradas en el Chaco Oriental, que comprende 79 especies, 34 de las cuales son registras por primera vez en esta ecorregión, siendo siete de ellas endémicas. Tres especies nuevas de la familia Sarcophagidae son descriptas. Catorce especies son primeros registros para Argentina y tres para Paraguay. Sobre la base del material colectado en cinco hábitats típicos de esta ecorregión se comparó a las comunidades de Calliphoridae y Sarcophagidae en términos de riqueza de especies, composición y abundancia entre hábitats y estaciones. La fluctuación temporal de los parámetros comunitarios fue evaluada en cada uno de los hábitats y su relación con variables climáticas. Sobre la base de estas comparaciones se caracterizaron las comunidades, y se asoció la ocurrencia de las especies en relación con las variables espaciotemporales. Esta tesis proporciona una primera comprensión de varios aspectos ecológicos de los ensamblajes de Calliphoridae y Sarcophagidae de la ecorregión de Chaco Oriental, y permite obtener una valiosa descripción de sus patrones de uso de recursos y fluctuación temporal.
... Ceropegia (including the stapelioids) and Aristolochia demonstrate enormous variation in flower size, structure, and scent composition, including some of the most bizarre and fetid flowers known (e.g., the carrion mimicking Stapelia gigantea and Aristolochia grandiflora; Davis, Endress, & Baum, 2008). As in Ceropegia, pollination has been studied in a small sample of Aristolochia species, revealing carrion and fecal mimicry, brood-site deception, and obligate mutualism (Berjano et al., 2009;Burgess, Singfield, Melendez, & Kevan, 2004;Sakai, 2002;Trujillo & Sérsic, 2006), as well as convergent evolution (in A. rotunda) of pollination by chloropid flies attracted to true bug odors (Oelschlägel et al., 2015). If Ceropegia floral evolution features pollination by kleptoparasitic flies, reproductive evolution in Aristolochia is a celebration of scuttle fly ecology. ...
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Coevolutionary processes, which have governed interactions between organisms throughout the history of life, also serve as an engine of ecosystem services for humans. The escalating arms races between plants and herbivores, flowers and pollinators, have generated a cornucopia of foods, raw materials, perfumes, spices, ornamentals, medicines, and drugs. Human history is replete with aesthetic as well as economic inspiration drawn from such plants. Our future may depend on similar inspiration, as we confront novel health, agricultural, and environmental challenges in the face of global change. Summary “Coevolution” was coined to conceptualize escalating arms races between plants and herbivores in evolutionary time, often mediated by natural products. Our current view embraces broader coevolutionary relationships between obligate mutualists, symbionts, parasites, and enemies, which frequently increase rates of diversification in coevolving lineages. Because humans benefit from the foods, materials, and drugs produced by plants in response to reciprocal selective pressures, coevolutionary “escape and radiate” diversification may amplify ecosystem services along with species richness, with humans as beneficiaries. For example, coevolutionary escalation of defenses between Burseraceae and their herbivores resulted in hundreds of resinous tree species, anchoring the trade of copal, frankincense, and myrrh across the ancient world. Examination of three diverse angiosperm orders (Asparagales, Malpighiales, and Gentianales), reveals ecosystem services in the form of alkaloids and hallucinogens, perfumes, spices, coffee, and rubber. Pollinator‐mediated selection by hawk moths and bats gave rise to heavily perfumed “moonflowers” (gardenias and jasmines) with aesthetic appeal to humans, and to immense blooming displays by agave plants, co‐opted by humans as a source of tequila and mezcal. Even when pollinator‐mediated diversification does not arise through coevolution, the resulting biotic richness provides evolutionary insights as well as ecosystem services. The convergent evolution of “kettle‐trap” flowers in species‐rich plant lineages (Aristolochia and Ceropegia) reveals the surprising value of small flies as pollinators and the opportunity to develop biocontrol that leverages floral features attractive to agricultural pests and disease vectors. This article highlights coevolution as a source of ecosystem services and potential solutions to the emerging challenges of global change. Coevolutionary processes, which have governed interactions between organisms throughout the history of life, also serve as an engine of ecosystem services for humans. The escalating arms races between plants and herbivores, flowers and pollinators, have generated a cornucopia of foods, raw materials, perfumes, spices, ornamentals, medicines, and drugs. Human history is replete with aesthetic as well as economic inspiration drawn from such plants. Our future may depend on similar inspiration, as we confront novel health, agricultural, and environmental challenges in the face of global change.
... Some deceptive species with flowers that bear strong colors and scents can attract insects, mainly beetles and flies, that oviposit within the flower while simultaneously leading to pollination [183,200,201]. In one of the most elaborate examples of this kind of pollination, several species of Aristolochia and Asarum (Aristolochiaceae) and Ceropegia (Apocynaceae) attract and temporarily entrap pollinatorstheir flowers usually have strong odors that simulate decaying organic matter [8,153,[202][203][204][205][206][207]. ...
... Some deceptive species with flowers that bear strong colors and scents can attract insects, mainly beetles and flies, that oviposit within the flower while simultaneously leading to pollination [183,200,201]. In one of the most elaborate examples of this kind of pollination, several species of Aristolochia and Asarum (Aristolochiaceae) and Ceropegia (Apocynaceae) attract and temporarily entrap pollinatorstheir flowers usually have strong odors that simulate decaying organic matter [8,153,[202][203][204][205][206][207]. ...
... Some deceptive species with flowers that bear strong colors and scents can attract insects, mainly beetles and flies, that oviposit within the flower while simultaneously leading to pollination [183,200,201]. In one of the most elaborate examples of this kind of pollination, several species of Aristolochia and Asarum (Aristolochiaceae) and Ceropegia (Apocynaceae) attract and temporarily entrap pollinatorstheir flowers usually have strong odors that simulate decaying organic matter [8,153,[202][203][204][205][206][207]. ...
Chapter
When I carefully examined the flower of the wood cranesbill (Geranium sylvaticum) in the summer of 1787, I discovered that the lower part of its corolla was furnished with fine, soft hairs on the inside and on both margins. Convinced that the wise creator of nature had not created even a single tiny hair without definite purpose, I wondered what purpose these hairs might serve. And it soon came to my mind that if one assumes that the five nectar droplets which are secreted by the same number of glands are intended as food for certain insects, one would at the same time not think it unlikely that provision had been made for this nectar not to be spoiled by rain and that these hairs had been fitted to achieve this purpose.