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Tropical Biology |
Smithsonian Tropical Research Institute, Apartado 2072, Ancón, Balboa, Republic of Panama
Received for publication May 4, 2001. Accepted for publication September 7, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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120 species distributed throughout the tropics and subtropics. All the Aristolochia species studied so far are pollinated by saprophagous flies of different families, which are presumably deceived by floral odor. Flowers of many species have trap-and-release mechanisms. The flowers attract and imprison pollinators during the female stage first day of flowering and release them after anther dehiscence. Pollination systems of A. maxima and A. inflata are different from those of other Aristolochia in lacking trap mechanisms. Furthermore, the pollinators oviposit in the flowers, and their larvae grow on the fallen, decaying flowers on the ground. Therefore, the plants have a mutualistic relationship with their pollinators. Self-compatible A. inflata is pollinated by Megaselia sakaiae (Phoridae, Diptera). The pollinator may be specialized to Aristolochia flowers, which is the only substrate for larval development. On the other hand, self-incompatible A. maxima is pollinated by Drosophila spp. (Drosophilidae, Diptera), which utilize Aristolochia flowers as a breeding site only occasionally. This pollination mutualism might have evolved from deceit pollination.
Key Words: Diptera • Drosophilidae • flower-breeding pollinator • Panama • Phoridae • tropical forest
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Many insects primarily visit flowers for pollen and nectar, but some pollinators visit flowers for mating and oviposition.
Pollination systems involving pollinators breeding on the flowers or inflorescence of the plant have been found in different plant groups. The pollination systems can be subdivided into three categories. First of all, plants that offer ovules or developing seeds as a breeding site to pollinators are known only from limited plant genera, Ficus (Moraceae) (Janzen, 1979
; Wiebes, 1979
), Yucca (Agavaceae) (Baker, 1986
), Trollius (Ranunculaceae) (Pellmyr, 1989
), Lithophragma (Saxiflagaceae) (Pellmyr and Thompson, 1992
), and possibly Piper (Ollerton, 1996
), probably because of the high cost for plants to sacrifice part of their ovules for pollinator development. The second category includes plants pollinated by pollen feeders developing on living flowers, mostly thrips (Thysanoptera). Thrips, agricultural and horticultural pests, are often found in flowers of many wild plants and are thought to rarely contribute to pollination (Mound and Marullo, 1996
; G. Francesco, the University of Milan, Italy and D. W. Roubik, Smithsonian Tropical Research Institute, Panama, unpublished data). They are regarded as principal pollinators only in limited plant species of Annonaceae (Webber and Gottsberger, 1995
; Momose, Nagamitsu, and Inoue, 1998
), Moraceae (Sakai, 2001)
, Winteraceae (Thien, 1980
; Pellmyr et al., 1990
), Zamiaceae (Mound and Terry, 2001)
, and others. The third group involves pollinators that oviposit on floral parts other than ovules. Their larvae develop on plant reproductive organs such as male inflorescences and corollas after pollination. The pollinators, usually dipteran (see DISCUSSION) or coleopteran (e.g., Rattray, 1913
; Henderson, 1986
; Pellmyr and Thien, 1986
; Norstog and Fawcett, 1989
; Armstrong and Irvine, 1990
) insects, may have evolved many times from nonpollinating herbivores feeding on living or dead plant reproductive organs. Our knowledge of these pollination systems, which involve most diverse plant and pollinator groups, is still fragmentary.
The present study reports pollination systems of Aristolochia maxima Jacq. and A. inflata H. B. & K., in which flower-breeding flies pollinate their host plants. Aristolochia, the most diverse genus of the family Aristolochiaceae, contains 120 species distributed throughout the tropics and subtropics (Mabberley, 1995
). Their zygomorphic flowers are diverse in size, shape, and color, but based on the same groundplan (Endress, 1994
). The perianth of the flowers has only three sepals. The sepals are united into a tubular calyx, of which three parts can be distinguished. The basal part is a chamber (utricle) around the fused styles, stigmas, and anthers (collectively known as the gynostemium) (Fig. 1). The utricle is connected to a tube ending with an expanded limb, which is often colorful and thought to visually attract pollinators.
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; Petch, 1924
; Brues, 1928
; Lindner, 1928; Brantjes, 1980
; Costa and Hime, 1983
; Wolda and Sabrosky, 1986
; Hall and Brown, 1993
). Their flowers are strongly protogynous. On the day the flowers open, they attract flies primarily by odor, and trap the flies inside the utricle. On the second day, the anthers dehisce and the flies are released with pollen load. Because the pollinators belong to saprophagus groups and it is unlikely that they depend on floral nectar and pollen of Aristolochia, the pollination system is regarded as deceptive. The pollination systems of A. maxima and A. inflata reported in this study are unique in the genus in that their pollinators oviposit and develop on the flowers. This paper shows that deceit pollination is not always the case with Aristolochia and suggests potential diversity of the plant–pollinator interactions in the genus. |
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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80-yr-old second growth up to 40 m in height. The canopy layer is dominated by Anacardium excelsum (Anacardiaceae) and Luehea seemannii (Tiliaceae). I used a 42-m tall tower crane with a 51-m jib permanently installed in the park (Parker, Smith, and Hogan, 1992
) to reach lianas growing on the forest canopy.
Aristolochia maxima and A. inflata are relatively common species in Central America (Pfeifer, 1966
). Both are lianas that often grow in thickets and secondary forests. The former is distributed from southern Florida to Panama and the latter from southern Mexico to Panama. At the study site, most flowers of the both species opened in the canopy layer of the forest 10–30 m above the ground, while some of the flowers of A. maxima occurred on thick stems in the understory. Preliminary observation and insect collection were conducted in October to December 1999. In 2000, Aristolochia maxima and A. inflata flowered from mid-October to early December and from early November to late December, respectively. In this flowering season, three individuals (M1, M2, M3) of A. maxima and one (I1) individual of A. inflata, within reach of the crane (1 ha) were studied. Specimens of the plants were deposited at the Smithsonian Tropical Research Institute (Summit Herbarium [SCZ]) and Panama University (PMA) (voucher specimens: A. maxima: S. Sakai 535; A. inflata: S. Sakai 551).
Calyx tubes of A. maxima are coriaceous, creamy white tinged with purple, and totally glabrous outside. The utricle is 3.5 x 2.0 cm and is obovoid with a dorsal dent on the distal third (Fig. 1c, d). The inner surface is mostly white with purple dots and covered with nectarial transparent hairs, especially on the dorsal surface and on the broad purple band above the gynostemium (Fig. 1d). The hairs are 1.2 mm long, are very sticky, and cling to each other. At the bottom around the base of the gynostemium, the utricle has a clear translucent "windowpane" fringed by a thin purple band on the inner surface (Fig. 1d). The other end of the utricle is connected with a glabrous tube, which expands into a limb (Fig. 1c). The limb is purple with yellow patches and thick purple hairs on the inner surface. The limb is erect when the flower opens. In the late afternoon of the first day of flowering, it gradually bends inward over the entrance of the tube, and the hairs on the limb wither. Pollen is very sticky, usually forming large clumps in the utricle after anther dehiscence and on the bodies of pollinators. Pollen grains are spherical, 30 µm in diameter.
Flowers of A. inflata are smaller and more delicate. The calyx is white and glabrous outside. The utricle is 1.3 x 1.0 cm and is ellipsoid (Fig. 1a). The flower also has a windowpane fringed by a reddish-brown band at the bottom of the utricle around the gynostemium (Fig. 1b). Inside the column of the gynostemium, transparent sticky liquid is secreted. The inner surface of the distal dome of the utricle is spongy, with suppressed hairs (Fig. 1b). The soft transparent hairs secrete nectar. The glabrous tube is connected with the glabrous limb, which is narrowly triangular, yellow inside, white outside. In this species, a calyx does not show clear changes in appearance from the outside in the course of flowering. Pollen is powdery. The inside of the utricle is sometimes dusted with pollen throughout after anther dehiscence. Pollen grains are spherical, 20 µm in diameter.
Fruits of A. maxima and A. inflata matured in early March and late January, respectively. They dehisce acropetally, and seeds are dispersed by wind. Mature fruits of A. maxima are cylindrical and large, measuring 12 x 5 cm, with 520 ± 140 seeds (N = 10) (mean ± SD, throughout the text), while that of A. inflata is narrow, cylindrical, and strongly six-ribbed, measuring 3.5 x 1.0 cm, with 140 ± 60 seeds (N = 15).
Pollination experiment
Pollination experiments were conducted on M1 in A. maxima and I1 in A. inflata. In both species, flowers for the experiments were enclosed in mesh bags before anthesis except flowers used for open-pollinated control. In A. maxima, geitonogamous pollen from second-day (male-stage) flowers on the same plant and cross pollen from M3 was applied to 13 and 12 first-day (female-stage) flowers, respectively, on 2 November at 0700 to 1100. Sixty-nine bagged flowers were left without hand-pollination as the bagged treatment. As control, 164 open-pollinated flowers were tagged and their fruit set was monitored. In A. inflata, geitonogamous pollen was applied to in total 19 1-d flowers on 24 and 27 November at 0700 to 1000, and 31 bagged flowers were left without hand-pollination as the bagged treatment. As the control, 109 open-pollinated flowers were also observed. Fruit set of the flowers was monitored until fruit dispersal. Differences in fruit set 2 wk after flowering between treatments were statistically examined with Fisher's exact test (one-sided) using the SAS system (SAS, 1988
).
Observation and collection of flower visitors
Insects in utricles were collected by sampling whole calyces. The insects were preserved in 50% alcohol or in dried state, and parts of them were stored at the Smithsonian Tropical Research Institute and Panama University. Some utricles with flies inside were brought to a laboratory, and behavior of the flies was observed through a hole made in the utricle.
To examine pollen loads of insects leaving flowers of A. maxima after anther dehiscence, first-day flowers of M1 were collected in the afternoon and placed in a mesh bag and kept overnight. The following morning, flies in the bag were sampled, and the numbers of pollen grains on their bodies were counted under a microscope. The numbers were compared among the following three insect groups: Coleoptera, Phoridae, and Drosophilidae. In A. inflata, insects were collected from second-day flowers on I1 at 0600 to 0700 to examine the pollen on their bodies.
Phorid and drosophilid flies were counted in flowers at different flowering stages. For A. maxima, insects in first-day flowers were counted at 0600–0700 and 1030–1130 and second-day flowers at 0600–0700 (20 flowers each); for A. inflata, first-day and second-day flowers were examined at 0600–0700 and 1100–1200 (10 flowers each).
Rearing
Twenty-four flowers of each species collected directly from inflorescences were kept in plastic containers with wet sand for 1 mo or more to examine insect species that had oviposited on the flowers. Insects that emerged from the flowers were collected and kept in alcohol.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Flower visitors
The most abundant insect families among flower visitors in A. maxima (N = 921) were Phoridae (53%), Drosophilidae (19%) (Diptera), and Staphylinidae (18%) (Coleoptera) (Table 2). All the flies of Phoridae except two belonged to a single species, Megaselia sakaiae. Most of them (99.7%, N = 376) were female. All (N = 177) of the drosophilid flies were various species of Drosophila, including D. aff. bromeliae, D. aff. florae, D. neocardini, D. malerkotliana, D. mesostigma, D. equinoxialis, and D. latifasciaeformis. Fifty-eight percent of Drosophila spp. (N = 69) were female. Megaselia flies were observed licking nectar secreted from hairs inside the utricles of A. maxima and A. inflata. I could not observe behavior of Drosophila in a utricle, because cutting the utricle disturbed flies and most of the flies left it immediately.
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All 210 insects found in utricles of A. inflata were Megaselia sakaiae. All of the individuals examined were female (N = 108). An individual of M. sakaiae from a second-day flower carried 66 ± 78 pollen grains, and 81% of the flies had 10 or more pollen grains on the body.
In A. maxima, utricles of most second-day flowers were already empty at 0600–0700, and 2.6 ± 2.2 phorid and 0.25 ± 0.43 drosophilid flies were found in first-day flowers. The number of drosophilid flies increased thereafter and was 0.65 ± 1.19 at 1030–1130 (Fig. 2). On the other hand, first-day flowers were almost empty, and 4.2 ± 1.7 phorid flies were still found in second-day flowers in A. inflata. There were 5.8 ± 1.9 phorids in first-day flowers at 1100–1200, and second-day flowers were empty (Fig. 2).
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15 d after flowering. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), it has rarely been demonstrated by hand-pollination. On the other hand, A. inflata is self-compatible because flowers pollinated with self-pollen showed high fruit set. The difference in self-compatibility may explain much higher fruit set of A. inflata (18.7%) than that of A. maxima (2.4%) in open-pollinated controls (Table 1).
Self-compatibility seems to be more common in the genus (Petch, 1924
; Razzak, Ali, and Ali, 1992
). Self-pollinated flowers set fruits in A. elegans [= A. littoralis] (Petch, 1924
). Fruit set of bagged flowers was not significantly different from that of open-pollinated flowers in A. bracteolata (Razzak, Ali, and Ali, 1992
). Cleistogamy is suspected in A. serpentaria (Pfeifer, 1966
). A single fruit from a bagged, untreated flower indicates that autogamy can occur in A. inflata, but pollinators are essential for successful fertilization even in this self-compatible plant, considering the fact that bagged flowers had lower fruit set than the open-pollinated controls (Table 1). Furthermore, cross-pollinated flowers of A. maxima and self-pollinated flowers of A. inflata had much higher fruit set than the open-pollinated controls of each species, suggesting that limitation of compatible pollen is an important proximate factor in determining fruit set in the two species (Table 1).
Megaselia sakaiae, the exclusive flower visitor to A. inflata, is the primary pollinator of A. inflata (Table 4). Visitation frequency of the flies (5.8 ± 1.9 flies/flower) and the number of pollen grains on the flies (66 ± 78 pollen grains/fly) were high enough to explain fruit set of 18.7% and 140 ± 60 seeds in a fruit in self-compatible A. inflata. Most eggs of the fly in A. inflata were found on and around a gynostemium, which had sticky exudate inside. Probably the exudate sticks to the flies when they partially put their bodies into the gynostemium to oviposit, and functions as glue to attach powdery pollen grains to the pollinator. The other flies reared in A. inflata, Zygothrica sp. and Drosophila aff. bromeliae, are thought to oviposit from outside of the flower, as most of them were reared not in the utricles but in the limbs (Table 3). Besides, Zigothrica sp. was frequently observed on a limb of A. inflata (personal observation), but never in a utricle. The thin tube of the calyx may exclude larger visitors than phorids.
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Considering the amount of body pollen on different flower visitors, Drosophila spp. are the primary pollinators of A. maxima. To fertilize a single flower of A. maxima, hundreds of cross-pollen grains are needed, since the species is self-incompatible, and a fruit contains as many as 520 ± 140 seeds. Thus a single visit of a pollinator with a large pollen load from another conspecific plant may be more important than visits of many insects with small pollen loads, most of which are from flowers on the same plant. Among insects that emerged from second-day flowers, only drosophilid flies had >100 pollen grains on their bodies. However, one cannot conclude that Drophila flies are the exclusive pollinators. Beetles, mostly Staphylinidae, were as abundant as Drosophila flies on A. maxima flowers, although 82% of the beetles collected on second-day flowers carried <10 pollen grains. Besides, the visit frequency of Phoridae is up to 8.8 times as high as that of Drosophilidae (Table 2), although they likewise had little body pollen. The beetles and phorids may also play a role in pollination of A. maxima.
Why do pollinator flies visit flowers of A. maxima and A. inflata? Probably odor and, to a less extent, floral color function as proximate attractants for pollinators as suggested in other species (Vogel, 1990
). What, then, prevents the flies in the utricle from leaving until the following day? Except for the limb in A. maxima, the calyx tube does not change in shape or position during flowering, and the limb does not keep flies from flying away. Actually, flies can leave the flower, as they were observed to leave first-day flowers when the flower was disturbed. However, most flies leave the flower only after anther dehiscence. One of the rewards the plants offer to the pollinators is a breeding site. It was confirmed that the pollinators, M. sakaiae and Drosophila spp., breed on flowers of A. inflata and A. maxima, respectively. Apparently, this is the first report of the pollinators breeding on Aristolochia flowers, although it was suggested as early as 1839 by Graham. While Hime and Costa (1985)
have already described Megaselia breeding on Aristolochia flowers, the contribution of the flies to pollination is unknown. The other reward for the pollinators is nectar secreted from the inner surface of the utricle. It must also be important especially in A. maxima, in which oviposition of the pollinators occurs less frequently than in A. inflata (Table 3). Thus, the pollination system can be regarded as a mix of nectar reward and decaying tissue as breeding sites.
Most studies on pollination systems of Aristolochia explain that the pollinator flies visit flowers because they are deceived by floral odor that mimics carrion, feces, fungi, etc. (Proctor, Yeo, and Lack, 1996
). Flowers of some species have been documented to have elaborate trap-and-release mechanisms, such as the hairs on the tube of A. grandiflora. The hairs allow flies to enter the utricle but not to exit and wither when the flower switches its sex from female to male so that the flies can leave the flower with pollen loads (Cammerloher, 1923
). Many Aristolochia species are known to have nectaries on the inner wall of the utricle (Cammerloher, 1923
; Petch, 1924
; Daumann, 1959
; Costa and Hime, 1983
), but the nectar is regarded as food to ensure survival of the imprisoned pollinators during captivity rather than a reward (Vogel, 1998
). Petch (1924)
observed many dead flies in flowers of A. gigas [= A. grandiflora], a species that does not provide any food to imprisoned flies. In a few Aristolochia species, nectar secreted at the floral entrance takes part in pollinator attraction (Daumann, 1959
; Vogel, 1998
).
The pollination system of A. maxima and A. inflata is different from the other Aristolochia species studied so far in that the plant does not deceive the pollinators but provides a breeding site for them. The nectar secreted from the inner surface of the utricle of A. maxima and A. inflata may also have more than a supplemental role. Megaselia sakaiae has been found only on Aristolochia flowers (Disney and Sakai, 2001
). It is possible that the nectar is essential for their ovule development and oviposition. In contrast with M. sakaiae, which has a high female ratio among flower visitors (99.7%), the proportion of females in Drosophila spp. was much lower (58%). There were far fewer Drosophila flies reared in flowers than M. sakaiae. The Drosophila flies might visit flowers not only to oviposit, but also to copulate and/or feed on the nectar. Lack of trap-and-release mechanism in both plants may reflect more mutualistic relationships of the plants with their pollinators than those of deceptive Aristolochia species.
The diversity within the Phoridae (2500 species) is high (Disney, 1994
). Adult flies are found in damp places, on or near many kinds of decomposing plants and animal matter, on flowers and fungi, and in rodent burrows, ant and termite nests, and caves. In addition to those habitats, larvae are known from seed capsules, feces, and many kinds of gastropods and insects (Peterson, 1987
; Disney, 1994
), but phorids ovipositing and breeding on living flowers are only known from a single plant host in Liliaceae other than Aristolochia (Disney, 1994
). Baumann (1978)
reported that 77 species of phorid flies have been recorded visiting 60 species of flowers, although they have rarely been recorded pollinating plants other than Aristolochia (but see Young, 1984
; Singer and Cocucci, 1999
).
The Phoridae is one of the dipteran families frequently found visiting Aristolochia flowers (Carr, 1924
; Brues, 1928
; Iwata, 1975
; Baumann, 1978
; Hime and Costa, 1985
; Hall and Brown, 1993
). Some of the flies were reported to oviposit (Petch, 1924
) and reproduce on Aristolochia flowers (Hime and Costa, 1985
). Although some phorid species recorded from Aristolochia flowers were also found from fungi, ant and wasp nests, feces, insect larvae and pupa, etc. (Robinson, 1971
), M. sakaiae is thought to be specialized to Aristolochia flowers (Disney and Sakai, 2001
). Megaselia sakaiae and M. aristolochiae, a close relative of M. sakaiae breeding on Aristolochia labiata flowers, have not been found in other places (Hime and Costa, 1985
; Disney and Sakai, 2001
).
Interestingly, two other species of Phoridae were found to breed on fallen Aristolochia flowers at the study site (Disney and Sakai, 2001
). Wingless females of Puliciphora pygmaea (Phoridae) were frequently observed on fallen flowers of A. maxima and A. inflata, and adults of both sexes were reared from the flowers (Table 4; Disney and Sakai, 2001
). The other species reared in fallen flowers of A. maxima was M. metropolitanoensis, a close relative of M. sakaiae and M. aristolochiae (Disney and Sakai, 2001
). Although adults have not been observed in the field, females of the species are thought to oviposit on fallen flowers of A. maxima because the species was not bred from flowers collected directly from the plant (Disney and Sakai, 2001
). Puliciphora pygmaea and M. metropolitanoensis could also be specific to Aristolochia flowers, as breeding sites other than fallen Aristolochia flowers are not known in both species. The pollinator of A. inflata might arise from phorid flies breeding on fallen Aristolochia flowers. A mutualism similar to that of A. inflata and M. sakaiae may also have evolved in a neotropical grass: Soderstrom and Calederón (1971)
suggested that two species of phorid flies visited and bred on Pariana (Gramineae) and perhaps were responsible for its pollination as well.
In contrast with Phoridae, Drosophilidae have rarely been reported as the predominant visitors or pollinators of Aristolochia flowers. The family is large with 3000 described species, and more than half of these belong to the genus Drosophila (Weeler, 1987
). Breeding sites and specificity for the sites in Drosophila are diverse. Their breeding sites include decomposing fruits and flowers and other plant materials, living leaves (mining in leaf tissue) and fungi (Carson, 1971
). Many Drosophila species are known to oviposit exclusively or occasionally on flowers and flower buds (Pipkin, Rodríguez, and León, 1966
; Brncic, 1986
; Vilela and Pereira, 1992
). The host flowers are usually bulky and fleshy. Drosophila flies may lay eggs within the floral tissue with a sharp ovipositor. Oviposition in the floral tissue rather than on a surface may be the reason why eggs of Drosophila could not be found in Aristolochia flowers.
The extent to which Drosophila flies depend on flowers as a breeding site and their host specificity vary greatly among species. For example, cosmopolitan species mostly associated with fallen fruits and garbage, including Drosophila melanogaster, D. ananassae, and D. busckii, occasionally breed on living flowers (Carson, 1971
; Brncic, 1986
). Other Drosophila species in the flavopilosa group are only known from flowers of one plant species, and they depend on flowers for both adult food and breeding site (Pipkin, Rodríguez, and León, 1966
; Vilela and Pereira, 1992
). In general terms, however, the species associated with flowers are seldom specialized to a single host species (Brncic, 1986
).
In contrast to A. inflata, which is pollinated by flies of a single species specialized to Aristolochia, A. maxima is pollinated by diverse species of Drosophila. Drosophila aff. bromeliae and D. aff. florae collected from A. maxima flowers belong to groups bromeliae and florae, respectively, that are "generalist flower-breeders," which breed on flowers of variety of species including Datura (Solanaceae) and Ipomea (Convolvulaceae) (Patterson and Stone, 1952
; Carson, 1971
). Drosophila latifasciaeformis visiting A. maxixma were also bred from Borassus flowers (Palmae) (Brncic, 1986
). Other Drosophila flies are opportunistic flower breeders. Drosophila cardinoides visiting and bred from A. maxima flowers has been reared from flowers of Araceae, Heliconiaceae, Solanaceae, Zingiberaceae, as well as fruit of Annonaceae and Clusiaceae, and mushrooms (Pipkin, 1965
; Brncic, 1986
). Drosophila malerkotliana and D. equinoxialis are common flies often reared from fallen fruits (Sevenster and Alphen, 1996
). Apparently A. maxima flowers are not the exclusive breeding site for the pollinator Drosophila species.
Plants pollinated by drosophilid flies breeding on repropductive organs of the plants have been reported only in a few taxonomic groups such as Alocasia spp. (Araceae) (van der Pijl, 1953
; Yafuso, 1993
) and Nypa fruticans (Palmae) (Essig, 1973
). The pollination system of A. maxima is quite different from that of Alocasia and Nypa in that the pollinators include many species and that the flowers are not the major breeding site of the pollinator flies. In A. maxima, nectar may play a more important role than oviposition sites in keeping the flies in the utricle. It may be related to a lack of specialization of the plant and pollinators.
Interaction between A. maxima and A. inflata
Since flowering periods and flower visitors of A. maxima and A. inflata considerably overlap, they have the potential to affect each other positively or negatively through flower visitors and pollinators. The flowering period of A. maxima precedes that of A. inflata by 2 wk, and M. sakaiae, pollinators of A. inflata, breeds on flowers of A. maxima as well as those of A. inflata. Flowering of A. maxima may contribute to population growth of the pollinators and have a positive effect on pollination of A. inflata. In contrast, the frequent visits of M. sakaiae to A. maxima may reduce the pollination success of A. inflata through interspecific pollen transfer and may decrease pollinator visits. Different timing of pollinator release and attraction (Fig. 2) is a possible mechanism for reducing interspecific pollinator movement, but the effect of a decrease in pollinator visits is unknown. In contrast, pollination success of A. maxima is unlikely to be affected by A. inflata. Aristolochia inflata flowers are thought to have little importance as breeding sites for the pollinators of A. maxima, because of the low host specificity of the pollinators and the rarity of Drosophila flies bred in A. inflata. Flowering of A. inflata may hardly reduce visit frequency of the pollinators to A. maxima, as the pollinators of A. maxima rarely visit flowers of A. inflata.
Dipteran pollinators breeding on flowers
Although not many plants have been reported to be pollinated by flies breeding on the flowers or inflorescences, it is clear that the pollination by flower-breeding insects has evolved more than once in different plant groups. Among myophilous plants, Trollius europaeus (Ranunculaceae) is unique in that developing seeds are the main reward for pollinators. The plant is pollinated by four anthomyiid species (Anthomyiidae, Diptera), which feed on pollen and nectar, mate in the flowers, and complete larval development in the seeds (Pellmyr, 1989
). In the other dipteran pollinators breeding on the flower, larval development occurs mostly on decomposing flowers or inflorescences after pollination. Tropical aroids, Alocasia spp. (Araceae), are pollinated by Colocasiomyia spp. breeding on inflorescences of the plants (Drosophilidae) (van der Pijl, 1953
; Yafuso, 1993
). Feil (1992)
observed that gall midges (Cecidomyiidae) pollinated flowers of Siparuna spp. (Monimiaceae) and that larvae of the midges develop on the flowers. Gall midges are also pollinators of Artocarpus interger (Moraceae), a species in which larvae of the midge grow by feeding on fungus mycelia on male inflorescences (Sakai, Kato, and Nagamasu, 2000)
. Similar plant–gall midge mutualism might occur in Pariana (Gramineae) (Soderstrom and Calederón, 1971
), Theobroma and Herrania (Sterculiaceae) (Young, 1985, 1986
), and Piper (Piperaceae) (Ollerton, 1996
).
The present study is the first report of pollination mutualism of plants and flower-breeding polliantors in Aristolochia, in which scaptomyiophily by deceit is thought to be dominant (Endress, 1994
). Future studies may reveal more Aristolochia species pollinated by flies breeding on the flowers, because only a limited number of species in this large genus have been studied in detail in a natural habitat. Fly larvae on flowers have been observed in other species (A. saccata, Graham, 1839
; A. elegams [= A. littoralis], Petch, 1924
; A. labiata, Hime and Costa, 1985
; A. gigantea, S. Sakai, personal observation). In most tropical Aristolochia species, the calyx and gynostemium are shed immediately after flowering and rapidly decompose (Pfeifer, 1966
). These floral characteristics might be a preadaptation for the pollination mutualism.
Origin of the apparent mutualism awaits further studies on pollination of more Aristolochia species and their phylogenetic relationships. It is possible that the pollinators breeding on Aristolochia flowers evolved either from pollinators deceived by flowers or from flies breeding on flowers without pollinating them. It is interesting that plants pollinated by flies breeding on inflorescences after pollination are also found in Araceae, in which many species are deceptive sapromyiophily (Endress, 1994
; Proctor, Yeo, and Lack, 1996
). It is also uncertain whether the supposed mutualisms in A. inflata and A. maxima have evolved independently in Aristolochia or whether shifts of pollinators occurred during the course of evolution. Considering that the pollinators of A. inflata can also reproduce on flowers of A. maxima and vice versa, a two-way shift between nonpollinating floral herbivores and pollinators could occur. Coevolution of Aristolochia and their pollinators may involve dynamic pollinator shifts between unrelated insects and differ markedly from that of the plants pollinated by ovule parasites, in which pollinator shifts rarely occur and even then only between closely related insect species (Machado et al., 2001)
.
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FOOTNOTES |
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2 Current address: Graduate School of Human and Environmental Studies, Kyoto University, Sakyo, Kyoto, Japan 606-8501 (sakai{at}bio.h.kyoto-u.ac.jp
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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