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Reproductive Biology |
2Department of Biology, Graduate School of Sciences, Kyushu University, 812-8581 Fukuoka, Japan; 3Entomological Laboratory, Faculty of Agriculture, University of the Ryukyus, 903-0213 Okinawa, Japan
Received for publication June 6, 2002. Accepted for publication October 3, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Alocasia • Araceae • Colocasiomyia • Drosophilidae • floral odor • pollination
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). However, far fewer studies have focused on the effects of floral scents.
Van der Pijl (1961)
pointed out that there are many similarities in floral scents, as well as other floral characteristics, among plants putatively pollinated by the same class of pollinators (pollination syndromes). Later, variations in floral scents that corresponded with differences in pollinator types or species were reported among related species or even within a species (Dodson et al., 1969
; Gregg, 1983
; Pellmyr, 1986
; Groth et al., 1987
; Bergström et al., 1992
; Dobson et al., 1997
). Recently, many researchers have investigated which compounds in floral scents are responsible for pollinator attraction, both ethologically (Haynes et al., 1991
; Heath et al., 1992
; Dobson et al., 1999
; von Helversen et al., 2000
) and physiologically (Thiéry et al., 1990
; Gabel et al., 1992
; Raguso et al., 1996
; Raguso and Light, 1998
). Compared to studies on these proximate causes, investigations on the impact of floral scents on plant fitness are quite rare (Galen, 1985
; Ackerman et al., 1997
).
In studies addressing the impact of visual cues, two approaches have been used to answer how variation in floral display size affects pollinator behavior and consequent reproductive success (Kudoh and Whigham, 1998
). One is to examine the correlation between the size of floral display and pollinator visitation or fitness gains by using phenotypic variation in size of floral display. The other is to examine pollinator responses or changes in fitness gains in relation to manipulations of size of floral display. These general approaches are expected to be also effective for elucidating the functions of olfactory cues. However, it is difficult to discriminate the effects of olfactory cues from those of visual cues (Dafni et al., 1997
). First, floral scents are produced by the petals, androecium, and/or are contained in nectar (Dobson, 1994
), and thus variations in olfactory cues might closely correlate with visual cues. Second, manipulation of scent production, for example by reducing scent-producing tissues, should also affect visual cues.
Alocasia odora C. Koch (Araceae) provides an ideal opportunity to overcome the above difficulties. The spadix (inflorescence) of A. odora emits strong scents, as in other araceous plants (Williams, 1983
; Williams and Whitten, 1983
; Dafni, 1984
; Gerlach and Schill, 1991
; Dobson, 1994
; Kite, 1995
; Kite and Hetterschieid, 1997
), and species-specific pollinator flies, Colocasiomyia alocasiae and C. xenalocasiae (Diptera: Drosophilidae), are attracted to the spadices by these scents (Yafuso, 1993
). The upper part of the spadix forms a well-developed sterile appendix (Fig. 1; Hay, 1998
), as in species of several tribes (Areae, Arisaemateae, Colocasiae, Schismatoglottideae, Thomsonieae, and Zomicarpeae [Mayo et al., 1997
]), and this appendix is thought to be the main source of floral scents in A. odora (Hay, 1998
) and other araceous plants (but see Patt et al., 1995
; Vogel and Martens, 2000
), such as Arum italicum, Typhonium divaricatum, Alocasia portei, A. macrorrhiza (Vogel, 1990
), Sauromatum guttatum (Skubatz et al., 1996
), and Dracunculus vulgaris (Seymour and Schultze-Motel, 1999
). The spadix of A. odora is surrounded by a spathe (leaf) on three sides, and this whole unit is surrounded by leaves, which makes it unlikely that the inflorescence provides any source of visual cues to the pollinators at a distance. Thus, olfactory stimuli from the spadix can be manipulated and their effects on pollinators can be investigated without concurrently affecting visual cues.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The flies are attracted to the spadices by strong, peculiar scents emitted by the spadices during their blooming sequences. At our study site, the flowering time of A. odora extends from November to July, with a peak blooming season from March to April. During a single flowering season, each reproducing ramet bears several spadices, which usually flower at different times. The spadix consists of four parts: a female zone (consisting of pistillate flowers), a male zone (consisting of staminate flowers), a sterile zone between them, and a terminal appendix (Fig. 1b; Honda-Yafuso, 1983
; Yafuso, 1994
; Hay, 1998
). The sterile zone appears to have two regions (Hay, 1998
): the lower whorl of the zone consists of united staminodes, each with a central hole, and the upper consists of structures resembling sterile synandria. During flowering, the whole spadix is surrounded by a leafy green spathe. The spathe is divided into a thicker lower portion housing the female zone and the lower sterile zone and a thinner upper portion housing the upper sterile zone, the male zone, and the appendix. When the inflorescence opens, the tightly convoluted upper spathe loosens with its limb erect, which enables pollinator flies to visit the female zone hidden below the male and sterile zones (Fig. 1). After 1 or 2 d in pistillate phase, the spathe constriction tightens the spadix at the sterile zone, preventing movements of flies between female and male zones, and then the staminate phase begins. In this way, self-pollination is minimized (Yafuso, 1993
). The staminate phase lasts for 2–3 d. The flies seem to remain on spadices throughout the flowering period.
Many flies in the genus Colocasiomyia have been reported to breed mono- or oligophagously in the spadices of aroids in the genera Aglaonema, Alocasia, Colocasia, and Homalomena (Carson and Okada, 1980
; Honda-Yafuso, 1983
; Toda and Okada, 1983
; Okada and Yafuso, 1989
; Yafuso and Okada, 1990
; Tsacas and Chassagnard, 1992
), occasionally with two different species living together on the same spadix. Colocasiomyia alocasiae and C. xenalocasiae are such "synhospitalic" species on the spadices of A. odora. They breed monophagously on A. odora (but can also be found on A. cucullata, which is believed to be an exotic introduction to Okinawa Island [T. Miyake and M. Yafuso, unpublished data]).
We conducted all experiments on A. odora on Okinawa Island, Japan, during the flowering season of 2000–2001. Since 99.5% of floral visitors we collected in the experiment examing pollinator attraction in the field were the two species of Colocasiomyia, we focused on only Colocasiomyia flies throughout this study.
Pollinator attraction to different parts of the spadix
Field experiment
The experiment was conducted in the latter half of May 2000 at the campus of the University of the Ryukyus and along the roadside of Adaniya, Kitanakagusuku, located 5 km northeast of the university. In both sites, we studied five spadices from different individual plants. The spathes of the spadices were cut from the peduncles just before anthesis, and each bare spadix was covered with a transparent polyethylene bag. The spadix was partitioned by tying the bag with strings into the following three parts: the appendix (upper-I part), the male zone with the upper sterile zone (upper-II part), and the female zone with the lower sterile zone (lower part) (Fig. 1b). The constriction of the sterile zone separates the upper and the lower parts. When tying the bag, we inserted a strip of sponge (12 mm in width) between the inflorescence and the bag to avoid damaging inflorescences and to prevent the floral visitors from moving between the parts. We made a window (2 x 2 cm) in each part of a bag through which pollinators could approach an inflorescence. Two to six days later, we collected the spadices after closing the windows with plastic tape. We brought the spadices to the laboratory and collected visiting flies in each part by aspiration.
The Friedman test combined with the Scheffé method for multiple comparisons was used to examine whether the number of attracted flies differed among the three parts of the spadix. We treated each inflorescence as a block in the statistical analysis.
Laboratory experiment
We collected 15 spadices in the pistillate phase from different individuals growing on the campus of the university. By anesthetizing with CO2, we collected all the visiting flies on the spadix, then put them into a plastic bottle (10 cm height and 6 cm diameter) until the experiment.
To test the attraction of each spadix part, we made volatile-attraction fly traps. We cut the spadix into the three parts (upper-I, upper-II, and lower parts) and put each part into a separate glass bottle (13 cm height, 5 cm diameter; GB in Fig. 2). The silicone plug of each bottle had two air passages: one was for the inflow of the air (approximately 900 mL/min) coming from the air pump (LUNG GX100, GEX Corporation, Osaka, Japan), and the other was the outlet for the air containing volatiles from the spadix parts. The outlet was jointed with a Tygon tube, which lead to a plastic catching bottle (10 cm height and 6 cm diameter; CB in Fig. 2). We fixed the catching bottle upside down at a height of 17 cm above the table surface and made a rectangular hole (20 x 15 mm; H in Fig. 2) in the cap, from which volatiles filling the catching bottle were emitted.
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The Friedman test and the Scheffé method for multiple comparisons were used to test if the number of visiting flies differed among the four catching bottles. We treated each trial as a block in the statistical analysis.
Fly-aggregating part of spadix
To examine where on the spadix the pollinator flies stay during flowering, we collected 10 spadices on 12 May 2000 on the campus of the university: five spadices were at the pistillate phase and five at the staminate phase. We cut each spadix at the constriction and collected the flies in each part by covering the separate parts of spadices with gauze nets. This enabled us to compare the number of the flies between the upper and lower parts. We brought the spadices to the laboratory, identified the flies to species in each portion of the spadix, and counted them.
For each phase, a nested ANOVA (Sokal and Rohlf, 1995
) was used to test for differences between fly species and between spadix parts.
Correlation between pollinator number and appendix size
We collected 27 spadices on 18 May 2000 at Sueyoshi Park (located 5 km southwest of the university) and 18 spadices on 21 May 2000 at the campus of the university. In each case, we cut off spadices in the pistillate phase and covered them with gauze nets. We brought the spadices to the laboratory, identified the flies to species, and counted them. We cut off the appendix of each and weighed it.
To test for a significant correlation between pollinator number and appendix size, Kendall's method was used. The analysis was performed using the StatView (version 5.0) statistical analysis software package (SAS Institute, Cary, North Carolina, USA).
Fruit set of manipulated inflorescences
To investigate the importance of olfactory attraction of flies on female reproductive success in A. odora, we compared fruit sets between spadices from which we had removed a part and intact (control) spadices. On 13 and 14 April 2001 at the campus of the university, we carefully unfolded the spathes of inflorescences just before anthesis. We subjected the spadices to three different treatments, using 25 spadices for each treatment. In one treatment, we cut the appendices (upper-I removal); in the second, we cut off the upper half of the spadix consisting of the appendix, the male zone, and the upper part of the sterile zone (upper-I and -II removal); in the third (control), we cut off the tip of the appendix (approximately 5 mm) to control for the effect of cutting. To establish the importance of pollinators for fruit set, 25 spadices were bagged throughout their flowering (bagged treatment).
We collected maturing infructescences on 16–21 June. Two infructescences could not be found and were excluded from the results. Differences in fruit set among the treatments were tested by the Kruskal-Wallis test, combined with the Scheffé method for multiple comparisons (Sokal and Rohlf, 1995
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 = 13.632, P < 0.05): the upper-I part, consisting of the appendix, attracted significantly more flies than did the upper-II part, consisting of the male zone and part of sterile zone, and the lower part (Fig. 3).
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2 = 35.490, P < 0.001): bottles with the upper-I part attracted significantly more flies than did either the bottle with the lower part or the control bottle (Fig. 4).
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= 0.342, P < 0.05 at Sueyoshi Park; = –0.106, P = 0.54 at the campus). The number of C. xenalocasiae, on the other hand, was positively correlated with appendix size at the campus site, and a marginally significant correlation was observed at the Sueyoshi Park site ( = 0.251, P = 0.0608 at Sueyoshi Park; = –0.409, P < 0.05 at the campus).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Dafni, 1984
; Vogel, 1990
; Gottsberger and Silberbauer-Gottsberger, 1991
; Lack and Diaz, 1991
; Dobson, 1994
; Kite, 1995
; Skubatz et al., 1995
; Beath, 1996
; Kite and Hetterschieid, 1997
; Seymour and Schultze-Motel, 1999
; Stránsk
and Valterová, 1999
; Gibernau and Barabé, 2000
; Gibernau et al., 2000
), which are thought to advertise flowers to pollinating insects, and beetles and flies are known as particularly important pollinator taxa (Mayo et al., 1997
; Bernhardt, 2000
; Larson et al., 2001
). In the present study, we show that the appendix is the main olfactory attractant in the spadix of A. odora, with attractiveness being shown also in the male zone of the spadix (Figs. 3 and 4). Scent production in Araceae, as well as thermogenesis, is reported to occur mainly in appendices (Vogel, 1990
; Skubatz et al., 1996
; Seymour and Schultze-Motel, 1999
), and Skubatz et al. (1996)
found that the excised appendix of Sauromatum guttatum attracted more than 30 insect species, although they did not investigate the attractiveness of the other parts of the spadix. Our findings support previous suggestions that floral scents responsible for pollinator attraction are emitted mainly by the appendix. We note that in genera where appendices are absent, floral odor is produced in the male zones (Vogel, 1990
; Mayo et al., 1997
). Anatomical observation of Alocasia's inflorescences (Vogel, 1990
; Hay, 1998
) together with our results suggest that the appendix is an organ derived from staminate flowers that evolved as a specialized pollinator-attracting structure by emitting volatiles.
Several studies have suggested that the variation in appendix lengths within species or between related species is based on pollinator attraction. For Colocasia esculenta, which belongs to a genus closely related to Alocasia (Hay, 1998
), Matthews (1995)
claims that interpopulational variation in the appendix length can be explained by the differing dependence on pollinators among populations. Spadices of Philodendron melinonii (Araceae) have a shorter male zone than those of P. solimoesence, a sympatric species with which it shares pollinators, and attracted fewer pollinating beetles (Gibernau et al., 2000
). Both species lack appendices and only their male zones emit odor. Furthermore, Gibernau et al. (1999)
found a positive correlation between the length of sterile male zone of P. solimoesence and the number of visiting beetles. In Arisaema flavum (Araceae), which is assumed to be autogamous, the rudimentary appendix implies that selective pressures for pollinator attraction are being exerted on appendices of outcrossing congeners (Vogel and Martens, 2000
). In A. odora, it is mainly the appendix that attracts the two pollinators, Colocasiomyia alocasiae and xenalocasiae. The correlation between the appendix size and the number of flies attracted, however, was not strong (Fig. 6). One reason for this may be the small sample sizes, i.e., the number of spadices we were able to obtain at any one time was rather low (N = 18 and 27). In addition, the patchy distribution of the flies in natural populations may have influenced our results, in that the visiting flies probably came from nearby inflorescences that were on their way to withering, from developing infructescences or from the ground nearby the infructescences where they had emerged. At any of these points, a closer inflorescence can be more attractive to the flies than a farther inflorescence with a larger appendix.
Alocasia odora–Colocasiomyia relationship
In Alocasia odora, the flies attracted by floral scents emitted by the upper part of a spadix went down to the lower part that was in the pistillate phase (Fig. 5, Table 1), where they mate and lay eggs (Yafuso, 1994
) and seem to feed on something. Thus, the primary attractant (i.e., reward, Faegri and van der Pijl, 1979
) of A. odora for the two Colocasiomyia species is spatially separated from the secondary attractant, i.e., the odors of the appendix. The reward appears to be a secretory substance associated with pistillate flowers, but the exact nature of the food has yet to be determined. When newly emerged flies were fed only water, most died within 3 d in the laboratory, but less than 20% of the flies died within 3 d if a spadix in the pistillate phase was supplied as food (T. Miyake and M. Yafuso, unpublished data). Thus, pistillate flowers provide nutrients for fly survival.
Before the staminate inflorescence of A. odora started, flies in the lower (pistillate) part moved to the upper part (Fig. 5, Table 1), where they remained during the subsequent staminate phase and again seemed to feed. They also mate during this phase, but only C. alocasiae lays eggs on the upper part of the spadix (Yafuso, 1994
). Then, the flies leave the spadix to find another in the pistillate phase. The movements of the flies within a spadix and between plants, along with the dichogamy of the spadix, promotes efficient outcrossing. However, the proximate causes of the movement within the spadix remain to be solved.
Alocasia odora has been known as the exclusive host plant for both Colocasiomyia alocasiae and C. xenalocasiae, although we found them in the spadix of the exotic introduced species A. cucullata in a small, private floricultural farm in a northern part of Okinawa Island, where the two Alocasia species grow side by side (T. Miyake and M. Yafuso, unpublished data). The odor emitted by the A. odora appendix appears to serve three olfactory functions for the flies: as a feeding cue, a sexual attractant, and an oviposition signal, as implied for Peltandra virginica (Araceae) (Patt et al., 1995
). In addition, a number of other Colocasiomyia species use specific araceous plants as mating sites and as exclusive host plants in Southeast Asia (Carson and Okada, 1980
; Honda-Yafuso, 1983
; Okada and Yafuso, 1989
; Yafuso and Okada, 1990
; Tsacas and Chassagnard, 1992
; Yafuso, 1994
), suggesting that Colocasiomyia species can recognize and discriminate their suitable araceous host-plant species. Although there is little available information on the pollination effectiveness of Colocasiomyia on their host plants, it is likely that as a result of the mating-site and breeding-site recognition of Colocasiomyia flies, species-specific floral scents provide a reproductive isolation mechanism by preventing interspecific pollen transfer when related species coexist sympatrically.
Effects of floral scents on plant fitness
Many insects respond to intraspecific variation in floral scents, which can thus affect patterns of insect visitation. Differences in floral scents can be used to evaluate the amount of rewards in a flower at a close distance (Dobson, 1991
; Dobson et al., 1999
; Dobson and Bergström, 2000
), but qualitative differences are also thought to provide variable attractiveness for pollinators (Dodson et al., 1969
; Galen and Kevan, 1983
; Pellmyr, 1986
; Schiestl et al., 1997
; Schiestl and Ayasse, 2001
). Floral scents are thus expected to have an influence on plant reproductive success through advertising. However, there have been only few studies on the relationship between floral scents and plant reproductive success. In Polemonium viscosum (Polemoniaceae), Galen (1985)
showed differences in seed set between two phenotypes with distinct floral scents: plants with skunky-scented flowers set more seeds in a fly-rich site and plants with sweet-scented flowers set more seeds in a bumble-bee-rich site. In another case, Ackerman et al. (1997)
found no difference in pollinarium removal and fruit set between scented and scentless phenotypes of a deceptive orchid, Tolumnia variegata (Orchidaceae). These studies, however, did not directly examine the olfactory display size, as we did here for A. odora.
Our findings show both that the number of flies attracted to the spadix is correlated with the size of the appendix and that removal of the appendix, which is the primary source of floral scents, significantly reduced fruit set in A. odora (Fig. 7). As far as we know, this is the first report of the magnitude of olfactory display on plant reproductive success. Although male fitness was not investigated, it might also be reduced by a decrease in pollinator numbers, because as much as a spoonful of pollen remaining at the constriction of the spadices implies that male function is limited by pollinator visits (Stanton and Preston, 1988
).
In both our field and laboratory experiments on pollinator attraction to A. odora, we found that the male zone adjacent to the appendix also played a role in attracting pollinator flies (Figs. 3 and 4). Because the field experiment (Fig. 3) was set up before flower opening, this attractiveness could not have been because of the passive absorption of volatiles from the appendix onto the male zone, but rather was the result of the attractiveness of the male zone itself. Our findings that fruit set was lower when the male zone was removed with the appendix may also support this conclusion (Fig. 7), although inflorescences in which the male zone is removed are prevented from self-pollinating, which can otherwise occasionally occur (bagged treatment in Fig. 7; Yafuso, 1993
).
Our study provides experimental evidence that the appendix of the araceous species A. odora plays a crucial role in attracting pollinator flies and thereby impacts fruit set and shows that this attraction is attributable to volatiles emitted from the appendix. Investigation of the volatile compounds responsible for pollinator attraction is needed to confirm that they are emitted from the appendix. Chemical studies of floral scents and determination of key compounds attracting the pollinators in partnerships between other Araceae plants and Colocasiomyia species found in Southeast Asia (Carson and Okada, 1980
; Honda-Yafuso, 1983
; Toda and Okada, 1983
; Okada and Yafuso, 1989
; Yafuso and Okada, 1990
; Tsacas and Chassagnard, 1992
) will provide insight into the selective pressures underlying speciation in these groups of plants and insects.
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FOOTNOTES |
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4 Author for reprint requests (tmiyascb{at}mbox.nc.kyushu-u.ac.jp
)
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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