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Reproductive Biology |
2Department of Zoology, Faculty of Science, Kyoto University, Sakyo, Kyoto 606-8502, Japan; 3Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu-cho, Sakyo, Kyoto 606-8501, Japan
Received for publication June 26, 2001. Accepted for publication January 10, 2002.
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ABSTRACT |
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Key Words: ant • Assara • Balanophora • Balanophoraceae • brood site • mutualism • Nacoleia • pyralid moth
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Wiebes, 1979
; Addicott, 1986
; Powell, 1992
; Pellmyr et al., 1997). Plants that offer ovules or seeds as rewards to pollinators include Trollius europaeus (Pellmyr, 1989
) and Lophocereus schottii (Fleming and Holland, 1998
). In contrast, several plant groups are pollinated by insects that breed on floral tissues other than ovules; these groups include Encephalartos (Rattray, 1913
), various palms (Henderson, 1986
), Zamia (Nordstog and Fawcett, 1989
), Eupomatia (Armstrong and Irvine, 1990
), Siparuna (Feil, 1992
), Alocasia (Yafuso, 1993
), and Carludovicoideae (Eriksson, 1994
). In most cases, these plants provide decaying floral parts, such as male inflorescences or corollas, and are pollinated by saprophagous Diptera or Coleoptera. However, we still know very little about the diversity of this unusual pollination system. Here, we report another example in which a plant provides floral decomposition as a reward to its pollinators. We also describe the first case in which moths act as the pollinating parasites breeding on decaying floral tissues.
Balanophora is a genus of root holoparasites that is widely distributed in the tropics and subtropics. In Japan, five species of Balanophora have been reported (Fig. 1), three of which apparently produce only females, suggesting reproduction by apomixis (Akuzawa, 1982
). The reproductive biology of the two remaining monoecious species, B. kuroiwai and B. tobiracola, is still in question. In the only previous study of pollination biology in the genus Balanophora, Govindappa and Shivamurthy (1975)
observed small honey bees, Apis florea, foraging for nectar and pollen. The authors considered the bees pollinators of B. abbreviata in India. However, honey bees have not been reported from the Ryukyu Archipelago (except for a small population on the Amami Islands; Sakagami, 1971
; Kato, 2000
), which covers much of the ranges of B. kuroiwai and B. tobiracola (Fig. 1). As for other genera of Balanophoraceae, some Costa Rican species (e.g., Helosis and Corynaea) are pollinated by tachinid flies (Gómez, 1983
), while an Amazonian species, Lophophytum mirable, is pollinated by small beetles (Chrysomelidae, Nitidulidae, Staphylinidae, and Curculionidae) that are attracted to the strong floral odor (Borchsenius and Olesen, 1990
). The latter species is thought to offer the beetles nutritive tissue for their broods or mating sites, although detailed observations have not been made.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). It bears reduced, pale-pink aboveground parts that are composed of scaly leaves and a fleshy, egg-like inflorescence (Fig. 2). An individual plant produces 2–13 inflorescences in winter, between late December and early January. Each inflorescence has 23.9 ± 5.2 male flowers clustered toward the basal end (mean ± SD, N = 10): The upper part of the inflorescence is covered with small, clavate protective organs (spadicles), among which numerous female flowers are aggregated. Stalkless female flowers lack perianths, and each contains a single ovule. As they flower, slender styles protrude through the spadicles, imparting a velvety surface to the inflorescence. We defined the beginning of female anthesis as the time of style emergence, which begins 2–3 d before the opening of the perianth lobes in male flowers. Nectar is secreted from extrafloral nectaries distributed at the pedicel bases of male flowers. In addition, certain spadicles secrete nectar, which collects as small droplets on the surface of the female part of an inflorescence. Inflorescences emit no detectable odor and last for 4–8 d before most flowers wither and turn brown. Infructescences are formed within 2 mo after flowering, after which the aboveground parts decay. Seeds are minute and numerous and can hardly be distinguished from unfertilized ovules.
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), and in our study site, it blooms from late October to early November. Unlike B. kuroiwai, the aboveground parts are yellow, and male flowers are arranged sparsely among female flowers (Fig. 3). Nectaries are distributed only at the pedicel bases of male flowers. An individual plant produces 1–6 inflorescences that last for 3–5 d.
Study sites and dates
Field studies of B. kuroiwai were conducted in an evergreen primary forest in Hyakuna, Okinawa Prefecture, Japan (25°8' N, 127°47' E, 35 m above sea level [asl]). The forest is situated on a slope of limestone outcrops and experiences a warm subtropical climate. The predominant species in the canopy are Mallotus philippensis (Euphorbiaceae) and Diospyros maritima (Ebenaceae), while Flagellaria indica (Flagellariaceae) and Alocasia odora (Araceae) dominate the understory. In the study site, we found a total of 317 terrestrial inflorescences around the base of the host tree, Pongamia pinnata. Preliminary observations on the habitat and rearing of insects feeding on infructescences were made in January 1998 and April 1999. Intensive field studies of the floral biology and flower visitors were carried out from 8 to 10 January 2000 and from 25 to 31 December 2000. We also conducted pollination experiments during the latter period. On 3 March 2001, we collected fruited infructescences to examine the fertilization of flowers and to rear herbivorous insects. Sample sizes for pollination experiments and insect rearing were kept small in the interest of conservation.
The study site of B. tobiracola was located near the coastline in an evergreen, subtropical forest at Iso, Kagoshima Prefecture, Japan (31°37' N, 130°34' E, 90 m asl). This forest is dominated by Castanopsis cuspidata and Lithocarpus edulis (Fagaceae). In the study site, we found a total of 189 inflorescences parasitizing the roots of Pittosporum tobira and Ligustrum japonicum. We studied the floral biology and flower visitors in this forest from 10 to 11 November 1999. Infructescences were collected on 28 December 1999 and 1 January 2001 for insect rearing.
Nectar secretion
To analyze diurnal patterns of nectar secretion, we collected nectar from inflorescences from which foragers were excluded and measured the volumes and sugar concentrations using micropipettes (Drummond, Pennsylvania, USA) and a pocket refractometer (Bellingham & Stanley, Kent, UK). Inflorescences from two B. kuroiwai plants were banded at their stems with sticky tape (Hagihara, Okayama, Japan) and bagged with nylon netting (0.25-mm mesh; Wataya, Kyoto, Japan) to exclude both flying and nonflying nectar consumers. We marked four male flowers on each of the inflorescences and measured nectar secretion at intervals of 5–9 h for 1 d. Since nectar on female parts was observed as exposed droplets on the surface of the inflorescences, 9–10 droplets were randomly selected and measured during each sampling hour. To see if nectar secretion patterns differed between sexes, data on the two parts were analyzed separately.
Balanophora tobiracola nectar was measured in the same way, using a total of 12 marked male flowers on four plants at intervals of 3–9 h.
Flower visitors
Flower visitors to B. kuroiwai inflorescences were observed for 30 h from 8 to 10 January 2000 during the first season and for 63 h from 25 to 31 December 2000 during the second season. Visitors to B. tobiracola were studied for 30 h from 10 to 11 November 1999. Observations were made over a span of 2–6 h, covering all periods of 24 h. Because ants visited the inflorescences of both species day and night, diurnal patterns of ant visits were studied by counting the number of ants on each of the three inflorescences every 2–3 h for 24 h. Flower visitors other than ants were collected following visitation, although some attempts to collect the visitors were unsuccessful. Red light was used for nocturnal observations to minimize the effect of light on flower visitors.
After field observations, dried specimens of the collected flower visitors were observed under a light microscope, and if pollen grains were found on their bodies, parts of the insects were observed under a scanning electron microscope (HITACHI S-2050, Ibaraki, Japan, 3.0 kV; Fig. 4).
Insect rearing
In order to rear insects feeding on floral tissues, 4–7 inflorescences of each species were collected and kept at room temperature in plastic cases containing moistened vermiculite.
Pollination experiments
In the second year of the study, we selected 18 B. kuroiwai inflorescences that were at the same phenological stage (just before anthesis) for pollination experiments. The nearest-neighbor distance of these inflorescences was >1 m, which avoided multiple sampling within a plant. We applied the following four treatments: (1) three inflorescences were bagged completely with nylon netting to impede access of all flower visitors (no-pollinator treatment), (2) four inflorescences were bagged similarly and self-pollinated by hand following anthesis (hand-selfed treatment), (3) three inflorescences were bagged with nylon netting that had small openings around the stems so that inflorescences could only be visited by ants (ants-only treatment), and (4) four inflorescences were kept unbagged with all male flower buds removed before anthesis (unbagged emasculation treatment) in order to estimate the outcrossing rate. In addition, four inflorescences were marked so that we could analyze natural conditions (open treatment).
Because we could not distinguish ripe seeds by their outward appearance, we examined the percentage of styles that had pollen tubes reaching the ovule and used this as an estimate of seed set. In the laboratory, 1104–2066 female flowers were randomly sampled from each of the treated inflorescences and fixed in FPA (40% formalin, concentrated propionic acid, 50% ethanol; 5 : 5 :90 by volume). We observed pollen tubes in the styles by aniline blue staining under a fluorescence microscope (Martin, 1959
; Fig. 4).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Craneflies, Limonia sp., also visited inflorescences in the evening to lay eggs. Although they were often found among B. kuroiwai, they oviposited around the bases of the plants or on the ground, but not directly on the inflorescence. They rarely touched male and female flowers as they walked among the plants.
Pollen grains of Balanophora have granulate exine and are 14–16 µm wide. They were found attached to the legs and ovipositor of Assara sp. 1 (Fig. 5), to the base of the proboscis of Nacoleia sp., and to the legs of Leptothorax sp.
Visitors to B. tobiracola inflorescences were mainly ants and cockroaches (Table 2). Ants (Paratrechina flavipes and Aphaenogaster sp.) visited inflorescences during the day and in the evenings to harvest nectar. We did not observe them moving between separate plants. In the evenings, two species of cockroaches (M. satsumana and Periplaneta japanna) visited inflorescences (Fig. 6); all individuals of the former species were brachypterous adults and those of the latter were larvae. They visited multiple plants in succession, and while harvesting nectar and pollen from male flowers, they touched anthers and stigmas with its legs and mouth. Pollen grains were found attached to the tarsi and mouthparts of Margattea satsumana and to the legs of Paratrechina flavipes and Aphaenogaster sp.
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Pyralid larvae also fed on infructescences of B. tobiracola. From infructescences collected on 1 January 2001, an average of 3.4 ± 1.7 individual pyralid moths, Assara sp. 2, emerged within 12 wk after collection (N = 7).
Pollination experiments
There was a significant reduction in the percentage of styles with developed pollen tubes (hereafter, fertilization rate) only when no pollinators visited the inflorescences (t test, P < 0.05; Fig. 10). Although the unbagged emasculation treatment yielded more developed pollen tubes than the open treatment, on average, low fertilization rates in two unbagged emasculated inflorescences (1.7 and 1.1%) suggest that effective cross-pollination occurs variably and that pollination success in open-treated flowers generally depends on self-pollination. Gametophytic self-incompatibility cannot be ruled out from our results of the hand-selfed treatment. However, Balanophora flowers were shown to be at least sporophytically self-compatible. The low fertilization rate in the hand-selfed treatment might have resulted from failure to apply enough pollen onto the female flowers. The result of the ants-only treatment indicated that ants were capable of pollinating Balanophora flowers. The observed difference in fertilization rates between the ants-only and open treatments might have resulted from the increased movement by ants that had trouble getting out of the bagged inflorescence.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Akuzawa (1982)
observed that the most frequent visitors to Balanophora inflorescences in Japan were ants. However, ants are regarded as poor pollinators because their small size and smooth integument preclude effective contact with anthers and stigmas (Faegri and van der Pijl, 1979; Proctor, Yeo, and Lack, 1996
). Moreover, ants are reported to reduce the viability of pollen with antibiotic substances secreted from their metapleural glands (Beattie et al., 1984
; Hull and Beattie, 1988). Nevertheless, recent studies document noteworthy cases in which ant pollination leads to viable seed set (Hickman, 1974
; Wyatt, 1981
; Svensson, 1985
; Peakall and Beattie, 1991
; Gómez and Zamora, 1992
; Gómez et al., 1996
). In B. kuroiwai, selective exclusion experiments showed that ants were capable of pollinating flowers and that antibiotic secretions were not always fatal to pollen survivorship. In both Balanophora species that we studied, ants visited the inflorescences throughout the nectar-secreting hours and came in frequent contact with plant reproductive organs. In turn, ants were not observed making sequential visits to inflorescences and are known to forage repeatedly on the same plant or flowers (Sudd and Franks, 1987
; Hölldobler and Wilson, 1990
). Therefore, we conclude that ants are the geitonogamous pollinators of Balanophora inflorescences. In many reported cases of ant pollination, pollen transfer by ants leads to high levels of geitonogamy (Svensson, 1985
; Peakall and Beattie, 1991
; Gómez and Zamora, 1992
; Gómez et al., 1996
).
Cockroaches are generally regarded as omnivorous scavengers and detritus feeders (Rentz, 1996
). However, cockroaches can also function as pollinators, as in the tropical woody climbing species Uvaria elmeri (Annonaceae), whose pollen and stigmatic exudate were harvested (Nagamitsu and Inoue, 1997
). Several observations also suggest that cockroaches feed on floral resources (Perry, 1978
; Proctor, Yeo, and Lack, 1996
; Rentz, 1996
). In our study, cockroaches visited inflorescences of Balanophora and were found with pollen grains on their bodies (Table 2). However, they are flightless and are less likely to cause effective cross-pollination between separate plants. Thus, we regard cockroaches to be more likely responsible for geitonogamous pollination.
With respect to B. kuroiwai, we consider pyralid moths to be the most likely cross-pollinators, and not mere parasites, for the following reasons: (1) they were the only flying visitors that carried pollen grains on their bodies and had contact with anthers and stigmas; (2) the observed low frequency of effective cross-pollination corresponded with the low frequency of moth visits; and (3) the larvae fed on the swollen, fleshy axes of the inflorescences and did not cause seed destruction. These observations suggest that the relationship between B. kuroiwai and pyralid moths is a new example of pollination mutualism in which vegetative tissue of the inflorescences is offered as a reward to herbivorous pollinators. Although we did not conduct pollination experiments in B. tobiracola, the resemblance in floral biology and the assemblage of flower visitors suggests that B. tobiracola has a breeding system similar to that of B. kuroiwai.
The classical examples of mutualism involving plants and their pollinating parasites, i.e., fig–fig wasp and yucca–yucca moth systems, have evolved into obligate reciprocal dependency. However, the mutualism between Balanophora and pyralid moths is not as highly specialized, because (1) Balanophora inflorescences secrete nectar during the day when moths are less active and (2) the adults emerge between April and May when no Balanophora inflorescences are available, suggesting that other host plants are available. Specialization may be prevented in Balanophora–pyralid moth mutualism, presumably due to the low frequency of effective outcrossing and the presence of pollinating ants, which assure a certain level of self-pollination. Such unspecialized mutualism is documented in Lithophragma plants and Greya moths, for which Thompson and Pellmyr (1992)
argued that selection does not favor specialized mutualism where there are effective co-pollinators. A similar situation can be seen in the Brazilian palm, Orbignya phalerata, which is pollinated by the nitidulid beetle Mystrops mexicana laying eggs in male inflorescences, while the plant is partly wind-pollinated (Anderson, Overal, and Henderson, 1988
).
In the only previous study of pollination biology in the genus Balanophora, small honey bees, Apis florea, pollinated B. abbreviata in India (Govindappa and Shivamurthy, 1975
). In the subalpine forests of Taiwan, dioecious B. spicata secreted nectar and were actively visited by Asian honey bees, Apis cerana, searching for nectar and pollen during the month of September (A. Kawakita, personal observations). It is possible that the basal lineage of Balanophora has adapted to pollination by honey bees, or simply bees. However, Asian honey bees have not been recorded on the Ryukyu Archipelago, with the exception of a small population found on the Amami Islands (Sakagami and Fukuda, 1971
; Kato, 2000
) and are not observed in many populations of B. kuroiwai and B. tobiracola. Moreover, Balanophora spp. bloom in winter when bees are least active. It is likely that the unique pollination system of Balanophora is an evolutionary consequence of the lack of effective pollinators during the winter months in subtropical forests. The reason why these Balanophora species bloom in winter is still unknown. Physiological constraints may account for this, since the flowering and fruiting seasons of Balanophora species (November–April) do not overlap with that of their hosts, Pongamia (May–November), Macaranga (April–July), Pittosporum (April–October), and Ligustrum (June–November).
Mutualisms in which plants provide brood sites for pollinators are not well documented, especially when they involve plants that sacrifice ovules or developing seeds (Pellmyr, 1989
; Thompson and Pellmyr, 1992
; Fleming and Holland, 1998
). In contrast, mutualism involving plants that offer decaying floral parts to the pollinators has evolved more repeatedly (Henderson, 1986
; Nordstog and Fawcett, 1989
; Armstrong and Irvine, 1990
; Feil, 1992
; Yafuso, 1993
). Such mutualism may be more widespread than currently known because the rewards provided by the plants are dispensable and not nourished after anthesis. Future pollination biology studies, as well as phylogenetic analyses, are needed to understand the diversity of pollination mutualism and the conditions favoring it in the course of evolution.
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FOOTNOTES |
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4 Author for reprint requests (kawakita{at}terra.zool.kyoto-u.ac.jp)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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