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(American Journal of Botany. 1999;86:56-61.)
© 1999 Botanical Society of America, Inc.

A new pollination system: dung-beetle pollination discovered in Orchidantha inouei (Lowiaceae, Zingiberales) in Sarawak, Malaysia1

Shoko Sakai3,a and Tamiji Inoue4,a

a Center for Ecological Research, Kyoto University, Sakyo-ku, Japan 606-8502


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Lowiaceae, a family of the Zingiberales, comprise 11 species in the single genus Orchidantha. Here we present the first report on the pollination of Lowiaceae and describe a new system of dung-beetle pollination from Sarawak, Borneo. Orchidantha inouei has a zygomorphic flower located just above the ground. Observations revealed that the plant is visited frequently and is pollinated by scarabaeid dung beetles, mainly members of the genus Onthophagus. All four species of Onthophagus collected on O. inouei have also been caught using traps baited with dung or carrion in Borneo. Onthophagus was presumably attracted to the dung-like odor of the flower. Pollination of O. inouei is different from other examples of beetle pollination in that its flower provides neither reward nor protected space. Dung beetles are excellent at following a particular dung scent. Orchidantha is the only genus that includes species lacking floral nectar. It is interesting that this deception pollination using dung beetles was found in Zingiberales, in which all known species have mutual and specialized relationships with their long-distance, but costly, pollinators—bees, birds, and bats.

Key Words: deceit pollination • dung beetle • Lowiaceae • mixed dipterocarp forest • Sarawak • Zingiberales


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The order Zingiberales is a group of monocotyledons, entirely restricted to the tropical regions (Dahlgren, Clifford, and Yeo, 1985). The order includes the following eight families, Lowiaceae, Musaceae (banana family), Heliconiaceae, Strelitziaceae (bird-of-paradise), Zingiberaceae (ginger), Costaceae, Cannaceae, and Marantaceae, all of which are quite distinctive with many unique and highly modified morphological characteristics (Kirchoff, 1991).

Pollination of Zingiberales has been studied in various species, especially in neotropical regions. Most species of Zingiberales have conspicuous and specialized flowers providing a large amount of floral nectar and attracting nectar-feeding vertebrates such as birds and bats or long-tongued bees. All the species in Zingiberales in which pollinators have been studied attract long-distance reliable pollinators (Table 1).


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  		Table 1. Pollinators of the Zingiberales. Pollinator groups found in the families and sources of the data are shown.

 
Lowiaceae are the only family in the Zingiberales in which pollination has not yet been studied. The family has 11 species in a single genus, Orchidantha, including a new species O. inouei to be described from Sarawak, Malaysia (Nagamasu and Sakai, 1999). The very restricted distribution of each of these species suggests that the genus may be a relict group (Fig. 1; Larsen, 1993). Because of the unpleasant odor Holttum (1970) suspected fly-pollination in O. fimbriata. Here we present the first report on the pollination of Lowiaceae from Sarawak, Malaysia.



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  		Fig. 1. Geographic distribution of the genus Orchidantha with the names of species in the area (from Larsen, 1993 ). ? indicates the unknown locality in Borneo of the only known collection of O. borneensis . Our study site, Lambir Hills National Park, Sarawak (4°20' N, 113°50' E), is shown by a solid circle.

 

   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The study site was a primary mixed dipterocarp forest in Lambir Hills National Park, Sarawak, Malaysia (4°20' N, 113°50' E, altitude 150–250 m, Fig. 1, Inoue et al., 1995). Two populations of Orchidantha inouei along a public trail to a waterfall (Sungai Latak) in the park were studied from 8 May to 27 June 1996. One population near a small tributary stream had ~15 reproductive individuals, and the other located in a gap in the forest had four reproductive plants.

Flower visitors to O. inouei were observed directly (38 h in total) or recorded by video cameras (66 h in total) from 24 May to 27 June 1996. The total records include observation from anthesis at 0730 to 0100 on the following day for 104 h in total. For observation at night, a light was covered by a sheet of red cellophane to minimize disturbance. Some of the flower visitors were collected, and their body pollen was examined under a binocular microscope.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Orchidantha inouei is a perennial herb, 0.7–1.3 m high with tufted leaves (Fig. 2). Inflorescences are sometimes embedded in the ground, and flowers are produced just above the ground. One to a few flowers per individual open sporadically. The flower possesses a column of tissue called "the prolongation" that unites the locular region of the ovary embedded in the litter on the ground and the perianth on the ground surface. The prolongation, a part of the ovary, is ~10 cm long and 4 mm in diameter (Kirchoff and Kunze, 1995). The flower is zygomorphic with a dark purple labellum with a central white line (Fig. 3). Five stamens and a three-lobed stigma are hidden under two lateral petals (Fig. 4). The top of the stigma is fringed by hairs, which receive pollen. The ventral surface of the stigma is mucilaginous with a transparent secretion.



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  		Fig. 2–6. Orchidantha inouei and its flower visitors. Figs. 2, 3 are courtesy of H. Nagamasu. 2. Overall aspect of a plant along a public trail in Lambir Hills National Park (height 1.2 m). 3. Flowers located just above the ground and a flower bud (c). A flower has five stamens and a stigma hidden under the two white lateral petals (a, 1.6 x 0.6 cm), and a purple labellum with a central white line (b, 8 x 3.5 cm). Scale = 5 cm. 4. Lateral petals (a), three-lobed stigma (b), and stamens (c) and with a labellum cut away. The ventral surface of the stigma is mucilaginous with a transparent secretion. The top of the stigma is covered with pollen. Scale = 5 mm. 5. An Onthophagus aurifex beetle with white pollen showing under lateral petals, under which the tip of the stigma is seen. Scale = 5 mm. 6. Paragymnopleurus pauliani inserting its head under lateral petals. Scale = 1 cm.

 
Anthesis occurs at 0730 with a moderately strong, unpleasant odor and anthers dehisce at the same time. Flowers do not secrete floral nectar. The odor is continuously released until midnight, gradually getting weaker at night. The flowers usually wither within 24 h, but sometimes remain until the next morning. Dichogamy was not found. Fruits of O. inouei are fusiform and ~6.5 x 2.5 cm, developing under the ground.

The only flower visitors that crawled under the lateral petals, where the stigma and anthers were hidden, were dung beetles (Coleoptera, Scarabaeidae) (Figs. 5–7Go). These dung beetles belonged to two genera, Onthophagus and Paragymnopleurus. Tiny dipterans, hemipterans, and coleopterans (Table 2) were observed flying around the flower. They sometimes landed on the lateral petals, but neither entered under the tepals nor carried pollen.



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  		Fig. 7. Diurnal patterns of visits by Onthophagus and Paragymnopleurus to Orchidantha inouei flowers.

 

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  		Table 2. A list of flower visitors collected from O. inouei with the number of individuals with body pollen in parentheses.

 
In the daytime, the small dung beetles, Onthophagus spp. (body length 6–10 mm), usually flew straight toward a flower, landed on the labellum, and climbed up along the central white line (Figs. 5, 8). They crept under the lateral petals slowly and sometimes moved back and forth, apparently confused, under the tepals. After a short while, they crept out and flew away. The beetles stayed under the tepals for 56 ± 32 s (N = 14). Visits of Onthophagus were not observed after dark (Fig. 7). Out of 30 visits of Onthophagus beetles observed, beetles made contact with the stigma in 18 cases, and white pollen on the beetle coming out of the flower was clearly recognized in 16 cases (Fig. 7). Pollen was usually attached to the dorsal surface of the head and thorax, but sometimes pollen covered the whole dorsal surface (Fig. 5). However, pollen was not transferred from the stamen to the stigma of the same flower by a single visit of Onthophagus without a pollen load. We collected four Onthophagus beetles that had crawled under the tepals and found that all of them carried pollen on their body (Table 2). The stigmas of some flowers were found to be covered with pollen (Fig. 4), probably following successful pollination.



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  		Fig. 8. Longitudinal sections of Onthophagus (upper-left) and Paragymnopleurus (lower-left) visiting a flower of O. inouei , and a ventral view of a dissected flower with the labellum cut away are shown. Scales = 5 mm.

 
The larger dung beetles, Paragymnopleurus (body length 13–20 mm) visited the flower from early morning until the evening (Fig. 7). They often landed on the ground or leaves near the flower and waddled toward the flower. They climbed the labellum and sometimes inserted their heads under the sepals for 17 ± 15 s (N = 11) (Figs. 6, 8), but they usually gave up exploring the source of the odor and left the flower after a short time. We often found several Paragymnopleurus aggregating around the base of the plant. Among 27 visits of Paragymnopleurus, they touched the stigma on 12 occasions (Fig. 7), but we could only observe pollen on the body on two occasions, even when the beetle crept under the tepals (Fig. 7). In the two cases, pollen was recognized on the dorsal surface of the head. We collected ten Paragymnopleurus beetles, three of which had been observed inserting their heads under the tepals, and none of them carried pollen (Table 2).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The results of our observations revealed that the major pollinators of Orchidantha inouei were dung beetles, Onthophagus (Coleoptera, Scarabaeidae). Onthophagus is a member of the tunneling guild of dung beetles, which dig a vertical tunnel below the dung pat (or carrion) and transport the dung to the bottom of the burrow. The stored dung is then used for adult feeding and raising larvae (Cambefort and Hanski, 1991). All four species of Onthophagus (O. aurifex, O. fujii, O. vulpes, and O. waterstradti) collected on O. inouei were also caught using traps baited with dung or carrion at different sites in Borneo (Hanski, 1983; Ochi and Kon, 1995; Kikuta et al., 1997). The flowers did not secrete nectar, as has also been reported for other species of Lowiaceae (Kirchoff and Kunze, 1995). We could not find any other reward for the pollinators in the flowers, and Onthophagus feeding on pollen was neither observed nor has been previously recorded. The mucilaginous secretion on the ventral surface of the stigma of O. inouei may function as a glue to hold deposited pollen on the pollinator. Onthophagus was presumably deceived by O. inouei with its dung- or carrion-like odor. The fact that the odor did not attract dung or carrion flies of Muscidae, Calliphoridae, and Scatophagidae suggests that the odor is not a precise imitation of that of dung or carrion. Flower visitors other than dung beetles, dipterans, hemipterans, and coleopterans, cannot be pollinators because they touch neither a stigma nor anthers.

Although Paragymnopleurus visited with almost the same frequency as Onthophagus, they rarely carried pollen. Paragymnopleurus barely penetrated beneath the lateral petals as it was too large to reach the anthers located in the narrow, innermost part of the corolla (Fig. 7). They also did not explore the corolla as thoroughly as Onthophagus and left the flower relatively quickly. Attractiveness of the odor for the two beetles may be different. The contribution to pollination by Paragymnopleurus is thought to be much smaller than that attributable to Onthophagus.

Many similar characteristics adapted to beetle pollination have evolved repeatedly in a wide diversity of families. In most beetle pollination, scent acts as the primary attractant (Gottsberger, 1990; Gottsberger and Silberbauer-Gottsberger, 1991). Beetle-pollinated flowers often provide the pollinators with a space protected from predators, such as the enclosed spathe in Araceae (Young, 1986) or the chamber of petals in Annonaceae (Gottsberger, 1989), which trap the pollinators in the flower for an extended period of time. Although these plants usually provide a relatively large amount of pollen and sometimes special nutritive tissues (Beach, 1982; Gottsberger, 1989, 1990), pollination without any reward at all has also been reported. Amorphophallus johnsonii (Araceae) is pollinated by carrion rather than dung beetles (Phaeochrous, Scarabaeidae) (Beath, 1996). Beetles are attracted by the strong odor, but the plant does not offer any substantial reward. However, beetles remain inside the spathe for the whole day, with the plant providing a safe refuge and probably a mating site.

Dung-beetle pollination in O. inouei is a form of deceit pollination in that the flower keeps the pollinators for only a few minutes or less and provide neither reward nor protection from predators. The structure of the flower is more similar to that of many zygomorphic bee-pollinated flowers found in Orchidaceae, Zingiberaceae, or Costaceae than to other beetle-pollinated flowers. The flowers have a labellum, which acts as a platform for the pollinators to enter the corolla. Their stamen and stigma hang over the labellum and are covered with the inner lateral petals. The anthers deposit pollen on the dorsal part of the pollinator, crawling into the narrow space between the labellum and anthers.

The much lower fruit set and larger fruit of Orchidantha in comparison to gingers, which favor similar habitat (S. Sakai, personal observation), was probably caused by lower pollination success of flowers using this deceit pollination system than those using rewards. Dung beetles are excellent dung searchers, flying for long distances in a search of a particular type of dung. Therefore, dung beetles may provide long-distance pollen transfer. Beetle pollination is rare in the understory of the dipterocarp forests in Lambir, although many beetle-pollinated plants are recorded in upper layers of the forest (Kato, 1996; Momose et. al., 1998).

In monocotyledons, scarabaeid beetle pollination has been found in Araceae, Palmae, and Cyclanthaceae, but not in Zingiberales. Almost all species in Zingiberales so far reported specialize in attracting long-distance yet costly pollinators (Table 1, and see references in Table 1). In Zingiberales, Orchidantha is the only genus that includes species lacking nectaries. Although the phylogenetic position of the Lowiaceae is still not clear (Kress, 1995), it is interesting that the deceit pollination system involving dung beetles has been found in the Zingiberales, in which most other members have fascinating mutual relationships with their pollinators.


   FOOTNOTES
 
1 The authors thank Dr. H. S. Lee and Dr. A. A. Hamid, Forest Department Sarawak, for their support and organization of our study; Dr. M. Kon, The University of Shiga Prefecture for insect identification and encouragement; Dr. Nagamasu for helpful suggestions and permission to use photographs; Dr. Turner, Singapore National University, for reading the manuscript and making helpful suggestions. This study was partly supported by Grants-in-Aid from the Japanese Ministry of Education, Science and Culture (Numbers 04041067, 06041013, and 09NP1501) and by JSPS Research Fellowships for Young Scientists for S. Sakai. Back

3 Author for correspondence. Back

4 Dr. Tamiji Inoue was killed in a plane crash in Lambir Hills National Park in 1997. Back


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