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. 2008 Nov 7;103(1):39–44. doi: 10.1093/aob/mcn212

A new pollination system: brood-site pollination by flower bugs in Macaranga (Euphorbiaceae)

Chikako Ishida 1, Masumi Kono 2, Shoko Sakai 3,*
PMCID: PMC2707287  PMID: 18996950

Abstract

Background and Aims

Macaranga (Euphorbiaceae) is a large genus of dioecious trees with approx. 260 species. To date, only one pollination study of the genus has reported brood-site pollination by thrips in M. hullettii. In this study, the pollination system of Macaranga tanarius is reported.

Methods

The study was conducted on Okinawa and Amami Islands, Japan. Flower visitors on M. tanarius were collected and their pollen load and behaviour on the flowers examined, as well as inflorescence structure and reward for the pollinators.

Key Results

The most abundant flower visitors found on the male and female inflorescences were Orius atratus (Anthocoridae, Hemiptera), followed by Decomioides schneirlai (Miridae, Hemiptera). Pollen load on O. atratus from flowering pistillate inflorescences was detected as well as from staminate flowers. Orius atratus and D. schneirlai are likely to use the enclosed chambers formed by floral bracts as breeding sites before and during flower anthesis, and feed on nectar on the adaxial surface of flower bracts. The extrafloral nectary has a ball-shaped structure and the contained nectar is not exposed; the hemipterans pierce the ball to suck out the nectar.

Conclusions

The results indicate that the plant is pollinated by flower bugs breeding on the inflorescences. This study may be the first report of pollination systems in which flower bugs are the main pollinators. Similarity of pollination systems between M. hullettii and M. tanarius indicates that the two brood-site pollination systems have the same origin. The pollinator species belongs to a predacious group, whose major prey includes thrips. The pollination system might represent a unique example of evolution from predatory flower visitors feeding on the pollinators (thrips) to the main pollinators.

Key words: Amami, brood-site pollination, dioecy, Euphorbiaceae, extrafloral nectary, Hemiptera, Macaranga tanarius, Okinawa, Orius atratus

INTRODUCTION

Flowering plants have evolved amazingly diverse pollination systems. Although the majority of plants provide nectar and/or pollen, various other rewards have been adopted, especially for insect pollinators, reflecting their diverse ecology. Such rewards include special kinds of oil (e.g. Sérsic and Coccuci, 1999; Coccuci and Vogel, 2001) or resin (e.g. Armbruster, 1997), mating sites (e.g. Gottsberger, 1999) and heat (e.g. Seymour et al., 2003; Yuval et al., 2006). The type of reward may be an important factor to determine specificity of the pollinators to plants and vice versa.

Close relationships between plants and pollinators are often found in brood-site (or nursery) pollination systems, in which plants provide breeding sites as a reward for pollination. In these pollination systems, pollinator larvae grow on the flowers or inflorescences, feeding on ovules, pollen and other reproductive organs (reviewed by Sakai, 2002; Dufaÿ and Anstett, 2003). Well-documented examples of such pollinators are ovule parasites of plants, including fig wasps pollinating figs (Moraceae; e.g. Janzen, 1979; Machado et al., 2001), yucca moths pollinating Yucca (Agavaceae; e.g. Pellmyr, 2003) and Epicephala moths pollinating Glochidion spp. and their allies (Phyllanthaceae; Kato et al., 2003). In these interactions, both plants and pollinators cannot survive without their obligate partners, and are considered to have tightly co-evolved.

Alternatively, specificity for and reliance on their partners may be variable or relatively low in other brood-site pollination systems, in which plants offer parts of reproductive organs other than ovules to their pollinators (Sakai, 2002). In these systems, shifts from one pollinator group to another may occur after evolution of brood-site pollination. However, such examples have rarely been reported, and frequencies of and conditions for shifts of pollinators are largely unknown.

In this study, the pollination system of Macaranga tanarius (Euphorbiaceae) is reported. Macaranga is a moderately large genus of dioecious trees including approx. 260 species. Many of these species are pioneer trees, and about 30 are myrmecophytes (Davies et al., 2001). Only one pollination study on the genus has reported brood-site pollination by thrips in M. hullettii (Moog et al., 2002). Although M. tanarius also has a brood-site pollination system, it was found that its pollinators were flower bugs (Hemiptera) rather than thrips. As far as is known, this is the first report of a plant pollinated mainly by hemipterans. The similarity of the pollination systems of M. tanarius and M. hullettii indicates that their brood-site pollination systems have the same origin, and a pollinator shift occurred after brood-site pollination had evolved in Macaranga.

MATERIALS AND METHODS

Study sites

Collection and observation in the field were conducted in the northern part of Okinawa Island (25°46'N, 126°38'E) in April 2007 and the eastern part and along the northern coast of Amami Island (28°20'N, 129°28'E) in May 2007. Both islands are in the subtropical region of Japan, about 330 km from each other. The annual mean temperature in Okinawa is about 22·4 °C, and the average annual total rainfall is about 2000 mm. The northern area of Okinawa is mostly covered with broadleaf evergreens of the genus Castanopsis, while the south-central section is largely occupied by cultivated land. The annual mean temperature of Amami is 21·1 °C, and the average annual total rainfall is about 3000 mm. Most parts of the island are covered by secondary Castanopsis forests or secondary Pinus forests. Cultivated lands is mainly in the coastal region of the island.

Study species

Macaranga tanarius (Euphorbiaceae) is a dioecious pioneer tree that grows up to 10 m tall and 15 cm in diameter at breast height. The trees are usually found in the open or in disturbed areas such as forest edges, roadsides and secondary forests. The species has a wide distribution from southern Japan through Peninsular Malaysia, Borneo, and New Guinea. In Japan, M. tanarius produces inconspicuous green inflorescences clustered at the end of the shoots in April–June.

A staminate inflorescence is composed of about ten branchlets bearing 15–30 apetalous flowers along a 15- to 20-cm-long rachis (Fig. 1B). Flowering trees can be recognized from a distance, since top of the branchlets are visible above the canopy. Each flower has approximately ten anthers, subtended by a bract approx. 0·5 mm in width and length. The flower is loosely covered by bracts when flowering (Fig. 1D). A pistillate inflorescence has branchlets thicker and shorter than those of a staminate inflorescence. The branchlets do not elongate above the leaves, thus they are not visible from outside of the canopy (Fig. 1A). Each branchlet produces five to ten apetalous flowers in clusters. Each flower has a two-lobed stigma and is subtended by a bract 0·5 mm in width and 1·0 cm in length (Fig. 1C). Pistillate inflorescences contain fewer flowers than staminate inflorescences. Stigmas are tightly covered with bracts even during anthesis, and there are only narrow gaps between overlapping bracts. The adaxial surface of the bracts of both sexes is covered with trichomes, which are especially dense around the base.

Fig. 1.

Fig. 1.

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Macaranga tanarius and pollinator: (A) overview of pistillate inflorescences (scale bar = 2 cm); (B) overview of staminate inflorescences (scale bar = 3 cm); (C) flowering pistillate inflorescence in which the outer bracts are extended to show the lobed stigma (scale bar = 5 mm); (D) flowering staminate inflorescences visited by Orius atratus (scale bar = 2 mm); (E) Orius atratus sucking nectar on the adaxial surface of a bract (scale bar = 1 mm); (F) scanning electron micrograph of nectaries on the adaxial surface of a bract (n, mature nectary before sucking; *, nectary already sucked and deflated; scale bar = 100 µm).

Flowering stages

Three flowering stages of trees were distinguished. Stage 1: in most of the inflorescences, the space between overlapping bracts is <1 mm; the size of immature anthers and stigmas is less than half the size at maturity (anther, <0·5 mm in width and length; stigma, <2 mm in length). Stage 2: the space is 1–3 mm; anthers or stigmas are almost the same size as those in mature flowers (anther, 0·5–1 mm in width and length; stigma, 2–4 mm in length). Stage 3: at least some of the flowers are in anthesis; in staminate flowers, anthers dehisce, and pollen is exposed; in pistillate flowers, the tip of the stigma is split and the surface seems wet (Fig. 1C).

Collection and observation of flower visitors

Flower visitors hidden inside the enclosed bracts were collected on 18 and 39 trees on Okinawa and Amami, respectively. First, part of the inflorescence was put into a plastic bag and then a branchlet was cut off to reduce possible loss of floral visitors during collection. All the collections were made during daytime (0700–1800 h). All insect visitors were identified to the order, and abundant adult hemipterans were identified to species level. Hemipteran larvae in subsamples were also indentified into species. Reference collections are kept at Kyoto University. In addition, highly mobile flower visitors were assessed by observing inflorescences directly (staminate, 5 h; pistillate, 7 h) or indirectly using a video camera (staminate, 10 h; pistillate, 6 h) both during daytime (0600–1800 h) and night-time (1800–2300 h).

To compare flower visitors between the sexes and among the flowering stages, insects were collected on five branchlets per tree from 22 staminate and 17 pistillate trees on Amami Island. The number and sex ratio of the main pollinator species, Orius atratus (see Results), were compared between the staminate and pistillate trees using the Mann–Whitney U-test, and among flowering stages of each sex using the Kruskal–Wallis test. The statistical tests were conducted using R software (R Development Core Team, 2005).

To assess pollen transfer, adult hemipterans were collected from 230 branchlets of seven pistillate trees at Stage 3 and 25 branchlets of three staminate trees at Stage 3 on Amami Island. The insects were examined for pollen load under a microscope.

In the field, behaviour of flower visitors inside the bracts was observed by carefully spreading apart the floral bracts to extend the openings. For observation in the laboratory, flower visitors collected alive were kept in a Petri dish with part of the inflorescences with about five flowers. Feeding behaviour was observed under a binocular microscope.

RESULTS

Flower visitors

In total, 1184 and 758 flower visitors were collected from staminate and pistillate inflorescences, respectively, before and during anthesis (Fig. 2) on Okinawa and Amami (Table 1). The adult insect visitors were dominated by two species of Hemiptera, Orius atratus (Anthocoridae) and Decomioides schneirlai (Miridae) (Table 1). The density of O. atratus did not differ between staminate (7·6 ± 10·0 individuals per 5 inflorescences, n = 22) and pistillate (4·2 ± 3·3, n = 17) trees, but the proportion of females was significantly higher on pistillate trees (0·91 ± 0·16, N = 14) than on staminate trees (0·56 ± 0·18, n = 16) (P = 0·00011, Mann–Whitney U-test). Both O. atratus and D. shneirlai were observed moving quickly on inflorescences. Among the visitors, 22·1–66·3 % were hemipteran larvae. The majority of the larvae on both staminate and pistillate inflorescences (98·6 % of 69 and 96·8 % of 63, respectively) were those of O. atratus, and the rest were those of D. shneirlai. During the observation periods for mobile visitors, no visitors other than the two hemipteran species were observed. Significant differences in the numbers and sex ratio of hemipterans among flowering stages were not observed.

Fig. 2.

Fig. 2.

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Number of hemipterans collected from five branchlets on staminate (A) and pistillate (B) inflorescences. Columns show an adult Orius atratus, an adult Decomioides schneirlai and hemipteran larvae as indicated. Vertical bars represent s.e.

Table 1.

Summary of flower visitors collected on staminate and pistillate trees on Okinawa and Amami Islands

No. of sites Sex No. of trees No. of branchlets No. of insects O. atratus (%) D. schneirlai (%) Hemipteran larvae (%) Others (%)
Okinawa (15) Staminate 13 66 440 42·5 20·0 37·3 0·2
Pistillate 5 41 86 65·1 12·8 22·1 0·0
Amami (16) Staminate 22 130 744 22·6 10·1 66·3 1·1
Pistillate 17 310 672 32·3 7·3 59·7 0·7
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‘Others’ include thrips and hemipteran insects.

Eighteen per cent (n = 50) and 9·3% (n = 107) of male and female O. atratus, respectively, collected from flowering pistillate inflorescences (Stage 3) had pollen loads. However, pollen was not found on D. schneirlai (n = 28; Table 2). In staminate inflorescences of Stage 3, 100% of O. atratus and D. schneirlai had pollen on their bodies (Table 2).

Table 2.

Proportion of hemipteran insects with body pollen collected from flowering pistillate and staminate inflorescences

Family, species Sex Pistillate tree (%) Staminate tree (%)
Anthocoridae, Orius atratus Male 18·0 (50) 100·0 (16)
Female 9·3 (107) 100·0 (10)
Miridae, Decomioides schneirlai Male 0·0 (15) 100·0 (2)
Female 0·0 (13) 100·0 (2)
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Sample sizes are given in parentheses.

Nectary and feeding behaviour of the pollinators

Ball-like structures filled with liquid were scattered on the adaxial base of the bracts covered with trichomes both on staminate and pistillate inflorescences (Fig. 1F). The cuticle on the nectary seemed to be relatively tough since it did not break when squeezed with the tips of tweezers. Hemipteran adults and larvae were observed to probe the adaxial base of the bract (Fig. 1E). They inserted their mouthparts and sucked the contents at the rate of 1–2 balls s−1. Once the content was sucked out, the ball became deflated (Fig. 1F). No signs of feeding damage were observed on bracts and other floral tissues, or of flower bugs feeding on pollen.

DISCUSSION

This study suggests that Macaranga tanarius is pollinated by flower bugs on Amami and Okinawa Islands. Other than hemipteran larvae, the flower bugs Orius atratus were the predominant visitors to both staminate and pistillate inflorescences of M. tanarius, on both Okinawa and Amami Islands. The presence of body pollen on O. atratus collected from pistillate inflorescences indicated that the bugs moved from staminate to pistillate trees, thus contributing to pollination. They were observed to search and suck nectar very actively on the inner surface of the bract. It is likely that they deposit pollen on stigmas when they crawl into the chamber formed by floral bracts, and when they are feeding on nectar on the inner surface of the bract. The contribution to pollination of the second most abundant species, Decomioides schneirlai, was uncertain, since it was not possible to find body pollen on individuals collected from pistillate inflorescences. Wind pollination is quite unlikely considering that pistillate flowers are tightly enclosed in the floral bracts during the whole flowering period, and that pistillate inflorescences are not exposed outside of the canopy. Thus we consider that O. atratus is the most important pollinator of M. tanarius, although the efficiency of the insects as pollinators still remains to be evaluated by measuring frequency of inter-tree movement and pollen deposition efficiency. Dominance of hemipterans (Miridae) among flower visitors on the plants has also been reported from west Malaysia (Moog, 2002).

As far as is known, this study is the first report of pollination systems in which flower bugs are the main pollinators. Only a few studies have reported hemipterans or flower bugs as pollinators, despite the fact that they are frequently found in flowers, feeding on flower visitors such as thrips (Yasunaga, 1997). Fahn and Shimony (2001) reported that hemipteran insects are the main flower visitors in Ecballium elaterium (Curcurbitaceae), yet their contribution as pollinators are uncertain. Another report showed that hemipteran larvae feeding on pollen facilitated selfing in Roridula (Roridulaceae; Anderson et al., 2003).

The presence of large numbers of hemipteran larvae in both staminate and pistillate inflorescences at all flowering stages suggests that the hemipterans use the inflorescences as breeding sites before and during flower anthesis. Orius spp. are known to lay their eggs within the plant tissue (Tommasini, 2003). Their larvae do not have functional wings, thus their mobility is quite limited. Enclosed chambers formed by floral bracts may be ideal sites for reproduction, since they provide a shelter from natural enemies as well as a food source. One remarkable character of this hemipteran pollination is that the main food for the pollinators provided by the plant is nectar secreted by the nectaries scattered on the adaxial surface of bracts (Fig. 1F). In most flowering plants, nectar is secreted from secretory tissues and exposed on the epidermis (reviewed by Pacini et al., 2003). However, the extrafloral nectary for pollinators of M. tanarius is a ball-shaped structure, and the nectar inside is not exposed unless the cuticle is torn open. This type of nectary can provide a food source only for insects with mouthparts suitable for inserting and sucking, such as hemipterans, and may contribute to eliminate nectar robbers. A similar structure of pollinator rewards is known for the elaiophore of oil-producing flowers of Sisyrinchium species (Iridaceae; Cucucci and Vogel, 2001). These flowers are pollinated by oil-collecting bees with special scrapers on their forelegs, with which they disrupt the cuticle.

Although O. atratus is likely to be the most important pollinator of M. tanarius, the importance of M. tanarius for the pollinator is unclear. The genus Orius comprises a group of flower bugs known to be predators of minute insects, such as thrips and mites, which are found on plants, while they also feed on pollen and other plant tissues. Species such as Orius tristicolor, O. insidiosus, O. sauteri and O. minutus are commonly used for biological pest control (e.g. Kawai, 1995; Kohno and Kashio, 1998; Tommasini, 2003). These species can also be reared on pollen, but their growth and/or survival rates are often significantly lower (Funao and Yoshiyasu, 1995; Richards and Schmidt, 1996; Maeda et al., 2002). Thus nectar composition or dependence of O. atratus on nectar for nutrient during the flowering period may be an interesting subject for further studies, considering that nitrogen-rich food seems to be essential for omnivorous Orius spp. (Coll and Guershon, 2002). Orius atratus was described about 10 years ago, and its ecology is mostly unknown. The species has been recorded from flowers of different trees, such as Mallotus japonicus (Euphorbiaceae), Schima wallichi (Theaceae) and Trema orientalis (Ulmaceae; Yasunaga, 1997). Since O. atratus has been collected out of flowering season of M. tanarius (Yasunaga, 1997), it may survive feeding on herbivorous insects when the nectar of M. tanarius is not available. Nevertheless, some circumstantial evidence indicates the importance of M. tanarius for O. atratus. For example, the northern limit of distribution of both M. tanarius and O. atratus, Amami Island, coincides (Ohba, 1989; Yasunaga, 1997). Moreover, O. atratus is most abundant in the flowering season of M. tanarius in Japan, judging from collection records of specimens (Ohba, 1989; Yasunaga, 2001).

Several other aspects of the pollination system remain to be revealed. For example, the advantage of breeding of pollinators on female plants is unclear. Dispersal of pollinators from female trees without pollen load does not contribute to reproductive success, while breeding of pollinators on staminate inflorescences well before anthesis may facilitate pollen dispersal by increasing the number of pollinators. Most dioecious plants with a brood-site pollination system attract pollinators by deceit to female plants without rewards (Dufaÿ and Anstett, 2003). Presence of many female conspecifics on pistillate inflorescences may promote visits of male pollinators, which carry more pollen than do females. The role of Decomioides schneirlai in this pollination system is also unknown; is it a co-pollinator of O. atratus, or competitor? Besides, it is not known what triggers movements of the sedentary pollinators between trees. There is no explanation either for why the sex ratio of O. atratus differs between staminate and pistillate trees.

Only one published study on pollination in the genus reported brood-site pollination by thrips in M. hullettii (Moog et al., 2002). Abundant thrips have also been observed on inflorescences of close relatives of the species (Ishida, 2008). Thrips are tiny insects with piercing/sucking mouthparts and are found on many different plants, although host specificity is largely unknown (Williams et al., 2001; Mound, 2005). Pollination by thrips has been reported in several plant groups, in most of which pollen is the major reward for the pollinators (e.g. Popowia, Momose et al., 1998; Macrozamia, Mound and Terry, 2001; Castilla, Sakai, 2001; Antiaropsis, Zerega et al., 2004). Among thrip-pollinated plants, Macaranga is unique in that its reward for pollinators is not pollen but nectar secreted by trichomes on the adaxial surface of bracts (Moog et al., 2002). In addition, thrips begin inhabiting and breeding in flowers well before anthesis.

The similarity of the pollination systems between M. hullettii and M. tanarius indicates that brood site pollination by thrips and flower bugs has the same origin. The thrips and hemipteran pollination systems found in Macaranga are common in that the pollinators use enclosed bract chambers as breeding and feeding sites before and during anthesis, both in staminate and pistillate trees. In addition, the plants provide nectar rather than pollen for the pollinators and their larvae, and the nectaries are located on the adaxial surface of bracts. Therefore, we consider that pollinator shifts between insects breeding on flowers have occurred after brood-site pollination.

One possible scenario might be that hemipteran visitors, which had been originally predators of thrips pollinators, became the main pollinators when plants evolved a ball-like nectary, which requires a strong piercing mouthpart to suck out the nectar. Both O. atratus and D. schneirlai belongs to a predacious group, whose major prey includes thrips. Predacious hemipteran insects are occasionally observed together with thrips on the inflorescence of Macaranga and Mallotus (S. Sakai, unpubl. res.), a sister genus of Macaranga (Kulju et al., 2007). Future studies might reveal that the pollination system represents a unique example of evolution from predatory flower visitors feeding on the pollinators (thrips) to main pollinators. Evolution and specificity of plant–pollinator interactions is still largely unknown in brood-site pollination systems other than pollination by ovule parasites. Macaranga may provide an interesting material for further studies.

ACKNOWLEDGEMENTS

We thank Dr Makoto Kato for comments on an earlier version of the manuscript and identification of hemipteran insects; Dr Katsuyuki Kohno for information on hemipterans; Dr Atsushi Kawakita for advice on the field study; Dr Hiroshi Tobe for permission to use research equipment; and two anonymous reviewers for useful comments on the earlier version of the manuscript. This study was financially supported in part by Grants-in-Aid for Scientific Research (no. 20405009) by the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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