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(American Journal of Botany. 2006;93:491-495.)
© 2006 Botanical Society of America, Inc.

Brief Communication

Loss of extrafloral nectary on an oceanic island plant and its consequences for herbivory1

Shinji Sugiura2,4, Tetsuto Abe3 and Shun'ichi Makino2

2Department of Forest Entomology, Forestry and Forest Products Research Institute (FFPRI), 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan; 3Department of Forest Vegetation, Forestry and Forest Products Research Institute (FFPRI), 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan

Received for publication August 16, 2005. Accepted for publication January 9, 2005.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Two Hibiscus (Malvaceae) species coexist on the oceanic Bonin (Ogasawara) Islands: Hibiscus glaber (an endemic species) and H. tiliaceus (the ancestral non-endemic species). Hibiscus tiliaceus produces extrafloral nectar from the sepals, while H. glaber does not. To clarify the effects of extrafloral nectar loss on Hibiscus–insect relationships, we examined herbivory and insect communities on flower buds of H. glaber and H. tiliaceus. Larvae of the endemic moth Rehimena variegata (Lepidoptera: Pyralidae) attacked 20% of the flower buds on H. glaber, while less than 0.2% of buds on H. tiliaceus were attacked. Introduced species of ants frequently visited the flower buds of H. tiliaceus to collect extrafloral nectar from the sepal, while they rarely visited those of H. glaber. Therefore, extrafloral nectar on H. tiliaceus sepals may function as a facultative defense against flower bud herbivory. The loss of extrafloral nectaries of H. glaber sepals may be related to the original paucity of native herbivores and ants on the Bonin Islands.

Key Words: antiherbivore defense • ants • endemic species • evolution • Hibiscus • introduced species • sepals


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Many plant species produce extrafloral nectar on organs such as leaves, stems, and buds, thereby attracting predators and parasitoids, such as ants and wasps, which in turn defend them against herbivores (e.g., Bentley, 1977 ; Cuautle and Rico-Gray, 2003 ; Rudgers, 2004 ). Extrafloral nectaries (EFNs) occur in a wide variety of plant taxa, particularly angiosperms, such as the Passifloraceae, Malvaceae, and Leguminosae. Many studies have suggested that the adaptive significance of EFNs is as an antiherbivore defense (e.g., Bentley, 1977 ; Rudgers, 2004 ), while a few have hypothesized other functions (e.g., Becerra and Venable, 1989 ). Furthermore, extrafloral nectar production has been known to influence insect communities on plants with EFNs (e.g., Rudgers and Gardener, 2004 ).

Oceanic islands that have never been connected to any continental landmass offer opportunities to study speciation and adaptive radiation (Darwin, 1859 ; Carlquist, 1974 ). On oceanic islands, the morphological and ecological evolution of land plants can involve habitat changes (niche expansion), life form (woodiness), sex expression (dioecism), and seed dispersal mode (loss of dispersal abilities; Carlquist, 1974 ; Ito, 1998 ). However, a less well-known phenomenon, the loss of EFNs on plants, has occurred on the Hawaiian Islands, which are representative oceanic islands (Keeler, 1985 ). In Hawaii, only 17 of 1442 indigenous plant species (1.2%) have EFNs (Keeler, 1985 ). This frequency of plants with EFNs is extremely low compared with other tropical regions (14.8–53.3%; reviewed in Blüthgen and Reifenrath, 2003 ; Oliveira and Freitas, 2004 ). The low frequency is thought to be related to the absence of native ants on the Hawaiian Islands (Keeler, 1985 ), which have been invaded by many ant species following human immigration (Reimer, 2003 ).

A similar loss of EFNs on plants, although on a much smaller scale, has likely occurred on the oceanic Bonin (Ogasawara) Islands, which are approximately 1000 km south of the Japanese archipelago. Two Hibiscus (Malvaceae) species coexist on the Bonin Islands: H. glaber Matsum. is endemic to the islands, while H. tiliaceus L. is widely distributed in coastal areas of the tropics and subtropics. Morphological and ecological evidence suggests that the two species are closely related (Kudoh et al., 1998 ; Takayama and Kato, 2001 ; Takayama et al., 2002 ). Using molecular phylogenetic analyses, Takayama et al. (2005) clarified that H. glaber is derived from H. tiliaceus. Hibiscus glaber is thought to have speciated from H. tiliaceus in the process of geographic isolation. Further migrations of H. tiliaceus into the islands following the speciation are thought to result in the coexistence of the two Hibiscus species on the Bonin Islands (Takayama et al., 2005 ). Like other Hibiscus species, H. tiliaceus and H. glaber have slender glands producing nectar on the abaxial leaf surface, near the petiole insertion (e.g., Pemberton, 1998 ; Cogni et al., 2003 ). On the Bonin Islands, H. glaber has tended to lose its nectaries on the major veins of the abaxial surface because H. glaber has fewer nectaries on the veins than does H. tiliaceus (Takayama and Kato, 2001 ). In this study, we report that H. tiliaceus has EFNs on the distinctive slits (ca. 2.5 mm length) of each of five sepals, as well as on the abaxial leaf veins, while H. glaber has no functional EFNs on the sepals. The nectaries on the H. tiliaceus sepals produced nectar that attracted many ants during the time of flower bud formation to the flowering stage.

These differences in EFN distribution among Hibiscus species on the Bonin Islands offer a unique opportunity to investigate the loss of EFNs in oceanic island plants. To clarify the effects of extrafloral nectar loss on Hibiscus–insect relationships, we compared herbivory and insect communities on flower buds of H. glaber and H. tiliaceus.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Study islands
The Bonin Islands are extinct volcanic islands in the northwestern Pacific Ocean, approximately 1000 km south of the Japanese mainland (Ogasawara Village, Tokyo Metropolitan, Japan). Chichijima Island is the largest island and has the most diverse flora (Fig. 1a; 27°04' N, 142°13' E; area 24 km2; altitude 0–318 m a.s.l.). Hahajima Island is ca. 50 km south of Chichijima Island (Fig. 1b; 26°39' N, 142°09' E; area ca. 21 km2; altitude 0–463 m a.s.l.). The mean annual temperature was 23.2°C, and the annual precipitation was 1292 mm from 1987 to 1998 on Chichijima Island (Toyoda, 2003 ). Therefore, the climate of the Bonin Islands is subtropical. Like other oceanic islands, the Bonin Islands support many endemic organisms, including vascular plants (137 species; Toyoda, 2003 ) and insects (338 species; Ohbayashi et al., 2003 ). Irrespective of the high endemism, many organisms have invaded the islands and infiltrated the endemic ecosystem (e.g., Yamashita et al., 2000 ; Ohbayashi et al., 2003 ).


Figure 1
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  		Fig. 1 Study site. (a) Sites where Hibiscus tiliaceus (squares) and H. glaber (circles) were studied on Chichijima Island. (b) Hibiscus tiliaceus study sites on Hahajima Island

 
Study plants
Hibiscus glaber and H. tiliaceus are woody species, growing up to 10 m tall (Satake et al., 1989 ). Individual flowers last for a single day on H. glaber and H. tiliaceus, like in other Hibiscus species (Toyoda, 2003 ). Both species flower in all seasons, but flowering is concentrated in June and July (Satake et al., 1989 ; Hirota et al., 2000 ; Toyoda, 2003 ). Hibiscus glaber grows at a variety of sites across the island, while H. tiliaceus grows at sandy and muddy sites on seashores and along brackish riverbanks (Kudoh and Kachi, 1997 ; Toyoda, 2003 ; Takayama et al., 2005 ). Although H. glaber rarely grows together with H. tiliaceus, both species coexist on Chichijima Island (Kudoh and Kachi, 1997 ; Takayama et al., 2005 ).

Study methods
We examined 21 individuals each of H. glaber and H. tiliaceus on Chichijima Island (Fig. 1b). Hibiscus glaber and H. tiliaceus plants were selected from five and six sites, respectively (Fig. 1b). Furthermore, to clarify the difference in H. glaber–insect relationships among islands, we examined 18 individuals of H. glaber at five sites on Hahajima Island (Fig. 1c). The number of Hibiscus individuals examined at a site ranged from one to eight, with a mean of 3.5 and 3.6 individuals of H. glaber on Chichijima and Hahajima Islands, respectively, and a mean of 3.5 H. tiliaceus on Chichijima Island. We could not examine the H. tiliaceus–insect relationship on islands other than Chichijima Island because H. tiliaceus is not abundant on other islands.

Although there are some differences in leaf morphology, flower size, and seed morphology (Kudoh et al., 1998 ; Takayama and Kato, 2001 ; Takayama et al., 2002 ), we determined the Hibiscus species by leaf shape and hair density (Takayama and Kato, 2001 ). We randomly selected 9–79 flower buds per plant at heights of 0–2.5 m. Most Hibiscus plants had a few flowers and many flower buds. For each flower bud or flower, we recorded the presence/absence of herbivorous insects or their signs and other insects or their signs. We rarely found insects on flower buds, although there were signs of insect feeding. To avoid underestimating host–plant interactions, we recorded a feeding sign as the presence of that insect group. Consequently, we compared the rate of appearance of insects between Hibiscus species on Chichijima Island and between islands in H. glaber using Student's t test (JMP version 5.0; SAS Institute). Proportional values were arcsine-transformed prior to this analysis.

The number of flower buds examined was 32.0 ± 10.8 (mean ± SD; range, 9–62; 682 from 21 plants) in H. tiliaceus on Chichijima Island, 32.5 ± 13.4 (range, 12–44; 673 from 21 plants) in H. glaber on Chichijima Island, and 42.5 ± 15.6 (range, 20–79; 765 from 18 plants) in H. glaber on Hahajima Island. This examination was conducted on 3–5 and 7–8 July 2005 on Hahajima and Chichijima Islands, respectively.

Insects were identified to family in the field using various characters, including adult and larval form and fecal pellets. To identify insects to species, we sampled several individuals on flower buds at some of the sites on Chichijima and Hahajima islands. For identification, we used keys to moths (Inoue, 1996 ), ants (Japanese Ant Database Group, 2003 ), psyllids (Inoue and Miyatake, 2001 ), and bugs (Yasunaga et al., 2001 ).

In our laboratory (Forestry and Forest Products Research Institute [FFPRI] in Tsukuba City, central Japan; 36°00' N, 140°07' E), moth larvae (middle–late instars) were reared individually in plastic petri dishes (90 mm diameter, 15 mm high) with Hibiscus flowers until adult eclosion to identify the moth species. Furthermore, we gave flower buds of H. glaber, H. tiliaceus, and H. syriacus L. to the moth larvae to infer the potential host range. Moth larvae sampled from H. glaber on Hahajima Island were used for feeding experiments with each Hibiscus species. We used three larvae per experiment. Flower buds of H. glaber and H. tiliaceus were sampled from Chichijima Island, while buds of H. syriacus, a species cultivated in Japan, were sampled at FFPRI.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Hibiscus tiliaceus produced extrafloral nectar from the sepals, while H. glaber did not (Fig. 2a). The flower buds of H. glaber were frequently attacked by moths (Fig. 2a, b). Although the moth larvae were observed to move among flower buds, they were frequently observed in flower buds (Fig. 2b). The larvae were not observed to feed on leaves or conceal themselves in leaf rolls. Under laboratory conditions, each larva fed on several flower buds before maturation. Mature larvae left the flower buds and pupated in withered leaves. Two weeks after pupation, adults (N = 7) emerged and were identified as Rehimena variegata Inoue (Lepidoptera: Pyralidae). Lepidopteran larvae attacked 20.8% and 28.6% of the flower buds of H. glaber on Chichijima and Hahajima islands, respectively, while only 0.20% of H. tiliaceus were attacked (Fig. 3; t test, Chichijima vs. Hahajima for H. glaber, t = 1.4, P = 0.16; H. glaber vs. H. tiliaceus on Chichijima, t = 5.4, P < 0.0001). Only 1 of 682 H. tiliaceus flower buds examined had been attacked by a lepidopteran larva. Although it was not available for identification, the feeding sign was similar to that of R. variegata. In the laboratory, all R. variegata larvae bore into and fed on flower buds of H. tiliaceus, H. syriacus, and H. glaber.


Figure 2
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  		Fig. 2 Flower buds and insects found on Hibiscus tiliaceus and H. glaber. (a) Flower buds of H. glaber (left) and H. tiliaceus (right); the left and right arrows show herbivory and extrafloral nectar production, respectively. (b) Longitudinal section of an H. glaber flower bud in which a late instar of Rehimena variegata was feeding. (c) Workers of the ant Pheidole indica visiting a flower bud to collect nectar from H. tiliaceus sepals. Bars: 10 mm (a, b), 5 mm (c)

 

Figure 3
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  		Fig. 3 Associations between insects and flower buds of Hibiscus tiliaceus and H. glaber. The bars indicate SE

 
Other insects visited flower buds of H. tiliaceus more frequently than those of H. glaber (Fig. 3). Ants frequently visited flower buds of H. tiliaceus (Fig. 2c), foraging on 11.5% of the flower buds of H. tiliaceus vs. 0.5% in H. glaber (t test, t = –2.7, P < 0.001). Ants (N = 29) collected on flower buds of H. tiliaceus included 20 workers of Pheidole indica Mayr, four of Tetramorium bicarinatum (Nylander), and four of Paratrechina amia (Forel), and a queen of Technomyrmex albipes (F. Smith). Most ants were observed to collect extrafloral nectar on H. tiliaceus sepals (Fig. 2c). Eggs or egg scars of a green lacewing (Neuroptera: Chrysopidae) were also found on the flower buds of H. tiliaceus only (Fig. 3). Nymphs and adults of a jumping plant louse (Psylloidea) and their signs were observed on the epicalyx (the base of the flower bud) of H. tiliaceus only (Fig. 3). Based on the morphological characters of its nymphs (N = 17) and adults (N = 4), the psyllid was identified as Mesohomotoma camphorae Kuwayama (Hemiptera: Carsidaridae). In M. camphorae colonies sampled on the flower buds of H. tiliaceus, nymphs of the unidentified green lacewing (N = 2) were also found. Furthermore, M. camphorae nymphs, which were covered with abundant cottony wax, produced nectar droplets from tips of their abdomens, attracting ants. Twice we observed ants guarding M. camphorae nymphs on H. tiliaceus flower buds. Mirids were observed on H. tiliaceus sepals (Fig. 3), and the collected individuals (N = 7) included three adults and two nymphs of Deraeocoris ryukyuensis Nakatani and two adults of Campylomma sp. (Homoptera: Miridae). Workers of the introduced honeybee Apis mellifera L. also collected extrafloral nectar on H. tiliaceus sepals (Fig. 3).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Insects on hibiscus flower buds
We observed that extrafloral nectar on H. tiliaceus sepals attracted ants (Figs. 2c, 3) and the flower buds were rarely attacked by moth larvae (Fig. 3). In contrast, we found no nectar production on H. glaber flower buds, which were frequently attacked by larval R. variegata (Fig. 3), which is morphologically similar to R. surusalis (Walker) and endemic to the Bonin Islands (Inoue, 1996 ). This is the first record of a host plant for R. variegata. Rehimena surusalis, which feeds on Hibiscus flowers, is widely distributed from East to Southeast Asia, excluding the Bonin Islands (Inoue et al., 1982 ). Therefore, similar to the host plant H. glaber (Takayama et al., 2005 ), R. variegata may have speciated from R. surusalis on the Bonin Islands following geographic isolation.

The psyllid M. camphorae was found only on H. tiliaceus (Fig. 3), as reported in Inoue and Miyatake (2001) . Mesohomotoma camphorae is widely distributed in the tropics and subtropics (Inoue and Miyatake, 2001 ) and is a phloem feeder that uses other Hibiscus species in other regions, but it did not use H. glaber in the Bonin Islands (Fig. 3; Inoue and Miyatake, 2001 ). Mesohomotoma camphorae nymphs produced nectar droplets that attracted ants. Because ants act as bodyguards for many homopterans (Buckley, 1987 ), they may have visited flower buds of H. tiliaceus more frequently to collect honeydew produced by homopterans, as well as extraloral nectar. The nymphs of green lacewings often prey on homopterans (Canard et al., 1984 ), and the lacewings frequently laid eggs on the flower buds of H. tiliaceus. We found lacewing nymphs in M. camphorae colonies sampled on the flower buds of H. tiliaceus, suggesting that the lacewing nymphs preyed on M. camphorae nymphs. Lacewing adults are nocturnal nectar feeders (Canard et al., 1984 ) and may collect extrafloral nectar from H. tiliaceus sepals at night. Because mirids are often carnivores (Wheeler, 2001 ), the two species recorded in H. tiliaceus may prey on psyllids. Therefore, predatory insects visited flower buds of H. tiliaceus more frequently than those of H. glaber.

Function of extrafloral nectar on H. tiliaceus sepals
The significant function of extrafloral nectar is thought to be antiherbivore defense (Bentley, 1977 ; Rudgers, 2004 ). Larvae of the moth R. variegata attacked flower buds of H. glaber more frequently than those of H. tiliaceus (Fig. 3). This suggested that the moth rarely laid eggs on the flower buds of H. tiliaceus or that the moth larvae were eliminated by other organisms. Ants and other predatory insects visited flower buds of H. tiliaceus more frequently than those of H. glaber (Fig. 3), suggesting that predation pressure by the moth R. variegata was stronger on H. tiliaceus because R. variegata larvae must move among flower buds to feed during maturation. Ants, which guard plants, frequently collected nectar from the H. tiliaceus sepals. Furthermore, nectar production by H. tiliaceus sepals was limited to the stages from flower-forming to flowering, which coincided with the stages when R. variegata larvae attacked H. glaber (Fig. 2a). Similar to other studies of EFN function (Bentley, 1977 ; Cuautle and Rico-Gray, 2003 ; Rudgers, 2004 ), the nectaries on H. tiliaceus sepals may function as a defense against flower–bud herbivores, although ant–exclusion experiments are needed to confirm this.

Why did H. glaber lose EFNs on its sepals?
Hibiscus glaber likely expanded its habitat from the seashore to the mountains during the process of speciation from ancestral H. tiliaceus (Takayama et al., 2005 ). The poor growing conditions (e.g., water stress) encountered in mountains may have induced H. glaber to lose its nectaries, as proposed for Hawaiian hibiscuses (Keeler, 1985 ).

Two selection pressures may be significant for the evolutionary maintenance of EFNs (Rudgers, 2004 ; Rutter and Rausher, 2004 ): the presence of herbivores and the presence of bodyguards, such as ants.

Organisms that newly immigrate to isolated habitats are released from the effects of their natural enemies (the escape-from-enemy hypothesis; Wolfe, 2002 ). Introduced plants can lose enemy resistance and in turn evolve increased size or fecundity (Maron et al., 2004 ). Ant plants are known to lose mutualistic interaction with specific ants because of the reduced herbivore challenge in insular habitats (Janzen, 1973 ). Such phenomena should occur in the EFN evolution of island plants. In the speciation of H. glaber from the ancestral H. tiliaceus, the absence of natural enemies (i.e., flower–bud herbivores) may have induced H. glaber to lose the nectaries on its sepals, although there is no evidence of the absence of herbivores in the ancient Bonin Islands.

On oceanic islands, the native flora and fauna are often disharmonic and unbalanced (Carlquist, 1974 ), e.g., they lack oaks (Quercus), mammals (except for bats), and amphibians. In Hawaii, there are no indigenous ant species (Reimer, 2003 ); consequently, most plants have tended to lose EFNs (Keeler, 1985 ). However, the frequency of plants with EFNs is higher on the oceanic Bonin Islands (Pemberton, 1998 ), which may be related to the presence of native ant species on the Bonin Islands, where 61 ant species have been recorded (Ohbayashi et al., 2003 ), although few of these are native (Terayama and Hasegawa, 1992 ). The ant fauna of the Bonin Islands includes many tramp species, which have invaded the islands following human immigration (Terayama and Hasegawa, 1992 ). Furthermore, only one of six endemic ant species is frequently found on most of the Bonin Islands, while the others are rare or are distributed on only a few islands (Japanese Ant Database Group, 2003 ; Ohbayashi et al., 2003 ). Therefore, native ant species may have originally been rare on the Bonin Islands. The frequency of plants with EFNs is higher on the Bonin Islands than on the Hawaiian Islands, but lower than elsewhere in the tropics and subtropics (Pemberton, 1998 ; Oliveira and Freitas, 2004 ). Actually, all the ant species collected on H. tiliaceus flower buds were considered as species introduced to the Bonin Islands (Terayama and Hasegawa, 1992 ; Japanese Ant Database Group, 2003 ). Therefore, the original paucity of the native ant fauna may also be related to the loss of EFNs on H. glaber sepals.


   FOOTNOTES
 
1 The authors thank K. Yamazaki for his valuable comments on this manuscript and Y. Miyatake and K. Hamaguchi for helping to identify psyllids and ants, respectively. The authors also thank the staffs of the National Forest Division of Ogasawara General Office for allowing them to use the study forests. This study was supported by the Global Environment Research Fund (F-051). Back

4 Author for correspondence (e-mail: ssugiura{at}ffpri.affrc.go.jp ) Back


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TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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