| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Reproductive Biology |
Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu-cho, Sakyo-ku, Kyoto, 606–8501 Japan
Received for publication December 14, 2003. Accepted for publication July 30, 2004.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: bird pollination • honey bee invasion • New Caledonia • plant-pollinator interactions • pollination
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Jaffré et al., 2001
). The high diversity and endemicity result from the long history of this land mass remaining above sea level after the breakup of Gondwanaland in the Mesozoic; they are also the result, in part, of the climatic and geological diversity of habitats within Grand Terre Island. The flora of New Caledonia is also characterized by an unusual abundance of archaic plant taxa (i.e., basal angiosperm lineages), such as the Amborellaceae, Winteraceae, and Monimiaceae (Takhtajan, 1986
). The Amborellaceae are thought to be the most basal family of angiosperms (Soltis et al., 1999
). These attributes of New Caledonian flora have attracted botanical and ecological interest, inspiring many studies of plants on the islands (e.g., De Laubenfels, 1959
; Jaffré et al., 1976
; Thien et al., 1985
, 2003
; Pellmyr et al., 1990
; Carpenter et al., 2003
; Kawakita and Kato, 2004
).
The floristically distinct area termed the New Caledonia Subkingdom by Takhtajan (1986)
also provides a fascinating ecosystem from the perspective of pollination mutualism. It is of great ecological and evolutionary interest to investigate original plant-pollinator interactions that have potentially shaped the uniqueness and richness of the flora in New Caledonia. Community-level plant-pollinator interactions are founded on mutualisms between plants and their pollinators, as well as on competition between plants for pollinators, and competition between pollinators for floral resources (Waser and Real, 1979
; Kevan and Baker, 1983
). Pioneering works on pollination systems in New Caledonia have demonstrated that the archaic Zygogynum subsp. are pollinated by primitive micropterigid moths (Thien et al., 1985
; Pellmyr et al., 1990
) that do not have nectar-collecting proboscides.
However, community-level studies on plant-pollinator interactions have not yet been made in New Caledonia. Such studies are important and necessary, because plant-pollinator interactions on oceanic islands are easily and rapidly degraded by the invasion of honey bees (Kato, 1992
; Kato et al., 1999
; Dupont et al., 2004
). Social bees were originally absent on most oceanic islands, as it was often difficult for them to cross the sea (Michener, 1979
). Although New Caledonia is not an oceanic island but rather a fragment of Gondwanaland, the only bees originally recorded in New Caledonia are solitary short-tongued bees in the families Colletidae, Halictidae, and Megachilidae (Michener, 1965
). Because honey bees can communicate the exact site of flowers to nestmates by dancing, they have often outcompeted native solitary bees, not only on oceanic islands but also in Australia (Paton, 1993
), North America (Barthell, 2001
), and the Neotropics (Roubik, 1978
), where social bees (stingless bees and/or bumblebees) but not honey bees were native.
Because the flora of New Caledonia has links with Australia, New Guinea, and New Zealand (Morat et al., 1984
), plant-pollinator interactions are predicted to be similar to those in Gondwanaland. Pollination systems of various plants in New Zealand were observed from 1920 to 1935, when introduced honey bees were not as abundant as they are now (Thomson, 1927
; Heine, 1938
). The data of these pioneering studies suggest that the most dominant pollination system in New Zealand was myophily, followed by general entomophily, melittophily, and ornithophily. However, the increase in populations of introduced honey bees and bumblebees caused a decrease in native pollinators (Craig et al., 2000
). The drastic changes in pollination mutualism in New Zealand suggest that it is urgent, if it is not already too late, that study of the original systems of pollination mutualism in New Caledonia be undertaken.
To investigate community-level pollination mutualism in the endemic ecosystem in New Caledonia, we surveyed pollinator visits to the flowers of diverse species of various vegetation types. We observed 99 plant species, encompassing 42 families of most major lineages of flowering plants. Our data highlight the uniqueness of pollination mutualism in New Caledonia, its links to other vegetation in the world, and the endangered status of the observed interactions. This is the first study that describes community-level plant-pollinator interactions in this floristic region, i.e., in the New Caledonian Subkingdom.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
|
; Kato, 2000
; Yamazaki and Kato, 2003
). All collected specimens were brought back to the laboratory for identification and determination of pollen attached to their bodies. If no insect visitors were observed during the whole 10-min period (and in additional observation), we looked at whether or not birds visited the flowers by studying the flowers from at least 10 m away for an additional 15 min. For flowers that were not visited by insects or birds during the daytime or that did not receive visits that would have led, in all likelihood, to effective pollination, we made additional observations in the evening and/or at night. Visitations by nocturnal insects and bats were studied as described for diurnal insects and birds, respectively. Thus, a data set of all bird/insect visits to flowers was created.
Principal components analysis and cluster analysis were performed on the data set to detect patterns of anthophilous insect communities on different plant species. In these analyses, observations of fewer than four visits were excluded. Thus, 77 observations on 71 plant species were included in the analysis. Flower visitors were grouped into 16 functional/taxonomical groups: thrips, Neuroptera, beetle, leafcutter bee, small bee, honey bee, wasp, ant, Diptera, hawk moth, gracillariid moth, micropterigid moth, other moths, butterfly, bird, and bat. Statistical analyses were made using SAS (1985)
in the Data Processing Center at Kyoto University.
In addition, we evaluated the behavior and/or pollen attachment on the bodies of flower visitors, and then determined the pollination system of each plant species. The frequency distribution of pollination systems of 95 native plant species in New Caledonia was compared to those of various ecosystems in different biogeographical regions: temperate deciduous forests in New Zealand (Thomson, 1927
; Heine, 1938
), a tropical rain forest in Kakachi, India (Devy and Davidar, 2003
), a tropical dipterocarp forest in Lambir, Sarawak (Momose et al., 1998
), subtropical forests on Amami Island, Japan (Kato, 2000
), temperate deciduous forests and grasslands at Mt. Yufu on Kyushu Island, Japan (Yamazaki and Kato, 2003
), cool temperate subalpine coniferous forests and meadows at Mt. Kushigata on Honshu Island, Japan (Kato et al., 1993
), and tropical rain forests in La Selva, Costa Rica (Kress and Beach, 1994
). Although only trees are included in the data set of Kakachi, both herbaceous and woody plants are included in the other data sets. In classifying flower visitors into groups, "long-tongued bee" was defined as a species with a proboscis longer than 10 mm. These included Amegilla in Lambir, Amegilla and Tetralonia on the Amami Islands, Bombus diversus and Tetralonia at Mt. Yufu, B. diversus, B. ussurensis, and B. consobrinus at Mt. Kushigata, and euglossine bees at La Selva.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
A total of 551 visits by Hymenoptera were recorded, and the most abundant hymenopteran superfamily was the Apoidea sensu stricto (98.2%), followed by the Ichneumonoidea. In the Apoidea, three families, five species, and 541 individuals were recorded, and the most abundant family was the exotic Apidae (89.8% of individuals) (Figs. 5–9), followed by the Halictidae (6%) and Megachilidae (3%). We did not observe colletid bees. Native bees were observed only on 11 plant species: Agatea pancheri, Hibbertia lucens, Lomandra insularis, Melochia odorata (Fig. 3), Ranunculus sp., Rauvolfia semperflorens var. semperflorens, Scaevola balansae, Stachytarpheta cayennensis, Stenocarpus phyllodineus, Guioa glauca var. vulgaris (Fig. 2), Storthocalyx pancheri (Fig. 4), and Tetracera billardieri. A scoliid wasp was observed on a flower of Neoguillauminia cleopatra (Fig. 10).
|
A total of 95 visits by Lepidoptera was recorded (Figs. 13– 21), and the most abundant family was the Pyralidae (38% of individuals), followed by the Sphingidae (19%), Gracillariidae (16%), Noctuidae (10%), Geometridae (3%), and Micropterigidae (5%).
We recorded 64 visits by birds on 17 plant species (Albizia guillainii, Archidendropsis paivana subsp. balansae, Deplanchea speciosa, Dubouzetia caudiculata, Geissois magnifica, Geissois pruinosa, Grevillea gillivayi, Melaleuca quiquenervia, Montrouziera sphaeroidea, Oxera morierei, Serianthes petitiana, Serianthus sachetae, Strasburgeria robusta, Syzygium acre). Observed birds were two honeyeater species, Lichmera incana incana and Guadalcanaria undulata (Meliphagidae), which used their slender bills to imbibe nectar from tubular flowers (Figs. 22–26).
Flower visitor assemblages on each plant species
The flower visitor assemblages varied greatly among plant species. To explain this variance, we used a principal components analysis. Flower visitors were classified into 16 groups: thrips, Neuroptera, beetle, leafcutter bee, small bee, honey bee, wasp, ant, Diptera, hawk moth, gracillariid moth, micropterigid moth, other moths, butterfly, bird, and bat. The percentages of these 16 groups found on each plant species were defined as the flower visitor spectrum of each plant species.
The flower visitor spectra for 77 observations (71 plant species) were used in the principal component analysis. Eigenvectors of first, second, and third principal components for each insect group are shown in Fig. 27. The major trend involved the alternation of dominant insect groups between [Apis + small bee + butterfly] and [pyralid moth + Neuroptera + beetle + Diptera + others]. Variance in the first principal component, PC1, contributed to 12.1% of the total variance. The second factor corresponded to the dominance of [leafcutter bee + wasp] over [bird + hawk moth + thrips] (PC2, 9.9%). The third factor was primarily related to the alternation between [bird + beetle] and [pyralid moth] (PC3, 9.0%). The cumulative percentages of variance of the first three principal components were 31.1%, suggesting that additional factors also contributed to the total variance.
|
|
|
C2 was composed of three plant species (Loxodiscus coriaceus [Sapindaceae], Avicenia marina var. resinifera [Aviceniaceae], Alphitonia neo-caledonica [Rhamnaceae]), and was characterized by the predominance of flies.
C3 was composed of one plant species (Zygogynum baillonii), which was visited only by a micropterigid moth species, Sabatinca sp.
C4 was composed of one plant species (Hedycarya engleriana), which was visited only by thrips.
C5 included Phyllanthus aeneus and Glochidion caledonicum (Euphorbiaceae), which were visited only by gracillariid moths (Epicephala subsp.) at night.
C6 was composed of two species, Cerbesa manghas (Apocynaceae) and Oxera morierei (Verbenaceae), which were visited only by a long-tongued crepuscular hawk moth, Gnathothlibus erotus (Sphingidae), in the evening.
C7 was composed of four plant species (Alstonia, plumosa var. communis [Apocynaceae], Dracophyllum ramosum [Epacridaceae], Morinda sp. [Rubiaceae], Nepenthes vieillardii [Nepenthaceae]), and was characterized by the predominance of pyralid, geometrid, and noctuid moths.
C8 was composed of six plant species and was characterized by the predominance of beetles. For example, flowers of Hedycarya cupulata (Monimiaceae) were visited only by staphylinid beetles. This clade included two plant species that were visited by many inactive beetles but that were considered to be pollinated by actively flying moths: Grevillea exul subsp. exul (Proteaceae) and Exocarpus neo-caledonicus (Santalaceae).
C9 was composed of seven species (Montrouziera sphaeroidea [Guttiferae], Deplanchea speciosa [Bignoniaceae], Syzygium acre [Myrtaceae], Geissois pruinosa [Cunoniaceae], Albizia guillainii [Mimosaceae], Strasburgeria robusta [Strasburgeriaceae], Grevillea gillivayi [Proteaceae]), all of which were visited only by birds.
C10 was composed of 36 plant species of various families, and was characterized by the dominance of honey bees.
Community-level comparison of pollination systems
Based on the results of the analyses, the behavior of the flower visitors, and pollen attachment to their bodies, we determined the pollination system of each plant species (Table 2). Although we did not directly observe bats visiting flowers, bats were observed flying towards three species of trees: Barringtonia asiatica, Fagraea berteroana, and Crossostylis grandiflora. The flowers of these species produced strong fragrance at night, and the following morning, many damaged flowers were found at the base of the trees. Based on this circumstantial evidence, these plants were inferred to be bat-pollinated. We did not observe insects visiting flowers of Amborella trichopoda (Fig. 12), but found that the pollen was easily dispersed by wind. We therefore assumed that this species was anemophilous.
Among the 95 native plant species whose pollination systems were determined, the most dominant system was melittophily (46.3%), followed by phalaenophily (20.0%), ornithophily (11.6%), cantharophily (8.4%), myophily (3.2%), chiropterophily (3.2%), and anemophily (3.2%). Figure 30 compares the frequency distributions of pollination systems observed in various ecosystems in different biogeographical regions.
|
The frequency distribution of pollination systems in New Caledonia resembles that of tropical rain forests in Lambir, but differs in the relative prevalence of phalaenophily and in the absence of melittophily by long-tongued bees.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). The low diversity of the bee fauna in New Caledonia and the small sizes of the native bees suggest that all the native bees colonized New Caledonia mainly from Australia over the sea after the break-up of Gondwanaland (Michener, 1965
, 1979
). In contrast with the immigration of these bees in the Tertiary (Michener, 1979
; Donovan, 1983
), Apis mellifera was quite recently introduced after 1950s (Crane, 1990
) and became extremely abundant thereafter. Native bees must have been abundant and played an important role in pollination before the immigration of honey bees. We recorded 544 bee visits to flowers, of which 498 were by honey bees, and 32 and 14 were by halictid and megachilid bees, respectively. These data suggest that native bees are now endangered, and that original plant-pollinator interactions have been altered. A recent study on reproductive traits of rain-forest trees in New Caledonia based on herbarium specimens (Carpenter et al., 2003
) estimated that most plant species are pollinated by small insects, but not including bees. The small flowers of these plant species usually produce nectar and/or pollen, which are easily utilized by small insects such as beetles, flies, and bees. However, the original pollination systems of the flowers that are now visited exclusively by honey bees are hypothesized to have been melittophilous with native bees, because anthophilous flies and beetles are uncommon in the pervasively xeric habitats of New Caledonia, and because bees are preadapted in xeric habitats (Michener, 1979
).
This hypothesis is supported by a similar case observed in the Ogasawara Islands of Japan (Kato, 1992
; Kato et al., 1999
). The Ogasawara Islands are oceanic, and the original bee fauna was composed of only 10 native (nine endemic) solitary species. On islands where introduced honey bees have become established, the floral resources of most plant species are utilized exclusively by honey bees, and the native bees are now almost extinct or endangered. However, on islands that have not been invaded by honey bees, the same plant species are visited and pollinated by native bees. Similar changes in pollinator fauna caused by the introduction of honey bees have been observed in New Zealand (Thomson, 1927
; Heine, 1938
; Craig et al., 2000
) and Tasmania (Goulson et al., 2003). It is thought, therefore, that the current predominance of honey bees in New Caledonia will have serious effects on plant-pollinator interactions, e.g., drastic decreases in populations of native bees, changes in patterns of gene flow among plants, and increased reproductive fitness of invasive exotic weeds. In contrast with these cases on oceanic islands, introduced honey bees have less impact on population dynamics of native bees in Panama (Roubik and Wolda, 2001
). However, Africanized honey bees are potential competitors of native bees (Frankie et al., 1997
), and sometimes alter the genetic structure of some canopy trees while they act as important pollinators in degraded Neotropical forests (Dick, 2002
).
The relative dominance of phalaenophily may be closely related to the low diversity of native bees. Because moth-pollinated flowers open up and secrete nectar in the evening and at night when bees are not active, these flowers are used neither by native bees nor by honey bees. Extremely elongated tubular flowers were visited only by crepuscular hawkmoths and constituted a distinct pollination system. In addition to the tubular flowers that are usually visited by pyralid, geometrid, and noctuid moths, some nontubular flowers such as Nepenthes (Nepenthaceae) and Exocarpus (Santalaceae) were also visited by moths searching for nectar. In Sumatra, Nepenthes gracilis was observed to be pollinated by pyralid moths (Kato, 1993
), and a similar pollination system was observed in N. vieillardii.
Moth-pollinated flowers included unique flowers that were visited, actively pollinated, and parasitized only by minute, host-specific gracillariid moths (Kato et al., 2003
; Kawakita and Kato, 2004
). These flowers belong to Glochidion subsp. and Phyllanthus (Gomphidium) subsp. (Euphorbiaceae); the latter has undergone an unusual diversification of up to 111 species (Schmid, 1991
). The diversification of Phyllanthus contributes to the prevalence of moth-pollination in New Caledonia.
Pollination by micropterigid moths has been reported for Zygogynum subsp. (Thien et al., 1985
; Pellmyr, 1990
), and was confirmed in this study in a moss forest at Mt. Koghi. Because Zygogynum flowers do not secrete nectar, nectar-seeking insects did not visit them. Micropterigid moths were active during the daytime, and pollen was attached to their bodies around the mouthparts.
Although nectar-feeding birds are not diverse in New Caledonia, ornithophilous plants are common. Strasburgeria, a monotypic genus of the endemic Strasburgeriaceae family, bears large nectariferous flowers, which were frequently visited by honeyeaters. The most dominant birds on flowers were meliphagid honeyeaters, which perch on branches and use their slender bills to collect nectar from tubular flowers. In Australia, about 250 plant species in the Myrtaceae, Proteaceae, Loranthaceae, and Epacridaceae are visited and pollinated by more than 100 species of birds (Armstrong, 1979
; Ford et al., 1979
; Williams and Adam, 1994
). Irrespective of differences in species diversity among flower-visiting birds, plant-bird interactions (dominance of honeyeaters, floral adaptation to ornithophily, and nectar-feeding behavior of birds) are similar between Australia and New Caledonia. Pollination disruption by the introduced honey bees observed in Australian bird-pollinated plants (Vaughton, 1996
) and in plants cultivated in orchards in New Zealand (Stewart and Craig, 1989
) suggests that pollen removal by honey bees may reduce pollination success in ornithophilous plants also in New Caledonia.
Pollination systems in New Caledonia have attracted worldwide interest from many botanists because archaic plants are thought to have maintained their archaic plant-pollinator interactions since the early radiation of basal angiosperms. Some examples include the interactions observed between Zygogynum (Winteraceae) and micropterigid moths, and between Hedycarya (Monimiaceae) and beetles/thrips. Pollination by thrips has also been observed in Australian plants of the Monimiaceae, in which male and female flowers serve as brood sites for larvae of the pollinating thrips (Williams et al., 2001
). In addition, flowers of the Neotropical Siparuna subsp. (Monimiaceae) are reported to be pollinated by cecidomyiid midges, whose larvae grow in male flower tissue (Feil, 1992
). It is interesting that the floral rewards of these archaic plants to the pollinators are not nectar but pollen (in Zygogynum) or floral tissue, used as brood sites by pollinator larvae (in Hedycarya and Siparuna). The archaic plant Amborella trichopoda was reported to have been visited by various insects (Thien et al., 2003
), whereas we considered it to be anemophilous. However, the high rate of galled fruits on this species suggests that the cecidomyiid midge might be an alternative agent for pollination.
In conclusion, community-level, plant-pollinator mutualism in New Caledonia was characterized by the dominance of melittophily, ornithophily, and phalaenophily. Although some archaic plants have maintained their archaic pollination systems, most plants have adopted pollination by honeyeaters, nocturnal moths, and diurnal nectar-seeking insects such as bees. Among these three pollination systems, the establishment of honey bees would have influenced melittophily most drastically. During our surveys, feral honey bees were commonly found in all vegetation types, at every altitude, and in every locality. Our study suggests that apiculture at least in and around natural vegetation should be reconsidered in order to conserve native plant-pollinator interactions and the invaluable endemic flora of New Caledonia.
|
|
|
|
FOOTNOTES |
|---|
2 E-mail: kato{at}zoo.zool.kyoto-u.ac.jp
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Barthell J. F. J. M. Randall R. W. Thorp A. M. Wenner 2001 Promotion of seed set in yellow star-thistle by honeybees: evidence of an invasive mutualism. Ecological Monographs 11: 1870-1883
Carpenter J. R. J. Read T. Jaffré 2003 Reproductive traits of tropical rain-forest trees in New Caledonia. Journal of Tropical Ecology 19: 351-365[CrossRef][ISI]
Craig J. S. Anderson M. Lout B. Creese N. Mitchell J. Ogden M. Roberts G. Ussher 2000 Conservation issues in New Zealand. Annual Review of Ecology and Systematics 31: 61-78
Crane E. 1990 Bees and beekeeping: science, practice and world resources. Comstock Publishing Associates, Ithaca, New York, USA
De Laubenfels D. J. 1959 Parasitic conifer found in New Caledonia. Science 130: 97
Devy M. S. P. Davidar 2003 Pollination systems of trees in Kakachi, a mid-elevation wet evergreen forest in Western Ghats, India. American Journal of Botany 90: 650-657
Dick C. W. 2002 Genetic rescue of remnant tropical trees by an alien pollinator. Proceedings of the Royal Society Biological Sciences, Series B 268: 2391-2396[CrossRef]
Donovan B. J. 1983 Comparative biogeography of native Apoidea of New Zealand and New Caledonia. GeoJournal 7: 511-516
Dupont Y. L. D. M. Hansen A. Valido J. M. Olesen 2004 Impact of introuduced honey bees on native pollination interactions of the endemic Echium wildpretti (Boraginaceae) on Tenerife, Canary Islands. Biological Conservation 118: 301-311[CrossRef][ISI]
Feil J. P. 1992 Reproductive ecology of dioecious Siparuna (Monimiaceae) in Ecuador: a case of gall midge pollination. Botanical Journal of the Linnean Society 110: 171-203
Ford H. A. D. C. Paton N. Forde 1979 Birds as pollinators of Australian plants. New Zealand Journal of Botany 17: 509-519[ISI]
Frankie G. W. S. B. Vinson M. A. Rizzardi T. L. Griswold S. O'Keef R. R. Snelling 1997 Diversity and abundance of bees visiting a mass flowering tree species in distrubed seasonal dry forest, Costa Rica. Journal of the Kansas Entomological Society 70: 281-296[ISI]
Goulson D. J. C. Staut A. R. Kells 2002 Do exotic bumblebees and honeybees compete with native flower-visiting insects in Tasmania. Journal of Insect Conservation 6: 179-189[CrossRef]
Heine E. M. 1938 Observations on the pollination of New Zealand flowering plants. Transactions of the New Zealand Institute 67: 133-148
Jaffré T. P. Brooks J. Lee R. D. Reeves 1976 Sebertia acuminata, a hyperaccumulator of nickel from New Caledonia. Science 193: 579-580
Jaffré T. P. Morat J.-M. Veillon F. Rigault G. Dagostini 2001 Composition and characterisation of the native flora of New Caledonia. Institute de recherche pour le développement, Nouméa, New Caledonia
Kato M. 1992 Endangered bee fauna and its floral hosts in the Ogasawara Islands. Japanese Journal of Entomology 60: 487-494
Kato M. 1993 Floral biology of Nepenthes gracilis (Nepenthaceae) in Sumatra. American Journal of Botany 80: 924-927[CrossRef][ISI]
Kato M. 2000 Anthophilous insect community and plant-pollinator interactions on Amami Islands in Ryukyu Archipelago, Japan. Contributions from Biological Laboratory, Kyoto University 29: 157-252 pl. 2–3
Kato M. M. Matsumoto T. Kato 1993 Flowering phenology and anthophilous insect community in the cool-temperate subalpine forests and meadows at Mt. Kushigata in the central part of Japan. Contributions from Biological Laboratory, Kyoto University 28: 119-172
Kato M. S. Shibata T. Yasui H. Nagamasu 1999 Impact of introduced honeybees, Apis mellifera, upon native bee communities in the Bonin (Ogasawara) Islands. Researches on Population Ecology 41: 217-228[CrossRef][ISI]
Kato M. A. Takimura A. Kawakita 2003 An obligate pollination mutualism and reciprocal diversification in the tree genus Glochidion (Euphorbiaceae). Proceeding of National Academy of Science 100: 5264-5267[CrossRef]
Kawakita A. M. Kato 2004 Evolution of obligate pollination mutualism in New Caledonian Phyllanthus (Euphorbiaceae). American Journal of Botany 91: 410-415
Kevan P. G. H. G. Baker 1983 Insects as flower visitors and pollinators. Annual Review of Entomology 28: 407-453[CrossRef][ISI]
Kress W. J. J. H. Beach 1994 Flowering plant reproductive systems. In L. A. McDade, K. S. Bawa, H. A. Hespenheide, and G. S. Hartshorn [eds.], La Selva: ecology and natural history of a neotropical rain forest, 19–33. University of Chicago Press, Chicago, Illinois, USA
Michener C. D. 1965 A classification of the bees of the Australian and South Pacific regions. Bulletin of the American Museum of Natural History 130: 1-362
Michener C. D. 1979 Biogeography of the bees. Annals of the Missouri Botanical Garden 66: 277-347[CrossRef][ISI]
Momose K. T. Yumoto T. Nagamitsu M. Kato H. Nagamasu S. Sakai R. D. Harrison T. Itioka A. A. Hamid T. Inoue 1998 Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. American Journal of Botany 85: 1477-1501
Morat P. J. M. Veillon H. S. Mackee 1984 Floristic relationships of New Caledonian rain forest phanerogams. In F. J. Radovsky, P. H. Raven, and S. H. Sohmer [eds.], Biogeography of the tropical Pacific, 71–128. Association of Systematics Collections, Bernice P. Bishop Museum, Honolulu, Hawaii, USA
Paton D. C. 1993 Honeybees in the Australian environment: does Apis mellifera disrupt or benefit the native biota?. BioScience 43: 95-103[CrossRef][ISI]
Stewart A. M. J. L. Craig 1989 Factors affecting pollinator effectiveness in Feijoa sellowiana. New Zealand Journal of Crop and Horticultural Science 17: 145-154[ISI]
Pellmyr O. L. B. Thien G. Bergström I. Groth 1990 Pollination of New Caledonian Winteraceae: opportunistic shifts or parallel radiation with their pollinators?. Plant Systematics and Evolution 173: 143-157[CrossRef][ISI]
Roubik D. W. 1978 Competitive interactions between Neotropical pollinators and Africanized honey bees. Science 201: 1030-1332
Roubik D. W. H. Wolda 2001 Do competing honey bees matter? Dynamics and abundance of native bees before and after honey bee invasion. Population Ecology 43: 53-62[CrossRef][ISI]
SAS. 1985 SAS user's guide. Statistics, version 5. SAS Institute, Cary, North Carolina
Schmid M. 1991 Euphorbiaceae, Phyllanthoideae, Phyllanthus. Flora de la Nouvelle-Calédonie et Dépendances 17: 31-323
Soltis P. S. D. E. Soltis M. W. Chase 1999 Angiosperm phylogeny inferred from multiple chloroplast genes as a tool for comparative biology. Nature 402: 402-404
Takhtajan A. 1986 Floristic regions of the world. University of California Press, Los Angeles, California, USA
Thien L. B. B. P. Bernhardt G. Gibbs O. Pellmyr G. Bergström I. Groth G. McPherson 1985 The pollination of Zygogynum (Winteraceae) by the moth, Sabatinca (Micropterigidae): an ancient association?. Science 227: 540-543
Thien L. B. T. L. Sage T. Jaffré P. Bernhardt V. Pontieri P. H. Weston D. Malloch H. Azuma S. W. Graham M. A. McPherson H. S. Rai R. F. Sage J.-J. Dupre 2003 The population structure and floral biology of Amborella trichopoda (Amborellaceae). Annals of the Missouri Botanical Garden 90: 466-490[CrossRef][ISI]
Thomson G. M. 1927 The pollination of New Zealand flowers by birds and insects. Transactions of the New Zealand Institute 57: 106-125
Vaughton G. 1996 Pollination disruption by European honeybees in the Australian bird-pollinated shrub Grevillea barklyana (Proteaceae). Plant Systematics and Evolution 200: 89-100[CrossRef][ISI]
Waser N. M. L. A. Real 1979 Effective mutualism between sequentially flowering plant species. Nature 281: 670-672[CrossRef][ISI]
Williams G. P. Adam 1994 A review of rainforest pollination and plant-pollinator interactions with particular reference to Australian subtropical rainforests. Australian Zoologist 29: 177-212
Williams G. P. Adam L. A. Mound 2001 Thrips (Thysanoptera) pollination in Australian subtropical rainforests, with particular reference to pollination of Wilkiera huegeliana (Monimiaceae). Journal of Natural History 29: 177-212
Yamazaki K. M. Kato 2003 Flowering phenology and anthophilous insect community in a grassland ecosystem at Mt. Yufu, Western Japan. Contributions from Biological Laboratory, Kyoto University 29: 255-318 pl. 4–5
This article has been cited by other articles:
|
|
 |
|
  T. ABE Threatened Pollination Systems in Native Flora of the Ogasawara (Bonin) Islands Ann. Bot., August 1, 2006; 98(2): 317 - 334. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
