American Journal of Botany 91(11): 1814±1827. 2004.

PLANT-POLLINATOR INTERACTIONS IN NEW CALEDONIA INFLUENCED BY INTRODUCED HONEY BEES1

MAKOTO KATO2 AND ATSUSHI KAWAKITA

Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu-cho, Sakyo-ku, Kyoto, 606±8501 Japan

The ¯ora of New Caledonia is characterized by remarkably high species diversity, high endemicity, and an unusual abundance of archaic plant taxa. To investigate community-level pollination mutualism in this endemic ecosystem, we observed ¯ower visitors on 99 plant species in 42 families of various types of vegetation. Among the 95 native plant species, the most dominant pollination system was melittophily (bee-pollinated, 46.3%), followed by phalaenophily (moth-pollinated, 20.0%), ornithophily (bird-pollinated, 11.6%), cantharophily (beetle-pollinated, 8.4%), myophily (¯y-pollinated, 3.2%), chiropterophily (bat-pollinated, 3.2%), and anemophily (wind- pollinated, 3.2%). The prevalence of ornithophily by honeyeaters shows an ecological link to pollination mutualism in Australia. The relative dominance of phalaenophily is unique to New Caledonia, and is proposed to be related to the low diversity of the original bee fauna and the absence of long-tongued bees. Although some archaic plants maintain archaic plant-pollinator interactions, e.g., Zygogynum pollinated by micropterigid moths, or Hedycarya pollinated by thrips and staphylinid beetles, the most dominant organism observed on ¯owers was the introduced honey bee, Apis mellifera. The plant species now visited by honey bees are thought to have originally been pollinated by native solitary short-tongued bees. Our data suggest that the unique systems of pollination mutualism in New Caledonia are now endangered by the establishment of highly invasive honey bees.

Key words: bird pollination; honey bee invasion; New Caledonia; plant-pollinator interactions; pollination.

The ¯ora of New Caledonia is characterized by remarkably that the archaic Zygogynum subsp. are pollinated by primitive high species diversity (about 3000 species of seed plants) and micropterigid moths (Thien et al., 1985; Pellmyr et al., 1990) high endemicity (84%; Morat et al., 1984; Jaffre et al., 2001). that do not have nectar-collecting proboscides. The high diversity and endemicity result from the long history However, community-level studies on plant-pollinator inter- of this land mass remaining above sea level after the breakup actions have not yet been made in New Caledonia. Such stud- of Gondwanaland in the Mesozoic; they are also the result, in ies are important and necessary, because plant-pollinator in- part, of the climatic and geological diversity of habitats within teractions on oceanic islands are easily and rapidly degraded Grand Terre Island. The ¯ora of New Caledonia is also char- by the invasion of honey bees (Kato, 1992; Kato et al., 1999; acterized by an unusual abundance of archaic plant taxa (i.e., Dupont et al., 2004). Social bees were originally absent on basal angiosperm lineages), such as the Amborellaceae, Win- most oceanic islands, as it was often dif®cult for them to cross teraceae, and Monimiaceae (Takhtajan, 1986). The Amborel- the sea (Michener, 1979). Although New Caledonia is not an laceae are thought to be the most basal family of angiosperms oceanic island but rather a fragment of Gondwanaland, the (Soltis et al., 1999). These attributes of New Caledonian ¯ora only bees originally recorded in New Caledonia are solitary have attracted botanical and ecological interest, inspiring many short-tongued bees in the families Colletidae, Halictidae, and studies of plants on the islands (e.g., De Laubenfels, 1959; Megachilidae (Michener, 1965). Because honey bees can com- Jaffre et al., 1976; Thien et al., 1985, 2003; Pellmyr et al., municate the exact site of ¯owers to nestmates by dancing, 1990; Carpenter et al., 2003; Kawakita and Kato, 2004). they have often outcompeted native solitary bees, not only on The ¯oristically distinct area termed the New Caledonia oceanic islands but also in Australia (Paton, 1993), North Subkingdom by Takhtajan (1986) also provides a fascinating America (Barthell, 2001), and the Neotropics (Roubik, 1978), ecosystem from the perspective of pollination mutualism. It is where social bees (stingless bees and/or bumblebees) but not of great ecological and evolutionary interest to investigate honey bees were native. original plant-pollinator interactions that have potentially Because the ¯ora of New Caledonia has links with Austra- shaped the uniqueness and richness of the ¯ora in New Ca- lia, New Guinea, and New Zealand (Morat et al., 1984), plant- ledonia. Community-level plant-pollinator interactions are pollinator interactions are predicted to be similar to those in founded on mutualisms between plants and their pollinators, Gondwanaland. Pollination systems of various plants in New as well as on competition between plants for pollinators, and Zealand were observed from 1920 to 1935, when introduced competition between pollinators for ¯oral resources (Waser honey bees were not as abundant as they are now (Thomson, and Real, 1979; Kevan and Baker, 1983). Pioneering works 1927; Heine, 1938). The data of these pioneering studies sug- on pollination systems in New Caledonia have demonstrated gest that the most dominant pollination system in New Zealand was myophily, followed by general entomophily, melittophily, 1 Manuscript received 14 December 2003; revision accepted 30 July 2004. and ornithophily. However, the increase in populations of in- The authors thank C. Lambert, T. Joseph, J.-J. Cassan, R. PouytieÂla, and troduced honey bees and bumblebees caused a decrease in all other staff at the Direction des Ressources Naturelles de la Province Sud native pollinators (Craig et al., 2000). The drastic changes in et Nord for their assistance and permission to study in New Caledonia, and pollination mutualism in New Zealand suggest that it is urgent, A. Takimura, L. Daniel, and T. Atkins for their help in the ®eld. This study was supported by a Japan Ministry of Education, Culture, Science, Sports, if it is not already too late, that study of the original systems and Technology Grant-in-Aid for Scienti®c Research (#12440217). of pollination mutualism in New Caledonia be undertaken. 2 E-mail: [email protected]. To investigate community-level pollination mutualism in the 1814 November 2004] KATO AND KAWAKITAÐPOLLINATION SYSTEMS IN NEW CALEDONIA 1815

TABLE 1. A list of study sites where we made surveys on ¯ower visitors in New Caledonia, with latitude, longitude, altitude, vegetation and rocks at each site.

Code Site Latitude Longitude Altitude Vegetationa Rockb S1 Tiebaghi 20Њ 27.3ЈS 164Њ13.1ЈE 350±580 M/F U S2 Chagrin 20Њ 26.1ЈS 164Њ15.0ЈE 30±150 S S S3 La Koumac 20Њ 32.2ЈS 164Њ20.8ЈE 100±200 F C S4 La Bouverie 20Њ 27.9ЈS 164Њ20.4ЈE 100±200 S S S5 Koumac 20Њ 34.6ЈS 164Њ17.9ЈE 0±5 G A S6 Col de Amoss 20Њ 18.6ЈS 164Њ25.1ЈE 300±350 F A S7 Tinip 20Њ 47.5ЈS 164Њ27.4ЈE 10±80 L A S8 Voh 20Њ 56.2ЈS 164Њ43.8ЈE 0±20 S A S9 Oundjo 21Њ 8.7ЈS 164Њ45.3ЈE 0±5 G A S10 Pouembout 21Њ 11.2ЈS 164Њ53.1ЈE 10±50 S C S11 Pindai 21Њ 17.1ЈS 164Њ58.5ЈE 10±60 L C S12 Nepoui 21Њ 18.1ЈS 165Њ0.3ЈE 10±50 L C S13 Hiengene 20Њ 40.1ЈS 165Њ55.4ЈE 10±40 F A S14 Col de Tango 21Њ 0.2ЈS 164Њ1.4ЈE 200±250 F A S15 Bopope 20Њ 54.5ЈS 165Њ7.1ЈE 300±400 F A S16 Poindimie 20Њ 56.6ЈS 165Њ21.6ЈE 0±20 F A S17 Cap Bocage 21Њ 10.2ЈS 165Њ32.4ЈE 0±20 M/G U S18 Chute de Ba 21Њ 11.9ЈS 165Њ33.6ЈE 20±50 F U S19 Col des Roussettes 21Њ 25.9ЈS 165Њ27.1ЈE 250±300 F U S20 Poro 21Њ 20.0ЈS 165Њ44.1ЈE 100±250 M U S21 Kouaoua 21Њ 23.5ЈS 165Њ46.4ЈE 200±250 M U S22 Col de Amieu 21Њ 35.5ЈS 165Њ48.5ЈE 300±360 F A S23 Plateau de Dogny 21Њ 36.9ЈS 165Њ52.3ЈE 400±1010 F A S24 Saramea 21Њ 38.5ЈS 165Њ51.3ЈE 140±190 F A S25 Mt. Mou 22Њ 4.01ЈS 165Њ20.2ЈE 500±1219 F/M U S26 Mt. Koghi 22Њ 10.7ЈS 166Њ30.9ЈE 400±1075 F/M U S27 Noumea 22Њ 16.4ЈS 166Њ24.0ЈE 0±5 S C S28 Riviere Bleue 22Њ 6.0ЈS 166Њ39.5ЈE 100±300 M/F U S29 Col de Mouirange 22Њ 13.3ЈS 166Њ40.3ЈE 300±400 M U S30 Prony 22Њ 19.4ЈS 166Њ48.2ЈE 50±150 M U S31 Col de Yate 22Њ 9.8ЈS 166Њ54.0ЈE 300±400 M U a F: forest; M: mangrove; L: sclerophyllus forest; M: maquis; S: shrubby savanna. b A: acidic; C: calcarious; S: silicaceous; U: ultrabasi®c. endemic ecosystem in New Caledonia, we surveyed pollinator looked at whether or not birds visited the ¯owers by studying the ¯owers visits to the ¯owers of diverse species of various vegetation from at least 10 m away for an additional 15 min. For ¯owers that were not types. We observed 99 plant species, encompassing 42 fami- visited by insects or birds during the daytime or that did not receive visits lies of most major lineages of ¯owering plants. Our data high- that would have led, in all likelihood, to effective pollination, we made ad- light the uniqueness of pollination mutualism in New Cale- ditional observations in the evening and/or at night. Visitations by nocturnal donia, its links to other vegetation in the world, and the en- insects and bats were studied as described for diurnal insects and birds, re- dangered status of the observed interactions. This is the ®rst spectively. Thus, a data set of all bird/insect visits to ¯owers was created. study that describes community-level plant-pollinator interac- Principal components analysis and cluster analysis were performed on the tions in this ¯oristic region, i.e., in the New Caledonian Sub- data set to detect patterns of anthophilous insect communities on different kingdom. plant species. In these analyses, observations of fewer than four visits were excluded. Thus, 77 observations on 71 plant species were included in the METHODS analysis. Flower visitors were grouped into 16 functional/taxonomical groups: thrips, Neuroptera, beetle, leafcutter bee, small bee, honey bee, wasp, ant, We made ®eld surveys of ¯ower visitors at 31 sites with diverse vegetation Diptera, hawk moth, gracillariid moth, micropterigid moth, other moths, but- types on Grande Terre Island in New Caledonia (Table 1; Fig. 1). The studied ter¯y, bird, and bat. Statistical analyses were made using SAS (1985) in the habitats covered 15 forests, ten maquis, three mangroves, three sclerophyllous Data Processing Center at Kyoto University. forests, and four shrubby savannas, which had formed on various rock foun- In addition, we evaluated the behavior and/or pollen attachment on the dations. bodies of ¯ower visitors, and then determined the pollination system of each Flower visitors were surveyed from 28 to 31 August and 7 to 13 September plant species. The frequency distribution of pollination systems of 95 native 2001, 19 to 29 March 2002, and 29 October to 8 November 2002. Whenever plant species in New Caledonia was compared to those of various ecosystems ¯owering plants were encountered, ¯ower visitors were observed and record- in different biogeographical regions: temperate deciduous forests in New Zea- ed for approximately 8 min per ¯ower stand. After this observation, the ¯ow- land (Thomson, 1927; Heine, 1938), a tropical rain forest in Kakachi, India ers were swept with a net for 2 min to collect all insect visitors remaining on (Devy and Davidar, 2003), a tropical dipterocarp forest in Lambir, Sarawak them. If no ¯ower visitor was found, we occasionally extended observation (Momose et al., 1998), subtropical forests on Amami Island, Japan (Kato, time up to1htodetect rare visitors. This sampling method is con®rmed to 2000), temperate deciduous forests and grasslands at Mt. Yufu on Kyushu be appropriate to detect an overall pattern of the anthophilous insect com- Island, Japan (Yamazaki and Kato, 2003), cool temperate subalpine coniferous munity (Kato et al., 1993; Kato, 2000; Yamazaki and Kato, 2003). All col- forests and meadows at Mt. Kushigata on Honshu Island, Japan (Kato et al., lected specimens were brought back to the laboratory for identi®cation and 1993), and tropical rain forests in La Selva, Costa Rica (Kress and Beach, determination of pollen attached to their bodies. If no insect visitors were 1994). Although only trees are included in the data set of Kakachi, both observed during the whole 10-min period (and in additional observation), we herbaceous and woody plants are included in the other data sets. In classifying 1816 AMERICAN JOURNAL OF BOTANY [Vol. 91

Fig. 1. Map of New Caledonia, showing study sites S1±S31. Shaded areas denote the distribution of ultrabasic rocks.

¯ower visitors into groups, ``long-tongued bee'' was de®ned as a species with (four species), Mimosaceae (four species), Proteaceae (four a proboscis longer than 10 mm. These included Amegilla in Lambir, Amegilla species), Sapindaceae (four species), and Verbenaceae (four and Tetralonia on the Amami Islands, Bombus diversus and Tetralonia at Mt. species). Yufu, B. diversus, B. ussurensis, and B. consobrinus at Mt. Kushigata, and euglossine bees at La Selva. Observed ¯ower visitorsÐA total of 748 visits were ob- RESULTS served to ¯owers of 99 plant species (Table 2). The most rep- resentative group (in numbers of individuals) was Hymenop- Observed plant speciesÐFrom 2001 to 2002, we made 126 tera (53%), followed by Coleoptera (20%), Lepidoptera (9%), observations (41 in March, seven in August, 13 in September, Thysanoptera (8%), Aves (6%), Diptera (3%), and others. In- and 65 in November) of ¯ower visitors to each plant species troduced honey bees (Apis mellifera) comprised 48% of total in New Caledonia. By means of these observations, we ob- visits. We recorded honey bees at 24 sites including the sum- served ¯ower visitors on 99 plant species from 71 genera and mits of Mt. Tiebaghi (S1) and Mt. Mou (S25) (Table 2), and 42 families (Table 2). The studied plants included two annuals, this suggests that honey bees have naturalized in natural veg- two climbing perennials, ®ve lianas, 10 perennials, 43 shrubs, etation. and 37 trees. Of the studied plant species, 96% were native A total of 551 visits by Hymenoptera were recorded, and (95 species), and 83% were endemic (82 species). The ob- the most abundant hymenopteran superfamily was the Apoidea served plants contained two species belonging to endemic sensu stricto (98.2%), followed by the Ichneumonoidea. In the families (Amborellaceae and Strasburgeriaceae). The Myrta- Apoidea, three families, ®ve species, and 541 individuals were ceae was the most representative plant family (with 11 spe- recorded, and the most abundant family was the exotic Apidae cies), followed by the Cunoniaceae (nine species), Euphorbi- (89.8% of individuals) (Figs. 5±9), followed by the Halictidae aceae (six species), Epacridaceae (®ve species), Dilleniaceae (6%) and Megachilidae (3%). We did not observe colletid

→

Figs. 2±26. Pollinator visits to ¯owers observed in New Caledonia. 2. Guioa glauca var. vulgaris visited by a native halictid bee, Nomia sp. 3. Melochia odorata visited by a native megachilid bee, Megachile sp. 4. Storthocalyx pancheri visited by a native halictid bee, Homalictus sp. 5. Tetracera billardieri visited by a honey bee, Apis mellifera. 6. Scaevora cylindrica visited by a honey bee. 7. Hugonia penicillanthemum visited by a honey bee. 8. Xanthostemon myrtifolius visited by a honey bee. 9. Cloezia ¯oribunda visited by a honey bee. 10. Neoguillauminia cleopatra visited by a scoliid wasp. 11. Hedycarya engleriana visited by a thrip. 12. Male ¯owers of Amborella trichopoda. 13. Morinda sp. visited by a pyralid moth. 14. Alstonia plumosa var. communis visited November 2004] KATO AND KAWAKITAÐPOLLINATION SYSTEMS IN NEW CALEDONIA 1817

by a noctuid moth. 15. Wikstroemia indica visited by a pyralid moth. 16. Dracophyllum ramosum visited by a pyralid moth. 17. Exocarpus phyllanthoides visited by a pyralid moth. 18. Female ¯owers of Nepenthes vieillardii visited by a pyralid moth. 19. Zygogynum baillonii visited by a micropterigid moth, Sabatinca sp. 20. Female gracillariid moth, Epicephala sp., ovipositing into the stigma of a female ¯ower of Glochidion caledonicum. 21. Stachytarpheta cayennensis visited by a pierid butter¯y, Anapheis java. 22. Montrouziera sphaeroidea visited by a honeyeater, Guadalcanaria undulata. 23. Syzygium acre visited by a honeyeater. 24. Geissois pruinosa visited by a honeyeater. 25. Grevillea gillivayi visited by a honeyeater, Lichmera incana incana. 26. Strasburgeria robusta visited by a honeyeater, Guadalcanaria undulata. 1818 AMERICAN JOURNAL OF BOTANY [Vol. 91

TABLE 2. A list of plant species on which ¯ower-visitors were observed in New Caledonia. For each plant species, habitat, nativeness, ¯ower shape, ¯ower symmetry, ¯ower color, site where an observation was made, date of the observation, number of observed ¯owers, time of the observation, number of observed visits by each ¯ower-visitor group, and estimated pollinator are shown.

Flower Flower Flower No. observed observation Family Plant species Code Habitata Nativenessb shapesc symmetryd colore Site Date ¯owersf timeg Amborellaceae Amborella trichopoda amb1 T E O A W S23 22-Mar 2002 3 D Anacardiaceae Schinus terebinthifolius ana1 T A O A W S13 25-Mar 2002 3 D Anacardiaceae Schinus terebinthifolius ana1 T A O A W S5 5-Nov 2002 3 D Apocynaceae Alstonia plumosa var. communis apo1 T E T A W S26 6-Nov 2002 3 N Apocynaceae Cerbesa manghas apo2 T N T A W S17 1-Nov 2002 2 N Apocynaceae Rauvol®a semper¯orens var. apo3 S E T A W S20 28-Mar 2002 2 D semper¯orens Ascleiadaccae Tylophora sp. asc1 C E O A P S23 22-Mar 2002 2 D Aviceniaceae Avicenia marina var. resinifera avi1 S N O A Y S9 5-Nov 2002 3 D Bignoniaceae Deplanchea speciosa big1 T E G Z O S28 29-Oct 2002 2 D Bignoniaceae Deplanchea speciosa big1 T E G Z O S28 31-Aug 2001 2 D Bignoniaceae Deplanchea speciosa big1 T E G Z O S28 19-Mar 2002 2 D Chrysobalanaceae Hunga gerontogea chr1 S E O Z W S2 9-Sep 2001 3 D Cunoniaceae Codia discolor cun1 S E B A C S1 5-Nov 2002 4 D Cunoniaceae Codia nitida cun2 S E B A C S28 30-Oct 2002 4 D Cunoniaceae Codia obcordata cun3 S E B A C S20 31-Oct 2002 4 D Cunoniaceae Codia obcordata cun3 S E B A C S26 6-Nov 2002 4 D Cunoniaceae Codia obcordata cun3 S E B A C S28 30-Oct 2002 4 D Cunoniaceae Cunonia sp. cun4 S E B A W S22 8-Sep 2001 3 D Cunoniaceae Geissois magni®ca cun5 T E B A R S21 28-Mar 2002 4 D Cunoniaceae Geissois pruinosa cun6 T E B A R S29 30-Mar 2002 4 D Cunoniaceae Pancheria elegans cun7 S E B A C S2 9-Sep 2001 4 D Cunoniaceae Pancheria elliptica cun8 S E B A C S26 8-Nov 2002 4 D Cunoniaceae Pancheria hirsuta cun9 S E B A C S25 12-Sep 2001 4 D Dilleniaceae Hibbertia pulchella dil1 S E O A Y S30 7-Nov 2002 2 D Dilleniaceae Hibbertia lucens dil2 S E O A Y S1 5-Nov 2002 2 D Dilleniaceae Hibbertia trachyphylla dil3 S E O A Y S28 29-Oct 2002 2 D Dilleniaceae Tetracera billardieri dil4 L N O A W S17 2-Nov 2002 2 D Elacocarpaceae Dubouzetia caudiculata ela1 S E G A C S1 5-Nov 2002 2 D Elacocarpaceae Elaeocarpus nodosus ela2 T E C A W S1 5-Nov 2002 3 D Elacocarpaceae Elaeocarpus seringii ela3 T E C A W S3 4-Nov 2002 3 D Epacridaceae Dracophyllum verticillatum epa1 P E T A W S26 6-Nov 2002 3 D Epacridaceae Dracophyllum ramosum epa2 P E T A W S17 2-Nov 2002 3 N Epacridaceae Dracophyllum ramosum epa2 P E T A W S28 30-Aug 2001 3 N Epacridaceae Styphelia albicans epa3 S E T A W S25 21-Mar 2002 3 D Epacridaceae Styphelia cymbulae epa4 S E T A W S20 28-Mar 2002 3 D Epacridaceae Styphella cymbulae epa4 S E T A W S28 19-Mar 2002 3 D Epacridaceae Styphella ¯oribunda epa5 S E T A R S20 31-Oct 2002 3 D Euphorbiaceae Glochidion caledonicum eup1 T E A A G S17 2-Nov 2002 3 N Euphorbiaceae Glochidion vieillardii eup2 T E A A G S17 2-Nov 2002 3 N Euphorbiaceae Neoguillauminia cleopatra eup3 S E A A G S17 6-Nov 2002 2 D Euphorbiaceae Phyllanthus aeneus eup4 S E A A W S26 27-Mar 2002 2 N Euphorbiaceae Phyllanthus bourgeoisii eup5 S E A A C S17 31-Oct 2002 3 N Euphorbiaceae Phyllanthus mangenotii eup6 S E A A W S17 1-Nov 2002 2 N Gesneriaceae Depanthus sp. gcs1 T E C Z W S23 22-Mar 2002 2 D Goodeniaceae Scaevola balansae goo1 S E C Z W S16 25-Mar 2002 2 D Goodeniaceae Scaevola balansae goo1 S E C Z W S28 19-Mar 2002 2 D Goodeniaceae Scaevora cylindrical goo2 S E C Z W S20 28-Mar 2002 2 D Guttiferae Montrouziera sphaeroidea gut1 T E S A P S28 29-Oct 2002 2 D Guttiferae Montrouziera sphaeroidea gut1 T E S A P S30 7-Nov 2002 2 D Guttiferae Montrouziera verticillata gut2 T E S A P S25 21-Mar 2002 1 D Laxmanniaccae Lomandra insularis lax1 P E O A W S20 31-Oct 2002 2 D Lecythidaceae Barringtonia asiatica lec1 T E B A W S17 2-Nov 2002 2 N Linaccae Hugonia penicillanthemum lin1 S E O A Y S28 30-Oct 2002 3 D Loganiaceae Fagraea berteroana log1 T E T A W S17 31-Oct 2002 2 N Loganiaceae Fagraea berteroana log1 T E T A W S26 20-Mar 2002 2 N Mimosaceae Albizia guillainii mim1 T E B A P S8 6-Nov 2002 4 D Mimosaceae Archidendropsis paivana subsp. mim2 T E B A W S10 3-Nov 2002 3 D balansae Mimosaceae Serianthes petitiana mim3 T E B A P S28 30-Oct 2002 3 D Mimosaceae Serianthus sachetae mim4 T E B A P S26 6-Nov 2002 3 Monimiaceae Hedycarya cupulata mon1 T E A A C S23 22-Mar 2002 2 D a A: annual; C: climber; L: liana; P: perennial; S: shrub; T: tree. b A: alien; E: endemic; N: non-endemic native. c A: apetalous; B: brush; C: cup-shaped; G: gullet; O: open; P: pallilionate; S: spherical; T: tubular. d A: actinomorphic; Z: zygomorphic. e C: cream; B: brown; G: green; O: orange; P: pink; R: red; W: white; Y: yellow. f 1: 1±9, 2: 10±99; 3: 100±999; 4: 1000±9999. g D: daytime; N: nighttime. November 2004] KATO AND KAWAKITAÐPOLLINATION SYSTEMS IN NEW CALEDONIA 1819

TABLE 2. Extended.

Number of observed visitors Hymenoptera Lepidoptera Estimated thrips neuropterans beetle honey bee leafcutter bee small bee wasp ant dipterans hawk moth gracillariid micropterigid other moths butter¯y bird bat total pollinator 1 1 wind 9 2 11 honey bee 15 15 honey bee 5 5 moth 5 5 hawk moth 4 2 6 honey bee

1 1 butter¯y 4 8 12 honey bee 3 4 7 bird 5 5 bird 33bird 8 8 honey bee 6 1 7 honey bee 16 16 beetle 6 6 honey bee 16 7 honey bee 15 15 honey bee 12 12 honey bee 2 2 bird 6 6 bird 12 12 beetle 3 3 beetle 7 7 honey bee 6 5 11 honey bee 3 1 4 honey bee 3 3 honey bee 42 2 44 honey bee 1 1 bird 2 2 honey bee 9 9 honey bee 8 8 honey bee 7 7 moth 1 6 7 moth 3 3 honey bee 6 6 honey bee 3 3 honey bee 2 2 honey bee 4 4 gracillariid 2 2 gracillariid 21 3 honey bee 4 4 gracillariid 3 3 gracillariid 2 2 gracillariid 4 4 honey bee 12 3 small bee 1 1 2 honey bee 1 1 honey bee 4 4 bird 4 4 bird 3 3 beetle 2 12 5honey bee 1 bat 8 8 honey bee 1 bat 1 bat 6 6 bird 15 1 16 honey bee

2 2 bird 2 2 bird 2 2 beetle 1820 AMERICAN JOURNAL OF BOTANY [Vol. 91

TABLE 2. Continued.

Flower Flower Flower No. observed Observation Family Plant species Code Habitata Nativenessb shapesc symmetryd colore Site Date ¯owersf timeg Monimiaceae Hedycarya cupulata mon1 T E A A C S26 20-Mar 2002 2 D Monimiaceae Hedycarya engleriana mon2 T E A A C S15 24-Mar 2002 2 D Monimiaceae Hedycarya parvifolia mon3 T E A A C S28 20-Mar 2002 2 D Myrtaceae Baeckea leratii myr1 S E O A W S28 29-Oct 2002 3 D Myrtaceae Baeckea leratii myr1 S E O A W S28 30-Oct 2002 3 D Myrtaceae Baeckea virgata myr2 S E O A W S17 2-Nov 2002 3 D Myrtaceae Baeckea virgata myr2 S E O A W S2 10-Sep 2001 3 D Myrtaceae Baeckea virgata myr2 S E O A W S20 31-Oct 2002 3 D Myrtaceae Cloezia ¯oribunda myr3 S E O A Y S28 29-Oct 2002 3 D Myrtaceae Eugenia sp. myr4 S E B A W S20 28-Mar 2002 3 D Myrtaceae Melaleuca quiquenervia myr5 T E B A W S28 19-Mar 2002 3 D Myrtaceae Melaleuca quiquenervia myr5 T E B A W S6 10-Sep 2001 3 D Myrtaceae Syzygium acre myr6 T E B A R S28 29-Oct 2002 2 D Myrtaceae Syzygium koumacense myr7 T E B A W S3 4-Nov 2002 2 D Myrtaceae Tristaniopsis guillainii var. myr8 S E O A Y S7 22-Mar 2002 3 D guillainii Myrtaceae Tristaniopsis yateensis myr9 S E O A Y S31 13-Sep 2001 3 D Myrtaceae Xanthostemon myrtifolius myr10 S E B A O S28 19-Mar 2002 3 D Nepenthaceae Nepenthes vieillardii nep1 P E O A B S28 29-Mar 2002 3 N Papilioaaceae Vigna marina pap1 C N P Z Y S27 28-Aug 2001 2 D Poaceae Chrysopogon aciculatus poa1 P N O A G S28 30-Aug 2001 3 D Poaceae Ischaemum sp. poa2 A N O A G S2 10-Sep 2001 3 D Proteaceae Grevillea exul subsp. exul pro1 T E B A W S17 2-Nov 2002 4 N Proteaceae Grevillea exul subsp. exul pro1 T E B A W S25 21-Mar 2002 3 D Proteaceae Grevillea exul subsp. rubiginosa pro2 T E B A W S28 30-Oct 2002 3 D Proteaceae Grevillea exul subsp. rubiginosa pro2 T E B A W S29 7-Nov 2002 3 D Proteaceae Grevillea gillivayi pro3 T E B A W S28 31-Aug 2001 3 D Proteaceae Stenocarpus phyllodineus pro4 S E T A W S1 5-Nov 2002 3 D Proteaceae Stenocarpus phyllodineus pro4 S E T A W S2 24-Mar 2002 3 D Proteaceae Stenocarpus umbelliferus pro5 S E T A C S20 28-Mar 2002 3 D Ranunculaceae Ranunculus sp. ran1 P A O A Y S14 3-Nov 2002 2 D Rhamnaceae Alphitonia neo-caledonica rha1 T E O A G S28 19-Mar 2002 3 D Rhamnaceae Alphitonia neo-caledonica rha1 T E O A G S28 30-Oct 2002 3 D Rhamnaceae Colubrina asiatica var. asiatica rha2 S N O A G S9 22-Mar 2002 3 D Rhizophoraceae Cerlops lagal rhi1 T N C A W S5 5-Nov 2002 3 D Rhizophoraceae Crossostylis grandi¯ora rhi2 T E B A W S14 3-Nov 2002 2 D Rubiaceae Morinda citrifolia rub1 S N T A W S17 27-Mar 2002 2 N Rubiaceae Morinda citrifolia rub1 S N T A W S17 1-Nov 2002 2 N Rubiaceae Morinda sp. rub2 L E T A B S11 3-Nov 2002 2 N Rubiaceae Normandia neocaledonica rub3 S E T A W S25 12-Sep 2001 2 D Santalaceae Exocarpus neo-caledonicus san1 S E O A C S28 30-Aug 2001 2 N Santalaceae Exocarpus phyllanthoides san2 S E O A C S1 5-Nov 2002 2 N Sapindaceae Elateostachys apetala sap1 T N O A W S10 3-Nov 2002 3 D Sapindaceae Guioa glauca var. glauca sap2 S E O A W S28 19-Mar 2002 3 D Sapindaceae Guioa glauca var. vulgaris sap3 S E O A W S28 30-Oct 2002 3 D Sapindaceae Loxodiscus coriaceus sap4 T E O Z P S26 8-Nov 2002 3 D Sapindaceae Storthocalyx pancheri sap5 S E O A W S20 28-Mar 2002 3 D Simaroubaceae Soulamea sp. sap6 T E O A C S29 30-Oct 2002 2 D Sterculiaceae Melochia odorata ste1 T N O A P S15 24-Mar 2002 3 D Sterculiaceae Melochia odorata ste1 T N O A P S19 31-Oct 2002 3 D Sterculiaceae Melochia odorata ste1 T N O A P S2 10-Sep 2001 3 D Strasbur geriaceae Strasburgeria robusta str1 T E O A C S25 12-Sep 2001 2 D Thymelacaceae Solmsia calophylla thy1 S E O A G S28 20-Mar 2002 3 D Thymelacaceae Wikstroemia indica thy2 S N T A C S1 5-Nov 2002 2 N Tiliaceae Triumfetta procumbens til1 P N O A Y S4 9-Sep 2001 2 D Verbenaceae Lantana camala ver1 P A T Z O S24 22-Mar 2002 3 D Verbenaceae Oxera inodora ver2 L E T Z W S17 27-Mar 2002 2 N Verbenaceae Oxera inodora ver2 L E T Z W S28 20-Mar 2002 2 N Verbenaceae Oxera morierei ver3 S E F Z W S23 7-Sep 2001 2 D Verbenaceae Stachytarpheta cayennensis ver4 P A C Z V S12 22-Mar 2002 2 D Verbenaceae Stachytarpheta cayennensis ver4 P A C Z V S15 24-Mar 2002 2 D Verbenaceae Stachytarpheta cayennensis ver4 P A C Z V S24 22-Mar 2002 2 D Violaceae Agatea pancheri vio1 L E P Z C S17 2-Nov 2002 2 D Violaceae Agatea schlechteri vio2 L E P Z C S28 30-Oct 2002 2 D Winteraceae Zygogynum baillonii wia1 T E O A P S26 8-Nov 2002 1 D Xyridaceae Xyris neocaledonica xyr1 P E O A Y S26 8-Nov 2002 1 D Zygophyllaceae Tribulus cistoides zyg1 A N O A Y S27 28-Aug 2001 2 D Total November 2004] KATO AND KAWAKITAÐPOLLINATION SYSTEMS IN NEW CALEDONIA 1821

TABLE 2. Extended continued.

Number of observed visitors Hymenoptera Lepidoptera Estimated thrips neuropterans beetle honey bee leafcutter bee small bee wasp ant dipterans hawk moth gracillariid micropterigid other moths butter¯y bird bat total pollinator 8 8 beetle 80 80 thrips 76 76 beetle 4 4 honey bee 3 3 honey bee 213 116honey bee 2 2 honey bee 3 3 honey bee 5 5 honey bee 2 2 honey bee 3 126 bird 8 8 honey bee 5 5 bird 15 15 honey bee 2 2 honey bee

21 21 honey bee 4 4 honey bee 2 5 7 moth 3 3 honey bee 14 14 honey bee/wind 3 3 honey bee/wind 60 2264 beetle 4 14 10 miscellaneous 3 3 honey bee 3 3 bird 77bird 3 1 4 honey bee 5 5 honey bee 2 2 honey bee 21 3 small bee 8 8 honey bee 6 6 honey bee 31 29 8 23 miscellaneous 9 9 honey bee 1 1 bat 1 1 hawk moth 2 2 hawk moth 8 8 moth 1 21 3 honey bee 5 3 8 moth 33moth 9 9 honey bee 7 7 honey bee 24 24 honey bee 2 33 5 miscellaneous 5 4 9 honey bee 2 2 ¯y 12 8 2 22 honey bee 4 8 4 16 honey bee 2 7 9 small bee 66bird 2 2 2 beetle 2 moth 5 5 honey bee 1 1 2 hawk moth 4 4 hawk moth 3 3 hawk moth 1 1 bird 9 2 11 honey bee 5 2 7 honey bee 34 6 1 41 honey bee 12 1 13 honey bee 5 5 honey bee 5 5 micropterigid 1 1 ¯y 2 1 2 honey bee 80 5 205 495 14 32 10 6 28 18 15 5 51 6 64 4 1038 1822 AMERICAN JOURNAL OF BOTANY [Vol. 91

idae), which used their slender bills to imbibe nectar from tubular ¯owers (Figs. 22±26).

Flower visitor assemblages on each plant speciesÐThe ¯ower visitor assemblages varied greatly among plant species. To explain this variance, we used a principal components anal- ysis. Flower visitors were classi®ed into 16 groups: thrips, Neuroptera, beetle, leafcutter bee, small bee, honey bee, wasp, ant, Diptera, hawk moth, gracillariid moth, micropterigid moth, other moths, butter¯y, bird, and bat. The percentages of these 16 groups found on each plant species were de®ned as the ¯ower visitor spectrum of each plant species. The ¯ower visitor spectra for 77 observations (71 plant spe- cies) were used in the principal component analysis. Eigen- vectors of ®rst, second, and third principal components for each insect group are shown in Fig. 27. The major trend in- volved the alternation of dominant insect groups between [Apis ϩ small bee ϩ butter¯y] and [pyralid moth ϩ Neurop- tera ϩ beetle ϩ Diptera ϩ others]. Variance in the ®rst prin- cipal component, PC1, contributed to 12.1% of the total var- iance. The second factor corresponded to the dominance of [leafcutter bee ϩ wasp] over [bird ϩ hawk moth ϩ thrips] (PC2, 9.9%). The third factor was primarily related to the al- ternation between [bird ϩ beetle] and [pyralid moth] (PC3, 9.0%). The cumulative percentages of variance of the ®rst three principal components were 31.1%, suggesting that ad- ditional factors also contributed to the total variance. Scatterplots of the loadings on PC1 and PC2 (Fig. 28) show that ¯owers with diverse shapes were used by honey bees, but that apetalous and spherical ¯owers were not visited by honey bees. Cup-shaped ¯owers had negative loadings on PC1, Fig. 27. Result of principal components analysis of the ¯ower visitor whereas apetalous ¯owers had positive loadings on PC1. spectra of 77 observations of 71 plant species. Eigenvectors of the ®rst (PC1) Loadings of tubular ¯owers were negative or close to zero on and the second (PC2) principal components calculated for each visitor group PC2, suggesting that tubular ¯owers had a tendency to be vis- are shown. Highest contribution ratios on PC1 and PC2 were detected in ited by birds and moths. The fact that various shapes of ¯ow- honey bees and wasps, respectively. ers had negative loadings on PC1 suggests that honey bees used diverse types of ¯owers as ¯oral hosts. bees. Native bees were observed only on 11 plant species: Cluster analysisÐThe ¯ower visitor spectra were subjected Agatea pancheri, Hibbertia lucens, Lomandra insularis, Mel- to cluster analysis. The dendrogram derived from the cluster ochia odorata (Fig. 3), Ranunculus sp., Rauvol®a semper¯o- analysis using Ward's minimum variance method is shown in rens var. semper¯orens, Scaevola balansae, Stachytarpheta Fig. 29. At 5% of the objective function, 77 spectra were di- cayennensis, Stenocarpus phyllodineus, Guioa glauca var. vul- vided into 10 clusters. garis (Fig. 2), Storthocalyx pancheri (Fig. 4), and Tetracera Cluster 1 (C1) was composed of 10 plant species that were billardieri. A scoliid wasp was observed on a ¯ower of Neo- visited by a few groups, including honey bees, small bees, and/ guillauminia cleopatra (Fig. 10). or birds. A total of 205 visits by beetles was recorded, and the most C2 was composed of three plant species (Loxodiscus cori- abundant family was the Staphylinidae (38% of individuals), aceus [Sapindaceae], Avicenia marina var. resinifera [Avicen- followed by the Helodidae (29%), Chrysomelidae (24%), Oed- iaceae], Alphitonia neo-caledonica [Rhamnaceae]), and was emeridae (4%), Curculionidae (3%), and Nitidulidae (1%). characterized by the predominance of ¯ies. A total of 95 visits by Lepidoptera was recorded (Figs. 13± C3 was composed of one plant species (Zygogynum bail- 21), and the most abundant family was the Pyralidae (38% of lonii), which was visited only by a micropterigid moth species, individuals), followed by the Sphingidae (19%), Gracillariidae Sabatinca sp. (16%), Noctuidae (10%), Geometridae (3%), and Micropteri- C4 was composed of one plant species (Hedycarya engler- gidae (5%). iana), which was visited only by thrips. We recorded 64 visits by birds on 17 plant species (Albizia C5 included Phyllanthus aeneus and Glochidion caledoni- guillainii, Archidendropsis paivana subsp. balansae, Deplan- cum (Euphorbiaceae), which were visited only by gracillariid chea speciosa, Dubouzetia caudiculata, Geissois magni®ca, moths (Epicephala subsp.) at night. Geissois pruinosa, Grevillea gillivayi, Melaleuca quiquener- C6 was composed of two species, Cerbesa manghas (Apo- via, Montrouziera sphaeroidea, Oxera morierei, Serianthes cynaceae) and Oxera morierei (Verbenaceae), which were vis- petitiana, Serianthus sachetae, Strasburgeria robusta, Syzy- ited only by a long-tongued crepuscular hawk moth, Gnath- gium acre). Observed birds were two honeyeater species, Lich- othlibus erotus (Sphingidae), in the evening. mera incana incana and Guadalcanaria undulata (Meliphag- C7 was composed of four plant species (Alstonia, plumosa November 2004] KATO AND KAWAKITAÐPOLLINATION SYSTEMS IN NEW CALEDONIA 1823

Fig. 28. Scatterplots obtained by principal component analysis of the ¯ower visitor spectra of 77 observations of 71 plant species. The loadings of the second principal component (PC2) are plotted against those of the ®rst principal component (PC1). Plots refer to observations categorized by ¯ower shape. Eigenvectors of the axes are shown in Fig. 27. The fact that various shapes of ¯owers had negative loadings on PC1 suggests that honey bees visited diverse types of ¯owers. var. communis [Apocynaceae], Dracophyllum ramosum [Epa- persed by wind. We therefore assumed that this species was cridaceae], Morinda sp. [Rubiaceae], Nepenthes vieillardii anemophilous. [Nepenthaceae]), and was characterized by the predominance Among the 95 native plant species whose pollination sys- of pyralid, geometrid, and noctuid moths. tems were determined, the most dominant system was melit- C8 was composed of six plant species and was characterized tophily (46.3%), followed by phalaenophily (20.0%), ornitho- by the predominance of beetles. For example, ¯owers of He- phily (11.6%), cantharophily (8.4%), myophily (3.2%), chi- dycarya cupulata (Monimiaceae) were visited only by staph- ropterophily (3.2%), and anemophily (3.2%). Figure 30 com- ylinid beetles. This clade included two plant species that were pares the frequency distributions of pollination systems visited by many inactive beetles but that were considered to observed in various ecosystems in different biogeographical be pollinated by actively ¯ying moths: Grevillea exul subsp. regions. exul (Proteaceae) and Exocarpus neo-caledonicus (Santala- From these comparisons, we draw the following generaliza- ceae). tions: (1) melittophily is generally the most dominant polli- C9 was composed of seven species (Montrouziera sphae- nation system, except in New Zealand and the canopies at roidea [Guttiferae], Deplanchea speciosa [Bignoniaceae], Sy- Kakachi. (2) Melittophily by long-tongued bees is lacking in zygium acre [Myrtaceae], Geissois pruinosa [Cunoniaceae], the canopies and on islands that have been isolated since the Albizia guillainii [Mimosaceae], Strasburgeria robusta [Stras- break-up of Gondwanaland (New Caledonia and New Zea- burgeriaceae], Grevillea gillivayi [Proteaceae]), all of which land). (3) Ornithophily is observed only in tropical ecosys- were visited only by birds. tems, and is more common in Gondwanaland and the Neo- C10 was composed of 36 plant species of various families, tropics than in Southeast Asia. (4) Myophily is dominant in and was characterized by the dominance of honey bees. temperate ecosystems. (5) Chiropterophily is absent from tem- perate ecosystems. Community-level comparison of pollination systemsÐ The frequency distribution of pollination systems in New Based on the results of the analyses, the behavior of the ¯ower Caledonia resembles that of tropical rain forests in Lambir, but visitors, and pollen attachment to their bodies, we determined differs in the relative prevalence of phalaenophily and in the the pollination system of each plant species (Table 2). Al- absence of melittophily by long-tongued bees. though we did not directly observe bats visiting ¯owers, bats were observed ¯ying towards three species of trees: Barring- DISCUSSION tonia asiatica, Fagraea berteroana, and Crossostylis grandi- ¯ora. The ¯owers of these species produced strong fragrance It is of serious concern that the most dominant ¯ower vis- at night, and the following morning, many damaged ¯owers itors in New Caledonia were the introduced honey bees. The were found at the base of the trees. Based on this circumstan- bee fauna of New Caledonia was originally much poorer than tial evidence, these plants were inferred to be bat-pollinated. that of Australia, being composed of four colletid, three hal- We did not observe insects visiting ¯owers of Amborella tri- ictid, and three megachilid genera, and the total number of bee chopoda (Fig. 12), but found that the pollen was easily dis- species is estimated to be only 28 (Donovan, 1983). The low 1824 AMERICAN JOURNAL OF BOTANY [Vol. 91

Fig. 29. Flower visitor spectra (sorted by visitor group) of 77 observations of 71 plant species (left) and dendrogram (right) derived from cluster analysis on the ¯ower visitor spectra. Plant species are grouped into 10 clusters at semi-partial r2 ϭ 0.02. diversity of the bee fauna in New Caledonia and the small were by halictid and megachilid bees, respectively. These data sizes of the native bees suggest that all the native bees colo- suggest that native bees are now endangered, and that original nized New Caledonia mainly from Australia over the sea after plant-pollinator interactions have been altered. A recent study the break-up of Gondwanaland (Michener, 1965, 1979). In on reproductive traits of rain-forest trees in New Caledonia contrast with the immigration of these bees in the Tertiary based on herbarium specimens (Carpenter et al., 2003) esti- (Michener, 1979; Donovan, 1983), Apis mellifera was quite mated that most plant species are pollinated by small insects, recently introduced after 1950s (Crane, 1990) and became ex- but not including bees. The small ¯owers of these plant species tremely abundant thereafter. Native bees must have been abun- usually produce nectar and/or pollen, which are easily utilized dant and played an important role in pollination before the by small insects such as beetles, ¯ies, and bees. However, the immigration of honey bees. We recorded 544 bee visits to original pollination systems of the ¯owers that are now visited ¯owers, of which 498 were by honey bees, and 32 and 14 exclusively by honey bees are hypothesized to have been mel- November 2004] KATO AND KAWAKITAÐPOLLINATION SYSTEMS IN NEW CALEDONIA 1825

Fig. 30. Community-level comparison of pollination systems of plants among various climatic zones (temperate, subtropical, and tropical) and among different geographic regions (Oceania, Asia, and Central America). See Materials and Methods for original references. ittophilous with native bees, because anthophilous ¯ies and and constituted a distinct pollination system. In addition to the beetles are uncommon in the pervasively xeric habitats of New tubular ¯owers that are usually visited by pyralid, geometrid, Caledonia, and because bees are preadapted in xeric habitats and noctuid moths, some nontubular ¯owers such as Nepen- (Michener, 1979). thes (Nepenthaceae) and Exocarpus (Santalaceae) were also This hypothesis is supported by a similar case observed in visited by moths searching for nectar. In Sumatra, Nepenthes the Ogasawara Islands of Japan (Kato, 1992; Kato et al., gracilis was observed to be pollinated by pyralid moths (Kato, 1999). The Ogasawara Islands are oceanic, and the original 1993), and a similar pollination system was observed in N. bee fauna was composed of only 10 native (nine endemic) vieillardii. solitary species. On islands where introduced honey bees have Moth-pollinated ¯owers included unique ¯owers that were become established, the ¯oral resources of most plant species visited, actively pollinated, and parasitized only by minute, are utilized exclusively by honey bees, and the native bees are host-speci®c gracillariid moths (Kato et al., 2003; Kawakita now almost extinct or endangered. However, on islands that and Kato, 2004). These ¯owers belong to Glochidion subsp. have not been invaded by honey bees, the same plant species and Phyllanthus (Gomphidium) subsp. (Euphorbiaceae); the are visited and pollinated by native bees. Similar changes in latter has undergone an unusual diversi®cation of up to 111 pollinator fauna caused by the introduction of honey bees have species (Schmid, 1991). The diversi®cation of Phyllanthus been observed in New Zealand (Thomson, 1927; Heine, 1938; contributes to the prevalence of moth-pollination in New Ca- Craig et al., 2000) and Tasmania (Goulson et al., 2003). It is ledonia. thought, therefore, that the current predominance of honey Pollination by micropterigid moths has been reported for bees in New Caledonia will have serious effects on plant-pol- Zygogynum subsp. (Thien et al., 1985; Pellmyr, 1990), and was linator interactions, e.g., drastic decreases in populations of con®rmed in this study in a moss forest at Mt. Koghi. Because native bees, changes in patterns of gene ¯ow among plants, Zygogynum ¯owers do not secrete nectar, nectar-seeking in- and increased reproductive ®tness of invasive exotic weeds. In sects did not visit them. Micropterigid moths were active dur- contrast with these cases on oceanic islands, introduced honey ing the daytime, and pollen was attached to their bodies around bees have less impact on population dynamics of native bees the mouthparts. in Panama (Roubik and Wolda, 2001). However, Africanized Although nectar-feeding birds are not diverse in New Ca- honey bees are potential competitors of native bees (Frankie ledonia, ornithophilous plants are common. Strasburgeria,a et al., 1997), and sometimes alter the genetic structure of some monotypic genus of the endemic Strasburgeriaceae family, canopy trees while they act as important pollinators in de- bears large nectariferous ¯owers, which were frequently vis- graded Neotropical forests (Dick, 2002). ited by honeyeaters. The most dominant birds on ¯owers were The relative dominance of phalaenophily may be closely meliphagid honeyeaters, which perch on branches and use related to the low diversity of native bees. Because moth-pol- their slender bills to collect nectar from tubular ¯owers. In linated ¯owers open up and secrete nectar in the evening and Australia, about 250 plant species in the Myrtaceae, Protea- at night when bees are not active, these ¯owers are used nei- ceae, Loranthaceae, and Epacridaceae are visited and pollinat- ther by native bees nor by honey bees. Extremely elongated ed by more than 100 species of birds (Armstrong, 1979; Ford tubular ¯owers were visited only by crepuscular hawkmoths et al., 1979; Williams and Adam, 1994). Irrespective of dif- 1826 AMERICAN JOURNAL OF BOTANY [Vol. 91 ferences in species diversity among ¯ower-visiting birds, a mid-elevation wet evergreen forest in Western Ghats, India. American plant-bird interactions (dominance of honeyeaters, ¯oral ad- Journal of Botany 90: 650±657. aptation to ornithophily, and nectar-feeding behavior of birds) DICK, C. W. 2002. Genetic rescue of remnant tropical trees by an alien pol- linator. Proceedings of the Royal Society Biological Sciences, Series B are similar between Australia and New Caledonia. Pollination 268: 2391±2396. disruption by the introduced honey bees observed in Austra- DONOVAN, B. J. 1983. Comparative biogeography of native Apoidea of New lian bird-pollinated plants (Vaughton, 1996) and in plants cul- Zealand and New Caledonia. GeoJournal 7: 511±516. tivated in orchards in New Zealand (Stewart and Craig, 1989) DUPONT, Y. L., D. M. HANSEN,A.VALIDO, AND J. M. OLESEN. 2004. Impact suggests that pollen removal by honey bees may reduce pol- of introuduced honey bees on native pollination interactions of the en- lination success in ornithophilous plants also in New Caledon- demic Echium wildpretti (Boraginaceae) on Tenerife, Canary Islands. Bi- ia. ological Conservation 118: 301±311. FEIL, J. P. 1992. Reproductive ecology of dioecious Siparuna (Monimiaceae) Pollination systems in New Caledonia have attracted world- in Ecuador: a case of gall midge pollination. Botanical Journal of the wide interest from many botanists because archaic plants are Linnean Society 110: 171±203. thought to have maintained their archaic plant-pollinator in- FORD, H. A., D. C. PATON, AND N. FORDE. 1979. Birds as pollinators of teractions since the early radiation of basal angiosperms. Some Australian plants. New Zealand Journal of Botany 17: 509±519. examples include the interactions observed between Zygogyn- FRANKIE, G. W., S. B. VINSON,M.A.RIZZARDI,T.L.GRISWOLD, S. O'KEEF, um (Winteraceae) and micropterigid moths, and between He- AND R. R. SNELLING. 1997. Diversity and abundance of bees visiting a dycarya (Monimiaceae) and beetles/thrips. Pollination by mass ¯owering tree species in distrubed seasonal dry forest, Costa Rica. Journal of the Kansas Entomological Society 70: 281±296. thrips has also been observed in Australian plants of the Mon- GOULSON, D., J. C. STAUT, AND A. R. KELLS. 2002. Do exotic bumblebees imiaceae, in which male and female ¯owers serve as brood and honeybees compete with native ¯ower-visiting insects in Tasmania. sites for larvae of the pollinating thrips (Williams et al., 2001). Journal of Insect Conservation 6: 179±189. In addition, ¯owers of the Neotropical Siparuna subsp. (Mon- HEINE, E. M. 1938. Observations on the pollination of New Zealand ¯ow- imiaceae) are reported to be pollinated by cecidomyiid midges, ering plants. Transactions of the New Zealand Institute 67: 133±148. whose larvae grow in male ¯ower tissue (Feil, 1992). It is JAFFREÂ , T., P. BROOKS,J.LEE, AND R. D. REEVES. 1976. Sebertia acuminata, interesting that the ¯oral rewards of these archaic plants to the a hyperaccumulator of nickel from New Caledonia. Science 193: 579± 580. pollinators are not nectar but pollen (in Zygogynum) or ¯oral JAFFREÂ , T., P. MORAT, J.-M. VEILLON,F.RIGAULT, AND G. DAGOSTINI. 2001. tissue, used as brood sites by pollinator larvae (in Hedycarya Composition and characterisation of the native ¯ora of New Caledonia. and Siparuna). The archaic plant Amborella trichopoda was Institute de recherche pour le deÂveloppement, NoumeÂa, New Caledonia. reported to have been visited by various insects (Thien et al., KATO, M. 1992. Endangered bee fauna and its ¯oral hosts in the Ogasawara 2003), whereas we considered it to be anemophilous. How- Islands. Japanese Journal of Entomology 60: 487±494. ever, the high rate of galled fruits on this species suggests that KATO, M. 1993. Floral biology of Nepenthes gracilis (Nepenthaceae) in Su- the cecidomyiid midge might be an alternative agent for pol- matra. American Journal of Botany 80: 924±927. KATO, M. 2000. Anthophilous insect community and plant-pollinator inter- lination. actions on Amami Islands in Ryukyu Archipelago, Japan. Contributions In conclusion, community-level, plant-pollinator mutualism from Biological Laboratory, Kyoto University 29: 157±252, pl. 2±3. in New Caledonia was characterized by the dominance of mel- KATO, M., M. MATSUMOTO, AND T. K ATO. 1993. Flowering phenology and ittophily, ornithophily, and phalaenophily. Although some ar- anthophilous insect community in the cool-temperate subalpine forests chaic plants have maintained their archaic pollination systems, and meadows at Mt. Kushigata in the central part of Japan. Contributions most plants have adopted pollination by honeyeaters, nocturnal from Biological Laboratory, Kyoto University 28: 119±172. moths, and diurnal nectar-seeking insects such as bees. Among KATO, M., S. SHIBATA,T.YASUI, AND H. NAGAMASU. 1999. Impact of in- troduced honeybees, Apis mellifera, upon native bee communities in the these three pollination systems, the establishment of honey Bonin (Ogasawara) Islands. Researches on Population Ecology 41: 217± bees would have in¯uenced melittophily most drastically. Dur- 228. ing our surveys, feral honey bees were commonly found in all KATO, M., A. TAKIMURA, AND A. KAWAKITA. 2003. An obligate pollination vegetation types, at every altitude, and in every locality. Our mutualism and reciprocal diversi®cation in the tree genus Glochidion study suggests that apiculture at least in and around natural (Euphorbiaceae). Proceeding of National Academy of Science 100: vegetation should be reconsidered in order to conserve native 5264±5267. plant-pollinator interactions and the invaluable endemic ¯ora KAWAKITA, A., AND M. KATO. 2004. Evolution of obligate pollination mu- tualism in New Caledonian Phyllanthus (Euphorbiaceae). American of New Caledonia. Journal of Botany 91: 410±415. 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