Pollination and reproduction of Psychotria homalosperma,an endangered distylous tree endemic to the oceanic Bonin (Ogasawara) Islands,Japan

Distyly is usually rare or not observed in species thriving on oceanic islands. The rarity of this breeding system is probably because of the difficulty of colonization for distylous plants and the paucity of pollinators on oceanic islands. However, the endemic and endangered tree Psychotria homalosperma has maintained its distylous nature in the oceanic Bonin Islands, Japan. To understand how the distylous breeding system of P. homalosperma has been maintained on these islands and to characterize the reproduction systems, we studied the pollination and reproductive biology of this species. Specifically, we observed current flower visitors and estimated their effects on plant reproduction. We also examined the floral traits and floral volatiles of P. homalosperma to infer its original pollinators, because plant–pollinator relationships in the Bonin Islands have recently been disrupted by anthropological activities. Finally, we examined the fruit set and pollen tube growth in the stigmas under hand and open pollination. Although original pollinators were presumed to be moths with long proboscises, the introduced honeybee, Apis mellifera, was the most common flower visitor. The honeybee carried pollen grains only unidirectionally, from the short‐ to long‐styled morphs, because it could not reach the hidden stigmas of the short‐styled flowers, and long‐styled flowers set fruits 1.7–38 times more than short‐styled ones. This case study indicates that the instability of pollinator fauna can cause distylous species to be rare on oceanic islands.     

Distyly and incompatibility in Psychotria homalosperma (Rubiaceae), an endemic plant of the oceanic Bonin (Ogasawara) Islands

Distyly rarely occurs on oceanic islands. Indeed, this form of polymorphism is absent on the Hawaiian Islands and in New Zealand. However, Psychotria homalosperma (Rubiaceae), which is endemic to the oceanic Bonin Islands of Japan, was presumed to maintain a distylous breeding system and floral morphology. We investigated the floral and reproductive characteristics of this species and examined incompatibility in self- and intramorph pollination. Psychotria homalosperma is morphologically and functionally distylous, based on findings with the examined populations, but its stigma and anther heights are not exactly reciprocal between the two morphs. This is the second example of distyly among the flora from the Bonin Islands, the other being the endemic P. boninensis. Both of these distylous species contrast with the Hawaiian Psychotria species, which have already become dioecious. The flowers of the long (L)-styled (pin) morph of the Bonin Islands plants are completely self- and intramorph incompatible, while the flowers of the short (S)-styled (thrum) morphs are partially intramorph compatible. The S-styled morph was more abundant in the examined populations from three islands of the archipelago, probably due to the existence of partial S–S intramorph compatibility.     

Origin and evolution of endemic plants of the Bonin (Ogasawara) Islands

The Bonin Islands are typical oceanic islands, located at the western part of the North Pacific Ocean and approximately 1,000 km south of mainland Japan. This archipelago consists of about 20 small islands. Although floristic diversity is low due to the small area and limited environmental diversity, the Bonin Islands harbor unique endemic flora as in other well-known oceanic islands. This paper presents a brief summary of the results obtained from recent studies on the endemic flora of the Bonin Islands. The results are reviewed in relation to the four stages of the evolution of endemic flora in the oceanic islands; migration, establishment, enlargement and diversification. The ancestors of the flora originated mostly from tropical and subtropical Southeast Asia or mainland Japan by rare events of long distance dispersal. The proportion of bird-dispersed species is relatively high as for other oceanic islands. Genetic data sets obtained from allozyme variation in some endemic species suggest that migration occurred several million years ago and genetic diversity is correlated with current population size. At the time of establishment, self-compatible plants are expected to have an advantage. However, the percentage of dioecious plants is relatively high. This is partly due to evolutionary changes from hermaphroditic ancestors to dioecy which occurred in two genera in the Bonin Islands. In addition, there are some examples of evolutionary changes from herbaceous ancestors to woody endemics. Adaptive radiation is found in some genera, although the number of congeneric endemic species is less than five. Studies of allozyme variation inPittosporum, Symplocos andCrepidiastrum showed that genetic identity is generally very high between congeneric species in spite of their distinct morphologies. This result suggests that divergence of these species occurred rather recently and distinct morphological differences are based on a limited number of genetic changes.     

Allozyme diversity and the evolution ofSymplocos (Symplocaceae) on the Bonin (Ogasawara) Islands

To study the origin and speciation of plants in oceanic islands, electrophoretic analyses have been done on three endemic species ofSymplocos in the Bonin Islands as well as on three other species;S. kuroki, S. nakaharae andS. tanakae which are considered to be closely related to the Bonin endemics. There occur three species:S. kawakamii, S. pergracilis andS. boninensis in Bonin. The genusSymplocos is one which is considered to be diversified in the Bonin Islands. Seven enzyme systems presumed to be encoded by 18 loci were examined. The genetic diversity was low in the island species, as reported in some oceanic island plants of Hawaii and the Bonin Islands. The three endemics share high genetic identities and they clustered together in the tree drawn by the UPGMA method, suggesting that they are a monophyletic group, that is, they result from a single introduction.     

Bird and insect pollinators differ in specialization and potential pollination services along disturbance and resource gradients

Combined studies of the communities and interaction networks of bird and insect pollinators are rare, especially along environmental gradients. Here, we determined how disturbance by fire and variation in sugar resources shape pollinator communities and interactions between plants and their pollinating insects and birds. We recorded insect and bird visits to 21 Protea species across 21 study sites and for 2 years in Fynbos ecosystems in the Western Cape, South Africa. We recorded morphological traits of all pollinator species (41 insect and nine bird species). For each site, we obtained estimates of the time since the last fire (range: 2–25 calendar years) and the Protea nectar sugar amount per hectare (range: 74–62 000 g/ha). We tested how post-fire age and sugar amount influence the total interaction frequency, species richness and functional diversity of pollinator communities, as well as pollinator specialization (the effective number of plant partners) and potential pollination services (pollination service index) of insects and birds. We found little variation in the total interaction frequency, species richness and functional diversity of insect and bird pollinator communities, but insect species richness increased with post-fire age. Pollinator specialization and potential pollination services of insects and birds varied differently along the environmental gradients. Bird pollinators visited fewer Protea species at sites with high sugar amount, while there was no such trend for insects. Potential pollination services of insect pollinators to Protea species decreased with increasing post-fire age and resource amounts, whereas potential pollination services of birds remained constant along the environmental gradients. Despite little changes in pollinator communities, our analyses reveal that insect and bird pollinators differ in their specialization on Protea species and show distinct responses to disturbance and resource gradients. Our comparative study of bird and insect pollinators demonstrates that birds may be able to provide more stable pollination services than insects.     

Specific features of pollination in the Manchurian birthwort, <Emphasis Type="Italic">Aristolochia manshuriensis</Emphasis>

An analysis of pollination system in Aristolochia manshuriensis has shown that flower structure in this species is strictly adapted to cross-pollination, but the possibility of an autogamous or geitonogamous type of self-pollination with the involvement of insects is not excluded. The flowers of A. manshuriensis are most frequently visited by flies of the family Anthomyiidae, which markedly contribute to their pollination. Males account for 65% of pollinator insects collected from the flowers.     

The birds and the seeds: opportunistic avian nectarivores enhance reproduction in an endemic montane aloe

Opportunistic bird pollination has become more evident in studies that confirm distinct differences in floral adaptations that attract opportunistic, rather than specialist, bird pollinators. Pollination syndrome studies investigating the effectiveness of different pollinator guilds on reproduction seldom do so by measuring seed viability. We studied pollination in Aloe peglerae, a high altitude endemic succulent of the Magaliesberg mountain range, previously thought to be largely sunbird (specialist) pollinated. Using field observation and pollinator exclusion treatments, i.e. (i) open to all visitors, (ii) bird excluded, and (iii) all visitors excluded, we established that birds contributed significantly more to fruit (2.3–5.6 times) and seed (1.3–1.4 times) set than insect or self-pollination, respectively. Overall, pollination by opportunistic avian nectarivores amplified seed production per aloe ~7 and 10 times compared to insects and self-pollination, respectively. One of three opportunistic nectarivores, the Cape Rock-Thrush (Monticola rupestris), played a significant role in pollination, contributing ~60 % of all probes at inflorescences. The difference in reproductive output between insect visited and visitor excluded flowers was not significant and suggests possible self-pollination in A. peglerae which is particularly unusual in Aloe species. Breeding system experiments would help clarify this. In assessing the effectiveness of pollinator guild on seed viability, we found no differences in percentage seed viability, seed germination or seedling emergence between exclusion treatments. Seed viability and germination were low and variable; however, ~19 % seedling emergence was observed across the treatments. Practically, the net effect of bird pollination may result in 8–12 times more potential seedlings compared to insect and self-pollination respectively. These findings highlight the importance of pollination by opportunistic avian nectarivores in Aloe.     

Reproductive ecology of <Emphasis Type="Italic">Agave colorata</Emphasis>: the importance of nectar-feeding bats and the germination consequences of self-pollination

Agave colorata is a paniculate agave distributed along the migratory route of the nectar-feeding bat Leptonycteris yerbabuenae. In this paper, we evaluate the importance of nectar-feeding bats in the reproduction of A. colorata in a population in Sonora, Mexico, and describe the germination consequences of self-pollination. We estimated abundance using five plots and set pollination treatments to evaluate the importance of bats. We recorded 14.8?±?6.8 plants/400 m², with a bimodal size distribution. Flowers are protandrous and visited mainly (>?20 visits/plant/30 min) by L. yerbabuenae. Pollination exclusion experiments showed that flowers excluded from diurnal visitors had maximum fruit set values (0.49?±?0.42), while the autonomous self-pollination treatment had the lowest value (0.03?±?0.06). Similarly, the greatest number of viable seeds per fruit was recorded in the diurnal exclusion treatment, while the greatest number of empty seeds was observed in the self-pollination treatment. Fruit set values among untreated plants varied from 32 to 54%, with a mean value of 41.8%. Seeds derived from self-pollination had a narrower window of opportunity for germination compared to seeds derived from nocturnal pollination. Self-pollinated seeds had lower germination, rate of germination or lag time in response to light, osmotic potential and heat shock treatments, compared to other pollination treatments, revealing an inbreeding cost. Overall, our results show that L. yerbabuenae is the likely major pollinator of the studied A. colorata population. However, under pollinator limitation A. colorata may produce seeds by autonomous self-pollination, at a cost expressed as lower germination.     

Bird pollination syndrome is the plant's adaptation to ornithophily,but nectarivorous birds are not so selective

Many tropical plants are pollinated by birds and several bird phylogenetical lineages have specialised to a nectar diet. The long-assumed, intimate ecological and evolutionary relationship between ornithophilous plants and phenotypically specialised nectarivorous birds has nevertheless been questioned in recent decades, where such plant–pollinator interactions have been shown to be highly generalised. In our study, we analysed two extensive interaction datasets: bird–flower and insect–flower interactions, both collected on Mt Cameroon, west-central Africa. We tested if: 1) insects and birds interact with distinct groups of plants; 2) plants with a typical set of ornithophilous floral traits (i.e. bird pollination syndrome) interact mainly with birds; 3) birds favour plants with bird pollination syndrome and; 4) if and how the individual floral traits and plant level nectar production predict bird visitation. Bird-visited plants were typically also visited by insects, while approximately half of the plants were visited by insects only. We confirmed the validity of the bird pollination syndrome hypothesis, as plants with bird-pollination syndrome traits were visited by birds at a higher rate and mostly hosted a lower frequency of visiting insects. However, these ornithophilous plants were not more attractive than the other plants for nectar-feeding birds. Nectar production per plant individual was a better predictor of bird visitation than any other floral trait traditionally related to the bird pollination syndrome. Our study thus demonstrated the highly asymmetrical relationship between ornithophilous plants and nectarivorous birds.     

Issue Information

A Orobanche boninsimae and its visitors, Japanese white-eyes (Zosterops japonicus). Photo by Akihiro Nishimura at Chichijima Island, the Bonin Islands, Japan. Nishimura & Takayama (2023) “First record of potential bird pollination in the holoparasitic genus Orobanche L.” Plant Species Biology, 6–17 https://doi.org/10.1111/1442-1984.12389

     

Quantity and quality components of effectiveness in insular pollinator assemblages

Ecologically isolated habitats (e.g., oceanic islands) favor the appearance of small assemblages of pollinators, generally characterized by highly contrasted life modes (e.g., birds, lizards), and opportunistic nectar-feeding behavior. Different life modes should promote a low functional equivalence among pollinators, while opportunistic nectar feeding would lead to reduced and unpredictable pollination effectiveness (PE) compared to more specialized nectarivores. Dissecting the quantity (QNC) and quality (QLC) components of PE, we studied the opportunistic bird–lizard pollinator assemblage of Isoplexis canariensis from the Canary Islands to experimentally evaluate these potential characteristics. Birds and lizards showed different positions in the PE landscape, highlighting their low functional equivalence. Birds were more efficient than lizards due to higher visitation frequency (QNC). Adult lizards differed from juveniles in effecting a higher production of viable seeds (QLC). The disparate life modes of birds and lizards resulted in ample intra- and inter-specific PE variance. The main sources of PE variance were visitation frequency (both lizards and birds), number of flowers probed (lizards) and proportion of viable seeds resulting from a single visit (birds). The non-coincident locations of birds and lizards on the PE landscape indicate potential constraints for effectiveness. Variations in pollinator abundance can result in major effectiveness shifts only if QLC is relatively high, while changes in QLC would increase PE substantially only at high QNC. The low functional equivalence of impoverished, highly contrasted pollinator assemblages may be an early diagnostic signal for pollinator extinction potentially driving the collapse of mutualistic services.     

THE EVOLUTION OF INSECT-MEDIATED SELF-POLLINATION FROM AN OUTCROSSING SYSTEM IN CALYPTRIDIUM (PORTULACACEAE)

Calyptridium monospermum (Portulacaceae) comprises two biological races visited by different groups of insects. One race, pollinated by a bumblebee, Bombus vosnesenskii (Apidae), is outcrossing, while the other race is pollinated casually by a variety of other insects whose visits result in insect-mediated self-pollination and geitonogamy within the inflorescence. Insect-mediated selfing is also the mode of pollination in the closely related species, C. umbellatum. While all plants of both species are self-compatible, insect visitation is necessary for good seed set. Selfing populations of C. monospermum exhibit many floral adaptations for insect-mediated self-pollination which parallel those of the selfing C. umbellatum, while retaining vegetative characteristics typical of C. monospermum. These floral traits involve flower color and odor, style and stamen orientation, size of stigmatic surfaces, number of pollen grains produced, density of open flowers on inflorescences, and presence or absence of protogyny. Artifical pollination experiments show that these floral adaptations are effective in increasing the probability of insect-mediated self-pollination. Insect-mediated selfing in C. umbellatum and in some populations of C. monospermum is encouraged and probably made necessary by the inconstant pollinating behavior of the insects which visit these plants, as shown by the large percentage of non-Calyptridium pollen recovered from the bodies of insects captured while visiting these plants.     

Differences in endemic insect assemblages among vegetation types on a small island of the oceanic Ogasawara Islands

Natural vegetation is often replaced by invasive alien plants on isolated oceanic islands. To determine how invasive alien plants affect insect diversity, we compared flying insects captured using Malaise traps among different vegetation types on a small island (Nishijima; 0.49 km²) in the oceanic Ogasawara (Bonin) Islands in the north‐western Pacific. The numbers of individuals and species, and the species composition of pollinators (bees), predators (wasps) and wood borers (cerambycid, mordellid and elaterid beetles) were compared among three vegetation types: Casuarina equisetifolia (an invasive alien tree) forest, natural forest and natural grassland (forest edge), during two seasons (June and October–November 2005). In traps, 80.0, 66.7, 87.5, 85.7 and 100.0% of bee, wasp, cerambycid, mordellid and elaterid beetle species, respectively, were endemic to the Ogasawara Islands. Grassland had the highest wasp and bee species richness, whereas natural forest had the highest species richness of wood‐boring beetles. The C. equisetifolia forest had the poorest species richness for most insect groups (except mordellid beetles). More individuals of most insect groups (except bees) were captured in June than in October–November. More individual bees and wasps were captured in grassland than in forests, whereas more individual mordellid and elaterid beetles were captured in forests than in grassland. The number of cerambycid individuals did not differ among vegetation types. Redundancy analysis suggested that most insect species preferred natural forest or grassland to alien forest. Therefore, further invasion of natural grassland and forest by the alien tree C. equisetifolia may negatively affect the endemic insect fauna of Nishijima.     

Allozyme diversity and the evolution ofCrepidiastrum (Compositae) on the Bonin (Ogasawara) Islands

The genusCrepidiastrum is distributed in East Asia and includes 7 species. In the Bonin Islands, three species ofCrepidiastrum occur, and all of them are endemic to the islands. For detecting the origin and speciation of these endemic species, electrophoretic studies have been done in three endemic species of the Bonin Islands as well as in the remaining four species ofCrepidiastrum, andYoungia denticulata which is considered to be closely related toCrepidiastrum. A total of 386 individuals were sampled from 14 populations. As a result, 17 loci of 10 enzyme systems were resolved and gene frequencies for each population were calculated. The genetic variability was low in island species, as reported in some oceanic island plants. Four groups were recognized in the dendrogram generated by the UPGMA method. The Bonin endemics were clustered together, suggesting a monophyletic origin.C. ameristophyllum andC. linguaefolium were found to be genetically very similar, and this may suggest recent and rapid speciation within the islands.     

Breeding system of the subantarctic plant species Pringlea antiscorbutica R. Br. and search for potential insect pollinators in the Kerguelen Islands

The reproductive biology of Pringlea antiscorbutica R. Br. (Brassicaceae), an endemic species from the southern Indian Ocean islands, is investigated here. Controlled crosses were performed between plants grown in a common garden on the Kerguelen Islands. Searching for potential insect pollinators, we investigated the flying ability of all insects known from the Kerguelen Islands. We showed evidence for self-compatibility, low pollen limitation in the absence of a biotic pollen vector and slight selfing depression in P. antiscorbutica. The insects present on the islands are mostly wingless and are not likely to be efficient pollinators of this species. Since P. antiscorbutica shows morphological adaptations to insect pollination despite the absence of pollinators in its present range, we conclude that this species recently evolved from insect pollination to wind and/or autonomous pollination.     

Efficient avian pollination of Strelitzia reginae outside of South Africa

In its native South Africa, endemic birds pollinate the complex flowers of Strelitzia reginae (bird of paradise) through a highly complex method of pollination. The plant is cultivated worldwide in warm-temperated regions but systematic pollination of the ornithophilous species by local birds has not been reported, and, consequently, seed production is rare outside of South Africa. We found that a member of the New World warblers, Geothlypis trichas, efficiently carried out pollination of S. reginae in southern California, thereby supplementing its typical diet of insects with the energy-rich nectar of S. reginae. Only occasionally, seeds were found in plantings not visited by these birds. The pollinator service provided by the warbler increases seed production in an area outside of South Africa. This could lead to adaptive changes in the exotic species, advance species establishment and persistence and possibly promote invasive behavior in a non-native environment.     

Allozyme diversity ofPittosporum (Pittosporaceae) on the Bonin (Ogasawara) Islands

The genusPittosporum includes about 160 species. Four species ofPittosporum occur in the Bonin Islands, and all of these are endemic to the islands. Electrophoretic studies of the four endemic species,P. tobira, from the Japanese mainland, andP. lutchuense var.denudatum from the Ryukyu Islands, were used to determine the origin and speciation pattern of the endemic species. 259 individuals were sampled from ten populations. Twenty loci in nine enzyme systems were resolved and used to calculate the gene frequencies for each population. A low genetic diversity was observed in three of the Bonin Island species, as is reported for other oceanic island plants. The exception,P. boninense, has the largest population size and widest distribution. A dendrogram generated by the UPGMA method shows two clusters. One consists of only the Bonin endemics, suggesting a monophyletic origin for these species.     

Effectiveness of ants as pollinators of<Emphasis Type="Italic"> Lobularia maritima</Emphasis>: effects on main sequential fitness components of the host plant

The effectiveness of ants as pollinators of Lobularia maritima (Cruciferae) was experimentally analyzed by assessing (1) their quantitative importance at flowers; (2) their effect on host plant seed production; (3) their effect on the performance of host plant progeny, estimated as seed germination, seedling emergence, seedling survival to flowering, and (4) the overall effect of ants on a cumulative, more realistic measure of plant fitness related to the recruitment probability. Flowers of L. maritima were visited during the 2 years of study (1996 and 1997) by more than 50 pollinator species belonging to about 30 families of disparate taxonomic affiliation, notably ants and flies. There was significant seasonal variability in insect abundance and type. Ants, especially Camponotus micans (Formicidae), visited the flowers of L. maritima in summer, representing 81.2% of the visits during this season. This ant species acted as a pollinator of L. maritima, with flowers visited exclusively by ants producing significantly more seeds than flowers from which all pollinators were excluded, whereas flowers visited by only winged insects did not differ from self-pollination. Ant-pollinated flowers produced seeds with a germination rate comparable to the other treatments. Moreover, seedlings from these seeds emerged as fast, and survived at the same rate as controls. Consequently, both ants and winged insects had similar overall effects on host plant recruitment probability (0.6 and 0.7% of initial ovules produced flowering offspring, respectively), a result similar to that of open-pollinated flowers (1.0%). This study demonstrated that the overall effectiveness of the ant C. micans as a summer pollinator of L. maritima was as high as that of other winged insects, contributing not only to the seed production of this crucifer but also to the recruitment of new flowering offspring. Received: 17 February 1999 / Accepted: 26 August 1999     

A method for quantifying the gene flow that results from a single bumblebee visit using transgenic oilseed rape,Brassica napus L. cv. Westar

Genetically modified plants containing selectable markers offer a unique opportunity for pollination biologists to investigate some of the major, but intractable questions about paternity distributions and their causes. Here, a method is reported that uses transgenic plants to enable the quantification of the outcrossed fertilizations that result from a single pollinator visit. Gene flow mediated by worker bumblebees (Bombus terrestris) was studied among plants of oilseed rape (Brassica napus L. cv. Westar) where transgenic paternity in seeds of a non-transgenic plant was manifested as herbicide resistance. Overall, 91% of the resistant seeds resulted from the first four flowers that were visited after the bumblebee left the transgenic plant, and none was found beyond the 14th successively visited flower. The possibilities for developing the method to address various questions in pollination biology are discussed.     

Ecological and genetic differentiation in Persea boninensis (Lauraceae) endemic to the Bonin (Ogasawara) Islands

Persea boninensis (Lauraceae) is an endemic tree species distributed throughout the Bonin Islands. It grows in a wide range of environments from dry to mesic forests, and has multiple flowering peaks that may correspond to different habitats on Chichijima Island of the Bonin Islands. We predicted that P. boninensis is differentiated into two groups with different habitats on these islands. We examined and compared the flowering phenology, morphology, and genetics of populations of species growing in dry and mesic forests. We also performed preliminary artificial crossing experiments. Based on our results, P. boninensis on the Chichijima Islands can be clearly divided into two genetic groups with different habitats and flowering times. Although the flowering time difference could act as an effective pre‐zygotic isolation mechanism between the two groups, there was still a 1‐month overlap in flowering time. Furthermore, our artificial crossing experiments between the two groups resulted in plants that set seeds. Therefore, there was no evidence of reproductive isolation after fertilization. Differences in flowering time as well as in growth habitat will have to occur to maintain genetic differentiation between the two groups of P. boninensis.