Tamiji Inoue

Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest

Flowerings and flower visitors were observed continuously in alowland dipterocarp forest in Sarawak, Malaysia, for 53 mo in1992-1996. Flower visitors of 270 plant species were observed orcollected, and pollinators were assessed by observing body contact tostigmas and anthers. We recognized 12 categories of pollination systems.Among them, plants pollinated by social bees included the largest numberof species (32%) and were followed by beetle-pollinated species(20%). Pollination systems were significantly related with somefloral characters (flowering time of day, reward, and floral shape), butnot with floral color. Based on the relationships between pollinatorsand floral characters, we described pollination syndromes found in alowland dipterocarp forest. The dominance of social bees and beetlesamong pollinators is discussed in relation to the general floweringobserved in dipterocarp forests of West Malesia. In spite of high plantspecies diversity and consequent low population densities of lowlanddipterocarp forests, long-distance-specific pollinators were uncommoncompared with theNeotropics.

Seasonality and vertical structure of light-attracted insect communities in a dipterocarp forest in Sarawak

Nocturnal flying insects were collected monthly for 13 months using ultra violet light-traps set at various vertical levels in a weakly-seasonal, tropical lowland dipterocarp forest in Sarawak, Malaysia. Abundance, faunal composition, size distribution and guild structure of these samples were analyzed with respect to temperal and vertical distributions. The nocturnal flying insect community in the canopy level was highly dominated by fig wasps (84%) in individual number, and by scarabaeid beetles (28%) in weight. A principal component analysis on monthly catches detected non-random, seasonal trends of insect abundance. The first two principal trends were an alternation of wetter (September to January) and less wet seasons (February to August) and an alternation between the least wet (January to March) and the other seasons. Many insect groups were less abundant in the least wet season than the other seasons, whilst inverse patterns were found in Scarabaeidae and Tenebrionidae. Significantly positive and negative correlations between monthly catch and rainfall were detected only in ovule-feeders and in phloem-feeders, respectively. Delayed, significant negative correlations between monthly catch and 1–3 month preceding rainfall were more frequently detected in phytophages, phloem-feeders, seed-feeders, wood-borers and scavengers. The peak in abundance along vertical levels were found at the canopy level (35 m) for phloem-, ovule-, seed-, root-, fungal-feeders and nectar collectors, at an upper subcanopy level (25 m) for scavengers and aquatic predators, and at a middle subcanopy level (17 m) for ants. Catches at the emergent level (45 m) did not exceed those at the canopy level.

Aggressive foraging of social bees as a mechanism of floral resource partitioning in an Asian tropical rainforest

Abstract Interference competition by aggressive foraging often explains resource partitioning, but mechanisms contributing to partitioning have rarely been studied in Asian social bee guilds. Foraging of social bees at canopy flowers of Santiria laevigata (Burseraceae) and honey-water feeders was studied in a lowland mixed-dipterocarp forest in Sarawak, Malaysia. Four stingless bee species (Apidae, Meliponinae), Trigona canifrons, T.␣fimbriata, T. apicalis and T. melina, aggressively defended flower patches and feeders. At the flowers, T.␣canifrons excluded other bees only in the morning when nectar flow peaked. At the feeders, the aggression resulted in asymmetric interference competition, which produced a dominance hierarchy among seven social bee species. Interspecific partitioning of the feeders was detected in time and height but not quality. Only time of the first arrival after feeder presentation was negatively correlated with the dominance hierarchy: more aggressive species arrived at the feeders later than less aggressive species. This result suggests that a trade-off between searching ability and defensive ability at flower patches gives rise to resource partitioning in the social bee guild.

Beetle pollination of Shorea parvifolia (section Mutica, Dipterocarpaceae) in a general flowering period in Sarawak, Malaysia

Pollination ecology of an emergent tree species, Shorea (section Mutica) parvifolia (Dipterocarpaceae), was studied using the canopy observation system in a lowland dipterocarp forest in Sarawak, Malaysia, during a general flowering period in 1996. Although the species has been reported to be pollinated by thrips in Peninsular Malaysia, our observations of flower visitors and pollination experiments indicated that beetles (Chrysomelidae and Curculionidae, Coleoptera) contributed to pollination of S. parvifolia in Sarawak. Beetles accounted for 74% of the flower visitors collected by net-sweeping, and 30% of the beetles carried pollen, while thrips accounted for 16% of the visitors, and 12% of the thrips carried pollen. The apical parts of the petals and pollen served as a reward for the beetles. Thrips stayed inside the flower almost continuously after arrival, and movements among flowers were rare. Fruit set was significantly increased by introduction of beetles to bagged flowers, but not by introduction of thrips. Hand-pollination experiments and comparison of fruit set in untreated, bagged, and open flowers suggested that S. parvifolia was mainly outbreeding.

Cockroach pollination and breeding system of Uvaria elmeri (Annonaceae) in a lowland mixed-dipterocarp forest in Sarawak.

Tropical forest plants are known to be pollinated by a diverse array of animals. Here we report on the pollination of a woody climber species, Uvaria elmeri (Annonaceae), by cockroaches in a lowland mixed-dipterocarp forest in Sarawak, Malaysia. To the best of our knowledge, this is the first report of pollination by cockroaches. The cauliflorous flowers in the understory are protogynous and bloomed for 50 h. An odor similar to decayed wood or a mushroom was secreted by flowers and was stronger during the male stage. Pollinators were cockroaches (Blattellidae) and drosophilid flies (Drosophilidae). Cockroaches, the main pollinators, visited flowers during both female and male stages at night, feeding on stigmatic exudate and pollen. Drosophilids, the secondary pollinators. mainly visited female-stage flowers during daytime, fed on stigmatic exudate. and laid eggs on stigmas. Neither autogamy nor self-compatibility was observed. Fruit production appeared to be pollen-limited. The fruit set, which was 2% of flowers in natural condition, was significantly lower than the 30% fruit set obtained by artificial cross-pollination. We discuss the traits of cockroaches as pollinators and the breeding system of U. elmeri.

Three pollination guilds and variation in floral characteristics of Bornean gingers (Zingiberaceae and Costaceae).

The pollinators of 29 ginger species representing 11 genera in relation to certain floral morphological characteristics in a mixed-dipterocarp forest in Borneo were investigated. Among the 29 species studied, eight were pollinated by spiderhunters (Nectariniidae), 11 by medium-sized Amegilla bees (Anthophoridae), and ten by small halictid bees. These pollination guilds found in gingers in Sarawak are comparable to the pollination guilds of neotropical Zingiberales, i.e., hummingbird-, and euglossine-bee-pollinated guilds. Canonical discriminant analysis revealed that there were significant correlations between floral morphology and pollination guilds and suggests the importance of plant-pollinator interactions in the evolution of floral morphology. Most species in the three guilds were separated on the plot by the first and second canonical variables. Spiderhunter-pollinated flowers had longer floral tubes, while Amegilla-pollinated flowers had wider lips than the others, which function as a platform for the pollinators. Pistils and stamens of halictid-pollinated flowers were smaller than the others. The fact that gingers with diverse morphologies in a forest with high species diversity were grouped into only three pollination guilds and that the pollinators themselves showed low species diversity suggests that many species of rare understory plants have evolved without segregating pollinators in each pollination guild.

Cospeciation of ants and plants

Cospeciation, in which both parties of an ecological interaction speciate in parallel with each other, has rarely been reported in biotic associations except the cases for host–parasite interaction. Many tropical plants house ants and thereby gain protection against herbivores. Although these ant–plant symbioses have been regarded as classical cases of coevolved mutualism, no evidence of cospeciation has been documented. The Asian ant–plant association between Crematogaster ants and Macaranga plants is highly species specific and the molecular phylogeny of the ants parallels the plant phylogeny, reflecting history of cospeciation. Evidence is presented that this association has been maintained over the past seven million years. Phylogeographic patterns of 27 ants from two Macaranga species suggest that allopatric cospeciations are still in progress in Asian wet tropics.

Six-Year Population Fluctuation of the Giant Honey Bee Apis dorsata (Hymenoptera: Apidae) in a Tropical Lowland Dipterocarp Forest in Sarawak

Abstract The giant honey bee Apis dorsata F. inhabits lowland tropical rainforests in Southeast Asia, where a general, community-wide flowering occurs at intervals of 4 yr on average. The numerical response by the honey bee population to the drastic increase of flower resources during general flowering was investigated for 6 yr by monthly light-trapping and by nest counts in a lowland dipterocarp forest in Borneo. The numbers of A. dorsata workers obtained by light-trapping were highest during general flowering periods, whereas very few workers were trapped in other periods. The abundance of A. dorsata nests showed temporal correspondence with the abundance of trapped workers, and the nests disappeared in the nonflowering periods. These data suggest that the A. dorsata population increases rapidly in response to general flowering and that this is initiated by nonseasonal, long-distance migration. Drones of A. dorsata were present during the general flowering period, but there is no evidence that reproduction by A. dorsata occurs only in general flowering periods. Fluctuation in abundance by the honey bee A. koschevnikovi Enderlein was also observed by monthly light-trapping. The temporal trend of this species was similar to that of A. dorsata, but sightings persisted even in the nonflowering periods. Both honey bees responded numerically to floral resources, but long-distance migration in A. koschevnikovi was unlikely.

Density-dependent ant attendance and its effects on the parasitism of a honeydew-producing scale insect, Ceroplastes rubens

The intensity of attendance by a honeydew-foraging ant, Lasuis niger, on the red wax scale insect, Ceroplastes rubens, was estimated at different manipulated densities in the field. The time that individual ants were present and the total attendance time (seconds x number of ants) of ants on scale-infested twigs significantly increased as the density of C. rubens increased, i.e. ant attendance was density dependent. To determine the effects of density dependence of ant attendance on parasitism of C. rubens by Anicetus beneficus, we measured parasitism rates in the field at different density levels of C. rubens both with ant attendance and with ants excluded. Parasitism rates were higher when ants were excluded, at each density level. Although the parasitism rate significantly deceased as scale density increased, whether or not ants attended, the difference in parasitism rate between density levels was strikingly less without ant attendance. Therefore, the density-dependent decrease of parasitism rate was more pronounced with ant attendance. Mortality not due to parasitism showed density dependence in both conditions and did not change when ants were excluded. These results indicate that attending ants reduce parasitism and that, as a consequence of the density dependence of ant attendance, the efficiency of reduction of parasitism by ants is enhanced at higher densities of C. rubens.

Population dynamics of animals in unpredictably-changing tropical environments

We studied population dynamics of a solitary phytophagous beetle,Epilachna viqintioctopunctata and a social stingless bee,Trigona minangkabau, in Sumatra, Indonesia for 5 years from 1981.Population increase ofEpilachna vigintioctopunctata was suppressed in months of normal rainfall (≥300mm) but was released in the 1982–1983 El Nino-Southern. Oscillation when rainfall dropped to 50% of the long-term average. Mechanisms might be direct; rainfall lowered egg hatchability and the time of adult’s residence on host plants. When dry weather continued for more than three generations, theEpilachna vigintioctopunctata population reached a density at which food shortage due to defoliation occurred. Although parasitism of immature stages was high, it was not a population-regulating factor. Thus, there were two types of ecological crunch: competition for food resources at the end of favourable dry periods and high mortality during heavy rainfall periods that usually followed El Nino-Southern Oscillation dry conditions.By an experimental addition of artificial nest sites, colony density ofTrigona minangkabau increased 2.5 times the original density of natural colonies. One-half of artificial nest sites were occupied by arboreal ants and thus competition for nest sites with ants suppressed further increase ofTrigona minangkabau. Intermediate rainfall was favourable forTrigona minangkabau because the rate of colony foundation decreased both during dry El Niño-Southern Oscillation months and months with heavy rain. Colony death was independent from rainfall. Many colonies that survived for 6 months persisted for >2 years and colony density was quite stable.Trigona minangkabau colonies could survive even under unfavourable periods, by hoarding resources in the nest. There was no significant ecological crunch during the study period and colony density almost always tracked the carrying capacity of the habitat, which was basically determined by nest-site abundance.Climatic conditions, especially rainfall, changed with various periodicities, 4–5 years for El Nino-Southern Oscillation, and 2 years for the monsoon and other shorter periods. The contribution of periodicities of 1 and 0.5 years, that were linked to movement of the sun, were weak, indicating that animals could not use seasonal changes of environments,e.g. daylength, to predict environmental changes. We discuss traits adaptive to such unpredictably-changing tropical environments. Separation of predictability of temporal environmental change and synchronous changes among patches improves our understanding. Low oviposition rate and resulting prolonged life-span ofEpilachna vigintioctopunctata, usually associated withK-selected traits of life history, seem to be adaptations for unpredictable environmental changes.