Introduction
Alpine ecosystems in higher latitudes are characterized by cool and short growing season, during which flowering of alpine plants progress rapidly. Many alpine plants depend on insects for pollination, and pollen limitation is a key factor affecting seed production of alpine plants (Kudo, 2022). Because temporal matching of flowering time and pollinator activity, and insect abundance are influenced by climate change, plant–pollinator interactions in alpine ecosystems are predicted to be disturbed by climate change (Inouye, 2015).
Bumble bees, syrphid flies, and non-syrphid flies are the most common and dominant pollinators in alpine ecosystems (Kearns, 1992; Pyke et al., 2011; Inouye, 2020). However, their frequencies and foraging activities vary among geographic regions and along elevational or latitudinal gradients. For instance, bumble bees are absent in New Zealand, where solitary bees and syrphid flies are important pollinators of alpine plants (Bischoff et al., 2013). The foraging range of floral resources of bumble bees becomes wider at higher elevations in the Colorado Rocky Mountains because of higher flowering overlaps among alpine plant species during a short summer (Miller-Struttmann & Galen, 2014). Furthermore, the importance of fly pollinators commonly increases with elevation and latitude due to higher tolerance to cool conditions in dipteran insects compared to hymenopteran insects (Strathdee & Bale, 1998; McCabe & Cobb, 2021). Thus, relative importance of the two major flower-visiting insect groups, i.e., flies and bees, as pollinators of alpine plants may vary among mountain regions at a geographic scale.
Humid tropical/subtropical alpine regions are the most sensitive ecosystems to climate change, where plant communities are composed of many endemic species within isolated mountain areas (Buytaert et al., 2011). Alpine ecosystems in lower latitudes are characterized by longer growing periods and moderate seasonal fluctuations in temperature compared to the alpine ecosystems in higher latitudes. Thus, flowering phenology and seasonal dynamics of flower-visiting insects may be different from the alpine ecosystems in higher latitudes. However, phenological studies on the tropical/subtropical alpine ecosystems are limited (e.g., Kudo & Suzuki, 2004; Pelayo et al., 2019, 2021). To predict the climate change impacts on the tropical/subtropical alpine ecosystems, therefore, clarification of the basic features of flowering phenology at community scale and flower-visiting insects is crucial.
The previous studies conducted in northern Japan (Kudo, 2016; Mizunaga & Kudo, 2017) reported that the abundance of bumble bees showed clear seasonality reflecting the colony development process in which only overwintered queens emerged in the early season and worker abundance increased abruptly in the middle of the season. In contrast, the frequency of flower visitation by dipteran insects was positively related to ambient temperature, but often has no clear seasonality, and they showed outbreaks at unpredictable times. Responding to the seasonal pattern of bumble bees, the group of bee-visited plants tended to have a bimodal flowering pattern, that is composed of early-flowering species and late-flowering species, although actual flowering periods strongly depended on snowmelt time. On the other hand, the group of fly-visited plants showed a unimodal flowering pattern in which many species flowered in the middle of season when the ambient temperature was high. These results suggest that different selective forces may act on flowering behavior between bee-visited and fly-visited species even within the same alpine plant communities. To test this possibility, comparisons of flowering phenology and flower visitors across multiple alpine ecosystems are necessary.
In the present study, we recorded flowering phenologies of alpine plant communities and seasonal dynamics of flower-visiting insects in the Hehuanshan area of central Taiwan. Taiwan is a mountainous island located in the tropical/subtropical climate zone, where more than 200 mountains exist above 3000 m elevations. The mountain flora of Taiwan is characterized by a high proportion of endemic species (60%: Hsieh, 2002). A recent study reported that alpine vegetation in Taiwan has been altered by climate change (Chou et al., 2011), and it is expected that plant­–pollinator interactions in the alpine ecosystems may also be influenced by climate change. Moreover, one recent study showing overdispersion in the flower color among closely related species in the alpine flora of Taiwan stresses the importance of plant-pollinator interaction at the community level (Tai et al., 2020). However, there is no information about the flowering patterns of alpine plant communities and the seasonal dynamics of flower-visiting insect communities. In order to clarify the interactions between flowering phenology and seasonal dynamics of flower visitors, we observed seasonal changes in the flower production of plants and the frequency of flower-visiting insects over two years. We expect that hymenopteran insects (mainly bumble bees) and dipteran insects are major flower visitors in the alpine ecosystem of Taiwan as well as mid-latitudinal alpine regions in the northern hemisphere. Our hypotheses are as follows:
1) Flowering of bee-visited plants may be concentrated during the active season of worker bees if bumble bees are major flower visitors in the alpine environment of Taiwan.
2) Flowering of fly-visited plants may vary among species if the seasonality of fly activity is less clear and unpredictable due to the stable temperature conditions during the flowering season.