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Temporal and Spatial Niche Partitioning of Bumblebee Species (Apidae: Bombus) on a Himalayan Mountain

Background Bumblebees are essential pollinators in many ecosystems. To maintain such ecosystem functions, bumblebee diversity remains an important concern. We measured abundance and diversity of bumblebee species along an elevational gradient over three flowering seasons. We hypothesized that co-occurring bumblebees partition niches over time and space. Methods We sampled bumblebees at six different meadows along Yulong Snow Mountain (Yunnan, SW China), a region known for high bumblebee diversity, over summer months (2017 – 2019). We analyzed the standardized abundances of the workers from different bumblebee species over 11 weeklong periods. We also analyzed the standardized abundances of the workers of each species at each of the six different meadows. Results Clear patterns of temporal niche partitioning were most apparent for the two, dominant species, B. friseanus and B. lepidus. Spatial niche partitioning was evident for rarer species which tended to be most abundant at lower elevations. Conclusions Temporal and spatial niche partitioning are among two of the ways that bumblebee diversity is maintained on Yulong Snow Mountain. This has future implications if changing climate conditions disrupt partitioning leading to increased interspecific competition.


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Bumblebees (Bombus Latreille) are important pollinators in numerous ecosystems and for some commercial crops 37 (Corbet, Williams and Osborne 1992;Goulson 2010;Kevan 1991;Memmott, Waser and Price 2004). As the 38 eusocial behavior of gynes and workers requires they collect enough pollen and nectar to feed growing colonies 39 (Heinrich 1979), this leads to longer foraging bouts and additional opportunities for conspecific pollen transfer 40 increasing cross-pollination events (Pleasants 1980). In addition, bumblebees are also uniquely adapted for surviving 41 at higher elevations due to thermoregulatory traits including large hairy bodies that can efficiently retain heat 1982). Consequently, with numerous adaptations to alpine conditions, bumblebee diversity is more likely 67 constrained by additional factors.

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The argument for biotic factors driving bumblebee distributions is based on the competitive exclusion principle 70 (Hardin 1960) in which two species occupying the same ecological niche end eventually in the local extinction of

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Without changes limiting direct interspecific competition the Himalayan region of Yunnan could not be a 78 bumblebee "hotspot." Instead, there would be fewer species with each restricted precisely to elevation zones in 79 which they were best adapted.

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Instead, variation in life-histories make it possible for closely related but sympatric species to decrease competition 82 and avoid extinction although their ecological niches overlap. For example, respective phenology may diverge 83 significantly leading to differing peak periods in which two or more species are most abundant and are exploiting 84 similar resources. This is known as temporal niche partitioning (Winder 2009

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Most of Yulong Snow Mountain is covered in conifer forests with an understory of Quercus species (Luo et al.

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2019). We restricted our study sites to wet meadows between or below forests and dry meadows located above

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As Yulong Snow Mountain has numerous meadows, we selected the largest at median sizes of 33,950 meters 136 squared (Table 1). We made this selection because large meadows tended to have less extreme gradients and fewer 137 confounding factors such as a high edge-to-total-area ratio. Smaller meadows in contrast tended to be very narrow 138 (in between conifer forests) with steep inclines. The dry meadow at the summit was the largest continuous meadow 139 so we sampled only a portion of its total area. Specifically, we sampled this meadow at its highest elevation, roughly 140 equivalent to the median size of the other meadows at lower elevations. The choice to sample only a portion of this summit meadow was made in part due to limitations imposed by steep gradients making sampling dangerous and with the conditions of our study region. The authors found that the upper foraging range for their bumblebee species time rain falls most days (Thomas 1993). This monsoon period also overlaps with the peak flowering season when 153 most bumblebee species are active. Rain was a constant complication for sampling as it made standardizing 154 collection efforts difficult. Weather in the Himalayas is often unpredictable changing quickly and making it perilous 155 to sample. Therefore, we often had to cancel or interrupt sampling at field sites during periods of heavy or severe 156 rainfall. To standardize collection efforts, bumblebees were captured for approximately 1 hour per site. Due to 157 frequent interruptions by unpredictable rains, we often had to remain at each site for 4 or more hours, collecting 158 bumblebees for short intervals between bouts of rain and fog until the total actual collection time pooled to 1 hour.

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Bumblebees were collected exclusively during daylight hours avoiding the time around solar noon (12 -2 PM) when 160 bumblebee flight activity declines due to increased solar radiation (Xu et al. 2021, unpublished data).

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Collections were made from June 24 th to July 26 th in 2017, from August 7 th to September 3 rd in 2018, and from July

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Each site was sampled weekly via aerial netting. Bumblebees were netted only when they were observed foraging 169 actively for nectar and/or pollen. Collected specimens were put into individual tubes to avoid cross contamination of 170 pollen loads for future analyses. Several tubes of different sizes were tried but the most effective was the 5mL screw 171 cap tube (VWR catalog number: 470225-026) because it easily held a single bumblebee but did not take up excess 172 space in field bags or in the freezer. Specimens were euthanized at the KIB field station (3200m).

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Only female workers were included in analyses to avoid potential confounding effects from different castes. The 181 periods of sampling over three summers when pooled led to a greater sampling effort in the middle of the summer 182 and fewer samplings toward the beginning and ends of summer. To account for the unevenness of sampling effort, 183 the combined summer collection period was split into 11 time periods. Each period was 7 days long, from June 24 th 184 to September 8 th . The total abundance of each species collected at each site was then divided by the number of times 185 that site had been sampled during that week period over the three summers (see supplemental [datasheet]) with 186 standardized abundances. All statistical analyses were done using R (R Core Team 2020), a statistical computing 187 language in the integrated development environment of RStudio (RStudio Team 2020) and using the data standardized abundance of each species over 11 week-long periods. To better compare the two most dominant species, with dominance determined by relative abundance, we created a second bar plot with an overlaid, smoothed, and conditional mean line. We then used a boxplot graph to show the distribution of each species over measures such as first recorded occurrence.

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Elevational Distribution Analysis

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We analyzed spatial patterns, to understand relative abundances of each species along an elevational gradient. First,

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we visualized the distributions of each species using a bar plot graph with an overlaid, smoothed, and conditional 204 mean. We then made a boxplot graph to further visualize the elevational distribution of different bumblebee species, 205 as above.

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Over three summers of sampling on Yulong Mountain, 14 different species of bumblebees were identified. Of these,  Cockerell, 1910] were excluded from further analyses as we caught less than five specimens of 212 each taxon. This left a total of 531 worker specimens that were used in the analysis. Bumblebee worker abundances, 213 elevational ranges, weighted mean week of occurrence, and active flight periods are summarized in Table 2.

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The standardized abundance of the remaining nine species over an 11-week period is shown in Figure 2. Two 217 species, B. friseanus and B. lepidus, were the most abundant (

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friseanus was more abundant later in the season (Fig. 3). Figure 4 shows the distribution when each species was 223 active.

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Standardized abundances (Fig. 4) showed that the two most commonly collected species, B. friseanus and B. 227 lepidus, were most common at middle elevations. Both species were less abundant at almost every other elevation.

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There appear to be at least two factors maintaining bumblebee diversity on Yulong Snow Mountain. The first is 234 temporal and based on the phenology of worker flights and foraging periods over the summer flowering season. The 235 temporal difference in peak abundances of B. friseanus and B. lepidus suggests a partitioning effect separating the 236 periods when each species is active (Fig. 3). Indeed, the weighted mean week of occurrence was more than three 237 weeks earlier for B. lepidus than for B. friseanus (Table 2). We also see some temporal partitioning of less abundant 238 species (Fig. 4). Previous studies on bumblebee diversity in other regions also show temporal partitioning. Lye et al.

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Spatial niche partitioning along an elevation gradient on Yulong Mountain appears to show its strongest influence 246 among the rarer bumblebee species as they showed more limited distributions based on elevation. It is possible that, 247 by remaining at lower elevations, these species avoid zones dominated by the two most common species. In appears to be little spatial partitioning along what appears to be a much broader elevational gradient. While B.

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In fact, our results are similar to findings in a report on bumblebees in the Himalayan range through Nepal 258 (Williams et al. 2010) as latitude through the Nepalese region is similar to Yulong. The large elevational gradient 259 and lengthy summer period of Yulong appears to contribute to bumblebee diversity on the mountain chain but may 260 also be indicative of driving factors for bumblebee diversity throughout temperate elevations within the Himalayan 261 chain. As elevational gradients produce many different niches for bumblebees this promotes specialization and the 262 most common species are able to partition when they are most active preventing excessive competition.

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This study covered 11-weeks from summer to early autumn but some bumblebee gynes begin emerging in Spring