Bumble bee niche overlap along an elevation gradient: how traits can inform novel competitive pressures under climate change.

doi:10.21203/rs.3.rs-2958420/v1

Download PDF

Research Article

Bumble bee niche overlap along an elevation gradient: how traits can inform novel competitive pressures under climate change.

https://doi.org/10.21203/rs.3.rs-2958420/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

Climate change-induced range shifts can disrupt interactions between species by moving them in and out of ecological communities. These disruptions can include impacts on competition for shared resources. Bumble bees (Bombus spp.) are important pollinators shifting their range upwards in elevation in response to climate change. These shifts could lead to altered competition between species and threaten co-existence. These impacts are particularly worrying at the tops of mountains where bumble bees are “trapped” and can no longer move up to higher elevations to track climate change. To better understand this issue, we investigated changes in bumble bee diet niche overlap between species along a 2296m elevation gradient in the southern Rocky Mountains. Additionally, we investigated how morphological and phenological traits impact diet composition (flower species visited) between bumble bee species and explored how the continued upward movement of bumble bee species under climate change into the mountaintop may affect trait overlap of newly co-occurring species. We found that diet niche overlap between bumble bee species increased with elevation. We also found that differences in morphological and phenological traits (body size, tongue length, date of activity) were correlated with differences in diet composition between bumble bee species. Finally, we described how bumble bee species moving farther up mountaintops would lead to increased trait overlap for high-elevation species. These shifts could have implications for future competition for resident high-elevation species on mountaintops and exacerbate the effects of climate change on high-elevation bumble bees.

plants

pollinators

montane

alpine

Rocky Mountains.

Climate change is causing many species to move their ranges upwards in elevation and towards the poles to track changing environmental conditions (Hughes 2000; Walther et al. 2002). Range shifts can modify community structure and disrupt ecosystems through the turnover of species in and out of ecological communities (Wardle et al. 2011). The rearrangement of competing species in communities may threaten coexistence, considering the ability of species competing for a shared resource to co-exist is facilitated by each competitor having distinct patterns of resource use, or a distinct “niche” (Chesson 2000). To fully account for the effects of climate change on species, it is important to study how biotic interactions like competition may change in addition to the impacts of abiotic factors.

Insects are critical to the pollination of over 85% of flowering plant species (Ollerton et al. 2011). Insect pollinator communities may be especially vulnerable to species’ range shifts under climate change, considering their strong dependence on host flower species for food (Michener 2007) and their high sensitivity to changing environmental variables (Kingsolver 2013). Spatial mismatches between pollinators and their host plants threaten pollination success (Gomez-Ruiz and Lacher 2019) and affect competition for both groups (Richman et al. 2020). Understanding how competing pollinator species partition their diet and how range changes may impact competition is important for understanding the impacts of climate change on plant-pollinator communities.

Mountain elevation gradients provide an opportunity to study how plant-pollinator communities change with elevation and how range shifts under climate change may alter competitive interactions. Mountains are climatically heterogeneous, making them hotspots for biodiversity and ‘natural experiments’ for understanding ecological responses to climatic change (Körner 2007). As elevation changes, different factors such as temperature, precipitation, productivity, area, and species interactions also change, supporting different numbers of species (McCain and Grytnes 2010). For many plant and pollinator taxa, species richness tends to peak at middle elevations along mountain ranges and decline into higher elevations (Wohlgemuth et al. 2008; Gallou et al. 2017; Chesshire et al. 2021; Sponsler et al. 2022b). As the richness of host flowers and their associated pollinators change, the spectrum of available resources and the number of species competing for that resource can alter the competitive pressures within a community (Doublet et al. 2022). As plant and pollinator species move in and out of communities to track climate change, competitive pressures will likely be affected. This is particularly worrying at the tops of mountains, where species can no longer move upwards in elevation to track climate change.

Bumble bees (Bombus spp.) are shifting their ranges in response to climate change (Kerr et al. 2015). Bumble bees are essential pollinators of native plants in mountain ecosystems (Bingham and Orthner 1998; Gorenflo et al. 2017; Minachilis et al. 2021); however, studies have documented dramatic bumble bee declines across the Northern Hemisphere (Kosior et al. 2007; Cameron et al. 2011). Climate change is a distinct driver of these losses, and its effects are independent of other important drivers like land-use change and pesticide use (Kerr et al. 2015; Soroye et al. 2020). In response to climate change, bumble bees are tracking warming temperatures by moving upwards in elevation to remain within a habitable range of environmental conditions (Kerr et al. 2015). However, at mountaintops, bumble bee species can no longer move upward to track suitable climate. The upward movement of colonizing species into the same environment as resident species at mountaintops will likely cause novel competitive interactions for shared floral resources that could exacerbate the effects of changing climate. Accounting for these novel competitive interactions is important for understanding how species will respond to climate change (Alexander et al. 2015).

Competition between co-occurring bumble bee species is heavily influenced by their dependence on the flowers that they visit for pollen and nectar food resources (Heinrich 1976). Exploitative competition, wherein species compete indirectly for a shared resource, is the primary mechanism for resource partitioning between bumble bee species (Inouye 1978). Since closely related species, like bumble bees, are similar in life history and morphology, they compete more strongly with each other for limited resources than more distantly related taxonomic groups (Burns and Strauss 2011). Co-existence between bumble bee species may be facilitated by traits that allow for niche partitioning of floral resources. For example, morphological trait variation among species, such as body size and tongue length, also may influence diet niche partitioning. Past research has found that bumble bee morphological traits influence which flowers species visit (Harder 1985; Sponsler et al. 2022a). Longer-tongued bumble bees, for example, are more likely to visit flowers that are more closed in shape (lip, funnel, and flag-shaped flowers) than their shorter-tongued counterparts that prefer more open-shaped flowers (disc, stalk-disc, bell, head-shaped flowers; Sponsler et al. 2022a). This difference in visitation may be attributed to species visiting flowers that are most energetically efficient for their morphology (Balfour et al. 2021). Phenology, or the timing of bumble bee activity, differs between species during the season and can also be a mechanism for diet niche partitioning since bumble bees can only access flowers that are open when they are actively foraging. Therefore, variation in morphology and phenology may be important indicators of variation in diet composition and niche partitioning between bumble bee species.

Past research on bumble bee competitive interactions along elevation gradients has shed light on the patterns and mechanisms underlying niche overlap. Using historical data collected between 1966 and 1969 by Macior (1974) in the Colorado Rocky Mountains, Miller-Struttmann and Galen (2014) found high niche overlap in the lowest and highest elevation zones of their study, with niche overlap peaks attributed to disturbance in the lowest zone (1,600-2,700m) and a shortened flowering window in the highest zone (3,500-4,300m). Additionally, they found that long-tongued bumble bees altered their foraging behavior in the alpine by becoming more generalized, suggesting that tongue length plays a role in determining what flowers species visit at different elevations (Miller-Struttmann and Galen 2014). Another study in the Rocky Mountains found that bumble bee species that have recently colonized alpine environments are likely to take better advantage of foraging early and late in the season, potentially making them more likely to outcompete resident species in a warming alpine environment (Miller-Struttmann et al. 2022). Still, patterns of niche overlap along elevation gradients, traits' influence in determining diet, and how climate change may impact competition between mountain bumble bees are poorly understood.

In this study, we investigated bumble bee distributions and floral resource partitioning along the elevation gradient of Pikes Peak in the Colorado Front Range. Further, we examined how bumble bee traits relate to floral resource partitioning to better understand niche partitioning and how it might change with elevational range shifts under climate change. We asked the questions: Q1: How does bumble bee diet niche overlap change along the elevation gradient?; Q2: Are phenology, body size, and tongue length correlated with bumble bee diet composition?; and Q3: How would the upward movement of bumble bee species impact phenological and morphological trait overlap at the top of the mountain? For Q1, we predicted that bumble bee diet niche overlap would increase with elevation, considering high-elevation mountain environments have short flowering seasons and less plant species diversity (McCain and Grytnes 2010; Stephens et al. 2022). For Q2, we predicted that phenology, body size, and tongue length values would correlate with diet composition for species, considering bumble bees should make choices that are most efficient for their morphology (Balfour et al. 2021) and should only be able to visit flowers that are open during their foraging period. For Q3, we predicted that the simulated upward movement of bumble bee species into the mountaintop would create increased overlap in phenology, body size, and tongue length trait space for resident high-elevation bumble bee species.

To test our questions, we conducted a four-year survey of bumble bee and host flower interactions along a 2295m elevation gradient on Pikes Peak (Fig. 1A), a mountain in the southern Front Range of the Rocky Mountains in Colorado, USA. We divided the elevation gradient into five equidistant zones (Fig. 1B). We estimated bumble bee and host flower species richness and diet niche overlap within each elevation zone. Next, we assessed if phenology, body size, and tongue length are related to diet composition in bumble bees by testing for correlations between diet and trait values. Finally, as a thought experiment, we explored how trait space overlap may change in the mountaintop under climate change by simulating the upward movement of bumble bee species.

Study area

The Front Range of Colorado, USA, in the southern Rocky Mountains, is a hotspot for bumble bee diversity; half of the United States’ 48 bumble bee species reside in Colorado, most of which occupy counties within or bordering the Front Range (Wright et al. 2017). The Front Range’s natural transition from low-elevation short-grass prairie, that begins around 1000m, to high-elevation mountain environments, that peak around 4300m, encompasses suitable habitat for many bumble bee species. The high species richness of the Front Range is useful for understanding bumble bee community patterns and niche partitioning along an elevation gradient as well as making predictions about the consequences of the upward movement of bumble bee species.

We carried out our study between May and September for four years (2019–2022) on Pikes Peak, the highest mountain (4302m) in the southern Front Range of Colorado (38° 50' 15.59" N, -105° 02' 23.40 W"). Observations were made on Pikes Peak along an elevation gradient ranging from 1990m to 4286m (Fig. 1A). The United States Department of Agriculture Forest Service manages most of the study area. Vegetation varies considerably along the elevation gradient: at the base of the mountain in the foothills (1981m-2438m), Gambel oak shrubs (Quercus gambelii) dominate dry, rocky slopes; as elevation increases, ponderosa pine (Pinus ponderosa) and aspen (Populus spp.) begin to dominate in the montane (2438m-3048m); in the subalpine (3048m-3474m), Engelmann spruce (Picea engelmannii) and limber pine predominate; finally, in the alpine (3475-4302m), trees disappear and are replaced by tundra vegetation such as sedges and mat-forming plants (Kelso 2012). High plant species turnover provides a range of floral resources that bumble bees can use along the elevation gradient.

Study design

Bumble bee and host flower interaction data were used to characterize bumble bee niche overlap along the elevational gradient. The bumble bee interaction data used in this study were a subset of a concurrent study on plant-pollinator interactions on Pikes Peak (see Funding). We recorded interactions along hiking trails and roadsides that spanned the elevation extent and observed flowers for at least 1-minute increments. The bumble bee had to touch the flower's stamen or pistil for an interaction to be recorded. Bumble bees found interacting with flowers in the field were usually collected via aspirator or net, frozen, and mounted for later identification. Individuals that could confidently be identified on sight, including the western bumble bee (Bombus occidentalis), which is declining in western North America, were released. All host flowers observed were identified to species using Ackerfield (2015). Each collected interaction data point had an associated date, WGS84 GPS coordinates, and elevation recorded. We sampled nearly every weekday during the span of the flowering period between late May and mid-August from 2019–2022. Two additional sampling days occurred in September of 2022 to include late-season plant-pollinator interaction data. Observation effort varied by year and elevation (Online Resource Fig. 1A & B, Online Resource Tables 1 and 2 for details). Some flower species were observed for long periods of 1-minute increments for the concurrent study at Pikes Peak, which may have overrepresented some host flower and bumble bee interactions. All collected bumble bees were identified to species and caste in the lab using the Leica Stereozoom S9i microscope and taxonomic keys and references (Byron 1980; Williams et al. 2014; Wright et al. 2017). In addition to our collected data, we also obtained tongue length (mm) and body size (mm) data from Colorado-based studies and guidebooks (Macior 1974; Wright et al. 2017) for our trait analyses. The tongue trait data were not available for all species and castes. Specifically, Bombus balteatus, B. fervidus, B. fraternus, B. griseocollis, B. huntii, B. insularis, B. pensylvanicus, and B. rufocinctus, as well as all male tongue length values were excluded from tongue trait analyses due to lack of data in Macior (1974).

Table 1

Percent of phenology, body size, and tongue length trait overlap for each unique pairing of resident bumble bee species constrained to high elevations and colonizing bumble bee (*Bombus*) species that were moved into the mountaintop. Interactions in bold are over 75% trait overlap.
	B. appositus	B. nevadensis	B. occidentalis	B. pensylvanicus	B. rufocinctus
Phenology
B. balteatus	63.5%	51.4%	48%	7.4%	56.3%
B. frigidus	40%	32.4%	49.2%	5.6%	35.4%
B. sylvicola	60.4%	79.2%	67.1%	4.7%	88.5%
Body Size
B. balteatus	76.9%	42.9%	83.3%	53.3%	58.3%
B. frigidus	50%	23.5%	76.9%	33.3%	81.8%
B. sylvicola	42.9%	13.3%	58.3%	25%	77.8%
Tongue Length
B. balteatus	X	X	X	X	X
B. frigidus	0%	1%	62.9%	X	X
B. sylvicola	2.8%	14.7%	84.7%	X	X

We divided observations along the elevational gradient into five equidistant zones (459m), taken from the bumble bee and flower interaction observation at the lowest observation (1990m) to the observation at the highest observation (4286m; Fig. 1B). Zone 1 was our lowest zone in the elevation gradient (1990m to 1449m), followed by zone 2 (2449m-2908m), zone 3 (2908m-3367m), zone 4 (3367m-3827m), and zone 5 (3827m-4286m). We chose to pool data collected from all four years for our analyses since our dataset is too limited to examine temporal patterns. Therefore, generalized results across all years helped us better understand the overall trends among elevation zones.

Statistical analysis

We conducted all analyses in R version 4.0.3 (R Core Team 2020). We checked the data for GPS errors by mapping data points using the “ggmap” package version 3.0.0 (Kahle and Wickham 2013) and checking elevation correspondence with latitude and longitude using the “elevatr” package version 0.4.2 (Hollister et al. 2021). Bumble bee observations were dropped from the dataset if their GPS points were incorrect (seven points), if their elevations appeared as outliers (> 300m different from the elevation points within the USGS Elevation Point Query Service; four points), or if we were unable to identify the host species (two points). We used the packages “bipartite” version 2.16, “ggridges” version 0.5.4, and “ggplot2” version 3.4.1 for data visualization (Dormann et al. 2009; Wilke 2022; Wickham 2016).

Assessing elevational patterns of species richness and sampling completeness

To help inform our understanding of diet niche partitioning between bumble bee species, we calculated the richness of host flower species and bumble bee species within each elevational zone. Host flower and bumble bee richness estimates give us insight into the breadth of available flower species and the number of bumble bees competing for them. Species richness for host flowers and bumble bees was estimated for each of the five elevational slices using rarefaction from the “iNEXT” package version 3.0.0 (Hsieh et al. 2022). To account for uneven sampling within each zone, we compared rarefied species richness estimates and their confidence intervals at n = 1,937 observations, the final observation of the maximum sampled zone (zone 2). All other zone species richness estimates were extrapolated to this point. To assess the thoroughness of sampling at each elevation zone, we estimated sample completeness for bumble bee and host flower species visited and their unique interactions using the “iNEXT” package (Hsieh et al. 2022).

Q1: How does bumble bee diet niche overlap change along the elevation gradient?

We used Horn’s index (Horn 1966) to calculate niche overlap in diet composition between bumble bee species, where 0 indicates no niche overlap and 1 indicates perfect niche overlap. We estimated niche overlap for bumble bees across the elevation gradient using non-parametric bootstraps that sampled without replacement using the “bootstrapnet” package version 1.0.0 (Stefan and Knight 2023). This approach allowed us to account for uneven sampling across the elevation gradient by comparing niche overlap estimates at equivalent observations and estimating uncertainty within each elevational zone. We chose to bootstrap without replacement to avoid the potential bias of overrepresenting common interactions between bumble bees and host flowers. In our bootstrap, we estimated niche overlap at a starting interval of N = 50 observations (approximately 10% of 491 unique flower and bumble bee interactions) and continued at n = 1 intervals until no more samples were left in each zone. This sampling procedure was replicated 1000 times. The mean niche overlap values for each zone were compared at n = 117 observations. We chose n = 117 since our least sampled zone (zone 5) had 118 interactions, and sampling below this value gave us confidence intervals for all zones. To test whether niche overlap increased with elevation (Q1), we ran a linear regression on each elevation zone's mean niche overlap estimates. To visualize differences in host flower diet composition between bumble bee species, we used nonmetric multidimensional scaling (NMDS) of diet compositions of bumble bees across all elevation zones, as well as within each zone using the “vegan” package version 2.5.7 (Oksanen et al. 2020).

Q2: Are phenology, body size, and tongue length correlated with bumble bee diet composition?

We used Mantel tests to examine the relationship between species traits (phenology, body size, and tongue length) and diet composition (plant species visited and frequency of these interactions) between each bumble bee species. We created a matrix of Bray-Curtis dissimilarity values for the frequency and composition of diet, as well as matrices of Euclidean distances of trait values (phenology, body size, tongue length) between each pairwise combination of bumble bee species. Bray-Curtis dissimilarity values, which range from 0 (complete similarity) to 1 (complete dissimilarity), were calculated using the “vegan” package (Oksanen et al. 2020). Euclidean distance dissimilarity values were calculated using the “stats” package version 4.0.3 (R Core Team 2020). In total, four matrices were created. We tested for correlation between the diet dissimilarity matrix and each trait matrix using Mantel tests from the “vegan” package (Oksanen et al. 2020). Mantel tests determine correlation by comparing observed matrices to a null model, where the matrix values are shuffled at random and tested for significance based on these permutations (Oksanen et al. 2020). The resulting Mantel test statistic value varies between − 1 and 1, with − 1 indicating perfect negative correlation and 1 indicating perfect positive correlation. To investigate whether body size variation correlates with tongue length variation, we ran Pearson's correlation on available female bumble bee tongue length and corresponding body size values in base R. Pearson’s correlation coefficient varies between − 1 and 1, with − 1 indicating perfect negative correlation and 1 indicating perfect positive correlation. Finally, to visualize diet composition in relation to trait variables, we created NMDS plots of species diet composition pooled across all elevation zones and overlaid with the average trait values for each species in multidimensional space using the “vegan” package (Oksanen et al. 2020).

Q3: How would the upward movement of bumble bee species impact phenological and morphological trait overlap at the top of the mountain?

To explore the effects that the continued upward movement of bumble bee species in response to climate change may have on the trait overlap of high-elevation mountaintop bumble bee species, we simulated the colonization of bumble bees currently found in the fourth zone into the fifth zone. To do this, we added 459m to the elevation data for bumble bees found in zone 4, which underlies the highest elevation zone, zone 5. Next, to identify colonizing and resident mountaintop species that may have high trait similarity under simulated climate change, we calculated the percent overlap of phenology, body size, and tongue length ranges between each unique pairing of resident and colonizing bumble bee species, as well as between high elevation specialists (Bombus balteatus, B. frigidus, and B. sylvicola) and colonizing bumble bee species. Percent trait overlap was calculated by dividing the shared trait space by the total trait space for both species. We highlighted bumble bee pairings with high trait overlap (> 75%) as more likely to have high competition for floral resources under climate change.

In this exercise, we assumed that bumble bees would move upwards but not their plant resources. This assumption was made on the basis that bumble bees will likely be able to respond to warming temperatures with range shifts more quickly than plants (Pyke et al. 2016). Therefore, plants were not included in this exploratory model. To visualize changes in the mountaintop’s bumble bee community trait overlap under this simulation, line segment graphs representing the range of occupied trait space between each pairing of resident and colonizing bumble bee species were plotted using the “ggplot” package (Wickham 2016).

We observed 19 out of Colorado’s 24 bumble bee species interacting with 148 host flowering plants, totaling in 491 unique bumble bee and host flower interactions (Online Resource Fig. 3). We observed 15 of the 18 species previously recorded for El Paso County and four species that were not previously recorded in Wright et al. (2017). Bombus centralis, B. bifarius, and B. flavifrons were the most dominant species in our flower-bumble bee network (Online Resource Fig. 3).

Bumble bee species varied in their elevation range, phenology, as well as in their body size and tongue length values (Online Resource Fig. 4A, Online Resource Fig. 4B). Bumble bee phenology is constrained by changing environmental variables with elevation; therefore, species with a longer phenological window tended to occupy lower elevations. Bombus griseocollis, B. nevadensis, B. huntii, and B. rufocinctus interacted with flowers for most of the summer study periods, whereas B. pensylvanicus, B. occidentalis, B. mixtus, B. balteatus, and B. sylvicola had narrow foraging windows (Online Resource Fig. 4A). Bombus griseocollis emerged and was abundant relatively early in the summer seasons compared to the rest of the species observed and was also most concentrated at the lowest elevations in the study (Online Resource Fig. 4A). Bombus pensylvanicus, which is in decline and categorized as vulnerable by the International Union for the Conservation of Nature, appeared to have a narrow foraging window (Hatfield et al. 2015); however, observations of this species were limited to four occurrences, and there is likely a longer window in reality (Online Resource Fig. 4A). Bombus balteatus, B. frigidus, and B. sylvicola were constrained to the highest elevations within the study extent, while B. griseocollis was most constrained at the lowest elevations (Online Resource Fig. 4B).

Assessing elevational patterns of species richness and sampling completeness

Bumble bee species richness estimation at n = 1937 observations was unimodal, with peaks in lower to middle elevational zones. Bumble bee species richness was greatest in zone 2 and similarly lowered in zones 1, 3, 4, and 5. Zones 2 and 4 were significantly different from one another. Rarefied and extrapolated bumble bee species richness at n = 1937 included 16 species in zone 1 (SE: +/- 3.27), 21 species in zone 2 (SE: +/- 2.32), 17 species in zone 3 (SE: +/- 5.80, 15 species in zone 4 (SE: +/- 2.40), and 15 species in zone 5 (SE: +/- 5.05) (Fig. 2A).

Host flower species richness peaked in zone 2 and dropped to its lowest point in zone 5. All confidence intervals were significantly different from one another with the exception of zone 3, whose confidence interval overlapped with zone 1, zone 2, and zone 4. Rarefied and extrapolated host flower species richness at n = 1937 included 80 species in zone 1 (SE: +/- 19.78), 117 species in zone 2 (SE: +/- 10.22), 99 species in zone 3 (SE: +/- 46.76, 51 species in zone 4 (SE: +/- 7.86), and 19 species in zone 5 (SE: +/- 4.57; Fig. 2B). The sample completeness for bumble bee and host flower species in each zone was generally high. Sample completeness for bumble bee and host flower interactions was lower, varying between 70% and 95% for the elevation zones (Online Resource Fig. 2).

Q1: How does bumble bee diet niche overlap change along the elevation gradient?

Bumble bee diet niche overlap increased linearly with elevation zone (t = 13.43, P-value = < 0.001; Fig. 3; Online Resource Fig. 5). Niche overlap values in the highest elevational zone (zone 5) were over three times greater than the lowest elevational zone (zone 1). Zones 1 and 2 were significantly different from zone 5. Niche overlap measurements compared at n = 117 included zone 1: 0.11 (lower 95% CI: 0.06, upper 95% CI: 0.18, zone 2: 0.15 (lower 95% CI: 0.08 upper 95% CI: 0.26), zone 3: 0.22 (lower 95% CI: 0.14, upper 95% CI: 0.36), zone 4: 0.26 (lower 95% CI: 0.17, upper 95% CI: 0.39), and Zone 5: 0.35 (lower 95% CI: 0.33, upper 95% CI: 0.36). NMDS plots showed differences in bumble bee species' diet composition relative to one another (Fig. 5).

Q2: Are phenology, body size, and tongue length correlated with bumble bee diet composition?

Euclidean distance values in phenology, body size, and tongue length between bumble bees were all positively and significantly correlated with differences in diet composition (Bray-Curtis dissimilarity) between species. The Mantel test statistic was 0.35 (P-value = 0.001) for phenology and diet differences, 0.26 (P-value = 0.014) for body size and diet differences, and 0.34 (P-value = 0.026) for female tongue length and diet differences (Fig. 4). Pearson’s product moment correlation coefficient between available female bumble bee tongue length and body size values were positively correlated at 0.78 (P-value < 0.01). NMDS plots for diet overlaid with continuous data for phenology, body size, and tongue length visually illustrated differences in diet as they relate to trait values (Fig. 6).

Q3: How would the upward movement of bumble bee species impact phenological and morphological trait overlap at the top of the mountain?

Eleven species resided in the mountaintop (zone 5) before simulating the colonization of lower elevation species upwards: Bombus balteatus, B. bifarius, B. centralis, B. fervidus, B. flavifrons, B. frigidus, B. huntii, B. insularis, B. melanopygus, B. mixtus, and B. sylvicola. Five additional bumble bee species, Bombus appositus, B. nevadensis, B. occidentalis, B. pensylvanicus, B. rufocinctus, colonized the mountaintop under our simulation, resulting in 16 different species residing at the mountaintop (Fig. 7). Adding these bumble bee species to the mountaintop increased the number of species occupying high trait space overlap (Fig. 7).

Percent phenological overlap between resident species restricted to high elevations (Bombus balteatus, B. frigidus, B. sylvicola) and potential future colonizing bee species at the top of the mountain was greatest (> 75%) for the combination of B. sylvicola and B. nevadensis (79.2%) as well as B. sylvicola and B. rufocinctus (88.5%) (Table 1). Out of resident species restricted to high elevations, Bombus sylvicola was the only species to have high phenological trait overlap with colonizing bee species (two total). Out of the colonizing bee species, Bombus nevadensis and B. rufocinctus had the greatest number (one) of high phenological trait overlap (> 75%) values with B. sylvicola (Table 1). The percentages of phenological overlap between all resident species and potential colonizing bumble bee species were also calculated (Online Resource Table 2).

Percent body size overlap between resident species restricted to high elevations (Bombus balteatus, B. frigidus, B. sylvicola) and potential future colonizing bee species at the top of the mountain was greatest (> 80%) for the combinations of B. balteatus and B. occidentalis (83.3%) as well as B. frigidus and B. rufoncintus (81.8%) (Table 1). Out of resident species restricted to high elevations, Bombus balteatus and B. frigidus had the greatest numbers (two) of high body size trait overlap (> 75%), followed by B. sylvicola with one interaction of high body size trait overlap (75%; Table 1). Out of colonizing bee species, Bombus occidentalis and B. rufocinctus had the greatest number of (two) high body size trait overlaps (> 75%), followed by B. appositus with one interaction of high body size trait overlap (> 75%) (Table 1). The percentages of body size overlap between all resident species and potential colonizing bumble bee species were also calculated (Online Resource Table 2).

Percent tongue length overlap between resident species restricted to high elevations (Bombus balteatus, B. frigidus, B. sylvicola) and potential future colonizing bee species at the top of the mountain was greatest (> 84%) for the combination of B. sylvicola and B. occidentalis (84.7%; Table 1). Out of resident species restricted to high elevations, Bombus sylvicola was the only species with high tongue length trait overlap with colonizing bee species (> 75%; Table 1). Out of colonizing bee species, Bombus occidentalis was the only species with high tongue length trait overlap with resident species (> 75%) (Table 1). The percentages of tongue length overlap between all resident species and potential colonizing bumble bee species were also calculated (Online Resource Table 2).

Overview

Our results show that (1) bumble bee species diet niche overlap increases with elevation, (2) phenology and morphology are correlated with diet between species, and (3) future mountaintop bumble bee species may have increased competition under climate change due to more species occupying similar morphological and phenological trait space. These results present new patterns of bumble bee niche overlap across an elevation gradient and suggest that morphological and phenological traits can be important for explaining diet composition and informing consequences of future upward movement of bumble bee species into mountaintop environments on competitive interactions.

Assessing elevational patterns of species richness and sampling completeness

As expected, both bumble bees and host flowers had unimodal peaks in species richness at middle-lower elevations. After peaking in zone 2, species richness for both taxa continued to taper with elevation. The unimodality in our findings is generally consistent with past studies that have investigated bumble bee and host flower species richness along elevation gradients across the globe (Goulson et al. 2008; Miller-Struttmann and Galen 2014; Sponsler et al. 2022b). Our estimates of bumble bee species richness were similar to Miller-Struttmann and Galen (2014), who found that bumble bee populations in the Colorado Front Range generally decreased in species richness with elevation. However, our estimates of nectar and pollen host flower richness were different from Miller-Struttmann and Galen (2014), who found increases in pollen host-flower species richness with elevation. Bumble bees vary in their probability of carrying pollen from one or multiple flower species with elevation (Miller-Struttmann and Galen 2014) and tend to visit a broader range of flowers for nectar resources than pollen (Goulson and Darvill 2004), which may explain differences in our results. Our estimates of bumble bee and host flower richness are valuable in informing niche overlap (Costa-Pereira et al. 2019) as they determine the availability of the shared resource.

Q1: How does bumble bee diet niche overlap change along the elevation gradient?

As predicted, bumble bee diet niche overlap increased with elevation and was greatest at the mountaintop, likely due to a restricted temporal flowering window and low plant species richness. Our results differ from Miller-Struttmann and Galen’s (2014) historical niche overlap analysis in the Colorado Front Range, which found high diet niche overlap at the top and bottom of the elevation gradient (Miller-Struttmann and Galen 2014). They attributed high niche overlap at the bottom of their elevation gradient to disturbance. While there is heavy traffic on designated paths at Pikes Peak, the extent of our study is largely protected from intensive land use and human development. Therefore, disturbance may be less of an influence than in Miller-Struttmann and Galen (2014).

Competition is logistically difficult to measure in the wild as it requires excluding bumble bee species from one another (Goulson et al. 2008; Brosi et al. 2017). Our niche overlap estimates are not a direct measure of competition but rather a statistic that measures the shared use of a resource. Past research has suggested that exploitative competition between bumble bee species is the primary mechanism driving niche partitioning between bumble bee species (Inouye 1978). Therefore, niche overlap is a valuable tool for identifying species utilizing a limited resource similarly and identifying potential novel competitive interactions under climate change.

Q2: Are phenology, body size, and tongue length correlated with bumble bee diet composition?

Differences in both morphological (tongue length and body size) and phenological traits were correlated with differences in diet between species. This supports the idea that morphological and phenological traits mediate diet niche partitioning (Goulson et al. 2008; Balfour et al. 2021; Sponsler et al. 2022a). We found that tongue length and body size were highly correlated. The non-independence of these traits makes it difficult to determine which trait is driving diet composition in bumble bees (Christmas et al. 2022; de Keyzer et al. 2016). Notwithstanding, our findings indicate the value that morphology has in helping to predict the diet of bumble bee species. Body size and tongue length values used in this analysis were taken from Colorado bumble bees used for past scientific research (Macior 1974; Wright et al. 2017). We assumed that while tongue length and body size may be different at Pikes Peak or may have changed since these past measurements, the relative relationships of these traits between species have likely remained similar, and therefore our findings from these data are still valuable to understanding trait impacts on diet.

Q3: How would the upward movement of bumble bee species impact phenological and morphological trait overlap at the top of the mountain?

Moving bumble bee observations upwards into the mountaintop created the addition of new species and pairs of co-occurring bumble bee species that may compete with one another under climate change. Of the three resident mountaintop species, B. sylvicola had the greatest number of high trait overlap interactions with colonizing species across all three traits. B. sylvicola is classified by the International Union for the Conservation of Nature as “least concern” (Hatfield et al. 2015b). However, recent genomic analysis of specimens initially identified as B. sylvicola has revealed the presence of a cryptic species, B. incognitus (Christmas et al. 2022). Two species being categorized as B. sylvicola may be conflating their population status. Additionally, high-elevation resident species such as B. sylvicola have lower tolerances for warming temperatures (Oyen et al. 2016) and may be less well adapted to take advantage of a longer foraging window in the alpine under climate change compared to colonizing species (Miller-Struttmann et al. 2022). Increased competitive pressures in addition to these pre-existing disadvantages may exacerbate the effects of climate change on resident alpine species.

Our approach to this simulation was simplistic and only considered individual comparisons of traits between co-occurring bumble bee species. We did not consider how the range shifts of host flowers might impact potentially novel competitive interactions at the tops of mountains since we assumed bumble bees will be more mobile in their response to warming temperatures than plants. In addition, we assumed that all bumble bees would move upwards in response to climate change at the same rate. This may not be realistic, as past research has documented species variation in bumble bee elevation shifts (Pyke et al. 2016; Marshall et al. 2020). Additionally, we assumed that bumble bee species' phenology would not change as they move upwards in elevation. Past research has found that bumble bees that have already colonized the alpine tend to be less genetically constrained, or “canalized,” in their phenology than resident bumble bees (Miller-Struttmann et al. 2022), so it may be reasonable to assume that phenologies will not change drastically between colonizing and resident species.

Our findings highlight the value of using trait measurements to predict potential novel competitive interactions under climate change. However, future research is needed to predict the outcomes of these novel competitive interactions. Additionally, considering the relative fitness of the different trait values species may have, rather than trait values alone, would also be valuable for predicting competitive outcomes (Funk and Wolf 2016) for future predictive models of novel competitive pressures under climate change.

In summary, our study shows that bumble bee diet niche overlap increases with elevation, morphological and phenological traits (body size, tongue length, date of activity) are correlated with diet composition between bumble bee species, and the upward movement of bumble bees under climate change may lead to new pairs of species with very similar trait values, increasing the likelihood that they will have a similar diet at the mountaintop under climate change. The effects of climate change may be exacerbated by the movement of species to remain within habitable environmental conditions. Our findings highlight the utility of using species traits to predict expected novel competitive interactions under climate change.

Acknowledgments

We thank Andrew Gaier, Anna Paraskevopoulos, Asia Kaiser, Jess Mullins, Virginia Scott, Isabella Manning, Nicole Perez, and Chloe Sommer for their field and laboratory work contributions. We also thank Deane Bowers, Adrian Carper, and members of the Resasco lab for their feedback on this manuscript. We thank the United States Department of Agriculture Forest Service, The Pikes Peak Ranger District, and the City of Manitou Springs for permission for fieldwork.

Funding: This research was funded by the National Science Foundation (NSF-DEB 2102974) and National Geographic Explorer award to JR and a CanBee Cocktails grant to KB.

Conflicts of interest/Competing interests: The authors declare that they have no conflict of interest.

Ethics Approval: Not applicable

Consent to Participate: Not applicable

Consent for Publication: Not applicable

Availability of Data and Material: Data will be published to Dryad upon acceptance.

Code Availability:Code will be published to Dryad upon acceptance.

Author Contributions JR and KB formulated the study idea. JR and KB performed the data collection. KB analyzed the data and wrote the manuscript with intellectual guidance from JR.

Ackerfield J (2015) The Flora of Colorado, 4th edn. Lipscomb B. Botanical Research Institute of Texas, Fort Worth.
Alexander JM, Diez JM, Levine JM (2015) Novel competitors shape species' responses to climate change. Nature 525(7570): 515–518 doi:10.1038/nature14952
Balfour NJ, Shackleton K, Arscott NA, Roll-Baldwin K, Bracuti A, Toselli G, Ratnieks FL (2021) Energetic efficiency of foraging mediates bee niche partitioning. Ecology 102(4):e03285. doi:10.1002/ecy.3285
Bingham RA, Orthner AR (1998) Efficient pollination of alpine plants. Nature 391:238–239. doi:10.1038/34564
Brosi BJ, Niezgoda K, Briggs HM (2017) Experimental species removals impact the architecture of pollination networks. Biology Letters 13(6):20170243. doi:10.1098/rsbl.2017.0243
Burns JH, Strauss SY (2011) More closely related species are more ecologically similar in an experimental test. Proceedings of the National Academy of Sciences 108(13):5302-5307 doi:10.1098/rsbl.2017.0243
Byron PA (1980) On the Ecology and Systematics of Coloradan Bumblebees. PhD Dissertation, Department of Environmental, Population and Organismic Biology, University of Colorado, Boulder, Colorado, USA.
Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, Griswold, TL (2011) Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences 108(2):662-667 doi:10:1073/pnas.1014743108
Chesshire PR, McCabe LM, Cobb NS (2021) Variation in plant–pollinator network structure along the elevational gradient of the San Francisco Peaks, Arizona. Insects 12(12):1060 doi:10.3390/insects12121060
Chesson P (2000) Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31(2000): 343-366 doi:10.1146/annurev.ecolsys.31.1.343
Christmas MJ, Jones JC, Olsson A, Wallerman O, Bunikis I, Kierczak M, Whitley KM, Sullivan I, Geib JC, Miller-Struttmann NE, Webster, MT (2022) A genomic and morphometric analysis of alpine bumblebees: Ongoing reductions in tongue length but no clear genetic component. Molecular Ecology 31(4):1111-1127. doi:10.1111/mec.16291
Costa-Pereira R, Araújo MS, Souza FL, Ingram T (2019) Competition and resource breadth shape niche variation and overlap in multiple trophic dimensions. Proceedings of the Royal Society B 286(1902): 20190369. doi:10.1098/rspb.2019.0369
de Keyzer CW, Colla SR, Kent CF, Rafferty NE, Richardson LL, Thomson JD (2016) Delving deeper: questioning the decline of long-tongued bumble bees, long-tubed flowers and their mutualisms with climate change. Journal of Pollination Ecology, 18(6):36-42. doi:10.26786/1920-7603(2016)15
Dormann CF, Fründ J, Blüthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. The Open Ecology Journal 2(1):7-24 doi:10.2174/1874213000902010007
Doublet V, Doyle T, Refoy I, Hedges S, Carvell C, Brown MJ, Wilfert L (2022) Increasing flower species richness in agricultural landscapes alters insect pollinator networks: Implications for bee health and competition. Ecology and Evolution 12(10):e9442 doi:10.1002/ece3.9442
Funk JL, Wolf AA (2016) Testing the trait-based community framework: Do functional traits predict competitive outcomes? Ecology 97(9):2206–2211 doi: 10.1002/ecy.1484
Gallou A, Baillet Y, Ficetola GF, Després L (2017) Elevational gradient and human effects on butterfly species richness in the French Alps. Ecology and Evolution 7(11):3672-3681 doi:10.1002/ece3.2803
Gómez-Ruiz EP, Lacher Jr TE (2019) Climate change, range shifts, and the disruption of a pollinator-plant complex. Scientific Reports 9(1):14048 doi:10.1038/s41598-019-50059-6
Gorenflo A, Diekötter T, van Kleunen M, Wolters V, Jauker F (2017) Contrasting pollination efficiency and effectiveness among flower visitors of Malva sylvestris, Borago officinalis and Onobrychis viciifolia. Journal of Pollination Ecology 21(1):62-70 doi:10.26786/1920-7603(2017)421
Goulson D, Darvill B (2004) Niche overlap and diet breadth in bumblebees; are rare species more specialized in their choice of flowers? Apidologie 35(1):55-63 doi:10.1051/apido:2003062
Goulson D, Lye GC, Darvill B (2008) Diet breadth, coexistence and rarity in bumblebees. Biodiversity and Conservation 17(13):3269-3288 doi:10.1007/s10531-008-9428-y
Harder LD (1985) Morphology as a predictor of flower choice by bumble bees. Ecology 66(1):198-210 doi:10.2307/1941320
Hatfield R, Jepsen S, Thorp R, Richardson L, Colla S, Foltz Jordan S (2015a) Bombus pensylvanicus. The IUCN Red List of Threatened Species, 2015.
Hatfield R, Jepsen S, Thorp R, Richardson L, Colla S (2015b) Bombus sylvicola. The IUCN Red List of Threatened Species, 2015.
Heinrich B (1976) Resource partitioning among some eusocial insects: bumblebees. Ecology 57(5):874-889 doi:10.2307/1941054
Hollister J, Shah T, Robitaille A, Beck M, Johnson M (2021) elevatr: Access Elevation Data from Various APIs. R package version 0.4.2.
Horn HS (1966) Measurement of "overlap" in comparative ecological studies. The American Naturalist 100(914):419-424 doi:10.1086/282436
Hsieh TC, Ma KH, Chao A (2022) iNEXT: iNterpolation and EXTtrapolation for species diversity. R package version 3.0.0.
Hughes L (2000) Biological consequences of global warming: is the signal already apparent? Trends in Ecology & Evolution 15(2):56-61 doi:10.1016/s0169-5347(99)01764-4
Inouye DW (1978) Resource partitioning in bumblebees: experimental studies of foraging behavior. Ecology 59(4):672-678 doi:10.2307/1938769
Kahle D, & Wickham H (2013) ggmap: Spatial visualization with ggplot2. The R Journal 5(1):144-161.
Kelso T (2012) Peak to Prairie: Botanical landscapes of the Pikes Peak region. Colorado College.
Kerr JT, Pindar A, Galpern P, Packer L, Potts SG, Roberts SM, Rasmont P, Schweiger O, Colla SR, Richardson LL, Wagner DL, Gall LF, Sikes DS, Pantoja A (2015) Climate change impacts on bumblebees converge across continents. Science 349(6244):177-180 doi:10.1126/science.aaa7031
Kingsolver JG, Diamond SE, Buckley LB (2013) Heat stress and the fitness consequences of climate change for terrestrial ectotherms. Functional Ecology 27(6):1415-1423 doi:10.1111/1365-2435.12145
Körner C (2007) The use of ‘altitude’ in ecological research. Trends in Ecology & Evolution 22(11):569-574 doi:10.1016/j.tree.2007.09.006
Kosior A, Celary W, Olejniczak P, Fijał J, Król W, Solarz W, Płonka P (2007) The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx 41(1):79-88 doi:10.1017/S0030605307001597
Macior LW (1974) Pollination ecology of the front range of the Colorado Rocky Mountains. Melanderia 15:1-59.
Marshall L, Perdijk F, Dendoncker N, Kunin W, Roberts S, Biesmeijer JC (2020) Bumblebees moving up: shifts in elevation ranges in the Pyrenees over 115 years. Proceedings of the Royal Society B 287(1938): 20202201 doi:10.1098/rspb.2020.2201
McCain CM, Grytnes JA (2010) Elevational gradients in species richness. Encyclopedia of Life Sciences. doi:10.1002/9780470015902.a0022548
Michener CD (2007) The Bees of the World, 4th edn. Johns Hopkins University Press, Baltimore.
Miller-Struttmann NE, Galen C (2014) High-altitude multi-taskers: bumble bee food plant use broadens along an altitudinal productivity gradient. Oecologia 176:1033-1045 doi:10.1007/s00442-014-3066-8
Miller‐Struttmann N, Miller Z, Galen C (2022) Climate driven disruption of transitional alpine bumble bee communities. Global Change Biology 28(21):6165-6179 doi:10.1111/gcb.16348
Minachilis K, Kantsa A, Petanidou T (2021) Bumblebees, the proficient mountain pollinators: evidence from Stachys germanica (Lamiaceae) along the altitudinal gradient of Mount Olympus, Greece. Biological Journal of the Linnean Society 134(3):732-744 doi:10.1093/biolinnean/blab113
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MH (2020) Vegan: Community Ecology Package. R package version 2.5-7.
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120(3):321-326 doi:10.1111/j.1600-0706.2010.18644.x
Oyen KJ, Giri S, Dillon ME (2016) Altitudinal variation in bumble bee (Bombus) critical thermal limits. Journal of Thermal Biology 59:52-57 doi:10.1016/j.jtherbio.2016.04.015
Pyke GH, Thomson JD, Inouye DW, Miller TJ (2016) Effects of climate change on phenologies and distributions of bumble bees and the plants they visit. Ecosphere 7(3):e01267 doi:10.1002/ecs2.1267
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Richman SK, Levine JM, Stefan L, Johnson CA (2020) Asynchronous range shifts drive alpine plant–pollinator interactions and reduce plant fitness. Global Change Biology 26(5):3052-3064. doi:10.1111/gcb.15041
Soroye P, Newbold T, Kerr J (2020) Climate change contributes to widespread declines among bumble bees across continents. Science 367(6478):685–688 doi:10.1126/science.aax8591
Sponsler D, Kallnik K, Requier F, Classen A, Maihoff AF, Sieger J, Steffan‐Dewenter I (2022a) Floral preferences of mountain bumble bees are constrained by functional traits but flexible through elevation and season. Oikos 2022(3):e08902 doi:10.1111/oik.08902
Sponsler DB, Requier F, Kallnik K, Classen A, Maihoff F, Sieger J, Steffan‐Dewenter I (2022b) Contrasting patterns of richness, abundance, and turnover in mountain bumble bees and their floral hosts. Ecology 103(7):e3712 doi:10.1002/ecy.3712
Ștefan V, Knight TM (2023) bootstrapnet: Bootstrap Network Metrics. R package version 1.0.0.
Stephens RE, Sauquet H, Guerin GR, Jiang M, Falster D, Gallagher RV (2022) Climate shapes community flowering periods across biomes. Journal of Biogeography 49(7):1205-1218 doi:10.1111/jbi.14375
Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJ, Fromentin J, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416(6879):389-395 doi:10.1038/416389a
Wardle DA, Bardgett RD, Callaway RM, Van der Putten WH (2011) Terrestrial ecosystem responses to species gains and losses. Science 332(6035):1273-1277 doi:10.1126/science.119747
Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis, 2nd edn. Springer, New York. doi:10.1007/978-0-387-98141-3
Wilke CS (2022) ggridges: Ridgeline Plots in 'ggplot2'. R package version 0.5.4.
Williams P, Thorp R, Richardson L, Colla S (2014) The Bumblebees of North America. Princeton University Press, New Jersey.
Wohlgemuth T, Nobis MP, Kienast F, Plattner M (2008) Modeling vascular plant diversity at the landscape scale using systematic samples. Journal of Biogeography 35(7):1226-1240. doi:10.1111/j.1365-2699.2008.01884.x
Wright A, Boyd CL, Bowers MD, Scott VL (2017) The Bumble Bees of Colorado. Princeton University Press, Princeton.

FinalOecologiaElectronicSupplementalMaterials.docx

Download PDF

Version 1

posted

You are reading this latest preprint version

Bumble bee niche overlap along an elevation gradient: how traits can inform novel competitive pressures under climate change.

Status:

Version 1

Abstract

Figures

Introduction

Materials and methods

Study area

Study design

Statistical analysis

Assessing elevational patterns of species richness and sampling completeness

Q1: How does bumble bee diet niche overlap change along the elevation gradient?

Q2: Are phenology, body size, and tongue length correlated with bumble bee diet composition?

Results

Assessing elevational patterns of species richness and sampling completeness

Q1: How does bumble bee diet niche overlap change along the elevation gradient?

Q2: Are phenology, body size, and tongue length correlated with bumble bee diet composition?

Discussion

Overview

Assessing elevational patterns of species richness and sampling completeness

Q1: How does bumble bee diet niche overlap change along the elevation gradient?

Q2: Are phenology, body size, and tongue length correlated with bumble bee diet composition?

Conclusion

Declarations

References

Supplementary Files

Status:

Version 1