Abstract
We use an extensive historical data set on bumble bee host choice collected almost 50 years ago by L. W. Macior (Melanderia 15:1–59, 1974) to examine how resource partitioning by bumble bees varies over a 2,700-m altitudinal gradient at four hierarchical scales: individual, colony, species and community. Bumble bee behavior, resource overlap between castes, and plant-bumble bee networks change with altitude in accordance with tightening temporal constraints on flowering and colony growth in alpine habitats. Individual bees were more likely to collect pollen from multiple sources at high altitude. Between-caste foraging niche overlap increased with altitude. Similarly, alpine forager networks were more highly nested than either subalpine or montane networks due to increased asymmetric specialization. However, interspecific resource partitioning showed a more complex spatial pattern with low niche overlap at intermediate altitude (subalpine) compared to montane (disturbed) and alpine (unproductive) sites. Results suggest that spatial variation in interspecific resource partitioning is driven by a shift in the behavior of long-tongued bumble bees. Long-tongued bumble bees specialized in the subalpine but generalized in montane and alpine zones. Our reanalysis of Macior’s data shows that bumble bee behavior varies substantially with altitude influencing plant-bumble bee interaction networks. Results imply that pollination services to alpine host plants will change dramatically as subalpine species with unique foraging strategies move upward under global warming.
This is a preview of subscription content, access via your institution.





References
Ahrné K, Bengtsson J, Elmqvist T (2009) Bumble bees (Bombus spp.) along a gradient of increasing urbanization. PLoS ONE 4:e5574
Alarcón R, Waser NM, Ollerton J (2008) Year-to-year variation in the topology of a plant-pollinator interaction network. Oikos 117:1796–1807
Aldridge G, Inouye DW, Forrest JRK, Barr WA, Miller-Rushing AJ (2011) Emergence of a mid-season period of low floral resources in a montane meadow ecosystem associated with climate change. J Ecol 99:905–913
Arceo-Gómez G, Ashman TL (2011) Heterospecific pollen deposition: does diversity alter the consequences? New Phytol 192:738–746
Ashman TL, Arceo-Gómez G (2013) Toward a predictive understanding of the fitness costs of heterospecific pollen receipt and its importance in co-flowering communities. Am J Bot 100:1061–1070
Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, Butterfield J, Buse A, Coulson JC, Farrar J, Good JEG, Harrington R, Hartley S, Jones TH, Lindroth RL, Press MC, Symrnioudis I, Watt AD, Whittaker JB (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16
Bascompte J (2009) Mutualistic networks. Front Ecol Environ 7:429–436
Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593
Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Natl Acad Sci 100:9383–9387
Bates D, Maechler M, Bolker BM (2011) lme4: linear mixed-effects models using S4 classes
Bell JM, Karron JD, Mitchell RJ (2005) Interspecific competition for pollination lowers seed production and outcrossing in Mimulus ringens. Ecology 86:762–771
Beniston M, Diaz HF, Bradley RS (1997) Climatic change at high elevation sites: an overview. Clim Change 36:233–251
Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BioMed Centr Ecol 6:9
Brock MT (2009) Prezygotic barriers to gene flow between Taraxacum ceratophorum and the invasive Taraxacum officinale (Asteraceae). Oecologia 161:241–251
Burgos E, Ceva H, Perazzo RPJ, Devoto M, Medan D, Zimmermann M, María Delbue A (2007) Why nestedness in mutualistic networks? J Theor Biol 249:307–313
Burkle LA, Alarcón R (2011) The future of plant-pollinator diversity: understanding interaction networks across time, space, and global change. Am J Bot 98:528–538
Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence and function. Science 339:1611–1615
Byron PA (1980) On the ecology and systematics of Coloradan bumble bees. Ph.D. thesis, University of California
CaraDonna PJ, Iler AM, Inouye DW (2014) Shifts in flowering phenology reshape a subalpine plant community. Proc Natl Acad Sci A:1–6
Charnov EL (1976) Optimal foraging, the marginal value theorem. Theor Popul Biol 2:129–136
Collinge SK, Prudic KL, Oliver JC (2003) Effects of local habitat characteristics and landscape context on grassland butterfly diversity. Conserv Biol 17:178–187
Dalsgaard B, Magård E, Fjeldså J, Martín González AM, Rahbek C, Olesen JM, Ollerton J, Alarcón R, Cardoso Araujo A, Cotton PA, Lara C, Machado CG, Sazima I, Sazima M, Timmermann A, Watts S, Sandel B, Sutherland WJ, Svenning JC (2011) Specialization in plant-hummingbird networks is associated with species richness, contemporary precipitation and quaternary climate-change velocity. PLoS ONE 6:e25891
Dormann CF (2011) How to be a specialist? Quantifying specialisation in pollination networks. Network 1:1–20
Dormann CF, Gruber B (2011) Bipartite: visualising bipartite networks and calculating some (ecological) indices
Dupont YL, Padrón B, Olesen JM, Petanidou T (2009) Spatio-temporal variation in the structure of pollination networks. Oikos 118:1261–1269
Elliott SE (2009) Surplus nectar available for subalpine bumble bee colony growth. Environ Entomol 38:1680–1689
Fang Q, Huang SQ (2012) Relative stability of core groups in pollination networks in a biodiversity hotspot over four years. PLoS ONE 7:e32663
Fang Q, Huang SQ (2013) A directed network analysis of heterospecific pollen transfer in a biodiverse community. Ecology 94:1176–1185
Flanagan RJ, Mitchell RJ, Knutowski D, Karron JD (2009) Interspecific pollinator movements reduce pollen deposition and seed production in Mimulus ringens (Phrymaceae). Am J Bot 96:809–815
Flanagan RJ, Mitchell RJ, Karron JD (2011) Effects of multiple competitors for pollination on bumblebee foraging patterns and Mimulus ringens reproductive success. Oikos 120:200–207
Forrest J, Inouye DW, Thomson JD (2010) Flowering phenology in subalpine meadows: does climate variation influence community co-flowering patterns? Ecology 91:431–440
Fox J, Weisberg S, Hong J, Anderson R, Firth D, Friendly M, Taylor S (2013) Effects: effect displays for linear, generalized linear, multinomial-logit, proportional-odds logit models and mixed-effects models
Galeano J, Pastor JM, Iriondo JM (2009) Weighted-Interaction Nestedness Estimator (WINE): a new estimator to calculate over frequency matrices. Environ Model Softw 24:1342–1346
Galen C (1999) Why do flowers vary? Bioscience 49:631–640
Galen C (2005) It never rains but then it pours: the diverse effects of water on flowering integrity and function. In: Reekie EG, Bazzaz FA (eds) Reproductive allocation in plants. Elsevier, San Diego, pp 77–92
Galen C, Gregory T (1989) Interspecific pollen transfer as a mechanism of competition: consequences of foreign pollen contamination for seed set in the alpine wildflower, Polemonium viscosum. Ecology 81:120–123
Geib JC, Galen C (2012) Tracing impacts of partner abundance in facultative pollination mutualisms: from individuals to populations. Ecology 93:1581–1592
Gomez JM, Perfectti F, Jordano P (2011) The functional consequences of mutualistic network architecture. PLoS ONE 6:e16143
Goulson D (2003) Bumble bees; their behavior and ecology. Oxford University Press, Oxford
Hagbery J, Nieh JC (2012) Individual lifetime pollen and nectar foraging preferences in bumble bees. Naturwissenschaften 99:821–832
Hodkinson ID (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev 80:489–513
Hothorn T, Bretz F, Westfal P (2012) multcomp: simultaneous inference in general parametric models
Inouye D (1977) Species structure of bumblebee communities in North America and Europe. In: Mattson W (ed) The role of arthropods in forest ecosystems. Springer, Berlin, pp 35–40
Inouye DW (1978) Resource partitioning in bumblebees: experimental studies of foraging behavior. Ecology 59:672–678
Inouye DW (1980) The effect of proboscis and corolla tube lengths on patterns and rates of flower visitation by bumblebees. Oecologia 45:197–201
Jakobsson A, Lázaro A, Totland O (2009) Relationships between the floral neighborhood and individual pollen limitation in two self-incompatible herbs. Oecologia 160:707–719
Johnson DR, Ebert-May D, Webber PJ, Tweedie CE (2011) Forecasting alpine vegetation change using repeat sampling and a novel modeling approach. Ambio 40:693–704
Kameyama Y, Kasagi T, Kudo G (2008) A hybrid zone dominated by fertile F1s of two alpine shrub species, Phyllodoce caerulea and Phyllodoce aleutica, along a snowmelt gradient. J Evol Biol 21:588–597
Kaspari M (2001) Taxonomic level, trophic biology and the regulation of local abundance. Glob Ecol Biogeogr 10:229–244
Kaspari M, Donnell SO, Kercher JR, Kaspari M, Donnell SO, Kercher JR (2000) Energy, density, and constraints to species richness: ant assemblages along a productivity gradient. Am Nat 155:280–293
Kearns CA, Oliveras DM (2009) Boulder County bees revisited: a resampling of Boulder Colorado bees a century later. J Insect Conserv 13:603–613
Kendall WD (2002) A brief economic history of Colorado. Prepared for the demography section, Colorado Department of Local Affairs. Center for Business and Economic Forcasting. Available at: http://cospl.coalliance.org/fedora/repository/co:3222/loc61502ec72002internet.pdf. (Last accessed 11-26-13)
Knee WJ, Medler JT (1965) Seasonal size increase of bumblebee workers (Hymenoptera-Bombus). Can Entomol 97:1149–1155
Körner C (2007) The use of “altitude” in ecological research. Trends Ecol Evol 22:569–574
Kudo G, Suzuki S (1999) Flowering phenology of alpine plant communities along a gradient of snowmelt timing. Polar Biosci 12:100–113
Levins R (1968) Evolution in changing environments: some theoretical explorations. Princeton University Press, Princeton
Lopezaraiza-Mikel ME, Hayes RB, Whalley MR, Memmott J (2007) The impact of an alien plant on a native plant-pollinator network: an experimental approach. Ecol Lett 10:539–550
Macior LW (1974) Pollination ecology of the front range of the Colorado Rocky Mountains. Melanderia 15:1–59
Mello MAR, Santos GMDM, Mechi MR, Hermes MG (2011) High generalization in flower-visiting networks of social wasps. Acta Oecol 37:37–42
Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc R Soc Lond Biol Sci 271:2605–2611
Miller-Rushing AJ, Inouye DW (2009) Variation in the impact of climate change on flowering phenology and abundance: an examination of two pairs of closely related wildflower species. Am J Bot 96:1821–1829
Moeller DA (2004) Facultative interactions among plants via shared pollinators. Ecology 85:3289–3301
Morales CL, Traveset A (2008) Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. Crit Rev Plant Sci 27:221–238
Namgail T, Rawat GS, Mishra C, Van Wieren SE, Prins HHT (2012) Biomass and diversity of dry alpine plant communities along altitudinal gradients in the Himalayas. J Plant Res 125:93–101
Norberg J, Urban MC, Vellend M, Klausmeier CA, Loeuille N (2012) Eco-evolutionary responses of biodiversity to climate change. Nat Clim Change 2:747–751
Obeso JR (1992) Geographic distribution and community structure of bumble bees in the northern Iberian peninsula. Oecologia 89:244–252
Olesen JM, Jordano P (2002) Geographic patterns in plant-polliantor mutualistic networks. Ecology 83:2416–2424
Olesen JM, Eskildsen LI, Venkatasamy S (2002) Invasion of pollination networks on oceanic islands: importance of invader complexes and endemic super generalists. Divers Distrib 8:181–192
Olesen JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89:1573–1582
Ollerton J, Cranmer L (2002) Latitudinal trends in plant-pollinator interactions: are tropical plants more specialised? Oikos 98:340–350
Pato J, Ramón Obeso J (2012) Growth and reproductive performance in bilberry (Vaccinium myrtillus) along an elevation gradient. Ecoscience 19:59–68
Pederson GT, Betancourt JL, McCabe GJ (2013) Regional patterns and proximal causes of the recent snowpack decline in the Rocky Mountains, USA. Geophys Res Lett 40:1–6
Pianka ER (1973) The structure of lizard communities. Annu Rev Ecol Syst 4:53–74
Pineiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2011) nlme: linear and nonlinear mixed effects models
Plowright RC, Jay SC (1968) Caste differentiation in bumblebees (Bombus LTAR.: HYM.). I. The determination of female size. Insect Soc 15:171–192
Popic TJ, Wardle GM, Davila YC (2013) Flower-visitor networks only partially predict the function of pollen transport by bees. Austral Ecol 38:76–86
Pyke GH (1982) Local geographic distributions of bumblebees near Crested Butte, Colorado: competition and community. Ecology 63:555–573
Pyke GH, Inouye DW, Thomson JD (2011) Activity and abundance of bumble bees near Crested Butte, Colorado: diel, seasonal, and elevation effects. Ecol Entomol 36:511–521
Pyke GH, Inouye DW, Thomson JD (2012) Local geographic distributions of bumble bees near Crested Butte, Colorado: competition and community structure revisited. Environ Entomol 41:1332–1349
R Development Core Team (2011) R: a language and environment for statistical computing
Ramos-Jiliberto R, Domínguez D, Espinoza C, Lopez G, Valdovinos FS, Bustamante RO, Medel R (2010) Topological change of Andean plant–pollinator networks along an altitudinal gradient. Ecol Complex 7:86–90
Rosenzweig C, Casassa G, Karoly DJ, Imeson A, Liu C, Menzel A, Rawlings S, Root TL, Seguin B, Tryjanowiski P (2007) Climate change 2007: impacts, adaptation and vulnerability. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) Contributions of Working Group II to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 79–131
Scaven VL, Rafferty NE (2013) Physiological effects of climate warming on flowering plants and insect pollinators and potential consequences for their interactions. Curr Zool 59:418–426
Schleuning M, Fründ J, Klein A-M, Abrahamczyk S, Alarcón R, Albrecht M, Andersson GKS, Bazarian S, Böhning-Gaese K, Bommarco R, Dalsgaard B, Dehling DM, Gotlieb A, Hagen M, Hickler T, Holzschuh A, Kaiser-Bunbury CN, Kreft H, Morris RJ, Sandel B, Sutherland WJ, Svenning J-C, Tscharntke T, Watts S, Weiner CN, Werner M, Williams NM, Winqvist C, Dormann CF, Blüthgen N (2012) Specialization of mutualistic interaction networks decreases toward tropical latitudes. Curr Biol 22:1925–1931
Shpigler H, Tamarkin M, Gruber Y, Poleg M, Siegel AJ, Bloch G (2013) Social influences on body size and developmental time in the bumblebee Bombus terrestris. Behav Ecol Sociobiol 67:1601–1612
Smith JG, Sconiers W, Spasojevic MJ, Ashton IW, Suding KN (2012) Phenological changes in alpine plants in response to increased snowpack, temperature, and nitrogen. Arct Antarct Alp Res 44:135–142
Spaethe J, Weidenmüller A (2002) Size variation and foraging rate in bumblebees (Bombus terrestris). Insect Soc 49:142–146
Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235–246
Thomson J (2003) When is it mutualism? Am Nat 162:S1–S9
Trøjelsgaard K, Olesen JM (2013) Macroecology of pollination networks. Glob Ecol Biogeogr 22:149–162
Vázquez DP, Morris WF, Jordano P (2005) Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol Lett 8:1088–1094
Wheeler B (2010) lmPerm: Permutation tests for linear models
Wyka T, Galen C (2000) Current and future costs of reproduction in Oxytropis sericea, a perennial plant from the Colorado Rocky Mountains, USA. Antarctic Alpine Res 32:438–448
Acknowledgments
We acknowledge L. Walter Macior for his meticulous contributions to the understanding of Rocky Mountain bumble bees and their food plants. We thank R. Holdo for advice on implementing the network analyses in R Statistical Software. Anonymous reviewers were especially helpful in improving the manuscript. This research was supported with funding from NSF grant 1045322.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Christina Marie Caruso.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Miller-Struttmann, N.E., Galen, C. High-altitude multi-taskers: bumble bee food plant use broadens along an altitudinal productivity gradient. Oecologia 176, 1033–1045 (2014). https://doi.org/10.1007/s00442-014-3066-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-014-3066-8
Keywords
- Alpine bumble bees
- Niche partitioning
- Generalization
- Productivity
- Bombus