Polar Biology

, Volume 40, Issue 11, pp 2253–2263 | Cite as

The response of pollen-transport networks to landscape-scale climate variation

  • Christine Urbanowicz
  • Ross A. Virginia
  • Rebecca E. Irwin
Original Paper


Climate variation can have profound effects on the composition and diversity of species as well as species physiology and behavior. Such effects may have ramifications on the network structure of interacting species within a community. Our aim was to understand how landscape-scale variation in temperature and wind exposure influenced plant–pollinator diversity, composition, and network structure. We constructed pollen-transport networks at six sites along a temperature gradient in west Greenland. Half of these sites were naturally sheltered from katabatic winds, while the other half were exposed. At each site, we measured temperature, wind speed, and the presence of flowering plants. We netted insects and identified the insects and the pollen carried on their bodies. Network structure was quantified using connectance, nestedness, and specialization, three metrics related to the robustness of networks to environmental variation. We tested how temperature and wind speed affected the diversity and composition of insects, pollen, and plants flowering in sites, and network structure. Temperature zone and wind exposure did not explain variation in the richness, evenness, or abundance of insects or pollen, or the richness of plants flowering in sites. However, the composition of pollen and plants flowering in sites varied across temperature zones and levels of wind exposure. Despite the observed changes in pollen and plant community composition, we found that network connectance, nestedness, and specialization were unresponsive to landscape-scale variation in temperature and wind exposure. High generalization and opportunism among Arctic plants and pollinators may contribute to this lack of response.


Arctic Climate Connectance Nestedness Pollen-transport networks Pollination 



We thank members of the Irwin Lab for feedback on this manuscript and Ruth Heindel for field assistance. We also thank Polar Field Services for logistical support in the field. Funding was provided by a National Science Foundation (NSF) Graduate Research Fellowship and an NSF IGERT Grant (Award Number 0801490). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

Supplementary material

300_2017_2138_MOESM1_ESM.pdf (15 kb)
Supplementary material 1 (PDF 15 kb)
300_2017_2138_MOESM2_ESM.pdf (163 kb)
Supplementary material 2 (PDF 163 kb)
300_2017_2138_MOESM3_ESM.pdf (14 kb)
Supplementary material 3 (PDF 13 kb)
300_2017_2138_MOESM4_ESM.pdf (42 kb)
Supplementary material 4 (PDF 42 kb)


  1. Alarcón R (2010) Congruence between visitation and pollen-transport networks in a California plant–pollinator community. Oikos 119:35–44. doi: 10.1111/j.1600-0706.2009.17694.x CrossRefGoogle Scholar
  2. Alarcón R, Waser NM, Ollerton J (2008) Year-to-year variation in the topology of a plant–pollinator interaction network. Oikos 117:1796–1807. doi: 10.1111/j.0030-1299.2008.16987.x CrossRefGoogle Scholar
  3. Almeida-Neto M, Ulrich W (2011) A straightforward computational approach for measuring nestedness using quantitative matrices. Environ Model Softw 26:173–178. doi: 10.1016/j.envsoft.2010.08.003 CrossRefGoogle Scholar
  4. Almeida-Neto M, Guimarães P, Guimarães PR et al (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239. doi: 10.1111/j.0030-1299.2008.16644.x CrossRefGoogle Scholar
  5. Argus GW (1965) The taxonomy of the Salix glauca complex in North America. Contrib Gray Herb Harv Univ 1–142Google Scholar
  6. Armbruster WS, Herzig AL (1984) Partitioning and sharing of pollinators by four sympatric species of dalechampia (Euphorbiaceae) in Panama. Ann Mo Bot Gard 71:1–16. doi: 10.2307/2399053 CrossRefGoogle Scholar
  7. Arroyo MTK, Armesto JJ, Primack RB (1985) Community studies in pollination ecology in the high temperate Andes of central Chile II. Effect of temperature on visitation rates and pollination possibilities. Plant Syst Evol 149:187–203. doi: 10.1007/BF00983305 CrossRefGoogle Scholar
  8. Bartomeus I, Ascher JS, Wagner D et al (2011) Climate-associated phenological advances in bee pollinators and bee-pollinated plants. Proc Natl Acad Sci USA 108:20645–20649. doi: 10.1073/pnas.1115559108 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. Proc Natl Acad Sci 100:9383–9387. doi: 10.1073/pnas.1633576100 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Beckerman AP, Petchey OL, Warren PH (2006) Foraging biology predicts food web complexity. Proc Natl Acad Sci USA 103:13745–13749. doi: 10.1073/pnas.0603039103 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bergman P, Molau U, Holmgren B (1996) Micrometeorological impacts on insect activity and plant reproductive success in an alpine environment, Swedish Lapland. Arct Alp Res 28:196–202. doi: 10.2307/1551760 CrossRefGoogle Scholar
  12. Bersier L-F, Banašek-Richter C, Cattin M-F (2002) Quantitative descriptors of food-web matrices. Ecology 83:2394–2407. doi: 10.1890/0012-9658(2002)083[2394:QDOFWM]2.0.CO;2 CrossRefGoogle Scholar
  13. Blüthgen N (2010) Why network analysis is often disconnected from community ecology: a critique and an ecologist’s guide. Basic Appl Ecol 11:185–195. doi: 10.1016/j.baae.2010.01.001 CrossRefGoogle Scholar
  14. Blüthgen N, Klein A-M (2011) Functional complementarity and specialisation: the role of biodiversity in plant–pollinator interactions. Basic Appl Ecol 12:282–291. doi: 10.1016/j.baae.2010.11.001 CrossRefGoogle Scholar
  15. Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9. doi: 10.1186/1472-6785-6-9 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Blüthgen N, Menzel F, Hovestadt T et al (2007) Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol 17:341–346. doi: 10.1016/j.cub.2006.12.039 CrossRefPubMedGoogle Scholar
  17. Böcher J, Kristensen NP, Pape T, Vilhelmsen L (2015) The Greenland entomofauna: an identification manual of insects spiders and their allies. Brill, BostonGoogle Scholar
  18. 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. doi: 10.3732/ajb.1000391 CrossRefPubMedGoogle Scholar
  19. Burkle L, Irwin R (2009) The importance of interannual variation and bottom–up nitrogen enrichment for plant–pollinator networks. Oikos 118:1816–1829. doi: 10.1111/j.1600-0706.2009.17740.x CrossRefGoogle Scholar
  20. Carstensen DW, Sabatino M, Trøjelsgaard K, Morellato LPC (2014) Beta diversity of plant-pollinator networks and the spatial turnover of pairwise interactions. PLoS ONE. doi: 10.1371/journal.pone.0112903 Google Scholar
  21. Devoto M, Bailey S, Memmott J (2011) The “night shift”: nocturnal pollen-transport networks in a boreal pine forest. Ecol Entomol 36:25–35. doi: 10.1111/j.1365-2311.2010.01247.x CrossRefGoogle Scholar
  22. Dormann CF, Fründ J, Blüthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Accessed 12 Oct 2015
  23. Dupont YL, Padrón B, Olesen JM, Petanidou T (2009) Spatio-temporal variation in the structure of pollination networks. Oikos 118:1261–1269. doi: 10.1111/j.1600-0706.2009.17594.x CrossRefGoogle Scholar
  24. Forrest J, Inouye DW, Thomson JD (2010) Flowering phenology in subalpine meadows: does climate variation influence community co-flowering patterns? Ecology 91:431–440. doi: 10.1890/09-0099.1 CrossRefPubMedGoogle Scholar
  25. Fort H, Vázquez DP, Lan BL (2016) Abundance and generalisation in mutualistic networks: solving the chicken-and-egg dilemma. Ecol Lett 19:4–11. doi: 10.1111/ele.12535 CrossRefPubMedGoogle Scholar
  26. Forup ML, Henson KSE, Craze PG, Memmott J (2008) The restoration of ecological interactions: plant–pollinator networks on ancient and restored heathlands. J Appl Ecol 45:742–752. doi: 10.1111/j.1365-2664.2007.01390.x CrossRefGoogle Scholar
  27. Fulkerson JR, Whittall JB, Carlson ML (2012) Reproductive ecology and severe pollen limitation in the polychromic tundra plant, Parrya nudicaulis (Brassicaceae). PLoS ONE 7:e32790. doi: 10.1371/journal.pone.0032790 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Geological Survey of Denmark and Greenland (2014) PROMICE: programme for monitoring of the Greenland ice sheetGoogle Scholar
  29. Gibson RH, Knott B, Eberlein T, Memmott J (2011) Sampling method influences the structure of plant–pollinator networks. Oikos 120:822–831. doi: 10.1111/j.1600-0706.2010.18927.x CrossRefGoogle Scholar
  30. Gornish ES, Tylianakis JM (2013) Community shifts under climate change: mechanisms at multiple scales. Am J Bot 100:1422–1434. doi: 10.3732/ajb.1300046 CrossRefPubMedGoogle Scholar
  31. Gotelli NJ, Ellison AM (2004) A primer of ecological statistics. Sinauer Associates Publishers, SunderlandGoogle Scholar
  32. Hegland SJ, Nielsen A, Lázaro A et al (2009) How does climate warming affect plant-pollinator interactions? Ecol Lett 12:184–195. doi: 10.1111/j.1461-0248.2008.01269.x CrossRefPubMedGoogle Scholar
  33. Heinrich B (1975) Energetics of pollination. Annu Rev Ecol Syst 6:139–170. doi: 10.1146/ CrossRefGoogle Scholar
  34. Heinrich B, Raven PH (1972) Energetics and pollination ecology. Science 176:597–602. doi: 10.1126/science.176.4035.597 CrossRefPubMedGoogle Scholar
  35. Hodkinson ID (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev 80:489–513. doi: 10.1017/S1464793105006767 CrossRefPubMedGoogle Scholar
  36. Huang S-Q, Shi X-Q (2013) Floral isolation in pedicularis: how do congeners with shared pollinators minimize reproductive interference? New Phytol 199:858–865. doi: 10.1111/nph.12327 CrossRefPubMedGoogle Scholar
  37. Hurlbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586. doi: 10.2307/1934145 CrossRefPubMedGoogle Scholar
  38. Jordano P (1987) Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. Am Nat 129:657–677CrossRefGoogle Scholar
  39. Kearns CA (2001) North American dipteran pollinators: assessing their value and conservation status. Conserv Ecol 5:5CrossRefGoogle Scholar
  40. Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, BoulderGoogle Scholar
  41. Kearns CA, Inouye DW (1997) Pollinators, flowering plants, and conservation biology. BioScience 47:297–307CrossRefGoogle Scholar
  42. Kingston AB, McQuillan PB (2000) Are pollination syndromes useful predictors of floral visitors in Tasmania? Austral Ecol 25:600–609. doi: 10.1111/j.1442-9993.2000.tb00065.x CrossRefGoogle Scholar
  43. Lundgren R, Olesen JM (2005) The dense and highly connected world of Greenland’s plants and their pollinators. Arct Antarct Alp Res 37:514–520CrossRefGoogle Scholar
  44. McAlpine JF, Peterson BV, Shewell GE, et al (1981) Manual of Nearctic diptera, vol 1, Monograph 27. Agriculture Canada, OttawaGoogle Scholar
  45. Moeller DA, Geber MA, Eckhart VM, Tiffin P (2011) Reduced pollinator service and elevated pollen limitation at the geographic range limit of an annual plant. Ecology 93:1036–1048. doi: 10.1890/11-1462.1 CrossRefGoogle Scholar
  46. Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405CrossRefGoogle Scholar
  47. Morris RJ (2010) Anthropogenic impacts on tropical forest biodiversity: a network structure and ecosystem functioning perspective. Philos Trans R Soc Lond B Biol Sci 365:3709–3718. doi: 10.1098/rstb.2010.0273 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Morris RJ, Gripenberg S, Lewis OT, Roslin T (2014) Antagonistic interaction networks are structured independently of latitude and host guild. Ecol Lett 17:340–349. doi: 10.1111/ele.12235 CrossRefPubMedGoogle Scholar
  49. Mu J, Peng Y, Xi X et al (2015) Artificial asymmetric warming reduces nectar yield in a Tibetan alpine species of Asteraceae. Ann Bot 116:899–906. doi: 10.1093/aob/mcv042 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Murcia C (1990) Effect of floral morphology and temperature on pollen receipt and removal in Ipomoea trichocarpa. Ecology 71:1098–1109. doi: 10.2307/1937378 CrossRefGoogle Scholar
  51. Nielsen A, Bascompte J (2007) Ecological networks, nestedness and sampling effort. J Ecol 95:1134–1141. doi: 10.1111/j.1365-2745.2007.01271.x CrossRefGoogle Scholar
  52. Oksanen J, Blanchet FG, Kindt R, et al (2015) Package “vegan”: Community Ecology PackageGoogle Scholar
  53. Olesen JM, Jordano P (2002) Geographic patterns in plant-pollinator mutualistic networks. Ecology 83:2416–2424. doi: 10.1890/0012-9658(2002)083[2416:GPIPPM]2.0.CO;2 Google Scholar
  54. Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc Natl Acad Sci 104:19891–19896. doi: 10.1073/pnas.0706375104 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Olesen JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89:1573–1582. doi: 10.1890/07-0451.1 CrossRefPubMedGoogle Scholar
  56. Ollerton J, Cranmer L (2002) Latitudinal trends in plant-pollinator interactions: are tropical plants more specialised? Oikos 98:340–350. doi: 10.1034/j.1600-0706.2002.980215.x CrossRefGoogle Scholar
  57. Petanidou T, Kallimanis AS, Tzanopoulos J et al (2008) Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecol Lett 11:564–575. doi: 10.1111/j.1461-0248.2008.01170.x CrossRefPubMedGoogle Scholar
  58. Pinheiro J, Bates D, DebRoy S, Sarkar D (2014) R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1-117Google Scholar
  59. Potts SG, Vulliamy B, Dafni A et al (2003) Linking bees and flowers: how do floral communities structure pollinator communities? Ecology 84:2628–2642. doi: 10.1890/02-0136 CrossRefGoogle Scholar
  60. Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber Press, Portland, ORGoogle Scholar
  61. Rader R, Edwards W, Westcott DA, Cunningham SA, Howlett BG (2011) Pollen transport differs among bees and flies in a human-modified landscape. Divers Distrib 17:519–529CrossRefGoogle Scholar
  62. Rasmussen C, Dupont YL, Mosbacher JB et al (2013) Strong impact of temporal resolution on the structure of an ecological network. PLoS ONE 8:e81694. doi: 10.1371/journal.pone.0081694 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Scaven VL, Rafferty NE (2013) Physiological effects of climate warming on flowering plants and insect pollinators and potential consequences for their interactions. Curr Zool 59:418–426CrossRefPubMedPubMedCentralGoogle Scholar
  64. Schleuning M, Fründ J, Klein A-M et al (2012) Specialization of mutualistic interaction networks decreases toward tropical latitudes. Curr Biol 22:1925–1931. doi: 10.1016/j.cub.2012.08.015 CrossRefPubMedGoogle Scholar
  65. Stang M, Klinkhamer PGL, Van Der Meijden E (2006) Size constraints and flower abundance determine the number of interactions in a plant–flower visitor web. Oikos 112:111–121. doi: 10.1111/j.0030-1299.2006.14199.x CrossRefGoogle Scholar
  66. Strona G, Fattorini S (2014) On the methods to assess significance in nestedness analyses. Theory Biosci Theor Den Biowissenschaften 133:179–186. doi: 10.1007/s12064-014-0203-1 CrossRefGoogle Scholar
  67. Tiusanen M, Hebert PDN, Schmidt NM, Roslin T (2016) One fly to rule them all—muscid flies are the key pollinators in the Arctic. Proc R Soc B 283:20161271. doi: 10.1098/rspb.2016.1271 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Totland Ø (1994) Influence of climate, time of day and season, and flower density on insect flower visitation in alpine Norway. Arct Alp Res 26:66–71. doi: 10.2307/1551879 CrossRefGoogle Scholar
  69. Tur C, Vigalondo B, Trøjelsgaard K et al (2014) Downscaling pollen–transport networks to the level of individuals. J Anim Ecol 83:306–317. doi: 10.1111/1365-2656.12130 CrossRefPubMedGoogle Scholar
  70. Tylianakis JM (2013) The global plight of pollinators. Science 339:1532–1533. doi: 10.1126/science.1235464 CrossRefPubMedGoogle Scholar
  71. Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445:202–205. doi: 10.1038/nature05429 CrossRefPubMedGoogle Scholar
  72. Ulrich W, Almeida-Neto M, Gotelli NJ (2009) A consumer’s guide to nestedness analysis. Oikos 118:3–17. doi: 10.1111/j.1600-0706.2008.17053.x CrossRefGoogle Scholar
  73. Vázquez DP, Aizen MA (2003) Null model analyses of specialization in plant–pollinator interactions. Ecology 84:2493–2501. doi: 10.1890/02-0587 CrossRefGoogle Scholar
  74. Vázquez DP, Melián CJ, Williams NM et al (2007) Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–1127. doi: 10.1111/j.0030-1299.2007.15828.x CrossRefGoogle Scholar
  75. Vázquez DP, Blüthgen N, Cagnolo L, Chacoff NP (2009) Uniting pattern and process in plant–animal mutualistic networks: a review. Ann Bot 103:1445–1457. doi: 10.1093/aob/mcp057 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Vicens N, Bosch J (2000) Weather-dependent pollinator activity in an apple orchard, with special reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae). Environ Entomol 29:413–420. doi: 10.1603/0046-225X-29.3.413 CrossRefGoogle Scholar
  77. Waser NM, Chittka L, Price MV et al (1996) Generalization in pollination systems, and why it matters. Ecology 77:1043–1060. doi: 10.2307/2265575 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of BiologyDartmouth CollegeHanoverUSA
  2. 2.Environmental Studies ProgramDartmouth CollegeHanoverUSA
  3. 3.Department of Applied EcologyNorth Carolina State UniversityRaleighUSA

Personalised recommendations