Humming along or buzzing off? The elusive consequences of plant-pollinator mismatches

Authors

  • Jason Ryan Straka University of Victoria
  • Brian M. Starzomski University of Victoria

DOI:

https://doi.org/10.26786/1920-7603(2014)18

Abstract

Temporal mismatches among plants and pollinators, driven by climate change, are considered a potential cause of population declines of these mutualists. However, field studies demonstrating population declines as a result of climate-driven phenological mismatches are uncommon, and the extent to which mismatches will be a problem in the future remains unclear. We revisit predicted consequences of climate-driven phenological mismatch in plant-pollinator systems by identifying nine previously-applied assumptions that are violated or insufficiently understood in real systems. Briefly, the assumptions are: (1) Dates of first-flowering (DFF) or dates of first activity (DFA) correctly describe phenology, and disparities between DFF and DFA represent the magnitude of mismatch. (2) “Optimal” matches are measured correctly. (3) Advancement of DFF or DFA will be the primary phenological change in the future. (4) Future phenological shifts will be independent for each species. (5) All plant-pollinator interactions are equally effective. (6) Populations of plants and pollinators are limited by mutualistic interactions. Some previous models have also assumed that the effects of future mismatches will not be influenced by (7) emergence of novel interactions, (8) competition or facilitation from altered co-flowering and co-flight, and (9) phenotypic plasticity and rapid adaptive evolution of phenology. Those assumptions affect the direction, extent, and accuracy of predicted consequences of future phenological mismatch. In discussing them, we identify important topics for future research in pollination ecology.

Author Biographies

Jason Ryan Straka, University of Victoria

Graduate student, School of Environmental Studies

Brian M. Starzomski, University of Victoria

Assistant Professor, School of Environmental Studies

References

Ackerman JD (1989) Limitations to sexual reproduction in Encyclia krugii (Orchidaceae). Systematic Botany 14:101–109. DOI: https://doi.org/10.2307/2419054

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. Journal of Ecology 99:905–913. DOI: https://doi.org/10.1111/j.1365-2745.2011.01826.x

Altermatt F (2010a) Climatic warming increases voltinism in European butterflies and moths. Proceedings of the Royal Society B: Biological Sciences 277:1281 –1287. DOI: https://doi.org/10.1098/rspb.2009.1910

Altermatt F (2010b) Tell me what you eat and I’ll tell you when you fly: diet can predict phenological changes in response to climate change. Ecology Letters 13:1475–1484. DOI: https://doi.org/10.1111/j.1461-0248.2010.01534.x

Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: Ecological and evolutionary causes and consequences. Ecology 85:2408–2421. DOI: https://doi.org/10.1890/03-8024

Augspurger CK (1981) Reproductive synchrony of a tropical shrub: experimental studies on effects of pollinators and seed predators in Hybanthus prunifolius (Violaceae). Ecology 62:775–788. DOI: https://doi.org/10.2307/1937745

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. Global Change Biology 8:1–16. DOI: https://doi.org/10.1046/j.1365-2486.2002.00451.x

Bartomeus I, Ascher JS, Gibbs J, Danforth BN, Wagner DL, Hedtke S & Winfree R (2013a) Historical changes in northeastern US bee pollinators related to shared ecological traits. Proceedings of the National Academy of Sciences 110:4656–4660. DOI: https://doi.org/10.1073/pnas.1218503110

Bartomeus I, Ascher JS, Wagner D, Danforth BN, Colla S, Kornbluth S, Winfree R (2011) Climate-associated phenological advances in bee pollinators and bee-pollinated plants. Proceedings of the National Academy of Sciences 108:20645–20649. DOI: https://doi.org/10.1073/pnas.1115559108

Bartomeus I, Park MG, Gibbs J, Danforth BN, Lakso AN, Winfree R (2013b) Biodiversity ensures plant–pollinator phenological synchrony against climate change. Ecology Letters 16:1331–1338. DOI: https://doi.org/10.1111/ele.12170

Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. Proceedings of the National Academy of Sciences of the United States of America 100:9383–9387. DOI: https://doi.org/10.1073/pnas.1633576100

Bazzaz FA (1990) The response of natural ecosystems to the rising global CO2 levels. Annual Review of Ecology and Systematics 21:167–196. DOI: https://doi.org/10.1146/annurev.ecolsys.21.1.167

Bender EA, Case TJ, Gilpin ME (1984) Perturbation experiments in community ecology: theory and practice. Ecology 65:1–13. DOI: https://doi.org/10.2307/1939452

Berenbaum M, Bernhardt P, Buchmann S, Calderone N, Goldstein P, Inouye DW, Kevan P, Kremen C, Medellin RA, Ricketts T (2007) Status of pollinators in North America. The National Academies Press, Washington, DC.

Berg MP, Kiers ET, Driessen G, van der Heijden M, Kooi BOB., Kuenen F, Liefting M, Verhoef HA, Ellers J (2010) Adapt or disperse: understanding species persistence in a changing world. Global Change Biology 16:587–598. DOI: https://doi.org/10.1111/j.1365-2486.2009.02014.x

Bond WJ (1994) Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Philosophical Transactions: Biological Sciences 344:83–90. DOI: https://doi.org/10.1098/rstb.1994.0055

Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83. DOI: https://doi.org/10.1038/nature04539

Bowers MA (1985) Bumble bee colonization, extinction, and reproduction in subalpine meadows in northeastern Utah. Ecology 66:914–927. DOI: https://doi.org/10.2307/1940554

Bowers MA (1986) Resource availability and timing of reproduction in bumble bee colonies (Hymenoptera: Apidae). Environmental Entomology 15:750–755. DOI: https://doi.org/10.1093/ee/15.3.750

Brosi BJ, Briggs HM (2013) Single pollinator species losses reduce floral fidelity and plant reproductive function. Proceedings of the National Academy of Sciences. In press. DOI: https://doi.org/10.1073/pnas.1307438110

Brown JH, Kodric-Brown A. 1979. Convergence, competition and mimicry in a temperate community of hummingbird pollinated plants. Ecology 60: 1022-35 DOI: https://doi.org/10.2307/1936870

Burd M (1994) Bateman’s principle and plant reproduction: The role of pollen limitation in fruit and seed set. The Botanical Review 60:83–139. DOI: https://doi.org/10.1007/BF02856594

Cartar RV, Dill LM (1990) Colony energy requirements affect the foraging currency of bumble bees. Behavioral Ecology and Sociobiology 27:377–383. DOI: https://doi.org/10.1007/BF00164009

Chagnon M, Ingras J, de Oliveira D (1993) Complementary aspects of strawberry pollination by honey and indigenous bees (Hymenoptera). Journal of Economic Entomology 86:416-420 DOI: https://doi.org/10.1093/jee/86.2.416

Cleland EE, Allen JM, Crimmins TM, Dunne JA, Pau S, Travers SE, Zavaleta ES, Wolkovich EM (2012) Phenological tracking enables positive species responses to climate change. Ecology 93:1765–1771. DOI: https://doi.org/10.1890/11-1912.1

Cook BI, Wolkovich EM, Parmesan C (2012) Divergent responses to spring and winter warming drive community level flowering trends. Proceedings of the National Academy of Sciences 109:9000–9005. DOI: https://doi.org/10.1073/pnas.1118364109

Cushing DH (1990) Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Advances in Marine Biology 26:249–293. DOI: https://doi.org/10.1016/S0065-2881(08)60202-3

Dafni A, Kevan PG, Husband BC (2005) Practical pollination biology. xv + 590 pp.

Davis CC, Willis CG, Primack RB, Miller-Rushing AJ (2010) The importance of phylogeny to the study of phenological response to global climate change. Philosophical Transactions of the Royal Society B: Biological Sciences 365:3201–3213. DOI: https://doi.org/10.1098/rstb.2010.0130

Diez JM, Ibáñez I, Miller-Rushing AJ, Mazer SJ, Crimmins TM, Crimmins MA, Bertelsen CD, Inouye DW (2012) Forecasting phenology: from species variability to community patterns. Ecology Letters 15:545–553. DOI: https://doi.org/10.1111/j.1461-0248.2012.01765.x

Donnelly A, Caffarra A, O’Neill BF (2011) A review of climate-driven mismatches between interdependent phenophases in terrestrial and aquatic ecosystems. International Journal of Biometeorology 55:805–817. DOI: https://doi.org/10.1007/s00484-011-0426-5

Doorn WG van (1997) Effects of pollination on floral attraction and longevity. Journal of Experimental Botany 48:1615–1622. DOI: https://doi.org/10.1093/jexbot/48.314.1615

Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecological Monographs 73:69–86. DOI: https://doi.org/10.1890/0012-9615(2003)073[0069:SMFPRT]2.0.CO;2

Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884. DOI: https://doi.org/10.1038/nature02808

Ehrlén J (1992) Proximate limits to seed production in a herbaceous perennial legume, Lathyrus vernus. Ecology 73:1820–1831. DOI: https://doi.org/10.2307/1940033

Eickwort GC, Ginsberg HS (1980) Foraging and mating behavior in Apoidea. Annual Review of Entomology 25:421–446. DOI: https://doi.org/10.1146/annurev.en.25.010180.002225

Ellwood E, Diez J, Ibáñez I, Primack R, Kobori H, Higuchi H, Silander J (2012) Disentangling the paradox of insect phenology: are temporal trends reflecting the response to warming? Oecologia 168:1161–1171. DOI: https://doi.org/10.1007/s00442-011-2160-4

Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British Plants. Science 296:1689–1691. DOI: https://doi.org/10.1126/science.1071617

Forrest J (2011) Plant-pollinator interactions in a changing climate. PhD Dissertation. [online] URL:http://hdl.handle.net

/1807/29723.

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: https://doi.org/10.1890/09-0099.1

Forrest J, Miller-Rushing AJ (2010) Toward a synthetic understanding of the role of phenology in ecology and evolution. Philosophical Transactions of the Royal Society B: Biological Sciences 365:3101 –3112. DOI: https://doi.org/10.1098/rstb.2010.0145

Forrest J, Thomson JD (2010) Consequences of variation in flowering time within and among individuals of Mertensia fusiformis (Boraginaceae), an early spring wildflower. American Journal of Botany 97:38–48. DOI: https://doi.org/10.3732/ajb.0900083

Forrest JR., Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecological Monographs 81:469–491. DOI: https://doi.org/10.1890/10-1885.1

Franks SJ, Sim S, Weis AE (2007) Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proceedings of the National Academy of Sciences 104:1278–1282. DOI: https://doi.org/10.1073/pnas.0608379104

Fründ J, Dormann CF, Holzschuh A, Tscharntke T (2012) Mechanisms of pollinator diversity effects on pollination in experimental plant communities. In: Ecological Society of America, Portland, Oregon

Fründ J, Dormann CF, Tscharntke T (2011) Linné’s floral clock is slow without pollinators – flower closure and plant‐pollinator interaction webs. Ecology Letters 14:896–904. DOI: https://doi.org/10.1111/j.1461-0248.2011.01654.x

Galen C, Stanton ML (1993) Short-term responses of alpine buttercups to experimental manipulations of growing season length. Ecology 74:1052–1058. DOI: https://doi.org/10.2307/1940475

Gilman RT, Fabina NS, Abbott KC, Rafferty NE (2012) Evolution of plant–pollinator mutualisms in response to climate change. Evolutionary Applications 5:2–16. DOI: https://doi.org/10.1111/j.1752-4571.2011.00202.x

Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD (2010) A framework for community interactions under climate change. Trends in Ecology & Evolution 25:325–331. DOI: https://doi.org/10.1016/j.tree.2010.03.002

Gordo O, Sanz JJ (2005) Phenology and climate change: a long-term study in a Mediterranean locality. Oecologia 146:484–495. DOI: https://doi.org/10.1007/s00442-005-0240-z

Gordo O, Sanz JJ (2006) Temporal trends in phenology of the honey bee Apis mellifera (L.) and the small white Pieris rapae (L.) in the Iberian Peninsula (1952–2004). Ecological Entomology 31:261–268. DOI: https://doi.org/10.1111/j.1365-2311.2006.00787.x

Goulson D (2010) Bumblebees: behaviour, ecology, and conservation. Oxford Univ. Pr. DOI: https://doi.org/10.1093/oso/9780199553068.001.0001

Gross RS, Werner PA (1983) Relationships among flowering phenology, insect visitors, and seed-set of individuals: experimental studies on four co-occurring species of goldenrod (Solidago: Compositae). Ecological Monographs:95–117. DOI: https://doi.org/10.2307/1942589

Harder LD, Aizen MA (2010) Floral adaptation and diversification under pollen limitation. Philosophical Transactions of the Royal Society B: Biological Sciences 365:529 –543. DOI: https://doi.org/10.1098/rstb.2009.0226

Harrison RD (2000) Repercussions of El Niño: drought causes extinction and the breakdown of mutualism in Borneo. Proceedings of the Royal Society of London. Series B: Biological Sciences 267:911 –915. DOI: https://doi.org/10.1098/rspb.2000.1089

Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø (2009) How does climate warming affect plant-pollinator interactions? Ecology Letters 12:184–195. DOI: https://doi.org/10.1111/j.1461-0248.2008.01269.x

Hegland SJ, Totland Ø (2008) Is the magnitude of pollen limitation in a plant community affected by pollinator visitation and plant species specialisation levels? Oikos 117:883–891. DOI: https://doi.org/10.1111/j.0030-1299.2008.16561.x

Hocking B (1968) Insect-flower associations in the high Arctic with special reference to nectar. Oikos:359–387. DOI: https://doi.org/10.2307/3565022

Hoover SER, Ladley JJ, Shchepetkina AA, Tisch M, Gieseg SP, Tylianakis JM (2012) Warming, CO2, and nitrogen deposition interactively affect a plant‐pollinator mutualism. Ecology Letters 15:227–234. DOI: https://doi.org/10.1111/j.1461-0248.2011.01729.x

Iler AM, Inouye DW, Høye TT, Miller-Rushing AJ, Burkle LA, Johnston EB (2013) Maintenance of temporal synchrony between syrphid flies and floral resources despite differential phenological responses to climate. Global Change Biology 19:2348–2359. DOI: https://doi.org/10.1111/gcb.12246

Inouye DW (1978) Resource partitioning in bumblebee guilds: experimental studies of foraging behavior. Ecology 59:672–678. DOI: https://doi.org/10.2307/1938769

Inouye DW (2000) The ecological and evolutionary significance of frost in the context of climate change. Ecology Letters 3:457–463. DOI: https://doi.org/10.1046/j.1461-0248.2000.00165.x

Inouye DW, Barr B, Armitage KB, Inouye BD (2000) Climate change is affecting altitudinal migrants and hibernating species. Proceedings of the National Academy of Sciences 97:1630–1633. DOI: https://doi.org/10.1073/pnas.97.4.1630

Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362. DOI: https://doi.org/10.1890/06-2128.1

Johnson DH (1980) The comparison of usage and availability measurements for evaluating resource preference. Ecology 61:65. DOI: https://doi.org/10.2307/1937156

Kaiser-Bunbury CN, Muff S, Memmott J, Müller CB, Caflisch A (2010) The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecology Letters 13:442–452. DOI: https://doi.org/10.1111/j.1461-0248.2009.01437.x

Kameyama Y, Kudo G (2009) Flowering phenology influences seed production and outcrossing rate in populations of an alpine snowbed shrub, Phyllodoce aleutica: effects of pollinators and self-incompatibility. Annals of Botany 103:1385–1394. DOI: https://doi.org/10.1093/aob/mcp037

Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado.

Kearns CA, Inouye DW (1994) Fly pollination of Linum lewisii (Linaceae). American Journal of Botany 81:1091–1095. DOI: https://doi.org/10.1002/j.1537-2197.1994.tb15602.x

Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annual Review of Ecology and Systematics 29:83–112. DOI: https://doi.org/10.1146/annurev.ecolsys.29.1.83

Kim J, Thorp RW (2001) Maternal investment and size-number trade-off in a bee, Megachile apicalis, in seasonal environments. Oecologia 126:451–456. DOI: https://doi.org/10.1007/s004420000540

Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman T-L (2005) Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution, and Systematics 36:467–497. DOI: https://doi.org/10.1146/annurev.ecolsys.36.102403.115320

Kodric-Brown A, Brown JH. 1979. Competition between distantly related taxa in the coevolution of plants and pollinators. American Zoologist 19: 1 1 1 5-27 DOI: https://doi.org/10.1093/icb/19.4.1115

Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith VS (2004) Species coextinctions and the biodiversity crisis. Science 305:1632–1634. DOI: https://doi.org/10.1126/science.1101101

Krebs CJ, Boonstra R, Cowcill K, Kenney AJ (2009) Climatic determinants of berry crops in the boreal forest of the southwestern Yukon. Botany 87:401–408. DOI: https://doi.org/10.1139/B09-013

Kudo G, Hirao A (2006) Habitat-specific responses in the flowering phenology and seed set of alpine plants to climate variation: implications for global-change impacts. Population Ecology 48:49–58. DOI: https://doi.org/10.1007/s10144-005-0242-z

Kudo G, Ida TY (In press) Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology.

Kudo G, Nishikawa Y, Kasagi T, Kosuge S (2004) Does seed production of spring ephemerals decrease when spring comes early? Ecological Research 19:255–259. DOI: https://doi.org/10.1111/j.1440-1703.2003.00630.x

Lawler JJ, White D (2008) Assessing the mechanisms behind successful surrogates for biodiversity in conservation planning. Animal Conservation 11:270–280. DOI: https://doi.org/10.1111/j.1469-1795.2008.00176.x

Lindsey AA, Newman JE (1956) Use of official weather data in spring time temperature analysis of an Indiana phenological record. Ecology 37:812–823. DOI: https://doi.org/10.2307/1933072

Liu Y, Reich PB, Li G, Sun S (2011) Shifting phenology and abundance under experimental warming alters trophic relationships and plant reproductive capacity. Ecology 92:1201–1207. DOI: https://doi.org/10.1890/10-2060.1

Mayer C, Adler L, Armbruster S, Dafni A, Eardley C, Huang S, Kevan P, Ollerton J, Packer L, Ssymank A (2011) Pollination ecology in the 21st century: key questions for future research. Journal of Pollination Ecology 3:8–23. DOI: https://doi.org/10.26786/1920-7603(2011)1

McKinney AM, CaraDonna PJ, Inouye DW, Barr B, Bertelsen CD, Waser NM (2012) Asynchronous changes in phenology of migrating Broad-tailed Hummingbirds and their early-season nectar resources. Ecology 93:1987–1993. DOI: https://doi.org/10.1890/12-0255.1

Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant–pollinator interactions. Ecology Letters 10:710–717. DOI: https://doi.org/10.1111/j.1461-0248.2007.01061.x

Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions.Proceedings of the Royal Society of London. Series B: Biological Sciences 271:2605 –2611. DOI: https://doi.org/10.1098/rspb.2004.2909

Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philosophical Transactions of the Royal Society B: Biological Sciences 365:3177. DOI: https://doi.org/10.1098/rstb.2010.0148

Miller-Rushing AJ, Inouye DW, Primack RB (2008) How well do first flowering dates measure plant responses to climate change? The effects of population size and sampling frequency. Journal of Ecology 96:1289–1296. DOI: https://doi.org/10.1111/j.1365-2745.2008.01436.x

Miller-Rushing AJ, Primack RB (2008) Global warming and flowering times in Thoreau’s Concord: a community perspective. Ecology 89:332–341. DOI: https://doi.org/10.1890/07-0068.1

Mitchell RJ, Flanagan RJ, Brown BJ, Waser NM, Karron JD (2009) New frontiers in competition for pollination. Annals of Botany 103:1403 –1413. DOI: https://doi.org/10.1093/aob/mcp062

Molnár A, Tökölyi J, Végvári Z, Sramkó G, Sulyok J, Barta Z (2012) Pollination mode predicts phenological response to climate change in terrestrial orchids: a case study from central Europe. Journal of Ecology 100:1141–1152. DOI: https://doi.org/10.1111/j.1365-2745.2012.02003.x

Mosquin T (1971) Competition for pollinators as a stimulus for the evolution of flowering time. Oikos:398–402. DOI: https://doi.org/10.2307/3543864

Motten AF, Campbell DR, Alexander DE, Miller HL (1981) Pollination effectiveness of specialist and generalist visitors to a North Carolina population of Claytonia virginica. Ecology 62:1278–1287. DOI: https://doi.org/10.2307/1937292

Olesen JM, Bascompte J, Dupont YL, Elberling H, Rasmussen C, Jordano P (2011) Missing and forbidden links in mutualistic networks. Proceedings of the Royal Society B: Biological Sciences 278:725 –732. DOI: https://doi.org/10.1098/rspb.2010.1371

Olesen JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89:1573–1582. DOI: https://doi.org/10.1890/07-0451.1

Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 37:637–669. DOI: https://doi.org/10.1146/annurev.ecolsys.37.091305.110100

Parsche S, Fründ J, Tscharntke T (2011) Experimental environmental change and mutualistic vs. antagonistic plant flower–visitor interactions. Perspectives in Plant Ecology, Evolution and Systematics 13:27–35. DOI: https://doi.org/10.1016/j.ppees.2010.12.001

Petanidou T, Kallimanis AS, Tzanopoulos J, Sgardelis SP, Pantis JD (2008) Long-term observation of a pollination network: fluctuation in species and interactions, relative invariance of network structure and implications for estimates of specialization. Ecology Letters 11:564–575. DOI: https://doi.org/10.1111/j.1461-0248.2008.01170.x

Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution 25:345–353. DOI: https://doi.org/10.1016/j.tree.2010.01.007

Proctor M, Yeo P, Lack A (1996) The Natural History of Pollination (Collins New Naturalist Library, Book 83). HarperCollins UK.

Rafferty NE, CaraDonna PJ, Burkle LA, Iler AM, Bronstein JL. (In press) Phenology of species interactions in a changing climate: an assessment of available approaches. Ecology & Evolution

Rafferty NE, Ives AR (2011) Effects of experimental shifts in flowering phenology on plant–pollinator interactions. Ecology Letters 14:69–74. DOI: https://doi.org/10.1111/j.1461-0248.2010.01557.x

Rafferty NE, Ives AR (2012) Pollinator effectiveness varies with experimental shifts in flowering time. Ecology 93:803–814. DOI: https://doi.org/10.1890/11-0967.1

Rathcke B (1983) Competition and facilitation among plants for pollination. Pollination Biology: 305–329. DOI: https://doi.org/10.1016/B978-0-12-583980-8.50019-3

Reed TE, Grøtan V, Jenouvrier S, Sæther BE, Visser ME (2013). Population growth in a wild bird is buffered against phenological mismatch. Science 340:488-491. DOI: https://doi.org/10.1126/science.1232870

Reid AM, Lortie CJ (2012) Cushion plants are foundation species with positive effects extending to higher trophic levels. Ecosphere 3:art96. DOI: https://doi.org/10.1890/ES12-00106.1

Roa R (1992) Design and analysis of multiple-choice feeding-preference experiments. Oecologia 89:509–515. DOI: https://doi.org/10.1007/BF00317157

Schemske DW, Willson MF, Melampy MN, Miller LJ, Verner L, Schemske KM, Best LB (1978) Flowering ecology of some spring woodland herbs. Ecology 59:351–366. DOI: https://doi.org/10.2307/1936379

Schweiger O, Biesmeijer JC, Bommarco R, Hickler T, Hulme PE, Klotz S, Kühn I, Moora M, Nielsen A, Ohlemüller R, Petanidou T, Potts SG, Pyšek P, Stout JC, Sykes MT, Tscheulin T, Vilà M, Walther G, Westphal C, Winter M, Zobel M, Settele J (2010) Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination. Biological Reviews 85:777–795. DOI: https://doi.org/10.1111/j.1469-185X.2010.00125.x

Sherry RA, Zhou X, Gu S, Arnone JA, Schimel DS, Verburg PS, Wallace LL, Luo Y (2007) Divergence of reproductive phenology under climate warming. Proceedings of the National Academy of Sciences 104:198–202. DOI: https://doi.org/10.1073/pnas.0605642104

Singer MC, Parmesan C (2010) Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy? Philosophical Transactions of the Royal Society B: Biological Sciences 365:3161 –3176. DOI: https://doi.org/10.1098/rstb.2010.0144

Sparks TH, Yates TJ (1997) The effect of spring temperature on the appearance dates of British butterflies 1883–1993. Ecography 20:368–374. DOI: https://doi.org/10.1111/j.1600-0587.1997.tb00381.x

Steffan-Dewenter I, Potts SG, Packer L (2005) Pollinator diversity and crop pollination services are at risk. Trends in Ecology & Evolution 20:651. DOI: https://doi.org/10.1016/j.tree.2005.09.004

Stelzer RJ, Chittka L, Carlton M, Ings TC (2010) Winter active bumblebees (Bombus terrestris) achieve high foraging rates in urban Britain. PLoS ONE 5:e9559. DOI: https://doi.org/10.1371/journal.pone.0009559

Thomson JD (1980) Skewed flowering distributions and pollinator attraction. Ecology 61:572–579. DOI: https://doi.org/10.2307/1937423

Thomson JD (1981) Spatial and temporal components of resource assessment by flower-feeding insects. The Journal of Animal Ecology:49–59. DOI: https://doi.org/10.2307/4030

Thomson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Philosophical Transactions of the Royal Society B: Biological Sciences 365:3187 –3199. DOI: https://doi.org/10.1098/rstb.2010.0115

Thórhallsdóttir TE (1998) Flowering phenology in the central highland of Iceland and implications for climatic warming in the Arctic. Oecologia 114:43–49. DOI: https://doi.org/10.1007/s004420050418

Totland Ø (2001) Environment-dependent pollen limitation and selection on floral traits in an alpine species. Ecology 82:2233–2244. DOI: https://doi.org/10.1890/0012-9658(2001)082[2233:EDPLAS]2.0.CO;2

Turnbull LA, Crawley MJ, Rees M (2000) Are plant populations seed-limited? A review of seed sowing experiments. Oikos 88:225–238. DOI: https://doi.org/10.1034/j.1600-0706.2000.880201.x

Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecology Letters 11:1351–1363. DOI: https://doi.org/10.1111/j.1461-0248.2008.01250.x

Van Strien AJ, Plantenga WF, Soldaat LL, Van Swaay CAM, WallisDeVries MF (2008) Bias in phenology assessments based on first appearance data of butterflies. Oecologia 156:227–235. DOI: https://doi.org/10.1007/s00442-008-0959-4

Vázquez DP, Morris WF, Jordano P (2005) Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecology Letters 8:1088–1094. DOI: https://doi.org/10.1111/j.1461-0248.2005.00810.x

Visser ME (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proceedings of the Royal Society B: Biological Sciences 275:649–659. DOI: https://doi.org/10.1098/rspb.2007.0997

Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proceedings of the Royal Society B: Biological Sciences 272:2561 –2569. DOI: https://doi.org/10.1098/rspb.2005.3356

Visser ME, Holleman LJM (2001) Warmer springs disrupt the synchrony of oak and winter moth phenology. Proceedings of the Royal Society of London. Series B: Biological Sciences 268:289 –294. DOI: https://doi.org/10.1098/rspb.2000.1363

Visser ME, Noordwijk AJ van, Tinbergen JM, Lessells CM (1998) Warmer springs lead to mistimed reproduction in great tits (Parus major). Proceedings of the Royal Society B: Biological Sciences 265:1867–1870. DOI: https://doi.org/10.1098/rspb.1998.0514

Wall MA, Timmerman-Erskine M, Boyd RS (2003) Conservation impact of climatic variability on pollination of the federally endangered plant, Clematis socialis (Ranunculaceae). Southeastern Naturalist 2:11–24. DOI: https://doi.org/10.1656/1528-7092(2003)002[0011:CIOCVO]2.0.CO;2

Waser NM (1979) Pollinator availability as a determinant of flowering time in ocotillo (Fouquieria splendens). Oecologia 39:107–121. DOI: https://doi.org/10.1007/BF00346001

Waser NM, Real LA (1979) Effective mutualism between sequentially flowering plant species. 281:670–672. DOI: https://doi.org/10.1038/281670a0

Widén B (1991) Phenotypic selection on flowering phenology in Senecio integrifolius, a perennial herb. Oikos 61:205–215. DOI: https://doi.org/10.2307/3545338

Willis CG, Ruhfel B, Primack RB, Miller-Rushing AJ, Davis CC (2008) Phylogenetic patterns of species loss in Thoreau’s woods are driven by climate change. Proceedings of the National Academy of Sciences 105:17029 –17033. DOI: https://doi.org/10.1073/pnas.0806446105

Willmer P (2011) Pollination and floral ecology. Princeton University Press. DOI: https://doi.org/10.23943/princeton/9780691128610.001.0001

Willmer P (2012) Ecology: pollinator–plant synchrony tested by climate change. Current Biology 22:131–132. DOI: https://doi.org/10.1016/j.cub.2012.01.009

Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecology letters 13:1–10. DOI: https://doi.org/10.1111/j.1461-0248.2009.01402.x

Downloads

Published

2014-04-01

How to Cite

Straka, J. R., & Starzomski, B. M. (2014). Humming along or buzzing off? The elusive consequences of plant-pollinator mismatches. Journal of Pollination Ecology, 13, 129–145. https://doi.org/10.26786/1920-7603(2014)18

Issue

Section

Reviews