Maintenance of temporal synchrony between syrphid flies and floral resources despite differential phenological responses to climate

Global Change Biology

Volumn 19, Issue 8, 2013, Pages 2348-2359

  Iler, Amy M ^a,b   Inouye, David W ^a,b   Høye, Toke T ^c   Miller Rushing, Abraham J ^b,d   Burkle, Laura A ^b,e   Johnston, Eleanor B ^b,f  

^a Bldg 142   (United States)

^b ROCKY MOUNTAIN BIOLOGICAL LABORATORY   (United States)

^c AARHUS UNIVERSITY   (Denmark)

^d Acadia National Park   (United States)

^e MONTANA STATE UNIVERSITY   (United States)

^f Climate Interactive   (United States)

Author keywords

Climate change; Hoverfly; Mismatch; Phenology; Pollinator; Rocky Mountain Biological Laboratory; Synchrony; Syrphidae

Indexed keywords

RAIN; SNOW;

ANNUAL VARIATION; CLIMATE CHANGE; CLIMATE VARIATION; FLORA; FLOWERING; FLY; FREEZING; PHENOLOGY; PLANT-POLLINATOR INTERACTION; POLLINATOR; PRECIPITATION (CLIMATOLOGY); SNOWMELT; SYNCHRONY;

ANGIOSPERM; ANIMAL; ARTICLE; CLIMATE CHANGE; DIPTERA; HOVERFLY; MISMATCH; PHENOLOGY; PHYSIOLOGY; POLLINATION; POLLINATOR; REPRODUCTION; ROCKY MOUNTAIN BIOLOGICAL LABORATORY; SEASON; STATISTICAL MODEL; SYNCHRONISM; SYRPHIDAE; TEMPERATURE; TIME; UNITED STATES;

CLIMATE CHANGE; HOVERFLY; MISMATCH; PHENOLOGY; POLLINATOR; ROCKY MOUNTAIN BIOLOGICAL LABORATORY; SYNCHRONY; SYRPHIDAE;

ANGIOSPERMS; ANIMALS; CLIMATE CHANGE; COLORADO; DIPTERA; LINEAR MODELS; POLLINATION; RAIN; REPRODUCTION; SEASONS; SNOW; TEMPERATURE; TIME FACTORS;

SYRPHIDAE;

EID: 84880132848     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/gcb.12246     Document Type: Article

References (80)

1. 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.
2. Allen-Wardell G, Bernhardt P, Bitner R et al. (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conservation Biology, 12, 8-17.
3. Anderson DR (2008) Model Based Inference in the Life Sciences: A Primer on Evidence. Springer, New York.
4. van Asch M, Tienderen PH, Holleman LJM et al. (2007) Predicting adaptation of phenology in response to climate change, an insect herbivore example. Global Change Biology, 13, 1596-1604.
5. Azmeh S, Owen J, Sorensen K et al. (1998) Mimicry profiles are affected by human-induced habitat changes. Proceedings of the Royal Society of London B, 265, 2285-2290.
6. Bale JS, Masters GJ, Hodkinson ID et al. (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology, 8, 1-16.
7. Bartomeus I, Ascher JS, Wagner D et al. (2011) Climate-associated phenological advances in bee pollinators and bee-pollinated plants. Proceedings of the National Academy of Sciences USA, 108, 20645-20649.
8. Biesmeijer JC, Roberts SPM, Reemer M et al. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science, 313, 351-354.
9. Bosch J, Kemp WP (2003) Effect of wintering duration and temperature on survival and emergence time in males of the orchard pollinator Osmia lignaria (Hymenoptera: Megachilidae). Environmental Entomology, 32, 711-716.
10. Burkle L, Irwin R (2009) The importance of interannual variation and bottom-up nitrogen enrichment for plant-pollinator networks. Oikos, 118, 1816-1829.
11. Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science, 339, 1611-1615.
12. Bynum MR, Smith WK (2001) Floral movements in response to thunderstorms improve reproductive effort in the alpine species Gentiana algida (Gentianaceae). American Journal of Botany, 88, 1088-1095.
13. Cahill AE, Aiello-Lammens ME, Fisher-Reid MC et al. (2013) How does climate change cause extinction? Proceedings of the Royal Society of London B, 280, 1-9.
14. Denlinger DL (2002) Regulation of diapause. Annual Review of Entomology, 47, 93-122.
15. Dittrich W, Gilbert F, Green P et al. (1993) Imperfect mimicry - a pigeon's perspective. Proceedings of the Royal Society of London B, 251, 195.
16. 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.
17. Ellwood ER, Diez JM, Ibanez I et al. (2012) Disentangling the paradox of insect phenology: are temporal trends reflecting the response to warming? Oecologia, 168: 1161-1171.
18. Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science, 296, 1689-1691.
19. Forister ML, Shapiro AM (2003) Climatic trends and advancing spring flight of butterflies in lowland California. Global Change Biology, 9, 1130-1135.
20. Forrest JRK, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecological Monographs, 81, 469-491.
21. 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.
22. Gordo O, Sanz JJ (2010) Impact of climate change on plant phenology in Mediterranean ecosystems. Global Change Biology, 16, 1082-1106.
23. Graham-Taylor LG, Stubbs AE, Brooke MD (2009) Changes in phenology of hoverflies in a central England garden. Insect Conservation and Diversity, 2, 29-35.
24. Harrington R, Woiwod I, Sparks T (1999) Climate change and trophic interactions. Trends in Ecology & Evolution, 14, 146-150.
25. Harte J, Torn MS, Chang FR et al. (1995) Global warming and soil microclimate - results from a meadow-warming experiment. Ecological Applications, 5, 132-150.
26. Haslett JR (1989a) Adult feeding by holometabolous insects - pollen and nectar as complementary nutrient sources for Rhingia campestris (Diptera, Syrphidae). Oecologia, 81, 361-363.
27. Haslett JR (1989b) Interpreting patterns of resource utilization: randomness and selectivity in pollen feeding by adult hoverflies. Oecologia, 78, 433-442.
28. Hegland SJ, Nielsen A, Lazaro A et al. (2009) How does climate warming affect plant-pollinator interactions? Ecology Letters, 12, 184-195.
29. Holloway BA (1976) Pollen-feeding in hover-flies (Diptera-Syrphidae). New Zealand Journal of Zoology, 3, 339-350.
30. Howarth B, Edmunds M (2000) The phenology of Syrphidae (Diptera): are they Batesian mimics of Hymenoptera? Biological Journal of the Linnean Society, 71, 437-457.
31. Howarth B, Edmunds M, Gilbert F (2004) Does the abundance of hoverfly (Syrphidae) mimics depend on the numbers of their Hymenopteran models? Evolution, 58, 367-375.
32. Høye TT, Forchhammer MC (2008) Phenology of high-arctic arthropods: effects of climate on spatial, seasonal, and inter-annual variation. Advances in Ecological Research, 40, 299-324.
33. Høye TT, Post E, Meltofte H et al. (2007a) Rapid advancement of spring in the High Arctic. Current Biology, 17, R449-R451.
34. Høye TT, Ellebjerg SM, Philipp M (2007b) The impact of climate on flowering in the High Arctic - the case of Dryas in a hybrid zone. Arctic Antarctic and Alpine Research, 39, 412-421.
35. Høye TT, Post E, Schmidt NM et al. (in press) Shorter flowering seasons and declining abundance of flower visitors in a warmer Arctic. Nature Climate Change. doi:10.1038/nclimate1909.
36. Iler AM, Høye TT, Inouye DW et al. (2013a) Nonlinear flowering responses to climate: are species approaching their limits of phenological change? Philosophical Transactions of the Royal Society B, doi: 10.1098/rstb.2012.0489.
37. Iler AM, Høye TT, Inouye DW et al. (2013b) Long-term trends mask variation in the direction and magnitude of short-term phenological shifts. American Journal of Botany, doi: 10.3732/ajb.1200490.
38. Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology, 89, 353-362.
39. Inouye DW, Morales MA, Dodge GJ (2002) Variation in timing and abundance of flowering by Delphinium barbeyi Huth (Ranunculaceae): the roles of snowpack, frost, and La Nina, in the context of climate change. Oecologia, 130, 543-550.
40. Inouye DW, Saavedra F, Lee-Yang W (2003) Environmental influences on the phenology and abundance of flowering by Androsace septentrionalis (Primulaceae). American Journal of Botany, 90, 905-910.
41. IPCC (2007) Climate change 2007: synthesis report. In: Contribution of Working Groups I, II, and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds Core writing team, Pachauri RK, Reisinger A). IPCC, Geneva, Switzerland, 104 pp.
42. Kearns CA (1992) Anthophilous fly distribution across an elevation gradient. American Midland Naturalist, 127, 172-182.
43. Kearns CA, Inouye DW (1994) Fly pollination of Linum lewisii (Linaceae). American Journal of Botany, 81, 1091-1095.
44. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annual Review of Ecology and Systematics, 29, 83-112.
45. Keil P, Konvicka M (2005) Local species richness of Central European hoverflies (Diptera: Syrphidae): a lesson taught by local faunal lists. Diversity and Distributions, 11, 417-426.
46. Klein AM, Vaissiere BE, Cane JH et al. (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society of London B, 274, 303-313.
47. Kudo G, Ida TY (in press) Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology. Available at: http://dx.doi.org/10.1890/12-2003.1 (accessed 24 April 2013).
48. Kudo G, Nishikawa Y, Kasagi T et al. (2004) Does seed production of spring ephemerals decrease when spring comes early? Ecological Research, 19, 255-259.
49. Lambert AM, Miller-Rushing AJ, Inouye DW (2010) Changes in snowmelt date and summer precipitation affect the flowering phenology of Erythronium grandiflorum (Glacier lily; Liliaceae). American Journal of Botany, 97, 1431-1437.
50. Larson BMH, Kevan PG, Inouye DW (2001) Flies and flowers: taxonomic diversity of anthophiles and pollinators. Canadian Entomologist, 133, 439-465.
51. Lundemo S, Totland Ø (2007) Within-population spatial variation in pollinator visitation rates, pollen limitation on seed set, and flower longevity in an alpine species. Acta Oecologica, 32, 262-268.
52. McGuire AD, Armbruster WS (1991) An experimental test for reproductive interactions between two sequentially blooming Saxifraga species (Saxifragaceae). American Journal of Botany, 78, 214-219.
53. Menzel A, Fabian P (1999) Growing season extended in Europe. Nature, 397, 659.
54. 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. American Journal of Botany, 96, 1821-1829.
55. 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.
56. Miller-Rushing AJ, Høye TT, Inouye DW et al. (2010) The effects of phenological mismatches on demography. Philosophical Transactions of the Royal Society B, 365, 3177-3186.
57. Myneni RB, Keeling CD, Tucker CJ et al. (1997) Increased plant growth in the northern high latitudes from 1981 to 1991. Nature, 386, 698-702.
58. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos, 120, 321-326.
59. Painter TH, Barrett AP, Landry CC et al. (2007) Impact of disturbed desert soils on duration of mountain snow cover. Geophysical Research Letters, 34, 12502.
60. Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Global Change Biology, 13, 1860-1872.
61. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37-42.
62. Pauw A, Hawkins JA (2011) Reconstruction of historical pollination rates reveals linked declines of pollinators and plants. Oikos, 120, 344-349.
63. Petanidou T, Vujic A, Ellis WN (2011) Hoverfly diversity (Diptera: Syrphidae) in a Mediterranean scrub community near Athens, Greece. Annales De La Société Entomologique De France, 47, 168-175.
64. Potts SG, Biesmeijer JC, Kremen C et al. (2010) Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution, 25, 345-353.
65. Price MV, Waser NM (1998) Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology, 79, 1261-1271.
66. R Development Core Team (2008) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, available at: http://www.R-project.org.
67. Rafferty NE, Ives AR (2011) Effects of experimental shifts in flowering phenology on plant-pollinator interactions. Ecology Letters, 14, 69-74.
68. Rotheray GE, Gilbert F (2011) The Natural History of Hoverflies. Forrest Text, Ceredigion, UK.
69. Roy DB, Sparks TH (2000) Phenology of British butterflies and climate change. Global Change Biology, 6, 407-416.
70. Schneider F (1969) Bionomics and physiology of aphidophagous Syrphidae. Annual Review of Entomology, 14, 103-124.
71. Sparks TH, Yates TJ (1997) The effect of spring temperature on the appearance dates of British butterflies 1883-1993. Ecography, 20, 368-374.
72. Steltzer H, Landry C, Painter TH et al. (2009) Biological consequences of earlier snowmelt from desert dust deposition in alpine landscapes. Proceedings of the National Academy of Sciences USA, 106, 11629-11634.
73. Stubbs AE, Falk SJ (2002) British Hoverflies. British Entomological and Natural History Society, Reading, UK.
74. Tauber MJ, Tauber CA (1976) Insect seasonality - diapause maintenance, termination, and post diapause development. Annual Review of Entomology, 21, 81-107.
75. Thomson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Philosophical Transactions of the Royal Society B, 365, 3187-3199.
76. Tobin PC, Nagarkatti S, Loeb G et al. (2008) Historical and projected interactions between climate change and insect voltinism in a multivoltine species. Global Change Biology, 14, 951-957.
77. Waldbauer GP (1988) Asynchrony between Batesian mimics and their models. American Naturalist, 131, S103-S121.
78. Waser NM, Ollerton J (2006) Plant-Pollinator Interactions: From Specialization to Generalization. The University of Chicago Press, Illinois, Chicago USA.
79. White J, Son Y, Park YL (2009) Temperature-dependent emergence of Osmia cornifrons (Hymenoptera: Megachilidae) adults. Journal of Economic Entomology, 102, 2026-2032.
80. Yasaka M, Nishiwaki Y, Konno Y (1998) Plasticity of flower longevity in Corydalis ambigua. Ecological Research, 13, 211-216.