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Pollination Declines- SLU talk

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Pollination Declines- SLU talk

  1. 1. Historical changes in bee community composition and phenology. Is there a pollination crisis? Ignasi Bartomeus nacho.bartomeus@gmail.com @ibartomeus
  2. 2. 4% of land was agricultur e in ~1800 >Z0%of land is agriculture , now 7 billion people 1 billion people 1880 1950 1980 2010we are +0.6ºc above the 1950-1980 mean temperature levels 1800
  3. 3. 4% of land was agricultur e in ~1800 >Z0%of land is agriculture , now 7 billion people 1 billion people 1880 1950 1980 2010we are +0.6ºc above the 1950-1980 mean temperature levels 1800
  4. 4. 4% of land was agricultur e in ~1800 >Z0%of land is agriculture , now 7 billion people 1 billion people 1880 1950 1980 2010we are +0.6ºc above the 1950-1980 mean temperature levels 1800
  5. 5. but… how are all these changes affecting plants and animals?
  6. 6. Trends Causes: Land Use Change Climate Change Consequences
  7. 7. 2010 Rachael Winfree
  8. 8. you can buy a DeLorean We could buy a Delorean!
  9. 9. American Natural History Museum John Ascher
  10. 10. Database: *Date *Collector *Coordinates Assemble long-term data:
  11. 11. Thisisnot theromantic triphe promised This is not the romantic trip he promised *American Museum of Natural History *University of Connecticut *Cornell University *Rutgers University *Connecticut Agricultural Station *University of New Hampshire *University of Massachusetts *Vermont State Bee Database *NewYork State Museum *Bohart Museum of Entomology.
  12. 12. Trends Bartomeus et al 2013 PNAS
  13. 13. What do we know about the “pollinator crisis”?
  14. 14. What do we know about the “pollinator crisis”? * Honeybees (managed) * Bumblebees Cameron et al. 2011Grixti et al. 2009,Colla et al. 2008,
  15. 15. What do we know about the “pollinator crisis”? * Honeybees (managed) * Bumblebees Cameron et al. 2011Grixti et al. 2009,Colla et al. 2008, useum collections throughout the United States (Fig. S1B and able S2). Comparisons of the historical and current data vealed extensive range reductions (Fig. 1 A, D, G, and H) and gnificant decreases in RA in all four species suspected of pop- ation decline (all P < 0.001) (Fig. 2); each was absent from gnificantly more sites predicted to have high occurrence prob- bilities than were stable species (Fisher’s exact tests; all P < 001) (Table S4). Declines in RA appear only within the last 20– 0 y, with RA values from current surveys lower than in any de- cade of the last century (Fig. S1C). The four allegedly stable species showed no clear patterns of range reduction (Fig. 1 B, C, E, and F and Tables S2, S4, and S5) or consistent declines in RA. Historically, B. occidentalis and B. pensylvanicus had among the broadest geographic ranges of any bumble bee species in North America (Fig. 1 and Table S5). However, the current surveys detected B. occidentalis only throughout the intermountain west and Rocky Mountains; it was largely absent from the western portion of its range (Figs. 1A and 2) (detected range-area re-
  16. 16. What do we know about the “pollinator crisis”? * Honeybees (managed) * Bumblebees Cameron et al. 2011Grixti et al. 2009,Colla et al. 2008, useum collections throughout the United States (Fig. S1B and able S2). Comparisons of the historical and current data vealed extensive range reductions (Fig. 1 A, D, G, and H) and gnificant decreases in RA in all four species suspected of pop- ation decline (all P < 0.001) (Fig. 2); each was absent from gnificantly more sites predicted to have high occurrence prob- bilities than were stable species (Fisher’s exact tests; all P < 001) (Table S4). Declines in RA appear only within the last 20– 0 y, with RA values from current surveys lower than in any de- cade of the last century (Fig. S1C). The four allegedly stable species showed no clear patterns of range reduction (Fig. 1 B, C, E, and F and Tables S2, S4, and S5) or consistent declines in RA. Historically, B. occidentalis and B. pensylvanicus had among the broadest geographic ranges of any bumble bee species in North America (Fig. 1 and Table S5). However, the current surveys detected B. occidentalis only throughout the intermountain west and Rocky Mountains; it was largely absent from the western portion of its range (Figs. 1A and 2) (detected range-area re- (Pathogens)
  17. 17. What we know about all other >400 bee genera? Biesmeijer et al. 2006
  18. 18. “for most pollinator species, the paucity of long-term data and the incomplete knowledge of even basic taxonomy and ecology make definitive assessment of status exceedingly difficult” NAS 2008
  19. 19. Assemble long-term data:
  20. 20. * 47 bee genera comprising 438 species. * >30,000 independently collected bee specimens Assemble long-term data: * >1500 collectors * >11000 collection events
  21. 21. * 47 bee genera comprising 438 species. Assemble long-term data: * >1500 collectors * >11000 collection events * >30,000 independently collected bee specimens
  22. 22. Restrict Geographical area & check no temporal bias.
  23. 23. Use independently collected specimens
  24. 24. 1) Richness
  25. 25. Rarefaction:“expected richness if sample size was equal” 180 200 220 240 Numberofbeespecies (excludingBombus) 1872-1913 1913-1931 1931-1960 1960-1965 1965-1972 1972-1981 1981-2002 2002-2006 2006-2008 2008-2011 12 14 16 18 NumberofBombusspecies 1877-1899 1899-1906 1906-1919 1919-1937 1937-1963 1963-1975 1975-1986 1986-2005 2005-2008 2008-2011 0 2 4 6 8 10 12 Numberofexoticspecies 1872-1914 1914-1932 1932-1960 1960-1965 1965-1972 1972-1981 1981-2002 2002-2006 2006-2008 2008-2011 Bee photo Bee photo Bee photo Numberofnon-BombusspeciesNumberofBombusspecies Coelioxys sayi Bombus citrinus (A) (B) (C) Anthidium manicatum ! {
  26. 26. 180 200 220 240 Numberofbeespecies (excludingBombus) 1872-1913 1913-1931 1931-1960 1960-1965 1965-1972 1972-1981 1981-2002 2002-2006 2006-2008 2008-2011 12 14 16 18 NumberofBombusspecies 1877-1899 1899-1906 1906-1919 1919-1937 1937-1963 1963-1975 1975-1986 1986-2005 2005-2008 2008-2011 0 2 4 6 8 10 12 Numberofexoticspecies 1872-1914 1914-1932 1932-1960 1960-1965 1965-1972 1972-1981 1981-2002 2002-2006 2006-2008 2008-2011 Bee photo Bee photo Bee photo Numberofnon-BombusspeciesNumberofBombusspecies Coelioxys sayi Bombus citrinus (A) (B) (C) Anthidium manicatum ! 140 people/km^2 1900’s Rarefaction:“expected richness if sample size was equal”
  27. 27. 180 200 220 240 Numberofbeespecies (excludingBombus) 1872-1913 1913-1931 1931-1960 1960-1965 1965-1972 1972-1981 1981-2002 2002-2006 2006-2008 2008-2011 12 14 16 18 NumberofBombusspecies 1877-1899 1899-1906 1906-1919 1919-1937 1937-1963 1963-1975 1975-1986 1986-2005 2005-2008 2008-2011 0 2 4 6 8 10 12 Numberofexoticspecies 1872-1914 1914-1932 1932-1960 1960-1965 1965-1972 1972-1981 1981-2002 2002-2006 2006-2008 2008-2011 Bee photo Bee photo Bee photo Numberofnon-BombusspeciesNumberofBombusspecies Coelioxys sayi Bombus citrinus (A) (B) (C) Anthidium manicatum ! p  =  0.07 Rarefaction:“expected richness if sample size was equal” 140 people/km^2 325 people/km^2 1900’s 2000’s1950’s
  28. 28. 180 200 220 240 Numberofbeespecies (excludingBombus) 1872-1913 1913-1931 1931-1960 1960-1965 1965-1972 1972-1981 1981-2002 2002-2006 2006-2008 2008-2011 12 14 16 18 NumberofBombusspecies 1877-1899 1899-1906 1906-1919 1919-1937 1937-1963 1963-1975 1975-1986 1986-2005 2005-2008 2008-2011 0 2 4 6 8 10 12 Numberofexoticspecies 1872-1914 1914-1932 1932-1960 1960-1965 1965-1972 1972-1981 1981-2002 2002-2006 2006-2008 2008-2011 Bee photo Bee photo Bee photo Numberofnon-BombusspeciesNumberofBombusspecies Coelioxys sayi Bombus citrinus (A) (B) (C) Anthidium manicatum ! p  =  0.01
  29. 29. 180 200 220 240 Numberofbeespecies (excludingBombus) 1872-1913 1913-1931 1931-1960 1960-1965 1965-1972 1972-1981 1981-2002 2002-2006 2006-2008 2008-2011 12 14 16 18 NumberofBombusspecies 1877-1899 1899-1906 1906-1919 1919-1937 1937-1963 1963-1975 1975-1986 1986-2005 2005-2008 2008-2011 0 2 4 6 8 10 12 Numberofexoticspecies 1872-1914 1914-1932 1932-1960 1960-1965 1965-1972 1972-1981 1981-2002 2002-2006 2006-2008 2008-2011 Bee photo Bee photo Bee photo Numberofnon-BombusspeciesNumberofBombusspecies Coelioxys sayi Bombus citrinus (A) (B) (C) Anthidium manicatum !p  =  0.01
  30. 30. 2) Species level
  31. 31. Effort Logistic regression estimate 1880 1900 1920 1940 1960 1980 2000 0.000.050.100.15 Halictus ligatus Year Proportionincollection ● ●● ● ●●●●●●● ● ● ● ● ● ●●●● ● ● ●● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ●● ● ● ● ●● ● ● ● ●● ●● ● ● ● ● ● ●● ● ●●● ● ● ● ●● ● ● ● ● ● ● ● ● ● ● ●● ● ● ● ● ● ● ● ● ●● ● ● ● ● ● ● ● ● ● ● ● ● ● ●● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ●
  32. 32. 1880 1900 1920 1940 1960 1980 2000 0.000.050.100.15 Andrena carlini Year Proportionincollection ● ●●● ● ● ● ● ● ●● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ●● ● ● ● ● ● ● ● ● ● ●●● ● ●● ● ● ● ● ● ● ● ● ● ● ● ●● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ●● ●● ● ● ● ● ●● ●● ● ● ● ● Logistic regression estimate Effort
  33. 33. Coelioxys Megachile Bombus Melissodes Osmia Colletes Andrena Hylaeus Halictus Lasioglossum Agapostemon Sphecodes Nomada Ceratina -0.04 -0.02 0.00 0.02 0.04 Rateofchange(estimate) Coelioxys Megachile Bombus Melissodes Osmia Colletes Andrena Hylaeus Halictus Lasioglossum Agapostemon Sphecodes Nomada Ceratina 187  species   29%  had  signi5icant  decreases   27%  had  signi5icant  increases
  34. 34. 1880 1900 1920 1940 1960 1980 2000 0.000.050.100.15 Macropis patellata Year Proportionincollection ● ●●● ●●●●●●●●●●●●●● ● ●●●●●● ● ● ● ● ● ● ●● ● ●●● ● ● ● ●●● ● ●●● ● ● ● ●●●● ● ● ● ●● ● ●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●● ● ●●●●●●●● ● ●●●●●●●● ● ●●●●●●●●●●●●●●●●●●●● Not recently in the database Macropis sp.
  35. 35. 1880 1900 1920 1940 1960 1980 2000 0.00.20.40.60.81.0 Bombus affinis Year Presence/Absence ● ● ●● ●●● ●●●●●● ● ● ● ● ●●●●● ● ●●●●●●●●●●●●●●●● ● ●●● ● ●●●●● ● ●●●●●●●●● ● ● ● ●●● ●● ● ● ● ● ●●●●●●●●●●●●●●●●●●●●●●●●●●●●● ● ●●●●●●●● ● ●●●●●● ● ●●●● ● ● ●●●●●●●●●●
  36. 36. Bombus affinis Bombus ashtoni Bombus pensylvanicus + Macropis patellata
  37. 37. 3)Traits
  38. 38. Coelioxys Megachile Bombus Melissodes Osmia Colletes Andrena Hylaeus Halictus Lasioglossum Agapostemon Sphecodes Nomada Ceratina -0.04 -0.02 0.00 0.02 0.04 Rateofchange(estimate) Coelioxys Megachile Bombus Melissodes Osmia Colletes Andrena Hylaeus Halictus Lasioglossum Agapostemon Sphecodes Nomada Ceratina Can BeeTraits explain theTrends?
  39. 39. λ of the relative change estimate = 0.24
  40. 40. Oligolectic Polylectic -0.04 -0.02 0.00 0.02 0.04 Rateofchange(estimate) 1 2 3 4 5 6 -0.04 -0.02 0.00 0.02 0.04 Body size (mm) Rateofchange(estimate) 40 60 80 100 120 140 -0.04 -0.02 0.00 0.02 0.04 Phenological breadth (days) Rateofchange(estimate) 42 44 46 48 50 -0.04 -0.02 0.00 0.02 0.04 Northernmost latitude recorded Rateofchange(estimate) !
  41. 41. Oligolectic Polylectic -0.04 -0.02 0.00 0.02 0.04 Rateofchange(estimate) 1 2 3 4 5 6 -0.04 -0.02 0.00 0.02 0.04 Body size (mm) Rateofchange(estimate) 40 60 80 100 120 140 -0.04 -0.02 0.00 0.02 0.04 Phenological breadth (days) Rateofchange(estimate) 42 44 46 48 50 -0.04 -0.02 0.00 0.02 0.04 Northernmost latitude recorded Rateofchange(estimate) !
  42. 42. Oligolectic Polylectic -0.04 -0.02 0.00 0.02 0.04 Rateofchange(estimate) 1 2 3 4 5 6 -0.04 -0.02 0.00 0.02 0.04 Body size (mm) Rateofchange(estimate) 40 60 80 100 120 140 -0.04 -0.02 0.00 0.02 0.04 Phenological breadth (days) Rateofchange(estimate) 42 44 46 48 50 -0.04 -0.02 0.00 0.02 0.04 Northernmost latitude recorded Rateofchange(estimate) ! Oligolectic Polylectic -0.04 -0.02 0.00 0.02 0.04 Rateofchange(estimate) 1 2 3 4 5 6 -0.04 -0.02 0.00 0.02 0.04 Body size (mm) Rateofchange(estimate) 40 60 80 100 120 140 -0.04 -0.02 0.00 0.02 0.04 Phenological breadth (days) Rateofchange(estimate) 42 44 46 48 50 -0.04 -0.02 0.00 0.02 0.04 Northernmost latitude recorded Rateofchange(estimate) !
  43. 43. Oligolectic Polylectic -0.04 -0.02 0.00 0.02 0.04 Rateofchange(estimate) 1 2 3 4 5 6 -0.04 -0.02 0.00 0.02 0.04 Body size (mm) Rateofchange(estimate) 40 60 80 100 120 140 -0.04 -0.02 0.00 0.02 0.04 Phenological breadth (days) Rateofchange(estimate) 42 44 46 48 50 -0.04 -0.02 0.00 0.02 0.04 Northernmost latitude recorded Rateofchange(estimate) !
  44. 44. Causes: Land use Change Winfree, Bartomeus, Cariveau 2011 AREES
  45. 45. 265 published studies, contributing a total of 674 measures of pollinator response to anthropogenic land use
  46. 46. 40% 47% 13% 22%29% 49% 32%27% 41% 39%39% 21% 39% 30% 30% Bees Butterflies Syrphid flies Birds Bats
  47. 47. ? ? ? 300 to 3,000 m radius a b
  48. 48. a Extreme habitat loss Abundance (31) Richness (17) b Moderate habitat loss –1.4 –1.2 –1.0 –0.8 –0.6 –0.4 Hedge’s d –0.2 0.0 0.2 0.4 Abundance (20) Richness (13) –1.2 –1.0 –0.8 –0.6 –0.4 Hedge’s d –0.2 0.0 0.2 0.4 igure 4 eptember 2011 12:49 ? ? ? ? ? ? ? ? ? ? 300 to 3,000 m radius a b Figure 3 Schematic showing the two study designs contrasted in this review. (a) Design focused on surrounding landscape cover. Sampling is generally done within a fixed habitat type. In the most common design, sites vary in the proportion of surrounding land cover composed of specific habitat types such as forest (dark green) ? ? ? ? ? ? ? 300 to 3,000 m radius gns contrasted in this review. (a) Design focused on surrounding done within a fixed habitat type. In the most common design, sites and cover composed of specific habitat types such as forest (dark green) hich landscape cover is assessed varies across studies but is typically ns, which we include in this category, vary either the linear distance to the habitat patch. (b) Design focused on local land-use type. These es among different habitat types. The surrounding landscape cover pe where pollinators are sampled are generally not reported. h show strong negative responses to land-use change in extreme in moderate systems (Supplemental Tables 2 and 3). Extreme in abundance and/or richness (e.g., Aizen & Feinsinger 1994, 2002, Ockinger & Smith 2006), whereas studies in moderately re varied responses (e.g., Bartomeus et al. 2010, Bergman et al. arisons across habitat types, rather than across landscape gra- ffects, and responses are predominantly positive for most taxa es, the ratio of negative-to-positive responses decreases from to 2.0 for moderate landscape studies, to 0.5 for across-habitat ratios decrease from 6.0 to 3.0 to 1.1, respectively (Supple- nses of syrphid flies and vertebrates are difficult to interpret dscape-scale studies that have been conducted (Supplemental ndance and/or richness often decrease with increasing human cape, but increase with conversion of natural to anthropogenic
  49. 49. a Extreme habitat loss Abundance (31) Richness (17) b Moderate habitat loss –1.4 –1.2 –1.0 –0.8 –0.6 –0.4 Hedge’s d –0.2 0.0 0.2 0.4 Abundance (20) Richness (13) –1.2 –1.0 –0.8 –0.6 –0.4 Hedge’s d –0.2 0.0 0.2 0.4 igure 4
  50. 50. Causes: Climate change Bartomeus et al. 2011 PNAS
  51. 51. daysfrom1January Phenology
  52. 52. daysfrom1January
  53. 53. daysfrom1January
  54. 54. daysfrom1January
  55. 55. daysfrom1January Year Time
  56. 56. daysfrom1January Year Temperature Time
  57. 57. Year Temperature Mean AprilTemperature daysfrom1January
  58. 58. daysfrom1January Year Temperature -10 species (Osmia, Andrena, Colletes & Bombus) -Early spring (Bombus queens)
  59. 59. daysfrom1January Year Temperature -Latitude -Sex -Day of collection -3447 specimens -763 collectors
  60. 60. daysfrom1January Year Temperature
  61. 61. daysfrom1January Year Temperature { ~10 days of mean advance
  62. 62. daysfrom1January Year Temperature { most dramatic advance in the last 40 years {
  63. 63. daysfrom1January Year Temperature Males Females Photo:AD Howell
  64. 64. daysfrom1January Year Temperature
  65. 65. daysfrom1January Year Temperature { Slope
  66. 66. By species: a measure of flight season for each species Advancingrate(days/year)
  67. 67. Andrena crataegi May Advancingrate(days/year)
  68. 68. Bombus impatiensAdvancingrate(days/year)
  69. 69. Osmia lignaria Advancingrate(days/year)
  70. 70. Colletes inaequalisApril Advancingrate(days/year)
  71. 71. Why Bee phenology is important? 85% of world plants are to some degree pollinated by animals (Ollerton et al 2011) Bees are the most effective pollinators (Neff & Simpson 1993)
  72. 72. Interactions have their own timing
  73. 73. 1885-2003 1936-1999 1936-2002 1971-1999 -0.4 -0.3 -0.2 -0.1 0.0 Slope We used 4 Published plant datasets in our study area All plants are commonly visited by the studied bees Advancingrate(days/year)
  74. 74. 1885-2003 1936-1999 1936-2002 1971-1999 -0.4 -0.3 -0.2 -0.1 0.0 SlopeAdvancingrate(days/year) Primack et al. 2004 (Massachusetts) No significant difference. 27 Plant species
  75. 75. 1885-2003 1936-1999 1936-2002 1971-1999 -0.4 -0.3 -0.2 -0.1 0.0 SlopeAdvancingrate(days/year) Bradley et al. 1999 (Wisconsin) 24 Plant species No significant difference.
  76. 76. 1885-2003 1936-1999 1936-2002 1971-1999 -0.4 -0.3 -0.2 -0.1 0.0 SlopeAdvancingrate(days/year) Cook et al. 2008 (NewYork State) 11 Plant species No significant difference.
  77. 77. 1885-2003 1936-1999 1936-2002 1971-1999 -0.4 -0.3 -0.2 -0.1 0.0 SlopeAdvancingrate(days/year) Abu-Asab et al. 2001 (Washington DC ) 44 Plant species No significant difference.
  78. 78. 1885-2003 1936-1999 1936-2002 1971-1999 -0.4 -0.3 -0.2 -0.1 0.0 SlopeAdvancingrate(days/year)
  79. 79. 1885-2003 1936-1999 1936-2002 1971-1999 -0.4 -0.3 -0.2 -0.1 0.0 SlopeAdvancingrate(days/year)
  80. 80. 1885-2003 1936-1999 1936-2002 1971-1999 -0.4 -0.3 -0.2 -0.1 0.0 SlopeAdvancingrate(days/year) Both “early” Bees and Plants show faster advances
  81. 81. Biodiversity as an insurance Bartomeus et al (in review)
  82. 82. 1960 1970 1980 1990 2000 2010 100120140160180200 Year Collectionday
  83. 83. 1960 1970 1980 1990 2000 2010 100120140160180200 Year Collectionday
  84. 84. year: p = 0.8; interaction sp*year: p = 0.01 baseline asynchrony stability
  85. 85. year: p = 0.8; interaction sp*year: p = 0.01
  86. 86. baseline asynchrony stability
  87. 87. Consequences for ecosystem services Bartomeus & Winfree 2013 F1000Research
  88. 88. 76% of crops are animal dependent (Klein et al 2007)
  89. 89. Repor compleme species (1 or “samp other mec evenness compleme dominant the most e date, the portance crop polli results (2 on pollina unknown, insect los evaluated pollinated We te from the a effectively crops, and placed by of honey (1) for m Wild Pollinators Enhance Fruit Set of Crops Regardless of Honey Bee Abundance Lucas A. Garibaldi,1 * Ingolf Steffan-Dewenter,2 Rachael Winfree,3 Marcelo A. Aizen,4 Riccardo Bommarco,5 Saul A. Cunningham,6 Claire Kremen,7 Luísa G. Carvalheiro,8,9 Lawrence D. Harder,10 Ohad Afik,11 Ignasi Bartomeus,12 Faye Benjamin,3 Virginie Boreux,13,14 Daniel Cariveau,3 Natacha P. Chacoff,15 Jan H. Dudenhöffer,16 Breno M. Freitas,17 Jaboury Ghazoul,14 Sarah Greenleaf,7 Juliana Hipólito,18 Andrea Holzschuh,2 Brad Howlett,19 Rufus Isaacs,20 Steven K. Javorek,21 Christina M. Kennedy,22 Kristin Krewenka,23 Smitha Krishnan,14 Yael Mandelik,11 Margaret M. Mayfield,24 Iris Motzke,13,23 Theodore Munyuli,25 Brian A. Nault,26 Mark Otieno,27 Jessica Petersen,26 Gideon Pisanty,11 Simon G. Potts,27 Romina Rader,28 Taylor H. Ricketts,29 Maj Rundlöf,5,30 Colleen L. Seymour,31 Christof Schüepp,32,33 Hajnalka Szentgyörgyi,34 Hisatomo Taki,35 Teja Tscharntke,23 Carlos H. Vergara,36 Blandina F. Viana,18 Thomas C. Wanger,23 Catrin Westphal,23 Neal Williams,37 Alexandra M. Klein13 *To whom correspondence should be addressed. E-mail: lgaribaldi@unrn.edu.ar Affiliations are listed at the end of the text
  90. 90. Trend Ecosystem Services Providers
  91. 91. *Richness weakly declining, except for Bombus *Specific responses are heterogenous. Only 4 species with steep declines. *Bees with short niche breadth and large body size are more likely to be affected. *ESP are less affected
  92. 92. Bees and plants have similar responses Climate change is altering bee phenology
  93. 93. Thank you - nacho.bartomeus@gmail.com This project is been possible thanks to... All collectors that collected the bees Co-authors: Rachael Winfree, John Ascher, Jason Gibbs, Bryan Danforth, David Wagner, Shannon Hedtke, Sheila Colla, Mia Park adn Dan Cariveau.
  94. 94. Local scale data from Burkle et al 2013 Science
  95. 95. April temperature is highly correlated with collection day.

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