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Historical changes in bee community
composition and phenology.
Is there a pollination crisis?
Ignasi Bartomeus
nacho.bartomeus@gmail.com
@ibartomeus
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% 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% 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
but… how are all these changes
affecting plants and animals?
Trends
Causes:
Land Use Change
Climate Change
Consequences
2010
Rachael
Winfree
you can
buy a
DeLorean
We could buy a
Delorean!
American Natural
History Museum
John Ascher
Database:
*Date
*Collector
*Coordinates
Assemble long-term data:
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.
Trends
Bartomeus et al 2013 PNAS
What do we know about the “pollinator crisis”?
What do we know about the “pollinator crisis”?
* Honeybees (managed)
* Bumblebees
Cameron et al. 2011Grixti et al. 2009,Colla et al. 2008,
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-
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)
What we know about all other >400 bee genera?
Biesmeijer et al. 2006
“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
Assemble long-term data:
* 47 bee genera comprising 438 species.
* >30,000 independently collected bee specimens
Assemble long-term data:
* >1500 collectors
* >11000 collection events
* 47 bee genera comprising 438 species.
Assemble long-term data:
* >1500 collectors
* >11000 collection events
* >30,000 independently collected bee specimens
Restrict Geographical area & check no temporal bias.
Use independently collected specimens
1) Richness
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
!
{
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”
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
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
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
2) Species level
Effort
Logistic regression estimate
1880 1900 1920 1940 1960 1980 2000
0.000.050.100.15
Halictus ligatus
Year
Proportionincollection
● ●●
●
●●●●●●●
●
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●
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1880 1900 1920 1940 1960 1980 2000
0.000.050.100.15
Andrena carlini
Year
Proportionincollection
● ●●● ●
●
●
●
●
●●
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●
●
●
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●
●
●
Logistic regression estimate
Effort
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
1880 1900 1920 1940 1960 1980 2000
0.000.050.100.15
Macropis patellata
Year
Proportionincollection
● ●●● ●●●●●●●●●●●●●●
●
●●●●●●
●
●
●
●
●
●
●●
●
●●●
●
●
●
●●●
●
●●●
●
●
●
●●●●
●
●
●
●●
●
●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●●
●
●●●●●●●●
●
●●●●●●●●
●
●●●●●●●●●●●●●●●●●●●●
Not
recently in
the
database
Macropis sp.
1880 1900 1920 1940 1960 1980 2000
0.00.20.40.60.81.0
Bombus affinis
Year
Presence/Absence
●
●
●●
●●●
●●●●●●
●
●
●
●
●●●●●
●
●●●●●●●●●●●●●●●●
●
●●●
●
●●●●●
●
●●●●●●●●●
●
●
●
●●●
●●
●
●
●
●
●●●●●●●●●●●●●●●●●●●●●●●●●●●●●
●
●●●●●●●●
●
●●●●●●
●
●●●●
●
●
●●●●●●●●●●
Bombus affinis
Bombus ashtoni
Bombus pensylvanicus
+ Macropis
patellata
3)Traits
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?
λ of the relative
change estimate = 0.24
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)
!
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)
!
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)
!
Causes:
Land use Change
Winfree, Bartomeus, Cariveau 2011 AREES
265 published studies,
contributing a total of
674 measures of
pollinator response to
anthropogenic land
use
40%
47%
13%
22%29%
49%
32%27%
41%
39%39%
21%
39%
30%
30%
Bees Butterflies Syrphid flies
Birds Bats
?
?
?
300 to 3,000 m radius
a
b
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
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
Causes:
Climate change
Bartomeus et al. 2011 PNAS
daysfrom1January
Phenology
daysfrom1January
daysfrom1January
daysfrom1January
daysfrom1January
Year
Time
daysfrom1January
Year
Temperature
Time
Year
Temperature
Mean AprilTemperature
daysfrom1January
daysfrom1January
Year
Temperature
-10 species (Osmia, Andrena,
Colletes & Bombus)
-Early spring (Bombus queens)
daysfrom1January
Year
Temperature
-Latitude
-Sex
-Day of collection
-3447 specimens
-763 collectors
daysfrom1January
Year
Temperature
daysfrom1January
Year
Temperature
{
~10 days of mean advance
daysfrom1January
Year
Temperature
{
most dramatic advance in the last 40 years
{
daysfrom1January
Year
Temperature
Males
Females
Photo:AD Howell
daysfrom1January
Year
Temperature
daysfrom1January
Year
Temperature
{
Slope
By species:
a measure of flight season for each species
Advancingrate(days/year)
Andrena crataegi
May
Advancingrate(days/year)
Bombus impatiensAdvancingrate(days/year)
Osmia lignaria
Advancingrate(days/year)
Colletes inaequalisApril
Advancingrate(days/year)
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)
Interactions have their own timing
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)
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
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.
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.
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.
1885-2003 1936-1999 1936-2002 1971-1999
-0.4
-0.3
-0.2
-0.1
0.0
SlopeAdvancingrate(days/year)
1885-2003 1936-1999 1936-2002 1971-1999
-0.4
-0.3
-0.2
-0.1
0.0
SlopeAdvancingrate(days/year)
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
Biodiversity as an insurance
Bartomeus et al (in review)
1960 1970 1980 1990 2000 2010
100120140160180200
Year
Collectionday
1960 1970 1980 1990 2000 2010
100120140160180200
Year
Collectionday
year: p = 0.8; interaction sp*year: p = 0.01
baseline
asynchrony
stability
year: p = 0.8; interaction sp*year: p = 0.01
baseline
asynchrony
stability
Consequences
for ecosystem
services
Bartomeus & Winfree 2013 F1000Research
76% of crops are animal dependent (Klein et al 2007)
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
Trend
Ecosystem
Services
Providers
*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
Bees and plants have similar responses
Climate change is altering bee phenology
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.
Local scale data from
Burkle et al 2013
Science
April temperature is highly correlated with collection day.

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