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33. N. L. Roberts, A. M. Piotrowski, J. F. McManus, L. D. Keigwin, ACKN OWLED GMEN TS the deglacial ventilation and circulation events from a more
Science 327, 75–78 (2010). This study was funded by the European Research Council, the broadened view.
34. W. Broecker, A. E. Putnam, Quat. Sci. Rev. 57, 17–25 Philip Leverhulme Trust, the U.S. National Science Foundation
(2012). (grants 0636787, 0944474, 0902957, and 1234664), and a Marie SUPPLEMENTARY MATERIALS
35. Y.-J. Wang et al., Science 294, 2345–2348 (2001). Curie Reintegration Grant. All the data reported in this paper are
36. K. A. Allen et al., Quat. Sci. Rev. 122, 180–191 (2015). www.sciencemag.org/content/349/6255/1537/suppl/DC1
available in the supplementary materials. We acknowledge the
37. Z. Liu et al., Science 325, 310–314 (2009). Materials and Methods
crew and science parties of RRS James Cook cruise JC094 and RV
Supplementary Text
38. P. Köhler, G. Knorr, E. Bard, Nat. Commun. 5, 5520 (2014). Nathaniel B. Palmer cruise NBP1103 who made this study possible.
Figs. S1 to S6
39. K. Matsumoto, Geophys. Res. Lett. 34, L20605 (2007). We also thank J. F. McManus and K. R. Hendry for the helpful
Tables S1 to S4
40. J. Southon, A. L. Noronha, H. Cheng, R. L. Edwards, Y. J. Wang, comments during the preparation of this manuscript and
References (42–54)
Quat. Sci. Rev. 33, 32–41 (2012). C. D. Coath, C. A. Taylor, S. Lucas, and C. Bertrand for help with
41. K. K. Andersen et al.North Greenland Ice Core Project sample preparation and analyses. Comments from two anonymous 20 May 2015; accepted 27 August 2015
members, Nature 431, 147–151 (2004). reviewers helped to improve the manuscript, inspiring us to look at 10.1126/science.aac6159

EVOLUTIONARY ECOLOGY 37.000′W), and Pennsylvania Mountain (39°15.803′N,

106°8.564′W).

Functional mismatch in a bumble bee B. sylvicola workers were collected from Niwot
Ridge and Pennsylvania Mountain. Mean tongue
length has decreased 0.61% annually and 24.4%
pollination mutualism under cumulatively in these taxa (F1,23 = 17.02, P = 0.0004
and F1,67 = 46.14, P < 0.0001) (Fig. 1 and table S1).
climate change

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Using archived specimens and field surveys of
bumble bees and host plants, we explored four
potential mechanisms for this change in tongue
Nicole E. Miller-Struttmann,1,2* Jennifer C. Geib,3 James D. Franklin,2 Peter G. Kevan,4 length: (i) decreasing body size, (ii) coevolution
Ricardo M. Holdo,2 Diane Ebert-May,5 Austin M. Lynn,2 Jessica A. Kettenbach,2,6 with floral traits, (iii) competition from subalpine
Elizabeth Hedrick,7 Candace Galen2 invaders, and (iv) diminishing floral resources.
Temporal changes in bumble bee tongue length
Ecological partnerships, or mutualisms, are globally widespread, sustaining agriculture and are not explained by plasticity in body size. When
biodiversity. Mutualisms evolve through the matching of functional traits between partners, phenotypic variance in tongue length is parti-
such as tongue length of pollinators and flower tube depth of plants. Long-tongued pollinators tioned among underlying sources, size accounts
specialize on flowers with deep corolla tubes, whereas shorter-tongued pollinators generalize for less than 20% of variation (table S1) (15). Size
across tube lengths. Losses of functional guilds because of shifts in global climate may disrupt has declined in some populations (B. balteatus:
mutualisms and threaten partner species. We found that in two alpine bumble bee species, F2,96 = 8.61, P = 0.0004; B. sylvicola: F1,76 = 29.01,
decreases in tongue length have evolved over 40 years. Co-occurring flowers have not become P < 0.0001) (fig. S1 and table S1) and is phe-
shallower, nor are small-flowered plants more prolific. We argue that declining floral resources notypically correlated with tongue length [corre-
because of warmer summers have favored generalist foraging, leading to a mismatch between lation coefficient (r) = 0.50 to 0.60, P < 0.005]
shorter-tongued bees and the longer-tubed plants they once pollinated. (fig. S1) but contributes little to its reduction over

L
time. After removing variance explained by body
ong-tongued bumble bees have coevolved ences resource acquisition and pollination effec- size, analysis of covariance shows significant tem-
to pollinate plants that possess elongated tiveness (9, 10). For bees, hummingbirds, bats, poral changes in tongue length (B. balteatus: F1,23 =
corolla tubes in a mutualistic relationship. moths, and flies, morphological matching in- 17.02, P = 0.0004; B. sylvicola: F1,67 = 46.14, P <
Recent declines in such long-tongued bee creases handling efficiency on flowers (9–14). 0.0001) (Fig. 1 and table S1).
populations suggest that historical selection Thus, changes that disrupt such matching can al- Selection to track the floral traits of host plants
regimes in these systems are changing (1–3), yet ter plant species recruitment and the trajectory of should favor short-tongued pollinators when flow-
the mechanisms driving these declines are un- coevolution. Although the climate change impacts ers become shallower or deep flowers less com-
clear. Spatial and temporal discrepancies with food on phenological and spatial overlap of mutualists mon (9, 10). We tested this hypothesis by comparing
plants, habitat destruction, and pressure from are well known, the role of climate change in flower depth of herbarium specimens collected
invasive competitors have been implicated (3–6), generating functional discrepancies between them from 1960–1982 and 2012–2013 near Mount
but the details of these declines and their causes is less understood. Using historical data, we show Evans and Niwot Ridge (15). In six species that
remain unresolved. that reduced flower abundance in bumble bee historically provided 88% of floral resources for
Matching of functional morphology between host-plants at the landscape scale has accompanied B. balteatus and B. sylvicola (18), the change in
partners increases benefits and reduces costs in recent warming, leading to evolutionary shifts in flower depth over time varied among species
mutualisms (7, 8). The match between flower foraging traits of two alpine bumble bee species (F6,13 = 9.42, P = 0.0004). Species that now have
tube depth and pollinator tongue length influ- (Bombus balteatus and B. sylvicola). Rapid evo- shallower flowers received few (<10%) bumble
lution of shorter tongues in these species may bee visits historically (fig. S2A). On Pennsylvania
1
Biological Sciences Department, Natural Sciences Building
inform our understanding of widespread declines Mountain and Niwot Ridge, short-tubed flowers
Rm NS247, SUNY College at Old Westbury, Old Westbury, NY in long-tongued Bombus specialists. show no systematic increase in abundance [co-
11568, USA. 2Division of Biological Sciences, University of We measured the change in tongue length of efficient of determination (R2) = 0.227, t1,4 = 1.21,
Missouri, Columbia, MO 65211, USA. 3Department of Biology, B. balteatus and B. sylvicola using specimens P = 0.294; R2 = 0.0004, t1,9 = –0.62, P = 0.952,
Appalachian State University, Boone, NC 28608, USA.
4
School of Environmental Sciences, University of Guelph,
collected from 1966–1980 and 2012–2014 in the respectively) (fig. S2, B and C), suggesting that
Guelph, ON, Canada N1G 2W1. 5Department of Plant Biology, central Rocky Mountains (15). These two species recent changes in floral trait distributions are
Michigan State University, East Lansing, MI 48824, USA. historically comprised 95 to 99% of bumble bees insufficient to drive tongue length adaptation
6
Department of Biological Sciences, Zoology Program, North at our high-altitude field sites (16–18). B. balteatus in bumble bees.
Carolina State University, Raleigh, NC 27695, USA.
7
Department of Life and Physical Sciences, Lincoln
workers were collected from three geographically Alternatively, shifts in bumble bee tongue
University, Jefferson City, MO 65101, USA. isolated locations: Mount Evans (39°35.033′N, length may reflect competition from subalpine
*Corresponding author. E-mail: [email protected] 105°38.307′W), Niwot Ridge (40°3.567′N, 105° congeners moving upward with climate change.

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R ES E A RC H | R E PO R TS

Comparisons of past (1960s and 1970s) (16, 17)

and present (2008 and 2011–2014) bumble bee
communities on Pennsylvania Mountain and in
the Front Range [Mount Evans and Niwot Ridge
combined (16)] indicate increased species diver-
sity (respectively, c2 = 293.4, df = 7, and c2 =
B. balteatus B. sylvicola
579.4, df = 12, P < 0.001) (Fig. 2, A and B),
12 12
past (1966-69, 77-80) past (1966-69, 77-80) immigration of short-tongued species from lower
present (2012-14) present (2012-14) altitudes, and a 24.1% decrease in the frequency of
10 10 long-tongued bees (Front Range: F1,1998 = 94,618,
Tongue length (mm)

* * * P < 0.0001; Pennsylvania Mountain: F1,1988 = 85.6,

8 8 P < 0.0001) (Fig. 2, C and D, and table S2) (15).
*
With increasing competition from immigrant spe-
6 6 cies, foraging breadth of resident bees should con-
tract (19, 20). Yet alpine bumble bee host choice
4 4 shows the opposite trend. In 2012–2014, we re-
surveyed bumble bee visitation on Mount Evans
2 2 and Niwot Ridge in accordance with historical
observations (18). Despite a 10-fold difference be-
0 0 tween past (n = 4099 visits observed) and pre-
Mt. Evans Niwot Ridge Penn. Mtn. Niwot Ridge Penn. Mtn. sent (n = 519 visits observed) collection effort,
Location

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Location surveys indicate that resident bumble bees have
broadened their diet. Resampling historical visita-
Fig. 1. Change in tongue length for B. balteatus and B. sylvicola on Mount Evans, Niwot Ridge, tion data to match present collection effort re-
and Pennsylvania Mountain. (A) B. balteatus. (B) B. sylvicola. Bars represent least squares means ± SE. veals that foraging breadth (Levin’s niche breadth)
(15). Asterisks denote significant differences (P < 0.05) between means. Dagger denotes a trend (15) increased from 2.61 to 7.01 for B. balteatus
(P < 0.06). [z score (Z) = 28.48, P < 0.0001] and 2.09 to 5.07

Mt. Evans and Niwot Ridge Pennsylvania Mountain

0.6
past (1966-69) 0.7 past (1977-79)
Proportion of community

Proportion of community
0.5 present (2012-14) present (2008,11,13)
0.6

0.4 0.5

0.4
0.3
0.3
0.2
0.2
0.1 0.1

0 0
B.hun B.ruf B.mix B.occ B.fri B.bif B.syl B.mel B.fla B.bal B.nev B.app B.mor B.mix B.fri B.bif B.syl B.cen B.fla B.bal B.nev
(na) (na) (5.09) (5.71) (5.73) (5.75) (5.79) (6.49) (7.81) (9.36) (10.13) (10.48) (11.83) (5.09) (5.73) (5.75) (5.79) (7.07) (7.81) (9.36) (10.13)
Bombus spp. (tongue length (mm)) Bombus spp. (tongue length (mm))

Mt. Evans and Niwot Ridge Pennsylvania Mountain B. balteatus B. sylvicola

0.6 0.4 0.6 0.6
past (1966-69) past (1977-79) past (1966-69) past (1966-69)
Density of bumble bees

Density of flowers visited

present (2012-14) present (2008,11,13) present (2012-14) present (2012-14)

0.5 0.5
0.3
0.4 0.4 0.4

0.2 0.3 0.3

0.2 0.2 0.2

0.1
0.1 0.1

0.0 0.0 0.0 0.0

2.5 5.0 7.5 10.0 12.5 2.5 5.0 7.5 10.0 12.5 0 5 10 15 20 0 5 10 15 20
Tongue length (mm) Tongue length (mm) Flower depth (mm) Flower depth (mm)

Fig. 2. Changing bumble bee community composition, bumble bee sity functions (15) indicates that bumble bee communities contain two
tongue length distributions, and tube depth distributions of visited predominant phenotypes, short-tongued and long-tongued [(C) and (D)].
flowers over time. (A and B) Bumble bee community composition. (C (E) and (F) show the tube depth density functions for flowers visited by,
and D) Bumble bee tongue length. (E and F) Flower tube depth dis- respectively, B. balteatus and B. sylvicola in the Front Range [Mount Evans
tribution. Bombus species abundance in alpine communities is indicated and Niwot Ridge (15)]. For tongue length [(C) and (D)] and tube depth [(E)
by the proportion of total foragers (15). Species are ordered by increasing and (F)], representative density functions for simulated communities (15)
tongue length [in (A), species’ names follow (18)]. Bimodality of the den- are shown.

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 RE S EAR CH | R E P O R T S

Fig. 3. Change in 10
flower abundance at past (1977-80)
*
8 present (2012-13)
landscape and local
00

Flowers m -2
scales along a 400-m 35 *

3800
6 *

3900
altitudinal gradient on

00
Pennsylvania Moun-

36
4

00

00
37
tain. (A) Map showing

35
areas where PFD 2
decreased (1.95 km2), is ¯
0
stable (1.29 km2), and
8

Total flower production

2
increased (0.10 km ). past (1977-80)
Unshaded (excluded) present (2012-13)
6
areas contain cliff, talus,

(millions)
N
mining disturbance, and
4
37

subalpine forest. (B)

00

PFD (mean ± SE) for 0 0.5 1 1.5 2

plots in krummholz 2
Kilometers
(KRUM); tundra slopes increasing PFD
decreasing PFD
(SLOPE); wet meadow 0
stable PFD excluded KRUM SLOPE SWALE FSUMMIT SUMMIT
(SWALE), false summit (3625) (3725) (3847) (3869) (3954)
(FSUMMIT); and sum- Habitat
mit (SUMMIT) habitats

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(altitude midpoint (m))
(N = 6 species; F4,385 =
5.55, P = 0.0002). Asterisks indicate significant differences at P < 0.05. (C) Total flower production (in millions) is the product of total surface area for (A) each habitat
(table S5) (15) and (B) mean PFD.

Fig. 4. Relative advantage 3.25°C) have become more frequent, occurring on

of generalizing as a func- Pennsylvania Mountain in only 12% of years from
tion of flower density and 1960 to 1985 but 48% of years since 1985 (c2 = 8.19,
the proportion of deep flow- df = 1, P < 0.0041) (fig. S3B).
ers in the community. Out- 3.0 On Pennsylvania Mountain, alpine bumble bees
comes with flight speed of 0.5 forage over hundreds of meters to provision their
m s−1 are shown (15). The 2.5 nests (28). To ask how warming has affected floral
Relative advantage

generalist is favored when its resources at this scale, we measured PFD of six
relative advantage is >1 (pink bumble bee host plants from 1977–1980 and 2012–
of generalist

2.0
shading). 2014 in five habitats along a 400-m altitudinal
1.5 span (table S5). Land surface area decreases with
altitude above tree line in the Rocky Mountains
1.0 (29), declining by more than an order of mag-
nitude on Pennsylvania Mountain, where 58%
0.5
0.2 of habitable terrain is found below 3800 m and
0.0 only 4% above 3938 m on the summit (Fig. 3A
0.4
10 and table S5). Because bumble bees forage across
we of
rs

8 0.6 the 400-m altitudinal range (28), we evaluated

flo on

6
ep rti

the temporal change in flower production at this

Flo 0.8
de opo

wer 4 landscape scale. For each habitat, we multiplied

s m -2 2
Pr

1.0 PFD (flowers per square meter) within sampling

plots by surface area (square meters) to estimate
of total flower production (15). PFD fell by 73 to
for B. sylvicola (Z = 19.78, P < 0.0001). Bumble records from Niwot Ridge show warming summer 80% within krummholz and slope habitats be-
bees have added flowers with shorter and more minimum temperatures over the past 56 years (27). low 3800 m, which occupy 1.95 km2. Conversely,
variable tube depth to their diet (B. balteatus: We see similar changes on Mount Evans (R2 = PFD increased by 75% in 0.10 km2 of summit
F1,1997 = 7554, P < 0.0001; B. sylvicola: F1,1997 = 0.383, t1,52 = 5.68, P < 0.0001) and Pennsylvania habitat (F4,385 = 5.55, P = 0.0002) (fig. 3B and
64,851, P < 0.0001) (Fig. 2, E and F, and table S3). Mountain (R2 = 0.341, t1,52 = 5.20, P < 0.0001) (fig. table S6). Because declines in flowering occurred
In response to warmer temperatures and dry- S3, A and B), where summer minimums have at low altitude, they affected the majority of the
ing soils, flowering has declined in alpine and increased ~2°C since 1960. We used a nonlinear mountain landscape; in these extensive habitats,
arctic habitats worldwide (21–24). Optimal for- model to characterize the relationship between millions of flowers were lost. Thus, even with
aging theory predicts that foragers will expand peak flower density (PFD; flowers per square gains of a few thousand flowers on the summit,
their niche in response to such resource scarcity meter) and summer minimum temperature. For total food resources for alpine bumble bees on
(25, 26). When bumble bees (B. balteatus) en- four bumble bee host species monitored in 6 years Pennsylvania Mountain have fallen by 60% since
counter low densities of preferred host plants, between 1977 and 2014 (15), average PFD on the 1970s (Fig. 3C).
they incorporate shallower flowers into their Pennsylvania Mountain rose as minimum summer Alpine regions are considered “canaries in the
diet (F1,194 = 29.39, P < 0.0001) (table S4) (15). The temperature increased from 1.8°C to 3.25°C but coal mine” for their sensitivity to global warming
expansion of foraging breadth over time in Front declined above this value (quadratic R2 = 0.19, t1,17 = (29). Using a simple model adapted from (26), we
Range bumble bees is congruent with this be- –2.18, P = 0.040) (fig. S3C) (15). Temperatures that tested whether reduced flowering in other eco-
havior (Fig. 2, E and F, and table S3). Climate are associated with reduced flowering (greater than systems could drive the evolution of pollinator

SCIENCE sciencemag.org 25 SEPTEMBER 2015 • VOL 349 ISSUE 6255 1543

R ES E A RC H | R E PO R TS

foraging traits as indicated for alpine bumble 30. G. H. Pyke, D. W. Inouye, J. D. Thomson, Environ. Entomol. 41, University of Colorado Herbarium; Colorado State University
bees (15). The model predicts changes in the en- 1332–1349 (2012). Herbarium; and the Missouri Botanical Garden loaned specimens.
31. D. Goulson, E. Nicholls, C. Botías, E. L. Rotheray, Science 347, Research was supported by NSF (grants DEB-79-10786 and
ergetic advantage of generalization with floral 1255957 (2015). 1045322). Data and specific code are archived at DOI: 10.5061/
density. Long-tongued bumble bees exhibit grea- dryad.10278 PRISM Climate Group data for Mount Evans and
ter specialization than that of short-tongued bees ACKN OWLED GMEN TS Pennsylvania Mountain are from www.prism.oregonstate.edu.
(16, 30). Across a range of flight speed and plant We acknowledge L. W. Macior and P. A. Byron for their meticulous
community composition (15), the advantage of work on Rocky Mountain bumble bees; J. Myrick, J. Guinnup,
SUPPLEMENTARY MATERIALS
A. Drew, L. Rimmer, J. Stoehr, M. Pallo, L. Hesh, and B. Lubinski
generalizing increases as flower density declines for laboratory and fieldwork; and the Mountain Research Station, www.sciencemag.org/content/349/6255/1541/suppl/DC1
(Fig. 4). Theoretical and empirical studies alike University of Colorado and Mount Evans Field Station, Denver Materials and Methods
suggest that with lower floral resources, fitness University for research facilities. The Arapaho National Forest, Figs. S1 to S4
Niwot Ridge Long-Term Ecological Research (NSF grant DEB- Tables S1 to S9
advantages of long-tongued specialist phenotypes References (32–59)
1027341) and Mountain Area Land Trust (Pennsylvania Mountain)
have diminished, potentially driving the rapid provided access to research sites. The Canadian National
evolution of shorter-tongued bees. We have doc- Collection of Insects; Rocky Mountain Herbarium, University of 9 March 2015; accepted 27 August 2015
umented decreases in bumble bee tongue length Wyoming; Kathryn Kalmbach Herbarium, Denver Botanic Garden; 10.1126/science.aab0868
within species and communities on three peaks
in the Rocky Mountains. Our analyses suggest that
reduced flower density at the landscape scale is
driving this shift in tongue length. Although pop- MITOCHONDRIAL IMPORT
ulations of long-tongued bees are undergoing
widespread decline (1, 3), shifts foraging strategies
may allow alpine bumble bees to cope with envi- Molecular architecture of the active

Downloaded from http://science.sciencemag.org/ on June 20, 2020

ronmental change. We see broader bumble bee
foraging niches, immigration by short-tongued
bumble bees, and shorter tongue length within
mitochondrial protein gate
resident bee populations as floral resources have
dwindled. In remote mountain habitats—largely Takuya Shiota,1,2 Kenichiro Imai,3 Jian Qiu,4* Victoria L. Hewitt,1† Khershing Tan,1
isolated from habitat destruction, toxins, and Hsin-Hui Shen,1 Noriyuki Sakiyama,3‡ Yoshinori Fukasawa,3 Sikander Hayat,5§
pathogens (31)—evolution is helping wild bees Megumi Kamiya,2 Arne Elofsson,5 Kentaro Tomii,3 Paul Horton,3 Nils Wiedemann,4,6
keep pace with climate change. Nikolaus Pfanner,4,6 Trevor Lithgow,1|| Toshiya Endo2,7||

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1544 25 SEPTEMBER 2015 • VOL 349 ISSUE 6255 sciencemag.org SCIENCE

Functional mismatch in a bumble bee pollination mutualism under climate change
Nicole E. Miller-Struttmann, Jennifer C. Geib, James D. Franklin, Peter G. Kevan, Ricardo M. Holdo, Diane Ebert-May, Austin
M. Lynn, Jessica A. Kettenbach, Elizabeth Hedrick and Candace Galen

Science 349 (6255), 1541-1544.

DOI: 10.1126/science.aab0868

Climate change decoupling mutualism

Many coevolved species have precisely matched traits. For example, long-tongued bumblebees are well adapted
for obtaining nectar from flowers with long petal tubes. Working at high altitude in Colorado, Miller-Struttmann et al. found
that long-tongued bumblebees have decreased in number significantly over the past 40 years. Short-tongued species,
which are able to feed on many types of flowers, are replacing them. This shift seems to be a direct result of warming

Downloaded from http://science.sciencemag.org/ on June 20, 2020

summers reducing flower availability, making generalist bumblebees more successful than specialists and resulting in the
disruption of long-held mutualisms.
Science, this issue p. 1541

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