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Climate change impacts on bumblebees converge across continents. [DOWNLOAD reprint at: http://www.macroecology.ca/Papers.html]

July 2015
Science 349(6244):177-180

DOI:10.1126/science.aaa7031

Authors:

Jeremy Kerr

University of Ottawa

Alana Pindar

University of Guelph

Paul Galpern

The University of Calgary

Laurence Packer

York University

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For many species, geographical ranges are expanding toward the poles in response to climate change, while remaining stable along range edges nearest the equator. Using long-term observations across Europe and North America over 110 years, we tested for climate change–related range shifts in bumblebee species across the full extents of their latitudinal and thermal limits and movements along elevation gradients. We found cross-continentally consistent trends in failures to track warming through time at species’ northern range limits, range losses from southern range limits, and shifts to higher elevations among southern species. These effects are independent of changing land uses or pesticide applications and underscore the need to test for climate impacts at both leading and trailing latitudinal and thermal limits for species. Bucking the trend Responses to climate change have been observed across many species. There is a general trend for species to shift their ranges poleward or up in elevation. Not all species, however, can make such shifts, and these species might experience more rapid declines. Kerr et al. looked at data on bumblebees across North America and Europe over the past 110 years. Bumblebees have not shifted northward and are experiencing shrinking distributions in the southern ends of their range. Such failures to shift may be because of their origins in a cooler climate, and suggest an elevated susceptibility to rapid climate change. Science, this issue p. 177

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This suggests predictive limits of our approach,

in that more-connected systems with more soil

evaporation and less-connected systems with

less soil evaporation will produce similar con-

tinental output flux isotope ratios.

The terrestrial hydrologic partitioning esti-

mated here corresponds to a total transpiration

of 55,000 ± 12,000 km

per year (mean ± 1 SD), a

total soil evaporation of 5000 ± 4000 km

per

year, and a total surface water evaporation of

2000 ± 2000 km

per year, assuming an inter-

ception of 23,000 ± 10,000 km

per year ( 27)

and a continental precipitation of 115,000 ±

2000 km

per year (28) (Fig. 3). The transpired

fraction determined here is consistent with

previous meta-analyses (Fig. 1C) and places an

observational constraint on transpiration esti-

mates from global Earth system models, which

range between 38 and 80% (4–6, 29). The frac-

tion of total evapotranspiration flux occurring

from surface waters, 2.9%, is also consistent with

values from global Earth system models, which

range from 2 to 4% when reported (29). Globally,

tropical forests provide the bulk of continental

transpiration, although these regions contribute

modest amounts of soil and surface water evap-

oration as well.

Transpiration fluxes form the primary link

between the water and carbon cycles, with water

lost from plant stomata du ring carbon assimila-

tion (i.e., plant water use efficiency) being a critical

factor determining ecosystem function and pro-

ductivity. Although we estimate that plant tran-

spiration is a majority of the evapotranspiration

flux, our results demonstrate that previous par-

titioning approaches may overestimate the con-

tribution of transpiration, because they do not

consider evaporation from multiple catchment

water pools and their connectivity. Furthermore,

isotopic partitioning approaches are sensitive to

bulk flux estimates and their uncertainti es, as

well as assumptions about interception rates, with

larger interception isotopically indistinguishable

from increased transpiration because both fluxes

areoftenassumedtobeunfractionatedrelativeto

their source waters (6, 20). Because a majority of

evaporation occurs from soils and not open

waters, more knowledge is needed of the role of

ecosystem structure and microclimate in deter-

mining sub-canopy evaporation rates.

Finally, the partial hydrologic disconnect be-

tween bound and mobile waters, which our es-

timates suggest is substantial and pervasive at

the global scale, has implications for prediction

and monitoring of both water quantity and qual-

ity within streams and rive rs. The hydrologic and

hydrochemical properties of surface water sys-

temsarestronglyinfluencedbyphysicalflow

paths within the near surface, and the low con-

nectivity found here suggests, for example, that

stream biogeochemistry may be less sensitive to

soil zone processes than it would be if hydrologic

connectivity were higher . Although we determined

a single average connectivity value, connectivity

varies with geography and in time as preferential

flow paths are activated and deactivated through-

out the year (30). Indeed, the relation between the

connectivity metric and soil-water transit time dis-

tributions is likely to be complex. Given the ubiq-

uitous nature of both water quantity and water

quality issues affecting watersheds worldwide, an

improved understanding of hydrologic connectivity

at variety of temporal and spatial scales is essential.

REFERENCES AND NOTES

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AC KN OW LE D GM E NT S

This project was funded by the NSF Macrosystems Biology

program, grant EF-01241286, and the U.S. Department of Defense.

D.N. acknowledges the support of the NSF Climate and Large Scale

Dynamic program as part of a Faculty Early Career Development

award (AGS-0955841). Support and resources from the Center for

High Performance Computing at the University of Utah are also

gratefully acknowledged. Bulk flux data used in this study are

available online from NASA (http://precip.gsfc.nasa.gov/,

http://gmao.gsfc.nasa.gov/merra/) and the Woods Hole

Oceanographic Institute (http://oaflux.whoi.edu/). Global surface

vapor isotope data are available as supplementary information in

(23). The model code and input data files used in this study are

available at http://waterisotopes.org.

SUPPLEMENTARY MATERIALS

www.sciencemag.org/content/349/6244/175/suppl/DC1

Materials and Methods

Figs. S1 to S3

References (31–37)

7 January 2015; accepted 2 June 2015

10.1126/science.aaa5931

CLIMATE CHANGE

Climate change impacts

on bumblebees converge

across continents

Jeremy T. Kerr,

* Alana Pindar,

Paul Galpern,

Laurence Packer,

Simon G. Potts,

Stuart M. Roberts,

Pierre Rasmont,

Oliver Schweiger,

Sheila R. Colla,

Leif L. Richardson,

David L. Wagner,

Lawrence F. Gall,

Derek S. Sikes,

Alberto Pantoja

†

For many species, geographical ranges are expanding toward the poles in response to

climate change, while remaining stable along range edges nearest the equator. Using

long-term observations across Europe and North America over 110 years, we tested for

climate change–related range shifts in bumblebee species across the full extents of their

latitudinal and thermal limits and movements along elevation gradients. We found

cross-continentally consistent trends in failures to track warming through time at species’

northern range limits, range losses from southern range limits, and shifts to higher

elevations among southern species. These effects are independent of changing land uses

or pesticide applications and underscore the need to test for climate impacts at both

leading and trailing latitudinal and thermal limits for species.

iological effects of climate change threaten

many species (1), necessitating advances in

techniques to assess their vulnerabilities

(2). In addition to shifts in the timing of

species’ life cycles, warming has caused

range expansion toward the poles and higher

elevations (3–6). Climate impacts could cause

losses from parts of species’ trailing range margins

(7), but those losses are infrequent ly observed (4).

Such responses depend on species’ traits, such as

SCIENCE sciencema g.org 10 JULY 2015 • VOL 349 ISSUE 6244 177

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heat or cold tolerance, that reflect shared evolu-

tionary history and climatic origins (e.g., tropical

or temperate) of taxa (8, 9). Climate change can

interact with other threats, like land-use intensi-

fication, to alter species’ responses to emerging

conditions (10). Such global changes can alter or

erode ecological services provided by the affected

species (11). Few species assemblages contribute

more to these services than bumblebees (Bombus),

many of which are declining (12, 13). No study has

yet evaluated climate change impacts across the

latitudinal and thermal limits of such a large spe-

cies assemblage spanning two continents.

We assembled a database of ~423,000 georef-

erenced observations for 67 European and North

American bumblebee species (fig. S1 and tables S1

and S2). Species observations were gathered from

the Global Biodiversity Information Facility (171,4 79

North American and 192,039 European records)

(14), Bumblebees of North America (15)(153,023

records), and the Status and Trends of European

Pollinators Collaborative Project (237,586 records).

We measured differences in species’ northern

and southern range limits, the warmest or coolest

temperatures occupied, and their mean elevations

in three periods (1975 to 1986, 1987 to 1998, and

1999 to 2010) (figs. S2 to S4) relative to a baseline

period (1901 to 1974) (16). We investig ated whether

land use affected these results. Finally, we used

high-resolution pesticide application data avail-

able in the United States after 1991 to investigate

whether total pesticide or neonicotinoid applica-

tions accounted for changes in bumblebee species’

range or thermal limits (table S3). Tests used

phylogenetic generalized least-squares models

(PGLS), using a phylogenetic tree constructed

from nuclear and mitochondrial markers (17), and

accounted for differences in sampling intensity

between time periods (Table 1).

If species expanded their northern range limits

to track recent warming, their ranges should show

positive (northward) latitudinal shifts, but cool

thermal limits should be stable through time. In

contrast to expectations and responses known

from other taxa (4), there has been no change in

the northern limits of bumblebee distributions

in North America or Europe (Fig. 1A). Despite

substantial warming (~ +2.5°C), bumblebee spe-

cies have also failed to track warming along their

cool thermal limits on both continents (Fig. 1B

and Table 1). These failures to track climate change

occur in parallel in regions that differ in their

intensities of human land use (e.g., Canada and nor-

thern Europe), which had no direct or interaction-

based effect in any statistical model (Table 1).

If bumblebee species climate responses resem-

ble most terrestrial ectotherm taxa (4), their south-

ern range limits should have remained stable with

increasing temperatures along species’ warm ther-

mal limits. However, bumblebee species’ range

losses from their historical southern limits have

been pronounced in both Europe and North

America, with losses growing to ~300 km in south-

ern areas on both continents (Fig. 1C). Throughout

North America, species also experienced range

losses from the warmest areas they historically

occupied, while European species’ range losses

extend across the warmest regions (where mean

temperatures exceed ~15°C) (Fig. 1D). These re-

sponses showed a significant phylogenetic signal,

with closely related bumblebee species showing

increasingly similar range shifts from southern

and warm thermal limits (Table 1). As with fail-

ures to expand northward or into cooler areas,

land-use changes do not relate to range losses

from bumblebee species’ southern or warm ther-

mal limits.

178 10 JULY 2015 • VOL 349 ISSUE 6244 sciencemag.org SCIENCE

Department of Biology, University of Ottawa, Ottawa, ON,

Canada, K1N6N5.

Faculty of Environmental Design,

University of Calgary, Calgary, Alberta, Canada.

Department

of Biology, York University, Toronto, Ontario, Canada.

School of Agriculture, Policy and Development, The

University of Reading, Reading, UK.

Department of Zoology,

Université de Mons, Mons, Belgium.

Department of

Community Ecology, Helmholtz Centre for Environmental

Research, Halle, Germany.

Wildlife Preservation Canada,

Guelph, Ontario, Canada.

Gund Institute, University of

Vermont, Burlington, VT, USA.

Department of Ecology and

Evolutionary Biology, University of Connecticut, Storrs, CT,

USA.

Peabody Museum of Natural Histo ry, Entomology

Division, Yale University, New Haven, CT, USA.

University of

Alaska Museum, University of Alaska Fairbanks, Fairbanks,

AK, USA.

United States Department of Agriculture,

Agricultural Research Service, Subarctic Agricultural

Research Unit, Fairbanks, AK, USA.

*Corresponding author. E-mail: jkerr@uottawa.ca †Present

address: United Nations Food and Agriculture Organization,

Santiago, Chile.

Table 1. PGLS models showing climate change and interactive effects

on North American and European bumblebees. Changes in latitude (km

north of equator), thermal (°C), or elevation (m) variables observed by 1999

to 2010 for ea ch species (relative to the 1901 to 1974 baseline period) are

regressed against predictors listed on the left. Models reported in each col-

umn were selected using AIC, which can include statistically nonsignificant

variables. Sample sizes in each time period (median n per species = 536)

were tested but excluded using AIC. Variable coefficients are given, with SEs

in parentheses. A dash indicates that this variable was not part of the AIC-

selected model. Ordinary least squares (OLS) regression summary statistics

(adjusted R

) are provided to enable comparison with PGLS results; OLS co-

efficients are similar.

Latitude Thermal

Elevation

Predictors

Northern Southern Cool Warm

Intercept –268.3 (614.7) 657.8 (150.4) 2.436 (0.5) 657.8 (150.4) 1075 (340.7)

............ ................ ................ ................ ............... ................ ................ ................ ............. ................ ............... ................ ................ ................ ................ ............... ................ ................ ................ ................ ............... .......

Latitudinal or thermal limit (1901–1974) 0.04 (0.08) –0.12 (0.04) –0.009 (0.05) 0.19 (0.1) –

Mean latitude (1999–2010) –––––0.21 (0.07)

Covariates

Continent 1158 (1039) ––10.59 (2.24) 384.5 (504.1)

D Crop land (1999–2010) –4.25 (7.68) ––––

D Pasture (1999–2010) –43.1 (60.71) ––––

Interactions with continent

Thermal or latitudinal limits (1901–1974) –0.12 (0.14) –––0.47 (0.12) –

D Crop land (1999–2010) –9.38 (41.73) ––––

D Pasture (1999–2010) 74.95 (74.35) ––––

Mean latitude (1999–2010) –––––0.03 (0.1)

Models of trait evolution

AIC (Independent) 915.5 863.2 291.3 274.5 863.6

AIC (Brownian motion) 962.4 897.4 339.3 293.9 916.4

AIC (Ornstein-Uhlenbeck) 917.5 861.8 293.3 264.9 865.4

AIC (Pagel) 915.3 862.2 293.1 273 860.8

Pagel’s l –0.15 0.49 0.04 0.64 –0.1

Equivalent OLS regression summary statistics

Adjusted R

0.15 0.14 –0.01 0.30 0.28

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Species with southern geographical ranges re-

treated to higher elevations across Europe and

North America (Table 1 and Fig. 2), consistent with

observations of range losses from their southern

range limits. Elevation shifts are larger in Europe

[i.e., Akaike’s information criterion (AIC)–based

model selection includes a small continental ef-

fect; intercept for Europe, 1459 m (366 SE); North

America, 1074 m (340 SE) (Fig. 2)]. Europe’smoun-

tainous areas are oriented predominantly east-west,

potentially inducing more pronounced upslope

shifts. Mean elevations of observations for south-

ern species have risen ~300 m since 1974. Observed

shifts along elevation gradients vary considera-

bly among species (3) but follow a coherent geo-

graphical pattern. Mean elevations among northern

species in Europe and North America shifted lower .

Over recent decades, alpine tree lines have advanced

upslope in response to human activities, geomor-

phological factors, and warming (18), potentially

overtaking nesting, overwintering, and forage hab-

itats in historically open areas. High-elevation hab-

itat changes could contribute to generalist pollinator

declines in mountainous areas (19), particularly

among bumblebee species whose ranges have not

expanded from their cold thermal limits.

In addition to land-use changes, we investigated

whether pesticide use affected shifts in thermal and

latitudinal range limits among bumblebees. Spa-

tially detailed, annual pesticide measurements,

including neonicotinoid insecticides, were available

for the United States after 1991. Neither total

pesticide nor neonicotinoid applications there

relate to observed shifts in bumblebee species’

historical ranges or thermal limits (table S1).

Neonicotinoid effects known from individual and

colony levels certainly contribute to pollinator de-

clines and could degrade local pollination services.

Neonicotinoid effects on bumblebees have been

demonstrated experimentally using field-realistic

treatments (20). These locally important effects do

not “scale up” to explain cross-continental shifts

along bumblebee species’ thermal or latitudinal

limits. The timing of climate change–related shifts

among bumblebee species underscores this obser-

vation: Range losses from species’ southern limits

and failures to track warming conditions began

before widespread use of neonicotinoid pesticides

(figs. S2 and S3).

Regional analyses suggest that latitudinal range

shifts toward the poles are accelerating in most

speciesgroups(3), while their trailing range mar-

gins remain relatively stable (4). Assemblages

showing pronounced northward range expan-

sions and limited southern-range losses, like

butt erflies, originated and diversified in tropical

climates and retain ancestral tolerances to warmer

condition s (21). Those species’ warming-related

extinction risks in temperate environment s are

low (8) but increase toward warmer areas where

climatic conditions resemble those under which

they evolved (7, 22). Drawing on comprehensive

range data, bumblebee species show opposite range

responses across continents relative to most ter-

restrial assemblages (4): rapid losses from the

south and lagging range expansions in the north.

Mechanisms leading to observed lags in range

responses at species’ northern or cool thermal

limits require urgent evaluation. Colonization of

previously unoccupied areas and maintenance of

new populations strongly affect whether species

track shifting climatic conditions (23), capacities

that appear insufficient among bumblebees. Ob-

served losses from species’ southern or warm

boundaries in Europe and North America, and

associated phylogenetic signals, are consistent

with ancestral limitations of bumblebees’ warm

thermal tolerances and evolutionary origins in

cool Palearctic conditions (24). Warming-related

extreme events cause bumblebee population losses

(25)byimposingdemandsfor energetically cost-

ly behavioral thermoregulation, even at high lati-

tudes and elevations (26). Such effects are not

yet observed for European bumblebees in cooler

regions, where species generally experience tem-

peratures exceeding those observed historically

within their ranges (Fig. 1D) (10). Range losses

there will likely accelerate without mitigation

from climatic refugia (27).

SCIENCE sciencema g.org 10 JULY 2015 • VOL 349 ISSUE 6244 179

Fig. 1. Climate change responses of 67 bumblebee species across full latitudinal and thermal lim-

its in Europe and North America. For each measur ement , the y axis shows differences in the latitude

of species’ range limits [(A) Northern, (C) Southern] or thermal limits [(B)Cool;(D) Warm], respectiv ely,

by 1999 to 2010 relativ e to baseline conditions for 1901 to 1974. Each point represents the mean of five

observations at the latitudinal or thermal limits for one bumblebee species (gr een circles for Europe and

pink for North America). Null expectations (dashed lines) are for no temporal change in latitudinal or

thermal limits. Range e xpansions from species’ historical northern limits (A) are indicated by positive

values, and positive values indicate range losses from species’ southern limits (B). Temperature changes

show whether bumblebee species are tracking differences along their thermal limits through time (no

change) , falling behind (positive values ), or retr eating mor e rapidly than mean conditions detect (negativ e

values ). Confidence bands (95%) f or regr essi on models (i.e ., with and withou t continent + interaction

against latitudinal or thermal change terms) with the lowest AIC are shown.

Fig. 2. Change in elevation of 67 bumblebee

species by 1999 to 2010 relative to their mean

latitude. Eleva tions are calculated using mean ele-

vations across species observations. The slopes are

similar between continents (according to regr ession

and PGLS analyses). The confidence bands (95%)

of regression slopes are shown.

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Climatechangeappearstocontributedistinc-

tively, and consistently, to accumulating range

compression among bumblebee species across

continents. Experimental relocation of bumble-

bee colonies into new areas could mitigate these

range losses. Assessments of climate change on

species’ ranges need to account for observations

across the full extent of species’ latitudinal and

thermal limits and explicitly test for interactions

with other global change drivers.

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ACK NOW LED GME NTS

This research was funded by the Natural Sciences and Engineering

Research Council of Canada strategic network (CANPOLIN:

Canadian Pollination Initiative) and Discovery Grant support and

University of Ottawa Research Chair in Macroecology and

Conservation to J.T.K. We are grateful to anonymous reviewers

whose comments improved this paper and to P. Williams for advice

and perspectives during development of the research. All data and

supporting scripts are available from Dryad Digital Repository:

doi:10.5061/dryad.gf774.

SUPPLEMENTARY MATERIALS

www.sciencemag.org/content/349/6244/177/suppl/DC1

Materials and Methods

Supplementary Text

Supplementary Acknowledgments

Figs. S1 to S4

Tables S1 to S3

References (28–55)

15 January 2015; accepted 21 May 2015

10.1126/science.aaa7031

PLACE CELLS

Autoassociative dynamics in the

generation of sequences of

hippocampal place cells

Brad E. Pfeiffer* and David J. Foster†

Neuronal circuits produce self-sustaining sequences of activity patterns, but the precise

mechanisms remain unknown. Here we provide evidence for autoassociative dynamics in

sequence generation. During sharp-wave ripple (SWR) events, hippocampal neurons

express sequenced reactivations, which we show are composed of discrete attractors.

Each attractor corresponds to a single location, the representation of which sharpens

over the course of several milliseconds, as the reactivation focuses at that location.

Subsequently, the reactivation transitions rapidly to a spatially discontiguous location. This

alternation between sharpening and transition occurs repeatedly within individual SWRs

and is locked to the slow-gamma (25 to 50 hertz) rhythm. These findings support

theoretical notions of neural network function and reveal a fundamental discretization

in the retrieval of memory in the hippocampus, together with a function for gamma

oscillations in the control of attractor dynamics.

n the well-known Hopfield model, a network

of recurrently excitable neurons stores dis-

cretememoriesasstableactivitypatterns

(attractors) to which partial patterns are

guaranteed to converge, based on synaptic

weights reflecting correlations between neu-

rons in the same pattern (“autoassociation”)

(1). Sequences of patterns can also be stored,

based on weights reflecting correlations be-

tween different patterns (“heteroassociation”),

but are generally unsustainable because any

noise leads to divergence in subsequent patterns.

A solution is to combine fast autoassociation for

each pattern with slower heteroassociation for

successive patterns, allowing each pattern to

be corrected via attractor network dynamics

before transitioning to the next pattern in the se-

quence (2, 3). This process should result in “jumpy”

sequences that sharpen individual pattern rep-

resentations before transitioning to successive

patterns; however, direct evidence is lacking, due

largely to the difficulty of obtaining data from

very large ensembles of neurons express ing inter-

nally generated sequences recorded at the time

resolution of neuronal dynamics.

Hippocampal SWR-associated place-cell se-

quences (4–10), often termed “replay,” are a unique

experimental model in which neurons with well-

defined receptive fields are activated outside those

receptive fields and in specific temporal sequen-

ces corresponding to physical trajectories through

space, all while the animal is stationary, and thus

in the absence of corresponding sequences of

stimuli or behaviors. We recently develo pe d meth -

ods to record simultaneously from very large num-

bers of hippocampal neurons (up to 263) with

place fields in a single environment (10), and we

applied these recording techniques to examine

the fine structure of SWR-associated place-cell

sequences to investigate the underlying mech-

anisms of this form of memory expression and

explore the circuit-level dynamics of an attrac-

tor system in vivo.

We recorded bilateral ensemble activity from

dorsal hippocampal neurons (figs. S1 and S2) of

five rat subjects across multiple recording ses-

sions as they explored open arenas or linear tracks

(Fig.1,A,B,G,andH).Weobtainedsimultaneous

recordings from large populations of hippocam-

pal neurons in each recording session (80 to 263

units per session; mean ± SEM = 159.2 ± 11.8 units

per session), allowing us to accurately decode

spatial informat ion from the hippocampal ensem-

ble activity patterns using a memory-less, uniform-

prior Bayesian decoding algorithm (fig. S3) (5, 10).

We identified SWRs that encoded temporally com-

pressed spatial trajectories through the current

environment (Fig. 1, C to F and I to L, and fig. S4)

(10), which we term “trajectory events” rather than

“replay” to reflect the observation that SWRs do

not always represent a perfect replay of imme-

diately prior behavior but instead reflect a more

broad array of spatial paths (8–10). Across all

sessions in the open field and linear track, we

identified 815 and 564 SWR events, respectively,

that met our criteria to be classified as trajectory

events.

Consistent with prior reports (5), trajectory events

displayed average velocities in a relatively nar-

row range (Fig. 2A); however , when we examined

trajectory events on a finer time scale, we ob-

served discontinuous trajectories, alternating be-

tween immobility (in which consecutive decoding

frames represented the same location) and rapid

movement (in which consecutive frames repre-

sented a sequential path of unique positions; fig.

180 10 JULY 2015 • VO L 34 9 IS SUE 6244 sciencemag.org SCIENCE

Solomon H. Snyder Department of Neuroscience, Johns

Hopkins University School of Medicine, Baltimore, MD, USA.

*Present address: Department of Neuroscience, University of

Texas Southwestern Medical Center, Dallas, TX, USA.

†Corresponding author. E-mail: david.foster@jhu.edu

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(6244), 177-180. [doi: 10.1126/science.aaa7031]349Science

2015)Lawrence F. Gall, Derek S. Sikes and Alberto Pantoja (July 9,

Schweiger, Sheila R. Colla, Leif L. Richardson, David L. Wagner,

Simon G. Potts, Stuart M. Roberts, Pierre Rasmont, Oliver

Jeremy T. Kerr, Alana Pindar, Paul Galpern, Laurence Packer,

continents

Climate change impacts on bumblebees converge across

Editor's Summary

, this issue p. 177Science

change.

because of their origins in a cooler climate, and suggest an elevated susceptibility to rapid climate

are experiencing shrinking distributions in the southern ends of their range. Such failures to shift may be

across North America and Europe over the past 110 years. Bumblebees have not shifted northward and

looked at data on bumblebeeset al.shifts, and these species might experience more rapid declines. Kerr

for species to shift their ranges poleward or up in elevation. Not all species, however, can make such

Responses to climate change have been observed across many species. There is a general trend

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Variance in heat tolerance in bumble bees correlates with species geographic range and is associated with several environmental and biological factors

Article

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Globally, insects have been impacted by climate change, with bumble bees in particular showing range shifts and declining species diversity with global warming. This suggests heat tolerance is a likely factor limiting the distribution and success of these bees. Studies have shown high intraspecific variance in bumble bee thermal tolerance, suggesting biological and environmental factors may be impacting heat resilience. Understanding these factors is important for assessing vulnerability and finding environmental solutions to mitigate effects of climate change. In this study, we assess whether geographic range variation in bumble bees in the eastern United States is associated with heat tolerance and further dissect which other biological and environmental factors explain variation in heat sensitivity in these bees. We examine heat tolerance by caste, sex, and rearing condition (wild/lab) across six eastern US bumble bee species, and assess the role of age, reproductive status, body size, and interactive effects of humidity and temperature on thermal tolerance in Bombus impatiens . We found marked differences in heat tolerance by species that correlate with each species' latitudinal range, habitat, and climatic niche, and we found significant variation in thermal sensitivity by caste and sex. Queens had considerably lower heat tolerance than workers and males, with greater tolerance when queens would first be leaving their natal nest, and lower tolerance after ovary activation. Wild bees tended to have higher heat tolerance than lab reared bees, and body size was associated with heat tolerance only in wild‐caught foragers. Humidity showed a strong interaction with heat effects, pointing to the need to regulate relative humidity in thermal assays and consider its role in nature. Altogether, we found most tested biological conditions impact thermal tolerance and highlight the stages of these bees that will be most sensitive to future climate change.

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As climatic and other impactful environmental changes continue to gain momentum pollination, services are poised to be harmed, and wild bee species are not an exception. In the present study, maximum entropy (MaxEnt) modeling was used to predict the potential climatic niches of five wild bee species, namely, Chalicodoma flavipes, Chalicodoma sicula, Coelioxys coturnix, Megachile minutissima, and Osmia submicans (all of Megachilidae: Megachilinae). The Maxent model performed better than random for the five species, and all model predictions were significantly robust, giving ratios above null expectations. Under future climate change scenarios, the Maxent model predicted habitat loss for C. flavipes, C. sicula, and M. minutissima in North Africa and habitat loss for O. submicans in Europe and North Africa in all scenarios. Conversely, the study showed that the cleptoparasitic bee Co. coturnix would expand their suitable habitat in most scenarios in Europe, Asia, and the United States, although this species would also suffer habitat loss in North Africa in two scenarios. Between the present situation and future scenarios, the potential distribution for all species decreased in their suitable habitat, with the exception of Co. coturnix. The present results are of considerable value for informed conservation programs and policy decisions regarding wild pollinators.

Sublethal doses of insecticide reduce thermal tolerance of a stingless bee and are not avoided in a resource choice test

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Insecticides and climate change are among the multiple stressors that bees face, but little is known about their synergistic effects, especially for non-Apis bee species. In laboratory experiments, we tested whether the stingless bee Tetragonula hockingsi avoids insecticide in sucrose solutions and how T. hockingsi responds to insecticide and heat stress combined. We found that T. hockingsi neither preferred nor avoided sucrose solutions with either low (2.5 × 10⁻⁴ ng µl⁻¹ imidacloprid or 1.0 × 10⁻⁴ ng µl⁻¹ fipronil) or high (2.5 × 10⁻³ ng µl⁻¹ imidacloprid or 1.0 × 10⁻³ ng µl⁻¹ fipronil) insecticide concentrations when offered alongside sucrose without insecticide. In our combined stress experiment, the smallest dose of imidacloprid (7.5 × 10⁻⁴ ng) did not significantly affect thermal tolerance (CTmax). However, CTmax significantly reduced by 0.8°C (±0.16 SE) and by 0.5°C (±0.16 SE) when bees were fed as little as 7.5 × 10⁻³ ng of imidacloprid or 3.0 × 10⁻⁴ ng of fipronil, respectively, and as much as 1.5°C (±0.16 SE) and 1.2°C (±0.16 SE) when bees were fed 7.5 × 10⁻² ng of imidacloprid or 3.0 × 10⁻² ng of fipronil, respectively. Predictions of temperature increase, and increased insecticide use in the tropics suggest that T. hockingsi will be at increased risk of the effects of both stressors in the future.

Macroecological perspectives on the competition between the native and invasive bumblebees in southern South America under climate change

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Nov 2023
BIOL INVASIONS

Bombus dahlbomii. We gathered a comprehensive database of occurrence records for B. dahlbomii, B. ruderatus, and B. terrestris from museums and citizen science sources. Multivariate bioclimatic niche analyses and species distribution models were used to determine the extent of climatic niche overlap between invasive and native species and the potential effects of current and future climatic scenarios on the distribution of these bumblebees. We found extensive pairwise niche overlap between the three bumble bee species, B. terrestris versus B. ruderatus (67%), B. terrestris versus B. dahlbomii (61%), and B. ruderatus versus B. dahlbomii (46%). Compared to its historical records, the current distribution of B. dahlbomii is narrowing and is expected to shrink even more under the most climatically pessimistic future scenario, while that of B. terrestris shows an extensive, still expanding distribution. However, the models show that in the case of a climatic pessimistic future scenario, B. terrestris will also slow down its expansion on the continent. Finally, we discuss the consequences of the large niche overlap between the introduced bumble bee species and endangered B. dahlbomii and the effect of climate change on these three species of bumble bees in South America. Abstract A handful of known bumble bee species (Bombus) have been transported worldwide and introduced in non-native regions for crop pollination, leading to long-lasting biological invasions. The introductions and invasions of European Bombus terrestris and, previously, of Bombus ruderatus in southern South America have been associated with sharp population declines of the giant Patagonian bumblebee,

Conserved, yet disruption-prone, gut microbiomes in neotropical bumblebees

Article

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Oct 2023

Bumblebees are important pollinators in natural ecosystems and agriculture, but many species are declining. Temperate-zone bumblebees have host-specific and beneficial gut microbiomes, which may have a role in mediating the effects of stressors. However, there is almost no published information on the gut microbiomes of tropical bumblebees. As temperate and tropical bumblebees encounter different floral resources and environmental conditions, their microbiomes could differ. Here, we characterized the gut microbiomes of four neotropical Bombus species and, for comparison, co-occurring solitary bees (genus Thygater ). We collected wild-foraging bees from multiple sites in central Colombia and used 16S rRNA gene sequencing to characterize their gut microbiomes. DNA barcoding and morphology were used to identify bumblebee species. We found that the microbiomes of neotropical bumblebees cluster with those of closely related temperate-zone species, in agreement with a model of bumblebee-symbiont codiversification. There was no evidence of geographic differences in microbiome composition between neotropical and temperate-zone bumblebees. These results suggest that the microbiome was conserved during bumblebee dispersal from North America, despite major shifts in ecology and life history. As previously observed in temperate-zone species, some neotropical bumblebees have highly disrupted microbiomes, in which conserved gut bacterial symbionts are replaced by environmental microbes. In these individuals, the gut microbial profile is more like that of solitary bees than of conspecifics. The gut parasites Nosema and Crithidia are also prevalent and associated with microbiome disruption. Our findings provide insights into the biogeography of bee microbiomes and a foundation for studying bee-microbe-stressor interactions in the neotropics. IMPORTANCE Social bees are an important model for the ecology and evolution of gut microbiomes. These bees harbor ancient, specific, and beneficial gut microbiomes and are crucial pollinators. However, most of the research has concentrated on managed honeybees and bumblebees in the temperate zone. Here we used 16S rRNA gene sequencing to characterize gut microbiomes in wild neotropical bumblebee communities from Colombia. We also analyzed drivers of microbiome structure across our data and previously published data from temperate bumblebees. Our results show that lineages of neotropical bumblebees not only retained their ancient gut bacterial symbionts during dispersal from North America but also are prone to major disruption, a shift that is strongly associated with parasite infection. Finally, we also found that microbiomes are much more strongly structured by host phylogeny than by geography, despite the very different environmental conditions and plant communities in the two regions.

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Climate tracking by alpine insect distribution across a century: concentric retreats, small refugia and strong elevational shifts in bumblebees

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Deuterium to hydrogen (D/H) ratios in Earth's hydrologic cycle have long served as important tracers of climate processes, yet the global HDO budget remains poorly constrained because of uncertainties in the isotopic compositions of continental evapotranspiration and runoff. Here bias-corrected satellite retrievals of HDO and H2O concentrations from the Tropospheric Emissions Spectrometer are used to estimate the marine atmospheric surface layer HDO vapor pressure deficit, from which we calculate the global flux-weighted average oceanic evaporation isotopic composition as −37.6‰. Using these estimates, combined with D/H ratios in precipitation, global mass balance suggests H isotope compositions for global runoff and terrestrial evapotranspiration of −77.3‰ and −40.0‰, respectively. By resolving the HDO budget, we establish an accurate global baseline for geochemically enabled Earth system models, demonstrate patterns in entrainment of moisture into the marine surface layer, and determine the isotopic composition of continental fluxes critical for global ecohydrologic investigations.

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Bees are subject to numerous pressures in the modern world. The abundance and diversity of flowers has declined, bees are chronically exposed to cocktails of agrochemicals, and they are simultaneously exposed to novel parasites accidentally spread by humans. Climate change is likely to exacerbate these problems in the future. Stressors do not act in isolation; for example pesticide exposure can impair both detoxification mechanisms and immune responses, rendering bees more susceptible to parasites. It seems certain that chronic exposure to multiple, interacting stressors is driving honey bee colony losses and declines of wild pollinators, but such interactions are not addressed by current regulatory procedures and studying these interactions experimentally poses a major challenge. In the meantime, taking steps to reduce stress on bees would seem prudent; incorporating flower-rich habitat into farmland, reducing pesticide use through adopting more sustainable farming methods, and enforcing effective quarantine measures on bee movements are all practical measures that should be adopted. Effective monitoring of wild pollinator populations is urgently needed to inform management strategies into the future. Copyright © 2015, American Association for the Advancement of Science.

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The effects of climate change on biodiversity are increasingly well documented, and many methods have been developed to assess species' vulnerability to climatic changes, both ongoing and projected in the coming decades. To minimize global biodiversity losses, conservationists need to identify those species that are likely to be most vulnerable to the impacts of climate change. In this Review, we summarize different currencies used for assessing species' climate change vulnerability. We describe three main approaches used to derive these currencies (correlative, mechanistic and trait-based), and their associated data requirements, spatial and temporal scales of application and modelling methods. We identify strengths and weaknesses of the approaches and highlight the sources of uncertainty inherent in each method that limit projection reliability. Finally, we provide guidance for conservation practitioners in selecting the most appropriate approach(es) for their planning needs and highlight priority areas for further assessments.

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P NATL ACAD SCI USA

The impact of anthropogenic climate change on terrestrial organisms is often predicted to increase with latitude, in parallel with the rate of warming. Yet the biological impact of rising temperatures also depends on the physiological sensitivity of organisms to temperature change. We integrate empirical fitness curves describing the thermal tolerance of terrestrial insects from around the world with the projected geographic distribution of climate change for the next century to estimate the direct impact of warming on insect fitness across latitude. The results show that warming in the tropics, although relatively small in magnitude, is likely to have the most deleterious consequences because tropical insects are relatively sensitive to temperature change and are currently living very close to their optimal temperature. In contrast, species at higher latitudes have broader thermal tolerance and are living in climates that are currently cooler than their physiological optima, so that warming may even enhance their fitness. Available thermal tolerance data for several vertebrate taxa exhibit similar patterns, suggesting that these results are general for terrestrial ectotherms. Our analyses imply that, in the absence of ameliorating factors such as migration and adaptation, the greatest extinction risks from global warming may be in the tropics, where biological diversity is also greatest. • biodiversity • fitness • global warming • physiology • tropical

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Methods Ecol. Evol.

1. Phylogenetic signal is the tendency of related species to resemble each other more than species drawn at random from the same tree. This pattern is of considerable interest in a range of ecological and evolutionary research areas, and various indices have been proposed for quantifying it. Unfortunately, these indices often lead to contrasting results, and guidelines for choosing the most appropriate index are lacking. 2. Here, we compare the performance of four commonly used indices using simulated data. Data were generated with numerical simulations of trait evolution along phylogenetic trees under a variety of evolutionary models. We investigated the sensitivity of the approaches to the size of phylogenies, the resolution of tree structure and the availability of branch length information, examining both the response of the selected indices and the power of the associated statistical tests. 3. We found that under a Brownian motion (BM) model of trait evolution, Abouheif’s Cmean and Pagel’s λ performed well and substantially better than Moran’s I and Blomberg’s K. Pagel’s λ provided a reliable effect size measure and performed better for discriminating between more complex models of trait evolution, but was computationally more demanding than Abouheif’s Cmean. Blomberg’s K was most suitable to capture the effects of changing evolutionary rates in simulation experiments. 4. Interestingly, sample size influenced not only the uncertainty but also the expected values of most indices, while polytomies and missing branch length information had only negligible impacts. 5. We propose guidelines for choosing among indices, depending on (a) their sensitivity to true underlying patterns of phylogenetic signal, (b) whether a test or a quantitative measure is required and (c) their sensitivities to different topologies of phylogenies. 6. These guidelines aim to better assess phylogenetic signal and distinguish it from random trait distributions. They were developed under the assumption of BM, and additional simulations with more complex trait evolution models show that they are to a certain degree generalizable. They are particularly useful in comparative analyses, when requiring a proxy for niche similarity, and in conservation studies that explore phylogenetic loss associated with extinction risks of specific clades.

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Mar 2013
GLOBAL ECOL BIOGEOGR

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AbstractI challenge (1) the assumption that habitat patches are natural units of measurement for species richness, and (2) the assumption of distinct effects of habitat patch size and isolation on species richness. I propose a simpler view of the relationship between habitat distribution and species richness, the ‘habitat amount hypothesis’, and I suggest ways of testing it. The habitat amount hypothesis posits that, for habitat patches in a matrix of non‐habitat, the patch size effect and the patch isolation effect are driven mainly by a single underlying process, the sample area effect. The hypothesis predicts that species richness in equal‐sized sample sites should increase with the total amount of habitat in the ‘local landscape’ of the sample site, where the local landscape is the area within an appropriate distance of the sample site. It also predicts that species richness in a sample site is independent of the area of the particular patch in which the sample site is located (its ‘local patch’), except insofar as the area of that patch contributes to the amount of habitat in the local landscape of the sample site. The habitat amount hypothesis replaces two predictor variables, patch size and isolation, with a single predictor variable, habitat amount, when species richness is analysed for equal‐sized sample sites rather than for unequal‐sized habitat patches. Studies to test the hypothesis should ensure that ‘habitat’ is correctly defined, and the spatial extent of the local landscape is appropriate, for the species group under consideration. If supported, the habitat amount hypothesis would mean that to predict the relationship between habitat distribution and species richness: (1) distinguishing between patch‐scale and landscape‐scale habitat effects is unnecessary; (2) distinguishing between patch size effects and patch isolation effects is unnecessary; (3) considering habitat configuration independent of habitat amount is unnecessary; and (4) delineating discrete habitat patches is unnecessary.

Thermal niches are more conserved at cold than warm limits in arctic-alpine plant species

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Aug 2013
GLOBAL ECOL BIOGEOGR

Understanding the stability of realized niches is crucial for predicting the responses of species to climate change. One approach is to evaluate the niche differences of populations of the same species that occupy regions that are geographically disconnected. Here, we assess niche conservatism along thermal gradients for 26 plant species with a disjunct distribution between the Alps and the Arctic. European Alps and Norwegian Finnmark. We collected a comprehensive dataset of 26 arctic-alpine plant occurrences in two regions. We assessed niche conservatism through a multispecies comparison and analysed species rankings at cold and warm thermal limits along two distinct gradients corresponding to (1) air temperatures at 2 m above ground level and (2) elevation distances to the tree line (TLD) for the two regions. We assessed whether observed relationships were close to those predicted under thermal limit conservatism. We found a weak similarity in species ranking at the warm thermal limits. The range of warm thermal limits for the 26 species was much larger in the Alps than in Finnmark. We found a stronger similarity in species ranking and correspondence at the cold thermal limit along the gradients of 2-m temperature and TLD. Yet along the 2-m temperature gradient the cold thermal limits of species in the Alps were lower on average than those in Finnmark. We found low conservatism of the warm thermal limits but a stronger conservatism of the cold thermal limits. We suggest that biotic interactions at the warm thermal limit are likely to modulate species responses more strongly than at the cold limit. The differing biotic context between the two regions is probably responsible for the observed differences in realized niches.

Climate change impacts on bumblebees converge across continents. [DOWNLOAD reprint at: http://www.macroecology.ca/Papers.html]

Abstract

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