Science - USA (2022-06-03)

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PHYSIOLOGY

Glyphosate impairs bee thermoregulation

T he world’s most common herbicide affects social homeostasis in bumble bee colonies

By J ames Crall

B

ees and other insect pollinators are crit-

ical to supporting ecosystems and ag-

ricultural productivity. Agrochemicals

can have considerable negative sub-

lethal effects on bees, threatening

bee populations and the ecosystem

services they provide. Understanding the im-

pacts of agrochemicals is essential to meet-

ing the demands of global food production

while protecting bees and other beneficial

insects. Insecticides, such as neonicotinoids,

have been a primary focus because of their

direct impacts on insects. But exposure to

noninsecticide agrochemicals is widespread

and could have important, unanticipated

consequences. On page 1122 of this issue,

Weidenmüller et al. ( 1 ) demonstrate that

the herbicide glyphosate—the world’s most

widely used agrochemical—impairs social

thermoregulation in buff-tailed bumble bees

(Bombus terrestris) (see the photo) , which is

critical for colony growth and the health of

these important pollinators.

Glyphosate targets the 5-enolpyruvylshi-

kimate-3-phosphate  synthase enzyme in the

shikimate pathway, which is required for

the synthesis of aromatic amino acids and

other secondary metabolites. This enzyme

is present in plants and many microorgan-

isms but absent in insects and other animals.

Glyphosate has thus been considered of little

direct concern to bees and other beneficial

insects. Although mounting evidence has

suggested that glyphosate may directly af-

fect bees, the extent and relevance of these

impacts remain unclear, particularly for spe-

cies other than European honey bees (Apis

mellifera). In their study, Weidenmüller et

al. use a split-colony experimental design to

demonstrate that exposure, through artificial

nectar, to low, environmentally realistic con-

centrations of glyphosate impairs the bumble

bee colony’s ability to regulate the tempera-

ture of the developing brood.

Bumble bees are a vitally important group

of pollinators in both unmanaged and agri-

cultural ecosystems. Temperature regulation

within the nest is critical for bumble bees

( 2 ). There, the temperature of the develop-

ing brood is actively maintained within a

narrow, optimal range. Thermoregulation is

performed either individually by the queen

during the early stages of nest founding

or collectively by workers in later colony

stages. Weidenmüller et al. provide direct

evidence that links brood temperature to

colony success. Specifically, maintaining the

brood within a narrow temperature range of

288 to 35 8 C has strong effects on the brood.

Outside of this range, both the growth rate

and survival of the developing brood decline

rapidly. Given the relatively small colony

size (often <100 workers) and annual colony

cycle (compared with perennial honey bee

colonies) of bumble bees, even temporary

reductions in brood growth and survival are

likely to have strong impacts on colony re-

production and fitness.

Although critical, thermoregulation is de-

manding. During incubation, bumble bees

contract flight muscles and decouple them

from the wings, generating heat that is

transferred to the brood through direct

contact with the hairless underside of the

abdomen. This is energetically costly, with

incubation requiring metabolic rates that

approach those during flight ( 2 ). Therefore,

incubation is closely tied to food resources

( 3 ), particularly carbohydrate-rich nectar.

Weidenmüller et al. show that the effects of

glyphosate on thermoregulation only occur

when food resources are limited. Although

the specific mechanisms underlying glypho-

sate’s impacts on thermoregulation remain

unknown, an intriguing possibility is that

glyphosate could affect bumble bee metabo-

lism and physiology through effects on the

microbiome ( 4 ). Glyphosate can perturb the

honey bee gut microbiome, including de-

creasing the abundance of dominant micro-

biota ( 5 ). The observed impacts on homeo-

static thermoregulation could potentially

emerge as a secondary effect of metabolic

dysfunction in bumble bees.

Beyond the microbiome, glyphosate has

been shown to affect behavior and navigation

in honey bees, which could in turn impair

colony food intake ( 6 ). Commercial glypho-

sate formulations, such as Roundup, can

also cause mortality in bumble bees ( 7 ). It

can be challenging, however, to disentangle

the effects of glyphosate per se from chemi-

cal coformulants. Many negative impacts of

commercial formulations, including lethal-

ity, may be caused by “inert” ingredients, not

glyphosate itself ( 7 ). In addition, studies to

date have focused primarily on A. mellifera ,

which, although important for agriculture,

represent just one of the roughly 20,000

species of bees. The effects of glyphosate on

other bees are almost entirely unknown.

The findings of Weidenmüller et al. are

especially important given the widespread

global use of glyphosate. Use of the herbi-

cide rose substantially after the introduc-

tion of glyphosate-resistant (“Roundup

Ready”) crops in the mid-1990s. Glyphosate

is now the most widely used agrochemi-

cal in history, with more than 1.6 billion

kg used in the United States alone since

1974 ( 8 ). Because of its low acute toxicity to

honey bees, mitigation of exposure to bees

is minimal and, consequently, exposure is

widespread. The possibility for potential

negative impacts of glyphosate exposure is

thus enormous, highlighting the critical im-

portance of future work exploring the scope

of these sublethal effects on the population

health of bumble bees and other pollinators.

The realization of the full extent of the

impacts of agrochemicals years (or decades)

after their introduction reflects, in part, the

fundamental difficulty of predicting complex

effects of pesticides on biodiversity. Although

environmental safety testing focuses on

acute, lethal toxicity, this is insufficient for

identifying multifaceted and often unpredict-

able effects on behavior, physiology, or repro-

duction that occur at sublethal exposures.

For example, neonicotinoid insecticides af-

fect bee navigation and cognition ( 9 ), forag-

ing efficiency ( 10 ), thermoregulation ( 11 ), and

colony growth ( 12 ) at concentrations well

Department of Entomology, University of Wisconsin–

Madison, Madison, WI, USA. Email: [email protected]

Buff-tailed bumble bees (Bombus terrestris) care

for a developing brood within the nest.

PHOTO: RICHARD BECKER/MINDEN PICTURES

3 JUNE 2022 • VOL 376 ISSUE 6597 1051