Environmental Quality Management / DOI 10.1002/tqem / Winter 2007 / 11

© 2007 Wiley Periodicals, Inc.Published online in Wiley InterScience (www.interscience.wiley.com).DOI: 10.1002/tqem.20160

“If the bee disap-

pears from the sur-

face of the earth,

man would have no

more than four

years to live. No

more bees, no more

pollination, no

more plants, no

more animals, no more man.”

This widely cited quote has been attributed to

Albert Einstein—although debunkers of “urban

legends” say it is doubtful that he actually au-

thored it. Regardless of the source, however, this

statement underscores the important role bees

play within the ecosystem and in the modern

human food web.

In order to bear fruit, three-quarters of all

flowering plants, including most food crops, rely

on pollinators for fertilization. Honeybees are the

insects most important to the human food chain.

They are the principal pollinators for hundreds of

vegetables, fruits, nuts, and flowers. But what if

we lost this important source of pollination?

Colony Collapse DisorderColony Collapse Disorder (or CCD) is a

bizarre, recently experienced phenomenon in

which worker bees from a beehive colony virtu-

ally vanish into

thin air, leaving the

vacated hive and

precious honey

supply behind.

Beekeepers are

watching their

hives become bare

in a matter of

weeks, sometimes days. This makes CCD difficult

to study. For example, a beekeeper who recently

traveled with two truckloads of bees to California

for pollination found nearly all of his bees gone

or dead upon arrival.

Commercial beekeepers are reporting losses of

50 to 90 percent, an unprecedented level even for

an industry accustomed to die-offs. Many scien-

tists are becoming increasingly alarmed at this

epidemic.

Honeybees pollinate one-third of the food

eaten by Americans. Some worry that what’s

shaping up to be a honeybee catastrophe could

disrupt the national or even global food supply.

The United States House of Representatives’

Committee on Agriculture has held hearings on

Charles H. Eccleston

The Case of theDisappearing Honeybees:An EnvironmentalHarbinger?

Colony Collapse Disorder may

portend a scary future for other

species—including humans

Charles H. Eccleston12 / Winter 2007 / Environmental Quality Management / DOI 10.1002/tqem

the “missing bee” phenomenon (see Berenbaum,

2007).

CCD CharacteristicsCCD typically involves the following abnor-

mal characteristics:

• Adult bees vanish from the hive, with little

trace of dead bees in or around the colony. This

is highly unusual since

bees normally do not

abandon a hive until

the “capped brood”

(offspring) have all

hatched; with CCD,

adult bees often disap-

pear with capped brood

still in the hive.

• Food stores of honey and bee pollen are aban-

doned.

• The abandoned hives are not immediately

robbed by other bees.

• Attacks by other predators, such as wax

moths, are delayed or do not occur at all

(meaning that the bees’ natural enemies ap-

pear to avoid the abandoned hives).

Even before the colony collapses, several

“early warning” signs can often be observed, in-

cluding the following:

• The queen is evident outside the hive (which

generally does not occur under normal cir-

cumstances).

• The workforce is composed of juvenile adults,

and is inadequate to maintain the brood.

• The bees appear reluctant to consume stored

food supplies.

Progression of CCDCCD was first reported in Florida in late 2006.

It has since spread to more than two dozen states

in the United States, as well as parts of Canada. It

has been found in several geographically separate

regions of North America, from the eastern

United States to the west coast.

Similar reports of bee disappearance are now

flowing in from parts of Europe, as well as India

and Brazil (although it is still uncertain whether

all reported cases are actually CCD).

Prior Instances of Bee DeclineIn the 1990s, France witnessed a similar pre-

cipitous decline in the bee population. The

problem was initially blamed on a newly intro-

duced pesticide, which the French government

subsequently banned. Later studies failed to find

a strong link with the pesticide, and French bee

populations still have not rebounded to previ-

ous levels.

In addition, a gradual decline in bee

colonies was witnessed from about 1970 to

2006. These declines were blamed on a range of

factors, including pesticide use, urbanization,

mites, and the loss of commercial beekeepers,

many of whom were retiring or leaving the

business.

Moreover, although widespread reports of

sudden bee disappearances did not surface until

late last year, it now appears that restricted occur-

rences of a disorder resembling CCD have been

observed as far back as 1896.

Honeybee Origins and CharacteristicsMany readers may be surprised to learn that

honeybees are not native to North America or Eu-

rope. They are thought to come from Southeast

Asia, although some recent research based on ge-

nomic studies indicates that their origin is actu-

ally in Africa.

Honeybees are finely tuned machines. As

such, they are sensitive barometers of environ-

mental degradation. A wide variety of pollutants

can kill them or markedly change their behavior.

It now appears that restrictedoccurrences of a disorderresembling CCD have been observedas far back as 1896.

Environmental Quality Management / DOI 10.1002/tqem / Winter 2007 / 13The Case of the Disappearing Honeybees: An Environmental Harbinger?

are present in humans whose immune systems

have been suppressed by Acquired Immuno-

deficiency Syndrome (AIDS) or cancer.

• Stress: Some studies suggest that honeybees

are responding to abnormal levels of stress.

One possible cause of stress is “bee jet lag,” as

more beekeepers haul truckloads of hives

across the country for pollination rental work.

Zigzagging around the country may also pro-

mote the spread of viruses and mites among

colonies. Further adding to the stress is subur-

ban sprawl, which in several states has limited

the bees’ natural forage areas.

• Climate change: A number of researchers be-

lieve that climate

change may be the

ultimate cause of

CCD, with extreme

and erratic weather

patterns generated

by global warming

placing undue stress

on hives. In fact,

temperatures re-

corded during the first half of 2006 (coinciden-

tally the same year when CCD was first ob-

served and assigned a name) showed it to be the

warmest year on record in the United States.

• Mobile phones: Media reports have attempted

to link CCD with the increasing use of cellu-

lar and cordless phones. These reports are

based on speculation, however, with no re-

search to demonstrate the link.

IAPVA recently completed genetic analysis pub-

lished in the journal Science suggests that a virus

called Israeli acute paralysis virus (IAPV) might be

contributing significantly to CCD (Stokstad,

2007). Scientists report circumstantial evidence

linking the arrival of honeybee imports from Aus-

tralia with the emergence of IAPV in the United

What Causes CCD?The specific causes of CCD remain a scientific

mystery. Some scientists even question whether

the disorder is real.

Multiple Theories of CausationTheories of causation run the gamut from ul-

traviolet radiation to UFO abductions. The list of

potentially plausible culprits spans a diverse

range of factors, including environmental

change, disease, malnutrition, and even radiation

from mobile phones.

Virtually all reported cases of honeybee disap-

pearance have occurred among commercial bee-

keepers, leading some to believe that beekeeping

practices may contribute to CCD. Some of the

factors widely discussed as potential causes in-

clude the following:

• Pesticide use: Although many believe this to be

a promising hypothesis, numerous studies have

failed to link any specific insecticide to CCD.

• Genetically modified (GM) crops: Some have

suggested that bees may be adversely affected

by pollen gathered from GM crops. Again,

however, little actual evidence can be found

to support the hypothesis.

• Varroa mites: These parasitic mites appear to

be a formidable killer of honeybees, due in

part to the viruses they harbor. As a result,

Varroa mites have been considered as a possi-

ble cause of CCD. But not all dying colonies

contain these mites, and no known viral dis-

eases affecting honeybees appear to be in-

volved in CCD.

• Micro-organisms: Genetic testing has revealed

one promising clue—the presence of numer-

ous micro-organisms in bees from hives or

colonies that are in decline. This suggests that

something in the bees’ environment is weak-

ening their immune systems. Biologists have

identified some fungi in affected bees that also

Virtually all reported cases ofhoneybee disappearance have

occurred among commercialbeekeepers, leading some to

believe that beekeeping practicesmay contribute to CCD.

Charles H. Eccleston14 / Winter 2007 / Environmental Quality Management / DOI 10.1002/tqem

States. This suggests that CCD may result at least

in part from importation of non-native invasive

species (NNIS).

The researchers found IAPV DNA in 25 out of

30 CCD-afflicted hives, but in only one of 21 un-

affected hives. The researchers also noted that

other factors (such as the Varroa mite, discussed

previously) might be contributing to CCD by

weakening honeybee immune systems and mak-

ing them more vulnerable to IAPV. Research on

IAPV is ongoing (Stokstad, 2007).

A lead member of the study, W. Ian Lipkin,

serves as director of

the Center for Infec-

tion and Immunology

at Columbia Univer-

sity’s Mailman School

of Public Health. In an

article about the study

in Scientific American

(Minkel, 2007), Lipkin

was quoted as stating, “We haven’t proven this is

the cause. It is a candidate for being a trigger for

CCD” (Minkel, 2007). The evidence reported in

the article points to a connection, however:

Lipkin and co-workers found that seem-

ingly healthy Australian bees were in-

fected with the IAPV virus and point out

that all of the CCD hives they examined

included or spent time near imported Aus-

tralian bees. Beekeepers from Down Under

have reported a “disappearing disease” but

not on the scale of CCD [according to an

entomologist with the U.S. Department of

Agriculture’s Agricultural Research Service

Bee Research Laboratory]. (Minkel, 2007)

The article further noted, “The smoking gun,

Lipkin says, would be to infect healthy or

stressed bees with IAPV and see if they catch

CCD. The researchers plan to carry out such

tests, but isolating the virus is challenging, he

adds” (Minkel, 2007).

The Dangers of OverspecializationA study by the National Academy of Sciences

has questioned whether American agriculture has

been relying too heavily on the honeybee as a pol-

linator. They caution that by depending primarily

on a single species for pollination, the United

States and other nations have put “all of their eggs

in one basket.” Even worse, some evidence points

to declines in population among thousands of po-

tential alternate pollinators—including native

species such as wasps, butterflies, and other bees

(Committee on the Status of Pollinators in North

America, National Research Council, 2007).

In the longer term, CCD may force us to re-

think many of our modern agricultural ap-

proaches, including not only our heavy depen-

dence on human-managed bees, but also other

practices such as relying on a few hybrid grains to

furnish the world’s wheat and rice supplies.

The CCD crisis demonstrates the importance

of biodiversity and the danger of depending on a

small number of highly specialized species. We

have to go back no further than the 1840s to wit-

ness how severe the ramifications can be.

By 1845, potatoes had become the leading

(and in many instances, the only) staple of the

Irish diet. Much worse, however, was the fact that

the entire potato crop depended on just a few

species of potatoes that were highly susceptible to

certain pathogens. When the potato crop fell vic-

tim to blight in the mid-1840s, the consequences

for the Irish population were catastrophic.

Although the actual cause of the blight is still

not fully understood, one plant pathologist, Jean

Beagle Ristanio, has suggested that a shipment of

potatoes from South America may have intro-

duced a pathogen into Europe. When the

pathogen reached Ireland, the entire potato crop

became a casualty of the resulting infection.

The CCD crisis demonstrates theimportance of biodiversity and thedanger of depending on a smallnumber of highly specializedspecies.

Environmental Quality Management / DOI 10.1002/tqem / Winter 2007 / 15The Case of the Disappearing Honeybees: An Environmental Harbinger?

as global warming, indiscriminate pesticide use,

and importation of NNIS. We can ill afford to go

down the path cautioned against in the quote

that began this article.

ReferencesBerenbaum, M. R. (2007, March 29). Statement of May R.Berenbaum, Professor and Head, Department of Entomology,University of Illinois Urbana-Champaign, and Chair, Com-mittee on the Status of Pollinators in North America, Board onLife Sciences and Board on Agriculture and Natural Resources,Division on Earth and Life Studies, National Research Coun-cil, The National Academies, before the Subcommittee onHorticulture and Organic Agriculture, Committee on Agricul-ture, U.S. House of Representatives. Colony Collapse Disorderand Pollinator Decline. Available online at http://www7.na-tionalacademies.org/ocga/testimony/Colony_Collapse_Disor-der_and_Pollinator_Decline.asp

Committee on the Status of Pollinators in North America, Na-tional Research Council. (2007). Status of pollinators in NorthAmerica. Washington, DC: National Academies Press. Avail-able online at http://www.nap.edu/catalog.php?record_id=11761

Great Irish Famine. (updated 2007, October 2). Wikipedia.com.

Minkel, J. R. (2007, September 7). Mysterious honeybee disap-pearance linked to rare virus. ScientificAmerican.com. Availableonline at http://www.sciam.com:80/article.cfm?articleId=E0E0362F-E7F2-99DF-3F4F781839D6C879&chanId=sa003

Stokstad, E. (2007, September 7). Genomics: Puzzling declineof U.S. bees linked to virus from Australia. Science, 317(5843),1304–1305.

Widespread famine ensued. It has been esti-

mated that around one million people (12 per-

cent of the Irish population) died in the three

years following the introduction of this

pathogen. The famine devastated Ireland and

had long-term effects on the nation’s culture

and demographics. It led to a 70-year decline in

population, with numbers stabilizing at half

their former level. Out of desperation, millions

of Irish immigrated to America (Great Irish

Famine, 2007).

Concluding ThoughtsEven if our current “bee crisis” does not result

in a catastrophe as severe as the potato famine, it

is a serious environmental wake-up call. Bees are

finely tuned instruments of nature, and are thus

perhaps more sensitive to environmental stresses

and “imported” pathogens than some other

species. Could they be the proverbial equivalent

of the “canary in the mine”?

Honeybees might simply be the first of many

species that ultimately will be weakened and ad-

versely affected by anthropogenic stressors such

Charles H. Eccleston, PhD, is a Certified Environmental Professional (CEP) and author of three leading textbooks on theNational Environmental Policy Act (NEPA) and environmental impact assessment published by John Wiley & Sons andCRC/Lewis Press. He is listed in Who’s Who in America and Who’s Who in the World as a leading expert on NEPA andenvironmental policy. Dr. Eccleston’s latest book, Megacrises: A Survivor’s Guide to the Future, addresses terrorism andother emerging global threats. He can be contacted at ecclestonc@msn.com.