Conceived and designed the experiments: Dv JHJ JP. Performed the experiments: JHJ RMU JP. Analyzed the data: Dv RMU. Contributed reagents/materials/analysis tools: Dv. Wrote the paper: Dv JHJ RMU JP.
The authors have declared that no competing interests exist.
Honey bees are an essential component of modern agriculture. A recently recognized ailment, Colony Collapse Disorder (CCD), devastates colonies, leaving hives with a complete lack of bees, dead or alive. Up to now, estimates of honey bee population decline have not included losses occurring during the wintering period, thus underestimating actual colony mortality. Our survey quantifies the extent of colony losses in the United States over the winter of 2007–2008.
Surveys were conducted to quantify and identify management factors (e.g. operation size, hive migration) that contribute to high colony losses in general and CCD symptoms in particular. Over 19% of the country's estimated 2.44 million colonies were surveyed. A total loss of 35.8% of colonies was recorded; an increase of 11.4% compared to last year. Operations that pollinated almonds lost, on average, the same number of colonies as those that did not. The 37.9% of operations that reported having at least some of their colonies die with a complete lack of bees had a total loss of 40.8% of colonies compared to the 17.1% loss reported by beekeepers without this symptom. Large operations were more likely to have this symptom suggesting that a contagious condition may be a causal factor. Sixty percent of all colonies that were reported dead in this survey died without dead bees, and thus possibly suffered from CCD. In PA, losses varied with region, indicating that ambient temperature over winter may be an important factor.
Of utmost importance to understanding the recent losses and CCD is keeping track of losses over time and on a large geographic scale. Given that our surveys are representative of the losses across all beekeeping operations, between 0.75 and 1.00 million honey bee colonies are estimated to have died in the United States over the winter of 2007–2008. This article is an extensive survey of U.S. beekeepers across the continent, serving as a reference for comparison with future losses as well as providing guidance to future hypothesis-driven research on the causes of colony mortality.
Honey bees are an essential component to modern American agriculture. The value of honey bee pollination services to U.S. agriculture has been estimated to be greater than 14 million dollars
Considering all the known and postential threats to honey bee colonies it is not surprising that honey bee populations have been declining over the last one half century. The National Agriculture Statistics Service (NASS) reported that there were 2.44 million honey-producing colonies in the United States as of February 2008
Unfortunately, NASS reports do not give an indication of annual winter losses. Commercial beekeepers have always relied on the ability to replace colonies lost in winter with new ones in the spring. Colonies that survive the winter quickly build their adult populations. Beekeepers can then “split” these colonies by removing half of the immature and adult bee population, introducing them into the equipment of a dead colony, and adding a new queen. This practice permits beekeepers to build their colony numbers back up by mid-summer even after suffering losses of 50% or more. Winter losses are, therefore, unrepresented in NASS figures unless beekeepers decide not to or are unable to replace winter losses. The survey described here is an attempt to quantify the extent of honey bee colony losses over the winter of 2007–2008.
High honey bee mortality appears to be widespread, as Canada
All members of the Apiary Inspectors of America (AIA) were asked to survey beekeepers in their states during the week of 23–30 March 2008. AIA members were asked to contact beekeepers by telephone that they felt were representative of their state's apiary industry, and to contact a minimum of 15 beekeepers: 5 part-time (1–50 colonies), 5 sideline (51–499 colonies), and 5 commercial (500+ colonies). They asked the following questions:
In what state and county do you keep your hives?
How many hives did you have alive in September 2007?
How many hives are alive now (March 2008)?
How many splits, increases, and/or colonies did you make/buy since September 2007?
Were your losses over this time period what you would consider to be normal?
What percentage of your hives that died had no dead bees in the hive or in the apiary?
To what do you attribute the cause of death for the hives that died?
What percentage of your hives did you send to CA for almond pollination?
Similarly, the United States Department of Agriculture (USDA)–Agricultural Research Service Beltsville Bee Research Lab conducted a survey of large commercial beekeepers, but their survey differed from the AIA survey in that it did not ask question #6. After the results were submitted, AIA and USDA surveyors were asked to report the number of beekeepers that refused to take the survey.
In addition, the survey questions were sent by e-mail to BEE_L, an internet mailing list, and to all Pennsylvania (PA) state local association presidents (n = 13) who were requested to send the questionnaire to all beekeepers on their e-mail distribution lists. The letter asked beekeepers to respond to a dedicated e-mail account. The results of three surveys, AIA, e-mail, and USDA, are reported here.
Total colony losses were calculated for each reporting operation, for the sum total of all respondents, and for various subgroup classifications. The mean of individual operation losses was calculated to determine the average loss among subgroups. Point estimates of the 95% Confidence Intervals (95% CI) were also calculated
Comparisons between total losses experienced by different groups of operations were conducted using the Chi Square test. Only significant results (P<0.05) are reported.
The total number of colonies lost with the symptom of no dead bees in the colony was calculated for individual operations by multiplying the number of colonies lost in an operation by the reported percentage lost without dead bees.
When calculating losses in individual states, colonies that were reported to be in more than one state during the period were counted multiple times; once in each listed state. This same practice is used by the National Agricultural Statistics Service when calculating the number of honey producing colonies in each state.
Response to the e-mail request was sparse for all states other than PA. The PA e-mail data were kept separate from the phone and USDA surveys, and grouped by county and then by climatic region as defined by the Pennsylvania State Climatologist (
In all, 23 state apiarist offices assisted in conducting the phone survey in their respective states. States that did not participate in the survey lack inspection programs, lack the necessary resources for such endeavors, or felt that the timing was not appropriate for obtaining reliable information in their state. In total, the AIA surveyed 305 beekeeping operations, representing a total of 324,571 managed colonies in September 2007. This represents approximately 13.3% of the 2.44 million honey-producing colonies managed in the United States in 2007
The combined dataset (AIA plus USDA) included 331 operations. The total number of colonies managed by these beekeepers in September 2007 was 474,336 representing 19.4% of the estimated 2.44 honey-producing colonies in the U.S. in the summer of 2007. The surveyed beekeepers reported having added a total of 81,501 new colonies to their operations between September 2007 and March 2008. In all, the total number of colonies living in March 2008 was 386,385. This represents a total loss of 35.8% (95% CI: 30.6–40.9%) and an average loss across all operations of 31.3% (95% CI: 7.4–54.1%). Should these surveys be representative of the losses across all operations, this suggests that between 0.75 and 1.00 million colonies died in the United States over the winter of 2007–2008.
Thirteen of the 22 surveyors responded to the request to report the number of beekeepers that refused to take the survey. Zero of 254 beekeepers refused, giving a 100% participation rate of individuals contacted directly by phone.
When the respondents were classified by operation size there was no difference in either the total or average loss (
Operation Size | Number of Respondents | Colonies Managed in September 2007 Plus Increases | Average Loss % (95% CI) | Total Loss % (95% CI) |
1 to 50 | 112 | 1,472 | 32.0 (23.3–40.6 | 33.2 (24.5–42.0) |
51 to 500 | 94 | 17,211 | 29.1 (19.9–40.6) | 31.2 (21.8–40.6) |
500+ | 125 | 455,653 | 32.2 (24.4–40.4) | 36.0 (27.6–44.4) |
More than One State | Number of Respondents | Colonies Managed in September 2007 Plus Increases | Average Loss % (95% CI) | Total Loss % (95% CI) |
No | 231 | 89,209 | 31.2 (25.2–37.2) | 34.6 (28.7–40.6) |
Yes | 100 | 450,144 | 31.5 (22.3–40.6) | 36.1 (25.7–46.4) |
Moved to CA | Number of Respondents | Colonies Managed in September 2007 Plus Increases | Average Loss % (95% CI) | Total Loss % (95% CI) |
No | 248 | 211,660 | 31.4 (25.6–37.2) | 28.6 (22.9–34.2) |
Yes | 83 | 344,177 | 30.9 (20.9–40.8) | 39.7 (29.2–50.3) |
One of the symptoms of CCD is the complete absence of bees in dead colonies or apiaries. This survey did not allow differentiation between true cases of CCD and colonies lost due to causes that share the “absence of dead bees” symptom. The 37.9% of operations (n = 102) that reported having at least some of their colonies die with this symptom and who reported the percentage of their losses with this symptom, had a significantly higher total loss of colonies (40.8%; 95% CI: 31.2–50.2%) than that experienced by operations that did not report this symptom (17.1%; 95% CI: 11.4–22.7%; χ2 = 3041, P<0.0001). At least 72.6% (n = 170) of all operations could not attribute any of their losses to CCD.
Large commercial operations were 4.5 and 1.8 times more likely to report having some of their colonies die without the presence of dead bees when compared to part-time and sideline beekeepers, respectively (Fisher's Exact test, P<0.0001;
Operation Size | Number of Respondents | % of Respondents with Some Incidence of No Dead Bees | Number of Colonies Lost | % of Colonies Lost Without Dead Bees |
1 to 50 | 95 | 14.7 | 490 | 13.5 |
51 to 500 | 84 | 34.5 | 5,135 | 32.5 |
500+ | 93 | 63.4 | 111,499 | 61.5 |
Three hundred and eighteen respondents answered the question as to whether they felt their losses were “normal” or not. Several respondents (n = 17) answered, “no–losses were less than normal”. These respondents had their answers changed to “yes” as the intent of the question was to identify beekeeper perception of acceptable and non-acceptable losses. Thirty-eight percent of all respondents felt their losses were not normal, having an average loss of 47.8% (95% CI: 29.0–56.7%) as compared to those experiencing what they felt were normal losses that had an average loss of 21.7% (95% CI: 15.9–27.5%).
Respondents were asked to identify why they thought their colonies died. Of the 229 persons responding to this question, 201 listed only one factor as responsible for their losses. Those reporting more than one reason were counted multiple times. The top five reasons given to explain death were poor quality queens, starvation, mites, CCD, and weather (
Cause | Rank | % of Operations Reporting | Number of Colonies Managed | Total Loss % (95% CI) |
1 | 31 | 145,655 | 18.5 (13.5–23.6) | |
2 | 28 | 34,145 | 19.8 (19.6–25.0) | |
3 | 24 | 143,463 | 31.7 (25.6–37.2) | |
4 | 9 | 150,870 | 48.2 (41.7–54.8) | |
5 | 9 | 25,180 | 24.4 (18.8–30.0) |
Considerable variability in total and average losses was reported from the various states (
State | All Respondents | Operations Reported in Multiple States | |||
Oper. (N) | Number colonies (September 2007+Increases) | Total Loss (CI 95%) | n | % total col | |
AL | 15 | 5,329 | 42.0 (14.8–69.1) | - | - |
AR | 20 | 17,456 | 17.4 (0–35.2) | - | - |
CA | 36 | 200,704 | 29.3 (13.9–44.6) | 31 | 90 |
FL | 23 | 75,297 | 40.0 (18.9–61.2) | 8 | 65 |
GA | 15 | 53,956 | 34.5 (8.1–60.8) | - | - |
IA | 10 | 685 | 39.4 (4.4–74.3) | - | - |
MD | 13 | 4,080 | 7.3 (0–22.2) | - | - |
MI | 15 | 7,302 | 56.2 (28.7–82.7 | 1 | 8 |
MS | 14 | 9,145 | 26.7 (3.9–49.9) | - | - |
MT | 13 | 62,865 | 27.7 (0.6–52.3 | 9 | 99 |
NC | 16 | 7,866 | 27.5 (3.5–51.4 | - | - |
ND | 18 | 113,842 | 25.6 (3.5–51.4) | 15 | 99 |
NJ | 15 | 23,532 | 15.1 (0–34.8) | 3 | 88 |
NM | 7 | 5,610 | 20.5 (0–57.8) | 3 | 21 |
NY | 9 | 29,035 | 18.8 (0–49.6) | 3 | 62 |
OH | 9 | 1,565 | 42.4 (34.0–81.3) | - | - |
PA | 32 | 16,141 | 27.0 (11.0–43.0) | 3 | 56 |
SD | 18 | 119,404 | 52.0 (27.0–76.9) | 3 | 20 |
TN | 8 | 516 | 26.5 (0–62.6) | - | - |
TX | 9 | 57,275 | 32.3 (0–69.2) | 9 | 100 |
UT | 25 | 17,104 | 32.3 (8.1–69.2) | - | - |
WI | 15 | 8,022 | 33.8 (7.6–60.0) | 1 | 52 |
WV | 17 | 3,786 | 51. 6(25.0–78.2) | 1 | 38 |
A total of 174 respondents answered the e-mail survey, with a total of 160 coming from PA. As there were insufficient responses from other states to make meaningful comparisons, only PA data were included in this comparison. Operations were divided into categories by climatic region as mentioned previously. Data on monthly temperature and precipitation for each of the 10 regions were obtained. Average precipitation did not affect the proportion of colonies lost in a region (R = 0.07739, P = 0.8317). However, there was a weak correlation with average temperature (R = −0.61758, P = 0.0571). Regions with relatively lower average temperatures had higher colony losses (
Honey bee losses continue to increase in the U.S. as demonstrated by the losses reported here and in the AIA survey from 2007
Commercial beekeepers are in tune with honey flows, the health status of their colonies and experience informs them what colony losses to expect in their specific region. Those beekeepers with multigenerational knowledge and experience can comment with authority on what “normal” losses are. Respondents to this survey were less likely to think their losses were “not normal” when compared to last year's survey
Stress associated with the movement of bees has been suggested as an underlying cause for increased mortality
The main symptom of CCD, a lack of dead bees present in hives from dead colonies, was more likely reported by beekeepers with large operations (
Of the perceived causes of losses starvation and poor queens were the most commonly identified. This is surprising, as both are manageable threats, suggesting a misdiagnosis of problems, a need to change management practices, and/or improved extension delivery methods.
A common practice in epidemiology is to look for spatial patterns to the occurrence of a disease or syndrome. With honey bee colonies making multiple moves around the country it is difficult to assign a colony loss to one region of the country. Losses were assigned to a specific state by the beekeeper and total losses varied by state (
This report documents colony losses in the U.S. While it remains difficult to accurately partition colony losses into discrete causes, our survey does indicate that one CCD symptom, the lack of dead bees in dead hives, is more common in larger operations, and operations reporting this condition had significantly higher losses than those that did not. This suggests that a contagious condition may be responsible for CCD. Continued surveys coupled with sample analysis from dead and dying colonies should provide clues as to the underlying cause increased rates of hive mortality in the U.S.
We thank the individual bee inspectors for their assistance in conducting this survey. We thank all respondents, including those contacted by phone and e-mail for their participation. We thank Mike Andree, Karen Roccasecca, Bart Smith, and Nathan Rice for compiling data. Funding was provided in part by the USDA-ARS Areawide Program to improve honey bee health. We also thank Rick Donovall and the anonymous reviewers of this paper for their comments.