Large-scale losses are not new to the beekeeping industry (Table 1). Many of the
symptoms similar to those expressed by CCD-affected colonies have been described before.
Like today, in the past, the cause for the colony collapse has not been ascertained with certainty,
although speculations as to the cause(s) are plentiful. In this paper we briefly review the past
history of colony collapses that are reminiscent of the present situation.
The first published record of this disorder appeared in 1869. An anonymous author
reported loss of bees which left behind hives with plenty of honey. It was speculated that the
death was due to a lack of pollen, poisonous honey, or a hot summer [4]. Subsequently, Aikin
[5] described losses in Colorado in 1891 and 1896 where large clusters disappeared or dwindled
to tiny clusters with queens in May, hence the name “May disease”. Investigations at the time
identified various fungi with these collapses. Burnside [6] was able to isolate, culture, and
reproduce symptoms very similar to CCD with a strain of Aspergillus fungi.
Stonebrood, caused by the fungus Aspergillus flavus, affects both immature and adult
bees. Infected larvae turn into solid, hard mummies that are not easily removed by the bees [7,
8]. Stonebrood-infected adults fly or crawl a considerable distance from colonies before dying
[6]. Superficially, the adults appear normal [6]. It is believed that stonebrood is spread through
the sharing of infected combs [9], as the fungus has been isolated on combs [10]. In addition,
Giauffret [11] believed that disruption of the intestinal flora of bees due to antibiotic use may
allow the fungus to spread. It is yet to be determined if the losses that are being seen today will,
like with stonebrood, appear suddenly and then disappear [12].
In three epidemics between 1905 and 1919, 90% of the honey bee colonies on the Island
of Wight in the United Kingdom died [13, 14]. Bees afflicted with this disorder could not fly,
but crawled from the entrance [15, 16]. Researchers disagreed as to the cause of this affliction.
Some concluded that the losses were due to acarine disease or the honey bee tracheal mite,
Acarapis woodi [13]. Others believed that starvation was the cause of the losses [14, 17]; while
still others thought Nosema disease caused the high losses [18]. Some affected beekeepers over
the years have blamed their losses on the so-called “Isle of Wight disease” whenever they could
not find another cause [14]. Bullamore [17] noted that genetics likely played a role and
emphasized the need to dispose of colonies after a maximum of 3 years.
In the Stawell district of Australia in 1910, 59% of colonies were lost and many more
were severely weakened [19]. Beuhne [19] noted that colonies that did not have their honey
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extracted and that were allowed to gather honey late in the season did especially poorly. He
concluded that honey made from Eucalyptus leucoxylon was too high in moisture, presumably
fermented, and so was not suitable for consumption by the bees [19]. The author also mentioned
that reliable accounts of severe losses from as far back as 1872 have been noted “at intervals of
some years” [19].
Instances of large-scale losses were also reported in 1915 in Portland, Oregon [15] and
from Florida to California in that same year [20], but these losses were not well documented. In
1917, widespread losses were reported in New Jersey, New York, Ohio, and Canada [21]. This
time, an overabundance of pollen was blamed and bees were found dead in front of the hives.
Root and Root [15] noted that this “disappearing disease” disappears within a short time without
treatment.
In the 1960’s, many reports of losses were published. In Texas and Louisiana, bees
disappeared in the fall and winter [20]. In the Rio Grande River region of Texas in particular, the
losses occurred after a period of unseasonable cold followed by 2 weeks of rain [22]. In
Louisiana, bees were tested and found to be free of nosema disease, septicemia, honey bee
tracheal mites, external parasites, and paralysis virus [23]. Roberge [24] noted that the bees had
suddenly stopped clustering and believed the problem was genetic. Bees were also lost in
California [25]. The remaining bees in the dwindled colonies appeared healthy and had plenty of
food stores.
In Australia, losses were high in 1975 [26]. Termed “disappearing syndrome”, losses
seemed to be due to dampness, poor nutrition, and stress [23]. Olley [26] noted that the
syndrome could be transmitted between closely adjacent colonies through robbing and suggested
that a virus was the cause. At about the same time, losses were reported in Mexico [27]. The
losses in Mexico, called “disappearing disease”, were blamed on the environment, as research
ruled out genetic factors [28]. In addition, paralysis virus and cold weather did not play a role
[27]. Many factors, such as diseases, poor nutrition, and genetics, could have worked together to
cause this syndrome [28]. An extensive survey conducted in 1975 indicated that the disorder
could be found in 27 states [29]. Witherell [30] ruled out poisonous pollen, poisonous nectar,
pesticide poisoning, and diseases caused by microorganisms, including viruses, as possible
causes.
In the late 1970’s, losses occurred in winter and spring in Florida [31]. Pathogens, food
or lack of it, weather, genetics, and management were all suspected causes. Studies of the effects
of protein sources on bee longevity and brood rearing showed that inadequate pollen substitutes
could cause bee loss [32]. Losses also occurred in Seattle, Washington, where bees failed to
cluster and were observed flying on a very cold day [33]. Losses in Texas at the time were not
due to nosema disease or septicemia [22].
In the mid-1990’s, losses again became evident in the northeastern United States [34].
Research showed that bee mortality could be reduced when Apistan, Terramycin extender
patties, and Fumidil-B were used, but that menthol and grease patties did not prevent loss. This
suggests that good nutrition and pest control may keep bees healthy and enable them to resist this
malady and that honey bee tracheal mites did not likely contribute to the losses.
During the winters of 1998-1999 and 1999-2000, heavy losses were reported in France.
Research showed that known honey bee diseases were present, alone or in combination with
each other, in 76% of the effected apiaries [35]. There were no combinations of diseases that
were more likely than the others, so the main suspects became colony mismanagement, nutrient
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deficiencies, and chemicals in the environment. Then, as now, the cause of the losses was
generally unknown