Atmospheric Produced Carbmates as a Possible Cause for Honeybee

Colony Collapse Disorder (CCD)

Robert Disselkamp
Solis Research
Richland, WA, United States
E-mail: thegreenphd@gmail.com

November 17, 2015.

Summary
The onset of the colony collapse disorder (CCD) in 2006 has been devastating
to the bee industry because the wintertime reduction in honeybees threatens the US
and global food supply. In this work, it is proposed that atmospheric carbamates
produced from available ground-level ammonia and carbon dioxide can lead to the
honeybee colony collapse disorder (CCD) effect. Carbamates are known powerful
insecticides so their production, if verified by field measurement and further
modeling, can lead to this condition. Using a computed carbamate insecticide LD50
value of 31.7 ppmm from the literature for similar carbamates, it is shown that the
computed wintertime carbamic acid concentration is 480 ppmm at an urban site in
northern India (Hisar), hence toxic to the honeybee. An estimate of the seasonal
effect in carbamic acid concentration based on temperature leads to an reduction by
a factor of 3000 the summertime estimated value, which for the India site during
summer is only 0.2 ppmm, hence non-lethal to the honeybee. Atmospheric
deposition into the bees food source, nectar, and other exposure such as pollen may
explain the CCD effect.
Keywords
Colony collapse disorder; toxicity; atmospheric carbamates; lethal dose.
Short Title
Atmospheric carbamates as a cause of bee colony collapse

1. Introduction
An emerging crisis recently has been the honeybee colony collapse disorder
(CCD) phenomena. There have been significant reductions, known to be seasonal, in
the domestic honeybee populations that the world relies upon for our food supply
as they support approximately 80% of the agricultural pollination capacity [1].
Despite detailed laboratory studies that indicate that honeybees that have died by
CCD carry in vivo pesticides, herbicides, and fungicides, the same is true of healthy
bees that have been analyzed [1].
Other possibilities for CCD include viral or bacterial infections. However, in
France where bees were analyzed to be infected, even when the infections were
reduced their bee populations still continue to decline [1]. The evidence implies that
this effect is unlikely (but still possible with other viral/bacterial strains).
A third possibility includes the effects of global climate change. This allencompassing topic is also likely, especially as is discussed here in terms of a trend
observed in one particular atmospheric pollutant, carbamates. Carbamates are
amino-carboxylate entities and a powerful class of insecticides [2,3], making their
atmospheric production particularly of concern as a cause of the CCD effect.
Carbamates are formed in the atmosphere, as is hypothesized here, by the reaction
of amines (e.g., ammonia) with carbon dioxide, that is facile under ambient
temperature conditions at high concentrations [4]. In this work, the high
concentration carbamate formation literature [4] is used to extrapolate carbamate
production under atmospheric conditions. The onset of CCD in about 2005 can be
correlated with the global distribution of ammonia and carbon dioxide considering
yearly trends, their seasonal variation, and geographic location, and can be used to
assert an explanation for the CCD effect. In this effort, reliance upon atmospheric
chemistry and insect (i.e., honeybee) toxicology [5,6] is utilized to develop a
hypothesis of CCD causation by atmospheric-derived carbamates.
There are certain characteristics associated with the CCD phenomenon that
suggest the honeybees are dying by atmospheric pollutant(s) [1]. In California, there
is a dramatic effect between healthy bee populations in summer, to bee attrition in
winter months. This seasonal change occurs every year beginning with the onset of
CCD. The troposphere in winter also experiences a dramatic decrease in actinic flux,
where a shift from a more oxidizing to reducing atmosphere takes place from
summer to winter. One such atmospheric pollutant is the NOx to NHy partitioning
that occurs, particularly ammonia formation in winter. This is not the only trace gas
pollutant undergoing this change, and could be associated with CCD, but is the only
cause considered here. In Florida, one commercial beekeeper noted that
approximately 1/3 of his bees were functioning normally, another 1/3 lethargic, and
1/3 cannot leave hive and eventually die. This could be associated with
characteristics of the lethal dose (LD33, LD67, LD100, etc.). Finally, urban air masses
that influence (e.g., transport to) a region where bees reside also play a role in the
CCD phenomenon.
2

2. Materials and Methods

This study is a paper study making use of the published literature. Hence, the
only materials used in this study are prior published works. No experiments were
performed.
3. Results and Discussion
A. Why carbamates?
Carbamates are amino-carboxylates that have been used as potent
insecticides. There are more than 40 different types of carbamate insecticides [7,8],
with the simplest being formed from the reaction between ammonia and carbon
dioxide [4]. Of unique interest to the CCD phenomena whose onset was the mid2000s is the ubiquitous nature of both these reagents in the atmosphere.
Furthermore, the seasonal variation and increase in atmospheric carbamic acid
(NH2COONH2) during the winter months where a reduced actinic flux persists, can
be attributed to a conversion of the nitrogen budget from NOx to NHy. This is
because the atmosphere is less oxidizing during the winter with a reduced oxidant
inventory correlated to a reduced actinic flux.
Because of the wide variety of carbamate pesticides known, and each having
a differing LD50 for different insect types, unfortunately it is not known what the
honeybee LD50 value is for carbamic acid. Nonetheless, an estimate can be made
based on assumed similarities among carbamate-type pesticides. For example,
based on work by Chauzat et al. [9] they discussed the toxicities (in mg/bee) of
various types of carbamate pesticides. Table 1 below summarizes the LD50 values,
based on an average honeybee mass (i.e., apis mellifera species) of 0.095 g [9].
Table 1. Summary of toxicity values for carbamate pesticides.
Carbamate pesticide type Adult bee LD50 (g/bee) a Adult bee LD50 (ppmm) b
Aldicarb
0.272
2.86
Carbaryl
1.34
14.1
Carbofuran
0.16
1.68
Oxamyl
10.26
108
Average
31.7
a - From ref.[9].
b - Based on an adult bee mass of 0.095 g.
Examining the results of Table 1 it is seen that the carbamates LD50 values
vary from about 1-110 ppm, with an average value of 31.7 ppmm. This result is
consistent with an older study [6] that listed the LD50 mass of carbamate primin
pesticide as 0.38 g, hence by the same analysis here yields the adult bee LD50 of
4.0 ppmm. Here it is shown that atmospheric carbamic acid at lethal concentrations,

while formed in the atmosphere, can undergo atmospheric deposition onto

frequented bee areas, such as in the bee food supply or exposure.
B. Sources of honeybee carbamate pesticide exposure
There are varying possible causes of exposure to pesticides the honeybees
could experience. These include: (1) the bees ingesting nectar during regular
feeding, colony maintenance, and pollination; (2) the bees adsorbing transexoskeleton pollutants contained within pollen, rainwater, and other plant life;
and/or (3) bees exposed to pollutants separate from pollination and vegetation.
Because the first of these is directly related to their food supply, this may be most
likely. Again, work by Chauzet [9] has measured the bee pollen concentrations in
France, as given in Table 2 below.
Table 2. Summary of carbamate pesticide residue in pollen in France (2002).
Carbamate pesticide type
Average pollen
concentration (ppbm) - a
Aldicarb
ND
Carbaryl
218.7
Carbofuran
14.0
Oxamyl
38.4
Average
90.4
ND Not detected.
a - From ref.[9].
It is seen in Table 2 that the average pollen concentrations are highly
variable, with an average of 90.4 ppb. Of interest, is comparing Table 1 and 2. This
comparison illustrates that because the average pollen concentration of 90.4 ppbm
is much lower than the LD50 value of 31.7 ppmm, it does not support pollen
concentration alone as a toxicity to bees in 2002, consistent with the onset of CCD in
about 2006.
C. Modeling of carbamates
There are many detailed tropospheric chemical models that can readily be
modified to include reactions of atmospheric carbamates, one example being
ISSOPIA [10]. To embellish these models it is necessary to include both the
thermodynamics (i.e., pseudo-equilibrium) and kinetics of carbamate formation and
decomposition. Here only carbamic acid is parameterized for these models. The
estimation of concentrations of carbamic acid, at equilibrium, relevant to an urban,
mid-summer (August) and mid-winter (January), scenario is estimated. To compute
the CA concentration, the following equation, taken from Park et al. [4], is used.

NH2COONH2 (i.e., CA) + CO2(aq) + H2O(l) <-> 2 NH4HCO3(aq)

(1)

This equilibrium is rapid [4] compared to aerosol lifetime, so the following

equilibrium expression can be written,
K = {[NH4HCO3]2}/{[NH2COONH2] [CO2(aq]]} .

(2)

A thermodynamic estimate of the reaction free energy, and hence equilibrium

constant, is possible. Table 3 presents free energy data. The data in Table 3, applied
to rxn(1) results in a reaction free energy of -14.6 kJ/mol at standard state, and a
value for K of 362 at a temperature of 298 K. The estimated CA concentration
according to eqn(2) is obtained from known [NH4HCO3(aq)] and [CO2(aq)]
concentrations. A more useful form of eqn(2) is its rearranged form,
[NH2COONH2] = {[NH4HCO3]2}/{K [CO2(aq]]}.

(3)

Table 3. Thermodynamic data for carbamic acid partitioning to ammonium

bicarbonate.
Species
Gfo (kJ/mol)
NH2COONH2 (CA)
-458.0 - a
CO2 (aq)
-386.2 - b
H2O (l)
-237.1 - b
+
NH4 (aq)
-79.4 b, c
HCO3- (aq)
-587.1 b, c
H2CO3 (aq)
-623.4 - b
A From ref.[11]. Latimer.
B From ref.[12]. Bard et al.
C The ammonium and bicarbonate values are combined for NH4HCO3(aq) in
rxn(1).
As discussed in the Introduction section, the kinetics of aqueous carbamic
acid formation from the reaction between CO2 and NH3 have been measured at
ambient temperature and high reagent concentration [4]. This work by Park et al.
[4] utilized high aqueous concentrations of 5 wt.%, and measured the formation and
partial decay of CA, where the formation reaction kinetics can be written,
d[CA]/dt = kf [NH3(aq)]2 [CO2(aq)].

(4)

It is seen that the aqueous CA production is second order in NH3 because two amino
groups are present in the CA molecule. Similarly, the decomposition of CA occurs in
their experiment by reaction with CO2, yielding (where kd is positive)
d[CA]/dt = -kd [CA] [CO2(aq)].

(5)

Utilizing the data of Park et al. [4] using [CA]=[NH3]=5 wt.%, in their Figure 1 (for
[CA] formation) and Figure 3 ([CA] decay) they observed respective lifetimes of 30
min. and 323 min. This results in calculated rate coefficients at 5 wt.% reagents of
kf=1.33x10-3/%2-min, and kd=6.19x10-4/%-min. A unit conversion to ppmm yields
kf=1.33x10-11/ppmm2-min and kd=6.19x10-12/ppmm-min. Other units may be more
suitable to certain models.
A. Estimated Urban Equilibrium Atmospheric Carbamic Acid
Concentration A simplified scenario
For the estimation of CA, data from a typical rural site is utilized. This
estimate is based on work of Ram et al. based on ground field measurements in the
Indo-Gangetic plain Hisar site, in northern India [13]. From this work, the
concentration of NH4HCO3 can be written,
[NH4HCO3] wt.% = {(%,NH4HCO3)(WSIS(g/m3))/(TSP(g/m3))}

(6)

The values in eqn(6) from Ram et al. [12] at the Hisar site are the wt.% of inorganic
ammonium carbonate (i.e., 12%), the total atmospheric water-soluble inorganic
concentration (i.e., WSIS(g/m3)=45.6, and the total aerosol condensed phase
concentration (TSP(g/m3)=147). The result is [NH4HCO3(aq)]=4 wt.%. It is
important to note in this dataset the concentrations of [NH4+]=[HCO3-], so have been
grouped into the combined compound [NH4HCO3(aq)].
With a value of [HCO3-]=4 wt.%, an estimate of the aqueous CO2(aq), or its
equivalent carbonic acid, can be obtained from the equation,
H2CO3 <-> H+ + HCO3- .

(7)

The data from Table 3 is used to compute a reaction free energy of 36.3
kJ/mol [12]. Hence an equilibrium constant of K=4.3x10-7 is computed at 298 K. At
neutral pH=7, the concentration ratio [H2CO3]/[HCO3-]=0.23. Using the [HCO3-]=4
wt.% value results in the [H2CO3]=0.92 wt.% concentration. Finally, substitution into
eqn(3) above yields [CA]=0.05 wt.%=480 ppmm. Of significance is that this value
represents the urban, wintertime, concentration, and that 480 ppmm is greater than
the 31.7 ppmm value LD50 value toxic to the honeybee. Recall, it is observed that
primarily wintertime is more detrimental to bee health than summertime. Next, an
estimate of summertime carbamic acid concentration will be estimated.
An estimated summertime carbamic acid concentration can be estimated
based on the kinetic analysis above where the [CA] production is second order in
ammonia concentration. The question is then, what is the expected seasonal
variation in NH3 expected, as this value has not been measured? Assuming a typical
mid-latitude seasonal summer to winter temperature decrease of 25 Celcius,
together with the observation of a 2.2-fold increase in NH3 mixing ratio per 0.5

Celcius (ppmm NH3/Celcius) decrease in temperature obtained from diurnal

measurements (IASI data) [11], this results in a 3000-fold increase in NH3 during
mid-winter compared to mid-summer. This appears to be a large enhancement,
nevertheless with this value the estimated summertime Hisar India urban
concentration is estimated to be 0.2 ppmm. Now this value is below the LD50 value
for the honeybee and so is not expected to be toxic during summer.
4. Conclusions
In this work it is proposed that atmospheric carbamates produced from
available ammonia and carbon dioxide can lead to the honeybee colony collapse
disorder (CCD) effect. Carbamates are known insecticides so their production, if
verified by field measurement and further modeling, can lead to this devastating
condition. Using a computed carbamate insecticide LD50 value of 31.7 ppmm, it is
shown that the wintertime carbamic acid concentration is 480 ppmm at an urban
site in northern India (Hisar), hence toxic to the honeybee. An estimate of the
seasonal effect in carbamic acid concentration based on temperature leads to an
estimated value during summer of only 0.2 ppmm, hence non-lethal to the
honeybee. Atmospheric deposition onto pollen and other bee frequented areas can
explain the CCD effect.
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7

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JMJ