Honey Bees: Estimating the Environmental Impact of Chemicals - Chapter 10 pdf

conifer-centrations in different honey types collected from meadow andforest areas far from any known source of pollution, and iv determinethe indicator capability of honey for bioavaila

10 The role of honey bees in

be presented as a circle with a few kilometers radius It seems that thehoney could be a good random sample, representative of a broad area.Radionuclides, cations, and chemical compounds deposited as fallout due

to global atmospheric pollution or as constitutive elements or trace ments of soil can migrate upwards by plant uptake Concentrations of 137Cs

ele-in various honey types durele-ing the 1990s ele-in Croatia are presented ele-in thisreport The results of analyses of honey samples archived in Austria,Germany, and Slovenia from 1952 through 1995 provide an intriguing andunique history of 137Cs pollution in Europe The research also documentsthe levels of 137Cs, 40K, Ca, Fe, Rb, Sr, Cu, Zn, Pb, Ni, Mn, and Cr in soils,coniferous tree branches, and honey, and compares the transfer from soilinto nectar honey, mixtures of nectar and honeydew honey, and honeydewhoney in fir and spruce forests in Croatia For all of the elemental concen-

trations investigated, no significant differences, at level P0.05, werefound between honeydew honey and mixed honey, regardless of the soiltype where the honey was collected from Elemental transfer factors fromsoils into nectar honey were significantly lower than those for honeydewhoney

Honey bees in radioactive environmental monitoring

In many cases, the spread of environmental contaminants is related to airpollution The first incidence of air pollution is lost in unrecorded history,but it certainly goes back to the time of the discovery of fire Air pollutionrefers to the presence in the outdoor atmosphere of one or more contami-nants, occurring in quantities, of a duration, and with characteristics thatare known to be injurious to human, animal, and plant life, or to property,

or that unreasonably interfere with the comfortable enjoyment of life andproperty [1] Once released from sources into the atmosphere, pollutantscan be transported large distances due to the global atmosphere circula-tion Any factor that restricts the air movement will prevent the movementand dispersion of pollutants entering the atmosphere In addition to large-scale effects of air movement, local air circulation in valleys and on theslopes of hills or mountains is very important from an air pollution view-point, especially during pollutant deposition processes.

In the past century, as well as nowadays, environmental pollution hasbeen closely connected to human activities and industrial development.Developments in the field of atomic energy have introduced radioactiveparticles as a new and serious type of environmental pollution Some ofthe radionuclides formed in nuclear reactions are the most potent poisonsknown Moreover, there is no way, except radioactive decay by time, ofneutralizing radionuclides Additionally, radionuclides cannot be detected

by human senses, and many members of the public are nervous of orfrightened by any manifestation of radioactivity

Radioactive pollution and random representative sample

Radionuclides, as well as heavy metals and trace elements, occur either asnormal constituents of soils or as a result of dry or wet depositionalprocesses due to global atmospheric contamination The natural radionu-clide 40K is a normal constituent of soils, while the presence of 137Cs in soils

is an artifact of global atmospheric radioactive pollution The cesiumisotope 137Cs was produced as a by-product of the atmospheric testing ofthermonuclear weapons during the period extending from the 1950s to the1970s It was distributed globally within the stratosphere and deposited aswet fallout and/or during dry deposition processes Since the 1970s, themain contributors of atmospheric radionuclides have been operationalreleases from nuclear power plants and nuclear reactor accidents The lastsignificant release of radioactive cesium that was deposited on the earth’ssurface occurred mainly in Europe, during and after the Chernobyl acci-dent of 1986

The contamination of Croatian territory following the Chernobyl dent is illustrated by the 137Cs content (kBq m2) that was found in the first

inci-25 cm of vertical soil profiles (Figure 10.1) Chernobyl-derived 137Cscontamination of the Croatian landscape was not uniform Lika and asmall part of Western Slavonija were the highest contaminated areas,while the Adriatic shore and Eastern Slavonija were significantly less cont-aminated The ratio between the highest (near Gracˇac) and the leastcontaminated area of Croatia was about 50:1 with respect to Chernobyl-derived 137Cs fallout [2]

A relatively short contamination period combined with great ences in the timing and amount of rain at the time of and immediately

differ-Honey and environmental monitoring in Croatia 161

following the accident produced the significant variations in

considered to be the result of local meteorological conditions during each

consequence of deposition by numerous events over an extended period,which minimizes any local variation, total weapon-testing-derived cesiumpollution can be regarded as generally uniform over the whole Croatianterritory

Deposited cesium penetrates slowly from the soil surface into deepersoil layers [3] depending strongly on the soil type [2] Sorption processes

and mica minerals, particularly illite, results in the rapid and nearly versible cesium immobilization in the topsoil layer [4] Meanwhile, cesium,

irre-as well irre-as the other radionuclides that behave like cations, can be movedupward by plant uptake This process depends on various factors: plant

Figure 10.1 137 Cs concentration (kBq m2) in the first 25 cm of vertical soil profiles

in Croatia.

species, sorption and desorption processes in soil, mineral soil tion, grain size and soil types, lateral cesium migration, and so on.

composi-Certain plant species are known as cesium pollution indicators, but theuptake by each individual plant can be very different In the first place, itdepends on the presence of free cesium in the species’ root system zoneand competitive effects of potassium [5–10] Different soil types show dif-ferences in the ratio of sorbed to fixed cesium, in soil size fractions, in pH

profiles and, consequently, in cesium transfer from soil to plants [11–18].Even after relatively homogeneous contamination, all of these factorscould introduce a wide range of contaminant variability in a local area.The representativity of any single-point taken sample could be questioned.Although additional samples could be taken near the sample in questionduring or shortly after the initial sampling, this option would be difficult toenact some years after the contamination In Table 10.1, this is illustrated

inside a circle of radius 150 m at Milanov vrh in the Gorski Kotar area.The terrain is a carbonate one, and the soil thickness ranges from a fewcentimeters up to several meters or more, with soil completely missing insignificant areas where carbonate rocks are exposed Moreover, the soilitself is not homogeneous Soil horizons are differently developed, and thethicknesses of layers of organic matter are also very different Gravel-size

deposited in the first 15 cm of vertical soil profiles were found to varythroughout the circle of radius 150 m and across the 5-year period by

found in soils developed on limestone than in soils developed on dolomite,

where the sample was collected or the year of collection

Honey and environmental monitoring in Croatia 163

Table 10.1 Activities of 137 Cs and 40 K (Bq kg1) in soils collected inside a circle of

radius 150 m at Milanov vrh

1994 51.2 0.8* 507.0 22.1 Beneath fir tree in forest

1994 208.0 1.3 367.1 22.9 Beneath fir tree in forest

1995 60.4 0.8 497.3 8.8 Beneath spruce tree in forest

1996 134.0 1.2 349.2 8.1 Beneath spruce tree in forest

1996 152.5 1.3 282.0 6.4 Beneath fir tree in forest

1997 157.0 2.2 449.4 14.8 From narrow forest meadow

1998 156.2 2.0 405.7 12.6 Beneath spruce tree beside forest road

1998 441.6 3.7 378.2 14.1 From the middle of wide forest meadow

1998 273.4 2.7 433.9 12.3 Beneath fir tree beside forest road Range 51.2–441.6 282.0–507.0

Mean  170.5120.6 407.672.5

Note

*Counting error.

Alternatively, plants and the bees that visit them can provide a means

of detecting and monitoring radionuclide pollution over large areas.Depending on the honey bee pasture types and the plant uptake factors

of honey [19–21] Heather plants, Calluna vulgaris especially, are species

well-known as indicators of cesium pollution [22, 23]

Honey bees and their products have been used as indicators and tors of a variety of environmental pollution because of their ability toreflect the immediate environmental conditions [24–29] In searching forand gathering food, honey bees set up flight patterns, which change asavailable sources or preferences change The total potential foraging area

moni-of a honey bee colony can be presented as a large circle extending outfrom the hive Honey bees readily fly up to 4 km in all directions from their

diminishing returns with respect to the economics of the energy consumed

by bees during very long foraging flights, a somewhat smaller area of some

nectar gathering It is very important to note that over such a large area,all of the numerous different environmental factors are included in thesamples produced by the bees

While collecting nectar and honeydew, honey bees provide a compositesample from thousands of different points spread across a large area On atypical day, a colony of honey bees will make several tens to hundreds ofthousands of foraging flights [31] Depending on the amount of nectar ineach honey sac, between 100 000 and 150 000 foraging flights are needed toproduce 1 kg of honey [32] To fill its honey sac, on average a foraging beeneeds to visit 80 to 150 individual flowers [33] Thus, the honey inside eachbeehive represents a random average sample collected from several tens

of millions of single points over a period of time It seems that a sample ofhoney is probably the best composited random sample and, as such, pro-vides the most representative values for the average concentrations ofbioavailable elements in an area’s environment

Sampling and analysis

Since 1990, 12 stationary apiaries (five placed in the Gorski Kotar area),

stocked with Apis mellifera carnica, have been used for environmental

monitoring of radionuclides In 1994, six colonies were placed in fir andspruce woods in the Gorski Kotar area and new measurements of radionu-clides and selected elements were begun, increasing the network of hivesbeing monitored by 1995

Measurements of radionuclides and selected elements in soil, ous trees, and different honey types have been carried out to: (i) followthe behavior and the fate of cesium in the environment, (ii) determine theindicator capability of honey for cesium, (iii) examine selected cation con-

conifer-centrations in different honey types collected from meadow andforest areas far from any known source of pollution, and (iv) determinethe indicator capability of honey for bioavailable elements in the environ-ment.

The Gorski Kotar area is relatively far away from any significant source

of environmental pollution This part of Croatia is exposed only to tants that are deposited as fallout from global atmospheric contamination.Honey, soil, fir and spruce branch samples are collected regularly at sixlocations: Milanov vrh, Trsˇc´e, Lividraga, Suha recˇina, Fuzˇine, andZalesina The positions of the soil, honey, fir, and spruce samplinglocations are shown in Figure 10.2

pollu-Soil sampling and analysis

Soil samples were taken regularly at the six above-mentioned locationsand at three additional locations in the Gorski Kotar area during theperiod from 1994 to 1998 Each sample was a composite taken from one

At each of the sampled locations, all samples were collected inside a circle

Honey and environmental monitoring in Croatia 165

Figure 10.2 Sketch map of the Gorski Kotar area, Croatia, indicating soil,

honey, fir, and spruce sampling locations.

of radius 150 m Two main soil types were analyzed; soils developed on thePaleozoic bedrock and Quaternary lacustrine sediments (predominantlysilicate soils), and soils developed on the Mesozoic limestones anddolomites (predominantly carbonate soils).

Air-dried soil was passed repeatedly through a 2-mm sieve and tered to produce material with a grain size less than 0.5 mm The sievedfraction was then dried at 105°C to a constant weight and stored in count-

gamma-spectrometric analysis Prior to X-ray fluorescence (XRF) analyses, sievedand dried soil samples were pressed into pellets

Honey sampling, analysis, and results

A control series of nectar honey types was collected during the summermonths from 1990 to 1996 from the whole Croatian territory Since 1993,samples of honey have been collected regularly in the summer and earlyautumn from the Gorski Kotar area, Croatia A long-time series of varioustypes of honeydew honey and heather honey was collected in Austria,Germany, and Slovenia from 1952 through 1995

Honey samples were collected mechanically, by extracting honey fromcombs Honey types (nectar honey, mixed nectar and honeydew honey,and honeydew honey) were identified on the basis of pollen analyses [34]and electrical conductivity measurements [35] carried out by using a multi-range conductivity meter HI 8733 (Hanna Instruments) Radionuclideactivity and selected element concentrations in honey were determined bygamma-ray spectrometry and the XRF method

A standard sample of 300 pollen grains was used for pollen and honeytype determination Results of pollen determination in some typical Croat-ian bush-tree and meadow nectar honeys collected in the period

honey samples collected during 1990 was not done Nectar honey types(meadow, mixed, or bush-tree) were selected on the basis of the prevailing

honey bee pasture on the respective locations Castanea sativa, Robinia

pseudoacacia, and Tilia sp were dominant pollen types in nectar bush-tree

honey collected between 1991 and 1993 Tilia sp was not found in samples

of honey from 1992 Crataegus sp was identified only in honey collected in

1992, Rubus sp only in honey collected in 1992 and 1995 Among meadow pollen types in honeys collected in 1991, Leguminosae and Umbelliferae were more prevalent than Taraxacum officinale, Trifolium sp., and Ono-

brychis viciaefolia In nectar meadow honeys collected in 1992 and 1993, Compositae and Brassicaceae dominated over Umbelliferae and Rosaceae.

Among pollen grains determined, in honey collected in the period

1994–1996, Castanea sativa, Robinia pseudoacacia, Taraxacum officinale,

Tilia sp., Centaurea sp., Trifolium sp., Leguminosae, Umbelliferae, and Brassicaceae were more prevalent than Lotus corniculatus, Onobrychis

viciaefolia, Plantago sp., Salvia sp., Campanula sp., Anthyllis sp., torolopus sp., and Thymus sp.

Alec-In contrast to nectar honey that would have been obtained primarilyfrom blossoms, honeydew is a sugar solution yielded by the hindgut ofhomopteran insects Honeydew appears on deciduous trees sporadically,but predominantly in coniferous woods Conifers are inhabited byhomopteran insects, among which leaf-lice and shield-shaped-lice prevail

Conifers are inhabited by green fir-lice (Cinaria pectinatae, mainly, but C.

pilicornis, C viridescens, Lachnus grossus or L piceae can be found

fre-quently in fir and spruce forests in the Gorski Kotar area) Occasionally,

shield-shaped-lice like Physokermes piceae or P hemycryphus can also be

found on the fir and spruce trees These insects pierce the bark of theyoungest branches and the needles of fir and spruce trees in search offood Honeydew is the secretion of these insects

The results of electrical conductivity measurements and pollen analyseswere used to distinguish nectar honey, mixed nectar and honeydew honey,and honeydew types of honey In the case when pollen grains were usually

was classified as nectar honey If pollen grains were present and electrical

classi-fied as mixed nectar and honeydew honey In cases when pollen grains

the sample was classified as honeydew honey

Honey and environmental monitoring in Croatia 167

Table 10.2 Pollen determination results of typical Croatian mixed bush-tree and

meadow nectar honey collected in early 1990s

Sample Pollen type (%)

Coniferous tree sampling and analysis

The youngest segments of fir and spruce branches (including ing bark and needles) were taken as composites up to 6 m above theground At each of the observed locations, 15 trees of both fir and sprucewere marked inside a circle of less than 150 m radius Branches were cutannually in early autumn, at the end of September or early October Thetips of the fir branches grown that year were collected only in 1994 Ineach of following years, the tips of the branches and older branch seg-ments, including the segments grown in 1994, were taken for analyses Thetips of the spruce branches were collected for the first time in 1995 In each

accompany-of following years, the tips accompany-of the branches and 1-year-old spruce branchsegments were also taken for analyses In order to check the possiblechanges in radionuclide activity during a year, the tips of the branches and1-year-old branch segments were sampled monthly from a single fir treeduring 1996 and 1997 Few fir and spruce trees were harvested in autumn

well as separately in needles and in the wooden parts of branches, ing the bark All samples were dried at 105°C to constant weight, homoge-

and measured by the gamma-spectrometric method Prior to XRF ses, samples were pressed into pellets

analy-The gamma-spectrometric method

spectrome-try, using a low-background hyper-pure germanium (HPGe) tor detector system coupled to a 4096 channel analyzer Depending onsample mass and activity, spectra were recorded for times ranging from

semiconduc-80 000 to 150 000 seconds, and analyzed with a personal computer (PC)

were calculated from the 661.6 and 1460.7 keV peaks, respectively.Double counting errors were taken as the detection limit The activities of

collection

The XRF method

Samples of soil, fir, and spruce material pressed into pellets or samples ofhoney in native form were placed in counting vessels Specimens were

X-rays were detected by the system’s Si-detector (resolution 165 eV at5.9 keV) and Canberra MCA S-100 software Counting times were 10 000

to 50 000 seconds United States National Bureau of Standards (NBS)Orchard Leaves SRM 1571 and Soil 5 were used for quantitative analysis

X-ray spectra were evaluated by International Atomic Energy Agency

Analysis – Elemental Sensitivities” [36]

Statistical evaluation

The majority of sampled honey was collected from a mixture of silicateand carbonate terrains Less than one-third of honey samples originatedfrom well-known, strictly silicate or carbonate terrain Because only asmall number of well-defined samples of soil or honey were available, only

the t-test was used in statistical evaluation of collected data Statistical

analyses of nectar honey compared to soil type were not done because ofthe small number of samples collected from the strictly silicate or carbon-ate terrains However, no significant differences have been found for themixed nectar and honeydew honey as well Taking into account the afore-mentioned facts, the average element concentrations in all of the soilsamples measured were taken for transfer factor calculations

Radionuclide activities in honey during the 1990s in Croatia

(meadow nectar, bush-tree, and mixed honey) that was collected between

1990 and 1996 in Croatia are presented in Table 10.3 Previously

in bush-tree and meadow nectar honey types [19, 37] This finding was

years after the serious cesium contamination event of the Chernobyl

below the instrument detection limit On the basis of data presented in

Honey and environmental monitoring in Croatia 169

Table 10.3 Activities of 137 Cs and 40 K (Bq kg1) in Croatian nectar honey types

(mixed, meadow, or bush-tree honey) collected between 1990 and 1996, Gorski Kotar area excluded

nd, not determined.

honey types decreased by approximately half the activity obtained in the

remained more or less the same during the whole time period studied

and competitive effects of potassium on the cesium uptake cannot beexcluded [6, 7, 9] While the potassium content was constant with time, the

plants is a consequence of cesium bioavailability in the plants’ root systemzone Plants are able to take up only free cesium because sorbed cesium isnot bioavailable [10, 12, 13, 16, 18] It seems that about 10 years afterinitial deposition, the average cesium bioavailability for most of themeadow and bush-tree nectar plants became insignificantly low compared

Significant differences in the activity levels and long-term behavior of

groups (collected from the Gorski Kotar area) containing honeydewhoney (Table 10.4) Honey groups collected from the Gorski Kotar areainclude nectar (predominantly meadow) honey, mixed nectar and honey-dew honey and, more or less pure fir and/or spruce honeydew honey The

samples collected from 1993 to 1996 in the Gorski Kotar area, cesium wasfound in relatively high concentrations; more than 10 times (or even over

100 times in some cases) higher than in nectar honey from Croatia in thesame respective year

Table 10.4 Activities of 137 Cs and 40 K (Bq kg1) in honey from the Gorski Kotar

area, collected between 1993 and 1999

nd, not determined.

This finding suggests than honeydew honey could be used as the

pre-sented data clearly indicated a general trend toward a decreasing value of

samples were composed of numerous nectar and mixed honeys (each lected in a single year) Few honeydew honey samples were collected in

very slowly with time as a consequence of its radioactive decay andbioavailability from coniferous plants

Honey as a long-term indicator of 137 Cs pollution in Central

European countries

As was mentioned earlier, honeydew honey can be used as an indicator of

in archived samples of collected honey, it was thought it would be possible

to retrospectively detect radioactive contamination events Numeroushoney samples that had been collected and kept by beekeepers over aperiod from 1952 to 1995 were found for locations in Central Europeancountries located between the North sea and the Adriatic sea (Austria,

activities, which were corrected for radioactive decay and recalculated on

Austrian spruce honeydew honey samples collected in the Alps regionfrom 1952 to 1994 (mainly in a circle of radius 30 km around Lunz am See)

Honey and environmental monitoring in Croatia 171

Figure 10.3 Activities of 137 Cs in Austrian dominantly spruce honeydew honey

col-lected in the Alps region, mainly in the surroundings of Lunz am See, between 1952 and 1994.

clearly indicates cesium fallout peaks (Figure 10.3) The expected steadydecrease in cesium activity following the initial fallout peaks from weapontesting and the much larger fallout from the Chernobyl accident has notoccurred In both cases, there was a reduction in cesium levels followingthe initial exposure events, but the activity levels did not return to the pre-exposure conditions Apparent reductions from 1989 through 1993, follow-ing the peak of the 1986 Chernobyl release, were contradicted by

mixed meadow and honeydew) honey samples collected in Germany(Table 10.5), as well as in mixed meadow/chestnut and honeydew honey

been found for the same year for the same or very similar types of honey

in both countries Such results could be explained by the fact that samples

of honey were collected from different locations, locations that have beencontaminated differently by cesium during the main fallout events in the

vul-garis) are significantly higher than in honeydew honey Heather is

con-sidered to be an excellent cesium pollution indicator, and so apparently is

Table 10.5 Activities of 137 Cs and 40 K (Bq kg1) in honey collected between 1965

1977 76.6 13.7 320.1 1.9 heather (Calluna vulgaris)

1977 93.0 13.8 125.4 1.2 heather (Calluna vulgaris)

1975 149.5 13.7 23.9 0.5 honeydew

1969 82.2 13.8 176.1 1.6 heather (Calluna vulgaris)

1968 106.3 14.0 238.1 1.9 heather (Calluna vulgaris)

1966 106.8 15.0 447.0 2.7 heather (Calluna vulgaris)