Environmental Monitoring and Assessment

, Volume 184, Issue 7, pp 4119–4126 | Cite as

Spatial and temporal variation of metal concentrations in adult honeybees (Apis mellifera L.)

  • Jozef J. M. van der Steen
  • Joop de Kraker
  • Tim Grotenhuis
Open Access
Article

Abstract

Honeybees (Apis mellifera L.) have great potential for detecting and monitoring environmental pollution, given their wide-ranging foraging behaviour. Previous studies have demonstrated that concentrations of metals in adult honeybees were significantly higher at polluted than at control locations. These studies focused at a limited range of heavy metals and highly contrasting locations, and sampling was rarely repeated over a prolonged period. In our study, the potential of honeybees to detect and monitor metal pollution was further explored by measuring the concentration in adult honeybees of a wide range of trace metals, nine of which were not studied before, at three locations in the Netherlands over a 3-month period. The specific objective of the study was to assess the spatial and temporal variation in concentration in adult honeybees of Al, As, Cd, Co, Cr, Cu, Li, Mn, Mo, Ni, Pb, Sb, Se, Sn, Sr, Ti, V and Zn. In the period of July–September 2006, replicated samples were taken at 2-week intervals from commercial-type beehives. The metal concentration in micrograms per gram honeybee was determined by inductive coupled plasma–atomic emission spectrometry. Significant differences in concentration between sampling dates per location were found for Al, Cd, Co, Cr, Cu, Mn Sr, Ti and V, and significant differences in average concentration between locations were found for Co, Sr and V. The results indicate that honeybees can serve to detect temporal and spatial patterns in environmental metal concentrations, even at relatively low levels of pollution.

Keywords

Metals Bioindication Pollution Honeybee 

Introduction

Bioindication is a time-dependent, sensitive registration of anthropogenic or anthropogenically altered environmental factors, by distinguished dimensions of biological objects and biological systems under defined circumstances (Stöcker 1980). Honeybees (Apis mellifera L.) are potentially highly useful as bioindicators in detecting and monitoring environmental pollution, given their worldwide usage for honey production and pollination and their wide-ranging foraging behaviour (Bromenshenk and Preston 1986; Raeymaekers 2006). Not surprisingly, studies on the use of honeybees and bee products for environmental monitoring have a relatively long history, dating back to at least 1935 (Crane 1984). Environmental pollutants included in these studies were, among others, pesticides, radioactive elements and heavy metals (Devillers and Pham-Delègue 2002). As for the latter, honeybees may take up heavy metals from all environmental compartments: soil, vegetation, air and water (Bromenshenk et al. 1985; Porrini et al. 2003). Heavy metals end up in these compartments after emission from a variety of mainly anthropogenic sources. A major source of heavy metals in the atmosphere, for example, is the combustion of fossil fuels which results in the emission of ultrafine metal-containing particles. These airborne particles eventually deposit on vegetation, soil or surface water. Honeybees pick up heavy metals from the environment through a wide range of pathways: by ingestion of polluted surface water, pollen and nectar, by impaction and inhalation of particles during flight and by adhesion of particles to their hairy bodies when moving over plant and soil surfaces during foraging. In this way, honeybees provide an integrated sample of the environmental compartments in the area within their flight range (c. 7 km2, Bromenshenk et al. 1985), and can therefore serve to indicate anomalies in the environmental distribution of trace metals in time and space (Raeymaekers 2006). Possible mechanisms behind detected anomalies can then be studied with other, more specific methods.

Heavy metals in bees and in bee products have been the subject of many studies (e.g. Bromenshenk et al. 1985; Conti and Botré 2001; Fakhimzadeh and Lodenius 2000; Kalnins and Detroy 1984; Leita et al. 1996; Roman 2005; Veleminsky et al. 1990). The most frequently studied metals were lead, cadmium, chromium, copper and zinc, which are known pollutants from transport and industrial activity, disseminated via combustion gases. Most studies focused on a limited number of metals and highly contrasting locations, and sampling was rarely repeated over a prolonged period. In our study, the potential of honeybees to detect and monitor metal pollution was further explored by measuring the concentration in adult honeybees of a wide range of 18 trace metals, 9 of which were not studied before, at three locations over a 3-month period. The specific objective of the study was to assess the spatial and temporal variation in concentration in adult honeybees of aluminium (Al), arsenic (As), cadmium (Cd), cobalt (Co), chromium (Cr), copper (Cu), lithium (Li), manganese (Mn), molybdene (Mo), nickel (Ni), lead (Pb), antimony (Sb), selenium (Se), tin (Sn), strontium (Sr), titanium (Ti), vanadium (V) and zinc (Zn). We chose to study the metal concentrations in adult worker bees as these are considered to provide more sensitive, reliable and up-to-date information about exposure of bees to metals in the environment than concentrations in pollen and honey (Bromenshenk et al. 1985; Jones 1987; Fakhimzadeh and Lodenius 2000; Porrini et al. 2002; Veleminsky et al. 1990).

Materials and methods

At three locations in the Netherlands, three honeybee colonies (replicates) per location were placed. During a 3-month period, from July to September 2006, samples of each honeybee colony were taken every 14 days. The concentration of metals in honeybees was determined chemically.

Study locations

Location Maastricht, Limburglaan

The study was conducted in Maastricht, Limburglaan. Maastricht is an urban area with cement industry and glass industry, and is located close to large industrial areas such as Liège in Belgium. The honeybee colonies were placed near the city centre, on the roof of the provincial government building.

Location Buggenum, Dorpstraat

Buggenum is a village in a rural area about 60 km north of Maastricht. In Buggenum, bricks are produced, and a large electric power plant is situated next to the village. This plant is powered by coal, natural gas and biomass.

Location Hoek van Holland, Prins Hendrikstraat

Hoek van Holland is situated in the Rijnmond region at the river mouth of the Nieuwe Waterweg, at the North Sea coast. The Rijnmond region includes the port of Rotterdam and a large industrial area where, among others, petrochemical industry, tank storage and tank transfer and waste treatment plants are situated.

Honey bee sampling method

Honeybee colonies were kept from winter till summer in the same apiary in Wageningen (The Netherlands) till distribution over the three locations. At each location, three honeybees colonies (A. mellifera) were placed. The colonies were kept in one-storey wooden hives with ten frames (Simplex measures NEN 061–50). This is the most commonly, commercially used type of hive in the Netherlands. During the study period of July, August and September 2006, every 2 weeks, a random sample of 100 to 150 worker honeybees was taken from the outer frame of the hive that was occupied with bees but without brood. Sampling was done by brushing bees with a plastic brush into a plastic container. This resulted in 18 bee samples per location (three replicates of six sampling dates) to be analysed for all metals per location. The samples were transported in a cooler box and stored in the freezer at −20 ± 5°C until analysis.

Measurement of heavy metal concentrations in bees

The chemical analyses on metals were carried out by the environmental research laboratory of the Province of Limburg (Hoofdgroep Milieu en Water, Bureau onderzoek en advies), using the inductive coupled plasma–atomic emission spectrometry (ICP-AES) technique. From each sample (i.e. from each combination of colony, sampling date and location), 25 frozen worker bees were taken at random from the sample. The bees were subsequently weighed, dried for 24 h at 120°C, weighed and destructed by boiling the sample at 170°C in a mixture of 25 ml HNO3 (70%) and HCl (37%) at a ratio of 1:3 (aqua regia). The resulting liquid was topped up to 50 ml with demi water. Five milliliters of the 50 ml was filtered over a cotton wool filter and analysed using ICP-AES. The resulting signals (nanograms per millilitre) were converted to nanograms per gram (parts per billion (ppb)) bee with a conversion factor (volume sample/(weight bees × mean percentage dry weight)) resulting in ppb metal dry weight which was subsequently converted to micrograms per gram bee (micrograms per gram dry material (dm)). The overall weight loss of the bee samples as a result of the drying process was 68%.

Statistical analyses

Per metal, a generalized linear mixed model analysis was done assuming a lognormal distribution of the concentration data. Differences in concentrations between dates or locations were considered significant at P values ≤0.05, using Tukey’s multiple comparisons test. Temporal differences in concentration were assessed by comparing the 2-week sample values for each location. Spatial differences in concentration were assessed by comparing the mean values of the entire 3-month study period between locations.

Results and discussion

Temporal and spatial variation in metal concentrations

The 2-week sample values of metal concentrations (averages of the three replicate samples) are presented for each location in Table 1. Different lowercase letters indicate per location (row) statistically significant differences between metal concentrations in samples taken at different dates. For nine of the metals included in our study, no differences between 2-week sample values were found, and the concentrations were apparently constant over time. For the other nine metals (Al, Cd, Co, Cr, Cu, Mn, Sr, Ti and V), significant differences between 2-week sample values were found in at least one of the study locations. The fluctuations in concentration indicate a significant variation in exposure of honeybees to these metals in the environment.
Table 1

Metal concentrations in worker honeybees (micrograms per gram dry matter) from three locations, sampled at 2-week intervals (July–September 2006)

Element

Location

Sampling date

20 July

3 Aug

17 Aug

31 Aug

14 Sept

28 Sept

Al

Maastricht

15.10b

10.75ab

5.9a

6.8a

9.89ab

9.3ab

Al

Buggenum

11.55bc

10.93bc

4.6a

6.6ab

15.52c

11.07bc

Al

Hoek van Holland

10.70bc

13.20c

6.15ab

5.57a

12.17c

9.49abc

As

Maastricht

0.72a

0.70a

0.66a

0.76a

0.68a

0.83a

As

Buggenum

0.70a

0.69a

0.77a

0.76a

0.70a

0.71a

As

Hoek van Holland

0.68a

0.67a

0.69a

0.69a

0.69a

0.75a

Cd

Maastricht

0.09ab

0.09ab

0.07a

0.17ab

0.24ab

0.75b

Cd

Buggenum

0.14a

0.25a

0.10a

0.18a

0.19a

0.71a

Cd

Hoek van Holland

0.13ab

0.06ab

0.05a

0.05a

0.50b

0.25ab

Co

Maastricht

0.10a

0.10a

0.08a

0.11a

0.14a

0.12a

Co

Buggenum

0.26ab

0.21ab

0.16a

0.33b

0.16a

0.16a

Co

Hoek van Holland

0.10a

0.11a

0.09a

0.10a

0.11a

0.09a

Cr

Maastricht

0.27b

0.21ab

0.16a

0.18ab

0.24ab

0.23ab

Cr

Buggenum

0.23ab

0.23ab

0.15a

0.21ab

0.25ab

0.28b

Cr

Hoek van Holland

0.27ab

0.22ab

0.18a

0.18a

0.28b

0.22ab

Cu

Maastricht

14.69a

18.37a

19.16a

16.86a

17.64a

19.74a

Cu

Buggenum

12.69ab

11.65a

11.85a

15.50ab

12.57ab

19.77b

Cu

Hoek van Holland

14.21a

14.33a

12.84a

13.13a

15.23a

15.80a

Li

Maastricht

0.05a

0.02a

0.01a

0.01a

0.02a

0.02a

Li

Buggenum

0.03a

0.02a

0.02a

0.01a

0.02a

0.03a

Li

Hoek van Holland

0.05a

0.04a

0.01a

0.01a

0.03a

0.01a

Mn

Maastricht

24.45ab

28.31ab

20.69a

41.98ab

68.76b

45.10ab

Mn

Buggenum

31.04a

28.42a

29.16a

47.34a

48.40a

50.80a

Mn

Hoek van Holland

32.11a

30.44a

26.48a

28.87a

34.48a

34.37a

Mo

Maastricht

0.77a

1.16a

1.07a

0.64a

0.73a

0.54a

Mo

Buggenum

0.53a

0.42a

0.36a

0.57a

0.75a

0.66a

Mo

Hoek van Holland

0.55a

0.55a

0.51a

0.50a

0.68a

0.46a

Ni

Maastricht

0.37a

0.44a

0.34a

0.26a

0.22a

0.19a

Ni

Buggenum

0.29a

0.47a

0.25a

0.28a

0.29a

0.29a

Ni

Hoek van Holland

0.43a

0.35a

0.29a

0.26a

0.41a

0.20a

Pb

Maastricht

0.41a

0.37a

0.26a

0.31a

0.55a

1.26a

Pb

Buggenum

0.27a

1.10a

0.19a

0.30a

0.53a

0.58a

Pb

Hoek van Holland

1.00a

0.30a

0.27a

0.35a

1.67a

0.55a

Sb

Maastricht

0.12a

0.10a

0.11a

0.11a

0.18a

0.13a

Sb

Buggenum

0.11a

0.10a

0.12a

0.15a

0.09a

0.12a

Sb

Hoek van Holland

0.19a

0.07a

0.11a

0.09a

0.10a

0.11a

Se

Maastricht

1.38a

1.23a

1.24a

1.30a

1.50a

1.53a

Se

Buggenum

1.35a

1.27a

1.24a

1.38a

1.28a

1.22a

Se

Hoek van Holland

1.24a

1.20a

1.21a

1.17a

1.15a

1.17a

Sn

Maastricht

0.51a

0.44a

0.47a

0.44a

0.62a

0.52a

Sn

Buggenum

0.54a

0.68a

0.49a

0.43a

0.50a

0.42a

Sn

Hoek van Holland

0.76a

0.47a

0.51a

0.47a

0.44a

0.44a

Sr

Maastricht

1.82ab

2.99b

1.54ab

0.95a

1.05a

1.00a

Sr

Buggenum

0.99a

1.02a

0.70a

0.86a

0.89a

1.00a

Sr

Hoek van Holland

2.18a

2.40a

1.97a

1.36a

1.33a

0.94a

Ti

Maastricht

0.45b

0.37ab

0.16a

0.22ab

0.43b

0.47b

Ti

Buggenum

0.34bc

0.41bc

0.09a

0.17ab

0.55c

0.39bc

Ti

Hoek van Holland

0.54c

0.51bc

0.20ab

0.17a

0.50bc

0.35abc

V

Maastricht

0.040ab

0.032ab

0.015a

0.015a

0.054b

0.033ab

V

Buggenum

0.028b

0.026b

0.006a

0.006a

0.042b

0.029b

V

Hoek van Holland

0.083a

0.14b

0.10a

0.093a

0.31b

0.31b

Zn

Maastricht

67.81a

72.36a

59.18a

72.03a

82.83a

100.46a

Zn

Buggenum

73.66a

75.54a

70.70a

94.52a

71.60a

95.44a

Zn

Hoek van Holland

63.38a

68.98a

61.61a

61.14a

71.49a

74.76a

Concentration values are calculated as means of three independent replicate samples

Different lowercase letters indicate per location (row) statistically significant differences between metal concentrations in samples taken at different days

For all but three metals, no significant differences in mean concentration (over the entire study period) between locations could be detected. This indicates that the overall environmental exposure of honeybees to the metals Al, As, Cd, Cr, Cu, Li, Mn, Ni, Pb, Sb, Se, Sn, Ti and Zn during the study period was comparable in Maastricht, Buggenum and Hoek van Holland. The overall mean concentrations of Co, Sr and V, however, differed significantly between the study locations (Table 2). These spatial differences might be caused by differences in industrial activity near these locations. Markedly more significant temporal (nine) than spatial (three) differences were found. This probably indicates that the temporal fluctuations in source strength over a 3-month period are greater than the more structural differences between locations. In a small and densely populated country as the Netherlands, spatial differences may be expected to be limited. However, as our method does not provide information on sources and mechanisms, any explanation of the observed differences, spatial as well as temporal, will remain speculative. In case the variations in metal concentrations in time and space detected with honeybees are considered to be a reason of concern, other, more specific methods will have to be used to investigate the causal mechanisms. For example, use could be made of the Enrichment Factor (Chester et al. 1999), to determine whether trace metals in the air have significant non-crustal sources.
Table 2

Metal concentrations in worker honeybees (micrograms per gram dry matter) in samples from three locations

Element

Maastricht

Buggenum

Hoek van Holland

Al

9.17a

9.33a

9.07a

As

0.72a

0.73a

0.69a

Cd

0.16a

0.21a

0.11a

Co

0.11a

0.21b

0.10a

Cr

0.21a

0.22a

0.22a

Cu

17.66a

13.75a

14.22a

Li

0.02a

0.02a

0.02a

Mn

35.08a

37.97a

30.99a

Mo

0.79a

0.53a

0.54a

Ni

0.30a

0.31a

0.31a

Pb

0.45a

0.42a

0.55a

Sb

0.12a

0.11a

0.11a

Se

1.36a

1.29a

1.19a

Sn

0.50a

0.51a

0.51a

Sr

1.42ab

0.90a

1.61b

Ti

0.33a

0.28a

0.34a

V

0.03a

0.02a

0.15b

Zn

74.72a

79.59a

66.70a

Concentration values are calculated as sample means over the entire study period (7 July to September 2006)

Different lowercase letters indicate per location (row) statistically significant differences between sample means over the entire study period

Comparison with previously reported concentrations

For Al, Co, Li, Mo, Sb, Sn, Sr, Ti and V, no previous reports on their concentrations in adult honeybees have been published. The ranges of the concentrations of these metals as found in our study are as follows: Al, 4.6–15.52 μg g−1; Co, 0.08–0.33 μg g−1; Li, 0.01–0.05 μg g−1; Mo, 0.36–1.16 μg g−1; Sb, 0.07–0.19 μg g−1; Sn, 0.44–0.76 μg g−1; Sr, 0.70–2.18 μg g−1; Ti, 0.09–0.55 μg g−1; and V, 0.006–0.31 μg g−1. For As, Cd, Cr, Cu, Mn, Ni, Pb, Se and Zn, published reports on concentrations in adult honeybees are available from a wide variety of sampling locations. These values are presented in Table 3, together with the ranges of concentrations found in our study. The method of analysis to determine metal concentrations in bees was either ICP-AES, as in our study, or atomic absorption spectrometry. Kump et al. (1996) compared both methods for Cr, Cu, Mn, Ni, Pb and Zn and found only significant differences between these methods for Cr. The concentrations of the metals measured in our study are all within the bandwidth of the values reported in the literature, with the exception of Mn and Se. The concentrations we found for these two metals are lower than reported from other studies, but in the same order of magnitude. In general, the metal concentrations in the present study were at the lower or middle-lower end of the spectrum of concentration values found in other studies and often match the range of concentrations reported for supposedly relatively ‘clean’ locations. This indicates that the level of metal pollution at our three study locations was relatively low. The high concentrations, in absolute terms, of Cu, Mn and Zn are comparable to values found in other studies and are most likely due to the relatively high natural concentrations of these metals in pollen (Lambers et al. 1998), on which the bees feed.
Table 3

Metal concentrations in adult honeybees in the current and previous studies

Element

Current study

Previous studies

Concentration range (μg g−1)

Concentration range (μg g−1)

Comments

Reference

As

0.67–0.83

<0.5–12.5

72 sites (rural–urban)

Bromenshenk et al. 1985

<0.1

Hives without CCA

Kalnins and Detroy (1984)

0.77–1.11

Hives with CCA

Kalnins and Detroy (1984)

Cd

0.05–0.75

<0.6–>1.8

72 sites (rural–urban)

Bromenshenk et al. 1985

2.89–3.43

Non-contaminated sites

Conti and Botré 2001

2.87–4.23

Sites in city centre/near highway

Conti and Botré 2001

0.03–0.18

Control sites

Fakhimzadeh and Lodenius (2000)

0.05–1.2

Industrial sites

Fakhimzadeh and Lodenius (2000)

1.1–1.9a

Near crossroad with heavy traffic

Leita et al. (1996)

0.14–0.16a

Agricultural-forest region

Roman (2005)

0.10–0.17a

Industrialized region

Roman (2005)

0.16–1.34

Relatively clean locality

Veleminsky et al. (1990)

0.74–1.75

Industrial locality

Veleminsky et al. (1990)

Cr

0.15–0.28

0.054–0.080

Non-contaminated sites

Conti and Botré 2001

0.052–0.116

Sites in city centre/near highway

Conti and Botré 2001

1.4 ± 0.2a

Different locations

Kump et al. (1996)

<0.06–0.34

Hives without CCA

Kalnins and Detroy (1984)

0.58–0.8

Hives with CCA

Kalnins and Detroy (1984)

<0.1–3.6

National park

Porrini et al. (2002)

<0.1–1.2

City centre

Porrini et al. (2002)

0.05–0.18a

Agricultural-forest region

Roman (2005)

0.16–0.23a

Industrialized region

Roman (2005)

Cu

11.65–19.77

13–15

Control sites

Fakhimzadeh and Lodenius (2000)

14–27

Industrial sites

Fakhimzadeh and Lodenius (2000)

35.7 ± 1.5a

Different locations

Kump et al. (1996)

8.68–9.70

Hives without CCA

Kalnins and Detroy (1984)

9.86–10.5

Hives with CCA

Kalnins and Detroy (1984)

15.16–30.55

Relatively clean locality

Veleminsky et al. (1990)

31.89–37.68

Industrial locality

Veleminsky et al. (1990)

Mn

20.69–50.80

75.7 ± 5.6a

Different locations

Kump et al. (1996)

Ni

0.19–0.47

0.12–0.42

National park

Porrini et al. (2002)

0.13–0.43

City centre

Porrini et al. (2002)

0.27–0.42a

Agricultural-forest region

Roman (2005)

0.36–0.50a

Industrialized region

Roman (2005)

Pb

0.19–1.67

0.52–1.00

Non-contaminated sites

Conti and Botré 2001

0.64–1.25

Sites in city centre/near highway

Conti and Botré 2001

0.58–0.62

Control sites

Fakhimzadeh and Lodenius (2000)

0.27–1.4

Industrial sites

Fakhimzadeh and Lodenius (2000)

1.4–3.0a

Near crossroad with heavy traffic

Leita et al. (1996)

0.15–0.55

National park

Porrini et al. (2002)

0.45–0.95

City centre

Porrini et al. (2002)

1.5–30

Far from–near busy highway

Pratt and Sikorski (1982)

0.28–0.29a

Agricultural-forest region

Roman (2005)

0.64–1.01a

Industrialized region

Roman (2005)

0.58–2.47

Relatively clean locality

Veleminsky et al. (1990)

3.68–9.28

Industrial locality

Veleminsky et al. (1990)

Se

1.15–1.53

1.84–2.38a

Agricultural-forest region

Roman (2005)

2.16–5.98a

Industrialized region

Roman (2005)

Zn

61.14–100.64

55–73

Control sites

Fakhimzadeh and Lodenius (2000)

59–100

Industrial sites

Fakhimzadeh and Lodenius (2000)

202 ± 5a

Different locations

Kump et al. (1996)

52.5–76.2a

Near crossroad with heavy traffic

Leita et al. (1996)

90.34–188.72

Relatively clean locality

Veleminsky et al. (1990)

153.34–204.4

Industrial locality

Veleminsky et al. (1990)

aICP-AES analyses

Sources of metals in the hive environment

The commercial-type beehives used in our experiment have metal or metal-based components, such as stainless steel frame holders and wood-preserving coatings. ICP-AES analysis of samples from the frame holders and from paint of the landing board at the hive entrance revealed traces of As, Cr, Cu and Ni in both types of material (L. Goessen, personal communication). Thus, we cannot exclude that at least part of the load of these metals in the sampled bees originated from hive-associated sources. Kalnins and Detroy (1984) studied the effect of the use of the wood preservative chromated copper arsenate (CCA) in hives on the concentrations of As, Cr and Cu in bees. They found that the use of CCA significantly enhanced the concentrations of As and Cr in bees, but the concentrations of Cu were not significantly affected (Table 3). The lack of effect on Cu is probably due to the much greater importance of pollen as a source of this metal in bees. The concentrations of As found in our study correspond with those from hives treated with CCA in Kalnins and Detroy’s study (1984) and are therefore probably the consequence of exposure to hive-associated sources rather than to sources in the external environment. As for Cr, the concentrations found in our study correspond with those from hives not treated with CCA, suggesting that the Cr-containing materials of the hive were not an important source of contamination in this case.

Conclusion

Our results indicate that honeybees can serve to detect temporal and spatial patterns in environmental metal concentrations, even at relatively low levels of pollution. A restriction on the potential use of apiculture for biomonitoring of metal pollution is posed by the application of metal components and metal-based wood preservatives in commercial-type beehives.

A next step will be to determine sources of variation in metal concentrations. For that purpose, larger scale studies are required that allow for detailed statistical analysis. For example, we will conduct a follow-up study on spatial variation of metal concentrations in honeybees covering 150 locations across the Netherlands, which will be analysed with geostatistical methods.

Notes

Acknowledgements

We thank Dr. M. Severijns, Dr. J. Pijnenburg (Province of Limburg) and Dr. P. Kummu (DCMR Rijnmond) for their help in selecting the study locations, Ing. L. Goessen (Province of Limburg) for the chemical analyses of the samples, Mr. J. Withagen (Wageningen UR) for the statistical analyses and Dr. P. Medrzycki for constructive discussions about the use of honeybees as bioindicators of heavy metals.

Open Access

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Copyright information

© The Author(s) 2011

Authors and Affiliations

  • Jozef J. M. van der Steen
    • 1
  • Joop de Kraker
    • 2
  • Tim Grotenhuis
    • 3
  1. 1.Plant Research InternationalWageningenNetherlands
  2. 2.Environmental Sciences ProgrammeOpen Universiteit NederlandHeerlenNetherlands
  3. 3.Section Environmental TechnologyWageningen UniversityWageningenNetherlands

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