Journal of Applied Ecology 2012, 49, 118–125
doi: 10.1111/j.1365-2664.2011.02079.x
Abundance and diversity of wild bees along gradients
of heavy metal pollution
Dawid Moroń1*, Irena M. Grześ2,3, Piotr Skórka4, Hajnalka Szentgyörgyi3,
Ryszard Laskowski3, Simon G. Potts5 and Michal-- Woyciechowski3*
1
Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, S l--awkowska 17, 31-016 Kraków,
Poland; 2Department of Zoology and Ecology, University of Agriculture, A. Mickiewicza 24, 31-120 Kraków, Poland;
3
Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland; 4Institute of
Zoology, Poznań University of Life Sciences, Wojska Polskiego 71 C, 60-625 Poznań, Poland; and 5School of
Agriculture, Policy and Development, Reading University, Reading, Berks RG6 6AR, UK
Summary
1. Wild bees are one of the most important groups of pollinators in the temperate zone. Therefore,
population declines have potentially negative impacts for both crop and wildflower pollination.
Although heavy metal pollution is recognized to be a problem affecting large parts of the European
Union, we currently lack insights into the effects of heavy metals on wild bees.
2. We investigated whether heavy metal pollution is a potential threat to wild bee communities by
comparing (i) species number, (ii) diversity and (iii) abundance as well as (iv) natural mortality of
emerging bees along two independent gradients of heavy metal pollution, one at Olkusz (OLK),
Poland and the other at Avonmouth (AVO), UK. We used standardized nesting traps to measure
species richness and abundance of wild bees, and we recorded the heavy metal concentration in pollen collected by the red mason bee Osmia rufa as a measure of pollution.
3. The concentration of cadmium, lead and zinc in pollen collected by bees ranged from a background level in unpolluted sites [OLK: 1Æ3, 43Æ4, 99Æ8 (mg kg)1); AVO: 0Æ8, 42Æ0, 56Æ0 (mg kg)1),
respectively] to a high level on sites in the vicinity of the OLK and AVO smelters [OLK: 6Æ7, 277Æ0,
440Æ1 (mg kg)1); AVO: 9Æ3, 356Æ2, 592Æ4 (mg kg)1), respectively].
4. We found that with increasing heavy metal concentration, there was a steady decrease in the
number, diversity and abundance of solitary, wild bees. In the most polluted sites, traps were empty
or contained single occupants, whereas in unpolluted sites, the nesting traps collected from 4 to 5
species represented by up to ten individuals. Moreover, the proportion of dead individuals of the
solitary bee Megachile ligniseca increased along the heavy metal pollution gradient at OLK from
0Æ2 in uncontaminated sites to 0Æ5 in sites with a high concentration of pollution.
5. Synthesis and applications. Our findings highlight the negative relationship between heavy metal
pollution and populations of wild bees and suggest that increasing wild bee richness in highly contaminated areas will require special conservation strategies. These may include creating suitable
nesting sites and sowing a mixture of flowering plants as well as installing artificial nests with wild
bee cocoons in polluted areas. Applying protection plans to wild pollinating bee communities in
heavy metal-contaminated areas will contribute to integrated land rehabilitation to minimize the
impact of pollution on the environment.
Key-words: Apoidea, biodiversity, cadmium, contamination, lead, pollen, pollinators, zinc
Introduction
Wild bees (hereafter bees) are a major group of pollinators in
the temperate zone (Kevan 1999). Bees provide key ecosystem
*Correspondence authors. E-mails: [email protected];
[email protected]
services essential to maintaining wild plant diversity (Ashman
et al. 2004; Aguilar et al. 2006; Potts et al. 2010) and agricultural productivity (Klein et al. 2007; Gallai et al. 2009; Lenda,
Skórka & Moroń 2010). Many plant species that are directly
dependent on insect pollination for fruit and seed production
(Wilkaniec, Giejdasz & Prószyński 2004; Morandin &
Winston 2005; Velthuis & van Door 2006) might experience
2011 The Authors. Journal of Applied Ecology 2011 British Ecological Society
Effects of heavy metals on wild bees 119
pollination limitation when pollinator species are scarce
(Ashman et al. 2004). Therefore, the declines of wild bee populations reported throughout Europe and North America (Steffan-Dewenter, Potts & Packer 2005; Biesmeijer et al. 2006;
Potts et al. 2010) are alarming.
Many potential factors that negatively affect wild bee communities and are suspected of being responsible for pollinator
decline have been identified. One of the major factors causing
declines of bee diversity and abundance is habitat loss and
fragmentation driven mostly by intensification of agriculture
(Banaszak 1995; Steffan-Dewenter 2003; Le Féon et al. 2010).
Other factors include pesticide use (Alston et al. 2007; Brittain
et al. 2010), the impact of non-native invasive species (Moroń
et al. 2009), competition with managed populations of Apis
mellifera (Walther-Hellwig et al. 2006) or Bombus terrestris
(Kenta et al. 2007), pathogen spread (Colla et al. 2006) and
genetic introgression (Kraus et al. 2011). Although heavy
metal pollution is likely to be a problem affecting much of the
European Union (Lado, Hengl & Reuter 2008), studies are
urgently needed to provide insights into the effects on bees.
Heavy metal contamination can have negative effects on
invertebrate diversity (Syrek et al. 2006; Beyrem et al. 2007;
Piola & Johnston 2008) as a result of differences between species in susceptibility to stress (Kammenga & Riksen 1996).
Taking into consideration the complicated interactions among
organisms (e.g. competition and predation), elimination of one
species group by heavy metal pollution could even increase the
diversity and ⁄ or abundance of others more resistant to pollution (Russell & Alberti 1998; Nahmani & Lavelle 2002; Migliorini et al. 2004). Some studies show an impact of heavy metals
on pollinators (Nieminen, Nuorteva & Tulisalo 2001; Mulder
et al. 2005). It has been demonstrated that metals (Cd, Cu, Fe,
Mn and Zn) may play a direct role in the widespread decline of
the butterfly Parnassius apollo in Finland (Nieminen, Nuorteva & Tulisalo 2001). On the other hand, Mulder et al. (2005)
hypothesized that butterfly decline in the NE of the Netherlands is an indirect effect of pollutant stress (e.g. Cd, Cu and
Zn) on plants. Very little evidence exists on how heavy metal
pollution affects solitary, wild bee communities (Moroń et al.
2010). Moroń et al. (2010) detected a direct negative impact of
Zn contamination on the survival of the solitary bee, Osmia
rufa, whereas Szentgyörgyi et al. (2011) did not find a significant correlation between heavy metal pollution (Cd, Pb and
Zn) and bumblebee diversity. Despite the small number of
studies, in a questionnaire undertaken by Kosior et al. (2007),
specialists considered heavy metal pollution to be one of the
most important factors causing bumblebee decline in Europe
(ranked 6th of 16 stressors).
The aim of our study was to investigate the relationship
between heavy metal pollution and wild bee communities. To
this end, we compared wild bee species richness and diversity
as well as the natural mortality of emerging bees along two gradients of heavy metal pollution, one in Poland and the other in
the UK, where the main pollutants were cadmium, lead and
zinc (Zygmunt, Maryański & Laskowski 2006; Stefanowicz,
Niklińska & Laskowski 2008). We used standardized nesting
traps to measure the species richness and abundance of wild
bees (Tscharntke, Gathmann & Steffan-Dewenter 1998; Westphal et al. 2008). We hypothesized that with increasing concentration of heavy metals in the environment, there would be a
reduction in wild bee species richness, abundance and diversity.
The study was conducted within the framework of the EU
Integrated Projects, ALARM and STEP, which assess largescale risks to biodiversity as well as population trends within
European pollinators (http://www.alarmproject.net, Settele
et al. 2005; http://www.STEP-project.net).
Materials and methods
FIELD SITES
The study was carried out in the vicinity of two Zn ⁄ Pb smelters, one
located in Olkusz (OLK), Poland (5016¢38¢¢N, 1928¢17¢¢E), and the
second in Avonmouth (AVO), UK (5130¢28¢¢N, 0241¢01¢¢W). Both
smelters produced a similar spectrum of heavy metal contamination,
that is, cadmium (Cd), lead (Pb) and zinc (Zn); however, the smelter
in OLK has operated since 1967, whereas the AVO smelter since 1923
(abandoned in 2003). Metal concentration in the soil layer in the
OLK region exceeds 20 mg kg)1 of cadmium, 800 mg kg)1 of lead
and 2200 mg kg)1 of zinc and in the AVO region exceeds
350 mg kg)1 of cadmium, 25 000 mg kg)1 of lead and
12 000 mg kg)1 of zinc (Stefanowicz, Niklińska & Laskowski 2008).
Seven meadow sites in OLK and five in AVO were selected along
the pollution gradient (Table 1) based on the concentration of metals
in the topsoil (Stefanowicz, Niklińska & Laskowski 2008) and representing the full range of pollution in the two regions. Mean annual
temperature and precipitation in the OLK area are 8 C and 650 mm
and in AVO are 11 C and 600 mm. Sites were more than 1 km apart
and had similar soils (OLK: poor sandy soils; AVO: alluvial gley
soils), size (c. 20 ha) and landscape (OLK: mixture of meadows and
Scots pine forests; AVO: agriculture fields and pastures). The distance
from a site centre to the nearest permanent grassland was not correlated with site pollution index (for more information, see Statistical
Analysis; OLK: rs = )0Æ07, N = 7, P = 0Æ91, AVO: rs = 0Æ6,
N = 5, P = 0Æ35). Also, the distances to the nearest watercourse
(OLK: rs = )0Æ39, N = 7, P = 0Æ40, AVO: rs = 0Æ50, N = 5,
P = 0Æ45), nearest forest (OLK: rs = 0Æ14, N = 7, P = 0Æ78, AVO:
rs = 0Æ20, N = 5, P = 0Æ78) and human settlements (OLK:
rs = 0Æ04, N = 7, P = 0Æ96, AVO: rs = 0Æ72, N = 5, P = 0Æ17)
were uncorrelated with the site pollution index. Study sites were
selected to keep plant communities constant along the gradients
(OLK: ChAll: Koelerion glaucae, ChCl: Molinio-Arrhenatheretea,
ChAss: Epilobio-Salicetum capreae, ChCl: Nardo-Callunetea, AVO:
ChAss: Arrhenatheretum elatioris) (Stefanowicz, Niklińska & Laskowski 2009). In addition for five of the seven sites at the OLK gradient (OLK1, OLK4–7), we did not detect a correlation between site
pollution index and plant species richness (OLK: rs = )0Æ10, N = 5,
P = 0Æ95; AVO gradient plant data were not available at the time of
bee sampling).
TRAP NESTS AND EXPERIMENTAL SET-UP
To evaluate the effects of heavy metal pollution on the diversity and
abundance of bees, standardized nest sites for above-ground nesting
bees (Tscharntke, Gathmann & Steffan-Dewenter 1998; Steffan-Dewenter 2002; Moroń et al. 2008; Westphal et al. 2008) were established
in each site. Studies were conducted during 2004–2006 in OLK area
2011 The Authors. Journal of Applied Ecology 2011 British Ecological Society, Journal of Applied Ecology, 49, 118–125
120 D. Moroń et al.
Table 1. Heavy metal (Cd – cadmium, Pb – lead, Zn – zinc) concentration in dry pollen collected by red mason bee Osmia rufa on sites along
pollution gradients near Olkusz (OLK) and Avonmouth (AVO), distance of these sites to sources of pollution and number of collected trap nests
Metal concentration (mg kg)1)
Number of traps
Site
Distance (km)*
Cd
Pb
Zn
2004
2005
2006
OLK1
OLK2
OLK3
OLK4
OLK5
OLK6
OLK7
AVO1
AVO2
AVO3
AVO4
AVO5
1Æ2
1Æ4
1Æ6
3Æ6
4Æ0
8Æ3
19Æ8
0Æ7
1Æ3
2Æ8
5Æ9
104Æ7
5Æ62
2Æ59
6Æ71
4Æ13
3Æ06
1Æ73
1Æ32
9Æ31
6Æ39
3Æ58
0Æ89
0Æ76
196Æ64
126Æ30
277Æ05
197Æ13
115Æ47
57Æ26
43Æ37
356Æ16
345Æ58
238Æ99
61Æ52
42Æ05
269Æ76
232Æ26
440Æ11
317Æ93
165Æ77
107Æ67
99Æ75
592Æ42
381Æ08
322Æ23
98Æ51
55Æ90
7
–
–
7
7
7
6
–
–
–
–
–
6
7
6
7
7
7
7
–
–
–
–
–
6
6
7
7
7
6
7
2
4
4
3
6
*Distance from the smelter; this measure is not consistent with distances to spoil tips that are also pollution sources; thus, distance from
the smelter is not strictly correlated with pollen contamination.
and in 2006 in AVO area. At each site, seven trees were randomly chosen separated by distances of >200 m, each fitted with one trap nest
for bees at a height of c. 3 m. Each trap consisted of 110, 25-cm-long
stems of common reed Phragmites australis (Cav.) Trin. ex Steud.
with nodes in the middle. The mean reed stem diameter was
7Æ8 ± 1Æ9 mm (range 6–12 mm). A bundle of stems was tied with a
string and covered with a plywood roof (OLK) or half a PVC pipe
(AVO). Trap nests were protected from attack by birds with metal
mesh. The traps were set up at the beginning of April and collected in
October. Because of random events (e.g. storms and vandalism), the
number of collected nests per site per year varied between 6 and 7 for
OLK and between 2 and 6 for AVO gradient (Table 1). During winter, trap nests were stored in laboratory conditions at +4 C. In
spring, all reed stems with brood chambers of bees were removed and
placed at room temperature in plastic containers. For each nest, the
species and the number of emerged individuals were identified.
To standardize our evaluation of pollution, we analysed heavy
metal concentrations in pollen collected by bees. Four randomly
selected trap nests in each site were populated with 75 cocoons of the
solitary red mason bee Osmia rufa (Linnaeus, 1758). We artificially
added O. rufa because the abundance of naturally occurring bees in
trap nests was generally too low to provide an adequate analysis of
heavy metals in collected pollen. The red mason bee is broadly distributed in Poland and the UK with no special associations with habitat
type or food preferences (polylectic species) (Banaszak 2010). Pollen
collected by female O. rufa and deposited in brood chambers as food
for larvae was excavated and used to evaluate heavy metal pollution.
CHEMICAL ANALYSES
Five samples of pollen deposited by O. rufa in five different stems of
common reed were randomly collected from each nest trap. We
selected pollen from brood cells in which individuals died before feeding on the collected pollen, that is, development stopped at the egg
stage. Before analysis, samples were homogenized and dried at
105 C. Samples were analysed for total concentrations of cadmium,
lead and zinc with AAnalyst 800 Spectrometer (PerkinElmer, Boston, MA, USA). Total fractions of cadmium and lead were analysed
using graphite furnace atomic absorption spectrometry (GF-ETAAS), and concentrations of zinc were analysed by flame atomic
absorption spectrometry (FAAS). Total metals were extracted with
Suprapur HNO3 (Merck, Darmstadt, Germany). Three blank samples were also analysed for background contamination, and analytical precision was assessed with three reference samples with known
metal concentrations (lyophilized bovine liver CRM 185R, European
Commision). Percentage recovery was 80%, 86% and 126% for cadmium, lead and zinc, respectively.
STATISTICAL ANALYSIS
Concentrations of the metals were highly correlated with the pollution gradients; therefore, we decided to describe the study sites with a
single measure of pollution rather than analysing separate models for
each metal separately or choosing one arbitrarily. We performed a
principal component analysis using metal concentrations in the pollen, and in further analyses, we used a pollution index defined as the
first principal component (PC1pollen) score of each site (Zygmunt,
Maryański & Laskowski 2006).
To examine the relationship between soil and pollen contamination, we used heavy metal concentrations in soil of OLK1, OLK4–7
and AVO1–5 given by Stefanowicz, Niklińska & Laskowski (2008).
We calculated the first principal component score (PC1soil) for soil
contamination as described for pollen. Then, we tested the correlation
between PC1soil and PC1pollen for each gradient with Spearman rank
correlation.
Spearman’s rank correlation was used to assess the relationship
between pollution level and the community of trap nesting bees by
comparing data on the number of individuals, the number of species
and the species diversity with the pollution index. The hierarchical
richness index (HRI) was used as a diversity measure (Sparks 2000).
The HRI provides an assessment of both taxonomic diversity and
abundance in a single measure (French 1994), and it ranks sites
according to easily definable objective criteria (Fabricius, Burger &
Hockey 2003). The relationship between contamination level and survival of wild bees was examined by assessing natural mortality against
the pollution index with Spearman’s rank correlation. Natural mortality was calculated as the number of adults emerging from the trap
nest divided by the number of brood cells. However, a sufficient
sample size for statistical analysis was only available for Megachile
ligniseca (Kirby, 1802) in the OLK gradient (sites OLK 1–3, 5–7).
2011 The Authors. Journal of Applied Ecology 2011 British Ecological Society, Journal of Applied Ecology, 49, 118–125
Abundance, species richness, diversity and natural mortality were calculated as the mean per trap nest per site per year. The data sets for
OLK and AVO gradients were analysed separately. Because O. rufa
were introduced into the sites, this species was excluded from all analyses. All statistical analyses were performed using R v.2.11 software
(R Development Core Team 2010).
Results
We recorded six bee species emerging from trap nests
(Table 2). Two species comprised about 60% of the total number of bees: Hoplitis adunca (Panzer, 1798) (32%) and Megachile ligniseca Alfken, 1924 (24%) at OLK, and M. centuncularis
(Linnaeus, 1758) (33%) and M. willughbiella (Kirby, 1802)
(32%) at AVO.
Concentrations of cadmium, lead and zinc in pollen collected by O. rufa ranged from background levels at unpolluted
sites [OLK: 1Æ3, 43Æ4, 99Æ8 (mg kg)1); AVO: 0Æ8, 42Æ0 56Æ0
(mg kg)1), respectively] to a high level [OLK: 6Æ7, 277Æ0, 440Æ1
(mg kg)1); AVO: 9Æ3, 356Æ2, 592Æ4 (mg kg)1)] at sites in the
vicinity of the smelters. Metal concentrations in pollen were
significantly correlated (Table 3a,b). In the principal component analysis, PC1 explained 97Æ0% and 97Æ2% of the total
variability in concentrations of metals at OLK and
AVO, respectively. The heavy metal concentration in pollen
(PC1pollen) was positively correlated with that in top soil
(PC1soil) (OLK: rs = +0Æ90, N = 5, P = 0Æ083, AVO:
rs = +1Æ00, N = 5, P = 0Æ017; Fig. 1).
Table 2. Species and number of solitary bees (excluding Osmia rufa)
collected from trap nests established along heavy metal pollution
gradient in Olkusz (OLK) and Avonmouth (AVO). All species
belong to superfamily Apoidea and family Megachilidae
Species
OLK
AVO
Hoplitis adunca
Megachile alpicola
Megachile centuncularis
Megachile ligniseca
Megachile willughbiella
Osmia caerulescens
190
115
88
141
0
65
0
0
25
11
24
16
Table 3. Correlation matrix of metal concentrations in pollen at
Olkusz (a) and Avonmouth (b)
(a) OLK
Zn
Pb
Cd
(b) AVO
Zn
Pb
Cd
Zn
Pb
1Æ00
0Æ98***
0Æ91**
1Æ00
0Æ97***
1Æ00
0Æ95*
0Æ98*
1Æ00
0Æ95*
*P < 0Æ05; **P < 0Æ01; ***P < 0Æ001.
AVO, Avonmouth; OLK, Olkusz.
Pollen pollution index (PC1pollen)
Effects of heavy metals on wild bees 121
3·5
2·5
1·5
0·5
–0·5
–1·5
–2·5
–2·5
–1·5
–0·5
0·5
1·5
2·5
3·5
Soil pollution index (PC1soil)
Fig. 1. Relationship between soil pollution index (PC1soil score) and
pollen pollution index (PC1pollen scores). Rhombi represent sites in
Olkusz area, and circles represent sites in Avonmouth area.
The mean number of bee species decreased with increasing
metal concentration (PC1pollen) (OLK: rs = )0Æ89, N = 7,
P = 0Æ012, AVO: rs = )0Æ82, N = 5, P = 0Æ089; Fig. 2a). In
the most polluted sites, we found none or only a single bee
species, whereas in unpolluted sites, we recorded 4–5 species.
Wild bee diversity (HRI) was negatively correlated with the
PC1pollen (OLK: rs = )0Æ86, N = 7, P = 0Æ024, AVO:
rs = )0Æ90, N = 5, P = 0Æ083; Fig. 2b). The number of
individual bees was significantly negatively correlated with
PC1pollen (OLK: rs = )0Æ86, N = 7, P = 0Æ024, AVO:
rs = )1Æ00, N = 5, P = 0Æ017; Fig. 2c). Up to ten individuals
emerged per trap in unpolluted sites and one individual from
the most polluted sites. The natural mortality of the solitary
bee M. ligniseca increased with increasing heavy metal concentration (PC1pollen) at the OLK gradient (rs = +0Æ94, N = 6,
P = 0Æ017; Fig. 3). The proportion of individuals that died
before emerging varied from 0Æ2 in uncontaminated sites to 0Æ5
in sites with a high level of pollution.
Discussion
Studies on the effects of heavy metal pollution on solitary, wild
bee communities are very rare (but see Moroń et al. 2010);
however, given the widely reported declines in pollinators in
parts of the world (e.g. Biesmeijer et al. 2006; Natural
Research Council 2006), it is critical to understand the underlying drivers of change if we mitigate against further losses and
avoid the negative impacts on pollination services (Potts et al.
2010). Heavy metal pollution is thought to affect pollinator
populations both negatively, for example, by harmful
intoxication (Beyrem et al. 2007; Piola & Johnston 2008), and
positively, for example, via a lower number of competitors
(Nahmani & Lavelle 2002; Migliorini et al. 2004). Despite this,
we only found a negative relationship between pollution and
bee community size (Fig. 2a,c). Decreasing hierarchial richness
index along the heavy metal gradients emphasizes the
combined effects of diminishing abundance as well as species
richness (Fig. 2b). Note that the same response to pollution
was found in two geographically distinct areas. The strong,
2011 The Authors. Journal of Applied Ecology 2011 British Ecological Society, Journal of Applied Ecology, 49, 118–125
122 D. Moroń et al.
1
1
(a)
Proportion of dead
individuals
Species
0·8
0·6
0·4
0·2
0
(b)
–3
–2
–1
0
1
2
3
Hierarchical
richness index
0·25
0
–2·5
–1·5
–0·5
0·5
1·5
2·5
3·5
Fig. 3. Relationship between natural mortality of emerged Megachile
ligniseca (per trap nest per site per year) and pollen pollution index
(PC1pollen scores) for the Olkusz gradient.
15
10
5
0
–3
–2
–1
0
1
2
0
1
2
3
10
8
Individuals
0·5
Pollen pollution index (PC1pollen)
20
(c)
0·75
6
4
2
0
–3
–2
–1
3
Pollen pollution index (PC1pollen)
Fig. 2. Relationship between (a) species richness, (b) diversity and (c)
abundance of wild bees (per trap nest per site per year) and pollen pollution index (PC1pollen scores). The rhombi represent sites along the
Olkusz gradient, whereas circles represent sites along the Avonmouth
gradient.
positive correlation between diversity of above-ground nesting
bees (about 5% of all bee species; Tscharntke, Gathmann &
Steffan-Dewenter 1998) and the diversity of all bee communities (Tscharntke, Gathmann & Steffan-Dewenter 1998; Westphal et al. 2008) supports the extrapolation of our findings to
all wild bee species.
The negative correlation between metal pollution and wild
bee communities may be the result of direct as well as indirect
mechanisms. Chronic intoxication of individuals by heavy
metals may lead directly to expenditure of additional energy
on detoxification (Silby & Calow 1989; Janczur, Kozłowski &
Laskowski 2000), which most frequently decreases fitness
parameters (Mozdzer et al. 2003). Indirectly, the pollution
affecting flowering plants (decreasing their diversity, abun-
dance and ⁄ or pollen quality; Sawidis & Reiss 1995) may, as a
result, reduce the availability of forage for bees. This study did
not determine whether direct or indirect mechanisms were
most important in the negative correlation between heavy metals and wild bee populations. However, a steady increase in
mortality among emerging M. ligniseca along the gradient
(Fig. 3) suggests that larvae feeding on contaminated pollen
were more at risk. Similar results were obtained for the wild
bee O. rufa, the larvae of which feed on pollen contaminated
with Zn (Moroń et al. 2010). This suggests a direct impact of
pollution on wild bee abundance, especially because plant
communities were comparable along the gradients.
This study is the first focusing on the contamination of pollen collected by wild bees rather than honeybees. Bee larvae
feed exclusively on pollen (Michener 2000); thus, in polluted
sites, they consume food that is contaminated with heavy
metals (Table 1). The main source of heavy metal pollution of
pollen is soil deposited on flowers or on the pollen during
transport to and placement in the bee’s nest (Szcze˛sna 2007;
Fig. 1). This suggests that the soil type (e.g. granulation) and
the type of flower can affect the deposition of heavy metals on
pollen (Szcze˛sna 2007). For bee species nesting in the ground,
the impact of polluted soil is likely to be even greater because
larvae are surrounded by highly contaminated material.
Adults may be intoxicated by heavy metals during nest building (e.g. excavating of soil) and constructing mud walls
between brood chambers. Different life strategies, for example,
sociality and food specialization (Michener 2000), may influence the susceptibility of bee species to heavy metal pollution.
Social species, for example, honeybees and bumblebees, can
cover long distances during foraging (Ratnieks 2000) and may
collect food outside the contaminated area, therefore avoiding
the negative effects of pollution. Polylectic species may avoid
collecting pollen from the plants that accumulate high levels of
heavy metals, but oligolectic bees that are linked with a specific
food source may be limited to foraging on more contaminated
plants. Because the susceptibility of wild bees to competition
varies with their biology, that is, whether they are social or solitary, oligolectic or polylectic species (Strickler 1979), pollution
2011 The Authors. Journal of Applied Ecology 2011 British Ecological Society, Journal of Applied Ecology, 49, 118–125
Effects of heavy metals on wild bees 123
may additionally modify the interactions among species. This,
however, requires further study.
Our findings demonstrate a negative correlation between
heavy metal pollution and populations of wild bees. We suggest that increasing wild bee richness in highly contaminated
areas will require special conservation strategies. Where there
is a direct effect of pollution (e.g. intoxication), the creation of
suitable sites for nesting may be most effective. We recommend
placing artificial nests in the contaminated areas because they
are simple to prepare and are low cost (Tscharntke, Gathmann
& Steffan-Dewenter 1998; Wilkaniec & Giejdasz 2003a;
Moroń et al. 2010). Additionally, wild bee abundance may be
boosted locally by attaching bee cocoons to the nests. It is
straightforward to produce cocoons of Anthophora plumipes
(Pallas 1772), Chelostoma florisomne (Linnaeus, 1758), O. rufa
and O. cornuta (Latreille, 1805) (Krunić & Stanisavljević
2006). There are many examples of successful management of
wild bees in agriculture, especially in orchards (Bosch & Kemp
2002; Wilkaniec & Giejdasz 2003b). However, only native bee
species should be introduced into contaminated habitats
because natural communities could be negatively affected by
non-native pollinators, for example, by competition (Kenta
et al. 2007).
In situations where bees are indirectly affected by pollution
(e.g. reduced plant species richness), it may be appropriate to
sow seed mixtures of wild flowers (Haaland, Naisbit & Bersier
2011). This would attract a large number of bees and bumblebees as well as hoverflies and some butterflies (Carreck & Williams 1997, 2002). Seed mixtures are beneficial to pollinators
and easy to establish, and by sowing in sequences from early
spring to summer, a long flowering period is provided (Haaland, Naisbit & Bersier 2011).
Implementation of conservation strategies to protect wild
bees across a range of heavy metal pollution levels will contribute to integrated land rehabilitation. Plants used in land rehabilitation (phytoremediation) will benefit from increased
numbers of pollinators because some are pollinated by insects
(e.g. Thlaspi spp.) (Baker, Reeves & Hajar 1994; Brown et al.
1994).
High concentrations of heavy metals in soils are a widespread problem (Lado, Hengl and Reuter 2008), and pollen
contamination is as detrimental to wild bees as habitat loss
or fragmentation (Kosior et al. 2007). It is possible that
some wild bee species will migrate from adjacent habitats to
polluted ones. However, the mean flight distance for most
wild bee species is <200 m (Gathmann & Tscharntke 2002)
so the boosting of populations on contaminated sites by
migrants does not seem very probable for most bee species.
It is more likely that bees nesting in contaminated sites will
forage further away. Szentgyörgyi et al. (2011) showed that
bumblebee diversity did not correlate with heavy metals in
the soil, which may be a consequence of their ability to fly
long distances (1–2 km; Greenleaf et al. 2007). The interrelationships between wild bees and plants are complex, and
our study emphasizes the need to undertake further investigations on bee communities in polluted habitats to develop
effective conservation strategies.
Acknowledgements
We wish to thank Tim Sparks for helpful comments on the initial manuscript.
Comments from three anonymous referees and the editor greatly improved the
quality of this paper. We thank A. Amirowicz, W. Celary, K. Kuszewska, P.
Mielczarek, S.P.M. Roberts, E. Ro_zej, A. Stefanowicz, E. Śliwińska, T. Tscheulin, M. Wantuch and M. Witek for their assistance in the field and laboratory.
This study was supported by the 6th EU Framework Programme within the
ALARM Integrated Project (GOCE-CT-2003-506675; Settele et al. 2005), the
7th EU Framework Programme within the STEP Collaborative Project (Status
and Trends of European Pollinators; 244090, http://www.STEP-project.net),
the research Grant of the Ministry of Science and Higher Education SPUB
3053 and DS ⁄ WBINOZ ⁄ INOS ⁄ 756 ⁄ 2007 and partially financed by research
project NN304 075135 from the Polish Ministry of Science and Higher Education to D. M. and M. W.
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Received 14 February 2011; accepted 29 September 2011
Handling Editor: Ingolf Steffan-Dewenter
2011 The Authors. Journal of Applied Ecology 2011 British Ecological Society, Journal of Applied Ecology, 49, 118–125