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Journal of Insect ConservationAn international journal devoted tothe conservation of insects and relatedinvertebrates ISSN 1366-638X J Insect ConservDOI 10.1007/s10841-012-9529-5

Sandpits provide critical refuge for bees andwasps (Hymenoptera: Apocrita)

Petr Heneberg, Petr Bogusch & JiříŘehounek

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ORIGINAL PAPER

Sandpits provide critical refuge for bees and wasps(Hymenoptera: Apocrita)

Petr Heneberg • Petr Bogusch • Jirı Rehounek

Received: 15 April 2012 / Accepted: 18 August 2012

� Springer Science+Business Media B.V. 2012

Abstract Evidence-based conservation allows the eval-

uation of both the collateral benefits and the drawbacks of a

wide range of human activities, like quarrying. In this

study, the community structure of bees and wasps

(Hymenoptera:Apocrita) in Central European sandpits was

investigated, focusing on the changes caused by quarrying

cessation and technical reclamation, as well as on the

changes caused by spontaneous succession leading to the

increased availability of food resources but also to the loss

of the number and size of available bare sand patches. The

bees and wasps demonstrated an exceptional ability to

colonize the newly emerging sand quarrying areas, and to

survive in them unless these were quarried as intensively as

to not allow the development of any early successional

vegetation. Both active and closed sandpits were found to

serve as important regional refuges for the persistence of

many rare species. In total, 221 species were detected, 53

of those were red-listed, with two species thought to be

regionally extinct. Typically, active quarrying was associ-

ated with the presence of Bembecinus tridens, Halictus

subauratus, H. maculatus, and Andrena nigroaenea. The

list of the species of conservation interest is provided, and

so is the detailed analysis of the life-history traits of the

species in relation to the presence of bare sand patches,

vegetation cover, quarrying intensity, and time elapsed

since the formation of each artificial habitat patch. Sandpits

as refuges for xerothermophilous and psammophilous

hymenopterans are usually completely and irreversibly lost

if the current legislature enforcing the technical reclama-

tion over spontaneous or assisted succession is applied in

all or most of the post-mining areas.

Keywords Artificial biotopes � Habitat conservation �Landscape restoration � Nest site availability �Post-industrial sites � Post-mining sites

Introduction

In recent years, the interest in the entomofauna of post-

industrial sites has increased (Babin-Fenske and Anand

2011; Milisa et al. 2010; Tropek et al. 2010; Harabis and

Dolny 2012; Heneberg 2012; Srba and Heneberg 2012). In

particular, post-mining sites, which are typically highly

degraded or even destroyed, represent habitats where suc-

cession starts on bare substrate. Conservation potential of

post-industrial sites was already demonstrated for butter-

flies (Benes et al. 2003; Turner et al. 2009; Lenda et al.

2012), dragonflies (Harabis and Dolny 2012), spiders

(Wheater et al. 2000), certain beetle species (Eyre et al.

2003; Warren and Buttner 2008; Boukal 2010; Topp et al.

2010), ants (Ottonetti et al. 2004, 2006), and the aquatic

invertebrates (Dumnicka and Galas 2006). Contrary to that,

post-industrial sites were found to be only slowly colonized

by taxa with low migration ability such as nematodes

Electronic supplementary material The online version of thisarticle (doi:10.1007/s10841-012-9529-5) contains supplementarymaterial, which is available to authorized users.

P. Heneberg (&)

Third Faculty of Medicine, Charles University in Prague,

Ruska 87, 100 00 Prague 10, Czech Republic

e-mail: petr.heneberg@lf3.cuni.cz

P. Bogusch

Faculty of Science, University of Hradec Kralove,

Rokitanskeho 62, 500 03 Hradec Kralove, Czech Republic

J. Rehounek

Calla—Association for Environmental Conservation, Ceske

Budejovice, Frani Sramka 35, 370 04 Ceske Budejovice 3,

Czech Republic

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J Insect Conserv

DOI 10.1007/s10841-012-9529-5

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(Hanel 2004, 2008), and are considered as potentially

deleterious (mostly due to the presence of residual con-

taminants) for the taxa migrating from the surrounding

landscape unaffected by the industrial activities (Lefcort

et al. 2010; Moron et al. 2012). Collectively, the results of

the above studies suggest that the post-industrial sites serve

as excellent refuges for disturbance-dependent endangered

organisms.

The legislation in many countries requires fast recla-

mation of these sites. At the present time, the Czech leg-

islation requires to re-establish the landscape to that before

quarrying. An exception are mines scheduled for inunda-

tion, where anthropogenic lakes are formed. The law pro-

vides powerful tools restricting the loss of land used for

agriculture or forestry, and thus the governmental author-

ities strictly target the re-establishment of forest and agri-

cultural land as the major (usually sole) target of quarry

reclamation. Strict application of these rules leads to the

very frequent destruction of valuable habitats, eradication

of rare species, and is often in conflict with nature con-

servation interests (Rehounkova et al. 2011). Despite the

legislation barriers, there is an increasing awareness that

post-mining sites might serve as local biodiversity hotspots

and as refuges of species of conservation interest (Tropek

et al. 2010; Koronatova and Milyaeva 2011; Prach et al.

2011), and that they should not be recognized as particu-

late, invariant and homogeneous, but rather as dynamic

entities supporting varying taxa in dependence on the

course and direction of succession of each respective post-

mining site (cf. the concept by Dennis et al. 2003). To

improve the current legislation on restoration and recla-

mation of the post-mining sites, conservation evidence of

the spontaneous succession processes is needed. The

inclusion of evidence-based conservation in the recent

legislative actions on environmental issues has the poten-

tial to dramatically improve the chances of forcing the

mining industry to deal with natural resource damages,

and, in particular, to deal with the provision of non-market

goods such as habitat for some endangered species

(Damigos and Kaliampakos 2003).

Among various insect groups proposed as typical bio-

logical indicators are the bees and wasps (Hymenop-

tera:Apocrita) (Taki et al. 2008; Howe et al. 2010; Mateos

et al. 2011; Vieira et al. 2011). Bees and wasps are espe-

cially useful as an indicator of the collateral benefits of the

quarrying activities since many of them require the pres-

ence of bare soil patches, and soil characteristics are con-

sidered as the limiting variables for the presence of at least

some of these species (Brockmann 1979; Cane 1991; Kim

et al. 2006; Polidori et al. 2010a; Heneberg 2012; Srba and

Heneberg 2012). The number of available high-quality

habitats for bees and wasps is rapidly decreasing

throughout the industrialized world. According to Farkac

et al. (2005), 41 species (13 %) of the superfamily Ves-

poidea are already thought to be extinct, and another 98

species (32 %) are thought to be endangered in the Czech

Republic. Similar numbers are known for the superfamily

Apoidea, as 146 Apoidea species (17 %) are thought to be

extinct, and another 370 species (44 %) are thought to be

endangered in the Czech Republic. Likewise, 52 % of

German bee species, 45 % of Swiss species, and 36 % of

British bee species are thought to be extinct or endangered

(Fellendorf et al. 2004). Bees and wasps are typically

associated with open habitats (steppes, rock outcrops, sand

dunes), many of which were turned in natural reserves.

Interestingly, the majority of Czech natural reserves known

for their extreme diversity of bees and wasps in 1940s and

1950s turned to be species-poor grassy or shruby habitats,

where the rare bee and wasp species occur only at few

small patches at the edges of each of the reserves. This

critical situation resulted from the widely implemented

conservation approach consisting of the ban of any human

activities within each reserve following its establishment.

The absence of any management and the removal of

grazing herbivores caused slow, but almost complete dis-

appearance of bare soil patches used by bees and wasps as

nest sites, resulting in almost complete disappearance of

numerous specialized ground-dwelling species from the

Czech landscape (Tropek and Rehounek 2011). It seems

that the only conservation management capable to reverse

the above-described situation is sod removal and controlled

re-introduction of herbivores or the introduction of distur-

bances caused by the operations of motor vehicles. These

methods were already applied at several nature reserves,

aimed to support survival of the last remaining population

of Bohemian sand pink (Dianthus arenarius subsp. bohe-

micus) in the reserve Klenec (Slechtova and Belohoubek

2010) and supported the return of numerous bees and

wasps in the reserve Na Plachte (Bogusch et al. 2006;

Bogusch unpubl.). These management approaches partially

resemble the activities associated with quarrying, which

thus deserve more thorough evaluation as provided in this

report. The species composition of hymenopterans at xe-

rothermophilous habitats in Central Europe is well known

(Westrich 1989; Blosch 2000; Farkac et al. 2005; Bogusch

et al. 2007; Wisniowski 2009; Macek et al. 2010), although

there are no comprehensive reports focusing exclusively on

the species composition of bees and wasps in sandpits and

other areas affected by active sand quarrying; these habitats

are reflected only in several faunistic reports dealing with

one or two localities each (Schluter 2002; Dvorak and

Bogusch 2008). Also worldwide, the species composition

of hymenopterans at post-industrial sites is poorly known.

The few exceptions are the data on the bee fauna of the

disused U.S. mining sites (Droege et al. 2009), German

limestone quarries (Krauss et al. 2009), and at a restored

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landfill in Southeast Canada (Richards et al. 2011). Helpful

summarization of evidence-based conservation approaches

supporting the bee habitats was recently published by

Dicks et al. (2010), however with no focus on post-mining

sites. Here we evaluate for the first time the community of

bees and wasps utilizing the sandpits, and analyze the

dynamics of this community in relation to the quarrying

cessation, reclamation activities, and to the presence of

bare sand patches and vegetation cover. The potential of

both active and disused sandpits in the conservation of

xerothermophilous and psammophilous bees and wasps is

discussed.

Materials and methods

Study area

The study was carried out in the Czech Republic (Central

Europe, 48—51�N, 12—19�E). In 2007, the Czech sand

quarrying industry included 169 active sandpits and grav-

elsand pits spanning over 114 km2 (Stary et al. 2008),

besides that there were numerous sites where the quarrying

had already been ceased. In the pilot experiment, sweeping

net collections were conducted at 16 randomly selected

localities. Based on the results of the pilot experiment,

which suggested a highly diversified presence of species of

conservation interest within each sandpit, the locations for

the installation of yellow-white Moericke traps’ were

selected. The traps were installed in 50 sandpits and gravel-

sandpits all over the Czech Republic (Fig. 1), together with

locations partially overlapping with those examined in the

first year (12 out of 16 initially screened sandpits). Since this

is the first study of bees and wasps of sandpits in extenso, the

selected sandpits were chosen to represent the whole spec-

trum of sandpits and gravel-sandpits present in the study

area. The altitude of the study sites ranged from 165 to

520 m above sea level. The study sites included sandpits in

agrarian lowlands (\250 m above sea level, mean annual

temperature 8.0–9.3 �C, mean annual precipitation

480–550 mm) and also those in the mostly woodland

uplands ([ 250 m above sea level, mean annual temperature

6.7–7.9 �C, mean annual precipitation 551–780 mm).

The study was based on a space-for-time substitution

paradigm (Pickett 1989). Thus, the sampling sites were

selected to represent the whole available range of quarrying

intensity, and to include the representative selection of

post-mining sites affected by either reclamation efforts or

subjected to spontaneous succession or natural regenera-

tion. The knowledge on the history of each respective study

site was based on the extensive monitoring of sandpits

performed by the first author in years 1992–2011 (Hene-

berg 2001; Heneberg 2009), and based on the aerial photos

taken in years 2008–2010, 2004–2006, and 2002–2003

(available from www.mapy.cz, cited as on 2 February 2012)

and in years 1949–1956 (available from kontaminace.

cenia.cz, cited as on 2 February 2012).

Sampling: pilot experiment

The pilot experiment included direct searching and

sweeping along transects, which covered the most attrac-

tive resourse patches in the 16 randomly selected sandpits,

and the close vicinity of all exposed vertical banks of each

sandpit. Within the sandpit, the surveyor walked at a slow

speed among any potentially attractive resource patches

and collected bees and wasps during an observational

period of 15 min; the observational period was eventually

shortened when more than ten specimens were captured at

the site. Species that could not be identified in the field

were killed by ethyl acetate vapors, and were kept for

identification later (cf. Banaszak-Cibicka and Zmihorski

2012). On transects, bees and wasps were netted by hand in

two periods, 20–29 April 2010 (leg. Jirı Rehounek, det. &

coll. Petr Bogusch) and 22–29 June 2010 (leg. Petr

Heneberg, det. & coll. Petr Bogusch).

Sampling: Moericke pan traps

Moericke traps were used to collect the specimens since

these traps have been successfully used for the collection of

bees and wasps in a wide range of habitats previously (cf.

Cruz-Sanchez et al. 2011; Vrdoljak and Samways 2012).

The traps were made from round-shaped 500 ml polypro-

pylene containers, 111 mm in diameter and 75 mm deep

(Simport, Beloeil, Canada), filled up to the upper quarter

with the soapy water with salt, which acted as a pre-

servative. The yellow-white combination of colors was

used consistently in the experiments. RAL 1021 rape yel-

low was sprayed only inside the traps, the outside remained

Fig. 1 Location of study sites (sandpits) in the Czech Republic.

Method of sampling at each of the sites is indicated

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white. This color combination is expected to provide rea-

sonable estimate of proportional species richness and

abundance and is ideal for comparative biodiversity sur-

veys (Vrdoljak and Samways 2012). Since this study did

not aim to provide the full inventory survey, no additional

colors were used. The collected specimens were tempo-

rarily stored in 75 % ethanol until pinned for identification.

To avoid the possible interference caused by differences in

overall diversity of Hymenoptera at individual sampling

sites, only up to 13 traps were allowed for each sandpit

(mean 9.5 ± 1.6 traps per each sandpit).

The sampling was conducted between 29 May and 10

July 2011 (leg. Petr Heneberg, det. & coll. Petr Bogusch).

At each respective locality, the yellow traps were installed

for 24 ± 2 h at a sunny, warm weather. In six exceptional

cases, the exposition of traps was prolonged to 42 h since

the respective capture was affected by cloudy weather and

showers not reflected in the weather forecast. Trapping was

performed only once at each respective locality. Since the

captures were performed in a range of 43 days, control

captures were conducted to assure that the abundance and

diversity of species captured were comparable within the

time period used. The repeated control captures were per-

formed at four localities sampled already on 29–30 May

2011, and sampled again on 9–10 July 2011. The repeated

captures revealed that there were no significant differences

in either abundance or diversity of bees and wasps (t test

between Chao-1 estimators P [ 0.05). Since this study did

not aim to provide the full inventory survey, we did not use

any additional capture term, which may result in under-

scoring of the early spring species (e.g., Andrena vaga). At

each study site, the Moericke traps were placed to micro-

habitats with the highest proportion of bare sand patches,

but preferably in the vicinity of flowering plants, since

these habitats were expected to attract the most diverse

spectrum of bees and wasps (Roulston and Goodell 2011).

The percentage of vegetation cover was measured by visual

estimation at each habitat patch, and the percentage of bare

sand was also measured (if available, bare sand patches

included also the those covered in part by Corynephorus

grasslands, dwarf annual siliceous grasslands, perennial

open siliceous grasslands, patches of Trifolium arvense,

and other types of sparsely vegetated habitats; vertical sand

slopes were also included; thus the percentage of grass-

lands and vegetation cover may add to more than 100 %).

Sampling: control datasets

The obtained data were compared in detail with three other

datasets obtained in the Czech Republic, the different

datasets were obtained in: a rare relict of naturally occur-

ring sand patches (sand dune Vesecky kopec, Sezemice:

Veska, district Pardubice, Czech Republic, 50�020N,

15�510E; Bogusch 2008), an area with bare soil patches

maintained by regular human disturbances (military

training areas throughout the Czech Republic, 48—51�N,

12—19�E, Bogusch 2010), and random habitats of the cul-

tural landscape (135 km2 area in the vicinity of Blatna,

district Strakonice, Czech Republic, 49�250N, 13�520E;

Bogusch 2003; Bogusch and Straka 2006). The material of

the above three studies was collected by the combination of

Moericke traps and sweeping. All three control datasets

originated from the same geographic area (Czech Republic)

and represented similar sampling effort (791–1,292 col-

lected specimens per each dataset). The number of sampling

sites and the diversity of microhabitats included was dif-

ferent, reflecting the features of each of the control datasets.

Statistical analyses

Analyzed were any members of the infraorder Apocrita,

with the exception of Formicidae. Since some of the con-

trol datasets did not include Apis mellifera and Bombus

spp., these taxa were omitted from all the analyses com-

paring the dataset obtained in sandpits with the three other

ones.

Rarefaction curves were computed in PAST v. 2.14

(Hammer et al. 2001) to analyze species diversity and

species richness of bees and wasps. The rarefaction algo-

rithm was based on the use of log Gamma function for

computing combinatorial terms as described by Krebs

(1989). To estimate the species richness, the Chao-1 esti-

mator was calculated (Colwell and Coddington 1994) using

the program available at http://www2.biology.ualberta.ca/

jbrzusto/rarefact.php [cited as 24 Feb 2012].

Basic diversity indices were calculated for each of the

datasets. These include the total number of species found,

the total number of individuals found, dominance

(expressed as 1—Simpson index, where 1 indicates com-

plete domination of the single species, and 0 indicates

equal representation of all the taxa), Shannon index

(reflecting entropy, ranging from 0 for communities with

only a single taxon to high values for communities with

many species, each with only few individuals), Buzas-

Gibson’s index (evenness measure), Brillouin’s index

(diversity index, which may be more appropriate when

assessing datasets obtained using Moericke traps since

these are selectively omitted by certain and yet poorly

specified groups of bees and wasps, Straka 2005), Menhi-

nick’s richness index (the ratio of the number of taxa to the

square root of sample size), Margalef’s species richness

index (having good discriminating ability, but sensitive to

sample size), equitability (evenness measure, where

Shannon diversity is divided by the logarithm of number of

taxa), Fisher’s alpha (diversity measure), and Berger-Par-

ker dominance index (number of individuals of the

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dominant species relativized to the total number of indi-

viduals) (Harper 1999). Approximate confidence intervals

were computed with a bootstrap procedure where 1,000

random samples were produced, each with the same total

number of individuals as in each original sample. To

compare the diversities, two methods were used. The first

one involved bootstrapping: The abundance data were

pooled, 1,000 random pairs of two independent samples

were then taken from this pool with the same number of

individuals as in the original two samples, and the diversity

indices were computed for each replicate pair. The number

of times when the random samples exceeded or equaled the

observed pairs indicated the probability that the observed

difference could have occurred by random sampling from

one parent population as indicated by the P value. In par-

allel, the permutation-based method was used, which

involved generation of 1,000 random matrices based on

two datasets, each with the same row and dataset totals as

in the original data matrix. The P value was computed as

for the bootstrap test above (Hammer et al. 2001). Identical

measures were applied when analyzing the microhabitats

present within the sandpits, and when analyzing the species

of conservation interest. All the above indexes were cal-

culated in PAST v. 2.14 (Hammer et al. 2001). Analyses

involving the information from the three control datasets

(urban landscape, sand dune, military training areas) did

not include Apis mellifera and Bombus spp. since these

species were omitted in some of the datasets used; how-

ever, these taxa were included in the analyses based on the

sandpit dataset alone.

The conservation status of the recorded species was

defined according to the Czech Red List of invertebrates

(Farkac et al. 2005). The species found were also categorized

according to their use of soil burrows or other cavities—three

categories were formed: (a) obligate soil burrowers (these

may include facultative burrowers and burrow adopters since

the biology of some species is only partially known, but

excludes species known to utilize at least partially other than

soil burrows), (b) parasites, and (c) others (e.g., cavity

adopters including shell cavity adopters, plant cavity spe-

cialists, species utilizing facultatively both the soil burrows

and plant cavities). Different ratios of these three groups

among the four datasets were tested by the v2 test. The species

found were also categorized according to their preferences for

the presence of bare sand patches as obligate specialists,

facultative specialists, and other specialists. The categoriza-

tion was performed according to Balthasar (1954), Westrich

(1989), Linsenmaier (1997), Blosch (2000), Wisniowski

(2009), and Macek et al. (2010).

Data from the sandpits were further divided according to

the microhabitat characteristics. Two control groups were

formed: the sites affected by already completed reclama-

tion efforts other than near-natural restoration and the sites

affected by yet incomplete reclamation efforts other than

near-natural restoration. All the remaining samples origi-

nated from the sandpits with active quarrying activities or

from the sandpits without active quarrying, but which were

not subject to any reclamation efforts. These sites were

arranged according to the presence of sand patches, vege-

tation cover, average time since the quarrying cessation at

the particular microhabitat (this variable is not related to

the quarrying activities in the whole sandpit), and the

quarrying intensity (distinguishing between sites with

active quarrying on a daily basis, sites with occasional

quarrying, and closed sandpits with at least 5 years since

the quarrying cessation.

Results

Macrohabitat level: Sandpits versus other habitats

We collected a total of 1258 individuals from 221 species

of bees and wasps, out of these were 1080 individuals (184

species) captured in Moericke traps and 178 individuals

(66 species) were obtained by sweeping. We used the

Chao-1 species richness estimator (corrected for unseen

species in the samples) to compare the species richness of

the sandpits’ dataset with the three other datasets of nearly

identical geographic origin. The Chao-1 estimator indi-

cated the presence of high species diversity in three out of

the four datasets, suggesting presence of 282 species in the

sandpits, as compared to 311 species in the random habi-

tats, 271 species at the sand dune, and 188 species in

military training areas (Table 1). Rarefaction of all the four

datasets indicated a high level of completeness of the

sandpit dataset (Fig. 2). In the battery of species diversity

and species richness indexes (Table 1), the sandpit com-

munity of bees and wasps was characterized by the low

value of its dominance index, suggesting equal species

abundance distribution. Similarly, the value of Shannon

and Brillouin’s diversity indexes was high (4.5 and 4.2,

respectively), reflecting high species diversity. Interest-

ingly, the community of bees and wasps in sandpits did not

have any highly dominant species as suggested by low

values of Berger-Parker index when compared to those

obtained by the analysis of any of the three control datasets

(Table 1). This corresponds to the absence of otherwise

dominant species such as Vespula germanica and Vespa

crabro (Fig. 3). The most abundant species in the sandpits

was Bembecinus tridens (7.7 % of all individuals col-

lected). Other abundant species with dominance over 2 %

were Trypoxylon minus, Lasioglossum morio, Lasioglos-

sum leucozonium, Diodontus minutus, Lasioglossum vil-

losulum and Tiphia femorata; these six species accounted

for 31.8 % of individuals collected. Most of these

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dominant species typically occur in aggregations (Bem-

becinus tridens, Trypoxylon minus, Diodontus minutus) or

use solitary nests with many individuals utilizing each of

the nests (Lasioglossum morio). Note that some of these

species were completely absent at the random habitats of

cultural landscape, and surprisingly also in the military

training areas (Fig. 3). Fifty-three species were represented

by only a single individual. The dominant families inclu-

ded Halictidae (51 species, 380 individuals), Crabronidae

(47 species, 363 individuals), Andrenidae (20 species, 100

individuals), Megachilidae (20 species, 48 individuals),

Chrysididae (17 species, 73 individuals), Colletidae (16 spe-

cies, 45 individuals) and Pompiliidae (15 species, 45

individuals).

Although all four studies were performed in a geo-

graphically similar area, a large number of species was

present in only one or few datasets (Fig. 4). Only 26 species

were detected in all four studies, whereas 153 species were

detected in two or three out of the four studies, and 221

species were present only in a single dataset. For example,

the most dominant taxon of the sandpit dataset, Bembecinus

tridens, was completely absent in a dataset originating from

random habitats of the cultural landscape and even in the

dataset from military training areas. Similarly, the most

dominant species of the other three datasets were absent

(Fig. 3). The observed differences raise the question on the

ecological traits of the generalists and specialists, and on

possible differences in their conservation status.

Macrohabitat level: conservation implications

and ecological traits

Segregation of the detected taxa according to their con-

servation status provided an unexpected result, showing

that the sandpits provide critical refuge for the species of

conservation interest (Fig. 5). At least 27 species (48 %)

recognized as endangered, critically endangered, extinct, or

recently discovered was shown to be present only in the

sandpit dataset, and absent in any of the other three data-

sets. Other five such species were present in the sandpits as

well as in the other datasets. These species combined

represent over 57 % of endangered, critically endangered,

extinct, or recently discovered species represented in all the

four datasets combined (Fig. 5c). In strong contrast, only

39 % of vulnerable species were represented in the sandpit

dataset, moreover only 11 % of these species were present

in sandpits but not in the other datasets (Fig. 5b). Similar

results were obtained on bees and wasps of the least con-

cern, in which case 53 % of the least concern species were

Table 1 Species richness and diversity indexes of sandpits, sand dune, military training areas and random habitats from the identical geographic

area

Sandpits Random habitats Sand dune Military training areas

Chao-1 ± SD 281.6 ± 16.7 311.0 ± 19.4 270.6 ± 34.4 187.8 ± 18.8

Dominance 0.023 0.057�, � 0.033�, � 0.036�, �

Shannon index 4.491 4.183�, � 4.019�, � 4.097�, �

Buzas-Gibson’s index 0.421 0.289�, � 0.392 0.493

Brillouin’s index 4.230 3.936 3.827 3.755

Menhinick’s index 6.243 6.315 4.274�, � 5.604

Margalef’s index 29.93 31.55 20.12�, � 19.64�

Equitability 0.839 0.771�, � 0.811�, � 0.853

Fisher’s alpha 76.26 79.81 43.35�, � 53.19�

Berger-Parker index 0.077 0.194�, � 0.115�, � 0.148�, �

n (species/individuals) 212/1,153 227/1,292 142/1,104 122/474

The significance of differences between the sandpit dataset and the other three datasets was tested by bootstrapping (� P \ 0.01), and permu-

tation (� P \ 0.01). Differences in Chao-1 estimator, Brillouin’s index and n were not evaluated)

200 400 600 800 1000 1200

Specimens

0

40

80

120

160

200

240

280

Tax

a (9

5% c

onfid

enc

e)

Random habitats

Sandpits

Sand dune

Military training areas

Fig. 2 Expected cumulative number of bee species as defined by

rarefaction curve and associated Chao-1 estimator. Data are shown for

this study (sandpits), as well as for the three control studies in other

types of habitats (random habitats, military training areas, and at the

sand dune) in the Czech Republic

J Insect Conserv

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represented in the sandpit dataset, but only 13 % were

present in sandpits but not in the other datasets (Fig. 5a).

All the 26 species present in all four datasets belonged to

the least concern species. All the species present in all but

one dataset belonged to the least concern or vulnerable

species (Fig. 5). Clearly, the sandpits provide habitats

absent in the surrounding cultural landscape, and even in

the partially similar habitats such as sand dunes and mili-

tary training areas. The list of the faunistically important

records from the sandpits is provided as the supplementary

material (Table S1, S2), the species diversity and species

richness indexes for endangered, critically endangered,

extinct, or recently discovered species are provided

(Table 2). Provided is also the full list of species found in

the sandpits and in the three control datasets (Table S3).

Since we have shown that the sandpits are capable to

attract numerous bees and wasps of conservation interest,

next we attempted to elucidate what groups are the most

affected by the presence or absence of bare sand patches

and early vegetation succession stages characteristic for the

sandpits. In sandpits, the majority of individuals were the

soil burrow specialists (67 % of individuals, 55 % of spe-

cies), followed by the others (18 % of individuals, 24 % of

species) and by the parasites (16 % of individuals, 22 % of

species). Higher share of soil burrow specialists was

recorded only at the sand dune. Contrary to that, the soil

A

Species

Dom

inan

ce [%

]

0

2

4

6

8

10

12

14

Bem

beci

nus

trid

ens

Try

poxy

lon

min

usLa

siog

loss

um m

orio

Lasi

oglo

ssum

leuc

ozon

ium

Dio

dont

us m

inut

usLa

siog

loss

um v

illos

ulum

Tip

hia

fem

orat

aH

alic

tus

sexc

inct

usLa

siog

loss

um m

alac

huru

mLa

siog

loss

um lu

cidu

lum

And

rena

vag

aLa

siog

loss

um p

olitu

mH

alic

tus

tum

ulor

umLa

siog

loss

um p

auxi

llum

Hed

ychr

um r

utila

ns

B

Species

Dom

inan

ce [%

]

0

5

10

15

20

25SandpitsRandom habitatsSand duneMilitary training areas

Ves

pula

ger

man

ica

Ves

pa c

rabr

oH

alic

tus

rubi

cund

usLa

siog

loss

um fu

lvic

orne

Lasi

oglo

ssum

mor

ioT

rypo

xylo

n fig

ulus

Col

lete

s da

vies

anus

Sph

ecod

es h

yalin

atus

Lasi

oglo

ssum

pau

xillu

mA

ndre

na m

inut

ula

Sph

ecod

es m

onili

corn

isH

ylae

us n

igrit

usLa

siog

loss

um c

alce

atum

Sph

ecod

es e

phip

pius

Sph

ecod

es g

ibbu

s

C

Species

Dom

inan

ce [%

]

0

2

4

6

8

10

12

14

Lasi

oglo

ssum

luci

dulu

mM

ellin

us a

rven

sis

Hal

ictu

s se

xcin

ctus

And

rena

flav

ipes

Col

lete

s cu

nicu

lariu

sB

embe

cinu

s tr

iden

sLa

siog

loss

um s

abul

osum

And

rena

min

utul

aA

ndre

na v

aga

Hal

ictu

s su

baur

atus

Ves

pa c

rabr

oA

ndre

na c

iner

aria

Sm

icro

myr

me

rufip

esA

ndre

na a

rgen

tata

Am

mop

hila

sab

ulos

a

D

Species

Dom

inan

ce [%

]

0

5

10

15

20

Ves

pula

ger

man

ica

Lasi

oglo

ssum

pau

xillu

mH

alic

tus

tum

ulor

umH

alic

tus

leuc

ahen

eus

Sph

ecod

es e

phip

pius

Am

mop

hila

cam

pest

risA

ndre

na p

roxi

ma

And

rena

flav

ipes

And

rena

ova

tula

Am

mop

hila

hey

deni

Pol

iste

s ni

mph

aP

odal

onia

hirs

uta

Lasi

oglo

ssum

leuc

ozon

ium

Hal

ictu

s si

mpl

exA

ndre

na h

elvo

la

Fig. 3 Overview of dominant species of bees and wasps determined

by this study (sandpits), and by the three control studies in other types

of habitats (random habitats, military training areas, and at the sand

dune) in the Czech Republic. The dominant species are listed for each

of the studies: a sandpits, b random habitats, c sand dune and

d military training areas, and compared with the status of each

respective species in each of the complementing studies

J Insect Conserv

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burrow specialists were less represented in the dataset from

random habitats of the cultural landscape (Table 3). Dif-

ferences between the sandpit dataset and all the three other

datasets were significant both at the level of individuals and

species (v2 test P \ 0.001 in each case, df = 2). Venn

diagram summarizing the differences and identities (Fig.

S1) did not suggest any major site-specific exclusion or

aggregation of species based on the above criterion.

When the species were divided according to their pref-

erences for the presence of bare sand patches (obligate

specialists, facultative specialists and species with other

preferences), the sandpits were shown to host mostly the

obligate bare sand specialists (45 % of individuals, 34 % of

species) and facultative bare sand specialists (47 %

of individuals, 50 % of species), whereas the number of

species with other preferences was low (8 % of individuals,

16 % of species). A higher share of bare sand specialists

was recorded only at the sand dune. Contrary to that, the

bare sand specialists were less represented in the dataset

from random habitats of the cultural landscape and from

the military training areas (Table 4). Differences between

the sandpit dataset and all the three other datasets were

significant both at the level of individuals and species

(v2 test P \ 0.001 in each case, df = 2). Venn diagram

summarizing the differences and identities (Fig. 6) sug-

gested the high number of obligate specialists shared by the

datasets from sandpits and from the sand dune (20 species)

in parallel with the presence of other 20 species that were

found exclusively at the sand dune (Fig. 6).

Microhabitat level: what are the critical variables

attracting bees and wasps into sandpits?

The species richness was significantly higher at sandpits

unaffected by reclamation when compared to the control

areas composed of the sandpits where the reclamation was

underway, and to the control areas composed of completely

reclaimed sandpits (Table 5). Interestingly, the areas

unaffected by reclamation hosted not only the larger total

number of individuals, and had a higher total diversity but

they also hosted a larger number of rare species; those

recognized as endangered, critically endangered, newly

emerging or locally extinct were present only in the dataset

from sandpits unaffected by reclamation (Table 5). Species

of the family Vespidae were absent in the reclaimed

sandpits and in sandpits under reclamation. Similarly,

species of the family Colletidae were completely absent in

the reclaimed sandpits. A low number of species of the

family Crabronidae was also recorded at these sites (the

proportional share of the total individuals recorded: 5.4 %

at the reclaimed sites, 22.0 % at sites under reclamation,

88 28

73 34 16 8 32

22 10

26

29 3 13 18

12

SANDPITS(Czech Republic)

1153 ex., 212 species

RANDOM HABITATS(vicinity of Blatná)

1292 ex., 227 species

SAND DUNE(Veská)

1104 ex., 142 species Czech MILITARY TRAINING AREAS

474 ex., 122 species

Fig. 4 Venn diagram showing overlap of the total datasets obtained

by this study (sandpits), and by the three control studies in other types

of habitats (random habitats, military training areas and at the sand

dune) in the Czech Republic

A

B

C

Fig. 5 Venn diagram showing overlap of the a least concern (LC)

species, b vulnerable (VU) species, and c rare species (EN—

endangered, CR—critically endangered, EX—regionally extinct,

NE—newly emerging) of the bees and wasps detected at four types

of the habitats (sandpits, random habitats, military training areas and

at the sand dune) in the Czech Republic

J Insect Conserv

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and 34 % at sites unaffected by reclamation). The pro-

portional share of Halictidae was similar across all the

three datasets, the share of Chrysididae even increased.

Among the species with over 10 recorded individuals, the

following were absent at both the reclaimed sites and at

those under reclamation: Andrena humilis, Andrena nig-

roaenea, Nysson distinguendus, Alysson spinosus, Andrena

barbilabris, Dinetus pictus, Miscophus ater, Hedychrum

rutilans, Halictus tumulorum, and Diodontus minutus.

At unreclaimed sites, the species richness and abundance

changed significantly depending on the presence of bare sand

patches (Table 6). The lowest species richness and abundance

was reached at sites with absent or nearly absent bare sand

patches, the highest species richness and abundance was

reached at sites with nearly the highest share of bare sand

patches (Table 6). No specific trends for individual families

were observed, only Halictidae seemed to prefer medium share

of bare sand patches, whereas Megachilidae and Vespidae

were absent at sites without any sand patches. Among the

species with over ten recorded individuals, the following

species preferred the sites with a large amount of available bare

sand patches: Halictus subauratus, Nysson distinguendus, A-

lysson spinosus, Andrena barbilabris, Halictus simplex, Din-

etus pictus, Hedychrum rutilans, Lasioglossum pauxilum,

Lasioglossum politum, Tiphia femorata, Diodontus minutus

and Bembecinus tridens. Contrary to that, Lasioglossum morio,

Lasioglossum leucozonium, Hedychrum gerstaeckeri and He-

dychrum niemelai were distributed across the whole gradient

of sites irrespectively on the presence or absence of bare sand

patches.

At unreclaimed sites, the species richness and abun-

dance changed significantly depending on changes in

vegetation cover (Table 7). Both the extremes (0 or 100 %

vegetation cover) values were avoided by the bees and

wasps; this was especially prominent when focusing on

the rare species recognized as critically endangered, newly

emerging or locally extinct. The differences in the

abundance of bees and wasps were over one order of

magnitude in some cases (Table 7). Species of the families

Table 2 Species richness and diversity indexes of rare bees and wasps (those recognized as endangered, critically endangered, extinct by Farkac

et al. (2005), or recently discovered) in sandpits, sand dune, military training areas and random habitats from the identical geographic area

Sandpits Random habitats Sand dune Military training areas

Chao-1 ± SD 48.1 ± 8.3 14.3 ± 5.9 16.2 ± 4.0 N/D

Dominance 0.064 0.153 0.156�, � 0.291�, �

Shannon index 3.130 1.979 2.119�, � 1.697�, �

Buzas-Gibson’s index 0.715 0.905 0.693 0.546

Brillouin’s index 2.601 1.401 1.768 1.347

Menhinick’s index 3.881 2.309 1.922�, � 1.890�, �

Margalef’s index 7.347 2.817 3.003�, � 2.701�

Equitability 0.903 0.952 0.853 0.737�, �

Fisher’s alpha 23.59 10.49 5.922 5.565

Berger-Parker index 0.162 0.250 0.282� 0.500�, �

n (species/individuals) 32/68 8/12 12/39 10/28

Significance of differences between the sandpit dataset and the other three datasets was tested by bootstrapping (� P \ 0.01), and permutation (�

P \ 0.01). Differences in Chao-1 estimator, Brillouin’s index and n were not evaluated). Chao-1 estimator for the military training areas was not

calculated since there were no doubletons

Table 3 Stratification of bees and wasps of the four Czech datasets

according to their nesting strategy

Sandpits Random

habitats

Sand

dune

Military

training areas

Soil burrow

specialists

772/116 419/88 873/90 294/69

Parasites 179/46 221/50 156/31 46/18

Others 202/50 652/89 75/21 134/35

Shown are the total number of individuals/number of species

Table 4 Stratification of bees and wasps of the four Czech datasets according to their preferences for bare sand patches

Sandpits Random habitats Sand dune Military training areas

Bare sand obligate specialists 521/73 126/32 755/59 80/21

Bare sand facultative specialists 543/106 606/132 275/64 266/69

Preferring other habitats 89/33 560/63 74/19 128/32

Shown are the total number of individuals/number of species

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Megachilidae and Vespidae were completely absent at both

extreme values of vegetation cover, families Colletidae and

Pompilidae were absent at sites with high vegetation cover.

Among the species with over 10 recorded individuals, the

following species were completely absent at both extreme

values of vegetation cover: Scolia sexmaculata, Nysson

distinguendus, Alysson spinosus, Andrena barbilabris,

Halictus simplex, Miscophus ater, Lasioglossum politum,

Halictus sexcinctus, Tiphia femorata; over 98 % of Bem-

becinus tridens individuals were also found outside of

habitat patches with extreme values of the vegetation

cover. No species preferred patches with[90 % vegetation

cover. There were also no species restricted to the micro-

habitats with 0 % vegetation cover. However, Andrena

barbilabris was present only at sites with 1–30 % vegeta-

tion cover. Numerous other species were also found only at

sites with low vegetation cover, however, the low total

number of captures of these species does not allow to

provide any definitive answer on their preferences.

At unreclaimed sites, the species richness and abun-

dance changed significantly depending on the time since

quarrying cessation at the particular microhabitat

(Table 8). The very early succession stages, within first

12 months following the quarrying cessation, were occu-

pied mainly by the families Andrenidae and Halictidae. In

particular, Andrena spp. and their parasites were recog-

nized as the pioneer species. With increasing time since

quarrying cessation, both the species diversity and abun-

dance increased during the first decade following quarrying

cessation. At the later stages, the diversity began to

decrease and the rare species were no longer present.

Interestingly, this phenomenon was not associated with any

significant increase in dominance (Table 8). Most bee and

wasp families preferred the period within 6–10 years fol-

lowing the quarrying cessation, only the family Apidae was

associated more strongly with the second year following

the quarrying cessation. Among the species with more than

ten recorded individuals, 90 % of the Bembecinus tridens

individuals were collected at the microhabitats within three

to 10 years following the quarrying cessation. These sites

were also preferred by Diodontus minutus, Lasioglossum

villossulum, and Nysson distinguendus. Early stages

(0–2 years following the quarrying cessation at the par-

ticular microhabitat) were preferred by Andrena barbila-

bris. Late stages ([10 years following the quarrying

cessation at the particular microhabitat) were preferred by

Lasioglossum morio.

Species richness and abundance changed significantly in

response to the level of quarrying activities in the whole

sandpit (macrohabitat level) and the time since cessation of

quarrying activities at the particular habitat patch (micro-

habitat level) at unreclaimed sites (Table 9). The lowest

species diversity was recorded in sandpits where the

quarrying activities were ceased over 5 years ago, the total

abundance of bees and wasps was comparable at all the

three types of macrohabitats (sandpits with quarrying on

daily bases, those with only occasional quarrying, and

those where the quarrying was ceased over 5 years ago).

However, the intensity of quarrying was positively corre-

lated with the level of Berger-Parker index and with the

dominance index, which reflects more intense disturbations

associated with the intensively quarried sites. All the three

types of macrohabitats hosted taxa of conservation interest,

although there were certain species-specific differences.

Species of the family Apidae were twice more frequent at

sites with quarrying at daily basis when compared to both

other datasets. Families Chrysididae and Colletidae were

over twice more frequently found in sandpits with quar-

rying activities ceased for more than 5 years. Family

Megachilidae was almost completely absent in sandpits

with quarrying activity at daily basis. Among the species

with over 10 recorded individuals, there were not any

A

B

C

Fig. 6 Venn diagram showing overlap of the a obligate bare sand

specialists, b facultative bare sand specialists, and c species with other

nesting strategies among the bees and wasps detected at four types of

the habitats (sandpits, random habitats, military training areas and at

the sand dune) in the Czech Republic

J Insect Conserv

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individuals of Bembecinus tridens, Halictus subauratus,

Halictus maculatus, and Andrena nigroaenea recorded in

sandpits with quarrying activities ceased for more than

5 years. Tiphia femorata, Hedychrum rutilans, and

Hedychrum gerstaeckeri were absent at sites with only

occasional quarrying. Miscophus ater, and Alysson spino-

sus were absent in sandpits with quarrying at daily basis.

Andrena barbilabris was recorded only in sandpits with

active quarrying on daily basis. Nysson distinguendus, and

Andrena humilis were present only in sandpits with occa-

sional quarrying. Within both, sites with occasional or

intensive quarrying, the species of the family Andrenidae

and Apidae preferred early succession stages (microhabi-

tats formed by quarrying 0–2 years ago), whereas the

family Crabronidae preferred microhabitats formed by

quarrying over 2 years ago.

Typically, Tiphia femorata, Lasioglossum politum,

Lasioglossum pauxillum, Miscophus ater, Alysson spino-

sus, Nysson distinguendus (100 % of individuals each),

Bembecinus tridens (94 % of individuals), and Dinetus

pictus (92 % of individuals) were detected as markers of

microhabitats formed by quarrying over 2 years ago (but in

parallel, many of these species were present specifically in

active quarries). Only Andrena barbilabris was among the

species with over ten recorded individuals found exclu-

sively at microhabitats formed by quarrying 0–2 years ago.

Discussion

The 221 bee and wasp species captured in sandpits during

the study comprised 16.5 % of the 1,343 species reported

from the Czech Republic by Bogusch et al. (2007). The

species richness was higher than those recorded in studies

of other disturbed sites (Czech military training areas,

Bogusch 2010) and higher than those of the naturally

occurring sand patches (sand dune, Bogusch 2008). Of note

is that the compared datasets differed in the number of sites

covered and in details of the sampling design, however the

number of sampled specimens was similar and the rare-

faction analysis (Fig. 2) provided the evidence that three of

the four datasets had very similar coverage of the species

present, while only one dataset (Czech military training

areas) was less complete. These data indicate that a sandpit

can be recognized as an important habitat for a diverse bee

and wasp fauna. There were no highly dominant species

(Berger-Parker index = 0.077, Table 1), completely absent

were the otherwise dominant species such as Vespula

germanica and Vespa crabro. The absence of any highly

dominant species probably reflects the surplus of nesting

habitats in the presence of only limited and highly diver-

sified food sources. In particular, the absence of Vespula

germanica and Vespa crabro is probably resulting from the

absence of appropriate nesting habitats (large cavities), and

Table 5 Number of least concern (LC), vulnerable (VU), endangered

(EN), critically endangered (CR), newly emerging (NE) and region-

ally extinct (EX) individuals per 10 traps, total number of individuals

per total number of traps, and species richness and diversity indexes

for sandpits unaffected by reclamation, reclaimed sandpits with yet

incomplete reclamation, and reclaimed sandpits with completed

reclamation

Sandpits unaffected by

reclamation

Reclaimed sandpits—yet

incomplete reclamation

Reclaimed sandpits—completed

reclamation

n LC individuals per 10 traps 18.0 12.0 9.8

n VU individuals per 10 traps 3.6 1.4 1.0

n EN individuals per 10 traps 0.5 – –

n CR individuals per 10 traps 0.6 – –

n NE individuals per 10 traps 0.1 – –

n EX individuals per 10 traps \0.1 – –

n (individuals/traps) 980/427 57/43 45/42

Chao-1 ± SD 254.2 ± 19.1 45.1 ± 8.8 64.8 ± 16.7

Dominance 0.028 0.053 0.093�, �

Shannon index 4.291 3.156 2.959�

Buzas-Gibson’s index 0.410 0.810 0.689

Brillouin’s index 4.033 2.587 2.333

Menhinick’s index 5.692 3.841� 4.174�

Margalef’s index 25.71 6.925� 7.093�

Equitability 0.828 0.937 0.888

Fisher’s alpha 63.7 23.63� 31.67

Berger-Parker index 0.0838 0.123 0.267�, �

Significance of differences between the sandpits unaffected by reclamation and the other two datasets was tested by bootstrapping (� P \ 0.01),

and permutation (� P \ 0.01). Differences in Chao-1 estimator, Brillouin’s index and n were not evaluated

J Insect Conserv

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Table 6 Number of least concern (LC), vulnerable (VU), endangered

(EN), critically endangered (CR), newly emerging (NE) and region-

ally extinct (EX) individuals per ten traps, total number of individuals

per total number of traps, and species richness and diversity indexes

for microhabitats examined in sandpits unaffected by reclamation,

stratified according to the relative share of bare sand patches at each

particular microhabitat

Bare sand [%] 0–10 11–30 31–50 51–70 71–90 91–100 %

n LC individuals per 10 traps 9.2 15.0 13.0 17.0 36.0 17.0

n VU individuals per 10 traps 0.4 0.3 2.4 0.4 4.7 5.5

n EN individuals per 10 traps 0.4 – – – 1.0 0.6

n CR individuals per 10 traps – 0.1 – 1.3 1.0 0.8

n NE individuals per 10 traps – 0.3 – 0.4 0.2 –

n EX individuals per 10 traps – – 0.2 – – –

n (individuals/traps) 24/24 109/70 76/49 43/23 254/60 472/201

Chao-1 ± SD N/D 84.1 ± 16.3 54.0 ± 9.0 32.0 ± 5.0 151.4 ± 18.8 155.2 ± 15.2

Dominance 0.087 0.055�, � 0.044 0.059 0.034 0.045�, �

Shannon index 2.705 3.371�, � 3.351 3.015 3.968 3.852�, �

Buzas-Gibson’s index 0.831 0.647 0.793 0.850 0.588 0.440

Brillouin’s index 2.009 2.887 2.804 2.413 3.529 3.546

Menhinick’s index 3.674� 4.310� 4.129�, � 3.660� 5.647 4.925

Margalef’s index 5.349� 9.379�, � 8.082�, � 6.115� 16.07� 17.22�, �

Equitability 0.936 0.886 0.935 0.949 0.882 0.824

Fisher’s alpha 32.72 28.69�, � 26.75�, � 22.40 49.74� 43.15�, �

Berger-Parker index 0.208 0.138 0.105 0.140 0.122 0.148�, �

Significance of differences between the total dataset from sandpits unaffected by reclamation and the particular categories was tested by

bootstrapping (� P \ 0.01), and permutation (� P \ 0.01). Differences in Chao-1 estimator, Brillouin’s index and n were not evaluated. Chao-1

estimator for the areas with 0–10 % of bare sand was not calculated since there were no doubletons

Table 7 Number of least concern (LC), vulnerable (VU), endangered

(EN), critically endangered (CR), newly emerging (NE) and region-

ally extinct (EX) individuals per ten traps, total number of individuals

per total number of traps, and species richness and diversity indexes

for microhabitats examined in sandpits unaffected by reclamation,

stratified according to the vegetation cover at each particular

microhabitat

Vegetation cover [%] 0 1–9 10–30 31–60 61–90 91–100

n LC individuals per 10 traps 4.0 9.4 26.0 20.0 16.0 9.5

n VU individuals per 10 traps 0.3 2.6 5.1 7.2 1.3 0.5

n EN individuals per 10 traps – 0.2 1.0 0.3 0.2 0.5

n CR individuals per 10 traps – 0.4 1.2 0.5 0.3 –

n NE individuals per 10 traps – – 0.1 0.1 0.2 –

n EX individuals per 10 traps – – 0.1 – 0.1 –

n (individuals/traps) 13/30 68/54 484/144 206/74 186/103 23/22

Chao-1 ± SD 72.5 ± 37.7 83.0 ± 26.3 216.6 ± 26.4 136.5 ± 23.4 109.5 ± 14.3 N/D

Dominance 0.089 0.071�, � 0.036 0.052�, � 0.036 0.089

Shannon index 2.458 2.983�, � 4.033 3.61�, � 3.77 2.608

Buzas-Gibson’s index 0.974 0.681 0.466 0.544 0.629 0.848

Brillouin’s index 1.656 2.501 3.702 3.202 3.317 1.95

Menhinick’s index 3.328 3.517�, � 5.500 4.738 5.059 3.336�

Margalef’s index 4.289� 6.636�, � 19.41�, � 12.58�, � 13.01�, � 4.784�

Equitability 0.989 0.886 0.841 0.856 0.890 0.941

Fisher’s alpha 75.95 19.12�, � 51.78� 35.44�, � 39.71�, � 23.3

Berger-Parker index 0.154 0.162 0.116 0.175�, � 0.102 0.174

Significance of differences between the total dataset from sandpits unaffected by reclamation and the particular categories was tested by

bootstrapping (� P \ 0.01), and permutation (� P \ 0.01). Differences in Chao-1 estimator, Brillouin’s index and n were not evaluated. Chao-1

estimator for the areas with 91–100 % vegetation cover was not calculated since there were no doubletons

J Insect Conserv

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from the absence of any large-scale sources of organic

material supporting their large colonies. Although we have

included the list of dominant species (Fig. 3), the presence/

absence of individual species was highly variable in

response to the habitat characteristics such as the presence

of bare sand patches, the time elapsed since the particular

microhabitat was formed, or the frequency of quarrying

activities. For example, the most dominant species, Bem-

becinus tridens, was completely absent in sandpits where

quarrying was ceased over 5 years ago, and was very rare

at certain microhabitats. Some other dominant species,

such as Lasioglossum morio, were distributed across all the

sandpit microhabitats independently on the characteristics

recorded in this paper. This is consistent with the known

high abundance of L. morio through the wide range of

habitats in the Czech Republic, where this species repre-

sents one of the most common and numerous bee species,

known for its eusocial life strategy. Interestingly, the

comparison with three other datasets from the geographi-

cally similar area revealed that the sandpits serve as an

important refuge for numerous rare taxa absent in the

surrounding landscape (Fig. 5). Since only the generalists

were distributed across all the sandpit microhabitats, the

identification of more narrowly defined microhabitats

within the sandpits, which provide the crucial resources for

the species of conservation interest, was attempted.

Since this is the very first large-scale study on bees and

wasps of sandpits, there is only negligible amount of

comparative material. To our knowledge, there are only

two studies dealing with disused sandpits, besides them

there are only incidental records collected during the

monitoring of random habitats of certain areas. First of the

two above mentioned studies focused on two disused

North-German sandpits (Schluter 2002). Similarly to the

ours, the study found out that both the former sandpits host

several rare species. The study noted the high prevalence of

species nesting in soil among these two families (over

80 %), which is even more than in this study (55 %) and

the more of the Czech sand dune study (63 %, Bogusch

2008), and which probably reflects the extensive remode-

lation of vegetation due to the reclamation of the sandpit to

the gliding field, while some of the habitat opportunities for

burrowing species were retained. In sum, the study iden-

tified 96 bee and 45 wasp species (1,267 individuals were

sampled), which corresponds to 30 % of North-German

bee species and to 26 % of North-German wasp species.

The number of species found was lower than in our study,

which probably reflects a substantially lower number of

localites sampled, however, the coverage of the known

species was higher. The species spectrum was only par-

tially overlapping (Schluter 2002), reflecting the differ-

ences in the geographic range.

Table 8 Number of least concern (LC), vulnerable (VU), endangered

(EN), critically endangered (CR), newly emerging (NE) and region-

ally extinct (EX) individuals per ten traps, total number of individuals

per total number of traps, and species richness and diversity indexes

for microhabitats examined in sandpits unaffected by reclamation,

stratified according to the time passed since quarrying ceased at each

particular microhabitat

Time since quarrying cessation [years] \1 year 1 2 3–5 6–10 11–20 [20

n LC individuals per 10 traps 7.2 15.0 15.0 22.0 29.0 17.0 14.0

n VU individuals per 10 traps 2.6 1.0 1.9 12.0 6.0 2.2 0.7

n EN individuals per 10 traps 0.4 – 0.2 1.5 0.9 0.3 –

n CR individuals per 10 traps – – 0.3 0.5 1.5 0.2 1.1

n NE individuals per 10 traps – – – 0.2 0.2 0.1 0.2

n EX individuals per 10 traps – – – – 0.1 0.1 –

n (individuals/traps) 47/46 62/39 101/58 146/41 342/91 190/96 92/56

Chao-1 ± SD 64.1 ± 17.2 60.6 ± 13.4 90.3 ± 19.7 98.7 ± 16.5 191.6 ± 26.8 158.1 ± 28.2 81.6 ± 14.2

Dominance 0.062 0.077�, � 0.101�, � 0.081�, � 0.038 0.033 0.051

Shannon index 3.09 3.085� 3.103 3.328�, � 3.905� 3.858 3.454

Buzas-Gibson’s index 0.785 0.684 0.530 0.507 0.507 0.640 0.688

Brillouin’s index 2.467 2.527 2.633 2.886 3.539 3.386 2.896

Menhinick’s index 4.084� 4.064� 4.179�, � 4.552� 5.299 5.369 4.796

Margalef’s index 7.013� 7.511� 8.884�, � 10.84�, � 16.62�, � 13.91� 9.952�, �

Equitability 0.928 0.890 0.830 0.830 0.852 0.896 0.902

Fisher’s alpha 29.18 26.59� 29.98�, � 32.1�, � 45.93�, � 44.55 36.61�

Berger-Parker index 0.170 0.226�, � 0.287�, � 0.240�, � 0.111 0.079 0.141

Significance of differences between the total dataset from sandpits unaffected by reclamation and the particular categories was tested by

bootstrapping (� P \ 0.01), and permutation (� P \ 0.01). Differences in Chao-1 estimator, Brillouin’s index and n were not evaluated

J Insect Conserv

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The other publicly available datasource dealing with

bees and wasps in sandpits is the report by Dvorak and

Bogusch (2008). The authors investigated a single disused

sandpit in a mountain region on Czech-German borders,

recording 69 species of bees and wasps. Certainly, the high

altitude of this habitat (900 m a.s.l.) stands behind only

negligible overlap between the bee and wasp species

recorded by the authors when compared to our dataset of

50 Czech sandpits (located 165–520 m a.s.l.), only the

common eurytopic species were shared among these two

datasets. Similar conclusions were reached by Mocek et al.

(2009) who investigated the species composition of the

stone quarry Broumov—Rozmital (550 m a.s.l.), and

recorded the prevalence of hylophilous species over those

occupying the xerothermophilous ones. Most of the

endangered species found in sandpits were those previously

inhabiting sand dunes and sandy river beds. Both these

habitats were characteristic for the lowlands and interme-

diate altitudes, but rare or absent in the surrounding

mountain regions. Bees and wasps were clearly bound to

the open and semi-open habitats, and thus the man-made

open habitats serve as important refuges in the urban

landscape of lower altitudes and in the forested landscape

of intermediate and higher altitudes.

When focusing on the more detailed characterization of

habitats utilized by the bees and wasps in sandpits, it was

possible to notice a significant decrease of both abundance

and diversity in sandpits under reclamation and in com-

pletely reclaimed sandpits, which was even more promi-

nent when focusing on the rare species alone (Table 5).

This is in agreement with the previous observations on the

other groups of organisms (Pensa et al. 2004; Krauss et al.

2009; Tropek et al. 2010; Alday et al. 2011; Baasch et al.

2012; Tropek et al. 2012), and argues that the spontaneous

or assisted succession should be allowed at least at those

sites, which are unlikely to be returned to productive

agricultural or horticultural such as those at steep slopes or

at the ‘‘poor‘‘ quality soils, where the conflict with any

economic interests should be low and the nature conser-

vation benefits prevail.

Within the unreclaimed sandpits, there was a wide

range of habitats, each preferred by a different community

of bees and wasps. Active sandpits were found to be

crucial habitats for numerous species, which were asso-

ciated only with the actively quarried sandpits and were

absent in those, where the quarrying was ceased over

5 years ago (e.g., Bembecinus tridens, Halictus subaura-

tus, Halictus maculatus, and Andrena nigroaenea). Some

Table 9 Number of least concern (LC), vulnerable (VU), endangered

(EN), critically endangered (CR), newly emerging (NE) and region-

ally extinct (EX) individuals per ten traps, total number of individuals

per total number of traps, and species richness and diversity indexes

for microhabitats examined in sandpits unaffected by reclamation, in

which quarrying had ceased, was occasional or regular

Macrohabitat quarrying intensity Ceased Occasional Regular

Time since quarrying cessation at the

particular microhabitat

Total 0–2 [2 Total 0–2 [2 Total

n LC individuals per 10 traps 17.0 9.6 25.0 21.0 14.0 17.0 15.0

n VU individuals per 10 traps 1.4 1.0 3.3 2.7 2.4 13.0 6.3

n EN individuals per 10 traps 0.3 0.2 0.9 0.7 0.2 0.4 0.3

n CR individuals per 10 traps 1.1 – 0.7 0.5 0.2 0.6 0.3

n NE individuals per 10 traps 0.2 – 0.1 0.1 – 0.2 0.1

n EX individuals per 10 traps – – 0.1 0.1 – – –

n (individuals/traps) 192/97 54/50 413/135 467/185 156/93 165/52 321/145

Chao-1 ± SD 92.0 ± 8.5 60.6 ± 12.6 196.8 ± 24.4 202.1 ± 22.1 122.6 ± 25.6 76.0 ± 10.7 153.1 ± 21.8

Dominance 0.028 0.047 0.031 0.029 0.064�, � 0.144�, � 0.062�, �

Shannon index 3.914 3.307 4.071 4.145 3.378�, � 2.92�, � 3.585�, �

Buzas-Gibson’s index 0.706� 0.827 0.528 0.518 0.543 0.371 0.429�, �

Brillouin’s index 3.447 2.657 3.717 3.799 2.961 2.562 3.252

Menhinick’s index 5.124 4.491� 5.462 5.645 4.323� 3.892�, � 4.688

Margalef’s index 13.31�, � 8.022� 18.26�, � 19.69� 10.5�, � 9.597�, � 14.38�, �

Equitability 0.918� 0.946 0.864 0.863 0.847 0.747 0.809

Fisher’s alpha 40.74�, � 36.04 49.79� 53.7 29.26�, � 24.4�, � 37.02�, �

Berger-Parker index 0.0833 0.130 0.116 0.107 0.192�, � 0.352�, � 0.193�, �

Within sandpits with occasional and regular quarrying, information on patches, in which 0–2 and [ 2 year(s) had passed since quarrying ceased

at each particular microhabitat, is also provided. Significance of differences between the total dataset from sandpits unaffected by reclamation

and the particular categories was tested by bootstrapping (� P \ 0.01), and permutation (� P \ 0.01). Differences in Chao-1 estimator, Brill-

ouin’s index and n were not evaluated

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species were even more specific, requiring the presence of

large sand patches, which were provided only at the sites

with sand quarrying at daily basis (Miscophus ater and

Alysson spinosus). It resembles the situation within birds,

where certain birds occupy the whole range of active

sandpits but are mostly omitting those where the quarrying

was ceased several years ago (e.g., sand martins, Riparia

riparia; Heneberg 2012), while the other bird species

require higher critical patch size and occupy only those

post-industrial sites, which are large in size (e.g., hoopoe,

Upupa epops, or northern wheatear, Oenanthe oenanthe;

Caplat and Fonderflick 2009). Importantly, the rich bee

and wasp sandpit communities host a wide range of

associated insects, particularly from the orders Diptera,

Coleoptera, and Hymenoptera, some parasitic and others

commensal. Their populations tightly depend on the

dynamics of their host populations, as shown for the

satellite flies (Polidori et al. 2005), Meloe spp. oil beetles

(Fellendorf et al. 2004) and cuckoo wasps (Polidori et al.

2010b, c).

With most of the bee and wasp species found in sand-

pits, there was a clear conflict between the requirements for

the presence of bare sand patches (major nesting resource

for the majority of recorded species) and the presence of

the other resources (sufficient food sources, non-zero

vegetation cover, presence of the host species, etc.) since

the vast majority of recorded species preferred microhab-

itats where all these variables were present. As suggested

earlier by Potts et al. (2005) and Cruz-Sanchez et al. (2011)

for the burnt areas, the community structure and relative

abundances of bees and wasps was driven by the variation

in availability of suitable resources, highlighting the

availability of bare soil, the abundance of stemmed plants

and the presence of pre-existing cavities. Active sandpits

are important for those species, which build their nests

entirely or mostly in loose sand, e.g., Bembecinus tridens,

Alysson spinosus and Andrena barbilabris of the numerous

species, and certainly for many very rare species found

only in one or several specimens (e.g., genus Oxybelus).

Their typical habitats (sand dunes and loess banks) are

absent through the whole country and the active sandpits

remain as the only sites where these species are still cur-

rently present. Most of the other ground nesting species

also do not nest in overgrown substrate (all listed in pre-

vious paragraph), thus the presence of bare sand patches is

one of the necessary needs of these species. It is important

to note that the species richness prediction at any particu-

late man-made habitat requires the extensive knowledge of

numerous characteristics independent of the conditions in

the man-made habitat itself (presence of species-rich

localities in the vicinity, species composition and abun-

dance of flowering plants or the insect prey, etc.; cf. Lenda

et al. 2012).

Of note is the conflict of evidence-based conservation of

bees and wasps with the current Czech law [the situation is

to the large extent similar in most other countries, although

some (e.g., Germany) already allow certain share of

quarried ground for spontaneous succession]. We face this

issue for years when focusing at the biodiversity conser-

vation in sandpits and post-mining sites. According to the

Czech law, these sites have to be reclaimed by re-estab-

lishment the landscape corresponding to that before min-

ing. Such re-restablishment is secured by implementation

of a very powerful law banning any loss of the land used in

the past for agriculture and forestry (the only common

exception is the formation of new water bodies). This law

is rigorously enforced, causing destruction of any open

habitats for bees and wasps and other xerothermophilous

and psammophilous species. Of course, productivity of

agriculture or forestry at the reclaimed sites is mostly low,

sometimes none (Prach et al. 2011; Rehounkova et al.

2011). There is already an effort driven by scientists, non-

governmental organizations and even some quarrying

companies to allow other types of restoration at a part of

the affected ground since spontaneous or directed succes-

sion is both cheap and nature-friendly. However, any such

activities are so far blocked by the bulletproof argument

claiming that there is not enough scientific knowledge

about near-natural restoration (Rehounkova et al. 2011). So

far, the only exceptions are the quarries turned to protected

areas due to the presence of some flagship species such as

sand martins (Riparia riparia, Heneberg 2012) before the

reclamation started. Other than these, only illegal sandpits

and those with unknown or bankrupt owners or operators

have a chance to be subject to the long-term spontaneous

succession. Also the importance of actively quarried sites is

completely underestimated since the current mining law

requires opening the new mining sites for the shortest

possible time. In many cases, ephemeral existence of these

sites combined with very intense quarrying leads to the

absence of most xerothermophilous and psammophilous

species commonly found at sites with less intense and more

long-term-oriented quarrying (cf. the data here on the

diversity of early post-mining microhabitats and those

allowed to develop for more two or more years, Tables 8,

9). As proposed by Damigos and Kaliampakos (2003),

when assessing the quarrying, we should count in also the

provision of non-market goods such as habitat for some

endangered species. Provision of such non-market goods

should be reflected by the legislature related to both active

quarrying and post-quarrying reclamation activities.

In conclusion, the present work demonstrates that bees

and wasps have a very good ability to colonize the newly

emerging sand quarrying areas, and to survive in them

unless these are quarried as intensively as they would not

allow the development of any early successional vegetation

J Insect Conserv

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on the ground. The community structure changes with time

following formation of each respective microhabitat and

also in relation to the quarrying intensity in the whole

sandpit (macrohabitat). The sandpits were shown to be

important for the regional persistence of some species,

some of which were thought to be extinct in the Czech

landscape. We argue that the early succession stages

associated with sandpits (both active and closed) should be

recognized as potentially important refuges for xero-

thermophilous and psammophilous bee and wasp species.

These refuges are completely and irreversibly lost when

applying the current legislature enforcing the technical

reclamation over spontaneous or assisted succession at all

(e.g., Czech Republic) or most (e.g., Germany) post-mining

areas. Given that the nutrient-poor disturbance-dependent

habitats (mimicked by the sandpits) are among the habitats

most seriously affected by rapid loss of temperate biodi-

versity, the above documented conflict with the current

nature conservation legislature is puzzling.

Acknowledgments We thank Jakub Straka for the revision of

determination of selected species, Pavel Tyrner for sharing the liter-

ature, and Danuse Vymetalkova for language editing. This study was

supported in part by the Ministry of the Environment of the Czech

Republic, and by the Charles University in Prague project PRVOUK

P31/2012. We are grateful to the two reviewers of the first version of

the manuscript for their valuable comments.

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