ORIGINAL PAPER

The effect of traffic intensity on ground beetle (Coleoptera:Carabidae) assemblages in central Sweden

Claudia Melis Æ Camilla Bjerk Olsen Æ Maria Hyllvang ÆMauro Gobbi Æ Bard G. Stokke Æ Eivin Røskaft

Received: 13 May 2009 / Accepted: 18 August 2009

� Springer Science+Business Media B.V. 2009

Abstract Ground beetle assemblages were studied by

pitfall trapping during summer 2006 in the municipality of

Leksand (Sweden) along a gradient in traffic intensity (10

replicates in high and low traffic and five in no traffic) and

at progressive distances from the roadside (5, 15, 40 and

80 m). The ground beetles’ activity density was larger in

high- with respect to low-traffic areas. Rarefaction analysis

showed that richness did not differ between high and low

traffic, whereas it was higher in high and low compared to

no-traffic areas. Rarefaction analysis performed in high-

and low-traffic areas separately showed that species rich-

ness was higher at shorter distance from the road in both

treatments. Gradient analysis showed that traffic intensity

influenced carabid species composition, although the

proportion of explained variation was rather low. Mean

body length differed between the three treatments, where

ground beetles were larger in no-traffic areas. The pro-

portion of macropterous and diet-generalist beetles did not

differ amongst the three treatments. However, there was a

difference in the proportion of macropterous beetles in

low-traffic areas amongst sampling distances, and in the

proportion of diet-generalist beetles amongst sampling

distances at both high- and low-traffic areas. The propor-

tion of diet-generalist beetles decreased with increasing

distance from the road in both treatments. Our study sug-

gests that major roads have a significant effect on ground

beetles assemblages. However, many changes in assem-

blages and morpho-ecological adaptations followed the

gradient in traffic intensity, suggesting that also minor

roads affect ground beetle composition. Therefore, efforts

to improve habitat connectivity should also consider low-

traffic roads.

Keywords Body size � Carabidae � Diversity �Fragmentation � Gradient � Insects � Road management

Introduction

Roads can cause an increase in animal mortality both as a

consequence of their construction and because of collision

with vehicles; they can alter the physical and chemical envi-

ronment, affect animal behaviour and favour the spreading of

invasive alien species (Forman and Alexander 1998; Forman

2000; Trombulak and Frissell 2000). Habitat loss and frag-

mentation, which are associated with road building, are rec-

ognized as the most important causes of changes in the

distribution and abundance of organisms and as the main

threats to global biodiversity (Walker and Steffen 1997).

C. Melis (&) � C. B. Olsen � M. Hyllvang

Department of Biology, Centre for Conservation Biology,

Faculty of Natural Sciences and Technology, Norwegian

University of Science and Technology, Realfagbygget,

7491 Trondheim, Norway

e-mail: claudia.melis@bio.ntnu.no

C. B. Olsen

e-mail: camillao30@hotmail.com

M. Hyllvang

e-mail: maria_hyllvang@hotmail.com

M. Gobbi

Museo Tridentino di Scienze Naturali, Sezione di Zoologia degli

Invertebrati e di Idrobiologia, Via Calepina 14, 38122 Trento,

Italy

e-mail: gobbi.mauro@tiscali.it

B. G. Stokke � E. Røskaft

Centre of Advanced Study, Drammensveien 78,

0271 Oslo, Norway

e-mail: bard.stokke@bio.ntnu.no

E. Røskaft

e-mail: roskaft@bio.ntnu.no

123

J Insect Conserv

DOI 10.1007/s10841-009-9240-3

Roads are also linked to increased modification and use of

habitats by humans (Forman 2000; Trombulak and Frissell

2000).

Several studies have been conducted in intensively

modified landscapes to assess the ‘barrier effect’ of roads

on animals with large home ranges (see Trombulak and

Frissell 2000 for a review), but the impact of roads on

smaller and often less mobile organisms, such as many

invertebrate species, is less known and neglected.

Epigeic beetles, mainly ground beetles (Coleoptera:

Carabidae), are frequently used for landscape ecological

studies investigating environmental changes due to human

activities. Ground beetles have been advocated as a useful

indicator group for assessment of biodiversity and have

several advantages in monitoring the effect of human

activities on the land mosaics (e.g. Rainio and Niemela

2003). For example, they vary taxonomically (species

richness), morphologically (wing development and body

length) and ecologically (habitat requirement) in relation

to the intensity of anthropogenic activities (Lovei and

Sunderland 1996; Niemela and Kotze 2000; Rainio and

Niemela 2003).

Ground beetles are not often studied in roadside habitats

and research has been focusing mainly on their habitat

preferences (Vermeulen 1993). The strongest effects of the

highway on beetle assemblages were detected in a narrow

strip adjacent to the road (Bohac et al. 2004). Even narrow

(3–5 m) and unpaved forest roads favour open habitat and

habitat-generalist ground beetles, while forest species follow

the opposite trend (Koivula 2003; Bohac et al. 2004). Species

with better dispersal ability (e.g. species with functional

wings) and able to live in different habitats (i.e. generalist

species) are usually favoured in fragmented environments

(e.g. Halme and Niemela 1993). Roads also affect the pattern

of movement: ground beetles rarely cross paved roads and

tended to move parallel to the road edge, which might reduce

the probability of an individual to colonize a new fragment of

suitable habitat considerably (Mader et al. 1990; Bohac et al.

2004; Koivula and Vermeulen 2005). Several studies found

that large, short-winged and strictly predatory (diet-spe-

cialist) ground beetles are less frequently trapped in dis-

turbed habitats (e.g. van Huizen 1979; Den Boer et al. 1980;

Kotze and O’Hara 2003; Magura et al. 2006). Gobbi and

Fontaneto (2008) recently recommended considering these

closely related traits instead of focusing only on species

richness when monitoring the effect of human activities on

the environment.

The aim of this study was to compare ground beetles

assemblages along a gradient in traffic intensity and across

distances from the road in Sweden. More specifically,

starting from the hypothesis that traffic is a disturbance

factor for ground beetles, we tested the following predic-

tions: (1) ground beetles activity density (i.e. abundance as

measured by pitfall traps), species richness and assemblage

vary along a gradient of traffic intensity, where lower

activity density and lower species richness is found in more

disturbed habitats (i.e. higher traffic intensity, shorter dis-

tance from the road); (2) larger ground beetles are trapped

more often in patches not adjacent to roads and their pro-

portion decreases with increasing traffic intensity; (3)

macropterous and diet-generalist beetles are trapped more

often in patches adjacent to high-traffic roads and their

activity density decreases with increasing distance from the

road.

Methods

Study area and sampling design

Field work was carried out in the municipality of Leksand

(Sweden, 60�440 N, 15�000 E), between the 6th of June and

the 20th of July 2006. We established 25 sampling sites

spread in the whole municipality area (1,225 km2, Fig. 1),

which were selected for their similarity in vegetation

composition and structure (height and density), altitude and

slope. The sampling sites were situated in mixed coniferous

forest at an early stage of succession, dominated by bil-

berry Vaccinium myrtillus at the field layer and by bryo-

phytes at the ground layer. At all sampling sites trees had

been logged less than 7 years before sampling all the way

to the road, so abiotic factors linked to tree presence, such

as light, would not affect our results. The sampling sites

differed in traffic intensity: ten were adjacent to a high-

traffic road (ca. 11,540 cars/day), 10 to a low-traffic road

(ca. 400 cars/day) and five were far (at least 200 m) from a

low-traffic road (no traffic). From now on we will use the

term ‘‘high-, low- and no-traffic areas’’ referring to traffic

intensity. Traffic intensity was measured by counting the

cars that drove past each sampling site during 15 min. This

was performed several times at each road adjacent to each

transect (mean = 10.90 ± 2.55, n = 20) throughout the

sampling period, and at different hours of the day to cover

the total possible variability. The roads in the municipality

area were either paved with roadsides of ca. 10 m or were

forest roads with roadsides of ca. 5 m. Road verges of

paved roads in high-traffic sampling sites were also wider

because they were mown more often (Saarinen et al. 2005).

However, it is important to consider the quality of the data

and the range of confounding factors that can be present.

The presence of some clustered sampling sites is due to the

difficulty to find areas with the same habitat type, altitude

and slope, where traffic intensity is the only varying

parameter. In order to reduce pseudoreplication, we

established sampling locations which were at least 100 m

apart (Digweed et al. 1995).

J Insect Conserv

123

Carabid sampling

We collected carabids by pitfall traps, which is a com-

monly used trapping method for this family (Lovei and

Sunderland 1996). The traps were 250 ml plastic cups

(7 cm diameter, 9.5 cm depth) filled with ca. 50 ml of

70% ethylene glycol, with 12 9 12 cm plastic roofs held

up by a metal string to prevent dilution of the preserva-

tion liquid. At each sampling site we established a tran-

sect perpendicular to the road and one pitfall trap was

placed out along it at 5, 15, 40 and 80 m distance from

the roadside. The same relative distance between traps

was kept in no-traffic areas, so that we had ten replicates

in high- and low-traffic and five in no-traffic areas. We

emptied the traps six times at weekly intervals (6th of

June to 20th of July 2006) and merged the samples from

the same trap. All adult carabids were stored in vials

containing 70% ethanol and later dried, prepared, counted

and classified to species level with the help of Lindroth

(1961). Wing morphology and body length were deter-

mined for each species. Wing morphology was deter-

mined by observing the presence of functional wings

(metathoracic alae) and their relative length with respect

to the elitrae (Table 1). Species with wings longer than

the elitrae were considered macropterous and therefore

assumed to have good dispersal ability, whereas species

with wings shorter than the elitrae were considered bra-

chypterous and assumed to have low dispersal ability

(Brandmayr et al. 2005). The body length of each dried

individual was measured as the distance from the margin

of the labrum to the apex of the elitrae (Gobbi et al.

2007). We also classified the ground beetles into two

groups according to their feeding habits: generalists and

predators (Table 1). This was done with the help of the

literature available for each species (Lindroth 1985;

Holland 2002; Brandmayr et al. 2005).

Fig. 1 Location of the 25

sampling sites in Leksand

municipality (Sweden). The

cross-hatched areas represent

water. Shaded areas represent

human settlements. Star, no

traffic; circle, low traffic;

triangle, high traffic

J Insect Conserv

123

Table 1 Ground beetles trapped in plots adjacent to high- and low-traffic roads and in areas far from roads (40, 40 and 20 sampling units,

respectively) in Leksand municipality (Sweden) during summer 2006

Species Diet Wing High traffic Low traffic No traffic Total

5 m 15 m 40 m 80 m Total 5 m 15 m 40 m 80 m Total

Carabus violaceus p b 2 9 14 9 34 4 4 2 22 32 42 108

Pterostichus oblongopunctatus p m 2 9 17 18 46 2 10 5 6 23 38 107

Pterostichus niger p m 6 4 13 5 28 13 12 7 11 43 14 85

Epaphius secalis p b 10 5 3 12 30 7 8 5 6 26 28 84

Agonum fuliginosum p m 9 0 5 8 22 1 8 23 5 37 17 76

Pterostichus nigrita p m 3 3 3 9 18 3 3 8 2 16 4 38

Carabus glabratus p b 0 5 6 8 19 0 0 1 4 5 12 36

Pterostichus diligens p m 3 1 2 7 13 3 5 4 1 13 5 31

Calathus micropterus p b 4 7 2 3 16 2 0 0 4 6 7 29

Harpalus laevipes g m 1 1 4 4 10 1 2 1 2 6 8 24

Carabus arcensis p b 3 0 5 12 20 0 0 0 0 0 0 20

Pterostichus melanarius p b 3 3 9 5 20 0 0 0 0 0 0 20

Harpalus latus g m 7 0 2 0 9 1 3 0 1 5 4 18

Notiophilus germinyi p m 1 0 2 0 3 4 3 1 3 11 3 17

Patrobus assimilis p b 2 2 3 6 13 0 0 0 2 2 2 17

Metallina lampros p m 0 6 0 0 6 2 4 1 0 7 3 16

Epaphius rivularis p b 6 0 6 3 15 0 0 0 0 0 0 15

Notiophilus biguttatus p m 0 3 2 3 8 1 0 2 0 3 3 14

Carabus hortensis p b 2 3 2 2 9 0 1 0 0 1 3 13

Carabus nemoralis p b 4 2 1 2 9 0 0 0 0 0 0 9

Pterostichus strenuus p b 4 0 0 0 4 1 2 0 0 3 2 9

Cychrus caraboides p b 0 1 2 2 5 0 0 2 1 3 0 8

Trechus rubens p m 1 0 1 1 3 0 3 0 0 3 2 8

Leistus terminatus p m 2 1 1 2 6 0 0 0 0 0 0 6

Patrobus atrorufus p b 0 1 3 0 4 0 0 0 0 0 2 6

Bembidion quadrimaculatum p m 0 4 0 0 4 1 1 0 0 2 0 6

Pterostichus minor p m 2 0 1 0 3 0 2 0 0 2 0 5

Agonum sexpunctatum p m 0 0 0 0 0 0 5 0 0 5 0 5

Amara ovata g m 0 0 0 0 0 2 0 0 0 2 3 5

Dyschiriodes globosus p b 1 0 0 0 1 1 1 1 0 3 0 4

Poecilus cupreus g m 0 1 0 0 1 3 0 0 0 3 0 4

Pterostichus adstrictus p m 0 0 1 0 1 0 0 0 2 2 1 4

Amara communis g m 2 0 0 0 2 1 1 0 0 2 0 4

Amara aulica g m 4 0 0 0 4 0 0 0 0 0 0 4

Cicindela campestris p m 1 1 0 0 2 0 1 0 0 1 0 3

Dicheirotrichus placidus p m 0 0 0 1 1 1 0 1 0 2 0 3

Loricera pilicornis p m 1 0 0 1 2 0 0 0 0 0 0 2

Bembidion bruxellense p m 0 0 0 0 0 0 1 0 0 0 1 2

Synuchus vivalis g b 0 0 0 0 0 0 0 1 0 0 1 2

Badister bullatus p m 2 0 0 0 2 0 0 0 0 0 0 2

Anisodactylus binotatus g m 0 0 0 0 0 0 2 0 0 2 0 2

Carabus nitens p b 0 0 0 0 0 0 0 1 0 1 0 1

Asaphidion flavipes p m 0 0 0 0 0 0 0 1 0 1 0 1

Poecilus versicolor p m 1 0 0 0 1 0 0 0 0 0 0 1

Agonum ericeti p b 0 0 0 0 0 1 0 0 0 1 0 1

Amara lunicollis g m 0 0 0 0 0 0 1 0 0 1 0 1

J Insect Conserv

123

Ordination and statistic

We measured species richness as the cumulative number of

species found. The specimens activity density was com-

pared between high- and low-traffic areas by means of

v2 test. We did a rarefaction analysis by the software

Ecosim 7.72 (Gotelli and Entsminger 2004) to obtain an

index of species richness at each treatment and at different

distances from the road in high- and low-traffic areas. This

method estimates number of species trapped for random

subsamples out of a larger sample.

We used canonical correspondence analysis (CCA) (ter

Braak 1986, 1987) to determine the major pattern of var-

iation in species composition that is explained by variation

in traffic intensity. For the CCA, in order to improve

clarity, species represented by less than five individuals

were removed, so that the total number of species was 29.

One hundred sample units were used (40 traps in high

traffic, 40 in low traffic and 20 in no traffic). The species–

environment interaction was examined using the Vegan

library in R (version 1.13-2, Oksanen et al. 2008). Rare

species were down-weighted according to standard proce-

dure. All other settings were default. We chose a unimodal

response model, since the length of the first axis in a

detrended correspondence analysis (DCA) (Hill and Gauch

1980) of the total data was above 4 standard deviation

units, as recommended by ter Braak and Prentice (1988)

and ter Braak (1995). Monte Carlo permutation tests (ter

Braak 1992) were used to test for the significance of the

relationship between species distribution and environmen-

tal variables (999 permutations), both for the overall model

including the three treatments (high, low and no traffic) and

for each treatment separately.

We compared the mean body size in the three treat-

ments by ANOVA, and Tukey’s Honestly Significant dif-

ferences (HSD) post hoc tests were used to distinguish

differences between traffic intensities. We tested the rela-

tionship between ground beetle body length and number of

cars per hour by fitting a linear model to the data and by

including species as categorical explanatory variable. For

this purpose we retained only the 14 species which

were found at all traffic intensities in the dataset (n of

individuals = 482). Akaike Information Criterion corrected

(AICc) for small sample sizes was used to select the most

parsimonious model (Burnham and Anderson 2002). The

proportions of individuals with different wing morpholo-

gies and feeding habits were compared between areas and

among distances by means of v2 tests. All the statistical

tests were performed using R 2.7.1 (R Development Core

Team 2008).

Results

Carabid captures

We captured 877 ground beetles from 47 different species

(Table 1). Carabus violaceus and Pterostichus oblongo-

punctatus constituted about 25% of the capture. Nineteen

species represented 88% of the capture with 768 individ-

uals. Four species were found only in high-traffic areas:

C. arcensis, C. nemoralis, Epaphius rivularis and P. mel-

anarius, whilst P. niger and Notiophilus germinyi were

found mostly in low-traffic areas.

The total number of individuals trapped in high traffic

was significantly higher with respect to low-traffic areas

(v2 = 20.40, df = 3, P \ 0.001) and further away from the

road in high-traffic areas (v2 = 15.48, df = 1, P \ 0.01),

but there was no significant difference among distances in

low-traffic areas (v2 = 5.77, df = 3, P = 0.12). We could

not compare the total number of species trapped in no-

traffic areas with the other two treatments because of dif-

ferent trapping effort. However, the rarefaction analysis

(Fig. 2) showed that at the maximum sample size (i.e. the

number of ground beetles captured) that could be calcu-

lated for the three areas the treatments did not differ sig-

nificantly between high-traffic and low-traffic areas

(Fig. 2a). Nevertheless species richness was higher in high-

and low-traffic areas with respect to no-traffic areas

(Fig. 2a). The rarefaction analysis performed in high- and

low-traffic areas separately showed that species richness

differed amongst distances from the road in both treatments

(Fig. 2b, c). The curve representing the capture at 5 m from

the road in high-traffic areas (Fig. 2b) was different than

that in low-traffic areas (Fig. 2c): at 5 m in high-traffic

areas the number of species increased much faster with the

Table 1 continued

Species Diet Wing High traffic Low traffic No traffic Total

5 m 15 m 40 m 80 m Total 5 m 15 m 40 m 80 m Total

Dicheirotrichus cognatus p m 0 0 0 0 0 0 0 1 0 1 0 1

Total 89 72 110 123 394 55 83 68 72 277 205 877

Species richness 28 21 25 22 37 21 23 19 15 37 23 47

The species richness is reported for each treatment and distance from the road. g generalist, p predator, m macropterous, b brachipterous

J Insect Conserv

123

size of the capture. The accumulation curve for 15–80 m in

high-traffic areas was rather similar to the one in 5–15 m in

low-traffic areas.

Gradient in species composition

The total inertia of the CCA ordination was 6.06 (Table 2).

The sum of the canonical eigenvalues was 0.25, which

means that traffic intensity accounts for 4.10% of the vari-

ation in species assemblage. The CCA ordination showed

that traffic caused a shift in species composition. In Fig. 3,

the horizontal axis indicates a gradient in species compo-

sition from high- to low-traffic areas, while the vertical axis

indicates a gradient in species composition from low-traffic

to no-traffic areas. Permutation tests showed that the overall

model was highly significant (Pseudo-F = 2.07, P \ 0.01)

and all the explanatory variables contributed significantly to

the model except no traffic (Table 2). The CCA-plot

showed that species like C. arcensis, C. nemoralis,

P. melanarius, E. rivularis and Leistus terminatus were

associated to high-traffic areas, whereas species like Ago-

num sexpunctatum, P. niger, Notiophilus germinyi were

associated to low-traffic areas. Bembidion quadrimacula-

tum, Cychrus caraboides and P. minor were negatively

linked to no-traffic areas and positively linked both to high-

and low-traffic areas. C. violaceus was associated with no-

traffic areas but this association was not strong.

Body length, wing development and diet

Mean ground beetle body length differed significantly

between the three treatments (ANOVA, F2,479 = 9.56,

P \ 0.001, Fig. 4), the Tukey HSD post hoc test showed

0

5

10

15

20

25

30

Num

ber

of s

peci

es

0

5

10

15

20

25

30

Sample size

5 m

15 m

40 m

80 m

0

5

10

15

20

25

30

35

40(a)

(b)

(c)

1 10 30 50 70 90 110

1 10 30 50 70

1 10 30 50 100 150 250 350

High traffic

Low traffic

No traffic

5 m

15 m

40 m

80 m

Fig. 2 Rarefaction curves illustrating how species richness increases

with the number of ground beetles captured within each treatment (a)

and within each sampling distance in high (b) and low (c) traffic in

Leksand municipality (Sweden) during summer 2006. Each curve has

been constructed by performing 1,000-iteration simulation by

randomly sub-sampling a growing number of individuals within each

treatment and sampling distance

Table 2 Summary of the CCA analysis of 100 traps, 29 species

(activity density data) of ground beetles and three traffic intensities in

Leksand municipality (Sweden) during summer 2006

CCA total variance Constrained variance Percentage of

explained

variation

6.059 0.248 4.10

Axes CCA1 CCA2

Eigen values 0.174 0.074

Inter-set correlation of constraining variables with axes in CCA

High traffic 0.978 0.211

Low traffic 0.755 0.654

No traffic 0.327 0.946

Permutation test Pseudo-F P

High traffic 2.819 \0.001

Low traffic 2.169 \0.05

No traffic 1.388 ns

The permutation tests of significance of the constraining variables are

reported

J Insect Conserv

123

that mean body length was significantly higher in no-traffic

areas with respect to both high- (P \ 0.001) and low-traffic

areas (P \ 0.01), whereas there was no significant differ-

ence between low- and high-traffic areas. We also ran a

linear model to explain body length with species and

number of cars per hour (n cars). The full model was: body

length * species ? n cars ? species: n cars, however the

model selection on a set including all the combinations of

these variables showed that the most parsimonious model

included only the main effect of species and mean number

of cars (delta AICc between the first and the second ranked

model = 6.57, Akaike weight = 0.94). This model

explained 98.45% of the variation in ground beetles body

length, with number of cars per hour having a small but

significant negative effect (b = -0.0006, t value = -2.92,

P \ 0.01).

The proportion of macropterous ground beetles did not

differ between high-, low- and no-traffic areas when all the

sampling distances where pooled together (Fig. 5a,

v2 = 0.45, df = 2, P = 0.79) and at high traffic among

sampling distances (Fig. 5a, v2 = 0.59, df = 3, P = 0.90).

However, there was a significant difference in the propor-

tion of macropterous ground beetles at low-traffic areas

among sampling distances (v2 = 11.74, df = 3, P \0.001), where the proportion of macropterous beetles was

lower at 80 m of distance from the road.

The proportion of diet-generalist beetles did not change

between high-, low- and no-traffic areas when all the sam-

pling distances where pooled together (Fig. 5b, v2 = 0.09,

df = 2, P = 0.96). Nevertheless the proportion of diet-

generalist beetles decreased with increasing distance from

the road in both treatments (high traffic: v2 = 13.74,

-1.5 -1.0 -0.5 0.0 0.5 1.0 1.5

-1.5

-1.0

-0.5

0.0

0.5

1.0

1.5

Noti ger

Noti big

Cara arcLeis ter

Cara hor

Cara glaCara vio

Cych car

Patr ass

Patr atr

Epap sec

Trec rub

Metal lam

Bemb qua

Pter obl

Pter nigPter mel

Pter nir

Pter min

Pter str

Pter dil

Cala mic

gA on ful

Agon sex

Amar ova

Harp lat

Harp lae

Epap rivHigh

No

Low

CCA 1

CC

A 2

Cara nem

Fig. 3 Relationship between traffic intensities and the 29 most

frequently trapped ground beetle species in Leksand municipality

(Sweden) during summer 2006 as determined by canonical corre-

spondence analysis. Each level of the nominal variable traffic

intensity is shown by a vector. The length and direction of each

vector is proportional to the strength of the association between the

environmental variables within each plot and the CCA axes. The

ordination scores determining the location of the vectors are

proportional to the weighted average of species scores. Thus, species

showing strong affinity to one particular traffic intensity are located

far away from the origin in the direction indicated by the vector.

Species names are abbreviations (first four letters of genus- and first

three letters of species name) from the list of species in Table 1

highlowno

510

1520

25

Bod

y le

ngth

(m

m)

Traffic intensity

Fig. 4 Box plot of body length of ground beetles captured in Leksand

municipality (Sweden) during summer 2006 in high, low and no

traffic

0

5

10

15

20

25

30

5 15 40 80

0

10

20

30

40

50

60

70

80

90 highlowno

Rel

ativ

e ab

unda

nce

, %

(a)

(b)

Distance from the road

Mac

ropt

erou

s sp

ecie

sG

ener

alis

t spe

cies

Fig. 5 Percentage of a macropterous and b generalists ground beetles

captured in different traffic treatments and distances from the road in

Leksand municipality (Sweden) during summer 2006

J Insect Conserv

123

df = 3, P \ 0.001; and low traffic: v2 = 9.65, df = 3,

P \ 0.05) (Fig. 5b).

Discussion

The sampling period is not covering the whole period of

activity of ground beetles in our study area and some early

or late species might have been missed. However, Sapia

et al. (2006) showed that it is possible to sample ground

beetles for a shorter period than the whole season without

greatly altering the diversity profile of the assemblage. The

differences between the diversity profiles of the continuous

versus pulsating sampling method relied on rare species, as

direct consequence of reduced trapping effort. The effect

of roads on specimens’ activity and on species richness has

not yet been thoroughly disclosed. In some cases reported

in literature (cf. Bohac et al. 2004), larger number of

species was found at the greatest distance from the road

while the larger number of specimens was found at the

closest distance from the road. According to our first

prediction, we found that both capture size and species

richness varied with traffic intensity. Capture was signifi-

cantly higher in high-traffic with respect to low-traffic

areas. As reported by Haskell (2000) we found that the

number of individuals captured in high-traffic areas

increased with increasing distance from the road, while

there was no significant difference in the number of indi-

viduals trapped at different distances from the road in low-

traffic areas. Ground beetles are likely to experience a

higher risk of being killed by cars in high-traffic areas and

this might explain why the occur in lower number closer to

the road; however most of the trapped carabid species are

nocturnal and would be likely to cross the road when

traffic intensity is lower. The rarefaction analysis, which

allowed us also to include no-traffic areas in the compar-

ison, showed that species richness was highest in high-

traffic areas and at closer distance (5–15 m) from the road.

This might support the suggestion of Vermeulen (1993)

and Koivula (2005) that roadside verges can be used as

corridors for dispersal by ground beetle species associated

to open habitats. In fact high-traffic roads have also wider

verges than low-traffic ones (Saarinen et al. 2005) and in

high-traffic roads verges are flatter with respect to low-

traffic ones, which might favour dispersal. However,

Eversham and Telfer (1994) reinterpreted this fact by

suggesting that road verges could serve as refugia for

stenotopic species, which have a higher chance of breeding

successfully in such disturbed habitats than in unmanaged

areas. Gobbi and Fontaneto (2008) showed that the most

perturbed habitats have highest values of species richness

due to the colonization by opportunistic species adapted to

live in a wide range of habitats.

The proportion of explained variation was rather low,

and we did not found a very clear separation in ground

beetle species composition. The capture in areas with dif-

ferent traffic intensity seemed to reflect individual species

differences more than showing a real effect on the

assemblage. The capture in high traffic consisted of species

adapted to live both in open habitat and forest such as

C. arcensis, C. nemoralis, P. melanarius and forest species

such as E. rivularis and L. terminatus (Lindroth 1985;

Holland 2002). Species associated with open areas such as

B. quadrimaculatum and P. minor were positively associ-

ated with both high- and low-traffic areas (Andersen 2000),

but were found at closer distance from the road. C. viola-

ceous, which is an open forest species, was mainly asso-

ciated to no-traffic areas but it was found also in high- and

low-traffic areas, although it was also found more abundant

further from the road. This result is consistent with the

finding of Keller and Largiader (2003) that large roads

constitute a barrier for the genetic flow of this species.

A. ovata is a species associated to open habitats and human

disturbance; however it was not found in high-traffic areas,

but occurred at low numbers both in low- and no-traffic

areas.

According to our second and third prediction, morpho-

ecological traits (body length, diet preference and wing

morphology) varied with traffic intensity. According to our

second prediction, mean body length was significantly

higher in no-traffic areas than in the other two areas and the

variable number of cars per hour had a small but significant

negative effect on body length of ground beetle assem-

blages. This suggests that traffic may be a disturbing factor

since large ground beetles are less often trapped in dis-

turbed and especially urbanised habitats (e.g. Kotze and

O’Hara 2003; Magura et al. 2006). This disturbance might

include vibrations induced by the cars on the soil surface

which might be a disturbing factor during larval develop-

ment. Body size is correlated to several life history traits

such as dispersal ability and development time (Peters

1983), smaller ground beetle species have generally shorter

larval stages and this might be an advantage in unstable

environments (Lovei and Sunderland 1996). However, the

variation in mean body size might be due to several factors:

a decrease in the importance of small species, and increase

in medium size or large species or a combination of these

(Magura et al. 2006). Large ground beetle species, with

median length[15 mm, are more often captured by pitfall

traps (Andersen 1995), pitfall trapping might therefore

underestimate the effect of traffic on body length. Con-

sidering our third prediction, we did not find a clear gra-

dient in the activity density of macropterous beetles,

although their proportion differed among distances in low-

traffic areas. Instead, there was a clear pattern in the pro-

portion of diet-generalist beetles, which were more

J Insect Conserv

123

abundant in high-traffic areas and followed a gradient in

activity density from high- to low-traffic areas and with

increasing distance from the road. Diet-generalist species

can more easily colonize and use disturbed environments,

because they can, by definition, exploit a wider range of

food items. These food items include vegetable matter that

is more abundant in early stage succession habitats which

increase as consequence of mowing associated to roads

maintenance, especially in high-traffic roads (Saarinen

et al. 2005).

There are limitations that are intrinsic in this type of

study and we were not able to explain a great deal of

variation in carabid species composition. Nevertheless, our

results are consistent with the previous research on traffic

impact on ground beetles. Our findings indicate that major

roads have a significant impact on ground beetle assem-

blages. However, many changes in assemblages and mor-

pho-ecological adaptations occur along a gradient in traffic

intensity, suggesting that also minor roads also impact on

ground beetles. Therefore, given the strong decline in

Europe of the most specialized species (Kotze and O’Hara

2003) and the relationship between carabid beetles and

their predators (insectivorous mammals, birds, reptiles and

amphibian) efforts to improve habitat connectivity should

consider low-traffic roads as well as major roads.

Acknowledgments We are grateful to Oddvar Hanssen (NINA) for

helping with the identification of the specimens. We would like to

thank Asa Rydell from Leksand municipality and Uno Skog from

Dalarna County for giving us permission to conduct the fieldwork.

Lars Dahlkvist from Dalarna County kindly provided information

about time of logging of the sampling plots. We are grateful to Vera

Sandlund, Arne Moksnes, Sigrid Lindmo, Carolyn Baggerud, Anne

Lohrmann and the Natural History Museum of Trondheim for helping

us to find or lending us equipment. This study was funded by the

Norwegian University for Science and Technology (CM, CBO, MH)

and the Lise og Arnfinn Hejes scholarship (CBO, MH).

References

Andersen J (1995) A comparison of pitfall trapping and quadrat

sampling of Carabidae (Coleoptera) on river banks. Entomol

Fenn 6:65–75

Andersen J (2000) What is the origin of the Carabid beetle fauna of

dry, anthropogenic habitats in western Europe? J Biogeogr

27:795–806

Bohac J, Hanouskova I, Matejka K (2004) Effect of habitat

fragmentation due to traffic impact of different intensity on

epigeic beetle communities in cultural landscape of the Czech

Republic. Ekologia (Bratislava) 22:35–46

Brandmayr P, Zetto T, Pizzolotto R (2005) I Coleotteri Carabidi per la

valutazione ambientale e la conservazione della biodiversita.

Manuale operativo. APAT – Agenzia Nazionale per la protezi-

one dell’ambiente e per i servizi tecnici, Roma. Manuali e linee

guida, 34 (in Italian)

Burnham KP, Anderson DR (2002) Model selection and multi-model

inference: a practical information-theoretic approach. Springer-

Verlag, Berlin, 488 pp

Den Boer PJ, van Huizen THP, Den Boer-Daanje W, Aukema B, Den

Bieman CFM (1980) Wing polymorphism and dimorphism in

ground beetles as stages in an evolutionary process (Coleoptera:

Carabidae). Entomol Gen 6:107–134

Digweed SC, Currie CR, Carcamo HA, Spence JR (1995) Digging out

the ‘‘digging-in effect’’ of pitfall traps: influences of depletion

and disturbance on catches of ground beetles (Coleoptera:

Carabidae. Pedobiologia 39:561–576

Eversham BC, Telfer MC (1994) Conservation value of roadside

verges for stenotopic heathland Carabidae: corridors or refugia?

Biodivers Conserv 3:538–545

Forman RTT (2000) Estimate of the area affected ecologically by the

road system in the United States. Conserv Biol 14:31–35

Forman RTT, Alexander LE (1998) Roads and their major ecological

effects. Annu Rev Ecol Syst 29:207–231

Gobbi M, Fontaneto D (2008) Biodiversity of ground beetles

(Coleoptera: Carabidae) in different habitats of the Italian Po

lowland. Agric Ecosyst Environ 127:273–276

Gobbi M, Rossaro B, Vater A, De Bernardi F, Pelfini M, Brandmayr P

(2007) Environmental features influencing Carabid beetle (Cole-

optera) assemblages along a recently deglaciated area in the

Alpine region. Ecol Entomol 32:682–689

Gotelli NJ, Entsminger GL (2004) EcoSim: null models software for

ecology. Version 7. Acquired Intelligence Inc. & Kesey-Bear.

Jericho. http://garyentsminger.com/ecosim/index.htm

Halme E, Niemela J (1993) Carabid beetles in fragments of

coniferous forest. Ann Zool Fenn 30:17–30

Haskell DG (2000) Effects of forest roads on macroinvertebrates soil

fauna of southern Appalachian Mountains. Conserv Biol 14:

57–63

Hill MO, Gauch HG (1980) Detrended correspondence-analysis—an

improved ordination technique. Vegetatio 42:47–58

Holland JM (2002) The agroecology of Carabid beetles. Intercept,

Andover

Keller I, Largiader CR (2003) Recent habitat fragmentation caused by

major roads leads to reduction of gene flow and loss of genetic

variability in ground beetles. Proc R Soc Lond B 270:417–423

Koivula JM (2003) The forest road network—a landscape element

affecting the spatial distribution of boreal carabid beetles

(Coleoptera, Carabidae). In: Szyszko J et al (eds) How to protect

or what we know about Carabid beetles. Warsaw Agricultural

University Press, Warsaw, pp 287–299

Koivula JM (2005) Effects of forest roads on spatial distribution of

boreal carabid beetles (Coleoptera: Carabidae). Coleopt Bull

59:465–487

Koivula JM, Vermeulen HJW (2005) Highways and forest fragmen-

tation—effects on Carabid beetles (Coleoptera, Carabidae).

Landsc Ecol 20:911–926

Kotze DJ, O’Hara RB (2003) Species decline—but why? Explana-

tions of carabid beetle (Coleoptera, Carabidae) declines in

Europe. Oecologia 135:138–148

Lindroth CH (1961) Sandjagare och jordlopare: fam. Carabidae, 2nd

edn. Almqvist & Wiksell, Stockholm (In Swedish)

Lindroth CH (1985) The Carabidae (Coleoptera) of Fennoscandia and

Denmark. Fauna Entomol Scand 15:1–232

Lovei GL, Sunderland KD (1996) Ecology and behaviour of ground

beetles (Coleoptera, Carabidae). Annu Rev Entomol 41:231–256

Mader H-J, Schell C, Kornacker P (1990) Linear barriers to arthropod

movements in the landscape. Biol Conserv 54:209–222

Magura T, Tothmeresz B, Lovei GL (2006) Body size inequality of

carabids along an urbanisation gradient. Basic Appl Ecol 7:

472–482

Niemela J, Kotze DJ (2000) GLOBENET: the search for common

anthropogenic impacts on biodiversity using Carabids. In:

Brandmayr P et al (eds) Natural history and applied ecology of

Carabid beetles. Pensoft, Sofia-Moscow, pp 241–246

J Insect Conserv

123

Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Henry M,

Stevens H, Wagner H (2008) Vegan: community ecology package.

R package version 1.13-2. http://vegan.r-forge.r-project.org/

Peters RH (1983) The ecological implications of body size.

Cambridge University Press, Cambridge

R Development Core Team (2008) R: A language and environment

for statistical computing. R Foundation for Statistical Comput-

ing, Vienna

Rainio J, Niemela J (2003) Ground beetles (Coleoptera: Carabidae) as

bioindicators. Biodivers Conserv 12:487–506

Saarinen K, Valtonen A, Jantunen J, Saarnio S (2005) Butterflies and

diurnal moths along road verges: does road type affect diversity

and abundance? Biol Conserv 123:403–412

Sapia M, Lovei G, Elzek Z (2006) Effects of varying sampling effort

on the observed diversity of carabid assemblages in the

Danglobe Project, Denmark. Entomol Fenn 17:345–350

ter Braak CJF (1986) Canonical correspondence analysis: a new

eigenvector technique for multivariate direct gradient analysis.

Ecology 67:1167–1179

ter Braak CJF (1987) The analysis of vegetation-environment

relationships by canonical correspondence analysis. Vegetatio

69:67–77

ter Braak CJF (1992) Permutation versus bootstrap significance tests

in multiple regression and ANOVA. In: Jockel K-H, Rothe G,

Sendler W (eds) Bootstrapping and related techniques. Springer

Verlag, Berlin, pp 79–86

ter Braak CJF (1995) Ordination. In: Jongman RHG, ter Braak CJF,

van Tongeren OFR (eds) Data analysis in community and

landscape ecology (New ed.). Cambridge University Press,

Cambridge, pp 91–173

ter Braak CJF, Prentice IC (1988) A theory of gradient analysis. Adv

Ecol Res 18:271–317

Trombulak SC, Frissell CA (2000) Review of ecological effects of roads

on terrestrial and aquatic communities. Conserv Biol 14:18–30

van Huizen THP (1979) Individual and environmental factors

determining flight in Carabid beetles. Misc Pap Landbouwhog-

esch Wagening 18:199–211

Vermeulen R (1993) The composition of Carabid fauna on poor sandy

road-side verges in relation with comparable open areas.

Biodivers Conserv 2:331–350

Walker B, Steffen W (1997) An overview of the implications of

global change for natural and managed terrestrial ecosystems.

Conserv Ecol 1(2) (online). URL: http://www.consecol.org/

vol1/iss2/art2/

J Insect Conserv

123