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Environmental Biology – module II
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Roskilde University
Preamble ............................................................................................................................................................................ 5
Summary of project .......................................................................................................................................................... 6
Urbanisation and environment....................................................................................................................................... 9
Pollution......................................................................................................................................................................... 9
Fragmentation ............................................................................................................................................................... 9
Biota ................................................................................................................................................................................ 9
Arthropods in conservation .......................................................................................................................................... 10
Bioindicators................................................................................................................................................................ 10
Environmental indicators ...................................................................................................................................... 10
Ecological indicators............................................................................................................................................... 10
Biodiversity indicators ........................................................................................................................................... 10
Ground beetles as bioindicators................................................................................................................................ 11
Effects of urbanisation on ground beetle assemblages .............................................................................................. 13
GLOBENET.................................................................................................................................................................. 13
Species richness ....................................................................................................................................................... 13
Generalists versus specialist.................................................................................................................................. 13
Body size .................................................................................................................................................................. 13
Variations between countries ................................................................................................................................ 14
Factors influencing body size and condition .......................................................................................................... 14
Seasonal activity.......................................................................................................................................................... 16
Biology and ecology of three ground beetles.............................................................................................................. 17
Carabus nemoralis (Müller 1764)................................................................................................................................. 17
Nebria brevicollis (Fabricus 1792)................................................................................................................................ 17
Pterostichus melanarius (Illiger 1783) ......................................................................................................................... 18
Ground beetle (Coleoptera: Carabidae) condition along an urbanisation gradient .............................................. 20
Abstract ........................................................................................................................................................................ 20
Resumé ......................................................................................................................................................................... 20
Introduction ................................................................................................................................................................. 21
Study organism, location, materials and methods ................................................................................................. 22
Results .......................................................................................................................................................................... 24
Body size .................................................................................................................................................................. 25
Condition ................................................................................................................................................................. 29
Temporal change..................................................................................................................................................... 29
Discussion .................................................................................................................................................................... 31
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Environmental Biology – module II
Seasonal activity of three common Danish ground beetles (Coleoptera, Carabidae) along a rural-urban
gradient ............................................................................................................................................................................ 33
Abstract ........................................................................................................................................................................ 33
Resumé ......................................................................................................................................................................... 33
Introduction ................................................................................................................................................................. 34
Material and methods ................................................................................................................................................ 35
Study species ........................................................................................................................................................... 36
Seasonal Activity..................................................................................................................................................... 37
Comparison of Cardinal Dates.............................................................................................................................. 38
Results .......................................................................................................................................................................... 39
General Trends in Seasonal Activity .................................................................................................................... 39
Comparison of the cardinal dates of activity ...................................................................................................... 40
Comparison of activity in Urban vs. Suburban vs. Rural habitats................................................................... 46
Comparison of Cardinal dates .............................................................................................................................. 49
Discussion .................................................................................................................................................................... 50
Acknowledements ...................................................................................................................................................... 53
References ........................................................................................................................................................................ 54
Introduction ................................................................................................................................................................. 54
Condition article.......................................................................................................................................................... 58
Activity article ............................................................................................................................................................. 60
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Roskilde University
Preamble
Conducting fieldwork during springtime, combined with achieving insight into insect ecology and
environmental change in a terrestrial setting, were our primary motives upon initiation of this project. Soon
our focus narrowed to beetles and the utilisation of them as bioindicators in conjunction with environmental
management. We were advised to contact Gabor Lövei at Danmarks Jordbrugsforskning (Danish Institute of
Agricultural Sciences), which in turn led us to the study of ground beetles along urbanisation gradients of
which this report is the culmination. Gabor offered us an established experimental set-up, based on an
international project on ground beetles, called GLOBENET. This not only gave us many suitable references to
similar research, but also included comprehensive data based on previous studies conducted at the same
locality in Sorø.
We would sincerely like to thank Gabor for his inspiration and patient assistance.
The report contains (1) a general summary of our work, an introduction to environmental
effects of urbanisation emphasizing ground beetles (Coleoptera, Carabidae) in terms of biodiversity, condition
and activity. Additionally, we introduce the focal species, bioindication in general, and the GLOBENET
research network which targets investigation of ground beetles along urbanisation gradients. (2) A scientific
article addressing differences in ground beetle condition along an urbanisation, and (3) a scientific gradient
article summarizing our work and results on the seasonal activities of 3 ground beetles common to Denmark.
This structure allows us to present the work we conducted during the semester and elaborate
on the background of this highly interesting topic. We apologize for the unavoidable repetition of certain
parts the report form causes.
In the back of the report you will find a detailed reference list divided into the references
referring to the three parts of the project; introduction, condition article, activity article.
Andy Howe & Mattias Enggaard
July 2006
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Environmental Biology – module II
Summary of project
The GLOBENET program argues that a simple protocol can be applied globally to assess patterns of change
in biodiversity due to human impact. GLOBENET outlines an experimental set-up and recommends a
gradient which covers three disturbance regimes – rural, suburban and urban. At each of these locations 40
pitfall traps are employed resulting in a total of 120 traps. The procedure aims at distinguishing effects of
urbanisation, and in theory allows results to be compared between biomes, countries and continents. If a
general pattern is established, management strategies could be exported, which hopefully would enhance the
output of conservation efforts. Ground beetles are chosen as the indicator group, which makes it possible to
conduct international research on species richness and community composition. Changes in morphology
(wing development, body size) and ecology (feeding type, habitat preference) are also suggested measures
for evaluating effects of human impact.
In this report we give a resume of previous GLOBENET results. For further information:
Niemelä et al. (2000) and www.helsinki.fi/science/Globenet/.
In our project we investigated an urbanisation gradient around Sorø Lake (Fig. 1), which once
consisted of a continuous beech (Fagus sylvatica) forest. The park around Sorø Akademi along side the lake
formed the urban habitat. We assumed this area experienced the highest degree of disturbance due to
intensive management, human trampling and most built-up area. Two separated sites made up our suburban
habitat, and both were situated at the edge of larger forest areas bordered by houses and gardens. The rural
habitat was placed in homogenous beech forest with scattered patches of pine, and although it was under
forestry management, this habitat was assumed to experience the least human disturbance.
Sorø
R
SU
U
Lake
N
SU
Fig. 1. Sketch of the study area around Sorø Lake. R stands for rural and indicates our forest habitat, SU
denotes the suburban habitat and finally U indicates the Sorø Akademi Park, which formed our urban
habitat.
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We conducted fieldwork in April, May and June of 2006. This entailed setting-up, maintaining
and fortnightly emptying of 120 traps. In addition, we conducted a number of soil samples to determine soil
moisture and soil organic matter. Laboratory work consisted of sorting the catch into ground beetles and
beetle prey (all other arthropods and annelids), and thereafter identifying target species. After sorting, beetle
size was measured (pronotum length) using a digital microscope, thereafter beetles were dried and weighed
to ascertain body mass (dry weight). Measurments were preformed twice to ensure accuracy.
The trapping effort resulted in 1015 target species individuals of which we obtained data on
body mass and size for 334 individuals of the species Carabus nemoralis (Müller 1764). Furthermore we
measured prey biomass, soil organic matter and soil moisture corresponding to 24 groups of 5 traps each.
Our starting point was to analyse three species we knew to be present in large numbers along the
urbanisation gradient. Unfortunately, we only caught 138 Nebria brevicollis (Fabricius 1792) and 55 Pterostichus
melanarius (Illiger 1783), which was inadequate to make comparisons between habitats. Lack of numbers can
partly be explained by an unusually chilly spring and the fact that these two species reach their maximum
activity later in season that C. nemoralis as a result of their reproductive strategy.
Besides the data we acquired, we had access to diversity and abundance data describing the
2004 and 2005 seasons from the same location (courtesy of G. Lövei & Z. Elek). This provided us with
information on the ground beetle community at Sorø with which we could make informed decisions about
our own experimental work. Of equal importance, this provided us with the appropriate data to establish
patterns of activity across the entire season. Little is known about ground beetle seasonal dynamics in
Denmark and behaviour could easily be a parameter of interest when looking at the effects of urbanisation on
fauna. Activity was studied for C. nemoralis, N. brevicollis and P. melanarius based on data from 2004 and 2005,
and we confirmed statements in the literature concerning relations between peak activity and reproduction
strategy. Furthermore, we found indications that the suburban habitat was different from park and forest
habitats based on displacement of activity patterns. We suggest this delay might be due to food limitation in
the suburban habitat, or otherwise an indication of a source-sink relationship between suburban sites – sinks
- and less disturbed areas farther within the forest or urban habitats - sources. Our results showed lower
levels of prey biomass in the suburban habitat, and, maybe of more interest, indications of worse condition
and lower body size of C. nemoralis from the suburban habitat. We have reason to believe the suburban
habitat is of poorer quality than urban and forest habitats. Despite our initial expectations, this might mean
that human impact is greater in suburban areas compared to the park.
Thus we investigated our main hypothesis – that increasing effects of disturbance, due to
urbanisation, occur when moving from rural to suburban to urban habitats – as tested by ground beetle
condition and seasonal activity. In addition, biodiversity of ground beetles along the same gradient had
already been studied.
We found that condition varied in time, and data from an entire season, or from consecutive
years, would probably improve results. We argue, however, that the initial period of the season, which we
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Environmental Biology – module II
investigated, might be the most relevant to concentrate studies of condition on. This being because beetle
condition in this period primarily reflects the environmental state of the previous season, when the majority
of ground beetles were preparing for hibernation as adults or in the sensitive larvae stage. Furthermore, early
season data reflects true habitat specific condition, as ground beetle migration will only have occurred to a
small degree.
With regards to seasonal activity we accomplished making descriptions of the temporal
dynamics of the three species from a Danish location, but the comparison between habitats could have been
bettered had data on climate i.e., temperature, humidity and rainfall been included. This would have made it
possible to compare tendencies between years.
In general the interpretation of condition and activity results would be improved were more
accurate data on environmental variables (soil moisture and organic matter) collected. Correspondingly, had
we used more traps (or were the weather warmer/greater “hunting luck”), an analysis of greater detail
including spatial differences within habitats (e.g. based on groups of 10 traps), could have been preformed.
These last objections are mainly concerned with logistic limitations.
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Urbanisation and environment
It is well known the human population is increasing, and a growing part prefers to live in or close to urban
centres. In Denmark, human population has increased more than five fold in the last 200 years and along
with it the degree of urbanisation. The number of people living in urban areas in Denmark constituted 21% in
1801, 38% in 1902 and as much as 85% in 2006 (from Statistics Denmark 1902, pp. 1-3 and 2006, p. 28). The
aim of a rural-urban gradient is to examine the effects varying degrees of human disturbance have on nature.
In the following we will deal with direct and indirect effects of human activities on arthropods from a ruralurban point of view. Impact on ground beetles specifically will be elaborated in a later section of this report.
Pollution
Industry and traffic emissions increase the amount of SO2 and N-compounds in the air, which are both
known to cause a decline in arthropod populations (McIntyre 2000 and references herein), lower water
availability (McDonnell et al. 1997 and references herein) and altered element dynamics (Pouyat et al. 1997).
Furthermore, the concentration of heavy metals is higher in urban settings compared with rural environs
(Pouyat et al. 1995 in Pouyat et al. 1997). Soil pH may be elevated, too, caused by the use of building materials
such as concrete (Gilbert 1989 in McKinney 2006) and human activities cause the so-called ‘heat island’
phenomenon, which implies urban average temperatures are 2-3 °C higher than the surrounding areas
(McDonnell 1993 in McDonnell 1997).
Fragmentation
For obvious reasons urbanisation reduces the amount of available habitat. Human constructions create
numerous more or less isolated patches of green areas, which undergo continuous disturbance (McIntyre
2000). This affects which species are capable of dispersing into a new habitat, and which species are able to
maintain a population in a habitat after settling (McIntyre 2000). Roads become the fate of many arthropods,
but they are also known to limit movement of ground beetles (Mader 1984 in Samways 2005, p. 70). This
suggests that dispersal is also affected by human constructions in rural areas.
Biota
In general, disturbance causes a reduction in biodiversity (Gray 1989), but at a local scale arthropod diversity
tends to be elevated due to urbanisation (McIntyre 2000). This is primarily caused by colonization by nonnative species, which benefit from the altered environmental conditions e.g. ‘heat island’ effect (McKinney
2006), or alternatively exotic species that are protected and cared for by humans indirectly. Urban diversity is
of course also affected by local factors including distance to sources of colonists, frequency and size of
disturbance and land use (McIntyre 2000).
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Environmental Biology – module II
Arthropods in conservation
Insects are of great functional importance to ecosystems, e.g. as pollinators, in food webs and nutrient
cycling. Many functions of insects are economically significant to humans (McIntyre et al. 2001).
Another feature is their use in preserving ecological integrity. In fact it is impossible to
measure every parameter of potential relevance in an ecosystem, but environmental monitoring and scientific
foundation is essential in conservation (Carignan & Villard 2001). According to McIntyre et al. (2001)
arthropods are “excellent candidates for studying how the formation of urban ecosystems impacts environment…”
and thus arthropods have a function as indicators of environmental state.
Bioindicators
This section is based on McGeoch (1998).
Bioindication is a tool for conservation; a shortcut to determine environmental health and to a certain degree
to predict biodiversity and the consequences of - human mediated - change in natural systems. Biological
indicators can be categorized into the following three broad definitions according to their use in
environmental monitoring.
Environmental indicators
McGeoch (1998) defines environmental indicators as “a species or group of species that responds predictably, in
ways that are readily observed and quantified, to environmental disturbance or to a change in environmental state”. In
this context these organisms can be thought of as “gauges of changes in environmental state”.
Ecological indicators
Ecological indicators on the other hand are defined as “a characteristic taxon or assemblage that is sensitive to
identified environmental stress factors, that demonstrates the effect of these stress factors on biota, and whose response is
representative of the response of at least a subset of other taxa present in the habitat.” As these indicators are
indicative of responses of other members of the ecosystem, their use provides an overall picture of an
environment, an ecological view.
Biodiversity indicators
A biodiversity indicator is “a group of taxa (e.g. genus, tribe, family or order, or a selected group of species from a
range of higher taxa), or functional group, the diversity of which reflects some measure of the diversity (e.g. character
richness, species richness, level of endemism) of other higher taxa in a habitat or set of habitats.” In this regard the
indicator can be used to indicate species richness of either closely related or completely different taxa.
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The following figure outlines the abovementioned definitions.
Fig. 2. Three categories of bioindication and the subsequent functions of bioindicators within the
categories (From McGeoch 1998).
From the three categories, and therefore in the broadest sense, a bioindicator can generally be
defined as “a species or group of species that readily reflects: the abiotic or biotic state of an environment
(environmental indicator); represents the impact of environmental change on a habitat, community or ecosystem
(ecological indicator); or is indicative of the diversity of a subset of taxa, or of wholesale diversity, within an area”
(biodiversity indicator) (McGeoch 1998). These three categories can be use in two distinct ways: environmental
and ecological bioindicators may be of use in determining and monitoring changes in an environment,
whereas use of a biodiversity indicator is relevant in the context of investigating the diversity of overall biota
in an environment.
Ground beetles as bioindicators
Using the aforementioned definitions the use of ground beetles in our study would fall into the category of
ecological indicator. Whereby ground beetles are being used in an attempt to demonstrate the affect of
urbanisation (viewed in this context as a stress factor) on selected ground beetle species.
McGeoch suggests that the benefits of ecological bioindication would be amplified, if an
ecological indicator’s response to a stressor could be demonstrated as being similar to that of other
substituent species from the tested environment. There exists, however, little evidence of an ecological
indicator fulfilling this (McGeoch 1998).
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Environmental Biology – module II
As described by Raino & Nimelä (2003 and references herein) ground beetles constitute
adequate bioindicators, because of:
ƒ
Widely and successfully used to survey species response to a changing environment
ƒ
Well known ecology and taxonomy, especially for the temperate region
ƒ
High dependency of biotic and abiotic factors, wide habitat requirements and sensitivity to change
ƒ
Cost effectiveness (i.e. easy to collect)
ƒ
Some ability to reflect changes in other species
ƒ
Economic importance (e.g. as predators of agricultural pests)
The use of bioindicators in conservation is not a problem-free endeavour. Carignan & Villard
(2001) mention two of the main arguments against bioindicators. (1) ”…since no two species occupy the same
niche, no single species should be expected to act as an indicator for an entire ecosystem” and (2) “…many factors
unrelated to the degradation of ecological integrity may affect the population status of an indicator species”. The former
issue can, to a certain degree, be dealt with by including several ground beetle species in a survey, whereas
the latter issue is more difficult to resolve. Again the use of many different species in combination with a
wealth of knowledge of causal factors may reduce this problem. For ground beetles, drawbacks could be in
line of seasonal activity patterns, patchy distribution, many generalists and difficulties in predicting ground
beetle richness (Raino & Niemelä 2003).
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Effects of urbanisation on ground beetle assemblages
Intensifying human-caused disturbance along a gradient from rural to urban areas is known to affect ground
beetles in a variety of ways.
GLOBENET
In the context of GLOBENET, profound evidence of responses in ground beetle assemblages have been
reported, but the response patterns seem to differ to varying degrees between countries (e.g. Niemelä et al.
2002; Gaublomme et al. 2005).
In the following the results of GLOBENET-studies from Japan (Ishitani et al. 2003), Hungary
(Magura et al. 2004), Belgium (Gaublomme et al. 2005), Denmark (Elek & Lövei 2005), Bulgaria, Canada and
Finland (Niemalä et al. 2002) will be compared in terms of species richness, opportunistic species, body size
of individuals and stated explanations for these differences.
Species richness
With exception of Hungary, Denmark and Bulgaria the hypothesis that species richness decreases from rural
to urban sites is confirmed (in Canada only when introduced species are excluded). In Bulgaria no significant
rural-urban changes in species richness were found, but on the contrary both in Denmark and Hungary
higher species richness was seen at urban sites compared to suburban and rural habitats.
Generalists versus specialist
The urban sites are often dominated numerically by fewer species, which tend to be habitat generalists,
whereas more forest specialists are encountered in suburban and rural areas (Gaublomme et al. 2005; Magura
et al. 2004). In Canada and Finland the same opportunistic genus (Calathus) dominated urban sites (48% and
46% of total catch, respectively). Ishitani et al. (2003), however, found forest specialists in all urbanisation
habitats, but larger sized specialists were absent in urban habitats. Conflicting results were also seen in
Hungary, where a forest specialist was dominant in suburban sites (48% of total catch), yet there were no
dominant species in the urban habitat.
Body size
Evidence of smaller and more mobile species from rural to urban habitats is generally observed (Gaublomme
et al. 2005; Niemelä et al. 2002; Ishitani et al. 2003; Magura et al. 2004). This is partly explained by Gray’s (1989)
hypothesis, which states that the mean size of species decreases with intensifying disturbance. The
relationship is supported by Blake et al. (19941), who found that community level mean body size of ground
1
The study did not follow the GLOBENET project protocol.
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Environmental Biology – module II
beetles relates to intensity of management, and suggested the relation is due to smaller species being better
adapted to coping with fluctuating resources in disturbed environments. An additional explanation could be
the fact that smaller species have larger dispersal capacity, e.g. ability of flight, which favours them in an
urban habitat of lower quality (Gaublomme et al. 2005). The latter was seen in Belgium and Bulgaria, whereas
in Finland and Canada, ground beetles capable of flight were significantly larger than flightless species
(Gaublomme et al. 2005). On the basis of findings of small mobile species in urban sites of large old forests,
Gaublomme et al. (2005) suggests that smaller body size is the result of low habitat quality caused by
disturbance rather than habitat fragmentation and isolation.
Variations between countries
Even within one group of organisms (Carabidae) there are many diverse responses to urbanisation. The
different patterns in ground beetle assemblages in relation to urbanisation that are seen in the above-cited
studies could find explanation in the different characteristics of the investigated cities i.e. spatial structures,
the degree of anthropogenic disturbance, age and degree of development, surrounding area (Ishitani et al.
2003). Furthermore, the geographical location, altitude and vegetation differ among cities (Gaublomme et al.
2005). Nor is the urbanisation gradient simple, but rather multidimensional, and includes many varying
parameters such as temperature, moisture, pollution, edaphic factors etc. (Ishitani et al. 2003). Also
interactions between species and annual fluctuations might confuse results.
Factors influencing body size and condition
Habitat quality in general induces changes in morphological characteristics, such as body size (Weller &
Ganzhorn 2004) and changes in ground beetle condition (Bommarco 1998). Condition is a relative measure of
fitness between body size and mass (Östman et al. 2001) or differences in body asymmetry (interpreted as a
sign of developmental stress) (Weller and Ganzhorn 2004). Variations in interspecific interactions (Sota et al.
2000), management and environmental conditions (Blake et al. 1994; Ribera et al. 2001) are all factors causing
differences in body size between populations.
Many examples of different characteristics relating to the physical habitat of ground beetles
have been seen to influence body size. When investigating changes in ground beetle populations, increases in
beetle condition have been observed in association with increasing habitat age from 1 to 4 yr (Barone & Frank
2003), but a study of regeneration of a habitat after pollution showed the average body size tended to
decrease (Braun et al. 2004). However, the two studies focused on populations and communities, respectively,
which result in different outcomes and give rise to different explanations. The results of Barone & Frank
(2003) are explained by a more diverse habitat, which coincides with fewer disturbances and therefore more
ground beetle prey, among other factors. The results of Braun et al. (2004) are thought to be due to a higher
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degree of ground beetle specialization in later stages of succession. Yet on the other hand, Kotze & O’Hara
(2003) actually observed that specialists in their study have larger bodies compared to generalist species.
Larger size variations (average size ratio decreased) were found going from sites having 2
species to sites with 3 or 4 species in a study emphasizing interspecific interactions (Sota et al. 2000; see also
Weller & Ganzhorn 2004). Loreau (1992) emphasized competition in ground beetle-assemblages as being of
greater importance compared to other insects, because of beetles being large in size, long-lived, and having
carnivorous tendencies. On the other hand Niemelä (1993), in a review, downplayed the importance of
interspecific competition, stating that the effect is simply unclear and not well supported.
Habitat management and disturbance affect body size, and within grasslands Blake et al.
(1994) reported decreasing body size as management intensity increased. Fluctuating resources in a disturbed
(highly managed) area favoured small species with high growth rates and dispersal ability (Blake et al. 1994).
Ribera et al. (2001) accomplished similar results, and argued that sites with higher degree of management,
and therefore disturbance, had more bare ground and lower biomass etc., and implicitly worse habitat
quality for ground beetles. Management effects include both land use and practice, e.g. organic farming leads
to higher ground beetle condition because of lower pesticide use, higher crop diversity, and more favourable
soil properties related to organic farming practice versus conventional farming (Östman et al. 2001;
Bommarco 1998). Natural and changing environments are likewise known to affect condition, in that less
stable environments supposedly are more prone to food shortage and therefore support ground beetles of
lower condition (Juliano 1986).
Different measures of habitat isolation and size affect ground beetles as well. Weller &
Ganzhorn (2004) found decreasing body size when isolation increased, but decreasing condition (fluctuating
asymmetry) with increasing isolation and habitat size. Higher area-perimeter ratio gave higher ground beetle
condition, which could be explained by better reproduction possibilities (Östman et al. 2001; Bommarco
1998).
Soil factors have been found to correlate with ground beetle body size caused indirectly by the
fact that soil characteristics might change with habitat age and disturbance degree (Blake et al. 1994; Barone &
Frank 2003). In woodlands, Blake et al. (1994) observed a positive relation between the soil organic matter
content and body size, whereas Barone & Frank (2003) found an increased ground beetle condition in
conjunction with increasing soil water content in wildflower areas. Opposed to this are the grassland results
of Blake et al. (1994), in which factors such as increasing soil water and organic matter content were related to
decreasing body sizes. Furthermore Barone & Frank (2003) presented indications of a positive relation
between the extent of vegetation cover and condition.
Sota et al. (2000) observed that in 9 out of 15 species of a spring breeding ground beetles, body
size was related to annual mean temperature. This implies that higher mean temperature leads to increased
body size, due to the greater amount of heat available to e.g. the development of larvae (Sota et al. 2000). In
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Environmental Biology – module II
addition Sota et al. (2000) found clear evidence that Carabus species exhibit differences in body size according
to sex, where females are larger than males.
To recapitulate, many biotic and abiotic variables affect body size and condition in single
species along landscape gradients and also in terms of the mean body size of ground beetle assemblages.
Seasonal activity
Investigations of beetle seasonal activity are necessary for several reasons. First of all, enhanced biological
and ecological are of course desirable for intrinsic reasons and necessary in the study of effects of
environmental change. Specific information on the life histories of ground beetles can be used to plan catch
periods for studies of diversity (Werner & Raffa 2003), or, as is the case in our study on beetle condition, for
ascertaining a general time of beetle emergence, which we subsequently used to plan our trapping period.
Beetle activity can be influenced by several biotic factors including prey density, level of
hunger, reproductive state (Wallin & Ekbom 1994) and abiotic factors such as temperature (Honek 1997),
amounts of precipitation (Thomas et al. 1998), light intensities and humidity (Thiele 1977). Several authors
have shown that carabid beetle assemblages differ along a rural-urban gradient (See section on GLOBENET).
However, studies of beetle seasonal activity along urbanisation or other disturbance gradients have, to our
knowledge, received little attention to date.
In our article on seasonal activity of three ground beetles along a rural-urban gradient we
investigated whether there were differences in activity among beetles from different habitats. Dülge (1994)
reported beetle seasonal activities could vary in the same beetle found in different geographical areas. On a
large scale, comparative studies of seasonal activity can investigate differences/similarities in seasonal
activities of beetles from different regions and even different countries or continents. In our case we focused
our attention at a smaller scale, that of an urbanisation gradient, and compared the activities of beetles in
different habitats along an urbanisation gradient, with the aim of investigating whether differences in
seasonal activities occurred in sites along the urbanisation gradient. As ground beetle seasonal activity has
also been shown to differ annually (Makarov 1994) we analysed data of beetle catches from two successive
years. To the best of our knowledge, this information on C. nemoralis, N. brevicollis and P. melanarius in
Denmark is scant or non-existent.
The most common methodology for attaining data on ground beetle seasonal activity is pitfall
trapping. This method relies on the activity of beetles themselves for results (Lövei & Sunderland 1996) and
provides a measurement of activity density, rather than of absolute density (French & Elliot 1999). Catch
quantity and composition depends on several factors including trap-construction, beetle activity and
behaviour (Lövei & Sunderland 1996).
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Biology and ecology of three ground beetles
Our scientific articles are, as mentioned above, based on three common ground beetle species; C. nemoralis, N.
brevicollis and P. melanarius. All three species have been found in great numbers across the Sorø rural-urban
gradient, which allows us to compare individual species between habitats. Unfortunately however, only
sufficient numbers of C. nemoralis were encountered in our field work during the spring of 2006, for which
reason the study on ground beetle condition is limited to this species. In the following we aim to briefly
present the three species in terms of their respective biologies and ecologies, and to establish the basis for
analysing different responses between habitats.
Carabus nemoralis (Müller 1764)
C. nemoralis is a eurytopic ground beetle found on all types of humus rich and moderately dry soil e.g. light
woods, parks, gardens, open and agricultural land (Lindroth 1985). In Denmark it is the most common
Carabus species and has the broadest distribution amongst the genus Carabus in Denmark (Bangsholt 1983). C.
nemoralis is nocturnal and a polyphagous predator feeding on a wide array of insects. It is also known to eat
fruit and bread in captivity (Larochelle 1990).
C. nemoralis is of medium size (22-26 mm). It is a spring breeder, reproducing in April-June
with new adults emerging in August-September (Lindroth 1985; Bangsholt 1983). C. nemoralis is
brachypterous2 (Bangsholt 1983)
In the Danish GLOBENET study, C. nemoralis numbers increased from rural to urban sites
(Elek & Lövei 2005). This observation was not seen in Finland, where C. nemoralis was consistently most
abundant at suburban sites (Alaruikka et al. 2002; Niemela et al. 2002; Venn et al. 2003). Similarly, Weller and
Ganzhorn (2004) reported greatest numbers of C. nemoralis at suburban sites in Germany. In Belgium, C.
nemoralis was caught only at rural sites (Gaublomme et al. 2005). Whereas in Canada, C. nemoralis was most
abundant at urban sites (Niemelä et al. 2002). These results reflect C. nemoralis eurytopic nature through its
broad preference of suitable habitats.
Nebria brevicollis (Fabricus 1792)
N. brevicollis is a eurytopic (generalist) woodland species being found predominantly in deciduous forests
(beech) throughout much of Scandinavia. N. brevicollis is also found inhabiting open country, often in parks
and gardens, where it prefers shaded areas (Lindroth 1985). It is very common and very widespread
throughout Denmark and is often found on a substrate of moist mull (Bangsholt 1983). N. brevicollis is
nocturnal and predatory, feeding mainly on insects (Larochelle 1990).
2
Possessing non-functional wings
17
Environmental Biology – module II
N. brevicollis is a small ground beetle (10-14 mm), being the smallest of the three ground
beetles under investigation in the present studies. N. brevicollis is macropterous3, having large, welldeveloped wings (Bangsholt 1983) and is considered as possessing good dispersal ability (Gaublomme et al.
2005). With regards to N. brevicollis reproduction strategy, Lindroth (1985) and Weller & Ganzhorn (2003)
report the beetle is an autumn breeder with new adults and overwintering adults occurring in spring. After
emergence, N. brevicollis exhibits intense activity in order to build up fat reserves. After this period the beetles
enter a period of aestivation, where they aggregate under bark of tree stumps and logs on the forest floor,
and in autumn, activity is resumed and breeding takes place (Lindroth 1985). Larvae, at different stages of
development, and a number of adults hibernate through the winter (Lindroth 1985).
Classification of N. brevicollis as a eurytopic woodland species is reflected in past GLOBENET
studies. It has been observed in forest patches across all habitats (rural, suburban and urban) in Belgium
(Gaublomme et al. 2005), Bulgaria (Niemelä et al. 2002), Denmark (Elek & Lövei 2005) and in a German study,
which was not associated with the GLOBENET project (Weller & Ganzhorn 2004). In the GLOBENET studies
the greatest numbers of beetles were found in the urban forests, followed by rural forest, with least amounts
caught in suburban forests (Table 1). Similarly Weller & Ganzhorn (2003) reported greatest catches of N.
brevicollis in urban forests, but with smallest catches in rural forests.
Pterostichus melanarius (Illiger 1783)
P. melanarius is a very eurytopic (generalist) species, but it is predominantly found in not too dry, open
grassland and meadows. It often inhabits areas of anthropogenic influence i.e. parks and gardens, but can
also be found along forest fringes and light woods (Lindroth 1986). It is both very common and widespread
throughout Denmark (Bangsholt 1983). P. melanarius is nocturnal and a mixed feeder, acquiring its
nourishment predominantly from insects, but seed and plant material may also make up part of its diet
(Larochelle 1990).
P. melanarius is small (12-18 mm) and dimorphic with ability of flight. The macropterous form
is very rare in Fennoscandinavia (Bangsholt 1983). Dimorphism was investigated in Denmark where 99.5% of
all investigated individuals were brachypterous, the remainder being macropterous (Bangsholt 1983). It is an
autumn breeder with reproduction taking place around August-September. Larval hibernation takes place in
the third instar and adult beetles emerge, after completing development, during the following spring and
summer. (Lindroth 1986) Beetles over-winter a second and sometimes third winter as adults (Wallin 1985).
In GLOBENET studies, P. melanarius has been found in all sites along the urbanisation
gradient (urban, suburban and rural) at all European locations and in Canada (Table 1). The very eurytopic
nature of P. melanarius is reflected in the total catch results from previous studies. It was most abundant at
3
Possessing functional wings
18
Roskilde University
rural sites in Finland (Alaruikka et al. 2002; Niemelä et al. 2002; Venn et al. 2003) and Germany (Weller &
Ganzhorn 2004), yet most abundant in urban sites in Denmark (Elek & Lövei 2005) and Bulgaria (Niemelä et
al. 2002). P. melanarius was most abundant at urban sites in the Canadian GLOBENET study, where it is not
endemic (Niemelä et al. 2002).
Table 1. Abundance of N. brevicollis, P. melanarius and C. nemoralis in 8 countries where species
distribution along urbanisation gradients have been studied (U = urban, SU = suburban and R = rural
habitats). *Study did not follow the GLOBENET project protocol.
N. brevicollis
Country
P. melanarius
C. nemoralis
Reference
U
SU
R
U
SU
R
U
SU
R
Finland
-
-
-
11
37
404
6
15
10
Alaruikka et al. 2002
Finland
-
-
-
34
84
416
3
28
18
Venn et al. 2003
Belgium
1299
501
655
-
-
10
-
-
10
Gaublomme et al. 2005
Denmark
818
117
169
1780
98
631
307
271
145
Elek & Lövei 2005
Japan
Ishitani et al. 2003
Canada
-
-
-
7970
2001
328
666
48
-
Niemelä et al. 2002
Bulgaria
269
9
17
78
50
38
-
-
-
Niemelä et al. 2002
Finland
-
-
-
34
84
416
3
28
18
Niemelä et al. 2002
496
334
252
7
17
29
17
22
10
Weller & Ganzhorn 2004*
Germany
The three species C. nemoralis, N. brevicollis and P. melanarius are eurytopic, which has been
shown in several studies, where the beetles were found in all habitats along urbanisation gradients (Table 1).
Based on results from Elek & Lövei (2005) we expected to find the three ground beetles in the rural-suburbanurban habitats, as we used the same localities along the urbanisation gradient in our studies of beetle
condition and seasonal activity. In that the beetles are present in all habitats allowed us to compare the
species between habitats along the urbanisation gradient. Beetle condition and activity can thereby be
compared in response to varying degrees of urbanisation.
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Environmental Biology – module II
Ground beetle (Coleoptera: Carabidae) condition along an
urbanisation gradient
Abstract
Condition of the ground beetle Carabus nemoralis was studied using pitfall trapping along an urbanisation gradient in Sorø, Denmark, as
a contribution to the Danglobe project.
We analyzed ground beetle body size and condition spatially across a rural-suburban-urban gradient, representing
increasing intensity of human disturbance, and temporally as changes during spring months of 2006, which coincided with the seasonal
activity peak of C. nemoralis. We calculated condition as the residuals to the regression between pronotum length and body mass.
Only females showed significant differences in body size and condition along the gradient and indications of lower
habitat quality at the suburban sites were found, i.e. decreasing body size and lower residual indices compared to rural and urban
habitats. We suggest that female condition and body size is more variable compared to male due to higher environmental dependency in
terms of greater energy demands connected with egg production etc. Condition changed over time, and the tendencies differed between
habitats along the urbanisation gradient. This underlines the importance of including the temporal dimension in analysis of ground
beetle condition.
Overall, indications that the suburban habitat ranks lower than urban and rural sites could be explained by
urbanisation-caused disturbance. Despite our expectations the suburban habitat appeared to be of worse quality than the urban habitat.
We suggest environmentally friendly park management lessens the potential impacts in the urban habitat.
Tilstandsændringer for løbebillen Carabus nemoralis blev undersøgt ved hjælp af fangstglasindsamlinger langs en urbaniseringsgradient
ved Sorø. Undersøgelsen var en del af Danglobe-projektet.
Resumé
Vi analyserede løbebillernes kropsstørrelse og tilstand både rumligt langs en forstyrrelsesgradient gående fra park over bebyggelsesnær
skov til ren skov, samt over tid i løbet af foråret, hvor C. nemoralis er overvejende aktiv. Løbebillernes tilstand blev beregnet som
residualerne mellem målt biomasse og forudsagt biomasse fra en regression mellem kropslængde og biomasse.
Kun hunnerne viste signifikante forskelle i kropsstørrelse og tilstand langs gradienten, hvilket hovedsageligt
udtryktes som mindre kropsstørrelse og lavere tilstand i bebyggelsnær skov end i park og ren skov. At udelukkende hunnerne viste
forskelle kan skyldes, at de modsat hannerne er mere miljøafhængige i kraft af deres energikrævende ægproduktion o.lig.
Løbebilletilstanden ændredes over tid og ændringerne var uensartede mellem habitaterne langs gradienten, hvilket understreger
vigtigheden af at tage højde for tidsaspektet i tilstandsundersøgelser.
Overordnet peger vores resultater i retning af, at den bebyggelsesnære lokalitet er af lavest kvalitet, hvilket kan finde
forklaring i stigende forstyrrelse som følge af urbanisering. Modsat vores forventninger lader den bebyggelsesnære skov til at være mere
påvirket end parken, hvilket dog kan skyldes, at naturnær parkdrift modvirker effekterne af urbanisering.
20
Roskilde University
Introduction
Arthropods are often chosen as indicators of urbanisation effects on ecosystems, due to their high abundance,
reproduction rate, functional diversity, economic importance and the fact that they relatively easy to sample
(McIntyre 2000; McIntyre et al. 2001). In general the use of bioindicators is a cost-effective way of assessing
human impact, and ground beetles (Coleoptera, Carabidae) are a frequently used indicator of environmental
condition (Rainio & Niemelä 2003). Ground beetles are sensitive to manmade disturbance and are diverse in
terms of ecology and taxonomy (Lövei & Sunderland 1996).
In context of the international Globenet Project (Niemelä et al. 2000), a common methodology
has been developed to study the changes in biodiversity of ground beetles along a rural-suburban-urban
gradient in the search of global patterns in the effects of human presence. A majority of published Globenet
project results have focused on community species composition and life history traits (e.g. Hungary (Magura
et al. 2004), Japan (Ishitani et al. 2003), Belgium (Gaublomme et al. 2005)). However, not only species presence
but other species- or population- level attributes could be useful, and possibly more sensitive, measures of
habitat alteration. As a part of Danglobe, the Danish component of the Globenet Project, this study is aimed
to test whether species level differences in ground beetle condition could be indicative of changing
environment during urbanisation.
Urbanisation alters the biotic and abiotic environment (McDonnel et al. 1997) and changing
habitat quality may be reflected in ground beetle morphological characteristics (Weller & Ganzhorn 2004) or
body size distribution (Magura et al. in press). Body size is affected by habitat type, disturbance and
management (Blake et al. 1994; Ribera et al. 2001) and an array of environmental factors, including soil
organic matter (Blake et al. 1994), habitat isolation (Weller & Ganzhorn 2004), temperature (Ernsting & Isaaks
1997), and interspecific interactions (Sota et al. 2000). Identically, nutritional condition is affected by soil
moisture, vegetation cover (Barone & Frank 2003), and the structure of habitat such as perimeter-to-area ratio
(Östman et al. 2001; Bommarco 1998).
Condition of ground beetle is food limited and food limitation varies in space (Bommarco
1998; Juliano 1986) and time (Östman 2005; Barone & Frank 2003). In this study we aim at investigating the
influence of urbanisation on ground beetle condition, both temporally and across habitats. Investigating
condition is a step to understand how landscape affects ground beetle populations through condition-related
dynamics e.g. survival and reproduction success (Juliano 1986).
We argue the initial period of the season to be the most relevant, as beetle activity is
approaching its peak (Fig. 1). Parallel to the approach of Bommarco (1998), who found that condition after
oviposition was a reliable estimate of overall condition; we argue that beetle condition between spring
emergence and female oviposition results in a reasonable estimate of complete seasonal condition. In
addition, beetle condition during this period primarily reflects the environmental state of the previous
season, when the sensitive and relatively immobile larvae were developing (Lövei & Sunderland 1996) and
21
Environmental Biology – module II
adult ground beetles were acquiring fat reserves in preparation for overwintering. Furthermore, we assume
their early season data will reflect true beetle condition, as ground beetle migration will only have occurred
to a small degree. We expect to find ground beetles of poorer condition in urban settings due to an expected
higher degree of human disturbance.
Study organism, location, materials and methods
The target species in this study, Carabus nemoralis (Müller 1764), is a eurytopic generalist common to light
woods, parks, gardens, open and agricultural land (Lindroth 1985) and with wide distribution in temperate
Europe (Turin 2003). In a preceding study great abundance of C. nemoralis was found all along the
urbanisation gradient, albeit numbers varied between years and site (Table 1). C. nemoralis is a spring breeder
reproducing in April-June with new adults emerging in August-September (Lindroth 1985; Bangsholt 1983).
Our study area was located in South Western Zealand, Denmark, in and around the town of
Sorø. Three habitats – rural, suburban and urban – were selected around the Sorø Lake ranging from the Sorø
Akademi Park to a managed beech forest. The habitats were no less than 1 km and no more than 6 km apart.
In each habitat, 4 sites with at least 50 m between each other were selected. At every site 2
groups of 5 traps each were set with at least 10 m between the individual traps. The 120 (3 urbanisation
stages x 40 traps/stages) traps were controlled fortnightly from the beginning of April to the end of May
2006.
The capture was sorted into ground beetles and prey, respectively. All non-ground beetle
catch, except slugs and snails, were considered a crude measure of ground beetle prey biomass. The prey was
pooled for each group of 5 traps and dried for at least 62 h at 65 °C before weighing. For each group of 5
traps, 2 soil samples were taken to determine soil moisture and organic matter. The soil samples where dried
for 24 h at 105 °C and weighed (to obtain the water content), after which they were burned at 550 °C for 2 h
and weighed again (to obtain the amount of dry organic matter). As mentioned above ground beetle
condition is food limited (i.e. prey biomass), and affected by microclimate parameters such as soil moisture
and soil organic matter, which is why we consider these as relevant background variables when studying
changes of ground beetle condition.
22
Roskilde University
Table 1. Data of overall ground beetle abundance and diversity and individual numbers of C. nemoralis in the different habitats along the
urbanisation gradient from the 2004 (Elek & Lövei 2005) and 2005 (Elek & Lövei unpubl.) Danglobe studies in the selected area. 2004 data is based
continuous sampling, whereas 2005 is pulsed sampling every second fortnight.
Year
Type of measure
Rural
Suburban
Urban
2004
Overall abundance
4255
1670
4389
Overall richness
25
21
37
No. of C. nemoralis
145
271
307
Overall abundance
1742
1283
1936
Overall richness
19
18
33
No. of C. nemoralis
46
170
67
2005
Cumulative activity, %
100
75
50
25
0
0
20
40
60
80
100
120
140
160
Time, days since the start of the study
Fig.1. Cumulative activity against time for C. nemoralis in 2004 (filled squares) and 2005 (open squares). The thick line illustrates equal activity
across the entire season without any activity peak. The pattern indicates that C. nemoralis is most active during spring (Apr – Jun).
(see Seasonal activity-article in this report)
23
Environmental Biology – module II
All individuals of C. nemoralis (identified using key by Lindroth 1985) were dried for at least 62 h at 65 °C,
sorted by gender and the dry body masses were established. Body size was characterized by the length of
pronotum. The measurement was made mediodorsally along the pronotum in an anterior-posterior direction
using a digital image under a microscope. The measurement was taken to a precision of 1/100 micron using
Leica IM50 software. For accuracy, both body mass and size were determined twice.
We calculated condition as the residuals to the regression pronotum and body mass. Due to
the size dimorphism separate regressions were established for males and females. This approach results in a
residual index (RI), which is the difference between the actual (measured) and the expected body mass of an
individual of a certain size. Positive values of the RI indicate a better-than-expected ground beetle condition;
negative indicate the opposite. Juliano (1986) showed in a feeding experiment that there is a positive
correlation between the ground beetle RI calculated for Brachynus sp. and its fat reserves, and Östman et al.
(2001) established a similar relation for Pterostichus sp.
Differences in body size (pronotum length) were tested with one-way ANOVAs followed by a
Tukey test. Biotic variables were tested for difference between habitats using one-way ANOVAs or KruskalWallis tests and multiple range tests, for those data not fulfilling parametric requirements. For analyses of
differences of male and female RI over time and between gradients we employed a general linear model as
not all data fulfilled the requirements of parametric tests, whereas tests for female differences of RI between
habitats and samplings were performed with one-way ANOVAs. The same analyses for males were
performed with Kruskal-Wallis tests for non-parametric data. Correlations were tested using Pearson’s
correlation coefficient and Spearman Rank tests. Tests were preformed using Systat 11 software.
Results
We captured 90 C. nemoralis individuals (34 males, 56 females) in the rural habitat, the urban site yielded 102
individuals (30 males, 72 females), and at the suburban site the catch amounted to 142 individuals (37 males,
105 females) (Table 2).
Analysis of body size, from rural to urban habitats (pronotum length) clearly indicated that
female C. nemoralis were smaller at the suburban habitat (Table 2). However, neither male nor female showed
signs of decrease in condition (residual index, RI) when compared spatially. When time was included in the
analysis, we encountered slight differences in RI between habitats, and there were indications of temporal
changes in condition between 1st, 2nd and 3rd sampling.
The variance in RI and body mass could partly be explained by the investigated variables:
prey biomass, numbers of C. nemoralis, soil moisture and organic matter. Except for prey biomass (KruskalWallis test, P = 0.002) we saw no differences between habitats in terms of the environmental variables: Soil
moisture (one way-ANOVA, F = 0.557, df = 2, P = 0.581), soil organic matter (one-way ANOVA, F = 1.398, df
= 2, P = 0.269), and C. nemoralis abundance (one-way ANOVA F = 0.628, df = 2, P = 0.543). Significantly lower
24
Roskilde University
levels of prey biomass were only found in suburban habitat in comparison to urban (Multiple range test, P <
0.05), thus no significant differences in other habitat combinations.
Body size
Suburban female ground beetles had significantly lower body sizes compared to rural and urban habitats
(one-way ANOVA, F = 7.837, df = 2, P = 0.003; followed by Tukey post hoc-test, P < 0.05). There was no
significant difference among male C. nemoralis (one-way ANOVA, F = 1.181, df = 2, P = 0.327). No differences
across the samplings were found (results not shown).
A non-significant negative tendency between values for male body size and soil moisture
(Pearson’s correlation, r = -0.381, P > 0.05) and for male body size and female RI occurred (Pearson’s
correlation, r = -0.328, P > 0.05,). On the other hand, we found a slight positive correlation between male body
size and prey biomass (Spearman Rank, r = 0.274, P > 0.05) (Table 4). Female body size was significantly,
negatively correlated with activity density (Pearson’s correlation, r = -0.42, P < 0.05) and positively with prey
biomass (Spearman Rank, r = 0.552, P < 0.01) (Table 4).
25
Environmental Biology – module II
Table 2. Characteristics of C. nemoralis in terms of RI and body size (μm) divided into gender and sampling site and time.
Male
RI
Sampling habitat and time
Female
Body size
RI
Body size
Mean
SE
Mean
SE
n
Mean
SE
Mean
SE
n
1st
-4.2
12.5
499.1
7.6
7
39.8
13.0
478.8
7.2
2
2nd
-4.5
2.9
432.5
2.9
39
-14.1
8.5
478.8
7.2
24
3rd
6.3
4.5
449.1
7.6
10
27.6
9.4
464.2
4.0
8
1st
-9.5
5.5
435.7
3.2
34
-20.5
16.8
443.3
5.9
11
2nd
-9.4
2.4
437.6
3.3
45
3.8
12.9
442.9
5.2
15
3rd
40.6
12.0
432.6
2.9
26
4.2
18.1
457.6
8.1
11
1st
-18.0
4.1
449.2
2.3
15
72.7
18.5
474.6
9.8
4
2nd
-3.3
4.5
447.9
2.3
40
12.5
13.8
468.5
3.9
19
3rd
13.9
6.9
442.4
3.5
17
-52.3
21.4
465.4
8.4
7
Rural
Suburban
Urban
26
Roskilde University
550
Male
Female
Body size
500
450
**
400
*
350
r
Ru
al
b
Su
n
ba
ur
n
ba
Ur
r
Ru
al
an
rb
bu
u
S
n
ba
Ur
Fig. 2. Body sizes (μm) at rural, suburban and urban as box plot (±SD, average, 25% quartile, and 75% quartile) separated in male and female.
Asterisks denote significant differences (* = P < 0.05, ** = P < 0.01).
150
Female
Male
RI
50
-50
-150
r
Ru
al
b
Su
ur
ba
n
ba
Ur
n
Ru
l
ra
b
Su
ba
ur
n
b
Ur
an
Fig. 3. Total RI for males and females, respectively. Boxes indicate ±SD, average, 25% quartile, and 75% quartile.
27
Environmental Biology – module II
Table 3. GLM results analyzing RI across habitats for both sexes, but 1st, 2nd and 3rd samplings separately.
Asterisks (*) denote significant results (* = P < 0.05).
Sampling period
df
SS
MS
F
H
P
1st
2
4676.8
2538.14
6.4
19.7
<0.05*
2nd
2
5700.8
2850.4
1.0
5.4
>0.05
3rd
2
3802.5
1901.2
4.3
3.9
<0.05*
Table 4. Pearson correlation coefficients, r, between male and female RI and body masses grouped in subsamples of 5 traps across the entire study
period and the measured variables: soil moisture, soil organic matter, activity density of C. nemoralis and prey biomass (n = 24). Cross (†) denotes
Spearman correlation coefficient. Asterisks denote significant results (* = P < 0.05, * *= P < 0.01).
Male
Variable
28
Female
RI
Body size
RI
Body size
Soil moisture
0.104
-0.381
0.279
0.087
Soil organic matter
-0.296
0.101
0.358
-0.026
Activity density
-0.062
-0.007
0.393*
-0.420*
Prey biomass †
0.021
0.274
0.115
0.552**
RI (female)
-0.200
-0.328
-
-0.060
Body size (male)
-0.056
-
-0.056
0.079
Roskilde University
Condition
When condition indices of all three collection periods were considered together, but separated by sex, there
were no significant differences among rural, suburban and urban habitats (Kruskal-Wallis test, male: P =
0.79, female: P = 0.72, Fig. 3). Males and females did not show sex specific differences in RI, either. However,
expanding the analysis to include the temporal differences between the 1st, 2nd and 3rd sampling results
indicated significant differences between habitats (Table 3). Significant differences in the 1st sampling were
due to higher female RI in urban compared to suburban habitats (one-way ANOVA, F = 5.491, df = 2, P =
0.017; followed by Tukey post hoc-test, P = 0.017). In the 3rd collection period we found higher female RI in
rural compared to urban sites (one-way ANOVA, F = 4.785, df = 2, P = 0.018; Tukey, P = 0.016), and female RI
tended also to differ between urban and suburban habitats (one-way ANOVA F = 4.785, df = 2, P = 0.018;
Tukey, P = 0.078). There were no differences in female (one-way ANOVA, F = 1.015, df = 2, P = 0.218)
condition during the 2nd sampling period. Male RI were not significantly different between habitats at any
time (Kruskal-Wallis test, P > 0.05 in all cases).
Variance in RI is partially correlated with supposed background variables. Female condition
was significantly correlated with the density activity of C. nemoralis (Pearson’s correlation, r = 0.393, P <
0.05,), and was not significantly correlated with soil organic matter (r = 0.358, P > 0.05) or soil moisture (r =
0.279, P > 0.05). Condition of males was not significantly correlated with any of the variables, but tended to
be related to soil organic matter (r = 0.296, P > 0.05) and to a minor negative extent to female RI (r = -0.2, P >
0.05).
Temporal change
During the study period a change in condition was detected (Table 2, Fig. 4) although no clear pattern
emerged. For females, a significant decrease in condition was seen in the urban habitat (one-way ANOVA, F
= 6.438, df = 2, P = 0.005; followed by Tukey post hoc-test 1st-3rd: P = 0.005, 2nd-3rd: P = 0.042; Fig. 4), while an
increase was indicated in rural area (one-way ANOVA, F = 4.867, df = 2, P = 0.015; 2nd-3rd: Tukey, P = 0.03).
Fig. 4 displays furthermore significant male condition increases over time in suburban (Kruskal-Wallis test,
1st-3rd: P < 0.01, 2nd-3rd: P < 0.01) and urban areas (Kruskal-Wallis test, 1st-3rd: P < 0.01).
29
Environmental Biology – module II
150
*
100
RI
50
0
3rd
2nd
1st
-50
-100
Rural
-150
Sampling
**
**
150
100
RI
50
0
2nd
1st
3rd
-50
-100
Suburban
-150
Sampling
**
100
*
**
80
60
40
RI
20
1st
2nd
3rd
0
-20
-40
-60
-80
Urban
Sampling
Fig. 4. Graphs representing habitat specific RI (±SE) at the 1st, 2nd and 3rd sampling for male (■) and
female (□) C. nemoralis. Solid lines refer to males, broken lines to females. Asterisks denote significant
differences (* = P < 0.05, **= P < 0.01).
30
Roskilde University
Discussion
The results of the study indicated that suburban habitat quality, and therefore condition of C. nemoralis, is
poorer compared to rural and urban habitats. The most apparent results are differences in female body size
(Table 2, Fig. 2), which demonstrate significantly lower body sizes in suburban compared to rural and urban
habitats. Weller & Ganzhorn (2004) found a similar decrease in body size of C. nemoralis, but this was
towards an urban core and not the intermediate suburban site, as our results indicate. The pattern of
suburban distinctiveness is moreover supported by a tendency towards larger female RI in urban compared
to suburban sites from 1st and 3rd samplings. In addition interesting parallels can be drawn to the 2004 and
2005 data for activity density of C. nemoralis, total ground beetle numbers and species richness (Table 1). The
suburban area exhibits least species richness (2004 and 2005) and lowest overall ground beetle activity
density (2004 and 2005), but the highest (2004 and 2006 (Table 2)) and second highest (2005) C. nemoralis
individual numbers. C. nemoralis is a generalist species and the activity density and species richness
differences could support the assumption of a low quality suburban habitat. Results of this study in terms of
significant positive correlations between female RI and numbers of C. nemoralis, and the negative correlation
between female body size and individual numbers (Table 4), suggest that biotic interactions influence C.
nemoralis.
It is striking that not only is female body size greater than male, but it appears that female
condition is also more related to habitat and environmental variables. Even though male body size is
significantly lower in the suburban habitat, we found no condition differences between sites after time was
taken into account, whereas female condition was different. We did not find significant correlations between
male condition and the supposed environmental background variables (Table 4). Generally female condition
seems noticeably more variable across the landscape, despite no significant differences between habitats
when looking at overall C. nemoralis abundance, soil moisture and organic matter (Table 4). Juliano (1986)
found that for Brachinus sp. the condition response for males was more variable than for females. The malefemale differences in condition and body size could be explained by the females’ need to invest large
amounts of energy in production of eggs and finding suitable oviposition sites to lay them, which make
them more prone to the effects of low habitat quality. Males roam to find food and females, but do not have
the same energy requirements as females. Food limitation of females is supported by the significant positive
correlation between female body size and prey biomass (Table 4).
The use of residual indices is considered a sensitive measure of condition, but our results
show that condition varies temporally, which can hinder comparison between different habitats, as opposed
a stable factor such as body size. This result is in line with those of Östman (2005), who concluded that
variations in condition between years could be greater than spatial variations in one single year. Caution
should therefore be exercised when interpreting results based on condition indices. It should be noted too,
that in our study, the number of female ground beetles caught per habitat may not always have been
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Environmental Biology – module II
sufficiently large. This could have been remedied by omitting these particular sampling data from analysis,
which we have chosen not to do.
Our work indicates the importance of urbanisation on ground beetle condition, but reveals no
clear overall tendency along the rural-suburban-urban gradient. We suggest that ‘benevolent park
management’, such as the return of cuttings to the understory instead of removal, and a heterogeneous
habitat with a high perimeter-to-area ratio resulting in many sheltered, woody patches and open grass fields,
as preferred by C. nemoralis, could counteract a uniform decrease in condition along the urbanisation
gradient. Furthermore, we suggest future studies of ground beetle condition include the degree of park
management as an important factor in determining the effects of rural-urban gradients on ground beetles.
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Roskilde University
Seasonal activity of three common Danish ground beetles
(Coleoptera, Carabidae) along a rural-urban gradient
Abstract
The seasonal activity of three ground beetles (Coleoptera, Carabidae) Carabus nemoralis, Nebria brevicollis and Pterostichus melanarius
were studied along an urbanisation gradient over two consecutive years in Sorø, Denmark. Seasonal activity was studied, as it is
potentially a useful ground beetle characteristic to concentrate on, when responses to the effects of urbanisation on ground beetles are
being investigated.
Seasonal activities of the three beetles were considered in three habitats – rural, suburban and urban – using the
quartile method, whereby three cardinal dates were established describing the beetles’ main activity periods and peak activities.
Results indicated that main activity periods of beetles in suburban habitats generally started between ten days to
three months later than those observed in urban and rural habitats. We conclude that the seasonal activities of the three studied ground
beetles are affected by urbanisation, however source-sink dynamics may potentially play a role.
Resumé
Aktivitet over to sæsoner for tre løbebiller (Coleoptera, Carabidae) - Carabus nemoralis, Nebria brevicollis og Pterostichus melanarius - blev
undersøgt langs en urbaniseringsgradient ved Sorø. Sæsonaktivitet blev anvendt, da det er et træk ved løbebiller, som potentielt kan
bruges til at vise løbebillers respons på urbanisering. Med udgangspunkt i tre kardinaldatoer, som beskriver løbebillernes hoved- og
maksaktivitetsperioder, blev sæsonaktiviteten undersøgt i tre habitater – det rurale, suburbane og urbane.
Resultaterne viste, at løbebillernes hovedaktivitetsperioder i det suburbane habitat begyndte mellem ti dage og tre
måneder senere end de tilsvarende aktivitetsperioder i det urbane og rurale habitat. Vi konkluderer, at urbanisering påvirker
løbebillernes sæsonaktivitet, og formoder at source-sink-dynamikker også kan spille en rolle.
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Environmental Biology – module II
Introduction
The growth of towns and cities and the subsequent loss of rural/undeveloped land, otherwise known as
urbanisation, is a spatial and temporal event, which apparently knows few limits (McDonnell et al. 1997).
Urbanisation of large areas surrounding human settlement continues in many parts of the world associated
with an increase in human activities and human habitation and is generally accompanied by anthropogenic
alteration of the landscape (McDonnell & Pickett 1990).
The spatial array of anthropogenic effects of urbanisation can be investigated along ruralurban gradients (McDonnell & Pickett 1990), as too can these effects over temporal scales. Within the field of
biodiversity, several authors have conducted research into the effects of urbanisation on ground beetle
(Coleoptera, Carabidae) assemblages along rural-urban gradients at various locations around the world as part
of the Globenet project (Niemelä et al. 2000; Niemelä et al. 2002 and Venn et al. 2003). Generally results point
towards urbanisation having a negative effect on ground beetles as species diversity tends to decrease
towards urban habitats along urbanisation gradients (Niemelä et al. 2002; Venn et al. 2003 and Ishitani et al.
2003).
In Denmark ground beetle assemblages along a rural-urban gradient around the town of Sorø
have been investigated by Elek & Lövei (2005), where ground beetle diversity increased towards the centre
of the gradient, i.e. diversity was highest at urban sites, although least diversity was seen in suburban areas.
Studies so far have mostly considered the compositional changes along urbanisation
gradients (e.g. Niemelä et al. 2002; Venn et al. 2003 and Ishitani et al. 2003). However, there are several
additional, potentially useful responses of ground beetles that can indicate changes in habitat quality and
suitability. These can include changes in condition (Östman et al. 2001), activity (Werner & Raffa 2003) and
measures of fitness such as fluctuating asymmetry (Weller & Ganzhorn 2004). Here we chose the analysis of
seasonal activity of three common Danish ground beetle species.
Reasons for studying seasonal activity of these three species over a rural-urban gradient are
several fold. Urbanisation is a known cause of disturbance in ecosystems and can cause alterations of biotic
and abiotic variables in ecosystems (McDonnel et al. 1997). Ambient air temperature is known to be higher in
urban and suburban areas compared with rural areas outside cities, a result of the so-called heat island effect
(McKinney 2006). As ground beetle rhythms are regulated by temperature and photoperiod (Thiele 1977), an
effect on beetle activity is plausible. Urbanisation increases biological homogenization as synanthropic nonnative species are favoured over more specialised ones (McKinney 2006). Potentially this could influence the
distribution and quality of ground beetles’ food base in habitats along rural-urban gradients and since
differing food quality affects ground beetle behaviour (Syszko et al. 2004), one might expect to observe
differences in beetle activity along these gradients. These and other effects of urbanisation may have
concomitant effects on ground beetle seasonal activity.
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Roskilde University
At the spatial level along an urbanisation gradient there are potentially source-sink dynamics
at work, whereby individuals from productive areas emigrate to neighbouring and less productive habitats.
This in part depends on the dispersal abilities of species (Dunning et al. 1992). Beetle life history can also
exhibit regional and annual differences (Dülge 1994; Makarov 1994).
This study focused on the seasonal activity of three ground beetle species along an
urbanisation gradient in 2004 and 2005. The species are common to Denmark (Bangsholt 1983) and include
Carabus nemoralis (Müller, 1764), a spring breeder, Nebria brevicollis (Fabricus, 1792), an autumn breeder and
Pterostichus melanarius (Illiger, 1798), an autumn breeder. The ecologies of these ground beetles are similar in
that they are all eurytopic generalists found inhabiting diverse habitats such as forests, light woods, open
grasslands and areas of direct anthropogenic influence such as parks and gardens (Bangsholt 1983; Lindroth
1985). Habitats of this nature are found along urbanisation gradients such as the one in the present study.
Furthermore, to our knowledge, there has been relatively little written on the seasonal activity
of the above mentioned species in Denmark since the work of Jørum (1976, 1980). C. nemoralis (7% of total
catch (tc) in 2004; 6% of tc in 2005), N. brevicollis (11% of tc in 2004; 29% of tc in 2005) and P. melanarius (24%
of tc in 2004; 16% of tc in 2005) have been captured at each habitat along the same rural-urban gradient (Elek
& Lövei 2005; Elek & Lövei unpubl. ), where they appeared to be dominant species. This study was thus
conducted to acquire more detailed information the seasonal activity (both temporal and spatial) of C.
nemoralis, N. brevicollis and P. melanarius in Denmark and to investigate whether an urbanisation gradient has
an influence on the seasonal activities of the three beetles along a rural-urban gradient.
Material and methods
Beetles were collected along a rural-urban gradient in and around the town of Sorø, South Zealand,
Denmark. The gradient comprised three separate habitat types – urban, suburban and rural. The urban
habitat was located within the managed parkland of the Sorø Akademi, virtually in the town centre. Beetles
were caught within various forest/bush patches and corridors of vegetation in the park. Bordering one side
of the urban habitat is a lake and the level of built-up area was about 40%.
The suburban habitat lies nearby an intensively managed forest approximately one kilometre
from the urban locality. The suburban locality fringed several residential areas and the built-up surface was
approx. 20%. The suburban forest was mainly composed of beech (Fagus sylvatica) and hornbeam (Carpinus
betulus).
The forest habitat was found approx. 3 km from the town centre and was made up
predominantly of beech. The forest was under management. The entire rural-urban gradient stretched up to
6 km at the furthest study areas and the distance between gradient habitats was at least 1 km.
In each habitat, four sites separated by at least 50 m were selected for pitfall trapping. Each
site consisted of two sets of five traps. A distance of 10 metres separated individual traps, and the two
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Environmental Biology – module II
groups were further separated by min. 20 m between their external traps. This gave 120 traps in total (3
habitats, 4 sites/habitats, 10 traps/site).
In 2004, trapping was undertaken between the end of April and mid-October and traps were
emptied fortnightly. In total, the trapping effort was 2640 weeks (120 traps x 22 weeks). In 2005, the trapping
period was between the start of May and the beginning of October, but a pulsating trapping method was
employed i.e. sampling for only 2 weeks every month, traps being closed for the remainder of the month.
This was done after a study by Sapia et al. (in press) found that the same diversity ordering was obtained as
that observed from continuous sampling. This minimized unnecessary over-trapping of carabids and other
organisms. The total trapping effort was 1440 weeks (120 traps x 12 weeks).
Plastic cups with a diameter of 70 mm functioned as pitfall traps and were filled with approx.
200 ml of 70 % ethylene glycol, as a killing and preserving agent. Traps were sunk into the ground so that
their rims were flush with the ground surface. Traps were covered by a 20 cm2 galvanised iron cover, which
was mounted on pegs, about 5 cm from the soil surface. Covers ensured traps were not disturbed by the
elements, leaves, small mammals and birds, and at the same time prevented unwanted by-catch.
The traps were emptied into glass vials containing 70% ethanol and kept at 4ºC until sorting
and identification in the laboratory. Identification keys by Lindroth (1985, 1986) as well as a reference
collection kept at the Flakkebjerg Research Centre were used.
The collection of ground beetles in 2004 and 2005 in Sorø has served two purposes. Principally
the collection was part of a Globenet project investigating the diversity of ground beetle assemblages across
a rural-urban gradient in Sorø, Denmark (Elek & Lövei 2005), and also to collect bionomics data on ground
beetles in Denmark. The present study on seasonal activity in C. nemoralis, N. brevicollis and P. melanarius is
motivated by the second aim. The present authors also used this evaluation to identify candidate species for
more detailed studies (see other paper).
Study species
C. nemoralis is a eurytropic generalist species commonly found on all types of humus rich and moderately
dry soils e.g. light woods, parks, gardens, open and agricultural land (Lindroth 1985). C. nemoralis has the
broadest distribution amongst the genus Carabus in Denmark (Bangsholt 1983). It is brachypterous and a
spring breeder, reproducing in April-June, with summer larvae and new adults emerging in AugustSeptember (Bangsholt 1983; Lindroth 1985). C. nemoralis is a polyphagous predator, feeding on a wide
variety of insects; it eats fruit and bread (at least in captivity) (Larochelle 1990). In a previous study at the
same location, Elek & Lövei (2005) found large numbers of C. nemoralis along a rural-urban gradient.
Numbers decreased, however, from urban to rural sites in 2004, whereas highest numbers were found in
suburban sites in 2005.
N. brevicollis is a eurytopic woodland species, found predominantly in deciduous forest (often
beech) throughout much of Scandinavia. Being a generalist, it is also found in open country, parks and
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Roskilde University
gardens, where it seeks shaded areas (Lindroth 1985). N. brevicollis is widespread throughout Denmark
(Bangsholt 1983) and despite being macropterous it has limited dispersal abilities (Nelemans 1987). The
species is predatory and feeds mainly on insects (Larochelle 1990). According to Lindroth (1985) and Weller
& Ganzhorn (2003), N. brevicollis is an autumn breeder, with newly emerged and overwintering adults
occurring in spring. After emergence, N. brevicollis exhibits intense activity, building up fat reserves. After
this period the beetles enter a period of aestivation, where they aggregate under bark of tree stumps and logs
on the forest floor, etc (Lindroth 1985). In autumn, activity is resumed and breeding takes place. Larvae, at
different stages of development, and a number of adults hibernate through the winter (Lindroth 1985). N.
brevicollis is present at all sites along a rural-urban gradient in Sorø, but the largest numbers were found in
urban habitats (Elek & Lövei 2005).
P. melanarius is a eurytopic species, predominantly found in open grassland and meadows. It
often inhabits areas of anthropogenic influence, e.g. parks and gardens, but can also be found along forest
fringes and light woods (Lindroth 1986). The species is both very common and widespread throughout
Denmark (Bangsholt 1983). P. melanarius is an autumn breeder, with reproduction taking place around
August-September. The third instar larvae hibernate and adult beetles emerge, after completing
development, during the following spring and summer (Lindroth 1986). Beetles overwinter a second and
sometimes third winter as adults (Wallin 1985). Dimorphism in P. melanarius in Denmark was investigated
by Bangsholt (1983) who found that 99.5% of studied individuals were brachypterous, the remainder being
macropterous. P. melanarius is a mixed feeder acquiring its nourishment predominantly from insects, but
seed and plant material may also make up part of its diet (Larochelle 1990). Elek & Lövei (2005) reported
highest abundance of P. melanarius in urban sites, followed by forest sites with lowest numbers being
observed at suburban sites.
Seasonal Activity
Seasonal activity was described using the quartile method (Fazekas et al. 1997), whereby the cumulative
numbers of beetles caught were plotted against time and three cardinal dates were established from the
seasonal activity curves. Cardinal dates were established as dates when 25%, 50% and 75% of the cumulative
beetle catch was reached. The main activity period was the period between the 25% and 75% quartiles and
the activity peak was determined as the 50% quartile. The peak and main activity periods were divided into
three stages: early, mid and late. We compared seasonal activity from different habitats along the ruralurban gradient for each species using quantile-quantile plots (Cleveland 1994). These were called activity
comparison plots (ACP) for ease of notation.
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Environmental Biology – module II
Comparison of Cardinal Dates
In an attempt to compare cardinal dates for beetles captured in different habitats along the urbanisation
gradient, we transformed x-axes of seasonal activity figures (figures not shown) to ‘days after start of
sampling’. Each cardinal date (dates when 25%, 50% and 75% of the cumulative catch was reached) was
obtained as a number and we used Pearson and Spearman Rank correlation tests (SYSTAT-Version 11
software) in an attempt to evaluate whether cardinal dates from different habitats and years exhibited
similarity. This also served to investigate whether sampling over one year is sufficient for quantifying
seasonal activity of ground beetles.
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Roskilde University
Results
General Trends in Seasonal Activity
In the case of C. nemoralis the observed seasonal activity data conformed to that typical of a spring breeder,
and was seen in all habitats along the rural-urban gradient (Figure 1). In 2004 and 2005 an initial peak in
May – June corresponded to the reproduction period of overwintering adults. This was followed by a period
of lower activity before new adults emerged in late August.
C. nemoralis (2004)
C. nemoralis (2005)
50
Relative no. of
individuals, %
Relative no. of
individuals, %
50
40
30
20
10
0
40
30
20
10
0
15 29 43 57 74 88 102 116 130 141 158
14
Time, days since the start of the study
Relative no. of
individuals, %
Relative no. of
individuals, %
98
126
154
50
50
40
30
20
10
0
40
30
20
10
0
15 29 43 57 74 88 102 116 130 141 158
14
Time, days since the start of the study
30
20
10
0
57
74
88
102
116
130
Time, days since the start of the study
141
158
Relative no. of individuals, %
40
43
70
98
126
154
P. melanarius (2005)
50
29
45
Time, days since the start of the study
P. melanarius (2004)
Relative no. of individuals, %
70
N. brevicolis (2005)
N. brevicolis (2004)
15
45
Time, days since the start of the study
50
40
30
20
10
0
14
45
70
98
126
154
Time, days since the start of the study
Figure 1 Relative catches per sampling of C. nemoralis, N. brevicollis and P. melanarius. Years are kept
separately (11 sample dates in 2004, 6 sample dates in 2005). ◊ indicates urban, □ urban and ∆ rural
habitats. (14 & 15 = mid-May; 43 & 45 = mid-June; 70 & 74 = mid-July; 98 & 102= mid-August; 126 & 130 =
start and mid-September respectively; 154 & 158 = start October)
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Environmental Biology – module II
The seasonal activity figures for N. brevicollis resembled that of a spring breeder, despite it
being an autumn breeder (Figure 1). The initial peak in mid-June, however, was most likely due to the
emergence of new adults and overwintering adults from the previous year (Jørum 1976). Summer
aestivation was followed by increased activity from late August onwards corresponding with their
reproduction period. The patterns were apparent in all habitats, but less clear in 2005 due to non-continuous
sampling (Figure 1).
P. melanarius showed a seasonal activity pattern indicative of an autumn breeder. This pattern
was seen across the gradient, although the picture for 2005 was somewhat distorted. In 2005 there appeared
to be no period of aestivation over the summer.
Comparison of the cardinal dates of activity
Carabus nemoralis
A total of 723 C. nemoralis were caught in 2004 along the urbanisation gradient. It was the sixth most
abundant ground beetle caught (Elek & Lövei 2005). During the 2005 trapping campaign a total of 301 C.
nemoralis were collected in pitfall traps.
In 2004, the main adult activity period in the urban habitat started in late May and finished in
late August with an activity peak in the beginning of August (Table 1). This main activity period lasted
approx. 13.5 weeks. In the suburban habitat, the main activity period began approx. 10 days later, in early
June. The main activity period in the suburban habitat had a similar duration (14.5 weeks) to that of the
urban habitat, ending in mid-September, with peak activity in early July. A somewhat shorter activity period
was observed in the rural habitat (8.5 weeks), but commencement of the MAP was at a similar time (early
June) to suburban and urban habitats. Peak activity was observed in mid-June and the MAP in the rural
habitat ended in early August.
In 2005, beetles from the urban habitat had a main activity period lasting for 14 weeks from
late May to late August (Table 1). The peak activity was observed in late July. MAP in the suburban habitat
was similar in length to the urban habitat (13.5 weeks), but began in early June and finished in midSeptember with peak activity in mid-August. The main activity period in the rural habitat was from midMay until late June with a duration of 6 weeks. Peak activity was found in early June.
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Roskilde University
Table 1 Results of number of individual beetles caught, main activity period (MAP), MAP in weeks and peak activity along a rural-urban gradient
in 2004 and 2005 for C. nemoralis.
2004
Carabus nemoralis
No. of indiv. caught
Main activity period (MAP)
Length of MAP (wk)
Activity peak
2005
URB
SUB
RUR
URB
SUB
RUR
307
271
145
85
170
46
late V - late VIII
early VI - mid IX
early VI - early VIII
late V - late VIII
early VI - mid IX
mid V - late VI
13.5
14.5
8.5
14
13.5
6
start VIII
early VII
mid VI
late VII
mid VIII
early VI
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Environmental Biology – module II
Nebria brevicollis
During the 2004 collection period N. brevicollis was the third most abundant ground beetle caught in pitfall
traps along the rural-urban gradient (Elek & Lövei 2005). In 2005, a total of 1452 N. brevicollis were
recorded.
In 2004, the main activity period in the urban habitat started in early June and ceased 13
weeks later in early September (Table 2). The peak of activity was observed in mid-June. In the suburban
habitat N. brevicollis had a main activity period of ca. 4 weeks, which started in early September and ended in
October. Peak activity in the suburban habitat was seen in mid-September. The MAP in the rural habitat was
similar to that seen in the urban habitat, with commencement in early June, activity peak in mid-June and
end in mid-September. The duration of MAP in rural sites was longer (14.5 weeks) than the urban habitat.
In 2005, N. brevicollis in the urban habitat displayed a main activity period lasting 18 weeks
from mid-May until mid-September (Table 2). Peak activity fell in late August. The MAP in the suburban
habitat was confined to September, beginning in early September, finishing late September and with its peak
in mid-September (duration of 3 weeks). In rural sites, the main activity period started in late August, ceased
in late September and peak activity was observed in mid-September. Duration of the rural MAP was 4.5
weeks.
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Roskilde University
Table 2 Results of number of individual beetles caught, main activity period (MAP), MAP in weeks and peak activity along a rural-urban gradient
in 2004 and 2005 for N. brevicollis.
2004
Nebria brevicollis
No. of indiv. caught
Main activity period
(MAP)
Length of MAP (wk)
Activity peak
2005
URB
SUB
RUR
URB
SUB
RUR
846
115
173
891
302
259
early VI - early IX
early IX - early X
early VI - mid IX
mid V - mid IX
early IX - late IX
late VIII - late IX
13
4
14.5
18
3
4.5
mid VI
mid IX
mid VI
late VIII
mid IX
mid IX
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Environmental Biology – module II
Pterostichus melanarius
In 2004, a total of 2509 P. melanarius were caught and it was the next most abundant beetle caught along the
urbanisation gradient (Elek & Lövei 2005). Along the same gradient a total of 799 beetles were caught during
trapping in 2005.
In 2004, the main activity period in the urban habitat was observed from mid-July until midAugust, lasting approx. 4 weeks (Table 3). P. melanarius activity peaked in early August. The suburban
population of P. melanarius exhibited a main activity period spanning over 6 weeks from early July until
mid-August, with peak activity seen in early August. The MAP in the rural habitat was observed from midJuly until mid-August, lasting about 4 weeks. The peak activity fell in late July.
In 2005, peak activity in the urban population was observed in early July (Table 3). The main
activity period was from mid-June until late July (approx 6.5 weeks). In contrast, the MAP in suburban sites
began in late June and lasted 7 weeks until mid-August. The peak of activity was observed in late July. In the
rural habitat, peak activity was observed in early July, but a shorter MAP was found lasting 5 weeks from
late June until late July.
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Table 3 Results of number of individual beetles caught, main activity period (MAP), MAP in weeks and peak activity along a rural-urban gradient
in 2004 and 2005 for P. melanarius.
2004
2005
Pterostichus melanarius
URB
SUB
RUR
URB
SUB
RUR
No. of indiv. Caught
1780
98
631
471
53
275
mid VII - mid VIII
early VII - mid VIII
mid VII - mid VIII
mid VI - late VII
4
6
4
6.5
7
5
early VIII
early VIII
late VII
early VII
late VII
early VII
Main activity period
(MAP)
Length of MAP (wk)
Activity peak
late VI - mid VIII late VI - late VII
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Environmental Biology – module II
Comparison of activity in Urban vs. Suburban vs. Rural habitats
Figure 2 presents beetle seasonal activities in the form of several activity comparison plots (ACP). In each
figure, the activity of beetles captured in two different habitats along the urbanisation gradient over two
years are presented. A line of equality was added which could be used to evaluate, albeit roughly, similarity
of beetles’ seasonal trends between habitats. That is, the closer the lines from years lie to the line of equality,
the more similar were the activities of beetles in each habitat. Also, the distance between lines from different
years gave an impression of how similar/dissimilar beetle activities were between years.
Carabus nemoralis
Generally the main activity period began and finished later in the suburban habitat than in urban (2004 and
2005; Figure 2) and rural sites (2005, but not 2004; Figure 2). Peak activity in the rural habitat was observed
earlier than urban (2004 and 2005; Table 1) and suburban (2004 and 2005; Table 1) sites. The length of rural
MAP was shorter in duration compared with urban and suburban sites (2004 and 2005; Table 1). Lines in the
activity plot were most similar in the comparison of urban and suburban habitats (Figure 2). However, the
ACP for urban vs. rural (Figure 2) and suburban vs. rural (Figure 2) generally exhibited similarity, in that
they tended to have the same form.
Nebria brevicollis
The main activity period of N. brevicollis in the suburban habitat began and finished later compared with the
urban (2004 and 2005; Figure 2 and Table 2) and rural sites (2004 and 2005; Figure 2 and Table 2). This
general trend is seen as none of the activity comparison lines are observed on the suburban side of the line of
equality (Figure 2).
The main activity period of N. brevicollis caught in urban sites started and finished before that
observed in beetles caught in rural sites in 2004 and 2005 (Figure 2 and Table 2), while suburban beetles
exhibited a later peak activity than either urban and rural beetles. This was, however, not surprising
considering the late start to suburban beetle’s main activity period in 2004 and 2005 (Table 2 and Figure 2). In
2004 and 2005 the duration N. brevicollis MAP was shortest in suburban sites (Table 2).
Pterostichus melanarius
In 2004 the start of P. melanarius main activity period in suburban sites began just before that observed in
urban and rural habitats, but thereafter, cessation of MAP in all three habitats took place around the same
time (Figure 2 and Table 3). This is seen clearly in (Figure 2) where the activity comparison line for 2004
nears the line of equality after the 25% point. Peak activity in suburban beetles occurred later than that
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Roskilde University
observed in urban and rural habitats in 2004 (Figure 2), although rural peak activity was seen before the
urban peak activity (Figure 2).
In 2005 the main activity period in the suburban habitat started and finished after that seen in
both urban and rural habitats. This was also true for peak activities (Figure 2). Comparison of urban and
rural habitats revealed the start of main activity periods to occur first in the urban habitat, but peak activity
was observed at the same time (Figure 2 and Table 3).
In both 2004 and 2005 the MAP in suburban sites was longer than urban and rural sites (Table
3).
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Environmental Biology – module II
N. brevicolis (urban vs. suburban)
C. nemoralis (urban vs. suburban)
P. melanarius (urban vs. suburban)
100
100
100
Cumulative activity, %
Suburban habitat
75
75
50
50
25
25
0
0
0
25
50
75
100
0
25
50
Cumul ati ve acti vi ty, %
Cumul ati ve acti vi ty, %
Ur ban habi tat
Ur ban habi tat
75
75
50
25
0
100
0
25
50
75
100
Cumulative activity, %
Urban habitat
C. nemoralis (urban vs. rural)
P. melanarius ( urban vs. r ural)
N. brevicolis (urban vs. rural)
100
100
75
Cumulative activity, %
Rural habitat
Cumulative activity, %
Rural habitat
100
75
50
25
75
50
50
25
25
0
0
0
25
50
75
0
100
0
0
25
Cumulative activity, %
Urban habitat
50
75
25
50
75
100
100
Cumul ati ve acti vi ty, %
Ur ban habi tat
Cumulative activity, %
Urban habitat
C. nemoralis (suburban vs. rural)
P. melanarius (suburban vs. rural)
N. brevicolis (suburban vs. rural)
100
Cumulative activity, %
Rural habitat
50
25
100
Cumulative activity, %
Rural habitat
100
75
75
50
25
75
50
25
0
0
25
50
75
100
0
0
0
Cumul ati ve acti vi ty, %
Subur ban habi tat
25
50
Cumulative activity, %
Suburban habitat
75
100
0
25
50
75
100
Cumulative activity, %
Suburban habitat
Fig. 3. Activity comparison plots (APC) for C. nemoralis, N. brevicollis and P. melanarius in rural, suburban and urban habitats in 2004 (♦) and 2005
(□). The straight line indicates the line of equality. See text for explanation.
48
Roskilde University
Comparison of Cardinal dates
Correlations between cardinal dates from both years were performed in order to investigate similarity of
these dates. We recognise this method is not particularly accurate and it was intended to supplement the
ACP plots. Correlations between all cardinal dates (from all habitats) were positively correlated between
years 2004 and 2005 for all beetles (Table 4). This shows that the cardinal dates derived from 2004 and 2005
are significantly similar. Otherwise, only few results were significant. Most coefficients of correlation were
quite high, and although not significant, this does show there was a degree of similarity between cardinal
dates from both years- exceptions are, however, observed.
Table 2 Results from correlation tests of cardinal dates from different habitats and years. ‘All’ denotes
cardinal dates from each habitat along the rural-urban gradient (18 dates); ‘Urban’, ‘Suburban’ and ‘Rural’
indicates that cardinal dates only from individual habitats are correlated over the two years (3x2 = 6
dates); 25%, 50% and 75% indicate that only these cardinal dates from habitats were tested over years (2x3
= 6 dates); * denotes a significant correlation (p<0.05). All values are (r) coefficients of correlation
(Pearson’s) unless a p-value is presented (Spearman Rank).
Cardinal dates No of cardinal dates in test
C. nemoralis
N. brevicollis
P. melanarius
All
18
0.87*
0.87*
p<0.05*
Urban
6
1.00*
0.98
0.68
Suburban
6
0.88
0.95
0.99*
Rural
6
0.92
0.97
0.82
25%
6
0.66
-1.00*
0.59
50%
6
0.00
0.71
0.63
75%
6
0.96
0.87
p<0.05*
49
Environmental biology – module II
Discussion
The simplest classification of ground beetle phenology is as either spring or autumn breeders after Larsson
(1939). Generally spring breeders reproduce in spring or early summer before becoming inactive during the
height of summer. Spring breeders have summer larvae, which are active during the summer period. Newly
developed adults emerge in autumn and overwinter as adults (Lindroth 1985). Autumn breeders, on the
other hand, reproduce in the autumn and overwinter as larvae. The new generation of adults is often not
found before June and their peak abundance is usually in the middle of summer (Lindroth 1985).
Results obtained in the present study show that the main activity period of C. nemoralis
started earlier than P. melanarius and N. brevicollis. In Figure 1 it is seen that already in the first sampling
interval high relative numbers of individuals were observed, this being most noticeable in 2005 for urban
and rural habitats (Figure 1). This confirms C. nemoralis spring breeding nature, as autumn breeders are
usually first seen later in spring/early summer.
An interesting result is seen for N. brevicollis in the urban habitat (2005), where approx. 30% of
the relative catch was trapped in the first sampling period. This result is quite different compared with the
results from the beginning of the trapping effort in all other sites across the urbanisation gradient, which
otherwise agree with N. brevicollis being an autumn breeder. Numbers of N. brevicollis caught in the urban
habitat are very high in comparison with other habitats (2004 and 2005; Table 2) and this suggests the urban
habitat is a preferred site by N. brevicollis. We would expect to see the seasonal activity curve for N. brevicollis
drop off abruptly in the late October/early November had the sampling effort been extended. This would
most likely have resulted in a seasonal activity curve reminiscent of that for N. brevicollis reported by Jørum
(1976).
Our results for seasonal activity of P. melanarius are in agreement with Jørum (1976), who
reported an initial increase of activity in late April – early May with peak activity in August. This is
particularly evident in data from 2004, whereas in 2005 P. melanarius peak activity is up to a month earlier in
urban and rural habitats. In 2005 P. melanarius appeared not to undergo a period of summer aestivation. This
is not unheard of, as many ground beetles exhibit lower activity over summer without them necessarily
being dormant (G. Lövei, pers. comm.).
Comparison of seasonal activity periods for the three ground beetles in different habitats
revealed a common pattern. The main activity periods of C. nemoralis, N. brevicollis and P. melanarius in
suburban habitats were generally observed to commence later in the season compared with beetle activities
from urban and rural habitats. C. nemoralis main activity period began up to ca. twenty days later in the
suburban habitat compared with urban and rural sites in both years. The main activity period also ended
later in the suburban habitat. N. brevicollis exhibited the same pattern, although the delay in suburban areas
was more pronounced. Commencement of the main activity period in N. brevicollis from suburban sites took
place at least three months later than urban and rural MAPs in 2004 and 2005. P. melanarius from the
50
Roskilde University
suburban habitat had a later start of up to ten days and end to its main activity period in 2005 compared
with urban and rural habitats. This was not true in 2004, where P. melanarius main activity period in the
suburban habitat started ca. ten days earlier and finished at roughly the same time as beetles from urban and
rural habitats.
Rural and urban habitats did not show clear patterns with regards to start and end times of
main activity periods for the three beetles.
Makarov (1994) mentioned, that different catch dynamics and times of oviposition in female
P. melanarius and Pterostichus niger, caught in different forest types, were due to biotopic peculiarities of each
habitat. Differences in reproduction phenologies in Loricera pilicornis were observed over two years, which
was suggested to be due to different weather conditions between years (Makarov 1994). Thomas et al. (1998)
found that periods of activity in P. melanarius were higher immediately after rainfall and ground beetle
rhythms are also known to be regulated by temperature (Thiele 1977) and (Honek 1997) has reported
temperature related affects of seasonal activity in ground beetles. It is possible that we observed temperature
related affects on the seasonal activities of the three investigated beetles. Ambient temperatures tend to
increase along urbanisation gradients, with higher temperatures measured in suburban and urban habitats
than outlying rural areas (McKinney 2006). Our results indicate, however, that suburban beetles’ activity
lags behind beetles from urban and rural habitats. Ground beetles rely on a certain ambient temperature in
order to begin foraging after winter hibernation (S.A. Nielsen suggests ca. 7º C in Denmark, pers. comm.).
Habitats in our study are at most 6 km from each other and thus, it does not seem plausible that large
temperature differences played a role in delaying main activity periods in the suburban habitat only. Local
microclimatic differences, on the other hand, could play a role, especially at the micro-habitat scale. It should
be noted, that we did not investigate temperature development along the rural-urban gradient. In another
study by the present authors (see other paper), we found no difference between soil moisture in habitats
along the rural-urban gradient. We can only say, that there could potentially be microclimatic differences in
habitats, which affect the seasonal activities of beetles.
The present authors, in another study, found significantly less prey amounts in the suburban
habitat compared to the urban habitat (see other paper). Peak activity in ground beetles has been shown to
coincide with prey availability in and around a cabbage field (Suenaga & Hamamura 2001) and prey
availability is known to affect ground beetle behaviour (Syszko et al. 2004). McKinney (2006) has mentioned,
that urbanisation increases biological homogenization. Therefore, urbanisation has the potential to influence
the abundance and distribution of ground beetle prey, which in turn could affect seasonal dynamics of
ground beetles. Although we did not investigate prey abundance in 2004 and 2005, the pattern of a later start
to beetles’ main activity periods in suburban habitats may point towards an affect of limited prey on
seasonal activity in ground beetles. For N. brevicollis and P. melanarius, whose larvae overwinter and feed
during the spring, limited prey could delay pupation and thereby the activity of adult beetles. This may be a
problem for P. melanarius, which is predominantly brachypterous in Denmark (Bangsholt 1983) and whose
51
Environmental biology – module II
dispersal ability relies on the locomotory facilities of its legs. The problem with this statement is, however,
that in 2004 the main activity period of P. melanarius in the suburban habitat began ca. ten days earlier than
urban and rural habitats. However, the number of caught P. melanarius was also much less in suburban sites,
in both years, compared to urban and rural habitats.
N. brevicollis is macropterous, but has limited dispersal abilities and produces functional
wings only when larvae experience adequate food supplies during their development (Nelemans 1987). C.
nemoralis and P. melanarius are both brachypterous (Bangsholt 1983). We report an abundance of N. brevicollis
in suburban habitats (Table 2). In fact, greater numbers were observed in 2005, when pulsed capturing was
employed, than in 2004, and higher numbers were found in suburban contra rural sites in 2005. Also
numbers of C. nemoralis are highest in suburban sites in 2005 and relatively high in 2004 (Table 1). Therefore,
conditions in the suburban habitat must fulfil some requirements of N. brevicollis and C. nemoralis life cycles
and an explanation to the later activity should be sought elsewhere. An alternative could be a case of sourcesink dynamics (Dunning et al. 1992), whereby N. brevicollis and C. nemoralis from neighbouring and more
productive habitats (urban) emigrate to the suburban habitat during the season. This is then revealed as a
later start to the main activity period in the suburban habitat. Again we are not able to definitively conclude
that that source-sink dynamics are involved based on the experiments set-up. Further studies involving
capture-recapture methods would be necessary to illuminate such a hypothesis.
Variations in activity periods in ground beetles caught from different habitats along the
urbanisation gradient suggest that local populations are exposed to differing environmental conditions. It
would appear these different factors influence beetles in suburban sites greatest, which we have observed as
a later start to beetle main activity periods. The present study concludes that urbanisation has a variety of
effects, which concomitantly influence seasonal activity of C. nemoralis, N. brevicollis and P. melanarius. These
effects can be abiotic in nature (e.g. temperature and moisture), or biotic (e.g. prey availability). There is no
doubt, however, that the seasonal activities of the three investigated beetles differ between habitats along the
urbanisation gradient in Sorø. We recommend future studies of seasonal activities along urbanisation
gradients incorporate investigations of both biotic and abiotic factors, where appropriate. This would
contribute to a more descriptive picture of the factors affecting ground beetles in different habitats along
rural-urban gradients.
In addition, results from correlations of all cardinal dates along the urbanisation gradient
from 2004 and 2005 revealed significant correlations. In that similarity of cardinal dates from both years was
relatively high, a one year study should be adequate for investigating effects of urbanisation on ground
beetle seasonal activities. This agrees somewhat with Werner & Raffa (2003), who reported a one year study
to be sufficient to provide a general overview of trends in adult ground beetles activity period.
52
Roskilde University
Acknowledements
This paper underwent the constructive scrutiny of Gabor Lövei, to whom we are deeply indebted. Not only
for constructive criticism, but also for guidance. A special thanks to Zoltan Elek (and G. Lövei) for the use of
their data on ground beetles from Sorø, upon which this paper is based.
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Environmental biology – module II
References
Gabor L. Lövei
Department of Crop Protection, Danish Institute of Agricultural Science, Flakkebjerg Research Centre, DK4200, Slagelse, Denmark.
Søren Achim Nielsen
Department of Life Sciences and Chemistry, Roskilde University, DK-4000 Roskilde, Denmark.
Introduction
Alaruikka, D, Kotze, JD, Matveinen, K & Niemelä, J (2002): “Carabid beetle and spider assemblages along a
forested urban-rural gradient in southern Finland”, Journal of Insect Conservation 6: pp. 195206.
Bangsholt, F. (1983): ”Sandspringernes og løbebillernes udbredelse og forekomst i Danmark ca. 1830
1981”, Scandinavian Science Press Ltd., Denmark. ISBN: 87-87491-11-7.
Barone, M & Frank, T (2003): “Habitat age increases reproduction and nutritional condition in a generalist
arthropod predator”, Oecologia 135: pp. 78-83.
Blake, S, Foster, GN, Eyre, MD & Luff, MD (1994): “Effects of habitat type and grassland management
practices on the body size distribution of carabid beetles”, Pedobiologia 38: pp. 502-512.
Bommarco, R (1998): “Reproduction and energy reserves of a predatory carabid beetle relative to
agroecosystem complexity”, Ecological Applications 8 (3): pp. 846-853.
Braun, SD, Jones, TH & Perner, J (2004): “Shifting average body size during regeneration after pollution – a
case study using ground beetle assemblages”, Ecological Entomology 29: pp. 543-554.
Carignan, V & Villard, MA (2001): “Selecting indicator species to monitor ecological integrity: a review”,
Environmental Monitoring and Assessment 78: pp. 45-61.
Dülge, R. (1994): “Seasonal activity of carabid beetles in wooded habitats in northwest German (Coleoptera,
Carabidae)”. In Desender, K., Dufrêne, Loreau, M., Luff, M.L., Maelfait, J-P. (eds.): “Carabid
Beetles, Ecology and Evolution”: pp. 125-131, Kluver Academic Publishers, Dordrecht, The
Netherlands.
Elek, Z & Lövei, G (2005): “Ground beetle (Coleoptera, Carabidae) assemblages along an urbanization
gradient near Sorø, Zealand, Denmark”, Entomologiske Meddelelser 73 (2): pp. 115-121.
French, BW & Elliot, NC (1999): “Spatial and temporal distribution of ground beetle (Coleoptera: Carabidae)
assemblages in riparian strips and adjacent wheat fields”, Community and Ecosystem
Ecology 28 (4): pp. 597-607.
54
Roskilde University
Gaublomme, E, Dhuyvetter, H, Verdyck, P & Desender, K (2005): “Effects of urbanisation on carabid beetles
in old beech forests”, European Carabidology 2003, Proceedings of the 11th European
Carabidologist Meeting, DIAS Report, No. 114: pp. 111-123.
Gray, JS (1989): “Effects of environmental stress on species rich assemblages”, Biological Journal of the
Linnean Society 37: pp. 19-32.
Honek, A (1997): “The effect of temperature on the activity of carabidae (Coleoptera) in a fallow field”,
European Journal of Entomology 94: pp. 97-104.
Ishitani, M, Kotze, DJ & Niemelä, J (2003): “Changes in carabid beetle assemblages across an urban-rural
gradient in Japan”, Ecography 26: pp. 481-489.
Juliano, SA (1986): “Food limitation of reproduction and survival for populations of Brachinus (Coleopera:
Carabidae)”, Ecology 67 (4): pp. 1036-1045.
Kotze, DJ & O’Hara, RB (2003): “Species decline – but why? Explanations of carabid beetle (Coleoptera,
Carabidae) declines in Europe”, Oecologia 135: pp. 138-148.
Lindroth, C.H. (1985): “The Carabidae (Coleoptera) of Fennoscandia and Denmark”, Fauna Entomologica
Scandinavica, Vol. 15, part 1. EJ Brill, Leiden, The Netherlands.
Lindroth, C.H. (1986): “The Carabidae (Coleoptera) of Fennoscandia and Denmark (Part 2)”, Scandinavian
Science Press Ltd., Denmark. ISBN: 900408182.8
Loreau, M (1992): ”Species abundance patterns and the structure of ground-beetle communities”, Ann. Zool.
Finnici 28: pp. 49-56.
Larochelle, A. (1990): “The food of carabid beetles (Coleoptera, Carabidae, including Cicindelinae)”,
Fabreries, Suppl. No. F, pp. 132.
Lövei, GL & Sunderland, KD (1996): “Ecology and behaviour of ground beetles (Coleoptera: Carabidae)”,
Annual Review of Entomology 41: pp. 231-56.
Magura, T, Tóthmérész, B & Molnár, T (2004): “Changes in carabid assemblages along an urbanization
gradient in the city of Debrecen, Hungary”, Landscape Ecology 19: pp. 747-759.
Makarov, K.V. (1994): “Annual reproduction rhythms of ground beetles: a new approach to the old
problem”. In Desender, K., Dufrêne, Loreau, M., Luff, M.L., Maelfait, J-P. (eds.): Carabid
Beetles: Ecology and Evolution: pp. 177-182, Kluver Academic Publishers, Dordrecht, The
Netherlands. ISBN: 0-7923-2464-1
McDonnel, MJ, Pickett, STA, Pouyat, RV, Parmelee, RW, Carreiro, MM & Medley, K (1997): “Ecosystem
processes along an urban-to-rural gradient”, Urban Ecosystems 1: pp. 21-36.
McIntyre, NE (2000): “Ecology of urban arthropods: a review and a call to action”, Ecology and Population
Biology 93 (4): pp. 825-835.
McIntyre, NE, Rango, J, Fagan, WF & Faeth, SH (2001): “Ground arthropod community in a heterogeneous
urban environment”, Landscape and Urban Planning 52, pp. 257-274.
55
Environmental biology – module II
McGeoch, MA (1998): “The selection, testing and application of terrestrial insects as bioindicators”,
Biological Revue 73: pp. 181-201.
McKinney, ML (2006): “Urbanisation as a major cause of biotic homogenization”, Biological Conservation
127: pp. 247-260.
Niemelä, J (1993): “Interspecific competition in ground-beetle assemblages (Carabidae): what have we
learned?”, Oikos 66 (2): pp. 325-335.
Niemelä, J, Kotze, DJ, Ashworth, A, Brandmayr, P, Desender, K, New, T, Penev, L, Samways, M & Spence,
J (2000): “The search for common anthropogenic impacts on biodiversity: a global network”,
Journal of Insect Conservation 4: pp. 3-9.
Niemelä, J, Kotze, DJ, Venn, S, Penev, L, Stoyanov, I, Spence, J, Hartley, D & Montes de Oca, (2002):
”Carabid beetle assemblages (Coleoptera, Carabidae) across urban-rural gradients: an
international comparison”, Landscape Ecology 17: pp. 387-401.
Pouyat, RV, McDonnel, MJ & Pickett, STA (1997): “Litter decomposition and nitrogen mineralization in oak
stands along an urban-rural land use gradient”, Urban Ecosystems 1: pp. 117-131.
Rainio, J & Niemelä, J (2003): “Ground beetles (Coleoptera: Carabidae) as bioindicators”, Biodiversity and
Conservation 12: pp. 487-506.
Ribera, I, Dolédec, S, Downie, IS & Forster, GN (2001): “Effect of land disturbance and stress on species traits
of ground beetle assemblages”, Ecology 82 (4): pp. 1112-1129.
Samways, MJ (2005): “Insect Diversity Conservation”, Cambridge Univ. Press, United Kingdom.
Sota, T, Takami, Y, Kubota, K, Ujiie, M & Ishikawa, R (2000): “Interspecific body size differentiation in
species assemblages of the carabid subgenus Ohomopterus in Japan”, Population Ecology 42:
pp. 279-291.
Statistics Denmark (2006): “Statistisk Årbog”, Danmarks Statistik, Copenhagen, Denmark.
Statistics Denmark (1902): ”Statistisk Årbog”, Statens Statistiske Bureau, Copenhagen, Denmark.
Thiele, HU (1977): “Carabid beetles in their environments”, Springer-Verlag, Berlin/Heidelberg, Germany.
Thomas, CFG, Parkinson, L, Marshall, EJP (1998): “Isolating the components of activity-density for the
carabid beelte Pterostichus melanarius in farmland”, Oecologia 116: pp. 103-112.
Venn, SJ, Kotze, DJ & Niemelä, J (2003): “Urbanisation effects on carabid diversity in boreal forests”,
European Journal of Entomology 100: pp. 73-80.
Wallin, H (1985): “Spatial and temporal distribution of some abundant carabid beetles in cereal fields and
adjacent habitats”, Pedobiologia 28:pp. 19-34.
Wallin, H & Ekbom, BS (1994): “Influence of hunger level and prey densities on movement patterns in three
pecies of Pterostichus beetles (Coleoptera: Carabidae)”, Environmental Entomology 23: p. 1171
181.
Weller, B & Ganzhorn, JU (2004): “Carabid beetle community composition, body size, and fluctuating
asymmetry along an urban-rural gradient”, Basic and Applied Ecology 5: pp. 193-201.
56
Roskilde University
Werner, SM & Raffa, KF (2003): “Seasonal activity of adult, ground-occurring beetles (Coleoptera) in
forests of North-eastern Wisconsin and the upper Peninsula of Michigan. American Midland
Naturalist 149: pp. 121-133.
Östman, Ö, Ekbom, B, Bengtson, J & Weibull, A (2001): “Landscape complexity and farming practice
influence the condition of polyphagous carabid beetles”, Ecological Applications 11 (2): pp.
480-488.
Östman, Ö (2005): “Asynchronous temporal variation among sites in condition in two carabid species”,
Ecological Entomology 30: pp. 63-69.
57
Environmental biology – module II
Condition article
Barone, M & Frank, T (2003): “Habitat age increases reproduction and nutritional condition in a generalist
arthropod predator”, Oecologia 135: pp. 78-83.
Bangsholt, F. (1983): ”Sandspringernes og løbebillernes udbredelse og forekomst i Danmark ca. 1830
1981”, Scandinavian Science Press Ltd., Denmark. ISBN: 87-87491-11-7.
Blake, S, Foster, GN, Eyre, MD & Luff, MD (1994): “Effects of habitat type and grassland management
practices on the body size distribution of carabid beetles”, Pedobiologia 38: pp. 502-512.
Bommarco, R (1998): “Reproduction and energy reserves of a predatory carabid beetle relative to
agroecosystem complexity”, Ecological Applications 8 (3): pp. 846-853.
Elek, Z & Lövei., G (2005): “Ground beetle (Coleoptera, Carabidae) assemblages along an urbanization
gradient near Sorø, Zealand, Denmark”, Entomologiske Meddelelser 73 (2): pp. 115-121.
Ernsting, G & Isaaks, A (1997): “Effects of temperature and season on egg size, hatchling size and adult size
in Notiophilus biguttatus”, Ecological Entomology 22: pp 32-40.
Ishitani, M, Kotze, DJ & Niemelä, J (2003): “Changes in carabid beetle assemblages across an urban-rural
gradient in Japan”, Ecography 26: pp. 481-489.
Juliano, S (1986): “Food Limitation of Reproduction and Survival for Populations of Brachinus (Coleoptera:
Carabidae)”, Ecology 67 (4): pp. 1036-1045.
Gaublomme, E, Dhuyvetter, H, Verdyck, P & Desender, K (2005): “Effects of urbanization on carabid beetles
in old beech forests”, European Carabidology 2003, Proceedings of the 11th European Carabidologist
Meeting, DIAS Report, No. 114 : pp. 111-123.
Lindroth, CH (1985): “The Carabidae (Coleoptera) of Fennoscandia and Denmark”, Fauna Entomologica
Scandinavica 15, part 1, E.J. Brill, Leiden, The Netherlands.
Lövei, GL & Sunderland, KD (1996): “Ecology and Behavior of Ground Beetles (Coleoptera: Carabidae)”,
Annual Review of Entomology 41: pp. 231-56.
Niemelä, J, Kotze, DJ, Ashworth, A, Brandmayr, P, Desender, K, New, T, Penev, L, Samways, M & Spence, J
(2000): “The search for common anthropogenic impacts on biodiversity: a global network“, Journal of
Insect Conservation 4: pp. 3-9.
McDonnel, MJ, Pickett, STA, Pouyat, RV, Parmelee, RW, Carreiro, MM & Medley, K (1997): “Ecosystem
processes along an urban-to-rural gradient”, Urban Ecosystems 1: pp. 21-36.
McIntyre, NE (2000): “Ecology of Urban Arthropods: A Review and a Call to Action”, Ecology and
Population Biology 93 (4): pp. 825-835.
McIntyre, NE, Rango, J, Fagan, WF & Faeth, SH (2001): “Ground arthropod community in a heterogeneous
urban environment”, Landscape and Urban Planning 52: pp. 257-274.
Magura, T, Tóthmérész, B & Lövei, GL (in press): “Body size inequality along an urbanization gradient”,
58
Roskilde University
Basic and Applied Ecology.
Magura, T, Tóthmérész, B & Molnár, T (2004): “Changes in carabid assemblages along an urbanization
gradient in the city of Debrecen, Hungary”, Landscape Ecology 19: pp. 747-759.
Rainio, J & Niemelä, J (2003): “Ground Beetles (Coleoptera: Carabidae) as Bioindicators”, Biodiversity and
Conservation 12: pp. 487-506.
Ribera, I, Dolédec, S, Downie, IS & Forster, GN (2001): “Effect of land disturbance and stress on species traits
of ground beetle assemblages”, Ecology 82 (4): pp. 1112-1129.
Sota, T, Takami, Y, Kubota, K, Ujiie, M & Ishikawa, R (2000): “Interspecific body size differentiation in
species assembleges of the carabid subgenus Ohomopterus in Japan”, Population Ecology 42: pp. 279291.
Turin, H (2000): ”De Nederlandse loopkevers. Nederlandse Fauna 3”, Nat. Naturhistorisch Museum,
Leiden, The Netherlands.
Weller, B & Ganzhorn, JU (2004): “Carabid beetle community composition, body size, and fluctuating
asymmetry along an urban-rural gradient”, Basic and Applied Ecology 5: pp. 193-201.
Östman; Ö (2005): “Asynchronous temporal variation among sites in condition of two carabid
species”, Ecological Entomology 30: pp. 63-69.
Östman, Ö, Ekbom, B, Bengtson, J & Weibull, A (2001): “Landscape Complexity and Farming Practice
Influence the Condition of Polyphagous Carabid Beetles”, Ecological Applications 11 (2): pp.
480-488.
59
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Activity article
Bangsholt, F. (1983): ”Sandspringernes og løbebillernes udbredelse og forekomst i Danmark ca. 1830
1981”, Scandinavian Science Press Ltd., Denmark. ISBN: 87-87491-11-7.
Cleveland, W.C. (1994): “The elements of graphing data”, Hobart Press, USA. ISBN: 0963488414
Dülge, R. (1994): “Seasonal activity of carabid beetles in wooded habitats in northwest German (Coleoptera,
Carabidae)”. In Desender, K., Dufrêne, Loreau, M., Luff, M.L., Maelfait, J-P. (eds.): “Carabid
Beetles, Ecology and Evolution”, pp. 125-131, Kluver Academic Publishers, Dordrecht, The
Netherlands.
Dunning, J.B., Danielson, B.J. & Pulliam, H.R. (1992): “Ecological processes that affect populations in
complex landscapes”, Oikos 65 (1): pp. 169-175.
Elek, Z. & Lövei, G. (2005): “Ground beetle (Coleoptera, Carabidae) assemblages along an urbanisation
gradient near Sorø, Zealand, Denmark”, Entomologiske Meddelelser 73 (2): pp.115-121.
Fazekas, J., Kádár, F., Sárospataki, M. & Lövei, G.L. (1997): “Seasonal activity, age structure and
egg
production of the ground beetle Anisodactylus signatus (Coleoptera: Carabidae) in
Hungary”, European Journal of Entomology 94: pp. 473-484.
Honek, A. (1997): “The effect of temperature on the activity of Carabidae (Coleoptera) in a fallow field”,
European Journal of Entomology 94: pp. 97-104.
Ishitani, M., Kotze, D.J. & Niemelä, J. (2003): “Changes in carabid beetle assemblages across an urban
rural gradient in Japan”, Ecography 26: pp. 481-489.
Jørum, P. (1976): ”En undersøgelse af løbebillefaunaens sammensætning og sæsonaktivitet i en dansk
bøgeskov (Coleoptera, Carabidae). Entomologiske Meddelelser 44: pp. 81-99.
Jørum, P. (1980): “Life cycles and annual activity patterns of Pterostichus melanarius (Illig.) and P. niger
(Schall.) (Coleoptera:Carabidae) in a Danish beech wood”, Entomologiske Meddelelser 48:
pp. 19-25.
Larochelle, A. (1990): “The food of carabid beetles (Coleoptera, Carabidae, including Cicindelinae)”,
Fabreries, Suppl. No. F: pp. 132.
Larsson,
S.G.
(1939):
„Entwicklungstypen
und
Entwicklungszeiten
der
dänischen
Carabiden“,
Entomologiske Meddelelser 20: pp. 277-560
Lindroth, C.H. (1985): “The Carabidae (Coleoptera) of Fennoscandia and Denmark (Part 1)”, Scandinavian
Science Press Ltd., Denmark. ISBN: 9004077278
Lindroth, C.H. (1986): “The Carabidae (Coleoptera) of Fennoscandia and Denmark (Part 2)”, Scandinavian
Science Press Ltd., Denmark. ISBN: 900408182.8
60
Roskilde University
Makarov, K.V. (1994): “Annual reproduction rhythms of ground beetles: a new approach to the old
problem”. In Desender, K., Dufrêne, Loreau, M., Luff, M.L., Maelfait, J-P. (eds.): Carabid
Beetles: Ecology and Evolution: pp. 177-182, Kluver Academic Publishers, Dordrecht, The
Netherlands. ISBN: 0-7923-2464-1
McDonnell, M.J. & Pickett, S.T.A. (1990): “Ecosystem structure and function along urban-rural gradients: an
unexploited opportunity for ecology”, Ecology 71 (4): pp. 1232-1237.
McDonnell, M.J, Steward, T.A., Pickett, A., Groffman, P., Bohlen, P., Pouyat, R.V., Zipperer, W.C.,
Parmelee, R.W., Carreiro, M.M & Medley, K. (1997): “Ecosystem processes along an urban-to
rural gradient”,
Urban Ecosystems 1: pp. 21-36.
McKinney, M.L. (2006): “Urbanization as a major cause of biotic homogenisation”, Biological Conservation
127: pp. 246-260.
Neleman, M.N.E. (1987): ”Possibilities for flight in the carabid beetle Nebria brevicollis (F.). The importance
of food during larval growth”, Oecologia 72: pp. 502-509.
Nielsen, S.A. (2006): Associate professor, Department of Life Sciences and Chemistry, Roskilde University,
Denmark.
Niemalä, J., Kotze, J., Ashworth, A., Brandmayr, P., Desender, K., New, T., Penev, L., Samways, M. &
Spence, J. (2000): “The search for common anthropogenic impacts on biodiversity: a global
network”, Journal of Insect Conservation 4: pp. 3-9.
Niemelä, J., Kotze, J., Venn, S., Penev, L., Stoyanov, I., Spence, J., Hartley, D. & Enrique Montes de Oca
(2002): “Carabid beetle assemblages (Coleoptera, Carabidae) across urban-rural gradients:
an international comparison, Landscape Ecology 17: pp. 387-401.
Sapia, M., Lövei, G. & Elek, Z. (in press): “Effects of varying sampling effort on the observed diversity of
carabid (Coleoptera: Carabidae) assemblages in the Danglobe Project, Denmark”,
Entomologica Fennica.
Suenaga, H. & Hamamura, T. (2001): “Occurrence of carabid beetles (Coleoptera: Carabidae) in cabbage
fields and their possible impact on lepidopteran pests”, Applied Entomological Zoology 36:
pp. 151-160.
Syszko, J., Gryuntal, S. & Schwerk, A. (2004): “Differences in locomotory activity between male and female
Carabus hortensis (Coleoptera: Carabidae) in a pine forest and a beech forest in relation to
feeding state”, Environmental Entomology 33 (5): pp. 1442-1446.
Thiele, H-U. (1977): “Carabid Beetles in Their Environments”, Springer-Verlag, Berlin/Heidelberg: 369 pp.
Thomas, C.F.G., Parkinson, L. & Marshall, E.J.P. (1998): “Isolating the components of activity-density for the
carabid beetle Pterostichus melanarius in farmland”, Oecologia 116: pp. 103-112.
Venn, S.J., Kotze, D.J. & Niemelä, J. (2003): “Urbanization effects on carabid diversity in boreal forests”,
European Journal of Entomology 100: pp. 73-80.
61
Environmental biology – module II
Wallin, H. (1985): “Spatial and temporal distribution of some abundant carabid beetles in cereal fields and
adjacent habitats”, Pedobiologia 28: pp.19-34.
Weller, B. & Ganzhorn, J.U. (2004): “Carabid beetle community composition, body size, and fluctuating
asymmetry along an urban-rural gradient”, Basic and Applied Ecology 5: pp. 193-201.
Werner, S.M.& Raffa, K.F. (2003): “Seasonal activity of adult, ground-occurring beetles (Coleoptera) in
forests of northeastern Wisconsin and the Upper Peninsula of Michigan“, American Midland
Naturalist 149: pp. 121-133.
Östman, Ö., Ekbom, B., Bengtsson, J. & Weibull, A-C. (2001): “Landscape complexity and farming practice
influence the condition of polyphagous carabid beetles”, Ecological Applications 11: pp. 480
488.
62