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European Carabidology 2003. Proceedings of the 11th European Carabidologist Meeting
DIAS Report, No. 114 (2005), 99-109.
Food preferences and food value for the carabid beetles Pterostichus
melanarius, P. versicolor and Carabus nemoralis
Shams Fawki, Susanne Smerup Bak & Søren Toft
Department of Zoology
University of Aarhus
DK-8000 Århus C
Assuming generalist feeding habits to be the original condition in carabid beetles, we tested
two alternative hypotheses about the evolution of food specialisation: that species specialised
on prey that 1) were already of high quality to the generalists, or 2) were of low quality to the
generalists due to chemical or other defences. We did this by evaluating in laboratory
experiments the food quality to three generalist carnivore species of various prey types,
selected among those on which carabids are known to have specialised (i.e. insects,
earthworms, molluscs, seeds). The carabids used were adults of Pterostichus melanarius
Illiger, Pterostichus versicolor Sturm and Carabus nemoralis Mueller. Insects were high-
quality food, earthworms were intermediate, and slugs and seeds were low quality food for all
species. For C. nemoralis, earthworms were the most preferred prey. The results support the
second hypothesis, that food specialisation evolved by breaking the defences of low quality
but presumably abundant prey.
Key words: Coleoptera, Carabidae, ground beetles, diet, food specialisation
Carabid beetles are among the most common predatory invertebrates in agricultural fields and
are considered biocontrol agents of different pests. Therefore their habitats, biology, and
feeding ecology have been intensively studied. Carabid beetles are mostly polyphagous
feeders, which consume a variety of living or dead animal and plant material (Lövei &
Sunderland, 1996; Toft & Bilde, 2002). However, feeding specialisations have evolved in
several groups of carabid beetles (review in Toft & Bilde, 2002) including mollusc feeders
(Hengeveld 1980a,b), earthworm feeders (Symondson et al., 2000), seed feeders (Jørgensen
& Toft, 1997a,b), and specialist insect hunters (e.g. Bauer, 1981).
Some generalist carnivore carabids have extremely broad diets, feeding on insects,
earthworms and molluscs in varying proportions, but the benefits derived from each of these
components are not well known. In spite of this, e.g. some Carabus species have been
referred to as earthworm and mollusc specialists (Hengeveld, 1980 a,c). Earthworms have
been found in high frequencies in the stomach contents of some generalist carabid beetles
(Symondson, 1994). Also Abax parallelepipedus larvae can be reared on a pure earthworm
diet (Symondson, 1994). This might indicate that earthworms are high quality food for some
generalist species. Many carabid beetles consume varying amounts of plant material (Johnson
& Cameron, 1969; Goldschmidt & Toft, 1997), but the importance of seeds as component in
the diet of the generalist species is still unknown. Conflicting evidence exists on the role of
slugs for generalist carabid beetles: Symondson et al. (1996) and Bohan et al. (2000) claim a
high preference for slugs in some carabids, while Mair & Port (2001a,b) report the opposite
for related species.
The aim of the current study was to evaluate two alternative hypotheses about the evolution of
feeding specialisation in carabid beetles raised by Toft and Bilde (2002). The first one
suggests that the food types on which some carabids have specialised tend to be high quality
food for the generalist feeders. In contrast, the second hypothesis suggests that the specialist
feeders have specialised on food types that are generally of low quality to generalists due to
chemical or other defences. Our approach assumes that generalist feeding habits are the
original condition in carabid beetles (Lindroth, 1992; Lövei & Sunderland, 1996) and that
present generalists reflect this situation. Therefore we investigated the preferences and the
value of different food types as food for adults of the generalist species Pterostichus
melanarius Illiger, Pterostichus versicolor Sturm and Carabus nemoralis Mueller. The food
types tested were selected to represent those on which some groups of carabids have
specialised, i.e. insects, earthworms, slugs, snails and seeds. Adult Diptera and grasshoppers
were selected to represent the insects mainly because they are easily obtained from laboratory
cultures, but adult Diptera are also natural prey of several species (Sunderland, 1975; Kromp,
1999). The possibility exists that prey may be insufficient as the only food, but make a
positive contribution to predator fitness as part of a mixed diet. We therefore tested the
selected prey types both in pure and in mixed diets.
Materials and methods
Pterostichus versicolor, 8-12.5 mm in length, is a day-active beetle, breeding from April to
July. Larvae develop from May to September (Van Dijk, 1994). It is a polyphagous species
(Hengeveld, 1980 b; Bruinink, 1990), consuming Diptera, aphids, ants, and larvae of
Lepidoptera and Coleoptera (Bruinink, 1990).
Carabus nemoralis, 22-26 mm in length, is a nocturnal species breeding in April. In some
studies C. nemoralis and other Carabus species are referred to as generalist feeders (Digweed,
1994; Turin et al., 2003) while in others they are referred to as specialist feeders preferring
molluscs and earthworms (Ayre, 2001; Hengeveld, 1980a,c). Digweed (1994) demonstrated
that C. nemoralis was able to follow mucus trails of slugs (Deroceras reticulatum) and
earthworms. This might indicate a preference for such prey.
Pterostichus melanarius, 12-18 mm in length, is a nocturnal species breeding in August-
September. It is a highly polyphagous species (Davies, 1953; Pollet & Desender, 1985;
Lindroth, 1985/6). Pollet & Desender (1985) reported up to 49 different prey types (at family
level) as food for P. melanarius, including lumbricids, caterpillars and many other insect
groups, as well as plant material. It has been reported to preferentially feed on slugs and to
have a significant impact in slug control (Symondson et al., 1996; Bohan et al., 2000).
Food and prey preparation
The following prey types were used in the experiments: adult houseflies Musca domestica,
adult fruit flies Drosophila melanogaster, grasshoppers Locusta migratoria, earthworms,
mainly Lumbricus terrestris, slugs Deroceras reticulatum, snails Cepaea hortensis, and seeds
of Taraxacum sp. Fruit flies or houseflies were used as supposedly high-quality comparison
prey in all experiments, as they are highly preferred prey for many generalist predators (Pollet
& Desender, 1985; Bilde et al., 2000; Toft & Bilde, 2002).
Fruit flies and houseflies were obtained from laboratory cultures. Grasshoppers were bought
from a commercial supplier. Earthworms, slugs, snails and seeds were collected from the
field. All prey types used were freeze-killed, and earthworms, slugs and snails were cut into
small pieces, before being offered.
The three carabid species were collected in a field at Stjær near Århus, Denmark, between
April-July 2002. Beetles were kept in plastic boxes for 1-2 weeks under laboratory conditions
before the standardisation period started. Each box contained pieces of wet cotton, leaf litter
or wet tissue for shelter, and ad libitum dog food (Techni-Cal Maintenance®, Martin Group,
Canada). For P. melanarius, houseflies were added to minimise cannibalism.
All beetles underwent a 5-days nutritional standardisation procedure before starting the
experiments. During these five days beetles were placed individually in Petri dishes (14 cm
Ø) with a wet cotton wad. The first 2-3 days the beetles were supplied with food ad libitum:
P. versicolor was offered a diet of dog food and fruit flies; C. nemoralis a diet of dog food
and houseflies; and P. melanarius a mixed diet of all food types used in Experiment 3. Food
items were served in small dishes. The remaining 2-3 days the beetles were starved. P.
versicolor and C. nemoralis were kept at room temperature (20- 24ºC) and ambient
photoperiod about 16L: 8D. P. melanarius was kept in an incubator at 19ºC and a photoperiod
of 16L: 8D. Only female P. versicolor and P. melanarius were used, while for C. nemoralis
both males and females were used. In all experiments the species were kept under the same
temperature and light conditions as during the standardisation period.
Experiment 1: Egg production of P. versicolor
Egg production was measured over two weeks (May 2002) on four different diet groups (N =
number of replicates): fruit flies (N = 6), earthworms (N = 5), slugs (N = 6), and a mixed diet
of the three (N = 6). Prey was renewed every second day to provide ad libitum food supply.
During the egg production experiment the females were placed individually in Petri dishes
(14 cm Ø). Each dish was divided into two parts by a low barrier of silicone that allowed the
beetles to move freely in the dish. One half was filled with moist sand for egg laying. A small
glass dish (19 mm Ø) with food was placed in the other half. For egg counting, eggs were
sieved every 2-3 days through a 1.2 mm sieve using a gentle stream of tap water (Mols et al.
1981). Eggs were counted under the binocular microscope. Fresh, moist sand and food were
added to the breeding dishes at the same time before females were returned. Midway in the
experiment, males were added to every female, and removed after 6h. Each female was
weighed before and after the egg production experiment to determine the body mass change.
Experiment 2: 24-h food consumption measurements with C. nemoralis
In May 2002, beetles were divided randomly into four different diet groups: houseflies (N =
10), earthworms (N = 9), slugs (N = 9), and a mixture of the three (N = 6). In the pure diets
the amounts offered for each beetle were 25 houseflies, or 1.5 g of slugs or earthworms. The
amounts offered in the mixed diet were 10 flies and 0.7 g of both slugs and earthworms.
To determine the consumption during the 24-h (dry mass) prey samples were weighed before
being offered (wet mass) and multiplied by a previously established dry mass/wet mass
conversion factor to obtain the dry mass of food offered. Food remains were dried in the
vacuum oven at 60 ºC for at least 5 days and weighed. The 24-h dry mass consumption was
calculated by subtracting the amount of dried food remains from the calculated dry mass of
food offered at the beginning of the 24-h measurements. To determine the conversion factor
for each prey type, six samples of c. 0.6 g of slugs and earthworms and six samples of 10
houseflies were dried in the vacuum oven at 60 ºC for at least 5 days. Each beetle was
weighed before and after the 24-h to determine its mass change. All treatments were run
Experiment 3: 24-h food consumption measurements with P. melanarius
In July 2002, females were divided randomly into six different diet groups (N = 16 in all
treatments): houseflies, grasshoppers, earthworms, slugs, snails, and seeds. All treatments
were run simultaneously. Each female was offered 25 houseflies in the pure housefly diet.
Approximately the same wet mass of other food types was offered to other females in the
other pure diet groups. In the mixed diet group, each female was supplied with 10 houseflies,
and the other food types were given in approximately the same amounts by weight. The
procedure followed was the same as in Experiment 2. For the prey used in Experiment 2, their
dry mass/wet mass conversion factors were reused here. For the new food types, conversion
factors were established by weighing, drying and re-weighing, using 5 seed samples of c. 0.1
g and 5 samples of c. 0.5 g of snails and grasshoppers.
Homogeneity of variances was tested using Bartlett’s or Levene’s test before the method of
analysis was chosen. Data were homogenised with a square-root or a Box-Cox
transformation, and one-way ANOVA was applied, followed by post- hoc pair-wise
comparisons of treatments using Student’s t-test. A Welch ANOVA test was used when no
transformation was able to homogenise the group variances. Subsequent pair-wise
comparisons were made using Welch ANOVA or one-way ANOVA tests. Within each series,
the basic α-level of 0.05 was adjusted with the sequential Bonferroni technique (Rice, 1989).
Experiment 1: Egg production of P. versicolor
Overall differences in egg production were not fully significant between diets (one-way
ANOVA: F3,19=2.90, P=0.062). Number of eggs produced by beetles fed slugs was
significantly lower than by beetles fed other diets (Fig. 1A).
Beetles fed mixed and fruit fly diets had gained mass by the end of the experiment, while
beetles fed earthworms or slugs had lost mass (Fig. 1B). The beetle mass change was not
significantly different between diets (Welch ANOVA: F3=2.42, P=0.13). This was probably
due to low sample sizes.
Experiment 2: 24-h food consumption measurements for C. nemoralis
There was a significant overall difference in prey consumption between different diets (one-
way ANOVA: F3,30=5.91, P=0.0027). Earthworm consumption was significantly higher than
that of houseflies and slugs both in pure diets (Student’s t-test) and in the mixed diet (Welch
ANOVA: F2=7.42, P=0.013; Fig. 2A). Housefly consumption in the mixed diet treatment was
remarkably low (indiscernible in Fig. 2A). Mixed diet consumption did not differ significantly
from earthworm consumption, but was significantly higher than housefly and slug
Beetle mass change was significantly different between diets (Welch ANOVA: F3=18.0,
P<0.0001). Mass change of beetles fed slugs was significantly lower than that of beetles fed
houseflies, earthworms or mixed diet (Fig. 2B). Mass change of the beetles fed houseflies,
earthworms and mixed diet did not differ significantly from each other.
Experiment 3: 24-h food consumption measurements for P. melanarius
Consumption by adult beetles was significantly different between diets (Welch ANOVA:
F5=40.2, P<0.0001). Earthworm consumption was significantly higher than the consumption
of houseflies, grasshoppers, slugs, snails and seeds (Fig. 3A). Seed consumption was
significantly lower than the consumption of the insect diets, but did not differ significantly
from slug and snail consumption. Grasshopper consumption was significantly higher than that
of slugs, snails and seeds, but did not differ significantly from housefly consumption.
There was a significant overall difference in the beetle mass change between diets (Welch
ANOVA: F5=27.4, P<0.0001). Beetles fed insect diets gained more mass than beetles fed
slugs, snails and seeds, but not more than beetles fed earthworms. Beetles fed seeds lost mass,
and this was significantly different from the mass change in other diet groups.
No. of eggs
Fruit flies Earthworms Slugs Mixed
Beetle mass change (mg)
Housefli es Earthworms Slugs Mixed diet
Beetle mass change (mg)
Consumption (mg )
AHouseflies Earthworms Slugs
Figure 1. Egg production (total
number of eggs per females during
two weeks) (A) and mass change (B)
in females of Pterostichus versicolor
kept on different diet regimes under
laboratory conditions. Error bars
indicate one SE. Different letters
indicate significant (p<0.05)
difference among treatments.
Figure 2. Food consumption (mg dry
mass in 24 h) (A) and body mass
change (B) in Carabus nemoralis
adults under different diet regimes.
Error bars indicate one SE. Different
letters indicate significant difference
Figure 3. Food consumption (mg dry mass in 24 h) (A) and body mass change (B) in
females of P. melanarius under different diet regimes. Error bars indicate one SE.
Different letters indicate significant difference among treatments.
Experiment 1 indicated that fruit flies were of high food quality for P. versicolor. Thus,
beetles fed fruit flies both gained weight and maintained a high rate of egg production (Fig.
1). This agrees with previous findings on carabid beetles and other generalist predators (Bilde
& Toft 1994, 2002; Bilde et al., 2000). Slugs were low quality food for P. versicolor because
the beetles both lost weight and produced very few eggs. Mixing fruit flies with slugs and
earthworms did not improve fecundity of P. versicolor (Fig. 1A) and increased mass gain
only non-significantly (Fig. 1B).
Despite that the beetles fed earthworms lost mass, they produced as many eggs as those in the
fruit fly and mixed diet treatments (Fig. 1). This might indicate that P. versicolor is more
efficient at converting earthworms than slugs into own biomass or eggs and thus have a
higher nutritional value than the slugs. As consumption was not measured it cannot be
decided whether this was due to pre- or post-digestive effects. Due to the limited duration of
the experiment (2 weeks) these results may not fully reflect the possible long-term effects of
the dietary restrictions.
Beetle mass changne (mg)
In Experiment 2 earthworms were the highly preferred prey for C. nemoralis, supporting
Hengeveld (1980a) that C. nemoralis is to a large part an earthworm consumer. Lukasiewicz
(1996) reported that Carabus species selectively preyed on large and slowly moving epigean
invertebrates such as earthworms. Houseflies were the highest quality food for C. nemoralis
as the mass gain of the beetles was high in spite of the low consumption (Fig. 2). Slugs were
low quality food, as the mass gain of beetles fed slugs was significantly lower than that of
other diets (Fig. 2B). These results confirm that C. nemoralis is a generalist carnivore
consuming a variety of prey types as reported by several authors (Digweed, 1994; Larochelle,
1990; Turin et al., 2003).
Insect diets were also of high quality for P. melanarius, since the beetles were able to increase
in mass in spite of only intermediate feeding rates. The beetles had a high earthworm
consumption capacity (Fig. 3A), supporting Symondson et al. (2000) reporting that P.
melanarius consume many earthworms when other prey types are scarce. But they were not
as high quality food as insects, because the beetles gained less mass on a much higher
consumption rate. The positive gain in weight of beetles on slug and snail diets in spite of
low consumption rates indicate that their low food quality is due to pre- rather than post-
digestive effects. Seeds were low-quality food for P. melanarius as the low consumption rate
was insufficient for maintaining their body mass (Fig. 3B).
Diptera (houseflies or fruit flies) were high quality food for all species, while slugs and snails
were low quality and earthworms were intermediate quality. Seeds were low quality and
probably useless for P. melanarius. Our results regarding molluscs confirm the suggestion of
Mair & Port (2001a,b) that generalist carabids have low preference for slugs and may accept
only small or dead ones. These authors ascribed this to the deterrent effects of the mucus.
However, mucus was not a factor in our experiments, since the beetles were fed small pieces
of mollusc meat.
The results refute the hypothesis that food types eaten by specialist feeders are also high
quality food for generalists. For example, slugs were low quality food for all beetles and even
for C. nemoralis, which have been considered a mollusc specialist (Hengeveld, 1980a). The
generalist predators seemingly gained nothing from the inclusion of earthworms and slugs in
the mixed diets. The results indicate that specialist feeders have adapted to food types that are
protected against the generalist feeders. A related question is whether the specialists’
performance can be enhanced by a mixed diet that includes prey of high quality for
generalists. This is not always the case. Thus, addition of insects to the diet of the seed-eaters
Amara similata and Harpalus rufipes did not improve the performance of the beetles
(Jørgensen & Toft, 1997a,b).
We are deeply indebted to Else Bomholt Rasmussen for assistance in the laboratory and help
with collecting of prey animals; to David Mayntz for statistical assistance; to Gabor Lövei and
an anonymous reviewer for many valuable comments; and to Gabor Lövei for taking on the
full editorial responsibility for this paper.
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