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Food preferences and food value for the carabid beetles Pterostichus melanarius, P. versicolor and Carabus nemoralis


Abstract and Figures

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 highquality 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.
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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
Building 135
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
Study species
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.
Standardisation period
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.
Statistical analysis
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
among treatments.
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.
bd de
Beetle mass changne (mg)
Consumption (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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... The evolution of food specialization in carabid beetles is uncertain, though there is agreement that a generalist insectivorous or carnivorous feeding habit is the ancestral condition (Thiele, 1977;Hengeveld, 1981;Lindroth, 1992). Fawki et al. (2005) tested whether the preferred prey of specialist carabid guilds are high-or low-quality food for generalist species, and concluded that specialist carabids have specialized to consume food which is of low quality to generalist carabids but supposedly abundantly available. Among the specialized carabids are the seed-eating (granivorous) ones. ...
... The range of food types tested was chosen to cover those on which some carabid groups have specialized, i.e. insects, earthworms, molluscs (slugs and snails), and seeds were used as a control diet. Houseflies have been reported before as a high-quality food for the generalist carabid predators (Fawki et al., 2005). Earthworms are one of the most abundant types of soil invertebrates in Europe, and several carabid species have been reported to eat earthworms (Pollet and Desender, 1985;Symondson, 1994;Symondson et al., 2000;Fawki et al., 2005). ...
... Houseflies have been reported before as a high-quality food for the generalist carabid predators (Fawki et al., 2005). Earthworms are one of the most abundant types of soil invertebrates in Europe, and several carabid species have been reported to eat earthworms (Pollet and Desender, 1985;Symondson, 1994;Symondson et al., 2000;Fawki et al., 2005). ...
Several studies have shown that the mainly granivorous carabid beetles, e.g. Amara spp., include animal food in their diet to a considerable extent. We therefore hypothesized that the performance of these beetles would be enhanced by dietary mixing including both seeds and animal food. In order to test this, we conducted laboratory feeding experiments with adults and larvae of Amara similata. Both adults and larvae were subjected to different diet treatments including: seeds, houseflies, grasshoppers, earthworms, slugs and snails in pure and mixed diets. Larval survival, development time, pupal and teneral weights were used as indicators of food quality for the larvae. For the adult beetles, mass change was used as an indicator of food quality. We found seeds to be high-quality food, while all pure animal diets were of low quality for both adults and larvae. Animal foods added to the seed diet had both positive and negative effects. A mixed diet of all foods enhanced the mass gain of adults compared with the seed diet, but reduced larval performance dramatically. Earthworms and grasshoppers added to seeds increased the pupal and teneral weights, while reduced larval survival. Thus, A. similata is omnivorous with a mainly granivorous feeding habit. It may gain benefits on some fitness parameters and incur costs on others from preying or scavenging on animal food. Therefore, the overall fitness consequences of a mixed seed-animal diet are uncertain.
... This dichotomous grouping suggests that seeds are not primary to diets of omnivorous carabids and would be mostly consumed upon random encounter rather than carabids foraging for seeds specifically (Cardina et al., 1996;Lovei & Sunderland, 1996). Studies on seed-feeding habits have revealed that the distinction between omnivory and granivory in carabid species is ambiguous, however, as the two feeding habits often overlap (Fawki et al., 2003;Fawki & Toft, 2005). For example, some carabid species originally proposed to feed strictly on animal prey were found to also include considerable amounts of weed seeds in their diets (Carbonne et al., 2020). ...
... Setting out on foraging bouts is associated with different risks and entails high costs related to food handling and processing (Schoener, 1971;Pyke et al., 1977). Carabid weed seed predators in this sense need not only to find weed seeds, the chosen seed type or seed patch must also offer high rewards at a low cost (Fawki et al., 2003;Sih, 1984). Clearly, the balance between reward and cost of different seed types is likely a major factor shaping seed selection decisions (Bretagnolle et al., 2015;Brousseau et al., 2018). ...
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Species of carabid (ground) beetles are among the most important postdispersal weed seed predators in temperate arable lands. Field studies have shown that carabid beetles can remove upwards of 65%–90% of specific weed seeds shed in arable fields each year. Such data do not explain how and why carabid predators go after weed seeds, however. It remains to be proven that weed seed predation by carabids is a genuine ecological interaction driven by certain ecological factors or functional traits that determine interaction strength and power predation dynamics, bringing about therefore a natural regulation of weed populations. Along these lines, this review ties together the lines of evidence around weed seed predation by carabid predators. Chemoperception rather than vision seems to be the primary sensory mechanism guiding seed detection and seed selection decisions in carabid weed seed predators. Selection of weed seeds by carabid seed predators appears directed rather than random. Yet, the nature of the chemical cues mediating detection of different seed species and identification of the suitable seed type among them remains unknown. Selection of certain types of weed seeds cannot be predicted based on seed chemistry per se in all cases, however. Rather, seed selection decisions are ruled by sophisticated behavioral mechanisms comprising the assessment of both chemical and physical characteristics of the seed. The ultimate selection of certain weed seed types is determined by how the chemical and physical properties of the seed match with the functional traits of the predator in terms of seed handling ability. Seed density, in addition to chemical and physical seed traits, is also an important factor that is likely to shape seed selection decisions in carabid weed seed predators. Carabid responses to seed density are rather complex as they are influenced not only by seed numbers but also by trait‐based suitability ranks of the different seed types available in the environment. The study elucidates the possible mechanisms that bring weed seeds and carabid predators together, and then, it highlights the key ecological factors that determine strength and dynamics of seed predation interactions.
... Beyond that, seed feeding habits in omnivorous carabids would be opportunistic and tend to arise mostly when alternative foods are scarce or hard to obtain 8 . Seed feeding habits in carabids often transcend the artificial limits imposed by the dietary specialization reasoning (omnivory vs. granivory), as seeds are featured in the diets of a large number of carabid taxa 25,26 . This evidence suggests that seed feeding habits in carabid species have evolved due to yet unexplored biological needs not necessarily exclusive to granivorous carabids sensu stricto. ...
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Ground beetles (Coleoptera: Carabidae) are among the most prevalent biological agents in temperate agroecosystems. Numerous species function as omnivorous predators, feeding on both pests and weed seeds, yet the sensory ecology of seed perception in omnivorous carabids remains poorly understood. Here, we explore the sensory mechanisms of seed detection and discrimination in four species of omnivorous carabids: Poecilus corvus, Pterostichus melanarius, Harpalus amputatus, and Amara littoralis. Sensory manipulations and multiple-choice seed feeding bioassays showed olfactory perception of seed volatiles as the primary mechanism used by omnivorous carabids to detect and distinguish among seeds of Brassica napus, Sinapis arvensis, and Thlaspi arvense (Brassicaceae). Seed preferences differed among carabid species tested, but the choice of desirable seed species was generally guided by the olfactory perception of long chain hydrocarbons derived from the seed coat surface. These olfactory seed cues were essential for seed detection and discrimination processes to unfold. Disabling the olfactory appendages (antennae and palps) of carabid beetles by ablation left them unable to make accurate seed choices compared to intact beetles.
... We selected 32 species of carabids, which can be assigned by their main food resource to one of four feeding groups (Table 1): herbivores, generalist carnivores, collembolan specialists, and one genus (Carabus) of large carnivores (Fawki, Smerup Bak, & Toft, 2003;Freude, Harde, Lohse, & Klausnitzer, 2004;Hengeveld, 1980;Homburg, Homburg, Schäfer, Schuldt, & Assmann, 2014;Honek, Martinkova, & Jarosik, 2003;Turin, Penev, & Casale, 2003). To analyze the degree of convergent evolution within these groups, we include at least two species with different degrees of specialization to the same feeding group. ...
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Closely related species are often assumed to be functionally similar. Phylogenetic information is thus widely used to infer functional diversity and assembly of communities. In contrast, evolutionary processes generating functional similarity of phylogenetically distinct taxa are rarely addressed in this context. To investigate the impact of convergent evolution on functional diversity (FD) and phylogenetic diversity (PD), we reconstructed the phylogenetic structure of carabid trophic groups. We then analyzed the mandible shapes using geometric morphometrics to link specialization in functional morphology with feeding specialization among herbivores, generalist carnivores, and specialized consumers of Collembola. Our results show that carabid feeding groups are paraphyletic. Herbivory evolved at least twice and specialization to Collembola predation at least three times. Species within feeding groups share a remarkably similar mandible morphology, which evolved convergently. While specialized mandibles of herbivores and collembolan specialists represent an adaptation to their main food source, the particular mandible morphologies do not necessarily reflect the degree of food specialization within feeding groups. Only a few species with a specialized herbivorous mandible may occasionally feed on animals, but the range of specific food resources in generalist carnivore species is large, despite an almost identical mandible shape. Thus, convergent evolution in specialized feeding groups reverses the relationship between PD and functional similarity compared with generalist carnivores. We conclude that phylogenetic relationship is a poor proxy of FD in carabids. Moreover, the inconsistencies between relatedness, morphological adaptation, and ecological function require caution in the characterization of functional groups. Rather than assuming general relationships between PD and FD, we suggest integrating the analysis of evolutionary processes into functional community analyses.
... We used two methods to measure the trophic position of organisms within the food web: 1) an estimate based on dietary preferences of each species obtained from the literature (Roth and Lima, 2003;Roth et al., 2006;Estes and Mannan, 2003;Cava et al., 2012;Curtis et al., 2006b;Arcese et al., 2002;Cabe, 1993;Campbell et al., 1990;Eastman, 2000;Government of Canada, 2017;Holland, 2017;Judd, 1901;Lowther and Cink, 2006;Lowther and Johnston, 2014;Reynolds, 2017;Saul, 2010;Spennemann and Watson, 2017;Vanderhoff et al., 2014a;Wiebe and Moore, 2017;Beal, 1911;Beal, 1907;Fawki et al., 2003;Moulton, 2011;Wheelwright, 1986;White and Stiles, 1990;Witmer, 1996;Baumeister, 2002;Larochelle, 1990;Vanderhoff et al., 2014b;Currier et al., 2020) and 2) an estimate inferred from stable nitrogen isotope comparisons (Mackintosh et al., 2004;Vander Zanden et al., 1997). Based on the dietary preferences, the trophic position (TP) of each species was calculated according to Eq. (2) (Vander Zanden et al., 1997) ...
Legacy persistent organic pollutants (POPs), including organochlorine pesticides (OCPs), polychlorinated biphenyls (PCBs), and polybrominated diphenyl ethers (PBDEs), persist for generations in the environment and often negatively impact endocrine functions in exposed wildlife. Protocols to assess the bioaccumulation potential of these chemicals within terrestrial systems are far less developed than for aquatic systems. Consequently, regulatory agencies in Canada, the United States, and the European Union rely primarily on aquatic information for the bioaccumulation assessment of chemicals. However, studies have shown that some chemicals that are not bioaccumulative in aquatic food webs can biomagnify in terrestrial food webs. Thus, to better understand the bioaccumulative behaviour of chemicals in terrestrial systems, we examined trophic magnification of hydrophobic POPs in an urban terrestrial food web that included an avian apex predator, the Cooper's hawk (Accipiter cooperii). Over 100 samples were collected from various trophic levels of the food web including hawk eggs, songbirds, invertebrates, and berries and analysed for concentrations of 38 PCB congeners, 20 OCPs, 20 PBDE congeners, and 7 other brominated flame retardants listed on the Government of Canada's Chemicals Management Plan. We determined trophic magnification factors (TMFs) for contaminants that had a 50% or greater detection frequency in all biota samples and compared these terrestrial TMFs to those observed in aquatic systems. TMFs in this terrestrial food web ranged between 1.2 (0.21 SE) and 15 (4.0 SE), indicating that the majority of these POPs are biomagnifying. TMFs of the legacy POPs investigated in this terrestrial food web increased in a statistically significant relationship with both the logarithm of the octanol-air (log KOA) and octanal-water partition (log KOW) coefficients of the POPs. POPs with a log KOA >6 or a log KOW >5 exhibited biomagnification potential in this terrestrial food web.
... L'intérêt nutritif des limaces pour les Carabidae n'est pas encore complétement établi par la communauté scientifique. Selon certains auteurs, la consommation de limaces résulterait d'une spécialisation de certains Carabidae pour une proie abondante de faible qualité nutritive, qui a cependant nécessité des adaptations pour outrepasser les mécanismes de défense de ces dernières (Fawki et al., 2005). Certaines expérimentations de laboratoire montrent qu'en présence de proies alternatives, certaines espèces de Carabidae ne s'attaquent pas aux limaces (Oberholzer and Frank, 2003) ou font état de préférences pour des limaces mortes (Mair and Port, 2001) et notamment Pterostichus madidus, abondant dans notre site d'étude. ...
L’agroforesterie, et plus particulièrement les systèmes sylvo-arables, sont des systèmes peu étudiés qui présentent des intérêts agronomiques et environnementaux en systèmes tempérés. Les systèmes agroforestiers pourraient notamment fournir un microclimat favorable aux cultures maraîchères conduites en agriculture biologique en contexte pédoclimatique méditerranéen. Cependant, il existe encore peu de références scientifiques sur le sujet, et l’issue des interactions entre arbres et cultures sont encore me connues. En particulier, le microclimat généré par des arbres âgés est susceptible de modifier les relations entre cultures, bio agresseurs et pré dateurs généralistes, qui peuvent conditionner la performance d’une association agroforestière. Cette thèse avait donc comme objectifs :➢ D’évaluer l’impact de l’ouverture de la canopée sur la biodiversité et l’activité densite des coléoptères carabiques.➢ D’identifier comment le microclimat peut influencer les processus de régulation naturelle.Les systèmes agroforestiers se développent sur des temps longs (pluriannuels): l’étude s’est focalisée sur un système ayant déjà des arbres âgés de 20 ans pour en étudier l’impact sur le microclimat et la faune du sol. Pour faire varier ce microclimat, un gradient d’ouverture de la canopée a été réalisé. La température de l’air ambiant, l’hygrométrie et le pourcentage d’ouverture du milieu ont ensuite été mesurés.En premier lieu, la faune du sol a été échantillonnée durant 2 ans (non révolus), et les structures des communautés de Carabidae ont été analysées d’un point de vue taxonomique et fonctionnelle, au moyen de 5 traits écologiques. Les résultats montrent que la structure taxonomique est peu affectée, mais qu’à la fois l’activité-densité spécifique des espèces et les traits fonctionnels sont modifiés par le gradient d’ouverture du milieu. En particulier, la fermeture de la canopée du système agroforestier favorise les espèces ayant une affinité pour des milieux fermés et humides.L’activité journalière de deux prédateurs abondants a été caractérisée dans une période estivale chaude (juillet), et plus douce (septembre). Les résultats montrent qu’à la fois la saison mais également l’ouverture de la canopée peuvent modifier les rythmes journaliers de l’Arachnidae et du Carabidae les plus abondants à cette période (Pardosa hortensis, Pseudoophonus rufipes).Dans un troisième temps, le travail s’est focalisé sur le potentiel de prédation des prédateurs de la faune du sol, au moyen de cartes sentinelles de prédation à deux périodes estivales, juin et aout. Les résultats montrent que sur au moins une période, le potentiel de prédation sur larves de lépidoptères (Cydia pomonella) est différent entre les traitements. Ces différences sont probablement corrélées aux différences d’activité-densité et aux différences microclimatiques induites par les différences de couverts arborés.Dans un dernier temps, l’étude s’est focalisée sur une culture, la salade, et les dégâts causés par les limaces dans les différents traitements, sur les feuilles visibles. Plus de dégâts sous les arbres ont été constatés, malgré une activité-densité d’Arion lusitanicus et de Deroceras reticulatum non supérieures au témoin au mois de juin où les dégâts ont fortement augmenté. Les méthodes utilisées (planches, pots pièges neutres et attractifs) ont présenté des efficacités différentes, dont l’intérêt respectif est discuté.
... A large and growing body of literature indicates that natural enemies are key regulators of herbivore populations, including those of slugs and snails. Some species of ground beetles (Carabidae) are particularly important predators of slugs and also common in many agricultural environments, including Pterostichus melanarius and Carabus nemoralis, which are present in both Europe and North America (Symondson et al. 1996;Bohan et al. 2000;Fawki et al. 2005;Pianezzola et al. 2013). The distribution of P. melanarius in agricultural fields, for example, has been found to be significantly associated with high densities of slugs, suggesting that populations of this predator track populations of slugs (Symondson et al. 1996;Bohan et al. 2000). ...
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Terrestrial molluscs are some of the most important herbivores in temperate habitats. They tend to be generalists and can be serious pests in agricultural fields, particularly no-till fields used for field and forage crops; however, farmers have access to few commercially available solutions, and the existing ones present many disadvantages (e.g. reliability, cost, environmental concerns). In this paper, we review these current management options with a focus on agronomic crops, as well as the biotic factors that influence mollusc feeding, such as natural enemies, plant nutritional content, and chemical defences. These biotic factors all have important direct consequences on mollusc fitness and can be manipulated in agricultural settings. We then review evidence from the latest research in the field of nutritional ecology to propose the use of the Geometric Framework, a well-established nutritional approach, to measure nutrient regulation and performance of terrestrial molluscs and develop ecologically based management programs that also relies on susceptibility to natural enemies. To illustrate our point, we detail a specific strategy being used by farmers in the Mid-Atlantic US to manage slug populations; in this system, farmers are using cover crops terminated after the cash crop is planted (also called “planting green”) and this approach appears to harness slug nutritional preferences and natural enemies to manage slug populations.
... The impact on raspberry beetle larvae is not necessarily associated with a high preference for larvae. Fawki et al. (2005) reported that for P. melanarius and C. nemoralis insects are high-quality, earthworms are intermediate, and slugs and seeds are low quality food for these species, whereas for C. nemoralis, earthworms are the preferred prey. But, it is important to note that pure diets of all prey types are nutritionally incomplete and most predators can improve their fitness and fecundity by choosing a mixed diet (Toft, 1996;Saska, 2008). ...
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The raspberry beetle (Byturus tomentosus F.) is a widespread pest of raspberry in Europe. Although it is being controlled chemically, alternative strategies should be developed, based on biological control by polyphagous predators. Laboratory feeding tests were used to investigate the role of raspberry beetle larvae in the diet of the carabid species, Pterostichus melanarius, P. niger, Carabus nemoralis and Harpalus rufipes. In no-choice and choice feeding tests with aphids or raspberry beetle larvae P. melanarius and P. niger preferred to consume raspberry beetle larvae. C. nemoralis quickly consumed both prey items. H. rufipes preferred to eat raspberry beetle larvae to Thlapsi arvense seeds. According to the consumed biomass of each food item, larvae of the raspberry beetle were preferred by each carabid species tested. Data reported here clearly indicate that large carabids - P. melanarius, P. niger, C. nemoralis and H. rufipes could play an important role in regulating raspberry pest populations.
... d part of the experiment the juveniles in the earthworm group had grown less and weighed significantly less than those of the mixed group and the mollusc group.This may indicate that earthworms are less suitable as a monotypic diet in the long run. Few studies have evaluated the quality of earthworms and snails/slugs for other generalist predators. Fawki et al. (2005) found that earthworms were only of intermediate quality and slugs were of low quality to generalist carabid beetles. Both groups were of low food quality to generalist harvestmen (Hvam and Toft 2008). Among both carabid beetles and harvestmen there are taxa that specialize in slugs and snails. These taxa must have somehow overcome the m ...
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Diet composition of slow worms (Anguis fragilis) from a Danish population was recorded from May to September 2006. Slow worms were maintained in cool conditions (at 8°C) for a maximum of 126 h, which made approximately half of the animals regurgitate. The method worked equally well on juveniles and adults. The regurgitations revealed that the slow worms preyed on small snails, slugs, pill millipedes (Glomeris marginata), earthworms and Lepidoptera larvae. There were seasonal changes in taxon composition of the diet but no ontogenetic or sex‐related differences. The food quality of selected prey types was tested on juveniles in a laboratory experiment. Mealworms gave a significantly lower gain in mass and snout–vent length than slugs, earthworms and a mix of all three prey types. A supplementary experiment revealed that slow worms from the present population completely rejected mealworms as prey. Earthworms seemed to be nutritionally inferior to molluscs.
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The paper reviews existing data on the food quality of cereal aphids for generalist predators. Data are presented for spiders, harvestmen, carabid and staphylinid beetles, cockroaches, ants and one species of bird. All results agree that cereal aphids are low-quality food compared to alternative prey types (in most studies fruit flies). This is associated both with a low consumption capacity for aphids and a low utilization efficiency of the aphid food. A pure aphid diet allows full juvenile development in only a few species. Aphids as part of mixed diets can have negative, neutral or positive effects, which depends on the quality of the remaining diet. The low consumption capacity for aphids is due to the development of a specific feeding aversion. Genetic variation in the ability to tolerate aphids has been documented, indicating that predators may be able to adapt to a higher proportion of aphids in the diet in areas where outbreaks are frequent. A consequence of these findings is that predator populations rely on alternative prey (e.g. Collembola and Diptera) for maintenance and reproduction, and are probably unable to benefit nutritionally from an aphid outbreak. The low food quality of aphids to generalist predators explains why generalist and specialist predators have widely different roles in aphid biocontrol, but does not rule out that under some conditions the generalists may be able to inhibit aphid population growth sufficiently to prevent an outbreak, as field experiments have indicated. Simulation modelling shows that a low consumption capacity for aphids has little influence on the ability to prevent aphid population increase at low aphid immigration rates, but a great influence at high aphid immigration rates. Modelling also indicates that there may be an optimal availability of high-quality alternative prey that maximizes the impact of generalist predators on aphid population growth.
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Adults of Carabus nemoralis Mueller and Scaphinotus marginatus Fischer were tested for orientation to mucus trails of the slug Derocerasr reticulatum ( Muller) and earthworms using an X-shaped orientation chamber. In early June, C. nemoralis females oriented to both slug and earthworm mucus, whereas males only oriented to earthworm mucus. Orientation disappeared in both sexes by late June. Brushing palpi and antennae with glycerol did not block orientation to earthworm mucus in C. nemoralis females. Variability in orientation may be driven by seasonal activity patterns, reproductive condition, or behavior modification during experiments caused by carbon dioxide anesthesia. Scaphinotus marginatus did not orient to either mucus type. It is unclear if sensilla on the palpi of these carabid species function in detection of mucus trails.
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Survey of the 135 species of the genus Carabus L. belonging to the European fauna (Coleoptera, Carabidae). Special part: Introduction, Checklist, Key to the adults, Key to the larvae, Species accounts. General part: Biology and ecology, Phylogeny, Biogeography, Conservation Biology, Carabus evaluations. 511 pages, ca. 540 illustrations and maps, 100 European transects.
Predation by Carabus granulatus on three invertebrate groups, Lumbricidae, larval Elateridae, and larval Tipulidae was examined using the serological method, and it was found that earthworms and larval tipulids were consumed. The frequency of detection of their antigens in the diet of predators was significantly correlated with the intensity of soil surface searching by these prey. Earthworms, probably the species active on the soil surface, such as Dendrobaena octaedra and D. rubida, represented a permanent food supply for C. granulatus. Larval tipulids were abundant only in some sites. They were intensely exploited by carabids in spring, when they were active on the soil surface. Larval elaterids did not occur on the soil surface, so they were rarely detected in the diet of carabids.
A feeding experiment was established to elucidate the extent of granivory and phytophagy among 24 species of insectivorous carabid beetles representing 12 genera. Consumption of three kinds of seeds and one kind of green plant matter by these carabids was compared to that of a predominantly granivorous species. Granivory and phytophagy was most prevalent among large generalist insectivores belonging to the subfamily Harpalinae, less so in the smaller Psydrinae, and not found (or very rare) among Scaritinae or specialist insectivores belonging to Carabinae. Phytophagy was less predominant than granivory.
(1) The gut contents of 1206 animals belonging to twenty-six species collected from pitfalls in 1973 were examined under a binocular microscope using x 100 magnification. (2) Fifteen taxa, which were mostly Staphylinidae, had no solid remains in the gut and were probably fluid-feeders. (3) Notiophilus biguttatus, Loricera pilicornis and Lamycetes fulvicornis fed primarily on Collembola, Tachyporus spp. on fungi, Agonum dorsale on aphids, Forficula auricularia on plant material and Bembidion lampros on Diptera and Collembola. Feronia melanaria, Harpalus rufipes and Nebria brevicollis contained a wide range of food and there was considerable overlap between species, but Coleoptera adults and larvae featured prominently in the diet of all three. Aphids were eaten by seven species and formed an appreciable part of the diet of Agonum dorsale and Forficula auricularia. (4) The list of aphid feeders was extended to twelve species by the examination of a further 1051 animals collected by daytime search of the ground zone of a spring barley crop. The importance of Agonum dorsale as an aphid feeder was confirmed and Risophilus atricapillus L., Calathus fuscipes Goeze, Tachyporus chrysomelinus, Amara familiaris Duftschmid and Nebria brevicollis were also shown to have fed on aphids. (5) For Bembidion lampros and Tachyporus spp. the percentage of animals containing food was higher for non-gravid females than for males or gravid females, whilst in Feronia melanaria and Agonum dorsale both gravid and non-gravid females gave a higher percentage than males. It is suggested that the efficiency of these species as potential agents of natural control could be influenced by the sex ratio and their time of breeding in relation to the timing of critical periods in the cycle of pest abundance.
1. Interactions between the polyphagous carabid predator Pterostichus melanarius (Illiger) and slugs were investigated from July to September 1992, before and after harvesting a rape crop. The experimental site comprised a long-term field study of the effects of different forms of cultivation (ploughing vs. non-inversion tillage), and methods of straw disposal (baling vs. incorporation of chopped straw) upon invertebrate populations and crop yields. Direct-drilling was also included as a no-tillage base-line. 2. Beetles (total 2078) were collected by pitfall trapping twice weekly. Each beetle was dissected, and its crop contents weighed and tested by enzyme-linked immunosorbent assay (ELISA) to determine the concentration and quantity of slug haemolymph it contained. Slugs [Deroceras reticulatum (Muller) and Arion intermedius Normand] were extracted from soil samples by gradual flooding, to estimate both numbers and biomass. 3. Significantly more P. melanarius were trapped in direct-drilled plots than in the tilled treatments. Within the tilled treatments, greater numbers of beetles were trapped where straw was incorporated by non-inversion tillage. 4. Crop weights were significantly greater in beetles from direct-drilled plots than in those from tilled treatments, as were both the concentrations and quantities of slug haemolymph they contained. Overall, ≈84% of beetles contained slug remains. 5. Greatest concentrations and quantities of slug remains were detected prior to the disposal of rape residues at the end of July, by baling or shallow incorporation in the soil. Cultivation had both short- and long-term effects upon the proportion of the diet of the beetles that was slugs. 6. Slug biomass declined following disposal of rape residues and it was only after this time that significant treatment differences emerged. 7. Positive relationships were found between the biomass of slugs in the soil and numbers of beetles trapped, the proportion of the beetles' diet that was slugs and the quantities of slug haemolymph in beetle crops. 8. Our results strongly suggest aggregation of P. melanarius to areas of high slug biomass in the soil and preferential feeding in such areas upon slugs. As this carabid is probably the commonest large predatory beetle in arable crops in Britain, these results clearly identify P. melanarius as a potentially important slug control agent.