Carabid Beetle Pterostichus Melanarius Research Articles

Dispersal of a carabid beetle in farmland is driven by habitat‐specific motility and preference at habitat interfaces

AbstractCarabid beetles are common predators of pest insects and weed seeds in agricultural systems. Understanding their dispersal across farmland is important for designing farms and landscapes that support pest and weed biological control. Little is known, however, about the effect of farmland habitat discontinuities on dispersal behaviour and the resulting redistribution of these beetles. We released 1,985 well‐fed and 1,680 food‐deprived individuals of the predatory carabid beetle Pterostichus melanarius (Illiger) (Coleoptera: Carabidae) on a farm in Wageningen, The Netherlands. We recaptured 23.6% of those beetles over a period of 23 days in 2010. The farmland comprised agricultural fields with various crop species and tillage, separated by strips of perennial vegetation. We developed discrete Fokker‐Planck diffusion models to describe dispersal based on motility (m2 day−1) and preferential behaviour at habitat interfaces. We used model selection and Akaike’s information criterion to determine whether movement patterns were driven by variation in motility between habitats, preferential behaviour at habitat interfaces, or both. Model selection revealed differences in motility among habitats and gave strong support for preferential behaviour at habitat interfaces. Behaviour at interfaces between crop and perennial vegetation was asymmetric, with beetles preferentially moving towards the crop. Furthermore, beetles had lower motility in perennial strips than in arable fields. Also between arable habitats movement was asymmetric, with beetles preferentially moving towards the habitat in which motility was lowest. Neither crop type nor tillage explained differences in motility between crop habitats. Recapture data representing dispersal patterns of beetles were best described by a model that accounted for differences in motility between farmland habitats and preferential behaviour at habitat interfaces. Motility in farmland and behaviour at interfaces can also be estimated for other organisms and farmland habitats to support design of farmland conducive to natural pest suppression. Landscape design for early recruitment of carabids into arable fields should take into account the quantity and quality of resource habitats in the landscape, their proximity to crop fields, movement rates, and the possibility of movement responses at interfaces between landscape elements.

Comparing three types of dietary samples for prey DNA decay in an insect generalist predator.

The rapidly growing field of molecular diet analysis is becoming increasingly popular among ecologists, especially when investigating methodologically challenging groups, such as invertebrate generalist predators. Prey DNA detection success is known to be affected by multiple factors; however, the type of dietary sample has rarely been considered. Here, we address this knowledge gap by comparing prey DNA detection success from three types of dietary samples. In a controlled feeding experiment, using the carabid beetle Pterostichus melanarius as a model predator, we collected regurgitates, faeces and whole consumers (including their gut contents) at different time points postfeeding. All dietary samples were analysed using multiplex PCR, targeting three different length DNA fragments (128, 332 and 612bp). Our results show that both the type of dietary sample and the size of the DNA fragment contribute to a significant part of the variation found in the detectability of prey DNA. Specifically, we observed that in both regurgitates and whole consumers, prey DNA was detectable significantly longer for all fragment sizes than for faeces. Based on these observations, we conclude that prey DNA detected from regurgitates and whole consumers DNA extracts are comparable, whereas prey DNA detected from faeces, though still sufficiently reliable for ecological studies, will not be directly comparable to the former. Therefore, regurgitates and faeces constitute a useful, nonlethal source for dietary information that could be applied to field studies insituations when invertebrate predators should not be killed.

Movement behaviour of the carabid beetle Pterostichus melanarius in crops and at a habitat interface explains patterns of population redistribution in the field.

Animals may respond to habitat quality and habitat edges and these responses may affect their distribution between habitats. We studied the movement behaviour of a ground-dwelling generalist predator, the carabid beetle Pterostichus melanarius (Illiger). We performed a mark-recapture experiment in two adjacent habitats; a large plot with oilseed radish (Raphanus sativus) and a plot with rye (Secale cereale). We used model selection to identify a minimal model representing the mark-recapture data, and determine whether habitat-specific motility and boundary behaviour affected population redistribution. We determined movement characteristics of P. melanarius in laboratory arenas with the same plant species using video recording. Both the field and arena results showed preference behaviour of P. melanarius at the habitat interface. In the field, significantly more beetles moved from rye to oilseed radish than from radish to rye. In the arena, habitat entry was more frequent into oilseed radish than into rye. In the field, movement was best described by a Fokker-Planck diffusion model that contained preference behaviour at the interface and did not account for habitat specific motility. Likewise, motility calculated from movement data using the Patlak model was not different between habitats in the arena studies. Motility (m2 d−1) calculated from behavioural data resulted in estimates that were similar to those determined in the field. Thus individual behaviour explained population redistribution in the field qualitatively as well as quantitatively. The findings provide a basis for evaluating movement within and across habitats in complex agricultural landscapes with multiple habitats and habitat interfaces.

Effect of light quality on movement of Pterostichus melanarius (Coleoptera: Carabidae)

Abstract Behaviour of nocturnal insects is routinely observed under red light, but it is unclear how the behaviour under red light compares to behaviour in complete darkness, or under a source of white light. Here, we measure movement behaviour of the nocturnal carabid beetle Pterostichus melanarius Illiger (Coleoptera: Carabidae) using camera recording under a near‐infrared (nir), red or white radiation source. Red light significantly reduced movement speed in females similar to the effect of white light and different from nir. Also movement activity and pause length were affected by radiation source, with a significant difference between nir and white light, and with intermediate values in red light. The results presented here indicate that P. melanarius has different movement behaviour under the three radiation sources and suggest that nir rather than red radiation is most appropriate for measuring behaviour in total darkness. However, in the field total darkness is rare both because of natural light sources such as the moon and stars but increasingly also because of ecological light pollution, and therefore red light may still be of use for observing ecologically and practically relevant natural night‐time behaviour.

Prey choice by carabid beetles feeding on an earthworm community analysed using species- and lineage-specific PCR primers

The carabid beetle Pterostichus melanarius is a major natural enemy of pests, such as aphids and slugs in agricultural systems. Earthworms are a dominant non-pest component of the diet of P. melanarius which help sustain the beetles during periods when the pest population is low or absent. In this study we wanted to test whether this predator exercises prey choice among different earthworm species or ecological groups. High levels of genetic diversity within morphological species of earthworm necessitated the development of primers that were specific not just to species but lineages and sub-lineages within species as well. Gut samples from beetles were analysed using multiplex-PCR and fluorescent-labelled primers. Calibratory feeding trials were undertaken to calculate median detection times for prey DNA following ingestion. Extensive testing demonstrated that the primers were species-specific, that detection periods were negatively related to amplicon size and that meal size had a highly significant effect on detection periods. Monte Carlo simulations showed that, in general, worms were being predated in proportion to their densities in the field with little evidence of prey choice, other than probable avoidance of the larger, deep-living species. There was no evidence that epigeic species were being taken preferentially in comparison with endogeic species. There was also no evidence that defensive secretions by Allolobophora chlorotica reduced predation pressure on this species by P. melanarius. We concluded that any management system that increases earthworm densities generally, regardless of component species, is likely to be optimal for increasing numbers of this beneficial beetle predator.

Invertebrate biodiversity affects predator fitness and hence potential to control pests in crops

Natural enemies that control pests usually allow farmers to avoid, or reduce, the use of pesticides. However, modern farming practices, that maximize yields, are resulting in loss of biodiversity, particularly prey diversity. Does this matter? Pests continue to thrive, and without alternative prey the predators should, perforce, concentrate their attentions upon the pests.We showed that a diverse diet significantly enhances predator fecundity and survival. Experiments were conducted using common generalist predators found in arable fields in Europe, the carabid beetle Pterostichus melanarius (Coleoptera: Carabidae) and the linyphiid spider Erigone atra (Araneae: Linyphiidae). We tested the hypothesis that mixed species diets were optimal, compared with restricted diets, with respect to parameters such as predator weights, egg weights, numbers of eggs laid, egg development times, egg hatching rates and predator survival. In carabids, an exclusive earthworm diet was as good as mixed diets containing earthworms for egg production and hatching, but less good than such mixed diets for increase in beetle mass and sustained egg laying. For spiders, aphids alone (Sitobion avenae) or with the Collembola Folsomia candida, drastically reduced survival. Aphids plus the Collembola Isotoma anglicana improved survival but only aphids with a mixed Collembola diet maximized numbers of hatching eggs.Predators offered only pests (slugs or aphids) had lowest growth rates and fecundity. We therefore demonstrated that conservation of a diversity of prey species within farmland, allowing predators to exploit a diverse diet, is essential if predators are to continue to thrive in crops and regulate agricultural pests.

Avoidance of conspecific odour by carabid beetles: a mechanism for the emergence of scale-free searching patterns

We monitored the movements of a starved model predator, the carabid beetle Pterostichus melanarius, in arenas containing test papers upon which beetles had previously walked and unexposed control papers. Significantly, beetles accumulated on the unexposed controls, indicating conspecific avoidance (i.e. behaviour designed to avoid locations previously traversed by individuals of the same species). This finding is novel and important because optimal Levy-flight (scale-free) search patterns for the location of sparsely and randomly distributed prey resources can emerge from conspecific avoidance. This finding may account for the shortcomings of random-walk (scale-finite) models when used to predict large-scale movement and search patterns by extrapolating from observations made at small scales.

Comparing the impact of conventional pesticide and use of a transgenic pest‐resistant crop on the beneficial carabid beetle Pterostichus melanarius

The potential impact of a chemical pesticide control method has been compared with that of transgenic plants expressing a protease inhibitor conferring insect resistance by utilising a tritrophic system comprising the crop plant Brassica napus (L.) (Oilseed rape), the pest mollusc Deroceras reticulatum (Müller) and the predatory carabid beetle Pterostichus melanarius (Illiger). Cypermethrin, as the most widely used pesticide in UK oilseed rape (OSR) cultivation, was selected as the conventional treatment. OSR expressing a cysteine protease inhibitor, oryzacystatin-1 (OC-1), was the transgenic comparator. In feeding trials, D. reticulatum showed no significant long-term effects on measured life history parameters (survival, weight gain, food consumption) as a result of exposure to either the cypermethrin or OC-1 treatment. However, D. reticulatum was able to respond to the presence of the dietary inhibitor by producing two novel proteases following exposure to OC-1-expressing OSR. Similarly, P. melanarius showed no detectable alterations in mortality, weight gain or food consumption when feeding on D. reticulatum previously fed either pesticide-contaminated or GM plant material. Furthermore, as with the slug, a novel form of protease, approximately M(r) 27 kDa, was induced in the carabid in response to feeding on slugs fed OC-1-expressing OSR.

Slug feeding in the carabid beetle Pterostichus melanarius: seasonality and dependence on prey size

As shown in Figure 2, activity of P. melanarius started in late April and increased during June in both years investigated. In July there was a slight decrease in activity, but from late July the numbers of trapped beetles increased again and reached a peak in late August to early September. This peak was higher in 1997 than in 1996. From the end of September onwards activity decreased, and in October/November only a few beetles were trapped. Males dominated the catch in all months except spring 1996 (ratio of males to females; April/May: 0.5, June: 0.9) and autumn 1996 (October/November: 0.4). The ratio of males to females caught for the whole period was 1.8. During spring (April‐June) it did not exceed 1.1, indicating an equal sex-ratio of hatchlings. In summer (July‐September), however, the activity of males was significantly higher than that of females reaching a ratio of 2.1 (� 2 � 7.7; P 0.05). Seasonal differences in crop volumes were also found. In spring (April‐June) the crop content was greater than during summer (July‐September; t � 4.55 for both years, P < 0.01; t � 2.07 for 1996, P < 0.05; t � 3.52 for 1997, P < 0.01). This was established for males (t � 3.65; P < 0.01) and females (t � 2.28; P < 0.05), and for slug-positive crops (t � 3.05 for both years, P < 0.01; t � 2.38 for 1996; t � 2.16; both P < 0.05) as well as for crops filled with other food (t � 2.76; P < 0.01). In males, crops containing other food were larger in spring than in summer (t � 3.64; P < 0.01), whereas in females, crops containing slug remains were larger in spring than in summer (t � 2.93; P < 0.05). To show further annual sexual differences in crop volumes, the data for June and July were pooled and compared with those for August and September. Thus, in early summer the crop volumes of both sexes did not differ, whereas in late summer, female beetles had significantly larger crop contents than males (t � 4.68 for both years; t � 3.47 for 1996; t � 2.75 for 1997; each P < 0.01). In total, 28.4% of P. melanarius tested positive for esterases of A. lusitanicus; of the females 39.7% tested positive, whereas with males it was only 22.2%. Thus the ratio of slug-positive females was significantly higher than that for males (� 2 � 16.19; P < 0.01). In 1996, the difference was clearer (� 2 � 14.63; P < 0.01) than 1997 (� 2 � 6.17; P < 0.05). Differences over time were analysed with the data pooled within months and within seasons. The combined data for summer (July‐September) showed a significantly lower positive ratio than the data for spring (t � 25.02; P < 0.01). Comparing data pooled within months, significant differences (on the basis of excluding empty crops) were found between April/May and June (� 2 � 7.23; P < 0.01), June and July (� 2 � 8.2; P < 0.01), September and October/November (� 2 � 5.04 in 1996; P < 0.05). During summer, the percentages of slug-positive beetles in different months were almost equal (July, 25.0%; August, 23.0%; September, 22.5%). But there was a large difference between sexes, as the

Predation and prey size choice by the carabid beetle Pterostichus melanarius (Coleoptera: Carabidae): the dangers of extrapolating from laboratory to field.

The impact of predation by the generalist carabid beetle Pterostichus melanarius (Illiger) on populations of the field slug Deroceras reticulatum (Müller), and the effects of prey size on the predator-prey interaction, were measured under semi-field conditions. It was hypothesized that environmental heterogeneity would lead to very different patterns of comparative mortality than might be deduced from size choice experiments conducted in the laboratory. Results from outdoor mini-plots, emulating conditions in a field of wheat, demonstrated that P. melanarius significantly reduced numbers of slugs from all size classes, with no apparent preferences. This was in marked contrast to results from earlier laboratory studies, where this beetle fed preferentially on the smallest slugs. The slugs in the mini-plots ranged in size from 2-100 mg and the numbers in the mini-plot reflected the size frequency distribution in the field. Beetles in mini-plots containing high densities of slugs increased significantly in weight, in contrast to beetles in mini-plots with low slug density or no added slugs, which did not. Enzyme-linked immunosorbent assays (ELISA), using anti-slug monoclonal antibodies, showed that where there was a higher density of slugs there was more slug protein in the guts of the beetles. It was concluded that environmental heterogeneity probably provided a greater number and diversity of refugia for smaller than for larger slugs, counteracting laboratory-measured size preferences measured in arenas without refugia. These results have implications for a range of ecological studies involving inter- and intra-specific prey size choice, and emphasize the dangers of extrapolating from the laboratory to the field.

Dynamics of the Relationship between a Generalist Predator and Slugs over Five Years

Although communities of generalist invertebrate predators are known to be capable of suppressing pests, little is known about the long-term population dynamics of individual species of generalist predators and single classes of prey in the field. We present evidence of a dynamic interaction between a generalist insect predator, the carabid beetle Pterostichus melanarius, and its slug prey. We analyzed the numbers of slugs and beetles in an arable field over a 5-yr period, during the main activity period of the beetles from June to September. The field contained 25 plots comprising five replicates of five cultural treatments. An index of the nutritional status of the 8497 beetles collected was obtained by weighing the crop of each beetle (a measure of total prey availability per predator). There was a strong relationship between the crop mass of the beetles and slug numbers in the soil, indicating that slugs were a major part of the diet of the beetles. The change in the beetle population from year to year was strongly related to both slug numbers in the soil and the crop mass of the beetles. This indicated that the slugs influenced the nutritional status, and hence the reproductive success, of the beetles. The predators had a significant effect on slug population growth between years but not between months within years. The temporal effect of these processes was a between-year coupling of beetle and slug population dynamics, buffered by feeding on other prey. The relationship appears to be similar to that between mammalian predators and limited numbers of prey species in the subarctic, where one prey species forms a substantial proportion of the total available food resources. Such relationships may be common in agroecosystems, where species diversity is low, and may be a significant factor driving periodic fluctuations in the abundance of both predators and pests.

DYNAMICS OF THE RELATIONSHIP BETWEEN A GENERALIST PREDATOR AND SLUGS OVER FIVE YEARS

Although communities of generalist invertebrate predators are known to be capable of suppressing pests, little is known about the long-term population dynamics of individual species of generalist predators and single classes of prey in the field. We present evidence of a dynamic interaction between a generalist insect predator, the carabid beetle Pterostichus melanarius, and its slug prey. We analyzed the numbers of slugs and beetles in an arable field over a 5-yr period, during the main activity period of the beetles from June to September. The field contained 25 plots comprising five replicates of five cultural treatments. An index of the nutritional status of the 8497 beetles collected was obtained by weighing the crop of each beetle (a measure of total prey availability per predator). There was a strong relationship between the crop mass of the beetles and slug numbers in the soil, indicating that slugs were a major part of the diet of the beetles. The change in the beetle population from year to year was strongly related to both slug numbers in the soil and the crop mass of the beetles. This indicated that the slugs influenced the nutritional status, and hence the reproductive success, of the beetles. The predators had a significant effect on slug population growth between years but not between months within years. The temporal effect of these processes was a between-year coupling of beetle and slug population dynamics, buffered by feeding on other prey. The relationship appears to be similar to that between mammalian predators and limited numbers of prey species in the subarctic, where one prey species forms a substantial proportion of the total available food resources. Such relationships may be common in agroecosystems, where species diversity is low, and may be a significant factor driving periodic fluctuations in the abundance of both predators and pests.

Foraging activity of the carabid beetle Pterostichus melanarius Ill. in field margin habitats

The foraging activity of the carabid beetle Pterostichus melanarius was studied in a capture–recapture experiment in field margin habitats. Two rectangular enclosures were installed over a succession of habitats with a decreasing prey availability: a hedge, a mixed crop strip and an adjacent crop culture. Marked starved and satiated individuals were released in the enclosures and recaptured during 8 days. Initial satiation state had a significant effect on activity. Also, the initial displacements of beetles depended both on the habitat and on the initial satiation state. P. melanarius appeared to have flexible habitat-use, depending mainly on three factors: the satiation state, the habitat preference of the species, and the prey availability in the habitat.

Activity and satiation state in Pterostichus melanarius: an experiment in different agricultural habitats

Summary1. A capture–recapture experiment was conducted to examine the effects of satiation state on the activity and foraging efficiency of the carabid beetle Pterostichus melanarius Ill., in four different habitats (a hedge, a transition zone between the hedge and the adjacent wheat crop, the margin of the wheat crop, and the centre of the wheat crop) in an agricultural ecosystem in France.2. Prey biomass and density decreased from the centre of the hedge to the crop margin and to the centre of the crop, where prey density was low but prey biomass was moderate. Starved and satiated beetles were released in circular enclosures and recaptured using pitfall traps for 6 days.3. Immediately after release, starved P. melanarius were significantly more active than satiated beetles, but this difference disappeared after the first day. At each recapture date, starved individuals had gained weight whereas satiated individuals had lost weight. The analysis of activity and weight variation at the end of the first day indicated that the centre of the crop seemed to be the most favourable habitat for starved individuals to find food rapidly, whereas the behaviour of satiated individuals was identical in all habitats.4. This experiment shows that habitat use of P. melanarius is flexible. The results are discussed in the context of the classical view of foraging behaviour in carabid beetles. The activity and foraging efficiency in P. melanarius in different habitats can be explained as the result of the interaction between individual satiation state, prey availability in the habitat, and particular preferences of the species.

Do earthworms help to sustain the slug predator Pterostichus melanarius (Coleoptera: carabidae) within crops? Investigations using monoclonal antibodies.

Earthworms provide a major potential source of alternative food for polyphagous predators, such as carabid beetles, that are natural enemies of slugs, aphids and other agricultural pests. Non-pest prey may foster larger numbers of natural enemies, which then help to control pests, or alternatively may help to divert the predators away from pest control. An earthworm-specific monoclonal antibody was developed to study carabid-earthworm interactions in the field and assess the role of earthworms as alternative prey. The antibody could identify as little at 7 ng of earthworm protein in an ELISA, and could detect earthworm remains in the foregut of the carabid beetle Pterostichus melanarius for 64 h after consumption. Thirty-six per cent of field-collected beetles contained earthworm remains. Quantities of earthworm proteins in the beetle foreguts were negatively related to total foregut biomass, suggesting that earthworm consumption increased as total prey availability declined. There was also a negative relationship between foregut biomass and beetle numbers, but both quantities and concentrations of earthworm proteins in beetle foreguts were positively related to beetle numbers. This suggests that as beetle activity-density increased, total prey availability declined, or, as prey availability declined, beetles spent more time searching. In these circumstances, beetles fed to a greater extent on earthworms, an acceptable but nonpreferred food item. Earthworms may, therefore, provide an ideal alternative prey for P. melanarius, helping to sustain it when pest numbers are low but allowing it to perform a 'lying-in-wait' strategy, ready to switch back to feeding on pests when they become available.

Spatial dynamics of predation by carabid beetles on slugs

Summary 1. An explicitly spatial sampling approach was employed to test the null hypothesis that the predation on slugs by the carabid beetle Pterostichus melanarius (Illiger) was opportunistic. 2. The beetles and slugs were sampled across a nested series of grids of sampling points, in a field of winter wheat during June and July 1997. 3. The spatial distribution of all slugs in June was found to change with the scale of the sampling grid, from random on the 0.25 m scale, through aggregation at 1 m, to random at 4 m. At the highest scale of 16 m, the slugs were significantly spatially aggregated. 4. The distribution of beetles in June was also spatially dynamic, with randomness observed at the 4 m and 8 m scales. At 16 m, significant aggregation was observed. 5. The dynamic distributions of slugs and beetles, at 16 m, were found not to be associated with, and thus were not determined by, soil or crop factors. 6. Comparison of slug and beetle populations showed, however, that the distributions at 16 m were dynamically associated with each other. In June where there were many slugs there were also many carabids, whilst in July where there were many carabids there were few slugs. 7. Approximately 11% of the beetles sampled across the 16 m grid in June and July were found to have ingested slug protein, following intensive enzyme‐linked immunosorbent assay (ELISA) testing. 8. The spatial distribution of these slug‐positive beetles was significantly associated with the distribution of the larger slug classes, over 25 mg. Where there were many large slugs in June there were many slug‐positive beetles. Conversely, in July few large slugs were found where there were many slug‐positive beetles. 9. Parametric analysis revealed that these changes in the large slug class, at each sampling point between June and July (growth), were negatively related to the local numbers of slug‐positive beetles, and that growth declined as the local numbers of beetles increased. 10. These findings suggest that predation was not opportunistic, but direct and dynamic, falsifying the null hypothesis. Moreover, this predation elicited significant changes in the spatial distribution and local density of the slugs, in a manner that may be termed spatially density dependent.

Isolating the components of activity-density for the carabid beetle Pterostichus melanarius in farmland.

The activity and density of the carabid beetle, Pterostichus melanarius, were studied over 10 weeks in a continuous mark-recapture experiment using a grid of pitfall traps spanning a hedgerow and extending approximately 30 m into two cereal fields; 1777 beetles were individually marked. The recapture rate was approximately 60% and 40% for males and females, respectively. Activity-density rose and fell four times between early June and mid August. Jolly-Seber estimates of density showed population density increasing to a single peak in late July. The mean population density in late July and August was relatively stable at approximately 0.26 m-2. Activity varied over the 10 weeks and was significantly higher during August than in June or July. The daily displacement distance frequencies, calculated from 750 male and 485 female recaptures of individually marked beetles, were distributed exponentially. Mean displacement distances were approximately 2.6 m day-1 during June and July, and 5.3 m day-1 during August. A diffusion model provided diffusion coefficients of 23.7 and 27.9 m2 day-1 for female and male beetles, respectively. The spatial distribution of P. melanarius was aggregated in patches. Spatial analysis by distance indices showed the spatial distribution of counts between successive periods of activity-density to be significantly associated. Approximately 5.75% of recaptures were from releases on the opposite side of the hedgerow. Approximately 20% of recaptures were from releases in opposite halves of the grid within the same field. The hedgerow acted as a significant barrier to dispersal between fields, with implications for the metapopulation structure of the species.