Predation on the slug Deroceras reticulatum by the carabid beetles Pterostichus madidus and Nebria brevicollis in the presence of alternative prey

1 Slugs are important pests in many agricultural crops and potential biological control agents are being studied as an alternative to molluscicides. Carabid beetles may be able to reduce slug populations, but their role as control agents may be influenced by the presence of alternative prey. 2 Attacks on the pest slug Deroceras reticulatum (Müller) by the carabid beetles Pterostichus madidus (Fabricius) and Nebria brevicollis (Fabricius) were investigated in the presence of alternative prey (earthworms and Calliphora fly larvae). Consumption of slug eggs and aphids was also investigated. 3 All five prey types were consumed to varying degrees during the experiments. Both beetle species showed a significant preference for Calliphora larvae over slugs. Pterostichus madidus showed a significant preference for earthworms over slugs. No preference was shown between earthworms or Calliphora larvae by P. madidus females or N. brevicollis. However, P. madidus males showed a significant preference for Calliphora larvae over worms. Pterostichus madidus showed no preference between slug eggs and aphids; N. brevicollis showed a significant preference for aphids over slug eggs. 4 The results from this study indicate that generalist beetles will often attack other prey in preferences to adult slugs. Slugs may not be preferred because of their mucus. Other prey items occur frequently in arable soils and generalist carabids may ignore slugs altogether and may only feed on them when slug density is high or other prey are unavailable.     

Predation by the carabid beetles Pterostichus madidus and Nebria brevicollis is affected by size and condition of the prey slug Deroceras reticulatum

1 Slugs are important pests in many agricultural crops but molluscicides commonly used to control slugs affect non‐target organisms. Encouraging biological control may help to reduce molluscicide use, but the efficiency of potential natural enemies needs to be investigated. 2 Serological tests have shown that certain carabid species consume slugs. These techniques, however, do not distinguish between scavenging and true predation, nor do they provide information on the size or other characteristics of the prey consumed. The study reported here was undertaken to establish whether scavenging of dead slugs might be an important factor contributing to positive serological test results. 3 Both Pterostichus madidus (Fabricius) and Nebria brevicollis (Fabricius) consumed Deroceras reticulatum (Müller) under laboratory conditions. Dead slugs were scavenged in preference to injured or healthy slugs. 4 Only small, live slugs (< 0.11 g) were killed by both beetle species, which may, therefore, be incapable of killing larger slugs. 5 These generalist beetle species appeared unable to overcome the defence mucus produced by slugs. The data suggest that positive serological results from field collected beetles may reflect scavenging rather than predation on live or injured slugs.     

Effect of predator size and temperature on the predation of Deroceras reticulatum (Muller) (Mollusca) by carabid beetles

Twenty-one carabid species were used in a laboratory study to determine the effect of beetle size and temperature on the predation of one day old Deroceras reticulatum (Muller) slugs. The beetles were caught in arable land at the study site. None of the five small-sized beetle species killed slugs, whereas five of the seven medium-sized beetle species and eight of the nine large-sized beetle species killed slugs. Four of the most abundant beetle species at the study site were used to assess the effect of temperature on the predation of 1-day-old slugs. There were significant differences in the proportion of beetles predating slugs at the different temperatures. Regression analysis showed that there was a significant increase in the proportion of Pterostichus madidus (Fabricius) and Harpalus rufipes (Degeer) beetles predating slugs as temperature increased. Nebria brevicollis (Fabricius) inflicted its highest level of slug mortality at 8°C and its larvae were the only predators to significantly increase slug mortality at 4°C, the lowest experimental temperature. Harpalus aeneus (Fabricius) inflicted significant levels of slug mortality at 20°C, the highest experimental temperature. It appeared that the predatory activity of these beetle species at the five experimental temperatures reflected their annual activity periods in the field.     

Effects of metaldehyde and methiocarb on feeding preferences and survival of a slug predator (Pterostichus melanarius (F.): Carabidae,Pterostichini)

The potential for reducing slug populations in crops through predation by generalist carabid beetles is well documented. However, few studies have considered interactions between biological and chemical control agents of slugs. Laboratory assays supported previous findings that the consumption of metaldehyde by slugs (Deroceras reticulatum) leads to increased duration of feeding bouts by carabid beetles (such as Pterostichini) on sub‐lethally affected individuals. However, a similar effect was not found for Pterostichus melanarius exposed to slugs fed on the other widely applied pelleted molluscicide formulation (methiocarb). Examination of beetle survival after consumption of slugs containing molluscicides demonstrated the strong biocidal properties of methiocarb, whereas metaldehyde consumption (ingested through slug predation) did not differ from control slugs killed by freezing. Beetle avoidance of slugs containing a more toxic molluscicide compound and the interaction between slug mucus production and beetle attack rates are discussed.     

Biodiversity vs. biocontrol: positive and negative effects of alternative prey on control of slugs by carabid beetles

Environment-friendly farming techniques seek to increase invertebrate biodiversity in part with the intention of encouraging greater numbers of predators that will help to control crop pests. However, in theory, this effect may be negated if the availability of a greater abundance and diversity of alternative prey diverts predators away from feeding on pests. The hypothesis that access to alternative prey can lead to reduced pest suppression under semi-field conditions was tested. Alternative prey type and diversity were manipulated in 70 mesocosms over 7+ weeks in the presence of the carabid Pterostichus melanarius (Illiger), a known predator of slugs, and reproducing populations of the slug Deroceras reticulatum (Müller). Significantly fewer slugs survived where no alternative prey were provided. Maximum slug numbers and biomass were found in treatments containing either carabids plus a high diversity of alternative prey (many species of earthworm and three of Diptera larvae) or a single additional prey (blowfly larvae, Calliphora vomitoria Linnaeus). In these treatments slug numbers and biomass were as high as in plots lacking predators. The effects of alternative prey were taxon-specific. Alternative prey strongly affected carabid fitness in terms of biomass and egg load. The fittest predators (those with access to high alternative prey diversity or C. vomitoria larvae) reduced slug numbers the least. The mean individual slug weights were greater in treatments with alternative prey than where no alternative prey were provided to the carabids. These results suggest that pests may survive and reproduce more rapidly in patches where predators have access to alternative prey.     

DOES TANDONIA BUDAPESTENIS (MOLLUSCA: PULMONATA) CONTAIN TOXINS? EVIDENCE FROM FEEDING TRIALS WITH THE SLUG PREDATOR PTEROSTICHUS MELANARIUS (COLEOPTERA: CARABIDAE)

Slugs are known to be killed and consumed by a range of invertebrateand vertebrate predators in the field. Carabid beetles (Coleoptera:Carabidae) in particular are major natural enemies of slugs,and have been shown to be capable of controlling certain speciesin a crop environment. This paper reports experiments to investigatethe effects, on the carabid Pterostichus melanarius, of feedingon the milacid slug Tandonia budapestensis. The slugs provedto be toxic, 50% of the beetles dying within two days. Mortalityof beetles fed on two other species of slug, Deroceras reticulatumand Arion distinctus, was not significantly different from thatfor beetles fed upon a control prey (Calliphora vomitoria).These results represent the only known case of a European slugproving to be toxic to potential predators, and is one of avery small number of reported instances of possible toxicityamongst terrestrial gastropods. The possibility that the orangeline down the dorsal keel of T. budapestensis may act as warningcoloration to birds is discussed. (Received 4 December 1996; accepted 5 March 1997)     

THE IMPORTANCE OF MUCUS AS A DEFENCE AGAINST CARABID BEETLES BY THE SLUGS ARION FASCIATUS AND DEROCERAS RETICULATUM

The effect of mucus exudation on the survival of Arion fasciatusand Deroceras reticulatum was studied by exposing mechanicallystimulated and control slugs to Carabidae beetles for 24 hours.A light stimulation, lasting three minutes, exhausted the copiousflow of mucus for one day. A generalist, Pterostichus niger,significantly preferred stressed D. reticulatum over controlones. Similarly, P. niger exclusively ate stressed individualsof A. fasciatus. Two beetles which specialize in gastropods,Cychrus caraboides and Carabus violaceus, consumed an equalnumber of stressed and control D. reticulatum and A. fasciatus.The susceptibility of the slug species to predation was different:for each beetle species, the proportion of available D. reticulatumpreyed upon was significantly higher than that of A. fasciatus.The differences in the behaviour of A. fasciatus and D. reticulatumin defending themselves against attacks is described. The mainreason why specialist beetles are able to hunt slugs successfullyis their ability to prevent the slugs from exuding large amountsof mucus. This may succeed by different means: C. violaceustargeted their killing strokes against the posterior part ofthe mantle while C. caraboides hit the head of the slug. Inboth case the strokes seemed to paralyze the slugs. (Received 31 March 1993; accepted 1 October 1993)     

Contrasting predation pressure of different ground beetles on slugs and their eggs

Slugs such as Deroceras reticulatum Müller (Pulmonata: Agriolimacidae) cause crop losses in temperate regions worldwide. Numerous species of ground beetles (Coleoptera: Carabidae) feed on slugs, but possible interactive effects are poorly known. Here, we compared predation pressure on slug eggs and slug immatures among Abax parallelepipedus Piller and Mitterpacher, Pterostichus niger Schaller, and Pterostichus melanarius Illiger. The latter was most effective against slug eggs but least effective against immature slugs compared to the other species, demonstrating some specificity of ground beetle predation on life stages. Slug egg predation of P. niger in combination with both other species was synergistic, with up to twice as many eggs consumed as for single species treatments. The effect of species combinations on immature slugs showed no differences from expectations based on single species treatments. Our results indicate that combinations of ground beetle species are favourable for the suppression of slugs in early life stages.     

Predation by the carabid beetle Harpalus rufipes on the pest slug Deroceras reticulatum in the laboratory

The Harpalini species Harpalus rufipes, as many other generalist carabids, consume a wide variety of prey and it is known to feed on pest slugs such as the grey field slug Deroceras reticulatum, but quantitative data about the predatory activity of H. rufipes on slugs are very scarce. In laboratory experiments, we assessed the capability of male H. rufipes to kill eggs and different‐sized slugs of the pest species D. reticulatum in either the absence or the presence of alternative live prey (dipteran larvae and aphids). We also investigated the preference of H. rufipes for eggs and hatchlings of D. reticulatum in a choice experiment. H. rufipes killed considerable amounts of eggs and small juveniles (≤5.0 mg) of D. reticulatum, both in no‐choice and in choice situations. Medium‐sized juvenile slugs (10–20 mg) were seldom killed only in no‐choice situations, and no large juveniles (50–60 mg) were killed. Dipteran larvae and aphids were killed also in no‐choice and in choice situations. The type of alternative prey presented with slug eggs affected the survival of the eggs to H. rufipes predation. The presence of dipteran larvae as alternative prey did not affect the survival of juvenile slugs. When eggs and small juvenile slugs were offered together, the survivals of both items were similar. The obtained results under laboratory conditions suggest that the generalist predator H. rufipes might realise an important contribution to the control of pest slugs.     

Tracking predator density dependence and subterranean predation by carabid larvae on slugs using monoclonal antibodies

1. Subterranean carabid larvae are more numerous than surface‐active adults, yet very little is known about their ecological significance, dietary preferences or ability to regulate populations of prey species, particularly pests. Part of the reason for this is that predator–prey interactions beneath the soil are almost impossible to observe. 2. Extensive field studies have shown that adult Pterostichus melanarius (Illiger) can affect the temporal and spatial dynamics of their slug prey. However, if larvae too are feeding on slugs, this could radically affect overall predator–prey dynamics. 3. We tested the hypotheses that P. melanarius larvae would kill and consume two slug species, Deroceras reticulatum Müller and Arion intermedius Normand, under laboratory and semi‐field conditions, and that there would be no significant difference in rates of predation on these slug species. 4. A new monoclonal antibody was developed that was capable of detecting the presence of slug proteins in the guts of P. melanarius larvae. 5. Pterostichus melanarius larvae killed both A. intermedius and D. reticulatum in the laboratory, feeding to a greater extent, and growing more rapidly, on the latter. The larvae were equally effective at reducing numbers of both slug species in a crop of wheat grown in semi‐field mini plots, but predation was affected by density‐dependent intra‐specific competition amongst the beetle larvae. 6. Future modelling of the dynamic interactions between carabids and slugs will need to take into account predation by larvae.     

How does a carabid predator find aggregations of slugs in the field? Electroantennograms and behavioural assays suggest chemical cues

Field studies suggest that the generalist carabid predator and scavenger Pterostichus melanarius Illiger aggregates to patches with a higher density of slug prey. The mechanisms behind such aggregation are unknown. Experiments were conducted to test the hypothesis that they are responding to chemical cues. Electroantennograms (EAGs) showed no response by P. melanarius antennae to live, nematode-infected, injured or freshly killed slugs, but a strong response to dead slugs that had been allowed to decay for up to 48 h. Such a response would enable the beetles to find carrion in the field and may also, as dead prey are likely to be spatially correlated with live ones, provide a mechanism by which P. melanarius finds patches with a higher density of live slugs. Subsequent video analyses of P. melanarius responses to patches of slug mucus within arenas showed that beetles with intact antennae could detect these patches because they spent more time, and moved greater distances, within them and increased their rate of turning. Thus, at close range, P. melanarius used their antennae to detect slug mucus and hence, by implication, live slugs. The apparent contradiction between EAG data and behavioural experiments is discussed. Together these result confirm that P. melanariusdoes respond to chemical cues from its slug prey in ways that could lead to aggregation in areas of higher slug density in the field.     

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.     

Seed consumption and dispersal of ant-dispersed plants by slugs

In beech-dominated forests in Central Europe, many spring geophytes show adaptations to seed dispersal by ants (myrmecochory). Ants, however, can be rare in such moist forests. Motivated by observations of slug feeding on seeds we investigated the seed consumption of two plant species, Anemone nemorosa and Asarum europaeum, by slugs, in a series of experiments. In a seed predation experiment in a beech forest, we found that seed removal was strongly reduced when gastropods were excluded from the seed depots. The contribution of insects, including ants, and rodents to seed removal was relatively less but differed between May and July. In the laboratory, slug species, in particular Arion sp., consumed seeds of both plant species. Slugs either consumed the elaiosomes of seeds or swallowed seeds intact. Swallowed seeds were defecated undamaged and germinated as well as control seeds when buried overwinter, indicating the potential for seed dispersal by slugs. We also recovered seeds of myrmecochores in the faeces of several slugs caught in forests. In a slug release experiment in the forest, slugs moved up to 14.6 m (mean 4.4 m) in 15 h, which is the median gut passage time of seeds based on measurements made in the laboratory. We also found that when slug-defecated seeds were offered to rodents, these were less attractive than control seeds, suggesting that passage through the slug gut reduces seed predation risk. Our results demonstrate that slugs are significant consumers of elaiosomes or entire seeds of ant-dispersed plants and that they can function as seed dispersers of these plants.     

Impact of oilseed rape expressing the insecticidal serine protease inhibitor, mustard trypsin inhibitor-2 on the beneficial predator Pterostichus madidus

Abstract Insect-resistant transgenic plants have been suggested to have deleterious effects on beneficial predators feeding on crop pests, through transmission of the transgene product by the pest to the predator. To test this hypothesis, effects of oilseed rape expressing the serine protease inhibitor, mustard trypsin inhibitor -2 (MTI-2), on the predatory ground beetle Pterostichus madidus were investigated, using diamondback moth, Plutella xylostella as the intermediary pest species. As expected, oilseed rape expressing MTI-2 had a deleterious effect on the development and survival of the pest. However, incomplete pest mortality resulted in survivors being available to predators at the next trophic level, and inhibition studies confirmed the presence of biologically active transgene product in pest larvae. Characterization of proteolytic digestive enzymes of P. madidus demonstrated that adults utilize serine proteases with trypsin-like and chymotrypsin-like specificities; the former activity was completely inhibited by MTI-2 in vitro. When P. madidus consumed prey reared on MTI-2 expressing plants over the reproductive period in their life cycle, no significant effects upon survival were observed as a result of exposure to the inhibitor. However, there was a short-term significant inhibition of weight gain in female beetles fed unlimited prey containing MTI-2, with a concomitant reduction of prey consumption. Biochemical analyses showed that the inhibitory effects of MTI-2 delivered via prey on gut proteolysis in the carabid decreased with time of exposure, possibly resulting from up-regulation of inhibitor-insensitive proteases. Of ecological significance, consumption of MTI-2 dosed prey had no detrimental effects on reproductive fitness of adult P. madidus.     

Implications for conservation biocontrol of spatio‐temporal relationships between carabid beetles and coleopterous pests in winter oilseed rape

1 The spatio‐temporal distributions of predatory carabid beetles (Coleoptera: Carabidae) and their potential prey, the larvae of three coleopterous pests, Meligethes aeneus (Fabricius) and Ceutorhynchus spp. [Ceutorhynchus pallidactylus (Marsham), the cabbage stem weevil, and Ceutorhynchus assimilis (Paykull), the cabbage seed weevil], were studied within a crop of winter oilseed rape. The distributions of Collembola were recorded as potential alternative prey. Insect distributions were analysed and compared using Spatial Analysis by Distance Indices. 2 Mature larvae of the pests dropped from the crop canopy to the soil for pupation in temporal succession from May to early July. Their distributions within the crop were irregular and differed with species. 3 Adults of seven species or genera of carabid were abundant and active within the crop during May and June: Nebria brevicollis (Fabricius), Anchomenus dorsalis (Pontoppidan), Loricera pilicornis (Fabricius), Amara similata (Gyllenhal), Asaphidion spp., Pterostichus madidus (Fabricius) and Pterostichus melanarius (Illiger). 4 During May, N. brevicollis was spatially associated with peak numbers of M. aeneus larvae and with Collembola. Anchomenus dorsalis was spatially associated with Ceutorhynchus spp. larvae during two peaks in the abundance of the latter in early and late June. Nebria brevicollis and A. dorsalis coincided in both time and space with larvae of the three coleopterous pests when they were most vulnerable to predation by epigeal predators and are therefore good candidates for conservation biocontrol. 5 The importance of carabid beeetles in the natural enemy complex in winter oilseed rape and their potential for biocontrol of spring and summer pests are discussed in relation to husbandry practices for the crop and its adjacent areas which could be manipulated to promote carabid survival for integrated pest management.     

Prey detection by some predatory Coleoptera (Carabidae and Staphylinidae)

The prey detection methods of 12 species of Carabidae and one species of Staphylinidae were investigated using video and orientation techniques. The species examined were Cicindela campestris, Cychrus caraboides, Carabus problematicus, C. violaceus, Calosoma maderae, Nebria complanata, Scarites abbreviates, Broscus cephaloles, Pterostichus madidus, P. melanarius, P. niger, Abax parallelepipedus and Staphylinus olens .
All the species examined were seen to respond to prey upon contact (either by tactile or gustatory reception) during locomotor activity. Tests using orientation chambers showed that some of the species would orientate towards prey in the absence of contact. Some species orientated using vision (C. campestris, C. maderae, S. abbreviates, A. parallelepipedus ). This was most frequent when tested with fast-moving prey. In others, orientation towards prey occurred when olfactory cues were available (P. madidus, P. melanarius, P. niger and A.parallelepipedus ). All of the species employing this method of prey detection belonged to the Pterostichini and it appears that the receptors involved are situated on the antennae. Although some species did not orientate towards prey in the absence of contact cues, some of these species were found to respond to slug mucus ( C. caraboides, C. problematicus, C. violaceus and S. abbreviates ). The receptors for this are probably situated on the terminal ends of the palps. The method of prey detection used is discussed in relation to the ecology of the species.     

Invasive slugs as under-appreciated obstacles to rare plant restoration: evidence from the Hawaiian Islands

Introduced slugs have invaded many parts of the world where they were recognized as important pests of gardens and agriculture, but we know little about the effects of introduced slugs on rare plants in natural areas. The Hawaiian Islands have no native slugs, but over a dozen introduced slug species are now established. We reviewed Rare Plant Recovery Plans produced by the U.S. Fish and Wildlife Service for Hawaii and found that introduced slugs were specifically mentioned as threats or potential threats to 59 rare plant species (22% of all endangered and threatened plants), based mainly on anecdotal observations by field biologists. We then initiated an experimental field study to assess the impact of slug herbivory on the growth and survival of two endangered plant species (Cyanea superba, and Schidea obovata), one non-endangered native species (Nestegis sandwicensis) and two co-occurring invasive plant species (Psidium cattleianum and Clidemia hirta). In mesic forest on the Island of Oahu, we tracked the fate of outplanted seedlings in replicated 1 m² plots, with and without slug control. Slugs decreased seedling survival of the endangered species by 51%, on average. Slugs did not significantly affect survival of the non-endangered or invasive plant species. Introduced slugs seem to be under-appreciated as a direct cause of plant endangerment. Invasive slugs may also facilitate the success of some invasive plant species by reducing competition with more palatable, native plant competitors. Slug control measures are relatively inexpensive and could facilitate rare plant establishment and population recovery.     

The energetic advantages of slug specialization in garter snakes (genus Thamnophis)

We tested the hypothesis that dietary specialization by foraging garter snakes is accompanied by increased assimilation efficiency on specialist prey items. Our comparison included two closely related garter snake species considered to be slug specialists (Thamnophis ordinoides and Thamnophis elegans terrestris), one fish specialist (Thamnophis couchii), and one diet generalist (Thamnophis elegans elegans). Our results suggest that slug specialists have an energetic advantage over non-slug-eating snakes when both eat slugs. Slug specialists T. ordinoides and T. e. terrestris both have higher assimilation and net assimilation efficiencies when eating slugs than do generalists T. e. elegans and T. couchii. The slug specialists did not experience decreased efficiency when eating fish. Therefore, there was no apparent digestive trade-off for the slug specialists when eating other prey.     

Prey preferences of six species of Carabidae (Coleoptera) and one Lycosidae (Araneae) commonly found in UK arable crop fields

Abstract: Laboratory experiments were used to determine the feeding preferences of six carabid beetles and one lycosid spider on aphid and collembolan prey. The first investigation used only five species of carabid Pterostichus melanarius Illiger, Pterostichus madidus F., Harpalus rufipes DeGeer, Nebria brevicollis F. and Carabus violaceus L., which had been caught most commonly in pitfall traps in the headland region of arable crop fields. When offered Brevicoryne brassicae L., Sitobion avenae F., Metopolophium dirhodum Walker and Rhopalosiphum padi L. as prey items, the species consistently consumed in high numbers was M. dirhodum . In subsequent experiments four carabids Pterostichus cupreus L., P. melanarius, P. madidus. H. rufipes and a lycosid spider Trochosa ruricola DeGeer whose distribution was shown by pitfall trapping to extend throughout the arable crop, were the chosen predators. These predators were offered a choice between M. dirhodum and entomobryid collembolans (a recognised alternative prey item) to gauge their preference between the two prey types. Both male and female P. cupreus and P. melanarius showed a significant preference for the aphid prey, while there was no significant preference displayed by the other species. The effect of temperature on the voracity of these five predators fed on M. dirhodum was investigated. There were significant differences in the number of aphids consumed by the species and sexes at the different temperatures. Regression analysis on the mean numbers of aphids eaten by each sex of the five predators, showed that in the majority of cases there was a significant increase in predation with increasing temperature. In considering the dietary preferences illustrated by these experiments, it appeared that P. cupreus and P. melanarius offered the greatest potential in controlling aphids on arable crops.     

The significance of facultative scavenging in generalist predator nutrition: detecting decayed prey in the guts of predators using PCR

Gut-content analyses using molecular techniques are an effective approach to quantifying predator-prey interactions. Predation is often assumed but scavenging is an equally likely route by which animal DNA enters the gut of a predator/scavenger. We used PCR (polymerase chain reaction) to detect scavenged material in predator gut homogenates. The rates at which DNA in decaying slugs (Mollusca: Pulmonata) and aphids (Homoptera: Aphididae) became undetectable were estimated. The detectability of DNA from both carrion types in the guts of the generalist predator Pterostichus melanarius (Coleoptera: Carabidae) was then determined. The effects of carrion age and weight, as well as beetle sex, on detection periods, were quantified. Laboratory trials measured prey preference of beetles between live and decaying prey. Further experiments measured, for the first time, feeding by P. melanarius on dead slugs and aphids directly in the field. In both field and laboratory, P. melanarius preferentially fed on dead prey if available, but preference changed as the prey became increasingly decayed. Disappearance rates for slug carrion in wheat fields and grasslands were estimated and P. melanarius was identified as the main scavenger. Comparison of the retention time for dead slugs in the field, with the detection period for decaying slug material in the guts of the predators, showed that PCR-based techniques are not able to distinguish between predated and scavenged food items. This could potentially lead to overestimation of the impact of predation on slugs (and other prey) by carabids. Possible implications of facultative scavenging by invertebrate predators for biocontrol and food-web research are discussed.