Ecological Entomology (1988) 13,293-299

The efficiency of pitfall trapping for polyphagous predatory Carabidae

NIGEL B . HALSALL and STEPHEN D. WRATTEN Department of Biology, The University, Southampton ABSTRACT. 1. The efficiency of pitfall trapping was investigated for seven carabid species, using time-lapse video recording equipment, in the laboratory. 2. The effects of differing substrates, trap designs and seasons of collection on the capture rates of the carabids was also investigated. 3. Capture rate differed significantly between the species studied. The differences in capture rates between the species were unrelated to beetle size, speed of movement and diurnal behaviour. 4. Few differences arose in the capture rates when type of substrate or trap or season of capture were changed.
Key words. Pitfall trap, efficiency, carabids, video.

Introduction

Pitfall traps have been used extensively to monitor the number and activity of surface-active invertebrates, especially Coleoptera and Araneida. Catches by these traps depend on the population size, locomotor activity (Mitchell, 1963; Greenslade, 1964) and susceptibility of capture of the animals. Therefore numbers caught represent only relative numbers o the f epigeal fauna present. However, because pitfall traps are cheap and require little labour they have been used as a major sampling method by, for example, workers studying the epigeal fauna present in cereal fields (Potts & Vickerman, 1974; Dunning et al., 1975; Sunderland, 1975; Edwards et al., 1978; Sunderland & Vickerman, 1980; Bryan & Wratten, 1984). The use of pitfall traps to compare species activities relies on the assumption that every Correspondence: M N. B. HalsaU, Department of r Biology, Building 44,The University, Southampton SO9 5NH.

species has the same chance of being captured. However, little if any work has been published to investigate this assumption. Related work includes that of Luff (1975), who demonstrated the differing efficiencies of several types of traps; Greenslade (1964) demonstrated that differently-set traps gave differing efficiencies; Obrtel (1971) maximized capture per unit area by manipulating the numbers of traps; Chiverton (1984) demonstrated that the content of the gut affected capture of a carabid species and Baars (1979) found that the use of continuous pitfall sampling could be used as a relative measure of the size of carabid populations. This paper describes the use of laboratory time-lapse video techniques to evaluate potential differences in efficiency of dry pitfall trapping within a range of seven carabid species. Efficiency in this case is defined as the proportion of encounters with the edge of the pitfall trap which result in capture. The data in this paper compare pitfall trap efficiency between carabid species under different experimental 293

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Niger B. Hahall and Stephen D . Wratten

conditions of substrate and trap type. Betweenspecies comparisons were made, not withinspecies comparisons between sites, which was done by Baars (1979). Trap efficiency was also compared between carabids caught in the autumn/winter and those caught in the spring/summer . Although there are potential problems associated with dry pitfall traps, such as avoidance, predation and aggregation, which may occur in the field, this work was restricted to the use of dry pitfall traps to limit the number of comparisons made. Any substantial differences demonstrated between species and between season will have implications for the interpretation of past and future field work which uses pitfall trapping as a sampling method for epigeal fauna.
Materials and Methods

The carabid species used for the studies represented a range of sizes that commonly occur in arable crops in the south of England. The smaller species, with an overall length of less than 6 mm (Luff, 1978), included Demetrias atricapillus (L.), Noriophilus biguttatus (F.) and Trechus quadrktriatus (Schrank); the mediumsued species, measuring 8-10 mm (Luff, 1978) included Agonum dorsale (Pont.) and Calathus melanocephalus (Goeze); and the Iirgest species, measuring 12-15 mm included Calarhus fuscipes (Goeze) and Nebria brevicollis (F.). All of the species were obtained from the Leckford Estate, Stockbridge, Hampshire. They were collected from field boundaries in October, November and December using an insect pooter (Southwood, 1978). Gutter traps (Luff, 1978), set in the open fields, were used to collect the beetles from April to July. Each trap consisted of a 2 m length of plastic rainwater guttering; this had a vertical side wall with a slight lip. At each end a stopend was fitted. At one of the ends an outlet pipe led vertically down into a plastic collection cup of height 13.5 cm and a diameter of 9.7 cm at the top tapering to 7 cm at the bottom. This cup contained stones and leaves as a refuge for the captured invertebrates. The beetles caught in the autumn/winter would be mostly from the new generation of adults ( N . Sotherton, pers. comm.), whereas the spring/summer caught ones would be a mixture of new generation adults and overwintered beetles.

The beetles were maintained in polystyrene boxes in a culture room. The boxes measured 17.5X 11.6x6.0cmandwerefilledtoadepthof2 cm with soil obtained from the field site. Refuges made from broken clay plant pots were placed on the soil surface. The culture room was maintained at 16 h light/24 h with a mean temperature of 15C and a 2C range. The beetles were fed every 3 days with second, third and fourth instar pea aphids (Acyrthosiphon pkum (Harris)) which had been cultured on broad bean Vicia faba (L.) cv. The Sutton. The medium sized to larger species were given twenty aphids per beetle, the smaller species were given ten. A 0 . 5 X 0 . 5 ~ 0 . 1 8 arena containing four pitm fall traps positioned in a silver sand or soil (as used in the boxes) substrate was used for the work. Sand was initially chosen as a substrate since this contrasted with the colour of the beetles, providing a clear video image. It also created a homogeneous surface giving the beetles unimpeded movement. Because this substrate is unnatural the initial experiments were repeated using a soil substrate. It was necessary to create contrast between the carabids and the substrate in this case by marking each beetle with a spot of white enamel paint on its right elytron. The hardboard walls o the arena were f covered with polythene which was coated with an aqueous suspension of PTFE (polytetrafluoroethylene). This coating prevented escape by the beetles. White polystyrene cups, 8 cm deep with a diameter of 8 cm at the top tapering to a diameter of 4.7 cm at the bottom, were used as traps. These were positioned in a square formation in the arena, with each cup being opposite the mid-point of a wall. The outermost point of each pitfall was 11.3cm from the nearest wall. The cups were set such that their rims were level with the substrate surface. The substrate used for the experiment was placed to a depth of 1 cm in the bottom of each trap to enable the beetles to bury themselves. Refuges made from broken clay plant pots were placed at the four comers of the arena and at the bottom of each trap. The experimental arena was situated in a plant growth room. This was maintained under conditions as described for the culture room above except that the light intensity was approximately 80,pE m-* s-' and the relative humidity varied from 60% to 70% rather than the 25 p E m-2s-'

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and a relative humidity of 5 0 4 0 % in the culture room. A Licor Inc. (U.S.A.) LI-IBSB quantum/radiometer/photometer fitted with a quantum sensor was used to measure the light intensity. A Gluck thermohydrograph was used to monitor the temperature and humidity. Ten individuals of each of the medium-sized to larger carabid species and fifteen of each of the smaller species were used. All beetles were starved for 24 h before the experiment in order to enhance foraging activity. The beetles were introduced into the arena at 17.00 hours 2 h before the start of the experiment during which period polystyrene cups, identical to those used for the traps, were inverted and placed over the traps in order to prevent premature capture. The inverted cups were removed after the 2 h period and subsequent activity was monitored over a 24 h period using time-lapse video equipment and either VHS or U-matic cassette recorders set in the 24 h time-lapse record mode. The equipment consisted of a National WV 1800B Vidicon monochrome video camera with a Fujinon CF 125C, 12.5 mm F 1.4 lens; a Melford D01-17 high resolution monochrome monitor; an NEC 9507 U-matic time-lapse video cassette recorder with time date generator and a Panasonic NV-8050 V H S video cassette recorder. The NEC video cassette recorder was used only in the first experiment for A .dorsale, T. quadrktiatus and N . brevicollis. After this time the Panasonic recorder was used, because of its better image quality during play-back. Some illumination was necessary in the dark period to enable the camera to produce an image. This was provided by two 60 W red tungsten bulbs positioned 60cm from the surface of the arena. These created a light intensity of approximately 3 p E m-2 s- at the substrate surface. Griffiths (1983) demonstrated that A.dorsale could not perceive red light from this source so it was assumed that the species used behaved in the red light as they would in the dark. The camera was positioned 100 cm from the substrate surface. This gave a field view of 45x59 cm. Pitfall trap efficiency was evaluated for each species under the following conditions: (1) Experiment 1. Silver sand was used as the substrate. Autumn-winter caught animals were used. (2) Experiment 2. Soil was used. Animals as 1. (3) Experiment 3. Sand and spring/summercaught animals were used. Also the plastic cup

pitfalls were set such that their lips were submerged approximately 1 cm below the sand surface. This experiment was camed out in an attempt to maximize the trap efficiency. (4) Experiment 4. As 1, but spring/summer-caught animals were used. Data were obtained from the video tapes during playback in the 12 h time-lapse mode. The frequency and nature of the encounters with the pitfall trap edges were recorded. Encounters with the trap edge resulted either in capture or avoidance/escape. Several categories of avoidance were noted (see Results). The speed of movement of each species was obtained by tracing the path of an individual with a permanent marker pen on an acetate sheet overlaying the monitor screen. The paths were traced from the point at which the beetle left the wall or refuge until it encountered a trap, refuge or wall. The mean speed of movement was calculated from ten tracks for each species in each experiment. The proportion of encounters resulting in c a p ture and no capture were calculated for each species. A G-test (Sokal & Rohlf, 1981) was used to evaluate whether there was overall heterogeneity of the numbers capturedlnot captured between the species for each experiment. Pair-wise G-tests, incorporating the Williams correction factor (Sokal & Rohlf, 1981), were used to compare the trap efficiency (numbers capturedlnot captured) for each species from one experiment to the next. This test was also used to evaluate the differences between each species within each experiment. A t-test was used to compare the mean speeds of movement between the experiments. The mean fresh weight of each species was recorded after 48 h of starvation. The beetles used for the experiments were weighed in groups of ten; the balance was sensitive to O.OOO1 g.
Resub

Initial reviewing of each 24 h tape revealed that N. biguffamwas almost exclusively active during the day. A.dorsale, C.melanocephalus, D.ahicapillus and N . brevicollis were almost exclusively nocturnal and C.fuscipes and T.quadristriatus were active throughout the day and night. The results given in Fig. 1 represent the capture efficiency (I), avoidance behaviours (11)

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Niger B. Hahall and Stephen D. Wratten

EXPERIMENT 1 W I N T E R S A N D LIPPED TRAP

EXPERIMENT 2 WINTER SOILLlPPEDTRAP

1 9 Z

EXPERIMENT4 SUMMER
T

SAND-

LIPPEOTRAP

EXPERIMENT 3 SUMMER S A N D LIPLESS TRAP

bq
%81.0FIG.1 . Behaviour of carabids i a pitfall-trap arena. The capture efficiency (proportion capture).( to n proportion non-capture ( 0 ) ) avoidance behaviour (proportion investigate and skirt (.)/skirt ($$) to (I); proportion investigate then retreat ( 0 ) ) (11); and speed of movement (given with 95% confidence limits) (111). Sample sizes are given above each column in observations of T p s I and 11. Key to species: ye C.f.=Calathus fuscipes; N.br.=Nebria brevicollis; N.b.=Notiophilus bigunarus; C.m.=Calarhus melanocephalus; T.q. =Trechus quadrirtriatus; A.d.=Agonum dorsale; D.a.=Demerrias atricapillus.

EY

Pitfall traps and carabid beetles

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and speeds of movement (111) for the four experiments. For the nocturnal species, results presented are from activity in the dark period only. This was because the number of encounters in the light period were very low. The proportion of encounters with the pitfall traps resulting in capture (efficiency) were low for all species throughout the experiments (Fig. 1).The greatest efficiency was 0.44recorded for N.brevicollk in experiment 3. This experiment was conducted with spring/summer-caught animals on a sand substrate with the trap type lipless. The lowest efficiency achieved was 0, recorded for D.atricapillus in experiment 4 . This experiment used spring/surnmer-caught animals with lipped traps set in a sand substrate. G-tests showed that there was overall heterogeneity in the capture efficiencies between the species for each of the experiments (P<O.001 for experiments 1,3 and 4; P~0.005 experiment for 2). Throughout the experiments D.atricapil1us was the least susceptible to capture. This species, unlike the others, never fell in the traps. On many encounters individuals of this species walked into the trap, spiralling down the walls, and then walked out. The few captures recorded resulted from individuals remaining inactive in the bottom of the trap, rather than being trapped there. C.fuscipes was one of the species more susceptible to capture in the first three experiments. However, in the experiment in which the spring/summer-caught animals were used on a sand substrate containing lipped traps it was one of the least susceptible. The pair-wise G-test used to compare the performance of individual species from one experiment to the next showed that there were no differences in capture efficiencies between the autumn/winter-caught carabids used on a sand substrate containing lipped traps (experiment 1) and the autumn/winter-caught carabids used on a soil substrate containing lipped traps (experiment 2). Differences did arise for some species when comparing experiment 1 with experiment 3 (spring/summer-caught carabids used on a sand substrate containing lipless traps). N. biguttatus and T.quadrktriatus were more readily caught in experiment 1 (P<O.Ol). Trap efficiency was greater in experiment 3 than it was in experiment 2 for N . brevicollis (R0.05).For N . biguttatus, however, the situation was the opposite (P<0.05). Two distinct types of avoidance behaviour

were recorded (Fig. 1). In the first, carabids approached the edge of the trap, lowered their bodies into the mouth of it and hung on with their hind legs; this will be termed investigate from now on. Within a few seconds they retreated. In the second type of avoidance behaviour the carabids approached the edge and skirted around it without any lowering into the trap. A number of the individuals that skirted also investigated, so this behaviour was therefore added as a subcategory of skirting. D.atricapillus, the species least prone to c p a ture, avoided being caught mainly by employing the skirting behaviour. C.melanocephalus evaded the traps mainly due to its investigate and retreat behaviour. For the other species neither of the avoidance behaviours predominated. There appeared to be no relationship between the capture rate and the type of avoidance behaviour. NO correlation between the mean fresh weight of each species and its capture rate was obtained. All of the species studied moved significantly faster in experiment 4 (that is the experiment using spring/summer-caught carabids for which speed was measured) than they did in experiment 1 (autumn/winter-caught carabids) (P<O.Ol for A.dorsale and D.atricapillus; P<O.001 for C .fwcipes, C.melanocephalus, N. biguttatus, N .brevicollk and T.quadristri&). Overall the speeds of movement did not differ between the experiment conducted on sand using carabids caught in the autumn/winter and the experiment using soil. There were two exceptions however; C.fiLFcipesmoved faster on the soil (P<O.OOl)and D.atricapillus moved faster on the sand (P<O.oOl).
Discussion

The low capture rates observed throughout the experiments were unexpected in the light of previous work. Luff (1975). working on factors influencing the efficiency of pitfall traps, found that the least efficient trap (a straight-sided can of tin plate) caught seventy-four A.dorsale in 100 encounters. The highest capture rate obtained for A.dorsale in the present work was 9% in experiments 2 and 3. However, Luff made his observations during normal daylight. As the present work and that of Luff (1978) have both classified A.dorsale as being nocturnal, any data

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Nigel B. Halsall and Stephen D . Wratten

carabid moved significantly faster than the autumn/winter-caught ones. This was of no consequence since the speed of movement did not affect capture rate. The carabids used for this work were collected from arable land and associated hedgerows. The sand substrate used for three of the experiments was therefore artificial. However, the lack of difference between the capture rates on the differing substrates demonstrated that the behavioural response to pitfalls was not altered by the sand medium. D.am.capillus has very effective adhesive setae on the tarsi (Stork, 1980) enabling the species to be a very adept climber (Lindroth, 1974). This study demonstrated that D.am*capillus evaded capture as a result of its climbing ability. So it may be concluded that this, and any other climbing-species, would be poorly represented in field pitfall catches, even if present at high densities. The heterogeneityof capture rate between the species in each experiment has implications for previous field work camed out using pitfall t r a p ping as the sampling method. Statements concerning the composition of the epigeal fauna derived from pitfall trapping are likely to be heavily biased. Data such as those presented in this paper could be used to correct field catches. Greenslade (1964) demonstrated that pitfall trapping cannot properly be used for the quantitative population assessment of the carabid fauna of any habitat, nor should it be employed to compare the numbers of one species in different habitats. This present work shows that, as well as being poorly-related to population densities, pitfall trap catches are unreliable because species moving at similar speeds and occumng at similar densities would still differ in numbers captured. Those differences in capture rate are unrelated to beetle size, speed of movement or diurnal behaviour.
Acknowledgment

obtained from work camed out in the daylight on such species would not reflect normal behaviour responses. Van der Drift (1951) showed that diurnal Notiophilus spp. avoid traps by visual means. However, in the present study T.quadristriatus, C.fuscipes and N . biguttatus were day-active but there was little difference, if any, in the capture rate between the day active and nocturnal species. Beetle size may affect capture rate; van der Drift (1951) showed that the small Notiophilus species have the ability to evade traps. These species being small can recover balance, if unbalanced, upon coming across a trap lip, thus avoidingcapture. Luff (1975) demonstrated that beetle size was an important factor that affected its capture rate and Greenslade (1964) also showed that the size and locomotor activity of the beetle were o importance; the larger the f beetle then the greater its chance of being caught. Greenslade attributed this to the fact that because the faster-moving larger beetles cover greater distances, this would increase the rate of trap encounters. For the present work, however, efficiencytook into account encounter rate wt the trap edge and it was also found ih that differences in capture efficiency between species were not related to the size or speed of movement of the beetle. These between-species differences in capture rate are more likely to be related to the species differing abilities to perceive the trap edge. All of the species studied live for one year only and undergo a Winter dormancy period or diapause (Thick, 1977). N.brevicollk also undergoes a summer inactivity period (Penney, 1966). A. dorsale, D. amkapillur and N . biguttutus are all spring breeders (Griffiths, 1983; Coombes, 1987; Thiele, 1977); that is these species overwinter as adults. CfiLFcipes, C.melanocephalur, N .brevicollis and T.quadristriatus are autumn breeders (Thiele, 1977; Penney, 1966; Mitchell, 1%3); that is they overwinter predominantly as larvae, although a small proportion overwinter as adults (Gilbert, 1956). Therefore the autumn breeders that were collected in the autumn/winter would have been entering their second year of life. This work demonstrated that capture rates for individual species did not differ significantly between the autumn/winter and spring/summer-caught carabids. All of the spring/summer-caught

This research was supported by a grant from the

Natural Environment Research Council.
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Pitfall traps and carabid beetles

Bryan,K.M. & Wratten,S.D. (1984)Theresponsesof polyphagous predators to prey spatial heterogeneity; aggregation by carabid and staphylinid beetles to their cereal aphid prey. Ecological Entomology, 9, 251-259. Chiverton, P.A. (1984) Pitfall trap catches of the carabid beetle Pterostichus melanarius, in relation to gut contents and prey densities, in insecticide treated and untreated spring barley. Entomologia Experimentalis et Applicata, 36,23-30. Coombes, D.S. (1987) Factors limiting the effectiveness of Demetrias atricapillus (L.) (Coleoptera: Carabidae) as a predator of cereal aphids. Ph.D. thesis, University of Southampton. Dunning, R. A., Baker, A.N. & Windley,R.F. (1975) Carabids in sugar beet crops and their possible role as aphid predators. Annals ofApplied Biology, 80, 125-128. van der Drift, J . (1951) Analysis of the animal community of a beech forest floor. Tijdrchrift vor Enfomologie, 94, 1-168. Edwards, C.A., Parsons, N., George, K.S. & Heilbroon, T. (1978) Carabids as predators of cereal aphids. Annual Report of Rothamsted Experimental Station for 1977, p. 101. Gilbert, 0. (1956) The natural histories of four species of Calathus (Coleoptera: Carabidae) living on sand dunes in Anglesey, North Wales. Oikos, 7,2247. Greenslade, P.J.M. (1964) Pitfall trapping as a method for studying populations of Carabidae (Coleoptera). Journal ofAnimal Ecology, 33,301310. Griffiths, E. (1983) The feeding ecology of the carabid beetle Agonum dorsale in cereal crops. Ph.D. thesis, University of Southampton. Lindroth, C.H. (1974) Handbooks for the Identification of British Insects, 4 (2), 1 4 8 . Luff, M.L. (1975) Some features influencing the efficiency of pitfall traps. Oecologia (Berlin), 19,345357.

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Luff, M.L. (1978) Die1 activity patterns of some field Carabidae. Ecological Entomology, 3 , 5 3 4 2 . Mitchell, B. (1963) Ecology of two carabid beetles. Bembidion lampros (Herbst) and Trechus quodrisiriatus(Schrank). I. Life cycles and feeding behaviour. Journal of Animal Ecology, 32, 289299. Obrtei, R. (1971) Number of pitfall traps in relation to the structure of the catch of soil surface Coleoptera. Acta Entomologica Bohemoslavaca, 68,3oQ309. Penney, M.M. (1966) Studies on certain aspects of the ecology of Nebria brevicollis (F.) (Coleoptera, Carabidae). Journal of Animal Ecology, 35, 505512. Potts, G.R. & Vickerman, G.P. (1974) Studies on the cereal ecosystem. Advances in Ecologicul Research, 8, 107-197. Sokal, R.R. & Rohlf, F.J. (1981) Biometry, 2nd edn. Freeman, New York. Southwood, T.R.E. (1978) Ecological Methodr with Particular Reference to the Study of Insect Populations, 2nd edn, pp. 236-237. Chapman and Hail, London. Stork, N.E. (1980) A scanning electron microscope study of tarsal adhesive setae in the Coleoptera. Journal of the Linnean Society, 68, 173-306. Sunderland, K.D. (1975) The diet of some predatory arthropods in cereal crops. Journal of Applied Ecology, 12,507-515. Sunderland, K.D. & Vickerman, G.P. (1980) Aphid feeding by some polyphagous predators in relation to aphid density in cereal fields. Journal ofApplied Ecology, 17,389-396. Thiele, H.U. (1977) Carabid Beetles in their Environments. Springer, Berlin.

Accepted 5 December 1987