Predator -Prey Interactions

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STUDIES ON PREDATOR -PREY INTREACTIONS IN THE SOIL

Nur Tjahjadi

UPSI Tanjung Malim, www.upsi.edu.my

Abstract

Three techniques, pitfall traps, rhizotron observation and time lapse photography were used to study the effect of predators on insect resting stages above and below ground. Locust and stick insect eggs, mustard beetle and mealworm pupae were compared as possible baits for increasing activity. Mealworm pupae (Tenebrio molitor) were selected. A time lapse cinematographic technique was developed and using an analysing projector, it was found that an eight minute interval between frames maximised the number of significant results obtained per unit cost. The parameters measured were pupal disappearance, contacts between predators and prey and the identity of predators. The results showed that predation was highest at the surface and lowest at 6 cm. Predator activity differed with depth according to taxa. Staphylinid activity was greatest at the soil surface, carabid activity predominated at the surface and 3 cm, whereas geophylid centipedes and campodeans proved to be subterranean with greatest activity at 3 cm and 6 cm. They were rarely or never encountered in pitfall traps. Observations on seasonal changes in predator activity above and below ground showed that predators were most active at contacting pupae in the spring and summer. However, variabilityin activity within a season such as the summer could be as great as between season. It was concluded that predation is a significant risk to below ground resting stages throughout the the year. All predatory groups were more active during darkness. A crop insecticide and a soil insecticide affected predatory activity mostly at the surface during the first three days only.

Keywords: Predator, prey, pitfall traps rhizotron, time lapse cinematography

INTRODUCTION

Plant material in the soil is characterised by dense root systems, the biomas of which may exceed that above ground several-fold (Sims & Singh, 1978). These dense root systems develop in part in response to intense competition between plants and soil fauna (Newman et al., 1989). Many animals spend sometime underground, and many pests are also underground root attackers or spend part of their life cycle below ground. The British species of crop pests listed in Gratwick (1992) has been used to compile Table 1. This shows the proportion of species with underground resting stages (eggs and pupae). Also shown is the proportion of animal which over winter in the soil in some stages of their life cycle. The result show that 41 per cent of pest species lay their eggs in the soil, 65 per cent pupate there and 54 per cent overwinter in the soil (Table 1.1). The impact of below-ground predation on plant productivity has been far less studied than that of phytophagous feeding on aerial parts.

A knowledge of the activity, population density, dispersal and foraging patterns of soil predators would be of value in determining the feasibility of using them as biocontrol agents of crop pests (Vickerman & Sunderland, 1980; Best et al., 1981; Chiverton, 1986; Luff, 1987; Booij & Noorlander, 1992 and Bailey, 1994). If suitable, they may reduce the need for pesticide inputs, an aim of much present day farm practice. Our knowledge of predation below ground is still very limited. Control of underground pests is notoriously difficult, especially when they are in a resting stage (eggs or pupae). These stages are often very difficult to control with pesticides, few of which are able withstand the hostile environment for synthetic chemicals the soil provides.

One question which arises is why resting stages are placed below ground. Possible answers are that the soil offers more physically stable conditions, protection from predators and parasitoids and a relatively moister environment than above-ground.

Due to difficulty to observing soil predator and prey under field conditions, their interactions with each other remain largely ignored. Those studies which have been published are usually non-quantitative and in the case of feeding studies rely heavily on gut content analyses (e.g. Sunderland, 1975 and Holopainen & Helenius, 1992). The feeding behaviour of predators has often been determined in the laboratory rather than in the field (Zhao et al., 1990 and Chaabane et al., 1993).

Quantitative information on the predator - prey interactions in the soil is necessary if effective pest management systems for soil insect pests are to be develop (Edwards et al., 1988). Several studies have indicated that plant protection measures have considerable effects on the population density of earthworms, carabids, staphylinids and other soil organisms (e.g. Nelemans, 1987, 1988; Loreau, 1988; Luff & Rushton, 1988; IPPG, 1989; Luff et al. 1989; Good & Giller, 1991; Cardwell et al, 1994 and Frambs, 1994).

Predation is process that involves interactions between prey defences and the foraging tactics of predators (Godfray & Pacala, 1992 and Malcolm, 1992) In studies of ground surface predator - prey interctions, it is commonplace to relate feeding and foraging behaviour simply by gut content analyses and pitfall trap data, but in the case of below-ground predation, this is more difficult.

Sunderland (1975) found solid food items in the guts of 7 species of carabids, 2 species of staphylinids and one species of lithobiid centipede, but many of the carabids only ingested the fluid contents of their prey. He also found that 15 species of staphylinids had no trace of solid remains in the guts.

Edwards et al. (1979) studied the effect of predation by carabids and othe polyphagous predators on the population of cereal aphids. Loughridge & Luff (1983) tested one species of carabid (Harpalus rufipes Degeer) in the laboratory and the field to see if it fed on aphids. Sunderland et al. (1987) studied a total of 7781 predators belonging to 105 species, and 81 species were found to have eaten aphids. They also showed that staphylinids (both larvae and adults) digested their aphid meal much more rapidly than did carabids and spiders.

Pitfall trapping is useful technique for the study of diverse assemblages of epigeal organisms. Modifications and adaptation made to pitfall traps have been reviewed by Southwood (1978) and Spence & Niemala, 1994. The interpretation of ecological information obtained by these traps has been extensively described. Many authors have suggested that differential species activity, weather conditions and trap placement influence results to such an extent that ecological inferences are difficult to make. Nevertheless, studies are being made which aim to improve the quantitative estimates of carabid populations using pitfall techniques (Clark et al, 1995).

Proponents of the method favour pitfall trapping because it allows continuous unattended sampling over a 24 hour period, and extended trapping equalises the effects of weather. Pitfall trap also permit several sites to be studied simultaneously and the number of animals caught is independent of the sampler's skill. The interaction between predator and prey in the soil cannot be measured by pitfall trapping alone and the reservations expressed by the opponents of pitfall traps should always be borne in mind.

Direct observation of the soil and the events occurring in it can be made using by rhizotrons. These can be of two types; minirhizotrons which use a series of glass tubes inserted into the soil, down which television monitored endoscopes can be inserted to view the soil profile; and large fixed rhizotrons, which are buried chambers with windows along the sides looking out into the soil profile (Carpenter et al. 1985).

The rhizotron used in the present study has previously been described by Sackville-Hamilton et al. (1991). It was designed to allow observations to be made on root herbivores and predator-prey interactions in the soil at different depths.

The main problem with rhizotron observations is that the population of predatory soil anthropods are patchily distributed, the predation process is quick and the number of predators seen in the rhizotron at any one time is small. These problems are even more acute for the users of minirhizotrons, where the area viewed is small, and the observation periods are short. These problems can be minimised by introducing baits to attract the soil fauna and by using time lapse cinematography, to scan long time periods during which little may be happening.

Predatory arthropods are typically abudant in the turf habitat (Cockfield & Potter, 1985), but their importance in regulating densities of pest arthropods in the soil is poorly documented. The predator population is rich in genera and species of beetle families Carabidae and Staphylinidae. Very many studies, recent examples being Wiedenmann et.al. (1992), Fan et.al. (1993), Clark et.al. (1994), Lys (1995) and Tolonen (1995) stress that the epigeal predator fauna is dominated by carabids.

These studies have indicated the importance of carabid predation in particular situations and against particular prey types. These beetle are generally polyphagous and the predator/prey interactions studied include such diverse prey as cutworms (Best & Beegle, 1977 and Brust et al. 1985, 1986), codling moth larvae (Riddick & Mills, 1995), aphids (Dixon & McKinlay, 1992; Holopainen & Helenius, 1992 and Ekbom, 1994), armyworms (Clark et al. 1994), colorado beetle (Cappaert et al. 1991; Heimpel & Houghgoldstein, 1992), cricket eggs (Griffith & Poulson, 1993), hemipteran eggs (Filippitsukamoto et al. 1995), slugs (Symondson & Liddell, 1995) and snails (Digweed, 1993). The papers quoted are a small sample of an extensive literature, most of which concentrates on the role of these beetle as epigeal predators. If one seeks information on their role below the soil surface it is much more difficult to find. Chaabane et al.(1993) has shown that carabids will feed on earthworm flesh in the laboratory and the gut content analysis (Holopainen & Helenius, 1992) has shown that collembola are ingested although these may not have been true soil dwelling species. The searching and foraging behaviour of carabids has been studied on the soil surface by using pitfall traps in the corn fields (Best et al.1994), soyabean fields (House & All, 1981), cereals (Edwards et al. 1988) and potatoes (Armstrong, 1995).

In the laboratory and in the field, Griffith & Brown (1992) examined foraging effort by assessing the number of holes dug by carabids to reach a buried cricket egg. Using antigens, Symondson & Liddell (1995) showed that carabids could forage into the soil for slugs. Filippitsukamoto et al. (1995) reported that carabids were the first known predators of hemipteran eggs laid in the soil. Humphreys & Mowat (1994) reported that carabids were the predators of cabbage root fly.

A body of theory views predation from the perspective of an economic process consisting of benefits derived from capturing and consuming prey versus the cost associated with obtaining energy (energy expended to pursue, capture and subdue a prey). The most successful predator maximises its energy intake per unit time or minimises its time spent acquiring a given amount of energy (Malcolm, 1992) The latter strategy minimises the risk of predation to the searcher.

Prey items (species, age class and quality) are assumed to exist in patches and it is also assumed that these patches differ in prey density or quality. The forager exploiting and choosing patches in a manner that maximises energy intake or maximises its prey encounter rate.

The theory assumes that these rules, evinced as behaviour, are subject to natural selection and predators which possess the most effective set of rules (e.g. those that lead to maximising energy intake) are the most fit, ie, they contribute most to the reproducing gene pool of the next generation.

Predators are believed to be important agents of selection and to elicit an impresive variety of adaptations in prey. The criteria outlined above suggest that selection in favour of antipredatory traits can occur only when some members of a prey population survive to reproduce after being detected, that is, when predators are less than 100 per cent efficient at one or more stages of their interactions with prey.

Prey animals have available to them numerous ways of avoiding predation. Not all these ways are equally effective, nor are they appropriate for all phase of an encounter with a given predator.

For a given phase of predation, the definiton of efficiency of antipredatory defence is the number of encounters that result in prey survival during the phase in question divided by total number of encouters in that phase. The overall antipredatory effectiveness is the subjugation phase (Ives & Dobson, 1987).

In many situations, it is difficult to measure the relative abudance and efficiency of predators. Predator impact depends upon such unknowable quantities as the predators rate feeding, time of feeding, selectivity and rate of encounter with the prey. Some of these relationships could be reconstructed if predators victims can be recognised.

An alternative approach is to study predation by offering baits Chaabane et al. (1993) used earthworm flesh as baits for carabids in the laboratory. Carcamo (1994) employed fly pupae as a bait for carabids to observe pupal disappearance in some crops. Lys (1995) has used artificial prey to calculate predation rates of carabid and staphylinids in winter wheat. Tolonen (1995) used Drosophila melanogaster pupae as bait to measure predation rates.

If predators leave measurable or countable traces of their activity on unsuccessfully attacked victims, the proportion of the prey population that was exposed to non-lethal attack during the subjugation phase can be calculated.

The nature and effectiveness of antipredatory defences can be evaluated by measuring the efficiency with which predators detect, pursue and subdue prey. The most effective defences of the prey is that used during the phase of predation in which efficiency of the predator is lowest.

The present study was confined to soil protection in an area of pasture. Initially, it was important to survey the area, establish which predators formed the dominant elements in the community and compare the efficiency of the proposed methods of observation. It was also necessary to decide upon suitable prey stages to utilise as baits in this study.

Prey defences have long interested biologists due to the extraordinary diversity of ways in which animals reduce the impact of predation. Endler (1988) categorised defences by their effectiveness in interrupting the behavioural sequence of a foraging predator through at least five stages - prey detection, identification, approach, subjugation and consumption.

Insects are potentially very vurnerable when in one of the immobile stages in the life cycle, i.e. eggs. Diapausing (overwintering) larvae and adults and pupae. These stages are found in a wide variety of species and it may be postulated that one reason for so many of these occurring in the soil is defence against predation. The assumption is that underground predation is more difficult and less common. Eggs can be laid in the soil at different depths, slugs for example, are able to lay eggs at 25 cm or more below ground and insect larvae may also pupate at different depths. The placement of resting stages in the soil requires the expenditure of energy, which may be presumed to increase with increasing depth. This expenditure would only be justified if depth was an important parameter in the protection of prey.

The effects on predator - prey interaction on prey buried at different depths is a major part of the present studies. Laboratory and field work have been carried out to determine : (1) how quickly predators find prey at different depths, (2) how rapidly the prey disappear (survival time of the prey at each depth), (3) which predators are active at each depth, (4) and the rate of predation at each depth. Superimposed upon these studies are the influences of seasonal and diurnal changes on predator activity.

Finally, a very important practical factor influencing predation in the soil is the impact of using insecticides. Without such data, there is no possibility of developing integrated pest management systems, and the effect of soil insecticides was incorporated into this study.

The research programme centred around four techniques: the use of pitfall traps, the rhizotron, laboratory experiments and time lapse cinematography to record predator - prey interaction. These were employed in parallel to observe how predator use a given environment most efficiently and how predatory success is influenced by time (seasonal changes) and place (different depth).

Table 1. The Proportion of invertebrate pests with resting stagaes in the soil (Gratwick, 1992)

Pest No. of % Below ground

Groups species cited Eggs Pupae Overwintering

Hemiptera 49 22 - 16

Thrips 2 0 - 0

Lepidoptera 47 9 34 36

Coleoptera 39 74 90 90

Diptera 34 44 79 79

Mites 15 0 - 0

Milipedes 5 100 - 100

Symphylids 3 100 - 100

Slugs 16 100 - 100

Snails 4 100 - 100

Overal 214 41 % 65 % 54 %

MATERIALS AND METHODS

The experiments were carried out at Treborth Botanic Garden, University of Wales, Bangor, Using pitfall traps, a rhizotron previously described by Sackville-Hamilton, et al (1991) and time lapse photography. Between January 1993 and December 1995, numbers of predatory soil arthropods were recorded using 20 pitfall traps. Traps used here simply consisted of plastic jars (7.5 cm high and diameter 6.0 cm at mouth). The rhizotron contains 34 windows (90cm x 50 cm) which allow the soil profile to be observed from 5-10 cm above the surface, down to 100 cm below. A time lapse camera was set up in one of the rhizotron windows to record predator - prey interactions.

Predator activity was defined in these observations as the number of times a predator contacted a given prey. In preliminary experiments with no baits, no predators were recorded during three days of filming and this was time consuming and unacceptably expensive. A time lapse unit was set up, composed of 4 sub units : camera motor, control unit, timer unit and flash. Colour possitive fim (Kodachrome 25, 16 mm x 30 m, containing 4,000) frames was used.

Locust and stick insect eggs, mustard beetle and mealworm pupae were compared as possible baits for increasing activity. Mealworm pupae (Tenebrio molitor) were selected. A time lapse cinematographic technique was developed and using an analysing projector, it was found that an eight minute interval between frames maximised the number of significant results obtained per unit cost. The parameters measured were pupal disappearance, contacts between predators and prey and the identity of predators.

RESULTS AND DISCUSSION

This study is one of the few attempts to assess the activity and importance of subterranean predation on the resting stages of insects, and the field study has been made possible by the use of a rhizotron which allows direct observation to be made. Oksamen et al. (1985), studying small predators and their prey emphasized that experiments should be performed under as natural condition as possible and this has been a guiding principle in the present work.

The use of a rhizotron is not however without problems.

1. It is difficult to identify soil dwelling organisms to species when they are behind glass and are active, and when they cannot be caught and killed without creating unacceptable levels of disturbance. This necessitates the use of broad taxa for classification and this is never satisfactory.

2. The area of soil profile which can be viewed is limited by the size of the windows and as ut is not possible to see any distance into the soil, it is virtually two dimensional, so that the volume of habitat which can be inspected is highly restricted. As a consequence, interactions between animals are rarely observed and the observational food web published by Gunn and Cherrett (1993) had to be based on years and years of regular observation. More frequent observations are only made possible by placing resting stages next to the windows in artificially high concentrations and after considerable soil disturbance. Moreover the prey chosen were not normally found in the soil and so may have been much less resistant to predator attack than resting stages normally found there. In effect, predators were attracted by artificial baits.

3. It is not known what unnatural effects the glass windows of the rhizotron introduce into the system. They produce a solid surface that is an obstacle for animals and plant root movement; the temperature could be effected and there will be some light effects, if only from the electronic flash of the time lapse camera. The substantial clay content of the soil (Sackville-Hamilton, et al. 1991) means that it cracks in drought conditions. These cracks always occur between the window and the glass, so opening fissures down which animals can move. This addressed in paper 5 where it is seen to be a common event even when no glass is involved. However, attempts were made to minimize soil retraction by irrigation.

4. As the investments in the rhizotron is substantial, it is not feasible to replicate it in different soil types or within the soil type.

Nevertheless, we can begin to record and measure the incidence of predation underground, in a way which has previously not been thought possible (McBrayer and Reihle, 1971). More especially, rhizotron observations extend the observations on surface active predators and add much new information on the activity of true soil invertebrates such as geophylid centipedes and diplurans.

Even when artificially placed prey are used, contact with potential predators occurs infrequently and recording these events at one speed, but viewing at another so that events are greatly speeded up (time lapse), allows rapid scanning, followed by concentration on those periods when activity is occurring. Lussenhop et al. (1990) observed soil invertebrate activity using a video camera, but the continous lights required by the video may disrupt predator activity and increase the temperature of the soil. Time-lapse cinematography has the advantage of using electronic flash, which circumvents these problems. However it is not without disadvantages, and selecting the time-lapse interval (8 minutes in the present study) is a compromise between saving time and resources and the increasing likehood of missing key events. In the present study, contacts between prey and predators are recorded, and continous feeding is readily observed, but the actual act of killing the prey is much less frequently seen.

Not all resting stages are equally vulnerable to predator attack in the soil, and the pupae of T. molitor were selected as a prey in the present study, because they are more vulnerable than the eggs tested. Stick insect eggs appeared to be well protected by their hard shells, and the emerging nymphs would escape from the soil, whilst mustard beetle pupae were small, and again many emerged before being attacked. These must represent some of the ways in which resting stages escape predation, but these defence mechanisms were not explicitly studied in the present thesis.

The number of contacts with potential prey is an easily measured parameter used extensively in the present study. It is a measure which reflects both the population of predators and their activity, in a similar way to catches in a pitfall trap. However unlike pitfall traps, where individuals are caught only once, the number of contacts per prey often reflects repeated contact by the same predator as it investigates and then begins to attack and feed on the pupa. To this extent, contacts are not independent events and this introduces statistical problems. However, in the present study, it is the number of contacts which is of interest, as it reflects the level of danger to which the prey is exposed and this measure carries no important implications about the number of predators involved. The technical effect is to produce aggregation in the counts for the number of contacts.

The present study has shown that typical surface active predators such as carabids and staphylinids which are encountered frequently in pitfall trap studies, also hunt below ground. In the case of laboratory studies, it is clear that they can burrow through loose soil and retrieve pupae from at least 6 cm. However, this energetically expensive hunting method is used much more frequently when the more readily available prey on the surface have been consumed. In the rhizotron, it was shown that supplying artificial tunnels from the surface to the lower layers where pupae were placed, greatly enhanced their rate of disappearance. There was also evidence that in dry conditions when the soil began to contract back from the glass, predators foraged down these cracks, and this can sometimes be seen in the films. The studies on the extent of cracking in the clayey soils of Treborth show that this is a natural and extensive phenomenon in dry weather, and must provide a substantial extension of the foraging range for these normally surface active animals (see paper 5). Some groups such as carabids seem to penetrate deeper, and play a more important role than others such as staphylinids.

What the present study has shown is the important role of the true underground fauna, which are not normally sampled in pitfall traps. Diplurans are a dominant group in this area. Although it is less clear how often they are responsible for killing a healthy pupa, there is no doubt of their importance in exploiting the pupae once they have died. Similar comment can be made about the roles of slugs and earthworms. Geophilid centipedes are specifically adapted to an underground predatory life style, where they use existing tunnels, often earthworm tunnels to move about. This has important implications for resting stages, which will be at increased danger of attack if they use existing worm burrows, or if a worm contacts them during the process of burrowing.

The ways in which underground predators interact is important but not understood. The intriguing observations in paper 5 suggest that as the surface predators penetrate further underground once resources on the surface become exchaused, the obligatory underground feeders such as Campodea go deeper. It may be that this is a response to increased competition for food, or it may be that predators such as carabids and staphylinids will also attack Diplura, which take avoiding action. In either event, the very deepest prey will come under increased pressure.

In general, the data collected in this study, both for the number of contacts with predators and the frequency of pupal disappearance, all suggest that it is safer for resting stages to be underground rather than on the surface and the deeper the animal goes the safer it becomes. Moreover, the diversity of predators is reduced with depth. Predation above ground by invertebrate predators is markedly relaxed during the winter, as the cold conditions, for which the overwintering inactive forms are an adaption, will also reduce the activity of predators. Vertebrate predators by contrast are likely to enhance their predation on these forms, as they must continue to find food over the winter to maintain body temperature, and there are few active invertebrates to hunt. At this time af the year, birds, shrews and rodents may be important surface active predators. By contrast, we have seen in Chapter 6 that invertebrate predators remain active below ground throughout the winter. Vertebrates as underground predators are restricted by the high energy costs of traveling. Moles specialize on large energy-rich and abundant lumbricid fauna could not survive on insect resting stages. Birds rely on bill length to probe into the soil, rather than on digging, and this is most effective in wet muddy conditions. The fact that so many insects do overwinter in the ground (Table 1) is a measure of the protection they must receive from adverse climatic conditions, vertebrate predators, and the difficulty of being located at depth even by specialized subterranean predators.

The rates at which Tenebrio pupae disappeared even at depth in the present study, should not however be taken to represent normal rates of disappearance. As stated, these pupae have not been selected for a subterranean life style (Beddington, 1975); they are present in much greater densities, and at much higher levels of aggregation that would normally be the case, and the earth had to be disturbed to place them there. All these factors may enchance rates of loss (Hassels & May, 1974; Hassel et al. 1976; Hassel et al. 1977; Hassel, 1985; Hassel & May, 1986 and Hassel, 1987).

Nevertheless, the rates of disappearance revealed suggest that underground predation is likely to be an important parameter in insect population dynamics, and so of concern to pest managers. It is therefore of interest to note the impact of pesticides on soil predation. In the studies on both overground and soil insecticides, pupal disappearance and predator contact with prey were reduced immediately after application, but the effects proved short-lasting, and relatively unimportant at depth.

However, it must be remembered that an important element in the effects that any insecticide have on natural communities is the area treated. Mobile animals quickly reinvade insecticide-treated areas, once the effects of the insecticide wear off, as they do rapidly with modern low persistence chemicals (Murdoch, et al. 1985; Murdoch & Oatens, 1988 and Judd & Mason, 1995). In the present experiments, the areas treated were only one square meter each. It is also difficult to disentangle the effects that low doses of insecticides have on mortality, compared with repellency. The latter only protects prey and predators if, as in this case, there is a small scale mosaic of treated and untreated areas, but the present study is interesting in its implications that treatment might (presumably through repellency) drive predators deeper into the soil. The effects observed are generally similar both with an insecticide which is likely to reach the soil only as run-off from crop spraying (permethrin) and with a more specifically designed insecticide for soil pests (dursban). An interesting extension of this would be to compare insecticide formulations such as granules, which are now commonly used for soil applications.

However, the results in general confirm the view that the soil is a robust ecological system, rather resilient to pesticide damage with its highly active microbial flora which can break down a wide range of chemicals, and its finely divided mineral and organic content which can adsorb both the pesticides and their breakdown products. It is for these reasons that soil animals are so difficult to control chemically, and why perhaps soil predators can also recover rapidly.

A study such as this usually raises more questions than it solves, and the reasons why some groups such as Diplura should show a strong preference for nocturnal activity, when they operate deep within the soil is unknown. However, it is hoped that the present study has shown that the use of rhizotrons can illuminate an important, and much neglected area of ecology, namely the activity and population dynamics of soil organisms.

Reference

Armstrong, G. 1995. Carabid beetle (Coleoptera, Carabidae) diversity and abundance in organic potatoes and conventionally grown seed potatoes in the north of Scotland. Pedobiologia 39: 231-237.

Asteraki, E.J. 1993. The potential of carabid beetles to control slugs in grass clover swards. Entomophaga 38: 193-198.

Asteraki, E.J., Hanks C.B. and Clements, R.O. 1992. The impact of two insecticides on predatory ground beetles (Carabidae) in newly sown grass. Annals of applied Biology 120: 25-39.

Bailey, R.R., Vandenberghe, E.P and McCarthy, B.C. 1994. New records and activity patterns of carabid beetles (Coleoptera, Carabidae) in Western Maryland. Coleopterist Bulletin 48: 319-323.

Beddington, J.R. 1975. Mutual interference between parasitoids or predators and its

effect on searching efficiency. Journal of Animal Ecology 44: 331-340.

Best, R.L. and Beegle, C.C. 1977. Food preference of Five species of carabids commonly found in Iowa cornfields. Environmental Entomology 6: 9-12.

Best, R.L., Beegle, C.C., Owents, J.C. and Oritz, M. 1981. Population density, dispersion and dispersal estimates for Scarite subriatus, Pterostichus chalchites and Harpalus pennsylvanicus (Carabidae) in lowa cornfield. Environmental Entomology 10: 847-856.

Booij, C.J.H. and Noorlander, J. 1992. Farming systems and insect predators. Agriculture Ecosystems and Environment 40: 125-135.

Brust, G.E., Stinner, B.R. and McCartney, D.A. 1985. Tillage and soil insecticide effects on predator black cutworm (Lepidoptera: Noctuidae) interactions in corn agroecosystems. Journal of Economic Entomology 78: 1389-1392.

Brust, G.E., Stinner, B.R. and Mc.Cartney, D.A. 1986. Predation by soil inhabiting arthropods in intercropped and monoculture agroecosystems. Agriculture Ecosystems & Environment 18: 145-154.

Carcamo, H.A. and Spence, J.R. 1994. Crop type effects on the activity and distribution of ground beetles (Coleoptera, Carabidae). Environmental Entomology 23: 684-692.

Cardwell, C., Hassall, M. and White, P. 1994. Effects of headland management on carabid beetle communities in Breckland cereal fields. Pedobiologia 38: 50-62.

Cappaert, D.L., Drummond, F.A. and Logan, P.A. 1991. Incidence of natural enemies of the colorado potato beetle, Leptinotarsa decemlineata (Coleoptera, Chrysomelidae) on a native host in Mexico. Entomophaga 36: 369-378.

Carpenter, A., Cherrett, J.M., Ford, J.B., Thomas, M. and Evans, E. 1985. An inexpensive rhizotron for research on soil and litter living organisms. Ecological interactions in soil. Eds. A.H. Fitter, D. Atkinson, D.J. Read, and M.B. Usher. Blackwell Sci. Publ. Oxford.

Chaabane, K., Josens, G. and Loreau, M. 1993. Quantitave assessment of consumption by Abax ater Villers (Coleoptera, Carabidae). Pedobiologia 37: 291-302.

Chiverton, P.A. 1986. Predator density manipulation and its effects on populations of Rhopalosiphum padi (Hom., Aphididae) in spring barley. Annals of applied Biology 109: 49-60.

Clark, M.S., Luna, J.M., Stone, N.D. and Youngman, R.R. 1994. Generalist predator consumption of armyworm (Lepidoptera, Noctuidae) and effect of predator removal on damage in no-till corn. Environmental Entomology 23: 617-622.

Clark, M.S., Luna, J.M. and Youngman, R.R. 1985. Estimation of adult carabid absolute densities in a no-till corn field by removal sampling. Applied Soil Ecology 2: 185-193.

Cockfield, S.D. and Potter, D.A. 1985. Predatory arthropods in high and low maintenance turfgrass. Canadian Entomology 117: 423-429.

Digweed, S.C. 1993. Selection of terrestrial gastropod prey by cychrine and Pterostichine ground beetles (Coleoptera, Carabidae). Canadian Entomology 125: 463-472.

Dixon, P.L. and McKinlay, R.G. 1992. Pitfall trap catches of and aphis predation by Pterostichus melanarius and Pterostichus madidus in insecticide treated and untreated potatoes. Entomologia Experimentalis Et Applicata 64: 63-72.

Edwards, C.A., Sunderland, K.D. and George, K.S. 1979. Studies on Polyphagous predators of cereal aphids. Journal of Applied Ecology 16: 811-823.

Edwards, C.A., Skinner, B.R., D. and Rabatin, S. (Eds) 1988. Biological interactions in soil. in Book Review of Journal of Animal Ecology 60: 1100-1101.

Ekbom, B. 1994. Arthropod predators of the pea aphid, Acyrthosiphon pisum Harr. (Hom., Aphididae) in peas (Pisum sativum L ), clover (Trifolium pratense L) and alfalfa (Medicago sativa L). Journal of Applied Entomology - Zeitschrift fur Angewandte Entomology 117: 469-474.

Endler, J.A. 1988. Frequency-dependent predation, crypsis and aposematic coloration. Phil.Trans.R.Soc.Lond. B 319: 505-523.

Fan, Y.Q., Liebman, M., Groden, E. and Alford, A.R. 1993. Abundance of carabids and other ground-dwelling arthropods in conventional versus low-input bean cropping system. Agriculture Ecosystems & Environment 43: 127-139.

Filippitsukamoto, L., Nomakuchi, S., Kuki, K. and Tojo, S. 1995. Adaptiveness of parental care in Parctstrachia japonensis (Hemiptera, Cydnidae). Annals of the Entomological Society of America 88: 374-383.

Frambs, H. 1994. The importance of habitat structure and food supply for carabid beetles (Coleoptera, Carabidae) in peat bogs. Memoirs of the Entomological Society of Canada 169: 145-159.

Godfray, H.C.J. and Pacala, S.W. 1992. Aggregation and population dynamics of parasitoids nd predators. American Naturalist 140:30-40.

Good J.A. and Giller, P.S. 1991. The effect of cereal and grass management on staphylinid (Coleoptera) assemblages in South West Ireland. Journal of Applied Ecology 28:810-826.

Gratwick, M. 1992. Crop pests in the UK. Chapman & Hall. London UK. 490p.

Greenslade, P.J.M. 1964. Pitfall trapping as a method for studying populations of Carabidae (Coleoptera). Journal of Animal Ecology 33:103-110.

Griffith, D.M. and Brown, J.S. 1992. A null model of patch assessment with an application to a carabid cave beetle. Oikos 64: 523-526.

Griffith, D. M. and Poulson, T.L. 1993. Mechanisms and consequenses of intraspesific competition in a crabid cave beetle. Ecology 74: 1373-1383.

Gunn, A. and Cherrett, J.M. 1993. The exploitation of food resources by soil meso- and macro invertebtates. Pedobiologia 37: 303-320.

Hassel, M.P. and May, R.M. 1974. Aggregationin predators and insect parasites nd its effect on stability. Journal of Animal Ecology 43: 567-594.

Hassel, M.P., Lawton, J.H. nd Beddington, J.R., 1976. The component of arthropod predation. I. The prey death-rate. Journal of Animal Ecology 45: 135-164.

Hassel, M.P., Lawton, J,H. and Beddington, J.R., 1997. Sigmoid functional response by invertebrate predators and parasitoids. Journal of Animal Ecology 46: 567-594.

Hassel, M.P., 1985. Insect Natural enemies as regulating factors. Journal of Animal Ecology 54: 323-334.

Hassel, M.P. and May, R.M. 1986. Generalist and spesialist natural enemies in insect predator-prey interactions. Journal of Animal Ecology 55: 923-940.

Hassel, M.P., 1987. Detecting regulation in patchily distributed animal populations. Journal of Animal Ecology 56: 705-713.

Head, G.C. 1973. Shedding of roots. In, Shedding of plant parts (ed, T.T.Kolowski) pp. 237-293. Accdemic Press, New York.

Heimpel, G.E. and Houghgoldstein, J.A. 1992. survey of arthropod predators of Leptinotarsa decemlineata (Say) 1 in Delaware Potato field. Journal of Agricultural Entomology 9: 137-142.

House, G.J. and All, J.N. 1981. Carabid beetles in soybean agroecosystem. Environmental Entomology 10: 194-196.

Holopainen, J.K. and Helenius, J. 1992. Gut content of ground beetles (Coleoptera, Carabidae), and activity of these and other epigeal predators during an outbreak of Rhopalosiphum padi. Acta Agricultural Scandinavica Section B-Soil nd Plnt Science 42: 57-61.

Huck, M.G. and Taylor, H.M. 1982. The rhizotron as a tool for root research. Advances in Agronomy 35: 1-35.

Hughes, L. and Westoby, M. 1992. Capitula in stick insect eggs and Elaisomes on seeds - convergent adaptations for burial by ants. Functional Ecology 6: 642-648.

Humphreys, I.C. and Mowat, D.J. 1994. Effects of some organic treatments on predators (Coleoptera, Carabidae) of cabbage root fly, Delia radicum L (Diptera, Anthomyiidae), and on alternative prey species. Pedobiologia 38: 513-518.

IPPG (Institute for plant protection Germany), 1989. Plant protection in agriculture and grassland in Braunschweig. Review of Applied Entomology 77: 6100.

Ives, A.R. and Dobson, A.P. 1987. Antipredator behaviour and the population dynamics of simple predator-prey systems. American Naturalist 130: 431-447.

Judd, K.W. and Mason, C.F. 1995. Colonisation of restored landfill site by invertebrates, with particular reference to the Coleoptera. Pedobiologia 39: 116-125.

Loreau, M. 1988. Determinants of the seasonal pattern in the niche structure of forest carabids. Pedobiologia 31, 5-87.

Loughridge, A.H. and Luff, M.L. 1983. Aphid predation by Harpalus rufipes Degeer (Coleoptera: Carabidae) in the laboratory and field. Journal of Applied Ecology 20: 451-462.

Luff, M.L. 1987. Biology of polyphagous ground beetles in Agriculture. Review of Agriculture Zoology 2: 237-278.

Luff, M.L., Eyre, M.D. and Rushton, S.P. 1989. Classification and ordination of habitats of ground beetles (Coleoptera: Carabidae) in North-East England. Journal of Biogeography 16: 121-130.

Luff, M.L. and Rushton, S.P. 1988. The effects of pasture improvement on the ground beetle and spider fauna of upland grassland. Aspects of Applied Biology 17: 67-74.

Lussenhop, J., Fogel, R., and Pregitzer, K. 1990. A new dawn for soil biology : video analysis of root-soil-microbial-faunal interactions. Agriculture Ecosystems & Environment 34: 235-249.

Lys, J.A. 1995. Observation of epigeic predators and predation on artificial prey in a cereal field. Entomologia Experimentalis et Applicata 75: 265-272.

Malcolm, S.B. 1992. Prey defence and predator foraging. In: Natural enemies. Ed Crawley M.J. Blackwell Scientific Publication. London.

McBrayer, J.F. and Reichle, D.E. 1971. Trophic structure and feeding rates of forest soil invertebrate populations. Oikos 22: 381-388.

Murdoch, W.W., Chesson, J., and Chesson, P.L. 1985. Biological control in theory and practice. American Naturalist 125: 344-366.

Murdoch, W.W. and Oatens, A.S. 1988. Aggregation by parasitoids and predators: effects on equilibrium and stability. American Naturalist 134: 288-310.

Nelemans, M.N.E. 1987. Possibilities for flight in the carabid beetle Nebria brevicolis (F). The importance of food during larval growth. Oecologia 72: 502-509.

Nelemans, M.N.E. 1988. Surface activity and growth of larvae of Nebria brevicolis (F) (Coleoptera: Carabidae). Nederlands Journal of Zoology 38: 74-95.

Newman, R.I., Ritz, K. and Jupp, A.P. 1989. The functioning of roots in the grassland ecosystem. Aspects of Applied Biology 22: 263-269.

Oksamen, T., Oksamen, L. and Fretwell, S.D. 1985. Surplus killing in the hunting strategy of small predators. American Naturalist 126: 328-346.

Riddick, E.W. and Mills, N.J. 1995. Seasonal activity of carabids (Coleoptera, Carabidae), affected by microbial and oil insecticides in an apple orchard in California. Environmental Entomology 24: 361-366.

Sackville-Hamilton, C.A.G., Cherrett, J.M., Ford, J.B., Sagar, G.R. and Whitbread, R. 1991. A modular rhizotron for studying soil organisms: Construction and establishment. In: Atkinson, D.. Robinson, D & Alexander, I.J. (Eds) Plant root growth: An Ecological Perspective. British Ecological Society Publication No.10 Blackwell Scientific Publications, Oxford. Pp 49-59.

Sims, P.L. and Singh, J.S. 1978. The structure and function of ten western North American grasslands II. Intra-seasonal dynamics in primary producer compartments. Journal of Ecology 66: 547-572.

Southwood, T.R.E. 1978. Ecological methods with particular reference to the study of insect populations. John Wiley and Sons. New York. 524p.

Spence, J.R. and Niemela, J.K. 1994. Sampling carabid assemblages with pitfall traps - The madness and the method. Canadian Entomologist 126: 881-894.

Sunderland, K.D. 1975. The diet of some predatory arthropods. Journal of Applied Ecology 12: 507-515.

Sunderland, K.D., Crook, N.E., Stacey, D.L. and Fuller, B.J. 1987. A study of feeding

by polyphagous predators on cereal aphids using ELISA and the gut dissection. Journal of Applied Ecology 24: 907-933.

Symondson, W.O.C. and Liddell, J.E. 1995. Decay-rates for slug antigens within the carabid predator Pterostichus melanarius monitored with a monoclonal-antibody. Entomologia Experimentalis et Applicata 75: 245-250.

Tolonen, T. 1995. Importance of generalist epigeal predator species in a cereal field - predation on baits. Journal of Applied Entomology 119: 113-117.

Vickerman, G.P. and Sunderland, K.P. 1980. Arthropods in cereal crops : nocturnal activity, vertical distribution and aphid predation. Journal of Applied Ecology 17: 755-766.

Wiedenmann, R.N., Larrain, P.L and Oneil R.J. 1992. Pitfall sampling of ground beetles (Coleoptera, Carabidae) in Indiana Soybean Fields. Journal of Kansas Entomological Society 65: 279-291.

Zhao, D.X., Boivin, G. and Stewart, R.K. 1990. Consumption of carrot weevil

(Coleoptera, Curculionidae) by 4 species of carabids on host plants in the

laboratory. Enthomophaga 35: 57-60.

Acknowledgement

I am grateful to the Department of Education of Indonesia and the British Council officials for the award and help. Dr J B Ford, Dr J M Cherrett and all Staff of School of Biological Science, University of Wales, Bangor for their encouraging and helping the research