Entomopathogenic fungi in predatory beetles (Col.: Carabidae andStaphylinidae) from agricultural fields

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ENTOMOPHAGA 40 (1), 1995, 77-85

E N T O M O P A T H O G E N I C F U N G I I N P R E D A T O R Y B E E T L E S (COL.: CARABIDAE A N D STAPHYLINIDAE) F R O M A G R I C U L T U R A L F I E L D S T. STEENBERG(I), V. LANGER& P. ESBJERG Royal Veterinary and Agricultural University,Departmentof Ecology and Molecular Biology, Section of Zoology, Biilowsvej 13, 1870 Frederiksberg C, Denmark

Prevalence of entomopathogenic fungi was studied in overwintering ground beetles (Col.: Carabidae) and rove beetles (Col.: Staphylinidae) collected from fields of lucerne, white cabbage and white cabbage undersown with white clover. In general infection levels in adult ground beetles and rove beetles were low (Carabidae: max. 7.6%, Staphylinidae: max. 7.0%). In comparison, prevalence of entomopathogenic fungi in carabid larvae was high (19-50%). At one study site an epizootic of Beauveria bassiana was observed, infecting 67% of the staphylinid Anotylus rugosus and 37% of the staphylinid Gyrohypnus angustatus. Beauveria bassiana was the predominant fungus isolated from ground beetles and rove beetles from all studied sites. Other fungal species included the hyphomycetes Metarhizium anisopliae, Paecilomycesfarinosus and Verticillium lecanii as well as Zoophthora radicans and Zoophthora philonthi (Zygomycetes: Entomophthorales). Two individuals of Anotylus rugosus were found to have a dual infection of Zoophthora philonthi and Beauveria bassiana. KEY-WORDS: Ground beetle, rove beetle, Anotylus rugosus, Beauveria bassiana, Zoophthora philonthL

Predatory beetles of the families Carabidae (ground beetles) and Staphylinidae (rove beetles) are important natural enemies of many insect pests in the agroecosystem (Thiele, 1977; Good & Giller, 1988). Removing polyphagous predators can lead to increased aphid densities (Chiverton, 1986; Helenius, 1990) and to population increase in certain lepidopteran species (Brown & Goyer, 1982). Most adult carabids and staphylinids forage actively on the ground surface, whereas the larvae frequently live below the soil surface. Abundance, activity and species composition of carabids and staphylinids are linked to the type of crop and management practices (e.g.Thiele, 1977; Luff, 1987; Andersen, 1991). Insects and other arthropods are infected by entomopathogenic fungi in nature, but little is known about the impact of biotic mortality factors, including fungal pathogens, on population dynamics of beneficial insects, e.g. the carabids (Luff, 1987). The entomopathogenic fungi Beauveria bassiana (Bals.) Vuillemin and Metarhizium anisopliae (Metch.) Sorokin have been isolated from several hundred host species (Gtisswald, 1938; Charles, 1941; Veen, 1968), including families of predacious beetles like Coccinellidae, Rhizo-

(') Present address: Danish Pest Infestation Laboratory, Skovbrynet 14, 2800 Lyngby, Denmark.

78

T. STEENBERG, V. LANGER & P. ESBJERG

phagidae and Cantharidae. These fungal species have an ubiquitous distribution, and are mainly found in soil (Domsch et al., 1980), a habitat closely linked to the life cycle of most carabids and staphylinids. Goettel et al. (1990) list a number of reports of fungal infections in carabids and staphylinids, and Larsson (1937-1940) mentions that postreproductive populations of the carabid genera Pterostichus Bonelli, Harpalus Latreille and Dromius Bonelli are, to a large extent, decimated by entomophthoralean fungi in summer. Inyayeva (1964) and Larsson (1957) reported fungal infections in carabid larvae, however, no information is available on the actual prevalence of entomopathogenic fungi in populations of carabids and staphylinids in the field. In laboratory rearings of carabids and staphylinids, however, infection by B. bassiana, M. anisopliae and other fungal species are not uncommon, and frequently these fungi cause epizootics in rearing units (Thiele, 1977; SamsCe-Petersen, L., personal communication). As both Beauveria bassiana and Metarhizium anisopliae are produced for microbial pest control (McCoy et al., 1988) knowledge of the natural occurrence of these fungi in beneficials is required for the evaluation of possible side effects. Both fungal species are relatively non-specific and are likely to influence insect species other than the target. The present study was aimed at investigating natural prevalences of fungi in carabids and staphylinids collected at different times of year from a range of crops under different cultivation methods. MATERIALS AND METHODS COLLECTIONOF SOILSAMPLES In 199 l-1992 carabids and staphylinids were sampled from three different sites, where no pesticides had been applied during the preceeding growth season. In November 1991 120 soil samples (10cm x 10 cm, depth 20cm) were taken from a field of white cabbage (Brassicae oleracea L.) (site A). Each soil sample was taken so it included a cabbage root system. In March 1992 54 soil samples (20 cm x 20 cm, depth 5 cm) were taken from a 3 year old field of lucerne (Medicago sativa L.) (site B). Both sites were located at T~strup, 15 km west of Copenhagen on a clay soil. In September 1992, soil samples were collected from an experimental field of white cabbage containing two treatments: white cabbage monoculture and white cabbage undersown with white clover (Trifolium repens L.) (site C). Twenty nine soil samples (15 cm diam., 15 cm deep) were taken in the monoculture plot and 15 from the plot undersown with white clover. Each soil sample included a cabbage root system. The field was located at Brenderup, Fyn, and the soil was a sandy loam. All soil samples were stored in plastic bags at 4~ before processing. In addition, diseased carabids and staphylinids were collected from other agricultural fields on several occasions during the investigation. EXTRACTION AND INCUBATION OF BEETLES

Live and dead beetles were extracted by hand sorting of the soil, followed by flotation in a Fenwick funnel. For soil samples from sites A and B, live as well as dead beetles of the predominant genera were collected and recorded. At site C only the most common staphylinid species Anotylus rugosus Fabricius and Gyrohypnus angustatus Stephens were collected for incubation. This allowed for examination of large numbers of the same species

79

ENTOMOPATHOGENIC FUNGI IN PREDATORY BEETLES

in contrast to collections from site A and B. Only live beetles were collected from site C. However, for each soil sample the presence of dead insects sporulating with fungus at the time of flotation was recorded, but no attempt was made to quantify this. Insects were incubated separately in 30 ml plastic cups each with a piece of moist filter paper (20~ for 8 weeks). Prior to incubation beetles collected in March were surface sterilized with 1% NaOC1 (1 rain.) followed by rinsing twice with sterile water, whereas beetles collected in autumn were not surface sterilized. During the first week of incubation, beetles were checked daily for mortality and for signs of fungal outgrowth from dead specimens. During weeks 2 to 8, beetles were checked at 3 day intervals.

TABLE 1

Prevalences of entomopathogenic fungi in overwintering ground beetles (Carabidae) sampled from lucerne (site A) and white cabbage (site B), after laboratory incubation Lucerne

White cabbage

No. infected by

Carabidae

~

No. infected by

9

9

~

2 1

2 I

1

1 l

l 1

9 18 3 4 2 45 1 24 18 1

~

~

~-

~

p

9

Imagines

Amara aenea DeGeer Amara familiaris Duftschmid Amara plebeja Gyllenhal Amara similata Gyllenhal Amara sp. Bembidion lampros Herbst Bembidion properans Stephen Bembidion obtusum Audinet-Serville Harpalus aeneus Fabricius Harpalus aflfmis Schrank Harpalus sp. Other carabids Larvae Amara fulva Miiller Harpalus sp. Other carabids

3 1

l

4 l

1

1

l

7

2

41 3

1

1

4 3

4 4

8 34

7 l

l

3

5

2

7

13

1 1

1 1

2 2

Imagines, Total

Numbers

9

0

1

10

132

3

0

0

1

4

58

L a r v a e , Total

Numbers

5

3

0

8

16

2

2

4

0

8

42

Numbers

14

3

l

18

148

5

2

4

1

12

100

2,0

0,7

12,2

100

5,0

2,0

4,0

1,0

12,0

100

TOTAL %

9,6

80

T. STEENBERG, V. LANGER & P. ESBJERG

IDENTIFICATIONOF BEETLES AND FUNGI

Adult carabids were identified according to Lindroth (1985, 1986) and adult staphylinids according to Hansen (1951, 1952, 1954). Larvae were identified to family level only, except for those specimens infected with fungus. Further identification followed Larsson (1957). Fungi were identified according to Samson (1981) and Keller (1991). DATA ANALYSIS

Data on prevalence of fungal infection from site C were analysed as a linear response function using the CATMOD procedure (SAS Institute, 1985). The probability of infection of a randomly chosen beetle was compared for the two cultivation methods (monoculture and culture undersown with clover) and for different areas of the field (blocks). The analysis was also used for testing whether the presence of dead, sporulating individuals of A. rugosus or other insects in the soil sample at the time of flotation could be connected to a higher level of infection among the living beetles from that particular soil sample. RESULTS T a b l e 1 and table 2 s h o w n u m b e r s o f beetles and p r e v a l e n c e o f different fungal species in c a r a b i d s and staphylinids respectively, f r o m the t w o study sites at T~strup (site A and B).

TABLE 2

Prevalences of entomopathogenic fungi in overwintering rove beetles (Staphylinidae) sampled from lucerne (site A) and white cabbage (site B), after laboratory incubation Lucerne No. infected by

White cabbage ~

No. infected by

g

g

Staphylinidae 9

Tachyporus chrysomelinus L. Tachyporus hypnorum Fabrieius Tachyporus obtusus L. Tachyporus sp. Anotylus inseccatus Gravenhorst Anotylus rugosus Fabricius Anotylus sculpturatus Gravenhorst

r,.

2 1

1

2

22

1 1

1

1

1

9 3 19

1

1

1

Other Staphylinidae

1

1

28 1 22

Imagin~,To~l

Num~rs

1

l

1

1

4

57

1

1

2

51

Larvae, Total

Numbe~

2

0

0

0

2

4

0

0

0

0

TOTAL

Numbe~ %

3 4,9

1 1,6

1 1,6

1 1,6

6 9,8

1 2,0

1 2,0

2 3,9

61 100

51 100

81

ENTOMOPATHOGENIC FUNGI IN PREDATORY BEETLES

Table 3 shows numbers and prevalence of fungi in A. rugosus collected at site C. Table 4 list the entomopathogenic fungi found on single specimens of caTabids and staphylinids from other localities during the study. At site A and B, species of Bembidion Latreille, Amara Bonelli and Harpalus Latreille were the predominant carabids in both lucerne and cabbage (table 1). In lucerne, species of the staphylinid genera Tachyporus Gravenhorst and Anotylus Thompson were abundant (table 2). A number of larvae of autumn breeding carabids were found in both fields, while only few larvae of staphylinids could be found in lucerne. 7.6% of the adult carabids and 50% of the carabid larvae were infected by entomopathogenic fungi in the lucerne. Similarly, from cabbage 6.9% of adult carabids and 19.1% of larvae proved to be infected (table 1). For staphylinids, infection levels were somewhat similar (lucerne: 7.0% of adults, 50% of larvae infected, cabbage: 3.9% of adults infected (table 2)). In both fields, Beauveria bassiana was the predominant fungus, killing 70.8% of the infected individuals in lucerne and 42.8% of the infected beetles from the cabbage field. In larvae and imagines from lucerne, other entomopathogenic fungi found included Metarhizium anisopliae, Verticillium lecanii (Zimmerm.) Virgas and Zoophthora radicans (Batko) Brefeld. In one specimen of Bembidion obtusum a mixed infection of B. bassiana and V. lecanii was found. In a few specimens from cabbage, M. anisopliae, Paecilomyces farinosus (Holm ex. S.F. Gray) Smith & Jones and V. lecanii were found beside B. bassiana.

TABLE 3

Prevalence of Beauveria bassiana in adults of Anotylus rugosus (Staphylinidae) sampled from white cabbage (site C). Two cultivation methods were employed." normal cultivation (monoculture) and undersowing with clover (clover) Beetles ~

Soil samples

Cultivation method

Monoculture Clover

Total no.

No. infected

% infected

Total no.

No. with sporulation 2

390 173

269 108

69,0 62,4

29 15

11 6

(~) Live collected beetles incubated in the laboratory. (2) Soil samples with sporulating cadavers at time of flotation.

In staphylinids collected at site C, infection levels of B. bassiana were high in both species sampled, with an average infection level of 67% for A. rugosus (N=563) (table 3). 37% of the sampled G. angustatus (N=30) were infected by Beauveria bassiana. In 17 out of 44 soil samples, insects sporulating with B. bassiana at the time of collection were observed. These insects were mainly staphylinids, but also a few infected beetle larvae and adult coccinellids were found. No significant differences in infection level could be attributed to undersowing with clover (Z2 = 1.17, P = 0.279), neither could the prevalence of fungus in beetles from a particular soil sample be related to the presence of sporulating cadavers in the same sample (Z2= 0.45, P = 0.504).

82

T. STEENBERG, V. LANGER & P. ESBJERG

A single specimen of the 563 Anotylus rugosus examined was infected by Metarhizium anisopliae. Four specimens were found to be infected by Zoophthora philonthi Balazy (Zygomycetes: Entomophthorales). Two of these individuals proved to be infected simultaneously by two species of entomopathogenic fungi sporulating first with Z. philonthi (following 2-3 days of incubation at 20~ and after a further 3-4 days of incubation, the two cadavers sporulated with Beauveria bassiana.

TABLE 4

Records of fungal infection in single specimens of ground beetles (Carabidae) and rove beetles (Staphylinidae) found in agricultural habitats, excluding species listed in tables 1 and 2 Host species

Fungal species

Carabidae, imagines Agonum dorsale Pontoppidan

Beauveria bassiana Paecilomyces farinosus Verticillium lecanii Beauveria bassiana Beauveria bassiana

Amara plebeja Gyllenhal Loricera pilicornis Fabricius Carabidae larvae Agonum, sp. Patrobus sp.

Verticillium lecanii Beauveria bassiana

Staphylinidae, imagines Aleocharinae spp. Anotylus rugosus Fabricius

Beauveria bassiana Beauveria bassiana Metarhizium anisopliae

Zoophthora philonthi Gyrohypnus angustatus Stephens Lathrobium spp. Staphylinus olens Miiller Tachyporus chrysomelinus L. Xantholinus liniaris Olivier

Beauveria bassiana Beauveria bassiana Paecilomyces farinosus Beauveria bassiana Beauveria bassiana

DISCUSSION In the present study both adults and larvae of a number of carabid and staphylinid species were found to be infected by entomopathogenic fungi. The infected species include several ranked highly as aphid predators: carabids such as Bembidion lampros, B. obtusum, Amara familiaris, A. aenea and staphylinids such as Tachyporus hypnorum, T. chrysomelinus and T. obtusus (Sunderland & Vickermann 1980) (cf. tables 1 and 2). Staphylinids of the genus Anotylus, in which an epizootic of Beauveria bassiana was observed, feed on dipteran eggs and larvae (Good & Giller, 1988). As these species are among the most abundant in cmciferous crops (Coaker & Williams, 1963; Andersen, 1982), they may be of significance as predators of the cabbage root fly Delia radicum L., which is a key pest in Northern Europe. The range and dominance of the fungal species found in the study agrees with the occurrence of these fungi in soils of Northern Europe (Steenberg, unpublished; V/inninen et

ENTOMOPATHOGENIC FUNGI IN PREDATORY BEETLES

83

al., 1989). Like the hyphomyceteous species the entomophthoralean species Zoophthora radicans also has a relatively wide host range (Keller, 1991).' However, Z. radicans apparently has not been reported from staphylinids previously (Kenneth & Ben Ze~v, 1989). Infection levels were low, never exceeding 7.6% of the adult overwintering Carabidae and Staphylinidae. Riedel & Steenberg (unpublished data) also found low infection levels, around 0.1%, in a survey of large numbers of a single carabid species (Bembidion lampros) from a number of localities. The prevalence in carabid larvae from site A and B was higher than prevalence in adults. This may be a focus of future interest as it may indicate a higher susceptibility among larvae. Reports of fungal infections in larvae are rare and mostly refer to special conditions. E.g. Inyayeva (1964) found larvae of Amara and Harpalus infected by B. bassiana and M. anisopliae at breeding sites where there were populations of up to 300 larvae per square meter. The high infection levels of B. bassiana in Anotylus rugosus and Gyrohypnus angustatus show that at least some populations of predators cannot be considered refractory to fungal infections. From literature only limited information is available on susceptibility of predatory beetles to entomopathogenic fungi in laboratory experiments (Kabacik-Wasylic & Kmitowa, 1973; Riedel & Steenberg, unpublished data) and in both investigations mortality due to fungal species like B. bassiana and Paecilomyces farinosus was low. Under field conditions however, this picture may change. The epizootic observed in A. rugosus raises the general question as to whether this reflects a high susceptibility in this species to Beauveria bassiana. Local density of A. rugosus in the soil around the cabbage roots was high compared to numbers in faunistic surveys (e.g Andersen, 1982), frequently exceeding 20 individuals per sample. This high local density combined with the high humidity in the crop may have favoured the fungal infection enough to reach an epizootic level within the population of Anotylus rugosus as well as in the G. angustams also sampled from site C. Naturally occuring infections of predators may add to the overall overwintering capacity of the entomopathogenic fungi. Entomopathogenic hyphomycetes overwinter either as propagules in soil, in host cadavers or in living, infected hosts that do not succumb to the infection before spring (Mtiller-Ktgler, 1965). Whether this may result in transmission of fungal infection from predators to other insects is as yet unknown. However, strains of B. bassiana from several species of Carabidae and Staphylinidae have proved to be very virulent to the pea leaf weevil Sitona lineatus L. (Riedel & Steenberg, unpublished data). Field studies are needed to evaluate the importance of entomopathogenic fungi in population development of predatory beetles, including fungal infections of insects during the growth season and the frequency of epizootics. Special attention should be given to fungal infections of larvae and pupae. Also, some consideration should be given to the impact of predator mobility and spring dispersion from overwintering sites into cultivated fields (Riedel, 1992, Wallin, 1985) on spread of entomopathogenic fungi. Additionally the potential side effects of broad spectrum mycoinsecticides, applied in the field, should include not only mortality of polyphagous predators, but also sublethal effects of importance for the performance of these beneficial insects, such as delayed spring emergence as well as reduced fitness. ACKNOWLEDGEMENTS We would like to thank Werner Riedel (Danish Plant Protection Centre, Lyngby) and Henrik Wallin (Swedish Agricultural University, Uppsala) for their help in identification of carabids and staphylinids and Siegfried Keller (Eidg. Forschungsanstalt, Ztirich) for identification of Zoophthora philonthi.

84

T. STEENBERG, V. LANGER & P. ESBJERG

Henrik Stryhn (Royal Veterinary and Agricultural University, Section of Mathematics) was very helpful in giving statistical advice and Judith Pell (Rothamsted Experimental Station) provided linguistic corrections. This study was funded by The Danish Agricultural and Veterinary Research Council, The Royal Veterinary and Agricultural University as well as the Programme for Strategic Environmental Research. RI~SUMI~ Champignons entomopathog~nes prrlevrs sur des colropt~res prrdateurs (Col. : Carabidae et Staphylinidae) provenant de champs cultivrs. La prrsence de champignons entomopathog~nes a 6t6 recherchre cbez des carabes (Col. : Carabidae) et des staphylins (Col. : Staphylinidae) rrcoltrs dans des champs de luzerne, de chou et d'une culture mrlangre chou-tr~fle blanc. Chez les adultes, le taux d'infection dans les deux groupes d'insectes est en grnrral tr/~s faible (Carabidae : max. 7,6 %, Staphylinidae : max. 7 %). Chez les larves de carabes par contre, le taux d'infection par les champignons est 61ev6 (19-50 %). Sur l'un des sites de l'rtude, une 6pizootie ~ Beauveria bassiana a 6t6 observre, l'infection portant sur 67 % des individus rrcoltrs appartenant/~ l'esp~ce Anotytus rugosus et 37 % des Gyrohypnus angustatus. B. bassiana est le champignon prrdominant isol6 /t partir des colropt~res de tousles sites 6tudirs. D'autres esp~ces fongiques ont 6t6 relevres: ce sont les hyphomyc&es Metarhizium anisopliae, Paecilomyces farinosus et Verticillium lecanii ainsi que Zoophthora radicans et Zoophthora philonthL Deux individus d'A. rugosus ont 6t6 retrouvrs infectrs "~ ia fois par Erynia et B. bassiana. Received : 3 January 1995 ; Accepted : 19 June 1995. REFERENCES Andersen, A . - - 1 9 8 2 . Carabidae and Staphylinidae (Col.) in swede and cauliflower fields in south-eastern Norway. - - Fauna norv. Ser. B., 29, 49-61. Andersen, A . - - 1 9 9 1 . Carabidae and Staphylinidae (Col.) frequently found in Norwegian agricultural fields. New data and review. - - Fauna norv. Ser. B, 38, 65-76. Brown, D. W. & Goyer, R. A. - - 1982. Effects of a predator complex on lepidopterous defoliators of Soybean. - - Environ. EntomoL, 11, 385-389. Charles, V. K. - - 1941. Preliminary check list of entomogeneous fungi of North America. United States Bureau of Entomology and Plant Quarantine. - - Insect Pest Survey Bulletin, 25, 707-785. Chiverton, P. A. - - 1986. Predatory density manipulation and its effect on populations of Rhopalosiphum padi (Hom. Aphididae) in spring barley. - - Ann. appl. Biol., 109, 49-60. Coaker, T. H. & Williams, D. A, - - 1963. The importance of some Carabidae and Staphylinidae as predators of the cabbage root fly, Erioischia brassicae (Bouchr). Ent. exp. & appl., 6, 156-164. Domsch, K. H., Gams, W. & Anderson, T. H. - - 1980. Compendium of Soil Fungi. Volume 1 and volume 2. - - Academic Press, London. Good, J . A . & Giller, P. S. - - 1988. A contribution to a check-list of Staphylinidae (Coleoptera) of potential importance in the integrated protection of cereal and grass crops. In: Integrated Crop Protection m cereals (R. Cavalloro & K.D. Sunderland, eds.), - - A.A. Balkema, Rotterdam/Brookfield, 81-98. Goettel, M.S., Poprawski, T.J., Vandenberg, J.D., Li, Z. & Roberts, D. W. - - 1990. Safety to nontarget invertebrates of fungal biocontrol agents. In: Safety of Microbial Insecticides (M. Laird, L.A. Lacey & E. W. Davidson, eds.). - - CRC Press Inc., Florida, 209-231. Grsswald, K. ~ 1938. Uber den insektentrtenden Pilz Beauveria bassiana. Bisher Bekanntes und eigene Versuche. - - Arbeiten aus der Biologischen Reichsanstalt fiir Land- und Forstwirtschaft, Berlin-Dahlem, 22, 400-454.

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Hansen, V. - - 1951. Biller XV. Rovbiller 1. del. Danmarks Fauna Vol. 57. - - G.E.C. Gads Forlag, K~benhavn, 274 pp. Hansen, V. - - 1952. Biller XV. Rovbiller 2. del. Danmarks Fauna Vol. 58. - - G.E.C. Gads Forlag. Kcbenhavn, 251 pp. Hansen, V. ~ 1954. Biller XV, Rovbiller 3. del. Danmarks Fauna Vol. 59. - - G.E.C. Gads Forlag, Kcbenhavn, 499 pp. I-lelenius, J. - - 1990. Effect of epigeal predators on infestation by the aphid Rhopalosiphum padi and on grain yield of oats in monocrops and mixed intercrops. - - Ent. exp. appl., 54, 225-236. Inyayeva, Z . I . - - 1 9 6 4 . The natural enemies of the Carabidae (Coleoptera). - - Ent. Rev., 43, 280-287. Keller, S . - 1991. Arthropod-pathogenic Entomopthorales of Switzerland. II. - - Erynia, Eryniopsis, Neozygites, Zoophthora and Tarichium. - - Sydowia, 43, 39-122. Kenneth, R.A. & Ben Zeev, I . S . - - 1 9 8 9 . Entomophthorales on Coleoptera: a collection of host/pathogen associations. - - OIBC/WPRS Bulletin, XII/4, 27-34. Kabacik-Wasylic, D. & Kmltowa, K . ~ 1973. The effect of single and mixed infections of entomopathogenic fungi on the mortality of the Carabidae (Coleoptera). - - Ecol. Pol., 21,645-655. Larsson, S. G . - 1937-1940. Entwicklungstypen und Entwicklungszeiten der d~inischen Carabiden. - - Entomologiske Meddelelser, 20, 281-560. Larsson, S. G. - - 1957. Larver. In: Danmarks Fauna Vol. 63 (Biller XIX), Aim. del. - - G.E.C. Gads Forlag, KObenhavn, 94-149. Lindrotb, C. H. - - 1985. The Carabidae (Coleoptera) of Fennoscandia and Denmark. Fauna Entomologica Scandinavica 15 (1). - - E. J. Brill/-Scandinavian Science Press Ltd., Leiden & Copenhagen, 225 pp. Lindroth, C. H. - - 1986. The Carabidae (Coleoptera) of Fennoscandia and Denmark. Fauna Entomologica Scandinavica 15 (2). - - E.J. Brill/-Scandinavian Science Press Ltd., Leiden & Copenhagen, 497 pp. Luff, M. L . - 1987. Biology of Polyphagous Ground Beetles in Agriculture. ~ Agric. Zool. Rev., 2, 237-278. McCoy, C.W., Samson, R.A. & Boucias, D. G . - 1988. Entomogeneous fungi. In: Handbook of Natural Pesticides, Vol. V: Microbial Pesticides, Part A, Entomogeneous Protozoa and Fungi (C. M. Ignoffo & N.B. Mandara, eds). ~ CRC Press, Boca Raton, FL, 151-236. Miiller-Kiigler, E . - 1965. Pilzkrankheiten bei Insekten. - - Paul Parey Verlag, Hamburg & Berlin, 444 pp. Riedel, W . - 1992. Hibernation and spring dispersal of polyphagous predators in arable land. Ph. D-thesis, University of Aarhus, 108 pp. Samson, R. A . - 1981. Identification: Entomopathogenic Deuteromycetes. In: Microbial Control of Pests and Plant Diseases 1970- 1980 (H. D. Burges, ed.). - - Academic Press, London, 93-106. SAS I n s t i t u t e - 1985. SAS Users Guide: Statistics, Version 5 Edition. Sunderland, K. D. & Viekermann, G. P. - - 1980. Aphid feeding by some polyphagous predators in relation to aphid density in cereal fields. - - J. appl. Ecol., 17, 389-396. Thiele, H . - U . - - 1977. Carabid Beetles in their Environments. - - Springer-Verlag, Berlin, Heidelberg, New York. Viinninen, I., Husberg, G.-B. & Hokkanen, H . - 1989. Occurrence of entomopathogenic fungi and entomoparasitic nematodes in cultivated soils in Finland. - - A c t a Entomol. Fenn., 53, 65-71. Veen, K . H . - 1968. Recherches sur la maladie due h Metarhizium anisopliae chez le criquet p~lerin. - - Mededelingen Landbouwhogeschool Wageningen Nederland, 68-5, 1-77. Wallin, H . - - 1 9 8 5 . Spatial and temporal distribution of some abundant carabid beetles (Col.: Carabidae) in cereal fields and adjacent habitats. - - Pedobiologia, 28, 19-34.

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