Laboratory Evaluation of Carabid Beetles (Coleoptera: Carabidae) as Predators of Diamondback Moth (Lepidoptera: Plutellidae) Larvae
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BIOLOGICAL CONTROL
Laboratory Evaluation of Carabid Beetles (Coleoptera: Carabidae) as
Predators of Diamondback Moth (Lepidoptera: Plutellidae) Larvae
H. SUENAGA1 AND T. HAMAMURA
National Research Institute of Vegetables, Ornamental Plants and Tea, Kusawa, Ano, Mie 514-2328, Japan
Environ. Entomol. 27(3): 767Ð772 (1998)
ABSTRACT Consumption of diamondback moth, Plutella xylostella (L.), larvae by 24 species of
adult carabids and 2 species of carabid larvae was investigated using small containers in a laboratory.
Thirteen species of adult carabids were evaluated for their suppressive effect on diamondback moth
larvae using small enclosed arenas simulating Þeld conditions. Consumption by adult carabids varied
from zero 4th instars per individual per day of each sex of Amara simplicidens Morawitz to 23/d for
a female Chlaenius posticalis Motschulsky. Larvae of Chlaenius micans (F.) and C. posticalis consumed
'191 and 92 early 4th instars of diamondback moths per individual, respectively, through the entire
larval period. These larvae were often observed in cabbage heads. In the enclosure experiment, C.
micans, C. posticalis, and Dolichus halensis (Schaller) caused .95% mortality for diamondback moth
larvae during 4-d trials. Pterostichus planicollis (Motschulsky) caused 71Ð77% mortality; the other 9
species in 6 genera, however, contributed ,20% to mortality. The high prey suppression by C. micans,
C. posticalis, and D. halensis can be attributed to the beetles habit of climbing plants as well as high
consumption rate. These results indicate that C. micans and C. posticalis (particularly the larvae of
these species) can be important predators of diamondback moth larvae; they have high consumption
rates and the habit of climbing plants in both immature and adult stages.
KEY WORDS Chlaenius micans, Plutella xylostella, predators, cabbage, ground beetles, Japan
THE DIAMONDBACK MOTH, Plutella xylostella (L.), has Carabids have been recorded as predators of
caused extensive losses to cruciferous crops world- dipteran pests such as Erioischia brassicae (Bouché)
wide because it has developed resistance to all classes (Wright et al. 1960, Coaker 1965) and cabbage maggot,
of insecticides including the microbial agent Bacillus Hylemya brassicae (Bouché) (Chapman and Ecken-
thuringiensis Berliner (Talekar and Shelton 1993). rode 1973, Wyman et al. 1976) in Þelds of cruciferous
This has encouraged research in cultural and biolog- crops. However, only a few workers have pointed out
ical control measures. To date, microbials (B. thurin- the possible inßuences of carabids on lepidopteran
giensis) and introduced parasitoids such as Diadegma larvae in Þelds of cruciferous crops (Dempster 1968,
semiclausum Hellen and Cotesia plutellae Kurdj have Yamada 1985, Sivapragasam et al. 1988). Parker (1970)
been used as the main biological control agents and Sivapragasam et al. (1988) showed that predators
throughout the world (Talekar and Shelton 1993 ). were responsible for the large unknown mortality of
However, predators such as carabid beetles and spi- Pieris rapae (L.) or P. xylostella. Hence, more studies
ders have rarely been used as biological control agents are desired to assess the role of predators in crucifer-
in Þelds of cruciferous crops (Lim 1992). ous crop Þelds.
Carabid beetles in agroecosystems have been in- Our study was done to identify the carabid species
vestigated intensively in northern Europe and North that are potential predators of diamondback moth
America as natural enemies of pest insects; their po- larvae in Japan. We used small containers and Þeld-
tential as biological control agents has been docu- simulating enclosed arenas for the feeding trials in a
mented in both Þeld and laboratory experiments (Luff laboratory. Two species of carabid larvae also were
1987, Lövei and Sunderland 1996). Particularly the tested to determine the consumption rate.
genera Pterostichus, Harpalus, and Bembidion are gen-
erally abundant in those regions and are efÞcient pred-
ators of cereal aphids (Edwards et al. 1979, Chiverton Materials and Methods
1986), lepidopteran larvae (Frank 1971, Fuller 1988, Carabid Beetles and Diamondback Moth Larvae.
Riddick and Mills 1994), and weevils (Barney and Carabid beetles were collected at the National Re-
Armbrust 1980, Baines et al. 1990). search Institute of Vegetables, Ornamental Plants and
Tea, Ano, Mie Prefecture, central Japan, from Novem-
1 Current address: Osumi Branch, Kagoshima Prefectural Agricul- ber 1994 to August 1996. White plastic pitfall traps
tural Experiment Station, 4938 Hosoyamada, Kushira, Kimotsuki-gun, (11.5 cm diameter opening, 7.5 cm diameter bottom,
Kagoshima 893Ð1601, Japan. 11.5 cm deep) were used to collect beetles. Five to 10
0046-225X/98/0767Ð0772$02.00/0 q 1998 Entomological Society of America768 ENVIRONMENTAL ENTOMOLOGY Vol. 27, no. 3 traps were set up in each of cabbage Þelds, adjacent simulating enclosed arenas. Plastic containers (33 by fallow, and the Þeld boundary and emptied daily. 48 cm, 10 cm deep) Þlled with granular compost to a Captured beetles were taken to the laboratory and depth of '5 cm were used as enclosed arenas. Each held individually in transparent styrol containers (9.5 had 8 cabbage (ÔYR NodokaÕ) seedlings (4- to 5-leaf cm diameter, 5.5 cm high) with moistened Þlter paper stage) in 2 rows, 14 cm between rows, and 10 cm on the bottom. They were starved for 1 d at 25 6 18C within a row. Second-instar diamondback moths (5Ð6 and a photoperiod of 14:10 (L:D) h before use in either per plant, '45 larvae per arena) were placed on the of the following 2 feeding trials (experiments 1 and 2). cabbage leaves with a soft brush. The containers were Each replication in a experiment was conducted at then maintained in a room of 15 6 18C for 1 d to allow different times when the carabids were caught in the larvae to settle on cabbage leaves. The number of traps, but mainly around the time of maximal capture. larvae was adjusted to 40 by removing extra larvae Campalita chinense (Kirby), which are voracious, before the feeding trials. The cabbage plants were also were captured in the traps but not evaluated for enclosed with transparent celluloid walls (30 by 44 by predation ability. This is because C. chinense was re- 22 cm). A moistened cotton ball was placed on the soil corded as an active soil surface forager in both imma- surface as a water supply for the beetles. Adult cara- ture and adult stages (Kuwayama and Oshima 1964), bids (8 individuals) of each sex and species were then hence it was regarded as a less valuable predator of introduced into the enclosures. Finally, the top of the diamondback moth. Rare species were not examined. wall was covered with white nylon gauze to prevent The sexes of most species were determined by exam- beetles from escaping. Carabids were allowed to feed ining the shape of the protarsi; the protarsi of males are on the diamondback moth larvae for 4 d under the dilated and pronounced (Riddick and Mills 1994) in same conditions as in experiment 1. Enclosures in most species. which no carabids were released were used as con- First or 2nd instars of Chlaenius micans (F.) and trols. Chlaenius posticalis Motschulsky were collected from The cabbage plants were cut off at ground level 4 d cabbage heads in the Þeld in early July 1996, starved later, and the larvae present on them were counted. for 1 d by the same method as for the adult carabids. Percentage larval mortality associated with carabid They were evaluated for the consumption rate of di- release was calculated as (mean number of live larvae amondback moth larvae in experiment 3. Larvae were in enclosures without carabids minus number of live determined to species according to the description by larvae in each enclosure with carabids)3100/mean Habu and Sadanaga (1965). number of live larvae in enclosures without carabids. Diamondback moth larvae used in the experiments We repeated this experiment 2Ð7 times for each spe- were from a laboratory culture reared using fresh cies, depending on the availability of the different cabbage leaves through the entire larval period. The species and sexes. Adults of each sex were placed larvae were removed with a soft brush as needed. together to meet 8 beetles when an insufÞcient num- Experiment 1: Consumption by Adult Carabids on ber of beetles was captured for each sex. Prey Larvae on Detached Cabbage Leaves. Adult cara- Experiment 3: Consumption by Larvae of C. micans bids of 24 species in 9 genera were evaluated for the and C. posticalis on Prey Larvae on Detached Cabbage consumption rate of 4th-instar diamondback moth. Leaves. Larvae of C. micans and C. posticalis starved for Adult carabids starved for 1 d were individually trans- 1 d were individually placed in the transparent styrol ferred to new styrol containers, supplied with a cab- containers (11 by 19 by 6.5 cm) with moistened Þlter bage leaßet (4 by 4 cm). Early 4th instars of diamond- paper (12 cm diameter) on the bottom. A larger cab- back moths were placed on the leaßet using a soft bage leaßet (3 by 10 cm) was then placed on the Þlter brush. The number of the larvae supplied was 3Ð5 paper and early 4th-instar diamondback moths were more than the maximal consumption in preliminary placed on the leaßet. The number of larvae placed was trials. Larger transparent styrol containers (11 by 19 by 3Ð5 more than were consumed the previous day, with 6.5 cm) and larger cabbage leaßets (3 by 10 cm) were '20 larvae per day around peak consumption. About used for Pterostichus planicollis (Motschulsky), Doli- the same time the next day, the larvae consumed were chus halensis (Schaller), and Chlaenius species be- investigated, after which remaining live larvae were cause of their high consumption rate. Corks (0.5 cm removed. New early 4th instars were then added to the high, 1 cm diameter) were placed under a corner of leaßets. These operations were conducted every day the small leaßet or 4 corners of the large leaßet. This until the carabid larvae Þnally stopped feeding (i.e., enabled the carabids to feed on the larvae present on when the larvae entered the prepupation stage) under the underside of the leaßets. The carabids were al- the same conditions as in experiment 1. lowed to feed on the larvae for 24 h at 25 6 18C and Occasionally, an insufÞcient number of prey larvae a photoperiod of 14:10 (L:D) h, and the numbers of were supplied to carabid larvae because the diamond- larvae consumed were investigated. The feeding trials back moth larvae temporarily became scarce during were conducted for 3Ð12 beetles for each species and the trials. The containers, Þlter papers, and cabbage sex. leaßets were replaced from time to time. Experiment 2: Suppression by Adult Carabids on Data Analysis. The following analyses were con- Prey Larvae on Intact Cabbage Plants. Thirteen spe- ducted using SAS (SAS Institute 1988). Consumption cies in 8 genera were further evaluated to determine rates obtained in experiment 1 were subjected to the the mortality of diamondback moth larvae in Þeld- KruskalÐWallis test (PROC NPAR1WAY, chi-square
June 1998 SUENAGA AND HAMAMURA: CARABID PREDATION ON DIAMONDBACK MOTH 769
Fig. 1. Mean consumption 6 SE of early 4th instars of diamondback moth by adult carabids during 24-h feeding trials
in small containers (9 cm diameter, 5 cm high). Values are 0 for both sexes of A. simplicidens. Females of A. congrua and A.
chalcites were not investigated.
approximation) because the Bartlett test showed that female, respectively) and Harpalus sinicus Hope and
variances were not homogeneous even when the data C. posticalis had the highest one (12.0 and 23.3 larvae
were square-root-transformed. We did not separate per female, respectively). Females of Bembidion
means because many species and unbalanced repli- morawitzi Csiki, which were '5 mm in length, had a
cations among species made a multiple comparison relatively high consumption rate (5.4 larvae) for their
complicated. Percentage mortalities (p) of diamond- size.
back moth larvae obtained in experiment 2 were trans- Experiment 2: Suppression by Adult Carabids on
formed to arcsine =(p/100) before they were sub- Prey Larvae on Intact Cabbage Plants. Percentage
jected to the general linear model procedure (PROC mortality of diamondback moth larvae differed among
GLM). Means were then separated by the TukeyÐ carabid species (F 5 36.7; df 5 12, 37; P , 0.001) (Fig.
Kramer multiple range test (MEANS statement with 2). The data in Fig. 2 show the averages of both sexes.
TUKEY option). Mean consumption rates by the cara- Males and females of C. micans caused 95 and 99%
bid larvae were separated using the Wilcoxon 2-sam- mortality on diamondback moth larvae during 4-d
ple test (PROC NPAR1WAY). trials, respectively. Male and mixed sexes of C. posti-
calis and both sexes of D. halensis also caused nearly
100% mortality of the prey larvae. Both sexes of P.
Results
planicollis caused lower mortality (71Ð77%) than the
Experiment 1: Consumption by Adult Carabids on aforementioned 3 species in spite of their high con-
Prey Larvae on Detached Cabbage Leaves. Adult cara- sumption rate in experiment 1. The other species
bids differed signiÞcantly in their consumption rate of caused less larval mortality; the mortality was ,20%
4th-instar diamondback moths (males, x2 5 145.9, df 5 with no signiÞcant difference in the mortality between
22, P , 0.001; females, x2 5 115.5, df 5 19, P , 0.001) these species. Most of the diamondback moth larvae
(Fig. 1). Female adults of C. micans, C. posticalis, P. reached 4th instars during 4 d.
planicollis, and D. halensis consumed 21Ð23 4th instars. Chlaenius micans, C. posticalis, and D. halensis were
In contrast, members of the genera Anisodactylus and sometimes observed crawling on the cabbage leaves in
Amara consumed #4 larvae; neither sex of Amara daylight or night hours, but were not observed feeding
simplicidens Morawitz consumed any larvae. Harpalus on the diamondback moth larvae. Amara sp. also was
and Chlaenius species varied in consumption rate. Har- observed crawling on the leaves in daylight hours;
palus tinctulus Bates and Chlaenius abstersus Bates had predation on larvae was not observed but feeding on
the lowest consumption rate (0.5 and 2 larvae per leaves and petioles was observed. In contrast, P. pla-770 ENVIRONMENTAL ENTOMOLOGY Vol. 27, no. 3
Fig. 2. Mean percentage mortality 6 SE of diamondback moth larvae caused by adult carabids introduced into enclosures
planted with cabbage seedlings. Bars followed by the same letter are not signiÞcantly different (P , 0.05; Tukey-Kramer
multiple range test [SAS Institute 1988]). Data of H. griseus and Amara sp. are averages of females only and that of P. chalcomus
are from males only. Both males and females or mixed sex were investigated for other species. A. chalcites and A. congrua were
possibly the main component species of Amara sp. They were not distinguished because they strongly resembled each other.
nicollis and Harpalus species often were hidden in the Discussion
soil during daylight hours.
Experiment 3: Consumption by Larvae of C. micans Adults of C. micans, C. posticalis, D. halensis, and P.
and C. posticalis on Prey Larvae on Detached Cabbage
planicollis showed a high consumption rate and a high
Leaves. Larvae of C. micans and C. posticalis consumed
suppressive effect in the laboratory. The high sup-
191 and 92 early 4th-instar diamondback moths during
the entire larval period (Table 1). C. micans consumed pressive effect of these species in the enclosure ex-
about twice as many larvae as C. posticalis for all stadia. periment indicates that they are active in climbing
The consumption by 3rd instars accounted for '80% plants as well as voracious. Actually, the former 3
of the total for both species. The larvae ceased feeding species were observed crawling on the cabbage leaves
'1 d before each molt. The entire larval period of C. during daylight hours in the experiment. Other Japa-
micans was a little longer than that of C. posticalis (18.3 nese researchers also observed that adults of C. micans
versus 16.3 d). Only 2 individuals of C. posticalis pu- (Inouye 1956), C. posticalis (Kuwayama and Oshima
pated; the other larvae of the 2 species died as larvae 1964), and D. halensis (Inouye 1952) climbed plants in
several days after the 3rd instars stopped feeding. the Þelds. Species of genus Chlaenius in Japan gener-
Table 1. Consumption of early 4th instars of diamondback moth by 2 species of carabid larvae and duration of period of carabid larvae
(mean 6 SE)
Carabid No. larvae consumeda Larval period, d
instar nb C. micans nb C. posticalis Pc C. micans C. posticalis Pc
1st 4 7.0 6 0.9 1 4.0 Ñ 3.5 60 3.5 Ñ
2nd 4 20.8 6 2.6 7 11.7 6 1.6 0.014 2.8 6 0.3 3.0 6 0 0.311
3rd 7 163.7 6 17.0 5 75.2 6 8.9 0.006 12.2 6 0.6 9.8 6 0.6 0.013
Totald 4 190.8 6 8.3 5 87.6 6 8.3 Ñ 18.3 6 0.6 12.8 6 0.6 Ñ
Ñ, Statistical analysis was not conducted because of the lack of replication.
a
Total number of larvae consumed during each stadium.
b
Number of carabid larvae examined for both consumption rate and larval period.
c
SigniÞcance for given differences between the 2 carabid species by Wilcoxon 2-sample test ([PROC NPAR1WAY], SAS Institute 1988).
d
Total consumptions and total periods of time of 1stÐ3rd instars of C. micans and of 2ndÐ3rd instars of C. posticalis.June 1998 SUENAGA AND HAMAMURA: CARABID PREDATION ON DIAMONDBACK MOTH 771
ally have a habit of climbing plants as well as having mation, and many overlapping leaves were expanded
a high consumption rate (Tanaka 1956). nearly horizontally when these species appeared; this
Diamondback moth larvae spend their entire life may have kept these carabids from climbing cabbage
span on cabbage foliage, indicating that carabid bee- plants.
tles must require the habit of climbing plants. There- On the contrary, a few larvae of C. micans and C.
fore, among the captured carabids, C. micans, C. pos- posticalis were captured in the traps; instead a variety
ticalis, and D. halensis are the good candidates for the of instars were often observed on cabbage heads to-
predators of diamondback moth larvae. Although P. gether with their sloughs, although the density was
planicollis may be a good candidate, it has been re- very low (unpublished data). This suggests that they
ported as a pest of spring seeding radish (Mizukoshi spend almost the entire larval period on cabbage
1993) and young trees (Habu and Sadanaga 1961) in plants. Yamada (1985) observed C. micans larvae on
Japan. In North America, Calleida decora (F.) is a cabbage plants from late June to mid-September and
foliage-dwelling carabid and is an important predator found in a laboratory experiment that the middle-
of the velvetbean caterpillar, Anticarsia gemmatalis stage larvae consumed '7 fourth-instar diamondback
Hübner, living on soybean leaves (Fuller 1988). moths per individual per day at 258C. We observed C.
In northern Europe and North America, the genera micans larvae feeding on mature larvae of P. rapae in
Chlaenius and Dolichus have received little attention cabbage heads. The larvae of C. micans were observed
because these 2 genera are less abundant or even rare feeding on lepidopteran larvae also in a sweet potato
in those regions (Desender et al. 1994, Cárcamo et al. Þeld (Togshi and Fujimura 1990). The frequent failure
1995). In particular, the genus Dolichus has never been in pupation of these carabid larvae may suggest that a
recorded in agricultural Þelds in those regions as far as mixed diet is necessary for their normal growth.
we know. In addition, Chlaenius sp. showed less ef- The feeding preference or foraging behavior of D.
fectiveness in killing larvae of codling moth, Cydia halensis larvae has not been known in detail. During
pomonella (L.), in a laboratory test (Riddick and Mills our census, many D. halensis larvae were captured in
1994); Chlaenius erythropus showed low percentages pitfall traps, but they were never found on cabbage
in positive reactions to antiserum prepared from lar- plants (unpublished data). This indicates that the lar-
vae of corn earworm, Heliothis zea (Boddie) vae of D. halensis cannot be effective predators of
(Lesiewicz et al. 1982). Also, in our experiments, C. diamondback moth larvae.
abstersus and Chlaenius pallipes Gebler exhibited a In conclusion, the larvae of C. micans and C. posti-
lower consumption rate than several Harpalus species. calis would be the most effective carabid species as
The low suppressive effect of the 9 species of Pteros- predators of diamondback moth larvae. They have a
tichus, Harpalus, Bembidion, Asaphidion, Platynus, and high consumption rate and a habit of climbing plants.
Amara shown in Fig. 2 may suggest that these species Adults of these species may be rather effective in
are inactive plant climbers as well as light eaters. suppressing soil-hiding noctuid larvae such as cabbage
Several species in these genera have been shown to armyworm, Mamestra brassicae (L.), and the common
prey on insects dwelling in the soil or near the soil cutworm Spodoptera litura (F.). Best and Beegle
surface, such as cabbage root ßy (Wright et al. 1960, (1977) and Clark et al. (1994) have pointed out that
Coaker 1965), onion maggot, Delia antiqua (Meigen) predaceous ability in a laboratory does not exactly
(GraÞus and Warner 1989), and alfalfa weevil, Hypera reßect suppressive effect on pests in the Þelds. Thus,
postica Gyllenhal (Barney and Armbrust 1980). They quantitative experiments in the Þelds will be required
also can feed on foliar-inhabiting insects such as lep- to demonstrate the efÞcacy of these 2 carabid species.
idopteran larvae (Lesiewicz et al. 1982, Riddick and
Mills 1994) and aphids (Edwards et al. 1979, Chiverton
1986). However, their predation seems to be restricted Acknowledgment
to the time when the insects wander on the soil surface We thank S.-I. Ueno (Department of Zoology, National
to seek pupation sites or drop off the crops. Science Museum, Tokyo) for his identiÞcation of adult Cara-
In contrast, many species of these genera are known bidae and for review of the manuscript.
to feed on seeds, thus occasionally can be crop pests
in Japan (Habu and Sadanaga 1961, 1965) and in other
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