Ent. exp. & appl. 6 (1963): 156--164. North-Holland Publishing Co., Amsterdam

T H E I M P O R T A N C E OF S O M E C A R A B I D A E A N D

S T A P H Y L I N I D A E AS P R E D A T O R S O F T H E C A B B A G E

FLY, ERIOISCHIA BRASSICAE ( B O U C H E )

BY

T. H. COAKER and D. A. WILLIAMS

National Vegetable Research Station, Wellesbourne, Warwick, England

R O O T

Carabid and staphylinid predators of the immature stages of the cabbage root fly were identified using the precipitin test.

Some of the staphylinids trapped were predatory and may have been responsible for a larger proportion of the total loss of the immature stages of the cabbage root fly than were the carabids. Several carabid species captured on brassica plots were found to have relatively high predatory values.

Of the predatory carabids, Bembidion lampros was the most frequently occurring and, together with 5 other species, constituted over 90% of the total carabids trapped on brassica plots.

Observations made by several workers on the predation of the cabbage root fly have recently been summerised by HUGHES & SALTER (1959). WISHART, DOANE & MAYBEE (1956) considered carabids, in particular Bembidion quadrimaculatum

oppositum Say, to be the most abundant species that they encountered in Canada, and staphylinids to be the more important predators of the egg stage. From studies carried out at Wellesbourne on the natural mortality of the immature stages, WRIGHT, HUGHES d~ WORRALL (1960) demonstrated an inverse relationship between the numbers of ground beetles trapped on brassica plots and the subsequent survival of the root fly. Bembidion lampros was chosen during these experiments as the representative species to indicate the abundance of the predaceous carabids, prin- cipally because it was the most common species encountered at that time of the year and because it exhibited a pattern of behaviour which benefited it as a pre- dator of the egg stage (MITCHELL, 1959). In addition, HUGHES (1959) derived a relationship between the numbers of both Bembidion sp. and Trechus spp. and the loss of root fly eggs, and concluded that these beetles were responsible for destroy- ing more than 90% of the eggs laid. These investigations have been continued and altogether some 60 species of carabids and staphylinids have been found on

brassica plots at Wellesbourne. In the work described below a precipitin test (WEST, 1950) was used to identify

the beetle species that were predatory on the immature stages of the cabbage root fly and an assessment was made of the relative predatory values of some of the carabid species. In addition to estimating the populations of ground beetles during the early part of 1961, a quantitative evaluation of the daily consumption of the

PREDATORS OF THE CABBAGE ROOT FLY 157

immature stages by beetles was obtained using a method similar to the described by DEMPSTER, RICHARDS & WALOFF (1959).

The precipitin test

The procedure followed for the preparation of the antigen and antiserum was similar to that described by DEMPSTER (1960). To prepare the antigen, one gram of cabbage root fly pupae was crushed in normal saline solution and allowed to stand for 24 hours at about 4 ~ C. It was then centrifuged and passed through a Sietz EK sterilising filter pad. The filtrate was made up to 10 ml with normal saline solution and, after precipitation of the soluble proteins, the resulting sus- pension containing the antigen was injected intramuscularly into the hind leg of a rabbit. After 5 or 6 similar injections separated by 10 day intervals, an antiserum of suitably high titre was obtained which was stored in 5- -10 ml lots at - - 1 0 ~ C. This gave a positive reaction with a standard pupal extract diluted to 1 : 8000 which in- dicated a sensitivity to one thirtieth of a root fly egg in saline solution. The anti- serum was also highly sensitive to extracts of root fly eggs and larvae.

Representative samples of beetles collected from the field at regular intervals were identified and then crushed on filter paper either whole or, in the larger species, as the gut only after dissection. They were then dried over phosphorus pentoxide and retained at room temperature for testing at a later date.

In most of the beetles tested, experiments showed that one root fly egg could be detected in the gut 24 hours after being eaten and, although in a few individuals this period was longer, it rarely exceeded 36 hours. A positive reaction in the precipitin test indicated, therefore, that the beetle had fed on one or more of the immature stages of the cabbage root fly within at least the previous 24 hours.

Results of the precipitin test

The proportions of the individuals of the various species of beetles collected from brassica plots between April and September, 1960 and 1961, and which reacted positively with the anti-cabbage root fly serum are shown in Table I. Because the antiserum also reacted with the closely allied species Delia cilicrura (Rond.), some errors could have been made. However, as this species was rarely encountered within the locality in which the beetles were trapped, its importance was discounted.

Information on the natural mortality of the immature stages of the cabbage root fly (HUGHES, 1959; COAKER • WILLIAMS, 1961) suggested that the largest proportion of loss occurred in the egg stage; therefore, most meals detected by the precipitin test probably were comprised of eggs. That most of the common carabids found or trapped feed on eggs is verified later in this paper, but it is unlikely that smaller species take late instar larvae or pupae unless previously damaged, although the larger species of the genera Amara, Harpalus and Feronia will readily do so. It is possible, therefore, that some of the positive results obtained may have arisen from scavenging. The high percentage of individuals which reacted positively with the anti-cabbage root fly serum among species of Harpalus and Amara indicated

158 T.H. COAKER AND D. A. WILLIAMS

that, at times, they must have been carnivorous in habit, although DAVIES (1953) considered them to be entirely herbivorous.

TABLE I

Results of testing beetle predator smears against anti-cabbage root fly serum

Number Percentage tested reacting

Carabidae Nebria brevicollis (F.) 178 11.8 Clivina fossor (L.) 91 12.0 Bembidion lampros (Herbst.) 750 20.0 B. quadrimaculatum (L.) 332 18.1 Trechus quadristriatus (Sch.) 104 11.5 T. obtusus Er. 33 4.9 Harpalus aeneus (F.) 365 23.8 H. rufipes (Deg.) 305 14.1 Amara familiar& (Duft.) 181 22.1 Feronia vulgaris (L.) 236 11.4 F. madida (F.) 39 2.7 Agonum viduum (Panz.) 31 3.2 .4. dorsale (Pont.) 68 4.4

Mean 12.3 Staphylinidae

Oxytelus rugosus (F.) 119 13.5 XanthoHnus longiventris Heer 30 20.0 Philonthus succicola Thom. 27 11.4 P. cognatus Steph. 23 4.5 Tachyporus hypnorum (F.) 76 6.6 T. solutus (Er.) 33 3.0 T. obtusus (L.) 38 5.3 Aleochara bilineata Gyll. 556 2.5 ,4. bipustulata (L.) 115 2.6

Mean 7.7

The abundance of the common predatory beetles in brassica plots

Pitfall traps ("one pound" i.e. 350 cc capacity glass jam-jars sunk in the soil), sited 10 cm away from brassica plants were used to collect the beetles. The traps were placed alongside alternate plants along two adjacent rows in the middle of the brassica plots. They were covered with 2.5 cm mesh screens resting above the top of the jars to protect the trapped beetles from predation by birds. All the beetles were removed daily from the traps, identified, counted, then returned to the plots.

The species of staphylinids found in the soil around brassica plants indicated that those trapped in pitfalls were not representative of all the species present in the soil. Examination of the soil within 0.6 X 0.6 m each enclosing one brassica plant, made between April and August 1961, when maximum numbers of cabbage root fly eggs and larvae were found, revealed mean numbers of between two to

PREDATORS OF THE CABBAGE ROOT FLY 159

six adult staphylinids per plant. The most common staphylinid species trapped or found were Aleochara bilineata, A. bipustulata and Oxytelus rugosus. These are shown in Table I together with the other most frequently encountered species which gave positive reactions with the anti-cabbage root fly serum. Fourteen species have been omitted from the table as these were only rarely trapped or found and gave negative reactions in the precipitin test.

Between April and May, the time when the first generation of the cabbage root fly was present, B. lampros was always the most common carabid species trapped. B. quadrimaculatum, H. ru[ipes and F. vulgaris were the most common during the second generation of the root fly in June and July. Altogether thirty carabid species were recorded but only six were numerically important. They were B. lampros, B. quadrirnaculatum, H. aeneus, H. ru[ipes, F. vulgaris and N. brevicollis, and constituted over 90% of the thirteen species which gave positive reactions with

the anti-cabbage root fly serum. The numbers of each beetle species caught in pitfall trops depend on both the

locomotor activity and density of the species. Species trapped less frequently, however, should not be regarded as being unimportant predators because it is pos- sible that they may be intimately confined around the plant root within the restricted habitat of the root fly eggs and larvae. The only carabids in this category were Trechus spp. which, during the years 1960--62 inclusive, were more frequently found from the end of August until October, although MITCHELL (1959) had pre- viously found them to be more numerous earlier in the season. The seasonal abun- dance of the carabids trapped, illustrated in Fig. 1 as 5 day totals from 60 pitfall traps, varied considerably from year to year. Neither the increased cover provided by the developing crop, nor the abundance of root fly stadia appeared to have affected the numbers present. Only the regular predominance of B. lampros and H. aeneus, during the first generation of the root fly, was evident.

Attempts were made during the first generation of the root fly in 1961 to estimate the populations of some of the more abundant carabid species within an area of cauliflowers measuring 45 m X 18 m. The area was surrounded on two sides by bare fallow and on the other two by a hedge and grass path, respectively. Marked carabids were released on several occasions in the centre of the plots but were never recovered in pitfall traps sited in the bare fallow at various distances from the perimeter of the experimental area. This suggested that little or no emigration of beetles occurred from the experimental area, and is supported by the observations of TmELE (1960) which showed that there was little intermixing between carabid populations in hedgerows and adjoining cultivated land. Therefore, assuming that population change by migration, mortality or by development from larva to adult was negligible between the observations, the mark and recapture data obtained in rater experiments were treated for a straight Lincoln index, using BAILEY'S (1952) modification.

Species of carabids were released on several occasions during 1961, and the proportion of those recaptured relative to those released was used to estimate the

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PREDATORS OF THE CABBAGE ROOT FLY 161

numbers of the various species present on the brassica plots. Only on one occasion were marked individuals of all four species recaptured (Table II). These four species made up 82% of the total predaceous carabids trapped, and the total population between 10--15th May, for example, can be estimated as being 1862 - - 2298. Thus, for the whole period covered by the first generation of the 0.82 root fly (16th April--31st May), the estimated population of predaceous carabids present, calculated from the five day trap totals, was 11,729. Of this total, a mean of 12.3% reacted positively with the anti-cabbage root fly serum, suggesting that in each 24 hour period this percentage of the population had fed on one or more stadia of the cabbage root fly. Hence, between 16th April and 31st May it was calculated that some 7,209 meals were taken (Table III).

TABLE II

Mark and recapture results and population estimates Jor the period 10.5--15.5.62.

No. Beetles No. Beetles Recaptured Population Total all Released Unmarked Marked I Estimate species

Marked (M) (N) (R) M ( N + 1) trapped

R + I

B. Mmpros 68 43 3 748 1246 H. aeneus 29 32 1 478 581 H. ru]~es 14 8 1 27 71 A. ]amil~r& 28 41 1 609 268

Total 1862 2166

By comparing the survival of the immature stages of the root fly in the presence and absence of carabid species, 24 per cent of a total of 700 eggs, larvae and pupae, calculated to have been lost around each brassica plant in 1961 can be accounted for in terms of predation by carabids (COAKER & WILLIAMS, 1962). From these data, the average daily meal taken by one carabid, within the experi-

mental area occupied by 750 plants, was estimated to have been 700 750 7209 • -4- =

18.2 eggs, larvae or pupae. A comparison of the estimated populations of the staphylinids from quadrat

sampling, and carabids from mark and recapture data for May 1961, suggested that there were more than twice as many staphylinids as carabids. The mean percentage reacting with the anti-cabbage root fly serum, however, was lower amongst the staphylinids than amongst the carabids, being 7.7% and 12.3%, respectively. If each predatory staphylinid consumed the same mean number of root fly stadia as was estimated for carabids, then about 34% of the total root fly mortality could be attributed to them. However, since over one third of the total root fly mortality remains unaccounted for (CoArER & WILLIAMS, 1962) it is possible that they were responsible for a higher proportion. The larvae in addition to the adults of carabids

162 T. H. COAKER AND D. A. WILLIAMS

and staphylinids, are also normally predators and were probably responsible for some of the unaccounted loss.

TABLE III

Number of Carabids trapped, estimated populations and number of mea~ taken/or each 5 day per~d

Period No. Beet les Estimated Estimated Trapped (~ Total (b) No. meals (c)

April 4 557 2473 1520 5 346 1536 944 6 295 1309 805

May 1 130 577 354 2* 518 2298 1413 3 409 1815 1116 4 147 652 400 5 107 475 292 6 134 594 365

Total 1643 * Period of mark and recapture

2298 b=-5~8 •

11729 7209

c -- (12.3 • 5) b

Comparison of predatory values of some carabid species

Direct comparisons of the predatory importance of several carabid species were made in the following laboratory experiment in 1962.

Ten cabbage root fly eggs were placed on smooth soil, around each of nine small cabbage plants which were growing 38 cm apart in troughs. Ten adult carabids were placed in each trough and a plastic (cellulose-acetate) barrier was erected inside the trough to stop the beetles escaping. A mesh dome was placed over the trough to prevent unwanted root flies from ovipositing around the plants. After an exposure period of three days the eggs remaining were taken from the soil and counted. On each occasion four different carabid species were compared, each species being confined in a separate trough. B. lampros was used as the standard species for comparison, and the ratio of the numbers of eggs the species consumed to those eaten by other species was used to define the predatory value of the individual species. The percentage of eggs eaten and the predatory values are given in Table IV. These indicate that B. lampros and T. obtusus were the most efficient predators. B. quadrimaculatum and H. aeneus were also comparatively good predators. The species with the highest predatory values were frequently noticed to be the most active of the species compared. They were never observed, however, to demonstrate positive searching behaviour, but found the batches of eggs by chance contact only, as was shown by the scattered distribution of the eggs eaten within the nine batches exposed. On several occasions, on the other hand, all the eggs under some plants were eaten whereas those under others were left untouched,

PREDATORS OF THE CABBAGE ROOT FLY 163

suggesting that the initial finding of a food source stimulated a further search within that restricted area, a reaction observed by MITCHELL (1959).

TABLE IV

Percentage of eggs eaten after being exposed to carabids for 3 days. Tile predator value, i.e.,

Mean% Mean predator value

85.6 (1.0)

65.6 (I.0) 62.3 (1.0)

72.4 (1.o)

82.3 (1.o) 72.7 (1.o) 67.4 (i.o) 72.6

47.8 (.77)

56.6 (.78)

53.3 (.65)

52.5

ratio with B. lampros, is in parenthesis.

52.9 41.2 (.62) (.48)

12.3 37.8 (.19) (.58)

20.0 18.9 (.28) (.26)

8.9 (.14)

61.1 20.0 (.74) (.24)

15.9 77.8 (.22) (1.07)

33.5 71.3 (0.50) (1.05)

57.0 16.1 17.9 28.3 37.3 8.9 74.5

1.0 .73 .68 .23 .23 .42 .49 .14 1.06

Comparisons between numbers of eggs eaten after 24, 48 and 72 hours' exposure to predation by B. lampros, B. quadrimaculatum, T. obtusus, and H. aeneus in- dicated that at least 50 per cent of the eggs were eaten during the first 24 hours. WISHART et al. (1956) and HOGtiES (1960) reported somewhat similar findings from field experiments, associating them with the availability of eggs, thereby reducing the chance of random contact by the beetle as the number of eggs decreased.

Assuming, therefore, that 50 per cent of the mean number of eggs (19.5) eaten by the carabids during the first 24 hours of the exposure period in the experiments comparing their relative predatory values, and that the proportion of these carabids which fed was the same as that calculated from the brassica plot data, i.e., 12.3 %,

then an average daily meal of 19.5 I00 • -- 15.9 eggs was taken per beetle in 12.3 4

the troughs. This amount is similar to the average daily meal, calculated from the field data, of 18.2 immature stages.

Although these estimations of the mean daily consumption of immature stages of

164 T . H . COAKER AND D. A. WILLIAMS

the root fly have many limitations, the similarity of the results derived from the field and laboratory experiments suggest that they are probably of the right order. Any reduction, therefore, in the numbers of carabids and/or staphylinids which have been shown to be predators of the root fly on brassica plots, would conse- quently increase proportionately the survival of the root fly above the low percen- tage normally surviving.

ZUSAMMENFA$SUNG

DIE BEDEUTUNG EINIGER CARABIDEN UND STAPHYLIN1DEN ALS PRA'DATOREN

DER KOHLFL1EGE, ERIOISCHIA BRASSICAE (BOUCH[~)

Carabiden und Staphyliniden werden als Priidatoren der Kohlfliege Erioischia brassicae (Bouchf) zu den wichtigsten Mortalit~itsfaktoren dieser Art gerechnet. Aus den zahlreichen, in Kohlparzellen gefundenen oder in Fallen gefangenen K~iferarten wurden diejenigen zu einem Priizipitintest ausgewiihlt, die sich yon den Entwicklungsstadien der Kohlfliege ern~ihren und deshalb als Priidatoren der Kohlfliege angesehen werden kiSnnen. Bei einem Vergleich der Verhiiltnisse innerhalb der positiv zu Kohlfliegen-Antiserum reagierenden Kiiferpopulationen zeigte sich, dab die Staphyliniden wahrscheinlich fiir einen grfl3eren Teil des Gesamtverlustes an Kohlfliegenstadien verantwortlich zu machen sind als die Carabiden. Unter den riiuberischen Carabiden kam Bembidion lampros am hiiufigsten vor und war zusammen mit fiinf anderen Arten fiir fiber 90% des Gesamtverlustes in den Kohlparzellen verantwortlich. Mehrere dieser Kiiferarten haben einen verhiiltnismiil3ig hohen pr/idatorischen Wert.

REFERENCES

BAILEY, N. T. J. (1952). Improvements in the interpretation of recapture data. J. Anim. Ecol. 21 : 120--127.

COAKER, T. H. & WILLIAMS, D. A. (1961). Entomology Report. Rep. Nat, Veg. Res. Sta. Wellesbourne for 1960. & (1962). Entomology Report. Rep. Nat. Veg. Res. Sta. Wellesbourne for 1961.

DAVIES, M. J. (1953). The contents of the crops of some British Carabid Beetles. Ent. Mon. Mag. 89 : 18--23.

DEMPSTER, J. P. (1960). A quantitative study of the predators on the eggs and larvae of the broom beetle, Phytodecta olivacea Forster, using the precipitin test. J. Anita. Ecol. 29: 149--167.

DEMPSTER, J. P., RICnARos, O. W. & WALOFF, N. (1959). Carabidae as predators on the pupal stage of the Chrysomelid beetle Phytodecta olivacea Forster. Oikos 10: 65--70.

HOGnES, R. D. (1959). The natural mortality of Erioischia brassicae (Bouchf) during the egg stage of the first generation. I. Anita. Ecol. 28: 343--357.

HUGHES, R. D. & SALTER, D. D. (1959). Natural mortality of Erioischia brassicae (Bouchf) during the immature stages of the first generation. J. Anita. Ecol. 28: 231--241.

MITCttELL, B. (1959). Studies on the ecology of two species of Carabidae which are probable predators of the cabbage root fly eggs. Ph.D. Thesis, Univ. of Birmingham.

THIELE, A. V. (1960). Gibt es Beziehungen zwischen der Tierwelt yon Hecken und angrenzenden Kulturfelden ? Z. angew. Ent. 47 : 122--127.

WEST, A. S. (1950). The precipitin test as an entomological tool. Canadian EAt. 82 : 241--244. WISHART, G., DOANE, J. F. & MAYBEE, G. E. (1956). Notes on beetles as predators of eggs of

Hylemya brassicae (Bouchf). Canadian Ent. 88: 634--639.

Received ]or publication: March 24, 1963.