Em. exp. & appl. 25 (I 979) I28- 135. Ned. Enromol. Ver. Amsterdam

CANNIBALISM IN XYLOCORIS FLA VIPES (HEMIPTERA: ANTHOCORIDAE), A PREDATOR OF STORED-PRODUCT

INSECTS

BY

RICHARD T. ARBOGAST Stored-Product Insects Research and Development Laboratory, Agricultural Research, Science and

Education Administration, U. S. Department of Agriculture, Savannah, Georgia 31403, U.S.A.

A laboratory study of the cannibalistic behavior of Xylocorisflavipes (Reuter) showed that nymphs and adults prey on all nymphal instars but not on eggs. It seems unlikely that either nymphs or adults could successfully attack healthy adults, and no such attacks were observed. However, nymphs were shown to feed on dead adults, and both stages probably feed on dead or dying individuals. The influence of various factors on the rate of cannibalism was investigated.

The predatory bug Xyfocorisflavipes (Reuter) occurs in storages where it preys upon the eggs, larvae, and pupae of stored-product beetles and moths, and it has shown promise as a biocontrol agent for these pests. Its effectiveness as a predator is probably enhanced by a cannibalistic nature that enables it to survive when prey is scarce, but this behavior is a hindrance to mass rearing. Here the cannibalistic behavior of X.fluvipes and some of the factors that influence it are examined.

GENERAL METHODS

Stock cultures of Xflavipes were maintained at 30’ t 1’ and 65% it 5% R. H. with a 12: 12-hr light-dark cycle, both on cultures of the red flour beetle, Tribolium custaneum (Herbst), in rolled oats and on late-stage larvae of the Indian meal moth, Plodiu interpuncteliu (Hfibner), that had been coddled by submersion for 10 min in a water bath at 46”.

When eggs of X.flavipe.7 were needed for tests, adults were kept in small cages with eggs of P. interpunctellu where they scattered their eggs loosely among the moth eggs. Adults of the predator were obtained by collecting an excess of 5th instars from stock cultures, confining them individually for one week, and then using those that had become adults. Mated females were obtained by confining pairs of adult males and females for 2 days. Unless mating was subsequently confirmed by oviposition the females were discarded.

All tests were done at 30” f 1” and 65% + 10% R.H.. Prey, when provided, was late-stage larvae of P. interpuncfellu that had been paralyzed by the sting of Brucon hebetor Say. Three types of cages were used: small cylindrical cages (3.2 cm inside

CANNIBALISM IN XYLOCORIS 129

diameter), large cylindrical cages (5.0 cm inside diameter), and tapered plastic cups with cardboard lids. The cylindrical cages were 2.6 cm high and were covered at both ends by fine-mesh nylon screen. The plastic cups were provided with a filter paper floor 3.0 cm in diameter.

TEST PROCEDURES AND RESULTS

Predation by nymphs and adults on eggs Xylocorisflavipes was not seen to prey on its own eggs. Although nymphs and

adults often probe the eggs with their mouthparts, they are apparently unable to penetrate the shell. Newly formed nymphs become vulnerable to cannibalism when they begin to force the operculum off the egg, and they are sometimes killed even before the operculum is completely free from the body of the shell. More often, however, they are killed as they emerge from the shell and undergo the intermediate molt, or shortly afterwards; their shriveled remains were often found still attached to the eggshell by the embryonic cuticle.

The inability of X.flavipes to prey on its own eggs was confirmed by a test in which groups of ten eggs, all less than 24 hr old, were placed in each of ten small cylindrical cages where they were exposed to attack by two adult virgin females until the last egg of the group hatched. No other prey was provided. Eggs were considered hatched when the operculum was broken away from the surrounding shell along any portion of its circumference. When hatching was completed (after 4-6 days), 97 of the 100 eggs had hatched compared with 96 of 100 control eggs that were not exposed to attack by adults. There was, however, a marked difference between the two sets in the survival of emerging and newly emerged nymphs. None of those exposed to attack by adults survived to the end of the exposure period, whereas 64 of those not exposed to adults did so. Most of the latter mortality can be attributed to attacks by other nymphs.

Predation by nymphs other nymphs

Xylocorisflavipes nymphs were reared from the 1st through the 5th stadium at various densities in large or small cylindrical cages and provided with various numbers of P. interpunctelfa larvae as prey. The initial densities used and the number of cages stocked with each density were as follows:

Nymphs/cage: 5 IO 15 20 or 25 30, 35,40, 50,60 Cages/replicate: 8 4 3 2 I

Two series of tests were conducted with large cages, one series in which there were four moth larvae as prey and another in which there was only one larva as prey. Another series was conducted in small cages with four larvae as prey. In all tests the prey larvae were replaced twice a week. Each test was replicated three times.

130 R. T. ARBOGAST

The cages were examined twice a week and the total number of adults was recorded until all nymphs, had either died or reached the adult stage. Mortality of the nymphs expressed as a k-value=log N,-log N,, where N, is the initial number of nymphs and N, is the number of adults produced (Varley et al., 1973) is plotted in Fig. 1 and suggests a strong correlation between mortality and initial density. The significance of this correlation cannot be proved by a simple statistical test because the estimates correlated are not independent (N, was used to calculate k-value), but the regression of log N, on log N, does provide a valid test of density dependence: if the slope of the regression line is significantly less than 1, density dependence is proven (Varley & Gradwell, 1968). Calculation of this regression for each of the three tests showed that mortality was in fact density-dependent in all of them. The difference between the observed slope and a slope of 1 was highly significant for the regression lines corresponding to A and B in Fig. 1 (t-test, P<O.Ol) but was less certain for that corresponding to C (P=O.O57).

iAJ 0.7-

0.6-

0.5-

Q) 0.4- >

; >

A 0.3-

ltll

n.

0.2-

j +y , , . , . , , ,

0 10 20 30 40 50 60

Nil

Fig. I. Relationship between mortality of nymphs of X.flavipes expressed as k-value and initial number

of nymphs per cage (N,). A - large cage, one moth larva twice weekly. B - small cage, four moth larvae

twice weekly. C - large cage, four moth larvae twice weekly.

CANNIBALISM IN XYLOCORIS 131

The mortality observed can be attributed largely to cannibalistic predation. This can be inferred from numerous observations made during the course of this and other tests. Dead nymphs were almost always excessively shriveled, a sign that they had been fed upon, and nymphs were frequently observed feeding on others of their kind.

Crowding per se had little effect on the rate of cannibalism. Although mortality increased more rapidly with increasing numbers of nymphs in small cages than in large ones when eight larvae per week were provided as food, the difference in slope between the two regression lines (Fig. 1, B and C) was not significant (P=O.O91). Increased cann’ibalism resulted instead from the intensified competition for food that accompanied crowding. Thus mortality increased much more rapidly with increasing density when the food supply was fixed.at two moth larvae per week than when it’was fixed at eight per week (t-test, P<O.Ol) (Fig. 1, A and C). The results of these tests showed that some nymphs are able to complete development despite severe competition for a limited food supply by preying more heavily on other nymphs.

An additional test was done which showed that a few nymphs can complete development even if the only food available is other nymphs. In this test, 20 eggs (newly laid to 72 hr old) were placed in each of five small cages; thereafter 20 more eggs were added to each cage twice a week to provide a continuous supply of 1st instars. One adult emerged in each of three cages after 18-21 days and one emerged in another cage after 50-52 days. The adults were removed as soon as they were discovered, and no more eggs were added; without a supply of 1st instars the nymphs remaining in the cages failed to reach adulthood. No adults were produced in the 5th cage even after 70 days, at which time the test was terminated.

Predation by adults on nymphs Nymphs were reared individually either in the presence or absence of an adult.

For each replicate, one egg of X. j’avipes and one moth larva were placed in each of 20 cups, and an adult was added to ten of the cups. The test was replicated five times with each of three types of adults: males, virgin females, and mated females. Observations were made daily and hatching, molting, and deaths of nymphs were recorded. The moth larvae were replaced as soon as they began to deteriorate. Eggs laid by mated females were removed after each observation. A few cups in which the adult died before the nymphs either died or reached the final molt were discarded and were not used in determining nymphal survival.

The results (Fig. 2) showed that males, virgin females, and mated females prey on nymphs, i.e., mortality of nymphs reared individually was significantly higher when adults were present than when they were not (t-test, PcO.01). The survivorship curves in Fig. 2 also indicate that females were more voracious than males and that mated females were more voracious than virgin females. Nymphal mortality was highest between hatching and the 1st molt, so relatively few nymphs remained for estimation of mortality during the later stages of development.

132 R. T. ARBOGAST

l.OO-

w E .- > .- > f ul

0.50- oc .- c 0’ 0” 0’

-e-e P” Adults

0.00 ! I I I I I H Ml M, Ma M4 MS

Event

Fig. 2. Survivorship curves for nymphs of X.jlavipes from hatch to final molt in presence or absence of adults. Each point represents mean for fifteen (no adults) or five (males, virgin females, mated females)

replicates. Vertical lines indicate one standard error on either side of mean. H represents hatch and

M,-M, represent molts l-5.

Furthermore, those nymphs that ‘reached the 1st molt may have been confined with adults less cannibalistic than most, so the survivorship curves in Fig. 2 may underestimate the usual rate of predation by adults on instars 2-5.

A 2nd test was therefore conducted in which no adults were introduced until after the nymphs had reached the 1st molt. The results of this test (Fig. 3) showed that adults did, in fact, kill more of instars 2-5 than was indicated by the results of the 1st test (Fig. 2). Again, mated females were the most voracious, though there was no difference between males and virgin females. Comparison of Figs 2 and 3 suggests that males and virgin females prey most heavily on 1st instars and that later instars are attacked at a rate that varies little with stage. This cannot be said for mated females, however. Although it is clear that mated females preyed more heavily on 1st than on 2nd instars, it is also clear that they preyed more heavily on 2nd instars when 2nd instars were the earliest stage encountered. This finding leads one to suspect that if 3rd instars had been the earliest stage exposed to mated females, the mortality between molts 2 and 3 would have been greater than indicated in Figs 2 and 3, and so on for each stage. Additional tests would thus be required to obtain a true picture of the mortality inflicted by mated females on 3rd, 4th, and 5th instars.

CANNlBALISM IN XYLOCORIS 133

NO

Adults

0.00 ! 1 I I 1 MI M2 M3 M4 MS

Event

Fig. 3. Survivorship curves for nymphs of A’. jlovipes reared from first to final molt in the presence or absence of adults. Each point represents mean for fifteen (no adults) or five (males, virgin females,

mated females) replicates. Vertical lines indicate one standard error on either side of mean. M,-M,

represent molts l-5.

The mortality inflicted on nymphs by starved and fed adults was compared to determine the effect of hunger on the rate of cannibalism. One adult was placed in each of 20 plastic cups, and a moth larva was added to ten of them. Two days later, one 1st instar was placed in each of these 20 cups and also in ten additional cups that contained neither adult X. jluvipes nor moth larvae. Mortality of the nymphs was determined after 1 day. The test was replicated five times each with males and virgin females.

Starvation resulted in increased cannibalism by adult males and virgin females. Thus mortality was nearly 100% among 1st instars exposed to starved adults for 1 day (Table I). Fed males inflicted essentially no mortality; fed females killed some nymphs but fewer than did starved females.

Feeding by nymphs on dead adults Xylocoris Jluvipes was reared individually in small cylindrical cages with only

dead adults as food. One newly hatched 1st instar was placed in each of 20 cages with two adults that had been killed by freezing. The insects were examined three times a week, and the dead adults were replaced with fresh material at that time.

In this test, nymphs were observed feeding with their stylets inserted through the

134 R. T. ARBOGAST

TABLE I

Effect of starvationfor 2 days on cannibalisticpredation by adult Xylocoris flavipes on 1st instars

Percentage mortality* among nymphs

Not exposed Exposed for I day to to adults Fed 63 Starved 6 d Fed 0 9 Starved p 0

3.05 I 5 4.0 + 2.4 100.0~0.0 18.Ok6.6 96.Ok4.0

* Mean f SE for ten replicates of ten nymphs each (unexposed nymphs) or for five replicates of ten

nymphs each (exposed nymphs).

intersegmental membranes of dead adults. Although these dead adults lost water rapidly and did not remain a suitable food source for very long, four of the nymphs did reach adulthood though development was slow 117-32 days (mean +SD=23.8?6.4) were required to reach the adult stage vs. about I I days for nymphs reared on paralyzed moth larvae]. Seven nymphs died as 5th instars, five as 4th instars, three as 3rd instars, and one as a 2nd instar.

DISCUSSION

Cannibalism in X. flavipes is apparently limited to predation on nymphs, saprophagous feeding on dead adults, and probably saprophagous feeding on dead nymphs. The results of the present study showed that all nymphal instars are attacked, but that the eggs are not. No successful attacks on adults were observed, and it seems unlikely that either nymphs or adults could subdue healthy adults, although they may prey on moribund individuals. Nymphs were shown to feed on dead adults, and saprophagous feeding by both nymphs and adults is probably not uncommon.

Cannibalism occurs at a high rate in crowded laboratory cultures and presents a problem in mass rearing X. fluvipes. The results of the present study indicate that this problem can be alleviated by separating eggs and adults before the eggs hatch and by providing an excess of food for the developing nymphs. Increasing the size of the rearing containers would be of little value since crowding in itself does not significantly affect the rate of cannibalism.

We can only speculate about the importance of cannibalism under natural conditions, because there are no quantitative estimates available for population levels of X. flavipes in storage habitats. Densities as high as those used in the present study probably do not occur except perhaps in situations where predators have congregated in the vicinity of prey aggregations. In such situations food would be abundant and cannibalism consequently low. On the other hand, prey scarcity frequently occurs during the early stages of infestation by storage pests, and under these circumstances cannibalism would serve to maintain the predator population. In fact, the effectiveness of X. flavipes in suppressing populations of stored-product beetles and moths (Arbogast, 1976, Press et al., 1975, LeCato et al.,

CANNIBALISM IN XYLOCORIS 135

1977) is probably enhanced by its cannibalistic behavior. The searching capacity of a predator, that is, its ability to find prey when prey populations are at low densities, is the most important quality that determines the effectiveness of the predator as a control agent (Doutt, 1964), and the capacity to survive is an obvious and important component of searching capacity. Because X. fravipes has little ability to withstand starvation (Arbogast et al., 1977), cannibalism must contribute significantly to its capacity for survival when prey density is low and must thus enhance its effectiveness as a control agent.

1 thank Margaret Carthon, Biological Technician at this laboratory, for assistance.

RESUME

LE CANNIBALISME DE XYLOCORIS FLAVIPES (HEM. ANTHOCORIDAE), PREDATEUR D’IN- SECTES DES DENREES STOCKEES

Les nymphes et les ad&es de Xylocorisflavipes (Reuter) consomment volontiers les membres de leur propre espbce. Une etude de laboratoire de ce cannibalisme a montrt que:

I) Ni les nymphes ni les adultes ne consomment les oeufs. 2) Les nymphes consomment les nymphes, et le taux de cannibalisme depend de la densite; cette

dependance provient pour I’essentiel de la competition alimentaire et non pas de la densite en elle- mime. Les nymphes peuvent achever leur dtveloppement en ne consommant que d’autres nymphes.

3) Les adultes consomment les nymphes; les femelles sont plus voraces que les males, et les femelles accouplees plus que les vierges. Les adultes provoquent la plus forte mortalitt parmi les nymphes du premier stade. Le taux de predation des adultes sur les nymphes est influence par la faim.

4) Les nymphes mangent les adultes morts et, au moins quelques unes, peuvent achever leur developpement saris aucune autre alimentation. II est peu vraisemblable que les nymphes et les adultes puissent attaquer avec succbs les adultes sains, mais probablement les unset les autres consomment des individus morts ou mourants.

Le cannibalisme doit augmenter la capacite de predation d’au moms quelques individus quand I’alimentation est peu abondante.

REFERENCES

ARBOGAST, R. T. (1976). Suppression of Oryzaephilus surinamensis (L.) (Coleoptera, Cucujidae) on shelled corn by the predator Xylocorisjluvipes (Reuter) (Hemiptera, Anthocoridae). J Ga. enr. Sot I1 : 67-71.

ARROGAST, R. T., LECATO, G. L. & CARTHON, M. (1977). Longevity of fed and starved Xylocorisflavipes (Reuter) (Hemiptera, Anthocoridae) under laboratory conditions. J. Cu. en?. Sot. 12 : 58-64.

DOUTT, R. L. (1964). Biological characteristics of entomophagous adults. In: P. DEBACH (Ed,). Biological Conlrolof Insect Pests and Weeds. Chapman & Hall, London, p. l45- 167.

LECATO. G L , COLLINS, J. M. & ARBOGAST, R. T. (1977). Reduction of residual populations of stored-

product insects by Xylocorisflavipes (Hemiptera: Anthocoridae). J Kans. enI. Sot. 50 : 84-88. PRESS. J W., FLAHERTY. B. R. & ARBOGAST, R. T. (1975). Control of the red flour beetle, Tribohum

castaneum, in a warehouse by a predaceous bug, Xylocorisjlavipes J Ga. eni Sot. 10 : 76-78. VARIEY, G. C. & GRADWELL, G. R. (1968). Population models for the wmter moth. In: T. R. E.

SOUTHWOOD (Ed ). Insect Abundance Symp R. em. Sot. Lond ‘No 4 p, 132-142.

VARLFY, G. C., GRADWELL, G. R. & HASSELL, M. P. (1973). Insect Population Ecology. An Analytical Approach. Blackwell Scientific Publications, Oxford. 212 pp.

Acceptedforpublication: October 9, 1978