Appl. Entomol. Zool. 39 (4): 661–667 (2004) http://odokon.ac.affrc.go.jp/
Predation of Dysdercus cingulatus (Heteroptera: Pyrrhocoridae) by the specialist predator Antilochus coqueberti (Heteroptera: Pyrrhocoridae)
Katsuyuki KOHNO,1,*,† BUI THI Ngan1 and Mitsuhiro FUJIWARA2 1 Okinawa Subtropical Station, Japan International Research Center for Agricultural Sciences; Ishigaki, Okinawa 907–0002, Japan 2 36 Ko, Wada, Hojo, Ehime 799–2465, Japan (Received 20 October 2003; Accepted 16 July 2004)
Abstract Antilochus coqueberti predators of each developmental stage exhibited a relatively broad prey size range against their prey Dysdercus cingulatus when a single prey individual was provided in the laboratory. On the other hand, when two prey individuals of different developmental stages were provided together for a single predator in the laboratory, younger predators tended to attack younger prey and older predators tended to attack older prey. This tendency is sim- ilar to that observed in the field. During its nymphal developmental period, the predator killed fewer prey individuals when fed older prey, and more prey individuals when fed younger prey individuals. Predators of all nymphal instars examined exhibited a Holling’s type II functional response to prey density, even if the developmental stages of the prey were different. The predatory properties of the predator elucidated in this study can provide a basis for a biologi- cal control program of D. cingulatus using its specialist predator A. coqueberti.
Key words: Antilochus coqueberti; Dysdercus cingulatus; prey size preference; prey consumption; functional re- sponse
Antilochus coqueberti (Fabricius) (Heteroptera: INTRODUCTION Pyrrhocoridae) is known to be a specialist predator Cotton is the most economically important natu- of the cotton stainer Dysdercus cingulatus (Fabri- ral fiber material in the world. One of the major ob- cius) (Heteroptera: Pyrrhocoridae) and related stacles hindering cotton cultivation is insect pest species (Corbett, 1923; Chauthani and Misra, infestation. The cotton stainers Dysdercus spp. 1966; Iwata, 1975, 1978b; Quayum and Nahar, (Heteroptera: Pyrrhocoridae) in particular cause 1980; Dhiman, 1985). In addition, Kohno et al. serious damage by feeding on developing cotton (2002) reported that A. coqueberti attacked all bolls and ripe cotton seeds and transmitting fungi pyrrhocorid and two alydid bug species inhabiting that develop on the immature lint and seeds the Southwest Islands of Japan, but did not attack (Maxwell-Lefroy, 1908; Freeman, 1947; Van Does- largid, lygaeid, coreid or rhopalid bugs, which are burg, 1968; Fuseini and Kumar, 1975; Iwata, 1975, similar in appearance to pyrrhocorid bugs. Kohno 1978a; Ahmad and Kahn, 1980; Ahmad and et al. (2002) also reported that A. coqueberti is Schaefer, 1987; Yasuda, 1992). These pests are dif- obligatorily predaceous; the natural host plants of ficult to control by insecticide because they are D. cingulatus such as Hibiscus tiliaceus or H. highly mobile and have many alternative wild host makinoi (Kohno, 2001; Kohno and Bui Thi, 2004) plants (Iwata, 1975, 1978a, b; Kohno and Bui Thi, are not available to A. coqueberti as food. There- 2004). Therefore, the use of natural enemies to fore, A. coqueberti has no harmful effect on these control these pests should be considered because plants, and should be regarded as a good potential natural enemies can be used not only in cultivated biological control agent against D. cingulatus in cotton fields, but also in vegetative stands contain- cotton fields. Kohno (2003) further reported that A. ing wild alternative host plants of cotton stainers. coqueberti has desirable characteristics as a biolog-
*To whom correspondence should be addressed at: E-mail: [email protected] † Present address: National Institute of Vegetable and Tea Science, 360 Kusawa, Ano cho, Mie 514–2392, Japan DOI: 10.1303/aez.2004.661
661 662 K. KOHNO et al. ical control agent against cotton stainers; that is, it tion of the mortality factors of the examined prey has great fecundity and no reproductive diapause is difficult, the daily nymphal mortality of D. cin- induced by a short photoperiod. Nevertheless, the gulatus under rearing conditions in the absence of predatory ability of A. coqueberti has not yet been predators is negligibly low (Kohno and Bui Thi, well studied. 2004). Therefore, all dead prey were judged to In the present study, we examined various prop- have been killed by the predator. Twenty predators erties of the predatory ability of A. coqueberti were examined under each experimental condition. against D. cingulatus in the laboratory. In addition, Prey size preferences of the predator. Two we observed the natural predation of A. coqueberti prey individuals of different developmental stages in the field in order to evaluate the results of our were kept in a container (8 cm diameter and 4 cm laboratory experiment. depth), and one predator individual of each devel- opmental stage was introduced into it. We recorded which of the two prey individuals was killed first, MATERIALS AND METHODS and the experiment was terminated when either of General experimental conditions. All labora- the two prey individuals was killed. This experi- tory experiments were conducted at a temperature ment was executed twenty times for every combi- of 25°C and with a photoperiod of 14L–10D. Each nation of developmental stages of predator and predator was reared in a transparent plastic con- prey. tainer and provided with prey and water. Functional response of the predator to prey A. coqueberti, the predator. All insects used in density. Various densities and developmental the present experiments were reared in the labora- stages of the prey were provided for predators of tory from eggs laid by mother insects collected in each instar in a container (8 cm diameter and 4 cm the field on Ishigaki-jima Island. All third-, fourth-, depth) as shown in Table 1. The number of killed and fifth-instar nymphs and adults used in the ex- prey was determined after 24 h. The number of periments were fed D. cingulatus nymphs or adults replications for each prey density was as follows: and water until the last molting before the experi- eight replications for a density of one, two or four ment, but the second instar nymphs used in the ex- prey individuals per container; four replications for periment were provided only water, because the a density of eight or sixteen prey individuals per first instar nymphs do not require anything but container; and two replications for a density of water until molting to the second instar (Kohno et thirty-two or sixty-four prey individuals per con- al., 2002). All insects were used at about one day tainer. past molting, having taken a diet of only water. Number of prey killed by predators of each D. cingulatus, the prey. The majority of insects instar. Each predator of each instar was fed suffi- used in the present experiments were collected in cient prey of each instar daily in a container (5 cm the field on Ishigaki-jima Island. Some of the in- diameter and 1 cm depth) and the number of killed sects, especially the younger instar nymphs, were prey was recorded. Twenty predator individuals reared in the laboratory and fed seeds of H. maki- were used for every experimental condition except noi from eggs laid in the laboratory by females col- for the condition of second-instar predator against lected in the field on Ishigaki-jima Island. Adults adult prey, for which ten predator individuals were were used as prey without distinction between used. sexes except for pregnant female, because the body Observation of predation in the field. Field ob- size of males and non-pregnant females does not servation of the predation of A. coqueberti against differ much. D. cingulatus was conducted in several of their nat- Effect of the developmental stage of prey on ural habitats on Ishigaki-jima Island from January successful attack rate of the predator. One prey of 1999 to September of 2003. When predation individual of each developmental stage was pro- was observed, the developmental stage of the prey vided for each predator individual of each develop- and that of the predator were recorded. mental stage in a container (5 cm diameter and 1 cm depth). Whether or not the prey was killed was confirmed after 24 h. Although the discrimina- Predation by Antilochus coqueberti 663
Table1. The combinations of the developmental stages of the predator Antilochus coqueberti and the prey Dysdercus cingulatus, and prey density in the experiments for elucidating the functional response of the predator to prey density
Predator Prey Prey number per container
2nd instar nymph 2nd instar nymph 1, 2, 4, 8, 16 3rd instar nymph 1, 2, 4, 8 4th instar nymph 1, 2, 4 5th instar nymph and Adult 1, 2 3rd instar nymph 2nd instar nymph 1, 2, 4, 8, 16, 32 3rd instar nymph 1, 2, 4, 8, 16 4th instar nymph 1, 2, 4, 8 5th instar nymph and Adult 1, 2, 4 4th instar nymph 2nd instar nymph 1, 2, 4, 8, 16, 32 3rd, 4th and 5th instar nymph 1, 2, 4, 8, 16 Adult 1, 2, 4, 8 5th instar nymph 2nd and 3rd instar nymph 1, 2, 4, 8, 16, 32, 64 4th and 5th instar nymph 1, 2, 4, 8, 16, 32 Adult 1, 2, 4, 8, 16
Table2.Percentages of each developmental stage of the RESULTS prey Dysdercus cingulatus killed by each developmental Effect of the developmental stage of prey on suc- stage of the predator Antilochus coqueberti within 24 h cessful attack rate of the predator Killed prey (percentage) Although every fourth- and fifth-instar predator Predator n examined killed a provided prey individual within 2nd 3rd 4th 5th Adult 24 h irrespective of the developmental stage of the instar instar instar instar prey, the proportions of killed prey were low when a fifth-instar (25%) or adult (5%) prey was pro- 2nd instar 20 100 100 90 25 5 3rd instar 20 100 100 100 100 55 vided for a second-instar predator or when a sec- 4th instar 20 100 100 100 100 100 ond-instar prey was provided for an adult predator 5th instar 20 100 100 100 100 100 (10%) (Table 2). The results obtained by this ex- Adult 20 10 65 95 95 95 periment may represent the ranges of acceptable prey size by predators of each developmental stage. killed prey increased; in contrast, the proportion of Prey size preferences of the predator killed prey decreased under all examined condi- The numbers of prey at each developmental tions (Fig. 1). Therefore the relationship between stage that were attacked first by a predator in each prey density and the number of killed prey under combination are shown in Table 3. Younger (sec- all examined conditions exhibited curves of a Type ond- and third-instar) predators in many cases II functional response (Holling, 1959), i.e., simple tended attacked younger prey first and older saturated curves. (fourth- and fifth-instar and adult) predators in many cases attacked older prey first. This tendency Number of prey killed by predators at each de- was particularly prominent in the case of second- velopmental stage instar and adult predators. However, the tendency The numbers of prey killed by predators at each was not clear when the difference of the develop- developmental stage increased according to the mental stages between two prey individuals pro- progress of the developmental stage of the predator vided in each combination was small, especially in (Table 4). Similarly, the number of killed prey was the case of fourth-instar predators. smaller when older prey individuals were provided, and the number was larger when younger prey in- Functional response of predator to prey density dividuals were provided (Table 4). However, only As the prey density increased, the number of three out of 10 second-instar predators killed adult 664 K. KOHNO et al.
Table3. Number of each developmental stage of the prey Dysdercus cingulatus attacked first by the predator Antilochus coque- berti in each combination of two prey individuals. Twenty replications were done for each combination. Numbers in boldface and in italics indicate that the values are significantly different from even at 1% and 5% risk by the binominal test, respectively.
Counterpart prey Second instar predator
2nd 3rd 4th 5th Adult
2nd — 10 14 19 20
3rd 10 — 13 19 20
Prey attacked at first 4th 6 7 — 17 20 5th 113— 20 Adult 000 0—
Counterpart prey Third instar predator
2nd 3rd 4th 5th Adult
2nd — 10 9 14 17
3rd 10 — 10 14 17
Prey attacked at first 4th 11 10 — 15 15 5th 6 6 5 —13 Adult 3357—
Counterpart prey Fourth instar predator
2nd 3rd 4th 5th Adult
2nd — 55 59
3rd 15 —81110
Prey attacked at first 4th 15 12 — 10 14 5th 15 910—12 Adult 11 10 6 8 —
Counterpart prey Fifth instar predator
2nd 3rd 4th 5th Adult
2nd — 32 11
3rd 17 — 335
Prey attacked at first 4th 18 17 —710 5th 19 17 13 — 11 Adult 19 15 10 9 —
Counterpart prey Adult predator
2nd 3rd 4th 5th Adult
2nd — 00 00
3rd 20 — 322
Prey attacked at first 4th 20 17 —66 5th 20 18 14 — 10 Adult 20 18 14 10 — Predation by Antilochus coqueberti 665
Fig. 1. Numbers and proportions of prey Dysdercus cingulatus at various developmental stages killed by a predator Antilochus coqueberti at various developmental stages within 24 h under various prey densities. Thick lines and vertical bars with anchors in- dicate the mean numbers and the ranges of killed prey within 24 h, respectively (left vertical axis). Thin lines indicate the propor- tion of prey killed within 24 h (right vertical axis).
Table4. Number of the prey Dysdercus cingulatus killed by the predator Antilochus coqueberti during each developmental stage of the predator when fed prey at each developmental stage. Each value is given as mean SD [minimum–maximum]. The number of replications for each treatment was twenty except for the second instar predator against adult prey.
Prey
2nd instar 3rd instar 4th instar 5th instar Adult
a
2nd instar 8.1 1.3 [6–10] 4.8 0.9 [4–6] 2.3 0.6 [2–4] 1.2 0.4 [1–2] 1.0 0.0 [1–1]
3rd instar 15.7 1.9 [13–20] 7.6 1.3 [6–10] 3.5 0.9 [3–6] 2.6 0.6 [2–4] 2.2 0.4 [2–3]
Predator 4th instar 23.8 3.6 [19–30] 16.1 2.4 [12–20] 8.1 1.1 [7–10] 6.1 1.1 [5–9] 4.4 1.0 [3–6] 5th instar 49.6 4.7 [41–58] 39.0 3.2 [32–44] 21.7 2.6 [17–25] 13.9 2.3 [11–18] 9.7 1.3 [8–12]
a Only 3 out of 10 second instar predators killed adult prey; the rest did not, and died. prey and the rest did not, and died. If each predator Observation of predation in the field is fed prey at the second-, third-, fourth-, and fifth- No first-instar predators or first-instar prey were instar and adult stages throughout the predator’s observed in the field. One hundred forty-five cases nymphal development, the total numbers of prey of predation against D. cingulatus by A. coqueberti killed by predators at each stage are estimated to be were observed in the field during the observation 97.2, 67.5, 35.6, 23.8, and 17.3, respectively. period. Most cases of predation were observed at vegetative stands containing H. makinoi. The fre- 666 K. KOHNO et al.
Table5. The combination of the developmental stage of the discuss the preferences of predators to the develop- predator Antilochus coqueberti and that of the prey Dysdercus mental stages of prey in the field more strictly, the cingulatus in each predation when predation was observed in developmental-stage structure of the prey popula- the field. Neither the first instar predator nor the first instar prey was observed in the field. tion in the field at the time of each observation should be considered; however, the results of our No. of predation against Dysdercus laboratory experiments (Tables 2 and 3) may well cingulatus observed in the field explain the results of our field observations (Table Predator n 5). Given the results of our laboratory experiments, 2nd 3rd 4th 5th Adult instar instar instar instar second-instar predators are also expected to show a preference for younger prey in the field. It may be 2nd instar 1 0 0 1 0 0 possible to conclude that the range of developmen- 3rd instar 16 6 4 3 2 1 tal stages of prey attacked by predators at each de- 4th instar 24 2 4 9 4 5 velopmental stage is relatively broad, although 5th instar 51 1 7 7 24 12 there is a tendency for younger predators to attack Adult 53 0 1 8 12 32 younger prey and for older predators to attack older prey. The relatively broad range of develop- quencies of the combinations of the developmental mental stages of prey used by the predator A. co- stages of A. coqueberti and those of D. cingulatus queberti is a desirable property for a potential bio- in each case of predation are summarized in Table logical control agent against D. cingulatus in the 5. Natural predation by a second instar predator field. was observed only once. The results (Table 5) seem Predators of every instar exhibited the Type II to show a tendency for smaller predators to attack functional response described by Holling (1959), smaller prey and larger predators to attack larger i.e., a simple saturated curve, to prey densitiy when prey; in particular, most adult predators attacked prey of any developmental stage was provided (Fig. adult prey. Additionally, third, fourth and fifth in- 1). This may imply that there is an upper limit to star predators seemed to have a wide spectrum in the rate of prey consumption by the predator. Our the range of developmental stages of their prey, as results showing that more prey was killed when predation by these predators against prey at all de- younger prey was provided and less prey was killed velopmental stages was observed in the field. when older prey was provided for predators at every instar (Table 4) also implies that there is an upper limit to the prey consumption amount at DISCUSSION each developmental stage. Therefore, it may be The results shown in Table 2 may indicate that necessary to examine the ratio of the number of A. adult and fifth-instar prey are too large for a sec- coqueberti to prey density when A. coqueberti is ond-instar predator and that second-instar prey are used as a biological control agent in the field. If an too small for an adult predator. As a general ten- artificially reared predator is released for control of dency, however, it is possible that the acceptable the prey D. cingulatus in the field, releasing while developmental-stage ranges of prey for each devel- the prey is still at a young instar is recommended opmental stage of predator is considerably broad. since more prey is killed when the provided prey is On the other hand, when two prey individuals of younger (Table 4). different developmental stages were provided for a All of the predatory properties of A. coqueberti predator at the same time, predators of every devel- elucidated in the present study can serve as the opmental stage exhibited stage-specific prefer- basis for planning a biological control program of ences; i.e., younger predators tended to kill D. cingulatus using A. coqueberti. Prey consump- younger prey first and older predators tended to kill tion by female predators is expected to have a close older prey first (Table 3). Although our field obser- relationship with fecundity. Such a relationship is vation of predation by second-instar predators was an indispensable piece of information for planning limited, younger predators preferably attacked a persistent biological control method using the younger prey and older predators preferably at- predator. Kohno (2003) reported the ovipositional tacked older prey in the field (Table 5). If we are to properties of the predator when it was fed one adult Predation by Antilochus coqueberti 667 prey daily; however, it is not clear whether or not Holling, C. S. (1959) Some characteristics of simple types of the prey supply in that study was sufficient. It is, predation and parasitism. Can. Entomol. 91: 385–398. therefore, necessary to examine the relationships Iwata, K. (1975) Shizen Kansatsusha no Shuki (Memoirs on Nature by an Observer). Asahi Shimbun Co., Tokyo. between the prey supply and the fecundity of the 584 pp. (in Japanese). predator in order to construct a more rigid control Iwata, K. (1978a) Konchu wo Mitsumete 50 Nen (Fifty-Year- program against D. cingulatus using A. coqueberti. Observation of Insects). Volume 1. Asahi Shimbun Co., In addition, if the mass rearing of the predator is Tokyo. 343 pp. (in Japanese). considered, possible cannibalism among the preda- Iwata, K. (1978b) Konchu wo Mitsumete 50 Nen (Fifty-Year- Observation of Insects). Volume 2. Asahi Shimbun Co., tors may raise their mortality. Thus, the cannibalis- Tokyo. 330 pp. (in Japanese). tic characteristics of the predator should also be Kohno, K. (2001) Host plant of Dysdercus poecilus (Het- elucidated in future studies. eroptera: Pyrrhocoridae) and its relative species in Ishi- gaki-jima Island, the Ryukyus, Japan. Rostria 50: ACKNOWLEDGEMENTS 31–34 (in Japanese with English summary). 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