ABSTRACT The host-feeding parasitoid Ooencyrtus nezarae Ishii accepted 0-7 d eggs of Riptortus clavatus Thunberg. Host acceptance behavior was divided ...
BEHAVIOR
Host Acceptance Behavior by the Host-Feeding Egg Parasitoid, Ooencyrtus nezarae (Hymenoptera: Encyrtidae): Host Age Effects KEIJI TAKASU1 AND YOSHIMI HIROSE 2 Institute of Biological Control, Faculty of Agriculture, Kyushu University, Fukuoka 812, Japan
Ann. Entomol. Soc. Am. 86(1): 117-121 (1993)
ABSTRACT The host-feeding parasitoid Ooencyrtus nezarae Ishii accepted 0-7 d eggs of Riptortus clavatus Thunberg. Host acceptance behavior was divided into four different behavioral phases: examining, drilling, host feeding, and ovipositing. The amount of feeding and number of eggs laid per host decreased with increasing host age. Females often rested during the host-feeding phase on 0-d hosts. Times of examining, feeding, and resting on 0-d hosts were longer than on the older hosts. Females appeared to regulate the amount of feeding and number of eggs laid based on host value, which decreases with increasing host age. KEY WORDS Ooencyrtus nezarae, host acceptance, host age
HOST ACCEPTANCE BEHAVIOR by egg parasitoids depends on the age of the egg (Vinson 1985, Pak 1986). Physical and physiological changes of hosts with increasing age affect whether parasitoid females oviposit (Hiehata et al. 1976, Strand & Vinson 1983, Pak 1986). The number of eggs deposited by females also differs with host age in gregarious parasitoid species (Lewis & Redlinger 1969, Marston & Ertle 1969, Parker & Pinnell 1974, Pak & Oatman 1982). Some of the variation in acceptance of hosts of different ages can be explained by optimal foraging theory (Pak 1986, Waage 1986), which predicts that on encountering a potential host, parasitoids should make "decisions" as to whether to oviposit or not, how many eggs to deposit, and of which sex, based on potential fitness gain per unit time (Charnov & Skinner 1985). Effects of host age on host acceptance by egg parasitoids have not been studied in hostfeeding species, except for species that occasionally host feed, such as Trichogramma species (Pak 1986). As far as we know, host feeding by egg parasitoids always occurs on hosts that are also used for oviposition (Jervis & Kidd 1986). For these parasitoids, hosts are important for maximizing both egg production and longevity (Jervis & Kidd 1986). Host-feeding parasitoids that forage optimally should decide how much host material to feed on, how much to leave for 1 Current address: Insect Biology & Population Management Research Laboratory, USDA-ARS, P.O. Box 748, Tifton, GA 31793. 2 To whom reprint requests should be addressed.
progeny, and how many eggs to oviposit. Physical and physiological changes in hosts caused by increasing age may affect feeding decisions as well as oviposition decisions of host-feeding egg parasitoids. Ooencyrtus nezarae Ishii is an egg parasitoid of several phytophagous Hemiptera including the bean bug, Riptortus clavatus Thunberg (Takasu & Hirose 1985, 1986). Adult females usually feed on host fluids after drilling and before ovipositing (Takasu & Hirose 1991). Host feeding is likely to be important for egg production in O. nezarae (K.T., unpublished data). Here we examine effects of host age on host acceptance and suitability and discuss implications of variation in host acceptance behavior toward hosts of different ages. Materials and Methods R. clavatus and O. nezarae used for this study were obtained from laboratory cultures and were reared as described by Takasu & Hirose (1988). R. clavatus eggs hatched 7-8 d after oviposition at 25°C. Unparasitized host eggs were held in clean tubes (18 by 3 cm) at 25°C for 0-7 d before experiments. On the day of emergence, male and female parasitoids were held in a test tube (18 by 3 cm) to ensure insemination of females. Afterward, because O. nezarae females normally do not lay eggs in a few days after emergence, females were kept individually in test tubes (15 by 1.5 cm) at 25°C for 3 d before experiments and provided with honey every day. The following experiments were done in the laboratory at 25°C,
0013-8746/93/0117-0121$02.00/0 © 1993 Entomological Society of America
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using 4-d females that had never oviposited and hosts of different ages. Host Acceptance. R. clavatus eggs usually are laid singly on host plants in nature (Takasu & Hirose 1985). Single host eggs 0, 1, 2, 3, 4, 5, 6, and 7 d old were attached with vinyl-acetate glue to a piece of filter paper (1 cm2). Individual female parasitoids were exposed to the filter paper in a test tube (15 by 1.5 cm). Behavior of females was observed under a binocular microscope from first contact until they left the hosts. Whether females oviposited at the first contact was recorded. Parasitism of hosts was identified by egg stalks of the parasitoids protruding from the host chorion (Takasu & Hirose 1988). Twenty females were tested for each host age. To examine acceptance behavior in detail, single host eggs 0, 2, 4, and 7 d2old were attached to a piece offilterpaper (1 cm ) and presented to a female parasitoid in a test tube (15 by 1.5 cm). Behavior was recorded by a Sony time-lapse video recorder attached to a binocular microscope. Video recordings were analyzed for behavioral sequence, time taken by each behavioral event, and number of eggs laid per host. Twenty females were tested for each host age. Host Suitability. Parasitized hosts on which acceptance behavior was examined in the above experiment were held in test tubes (15 by 1.5 cm) and reared at 25°C. Emergence date, number, and sex of parasitoids were recorded for each host. Preadult survival rate of parasitoid progeny from each host age class was determined as the number of eggs laid in hosts relative to number of adults that emerged. Forewing length of the emerged adults also was measured. Twenty parasitized hosts were examined for each host age. Voucher Specimens. Voucher specimens of O. nezarae have been deposited in the Institute of Biological Control, Faculty of Agriculture, Kyushu University.
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Table 1. Host acceptance behavior of O. nezarae on R. clavatus eggs Phase
Bout
Behavior
Drumming Standing still, preening Drilling Tapping, ovipositor rotating, touching, ovipositor withdrawing 0 Standing still, preening Resting Drumming, ovipositor inserting, Host feeding Feeding touching, ovipositor withdrawing, host liquid rapping Resting Standing still, preening Ovipositing Ovipositing Drumming, ovipositor inserting, touching, an egg laying, ovipositor withdrawing 0 Standing still, preening Resting
Examining
Examining Resting0 Drilling
' Occasionally occurred.
her antennae and remained motionless or preened (resting bout). The drilling phase usually consisted of one drilling bout, but one or more resting bouts occasionally occurred between drilling bouts (Table 1). After drumming, the female elevated her body and lowered her abdomen to tap the lateral surface of the host egg with the tip of her ovipositor. After several seconds of tapping, she inserted her ovipositor. During insertion, the sheath was removed from the ovipositor and the abdomen was returned to normal position. She continually rotated her ovipositor for penetration of the host egg chorion. Then she suddenly lowered her body and touched the surface of the host at the point where her ovipositor entered. Touching continued for several seconds before she raised her abdomen again. The action of touching was repeated six to eight times, after which the ovipositor was removed and sheathed. Females occasionally rested during this phase. The host-feeding phase consisted of 10-40 feeding bouts and one or more resting bouts (TaResults ble 1). After drilling, the parasitoid reinserted Host Acceptance. The percentages of females her ovipositor into the host and moved it up and that oviposited in 0-, 1-, 2-, 3-, 4-, 5-, 6-, and 7-d down several times, resulting in a drop of transhosts onfirstcontact were 85,85,90,100,95,100, lucent liquid forming at the point of ovipositor 95, and 95%, respectively. These acceptance insertion. After removing and sheathing her ovirates were not significantly different (chi-square positor, she backed away and lapped up the drop. She then inserted her ovipositor into the test of homogeneity of proportions, P > 0.05). Pattern of Host Acceptance Behavior. Behav- host again. Each feeding bout, from ovipositor ior after contacting hosts could be divided into insertion to lapping, required 1—5 min and was four phases: examining, drilling, host feeding, repeated 10-40 times. During this phase, feand ovipositing. Each phase consisted of one or males often rested on hosts for several minutes to more bouts that included several behaviors (Ta- > l h . The ovipositing phase usually consisted of ble 1). The examining phase usually consisted of one three to five ovipositing bouts, although resting examining bout, but occasionally two or more bouts occasionally occurred during this phase examining bouts occurred separated by resting (Table 1). After she completed feeding, she again bouts (Table 1). On contacting a host egg, a fe- inserted her ovipositor and repeated three or male mounted and walked over it while drum- four times the same touching action as observed ming her antennae. She occasionally lowered in drilling. Then she laid an egg into the host and
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HOST ACCEPTANCE BEHAVIOR OF
Table 2. Effect of host age on oviposition Host age, d
Mean no. of punctures per host0
Mean no. of e:ggs per host0
0 2 4 7
1.9a 1.7a 1.3b 1.2b
5.6a 5.4a 5. lab 4.5b
° Means followed by different letters in the same column differed significantly (P < 0.05, Duncan's multiple range test).
withdrew her ovipositor. Each ovipositing bout took 2-4 min. After she finished ovipositing, she drummed and tapped to find the puncture and then laid the next egg through it. Three to five eggs were deposited through the same puncture of the host. After the final oviposition, the parasitoid drummed the host. Then she descended from the host or began to tap another point on the lateral surface of the host egg for drilling. When she laid additional eggs in the same host, she repeated the behavioral sequence at another point on the host. Host Acceptance Behavior Toward Hosts of Different Ages. Mean number of feeding bouts made by females decreased with increasing host age (39.8,22.2,13.5, and 11.2 on 0-, 2-, 4-, and 7-d
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hosts, respectively). The number of feeding bouts on 0-d hosts was significantly greater than that on the older hosts (Duncan's multiple range test, P < 0.05). Females frequently oviposited through two punctures on a 0-d host, and the proportion of females ovipositing through two punctures on a host decreased with increasing host age. Mean number of the punctures per host made by a female was significantly larger on 0- and 2-d hosts than on 4- and 7-d hosts (P < 0.05) (Table 2). Mean number of parasitoid eggs laid in a host decreased with increasing host age and differed significantly between 0- or 2-d hosts and 7-d hosts (P < 0.05) (Table 2). Resting bouts occurred most often during the host-feeding phase on 0-d hosts. Mean time taken for resting bouts during the host-feeding phase was significantly longer on 0-d hosts than on the older hosts (P < 0.05) (Fig. 1). Handling Time. Total time for feeding and resting on each host decreased with increasing host age, so that total time taken for all behavioral phases on a host (i.e., mean handling time) was significantly longer for 0-d hosts than for 2-, 4-, and 7-d hosts (P < 0.05) (Table 3).
50 Types of hosts a
•r=
0 day ^ 2 day ^ 4 day
E30-J
• 7 day
O)
c
20-
c
Examining
Drilling
Host-feeding Ovipositing
Fig. 1. Frequency of mean resting time during examining, drilling, host-feeding, and ovipositing phases. Within a phase, bars capped by diflFerent letters diflFered significantly (P < 0.05, Kruskal-Wallis test).
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Table 3. Total time taken for behavior by parasitoids attacking host eggs of different ages Mean total time, min" Host age, Examining Drilling d '' feeding O v i P ° s i t i n g 0 2 4 7
4.6a 3.9b 3.7b 3.9b
85.7a 82.8a 84.1a 61.5a
51.6a 27.4b 18.2c 15.4c
17.2a 15.4a 15.8a 13.8a
Restin
g Total
53.6a 215.4a 12.2b 141.7b 6.4c 129.2b 4.1c 98.7b
" Times are for behavioral phases, excluding resting time. Means followed by different letters in the same column differed significantly (P < 0.05, Kruskal-Wallis test).
Host Suitability. Percentage survival of the parasitoid progeny for 7-d hosts was significantly (P < 0.05) lower than that for 2- and 4-d hosts but was not significantly lower than that for 0-d hosts (Table 4). Four to seven parasitoids emerged from each host. In all hosts tested, one male and three to five females emerged from each host, except for a 0-d host from which two males and five females emerged. Sex ratio of parasitoid progeny did not significantly differ among host ages (Table 4). For both sexes of parasitoids, there were no significant differences in mean development time from egg to adult among 0-, 2-, 4-, and 7-d hosts (females: 14.9, 14.9, 15.0, and 15.0 d; males: 14.7, 14.8, 14.7, and 14.8 d, respectively) (Duncan's multiple range test, P > 0.05). Regardless of sex, there were no significant differences in mean fore wing length of parasitoid adults among 0-, 2-, 4- and 7-d hosts, (females: 0.93, 0.94, 0.93, and 0.95 mm; males: 0.77, 0.78, 0.77, and 0.78 mm, respectively) (Duncan's multiple range test, P > 0.05). Discussion Host age had large effects on feeding, resting, and ovipositing behavior of O. nezarae. Although all host ages were accepted, the number of feeding bouts and the number of eggs laid per host decreased with increasing host age. Time spent feeding and resting was longer on 0-d hosts than on the older hosts. This resulted in longer hanTable 4. Effects of host age on survival and sex ratio of parasitoid progeny Host age, d
% Survival"-6
Sex ratio (% males )b
88.0ab 96.3a 96.1a 72.1b
21.6a 20.5a 20.6a 28.6a
° Proportion of number of parasitoid adults to number of eggs laid in 20 hosts of each age. h Percentages followed the different letters in the same column differed significantly (P < 0.05, chi-square test of homogeneity of proportions).
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dling time on 0-d hosts (mean, 215 min) compared with that on the older hosts (means, 98— 141 min). Such a large effect of host age on handling time of egg parasitoids has not been reported before. The number of feeding bouts decreased with increasing host age. This decrease is probably caused by the decreasing amount of host contents that females can extract. O. nezarae females fed on host fluid such as yolk or hemolymph that exudes from punctures of hosts after the pumping action of the ovipositor. Newly deposited R. clavatus eggs consist almost entirely of yolk, but as the host embryo develops the amount of yolk decreases. A 7-d egg in which the embryo has almost completed development contains only a small amount of hemolymph (K. T., unpublished data). We often observed a large droplet of host fluid exuded from the puncture after the paras itoid's pumping action on 0- or 2-d hosts, but droplets exuded from 4- and 7-d hosts were much smaller. Females often rested for several minutes over 1 h on 0-d hosts. Such resting during host acceptance in egg parasitoids has not been reported, except in O. kuvanae (Howard), a relative of O. nezarae (Maple 1937). Resting in O. nezarae appears to be associated with host feeding. After feeding on prey, insect predators are known to pause to digest the prey consumed before resuming prey search (Holling 1966). In the current study, most resting bouts occurred during the host-feeding phase on 0-d hosts, from which females fed on a large amount of host fluid. This suggests that they become satiated in the course of host-feeding phase and then rest to digest the host fluid. Some gregarious egg parasitoids are known to allocate eggs they lay in a host based on host age (Lewis & Redlinger 1969, Marston & Ertle 1969, Parker & Pinnell 1974, Pak & Oatman 1982). It has been suspected that parasitoids can estimate the value of a host for progeny development (the number and quality of parasitoid progeny that it can support) (Pak 1986) and regulate the number of eggs laid (Waage 1986). In the current study, the number of eggs laid decreased with increasing host age. Progeny survival, developmental time, or size of emerged parasitoids did not differ among host ages, except for lower survival rate of parasitoids in 7-d hosts. The amount of host material on which O. nezarae larvae feed appears to decrease with increasing host age. Parasitoid larvae do not feed on sclerotized parts of heads or legs of host embryo, and these parts remain in hosts after parasitoid emergence (K. T., unpublished data). These facts suggest that O. nezarae females adjust the number of eggs laid in hosts to host value. We observed host acceptance behavior of O. nezarae on single host eggs of different ages in this study because host eggs are usually laid sin-
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TAKASU & HiROSE: HOST ACCEPTANCE BEHAVIOR OF Ooencyrtus nezarae
gly in nature. Factors such as host distribution and host encounter rate by parasitoids, however, may affect host acceptance behavior by parasitoids (e.g., acceptance-contact ratio, feeding frequency, and the number and sex of eggs laid per host). In the egg parasitoids, Trichogramma spp., clutch size and sex ratio differ between single and clumped hosts and between high and low host encounter rates (Waage 1986). The amount and frequency of host feeding by several parasitoids vary with different host encounter rate (Jervis & Kidd 1986). Future study on the effect of host distribution and host encounter rate on host acceptance behavior is needed.
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Marston, N. & L. R. Ertle. 1969. Host age and parasitism by Trichogramma minutum (Hymenoptera: Trichogrammatidae). Ann. Entomol. Soc. Am. 62: 1476-1482. Pak, G. A. 1986. Behavioural variations among strains of Trichogramma spp.: a review of the literature on host-age selection. J. Appl. Entomol. 101: 55-64. Pak, G. A. & E. R. Oatman. 1982. Biology of Trichogramma brevicapillum. Entomol. Exp. Appl. 32: 61-67. Parker, F. D. & R. E. Pinnell. 1974. Effectiveness of Trichogramma spp. in parasitizing eggs of Pieris rapae and Trichoplusia ni in the laboratory. Environ. Entomol. 3: 935-938. Strand, M. R. & S. B. Vinson. 1983. Factors affecting host recognition and acceptance in the egg parasiAcknowledgments toid Telenomus heliothidis (Hymenoptera: Scelionidae). Environ. Entomol. 12: 1114-1119. We thank W. Sheehan for reviewing the manuscript. This study was supported by a grant from Japan Min- Takasu, K. & Y. Hirose. 1985. Seasonal egg parasitism of phytophagous stink bugs in a soybean field in istry of Agriculture, Forestry and Fisheries, and a JSPS Fukuoka (In Japanese with English summary). ProFellowship for Japanese Junior Scientists to K.T. ceedings of the Association for Plant Protection of Kyushu 31: 127-131. References Cited 1986. Kudzu-vine community as a breeding site of Ooencyrtus nezarae Ishii (Hymenoptera: EnCharnov, E. L. & S. W. Skinner. 1985. Complemencyrtidae), an egg parasitoid of bugs attacking soytary approaches to the understanding of parasitoid bean. Jpn. J Appl. Entomol. Zool. 30: 302-304 (in oviposition decisions. Environ. Entomol. 14: 383Japanese with English abstract). 391. 1988. Host discrimination in the parasitoid OoenHiehata, K., Y. Hirose & H. Kimoto. 1976. The efcyrtus nezarae: the role of the egg stalk as an exterfect of the host age on the parasitism by three spenal marker. Entomol. Exp. Appl. 47: 45-48. cies of Trichogramma (Hymenoptera: Trichogram1991. The parasitoid Ooencyrtus nezarae (Hymatidae), egg parasitoids of Papilio xuthus Linn6 menoptera: Encyrtidae) prefers hosts parasitized by (Lepidoptera: Papilionidae). Jpn. J. Appl. Entomol. conspecifics over unparasitized hosts. Oecologia 87: Zool. 20: 31-36 (in Japanese with English synop319-323. sis). Holling, C. S. 1966. The functional response of in- Vinson, S. B. 1985. The behavior of parasitoids, pp. 417-469. In G. A. Kerkut & L. I. Gilbert [eds.], vertebrate predators to prey density. Mem. EntoComprehensive insect physiology biochemistry mol. Soc. Can. 48: 1-86. and pharmacology, vol. 9 Behaviour. Pergamon Jervis, M. A. & N.A.C. Kidd. 1986. Host-feeding Press, Oxford. strategies in hymenopteran parasitoids. Biol. Rev. 61: 395-434. Waage, J. K. 1986. Family planning in parasitoids: Lewis, W. J. & L. M. Redlinger. 1969. Suitability of adaptive patterns of progeny and sex allocation, pp. eggs of the almond moth, Cadra cautella, of various 63-95. In J. Waage & D. Greathead [eds.], Insect ages for parasitism by Trichogramma evanescens. parasitoids. 13th Symposium of the Royal EntomoAnn. Entomol. Soc. Am. 62: 1482-1484. logical Society of London, Academic Press, LonMaple, J. D. 1937. The biology of Ooencyrtus don. johnsoni (Howard), and the role of the egg shell in the respiration of certain encyrtid larvae (HyReceived for publication 23 March 1992; accepted menoptera). Ann. Entomol. Soc. Am. 30: 123-154. 28 September 1992.
