Biological Control 97 (2016) 57–62

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Biological Control

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Effect of parasitoid density on the timing of parasitism and development duration of progeny in Sclerodermus pupariae (Hymenoptera: Bethylidae) ⇑ Shang–Kun Gao, Ke Wei, Yan–Long Tang , Xiao–Yi Wang, Zhong–Qi Yang

Key Laboratory of Forest Protection, China State Forestry Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing 100091, China highlights graphical abstract

 Sclerodermus pupariae parasitoid density affected adult and offspring performance.  Intraspecific cooperation improved the parasitic efficacy of wasps on one host.  The parasitoids well displayed mutually beneficial behaviors.

article info abstract

Article history: The gregarious idiobiont ectoparasitoid, Sclerodermus pupariae Yang et Yao, is a natural enemy that par- Received 20 October 2015 asitizes buprestid and cerambycid larvae in China. In a recent laboratory study of mass–reared Revised 25 February 2016 female parasitoids on larvae of the substitute host, gebleri, the subsequent offspring were Accepted 6 March 2016 widely released to control target pests. To develop cost–effective techniques for rearing parasitoids, Available online 8 March 2016 and improve the parasitic efficiency of Sclerodermus pupariae, several parasitoid–host ratios have been investigated. However, the mechanism whereby increasing the density of inoculated female wasps on Keywords: a host affects female parasitoid fitness (adult performance and progeny developmental duration) remains Sclerodermus pupariae unclear. In the present study, we examined the influence of parasitoid density (one to eight female wasps Parasitoid density Adult performance per host) on the time to first attack, paralyzing time, pre–oviposition period and oviposition period of Developmental duration foundresses and developmental duration of offspring. We showed that the time to first attack, paralyzing Quasi–social parasitoids time, pre–oviposition period and oviposition period of foundresses were significantly negatively associ- ated with parasitoid density, but that developmental duration of progeny was only affected at the larval stage. An increase in the parasitoid density to more than three female wasps per host had no significant influence on the investigated parameters. Our results suggest that host nutrition was adequate, and intraspecific interaction enhanced the parasitic efficiency of wasps sharing a single host. Furthermore, it is known that a suitable parasitoid–host ratio can play an important role in promoting mutually ben- eficial behaviors which enhance adult performance. Ó 2016 Elsevier Inc. All rights reserved.

1. Introduction

Parasitoid wasps of the family Bethylidae are widely used as biological control agents for some woodborer in Asia ⇑ Corresponding author. E-mail address: [email protected] (Y. Tang). (Tang et al., 2012; Wang, 2005; Wang et al., 2010; Yang et al., http://dx.doi.org/10.1016/j.biocontrol.2016.03.003 1049-9644/Ó 2016 Elsevier Inc. All rights reserved. 58 S. Gao et al. / Biological Control 97 (2016) 57–62

2013). For example, Scleroderma guani is one of the most widely the developmental duration of progeny. We compared parasitism used natural enemy species of small and medium sized larvae of parameters such as time to first attack, time to paralysis, pre– several long–horned beetles in China (Chen and Cheng, 2000; oviposition period, oviposition period and development durations Huang et al., 2006; Ma, 2007; Xiao and Wu, 1983; Xu et al., of offspring at various maternal parasitoid densities. 2002; Yao and Yang, 2008; Zhou and Yang, 1997). The gregarious idiobiont ectoparasitoid Sclerodermus pupariae Yang et Yao (Hyme- 2. Materials and methods noptera: Bethylidae) is a species newly discovered from Tianjin, China. This species which parasitizes the pupal or late larval stages 2.1. Experimental materials of the emerald ash borer beetle, Agrilus planipennis, has been found in northern China, 15 states of the USA, and two provinces of We established our laboratory population of S. pupariae from A. Canada, where it causes substantial economic and environmental planipennis larvae collected in the late autumn of 2011 at Guan- damage (Yang et al., 2012; Haack et al., 2002). gang Forest Park, Dagang District, Tianjin, China. Prior to our exper- Sclerodermus pupariae overwinters as apterous females in emer- iment, we reared 30 generations of parasitoids on T. gebleri larvae ald ash borer galleries or in ash bark crevices and emerges in late in the laboratory to exclude the possible influences of the host June. When a female parasitoid locates an A. planipennis larva, source (King, 1987). The parasitoids were maintained at 25 ± 5 °C the duration of the pre–oviposition period is approximately one and 60–70% RH under a LD 10:14 h light regime. The substitute week; the female then lays 26–58 eggs, depending on host size. host species (T. gebleri) used in mass–rearing S. pupariae, was col- Eggs hatch within approximately 2 d, and the larvae develop lected from Tianjin, China. Host larvae were weighed using an ana- ° within one week at 25 C. The duration of the pupal stage last is lytical balance (sensitivity 0.1 mg), and 96 larvae (weight range 15–20 d and 24–56 adult wasps are produced per brood. The aver- 200.0–240.0 mg) were selected for our experiment. Although there age sex ratio is 22:1 females to males. During the developmental was a 40 mg variation among the hosts used, our preliminary test period of offspring, the female parasitoids provide maternal care. indicated that the interaction between host weight and foundress This consists of the following aspects: (i) the female cleans the host numbers were not significant. We regarded host size as a constant. body removing frass and dirt; (ii) if any eggs or larvae fall off the host, the female picks them up and replace them on the host; 2.2. Inoculation of Sclerodermus pupariae (iii) if any of the progeny are infested by bacteria or fungi, the female moves these larvae far from the brood and excretes an We randomly selected 432 mated and healthy female wasps antibiotic substance to prevent microbial spread; (iv) the mothers with an average age of one week after emergence. Individual hosts leave their progeny to search for additional hosts only after the off- were exposed to different numbers of female parasitoids (from one spring have successfully emerged as adults (Wu et al., 2008a; Yang to eight) in a vial (5 Â 1 cm). The opening of each vial was blocked et al., 2012). with a cotton plug. We conducted 12 trials for each of the eight Under laboratory or field conditions, Sclerodermus pupariae also parasitoid–host ratios examined. All experimental were attacks major pests of trees such as wild apple trees, pine wood, maintained in an artificial–climate chamber at 25 ± 1 °C and RH deciduous broadleaf tree species, oak trees and other landscaping 60–70%, under a LD 14:10 h light regime. greening trees specie in China (Tang et al., 2014b; Wu et al., 2008b; Wang et al., 2010, 2014). Previous studies have mainly focused on the mechanism whereby this generalist parasitoid 2.3. Observation of female parasitoid performance adapts to different–sized hosts under a one wasp–one host rela- tionship. Wei et al. (2014) found that S. pupariae optimized its We defined the time to first attack as the period between inoc- developmental times and progeny size according to the abundance ulation and the first wasp sting (to the host). Furthermore, the per- of different–sized beetle larvae (Massicus raddei). Furthermore, the iod between the first wasp sting and the onset of paralysis in host parasitic efficiency on novel hosts was enhanced by learning expe- larvae was defined as the paralysis time. We monitored the time to rience (Wei et al., 2013). These findings indicate that S. pupariae is first attack and paralysis time every 20 min. S. pupariae is a synovi- an important natural enemy and population controller of wood genic parasitoid, with oogenesis occurring after females are stimu- borer beetles in China, and that this parasitoid has strong host lated by feeding on host hemolymph (Wei et al., 2014). Hence, we searching and attacking abilities. defined the pre–oviposition period as the time interval between The success of biological control with inundative parasitoid host paralysis and the first egg laid. We defined the oviposition releases depends, in part, on the efficiency and quality of the arti- period as the period between the first and last eggs laid. ficial mass–rearing system (Chambers, 1977). Currently, the larvae of populnea and the pupae of Tenebrio molitor have been 2.4. Parasitoid offspring developmental processes at different maternal used as substitute hosts for artificially mass–rearing S. guani. Addi- densities tionally, our laboratory has reported that the long–horned beetle larva, , is high–quality substitute host of Scleroder- We monitored the developmental processes of parasitoid off- mus due to its comparatively large body size. Furthermore, the spring (oviposition to emergence) for each replicate. The egg stage self–defense behaviors of T. gebleri are typically very weak. In gen- was calculated as the time interval between the first egg laid and eral, a middle–instar T. gebleri larva can be successfully parasitized the first larva emergence. We defined the larval stage as the period by a single S. pupariae female. However, artificially mass–rearing S. between the emergence of the first larva and the first cocoon. pupariae has led to several problems as follows: (i) a single wasp Finally, the pupal stage was considered the time interval between can paralyze a large host because of its strong aggressive behav- the emergence of the first cocoon and the first adult. All parasitized iors; (ii) the offspring of a single maternal wasp cannot effectively hosts were observed twice daily under a microscope. utilize all host resources; and (iii) if the parasitoid density is increased, two or more wasps can share a single host (quasi–social- 2.5. Data analysis and statistics ity, Tang et al., 2014a), and this directly induces higher a parasitism rate and enhanced host utilization. All observations were recorded using Windows Excel 2003. We The objective of our present study was to examine the effect of used one–way analysis of variance (ANOVA) to assess the differ- the number of female founders on the timing of parasitism and on ences among means in adult performance (time to first attack, S. Gao et al. / Biological Control 97 (2016) 57–62 59 paralysis period, pre–oviposition time, and oviposition periods), offspring performance (egg stage, larval stage, and pupal stage) and time to complete development of S. pupariae. Furthermore, we performed the Kruskal–Wallis test to compare differences among treatments in time to first attack, paralysis period, pre–oviposition time, and oviposition periods of foundresses, larval stage of offspring and time to complete development. We conducted regression analyses were used to assess the various relationships among time to first attack, paralysis time, pre– oviposition period, oviposition period and foundresses density.

3. Results

3.1. Experimental observations

During the initial phase after introduction into the vial, some female wasps immediately started stinging the host, whereas Fig. 1. Relationship between foundress number and the time to first attack. Effect of foundress number is for time to first attack (y = 71.825x2 À 824.01x + 2309.4, others moved over the cotton plug to escape. During the paralysis 2 R = 0.4861, ANOVA: F2,93 = 43.988, P < 0.001). phase, females stabbed at the end of host’s abdomen with their aci- cular ovipositor, and secreted toxins to paralyze the host larva. We deemed the host paralyzed when it stopped struggling and the 3.4. Relationship between parasitoid density and pre–oviposition head capsules remained motionless when probed with a pincette. period During the pre–oviposition phase, female wasps started to clean the paralyzed host and absorb hemolymph outflow via biting into The pre–oviposition period of S. pupariae decreased as the the epidermis near the palate. This extra nutrition led to gradual maternal parasitoid density increased, according to a significant expansion of the abdomen in some maternal wasps. During the quadratic term (F2,93 = 18.603, P < 0.001; Fig. 3). The pre–oviposi- egg–laying phase, wasps gave priority to laying eggs on the tion period was significantly longer when one foundress per host inter–segmental membranes of the host, and continued laying eggs was introduced than when two or more female wasps per host until the entire host was covered with eggs. During the maternal were introduced (n = 96, H = 23.496, P = 0.001). care phase, the mothers visited each egg and patted them with their antennaes gently and continuously. When eggs fell off the 3.5. Relationship between parasitoid density and oviposition period host surface, the mothers clasped these eggs with their mandibles and replaced them. Furthermore, mothers also touched their off- The oviposition period of S. pupariae decreased significantly as spring with their mouthparts and patted them continuously with the parasitoid density increased from one female wasp per host their antennae throughout the larval stage. If larvae overlapped, to three female wasps per host (n = 36, H = 27.387, P < 0.001); how- mothers clasped these larvae with their mandibles and dispersed ever, when the parasitoid density was increased to more than three them. Mothers also moved dead or melanotic larvae far from the female wasps per host, the oviposition period did not differ signif- host. During the pupal stage, mothers still visited the cocoons icantly among treatments (n = 60, H = 6.766, P = 0.149). The dura- and patted them continuously; furthermore, they bit a hole in tion of the time to reach egg It took females significantly longer the cocoon before progeny emergence. to reach the egg–laying was significantly longer when one female wasp per host was introduced (mean 5.71 days) than when two 3.2. Relationship between parasitoid density and the time to first or more female wasps per host were introduced (n = 96, attack H = 65.275, P < 0.001). While female wasps laid eggs between day five and day six when one female wasp per host was introduced, The time to first attack of S. pupariae differed significantly among treatments (n = 96, H = 35.147, P < 0.001; Fig. 1). At the low- est parasitoid density (one female wasp per host), the time to first attack was approximately 1913 minutes, however, as the para- sitoid density increased, the time to first attack decreased (two female wasps per host, 533 min; three female wasps per host, 376 min). when the parasitoid density was increased to more than three female wasps per host, the time to first attack (200 min) did not differ significantly among treatments (n = 60, H = 1.52, P = 0.823).

3.3. Relationship between parasitoid density and host paralysis time

The results of our regression analyses revealed that the paraly- sis time decreased significantly as the parasitoid density increased (n = 96, H = 59.405, P < 0.001). This relationship was best fitted by a quadratic term (y = 25.089x2 À 337.49x + 1331.2, R2 = 0.5996, ANOVA: F = 69.639, P < 0.001; Fig. 2). Typically, a host could 2,93 Fig. 2. Relationship between foundress number and paralysis time. Effect of be paralyzed within 24 h, even in the lowest parasitoid density foundress number is for paralysis time (y = 25.089x2 À 337.49x + 1331.2, 2 treatments. R = 0.5996, ANOVA: F2,93 = 69.639, P < 0.001). 60 S. Gao et al. / Biological Control 97 (2016) 57–62

(male: n = 60, H = 7.947, P = 0.094; female: n = 60, H = 2.984, P = 0.56).

4. Discussion

Previous studies of parasitoid–host systems have mainly focused on the one–parasitoid–one–host, one–parasitoid–several hosts, and several parasitoids–several hosts models (Abrams and Kawecki, 1999; Fortuna et al., 2012; Harvey et al., 2015; Jiang et al., 2008). With the exception of mass–rearing studies of para- sitic natural enemy insects under limited and closed laboratory conditions, data regarding several parasitoids–one–host models are lacking. However, in a recent mass–rearing laboratory study of Sclerodermus parasitoids, several female wasps were inoculated onto a single larger body–size substitute host to improve the rates Fig. 3. Relationship between foundress number and pre-oviposition period. Effect of successful parasitism and enhance host nutrition. In this system, À of foundress number is for pre-oviposition period (y = 0.0325x2 0.4169x limited space, high encounter rates, and quantitative resource + 5.7507, R2 = 0.2857, ANOVA: F = 18.603, P < 0.001). 2,93 caused a parasitoid or parasitoids to semi–coercively parasitize a single host. but after only two days when eight female wasps per host were In previous studies, the performance of adult parasitoids was introduced (F2,93 = 164.8, P < 0.001) (Fig. 4). assessed using fecundity, progeny, and individual body size of off- spring (Giang and Takatoshi, 2007; Harvey et al., 2015). In the pre- 3.6. Relationship between parasitoid density and developmental sent study, we measured the parasitic rate by evaluating the time duration of parasitoid offspring that female parasitoids spent in each phase, including the time to first attack, paralysis time, pre–oviposition and oviposition period. We determined significant differences in the larval stage We found that when two or three female parasitoids were simulta- (n = 96, H = 33.914, P < 0.001), but not in the egg stage (n = 96, neously introduced to a single host, the time to first attack, paral- H = 6.038, P = 0.535) or the pupal stage (male: n = 96, H = 6.14, ysis time, pre–oviposition, and oviposition period were shorter P = 0.523; female: n = 96, H = 5.504, P = 0.599) among treatments than when parasitoids were introduced individually. Liu et al. (Table 1). The developmental durations of male and female off- (2011) reported the existence of trade–offs before host–parasitoid spring were significantly longer when fewer maternal wasps were interactions, according to host size–related quality. Under closed introduced (male: n = 96, H = 58.761, P < 0.001; female: n = 96, conditions times to first attack were decreased, probably because H = 57.932, P < 0.001). of (i) higher encounter rates with the host; (ii) greater use of pher- omone (possibly an aggregation pheromone) necessary for mark- 3.7. Relationship between parasitoid density and time to complete ing a relatively larger host aggregate (Nufio and Papaj, 2001; development of one generation Vinson, 1985). Parasitoids could paralyze their host, but this required a greater time commitment, thereby decreasing the adult The time to complete development of one generation was wasp’s fitness. The presence of multiple parasitoids on a single host approximately one month and differed significantly between treat- resulted in more frequent parasitoid stinging and venom secretion, ments (male: n = 96, H = 58.761, P < 0.001; female: n = 96, thereby accelerating host paralysis and increasing nutritional H = 57.932, P < 0.001). The time to complete development of one replenishment. generation was significantly longer when one female wasp per Generally, intraspecific competition occurs as an aggregated host was introduced than when two or more female wasps per host response of many parasitoids to a single host because of limited were introduced, but did not differ significantly among treatments food resources, habitat, breeding sites, or other factors, i.e., when more than three female wasps per host were introduced intraspecific competition for oviposition sites (Nakamura, 1968; Zimmerman, 1982). However, when breeding quasi–social Sclero- dermus, an increase in the parasitoid–host ratio would facilitate intraspecific cooperation but not competition by making larger hosts available to parasitoids (Tang et al., 2014a). In our present study, we found that the duration of the time to reach egg laying was significantly longer when one or two parasitoids were exposed to a single host than when three parasitoids were exposed to a sin- gle host. Thus, intraspecific cooperation among S. pupariae individ- uals was reflected mainly in faster oviposition rates and enhanced host utilization. However, when the parasitoid density was increased to more than three female wasps per host, we deter- mined no significant difference among treatments. Our results indicate the optimal size of the parasitoid population functions in concert with the host, to stabilize the population dynamics (Barclay, 1986) with no detectable mutual interference between parasitoids. The optimal population size may be achieved by (i) having only three mothers in every group of foundresses involved during the period between exposure to the host and oviposition; or Fig. 4. Relationship between foundress number and oviposition period. Effect of foundress number is for oviposition period (y = 0.0806x2 À 1.0742x + 6.5647, (ii) having more than three mothers involved during the period 2 R = 0.7799, ANOVA: F2,93 = 164.8, P < 0.001). between exposure to the host and oviposition with no significant S. Gao et al. / Biological Control 97 (2016) 57–62 61

Table 1 The developmental duration of offspring and time to complete development of S. pupariae inoculated with various foundress numbers. Data in the table refer to mean ± SE. Different letters within a column indicate significant differences among treatments (P < 0.05).

Parasitoid– Egg stage Larval stage Pupal stage of Pupal stage of Developmental Developmental Time to complete Time to complete host ratios male wasps female wasps duration of male duration of female development of male development of wasps wasps wasps female wasps 1:1 2.71 ± 0.26 a 7.38 ± 0.48 a 12.58 ± 0.67 a 13.58 ± 0.47 a 22.67 ± 1.09 a 23.67 ± 0.98 a 35.92 ± 1.49 a 36.92 ± 1.39 a 2:1 2.83 ± 0.33 a 7.21 ± 0.62 a 12.33 ± 0.65 a 13.33 ± 0.78 a 22.38 ± 0.98 ab 23.38 ± 1.02 ab 32.92 ± 1.99 b 33.92 ± 2.12 b 3:1 2.88 ± 0.23 a 6.54 ± 0.50 b 12.33 ± 0.65 a 13.42 ± 0.51 a 21.75 ± 0.81 bc 22.83 ± 0.78 bc 30.77 ± 1.01 c 31.85 ± 1.08 c 4:1 2.58 ± 0.47 a 6.38 ± 0.48 b 12.58 ± 0.79 a 13.33 ± 0.65 a 21.54 ± 0.86 bc 22.29 ± 0.72 c 29.92 ± 1.11 cd 30.67 ± 1.02 cd 5:1 2.63 ± 0.43 a 6.50 ± 0.37 b 12.42 ± 0.79 a 13.08 ± 0.67 a 21.54 ± 0.72 bc 22.21 ± 0.84 c 29.88 ± 0.94 cd 30.55 ± 1.23 cd 6:1 2.67 ± 0.44 a 6.46 ± 0.45 b 12.25 ± 0.97 a 13.17 ± 0.58 a 21.38 ± 1.30 c 22.29 ± 0.69 c 29.31 ± 1.70 cd 30.22 ± 0.98 cd 7:1 2.54 ± 0.50 a 6.29 ± 0.26 b 12.25 ± 0.45 a 13.38 ± 0.64 a 21.08 ± 0.70 c 22.21 ± 0.58 c 28.77 ± 1.18 d 29.89 ± 1.26 cd 8:1 2.71 ± 0.45 a 6.50 ± 0.48 b 12.08 ± 0.79 a 13.32 ± 0.61 a 21.29 ± 0.94 c 22.53 ± 0.65 c 28.97 ± 1.34 d 30.21 ± 1.00 d

effect on the performances of the group of foundresses. We pro- regarding the larval stage may be related to the maternal care pose that the second scenario is more likely, because we observed provided by foundresses (Xu and Yan, 1985). In our present study, that every mother supplied nourishment via clearly extended we observed that when larvae fell off an infested host, mothers abdomens. clasped these eggs with their mandibles and replaced them; In previous studies, the optimal parasitoid population size var- furthermore, mothers did not leave or die until their offspring ied according to species, body–size, and host quality. For example, began to spin their cocoons. A greater level of maternal care the optimal population size in mass–reared S. guani was not provided by higher number of multiparous mothers improved observed until the parasitoid–host ratios were exceeded 3:1 the development and eclosion synchronicity of their offspring (Monochamus alternatus; Wu et al., 2008b), 4:3 (S. populnea; Zhou and enabled these offspring to mate adequately within a short time et al., 2006), 1:5 (Ptilineurus marmoratus; Chen et al., 1995), or period. In conclusion, the social behaviors of Sclerodermus pupariae 2:1 (Tenebrio molitor; Dai et al., 2005). In our present study, the regarding collaboratively subduing a host and mutually fostering optimal parasitoid population size was related to the host larval offspring were beneficial in utilizing larger hosts. Our present size—three parasitoids on a single T. gebleri larval, weighing results support the recent finding that quasi–social parasitoids between 200.0 mg and 240.0 mg was found to be most efficient. act in a mutually beneficial manner when attacking large hosts There is considerable evidence to suggest that the optimal para- (Tang et al., 2014a). sitoid population size prevents excessive egg laying or breeding When parasitic natural enemies are released to control target (Wylie, 1971). When introduced to a single host, parasitoids pests in the field, parasitoid effectiveness is influenced by many secrete physical or chemical markings to prevent super–parasitism variables, such as climatic factors, food quality and quantity, inter- or multi–parasitism, and reduce intraspecific competition (Nufio specific competition, spatial distribution, and habitats. For exam- and Papaj, 2001; Wylie, 1971). Most parasitoids use host–marking ple, Curculionidae and Scolytidae larvae and pupae are frequently pheromones to determine the optimal egg–laying rate and quan- infested by S. pupariae. Therefore, optimal parasitoid–host ratios tity of progeny produced for each host. For example, in the para- are not only important for inferring the population dynamic phe- sitoid wasp, Telenomus fariai, larger numbers of progeny require nomena of pests and natural enemies, but may also play a crucial more time for egg laying; therefore, later females arriving on the role in facilitating the development of economically viable pest host determine the host’s fitness before embarking on their repro- control strategies (Pu, 1983). Our present results suggest that ductive investment (Bosque and Rabinnovich, 1979). Additionally, intraspecific cooperation enhances the parasitic efficacy of wasps resistance pheromone is also secreted to prevent the same insects sharing a single host. Our findings highlight the importance of a from excessively laying eggs (Ikemoto, 1972; Kozlowski et al., suitable parasitoid–host ratio in promoting mutually beneficial 1983; Messina and Renwick, 1985) and thus prevent dispropor- behaviors that enhance adult performance. tionate intraspecific competition among offspring. Chemicals with communication functions can help insects avoid excessive compe- Acknowledgments tition, accommodate population density, and improve progeny fit- ness (Klomp, 1964). We propose that the optimal parasitoid This research was supported by the State Key Program of population size is essential for interspecific mutual coordination, National Natural Science of China (Grant No. 31230015) and the distributing time and space for eggs at the individual level, and National Natural Science Foundation of China (Grant No. achieving ‘‘ideal free distribution” (Tregenza et al., 1996) under 31370654). conditions of limited host resources. 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