Comparing Immature Development and Life History Traits in Two
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1 Journal of Integrative Agriculture Advance Online Publication 2014 Doi: /S (14) Comparing Immature Development and Life History Traits in Two Coexisting Host-feeding Parasitoids, Diglyphus isaea and Neochrysocharis formosa (Hymenoptera: Eulophidae) 1 ZHANG Yi-bo*, LU Shu-long*, LIU Wan-xue, WANG Wen-xia, WANG Wei and WAN Fang-hao State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing , P.R. China Abstract Coexisting natural enemies that share a common host resource in the same guild usually exhibit variation in their life history traits, due to their need to share a similar ecological niche while reducing competition. In this study, we compared the immature development times and adult life history traits of two coexisting, host-feeding parasitoids, Diglyphus isaea Walker and Neochrysocharis formosa Westwood (Hymenoptera: Eulophidae), which both attack larvae of the same agromyzid leafminers. These two species are both synovigenic, idiobiont parasitoids, whose adults consume host fluids ( host feeding ) and lay anhydropic eggs. Of the two, D. isaea has a larger body but little or no initial egg load, and engages in similar lifetime host-feeding events. However, it achieves higher fecundity, longer adult longevity, and higher host suppression ability than N. formosa, which has a smaller body and higher initial egg load. D. isaea although engages in similar lifetime host-feeding events with N. formosa, all of its gains in life history traits per host-feeding event of D. isaea were larger than those of N. formosa. The age-specific fecundity and host mortality curves of N. formosa were more skewed in early life than those of D. isaea. In addition, the ovigeny index of N. formosa was negatively correlated to body size. Our results confirmed that two coexisting parasitoids, which share the same host resource, show different immature development patterns and life history traits, suggesting that different resource allocation may be a common model that promotes the coexistence of species within a guild. Key words: Parasitoid, host feeding, initial egg load, ovigeny index, fecundity, longevity INTRODUCTION How to explain the coexistence of species that exploit a common resource is one of the major issues in ecology (Chesson 2000; Le Lann et al. 2012). Generally speaking, species sharing the same resources should exhibit niche partitioning to reduce the effects of resource competition, such as by resource specialization (Tilman 1982) or through shifting the temporal and/or spatial pattern of resource exploitation Zhang Yi-bo, Tel: , zhangyibo20 11@gmail.com, lushulongyuan@hotmail.com. Correspondence LIU Wan-xue, Tel: , liuwanxue@263.net * These authors contributed equally to this study.
2 (Chesson 2000; Chase and Leibold 2003). In a resource niche, different life history trade-offs result from the abundance and distribution of resources, as for example between early and later reproduction and between reproduction and survival (Ellers and van Alphen 1997; Harvey 2008; Harvey et al. 2009; Le Lann et al. 2012). Coexisting species could therefore differ substantially in their age-specific life history trait curves (host feeding, fecundity, and host mortality) and the associated allocation of capital and income nutrients to reproduction and survival, depending on their resource niche (Boggs 1997; Ellers and Jervis 2003). Parasitic hymenoptera are excellent model organisms to study questions about exploitation of shared resources (Godfray 1994). Parasitoids lay their eggs in, on, or near the bodies of their hosts (usually other insects), and developing parasitoid larvae feed exclusively on host tissues until they emerge as adults. Based on the temporal pattern of egg development before and after adult emergence, parasitoid species can be classified into proovigenic (species that emerge as adults with a set of mature eggs, providing them with a fixed and limited egg supply) and synovigenic (species able to produce eggs continuously throughout their adult life) (Jervis et al. 2001, 2008). Parasitoid life-history evolution should in theory optimize and integrate three processes: (a) resource utilization by the parasitoid larva, (b) allocation of some larval resources to the adult, and (c) adult acquisition of additional nutrients (Einum and Fleming 2000; Jervis et al. 2008). Allocation of larval-acquired resources to the adult stage varies among parasitoid species and strongly affects initial egg load, which is derived from finite larval resources (Heimpel et al. 1997). On the other hand, synovigenic parasitoids must find and consume additional nutrients for egg maturation and body maintenance (Jervis et al. 2008). Additional resources are derived from non-host sources (e.g., nectar, hemipteran honeydew, pollen, leaf exudates, etc.) and host resources (host hemolymph or tissues) (Jervis and Kidd 1986; Jervis et al. 1993; Heimpel and Collier 1996; Bernstein and Jervis 2007; Lee and Heimpel 2008). The nutrients obtained by female parasitoids can be stored or used for somatic maintenance, locomotion or ovigenesis (Olson and Andow 1998; Rivero and Casas 1999a, b; Zhang et al. 2011), thus contributing to the lifetime fitness of the parasitoid. Although they are well studied in individual parasitoid species (Kraaijeveld and Godfray 1997), among species that do not share the same host (Jervis et al. 2001; Jervis and Ferns 2004), among those species sharing the same host but belonging to different climatic regions (Moiroux et al. 2010) or under the influence of a third competitor (Vayssade et al. 2012), trade-offs in life history traits, such as fecundity and longevity are less well explored in parasitoid complexes associated with the same host species and stage in the same habitat (Harvey 2008; Harvey et al. 2009; Le Lann et al. 2012). Therefore, comparing and contrasting the immature and life history traits of two coexisting species would improve our understanding of the interactions between coexisting species. 2
3 Diglyphus isaea Walker (Hymenoptera: Eulophidae) and Neochrysocharis formosa Westwood (Hymenoptera: Eulophidae) are two of the most common synovigenic idiobiont parasitoids of agromyzid leafminer species, parasitizing host larvae and feeding on host hemolymph (Minkenberg 1989; Saito et al. 1996; Song et al. 2005; Burgio et al. 2007; Zhang et al. 2011). Diglyphus isaea is a biparental, arrhenotokous ectoparasitoid, and a non-concurrent and destructive host feeder (Kaspi and Parrella 2005; Zhang et al. 2010a, b), while N. formosa is an arrhenotokous and/or thelytokous endoparasitoid (Saito et al. 1996; Saito 2004; Hagimori et al. 2006, 2008). Both parasitoids coexist in Yunnan Province, southwest China (Liu et al. 2013). We hypothesized that these two coexisting parasitoids sharing the same host resource would display differences in their immature development and life history traits. Our specific goals were (a) to explore the links between egg load (initial egg load and potential egg load) and life history traits, female body size and pupal developmental period; (b) to compare and contrast the divergences of life history traits (such as the number of host feeding events, longevity, fecundity, and host mortality) of the two species and the differences in the age-specific curves of each life history trait; and (c) to analyze the gains of these traits per host feeding event between these two parasitoids. RESULTS Developmental traits of immature parasitoids In comparing the duration of the larval, pupal, and total immature stages of the two parasitoids, two-way ANOVA showed significant effects of species and sex, but no interaction between species and sex in the larval stage (F 1, 101 =79.16, P< for species; F 1, 101 =4.98, P=0.028 for sex; F 1, 101 =0.79, P= for interaction; Table 1), the pupal stage (F 1, 101 =621.03, P< for species; F 1,101 =6.00, P= for sex; F 1, 101 =0.01, P= for interaction; Table 1) or the total immature stage (F 1, 101 =661.50, P < for species; F 1,101 =11.51, P= for sex; F 1,101 =0.42, P=0.516 for interaction; Table 1). The developmental durations of all stages (larval, pupal, and total immature stage) of D. isaea were significantly shorter than those of N. formosa (Tukey-Kramer tests: two parasitoid species comparison, P<0.05, Table 1). Meanwhile, the developmental durations of all stages (larval, pupal, and total immature stage) of females were significantly longer than those of males (Tukey-Kramer tests: all intraspecific comparisons were statistically significant, Table 1). Initial egg load of D. isaea (0.2±0.1 SE, n=30, range 0 to 1) was significantly lower than that of N. formosa (7.7±0.4 SE, n=29, range 4 to 12), while body size and egg volume of D. isaea (body size: 0.42 mm; egg volume: mm 3 ) were significantly larger than for N. formosa (body size: 0.27 mm; egg volume: mm 3 ) (t=14.699, df=40, P< for body size; t=-3.211, df=55, P= for egg volume). No significant correlation was detected between body size and initial egg load in D. isaea (F 1, 28 =2.61, 3
4 r 2 =0.0882, P=0.1176, Fig. 1a), while the significant linear regressions of body size with initial egg load (hind tibia length: slope=14.81, intercept=-32.61, r 2 =0.58, F 1, 28 =37.61, P<0.0001, Fig.1b) and with pupal development time (slope=0.12, intercept=-11.84, r 2 =0.44, F 1, 28 =21.10, P<0.0001, Fig. 2) were found in N. formosa. The potential lifetime egg production (lifetime fecundity added to the remaining egg load) of both parasitoids in the host-feeding treatment showed a strong linear relationship with adult body size (D. isaea: slope=26.54, intercept=-46.30, r 2 =0.67, F 1, 22 =42.27, P<0.0001; N. formosa: slope=79.36, intercept= , r 2 =0.51, F 1, 20 = 19.63, P=0.0003, Fig. 1). Based on the above results, we further calculated the Ovigeny Index (OI) values for each parasitoid as for D. isaea and 0.12 for N. formosa. As D. isaea has almost no eggs at emergence, the negative relationship between body size and OI was only found in N. formosa. Life history traits of the two host feeding parasitoids Host feeding significantly increased all the life history traits of the two parasitoids compared to having access to water only. This was true for fecundity (D. isaea: χ 2 = , df=1, P<0.0001; N. formosa: χ 2 = , df=1, P<0.0001), mortality (D. isaea: χ 2 = , df=1, P<0.0001; N. formosa: χ 2 = , df=1, P<0.0001), and longevity (D. isaea: χ 2 = , df=1, P<0.0001; N. formosa: χ 2 = , df=1, P <0.0001). In the starvation treatment, the longevity of D. isaea was significantly shorter than that of N. formosa (χ 2 = , df=1, P=0.0005). Similarly, the fecundity (χ 2 = , df=1, P<0.0001), and mortality (χ 2 = , df=1, P<0.0001) of D. isaea in the starvation treatment were both significant lower than those of N. formosa (Table 2, Fig. 3). The host feeding of two parasitoids in the host food treatment had no significant difference (χ 2 =3.3621, df=1, P=0.0667), but the fecundity (χ 2 = , df=1, P< ), mortality (χ 2 = , df=1, P<0.0001) and longevity (χ 2 = , df=1, P<0.0001) of D. isaea in the host food treatment were all significant larger or longer than those of N. formosa in the same treatment (Table 2, Fig. 3). The age-specific curves of host feeding, fecundity and mortality The age-specific curves of host-feeding events for the two parasitoid species differed substantially (Species: F 1, 20 =0.92, P=0.3479; Age: F 19, 655 =3.94, P<0.0001; Species Age: F 19, 655 =1.95, P=0.0093; Fig. 4a). The daily number of host-feeding events by N. formosa gradually increased over the first 3-4 days, remained fairly constant for the following 3 weeks, and then declined. Similarly, the number of daily host-feeding events by D. isaea increased over the first 3-4 days and remained constant for nearly 2 weeks, then declined and kept stable again, amounting to a significantly longer host feeding period. 4
5 The age-specific curves of fecundity for the two parasitoid species also differed substantially, resulting in a significant interaction between species and age (Species: F 1, 20 =16.27, P=0.0007; Age: F 19, 635 =4.20, P<0.0001; Species Age: F 19, 635 =2.75, P<0.0001; Fig. 4b). The age-specific fecundity curve of N. formosa in the first three days ranged from 4 to 6 eggs, whereas the curve of D. isaea ranged from 0 to 2 eggs during this period. After three days, the daily fecundity of N. formosa fluctuated considerably, peaked at 8.1 eggs on day 10, and then declined over the following two weeks. For D. isaea, daily fecundity increased sharply during the first 5 days, peaked on day 5 (7.6 eggs), and then decreased slowly over a long period, indicating that N. formosa had no preoviposition period, while D. isaea had a one day preoviposition period. The age-specific curves of host mortality between the two species were quite different as well (Species: F 1, 20 =29.84, P<0.0001; Age: F 19, 648 =5.76, P<0.0001; Species Age: F 19, 648 =2.48, P=0.0005; Fig. 4c). The dynamical trends of mortality were similar to those of fecundity. The gains of fecundity, mortality and longevity per host-feeding event The gains per host feeding varied between the two parasitoids. The daily host-feeding events of N. formosa were almost the same with D. isaea (F 1, 43 =1.19, P =0.2820, Table 3, Figure 4a), while the gains in other traits per host feeding by D. isaea were over 2-fold greater than for N. formosa (fecundity: F 1, 43 =18.98, P<0.0001; mortality: F 1, 43 =54.77, P<0.0001; longevity: F 1, 43 =11.57, P=0.0015, Table 3). While D. isaea fed on only 2.60±0.30 (SE) hosts (range ) per day, a single host-feeding increased fecundity by 2.57±0.23 eggs (range ), resulted in 6.24±0.42 (range ) additional host mortality, and prolonged adult parasitoid life by 0.44±0.06 days (range ). By contrast, N. formosa consumed 2.96±0.10 (SE) hosts per day (range ), but a single host-feeding resulted in an increase of only 1.39±0.11 eggs (range ), 2.64±0.11 (range ) additional host mortality, and 0.21±0.01 additional days (range ) of longevity. DISCUSSION Both species in this study are synovigenic and idiobiont parasitoids sharing the same host, whose adults consume host fluids ( host feeding ) and lay anhydropic eggs. Of the two, D. isaea emerged with a larger body size and fewer initial eggs, and engaged in fewer host-feeding events during its adult life. Even so, it achieved bigger egg volume, higher fecundity, longer adult longevity, and higher host suppression ability than N. formosa, which had a smaller body size but greater initial egg load (Table 4). Even though the lifetime numbers of host-feeding events of two wasps were similar, all gains of D. isaea from these host-feeding events were larger than those of N. formosa. In addition, the age-specific fecundity curve of D. isaea rose slowly and peaked late in life, while that of N. formosa increased early and sharply (Table 4). The two parasitoids made different trade-offs of resource utilization during their immature stage. D. 5
6 isaea invested more resources in building a larger body and bigger egg volume but lower initial egg load, compared with N. formosa. Harvey and Strand (2002) suggested that the development times of parasitoids can vary with host feeding ecology, but this would not explain our results as both parasitoids used the same host resource in this study. However, two possibilities could improve our understanding of these results. First, the immature parasitoids may have experienced different micro-climate conditions, as D. isaea is an ectoparasitoid, whose eggs are laid on the host body, while N. formosa is an endoparasitoid, whose eggs are laid directly in the host body and bathed by host hemolymph. Different environmental conditions, especially temperature, would then result in different developmental rates (Gillooly et al. 2001, 2002; Le Lann et al. 2011). Meanwhile, our results are consistent with previous studies (Mayhew and Blackburn 1999; Jervis and Ferns 2011), which found that ectoparasitoid could evolve to enhance the pre-adult developmental rate to escape the risk of juvenile mortality stemming from extrinsic biotic factors. Second, our findings may be influenced by the different initial egg loads, as the initial egg load of N. formosa was larger than that of D. isaea. Many previous studies have shown that ovarian development and oogenesis of Hymenoptera parasitoids commenced at the pupal stage (Volkoff and Daumal 1994; Boggs 1997; Harvey and Strand 2002), meaning that initial egg load could therefore affect pupal development time. In this study, host feeding by the two parasitoids not only enhanced fecundity, but also increased adult longevity. Similar results had been found in other host-feeding parasitoids elsewhere, such as Aphytis melinus (Debach) (Collier 1995) and Eupelmus vuilletti (Crawford) (Giron et al. 2004). Both Giron et al. (2004) and Casas et al. (2005) found that host feeding increased both egg production and longevity in E. vuilletti. Kapranas and Luck (2008) likewise suggested that host feeding increased the longevity and fecundity of two strictly synovigenic parasitoids, Metaphycus flavus Howard and Metaphcus luteolus Timberlake, although nutrients obtained from host feeding were differently allocated to reproduction versus somatic maintenance. However, Heimpel et al. (1994) found that host feeding by parasitoid Aphytis lingnananesis Compere did not substantially increase its longevity but did promote egg production, while host feeding had no significant effect on either the fecundity or longevity of Aphytis melinus (Heimpel et al. 1997). Likewise, Harvey (2008) found that host feeding by Gelis agilis Fabricius, a host-feeding hyperparasitoid on Cotesia glomerata L., did not have a maintenance function and did not significantly increase fecundity and longevity. Havery et al. (2012) further confirmed that G. agilis females feeding on both hosts and supplementary sugars achieved optimal egg production and fecundity. These cases illustrate that host feeding contributed to lifetime fitness of the parasitoid, but the extent to which this behavior affects life history traits varies significantly among species. As the effects of host feeding on life history traits varied among parasitoid species, it was necessary to evaluate the gains of host feeding events. In this study, N. formosa had similar lifetime host-feeding events as D. isaea, but the gains per host feeding by N. formosa were substantially lower. D. isaea had much higher efficiency acquiring and utilizing host nutrients than N. formosa. These results are congruent with some previous study results. A single host-feeding meal of A. melinus females produced an increase of 6
7 nearly four eggs and increased lifespan by 0.61 days (Heimpel et al. 1997). Giron et al. (2004) found that E. vuilletti females achieved a net gain of 1.53 eggs per host-feeding event and that each host-feeding increased adult longevity by 0.33 days. Wu and Heimpel (2007) found that Aphelinus albipodus (Hayat and Fatima) females could mature an additional 1.8 eggs for each host-feeding meal. These differences in gains per host-feeding event might simply be due to the different parasitoid or host species. The two parasitoids in this study shared the same host (L. sativae larvae), so the total nutrients of a host would be similar and the effects originating from host could be excluded. However, two possible differences between the parasitoids could be responsible for the differences in the gains resulted from each host-feeding event. First, host-feeding by D. isaea can be classified as non-concurrent and destructive (Zhang et al. 2010b), as D. isaea would either feed on a given host s haemolymph or parasitize a perfect, untouched host. On the other hand, N. formosa could be either non-concurrent and destructive or on occasion concurrent (in which parasitoids can use the same host for feeding and oviposition at one time) and destructive, as 24% of hosts that were fed on by N. formosa (56 of 233) were also parasitized (personal observation, unpublished). Second, D. isaea have much bigger body size than N. formosa, meaning they have a larger abdomen potentially capable of storing more nutrients from a single host-feeding event than N. formosa. If that is so, the amount of nutrients acquired per host-feeding by D. isaea would be larger than for N. formosa. While a positive relationship between body size and initial egg load and potential egg load was found in N. formosa, within species the ovigeny index was negatively correlated with body size. With a large body size, the total amount of available resources increases, but the increase in allocation to initial egg load (the numerator in the ovigeny index) is proportionately smaller than the increase in allocation to initial reserves (which contribute later to lifetime potential fecundity, the denominator in the index), resulting in a decrease in the ovigeny index (Ellers and Jervis 2003). This decrease was similar to those of Aphaereta genevensis Fischer (Thorne et al. 2006) and Ibalia leucospoides (Fischbein et al. 2013), and could be predicted by adaptive models (West et al. 1999). The age-specific fecundity curve in N. formosa exhibited a peak early in life and then declined, whereas the fecundity curve of D. isaea was more dampened. Similarly, N. formosa females had a higher rate of egg production early in life, but produced significantly smaller eggs and a lower total mean realized fecundity than D. isaea. We found that D. isaea had a higher reproductive effort throughout life than N. formosa. According to predictions by life history theory, higher reproductive effort usually results in a longevity cost (Ellers 1996; Ellers and van Alphen 1997; Rivero and West 2002). Obviously, our results do not fully match this theory. Possibly, different allocations of capital nutrients (or larval resources) resulted in the different initial egg loads (8 for N. formosa but just for D. isaea). This high initial load meant that N. formosa had no preoviposition period and could lay eggs immediately after emergence, while D. isaea could not. In addition, the different abilities of the parasitoids in nutrient acquiring could explain the divergence of our results from this life history theory. Even though the two parasitoids had a similar number of host-feeding events, D. isaea achieved bigger gains per host-feeding event than N. formosa. We 7
8 concluded that the allocation and acquisition of capital and incoming nutrients to reproduction influences the shape of a species age-specific fecundity curve in parasitoids (Boggs 1997; Ellers and Jervis 2003; Jervis et al. 2008; Harvey 2008). In conclusion, two coexisting parasitoids sharing the same host resource showed quite different immature development and life history traits. Our results suggested that these different life history traits enable them to coexist and exploit the same host resource with different models of resource utilization. It may be a common model that promotes the coexistence of species within a guild (e.g., Harvey et al. 2009; Le Lann et al. 2012). Meanwhile, our results could shade a light to the implications of biological control using these two parasitoids. N. formosa adapt to be inundative release, as it has a high rate of egg production in early life with no preoviposition period and can lay eggs to suppress the pest population immediately after emergence. On the other hand, D. isaea can be seasonal inoculative release, of which control on pest population is obtained over many pest generations and can have a long term impact if crops are grown for a season-long period. It thus would provide insight into new IPM strategies against leafminer pests using two parasitoids in greenhouses and fields in China. MATERIAL AND METHODS Insect cultures Cultures of D. isaea, N. formosa, and Liriomyza sativae Blanchard were obtained from insects reared at the Department of Biological Invasions (DBI), Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China. Hosts and parasitoids were originally collected from agricultural fields in the vicinity of Chenggong County ( E, 24.9 N, at an elevation of 6 m a.s.l.), Kunming City, Yunnan Province, and were then maintained in the laboratory at 27±1 o C, 70±5% RH, and a 14:10 h L:D photoperiod. L. sativae larvae used in all experiments were maintained on kidney bean (Phaseolus vulgaris L.) in gauze cages ( cm 3 ) at DBI. Similarly, all D. isaea and N. formosa were reared using kidney bean leaves colonized by L. sativae larvae in gauze cages ( cm 3 ) at DBI. In order to obtain freshly emerged, mated parasitoids, pupae were isolated from bean leaves, placed individually in 1.5 ml microcentrifuge tubes and checked every two hours for adult emergence. When a female parasitoid emerged, a male (less than 2 days old) that was previously provided with a 10% honey ( w / v ) solution was introduced with an aspirator. Parasitoids handled in this manner mated quickly after introduction of the male. 8
9 Developmental traits of the immature parasitoids To obtain data on larval and pupal development, bean leaves infested with 2nd-3rd instar L. sativae larvae (ca 15-20/leaf) were detached from the plants and the end of petioles were wrapped by cotton soaked with distilled water for keeping fresh. Each leaf was placed in glass Petri dishes (9 cm dia, 1.5 cm height) with a water-soaked filter paper underneath each leaf. Total ten dishes were prepared, of which five were supplied for D. isaea, the rest was for N. formosa. Two mated parasitoids (2-3d age) were added into each Petri dish for laying egg. After two hours, parasitoids were removed. Petri dishes with infested leaves were then checked daily until parasitoids emerged. Parasitoid development was monitored daily and the time to pupation recorded by transparency, as larvae are clear but pupae are black. The stage and size of eggs of both wasps were too short and small to be clearly identified, so we combined egg and larval stages together as the egg-larval stage (hereafter termed larval stage ) during this experiment. When parasitoids emerged, 30 females and 30 males were frozen at -20 o C, and we later measured the length their hind tibia as an indicator of total body size (Cohen et al. 2005). Ovaries were then dissected and the number of mature eggs (initial egg load) was determined for each individual. Length (L) and width (W) of 30 randomly chosen mature eggs from each female were measured with a micrometer, and the volume (V) of each egg was estimated by the equation V= (π L W W)/6 [taken as an ellipsoid, Giron and Casas (2003).]. Initial egg load and egg volume were measured on the same parasitoid individual. Life history traits of the two host feeding parasitoids Newly emerged and mated parasitoid females were randomly arranged into two types of food treatments: starvation and given hosts for host feeding. In the starvation treatment (n=25 for D. isaea, n=31 for N. formosa, n means sample size), only distilled water was supplied for 24 h, and the host was available only for reproduction for 6 h, but host feeding was forbidden during this period. In the host feeding treatment (n=23 for D. isaea, n=21 for N. formosa), distilled water was daily available for 24 h but the host available for host feeding and reproduction for 6 h. Single parasitoid was first transferred to a glass Petri dish (9 cm diameter, 2.0 cm height), where one bean leaf infected with twenty 2nd-3rd instars of L. sativae was supplied for 6 h (from 12:00 noon to 6:00 p.m.). The leaf petioles were wrapped with cotton soaked with distilled water, and a circular filter paper (9 cm dia) saturated with distilled water was set underneath the bean leaves to keep the leaf moist. In the starvation treatment, the parasitoids were allowed to lay eggs, but host feeding was prevented by gently nudging them off the host with an insect pin as soon as the parasitoids tried to feed on fluids oozing from ovipositor-induced wounds. Observations were terminated when two host-feeding events were observed during the 6 h treatment period. In the host feeding treatment, host-feeding behavior was daily permitted for 6 h, during which the number of host-feeding events was recorded. After 6 h exposure (from 9
10 6:00 p.m to 12:00 noon of the next day), parasitoids were transferred to another plastic Petri dish (5.5 cm diameter, 1.6 cm height), where they had access to distilled water (smeared on the inside of the Petri dishes with a small brush) as appropriate. These plastic Petri dishes were sealed with parafilm and observed daily for parasitoid survival. Each parasitoid was transferred daily to a new glass Petri dish with a fresh leaf and hosts until wasp death. After observation, all the glass Petri dishes were labeled and stored under constant conditions. Fecundity (parasitoid offspring) and host mortality (the total number of host dead) from the leaves bearing exposed hosts were examined under a binocular microscope complemented with transmitted light after two days. The gain of each host-feeding meal for each parasitoid was calculated using the method of Heimpel et al. (1997). Correcting the average fecundity (or mortality and longevity) of the host-feeding parasitoids with that of parasitoids supplied only with distilled water was conducted, and then the gain of each trait per host-feeding meal was equal to the corrected trait divided by the number of host feedings. Dead parasitoids in all treatments were immediately frozen at -20 o C, and the hind tibia length and remaining egg load measured. The longevity of both wasps was measured by counting the number of days between adult eclosion and death. As a control (hosts not exposed to parasitoids), bean leaf discs infested with L. sativae larvae were held in glass Petri dishes as mentioned above. After 6-7 days, the natural mortality of leafminer was record and this mortality was used to calculate the real total number of hosts killed by parasitoids. Statistical analysis Two-way ANOVA was used to detect significant differences in the larval stage, pupal stage, and total immature development time. Parasitoid species (D. isaea and N. formosa) and sex (female and male) were taken as two factors, as all the development times of the two parasitoids met assumptions of normality and homoscedasticity. Tukey multiple comparisons among means of larval stage, pupal stage, and total immature development time were conducted when any of the main factors were significant. A general regression model was used to analyze the regression relationships of body size and pupal development time with initial egg load in N. formosa, and was used to analyze the regression relationships of potential lifetime egg production with hind tibia length in both wasps. The differences in initial egg load, egg size, and body size between the two wasps were compared using two sample T- tests, respectively. We used non-parametric methods (Kruskal-Wallis test) to compare the intraspecific differences in the number of host-feeding events, fecundity, mortality, and adult longevity between the starvation and host-feeding treatment and to compare the interspecific differences of these traits in the same treatment (water or water with host), as fecundity, mortality, and adult longevity of both parasitoids in the water (starvation) treatment did not meet the assumption of normal distribution and equal variances for 10
11 parametric methods, even after transformation. The Weibull distribution was used to describe survivorship curves for females of each parasitoid species when they were fed different treatment diets (access to host feeding or not). The age-specific curves of host feeding, fecundity and mortality between D. isaea and N. formosa were analyzed using Repeated Measures analysis. This analysis tests for differences between the two species independent of time, for time effects, and whether these curves of two species differ over time. To avoid missing most values for differences in date of wasp death, data for only the first 20 days of life were analyzed. Meanwhile, the data were tested for homogeneity of variance and normal distribution, with analysis of variance (ANOVA) complemented by Tukey s Honestly Significant Different (HSD) test used to compare daily differences in host feeding, fecundity gain per host feeding event, mortality gain per host feeding event, and longevity gain per host feeding event. For all tests, a threshold of P<0.05 was used. Analyses were carried out with SAS software version 9.2. Acknowledgements We would like to thank Prof. Gabor Lövei (Aarhus University, Denmark) for critical editing of the original manuscript and Prof. Zhao Zhi-Mo (Southwest University, China) for providing valuable suggestions for data analysis. This work was supported by the National Natural Science Foundation of China ( ), the National Basic Research Program of China (2013CB127605) and the Beijing Municipal Natural Science Foundation ( ). References Bernstein C, Jervis M A. Food-searching in parasitoids: the dilemma of choosing between intermediate or future fitness gains In: Wajnberg E, van Alphen J J M, eds, Behavioural ecology of parasitoids. Blackwell, pp Boggs C L Reproductive allocation from reserves and income in butterfly species with differing adult diets. Ecology, 78, Burgio G, Lanzoni A, Navone P, van Achterberg K, Mastetti A Parasitic hymenoptera fauna on Agromyzidae (Diptera) colonizing weeds in ecological compensation areas in northern Italian agro-ecosystems. Journal of Economic Entomology, 100, Casas J, Pincebourde S, Mandon N, Vannier F, Poujol R, Giron D Lifetime nutrient dynamics reveal simultaneous capital and income breeding in a parasitoid. Ecology, 86, Chase J M, Leibold M A Ecological Niches Linking Classical and Contemporary Approaches. University of Chicago Press, Chicago, USA. Chesson P Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics, 31, Cohen J E, Jonsson T, Müller C B, Godfray H C J, Savage V M Body sizes of hosts and parasitoids in individual 11
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13 Heimpel G E, Rosenheim J A, Kattari D Adult feeding and lifetime reproductive success in the parasitoid Aphytis melinus. Entomologia Experimentalis et Applicata, 83, Jervis M A, Heimpel G E, Ferns P N, Harvey J A, Kidd N A C Life-history strategies in parasitoid wasps: a comparative analysis of ovigeny. Journal of Animal Ecology, 70, Jervis M, Ferns P Towards a general perspective on life-history evolution and diversification in parasitoid wasps. Biological Journal of the Linnean Society, 104, Jervis M, Ferns P The timing of egg maturation in insects: ovigeny index and intial egg load as measures of fitness and of resource allocation. Oikos, 107, Jervis M A, Kidd N A C Host-feeding strategies in hymenopteran parasitoids. Biological Reviews, 61, Jervis M A, Kidd N A C, Fitton M G, Huddleston T, Dawah H A Flower - visiting by Hymenopteran parasitoids. Journal of Nature History, 27, Jervis M A, Ellers J, Harvey J A Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annual Review of Entomology, 53, Kaspi R, Parrella M P Abamectin compatibility with the leafminer parasitoid Diglyphus isaea. Biological Control, 35, Kapranas A, Luck R F Egg maturation, host feeding, and longevity in two Metaphycus species parasitoids of soft scale insects. Biological Control, 47, Kraaijeveld A R, Godfray H C J Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature, 389, Le Lann C, Wardziak T, van Baaren J, van Alphen J J M Thermal plasticity of metabolic rates linked to life-history traits and foraging behavior in a parasitic wasp. Functional Ecology, 25, Le Lann C, Visser B, van Baaren J, van Alphen J J M, Ellers J Comparing resource exploitation and allocation of two closely related aphid parasitoids sharing the same host. Evolutionary Ecology, 26, Lee J C, Heimpel G E Floral resources impact longevity and oviposition rate of a parasitoid in the field. Journal of Animal Ecology, 77, Liu W X, Wang W X, Wang W, Zhang Y B, Wan F H Characteristics and application of Diglyphus parasitoids (Hymenoptera: Eulophidae: Eulophinae) in controlling the agromyzid leafminers. Acta Entomologia Sinica, 56, (in Chinese) Mayhew P J, Blackburn T M Does development mode organize life-history traits in the parasitoid Hymenoptera? Journal of Animal Ecology, 68, Minkenberg O Temperature effect on the life history of the eulophid wasp Diglyphus isaea, an ectoparasitoid of leafminers (Liriomyza spp.) on tomatoes. Annals of Applied Biology, 115, Moiroux J, Le Lann C, Seyahooei M A, Vernon P, Pierre J S, van Baaren J, van Alphen J M Local adaptations of life-history traits of a Drosophila parasitoid, Leptopilina boulardi: does climate drive evolution? Ecological Entomology, 35, Olson D M, Andow D A Larval crowding and adult nutrition effects on longevity and fecundity of female Trichogramma nubilale Ertle & Davis (Hymenoptera: Trichogrammatidae). Environmental Entomology, 27,
14 Rivero A, West S A The physiological costs of being small in a parasitic wasp. Evolutionary Ecology Research, 4, Rivero A, Casas J. 1999a. Rate of nutrient allocation to egg production in a parasitic wasp. Proceedings of the Royal Society of London series B-Biology Sciences, 266, Rivero A, Casas J. 1999b. Incorporating physiology into parasitoid behavioral ecology: the allocation of nutritional resources. Research Population Ecology, 41, Saito T Insecticide susceptibility of the leafminer, Chromatomyia horticola (Goureau) (Diptera: Agromyzidae). Applied of Entomology and Zoology, 39, Saito T, Ikeda F, Ozawa A Effects of pesticides on parasitoid complex of serpentine leafminer Liriomyza trifolii (Burges) in Shizuoka prefecture. Japanese Journal of Applied Entomology, 20, Song L Q, Gao Y, Zhang W Q, Gu D X, Xu Z F, Gu D J Bionomics of Chrysonotomyia formosa (Westwood) (Hymenoptera: Eulophidae). Acta Entomologia Sinica, 48, (in Chinese) Tagami Y, Doi M, Sugiyama K, Tatara A, Saito T Survey of leafminers and their parasitoids to find endosymbionts for improvement of biological control. Biological Control, 38, Thorne A D, Pexton J J, Dytham C, Mayhew P J Small body size in an insect shifts development, prior to adult eclosion, towards early reproduction. Proceedings of the Royal Society of London series B-Biology Sciences, 273: Tilman D Resource Competition and Community Structure. Princeton University Press, Princeton, USA. Vayssade C, Martel V, Moiroux J, Fauvergue X, van Alphen J J M, van Baaren J The response of life-history traits to a new species in the community: a story of Drosophila parasitoids from the Rhône and Saône valleys. Biological Journal of the Linnean Society, 107, Volkoff A N, Daumal J Ovarian cycle in immature and adult stages of Trichogramma cacoeciae and T. brassicae (Hym. Trichogrammatidae). Entomophaga, 39, West G B, Brown J H, Enquist B J The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science, 284, Wu Z S, Heimpel G E Dynamic egg maturation strategies in an aphid parasitoid. Physiological Entomology, 32, Zhang Y B, Liu W X, Wan F H, Li Q. 2010a. Oviposition and host feeding behavior of Diglyphus isaea female wasp on the larval of Liriomyza sativae. Chinese Journal of Biological Control, 26, (in Chinese) Zhang Y B, Liu W X, Wan F H, Li Q. 2010b. Effect of nutritional status on the parasitism and host feeding behavior of Diglyphus isaea Walker. Acta Entomologia Sinica, 53, (in Chinese) Zhang Y B, Liu W X, Wang W, Wan F H, Li Q Lifetime gains and patterns of accumulation and mobilization of nutrients in females of the synovigenic parasitoid, Diglyphus isaea Walker (Hymenoptera: Eulophidea), as a function of diet. Journal of Insect Physiology, 57,
15 1 Table 1 Immature developmental times (Mean±SE) of Diglyphus isaea and Neochrysocharis formosa. Wasps sex Larval stage (hours) Pupal stage (hours) Immature stage (hours) D. isaea female 99.5±1.1 Ba 103.6±1.4 Ba 204.2±2.2 Ba male 95.9±1.4 Bb 100.5±1.6 Bb 196.2±1.6 Bb N. formosa female 121.1±1.1 Aa 169.0±2.3 Aa 290.0±3.0 Aa 2 3 male 115.4±3.7 Ab 163.1±3.1 Ab 278.6±5.0 Ab Means in columns followed by different lowercase letters showed significant differences between different intraspecific sexes at P 0.05; Means in columns followed by different capital letters showed significant differences between the same interspecific sex at P 0.05 (Two-way ANOVA, SAS). 15
16 Table 2 Influence of host feeding on life-history traits (Mean ± SE) in Diglyphus isaea and Neochrysocharis formosa. Wasp species Treatments (n=replication) Host feeding (No. host-feeding events per female) Fecundity (No. eggs laid per female) Mortality (Total No. dead hosts affected by female) Longevity (days) D. isaea Starvation (n=25) 1.2±0.1 Bb 2.2±0.2 Bb 5.3±0.2 Ab Host food (n=23) 56.6±4.3 A 125.6±3.8 Aa 319.3±9.4 Aa 25.3±1.6 Aa N. formosa Starvation (n=31) 5.5±1.0 Ab 13.0±2.3 Ab 4.7±0.9 Bb Host food (n=21) 43.7±3.3 A 62.7±4.2 Ba 126.8±7.1 Ba 14.6±1.0 Ba Means in columns followed by different lowercase letters showed significant intraspecific differences between different treatments at P 0.05; Means in columns followed by different capital letters showed significant interspecific differences in the same treatment at P 0.05 (Kruskal Wallis test, SAS). 16
17 Table 3 Daily host-feeding events, and fecundity, mortality, and longevity gains per host-feeding event (Mean ± SE) of Diglyphus isaea and Neochrysocharis formosa in host-feeding treatment. Daily host-feeding event Fecundity gain per event Mortality gain per event Longevity gain per event Species (No. host feeding event (No. egg gained by each (No. host dead gained by (No. days gained by each host per day) host feeding event ) each host feeding event) feeding event) D. isaea 2.60±0.30 a 2.57±0.23 a 6.24±0.42 a 0.44±0.06 a N. formosa 2.96±0.10 a 1.39±0.11 b 2.64±0.11 b 0.21±0.01 b Means in columns followed by different letters are significantly different between the two species at P 0.05 (ANOVA, SAS). 17
18 Table 4 Life history traits of two coexisting parasitoids Diglyphus isaea and Neochrysocharis formosa. Life history traits D. isaea N. formosa Ovigeny index 0.002, extreme synovigeny 0.12, relative weak synovigeny Ecto/endoparasitoid ectoparasitoid endoparasitoid Idio-/koinobiont idiobiont idiobiont Body size big small Egg type anhydropic egg anhydropic egg Egg volume big small Development time and Longevity short immature stage and long adult longevity long immature stage and short adult longevity Type of host-feeding non-concurrent and destructive non-concurrent and/or concurrent destructive Lifetime host feeding similar similar Gain per host-feeding event high low Lifetime fecundity large small Host mortality large small Age-specific fecundity curve slow Fast 18
19 Fig. 1. Initial egg load (eggs per ovary) and potential lifetime egg production (eggs for lifetime) as function of hind tibia length in Diglyphus isaea (a) and Neochrysocharis formosa (b). 19
20 Fig. 2. Relationship between the pupal developmental time and initial egg load at emergence in Neochrysocharis formosa. 20
21 Fig. 3. Survivorship curves for Diglyphus isaea and Neochrysocharis formosa females feeding on different diet treatments, where host means access to host feeding (Weibull distribution, SAS). 21
22 Fig. 4. Age-specific curves for the number of host-feeding events (a), fecundity (b) and the number of dead hosts (c) for each female Diglyphus isaea and Neochrysocharis formosa provided with water and excess hosts. Line bars represents standard error of the mean. 22
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