Demographic Analysis of the Fitness of Problepsis Superans

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Demographic Analysis of the Fitness of Problepsis superans (Lepidoptera: Geometridae) Feeding on Three Ligustrum (Lamiales: Oleaceae) Species Author(s): Liang-Xiong Hu, Ye Chen, Zheng-Sheng He, Zhi-Wen Zou, and Bin Xia Source: Journal of Economic Entomology, 107(3):1045-1054. 2014. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/EC13468

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. ECOLOGY AND BEHAVIOR Demographic Analysis of the Fitness of Problepsis superans (Lepidoptera: Geometridae) Feeding on Three Ligustrum (Lamiales: Oleaceae) Species

1,2 2 2 1 1,3 LIANG-XIONG HU, YE CHEN, ZHENG-SHENG HE, ZHI-WEN ZOU, AND BIN XIA

J. Econ. Entomol. 107(3): 1045Ð1054 (2014); DOI: http://dx.doi.org/10.1603/EC13468 ABSTRACT Using the age-stage, two-sex life table, the effects of three ligustrum species, Ligus- trum ϫ vicaryi Hort., Ligustrum quihoui Carrie`re, and Ligustrum lucidum Aiton, on the Þtness of Problepsis superans (Butler, 1885) (Lepidoptera: Geometridae) were assayed by considering life table parameters of P. superans at 27 Ϯ 1ЊC, 70 Ϯ 5% relative humidity, and a photoperiod of 16:8 (L: D) h. The means and SEs of population parameters were calculated using the jackknife and bootstrap methods. The total developmental time of larval stage of P. superans on L. ϫ vicaryi was signiÞcantly shorter than that on L. ϫ vicaryi and L. quihoui, whereas higher fecundity was observed on L. ϫ vicaryi. The highest value of the Þnite rate of increase was observed on L. ϫ vicaryi. The intrinsic rate of increase of P. superansonL. ϫ vicaryi, L. quihoui, and L. lucidum, was 0.147 Ϯ 0.004, 0.130 Ϯ 0.004, and 0.112 Ϯ 0.005, respectively, which differed signiÞcantly among the three ligustrum species. The net reproductive rate varied from 122.8 Ϯ 24.7 female offspring on L. lucidum to 242.2 Ϯ 36.2 female offspring on L. ϫ vicaryi. The lowest mean generation time was observed on L. ϫ vicaryi. The gross reproductive rate of P. superans on the three ligustrum species did not signiÞcantly differ. Based on growth and population parameters, the suitability of the three ligustrum species to P. superans is ranked from high to low in the order as L. ϫ vicaryi, L. quihoui, and L. lucidum.

KEY WORDS Ligustrum ϫ vicaryi, Ligustrum quihoui, Ligustrum lucidum, life table

Ligustrum ϫ vicaryi Hort. with chlorophyll-less gold- southern Russia, and China (Fang 2003). There is little en-color leaves on the upper canopy, is a hybrid of information available on the biology, host plants, and Californian Ligustrum ovalifolium Hasskarl variety au- life history of P. superans. reo-marginatum and Ligustrum vulgare L., and is The effects of host cultivars on the biology of insects widely used as a landscape shrub for horticultural are important in understanding host suitability of ornamentation in China (Yuan et al. 2010). Ligustrum plant-infesting insect species (Xue et al. 2010). Life quihoui Carrie`re (waxy leaf privet) is a shrubby, table studies are fundamental to population ecology. semievergreen to evergreen privet, and used for A life table gives the most complete description of the hedgerow plant for urban road and residential area survivorship, development, stage differentiation, and greening in China (Zhu and Li 2004). The two plants reproduction of a population and provides basic data are often arranged simultaneously for colored vege- on population growth parameters (Gabre et al. 2005). tation landscaping. Ligustrum lucidum W.T. Aiton, an Among the life table parameters, the intrinsic rate evergreen shrub or small tree that belongs to the genus of increase (r) is a key demographic parameter useful Ligustrum L. in Oleaceae, is a precious Kudingcha for predicting the growth potential of an insect pop- beverage plant and medicinal plant, with a variety of ulation under a given environmental condition (Rick- medicinal values (Shi et al. 1998). These three ligustrum species are widely applied to urban greening lefs and Miller 1999, Southwood and Henderson 2000). with the development of cities and towns in China The value of r has also been commonly used to eval- (Zhu and Li 2004, Cai 2009). uate the level of plant resistance to insects (Ruggle Problepsis superans (Butler, 1885) (Lepidoptera: and Gutierrez 1995, Razmjou et al. 2006). Host plants Geometridae) is a defoliator pest of the garden plant displaying higher values of r are relatively more sus- L. quihoui (Wu et al. 2011). P. superans is found in ceptible than plants with lower values of r. Knowledge Japan (Fang 2003, Sihvonen 2005), North Korea, of cultivar susceptibility or resistance and the life table parameters of a pest might be fundamental compo- 1 Department of Biological Science, Nanchang University; Nan- nents of an integrated pest management program for chang, Jiangxi 330031, China. any crops. Such information can contribute to detect 2 College of life Science, Jiujiang University, Jiujiang, Jiangxi 332000, China. and monitor pest infestations, cultivar selection, and 3 Corresponding author, e-mail: [email protected]. crop breeding (Toapanta et al. 2005, Razmjou et al.

0022-0493/14/1045Ð1054$04.00/0 ᭧ 2014 Entomological Society of America 1046 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 3

2006, Zare et al. 2013). However, no such studies were were replaced with fresh ones every day at the same time conducted for P. superans on different host plants. throughout the duration of larval development. Devel- Most of the traditional female age-speciÞc life ta- opmental periods, mortality of eggs, larval growth, pu- bles, e.g., the LewisÐLeslie matrix (Lewis 1942, Leslie pation duration, and emergence rate were recorded 1945, Birch 1948), ignore the male population and the daily, and larval instars were identiÞed based on the variable developmental rates among individuals and remains of head capsules. stage differentiation. However, most economic insect Adults Rearing. After emergence of new-born pests are sexual, and both sexes may cause economical adults, a pair of P. superans male and female was loss. Moreover, developmental rates often differ be- transferred to a 1,000-ml transparent plastic bowl with tween the sexes and among individuals (Istock 1981). thin mesh holes at the top of the cover for aeration To consider both sexes and variable development at the above-mentioned conditions. The oviposition rates among individuals, Chi and Liu (1985) devel- container was daily provided with a 10% honey water oped an age-stage, two-sex life table theory. This life solution on an absorbent cotton ball for feeding and table theory takes the stage differentiation and male fresh leaves of each host plant for oviposition until the population into consideration. The age-stage, two- female adult died. In the case of early death of females, sex life table theory has been applied to insect and the single male was also provided daily with 10% mite species by a number of researchers (Abou Zied honey solution until death. Preoviposition, oviposition et al. 2003, Gabre et al. 2005, Kavousi et al. 2009, Hu periods, and adult duration were also recorded. The et al. 2010, Farhadi et al. 2011, Huang et al. 2012, eggs laid daily were recorded and transferred into a Jin et al. 2012, Ravuiwasa et al. 2012, Azimi et al. plastic cup (50 ml) with a Þne writing brush. 2013, Yu et al. 2013, Zare et al. 2013). Life Table Study. The raw life history data on all The objective of this study was to obtain a prelim- individuals of P. superans were analyzed according inary understanding of the suitability of the three to the age-stage, two-sex life table (Chi and Liu ligustrum species as host plants to P. superans by con- 1985) and the method described by Chi (1988). For sidering life table parameters and the main biological the tedious and complicated calculations involved characteristics of the pest. This information will be in the analyses of raw data and the life table, the user- necessary for the development of a control program friendly computer program TWOSEX-MSChart was for P. superans on the three ligustrum species. used to estimate parameters (Chi 2012). This program is available at http://140.120.197.173/Ecology/Download/ Materials and Methods Twosex.rar and http://www.znu.ac.ir/agriculture/ pages/plantprotection/software/index.htm. The follow- ϫ Plants. Plants used in this study were L. vicaryi ing parameters were calculated: age-stage-speciÞc sur- (also named the golden leaf ligustrum), L. quihoui, and vival rate (s , where x is the age and j is the stage), L. lucidum. Host plants were planted in the gardening xj age-stage-speciÞc fecundity (fxj), age-speciÞc survival base located in the College of Life Science of Jiujiang rate (l ), age-speciÞc fecundity (m ), age-stage life ex- University, Jiujiang, China. During the experiments, x x pectancy (exj), and reproductive value (vxj), adult all plants were irrigated at the same time and no preoviposition period (APOP) of female, and total fertilizers or pesticides were used. preoviposition period (TPOP) of female counted from P. superans Colony. P. superans larvae were origi- birth. The population parameters (r, intrinsic rate of nally collected from the campus landscape shrubs, and ␭ increase; , Þnite rate of increase; R0, net reproduc- subsequently reared on the three ligustrum species. tion rate; T, the mean generation time; and GRR, Before the experiments, larvae were reared separately gross reproductive rate) were calculated accord- on the above-mentioned host plants for two successive ingly. Intrinsic rate of increase was estimated using generations to eliminate the effects of previously in- the iterative bisection method from the EulerÐLotka gested food. The stock culture was maintained in an ϱ Ϫr͑xϩ1͒ ϭ artiÞcial climate box (950 by 850 by 1,850 mm; Shang- formula: ͚ e lxmx 1 with age indexed from hai Permanent Science and Technology Co. Ltd., xϭ0 Shanghai, China) in the laboratory of Department of 0 (Goodman 1982). The mean generation time (T) Life Science, Jiujiang University, in 2012. The climate was deÞned as the length of time require by a pop- condition was set as 27 Ϯ 1ЊC, 75 Ϯ 5% relative hu- ulation to increase to R0-fold of its size at the stable midity (RH), and a photoperiod 16:8 (L:D) h. The age-stage distribution and was calculated as T ϭ eggs obtained from the second-generation adults were (lnR0)/r. The age-stage life expectancy (exj) was used in the following experiments. calculated according to Chi and Su (2006). The Larvae and Pupae Rearing. Sixty eggs oviposited on relationship between the net reproductive rates R0 the leaves of one of the ligustrum species within a 24-h and the mean female fecundity F can be described ϭ ϫ period were randomly selected and put in a plastic as R0 F (Nf/N), where N is the total number of bowl (1,000 ml) in an illumination incubator under the eggs used for the life table study at the beginning, above-mentioned conditions. Hatched larvae were and Nf is the number of female adults emerging from placed individually in fresh host leaves in plastic petri these N eggs (Chi 1988). The means and SEs of dishes (9 cm in diameter) with a hole in the center of population parameters were calculated using the the lid, which was covered with muslin cloth for aera- jackknife (Sokal and Rohlf 1995) and bootstrap tion. The leaves with the petiole dipped in wet cotton method (Efron and Tibshirani 1993). During the June 2014 HUETAL.: LIFE TABLE OF Problepsis superans 1047

Table 1. Life history statistics (mean ؎ SE; n)ofP. superans reared on L. ؋ vicaryi, L. quihoui, and L. lucidum at 27 ؎ 1°C and RH 5% ؎ 75

L. ϫ vicaryi L. quihoui L. lucidum Parameters Stages n n n mean Ϯ SE mean Ϯ SE mean Ϯ SE Developmental time (d) Egg 58 5.88 Ϯ 0.04 58 5.90 Ϯ 0.04 59 5.90 Ϯ 0.04 First instar 56 4.11 Ϯ 0.04a 55 4.80 Ϯ 0.05b 55 5.85 Ϯ 0.12c Second instar 55 2.20 Ϯ 0.05a 54 2.44 Ϯ 0.10a 53 3.15 Ϯ 0.13b Third instar 55 2.47 Ϯ 0.10a 53 2.94 Ϯ 0.08b 52 3.02 Ϯ 0.10c Fourth instar 55 2.89 Ϯ 0.06a 53 3.11 Ϯ 0.08a 52 3.67 Ϯ 0.10b Fifth instar 55 6.80 Ϯ 0.13a 52 7.37 Ϯ 0.11b 50 8.56 Ϯ 0.17c Pupa 55 8.31 Ϯ 0.13 52 8.35 Ϯ 0.08 47 8.49 Ϯ 0.07 Egg-pupa 55 32.64 Ϯ 0.19a 52 34.92 Ϯ 0.21b 47 38.60 Ϯ 0.34c Adult longevity (d) Male 28 8.18 Ϯ 0.39a 26 7.31 Ϯ 0.30ab 23 6.87 Ϯ 0.22b Female 27 8.89 Ϯ 0.40a 26 8.08 Ϯ 0.36ab 24 7.04 Ϯ 0.32b APOP (d) Female 27 1.30 Ϯ 0.09 26 1.19 Ϯ 0.08 24 1.21 Ϯ 0.09 TPOP (d) Female 27 33.89 Ϯ 0.28a 26 36.88 Ϯ 0.22b 24 39.90 Ϯ 0.50c Oviposition period (d) Female 27 7.26 Ϯ 0.38a 26 6.23 Ϯ 0.35ab 24 5.33 Ϯ 0.32b Fecundity (F) (eggs per female) Female 27 538.4 Ϯ 25.6a 26 445.6 Ϯ 25.1 24 308.0 Ϯ 39.8c

APOP (d), adult preoviposition period; TPOP (d), total preoviposition period. Means within a row sharing the same letter are not signiÞcantly different at the 5% level using TukeyÐKramer test. bootstrap procedure, the total number of bootstrap ences in TPOP of P. superans reared on different hosts. samples was 10,000 times. Data concerning devel- In contrast, the APOP did not show any signiÞcant opment time, longevity, fecundity, and population difference among the three species. The longevities of parameters on different host plants were compared both male and female adults on L. ϫ vicaryi were using the TukeyÐKramer procedure (Dunnett signiÞcantly longer than those observed on L. lucidum; 1980). however, there was no signiÞcant difference between L. ϫ vicaryi and L. quihoui or between L. quihoui and Results L. lucidum. Fecundity. The fecundity of P. superans on L. luci- Developmental Time and Adult Longevity. Effects dum was signiÞcantly lower than on L. ϫ vicaryi and of the three ligustrum species on the developmental L. quihoui; however, there was no signiÞcant differ- time and adult longevity as well as fecundity of P. ence between L. ϫ vicaryi and L. quihoui. The highest superans are given in Table 1. The pest could complete fecundity was observed on L. ϫ vicaryi, suggesting its development on the species without any abnor- that P. superans is well-adapted to this species. mality in shape and size. The durations of all devel- Life Table Parameters. The age-stage-speciÞc sur- opmental stages of P. superans except the incubation vival rate (sxj)ofP. superans (Fig. 1) gives the prob- period of eggs, APOP, and pupa period were affected ability that a newly laid egg will survive to age x and by different ligustrum species. Furthermore, signiÞ- stage j. Overlapping between stages shows the variable cant difference was observed on the Þrst instar, third developmental rate among individuals. These curves instar, Þfth instar, preadult, and TPOP among the also show the survivorship and stage differentiation three ligustrum species. The developmental periods rate of P. superans on different species. Relative num- were signiÞcantly higher in the second- and fourth- ber alive in each age-stage group of P. superans on the instar larvae fed on L. lucidum than on L. ϫ vicaryi or L. quihoui, but not between L. ϫ vicaryi and L. quihoui. ligustrum species is shown in Fig. 1. The male adults The total preadult period of P. superans on the three emerged earlier, but lived a few days less than the ligustrum species differed signiÞcantly and varied females. The age-speciÞc survival rate (lx), age-stage- greatly from 32.64 Ϯ 0.19 d to 38.60 Ϯ 0.34 d. The speciÞc fecundity (fx8), the age-speciÞc fecundity highest developmental time was observed on L. luci- (mx), and age-speciÞc maternity (lxmx) are shown in ϫ dum. In general, the developmental time of the larval Fig. 2. Fecundity curves of P. superans on L. vicaryi stage of P. superans on L. lucidum was signiÞcantly begin earlier than that of L. quihoui and L. lucidum. longer than on L. ϫ vicaryi and L. quihoui. For exam- The age-speciÞc survival rate (lx) is the probability ple, the Þrst- or Þfth-instar larvae of P. superans on L. that a new egg will survive to age x and is calculated lucidum lasted the longest developmental time, by pooling all individuals of both sexes and those died whereas the shortest period was found on L. ϫ vicaryi. during the preadult stages. The curve lx is a simpliÞed It demonstrated that the developmental rate of P. version of the curves in Fig. 1. superans on L. lucidum was slower than those on L. ϫ The mean number of offspring produced by indi- vicaryi and L. quihoui. Both adult males and females vidual P. superans of age x and stage j per day was developed more quickly on L. lucidum than on L. ϫ shown with the age-stage fecundity (fxj) in Fig. 2. vicaryi or L. quihoui. Because only adult females produce offspring, there Ϯ Mean TPOP of P. superans was 39.90 0.50 d on L. was only a single curve fx8. The fx8 shows that the lucidum, 36.88 Ϯ 0.22 d on L. quihoui, and 33.89 Ϯ female is the eighth life stage. For example, the num- 0.28 d on L. ϫ vicaryi. There were signiÞcant differ- ber of offspring produced by each female on L. ϫ 1048 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 3

had the largest ␭ value, and those on L. lucidum had the smallest ␭ value, whereas those on L. quihoui had intermediate ␭ value (Table 2). The r is in accord with the ␭. The intrinsic rate of increase was 0.147 Ϯ 0.004, 0.130 Ϯ 0.004, and 0.112 Ϯ 0.005 dϪ1 on L. ϫ vicaryi, L. quihoui, and L. lucidum, respectively, and the highest value was recorded on L. ϫ vicaryi. The net re- Ϯ productive rate (R0) value varied from 122.8 24.7 female offspring on L. lucidum to 242.2 Ϯ 36.2 female offspring on L. ϫ vicaryi. The mean generation time (T)ofP. superans on the three ligustrum species differed signiÞcantly. The highest amounts of the gross reproductive rate (mean number of eggs per female per generation) of P. superans were observed on L. ϫ vicaryi; however, there were no signiÞcant differences among the GRRs on the three ligustrum species.

Discussion It is well-known that growth, development, and survival of insects depend on the quality and quantity of food they consume (Scriber and Slansky 1981). The effects of a host plant on different life history traits of insects, including larval and postlarval development have been proven for various insects, such as Diapho- rina citri (Kuwayama) (Homoptera: Psyllidae) (Tsai and Liu 2000), Aphis spiraecola Patch (Homoptera: Aphididae) (Tsai and Wang 2001), Erinnyis ello (L.) (Lepidoptera: Sphingidae) (Barrigossi et al. 2002), Spodoptera litura (F.) (Lepidoptera: Noctuidae) (Pansaree et al. 2006, Xue et al. 2010), Ennomos sub-

Fig. 1. Age-stage-speciÞc survival rate (sxj)ofP. superans signarius Hu¨ bner (Lepidoptera: Geometridae) (Ryall reared on L. ϫ vicaryi, L. quihoui, and L. lucidum at 27 Ϯ 1ЊC 2010), and Pieris brassicae (L.) (Lepidoptera: Pieri- and 75 Ϯ 5% RH. dae) (Hasan and Ansari 2010). There are few documents available on the biology or vicaryi started on day 32, peaked on day 36, and de- host plants of P. superans. In this study, the age-stage, clined to 0 on day 48. two-sex life table technique was applied to examine the

The age-stage-speciÞc life expectancy (exj) was cal- Þtness of P. superans maintained on the three ligustrum culated according to Chi and Su (2006). The age-stage species. Our results showed that P. superans could feed, life expectancies of P. superans on the ligustrum spe- survive, and develop on the three ligustrum species, but cies are shown in Fig. 3. The life expectancy of a new host variability signiÞcantly affected its development, egg on L. ϫvicaryi, L. quihoui, and L. lucidum were 38.45, fecundity, and life table parameters. 38.53, and 40.38 d, respectively. The contribution of an A plantÕs nutritional quality, secondary metabolites, individual of age x and stage j to the future population is and morphological condition can affect the survival, described by the age-stage reproductive value (vxj; Fig. population growth, and fecundity of herbivorous in- 4). The reproductive value of a newborn (v01) is exactly sects (Agrawal 2000, Dent 2000, Dicke 2000, Awmack equal to the Þnite rate of increase. The major peak and Leather 2002, White 2005, Hwang et al. 2008, reproductive values of females reared on L. ϫ vicaryi, L. Fuentealba and Bauce 2012). The population growth ϭ quihoui, and L. lucidum were at the age of 34 d (v34 parameters of P. superans varied in response to the ϭ ϭ 367.13), 37 d (v37 324.74), and 35 d (v35 240.54), three ligustrum species. Developmental period of P. respectively. It shows that individuals at the peak repro- superans preadult on different ligustrum species in this duction can contribute much more than a newborn egg. study ranged from 32.64 Ϯ 0.19 to 38.6 Ϯ 0.337 d. Life For example, a newly laid egg on L. ϫ vicaryi has a span of male was less than that of female (Table 1). reproductive value 1.16, but a female of age 34 d has a Patel et al. (1986) reported that the development of S. much higher reproductive value 367.13. litura pupae was not signiÞcantly affected by cotton The means and SEs of population parameters (r, ␭, host plants on which their larvae fed. However, Xue

R0, GRR, and T)ofP. superans on the three ligustrum et al. (2010) showed that the S. litura pupae developed species are estimated using the jackknife and boot- signiÞcantly faster on cowpea than on Chinese cab- strap methods and listed in Table 2. Among the three bage, sweet potato, and tobacco, although the differ- ligustrum species, the r, ␭, and T values estimated by ence was Ͻ1 d longer on sweet potato, 1 d longer on the jackknife and bootstrap methods showed signiÞ- tobacco, and 1.5 d longer on Chinese cabbage. In our cant differences. The cohorts reared on L. ϫ vicaryi study, the pupae developed a little faster on L. ϫ June 2014 HUETAL.: LIFE TABLE OF Problepsis superans 1049

Fig. 2. Age-speciÞc survival rate (lx), female age-stage-speciÞc fecundity (fx8), age-speciÞc fecundity (mx), and age- ϫ Ϯ Њ Ϯ speciÞc maternity (lxmx)ofP. superans reared on L. vicaryi, L. quihoui, and L. lucidum at 27 1 C and 75 5% RH.

vicaryi than on L. lucidum and L. lucidum; however, no our experiments, performed signiÞcantly better on signiÞcant differences were found on the three ligu- L. ϫ vicaryi and L. quihoui than on L. lucidum. The strum species. better r of P. superans found on L. ϫ vicaryi and on L. The age of Þrst reproduction by females has an quihoui was mainly the result of the greater overall important effect on population growth (Rezaie et al. fecundity of this pest. The poor performance of P. 2013). The APOPs of P. superans on the three ligus- superans on L. lucidum was the result of poor fecun- trum species were not signiÞcantly different; however, dity, longer developmental time, and a higher larval the TPOP showed signiÞcant differences. Most ento- mortality rate (Tables 1 and 2). mologists calculate only APOP. In respect to the effect The population growth parameters of P. superans on of preoviposition period on population growth, TPOP the three species are shown in Table 2. Life cycle, offers more meaningful statistics than APOP because intrinsic rate of increase, and some other develop- it honestly reveals the time from birth to the beginning mental and demographic parameters of P. superans of reproduction of the next generation. In short, APOP were considerably affected by the diet on the three was calculated based on the adult age, while TPOP ligustrum species (Tables 1 and 2). The demographic ␭ took the total preadult age into consideration. The parameters (r, , R0, and T)ofP. superans population fecundity of P. superans on L. lucidum signiÞcantly on L. lucidum differed signiÞcantly from those on L. ϫ differed from that on other species, and the highest vicaryi and L. quihoui (Table 2). For example, the fecundity was observed on L. ϫ vicaryi. intrinsic rate of increase (r) was 0.112 Ϯ 0.005 on L. The present experiments demonstrated signiÞcant lucidum, 0.130 Ϯ 0.004 on L. quihoui, and 0.147 Ϯ 0.004 differences in the performance of P. superans on the on L. ϫ vicaryi. The intrinsic rate of increase (r)is three ligustrum species. P. superans population used in reßective of many factors such as fecundity, survival, 1050 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 3

Fig. 3. Age-stage-speciÞc life expectancy (exj)ofP. superans reared on L. ϫ vicaryi, L. quihoui, and L. lucidum at 27 Ϯ 1ЊC and 75 Ϯ 5% RH. and generation time, and shows the potential of a Fig. 4. Age-stage-speciÞc reproductive value (vxj)ofP. population to increase under the conditions tested. superans reared on L. ϫ vicaryi, L. quihoui, and L. lucidum at Among the life table parameters, r would be the more 27 Ϯ 1ЊC and 75 Ϯ 5% RH. appropriate index to evaluate the performance of an insect on different host plants (Kocourek et al. 1994, observed on L. ϫ vicaryi, while the lowest rate of these Southwood and Henderson 2000). The net productive stages was observed on L. lucidum, and the interme- rate of P. superans on L. lucidum was signiÞcantly diate rate was on L. quihoui. The total mortality of Þrst- lower than those on L. ϫ vicaryi and L. quihoui, which to fourth-instar larvae on L. lucidum was 11.86%, varied from 122.8 Ϯ 24.7 female offspring on L. luci- whereas on L. ϫ vicaryi and L. quihoui it was 5.17 and dum to 242.2 Ϯ 36.2 female offspring on L. ϫ vicaryi. 8.63%, respectively. As a result, there was a lower ϫ The highest value of r and R0 on L. vicaryi showed survival rate of mid-instar larvae on L. lucidum com- that this species is a more suitable food source for pared with the other host species (Fig. 2). Low mor- population growth of P. superans in comparison to L. talities were observed at the Þfth-instar larvae and quihoui and L. lucidum. pupal stage of P. superans reared on the three ligus- Because the age-stage, two-sex life table incorpo- trum species. Therefore, the age-stage-speciÞc sur- rates variation among individuals in developmental vival rates of the Þfth-instar larvae and pupae stage rates, stage overlaps in the survival rate can be ob- were higher than that of the mid-instar on the three served. In our study, signiÞcant overlaps were also ligustrum species. Because the survival rate of adults observed (Fig. 1). At the age of 26 d, we observed the is separated as female and male, they look much lower Þfth-instar larvae and pupae at the same time. The than the preadult. But the age-speciÞc survival rate highest age-stage-speciÞc survival rate of larvalÐpupal (lx) shows the survival rate of adult is not much lower stages and adult male and female of P. superans were than that of the preadult. June 2014 HUETAL.: LIFE TABLE OF Problepsis superans 1051

؊1 ␭ ؊1 ؎ Table 2. Mean SE of the intrinsic rate of increase (r;d ), ﬁnite rate of increase ( ;d ), net reproductive rate (R0; offspring per individual), mean generation time (T), and gross reproductive rate (GRR; offspring per individual) of P. superans reared on L. ϫ vicaryi, L. quihoui, and L. lucidum at 27 Ϯ 1°C and 75 Ϯ 5% RH

Statistical Intrinsic rate of Finite rate of Net reproduction Mean generation Gross reproduction Species Ϫ1 ␭ Ϫ1 method increase r (d ) increase (d ) rate R0 (offspring) time (T;d) rate GRR (offspring) Jackknife L. ϫ vicaryi 0.148 Ϯ 0.004a 1.160 Ϯ 0.005a 242.3 Ϯ 36.7a 37.2 Ϯ 0.3a 394.8 Ϯ 58.9 L. quihoui 0.131 Ϯ 0.004b 1.140 Ϯ 0.005b 193.1 Ϯ 30.7a 40.4 Ϯ 0.2b 330.4 Ϯ 51.7 L. lucidum 0.113 Ϯ 0.005c 1.120 Ϯ 0.006c 123.2 Ϯ 25.2b 42.8 Ϯ 0.7c 297.2 Ϯ 74.6 Bootstrap L. ϫ vicaryi 0.147 Ϯ 0.004a 1.159 Ϯ 0.005a 242.2 Ϯ 36.2a 37.2 Ϯ 0.3a 377.7 Ϯ 53.9 L. quihoui 0.130 Ϯ 0.004b 1.139 Ϯ 0.005b 193.2 Ϯ 30.2a 40.4 Ϯ 0.2b 329.9 Ϯ 44.7 L. lucidum 0.112 Ϯ 0.005c 1.118 Ϯ 0.006c 122.8 Ϯ 24.7b 42.8 Ϯ 0.6c 279.7 Ϯ 64.5

Means, which are estimated by the same statistical method, within a column sharing the same letter are not signiÞcantly different at the 5% level using the TukeyÐKramer test.

ϫ Chi (1988) demonstrated the relationship between superans on L. vicaryi, whereas Nf was 27. Our data the net reproductive rate R0 and the mean female for R0, which was estimated with the jackknife ϭ ϫ fecundity F for two-sex life table by using R0 F method, and F are consistent. The relationship be- (Nf/N). In this study, for example, N was 60 eggs of P. tween the mean fecundity and the net reproductive

ϫ Ϯ Fig. 5. Frequency distribution of the rpseudo and rB of P. superans reared on L. vicaryi, L. quihoui, and L. lucidum at 27 1ЊC and 75 Ϯ 5% RH. 1052 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 3

ϫ Fig. 6. Frequency distribution of the R0-pseudo and R0,B of P. superans reared on L. vicaryi, L. quihoui, and L. lucidum at 27 Ϯ 1ЊC and 75 Ϯ 5% RH. rate estimated by the bootstrap technique was, however, reproductive value also increases. When most female slightly inconsistent with the relationship proved by the individuals complete preadult development and begin mathematical method by Chi and Su (2006). Because the to produce eggs, the cohort soon achieves its highest net reproductive rate (R0) incorporates the survival rate, contribution to the population (Gabre et al. 2005). Յ the equation R0 F will always apply. If preadult mor- This peak is consistent with the peak of lxmx in Fig. 2. Ͻ tality occurs, then certainly R0 F. Yu et al. (2005) The jackknife and bootstrap techniques are usually proved the relationship among GRR, R0,and the preadult used to estimate the variance of life table parameters Ͻ ϫ Ͻ survivorship (la)asR0 la GRR GRR. For example, to correct for bias (Jha et al. 2012). For all population ϫ on L. vicaryi, R0 is 242.2, la is 0.92, and GRR is 377.7 parameters, the variance estimated by the jackknife (Tables 1 and 2). Thus, the relationship 242.2 Ͻ 0.92 by technique is much higher than that estimated by the 377.7 Ͻ 377.7 is consistent. All of our results for P. su- bootstrap technique (Jha et al. 2012). Our results also perans on the three ligustrum species are consistent with showed this situation (Table 2). The differences in the the relationships given by the above equation. frequency distributions of the intrinsic rate (r) and net

In this study, the peak reproductive value of P. reproductive rate (R0) estimated with the jackknife superans on L. ϫ vicaryi occurred at the age of 34 d and bootstrap methods are elucidated in the values (Fig. 4). This value falls between the mean TPOP of the variables (Figs. 5 and 6). Efron (1982) re- (33.89 Ϯ 0.28 d) for all P. superans females (Table 1) ported that the bootstrap technique has a higher and the peak (36 d) of lxmx in Fig. 2. The results reliability than the jackknife technique for estimat- suggest that when the females begin to reproduce, the ing variances. The frequency distribution of sample June 2014 HUETAL.: LIFE TABLE OF Problepsis superans 1053 means estimated by the bootstrap technique Þt the Chi, H. 2012. TWOSEX-MSChart: a computer program for normal distribution, and smaller variances occurred, the age-stage, two-sex life table analysis. (http://140.120. while the jackknife results with larger variances failed 197.173/Ecology/Download/TWOSEX-MSChart.zip). the normality test (Figs. 5 and 6). When the jackknife Chi, H., and H. Liu. 1985. Two new methods for the study technique was applied to calculate the SE of the net of insect population ecology. Bull. Inst. Zool. Acad. Sin. reproductive rate, biologically meaningless zeros 24: 225Ð240. would be generated, whereas the bootstrap technique Chi, H., and H. Y. Su. 2006. Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconi- did not lead to this problem (Huang and Chi 2012, Jha dae) and its host Myzus persicae (Sulzer) (Homoptera: et al. 2012, Yu et al. 2013). We can see this in the study Aphididae) with mathematical proof of the relationship (Fig. 6). Although the jackknife technique has been between female fecundity and the net reproductive rate. widely applied to estimate life table demographic pa- Environ. Entomol. 35: 10Ð21. rameters (e, g. Chi and Yang (2003), Saei Dehghan et Chi, H., and T. C. Yang. 2003. Two-sex life table and pre- al. 2009, Faal-mohammadali et al. 2013, Zare et al. dation rate of Propylaea japonica Thunberg (Coleoptera: 2013) noticed the problem and explicitly stated that “It Coccinellidae) fed on Myzus persicae (Sulzer) (Ho- results in some degree of discrepancy between the moptera: Aphididae). Environ. Entomol. 32: 327Ð333. estimated means and their deÞnition.” This study Dent, D. 2000. Host plant resistance, pp. 123Ð179. In D. again suggests that the jackknife technique should not Dent (ed.), Insect pest management. CABI Publishing, be used for the estimation of SEs of the net repro- Oxfordshire, United Kingdom. ductive rate. At the same time, we must take particular Dicke, M. 2000. Chemical ecology of host-plant selection by herbivorous arthropods: a multitrophic perspective. caution when applying resampling methods such as Biochem. Syst. Ecol. 28: 601Ð617. the jackknife and the bootstrap (Jha et al. 2012). Dunnett, C. W. 1980. Pairwise multiple comparisons in the Our data indicate that P. superans can successfully homogeneous variance, unequal sample size case. J. Am. survive, reproduce, and can potentially become a se- Stat. Assoc. 75: 789Ð795. rious pest on the three ligustrum species. Knowledge Efron, B. 1982. The jackknife, the bootstrap and other re- of Þtness and biology of P. superans on these species sampling plans. Society for Industrial and Applied Math- can help us understand the population dynamics and ematics, Philadelphia, PA. management of this insect. Plant cultivar traits such as Efron, B., and R. J. Tibshirani. 1993. An introduction to the toxicity, content of nutrients, feeding deterrent, and bootstrap. Chapman & Hall, New York, NY. physical characteristics may affect these parameters, Faal-mohammadali, H., A. Seraj, and K. Talebi-Jahromi. which should be investigated in the future. 2013. Effects of traditional insecticides on Habrobracon hebetor (Hymenoptera: Braconidae): bioassay and life- table assays. Arch. Phytopathol. Plant Prot. 46: 1Ð14. Acknowledgments Fang, Y. Q. 2003. Butterßies and moths of Mount Lushan. Jiangxi University Press, Nanchang, China. We thank Hsin Chi for providing software and guiding Farhadi, R., H. Allahyari, and H. Chi. 2011. Life table and data statistics and articleÕs modiÞcation. We are sincerely predation capacity of Hippodamia variegata (Coleoptera: grateful to the editor and the two anonymous reviewers for Coccinellidae) feeding on Aphis fabae (Hemiptera: Aphi- critical suggestions and improvement of this article. The didae). Biol. Control 59: 83Ð89. project was supported by the National Natural Science Foun- Fuentealba A., and E. Bauce. 2012. 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