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Cold Temperatures Increase Cold Hardiness in the Next Generation Ophraella communa Beetles

  • Zhong-Shi Zhou,

    Affiliation State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China

  • Sergio Rasmann,

    Affiliation Ecology and Evolutionary Biology, University of California Irvine, Irvine, California, United States of America

  • Min Li,

    Affiliation Fujian Entry-Exit Inspection and Quarantine Bureau, Fuzhou, China

  • Jian-Ying Guo,

    Affiliation State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China

  • Hong-Song Chen,

    Affiliation State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China

  • Fang-Hao Wan

    Affiliation State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China

Cold Temperatures Increase Cold Hardiness in the Next Generation Ophraella communa Beetles

  • Zhong-Shi Zhou, 
  • Sergio Rasmann, 
  • Min Li, 
  • Jian-Ying Guo, 
  • Hong-Song Chen, 
  • Fang-Hao Wan


The leaf beetle, Ophraella communa, has been introduced to control the spread of the common ragweed, Ambrosia artemisiifolia, in China. We hypothesized that the beetle, to be able to track host-range expansion into colder climates, can phenotypically adapt to cold temperatures across generations. Therefore, we questioned whether parental experience of colder temperatures increases cold tolerance of the progeny. Specifically, we studied the demography, including development, fecundity, and survival, as well as physiological traits, including supercooling point (SCP), water content, and glycerol content of O. communa progeny whose parents were maintained at different temperature regimes. Overall, the entire immature stage decreased survival of about 0.2%–4.2% when parents experienced cold temperatures compared to control individuals obtained from parents raised at room temperature. However, intrinsic capacity for increase (r), net reproductive rate (R0) and finite rate of increase (λ) of progeny O. communa were maximum when parents experienced cold temperatures. Glycerol contents of both female and male in progeny was significantly higher when maternal and paternal adults were cold acclimated as compared to other treatments. This resulted in the supercooling point of the progeny adults being significantly lower compared to beetles emerging from parents that experienced room temperatures. These results suggest that cold hardiness of O. communa can be promoted by cold acclimation in previous generation, and it might counter-balance reduced survival in the next generation, especially when insects are tracking their host-plants into colder climates.


In a changing environment, such as during range expansion, organismal rapid adaptation to novel environmental conditions is needed for assuring survival [1]. If the new environment a parent is experiencing predicts the characteristics of the progeny’s environment, then parents may enhance their net reproductive success by differentially allocating resources to their offspring so to create novel phenotypes more adapted to the novel environment. Such maternal effects have been reported in both animals and plants [2], [3], [4], [5], [6]. For example, an insect mother’s experience of environmental changes such as photoperiod, temperature and nutrition have been shown to impact several physiological and ecological traits [2], [3], [4], [5], [7], [8], as well as improve fitness related traits (e.g. development and fecundity) of the offspring [2], [3], [4], [9]. Many previous studies have shown that insect’s growth and population development in progeny were influenced by their mother’s experiences of temperature changes [10], [11], [12], [13], [14], [15], [16], [17], [18], [19], [20], [21], [22]. For example, repeated exposition to cold temperatures in female flies resulted in a change in sex ratio and number of offspring [21], [22].

Because of insects’ ectothermic physiology, temperature, among other environmental factors, is a key factor affecting individual survival, fecundity and population establishment in the field [10], [16], [23], [24], [25], [26], [27]. Insects may be significantly impacted if temperature deviates from the optimum range [18], however, the amplitude of the impact depends on the rate, intensity, and duration of temperature change [28], [29]. Resistance to cold temperatures, or cold hardiness of insects, is reflected by four variables relating to insect physiology including; water content, accumulation of glycerol or other low molecular weight polyols and sugars (cryoprotectants), supercooling point (SCP), and survival capacity under low temperature [28], [30], [31], [32], [33], [34]. Previous studies revealed that better cold hardiness is typically associated with lower SCP, lower water content, and higher glycerol content in the insect [28], [30], [31], [35], [36], [37], [38], [39], [40].

Maternal effects result in alterations of the offspring phenotype [2], [3], [5], in which, biological and ecological adaptability of offspring can be related to mother’s experience [4], [7], [8], [41]. We can thus posit that temperature-driven maternal effects are an excellent strategy for insect herbivores to be able to track range expansion of the host plant into colder climates. Therefore, we here specifically hypothesized that mother’s experience of cold temperatures can pass on to the offspring, promoting faster development, higher fecundity and higher cold hardiness in the next generation. We tested this hypothesis using Ophraella communa (Coleoptera: Chrysomelidae). Adults and larvae of the beetle feed on leaves of the common ragweed Ambrosia artemisiifolia [42], [43], [44]. Due to the insect potential to drastically reduce plant fecundity [45], [46], [47], O. communa is currently considered as biological control agent for reducing the spreading of the common ragweed. However, insects may be disfavored when common ragweed populations are expanding into colder regions of China [48]. This may provide the plant an “enemy-free space” [30], [35]. Indeed, previous study revealed that the development and female fecundity of O. communa were affected after 2 hours of low temperature stresses [17]. However, during the gradual temperature decrease from summer to winter, cold hardiness of O. communa is progressively increased [37]. Adults overwinters in soil and can even survive severe subzero temperatures during winter [43]. Therefore, if maternal effects are adaptive [49], we should expect cold hardiness of the progeny being enhanced by maternal and paternal cold experience. We measured fitness parameters (survival rate, longevity, fecundity, and life table analyses) and cold hardiness indices (SCP, water and glycerol contents) of O. communa offspring originated from parents that experienced different temperature regimes for several days.

Materials and Methods

Host Plants and Insects

The common ragweed, Ambrosia artemisiifolia is the most widespread plant of the genus Ambrosia in North America and has become invasive in most European as well as Asian countries such as Japan and China [48]. Seeds were harvested in Hunan province, China, and seedlings, grown in nurseries, were individually transplanted into plastic pots (Φ15 cm) with uniform loamy clay soil from vegetable field. Potted plants were kept in greenhouse under 26–29°C, 65±5% RH, and L14:D10 photoperiod, watered once every four days, and fertilized (N:P:K at the ratio of 13∶7:15) twice a month. Plants were used for experiments when they reached a height of about 50 cm.

Ophraella communa pupae were collected from A. artemisiifolia plants in Miluo county (28°49.089′N, 113°03.876′E), Hunan province, China, and then stored in a transparent plastic box (19 cm × 12 cm × 6 cm) covered with organdy mesh fabric in an insectary at 28°C, 70±5% RH, and L14:D10 photoperiod. An initial double pair of adults per plant was let freely reproduce, and after the fourth generation of continuous rearing, newly emerged, unmated adults were separated according to gender (n = 20 adults per plant) for two days before being randomly assigned to the different treatments (see below).

Both A. artemisiifolia and O. communa are not protected in China, thus no specific permissions were required for these locations/activities (e.g, the authority responsible for a national park or other protected area of land, the relevant regulatory body concerned with protection of wildlife, etc.).

Transgenerational Temperature Effect on O. communa Development, Survivorship, and Fecundity

Previous studies have shown that minimum threshold temperatures of egg, larva, pupa and entire immature stage of O. communa were 14.1°C, 16.9°C, 9.0°C and 13.3°C, respectively [42], and female fecundity decreased by 26.4% to 70.4% after pupal cold-storage at 4–12°C for 20 days [50]. Based on these findings, the present experiment was designed as follows: 30 females and 30 males (kept separated) were put in similar plastic boxes as above, and transferred randomly in three environmental chambers (PRY-450D, Ningbo Haishu Aifu Experimental Equipment Co. Ltd., Zhejiang, China). Each chamber was set with identical environmental parameters (humidity 70±5% RH, photoperiod L14:D10) except for temperatures that were set at 8, 6, 4°C in each chamber respectively. Individuals in the control group were kept in the insectary under same light and humidity conditions as above but at a temperature of 28°C. Thus, the experiment included four temperature treatments, resulting in a total number of beetles used = 30 individuals * 2 sexes * 4 treatments = 240 adults. After eight days at different temperatures, out of the 30 males and 30 females in each box, 6 males and 6 females were randomly chosen and placed by pair on individual potted plants to obtain 80 experimental eggs (the F1 generation/or progeny) per treatment (eggs were randomly collected from each pair resulting in 13–15 eggs per female/treatment). This whole procedure for obtaining the 80 experimental eggs was repeated 5 times to generate the independent replicates for each treatment (n = 5 replicates/treatment). For each treatment, all 80 eggs that were less than 12 hrs-old were placed in plastic basin (50×30 cm) and let emerge to obtain the larval stage. Larvae were maintained on A. artemisiifolia plants until pupation. Pupae were then detached from leaves, placed in an unsealed cuvette individually, and monitored daily until adult emergence. Survival rates and developmental period of the different developmental stages (egg, larval, pupae, and entire immature stage) were recorded.

Newly emerging adults were randomly sampled and paired by sex, and provided daily with fresh A. artemisiifolia leaves as oviposition substrate (N = 25 adult pairs per treatment and per replicate). All eggs laid on twigs were counted until the female died. Longevity of adult beetles was finally recorded.

Transgenerational Temperature Effect on Physiological Parameters Related to Cold Hardiness

To assess insect’s water content of progeny, 10 F1 adults of similar size and weight were randomly chosen from the treatments described above. Each beetle was weighed on an electronic balance (AB204-S, sensitivity ≤0.1 mg, Mettler Toledo, Greifensee, Switzerland) to determine its fresh weight (FW) before being placed in an oven at 70°C for 48 h and reweighed individually to obtain dry weight (DW), and then water content (WC) calculated as WC = (FW – DW)/FW×100%.

For measuring SCP, an additional 30 F1 adult beetles from each treatment were removed from ragweed plants and then starved for 12 h. Each adult beetle abdomen was fixed to a thermocouple that was attached to an automatic data recorder (uR100, Model 4152, Yokogawa Electric Co., Seoul, Korea) via a bridge. The thermocouple with the adult was then lowered into a freezing chamber at −25°C and the body temperature of the adult beetle was monitored as it decreased at a rate of about 1°C per minute from 28°C [30]. The SCP was taken to be the temperature recorded by the thermocouple just before the sudden increase in temperature caused by the emission of the latent heat of crystallization [51].

Finally, glycerol was measured from 5 male and 5 female F1 adult beetles from each treatment. The whole-body glycerol content of beetles was determined using an enzymatic assay (337-40A, Sigma Chemical Company, St. Louis, MO, USA) as in [38]. Briefly, twelve hours-starved individual adults were homogenized in 25 mM sodium phosphate buffer (pH 7.4) and then centrifuged at 12,000 g for 10 min at 25°C. The supernatant was then deproteinized with 6% (w/v) perchloric acid, and the protein precipitate that formed was removed by centrifugation (12,000 g for 5 min). The supernatant was then neutralized with 5 M potassium carbonate to pH 7.0. Glycerol levels were determined spectrophotometrically by measuring sample absorbance at 540 nm [52].

Statistical Analyses

We conducted one-way ANOVAs for testing temperature effect on survival rates and developmental durations of eggs, larvae, pupae, and the entire immature stage, as well as for the testing treatment effect on life-table parameters estimated as follow: 1) net reproductive rate ; 2) mean generation time ; 3) finite rate of increase λ = exp(r); where x is the age in days of the beetle; lx is the age-specific survival rate; mx is age-specific fecundity, and 4) the intrinsic rate of increase (r) estimated by using the Euler-Lotka formula with age indexed from 0 [53], [54], [55]. Overall, if stage differentiation was ignored, a single age-specific survival rate (lx) curve of progeny O. communa gave the probability that an egg will survive to age x in all treatments. The computer program TWOSEXMSChart was used to analyze the life history raw data [54], [56].

Two-way ANOVAs were conducted for testing the interactive effects of temperature, and gender on the survival rates, longevities and cold hardiness physiological parameters of O. communa adults. Prior to analyses, the developmental duration and the survival rates of insects were log10(x+1) and arcsine square-root-transformed, respectively, to meet normality assumptions. Student’s post-hoc analyses were performed to measure treatment differences [57].


Transgenerational Temperature Effect on O. communa Life-history Traits

Immature stage.

Overall, temperature experienced by parents did not affect development time of immature stages in the next generation (Table 1). However, temperature treatment strongly affected survival (Table 1, Fig. 1). In particular, the overall immature stage survived 8% worst when parents were placed at cold temperatures when compared to control 28°C (Fig. 1).

Figure 1. Transgenerational cold treatment induction on next generation O. communa immature stages survival (shown is average±1SE).

Parent beetles experienced cold temperatures (4, 6, 8°C), or normal room temperatures of 28°C for eight days prior mating. Different letters above bars mean significant differences (P<0.05, Tukey HSD post-hoc test).

Table 1. One-way ANOVAs for temperature treatment effect on O. communa development time and survival of each immature stage of the beetle life cycle (egg, larva, and pupa) and the entire immature stage.


After cold temperature treatment, adults in the next generation lived longer, with in average a 13% difference in longevity between the 4°C and the 28°C treatment (Table 2, Fig. 2A). Also, all adults descending from parents that experienced 28°C before mating survived (Fig. 2B). We also found temperature variation effect of parent beetles on the next generation female fecundity (Fig. 2C, F3,16 = 16.20, P<0.0001), with parents experiencing 4°C producing 21% more fecund females when compared to the average of the other treatments.

Figure 2. Transgenerational cold treatment induction on next generation O. communa A) development time, B) survival, and C) female fecundity (shown is average±1SE).

Parent beetles experienced cold temperatures (4, 6, 8°C), or normal room temperatures of 28°C for eight days prior mating. Different letters above bars mean significant differences (P<0.05, Tukey HSD post-hoc test).

Table 2. Two-way ANOVAs for effects of temperature treatment, and gender on O.communa next generation adult survival and longevity.

Life-table parameters.

Parents’ cold temperature experience significantly affected the net reproductive rates (R0) (F3,16 = 4254.35, P<0.0001), mean generation time (T) (F3,16 = 13.80, P<0.0001), finite increase rates (λ) (F3,16 = 16.36, P<0.0001), and intrinsic increase capacities (r) (F3,16 = 70.86, P<0.0001) of the progeny. Maximum r, R0 and λ-values were observed when parents experienced 4°C eight days of cold treatments. Mean generation time (T) had more idiosyncratic responses, with a maxima value when parents experienced 6°C.

Transgenerational Temperature Effect on O. communa Cold Hardiness and Physiological Traits

Parents experiencing cold temperatures influenced next generation adults’ physiological traits by increasing overall cold hardiness (Table 3, Fig. 3). Water content in progeny adult beetles was similar independent of cold treatments experienced by the parents (Table 3). On the other hand, cold treatment increased the glycerol content in insects with in average the three cold treatment together increasing glycerol levels by 32% in the next generation when compared to the 28°C treatment (Fig. 3A). Female beetles contain 24% more glycerol than males (Table 3). Insects that experienced colder temperatures had the lowest supercooling point (i.e. more negative temperatures) (Fig. 3B). We did not detect gender differences in supercooling point, although females had a slightly lower SCP than males (−13.57°C for females versus –12.85°C for males).

Figure 3. Transgenerational cold treatment induction of increased cold hardiness in O. communa.

Shown is A) average (±1SE) glycerol content, and B) supercooling point (SCP) of females (open bars) and males (grey bars) beetles when parents experienced cold temperatures (4, 6, 8°C), or normal room temperatures of 28°C. Different letters above bars mean significant differences (P<0.05, Tukey HSD post-hoc test).

Table 3. Two-way ANOVAs for effects of temperature treatment, and gender on O. communa next generation adult water content, glycerol content, and supercooling point (SCP).


With the present study we show that previous generation cold experience impact survival, longevity, fecundity and physiological parameters in the progeny beetles. Particularly, adult’s experience of cold temperatures decreased progeny overall survival, but resulted in an increased fecundity and longevity in the next generation adults. Additionally, we observed increased cold hardiness in the progeny, which was explained by the beetles’ increased body glycerol content, and lower supercooling point.

Insects living in temperate regions have to cope with low winter temperatures, which may strongly influence the establishment and persistence of perennial populations in the field [37], [38], [58]. In general, survival rates of insects decrease with decreasing temperatures [23], [25], [27], [59], and this phenomenon has been also observed in O. communa [17], [23], [42]. Many insect species are thus able to increase their over-wintering survival through increased cold hardiness during the pre-winter months [31], [43], [60], [61], [62], [63]. However, previous studies have only reported responses of the insects’ current generation to adverse low temperatures [23], [25], [27], [59]. Whether low temperature experience of insects can stimulate increased tolerance to cold in the next generation remained until now an open question.

Additionally, at low temperatures, resources of the insect are diverted into high-quality egg production, which, due to physiological trade-offs, result in overall reduced fecundity [64]. Subsequently, because high quality eggs impose an increase in the metabolic rates, females may additionally experience reduced longevity [13], [14], [15], [65], [66], [67]. Because previous studies explored only the effects of low temperatures on one generation, positive physiological adaptation transmitted to the next generation remained hidden. Indeed, as we report here, higher longevity and increased cold hardiness may be seen as counterbalancing adaptations against reduced survival in the next generation.

Insects in nature have evolved various physiological mechanisms to improve their cold-hardiness, and hence their survival under cold environments [35], [39], [40], [74], [75], [76], [77], [78]. Indeed, cold acclimation often results in insects accumulating reserves of glycogen that are subsequently broken down into glycerol during cold temperatures in order to improve their cold-hardiness [31], [79], [80], [81], [82]. Additionally, in insects, glycerol accumulation is often associated with both lower SCP and reduced water content [32], [33], [34], [83]. Thus, insects can often improve their cold hardiness via physiological changes meditated by cold acclimation [28], [35], [36]. Our experiments showed that higher levels of glycerol content point in the progeny is mediated by maternal and paternal cold environment, in which, the coldest temperatures trigger females to allocate higher levels of glycerol in the progeny. This results in bettles to have lower supercooling points when parents experienced colder temperatures. It has been demonstrated that cold hardiness, via changes in the relative composition of their body fluids and fats, is a plastic trait that can be influenced by fluctuations in abiotic factors (e.g., temperature) throughout the breeding season of O. communa [37], [38]. The present experiment is in line with the idea that O. communa has strong environmentally-driven phenotypic plasticity to cold adaptation, and this can be transmitted to the next generation. Future work will need to assess whether increase in cold hardiness as shown here finally results in increased survival when next generation beetles are placed at low temperatures.

Transgenerational or maternal effects in animals are common, contribute to the complexity of phenotypes’ deployment in the progeny [2], [3], [4], [9], and are thought to have strong ecological and evolutionary significance [2], [3], [5], [4], [9]. For example, in Drosophila melanogaster, cold exposure associated with variation in feeding regimes resulted in fewer, smaller offspring, and resulted in a male-biased sex ratio [21], [22]. Similarly, A different nutritional experience resulted in modified offspring survival and fecundity in the gypsy moth, Lymantria dispar [84]. In our study, although cold temperatures have a little effect on progeny O. communa larval survival, progeny of females that experienced the coldest temperatures (4°C for 8 days) could lay more eggs compared to control.

Ultimately, explaining such results requires understanding by which mechanisms parent beetles’ experience of different environments can influence the physiology of their offsprings. In plants, it has recently been shown that small interfering RNAs and phytohormones are needed to mediated transgenerational priming for increased resistance against biotic and abiotic stresses [6], [85], [86]. Future work is thus necessary for measuring iRNAs-mediated transgenerational effects in beetles [87].

Independently of the mechanisms behind the observed results, we believe that previous generation environmentally-induced cold hardiness in O. communa populations may be a mechanism for insects tracking host-plant expansion into colder climates.

Life table analysis is a good appraisal tool for estimating the dynamics of insects’ populations [42], [54], [55], and has been widely applied for comparing the development and expansion potential of an insect population under various environmental conditions [42], [68], [69], [70], [71], [72], [73]. For instance, higher population expansion potential has been associated with higher intrinsic capacity for increase (r), higher net reproductive rate (R0), and higher finite rate of increase (λ) (42,68,73). Our results show that the intrinsic capacity for increase (r), the net reproductive rate (R0) and the finite rate of increase (λ) of O. communa progeny revealed the highest values after parents experienced the low temperature treatments of 4°C for 8 days. This implies that the descendants of O. communa can inherit the potential to foster population expansion when their parent experience low temperatures, such as when following the northward range expansion of ragweeds.

Such studies are thus not only needed to improve knowledge of fundamental physiological processes, but are also needed to further improve biological control practices of noxious and biodiversity-threatening weeds worldwide.


We are very thankful to the anonymous reviewers whose appropriate commentary strengthened the manuscript. We are also very grateful to Prof. Alan Watson (Department of Plant Science, McGill University) to revise the English language of this manuscript. We thank Mr. Min Luo, Ms. Wei Guo and Dr. You-Zhi Li (Hunan Agricultural University), Mr. Xing-Wen Zheng, Mr. Yong-Xiang Fang and Ms. Hai-Yan Zheng (Jiangxi Agricultural University), and Prof. Yuan-Hua Luo (Institute of Plant Protection, Hunan Academy of Agricultural Sciences, Changsha, China) for their help during the experiment.

Author Contributions

Conceived and designed the experiments: ZSZ FHW. Performed the experiments: ML HSC ZSZ. Analyzed the data: ZSZ SR JYG. Wrote the paper: ZSZ SR FHW.


  1. 1. Bradshaw AD, McNeilly T (1991) Evolutionary response to global climatic change. Ann Bo 67: 5–14.
  2. 2. Bernardo J (1996) Maternal effects in animal ecology. Am Zool 36: 83–105.
  3. 3. Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13: 403–407.
  4. 4. Gibbs M, Breuker CJ, Hesketh H, Hails RS, van Dyck H (2010) Maternal effects, flight versus fecundity trade-offs, and offspring immune defence in the Speckled Wood butterfly, Pararge aegeria. BMC Evol Biol 10: 345–354.
  5. 5. Agrawal AA, Laforsch C, Tollrian R (1999) Transgenerational induction of defences in animals and plants. Nature 401: 60–63.
  6. 6. Rasmann S, De Vos M, Casteel C, Tian D, Sun JY, et al. (2012) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol 158: 854–863.
  7. 7. Marshall DJ, Keough MJ (2003) Effects of settler size and density on early post-settlement survival of Ciona intestinalis in the field. Mar Ecoly-Prog Ser 259: 139–144.
  8. 8. Marshall DJ, Keough MJ (2006) Complex life cycles and offspring provisioning in marine invertebrates. Integr Comp Biol 46: 643–651.
  9. 9. Mousseau TA, Dingle H (1991) Maternal effects in insect life histories. Ann Rev Entomol 36: 511–534.
  10. 10. Uçkan F, Gülel A (2001) The effects of cold storage on the adult longevity, fecundity and sex ratio of Apanteles galleriae Wilkinson (Hym.: Braconidae). Turk J Zool 25: 187–191.
  11. 11. Coulson SC, Bale JS (1992) Effect of rapid cold hardening on reproduction and survival of offspring in the housefly Musca domestica. J Insect Physiol 38: 421–424.
  12. 12. Irwin JT, Lee RE Jr (2000) Mild winter temperatures reduce survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae). J Insect Physiol 46: 655–661.
  13. 13. Roff DA (2002) Life History Evolution. Sunderland, Massachusetts, USA: Sinauer Associates, Inc.
  14. 14. Jervis MA, Boggs CL, Ferns PN (2005) Egg maturation strategy and its associated trade-offs: a synthesis focusing on Lepidoptera. Ecol Entomol 30: 359–375.
  15. 15. Jervis MA, Ferns PN, Boggs CL (2007) A trade-off between female lifespan and larval diet breadth at the interspecific level in Lepidoptera. Evol Ecol 21: 307–323.
  16. 16. Sharaf N, Batta Y (1996) Effect of temperature on life history of Eretmocerus mundus Mercet (Hymenoptera: Aphelinidae). Dirasat, Agric Sci 23: 214–219.
  17. 17. Luo M, Guo JY, Zhou ZS, Wan FH, Gao BD (2011) Effects of short-term low temperature stress on the development and fecundity of Ophraella communa LeSage (Coleoptera: Chrysomelidae). Acta Entomol Sin 54: 76–82.
  18. 18. Roff DA, Sokolovska N (2004) Extra-nuclear effects on growth and development in the sand cricket. J Evol Biol 17: 663–671.
  19. 19. Steigenga MJ, Fischer K (2007) Within- and between-generation effects of temperature on life-history traits in a butterfly. J Therm Biol 32: 396–405.
  20. 20. Chen WL, Leopold RA, Harris MO (2008) Cold storage effects on maternal and progeny quality of Gonatocerus ashmeadi Girault (Hymenoptera: Mymaridae). Biol Control 46: 122–132.
  21. 21. MacAlpine JLP, Marshall KE, Sinclair BJ (2011) The effects of CO2 and chronic cold exposure on fecundity of female Drosophila melanogaster. J Insect Physiol 57: 35–37.
  22. 22. Marshall KE, Sinclair BJ (2010) Repeated stress exposure results in a survivalreproduction trade-off in Drosophila melanogaster. P Roy Soc Lond B Bio 277: 963–969.
  23. 23. Huang Z, Ren SX, Musa PD (2008) Effects of temperature on development, survival, longevity, and fecundity of the Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) predator, Axinoscymnus cardilobus (Coleoptera: Coccinellidae). Biol Control 46: 209–215.
  24. 24. Chantarasa-Are S, Hirashima Y, Miura T (1984) Effects of temperature and food on the development and reproduction of Anagrus incarnates Haliday (Hymentoptera: Mymaridae), an egg parasitoid of the rice planthoppers. Esakia 22: 145–158.
  25. 25. Huffaker CB, Berryman A, Turchin P (1999) Dynamics and regulation of insect populations. In: Huffaker CB, Gutierrez AP, editors. Ecological Entomology, 2nd edn. New York: Wiley. 269–305.
  26. 26. Gilchrist GW, Huey RB (2001) Parental and developmental temperature effects on the thermal dependence of fitness in Drosophila melanogaster. Evolution 55: 209–214.
  27. 27. van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM (2006) Assession risks of releasing exotic biological control agents of arthropod pests. Ann Rev Entomol 51: 609–643.
  28. 28. Goto M, Li YP, Honma T (2001) Changes of diapause and cold hardiness in the Shonai ecotype larvae of the rice stem borer, Chilo suppressalis Walker (Lepidoptera: Pyralidae) during overwintering. Appl Entomol Zool 36: 323–328.
  29. 29. Sung DY, Kaplan F, Lee KJ, Guy CL (2003) Acquired tolerance to temperature extremes. Trends Plant Sci 8: 179–187.
  30. 30. Liu ZD, Gong PY, Wu KJ, Wei W, Sun JH, et al. (2007) Effects of larval host plants on over-wintering preparedness and survival of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). J Insect Physiol 53: 1016–1026.
  31. 31. Ishiguro S, Li YP, Nakano K, Tsumuki H, Goto M (2007) Seasonal changes in glycerol content and cold hardiness in two ecotypes of the rice stem borer, Chilo suppressalis, exposed to the environment in the Shonai district, Japan. J Insect Physiol 53: 392–397.
  32. 32. Holmstrup M, Costanzo J, Lee RE Jr (1999) Cryoprotective and osmotic responses to cold acclimation and freezing in freeze-tolerant and freeze-intolerant earthworms. J Comp Physiol B 169: 207–214.
  33. 33. Neven LG (1999) Cold hardiness adaptations of codling moth, Cydia pomonella. Cryobiology 38: 43–50.
  34. 34. Rivers DB, Lee RE Jr, Denlinger DL (2000) Cold hardiness of the fly pupal parasitoid Nasonia vitripennis is enhanced by its host Sarcophaga crassipalpis. J Insect Physiol 46: 99–106.
  35. 35. Wang HS, Kang L (2005) Effect of cooling rates on the cold hardiness and cryoprotectant profiles of locust eggs. Cryobiology 51: 220–229.
  36. 36. Terblanche JS, Sinclair BJ, Klok CJ, McFarlane ML, Chown SL (2005) The effects of acclimation on thermal tolerance, desiccation resistance and metabolic rate in Chirodica chalcoptera (Coleoptera: Chrysomelidae). J Insect Physiol 51: 1013–1023.
  37. 37. Zhou ZS, Guo JY, Li M, Ai HM, Wan FH (2011) Seasonal changes in cold hardiness of Ophraella commun. Entomol Exp Appl 140: 85–90.
  38. 38. Zhou ZS, Guo JY, Michaud JP, Li M, Wan FH (2011) Variation in cold hardiness among geographic populations of the ragweed beetle, Ophraella communa LeSage (Coleoptera: Chrysomelidae), a biological control agent of Ambrosia artemisiifolia L. (Asterales: Asteraceae), in China. Biol Invasions 13: 659–667.
  39. 39. Salt RW (1961) Principles of insect cold-hardiness. Ann Rev Entomol 6, 55–74.
  40. 40. Asahina E (1969) Frost resistance in insects. Adv Insect Physiol 6: 1–49.
  41. 41. Marshall DJ, Bolton TF, Keough MJ (2003) Offspring size affects the post-metamorphic performance of a colonial marine invertebrate. Ecology 84: 3131–3137.
  42. 42. Zhou ZS, Guo JY, Chen HS, Wan FH (2010) Effects of temperature on survival, development, longevity and fecundity of Ophraella communa (Coleoptera: Chrysomelidae), a biological control agent against invasive ragweed, Ambrosia artemisiifolia L. (Asterales: Asteraceae). Environ Entomol 39: 1021–1027.
  43. 43. Goeden RD, Ricker DW (1985) The life history of Ophraella notulata (F.) on Westhern California (Coleoptera: Chrysomelidae). Pan-pac Entomol 61: 32–37.
  44. 44. Palmer WA, Goeden RD (1991) The host range of Ophraella communa Lesage (Coleoptera: Chrysomelidae). Coleopts Bull 45: 115–120.
  45. 45. LeSage L (1986) A taxonomic monograph of the Nearctic Galerucine genus Ophraella Wilcox (Coleoptera: Chrysomelidae). Mem Entomol Soci Can 133: 1–75.
  46. 46. Teshler MP, Teshler I, DiTommaso A, Watson AK (2000) Inundative biological control of common ragweed (Ambrosia artemisiifolia) using Ophraella communa (Coleoptera: Chrysomelidae). Weed Sci Soci Am Abst 40: 29.
  47. 47. Teshler MP, DiTommaso A, Gagnon JA, Watson AK (2002) Ambrosia artemisiifolia L., common ragweed (Asteraceae). In: Mason PG, Huber JT, editors. Biological Control Programmes in Canada, 1981–2000. New York: CABI Publishing, Wallingford, UK. 290–294.
  48. 48. Wan FH, Liu WX, Ma J, Guo JY (2005) Ambrosia artemisiifolia and A. trifida. In: Wan FH, Zheng XB, Guo JY, editors. Biology and Management of Invasive Alien Species in Agriculture and Forestry. Beijing: Science Press, China. 662–688.
  49. 49. Agrawal AA (2001) Transgenerational consequences of plant responses to herbivory: An adaptive maternal effect? Am Nat 157: 555–569.
  50. 50. Zhou ZS, Guo JY, Wan FH, Chen HS, Peng ZP, et al. (2008) Impacts of low temperature storage on survival and fecundity of Ophraella communa Lesage (Coleoptera: Chrysomelidae). Chin J Biol Control 24: 376–378.
  51. 51. Wang HS, Zhou CS, Guo W, Kang L (2006) Thermoperiodic acclimations enhance cold hardiness of the eggs of the migratory locust. Cryobiology 53: 206–217.
  52. 52. Yoder JA, Benoit JB, Denlinger DL, Rivers DB (2006) Stress-induced accumulation of glycerol in the flesh fly, Sarcophaga bullata: Evidence indicating anti-desiccant and cryoprotectant functions of this polyol and a role for the brain in coordinating the response. J Insect Physiol 52: 202–214.
  53. 53. Goodman D (1982) Optimal life histories, optimal notation, and the value of reproductive value. Am Nat 119: 803–823.
  54. 54. Chi H, Liu H (1985) Two new methods for the study of insect population ecology. Bull Inst Zool Acad Sin 24: 225–240.
  55. 55. Chi H (1988) Life-table analysis incorporating both sexes and variable development rate among individuals. Environ Entomol 17: 26–34.
  56. 56. Chi H (2005) TWOSEX-MSChart: computer program for agestage, two-sex life table analysis. Taichung, Taiwan: National Chung Hsing University. (
  57. 57. SAS Institute (2004) SAS User’s® Guide: Statistics. Cary, NC: SAS Institute.
  58. 58. Rako L, Hoffmann AA (2006 ) Complexity of cold acclimation response in Drosophila melanogaster. J Insect Physiol 52: 94–104.
  59. 59. Daane KM, Malakar-Kuenen RD, Walton VM (2004) Temperature-dependent development of Anagyrus pseudococci (Hymenoptera: Encyrtidae) as a parasitoid of the vine mealybug, Planococcus Wcus (Homoptera: Pseudococcidae). Biol Control 31: 123–132.
  60. 60. Block W (1990) Cold tolerance of insects and other arthropods. Philos Trans R Soc Lond B Biol Sci 326: 613–633.
  61. 61. Montiel PO (1998) Profiles of soluble carbohydrates and their adaptive role in maritime Antarctic arthropods. Polar Biol 19: 250–256.
  62. 62. Block W, Convey P (2001) Seasonal variation in body-water content of an Antarctic springtail–a response to climate change? Polar Biol 24: 764–770.
  63. 63. Worland MR, Convey P (2008) The significance of the moult cycle to cold tolerance in the Antarctic collembolan Cryptopygus antarcticus. J Insect Physiol 54: 1281–1285.
  64. 64. Berger D, Walters R, Gotthard K (2008) What limits insect fecundity? Body size- and temperature-dependent egg maturation and oviposition in a butterfly. Funct Ecol 22: 523–529.
  65. 65. Papaj DR (2000) Ovarian dynamics and host use. Ann Rev Entomol 45: 423–448.
  66. 66. Carey JR (2001) Insect biodemography. Ann Rev Entomol 46: 79–110.
  67. 67. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85: 1771–1789.
  68. 68. Tanigoshi LK, McMurtry JA (1977) The dynamics of predation of Stethorus picopes (Coleoptera: Coccinellidae) and Typhlodromus floridanus on the prey Oligonychus punicae (Acarina: Phytoseiidae, Tetranychidae) I. Comparative life history and life table studies. Hilgardia 8: 237–288.
  69. 69. Kavous A, Chi H, Talebi K, Bandani A, Ashouri A, et al. (2009) Demographic Traits of Tetranychus urticae Koch (Acari: Tetranychidae) on Leaf Discs and Whole Leaves. J Econ Entomol 102: 595–601.
  70. 70. Inés SM, Elba SN, Samuel P, Chi H, Alicia R (2009) Impact of glyphosate on the development, fertility and demography of Chrysoperla externa (Neuroptera: Chrysopidae): Ecological Approach. Chemosphere 76: 1451–1455.
  71. 71. Farhadi R, Allahyari H, Chi H (2011) Life table and predation capacity of Hippodamia variegata (Coleoptera: Coccinellidae) feeding on Aphis fabae (Hemiptera: Aphididae). Biol Control 59: 83–89.
  72. 72. Huang YB, Chi H (2012) Age-stage, two-sex life tables of Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) with a discussion on the problem of applying female age-specific life tables to insect populations. Insect Sci 19: 263–273.
  73. 73. Jha RK, Chi H, Tang LC (2012) A comparison of artificial diet and hybrid sweet corn for the rearing of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) based on life table characteristics. Environ Entomol 41: 30–39.
  74. 74. Lee Jr RE (1991) Principles of insect low temperature tolerance.In: Lee Jr RE, Denlinger DL, editors. Insects at low temperature. New York: Chapman & Hall. 17–46.
  75. 75. Danks HV (1996) The wider integration of studies on insects cold-hardiness. Eur J Entomol 93: 383–403.
  76. 76. Sinclair BJ (1999) Insect cold tolerance: how many kinds of frozen? Eur J Entomol 96: 157–164.
  77. 77. Bale JS (2002) Insects and low temperatures: from molecular biology to distributions and abundance. Philos Trans R Soc Lond B Biol Sci 357: 849–862.
  78. 78. Costanzo JP, Humphreys T, Lee RE Jr, Moore JB, Lee MR, et al. (1998) Long-term reduction of cold hardiness following ingestion of icenucleating bacteria in the Colorado potato beetle, Leptinotarsa decemlineata. J Insect Physiol 44: 1173–1180.
  79. 79. Tsumuki H, Kanehisa K (1978) Carbohydrate content and oxygen uptake in larvae of rice stem borer, Chilo suppressalis Walker. Ber Ohara Inst Landwirt Biol Okayama Univ 17: 98–110.
  80. 80. Tsumuki H (1990) Environmental adaptations of the rice stem borer, Chilo suppressalis, and the blue alfalfa aphid, Acyrthosiphon kondoi, to seasonal fluctuations. In: Hoshi M, Yamashita O, editors. Advances in Invertebrate Reproduction, vol. 5. Amsterdam: Elsevier Science Publishers. 273–278.
  81. 81. Muise AM, Storey KB (1999) Regulation of glycogen synthetase in a freeze-avoiding insect: role in cryoprotectant glycerol synthesis. CryoLetters 20: 223–228.
  82. 82. Li YP, Ding L, Goto M (2002) Seasonal changes in glycerol content and enzyme activities in overwintering larvae of the Shonai ecotype of the rice stem borer, Chilo suppressalis Walker. Arch Insect Biochem Physiol 50: 53–61.
  83. 83. Nedvěd O, Lavy D, Verhoef HA (1998) Modelling the time-temperature relationship in cold injury and effect of high temperature interruptions on survival in a chill-sensitive collembolan. Funct Ecol 12: 816–824.
  84. 84. Diss AL, Kunkel JG, Montgomery ME, Leonard DE (1996) Effects of maternal nutrition and egg provisioning on parameters of larval hatch, survival and dispersal in the gypsy moth, Lymantria dispar L. Oecologia. 106: 470–477.
  85. 85. Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12: 133–139.
  86. 86. Luna E, Bruce TJA, Roberts MR, Flors V, Ton J (2012) Next generation systemic acquired resistance. Plant Physiol 158: 844–853.
  87. 87. Chitwood DH, Timmermans MCP (2010) Small RNAs are on the move. Nature 467: 415–419.