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10-2012 Comparison of Reproductive and Flight Capacity of sticticalis (: Pyralidae), Developing From Diapause and Non-Diapause Larvae Daosong Xie Chinese Academy of Agricultural Sciences

Lizhi Luo Chinese Academy of Agricultural Sciences

Thomas W. Sappington Iowa State University, [email protected]

Xingfu Jiang CFohilnloesew Ac thiadems andy of aAddgricituionlturalal Scienworkcess at: http://lib.dr.iastate.edu/ent_pubs Part of the Agriculture Commons, Sciences Commons, Biology Commons, Comparative aLeind Z Ehvaonlutg ionary Physiology Commons, Entomology Commons, and the Structural Biology Chommoninese Academs y of Agricultural Sciences The ompc lete bibliographic information for this item can be found at http://lib.dr.iastate.edu/ ent_pubs/197. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html.

This Article is brought to you for free and open access by the Entomology at Digital Repository @ Iowa State University. It has been accepted for inclusion in Entomology Publications by an authorized administrator of Digital Repository @ Iowa State University. For more information, please contact [email protected]. Comparison of Reproductive and Flight Capacity of (Lepidoptera: Pyralidae), Developing From Diapause and Non-Diapause Larvae Author(s): Daosong Xie, Lizhi Luo, Thomas W. Sappington, Xingfu Jiang, and Lei Zhang Source: Environmental Entomology, 41(5):1199-1207. 2012. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1603/EN11068 URL: http://www.bioone.org/doi/full/10.1603/EN11068

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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. PHYSIOLOGICAL ECOLOGY Comparison of Reproductive and Flight Capacity of Loxostege sticticalis (Lepidoptera: Pyralidae), Developing From Diapause and Non-Diapause Larvae

1,2 1,3 4 1,3 1 DAOSONG XIE, LIZHI LUO, THOMAS W. SAPPINGTON, XINGFU JIANG, AND LEI ZHANG

Environ. Entomol. 41(5): 1199Ð1207 (2012); DOI: http://dx.doi.org/10.1603/EN11068 ABSTRACT The beet webworm, Loxostege sticticalis (L.) (Lepidoptera: Pyralidae), uses both diapause and migration as life history strategies. To determine the role of diapause plays in the population dynamics of L. sticticalis, the reproductive and ßight potentials of adults originating from diapause and nondiapause larvae were investigated under controlled laboratory conditions. Preovi- position period, lifetime fecundity, and daily egg production of females originating from diapause larvae were not signiÞcantly different from those originating from nondiapause larvae, showing that diapause has no signiÞcant effect on reproductive capacity when adults are provided with an adequate carbohydrate source. However, females that developed from diapause larvae lived signiÞcantly longer than those from nondiapause larvae. Flight capacity, including ßight duration, distance and velocity of 3-d-old adults were all signiÞcantly greater in adults originating from diapause larvae than those from nondiapause larvae. L. sticticalis adults developing from diapause larvae tended to have more extreme values of longest ßight duration and furthest ßight distance than those from nondiapause larvae. Together, these results suggest that long-distance ßight potential of L. sticticalis is greater after larval diapause than after direct development to adulthood. However, there were no signiÞcant differences between sexes within the two categories of in terms of total ßight duration, total ßight distance, ßight velocity, and longest ßight duration.

KEY WORDS Loxostege sticticalis, diapause, reproduction, ßight

Diapause is a dynamic adaptation to arrest develop- between diapause and other life history traits (Roff ment at a speciÞc stage for a given species (Andrew- 1992). However, in a few species, diapause in an im- artha 1952; Dingle 1978; Tauber et al. 1986; Hodek mature stage is positively correlated with fecundity of 1996, 2002). As a distinct life history strategy, diapause the resultant adults (Spence 1989, Fantinou et al. 2004, enables the species to synchronize their life cycles to Wang et al. 2006b). the seasons and the host plants (Masaki 1980, Hodek Migration is also an important adaptation to tem- 2002), and plays an important role in population dy- porary habitat patches that vary in availability and namics. In addition, the effects of diapause on life quality both in space and time (Southwood 1977). By history traits after its termination may also inßuence determining where and when reproduction occurs, population dynamics of a species. For example, several migration has a major inßuence on adult Þtness. Mi- studies indicated that diapause may incur a cost. That gration is thus a fundamental component of the life is, individuals that have experienced diapause phase histories for migratory species and plays a key role in may have lower egg production, shorter adult longev- their population dynamics (Dingle 1984). However, ity, or both compared with individuals originated from effects of overwintering diapause of immature stages a nondiapausing population (Williams 1966, Gebre- on the subsequent ßight capacity of adults are poorly Amlak 1989, Ishihara and Shimada 1995, Kroon and understood at present. Evidence of research from Veenendaal 1998, Saunders 2000, Ellers and Van Al- Lepidoptera species (Van Dyck and Wiklund 2002, phen 2002). Such phenomena represent a trade-off Fric et al. 2006, Sarvary et al. 2008), suggesting that adults that experienced diapause as larvae may differ in ßight performance from those that developed di- 1 State Key Laboratory for Biology of Plant Diseases and rectly to adulthood. Therefore, investigation of the Pests; Institute of Plant Protection, Chinese Academy of Agricultural Sciences. Yuanmingyuan West Road, Beijing 100193, China. reproductive and ßight capacity of the postdiapause 2 College of Plant Science and Technology, Huazhong Agricultural population will be of great importance in fully under- University, Wuhan 430070, China. standing the population dynamics of relevant species. 3 Corresponding authors, e-mail: [email protected] and xfjiang@ The beet webworm, Loxostege sticticalis (L.) (Lep- ippcaas.cn. 4 USDA-ARS Corn and Crop Genetics Research Unit, Ge- idoptera: Pyralidae), which overwinters as a diapaus- netics Laboratory, Iowa State University, Ames, IA 50011. ing mature larva, is a serious economic pest of crops

0046-225X/12/1199Ð1207$04.00/0 ᭧ 2012 Entomological Society of America 1200 ENVIRONMENTAL ENTOMOLOGY Vol. 41, no. 5 and fodder within a belt zone from 36Њ Nto55Њ Nin Materials and Methods China (Pepper 1938, Knor et al. 1993, Luo 2004, Luo Insect Rearing. A laboratory population of L. stic- et al. 2009). Unlike other seasonal migrants, the beet ticalis was established by collecting diapausing larvae webworm can survive only in areas where the larvae from the Þeld in Siziwangqi (41Њ 53Ј N, 111Њ 70Ј E) of can enter diapause, because reproduction and distri- Inner Mongolia, China in 2008. Larvae were reared in bution of adult L. sticticalis are greatly limited by a climatic chamber (RXZ-430B; Ningbo, China) at temperature and precipitation (Pepper 1938). Larval 22 Ϯ 1ЊC, 70Ð80% RH, and a photoperiod of 16:8 (L:D) diapause is the only life history strategy that can carry h until pupation and adult emergence. Adults emerg- a population through the winter. Diapause of L. stic- ing on the same day were collected and kept together ticalis is regulated by both photoperiod and temper- in a 1.5-liter plastic cage for mating and oviposition. ature (Goryshin et al. 1980, Omelyuta 1981, Tian and Adults were provided with 10% glucose solution (wt: Gao 1986, Chen et al. 1987, Huang et al. 2009). The vol) as supplemental food, which was renewed daily, mature larva continues development under a photo- and their eggs were laid in the plastic cage on gauze. period of 16:8 (L:D) h, but enters diapause when the Ͻ Larvae were maintained in 500-ml beakers and fed photoperiod is 16 h. Temperature, food plant, and daily with fresh leaves of lambsquarters, Chenopodium larval density also have a signiÞcant effect on diapause album L. When larvae stopped feeding, sterilized soil rate of the mature larvae (Khomyakova et al. 1986, containing Ϸ10% water was added to the bottom of the Tian and Gao 1986, Knor et al. 1993). beakers to a depth of around 5 cm, which provided a Reproduction and migration are the biological char- substrate for cocoon formation, pupation, and adult acteristics of moths, which inßuence the occurrence emergence. and damage of the resultant populations. The beet Obtaining Diapause and Nondiapause Populations. webworm can complete two or three generations an- Insects of the parental generation were reared under nually in northern China (Luo and Li 1992, Luo and the above conditions of 16:8 (L:D) h at 22ЊC with fresh Qu 2005), but substantial economic damage is caused leaves of lambsquarters. Newly hatched larvae pro- mainly by Þrst-generation larvae, whose populations duced by these parents were reared at a density of 10 are directly affected by the fecundity of adults devel- larvae per 500-ml beaker and divided into two groups. oped from the diapausing larvae. Migration is then one To induce diapause, one group was kept in a climatic of the principal factors determining where outbreaks chamber at 22 Ϯ 1ЊC, 75% RH, and a photoperiod of of L. sticticalis occur. Evidence from behavioral char- 12:12 (L:D) h (light intensity during the photoperiod acterization of migratory movement (Chen et al. 1992, was Ϸ6,000 lux). Under these conditions, 98Ð100% of Luo and Li 1992, Feng et al. 2004, Sun and Gao 2004, mature larvae entered diapause (Huang et al. 2009). Cao et al. 2006); coupled with elucidation of migratory Diapausing larvae (Ϸ150) were placed in a refriger- routes (Sun and Chen 1995, Chen et al. 2004, Cao et ator and held at 0ЊC (BCD-261EA; Electrolux, China) al. 2006, Zhang et al. 2008); distance and causes (Sun for 5 mo to simulate winter Þeld conditions. They then and Chen 1995, Qu et al. 1999, Jiang et al. 2010a), were transferred to environmental chambers at 22 Ϯ indicate that the ßight potential of this long-range 1ЊC with a photoperiod of 16:8 (L:D) h until pupation migratory pest has an impact on areas, which are at risk and adult emergence. To obtain nondiapause larvae, of damage in a given year. Migration may occur when another group was maintained continuously in a the mass emergence period of overwintering adults is chamber at 22 Ϯ 1ЊC, 75% RH, and a photoperiod of not synchronized with host phenology at the over- 16:8 (L:D) h until pupation and adult emergence. wintering site (Chen and Yang 1999), but little is Determination of Reproductive Capacity. Newly known about the ßight activity of the overwintered emerged adults were paired in plastic cages (1.5 li- generation. Therefore, it is of great importance to ters). Each maleÐfemale pair comprising a replicate compare reproductive and ßight capacity of adults was provided with a 10% glucose solution (wt: vol). originating from diapause and nondiapause larvae, Twenty-Þve and 24 pairs of adults originating from which helps to understand the role of diapause in diapause and nondiapause larvae, respectively, were population dynamics. kept in a chamber under 122ЊC, 75% RH, and a pho- In the current study, we tested the hypothesis that toperiod of 16:8 (L:D) h. Preoviposition period, ovi- costs are associated with diapause in L. sticticalis, position period, mean lifetime egg production, mean which provides an excellent experimental model to daily egg production per female, and the longevity of investigate the inßuences of diapause on future re- females and males were recorded. Data were excluded production and migration. The effects of diapause from the analyses if either males or females escaped on reproduction and ßight capacity of L. sticticalis during the experiment. The experiments were termi- of the overwintered generation were measured un- nated when all of the males and females had died. der laboratory conditions, and ßight performance of Determination of Flight Potential. Flight activity of males and females derived from diapause and non- L. sticticalis originating from diapause and nondia- diapause larvae were investigated. This information pause larvae was monitored by a computer-aided is essential to the development of a theoretical foun- ßight information system (Jiaduo Science, Industry dation for managing overwintering populations and and Trade Co., Henan, China), as described in previ- for improving forecasts of the population dynamics ous studies (Luo and Li 1992, Luo et al. 2002). Flight of this pest. tests were conducted on a 24-channel ßight mill sys- October 2012 XIE ET AL.: REPRODUCTION AND FLIGHT POTENTIAL FOR L. sticticalis 1201

Fig. 1. Comparison of longevity of L. sticticalis adults originating from diapause and nondiapause larvae at 22ЊC, 75% RH, and a photoperiod of 16:8 (L:D) h. Sample sizes for adults originating from diapause and nondiapause larvae were 22 and 24 pairs, respectively. Data are presented as means Ϯ SE. Asterisk indicates means for females originating from diapause and nondiapause larvae differed signiÞcantly (t-test, *P Ͻ 0.05). tem. The ßight mill arm was made of a special alloy average velocity, longest ßight duration, and furthest wire (0.03 cm in diameter, 15 cm long) and mounted ßight distance were recorded automatically by the to permit horizontal revolutions with very little fric- system. Longest ßight duration and furthest ßight dis- tion by using magnetic suspension. tance were those of the single longest uninterrupted Three-day-old unmated females and males originat- ßight. ing from diapause or nondiapause larvae were selected Data Analysis. All data were checked for Þt to a for testing, because 1- and 2-d-old adults exhibit lower normal distribution by using the KolmogorovÐSmir- ßight activity (Luo and Li 1992). Test moths with nov test, implemented in SPSS 11.0 (SPSS 1999). The forewing lengths ranged from 2.2 to 2.6 cm were se- reproductive and ßight parameters of adults originat- lected for the experiments and tethered. To facilitate ing from diapause and nondiapause larvae were mea- attachment of tethers, the adults were lightly anes- sured by independent-samples t-test. All values ob- thetized for 4Ð5 s by placing each inside a glass tube tained from the studies are presented as means Ϯ SE. (1.5 by 7 cm) containing an ether-soaked cotton wick. The differences of the ßight parameters were ana- The tether consisted of an alloy wire with a 1-mm lyzed further by comparing the frequency distribution (diameter) loop at one end and a 1.5-mm straight of longest ßight duration and furthest ßight distance portion of wire perpendicular to the loop. The loop between the two categories of moths by using a pro- was attached to the mesothorax with 502 superglue cedure for two sample t-test between percents avail- (Chuanghui Adhesive Co., Shenzhen, China) after the able at https://www.statpac.com/statistics-calculator/ scales and hairs at the attachment site were removed percents.htm#D2HTopicM13. with a soft brush. The anesthesia, measurement of wings, and tethering the moths took place in light. Results After tethering, the moths were subjected to 60 min acclimatization to the darkness, transferred to a dark Reproductive Capacity. There were no signiÞcant climate-control chamber and attached to the ßight differences in the preoviposition period (t ϭ 1.000, mill arm. The tests were performed in darkness, at 20 Ϯ df ϭ 44, P ϭ 0.323); oviposition period (t ϭ 0.382, df ϭ 1ЊC and 70Ð80% RH, conditions promoting maximum 44, P ϭ 0.704); lifetime egg production per female (t ϭ ßight capacity of L. sticticalis (Luo and Li 1992). Data 0.376, df ϭ 44, P ϭ 0.709); mean daily egg production were recorded from 1930 to 0730 hours of local time, per female (t ϭ 0.442, df ϭ 44, P ϭ 0.661); and the the time corresponding to the period of mass ßight of longevity of males (t ϭ 0.681, df ϭ 44, P ϭ 0.500; Fig. L. sticticalis in the Þeld (Feng at al. 2004). Approxi- 1) among adults originating from diapause or nondia- mately 60 adults were observed for each treatment. pause larvae. However, longevity of female adults Adults were excluded from the data analyses if they originating from diapause larvae was signiÞcantly lon- were found detached from the tether or with a broken ger than that of female adults from nondiapause larvae wing after the test period. In addition, data from moths (t ϭ 2.308, df ϭ 44, P ϭ 0.026; Fig. 1) under laboratory with total ßight duration Ͻ30 min were discarded, conditions. because it is possible that low ßight activity is an Flight Potential. Data from adults originating from artifact of handling or trauma during the tethering diapause and nondiapause larvae were examined by process. gender. There were no signiÞcant differences be- Flight capacity of L. sticticalis was characterized tween males and females in total ßight duration (dia- using the standards of Luo et al. (2002). Flight pa- pause: t ϭ 0.326, df ϭ 43, P ϭ 0.746; nondiapause: t ϭ rameters, including total ßight duration and distance, 0.580, df ϭ 38, P ϭ 0.566); total ßight distance (dia- 1202 ENVIRONMENTAL ENTOMOLOGY Vol. 41, no. 5

Table 1. Flight capacity parameters of 3-d-old L. sticticalis developing from diapause and nondiapause larvae during a 12-h tethered-flight test

No. of Total ßight Total ßight Flight Longest ßight Origin Gender individuals duration (h) distance (km) velocity (km/h) duration (h) Adults developing from diapause larvae Female 25 7.74 Ϯ 0.63 27.09 Ϯ 3.16 3.36 Ϯ 0.20 4.60 Ϯ 0.64 Male 20 8.05 Ϯ 0.72 27.14 Ϯ 3.14 3.21 Ϯ 0.22 5.82 Ϯ 0.65 Adults developing from nondiapause larvae Female 19 5.62 Ϯ 0.74 12.68 Ϯ 2.91 2.67 Ϯ 0.19 2.83 Ϯ 0.41 Male 21 6.26 Ϯ 0.79 17.58 Ϯ 3.00 2.56 Ϯ 0.19 2.64 Ϯ 0.43

There were no signiÞcant differences between sexes within origin for any of the parameters measured (P Ͼ 0.05) as determined by independent-samples t-test. Data are presented as means Ϯ SE. pause: t ϭ 0.010, df ϭ 43, P ϭ 0.992; nondiapause: t ϭ diapause and nondiapause larvae (Fig. 2). Adults orig- 0.279, df ϭ 38, P ϭ 0.782); average ßight velocity inating from diapause larvae showed signiÞcantly (diapause: t ϭ 0.497, df ϭ 43, P ϭ 0.622; nondiapause: greater total ßight duration (t ϭ 2.696, df ϭ 83, P ϭ t ϭ 0.415, df ϭ 38, P ϭ 0.680); and longest ßight 0.008; Fig. 2A); total ßight distance (t ϭ 3.298, df ϭ 83, duration (diapause: t ϭ 1.325, df ϭ 43, P ϭ 0.192; P ϭ 0.001; Fig. 2B); and velocity (t ϭ 3.457, df ϭ 83, nondiapause: t ϭ 0.310, df ϭ 38, P ϭ 0.759) (Table 1). P ϭ 0.001; Fig. 2C). These differences were analyzed Therefore, male and female data were pooled for sub- further by comparing the frequency distribution of sequent analyses. longest ßight duration and furthest ßight distance be- SigniÞcant differences were observed in ßight po- tween the two categories of moths (Fig. 3). A large tential between adult L. sticticalis developing from proportion of adults originating from diapause larvae

Fig. 2. Total ßight duration (A), total ßight distance (B), and mean ßight velocity (C) of 3-d-old L. sticticalis adults during a 12-h tethered-ßight test. Sample sizes for ßight treatments of adults originating from nondiapause and diapause larvae were 40 and 45, respectively. Data are presented as means Ϯ SE. Asterisks indicate means are signiÞcantly different (t-test, **P Ͻ 0.01). October 2012 XIE ET AL.: REPRODUCTION AND FLIGHT POTENTIAL FOR L. sticticalis 1203

Fig. 3. Frequency (percentage) distribution of longest ßight duration (A) and furthest ßight distance (B) of 3-d-old L. sticticalis during a 12-h ßight mill test. Sample sizes for ßight treatments of adults originating from nondiapause and diapause larvae were 40 and 45, respectively. Asterisks indicate percentage are signiÞcantly different (t-test, *P Ͻ 0.05).

(n ϭ 45) engaged in long-duration ßight, with 73.3 and tween the percents of adults that ßew Ͼ3h(t ϭ 3.101, 40%, making a continuous ßight Ͼ3 h and Ͼ5h,re- df ϭ 83, P ϭ 0.003) and Ͼ5h(t ϭ 3.468, df ϭ 83, P ϭ spectively, during the 12-h test period (Fig. 3A). In 0.008) originating from diapause and nondiapause lar- contrast, only 40 and 7.5% of adults originating from vae, respectively. Only 6.7% of adults originating from nondiapause larvae (n ϭ 40) ßew Ͼ3 h and Ͼ5h, diapause larvae did not make a long-duration ßight Ͼ1 respectively. Only 6.7% of adults originating from dia- h, whereas 20% of adults originating from nondiapause pause larvae did not make a long-duration ßight Ͼ1h, larvae ßew Յ1 h, although the difference is no signif- whereas 20% of adults originating from nondiapause icant (t ϭ 1.822, df ϭ 83, P ϭ 0.072). Similarly, L. larvae ßew Յ1 h. Similarly, L. sticticalis adults devel- sticticalis adults developing from diapause larvae oping from diapause larvae tended to have more ex- tended to have signiÞcantly more extreme values of treme values of furthest single ßight distance than furthest single ßight distance than those from non- those from nondiapause larvae (Fig. 3B), with 51.1% diapause larvae (Fig. 3B), with 51.1% versus 27.5%, versus 27.5%, respectively, ßying Ͼ16 km. Therefore, respectively, ßying Ͼ16 km (t ϭ 2.217, df ϭ 83, P ϭ although adults of both groups were capable of long- 0.029). Therefore, although adults of both groups duration and long-distance ßights, those originating were capable of long-duration and long-distance from diapause larvae displayed greater ßight potential ßights, those adults originating from diapause larvae on the ßight mill system. These differences were an- displayed greater ßight potential on the ßight mill alyzed further by comparing the frequency distribu- system. tion of longest ßight duration and furthest ßight dis- tance between the two categories of moths (Fig. 3). A Discussion large proportion of adults originating from diapause larvae (n ϭ 45) engaged in long-duration ßight, with For some insects, diapause has a negative effect on 73.3 and 40%, making a continuous ßight Ͼ3 h and Ͼ5 postdiapause adult life-history traits. In a multivotine h, respectively, during the 12-h test period (Fig. 3A). bruchid, Kytorhinus sharpianus Bridwell, fecundity of In contrast, only 40 and 7.5% of adults originating from postdiapause females is less than that of females that nondiapause larvae (n ϭ 40) ßew Ͼ3 h and Ͼ5h, developed from nondiapause larvae (Ishihara and Shi- respectively. There were signiÞcant differences be- mada 1995). In the spider mite, Tetranychus urticae 1204 ENVIRONMENTAL ENTOMOLOGY Vol. 41, no. 5

Koch, there is a negative correlation between dia- L. sticticalis. In contrast to our results, Jiang et al. pause duration and postdiapause reproduction (lon- (2010b) found that diapause did incur a cost in this gevity, total egg production, average oviposition rate) species, in the form of prolonged preoviposition and (Kroon and Veenendaal 1998). In the parasitoid wasp, oviposition periods, and reduced fecundity. Postdia- Asobara tabida Nees, individuals that experienced dia- pause conditions in their study were not different pause have lower fecundity and higher mortality than than ours, except that adults were provided with a those that developed directly (Ellers and Van Alphen 5% glucose solution, whereas adults in the current 2002). Such negative correlations between diapause study were provided with a 10% glucose solution. and reproduction are often explainable by the partial The implication is that energy depletion during lar- depletion of metabolic reserves, which play an impor- val diapause can be compensated through adequate tant role in diapause in many overwintering insects supplemental food intake as an adult. Therefore, the (Tauber et al. 1986, Danks 1987). Although diapause reproductive potential of L. sticticalis may be de- typically is characterized by decreased respiratory termined by both the amount of energy expended metabolism (Danks 1987, Guppy and Withers 1999), a during diapause and energy intake after adult emer- low metabolic rate can draw heavily on nutrient re- gence, but further studies are needed to verify this. serves (Tauber et al. 1986). The beet webworm is a long-distance migratory However, not all species show diapause-associated insect, and the ßight capacity of diapause- and non- costs in successive life history traits. For example, in diapause-derived moths was tested on ßight mills. In the Colorado potato beetle, Leptinotarsa decemlineata addition to measuring total ßight duration, total dis- (Say), females that experience diapause show no ap- tance, and mean velocity, the longest ßight duration is parent reduction in fecundity (Peferoen et al. 1981, used as the major criterion to measure ßight potential Jansson et al. 1989, Ferro et al. 1991). Diapause even of L. sticticalis in this study. The furthest ßight distance has been associated with greater fecundity in the is also considered as a secondary parameter, which is grasshopper Tetrix undulata (Sow.) (Poras 1976); Gra- determined by both ßight duration and ßight velocity. pholitha funebrana Tr. (Saringer and Szentkiralyi Distances measured on ßight mills will underestimate 1980); four pond skater species, Gerris buenoi actual migratory ßight distance in the Þeld, because of Kirkaldy, Gerris comatus Drake and Hottes, Gerris the drag of the ßight arm and absence of wind that can pingreensis Drake and Hottes, and Limnoporus dissor- affect velocity greatly. Flight velocity itself, although tis Drake and Harris (Spence 1989); and cabbage bee- it contributes to distance ßown, may not be a good tle Colaphellus bowringi Baly (Wang et al. 2006b). In index of ßight potential unless it is accompanied by the goldenrod gall ßy E. solidaginis, larvae exposed to long ßight duration (Luo and Li 1992; Luo et al. 1995, cold winter microenvironments had higher survival 2002). rates and postdiapause fecundity (Irwin and Lee 2002, Results obtained in this study showed that diapause 2003). The duration of diapause is also positively cor- had a positive effect on the migratory ßight potential related with fecundity in the corn stalk borer Sesamia of L. sticticalis. This may be related to increased ca- nonagrioides (Fantinou et al. 2004). pacity, increased propensity to engage in ßight, or The relationship between diapause and reproduc- both. The signiÞcant increase in velocity of adults tion was estimated in L. sticticalis. Mean total egg derived from diapause larvae suggests a possible in- production and daily egg production of the females crease in capacity itself. Findings of enhanced ßight derived from diapause larvae were similar to those of potential in diapause-derived individuals have been females originating from nondiapause larvae. More- found in some other insects, such as Colorado potato over, adults originating from diapause larvae did not beetle, Leptinotarsa decemlineata (Say) (Weber and differ signiÞcantly in preoviposition and oviposition Ferro 1996) and diamondback , Plutella xylostella periods from adults derived from nondiapause larvae. (L.) (Shirai 1991). Although sex-related differences in Together, our results revealed no sublethal effects of ßight potential have been observed in some noctuids diapause on reproductive capacity or longevity. (Sharp et al. 1975, Parker and Gatehouse 1985, Sap- Among cold-tolerant insect species, low tempera- pington and Showers 1991) and other Lepidoptera tures during diapause may promote signiÞcant ener- (Dorhout et al. 2008), at least at certain ages, there getic savings (Irwin and Lee 2002, 2003). The over- were no obvious differences between male and female wintering sites of L. sticticalis are generally located in L. sticticalis at3dofageunder controlled laboratory northern areas of China around 36Њ N, where mild conditions. winter temperatures are typically below 0ЊC but can Unlike many other insects, the beet webworm pos- reach even lower than Ϫ20ЊC. Thus, low overwinter- sesses both the option to diapause and to engage in ing temperatures may reduce the energetic costs of long-distance migration, which constitutes consider- diapause. Reduced cost of diapause at low tempera- able life-history ßexibility in distributing its offspring tures has been conÞrmed in Eurosta solidaginis over space and time. Even though our results show (Fitch) (Irwin and Lee 2002, 2003) and Diplolepis that diapause enhances ßight potential in L. sticticalis, spinosa (Ashmead) (Williams et al. 2003), although we also found that long ßights are not uncommon in the effect of low temperature on diapause mainte- adults with a nondiapause larval history. Furthermore, nance is less well understood. some adults with a diapause larval history did not However, the relationship between diapause and make long ßights. Thus, these two life-history strate- reproductive costs may not be so simple in the case of gies are not coupled in an obligate way, but both are October 2012 XIE ET AL.: REPRODUCTION AND FLIGHT POTENTIAL FOR L. sticticalis 1205 available to each individual as potential options. Both photoperiod and temperature on development and dia- strategies can be used to avoid adverse conditions pause. Acta Phytophyl. Sin. 14: 253Ð258. when environmental risks warrant. Diapause in this Chen, X., J. G. Chen, Y. Xue, L. P. Hao, Y. Zhang, and K. J. species represents primarily an adaptation to survive Zhao. 2004. Immigration of the 1999 outbreak popula- cold winters. Migration seems to be an adaptation to tions of the meadow moth, Loxostege sticticalis L. (Lep- exploit ephemeral oviposition sites in suitable envi- idoptera: Pyralidae) into the northeastern part of China. ronments. In spring, the beet webworm migrates long Acta Entomol. Sin. 47: 599Ð606. Chen, Y. B., and L. W. Yang. 1999. Studies on migration of distances from overwintering areas on the wind. The beet webworm. Inner Mongolia Agric. Sci. Technol. 6: increased longevity of female adults originating from 36Ð41. a diapause population (Jiang et al. 2010b, Fig. 1E this Danks, H. V. 1987. Insect dormancy: an ecological perspec- study) helps ensure that they have enough time for tive. Biological Survey of Canada (Terrestrial Arthro- both migration and reproduction. Great ßight ca- pods), Ottawa, Canada. pacity minimizes reproductive risk by making it Dingle, H. 1978. Migration and diapause in tropical, tem- easier to Þnd oviposition sites and concentrate egg perate, and island milkweed bugs, pp. 254Ð276. In H. production in a short period just after cessation of Dingle (ed.), Evolution of insect migration and diapause. migration. Springer, New York. In conclusion, the effect of diapause on postdia- Dingle, H. 1984. Behaviour, genes and life histories: com- pause Þtness, where female fecundity is traded off for plex adaptations in uncertain environments, pp. 169Ð194. survival of adverse conditions via diapause, appears to In P. W. Price, C. N. Slobodchikoff, and W. S. Gaud (eds.), A new ecologyÐnovel approaches to interactive systems. be mitigated in L. sticticalis by adequate energy intake Wiley, New York. by adults. Supplemental carbohydrates from nectar Dorhout, D. L., T. W. Sappington, L. C. Lewis, and M. E. feeding by adults facilitates migration in the oriental Rice. 2008. Flight behaviour of European corn borer armyworm, Mythimna separata (Walker) (Wang et al. infected with Nosema pyrausta. J. Appl. Entomol. 135: 2006a), and may inßuence migratory capacity in L. 25Ð37. sticticalis. The reason for enhanced migratory capacity Ellers, J., and J.J.M. Van Alphen. 2002. A trade-off between in postdiapause adults is unclear, although it may re- diapause duration and Þtness in female parasitoids. Ecol. ßect a predictable lack of suitable habitat in overwin- Entomol. 27: 279Ð284. tering areas in the early spring. Although factors con- Fantinou, A. A., D.C.H. Perdikis, and K. F. Zota. 2004. Re- trolling diapause have been explored for this species productive responses to photoperiod and temperature by (Jiang et al. 2010b), further research is needed to diapausing and nondiapausing populations of Sesamia elucidate the factors inßuencing the decision to mi- nonagrioides Lef. 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