Effects of constant and stage-specific-alternating temperature on the survival, development and reproduction of the oriental armyworm, Mythimna separata (Walker) (Lepidoptera: Noctuidae)

State Key Laboratory of Crop Stress Biology in Arid Areas/College of Plant Protection, Northwest A&F University, Yangling 712100, P.R.China

1. lntroduction

The oriental armyworm, Mythimna separata (Walker), is a typical migratory pest in Eastern Asia and some parts of Oceania (Farrow and McDonald 1987; Chen et al. 1995).Millet (Pennisetum spp.) and wheat (Triticum spp.) were recorded to suffer from this pest for thousands of years in China (Zou 1956). As a polyphagous species that can feed on host plants in sixteen families, M. separata prefer hosts in Gramineae, including the primary cereal crops such as wheat (Triticum aestivum L.), corn (Zea mays L.), and rice (Oryza sativa L.), as well as pastutes including wild oat (Avena fatua L.), crabgrass (Digitaria sanguinalis L.Scop.) and barnyard grass (Echinochloa crusgali L. Beauv.)(Lin 1990; Wang et al. 2006). Yearly seasonal roundtrip migration of M. separata in continuous generations across latitudes in China was confirmed by the outstanding mark and recapture study (Li et al. 1964), as well as subsequent radar observations and weather analyses (Chen et al.1995; Feng et al. 2008). Its powerful flight capability, high fecundity, and huge food consumption in the late larval instar stage makes outbreaks difficult to predict and prevent. The oriental armyworm has caused six nationwide disasters in China in the 1970s and has locally but severely outbroken in North and Northeast China in the 21th century (Jiang et al.2011; Zhang et al. 2012).

Insects have diverse adaptive strategies to escape from deteriorating habitats: dormancy (including quiescence and diapause) in the time scale and migration in the space scale (Southwood 1977; Sobreck 1978; McNeil et al. 1995;Chapman et al. 2015). External environmental factors including temperature can act as cues for migratory insects to change life history pathways (Jiang et al. 2011; Dingle 2014). Previous research revealed that high temperatures above 30°C at an immature stage decreased the survival,reproduction and flight capacity of M. separata (Jiang et al.1998, 2000), whereas temperatures below 20°C delayed the pre-calling period (between eclosion and sex-pheromone release) (Han and Gatehose 1991). Low temperature stress (5°C) in the first 24 h after eclosion changed oriental armyworms from migratory to resident mode (Zhang et al.2008). The lifetime of M. separata lasts roughly 40 to 120 d in the temperature range of 18 to 32°C (Li et al. 1992). Over the course of this time period, natural populations are likely to experience a marked abiotic environment changes. In addition, migratory insects were generally expected to evolved pre-emptive departure from habitats in response to changes in the environment before habitats became too serious (Dingle and Drake 2007; Dingle 2014). Thus, we predicted that insect migration initiation depends not only on temperature, but also on temperature variation trends.Previous research has mainly focused on the effects of constant temperature on insect biological parameters,whereas relatively limited information exists about the effects of fluctuating conditions.

The pupal stage is the period when larval tissues degrade and adult tissues are established (Dubrovsky 2005).Substances and energy for adult tissue construction in Noctuidae come from their accumulations in larval stage.Temperature in this stage is important for the development of M. separata, because it can influence the energy cost and allocation, which subsequently impact the survival,development, reproduction, and flight of M. separata in the adult stage.

Life tables provide comprehensive information about survival rates, developmental periods in different stages, and fecundity of female insects (Chi 1988). Previous research has used life table to study M. sepatara across different constant temperatures (Li et al. 1992). However, these traditional age-specific life table ignore the contribution of males to the population and stage overlap among individuals, which were reproduced during the same day but have different developmental rates (Chi and Liu 1985; Chi 1988). This limitation can be overcome by using age-stage, two-sex life table. In this study, such a life table was constructed for the armyworms reared at three different constant temperatures (20, 25 and 30°C),and three stage-specific-alternating temperatures (20–25,25–20 and 25–30°C) where insects received an increasing or decreasing temperature treatment starting at the pupal stage. This study expands our knowledge of the relationship between ambient temperature and oriental armyworm population development, and adaptive strategies in changing environment.

2. Materials and methods

2.1. lnsect rearing

Larvae of M. separata were collected from corn fields in Xingping, Shaanxi, China (34.28°N, 108.42°E) in early July, 2014. The population was then reared for over fifteen generations in a laboratory prior to conducting temperature experiments. Rearing conditions were set to a temperature of (25±1)°C, a photoperiod of 14 h L:10 h D, and a relative humidity (RH) of (75±10)% in growth chambers(MGC-450HP-2, Shanghai Yiheng Science Instruments Ltd., Shanghai). The parent generation was reared in transparent plastic cups (5.0 cm in diameter of bottom,6.5 cm in diameter of top and 8.0 cm in height). Larvae were reared on fresh wild oats (Avena fatua L.), a familiar gramineous grass. First to third instar larvae were reared in larger groups, whereas fourth to sixth instar larvae were reared with fewer than ten per cup. Mature larvae were transferred to new cups with peat soil covering the bottom for pupation. Sex was distinguished on 2-d-old pupae. Newly emerged adults were paired within 24 h after eclosion, and each pair was placed in a new plastic cup and covered with transparent plastic film with fine holes. Adults were fed with cotton balls soaked in a 5% honey solution and folded paper was supplied for oviposition. Eggs were collected daily from fifteen pairs and used for the life table study.

2.2. Temperature treatments

Twelve egg masses laid on folded paper within a 24 h period were randomly selected. In total, 99 to 108 eggs were transferred into five plastic cups for each temperature treatment. Three constant and three stage-specificalternating temperature treatments were: (I) 20°C all life span (20°C); (II) 20°C from egg to larval stage and 25°C from pupal to adult (20–25°C); (III) 25°C from egg to larval stage and 20°C from pupal to adult (25–20°C); (IV) 25°C all life span (25°C); (V) 25°C from egg to larval stage and 30°C from pupal to adult (25–30°C) and (VI) 30°C all life span(30°C). The humidity, photoperiod, food, and containers for rearing were the same as for their parents. The density of oriental armyworms was less than 20 per cup until third instar larval stage, and fewer than ten per cup from fourth instar larval stage to the pre-pupal period. All larvae were fed once each day, except sixth instar larvae which were fed twice to ensure sufficient food. They were examined daily to determine the instar stage until pupation. Pupae were observed to distinguish sex on the second day after pupation and examined daily. The pupae that turned dark in color and did not react to touch were considered dead. Larvae were examined daily to determine the instar stage until pupation.Armyworms of stage-specific-alternating treatments II, III and V were then transferred to another chamber with the appropriate temperature. In cases where a moth died after pairing, another young moth of the same sex was recruited from the same treatment. The data of recruited individuals were removed from life table analysis. Survival and fecundity were recorded daily until all individuals died.

2.3. Data analysis

Raw life table data were analyzed using the TWOSEXMSChart Program (Chi 2013), based on the theory and methods of age-stage, two-sex life table (Chi and Liu 1985;Chi 1988). The following parameters were calculated according to daily live individuals in different developmental stages and daily fecundity of females:

(1) Parameters of development: the developmental period in immature stage, adult pre-oviposition period (APOP) of female adult, total pre-oviposition period (TPOP) of female counted from birth, and oviposition period (OP);

(2) Parameters for survival: the age-stage-specific survival rate (sxj), and the age-specific survival rate (lx) (Chi 1988):

Where, x is age; j is developmental stage; n is initial number of eggs; nxjis number of lived individuals in age x,stage j; k is number of life stages;

(3) Parameters of reproduction: the age-stage-specific fecundity (fxj), and the age-specific fecundity (mx):

Where, fxjrepresents the number of offspring produced by adult females at age x, stage j;

(4) Parameters of population: the intrinsic rate of increase(r) was estimated by the Euler-Lotka formula with age indexed from 0 (Goodman 1982):

The net reproductive rate (R0), finite rate of increase (λ)and the mean generation time (T) were also calculated:

The age-stage-specific life expectancy (exj) represents the time that an individual of age x and stage j is expected to live:

Where, s′iyrepresents the probability that an individual of age x, stage j will survive to age i, stage y by assuming s′xj=1; age-stage-specific reproductive value (vxj) represents the contribution of individuals of age x and stage j to the future populations (Tuan et al. 2014):

Means and standard errors of duration periods from different treatments were statistically compared with oneway analysis of variance (ANOVA) and separated by the Tukey-Kramar test (P＜0.05) (Dunnett 1980) using SPSS Software (SPSS 17.0). Means and standard errors of APOP, TPOP, oviposition days and population parameters were calculated by using the bootstrap methods (Efron and Tibshirani 1994; Huang and Chi 2013) with 100 000 bootstraps. The differences of APOP, TPOP, OP, R0, T, r,and λ among temperature treatments were compared using the paired bootstrap test included in the TWOSEX-MSChart Program (Tuan et al. 2014).

3. Results

The durations of each stage, APOP, TPOP, oviposition days, and female fecundity are listed in Table 1. The duration of egg and larval stages decreased with increasing temperature. The pupal period under 20 and 25–20°C was significantly longer than that of 20–25 and 25°C, followedby 25–30 and 30°C. In higher temperatures, the duration of the pupal stage and/or the overall life span was shortened for both sexes. The longevity of females at 25–20°C was similar to that at 20°C, and the longevity of females at 20–25°C approached that at 25°C. No significant differences were found in the longevity of males at 20, 20–25, 25–20 and 25°C. The shortest APOP occurred at 25°C (2.69 d).Both low and high temperatures prolonged APOP. APOP of armyworms in 20°C beginning at the pupal stage (6.91 d) was similar to that of armyworms subjected to the constant 20°C treatment (7.48 d), and was significantly longer than those who experienced 20°C only prior to pupal stage (4.57 d).TPOP in different treatments decreased in the order of 20,25–20, 20–25, 25, 25–30 and 30°C, with the exception of 25 and 25–30°C where no significant differences were observed. Oviposition days were the shortest in 30°C (4.11 d), followed by 25–30°C (5.63 d), while no significant differences were observed among the other four treatments.

Table 1 Developmental duration and fecundity of Mythimna separata reared at different temperatures

The sxjcurves showed significant overlap between stages across all treatments (Fig. 1). The stage-specific survival rate curve (Fig. 2) shows that larval survival rates were higher at 25, 25–20 and 25–30°C, over 69% of the survival rate in the three temperature treatments developed into pupal stage. Those that experienced 20 or 30°C in egg and larval stage pupated less successfully with survival rate of 56–59%.

The lxcurves (simplified from sxj), the mxcurves and lxmxcurves of M. separata were shown in Fig. 3. Among the six treatments, the maximum mxunder 25°C occurred at age 38 days with a peak of 130.6 offspring. For the treatments of 25–20, 20–25 and 20°C, there were lower maximum mxvalues (98.7, 72.6 and 64.6 offspring, respectively) and later oviposition peaks (age 47, 49 and 57 d, respectively).However, for the treatments of 25–30 and 30°C, oviposition peak age was similar to that of 25°C (age 37 and 38 d,respectively), although the maximum mxwas lower (62.4 and 85.4 offspring, respectively).

The population parameters r and λ were the highest in 25°C, followed by that at 25°C in egg and larval stage and 30°C in pupal and adult stages. The lowest r and λ were observed at 20°C. The r and λ at 30°C were a little higher than that at 20°C with no significant difference. The R0was the highest at 25°C and the lowest at 30°C. In the other four treatments (20–25, 25–20, 25–30 and 20°C), R0was significantly higher than that at 30°C, and R0at 25–30 and 20°C was significantly lower than that at 25°C. The T declined with rising temperature (Table 2).

Fig. 1 Age-stage-specific survival rate (sxj) of Mythimna separata reared at different temperatures. A, 20°C. B, 20–25°C.C, 25–20°C. D, 25°C. E, 25–30°C. F, 30°C. 20, 25 and 30°C represent that M. separata was reared at 20, 25 and 30°C in all the developmental stages, respectively; 20–25, 25–20 and 25–30°C indicate that M. separata was reared at 20, 25 and 25°C before pupation, respectively, and then transferred to 25, 20 and 30°C after pupation, respectively. L1, L2, L3, L4, L5 and L6 represent 1st, 2nd, 3rd, 4th, 5th and 6th instar larvae, respectively.

The life expectancy at 30°C was much shorter than in other treatments and was the longest at 20°C. There was little difference in life expectancy between 25 and 25–30°C,as well as between 25–20 and 20–25°C, although shorter life expectancy was observed at 25 and 25–30°C (Fig. 4).The vxjincreased sharply when females began to lay eggs(Fig. 5). The adult peak vxjoccured at age 54 d (10 d after emergence) in 20°C and at age 45 d (9 d fter emergence)in 20–25°C, which were both later than all other treatments(averaging 6 to 7 d after emergence). The peak vxjin the adult stage was the highest in 25°C (890.8) and the lowest in 30°C (277.9).

4. Discussion

Fig. 2 Stage-specific survival rate of Mythimna separata reared at different temperatures. E, egg; L1–L6, 1st to 6th instar larvae; PP, pre-pupal; P, pupal; A, adult. 20, 25 and 30°C represent that M. separata was reared at 20, 25 and 30°C in all the developmental stages, respectively; 20–25, 25–20 and 25–30°C indicate that M. separata was reared at 20, 25 and 25°C before pupation, respectively, and then transferred to 25,20 and 30°C since pupation, respectively.

The developmental duration of M. separata in each preadult stage was temperature-dependent (Table 1), and declined with increasing temperature. This finding is in agreement with previous research in M. separata (Li et al.1992; Jiang et al. 1998) as well as in other two armyworm species, M. (Psedaletia) unipuncta (Guppy 1969) and M. convecta (Smith 1984). This finding may be attributed to a higher rate of metabolism under higher temperatures.The duration of the pupal stage in 25–20°C was the same as in 20°C, and the duration in 20–25°C was same as in 25°C, suggesting that the developmental duration of the pupal stage largely depends on temperature, at optimal or low optimal temperature treatments.

The sxjcurves (Fig. 1) evidently showed overlaps between stages as a result of the developmental rate differentiation among individuals, which were not present in the traditional lxcurves (Fig. 3). The survival rate was mainly affected by the temperature before pupation. Interestingly, relatively low numbers survived to third instar larval stage when eggs and larvae were reared at 20°C, while individuals reared at 30°C dramatically decreased after the pupal stage (Fig. 2).In a previous life table analysis of M. separata, the mortality before the fourth instar larval stage was higher at 16 and 20°C than in other treatments (Li et al. 1992), which was in agreement with our results. Insects have alternative life strategies to maximize their progeny in unstable fluctuating habitats, including: 1) grow faster to increase generations within specific seasonal period, and 2) eat more to amplify fecundity within a generation. In this study, oriental armyworms used the former strategy in high temperature treatments. However, they also faced rapid metabolism and a relatively short feeding period in the larval stage,which may have limited energy accumulation to support tissues reconstruction in the pupal stage and vitellogenesis in the adult stage. Since high juvenile mortality was previously found in result of nutritional stress at extreme high temperatures (Arendt 1997; Nylin and Gotthard 1998),we inferred that insufficient nutrition at 30°C may be the most important factor inducing high mortality of M. separata observed in the pupal stage, although older larvae rarely stopped feeding (day and night). The latter strategy was preferred by M. separata in low suitable temperatures. A larger fecundity required more nutrition accumulation in immature stages. As M. separata consumed the majority of food in the larval stage, especially in fifth and sixth instar larval stages (13.03 and 82.9% of total food intake,respectively) (Lin 1990), a longer larval period should have induced more eggs. However, longer development time seems to increase mortality prior to reproduction in many other insect species (Sibly and Atkinson 1994) resulting from higher risk of predation, pathogen infection or endocrine disorders (Nylin and Gotthard 1998). We thought endocrine disorders may be responsible for the relatively high mortality of M. separata before the third instar larval stage.

The APOP of M. separata was significantly influenced by temperature (Table 1). For the constant temperature treatments, both low and high temperatures delayed APOP.This phenomenon has been observed in many other noctuid migratory species (Fitt 1989). Low temperature lengthened precalling period of M. convecta, a relative species of M. separata endemic to Australia (Socorro and Gregg 1997). In pupalalternating temperature treatments, APOP of M. separata was largely determined by the temperature after pupation,and by the temperature through life time. In the studies of M. (Pseudaletia) unipuncta, a sibling species of M. separata in North America, declining temperature in either pupal or adult stages, and in both stages, delayed the pre-calling period of males (Turgeon and McNeil 1983; Delisle and McNeil 1987). It is difficult to determine whether individuals are residents or migrants by phenotype in holometabolic migratory insects (Dingle 2014). However, given that many insect species experience a temporary reproductive inhibition and that sex matured adults do not start migration,namely “oogenesis-flight syndrome”, APOP can provide a good indication of the time for migration (Han and Gatehouse 1991; Sappington and Showers 1992; Colvin and Gatehouse 1993). The oriental armyworm also corresponds“oogenesis-flight syndrome” (Jiang et al. 2011). Therefore,we suggest that the probability of migration tends to increase when M. separata experiences high or low temperatures,either before or after the pupal stage.

Fig. 3 Age-specific survival rate (lx), fecundity (mx), and net maternity (lxmx) of Mythimna separata reared at different temperatures.A, 20°C. B, 20–25°C. C, 25–20°C. D, 25°C. E, 25–30°C. F, 30°C. 20, 25 and 30°C represent that M. separata was reared at 20, 25 and 30°C in all the developmental stages, respectively; 20–25, 25–20 and 25–30°C indicate that M. separata was reared at 20, 25 and 25°C before pupation, respectively, and then transferred to 25, 20 and 30°C after pupation, respectively.

Table 2 Population parameters of Mythimna separata calculated by bootstrap methods reared at different temperatures

Fig. 4 Age-stage-specific life expectancy (exj) of Mythimna separata reared at different temperatures. A, 20°C. B, 20–25°C.C, 25–20°C. D, 25°C. E, 25–30°C. F, 30°C. 20, 25 and 30°C represent that M. separata was reared at 20, 25 and 30°C in all the developmental stages, respectively; 20–25, 25–20 and 25–30°C indicate that M. separata was reared at 20, 25 and 25°C before pupation, respectively, and transferred to 25, 20 and 30°C after pupation, respectively. L1, L2, L3, L4, L5 and L6 represent 1st,2nd, 3rd, 4th, 5th and 6th instar larvae, respectively.

Population parameters including r, λ and R0are generally employed to evaluate growth potentials across various environmental conditions (Tuan et al. 2014). Migratory insects are traditionally categorized as “r strategy” (Solbreck 1978), because of their spasmodic population outbreaks within a short period due in part to their remarkable fecundity and astonishing food intake, especially for many noctuids (e.g., Spodoptera, Myhimna) (Fitt 1989). The r and λ decreased when the oriental armyworms were reared under non-optimal temperature in some of or the whole developmental stages. When the ambient environment turned harsh, insects allocated more substance and energy to motor systems other than reproductive systems. In a single generation, migration reduces the number of offspring,while over the course of an entire year, migration results in major benefits, with subsequent generations continuously feeding and reproducing, and avoiding the risk of massive mortality under harsher environmental conditions (Chapman et al. 2012).

Fig. 5 Age-stage-specific reproductive value (vxj) of Mythimna separata reared at different temperatures. A, 20°C. B, 20–25°C.C, 25–20°C. D, 25°C. E, 25–30°C. F, 30°C. 20, 25 and 30°C represent that M. separata was reared at 20, 25 and 30°C in all the developmental stages, respectively; 20–25, 25–20 and 25–30°C indicate that M. separata was reared at 20, 25 and 25°C before pupation, respectively, and then transferred to 25, 20 and 30°C after pupation, respectively. L1, L2, L3, L4, L5 and L6 represent 1st, 2nd, 3rd, 4th, 5th and 6th instar larvae, respectively.

The oriental armyworms that leave a hot environment can benefit their offspring in the new living conditions at a cost of fecundity. Pervious experiments indicate that the production system of M. separata was more sensitive to high temperature than flight capacity. Reproduction was suppressed whereas flight capacity was not when temperatures increased to 27°C, while both were inhibited over 30°C (Jiang et al. 2000). These results coincided with the migration in spring and early summer in China: mature larvae or pupae of oriental armyworms overwinter in the area south of 33°N. The overwintered adults immigrate to Yangtzi-Huai River Plain in March–April so that the larvae of the first generation feed on winter wheat. Then adults of the first generation generally immigrate northward to the North and Northeast China in late-May to early-June so that the larvae of second generation damage summer corn in late-June to mid-July (Li et al. 1964; Chen et al. 1995; Jiang et al.2011). Mean temperature of July in Yangtzi-Huai River Basin exceeds 27°C, while that in northern Hebei, Liaoning and the southern Jilin Province is between 23 and 25°C (Domr?s and Peng 1988). If they stayed in thte Yangtzi-Huai River Basin,which was dominated by a subtropical high pressure belt of the northwest Pacific Ocean, the pupae would be unable to tolerant hot and dry climate. Without sufficient energy to support long-distance flight, adults would then fail to find new suitable habitats, as was inferred by our laboratory life table. Therefore, it is advantageous for M. separata to preemptively emigrate to North and Northeast China before the environment in the Yangtzi-Huai River Basin becomes too harsh with rising temperatures.

By comparing results of constant temperature and pupalalternating temperature, we found that the survival rate of the immature stage mainly depended on temperature before pupation. In addition, the pupal period was largely determined by temperature after pupation. APOP,fecundity and population parameters were all influenced by temperature both before and after pupation.

5. Conclusion

High temperature leads to massive mortality of pupae and severe inhibition of fecundity, while low suitable temperatures caused relatively high mortality before third instar larval stage in M. separata. Low or high temperatures after pupal stage, or throughout the entire lifespan delayed APOP and inhibited reproduction, which may increase the probability to initiate migration. This new comprehensive information from our age-stage, two-sex life table broadens the knowledge of adaptive strategies in M. separata to depart from detrimental habitats based on changing environmental cues.

Acknowledgements

This work was supported by the Special Fund for Agro-scientific Research in the Public Interest of China(201403031).

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