Ecological Mechanisms Of Migration And Re-emigration In Cnaphalocrocis Medinalis (Guenee)

The rice leaf roller, Cnaphalocrocis medinalis (Guenee), is one of the most serious pests in the Asian rice production and is confirmed to be a high-altitude nocturnal windborne migrant. The outbreak frequency of this species continued to increase in the whole China since 2003 and caused huge loss on rice production. It has been proved that the moths migrate annually from southern to northern areas in the spring and summer and then return to the southern areas in the autumn. However, the C. medinalis adults have strong re-emigratory flight capacity. Moreover, the migration process is composed of a series of night-time flights rather than one continuous flight. Moths usually land at dawn and emigrate in the following evening. All of these reasons made the complex aerial flight process of this pest. At present, the flight-oogenesis relationship in the process of re-emigration and its ecological and physiological mechanisms were not quite so clear-cut. So exact time parameters set in migratory phase were still unable to be determined. It is a real problem to accurately forecast the occurrence of C. medinalis compared with those species flying once only. Before trajectory analysis was widely used in C. medinalis, we always felt helpless to provide precise estimates for a middle or small-scale flight path and the forecasting on occurrence could just stay in the qualitative level at large scales.In the present study, the take-off behavior of caged C. medinalis both in field conditions and climate chamber were observed, and the effects of light intensity and ambient temperature on take-off proportion were investigated. Larval and adult developmental responses to crowding and food stress were analyzed. The re-emigratory flight performance and its relation to flight intensity, population characteristics, environmental factors and reproductive development were examined by tethered flight using computer-interfaced flight mills. The ecological mechanisms of taking-off, first migration and re-emigration were explored. These results may provide reliable parameters for trajectory analysis and help develop effective population monitoring and forecasting measures. The main results were summarized as follows:1. Take-off behavior of C. medinalis(1) The emigration peak period of C. medinalis in double-cropped early-season rice field in Yongfu, Guangxi were confirmed by systematic field surveys and female ovarian dissection in 2011. The take-off behavior, time, proportion and ovarian development of emigrants in the field of natural state were studied through large-size cage experiment. And its relation to environmental factors such as light intensity and weather condition (wind and rain) were also analyzed. The whole process of take-off behavior of C. medinalis occurred in 20-40 minutes after sunset and reached a peak period at the endiri’g of evening twilight. There were no individuals taking-off before sunset. The highest landing proportion in top area of the cage was observed. Heavy rain and wind at 2-3 grades could obviously reduce its take-off propensity. The ovarian development showed significant difference between emigrants and residents, which meant that the oogenesis-flight syndrome occurred in its first long distance migration.(2) Take-off behavior of C. medinalis was also observed with unmated females and males of 1 to 6-day-old in climate chamber. The relationships between take-off activity of emigrant and local breeding population, moth ages, sexes and environment factors were investigated. Simulated dusk and a self-developed observation device were used in this study. There was significant difference in flight frequency of virgin moths at different ages. The number of take-off was lowest during the first 24 hours after eclosion and reached peak period quickly at the second day. The emigrant population had a long pre-oviposition period for 7.6 days, which meant that C. medinalis had a long migrating period and their propensity and capacity to migrate could be maintained for a quite long time after eclosion. The local breeding population had significantly lower average take-off frequency than emigrant population, but it still occupied a certain proportion of emigrants. This result suggested that migration was the hereditary character of C. medinalis with species specificity, which would not be lost completely even under laboratory continuous breeding. A certain proportion of emigrants always existed in any field generation. Light intensity and ambient temperature had significant effects on flight and landing behavior of C. medinalis adults. Occurrence of the take-off behavior needed the triggering of optimum light intensity below 30 Ix, and the proportion of take-off reached a peak at the light density ranged from 0.1 to 1.0 1x. The ambient temperature suitable for take-off was ranged from 20℃ to 30℃ and the optimum temperature was 26.6℃. Take-off proportion reached a peak at 26℃ whereas a high temperature above 26℃ would inhibit take-off. There were no individuals taking-off at 10℃. The response of taking-off to ambient temperature was a bit different between females and males. A significantly higher proportion of females would take off at optimum temperature and illumination conditions compared with males during the first long distance migration. However, males showed higher take-off propensity when temperature was lower than 20℃ than females, indicating that low temperature threshold for take-off of males was lower than that of females.2. Effects of larval density and food stress on migration of C. medinalis adultsIt has been known that the temperature and photoperiod were the cues to trigger the migrating behavior of C. medinalis. However, the effect of food conditions on the migration of this insect is still unclear. In the present study, larval and adult developmental responses to crowding and food stress were investigated. The results showed that a high larval rearing density significantly reduced pupal mass, survival rate and female fecundity. Larvae developed rapidly under crowding conditions, and time to pupation was 2d earlier than individuals reared alone. By contrast, short-term starvation and associated compensatory growth prolonged larval development time by 3 d to 4 d and pupal development time by 1 d to 2 d. It also reduced the pupal mass, but showed no detectable effects on female reproductive performance. The effect of starvation treatment on larval development was highest in the 4L-36h group, followed by the 5L-36h,4L-24h and 5L-24h-groups. Both sexes had similar development strategies; however, females seemed to be more sensitive to crowding and food shortage than males. All treatments did not significantly increase female pre-oviposition period. Therefore, we concluded that life developmental responses to crowding and food shortage in this species were different. Adult migration propensity was not enhanced under such stress conditions during the larval phase.3. Re-emigratory flight performance of C. medinalisThe flight and re-migration performance of C. medinalis were examined by tethered flight using computer-interfaced flight mills in 2-d-old virgin females and males when taking-off behavior occurred for the first time. We investigated the nocturnally active flight rhythm. Effects of flight intensity on take-off proportion and re-migration times were analyzed. Flight and re-migration capacity of C. medinalis origin from field and laboratory populations were compared. The results showed that nocturnally flight activity of migratory individuals occurred throughout the 12 h scotophase and peaked at 4-6 h after artificial dusk. Flight duration for strong migratory type of moths at one night was 7.6 h and migratory type was 4.9 h. Re-migratory times and take-off proportion in the treatment of testing for 8 h every night were lower than that of 4 h treatment. There were significant differences in re-emigratory flight capacity between field and laboratory-reared insects. Strong re-migration propensity of field populations had been observed, which could fly for five successive nights on average, and nine nights maximum. Rearing for just one generation had no negative influence on their flight performance except the reduction in re-migration times, which had three successive flights on average and 6 maximum. But parameters included duration, distance, velocity and successive flight times were significantly decreased when insects were reared for two generations in laboratory. Most of the moths could fly for twice only. The long-duration flight behavior of unmated females was similar to that of unmated males under the flight patterns of low intensity. Their propensity and capacity to flight, however, were still different. Females showed better flight endurance and greater flight potentials than males under the flight patterns of high intensity. Longer wing-beating duration and higher flight willingness after midnight were performed in females in the first testing night. There were also significant differences in re-emigration times, take-off proportion and flight parameters between females and males flying for 4-6 nights and tested for 8 h every night.4. Effects of temperature on re-emigratory flight performance of C. medinalisAmbient temperature had a significant influence on re-emigratory flight behavior, although flight activities could be performed normally at all temperatures ranged from 20℃ to 29℃ and there were no significant differences in all measured flight parameters between females and males under the same treatment. Longest flight duration, fastest flight speed and greatest flight distance were performed at 26℃, as well as the highest take-off proportion and re-emigration times. Adults could fly for 3.42 successive nights on average and six nights maximum at 26℃. By contrast, most individuals could only complete a continuous flight for one night and could not take off for the second night under other three temperatures. Although re-emigration performance tested at 20℃ and 23℃ were similar as 29℃, different influences on flight behavior were observed. Flight velocity was greatly reduced at lower temperatures, while mortality rate of moths after successive passive flights at 29℃ was significantly higher than any other temperatures, showing that high temperature had greater impact on survival rate of moths and resulted in a long-duration flight than low temperature.5. Interrelationship between migration and reproduction in C. medinalisDaily flight muscle and ovarian development of virgin females were investigated by tethered flight and systematic dissection. We compared the re-emigratory flight performance between mated and unmated females. The interactions between flight and reproduction in the process of re-emigration were analyzed. The flight muscle histolysis did not take place after a series of night-time flights. The development of flight apparatus and reproductive system were synchronized in the process of re-migration. Effects of re-emigratory flight on reproduction of moths were strongly dependent on the flight duration. Continuous flight for 1 to 3 times significantly accelerated the ovarian development, and inhibitory effect appeared with the onset of the sixth flight. It is suggested that a short period of flight may stimulate the reproductive development, whereas passive flight to exhaustion incurs a reproductive cost caused by a prolonged pre-oviposition period, decreased mating percentage and frequency. Furthermore, mating status and oviposition did not seem to influence the re-emigratory flight performance. Together, we propose a new conceptual migratory model for this species based on the results of this and previous studies:The first long distance migration initiates in the stage when adults are sexually immature, however, ovarian development and flight are synchronized in the process of re-migration, showing the apparent absence of the oogenesis-flight syndrome. We hypothesize that C. medinalis may pursue mating during the migratory phase and oviposit a part of eggs en route.