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Influence of number of eggs oviposited on (A) flight distance, (B) flight velocity, and (C) flight duration of mated female beet webworms on flight mills. (A) Linear regression of flight parameters (Y) on the number of eggs laid (X) by mated females: Y = 30.30–0.066 X, t = -4.60, P < 0.0001, n = 111; (B) Y = 3.01–0.005 X, t = -4,24, P < 0.0001, n = 111; (C) Y = 9.84–0.02 X, t = -4.60, P < 0.0001, n = 111. doi:10.1371/journal.pone.0166859.g001
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Flight and reproduction are usually considered as two life history traits that compete for resources in a migratory insect. The beet webworm, Loxostege sticticalis L., manages the costs of migratory flight and reproduction through a trade-off in timing of these two life history traits, where migratory behavior occurs during the preoviposition perio...
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... Beet webworm is generally considered as a dangerous agricultural pest, similar to the migratory locust Locusta migratoria L. [2]. The cyclical phenomenon of beet webworm outbreaks has attracted the attention of researchers [3][4][5]. However, the overwintering pattern of beet webworm and the mechanisms involved have not been widely examined. ...
The beet webworm (Loxostege sticticalis L.) is an important agricultural pest and can tolerate harsh environmental conditions by entering diapause. The diapause mechanism of beet webworm is unknown. Therefore, we conducted a transcriptomic study of the process from diapause induction to diapause release in beet webworms. The results revealed 393 gene modules closely related to the diapause of beet webworm. The hub gene of the red module was the HDACI gene, which acts through histone deacetylase (HDAC) enzymes. HDAC enzyme activity was regulated by the light duration and influenced the JH content under induced beet webworm diapause conditions (12 h light:12 h dark). In addition, transcriptomic data suggested that circadian genes may not be the key genes responsible for beet webworm diapause. However, we showed that the photoperiod affects HDAC enzyme activity, and HDAC can regulate the involvement of JH in beet webworm diapause. This study provided a new module for studying insect diapause and links histone acetylation and diapause at the transcriptome level.
... Previous study revealed that external environmental factors as well as the days after emergence could influence the migratory strategies in Spodoptera exigua (Hübner) [11] and Loxostege sticticalis L. [12]. Recent works have showed that a short critical period is involved in the regulation roles of migration and reproduction in most migratory insects [13][14][15]. During this critical period, extreme environmental conditions such as starvation, a long photoperiod and a low temperature can up-regulate the expression of the allatotropin (AT) gene and accelerate the synthesis of JH by the corpora allata (CA), which thereby may lead to the increased level of JH and result in the early spawning and decreased flight ability in female moths [16]. ...
Mythimna separata (Walker) is a main cereal crop pest that causes extensive damage to the world grain production. The effects of juvenile hormone on M. separata populations remain poorly understood. Here, we explored how JH analog (JHA) affected reproductive traits of both migrant and resident populations in this pest. Our results showed that the influence of JHA treatment on reproduction depended on adult age (days after emergence) of exposure to JHA and populations. Exposure of M. separata residents to JHA (methoprene) on day 1 and day 2 after adult emergence significantly shortened the pre-oviposition period, but increased the lifetime fecundity, mating frequency and grade of ovarian development compared to the controls. However, M. separata migrants exposed to JHA only on day 1 facilitated their reproduction, resulting in a reduction in the pre-oviposition period but an increase in lifetime fecundity, mating frequency and grade of ovarian development. In addition, exposure to JHA from day 2 to day 4 did not significantly affect the ovarian and reproductive development in both migrant and resident populations. These results indicated that the first two days after adult emergence were the sensitive period for residents. In contrast, only the first day after adult emergence was the sensitive stage for migrants. Our findings will contribute to a better understanding of JHA function on M. separata populations.
... Migratory insects with wings not undergoing morphological differentiation can fly on consecutive nights to complete their long-distance migration, and this is referred to as multi-stop migration (Chapman et al., 2010;Wang et al., 2017). Although reproduction is inhibited before migratory flight, an increasing number of studies have shown that migration tends to promote the ovarian development of the female moths, shortens the preoviposition period and actuates synchronized oviposition (Cheng et al., 2012;Zhang et al., 2015;Cheng et al., 2016;Ge et al., 2021). Migrating moths captured by highaltitude searchlights on the island of Bohai Strait, China, in spring, such as Mythimna separata, Agrotis ipsilon and Plutella xylostella, possess well-developed ovaries and have already mated (Zhao et al., 2009;Fu et al., 2014;Liu et al., 2015;Vargas et al., 2018). ...
Despite the importance of reproduction in insects, its relation with multi-stop flight remains poorly understood in migratory species. To clarify whether reproductive maturation commences during the multi-stop flight or after the completion of migration, we conducted physiological and behavioral assays in the rice leaf roller Cnaphalocrocis medinalis with laboratory-simulated conditions and field-captured populations. We found that the ovarian development was significantly promoted by tethered flight treatment for 1-2 nights when compared to the unflown group, while the flight muscle development was not impaired. There was no significant difference in flight duration, flight distance and flight velocity between mated and virgin female moths, indicating that mated moths remained competent for the subsequent flights as did the virgins. Using an integrated field assay, we identified that over 60% of the female moths in the migratory populations captured by high-altitude searchlights in Immigration period of a season had completed the ovarian development and mating. Sexually mature and mated moths collected in the rice field in Emigration period were found capable of engaging in migratory takeoff , as observed using an indoor This article is protected by copyright. All rights reserved. monitoring platform. Overall, our findings point out that C. medinalis managed to complete reproductive maturation to large extent during the multi-stop migratory flight without compromising the migration performance. Such a cost-effective strategy ensures a successful migration for the moths. These findings advance our understanding of the relationship between reproduction and migration, thus shedding light on the development of novel control measures for the outbreak of migratory insect pests.
... The behaviour strategies of insects, like many animals, are associated with physiological processes, particularly the optimal resource allocation between flight and reproduction, which affects insect migratory behaviour and even causes a shift between migration and reproduction (Auerswald & Gäde, 2000;Cheng et al., 2016;. Many migratory insect species use the strategy of long-distance migration to mitigate the energetic costs in complex and variable environments by managing the cost of migration reproduction trade-offs during the preoviposition period (Chapman et al., 2015;Dingle, 1972;Dixon et al., 1993;Kennedy, 1961). ...
... The total triglyceride content of newly emerged adults (1-day-old) from each migrant and resident population was measured using a previously described extraction method (Cheng et al., 2016). After the removal of the head and wings, each insect was weighed and homogenized with a tissue homogenizer (Sangon Biotech, Beijing) in a 1.5-ml microcentrifuge tube using 1 ml of lysis buffer, and the homogenate was then placed in a boiling water bath (70°C for 10 min). ...
Mythimna separata (Walker) is a destructive grain crop pest in China and other Asian countries. However, the effects of fluctuating environmental conditions on M. separata populations remain poorly understood. Here, we investigated how fluctuating temperatures affect the development, reproduction, flight capacity and energy reserves of both migrant and resident populations of M. separata. Our experiments demonstrated that fluctuating temperatures (20–30°C) significantly accelerated development but inhibited adult reproduction and reduced triglyceride reserves in both migrant and resident populations compared with a constant temperature of 25°C, because the larval period, pupal period, lifetime fecundity, mating frequency, ovarian development and triglyceride content significantly decreased, while the preoviposition period obviously increased. A relative decreased tendency of flight capacity was observed for migrants and residents under fluctuating temperatures. We also confirmed that populations and sexes differed in their responses to temperature variations. Mythimna separata residents showed slower development, weaker flight capacity and lower triglyceride content but greater reproductive performance than the migrants under both fluctuating and constant temperatures. Furthermore, female migrants had greater flight potential and triglyceride levels than those of males at both constant temperature and fluctuating temperatures. These findings expand our knowledge of the relationships between fluctuating temperatures and armyworm development, reproduction, energy reserves and adaptive strategies in a complex ambient environment.
... Flight capability also declined with age, similar to the findings for C. medinalis (Pan et al. 2013) and Ostrinia nubilalis (Dorhout et al. 2008). Generally, flight capability has a strong positive correlation with the development of insect flight muscles (Marden 2000;Cheng et al. 2016), increasing with hypertrophy of the flight muscles. ...
The Asian corn borer, Ostrinia furnacalis, is the most notorious corn pest in East Asia and Oceania. The larvae seriously damage crops and lower yields. A previous study found that the O. furnacalis can migrate seasonally. However, the influencing factor on the flight performance of this pest has not yet been investigated. Here, the flight performance and its influencing factors of O. furnacalis were tested using computer-monitored flight mills. The results showed that the longest total flight of an individual was 71.49 km with a mean speed of 6.36 km·h⁻¹ (1.77 m·s⁻¹). Flight performance reached the peak when the moths were 2-days old, with a mean flight distance of 18.89 ± 2.03 km, mean flight duration of 7.34 ± 0.62 h and mean flight speed of 2.47 ± 0.10 km·h⁻¹ (0.69 m·s⁻¹). The flight capability of females was always higher than that of males. Mating status and nutritional status affected partial flight variables. For both sexes, only temperature and relative humidity among the abiotic factors significantly involved flight performance, which was most significant at 25–30 °C and 55–65%. Our study demonstrated that O. furnacalis have a high capability for migration and determined the influencing factors on flight performance. These results provide essential information for forecasting and management of this pest.
... The hypothetical oogenesis-flight syndrome, posits reciprocal regulation of these energy-demanding behaviors in females, has been discussed and evaluated in various insect species 1,[7][8][9][10][11][12][13] . The evidence for this is, however, contradictory, being confirmed for some animal species 7,8,13 , but not others [9][10][11][12] . ...
... The hypothetical oogenesis-flight syndrome, posits reciprocal regulation of these energy-demanding behaviors in females, has been discussed and evaluated in various insect species 1,[7][8][9][10][11][12][13] . The evidence for this is, however, contradictory, being confirmed for some animal species 7,8,13 , but not others [9][10][11][12] . Although the data are still sparse, activating effects of flying on agonistic 2,3 and courtship 4 behaviors were obtained in crickets. ...
In the cricket Gryllus bimaculatus, flying occurs soon after the last imaginal molt and precedes the mating behavior in natural conditions. Here, we tested the hypothesis that flying may improve subsequent behavioral performance in a novel environment in female crickets. We developed a behavioral set-up to test female cricket responsiveness to male calling song as well as their ability to locate and find the source of the song. The male song was produced by a loudspeaker hidden behind the fabric wall of a spacious square arena. Forced flight prior to the test promoted female sexual searching behavior in the novel environment. After the flight, more females reached the hidden source zone, spent more time near the source and finally more of them climbed over the wall section immediately in front of the hidden loudspeaker. At the same time, their behavior in the arena did not differ from the control group when the calling song was not delivered, suggesting that flight exerts its behavioral effects by influencing sexual motivation. Our results support the suggestion that preceding intense locomotion facilitates sexual searching behavior of females in a novel environment.
... In particular, higher reproductive effort can be observed from insect dispersers whose flight muscles are histolized after the onset of oviposition in the new breeding patch [38], as reported in the beet webworm, Loxostege sticticalis Lezed. In this insect, resources from histolysis are reused to sustain fecundity [138]. ...
Dispersal represents a key life-history trait with several implications for the fitness of organisms, population dynamics and resilience, local adaptation, meta-population dynamics, range shifting, and biological invasions. Plastic and evolutionary changes of dispersal traits have been intensively studied over the past decades in entomology, in particular in wing-dimorphic insects for which literature reviews are available. Importantly, dispersal polymorphism also exists in wing-monomorphic and wingless insects, and except for butterflies, fewer syntheses are available. In this perspective, by integrating the very latest research in the fast moving field of insect dispersal ecology, this review article provides an overview of our current knowledge of dispersal polymorphism in insects. In a first part, some of the most often used experimental methodologies for the separation of dispersers and residents in wing-monomorphic and wingless insects are presented. Then, the existing knowledge on the morphological and life-history trait differences between resident and disperser phenotypes is synthetized. In a last part, the effects of range expansion on dispersal traits and performance is examined, in particular for insects from range edges and invasion fronts. Finally, some research perspectives are proposed in the last part of the review.
... The variation in flight performance may be caused by internal speciesspecific temporal changes in physiology (Farnworth 1972, Saito 2000. Insect flight is closely related to the development of flight muscles (Heinrich 1971, Marden 2000, Cheng et al. 2016). Flight performance likely increases in early adults owing to increased mass of the flight muscles (Lorenz 2007). ...
Mamestra brassicae L. is an important, regionally migratory pest of vegetable crops in Europe and Asia. Its migratory activity contributes significantly to population outbreaks, causing severe crop yield losses. Because an in-depth understanding of flight performance is key to revealing migratory patterns, here we used a computer-linked flight mill and stroboscope to study the flight ability and wingbeat frequency (WBF) of M. brassicae in relation to sex, age, temperature, and relative humidity (RH). The results showed that age significantly affected the flight ability and WBF of M. brassicae, and 3-d-old individuals performed the strongest performance (total flight distance: 45.6 ± 2.5 km; total flight duration: 9.3 ± 0.3 h; WBF: 44.0 ± 0.5 Hz at 24°C and 75% RH). The age for optimal flight was considered to be 2-3 d old. Temperature and RH also significantly affected flight ability and WBF; flight was optimal from 23°C to 25°C and 64-75% RH. Because M. brassicae thus has great potential to undertake long-distance migration, better knowledge of its flight behavior and migration will help establish a pest forecasting and early-warning system.
... Because proteins are a much lower energetic source than are lipids (5.3 kJ g 21 and 37.6 kJ g 21 , respectively), this suggests that the oxidation of proteins was mostly driven by water needs, as protein supplies five times more total water than do lipids [16]. Muscle loss during reproduction has been documented in insects [31,32], fish [33], reptiles [34], birds [35,36] and mammals [37,38]. Protein mobilization is typically associated with extended fasting and is thought to cover energy and amino acid requirements when lipid reserves and food intake are insufficient [9,39]. ...
The use of fat to support the energy needs of reproduction (i.e. capital breeding) has been studied in a diversity of taxa. However, despite reproductive output (i.e. young or eggs) being approximately 70% water, little is known about the availability of internal resources to accommodate the hydric demands of reproduction. Recent research suggests that dehydration increases the catabolism of muscle as a means of maintaining water balance. Accordingly, we investigated the interactive effects of reproductive investment and water deprivation on catabolism and reproductive output in female Children's pythons (Antaresia childreni). Both reproductive and non-reproductive females were either provided water ad libitum or were water-deprived for three weeks at the time when reproductive females were gravid. We found that water-deprived reproductive females had, in general, greater body mass loss, epaxial muscle loss, plasma osmolality and plasma uric acid concentrations relative to the other groups. Furthermore , water-deprived females had similar clutch sizes compared with females with access to water, but produced lighter eggs and lower total clutch masses. Our results provide the first evidence that selective protein catabolism can be used to support water demands during reproduction, and, as a result, these findings extend the capital breeding concept to non-energetic resources.
... Multiple systems exist for doing this, including wind tunnels (Vogel, 1966) (reviewed for the use in birds in Hedenström & Lindström, 2017) and free-flight chambers (Byrne, 1999;Blackmer et al., 2004;Perez-Mendoza et al., 2011). Recently, however, there has been a resurgence in the use of tethered flight systems as a means of determining the flight potential of migratory insects (Attisano et al., 2015;Jones et al., 2015;Cheng et al., 2016;Jones et al., 2016;Marti-Campoy et al., 2016). Tethered flight mills enable the continuous measurement of flight parameters over a prolonged period of time and have been used for the past 50-60 years to study behaviour both during foraging flights [e.g. ...
... (i) Mean monthly day lengths (yellow) and mean monthly low temperature (blue) at the monarch overwintering site; (ii) increasing photoperiod and low temperatures shift the orientation of fall migrants north; (iii) this orientation remains the same under constant photoperiod. (b) The association of oviposition and flight propensity in the female beet webworm, Loxostege sticticalis (Cheng et al., 2016). (i-iii) Changes in flight distance (m) (i), flight velocity (km h -1 ) (ii) and flight duration (h) (iii) with increasing days after oviposition with mated (solid circle •) and virgin (empty circle ○) females. ...
... The syndrome explains the pattern when egg development and mating are suppressed during migratory flight and subsequently stimulated after migration is terminated. Peak flight activity during pre-reproduction as well as a decrease in flight performance with the onset of oviposition has been shown in many species as evidence of the oogenesis-flight syndrome (Dingle, 1966;Armes & Cooter, 1991;Colvin & Gatehouse, 1993b;Schumacher et al., 1997b;Cheng et al., 2016) (Fig. 5b). The syndrome is not, however, universally present among all migratory insects, and tethered flight has been used to show that some species are capable of long-distance flights both post-mating and post-oviposition (Sappington & Showers, 1992b;Schumacher et al., 1997b;X. ...
1. Every year billions of insects engage in long‐distance, seasonal mass migrations which have major consequences for agriculture, ecosystem services and insect‐vectored diseases. Tracking this movement in the field is difficult, with mass migrations often occurring at high altitudes and over large spatial scales.
2. As such, tethered flight provides a valuable tool for studying the flight behaviour of insects, giving insights into flight propensity (e.g. distance, duration and velocity) and orientation under controlled laboratory settings. By experimentally manipulating a variety of environmental and physiological traits, numerous studies have used this technology to study the flight behaviour of migratory insects ranging in size from aphids to butterflies. Advances in functional genomics promise to extend this to the identification of genetic factors associated with flight. Tethered flight techniques have been used to study migratory flight characteristics in insects for more than 50 years, but have never been reviewed.
3. This study summarises the key findings of this technology, which has been employed in studies of species from six Orders. By providing detailed descriptions of the tethered flight systems, the present study also aims to further the understanding of how tethered flight studies support field observations, the situations under which the technology is useful and how it might be used in future studies.
4. The aim is to contextualise the available tethered flight studies within the broader knowledge of insect migration and to describe the significant contribution these systems have made to the literature.
