Convergent patterns of long-distance nocturnal migration in noctuid moths and passerine birds

Vast numbers of insects and passerines achieve long-distance migrations between summer and winter locations by undertaking high-altitude nocturnal flights. Insects such as noctuid moths fly relatively slowly in relation to the surrounding air, with airspeeds approximately one-third of that of passerines. Thus, it has been widely assumed that windborne insect migrants will have comparatively little control over their migration speed and direction compared with migrant birds. We used radar to carry out the first comparative analyses of the flight behaviour and migratory strategies of insects and birds under nearly equivalent natural conditions. Contrary to expectations, noctuid moths attained almost identical ground speeds and travel directions compared with passerines, despite their very different flight powers and sensory capacities. Moths achieved fast travel speeds in seasonally appropriate migration directions by exploiting favourably directed winds and selecting flight altitudes that coincided with the fastest air streams. By contrast, passerines were less selective of wind conditions, relying on self-powered flight in their seasonally preferred direction, often with little or no tailwind assistance. Our results demonstrate that noctuid moths and passerines show contrasting risk-prone and risk-averse migratory strategies in relation to wind. Comparative studies of the flight behaviours of distantly related taxa are critically important for understanding the evolution of animal migration strategies.     

Quantifying interspecific variation in dispersal ability of noctuid moths using an advanced tethered flight technique

Dispersal plays a crucial role in many aspects of species' life histories, yet is often difficult to measure directly. This is particularly true for many insects, especially nocturnal species (e.g. moths) that cannot be easily observed under natural field conditions. Consequently, over the past five decades, laboratory tethered flight techniques have been developed as a means of measuring insect flight duration and speed. However, these previous designs have tended to focus on single species (typically migrant pests), and here we describe an improved apparatus that allows the study of flight ability in a wide range of insect body sizes and types. Obtaining dispersal information from a range of species is crucial for understanding insect population dynamics and range shifts. Our new laboratory tethered flight apparatus automatically records flight duration, speed, and distance of individual insects. The rotational tethered flight mill has very low friction and the arm to which flying insects are attached is extremely lightweight while remaining rigid and strong, permitting both small and large insects to be studied. The apparatus is compact and thus allows many individuals to be studied simultaneously under controlled laboratory conditions. We demonstrate the performance of the apparatus by using the mills to assess the flight capability of 24 species of British noctuid moths, ranging in size from 12–27 mm forewing length (~40–660 mg body mass). We validate the new technique by comparing our tethered flight data with existing information on dispersal ability of noctuids from the published literature and expert opinion. Values for tethered flight variables were in agreement with existing knowledge of dispersal ability in these species, supporting the use of this method to quantify dispersal in insects. Importantly, this new technology opens up the potential to investigate genetic and environmental factors affecting insect dispersal among a wide range of species.     

A Simple Flight Mill for the Study of Tethered Flight in Insects

Flight in insects can be long-range migratory flights, intermediate-range dispersal flights, or short-range host-seeking flights. Previous studies have shown that flight mills are valuable tools for the experimental study of insect flight behavior, allowing researchers to examine how factors such as age, host plants, or population source can influence an insects'' propensity to disperse. Flight mills allow researchers to measure components of flight such as speed and distance flown. Lack of detailed information about how to build such a device can make their construction appear to be prohibitively complex. We present a simple and relatively inexpensive flight mill for the study of tethered flight in insects. Experimental insects can be tethered with non-toxic adhesives and revolve around an axis by means of a very low friction magnetic bearing. The mill is designed for the study of flight in controlled conditions as it can be used inside an incubator or environmental chamber. The strongest points are the very simple electronic circuitry, the design that allows sixteen insects to fly simultaneously allowing the collection and analysis of a large number of samples in a short time and the potential to use the device in a very limited workspace. This design is extremely flexible, and we have adjusted the mill to accommodate different species of insects of various sizes.     

Challenges and prospects in the telemetry of insects

Radio telemetry has been widely used to study the space use and movement behaviour of vertebrates, but transmitter sizes have only recently become small enough to allow tracking of insects under natural field conditions. Here, we review the available literature on insect telemetry using active (battery‐powered) radio transmitters and compare this technology to harmonic radar and radio frequency identification (RFID) which use passive tags (i.e. without a battery). The first radio telemetry studies with insects were published in the late 1980s, and subsequent studies have addressed aspects of insect ecology, behaviour and evolution. Most insect telemetry studies have focused on habitat use and movement, including quantification of movement paths, home range sizes, habitat selection, and movement distances. Fewer studies have addressed foraging behaviour, activity patterns, migratory strategies, or evolutionary aspects. The majority of radio telemetry studies have been conducted outside the tropics, usually with beetles (Coleoptera) and crickets (Orthoptera), but bees (Hymenoptera), dobsonflies (Megaloptera), and dragonflies (Odonata) have also been radio‐tracked. In contrast to the active transmitters used in radio telemetry, the much lower weight of harmonic radar and RFID tags allows them to be used with a broader range of insect taxa. However, the fixed detection zone of a stationary radar unit (< 1 km diameter) and the restricted detection distance of RFID tags (usually < 1–5 m) constitute major constraints of these technologies compared to radio telemetry. Most of the active transmitters in radio telemetry have been applied to insects with a body mass exceeding 1 g, but smaller species in the range 0.2–0.5 g (e.g. bumblebees and orchid bees) have now also been tracked. Current challenges of radio‐tracking insects in the field are related to the constraints of a small transmitter, including short battery life (7–21 days), limited tracking range on the ground (100–500 m), and a transmitter weight that sometimes approaches the weight of a given insect (the ratio of tag mass to body mass varies from 2 to 100%). The attachment of radio transmitters may constrain insect behaviour and incur significant energetic costs, but few studies have addressed this in detail. Future radio telemetry studies should address (i) a larger number of species from different insect families and functional groups, (ii) a better coverage of tropical regions, (iii) intraspecific variability between sexes, ages, castes, and individuals, and (iv) a larger tracking range via aerial surveys with helicopters and aeroplanes equipped with external antennae. Furthermore, field and laboratory studies, including observational and experimental approaches as well as theoretical modelling, could help to clarify the behavioural and energetic consequences of transmitter attachment. Finally, the development of commercially available systems for automated tracking and potential future options of insect telemetry from space will provide exciting new avenues for quantifying movement and space use of insects from local to global spatial scales.     

Female butterflies modulate investment in reproduction and flight in response to monsoon‐driven migrations

Migratory species may display striking phenotypic plasticity during individual lifetimes. This may include differential investment in body parts and functions, differential resource use and allocation, and behavioural changes between migratory and non‐migratory phases. While migration‐related phenotypic changes are well‐reported, their underlying mechanisms are usually poorly understood. Here we compare individuals from migratory (reproductive diapause) and non‐migratory (reproductive) phases of closely related aposematic butterfly species to study how sexual dimorphism and migratory behaviour underlie significant morphological tradeoffs, and propose a plausible scenario to explain the migration‐related phenotypic plasticity observed in females of migratory species. We found that female butterflies invested significantly more in their abdominal mass compared to males irrespective of their migratory phase, and underwent a clear shift in their body mass allocation after the switch from the reproductive diapause phase to the reproductive phase. In reproductive phase, females invested much more in reproductive tissue. This switch occurred as a result of increased abdominal mass (i.e. reproductive tissue mass) without significant reduction in the thoracic mass (i.e. flight muscle mass). Migratory males, however, were not significantly different from non‐migratory males in terms of relative investment in flight and reproductive tissues. These patterns were consistent between migratory and non‐migratory aposematic species within and across clades. While migratory habits may influence the physiology and behaviour of both sexes, long‐distance migration affected female morphology much more markedly compared to that of males. These results show the sex‐specific nature of adaptations to migratory behaviour, and suggest that seemingly disparate life‐history traits such as aposematism and migration may have similar influences on the lifetime energetic investments of insects.     

温、湿度对粘虫蛾飞行能源物质利用的影响

系统研究了不同温、湿度对粘虫蛾飞行能源物质消耗的影响,结果表明,温、湿度对成虫飞行能源物质消耗有显著影响,在适宜的温、湿度下飞行时,粘虫蛾主要飞行能源物质（甘油三酯和糖原）消耗最少,其飞行单位距离所需的甘油三酯也最少,即能源利用效率最高,随着温,湿度从适宜到不适宜,甘油三酯消耗有逐渐增多的趋势,但温,湿度对成虫飞行能源物质消耗会因蛾龄及性别的不同而异,在所测试的几种温,湿度下（高温35℃除外）,5日龄成虫在飞行中消耗的甘油三酯最多,低龄和高龄时消耗均较少,高温下飞行时,雄蛾比雌蛾消耗的能源物质多,而在高温或低湿条件下,雌蛾比雄蛾消耗的多,进一步对影响成虫飞行能源物质消耗的海藻糖酶活力及呼吸强度研究表明,温、湿度对海藻糖酶活性有明显影响,在适宜的温,湿度下,酶的活性高,反之,酶的活性降低,其中高温对酶活性的抑制作用比低温明显,但高湿和低湿对酶活性的抑制作用基本一致,成虫呼吸强度随温度的升降而升降,飞行初期成虫呼吸强度急剧增加,但0.5h后开始下降并维持在一个较稳定的水平,根据所获结果对温、湿度与粘虫蛾飞行能源物质消耗之间的内在联系进行了讨论.     

Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts

Monarch butterflies (Danaus plexippus) are parasitized by the protozoan Ophryocystis elektroscirrha throughout their geographical range. Monarchs inhabiting seasonally fluctuating environments migrate annually, and parasite prevalence is lower among migratory relative to non‐migratory populations. One explanation for this pattern is that long‐distance migration weeds out infected animals, thus reducing parasite prevalence and transmission between generations. In this study we experimentally infected monarchs from a migratory population and recorded their long‐distance flight performance using a tethered flight mill. Results showed that parasitized butterflies exhibited shorter flight distances, slower flight speeds, and lost proportionately more body mass per km flown. Differences between parasitized and unparasitized monarchs were generally not explained by individual variation in wing size, shape, or wing loading, suggesting that poorer flight performance among parasitized hosts was not directly caused by morphological constraints. Effects of parasite infection on powered flight support a role for long‐distance migration in dramatically reducing parasite prevalence in this and other host–pathogen systems.     

Wing size but not wing shape is related to migratory behavior in a soaring bird

Both wing size and wing shape affect the flight abilities of birds. Intra and inter‐specific studies have revealed a pattern where high aspect ratio and low wing loading favour migratory behaviour. This, however, have not been studied in soaring migrants. We assessed the relationship between the wing size and shape and the characteristics of the migratory habits of the turkey vulture Cathartes aura, an obligate soaring migrant. We compared wing size and shape with migration strategy among three fully migratory, one partially migratory and one non‐migratory (resident) population distributed across the American continent. We calculated the aspect ratio and wing loading using wing tracings to characterize the wing morphology. We used satellite‐tracking data from the migratory populations to calculate distance, duration, speed and altitude during migration. Wing loading, but not aspect ratio, differed among the populations, segregating the resident population from the completely migratory ones. Unlike what has been reported in species using flapping flight during migration, the migratory flight parameters of turkey vultures were not related to the aspect ratio. By contrast, wing loading was related to most flight parameters. Birds with lower wing loading flew farther, faster, and higher during their longer journeys. Our results suggest that wing morphology in this soaring species enables lower‐cost flight, through low wing‐loading, and that differences in the relative sizes of wings may increase extra savings during migration. The possibility that wing shape is influenced by foraging as well as migratory flight is discussed. We conclude that flight efficiency may be improved through different morphological adaptations in birds with different flight mechanisms.     

Long‐range seasonal migration in insects: mechanisms,evolutionary drivers and ecological consequences

Myriad tiny insect species take to the air to engage in windborne migration, but entomology also has its ‘charismatic megafauna’ of butterflies, large moths, dragonflies and locusts. The spectacular migrations of large day‐flying insects have long fascinated humankind, and since the advent of radar entomology much has been revealed about high‐altitude night‐time insect migrations. Over the last decade, there have been significant advances in insect migration research, which we review here. In particular, we highlight: (1) notable improvements in our understanding of lepidopteran navigation strategies, including the hitherto unsuspected capabilities of high‐altitude migrants to select favourable winds and orientate adaptively, (2) progress in unravelling the neuronal mechanisms underlying sun compass orientation and in identifying the genetic complex underpinning key traits associated with migration behaviour and performance in the monarch butterfly, and (3) improvements in our knowledge of the multifaceted interactions between disease agents and insect migrants, in terms of direct effects on migration success and pathogen spread, and indirect effects on the evolution of migratory systems. We conclude by highlighting the progress that can be made through inter‐phyla comparisons, and identify future research areas that will enhance our understanding of insect migration strategies within an eco‐evolutionary perspective.     

昆虫定向机制研究进展

许多昆虫具有定向运动的行为。对部分社会性昆虫和迁飞性昆虫定向行为的大量研究已经初步阐明太阳、地磁场、天体、风及地面标志物等都可能成为昆虫返巢和迁飞定向的线索。社会性昆虫具有对不同定向线索进行整合而实现精确导航的能力。日间迁飞性昆虫利用时间补偿太阳罗盘进行定向的机制亦已明确,但夜间迁飞昆虫的定向机制尚需深入研究。迁飞性害虫定向机制的明确将有助于判断害虫迁飞路径及降落区域,为迁飞害虫的准确预测提供科学依据。本文对昆虫的定向机制研究进展进行了综述。     

METHOPRENE INFLUENCES REPRODUCTION AND FLIGHT CAPACITY IN ADULTS OF THE RICE LEAF ROLLER,Cnaphalocrocis Medinalis (GUENỂE) (LEPIDOPTERA: PYRALIDAE)

Juvenile hormone (JH) influences many aspects of insect biology, including oogenesis‐flight syndrome tradeoffs between migration and reproduction. Drawing on studies of many migratory insects, we posed the hypothesis that JH influences migratory capacity and oogenesis in the rice leaf roller, Cnaphalocrocis medinalis. We treated adults moths (days 1, 2 and 3 postemergence) with the JH analog (JHA), methoprene, and then recorded the influences of JHA treatments on reproduction. JHA treatment on day 1 postemergence, but not on the other days, shortened the preoviposition period, although JHA did not influence total fecundity, oviposition period, or longevity. We infer day 1 postemergence is the JH‐sensitive stage to influence reproduction. Therefore, we treated moths on day 1 postemergence with JHA and recorded flight capacity, flight muscle mass, and triacylglycerol (TAG) accumulation. JHA treatments did not influence flight speed, but led to reductions in flight durations and flight distances. At day 3 posttreatment (PT), JHA‐treated females flew shorter times and less distance than the controls; JHA‐treated males, however, only flew shorter times than the controls. JHA treatments led to reductions in flight muscle mass in females at days 2–3 PT and reductions in TAG content in females at day 3 PT, but, these parameters were not influenced by JHA in males. These findings strongly support our hypothesis, from which we infer that JH is a major driver in C. medinalis oogenesis‐flight syndrome tradeoffs. Our data also reveal a JH‐sensitive stage in adulthood during which JH influences the oocyte‐flight syndrome in C. medinalis.     

Barometer logging reveals new dimensions of individual songbird migration

Recent advances in tracking technology are based on the use of miniature sensors for recording new aspects of individual migratory behaviour. In this study, we have used activity data loggers with barometric and temperature sensors to record the flight altitudes as well as ground elevations during stationary periods of migratory songbirds. We tracked one individual of red‐backed shrike and one great reed warbler along their autumn migration from Europe to Africa. Both individuals performed their migration stepwise in travel segments and climbed most metres during the passage across the Mediterranean Sea and the Sahara Desert and least metres during the first flight segment in Europe. The great reed warbler reached its highest flight altitude of 3950 m a.s.l. during the travel segment from Europe to west Africa, while the red‐backed shrike reached 3650 m a.s.l as maximum flight altitude during its travel segment from Sahel to southern Africa. Both individuals used both lowlands and highlands for resting periods along their migrations. Furthermore, temperature decreased with increasing altitude during migratory flights for both individuals, highlighting the potential to determine flight duration from temperature measurements. Finally, we discuss how barometric data could be used to investigate birds’ responses to changes in air pressure as a cue for departures on migratory flights. This new technique, i.e. using a miniature data logger with barometric pressure sensor to estimate flight altitudes and ground elevations, will open up new avenues for research and importantly advance our understanding on how small birds behave during migratory flights.     

Wind selection and drift compensation optimize migratory pathways in a high-flying moth

Numerous insect species undertake regular seasonal migrations in order to exploit temporary breeding habitats [1]. These migrations are often achieved by high-altitude windborne movement at night [2-6], facilitating rapid long-distance transport, but seemingly at the cost of frequent displacement in highly disadvantageous directions (the so-called "pied piper" phenomenon [7]). This has lead to uncertainty about the mechanisms migrant insects use to control their migratory directions [8, 9]. Here we show that, far from being at the mercy of the wind, nocturnal moths have unexpectedly complex behavioral mechanisms that guide their migratory flight paths in seasonally-favorable directions. Using entomological radar, we demonstrate that free-flying individuals of the migratory noctuid moth Autographa gamma actively select fast, high-altitude airstreams moving in a direction that is highly beneficial for their autumn migration. They also exhibit common orientation close to the downwind direction, thus maximizing the rectilinear distance traveled. Most unexpectedly, we find that when winds are not closely aligned with the moth's preferred heading (toward the SSW), they compensate for cross-wind drift, thus increasing the probability of reaching their overwintering range. We conclude that nocturnally migrating moths use a compass and an inherited preferred direction to optimize their migratory track.     

NUMERICAL SIMULATION OF THE PATHWAYS OF MIGRATING INSECTS

Abstract  Based on boundary layer meteorology and behavioural ecology of insect migration, a numerical TRA model was established. The spatial and temporal resolutions of the standard meteorological data are far insufficient for insect migration studies; so, a one dimension TKE closure scheme (E-ε scheme) was adopted to simulate the wind and temperature profiles en route based on the conventional surface and 850 hPa wind and temperature data of Chinese National Meteorological Bureau. Then the migrating behaviour of insects was parameterized as some proper mathematical expressions to determine their timing and their flight height, speed and direction from the wind and temperature profiles simulated by the PBL sub-model, and so their flight pathways could be estimated by a simple algorithm. Finally, the hourly episodes of the airborne migrants were output which consists of the latitude, longitude and flying altitude. The TRA model was verified by mark-release-recapture studies of Mythimna separata, Loxostege sticticalis , and Agrotis ipsilon . The results suggest that the parameterizing scheme of migratory behaviour, the numerical simulation scheme of wind and temperature in PBL and the TRA procedure developed in this paper should be reasonable and feasible. This model provides a useful tool for inter-regional forecast of migratory insect pests.     

Monarch butterflies reared under autumn-like conditions have more efficient flight and lower post-flight metabolism

1. Many migratory animals undergo physiological and behavioural changes to prepare for and sustain long-distance movements. Because insect migrations are common and diverse, studies that examine how migratory insects meet the energetic demands of long-distance movements are badly needed. 2. Monarch butterflies (Danaus plexippus) migrate up to 4000 km annually from eastern North America to wintering sites in central Mexico. Autumn generation monarchs undergo physiological and behavioural changes in response to environmental cues to initiate migration. In particular, exposure to cooler temperatures and shorter day lengths in early autumn causes monarchs to enter the hormonally induced state of reproductive diapause. 3. This study examined differences in flight-associated metabolic rate (MR) and flight performance metrics for monarchs experimentally reared under autumn-like conditions (typically experienced before the southward migration) relative to monarchs reared under summer-like conditions. 4. Adult monarchs reared under autumn-like conditions showed lower post-flight MRs, greater flight efficiency, and lower measures of reproductive activity relative to monarchs reared under summer-like conditions. Increases in post-flight metabolism were associated with monarch body weight, age, and flight velocity. 5. These findings suggest that a trans-generational shift in flight energetics is an important component of the monarch's complex migratory syndrome, and that physiological changes that accompany reproductive diapause facilitate energy conservation during flight.     

Body condition and feather molt of a migratory shorebird during the non‐breeding season

Migratory shorebirds have some of the highest fat loads among birds, especially species which migrate long distances. The upland sandpiper Bartramia longicauda makes long‐distance migrations twice a year, but variation in body condition or timing of feather molt during the non‐breeding season has not been studied. Molt is an important part of the annual cycle of migratory birds because feather condition determines flight performance during migration, and long‐distance movements are energetically costly. However, variation in body condition during molt has been poorly studied. The objective of our field study was to examine the timing and patterns of feather molt of a long distance migratory shorebird during the non‐breeding season and test for relationships with body size, fat depots, mass, and sex. Field work was conducted at four ranches in the Northern Campos of Uruguay (Paysandú and Salto Departments). We captured and marked 62 sandpipers in a 2‐month period (Nov–Jan) during four non‐breeding seasons (2008–2012). Sex was determined by genetic analyses of blood samples taken at capture. Molt was measured in captured birds using rank scores based on published standards. Body mass and tarsus length measurements showed female‐biased sexual size dimorphism with males smaller than females. Size‐corrected body mass (body condition) showed a U‐shaped relationship with the day of the season, indicating that birds arrived at non‐breeding grounds in relatively good condition. Arriving in good body condition at non‐breeding grounds is probably important because of the energetic demands due to physiological adjustments after migration and the costs of feather molt.     

On the sex-specific mechanisms of butterfly flight: flight performance relative to flight morphology, wing kinematics, and sex in Pararge aegeria

Many evolutionary ecological studies have documented sexual dimorphism in morphology or behaviour. However, to what extent a sex-specific morphology is used differently to realize a certain level of behavioural performance is only rarely tested. We experimentally quantified flight performance and wing kinematics (wing beat frequency and wing stroke amplitude) and flight morphology (thorax mass, body mass, forewing aspect ratio, and distance to centre of forewing area) in the butterfly Pararge aegeria (L.) using a tethered tarsal reflex induced flight set-up under laboratory conditions. On average, females showed higher flight performance than males, but frequency and amplitude did not differ. In both sexes, higher flight performance was partly determined by wing beat frequency but not by wing stroke amplitude. Dry body mass, thorax mass, and distance to centre of forewing area were negatively related to wing beat frequency. The relationship between aspect ratio and wing stroke amplitude was sex-specific: females with narrower wings produced higher amplitude whereas males show the opposite pattern. The results are discussed in relation to sexual differences in flight behaviour.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 675–687.     

Heritability and physiological correlates of migratory tendency in the grasshopper Melanoplus sanguinipes

Abstract. Durations of tethered flights by the North American migratory grasshopper Melanoplus sanguinipes Fabricius are bimodally distributed: most individuals either will not fly, or else will fly for many hours. This observation suggests a simple measure (the ‘one‐hour rule’) for distinguishing migrants from non‐migrants. This measure is repeatable (repeatability = 0.6–0.7). Using laboratory‐reared offspring of grasshoppers from an Arizona population of mixed migratory tendency, a breeding experiment was conducted to determine the heritability of migratory tendency and possible correlated responses to selection on migratory behaviour. When migratory tendency is considered as a threshold trait, the heritability of liability is in the range 0.5–0.6. Most families in the breeding experiment had at least some migrants among their offspring; selection on migratory incidence had a correlated effect on the durations of flights by these individuals. The magnitude of thoracic lipid reserves showed a modest correlated response to selection on migratory behaviour. Thoracic and abdominal lipid reserves in identified migrants are reduced by flight, indicating that lipid is mobilized and consumed during flight in this species.