Orientation in high-flying migrant insects in relation to flows: mechanisms and strategies

High-flying insect migrants have been shown to display sophisticated flight orientations that can, for example, maximize distance travelled by exploiting tailwinds, and reduce drift from seasonally optimal directions. Here, we provide a comprehensive overview of the theoretical and empirical evidence for the mechanisms underlying the selection and maintenance of the observed flight headings, and the detection of wind direction and speed, for insects flying hundreds of metres above the ground. Different mechanisms may be used—visual perception of the apparent ground movement or mechanosensory cues maintained by intrinsic features of the wind—depending on circumstances (e.g. day or night migrations). In addition to putative turbulence-induced velocity, acceleration and temperature cues, we present a new mathematical analysis which shows that ‘jerks’ (the time-derivative of accelerations) can provide indicators of wind direction at altitude. The adaptive benefits of the different orientation strategies are briefly discussed, and we place these new findings for insects within a wider context by comparisons with the latest research on other flying and swimming organisms. This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’.

[1]  Phillip M. Stepanian,et al.  Nocturnally migrating songbirds drift when they can and compensate when they must , 2016, Scientific Reports.

[2]  S. Rennie,et al.  Common orientation and layering of migrating insects in southeastern Australia observed with a Doppler weather radar , 2014 .

[3]  Kongming Wu,et al.  Seasonal Migration of Helicoverpa armigera (Lepidoptera: Noctuidae) Over the Bohai Sea , 2009, Journal of economic entomology.

[4]  J. Tautz,et al.  Air movement sensitive hairs and interneurons inLocusta migratoria , 1982, Journal of comparative physiology.

[5]  J. Riley,et al.  The long‐distance migration of Nilaparvata lugens (Stål) (Delphacidae) in China: radar observations of mass return flight in the autumn , 1991 .

[6]  R. Voigt,et al.  Sensory processing of water currents by fishes. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[7]  V. Alistair Drake,et al.  Animal Orientation Strategies for Movement in Flows , 2011, Current Biology.

[8]  J. Riley,et al.  Does a ‘turbophoretic’ effect account for layer concentrations of insects migrating in the stable night-time atmosphere? , 2009, Journal of The Royal Society Interface.

[9]  A. Reynolds,et al.  Aphid aerial density profiles are consistent with turbulent advection amplifying flight behaviours: abandoning the epithet ‘passive’ , 2009, Proceedings of the Royal Society B: Biological Sciences.

[10]  Matthew J. McHenry,et al.  The biomechanics of sensory organs , 2009 .

[11]  R. B. Srygley,et al.  Optimal strategies for insects migrating in the flight boundary layer: mechanisms and consequences. , 2007, Integrative and comparative biology.

[12]  T. Alerstam,et al.  Adaptive strategies in nocturnally migrating insects and songbirds: contrasting responses to wind. , 2016, Journal of Animal Ecology.

[13]  A. Reynolds,et al.  A single wind-mediated mechanism explains high-altitude ‘non-goal oriented’ headings and layering of nocturnally migrating insects , 2010, Proceedings of the Royal Society B: Biological Sciences.

[14]  C. G. Johnson,et al.  Migration and dispersal of insects by flight. , 1971 .

[15]  Rory P. Wilson,et al.  Convergent evolution in locomotory patterns of flying and swimming animals. , 2011, Nature communications.

[16]  A. Reynolds,et al.  Flight altitude selection increases orientation performance in high-flying nocturnal insect migrants , 2011, Animal Behaviour.

[17]  B. Frost,et al.  Virtual migration in tethered flying monarch butterflies reveals their orientation mechanisms , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Jonathan P. Dyhr,et al.  Luminance-dependent visual processing enables moth flight in low light , 2015, Science.

[19]  M. Dacke,et al.  Visual Navigation in Nocturnal Insects. , 2016, Physiology.

[20]  Don R. Reynolds,et al.  Flight Orientation Behaviors Promote Optimal Migration Trajectories in High-Flying Insects , 2010, Science.

[21]  M. Byrne,et al.  Dung Beetles Use the Milky Way for Orientation , 2013, Current Biology.

[22]  Mandyam V Srinivasan,et al.  Visual control of navigation in insects and its relevance for robotics , 2011, Current Opinion in Neurobiology.

[23]  A. D. Smith,et al.  A radar study of emigratory flight and layer formation by insects at dawn over southern Britain , 2007, Bulletin of Entomological Research.

[24]  D. R. Reynolds,et al.  A Long-Range Migration of Grasshoppers Observed in the Sahelian Zone of Mali by Two Radars , 1983 .

[25]  Eric J. Warrant,et al.  Nocturnal Vision and Landmark Orientation in a Tropical Halictid Bee , 2004, Current Biology.

[26]  Orientation Cues for High-Flying Nocturnal Insect Migrants: Do Turbulence-Induced Temperature and Velocity Fluctuations Indicate the Mean Wind Flow? , 2010, PloS one.

[27]  A. Reynolds,et al.  Detection of flow direction in high-flying insect and songbird migrants , 2015, Current Biology.

[28]  J. Riley,et al.  Visual detection of wind-drift by high-flying insects at night: a laboratory study , 1988, Journal of Comparative Physiology A.

[29]  Kongming Wu,et al.  Nocturnal migration of dragonflies over the Bohai Sea in northern China , 2006 .

[30]  Thomas Alerstam,et al.  The problem of estimating wind drift in migrating birds. , 2002, Journal of theoretical biology.

[31]  D. Reynolds,et al.  Insect Migration: Long-range insect migration in relation to climate and weather: Africa and Europe , 1995 .

[32]  A. S. Edwards,et al.  Observations of the autumn migration of the rice leaf roller Cnaphalocrocis medinalis (Lepidoptera: Pyralidae) and other moths in eastern China. , 1995 .

[33]  J. Riley,et al.  Radar observations of concentrations of insects above a river in Mali, West Africa , 1979 .

[34]  Timothy J. Lang,et al.  Observations of Quasi-Symmetric Echo Patterns in Clear Air with the CSU–CHILL Polarimetric Radar , 2004 .

[35]  Sanjay P Sane,et al.  Encoding properties of the mechanosensory neurons in the Johnston's organ of the hawk moth, Manduca sexta , 2014, Journal of Experimental Biology.

[36]  Andrew M. Hein,et al.  Energetic and biomechanical constraints on animal migration distance. , 2012, Ecology letters.

[37]  Nathan F. Putman,et al.  Longitude Perception and Bicoordinate Magnetic Maps in Sea Turtles , 2011, Current Biology.

[38]  A. Reynolds,et al.  Wind-Related Orientation Patterns in Diurnal, Crepuscular and Nocturnal High-Altitude Insect Migrants , 2016, Front. Behav. Neurosci..

[39]  G. W. Schaefer,et al.  Spruce budworm (Lepidoptera: Tortricidae) moth flight and dispersal: new understanding from canopy observations, radar, and aircraft. , 1980 .

[40]  D. Reynolds,et al.  A seasonal switch in compass orientation in a high-flying migrant moth , 2008, Current Biology.

[41]  Michael B. Bonsall,et al.  Seasonal migration to high latitudes results in major reproductive benefits in an insect , 2012, Proceedings of the National Academy of Sciences.

[42]  Mandyam V. Srinivasan,et al.  Motion detection in insect orientation and navigation , 1999, Vision Research.

[43]  Spatial dispersion of aerial plankton over east-central Florida: Aeolian transport and coastline concentrations , 2001 .

[44]  Nathan F. Putman,et al.  Multi-Modal Homing in Sea Turtles: Modeling Dual Use of Geomagnetic and Chemical Cues in Island-Finding , 2016, Front. Behav. Neurosci..

[45]  Solitary wave disturbances of the nocturnal boundary layer revealed by radar observations of migrating insects , 1985 .

[46]  Eric J. Warrant,et al.  Vision and visual navigation in nocturnal insects. , 2011, Annual review of entomology.

[47]  D. Reynolds,et al.  The significance of midsummer movements of Autographa gamma: Implications for a mechanistic understanding of orientation behavior in a migrant moth , 2013 .

[48]  Michael Gewecke,et al.  Flight orientation of swarming Locusta migratoria , 1984 .

[49]  J. Westbrook,et al.  Radar observations of orientation of noctuids migrating from corn fields in the Lower Rio Grande Valley , 1995 .

[50]  S. Sane,et al.  Antennal Mechanosensors Mediate Flight Control in Moths , 2007, Science.

[51]  Kenneth Wilson,et al.  Long-range seasonal migration in insects: mechanisms, evolutionary drivers and ecological consequences. , 2015, Ecology letters.

[52]  D. Kobayashi,et al.  “Going with the Flow” or Not: Evidence of Positive Rheotaxis in Oceanic Juvenile Loggerhead Turtles (Caretta caretta) in the South Pacific Ocean Using Satellite Tags and Ocean Circulation Data , 2014, PloS one.

[53]  Tateo Shimozawa,et al.  Cricket Wind Receptors: Thermal Noise for the Highest Sensitivity Known , 2003 .

[54]  Ian P. Woiwod,et al.  Wind Selection and Drift Compensation Optimize Migratory Pathways in a High-Flying Moth , 2008, Current Biology.

[55]  J. Kennedy,et al.  The migration of the Desert Locust (Schistocerca gregaria Forsk.) I. The behaviour of swarms. II. A theory of long-range migrations , 1951, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[56]  J. C. Andre,et al.  Phil. Trans. R. Soc. Lond. B-1989-Andre-407-22-1 , 2014 .

[57]  Eric Warrant,et al.  Visual tracking in the dead of night , 2015, Science.

[58]  R. Farrow Interactions Between Synoptic Scale and Boundary-Layer Meteorology on Micro-Insect Migration , 1986 .

[59]  Wei Xian,et al.  Bat wing sensors support flight control , 2011, Proceedings of the National Academy of Sciences.

[60]  Willem Bouten,et al.  Wind selectivity and partial compensation for wind drift among nocturnally migrating passerines , 2012, Behavioral ecology : official journal of the International Society for Behavioral Ecology.

[61]  S. Dance,et al.  The accuracy of Doppler radar wind retrievals using insects as targets , 2010 .

[62]  Don R. Reynolds,et al.  Orientation at Night by High-Flying Insects , 1986 .

[63]  R. Gegear,et al.  A magnetic compass aids monarch butterfly migration , 2014, Nature Communications.

[64]  Sidney A. Gauthreaux Radar Entomology: Observing Insect Flight and Migration V. Alistair Drake Don R. Reynolds , 2013, Animal Behaviour.

[65]  Sabrina Fossette,et al.  Current-Oriented Swimming by Jellyfish and Its Role in Bloom Maintenance , 2015, Current Biology.

[66]  Collective orientation by nocturnally migrating australian plague locusts, Chortoicetes terminifera (Walker) (Orthoptera: Acrididae): a radar study , 1983 .

[67]  Thomas Alerstam,et al.  Convergent patterns of long-distance nocturnal migration in noctuid moths and passerine birds , 2011, Proceedings of the Royal Society B: Biological Sciences.

[68]  K. Horton,et al.  Wind drift explains the reoriented morning flights of songbirds , 2016 .

[69]  E. Warrant,et al.  Colour Vision in Diurnal and Nocturnal Hawkmoths1 , 2003, Integrative and comparative biology.