The Earth’s Magnetic Field and Visual Landmarks Steer Migratory Flight Behavior in the Nocturnal Australian Bogong Moth

Like many birds [1], numerous species of nocturnal moths undertake spectacular long-distance migrations at night [2]. Each spring, billions of Bogong moths (Agrotis infusa) escape hot conditions in different regions of southeast Australia by making a highly directed migration of over 1,000 km to a limited number of cool caves in the Australian Alps, historically used for aestivating over the summer [3, 4]. How moths determine the direction of inherited migratory trajectories at night and locate their destination (i.e., navigate) is currently unknown [5-7]. Here we show that Bogong moths can sense the Earth's magnetic field and use it in conjunction with visual landmarks to steer migratory flight behavior. By tethering migrating moths in an outdoor flight simulator [8], we found that their flight direction turned predictably when dominant visual landmarks and a natural Earth-strength magnetic field were turned together, but that the moths became disoriented within a few minutes when these cues were set in conflict. We thus conclude that Bogong moths, like nocturnally migrating birds [9], can use a magnetic sense. Our results represent the first reliable demonstration of the use of the Earth's magnetic field to steer flight behavior in a nocturnal migratory insect.

[1]  R. B. Pinter,et al.  What causes edge fixation in walking flies? , 1990, The Journal of experimental biology.

[2]  R. Cardé Animal Migration: Seasonal Reversals of Migrant Moths , 2008, Current Biology.

[3]  James J. Foster,et al.  A Snapshot-Based Mechanism for Celestial Orientation , 2016, Current Biology.

[4]  R. Muheim,et al.  A New View on an Old Debate: Type of Cue-Conflict Manipulation and Availability of Stars Can Explain the Discrepancies between Cue-Calibration Experiments with Migratory Songbirds , 2016, Front. Behav. Neurosci..

[5]  Henrik Mouritsen,et al.  The Radical-Pair Mechanism of Magnetoreception. , 2016, Annual review of biophysics.

[6]  P. Berthold,et al.  Bird Migration: A General Survey , 2002 .

[7]  W. Wiltschko,et al.  Magnetic Compass of European Robins , 1972, Science.

[8]  W. Cochran,et al.  Migrating Songbirds Recalibrate Their Magnetic Compass Daily from Twilight Cues , 2004, Science.

[9]  E. Batschelet Circular statistics in biology , 1981 .

[10]  H. Mouritsen,et al.  Night-migratory garden warblers can orient with their magnetic compass using the left, the right or both eyes , 2010, Journal of The Royal Society Interface.

[11]  H. Mouritsen,et al.  A magnetic compass that might help coral reef fish larvae return to their natal reef , 2016, Current Biology.

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

[13]  Eric J. Warrant,et al.  The remarkable visual capacities of nocturnal insects: vision at the limits with small eyes and tiny brains , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[14]  Sönke Johnsen,et al.  The physics and neurobiology of magnetoreception , 2005, Nature Reviews Neuroscience.

[15]  Stanley Heinze,et al.  Sun Compass Integration of Skylight Cues in Migratory Monarch Butterflies , 2011, Neuron.

[16]  G. Sword,et al.  Behavioral evidence for a magnetic sense in the oriental armyworm, Mythimna separata , 2017, Biology Open.

[17]  K. Lohmann,et al.  A Light-Independent Magnetic Compass in the Leatherback Sea Turtle. , 1993, The Biological bulletin.

[18]  I. Common A study of the ecology of the adult bogong moth, Agrotis Infusa (Boisd) (Lepidoptera: Noctuidae), with special reference to its behaviour during migration and aestivation. , 1954 .

[19]  R. B. Srygley,et al.  Experimental evidence for a magnetic sense in Neotropical migrating butterflies (Lepidoptera: Pieridae) , 2006, Animal Behaviour.

[20]  O. Güntürkün,et al.  The Neural Basis of Long-Distance Navigation in Birds. , 2016, Annual review of physiology.

[21]  S. Åkesson,et al.  Polarized Light Cues Underlie Compass Calibration in Migratory Songbirds , 2006, Science.

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

[23]  H. Mouritsen,et al.  Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird , 2014, Nature.

[24]  Oliveira,et al.  Do neotropical migrant butterflies navigate using a solar compass? , 1998, The Journal of experimental biology.

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

[26]  B. Frost,et al.  Do monarch butterflies use polarized skylight for migratory orientation? , 2005, Journal of Experimental Biology.

[27]  H. Mouritsen,et al.  The quantum needle of the avian magnetic compass , 2016, Proceedings of the National Academy of Sciences.

[28]  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.

[29]  B. Frost,et al.  The Australian Bogong Moth Agrotis infusa: A Long-Distance Nocturnal Navigator , 2016, Front. Behav. Neurosci..

[30]  Janice G. Mather,et al.  Magnetic compass sense in the large yellow underwing moth, Noctua pronuba L. , 1982, Animal Behaviour.

[31]  H. Mouritsen Magnetoreception in birds and its use for long-distance migration , 2022, Sturkie's Avian Physiology.

[32]  H. Mouritsen,et al.  Weak Broadband Electromagnetic Fields are More Disruptive to Magnetic Compass Orientation in a Night-Migratory Songbird (Erithacus rubecula) than Strong Narrow-Band Fields , 2016, Front. Behav. Neurosci..

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

[34]  J. Kirschvink,et al.  Uniform magnetic fields and double-wrapped coil systems: improved techniques for the design of bioelectromagnetic experiments. , 1992, Bioelectromagnetics.

[35]  Steven M. Reppert,et al.  Illuminating the Circadian Clock in Monarch Butterfly Migration , 2003, Science.

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

[37]  B. R. Moore,et al.  A modification of the Rayleigh test for vector data , 1980 .

[38]  K. Green Migratory Bogong Moths (Agrotis Infusa) Transport Arsenic and Concentrate It to Lethal Effect by Estivating Gregariously in Alpine Regions of The Snowy Mountains of Australia , 2008 .