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Draft:Eric James Warrant

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Eric James Warrant
Born7 March 1962
Gosford, New South Wales, Australia
Alma materAustralian National University (PhD, 1990), University of New South Wales (1984)
Known forVision, navigation, and migration of nocturnal insects
AwardsDela med Dig Prize for Science Communication (2021), PROSE Award for Textbook/Biological and Life Sciences (2015), Ig-Nobel Prize in Biology and Astronomy (2013), Short-List, Körber European Science Prize (2006)
Scientific career
FieldsVisual ecology, nocturnal vision, animal navigation, animal migration

Eric James Warrant, PhD (born 7 March 1962) is an Australian-Swedish neuroethologist known for his entomological research on how the optics of eyes are optimized for life at different light levels.[1] His work concerns the vision and visual navigation of nocturnal insects and the sensory basis of long-distance nocturnal migration. He is currently a Professor of Functional Zoology at Lund University in Sweden.[1]

Early Life and Career

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Warrant was born in Gosford, New South Wales, Australia and grew up on the edge of a coastal rainforest north of Sydney, where he first discovered his love of insects.[1][2][3]

Warrant completed a double honors degree in physics and entomology in 1984 at the University of New South Wales.[3] He finished his PhD in neurobiology at Australian National University in 1990, working under the supervision of George Adrian Horridge and Peter McIntyre to study arthropod vision.[2] His thesis was on the optics of arthropod superposition compound eyes.[2] He used several species of South African dung beetles from the genus Onitis as model organisms.[2]

From 1990 to 1992, Warrant was a postdoctoral fellow under Dan-Eric Nilsson at Lund University.[3] His work concerned how the eyes of nocturnal animals are optimized to improve dim-light vision, and how early and higher stages of visual processing might improve visual performance at night.[3] He stayed on as a research fellow until 1997.[1] He became a Professor of Zoology at Lund University in 2002.[1] In 2010, he became a visiting professor at the Research School of Biology at Australian National University, and a visiting fellow there in 2018.[1] He has worked as an adjunct professor at University of South Australia since 2018, and became the head of the Division of Sensory Biology there in 2024.[1]

Warrant is a founding member of the Lund Vision Group researching comparative vision, and became their leader in 2022.[2][3] There, he investigates the design and evolution of eyes, how they adapt to different habitats, and how vision and the senses are used in navigation and controlling behavior.[4] Warrant is also a member of eSSENCE, the e-Science Collaboration on computational research organized by the universities of Uppsala, Lund, and Umeå.[2][5]

He founded and directed the Solander Program from 2005 until 2017, a research exchange program between 21 universities in Sweden, Australia, and New Zealand, the Universities of Lund, Melbourne, Queensland, New South Wales, and Auckland.[1]

Research

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Key discoveries:[1]

  1. First to determine nocturnal insects have extraordinary night vision despite having tiny eyes and brains, and that they rely on visual information to orient and navigate at night.
  2. Found some nocturnal insects possess trichromatic color vision, necessary to find flowers at night.
  3. Illustrated some nocturnal insects use visual landmarks to navigate home after a long foraging trip at night, and some use the weak pattern of polarized light that forms around the moon to maintain a straight-line course. If the moon is absent, they instead rely on the broad band of light in the Milky Way.
  4. Discovered the Bogong moth uses the earth's magnetic field and the stars as compasses to reach its final migration destination, a place it has never previously been.
  5. Demonstrated the visual abilities of nocturnal insects are based on neuronal summation mechanisms in the brain, a processing strategy that significantly increases the reliability of vision in dim light by summing light in time and space to enhance the perception of slower and coarser visual details while maintaining color information. This real-time processing strategy was implemented in camera technology.

South African Dung Beetle Onitis

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Warrant completed his PhD on the optics of arthropod superposition compound eyes, which are designed to gather and focus more light from multiple facets on the eye called ommatidia onto a single point on the retina. This lends to more light sensitivity and is ideal for nocturnal environments.

Arthropod Eye Design[6]

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The arthropod eye is designed to detect changes in its environment that may impact reproduction, feeding, or escape. Due to the large variations in the type and quantity of light available in arthropod habitats, the arthropod visual system differs across genus and even species. Warrant conducted in-depth research on arthropod eye design, identifying principle design parameters such as eye size, eye shape, visual field size, pupil size, spectral and polarization sensitivity among many species. He extensively examined the effect of physical constraints such as lens size, focal length, and structure of ommatidium, rhabdoms, and crystalline cones on the vision of arthropods and how they navigate their world. His work underlined the importance of adequate sensitivity to light and adequate spatial resolving power in allowing arthropods to perform the visual tasks necessary for survival.

Optical Maturation[7][8]

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Warrant found that beetle eye maturation proceeds quickly during the first 3 days following ecdysis. Full maturation is usually attained by the end of the second week of development. This is done to sharpen the blur-circle on the retina and improve vision by focusing light striking the retina on target rhabdoms to produce clearer images. This is especially important at night to navigate and avoid predators. According to Warrant, the Onitis has neither an exceptionally sensitive eye nor very poor resolution compared to other species, likely due to its environment being crepuscular. He also described that the quality of the retinal image in the Onitis beetle is matched to the spacing of the photoreceptors in the retina. The arrangement and density of the photoreceptors are optimized to provide the amount of detail and visual information that the beetle's visual processing system can accommodate.

Limitations to Resolution[6]

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Warrant determined that the quality of light available, imperfect optics, and imperfect vision limit spatial resolution in the arthropod eye. Regarding quality of light, he found that species with longer photoreceptors and wider pupils tend to be more sensitive to point source stimulation, while those with smaller pupils and photoreceptors–– especially if they are diurnal–– tend to have an intrinsically reduced response to each absorbed photon than those with larger pupils and photoreceptors. On imperfect optics, aberrations and diffraction provide sources of imperfection in viewed images. The more extensive these imperfections, the more degraded the image formed on the retina and the less resolved the image perceived. Finally, a retina is imperfect because of the inability of each rhabdom to unambiguously determine what rays of light it absorbs actually originate from its own angle of visual space. Cross-absorption of light between rhabdoms that aren't shielded by light-absorbing pigment granules, which keep reflections internal, also cause lower spatial resolution.

Deep Sea Animals[9][10]

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Warrant determined that the eyes of deep sea fish generally become smaller and less sensitive to point sources of light, such as bioluminescence, with increasing depth. He found that at all depths, the eyes of animals active on and over the nutrient-rich sea floor are generally larger than the eyes of pelagic species, or those that live in more open waters. He also discovered that the retinal ganglion cells of sea-floor species frequently arranged in a horizontal visual streak along the retina. He determined this adaptation is for viewing the wide, flat horizon of the sea floor and all the animals living there.

Visual Performance in Nocturnal Insects

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Warrant has made significant contributions to the study of visual performance and color vision at night in the European elephant hawkmoth Deiliphila elpenor and the Central American sweat bee Megalopta genalis.

European Elephant Hawkmoth Deiliphila elpenor[11][12][13]

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The elephant hawkmoth Deiliphila elpenor can see in low-light conditions and has trichromatic color vision, allowing it to forage nectar from nocturnal flowers.[11] Warrant and his research group were the first to claim that D. elpenor uses color vision for object discrimination at nocturnal intensities.[12] He first determined that the hawkmoth can discriminate blue and yellow from all shades of grey at most light intensities, using color rather than achromatic cues to feed from flowers at dusk.[12] In testing this, he simultaneously showed D. Elpenor has color constancy. He also showed that this moth's color vision works at much lower light intensities than that of humans, who are not able to discern shades of blue or yellow as accurately in the same light intensities.[12] Warrant confirmed this is due to D. elpenor's large superposition compound eyes and neural summation mechanisms, which increase contrast sensitivity and visual information rate over large ranges of light intensity.[12][13] This is at the cost of resolution.[13]

Central American Sweat Bee Megalopta genalis[14][15]

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The Megalopta genalis is a species of nocturnal bee that has low-light and trichromatic color vision, allowing it to locate flowers and navigate night.[14] Warrant was the first to provide anatomical and physiological evidence of polarization vision in the M. genalis for use in navigation.[14] Polarization vision is the ability to detect the electric field component of light that oscillates in parallel planes; insects often detect this pattern and use it as a compass.[14] He found that the bee has wide rhabdoms fit for a wide spatial receptive field, and that the microvilli within the rhabdoms are specifically adapted to the unidirectional polarization pattern occurring at twilight.[14] He also determined that this bee has an anatomically distinct dorsal rim area, a specialized region of the compound eye containing a specific arrangement of ommatidia sensitive to polarized light at low light intensities. He found a high sensitivity in this dorsal rim area that optimized the signal-to-noise ratio of incoming light, allowing the bee to effectively filter out interfering effects from skylight present during its activity periods.[14] This allows color discrimination in dim light using sensory matched filters.[16] Warrant compared the eyes of the M. genalis to the compound eyes of the worker honeybees Apis mellifera and the diurnal halictid bee Lasioglossum leucozonium. He found the M. genalis exhibits specific retinal and optical adaptations for dim-light vision.[15] These include larger ommatidia, wider rhabdoms, and additional neuronal summation mechanisms in the retina allowing the M. genalis to sum signals from large groups of ommatidia better than those of the diurnal bees.[15]

Nocturnal Navigation and Migration

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South African Dung Beetle Onitis

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In 1996, Warrant participated in a scarab biology conference in South Africa that led to a project on the visual orientation of nocturnal and diurnal ball-rollers.[2] He and Marie Dacke, then a PhD student, discovered the celestial compass systems that dung beetles use to hold a straight rolling course.[17][18] Dung beetles orient themselves using the position of the stars and moon, as well as polarized light patterns formed around the moon, which enable them to maintain a straight trajectory while ball-rolling and orienting themselves.[19] They earned an Ig Nobel Prize for their work in 2013.

Warrant also was the first to demonstrate that the celestial cue preference differs between nocturnal and diurnal beetles in a way that reflects their visual ecologies.[20] Nocturnal beetles primarily used polarized skylight from the moon to orient themselves, but when forced to ball-roll during the day, they instead use the sun itself as their primary orientation cue rather than its polarized light.[20] This is in contrast to diurnal beetles, which use a celestial body for their compass regardless of the time of day and do not rely on polarized light.[20] This is reflected in the compass neurons in the brains of these beetles; compass neurons in diurnal beetles are tuned only to the sun, while the same neurons in nocturnal species switch exclusively to polarized light at lunar light intensities.[20] These neurons are thus responsible for encoding preferences for particular celestial cues and are dynamic according to light conditions.[20]

Central American Sweat Bee Megalopta genalis[21]

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Megalopta genalis is able to navigate home under a forest canopy at light intensities ten times dimmer than starlight by memorizing visual landmarks around the nest entrance in its frontal visual field. Warrant and his research group were the first to demonstrate that the M. genalis is also able to distinguish dorsal landmarks during homing by using local foliage patterns created by the canopy against the brighter sky.

Australian Bogong Moth Agrotis infusa

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During the Bogong month's annual migration, it travels from all over southeast Australia toward a small number of alpine caves in the Australian Alps, aggregating in large numbers despite never having previously been there.[22][23] Warrant discovered that the Bogong moths use the starry night sky as a compass to distinguish geographical cardinal directions and steer migration in their inherited migratory direction.[24] They are the first invertebrate known with this ability.[22] He determined the moth's celestial compass by tethering spring and autumn migratory moths in a flight simulator. He found that under naturalistic moonless night skies and in a nulled geomagnetic field to disable the moth's known magnetic sense, the moths fly in their seasonally appropriate migratory directions.[24] He also found that visual interneurons in different regions of the moth brain respond specifically to rotations of the night sky and were tuned to a common sky orientation, firing maximally when the moth headed southward–– its appropriate direction.[24] Warrant suggested from this that the Bogong moth uses stellar cues and the Earth's magnetic field to create a robust compass system for long-distance nocturnal navigation.[24]

Technological Developments

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Dim-light Camera Imaging[25]

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Alongside Almut Kelber, Anna Stöckl, and David O'Carroll, Warrant determined the optical and neural principles nocturnal insects use to see color at night, navigate to and from their home bases in a dark environment, and detect optic flow during flight. The visual abilities of these insects are based on neuronal summation mechanisms in the brain, a processing strategy that increases the reliability of vision in dim light by summing light in time and space. This enhances the perception of slower and coarser visual details while maintaining color information. Warrant and his group converted these principles into computer vision algorithms in collaboration with Toyota to dramatically improve dim-light camera imaging.

LIDAR[26]

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LIDAR, or Light Detection and Ranging, is a remote sensing technology that uses laser pulses to measure distances and create high-resolution maps. Warrant developed the usage of LIDAR to monitor flight activities and migration of nocturnal moths.

Remote Infrared Microscopy[27]

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Warrant determined that since infrared light doesn't resolve surface roughness, the wings of moths appear glossy at longer wavelengths, which is a property that provides a unique reflectance spectra between species. This spectra could be used for remote identification of free-flying moth species over considerable distances.

Honors and decorations[1]

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  1. Vice Chairman –– National Committee for Biology, Royal Swedish Academy of Sciences (2008–2017)
  2. Advisory Board; Senior Editorial Board –– Journal of Comparative Physiology A (2008–2020; 2020)
  3. President –– Royal Physiographic Society in Lund, Sweden (2025)
  4. Academic Editorial Board –– Proceedings of the Royal Society B: Biological Sciences (2014)
  5. Executive Committee –– International Society of Neuroethology, Lawrence, USA (2016–2024)
  6. President –– International Society of Neuroethology, Lawrence, USA (2019–2024)
  7. Chairman –– Committee for Organismic Biology, Swedish Research Council (2017–2020)
  8. The Short-List, Körber European Science Prize (2006)
  9. Foreign Fellow –– Royal Danish Academy of Sciences and Letters, Denmark (2008)
  10. Ig-Nobel Prize in Biology and Astronomy –– Annals of Improbable Research, Cambridge, USA (2013)
  11. PROSE Award for Textbook/Biological and Life Sciences –– Association of American Publishers, Washington, D.C. (2015)
  12. President –– Academic Society of Lund, Sweden (2019)
  13. Dela med Dig Prize for Science Communication –– Swedish Research Council (2021)

Bibliography[28][29][30]

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Co-authored Books

  • Warrant, E., & Nilsson, D.-E. (Eds.). (2006). Invertebrate vision. Cambridge University Press.
  • Cronin, T. W. (2014). Visual ecology. Princeton University Press.
  • Emde, G. von der, & Warrant, E. (Eds.). (2016). The ecology of animal senses: Matched filters for economical sensing. Springer.

References

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  1. ^ a b c d e f g h i j "Curriculum Vitae Professor Dr. Eric J. Warrant" (PDF).
  2. ^ a b c d e f g Zupanc, Günther K. H.; Homberg, Uwe; Helfrich-Förster, Charlotte; Warrant, Eric J.; Simmons, Andrea Megela (2024-03-01). "One hundred years of excellence: the top one hundred authors of the Journal of Comparative Physiology A". Journal of Comparative Physiology A. 210 (2): 109–144. doi:10.1007/s00359-024-01699-1. ISSN 1432-1351. PMC 10995051. PMID 38551673.
  3. ^ a b c d e Warrant, Eric J. (2024-03-01). "A formative journal for a formative career: a personal recollection of how JCPA has inspired and guided my research life". Journal of Comparative Physiology A. 210 (2): 203–210. doi:10.1007/s00359-023-01683-1. ISSN 1432-1351. PMC 10994867. PMID 38082048.
  4. ^ "Lund Vision Group". Lund University. Retrieved 2024-11-18.
  5. ^ "eSSENCE: The e-Science Collaboration". Lund University. Retrieved 2024-11-18.
  6. ^ a b Warrant, Eric J.; McIntyre, Peter D. (1993-04-01). "Arthropod eye design and the physical limits to spatial resolving power". Progress in Neurobiology. 40 (4): 413–461. doi:10.1016/0301-0082(93)90017-M. ISSN 0301-0082. PMID 8446759.
  7. ^ Warrant, Eric J.; McIntyre, Peter D.; Caveney, Stanley (1990-12-01). "Maturation of optics and resolution in adult dung beetle superposition eyes". Journal of Comparative Physiology A. 167 (6): 817–825. doi:10.1007/BF00189770. ISSN 1432-1351.
  8. ^ Warrant, Eric J.; McIntyre, Peter D. (1990-12-01). "Limitations to resolution in superposition eyes". Journal of Comparative Physiology A. 167 (6): 785–803. doi:10.1007/BF00189768. ISSN 1432-1351.
  9. ^ Warrant, Eric (2004-10-01). "Vision in the dimmest habitats on Earth". Journal of Comparative Physiology A. 190 (10): 765–789. doi:10.1007/s00359-004-0546-z. ISSN 1432-1351.
  10. ^ Warrant, Eric J.; Locket, N. Adam (2007-03-15). "Vision in the deep sea". Biological Reviews. 79 (3): 671–712. doi:10.1017/S1464793103006420. ISSN 1464-7931. PMID 15366767.
  11. ^ a b Warrant, Eric; Somanathan, Hema (2022-10-24). "Colour vision in nocturnal insects". Philosophical Transactions of the Royal Society B: Biological Sciences. 377 (1862). doi:10.1098/rstb.2021.0285. ISSN 0962-8436. PMC 9441242. PMID 36058247.
  12. ^ a b c d e Stöckl, Anna Lisa; O'Carroll, David Charles; Warrant, Eric James (2016-03-21). "Neural Summation in the Hawkmoth Visual System Extends the Limits of Vision in Dim Light". Current Biology: CB. 26 (6): 821–826. doi:10.1016/j.cub.2016.01.030. ISSN 1879-0445. PMID 26948877.
  13. ^ a b c Kelber, Almut; Balkenius, Anna; Warrant, Eric J. (2002-10-31). "Scotopic colour vision in nocturnal hawkmoths". Nature. 419 (6910): 922–925. doi:10.1038/nature01065. ISSN 0028-0836. PMID 12410310.
  14. ^ a b c d e f Greiner, Birgit; Cronin, Thomas W.; Ribi, Willi A.; Wcislo, William T.; Warrant, Eric J. (2007-06-01). "Anatomical and physiological evidence for polarisation vision in the nocturnal bee Megalopta genalis". Journal of Comparative Physiology A. 193 (6): 591–600. doi:10.1007/s00359-007-0214-1. ISSN 1432-1351. PMID 17530313.
  15. ^ a b c Greiner, Birgit; Ribi, Willi A.; Warrant, Eric J. (2004-04-03). "Retinal and optical adaptations for nocturnal vision in the halictid bee Megalopta genalis". Cell and Tissue Research. 316 (3): 377–390. doi:10.1007/s00441-004-0883-9. ISSN 0302-766X. PMID 15064946.
  16. ^ Warrant, Eric J. (2016-10-24). "Sensory matched filters". Current Biology: CB. 26 (20): R976–R980. doi:10.1016/j.cub.2016.05.042. ISSN 1879-0445. PMID 27780072.
  17. ^ Dacke, Marie; Byrne, Marcus; Smolka, Jochen; Warrant, Eric; Baird, Emily (2013-01-01). "Dung beetles ignore landmarks for straight-line orientation". Journal of Comparative Physiology A. 199 (1): 17–23. doi:10.1007/s00359-012-0764-8. ISSN 1432-1351. PMID 23076443.
  18. ^ Byrne, Marcus; Dacke, Marie; Nordström, Peter; Scholtz, Clarke; Warrant, Eric (2003-06-01). "Visual cues used by ball-rolling dung beetles for orientation". Journal of Comparative Physiology A. 189 (6): 411–418. doi:10.1007/s00359-003-0415-1. ISSN 1432-1351. PMID 12728329.
  19. ^ Dacke, Marie; Byrne, Marcus J.; Scholtz, Clarke H.; Warrant, Eric J. (2004-02-22). "Lunar orientation in a beetle". Proceedings of the Royal Society of London. Series B: Biological Sciences. 271 (1537): 361–365. doi:10.1098/rspb.2003.2594. ISSN 0962-8452. PMC 1691606. PMID 15101694.
  20. ^ a b c d e Jundi, Basil el; Warrant, Eric J.; Byrne, Marcus J.; Khaldy, Lana; Baird, Emily; Smolka, Jochen; Dacke, Marie (2015-08-24). "Neural coding underlying the cue preference for celestial orientation". Proceedings of the National Academy of Sciences of the United States of America. 112 (36): 11395–11700. doi:10.1073/pnas.1501272112. PMC 4568659. PMID 26305929.
  21. ^ Chaib, Sandra; Dacke, Marie; Wcislo, William; Warrant, Eric (2021-08-23). "Dorsal landmark navigation in a Neotropical nocturnal bee". Current Biology: CB. 31 (16): 3601–3605.e3. doi:10.1016/j.cub.2021.05.029. ISSN 1879-0445. PMID 34115977.
  22. ^ a b "Eric Warrant - My Story - iMagazine". www.ikfoundation.org. Retrieved 2024-11-18.
  23. ^ "Nocturnal navigators". butterfly-conservation.org. 2023-08-26. Retrieved 2024-11-18.
  24. ^ a b c d Warrant, Eric; Dreyer, David; Adden, Andrea; Chen, Hui; Frost, Barrie; Mouritsen, Henrik; Xu, Jingjing; Green, Ken; Whitehouse, Mary (2024-05-16), Bogong moths use a stellar compass for long-distance navigation at night, doi:10.21203/rs.3.rs-4394686/v1, retrieved 2024-11-18
  25. ^ Warrant, Eric; Oskarsson, Magnus; Malm, Henrik (2014-08-19). "The Remarkable Visual Abilities of Nocturnal Insects: Neural Principles and Bioinspired Night-Vision Algorithms". Proceedings of the IEEE. 102 (10): 1411–1426. doi:10.1109/JPROC.2014.2332533. ISSN 0018-9219.
  26. ^ Chen, Hui; Li, Meng; Månefjord, Hampus; Travers, Paul; Salvador, Jacobo; Müller, Lauro; Dreyer, David; Alison, Jamie; Høye, Toke T.; Gao Hu; Warrant, Eric; Brydegaard, Mikkel (2024-05-17). "Lidar as a potential tool for monitoring migratory insects". iScience. 27 (5): 109588. doi:10.1016/j.isci.2024.109588. ISSN 2589-0042. PMC 11031831. PMID 38646171.
  27. ^ Li, Meng; Seinsche, Clara; Jansson, Samuel; Hernandez, Julio; Rota, Jadranka; Warrant, Eric; Brydegaard, Mikkel (2022-06-22). "Potential for identification of wild night-flying moths by remote infrared microscopy". Journal of the Royal Society Interface. 19 (191). doi:10.1098/rsif.2022.0256. ISSN 1742-5662. PMC 9214284. PMID 35730175.
  28. ^ von Der Emde, Gerhard; Warrant, Eric, eds. (2016). The Ecology of Animal Senses. doi:10.1007/978-3-319-25492-0. ISBN 978-3-319-25490-6.
  29. ^ Cronin, Thomas W.; Johnsen, Sönke; Marshall, Justin; Warrant, Eric J. (2014-08-10). Visual Ecology. Princeton University Press. ISBN 978-1-4008-5302-1.
  30. ^ Warrant, Eric; Nilsson, Dan-Eric (2006-10-05). Invertebrate Vision. Cambridge University Press. ISBN 978-0-521-83088-1.
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