A Novel Interception Strategy in a Miniature Robber Fly with Extreme Visual Acuity

Trevor J. Wardill; Samuel T. Fabian; Ann C. Pettigrew; Doekele G. Stavenga; Karin Nordström; Paloma T. Gonzalez-Bellido

doi:10.1016/j.cub.2017.01.050

A Novel Interception Strategy in a Miniature Robber Fly with Extreme Visual Acuity

Trevor J. Wardill, Samuel T. Fabian, Ann C. Pettigrew, Doekele G. Stavenga, Karin Nordström, Paloma T. Gonzalez-Bellido

Research output: Contribution to journal › Article › peer-review

71 Scopus citations

Abstract

Our visual system allows us to rapidly identify and intercept a moving object. When this object is far away, we base the trajectory on the target's location relative to an external frame of reference [1]. This process forms the basis for the constant bearing angle (CBA) model, a reactive strategy that ensures interception since the bearing angle, formed between the line joining pursuer and target (called the range vector) and an external reference line, is held constant [2–4]. The CBA model may be a fundamental and widespread strategy, as it is also known to explain the interception trajectories of bats and fish [5, 6]. Here, we show that the aerial attack of the tiny robber fly Holcocephala fusca is consistent with the CBA model. In addition, Holcocephala fusca displays a novel proactive strategy, termed “lock-on” phase, embedded with the later part of the flight. We found the object detection threshold for this species to be 0.13°, enabled by an extremely specialized, forward pointing fovea (∼5 ommatidia wide, interommatidial angle Δφ = 0.28°, photoreceptor acceptance angle Δρ = 0.27°). This study furthers our understanding of the accurate performance that a miniature brain can achieve in highly demanding sensorimotor tasks and suggests the presence of equivalent mechanisms for target interception across a wide range of taxa.

Original language	English (US)
Pages (from-to)	854-859
Number of pages	6
Journal	Current Biology
Volume	27
Issue number	6
DOIs	https://doi.org/10.1016/j.cub.2017.01.050
State	Published - Mar 20 2017
Externally published	Yes

Bibliographical note

Funding Information:
This work was funded by the Air Force Office of Scientific Research (FA9550-15-1-0188 to P.T.G.-B. and K.N. and FA9550-15-1-0068 to D.G.S.), an Isaac Newton Trust/Wellcome Trust ISSF/University of Cambridge Joint Research Grant (097814/Z/11/Z) to P.T.G.-B., a Biotechnology and Biological Sciences Research Council David Phillips Fellowship (BBSRC, BB/L024667/1) to T.J.W., a Royal Society International Exchange Scheme grant to P.T.G.-B. (75166), a Swedish Research Council grant (2012-4740) to K.N., and a Shared Equipment Grant from the School of Biological Sciences (University of Cambridge, RG70368). The TEM images were obtained at the CAIC in Cambridge. We are thankful to Elke K. Buschbeck for providing technical and practical advice and for her generosity sharing her equipment to obtain the focal length measurements. We thank Michael Land, Rob Olberg, Claude Desplan, and Tom Cronin for helpful comments on the manuscript; Francis Velasquez for his continuous logistic support; staff at Nixon Park for supporting fieldwork; York College for kindly providing us access to their facilities; and Brian Jones for laser cutting assistance. We are thankful to Mary Sumner for fly tracking and data analysis support.

Publisher Copyright:
© 2017 The Author(s)

Keywords

flight
interception strategy
invertebrate
moving target
predation
retina
spatial resolution
tracking
vision

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title = "A Novel Interception Strategy in a Miniature Robber Fly with Extreme Visual Acuity",

abstract = "Our visual system allows us to rapidly identify and intercept a moving object. When this object is far away, we base the trajectory on the target's location relative to an external frame of reference [1]. This process forms the basis for the constant bearing angle (CBA) model, a reactive strategy that ensures interception since the bearing angle, formed between the line joining pursuer and target (called the range vector) and an external reference line, is held constant [2–4]. The CBA model may be a fundamental and widespread strategy, as it is also known to explain the interception trajectories of bats and fish [5, 6]. Here, we show that the aerial attack of the tiny robber fly Holcocephala fusca is consistent with the CBA model. In addition, Holcocephala fusca displays a novel proactive strategy, termed “lock-on” phase, embedded with the later part of the flight. We found the object detection threshold for this species to be 0.13°, enabled by an extremely specialized, forward pointing fovea (∼5 ommatidia wide, interommatidial angle Δφ = 0.28°, photoreceptor acceptance angle Δρ = 0.27°). This study furthers our understanding of the accurate performance that a miniature brain can achieve in highly demanding sensorimotor tasks and suggests the presence of equivalent mechanisms for target interception across a wide range of taxa.",

keywords = "flight, interception strategy, invertebrate, moving target, predation, retina, spatial resolution, tracking, vision",

author = "Wardill, {Trevor J.} and Fabian, {Samuel T.} and Pettigrew, {Ann C.} and Stavenga, {Doekele G.} and Karin Nordstr{\"o}m and Gonzalez-Bellido, {Paloma T.}",

note = "Funding Information: This work was funded by the Air Force Office of Scientific Research (FA9550-15-1-0188 to P.T.G.-B. and K.N. and FA9550-15-1-0068 to D.G.S.), an Isaac Newton Trust/Wellcome Trust ISSF/University of Cambridge Joint Research Grant (097814/Z/11/Z) to P.T.G.-B., a Biotechnology and Biological Sciences Research Council David Phillips Fellowship (BBSRC, BB/L024667/1) to T.J.W., a Royal Society International Exchange Scheme grant to P.T.G.-B. (75166), a Swedish Research Council grant (2012-4740) to K.N., and a Shared Equipment Grant from the School of Biological Sciences (University of Cambridge, RG70368). The TEM images were obtained at the CAIC in Cambridge. We are thankful to Elke K. Buschbeck for providing technical and practical advice and for her generosity sharing her equipment to obtain the focal length measurements. We thank Michael Land, Rob Olberg, Claude Desplan, and Tom Cronin for helpful comments on the manuscript; Francis Velasquez for his continuous logistic support; staff at Nixon Park for supporting fieldwork; York College for kindly providing us access to their facilities; and Brian Jones for laser cutting assistance. We are thankful to Mary Sumner for fly tracking and data analysis support. Publisher Copyright: {\textcopyright} 2017 The Author(s)",

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AU - Stavenga, Doekele G.

AU - Nordström, Karin

AU - Gonzalez-Bellido, Paloma T.

N1 - Funding Information: This work was funded by the Air Force Office of Scientific Research (FA9550-15-1-0188 to P.T.G.-B. and K.N. and FA9550-15-1-0068 to D.G.S.), an Isaac Newton Trust/Wellcome Trust ISSF/University of Cambridge Joint Research Grant (097814/Z/11/Z) to P.T.G.-B., a Biotechnology and Biological Sciences Research Council David Phillips Fellowship (BBSRC, BB/L024667/1) to T.J.W., a Royal Society International Exchange Scheme grant to P.T.G.-B. (75166), a Swedish Research Council grant (2012-4740) to K.N., and a Shared Equipment Grant from the School of Biological Sciences (University of Cambridge, RG70368). The TEM images were obtained at the CAIC in Cambridge. We are thankful to Elke K. Buschbeck for providing technical and practical advice and for her generosity sharing her equipment to obtain the focal length measurements. We thank Michael Land, Rob Olberg, Claude Desplan, and Tom Cronin for helpful comments on the manuscript; Francis Velasquez for his continuous logistic support; staff at Nixon Park for supporting fieldwork; York College for kindly providing us access to their facilities; and Brian Jones for laser cutting assistance. We are thankful to Mary Sumner for fly tracking and data analysis support. Publisher Copyright: © 2017 The Author(s)

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N2 - Our visual system allows us to rapidly identify and intercept a moving object. When this object is far away, we base the trajectory on the target's location relative to an external frame of reference [1]. This process forms the basis for the constant bearing angle (CBA) model, a reactive strategy that ensures interception since the bearing angle, formed between the line joining pursuer and target (called the range vector) and an external reference line, is held constant [2–4]. The CBA model may be a fundamental and widespread strategy, as it is also known to explain the interception trajectories of bats and fish [5, 6]. Here, we show that the aerial attack of the tiny robber fly Holcocephala fusca is consistent with the CBA model. In addition, Holcocephala fusca displays a novel proactive strategy, termed “lock-on” phase, embedded with the later part of the flight. We found the object detection threshold for this species to be 0.13°, enabled by an extremely specialized, forward pointing fovea (∼5 ommatidia wide, interommatidial angle Δφ = 0.28°, photoreceptor acceptance angle Δρ = 0.27°). This study furthers our understanding of the accurate performance that a miniature brain can achieve in highly demanding sensorimotor tasks and suggests the presence of equivalent mechanisms for target interception across a wide range of taxa.

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A Novel Interception Strategy in a Miniature Robber Fly with Extreme Visual Acuity

Abstract

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Keywords

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