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Low-resolution vision in a velvet worm (Onychophora)

Kirwan, John D. LU ; Graf, Josefine ; Smolka, Jochen LU ; Mayer, Georg ; Henze, Miriam J. LU and Nilsson, Dan Eric LU (2018) In Journal of Experimental Biology 221(11).
Abstract

Onychophorans, also known as velvet worms, possess a pair of simple lateral eyes, and are a key lineage with regard to the evolution of vision. They resemble ancient Cambrian forms, and are closely related to arthropods, which boast an unrivalled diversity of eye designs. Nonetheless, the visual capabilities of onychophorans have not been well explored. Here, we assessed the spatial resolution of the onychophoran Euperipatoides rowelli using behavioural experiments, three-dimensional reconstruction, anatomical and optical examinations, and modelling. Exploiting their spontaneous attraction towards dark objects, we found that E. rowelli can resolve stimuli that have the same average luminance as the background. Depending on the assumed... (More)

Onychophorans, also known as velvet worms, possess a pair of simple lateral eyes, and are a key lineage with regard to the evolution of vision. They resemble ancient Cambrian forms, and are closely related to arthropods, which boast an unrivalled diversity of eye designs. Nonetheless, the visual capabilities of onychophorans have not been well explored. Here, we assessed the spatial resolution of the onychophoran Euperipatoides rowelli using behavioural experiments, three-dimensional reconstruction, anatomical and optical examinations, and modelling. Exploiting their spontaneous attraction towards dark objects, we found that E. rowelli can resolve stimuli that have the same average luminance as the background. Depending on the assumed contrast sensitivity of the animals, we estimate the spatial resolution to be in the range 15-40 deg. This results from an arrangement where the cornea and lens project the image largely behind the retina. The peculiar ellipsoid shape of the eye in combination with the asymmetric position and tilted orientation of the lens may improve spatial resolution in the forward direction. Nonetheless, the unordered network of interdigitating photoreceptors, which fills the whole eye chamber, precludes high-Acuity vision. Our findings suggest that adult specimens of E. rowelli cannot spot or visually identify prey or conspecifics beyond a few centimetres from the eye, but the coarse spatial resolution that the animals exhibited in our experiments is likely to be sufficient to find shelter and suitable microhabitats from further away. To our knowledge, this is the first evidence of resolving vision in an onychophoran.

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author
; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Euperipatoides rowelli, Eye, Object taxis, Spatial resolution, Vision, Visually guided behaviour
in
Journal of Experimental Biology
volume
221
issue
11
article number
175802
publisher
The Company of Biologists Ltd
external identifiers
  • pmid:29626113
  • scopus:85048309444
ISSN
0022-0949
DOI
10.1242/jeb.175802
language
English
LU publication?
yes
id
ffd740c3-5fdd-499b-8095-d58daf074d57
date added to LUP
2018-06-26 15:30:51
date last changed
2024-04-15 08:37:34
@article{ffd740c3-5fdd-499b-8095-d58daf074d57,
  abstract     = {{<p>Onychophorans, also known as velvet worms, possess a pair of simple lateral eyes, and are a key lineage with regard to the evolution of vision. They resemble ancient Cambrian forms, and are closely related to arthropods, which boast an unrivalled diversity of eye designs. Nonetheless, the visual capabilities of onychophorans have not been well explored. Here, we assessed the spatial resolution of the onychophoran Euperipatoides rowelli using behavioural experiments, three-dimensional reconstruction, anatomical and optical examinations, and modelling. Exploiting their spontaneous attraction towards dark objects, we found that E. rowelli can resolve stimuli that have the same average luminance as the background. Depending on the assumed contrast sensitivity of the animals, we estimate the spatial resolution to be in the range 15-40 deg. This results from an arrangement where the cornea and lens project the image largely behind the retina. The peculiar ellipsoid shape of the eye in combination with the asymmetric position and tilted orientation of the lens may improve spatial resolution in the forward direction. Nonetheless, the unordered network of interdigitating photoreceptors, which fills the whole eye chamber, precludes high-Acuity vision. Our findings suggest that adult specimens of E. rowelli cannot spot or visually identify prey or conspecifics beyond a few centimetres from the eye, but the coarse spatial resolution that the animals exhibited in our experiments is likely to be sufficient to find shelter and suitable microhabitats from further away. To our knowledge, this is the first evidence of resolving vision in an onychophoran.</p>}},
  author       = {{Kirwan, John D. and Graf, Josefine and Smolka, Jochen and Mayer, Georg and Henze, Miriam J. and Nilsson, Dan Eric}},
  issn         = {{0022-0949}},
  keywords     = {{Euperipatoides rowelli; Eye; Object taxis; Spatial resolution; Vision; Visually guided behaviour}},
  language     = {{eng}},
  month        = {{06}},
  number       = {{11}},
  publisher    = {{The Company of Biologists Ltd}},
  series       = {{Journal of Experimental Biology}},
  title        = {{Low-resolution vision in a velvet worm (Onychophora)}},
  url          = {{http://dx.doi.org/10.1242/jeb.175802}},
  doi          = {{10.1242/jeb.175802}},
  volume       = {{221}},
  year         = {{2018}},
}