Flying animals need to accurately detect, identify and track fast-moving objects and these behavioral requirements are likely to strongly select for abilities to resolve visual detail in time. However, evidence of highly elevated temporal acuity relative to non-flying animals has so far been confined to insects while it has been missing in birds. With behavioral experiments on three wild passerine species, blue tits, collared and pied flycatchers, we demonstrate temporal acuities of vision far exceeding predictions based on the sizes and metabolic rates of these birds. This implies a history of strong natural selection on temporal resolution. These birds can resolve alternating light-dark cycles at up to 145 Hz (average: 129, 127 and 137, respectively), which is ca. 50 Hz over the highest frequency shown in any other vertebrate. We argue that rapid vision should confer a selective advantage in many bird species that are ecologically similar to the three species examined in our study. Thus, rapid vision may be a more typical avian trait than the famously sharp vision found in birds of prey.
Funding: Financial support was provided by Carl Trygger’s Foundation (grant numbers CTS 09: 425 and CTS10: 432, to AÖ; URL: http://www.carltryggersstiftelse.se ), The Swedish Research Council Formas (grant number 22-2007-729, to AÖ; URL: http://www.formas.se ) and The Swedish Research Council (grant number 621-2012-3722, to AQ; URL: http://www.vr.se ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Copyright: © 2016 Boström et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Results and Discussion
We have performed behavioral experiments to estimate temporal resolution of the complete visual pathway in three species of small passerine birds: blue tit (Cyanistes caeruleus), collared flycatcher (Ficedula albicollis) and pied flycatcher (F. hypoleuca). We used an operant conditioning approach in which the birds were trained and tested for the task of distinguishing flickering from constant stimuli produced by LED-arrays simulating daylight. Flickering and constant lamps became indistinguishable at frequencies of up to 131 Hz for blue tits (Fig 1), 141 Hz for collared flycatchers and 146 Hz for pied flycatchers (Fig 2). All three species had the highest flicker fusion frequencies (the critical flicker fusion frequency: CFF) at the same light intensity, 1500 cdm-2. The average CFFs of these species, 130.3 ± 0.94 Hz (±SD) in three blue tits, 128.1 ± 9.8 Hz in seven collared flycatchers and 138.2 ± 6.5 Hz in eight pied flycatchers, are clearly higher than those of humans (around 50–100 Hz depending on stimulus size [1]) and around 40 Hz higher than for any other vertebrate tested to date [2, 3].
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TIFF original image Download: Fig 1. Flicker fusion frequencies for blue tits by three different light stimuli intensities. Averages and ranges are shown with filled circles and brackets, respectively. Twelve individual blue tits were tested once at one of the light intensities 750, 1500 (n = 3) and 3000 cdm-2 (n = 6). The critical flicker fusion frequency (CFF), with a maximum of 131 Hz and 130.3 ± 0.94 Hz (±SD) on average, was reached at 1500 cdm-2. https://doi.org/10.1371/journal.pone.0151099.g001
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