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].

PPT PowerPoint slide

PowerPoint slide PNG larger image

larger image 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

PPT PowerPoint slide

PowerPoint slide PNG larger image

larger image TIFF original image Download: Fig 2. Flicker fusion frequencies for collared (closed diamonds) and pied flycatchers (open squares). Averages are shown together with ranges (brackets). Seven collared and eight pied flycatchers were repeatedly tested at up to five different light intensities each: 160 (n = 5 collared + 4 pied), 350 (n = 7 + 4), 750, 1500 (n = 7 + 8) and 3500 cdm-2 (n = 6 + 7). The critical flicker fusion frequency (CFF), with a maximum of 141 Hz and 128.1 ± 9.8 Hz (±SD) on average for the collared flycatchers and up to 146 Hz and 138.2 ± 6.5 Hz on average for the pied flycatchers, was attained in both species at 1500 cdm-2. https://doi.org/10.1371/journal.pone.0151099.g002

High CFF has been shown to correlate with high metabolic rate and small body size, predicting that vertebrates with the size and metabolic rate of small passerines should perceive visual flicker up to 100 Hz [2]. Our results however exceeded the CFFs that one would predict, given the sizes and metabolic rates of the species tested, by 30–50% (95–97 Hz) [2], implying an evolutionary history of strong selection for maximizing temporal acuity.

All three species are agile flyers, active during daylight and regularly navigate at high speed through dense forest. Blue tits are insectivorous during the breeding season and flycatchers throughout the year, regularly catching prey on the wing. High temporal resolution of the visual system is necessary for fast-flying and maneuvering organisms, which need to rapidly integrate information [4] to allow accurate pattern recognition [5], motion tracking [2] and depth perception, which in birds is maintained through optic flow [6]. Extremely high temporal acuity of vision has previously been demonstrated in some insects [7]. However, many birds should also be under selection for this trait, not least those catching fast-flying insects on the wing and therefore attempting to match the insects’ aerobatics, or having to avoid motion blur when navigating through dense vegetation or other complex environments. The daylight activity typical of most bird species is reflected by retinas rich in cones, which have more than four times faster post-stimulus recovery rates than rods [8]. Birds’ fast metabolism and small sizes both increase maneuverability, and their high metabolic rates also enable fast changes in the photoreceptor membrane [2].

Although the airborne and diurnal lifestyles of birds have long been suggested to favor high temporal acuity of vision [9–11], empirical evidence for generally higher CFFs than in other vertebrates has been lacking. Only Dodt’s and Wirth’s [12] electroretinograms (ERGs) reaching about 140 Hz in the pigeon, Columba livia, exceed the range of CFFs recorded in other vertebrates (see [2, 13]), but may not be directly comparable to behavioral results. In vertebrates, ERGs produce accurate estimates of retinal response but exclude temporal summation of signals from the retinal neurons leading to results significantly higher than those based on behavioral assays [14]. One reason for the lack of evidence of extreme temporal acuity in birds may be that few studies have reached CFF by using sufficiently high light intensities for temporal acuity to peak [15]. Another reason may be that behavioral studies have focused on species that forage on immobile or slowly moving food items or live in low-light conditions: (average highest frequency measured) budgerigar (69 Hz) [16], pigeon (75 Hz (from graph)) [17] and chicken (90 Hz [18] (from graph, white light) and 87 Hz [15]).

The behavioral requirements of birds in flight to accurately detect, identify and track objects whose image moves rapidly over the retina are likely to select for abilities to resolve visual detail in time rather than space. Visual performance is ultimately limited by the ambient light level. In addition energy constraints present a limiting factor (c.f. [19]), possibly exacerbated in birds by their large and avascular retinas. This should result in trade-offs between different aspects of vision that explain why birds in general, compared to raptors, have quite poor spatial resolution [20]. Eagles, which forage in open and brightly lit habitats, have developed the sharpest vision known [20, 21], allowing them to spot prey over long distances. However, tracking objects moving at high angular velocity should take priority when hawking for insects and while flying in complex environments, for instance when small passerines head for cover in dense vegetation. Motion tracking is improved by increasing visual refresh rates (Fig 3), but since this action decreases the visual integration time it becomes necessary to integrate over larger receptive fields to maintain the photon catch, leading to lower spatial acuity [22]. This is particularly true as light levels fall. We therefore expect fast-eyed species like tits and flycatchers to have compromised spatial acuity, the lower limit of which should be determined by the need to identify behaviorally important cues, such as prey or twigs and other obstacles in the flight path.

PPT PowerPoint slide

PowerPoint slide PNG larger image

larger image TIFF original image Download: Fig 3. The flight paths of two blue bottle flies (Calliphora vomitoria) sampled from high-speed video (S1 Movie): A) at the rate of the visual system of a human (40 frames/s) and B) at the rate of a pied flycatcher (120 frames/s) at a light intensity of approximately 500 cdm-2. The flycatcher refreshes visual input almost three times faster, resulting in a much more detailed view of the flight paths of the flies. https://doi.org/10.1371/journal.pone.0151099.g003

To the best of our knowledge, the temporal resolution data presented here are the first available for actively flying birds that feed on fast-moving prey. Our study is also the first to determine the CFF of the vision system of wild birds with predominantly diurnal habits. Thus, many other ecologically similar bird species may have been driven to such physiological extremes, either by flying in complex environments or due to an evolutionary arms race between predatory species and their prey. The fast vision of these small passerines may very well be a more typical avian trait than the sharp spatial vision found in birds of prey.