Most species of birds rely on vision for many important behaviors, and it is no surprise that some species have evolved vision of extremely high acuity. Birds have excellent color vision abilities (e.g., Martin and Osorio 2008; Olsson et al. 2015), some species of acciptriform raptors have the highest spatial acuities known in any animal (Fischer 1969; Reymond 1985), and pigeons (Dodt and Wirth 1953) as well as blue tits and Old World flycatchers (Boström et al. 2016) see the world with a temporal resolution unsurpassed by any other vertebrate. The evolutionary benefit from maximizing spectral, spatial or temporal acuity may be found in the ecology of birds.
While a lot of efforts has been devoted to studies on color vision (for references see Martin and Osorio 2008; Hart and Hunt 2007; Olsson et al. 2015) and spatial resolution (e.g., Ghim and Hodos 2006; Harmening et al. 2009; Lind and Kelber 2011; Lind et al. 2012 and references therein) of birds, our knowledge about avian temporal visual acuity is still quite limited (cf. Dodt and Wirth 1953; Greenwood et al. 2004; Boström et al. 2016), and there are very few clues in the literature as to how widespread ultra-rapid vision is among birds.
As the highest temporal resolution has been found in three small species of insectivorous passerines (Boström et al. 2016), we suggest four possible hypotheses that can be tested: (a) Very high temporal resolution may be a synapomorphy of Passeriformes. (b) It may be a common feature for small fast moving birds with high metabolic rates. Animals that fly fast and control flight by visual cues require high temporal resolution. This has been demonstrated in insect species such as flies and dragonflies (Vogel 1957; Ruck 1958, 1961). Moreover, it has recently been hypothesized that vertebrates with small body size and high metabolic rates should have high temporal acuity (Healy et al. 2013). (c) High temporal acuity could also be closely related to a diurnal activity cycle and a life in very bright habitats. This is suggested by the fact that temporal resolution generally is higher in brighter light levels, and for cone-based as compared to rod-based vision (e.g., Lisney et al. 2011). Finally (d), lifestyles that require accurate tracking of rapid motion may select for high temporal resolution. If so, then raptors and insectivorous birds catching fast flying prey in flight and forest birds speeding through canopies should have the highest resolution.
Similar hypotheses have been formulated for insects already more than 50 years ago. Autrum (1949), and Autrum and Stoecker (1950) studied fly and bee vision and, comparing their results with those obtained in slower moving insects concluded that only fast flying insects have high temporal resolution. Their behavioral results were confirmed by their own and later (e.g. Laughlin and Weckström 1993) electrophysiological results showing that diurnal, fast flying species have faster phototransduction and potassium channels in the photoreceptors than slowly flying and nocturnal species.
Temporal resolution is commonly assessed by measuring flicker fusion frequencies (FFFs), the frequencies at which temporally alternating light–dark stimuli cease to appear as flickering and are perceived as continuous by the observer. FFF increases logarithmically with the luminance of the flickering light, according to the Ferry-Porter Law (Brown 1965), up to a peak value. It is, therefore, common to determine this critical flicker fusion frequency (CFF), the maximal FFF at any luminance, which is the most coherent value for the comparison between species (e.g., Ordy and Samorajski 1968; Jenssen and Swenson 1974; Healy et al. 2013).
Flicker fusion frequency can be estimated both electrophysiologically by electroretinography (ERG), and behaviorally. ERGs are likely to estimate higher FFFs since they measure neuronal transmission at an early processing stage in the retina, and do not take temporal summation, that may occur at later stages into account (D’Eath 1998; Lisney et al. 2012).
Behavioral studies take into account the complete visual pathway of the tested individual and provide an estimate of what the animal perceives. Early studies on birds and insects used an optomotor response to moving gratings to behaviorally determine CFF, however, it is not fully clear that their results are not limited by spatial resolution (Crozier and Wolf 1941, 1944; Autrum and Stoecker 1950). Newer studies use operant conditioning with stationary stimuli (e.g. Ginsburg and Nilsson 1971; Lisney et al. 2011). For those few species of mammals and birds, in which both ERGs and behavioral tests have been performed, higher flicker fusion frequencies have been documented with ERG (Lisney et al. 2012 and references therein).
Behavioral studies have documented the highest CFF among vertebrates in birds. Three species of small, insectivorous passerines—blue tit (Cyanistes caeruleus), collared flycatcher (Ficedula albicollis) and pied flycatcher (F. hypoleuca)—were discriminated light flickering with up to 130–145 Hz from a continuous light, at a luminance of 1500 cd/m2 (Boström et al. 2016). For comparison, humans can only detect flicker at much lower frequencies, around 50-60 Hz (Brundett 1974), as can most other non-avian vertebrates, although rhesus monkeys can reach at least 95 Hz (Schumake et al. 1968). Comparable behavioral studies with stationary flickering stimuli are rare in birds. Several studies have determined FFFs in chickens, with slightly variable results (71.5 Hz at 100 cd/m2, Jarvis et al. 2002; 74 Hz at 800 cd/m2, Rubene et al. 2010) but only one individual reached the CFF (100 Hz in one bird, and 87 Hz on average for 15 birds, at 1375 cd/m2, Lisney et al. 2011). An older study on budgerigars used a similar technique but very low light intensities (Ginsburg and Nilsson 1971) and found the highest FFF of 74.4 Hz in one of two tested birds at 17 cd/m2, a light level comparable to sunrise or sunset (Lind and Kelber 2009).
ERG studies have rarely used very bright light stimuli, and only in three species of birds reached a point close to CFF: between 45 and 70 Hz in owls (Asio flammeus, Bornschein and Tansley 1961; Athene noctula, Porciatti et al. 1989), up to 119 Hz in domesticated hens (Gallus gallus domesticus, Lisney et al. 2011, 2012) and 143 Hz in pigeons (Columba livia, Dodt and Wirth 1953). Although CFF of pigeons is en par with the passerines, and the hen CFF is not far below, these CFFs that were determined with ERG recordings are not directly comparable to the behaviorally determined results.
With this lack of data, it is impossible to decide which of our four hypotheses may account for the extremely high temporal resolution found in the passerines. In this study, we have behaviorally tested FFF as a measure of temporal resolution in the budgerigar (Melopsittacus undulatus) with the aim to shed new light on the four different hypotheses presented above.
Budgerigars are suited to assess whether very high CFF is common and limited to passerines (a), since they belong to Psittaciformes, a phylogenetic sister group to Passeriformes (Hackett et al. 2008; Jarvis et al. 2014). Budgerigars are small, actively flying, exclusively diurnal birds with relatively high metabolic rates (Weathers and Schoenbaechler 1976) but unlike blue tits and Old World flycatchers they are granivores and do not live in woods but in open landscapes, allowing us to disentangle hypotheses (b: high metabolic rates—high CFF), (c: diurnal lifestyle—high CFF) and (d: insectivory and/or forest life—high CFF).
We also wanted to estimate temporal acuity in budgerigars because they are the third most common pet bird worldwide (Perrins 2003). Pet birds are generally kept indoors, mainly in artificial light. Incandescent light bulbs, which have been very common and suitable for avian husbandry, are being phased out worldwide due to their poor energy efficiency (US Congress and Natural Resources 2005; European Commission 2009) and replaced by various types of fluorescent or light-emitting diod (LED) lamps. In areas where alternating current (AC) power supply has a 50 Hz frequency, many of these lamps flicker at 100 Hz (accordingly, in a number of American countries, 120 Hz). Although this flicker frequency is too high to be perceived by humans, it may induce general stress and impaired welfare in birds with higher FFFs (e.g., Nuboer et al. 1992; Prescott et al. 2003), as has been shown in several studies on starlings (Sturnus vulgaris) (Maddocks et al. 2001; Greenwood et al. 2004; Smith et al. 2005; Evans et al. 2006, 2012). If flicker fusion frequencies in budgerigars supersede those of fluorescent and LED lamps, it may spell welfare problems for many pet birds.