|Eklöf, J. Vision in echolocating bats - Doctoral thesis Zoology Department, Göteborg University 2003
Vision in Echolocating Bats
illustrations by Olof Helje
The use of ultrasonic echolocation (sonar) in air is seriously constrained by the attenuation of high frequency sounds and unwanted echoes from the background (called clutter). Therefore, in many situations, echolocating bats have to rely on other sensory cues. The aim of this thesis is to investigate the use of vision by echolocating bats.
One of the most fundamental roles of the eyes is to register the amount of ambient light, in order to establish photoperiodic cycles. Some tropical bats avoid too bright conditions, i.e. moonlit nights probably due to increased predation risk, a behaviour not found in high latitude species.
Although echolocation is the key innovation that have made it possible for bats to fly at night, vision is retained as an important complement; and indeed bats use an array of different sensory inputs to solve the different tasks of life.
VISION IN ECHOLOCATING BATS
The microchiropteran eye
The eyes of Microchiroptera1 rank among the smallest in mammals (Tab 1), although there are considerable differences in both eye size and morphology across species, reflecting a great ecological diversity (Chase 1972; Hope & Bhatnagar 1979a; b; Marks 1980; Suthers & Bradford 1980; Bell & Fenton 1986; Paper IV). In general, the eyes of frugivorous and nectarivorous Microchiroptera are larger than those of insectivorous species. Bats roosting in relatively exposed sites, and those that sometimes are active in dusk- and daylight conditions such as many members of the family Emballonuridae also have relatively large eyes. Hence eye size seems to reflect how much bats are exposed to light in their daily life.
Footnote 1. The Microchiroptera includes ca 800 species of echolocating bats but excludes the generally non-echolocating Megachiroptera or flying foxes, which are not considered in this thesis.
|The eye size and visual performance vary considerably between different species of Vespertilionidae. The northern bat Eptesicus nilssonii (left) has a visual acuity of ca 0.8° arc, the brown long eared-bat Plecotus auritus (middle), ca 0.5° arc, and Myotis spp. (right), 3 - 6° arc (Paper III, Paper IV).|
|The microchiropteran eyes are shaped for nocturnal conditions in that they have large corneal surfaces and lenses relative to the size of the eye. They also have relatively large receptor fields, which give them good light gathering power at the expense of acuity, i.e. the ability to resolve fine spatial details (Suthers 1970; Suthers & Wallis 1970). The bat retina, which is relatively thin (91-126 mm) compared to that of voles (178 mm) and rats (198 mm), for example, consists mainly of rods, which are arranged loosely in visual streaks (Chase 1972; Marks 1980; Pettigrew et al. 1998). However, cones or at least cone like structures (receptor cells with pedicles) are present at least in the fruit-eating bats Artibeus lituratus and Phyllostomus hastatus (Phyllostomidae) and the aerial hawking insectivorous Saccopteryx bilineata, Saccopteryx leptura and Rhynconycteris naso (Emballonuridae) (Suthers 1970; Chase 1972).
Suthers and Wallis (1970) studied the eyes of two species of Vespertilionidae (Myotis sodalis and Pipistrellus subflavus) and four species of Phyllostomidae (the vampire bat Desmodus rotundus, and the fruit-eating Carollia perspicillata, Anoura geoffroyi and Phyllostomus hastatus), and concluded that the visual capabilities of all the species tested would allow the bats to see well at ranges beyond that of echolocation. Due to the more or less spherical lenses (small species tend to have more asymmetric lenses; Chase 1972), it also follows that most Microchiroptera have a short focal distance and hence a great depth of focus (Suthers & Wallis 1970). In fact, microchiropteran bats seem to be farsighted, indicating that vision is used predominantly at long ranges, which is where echolocation does not work so well.
|The brain and the retinal pathways
The relative size of the internal brain structures of bats differs between insectivorous, sangivorous and carnivorous species on one hand and frugivorous and nectarivorous species on the other (Jolicoeur & Baron 1980; Barton et al. 1995; Barton & Harvey 2000). Whereas insect eating bats have enlarged echo-acoustic brain structures, fruit eating species have relatively large olfactory- and visual bulbs, clearly reflecting the different feeding strategies in the various species.
|Three examples of large-eyed bats: Species of the family Emballonuridae (left) have larger eyes than other insectivorous aerial-hawkers, probably reflecting an unusual visual capacity among bats. The large eyed Megaderma lyra (Megadermatidae) (middle) show a flexible hunting strategy and uses vision in combination with sonar and passive hearing. Macrotus californicus (Phyllostomidae) (right) is the only microchiropteran bat shown to be capable of catching insects using vision alone.|
|What bats can see
Brightness discrimination and light sensitivity
At the most basic level, vision is involved in the establishment of photoperiodic cycles, and serves to distinguish daylight from darkness. It was previously believed that this was the sole purpose of the microchiropteran eye (Eisentraut 1969 cited in Dietrich & Dodt 1970). The bat’s activity cycle is controlled by an endogenous circadian rhythm, which is synchronized with the daylight cycle by light sampling behaviour. This means that, before they emerge from the roost to feed, the bats move from the darker areas in their roosts to lighter areas near the entrance, in order to test the outdoor light level (Erkert 1982). Cloudiness and moonlight can thus affect the time of emergence. On moonlit nights, many tropical microchiropterans typically reduce their foraging activity, presumably due to increased predation risk (Morrison 1978; Usman et al. 1980; Fleming 1988) or perhaps lower availability of food (Lang et al. 2002). In contrast, bat activity at high latitudes is not influenced by moonlight to any high extent (Paper VI). On twelve nights in August-September 2000, the impact of moonlight on bat swarming activity (associated with mating season) was studied at an abandoned mine in southern Sweden. Bat activity at and near the mine entrance did not vary with moon phase, or cloud cover, suggesting that moonlight had no effect on the bats’ behaviour. It seems likely that insectivorous bats at high latitudes may not have been exposed to significant nocturnal predator pressure, leading to the evolution of lunar phobia, as many tropical bats. In contrast to high-latitude bats, the latter have to face specialized bat predators such as bat falcons (Falco rufigularis). Furthermore, high latitude bats are exposed to relatively bright light conditions throughout the summer. They do react to light, but not by decreasing their activity, instead, they fly closer to protective vegetation or sometimes high in the air (Rydell et al. 2002). This kind of behaviour is also seen in species that migrate during the day, such as the noctule, Nyctalus noctula (Ahlén 1997). Both types of behaviour may have the purpose of avoiding predatory birds (e.g. small hawks and falcons).
|Many tropical bats minimize their activity in moonlight, presumably due to predation risk. This behaviour is not found among high latitude bats (Paper VI)|
|As may be expected from a retina consisting predominantly of rods, the visual sensitivity generally declines as the ambient illumination increases towards daylight (Hope & Bhatnagar 1979b). This indicates that the bat eyes work better in dim light than in bright light. This has been verified behaviourally by Bradbury & Nottebohm (1969), who found that Myotis lucifugus avoids obstacles better under ambient illuminations resembling dusk, than they do in bright daylight. These findings may explain why early studies, which were made in room illumination, usually failed to prove any major visual capacity in microchiropteran bats (e.g. Eisentraut 1950; Curtis 1952).
Light tolerance has been estimated in three species of Vespertilionidae (Myotis myotis, Dietrich & Dodt 1970; Eptesicus serotinus, Bornschein 1961; and Eptesicus fuscus, Hope & Bhatnagar 1979b) and three species of Phyllostomidae (Desmodus rotundus, Carollia perspicillata, and Artibeus jamaicensis, Hope & Bhatnagar 1979b) by measuring the luminance of light stimuli required to provoke electroretinogram responses. Among the vespertilionids, Eptesicus fuscus showed the highest light tolerance, and among the phyllostomids, which generally responded to lower luminance levels than the vespertilionids, Artibeus jamaicensis showed the highest tolerance. This presumably reflects the relative importance of vision in the different species, but perhaps more importantly the time at which these species normally emerge in the evening, and to what extent they are exposed to bright light (Hope & Bhatnagar 1979a; b). The Emballonuridae Emballonura spp. and Saccopteryx spp., some of which roost at exposed sites and often fly in daylight (Lekagul & McNeely 1977; Bradbury & Vehrencamp 1976; Kalko 1995), would thus be expected to be more light tolerant than other bats. Although, light tolerance levels have not been measured in these bats directly, the small receptive fields and the low receptor-to-ganglion ratio (ca 1:10) in Saccopteryx spp., compared to that of other microchiropteran species (ca 1:100), indicate a high light tolerance and good resolving power as expected. In fact they resemble diurnal mammals in this respect (Chase 1972). Nevertheless, the eyes of Microchiroptera work well under low ambient illumination, although the sensitivity to different light levels and the ability of brightness discrimination vary considerably between the different families and species.
The eyes of microchiropterans are primarily adapted to function in low light levels. This carries the disadvantage of a relative poor ability to resolve fine spatial details (acuity). The ability of spatial resolution of the bat eye can be estimated either anatomically, by calculating the density of retinal ganglion cells (Marks 1980; Pettigrew et al. 1998; Heffner et al. 2001) or behaviourally, by presenting the bats with striped patterns of different fineness (Suthers 1966; Bell & Fenton 1986; Paper IV). When the visual acuity is measured with the latter method, it is often referred to as grating acuity and is expressed as degrees of arc or as cycles per degree, where one cycle is one pair of black and white stripes. The two methods give indications of the minimum separable angles, i.e. the minimum distance between two points that an animal needs in order to separate them.
|The device used for the optomotor response tests (Paper IV), in which a bat is presented with rotating, striped patterns of different fineness. The bat responds to the revolving patterns by moving its head in a stereotype manner. The thickness of the stripes corresponds to the bats visual resolving power (acuity), measured as degrees of arc.|
|Comparisons between the two methods should be treated carefully because the acuity values estimated by counting retinal ganglion cells tend to be higher than those estimated from behavioural studies. This suggests that the anatomical method gives a theoretical minimum, rather than an indication of what the bats actually respond to. Nevertheless, Table 2 should give an idea of the wide range of spatial resolution ability that has been documented in different species of microchiropteran bats, from the coarse vision of the small Myotis spp. (Vespertilionidae) (3-5º arc, Paper IV) to the relatively fine visual ability of Macrotus californicus (Phyllostomidae) (0.06° arc, Bell & Fenton 1986). Macrotus californicus has by far the best resolving power found in any microchiropteran bat studied so far, and is comparable to that of a dog in this respect (Heffner & Heffner 1992). It is also the only microchiropteran known to be capable of detecting insects, using vision alone (Bell 1985).
The visual resolving power is never a fixed value, but depends on the ambient light intensity. In the common vampire bat Desmodus rotundus, for example, the acuity drops from 0.8° arc at a light intensity of ca 310 lux to over 2º arc in ca 0.004 lux (Manske & Schmidt 1976). Other bats, such as Macrotus californicus (0.06° arc) and Antrozous pallidus (0.25° arc) retain their visual acuity down to light levels as low as ca 0.002 lux (Bell & Fenton 1986). In comparison, species of Megachiroptera, which do not echolocate, has been shown to respond to striped patterns of 0.8° in light levels of ca 0.0005 lux, whereas humans responds only to patterns of 1.3° arc under the same conditions (Neuweiler 1967). Hence, in very dim light, bats can see better than humans.
|Tab 2 - Visual acuity in Microchiroptera (expressed as degrees of arc).|
Bats can visually distinguish patterns and shapes of objects. The nectarivorous Anoura geoffroyi (Phyllostomidae) distinguishes rectangles from solid discs of the same surface area, when trained to seek food at the discs (Suthers & Chase 1966; Suthers et al. 1969). This species is also able to distinguish outlines of erected triangles from inverted ones, as long as the baselines of the triangles are intact. However, when the bats were presented with two sides of a triangle, i.e. an outline of a triangle without a base, the shape was no longer distinguished from other shapes. This indicates that Anoura geoffroyi does not possess a concept of form, but rather perceive the relative position of horizontal lines. Similar conclusions were drawn from studies of common vampire bats Desmodus rotundus (Phyllostomidae). This species is able to separate vertical stripes but not horizontal stripes from circles of the same area (Schmidt & Manske 1978; Manske & Schmidt 1979). In contrast, the insectivorous species Vespertilio superans (Vespertilionidae) cannot distinguish objects of different shapes but equal size, and responds only to the size of the surface areas (Chung et al. 1990). The only bat that has been shown unambiguously to respond to shapes alone is the frugivorous phyllostomid Carollia perspicillata. This species can discriminate squares from circles, even if the squares are rotated (Suthers et al. 1969).
Given that microchiropteran bats are all more or less nocturnal, true colour vision seems unlikely to occur in these animals, as it would probably be of minor importance. Nevertheless, cones occur in the retinas of some species, although most authors report only rods (reviewed by Suthers 1970; Chase 1972). Nevertheless, there is evidence that at least two different photo pigments occur in the eyes of Microchiroptera (Chase 1972; Hope & Bhatnagar 1979a). Electroretinogram response tests have shown sensitivity peaks around 500 nm and 570 nm in the vespertilionid species Myotis myotis (Dietrich & Dodt 1970) and Eptesicus fuscus (Hope & Bhatnagar 1979a) and the phyllostomid species Artibeus jamaicensis, Desmodus rotundus and Carollia perspicillata (Hope & Bhatnagar 1979a). There is also preliminary evidence that there is a spectral sensitivity peak in the near UV-range (around 390 nm) in the nectarivorous phyllostomid Glossophaga soricina (Lopez et al. 2001). It is thus possible that this species is able to perceive ultraviolet light reflected from fruits and plants.
Long distance navigation
The fact that the eyes of most bats function better beyond than within the range of echolocation (Suthers & Wallis 1970) suggests that visual cues may preferably be used in preference to echolocation for navigation and orientation over longer distances.
|Balantiopteryx plicata (Emballonuridae) relies on visual cues when presented with conflicting information from vision and sonar, for example in front of a window (Paper V).|
|The frequent observation that bats have a tendency to crash into windows of buildings when released indoors (Fenton 1975), during migration (Timm 1988), or commuting (Test 1967), suggests that they predominantly rely on vision rather than on echolocation in situations when both acoustic and visual cues are available. The performance is greatly improved, i.e. there are fewer collisions, when the bats are blinded (Davis & Barbour 1965) or when they are flown under dark conditions, and hence are “forced” to rely on echolocation alone. The insectivorous Balantiopteryx plicata (Emballonuridae) was studied at different times of the day in an empty mesh greenhouse (Paper V). At night they flew smoothly and could easily avoid the ceiling and the walls of the greenhouse, but during the day and at dusk and dawn they often tried to fly through the mesh and thereby crashed into it. The bats used echolocation consistently and without any dramatic change in echolocation call structure that could be related to the prevailing light conditions. The study indicates that emballonurid bats trust their eyes over their ears when exposed to contradictory auditory and visual cues.
When moving towards resting places and specific sites within roosts, bats sometimes face extremely unfavourable conditions for orientation, such as darkness, acoustic clutter from the walls of the roost, and simultaneous echolocation calls from many individuals. It is therefore likely that arrays of different sensory cues are used in such situations, and also that a good spatial memory is of great importance (Höller & Schmidt 1996). When introduced in a dark flight cage, Nyctophilus spp. (Vespertilionidae) ceased to echolocate after 6-8 hours of flight (Grant 1991), suggesting that they can learn to orient inside the cage, using spatial memory alone. In the same way, Megaderma lyra (Megadermatidae) remembers the positions of narrow openings with an accuracy of 2 cm, and if an obstacle is removed from the flight path, the bats may continue to avoid that position for days (Neuweiler & Möhres 1966). However, bats do not trust their spatial memory exclusively, but can compare stored data with new echo-acoustical and visual information (Joermann et al. 1988; Schmidt et al. 1988; Höller 1995). When flying in a room of subdued daylight, the two frugivores Carollia perspicillata and Phyllostomus hastatus (Phyllostomidae) are able to see and avoid obstacles consisting of 30 cm wide strips of cloth in their flight path (Chase & Suthers 1969). Those that were deafened with earplugs avoided the obstacles significantly better than those that were both deafened and blindfolded, showing that they could obtain visual information of features in the environment during flight. These results are consistent with those of Bradbury and Nottebohm (1969), who found that Myotis lucifugus (Vespertilionidae) avoided collisions in a string maze better in dim light than in total darkness. Rother and Schmidt (1982) noted that Phyllostomus discolor (Phyllostomidae) uses fewer sonar pulses in adequate illumination than in darkness. When flying the bats in a string maze, the same authors also showed that fewer pulses were used if the obstacles exceeded 0.25 mm in width. The results suggest that vision can shorten the bats’ reaction time for avoiding obstacles in a flight path, as long as there is enough ambient light and the obstacles are of sufficient size (given by the visual acuity threshold and the range).
Vision in foraging and prey detection
At close range, echolocation usually gives more detailed information about the prey than vision (Suthers & Wallis 1970; Pettigrew 1980). However, in some situations, it may be favourable to change the modality with which to search for prey, and indeed, many bats use a variety of sensory cues, including smell (Hessel & Schmidt 1994; Kalko et al. 1996; Helversen et al. 2000), passive listening for prey generated sounds (Fiedler 1979; Ryan & Tuttle 1987; Arlettaz et al. 2001), tactile information (Baron et al. 1996c), visual cues (Bell 1985), and vampire bats possess the ability of thermo-perception (Kürten & Schmidt 1982).
For bats that search for insects within or near vegetation, separation of prey echoes from the background clutter is usually a severe problem when using sonar alone (Jensen et al. 2001). In such situations bats have to rely on additional sensory cues to locate the prey. Nevertheless, few studies have addressed the obvious possibility that visual cues may be used for detection of prey in acoustically complex environments. However, when northern bats (Eptesicus nilssonii) search for stationary targets among high grass (clutter), this seems indeed to be the case (Paper II, Paper III). During early summer in Sweden, ghost swift moths Hepialus humuli (Lepidoptera: Hepialidae) swarm in stationary display flight over and among grass at dusk. These moths are large (ca 6 cm wingspan) and conspicuously silvery white (Andersson et al. 1998), and in contrast to most other moths, they lack ultrasonic hearing (Rydell 1998), and are intensively exploited by northern bats patrolling in the air over the field (Andersson et al. 1998; Rydell 1998; Jensen et al. 2001). In an experimental set-up, making use of this natural foraging situation, Hepialus humuli were presented to the bats, either with their white dorsal side up or with their dark ventral side up. It was found that the white moths were attacked more frequently than the dark ones, indicating that the bats were guided by visual cues (Paper II).
|The aerial hawking northern bat, Eptesicus nilssonii (Vespertilionidae), uses visual cues as a complement to echolocation when searching for moths in acoustically complex environments (Paper II, III).|
|The brown long-eared bat Plecotus auritus (Vespertilionidae) is a gleaning insectivore, which usually uses its large and sensitive ears to passively locate its prey by the noise they make (Anderson & Racey 1991). However Plecotus auritus also has relatively big eyes (Cranbrook 1963, Tab 1), suggesting that they have relatively good vision. We investigated if brown long-eared bats exploit visual cues when searching for prey (Paper I). By using petri dishes, containing mealworms that either were available to the bats or presented under glass, and presenting these in different levels of illumination, we provided the bats with visual cues, sonar cues or both. The bats did best in situations where both sonar cues and visual cues were available, but the visual information seemed to be more important than sonar.|
|Gleaning brown long-eared bats, Plecotus auritus (Vespertilionidae), feeding from bowls presenting different sensory cues, seem to prefer visual information to sonar cues. (Paper I).|
|The California leaf-nosed bat Macrotus californicus (Phyllostomidae), a gleaner that normally searches for prey on the ground, has been shown to locate prey by using auditory- and visual cues as well as by sonar. Indeed this bat shows a particularly flexible hunting behaviour. In moonlight Macrotus californicus can see well enough to hunt using vision alone (Bell 1985). This allows the bat to hunt without alerting the prey with ultrasound (Fullard 1987; Rydell 1992a), and also to detect stationary targets, which otherwise would be hard to detect (Arlettaz et al. 2001; Jensen et al. 2001; Paper II). In visual acuity tests Macrotus californicus responded to stripes subtending 0.06° arc, (Tab 2), which is the best visual acuity found in any microchiropteran bat (Bell & Fenton 1986). Moreover, the eyes of Macrotus californicus are relatively large and have a much higher degree of binocular overlap (50°) than in other bats (for example Antrozous pallidus 25° and Eptesicus fuscus 19°, Bell & Fenton 1986). This suggests that Macrotus californicus has good stereoscopic vision and that the near field distance perception is of great importance (McIlwain 1996), as would be expected in a species that forage visually. Macrotus californicus exploits diurnal prey, that are stationary at night and therefore unavailable to other bats (e.g. Howell 1920 cited in Bell & Fenton 1986).
The African yellow-winged bat Lavia frons (Megadermatidae) employs feeding tactics that involve both gleaning and aerial hawking. This species is a sit-and-wait predator, which scans the vicinity while hanging from a branch, waiting for insects to pass by. Lavia frons is active in relative bright ambient illumination, at dusk as well as late mornings, and is often seen catching prey against the sky. It has large eyes and may be able to see insects against the bright sky (Vaughan & Vaughan 1986). Nyctophilus gouldi and Nyctophilus geoffroyi (Vespertilionidae), also combine aerial hawking with gleaning, and have been shown to use different sensory cues according to circumstances. As in Lavia frons, visual cues are preferentially used to detect prey in the air, whereas auditory cues are used to detect prey on the ground (Grant 1991). The visual acuity of Nyctophilus gouldi is nowhere near that of Macrotus californicus and Antrozous pallidus, but rather similar to that of other aerial hawking Vespertilionidae (Tab 2), which explains why they cannot find prey on the ground visually.
Eklöf & Anderson (unpublished) observed northern bats (Eptesicus nilssonii, Vespertilionidae) feeding under midnight sun conditions in northern Norway. The bats caught prey against the bright sky and sometimes without detectable sonar signals. However, based on the performance of Eptesicus fuscus (Tab 2) it seems unlikely that Eptesicus nilssonii has sufficient resolving power to detect small airborne prey visually. A 2 cm insect is first detected at a distance of ca 1 m using vision (considering a visual acuity of 0.7° -1° arc, Tab 2), but the same object is first detected at ca 5 m using echolocation (Kick 1982), which thus suggests that echolocation would be the preferred sense. On the other hand, when northern bats search for ghost swift moths (described above), vision increases the chance of detection of the prey, only because they exceed 5 cm in wingspan and are detected at rather close range (3.5 m) (Paper III). Smaller targets are detected using echolocation alone.
Little brown bats (Myotis lucifugus) have been observed to catch prey apparently without using echolocation (D. R. Griffin personal comm.) This species’ visual resolving power is even poorer than that of the northern bat, and in addition, its prey items are even smaller, so it is thus highly unlikely that vision is involved in prey catching. In this species the apparent absence of echolocation calls must have another explanation. In fact, earlier observations of northern bats (Rydell 1992b) and little brown bats (Rydell et al. 2002) have suggested that attempted insect captures are always associated with echolocation calls, even in bright light conditions at high latitudes.
Under conditions that appear to us to be completely dark (0 lux), bats may still be able to see conspicuous insects. For example, it has been reported that bat activity is high where fireflies occur (Lloyd 1989), and it has been shown that some fireflies stop flashing when approached by bats (Farnworth 1973). This suggests that the light emitted by fireflies may guide the bats or at least evoke their curiosity. More interestingly, fireflies are not eaten by bats and were rejected by Eptesicus fuscus in feeding experiments (Vernon 1981). In the same study, the bats were presented with flashing fireflies as well as with artificial flashes. The bats responded to the flashes, although it was not clear if they associated the flashes with food or with unpalatability. It seems possible that firefly flashes may function as a visual aposematic signal to bats.
In general, fruit- and nectar feeding bats have larger eyes (Tab 1), better visual resolving power (Tab 2) and enlarged visual and olfactory bulbs, compared to insectivorous species (Jolicoeur & Baron 1980; Barton et al. 1995; Barton & Harvey 2000). They also perceive and respond to different patterns more readily than insectivorous species (Suthers & Chase 1966; Suthers et al. 1969), suggesting that vision may perhaps play a more important role in these bats than in most insectivores.
As discussed earlier, vision seems to be important in escape behaviour (Chase 1981; Chase 1983; Mistry 1990). Presumably it is also important in detection of predators; it is much easier to approach a blindfolded bat than a non-blindfolded individual (Chase 1972). Species of the family Emballonuridae often fly earlier in the evening than most other bats, and sometimes even in the afternoon and they often roost on exposed and well lit sites such as tree trunks (e.g. Bradbury & Vehrencamp 1976). A Saccopteryx sp. will quite easily detect an approaching person, and take flight without emitting any echolocation calls (Suthers 1970), and Rhynconycteris naso seems to be disturbed more easily by seeing an approaching figure at a distance, than by sudden sounds or vibrations at close range (Dalquest 1957). Vaughan and Vaughan (1986) noted that Lavia frons (Megadermatidae), which also roosts exposed, seems to be constantly alert during the day, scanning its surroundings for predators. In fact, the authors almost never saw a bat with its eyes closed, and were never able to approach one undetected.
The echolocation detection range of a 19 mm insect is around 5 m for Eptesicus fuscus (Kick 1982), and the visual acuity of this species is 0.7°-1° arc, Tab 2). This allows visual detection of the 19 mm object only when it is closer than ca 1 m. This simple calculation strongly suggests that echolocation is the more accurate sense at close range and for small objects. However, larger objects can be detected visually at distances of hundreds of meters, far beyond the range of echolocation. For example, an object of 5 m diameter can potentially be detected visually by Eptesicus fuscus at a distance of ca 300 m. Using echolocation; the same object is detected at a distance of only 25-30 m at most (depending on call strength, attenuation etc., Lawrence and Simmons 1982; M. B. Fenton personal comm.). This supports the general view that vision is used primarily for detection of large objects and landmarks and for navigating over longer distances (Davis 1966; Layne 1967; Griffin 1970; Höller and Schmidt 1996). Nevertheless, for bats with better visual resolving power, vision can be used and even replace echolocation, at short distances. The California leaf nosed bat Macrotus californicus, referred to above, can visually detect a 19 mm insect at a distance of ca 18 m. This presumably gives this bat a longer range of operation if they use vision instead of echolocation, at least under conditions of moonlight or bright starlight (Bell & Fenton 1986). Other bats, such as some Emballonuridae, which have visual acuities below 0.4° arc (Tab 2), can visually detect insect sized objects (1 cm) at distances less than 1 m, suggesting a range of operation roughly similar for vision as for sonar. One could therefore assume that emballonurid bats could use either vision or echolocation to detect prey, as suggested by Pettigrew (1980). He observed one species of Emballonuridae (Craseonycteris thonglongyai) catching prey against a bright sky apparently without using echolocation and suggested that the bats could see the insects as silhouettes against the sky.
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Papers included in the thesis
PAPER I. Eklöf, J. & Jones, G. 2003. Use of vision in prey detection by brown long-eared bats Plecotus auritus. - Animal
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