Eklöf, J. Vision in echolocating bats - Doctoral thesis Zoology Department, Göteborg University 2003

Vision in Echolocating Bats

Johan Eklöf

illustrations by Olof Helje

svensk sammanfattning

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ABSTRACT

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.

Bat eyes are generally small, especially among aerial hawking insectivores, with the exception of members of the family Emballonuridae. In gleaning, and in frugivorous species, however, the eyes tend to be larger and more prominent. The eyes of all bats are well adapted to low illumination, having mainly rod-based retinas, large corneal surfaces and lenses, and generally large receptor fields. Bats can easily detect small differences in brightness on clear nights, and the visual acuity remains relatively good in dim illuminations. The visual resolving power (as obtained from counts of retinal ganglion cells or by optomotor response tests) varies considerably among the different species of bats, from less than 0.06° of arc in Macrotus californicus (Phyllostomidae) to almost 5° in aerial hawking Myotis species (Vespertilionidae). Generally, the visual acuity is similar to that of rats and mice, suggesting that cm-sized object can be discriminated at ranges less than a few metres. Studies on pattern discrimination have yielded highly variable results. Fruit and nectar eating species respond to patterns to a larger extent than aerial insectivores.

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.
As sonar only works well at short ranges, vision is primarily used for detection of landmarks and to avoid objects when moving over long distances, for example during seasonal migration and when commuting between feeding sites. In these situations, there seems to be precedence of vision over sonar. At short range, within that of echolocation, bats may defer to visual cues in addition to sonar and spatial memory to solve different tasks of orientation, especially when there is conflicting information. Light conditions and time of the day may determine the behaviour of the bats and thus which sensory cues will be used.
There is an increasing amount of data suggesting that vision might be of importance in some situations and some aspects of foraging, especially for frugivorous and nectarivorous bats, which can make use of differences in brightness and spectral composition, to find different food items. But even in species traditionally considered to rely heavily on echolocation, such as most insectivorous bats, vision seems to play a more important role than has been recognised previously. The gleaning brown long-eared bat (Plecotus auritus, Vespertilionidae), known to forage mostly by using passive listening, detects prey more readily by using vision than by using sonar, and the aerial hawking northern bat (Eptesicus nilssonii, Vespertilionidae), use visual information in addition to sonar to find large stationary prey in clutter.

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.

Tab 1 - Eye size in Microchiroptera in relation to taxonomic affinity and general
feeding behaviour


 
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.
The size and lamination of the main targets of retinal projections in the brain: the superior colliculus (which transmits visual information and controls head- and eye movements) and the lateral geniculate body (a processing station on the way from the retina to the visual centre, which e.g. serves to enhance contrasts) have been studied in Artibeus, Eptesicus (Cotter 1985), Myotis (Cotter & Pentney 1979; Crowle 1980) and Pteronotus (Covey et al. 1987). Megadermatids and fruit eating phyllostomids show the thickest and most developed layers in the superior colliculus, at least in the superficial ones, which receive exclusively visual input. Also gleaning species tend to have relatively large superior colliculi. Open-air insectivorous species on the other hand, seem to have superior colliculi consisting almost entirely of the deeper layers, which receive a variety of different sensory inputs (including visual stimuli). However, some insectivorous bats, like the Emballonuridae (especially Saccopteryx and Cyttarops) have relatively large superior colliculi and resemble frugivores in this respect, although their total brain volume is smaller than in most other microchiropteran families (Baron et al. 1996b). This may perhaps reflect the fact that most emballonurid species roost in exposed sites and therefore live in bright light conditions. However, considering that the Emballonuridae form a basal clade in the phylogenetic tree, it may just as well suggest that bat ancestors had a well-developed visual system. (Simmons & Geisler 1998). The projections to the superior colliculus are similar to those of most mammals, in that they have no binocular overlap, and thus the left superior colliculus receives input only from the right eye and vice versa (Pettigrew 1986; Neuweiler 2000). In Megachiroptera and in primates, both superior colliculi receive input from both eyes, and hence these animals have better stereoscopic vision than Microchiroptera. (Interestingly the microchiropteran family Rhinolophidae, which contain highly specialized echolocators, show similarities to Megachiroptera in this respect (Reimer 1989). This may reflect phylogenetic relationship rather than visual adaptation, however (e.g. Springer et al. 2001)).
The lateral geniculate body consists of two parts, the ventral lateral geniculate, which has connections with several other brain structures, and the dorsal lateral geniculate, which connects to the visual cortex. In most Microchiroptera, a larger proportion of the nerves are projected to the ventral side of the lateral geniculate body, suggesting that vision is important for orientation rather than for cognitive tasks (Neuweiler 2000). However, the sizes of the retinal pathways vary between genera. The nerves are generally larger in frugivores (Phyllostomus hastatus, Anoura geoffroyi, Suthers & Bradford 1980; and Artibeus jamaicensis, Cotter 1985) than in insectivores (Eptesicus fuscus, Cotter 1985; and Pteronotus parnellii, Covey et al. 1987), although, again, insectivorous Emballonuridae and Megadermatidae are exceptions. Both have relatively large visual pathways projecting through the dorsal lateral geniculate to the visual cortex. This suggests that vision is more important in these species, and they show similarities to the visually oriented Megachiroptera in this respect (Neuweiler 2000), and may reflect phylogenetic relationship (Springer et al. 2001). For a comparison of different brain structures between all groups of Microchiroptera, see Baron et al. (1996a; b; c).

 

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).
The ability of bats to detect small differences in brightness, i.e. brightness discrimination, was first studied by Eisentraut (1950), who found that Plecotus auritus and Eptesicus serotinus (Vespertilionidae) could easily distinguish black cards from white. Curtis (1952) trained the vespertilionids Eptesicus fuscus and Myotis lucifugus to search for food at the illuminated end of a box, and found that the bats’ ability of brightness discrimination is similar to that of rats and mice. Brightness discrimination performance in Eptesicus fuscus peaks around 10 lux, which is equivalent to the light level prevailing at dusk and dawn, but remains good in illuminations as low as 0.001 lux, conditions which resembles darkness to a human eye adapted to low light intensity. As a comparison, a light level of 0.1 lux is equivalent to light levels at full moon, and on overcast nights the amount of light drops to 0.0001 lux (Ryer 1997). Based on focal distance and diameter of the dilated pupil, Dietrich and Dodt (1970) calculated that the light gathering power of Myotis myotis is 4-5 times that of man. This suggests that bats can readily use visual cues at dusk, when they normally emerge from their roosts, and probably also under nocturnal conditions (Ellins & Masterson 1974).

 

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.

Spatial resolution

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).  

Pattern discrimination

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).
In conclusion, studies on pattern discrimination have yielded highly variable results, but in general it seems as if fruit- and nectar-eating microchiropterans respond to patterns and shapes more readily than insectivorous species. This may perhaps reflect that plants are more easily detected by vision, and less detectable by sonar than insects, and that frugivores therefore may use a different search image when foraging.


Perception of colour

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.


Vision in orientation and navigation

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.
Several species of Microchiroptera make long distance movements and some even perform seasonal migration (Griffin 1970). It seems unlikely that ultrasonic echolocation plays any major role in orientation over long distances, as it works only at short range. For example, insect sized targets can be detected a few metres away at best (Kick 1982), although trees, hillsides or the ground obviously may be detected much further away. However, even during the most favourable conditions, bats do not pay attention to echoes returning from more than 100 m or so away (Altringham 1996) and therefore, migration over long distances is almost certainly guided by other senses, including vision (Griffin 1970). Bats can use distant low frequency sounds for orientation over moderate distances, indicating that passive hearing may also be involved in navigation over longer distances (Griffin 1970; Buchler & Childs 1981). There is also some evidence that bats possess magnetic material (Buchler & Wasilewski 1985), but if they possess a magnetic sense like birds (Wiltschko & Wiltschko 1995) or not, is still unknown.
When migrating at night, it is possible that stars can serve as navigational cues for some species of bats. For example, Eptesicus fuscus can see point light sources, which simulate bright white and blue stars against the night sky, if these are located at > 6o angle (Childs & Buchler 1981). This species is also able to orient and navigate in relation to the post-sunset glow in the west (Buchler & Childs 1982).
In homing experiments with bats released within 10 km from their roost, the bats have been demonstrated to do well, using echolocation alone. This suggests that they are acoustically familiar with a relatively large home territory (Williams et al. 1966; Williams & Williams 1967; Davis & Barbour 1970). Nevertheless, blinded bats tend to fly slower and closer to the ground than non-treated bats (Mueller 1968), indicating that they change their orientation behaviour when they no longer are able to see. Bats also seem to rely heavily on their spatial memory, as they often follow the same paths night after night (Höller 1995).
When commuting between roost- and feeding sites during dusk and dawn periods, bats often follow outlines in the landscape, such as river banks, forest edges, hedgerows and hillsides (Racey & Swift 1985; Limpens & Kapteyn 1991; Verboom & Huitema 1997). The reason may be to minimise predation risk (Swift 1998), or to use outlines as acoustic landmarks, which perhaps facilitate navigation by sonar (Verboom et al. 1999). More likely, however, landscape outlines and silhouettes provide the bats with visual cues, contrasting against the twilight sky, and such cues are probably essential for orientation and navigation along travelling routes (Davis 1966; Layne 1967; Griffin 1970; Manske & Schmidt 1979; Höller and Schmidt 1996).

 

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.


Close range orientation and navigation

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).
Joermann et al. (1988) studied landing performance in two captive species of Phyllostomidae (Desmodus rotundus and Phyllostomus discolor). The bats were presented with visual illusions of landing grids, which thus gave them conflicting acoustic and visual information. Although the grids were not detectable by echolocation, the bats seemed to aim for them, and only ca 30 cm in front of the illusions the bats interrupted the approach and turned away. The authors concluded that bats rely mainly on echo-acoustical cues at close range, but in some situations they defer to visual cues in an early phase of detection, even within the range of echolocation.
To investigate what sense the Anoura geoffroyi (Phyllostomidae) (Chase 1981; 1983) and the Tadarida brasiliensis (Molossidae) (Mistry 1990) would defer to when escaping from a roost, the bats were flown in a Y-maze, in which one exit was blocked with Plexiglas and illuminated with a light source. The other exit was open but dark. When tested in daytime, nearly all bats chose the illuminated “exit”, thus indicating that they believed the light was an opening. However, when releasing bats at night, the escape behaviour was the opposite, the bats choosing the dark exit. It was suggested that the synchrony of light schedules to the bats’ circadian rhythm might determine the use of the appropriate sense (Mistry 1990).

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).


Insectivores and carnivores

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.


Frugivores and nectarivores

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.
Hessel and Schmidt (1994) investigated which sensory cues Carollia perspicillata (Phyllostomidae) uses when orienting toward a food source. The bats were presented with a triple choice of passive acoustic-, olfactory-, and visual cues. At least initially, the visual cue was the most frequently preferred stimulus. But after training the bats changed their behaviour and responded more to the olfactory stimulus. The experiment suggests that Carollia perspicillata can detect new sources of food using visual cues, and that they subsequently rely more on olfaction as the food source becomes known. Indeed these bats seem to possess a remarkable sense of olfaction (Fleming 1988; Laska 1990).
Kalko et al. (1996) showed that fig eating Microchiroptera do not use vision when foraging, presumably because figs eaten by these bats are visually inconspicuous. Instead, they rely mainly on olfactory cues, combined with broadband echolocation. In fact, most bat-pollinated plants are greenish, pink and white, which presumably reflect the fact that bats are most likely colour-blind (Suthers 1970; Faegri & van der Pijl 1979). On the contrary, many species of bat pollinated Parkia (Leguminosae: Mimosoideae) have bright red and yellow colours (Hopkins 1984). It is also suggested that dark flowers can be seen as silhouettes, against the sky and that pale flowers appear conspicuous against dark foliage (Start 1974, cited in Hopkins 1984). If the bats make use of such differences in contrast, one would expect to find that the position of differently coloured flowers vary accordingly in relation to the foliage, i.e., red flowers far from foliage and yellow flowers closer, which in fact, seems to be the case.
The capitula of Parkia are also highly reflective under moonlight and starlight conditions, and are therefore presumably visible to pollinating bats (Hopkins 1984). Many pollinators make use of a broad spectrum reflected from flowers, fruits or seeds, including ultraviolet (UV) light (for example insects, Kevan et al. 2001; and birds, Church et al. 2001). Ultraviolet vision seems, however, to be absent in most mammals, although some rodents have been shown to have UV sensitive retinas (Jacobs et al. 1991). Recently, it was suggested that bats might perceive UV-light, as there is evidence for a spectral sensitivity peak around 390 nm (i.e. in the near UV-range) in the nectarivorous Glossophaga soricina (Lopez et al. 2001). However, if the bats actually use UV reflecting surfaces as orienting cues is still uncertain, although Willson and Whelan (1989) have shown that UV-reflectance is indeed relatively common throughout the plant kingdom. The Passiflora species, Passiflora galbana and Passiflora mucronata, two plants which flowers are exploited by the nectarivorous glossophaginae bats, reflect light down to ca 400 nm and 370 nm (upper UV range), respectively. This should be compared to the hummingbird pollinated Passiflora speciosa, which has its main reflection above 570 nm (Varassin et al. 2001), perhaps reflecting the spectral sensitivity of the pollinators. Furthermore, 80% of nocturnal Lepidoptera have wing patterns that reflect UV, compared to ca 30% in diurnal species (Lyytinen 2001 cited in Honkavaara et al. 2002). On the other hand, this may imply that bats cannot make use of the ultraviolet light, in contrast to birds, which usually forage in daylight.


Predator surveillance and social behaviour

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 evidence for the use of vision in social behaviour is mainly anecdotal. Social grooming occurs in the vampire Desmodus rotundus (Phyllostomidae) and may serve to identify individuals (Wilkinson 1986), although it is generally rare (Fleming 1988). Goodwin and Greenhall (1961) noted that avian vampire bats (Diaemus youngi) show grooming behaviour when seeing a mirror reflection, indicating that vision might be involved in this behaviour. Sometimes bats are also observed to imitate other individuals grooming themselves (Vaughan & Vaughan 1986).
Some bat species have distinct fur patterns, which may serve as visual recognition signals (Fenton 2001), in addition to scents and sound, although fur patterns may also serve as camouflage (Neuweiler 2000). Threat displays are common in for example Carollia perspicillata (Phyllostomidae), and includes wing shaking, harsh sounds, and aggressive looks such as extension of the tongue (Fleming 1988). Sexual displays are also common. The monogamous Lavia frons and Cardioderma cor (Megadermatidae), perform stereotypical circular flights, described as aerial ballets (McWilliam 1987; Vaughan & Vaughan 1986). Among Saccopteryx bilineata (Emballonuridae), the males defend territories where they maintain harems. In front of the females of the harem, they perform sexual displays, which include stereotyped singing, and also shaking of wings and hovering. The wing shaking presumably enhances the effect of olfactory glands by spreading pheromones, but it may also function as a visual signal to draw the females’ attention (Chase 1972).


Multimodality – vision and echolocation

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.
The Australian ghost bat Macroderma gigas (Megadermatidae) also has a similar prey detection range for vision as for echolocation. Since this species also has good auditory sensitivity in the sonic range (Fiedler 1979; Kulzer et al. 1984), it switches between vision, echolocation and passive listening (Pettigrew et al. 1986; Pettigrew et al. 1983). For frequencies below 20 kHz, the acoustic axis (as defined from the directionality of the pinna and noseleaf) of Macroderma gigas is aligned with the visual axis (defined by areas of highest ganglion cell density), indicating that auditory cues help the bats to visually detect the source of the sound (Pettigrew 1988). In fact, a major function of sound localisation in animals is to direct the eyes toward the sound-source (Heffner & Heffner 1992; Heffner et al. 1999). This reflex is even quicker than the reaction to a flashlight (Whittington et al. 1981), and hence suggests that hearing is closely co-ordinated with vision (Heffner 1997).
Sound localisation acuity is related to retinal organisation and the width of fields of best vision (defined as the portion of the retina with at least 75% of maximum ganglion cell density, Heffner et al. 2001). Animals with narrow fields of best vision (foveae) have generally better localisation acuity than animals with broad or elongated fields of best vision (visual streaks). The retinas of microchiropteran bats are loosely arranged in visual streaks and the density of ganglion cells falls irregularly toward the periphery. The field of best vision is concentrated in the temporal part of the retina and seems to be broader in frugivores than in insectivorous species (Heffner et al. 2001). Overall, there is a higher ganglion cell density in the inferior part of the retina than in the superior (Marks 1980; Pettigrew et al. 1988; Koay et al. 1998; Heffner et al. 2001; Eklöf unpublished). This means that the sharpest image on the retina results from light reaching the eye from above, and consequently, the bat eyes focus slightly upwards. Without moving their heads, bats are looking up (Pettigrew 1988). The functional significance of this can be difficult to establish, but it seems likely that vision and echolocation have evolved to provide the bat with as little information overlap as possible. While echolocation call emission and hearing is most effective in the flight direction and downwards (Schnitzler & Grinnell 1977; b), vision serves as a complement by being most effective upwards it thus gives additional information of obstacles and landmarks further away. In Megachiroptera, which do not echolocate, one would thus expect the fields of best vision to be above rather than below the optic disk, which in fact seems to be the case (Pettigrew 1986).
All bats have well developed retinofugal projections (pathways of information from retina to visual cortex) to the lateral geniculate nuclei as well as to the superior colliculus (see above), which are the main targets for retinal projections in mammals (Pentney & Cotter 1976; Suthers & Bradford 1980; Reimer 1989). In the superior colliculus, different sensory modalities are integrated and transformed, and the output may be perceived as a “new product” (Stein & Meredith 1993). The capacity to deal with multisensory information is however developed first after experience of multimodal inputs (Wallace & Stein 2001). The superior colliculus controls for example eye movements, which serves to keep objects of interest in the focal field. Auditory projections to the superior colliculus are generally sparse in mammals. However, in the mustache bat Pteronotus parnellii (Mormoopidae), at least three areas in the brain stem contribute with well-developed auditory projections to the superior colliculus. It has been shown that pinna movements can be controlled in the same way as eye movements in other mammals (Covey et al. 1987), and thus that orienting behaviour can be influenced through auditory as well as through visual feedback. It is also known that auditory stimuli can trigger visuomotor neurones and hence that the eyes can respond to sounds (Stein & Meredith 1993). Combined sensory inputs can enhance perception and detection, but also cause behavioural depression, for example when the cues are contradictory, as in the case with bats and windows (discussed above). Cats have been shown to respond “half way” between contradicting sounds and images (Stein & Meredith 1993), but in most cases when animals have multiple cues to choose from, one can see a clear sensory hierarchy (e.g. Dyer & Gould 1981), so also in bats (Chase 1983). However, the hierarchy can change depending on the behavioural context. Visual cues have been shown to have precedence over auditory cues in for example escape behaviour and when commuting (Chase 1981; Chase 1983; Mistry 1990; Paper V). In cases where echolocation and visual cues are complementary rather than contradictory, the bats may still rely on vision over sonar. In a study on brown long-eared bats (Plecotus auritus), feeding from bowls presenting different sensory cues (Paper I), the bats scored best in situations where both visual and sonar cues were present. The visual information seemed however to be the more important.
It has been suggested that there sometimes can be interference between the two senses. For example, Simmons (cited in Chase 1981) has noted that some bats have a problem learning acoustic discrimination when visual cues are present, but can easily perform the same task in darkness. When trained to respond to black or white triangles of different size, Myotis lucifugus (Vespertilionidae) responded to brightness cues rather than the size of the triangles, although these bats are capable of size discrimination by echolocation (Ellins 1970; Masterson & Ellins 1974). This suggests that interference may have occurred, or at least that the bats had a preference for visual cues in this case.
It is not yet known if bats can perform cross-modal recognition, i.e. learning an object using one sense and then immediately recognising the same object by using another sense, which is the case with for example bottle nose dolphins Tursiops truncatus. These animals can integrate information from vision to echolocation just as well as from echolocation to vision. Hence, what the dolphins perceive from one sense is functionally similar of what it perceives from the other (Pack & Herman 1995).
Although the question of how sensory inputs are combined in bats remains unsolved, several authors have shown the importance of multimodality (Pettigrew et al. 1983; Schmidt 1988; Hessel & Schmidt 1994). In a two choice test, two phyllostomid bats (Desmodus rotundus and Phyllostomus discolor) were trained to respond to a combination of visual, olfactory and acoustic stimuli, and were then presented with one of the three modalities separately (Schmidt et al. 1988). It was found that Phyllostomus discolor chose the visual stimuli to a higher degree, whereas Desmodus rotundus preferred the passive acoustic stimuli. However, both bats were able to respond to all three modalities, although responses to the olfactory stimuli needed additional training, as also noted by Hessel and Schmidt (1994), when studying Carollia perspicillata. However when the Carollia had learned to respond to the olfactory cue, this became the preferred stimuli, which was not the case with Desmodus or Phyllostomus, which both used two other senses. This clearly shows that bats use an array of different senses in the field, and that ecology, feeding strategies and behavioural context all influence the use of different modalities.
Echolocation may be the most important innovation throughout bat evolution, allowing these animals to explore a niche of their own. But there is more to the sensory ecology of microchiropteran bats, where vision is an important piece of the puzzle and certainly needs further attention in the future.

 
 

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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
Behaviour 66, 949-953

PAPER II. Eklöf, J., Svensson, A. M. & Rydell, J. 2002. Northern bats (Eptesicus nilssonii) use vision but not flutter-detection when searching for prey in clutter. - Oikos 99, 347-351

PAPER III. Rydell, J. & Eklöf, J. 2003. Vision complements echolocation in the aerial hawking northern bat (Eptesicus nilssonii)
- Naturwissenschaften 90, 481-483

PAPER IV. Eklöf, J. 2003.
Visual acuity and eye size in insectivorous bats. - Manuscript

PAPER V. Eklöf, J., Tranefors, T. & Vázquez, L-B. 2002. Precedence of visual cues in the emballonurid bat Balantiopteryx plicata. - Mammalian Biology 67, 42-46

PAPER VI. Karlsson, B-L., Eklöf, J. & Rydell, J. 2002. No lunar phobia in swarming insectivorous bats (family Vespertilionidae). - Journal of Zoology London 256, 473-477

 

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