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 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).

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).

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.

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).

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