Vision in echolocating bats
Johan Eklöf
Dissertation
Göteborg University
Department of Zoology
Box 463
SE-405 30 Göteborg
Sweden
Avhandling för filosofie doktorsexamen i zoomorfologi, som enligt
Naturvetenskapliga fakultetens beslut kommer att offentligen försvaras
onsdagen den 28 maj 2003, kl 10:00 i föreläsningssalen, Zoologiska
institutionen, Medicinaregatan 18, Göteborg. Fakultetsopponent är
Professor Paul Racey, University of Aberdeen.
0
Bat - Bats
bat (b t)
n. A binge; a spree
n. A stout wooden stick; a cudgel
n. Any of various nocturnal flying mammals of the order
Chiroptera, having membranous wings that extend from the
forelimbs to the hind limbs or tail and anatomical adaptations
for echolocation, by which they navigate and hunt prey
v. To hit
v. To wander about aimlessly
v. To discuss or consider at length
bats
adj. Crazy; insane
bat out
To produce in a hurried or informal manner
off the bat
Without hesitation; immediately
go to bat for
To give assistance to; defend
not bat an eye
To show no emotion; appear unaffected
have bats in
(one's) belfry
To behave in an eccentric, bizarre manner
Göteborg University 2003
ISBN 91-628-5699-5
1
A doctoral thesis at a university in Sweden is produced either
as a monograph or as a collection of papers. In the latter
case, the introductory part constitutes the formal thesis,
which summarises the accompanying papers. They have
already been published or are manuscripts at various stages
(in press, submitted or in ms).
Illustrations by Olof Helje
2
3
Eklöf, J. Vision in echolocating bats
Zoology Department, Göteborg University
Key words: acoustic clutter, foraging tactics, Microchiroptera,
perception, sensory ecology, ultrasound, visual acuity
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
4
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.
5
Eklöf, J. Syn hos ekolokaliserande fladdermöss
Zoologiska institutionen, Göteborgs universitet
SAMMANFATTNING
Fladdermöss av underordningen Microchiroptera använder sig av
ekolokalisation (sonar; SOund Navigation And Ranging) för att orientera och
för att finna byten i mörker. Sonar ersätter således till viss del den
funktion som synen har hos många andra djur. På grund av uttunningen
av ljudvågor i luft och så kallat ”klotter” är dock räckvidden vanligen
begränsad till ett fåtal meter. Fladdermöss måste därför använda sig av
andra sinnesintryck för att komplettera den ibland begränsade
information som sonar ger. I denna avhandling belyser jag synens roll i
fladdermössens liv.
Fladdermössens ögon är vanligen små och kan verka obetydliga, men
variationen är stor. Hos arter som plockar byten från underlag (gleaners)
och bland fruktätare finner man de största ögonen. Alla fladdermusögon
är dock anpassade för svagt ljus, med stora linser och breda receptorfält.
Fladdermöss är relativt bra på att upptäcka små skillnader i belysning och
deras synskärpa försämras inte nämnvärt i ljusförhållanden vi skulle
uppfatta som totalt mörker. Synskärpa eller upplösningsförmåga varierar
dock mycket mellan olika arter. Man kan mäta upplösningsförmåga
antingen teoretiskt genom att räkna ganglieceller i ögat, eller genom
beteendestudier, i vilka fladdermössen presenteras med roterande
linjemönster av olika storlek. Vissa av våra svenska Myotis-arter ser inte
mycket bättre än att de kan separera objekt med 5° mellanrum, medan
den amerikanska Macrotus californicus kan separera objekt med mindre
än 0.06°, vilket ungefär motsvarar upplösningsförmågan hos en hund.
Huruvida fladdermöss kan skilja ut olika former och mönster med hjälp
av synen verkar också variera betydligt mellan olika arter, men generellt
verkar frukt- och nektarätare vara bättre på detta än sina insektsätande
släktingar.
En av de mest grundläggande av ögats funktioner är att registrera
mängden ljus i omgivningen och på så vis kalibrera den inre klockan.
Vissa tropiska fladdermöss undviker att flyga ut om natten är för ljus, till
exempel då det är fullmåne, ett beteende vi inte finner i någon högre
utsträckning bland fladdermössen på våra breddgrader.
Eftersom sonar endast fungerar tillfredsställande på korta avstånd,
används synen främst på längre håll, för att till exempel finna landmärken
6
och för att undvika hinder på väg till och från födoplatser, eller under
migration. I sådana situationer verkar det som om synintryck är viktigare
än information från sonar. Även inom räckvidden för sonar kan man
ibland se att fladdermöss förlitar sig till synen, särskilt om sonar- och
synintryck står i konflikt. Mängden ljus och tiden på dygnet kan också
avgöra vilket av sinnena som har företräde.
Frukt- och nektarätande fladdermöss har generellt sett
bättre syn än insektsätare och kan förmodas utnyttja synen i relativt stor
utsträckning då de söker efter föda. Men även insektsätare tar hjälp av
syninformation då det behövs. Långörad fladdermus Plecotus auritus
plockar ofta stillasittande insekter från blad och använder då framför allt
sin känsliga hörsel för att lokalisera ljud som bytena själva åstadkommer.
Den använder dock synintryck hellre än ekolokalisation som komplement
till den passiva hörseln. Nordisk fladdermus Eptesicus nilssonii använder
sig delvis av syn för att finna stora stillastående byten bland växtlighet,
byten som är svåra att urskilja med hjälp av sonar. Detta trots att de har
en relativt begränsad visuell upplösningsförmåga, ca 1°, vilket är ungefär
60 gånger sämre än en människas.
Ekolokalisationen är utan tvekan det som gjort fladdermössen till en av
de mest framgångsrika och mångskiftande däggdjursgrupperna på jorden.
De har dock behållit ett funktionellt synsinne som ett viktigt komplement.
De, liksom vi använder sig av så många olika sinnesintryck som möjligt
för att lösa livets uppgifter.
7
CONTENTS
INTRODUCTION.……………………………………………………...10
VISION IN ECHOLOCATING BATS
The microchiropteran eye………………………………………….. 12
The brain and the retinal pathways………………………………… 15
What bats can see…………………………………………………... 17
Vision in orientation and navigation……………………………….. 24
Vision in foraging and prey detection……………………………....27
Predator surveillance and social behaviour………………………....33
Multimodality – vision and echolocation………………...…….… . 34
ACKNOWLEDGEMENTS....…………….……………………….…... 38
REFERENCES…………………………….…………………………… 39
PAPER I.
Eklöf, J. & Jones, G. 2003.
Use of vision in prey detection by brown long-eared
bats Plecotus auritus. - Animal Behaviour (In Press)..… 48
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….…………………………………. 62
PAPER III.
Rydell, J. & Eklöf, J. 2003.
Vision complements echolocation in the aerial
hawking northern bat (Eptesicus nilssonii)
- Submitted manuscript……………………………...…. 70
PAPER IV.
Eklöf, J. 2003.
Visual acuity and eye size in insectivorous bats.
- Manuscript………………………...…………………... 80
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……………………………………………………. 92
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….……………………………….100
8
9
B
ats (Order: Chiroptera) are among the most diverse and abundant
mammals on earth and the thousand or so species comprise about one
fourth of all mammalians. Bats occur throughout the world, except the
Polar Regions, and show a remarkable wide range of habitat use,
behaviour, morphology, and diet. Most bats feed on insects but there are
also bats that feed on fruit, nectar, fish, small vertebrates, and blood. Bats
are the only mammals that have evolved active flight, and they can
navigate through complete darkness by using echolocation or sonar
(SOund Navigation And Ranging). Bats live almost everywhere, in tropical
jungles as well as in cities; they inhabit caves, trees, houses, churches,
bridges, coiled banana leafs, bamboo canes, and some species even build
their own tents by using large leaves. Bats have a remarkable spatial
memory and are quick learners. They can form colonies of up to 20
million individuals, eat hundreds or thousands of insects every night and
migrate across continents. Many bats hibernate through a cold winter and
some can reach more than 40 years of age. Despite this, bats are seldom
people’s number one choice of favourite animal. Instead, bats have
become symbols of darkness, doom and occultism in the western world.
They often appear in not so flattering contexts, such as in myths, scary
movies, heavy metal lyrics, and are often one of the most important
ingredients in witches’ brews. Being called an old bat is not a
compliment, and having a bat in one’s belfry is not very often socially
accepted. In the eastern world, however, bats are considered as symbols
of fortune and a long, prosperous life. Nevertheless, the bats’ leathery
wings and their ability to navigate through the night are presumably two
reasons behind their often somewhat scary reputation, as well as the two
main reasons behind their success as a group. But how do they perceive
the world; or as Thomas Nagel (1974) put it in his classic paper: what is it
like to be a bat?
All information about the surrounding world is filtered through our
senses and processed in our brains in order to give us just the right kind
and amount of information to help us make proper decisions. This is true
for all animals, although the senses receiving the information and the
brains that process it differ across the animal kingdom. The type and
amount of information that is needed obviously varies considerably
depending on life style. What humans cannot perceive tend to be called
ultra-, infra-, or extra-something. We do not know what ultraviolet light
looks like, only that it gives us a nice tan. We cannot hear infrasounds
although elephants can, which is why we and not the elephants invented
10
the telephone. Many animals live entirely in the world of ultra-, or infra-,
making it hard for us to relate to their every day life, or as Thomas
Carlyle (1837) elegantly put it: “In every object there is inexhaustible
meaning; the eye sees in it what the eye brings means of seeing. To
Newton and to Newton’s dog Diamond, what a different pair of
universes.” Bat echolocation is different from any of the senses that we
are familiar with, and therefore, we cannot know or even imagine how
they experience the world; or as in the words of Thomas Nagel (1974):
“Anyone who has spent some time in an enclosed space with an excited
bat knows what it is to encounter a fundamentally alien form of life.”
With this in mind, it may seem impossible to study sensory ecology, and
still, we try. We accept that there is information outside our perception
range, although we will never be able to fully understand those things.
We may perhaps be able to understand how a bat collects and uses
information from the environment, but never what this really is like for
the bat. We may however, from a human point of view, describe
behaviour and reactions of animals under defined conditions. For
example, when studying bats flying, and recording and describing
echolocation calls, we can tell that sonar is a high precision tool, as good
as vision for perceiving and identifying objects, only entirely different.
But we begin to understand that echolocation alone is not enough to fully
experience the world as a bat. As high frequency sounds attenuate rapidly
in air, the effective range of echolocation is limited to a few metres in
practice. Background echoes, known as clutter, also impose severe
constraints on the use of sonar, and for a bat to perceive distant objects or
objects hidden in vegetation, other senses must be used. One of these
senses is vision. However, looking at a typical bat eye gives little hope of
any breathtaking visual adventures. The eyes are often small and
inconspicuous, especially compared to the more fanciful ears and noseleafs of many bats, and considering our own sensory limits and the fact
that bats fly at night, it is not hard to imagine why an expression like “as
blind as a bat” exists. But still, bats do have eyes and perhaps “as blind
as we would be if we had bat eyes” would be a more suitable expression.
As I will discuss in this thesis, bats do have eyes that function for bats. In
the same way humans have a sense of smell that function for humans,
although a dog, or a bat for that matter, probably would not be impressed!
The aim of this introductory chapter is to put my work into perspective by
summarizing current knowledge of the role of vision in the lives of the
echolocating bats.
11
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.
Family &
Species
Vespertilionidae
gleaning insectivores
Eye ball axial
length (mm)
Lens axial
Lens radial
Eyediameter (mm) diameter (mm) weight (mg)
Mean bodyweight (g)
Plecotus auritus
Myotis myotis
--3.1 2
--1.3 2
1.65 7
1.6 2
-----
76
26 6
--1.68 1
--1.9 5
----1.7 2
0.77 9
0.6 1
--------1.03 2
0.91 9
0.94 1
----0.95 7
1.25 7
1.43 2
64
--4.4 4
---------
14 4
7.3 8
10 4
10.5 11
56
10 10
27 6
2.6 9
-----
1.5 9
1.1 9
---
1.8 9
1.4 9
---
10.4 9
7.4 9
4.6 9
79
49
39
Vespertilionidae
aerial-hawking insectivores
Eptesicus fuscus
Myotis sodalis
Myotis lucifugus
Nyctophilus gouldi
Myotis mystacinus
Myotis daubentonii
Nyctalus noctula
Emballonuridae
aerial-hawking insectivores
Saccopteryx bilineata
Saccopteryx leptura
Rhynconycteris naso
12
Tab 1 - cont
Species
Molossidae
aerial-hawking insectivores
Molossus ater
Eumops perotis
Eye ball axial
length (mm)
Lens axial
Lens radial
Eyediameter (mm) diameter (mm) weight (mg)
mean bodyweight (g)
--3.3 6
-----
-----
3.44 9
---
26 9
486
0.66 9
---
---
0.6 9
69
1.8 5
---
--0.49 9
--0.68 9
-----
--7 12
7.0 5
---
---
---
120 6
2.62 1
3.9 9
3.94 1
2.0 9
--------4.0 6
---
1.28 1
1.9 9
1.95 1
----2.0 9
--1.9 9
-----
1.75 1
2.4 9
2.44 1
----2.3 9
--2.2 9
-----
8.5 4
1.04 9
40 3
6.22 9
14 3
11.75 9
24.2 9
70.0 9
27.4 4
30.4 9
16 4
69
77 3
99
15 3
18 9
12 9
40 9
38 4
61 9
2.5 7
---
-----
-----
11 4
14.1 9
29 4
40 9
2.1 6
---
---
---
58 6
----0.9 9
--0.35 9
0.42 9
--0.7 9
0.7 9
1.8 9
1.16 9
0.90 9
16 9
79
18 9
Natalidae
aerial-hawking insectivores
Natalus tumidirostris
Rhinolophidae
flutter-detecting insectivores
Rhinolophus rouxi
Rhinolophus hipposideros
Megadermatidae
gleaning insectivores/carnivores
Macroderma gigas
Phyllostomidae
frugivores and nactarivores
Carollia perspicillata
Micronycteris megalotis
Phyllostomus hastatus
Glossophaga soricina
Anoura geoffroyi
Sturnira lilium
Vampyrops helleri
Chiroderma villosum
Artibeus jamaicensis
Artibeus lituratus
Phyllostomidae
sanguivores
Desmodus rotundus
Diaemus youngi
Noctilionidae
piscivores
Noctilio leporinus
Mormoopidae
aerial-hawking insectivores
Mormoops megalophylla
Pteronotus davyi
Pteronotus parnellii
1
Suthers & Wallis 1970, 2 Suthers 1970, 3 Suthers & Bradford 1980, 4 Marks 1980,
Pettigrew et al. 1988, 6 Baron et al. 1996a, 7 Paper IV, 8 Thomson 1982, 9 Chase 1972,
10
Bogdanowicz 1994, 11 Grant 1991, 12 Greenway & Hutson 1990
5
13
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 µm) compared to that of voles (178 µm)
and rats (198 µm), 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 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).
14
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
15
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.
16
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
17
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
18
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.
19
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).
20
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 2° 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). Behavioural acuity
values (b) come from optomotor response tests, and theoretical values (t) are calculated from the
number of ganglion cells per unit area of the retina. Acuity is the minimum separable angle, i.e.
the best values obtained for each species. Asterisks (*) indicate that the ambient light level was
not measured (or that acuity was measured theoretically). For consistency, the values of visual
acuity and light levels were sometimes converted from other units, used in the original paper.
Species
Vespertilionidae;
gleaning insectivores
Antrozous pallidus
Plecotus auritus
Light
(lux)
Visual
acuity
Reference
0.004
0.7
0.25°
0.5°
Bell & Fenton 1986
Paper IV
b
b
*
*
1-10
3600-4800
4400
*
*
0.1
0.1
0.1-0.3
33
6400
3200
40-5500
5000
1°
0.7°
0.8°
0.9°
0.9°
3-6°
0.8°
5°
5°
5°
0.9°
0.9°
0.9°
0.9°
1.5°
Bell & Fenton 1986
Koay et al. 1998
Paper III
Fenton & Portfors unpubl
Fenton & Portfors unpubl
Suthers 1966
Pettigrew et al. 1988
Paper IV
Paper IV
Paper IV
Fenton & Portfors unpubl
Fenton & Portfors unpubl
Fenton & Portfors unpubl
Fenton & Portfors unpubl
Fenton & Portfors unpubl
b
t
b
b
b
t
b
b
b
b
b
b
b
b
*
*
*
0.5°
0.7°
0.4°
Pettigrew et al. 1988
Suthers 1966
Pettigrew et al. 1988
t
b
t
Method
Vespertilionidae;
aerial-hawking insectivores
Eptesicus fuscus
Eptesicus fuscus
Eptesicus nilssonii
Eptesicus capensis
Eptesicus zuluensis
Myotis lucifugus
Nyctophilus gouldi
Myotis brandtii
Myotis mystacinus
Myotis daubentonii
Miniopterus screibersii
Pipistrellus nanus
Pipistrellus rueppellii
Scotophilus borbonicus
Nycticeius schlieffeni
Emballonuridae
aerial-hawking insectivores
Saccopteryx bilineata
Saccopteryx leptura
Taphozus georgianus
21
Tab 2 – cont
Species
Molossidae;
aerial-hawking insectivores
Molossus ater
Tadarida pumila
Tadarida midas
Light
(lux)
Visual
acuity
Reference
*
81-5800
20000
10°
0.9°
0.9°
Chase 1972
Fenton & Portfors unpubl
Fenton & Portfors unpubl
b
b
b
*
160-4800
1.4°
0.9°
Pettigrew et al. 1988
Fenton & Portfors unpubl
t
b
*
*
0.3°
0.3°
Pettigrew et al. 1988
Pettigrew et al. 1988
t
t
*
*
*
*
*
*
0.3°
3°
0.7°
0.3°
0.5°
0.4°
Suthers 1966
Chase 1972
Suthers 1966
Chase 1972
Heffner et al. 2001
Pettigrew et al. 1988
b
b
b
b
t
t
*
3.1
0.04
*
0.7°
0.8°
2.5°
3°
Suthers 1966
Manske & Schmidt 1976
Manske & Schmidt 1976
Chase 1972
b
b
b
b
0.002
0.06°
Bell & Fenton 1986
b
*
*
*
*
*
0.0005
0.3°
0.06°
0.045°
0.01°
0.009°
1.3°
Heffner & Heffner 1992
Heffner & Heffner 1992
Hughes 1977
Cowey & Ellis 1967
Hughes 1977
Neuweiler 1967
t
t
t
b
t
b
Method
Rhinolophidae
flutter-detecting insectivores
Rhinolophus rouxi
Rhinolophus fumigatus
Megadermatidae
gleaning insectivores/carnivores
Megaderma lyra
Macroderma gigas
Phyllostomidae
frugivores and nectarivores
Carollia perspicillata
Glossophaga soricina
Anoura geoffroyi
Sturnira lilium
Artibeus jamaicensis
Artibeus cinereus
Phyllostomidae
sanguivores
Desmodus rotundus
Desmodus rotundus
Desmodus rotundus
Diaemus youngi
Phyllostomidae
Gleaning insectivores
Macrotus californicus
Other mammals;
Rattus (rat)
Canis (dog)
Felis (cat)
Macaca (macaque)
Homo (man)
Homo (man)
22
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
23
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 > 6° 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
24
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
25
(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
26
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).
27
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).
28
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).
29
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,
30
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,
31
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.
32
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).
33
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
34
(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
35
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
36
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.
37
Acknowledgements
First of all I would like to acknowledge all the co-authors of this thesis for obvious
reasons, and I wish to thank Olof Helje for making the splendid bat illustrations. Then I
wish to thank my supervisor and mentor -Jens Rydell – and also, many thanks to the rest
of the Rydell family for your great hospitality.
There are several people having answered several more or less stupid questions on
bats, vision, statistics, experimental design, the meaning of life and other various topics
throughout the years. Especially I would like to thank Donald R Griffin and Brock
Fenton, but also Eric Warrant, Dan E Nilsson, Tom, Gareth Jones, Susan Swift, Kristina
Mieziewska, Winston Lancaster; and of course, many thanks to Cajsa, John G,
Christoffer, Gim, Jen, Christin, John R, Marc, Jenny, Kalle, Kristina, Cess, Bomull,
Tobias, Annika, Christoffer and Staffan, just to mention a few of you.
Just as many people have helped me to make the every day work possible; at the
department, by joining me in the field, on conferences, courses and work shops and to
some extent even in the lab (although some may think I do not know what that is); having
helped me arrange field work and experiments, being guides, eye suppliers, hosts, or just
good company during batting. Especially I wish to thank Monica, Tompa and Cajsa,
thanks also to Maria, Héctor, Henke, Luis-Bernardo, Hans, Marie, Gabriela, Stefan, Åsa,
Per, Britt-Louise, Anna, Lee, Dr. F-Jo, Blomman, Karl-Johan, Stefan, Sean, Jorge, Jenny,
Andreas, Eric, Lars-Erik, Cess, Annemarie, Magnus, Berndt, Dave, Anne-Sofie, Bengt,
Mia, Lilioth, the “NASBR and Chamela-students”, the Lövhaugs, all other department
employees not mentioned, and of course Mexican hospitality and British humour.
For unknown reasons, I have been deeply involved, not only in research and
teaching, but also in the work of the faculty board, the Swedish Association of Scientists
and the Students’ Union. I wish to thank the various members of all the different working
groups and committees, not at least Cajsa, Marie, Stefan Henrik, and Andreas.
There are other things but science, like having almost normal conversations, sharing
stupid ideas, trying to do music, lying on beaches, e-mailing, having coffee and drinking
beer, and presumably some other stuff as well. For those things, I wish to thank Per and
Andreas for helping me to create “PSL” which for a while brought order to my life, much
in the same way as “Johnny” did, only different. I wish to thank the e-mailers, the
floorballers, the chatters, the Herb Boys crew and fan club, the coffee drinkers and the
travellers. There is no doubt that the Friday after work sessions have been almost as
important as the actual research for being able to finish this thesis. I wish to acknowledge
the most frequent ones: Christoffer, Anna, Viktoria, Ågot and lately Jenny P. But of
course, Sara, Erik, Fredrik, Jenny T, Linda, Tove, Goran and a whole bunch of other youknow-who-you-are. There are two persons having shared my biology- as well as my non
biology-time, to a larger extent than perhaps any others: first of all, thank you Cajsa for
not bringing your calculator; and for numerous moments thereafter, and second, Tompa,
for making everyday April fools day.
Thank you all on the second floor: Per, Bengt, Stig, Gunnar, Anders, Inger, Lena,
Åke, Jan, Sebbe, Björn, Jenny, Malin, Urban, Anna H, Anna Z, Monica, Susanne, Ulla,
Mare, Christoffer, Arne, Marcus, other hangarounds, not mentioned, past and present.
Thank you mom, dad, and Kristian, and thanks to all friends in the real world. My work
has been funded by Kungliga och Hvitfeldtska Stiftelsen, Lunds Djurskyddsfond, Knut
och Alice Wallenbergs Stiftelse, Folke Eklöf, Adlerbertska Forskningsstiftelsen, Wilhelm
och Martina Lundgrens Vetenskapsfond, Kungliga vetenskaps- och Vitterhetssamhället i
Göteborg, Stiftelserna Paul och Marie Berghaus Donationsfond, J A Ahlstrands
Testamentsfond, Lars Hiertas Minne, and Rådman & Fru Ernst Collianders Stiftelse FVÄ,
and of course CSN.
Finally I wish to acknowledge (please fill out your name); believe me you are not really forgotten.
38
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47
I
”Love looks not with the eyes,
but with the mind; and therefore
is winged Cupid painted blind”
- William Shakespeare
48
49
Animal Behaviour – In Press
Use of vision in prey detection by brown long-eared bats Plecotus auritus
JOHAN EKLÖF1 & GARETH JONES2
1
2
Zoology Department, Göteborg University, Sweden
School of Biological Sciences, University of Bristol, UK
Eklöf & Jones, Use of vision in Plecotus auritus
Correspondence
Johan Eklöf, Zoology Department, Göteborg University, Box 463, SE-405 30
Göteborg, Sweden. E-mail: [email protected]
Gareth Jones, School of Biological Sciences, University of Bristol, Woodland
Road, Bristol BS8 1UG, UK
ABSTRACT
We investigated the ability of brown long-eared bats (Plecotus auritus) to make
use of visual cues when searching for food. By using petri dishes containing
mealworms that were subjected to different levels of illumination, we presented
four bats with different sensory cues: visual cues, sonar cues and a combination
of these. The bats preferred situations where both sonar cues and visual cues
were available, and the visual information was more important than the sonar
cues. The bats did, however, emit echolocation calls throughout the experiments.
50
Microchiropteran bats use echolocation for orientation, and often for prey
detection, and can thus operate in darkness and under unpredictable lighting
(Griffin 1958). However, as high frequency sounds attenuate quickly in air, and
limit the echolocation range (Kick 1982; Kalko & Schnitzler 1993; Fenton et al.
1995), sonar cannot be effectively used for detection of small targets over long
distances. Also, for echolocating bats foraging close to vegetation, separation of
prey from the background clutter (echoes from objects other than the target of
interest) is usually problematic (Schnitzler & Kalko1998; Arlettaz et al. 2001;
Jensen et al. 2001). Therefore, some bats use for example prey-generated sounds
(Ryan & Tuttle 1987; Arlettaz et al. 2001) and smell (Thies et al. 1998) as
additional cues when searching for prey. Few studies have addressed the
possibility that visual cues may also be important for detection of prey. The
aerial hawking northern bat (Eptesicus nilssonii: Vespertilionidae), is guided by
visual cues when searching for the large and conspicuously white ghost swifts
Hepialus humuli (Lepidoptera), hovering among high grass (clutter) at dusk
(Eklöf et al. 2002). Other aerial hawking bats, such as Craseonycteris
thonglongyai (Emballonuridae) might potentially use visual cues by making use
of the bright sky, against which insects are seen as silhouettes (Pettigrew 1980).
The California leaf-nosed bat (Macrotus californicus) uses a gleaning foraging
tactic, and catches prey from the ground. This species is the only bat so far
shown to be capable of catching prey by using vision alone (Bell 1985).
The brown long-eared bat Plecotus auritus is also a gleaning bat,
that sometimes takes insects from leaves (Swift 1998). This means that it faces
the problems of detecting prey in a cluttered environment. Its echolocation calls
are faint and short FM (frequency modulated) sweeps (Ahlén 1981; Parsons &
Jones 2000) which may be an adaptation for foraging close to vegetation or,
alternatively, may be used only for spatial orientation (Arlettaz et al. 2001).
Passive listening plays a major role for detecting the prey in the long-eared bat
(Anderson & Racey 1991). The ears are large and the hearing is exceptionally
sensitive to sounds around 15 kHz, close to the frequencies emitted by insects
moving in clutter (Coles et al. 1989).
Plecotus auritus also has relatively big eyes compared to many
other insectivorous bats (Cranbrook 1963), suggesting that these bats also have
relatively good vision. Eisentraut (1950) was able to train brown long-eared bats
to discriminate between black and white 9-cm square shaped cards, but when he
presented the bats with a circle and a cross they failed to make the right choice.
This indicates that P. auritus can discriminate between different targets by using
vision, but not different patterns. This is in contrast to some phyllostomid bats
(Suthers & Chase 1966; Suthers et al. 1969), which show more sophisticated
discrimination of patterns. However, Eisentraut’s experiments were carried out
in bright light, and as subsequently shown by several authors, microchiropteran
vision works better in dim ambient light (i.e. dusk and dawn illumination) than in
bright daylight (Bradbury & Nottebohm 1969; Ellins & Masterson 1974; Hope &
Bhatnagar 1979).
The aim of this study is to investigate if brown long eared bats
use visual cues in addition to sonar cues when searching for prey. Its large eyes
and gleaning foraging behaviour suggest that this may be the case. We quantified
51
the ability of brown long eared bats to find prey by using vision alone; i.e. to find
prey on dark and dimly illuminated backgrounds and also behind a transparent
surface.
METHODS
The study was conducted in the School of Biological Sciences at Bristol
University, UK. Four female Plecotus auritus were captured at their roost
(Ilminster, Somerset) 23 April, and released at capture site 12 May 2002. They
were kept in a 2.2m x 3m x 3m flight room, where also the experiments took
place. The room had ventilation installed and the bats could move around freely
and they had several places to hide, including boxes and pieces of cloths on the
walls. The bats were fed on mealworms with vitamin supplements. They were
fed by hand the first day, presented with bowls containing mealworms the
second day, and could feed by themselves from the bowls from day three. Water
was given in the same kind of bowls and was available to the bats on the flight
room floor all the time (and changed twice every day). The temperature of the
room was 13-16° C, except during the experiments, when it was 20° C. The
daylight period was partly reversed (lights on at 03:00 and off at 16:00) with
experiments starting at ca. 18:00. All the bats lost a little weight (0.5 - 1g) during
the first two days, but on the day of release, they all had their original weight
except one that had gained 1g.
Experiment 1
Two halogen light sources (Schott) with two fibre-optic goose necks each were
placed on the floor in the flight room. At the end of each goose neck, we attached
plastic tubes, two of them with neutral density light filters (reducing light
intensity with 50%), and the other two with dark covers (letting no light
through). This set-up provided us with two circular 25-cm diameter areas of dim
light (4 lux; measured with a Gossen Mavolux digital light meter) and two
similar “areas of darkness” (0.2 lux), 30-40cm apart on the flight room floor. The
overall illumination in the room never exceeded 0.1 lux. The plastic tubes on the
fibre-optic goose necks could be switched and, hence, the arrangement of the lit
and dark areas could be changed. On the floor; under each goose neck we put a
petri dish (9 cm diameter, 1.8 cm deep), placed inside the lid belonging to it,
either with mealworms in the petri dish itself or in the lid (hence between lid and
dish). This provided four different combinations of sensory cues.
1: lit area with mealworms in the dish (visual and sonar cues).
2: lit area with mealworms placed in the lid (visual cues only)
3: dark area with mealworms in the dish (sonar cues only).
4: dark area with mealworms in the lid (no cues except from the dish itself).
We assume that acoustical cues arising from the mealworms moving in the
dishes or the lids were the same in all cases.
During the experiment the bats were flying individually in the
flight room for 30-40 minutes, feeding from the petri dishes. Each landing at a
52
dish was recorded as a foraging attempt, and as soon as a landing was recorded
the arrangement of the feeding situation was changed. To prevent the bats from
using spatial memory the experimental area was divided in two parts (A & B),
which were used alternately, so that a foraging attempt in area A was followed
by an experiments in area B. The light sources could be placed at four different
positions within each area, and the positions were changed at random after each
feeding attempt. Also the arrangement of the four petri dishes (presenting the
different sensory cues) was changed at random after each feeding attempt.
Hence, in total there were 32 potential positions for each petri dish.
An infra red sensitive video camera (Sony Mini DV TRV9E
Handycam) with a wide-angle lens was placed above the experimental area. It
was connected to a monitor placed outside the flight room and thus making it
possible to survey the experiments without disturbing the bats.
In order to test if the probability of a feeding attempt at a certain
dish was the same for all bats, i.e. if we could treat the bats as one group, we
applied a Chi square test of homogeneity (testing if a specific distribution is the
same in different situations, in this case for the different bat individuals). Then
we made pair-wise comparisons between dish preferences, i.e. we compared the
probability that one dish was preferred over another. We did so by using 95%
confidence intervals, i.e. intervals having 95% probability of covering our
estimated preferences (number of captures in each category divided by total
number of captures) for the different feeding dishes. As we calculated several
intervals using the same data set, we applied the Bonferroni method for multiple
comparisons.
Experiment 2
To exclude the possibility that the bats considered the light or the petri dishes
rather than the actual prey items as potential food sources, we presented the bats
with two lit areas, one with a petri dish containing mealworms, and one with an
empty dish. The set-up was similar to the one in experiment 1, although only one
light source (with two goose necks) was used, and this time all four bats were
flying simultaneously. We also placed a bat detector (Ultra Sound Advice S-25
set in frequency-division mode) next to one of the petri dishes, and connected it
to a speaker outside the flight room. The different positions of the light source
and the arrangement of the two petri dishes together with the position of the bat
detector, were changed after each feeding attempt and randomised in a similar
manner as in experiment 1. This experiment was also surveyed using an IR
sensitive video camera. The number of feeding attempts at the two petri dishes
was compared using Chi square statistics, and echolocation calls from feeding
bats were noted.
53
RESULTS
General observations
When released in the flight room, the bats typically flew across the feeding area
a few times before deciding from which dish to feed. They usually hovered just
above one of the dishes (10 – 15 cm) for a short period and then landed next to it.
The bats then crawled into the dish to feed. On a few occasions, bats crawled
around the feeding area on the floor to investigate the different dishes. After
capture of a mealworm, the bats consumed it while hanging on one of the walls
in the flight room. Bats moving around consistently emitted detectable
echolocation calls.
Experiment 1
The number of feeding attempts and estimates of preference at the different
dishes are presented in table 1. We found no significant differences between bat
individuals in their probability of feeding at a certain dish (?29 = 7.94, p>0.05).
This means that we do not gain any statistically significant information by
treating the individuals separately, and we therefore pooled the results.
When comparing the number of feeding attempts between each
of the four foraging situations (data and statistics in tab. 1 and 2), we found that
in lit situations, it made no difference if sonar cues were added or not. However,
there were more feeding attempts when sonar cues and visual cues were present,
compared to when only sonar cues were available. This suggests that the bats
predominantly used vision when they searched for prey.
When comparing the frequency of foraging attempts at situations
providing visual or sonar cues only, the bats scored better at the visual cues, and
when comparing sonar cues only to the no cue situation, we found no significant
difference. This analysis too suggests that the bats predominantly relied on
vision and it also suggests that they could not find prey items using sonar alone.
Experiment 2
There were significantly more feeding attempts at lit petri dishes containing
mealworms than at lit empty ones (?21 = 7.7, p <0.01, n =39 & 18 respectively).
This suggests that the bats were able to detect mealworms either acoustically or
visually, and that they did not associate structural features of the food dish with
reward. Hence, the bats were not only heading for the light or the dishes alone.
Echolocation calls were detected both from bats approaching the dish with
mealworms, as well as from bats investigating the empty dish.
54
DISCUSSION
We found that long-eared bats are capable of visual detection of prey, at least
under the light intensity of 4 lux, and that they prefer visual cues to sonar cues if
given a choice. The results also indicate that the bats were unable to detect the
prey items using sonar alone.
There is both experimental and observational evidence that
echolocating bats make use of vision and even give precedence to visual stimuli
in some situations, including long distance orientation (Griffin 1970), detection
of landmarks (Davis 1966), obstacle avoidance (Bradbury & Nottebohm 1969)
and prey detection (Bell 1985). When selecting an escape route in an
experimental set-up, the phyllostomid Anoura geoffroyi used visual cues alone
and disregarded acoustical cues that also were provided (Chase 1981, 1983). The
observation that bats have a tendency to crash into windows of buildings when
released indoors (Fenton 1975) or during natural migration (Timm 1989) also
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. fewer crashes) when the bats are blinded (Davis &
Barbour 1965) or when flying under natural dark conditions, and hence are
“forced” to rely on echolocation (Eklöf et al. 2002). Suthers and Wallis (1970)
studied the eyes of two species of Vespertilionidae (Myotis sodalis and
Pipistrellus subflavus) and four different phyllostomids (Desmodus rotundus,
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 beyond the range of echolocation. Due to the more or less
spherical lenses, it also follows that Microchiroptera has 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
preferably over longer distances, where it may not overlap with echolocation,
which is a short-range operation (Kick 1982; Fenton et al. 1995). Nevertheless
there are some bats, such as Phyllostomus hastatus, which also use vision within
the range covered by their echolocation system, i.e. when approaching a landing
spot (Joermann et al. 1988).
We cannot exclude the possibility that the bats used passive
listening to detect the mealworms, as some other gleaning bats do (Arlettaz et al.
2001). Sounds coming from the prey could have been detected from any of the
dishes, including the dishes with visual cues only and the no cue situation, as live
mealworms were crawling under the petri dishes (in the lids). Also olfactory cues
from the mealworms may have been available to the bats in all four feeding
situations. Hence, olfactory cues and prey-generated sounds may explain some
of the feeding attempts at petri dishes with prey in the lids.
During the experiments, bats were sometimes seen hovering at
positions where no petri dish was available, but where dishes had been available
previously, presumably relying on spatial memory (Neuweiler & Möhres 1966;
Grant 1991; Höller & Schmidt 1996). Hence, the bats tended to revisit positions
where they previously had been rewarded and it seems possible that the results
55
are influenced to some extent by this. However, we believe that our experimental
design, where the position of the dishes were changed after every feeding
attempt, would minimise these effects, and that the results show preference for
feeding dishes, rather than spatial memory.
The results of Experiment 2 allowed rejection of the hypothesis
that bats associated structural features of the food dish with reward, and were
therefore attracted to features of the dishes by associative learning (Siemers
2001). However, as all the bats flew simultaneously in this experiment, we
cannot exclude the possibility that some individuals sometimes explored the
dishes without getting a reliable indication of reward. In the first experiment
there were equally many feeding attempts at the petri dishes providing sonar
cues as at the no cue dishes, which means that we found no indication that the
bats could detect the prey items by using sonar alone. One can therefore
hypothesize that bats having to rely exclusively on sonar may learn to recognize
structures rather than prey.
There were more feeding attempts at the petri dishes providing
visual cues only compared to those that provided sonar cues only. This suggests
that the long-eared bats were capable of finding prey visually and that they even
preferred using vision when possible. Long-eared bats emerge from their roosts
late in the evening (15-55 minutes after sunset depending on the latitude; Swift
1998), which means that they normally operate in very low light levels (<1 lux).
Their technique of gleaning insects off leaves also means that they do not use the
bright sky to backlight prey, which has been suggested to be the case for some
aerial hawking bats (Pettigrew 1980; Vaughan & Vaughan 1986). However,
Eptesicus fuscus (Vespertilionidae) can discriminate differences in brightness in
ambient illumination as low as 0.001 lux, conditions which resemble darkness to
a human dark adapted eye, although the optimal performance is around 10 lux,
which is equivalent to dusk and dawn conditions (Ellins & Masterson 1974).
This suggests that bats can use visual cues under nocturnal conditions. The
resolving power of vespertilionid bats typically ranges between 0.7 and 1 degree
of arc (Marks 1980; Bell & Fenton 1986; Pettigrew et al. 1988), which means
that an object of mealworm size (ca. 2 cm) can be detected from a distance of ca.
1 m. The eyes of long-eared bats are larger than those of most other
Vespertilionidae (Cranbrook 1963), suggesting that they presumably also have
better visual acuity as well as light sensitivity (Land & Nilsson 2002). As the
bats in this study usually hovered above the petri dishes on a height of 10-15 cm,
the mealworms were most likely visible to the bats at least on the lit surfaces.
Cranbrook (1963) noted that long-eared bats, despite their big eyes, did not seem
to look for the food when feeding from bowls, but rather felt about until a prey
item was captured. Studies on northern bats (Eptesicus nilssonii,
Vespertilionidae) catching ghost swifts (Hepialis humulii) suggest that vision is
used primarily in an initial search phase to detect prey, rather than in the terminal
attack (Eklöf et al. 2002). In a similar manner, phyllostomid bats detect landing
grids visually, but use echolocation when performing the actual landing
operation (Joermann et al. 1988). Hence, it seems possible that the long-eared
bats used visual cues for detection, but exploited additional information, such as
echolocation and passive listening during the final pursuit.
56
ACKNOWLEDGEMENTS
We wish to acknowledge Marc Holderied and Julian Partridge for comments on
the experimental design and Jens Rydell for comments on the manuscript. We
also wish to thank John Gustafsson and Catrin Bergqvist for statistical advice.
The study was supported by ”Stiftelsen Paul och Marie Berghaus
donationsfond”, and ”Adlerbertska forskningsstiftelsen” (JE). Research was
performed under licence from English Nature.
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59
Table 1. – The number of feeding attempts and mean proportions of attempts at
petri dishes providing four individuals of Plecotus auritus with different sensory
cues.
sensory cue
visual only
visual/sonar
sonar only
none
bat # 1
12
16
13
3
total
44
bat # 2
27
21
10
8
66
bat # 3
11
14
5
3
33
bat # 4 total
17
21
7
6
51
mean proportion
67
0.34
72
0.38
35
0.18
20
0.10
194
1.0
60
Table 2. – Pair-wise differences between mean proportions of attempts made to
dishes providing different sensory cues, with 95% Bonferroni-corrected
confidence intervals for each difference. If a confidence interval includes zero,
the bats were equally likely to make feeding attempts at the two types of dish.
Sensory cue comparison
p(visual cues) – p(visual/sonar cues)
Confidence interval
-0.04±0.17
preferred dish
no preference
p(visual cues) – p(sonar cues)
0.16±0.14
visual
p(visual/sonar cues) – p(sonar cues)
0.20±0.14
visual/sonar
p(visual cues) – p(no cue)
0.24±0.12
visual
p(visual/sonar cues) – p(no cue)
0.27±0.13
visual/sonar
p(sonar cues) – p(no cue)
0.08±0.10
no preference
61
II
“The Eocene brought
mammals mean
And bats began to sing;
Their food they found by
ultrasound
And chased it on the wing.”
- John D Pye
62
63
64
65
66
67
68
69
III
“You can't depend on your
eyes when your imagination
is out of focus”
- Mark Twain
70
71
Submitted manuscript
Vision complements echolocation in an aerial-hawking bat
Jens Rydell and Johan Eklöf
Zoology Department, Göteborg University, Box 463, SE 405 30 Göteborg,
Sweden.
Corresponding author:
Johan Eklöf, address as above
Tel. +46-317733666
Fax. +46-31416729
E-mail: [email protected]
Abstract
The northern bat Eptesicus nilssonii hawks flying insects in the air using
frequency-modulated echolocation calls. It is known to detect and catch visually
conspicuous prey (white moths) hovering low among grass stalks. To overcome
the problem with acoustic clutter from the grass that interferes with target echo
detection, the bats made use of visual cues in addition to those of echolocation.
However, vision increased the chance of detection only when the moths were at
least 5 cm in wingspan. Smaller targets were detected using echolocation alone.
The mean detection range was 3.5 m, which suggests a visual acuity of 49´ of
arc. This is consistent with results of optomotor response tests and counts of
retinal ganglion cells in closely related species. The results suggest that vision in
Eptesicus bats is not sufficiently sharp for prey detection under normal
conditions but only when the prey is unusually large and conspicuous.
Nevertheless, the northern bat shows flexibility in prey-detection techniques not
previously recognised among aerial-hawking bats.
Key words: acoustic clutter, Hepialidae, insectivorous bats, nocturnality,
ultrasound, visual acuity.
72
Introduction
Functions normally served by vision in most vertebrates have been taken over by
ultrasonic echolocation in insectivorous bats. In particular, the detection and
tracking of flying insects is usually believed to be entirely acoustic (Kalko &
Schnitzler 1993). Ultrasonic echolocation allows detection of very small targets,
but its practical range is normally limited to a few metres, which is due to severe
atmospheric attenuation and spreading loss of high-frequency sound and the poor
reflective power of targets as small as insects (Lawrence & Simmons 1982, Kick
1982). On the other hand, although the eyes of insectivorous bats are small, they
generally have good light-gathering capacity and good focal depth (Suthers
1970, Suthers & Wallis 1970). Vision can therefore be assumed to provide
important cues particularly at ranges beyond that of echolocation, and is
presumably useful for orientation and navigation at night.
However, adaptation of the visual system for nocturnal conditions occurs
partly at the expense of acuity, the ability to resolve details, and this presumably
limits the use of vision for some short-range purposes such as finding prey
(Suthers 1970). Nevertheless, at least some bat species, particularly those that
glean prey from surfaces and for which acoustic clutter (background echoes)
makes echolocation less useful (Arlettaz et al. 2001), have a visual acuity that is
good enough for detection of insects and other objects at close range (Bell 1985,
Joermann et al. 1988).
We recently discovered that vision also plays a role in prey detection by the
northern bat Eptesicus nilssonii (Family Vespertilionidae), an aerial-hawking
species (Eklöf et al. 2002). However, because aerial-hawking bats generally
seem to have poor visual acuity (Suthers 1970), this can be expected to set a
lower limit to the size of insects that can be detected by vision.
Experimental setting and methods
To determine the visual acuity for E. nilssonii foraging under practical
conditions in the field, we took advantage of a natural situation where bats
regularly exploit groups of male ghost swift moths Hepialus humuli (Hepialidae)
displaying over hayfields during midsummer evenings in southern Sweden
(57°N). These moths are silvery white and highly reflective on the dorsal side
and display visually in hovering flight among the grass panicles to attract
females (Andersson et al. 1998). Hepialids are unusual among larger moths in
that they are earless and do not show any evasive response to bat echolocation
calls, whether these are natural or synthetic (Rydell 1998).
At two different moth display sites, each regularly patrolled simultaneously
by up to 10 northern bats (which were not marked), we added dead and spread
individuals to the naturally displaying moth population. The dead moths were
glued on top of steel wires and presented pair wise about 2 m apart and 0.5-0.7 m
above the grass in various parts of the fields. One moth in a pair had its white
73
(dorsal) side up and the other had its dark grey (ventral) side up towards the
patrolling bats. We assumed that the two were equally detectable by echolocation
but that the white moth was more detectable by vision. This assumption was
based on a previous experiment, showing that the moths´ silvery white
coloration, which also contains a UV-component, is particularly contrasting
during their natural display time just after sunset and against a background of
green grass (Andersson et al. 1998). We thus expected the white and the dark
moth to be attacked with equal frequency if bats use echolocation alone but with
unequal frequency if they also use visual cues. To determine the minimum size
of moths detectable by vision, we presented pairs of moths (one white and one
dark) which were either intact (ca. 6 cm wingspan; Eklöf et al. 2002) or where
both had the wingtips cut to give a total wingspan of either 5, 4 or 3 cm. Hence,
size differed between the pairs of moths but the white and the dark moth that
formed a pair were always of the same size. The moths were replaced when
destroyed by the bats, but otherwise reused as long as possible.
To prevent the bats from learning the exact positions of the moths, the pairs
were moved at least a few metres following each attack by a bat. Hence each pair
of moths was attacked only once while in each position. We deliberately
presented the moths at a height where the bats´ echolocation would be
complicated by clutter from the grass, overlapping with echoes from the moths,
so that the bats were encouraged to use visual cues to find the moths. The extent
of the ”clutter overlap zone”, which depends on the duration of the echolocation
calls (7-8 ms), was 0.6-1.2 m above the grass (Jensen et al. 2001).
Moths and bats were observed visually and also acoustically with a Pettersson
D-940 bat detector from a distance of 2-10 m. The visual observations were
facilitated by the relatively good light conditions prevailing at 57°N around
midsummer (June 2002), which always made it possible to see what happened in
sufficient detail. The experiments were performed only as long as moths were
displaying naturally nearby, which occurred for about 30 minutes each evening
(Andersson et al. 1998).
Results
Neither bats nor moths showed any obvious response to our presence. The bats
seemed to forage normally, perhaps because they had become habituated to our
presence over several seasons. The bats typically patrolled in large circles over
the field at a height of 3-4 m (mean 3.5 m). The height was determined by using
a measured and marked lamppost at the edge of the field as a reference. The bats
always emitted echolocation calls during the search as well as throughout the
attacks on the moths. An attacking bat typically performed a rapid and more or
less vertical dive towards the grass while switching from search phase
echolocation calls to a typical “feeding-buzz”, i.e. short pulses and high pulse
repetition rate (Jensen et al. 2001). This behaviour strongly suggests that the
attacks consistently were guided by echolocation.
We counted the number of attacks on white and dark moths and compared the
results for each moth size using one-tailed chi square statistics. Attacks on white
moths were more frequent than on dark moths when the moths were 5 cm or
larger (Fig. 1), suggesting that the detection was facilitated by vision in these
74
cases. The detection of 4 cm and 3 cm moths were apparently not facilitated by
vision and therefore must have been guided entirely by echolocation. We
expected the total number of attacks on large moths to be more frequent than on
smaller moths, because the larger size presumably increased the chance of
detection. Although this appeared to be the case, the absolute attack frequency
(the number of attacks per bat) was difficult to measure because the number of
bats searching for moths over the field changed constantly.
Discussion
Because 5 cm moths were detected visually at a range of 3.5 m, the distance
between the wing tips of the moths represents 49´ of arc. This agrees very well
with theoretical estimates of visual acuity based on counts of retinal ganglion
cells, suggesting 40´ of arc (Pettigrew et al. 1998, Koay et al. 1988) and
behavioural tests of the optomotor response, suggesting at least 1° of arc, in the
closely related species Eptesicus fuscus from North America (Bell & Fenton
1986). Unpublished optomotor response tests of other Eptesicus species, namely
E. capensis and E. zuluensis from southern Africa, suggest that these species
have a visual acuity of at least 54´of arc (M. B. Fenton & C. V. Portfors,
personal communication). Our experiment is the first estimate of the visual
acuity of E. nilssonii.
The visual acuity of Eptesicus spp. appears to be intermediate among bats. It
is much better than in many other aerial-hawking insectivores, e.g. Myotis spp.
(3-6°) (Suthers 1966) but not as good as that of some gleaning insectivores, e.g.
Macrotus californicus and Antrozous pallidus (4´ and 15´, respectively) (Bell &
Fenton 1986). It is comparable to that of vampires and frugivores of the family
Phyllostomidae (42´-16´) and insectivores of the family Emballonuridae (42´23´) (Pettigrew et al. 1998, Suthers 1966, Manske & Schmidt 1976). Why the
visual acuity differs so much among species and genera of bats is not clear.
The repertoire of detection techniques used by northern bats searching for
insects is wide. E. nilssonii usually feeds on swarming insects in open air (Rydell
1989), where echolocation is relatively straightforward and insects or swarms of
insects can be detected through single echoes, so called “glints”. Insects that
move rapidly near vegetation, so that acoustic clutter masks the echoes from the
insects, are detected through their shift in position relative to the background.
This technique obviously requires comparison of the echoes containing both the
target and the background between several successive pulses (Jensen et al. 2001).
When the insects stay among clutter and do not move relative to the background,
as in the present case, few echolocation cues are available and the bats
apparently employ vision to enhance the detection. We have shown previously
that E. nilssonii do not make use of the Doppler-effects induced by the wing
movements of the hovering moths (Eklöf et al. 2002).
However, if vision is useful or not in a particular foraging situation
depends not only on the size of the target and the range, but presumably also on
the contrast between the target and the background and the prevailing light
conditions (Andersson et al. 1998, Ellins & Masterson 1974). In our case, the
prey insects were much larger than most other prey eaten by this species (Rydell
1989) and they also displayed an unusually high contrast against the background
75
(Anderson et al. 1998). Hence, the use of vision for prey detection is probably
unusual in this species, and we can therefore assume that it normally relies on
echolocation alone for this purpose. Nevertheless, our study shows that
echolocating bats are flexible and ready to use whatever information is available
to find food, and, assuming that the visual acuity of E. nilssonii is similar to that
of E. fuscus, we find that these bats are able to use their full visual capacity in the
field.
Acknowledgements
We acknowledge the landowners whose hay fields we partly devastated and T.
Tranefors for practical help and M. B. Fenton and C. V. Portfors for giving
access to unpublished data. The work was funded by the Science Research
Council of Sweden.
References
Andersson S, Rydell J, Svensson MGE (1998) Light, predation and the lekking
behaviour of the ghost swift Hepialus humuli (L.) (Lepidoptera:
Hepialidae). Proc R Soc Lond B 265: 1345-1351
Arlettaz R, Jones G & Racey PA (2001) Effect of acoustic clutter on prey
detection by bats. Nature 414: 742-745
Bell GP (1985) The sensory basis of prey location by the California leaf-nosed
bat Macrotus californicus (Chiroptera: Phyllostomidae). Behav Ecol
Sociobiol 16: 343-348
Bell GP, Fenton MB (1986) Visual acuity, sensitivity and binocularity in a
gleaning insectivorous bat, Macrotus californicus (Chiroptera:
Phyllostomidae). Anim Behav 34: 409-414
Eklöf J, Svensson AM, Rydell J (2002) Northern bats (Eptesicus nilssonii) use
vision but not flutter-detection when searching for prey in clutter. Oikos
99: 347-351
Ellins SR, Masterson FA (1974) Brightness discrimination thresholds in the bat
Eptesicus fuscus. Brain Behav Evol 9: 248-263
Jensen ME, Miller LA, Rydell J (2001) Detection of prey in clutter by the
northern bat, Eptesicus nilssonii. J Exp Bio 204: 199-208
Joermann G Schmidt U, Schmidt C (1988) The mode of orientation during flight
and approach to landing in two Phyllostomid bats. Ethology 78: 332-340
Kalko EKV, Schnitzler HU (1993) Plasticity of echolocation signals of
European pipistrelle bats in search flight: implications for habitat use and
prey detection. Behav Ecol Sociobiol 33: 415-428
Kick S (1982) Target-detection by the echolocating bat, Eptesicus fuscus. JComp
Physiol A 145: 432-435
Koay G, Kearns D, Heffner HE, Heffner RS (1998) Passive sound-localization
ability of the big brown bat (Eptesicus fuscus). Hearing Res 119: 37-48
76
Lawrence BD, Simmons JA (1982) Measurements of atmospheric attenuation at
ultrasonic frequencies and the significance for echolocation by bats. J
Acoust Soc Am 71: 585-590
Manske U, Schmidt U (1976) Untersuchungen zur optischen
Musterunterscheidung bei der Vampirfledermaus, Desmodus rotundus. Z
Tierpsychol 49: 120.
Pettigrew JD, Dreher B, Hopkins CS, McCall MJ, Brown M (1988) Peak
density and distribution of ganglion cells in the retinae of
microchiropteran bats: Implications for visual acuity. Brain Behav Evol
32: 39-56
Rydell J (1989) Food habits of northern (Eptesicus nilssoni) and brown longeared (Plecotus auritus) bats in Sweden. Holarct Ecol 12: 16-20
Rydell J (1998) Bat defence in lekking ghost swift (Hepialus humuli), a moth
without ultrasonic hearing. Proc R Soc Lond B 265: 1373-1376
Suthers RA (1966) Optomotor responses by echolocating bats. Science 152,
1102-1104
Suthers RA (1970) Vision, olfaction and taste. In: Wimsatt WA (ed) Biology of
Bats vol. II. Academic Press, New York, pp 265-281
Suthers RA, Wallis NE (1970) Optics of the eyes of echolocating bats. J Vision
Res 10: 1165-1173.
77
Attacks on moths (%)
Figure 1. - Frequency of attacks by northern bats Eptesicus nilssonii on dead and
spread moths Hepialus humuli mounted on top of wires and presented to
foraging bats in a field among naturally occurring moths. Moths were cut to
different sizes (wingspans) and displayed pair wise, one showing its white dorsal
side up and the other the dark grey ventral side. Higher attack frequency on
white than on dark moths indicates that the bats detected the moths using visual
cues. The asterisk indicates that the 6 cm moths were not cut, but presented at
their natural size (mean 6 cm).
100
n=62
P<0.001
n=56
P<0.01
n=51
n.s
n=45
n.s
50
10
6cm* 5cm 4cm
Moth size
3cm
78
79
IV
“And Bats flew round
in fragrant skies
and wheel'd or lit
the flimsy shapes
that haunt the dusk;
with ermine capes
and woolly breasts,
and beaded eyes.”
?
- Alfred Tennyson
80
81
Manuscript
Visual acuity and eye size in four species of insectivorous bats
Johan Eklöf
Zoology Department, Göteborg University, Box 463, SE-405 30 Göteborg,
Sweden, E-mail: [email protected]
Abstract
Behavioural tests on optomotor responses establish a visual acuity threshold in
four species of bats of the family Vespertilionidae. Three species of Myotis spp.,
which are aerial-hawking bats, responded only to a stripe pattern equivalent to 5
degrees of arc, whereas Plecotus auritus, which is a gleaner, responded down to
0.5 degrees of arc. Eye diameter was positively correlated with visual acuity, and
varied from 0.9 mm in Myotis mystacinus to 1.8 mm in Plecotus auritus. These
results are consistent with earlier findings. The variation in eye size and visual
acuity presumably reflects differences in foraging technique (aerial-hawking vs.
gleaning) and, in particular, how vision is used as a complement to sonar.
Key words: Chiroptera, grating, optomotor response, resolving power, spatial
resolution, vision
Introduction
The microchiropteran eyes are generally adapted for nocturnal conditions in that
they have large corneal surfaces and lenses relative to the size of the eye, and
generally 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). Bat eyes are generally better suited for long- than short
distance operation, and due to the short effective range of sonar, vision is
probably of major importance in guidance over longer distances (Griffin 1958,
1970). Loss of vision drastically reduces the homing performance in many bats
(Williams et al. 1966, Hassell 1963, 1966, Davis & Barbour 1970).
At least some bats are able to use vision over short distances as well, for
example during escape and obstacle avoidance (Chase 1981, 1983, Chase &
Suthers 1969, Bradbury & Nottebohm 1969). There is also evidence that some
species of bats use visual cues to find prey (Bell 1985, Grant 1991, Vaughan &
Vaughan 1996, Eklöf et al. 2002), a task which presumably requires relatively
fine detail discrimination.
Visual acuity has been estimated theoretically, based on counts of the number
of retinal ganglion cells, in several species of bats (Marks 1980, Pettigrew et al.
1988, Heffner et al. 2001), and has shown a large range of variation; from 16’ of
arc in the gleaning carnivorous species Macroderma gigas (Megadermatidae) to
1.4° of arc in Rhinolophus rouxi (Rhinolophidae), an insectivorous flutterdetector (Pettigrew et al. 1988). Optomotor response tests have also shown that
82
the visual acuity varies considerably between species of bats (Suthers 1966,
Manske & Schmidt 1976, Bell & Fenton 1986).
The evidence thus suggests that visual acuity may be correlated with the food
searching technique among bats. In particular, gleaners seem to have better
visual acuity than those that catch insects in the air. The purpose of this study
was to test this hypothesis by examining the optomotor response in some
sympatric insectivorous vespertilionid bats that use different foraging techniques
(gleaning and aerial-hawking), in order to establish a behavioural visual acuity
threshold for these particular species. We also tested the assumption that visual
acuity is positively related to the size of the eyes among insectivorous bats.
Materials and methods
The experiments were performed at the old magnetite mine of Taberg, located
south of Jönköping (57ºN) in southern Sweden. The bats were caught in a mist
net set outside the mine entrance. They were tested for optomotor responses
immediately after capture or as soon they had come to rest. The tests were made
outdoors in the evening between August and November 2002, and between
March and April 2003. To achieve optomotor responses, we used a device
similar to that employed by Suthers (1966) and Bell & Fenton (1986). A bat was
placed in a 20 cm high, 10 cm diameter Plexiglas cylinder surrounded by a 30
cm high and 60 cm diameter, revolving drum (Fig. 1). The natural light was
insufficient for direct observation of the response in most cases, so the study area
was lit up by a 40 W light bulb placed ca. 2 m above and 5 m away from the setup. This provided a light intensity of 0.1-0.7 lux inside the drum (Photometer
IL1400A, International Light Inc.). The drum could be rotated freely and
independently of the cylinder containing the bat. Sinusoidal grating patterns, i.e.
stripes with continuously changing luminance from black to white, of different
fineness was attached to the inside of the drum. The drum was then rotated
around the bat by hand at ca. 5 rpm randomly in both directions, and the
behaviour of the bat was observed from above. Using sinusoidal patterns instead
of black and white stripes reduces the risk of optical illusions, which could
otherwise elicit responses from the bats and thus make the results hard to
interpret (D. Nilsson & E. Warrant personal comm.). We used six gratings with
different stripe width (distance from white to white): 2.84 cm, 1.42 cm, 0.57 cm,
0.43 cm, 0.28 cm and 0.14 cm. From the bats´ point of view this is equivalent to
subtending angles of 5°, 2.5°, 1°, 0.75° (45’), 0.5° (30’) and 0.25° (15’) of arc.
When a response was achieved the grating was switched to a finer pattern until
no response could be recorded, indicating that the bats no longer could resolve
the pattern. At this point a wider pattern was reintroduced to make sure that the
bats still responded to moving stripes. This also served as a control for responses
to stimuli other than the stripes, such as noise originating from the drum.
After testing optomotor responses, we photographed the bats, using a Pentax
645 camera, on 50 ASA medium format slide film. We held the bats by hand so
that the face of the bat was perpendicular to the camera. A ruler was held next to
the bats, providing us with a cm-scale. The photos were scanned and magnified
17x – 33x, and the eye size of the individual bats were measured from the
83
computer screen. The bats were released outside the mine immediately after the
photographs had been taken.
Results
Sixteen individual bats belonging to four different species were caught and
tested: Plecotus auritus, Myotis mystacinus, M. brandtii and M daubentonii.
When tested, the bats typically moved about in the Plexiglas cylinder for a while
before coming to rest, and they sometimes continued to move around during the
tests. However, most bats unambiguously responded to the rotating stripes by
moving their heads in a snappy, stereotyped manner, either following the
rotational direction or the opposite direction, as described earlier by other
authors (Suthers 1966; Bell & Fenton 1986).
The results were relatively consistent within a species and genus but differed
considerably between the two genera. The species of Myotis responded only to
the largest pattern (5° of arc), while all the Plecotus auritus individuals except
one responded down to the pattern equivalent to 1-0.5° of arc (Table 1).
The eye size varied with visual acuity as expected (Table 1). The Myotis
species had smaller eyes (ca. 1 mm diameter) than Plecotus auritus (ca. 1.7 mm).
Discussion
Visual acuity is highly variable among vespertilionid bats, which presumably
reflects the extent to which bats of the different genera make use of vision and
what they do with it. As might have been expected, the relatively big-eyed
gleaner Plecotus auritus did much better than the aerial-hawking and trawling
Myotis spp., which also had much smaller eyes.
The reaction to the 5° but not to the 2.5° pattern by the Myotis species used in
this study is consistent with an earlier investigation of another Myotis species,
the little brown bat (M. lucifugus), which responded down to 3-6° (Suthers
1966). A visual acuity in this range suggests that these bats can only detect 5-9
cm objects at a distance of 1 m, and hence it seems unlikely that they can use
vision to detect the insects that they eat. Prey items captured by any of these
species are much smaller than this and they are presumably detected using sonar
cues alone (Swift & Racey 1983, Kalko & Schnitzler 1989). However, vision
could well be used to detect large objects at distances beyond the range of
echolocation, i.e. objects important for orientation and navigation. Indeed, it has
been shown that loss of vision drastically reduces the homing performance by
other Myotis species, such as M. sodalis (Hassell 1963, 1966, Davis & Barbour
1970) and M. austroriparius (Layne 1967).
Nevertheless, Bradbury and Nottebohm (1969) showed that hearing impaired
M. lucifugus could avoid 2 mm wide strings in dim light, when the strings
contrasted sharply against the background. Considering their visual acuity, it is
unlikely that the bats could have seen the strings more than 5 cm away.
Nevertheless, the results from this and other studies (Mueller 1966, 1968)
suggest that vision may be important for normal flight behaviour in these bats,
although contrast sensitivity might perhaps be more important that visual acuity
in some cases.
84
The brown long-eared bat Plecotus auritus responded to patterns equivalent to
30’ of arc, which means that this species should be able to detect objects as small
as 0.9 cm at a distance of 1 m. Among the Vespertilionidae, only Antrozous
pallidus has been shown to have a better resolving power (15’; Bell & Fenton
1986). These results and the fact that P. auritus has larger eyes than most
Vespertilionids (Cranbrook 1963; Tab 1.) suggest that it should be possible for
long-eared bats to detect prey sized objects visually. It typically feeds on
relatively large insects including many moths and beetles (Swift & Racey 1983,
Rydell 1989). As P. auritus is a gleaner and sometimes takes insects from leaves
(Swift 1998), it faces potential problems with clutter and therefore use other
sensory cues in addition to sonar. In fact, passive listening plays a major role in
prey detection by P. auritus (Anderson & Racey 1991). These bats are
exceptionally sensitive to sounds around 15 kHz, which is close to the
frequencies emitted by insects moving in clutter (Coles et al. 1989). However,
the long-eared bats may also use visual information when searching for prey. In
a recent study on feeding behaviour, it was shown that P. auritus preferred to use
visual cues to sonar when possible, and that they could detect ca. 2 cm long
mealworms visually (Eklöf & Jones, in press).
Visual acuity has previously been tested in a number of species (Table 2),
both behaviourally by optomotor response tests (Suthers 1966, Bell & Fenton
1986), and theoretically by counting the number of retinal ganglion cells (Koay
et al. 1998, Heffner et al. 2001). Both methods give indications of the minimum
separable angles, i.e. the minimum distance between two points that an animal
need in order to be able to separate them. The acuity values estimated by
counting retinal ganglion cells tend to be higher than those estimated from
behavioural studies, suggesting that the anatomical method gives a theoretical
threshold, rather than what the bats actually respond to. Nevertheless, although
the acuity values obtained from the different methods are roughly in the same
order, comparisons across the two methods should be made with care.
As shown by the literature data presented in Table 2, frugivorous and
nectarivorous bats seem to have better spatial resolution than most insectivorous
species. Nevertheless, the finest spatial resolution in any bat (3’38’’) is found in
the gleaning insectivore Macrotus californicus (Phyllostomidae), and this
happens to be the only bat known to find prey, using vision alone (Bell 1985,
Bell & Fenton 1986). Indeed, gleaning insectivores may have better visual acuity
than aerial-insectivores in general, and this suggests that the aerial-hawking
insectivores rely mostly on echolocation rather than vision for detection of small
targets, while the opposite may be true in gleaners. At the same time it seems as
if, among aerial-hawking insectivores, Emballonuridae have better resolution
than Vespertilionidae.
The visual resolving power may depend on ambient light intensity. In the
common vampire bat Desmodus rotundus, for example, the acuity drops from
48’ at a light intensity of 31 mL (ca. 310 lux) to over 2° in 4*10-4 mL (ca. 0.004
lux) (Manske & Schmidt 1976). Other bats, such as Macrotus californicus and
Antrozous pallidus retain their visual acuity down to light levels as low as 2*10-4
mL (ca. 0.002 lux) (Bell & Fenton 1986). As a comparison, a light level of 0.1
lux is equivalent to light levels at full moon, and similar to the conditions in this
85
study. On overcast nights the amount of light drops to 0.0001 lux (Ryer1997).
Eptesicus fuscus responds optimally to brightness discrimination in ambient light
levels around 10 lux (conditions equivalent to dusk or dawn) but performs well
down to levels of 0.001 lux (Ellins & Masterson 1974). As the ambient
illumination increases towards daylight conditions the visual sensitivity
generally declines, although the light tolerance varies between species (Hope &
Bhatnagar 1979). Bradbury & Nottebohm (1969) found that Myotis lucifugus
avoids obstacles better under ambient illumination resembling dusk than in
daylight, which also indicates that the eyes of microchiropteran bats work better
in dim light than in bright light. Nevertheless, in a study on optomotor response
(Fenton et al. unpublished), several bats responded to striped patterns of 0.9° (the
narrowest available in the study) even in bright daylight. Ambient light levels
and the way it is measured, if reported at all, varies between different optomotor
response studies, which make the results somewhat hard to compare.
Acknowledgements
I wish to acknowledge Bengt Svensson for building the optomotor device, LarsErik Appelquist for making it possible to work at Taberg, Åsa Norén-Klingberg,
Jens Rydell, Stefan Pettersson and Karl-Johan Börjesson for help in the field and
comments on the manuscript.
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88
Fig. 1. – The device used for the optomotor response tests, 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 (or minutes)
of arc (illustrated by Olof Helje).
89
Tab. 1. – Eye diameter and optomotor responses to patterns of different fineness in four species of
insectivorous bats. The asterisks indicate that the 5o pattern was not tested and that the bat did not
respond to finer patterns.
Ambient
light (lux)
Eye diameter
(mm)
Minimum
separable angle
Species
Ind.
Plecotus auritus
1
2
3
4
5
6
7
8
0.6
0.6
0.6
0.1
0.1
0.7
0.2
0.3
1.6
1.8
not measured
1.7
1.7
not measured
not measured
not measured
45’
2.5°
1°
1°
45’
30’
45’
1°
Myotis mystacinus 1
2
3
0.6
0.6
0.1
1.0
0.9
not measured
no response*
no response*
5°
Myotis brandtii
1
2
0.1
0.1
not measured
not measured
5°
5°
Myotis daubentoni 1
2
3
0.1
0.1
0.3
1.2
1.3
not measured
5°
no response
5°
90
Tab. 2. – Visual acuity expressed as degrees of arc in Microchiroptera obtained from previous studies.
Behavioural acuity values come from optomotor responses, and theoretical values are calculated from the
number of retinal ganglion cells. Acuity is the minimum separable angle, i.e. the best values for each species.
Asterisks indicate that the ambient light level was not measured (or acuity was measured theoretically). For
consistency, the values of visual acuity were sometimes converted from other units, used in the original paper.
Visual
acuity
Author
3.6’
15’
Bell & Fenton 1986
Bell & Fenton 1986
b
b
b) Vespertilionidae; aerial-hawking and trawling insectivores
Eptesicus fuscus
*
1°
Eptesicus fuscus
40’-43’
Myotis lucifugus
*
3-6°
Nyctophilus gouldi
50’
Bell & Fenton 1986
Koay et al. 1998, Marks 1980
Suthers 1966
Pettigrew et al. 1988
b
t
b
t
c) Emballonuridae; aerial-hawking insectivores
Saccopteryx bilineata
Saccopteryx leptura
*
Taphozus georgianus
29’
42’
23’
Pettigrew et al. 1988
Suthers 1966
Pettigrew et al. 1988
t
b
t
d) Molossidae; aerial-hawking insectivores
Molossus ater
*
10°
Chase 1972
b
e) Rhinolophidae; flutter-detecting insectivores
Rhinolophus rouxi
1.4°
Pettigrew et al. 1988
t
f) Megadermatidae; gleaning insectivores/carnivores
Megaderma lyra
20’
Macroderma gigas
16’
Pettigrew et al. 1988
Pettigrew et al. 1988
t
t
g) Phyllostomatidae; frugivores and sanguivores
Carollia perspicillata
*
Anoura geoffroyi
*
Artibeus jamaicensis
Artibeus cinereus
Desmodus rotundus
*
Desmodus rotundus
3.1
Desmodus rotundus
0.04
16’
42’
27’
22’
42’
48’
2.5°
Suthers 1966
Suthers 1966
Heffner et al. 2000
Pettigrew et al. 1988
Suthers 1966
Manske & Schmidt 1976
Manske & Schmidt 1976
b
b
t
t
b
b
b
h) Other mammals
Rattus (rat)
Canis (dog)
Felis (cat)
Macaca (macaque)
Homo (man)
20’
3.6’
2.7’
38’’
32’’
Heffner & Heffner 1992
Heffner & Heffner 1992
Hughes 1977
Cowey & Ellis 1967
Hughes 1977
t
t
t
b
t
Species
Light
(lux)
a) Vespertilionidae; gleaning insectivores
Macrotus californicus
0.002
Antrozous pallidus
0.004
*
*
*
*
*
Method
(behav/theor)
91
V
“The bat that flits at close of Eve
Has left the brain that won't
believe.”
- William Blake
92
93
94
95
96
97
98
99
“I'm waiting for the night to fall
I know that it will save us all
When everything's dark
Keeps us from the stark reality”
VI
- Martin L Gore
100
101
102
103
104
105
106
107