Vision in echolocating bats - Fladdermus.net
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Vision in echolocating bats - Fladdermus.net
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<strong>Vision</strong> <strong>in</strong> echolocat<strong>in</strong>g <strong>bats</strong><br />
Johan Eklöf<br />
Dissertation<br />
Göteborg University<br />
Department of Zoology<br />
Box 463<br />
SE-405 30 Göteborg<br />
Sweden<br />
Avhandl<strong>in</strong>g för filosofie doktorsexamen i zoomorfologi, som enligt<br />
Naturvetenskapliga fakultetens beslut kommer att offentligen försvaras<br />
onsdagen den 28 maj 2003, kl 10:00 i föreläsn<strong>in</strong>gssalen, Zoologiska<br />
<strong>in</strong>stitutionen, Medic<strong>in</strong>aregatan 18, Göteborg. Fakultetsopponent är<br />
Professor Paul Racey, University of Aberdeen.<br />
0
Bat - Bats<br />
bat (b t) n. A b<strong>in</strong>ge; a spree<br />
n. A stout wooden stick; a cudgel<br />
n. Any of various nocturnal fly<strong>in</strong>g mammals of the order<br />
Chiroptera, hav<strong>in</strong>g membranous w<strong>in</strong>gs that extend from the<br />
forelimbs to the h<strong>in</strong>d limbs or tail and anatomical adaptations<br />
for echolocation, by which they navigate and hunt prey<br />
v. To hit<br />
v. To wander about aimlessly<br />
v. To discuss or consider at length<br />
<strong>bats</strong> adj. Crazy; <strong>in</strong>sane<br />
bat out To produce <strong>in</strong> a hurried or <strong>in</strong>formal manner<br />
off the bat Without hesitation; immediately<br />
go to bat for To give assistance to; defend<br />
not bat an eye To show no emotion; appear unaffected<br />
have <strong>bats</strong> <strong>in</strong><br />
(one's) belfry To behave <strong>in</strong> an eccentric, bizarre manner<br />
Göteborg University 2003 ISBN 91-628-5699-5<br />
1
A doctoral thesis at a university <strong>in</strong> Sweden is produced either<br />
as a monograph or as a collection of papers. In the latter<br />
case, the <strong>in</strong>troductory part constitutes the formal thesis,<br />
which summarises the accompany<strong>in</strong>g papers. They have<br />
already been published or are manuscripts at various stages<br />
(<strong>in</strong> press, submitted or <strong>in</strong> ms).<br />
Illustrations by Olof Helje<br />
2
Eklöf, J. <strong>Vision</strong> <strong>in</strong> echolocat<strong>in</strong>g <strong>bats</strong><br />
Zoology Department, Göteborg University<br />
Key words: acoustic clutter, forag<strong>in</strong>g tactics, Microchiroptera,<br />
perception, sensory ecology, ultrasound, visual acuity<br />
ABSTRACT<br />
The use of ultrasonic echolocation (sonar) <strong>in</strong> air is seriously constra<strong>in</strong>ed<br />
by the attenuation of high frequency sounds and unwanted echoes from<br />
the background (called clutter). Therefore, <strong>in</strong> many situations,<br />
echolocat<strong>in</strong>g <strong>bats</strong> have to rely on other sensory cues. The aim of this<br />
thesis is to <strong>in</strong>vestigate the use of vision by echolocat<strong>in</strong>g <strong>bats</strong>.<br />
Bat eyes are generally small, especially among aerial hawk<strong>in</strong>g<br />
<strong>in</strong>sectivores, with the exception of members of the family<br />
Emballonuridae. In glean<strong>in</strong>g, and <strong>in</strong> frugivorous species, however, the<br />
eyes tend to be larger and more prom<strong>in</strong>ent. The eyes of all <strong>bats</strong> are well<br />
adapted to low illum<strong>in</strong>ation, hav<strong>in</strong>g ma<strong>in</strong>ly rod-based ret<strong>in</strong>as, large<br />
corneal surfaces and lenses, and generally large receptor fields. Bats can<br />
easily detect small differences <strong>in</strong> brightness on clear nights, and the<br />
visual acuity rema<strong>in</strong>s relatively good <strong>in</strong> dim illum<strong>in</strong>ations. The visual<br />
resolv<strong>in</strong>g power (as obta<strong>in</strong>ed from counts of ret<strong>in</strong>al ganglion cells or by<br />
optomotor response tests) varies considerably among the different species<br />
of <strong>bats</strong>, from less than 0.06° of arc <strong>in</strong> Macrotus californicus<br />
(Phyllostomidae) to almost 5° <strong>in</strong> aerial hawk<strong>in</strong>g Myotis species<br />
(Vespertilionidae). Generally, the visual acuity is similar to that of rats<br />
and mice, suggest<strong>in</strong>g that cm-sized object can be discrim<strong>in</strong>ated at ranges<br />
less than a few metres. Studies on pattern discrim<strong>in</strong>ation have yielded<br />
highly variable results. Fruit and nectar eat<strong>in</strong>g species respond to patterns<br />
to a larger extent than aerial <strong>in</strong>sectivores.<br />
One of the most fundamental roles of the eyes is to register the amount of<br />
ambient light, <strong>in</strong> order to establish photoperiodic cycles. Some tropical<br />
<strong>bats</strong> avoid too bright conditions, i.e. moonlit nights probably due to<br />
<strong>in</strong>creased predation risk, a behaviour not found <strong>in</strong> high latitude species.<br />
As sonar only works well at short ranges, vision is<br />
primarily used for detection of landmarks and to avoid objects when<br />
mov<strong>in</strong>g over long distances, for example dur<strong>in</strong>g seasonal migration and<br />
when commut<strong>in</strong>g between feed<strong>in</strong>g sites. In these situations, there seems<br />
4
to be precedence of vision over sonar. At short range, with<strong>in</strong> that of<br />
echolocation, <strong>bats</strong> may defer to visual cues <strong>in</strong> addition to sonar and<br />
spatial memory to solve different tasks of orientation, especially when<br />
there is conflict<strong>in</strong>g <strong>in</strong>formation. Light conditions and time of the day may<br />
determ<strong>in</strong>e the behaviour of the <strong>bats</strong> and thus which sensory cues will be<br />
used.<br />
There is an <strong>in</strong>creas<strong>in</strong>g amount of data suggest<strong>in</strong>g that<br />
vision might be of importance <strong>in</strong> some situations and some aspects of<br />
forag<strong>in</strong>g, especially for frugivorous and nectarivorous <strong>bats</strong>, which can<br />
make use of differences <strong>in</strong> brightness and spectral composition, to f<strong>in</strong>d<br />
different food items. But even <strong>in</strong> species traditionally considered to rely<br />
heavily on echolocation, such as most <strong>in</strong>sectivorous <strong>bats</strong>, vision seems to<br />
play a more important role than has been recognised previously. The<br />
glean<strong>in</strong>g brown long-eared bat (Plecotus auritus, Vespertilionidae),<br />
known to forage mostly by us<strong>in</strong>g passive listen<strong>in</strong>g, detects prey more<br />
readily by us<strong>in</strong>g vision than by us<strong>in</strong>g sonar, and the aerial hawk<strong>in</strong>g<br />
northern bat (Eptesicus nilssonii, Vespertilionidae), use visual<br />
<strong>in</strong>formation <strong>in</strong> addition to sonar to f<strong>in</strong>d large stationary prey <strong>in</strong> clutter.<br />
Although echolocation is the key <strong>in</strong>novation that have made it possible<br />
for <strong>bats</strong> to fly at night, vision is reta<strong>in</strong>ed as an important complement; and<br />
<strong>in</strong>deed <strong>bats</strong> use an array of different sensory <strong>in</strong>puts to solve the different<br />
tasks of life.<br />
5
Eklöf, J. Syn hos ekolokaliserande fladdermöss<br />
Zoologiska <strong>in</strong>stitutionen, Göteborgs universitet<br />
SAMMANFATTNING<br />
Fladdermöss av underordn<strong>in</strong>gen Microchiroptera använder sig av<br />
ekolokalisation (sonar; SOund Navigation And Rang<strong>in</strong>g) för att orientera och<br />
för att f<strong>in</strong>na byten i mörker. Sonar ersätter således till viss del den<br />
funktion som synen har hos många andra djur. På grund av uttunn<strong>in</strong>gen<br />
av ljudvågor i luft och så kallat ”klotter” är dock räckvidden vanligen<br />
begränsad till ett fåtal meter. Fladdermöss måste därför använda sig av<br />
andra s<strong>in</strong>nes<strong>in</strong>tryck för att komplettera den ibland begränsade<br />
<strong>in</strong>formation som sonar ger. I denna avhandl<strong>in</strong>g belyser jag synens roll i<br />
fladdermössens liv.<br />
Fladdermössens ögon är vanligen små och kan verka obetydliga, men<br />
variationen är stor. Hos arter som plockar byten från underlag (gleaners)<br />
och bland fruktätare f<strong>in</strong>ner man de största ögonen. Alla fladdermusögon<br />
är dock anpassade för svagt ljus, med stora l<strong>in</strong>ser och breda receptorfält.<br />
Fladdermöss är relativt bra på att upptäcka små skillnader i belysn<strong>in</strong>g och<br />
deras synskärpa försämras <strong>in</strong>te nämnvärt i ljusförhållanden vi skulle<br />
uppfatta som totalt mörker. Synskärpa eller upplösn<strong>in</strong>gsförmåga varierar<br />
dock mycket mellan olika arter. Man kan mäta upplösn<strong>in</strong>gsförmåga<br />
ant<strong>in</strong>gen teoretiskt genom att räkna ganglieceller i ögat, eller genom<br />
beteendestudier, i vilka fladdermössen presenteras med roterande<br />
l<strong>in</strong>jemönster av olika storlek. Vissa av våra svenska Myotis-arter ser <strong>in</strong>te<br />
mycket bättre än att de kan separera objekt med 5° mellanrum, medan<br />
den amerikanska Macrotus californicus kan separera objekt med m<strong>in</strong>dre<br />
än 0.06°, vilket ungefär motsvarar upplösn<strong>in</strong>gsförmågan hos en hund.<br />
Huruvida fladdermöss kan skilja ut olika former och mönster med hjälp<br />
av synen verkar också variera betydligt mellan olika arter, men generellt<br />
verkar frukt- och nektarätare vara bättre på detta än s<strong>in</strong>a <strong>in</strong>sektsätande<br />
släkt<strong>in</strong>gar.<br />
En av de mest grundläggande av ögats funktioner är att registrera<br />
mängden ljus i omgivn<strong>in</strong>gen och på så vis kalibrera den <strong>in</strong>re klockan.<br />
Vissa tropiska fladdermöss undviker att flyga ut om natten är för ljus, till<br />
exempel då det är fullmåne, ett beteende vi <strong>in</strong>te f<strong>in</strong>ner i någon högre<br />
utsträckn<strong>in</strong>g bland fladdermössen på våra breddgrader.<br />
Eftersom sonar endast fungerar tillfredsställande på korta avstånd,<br />
används synen främst på längre håll, för att till exempel f<strong>in</strong>na landmärken<br />
6
och för att undvika h<strong>in</strong>der på väg till och från födoplatser, eller under<br />
migration. I sådana situationer verkar det som om syn<strong>in</strong>tryck är viktigare<br />
än <strong>in</strong>formation från sonar. Även <strong>in</strong>om räckvidden för sonar kan man<br />
ibland se att fladdermöss förlitar sig till synen, särskilt om sonar- och<br />
syn<strong>in</strong>tryck står i konflikt. Mängden ljus och tiden på dyg<strong>net</strong> kan också<br />
avgöra vilket av s<strong>in</strong>nena som har företräde.<br />
Frukt- och nektarätande fladdermöss har generellt sett<br />
bättre syn än <strong>in</strong>sektsätare och kan förmodas utnyttja synen i relativt stor<br />
utsträckn<strong>in</strong>g då de söker efter föda. Men även <strong>in</strong>sektsätare tar hjälp av<br />
syn<strong>in</strong>formation då det behövs. Långörad fladdermus Plecotus auritus<br />
plockar ofta stillasittande <strong>in</strong>sekter från blad och använder då framför allt<br />
s<strong>in</strong> känsliga hörsel för att lokalisera ljud som bytena själva åstadkommer.<br />
Den använder dock syn<strong>in</strong>tryck hellre än ekolokalisation som komplement<br />
till den passiva hörseln. Nordisk fladdermus Eptesicus nilssonii använder<br />
sig delvis av syn för att f<strong>in</strong>na stora stillastående byten bland växtlighet,<br />
byten som är svåra att urskilja med hjälp av sonar. Detta trots att de har<br />
en relativt begränsad visuell upplösn<strong>in</strong>gsförmåga, ca 1°, vilket är ungefär<br />
60 gånger sämre än en människas.<br />
Ekolokalisationen är utan tvekan det som gjort fladdermössen till en av<br />
de mest framgångsrika och mångskiftande däggdjursgrupperna på jorden.<br />
De har dock behållit ett funktionellt syns<strong>in</strong>ne som ett viktigt komplement.<br />
De, liksom vi använder sig av så många olika s<strong>in</strong>nes<strong>in</strong>tryck som möjligt<br />
för att lösa livets uppgifter.<br />
7
CONTENTS<br />
INTRODUCTION.……………………………………………………...10<br />
VISION IN ECHOLOCATING BATS<br />
The microchiropteran eye………………………………………….. 12<br />
The bra<strong>in</strong> and the ret<strong>in</strong>al pathways………………………………… 15<br />
What <strong>bats</strong> can see…………………………………………………... 17<br />
<strong>Vision</strong> <strong>in</strong> orientation and navigation……………………………….. 24<br />
<strong>Vision</strong> <strong>in</strong> forag<strong>in</strong>g and prey detection…………………………….... 27<br />
Predator surveillance and social behaviour……………………….... 33<br />
Multimodality – vision and echolocation………………...…….… . 34<br />
ACKNOWLEDGEMENTS....…………….……………………….…... 38<br />
REFERENCES…………………………….…………………………… 39<br />
PAPER I. Eklöf, J. & Jones, G. 2003.<br />
Use of vision <strong>in</strong> prey detection by brown long-eared<br />
<strong>bats</strong> Plecotus auritus. - Animal Behaviour (In Press)..… 48<br />
PAPER II. Eklöf, J., Svensson, A. M. & Rydell, J. 2002.<br />
Northern <strong>bats</strong> (Eptesicus nilssonii) use vision but not<br />
flutter-detection when search<strong>in</strong>g for prey <strong>in</strong> clutter.<br />
- Oikos 99, 347-351….…………………………………. 62<br />
PAPER III. Rydell, J. & Eklöf, J. 2003.<br />
<strong>Vision</strong> complements echolocation <strong>in</strong> the aerial<br />
hawk<strong>in</strong>g northern bat (Eptesicus nilssonii)<br />
- Submitted manuscript……………………………...…. 70<br />
PAPER IV. Eklöf, J. 2003.<br />
Visual acuity and eye size <strong>in</strong> <strong>in</strong>sectivorous <strong>bats</strong>.<br />
- Manuscript………………………...…………………... 80<br />
PAPER V. Eklöf, J., Tranefors, T. & Vázquez, L-B. 2002.<br />
Precedence of visual cues <strong>in</strong> the emballonurid bat<br />
Balantiopteryx plicata. - Mammalian Biology 67,<br />
42-46……………………………………………………. 92<br />
PAPER VI. Karlsson, B-L., Eklöf, J. & Rydell, J. 2002.<br />
No lunar phobia <strong>in</strong> swarm<strong>in</strong>g <strong>in</strong>sectivorous <strong>bats</strong><br />
(family Vespertilionidae). - Journal of Zoology<br />
London 256, 473-477….……………………………….100<br />
8
B ats (Order: Chiroptera) are among the most diverse and abundant<br />
mammals on earth and the thousand or so species comprise about one<br />
fourth of all mammalians. Bats occur throughout the world, except the<br />
Polar Regions, and show a remarkable wide range of habitat use,<br />
behaviour, morphology, and diet. Most <strong>bats</strong> feed on <strong>in</strong>sects but there are<br />
also <strong>bats</strong> that feed on fruit, nectar, fish, small vertebrates, and blood. Bats<br />
are the only mammals that have evolved active flight, and they can<br />
navigate through complete darkness by us<strong>in</strong>g echolocation or sonar<br />
(SOund Navigation And Rang<strong>in</strong>g). Bats live almost everywhere, <strong>in</strong> tropical<br />
jungles as well as <strong>in</strong> cities; they <strong>in</strong>habit caves, trees, houses, churches,<br />
bridges, coiled banana leafs, bamboo canes, and some species even build<br />
their own tents by us<strong>in</strong>g large leaves. Bats have a remarkable spatial<br />
memory and are quick learners. They can form colonies of up to 20<br />
million <strong>in</strong>dividuals, eat hundreds or thousands of <strong>in</strong>sects every night and<br />
migrate across cont<strong>in</strong>ents. Many <strong>bats</strong> hibernate through a cold w<strong>in</strong>ter and<br />
some can reach more than 40 years of age. Despite this, <strong>bats</strong> are seldom<br />
people’s number one choice of favourite animal. Instead, <strong>bats</strong> have<br />
become symbols of darkness, doom and occultism <strong>in</strong> the western world.<br />
They often appear <strong>in</strong> not so flatter<strong>in</strong>g contexts, such as <strong>in</strong> myths, scary<br />
movies, heavy metal lyrics, and are often one of the most important<br />
<strong>in</strong>gredients <strong>in</strong> witches’ brews. Be<strong>in</strong>g called an old bat is not a<br />
compliment, and hav<strong>in</strong>g a bat <strong>in</strong> one’s belfry is not very often socially<br />
accepted. In the eastern world, however, <strong>bats</strong> are considered as symbols<br />
of fortune and a long, prosperous life. Nevertheless, the <strong>bats</strong>’ leathery<br />
w<strong>in</strong>gs and their ability to navigate through the night are presumably two<br />
reasons beh<strong>in</strong>d their often somewhat scary reputation, as well as the two<br />
ma<strong>in</strong> reasons beh<strong>in</strong>d their success as a group. But how do they perceive<br />
the world; or as Thomas Nagel (1974) put it <strong>in</strong> his classic paper: what is it<br />
like to be a bat?<br />
All <strong>in</strong>formation about the surround<strong>in</strong>g world is filtered through our<br />
senses and processed <strong>in</strong> our bra<strong>in</strong>s <strong>in</strong> order to give us just the right k<strong>in</strong>d<br />
and amount of <strong>in</strong>formation to help us make proper decisions. This is true<br />
for all animals, although the senses receiv<strong>in</strong>g the <strong>in</strong>formation and the<br />
bra<strong>in</strong>s that process it differ across the animal k<strong>in</strong>gdom. The type and<br />
amount of <strong>in</strong>formation that is needed obviously varies considerably<br />
depend<strong>in</strong>g on life style. What humans cannot perceive tend to be called<br />
ultra-, <strong>in</strong>fra-, or extra-someth<strong>in</strong>g. We do not know what ultraviolet light<br />
looks like, only that it gives us a nice tan. We cannot hear <strong>in</strong>frasounds<br />
although elephants can, which is why we and not the elephants <strong>in</strong>vented<br />
10
the telephone. Many animals live entirely <strong>in</strong> the world of ultra-, or <strong>in</strong>fra-,<br />
mak<strong>in</strong>g it hard for us to relate to their every day life, or as Thomas<br />
Carlyle (1837) elegantly put it: “In every object there is <strong>in</strong>exhaustible<br />
mean<strong>in</strong>g; the eye sees <strong>in</strong> it what the eye br<strong>in</strong>gs means of see<strong>in</strong>g. To<br />
Newton and to Newton’s dog Diamond, what a different pair of<br />
universes.” Bat echolocation is different from any of the senses that we<br />
are familiar with, and therefore, we cannot know or even imag<strong>in</strong>e how<br />
they experience the world; or as <strong>in</strong> the words of Thomas Nagel (1974):<br />
“Anyone who has spent some time <strong>in</strong> an enclosed space with an excited<br />
bat knows what it is to encounter a fundamentally alien form of life.”<br />
With this <strong>in</strong> m<strong>in</strong>d, it may seem impossible to study sensory ecology, and<br />
still, we try. We accept that there is <strong>in</strong>formation outside our perception<br />
range, although we will never be able to fully understand those th<strong>in</strong>gs.<br />
We may perhaps be able to understand how a bat collects and uses<br />
<strong>in</strong>formation from the environment, but never what this really is like for<br />
the bat. We may however, from a human po<strong>in</strong>t of view, describe<br />
behaviour and reactions of animals under def<strong>in</strong>ed conditions. For<br />
example, when study<strong>in</strong>g <strong>bats</strong> fly<strong>in</strong>g, and record<strong>in</strong>g and describ<strong>in</strong>g<br />
echolocation calls, we can tell that sonar is a high precision tool, as good<br />
as vision for perceiv<strong>in</strong>g and identify<strong>in</strong>g objects, only entirely different.<br />
But we beg<strong>in</strong> to understand that echolocation alone is not enough to fully<br />
experience the world as a bat. As high frequency sounds attenuate rapidly<br />
<strong>in</strong> air, the effective range of echolocation is limited to a few metres <strong>in</strong><br />
practice. Background echoes, known as clutter, also impose severe<br />
constra<strong>in</strong>ts on the use of sonar, and for a bat to perceive distant objects or<br />
objects hidden <strong>in</strong> vegetation, other senses must be used. One of these<br />
senses is vision. However, look<strong>in</strong>g at a typical bat eye gives little hope of<br />
any breathtak<strong>in</strong>g visual adventures. The eyes are often small and<br />
<strong>in</strong>conspicuous, especially compared to the more fanciful ears and noseleafs<br />
of many <strong>bats</strong>, and consider<strong>in</strong>g our own sensory limits and the fact<br />
that <strong>bats</strong> fly at night, it is not hard to imag<strong>in</strong>e why an expression like “as<br />
bl<strong>in</strong>d as a bat” exists. But still, <strong>bats</strong> do have eyes and perhaps “as bl<strong>in</strong>d<br />
as we would be if we had bat eyes” would be a more suitable expression.<br />
As I will discuss <strong>in</strong> this thesis, <strong>bats</strong> do have eyes that function for <strong>bats</strong>. In<br />
the same way humans have a sense of smell that function for humans,<br />
although a dog, or a bat for that matter, probably would not be impressed!<br />
The aim of this <strong>in</strong>troductory chapter is to put my work <strong>in</strong>to perspective by<br />
summariz<strong>in</strong>g current knowledge of the role of vision <strong>in</strong> the lives of the<br />
echolocat<strong>in</strong>g <strong>bats</strong>.<br />
11
VISION IN ECHOLOCATING BATS<br />
The microchiropteran eye<br />
The eyes of Microchiroptera 1 rank among the smallest <strong>in</strong> mammals (Tab<br />
1), although there are considerable differences <strong>in</strong> both eye size and<br />
morphology across species, reflect<strong>in</strong>g a great ecological diversity (Chase<br />
1972; Hope & Bhatnagar 1979a; b; Marks 1980; Suthers & Bradford<br />
1980; Bell & Fenton 1986; Paper IV). In general, the eyes of frugivorous<br />
and nectarivorous Microchiroptera are larger than those of <strong>in</strong>sectivorous<br />
species. Bats roost<strong>in</strong>g <strong>in</strong> relatively exposed sites, and those that<br />
sometimes are active <strong>in</strong> dusk- and daylight conditions such as many<br />
members of the family Emballonuridae also have relatively large eyes.<br />
Hence eye size seems to reflect how much <strong>bats</strong> are exposed to light <strong>in</strong><br />
their daily life.<br />
Footnote 1. The Microchiroptera <strong>in</strong>cludes ca 800 species of echolocat<strong>in</strong>g <strong>bats</strong> but excludes<br />
the generally non-echolocat<strong>in</strong>g Megachiroptera or fly<strong>in</strong>g foxes, which are not considered<br />
<strong>in</strong> this thesis.<br />
Tab 1 - Eye size <strong>in</strong> Microchiroptera <strong>in</strong> relation to taxonomic aff<strong>in</strong>ity and general<br />
feed<strong>in</strong>g behaviour.<br />
Family & Eye ball axial Lens axial Lens radial Eye- Mean body-<br />
Species length (mm) diameter (mm) diameter (mm) weight (mg) weight (g)<br />
Vespertilionidae<br />
glean<strong>in</strong>g <strong>in</strong>sectivores<br />
Plecotus auritus --- --- 1.65 7 --- 7 6<br />
Myotis myotis 3.1 2 1.3 2 1.6 2 --- 26 6<br />
Vespertilionidae<br />
aerial-hawk<strong>in</strong>g <strong>in</strong>sectivores<br />
Eptesicus fuscus --- 0.77 9 0.91 9 6 4 14 4<br />
Myotis sodalis 1.68 1 0.6 1 0.94 1 --- 7.3 8<br />
Myotis lucifugus --- --- --- 4.4 4 10 4<br />
Nyctophilus gouldi 1.9 5 --- --- --- 10.5 11<br />
Myotis mystac<strong>in</strong>us --- --- 0.95 7 --- 5 6<br />
Myotis daubentonii --- --- 1.25 7 --- 10 10<br />
Nyctalus noctula 1.7 2 1.03 2 1.43 2 --- 27 6<br />
Emballonuridae<br />
aerial-hawk<strong>in</strong>g <strong>in</strong>sectivores<br />
Saccopteryx bil<strong>in</strong>eata 2.6 9 1.5 9 1.8 9 10.4 9 7 9<br />
Saccopteryx leptura --- 1.1 9 1.4 9 7.4 9 4 9<br />
Rhynconycteris naso --- --- --- 4.6 9 3 9<br />
12
Tab 1 - cont<br />
Eye ball axial Lens axial Lens radial Eye- mean body-<br />
Species length (mm) diameter (mm) diameter (mm) weight (mg) weight (g)<br />
Molossidae<br />
aerial-hawk<strong>in</strong>g <strong>in</strong>sectivores<br />
Molossus ater --- --- --- 3.44 9 26 9<br />
Eumops perotis 3.3 6 --- --- --- 48 6<br />
Natalidae<br />
aerial-hawk<strong>in</strong>g <strong>in</strong>sectivores<br />
Natalus tumidirostris 0.66 9 --- --- 0.6 9 6 9<br />
Rh<strong>in</strong>olophidae<br />
flutter-detect<strong>in</strong>g <strong>in</strong>sectivores<br />
Rh<strong>in</strong>olophus rouxi 1.8 5 --- --- --- ---<br />
Rh<strong>in</strong>olophus hipposideros --- 0.49 9 0.68 9 --- 7 12<br />
Megadermatidae<br />
glean<strong>in</strong>g <strong>in</strong>sectivores/carnivores<br />
Macroderma gigas 7.0 5 --- --- --- 120 6<br />
Phyllostomidae<br />
frugivores and nactarivores<br />
Carollia perspicillata 2.62 1 1.28 1 1.75 1 8.5 4 16 4<br />
Micronycteris megalotis 3.9 9 1.9 9 2.4 9 1.04 9 6 9<br />
Phyllostomus hastatus 3.94 1 1.95 1 2.44 1 40 3 77 3<br />
Glossophaga soric<strong>in</strong>a 2.0 9 --- --- 6.22 9 9 9<br />
Anoura geoffroyi --- --- --- 14 3 15 3<br />
Sturnira lilium --- 2.0 9 2.3 9 11.75 9 18 9<br />
Vampyrops helleri --- --- --- 24.2 9 12 9<br />
Chiroderma villosum --- 1.9 9 2.2 9 70.0 9 40 9<br />
Artibeus jamaicensis 4.0 6 --- --- 27.4 4 38 4<br />
Artibeus lituratus --- --- --- 30.4 9 61 9<br />
Phyllostomidae<br />
sanguivores<br />
Desmodus rotundus 2.5 7 --- --- 11 4 29 4<br />
Diaemus youngi --- --- --- 14.1 9 40 9<br />
Noctilionidae<br />
piscivores<br />
Noctilio lepor<strong>in</strong>us 2.1 6 --- --- --- 58 6<br />
Mormoopidae<br />
aerial-hawk<strong>in</strong>g <strong>in</strong>sectivores<br />
Mormoops megalophylla --- --- --- 1.8 9 16 9<br />
Pteronotus davyi --- 0.35 9 0.7 9<br />
1.16 9 7 9<br />
Pteronotus parnellii 0.9 9 0.42 9 0.7 9 0.90 9 18 9<br />
1 Suthers & Wallis 1970, 2 Suthers 1970, 3 Suthers & Bradford 1980, 4 Marks 1980,<br />
5 Pettigrew et al. 1988, 6 Baron et al. 1996a, 7 Paper IV, 8 Thomson 1982, 9 Chase 1972,<br />
10 Bogdanowicz 1994, 11 Grant 1991, 12 Greenway & Hutson 1990<br />
13
The microchiropteran eyes are shaped for nocturnal conditions <strong>in</strong> that<br />
they have large corneal surfaces and lenses relative to the size of the eye.<br />
They also have relatively large receptor fields, which give them good<br />
light gather<strong>in</strong>g power at the expense of acuity, i.e. the ability to resolve<br />
f<strong>in</strong>e spatial details (Suthers 1970; Suthers & Wallis 1970). The bat ret<strong>in</strong>a,<br />
which is relatively th<strong>in</strong> (91-126 µm) compared to that of voles (178 µm)<br />
and rats (198 µm), for example, consists ma<strong>in</strong>ly of rods, which are<br />
arranged loosely <strong>in</strong> visual streaks (Chase 1972; Marks 1980; Pettigrew et<br />
al. 1998). However, cones or at least cone like structures (receptor cells<br />
with pedicles) are present at least <strong>in</strong> the fruit-eat<strong>in</strong>g <strong>bats</strong> Artibeus<br />
lituratus and Phyllostomus hastatus (Phyllostomidae) and the aerial<br />
hawk<strong>in</strong>g <strong>in</strong>sectivorous Saccopteryx bil<strong>in</strong>eata, Saccopteryx leptura and<br />
Rhynconycteris naso (Emballonuridae) (Suthers 1970; Chase 1972).<br />
Suthers and Wallis (1970) studied the eyes of two species<br />
of Vespertilionidae (Myotis sodalis and Pipistrellus subflavus) and four<br />
species of Phyllostomidae (the vampire bat Desmodus rotundus, and the<br />
fruit-eat<strong>in</strong>g Carollia perspicillata, Anoura geoffroyi and Phyllostomus<br />
hastatus), and concluded that the visual capabilities of all the species<br />
tested would allow the <strong>bats</strong> to see well at ranges beyond that of<br />
echolocation. Due to the more or less spherical lenses (small species tend<br />
to have more asymmetric lenses; Chase 1972), it also follows that most<br />
Microchiroptera have a short focal distance and hence a great depth of<br />
focus (Suthers & Wallis 1970). In fact, microchiropteran <strong>bats</strong> seem to be<br />
farsighted, <strong>in</strong>dicat<strong>in</strong>g that vision is used predom<strong>in</strong>antly at long ranges,<br />
which is where echolocation does not work so well.<br />
The eye size and visual performance vary considerably between different species of Vespertilionidae.<br />
The northern bat Eptesicus nilssonii (left) has a visual acuity of ca 0.8° arc, the brown long eared-bat<br />
Plecotus auritus (middle), ca 0.5° arc, and Myotis spp. (right), 3 - 6° arc (Paper III, Paper IV).<br />
14
The bra<strong>in</strong> and the ret<strong>in</strong>al pathways<br />
The relative size of the <strong>in</strong>ternal bra<strong>in</strong> structures of <strong>bats</strong> differs between<br />
<strong>in</strong>sectivorous, sangivorous and carnivorous species on one hand and<br />
frugivorous and nectarivorous species on the other (Jolicoeur & Baron<br />
1980; Barton et al. 1995; Barton & Harvey 2000). Whereas <strong>in</strong>sect eat<strong>in</strong>g<br />
<strong>bats</strong> have enlarged echo-acoustic bra<strong>in</strong> structures, fruit eat<strong>in</strong>g species<br />
have relatively large olfactory- and visual bulbs, clearly reflect<strong>in</strong>g the<br />
different feed<strong>in</strong>g strategies <strong>in</strong> the various species.<br />
The size and lam<strong>in</strong>ation of the ma<strong>in</strong> targets of ret<strong>in</strong>al<br />
projections <strong>in</strong> the bra<strong>in</strong>: the superior colliculus (which transmits visual<br />
<strong>in</strong>formation and controls head- and eye movements) and the lateral<br />
geniculate body (a process<strong>in</strong>g station on the way from the ret<strong>in</strong>a to the<br />
visual centre, which e.g. serves to enhance contrasts) have been studied <strong>in</strong><br />
Artibeus, Eptesicus (Cotter 1985), Myotis (Cotter & Pentney 1979;<br />
Crowle 1980) and Pteronotus (Covey et al. 1987). Megadermatids and<br />
fruit eat<strong>in</strong>g phyllostomids show the thickest and most developed layers <strong>in</strong><br />
the superior colliculus, at least <strong>in</strong> the superficial ones, which receive<br />
exclusively visual <strong>in</strong>put. Also glean<strong>in</strong>g species tend to have relatively<br />
large superior colliculi. Open-air <strong>in</strong>sectivorous species on the other hand,<br />
seem to have superior colliculi consist<strong>in</strong>g almost entirely of the deeper<br />
layers, which receive a variety of different sensory <strong>in</strong>puts (<strong>in</strong>clud<strong>in</strong>g<br />
visual stimuli). However, some <strong>in</strong>sectivorous <strong>bats</strong>, like the<br />
Emballonuridae (especially Saccopteryx and Cyttarops) have relatively<br />
large superior colliculi and resemble frugivores <strong>in</strong> this respect, although<br />
their total bra<strong>in</strong> volume is smaller than <strong>in</strong> most other microchiropteran<br />
families (Baron et al. 1996b). This may perhaps reflect the fact that most<br />
emballonurid species roost <strong>in</strong> exposed sites and therefore live <strong>in</strong> bright<br />
light conditions. However, consider<strong>in</strong>g that the Emballonuridae form a<br />
basal clade <strong>in</strong> the phyloge<strong>net</strong>ic tree, it may just as well suggest that bat<br />
ancestors had a well-developed visual system. (Simmons & Geisler<br />
1998). The projections to the superior colliculus are similar to those of<br />
most mammals, <strong>in</strong> that they have no b<strong>in</strong>ocular overlap, and thus the left<br />
superior colliculus receives <strong>in</strong>put only from the right eye and vice versa<br />
(Pettigrew 1986; Neuweiler 2000). In Megachiroptera and <strong>in</strong> primates,<br />
both superior colliculi receive <strong>in</strong>put from both eyes, and hence these<br />
animals have better stereoscopic vision than Microchiroptera.<br />
(Interest<strong>in</strong>gly the microchiropteran family Rh<strong>in</strong>olophidae, which conta<strong>in</strong><br />
highly specialized echolocators, show similarities to Megachiroptera <strong>in</strong><br />
this respect (Reimer 1989). This may reflect phyloge<strong>net</strong>ic relationship<br />
rather than visual adaptation, however (e.g. Spr<strong>in</strong>ger et al. 2001)).<br />
The lateral geniculate body consists of two parts, the<br />
ventral lateral geniculate, which has connections with several other bra<strong>in</strong><br />
15
structures, and the dorsal lateral geniculate, which connects to the visual<br />
cortex. In most Microchiroptera, a larger proportion of the nerves are<br />
projected to the ventral side of the lateral geniculate body, suggest<strong>in</strong>g that<br />
vision is important for orientation rather than for cognitive tasks<br />
(Neuweiler 2000). However, the sizes of the ret<strong>in</strong>al pathways vary<br />
between genera. The nerves are generally larger <strong>in</strong> frugivores<br />
(Phyllostomus hastatus, Anoura geoffroyi, Suthers & Bradford 1980; and<br />
Artibeus jamaicensis, Cotter 1985) than <strong>in</strong> <strong>in</strong>sectivores (Eptesicus fuscus,<br />
Cotter 1985; and Pteronotus parnellii, Covey et al. 1987), although,<br />
aga<strong>in</strong>, <strong>in</strong>sectivorous Emballonuridae and Megadermatidae are exceptions.<br />
Both have relatively large visual pathways project<strong>in</strong>g through the dorsal<br />
lateral geniculate to the visual cortex. This suggests that vision is more<br />
important <strong>in</strong> these species, and they show similarities to the visually<br />
oriented Megachiroptera <strong>in</strong> this respect (Neuweiler 2000), and may<br />
reflect phyloge<strong>net</strong>ic relationship (Spr<strong>in</strong>ger et al. 2001). For a comparison<br />
of different bra<strong>in</strong> structures between all groups of Microchiroptera, see<br />
Baron et al. (1996a; b; c).<br />
Three examples of large-eyed <strong>bats</strong>: Species of the family Emballonuridae (left) have larger eyes than other<br />
<strong>in</strong>sectivorous aerial-hawkers, probably reflect<strong>in</strong>g an unusual visual capacity among <strong>bats</strong>. The large eyed<br />
Megaderma lyra (Megadermatidae) (middle) show a flexible hunt<strong>in</strong>g strategy and uses vision <strong>in</strong> comb<strong>in</strong>ation<br />
with sonar and passive hear<strong>in</strong>g. Macrotus californicus (Phyllostomidae) (right) is the only microchiropteran<br />
bat shown to be capable of catch<strong>in</strong>g <strong>in</strong>sects us<strong>in</strong>g vision alone.<br />
16
What <strong>bats</strong> can see<br />
Brightness discrim<strong>in</strong>ation and light sensitivity<br />
At the most basic level, vision is <strong>in</strong>volved <strong>in</strong> the establishment of<br />
photoperiodic cycles, and serves to dist<strong>in</strong>guish daylight from darkness. It<br />
was previously believed that this was the sole purpose of the<br />
microchiropteran eye (Eisentraut 1969 cited <strong>in</strong> Dietrich & Dodt 1970).<br />
The bat’s activity cycle is controlled by an endogenous circadian rhythm,<br />
which is synchronized with the daylight cycle by light sampl<strong>in</strong>g<br />
behaviour. This means that, before they emerge from the roost to feed,<br />
the <strong>bats</strong> move from the darker areas <strong>in</strong> their roosts to lighter areas near<br />
the entrance, <strong>in</strong> order to test the outdoor light level (Erkert 1982).<br />
Cloud<strong>in</strong>ess and moonlight can thus affect the time of emergence. On<br />
moonlit nights, many tropical microchiropterans typically reduce their<br />
forag<strong>in</strong>g activity, presumably due to <strong>in</strong>creased predation risk (Morrison<br />
1978; Usman et al. 1980; Flem<strong>in</strong>g 1988) or perhaps lower availability of<br />
food (Lang et al. 2002). In contrast, bat activity at high latitudes is not<br />
<strong>in</strong>fluenced by moonlight to any high extent (Paper VI). On twelve nights<br />
<strong>in</strong> August-September 2000, the impact of moonlight on bat swarm<strong>in</strong>g<br />
activity (associated with mat<strong>in</strong>g season) was studied at an abandoned<br />
m<strong>in</strong>e <strong>in</strong> southern Sweden. Bat activity at and near the m<strong>in</strong>e entrance did<br />
not vary with moon phase, or cloud cover, suggest<strong>in</strong>g that moonlight had<br />
no effect on the <strong>bats</strong>’ behaviour. It seems likely that <strong>in</strong>sectivorous <strong>bats</strong> at<br />
high latitudes may not have been exposed to significant nocturnal<br />
predator pressure, lead<strong>in</strong>g to the evolution of lunar phobia, as many<br />
tropical <strong>bats</strong>. In contrast to high-latitude <strong>bats</strong>, the latter have to face<br />
specialized bat predators such as bat falcons (Falco rufigularis).<br />
Furthermore, high latitude <strong>bats</strong> are exposed to relatively bright light<br />
conditions throughout the summer. They do react to light, but not by<br />
decreas<strong>in</strong>g their activity, <strong>in</strong>stead, they fly closer to protective vegetation<br />
or sometimes high <strong>in</strong> the air (Rydell et al. 2002). This k<strong>in</strong>d of behaviour<br />
is also seen <strong>in</strong> species that migrate dur<strong>in</strong>g the day, such as the noctule,<br />
Nyctalus noctula (Ahlén 1997). Both types of behaviour may have the<br />
purpose of avoid<strong>in</strong>g predatory birds (e.g. small hawks and falcons).<br />
The ability of <strong>bats</strong> to detect small differences <strong>in</strong><br />
brightness, i.e. brightness discrim<strong>in</strong>ation, was first studied by Eisentraut<br />
(1950), who found that Plecotus auritus and Eptesicus serot<strong>in</strong>us<br />
(Vespertilionidae) could easily dist<strong>in</strong>guish black cards from white. Curtis<br />
(1952) tra<strong>in</strong>ed the vespertilionids Eptesicus fuscus and Myotis lucifugus<br />
to search for food at the illum<strong>in</strong>ated end of a box, and found that the <strong>bats</strong>’<br />
ability of brightness discrim<strong>in</strong>ation is similar to that of rats and mice.<br />
Brightness discrim<strong>in</strong>ation performance <strong>in</strong> Eptesicus fuscus peaks around<br />
17
10 lux, which is equivalent to the light level prevail<strong>in</strong>g at dusk and dawn,<br />
but rema<strong>in</strong>s good <strong>in</strong> illum<strong>in</strong>ations as low as 0.001 lux, conditions which<br />
resembles darkness to a human eye adapted to low light <strong>in</strong>tensity. As a<br />
comparison, a light level of 0.1 lux is equivalent to light levels at full<br />
moon, and on overcast nights the amount of light drops to 0.0001 lux<br />
(Ryer 1997). Based on focal distance and diameter of the dilated pupil,<br />
Dietrich and Dodt (1970) calculated that the light gather<strong>in</strong>g power of<br />
Myotis myotis is 4-5 times that of man. This suggests that <strong>bats</strong> can readily<br />
use visual cues at dusk, when they normally emerge from their roosts,<br />
and probably also under nocturnal conditions (Ell<strong>in</strong>s & Masterson 1974).<br />
Many tropical <strong>bats</strong><br />
m<strong>in</strong>imize their activity<br />
<strong>in</strong> moonlight,<br />
presumably due to<br />
predation risk. This<br />
behaviour is not found<br />
among high latitude<br />
<strong>bats</strong> (Paper VI)<br />
As may be expected from a ret<strong>in</strong>a consist<strong>in</strong>g predom<strong>in</strong>antly of rods, the<br />
visual sensitivity generally decl<strong>in</strong>es as the ambient illum<strong>in</strong>ation <strong>in</strong>creases<br />
towards daylight (Hope & Bhatnagar 1979b). This <strong>in</strong>dicates that the bat<br />
eyes work better <strong>in</strong> dim light than <strong>in</strong> bright light. This has been verified<br />
behaviourally by Bradbury & Nottebohm (1969), who found that Myotis<br />
lucifugus avoids obstacles better under ambient illum<strong>in</strong>ations resembl<strong>in</strong>g<br />
dusk, than they do <strong>in</strong> bright daylight. These f<strong>in</strong>d<strong>in</strong>gs may expla<strong>in</strong> why<br />
early studies, which were made <strong>in</strong> room illum<strong>in</strong>ation, usually failed to<br />
prove any major visual capacity <strong>in</strong> microchiropteran <strong>bats</strong> (e.g. Eisentraut<br />
1950; Curtis 1952).<br />
Light tolerance has been estimated <strong>in</strong> three species of<br />
Vespertilionidae (Myotis myotis, Dietrich & Dodt 1970; Eptesicus<br />
serot<strong>in</strong>us, Bornsche<strong>in</strong> 1961; and Eptesicus fuscus, Hope & Bhatnagar<br />
18
1979b) and three species of Phyllostomidae (Desmodus rotundus,<br />
Carollia perspicillata, and Artibeus jamaicensis, Hope & Bhatnagar<br />
1979b) by measur<strong>in</strong>g the lum<strong>in</strong>ance of light stimuli required to provoke<br />
electroret<strong>in</strong>ogram responses. Among the vespertilionids, Eptesicus fuscus<br />
showed the highest light tolerance, and among the phyllostomids, which<br />
generally responded to lower lum<strong>in</strong>ance levels than the vespertilionids,<br />
Artibeus jamaicensis showed the highest tolerance. This presumably<br />
reflects the relative importance of vision <strong>in</strong> the different species, but<br />
perhaps more importantly the time at which these species normally<br />
emerge <strong>in</strong> the even<strong>in</strong>g, and to what extent they are exposed to bright light<br />
(Hope & Bhatnagar 1979a; b). The Emballonuridae Emballonura spp.<br />
and Saccopteryx spp., some of which roost at exposed sites and often fly<br />
<strong>in</strong> daylight (Lekagul & McNeely 1977; Bradbury & Vehrencamp 1976;<br />
Kalko 1995), would thus be expected to be more light tolerant than other<br />
<strong>bats</strong>. Although, light tolerance levels have not been measured <strong>in</strong> these<br />
<strong>bats</strong> directly, the small receptive fields and the low receptor-to-ganglion<br />
ratio (ca 1:10) <strong>in</strong> Saccopteryx spp., compared to that of other<br />
microchiropteran species (ca 1:100), <strong>in</strong>dicate a high light tolerance and<br />
good resolv<strong>in</strong>g power as expected. In fact they resemble diurnal<br />
mammals <strong>in</strong> this respect (Chase 1972). Nevertheless, the eyes of<br />
Microchiroptera work well under low ambient illum<strong>in</strong>ation, although the<br />
sensitivity to different light levels and the ability of brightness<br />
discrim<strong>in</strong>ation vary considerably between the different families and<br />
species.<br />
Spatial resolution<br />
The eyes of microchiropterans are primarily adapted to function <strong>in</strong> low<br />
light levels. This carries the disadvantage of a relative poor ability to<br />
resolve f<strong>in</strong>e spatial details (acuity). The ability of spatial resolution of the<br />
bat eye can be estimated either anatomically, by calculat<strong>in</strong>g the density of<br />
ret<strong>in</strong>al ganglion cells (Marks 1980; Pettigrew et al. 1998; Heffner et al.<br />
2001) or behaviourally, by present<strong>in</strong>g the <strong>bats</strong> with striped patterns of<br />
different f<strong>in</strong>eness (Suthers 1966; Bell & Fenton 1986; Paper IV). When<br />
the visual acuity is measured with the latter method, it is often referred to<br />
as grat<strong>in</strong>g acuity and is expressed as degrees of arc or as cycles per<br />
degree, where one cycle is one pair of black and white stripes. The two<br />
methods give <strong>in</strong>dications of the m<strong>in</strong>imum separable angles, i.e. the<br />
m<strong>in</strong>imum distance between two po<strong>in</strong>ts that an animal needs <strong>in</strong> order to<br />
separate them.<br />
19
The device used for the optomotor response tests (Paper IV), <strong>in</strong> which a bat is presented with<br />
rotat<strong>in</strong>g, striped patterns of different f<strong>in</strong>eness. The bat responds to the revolv<strong>in</strong>g patterns by<br />
mov<strong>in</strong>g its head <strong>in</strong> a stereotype manner. The thickness of the stripes corresponds to the <strong>bats</strong><br />
visual resolv<strong>in</strong>g power (acuity), measured as degrees of arc.<br />
Comparisons between the two methods should be treated carefully<br />
because the acuity values estimated by count<strong>in</strong>g ret<strong>in</strong>al ganglion cells<br />
tend to be higher than those estimated from behavioural studies. This<br />
suggests that the anatomical method gives a theoretical m<strong>in</strong>imum, rather<br />
than an <strong>in</strong>dication of what the <strong>bats</strong> actually respond to. Nevertheless,<br />
Table 2 should give an idea of the wide range of spatial resolution ability<br />
that has been documented <strong>in</strong> different species of microchiropteran <strong>bats</strong>,<br />
from the coarse vision of the small Myotis spp. (Vespertilionidae) (3-5º<br />
arc, Paper IV) to the relatively f<strong>in</strong>e visual ability of Macrotus<br />
californicus (Phyllostomidae) (0.06° arc, Bell & Fenton 1986). Macrotus<br />
californicus has by far the best resolv<strong>in</strong>g power found <strong>in</strong> any<br />
microchiropteran bat studied so far, and is comparable to that of a dog <strong>in</strong><br />
this respect (Heffner & Heffner 1992). It is also the only<br />
microchiropteran known to be capable of detect<strong>in</strong>g <strong>in</strong>sects, us<strong>in</strong>g vision<br />
alone (Bell 1985).<br />
20
The visual resolv<strong>in</strong>g power is never a fixed value, but depends on the<br />
ambient light <strong>in</strong>tensity. In the common vampire bat Desmodus rotundus,<br />
for example, the acuity drops from 0.8° arc at a light <strong>in</strong>tensity of ca 310<br />
lux to over 2° arc <strong>in</strong> ca 0.004 lux (Manske & Schmidt 1976). Other <strong>bats</strong>,<br />
such as Macrotus californicus (0.06° arc) and Antrozous pallidus (0.25°<br />
arc) reta<strong>in</strong> their visual acuity down to light levels as low as ca 0.002 lux<br />
(Bell & Fenton 1986). In comparison, species of Megachiroptera, which<br />
do not echolocate, has been shown to respond to striped patterns of 0.8°<br />
<strong>in</strong> light levels of ca 0.0005 lux, whereas humans responds only to patterns<br />
of 1.3° arc under the same conditions (Neuweiler 1967). Hence, <strong>in</strong> very<br />
dim light, <strong>bats</strong> can see better than humans.<br />
Tab 2 - Visual acuity <strong>in</strong> Microchiroptera (expressed as degrees of arc). Behavioural acuity<br />
values (b) come from optomotor response tests, and theoretical values (t) are calculated from the<br />
number of ganglion cells per unit area of the ret<strong>in</strong>a. Acuity is the m<strong>in</strong>imum separable angle, i.e.<br />
the best values obta<strong>in</strong>ed for each species. Asterisks (*) <strong>in</strong>dicate that the ambient light level was<br />
not measured (or that acuity was measured theoretically). For consistency, the values of visual<br />
acuity and light levels were sometimes converted from other units, used <strong>in</strong> the orig<strong>in</strong>al paper.<br />
Light Visual<br />
Species (lux) acuity Reference Method<br />
Vespertilionidae;<br />
glean<strong>in</strong>g <strong>in</strong>sectivores<br />
Antrozous pallidus 0.004 0.25° Bell & Fenton 1986 b<br />
Plecotus auritus 0.7 0.5° Paper IV b<br />
Vespertilionidae;<br />
aerial-hawk<strong>in</strong>g <strong>in</strong>sectivores<br />
Eptesicus fuscus * 1° Bell & Fenton 1986 b<br />
Eptesicus fuscus * 0.7° Koay et al. 1998 t<br />
Eptesicus nilssonii 1-10 0.8° Paper III -<br />
Eptesicus capensis 3600-4800 0.9° Fenton & Portfors unpubl b<br />
Eptesicus zuluensis 4400 0.9° Fenton & Portfors unpubl b<br />
Myotis lucifugus * 3-6° Suthers 1966 b<br />
Nyctophilus gouldi * 0.8° Pettigrew et al. 1988 t<br />
Myotis brandtii 0.1 5° Paper IV b<br />
Myotis mystac<strong>in</strong>us 0.1 5° Paper IV b<br />
Myotis daubentonii 0.1-0.3 5° Paper IV b<br />
M<strong>in</strong>iopterus screibersii 33 0.9° Fenton & Portfors unpubl b<br />
Pipistrellus nanus 6400 0.9° Fenton & Portfors unpubl b<br />
Pipistrellus rueppellii 3200 0.9° Fenton & Portfors unpubl b<br />
Scotophilus borbonicus 40-5500 0.9° Fenton & Portfors unpubl b<br />
Nycticeius schlieffeni 5000 1.5° Fenton & Portfors unpubl b<br />
Emballonuridae<br />
aerial-hawk<strong>in</strong>g <strong>in</strong>sectivores<br />
Saccopteryx bil<strong>in</strong>eata * 0.5° Pettigrew et al. 1988 t<br />
Saccopteryx leptura * 0.7° Suthers 1966 b<br />
Taphozus georgianus * 0.4° Pettigrew et al. 1988 t<br />
21
Tab 2 – cont<br />
Light Visual<br />
Species (lux) acuity Reference Method<br />
Molossidae;<br />
aerial-hawk<strong>in</strong>g <strong>in</strong>sectivores<br />
Molossus ater * 10° Chase 1972 b<br />
Tadarida pumila 81-5800 0.9° Fenton & Portfors unpubl b<br />
Tadarida midas 20000 0.9° Fenton & Portfors unpubl b<br />
Rh<strong>in</strong>olophidae<br />
flutter-detect<strong>in</strong>g <strong>in</strong>sectivores<br />
Rh<strong>in</strong>olophus rouxi * 1.4° Pettigrew et al. 1988 t<br />
Rh<strong>in</strong>olophus fumigatus 160-4800 0.9° Fenton & Portfors unpubl b<br />
Megadermatidae<br />
glean<strong>in</strong>g <strong>in</strong>sectivores/carnivores<br />
Megaderma lyra * 0.3° Pettigrew et al. 1988 t<br />
Macroderma gigas * 0.3° Pettigrew et al. 1988 t<br />
Phyllostomidae<br />
frugivores and nectarivores<br />
Carollia perspicillata * 0.3° Suthers 1966 b<br />
Glossophaga soric<strong>in</strong>a * 3° Chase 1972 b<br />
Anoura geoffroyi * 0.7° Suthers 1966 b<br />
Sturnira lilium * 0.3° Chase 1972 b<br />
Artibeus jamaicensis * 0.5° Heffner et al. 2001 t<br />
Artibeus c<strong>in</strong>ereus * 0.4° Pettigrew et al. 1988 t<br />
Phyllostomidae<br />
sanguivores<br />
Desmodus rotundus * 0.7° Suthers 1966 b<br />
Desmodus rotundus 3.1 0.8° Manske & Schmidt 1976 b<br />
Desmodus rotundus 0.04 2.5° Manske & Schmidt 1976 b<br />
Diaemus youngi * 3° Chase 1972 b<br />
Phyllostomidae<br />
Glean<strong>in</strong>g <strong>in</strong>sectivores<br />
Macrotus californicus 0.002 0.06° Bell & Fenton 1986 b<br />
Other mammals;<br />
Rattus (rat) * 0.3° Heffner & Heffner 1992 t<br />
Canis (dog) * 0.06° Heffner & Heffner 1992 t<br />
Felis (cat) * 0.045° Hughes 1977 t<br />
Macaca (macaque) * 0.01° Cowey & Ellis 1967 b<br />
Homo (man) * 0.009° Hughes 1977 t<br />
Homo (man) 0.0005 1.3° Neuweiler 1967 b<br />
22
Pattern discrim<strong>in</strong>ation<br />
Bats can visually dist<strong>in</strong>guish patterns and shapes of objects. The<br />
nectarivorous Anoura geoffroyi (Phyllostomidae) dist<strong>in</strong>guishes rectangles<br />
from solid discs of the same surface area, when tra<strong>in</strong>ed to seek food at the<br />
discs (Suthers & Chase 1966; Suthers et al. 1969). This species is also<br />
able to dist<strong>in</strong>guish outl<strong>in</strong>es of erected triangles from <strong>in</strong>verted ones, as<br />
long as the basel<strong>in</strong>es of the triangles are <strong>in</strong>tact. However, when the <strong>bats</strong><br />
were presented with two sides of a triangle, i.e. an outl<strong>in</strong>e of a triangle<br />
without a base, the shape was no longer dist<strong>in</strong>guished from other shapes.<br />
This <strong>in</strong>dicates that Anoura geoffroyi does not possess a concept of form,<br />
but rather perceive the relative position of horizontal l<strong>in</strong>es. Similar<br />
conclusions were drawn from studies of common vampire <strong>bats</strong> Desmodus<br />
rotundus (Phyllostomidae). This species is able to separate vertical stripes<br />
but not horizontal stripes from circles of the same area (Schmidt &<br />
Manske 1978; Manske & Schmidt 1979). In contrast, the <strong>in</strong>sectivorous<br />
species Vespertilio superans (Vespertilionidae) cannot dist<strong>in</strong>guish objects<br />
of different shapes but equal size, and responds only to the size of the<br />
surface areas (Chung et al. 1990). The only bat that has been shown<br />
unambiguously to respond to shapes alone is the frugivorous<br />
phyllostomid Carollia perspicillata. This species can discrim<strong>in</strong>ate<br />
squares from circles, even if the squares are rotated (Suthers et al. 1969).<br />
In conclusion, studies on pattern discrim<strong>in</strong>ation have<br />
yielded highly variable results, but <strong>in</strong> general it seems as if fruit- and<br />
nectar-eat<strong>in</strong>g microchiropterans respond to patterns and shapes more<br />
readily than <strong>in</strong>sectivorous species. This may perhaps reflect that plants<br />
are more easily detected by vision, and less detectable by sonar than<br />
<strong>in</strong>sects, and that frugivores therefore may use a different search image<br />
when forag<strong>in</strong>g.<br />
Perception of colour<br />
Given that microchiropteran <strong>bats</strong> are all more or less nocturnal, true<br />
colour vision seems unlikely to occur <strong>in</strong> these animals, as it would<br />
probably be of m<strong>in</strong>or importance. Nevertheless, cones occur <strong>in</strong> the ret<strong>in</strong>as<br />
of some species, although most authors report only rods (reviewed by<br />
Suthers 1970; Chase 1972). Nevertheless, there is evidence that at least<br />
two different photo pigments occur <strong>in</strong> the eyes of Microchiroptera (Chase<br />
1972; Hope & Bhatnagar 1979a). Electroret<strong>in</strong>ogram response tests have<br />
shown sensitivity peaks around 500 nm and 570 nm <strong>in</strong> the vespertilionid<br />
species Myotis myotis (Dietrich & Dodt 1970) and Eptesicus fuscus<br />
(Hope & Bhatnagar 1979a) and the phyllostomid species Artibeus<br />
23
jamaicensis, Desmodus rotundus and Carollia perspicillata (Hope &<br />
Bhatnagar 1979a). There is also prelim<strong>in</strong>ary evidence that there is a<br />
spectral sensitivity peak <strong>in</strong> the near UV-range (around 390 nm) <strong>in</strong> the<br />
nectarivorous phyllostomid Glossophaga soric<strong>in</strong>a (Lopez et al. 2001). It<br />
is thus possible that this species is able to perceive ultraviolet light<br />
reflected from fruits and plants.<br />
<strong>Vision</strong> <strong>in</strong> orientation and navigation<br />
Long distance navigation<br />
The fact that the eyes of most <strong>bats</strong> function better beyond than with<strong>in</strong> the<br />
range of echolocation (Suthers & Wallis 1970) suggests that visual cues<br />
may preferably be used <strong>in</strong> preference to echolocation for navigation and<br />
orientation over longer distances.<br />
Several species of Microchiroptera make long distance<br />
movements and some even perform seasonal migration (Griff<strong>in</strong> 1970). It<br />
seems unlikely that ultrasonic echolocation plays any major role <strong>in</strong><br />
orientation over long distances, as it works only at short range. For<br />
example, <strong>in</strong>sect sized targets can be detected a few metres away at best<br />
(Kick 1982), although trees, hillsides or the ground obviously may be<br />
detected much further away. However, even dur<strong>in</strong>g the most favourable<br />
conditions, <strong>bats</strong> do not pay attention to echoes return<strong>in</strong>g from more than<br />
100 m or so away (Altr<strong>in</strong>gham 1996) and therefore, migration over long<br />
distances is almost certa<strong>in</strong>ly guided by other senses, <strong>in</strong>clud<strong>in</strong>g vision<br />
(Griff<strong>in</strong> 1970). Bats can use distant low frequency sounds for orientation<br />
over moderate distances, <strong>in</strong>dicat<strong>in</strong>g that passive hear<strong>in</strong>g may also be<br />
<strong>in</strong>volved <strong>in</strong> navigation over longer distances (Griff<strong>in</strong> 1970; Buchler &<br />
Childs 1981). There is also some evidence that <strong>bats</strong> possess mag<strong>net</strong>ic<br />
material (Buchler & Wasilewski 1985), but if they possess a mag<strong>net</strong>ic<br />
sense like birds (Wiltschko & Wiltschko 1995) or not, is still unknown.<br />
When migrat<strong>in</strong>g at night, it is possible that stars can serve<br />
as navigational cues for some species of <strong>bats</strong>. For example, Eptesicus<br />
fuscus can see po<strong>in</strong>t light sources, which simulate bright white and blue<br />
stars aga<strong>in</strong>st the night sky, if these are located at > 6 ° angle (Childs &<br />
Buchler 1981). This species is also able to orient and navigate <strong>in</strong> relation<br />
to the post-sunset glow <strong>in</strong> the west (Buchler & Childs 1982).<br />
In hom<strong>in</strong>g experiments with <strong>bats</strong> released with<strong>in</strong> 10 km<br />
from their roost, the <strong>bats</strong> have been demonstrated to do well, us<strong>in</strong>g<br />
echolocation alone. This suggests that they are acoustically familiar with<br />
a relatively large home territory (Williams et al. 1966; Williams &<br />
Williams 1967; Davis & Barbour 1970). Nevertheless, bl<strong>in</strong>ded <strong>bats</strong> tend<br />
24
to fly slower and closer to the ground than non-treated <strong>bats</strong> (Mueller<br />
1968), <strong>in</strong>dicat<strong>in</strong>g that they change their orientation behaviour when they<br />
no longer are able to see. Bats also seem to rely heavily on their spatial<br />
memory, as they often follow the same paths night after night (Höller<br />
1995).<br />
When commut<strong>in</strong>g between roost- and feed<strong>in</strong>g sites dur<strong>in</strong>g<br />
dusk and dawn periods, <strong>bats</strong> often follow outl<strong>in</strong>es <strong>in</strong> the landscape, such<br />
as river banks, forest edges, hedgerows and hillsides (Racey & Swift<br />
1985; Limpens & Kapteyn 1991; Verboom & Huitema 1997). The reason<br />
may be to m<strong>in</strong>imise predation risk (Swift 1998), or to use outl<strong>in</strong>es as<br />
acoustic landmarks, which perhaps facilitate navigation by sonar<br />
(Verboom et al. 1999). More likely, however, landscape outl<strong>in</strong>es and<br />
silhouettes provide the <strong>bats</strong> with visual cues, contrast<strong>in</strong>g aga<strong>in</strong>st the<br />
twilight sky, and such cues are probably essential for orientation and<br />
navigation along travell<strong>in</strong>g routes (Davis 1966; Layne 1967; Griff<strong>in</strong><br />
1970; Manske & Schmidt 1979; Höller and Schmidt 1996).<br />
Balantiopteryx plicata<br />
(Emballonuridae) relies on<br />
visual cues when presented<br />
with conflict<strong>in</strong>g <strong>in</strong>formation<br />
from vision and sonar, for<br />
example <strong>in</strong> front of a<br />
w<strong>in</strong>dow (Paper V).<br />
The frequent observation that <strong>bats</strong> have a tendency to crash <strong>in</strong>to w<strong>in</strong>dows<br />
of build<strong>in</strong>gs when released <strong>in</strong>doors (Fenton 1975), dur<strong>in</strong>g migration<br />
(Timm 1988), or commut<strong>in</strong>g (Test 1967), suggests that they<br />
predom<strong>in</strong>antly rely on vision rather than on echolocation <strong>in</strong> situations<br />
when both acoustic and visual cues are available. The performance is<br />
greatly improved, i.e. there are fewer collisions, when the <strong>bats</strong> are bl<strong>in</strong>ded<br />
25
(Davis & Barbour 1965) or when they are flown under dark conditions,<br />
and hence are “forced” to rely on echolocation alone. The <strong>in</strong>sectivorous<br />
Balantiopteryx plicata (Emballonuridae) was studied at different times of<br />
the day <strong>in</strong> an empty mesh greenhouse (Paper V). At night they flew<br />
smoothly and could easily avoid the ceil<strong>in</strong>g and the walls of the<br />
greenhouse, but dur<strong>in</strong>g the day and at dusk and dawn they often tried to<br />
fly through the mesh and thereby crashed <strong>in</strong>to it. The <strong>bats</strong> used<br />
echolocation consistently and without any dramatic change <strong>in</strong><br />
echolocation call structure that could be related to the prevail<strong>in</strong>g light<br />
conditions. The study <strong>in</strong>dicates that emballonurid <strong>bats</strong> trust their eyes<br />
over their ears when exposed to contradictory auditory and visual cues.<br />
Close range orientation and navigation<br />
When mov<strong>in</strong>g towards rest<strong>in</strong>g places and specific sites with<strong>in</strong> roosts, <strong>bats</strong><br />
sometimes face extremely unfavourable conditions for orientation, such<br />
as darkness, acoustic clutter from the walls of the roost, and simultaneous<br />
echolocation calls from many <strong>in</strong>dividuals. It is therefore likely that arrays<br />
of different sensory cues are used <strong>in</strong> such situations, and also that a good<br />
spatial memory is of great importance (Höller & Schmidt 1996). When<br />
<strong>in</strong>troduced <strong>in</strong> a dark flight cage, Nyctophilus spp. (Vespertilionidae)<br />
ceased to echolocate after 6-8 hours of flight (Grant 1991), suggest<strong>in</strong>g<br />
that they can learn to orient <strong>in</strong>side the cage, us<strong>in</strong>g spatial memory alone.<br />
In the same way, Megaderma lyra (Megadermatidae) remembers the<br />
positions of narrow open<strong>in</strong>gs with an accuracy of 2 cm, and if an obstacle<br />
is removed from the flight path, the <strong>bats</strong> may cont<strong>in</strong>ue to avoid that<br />
position for days (Neuweiler & Möhres 1966). However, <strong>bats</strong> do not trust<br />
their spatial memory exclusively, but can compare stored data with new<br />
echo-acoustical and visual <strong>in</strong>formation (Joermann et al. 1988; Schmidt et<br />
al. 1988; Höller 1995). When fly<strong>in</strong>g <strong>in</strong> a room of subdued daylight, the<br />
two frugivores Carollia perspicillata and Phyllostomus hastatus<br />
(Phyllostomidae) are able to see and avoid obstacles consist<strong>in</strong>g of 30 cm<br />
wide strips of cloth <strong>in</strong> their flight path (Chase & Suthers 1969). Those<br />
that were deafened with earplugs avoided the obstacles significantly<br />
better than those that were both deafened and bl<strong>in</strong>dfolded, show<strong>in</strong>g that<br />
they could obta<strong>in</strong> visual <strong>in</strong>formation of features <strong>in</strong> the environment<br />
dur<strong>in</strong>g flight. These results are consistent with those of Bradbury and<br />
Nottebohm (1969), who found that Myotis lucifugus (Vespertilionidae)<br />
avoided collisions <strong>in</strong> a str<strong>in</strong>g maze better <strong>in</strong> dim light than <strong>in</strong> total<br />
darkness. Rother and Schmidt (1982) noted that Phyllostomus discolor<br />
(Phyllostomidae) uses fewer sonar pulses <strong>in</strong> adequate illum<strong>in</strong>ation than <strong>in</strong><br />
darkness. When fly<strong>in</strong>g the <strong>bats</strong> <strong>in</strong> a str<strong>in</strong>g maze, the same authors also<br />
26
showed that fewer pulses were used if the obstacles exceeded 0.25 mm <strong>in</strong><br />
width. The results suggest that vision can shorten the <strong>bats</strong>’ reaction time<br />
for avoid<strong>in</strong>g obstacles <strong>in</strong> a flight path, as long as there is enough ambient<br />
light and the obstacles are of sufficient size (given by the visual acuity<br />
threshold and the range).<br />
Joermann et al. (1988) studied land<strong>in</strong>g performance <strong>in</strong> two<br />
captive species of Phyllostomidae (Desmodus rotundus and Phyllostomus<br />
discolor). The <strong>bats</strong> were presented with visual illusions of land<strong>in</strong>g grids,<br />
which thus gave them conflict<strong>in</strong>g acoustic and visual <strong>in</strong>formation.<br />
Although the grids were not detectable by echolocation, the <strong>bats</strong> seemed<br />
to aim for them, and only ca 30 cm <strong>in</strong> front of the illusions the <strong>bats</strong><br />
<strong>in</strong>terrupted the approach and turned away. The authors concluded that<br />
<strong>bats</strong> rely ma<strong>in</strong>ly on echo-acoustical cues at close range, but <strong>in</strong> some<br />
situations they defer to visual cues <strong>in</strong> an early phase of detection, even<br />
with<strong>in</strong> the range of echolocation.<br />
To <strong>in</strong>vestigate what sense the Anoura geoffroyi<br />
(Phyllostomidae) (Chase 1981; 1983) and the Tadarida brasiliensis<br />
(Molossidae) (Mistry 1990) would defer to when escap<strong>in</strong>g from a roost,<br />
the <strong>bats</strong> were flown <strong>in</strong> a Y-maze, <strong>in</strong> which one exit was blocked with<br />
Plexiglas and illum<strong>in</strong>ated with a light source. The other exit was open but<br />
dark. When tested <strong>in</strong> daytime, nearly all <strong>bats</strong> chose the illum<strong>in</strong>ated “exit”,<br />
thus <strong>in</strong>dicat<strong>in</strong>g that they believed the light was an open<strong>in</strong>g. However,<br />
when releas<strong>in</strong>g <strong>bats</strong> at night, the escape behaviour was the opposite, the<br />
<strong>bats</strong> choos<strong>in</strong>g the dark exit. It was suggested that the synchrony of light<br />
schedules to the <strong>bats</strong>’ circadian rhythm might determ<strong>in</strong>e the use of the<br />
appropriate sense (Mistry 1990).<br />
<strong>Vision</strong> <strong>in</strong> forag<strong>in</strong>g and prey detection<br />
At close range, echolocation usually gives more detailed <strong>in</strong>formation<br />
about the prey than vision (Suthers & Wallis 1970; Pettigrew 1980).<br />
However, <strong>in</strong> some situations, it may be favourable to change the modality<br />
with which to search for prey, and <strong>in</strong>deed, many <strong>bats</strong> use a variety of<br />
sensory cues, <strong>in</strong>clud<strong>in</strong>g smell (Hessel & Schmidt 1994; Kalko et al. 1996;<br />
Helversen et al. 2000), passive listen<strong>in</strong>g for prey generated sounds<br />
(Fiedler 1979; Ryan & Tuttle 1987; Arlettaz et al. 2001), tactile<br />
<strong>in</strong>formation (Baron et al. 1996c), visual cues (Bell 1985), and vampire<br />
<strong>bats</strong> possess the ability of thermo-perception (Kürten & Schmidt 1982).<br />
27
Insectivores and carnivores<br />
For <strong>bats</strong> that search for <strong>in</strong>sects with<strong>in</strong> or near vegetation, separation of<br />
prey echoes from the background clutter is usually a severe problem<br />
when us<strong>in</strong>g sonar alone (Jensen et al. 2001). In such situations <strong>bats</strong> have<br />
to rely on additional sensory cues to locate the prey. Nevertheless, few<br />
studies have addressed the obvious possibility that visual cues may be<br />
used for detection of prey <strong>in</strong> acoustically complex environments.<br />
However, when northern <strong>bats</strong> (Eptesicus nilssonii) search for stationary<br />
targets among high grass (clutter), this seems <strong>in</strong>deed to be the case<br />
(Paper II, Paper III). Dur<strong>in</strong>g early summer <strong>in</strong> Sweden, ghost swift<br />
moths Hepialus humuli (Lepidoptera: Hepialidae) swarm <strong>in</strong> stationary<br />
display flight over and among grass at dusk. These moths are large (ca 6<br />
cm w<strong>in</strong>gspan) and conspicuously silvery white (Andersson et al. 1998),<br />
and <strong>in</strong> contrast to most other moths, they lack ultrasonic hear<strong>in</strong>g (Rydell<br />
1998), and are <strong>in</strong>tensively exploited by northern <strong>bats</strong> patroll<strong>in</strong>g <strong>in</strong> the air<br />
over the field (Andersson et al. 1998; Rydell 1998; Jensen et al. 2001). In<br />
an experimental set-up, mak<strong>in</strong>g use of this natural forag<strong>in</strong>g situation,<br />
Hepialus humuli were presented to the <strong>bats</strong>, either with their white dorsal<br />
side up or with their dark ventral side up. It was found that the white<br />
moths were attacked more frequently than the dark ones, <strong>in</strong>dicat<strong>in</strong>g that<br />
the <strong>bats</strong> were guided by visual cues (Paper II).<br />
The aerial hawk<strong>in</strong>g northern bat,<br />
Eptesicus nilssonii (Vespertilionidae),<br />
uses visual cues as a complement to<br />
echolocation when search<strong>in</strong>g for<br />
moths <strong>in</strong> acoustically complex<br />
environments (Paper II, III).<br />
28
The brown long-eared bat Plecotus auritus (Vespertilionidae) is a<br />
glean<strong>in</strong>g <strong>in</strong>sectivore, which usually uses its large and sensitive ears to<br />
passively locate its prey by the noise they make (Anderson & Racey<br />
1991). However Plecotus auritus also has relatively big eyes (Cranbrook<br />
1963, Tab 1), suggest<strong>in</strong>g that they have relatively good vision. We<br />
<strong>in</strong>vestigated if brown long-eared <strong>bats</strong> exploit visual cues when search<strong>in</strong>g<br />
for prey (Paper I). By us<strong>in</strong>g petri dishes, conta<strong>in</strong><strong>in</strong>g mealworms that<br />
either were available to the <strong>bats</strong> or presented under glass, and present<strong>in</strong>g<br />
these <strong>in</strong> different levels of illum<strong>in</strong>ation, we provided the <strong>bats</strong> with visual<br />
cues, sonar cues or both. The <strong>bats</strong> did best <strong>in</strong> situations where both sonar<br />
cues and visual cues were available, but the visual <strong>in</strong>formation seemed to<br />
be more important than sonar.<br />
Glean<strong>in</strong>g brown long-eared <strong>bats</strong>,<br />
Plecotus auritus (Vespertilionidae),<br />
feed<strong>in</strong>g from bowls present<strong>in</strong>g<br />
different sensory cues, seem to<br />
prefer visual <strong>in</strong>formation to sonar<br />
cues. (Paper I).<br />
The California leaf-nosed bat Macrotus californicus (Phyllostomidae), a<br />
gleaner that normally searches for prey on the ground, has been shown to<br />
locate prey by us<strong>in</strong>g auditory- and visual cues as well as by sonar. Indeed<br />
this bat shows a particularly flexible hunt<strong>in</strong>g behaviour. In moonlight<br />
Macrotus californicus can see well enough to hunt us<strong>in</strong>g vision alone<br />
(Bell 1985). This allows the bat to hunt without alert<strong>in</strong>g the prey with<br />
ultrasound (Fullard 1987; Rydell 1992a), and also to detect stationary<br />
targets, which otherwise would be hard to detect (Arlettaz et al. 2001;<br />
Jensen et al. 2001; Paper II). In visual acuity tests Macrotus californicus<br />
responded to stripes subtend<strong>in</strong>g 0.06° arc, (Tab 2), which is the best<br />
visual acuity found <strong>in</strong> any microchiropteran bat (Bell & Fenton 1986).<br />
29
Moreover, the eyes of Macrotus californicus are relatively large and have<br />
a much higher degree of b<strong>in</strong>ocular overlap (50°) than <strong>in</strong> other <strong>bats</strong> (for<br />
example Antrozous pallidus 25° and Eptesicus fuscus 19°, Bell & Fenton<br />
1986). This suggests that Macrotus californicus has good stereoscopic<br />
vision and that the near field distance perception is of great importance<br />
(McIlwa<strong>in</strong> 1996), as would be expected <strong>in</strong> a species that forage visually.<br />
Macrotus californicus exploits diurnal prey, that are stationary at night<br />
and therefore unavailable to other <strong>bats</strong> (e.g. Howell 1920 cited <strong>in</strong> Bell &<br />
Fenton 1986).<br />
The African yellow-w<strong>in</strong>ged bat Lavia frons<br />
(Megadermatidae) employs feed<strong>in</strong>g tactics that <strong>in</strong>volve both glean<strong>in</strong>g and<br />
aerial hawk<strong>in</strong>g. This species is a sit-and-wait predator, which scans the<br />
vic<strong>in</strong>ity while hang<strong>in</strong>g from a branch, wait<strong>in</strong>g for <strong>in</strong>sects to pass by.<br />
Lavia frons is active <strong>in</strong> relative bright ambient illum<strong>in</strong>ation, at dusk as<br />
well as late morn<strong>in</strong>gs, and is often seen catch<strong>in</strong>g prey aga<strong>in</strong>st the sky. It<br />
has large eyes and may be able to see <strong>in</strong>sects aga<strong>in</strong>st the bright sky<br />
(Vaughan & Vaughan 1986). Nyctophilus gouldi and Nyctophilus<br />
geoffroyi (Vespertilionidae), also comb<strong>in</strong>e aerial hawk<strong>in</strong>g with glean<strong>in</strong>g,<br />
and have been shown to use different sensory cues accord<strong>in</strong>g to<br />
circumstances. As <strong>in</strong> Lavia frons, visual cues are preferentially used to<br />
detect prey <strong>in</strong> the air, whereas auditory cues are used to detect prey on the<br />
ground (Grant 1991). The visual acuity of Nyctophilus gouldi is nowhere<br />
near that of Macrotus californicus and Antrozous pallidus, but rather<br />
similar to that of other aerial hawk<strong>in</strong>g Vespertilionidae (Tab 2), which<br />
expla<strong>in</strong>s why they cannot f<strong>in</strong>d prey on the ground visually.<br />
Eklöf & Anderson (unpublished) observed northern <strong>bats</strong><br />
(Eptesicus nilssonii, Vespertilionidae) feed<strong>in</strong>g under midnight sun<br />
conditions <strong>in</strong> northern Norway. The <strong>bats</strong> caught prey aga<strong>in</strong>st the bright<br />
sky and sometimes without detectable sonar signals. However, based on<br />
the performance of Eptesicus fuscus (Tab 2) it seems unlikely that<br />
Eptesicus nilssonii has sufficient resolv<strong>in</strong>g power to detect small airborne<br />
prey visually. A 2 cm <strong>in</strong>sect is first detected at a distance of ca 1 m us<strong>in</strong>g<br />
vision (consider<strong>in</strong>g a visual acuity of 0.7° -1° arc, Tab 2), but the same<br />
object is first detected at ca 5 m us<strong>in</strong>g echolocation (Kick 1982), which<br />
thus suggests that echolocation would be the preferred sense. On the<br />
other hand, when northern <strong>bats</strong> search for ghost swift moths (described<br />
above), vision <strong>in</strong>creases the chance of detection of the prey, only because<br />
they exceed 5 cm <strong>in</strong> w<strong>in</strong>gspan and are detected at rather close range (3.5<br />
m) (Paper III). Smaller targets are detected us<strong>in</strong>g echolocation alone.<br />
Little brown <strong>bats</strong> (Myotis lucifugus) have been observed<br />
to catch prey apparently without us<strong>in</strong>g echolocation (D. R. Griff<strong>in</strong><br />
personal comm.) This species’ visual resolv<strong>in</strong>g power is even poorer than<br />
that of the northern bat, and <strong>in</strong> addition, its prey items are even smaller,<br />
30
so it is thus highly unlikely that vision is <strong>in</strong>volved <strong>in</strong> prey catch<strong>in</strong>g. In<br />
this species the apparent absence of echolocation calls must have another<br />
explanation. In fact, earlier observations of northern <strong>bats</strong> (Rydell 1992b)<br />
and little brown <strong>bats</strong> (Rydell et al. 2002) have suggested that attempted<br />
<strong>in</strong>sect captures are always associated with echolocation calls, even <strong>in</strong><br />
bright light conditions at high latitudes.<br />
Under conditions that appear to us to be completely dark<br />
(0 lux), <strong>bats</strong> may still be able to see conspicuous <strong>in</strong>sects. For example, it<br />
has been reported that bat activity is high where fireflies occur (Lloyd<br />
1989), and it has been shown that some fireflies stop flash<strong>in</strong>g when<br />
approached by <strong>bats</strong> (Farnworth 1973). This suggests that the light emitted<br />
by fireflies may guide the <strong>bats</strong> or at least evoke their curiosity. More<br />
<strong>in</strong>terest<strong>in</strong>gly, fireflies are not eaten by <strong>bats</strong> and were rejected by<br />
Eptesicus fuscus <strong>in</strong> feed<strong>in</strong>g experiments (Vernon 1981). In the same<br />
study, the <strong>bats</strong> were presented with flash<strong>in</strong>g fireflies as well as with<br />
artificial flashes. The <strong>bats</strong> responded to the flashes, although it was not<br />
clear if they associated the flashes with food or with unpalatability. It<br />
seems possible that firefly flashes may function as a visual aposematic<br />
signal to <strong>bats</strong>.<br />
Frugivores and nectarivores<br />
In general, fruit- and nectar feed<strong>in</strong>g <strong>bats</strong> have larger eyes (Tab 1), better<br />
visual resolv<strong>in</strong>g power (Tab 2) and enlarged visual and olfactory bulbs,<br />
compared to <strong>in</strong>sectivorous species (Jolicoeur & Baron 1980; Barton et al.<br />
1995; Barton & Harvey 2000). They also perceive and respond to<br />
different patterns more readily than <strong>in</strong>sectivorous species (Suthers &<br />
Chase 1966; Suthers et al. 1969), suggest<strong>in</strong>g that vision may perhaps play<br />
a more important role <strong>in</strong> these <strong>bats</strong> than <strong>in</strong> most <strong>in</strong>sectivores.<br />
Hessel and Schmidt (1994) <strong>in</strong>vestigated which sensory<br />
cues Carollia perspicillata (Phyllostomidae) uses when orient<strong>in</strong>g toward<br />
a food source. The <strong>bats</strong> were presented with a triple choice of passive<br />
acoustic-, olfactory-, and visual cues. At least <strong>in</strong>itially, the visual cue was<br />
the most frequently preferred stimulus. But after tra<strong>in</strong><strong>in</strong>g the <strong>bats</strong> changed<br />
their behaviour and responded more to the olfactory stimulus. The<br />
experiment suggests that Carollia perspicillata can detect new sources of<br />
food us<strong>in</strong>g visual cues, and that they subsequently rely more on olfaction<br />
as the food source becomes known. Indeed these <strong>bats</strong> seem to possess a<br />
remarkable sense of olfaction (Flem<strong>in</strong>g 1988; Laska 1990).<br />
Kalko et al. (1996) showed that fig eat<strong>in</strong>g Microchiroptera do not use<br />
vision when forag<strong>in</strong>g, presumably because figs eaten by these <strong>bats</strong> are<br />
visually <strong>in</strong>conspicuous. Instead, they rely ma<strong>in</strong>ly on olfactory cues,<br />
31
comb<strong>in</strong>ed with broadband echolocation. In fact, most bat-poll<strong>in</strong>ated<br />
plants are greenish, p<strong>in</strong>k and white, which presumably reflect the fact that<br />
<strong>bats</strong> are most likely colour-bl<strong>in</strong>d (Suthers 1970; Faegri & van der Pijl<br />
1979). On the contrary, many species of bat poll<strong>in</strong>ated Parkia<br />
(Legum<strong>in</strong>osae: Mimosoideae) have bright red and yellow colours<br />
(Hopk<strong>in</strong>s 1984). It is also suggested that dark flowers can be seen as<br />
silhouettes, aga<strong>in</strong>st the sky and that pale flowers appear conspicuous<br />
aga<strong>in</strong>st dark foliage (Start 1974, cited <strong>in</strong> Hopk<strong>in</strong>s 1984). If the <strong>bats</strong> make<br />
use of such differences <strong>in</strong> contrast, one would expect to f<strong>in</strong>d that the<br />
position of differently coloured flowers vary accord<strong>in</strong>gly <strong>in</strong> relation to the<br />
foliage, i.e., red flowers far from foliage and yellow flowers closer, which<br />
<strong>in</strong> fact, seems to be the case.<br />
The capitula of Parkia are also highly reflective under<br />
moonlight and starlight conditions, and are therefore presumably visible<br />
to poll<strong>in</strong>at<strong>in</strong>g <strong>bats</strong> (Hopk<strong>in</strong>s 1984). Many poll<strong>in</strong>ators make use of a broad<br />
spectrum reflected from flowers, fruits or seeds, <strong>in</strong>clud<strong>in</strong>g ultraviolet<br />
(UV) light (for example <strong>in</strong>sects, Kevan et al. 2001; and birds, Church et<br />
al. 2001). Ultraviolet vision seems, however, to be absent <strong>in</strong> most<br />
mammals, although some rodents have been shown to have UV sensitive<br />
ret<strong>in</strong>as (Jacobs et al. 1991). Recently, it was suggested that <strong>bats</strong> might<br />
perceive UV-light, as there is evidence for a spectral sensitivity peak<br />
around 390 nm (i.e. <strong>in</strong> the near UV-range) <strong>in</strong> the nectarivorous<br />
Glossophaga soric<strong>in</strong>a (Lopez et al. 2001). However, if the <strong>bats</strong> actually<br />
use UV reflect<strong>in</strong>g surfaces as orient<strong>in</strong>g cues is still uncerta<strong>in</strong>, although<br />
Willson and Whelan (1989) have shown that UV-reflectance is <strong>in</strong>deed<br />
relatively common throughout the plant k<strong>in</strong>gdom. The Passiflora species,<br />
Passiflora galbana and Passiflora mucronata, two plants which flowers<br />
are exploited by the nectarivorous glossophag<strong>in</strong>ae <strong>bats</strong>, reflect light down<br />
to ca 400 nm and 370 nm (upper UV range), respectively. This should be<br />
compared to the humm<strong>in</strong>gbird poll<strong>in</strong>ated Passiflora speciosa, which has<br />
its ma<strong>in</strong> reflection above 570 nm (Varass<strong>in</strong> et al. 2001), perhaps<br />
reflect<strong>in</strong>g the spectral sensitivity of the poll<strong>in</strong>ators. Furthermore, 80% of<br />
nocturnal Lepidoptera have w<strong>in</strong>g patterns that reflect UV, compared to ca<br />
30% <strong>in</strong> diurnal species (Lyyt<strong>in</strong>en 2001 cited <strong>in</strong> Honkavaara et al. 2002).<br />
On the other hand, this may imply that <strong>bats</strong> cannot make use of the<br />
ultraviolet light, <strong>in</strong> contrast to birds, which usually forage <strong>in</strong> daylight.<br />
32
Predator surveillance and social behaviour<br />
As discussed earlier, vision seems to be important <strong>in</strong> escape behaviour<br />
(Chase 1981; Chase 1983; Mistry 1990). Presumably it is also important<br />
<strong>in</strong> detection of predators; it is much easier to approach a bl<strong>in</strong>dfolded bat<br />
than a non-bl<strong>in</strong>dfolded <strong>in</strong>dividual (Chase 1972). Species of the family<br />
Emballonuridae often fly earlier <strong>in</strong> the even<strong>in</strong>g than most other <strong>bats</strong>, and<br />
sometimes even <strong>in</strong> the afternoon and they often roost on exposed and<br />
well lit sites such as tree trunks (e.g. Bradbury & Vehrencamp 1976). A<br />
Saccopteryx sp. will quite easily detect an approach<strong>in</strong>g person, and take<br />
flight without emitt<strong>in</strong>g any echolocation calls (Suthers 1970), and<br />
Rhynconycteris naso seems to be disturbed more easily by see<strong>in</strong>g an<br />
approach<strong>in</strong>g figure at a distance, than by sudden sounds or vibrations at<br />
close range (Dalquest 1957). Vaughan and Vaughan (1986) noted that<br />
Lavia frons (Megadermatidae), which also roosts exposed, seems to be<br />
constantly alert dur<strong>in</strong>g the day, scann<strong>in</strong>g its surround<strong>in</strong>gs for predators. In<br />
fact, the authors almost never saw a bat with its eyes closed, and were<br />
never able to approach one undetected.<br />
The evidence for the use of vision <strong>in</strong> social behaviour is<br />
ma<strong>in</strong>ly anecdotal. Social groom<strong>in</strong>g occurs <strong>in</strong> the vampire Desmodus<br />
rotundus (Phyllostomidae) and may serve to identify <strong>in</strong>dividuals<br />
(Wilk<strong>in</strong>son 1986), although it is generally rare (Flem<strong>in</strong>g 1988). Goodw<strong>in</strong><br />
and Greenhall (1961) noted that avian vampire <strong>bats</strong> (Diaemus youngi)<br />
show groom<strong>in</strong>g behaviour when see<strong>in</strong>g a mirror reflection, <strong>in</strong>dicat<strong>in</strong>g that<br />
vision might be <strong>in</strong>volved <strong>in</strong> this behaviour. Sometimes <strong>bats</strong> are also<br />
observed to imitate other <strong>in</strong>dividuals groom<strong>in</strong>g themselves (Vaughan &<br />
Vaughan 1986).<br />
Some bat species have dist<strong>in</strong>ct fur patterns, which may<br />
serve as visual recognition signals (Fenton 2001), <strong>in</strong> addition to scents<br />
and sound, although fur patterns may also serve as camouflage<br />
(Neuweiler 2000). Threat displays are common <strong>in</strong> for example Carollia<br />
perspicillata (Phyllostomidae), and <strong>in</strong>cludes w<strong>in</strong>g shak<strong>in</strong>g, harsh sounds,<br />
and aggressive looks such as extension of the tongue (Flem<strong>in</strong>g 1988).<br />
Sexual displays are also common. The monogamous Lavia frons and<br />
Cardioderma cor (Megadermatidae), perform stereotypical circular<br />
flights, described as aerial ballets (McWilliam 1987; Vaughan &<br />
Vaughan 1986). Among Saccopteryx bil<strong>in</strong>eata (Emballonuridae), the<br />
males defend territories where they ma<strong>in</strong>ta<strong>in</strong> harems. In front of the<br />
females of the harem, they perform sexual displays, which <strong>in</strong>clude<br />
stereotyped s<strong>in</strong>g<strong>in</strong>g, and also shak<strong>in</strong>g of w<strong>in</strong>gs and hover<strong>in</strong>g. The w<strong>in</strong>g<br />
shak<strong>in</strong>g presumably enhances the effect of olfactory glands by spread<strong>in</strong>g<br />
pheromones, but it may also function as a visual signal to draw the<br />
females’ attention (Chase 1972).<br />
33
Multimodality – vision and echolocation<br />
The echolocation detection range of a 19 mm <strong>in</strong>sect is around 5 m for<br />
Eptesicus fuscus (Kick 1982), and the visual acuity of this species is 0.7°-<br />
1° arc, Tab 2). This allows visual detection of the 19 mm object only<br />
when it is closer than ca 1 m. This simple calculation strongly suggests<br />
that echolocation is the more accurate sense at close range and for small<br />
objects. However, larger objects can be detected visually at distances of<br />
hundreds of meters, far beyond the range of echolocation. For example,<br />
an object of 5 m diameter can potentially be detected visually by<br />
Eptesicus fuscus at a distance of ca 300 m. Us<strong>in</strong>g echolocation; the same<br />
object is detected at a distance of only 25-30 m at most (depend<strong>in</strong>g on<br />
call strength, attenuation etc., Lawrence and Simmons 1982; M. B.<br />
Fenton personal comm.). This supports the general view that vision is<br />
used primarily for detection of large objects and landmarks and for<br />
navigat<strong>in</strong>g over longer distances (Davis 1966; Layne 1967; Griff<strong>in</strong> 1970;<br />
Höller and Schmidt 1996). Nevertheless, for <strong>bats</strong> with better visual<br />
resolv<strong>in</strong>g power, vision can be used and even replace echolocation, at<br />
short distances. The California leaf nosed bat Macrotus californicus,<br />
referred to above, can visually detect a 19 mm <strong>in</strong>sect at a distance of ca<br />
18 m. This presumably gives this bat a longer range of operation if they<br />
use vision <strong>in</strong>stead of echolocation, at least under conditions of moonlight<br />
or bright starlight (Bell & Fenton 1986). Other <strong>bats</strong>, such as some<br />
Emballonuridae, which have visual acuities below 0.4° arc (Tab 2), can<br />
visually detect <strong>in</strong>sect sized objects (1 cm) at distances less than 1 m,<br />
suggest<strong>in</strong>g a range of operation roughly similar for vision as for sonar.<br />
One could therefore assume that emballonurid <strong>bats</strong> could use either<br />
vision or echolocation to detect prey, as suggested by Pettigrew (1980).<br />
He observed one species of Emballonuridae (Craseonycteris<br />
thonglongyai) catch<strong>in</strong>g prey aga<strong>in</strong>st a bright sky apparently without us<strong>in</strong>g<br />
echolocation and suggested that the <strong>bats</strong> could see the <strong>in</strong>sects as<br />
silhouettes aga<strong>in</strong>st the sky.<br />
The Australian ghost bat Macroderma gigas<br />
(Megadermatidae) also has a similar prey detection range for vision as for<br />
echolocation. S<strong>in</strong>ce this species also has good auditory sensitivity <strong>in</strong> the<br />
sonic range (Fiedler 1979; Kulzer et al. 1984), it switches between vision,<br />
echolocation and passive listen<strong>in</strong>g (Pettigrew et al. 1986; Pettigrew et al.<br />
1983). For frequencies below 20 kHz, the acoustic axis (as def<strong>in</strong>ed from<br />
the directionality of the p<strong>in</strong>na and noseleaf) of Macroderma gigas is<br />
aligned with the visual axis (def<strong>in</strong>ed by areas of highest ganglion cell<br />
density), <strong>in</strong>dicat<strong>in</strong>g that auditory cues help the <strong>bats</strong> to visually detect the<br />
source of the sound (Pettigrew 1988). In fact, a major function of sound<br />
localisation <strong>in</strong> animals is to direct the eyes toward the sound-source<br />
34
(Heffner & Heffner 1992; Heffner et al. 1999). This reflex is even<br />
quicker than the reaction to a flashlight (Whitt<strong>in</strong>gton et al. 1981), and<br />
hence suggests that hear<strong>in</strong>g is closely co-ord<strong>in</strong>ated with vision (Heffner<br />
1997).<br />
Sound localisation acuity is related to ret<strong>in</strong>al organisation<br />
and the width of fields of best vision (def<strong>in</strong>ed as the portion of the ret<strong>in</strong>a<br />
with at least 75% of maximum ganglion cell density, Heffner et al. 2001).<br />
Animals with narrow fields of best vision (foveae) have generally better<br />
localisation acuity than animals with broad or elongated fields of best<br />
vision (visual streaks). The ret<strong>in</strong>as of microchiropteran <strong>bats</strong> are loosely<br />
arranged <strong>in</strong> visual streaks and the density of ganglion cells falls<br />
irregularly toward the periphery. The field of best vision is concentrated<br />
<strong>in</strong> the temporal part of the ret<strong>in</strong>a and seems to be broader <strong>in</strong> frugivores<br />
than <strong>in</strong> <strong>in</strong>sectivorous species (Heffner et al. 2001). Overall, there is a<br />
higher ganglion cell density <strong>in</strong> the <strong>in</strong>ferior part of the ret<strong>in</strong>a than <strong>in</strong> the<br />
superior (Marks 1980; Pettigrew et al. 1988; Koay et al. 1998; Heffner et<br />
al. 2001; Eklöf unpublished). This means that the sharpest image on the<br />
ret<strong>in</strong>a results from light reach<strong>in</strong>g the eye from above, and consequently,<br />
the bat eyes focus slightly upwards. Without mov<strong>in</strong>g their heads, <strong>bats</strong> are<br />
look<strong>in</strong>g up (Pettigrew 1988). The functional significance of this can be<br />
difficult to establish, but it seems likely that vision and echolocation have<br />
evolved to provide the bat with as little <strong>in</strong>formation overlap as possible.<br />
While echolocation call emission and hear<strong>in</strong>g is most effective <strong>in</strong> the<br />
flight direction and downwards (Schnitzler & Gr<strong>in</strong>nell 1977; b), vision<br />
serves as a complement by be<strong>in</strong>g most effective upwards it thus gives<br />
additional <strong>in</strong>formation of obstacles and landmarks further away. In<br />
Megachiroptera, which do not echolocate, one would thus expect the<br />
fields of best vision to be above rather than below the optic disk, which <strong>in</strong><br />
fact seems to be the case (Pettigrew 1986).<br />
All <strong>bats</strong> have well developed ret<strong>in</strong>ofugal projections<br />
(pathways of <strong>in</strong>formation from ret<strong>in</strong>a to visual cortex) to the lateral<br />
geniculate nuclei as well as to the superior colliculus (see above), which<br />
are the ma<strong>in</strong> targets for ret<strong>in</strong>al projections <strong>in</strong> mammals (Pentney & Cotter<br />
1976; Suthers & Bradford 1980; Reimer 1989). In the superior colliculus,<br />
different sensory modalities are <strong>in</strong>tegrated and transformed, and the<br />
output may be perceived as a “new product” (Ste<strong>in</strong> & Meredith 1993).<br />
The capacity to deal with multisensory <strong>in</strong>formation is however developed<br />
first after experience of multimodal <strong>in</strong>puts (Wallace & Ste<strong>in</strong> 2001). The<br />
superior colliculus controls for example eye movements, which serves to<br />
keep objects of <strong>in</strong>terest <strong>in</strong> the focal field. Auditory projections to the<br />
superior colliculus are generally sparse <strong>in</strong> mammals. However, <strong>in</strong> the<br />
mustache bat Pteronotus parnellii (Mormoopidae), at least three areas <strong>in</strong><br />
the bra<strong>in</strong> stem contribute with well-developed auditory projections to the<br />
35
superior colliculus. It has been shown that p<strong>in</strong>na movements can be<br />
controlled <strong>in</strong> the same way as eye movements <strong>in</strong> other mammals (Covey<br />
et al. 1987), and thus that orient<strong>in</strong>g behaviour can be <strong>in</strong>fluenced through<br />
auditory as well as through visual feedback. It is also known that auditory<br />
stimuli can trigger visuomotor neurones and hence that the eyes can<br />
respond to sounds (Ste<strong>in</strong> & Meredith 1993). Comb<strong>in</strong>ed sensory <strong>in</strong>puts<br />
can enhance perception and detection, but also cause behavioural<br />
depression, for example when the cues are contradictory, as <strong>in</strong> the case<br />
with <strong>bats</strong> and w<strong>in</strong>dows (discussed above). Cats have been shown to<br />
respond “half way” between contradict<strong>in</strong>g sounds and images (Ste<strong>in</strong> &<br />
Meredith 1993), but <strong>in</strong> most cases when animals have multiple cues to<br />
choose from, one can see a clear sensory hierarchy (e.g. Dyer & Gould<br />
1981), so also <strong>in</strong> <strong>bats</strong> (Chase 1983). However, the hierarchy can change<br />
depend<strong>in</strong>g on the behavioural context. Visual cues have been shown to<br />
have precedence over auditory cues <strong>in</strong> for example escape behaviour and<br />
when commut<strong>in</strong>g (Chase 1981; Chase 1983; Mistry 1990; Paper V). In<br />
cases where echolocation and visual cues are complementary rather than<br />
contradictory, the <strong>bats</strong> may still rely on vision over sonar. In a study on<br />
brown long-eared <strong>bats</strong> (Plecotus auritus), feed<strong>in</strong>g from bowls present<strong>in</strong>g<br />
different sensory cues (Paper I), the <strong>bats</strong> scored best <strong>in</strong> situations where<br />
both visual and sonar cues were present. The visual <strong>in</strong>formation seemed<br />
however to be the more important.<br />
It has been suggested that there sometimes can be<br />
<strong>in</strong>terference between the two senses. For example, Simmons (cited <strong>in</strong><br />
Chase 1981) has noted that some <strong>bats</strong> have a problem learn<strong>in</strong>g acoustic<br />
discrim<strong>in</strong>ation when visual cues are present, but can easily perform the<br />
same task <strong>in</strong> darkness. When tra<strong>in</strong>ed to respond to black or white<br />
triangles of different size, Myotis lucifugus (Vespertilionidae) responded<br />
to brightness cues rather than the size of the triangles, although these <strong>bats</strong><br />
are capable of size discrim<strong>in</strong>ation by echolocation (Ell<strong>in</strong>s 1970;<br />
Masterson & Ell<strong>in</strong>s 1974). This suggests that <strong>in</strong>terference may have<br />
occurred, or at least that the <strong>bats</strong> had a preference for visual cues <strong>in</strong> this<br />
case.<br />
It is not yet known if <strong>bats</strong> can perform cross-modal<br />
recognition, i.e. learn<strong>in</strong>g an object us<strong>in</strong>g one sense and then immediately<br />
recognis<strong>in</strong>g the same object by us<strong>in</strong>g another sense, which is the case<br />
with for example bottle nose dolph<strong>in</strong>s Tursiops truncatus. These animals<br />
can <strong>in</strong>tegrate <strong>in</strong>formation from vision to echolocation just as well as from<br />
echolocation to vision. Hence, what the dolph<strong>in</strong>s perceive from one sense<br />
is functionally similar of what it perceives from the other (Pack &<br />
Herman 1995).<br />
Although the question of how sensory <strong>in</strong>puts are comb<strong>in</strong>ed <strong>in</strong> <strong>bats</strong><br />
rema<strong>in</strong>s unsolved, several authors have shown the importance of<br />
36
multimodality (Pettigrew et al. 1983; Schmidt 1988; Hessel & Schmidt<br />
1994). In a two choice test, two phyllostomid <strong>bats</strong> (Desmodus rotundus<br />
and Phyllostomus discolor) were tra<strong>in</strong>ed to respond to a comb<strong>in</strong>ation of<br />
visual, olfactory and acoustic stimuli, and were then presented with one<br />
of the three modalities separately (Schmidt et al. 1988). It was found that<br />
Phyllostomus discolor chose the visual stimuli to a higher degree,<br />
whereas Desmodus rotundus preferred the passive acoustic stimuli.<br />
However, both <strong>bats</strong> were able to respond to all three modalities, although<br />
responses to the olfactory stimuli needed additional tra<strong>in</strong><strong>in</strong>g, as also noted<br />
by Hessel and Schmidt (1994), when study<strong>in</strong>g Carollia perspicillata.<br />
However when the Carollia had learned to respond to the olfactory cue,<br />
this became the preferred stimuli, which was not the case with Desmodus<br />
or Phyllostomus, which both used two other senses. This clearly shows<br />
that <strong>bats</strong> use an array of different senses <strong>in</strong> the field, and that ecology,<br />
feed<strong>in</strong>g strategies and behavioural context all <strong>in</strong>fluence the use of<br />
different modalities.<br />
Echolocation may be the most important <strong>in</strong>novation<br />
throughout bat evolution, allow<strong>in</strong>g these animals to explore a niche of<br />
their own. But there is more to the sensory ecology of microchiropteran<br />
<strong>bats</strong>, where vision is an important piece of the puzzle and certa<strong>in</strong>ly needs<br />
further attention <strong>in</strong> the future.<br />
37
Acknowledgements<br />
First of all I would like to acknowledge all the co-authors of this thesis for obvious<br />
reasons, and I wish to thank Olof Helje for mak<strong>in</strong>g the splendid bat illustrations. Then I<br />
wish to thank my supervisor and mentor -Jens Rydell – and also, many thanks to the rest<br />
of the Rydell family for your great hospitality.<br />
There are several people hav<strong>in</strong>g answered several more or less stupid questions on<br />
<strong>bats</strong>, vision, statistics, experimental design, the mean<strong>in</strong>g of life and other various topics<br />
throughout the years. Especially I would like to thank Donald R Griff<strong>in</strong> and Brock<br />
Fenton, but also Eric Warrant, Dan E Nilsson, Tom, Gareth Jones, Susan Swift, Krist<strong>in</strong>a<br />
Mieziewska, W<strong>in</strong>ston Lancaster; and of course, many thanks to Cajsa, John G,<br />
Christoffer, Gim, Jen, Christ<strong>in</strong>, John R, Marc, Jenny, Kalle, Krist<strong>in</strong>a, Cess, Bomull,<br />
Tobias, Annika, Christoffer and Staffan, just to mention a few of you.<br />
Just as many people have helped me to make the every day work possible; at the<br />
department, by jo<strong>in</strong><strong>in</strong>g me <strong>in</strong> the field, on conferences, courses and work shops and to<br />
some extent even <strong>in</strong> the lab (although some may th<strong>in</strong>k I do not know what that is); hav<strong>in</strong>g<br />
helped me arrange field work and experiments, be<strong>in</strong>g guides, eye suppliers, hosts, or just<br />
good company dur<strong>in</strong>g batt<strong>in</strong>g. Especially I wish to thank Monica, Tompa and Cajsa,<br />
thanks also to Maria, Héctor, Henke, Luis-Bernardo, Hans, Marie, Gabriela, Stefan, Åsa,<br />
Per, Britt-Louise, Anna, Lee, Dr. F-Jo, Blomman, Karl-Johan, Stefan, Sean, Jorge, Jenny,<br />
Andreas, Eric, Lars-Erik, Cess, Annemarie, Magnus, Berndt, Dave, Anne-Sofie, Bengt,<br />
Mia, Lilioth, the “NASBR and Chamela-students”, the Lövhaugs, all other department<br />
employees not mentioned, and of course Mexican hospitality and British humour.<br />
For unknown reasons, I have been deeply <strong>in</strong>volved, not only <strong>in</strong> research and<br />
teach<strong>in</strong>g, but also <strong>in</strong> the work of the faculty board, the Swedish Association of Scientists<br />
and the Students’ Union. I wish to thank the various members of all the different work<strong>in</strong>g<br />
groups and committees, not at least Cajsa, Marie, Stefan Henrik, and Andreas.<br />
There are other th<strong>in</strong>gs but science, like hav<strong>in</strong>g almost normal conversations, shar<strong>in</strong>g<br />
stupid ideas, try<strong>in</strong>g to do music, ly<strong>in</strong>g on beaches, e-mail<strong>in</strong>g, hav<strong>in</strong>g coffee and dr<strong>in</strong>k<strong>in</strong>g<br />
beer, and presumably some other stuff as well. For those th<strong>in</strong>gs, I wish to thank Per and<br />
Andreas for help<strong>in</strong>g me to create “PSL” which for a while brought order to my life, much<br />
<strong>in</strong> the same way as “Johnny” did, only different. I wish to thank the e-mailers, the<br />
floorballers, the chatters, the Herb Boys crew and fan club, the coffee dr<strong>in</strong>kers and the<br />
travellers. There is no doubt that the Friday after work sessions have been almost as<br />
important as the actual research for be<strong>in</strong>g able to f<strong>in</strong>ish this thesis. I wish to acknowledge<br />
the most frequent ones: Christoffer, Anna, Viktoria, Ågot and lately Jenny P. But of<br />
course, Sara, Erik, Fredrik, Jenny T, L<strong>in</strong>da, Tove, Goran and a whole bunch of other youknow-who-you-are.<br />
There are two persons hav<strong>in</strong>g shared my biology- as well as my non<br />
biology-time, to a larger extent than perhaps any others: first of all, thank you Cajsa for<br />
not br<strong>in</strong>g<strong>in</strong>g your calculator; and for numerous moments thereafter, and second, Tompa,<br />
for mak<strong>in</strong>g everyday April fools day.<br />
Thank you all on the second floor: Per, Bengt, Stig, Gunnar, Anders, Inger, Lena,<br />
Åke, Jan, Sebbe, Björn, Jenny, Mal<strong>in</strong>, Urban, Anna H, Anna Z, Monica, Susanne, Ulla,<br />
Mare, Christoffer, Arne, Marcus, other hangarounds, not mentioned, past and present.<br />
Thank you mom, dad, and Kristian, and thanks to all friends <strong>in</strong> the real world. My work<br />
has been funded by Kungliga och Hvitfeldtska Stiftelsen, Lunds Djurskyddsfond, Knut<br />
och Alice Wallenbergs Stiftelse, Folke Eklöf, Adlerbertska Forskn<strong>in</strong>gsstiftelsen, Wilhelm<br />
och Mart<strong>in</strong>a Lundgrens Vetenskapsfond, Kungliga vetenskaps- och Vitterhetssamhället i<br />
Göteborg, Stiftelserna Paul och Marie Berghaus Donationsfond, J A Ahlstrands<br />
Testamentsfond, Lars Hiertas M<strong>in</strong>ne, and Rådman & Fru Ernst Collianders Stiftelse FVÄ,<br />
and of course CSN.<br />
F<strong>in</strong>ally I wish to acknowledge (please fill out your name); believe me you are not really forgotten.<br />
38
References<br />
Ahlén, I. 1997. Migratory behaviour of <strong>bats</strong> at south Swedish coasts. Z. Säugetierk. 62, 375-380<br />
Altr<strong>in</strong>gham, J. D. 1996. Bats: biology and behaviour. Oxford University Press, Oxford UK<br />
Anderson, M. E. & Racey, P. A. 1991. Feed<strong>in</strong>g behaviour of captive long eared-<strong>bats</strong>, Plecotus<br />
auritus. Anim. Behav. 42, 489-493<br />
Andersson, S., Rydell, J. & Svensson, M. G. E. 1998. Light, predation and the lekk<strong>in</strong>g behaviour of<br />
the ghost swift Hepialus humuli (L.) (Lepidoptera: Hepialidae). Proc. R. Soc. Lond. B 264, 1345-<br />
1351<br />
Arlettaz, R., Jones, G. & Racey, P. A. 2001. Effect of acoustic clutter on prey detection by <strong>bats</strong>.<br />
Nature 414, 742-745<br />
Baron, G., Stephan, H. & Frahm, H. D. 1996a. Comparative neurobiology <strong>in</strong> Chiroptera vol. I<br />
Macromorphology, bra<strong>in</strong> structures, tables and atlases. Birkhäuser Verlag, Basel, Switzerland<br />
Baron, G., Stephan, H. & Frahm, H. D. 1996b. Comparative neurobiology <strong>in</strong> Chiroptera vol. II Bra<strong>in</strong><br />
characteristics <strong>in</strong> taxonomic units. Birkhäuser Verlag, Basel, Switzerland<br />
Baron, G., Stephan, H. & Frahm, H. D. 1996c. Comparative neurobiology <strong>in</strong> Chiroptera vol. III Bra<strong>in</strong><br />
characteristics <strong>in</strong> functional systems, ecoethological adaptation, adaptive radiation and evolution.<br />
Birkhäuser Verlag, Basel, Switzerland<br />
Barton, R. A., Purvis, A. & Harvey, P. H. 1995. Evolutionary radiation of visual and olfactory bra<strong>in</strong><br />
systemes <strong>in</strong> primates, <strong>bats</strong> and <strong>in</strong>sectivores. Phil. Trans. R. Soc. Lond. B 348, 381-392<br />
Barton, R. A. & Harvey, P. H. 2000. Mosaic evolution of bra<strong>in</strong> structure <strong>in</strong> mammals. Nature 405,<br />
1055-1058<br />
Bell, G. P. 1985. The sensory basis of prey location by the California leaf-nosed bat Macrotus<br />
californicus (Chiroptera: Phyllostomidae). Behav. Ecol. Sociobiol. 16, 343-347<br />
Bell, G. P. & Fenton, M. B. 1986. Visual acuity, sensitivity and b<strong>in</strong>ocularity <strong>in</strong> a glean<strong>in</strong>g<br />
<strong>in</strong>sectivorous bat, Macrotus californicus (Chiroptera: Phyllostomidae). Anim. Behav. 34, 409-414<br />
Bogdanowicz, W. 1994. Myotis daubentonii. Mammalian Species 475, 1-9<br />
Bornsche<strong>in</strong>, H. 1961. Vergleichende Elektrophysiologie der Ret<strong>in</strong>a. In: Das Visuelle System.<br />
Neurophysiologie und Psychophysik (Jung, R. & Kornhuber, H. eds.). Berl<strong>in</strong>, Spr<strong>in</strong>ger-Verlag pp<br />
74-79<br />
Bradbury, J. & Nottebohm, F. 1969. The use of vision by the little brown bat, Myotis lucifugus,<br />
under controlled conditions. Anim. Behav. 17, 480-485<br />
Bradbury, J. W. & Vehrencamp, S. L. 1976. Social Organization and Forag<strong>in</strong>g <strong>in</strong> Emballonurid Bats<br />
I. Field studies. Behav. Ecol. Sociobiol. 1, 337-381<br />
Buchler, E. R. & Childs, S. B. 1981. Orientation to distant sounds by forag<strong>in</strong>g big brown <strong>bats</strong><br />
(Eptesicus fuscus). Anim. Behav. 29, 428-432<br />
Buchler, E. R. & Childs, S. B. 1982. Use of the post-sunset glow as an orientation cue by big brown<br />
<strong>bats</strong> (Eptesicus fuscus). J. Mammal. 63, 243-247<br />
39
Buchler, E. R. & Wasilewski, P. J. 1985. Mag<strong>net</strong>ic remanence <strong>in</strong> <strong>bats</strong>. In: Mag<strong>net</strong>ite<br />
Biom<strong>in</strong>eralization and Mag<strong>net</strong>oreception <strong>in</strong> Organisms: A New Biomag<strong>net</strong>ism. (Kirschv<strong>in</strong>k, J. L.,<br />
Jones, D. S. and MacFadden, B. J. eds.). New York: Plenum press, pp 483-487<br />
Chase, J. 1972. The role of vision <strong>in</strong> echolocat<strong>in</strong>g <strong>bats</strong>. Ph.D thesis, Indiana University<br />
Chase, J. 1981.Visually guided escape responses of microchiropteran <strong>bats</strong>. Anim. Behav. 29, 708-<br />
713<br />
Chase, J. 1983. Differential responses to visual and acoustic cues dur<strong>in</strong>g escape <strong>in</strong> the bat Anoura<br />
geoffroyi: cue preferences and behaviour. Anim. Behav. 31, 526-531<br />
Chase, J. & Suthers, R. A. 1969. Visual obstacle avoidance by echolocat<strong>in</strong>g <strong>bats</strong>. Anim. Behav. 17,<br />
201-207<br />
Childs, S. B. & Buchler, E. R. 1981. Perception of simulated stars by Eptesicus fuscus<br />
(Vespertilionidae): A potential navigational mechanism. Anim. Behav. 29, 1028-1035<br />
Chung, K. S., Lee, J. H. & Park, S. R. 1990. Visual pattern discrim<strong>in</strong>ation <strong>in</strong> the Oriental discoloured<br />
bat, Vespertilio superans. Korean J. Zool. 33, 127-132<br />
Church, S. C., Merrison, A. S. L. & Chamberla<strong>in</strong>, T. M. M. 2001. Avian ultraviolet vision and<br />
frequency dependent seed preferences. J. Exp. Biol. 204, 2491-2498<br />
Cotter, J. R. 1985. Ret<strong>in</strong>ofugal Projections of the Big Brown Bat, Eptesicus fuscus and the<br />
neotropical Fruit Bat, Artibeus jamaicensis. Am. J. Anat. 172, 105-124<br />
Cotter, J. R. & Pentney, R. P. 1979. Ret<strong>in</strong>ofugal projections of nonecholocat<strong>in</strong>g (Pteropus giganteus)<br />
and echolocat<strong>in</strong>g (Myotis lucifugus) <strong>bats</strong>. J. Comp. Neurol. 184, 381-399<br />
Covey, E., Hall, W. C. & Kobler, J. B. 1987. Subcortical connections of the Superior colliculus <strong>in</strong> the<br />
Mustache bat, Pteronotus parnellii. J. Comp. Neurology 263, 179-197<br />
Cowey, A. & Ellis, C. M. 1967. Visual acuity of rhesus and squirrel monkeys. J. Comp.<br />
Physiol.Psychol. 64, 80-84<br />
Cranbrook, The Earl of. 1963. Notes on the feed<strong>in</strong>g habits of the long-eared bat. Trans. Suff. Nat.<br />
Hist. Soc. 11, 1-3<br />
Crowle, P. K. 1980. Ret<strong>in</strong>ofugal projections to subcortical visual centers <strong>in</strong> the microchiropteran bat,<br />
Myotis sodalis. Proc. Mont. Acad. Sci. 30, 1-11<br />
Curtis, W. E. 1952. Quantative studies on echolocation <strong>in</strong> <strong>bats</strong> (Myotis lucifugus); studies on vision <strong>in</strong><br />
<strong>bats</strong> (Myotis l.and Eptesicus fuscus); and quantative studies on vision <strong>in</strong> owls (Tyto alba pract<strong>in</strong>cola).<br />
PhD-thesis, Cornell University, Ithaca, NY<br />
Dalquest, W. W. 1957. Observations on the sharp-nosed bat, Rhynconycteris naso (Maximilian).<br />
Texas. J. Sci. 9, 219-226<br />
Davis, R. 1966. Hom<strong>in</strong>g performance and hom<strong>in</strong>g ability <strong>in</strong> <strong>bats</strong>. Ecol. Monogr. 36, 201-237<br />
Davis, W. H.. & Barbour, R. W. 1965. The use of vision <strong>in</strong> flight by the bat Myotis sodalis. Am.<br />
Midl. Nat. 74, 497-499<br />
Davis, W. H. & Barbour, R. W. 1970. Hom<strong>in</strong>g <strong>in</strong> bl<strong>in</strong>ded <strong>bats</strong> (Myotis sodalis). J. Mammal. 51, 182-<br />
184<br />
Dietrich, C. E. & Dodt, E. 1970. Structural and some physiological f<strong>in</strong>d<strong>in</strong>gs on the ret<strong>in</strong>a of the bat<br />
Myotis myotis. Symp. Electroret<strong>in</strong>ography (ed. A. Wirth). Pac<strong>in</strong>i, Pisa, 120-132<br />
40
Dyer, F. C. & Gould, J. L. 1981. Honey bee orientation: a backup system for cloudy days. Science<br />
214, 1041-1042<br />
Eisentraut, M. 1950. Dressurvessuche zur festellung e<strong>in</strong>es optischen orientierungsvermögens der<br />
fledermmäuse. Vere<strong>in</strong>. Vaterl. Naturk. Im Vurttemberg, Stuttgart. 106, 34-45<br />
Eklöf, J. & Jones, G. 2003 (Paper I). Use of vision <strong>in</strong> prey detection by brown long-eared <strong>bats</strong>,<br />
Plecotus auritus. Anim. Behav. (In Press)<br />
Eklöf, J., Tranefors, T. and Vazquez, L. B. 2002 (Paper V). Precedence of visual cues <strong>in</strong> the<br />
emballonurid bat Balantiopteryx plicata. Mamm. Biol. 67, 42-46<br />
Eklöf, J., Svensson, A. M. & Rydell. J. 2002 (Paper II). Northern <strong>bats</strong> (Eptesicus nilssonii) use<br />
vision but not flutter-detection when search<strong>in</strong>g for prey <strong>in</strong> clutter. Oikos 99, 347-351<br />
Ell<strong>in</strong>s, S. R. 1970. The role of vision <strong>in</strong> the sensory orientation of the echolocat<strong>in</strong>g bat, Myotis<br />
lucifugus. Thesis, Newark, Del.<br />
Ell<strong>in</strong>s, S. R. & Masterson, F. A. 1974. Brightness discrim<strong>in</strong>ation thresholds <strong>in</strong> the bat, Eptesicus<br />
fuscus. Bra<strong>in</strong>, Behav. Evol. 9, 248-263<br />
Erkert, H. G. 1982. Ecological Aspects of Bat Activity Rythms. In: Ecology of Bats (Kunz, T. H.<br />
ed.). Plenum Press, New York, pp 201-242<br />
Faegri, K. & Pijl, L. van der 1979. The pr<strong>in</strong>ciples of poll<strong>in</strong>ation ecology. Pergamon, Oxford<br />
Farnworth, E. G. 1973. Flash<strong>in</strong>g behaviour, ecology and systematics of the Jamaican lampyrid<br />
fireflies. Ph.D. Dissertation, Univ. Of Florida, Ga<strong>in</strong>esville<br />
Fenton, M. B. 1975. Observations on the biology of some Rhodesian <strong>bats</strong>, <strong>in</strong>clud<strong>in</strong>g a key to the<br />
Chiroptera of Rhodesia. Life Sci. Contr. R. Ont. Mus. 104, 1-27<br />
Fenton, M. B. 2001. Bats. Checkmark Books, NY.<br />
Fenton, M. B., Audet, D., Obrist, M. K. & Rydell, J. 1995. Signal strength, tim<strong>in</strong>g, and selfdeafen<strong>in</strong>g:<br />
the evolution of echolocation <strong>in</strong> <strong>bats</strong>. Paleobiology 21, 229-242<br />
Fiedler, J. 1979. Prey catch<strong>in</strong>g with and without echolocation <strong>in</strong> the Indian false vampire bat<br />
(Megaderma lyra). Behav. Ecol. Sociobiol. 6, 155-160<br />
Flem<strong>in</strong>g, T. H. 1988. The short-tailed fruit bat, a study <strong>in</strong> plant-animal <strong>in</strong>teractions. The University of<br />
Chicago Press, Chicago and London, pp 365<br />
Fullard, J. H. 1987. Sensory ecology and neuroethology of moths and <strong>bats</strong>: <strong>in</strong>teractions <strong>in</strong> a global<br />
perspective. In: Recent advances <strong>in</strong> the study of <strong>bats</strong> (Fenton, M. B, Racey, P. A. & Rayner, J. M. V.<br />
eds.). Cambridge University Press, Cambridge, pp 244-272<br />
Goodw<strong>in</strong>, G. G. & Greenhal, A. M. 1961. A review of the <strong>bats</strong> of Tr<strong>in</strong>idad and Tobago. Bull. Amer.<br />
Mus. Nat. Hist. 122, 3<br />
Grant, J. D. A. 1991. Prey location by two Australian long-eared <strong>bats</strong>, Nyctophilus gouldi and N.<br />
geoffroyi. - Australian J. Zool. 39, 45-56<br />
Greenway, F. & Hutson, A. M. 1990. A field guide to British <strong>bats</strong>. Bruce Coleman Books, Oyster<br />
books Ltd, Somerset<br />
Griff<strong>in</strong>, D. R. 1970. Migration and hom<strong>in</strong>g of <strong>bats</strong>. In: Biology of Bats, Vol. II. (Wimsatt, W. A ed.),<br />
Academic Press, NY pp 233-264<br />
41
Heffner, R. S. 1997. Comparative study of sound localization and its anatomical correlates <strong>in</strong><br />
mammals. Acta Otolaryngol Suppl. 532, 46-53<br />
Heffner, R. S. & Heffner, H. E. 1992. Visual Factors <strong>in</strong> Sound Localization <strong>in</strong> Mammals. J. Comp.<br />
Neurobiology 317, 219-232<br />
Heffner, R. S., Koay, G. & Heffner, H. E. 1999. Sound localization <strong>in</strong> an old-world fruit bat,<br />
(Rousettus aegyptiacus): Acuity, use of b<strong>in</strong>aural cues, and relationship to vision. J. Comp. Psych.113,<br />
297-306<br />
Heffner, R. S., Koay, G. & Heffner, H. E. 2001. Sound localization <strong>in</strong> a new-world frugivorous bat,<br />
Artibeus jamaicensis: Acuity, use of b<strong>in</strong>aural cues, and relationship to vision. J. Acoust. Soc. Am.<br />
109, 412-421<br />
Helversen, O. von., W<strong>in</strong>kler, L. & Bestmann, H. J. 2000. Sulphur-conta<strong>in</strong><strong>in</strong>g "perfumes" attract<br />
flower-visit<strong>in</strong>g <strong>bats</strong>. J. Comp. Physiol. A. 186, 143-153<br />
Hessel, K. & Schmidt, U. 1994. Multimodal orientation <strong>in</strong> Carollia perspicillata (Phyllostomidae).<br />
Folia Zoologica 43, 339-346<br />
Honkavaara, J., Koivula, M., Korpimäki, E., Siitari, H. & Viitala, J. 2002. Ultraviolet vision and<br />
forag<strong>in</strong>g <strong>in</strong> terrestrial vertebrates. Oikos 98, 505-511<br />
Hope, G. M. & Bhatnagar, K. P. 1979a. Electrical responses of bat ret<strong>in</strong>as to spectral stimulation:<br />
comparisons of four microchiropteran species. Experentia 35, 1189-1191<br />
Hope, G. M. & Bhatnagar, K. P. 1979a. Effect on light adaptation on electrical responses on the<br />
ret<strong>in</strong>a of four species of <strong>bats</strong>. Experentia 35, 1191-1192<br />
Hopk<strong>in</strong>s, H. C. 1984. Floral biology and poll<strong>in</strong>ation ecology of the neotropical species of Parkia. J.<br />
Ecology 72, 1-23<br />
Hughes, A. 1977. The topography of vision <strong>in</strong> mammals of contrast<strong>in</strong>g life<br />
style: Comparative optics and ret<strong>in</strong>al organisation. In: Handbook of sensory<br />
physiology vol VII/5. The visual system <strong>in</strong> vertebrates (Crescitelli, F. Ed.).<br />
Spr<strong>in</strong>ger-Verlag, Berl<strong>in</strong>, pp. 613-756.<br />
Höller, P. 1995. Orientation by the Bat Phyllostomus discolor (Phyllostomidae) on the Return Flight<br />
to its Rest<strong>in</strong>g Place. Ethology 100, 72-83<br />
Höller, P. & Schmidt, U. 1996. The orientation behaviour of the lesser spearnosed bat, Phyllostomus<br />
discolor (Chiroptera) <strong>in</strong> a model roost. J. Comp. Physiol. A. 179, 245-254<br />
Jacobs, G. H., Neitz, J. & deegan, ll. 1991. Ret<strong>in</strong>al receptors <strong>in</strong> rodents maximally sensitive to<br />
ultraviolet light. Nature 353, 544-554<br />
Jensen, M. E., Miller, L. A. and Rydell, J. 2001. Detection of prey <strong>in</strong> clutter by the northern bat,<br />
Eptesicus nilssonii. J. Exp. Biol. 204, 199-208<br />
Joermann, G., Schmidt, U. and Schmidt, C. 1988. The mode of orientation dur<strong>in</strong>g flight and approach<br />
to land<strong>in</strong>g <strong>in</strong> two Phyllostomid <strong>bats</strong>. Ethology 78, 332-340<br />
Jolicoeur, P. & Baron, G. 1980. Bra<strong>in</strong> Center Correlations among Chiroptera. Bra<strong>in</strong> Behav. Evol. 17,<br />
419-431<br />
Kalko, E. K. V. 1995. Echolocation signal design, forag<strong>in</strong>g habitats and guild structure <strong>in</strong> six<br />
Neotropical sheath-tailed <strong>bats</strong> (Emballonuridae). In: Ecology, evolution and behaviour of <strong>bats</strong><br />
(Racey, P. A. & Swift, S. M. eds.). Symp. Zool. Soc. Lond. 67, 259-273<br />
42
Kalko, E. K. V & Schnitzler, H. U. 1993. The echolocation and hunt<strong>in</strong>g behavior of Daubenton’s bat,<br />
Myotis daubentoni. Behav. Ecol. Sociobiol. 24, 225-238<br />
Kalko, E. K. V., Herre, E. A. & Handley Jr, C. O. 1996. Relation of fig fruit characteristics to fruiteat<strong>in</strong>g<br />
<strong>bats</strong> <strong>in</strong> the New and Old world tropics. J. Biogeography 23, 565-576<br />
Karlsson, B-L., Eklöf, J. & Rydell, J. 2001 (Paper VI). No lunar phobia <strong>in</strong> swarm<strong>in</strong>g <strong>in</strong>sectivorous<br />
<strong>bats</strong> (family Vespertilionidae). J. Zool. Lond. 256, 473-477<br />
Kevan, P. G., Chittka, L. & Dyer, A. G. 2001. Limits to the salience of ultraviolet: lessons from<br />
colour vision <strong>in</strong> bees and birds. J. Exp. Biol. 204, 2571-2580<br />
Kick, S. 1982. Target-detection by the echolocat<strong>in</strong>g bat, Eptesicus fuscus. J. Comp. Physiol. A 145,<br />
432-435<br />
Koay, G., Kearns, D., Heffner, H. E. & Heffner, R. S. 1998. Passive sound-localization ability of the<br />
big brown bat (Eptesicus fuscus). Hear<strong>in</strong>g Research 119, 37-48<br />
Kulzer, E., Nelson, J. E., McKean, J. L. & Möhres, F. P. 1984. Prey catch<strong>in</strong>g behaviour and<br />
echolocation <strong>in</strong> the Australian ghost bat, Macroderma gigas (Microchiroptera: Megadermatidae).<br />
Aust. Mammal. 7: 37-50<br />
Kürten, L. & Schmidt, U. 1982. Thermo-perception <strong>in</strong> the common vampire bat (Desmodus<br />
rotundus). J. Comp. Physiol. A 146, 223-228<br />
Lang, A. B., Kalko, E. K. V., Dechmann, D. K. N. & Bockholdt, C. 2002. Associations of lunarcorrelated<br />
activity rythms of Neotropical Katydids with activity patterns of the glean<strong>in</strong>g <strong>in</strong>sectivorous<br />
Round-eared bat, Tonatia silvicola. Abstract 32 nd NASBR, p 58<br />
Laska, M. 1990. Olfactory sensitivity to food odor components <strong>in</strong> the short-tailed fruit bat, Carollia<br />
perspicillata (Phyllostomatidae, Chiroptera). J. Comp. Physiol. A 166, 395-399<br />
Lawrence, B. D. & Simmons, J. A. 1982. Measurements of atmospheric attenuation at ultrasonic<br />
frequencies and the significance for echolocation by <strong>bats</strong>. J. Acoust. Soc. Amer. 71, 585-590<br />
Layne, J. N. 1967. Evidence for the use of vision <strong>in</strong> diurnal orientation of the bat Myotis<br />
austroriparius. Anim. Behav. 15, 409-415<br />
Lekagul, B. & McNeely, J. A. 1977. Mammals of Thailand. Assoc. Consev. Wildlife, Bangkok<br />
Limpens, H. J. G. A. & Kapteyn, K. 1991. Bats, their behaviour and l<strong>in</strong>ear landscape elements.<br />
Myotis 29, 39-48<br />
Lloyd, J. E. 1989. Bat (Chiroptera) connections with firefly (Coleoptera: Lampyridae) lum<strong>in</strong>escence,<br />
I: Potential significance, historical evidence, and opportunity. The Coleopterists Bullet<strong>in</strong>, 83-91<br />
Lopez, J. W<strong>in</strong>ter, Y. & Helversen, O. von 2001. Behavioural measurements of spectral sensitivity <strong>in</strong><br />
a flower visit<strong>in</strong>g bat (Glossophaga soric<strong>in</strong>a). Abstracts 12 th International Bat research Conference,<br />
Bangi, Selangor, Malaysia, pp 58<br />
Manske, U. & Schmidt, U. 1976. Visual acuity of the vampire bat, Desmodus rotundus, and its<br />
dependence upon light <strong>in</strong>tensity. Z. Tierpsychol. 42, 215-221<br />
Manske, U. & Schmidt, U. 1979. Untersuchungen zur optischen Musterunterscheidung bei der<br />
Vampirfledermaus, Desmodus rotundus. Z. Tierpsychol. 49, 120<br />
Marks, J. M. 1980. Ret<strong>in</strong>al ganglion cell topography <strong>in</strong> <strong>bats</strong>. MA thesis. Bloom<strong>in</strong>gton, IN: Indiana<br />
Univ.<br />
43
Masterson, F. A. & Ell<strong>in</strong>s, S. R. 1974. The role of vision <strong>in</strong> the orientation of the echolocat<strong>in</strong>g bat,<br />
Myotis lucifugus. Behaviour LI, 1-2, 88-98<br />
McIlwa<strong>in</strong>, J. T. 1996. An <strong>in</strong>troduction to the biology of vision. Cambridge University Press,<br />
Cambridge<br />
McWilliam, A. N. 1987. Territorial and pair behaviour of the African false vampire bat,<br />
Cardioderma cor (Chiroptera: Megadermatidae), <strong>in</strong> coastal Kenya. J. Zool. Lond. 213, 243-252<br />
Mistry, S. 1990. Characteristics of the visually guided escape response of the Mexican free-tailed bat,<br />
Tadarida brasiliensis mexicana. Anim. Behav. 39, 314-320<br />
Morrison, D. W. 1978. Lunar phobia <strong>in</strong> a neotropical fruit bat, Artibeus jamaicensis (Chiroptera,<br />
Phyllostomidae). Anim. Behav. 26, 852-855<br />
Mueller, H. C. 1968. The role of vision <strong>in</strong> vespertilionid <strong>bats</strong>. Am. Midl. Nat. 79, 524-525<br />
Nagel, T. 1974. What is it like to be a bat? Phil. Rev. 83, 535-450<br />
Neuweiler, G. 1967. Interaction of other sensory systems with the sonar system. In: Les Systemes<br />
Sonars Animaux Biologie et Bionique (ed. Busnel, R. G.). Nato Adv. Study Inst. Frascati, pp 509-<br />
533<br />
Neuweiler, G. 2000. The biology of <strong>bats</strong>. Oxford university Press, NY<br />
Neuweiler, G. & Möhres, F. P. 1966. The role of spatial memory <strong>in</strong> the orientation. In: Les Systemes<br />
Sonars Animaux Biologie et Bionique (ed. Busnel, R. G.). Nato Adv. Study Inst. Frascati, pp 129-<br />
140<br />
Pack, A. A. & Herman, L. M. 1995. Sensory <strong>in</strong>tegration <strong>in</strong> the bottlenosed dolph<strong>in</strong>: Immediate<br />
recognition of complex shapes across the senses of echolocation and vision. J. Acoust. Soc. Am. 98,<br />
722-733<br />
Pentney, R. P. & Cotter, J. R. 1976. Ret<strong>in</strong>ofugal projections <strong>in</strong> an echolocat<strong>in</strong>g bat. Bra<strong>in</strong> Research<br />
115, 479-484<br />
Pettigrew, J. D. 1980. Microbat vision and echolocation <strong>in</strong> an evolutionary context. In: Nachtigall, P.<br />
E. and Moore, P. W. B. (eds.), Animal Sonar. Processes and Performance. New York, Plenum Press,<br />
pp 645-650<br />
Pettigrew, J. D. 1986. Fly<strong>in</strong>g primates? Mega-<strong>bats</strong> have the advanced pathway from eye to midbra<strong>in</strong>.<br />
Science 231, 1304-1306<br />
Pettigrew, J. D. 1988. Microbat vision and echolocation <strong>in</strong> an evolutionary context. NATO ASI<br />
Series A Life Sciences 156, 645-650<br />
Pettigrew, J. D., Coles, R. B., Guppy, A., Brown, M. & Nelson, J. 1983. Sensory abilities of the<br />
Australian ghost bat, Macroderma gigas. Neurosci. Letts. Suppl. 11, 568<br />
Pettigrew, J. D. Baker, G. B., Baker-Gabb, D., Baverstock, G., Coles, R., Conole, L., Churchill, S.,<br />
Fitzherbert, K., Guppy, A., Hall, L., Helman, P., Nelson, J., Priddel, D., Pulsford, I., Richards, G.,<br />
Schulz, M. & Tidemann, C. R. 1986. The Australian ghost bat, Macroderma gigas, at P<strong>in</strong>e Creek,<br />
Northern territory. Macroderma 2, 10-19<br />
Pettigrew, J. D., Dreher, B., Hopk<strong>in</strong>s, C. S. McCall, M. J. & Brown, M. 1988. Peak density and<br />
distribution of ganglion cells <strong>in</strong> the ret<strong>in</strong>ae of microchiropteran <strong>bats</strong>: Implications for visual acuity.<br />
Bra<strong>in</strong> Behav. Evol. 32, 39-56<br />
44
Racey, P. A. & Swift, S. M. 1985. Feed<strong>in</strong>g ecology of Pipistrellus pipistrellus dur<strong>in</strong>g pregnancy and<br />
lactation. I. Forag<strong>in</strong>g behaviour. J. Anim. Ecol. 54, 205-215<br />
Reimer, K. 1989. Ret<strong>in</strong>ofugal projections <strong>in</strong> the rufous horseshoe bat, Rh<strong>in</strong>olophus rouxi. Anat.<br />
Embryol. 180, 89-98<br />
Rother, G. & Schmidt, U. 1982. Der e<strong>in</strong>fluss visueller <strong>in</strong>formation auf die Echoortung bei<br />
Phyllostomus discolor (Chiroptera). Z. Zäugertierkunde 47, 324-334<br />
Ryan, J. & Tuttle, M. D. 1987. The role of prey-generated sounds, vision, and echolocation <strong>in</strong> prey<br />
localization by the African bat Cardioderma cor (Megadermatidae). J. Comp. Physiol. A 161, 59-66<br />
Rydell, J. 1992a. Exploitation of <strong>in</strong>sects around street lamps by <strong>bats</strong> <strong>in</strong> Sweden. Funct. Ecol. 6, 744-<br />
750<br />
Rydell, J. 1992b. Occurrence of <strong>bats</strong> <strong>in</strong> northernmost Sweden (65°N) and their feed<strong>in</strong>g ecology <strong>in</strong><br />
summer. J. Zool. Lond. 227, 517-529<br />
Rydell, J. 1998. Bat defence <strong>in</strong> lekk<strong>in</strong>g ghost swift (Hepialus humuli), a moth without ultrasonic<br />
hear<strong>in</strong>g. Proc. R. Soc. Lond. B 265, 1373-1376<br />
Rydell, J., Parker McNeill, D. & Eklöf, J. 2002. Capture success of little brown <strong>bats</strong> feed<strong>in</strong>g on<br />
mosquitoes. J. Zool. Lond. 256, 379-381<br />
Ryer, A. 1997. Light measurement handbook. International Light, Newburyport, MA.<br />
Schmidt, U. 1988. Orientation and sensory functions <strong>in</strong> Desmodus rotundus. In: Natural history of<br />
vampire <strong>bats</strong> (Greenhall, A. M. & Schmidt, U. eds.) CRC Press, Inc. Boca Raton Florida, pp 143-166<br />
Schmidt, U. & Manske, U. 1978. Visual pattern discrim<strong>in</strong>ation <strong>in</strong> the vampire bat, Desmodus<br />
rotundus. Congressus Theriologicus Internationalis 2, 59<br />
Schmidt, U., Joermann, G. & Rother, G. 1988. Acoustical vs. visual orientation <strong>in</strong> neotropical <strong>bats</strong>.<br />
In: Animal Sonar (Nachtigall, P. E. & Moore, P. W. B. eds.), Plenum Publish<strong>in</strong>g Corporation, pp<br />
589-593<br />
Schnitzler, H. U. & Gr<strong>in</strong>nell, A. D. 1977a. Directional sensitivity of echolocation <strong>in</strong> the horse shoe<br />
bat, Rh<strong>in</strong>olophus ferrumequ<strong>in</strong>um. I. Directionality of sound emission. J. Comp. Physiol. 116, 51-61<br />
Schnitzler, H. U. & Gr<strong>in</strong>nell, A. D. 1977b. Directional sensitivity of echolocation <strong>in</strong> the horse shoe<br />
bat, Rh<strong>in</strong>olophus ferrumequ<strong>in</strong>um. II. Behavioral directionality of hear<strong>in</strong>g. J. Comp. Physiol. 116, 63-<br />
76<br />
Simmons, N. B. & Geisler, J. H. 1998. Phyloge<strong>net</strong>ic relationships of Icaronycteris, Archaeonycteris,<br />
Hassianycteris, and Palaeochiropteryx to extant bat l<strong>in</strong>eages, with comments on the evolution and<br />
forag<strong>in</strong>g strategies <strong>in</strong> Microchiroptera. Bull. Amer. Mus. Nat. Hist. 235<br />
Spr<strong>in</strong>ger, M. S., Teel<strong>in</strong>g, E. & Stanhope, M. J. 2001. External nasal cartilages <strong>in</strong> <strong>bats</strong>: Evidence for<br />
Microchiropteran monophyly? J. Mamm. Evol. 8, 231-236<br />
Ste<strong>in</strong>, B. E. & Meredith, A. 1993. The merg<strong>in</strong>g of the senses. The MIT Press, Cambridge, MA<br />
Suthers, R. A. 1966. Optomotor responses by echolocat<strong>in</strong>g <strong>bats</strong>. Science 152, 1102-1104<br />
Suthers, R. A. 1970. <strong>Vision</strong>, olfaction and taste. In: Biology of Bats Vol. II (Wimsatt, W. A. ed.).<br />
Academic Press, New York, pp 265-281<br />
Suthers, R. A. & Bradford, M. R. 1980. Visual systems and the evolutionary relationships of the<br />
Chiroptera. Proc. 5th Int. Bat. Res. Conf. 331-346<br />
45
Suthers, R. A. & Chase, J. 1966. Visual pattern discrim<strong>in</strong>ation by an echolocat<strong>in</strong>g bat. Amer. Zool. 6,<br />
573<br />
Suthers, R. A. & Wallis, N. E. 1970. Optics of the eyes of echolocat<strong>in</strong>g <strong>bats</strong>. J. <strong>Vision</strong> Res. 10, 1165-<br />
1173<br />
Suthers, R. A., Chase, J. & Bradford, B. 1969. Visual form discrim<strong>in</strong>ation by echolocat<strong>in</strong>g <strong>bats</strong>. Biol.<br />
Bull. 137, 535-546<br />
Swift, S. M. 1998. Long-eared <strong>bats</strong>. T & AD Poyser Natural History. London<br />
Test, F. H. 1967. Indicated use of sight <strong>in</strong> navigation by molossid <strong>bats</strong>. J. Mamm. 48, 482-483<br />
Thomson, C. E. 1982. Myotis sodalis. Mammalian species 163, 1-5<br />
Timm, R. M. 1989. Migration and molt patterns of red <strong>bats</strong>, Lasiurus borealis (Chiroptera:<br />
Vespertilionidae). Ill<strong>in</strong>ois. Bull. Chic. Acad. Sci. 14, 1-7<br />
Usman, K., Habersetzer, R., Subbaraj, R., Gopalkrishnaswamy, G. & Paramandam, K. 1980.<br />
Behaviour of <strong>bats</strong> dur<strong>in</strong>g a lunar eclipse. Behav. Ecol. Sociobiol. 7, 79-80<br />
Varass<strong>in</strong>, I. G., Trigo, J. R. & Sazima, M. 2001. The role of nectar production, flower pigments and<br />
odour <strong>in</strong> the poll<strong>in</strong>ation of four species of Passiflora (Passifloraceae) <strong>in</strong> south-eastern Brazil. Bot. J.<br />
L<strong>in</strong>n. Soc. 136, 139-152<br />
Vaughan, T. A. & Vaughan, R. P. 1986. Seasonality and the behaviour of the African yellow-w<strong>in</strong>ged<br />
bat. J. Mamm. 67, 91-102<br />
Verboom, B. & Huitema, H. 1997. The importance of l<strong>in</strong>ear landscape elements for the pipistrelle<br />
Pipistrellus pipistrellus and the serot<strong>in</strong>e bat Eptesicus serot<strong>in</strong>us. Landscape Ecology 12 (2), 117-125<br />
Verboom, B., Boonman, A. M. & Limpens, H. J. G. A. 1999. Acoustic perception of landscape<br />
elements by the pond bat (Myotis dasycneme) J. Zool. Lond. 248, 59-66<br />
Vernon, C. L. 1981. The use of vision <strong>in</strong> prey selection by the Big brown bat, Eptesicus fuscus.<br />
Master thesis, the University of Wiscons<strong>in</strong>-Milwaukee<br />
Wallace, M. T. & Ste<strong>in</strong>, B. E. 2001. Sensory and multisensory responses <strong>in</strong> the newborn monkey<br />
superior colliculus. J. Neurosci. 21, 8886-8898<br />
Whitt<strong>in</strong>gton, D. A., Hepp-Raymond, M. C. & Flood, W. 1981. Eye and head movements to auditory<br />
targets. Exp. Bra<strong>in</strong> Res. 41, 358-363<br />
Wilk<strong>in</strong>son, G. S. 1986. Social groom<strong>in</strong>g <strong>in</strong> the vampire bat, Desmodus rotundus. Anim. Behav. 34,<br />
1880-1889<br />
Williams, T. C. & Williams, J. M. 1967. Radiotrack<strong>in</strong>g of hom<strong>in</strong>g <strong>bats</strong>. Science 155, 1435-1436<br />
Williams, T. C., Williams, J. M. & Griff<strong>in</strong>, D. R. 1966. Hom<strong>in</strong>g ability of the neotropical bat<br />
Phyllostomus hastatus. Anim. Behav. 14, 468-473<br />
Willson, M. F. & Whelan, C. J. 1989. Ultraviolet reflectance of fruits of vertebrate-dispersed plants.<br />
Oikos 55, 341-348<br />
Wiltschko, W. & Wiltschko, R. 1995. Mag<strong>net</strong>ic orientation <strong>in</strong> animals. Spr<strong>in</strong>ger-Verlag, Berl<strong>in</strong><br />
46
”Love looks not with the eyes,<br />
but with the m<strong>in</strong>d; and therefore<br />
is w<strong>in</strong>ged Cupid pa<strong>in</strong>ted bl<strong>in</strong>d”<br />
- William Shakespeare<br />
48<br />
I
Animal Behaviour – In Press<br />
Use of vision <strong>in</strong> prey detection by brown long-eared <strong>bats</strong> Plecotus auritus<br />
JOHAN EKLÖF 1 & GARETH JONES 2<br />
1 Zoology Department, Göteborg University, Sweden<br />
2 School of Biological Sciences, University of Bristol, UK<br />
Eklöf & Jones, Use of vision <strong>in</strong> Plecotus auritus<br />
Correspondence<br />
Johan Eklöf, Zoology Department, Göteborg University, Box 463, SE-405 30<br />
Göteborg, Sweden. E-mail: johan.eklof@zool.gu.se<br />
Gareth Jones, School of Biological Sciences, University of Bristol, Woodland<br />
Road, Bristol BS8 1UG, UK<br />
ABSTRACT<br />
We <strong>in</strong>vestigated the ability of brown long-eared <strong>bats</strong> (Plecotus auritus) to make<br />
use of visual cues when search<strong>in</strong>g for food. By us<strong>in</strong>g petri dishes conta<strong>in</strong><strong>in</strong>g<br />
mealworms that were subjected to different levels of illum<strong>in</strong>ation, we presented<br />
four <strong>bats</strong> with different sensory cues: visual cues, sonar cues and a comb<strong>in</strong>ation<br />
of these. The <strong>bats</strong> preferred situations where both sonar cues and visual cues<br />
were available, and the visual <strong>in</strong>formation was more important than the sonar<br />
cues. The <strong>bats</strong> did, however, emit echolocation calls throughout the experiments.<br />
50
Microchiropteran <strong>bats</strong> use echolocation for orientation, and often for prey<br />
detection, and can thus operate <strong>in</strong> darkness and under unpredictable light<strong>in</strong>g<br />
(Griff<strong>in</strong> 1958). However, as high frequency sounds attenuate quickly <strong>in</strong> air, and<br />
limit the echolocation range (Kick 1982; Kalko & Schnitzler 1993; Fenton et al.<br />
1995), sonar cannot be effectively used for detection of small targets over long<br />
distances. Also, for echolocat<strong>in</strong>g <strong>bats</strong> forag<strong>in</strong>g close to vegetation, separation of<br />
prey from the background clutter (echoes from objects other than the target of<br />
<strong>in</strong>terest) is usually problematic (Schnitzler & Kalko1998; Arlettaz et al. 2001;<br />
Jensen et al. 2001). Therefore, some <strong>bats</strong> use for example prey-generated sounds<br />
(Ryan & Tuttle 1987; Arlettaz et al. 2001) and smell (Thies et al. 1998) as<br />
additional cues when search<strong>in</strong>g for prey. Few studies have addressed the<br />
possibility that visual cues may also be important for detection of prey. The<br />
aerial hawk<strong>in</strong>g northern bat (Eptesicus nilssonii: Vespertilionidae), is guided by<br />
visual cues when search<strong>in</strong>g for the large and conspicuously white ghost swifts<br />
Hepialus humuli (Lepidoptera), hover<strong>in</strong>g among high grass (clutter) at dusk<br />
(Eklöf et al. 2002). Other aerial hawk<strong>in</strong>g <strong>bats</strong>, such as Craseonycteris<br />
thonglongyai (Emballonuridae) might potentially use visual cues by mak<strong>in</strong>g use<br />
of the bright sky, aga<strong>in</strong>st which <strong>in</strong>sects are seen as silhouettes (Pettigrew 1980).<br />
The California leaf-nosed bat (Macrotus californicus) uses a glean<strong>in</strong>g forag<strong>in</strong>g<br />
tactic, and catches prey from the ground. This species is the only bat so far<br />
shown to be capable of catch<strong>in</strong>g prey by us<strong>in</strong>g vision alone (Bell 1985).<br />
The brown long-eared bat Plecotus auritus is also a glean<strong>in</strong>g bat,<br />
that sometimes takes <strong>in</strong>sects from leaves (Swift 1998). This means that it faces<br />
the problems of detect<strong>in</strong>g prey <strong>in</strong> a cluttered environment. Its echolocation calls<br />
are fa<strong>in</strong>t and short FM (frequency modulated) sweeps (Ahlén 1981; Parsons &<br />
Jones 2000) which may be an adaptation for forag<strong>in</strong>g close to vegetation or,<br />
alternatively, may be used only for spatial orientation (Arlettaz et al. 2001).<br />
Passive listen<strong>in</strong>g plays a major role for detect<strong>in</strong>g the prey <strong>in</strong> the long-eared bat<br />
(Anderson & Racey 1991). The ears are large and the hear<strong>in</strong>g is exceptionally<br />
sensitive to sounds around 15 kHz, close to the frequencies emitted by <strong>in</strong>sects<br />
mov<strong>in</strong>g <strong>in</strong> clutter (Coles et al. 1989).<br />
Plecotus auritus also has relatively big eyes compared to many<br />
other <strong>in</strong>sectivorous <strong>bats</strong> (Cranbrook 1963), suggest<strong>in</strong>g that these <strong>bats</strong> also have<br />
relatively good vision. Eisentraut (1950) was able to tra<strong>in</strong> brown long-eared <strong>bats</strong><br />
to discrim<strong>in</strong>ate between black and white 9-cm square shaped cards, but when he<br />
presented the <strong>bats</strong> with a circle and a cross they failed to make the right choice.<br />
This <strong>in</strong>dicates that P. auritus can discrim<strong>in</strong>ate between different targets by us<strong>in</strong>g<br />
vision, but not different patterns. This is <strong>in</strong> contrast to some phyllostomid <strong>bats</strong><br />
(Suthers & Chase 1966; Suthers et al. 1969), which show more sophisticated<br />
discrim<strong>in</strong>ation of patterns. However, Eisentraut’s experiments were carried out<br />
<strong>in</strong> bright light, and as subsequently shown by several authors, microchiropteran<br />
vision works better <strong>in</strong> dim ambient light (i.e. dusk and dawn illum<strong>in</strong>ation) than <strong>in</strong><br />
bright daylight (Bradbury & Nottebohm 1969; Ell<strong>in</strong>s & Masterson 1974; Hope &<br />
Bhatnagar 1979).<br />
The aim of this study is to <strong>in</strong>vestigate if brown long eared <strong>bats</strong><br />
use visual cues <strong>in</strong> addition to sonar cues when search<strong>in</strong>g for prey. Its large eyes<br />
and glean<strong>in</strong>g forag<strong>in</strong>g behaviour suggest that this may be the case. We quantified<br />
51
the ability of brown long eared <strong>bats</strong> to f<strong>in</strong>d prey by us<strong>in</strong>g vision alone; i.e. to f<strong>in</strong>d<br />
prey on dark and dimly illum<strong>in</strong>ated backgrounds and also beh<strong>in</strong>d a transparent<br />
surface.<br />
METHODS<br />
The study was conducted <strong>in</strong> the School of Biological Sciences at Bristol<br />
University, UK. Four female Plecotus auritus were captured at their roost<br />
(Ilm<strong>in</strong>ster, Somerset) 23 April, and released at capture site 12 May 2002. They<br />
were kept <strong>in</strong> a 2.2m x 3m x 3m flight room, where also the experiments took<br />
place. The room had ventilation <strong>in</strong>stalled and the <strong>bats</strong> could move around freely<br />
and they had several places to hide, <strong>in</strong>clud<strong>in</strong>g boxes and pieces of cloths on the<br />
walls. The <strong>bats</strong> were fed on mealworms with vitam<strong>in</strong> supplements. They were<br />
fed by hand the first day, presented with bowls conta<strong>in</strong><strong>in</strong>g mealworms the<br />
second day, and could feed by themselves from the bowls from day three. Water<br />
was given <strong>in</strong> the same k<strong>in</strong>d of bowls and was available to the <strong>bats</strong> on the flight<br />
room floor all the time (and changed twice every day). The temperature of the<br />
room was 13-16° C, except dur<strong>in</strong>g the experiments, when it was 20° C. The<br />
daylight period was partly reversed (lights on at 03:00 and off at 16:00) with<br />
experiments start<strong>in</strong>g at ca. 18:00. All the <strong>bats</strong> lost a little weight (0.5 - 1g) dur<strong>in</strong>g<br />
the first two days, but on the day of release, they all had their orig<strong>in</strong>al weight<br />
except one that had ga<strong>in</strong>ed 1g.<br />
Experiment 1<br />
Two halogen light sources (Schott) with two fibre-optic goose necks each were<br />
placed on the floor <strong>in</strong> the flight room. At the end of each goose neck, we attached<br />
plastic tubes, two of them with neutral density light filters (reduc<strong>in</strong>g light<br />
<strong>in</strong>tensity with 50%), and the other two with dark covers (lett<strong>in</strong>g no light<br />
through). This set-up provided us with two circular 25-cm diameter areas of dim<br />
light (4 lux; measured with a Gossen Mavolux digital light meter) and two<br />
similar “areas of darkness” (0.2 lux), 30-40cm apart on the flight room floor. The<br />
overall illum<strong>in</strong>ation <strong>in</strong> the room never exceeded 0.1 lux. The plastic tubes on the<br />
fibre-optic goose necks could be switched and, hence, the arrangement of the lit<br />
and dark areas could be changed. On the floor; under each goose neck we put a<br />
petri dish (9 cm diameter, 1.8 cm deep), placed <strong>in</strong>side the lid belong<strong>in</strong>g to it,<br />
either with mealworms <strong>in</strong> the petri dish itself or <strong>in</strong> the lid (hence between lid and<br />
dish). This provided four different comb<strong>in</strong>ations of sensory cues.<br />
1: lit area with mealworms <strong>in</strong> the dish (visual and sonar cues).<br />
2: lit area with mealworms placed <strong>in</strong> the lid (visual cues only)<br />
3: dark area with mealworms <strong>in</strong> the dish (sonar cues only).<br />
4: dark area with mealworms <strong>in</strong> the lid (no cues except from the dish itself).<br />
We assume that acoustical cues aris<strong>in</strong>g from the mealworms mov<strong>in</strong>g <strong>in</strong> the<br />
dishes or the lids were the same <strong>in</strong> all cases.<br />
Dur<strong>in</strong>g the experiment the <strong>bats</strong> were fly<strong>in</strong>g <strong>in</strong>dividually <strong>in</strong> the<br />
flight room for 30-40 m<strong>in</strong>utes, feed<strong>in</strong>g from the petri dishes. Each land<strong>in</strong>g at a<br />
52
dish was recorded as a forag<strong>in</strong>g attempt, and as soon as a land<strong>in</strong>g was recorded<br />
the arrangement of the feed<strong>in</strong>g situation was changed. To prevent the <strong>bats</strong> from<br />
us<strong>in</strong>g spatial memory the experimental area was divided <strong>in</strong> two parts (A & B),<br />
which were used alternately, so that a forag<strong>in</strong>g attempt <strong>in</strong> area A was followed<br />
by an experiments <strong>in</strong> area B. The light sources could be placed at four different<br />
positions with<strong>in</strong> each area, and the positions were changed at random after each<br />
feed<strong>in</strong>g attempt. Also the arrangement of the four petri dishes (present<strong>in</strong>g the<br />
different sensory cues) was changed at random after each feed<strong>in</strong>g attempt.<br />
Hence, <strong>in</strong> total there were 32 potential positions for each petri dish.<br />
An <strong>in</strong>fra red sensitive video camera (Sony M<strong>in</strong>i DV TRV9E<br />
Handycam) with a wide-angle lens was placed above the experimental area. It<br />
was connected to a monitor placed outside the flight room and thus mak<strong>in</strong>g it<br />
possible to survey the experiments without disturb<strong>in</strong>g the <strong>bats</strong>.<br />
In order to test if the probability of a feed<strong>in</strong>g attempt at a certa<strong>in</strong><br />
dish was the same for all <strong>bats</strong>, i.e. if we could treat the <strong>bats</strong> as one group, we<br />
applied a Chi square test of homogeneity (test<strong>in</strong>g if a specific distribution is the<br />
same <strong>in</strong> different situations, <strong>in</strong> this case for the different bat <strong>in</strong>dividuals). Then<br />
we made pair-wise comparisons between dish preferences, i.e. we compared the<br />
probability that one dish was preferred over another. We did so by us<strong>in</strong>g 95%<br />
confidence <strong>in</strong>tervals, i.e. <strong>in</strong>tervals hav<strong>in</strong>g 95% probability of cover<strong>in</strong>g our<br />
estimated preferences (number of captures <strong>in</strong> each category divided by total<br />
number of captures) for the different feed<strong>in</strong>g dishes. As we calculated several<br />
<strong>in</strong>tervals us<strong>in</strong>g the same data set, we applied the Bonferroni method for multiple<br />
comparisons.<br />
Experiment 2<br />
To exclude the possibility that the <strong>bats</strong> considered the light or the petri dishes<br />
rather than the actual prey items as potential food sources, we presented the <strong>bats</strong><br />
with two lit areas, one with a petri dish conta<strong>in</strong><strong>in</strong>g mealworms, and one with an<br />
empty dish. The set-up was similar to the one <strong>in</strong> experiment 1, although only one<br />
light source (with two goose necks) was used, and this time all four <strong>bats</strong> were<br />
fly<strong>in</strong>g simultaneously. We also placed a bat detector (Ultra Sound Advice S-25<br />
set <strong>in</strong> frequency-division mode) next to one of the petri dishes, and connected it<br />
to a speaker outside the flight room. The different positions of the light source<br />
and the arrangement of the two petri dishes together with the position of the bat<br />
detector, were changed after each feed<strong>in</strong>g attempt and randomised <strong>in</strong> a similar<br />
manner as <strong>in</strong> experiment 1. This experiment was also surveyed us<strong>in</strong>g an IR<br />
sensitive video camera. The number of feed<strong>in</strong>g attempts at the two petri dishes<br />
was compared us<strong>in</strong>g Chi square statistics, and echolocation calls from feed<strong>in</strong>g<br />
<strong>bats</strong> were noted.<br />
53
General observations<br />
RESULTS<br />
When released <strong>in</strong> the flight room, the <strong>bats</strong> typically flew across the feed<strong>in</strong>g area<br />
a few times before decid<strong>in</strong>g from which dish to feed. They usually hovered just<br />
above one of the dishes (10 – 15 cm) for a short period and then landed next to it.<br />
The <strong>bats</strong> then crawled <strong>in</strong>to the dish to feed. On a few occasions, <strong>bats</strong> crawled<br />
around the feed<strong>in</strong>g area on the floor to <strong>in</strong>vestigate the different dishes. After<br />
capture of a mealworm, the <strong>bats</strong> consumed it while hang<strong>in</strong>g on one of the walls<br />
<strong>in</strong> the flight room. Bats mov<strong>in</strong>g around consistently emitted detectable<br />
echolocation calls.<br />
Experiment 1<br />
The number of feed<strong>in</strong>g attempts and estimates of preference at the different<br />
dishes are presented <strong>in</strong> table 1. We found no significant differences between bat<br />
<strong>in</strong>dividuals <strong>in</strong> their probability of feed<strong>in</strong>g at a certa<strong>in</strong> dish (? 2 9 = 7.94, p>0.05).<br />
This means that we do not ga<strong>in</strong> any statistically significant <strong>in</strong>formation by<br />
treat<strong>in</strong>g the <strong>in</strong>dividuals separately, and we therefore pooled the results.<br />
When compar<strong>in</strong>g the number of feed<strong>in</strong>g attempts between each<br />
of the four forag<strong>in</strong>g situations (data and statistics <strong>in</strong> tab. 1 and 2), we found that<br />
<strong>in</strong> lit situations, it made no difference if sonar cues were added or not. However,<br />
there were more feed<strong>in</strong>g attempts when sonar cues and visual cues were present,<br />
compared to when only sonar cues were available. This suggests that the <strong>bats</strong><br />
predom<strong>in</strong>antly used vision when they searched for prey.<br />
When compar<strong>in</strong>g the frequency of forag<strong>in</strong>g attempts at situations<br />
provid<strong>in</strong>g visual or sonar cues only, the <strong>bats</strong> scored better at the visual cues, and<br />
when compar<strong>in</strong>g sonar cues only to the no cue situation, we found no significant<br />
difference. This analysis too suggests that the <strong>bats</strong> predom<strong>in</strong>antly relied on<br />
vision and it also suggests that they could not f<strong>in</strong>d prey items us<strong>in</strong>g sonar alone.<br />
Experiment 2<br />
There were significantly more feed<strong>in</strong>g attempts at lit petri dishes conta<strong>in</strong><strong>in</strong>g<br />
mealworms than at lit empty ones (? 2 1 = 7.7, p
DISCUSSION<br />
We found that long-eared <strong>bats</strong> are capable of visual detection of prey, at least<br />
under the light <strong>in</strong>tensity of 4 lux, and that they prefer visual cues to sonar cues if<br />
given a choice. The results also <strong>in</strong>dicate that the <strong>bats</strong> were unable to detect the<br />
prey items us<strong>in</strong>g sonar alone.<br />
There is both experimental and observational evidence that<br />
echolocat<strong>in</strong>g <strong>bats</strong> make use of vision and even give precedence to visual stimuli<br />
<strong>in</strong> some situations, <strong>in</strong>clud<strong>in</strong>g long distance orientation (Griff<strong>in</strong> 1970), detection<br />
of landmarks (Davis 1966), obstacle avoidance (Bradbury & Nottebohm 1969)<br />
and prey detection (Bell 1985). When select<strong>in</strong>g an escape route <strong>in</strong> an<br />
experimental set-up, the phyllostomid Anoura geoffroyi used visual cues alone<br />
and disregarded acoustical cues that also were provided (Chase 1981, 1983). The<br />
observation that <strong>bats</strong> have a tendency to crash <strong>in</strong>to w<strong>in</strong>dows of build<strong>in</strong>gs when<br />
released <strong>in</strong>doors (Fenton 1975) or dur<strong>in</strong>g natural migration (Timm 1989) also<br />
suggests that they predom<strong>in</strong>antly rely on vision rather than on echolocation <strong>in</strong><br />
situations when both acoustic and visual cues are available. The performance is<br />
greatly improved (i.e. fewer crashes) when the <strong>bats</strong> are bl<strong>in</strong>ded (Davis &<br />
Barbour 1965) or when fly<strong>in</strong>g under natural dark conditions, and hence are<br />
“forced” to rely on echolocation (Eklöf et al. 2002). Suthers and Wallis (1970)<br />
studied the eyes of two species of Vespertilionidae (Myotis sodalis and<br />
Pipistrellus subflavus) and four different phyllostomids (Desmodus rotundus,<br />
Carollia perspicillata, Anoura geoffroyi and Phyllostomus hastatus), and<br />
concluded that the visual capabilities of all the species tested would allow the<br />
<strong>bats</strong> to see well beyond the range of echolocation. Due to the more or less<br />
spherical lenses, it also follows that Microchiroptera has a short focal distance<br />
and hence a great depth of focus (Suthers & Wallis 1970). In fact,<br />
microchiropteran <strong>bats</strong> seem to be farsighted, <strong>in</strong>dicat<strong>in</strong>g that vision is used<br />
preferably over longer distances, where it may not overlap with echolocation,<br />
which is a short-range operation (Kick 1982; Fenton et al. 1995). Nevertheless<br />
there are some <strong>bats</strong>, such as Phyllostomus hastatus, which also use vision with<strong>in</strong><br />
the range covered by their echolocation system, i.e. when approach<strong>in</strong>g a land<strong>in</strong>g<br />
spot (Joermann et al. 1988).<br />
We cannot exclude the possibility that the <strong>bats</strong> used passive<br />
listen<strong>in</strong>g to detect the mealworms, as some other glean<strong>in</strong>g <strong>bats</strong> do (Arlettaz et al.<br />
2001). Sounds com<strong>in</strong>g from the prey could have been detected from any of the<br />
dishes, <strong>in</strong>clud<strong>in</strong>g the dishes with visual cues only and the no cue situation, as live<br />
mealworms were crawl<strong>in</strong>g under the petri dishes (<strong>in</strong> the lids). Also olfactory cues<br />
from the mealworms may have been available to the <strong>bats</strong> <strong>in</strong> all four feed<strong>in</strong>g<br />
situations. Hence, olfactory cues and prey-generated sounds may expla<strong>in</strong> some<br />
of the feed<strong>in</strong>g attempts at petri dishes with prey <strong>in</strong> the lids.<br />
Dur<strong>in</strong>g the experiments, <strong>bats</strong> were sometimes seen hover<strong>in</strong>g at<br />
positions where no petri dish was available, but where dishes had been available<br />
previously, presumably rely<strong>in</strong>g on spatial memory (Neuweiler & Möhres 1966;<br />
Grant 1991; Höller & Schmidt 1996). Hence, the <strong>bats</strong> tended to revisit positions<br />
where they previously had been rewarded and it seems possible that the results<br />
55
are <strong>in</strong>fluenced to some extent by this. However, we believe that our experimental<br />
design, where the position of the dishes were changed after every feed<strong>in</strong>g<br />
attempt, would m<strong>in</strong>imise these effects, and that the results show preference for<br />
feed<strong>in</strong>g dishes, rather than spatial memory.<br />
The results of Experiment 2 allowed rejection of the hypothesis<br />
that <strong>bats</strong> associated structural features of the food dish with reward, and were<br />
therefore attracted to features of the dishes by associative learn<strong>in</strong>g (Siemers<br />
2001). However, as all the <strong>bats</strong> flew simultaneously <strong>in</strong> this experiment, we<br />
cannot exclude the possibility that some <strong>in</strong>dividuals sometimes explored the<br />
dishes without gett<strong>in</strong>g a reliable <strong>in</strong>dication of reward. In the first experiment<br />
there were equally many feed<strong>in</strong>g attempts at the petri dishes provid<strong>in</strong>g sonar<br />
cues as at the no cue dishes, which means that we found no <strong>in</strong>dication that the<br />
<strong>bats</strong> could detect the prey items by us<strong>in</strong>g sonar alone. One can therefore<br />
hypothesize that <strong>bats</strong> hav<strong>in</strong>g to rely exclusively on sonar may learn to recognize<br />
structures rather than prey.<br />
There were more feed<strong>in</strong>g attempts at the petri dishes provid<strong>in</strong>g<br />
visual cues only compared to those that provided sonar cues only. This suggests<br />
that the long-eared <strong>bats</strong> were capable of f<strong>in</strong>d<strong>in</strong>g prey visually and that they even<br />
preferred us<strong>in</strong>g vision when possible. Long-eared <strong>bats</strong> emerge from their roosts<br />
late <strong>in</strong> the even<strong>in</strong>g (15-55 m<strong>in</strong>utes after sunset depend<strong>in</strong>g on the latitude; Swift<br />
1998), which means that they normally operate <strong>in</strong> very low light levels (
ACKNOWLEDGEMENTS<br />
We wish to acknowledge Marc Holderied and Julian Partridge for comments on<br />
the experimental design and Jens Rydell for comments on the manuscript. We<br />
also wish to thank John Gustafsson and Catr<strong>in</strong> Bergqvist for statistical advice.<br />
The study was supported by ”Stiftelsen Paul och Marie Berghaus<br />
donationsfond”, and ”Adlerbertska forskn<strong>in</strong>gsstiftelsen” (JE). Research was<br />
performed under licence from English Nature.<br />
REFERENCES<br />
Ahlén, I. 1981. Identification of Scand<strong>in</strong>avian <strong>bats</strong> by their sounds. Uppsala:<br />
Swedish University of Agricultural Sciences, Department of Wildlife Ecology.<br />
Anderson, M. E. & Racey, P. A. 1991. Feed<strong>in</strong>g behaviour of captive long<br />
eared-<strong>bats</strong>, Plecotus auritus. Animal Behaviour, 42, 489-493<br />
Arlettaz, R., Jones, G. & Racey, P. A. 2001. Effect of acoustic clutter on prey<br />
detection by <strong>bats</strong>. Nature, 414, 742-745.<br />
Bell, G. P. 1985. The sensory basis of prey location by the California leaf-nosed<br />
bat Macrotus californicus (Chiroptera: Phyllostomidae). Behavioral Ecology and<br />
Sociobiology, 16, 343-347.<br />
Bell, G. P. & Fenton, M. B. 1986. Visual acuity, sensitivity and b<strong>in</strong>ocularity <strong>in</strong><br />
a glean<strong>in</strong>g <strong>in</strong>sectivorous bat, Macrotus californicus (Chiroptera:<br />
Phyllostomidae). Animal Behaviour, 34, 409-414.<br />
Bradbury, J. & Nottebohm, F. 1969. The use of vision by the little brown bat,<br />
Myotis lucifugus, under controlled conditions. Animal Behaviour, 17, 480-485.<br />
Chase, J. 1981.Visually guided escape responses of microchiropteran <strong>bats</strong>.<br />
Animal Behaviour, 29, 708- 713.<br />
Chase, J. 1983. Differential responses to visual and acoustic cues dur<strong>in</strong>g escape<br />
<strong>in</strong> the bat Anoura geoffroyi: cue preferences and behaviour. Animal Behaviour,<br />
31, 526-531.<br />
Coles, R. B., Guppy, A., Anderson, M. E. & Schlegel, P. 1989. Frequency<br />
sensitivity and directional hear<strong>in</strong>g <strong>in</strong> the glean<strong>in</strong>g bat, Plecotus auritus (L<strong>in</strong>naeus<br />
1758). Journal of Comparative Physiology A, 165, 269-280.<br />
Cranbrook, The Earl of. 1963. Notes on the feed<strong>in</strong>g habits of the long-eared<br />
bat. Transaction of Suffolk Natural History Society, 11, 1-3.<br />
Davis, R. 1966. Hom<strong>in</strong>g performance and hom<strong>in</strong>g ability <strong>in</strong> <strong>bats</strong>. Ecological<br />
Monographs, 36, 201-237.<br />
Davis, R. & Barbour, R. W. 1965. The use of vision <strong>in</strong> flight by the bat Myotis<br />
sodalis. The American Midland Naturalist, 74, 497-499.<br />
Eisentraut, M. 1950. Dressurvessuche zur festellung e<strong>in</strong>es optischen<br />
orientierungsvermögens der fledermmäuse. Vere<strong>in</strong> für Vaterländische<br />
Naturkunde In Vürttemberg, Stuttgart, 106, 34-45.<br />
57
Eklöf, J., Tranefors, T. & Vazquez, L. B. 2002. Precedence of visual cues <strong>in</strong><br />
the emballonurid bat Balantiopteryx plicata. Mammalian Biology, 67, 42-46.<br />
Eklöf, J., Svensson, A. M. & Rydell, J. 2002. Northern <strong>bats</strong> (Eptesicus<br />
nilssonii) use vision but not flutter-detection when search<strong>in</strong>g for prey <strong>in</strong> clutter.<br />
Oikos, 99, 347-351.<br />
Ell<strong>in</strong>s, S. R. & Masterson, F. A. 1974. Brightness discrim<strong>in</strong>ation thresholds <strong>in</strong><br />
the bat, Eptesicus fuscus. Bra<strong>in</strong>, Behaviour and Evolution, 9, 248-263.<br />
Fenton, M. B. 1975. Observations on the biology of some Rhodesian <strong>bats</strong>,<br />
<strong>in</strong>clud<strong>in</strong>g a key to the Chiroptera of Rhodesia. Life Science Contributions of the<br />
Royal Ontario Museum, 104, 1-27.<br />
Fenton, M. B., Audet, D., Obrist, M. K. & Rydell, J. 1995. Signal strength,<br />
tim<strong>in</strong>g, and self-deafen<strong>in</strong>g: the evolution of echolocation <strong>in</strong> <strong>bats</strong>. Paleobiology,<br />
21 (2), 229-242.<br />
Grant, J. D. A. 1991. Prey location by two Australian long-eared <strong>bats</strong>,<br />
Nyctophilus gouldi and N. geoffroyi. - Australian Journal of Zoology, 39, 45-56.<br />
Griff<strong>in</strong>, D. R. 1958. Listen<strong>in</strong>g <strong>in</strong> the Dark. New haven: Yale University Press.<br />
Griff<strong>in</strong>, D. R. 1970. Migration and hom<strong>in</strong>g of <strong>bats</strong>. In: Biology of Bats, Vol. II.<br />
(Ed. By W. A. Wimsatt), pp. 233-264. New York, Academic Press.<br />
Hope, G. M. & Bhatnagar, K. P. 1979. Effect on light adaptation on electrical<br />
responses on the ret<strong>in</strong>a of four species of <strong>bats</strong>. Experentia, 35, 1191-1192.<br />
Höller, P. & Schmidt, U. 1996. The orientation behaviour of the lesser<br />
spearnosed bat, Phyllostomus discolor (Chiroptera) <strong>in</strong> a model roost. Journal of<br />
Comparative Physiology A, 179, 245-254.<br />
Jensen, M. E., Miller, L. A. and Rydell, J. 2001. Detection of prey <strong>in</strong> clutter by<br />
the northern bat, Eptesicus nilssonii. Journal of Experimental Biology, 204, 199-<br />
208.<br />
Joermann, G., Schmidt, U. and Schmidt, C. 1988. The mode of orientation<br />
dur<strong>in</strong>g flight and approach to land<strong>in</strong>g <strong>in</strong> two Phyllostomid <strong>bats</strong>. Ethology, 78,<br />
332-340.<br />
Kalko, E. K. V. & Schnitzler, H.-U. 1993. Plasticity of echolocation signals of<br />
European pipistrelle <strong>bats</strong> <strong>in</strong> search flight: implications for habitat use and prey<br />
detection. Behavioral Ecology and Sociobiology, 33, 415-428.<br />
Kick, S. 1982. Target-detection by the echolocat<strong>in</strong>g bat, Eptesicus fuscus.<br />
Journal of Comparative Physiology A, 145, 432-435<br />
Land, M. F. & Nilsson, D. E. 2002. Animal Eyes. Oxford Animal Biology<br />
Series. Oxford University Press.<br />
Marks, J. M. 1980. Ret<strong>in</strong>al ganglion cell topography <strong>in</strong> <strong>bats</strong>. MA thesis, Indiana<br />
University, Bloom<strong>in</strong>gton.<br />
Neuweiler, G. & Möhres, F. P. 1966. The role of spatial memory <strong>in</strong> the<br />
orientation. In: Les Systemes Sonars Animaux Biologie et Bionique (Ed. by R. G.<br />
Busnel), pp. 129-140. Frascati: NATO Advanced Study Institute.<br />
Parsons, S. & Jones, G. 2000. Acoustic identification of twelve species of<br />
echolocat<strong>in</strong>g bat by discrim<strong>in</strong>ant function analysis and artificial neural <strong>net</strong>works.<br />
Journal of Experimental Biology, 203, 2641-2656.<br />
Pettigrew, J. D. 1980. Microbat vision and echolocation <strong>in</strong> an evolutionary<br />
context. In: Animal Sonar. Processes and Performance (Ed. by P. E. Nachtigall<br />
& P. W. B. Moore), pp. 645-650. New York: Plenum Press.<br />
58
Pettigrew, J. D., Dreher, B., Hopk<strong>in</strong>s, C. S. McCall, M. J. & Brown, M.<br />
1988. Peak density and distribution of ganglion cells <strong>in</strong> the ret<strong>in</strong>ae of<br />
microchiropteran <strong>bats</strong>: Implications for visual acuity. Bra<strong>in</strong>, Behaviour and<br />
Evolution, 32, 39-56.<br />
Ryan, J. & Tuttle, M. D. 1987. The role of prey-generated sounds, vision, and<br />
echolocation <strong>in</strong> prey localization by the African bat Cardioderma cor<br />
(Megadermatidae). Journal of Comparative Physiology A, 161, 59-66<br />
Schnitzler, H.-U. & Kalko, E.K.V. 1998. How echolocat<strong>in</strong>g <strong>bats</strong> search and<br />
f<strong>in</strong>d food. In: Bat Biology and Conservation (Ed. by T. H. Kunz & P. A. Racey),<br />
pp. 183-204. Wash<strong>in</strong>gton D.C.: Smithsonian Institution Press.<br />
Siemers, B.M. 2001. F<strong>in</strong>d<strong>in</strong>g prey by associative learn<strong>in</strong>g <strong>in</strong> glean<strong>in</strong>g <strong>bats</strong>:<br />
experiments with a Natterer’s bat Myotis nattereri. Acta Chiropterologica, 3,<br />
211-215.<br />
Suthers, R. A. & Chase, J. 1966. Visual pattern discrim<strong>in</strong>ation by an<br />
echolocat<strong>in</strong>g bat. American Zoologist, 6, 573<br />
Suthers, R. A., Chase, J. & Bradford, B. 1969. Visual form discrim<strong>in</strong>ation by<br />
echolocat<strong>in</strong>g <strong>bats</strong>. Biological Bullet<strong>in</strong>, 137, 535-546.<br />
Suthers, R. A. & Wallis, N. E. 1970. Optics of the eyes of echolocat<strong>in</strong>g <strong>bats</strong>.<br />
Journal of <strong>Vision</strong> Research, 10, 1165-1173<br />
Swift, S. M. 1998. Long-eared <strong>bats</strong>. London: T & AD Poyser Natural History.<br />
Thies, W., Kalko, E. K. V & Schnitzler, H-U. 1998. The roles of echolocation<br />
and olfaction <strong>in</strong> two neotropical fruit-eat<strong>in</strong>g <strong>bats</strong>, Carollia perspicillata and C.<br />
castanea feed<strong>in</strong>g on piper. Behavioral Ecology and Sociobiology, 42, 397-409<br />
Timm, R. M. 1989. Migration and molt patterns of red <strong>bats</strong>, Lasiurus borealis<br />
(Chiroptera: Vespertilionidae). Ill<strong>in</strong>ois Bullet<strong>in</strong> of the Chicago Academy of<br />
Sciences, 14, 1-7.<br />
Vaughan, T. A. & Vaughan, R. P. 1986. Seasonality and the behaviour of the<br />
African yellow-w<strong>in</strong>ged bat. Journal of Mammalogy, 67 (1), 91-102<br />
59
Table 1. – The number of feed<strong>in</strong>g attempts and mean proportions of attempts at<br />
petri dishes provid<strong>in</strong>g four <strong>in</strong>dividuals of Plecotus auritus with different sensory<br />
cues.<br />
sensory cue bat # 1 bat # 2 bat # 3 bat # 4 total mean proportion<br />
visual only 12 27 11 17 67 0.34<br />
visual/sonar 16 21 14 21 72 0.38<br />
sonar only 13 10 5 7 35 0.18<br />
none 3 8 3 6 20 0.10<br />
total 44 66 33 51 194 1.0<br />
60
Table 2. – Pair-wise differences between mean proportions of attempts made to<br />
dishes provid<strong>in</strong>g different sensory cues, with 95% Bonferroni-corrected<br />
confidence <strong>in</strong>tervals for each difference. If a confidence <strong>in</strong>terval <strong>in</strong>cludes zero,<br />
the <strong>bats</strong> were equally likely to make feed<strong>in</strong>g attempts at the two types of dish.<br />
Sensory cue comparison Confidence <strong>in</strong>terval preferred dish<br />
p(visual cues) – p(visual/sonar cues) -0.04±0.17 no preference<br />
p(visual cues) – p(sonar cues) 0.16±0.14 visual<br />
p(visual/sonar cues) – p(sonar cues) 0.20±0.14 visual/sonar<br />
p(visual cues) – p(no cue) 0.24±0.12 visual<br />
p(visual/sonar cues) – p(no cue) 0.27±0.13 visual/sonar<br />
p(sonar cues) – p(no cue) 0.08±0.10 no preference<br />
61
“The Eocene brought<br />
mammals mean<br />
And <strong>bats</strong> began to s<strong>in</strong>g;<br />
Their food they found by<br />
ultrasound<br />
And chased it on the w<strong>in</strong>g.”<br />
- John D Pye<br />
62<br />
II
“You can't depend on your<br />
eyes when your imag<strong>in</strong>ation<br />
is out of focus”<br />
- Mark Twa<strong>in</strong><br />
III<br />
70
Submitted manuscript<br />
<strong>Vision</strong> complements echolocation <strong>in</strong> an aerial-hawk<strong>in</strong>g bat<br />
Jens Rydell and Johan Eklöf<br />
Zoology Department, Göteborg University, Box 463, SE 405 30 Göteborg,<br />
Sweden.<br />
Correspond<strong>in</strong>g author:<br />
Johan Eklöf, address as above<br />
Tel. +46-317733666<br />
Fax. +46-31416729<br />
E-mail: johan.eklof@zool.gu.se<br />
Abstract<br />
The northern bat Eptesicus nilssonii hawks fly<strong>in</strong>g <strong>in</strong>sects <strong>in</strong> the air us<strong>in</strong>g<br />
frequency-modulated echolocation calls. It is known to detect and catch visually<br />
conspicuous prey (white moths) hover<strong>in</strong>g low among grass stalks. To overcome<br />
the problem with acoustic clutter from the grass that <strong>in</strong>terferes with target echo<br />
detection, the <strong>bats</strong> made use of visual cues <strong>in</strong> addition to those of echolocation.<br />
However, vision <strong>in</strong>creased the chance of detection only when the moths were at<br />
least 5 cm <strong>in</strong> w<strong>in</strong>gspan. Smaller targets were detected us<strong>in</strong>g echolocation alone.<br />
The mean detection range was 3.5 m, which suggests a visual acuity of 49´ of<br />
arc. This is consistent with results of optomotor response tests and counts of<br />
ret<strong>in</strong>al ganglion cells <strong>in</strong> closely related species. The results suggest that vision <strong>in</strong><br />
Eptesicus <strong>bats</strong> is not sufficiently sharp for prey detection under normal<br />
conditions but only when the prey is unusually large and conspicuous.<br />
Nevertheless, the northern bat shows flexibility <strong>in</strong> prey-detection techniques not<br />
previously recognised among aerial-hawk<strong>in</strong>g <strong>bats</strong>.<br />
Key words: acoustic clutter, Hepialidae, <strong>in</strong>sectivorous <strong>bats</strong>, nocturnality,<br />
ultrasound, visual acuity.<br />
72
Introduction<br />
Functions normally served by vision <strong>in</strong> most vertebrates have been taken over by<br />
ultrasonic echolocation <strong>in</strong> <strong>in</strong>sectivorous <strong>bats</strong>. In particular, the detection and<br />
track<strong>in</strong>g of fly<strong>in</strong>g <strong>in</strong>sects is usually believed to be entirely acoustic (Kalko &<br />
Schnitzler 1993). Ultrasonic echolocation allows detection of very small targets,<br />
but its practical range is normally limited to a few metres, which is due to severe<br />
atmospheric attenuation and spread<strong>in</strong>g loss of high-frequency sound and the poor<br />
reflective power of targets as small as <strong>in</strong>sects (Lawrence & Simmons 1982, Kick<br />
1982). On the other hand, although the eyes of <strong>in</strong>sectivorous <strong>bats</strong> are small, they<br />
generally have good light-gather<strong>in</strong>g capacity and good focal depth (Suthers<br />
1970, Suthers & Wallis 1970). <strong>Vision</strong> can therefore be assumed to provide<br />
important cues particularly at ranges beyond that of echolocation, and is<br />
presumably useful for orientation and navigation at night.<br />
However, adaptation of the visual system for nocturnal conditions occurs<br />
partly at the expense of acuity, the ability to resolve details, and this presumably<br />
limits the use of vision for some short-range purposes such as f<strong>in</strong>d<strong>in</strong>g prey<br />
(Suthers 1970). Nevertheless, at least some bat species, particularly those that<br />
glean prey from surfaces and for which acoustic clutter (background echoes)<br />
makes echolocation less useful (Arlettaz et al. 2001), have a visual acuity that is<br />
good enough for detection of <strong>in</strong>sects and other objects at close range (Bell 1985,<br />
Joermann et al. 1988).<br />
We recently discovered that vision also plays a role <strong>in</strong> prey detection by the<br />
northern bat Eptesicus nilssonii (Family Vespertilionidae), an aerial-hawk<strong>in</strong>g<br />
species (Eklöf et al. 2002). However, because aerial-hawk<strong>in</strong>g <strong>bats</strong> generally<br />
seem to have poor visual acuity (Suthers 1970), this can be expected to set a<br />
lower limit to the size of <strong>in</strong>sects that can be detected by vision.<br />
Experimental sett<strong>in</strong>g and methods<br />
To determ<strong>in</strong>e the visual acuity for E. nilssonii forag<strong>in</strong>g under practical<br />
conditions <strong>in</strong> the field, we took advantage of a natural situation where <strong>bats</strong><br />
regularly exploit groups of male ghost swift moths Hepialus humuli (Hepialidae)<br />
display<strong>in</strong>g over hayfields dur<strong>in</strong>g midsummer even<strong>in</strong>gs <strong>in</strong> southern Sweden<br />
(57°N). These moths are silvery white and highly reflective on the dorsal side<br />
and display visually <strong>in</strong> hover<strong>in</strong>g flight among the grass panicles to attract<br />
females (Andersson et al. 1998). Hepialids are unusual among larger moths <strong>in</strong><br />
that they are earless and do not show any evasive response to bat echolocation<br />
calls, whether these are natural or synthetic (Rydell 1998).<br />
At two different moth display sites, each regularly patrolled simultaneously<br />
by up to 10 northern <strong>bats</strong> (which were not marked), we added dead and spread<br />
<strong>in</strong>dividuals to the naturally display<strong>in</strong>g moth population. The dead moths were<br />
glued on top of steel wires and presented pair wise about 2 m apart and 0.5-0.7 m<br />
above the grass <strong>in</strong> various parts of the fields. One moth <strong>in</strong> a pair had its white<br />
73
(dorsal) side up and the other had its dark grey (ventral) side up towards the<br />
patroll<strong>in</strong>g <strong>bats</strong>. We assumed that the two were equally detectable by echolocation<br />
but that the white moth was more detectable by vision. This assumption was<br />
based on a previous experiment, show<strong>in</strong>g that the moths´ silvery white<br />
coloration, which also conta<strong>in</strong>s a UV-component, is particularly contrast<strong>in</strong>g<br />
dur<strong>in</strong>g their natural display time just after sunset and aga<strong>in</strong>st a background of<br />
green grass (Andersson et al. 1998). We thus expected the white and the dark<br />
moth to be attacked with equal frequency if <strong>bats</strong> use echolocation alone but with<br />
unequal frequency if they also use visual cues. To determ<strong>in</strong>e the m<strong>in</strong>imum size<br />
of moths detectable by vision, we presented pairs of moths (one white and one<br />
dark) which were either <strong>in</strong>tact (ca. 6 cm w<strong>in</strong>gspan; Eklöf et al. 2002) or where<br />
both had the w<strong>in</strong>gtips cut to give a total w<strong>in</strong>gspan of either 5, 4 or 3 cm. Hence,<br />
size differed between the pairs of moths but the white and the dark moth that<br />
formed a pair were always of the same size. The moths were replaced when<br />
destroyed by the <strong>bats</strong>, but otherwise reused as long as possible.<br />
To prevent the <strong>bats</strong> from learn<strong>in</strong>g the exact positions of the moths, the pairs<br />
were moved at least a few metres follow<strong>in</strong>g each attack by a bat. Hence each pair<br />
of moths was attacked only once while <strong>in</strong> each position. We deliberately<br />
presented the moths at a height where the <strong>bats</strong>´ echolocation would be<br />
complicated by clutter from the grass, overlapp<strong>in</strong>g with echoes from the moths,<br />
so that the <strong>bats</strong> were encouraged to use visual cues to f<strong>in</strong>d the moths. The extent<br />
of the ”clutter overlap zone”, which depends on the duration of the echolocation<br />
calls (7-8 ms), was 0.6-1.2 m above the grass (Jensen et al. 2001).<br />
Moths and <strong>bats</strong> were observed visually and also acoustically with a Pettersson<br />
D-940 bat detector from a distance of 2-10 m. The visual observations were<br />
facilitated by the relatively good light conditions prevail<strong>in</strong>g at 57°N around<br />
midsummer (June 2002), which always made it possible to see what happened <strong>in</strong><br />
sufficient detail. The experiments were performed only as long as moths were<br />
display<strong>in</strong>g naturally nearby, which occurred for about 30 m<strong>in</strong>utes each even<strong>in</strong>g<br />
(Andersson et al. 1998).<br />
Results<br />
Neither <strong>bats</strong> nor moths showed any obvious response to our presence. The <strong>bats</strong><br />
seemed to forage normally, perhaps because they had become habituated to our<br />
presence over several seasons. The <strong>bats</strong> typically patrolled <strong>in</strong> large circles over<br />
the field at a height of 3-4 m (mean 3.5 m). The height was determ<strong>in</strong>ed by us<strong>in</strong>g<br />
a measured and marked lamppost at the edge of the field as a reference. The <strong>bats</strong><br />
always emitted echolocation calls dur<strong>in</strong>g the search as well as throughout the<br />
attacks on the moths. An attack<strong>in</strong>g bat typically performed a rapid and more or<br />
less vertical dive towards the grass while switch<strong>in</strong>g from search phase<br />
echolocation calls to a typical “feed<strong>in</strong>g-buzz”, i.e. short pulses and high pulse<br />
repetition rate (Jensen et al. 2001). This behaviour strongly suggests that the<br />
attacks consistently were guided by echolocation.<br />
We counted the number of attacks on white and dark moths and compared the<br />
results for each moth size us<strong>in</strong>g one-tailed chi square statistics. Attacks on white<br />
moths were more frequent than on dark moths when the moths were 5 cm or<br />
larger (Fig. 1), suggest<strong>in</strong>g that the detection was facilitated by vision <strong>in</strong> these<br />
74
cases. The detection of 4 cm and 3 cm moths were apparently not facilitated by<br />
vision and therefore must have been guided entirely by echolocation. We<br />
expected the total number of attacks on large moths to be more frequent than on<br />
smaller moths, because the larger size presumably <strong>in</strong>creased the chance of<br />
detection. Although this appeared to be the case, the absolute attack frequency<br />
(the number of attacks per bat) was difficult to measure because the number of<br />
<strong>bats</strong> search<strong>in</strong>g for moths over the field changed constantly.<br />
Discussion<br />
Because 5 cm moths were detected visually at a range of 3.5 m, the distance<br />
between the w<strong>in</strong>g tips of the moths represents 49´ of arc. This agrees very well<br />
with theoretical estimates of visual acuity based on counts of ret<strong>in</strong>al ganglion<br />
cells, suggest<strong>in</strong>g 40´ of arc (Pettigrew et al. 1998, Koay et al. 1988) and<br />
behavioural tests of the optomotor response, suggest<strong>in</strong>g at least 1° of arc, <strong>in</strong> the<br />
closely related species Eptesicus fuscus from North America (Bell & Fenton<br />
1986). Unpublished optomotor response tests of other Eptesicus species, namely<br />
E. capensis and E. zuluensis from southern Africa, suggest that these species<br />
have a visual acuity of at least 54´of arc (M. B. Fenton & C. V. Portfors,<br />
personal communication). Our experiment is the first estimate of the visual<br />
acuity of E. nilssonii.<br />
The visual acuity of Eptesicus spp. appears to be <strong>in</strong>termediate among <strong>bats</strong>. It<br />
is much better than <strong>in</strong> many other aerial-hawk<strong>in</strong>g <strong>in</strong>sectivores, e.g. Myotis spp.<br />
(3-6°) (Suthers 1966) but not as good as that of some glean<strong>in</strong>g <strong>in</strong>sectivores, e.g.<br />
Macrotus californicus and Antrozous pallidus (4´ and 15´, respectively) (Bell &<br />
Fenton 1986). It is comparable to that of vampires and frugivores of the family<br />
Phyllostomidae (42´-16´) and <strong>in</strong>sectivores of the family Emballonuridae (42´-<br />
23´) (Pettigrew et al. 1998, Suthers 1966, Manske & Schmidt 1976). Why the<br />
visual acuity differs so much among species and genera of <strong>bats</strong> is not clear.<br />
The repertoire of detection techniques used by northern <strong>bats</strong> search<strong>in</strong>g for<br />
<strong>in</strong>sects is wide. E. nilssonii usually feeds on swarm<strong>in</strong>g <strong>in</strong>sects <strong>in</strong> open air (Rydell<br />
1989), where echolocation is relatively straightforward and <strong>in</strong>sects or swarms of<br />
<strong>in</strong>sects can be detected through s<strong>in</strong>gle echoes, so called “gl<strong>in</strong>ts”. Insects that<br />
move rapidly near vegetation, so that acoustic clutter masks the echoes from the<br />
<strong>in</strong>sects, are detected through their shift <strong>in</strong> position relative to the background.<br />
This technique obviously requires comparison of the echoes conta<strong>in</strong><strong>in</strong>g both the<br />
target and the background between several successive pulses (Jensen et al. 2001).<br />
When the <strong>in</strong>sects stay among clutter and do not move relative to the background,<br />
as <strong>in</strong> the present case, few echolocation cues are available and the <strong>bats</strong><br />
apparently employ vision to enhance the detection. We have shown previously<br />
that E. nilssonii do not make use of the Doppler-effects <strong>in</strong>duced by the w<strong>in</strong>g<br />
movements of the hover<strong>in</strong>g moths (Eklöf et al. 2002).<br />
However, if vision is useful or not <strong>in</strong> a particular forag<strong>in</strong>g situation<br />
depends not only on the size of the target and the range, but presumably also on<br />
the contrast between the target and the background and the prevail<strong>in</strong>g light<br />
conditions (Andersson et al. 1998, Ell<strong>in</strong>s & Masterson 1974). In our case, the<br />
prey <strong>in</strong>sects were much larger than most other prey eaten by this species (Rydell<br />
1989) and they also displayed an unusually high contrast aga<strong>in</strong>st the background<br />
75
(Anderson et al. 1998). Hence, the use of vision for prey detection is probably<br />
unusual <strong>in</strong> this species, and we can therefore assume that it normally relies on<br />
echolocation alone for this purpose. Nevertheless, our study shows that<br />
echolocat<strong>in</strong>g <strong>bats</strong> are flexible and ready to use whatever <strong>in</strong>formation is available<br />
to f<strong>in</strong>d food, and, assum<strong>in</strong>g that the visual acuity of E. nilssonii is similar to that<br />
of E. fuscus, we f<strong>in</strong>d that these <strong>bats</strong> are able to use their full visual capacity <strong>in</strong> the<br />
field.<br />
Acknowledgements<br />
We acknowledge the landowners whose hay fields we partly devastated and T.<br />
Tranefors for practical help and M. B. Fenton and C. V. Portfors for giv<strong>in</strong>g<br />
access to unpublished data. The work was funded by the Science Research<br />
Council of Sweden.<br />
References<br />
Andersson S, Rydell J, Svensson MGE (1998) Light, predation and the lekk<strong>in</strong>g<br />
behaviour of the ghost swift Hepialus humuli (L.) (Lepidoptera:<br />
Hepialidae). Proc R Soc Lond B 265: 1345-1351<br />
Arlettaz R, Jones G & Racey PA (2001) Effect of acoustic clutter on prey<br />
detection by <strong>bats</strong>. Nature 414: 742-745<br />
Bell GP (1985) The sensory basis of prey location by the California leaf-nosed<br />
bat Macrotus californicus (Chiroptera: Phyllostomidae). Behav Ecol<br />
Sociobiol 16: 343-348<br />
Bell GP, Fenton MB (1986) Visual acuity, sensitivity and b<strong>in</strong>ocularity <strong>in</strong> a<br />
glean<strong>in</strong>g <strong>in</strong>sectivorous bat, Macrotus californicus (Chiroptera:<br />
Phyllostomidae). Anim Behav 34: 409-414<br />
Eklöf J, Svensson AM, Rydell J (2002) Northern <strong>bats</strong> (Eptesicus nilssonii) use<br />
vision but not flutter-detection when search<strong>in</strong>g for prey <strong>in</strong> clutter. Oikos<br />
99: 347-351<br />
Ell<strong>in</strong>s SR, Masterson FA (1974) Brightness discrim<strong>in</strong>ation thresholds <strong>in</strong> the bat<br />
Eptesicus fuscus. Bra<strong>in</strong> Behav Evol 9: 248-263<br />
Jensen ME, Miller LA, Rydell J (2001) Detection of prey <strong>in</strong> clutter by the<br />
northern bat, Eptesicus nilssonii. J Exp Bio 204: 199-208<br />
Joermann G Schmidt U, Schmidt C (1988) The mode of orientation dur<strong>in</strong>g flight<br />
and approach to land<strong>in</strong>g <strong>in</strong> two Phyllostomid <strong>bats</strong>. Ethology 78: 332-340<br />
Kalko EKV, Schnitzler HU (1993) Plasticity of echolocation signals of<br />
European pipistrelle <strong>bats</strong> <strong>in</strong> search flight: implications for habitat use and<br />
prey detection. Behav Ecol Sociobiol 33: 415-428<br />
Kick S (1982) Target-detection by the echolocat<strong>in</strong>g bat, Eptesicus fuscus. JComp<br />
Physiol A 145: 432-435<br />
Koay G, Kearns D, Heffner HE, Heffner RS (1998) Passive sound-localization<br />
ability of the big brown bat (Eptesicus fuscus). Hear<strong>in</strong>g Res 119: 37-48<br />
76
Lawrence BD, Simmons JA (1982) Measurements of atmospheric attenuation at<br />
ultrasonic frequencies and the significance for echolocation by <strong>bats</strong>. J<br />
Acoust Soc Am 71: 585-590<br />
Manske U, Schmidt U (1976) Untersuchungen zur optischen<br />
Musterunterscheidung bei der Vampirfledermaus, Desmodus rotundus. Z<br />
Tierpsychol 49: 120.<br />
Pettigrew JD, Dreher B, Hopk<strong>in</strong>s CS, McCall MJ, Brown M (1988) Peak<br />
density and distribution of ganglion cells <strong>in</strong> the ret<strong>in</strong>ae of<br />
microchiropteran <strong>bats</strong>: Implications for visual acuity. Bra<strong>in</strong> Behav Evol<br />
32: 39-56<br />
Rydell J (1989) Food habits of northern (Eptesicus nilssoni) and brown long-<br />
eared (Plecotus auritus) <strong>bats</strong> <strong>in</strong> Sweden. Holarct Ecol 12: 16-20<br />
Rydell J (1998) Bat defence <strong>in</strong> lekk<strong>in</strong>g ghost swift (Hepialus humuli), a moth<br />
without ultrasonic hear<strong>in</strong>g. Proc R Soc Lond B 265: 1373-1376<br />
Suthers RA (1966) Optomotor responses by echolocat<strong>in</strong>g <strong>bats</strong>. Science 152,<br />
1102-1104<br />
Suthers RA (1970) <strong>Vision</strong>, olfaction and taste. In: Wimsatt WA (ed) Biology of<br />
Bats vol. II. Academic Press, New York, pp 265-281<br />
Suthers RA, Wallis NE (1970) Optics of the eyes of echolocat<strong>in</strong>g <strong>bats</strong>. J <strong>Vision</strong><br />
Res 10: 1165-1173.<br />
77
Figure 1. - Frequency of attacks by northern <strong>bats</strong> Eptesicus nilssonii on dead and<br />
spread moths Hepialus humuli mounted on top of wires and presented to<br />
forag<strong>in</strong>g <strong>bats</strong> <strong>in</strong> a field among naturally occurr<strong>in</strong>g moths. Moths were cut to<br />
different sizes (w<strong>in</strong>gspans) and displayed pair wise, one show<strong>in</strong>g its white dorsal<br />
side up and the other the dark grey ventral side. Higher attack frequency on<br />
white than on dark moths <strong>in</strong>dicates that the <strong>bats</strong> detected the moths us<strong>in</strong>g visual<br />
cues. The asterisk <strong>in</strong>dicates that the 6 cm moths were not cut, but presented at<br />
their natural size (mean 6 cm).<br />
Attacks on moths (%)<br />
100<br />
50<br />
10<br />
n=62<br />
P
“And Bats flew round<br />
<strong>in</strong> fragrant skies<br />
and wheel'd or lit<br />
the flimsy shapes<br />
that haunt the dusk;<br />
with erm<strong>in</strong>e capes<br />
and woolly breasts,<br />
and beaded eyes.”<br />
- Alfred Tennyson<br />
IV<br />
80
Manuscript<br />
Visual acuity and eye size <strong>in</strong> four species of <strong>in</strong>sectivorous <strong>bats</strong><br />
Johan Eklöf<br />
Zoology Department, Göteborg University, Box 463, SE-405 30 Göteborg,<br />
Sweden, E-mail: johan.eklof@zool.gu.se<br />
Abstract<br />
Behavioural tests on optomotor responses establish a visual acuity threshold <strong>in</strong><br />
four species of <strong>bats</strong> of the family Vespertilionidae. Three species of Myotis spp.,<br />
which are aerial-hawk<strong>in</strong>g <strong>bats</strong>, responded only to a stripe pattern equivalent to 5<br />
degrees of arc, whereas Plecotus auritus, which is a gleaner, responded down to<br />
0.5 degrees of arc. Eye diameter was positively correlated with visual acuity, and<br />
varied from 0.9 mm <strong>in</strong> Myotis mystac<strong>in</strong>us to 1.8 mm <strong>in</strong> Plecotus auritus. These<br />
results are consistent with earlier f<strong>in</strong>d<strong>in</strong>gs. The variation <strong>in</strong> eye size and visual<br />
acuity presumably reflects differences <strong>in</strong> forag<strong>in</strong>g technique (aerial-hawk<strong>in</strong>g vs.<br />
glean<strong>in</strong>g) and, <strong>in</strong> particular, how vision is used as a complement to sonar.<br />
Key words: Chiroptera, grat<strong>in</strong>g, optomotor response, resolv<strong>in</strong>g power, spatial<br />
resolution, vision<br />
Introduction<br />
The microchiropteran eyes are generally adapted for nocturnal conditions <strong>in</strong> that<br />
they have large corneal surfaces and lenses relative to the size of the eye, and<br />
generally large receptor fields, which give them good light gather<strong>in</strong>g power at<br />
the expense of acuity, i.e. the ability to resolve f<strong>in</strong>e spatial details (Suthers 1970;<br />
Suthers & Wallis 1970). Bat eyes are generally better suited for long- than short<br />
distance operation, and due to the short effective range of sonar, vision is<br />
probably of major importance <strong>in</strong> guidance over longer distances (Griff<strong>in</strong> 1958,<br />
1970). Loss of vision drastically reduces the hom<strong>in</strong>g performance <strong>in</strong> many <strong>bats</strong><br />
(Williams et al. 1966, Hassell 1963, 1966, Davis & Barbour 1970).<br />
At least some <strong>bats</strong> are able to use vision over short distances as well, for<br />
example dur<strong>in</strong>g escape and obstacle avoidance (Chase 1981, 1983, Chase &<br />
Suthers 1969, Bradbury & Nottebohm 1969). There is also evidence that some<br />
species of <strong>bats</strong> use visual cues to f<strong>in</strong>d prey (Bell 1985, Grant 1991, Vaughan &<br />
Vaughan 1996, Eklöf et al. 2002), a task which presumably requires relatively<br />
f<strong>in</strong>e detail discrim<strong>in</strong>ation.<br />
Visual acuity has been estimated theoretically, based on counts of the number<br />
of ret<strong>in</strong>al ganglion cells, <strong>in</strong> several species of <strong>bats</strong> (Marks 1980, Pettigrew et al.<br />
1988, Heffner et al. 2001), and has shown a large range of variation; from 16’ of<br />
arc <strong>in</strong> the glean<strong>in</strong>g carnivorous species Macroderma gigas (Megadermatidae) to<br />
1.4° of arc <strong>in</strong> Rh<strong>in</strong>olophus rouxi (Rh<strong>in</strong>olophidae), an <strong>in</strong>sectivorous flutterdetector<br />
(Pettigrew et al. 1988). Optomotor response tests have also shown that<br />
82
the visual acuity varies considerably between species of <strong>bats</strong> (Suthers 1966,<br />
Manske & Schmidt 1976, Bell & Fenton 1986).<br />
The evidence thus suggests that visual acuity may be correlated with the food<br />
search<strong>in</strong>g technique among <strong>bats</strong>. In particular, gleaners seem to have better<br />
visual acuity than those that catch <strong>in</strong>sects <strong>in</strong> the air. The purpose of this study<br />
was to test this hypothesis by exam<strong>in</strong><strong>in</strong>g the optomotor response <strong>in</strong> some<br />
sympatric <strong>in</strong>sectivorous vespertilionid <strong>bats</strong> that use different forag<strong>in</strong>g techniques<br />
(glean<strong>in</strong>g and aerial-hawk<strong>in</strong>g), <strong>in</strong> order to establish a behavioural visual acuity<br />
threshold for these particular species. We also tested the assumption that visual<br />
acuity is positively related to the size of the eyes among <strong>in</strong>sectivorous <strong>bats</strong>.<br />
Materials and methods<br />
The experiments were performed at the old mag<strong>net</strong>ite m<strong>in</strong>e of Taberg, located<br />
south of Jönköp<strong>in</strong>g (57ºN) <strong>in</strong> southern Sweden. The <strong>bats</strong> were caught <strong>in</strong> a mist<br />
<strong>net</strong> set outside the m<strong>in</strong>e entrance. They were tested for optomotor responses<br />
immediately after capture or as soon they had come to rest. The tests were made<br />
outdoors <strong>in</strong> the even<strong>in</strong>g between August and November 2002, and between<br />
March and April 2003. To achieve optomotor responses, we used a device<br />
similar to that employed by Suthers (1966) and Bell & Fenton (1986). A bat was<br />
placed <strong>in</strong> a 20 cm high, 10 cm diameter Plexiglas cyl<strong>in</strong>der surrounded by a 30<br />
cm high and 60 cm diameter, revolv<strong>in</strong>g drum (Fig. 1). The natural light was<br />
<strong>in</strong>sufficient for direct observation of the response <strong>in</strong> most cases, so the study area<br />
was lit up by a 40 W light bulb placed ca. 2 m above and 5 m away from the setup.<br />
This provided a light <strong>in</strong>tensity of 0.1-0.7 lux <strong>in</strong>side the drum (Photometer<br />
IL1400A, International Light Inc.). The drum could be rotated freely and<br />
<strong>in</strong>dependently of the cyl<strong>in</strong>der conta<strong>in</strong><strong>in</strong>g the bat. S<strong>in</strong>usoidal grat<strong>in</strong>g patterns, i.e.<br />
stripes with cont<strong>in</strong>uously chang<strong>in</strong>g lum<strong>in</strong>ance from black to white, of different<br />
f<strong>in</strong>eness was attached to the <strong>in</strong>side of the drum. The drum was then rotated<br />
around the bat by hand at ca. 5 rpm randomly <strong>in</strong> both directions, and the<br />
behaviour of the bat was observed from above. Us<strong>in</strong>g s<strong>in</strong>usoidal patterns <strong>in</strong>stead<br />
of black and white stripes reduces the risk of optical illusions, which could<br />
otherwise elicit responses from the <strong>bats</strong> and thus make the results hard to<br />
<strong>in</strong>terpret (D. Nilsson & E. Warrant personal comm.). We used six grat<strong>in</strong>gs with<br />
different stripe width (distance from white to white): 2.84 cm, 1.42 cm, 0.57 cm,<br />
0.43 cm, 0.28 cm and 0.14 cm. From the <strong>bats</strong>´ po<strong>in</strong>t of view this is equivalent to<br />
subtend<strong>in</strong>g angles of 5°, 2.5°, 1°, 0.75° (45’), 0.5° (30’) and 0.25° (15’) of arc.<br />
When a response was achieved the grat<strong>in</strong>g was switched to a f<strong>in</strong>er pattern until<br />
no response could be recorded, <strong>in</strong>dicat<strong>in</strong>g that the <strong>bats</strong> no longer could resolve<br />
the pattern. At this po<strong>in</strong>t a wider pattern was re<strong>in</strong>troduced to make sure that the<br />
<strong>bats</strong> still responded to mov<strong>in</strong>g stripes. This also served as a control for responses<br />
to stimuli other than the stripes, such as noise orig<strong>in</strong>at<strong>in</strong>g from the drum.<br />
After test<strong>in</strong>g optomotor responses, we photographed the <strong>bats</strong>, us<strong>in</strong>g a Pentax<br />
645 camera, on 50 ASA medium format slide film. We held the <strong>bats</strong> by hand so<br />
that the face of the bat was perpendicular to the camera. A ruler was held next to<br />
the <strong>bats</strong>, provid<strong>in</strong>g us with a cm-scale. The photos were scanned and magnified<br />
17x – 33x, and the eye size of the <strong>in</strong>dividual <strong>bats</strong> were measured from the<br />
83
computer screen. The <strong>bats</strong> were released outside the m<strong>in</strong>e immediately after the<br />
photographs had been taken.<br />
Results<br />
Sixteen <strong>in</strong>dividual <strong>bats</strong> belong<strong>in</strong>g to four different species were caught and<br />
tested: Plecotus auritus, Myotis mystac<strong>in</strong>us, M. brandtii and M daubentonii.<br />
When tested, the <strong>bats</strong> typically moved about <strong>in</strong> the Plexiglas cyl<strong>in</strong>der for a while<br />
before com<strong>in</strong>g to rest, and they sometimes cont<strong>in</strong>ued to move around dur<strong>in</strong>g the<br />
tests. However, most <strong>bats</strong> unambiguously responded to the rotat<strong>in</strong>g stripes by<br />
mov<strong>in</strong>g their heads <strong>in</strong> a snappy, stereotyped manner, either follow<strong>in</strong>g the<br />
rotational direction or the opposite direction, as described earlier by other<br />
authors (Suthers 1966; Bell & Fenton 1986).<br />
The results were relatively consistent with<strong>in</strong> a species and genus but differed<br />
considerably between the two genera. The species of Myotis responded only to<br />
the largest pattern (5° of arc), while all the Plecotus auritus <strong>in</strong>dividuals except<br />
one responded down to the pattern equivalent to 1-0.5° of arc (Table 1).<br />
The eye size varied with visual acuity as expected (Table 1). The Myotis<br />
species had smaller eyes (ca. 1 mm diameter) than Plecotus auritus (ca. 1.7 mm).<br />
Discussion<br />
Visual acuity is highly variable among vespertilionid <strong>bats</strong>, which presumably<br />
reflects the extent to which <strong>bats</strong> of the different genera make use of vision and<br />
what they do with it. As might have been expected, the relatively big-eyed<br />
gleaner Plecotus auritus did much better than the aerial-hawk<strong>in</strong>g and trawl<strong>in</strong>g<br />
Myotis spp., which also had much smaller eyes.<br />
The reaction to the 5° but not to the 2.5° pattern by the Myotis species used <strong>in</strong><br />
this study is consistent with an earlier <strong>in</strong>vestigation of another Myotis species,<br />
the little brown bat (M. lucifugus), which responded down to 3-6° (Suthers<br />
1966). A visual acuity <strong>in</strong> this range suggests that these <strong>bats</strong> can only detect 5-9<br />
cm objects at a distance of 1 m, and hence it seems unlikely that they can use<br />
vision to detect the <strong>in</strong>sects that they eat. Prey items captured by any of these<br />
species are much smaller than this and they are presumably detected us<strong>in</strong>g sonar<br />
cues alone (Swift & Racey 1983, Kalko & Schnitzler 1989). However, vision<br />
could well be used to detect large objects at distances beyond the range of<br />
echolocation, i.e. objects important for orientation and navigation. Indeed, it has<br />
been shown that loss of vision drastically reduces the hom<strong>in</strong>g performance by<br />
other Myotis species, such as M. sodalis (Hassell 1963, 1966, Davis & Barbour<br />
1970) and M. austroriparius (Layne 1967).<br />
Nevertheless, Bradbury and Nottebohm (1969) showed that hear<strong>in</strong>g impaired<br />
M. lucifugus could avoid 2 mm wide str<strong>in</strong>gs <strong>in</strong> dim light, when the str<strong>in</strong>gs<br />
contrasted sharply aga<strong>in</strong>st the background. Consider<strong>in</strong>g their visual acuity, it is<br />
unlikely that the <strong>bats</strong> could have seen the str<strong>in</strong>gs more than 5 cm away.<br />
Nevertheless, the results from this and other studies (Mueller 1966, 1968)<br />
suggest that vision may be important for normal flight behaviour <strong>in</strong> these <strong>bats</strong>,<br />
although contrast sensitivity might perhaps be more important that visual acuity<br />
<strong>in</strong> some cases.<br />
84
The brown long-eared bat Plecotus auritus responded to patterns equivalent to<br />
30’ of arc, which means that this species should be able to detect objects as small<br />
as 0.9 cm at a distance of 1 m. Among the Vespertilionidae, only Antrozous<br />
pallidus has been shown to have a better resolv<strong>in</strong>g power (15’; Bell & Fenton<br />
1986). These results and the fact that P. auritus has larger eyes than most<br />
Vespertilionids (Cranbrook 1963; Tab 1.) suggest that it should be possible for<br />
long-eared <strong>bats</strong> to detect prey sized objects visually. It typically feeds on<br />
relatively large <strong>in</strong>sects <strong>in</strong>clud<strong>in</strong>g many moths and beetles (Swift & Racey 1983,<br />
Rydell 1989). As P. auritus is a gleaner and sometimes takes <strong>in</strong>sects from leaves<br />
(Swift 1998), it faces potential problems with clutter and therefore use other<br />
sensory cues <strong>in</strong> addition to sonar. In fact, passive listen<strong>in</strong>g plays a major role <strong>in</strong><br />
prey detection by P. auritus (Anderson & Racey 1991). These <strong>bats</strong> are<br />
exceptionally sensitive to sounds around 15 kHz, which is close to the<br />
frequencies emitted by <strong>in</strong>sects mov<strong>in</strong>g <strong>in</strong> clutter (Coles et al. 1989). However,<br />
the long-eared <strong>bats</strong> may also use visual <strong>in</strong>formation when search<strong>in</strong>g for prey. In<br />
a recent study on feed<strong>in</strong>g behaviour, it was shown that P. auritus preferred to use<br />
visual cues to sonar when possible, and that they could detect ca. 2 cm long<br />
mealworms visually (Eklöf & Jones, <strong>in</strong> press).<br />
Visual acuity has previously been tested <strong>in</strong> a number of species (Table 2),<br />
both behaviourally by optomotor response tests (Suthers 1966, Bell & Fenton<br />
1986), and theoretically by count<strong>in</strong>g the number of ret<strong>in</strong>al ganglion cells (Koay<br />
et al. 1998, Heffner et al. 2001). Both methods give <strong>in</strong>dications of the m<strong>in</strong>imum<br />
separable angles, i.e. the m<strong>in</strong>imum distance between two po<strong>in</strong>ts that an animal<br />
need <strong>in</strong> order to be able to separate them. The acuity values estimated by<br />
count<strong>in</strong>g ret<strong>in</strong>al ganglion cells tend to be higher than those estimated from<br />
behavioural studies, suggest<strong>in</strong>g that the anatomical method gives a theoretical<br />
threshold, rather than what the <strong>bats</strong> actually respond to. Nevertheless, although<br />
the acuity values obta<strong>in</strong>ed from the different methods are roughly <strong>in</strong> the same<br />
order, comparisons across the two methods should be made with care.<br />
As shown by the literature data presented <strong>in</strong> Table 2, frugivorous and<br />
nectarivorous <strong>bats</strong> seem to have better spatial resolution than most <strong>in</strong>sectivorous<br />
species. Nevertheless, the f<strong>in</strong>est spatial resolution <strong>in</strong> any bat (3’38’’) is found <strong>in</strong><br />
the glean<strong>in</strong>g <strong>in</strong>sectivore Macrotus californicus (Phyllostomidae), and this<br />
happens to be the only bat known to f<strong>in</strong>d prey, us<strong>in</strong>g vision alone (Bell 1985,<br />
Bell & Fenton 1986). Indeed, glean<strong>in</strong>g <strong>in</strong>sectivores may have better visual acuity<br />
than aerial-<strong>in</strong>sectivores <strong>in</strong> general, and this suggests that the aerial-hawk<strong>in</strong>g<br />
<strong>in</strong>sectivores rely mostly on echolocation rather than vision for detection of small<br />
targets, while the opposite may be true <strong>in</strong> gleaners. At the same time it seems as<br />
if, among aerial-hawk<strong>in</strong>g <strong>in</strong>sectivores, Emballonuridae have better resolution<br />
than Vespertilionidae.<br />
The visual resolv<strong>in</strong>g power may depend on ambient light <strong>in</strong>tensity. In the<br />
common vampire bat Desmodus rotundus, for example, the acuity drops from<br />
48’ at a light <strong>in</strong>tensity of 31 mL (ca. 310 lux) to over 2° <strong>in</strong> 4*10 -4 mL (ca. 0.004<br />
lux) (Manske & Schmidt 1976). Other <strong>bats</strong>, such as Macrotus californicus and<br />
Antrozous pallidus reta<strong>in</strong> their visual acuity down to light levels as low as 2*10 -4<br />
mL (ca. 0.002 lux) (Bell & Fenton 1986). As a comparison, a light level of 0.1<br />
lux is equivalent to light levels at full moon, and similar to the conditions <strong>in</strong> this<br />
85
study. On overcast nights the amount of light drops to 0.0001 lux (Ryer1997).<br />
Eptesicus fuscus responds optimally to brightness discrim<strong>in</strong>ation <strong>in</strong> ambient light<br />
levels around 10 lux (conditions equivalent to dusk or dawn) but performs well<br />
down to levels of 0.001 lux (Ell<strong>in</strong>s & Masterson 1974). As the ambient<br />
illum<strong>in</strong>ation <strong>in</strong>creases towards daylight conditions the visual sensitivity<br />
generally decl<strong>in</strong>es, although the light tolerance varies between species (Hope &<br />
Bhatnagar 1979). Bradbury & Nottebohm (1969) found that Myotis lucifugus<br />
avoids obstacles better under ambient illum<strong>in</strong>ation resembl<strong>in</strong>g dusk than <strong>in</strong><br />
daylight, which also <strong>in</strong>dicates that the eyes of microchiropteran <strong>bats</strong> work better<br />
<strong>in</strong> dim light than <strong>in</strong> bright light. Nevertheless, <strong>in</strong> a study on optomotor response<br />
(Fenton et al. unpublished), several <strong>bats</strong> responded to striped patterns of 0.9° (the<br />
narrowest available <strong>in</strong> the study) even <strong>in</strong> bright daylight. Ambient light levels<br />
and the way it is measured, if reported at all, varies between different optomotor<br />
response studies, which make the results somewhat hard to compare.<br />
Acknowledgements<br />
I wish to acknowledge Bengt Svensson for build<strong>in</strong>g the optomotor device, Lars-<br />
Erik Appelquist for mak<strong>in</strong>g it possible to work at Taberg, Åsa Norén-Kl<strong>in</strong>gberg,<br />
Jens Rydell, Stefan Pettersson and Karl-Johan Börjesson for help <strong>in</strong> the field and<br />
comments on the manuscript.<br />
References<br />
Anderson, M. E. & Racey, P. A. 1991. Feed<strong>in</strong>g behaviour of captive long eared-<strong>bats</strong>,<br />
Plecotus auritus. Animal Behaviour 42, 489-493.<br />
Baker, A. G. & Emerson, V. F. 1983. Grat<strong>in</strong>g acuity of the mongolian gerbil (Meriones<br />
unguiculatus). Behaviour and Bra<strong>in</strong> Research 8, 195-209.<br />
Bell, G. P. 1985. The sensory basis of prey location by the California leaf-nosed bat<br />
Macrotus californicus (Chiroptera: Phyllostomidae). Behavioral Ecology and<br />
Sociobiology 16, 343-347.<br />
Bell, G. P. & Fenton, M. B. 1986. Visual acuity, sensitivity and b<strong>in</strong>ocularity <strong>in</strong> a glean<strong>in</strong>g<br />
<strong>in</strong>sectivorous bat, Macrotus californicus (Chiroptera: Phyllostomidae). Animal Behaviour<br />
34, 409-414.<br />
Bradbury, J. & Nottebohm, F. 1969. The use of vision by the little brown bat, Myotis<br />
lucifugus, under controlled conditions. Animal Behaviour 17, 480-485.<br />
Chase, J. 1972. The role of vision <strong>in</strong> echolocat<strong>in</strong>g <strong>bats</strong>. PhD Thesis, University of<br />
Indiana,Bloom<strong>in</strong>gton.<br />
Chase, J. 1981.Visually guided escape responses of microchiropteran <strong>bats</strong>. Animal<br />
Behaviour 29, 708-713.<br />
Chase, J. 1983. Differential responses to visual and acoustic cues dur<strong>in</strong>g escape <strong>in</strong> the bat<br />
Anoura geoffroyi: cue preferences and behaviour. Animal Behaviour 31, 526-531.<br />
Chase, J. & Suthers, R. A. 1969. Visual obstacle avoidance by echolocat<strong>in</strong>g <strong>bats</strong>. Animal<br />
Behaviour 17, 201-207.<br />
86
Coles, R. B., Guppy, A., Anderson, M. E. & Schlegel, P. 1989. Frequency sensitivity and<br />
directional hear<strong>in</strong>g <strong>in</strong> the glean<strong>in</strong>g bat, Plecotus auritus (L<strong>in</strong>naeus 1758). Journal of<br />
Comparative Physiology A 165, 269-280.<br />
Cowey, A. & Ellis, C. M. 1967. Visual acuity of rhesus and squirrel monkeys. Journal of<br />
Comparative Physiology and Psychology 64, 80-84<br />
Cranbrook, The Earl of. 1963. Notes on the feed<strong>in</strong>g habits of the long-eared bat.<br />
Transaction of Suffolk Natural History Society 11, 1-3.<br />
Davis, W. H. & Barbour, R. W. 1970. Hom<strong>in</strong>g <strong>in</strong> bl<strong>in</strong>ded <strong>bats</strong> (Myotis sodalis). Journal of<br />
Mammalogy 51, 182-184<br />
Davis, R. & Barbour, R. W. 1965. The use of vision <strong>in</strong> flight by the bat Myotis sodalis.<br />
The American Midland Naturalist 74, 497-499<br />
Eklöf, J., Svensson, A. M. & Rydell. J. 2002. Northern <strong>bats</strong> Eptesicus nilssonii use vision<br />
but not flutter-detection when search<strong>in</strong>g for prey <strong>in</strong> clutter. Oikos 99, 347-351.<br />
Eklöf, J. & Jones, G. 2003. Use of vision <strong>in</strong> prey detection by brown long-eared <strong>bats</strong><br />
Plecotus auritus. Animal Behaviour (<strong>in</strong> press).<br />
Ell<strong>in</strong>s, S. R. and Masterson, F. A. 1974. Brightness discrim<strong>in</strong>ation thresholds <strong>in</strong> the bat,<br />
Eptesicus fuscus. Bra<strong>in</strong>, Behaviour and Evolution 9, 248-263.<br />
Grant, J. D. A. 1991. Prey location by two Australian long-eared <strong>bats</strong>, Nyctophilus gouldi<br />
and N. geoffroyi. Australian Journal of Zoology 39, 45-56.<br />
Griff<strong>in</strong>, D. R. 1958. Listen<strong>in</strong>g <strong>in</strong> the dark. Yale University Press, New Haven.<br />
Griff<strong>in</strong>, D. R. 1970. Migration and hom<strong>in</strong>g of <strong>bats</strong>. In: Biology of Bats Vol. II (Wimsatt,<br />
W. A ed.). Academic Press, New York, pp. 233-264.<br />
Hassell, M. D. 1963. A study of hom<strong>in</strong>g <strong>in</strong> the Indiana bat, Myotis sodalis. Transactions<br />
of the Kentucky Academy of Science 24, 1-4.<br />
Hassell, M. D. 1966. The need of vision <strong>in</strong> hom<strong>in</strong>g by Myotis sodalis. Journal of<br />
Mammalogy 47, 356-357.<br />
Heffner, R. S., Koay, G. & Heffner, H. E. 2001. Sound localization <strong>in</strong> a new-world<br />
frugivorous bat, Artibeus jamaicensis: Acuity, use of b<strong>in</strong>aural cues, and relationship to<br />
vision. Journal of the Acoustical Society of America 109, 412-421.<br />
Hope, G. M. & Bhatnagar, K. P. 1979. Effect on light adaptation on electrical responses<br />
on the ret<strong>in</strong>a of four species of <strong>bats</strong>. Experentia 35, 1191-1192.<br />
Hughes, A. 1977. The topography of vision <strong>in</strong> mammals of contrast<strong>in</strong>g life<br />
style: Comparative optics and ret<strong>in</strong>al organisation. In: Handbook of sensory<br />
physiology vol VII/5. The visual system <strong>in</strong> vertebrates (Crescitelli, F. Ed.).<br />
Spr<strong>in</strong>ger-Verlag, Berl<strong>in</strong>, pp. 613-756.<br />
Kalko, E. K. V. & Schnitzler, H.-U. 1989. The echolocation and hunt<strong>in</strong>g<br />
behavior of Daubenton’s bat, Myotis daubentoni. Behavioral Ecology and Sociobiology<br />
24, 225-238.<br />
87
Koay, G., Kearns, D., Heffner, H. E. & Heffner, R. S. 1998. Passive sound-localization<br />
ability of the big brown bat (Eptesicus fuscus). Hear<strong>in</strong>g Research 119, 37-48.<br />
Layne, J. N. 1967. Evidence for the use of vision <strong>in</strong> diurnal orientation of the bat Myotis<br />
austroriparius. Animal Behaviour 15, 409-415.<br />
Manske, U. & Schmidt, U. 1976. Untersuchungen zur optischen Musterunterscheidung<br />
bei der Vampirfledermaus, Desmodus rotundus. Zeitschrift für Tierpsychologie 49, 120.<br />
Marks, J. M. 1980. Ret<strong>in</strong>al ganglion cell topography <strong>in</strong> <strong>bats</strong>. MA thesis, Indiana Univ.,<br />
Bloom<strong>in</strong>gton, IN.<br />
Mueller, H. C. 1966. Hom<strong>in</strong>g and distance-orientation <strong>in</strong> <strong>bats</strong>. Zeitschrift für<br />
Tierpsychologie 23, 403-421.<br />
Mueller, H. C. 1968. The role of vision <strong>in</strong> vespertilionid <strong>bats</strong>. The American Midland<br />
Naturalist 79, 524-525.<br />
Pettigrew, J. D., Dreher, B., Hopk<strong>in</strong>s, C. S. McCall, M. J. & Brown, M. 1988. Peak<br />
density and distribution of ganglion cells <strong>in</strong> the ret<strong>in</strong>ae of microchiropteran <strong>bats</strong>:<br />
Implications for visual acuity. Bra<strong>in</strong>, Behaviour and Evolution 32, 39-56.<br />
Rydell, J. 1989. Food habits of northern (Eptesicus nilssoni) and brown long-<br />
eared (Plecotus auritus) <strong>bats</strong> <strong>in</strong> Sweden. Holarctic Ecology 12, 16-20.<br />
Ryer, A. 1997. Light measurement handbook. International Light, Newburyport, MA.<br />
Suthers, R. A. 1966. Optomotor responses by echolocat<strong>in</strong>g <strong>bats</strong>. Science 152, 1102-1104.<br />
Suthers, R. A. 1970. <strong>Vision</strong>, olfaction and taste. In: Biology of Bats Vol II (Wimsatt, W.<br />
A. ed.). Academic Press, New York, pp. 265-281.<br />
Suthers, R. A. & Wallis, N. E. (1970) Optics of the eyes of echolocat<strong>in</strong>g <strong>bats</strong>. Journal of<br />
<strong>Vision</strong> Research 10, 1165-1173<br />
Swift, S. M. 1998. Long-eared <strong>bats</strong>. Poyser Natural History. London.<br />
Swift, S. M. & Racey, P. A. 1983. Resource partition<strong>in</strong>g <strong>in</strong> two species of vespertilionid<br />
<strong>bats</strong> (Chiroptera) occupy<strong>in</strong>g the same roost. Journal of Zoology London 200, 249-259.<br />
Vaughan, T. A. & Vaughan, R. P. 1986. Seasonality and the behaviour of the African<br />
yellow-w<strong>in</strong>ged bat. Journal of Mammalogy 67, 91-102.<br />
Williams, T. C., Williams, J. M. & Griff<strong>in</strong>, D. R. 1966. Hom<strong>in</strong>g ability of the neotropical<br />
bat Phyllostomus hastatus. Animal Behaviour 14, 468-473.<br />
88
Fig. 1. – The device used for the optomotor response tests, <strong>in</strong> which a bat is presented<br />
with rotat<strong>in</strong>g, striped patterns of different f<strong>in</strong>eness. The bat responds to the revolv<strong>in</strong>g<br />
patterns by mov<strong>in</strong>g its head <strong>in</strong> a stereotype manner. The thickness of the stripes<br />
corresponds to the <strong>bats</strong> visual resolv<strong>in</strong>g power (acuity), measured as degrees (or m<strong>in</strong>utes)<br />
of arc (illustrated by Olof Helje).<br />
89
Tab. 1. – Eye diameter and optomotor responses to patterns of different f<strong>in</strong>eness <strong>in</strong> four species of<br />
<strong>in</strong>sectivorous <strong>bats</strong>. The asterisks <strong>in</strong>dicate that the 5 o pattern was not tested and that the bat did not<br />
respond to f<strong>in</strong>er patterns.<br />
Ambient Eye diameter M<strong>in</strong>imum<br />
Species Ind. light (lux) (mm) separable angle<br />
Plecotus auritus 1 0.6 1.6 45’<br />
2 0.6 1.8 2.5°<br />
3 0.6 not measured 1°<br />
4 0.1 1.7 1°<br />
5 0.1 1.7 45’<br />
6 0.7 not measured 30’<br />
7 0.2 not measured 45’<br />
8 0.3 not measured 1°<br />
Myotis mystac<strong>in</strong>us 1 0.6 1.0 no response*<br />
2 0.6 0.9 no response*<br />
3 0.1 not measured 5°<br />
Myotis brandtii 1 0.1 not measured 5°<br />
2 0.1 not measured 5°<br />
Myotis daubentoni 1 0.1 1.2 5°<br />
2 0.1 1.3 no response<br />
3 0.3 not measured 5°<br />
90
Tab. 2. – Visual acuity expressed as degrees of arc <strong>in</strong> Microchiroptera obta<strong>in</strong>ed from previous studies.<br />
Behavioural acuity values come from optomotor responses, and theoretical values are calculated from the<br />
number of ret<strong>in</strong>al ganglion cells. Acuity is the m<strong>in</strong>imum separable angle, i.e. the best values for each species.<br />
Asterisks <strong>in</strong>dicate that the ambient light level was not measured (or acuity was measured theoretically). For<br />
consistency, the values of visual acuity were sometimes converted from other units, used <strong>in</strong> the orig<strong>in</strong>al paper.<br />
Light Visual Method<br />
Species (lux) acuity Author (behav/theor)<br />
a) Vespertilionidae; glean<strong>in</strong>g <strong>in</strong>sectivores<br />
Macrotus californicus 0.002 3.6’ Bell & Fenton 1986 b<br />
Antrozous pallidus 0.004 15’ Bell & Fenton 1986 b<br />
b) Vespertilionidae; aerial-hawk<strong>in</strong>g and trawl<strong>in</strong>g <strong>in</strong>sectivores<br />
Eptesicus fuscus * 1° Bell & Fenton 1986 b<br />
Eptesicus fuscus 40’-43’ Koay et al. 1998, Marks 1980 t<br />
Myotis lucifugus * 3-6° Suthers 1966 b<br />
Nyctophilus gouldi 50’ Pettigrew et al. 1988 t<br />
c) Emballonuridae; aerial-hawk<strong>in</strong>g <strong>in</strong>sectivores<br />
Saccopteryx bil<strong>in</strong>eata 29’ Pettigrew et al. 1988 t<br />
Saccopteryx leptura * 42’ Suthers 1966 b<br />
Taphozus georgianus 23’ Pettigrew et al. 1988 t<br />
d) Molossidae; aerial-hawk<strong>in</strong>g <strong>in</strong>sectivores<br />
Molossus ater * 10° Chase 1972 b<br />
e) Rh<strong>in</strong>olophidae; flutter-detect<strong>in</strong>g <strong>in</strong>sectivores<br />
Rh<strong>in</strong>olophus rouxi 1.4° Pettigrew et al. 1988 t<br />
f) Megadermatidae; glean<strong>in</strong>g <strong>in</strong>sectivores/carnivores<br />
Megaderma lyra 20’ Pettigrew et al. 1988 t<br />
Macroderma gigas 16’ Pettigrew et al. 1988 t<br />
g) Phyllostomatidae; frugivores and sanguivores<br />
Carollia perspicillata * 16’ Suthers 1966 b<br />
Anoura geoffroyi * 42’ Suthers 1966 b<br />
Artibeus jamaicensis 27’ Heffner et al. 2000 t<br />
Artibeus c<strong>in</strong>ereus 22’ Pettigrew et al. 1988 t<br />
Desmodus rotundus * 42’ Suthers 1966 b<br />
Desmodus rotundus 3.1 48’ Manske & Schmidt 1976 b<br />
Desmodus rotundus 0.04 2.5° Manske & Schmidt 1976 b<br />
h) Other mammals<br />
Rattus (rat) * 20’ Heffner & Heffner 1992 t<br />
Canis (dog) * 3.6’ Heffner & Heffner 1992 t<br />
Felis (cat) * 2.7’ Hughes 1977 t<br />
Macaca (macaque) * 38’’ Cowey & Ellis 1967 b<br />
Homo (man) * 32’’ Hughes 1977 t<br />
91
“The bat that flits at close of Eve<br />
Has left the bra<strong>in</strong> that won't<br />
believe.”<br />
- William Blake<br />
92<br />
V
“I'm wait<strong>in</strong>g for the night to fall<br />
I know that it will save us all<br />
When everyth<strong>in</strong>g's dark<br />
Keeps us from the stark reality”<br />
- Mart<strong>in</strong> L Gore<br />
VI<br />
100
101
102
103
104
105
106
107