ORIGINAL PAPER
Y. Win e
Ene ge ic cos o ho e ing ¯igh in a nec a - eeding ba
measu ed wi h as - esponse espi ome y
Accep ed: 28 Ap il 1998
Abs ac Ho e - eeding glossophagine ba s p o ide, in
addi ion o he hummingbi ds, a second e eb a e
model o he analysis o ho e ing ¯igh based on me -
abolic measu emen and ae odynamic heo y. In his
s udy, he powe inpu o ho e ing Glossophaga so icina
ba s (11.9 g) was measu ed by s anda d espi ome y
and as - esponse (<0.2 s) oxygen analysis. Ba s needed
5±7 s a e a es - o-¯igh ansi ion o e u n o a e-
spi a o y s eady s a e. The e o e, only ho e ing e en s
p eceeded by a 7-s ¯igh in e al we e e alua ed. _
VO2
du ing ho e ing ¯uc ua ed wi h a equency o 3±5 Hz,
which co esponded in equency o he licking mo e-
men o he ongue. Du ing ho e ing, ba s o en may
ha e hypo en ila ed as indica ed by educed _
VO2and a
espi a o y exchange a io (RER) well below he s eady-
s a e alue o 1. S eady-s a e oxygen consump ion (and
de i ed powe inpu ) du ing ho e ing was es ima ed o
be 27 (25±29) ml O
2
g
)1
h
)1
(158 W kg
)1
o 1.88 W) in
he 11.9-g ba s as indica ed by h ee independen ®nd-
ings: (1) _
VO2was 26 ml O
2
g
)1
h
)1
a e 6.5 s o ho e -
ing, (2) he mean RER du ing single ho e ing e en s was
a i s s eady-s a e le el o 1 only a oxygen up ake a es
o 25±29 ml g
)1
h
)1
, and (3) when he oxygen po en ially
eleased om es ima ed oxygen s o es was added o he
measu ed oxygen up ake, he uppe limi o oxygen
consump ion du ing ho e ing was ound o be 29 ml
O
2
g
)1
h
)1
. Ho e ing powe inpu was abou 1.2 imes
he alue o minimum ¯igh powe inpu (Win e and
on Hel e sen 1998) and hus well below he 1.7±2.6
die ence in powe ou pu pos ula ed by ae odynamic
heo y (No be g e al. 1993). Mass speci®c powe inpu
was 40% less han in hummingbi ds. Thus, wi hin he
possible modes o ho e ing ¯igh , Glossophaga ba s seem
o ope a e a he high-eciency end o he spec um.
Key wo ds Ho e ing ¯igh powe á
Ae odynamics áFas - esponse espi ome y áBa á
Hummingbi d
Abb e ia ions RER espi a o y exchange a io
( espi a o y _
VCO2=_
VO2)áRQ espi a o y quo ien
(me abolic _
VCO2=_
VO2)áSwing a ea, S
hw
and S
aw
a eas
o hand and a m wing, bwing span, l
hw
and l
aw
leng h
o hand and a m wing
In oduc ion
The nec a - eeding Glossophaginae a e a g oup o neo-
opical ba s highly specialized o eeding om ¯owe s
by nigh (c . Doba 1985; on Hel e sen 1993). Like
hummingbi ds, ¯owe - eeding glossophagine ba s usu-
ally ho e while isi ing hei ¯owe s, and hey ha e
e ol ed ¯igh kinema ics specialized o ecien ho e -
ing in a way ha appea s o be unique among ba s. Tha
is, as he wing execu es a backs oke i s ip ( he dis al
wing iangle) is supina ed, so ha he mo phologically
lowe su ace is u ned upwa d. As a esul , ae ody-
namically eec i e li is gene a ed du ing he back-
s oke as well as he s oke o wa d and down ( on
Hel e sen and on Hel e sen 1975; on Hel e sen 1986).
I was he goal o his s udy o de e mine he me a-
bolic powe inpu du ing ho e ing ¯igh in Glossophaga.
I is in e es ing o know his cos o bo h p oxima e and
ul ima e easons. 1. Ho e ing ¯igh ma ks he lowe
endpoin o possible ¯igh speeds so ha o an in e-
g a ed unde s anding o ¯igh mechanics and ene ge ics
i will be necessa y o know bo h he me abolic powe
inpu and ae odynamic powe ou pu du ing ho e ing
¯igh . 2. Fo he cos /bene® analysis o a o aging ba ,
he con ibu ion o he ene gy expended in ho e ing
¯igh is impo an . I ho e ing is ene ge ically expensi e,
i may ha e ac ed as an impo an physiological con-
s ain du ing he e olu ion o he beha iou al algo-
i hms o making o aging decisions.
J Comp Physiol B (1998) 168: 434±444 ÓSp inge -Ve lag 1998
Y. Win e
Ins i u u
È Zoologie II, Uni e si a
È E langen,
S aud s asse 5, D-91058 E langen, Ge many
e-mail: [email p o ec ed]
Ae odynamic conside a ions sugges ha he ene -
ge ic cos o ho e ing ¯igh migh be e y high, well
abo e he cos o le el o wa d ¯igh (c . No be g 1990;
No be g e al. 1993). In p e ious s udies wi h Glossop-
haga so icina, me abolic powe inpu du ing o wa d
¯igh (Win e e al. 1993; Win e and on Hel e sen
1998) and ae odynamic powe ou pu du ing ho e ing
and o wa d ¯igh (No be g e al. 1993) ha e been de-
e mined. The analysis o ho e ing and o wa d ¯igh in
Glossophaga based on kinema ic and mo phological
da a and ae odynamic heo y p edic s an ae odynamic
powe ou pu du ing ho e ing ha amoun s o 170±
260% o he alue du ing le el o wa d ¯igh (No be g
e al. 1993).
Howe e , ecen measu emen s o oxygen consump-
ion by Glossophaga du ing ho e ing ¯igh a a eede
unc ioning as a espi ome ic mask did no con® m
such a la ge die ence (Win e e al. 1998). _
VO2du ing
ho e ing was e en lowe han he oxygen demand
du ing le el o wa d ¯igh . The espi a o y exchange
a io (RER) ound in hese measu emen s was 0.8,
which is below he expec ed alue o 1 (oxidiza ion o
nec a ca bohyd a es), and his disc epancy migh in-
dica e ha he ba s did no each a s eady s a e while
ho e - eeding. In his case he measu ed oxygen up ake
would no e¯ec he ac ual ene gy consump ion in he
muscles so ha de®ni e conclusions abou he powe
inpu canno be d awn. These measu emen s we e based
on a con en ional espi ome ic analysis sys em wi h a
ela i ely slow esponse ime, as compa ed o he du-
a ion o he e en s. Measu emen s consis ed only o
single alues o o al oxygen up ake du ing single
ho e ing e en s and did no allow he moni o ing o
ins an aneous _
VO2.
To ci cum en his p oblem, I used in he p esen
s udy a as - esponse oxygen analysis echnique ( e-
sponse ime <0.2 s) o be able o de e mine changes in
_
VO2du ing he 5±7 s ho e ing e en s. A ho e ing du a-
ion o 5±7 s, while s ill sho i compa ed wi h he
minu e-long ho e ing ¯igh s o hummingbi ds o
hawkmo hs, should be sucien o a Glossophaga o
come in o he espi a o y s eady s a e. This is sugges ed
by he esul s o an indi ec es ima e o he du a ion o
he uns eady phase which was ob ained he e. I is c i ical
o ake in o accoun such uns eady eec s i e-
spi ome ic da a a e o be used o in e ences abou he
powe inpu du ing ho e ing.
Ma e ials and me hods
This s udy was based on ou indi iduals (2 emales, 2 males) o
Glossophaga so icina an illa um (Rehn 1902) (Phyllos omidae:
Glossophaginae) which had been bo n and aised in a b eeding
colony o abou 60 ba s main ained in a opical g eenhouse a
E langen Uni e si y ( he b eeding s ock o igina ed om Jamaica).
The ba s ¯y abou eely and eed by ho e ing in he g eenhouses,
so ha hey a e well ained o ¯igh . The mean body masses and
wing measu es o he indi iduals used o he espi ome ic mea-
su emen s a e gi en in Table 1.
Fligh cage and nec a eede
The expe imen al p ocedu es and equipmen ha e been desc ibed
p e iously (Win e and on Hel e sen 1998; Win e e al. 1998) and
only a b ie accoun is gi en he e. Measu emen s we e conduc ed in
a clima e-con olled oom (22 °C1°, 57% el. humidi y,
0.975 kPa ai p essu e) wi h he pho ope iod se o 12 h:12 h L:D.
The body mass o he expe imen al animal was moni o ed du ing a
measu emen se ies wi hou handling he animal, as a ba always
e u ned o es ing o a oos ha was suspended om an elec-
onic balance. The a i®cial nec a eede was used o unc ion as a
espi ome ic mask. The ¯ow o nec a (a solu ion o glucose,
uc ose and suc ose) in o his eede was achie ed by a compu e -
ope a ed pump and was hus unde he con ol o he expe imen e .
Reducing he a e o nec a ¯ow led o a p olonga ion o he ho e -
eeding isi s by he ba s. As a modi®ca ion o he espi ome ic
eede mask desc ibed ea lie (see d awing in Win e e al. 1998), a
compu e -con olled lid was added di ec ly abo e he eede
opening which olded down au oma ically a e a ba had depa ed
om he eede and s ayed closed o 40 s p e en ing access o he
nec a . This empo a y ood es ic ion caused he ba s o eed
especially in ensi ely a e he ¯ap had opened, inc easing he du-
a ion o hei isi s o as much as 7 s (as compa ed wi h a maxi-
mum o 4.4 s wi h he p e ious a angemen ).
Respi ome y
Ra es o O
2
and CO
2
exchange o a ba ho e ing a he ¯ow-
h ough eede mask we e de e mined wi h a s anda d e-
spi ome ic analysis sys em as desc ibed in Win e e al. (1998). The
sys em was modi®ed, howe e , o he as - esponse _
VO2measu e-
men s; o his, he oxygen senso cell (Ame ek [now AEI Tech-
nologies] N-37M wi h 0.25-ml in e nal senso olume) was placed
up igh in he ¯igh cage and connec ed by a 3-cm ube o he
espi ome ic mask. To minimize washou delay, no ®l e o des-
iccan was placed be ween senso and mask. Componen s behind
he gas ou le o he senso we e: desiccan , ®l e , mass ¯ow con-
olle (B onkho s ) and memb ane pump (Wisa). The ¯ow a e
h ough he senso was cons an a 800 ml min
)1
s anda d em-
pe a u e and p essu e, d y (STPD). As shown be o e (Win e e al.
1998) his ¯ow a e was mo e han wice he minimum a e o
cap u ing all exhaled gases om Glossophaga. The senso was
calib a ed unde hese ope a ing condi ions wi h injec ions o N
2
(N
2
-dilu ion echnique, Fedak e al. 1981). A his high ¯ow a e,
he baseline o he senso showed ¯uc ua ing d i s. A po en ial
e o esul ing om such d i ing was a oided, howe e , by de-
e mining he baseline be o e and a e each o he 5- o 10-s
measu emen in e als. Da a we e collec ed a a a e o 50 Hz.
To al olumes o O
2
exchanged du ing ho e ing we e calcula ed by
in eg a ing he signal en elope o oxygen deple ion, and hen
subsequen ly co ec ed o CO
2
p oduc ion using equa ion 3b om
Wi he s (1977), wi h espi a o y quo ien (RQ) alues aken om
Table 1 Mo phological da a o 4 indi iduals o Glossophaga
so icina an illa um (Rehn 1902). Mass was mean body mass du ing
he ho e ing measu emen s, (Swing a ea, S
hw
and S
aw
a eas o
hand and a m wing, bwing span, l
hw
and l
aw
leng h o hand and
a m wing). De®ni ion o mo phological quan i ies as in No be g
and Rayne 1987. S includes a eas o body and ail memb ane (ca.
10%). Wings we e measu ed (using Sigma Scan so wa e) om
scanned pho og aphs o he ba s held on hei backs wi h ou -
s e ched wings
Sex Mass
(g)
S
(m
2
)
S
hw
(m
2
)
S
aw
(m
2
)
b
(m)
l
hw
(m)
l
aw
(m)
F
1
11.2 0.0111 0.00235 0.00265 0.271 0.072 0.044
F
2
12.7 0.0114 0.00248 0.00267 0.276 0.073 0.044
M
1
11.4 0.0100 0.00217 0.00232 0.265 0.067 0.044
M
2
12.3 0.0114 0.00243 0.00265 0.276 0.073 0.043
435
mean alues de e mined du ing his s udy wi h he s anda d e-
spi ome ic se up (Fig. 3C). As ¯ow a es we e de e mined wi h a
mass ¯ow con olle behind he senso , an addi ional co ec ion o
STP was no necessa y. The ai passing h ough he senso was no
d ied un il a e he senso , so ha he d op in O
2
-concen a ion
measu ed du ing a ho e ing e en was pa ially caused by dilu ion
wi h exhaled wa e apou . In he absence o de ailed in o ma ion
on espi a o y pa ame e s in Glossophaga, i was no possible o
es ima e he quan i y o his exhaled wa e apou wi h sucien
p ecision. The e o e, I pe o med a `biological calib a ion' o he
as - esponse oxygen analysis sys em. Fo his I compa ed he
mean signal in eg als om he as - esponse sys em wi h an
equi alen da ase (ho e ing e en s o equal du a ion) om he
s anda d espi ome ic se -up which was calib a ed con en ionally.
This ga e a ac o by which he signals om he as - esponse
sys em had o be mul iplied in o de o a i e a he same mean
alue o oxygen up ake o bo h da a se s.
To op imize he ¯ow o gas, he espi ome ic mask was al e ed
sligh ly om ou ea lie e sion depic ed in Win e e al. (1998).
The gas ou le a he mask was mo ed o he a end o he ube o
achie e a s aigh ¯ow o he gas om he opening o he eede
ube o he gas exi . To p e en he ba om blocking he gas ou le
o he mask wi h i s ongue du ing eeding, he uppe hal o he
eede ube was p o ec ed wi h wi e mesh placed inside he ube.
The as - esponse measu emen s we e pe o med wi h only one
animal, as his measu emen se up wi hou ®l e and desiccan
places he oxygen senso a a high isk o damage (d ople s o sali a
o nec a en e ing he 750 °C ce amic senso cell may se iously
damage i ).
Lag o _
VO2 esponse a e es - o-wo k ansi ion
When a es ing ba akes o o ¯y, i s espi a o y gas exchange does
no immedia ely e¯ec s eady s a e a es. The du a ion o he
ansien phase o gas exchange was de e mined indi ec ly by an-
alyzing he ela ionship be ween he oxygen up ake du ing a ho -
e ing e en and he du a ion o he o al ¯igh in e al p eceding
his ho e ing e en . The du a ion o each ¯igh in e al was mea-
su ed wi h an accu acy o 1 s by compa ing he ime when he
balance connec ed o he oos signalled ake-o wi h he ime o
in e up ion o he ligh beam a he espi ome ic mask. Fo he
analysis, ho e ing e en s we e g ouped in o 1-s classes o `¯igh
du a ion be o e ho e ing' and he mean oxygen up ake du ing
ho e ing was de e mined o each o hese classes. Da a plo s e-
ealed an asymp o ic cu e, om which he minimum ¯igh du-
a ion (whe e _
VO2was he same as a e longe ¯igh s) was
de e mined (Fig. 1).
Con ols
Swallowing and b ea hing
The swallowing o nec a migh inhibi b ea hing and he e o e
oxygen up ake du ing ho e ing. To es o such a possible hand-
icap caused by swallowing nec a _
VO2was measu ed du ing ho -
e ing isi s a he eede unde wo die en condi ions: (1) he ba
ecei ed a egula nec a ewa d (wi h swallowing) o (2) he ba did
no ecei e a nec a ewa d (wi hou swallowing). Fo hese mea-
su emen s, he compu e -con olled nec a pumps we e ac i a ed
such ha he ba ecei ed a nec a ewa d only du ing e e y second
isi a he eede . Thus ho e ing e en s wi h swallowing (nec a
ewa d) al e na ed wi h ho e ing e en s wi hou swallowing (no
nec a ewa d).
Suppo ing body mass on he eede mask
To es o he possibili y ha a ba may suppo some o i s weigh
on he eede mask du ing ho e ing, I measu ed he e ical o ce
exe ed by he ba on he eede . The eede mask o his mea-
su emen was ®xed on op o a p og ammable elec onic Me le
PM-100 balance, 30 cm abo e he balance pla e. To p e en he ai
accele a ed downwa d by he ho e ing ba om exe ing a o ce on
he balance pla e, he pla e was shielded om his ai cu en by a
piece o ca dboa d (wi h a small hole o he eede holde ).
Measu emen s we e pe o med wi h h ee indi iduals o Glossop-
haga so icina wi h a mean body mass du ing he measu emen s o
11.4 g. Fo ®nal da a analysis, he o ce measu emen s du ing he
las 250 ms o a ho e ing e en we e no included because du ing
he ba 's depa u e he balance became uns able.
Resul s
Lag o _
VO2 esponse a e es - o-wo k ansi ion
The ime in e al du ing which a ba had been in ¯igh
p io o ho e ing a he eede was a iable. The mini-
mum ¯igh in e al be o e a ho e ing e en was 2 s,
which was he ime needed o ¯y om he es ing place
di ec ly o he eede . On mos occasions, howe e , a ba
had been in ¯igh o longe han 2 s be o e a gi en
ho e ing e en . Plo ing he `du a ion o ¯igh in e al
be o e ho e ing' agains he mean _
VO2du ing ho e ing
(Fig. 1) e ealed ha oxygen up ake du ing ho e ing
was educed when he ho e ing e en had been p eceded
by only a sho ¯igh in e al, less han 5±7 s in du a ion.
The e o e, he da a analysed in his s udy we e es ic ed
o ho e ing e en s ha we e p eceded by a ¯igh in e al
o a leas 7 s o be su e ha measu emen s o _
VO2du ing
ho e ing we e no in¯uenced by non-s eady-s a e espi-
a ion ollowing he es - o-¯igh ansi ion.
Mean gas exchange du ing single ho e ing e en s
Measu emen s o gas exchange (O
2
and CO
2
) wi h he
s anda d espi ome ic se up we e pe o med o he
Fig. 1 Mean a es o oxygen consump ion (STPD) du ing single
ho e ing e en s o Glossophaga ba s as a unc ion o he du a ion o
he ¯igh in e al p io o ho e ing ( alues a e means 1 SD om 4
indi iduals). The ¯igh in e al gi en he e is he ime be ween he
depa u e om he balance- oos and he a i al a he pho ocell-
equipped espi ome y eede mask. The do ed e ical line a se en
seconds indica es he beginning o he pla eau phase, in which _
Vo2
du ing ho e ing was independen o he p e-ho e ing ¯igh in e al.
The accu acy o iming was 1 s
436
ou indi iduals du ing 1651 ho e ing e en s wi h a
du a ion o up o 6.9 s. F om hese s anda d measu e-
men s only mean alues o _
VO2and _
VCO2we e ob ained
o a single ho e ing e en . O hese e en s, 970 we e
p eceded by a ¯igh in e al o a leas 7 s du a ion and
we e included in he ollowing analysis. The o al ol-
ume o oxygen aken up du ing a single ho e ing e en
inc eased linea ly wi h he du a ion o ha e en
(Fig. 2). I is in e es ing o no e ha he a iabili y o
oxygen up ake changed wi h he du a ion o he ho e ing
e en s. Among he ho e ing e en s o less han 4 s du-
a ion, oxygen up ake a ied by abou a ac o o wo
a ound he mean ( eg ession line in Fig. 2) while ho -
e ing e en s ha las ed o longe han 4 s we e always
accompanied by a high a e o oxygen up ake.
The mean a e o gas exchange (ml g
)1
h
)1
) o whole
ho e ing e en s also a ied wi h he du a ion o he
e en (Fig. 3): i was high du ing long and sho ho e s
bu low du ing ho e s be ween 1.5 s and 4 s du a ion.
As can be seen by compa ing Figs. 2 and 3, he lowe
mean a e o gas exchange du ing ho e ing e en s o
medium du a ion, was mainly caused by he occu ence
o a la ge numbe o such e en s wi h a low o al ox-
ygen up ake. Pa allel o his, he espi a o y exchange
a io (RER, as opposed o he cellula RQ) was a ound
1 du ing sho ho e ing isi s bu d opped o a alue
a ound 0.8 du ing ho e ing e en s o medium du a ion
(Fig. 3C). Only ho e ing e en s las ing longe han 5 s
we e again accompanied by a highe RER, which ap-
p oached 0.9 du ing 6-s ho e s.
Ven ila ion in ensi y and RER
A empo a y de ia ion o he RER om he s eady-s a e
alue o 1 may be caused by hypo en ila ion (see Dis-
cussion). I his is he case, a low RER should be asso-
cia ed wi h a low a e o en ila ion (hypo en ila ion)
and he RER should inc ease a highe a es o en i-
la ion. Such a ela ionship was ound when he mean
a e o gas exchange calcula ed as _
VO2_
VCO2=2 was
plo ed agains he RER. A RER 1, mean gas ex-
change was a ound 27 (25±29) ml g
)1
h
)1
, bu d opped
signi®can ly a RER 0.8. I appea s jus i®ed o use
he mean a e o gas exchange as an index o en ila ion
in ensi y, as he wo a es we e signi®can ly co ela ed
wi h each o he (Fig. 4, inse ). This is expec ed when
highe a es o gas exchange a e caused by a highe
en ila ion in ensi y.
Fas - esponse _
VO2
The de ia ion o he RER om he s eady s a e alue o
1 (Fig. 3C) and he change in _
VO2du ing longe (as
compa ed o sho e ) ho e ing e en s indica ed ha
s anda d espi ome y, which only ga e a single a e age
o e a comple e ho e ing e en , was insucien o
ob aining an es ima e o he s eady s a e oxygen de-
mand. This is because he ins an aneous a e o oxygen
up ake p obably changed du ing ho e ing. Fo his
Fig. 2 Oxygen up ake (STPD) o Glossophaga ba s (n4) du ing
ho e - eeding a a espi ome y mask. The eg ession line (V
o2
[llg
)1
]
5.55 [s]) was d awn o show ha a iabili y o oxygen up ake was
no cons an o e he ange o ho e ing e en du a ions. Ins ead,
du ing ho e ing e en s o longe han 4 s du a ion, oxygen up ake
was less a iable and almos always abo e a e age. The da a shown
a e om ho e ing e en s ha we e p eceded by a ¯igh in e al o a
leas 7sdu a ion(seeFig.1)
Fig. 3A±C Ra es o gas exchange (STPD, means 1 SD) o ou
Glossophaga ba s (see Table 1) du ing single ho e - eeding e en s a a
espi ome y mask. The da a in Aa e he indi idual mean alues and
da a in Bcombine he means om A. The espi a o y exchange a io
(RER) in Cwas calcula ed om he da a in B. I ep esen s he mean
RER om o al ho e ing pe iods and no he ins an aneous a io
du ing a ho e ing e en . Da a a e om ho e ing e en s ha we e
p eceded by a ¯igh in e al o a leas 7 s du a ion (see Fig. 1)
437
eason I employed a as - esponse oxygen analysis sys-
em ( esponse ime <0.2 s) in o de o moni o di ec ly
changes in _
VO2du ing and owa ds he end o longe
ho e ing e en s. Fo his pu pose, only ho e ing e en s
longe han 5 s we e analysed (n15). The measu e-
men s e ealed la ge ¯uc ua ions in _
VO2du ing ho e ing
(Fig. 5A), p obably caused by a modula ion o b ea h-
ing in ensi y. Du ing he ® s second o a ho e ing ¯igh
hese oscilla ions we e o small ampli ude, a a equency
o abou 5 Hz. The ea e , he ampli ude inc eased and
he equency dec eased o abou 3 Hz, which mos
likely co esponded o he licking equency o he on-
gue. Obse a ions o he ho e ing ba wi h an in a ed
ideo sys em du ing he measu emen s showed ha
licking equency was highe du ing he ® s second,
be o e he ba had s a ed o imbibe he nec a solu ion,
and d opped o a lowe a e a e he ba had con ac ed
he nec a . The esponse ime o he O
2
-analysis sys em
was s ill oo slow o esol e he b ea hing equency,
which would be expec ed o be synch onized wi h he
wingbea cycle a abou 15 Hz. The mean a e o _
VO2as
de e mined om he 15 measu emen s ob ained, in-
c eased du ing a ho e ing e en , eaching a alue o
26 ml O
2
g
)1
h
)1
a e 7 s o ho e ing (Fig. 5B).
Con ols
Swallowing and b ea hing
To es o he possibili y ha he swallowing o nec a
in e e es wi h b ea hing, _
VO2was de e mined du ing a
measu emen se ies in which he ba ecei ed a nec a
po ion du ing only e e y second eede isi (Fig. 6).
Du ing his expe imen , a ba ho e ed o a longe
du a ion when i did ecei e a nec a ewa d a he
eede han when i did no . As obse ed be o e
(Fig. 3B), mean _
VO2was highe when a ho e ing e en
las ed longe . Howe e , he e was no indica ion ha
nec a in ake in e e ed nega i ely wi h oxygen up ake.
I he swallowing o nec a had had a nega i e eec on
b ea hing, one would expec lowe alues o _
VO2du ing
isi s when nec a was consumed. Such an eec was no
obse ed (ANCOVA, P> 0.7, 0.101, n114,
ho e ing du a ion as co a ia e).
Suppo ing body mass on he eede mask
du ing ho e ing
A ba suppo ed only a small ac ion o i s body mass
by leaning on he eede mask (as measu ed wi h he
eede on an elec onic balance). A he beginning o a
ho e ing e en a ba pushed i s head in o he eede
Fig. 4 Change o RER wi h he mean a e o gas exchange, which is
used he e as an index o lung en ila ion in ensi y. _
Vco2and _
Vo2
du ing single ho e ing e en s, we e posi i ely co ela ed o each o he
(inse eg ession line). Thus highe a es o gas exchange we e mos
likely caused by a highe en ila ion in ensi y, so ha he mean a es
o O
2
and CO
2
exchange ([Vco
2
+Vo
2
]/2)canbeusedasanindexo
en ila ion in ensi y. The ho izon al dashed line a RER 1 indica es
he s eady-s a e alue (RER me abolic RQ) expec ed du ing
nec a -suga ca abolism. Da a as in Fig. 3
Fig. 5A±B Ra es o oxygen up ake o a Glossophaga ba while
ho e ing a a espi ome y mask o a leas 5 s. Measu emen s we e
made wi h a as - esponse oxygen analysis sys em ( esponse ime
<0.2 s). (A) The ®ne line wi hou symbols is an o iginal ace
ob ained wi h 50-Hz sampling. The ci cles a e means o he o iginal
da a calcula ed o e 500-ms in e als (2 Hz). (B) Oxygen up ake
du ing 15 sepa a e ho e s (®ne lines, 2 Hz as in A)and heo e all
mean (bold line, n15). The lines a e do ed om he ime when he
ba had le he eede ; he o e all mean (bold line) was ob ained while
he ba was s ill a he eede . No e in (A) ha he oscilla ion o he
o iginal ace changed du ing he ho e ing e en , mos p obably in
synch ony wi h he licking equency o he ongue. Be o e he ® s
nec a ewa d had been gi en, licking equency was a ound 5 Hz
(wi h a low a iabili y in O
2
-up ake) and d opped o a ound 3 Hz
a e he ba s a ed imbibing he nec a (wi h high a iabili y in O
2
-
up ake). The ba 's ongue could no block he gas ou le hole o he
mask because a mesh es ic ed he ongue's access o he bo om hal
o he eede ube. Da a a e om male 1 (see Table 1 and Fig. 3A)
438
mask om below and he eby p oduced an upwa d
o ien ed o ce (li ) agains he mask. This li o ce
anged be ween )5mN and )16 mN (Fig. 7). A e
abou 1 s he ini ial li o ce u ned in o a downwa d
o ien ed o ce (leaning on o he mask) wi h a magni ude
o up o 5.5 mN (equi alen o a body mass suppo o
0.56 g). Thus, a ba suppo ed less han 5% o i s body
mass by leaning on he eede mask.
Discussion
Lag o _
VO2 esponse a e a es - o-wo k ansi ion
The goal o his s udy was o elucida e he me abolic
powe inpu equi ed o ho e ing by a nec a - eeding
glossophagine ba . One o he dicul ies in s udying he
ho e ing ene ge ics o Glossophaga is ha he indi idual
ho e ing ¯igh s a e e y b ie ; hey almos always las
less han 1 s when he ba isi s ¯owe s in he ®eld, and
e en in he labo a o y hei du a ion is well below 10 s.
Deducing powe inpu by espi ome y can be dicul
du ing sho - e m ac i i ies, as he gas exchange an-
sien s be ween he lung and he a mosphe e gi e a dis-
o ed e¯ec ion o e en s aking place in he issues
because o in e ening ci cula o y delays and he bu -
e ing eec s o gas s o es. I was c ucial o his s udy o
ha e a leas a ough es ima e o he du a ion o he
ansien phase a e a es - o-wo k ansi ion, and o be
able o pe o m he measu emen s o oxygen up ake
du ing he s eady-s a e phase o ho e ing. An indi ec
es ima e o he du a ion o his ansien phase in
Glossophaga is p o ided by he ela ionship ound he e
be ween he mean _
VO2du ing ho e ing ¯igh and he
du a ion o he p eceding in e al o o wa d ¯igh
(Fig. 1): a e making he ansi ion om es ing o ¯y-
ing a Glossophaga ook abou 5±7 s o each i s new
espi a o y s eady-s a e. Be o e his pe iod o adjus -
men had elapsed, he oxygen up ake measu ed du ing
ho e ing was dis inc ly lowe han ha ound a e
longe ¯igh s. Fo his eason, only he measu emen s
p eceded by a ¯igh in e al o a leas 7-s du a ion we e
e alua ed in he p esen s udy. In ou p e ious analysis
o oxygen up ake by Glossophaga du ing ho e ing ¯igh
(Win e e al. 1998), his aspec was no aken in o ac-
coun , and hence he gas consump ion a es epo ed in
he o me s udy we e gene ally lowe .
_
VO2and le el o wa d ¯igh
One way o es whe he he me hod chosen he e ga e
ealis ic esul s is o compa e he u no e a es mea-
su ed du ing b ie ho e ing ¯igh s (<1 s) wi h he p e-
iously de e mined cos o o wa d ¯igh in Glossophaga
(Win e e al. 1993; Win e and on Hel e sen 1998).
A e he swi ch om one wo k le el ( o wa d ¯igh ) o
ano he (ho e ing ¯igh ), he espi a o y a e should
ini ially s ill e¯ec he a e o he p e ious wo k le el.
The p e ious es ima e o o wa d ¯igh cos was
based on an indi ec me hod in which bo h daily ene gy
expendi u e and he daily du a ion o ¯igh ac i i y we e
quan i®ed. Fligh cos was hen es ima ed by ela ing 24-
h ¯igh ac i i y wi h daily ene gy expendi u e using
mul iple eg ession analysis, aking in o accoun me a-
bolic expendi u es o es ing. The esul o hese mea-
su emen s o Glossophaga is b acke ed by es ima es o
¯igh cos in small espe ilionid ba s using a die en
Fig. 6 Mean oxygen up ake du ing single ho e ing e en s o a
Glossophaga ba a a espi ome ic eede mask. Nec a ood was
a ailable only du ing e e y o he ho e ing isi o he eede (®lled
ci cles). Imbibing nec a s ongly aec ed he du a ion o a ho e ing
isi bu had no appa en eec on he a e o oxygen up ake du ing
ho e ing. The e was no die ence in mean oxygen up ake be ween
ho e ing e en s wi h and wi hou a ood ewa d (ANCOVA,
P>0.7, 0.101, n114, ho e ing du a ion as co a ia e)
Fig. 7 The downwa d o ien ed e ical o ce exe ed on he eede
mask by h ee ho e ing Glossophaga so icina ba s. Nega i e alues
we e caused by an upwa d o ien ed o ce (li ) on he mask. A li
o ce was p oduced by a ba du ing he ini ial inse ion o i s head in o
he mask. Da a a e means 1 SD om h ee indi iduals ho e ing o
du a ions be ween 1.5 and 2 s (open ci cle: n31, mass 11.3 g; ®lled
ci cle: n20, mass 10.5 g; iangle: n36, mass 12.5 g). These da a
include he alues om wo indi iduals published p e iously (Win e
e al. 1998). The e ical o ce applied by a ba du ing ho e ing on o
he eede mask was measu ed (sampled a a a e o 7 Hz) wi h he
eede mask (wi hou espi ome y ube o pho ocell elec onic wi ing)
moun ed 30 cm abo e an elec onic balance (Me le PM-100). The
opening o he eede mask was o ien ed downwa ds a a 45°angle.
The balance was shielded om he ai accele a ed downwa ds by he
ho e ing ba . As he balance became uns eady du ing he ba 's ake-
o, da a om he las 0.25 s o a ho e ing e en we e no included
439
me hod (doubly labelled wa e me hod, Speakman and
Racey 1991) and ® s well wi h he da a o ® e o he
species o glossophagine ba s anging in body mass om
7 g o 28 g (Win e and on Hel e sen 1998).
As expec ed, _
VO2du ing sho ho e ing e en s (<1 s,
22.2 1.7 ml O
2
g
)1
h
)1
, Fig. 3B) was no signi®can ly
die en om ou p e ious es ima e o _
VO2du ing o -
wa d ¯igh a medium speed (23.8 1.8 ml O
2
g
)1
h
)1
o 11.7 g ba s, Win e e al. 1993; Win e and on
Hel e sen 1998). In addi ion, he RER also co e-
sponded o he expec ed s eady-s a e alue o 1 (Fig. 3C,
ca abolism o suga ca bohyd a es). The measu emen s
o _
VO2ob ained du ing his s udy du ing sho ho e ing
isi s we e hus in gene al ag eemen wi h he expec ed
alue o he cos o o wa d ¯igh .
_
VO2du ing ho e ing
Two phenomena make i dicul o measu e he s eady-
s a e oxygen consump ion o Glossophaga in ho e ing
¯igh : (1) he b ie du a ion o ho e ing and (2) he
p esumed endency o hypo en ila e while ho e ing (see
below). Th ee independen ®ndings o his s udy, how-
e e , indica e ha he s eady-s a e oxygen consump ion
o ho e ing 11.9 g Glossophaga was be ween 25 and
29 ml O
2
g
)1
h
)1
(o 298±345 ml O
2
h
)1
): (1) _
VO2mea-
su ed wi h he as - esponse O
2
analyse was 26 ml
O
2
g
)1
h
)1
a e 6.5 s o ho e ing (Fig. 5), (2) i was only
when he O
2
up ake was high, 25±29 ml O
2
g
)1
h
)1
, ha
he RER was a i s s eady-s a e le el o 1 (Fig. 4), and
(3) i an es ima e o he oxygen po en ially eleased om
body oxygen s o es was added o he measu ed oxygen
up ake, he uppe limi o oxygen consump ion du ing
ho e ing was ound o be 29 ml O
2
g
)1
h
)1
(Fig. 8).
These h ee poin s will be discussed in de ail below.
Fas - esponse measu emen s o O
2
-up ake
The a e o oxygen up ake was 26 ml g
)1
h
)1
(Fig. 5)
a e 6.5 s o ho e ing ¯igh , a du a ion ha should be
sucien ly long o he espi a o y s eady s a e o be
eached. A es ing ba which ini ia ed ¯igh needed only
5±7 s o come in o espi a o y s eady s a e (Fig. 1) al-
hough me abolic powe inc eased 3±10- old (depending
on he he mo egula o y eo du ing es ing). In con-
as , ¯igh powe o ho e ing ¯igh is less han 1.5
imes as g ea as ha o o wa d le el ¯igh .
RER and hypo en ila ion
Nec a - eeding Glossophaga consume nec a -suga ;
hence hei me abolic RQ du ing eeding ac i i y should
be 1, as is he case in o he nec a - eede s such as
hummingbi ds (Sua ez e al. 1990). Du ing his s udy,
howe e , he RER was o en well below 1 (Fig. 3C) and
his may ha e been caused by hypo en ila ion. Hypo-
en ila ion leads o a change in pulmona y pa ial
p essu es o O
2
(dec ease) and CO
2
(inc ease). In u n,
hese changes o pa ial p essu e in¯uence he a es o
al eola gas exchange. This eec , howe e , is die en
o CO
2
han o O
2
because he CO
2
-binding cu e o
he blood is much s eepe han he co esponding O
2
-
binding cu e. The e o e, changes in pulmona y pa ial
p essu es will cause a ansien supp ession o CO
2
ex-
change, whe eas he ini ial eec on he al eola oxygen
exchange is only small (e.g. Widdicombe and Da ies
1991; Scheid 1996). Du ing he sho -du a ion phe-
nomena in es iga ed he e, educed en ila ion could
hus lead o a educ ion in measu ed a es o gas ex-
change and a concomi an d op in RER (Fig. 3). This
explana ion is suppo ed by he obse a ion ha highe
a es o mean gas exchange (de e mined he e as
VO2VCO2=2we e posi i ely co ela ed wi h a highe
RER (Fig. 4). The s eady-s a e alue o 1 (RER
me abolic RQ) was a ained only wi h gas-exchange
a es o 25±29 ml O
2
g
)1
h
)1
. This ange b acke s he
Fig. 8 Es ima e o maximum powe inpu du ing ho e ing ¯igh in
Glossophaga. Filled ci cles and co esponding eg ession line aa e he
mean alues o measu ed oxygen up ake du ing ho e ing ¯igh s o
die ing du a ions (da a aken om Fig. 3B; eg ession aVo
2
[ul
g
)1
]5.80 [s], calcula ed om he plo ed means). Small do s show
he dis ibu ion o he co esponding aw da a ( om Fig. 2). I was
assumed ha ba s buil up an oxygen de®ci du ing ho e ing and ha
he obse ed ailu e o sus ain ho e ing o longe han 6.5 s was
caused by exhaus ion o in e nal oxygen s o es and/o anae obic
capaci ies. Powe inpu was hus uelled by bo h espi a o y oxygen
up ake and he deple ion o oxygen s o es and/o anae obic capaci ies.
Measu ed oxygen up ake o a 6.5 s ho e ing e en was 37.7 llg
)1
(as
gi en by eg ession a). The capaci y o oxygen s o age and/o
anae obic me abolism was assumed o equal he alue o a
hummingbi d, es ima ed a 15 llO
2
pe g body mass (see ex ). This
alue o 15 llg
)1
was added (line b) o he measu ed oxygen up ake
o 37.7 llg
)1
du ing a 6.5 s ho e ing e en . The esul ing alue o
52.7 llg
)1
is he es ima ed maximum s eady s a e oxygen demand o
6.5 s o ho e ing. This da a poin was connec ed o he o igin by line
c. The slope o line cco esponds o a _
Vo2du ing ho e ing o 29.2 ml
g
)1
h
)1
.Linedgi es he minimum espi a o y oxygen up ake
necessa y o sus aining ho e ing ¯igh . This was calcula ed by
subs ac ing es ima ed oxygen s o age capaci y (15 llg
)1
) om he
es ima ed s eady s a e demand gi en by line c. No e ha i ually all
measu emen s o oxygen up ake (small do s) we e in ac abo e his
p oposed lowe limi o espi a o y oxygen demand (line d)
440
di ec ly measu ed _
VO2o 26 ml O
2
g
)1
h
)1
a e 6.5 s o
ho e ing.
Why Glossophaga migh ha e e ol ed a gene al en-
dency o educe b ea hing du ing ho e ing is unclea .
The imbibing o nec a pe se did no supp ess oxygen
up ake. A compa ison o ho e ing e en s wi h and
wi hou nec a a ailabili y did no indica e a die ence in
_
VO2(Fig. 6). One possibili y is ha hypo en ila ion
du ing he eeding om ¯owe s migh p e en he in-
hala ion o pollen while he head is wi hin a ¯owe 's
co olla. An addi ional eason may s em om he ac
ha he bell-shaped ¯owe s, ypical o some glos-
sophagine-pollina ed plan s, a e especially small, o en
no la ge han a `head-mask' o he ba (Vogel 1968,
1969; on Hel e sen 1993, 1996) and hus may be i -
ually sealed by he head du ing ho e ing (Fig. 9). In
addi ion, wi h a idal olume o each b ea h o abou
2 ml o ai s
)1
di ided by b ea hing equency (3 o
15 Hz. Fig. 5) he con ec i e exchange in o he ¯owe
co olla may be low ( idal olume es ima ed wi h oxygen
ex ac ion eciency equal o 0.2 as in 100-g Phyllos o-
mus du ing ¯igh , Thomas e al. 1984). Wi h he ¯ow o
esh ai in o he ¯owe co olla impeded, he limi ed gas
exchange possible migh no be wo h he en ila o y
eo (al hough his eo may be low due o he me-
chanical linkage o en ila ion o wingbea equency,
c . Thomas 1987).
Capaci y o oxygen s o age and/o anae obiosis
On a e age, he measu ed mean _
VO2du ing a ho e ing
e en did no exceed 22 ml g
)1
h
)1
(Fig. 3B) which was
below he es ima ed s eady s a e demand o 25±29 ml
O
2
g
)1
h
)1
. The e o e, i is mos likely ha he ATP o
ho e ing me abolism pa ially came om oxygen s o es
and/o anae obic p ocesses. This emained unaccoun ed
o by he espi ome ic measu emen s. The amoun o
oxygen s o age and/o anae obic capaci y is unknown
o Glossophaga, bu da a om hummingbi ds may al-
low an app oxima ion o his alue. Da a ob ained by
Chai and Dudley (1996) du ing hei in es iga ions o
he limi s o ho e ing ¯igh pe o mance may be used o
his pu pose.
No mally, hummingbi ds a e capable o sus aining
ho e ing ¯igh o ex ended pe iods o up o se e al
minu es. When A chilochus hummingbi ds, howe e , a e
o ced o ho e in a hypoxic and hypodense ai /helium
mix u e wi h 13% O
2
, hey ail o ho e a e 6 s (Chai
and Dudley 1996). In such hypodense ai , he ¯igh
muscle powe ou pu o ho e ing is abou 20% highe
han in no mal ai ; he oxygen up ake du ing ho e ing
emains a he no moxic, s eady s a e a e o
45 ml g
)1
h
)1
. Thus, he bi ds build up a 20% oxygen
de®ci pe second. When hey e mina e ho e ing ¯igh
a e 6 s hey ha e buil up a de®ci co esponding o he
oxygen demand o 1.2 s o ho e ing ¯igh o 15 ll pe g
o body mass. This is consis en wi h he ®nding ha
when he same hummingbi ds a e o ced o b ea he pu e
helium du ing ho e ing, he bi ds pe o m a ``ballis ic
descen '' a e 1.5 s o ho e ing (Chai and Dudley 1996).
He e, hey p esumably o e -exploi hei oxygen s o es
and/o anae obic capaci y.
Using he same capaci y o oxygen s o age (and/o
anae obic capaci y) o 15 llO
2
g
)1
o a Glossophaga
ba , one can es ima e an uppe limi o powe inpu
du ing ho e ing. Such an es ima e is p esen ed in Fig. 8.
Du ing ho e ing ¯igh s o 6.5 s du a ion ( he maximum
du a ion obse ed du ing his s udy) a Glossophaga had
an es ima ed maximum o 52.7 llO
2
g
)1
a ailable o
me abolism which co esponds o an expendi u e o
29 ml O
2
g
)1
h
)1
. These 52.7 llg
)1
esul when he
measu ed up ake o 37.7 llO
2
g
)1
du ing a 6.5 s ho -
e ing ¯igh is added o he es ima ed oxygen s o e de-
ple ion (and/o anae obic capaci y) o 15 llO
2
g
)1
.
The e is no eason o assume he e olu ion o an
Fig. 9 Ho e - eeding Glossop-
haga so icina a a Palia ana
p asina a (Gesne iaceae) ¯owe .
No e ha he bell-shaped co-
olla ® s like a head-mask on
he ba 's ace. (pho og aph a-
ken by O. . Hel e sen in he
labo a o y a a plan g own
om seeds collec ed by M.
Sazima in Vi o ia, Espi i o
San o, B azil)
441
especially high ole ance o anae obic me abolism in
Glossophaga as compa ed o hummingbi ds, in iew o
he ac ha ho e ing du a ions o Glossophaga wi hin
he na u al en i onmen a e sho (no mally below 1 s,
pe sonal obse a ion, Tschapka 1993). Thus i seems
unlikely ha ho e ing powe inpu in Glossophaga ex-
ceeded 29 ml O
2
g
)1
h
)1
.
Powe inpu du ing ho e ing
The combined e idence o he amoun o powe inpu
du ing ho e ing ¯igh in Glossophaga can be summa ized
as ollows. Ou ini ial measu emen s e ealed a _
VO2o
16.7 ml O
2
g
)1
h
)1
du ing 4 s ho e ing ¯igh s (Win e e
al. 1998). Since hen we lea ned ha a Glossophaga, a e
depa ing om i s oos , needs o ha e been in ¯igh o
abou 5±7 s be o e achie ing a espi a o y s eady s a e
(Fig. 1). When espi a o y measu emen s du ing ho e -
ing we e es ic ed o ho e ing e en s p eceeded by a
¯igh in e al o a leas 7-s du a ion, he mean O
2
mea-
su ed du ing single ho e ing ¯igh s (4±7 s) was 21 ml
g
)1
h
)1
(Fig. 3B). Howe e , e en he e, he de ia ion o
he RER om he s eady s a e alue o 1 (Fig. 3C) and
he change in _
VO2du ing longe (as compa ed o sho e )
ho e ing e en s indica ed ha s anda d espi ome y,
which only ga e a single a e age o e a comple e ho e -
ing e en , was insucien o ob aining an es ima e o he
s eady s a e oxygen demand. This is because he ins an-
aneous a e o oxygen up ake p obably changed du ing
ho e ing. Fo his eason I employed a as - esponse
oxygen analysis sys em ( esponse ime <0.2 s) in o de o
di ec ly moni o changes in _
VO2du ing and owa ds he
end o longe ho e ing e en s. These measu emen s e-
ealed ha _
VO2inc eased om an ini ial alue below 20 o
a alue o 26 ml g
)1
h
)1
a e 6±7 s o ho e ing (Fig. 5),
and his ime in e al should be sucien o a ho e ing
Glossophaga ba o come in o espi a o y s eady-s a e. A
die en line o e idence a i ed a he same es ima e.
Anaylsis o he da a ob ained by s anda d espi ome y
(one alue o mean _
VO2 o a single ho e ing e en )
showed ha only a highe a es o gas exchange (25±
29 ml g
)1
h
)1
) was he RER du ing a ho e ing e en a i s
s eady s a e a e o 1 (Fig. 4). A maximum alue o _
VO2
o 29 ml g
)1
h
)1
was also sugges ed when an es ima e o
oxygen s o age capaci y was added o he mean 22 ml
O
2
g
)1
h
)1
consumed du ing 6.5 s ho e ing e en s
(Fig. 8). S eady s a e oxygen demand o ho e ing Glos-
sophaga so icina was hus ound he e o be 27 (25±29) ml
O
2
g
)1
h
)1
which co esponds o a powe inpu o 158 W
kg
)1
o 1.88 W o he 11.9-g ba s.
Addi ional in¯uences on ho e ing
The ho e ing du ing he measu emen s may ha e been
in¯uenced by some addi ional ac o s which a e unlikely
o signi®can ly aec he conclusions d awn om his
s udy. Fo comple eness hey a e lis ed below, bu as
mos ha e been discussed in de ail p e iously (No be g
e al. 1993; Win e e al. 1998), his discussion is no
ei e a ed a ull leng h.
1. Ba s app oached he eede ollowing a pendulum-
swing-like ¯igh pa h wi h he dead cen e a he le el o
he eede , hus con e ing kine ic in o po en ial ene gy
du ing he ®nal app oach pa h. The ene gy sa ed o
ho e ing om his eec , howe e , is unlikely o las o
mo e han a ew en hs o a second.
2. Due o he g ound eec , he downwa dly induced
ai ¯ow may eci cula e wi hin a con®ned space (Rayne
and Thomas 1991). As he bo om o he ¯igh cage he e
was made o ne ing ha le ai h ough and he solid ¯oo
was app oxima ely six wing spans om he ho e ing ba ,
his po en ial eec was likely o be e y small (No be g
e al. 1993). In addi ion, Ba holomew and Ligh on
(1986), who compa ed measu emen s o _
VO2in hum-
mingbi ds wi hin enclosu es (wi h a po en ial g ound e -
ec ) o hose in ee- anging bi ds, ound no die ence.
3. Du ing ho e ing, ba s pa ially suppo ed hei
body mass by leaning on he espi ome y mask, despi e
i s being o ien ed downwa ds a a 45°angle (Fig. 7).
Measu emen s o he e ical o ce exe ed on he eede
mask (wi h an elec onic balance) showed, howe e , ha
ba s suppo ed less han 5% o hei body mass, so ha
he associa ed ene gy sa ings we e equally small.
4. Ba s ha e excep ionally la ge skin a eas and may
lose ca bon dioxide h ough hei well ascula ised, hin
¯igh memb anes (He eid II e al. 1968). Du ing ho -
e ing ¯igh , howe e , cu aneous gas exchange would be
expec ed o amoun o less han 1% o he o al ca bon
dioxide ou pu (Win e e al. 1998) and hus canno
explain he obse ed de ia ion in RER.
5. While i is a common expe ience o adul humans
ha we canno simul aneously b ea he and swallow, his
is a he he excep ion han he ule wi hin mammals
(Tillmann and Wus ow 1982). The measu emen s pe -
o med he e demons a ed ha he swallowing o nec a
did no inhibi oxygen up ake as _
VO2was he same
du ing ho e ing isi s wi h and wi hou swallowing o
nec a (Fig. 6).
Powe inpu and powe ou pu
This s udy complemen s wo ea lie s udies ca ied ou
a ou labo a o y wi h Glossophaga so icina,on(1)
powe inpu du ing le el o wa d ¯igh (Win e e al.
1993; Win e and on Hel e sen 1998) and (2) ae ody-
namic powe ou pu du ing ho e ing and le el o wa d
¯igh (No be g e al. 1993). We can hus now compa e
he ¯igh cos s o wo modes o ¯igh ( o wa d and
ho e ing ¯igh ), as well as wo die en ways o es i-
ma ing he cos o ¯igh : ae odynamic heo y and
me abolic measu emen s. The cos o le el o wa d
¯igh a medium speed in Glossophaga has been es i-
ma ed a 1.63 0.12 W (Win e e al. 1993; Win e
and on Hel e sen 1998) o indi iduals wi h nea ly he
same a e age mass (11.7 g) as used in he p esen s udy
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