Trapped in the darkness of the night: thermal and energetic constraints of daylight flight in bats.

0.29 MB·English

by  Voigt, Christian C.

Proc.R.Soc.B (2011) 278, 2311–2317
doi:10.1098/rspb.2010.2290
Publishedonline 5January 2011
Trapped in the darkness of the night:
thermal and energetic constraints
of daylight flight in bats
Christian C. Voigt1,2,* and Daniel Lewanzik1
1Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Straße 17, 10315 Berlin, Germany
2Department of Animal Behaviour, Freie Universita¨t Berlin, Berlin, Germany
Batsareoneofthemostsuccessfulmammaliangroups,eventhoughtheirforagingactivitiesarerestricted
to the hours of twilight and night-time. Some studies suggested that bats became nocturnal because of
overheating when flying in daylight. This is because—in contrast to feathered wings of birds—dark and
naked wing membranes of bats efficiently absorb short-wave solar radiation. We hypothesized that bats
face elevated flight costs during daylight flights, since we expected them to alter wing-beat kinematics
to reduce heat load by solar radiation. To test this assumption, we measured metabolic rate and body
temperature during short flights in the tropical short-tailed fruit bat Carollia perspicillata at night
and during the day. Core body temperature of flying bats differed by no more than 28C between night
anddaytimeflights,whereasmass-specificCO productionrateswerehigherby15percentduringdaytime.
2
We conclude that increased flight costs only render diurnal bat flights profitable when the relative energy
gainduringdaytimeishighandriskofpredationislow.Ancestralbatspossiblyhaveevolveddark-skinned
wingmembranestoreducenocturnalpredation,butalowdegreeofreflectanceofwingmembranesmade
themalsopronetooverheatingandelevatedenergycostsduringdaylightflights.Inconsequence,batsmay
have becometrapped inthe darkness of the night once dark-skinned wing membraneshad evolved.
Keywords: locomotion; hyperthermia; energetics; optimal foraging; Chiroptera
1. INTRODUCTION (e.g. [14]). Laboratoryexperimentswith small European
Bats are one of the most successful groups of mammals, insectivorous bats indicated that flying bats have similar
dominating mammalian assemblages in tropical ecosys- corebodytemperatureswhenexposedtodarknessorarti-
tems and only being outnumbered by rodents in species ficial light, which is inconsistent with the idea that light
numbers worldwide [1–3]. Yet, foraging activities of imposes a physiological constraint on bat flight [13].
bats are predominantly restricted to the hours of twilight However, core body temperatures have not been
and night time, leaving the diurnal aerial niche to birds measured for bats flying during the day at natural light
[4]. To date, three not mutually exclusive hypotheses and temperature levels.
have been formulated to explain the obligate nocturnal Most studies so far support the ‘predator-avoidance
nicheofbats:competitionwithbirds[5,6],hyperthermia hypothesis’.Forexample,islandpopulationsoffrugivorous
[7–9] and predator avoidance [10–12]. All of these pteropodids(flyingfoxes)andinsectivorousvespertilionids
explanations can be subsumed as risk-averse strategies, have been shown to forage partly at daylight, probably
suggesting that sporadic daylight flight may occur when because raptorial predators are absent from these remote
survival is more at risk for bats foraging exclusively at places [15–18].Indeed, model calculations and empirical
night than for bats foraging at both day and night. workindicatedthatdiurnalflightsareparticularlyriskyfor
Of the three hypotheses, the ‘competition with birds’ small insectivorous bats when raptorial predators are pre-
hypothesis has received least support. During midsum- sent [7,8,13]. On the other hand, vespertilionid bats
mer, for example, foraging activity of Scandinavian bats fromScandinaviaforagedindaylightaroundmidsummer,
partly overlapped with that of potential competitors albeitduringthedarkestpartoftheday,althoughraptorial
such as swallows (Hirundinae; Aves), but both groups birdsoccurredinthesamearea[5].Andeventhoughbirds
never hunted in the same aerospace or interacted antag- ofpreyandcompetingswallowsand swiftsare missing on
onistically [5]. A survey on the British Isles confirmed theAzoreanislands,theinsectivorousbatNyctalusazoreum
that interactions between diurnal foraging bats and forages mostlyat night and onlypartiallyat daytime [19],
birds are rare [13] (but see [6]). suggestingthatotheroradditionalfactorsthanriskofpre-
The ‘hyperthermia hypothesis’ presumes that bats are dation or competition are involved in the evolution of bat
pronetooverheatingasbatwingmembranesarenotinsu- nocturnality. In summary, clear support for any of the
lated and therefore short-wave (visible) solar radiation three hypotheses is either weak or ambiguous (reviewed
may drive core body temperatures to critical and poten- in [20]). Here, we investigated whether bats face thermal
tially lethal levels [7–9,12]. Birds, on the other hand, and energetic constraints when flying in daylight. In par-
do not overheat because feathers are excellent insulators ticular, we were interested in metabolic rates and core
body temperatures (T ) of bats flying at natural levels of
b
solar radiationand ambient temperature.
*Authorforcorrespondence([email protected]).
Received21October2010
Accepted6December2010 2311 Thisjournalisq2011TheRoyalSociety
2312 C. C. Voigt & D. Lewanzik Daylight flight in bats
Metabolic rates of flying bats are 8–15 times higher ‘elevatedflightcost’hypothesisbymeasuringthemetabolic
than during rest [21–24]. Owing to these extreme levels rate using the Na-bicarbonate method [33] and by deter-
of physical activity, flying bats have to dissipate large mining core body temperatures in tropical short-tailed
amounts of heat. In addition to producing endogenous fruitbats,Carolliaperspicillata(Phyllostomidae;Chiroptera)
heat during flight, bats also take up heat from their when flying for short periods at night and at daytime. We
environment. For example, T of flying Phyllostomus has- predicted that T and metabolic rates are higher for bats
b b
tatus increased linearly from about 398C to 428C when flying at daytimethan for batsflyingatnight.
ambient temperature (T) increased from 18 to 318C,
a
suggestingthatbatsmayfacehyperthermiaevenindark-
ness or inside a cave when T is high [9]. Absorption of
a 2. MATERIAL AND METHODS
short-wave solar radiation probably adds surplus heat to
(a)Validation experiments inrestingC. perspicillata
batswhenflyingindaylight.Infact,batwingmembranes
We chose C. perspicillata as our focal species because it is a
have a low degree of reflectance (i.e. albedo) and absorb
commonfruit-eatingbatspecieswithacircumtropicaldistri-
up to 90 per cent of short-wave solar radiation [25,26].
bution in the Neotropics and an exclusively nocturnal
A model calculation predicted that maximum exogenous
foragingactivity[34].Sincepreviousmodelcalculationspre-
heat uptake from solar radiation may be eight times
dictedthat20gbats such asC.perspicillata shouldrarelybe
higher than endogenous heat production in 20g bats
constrainedbyhyperthermiaclosetotheequator[7,12],we
flyinginbroaddaylight[27].Thus,batsflyingindaylight
expected no adverse effects on health from potential
have to find ways to dissipate heat, or they are prone to
hyperthermia during daylight.
the health hazards of hyperthermia. Indeed, a recently
We used the Na-bicarbonate method to determine the
suggested hypothesis, the so-called ‘heat dissipation
rateof CO production (V_ ) in flying bats as outlined by
limit theory’, postulates that heat dissipation may be a 2 CO2
Voigt et al. [35]. We first performed a validation study with
more general physiological constraint influencing limits
11 male C. perspicillata. In March 2010, we captured bats
of energy expenditures in endotherm animals [28,29].
between 17.00 and 22.00h using 6 and 9m mist nets
Overall,batscanmakeuseoftwomajorroutesforheat
(2.5m height, Ecotone, Gdynia, Poland) in the vicinity
dissipation: respiratory evaporation and cutaneous heat
of La Selva Biological Station in Costa Rica (108250N,
loss. Since neither breathing frequencies nor breath
848000W).Aftermarkingbatsindividuallywithsplitforearm
volumeshavebeenshowntovaryinbatsflyingatdifferent
bands (A.C. Hughes Ltd, Middlesex, UK, size XB), we
T inwindtunnels,respiratoryevaporativeheatlossseems
a transferred them into flight cages (1m3) where they were
to account for only a small portion of heat loss (an esti-
either kept individually or in groups of two for a maximum
mated 14% of total heat loss in P. hastatus [9]). Thus,
of 8 days at ambient conditions and at the natural photo-
the major route of heat loss must come from cutaneous
period. All bats were released close to their site of capture
heat exchange [9]. Since bats lack sweat glands on their
after the end of experiments. For validation, we compared
wing membranes [30], they cannot cool their bodies via
V_ as measured with the Na-bicarbonate method and
evapotranspiration and chiefly depend on the cooling CO2
with V_ as measured by respirometry. To assess V_
effect of convective airstreams. Some bat species that fly CO2 CO2
based on Na-bicarbonate, it is essential to estimate the
partly in daylight have thermal spots along their body
totalbicarbonatepoolsize.Forthis,weconductedadilution
flanksthatmostprobablydissipatebodyheatwhenexposed
experiment according to Speakman & Thomson [36] and
to solar radiation or high T (Tadarida brasiliensis [31]).
a Hambly et al. [37]. Stable carbon isotope ratios were
Besidesthat, bats are onlyable to dissipate heat from their
measured using a gas bench coupled to an isotope ratio
dark and naked wing membranes via convective cooling.
mass spectrometer (Delta VAdvantage, Thermo Finnigan,
Atlowtemperatures,thisprovestobesufficientfordaylight
Bremen, Germany) as outlined in Voigt et al. [35]. The
flights—for example during midsummer days (T ¼208C
a ratio of 13C:12C was measured in relation to a reference
[5]) and in laboratory trials (T ¼248C [13]). Then, T of
a b gas, which was calibrated to international standards (NBS
flying bats remains at normal, sublethal levels [13]. How-
22 and Vienna-Pee Dee Belemnite¼PDB) and expressed
ever, bats may be constrained in dissipating sufficient heat
in the dnotation (‰). Precision was better than +0.1‰
ifexogenousheatfromsolarradiationisabsorbedaddition-
(1 s.d.). We converted the d values into atom per cent
allybywingmembranesand whenT isequaltoorhigher
a (AP13C; %) according to Slater et al. [38] and plotted the
than T .
b natural logarithm of CO (mol) added to the vacutainers
As flying bats flap their wing membranes in complex 2
against the natural logarithm of AP13C. We then calculated
ways [32], heat absorbance and dissipation are not static
a least-squares linear regression to predict ln(CO ) (mol)
during flight. Also, wing tension is known to influence 2
based on ln(AP13CE). AP13CE is the enrichment in 13C
theamountof absorbedheatinthatarelaxedwingmem-
above baseline levels in atom per cent. We calculated the
braneabsorbsmoreheatthanatautwingmembrane[26].
totalbicarbonate pool,N (mol)as
Thus,batscouldaltertheirwing-beatkinematicstoreduce c
the amount of absorbed short-wave solar radiation when N ¼20(cid:2)eð(cid:3)7:2421(cid:3)1:5458(cid:2)lnpeakAP13CEÞ: ð2:1Þ
c
flyingathighT indaylight.Ifthisisdoneinasuboptimal
a
way for thrust and lift production, or if bats fly faster to The numbers 27.2421 and 21.5458 refer to the
escape direct sunlight, we predicted bats to face elevated regressionequationofthedilutionexperiment.Weincluded
flight costs at daytime. This could alter key components thefactor20inequation(2.1)tocompensateforthe20-fold
ofoptimalforaging,namelytheenergycostsofcommuting difference used for the dilution and for the animal
andfeeding.Asaconsequence,batsmaybeforcedintothe experiments.
nocturnal niche when foraging yields a better energy gain To assess whether CO production rates (V_ )
2 CO2
at night than at day. We tested this newly postulated measured by indirect calorimetry matched those estimated
Proc.R.Soc.B(2011)
Daylight flight in bats C. C. Voigt & D. Lewanzik 2313
by the Na-bicarbonate method, we conducted respiro- lines differed from those of the line of equivalence and also
metric measurements with bats exposed to 158C (n¼5) whether they differed among each other using Student’s
and to 308C (n¼6) in a flow-through set-up. Before t-tests.
each experiment, we weighed the bats to the nearest We estimated the number of bicarbonate body compart-
1mg using a precision electronic balance (PM-100, ments involved during isotopic elimination for resting
Mettler, Switzerland). A single bat was then placed in a C. perspicillata by calculating the reaction progress variable
custom-built 3-l respirometry chamber in which tempera- (12F)according to Cerlinget al.[41]and theequation
ture was kept constant using a water bath. CO and
2 AP13CEð1Þ(cid:3)AP13CEðtÞ
water vapour were scrubbed off from the inlet air through 1(cid:3)F ¼ ; ð2:3Þ
tubes filled with ascarite and drierite. Then, air wasflushed AP13CEð1Þ(cid:3)AP13CEð0Þ
through the chamber at a rate of 1.8lmin21 as measured where AP13CE (1) equals the 13C enrichment above base-
by a mass flow controller (Bronkhorst, Melsungen, line after infinite time and AP13CE(0) the 13C enrichment
Germany). A subsampler routed a portion of the outlet above baseline at time 0. We plotted the natural logarithm
air to the cavity ring-down spectrometer (G1101 CO2 Iso- of (12F) against post-injection time and assessed the
topic Analyser, Picarro, Sunnyvale, CA, USA). This linearityoftherelationship byinspection.
instrument measured concentrations of 13CO and 12CO
2 2
(ppmV), in addition to d13C (‰) in the outlet air stream (b)Flightexperimentsin C.perspicillata
of the respirometry chamber. Aftervalidationexperiments,wereleased5ofthe11batsand
All animals received 200mg of 30 per cent (mass/mass) captured 4 additional males to minimize the time animals
honey water before we injected 200mg of the aqueous spentincaptivity.Flightexperimentsweresimilartothevali-
13C-enriched Na-bicarbonate solution intraperitoneally (IP) dation experiments except that we allowed bats to fly for
using a sterile needle and syringe. Immediately afterwards, 1.5min approximately 21min post-injection. Before per-
animals were returned to the respirometry chamber. Then, forming flight experiments with one bat at a time, we
we monitored changes in 13CO enrichment in relation to allowed each bat to fly in the flight cage so that they would
2
12CO over the following 60min. We focused on a 15min getaccustomedtothecageinterior.Shortlybeforetheexper-
2
period5minafterpeakenrichment,becausepreviousstudies iments,theanimalswerefedwith200mg30percent(m/m)
indicatedalinearwashoutofthelabelwithinthisperiod.For honey water to ensure that bats would oxidize mostly
each 1min period of this interval, we calculated V_ by carbohydrates during flight [42]. We injected 200mg of
CO2
multiplying the combined concentrations of 13CO and Na-bicarbonateIPandthenputthebatintotherespirometry
2
12CO (ppmV) with the flow-through rate in the chamber chamber as outlined above. At approximately t¼20min
2
using eqn (10.5) from Lighton [39] and assuming that bats post-injection, we opened the chamber and released the bat
exclusively oxidized sugar (respiratory exchange ratio¼1.0). in a nearby flight cage (3m length, 2m width, 2m height)
For the same 1min periods, we calculated the fractional within 20–30s. The flight room was illuminated by dim
isotopicturnoveraccordingto red light at night so that we were able to observe the bats.
Experiments in daylight were performed between 10.00
k ¼½AP13CEðt(cid:3)1minÞ(cid:3)AP13CEðtÞ(cid:4)=min; ð2:2Þ and 15.00h using the same flight cage. Since the ceiling of
c
the flight cage consisted of a 1cm2 wire mesh screen, bats
whereAP13CEwasthe13Cenrichmentabovebackgroundat were exposed to natural sunlight. The time delay between
timetandattimet21min.k (min21)wasmultipliedbythe the last breath collection of the pre-flight period and the
c
totalbodybicarbonatepoolN (mol)andconvertedtoV_ onset of flight in the cage was recorded to the nearest 1s
c CO2
(mlmin21). using a stopwatch. We allowed bats to fly continuously for
We used two different methods to calculate the total a 1.5min interval. If bats tried to land, we encouraged
body bicarbonate pool (N ) of bats: the plateau and the them to resume flight by approaching them or by gently
c
intercept method [40]. When using the plateau method, touchingthewallwithahandatadistanceofapproximately
we referred to the maximal post-injection enrichment of 0.5mtothebat.Theflightdurationwasalsomeasuredwith
13C in exhaled breath expressed in AP13CE (%) for adigitalstopwatchtothenearestsecond.Werecapturedbats
equation (2.1). When using the intercept method, we with a hand-net and then measured core body temperature
extrapolated the isotope elimination curve to t¼0min (T )tothenearest0.18Cbygentlyputtingthethermocouple
b
(i.e. the intercept with the y-axis), based on least-squares ofadigitalthermometer(GTH1170,Greisingerelectronic,
linear regression equations calculated for the natural logar- Regenstauf,Germany)atleast10mmintothebat’srectum.
ithm of isotopic enrichments between 5 and 15min after After the temperature measurements reached a plateau, we
peak enrichment. We then inserted this intercept into tried to gently move the thermocouple deeper into the
equation (2.1) to calculate the estimated total body bicar- rectumtoensurethatmeasuredtemperatureswererepresen-
bonate pool N . For each experimental run, we averaged tativeofthecorebodytemperature.Approximately80–100s
c
V_ of 1min intervals measured by indirect calorimetry aftertheendoftheflightperiod,batswereputbackintothe
CO2
and V_ of 1min intervals measured by Na-bicarbonate. respirometrychamberwhereisotopicenrichmentofexhaled
CO2
All V_ values were converted to standard temperature breath and V_ was recorded using the Picarro Isotope
CO2 CO2
and pressure conditions. Analyser. After a 30min post-flight period, animals were
We plotted V_ based on respirometry and on the transferredbackto themaintenance cage.
CO2
Na-bicarbonate method, and calculated least-squares linear We estimated the isotopic enrichment in the exhaled
regressions for the two datasets with the plateau and inter- breath of bats at the onset of flight by calculating a least-
cept approaches separately. After confirming that the squares linear regression on the natural logarithm of
datasets fulfilled the requirements for regression analysis, AP13CE in the exhaled breath of the pre-flight period
wetestedwhethertheslopesandinterceptsoftheregression (3–5min duration). We defined the pre-flight period as the
Proc.R.Soc.B(2011)
2314 C. C. Voigt & D. Lewanzik Daylight flight in bats
timepointafterpeakenrichmentwhenthedeclineofisotopic (a) 6
enrichments turned linear and before we removed the bat
fromthechamber.Byextrapolation,weestimatedtheisoto- 5
nt
picenrichmentinexhaledbreathwhenanimalsstartedtofly e
m
intheflightcage.Weusedasimilarapproachfortheisotopic ch%) 4
enrichmentofexhaledbreathatthetimewhenbatsstopped nriE;
eC 3
flying; that is, we used the natural logarithm of isotopic C 3
enrichments of the post-flight period (10min duration) to 13 1P
s A 2
calculate a regression equation after the least-squares es(
c
method.Thedifference in the natural logarithmofAP13CE ex 1
between the pre-flight and post-flight time divided by the
flight time yielded the isotope elimination rate of carbon 0
isotopes(k )during flight.
c
Since the validation experiment suggested that V_ is (b) 0
CO2
overestimated when calculated based on k and N , we
c c
usedthefactordifferencebetweenV_ basedonrespirome- –1
CO2
try and V_ based on isotopic washout to compensate for
CO2
this overestimation. For this, we calculated V_CO2 of resting F) –2
bats during a 10min post-flight period using both isotopic –
1
dthaetatwanodV_respiorofmpoesttr-yfl.iWghetrthesetnincgablcautslaatenddtahsesurmateiodbtheatwtteheins ln( –3
CO2
ratio remains constant in flying bats; that is, we multiplied
the V_ of flying bats based on the Na-bicarbonate –4
CO2
method with the ratio derived from post-flight resting bats.
To control for the effect of body mass difference between –5
daytime and night-time experiments, we calculated the 0 10 20 30 40 50 60
mass-specific metabolic rate(mlCO g21h21). time elapsed since injection (min)
2
Environmental variables such as solar radiation and Ta Figure 1. (a) Elimination of 13C label and (b) the reaction
were recorded during each experiment at a weather station progress variable after intraperitoneal injection of 200mg of
about 200m away from the flight cage. Solar radiation was 13C-labelled Na-bicarbonate in 11 male C. perspicillata. The
averaged over 30min intervals and accessed via the web solid lineindicatesthemeanvaluesof13Cenrichment above
page of the station (http://www.ots.ac.cr/meteoro/default. baseline(AP13CE;%)andtheln-convertedreactionprogress
php?pestacion=2 accessed on15 May 2010). variable,respectively.Thegreyareasindicatetherange+1s.d.
We calculated Wilcoxon matched-pairs signed-ranks test
using GRAPHPAD v. 3 (GraphPad Software, Inc., San Diego, 2.0
USA) to test for differences in body mass, T , and mass-
b
specific metabolic rate when bats flew at night and at day.
For all statistics, we used an alpha value of 5 per cent. All
values arepresented as means+standarddeviation.
1.5
1)
3. RESULTS –n
mi
(a) Validation experiments in resting
ml 1.0
C. perspicillata
(
2
Bats of the validation experiment weighed on average o
c
22.1+1.4g. Within a few minutes after IP injection of V
the labelled Na-bicarbonate, the 13C label equilibrated
0.5
in the bats’ body bicarbonate pool (figure 1a). On aver-
age, peak 13C enrichments above baseline levels (5.87+
1.23atom%) occurred 11.3+2.4min post-injection.
Intercept values of maximum AP13CE equalled 7.37+
1.74atom%. After the peak, k averaged 0.078+
c 0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0
0.016min21 and the dynamics of the reaction progress Vco (mlmin–1)
2
variable suggested a linear decline, and thus a single
pool involved in the washout of the 13C label for a Figure2.Carbondioxideproductionrate(V_ ;mlmin21)
30min post-peak period (figure 1b). The comparison measured by indirect calorimetry in relaCtiOo2n to V_
between respirometry and the Na-bicarbonate method (mlmin21) measured by the Na-bicarbonate method. ToCtOa2l
revealed that the Na-bicarbonate method yielded higher bicarbonate pool size was estimated by either the plateau
V_ values than the indirect calorimetry (figure 2). (filled circles) or the interceptmethod (opencircles).
CO2
V_ averaged 0.73+0.37mlmin21 when measured
CO2
with indirect calorimetry, while V_ averaged 1.84+ exceeded the respirometric value by 151+26 and 89+
CO2
0.91 and 1.40+0.71mlmin21 based on the intercept 18 per cent, respectively. Despite this discrepancy, the
and the plateau approach of the Na-bicarbonate coefficient of determination for the relationship between
method, respectively. Thus, the Na-bicarbonate method V_ as measured with the Na-bicarbonate method and
CO2
Proc.R.Soc.B(2011)
Daylight flight in bats C. C. Voigt & D. Lewanzik 2315
(a) 46 (b) 28
26
44 n
o 24
y temperature (°C) 4402 ecific CO producti2–1–1ate (ml g h) 11226802
d pr
bo 38 ss-s 14
a
m
12
36 10
night day night day
Figure3.(a)Corebodytemperature(8C)and(b)mass-specificCO productionrate(mlg21h21)inC.perspicillataflyingat
2
nightand during theday.
respirometrywashigh,equalling94and97percentwhen that T and flight metabolism are elevated when bats fly
b
using the intercept and the plateau method, respectively. at natural levels of daylight and T.
a
Because of the higher r2 value, we used the plateau At night, T of flying C. perspicillata was 38C higher
b
method for calculating V_ of flying bats. than that of conspecifics resting at about 308C T
CO2 a
[43,44]. Thus, endogenous heat production increased
(b) Flight experiments in C. perspicillata Tb of flying bats even at night. When flying during day-
During experiments in daylight, solar radiation averaged time, Tb increased by an additional 28C to about 428C.
545+189Wm22 and T 31.5+1.38C. In contrast, T Although this value is in the upper range of physiologi-
a a
dropped to 24.5+1.28C during night-time experiments cally normal Tb, we never observed effects of elevated
(Tadifference:7.0+2.08C:10pairs;Tþ ¼55,T2¼0.0; Tb in post-flight bats, such as panting or prostration.
p¼0.002). Bats weighed on average 19.5+1.4 and We conclude from this observation that bats are capable
20.8+1.2g when flying at night or at daytime, respect- of tolerating excess heat load when exposed for short
ively. The difference of 1.3+0.8g between night and periods to solar radiation and high Ta. Overall, our data
daytime was significant (10 pairs; Tþ ¼55, T2¼0.0; of high Tb in post-flight Carollia are consistent with the
p¼0.002). After flying for 1.5min at night, T averaged hyperthermia hypothesis (i.e. the combined effect of
b
40.2+0.88C and CO2 production rate 5.53+ solar radiation and increased Ta drives Tb of flying bats
0.81mlmin21 (n¼10 bats). After flying for 1.5min in higher) [7–9,12]. We argue that bats could nonetheless
daylight, T of post-flight C. perspicillata averaged forage for short periods in daylight (e.g. they could
b
41.9+0.98C, a difference of 1.7+0.88C between night switch between close foraging patches or hunt insects
and day (10 pairs; Tþ ¼55, T2¼0.0; p¼0.002; during brief foraging bouts). This could be particularly
figure 3a). Carbon dioxide production rates of diurnally advantageous when solar radiation is less intense—for
flying bats averaged 6.69+0.72mlmin21 and were example, during cloudy days or under a forest canopy.
higher than when bats flew at night (10 pairs; Tþ¼45, Why do bats not fly more often in daylight, then?
T2¼0.0; p¼0.004). Since bats flying during the day Metabolic rates were about 15 per cent higher when
and at night-time differed in body mass, we calculated C. perspicillata flew in daylight than when they flew at
mass-specific metabolic rates (ml CO g21h21). Mass- night. Differences in flight metabolism between diurnal
2
specific metabolic rates were significantly higher during and nocturnal bats have strong implications for optimal
daytime flights (19.4+2.4ml CO g21h21) than feeding strategies of bats. When exposed to sunlight, bats
2
during night flights (17.0+2.3ml CO2g21h21; 10 may only be able to dissipate excess heat if Ta is low,
pairs; Tþ¼49.0, T2¼26; p¼0.0273), an increase becauseconvective heat loss isafunction ofthe difference
of 15.3+19.0 per cent in mass-specific metabolic rate between ambient and body temperature. This might
between day and night (figure 3b). explain,forexample,whytemperate-zonebatsareconduct-
ingdiurnalflightsinwinter [45]oraround midsummerat
high latitudes [5]. By contrast, at high T bats may not be
a
4. DISCUSSION able to reduce the combined heat load of muscular work,
We tested whether bats flying at daytime experienced air temperature and solar short-wave radiation. Then,
highercorebodytemperatures(T )andhighermetabolic bats face elevated flight costs, and diurnal flights may
b
rates than during nocturnal flights. Indeed, we demon- only turn profitable if the flight period is short, food
strated that bats encountered a 28C increase in core rewardishighand/orpredationriskislow.Higherforaging
body temperature and a 15 per cent increase in mass- costsofdiurnallyactivebatsmaybeparticularlydisadvan-
specific metabolic rate when flying in daylight than tageousinsituationswhenbatscompetewithbirdsoverthe
when flying at night. These findings support the same food sources (i.e. a foraging patch may become
hyperthermia and elevated flight-cost hypotheses. To the unprofitable for bats, but may still be profitable to birds,
best of our knowledge, this is the first study to show if batsand birds encounter divergent foraging costs).
Proc.R.Soc.B(2011)
2316 C. C. Voigt & D. Lewanzik Daylight flight in bats
Butsomebatsfromremoteoceanislandsflyindaylight, Lucknerfor isotopicanalysis.SilkeL.Voigt-Heucke,Heribert
for example large pteropodid bats on the Samoan or Hofer, Detlev Kelm and Ana Popa-Lisseanu provided helpful
Comoranislands[16,18].Sinceraptorialbirdsaremissing comments on earlier versions of the manuscript. We are very
grateful for the support of the Organization for Tropical
on these islands, the presence of diurnallyactive pteropo-
Studies, particularly the staff of La Selva Biological Station.
dids has long been considered as an argument for the
Experiments complied with current laws in Costa Rica and a
predator-avoidance hypothesis (e.g. [20]). However, researchpermitwasgrantedbySINAC.
flying foxes are more efficient in gliding than small bats
[46], and therefore pteropodids may compensate for the
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