Similar to insects, birds and pterosaurs, bats have evolved powered flight.
But in contrast to other flying taxa, only bats are furry. Here, we asked
whether flight is impaired when bat pelage and wing membranes get wet. We
studied the metabolism of short flights in Carollia sowelli, a bat that is
exposed to heavy and frequent rainfall in neotropical rainforests. We expected
bats to encounter higher thermoregulatory costs, or to suffer from lowered
aerodynamic properties when pelage and wing membranes catch moisture.
Therefore, we predicted that wet bats face higher flight costs than dry ones.
We quantified the flight metabolism in three treatments: dry bats, wet bats
and no rain, wet bats and rain. Dry bats showed metabolic rates predicted by
allometry. However, flight metabolism increased twofold when bats were wet, or
when they were additionally exposed to rain. We conclude that bats may not
avoid rain only because of sensory constraints imposed by raindrops on
echolocation, but also because of energetic constraints

Lewanzik, Daniel

Schneeberger, Karin

Voigt, Christian C.

Voigt-Heucke, Silke L.

PubMed

Institutional Repository of the Freie Universität Berlin

 published online 4 May 2011Biol. Lett. Christian C. Voigt, Karin Schneeberger, Silke L. Voigt-Heucke and Daniel Lewanzik Rain increases the energy cost of bat flight  Supplementary dataml http://rsbl.royalsocietypublishing.org/content/suppl/2011/04/29/rsbl.2011.0313.DC1.ht "Data Supplement"Referencesrlshttp://rsbl.royalsocietypublishing.org/content/early/2011/04/29/rsbl.2011.0313.full.html#related-u Article cited in: #ref-list-1http://rsbl.royalsocietypublishing.org/content/early/2011/04/29/rsbl.2011.0313.full.html This article cites 9 articles, 2 of which can be accessed freeP<P Published online 4 May 2011 in advance of the print journal.This article is free to accessSubject collections (663 articles)ecology    Articles on similar topics can be found in the following collectionsEmail alerting service hereright-hand corner of the article or click Receive free email alerts when new articles cite this article - sign up in the box at the toppublication. Citations to Advance online articles must include the digital object identifier (DOIs) and date of initial online articles are citable and establish publication priority; they are indexed by PubMed from initial publication.the paper journal (edited, typeset versions may be posted when available prior to final publication). Advance Advance online articles have been peer reviewed and accepted for publication but have not yet appeared in http://rsbl.royalsocietypublishing.org/subscriptions go to: Biol. Lett.To subscribe to  on August 16, 2013rsbl.royalsocietypublishing.orgDownloaded from  on August 16, 2013rsbl.royalsocietypublishing.orgDownloaded from Biol. Lett.doi:10.1098/rsbl.2011.0313Published onlinePhysiologyRain increases the energycost of bat flightChristian C. Voigt1,2,*, Karin Schneeberger1,Silke L. Voigt-Heucke2 and Daniel Lewanzik11Evolutionary Ecology Research Group, Leibniz Institute for Zoo andWildlife Research, Alfred-Kowalke-Strasse 17, 10315 Berlin, Germany2Animal Behaviour, Freie Universita¨t Berlin, Takustrasse 6,14195 Berlin, Germany*Author for correspondence (voigt@izw-berlin.de).Similar to insects, birds and pterosaurs, batshave evolved powered flight. But in contrast toother flying taxa, only bats are furry. Here, weasked whether flight is impaired when batpelage and wing membranes get wet. We studiedthe metabolism of short flights in Carolliasowelli, a bat that is exposed to heavy and fre-quent rainfall in neotropical rainforests. Weexpected bats to encounter higher thermoregula-tory costs, or to suffer from lowered aerodynamicproperties when pelage and wing membranescatch moisture. Therefore, we predicted thatwet bats face higher flight costs than dry ones.We quantified the flight metabolism in threetreatments: dry bats, wet bats and no rain, wetbats and rain. Dry bats showed metabolic ratespredicted by allometry. However, flight meta-bolism increased twofold when bats were wet, orwhen they were additionally exposed to rain. Weconclude that bats may not avoid rain onlybecause of sensory constraints imposed by rain-drops on echolocation, but also because ofenergetic constraints.Keywords: aerodynamics; Chiroptera; energetics;flight costs; thermoregulation; vertebrate flight1. INTRODUCTIONIn vertebrates, powered flight has evolved three times,but only Chiroptera are furry and use flexible wingmembranes for flapping flight. So far, the aerodynamicsand energetics of bat flight have been mainly studiedunder ideal conditions, such as in controlled laboratorysettings and in wind tunnels [1,2]. But it is unknownhow flying bats perform when conditions turn subopti-mal, such as during rain. Indeed, field observationsconfirm that bats avoid rain. For example, insectivoroushoary bats (Lasiurus cinereus) stop foraging and retreatinto the vegetation during heavy rainfall but continueto forage in light rain [3]. Two explanations seem plaus-ible for this behaviour. First, raindrops may interferewith echolocation, making it less easy for bats todetect insect prey or obstacles [4]. Second, perhapsbats avoid rain because the moistening of their bodyinflicts energy costs on flight by reducing lift andthrust production, or by adding thermoregulatorycosts. Indeed, when 0.1 ml of water droplets evaporatefrom the body surface during a 1 min flight, an 18 gElectronic supplementary material is available at http://dx.doi.org/10.1098/rsbl.2011.0313 or via http://rsbl.royalsocietypublishing.org.Received 18 March 2011Accepted 12 April 2011bat has to invest 4 Wof thermoregulatory costs in orderto maintain normal body temperature [5]. This isabout twice the flight cost that the same bat wouldencounter under dry conditions [2].Here, we test the idea that rain imposes energy costson flying bats. We quantified the metabolic rate of shortflights in Sowell’s short-tailed fruit bat (Carollia sowelli ).This Central American species encounters frequent andheavy rainfall. We studied flight metabolism using the13C-labelled Na-bicarbonate (NaB) method, modifiedfor bolus injections in flying endotherms [6]. Weexposed bats to three treatments in an outdoor flightenclosure.We tested bats flying under (i) dry conditions,(ii) with moistened pelage and wing membranes butwithout rain, and (iii) as in (ii) but with rain. We pre-dicted that flight metabolism is higher when bats arewet or when they are additionally exposed to rain thanwhen they are dry.2. MATERIAL AND METHODSIn 2010, we captured 10 adult Carollia sowelli (six males and fourfemales) between 17.00 and 19.00 h, using 6 and 9 m mist nets(2.5 m height, Ecotone, Gdynia, Poland) at La Selva BiologicalStation in Costa Rica (108250 N, 848000 W). Individually markedbats were kept in groups of two to four in outdoor flight cages(1 m3). Experiments were conducted under the permission ofSINAC in Costa Rica and according to the local regulations of theOrganization for Tropical Studies. Bats were exposed to three treat-ments in random order. Animals were allowed to fly without rain,either dry (dry bats) or after moistening their pelage and wing mem-branes with tap water (wet bats/no rain). Lastly, we exposed wet batsto moderate rainfall (wet bats/with rain). We conducted one trial pernight with a given individual. Rain experiments were usually con-ducted during natural rain. In the absence of rain, we sprayedwater above the cage ceiling (wire mesh) with a water hose so thatartificial raindrops fell vertically into the flight cage. We measuredthe amount of water that had accumulated in a bucket set up inthe middle of the flight cage. On average, bats experienced 0.88+0.3 l min21 m22 rain during the rain trials, which was similar to amoderate tropical rain (C. C. Voigt 2010, personal observation).We used the NaB technique as outlined in Hambly et al. [6] andmodified according to Voigt & Lewanzik [7] for instantaneousmeasurements of 13C enrichments in exhaled breath using a cavityringdown spectrometer. We performed experiments with one batat a time. After administering 200 mg isotonic 13C-labelled NaBsolution (0.29 mol l21; Euriso-Top GmbH, Saarbru¨cken, Germany)intraperitoneally, we transferred bats into a 1.8 l chamber in whichthe temperature was kept constant at 308C (see [7] for a detaileddescription of the set-up). At about time (t) ¼ 12 min post-injection,we transferred bats into a nearby octagonal outdoor flight cage(15.6 m2, 2 m height) that was dimly illuminated. After the batshad flown for on average 72.5+8.5 s, we brought them back tothe chamber where they stayed for a 10 min post-flight period.Bats were weighed to the nearest 0.01 g using a precision electronicbalance (PM-100, Mettler, Switzerland) and transferred back to themaintenance cage. After the experiments, bats were released close tothe site of their capture. For data analysis, we focused on a 20 minperiod about 3 min after peak enrichment in 13C. This interval con-sisted of a pre-flight period (ca 5 min), the flight period (ca 5 min,including transfers) and the post-flight period (ca 10 min). To calcu-late the fractional turnover of 13C (kc; min21) in flying bats, weconverted delta values into atom% [8] and computed linearregressions after the least-squares method for the ln-transformed iso-topic data against time for the pre- and post-flight periods separately.These regressions served to extrapolate the 13C enrichment in theexhaled breath of animals at the onset and end of the flight trial.The time delay between the end of the pre-flight and onset of flight(start) was ca 27 s and the delay between the end of flight (stop) andonset of post-flight period was ca 80 s. We calculated kc for flyingbats according to: kc ¼ [AP13CEstop – AP13CEstart]/t, where AP13CEwas the 13C excess enrichment (in atom%) at the start and stop ofthe flight trial and t the flight duration (min). kc (min21)wasmultipliedby the total body bicarbonate pool Nc (mol) as calculated by the pla-teau method [7], and converted to carbon dioxide production rate( _V co2 ; ml min21) by multiplication with 22.4 l mol21. Since previousvalidation experiments suggested that _V co2 is overestimated whenbased on kc and Nc (e.g. [6]), we used a correction factor to estimateThis journal is q 2011 The Royal Society0 5 10 15 20 0 5 10 15 20 0 5 10 15 20CO2 productionrate (ml min–1 ) 3.02.52.01.51.00.50ln (enrichment)0.51.01.52.0(a) (c) (e)(d) ( f )(b)time elapsed since peak (min)time elapsed since peak (min) time elapsed since peak (min)pre-flight post-flightFigure 1. Elimination of 13CO2 from the body bicarbonate pool (note logarithmic scale) and rate of CO2 production(ml min21) in Carollia sowelli in relation to time elapsed since peak enrichment ((a,b) dry; (c,d) wet þ no rain; (e, f ) wet þrain). Solid lines depict means and light grey areas the range of+one standard deviation. Dashed lines indicate the fractionalturnover of flying bats based on extrapolated 13C enrichments at the onset and end of the flight period (dark grey rectangle,flight period).dry wet + no rain wet + rain metabolism of flying bats (ml CO 2 min–1 )04812162024Figure 2. Metabolic rates (ml CO2 min21) of flying Carolliasowelli when either exposed to dry conditions, wet fur and2 C. C. Voigt et al. Bats in the rain on August 16, 2013rsbl.royalsocietypublishing.orgDownloaded from the _V co2 of flying bats. This correction factor was derived from therespirometric and isotopic measurements of the _V co2 of the pre-flight period. We calculated the kc of resting bats using the slope ofthe pre-flight regression equation. By multiplying kc (min21) withNc (mol) and 22.4 l mol21, we derived _V co2 according to the isotopicdata, and by multiplying the combined concentrations of 13CO2 and12CO2 (ppm) of the same pre-flight period with the flow-throughrate in the chamber, we obtained _V co2 according to the respirometricdata [9]. A general linear model with _V co2 based on isotopic data asthe independent variable, _V co2 based on respirometry as the depen-dent variable and individuals as cofactor demonstrated the highprecision of this model (multiple r ¼ 0.842). We then used the ratioof respirometric and isotopic _V co2 of pre-flight resting bats to calculatethe _V co2 of flying bats based on kc and Nc.We tested for differences in body masses among treatmentsusing repeated measures analysis of variance, and for differencesin resting _V co2 between pre- and post-flight period and among indi-viduals and treatments using a general linear model. We used aFriedman test followed by post hoc Dunn’s test to test for differ-ences in _V co2 rate among treatments because variances variedgreatly among treatments for _V co2 of flying bats. We assumed analpha value of 5 per cent and used SYSTAT (v. 11). Data arepresented as means+1 s.d.no rain, or wet fur and rain. Box margins indicate the 25and 75 percentiles, whiskers the five and 95 percentiles, thecentre line of the box the median. Significant differencesbetween treatments are indicated by horizontal lines. Thedashed line marks the predicted flight metabolism.3. RESULTSResting metabolic rates differed among individuals(F9,47 ¼ 2.51; p ¼ 0.020) and treatments (F2,47 ¼ 6.1,p ¼ 0.004; in the electronic supplementary material,table S1), but not between pre- and post-flight periods(F1,47 ¼ 0.38, p ¼ 0.542; figure 1). Following peakenrichments of 13C in bat breath after about 7 min,13C enrichment declined steadily in resting C. sowelli(figure 1). Bat pelage clumped partly together whenwe moistened bats with water. But despite thisadditional load of water, bats did not differ in bodymass among treatments (F2,29 ¼ 135.2, p ¼ 0.51).Experimental bats weighed on average 17.7+2.2 g.Flight metabolism of bats differed among treatments(n ¼ 10, k ¼ 3, Fr ¼ 12.7, p ¼ 0.0017; figure 1). Meta-bolic rates of dry bats averaged 6.1+2.5 ml CO2min21, which did not deviate from the predicted valueof 6.0 ml CO2 min21 for a 17.7 g bat ([2]; Studentt-test, t9 ¼ 0.39, p ¼ 0.702). Wet bats encounteredBiol. Lett.higher flight metabolic rates than dry bats (no rain:12.9+6.0 ml CO2 min21; mean rank difference ¼12.5, p, 0.01; with rain: 13.6+5.4 ml CO2 min21;mean rank difference ¼ 11.8, p , 0.01; figure 2).Exposure to the rain did not alter wet bats’ metabolicrates (mean rank difference ¼ 0.7; p . 0.05).4. DISCUSSIONBats exhibited a higher flight metabolism with wet furthan with dry fur. Since exposure to rain did not addsurplus energy costs for flying bats, we infer that themoistening of the pelage and wing membranes wasassociated with the increased metabolic rate and not,Bats in the rain C. C. Voigt et al. 3 on August 16, 2013rsbl.royalsocietypublishing.orgDownloaded from for example, an altered flight behaviour caused by fall-ing raindrops. Theoretically, flight costs should increaseto some extent because water trapped in the pelage addsmass to bats. However, a twofold increase in flight costswould involve an additional water load of 25 g for an18 g bat [2], which seems to be an unlikely scenario. Poss-ibly, we could not detect any difference in body massbetween dry and wet bats because the amount of watertrapped in the pelage was negligible in relation tothe large variation in body mass between days. Thecooling effect of water evaporating from the bodysurface of flying bats could add thermoregulatory coststo flight metabolism. A difference of approximately7.5 ml CO2min21 in flight metabolism between dryand wet bats translates into 2.1 W, when assuming carbo-hydrate oxidation. An additional metabolic rate of 2.1 Wmay compensate for the evaporative cooling effect of0.05 g H2O, an amount of evaporative water loss thatseems possible for an 18 g bat flying for a 1 min period.However, we cannot prove unambiguously that theelevated flight costs of wet bats are solely caused byincreased thermoregulatory costs, since we lack detailedmeasurements of evaporative water loss in our studyanimals. Indeed, high humidity during rain may lowerthe rate of evaporation and, consequently, the coolingeffect [10]. Alternatively, lift and thrust production maychange whenwet bats increase flight speed or when aero-dynamic properties of pelage and wing membranessuffer. This could also inflict energy costs on the flightof wet bats.Increased flight metabolism of wet bats may explainwhy bats reduce or cease foraging activities in rain.Bats may only continue to forage in rain whenresources offer sufficient energy gain. For example,we observed Noctilio albiventris hunting swarminginsects at a streetlight even in rain [11], and fruit-eating bats are known to forage in drizzling andmoderate rain [12]. Sensory constraints may presentan additional problem for echolocating bats whenflying in rain, but bats may rather reduce flight activitybecause of overly high foraging costs when pelage andwing membranes become wet, and not because theylose orientation or the ability to detect prey.We thank Ivailo Borrisov for help during fieldwork and theCosta Rican authorities and the Organization for TropicalStudies for research permission. We also thank threeBiol. Lett.anonymous reviewers for their constructive comments thathelped to improve the manuscript.1 Hedenstro¨m, A., Johannsson, L. C., Wolf, M., vonBusse, R., Winter, Y. & Spedding, G. R. 2007 Batflight generates complex aerodynamic tracks. Science316, 894–897. (doi:10.1126/science.1142281)2 Speakman, J. R. & Thomas, D. 2003 Physiological ecologyand energetics of bats. In Bat ecology (eds T. H. Kunz &B. M. Fenton), pp. 430–492. Chicago, IL: The Universityof Chicago Press.3 Belwood, J. J. & Fullard, J. H. 1984 Echolocation andforaging behaviour in the Hawaiian hoary bat, Lasiuruscinereus semotus. Can. J. Zool. 62, 213–221. (doi:10.1139/z84-306)4 Griffin, D. R. 1971 The importance of atmosphericattenuation for the echolocation of bats (Chiroptera).Anim. Behav. 19, 55–61. (doi:10.1016/S0003-3472(71)80134-3)5 Schmidt-Nielsen, K. 1997 Animal physiology: adaptationand environment. Cambridge, UK: Cambridge UniversityPress.6 Hambly, C., Harper, E. J. & Speakman, J. R. 2002 Costof flight in the zebra finch (Taenopygia guttata): a novelapproach based on elimination of 13C labelled bicarbon-ate. J. Comp. Physiol. B 172, 529–539. (doi:10.1007/s00360-002-0279-7)7 Voigt, C. C. & Lewanzik, D. 2011 Trapped in the dark-ness of the night: thermal and energetic constraints ofdaylight flight in bats. Proc. R. Soc. B 278. (doi:10.1098/rspb.2010.2290)8 Slater, C., Preston, T. & Weaver, L. T. 2001 Stable iso-topes and the international system of units. RapidCommun. Mass Spectrom. 15, 1270–1273. (doi:10.1002/rcm.328)9 Lighton, J. R. B. 2008Measuring metabolic rates: a manualfor scientists. Oxford, UK: Oxford University Press.10 Webb, D. R. & King, J. R. 1984 Effects of wetting oninsulation of bird and mammal coats. J. Therm. Biol. 9,189–191. (doi:10.1016/0306-4565(84)90020-2)11 Voigt, C. C., So¨rgel, K. & Dechmann, D. K. N. 2010Refuelling while flying: foraging bats combustfood rapidly and directly to fuel flight. Ecology 91,2908–2917. (doi:10.1890/09-2232.1)12 Thies, W., Kalko, E. K. V. & Schnitzler, U. 2006 Influ-ence of environment and resource availability on activitypatterns of Carollia castanea (Phyllostomidae) inPanama. J. Mammal. 87, 331–338. (doi:10.1644/05-MAMM-A-161R1.1)

Rain increases the energy cost of bat flight

Voigt, C.

Schneeberger, K.

Voigt-Heucke, S.

Lewanzik, D.

MPG.PuRe

https://refubium.fu-berlin.de/bitstream/fub188/16353/1/rsbl.2011.0313.full.pdf

Rain increases the energy cost of bat flight

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