Skip to main content
Log in

High manoeuvring costs force narrow-winged molossid bats to forage in open space

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Molossid bats are specialised aerial-hawkers that, like their diurnal ecological counterparts, swallows and swifts, hunt for insects in open spaces. The long and narrow wings of molossids are considered energetically adapted to fast flight between resource patches, but less suited for manoeuvring in more confined spaces, such as between tree-tops or in forest gaps. To understand whether a potential increase in metabolic costs of manoeuvring excludes molossids from foraging in more confined spaces, we measured energy costs and speed of manoeuvring flight in two tropical molossids, 18 g Molossus currentium and 23 g Molossus sinaloae, when flying in a ~500 m3 hexagonal enclosure (~120 m2 area), which is of similar dimensions as typical forest gaps. Flight metabolism averaged 10.21 ± 3.00 and 11.32 ± 3.54 ml CO2 min−1, and flight speeds 5.65 ± 0.47 and 6.27 ± 0.68 m s−1 for M. currentium and M. sinaloae respectively. Metabolic rate during flight was higher for the M. currentium than for the similar-sized, but broader-winged frugivore Carollia sowelli, corroborating that broad-winged bats are better adapted to flying in confined spaces. These higher metabolic costs of manoeuvring flight may be caused by having to fly slower than the optimal foraging speed, and by the additional metabolic costs for centripetal acceleration in curves. This may preclude molossids from foraging efficiently between canopy trees or in forest gaps. The surprisingly brief burst of foraging activity at dusk of many molossids might be related to the cooling of the air column after sunset, which drives airborne insects to lower strata. Accordingly, foraging activity of molossids may quickly turn unprofitable when the abundance of insects decreases above the canopy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

AP13CE:

13C Excess enrichment (in atom %)

AR:

Aspect ratio

F lift :

Lift force (N)

F centripetal :

Centripetal force (N)

g :

Gravitational force (9.81 m s−2)

m b :

Body mass (kg)

MC:

Molossus currentium

MS:

Molossus sinaloae

k c :

Fractional turnover (min−1)

N c :

Body bicarbonate pool (mmol)

t :

Time (min)

v :

Flight speed (m s−1)

v flown :

Flown flight speed (m s−1)

v mr :

Maximum range flight speed (m s−1)

v mp :

Minimum power flight speed (m s−1)

\( \dot{V}_{{{\text{CO}}_{ 2} }} \) :

Rate of CO2 production (ml min−1)

References

  • Aubauer R (1994) Dreidimensionale Flugbahnverfolgung von Fledermäusen Fortschritte der Akustik – DAGA 94. DPG-Verlag, Bad Honnef, Germany

  • Barton AM, Fetcher N, Redhead S (1989) The relationship between treefall gap size and flight flux in a Neotropical rain forest in Costa Rica. J Trop Ecol 5:437–439

    Article  Google Scholar 

  • Chapman JW, Reynolds DR, Smith AD (2003) Vertical-looking radar: a new tool for monitoring high altitude insect migration. Bioscience 53:503–511

    Article  Google Scholar 

  • Dechmann DKN, Kranstauber B, Gibbs D, Wikelski M (2010) Group hunting: a reason for sociality in molossid bats? PLoS ONE 5:e9012

    Article  PubMed  Google Scholar 

  • Dechmann DKN, Ehret S, Gaub A, Kranstauber B, Wikelski M (2011) Low metabolism in a tropical bat from lowland Panama measured with heart rate telemetry: an unexpected life in the slow rate. J Exp Biol 214:3605–3612

    Article  PubMed  Google Scholar 

  • Engel S, Lease HM, McDowell NG, Corbett AH, Wolf BO (2009) The use of tunable diode laser absorption spectroscopy for rapid measurements of the δ13C of animal breath for physiological and ecological studies. Rapid Commun Mass Spectrom 23:1281–1286

    Article  PubMed  CAS  Google Scholar 

  • Esbérard CEL, Bergallo HG (2010) Foraging activity of the free-tailed bat Molossus molossus (Chiroptera; Molossidae) in southeastern Brazil. Braz J Biol 70:011–1014

    Google Scholar 

  • Fenton MB (1972) The structure of aerial-feeding bat faunas as indicated by ears and wing elements. Can J Zool 50:287–296

    Article  Google Scholar 

  • Freeman PW (1979) Specialized insectivory: beetle-feeding and moth eating molossid bats. J Mammal 60:467–479

    Article  Google Scholar 

  • Garland T Jr, Adolph SC (1994) Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol Zool 67:707–828

    Google Scholar 

  • Grodzinski U, Spiegel O, Korine C, Holderied MW (2009) Context-dependent flight speed: evidence for energetically optimal flight speed in the bat Pipistrellus kuhlii? J Anim Ecol 78:540–548

    Google Scholar 

  • Hails CJ (1979) A comparison of flight energetics in hirundines and other birds. Comp Biochem Physiol 63:581–585

    Article  Google Scholar 

  • Hambly C, Voigt CC (2011) Measuring energy expenditure in birds using bolus injections of 13C labelled Na-bicarbonate. Comp Biochem Physiol A 158:323–328

    Article  Google Scholar 

  • Hambly C, Harper EJ, Speakman JR (2002) Cost of flight in the zebra finch (Taenopygia guttata): a novel approach based on elimination of 13C labelled bicarbonate. J Comp Physiol B 172:529–539

    Article  PubMed  CAS  Google Scholar 

  • Hambly C, Pinshow B, Wiersma P, Verhulst S, Piertney SB, Harper EJ, Speakman JR (2004a) Comparison of the cost of short flights in a nectarivorous and a non-nectarivorous bird. J Exp Biol 207:3959–3968

    Article  PubMed  CAS  Google Scholar 

  • Hambly C, Harper EJ, Speakman JR (2004b) The energy cost of loaded flight is substantially lower than expected due to alterations in flight kinematics. J Exp Biol 207:3969–3976

    Article  PubMed  CAS  Google Scholar 

  • Holderied MW, von Helversen O (2003) Echolocation range and wingbeat period match in aerial-hawking bats. Proc Roy Soc B 270:2293–2299

    Article  CAS  Google Scholar 

  • Holderied MW, Jones G, von Helversen O (2006) Flight and echolocation behaviour of whiskered bats commuting along a hedgerow: range-dependent sonar signal design. Doppler tolerance and evidence for ‘acoustic focussing’. J Exp Biol 209:116–1826

    Google Scholar 

  • Jung K, Kalko EKV (2011) Adaptability and vulnerability of high flying neotropical aerial insectivorous bats to urbanization. Diversity Distrib 17:1–13

    Article  Google Scholar 

  • Masman D, Klaasen M (1987) Energy expenditure during free flight in trained and free-living Eurasian kestrels Falco tinnunculus. Auk 104:603–616

    Google Scholar 

  • McCracken GF, Gillam EH, Westbrook JK, Lee YF, Jensen ML, Balsley BB (2008) Brazilian free-tailed bats (Tadarida brasiliensis: Molossidae, Chiroptera) at high altitude: links to migratory insect populations. Integr Comp Biol 48:107–118

    Article  PubMed  Google Scholar 

  • Norberg UM (1986) Evolutionary convergence in foraging niche and flight morphology in insectivorous aerial hawking birds and bats. Ornis Scand 117:253–269

    Article  Google Scholar 

  • Norberg UM, Rayner JMV (1987) Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Phil Trans Roy Soc Lond B 316:335–427

    Article  Google Scholar 

  • Pennycuick CJ (1975) Mechanics of flight. In: Farner DS, King JR (eds) Avian biology, vol 5. Academic Press, London, pp 1–75

  • Pennycuick CJ (2008) Modelling the flying bird. Academic Press, London

    Google Scholar 

  • Rayner JMV (1982) Avian flight energetics. Ann Rev Physiol 44:109–119

    Article  CAS  Google Scholar 

  • Rayner JMV (1999) Estimating power curves of flying vertebrates. J Exp Biol 202:3449–3461

    Google Scholar 

  • Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge

    Google Scholar 

  • Schmidt-Wellenburg CA, Biebach H, Daan S, Visser GH (2007) Energy expenditure and wing beat frequency in relation to body mass in free flying Barn Swallows (Hirundo rustica). J Comp Physiol B 177:327–337

    Article  PubMed  Google Scholar 

  • Speakman JR (1997) Doubly labeled water: theory and practice. Chapman and Hall, London

    Google Scholar 

  • Speakman JR, Racey PA (1991) No cost of echolocation for bats in flight. Nature 350:421–423

    Article  PubMed  CAS  Google Scholar 

  • Speakman JR, Thomas D (2003) Physiological ecology and energetics of bats. In: Kunz TH, Fenton BM (eds) Bat ecology. The University of Chicago Press, Chicago, pp 430–492

    Google Scholar 

  • Speakman JR, Thomson SC (1997) Validation of the labelled bicarbonate technique for measurement of short-term energy expenditure in the mouse. Z Ernährungswiss 36:273–277

    Article  PubMed  CAS  Google Scholar 

  • Vaughan TA (1986) Morphology and flight characteristics of molossid bats. J Mammal 47:249–260

    Article  Google Scholar 

  • Voigt CC, Lewanzik D (2011) Trapped in the darkness of the night: thermal and energetic constraints of daylight flight in bats. Proc Roy Soc Lond B 278:2311–2317

    Google Scholar 

  • Voigt CC, von Helversen O, Michener R, Kunz TH (2001) The economics of harem maintenance in the sac-winged bat, Saccopteryx bilineata (Emballonuridae). Behav Ecol Sociobiol 50:31–36

    Article  Google Scholar 

  • Voigt CC, Kelm DH, Visser GH (2006) Field metabolic rates of phytophagous bats: do pollination strategies of plants make life of nectar-feeders spin faster? J Comp Physiol B 176:213–222

    Article  PubMed  Google Scholar 

  • Voigt CC, Schuller BM, Greif S, Siemers BM (2010) Perch-hunting in insectivorous Rhinolophus bats is related to the high energy costs of manoeuvring in flight. J Comp Physiol B 180:1079–1088

    Article  PubMed  Google Scholar 

  • Voigt CC, Schneeberger K, Voigt-Heucke SL, Lewanzik D (2011) Rain increases the energy cost of bat flight. Biol Lett 7:793–795

    Google Scholar 

  • Winter Y, von Helversen O (1998) The energy cost of flight: do small bats fly more cheaply than birds? J Comp Physiol B 168:105–111

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Daniel Lewanzik, Ivailo Borrisov, Karin Schneeberger and Silke L. Voigt-Heucke for help during the 2010 field work, and Daniela Rabaiotti, Eugenia Cordero, Frederick Sutton and Luke Worley for help during the 2011 field work. They thank Silke Voigt-Heucke for comments on an earlier draft, the organisation for tropical studies for allowance to work at La Selva biological station and the authorities for granting research permission.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christian C. Voigt.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Voigt, C.C., Holderied, M.W. High manoeuvring costs force narrow-winged molossid bats to forage in open space. J Comp Physiol B 182, 415–424 (2012). https://doi.org/10.1007/s00360-011-0627-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-011-0627-6

Keywords

Navigation