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Volume 92, No. 3 September 2017THE QUARTERLY REVIEW OF BIOLOGY

PRINCIPLES AND PATTERNS OF BAT MOVEMENTS:FROM AERODYNAMICS TO ECOLOGY

Christian C. Voigt*

Department of Evolutionary Ecology, Leibniz Institute for Zoo and Wildlife Research

10315 Berlin, Germany

Institute of Biology, Freie Universität Berlin

14195 Berlin, Germany

e-mail: [email protected]

Winifred F. Frick

Bat Conservation International

Austin, Texas 78716 USA

Ecology and Evolutionary Biology, University of California

Santa Cruz, California 95064 USA


Marc W. Holderied

School of Biological Sciences, Bristol University

Bristol BS8 1TQ United Kingdom


Richard Holland

School of Biological Sciences, Bangor University

Bangor, Gwynedd LL57 2UW United Kingdom


Gerald Kerth

Applied Zoology and Conservation, University of Greifswald

D-17489 Greifswald, Germany


The Quarterly Review of Biology, September 2017, Vol. 92, No. 3

Copyright © 2017 by The University of Chicago Press. All rights reserved.

0033-5770/2017/9203-0002$15.00

267

This content downloaded from 137.222.190.033 on February 16, 2018 07:18:24 AMAll use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).

268 Volume 92THE QUARTERLY REVIEW OF BIOLOGY

Marco A. R. Mello

Department of General Biology, Federal University of Minas Gerais

31270-901 Belo Horizonte, MG, Brazil


Raina K. Plowright

Department of Microbiology and Immunology, Montana State University

Bozeman, Montana 59717 USA


Sharon Swartz

Department of Ecology and Evolutionary Biology and School of Engineering, Brown University

Providence, Rhode Island 02912 USA


Yossi Yovel

Department of Zoology, Faculty of Life Sciences, and the “Sagol” School of Neuroscience,

Tel-Aviv University

Tel-Aviv, Israel


* Coauthorship order is alphabetical

keywords

A

biomechanics, cognition, echolocation, energetics, emerging infectious diseases,migration, mutualism, sociality

abstract

Movement ecology as an integrative discipline has advanced associated fields because it presents notonly a conceptual framework for understanding movement principles but also helps formulate predictionsabout the consequences of movements for animals and their environments. Here, we synthesize recent stud-ies on principles and patterns of bat movements in context of the movement ecology paradigm. The motioncapacity of bats is defined by their highly articulated, flexible wings. Power production during flight fol-lows a U-shaped curve in relation to speed in bats yet, in contrast to birds, bats use mostly exogenous nu-trients for sustained flight. The navigation capacity of most bats is dominated by the echolocation system,yet other sensory modalities, including an iron-based magnetic sense, may contribute to navigation de-pending on a bat’s familiarity with the terrain. Patterns derived from these capacities relate to antagonisticand mutualistic interactions with food items. The navigation capacity of bats may influence their soci-ality, in particular, the extent of group foraging based on eavesdropping on conspecifics’ echolocationcalls. We infer that understanding the movement ecology of bats within the framework of the movementecology paradigm provides new insights into ecological processes mediated by bats, from ecosystem servicesto diseases.

Introduction

BATS are an evolutionary and ecologicalsuccess story. Since their first appear-

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ance in the fossil record around 50 millionyears ago, they have radiated into numerousclades.Having reached all continents except

2.190.033 on February 16, 2018 07:18:24 AMs and Conditions (http://www.journals.uchicago.edu/t-and-c).

MOVEMENT ECOLOGY OF BATSSeptember 2017 269

for Antarctica, bats now count formore than1300 species (Tsang et al. 2016). Two adap-tations seem to be central for their success—powered flight and echolocation—and bothof these adaptations are key to understand-ing their movement ecology. Building a con-ceptual framework that accounts for thecauses,mechanisms, andspatiotemporalpat-ternsofbat movements in an ecological andevolutionary context is a serious challenge.Fortunately, the seminal paper of Nathanet al. (2008), which helped forge movementecology as a recognized subfield, synthesizeddiverse areas of study to advance a novel con-ceptual framework that provides a scaffold toconnectmanyaspectsof batmovement.Here,we clarify the understanding that bat move-ment ecology cannot be achieved through ac-cumulation of isolated data, but only throughinvestigating the processes of movement atmultiple scales.

We discuss recent progress in some of thefundamental aspects of bat movement ecol-ogy. In the first section, we introduce themovement ecology paradigm and suggesthow to use it to study the spatial behaviorsof bats. In the second section, we summa-rize current advances in the understandingof some of the mechanistic components ofmovement (sensu Nathan et al. 2008) andfocus on the motion capacity (morphology,physiology) and navigation capacity of bats(sensory ecology). In the third section, wefocus on external factors, and review someof the consequences of bat movement, par-ticularly in light of recently emerging fieldssuch as foraging, sociality, and disease trans-mission. Finally, we point to important gapsin knowledge and propose new avenues forresearch.

movement ecology and bats

The conceptual framework of movementecology (Nathan et al. 2008) is a powerfuland productive tool for understanding ani-mal movement across scales. Briefly, theauthors suggested four major mechanistic,interlinked components to explain variationin organismal movement: the internal state(whymove?),motioncapacity(howtomove?),navigation capacity (when and where tomove?), and external factors affectingmove-

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ment.Letususe as anexample themigrationof temperate bats. Several bat species fromtemperate zonesmigrate seasonally betweenanareawheretheyspendmostof thesummerand they give birth to their offspring, and an-other area where they hibernate (Figure 1A;Popa-LisseanuandVoigt 2009).The internalstate, or motivation, for bats during springmigration is to reach an area that offers suffi-cient resources for reproduction (i.e., preg-nancy, lactation, and successful weaning ofjuveniles). The motion capacity of bats in-volves theirphysiological conditionafterhav-ing emerged from hibernation, the necessityto fattenupbeforemigration, and thephysio-logical constraints imposed on female bats byreproduction (e.g., using torpor during stop-overs might compromise offspring growth).Navigation capacity involves orientation inuncharted terrain when moving over longdistancesbecausesuccessfullynavigatingbatsuse various sensory modalities (such as mag-netic sensing, vision, and olfaction) to findthewaytothepreferredsummerarea.Extrin-sic factors affecting spring migration mayinclude ambient temperature, precipitation,and food density, for example.

Onceestablishedat summerhabitats,move-ment patterns change for females due to theprimary focus on reproduction (Figure 1B).Here, bats most likely move in familiar ter-rain and accordingly prioritize other navi-gational strategies, which involve differentsensorymodalities thanthoseusedduringmi-gration. Their motion capacity is potentiallydictatedby theenergetic andtimeconstraintsrelated to pregnancy, lactation, territorial be-havior, or mating. Variations in this thememight occur for bats in the summer habitat,whentheyareconstrained in theirmovementto a central place—e.g., byhaving to return tothe maternity colony for nursing juveniles(females) or by defending a mating roost(males). Then bats may restrict their move-ments to a minimum and commute quicklytoward preferred foraging patches wherethey perform so-called area-restricted forag-ing (Figure 2B).

In contrast, after maternity colonies havedispersed, batsmight change theirmovementbehavior when exploring the area for alter-native roosts or potential mates (Figure 2A).Wenote,however, that thedescribedschemes



are massively simplified. Ecological and be-havioral variation observed in the more than1300bat speciesworldwide likely encompassothermovement patterns of yet undescribedcomplexity. Thus, we envision the task of thisreview to stimulate research in this area toimprove our understanding of the mecha-nisms and consequences of bat movements.

mechanisms of bat movements

Here, we will focus on two out of the fourmechanisms defined by Nathan et al. (2008):motion and navigational capacity. The moti-vation for moving (internal state) is difficultto quantify, but could best be described bythe need for survival (escaping harsh condi-tions or predators, searching for food) andreproduction (searching for a mate, givingbirth, suckling juveniles). The external fac-tors are as manifold as the environments inwhich bats live. Thus, it would be beyond thescope of this review to provide a comprehen-sive overview of all relevant external factorsaffecting bat movements.

Motion Capacity

morphology and aerodynamics

Understanding the structure and functionof thebatflight apparatus canplay a valuablerole in how we interpret other elements ofthe movement ecology paradigm—why and


where batsmove. The primarymode of loco-motion for bats isflight. Theflight apparatusof bats shares similarities with that of otherflying animals, but bats differ from insects,pterosaurs (theextinct cladeof reptiles capa-ble of powered flight), and birds in distinc-tive traits. Bat wings are framed by bones,like those of birds and pterosaurs. However,in contrast to the bird wing skeleton, bat wingbones vary greatly in their density, relativeproportion of mineral and protein, and me-chanical properties. Moreover, bones of thebat hand-wing are far less stiff than the bonesinmost vertebrate limbs (Swartz andMiddle-ton 2008; Dumont 2010). Bat wings possesssubstantially more joints than wings of anyother animal. To govern this large array ofdistinct elements, bat wings are controlledby a wider repertoire of muscles than thoseofotherflyers. Inaddition, thetissuebetweenthebones,unusually thin skinplusothercon-nective tissues, is also highly compliant incomparison to relatively stiff chitinous cuti-cle of insect wings and keratinous feathersof birds (Cheney et al. 2015). The skin of thebat wing is not only highly deformable andsoft, its stiffness can be actively controlled byarrays of muscles imbedded within the der-mis (Cheney et al. 2014). Together, this suiteof unique attributes provides bats with wingscharacterized by a high level of flexibility un-der specific control of themotor system.

Direct measurements of the structure andmotion of wakes shed by flying animals al-

Figure 1. Schematic Pictures of Two Contrasting Movement Patterns Suggested For a Temperate

Zone Bat

Long-distance migration between summer and winter roosts (A) and short foraging flights around the sum-mer roosts (B). Note differences in spatial and temporal scales between A and B. Depicted migratory movementsinclude several seasonal trips during subsequent years, whereas depicted foraging movements include trip dur-ing several consecutive days. See the online edition for a color version of this figure.



low researchers to assess the aerodynamicforces they produce (Spedding et al. 2003).Recently, application of particle image velo-cimetry (PIV) has shown that the wakes ofbats, like their wings, are generally similarto those of birds, but distinct from those ofinsects (Figure 3; Bomphrey 2012). In bats,themajority of the aerodynamic force is pro-duced during the downstroke. Also, wakesproduced by bats tend to be more complexthan those of birds of similar size whenflyingat similar speed, perhaps because of differ-ences in howdrag is overcome (Hedenströmet al. 2007;Hubel et al. 2010, 2012;Wolf et al.2010). During hovering and slow forwardflight, some bats produce stable leading edgevortices (LEVs; Muijres et al. 2008, 2014;Chin and Lentink 2016). In general, LEVsare often observed in slow animal flight, andgenerate additional lift in conditions thatwould otherwise typically lead to stall; in somebats, they may also form during the upstroke.

The distinctive structural design of batwings, the physical substrate for flight, playsa significant role in theirmovement ecology.A highly articulated wing, withmany degreesof freedomunder direct control ofmuscularactuation, provides multiple kinematic strat-egies to achieve a particular locomotor task;in this case, implementing a wingbeat cyclethat generates aerodynamic forces of spe-cific magnitude and orientation. Bats show ahigh degree of individual variation in three-


dimensional motions of the wing. Detailedanalyses of wingbeat kinematics of bats overa range of speeds or carrying loads demon-strate that bats achieve increases in aerody-namic forces in various ways, for example, byaltering speed of motion or by changing de-gree to which particular joints are extended(Hubel et al. 2010; Iriarte-Diaz et al. 2012).Actively controllable skin stiffness confersa valuable dimension to this dynamic flex-ibility. Camber, the front-to-back curvatureof an airfoil, has a strong influence on lift,andmodulation of wingmembrane stiffnessby contraction and relaxation of musclesin the skin can thus directly affect aerody-namics (Spedding et al. 2003; Song et al.2008). Taken together, the unique architec-ture of the skeleton, muscles, and skin of batwings may confer versatility in flight behaviorthat exceeds approximations derived fromaerodynamic theory and that enables batsto accomplish not only challenging aerial be-haviors such as hovering flight or landinghead-under-heels (Bergou et al. 2015), butalso the fastest powered flight speeds re-corded for any vertebrate (McCracken et al.2016).

the power requirements and fuel

sources of bat flight

Aerial locomotion is energetically costlybecause animals have to overcome gravity to

Figure 2. Schematic Picture of Two Contrasting Movement Patterns Observed in Common Noctule

Bats (Nyctalus noctula)

Suggested combined exploratory and foraging flight (A) and commuting flights with area restricted foragingat a resource dense patch (B). Modified from Roeleke et al. (2016). See the online edition for a color version ofthis figure.



remain airborne and drag to move forward.According tofixed-wingaerodynamic theory,mechanical and thus also metabolic powerrequirements of flight should vary with flightspeed in a U-shaped manner (Pennycuick1975; Rayner 1982). Almost all previous stud-ies confirm this expectation (for an example,see Figure 4), yet they were done in bats fly-ing under controlled conditions in a windtunnel with quasi-laminar air flow. This situ-ation is almost never found in nature. Real-istically, foraging bats usually fly in curvedtrajectories, for example, to avoid obstacles,to navigate along nonlinear landscape fea-tures, or to pursue insects on the wing. Flightpaths that deviate from the linear trajecto-ries tested in the laboratory, such as in a clut-tered habitat, may add substantial energetic


costs to flying bats (Voigt et al. 2010a). Forexample, countering centripetal accelerationmay even double or triple flight costs, de-pending on the curvature of the flight pathand the speed at which bats are flying (Voigtand Holderied 2012). This may explain whyfast-flying species with high aspect ratio, suchas molossid bats, are not able to efficientlyexploit resources from smaller spaces likecanopy gaps. Additional environmental con-ditions, such as precipitation,may further in-crease the metabolic requirements of flight(Voigt et al. 2011).

Similar to flying birds, bats face a signifi-cant difference in metabolic rates when air-borne compared to when resting (Winterand von Helversen 1998; Voigt et al. 2012a).These power requirements have to be sup-

Figure 3. Wake Vortices of a Flying Bat

Vortices generated by the body and wings of a 20 g nectar-feeding bat, Leptonycteris yerbabuenae, flying fromleft to right (as indicated by the arrow) in a wind tunnel, as seen from three different perspectives: (A) side view,(B) top view, and (C) oblique top view. Vortices represent surfaces of equal absolute vorticity, indicated in darkgray for downwash and light gray for upwash movements. Reprinted with permission from Hedenström andJohansson (2015). See the online edition for a color version of this figure.



plied by some source of quickly availablenutrient. The source of energy during theimmediate onset of flight is glycogen, a mac-romolecule that is available in flight musclesor in the liver. The disadvantage of glyco-gen is its low energy density, because as a hy-drophilic carbohydrate it is not stored in acompact form similar tohydrophobic triacyl-glycerols (TAG) in adipocytes. On the otherhand, hydrophobic and relatively large fattyacids derived fromTAG are difficult to trans-port in the aqueousmedium of cells and alsoacross membranes (Weber et al. 1996). Thisis particularly true for mammals that seemto lack efficient transporting enzymes thatare available, for example, to birds (McGuireandGuglielmo2009;Weber2009, 2011;Price2010). As a consequence, bats use consumednutrients directly and rapidly as an oxidativefuel (Voigt and Speakman 2007;Welch et al.2008; Amitai et al. 2010; Voigt et al. 2012b).Further, in contrast to birds, bats cannot relyonTAGfromfatdeposits as thesoleoxidativefuel to remain airborne (but see McGuireet al. 2013). For example, nectar-feeding orfruit-eating bats that ingest mostly carbohy-drates power flight almost exclusively by oxi-dizing immediately consumed sugars (Voigtand Speakman 2007; Welch et al. 2008; Ami-tai et al. 2010). Failure tofindnectar or fruitsmay ultimately force them to land until suffi-cient glycogenhasbeen synthesized topowerthe next takeoff. Thus, nectar- and fruit-eating bats seem to be on a constant rush for


their sugary diet (Kelm et al. 2011). For mostother bats, insects are the main food sourceand these are mostly rich in proteins. Recentstudies pointed out that insectivorous batsfuel their high energy expenditure throughthe rapid oxidation of insect nutrients (Voigtet al. 2010b). Migratory bats that travel longdistances have been observed to hunt enroute, albeit rarely (Krüger et al. 2014; Voigtet al. 2017). During this formof aerial refuel-ing, migratory bats oxidize the protein por-tion of consumed insects and route the fatportion to their own body reserves. This strat-egy enables migratory bats to make use offatty acids later, for example, when ambientconditions deteriorate along their journeyor latest when entering torpor at their hiber-nacula (Voigt et al. 2012b).

Navigation Capacity of Bats

Any organism with an ability to move re-quires an ability to navigate and thus navi-gation capacity is an essential component ofunderstanding movement ecology (Nathanet al. 2008). An animal’s navigation capacitygreatly influences the movement path and,ultimately, the life-history strategy availableto the animal. For example, migration andlong-distance central place breeding requirean ability to return to a knowngoal fromareasnot previously visited (Papi 1992). The termnavigation has various definitions depend-ing on the context, but at its broadest is theability to orient toward a known goal (Griffin1952; Papi 1992). How animals do this de-pends on their sensory capacity and familiar-ity with the environment they are navigatingthrough. Animals can employ a variety ofmechanisms to navigate, from simple trailfollowing or beaconing through route reca-pitulation and path integration to complexinternally represented maps of space (Papi1992; Jeffery 2003). With the capacity forboth long-distance foraging movements andreturnmigrations, bats demonstrate the abil-ity to navigate across different scales. Trans-location manipulations have demonstratedthat bats can move not only in their familiarenvironment, but also can navigate fromareas never previously visited (Holland 2007),so-called “true navigation” (Holland 2014).

Figure 4. Metabolic andMechanicalFlightPower

(W) of a Bat in Relation to Flight Speed

Flight power of a 20 gCarollia perspicillata in a wind tun-nel at varying wind speeds. From von Busse et al. (2013).See the online edition for a color version of this figure.



navigation over familiar terrain

In a familiar area, learned landmarks canprovidecues thatareused to indicatecurrentpositions with respect to the goal. For mostanimals this means visual cues but, for bats,echolocation is a secondmechanismbywhichlandmarks can potentially provide the refer-ence.Anumberof experiments in laboratorysettings indicate that echolocation is used tostoreandrepresent space inthebrain fornav-igation (Geva-Sagiv et al. 2015), but whetherthis is used for navigation over longer dis-tances during commuting or foraging in a fa-miliar area is uncertain, due to its relativelyshort range(approximately30m).Neverthe-less, some exploratory work in the 1960s in-volving blindfolded bats did find that theywere able to home from within approxi-mately 15 km (Williams and Williams 1967)and that if hearing was also removed theycould no longer do so (Stones and Branick1969).Whether this was due to a nonspecificeffect of removing two crucial senses ratherthan an impact on a navigation mechanismremains unclear, but this should be revisited.Other animals such as blind cave fish areable to use short-range sensory systems (thelateral line) to link landmarks not simulta-neously in range and remember order, andso it is possible that bats can learn routesin this way (de Perera 2004). Visual cues ap-pear to be important for navigation in batsbeyond this range (Williams and Williams1967; Tsoar et al. 2011).

navigation in unfamiliar terrain:

true navigation

Animals that cancorrect fordisplacementsoutside their normalhome range and returnto a known goal are said to display true nav-igation (Holland 2014). It is hypothesizedthat true navigation is a two-step process,whereby the animal first locates its positionwith respect to its desired goal (themap step)and then identifies the direction to move toreach the goal (the compass step). This hasbeen termed the map and compass theoryof true navigation (Kramer 1953). A numberof displacement experiments in the 1950sand 1960s indicated that some bat species


could home from long distances (as much as450 km), indicating a true navigation capac-ity (Davis 1966). Nevertheless, until recently,nothing was known about the sensory sys-tems or environmental cues used in true nav-igation in bats (Holland 2007). However, areemerging field of study of bat navigationhas indicated that some species possess amag-netic compass sense (Holland et al. 2006,2010) and that this is calibrated by polarizedlight cues at sunset (Greif et al. 2014; but seeLindecke et al. 2015), an ability not sharedby any other mammal taxon to our currentknowledge. Further evidence suggests thatthe magnetic sense detects polarity (Wanget al. 2007) and is detected by a magneticparticle-based sensory system (Holland et al.2008). Whether bats also possess an inclination-based magnetic compass, detected throughphotoreceptive molecules in the eye as birds(Mouritsen2012)and somerodentsdo(Mal-kemper et al. 2015), remains to be seen. Thecues used by animals to locate their positionin unfamiliar areas (step one in true naviga-tion) have remained controversial, but gath-ering bodies of evidence suggest that theEarth’s magnetic field and olfactory cues mayboth play a role (Holland 2014). As of yet, noinvestigation has beenmade to study the roleof these cues in true navigation in bats, al-though in birds, the magnetite-based senseis linked to the map sense rather than thecompass sense (Holland and Helm 2013).Thus, the presence of a magnetic particlesense in bats hints at the possibility of its rolein the true navigation map.

In addition to true navigation, it also re-mains to be determined whether bats mak-ing their first migratory journey do so on thebasis of an inherited compass direction, as isthe case in songbirds, or whether they relyentirely on following conspecifics. A recentstudy of the relatedness of migratory batskilled at wind farms did not provide any evi-dence for social transmission of migration(Baerwald and Barclay 2016).

orientation in familiar terrain,

i.e., sensory-motor control

Most bat species use biological sonar forclose-range orientation and route following



( Jones and Teeling 2006), two navigationstrategies that are important for many navi-gation tasks. Since the acoustic behaviors ofseveral bat species’ biosonar have been char-acterized in sufficient detail (e.g., Rhino-lophidae: Neuweiler 2000; Schnitzler andDenzinger 2011) and because the physicallaws of echo generation and propagationcan be modeled with sufficient accuracy,recent research efforts have focused on ex-tracting movement rules from behavioralmovement data by estimating the availableechoic information (e.g., Giuggioli et al.2015; Vanderelst et al. 2015). Vanderelstand colleagues modeled echoacoustic in-puts and auditory processing to understandthe available sensory information as a func-tion of position and orientation in artificialandnatural two- andthree-dimensionalhabi-tats (Vanderelst et al. 2015). Virtual bats withnaturalistic constraints on movement abili-ties navigated successfully through artificialmazes based on biosonar input. Successfulnavigation and obstacle avoidance was facili-tated by very simple stochastic parameters,without the need for reconstructing the spa-tial dimension of the environment (Vander-elst et al. 2015). This example highlights howsurprisingly simple rules of sensory-motor in-tegration can give rise to complex and natu-ralistic movement coordination patterns.

Sensory systems are not sufficient fornavigation on their own. A complementarynecessary component is a mechanism fortranslating sensory input into movement.The different types of sensory modalitiesmentioned above can each provide the batwith an estimate of the azimuth, its angularposition in relation to the sun or moon, andsometimes distance to its target (e.g., homeroost, foraging grounds, hibernation cave).Thebatmust thenusesomenavigationmech-anism to move toward its target. When thetarget (or a landmark on the way) is withinthe sensing range, the bat can fly directly to-ward it, but when navigating over many ki-lometers, this is often not the case. In suchlong-range navigations, a bat will probablyupdate its sensory estimations on the wayand will correct its movement accordingly.We currently have little understanding ofhow animals translate sensory information


into movement. Data and theory suggest thatinmany cases flying in a straight trajectory to-ward the target might not be the outcome ofthis process. External factors such as weatherconditions can play a role in the selection ofa route—for instance, a bat might try to avoidheadwind (Sapir et al. 2014). A curved trajec-torymight also stem from sensory limitations(Benhamou 2003; Bar et al. 2015).

Consequences of Bat Movements

bat movements and feeding:

antagonisms and mutualisms

Amajor factor that forcesbats tomoveonadaily basis is the search for food. In this con-text, their interactions with amyriad of otherorganisms play a major role in evolutionaryprocesses, as bats are important arthropodpredators, seed dispersers, and pollinatorsworldwide (Kunz et al. 2011; Fleming andKress 2013). Some bat species have markeddietary preferences and need to or choose tofly long distances to find their favorite food(Tsoar et al. 2011; Fahr et al. 2015; Oleksyet al. 2015; Abedi-Lartey et al. 2016; Roelekeet al. 2016). The sensory systems of bats, par-ticularly their biosonar, used for moving indifferent habitats, may be a strong selectiveforce on the dietary items they consume.Some moths may detect echolocation callsof insect-feeding bats, and the coevolution-ary arms race between predator and preyhas led to highly developed auditory abili-ties in both. In addition, effective counter-strategies, such as stealth-hawking (Goerlitzet al. 2010) and counterclicking of moths todeter approaching bats (Ratcliffe and Ful-lard 2005; Corcoran et al. 2009), have evolvedas part of this antagonistic interaction.

Sensory abilities of bats also influence fruitorfloral traits. For example, the specific smellof bat-dispersed fruits and the shapes offloralstructures, such as in echo-reflecting tropi-cal vines (von Helversen and von Helversen1999) and pitcher plants (Simon et al. 2011;Schöner et al. 2015), are largely influencedby the navigational capacities of bats. Wespeculate that a combination of motion andnavigationcapacity of batsmay affect seeddis-persal orcross-pollinationand, consequently,



thus the distribution of plants in general andreproductive success of individual plants inparticular. At least 172 species of pteropodidbats in the Old World and 106 species ofphyllostomid bats in the New World feed onfruits or flowers (Fleming and Kress 2013),and most of those bats deliver mutualisticservices to the plants they visit (but see Wag-ner et al. 2015). Phyllostomid bats that areknown to pollinate at least 137 plant speciesof 34 families and disperse the seeds of atleast 306 plant species of 57 families (Lobovaet al. 2009). Pteropodid bats deliver pollina-tion and dispersal services of high economicvalue in the Paleotropics (Ghanem andVoigt 2012), whereas phyllostomid bats playan important role in forest regeneration inthe Neotropics (Muscarella and Fleming2007). Phyllostomid bats visit an impres-sive diversity of plants, yet their pollinationservices typically occur within the familiesAgavaceae,Bignoniaceae,Bombacaceae,Cac-taceae, and Fabaceae, and their seed disper-sal services on their families Cecropiaceae,Clusiaceae, Moraceae, Piperaceae, and So-lanaceae (Fleming and Kress 2013). Thoseplant families often appear as hubs or con-nectors in bat-plant networks (Mello et al.2015), so their phenologymight have a stronginfluence on phyllostomid bat movements(Andrade et al. 2013).

Phyllostomid and pteropodid bats that de-pend on flowers and fruits for food mightbe, in some cases, forced to forage mainly inthe habitats where their favorite food plantsare easier to find, no matter how far apartthey are (Mildenstein et al. 2005; Thies et al.2006). The most well-known example of mi-gratory phytophagous bats that move longdistanceswhile foraging are someglossopha-gines, especially of the genus Leptonycteris,which move over hundreds of kilometersacross the Sonoran Desert in northern Mex-ico and into the southwestern United Stateseach year to follow the blooming of cactiand agaves (Wilkinson and Fleming 1996).

The feeding preferences of frugivorousbats seem to influence their foraging deci-sions even within a population as, for in-stance, individual Sturnira lilium differ inthe fruit genera they prefer (Muylaert et al.


2014), and consequently differ also in themain habitats they use, depending on theavailability of different edible fruits. Novelevidence points out that nomadism and mi-gration may be influenced by flower andfruit availability in some phyllostomid bats,such as Pygoderma bilabiatum (Esbérard et al.2011) and Sturnira lilium (Mello et al. 2008).In summary, a combination of dietary spe-cialization, plant phenology (e.g., unpredict-able fluctuations), plant distribution (e.g.,patchiness), and climate seasonality appearskey to understanding themovement ecologyof these and other phytophagous bats.

interactions between sociality and

movement capacity of bats

In many social species, individuals stronglybenefit from coordinating their collectivemovements. Examples include flocks of mi-grating birds and fish swarms that escapefrom predators, and bats that collectivelymove from roost to roost or that hunt to-gether. To achieve coordination, the individ-uals involved need to transfer information toone another about their position and theiractivities and intentions. In bats, informationtransferhasbeen shown tohelpcolonymem-bers to coordinate roosting behavior (KerthandReckardt 2003; Kerth et al. 2006; Fleisch-mann et al. 2013) and group foraging (Wil-kinson 1992; Dechmann et al. 2009; Cvikelet al. 2015a). In some of these species, com-munal roosts serve as centers where colonymembers exchange information about re-sources (e.g., Wilkinson 1992) but bats canalso benefit from social information out-side the colony whenon thewing (Wilkinson1992; Dechmann et al. 2009; Cvikel et al.2015a).

Flight involves high metabolic rates andthe strong reliance of bats on recently in-gested food items as the predominant ox-idative fuel may force bats to forage withparticularly high efficiency, for example, byeavesdropping on conspecifics. Duringflight,echolocating bats constantly adjust their bio-sonar signals based on the task they are per-forming thus revealing information that isavailable to other bats about their forag-



ing. For example,many bats emit a typical se-quenceofcalls (termeda feedingbuzz)whenattacking prey, thus inadvertently announc-ing thepresenceof food topotential compet-itors (Schnitzler et al. 2003). Indeed, manybat species have been found to be attractedto buzzing conspecifics (Balcombe and Fen-ton 1998; Fenton 2003; Gillam 2007; Dech-mann et al. 2009; Knörnschild et al. 2012).Importantly, due to the physics of soundpropagation, the range fromwhichabuzzingconspecific can be detected is around an or-der ofmagnitude larger than the range fromwhich an insect can be detected (Cvikel et al.2015a; Giuggioli et al. 2015). This range dis-crepancy, in combination with the urgentneed to supply fuel to power foraging, prob-ably pushed the evolution of collective for-aging (Dechmann et al. 2009; Cvikel et al.2015a). For instance, in species that forageon ephemeral and clumped prey, it is ad-vantageous for bats to search together whileremaining within an eavesdropping rangefrom other conspecifics. Such a collectivesearch, in which the group of bats is essen-tially operating as an array of sonar-sensors,can increase theefficiency offindingpatchesof prey (Figure 5; Dechmann et al. 2009; Cvi-kel et al. 2015a). Interestingly, attentive socialcommunication (e.g., social vocalizations)may often not be necessary for this collectivemovement,which inmanyspecies isprobablyfully facilitatedvia theecholocation signals ofthe bats (but not in all, e.g., Wilkinson andBoughman 1998). Movement in such situa-tions is expected to be a combination of in-dividual searching patterns along with socialattraction to conspecifics.

Echolocation could also enable foragingin small groups that have been reported inseveral bat species that hunt for aerial prey(Dechmann et al. 2009), whereas in speciesthat glean their food from the vegetation, in-dividuals may typically hunt on their own(Melber et al. 2013). Yet, bats that trawl in-sects from water surfaces may contrast withtypical gleaners. Giuggioli et al. modeledperceived echo levels of two interacting indi-viduals and found that a very simple interac-tion rule suffices to create the entire rangeof observed interactions, including chases,


tandemflights,andcollisionavoidance(Giug-gioli et al. 2015). The simple rule is that oncea bat hears the echo bouncing off the otherindividual, it will start to align its flight di-rection with that of the other individual witha response delay of up to 500 ms and withinits lateral acceleration constraints (Giuggioliet al. 2015).

Bats have been shown to be able to rec-ognize the echolocation signals of specificindividuals (Kazial et al. 2008; Yovel et al.2009). Several bats could thus maintain a co-herent group of conspecifics based on rec-ognition of the echolocation signals of itsmembers. Some bats probably also use so-cial vocalizations to actively guide collectivemovement. In Phyllostomus hastatus, for ex-ample, “screech” vocalizations serve the pur-pose of maintaining a group of familiarindividuals while foraging (Wilkinson andBoughman 1998). In several other bat spe-cies, social calls have been shown to attractconspecifics to communal roosts (Chaverriet al. 2010; Schöner et al. 2010).

But there are also constraints on collec-tivemovement in bats. On the ultimate level,

Figure 5. Schematic Picture About the Role of

EcholocationCalls as InadvertentCues

for Promoting Hunting Efficiency Via

Group Foraging

Bats may gain information about the location ofephemeral patchily distributed prey (e.g., swarms byeavesdropping on echolocation calls of conspecifics).The range fromwhich a conspecific canbeheard ismuchlarger than the range from which prey can be detectedand bats can thus benefit from searching individuallywhile remaining in a range that allows eavesdroppingon nearby individuals. Reprinted with permission fromCvikel et al. (2015a).



competition probably plays a role in shapingthe foraging movement of bats. Food de-pletion has been suggested to be an impor-tant factor, but supporting data are lacking.Moreover, conflicts of interest among groupmemberscan strongly influence theoutcomeof collectivemovements in bats. During roostswitching in Bechstein’s bats (Myotis bechstei-nii), the level of conflict among colonymem-bers about the suitability of a given potentialroost strongly influenced whether a consen-sus about communal roosting is reached. Ifthe experimentally induced conflict of in-terests became too strong, the colony tempo-rarily formed subgroups that reflected theindividual interests of the bats roosting to-gether (Kerth et al. 2006; Fleischmann et al.2013). Incontrast,brownlong-earedbats(Ple-cotus auritus) that experienced the same highlevel of conflict of interest always achieveda colony-wide consensus about communalroosts(FleischmannandKerth2014).Indeed,bats may even coordinate their movementsbetween roosts with that of other co-occurringspecies (Zeus et al. 2017).

On the proximate level, sensory interfer-ence generated by the echolocation signalsof nearby bats (i.e., jamming) has been hy-pothesized to reduce the profitability of hunt-ing in a group (Ulanovsky et al. 2004; Gillamet al. 2007), but evidence is still under debate.Recent audio recordings on-board of wildbats imply an attention tradeoff that mightimpair bats when foraging in a tight group(Cvikel et al. 2015b). According to this hy-pothesis, batsmust allocate sensory attentionto nearby flying conspecifics at the cost ofsearching for prey. This tradeoff thus sug-gests an intermediate bat density that is mostbeneficial for foraging, ononehand, increas-ing prey-detection efficiency via collectivesearching but, on the other hand, not im-pairing foraging due to interference. Lastly,atmospheric attenuation of echolocation callsmight hamper the ability of bats to know thewhereabouts of group members, e.g., malebats aiming to control the movements of fe-males at night as part of a mate-guardingstrategy (Hoffmann et al. 2007). Clearly,understanding collective behavior in bats re-mains a key question on the way to under-standing their movement.


bat movements and diseases

Bats are associated with a number of highprofile zoonoticpathogens, including rabies,severeacuterespiratorysyndrome(SARS)co-ronavirus, and Ebola, Nipah, Hendra, andMarburg viruses (Calisher et al. 2006; Hay-man et al. 2013). Recent work suggests thatbats may host more zoonotic viruses thanother mammalian groups (Luis et al. 2013).Moreover, their competence as viral reser-voirhostsmaybeaconsequenceofevolution-ary adaptations that allow sustained flight(O’Shea et al. 2014; Brook and Dobson2015). Bats expend around twice as muchmetabolic energy as do nonflying eutherianmammals over their lifetimes (Austad andFischer 1991) and, in flight, the metabolicrate of bats may increase fifteenfold com-pared to basal metabolic rates (Voigt et al.2012a). Recent genomic studies suggestedthat bats evolved mechanisms that limit thecellular andDNAdamageassociatedwithox-idative stress caused by flight (see referencesin Brook and Dobson 2015), which may im-prove bats’ defenses against intracellular in-fections, such as viruses (Zhang et al. 2013;Brook and Dobson 2015). O’Shea and col-leagues proposed an alternative hypothesis,that the high body temperatures and meta-bolic rates imposed by dailyflight could haveselected for lower virulence in coevolvedpathogens (O’Shea et al. 2014). In contrastto their apparent tolerance to viruses, batshave been severely affected by the emerginginfectious fungal pathogen (Pseudogymnoas-cus destructans) causing white-nose syndrome(WNS; Blehert et al. 2009; Lorch et al. 2011).WNS has killed millions of hibernating batssince it was introduced to North Americaover the past decade andhas been spreadingwest through the movement of bats (Fricket al. 2015).

As humans influence the structure andconnectivity of bat populations, we can ex-pect to see changes in the excretion andspillover of bat-borne zoonotic pathogens.Habitat loss directly affects bat movementand pathogen spillover. For example, as hu-mans have destroyed bat feeding habitats insubtropical Australia, pteropodid bats havesought alternative food sources in urban ar-



eas, leading to spillover ofHendra virus frombats to horses, and subsequently humans(Plowright et al. 2015; Figure 6). A numberof hypotheses link these urban bats to spill-over: one hypothesis is that decreasedmove-ment of urban bats, and therefore decreasedconnectivity, leads to decreased populationimmunity and larger outbreaks of virus shed-ding; another hypothesis is that urban batsexperience food shortages that lead to in-creased virus shedding (Plowright et al.2011, 2016). Similarly, Nipah virus spilloverhas been linked to urban pteropodid batsdrinking date palm sap from collection potsin Bangladesh, although the mechanismslinkingbats and virus shedding areunknown(Luby et al. 2006). Therefore, we concludethat linkingbatmovement ecology todiseaseecology is critical to understand the role ofbats as reservoir hosts, spillover risk, and theimpact of disease on populations (De Castroand Bolker 2004; Wibbelt et al. 2010; Plow-right et al. 2015).

Future Directions: Linking Principles

to Patterns Based on Fine-Scale

Movement Paths

In this review, we contextualize bat move-ments in the general conceptual frameworkof movement ecology (Nathan et al. 2008).We have specified some of the unique fea-tures that bats have evolved in relation totheir movement ecology. We have also high-lighted some benefits and disadvantages ofspecific motion and navigation capacitiesfor bats. Further, we have outlined some ofthe consequences that underlying mecha-nisms impose on bat-resource interaction,on their sociality, and on disease dynamics.Movement ecology has progressed over thepast decade because of concurrent advancesin technologies allowing new types of em-pirical studies alongside synthesis across dis-ciplines that together provide emergentinsights that define the movement ecologyparadigm. Technical advances do not onlyinclude molecular methods such as geno-type sequencing or stable isotopes but,most significantly, the technology for track-ing movements on fine temporal and spatialscales (Bridge et al. 2011). The biggest chal-


lenge for tracking animals using remote te-lemetry has always been the limits on thesize of devices that could be attached. Thereis a tradeoff between accuracy of positioningand battery life/weight, i.e., the more accu-rate the device (GPS precision) and the lon-ger it can record, the heavier it is (Bridgeet al. 2011; Kays et al. 2015). Recently, 1–3 gtracking units became available that allowusers to monitor the movement of a batweighing less than 30 g, which means thatmanyof themigratingmedium-sizedbat spe-cies (e.g., Lasiurus cinereus, Nyctalus noctula)could inprinciple be tracked througha com-pletemigration if the tagged animal is recap-tured and the unit retrieved (Weller et al.2016).Manyresearchareas, suchas theafore-mentioned studies on bat-plant interactions,bat sociality, anddisease transmission, amongothers, look forward to the adoption of theserapidly evolving techniques. We envision thefollowing exciting questions that may be an-sweredby linking theproximate andultimatecauses of bat movement:

Linking morphology to motion capacity and fitness.What is the scope of intraspecific variation inwing morphology, and its consequences formotion capacity and fitness? We observelarge intraspecific variation of wing mor-phology in bat species (Norberg and Rayner1987), yet it is not known whether this mor-phological variation has consequences forindividuals with respect to foraging, socialbehavior, and individual fitness. Miniatur-ized GPS tags will help in the future to shedlight on how individual motion capacity re-lated to morphology may facilitate or impaircertain feeding behaviors, foraging success,and migration capacity, leading ultimately tointraspecific variation in reproductive fitness.

Linking strategic fuel choice to motion capacityand landscape-scale movements. Which fueltypes are optimal for responding to dailyand seasonal fluctuations in resource abun-dance, particularly in context to phenotypicplasticity of digestive organs? Powered flightis energetically costly. Moreover, because batsappear to be constrained by the mammalianblueprint (i.e., no exclusive use of endoge-nous fuel sources for sustained flight), theymay be constrained in the length and dura-tion of daily movements. Fuel use may also



Figure 6. Conditions Required For Bat Virus Spillover, Illustrated For Hendra Virus in Australia

First, the pathogen reservoir must be present; second, bats must be infected and, in most cases, shedding path-ogen; third, the viruses must survive outside of its reservoir host (if transmitted indirectly), with access to therecipient host; fourth, recipient hosts must be exposed to the source of the virus in sufficient quantity for aninfection to establish; and, finally, recipient hosts must be susceptible to the virus. The area depicted in the layersis southeastern Queensland, Australia. The dark areas over layer 1 correspond to 20 km foraging zones aroundknown bat roost sites. Locations of the four horses on the bottom layer correspond to those of Hendra virusspillover events in 2011. From Plowright et al. (2015). See the online edition for a color version of this figure.

This content downloaded from 137.222.190.033 on February 16, 2018 07:18:24 AMAll use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).


influence population connectivity in natu-rally or anthropogenically fragmented land-scapes if certain landscape features, such ascities or lakes, present barriers, i.e., when dis-tances exceed capacity to sustain flights with-out refueling over inhospitable terrain.

Understanding the context-dependent use of sen-sory cues for the navigation capacity of bats. Howare different sensory cues used hierarchi-cally in bat orientation and navigation? Therole of magnetic sensing for movement infamiliar and unfamiliar terrain is of particu-lar interest. Current evidence suggests theexistence of an iron-based magnetic sense,yet the location and structure of this sen-sory system remains unknown. Also, it isunknown how the hierarchy of sensory mo-dalities change when bats switch from famil-iar to unfamiliar terrain, or when availablecues change during diel or seasonal cycles. Amultidisciplinary approachhas beenadoptedto solve similar questions in bird naviga-tion, involvingmolecular biology, chemistry,quantum physics, and neurobiology (Hol-land 2014). A similar approachwill undoubt-edly prove fruitful in bat navigation.

Understanding the influence of navigation ca-pacity on bat sociality. What is the influenceof inadvertent public cues on bat sociality?The audible nature of bat echolocation calls(audible at least to other bats) seems to haveconsequences for bat sociality, yet atmos-pheric attenuation may limit the use of echo-location calls for eavesdropping conspecifics.Our current understanding of how physicalfeatures of bat vocalizations are propagatingor limiting certain social systems is incom-plete. Further, howmuchdo intraspecific var-iations of navigation capacity affect bat sociality?Recent studies have shed light on intraspe-cific variation in echolocation calls andothervocalizations of bats, but our knowledge howsuch variation might foster certain social tac-tics remains largely unknown. Our currentunderstanding is hampered by a lack of dataon hownavigation capacity varies across indi-viduals and whether intraspecific (e.g., sex-specific) variation may influence movementstrategies and social behaviors.

Understanding the consequences of the navigationcapacity of bats for the interaction with food itemson the landscape level. What is the influenceof bat movements on antagonistic interac-tions with their prey andmutualistic interac-


tions with plants? Recent studies highlightthe strong interaction between insect-feedingbats and their insect prey, which can be seenas a textbook example of an arms race be-tween a consumer and its prey. Current stud-ies focus on details of this interaction in a1:1 situation, yet consequences for insectsand plants (or bats) on the population orlandscape level are yet to be discovered. Thereis also strong evidence pointing out that fruitand flower availability might even influencethe occurrence of migration, nomadism, ter-ritorialism, and central place foraging in var-ious bat species. Those variations in movementstrategy in response to food availabilitymightbe better understood in the light of novelanalytical frameworks (e.g., Abrahms et al.2017).

Linking motion capacity to pathogen transmis-sion risk. How does bat movement affect thespread of pathogens and risk of spillover?Studies of bat movements and disease havebeen limited by the weight of tags (Haymanet al. 2013). Therefore, little is known abouthow bat pathogens spread and persist in batpopulations in time and space. Improvedtag technologies may soon permit better es-timation of both local (within colony) move-ments andbroad-scalemigratorymovementsin ways that will further our understandingof transmission and disease dynamics in bathosts. Coupling empirical estimates of batmovements withmodeling of disease dynam-ics will be crucial for predicting risk of spill-over from bat populations serving as viralreservoirs as well as assessing impacts fromemerging diseases such as white-nose syn-drome.

Future studies on bat movements holdpromise to confirm and challenge currenthypotheses about the biology and ecology ofthisdiversegroupofmammals.Weanticipatethat novel technologies, such as on-boardsensors,will challengemanyconclusions thatwere once considered to be established text-book wisdom, thus broadening not only ourunderstanding of bat movement ecology butproviding novel insights into general biolog-ical and ecological processes. Conversely,conceptual advances in movement ecologyshould inform how we study bat movementsto provide new integrative insights into eco-logical processes and patterns, including bio-



diversity ( Jeltschetal. 2013).Thus,we foreseea productive future in the study of bat move-ments, particularly for studies that combineboth underlying principles and derived pat-terns.

acknowledgments

Christian C. Voigt wishes to thank theGermanNationalScience Foundation (DFG) for financial support of theInternational Berlin Bat Meeting: Movement Ecology


of Bats (DFG-VO890/27). This study was also partlyfunded by the BioMove Training Group (DFG-GRK2118/1) and a priority program (DFG-SPP 1596) toVoigt. Marco A. R. Mello was funded by the Minas Ge-rais Research Foundation (FAPEMIG: APQ-01043-13and PPM-00324 -15) and the Alexander von HumboldtFoundation (AvH: 3.4 -8151/15037). Raina K. Plow-right is supported by the U.S. National Institute of Gen-eral Medical Sciences IDeA Program (P20GM103474 andP30GM110732), Montana University System ResearchInitiative (51040-MUSRI2015-03), DARPA (D16AP00113),and SERDP (RC-2633).

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Associate Editor: Liliana M. Dávalos-ÁlvarezHandling Editor: Daniel E. Dykhuizen


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