Bat MigrationT. H. Fleming, University of Miami, Coral Gables, FL, USA

ã 2010 Elsevier Ltd. All rights reserved.

Introduction

Migration is an essential feature of the life history ofa substantial fraction of the world’s animal fauna. Amongvertebrates, migration, which can be defined as a seasonal,usually two-way, movement from one habitat to anotherto avoid unfavorable climatic conditions and/or to seekmore favorable energetic conditions, is common in fishand birds. It is less common in amphibians, reptiles, andmammals. Among volant vertebrates, it is much morecommon in birds than in bats, and birds migrate muchlonger distances, on average, than bats. Nonetheless, aconsiderable number of bats, including both temperateand tropical species, undergo significant seasonal move-ments between habitats. As I discuss in this article, thesemovements have important population and conservationconsequences. In a world of global climate change andincreased extinction risk for an estimated 25% of theworld’s mammals, migratory species are especially vul-nerable to extinction risks and are of major conservationconcern. These concerns include the effect of wind tur-bine farms on migratory bats and their roles as reservoirsfor emerging diseases that can be fatal to humans.

An Overview of Bat Migration

Temperate Bats

Until recently, migration in bats had mostly been studiedin temperate regions of North America and Europe wheremigratory behavior is closely associated with hibernation.Results of those studies indicate that temperate bats exhibitthree broad patterns of spatial behavior: (i) sedentary (non-migratory) behavior in which bats breed and hibernatewithin a 50-km radius or less; (ii) regional migration inwhich batsmigrate 100–500 kmbetween summer andwinterroosts; and (iii) long-distancemigrants inwhich bats migrate1000 km or more between seasonal roosts. Examplesof European sedentary taxa include species of Eptesicus,Plecotus, andRhinolophus and certain species ofMyotis. TheirNorth American counterparts include Eptesicus fuscus,Corynorhinus rafinesquii, and Antrozous pallidus. Europeanregional migrants include several species of Myotis, andNorth American taxa include several species ofMyotis andPipistrellus (or Perimyotis) subflavus. European long-distancemigrants include several species of Nyctalus as well as twospecies of Pipistrellus and Vespertilio murinus. Although theymigrate relatively long distances between summer and

winter roosts, they do so within, rather than between,continents, unlike many European migratory birds whichare intercontinental migrants. In North America, long-distance migrants include species of Lasiurus, Lasionycterisnoctivagans, and the subtropical/tropical seasonal migrantsLeptonycteris curasoae, L. nivalis, Choeronycteris mexicana,and Tadarida brasiliensis. With the possible exception ofLasiurus species, these taxa are also intracontinentalmigrants. Unlike other temperate migrants, these speciesdo not hibernate.

As is the case in birds, temperate zone long-distancemigrant bats tend to differ morphologically from moresedentary species and are adapted for rapid, energeticallyefficient flight. They have wings with high aspect ratios(i.e., they are long and narrow), pointed wing tips, andhigh wing loading. As a result, most insectivorous long-distance migrants forage in uncluttered air space awayfrom vegetation where slow, highly maneuverable flightis not needed. In addition, many long-distance migrants(e.g., the European species plus Lasiurus and Lasionycteris

in North America) roost in small colonies (or are solitary)in trees and buildings rather than in large numbers incaves, as is often the case in regional migrants and seden-tary species. Exceptions to this include North AmericanT. brasiliensis and L. curasoae which are highly gregariouscave dwellers year round.

Not all individuals of species of temperate migra-tory bats undergo seasonal migrations. Partial migrationoccurs in a number of species, including long-distancemigrants. In Europe, partial migrants include species ofNyctalus and Pipistrellus and V. murinus. In North America,partial migrants include Lasiurus cinereus, L. noctivagans,L. curasoae, and T. brasiliensis. In Europe, sedentary popu-lations of P. nathusii share hibernation caves with mig-ratory populations, whereas sedentary and migratorypopulations of V. murinus have geographically separateranges year round. A situation similar to that of V. murinusis seen in North American T. brasiliensis in which westernand southeastern populations in the United States aresedentary and seasonal populations in the south-centralUnited States overwinter in Mexico.

Regardless of the distances involved, most temperatezone migratory bats undergo a characteristic annual phys-iological and reproductive cycle that is closely tied tohibernation. This cycle includes hyperphagia and fatdeposition in the fall and mating in the fall or winter.Unlike birds, which sometimes increase their body massby 50% by fat deposition prior to migration, bats increase

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their mass by only 12–26% by fat deposition. Also, unlikebirds, bats must use most of the fat they deposit prior to orduring migration as a fuel source during hibernation.Conservation of stored fat for use during hibernation isan important reason why many temperate bats migraterelatively short distances. Finally, the annual reproductivecycle of temperate bats usually involves mating in the fallprior to hibernation. In some species (e.g., N. noctula,P. nathusii), mating occurs along female migratory path-ways with males defending roost sites which are visited byfemales for mating. In other species (e.g.,Myotis species inNorth America), individuals of both sexes form ‘swarms’at the entrances of hibernation or other caves, probablyfor mating. After mating, females of hibernating speciesstore viable sperm in their oviducts during the winter andovulate and undergo fertilization in the spring prior tomigrating to their summer maternity roosts. In nonhiber-nating long-distance migrants such as Lasiurus borealis,L. curasoae, and T. brasiliensis, mating and fertilizationoccur simultaneously prior to or during spring migration.

Tropical Bats

Migratory behavior is much less common in tropical batsthan in temperate bats and is never associated with hiber-nation. Whereas temperate bats migrate and hibernateto avoid habitats that are energetically and physiologi-cally unfavorable during winter, tropical, and subtropicalbats usually migrate along food resource gradients oramong seasonally ephemeral resource patches. A clearexample of this is the nectar-feeding, long-distancemigrant L. curasoae in Mexico and the southwesternUnited States. During the fall and winter, populationsin western Mexico live in tropical dry forest and visitflowers produced by trees and shrubs during an annualflowering peak. After mating, many pregnant females(but few males) migrate 1000 km or more to the SonoranDesert of northwestern Mexico and Arizona along a ‘nec-tar corridor’ of blooming columnar cacti. Once in theSonoran Desert, they form maternity colonies and feedat a super-rich source of nectar and pollen producedby several species of spring-blooming columnar cacti.Populations of this species living in central or southernMexico are more sedentary because their floral resourcesare available year round. In Africa, several species offruit-eating pteropodid bats, including Eidolon helvum,

Myonycteris torquata, and Nanonycteris veldkampi, migrateup to 1500 km away from equatorial forests to savannawoodlands to feed on seasonal bursts of fruit. In easternAustralia, the pteropodid bat Pteropus poliocephalus containssedentary coastal populations that feed on fig fruits yearround and inland populations that migrate hundredsof kilometers between ephemeral but rich patches offlowering eucalypt trees. Finally, several species of insec-tivorous rhinolophid and vespertilionid bats undergo

short-distance migrations between coastal and inlandhabitats in East Africa in response to seasonal changes infood availability.

Methods for Studying Bat Migration

Obtaining precise quantitative data on the distances thatbats migrate and their migratory pathways has been tech-nologically challenging. From the 1930s until recently,placing numbered aluminum bands on bats was the pre-dominant method used to study bat (and bird) migration.This method involves banding bats at one roost (either asummer or winter roost), and then attempting to recapturebanded bats (or recover their bands) somewhere else. Thismethod is very labor intensive and inefficient because onlya tiny fraction (¼1%) of banded bats are usually everrecovered away from their original banding sites. Forexample, over 400 000T. brasiliensiswere banded in winterroosts in Mexico and summer roosts in the southernUnited States in the 1950s and 1960s, and only a handfulwere ever recovered away from their banding sites.

In addition to banding, methods that are currentlybeing used to study bat migration include analyses involv-ing DNA and stable isotopes and tracking studies usingradio or satellite transmitters. Control region mitochon-drial DNA is potentially very informative about geneticconnections among distant roosts from which migratoryconnections can be inferred. A study of L. curasoae usingthis technique, for example, was able to identify twopathways along which females moved from south-centralMexico into the Sonoran Desert and southeasternArizona, respectively, using data from only 49 individualscaptured at a total of 13 roosts. Since this species isfederally endangered in the United States and Mexico,large-scale banding operations were not feasible and othermethods were needed to determine the scale of its migra-tory movements. Genetic analysis proved to be a veryefficient method to obtain this information and to identifyroosts in Mexico of special conservation concern (e.g., mat-ing roosts). Other species whose migratory behavior hasbeen studied using genetic techniques include Miniopterus

schreibersii, N. noctula, and T. brasiliensis.Another analytical technique that has provided impor-

tant new insights into the migratory behavior of hard-to-study bats is stable isotope analysis. Stable isotopesof carbon and hydrogen are especially useful for this.The 13C stable isotope of carbon allows one to determinewhether herbivorous animals are feeding on plants thatuse the CAM, C4, or C3 photosynthetic pathway. Thefirst two pathways are used by succulent plants (e.g., cactiand agaves) or tropical grasses (e.g., corn), respectively, andare enriched in 13C compared with the more common C3plants. By analyzing carbon stable isotopes in muscle tissuetaken from museum specimens collected throughout its

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geographic range in Mexico and the southwestern UnitedStates, Fleming and colleagues found that individuals ofL. curasoae use CAM plants (primarily columnar cacti in thespring and agaves in the fall) as food sources during migra-tion and C3 plants during the winter. Knowing that colum-nar cacti occur in the Pacific coastal lowlands of Mexicoand that agaves occur in upland portions of the SierraMadre, they were able to identify the likely ‘nectar corri-dors’ along which these bats fly during migration.

Deuterium (D), the stable isotope of hydrogen, is use-ful for determining the migration distances of solitaryroosting insectivores such as L. cinereus and L. noctivagans.Values of D vary inversely with latitude, elevation, anddistance from coasts and can indicate approximatelywhere bats were living when new tissue such as hair wasproduced. Since the aforementioned bats tend to moltbefore migrating in the fall, an analysis of hair samplesfrom bats caught during migration or in their winterlocations can be used to determine how far they migratedafter molting. This technique has been used to determinemigration distances of 1800–2600 km for both males andfemales of L. cinereus in North America. Some bats molt-ing during the summer in Canada were captured inMexico in the winter. The researchers concluded thatthis technique holds considerable promise for studyinglong-distance migration in bats.

Radiotagging and satellite tracking are two methodsfor directly studying the migratory behavior of bats. Radiotransmitters weighing <1 g are readily available and havebeen used to study the foraging and roosting behavior ofmany species of bats, including species weighing <10 g.Except for the Australian Pteropus poliocephalis, which cancarry transmitters with large batteries because of theirlarge size, they have not yet been used to study batmigration for at least two reasons: (i) the battery life ofthese transmitters is short (about 2 weeks) and limits theamount of data that can be gathered from individual bats;(ii) since they migrate at night and sometimes at substan-tial altitudes (up to 2400m), following radiotagged batsduring migration involves potentially dangerous nighttime airplane flights over unknown terrain. Less danger-ous but more costly in terms of transmitters (which cur-rently cost US$1–3K) and daily or weekly downloads,satellite transmitters offer great potential for studyingmigration in bats, as it does for birds. Solar-poweredsatellite transmitters now weigh 12 g and have been usedto study foraging and migration movements of one speciesof pteropodid bat that roosts in tree canopies (rather thanin caves) during the day. Richter and Cumming studied themovements of four individuals of the 300 g frugivore Eidolonhelvum that they tagged in central Zambia, Africa. Thesebats foraged up to 59 km from their day roost and traveled878–1975 km over a period of two or more weeks whenflying north to the Democratic Republic of Congo. Duringthe return trips, these bats averaged 90 km per night.

Satellite transmitters equipped with conventional bat-teries (total package weight¼ 33–40 g) have been placedon two young males of Pteropus poliocephalus weighing 790and 857 g in south-eastern Australia. Over the course ofabout a year, these bats made round trips of >2000 kmspanning over 4� latitude as they moved up to 400 kmamong roosts in response to changes in the local availabil-ity of eucalypt blossoms.

Population and Genetic Consequencesof Migration

Migration can have strong effects on the populationand genetic structure of bats. In temperate bats, malesand females typically hibernate in the same caves andare largely trophically inactive during winter. Duringthe trophically active season, the behavior of males andfemales of migratory species often differs with respectto distances they migrate and locations where theyspend the summer. In many species, females migratelonger distances and form larger summer (maternity)colonies than males. As a result, the sexes are often geo-graphically separated at a variety of spatial scales duringthe summer. An extreme example of this is Lasiurus ciner-eus in which males spend the summer in the mountainsof western North America and females roost in north-central and northeastern United States and Canada.Sex-biased migration and seasonal spatial segregation ofmales and females also occur in L. curasoae andT. brasiliensisin North America. In both species, females migrate northfrom south-central Mexico to form large maternity colo-nies in the Sonoran Desert and south-central United States,respectively.

Seasonal movements can also have community conse-quences whenever regional and long-distance migrantsmove into and out of habitats containing resident species.In West Africa, for example, three species of frugivorouspteropodid bats migrate from equatorial forests to morenorthern savanna woodlands where they join a residentcommunity of several species of frugivorous bats andbirds. Differences in habitat and fruit preferences reducepotential competition among these species. A similar sit-uation is seen in East Africa where several species ofmigrant insectivorous bats join a community of residentinsectivores during periods of increased insect availability.Differences in morphology and foraging behavior againallow these species to coexist. Finally, seasonal influxes ofmigrant nectarivores and insectivores increase the speciesrichness of bats in Sonoran Desert communities duringthe summer. As in the other two examples, differencesin diets and foraging behavior minimize competitionbetween residents and migrants.

As might be expected given their high mobility, thegenetic structure of migrant species also differs from that

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of nonmigrants in a predictable way: a lower degree ofgenetic subdivision and larger effective population sizesin migratory species. An extreme example of a sedentaryspecies is the Australian megadermatid Macroderma gigas

in which widely separated colonies seldom exchangegenes. As a result, Wright’s index of subdivision Fst forthis species is about 0.87 (out of 1.0 for complete subdivi-sion; a value of 0.0 represents complete panmixia). At theother extreme is the long-distance migrant N. noctula

whose Fst is 0.006 and whose region of panmixia in centralEurope has a diameter of about 3000 km. Other species inboth mobility classes have less extreme levels of Fst, butvalues for nonmigratory species are generally >0.10whereas those of migrant species are <0.10.

Conservation Consequences of Migration

Because their annual ranges often encompass substantialgeographic areas that usually cross different federal orinternational boundaries, the conservation of migratorybats, like that of migratory birds, can be challenging. Con-sequently, conservation efforts need to be geographicallyand politically broad in scope. This conservation mustinvolve protecting a variety of different roost sites, includ-ing those used for mating, migration, and maternity, as wellas the foraging habitats around critical roost sites. In addi-tion, habitats used en route during migration, includingstopover habitats where bats can refuel, need protection.Plant-visiting bats such as the nectarivore L. curasoae andthe frugivore E. helvum likely migrate along specific foodcorridors that also need protection. Based on their satellite-tracking results, for example, Richter and Cumming notedthat only a fraction of the migratory pathway along whichE. helvum flies between the Democratic Republic of theCongo and Zambia is currently protected. Loss of foresthabitat containing fruiting trees along this pathway couldseriously disrupt its annual migration. Similarly, destruc-tion of parts of the columnar cactus ‘nectar corridor’ alongthe Pacific coast of Mexico would have a strong negativeeffect on migrating pregnant females of L. curasoae. Basedon levels of fat that these bats deposit prior to and duringmigration, Fleming has estimated that the maximum flightrange of these bats is about 550 km. If the average distancebetween rich patches of cacti exceeds this value, then themigration of thousands of bats could be disrupted. Andbecause intact populations of fall-blooming agaves arealso needed by this species to complete the return leg ofits migration, habitat protection over a large portion ofwestern Mexico is needed. Migration of insectivorous batsis usually much more diffuse geographically than that ofplant visitors, but they also need intact foraging habitat, aswell as protected stopover roost sites. A landscape that isdevoid of safe caves, intact forests, and unpolluted lakes andstreams is just as threatening to the existence of migrating

insect bats as a landscape devoid of flowering and fruitingplants is to plant visitors.

In addition to the usual litany of threats to bats andother wildlife (e.g., habitat destruction, pollution, andspecifically for bats, malicious destruction of their colo-nies in caves and other roosts), a new threat to theirconservation has emerged recently – wind turbine farms.In an effort to tap alternate sources of energy, windfarms have increased markedly in number and size inEurope, Australia, and North America in recent years.While these establishments clearly have positive valuefor energy production, they can have negative value forwildlife because they kill migratory birds and bats.In North America and Europe, for example, peak batfatalities occur in late summer and fall and are heavilyconcentrated in long-distance migrants such as species ofNyctalus and P. nathusii in Europe and species of Lasius inNorth America. In the United States, wind farms locatedin forested parts of the east coast experience higher killrates than those located in the Rocky Mountains andPacific Northwest. Why lasiurine bats, which migrate inflocks despite being solitary roosters during the summer,are more vulnerable to fatal interactions with wind tur-bines is not yet known. Fatalities are most common onnights with low wind speed (<6m s�1) and before andafter the passage of storm fronts when large numbers ofbats (and birds) are likely to be migrating. Bat fatalitiesoccur only when turbines are spinning, not when they arestationary. After reviewing available data, Arnett and col-leagues concluded that the number of bat fatalities atwind farms could be reduced substantially by temporarilystopping turbines at night at certain times of the year andunder certain climatic conditions.

My final topic – one that has important conservationimplications, especially for migrant bats, as well as healthimplications for humans – is bats as reservoir hosts foremerging viruses. It has long been known that bats areimportant reservoirs for rabies virus and that they some-times (but rarely) transmit it to humans. According to areview by Calisher and colleagues, bats are known toharbor a substantial number of viruses only a few ofwhich are known to be pathogenic when transmitted tomammals, including humans. In addition to rabies, theseinclude other lyssaviruses (Family Rhabodviridae) aswell as Hendra and Nipah viruses (Family Paramyxovir-idae) and possibly SARS-Coronavirus-like viruses (FamilyCoronaviridae). Hendra virus has been found in species ofPteropus in Australia; Nipah virus has been found in speciesof Pteropus in South and Southeast Asia and SARS corona-virus occurs in species of Rhinolophus in Eurasia. BothHendra and Nipah viruses have been found in humansvia transmission from intermediate host mammals (e.g.,pigs). Ebola virus RNA has been found in three speciesof African pteropodids, including E. helvum, but not thevirus itself.

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Because they are geographically wide ranging, migrantbats have the potential to spread pathogenic viruses overwide areas. Outbreaks of rabies virus in Europe, for exam-ple, have occurred along the migration routes of P. nathusii,and different geographic variants of this virus have beenfound in two North American migrants, P. subflavus andT. brasiliensis. Migrant bats in general have a classic meta-population structure featuring discrete populations (roosts)interconnected by dispersal or migration; between-colonymovements can expose resident as well as migrant popula-tions to new variants of rabies or exchange virus variantsamong colonies. Calisher and colleagues suggested that thiskind of population structure has the potential for seasonalvirus transmission, annual outbreaks of viral diseases, andperiodic outbreaks among spatially separate populations.Geographically discrete outbreaks of rabies in the (nonmi-gratory) vampire bat Desmodus rotundus or outbreaks ofHendra virus in migratory Australian Pteropus bats mayreflect this. Finally, the long-distance migrant E. helvumhas the potential for spreading infectious diseases overlarge areas of sub-Saharan Africa.

The conservation implications of the fact that batsharbor pathogenic organisms are enormous. A major rea-son why bats in general are persecuted throughout LatinAmerica is the fear of ‘vampiros y la rabia.’ The associationbetween rabies and bats, in vampires or otherwise, is wellknown throughout the world, and bats tend to be malignedworldwide as a result. Because of this association, theecologically beneficial ‘services’ provided by bats such ascontrol of injurious insect populations (e.g., T. brasiliensisand cotton-boll worms), and the broad dispersal of pollenand seeds (e.g., by L. curasoae and E. helvum) tend to beoverlooked. In truth, the positive benefits of migratory (andnonmigratory) bats far outweigh their negative aspects.Migratory bats play an important role in many ecosystemsaround the world, and their conservation is essential.

Conclusions

Many species of bats are migratory and serve as ‘mobilelinks’ between geographically separate habitats andecosystems. They move energy and nutrients among eco-systems, help to control insects on a broad scale, and serve

as wide disseminators of pollen, seeds, and pathogens.Like their avian counterparts, migratory bats have manymorphological, physiological, and behavioral adaptationsfor ‘life on the move.’ Because of their mobile lifestyles,these bats have special conservation needs that must beaddressed politically at the national or international level.Although they sometimes harbor pathogenic organisms,their positive attributes far outweigh their negative attri-butes. Increased public awareness of the lives of thesefascinating bats worldwide is the key to their conservation.

See also: Bats: Orientation, Navigation and Homing; Bird

Migration.

Further Reading

Arnett EB, Brown WK, Erickson WP, et al. (2008) Patterns of batfatalities at wind energy facilities in North America. Journal of WildlifeManagement 72: 61–78.

Calisher CH, Childs JE, Field HE, Holmes KV, and Schountz T (2006)Bats: Important reservoir hosts of emerging viruses. ClinicalMicrobiology Reviews 19: 531–545.

Cleveland CJ, Betke M, Federico P, et al. (2006) Economic value of thepest control service provided by Brazilian free-tailed bats in south-central Texas. Frontiers in Ecology and the Environment 5: 238–243.

Cryan PM, Bogan MA, Rye RO, Landis GP, and Kester CL (2004) Stablehydrogen isotope analysis of bat hair as evidence for seasonal moltand long-distance migration. Journal of Mammalogy 85: 995–1001.

Cryan PM and Diehl RH (2009) Analyzing bat migration. In: Kunz TH (ed)Ecological and Behavioral Methods for the Study of Bats, vol. 2, pp.477–488.

Federico P, Hallam TG, McCracken GF, et al. (2008) Brazilian free-tailedbats as insect pest regulators in transgenic and conventional cottoncrops. Ecological Applications 18: 826–837.

Fleming TH (2004) Nectar corridors: migration and the annual cycleof lesser long-nosed bats. In: Nabhan GP (ed.) ConservingMigratory Pollinators and Nectar Corridors in Western NorthAmerica, pp. 23–42. Tucson, AZ: University of Arizona Press.

Fleming TH and Eby P (2003) Ecology of bat migration. In: Kunz TH andFenton MB (eds.) Bat Ecology, pp. 156–208. Chicago: University ofChicago Press.

Fleming TH, Nunez RA, and Sternberg LSL (1993) Seasonal changes inthe diets of migrant and non-migrant nectarivorous bats as revealedby carbon stable isotope analysis. Oecologia 94: 72–75.

Hutterer R, Ivanova T, Meyer-Cords C, and Rodrigues L (2005) Batmigrations in Europe: A review of banding data and literature. In:Naturschutz und Biologische Vielfalt, vol. 28, 180 pp. FederalAgency for Nature Conservation in Germany.

Richter HV and Cumming GS (2008) First application of satellitetelemetry to track African straw-coloured fruit bat migration.Journal of Zoology 275: 172–176.