Mikula_et_al-2016-Bats as Prey of Diurnal Birds-MammRv (1)

8/18/2019 Mikula_et_al-2016-Bats as Prey of Diurnal Birds-MammRv (1)

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INTRODUCTION

Predation is an important selective pressure that can affectindividuals, populations, and communities of prey species(Begon et al. 2005). Although predator–prey interactionsare well known for a wide variety of animals, for certain

taxa the diversity of their predators and the effects that pre-dation impose on their populations are poorly understood.This is especially the case for bats (Chiroptera; Lima & Dill1990, Caro 2005). This taxon is the second largest mamma-lian order, comprising more than 1200 species (Gunnell &Simmons 2012), and is among the most taxonomically andecologically diverse groups of mammals (Kunz & Fenton2003).

In general, bats are K-strategists with long life spans andsmall litter sizes (Kunz & Fenton 2003), and life-history traits directly related to effective avoidance of predation(Speakman 1991a, 1995, Rydell et al. 1996). Because of theirlife history and agile flight, bats have traditionally beenregarded as having relatively few natural predators andrarely experiencing predation; some authors have evendescribed bats as UFOs: ‘uncatchable flying objects’(Jędrzejewska & Jędrzejewski 1998). This perspective isprobably associated with the scattered nature of bat preda-tion records; reports are typically published in local journalsthat may be difficult to access or in monographs and speciesaccounts from specific geographic regions (Sparks et al.2000). Moreover, many relevant reports are limited to non-English sources (reducing accessibility for readers from dif-ferent language backgrounds), and even those accounts may sometimes contain comprehensive reviews of predation of

bats at only national levels (e.g. Bekker & Mostert 1991,Haensel & Sömmer 2002, Duquet & Nadal 2012). Further-more, because of their nocturnality, bats are relatively diffi-cult to observe and study, exacerbating the low chances of observing behavioural events. An accumulation of reportson predation of bats is, however, gradually changing tradi-tional knowledge on the topic, suggesting that bats may have a wide suite of natural predators including arthropods,fishes, amphibians, reptiles, and mammals (Sparks et al.2000, Molinari et al. 2005, Esbérard & Vrcibradic 2007,Nyffeler & Knörnschild 2013, de Noronha et al. 2015).Available literature indicates that the most common and

effective predators of bats are, however, birds, especially owls (Strigiformes; Speakman 1991a, Obuch 1998, del Hoyoet al. 1999, Lesiński et al. 2009a, b), which prey upon themduring their coincidental nocturnal activities. Perhaps unex-pectedly, due to the apparently differing activity schedules,another important group of potential predators of bats arediurnal avian raptors – falcons, hawks, and eagles – thathunt predominantly during the day.

Previous researchers have found that predation by birdscould be responsible for about 10% of annual mortality of

bats in the temperate zone (Speakman 1991a). Over 90%of bats taken by predators are apparently killed by owls,whereas only 5% fall prey to diurnal raptors (Speakman1991a). In the temperate zone, however, daytime flying by bats is typically very unusual. Speakman (1990), forexample, mentioned observations of only 420 cases of

diurnal activity by bats (collected during a British nationalsurvey in 1986–1987) and suggested that daytime flying isat least 100 times less frequent than flying during thenight. However, supported by releasing experiments, thediurnal predation rate on bats was estimated to be 100–1000 times higher than the nocturnal predation rate whenstandardised for the duration of bat activity at night andduring the day (Speakman 1991b, Speakman et al. 1994,Speakman 1995). Despite their limited diurnal activity (Speakman 1990), numerous reports of predation of batsby numerous raptors have been found worldwide(del Hoyo et al. 1994, Sparks et al. 2000, Ferguson-Lees &Christie 2001, Haensel & Sömmer 2002). This seemingly widespread phenomenon has, however, received very little attention even though it may influence many aspects of bat behaviour. Indeed, the interaction betweenbats and diurnal predatory birds could act as animportant adaptive pressure potentially influencing theevolution of bat primary activity into nocturnality (Rydell & Speakman 1995, Speakman 1995, Lima &O’Keefe 2013).

The aim of the present study is to review and synthesiseglobal data on predation of bats by diurnal birds of prey (Accipitriformes and Falconiformes) and other diurnal birdtaxa. Although predation of bats by diurnal avian predators

appears to be underestimated and insufficiently studied, wehypothesized that it is likely to be more frequent and morewidely distributed than previously thought.

METHODS

Data searching and exclusions

An extensive study of bibliographic sources was conductedin order to detect all relevant information on predation of bats by diurnal birds. We defined predation as ‘consumption

of one organism (the prey) by another organism (the preda-tor), in which the prey is alive when the predator firstattacks it’ (Begon et al. 2005). Therefore, we used only records that could be considered, on the basis of dietary andmorphological characteristics of birds, as attacks for thepurpose of capture and subsequent prey consumption,although in many cases, the prey was not successfully caught or when caught it was not consumed by the preda-tor. Furthermore, we focused mainly on predation eventsthat took place during the day: as daytime predation we

Predation of bats by diurnal birds P. Mikula et al.

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considered all cases where diurnal bird predators were ableto orientate themselves and hunt bats visually (including atdawn and dusk); we also included night attacks on bats illu-minated by artificial light.

In our search for scientific papers, we utilised mainly theThomson Reuters (Web of Science and Zoological Record)

and Scopus databases, Google Scholar, and Google Books.When a suitable paper was found, its references (backwardsearch) and citation records (forward search) were used tosearch for other relevant articles. Additionally, we searchedfor bat predation records in previously undescribed sourcesby conducting Internet searches for trip reports, images, andvideos carried by Google, Google Images, Flickr, andYouTube. We searched not only in the English language andLatin script but also in numerous other national languages(for language index see Appendix S1) and scripts, althoughthe search was restricted by our knowledge of particularlanguages.

For analyses we included only reports where birds hadbeen observed unequivocally attacking or catching bats orwhere such an event could be inferred from the text. We didnot distinguish between successful and unsuccessfulhunting attempts when the observation satisfied this crite-rion. To avoid pseudoreplication, we excluded records fromsecondary sources (mainly books and reviews) if we wereable to obtain the original source; if we were not, recordsfrom secondary sources were treated similarly to theprimary records. Where multiple sources mentioned thesame predation event, we used only the oldest source in thedata set for analysis. Our data set did not include caseswhere birds were observed sitting or flying near roosting

places of bats if no direct observations of bat hunting hadbeen recorded.

Some recorded attacks on bats by diurnal birds did notsatisfy our criteria of being predation attempts. Non-predatory attacks usually belonged to the class of defensivebird behaviour known as mobbing. Thus, we excluded casesof birds chasing bats, or where bat deaths were caused by birds unlikely to consume the bats as food, such as peafowlPavo sp., swifts (Apodidae), swallow Hirundo rustica, black-birds Agelaius spp., and some tits (Paridae; Tugendhat 1966,Kervyn 1998, Sparks et al. 2000, Suzuki 2012). We alsoexcluded cases where birds attacked bats or killed them

during competition for nesting holes, as observed in wood-peckers (Picidae), starling Sturnus vulgaris, and parakeetPsittacula krameri (Mason et al. 1972, Bekker & Mostert1991, Kervyn 1998, Menchetti et al. 2014). In addition, weexcluded cases where small diurnal raptors were observedchasing large bat species, when successful predation washighly unlikely (e.g. falcons Falco amurensis and Falcosubbuteo were observed chasing Eidolon helvum bats inKasanka forest, Zambia; Anonymous 2010, Willems pers.comm.).

Maps and relevant geographical information

In the preparation of maps and in our geographical assess-ment, we excluded records with highly generalised and geo-graphically unspecified information on predation of bats.We included only records with specified geographical posi-

tions at the spatial level of country or smaller geographicalareas (e.g. Guatemala or Malay Peninsula). In each case wespecified the exact geographical position with restrictionsdetailing how this was known. When the country or geo-graphical location was not specified in greater detail, geo-graphical coordinates were marked in the centre of the areathat resulted from superimposing the position given and thebird and/or bat species’ distribution (if available) at the site.

Because of the various methods used by the people col-lecting the data (such as direct observations, pellet analyses,collection of prey remnants under nests, prey delivery observations to nest, excavations on nesting sites, tripreports, photo and video records, and personal communica-tions) and the differing status of the records (from anec-dotal notes to systematic long-term research), the numberof attacks by birds on bats was counted as the number of sources (papers, trip reports etc.) in which hunting attemptswere described, even when predation events were tempo-rally separated and included more than one individual bator bats of several taxa. However, if one source containedrecords for more diurnal avian species or from multiplelocalities (natural habitats: distance of at least a few kilometres; urban areas: on the level of different cities), wenoted each locality as a separate case.

All country and bat records for each avian species are

included in Appendices S2 and S3; for references see Appen-dix S4. Data on global diversity, body lengths and weights of the raptors and other diurnal birds were obtained from theornithological literature (del Hoyo et al. 2015).

Geographical Information System analyses

All information collected was transformed into maps usingArcGIS 10.1 (ESRI, Redlands, California, USA), an inte-grated collection of Geographical Information System soft-ware products (Anonymous 2012). In this way, all recordedsites were georeferenced.

In order to investigate the pattern of records, weemployed the kernel density function, a non-parametrictechnique used to estimate the probability density functionof a random variable. Kernel density estimation is a funda-mental data-smoothing technique, where inferences aboutthe population of data are made, based on a finite datasample. This estimates the density function directly fromthe data without making any assumptions about the under-lying distribution and constitutes a general density estima-tion tool, applied directly in ArcGIS. In this study, kernel

P. Mikula et al. Predation of bats by diurnal birds

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density estimation was applied to map the distribution of records, on the basis of the type of source (scientific litera-ture or Internet search).

Visualisation of bat predators in the raptorphylogenetic tree

To visualise bat predation activity in diurnal raptors, aphylogenetic tree of extant raptor genera was constructedbased on consensus avian phylogenetic tool available athttp://birdtree.org/ (Jetz et al. 2012). As an outgroup weused gulls (Laridae). As the source of our consensus treewe used the ‘Hackett All Species tree’ with 1000 randomly generated trees. The most credible tree was then deter-mined using the tool TreeAnnotator v1.8.2 in the softwareBEAST v1.8.2 (Drummond & Rambaut 2007). Theconsensus tree was then graphically adjusted in FigTreev1.4.2 (Andrew Rambaut, University of Edinburgh, UK;http://tree.bio.ed.ac.uk/software/figtree/). We excluded thesister group of Accipitriformes, new world vultures(Cathartiformes), because of an absence of bat huntingbehaviour in whole lineage. In addition, other diurnalnon-raptorial bird groups were not visualised due to frag-mentary records.

RESULTS

Geographic distribution of attacks on batsby diurnal birds

Altogether we obtained 1530 cases of predation of

bats by diurnal raptors and other diurnal birds (711Accipitriformes, 608 Falconiformes, and 211 non-raptorbirds). Attacks on bats by diurnal birds were reported from109 countries from all continents with the exception of Ant-arctica. Records of raptors attacking bats were obtainedfrom 107 countries (26 countries in Africa, 27 in Asia, fivein Australia and Oceania, 26 in Europe, 13 in North andCentral America, 10 in South America; Fig. 1a, b). Recordsof non-raptors attacking bats were obtained from 45 coun-tries (eight countries in Africa, 16 in Asia, one in Australiaand Oceania, 14 in Europe, four in North and CentralAmerica, two in South America; Fig. 1c). The kernel density

function revealed that the density of scientific literaturerecords was highest in developed countries (Fig. 2a),whereas Internet-derived records reached high densities alsooutside these countries (Fig. 2b).

The northernmost observations of predation on bats by Falconiformes, Accipitriformes, and other birds were fromTroms county (northern Norway) at 69°00’N, 19°00’E,Luleå (northern Sweden) at 65°30’N, 21°40’E and Tafjorden(western Norway) at 62°14’N, 07°25’E, respectively. In thefirst case, Falco columbarius attacked Eptesicus nilssonii

(Frafjord 2012); in the second case, Accipiter nisus attackedthe same species (Rydell 1992). Larus argentatus, Laruscanus, and Corvus cornix were observed sitting near mater-nity roosts of Pipistrellus pygmaeus or trying to catch themnear Tafjorden (Michaelsen et al. 2014, Michaelsen pers.comm.).

The most poleward records for Falconiformes from theSouthern Hemisphere were from Puerto Madryn (Patago-nia, Argentina) at 42°46’S, 65°2’W and Mount Cookson(South Island, New Zealand) at 42°33’S, 173°8’E. In the firstlocation, Falco sparverius was preying probably uponTadarida brasiliensis (Pagnoni 2013). In the second case,archaeological excavations revealed skeletal remains of Mystacina robusta and Mystacina tuberculata at predator-accumulated deposits attributed to Falco novaeseelandiae(Worthy & Holdaway 1995). For Accipitriformes, two indi-viduals of Eptesicus vulturnus were found in the non-breeding diet of Accipiter novaehollandiae in Tasmania(Australia) approximately at 41°40’S, 147°37’E (Olsen et al.1990). Of non-raptors, Ojeda and Chazarreta (2006)observed Campephilus magellanicus delivering a bat to itsnestlings in the Nahuel Huapi National Park (Patagonia,Argentina) at 41°08’S, 71°12’W. In the Australian subtrop-ics, Strepera graculina and Dacelo novaeguineae wereobserved attacking released Chalinolobus morio, Eptesicusregulus, Nyctophilus gouldi, and Vespadelus darlingtoni in theCentral Highlands of Victoria (Australia) at 37°30′S,143°45′E (Speakman et al. 1994).

Distribution of attacks on bats within

groups of diurnal birdsWe found evidence of predation on bats in 143 species of diurnal raptors from 47 genera and three families(Accipitridae 106 spp., Falconidae 36 spp., Pandionidae 1sp.; for details, see Appendix S2). Bat-hunting by raptorswas found in about 42% of all species and in 61% of generain the family Accipitridae, and in more than 56% and 36%,respectively, in the family Falconidae. This suggests that pre-dation of bats is a widespread phenomenon present in themajority of extant raptor groups (Fig. 3).

We found evidence of bat hunting in 94 species of non-raptorial diurnal birds from 28 families (Alcedinidae 9

spp., Anatidae 1 sp., Ardeidae 5 spp., Bucerotidae 11 spp.,Cariamidae 1 sp., Ciconiidae 1 sp., Coraciidae 1sp., Corvidae 19 spp., Cotingidae 1 sp., Cracticidae 4 spp.,Cuculidae 3 spp., Dendrocolaptidae 1 sp., Dicruridae 2spp., Icteridae 2 spp., Laniidae 9 spp., Laridae 8 spp.,Malaconotidae 3 spp., Meropidae 1 sp., Momotidae 1 sp.,Muscicapidae 1 sp., Paridae 1 sp., Phoeniculidae 1sp., Picidae 2 spp., Ramphastidae 2 spp., Sturnidae 1 sp.,Turdidae 1 sp., Tyrannidae 1 sp., Vireonidae 1 sp.; Appendix S3). The three families with the highest incidence of bat




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hunting were Cracticidae (33% of all species), Laniidae(29%), and Bucerotidae (18%).

Bat species caught by diurnal bird predators

At least 124 species of bats from 48 genera and 11families (Emballonuridae 4 spp., Hipposideridae 5 spp.,Megadermatidae 1 sp., Molossidae 18 spp., Mormoopidae 3spp., Mystacinidae 2 spp., Nycteridae 2 spp., Phyllostomidae8 spp., Pteropodidae 22 spp., Rhinolophidae 6 spp.,Vespertilionidae 53 spp.) were identified as victims of pre-

dation attempts by diurnal raptors. We also recorded onecapture of Noctilio sp., extending the bat family diversity forNoctilionidae. A few other bat taxa were found to be preyedupon by raptors (Appendix S2). Altogether, the recordedbats represent more than 10% and 63% of global diversity of bat species and families, respectively.

In more than 42% of the 1319 cases of bats preyed uponby raptors, the bats were not identified even to the family level (typically, authors were unable to identify the bats,while in a few cases, we were unable to obtain the full text of the original source). The highest numbers of reported pre-

(a)

(b)

(c)

Fig. 1. Global distribution of attempted and

actual predation on bats by Accipitriformes (a),

Falconiformes (b), and other groups of diurnal

birds (non-raptors; c). Each documented case

of predation on bats is represented by a grey

dot; each black dot represents a case for each

predator group identified in (a), (b), and (c).




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dation (in descending number of cases) concerned batsfrom the family Molossidae, followed by Vespertilionidae,Pteropodidae, Phyllostomidae, Emballonuridae, Hippo-sideridae, and Rhinolophidae; all other families constitutedless than 1% of records (Table 1).

At least 50 species of bats from 24 genera and six families(Emballonuridae 1 sp., Hipposideridae 1 sp., Molossidae4 spp., Phyllostomidae 3 spp., Pteropodidae 6 spp.,Vespertilionidae 35 spp.) were recorded as victims of

predation or predation attempts by non-raptorial diurnalbirds (Appendix S3). Identified bat taxa made up about 4%and 32%of global diversity of batspecies andfamilies,respec-tively. Of the 211 records of bats being preyed upon by non-raptors, about 42% represented unidentified bats. Afterunidentified bat records were removed, the bats of the family Vespertilionidae were most frequently associated with preda-tion, followed by Molossidae, Pteropodidae, Phyllostomidae,Emballonuridae, and Hipposideridae (Table 1).

Fig. 2. Kernel density maps based on source

type. Scientific literature records (a) reach

highest densities mainly in temperate and well-

studied areas, whereas the density of Internet

records (b) shows a more diffuse pattern.

Fig. 3. Genera of birds known to hunt bats,indicated in a raptor phylogeny. Visualisation

of the consensual phylogenetic tree of raptor

genera was made by the avian phylogenetic

tool available at http://birdtree.org/ (Jetz et al.

2012). Genera in which at least one bat-

hunting species was present are highlighted in

black; others are grey. Bats as targets of

diurnal raptors’ predatory attempts were

recorded in the majority of extant lineages and

genera.




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DISCUSSION

Bats as prey of diurnal birdsIn addition to the traditionally accepted view that owls arethe major avian predators of bats, here we demonstrate thatbats have regularly been observed being caught by a widerange of diurnal birds. Our results suggest that bats are atsignificant risk of predation during daylight hours and aresupportive of the avian predation hypothesis for the evolu-tion of nocturnality in bats (Speakman 1995). It seems thatbird species capable of catching and consuming bats do soopportunistically, although hunting success, proportion,and species spectra of bats attacked differ among avian taxa.

Almost all bat-hunting bird taxa, including raptors, are

predominantly predators of prey types other than bats (delHoyo et al. 1994, Ferguson-Lees & Christie 2001). In fact, Macheiramphus alcinus is the only species of diurnal bird(and probably the only vertebrate predator) that consis-tently preys predominantly on bats (Chapin 1932, Fentonet al. 1977, Black et al. 1979). It is also the sole diurnalraptor with several unique morphological and behaviouraladaptations that enable it to feed primarily on bats duringcrepuscular periods. Macheiramphus alcinus has shifted itsdominant activity to days with reduced visibility, when itslarge eyes provide enhanced vision (Ferguson-Lees &Christie 2001). The species’ enlarged gape suggests conver-

gent evolution with swifts, swallows, and nightjars(Caprimulgiformes), and permits the ingestion of relatively large intact prey (Jones et al. 2012). Its prey is, moreover,typically captured, processed, and swallowed in flight(Eccles et al. 1969, Black et al. 1979, Ballance 1981), so thatits behaviour resembles that of aerial feeders more than thatof other raptors that usually process their prey at a perch(Ferguson-Lees & Christie 2001). In contrast, Falcorufigularis feeds on bats only occasionally (birds and insectsare its main diet; Beebe 1950, Seijas 1996) and has no

special adaptations; its gape and eye size are proportionally comparable with those of other diurnal raptors (Hall et al.2009, Jones et al. 2012).

On a local level, however, small and medium-sized batsmost often of the families Vespertilionidae and Molossidaeoccur in the diet of several falcons such as Falco rufigularis,Falco sparverius, Falco subbuteo, Falco tinnunculus, Falcobiarmicus, and Falco columbarius (Twente 1954, Black 1956,Baker 1962, Van Jaarsveld 1988, Yosef 1991, Seijas 1996,Martinez & Lee 2013, Mikula et al. 2013). Exceptions arelarger falcons (e.g. Falco peregrinus and Falco biarmicus)that are also capable of successful predation of even largerbats of the family Pteropodidae (Clunie 1972, Worthy &Anderson 2009). Falconids appear to be very successful batpredators and, locally, bats can represent a substantial part

of their diet (e.g. Baker 1962, Clunie 1972, Kirven 1976,Seijas 1996, Worthy & Anderson 2009, Foysal 2015). Largebats (mainly Pteropodidae) are also usually caught by Haliaeetus, Hieraaetus, Aquila, Nisaetus, Polemaetus,Stephanoaetus, and Pithecophaga eagles (e.g. Kennedy 1985,Stuart & Stuart 2004, Welbergen 2006, Anonymous 2010,Fam & Nijman 2011), but predation on smaller bats hasalso been recorded (Fenton et al. 1994, van Beirs 2004,Brown 2004). Smaller accipitrids prey frequently uponsmaller bats mainly of the Molossidae and Vespertilionidaefamilies (e.g. Baker 1962, Lindskog 1976, Manakadan &Natarajan 1992, Rydell 1992, Fenton et al. 1994). When

attacking bats as novel prey, raptors occasionally exhibitinitial neophobia, although they quickly overcomethis to become successful predators of bats (Mikula et al.2013).

On the other hand, records of predation of bats werecompletely absent among South American caracaras(Falconidae) and scavenging new world and old world vul-tures (except genus Gyps). Moreover, predation of bats wasnot recorded in raptor taxa with specialised dietary demands (e.g. the bee-eating genus Pernis, ichtyophagous

Table 1. Bat families taken by diurnal birds.

Percentages of predation records containing

identified bats are grouped by bat family and

summarised for three groups of diurnal avian

predators (Accipitriformes: n = 426;

Falconiformes: n = 335; other birds: n = 122)

Bat family

Taken by

Accipitriformes (%)

Taken by

Falconiformes (%)

Taken by other birds

(non-raptors; %)

Emballonuridae 1.6 1.8 0.8

Hipposideridae 1.9 0 0.8

Megadermatidae 0.2 0.6 0

Molossidae 43.2 32.2 9

Mormoopidae 0.2 1.2 0Mystacinidae 0 0.3 0

Noctilionidae 0 0.3 0

Nycteridae 0.7 0 0

Phyllostomidae 3.3 2.7 4.9

Pteropodidae 29.3 3.9 8.2

Rhinolophidae 1.4 0.6 0

Vespertilionidae 22.8 58.8 77




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Ichtyophaga, snake-eating Circaetus, except in one case, andmalacophagous Rostrhamus and Helicolestes). We assumethat the absence of information on predation of bats by members of the subfamily Harpiinae, as well as in a few other taxa, was due primarily to a scarcity of data on theirdiet.

In other birds (non-raptors), bats were frequently foundto be preyed upon by gulls (Holroyd & Beaubien 1983,Speakman 1991b), hornbills (Bucerotidae; Kemp 2001) andespecially by larger passerines (Passeriformes; Schwan &Hikes 1979, Boxall 1982, Sarkozi & Brooks 2003, Hernándezet al. 2007, Farina et al. 2011, Mikula 2013). We found thatout of 28 families and 94 bat-hunting species of non-raptors, 14 families and 47 species belong to the passerineclade. However, more than one-third of passerine familiesand nearly 80% of species are placed in the superfamily Corvoidea. Members of this superfamily, and particularly the corvids (Corvidae) that represent ∼40% of passerinepredators of bats, are large-brained opportunistically feeding generalists exhibiting very flexible behaviour andsuccessful adaptations to local conditions (reviewed by Jacobs et al. 2014). These adaptations enable them to utilisebats as a food source when the opportunity arises.

Overall, a considerable proportion of the bats that werecaptured by birds represented common species in theirrespective geographic regions. Our results suggest that batsof the families Molossidae, Vespertilionidae, and Pteropodidaeareamong those especially vulnerable to diurnalpredation by birds. We believe that certain adaptations make these batsparticularly vulnerable to predation by mainly visually ori-ented predators (such as diurnal birds): their relatively fre-

quent diurnal activity (Vespertilionidae and Pteropodidae,mainly genus Pteropus; e.g. Speakman 1990, Thomson et al.1998), roosting in super-abundant communities even up toseveral million members (Molossidae and Pteropodidae;Sprunt 1951, Lee & Kuo 2001,Anonymous 2010),and restingin open roosts (Pteropodidae; Kunz & Fenton 2003).However, high prevalence of the aforementioned bat groupsinthe dietof diurnalbirdsmaysimplyresultfromthefactthatthese three families are the most species-rich bat families.

Where are bats caught?

NATURAL HABITATS

In natural habitats, bats are regularly taken by predatory birds near roosting places, where bats typically live in denseaggregations. Many raptor species are attracted to such loca-tions to prey upon the resident bats. Around the world,there are many examples of such behaviour, especially intropical and subtropical regions. For example, atGomantong and Niah caves at Borneo, a wide variety of raptor species have been observed sitting or catching bats

near cave entrances. Moreover, substantial amounts of raptors’ remains are found directly inside or in the vicinity of caves, indicating long-term use of these areas by them(Smythies 1968, Thiollay 1983, Sheldon et al. 2001, Lim &Cranbrook 2002, Stimpson 2009). Raptor aggregations nearcaves are found worldwide; observations of bat hunting in

the vicinity of bat caves came, for instance, from the USA(Stager 1941, Constantine 1948, Sprunt 1951, Twente 1954,Black 1956, Baker 1962, Harden 1972, Looney 1972, Lee &Kuo 2001), Mexico (Anonymous 2014a, van Beirs 2014),Puerto Rico (Rodríguez-Durán & Lewis 1985), Burma(Smythies 1953), Thailand (Beckemeyer 2000, Round et al.2006, Dreyer 2010, Anonymous 2014b), Australia (Lewis1987), South Africa (Laycock 1982), Uganda (van Beirs2004), and Zambia (Black et al. 1979).

Hunting near caves or other roosting places of bats is notan unknown phenomenon among a wide variety of arthro-pod and vertebrate predators (Twente 1956, Molinari et al.2005, Esbérard & Vrcibradic 2007, Nyffeler & Knörnschild2013). Black et al. (1987) even suggested that communally roosting bats emerging in large numbers can representeasily accessible prey and act as a selective force in theevolution of specialised bat-hunting raptors such as Macheiramphus alcinus; this species is capable of huntingbats in the open air (Lendrum 1977) but prefers to huntnear roosting places (Finch 1978, Black et al. 1979). Otherraptors also hunt bats near caves or other roosting places. Inthe new world, Accipiter cooperii, Accipiter striatus, Buteo jamaicensis, Buteo swainsonii, Circus hudsonius, Falco peregrinus, and Falco sparverius were observed huntingmainly Tadarida brasiliensis bats near several caves in the

USA and Puerto Rico (Sprunt 1950, Twente 1954, Black 1956, Baker 1962, Harden 1972, Looney 1972,Rodríguez-Durán & Lewis 1985, Lee & Kuo 2001, Martinez& Lee 2013). Around the Mexican bat cave ‘El Volcán de losMurciélagos’ several raptor species, including Accipiter bicolor , Accipiter cooperii, Buteo albonotatus, Buteobrachyurus, Buteo plagiatus, Buteogallus urubitinga,Chondrohierax uncinatus, Falco rufigularis, Micrastur ruficollis, Micrastur semitorquatus, and Rupornis magnirostris(Boland 2009, Binns & Beer 2011, Anonymous 2014a, c, vanBeirs 2014), were observed feeding on communally roostingbats. Very diverse raptor assemblages can also be found near

tropical caves in Thailand and Malaysia, where mainly Tadarida plicata bats roost in huge aggregations; amongrecords mainly from Internet searches we found informa-tion on numerous bat-hunting raptor species: Accipiter badius, Accipiter gularis, Accipiter trivirgatus, Accipiter virgatus, Aviceda jerdoni, Butastur indicus, Buteo japonicus,Falco peregrinus, Falco severus, Falco tinnunculus, Haliastur indus, Ictinaetus malayensis, Lophotriorchis kienerii, Macheiramphus alcinus, Nisaetus nanus, and Spilornis cheela(Smythies 1968, Thiollay 1983, Beckemeyer 2000, Lim &




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Cranbrook 2002, Stimpson 2009, Dreyer 2010, Anonymous2014b). Additionally, numerous bat predation records camefrom the vicinity of the Murchison Falls in Uganda, wherebats emerging from the cave are pursued by Aquila rapax ,Buteo buteo, Falco ardosiaceus, Falco cuvierii, Falco peregrinus, Gypohierax angolensis, Haliaeetus vocifer ,

Hieraaetus wahlbergi, Macheiramphus alcinus, and Milvusmigrans (Brown 2004, Dobbs & Twino-beku 2004, van Beirs2004, Woolley & Casson 2008). Many of these records,mainly from tropical areas, are derived not from the scien-tific literature but from Internet searches. Supported by ouranalyses, Internet sources can provide important informa-tion on bird–bat relationships in the tropics.

Another example of the capacity of raptors to exploit rarebut aggregated food sources is provided by the Fibwe batforest in Zambia, where pteropodids (mainly Eidolonhelvum) aggregate seasonally in vast numbers (up to 10million individuals; Stuart & Stuart 2004, Anonymous 2010,Willems pers. comm.). These aggregations are accompaniedby many species of medium-sized to large raptors ( Aquilanipalensis, Aquila spilogaster , Buteo buteo, Clanga clanga,Clanga pomarina, Haliaeetus vocifer , Hieraaetus ayresii, Milvus migrans, Polemaetus bellicosus, and Stephanoaetuscoronatus) that visit this site to prey upon roosting bats. Fur-thermore, highly unusual raptors such as vultures(Gypohierax angolensis and Gyps africanus) also take advan-tage of the opportunity to prey on these bats (Stuart &Stuart 2004, Anonymous 2010, Willems pers. comm.).

As well as hunting near caves and dense bat aggregations,many raptor species were observed lurking near bat sheltersin cliffs, man-made structures, and vegetation, and attack-

ing migrating or released bats, as described for severalaccipitrids (Mumford 1980, Kemp & Rautenbach 1987, Byre1990, Rautenbach et al. 1990, Fenton et al. 1994, Pikachaet al. 2012) as well as falconids (Twente 1954, Meinesz et al.1982, Thomsett 1987, Fenton et al. 1994, Yancey et al. 1996).Aerial attackers of bats, such as Falco rufigularis, prefer tohunt bats in or over forest canopy and above lakes andrivers (Beebe 1950, Pierson & Donahue 1983, Robinson1994, Parker 1997). In fact, attacks on bats away from batroosts are not exceptional events for open-air hunting orambush raptors preying upon bats (Borowski 1968,Lindskog 1976, Van Jaarsveld 1988, Roworth & Wright

1989, Byre 1990, Yosef 1991, Michalak 1997, Rollie &Christie 2006).

URBAN AREAS

Bats now frequently use man-made buildings and structuresin urban habitats as roosting places (Lausen & Barclay 2006,Lesiński et al. 2009a). However, roosting in buildings may expose them to increased predation by opportunistic preda-tors that can reach high numbers in urban areas (reviewed

by Russo & Ancillotto 2015). Attacks on bats by falconids(Fry 1964, Garber 1977, Hanmer & Blackwood 1982, Negroet al. 1992, 2000, Hunter 2009, Martinez & Lee 2013, Mikulaet al. 2013) and accipitrids (Eccles et al. 1969, Mumford1980, Manakadan & Natarajan 1992) were often reportednear the bats’ roosting places in houses in parts of old

buildings such as church towers, or when bats were releasedfrom captivity. In some cases, raptors were even observedsystematically waiting for emerging bats in the vicinity of their roosting places and catching them directly at roostopenings (Martinez & Lee 2013, Mikula et al. 2013). Suc-cessful attacks on bats further from their roosting placesand in open air were also observed in urban areas (Metcalf 1983, Craves 1994).

Several urban avian predators of bats take advantage of artificial light sources to extend their activity into nocturnaltimes, and sometimes successfully hunt bats attracted to theinsects found near lights (Tryjanowski & Lorek 1998, Negroet al. 2000, Rejt 2004, DeCandido & Allen 2006). Thesefindings support the hypothesis that anthropogenic roost-ing places can act as ecological traps for synurbic species of bats via their exposure to increased predation pressure(reviewed by Russo & Ancillotto 2015); however, the overallimpact of predation on bat populations needs to be studiedin greater detail.

Non-raptors as predators

We found considerably less information on predation of bats by birds other than raptors. Most predation recordsrepresented hunting attempts by opportunistic omnivores,

e.g. corvids, gulls, hornbills, roadrunners Geococcyx spp., titsParus major , and carnivorous shrikes (Laniidae). In mostcases, this behaviour was spontaneous and opportunistic;attacks usually occurred in the open air and, therefore,hunting success was rather incidental. Furthermore, the lack of morphological and behavioural adaptations the preda-tors have for this prey type probably leads to low huntingsuccess. For instance, non-raptorial bird species usually usetheir beaks to catch prey (Lefevre 2005, Collin 2011) insteadof using the claws employed by raptors (Sprunt 1951,Garber 1977, Byre 1990, Rollie & Christie 2006). In theseoccasional bat-hunting species, analysis of their diet and

systematic observations may reveal important insights intotheir feeding behaviour. For instance, although informationon predation of bats by ravens Corvus corax from directobservations is very fragmentary, detailed studies of theirpellets from long-term accumulations confirm the occur-rence of eight bat species in their diet (Obuch 2007).

In general, bats comprise only very small proportions of the diet of diurnal birds, and hunting attempts are only occasionally successful. An exception to this rule can occurin local bird populations hunting near roosting places of




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bats. For instance, aerial attacks on bats by true shrikesLanius spp. are very common, but infrequently result insuccess (Bent 1950, Young 1980, Gorman 1998). However, itseems that shrikes may increase their hunting success by remaining near crevices used by bats as roosts (Herrmann2004). This hunting technique was observed in several

species of bird that were able to catch bats very successfully at roost entrances, directly in roosting places or when batswere unable to escape and their mobility was reduced(when they fell on the ground, or were hibernating orinjured). For instance, such predatory attempts wererecorded in tits (Estók et al. 2010), corvids (Hochachka &Scharf 1986, Pačenovský 2006, Mikula 2013, Michaelsenet al. 2014), gulls (Holroyd & Beaubien 1983, Collin 2011,Michaelsen et al. 2014), butcherbirds (Cracticidae; Young1980), and roadrunners (Herreid 1960, Martínez-Coronelet al. 2009). In this way, some urban populations of corvidsand gulls can be very effective bat predators (e.g. Forestman2006, Collin 2011). This suggests that bat populations may be effectively regulated by bird predators at the local leveland, moreover, points to the vulnerability of urban batpopulations to opportunistic predators. In addition, somebirds, especially corvids and gulls, are able to utilise com-munal hunting to their advantage to increase their successat hunting bats (Clay 1959, Cleeves 1969, Lefevre 2005,Hernández et al. 2007).

Support for the avian predation hypothesis

Additional support for the avian predation hypothesis forthe evolution of nocturnality in bats came from observa-

tions on bats living on raptor-free islands. Perhaps the best-known case is that of Nyctalus azoreum, a bat speciesendemic to the Azorean archipelago. This species exhibits anunusually high degree of diurnal activity that appears toreflect its release from predation risk by diurnal raptors(Moore 1975, Speakman & Webb 1993). Such an activity pattern has also been found in some other island bat popu-lations where large avian predators are absent or rare, suchas in the insectivorous bat Hipposideros ruber on São ToméIsland (Russo et al. 2011) and several pteropodids such asPteropus melanotus on Christmas Island (Hall et al. 2014)and Pteropus samoensis on American Samoa (Thomson

et al. 1998). On Fiji, however, where Falco peregrinus ispresent (Clunie 1972), the subspecies of Pteropus samoensisis also diurnal but appears to behave more cryptically (Wilson & Engbring 1992).

Bats have been observed to shift their emergence timewhen diurnal predators are present (e.g. Fenton et al. 1994,Welbergen 2006). In addition, lunar phobia exists mainly among tropical bats of all trophic guilds but is almostabsent among temperate insectivorous bats (reviewed by Lima & O’Keefe 2013). Such a pattern could be explained by

the presence in tropical ecosystems of avian bat predators,such as Macheiramphus alcinus and Falco rufigularis, and of a higher diversity of carnivorous birds such as owls, whichcan represent substantial risk of predation for bats duringmoonlit nights (del Hoyo et al. 1994, 1999, Kissling et al.2011). Presence of light avoidance behaviour was, moreover,

experimentally supported in insectivorous and frugivorousbats (Stone et al. 2009, Lewanzik & Voigt 2014). The noctur-nal activity pattern of bats could therefore be permanently maintained by the constantly present high risk of diurnalpredation by avian predators (Speakman 1995).

CONCLUSIONS

Our results show that attacks on bats by diurnal birds areglobally distributed and reach the geographical limits of thecoexistence of both animal groups. Such predatory attemptsare present in the majority of extant raptor lineages as wellas in numerous other groups of diurnal birds. Moreover,bats in the majority of extant bat families fall victim to pre-dation by diurnal birds. Our results are thus supportive of the avian predation hypothesis: predation by diurnal birdscould act as one of major factors affecting the scarcity of daytime activity in bats, and as a driver of the evolution of bat nocturnality.

ACKNOWLEDGEMENTS

We would like to thank Renate Alton, Omar Al-Sheikhly,Mark D. Anderson, Peter Bačkor, Colin Beale, Keith Betton,Rob Bijlsma, Massimo Biondi, BirdWatch Zambia, Brian

Blaylock, Maurice Boët, Mareike Bollen, Mark Brown,Herve Brule, Center for Wildlife Conservation Cambodia,Nicoletta Chiozzi, Dominique Conrad, Julie A. Craves,Stephen Debus, Christiane Denys, Joe DiCostanzo, PieterVan Dorsselaer, Pavla Doubková, Christian Dronneau,Muriel Dubray, Petra Fahle, Andy Featherstone, KarlFrafjord, Lenka Glosová, Oscar Gordo, Marco A. M.Granzinolli, Margaret A. Griffiths, Troy W. Grovenburg,Ferenc Halász, Peter Hewitt, Kuan-Chieh Hung, TomJenner, Rudy Jocqué, Ron Johnstone, Holger Kolberg, Mar-garet Koopman, Alexander Krikellis, Sergei Kruskop, Robin-son Lance, Lauraine Leigh, Grzegorz Lesiński, Wen-Horn

Lin, Rebecca Mabuza, Ian Macalpine-Leny, Bojan Marčeta,Brian Marshall, Bruno Massa, Štefan Matis, Jean Meguin,Tore C. Michaelsen, Edita Miková, Campbell Murn, RenaudNadal, Barure Nirmala, Hans Oelke, Han Olff, Jerry Olsen,Karin Persson, Gary Presland, Hans-Ulrich Raake, WolfgangRackow, Roger Riddington, Chris Risley, Travis Rosenberry,Martin Sanford, Norbert Schäffer, Anja Schuhn, Ron Searleand his family, Donald Seriff, Dione Seripierri, Clark Sherman, Christoph Siems-Wedhorn, John R. Speakman,Gero Speer, Ian M. Spence, Tadeusz Stawarczyk, Toshitaka




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N. Suzuki, Craig Symes, Wendy Tatar, Russell Thorstrom,Stephanie Tyler, Marcel Uhrin, Sam Veansa, Ben Verboom,Anne Weiserbs, Chip Weseloh, Frank Willems, and JosephWunderle, who kindly sent us copies of some articles oroffered personal observations in this topic. We are also very thankful to Ivan Horáček, who helped us with the identifi-

cation of bat taxa from Internet photos.

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SUPPORTING INFORMATION

Additional supporting information may be found in theonline version of this article at the publisher’s web-site.

Appendix S1. Index of all languages used in literaturesearching.Appendix S2. Summary table of diurnal raptors(Accipitriformes and Falconiformes) reported to capturebats with list of localities at country level and bat taxa(arranged in alphabetical order).Appendix S3. Summary table of non-raptorial diurnalbirds reported as bat hunters with list of localities atcountry level and bat taxa (arranged in alphabetical order).Appendix S4. References used in the Appendices.



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