Documentos de Académico
Documentos de Profesional
Documentos de Cultura
REVIEW
Keywords
avian predation hypothesis, bats, diurnal
birds, nocturnality, predation
*Correspondence author.
Submitted: 16 September 2015
Returned for revision: 1 October 2015
Revision accepted: 16 October 2015
Editor: KH
doi:10.1111/mam.12060
ABSTRACT
1. Predation is an important selective pressure that can influence prey species in
numerous ways. Predatorprey relationships are, however, poorly understood in
taxa not typically associated with these interactions; this is especially the case
when bats (Chiroptera) are the prey.
2. The main aim here is to review and synthesise global information on the predation of bats by birds of prey (Accipitriformes and Falconiformes) and other
diurnal bird groups.
3. We compiled data on incidences of predation of bats by diurnal birds, through
an extensive multilingual study of bibliographic and Internet-based sources. Scientific papers were found mainly via the Thomson Reuters (Web of Science and
Zoological Record) and Scopus databases, Google Scholar, and Google Books.
Additional data were found through Internet searches of trip reports, images and
videos carried by Google, Google Images, Flickr, and YouTube.
4. In total, more than 1500 cases of bats being attacked by diurnal predatory birds
were obtained. Reports were documented from every continent (except Antarctica) and from 109 countries, and were thus distributed globally between 70N
and 43S. Overall, we found evidence for predation of bats by 143 species of
diurnal raptors (Accipitriformes 107 spp. and Falconiformes 36 spp.) and by 94
non-raptor bird species from 28 families. At least 124 and 50 bat species were
taken as prey by raptors and by other diurnal bird species, respectively.
5. Attacks on bats by diurnal raptors were found to be distributed globally and
were present in the majority of extant raptor lineages. Attacks on bats by other
diurnal birds were also occasionally recorded. Furthermore, the majority of extant
bat families featured as prey. These results strongly suggest that predation by birds
may act as a major factor affecting the scarcity of daytime activity in bats and as a
driver in the evolution of bat nocturnality.
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
INTRODUCTION
Predation is an important selective pressure that can affect
individuals, populations, and communities of prey species
(Begon et al. 2005). Although predatorprey interactions
are well known for a wide variety of animals, for certain
taxa the diversity of their predators and the effects that predation impose on their populations are poorly understood.
This is especially the case for bats (Chiroptera; Lima & Dill
1990, Caro 2005). This taxon is the second largest mammalian order, comprising more than 1200 species (Gunnell &
Simmons 2012), and is among the most taxonomically and
ecologically diverse groups of mammals (Kunz & Fenton
2003).
In general, bats are K-strategists with long life spans and
small 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 their
life history and agile flight, bats have traditionally been
regarded as having relatively few natural predators and
rarely experiencing predation; some authors have even
described bats as UFOs: uncatchable flying objects
(Jedrzejewska & Jedrzejewski 1998). This perspective is
probably associated with the scattered nature of bat predation records; reports are typically published in local journals
that may be difficult to access or in monographs and species
accounts from specific geographic regions (Sparks et al.
2000). Moreover, many relevant reports are limited to nonEnglish sources (reducing accessibility for readers from different 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 & Smmer 2002, Duquet & Nadal 2012). Furthermore, because of their nocturnality, bats are relatively difficult to observe and study, exacerbating the low chances of
observing behavioural events. An accumulation of reports
on predation of bats is, however, gradually changing traditional 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, Esbrard & Vrcibradic 2007,
Nyffeler & Knrnschild 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 Hoyo
et al. 1999, Lesinski et al. 2009a, b), which prey upon them
during their coincidental nocturnal activities. Perhaps unexpectedly, due to the apparently differing activity schedules,
another important group of potential predators of bats are
diurnal avian raptors falcons, hawks, and eagles that
hunt predominantly during the day.
Previous researchers have found that predation by birds
could be responsible for about 10% of annual mortality of
2
P. Mikula et al.
METHODS
Data searching and exclusions
An extensive study of bibliographic sources was conducted
in 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 predator), in which the prey is alive when the predator first
attacks it (Begon et al. 2005). Therefore, we used only
records that could be considered, on the basis of dietary and
morphological characteristics of birds, as attacks for the
purpose 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 predator. Furthermore, we focused mainly on predation events
that took place during the day: as daytime predation we
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
P. Mikula et al.
RESULTS
Geographic distribution of attacks on bats
by diurnal birds
Altogether we obtained 1530 cases of predation of
bats by diurnal raptors and other diurnal birds (711
Accipitriformes, 608 Falconiformes, and 211 non-raptor
birds). Attacks on bats by diurnal birds were reported from
109 countries from all continents with the exception of Antarctica. Records of raptors attacking bats were obtained
from 107 countries (26 countries in Africa, 27 in Asia, five
in Australia and Oceania, 26 in Europe, 13 in North and
Central America, 10 in South America; Fig. 1a, b). Records
of non-raptors attacking bats were obtained from 45 countries (eight countries in Africa, 16 in Asia, one in Australia
and Oceania, 14 in Europe, four in North and Central
America, two in South America; Fig. 1c). The kernel density
function revealed that the density of scientific literature
records was highest in developed countries (Fig. 2a),
whereas Internet-derived records reached high densities also
outside these countries (Fig. 2b).
The northernmost observations of predation on bats by
Falconiformes, Accipitriformes, and other birds were from
Troms county (northern Norway) at 6900N, 1900E,
Lule (northern Sweden) at 6530N, 2140E and Tafjorden
(western Norway) at 6214N, 0725E, respectively. In the
first case, Falco columbarius attacked Eptesicus nilssonii
4
P. Mikula et al.
P. Mikula et al.
(a)
(b)
(c)
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
P. Mikula et al.
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
P. Mikula et al.
Bat family
Taken by
Accipitriformes (%)
Taken by
Falconiformes (%)
Emballonuridae
Hipposideridae
Megadermatidae
Molossidae
Mormoopidae
Mystacinidae
Noctilionidae
Nycteridae
Phyllostomidae
Pteropodidae
Rhinolophidae
Vespertilionidae
1.6
1.9
0.2
43.2
0.2
0
0
0.7
3.3
29.3
1.4
22.8
1.8
0
0.6
32.2
1.2
0.3
0.3
0
2.7
3.9
0.6
58.8
0.8
0.8
0
9
0
0
0
0
4.9
8.2
0
77
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
DISCUSSION
Bats as prey of diurnal birds
P. Mikula et al.
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
P. Mikula et al.
Non-raptors as predators
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
URBAN AREAS
P. Mikula et al.
CONCLUSIONS
Our results show that attacks on bats by diurnal birds are
globally distributed and reach the geographical limits of the
coexistence of both animal groups. Such predatory attempts
are present in the majority of extant raptor lineages as well
as in numerous other groups of diurnal birds. Moreover,
bats in the majority of extant bat families fall victim to predation by diurnal birds. Our results are thus supportive of
the avian predation hypothesis: predation by diurnal birds
could 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
Support for the avian predation hypothesis
Additional support for the avian predation hypothesis for
the evolution of nocturnality in bats came from observations on bats living on raptor-free islands. Perhaps the bestknown case is that of Nyctalus azoreum, a bat species
endemic to the Azorean archipelago. This species exhibits an
unusually high degree of diurnal activity that appears to
reflect 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 populations where large avian predators are absent or rare, such
as in the insectivorous bat Hipposideros ruber on So Tom
Island (Russo et al. 2011) and several pteropodids such as
Pteropus melanotus on Christmas Island (Hall et al. 2014)
and Pteropus samoensis on American Samoa (Thomson
et al. 1998). On Fiji, however, where Falco peregrinus is
present (Clunie 1972), the subspecies of Pteropus samoensis
is also diurnal but appears to behave more cryptically
(Wilson & Engbring 1992).
Bats have been observed to shift their emergence time
when 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 almost
absent among temperate insectivorous bats (reviewed by
Lima & OKeefe 2013). Such a pattern could be explained by
10
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
P. Mikula et al.
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
11
REFERENCES
P. Mikula et al.
12
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
P. Mikula et al.
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
13
P. Mikula et al.
14
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
P. Mikula et al.
Mammal Review (2016) 2016 The Mammal Society and John Wiley & Sons Ltd
SUPPORTING INFORMATION
Additional supporting information may be found in the
online version of this article at the publishers web-site.
Appendix S1. Index of all languages used in literature
searching.
Appendix S2. Summary table of diurnal raptors
(Accipitriformes and Falconiformes) reported to capture
bats with list of localities at country level and bat taxa
(arranged in alphabetical order).
Appendix S3. Summary table of non-raptorial diurnal
birds reported as bat hunters with list of localities at
country level and bat taxa (arranged in alphabetical order).
Appendix S4. References used in the Appendices.
15