Mammalia 2019; 83(1): 53–63
Daniel M. Parker* and Richard T.F. Bernard
The use of acoustic detectors for assessing bat
species richness and functional activity in a South
African National Park
https://doi.org/10.1515/mammalia-2017-0055
Received May 15, 2017; accepted February 27, 2018; previously
­published online April 14, 2018
Abstract: Insectivorous bats are a difficult group of
mammals to survey because they are small, nocturnal,
fly and often roost in hard to reach places during the day.
However, bats should not be neglected from biodiversity
assessments because they play pivotal roles in pest reg-
ulation and as biological indicators. We used acoustic
detectors to sample bat species richness at three sites
within the Mapungubwe National Park (MNP), South
Africa during the austral winter and summer of 2013. A
minimum of 11 species from six families were recorded,
with the clutter-edge foraging bats (Miniopteridae and
Vespertilionidae) and open-air foraging bats (Molossi-
dae), dominating. Bat activity was significantly higher
in summer compared to winter and this is likely linked
to higher prey availability and reduced thermoregula-
tory costs at this time. Our results represent the first
assessment of bat species richness in the MNP and our
data compare favourably with historical records for the
region. In addition, we provide evidence for the pres-
ence of at least one undescribed species. We advocate
the use of acoustic detectors for future bat surveys as
long as comprehensive reference call library data are
available.
Keywords: biodiversity; Chiroptera; echolocation;
Limpopo River; subtropical.
*Corresponding author: Daniel M. Parker, Wildlife and Reserve
Management Research Group, Department of Zoology and
Entomology, Rhodes University, PO Box 94, Grahamstown 6140,
South Africa; and School of Biology and Environmental Sciences,
University of Mpumalanga, Private Bag X11283, Nelspruit 1200,
South Africa, e-mail: daniel.parker@ump.ac.za
Richard T.F. Bernard: Wildlife and Reserve Management Research
Group, Department of Zoology and Entomology, Rhodes University,
PO Box 94, Grahamstown 6140, South Africa; and School of Biology
and Environmental Sciences, University of Mpumalanga, Private Bag
X11283, Nelspruit 1200, South Africa
Introduction
Of the 354  mammal species listed for southern Africa,
almost 20% are insectivorous bats; there are 68  species
of insectivorous bats in the southern African sub-region,
while in southern and Central Africa, there are as many
as 115  species (Monadjem et  al. 2010). Because of this
diversity, bats are excellent for the study of factors that
affect diversity (e.g. the effectiveness of protected areas
at protecting biodiversity). Bats are also widely acknowl-
edged as playing important ecological roles as predators
of insect pests (MacSwiney et al. 2008) and as important
indicator species for environmental health (Favilla and
Halffter 1997, McCracken et al. 2012). Although bats form a
substantial part of the mammalian biodiversity at any site,
they are often overlooked because of their cryptic behav-
iour (being nocturnal, flying, and living during the day
in caves, crevices, roofs and other hard to reach places).
However, for a full understanding of the diversity of an
area, bats should not be ignored.
The extreme North of South Africa has historically
been a stronghold for bats in southern Africa (Rautenbach
et  al. 1984). The apparently high diversity is believed to
be linked to the larger river systems (the Limpopo, in par-
ticular) which provide important habitat and resources,
and act as subtropical dispersal corridors (Rautenbach
et al. 1985). For example, in the Pafuri area of the Kruger
National Park, near the confluence of the Limpopo and
Luvhuvu rivers, some 44 bat species have been recorded,
representing 80% of the total South African bat diversity
(http://www.pafuri.co.za/bats.php). This list includes
South African species which occur only at Pafuri (e.g. Hip-
posideros vittatus Peters 1852, Nycteris woodii Andersen
1914 and Tadarida fulminans Thomas 1903).
Historically, studies of bat species richness and
overall community structure in Africa have relied
heavily on the live-capture of specimens to infer diver-
sity (Rautenbach et al. 1996, Cumming et al. 1997, Korine
and Pinshow 2004). In fact, almost all of our existing
knowledge of the bat communities of the extreme north-
ern part of South Africa, which is a known bat diversity
hotspot (Cooper-Bohannon et  al. 2016), comes from
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54      D.M. Parker and R.T.F. Bernard: Mapungubwe bats

live-capture studies (Rautenbach et al. 1984, 1985). This Materials and methods
is significant because when only using live-capture
to assess the species richness of bats, species may be
Study area
missed (O’Farrell and Gannon 1999) and it may be dif-
ficult to detect rare species (Flaquer et  al. 2007). Bat
MNP is located at the confluence of the Shashe and
acoustic data, therefore, has the potential to provide
Limpopo Rivers, South Africa (Lat: −22.2 S, Long: 29.4 E;
more detailed information on the distribution ranges
Figure 1). MNP was first identified as a site of natural and
and habitat preferences of bat species (Adams et  al.
cultural significance in 1922  when nine farms were set
2015) which may have been considered rare because
aside as a botanical reserve, and later (in 1947) declared
they are hard to capture. Acoustic data can also facili-
a wildlife sanctuary (SANParks 2013). However, the Apart-
tate the more accurate assignment and revision of IUCN
heid Government of 1948 repealed the declaration and
Redlist categories and associated information to better
settled white farmers in the area because the existence
conserve threatened bat species.
of an advanced African Kingdom was contrary to their
At any one location, the community of bats, which
rationale for Apartheid. Although the key archaeological
may be from five to 20  species, will include species
sites of the area (K2 and Mapungubwe Hill) were eventu-
with different foraging strategies (Monadjem et  al.
ally granted National Monument status in 1983 and 1984,
2010, Taylor et  al. 2013a). These strategies, which are
respectively, it was not until 1998 that MNP was given
closely linked to flight ability and echolocation, include
formal protection as a National Park and later (2003)
open-air foragers that fly high above the ground and
recognised as a World Heritage Site (SANParks 2013). In
catch flying insects; clutter-edge foragers that feed at
2006, a memorandum of understanding between the gov-
the edges of vegetation; and clutter foragers that fly
ernments of South Africa, Botswana and Zimbabwe was
within cluttered space such as between and within the
signed, in an effort to create a transfrontier park (known
branches of trees and feed on prey that may be in flight
as the Greater Mapungubwe Transfrontier Conservation
or sedentary (Monadjem et al. 2010). Importantly, echo-
Area) (SANParks 2013).
location calls can be used to identify the species and its
The size of the declared MNP is 15,237  ha and this
foraging strategy.
area includes seven privately owned, but contracted
We acknowledge that most studies which have
properties (SANParks 2013). Mean annual rainfall ranges
assessed the tools available for compiling bat species
between 350 and 400  mm and usually falls during the
inventories advocate for a combined approach (i.e.
austral summer months. Summers are hot (tempera-
using more than one sampling technique) (O’Farrell
tures often reaching 45°) and winters are normally
and Gannon 1999, Korine and Pinshow 2004, Flaquer
mild, but frost can occur (SANParks 2013). Elevation in
et al. 2007). However, with the constant improvement of
acoustic detectors and the associated analysis software,
the ability to document bat species presence and distri-
butions is greatly improved (see Adams et  al. 2015). In
addition, the use of acoustic detectors avoids the neces-
sity for handling these small mammals that can suffer
from capture myopathy (Jung et al. 2002). Moreover, some
bat species that are notoriously difficult to live-capture
can be detected using ground-based acoustic detectors
(Adams et al. 2015). In this paper we use acoustic detec-
tors to assess the species richness and activity levels of
bats at three sites in the Mapungubwe National Park
(MNP) of South Africa. MNP is a World Heritage Site and
is located in the extreme North of South Africa. Although
bat museum specimens have been collected from the
area, they are generally sparse given the significance of
Figure 1: The Mapungubwe National Park, South Africa showing the
the Limpopo River valley as a bat biodiversity hotspot
position of the three sites used to sample bats using SM2 Songme-
(Rautenbach et  al. 1984, 1985) and were all collected at ters in the austral winter and summer 2013.
least 15  years prior to the official promulgation of the (A) Limpopo tented camp, (B) Confluence viewpoint and
National Park (Monadjem et al. 2010). (C) Poacher’s corner.

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the park is generally low (400–600 m) and the highest
point is 626  m. The geology of the area is diverse but
weathered granitic outcrops or “koppies” dominate
the landscape and provide habitat for a diverse range
of plants and animals. A unique feature of the MNP is
the Limpopo floodplain where tall riparian woodland or
gallery forest is present (officially known as subtropi-
cal alluvial ­vegetation). The dominant tree species in
this ­threatened habitat include Acacia xanthophloea,
Xanthocercis zambesiaca, Hyphaene petersiana and
Salvadora australis (SANParks 2013). It is important to
note that this vegetation type consists mostly of large
trees with an underdeveloped sub-canopy, providing
­important flightpaths between the trees themselves for
bats.
Acoustic sampling
Sampling at each site within MNP was conducted using
two SM2 Song Meters (Wildlife Acoustics, Concord, MA,
USA). We sampled for five consecutive nights (Skalak
et  al. 2012) approximately midway through the austral
winter and summer of 2013. The winter sampling took
place between 1 and 5 July 2013 and included individual
sampling stations at the tented camp (n = 6 trap nights),
confluence view point (n = 2 trap nights), and poacher’s
corner (n = 2 trap nights) sites (Figure 1). The summer
sampling was conducted between 4 and 8  November
2013 and included individual sampling stations at the
tented camp (n = 6 trap nights) and poacher’s corner
(n = 4 trap nights) sites (Figure 1). We excluded the con-
fluence view point site from the summer sampling. This
was because it was (a) relatively close to the poacher’s
corner site and (b) because the winter sampling recorded
substantially more noise rather than actual bat calls,
possibly because this site was at the top of the granite
hill overlooking the Limpopo River floodplain and had
very few large trees. Individual sampling stations (in
both seasons) were positioned at least 50 m apart (range:
53  m–1.9 km) and faced different directions rendering
them statistically independent. All sampling stations
(except for the confluence viewpoint site) were located
in Limpopo gallery forest habitat. The tented camp site
was located approximately 200  m from the Limpopo
River itself and consisted of several permanent, man-
made structures (i.e. canvas tents on wooden platforms
and a small house and workshop) within the forest.
During sampling, the bat detectors were placed facing
potential flight paths. The poacher’s corner site was on
the Limpopo River itself with the detector positioned on
D.M. Parker and R.T.F. Bernard: Mapungubwe bats      55
a large branch over-hanging the water (i.e. at the wood-
land edge).
Each SM2 bat detector is equipped with a water-
proof acoustic microphone connected to a waterproof
unit, which includes four interchangeable flashcards for
storing recordings. The units were programmed to record
in mono L (i.e. with one microphone on the left mic input)
at a 384 kHz sampling frequency with 16 bit sample reso-
lution and only to record sounds above 12 dB. Each detec-
tor was mounted ~1.5  m above ground to prevent false
recordings from wind and rain and placed at a 45° angle
with the microphones pointing upwards to ensure that
they remained waterproof. Recordings of bat calls were
made from sunset to sunrise in each season to coincide
with the observed bi-modal peaks in the nocturnal activ-
ity of bats.
Individual calls were identified to species level manu-
ally using SonoBAT software (DNDesign, Arcata, CA, USA)
with reference to the Rhodes University bat call library
(consisting of 21  species that were passive recordings
from bats found in day roosts at MNP and elsewhere in
southern Africa) and published data (Monadjem et  al.
2010, 2017, Happold and Happold 2013, Taylor et al. 2013a,
Linden et al. 2014, Weier et al. 2017). Aspects of the calls
which were taken into account during species identifica-
tion were: Fc = the characteristic frequency – the flattest
portion of the call (kHz); Fmax = maximum frequency
(kHz); Fmin = minimum frequency (kHz); FK = frequency
at the “knee” or where the call slope switches abruptly
from a downward to a level slope; the call duration (ms)
and the number of calls/second. The process of species
identification was collaborative, whereby both observers
(DP and RB) screened individual calls together and agreed
on a positive identification. If a call could not be identified
using our library or the published literature, it was des-
ignated as unknown and not used in the later analyses.
Using this approach, the number of species at each sam-
pling station was calculated per hour per night. The pro-
gramme EstimateS (Colwell 2013) was used to calculate
the species richness. Two species richness estimators, the
Incidence Coverage-based Estimator (ICE) (Chazdon et al.
1998, Chao et al. 2000) and Chao 2 (Chao 1984) were also
calculated to assess sampling efficiency. This process was
limited in that individual bats of the same species could
not be identified. Thus, bat species activity was calcu-
lated using an activity index (following Hayes 1997, Skalak
et  al. 2012), and used as a proxy for species abundance.
For each hour of the night, at each site, the presence or
absence (1 or 0) of each species was recorded. These activ-
ity “events” (i.e. each 1) were then summed and divided
by the total number of possible hourly events for each site
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56      D.M. Parker and R.T.F. Bernard: Mapungubwe bats
(Skalak et al. 2012). Recorded species were also allocated
to foraging strategies based on the published literature
(Monadjem et al. 2010). The difference between overall bat
activity in winter and summer was tested using a Mann-
Whitney U-test in R (R Development Core Team 2014).
Assignment of species
We recorded 20 putative bat species at MNP (see Results).
Of these 20  species assignments, we are most confident
of our identification of seven species (Hipposideros caffer­
Sundevall 1846, Rhinolophus smithersi Taylor et al. 2012,
Rhinolophus simulator Andersen 1904, Nycteris ­thebaica
Geoffroy 1818, Otomops martiensseni Matschie 1897,
­Neoromicia nana Peters 1952, Neoromicia ­zuluensis Roberts
1924). The distinctive calls of H. caffer, R. smithersi, R. simu-
lator, O. martiensseni and N. nana meant that the calls of
these species were extremely unlikely to be incorrectly
assigned (Supplementary Appendix 1). In addition, we
were able to record the echolocation calls of R.  smithersi,
N. ­thebaica and N. zuluensis from day roosts in MNP during
our sampling trips, providing site-specific reference calls for
these species. Moreover, most of these seven species show
very little overlap with other southern African bat species
(Table 1). Although O. martiensseni is an extremely diffi-
cult/near impossible species to live-capture, its presence
within MNP has recently been independently confirmed
using acoustic-only detection (Adams et al. 2015).
The remainder of the molossids (five species), a mini-
opterid (one species) and vespertilionids (four species)
were more challenging to assign to species level. However,
previous acoustic and live-capture sampling of bats in the
Soutpansberg mountain range (~100 km South of MNP) has
recorded all 10 of these species (Taylor et al. 2013a, Linden
et  al. 2014, Weier et  al. 2017). Importantly, our acoustic
data compares favourably with the acoustic data presented
in Taylor et al. (2013a), Linden et al. (2014) and Monadjem
et  al. (2017) for Pipistrellus rusticus Tomes 1861, Neoromi-
cia capensis Smith 1829, Laephotis botswanae Setzer 1971,
Chaerephon ansorgei Thomas 1913, Chaerephon pumilus
Cretzschmar 1826, Mops midas Sundevall 1843, Mops
c­ondylurus Smith 1833 and Tadarida aegyptiaca Geoffroy
Saint Hilaire 1818 (see Supplementary Appendix 1).
The call characteristics presented in our study for
Myotis tricolor Temminck 1832 and Miniopterus natal-
ensis do not correspond to the data presented by Taylor
et  al. (2013a) for the same putative species. While the
mean characteristic frequency (Fc) which we recorded
for M. tricolor (42.7 kHz) was lower than that presented in
Taylor et al. (2013a) (52.4 kHz) and Monadjem et al. (2010)
(47.8 kHz), the calls which we assigned as M. tricolor also
had a broad bandwidth (~30 kHz) and were of a short dura-
tion (~3 ms), which is consistent with the published liter-
ature ­(Monadjem et  al. 2010, Taylor et  al. 2013a, Linden
et al. 2014). Thus, we suspect that what we have assigned
as M.  tricolor is likely to be correct but an example of
local variation in call structure, especially since our sam-
pling was conducted along the Limpopo River and not at
the higher elevations (845–1618  m) of the Soutpansberg
(Taylor et al. 2013a).
The characteristic frequency which we recorded
for Miniopterus natalensis (49.9 kHz) is lower than the
characteristic frequency cited by Taylor et  al. (2013a)
(54.1  kHz) but it compares favourably with the char-
acteristic frequency quoted by Monadjem et  al. (2010)
(49.7 kHz). In addition, Taylor et al. (2013b) state that the
typical frequency at the “knee” (FK; where the call slope
switches abruptly from a downward to a level slope) for
M. ­natalensis is between 54 and 58 kHz. Our data for the FK
of M. natalensis (53.61 ± 2.27 kHz) essentially falls within
this range. Furthermore, all other call parameters, includ-
ing maximum frequency (Fmax), bandwidth and duration
compare favourably with published ranges (Monadjem
et al. 2010, Taylor et al. 2013a).
We were unable to confidently assign species iden-
tifications to three species which were recorded during
our study (Rhinolophus sp. and two unknown vesper-
tilionids). We believe that the unknown Rhinolophus
species is likely to be an undescribed species for southern
Africa given the unique call structure of rhinolophid bats
(see Supplementary Appendix 1). This putative species
(Fc = 100  kHz) has also been recorded from at least two
sites in the Soutpansberg using acoustic detectors (Taylor
et  al. 2013a), but has never been captured and acces-
sioned in any museum collection (Monadjem et al. 2010).
The unknown vespertilionid (36 kHz) could potentially be
Scotophilus dinganii Smith 1833 (Monadjem et  al. 2010).
The species has been collected from MNP historically and
our acoustic data indicates a peak frequency of 36.3 kHz,
an intermediate bandwidth (22.5 kHz) and an intermedi-
ate duration (5.8 ms). These parameters are similar to the
published call parameters for S. dinganii (Monadjem et al.
2010, Taylor et al. 2013a) but they need to be confirmed by
live-capture from our study site. The unknown vespertil-
ionid (72 kHz) was only recorded once during our winter
sampling which makes it difficult to assess the overall call
parameters and how they compare to existing data. It is
possible that this recording was merely a variation of the
call of Neoromicia nana (Fc = 68.5 kHz). However, further
sampling and/or live-capture is required to confirm this
suspicion.
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 Table 1: Summary table of the 20 putative bat species identified at three sites within the Mapungubwe National Park, South Africa in winter (July) and summer (November) 2013.

Species Overlap species Foraging n Season Call characteristics

category
Fc Fmax Fmin FK DUR CALLS

Hipposideridae
 Hipposideros caffer – Clutter 14 Both 143.00 ± 1.64 143.28 ± 1.63 124.99 ± 5.92 143.14 ± 1.64 7.41 ± 0.91 12.29 ± 7.81
Rhinolophidae
 Rhinolophus smithersi – Clutter/clutter- 19 Both 47.23 ± 1.62 47.47 ± 1.50 43.27 ± 2.65 47.26 ± 1.54 44.74 ± 22.83 8.02 ± 3.70
edge
 Rhinolophus simulator – Clutter 20 Both 79.70 ± 1.02 79.86 ± 0.99 75.43 ± 4.93 79.71 ± 1.01 37.79 ± 9.97 7.46 ± 3.46
 Rhinolophus sp. (100 kHz) – Clutter (?) 12 Both 100.72 ± 0.52 100.93 ± 0.77 91.34 ± 6.08 100.72 ± 0.52 34.89 ± 14.42 8.32 ± 3.39
Nycteridae
 Nycteris thebaica M. fraterculus/N. nana Clutter 1 Winter 62.50 83.40 62.40 63.10 1.68 11.63
Molossidae
 Chaerephon ansorgei T. ventralis/C. nigeriae/ Open-air 20 Both 18.21 ± 1.01 20.92 ± 3.39 17.59 ± 1.03 19.38 ± 1.49 10.07 ± 3.03 2.47 ± 1.43
T. fulminans
 Chaerephon pumilus T. aegyptiaca/M. Open-air 20 Both 26.65 ± 2.53 34.87 ± 5.75 24.67 ± 2.68 29.72 ± 3.05 8.80 ± 2.65 4.24 ± 1.89
condylurus/T. mauritianus
 Mops condylurus C. pumilus/T. aegyptiaca/ Open-air 6 Both 29.12 ± 0.70 30.72 ± 1.52 28.45 ± 0.50 29.82 ± 0.97 15.44 ± 3.78 5.57 ± 1.11
T. perforatus
 Mops midas O. martiensseni Open-air 13 Both 13.11 ± 1.04 14.66 ± 1.46 12.33 ± 1.42 13.71 ± 0.98 14.79 ± 7.35 4.29 ± 2.73
 Otomops martiensseni M. midas Open-air 20 Both 10.74 ± 0.63 11.52 ± 0.60 10.28 ± 0.50 10.81 ± 0.64 22.68 ± 13.89 3.98 ± 2.40
 Tadarida aegyptiaca T. mauritianus/C. pumilus Open-air 20 Both 23.68 ± 1.51 29.23 ± 5.77 22.47 ± 1.74 25.72 ± 2.92 9.87 ± 3.93 4.10 ± 2.72
Miniopteridae
 Miniopterus natalensis P. rusticus Clutter-edge 15 Both 49.91 ± 0.95 67.84 ± 4.75 49.39 ± 0.88 53.61 ± 2.27 4.96 ± 1.31 7.30 ± 2.65
Vespertilionidae
 Laephotis botswanae S. dingani/M. Clutter-edge 20 Both 31.46 ± 1.47 53.20 ± 7.20 30.75 ± 1.28 37.38 ± 1.77 6.49 ± 2.68 6.79 ± 2.71
welwitschii/E. hottentotus
 Myotis tricolor M. bocagei Clutter-edge 4 Both 42.68 ± 0.70 70.40 ± 3.85 40.88 ± 1.98 52.68 ± 3.43 3.03 ± 0.70 11.20 ± 7.85
 Neoromicia capensis S. viridis/N. schlieffeni Clutter-edge 20 Both 39.54 ± 1.17 63.06 ± 5.75 38.59 ± 1.21 46.16 ± 3.94 5.18 ± 1.45 7.36 ± 2.31
 Neoromicia nana N. thebaica Clutter-edge 20 Both 68.53 ± 2.10 85.09 ± 10.70 67.61 ± 2.57 72.45 ± 3.38 4.24 ± 0.83 8.15 ± 3.64
 Neoromicia zuluensis P. hesperidus/P. rusticus Clutter-edge 20 Both 48.11 ± 1.17 63.23 ± 4.44 47.70 ± 1.36 52.09 ± 2.33 4.91 ± 1.36 7.47 ± 2.12
 Pipistrellus rusticus M. natalensis/H. anchiettae Clutter-edge 19 Both 55.20 ± 0.92 64.41 ± 3.75 54.00 ± 1.05 57.68 ± 1.34 4.70 ± 1.59 6.11 ± 3.12
 Unknown vespertilionid L. botswanae/S. dingani/ Clutter-edge (?) 12 Both 36.36 ± 1.02 57.92 ± 7.02 35.43 ± 1.47 41.28 ± 1.49 5.83 ± 2.15 6.65 ± 1.56
(36 kHz) E. hottentotus
 Unknown vespertilionid N. nana Clutter-edge (?) 1 Winter 72.5 88.4 72.5 77.5 2.34 7.12
(72 kHz)

Data are means ± SD. n, The number of independent bat calls used to determine the call parameters; Season, the season(s) in which each species was recorded; Fc, the characteristic
­frequency – the flattest portion of the call (kHz); Fmax, maximum frequency (kHz); Fmin, minimum frequency (kHz); FK, frequency at the “knee” or where the call slope switches abruptly from a

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downward to a level slope V; DUR, call duration (ms); CALLS, the number of calls/second; Foraging category and overlap species following Monadjem et al. (2010).
D.M. Parker and R.T.F. Bernard: Mapungubwe bats      57
 58      D.M. Parker and R.T.F. Bernard: Mapungubwe bats

Results A 12

Using acoustic monitoring at three sites, a total of 20 puta- 10

tive bat species representing six families were recorded in

the winter (July) and summer (November) of 2013 at MNP 8

(Table 1). The clutter-edge foraging bats (Miniopteridae Overall

Species richness
and Vespertilionidae) were the most speciose (possibly 6 Rhinolophids
Molossids
nine species), followed by the open-air foraging bats (pos- Vespertilionids

sibly six Molossid species). The bats which forage amongst 4

cluttered vegetation (Hipposideridae and Rhinolophidae)

were not as well represented as the other groups (Table 1). 2

Almost all of the species were recorded in both winter and

summer. However, Nycteris thebaica and an unknown ves- 0
0 2 4 6 8 10 12
pertilionid (Unknown Vesper. 72 kHz) were only recorded Hours after sunset
–2
during the winter sampling (Table 1).
The ICE and Chao 2 species richness estimators indi- B 10 Overall
cated that the acoustic detectors missed approximately Rhinolophids
Molossids
one species over the entire 20 trap nights of sampling Vespertilionids
8
(Figure 2; ICE = 21.09; Chao 2 = 20.95).
Overall bat species richness declined as the night pro-
6
gressed and was generally lower in the winter compared
Species richness

to the summer (Figures 3 and 4). By contrast, bat species

richness stayed consistently high (~17  species) during 4

the night in summer, but dropped off sharply at dawn

(Figures 3 and 4). At the site level, the species richness 2

of the rhinolophids (clutter foragers) did increase during

the early hours of the morning at the poacher’s corner 0
0 2 4 6 8 10 12

Hours after sunset

–2

35
C 9.0

8.0
30
Overall
7.0 Rhinolophids
Molossids
25 6.0 Vespertilionids
Species richness

5.0
Species richness

20
4.0

15 S(est) 3.0
ICE mean
Chao 2 mean 2.0
10 1.0

0.0
5 0 2 4 6 8 10 12
–1.0
Hours after sunset
0 –2.0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
Trap night Figure 3: Changes in bat species richness (by family) at three differ-
ent sites in winter (2013) at Mapungubwe National Park, South Africa.
Figure 2: Species accumulation curve for all acoustic data (winter (A) Tented camp, (B) Poacher’s corner and (C) Confluence viewpoint.
and summer 2013) recorded at Mapungubwe National Park, South
Africa.
S(est) is the observed data (smoothed over 100 iterations) and
and confluence viewpoint sites in winter (Figure  3). The
the ICE and Chao 2 are the species richness estimators. Error bars molossids were generally the most diverse group during
represent SD. the night at all three sites in the winter, closely followed

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 D.M. Parker and R.T.F. Bernard: Mapungubwe bats      59

A A 1.20
14.0
Overall
Rhinolophids
Molossids 1.00
12.0 Vespertilionids

0.80
10.0

Activity index
Overall
0.60 Rhinolophids
8.0 Molossids
Species richness

Vespertilionids
0.40
6.0

0.20
4.0

0.00
2.0 0 2 4 6 8 10 12
Hours after sunset

0.0 B 0.90
0 2 4 6 8 10 12
0.80
–2.0 Hours after sunset
0.70

B 16.0 Overall 0.60

Activity index
Rhinolophids
14.0 Molossids 0.50
Vespertilionids Overall
Rhinolophids
0.40 Molossids
12.0 Vespertilionids
0.30
10.0
0.20
Species richness

8.0
0.10

6.0 0.00
0 2 4 6 8 10 12
4.0 Hours after sunset

2.0 C 1.60

0.0 1.40
0 2 4 6 8 10 12

–2.0 1.20
Hours after sunset

1.00
Activity index

Figure 4: Changes in bat species richness (by family) at two Overall

Rhinolophids
­different sites in summer (2013) at Mapungubwe National Park, 0.80 Molossids
Vespertilionids
South Africa. 0.60
(A) Tented camp and (B) Poacher’s corner.
0.40

0.20

0.00
by the vespertilionids (Figure 3). Very similar trends 0 2 4 6 8 10 12

were observed during the summer sampling (Figure 4). Hours after sunset

However, rhinolophid species richness (although still

low) at the poacher’s corner site was not as variable over
the course of the nights sampled.
Overall bat activity declined as the night progressed
in the winter and was significantly lower in the winter
compared to the summer (Figures 5 and 6; W = 301,
df = 38, p < 0.05). In summer, bat activity stayed consist-
ently high during the night (Figure 6). At the site level,
the rhinolophids were not very active in the winter,
but their activity did increase slightly during the early
hours of the morning at the poacher’s corner and con-
fluence viewpoint sites (Figure 5). The molossids were
the most detected group during the night at all three
sites in the winter, followed by the vespertilionids
Figure 5: Changes in bat activity (by family) at three different sites
in winter (2013) at Mapungubwe National Park, South Africa.
(A) Tented camp, (B) Poacher’s corner and (C) Confluence viewpoint.
(Figure 5). However, very little vespertilionid activ-
ity was recorded at the confluence viewpoint in winter
(Figure 5). Very similar trends were observed during the
summer sampling, but the separation between the three
family groups was more distinct (Figure 6). Molossids
appeared to dominate the bat community at the tented
camp but the poacher’s corner site showed what appears
to be increased abundance of the vespertilionids and
­rhinolophids (Figure 6).

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60      D.M. Parker and R.T.F. Bernard: Mapungubwe bats

A 1.40 1859, Pipistrellus hesperidus Temminck 1840 and Scot-

ophilus dinganii; Monadjem et  al. 2010). Because of our
1.20
acoustic-only approach it is possible that we were unable
1.00 to assign recordings to one or more of these species, espe-
cially those that are considered more common in the area
Activity index

0.80
Overall
Rhinolophids (e.g. S. dinganii; Monadjem et  al. 2010). However, it is
Molossids
0.60 Vespertilionids important to note that no echolocation calls have been
0.40 recorded for T. perforatus in southern Africa (Monadjem
et  al. 2010). Nevertheless, our approach did detect four
0.20
to potentially seven additional species which have not
0.00
0 2 4 6 8 10 12
been collected as museum specimens from the area (viz.
Hours after sunset a Rhinolophus sp., Mops condylurus, Otomops martienss-
eni, Laephotis botswanae, Myotis tricolor and possibly two
B 2.00
unknown vespertilionids at characteristic frequencies of
1.80
~36 and 72 kHz, respectively).
1.60
Clement et  al. (2014) highlight that acoustic surveys
1.40
of bats may be prone to an increased number of false posi-
Activity index

1.20

1.00 Overall tives (i.e. greater Type I statistical error) when not used in
Rhinolophids

0.80
0.60
0.40
0.20
0.00
0 2 4 6 8 10
Hours after sunset
Figure 6: Changes in bat activity (by family) at two different sites in
summer (2013) at Mapungubwe National Park, South Africa.
(A) Tented camp and (B) Poacher’s corner.
Discussion
Our results represent the first detailed assessment of the
bat species richness and functional activity of the MNP.
Importantly, our acoustic data compare favourably with
historical museum records for the area (Monadjem et al.
2010). Museum specimens have been collected at or
near the confluence of the Limpopo and Shashe Rivers
­(Monadjem et  al. 2010) and include 13 of the species
which we recorded acoustically (viz. Hipposideros caffer,
Rhinolophus smithersi, Rhinolophus simulator, Nycteris
thebaica, Chaerephon ansorgei, Chaerephon pumilus,
Mops midas, Tadarida aegyptiaca, Miniopterus natalen-
sis, Neoromicia capensis, Neoromicia nana, Neoromicia
zuluensis and Pipistrellus rusticus). We failed to record
the other nine species which have been accessioned
as museum specimens from the area (viz. Rhinolophus
darlingi Andersen 1905, Taphozous perforatus Geoffroy
Saint-Hilaire 1818, Nycteris woodii, Sauromys petrophilus
Roberts 1917, Eptesicus hottentotus Smith 1833, Hypsugo
anchietae Seabra 1900, Nycticeinops schlieffeni Peters
Molossids
Vespertilionids
combination with other techniques such as live-capture
or analytical approaches such as occupancy modelling.
The authors argue that the potential for the misidentifica-
tion of bat species in acoustic-only surveys can negatively
affect accurate inferences of patterns of diversity (Clement
12
et al. 2014). Thus, it is important to acknowledge such a
limitation in our study, especially since we did not develop
a local bat call library based on live-captures. In addition,
there can be significant variation in the call structures of
bats (Monadjem et  al. 2017) and by using acoustic-only
sampling, it is not possible to know exactly how large this
variation is for our study site. The calls of Hipposideros
caffer, Rhinolophus smithersi, Rhinolophus simulator, Rhi-
nolophus sp., Otomops martiensseni and Neoromicia nana
have very little/no overlap with other species (Monadjem
et al. 2010, Taylor et al. 2013a). In addition, we recorded
exemplar calls for R. smithersi, Nycteris thebaica and
Neoromicia zuluensis from day roosts in MNP during our
sampling trips. However, these represent only eight of
our proposed 20  species assignments. All other species
have at least some overlap with several species (Table 1,
Monadjem et  al. 2010). We acknowledge, therefore, that
our species assignments, for the molossids and vespertil-
ionids in particular, are tentative until they can be verified
through live-capture.
An alternative would be to adopt a more conserva-
tive approach whereby species with broadly overlapping
frequencies are combined into single species-groups
(Taylor et  al. 2013a) until verification. Following such
an approach, Chaerephon pumilus, Tadarida aegyptiaca
and Mops condylurus would likely form one group and
Miniopterus natalensis and Pipistrellus rusticus a second
(Taylor et al. 2013a). In addition, what we have assigned

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as Laephotis botswanae, Neoromicia capensis and Neoro-
micia zuluensis may form part of a larger, third group with
Scotophilus dinganii and Eptesicus hottentotus (Taylor
et al. 2013a). The latter two species, although not identi-
fied by us, have been previously collected in the MNP
area (Monadjem et  al. 2010). Thus, if we excluded our
two unidentified species, and Nycteris thebaica because
it was only recorded in one pass, our study has identified
a minimum of 11 bat species for MNP using acoustic sam-
pling only.
Bat activity was higher in summer than winter and
this supports previous work (Taylor et  al. 2013b). The
increased activity in the summer months is likely linked
to the increased activity levels of insect prey (Taylor et al.
2013b). Indeed, Taylor et  al. (2013b) demonstrated that
seasonal changes in bat activity are tightly linked to higher
insect prey availability. Bat activity will also increase
during pregnancy and this is often in the summer months
in southern Africa (Monadjem et  al. 2010). In addition,
increased activity is also linked to reduced thermoregula-
tory costs during the summer months (Schmidt-Nielsen
1984). Given their high surface area to volume ratios, bats
are less likely to lose significant metabolic heat in the
summer while foraging compared to the winter when tem-
peratures are lower (Schmidt-Nielsen 1984).
Qualitative differences in functional bat activity were
evident in our study. Molossid bats were generally most
active (AI consistently > 0.2) at all sites in summer and
winter, followed by the vespertilionid (AI generally < 0.2)
and then the rhinolophid bats (AI generally < 0.1). Such
a finding is unsurprising given the known differences
in acoustic detectability across bat species and fami-
lies (Monadjem et  al. 2017). In general, molossid bats in
southern Africa have the greatest maximum detection dis-
tance (~25  m), followed by the vespertilionids (5–20  m),
and finally the rhinolophids (<2  m) (Monadjem et  al.
2017). This trend is due to the molossids generally calling
at lower frequencies than the other two families and so
their echolocation calls do not attenuate as quickly as
the higher frequency calls of the vespertilionids and rhi-
nolophids (Monadjem et al. 2017). In addition, low-inten-
sity or whispering bats are also often under-represented in
activity or relative abundance data from acoustic surveys
(Monadjem et al. 2017). The fact that we only recorded the
whispering Nycteris thebaica once during the winter sam-
pling supports this contention.
Qualitative differences were also observed at the indi-
vidual site level. Although the molossid bats (open-air for-
agers) dominated bat activity at all sites in summer and
winter, the vespertilionid (clutter-edge foragers) and rhi-
nolophid bats (clutter foragers) tended to be more active/
D.M. Parker and R.T.F. Bernard: Mapungubwe bats      61
abundant at the poacher’s corner site than both the tented
camp and confluence viewpoint sites. These differences
in activity are likely due to the variability of the habitat,
and hence resources available to bats, at the sites. The
poacher’s corner site was probably the most diverse site,
in terms of habitat, compared to the other two sites. The
detector was placed along the Limpopo River which was
lined with tall trees and has a well-established understory.
In addition, several dis-used military buildings (includ-
ing an old ammunition bunker) and rocky cliff faces are
located nearby to this site. These conditions clearly suit
both the foraging and roosting requirements of many of
the vespertilionid and rhinolophid bats recorded in our
study (Monadjem et  al. 2010) and thus why their activ-
ity was greatest at this site. The confluence viewpoint
site was located above (~150  m) the Limpopo River on a
large granite outcrop with several large crevasses present
which would likely provide suitable roosting sites for
both molossids and rhinolophids (Monadjem et al. 2010).
Without suitable roost sites, and being some distance
from suitable foraging habitat, the confluence viewpoint
was probably not ideal for monitoring vespertilionid activ-
ity. By contrast, the tented camp site probably provided
more of an intermediate sampling site compared to the
other two. The tented camp site had several man-made
structures present (suitable for all three bat families) and
many tall trees (suitable for vespertilionid roosting), but
the understory was not as well-developed as the poacher’s
corner site, perhaps explaining the substantially lower
clutter-foraging bat activity.
In conclusion, our study has demonstrated that acous-
tic detectors can be used successfully for a preliminary
survey of bats along the Limpopo River, which is a known
bat biodiversity hotspot in southern Africa. Our species
richness estimators indicate that although we may have
missed one potential species, our sampling was sufficient
to detect the vast majority of the bat community present
at MNP. Significantly, our work shows that with access
to an adequate call reference library and published call
parameters, acoustic detectors can provide reliable infor-
mation about bat species richness in subtropical habitats.
However, the assessment we present here would clearly
benefit from additional sampling in the form of live-cap-
tures and more acoustic trap nights. There is at least one
species which we recorded acoustically that appears to be
new to science (Rhinolophus sp. 100 kHz). MNP is only the
second location in South Africa where this putative species
has been recorded and we recommend an intensive effort
to capture and describe the species. We further recom-
mend that a concerted effort be made to formalise a com-
prehensive (and perhaps open-access) bat call reference
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62      D.M. Parker and R.T.F. Bernard: Mapungubwe bats
library for southern Africa, initially through the collabora-
tion of bat biologists, but later with targeted expeditions
to fill any known gaps. Although the s­ cientific community
in southern Africa has gone some way to publish verified
bat call parameters (see Monadjem et al. 2010, 2017, Taylor
et al. 2013a,b, Linden et al. 2014, Weier et al. 2017), these
remain, apart from Monadjem et  al. (2010), largely site-
specific and there is much need for a national database.
Such a database would potentially obviate the need to
always combine acoustic surveys with live-captures, and
this would be a far more ethical approach to bat sampling
in a time when we continue to lose biodiversity at a rapid
rate on a global scale.
Acknowledgments: We thank Rhodes University for fund-
ing this work and the support and assistance of SAN-
Parks. Our field assistants: Penny Bernard, Kelly Bernard,
Andrea Parker and Keagan Parker (in utero) are also
warmly acknowledged for their invaluable assistance. The
manuscript was improved by the constructive comments
of Peter Taylor, Stéphane Aulagnier and three anonymous
referees.
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