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RESEARCH ARTICLE
A giant among dwarfs: a new species of galago (Primates:
Galagidae) from Angola
Magdalena S. Svensson
1
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Elena Bersacola
1
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Michael S. L. Mills
2
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Rachel A. Munds
3
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Vincent Nijman
1
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Andrew Perkin
1,4
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Judith C. Masters
5
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S
ebastien Couette
6
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K. Anne-Isola Nekaris
1
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Simon K. Bearder
1
1
Nocturnal Primate Research Group, Oxford
Brookes University, Oxford OX3 0BP, UK
2
A. P. Leventis Ornithological Research
Institute, University of Jos, Jos 930001,
Nigeria
3
Department of Anthropology, University of
Missouri Columbia, Columbia, Missouri
65211
4
Tanzania Forest Conservation Group, Dar
es Salaam, Tanzania
5
African Primate Initiative for Ecology and
Speciation, Africa Earth Observatory
Network, Earth Stewardship Science
Research Institute, Nelson Mandela
Metropolitan University, Port Elizabeth
6031, South Africa
6
EPHE, PSL Research University, Paris,
France & UMR CNRS 6282
“Biog
eosciences”, Univ. Bourgogne Franche-
Comt
e, Dijon, 21000, France
Correspondence
Magdalena Svensson, Nocturnal Primate
Research Group, Oxford Brookes
University, Oxford, UK.
Email: svensson_magdalena@hotmail.com
Abstract
Objectives: Based on vocalization recordings of an unknown galago species, our main objectives
were to compare morphology and call structure with known closely-related taxa and describe a
new species of galago.
Materials and methods: We conducted field surveys in three forest habitats along the escarp-
ment region in western Angola (Kumbira Forest, Bimbe Area, and Northern Scarp Forest), and
examined galago specimens from museums worldwide. We digitized and analyzed calls using Avi-
soft SASLab Pro software. We also compared museum specimens from Angola with other Galago
and Galagoides specimens, and conducted comparative analyses (ANOVA and between group prin-
ciple component analysis) based on a set of twelve linear measurements of skulls and teeth.
Results: We describe the new species to which we give the name Angolan dwarf galago, Gala-
goides kumbirensis sp. nov. The new species has a loud and characteristic crescendo call, used by
other Galagoides spp. (sensu stricto) in West Africa to attract companions and repel rivals. How-
ever, this call shows species-typical differences from its closest relatives. Galagoides kumbirensis sp.
nov. is also distinguished by differences in the skull morphology, pelage color and facial markings,
as well as a larger body size, similar to that of Galago moholi, which is not known to be sympatric.
Conclusion: This discovery points to the importance of Angolan forests as refuges for endemic
biodiversity. These forests are under severe threat from overexploitation, and there is an urgent
need to establish conservation measures and designate protected areas.
KEYWORDS
Bushbaby, cryptic species, Galagoides, morphology, strepsirrhine
1
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INTRODUCTION
Previously unrecognized species of terrestrial mammals are being dis-
covered at an ever-increasing rate as researchers expand their activities
into new areas of forests and woodlands, and conduct extensive sur-
veys (Ceballos & Ehrlich, 2009; Mittermeier, Rylands, & Wilson, 2013;
Wilson & Mittermeier, 2011). Some of these discoveries are made
because of a change in views of what a species is, that is, dependent
on which species concept is adopted (Cotterill, Taylor, Gippoliti, Bishop,
& Groves, 2014; Groves & Grubb, 2011; Isaac, Mallet, & Mace, 2004)
and owing to the use of different technologies, including molecular
analysis, to recognize species diversity within cryptic taxa (i.e., species
that are very similar morphologically even though they are reproduc-
tively isolated: Bickford et al., 2007). In the field crucial information on
the presence of cryptic taxa is often gathered with the aid of new
methodologies such as camera trapping and remote recording (Hart
et al., 2012; Li, Zhao, & Fan, 2015). In an era when many new species
descriptions rely heavily on genetic evidence, it has become atypical to
distinguish new taxa based on morphology and vocalizations alone.
However, in groups such as molluscs (Alvim & Pimenta, 2013), crusta-
ceans (Vonk & Jaume, 2014), insects (Gibbs, 2010; Hertach, Trilar,
Wade, Simon, & Nagel, 2015), birds (Ng, Eaton, Verbelen, Hutchinson,
Am J Phys Anthropol 2017; 1–14 wileyonlinelibrary.com/journal/ajpa V
C2017 Wiley Periodicals, Inc.
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1
Received: 16 August 2016
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Revised: 1 January 2017
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Accepted: 2 January 2017
DOI 10.1002/ajpa.23175
& Rheindt, 2016), and nocturnal mammals (Helgen, Leary, & Aplin,
2010; Munds, Nekaris, & Ford, 2013; Reeder, Helgen, Vodzak, Lunde,
& Ejotre, 2013), new taxa continue to be described in the absence of
molecular data. The delimitation of these taxa using molecular data
have repeatedly confirmed separations based on morphology and
vocalizations (Mittermeier et al., 2013; Nekaris & Bearder, 2011; Pozzi,
Disotell, & Masters, 2014; Pozzi et al., 2015; Wollscheid-Lengeling,
Boore, Brown, & Wägele, 2001).
The well-studied Order Primates is a case in point: most new pri-
mate species recognized in the 21st century are the result of the taxo-
nomic elevation of previously known subspecies to species (Groves,
2001; Macaca spp.: Kitchener & Groves, 2002; Aotus spp.: Defler &
Bueno, 2007; Nomascus spp.: Thinh, Mootnick, Thanh, Nadler, & Roos,
2010; Microcebus spp.: Hotaling et al., 2016). Taxa wholly new to sci-
ence, however, are also being described (e.g., Rungwecebus kipunji:
Davenport et al., 2006; Jones et al., 2005; Tarsius tumpara: Shekelle,
Groves, Merker, & Supriatna, 2008; Rhinopithecus strykeri: Geissmann
et al., 2010; Nycticebus kayan: Munds et al., 2013).
Both morphological and genetic evidence suggest that a far greater
number of cryptic species may yet be revealed within the galagos
(Family Galagidae, also known as bushbabies; Grubb et al., 2003;
Nekaris, 2013; Oates, 2011; Pimley, 2009; Pozzi et al., 2014, 2015).
The galagos of the African mainland consist of 18 named and described
species, although their taxonomy remains debated, with various
arrangements of described species and sub-species being proposed
(Butynski, Kingdon, & Kalina, 2013; Nekaris, 2013; Nekaris & Bearder,
2011; Masters & Couette, 2015). We here follow the taxonomy of
Nekaris (2013), which is largely identical to that of Butynski et al.
(2013) but differs from Groves (2001) in that it recognizes the genera
Galagoides and Sciurocheirus, which Groves subsumed under the genus
Galago. In addition, we recognize the recently proposed genus
Paragalago, for the eastern dwarf galagos, which includes the taxa Gd.
rondoensis,Gd. zanzibaricus, Gd. orinus, Gd.cocos and Gd. granti (Masters
et al., 2017).
Galagos are a monophyletic taxon originating in the Late Eocene
that comprises six distinct radiations (Pozzi, 2016; Pozzi et al., 2014,
2015). Dwarf galagos occur over much of Africa, with Galagoides thomasi
and Gd. demidovii (alsoreferredtoasGd. demidoff, Groves, 2001;
Jenkins, 1987; Masters & Couette, 2015; Olson, 1979) occurring as far
west as Senegal and Guinea Bissau, and Paragalago granti occurring as
far east as the shores of Mozambique, with some species and subspecies
being endemic to montane complexes (P. orinus)andoffshore islands
(P. zanzibaricus zanzibaricus and Gd. demidovii poensis) (Nekaris, 2013).
The nocturnal galagos fit the cryptic pattern in that they recognize
each other and communicate via vocal, chemical and subtle morpholog-
ical differences that may be cryptic to humans, rather than adopting
the colorful pelages and sexually dimorphic features of diurnal primates
(Masters, 1993; Pozzi et al., 2015). In the field, researchers have relied
particularly on vocalizations and behavior to distinguish otherwise mor-
phologically similar and difficult to distinguish species (Bearder &
Svoboda, 2013; Nash, Zimmermann, & Butynski, 2013; Zimmermann,
1990). In multiple classical studies it has been shown that it is possible
to differentiate between species by observing their locomotion, behav-
ior and habitats (Ambrose, 1999; Charles-Dominique & Bearder, 1979;
Crompton, Lieberman, & Oxnard, 1987; Harcourt & Nash, 1986;
Weisenseel, Chapman, & Chapman, 1993). All galagos produce adver-
tising calls that are used to maintain contact between dispersed individ-
uals, indicating spatial position and movement (Bearder, Honess, &
Ambrose, 1995). Galago species can be categorized into eight different
vocal groups: click callers (Euoticus spp.), croak callers (Sciurocheirus
spp.), repetitive callers (G. senegalensis,G. moholi,andG. matschiei),
trailing callers (Otolemur spp.), rolling callers (P. rondoensis and
P. zanzibaricus), scaling callers (P. orinus), incremental callers (P. cocos
and P. granti) and crescendo callers (Gd. thomasi and Gd. demidovii)
(Grubb et al., 2003). Advertising calls exhibit marked specific variations,
which make them particularly suitable for species discrimination (Bearder
et al., 1995; Masters, 1993). In addition, complex vocal repertoires are
often species-unique. For example, after being considered the same spe-
ciesforover50years,lessergalagosG. moholi and G. senegalensis were
eventually classified as separate species due to substantially different
vocal repertoires (Zimmermann, 1990; Zimmermann, Bearder, Doyle, &
Andersson, 1988). This separation of the G. senegalensis and G. moholi
wasalsosuggestedbasedondifferences in adult body mass and repro-
ductive parameters (Izard & Nash, 1988).
Other features used to distinguish galago species include pelage
characteristics, facial markings, reproductive anatomy and other mor-
phological attributes. Anderson (1999, 2001), and Anderson, Ambrose,
Bearder, Dixson, and Pullen (2000) used the cuticle scales of hairs and
the arrangement of friction pads on the hands and feet to help distin-
guish between G. senegalensis and G. moholi, and between greater gala-
gos Otolemur crassicaudatus and O. garnetti. Ambrose (2003, 2013)
described a new species of squirrel galago (Sciurocheirus makandensis)
based on facial markings, vocalization and pelage coloration. The east-
ern dwarf galagos (P. orinus, P. rondoensis, P. granti, P. cocos,and
P. zanzibaricus) can all be classified as distinct species on the basis of
correlated differences in vocalizations and penile morphology
(Anderson, 1999; Perkin, 2007; Masters et al., 2017). Although differ-
ences in skull morphology are more subtle in cryptic species, Masters
and Bragg (2000) found that O. crassicaudatus and O. garnettii could be
discriminated using ear and palate length, and Gd. demidovii and Gd.
thomasi using ear and skull length.
Here we report on a new species of dwarf galago from Angola
that has a unique combination of traits, and several features that are
diagnostically different from other galagos. In terms of pelage colora-
tion, skull shape and vocal behavior this species resembles other west-
ern dwarf galagos (Galagoides spp.), but their body size is like that of
lesser galagos (Galago spp.). Three galagid species have been reported
to occur in Angola, that is, O. crassicaudatus monteiri,G. moholi,andGd.
demidovii phasma, whereas the occurrence of a fourth species, Gd. tho-
masi in the country is based solely on museum specimens (Bersacola,
Svensson, & Bearder, 2015; Nekaris, 2013). Machado (1969) reported
Gd. demidovii to occur only in parts of the Lunda Norte Province, situ-
ated in the far north-east of the country, and in the north-western
Angolan provinces of Zaire and Uige.
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SVENSSON ET AL.
A Perkin and JC Masters examined the collections of the Field
Museum of Natural History in Chicago (FMNH) in 2007 and consid-
ered three specimens labelled as ‘Galago’collected in the escarpment
area of Angola to be distinct due to their large body size, and noted
that they possessed a Galagoides type skull rather than a Galago one.
Masters and Couette (2015) identified these skulls using multivariate
morphometrics as Gd. thomasi. Based on museum specimens, Nash,
Bearder, and Olson (1989) tentatively listed Gd. thomasi as present in
northern Angola, including the Angolan Escarpment (termed ‘Luanda
highlands’by Nash et al., 1989). Reviewing geographic variation of Gd.
thomasi, Kingdon (2015) was of the opinion that distinct populations,
possibly even a new subspecies or species, occurred on the Angolan
Escarpment and in the Katanga Province of the Democratic Republic of
Congo (DRC). In contrast, neither Groves (2001), based on studies of
museum specimens, nor Bersacola et al. (2015), based on field surveys,
found evidence of Gd. thomasi in Angola.
In 2005 vocal recordings of a dwarf galago were made by MSL
Mills along the central Angolan Escarpment and sent for identification
to the Nocturnal Primate Research Group (NPRG) at Oxford Brookes
University. These calls were compared with those from the NPRG’s
extensive sound library of all known galagos (Bearder, Honess, Bayes,
Anderson, & Ambrose, 1996). The vocalizations recorded from Angola
were crescendo calls, identifying them as having been emitted by a
Galagoides species, but different enough to lead to speculation that
they belong to a previously undescribed species. Following in situ sur-
veys and examination of museum specimens, in this paper we describe
the new species, compare it to other sympatric and allopatric taxa,
assess its conservation status, and outline an agenda for future work.
2
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MATERIALS AND METHODS
2.1
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Study area
Four biomes represent the land ecosystems in Angola, namely the
Zambezian biome (covering 85% of the country), Guinea-Congolese
biome (10.7%), the Karoo-Namib biome (2.6%), and the Afro-Upstream
biome (0.5%) (Kuedikuenda & Xavier, 2009). Within Angola these
biomes include 15 different ecoregions, including desert, savannah
woodlands, grasslands, dry forests, montane forest-grassland mosaics,
forest-savannah mosaic, miombo woodlands and mangroves (Olson
et al., 2001). The Angolan Escarpment is located in the western part of
the country, and stretches for 1000 km from north to south, forming
part of the Great Escarpment of southern Africa (hereafter “Great
Escarpment”) (Clark, Barker, & Mucina, 2011). Several ecological
regions meet at the Angolan Escarpment, making it a complex area
where topographical features have led to significant levels of endem-
ism and floristic diversity (Clark et al., 2011; Figueiredo, 2010; Hall,
1960; Romeiras, Figueira, Duarte, Beja, & Darbyshire, 2014). Angola is
believed to support more vertebrate species endemic to the Great
Escarpment than any other country, except South Africa (Clark et al.,
2011). Between the early 1970s and 2002, surveys in Angola were lim-
ited due to the protracted civil war, and subsequently the expense and
logistical difficulties of operating in the country prevented much biolog-
ical exploration. Now that systematic biological surveys are resumed,
researchers expect that further endemic species will be discovered in
this region (Clark et al., 2011; Vetter, 2003). We visited four study sites
in north-western Angola: Kumbira forest (submontane/dry Congo basin
forest); Bimbe (dry thicket islands in tall grass savannah with stream
beds); Northern Scarp Forest (moist forest) and Calandula (miombo
woodland/gallery forest).
2.2
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Data acquisition
MS Svensson, E Bersacola, MSL Mills and SK Bearder conducted noc-
turnal surveys in Angola between 5 and 19 September 2013. The sur-
veys lasted for 39 h, walking on small roads and established paths and
recording the habitat use and height in the canopy for each animal
observed (for a more detailed description of the survey method see
Bersacola et al., 2015). Nocturnal animals were photographed with a
Canon EOS 600D camera, with Canon 70-200 mm EF Zoom lens and
Canon Speedlight 430EX II flash.
2.3
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Vocalizations
At each survey site we recorded calls of galagos before sunrise (04:30–
05:30) and after sunset (18:00–22:00). We remained stationary at
recording sites throughout recording sessions. We made recordings
using a Fostex Field Recorder equipped with a Sennheiser K6-ME67
directional microphone. We digitized calls using Avisoft SASLab Pro
software (R. Specht, Berlin; version 5.2). We compared our results with
vocalizations of the Galagoides taxa (Gd. demidovii and Gd. thomasi), as
these are the only other crescendo callers, and with G. moholi as the
only other small galago found in Angola (a repetitive caller, Bearder
et al., 1995). Recordings were converted into spectrograms with a fre-
quency resolution of 48 kHz (FFT length 512; 50% overlap; Hamming
window). We focused on fundamental frequency (first harmonic, meas-
ured in kHz), crescendo unit length (the basic element of the crescendo
phrase, measured in s), twitter unit length (the basic element of the
twitter phrase, measured in s) and formant (dominant frequency, meas-
ured in kHz). We used a one-way ANOVA to test for differences
among the four species followed by Tukey’sHSDpost hoc test for pair-
wise differences between species.
2.4
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Morphology
During visits to the FMNH in Chicago in 2011, A Perkin and JC Mas-
ters examined the skulls and skins of three distinct types of small gal-
ago collected in Angola: G. moholi, Gd. demidovii and specimens whose
taxonomic identity remained inconclusive but were tentatively named
Gd. thomasi. Knowing that Angolan specimens existed at FMNH in
2015 RA Munds revisited the anomalous specimens (FMNH 81755,
81756, and 81758).
In order to assess the taxonomic status of the three specimens
from Angola we ran a multivariate analysis based on a set of twelve lin-
ear measurements of skulls and teeth. JC Masters measured the fron-
tal, suppraoccipital, snout, premaxilla, toothcomb, and skull lengths, the
cranial height, the first lower molar, mastoid and palate widths, and the
SVENSSON ET AL.
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3
widths of the interorbital and temporal constrictions (for description
and schematic illustration see Masters & Couette, 2015; Table 1 and
Figure 1). The dataset was composed of 50 specimens of Gd. demidovii,
50 specimens of Gd. thomasi and 50 specimens of G. moholi,plusthe
three specimens from Angola. JC Masters collected measurements in
several institutions around the world [American Museum of Natural
TABLE 1 Comparison of characteristics of Galagoides kumbirensis sp. nov. and similar species with which it could be confused
Variables
Gd. kumbirensis
sp. nov. Gd. demidovii Gd. thomasi G. moholi
Morphology
a
Head-body
length (mm)
$# 159 (149–171)
n53
$# 129 (73–155)
n5200
$# 146 (123–166)
n547
$# 150 (88-205)
n5826
Tail (mm) $# 195 (179–208)
n53
$# 179 (110–215)
5199
$# 195 (150–223)
n546
$# 225 (200-258)
n582
Greatest length
of skull (mm)
$# 40 (40–41) n53$# 37 (32–41)
n5100
$# 38 (35–42)
n566
$# 39 (36-42)
n5150
Ear height (mm) $# 31 (29–33) n53$# 24 (14–35)
n5180
$# 29 (23–33)
n546
$# 37 (31-41)
n585
Hind foot (mm) $# 52 (50–53) n53$# 46 (35–60)
n5191
$# 52 (39–58)
n546
$# 57 (51-62)
n591
Muzzle Upturned muzzle Upturned muzzle Long pointed muzzle Short slanted muzzle
Tail Dark long-haired tail Long nonbushy Nonbushy, same
color as dorsum
Long, dark, thin
Facial markings Circumocular
markings
Dark, round Dark, round Indistinct Dark, diamond-
shaped
Muzzle Dark, merges into
eye rings
Dark, merges into
eye rings
Dark, disconnected
from eye rings
Light
Nose tip Dark Light Dark Dark
Face shade Dark Dark Medium Medium
Light nose stripe Short, broad Short Long, stripe broad-
ens on forehead
Long, broad
Inside ear color Light Light Light Graded
Vocalization Advertisement calls Crescendo-twitter Crescendo Multiple crescendo Bark
Crescendo unit
length (s)
0.269 60.044,
n514
0.086 60.020,
n532
0.095 60.033,
n510
N/A
Twitter unit length (s) 0.068 60.015,
n514
N/A N/A N/A
Fundamental
frequency (kHz)
1039 6311,
n514
889 6219,
n532
2188 61824,
n510
691 674,
n55
Formant (kHz) 3721 61713, n514 1629 61405, n532 5141 61818, n510 1009 6199, n55
Pitch at end of
crescendo
Decreasing Decreasing Increasing N/A
No of calls in
each crescendo
sequence
1 1 Multiple N/A
Ecology Strata use Mid-high Low Mid-high All
Known sympatry
with Gd. kumbiren-
sis sp. nov.
Yes No No
Habitat use Moist forest, primary
and secondary
Rainforest,
evergreen,
deciduous, gallery,
riparian strips,
edge vegetation,
tree falls
Rainforest, ever-
green, deciduous,
gallery
Acacia woodland-
savanna, semi-arid
habitats, riparian
strips
a
All measurements taken from Butynski, Kingdon & Kalina (2013) except the ones for Galagoides kumbirensis sp. nov.
4
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SVENSSON ET AL.
History, New York, USA (AMNH); Museum of Comparative Zoology,
Cambridge, USA (MCZ); Field Museum of Natural History, Chicago,
USA (FMNH); Mus
eum National d’Histoire Naturelle, Paris, France
(MNHN); Natural History Museum, London, UK (NHM); National
Museum of Kenya, Nairobi, Kenya (NMK); Royal Museum of Central
Africa, Tervuren, Belgium (RMCA) and National Museum of Zimbabwe,
Bulawayo, Zimbabwe (NMZ)] and measured specimens using digital
calipers according to the procedure described in Masters and Couette
(2015). JC Masters measured 40 specimens twice and estimated the
percentage of intraobserver measurement error using the method pro-
posed by Bailey and Byrnes (1990). Error represented 2.4% of total
variation in our sample and can be considered as insignificant.
The morphometric procedures were conducted by S Couette, who
applied a size correction to the raw data using the Burnaby (1966) pro-
cedure that proposes to compute an isometric vector from all linear
measurements and back project these measurements in a space
orthogonal to this vector. Shape and size were analyzed separately.
The raw data were logged prior to the size correction. The geometric
mean (GM), considered as a proxy of the overall size, is the matrix
product without units of the isometric vector and the raw data. All the
statistical analyses were conducted using R 3.0.2. software (R Core
Team, 2013) and the package MASS (Venables & Ripley, 2002). No
body weights were available for specimens FMNH 81755, 81756, and
81758.
3
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RESULTS
During nocturnal surveys in September 2013 36 live individuals of the
new species of dwarf galago were observed in north-western Angola,
that is, on 17 occasions in Kumbira, one in Bimbe and on 18 occasions
in the Northern Scarp Forest (Figure 1). Where possible we took photo-
graphs. All observations were made within 3–10 m of the animals using
red light, so that we were able to observe and identify the species
clearly without the animals being blinded or disturbed by our lights
(Svensson & Bearder, 2013). We recorded 37 vocalizations of the new
species at all three sites: Kumbira (n515), Bimbe (n53) and Northern
Scarp Forest (n519), 14 of which were crescendo-twitter calls of high
enough quality to be analyzed (see below). The location where, in 2005,
MSL Mills had previously heard, and recorded, the calls of the species is
approximately 4 km north of Kumbira Forest (118040S, 148150E).
The facial morphology and vocal behavior identified the new spe-
cies as a western dwarf galago, Galagoides sp., but in terms of general
appearance, size and mass it was more similar to a lesser galago, Galago
spp. The new species was observed to use mid to high strata, with a
median height of 12 m (n536) and ranging between 2 and 32 m (see
more details in Bersacola et al., 2015). It was observed leaping and
climbing on branches of all sizes, but it was never observed on the
ground. During the surveys we also observed and recorded calls of Gd.
demidovii,O. crassicaudatus,andG. moholi. We here describe the new
species: the Angolan dwarf galago (Galagoides kumbirensis sp. nov.).
Galagoides kumbirensis Svensson, Bersacola, Mills, Munds,
Nijman, Perkin, Masters, Couette, Nekaris, Bearder sp. nov. ZooBank
LSID urn:lsid:zoobank.org:pub:5A044D3B-06D9-4B6F-9366-27EAF470
F374 (Article published 2017).
3.1
|
Syntypes
FMNH 81755 adult female, skin and skull; FMNH 81756, adult male,
skin, and skull (Figure 2A,B) and FMNH 81758 adult female, skin and
skull. Collected by G. H. Heinrich in 1954 in Cuanza Norte, Cameba-
tela, 30 km W, Canzele, Quai Sai River (this appears to be a typographic
error and most likely refers to the Cuale do Sul River), Angola (088190S,
158110E) 800 m above sea level (asl). Housed at FMNH.
3.2
|
Paratype
Adult in photograph (Figure 2C). Photograph taken in type locality in
Kumbira Forest, Angola (118080S, 148170E) 900 m asl. The Kumbira
population is designated as the source population for physical speci-
mens in support of the FMNH syntypes.
3.3
|
Type locality
Kumbira Forest (around 118080S, 148170E), within the Angolan Escarp-
ment of north-western Angola.
3.4
|
Diagnosis
Galagoides kumbirensis sp. nov. is allied to the other West African Gala-
goides by its distinctive crescendo call, unlike the East African species
of Paragalago that do not give a crescendo. Galagoides kumbirensis sp.
nov. is easily distinguished from other western Galagoides by the
unique pattern of units within the call, the ‘crescendo-twitter’:a
FIGURE 1 Extent of occurrence (EOO) of Gd. kumbiraensis sp.
nov. Key: 1study sites where the species was observed in 2013; 䉬
location where museum specimen were collected in 1954
SVENSSON ET AL.
|
5
relatively short sequence (1–2 s) of longer notes (2–3s
21
)becoming
louder and changing to a variable series (0.3–1.3 s) of staccato notes
(10 s
21
) that descend in pitch (twitter). The crescendo-twitter is only
ever given once per bout (Figure 3). The new species is similar in size
and markings to G. moholi (Figure 4; Table 1) but its skull shape is char-
acterized by a slender, longer muzzle, making it more similar to that of
Galagoides (Figure 5). In a principal components analysis based on the
craniodental morphology of the four small-bodied galagid genera (Gal-
ago, Galagoides, Paragalago,andSciurocheirus), the major variable con-
tributing to generic separation was premaxillary length, that is, the
FIGURE 2 (A, B) Skin and skull of one of the syntypes of Gd. kumbirensis sp. nov. (FMHN 81756); (C) paratype (in situ Kumbira Forest)
6
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SVENSSON ET AL.
length of the premaxillary tube that gives Galagoides its long, tapering
upper jaw (Masters et al., 2017). The snout of Galago species is short,
with a small relictual nub on the median line between the two premax-
illae, which suggests that the extended dwarf galago condition is ances-
tral (G
enin et al., 2016). The premaxillae of Paragalago spp. are
intermediate in length between those seen in Galago and Galagoides.
The face of the new species is relatively gray with a short and broad
white nose stripe.
3.5
|
Description
We describe G. kumbirensis sp. nov. based on both the syntypes and
the paratype. A small gray-brown galago with a darker, long-haired tail.
Degree of sexual dimorphism is unknown but likely to be low, as in
most small-bodied galago taxa. Muzzle slightly up-turned, pink below
and dark above, merging into dark eye-rings with a conspicuous white
nose stripe between the eyes. The remainder of the face gray, suffused
with brown, and set offfrom white cheeks, chin, and neck. Inner ears
white towards the base and yellowish towards margins. Ears gray
above with two light spots where the ears join the crown. Crown, dor-
sum, forelimbs, thighs, and flanks gray with a brown wash. Ventrum,
surface of forelimbs and hindlimbs creamy yellow. Yellow strongest
where the light ventrum merges into the darker dorsum. Tail darker
towards the tip and slightly longer than the body. Tail held curled when
at rest. Head-body measures range 170–200 mm (n53), tail 170–
240 mm (n53), hind foot 50–53 mm (n53), ear 29–33 mm (n53)
(sexes combined for all measurements; Table 1).
FIGURE 3 Vocalization spectrograms of advertisement calls. Gd. kumbirensis sp. nov—crescendo-twitter; Gd. demidovii—crescendo; Gd. tho-
masi—multiple crescendo; G. moholi—bark. Vocalization recordings of Gd. kumbirensis sp. nov are available at www.wildsolutions.nl.
SVENSSON ET AL.
|
7
3.6
|
Vocalization
The distinguishing vocal feature of Gd. kumbirensis sp. nov. is the twitter
sequence following the crescendo call (Table 1). In the recorded calls of
Gd. kumbirensis sp. nov. that were of suitable quality for spectrographic
analysis (n514), the number of crescendo units in a call ranged between
2 and 17 and twitter units between 4 and 10. The mean fundamental fre-
quency of the crescendo-twitter was 1039 6311 kHz (n514) and the
mean formant 3721 61713 kHz (n514); mean crescendo unit length
0.269 60.044 s (n514)andmeantwitterunitlength0.06860.015 s
(n514) (Figure 3). The four species showed clear differences in the values
obtained for these four call parameters (ANOVA, all F
3,57
>8.204, all
p<.001) (Table 1). Post hoc tests show that Gd. kumbirensis sp.nov.differs
in its fundamental frequency from Gd. thomasi (Tukey’sHSD,meandiffer-
ence 21148, p5.003), and in its formant from Gd. demidovii (mean differ-
ence 22092, p<.001), and from G. moholi (mean difference 22711,
p<.006), but not from Gd. thomasi (mean difference 21420, p<.115).
3.7
|
Habitat
Observed in moist, tall forest, primary, and secondary (Kumbira and
Northern Scarp Forest) and semiarid baobab savannah-woodland in
FIGURE 4 Comparison of skins and skulls: Gd. kumbirensis sp. nov., Gd. demidovii,Gd. thomasi and G. moholi
8
|
SVENSSON ET AL.
areas where tree-lined water courses allowed access (Bimbe; Table 1).
Encounter rate was higher in moist forest (2.60–2.67 individuals/km)
compared to savannah-woodland (0.17 individuals/km, see Bersacola
et al., 2015 for more information and statistical analyses).
The species has been observed at altitudes of between 285 and
910 m asl, that is, 860–910 m asl in Kumbira, 285 m asl in Bimbe and
465–745 m asl in Northern Scarp Forest. The 2005 vocalization
recordings were made at 900 m asl, and the syntypes was collected at
800 m asl. Forest in the northern Angolan Escarpment descends down
to approximately 250 m and up to 1,200 m asl and Gd. kumbirensis sp.
nov. was observed over most of this range.
3.8
|
Distribution and conservation status
Currently known only from four sites (Figure 1). Based on the habitat
types in which we observed Gd. kumbirensis sp. nov., and its altitudinal
distribution, and taking into account geographical barriers, including
the steep escarpment, three scenarios can be envisaged. The first is a
conservative one, assuming the species is confined to the central and
northern portion of the Angolan Escarpment, thus including the four
known locations, in which its extent of occurrence (EOO, IUCN, 2014)
is just under 20,000 km
2
(Figure 1). Using a more liberal estimate, its
range may extend in the north up to the Congo River (including small
parts of the DRC), with its north-west range restricted by the relatively
steep ridge west of Kinshasa or by the Kasai River, increasing its area
to 112,000 or 405,000 km
2
,respectively.
While the exact distribution range of Gd. kumbirensis sp.nov.is
not known, some inferences as to its conservation status can be made.
While still largely forested, its area of occurrence is subject to severe
pressure from commercial timber logging and deforestation for farming
and charcoal production (Bersacola et al., 2015; C
aceres, Melo, Barlow,
& Mills, 2016; Hansen et al., 2013). None of the locations where we
observed this species falls within a protected area. In the absence of
data from the more northern and north-eastern areas, and applying a
cautionary principle, we recommend that Gd. kumbirensis sp. nov.
should be listed as Vulnerable on the IUCN Red List on the basis of cri-
teria B1ab(iii); that is, an estimated EOO of less than 20,000 km
2
,
known from fewer than 10 locations, and a continued decline in the
area, extent and/or habitat quality (IUCN, 2014) When more informa-
tion on the species’distribution and its threats becomes available this
assessment should be re-evaluated.
All primates are listed in Appendix II of the Convention on Interna-
tional Trade in Endangered Species of Wild Fauna and Flora (CITES),
apart from those listed in Appendix 1. Angola joined the Convention in
October 2013, which came into force in December 2013. In the
absence of any data on international trade in the species (Svensson,
Ingram, Nekaris, & Nijman, 2015) we suggest adopting the default posi-
tion and including the species in Appendix II, thus regulating but not
banning any future international trade.
3.9
|
Etymology
The species was first observed in situ in Kumbira Forest, an area under
great pressure from commercial logging (Bersacola et al., 2015; C
aceres
et al., 2016). Kumbira is considered a hotspot for many endemic spe-
cies in Angola (C
aceres et al., 2015) and by using this name we aim to
draw attention to the area.
3.10
|
Suggested common name
Angolan dwarf galago (English), galago angolano (Portuguese).
3.11
|
Similar species: habitat use, vocalizations,
pelage, and facial features
Galagoides demidovii. Sympatric with Gd. kumbirensis sp.nov.inatleast
two sites (Bimbe and Northern Scarp Forest). Prefers undergrowth
<5 m, often in secondary growth and forest edge. Usually observed
running along fine branches (<1 cm diameter). Crescendo with a long
series (>4 s) of rapid notes (10 s
21
) building in pitch and intensity and
ending in longer, slower notes (6 s
21
) that descend in pitch (Figure 3).
Usually given only once or twice per bout. Other calls in the repertoire
include ‘chips’(alarm call) and ‘explosive buzz’(contact avoidance)
(Ambrose, 1999). Facial markings are similar to Gd. kumbirensis sp. nov.
FIGURE 5 Top: Between group principal component analysis
(BGPCA) on the twelve size corrected variables of four species of
galago. Principal component analysis was conducted on the mean
of each species and specimens were projected in this space.
Distances between specimens relate to cranial shape differences.
Bottom: Comparison of galago skulls based on average greatest
length of skull, A) Gd. kumbirensis sp. nov. (black line) versus G.
moholi (gray), B) Gd. kumbirensis sp. no. (black line) versus Gd.
demidovii (gray)
SVENSSON ET AL.
|
9
(Table 1), although Gd. demidovii is considerably smaller in size. Dorsum
and tail browner, tail relatively thin and short (Figure 4B). Nose narrow
and upturned, ears relatively shorter and eye sockets less broad
(Ambrose & Butynski, 2013; Bearder et al., 1995; Nekaris, 2013).
Galagoides thomasi. Not known to be sympatric with Gd. kumbiren-
sis sp. nov. Occupies similar height in the canopy as Gd. kumbirensis sp.
nov. (Table 1), usually >5 m on branches of any size. Crescendo con-
sists of a relatively short series (2–3 s) of brief notes (6 s
21
), gradually
increasing in speed of repetition (10 s
21
), pitch and volume until the
end of the call which is high pitched (almost inaudible, Figure 3). Each
individual usually repeats these calls in a sequence, with the first call
being the loudest and subsequent calls becoming quieter (multiple cre-
scendo). Other calls in the repertoire include ‘trills’(assembly call) and
‘chips’(alarm call) which are often interspersed with ‘grunts’and
‘buzzes’(Ambrose, 1999). Somewhat smaller in size, dorsal pelage
darker and browner with less contrast between the dorsum and ven-
trum (Figure 4C). Tail browner, shorter, and less bushy. Circumocular
markings indistinct and long light nose stripe broadens on forehead
(Ambrose and Butynski, 2013; Bearder et al., 1995; Nekaris, 2013).
Galago moholi. Not known to be sympatric with Gd. kumbirensis sp.
nov. but also present in Angola. Prefers drier woodland-savannah and
edge vegetation. Observed using all strata on branches of all sizes. Like
other members of the genus Galago, the advertising call is a repetitive
call: a series of single, double, or triple barks repeated many times (Fig-
ure 3). Never heard to give a crescendo. Similar in body size (Figure
4D) but longer hind limbs suited to long leaps and hops along the
ground. Dorsum without a brown wash and tail similar in size and color
but less bushy, particularly towards the base. Circumocular markings
black and diamond-shaped, inner ears darker and muzzle shorter,
broader and lighter in color (Bearder et al., 1995; G
enin et al., 2016;
Nekaris, 2013; Pullen & Bearder, 2013).
3.12
|
Comparison among Gd. kumbirensis sp. nov., Gd.
demidovii,Gd. thomasi and G. moholi
3.12.1
|
Size of skull
Figure 6 presents the boxplot of the log (GM) by species. The three
specimens from Angola show a mean size of 7.79 with a standard devi-
ation of 0.02. Their mean value of log (GM) plotted in the higher part
of the size range of G. moholi (mean 57.68, SD 50.13), greater than
the size of Gd. demidovii (mean57.55, SD 50.14) and Gd. thomasi
(mean 57.59, SD 50.17). We compared skull size across the four spe-
cies using an ANOVA, and the difference was significant (F58.6,
n5153, p<0.001). Tukey HSD post hoc statistics allowed the distinc-
tion of two size groups: a first group composed of Gd. demidovii and
Gd. thomasi, and a second group composed of G. moholi and the Gd.
kumbirensis sp. nov. Therefore, size analysis indicated a similarity in size
between the Gd. kumbirensis sp. nov. and G. moholi.
3.12.2
|
Shape of skull
We applied a between group principle component analysis (BGPCA) on
the logged size-corrected measurements of all 153 specimens. This
method consists of computing a PCA on the mean values for each
group, defining the BGPCA space and projecting the individuals in this
space by applying the BGPCA parameters (i.e., the variable loadings) to
the shape variables of each specimen (Mitteroecker & Bookstein,
2011). BGPCA extracted two components that express 91% of the
total variation, with PC1 accounting for 88.6% and PC2 accounting for
3.3% of the variance (Figure 5). Group variation along PC1 describes
essentially the variation in shape of the premaxilla, with longer
FIGURE 6 Boxplot of the logged geometric mean by species
illustrating the differences in cranial size. ANOVA test and post hoc
Tukey HSD were conducted highlighting significant size differences
(***p<0.001) for nonsignificant size variation (n.s., p>0.05)
between species
TABLE 2 Loadings of the cranial variables on the first two axes of
the between group principle component analysis
Variables PC1 PC2
Supraoccipital length 0.210 0.039
Cranial height 0.090 20.050
Frontal length 0.122 0.533
Interorbital constriction 0.012 20.392
Cheek teeth width 20.010 20.346
Palate width 0.124 20.346
Total skull length 0.011 20.296
Snout length 20.102 20.211
Mastoid width 0.096 20.023
Temporal constriction 0.181 20.102
Premaxilla 20.913 0.101
Toothcomb length 0.179 0.428
10
|
SVENSSON ET AL.
premaxillae having negative scores and shorter ones having positives
scores along the PC (Table 2). Galagoides demidovii and Gd. thomasi
grouped together on the negative end of PC1, whereas G. moholi speci-
mens were separated positively from the other on PC1. All three Ango-
lan specimens were grouped together and very close to the group
composed of Gd. demidovii and Gd. thomasi.TheGalagoides spp. largely
overlapped so that it was not possible to attribute Gd. kumbirensis sp.
nov. to one or the other species based on shape analysis. It is clear
that, in terms of shape, the Angolan specimens group with the genus
Galagoides rather than Galago. In the BGPCA performed by MasterS
et al. (2017), the new genus Paragalago fell in an intermediate position
between Galago and Galagoides.
We tested the difference in shape variables between groups using
a MANOVA, and the results indicated a significant difference in shape
between genera (F551.1, Pillai’strace51.03, p<0.001). The differ-
ence was in accordance with the PCA results. In order to allocate the
Angolan specimens to one or another genus based on the shape analy-
sis, we computed a linear Discriminant Analysis, grouping by genus.
We used all the specimens for this analysis except the Angolan ones.
Two discriminant axes were significant, perfectly separating the genus
Galago from the two Galagoides spp. After cross validation, all speci-
mens of G. moholi were correctly classified by the analysis, whereas a
third of the Gd. demidovii specimens were classified as Gd. thomasi and
vice versa. After integrating Gd. kumbirensis sp. nov. into the analysis,
all three specimens were allocated to Gd. thomasi with posterior classi-
fication of 93.7, 76.0, and 78.7%. The cranial shape of the Angolan
specimens is highly similar to that of Gd. thomasi.
4
|
DISCUSSION
In this paper we have demonstrated significant differences in morphol-
ogy and size as well as advertising call structures between Gd. kumbir-
ensis sp. nov. and closely related taxa (Table 1). We ascribe Gd.
kumbirensis sp. nov. to the genus Galagoides on the basis of its cre-
scendo call and similar skull shape characterized by a slender, upturned,
muzzle. Galagoides skulls can be differentiated from those of Paragalago
by fact that the premaxillae are noticeably more extended, and the
skulls are more globular in shape; the skulls of Paragalago spp. tend to
be more ovoid (Masters et al., 2017). The recognition of Gd. kumbirensis
sp. nov. as a species distinct from other galagos is valid when following
a Phylogenetic Species Concept, that is, it represents a phylogeny clus-
ter, diagnosably distinct from other such clusters, within which there is
a parental pattern of ancestry and descent (Cracraft, 1989; Groves,
2001), but also under the Recognition Concept (Paterson, 1985) on the
basis of its unique specificmaterecognitioncall.
The use of habitat by Gd. kumbirensis sp. nov. appears to be most
similar to Gd. thomasi (running, climbing and leaping on supports of all
sizes mostly above 5 m) but Gd. kumbirensis sp. nov. can be distin-
guished from this species by its larger size, different coloration and dis-
tinctive pattern of calling. Galagoides demidovii was found sympatrically
with the new species in two out of three sites, using lower vegetation
strata where it was mainly limited to small branches (Bersacola et al.,
2015, in which Gd. kumbirensis sp. nov. was referred to as Galagoides
sp. nov. 4). Again, there are distinctive differences in body size, pelage
color and vocalizations. The new species was most similar in size to G.
moholi, which appears widespread in Angola but in much drier habitats
(Bersacola et al., 2015). Galago moholi and Gd. kumbirensis sp. nov. are
not sympatric, and differ markedly in behavior, morphology and ecol-
ogy. In addition, while the relative abundance of sympatric Gd. demido-
vii appeared to be influenced by structural characteristics of the
habitat, Bersacola et al. (2015) could not find any evidence that this
was true for Gd. kumbirensis sp. nov. However, similar to Gd. demidovii,
Gd. kumbirensis sp. nov. appeared to occur more often in humid forests,
rather than the savannah-woodland environments where most Galago
spp. are typically found.
Many questions remain to be answered about the distribution,
behavior, life history traits and ecology of the new species. Prior to this
study, it was provisionally identified as Gd. thomasi, which lives sympa-
trically with Gd. demidovii in most parts of its range, including the adja-
cent Congo basin (Ambrose & Butynski, 2013). At present we have no
evidence of Gd. thomasi in Angola, where it appears to be replaced by
the ecologically similar Gd. kumbirensis sp. nov., that also lives sympatri-
cally with Gd. demidovii.
The structure of the crescendo call of Gd. kumbirensis sp.nov.is
more similar to that of Gd. demidovii (ending in staccato notes that
descend in pitch, Figure 3) than it is to that of Gd. thomasi,possibly
indicating a closer evolutionary relationship and a more recent common
ancestor between Gd. kumbirensis sp.nov.andGd. demidovii than
between Gd. kumbirensis sp. nov. and Gd. thomasi. If this is the case, it
is possible that the new species arose when an ancestor of Gd. demido-
vii became isolated along the Angolan Escarpment, and that it later
spread north to overlap with Gd. demidovii and replace Gd. thomasi.
Alternatively Gd. kumbirensis sp. nov. evolved in isolation and Gd. demi-
dovii later expanded southwards onto the Angolan Escarpment.
As noted in the introduction, the escarpment area of Angola is well
known as an important biodiversity hotspot, with many endemic and
rare species, often strikingly different from species elsewhere (Clark
et al., 2011; Hall, 1960; Figueiredo, 2010). These species are thought
to have speciated and adapted long before the Quaternary (Morley &
Kingdon, 2013). This process was possible as the Angolan Escarpment
climate, due to the Benguela Current meeting tropical waters at the
Angolan shores, was less affected by climatic changes than other more
inland regions. As such the Angolan Escarpment remained constantly
humid, allowing birds and mammals to develop in isolation during both
wet and dry periods (Hall, 1960; Fjeldså & Lovett, 1997).
Angola ratified the Convention on Biological Diversity (CBD) in
1998 indicating its commitment to biodiversity conservation in the
country. Through its National Biodiversity Strategy and Action Plan
(Anonymous, 2007) it is committed to incorporating measures for the
conservation and sustainable use of biological diversity into develop-
ment policies and programs. Strategic Areas C (biodiversity manage-
ment of protected areas), F (institutional strengthening) and G
(legislation and implementation), highlighted in the Action Plan, in par-
ticular, can bring direct and tangible conservation benefits to Gd.
SVENSSON ET AL.
|
11
kumbirensis sp. nov. if implemented. Both the organization of effective
management in existing protected areas and an increase in the pro-
tected area network would constitute important strategic interven-
tions. Further, it is recognized that institutional capacity in Angola is
often weak in terms of human and financial resources and the imple-
mentation of any biodiversity conservation policy or measure crucially
depend, on building the capacity of individuals and institutions. Finally,
a review and, if needed, urgent correction, of existing legislation is
required to ensure environmental agreements, including the CBD and
CITES are followed as intended (Anonymous, 2007). The rate of log-
ging in Angola is one of the fastest known in the world (Hansen et al.,
2013), with the Angolan Escarpment being a case in point (C
aceres
et al., 2016) which underlines the urgent need for further research to
set priorities for future conservation, and the need to designate more
protected areas.
Although birds are relatively well studied in the Angolan Escarp-
ment (C
aceres et al., 2015; Ryan et al., 2004), there is a dearth of
knowledge when it comes to mammal species. Other endemic primates
such as Miopithecus talapoin and Cercopithecus mitis mitis are known to
be present (Bersacola, Svensson, Bearder, Mills, & Nijman, 2014), but
little is known about their distribution or threats. Recent political and
economic developments within Angola have created opportunities to
conduct further research into the ecology and status of Gd. kumbirensis
sp. nov. and other endemic mammals. This research will enable the col-
lection of additional data (genetic, morphological, behavioral, etc.) to be
used in a comprehensive phylogenetic analysis to elucidate the evolu-
tionary relationships between Gd. kumbirensis sp. nov. and other Gala-
goides species, and, possibly, estimating a date for the separation
between Gd. kumbirensis sp. nov. and its sister species.
ACKNOWLEDGMENTS
Special thanks go to CP Groves and JF Oates who provided advice
throughout this project. We also thank American Museum of Natural
History, New York, USA; Museum of Comparative Zoology,
Cambridge, USA; Field Museum of Natural History, Chicago, USA;
Mus
eum National d’Histoire Naturelle, Paris, France; Natural History
Museum, London, UK; National Museum of Kenya, Nairobi, Kenya;
Royal Museum of Central Africa, Tervuren, Belgium and National
History Museum of Zimbabwe, Bulawayo, Zimbabwe, for allowing us
to study their collections and to FMNH for allowing us to publish
the pictures of the type specimens. Our thanks also go to MH
Ahsan for helping us gather information from FMNH and to C
McMahon for her hospitality whilst in Angola. We thank T Baron for
his assistance with Angolan visas. We are grateful for support from
the Fredrika Bremer F€
orbundet and the Iris Jonz
en-Sandbloms &
Greta Jonz
ens Stiftelse. We thank two anonymous reviewers for
constructive comments and suggestions for improvement. This pro-
ject was conceived by MS Svensson, E Bersacola, MSL Mills & SK
Bearder collecting the data in the field, A Perkin, RA Munds & JC
Masters collected the data in museum collections. V Nijman, S Cou-
ette & KAI Nekaris analyzed the data and MS Svensson, E Bersacola,
MSL Mills, JC Masters, A Perkin, KAI Nekaris, V Nijman & SK
Bearder wrote the article. We have no conflict of interest to report.
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How to cite this article: Svensson MS, Bersacola E, Mills MSL,
et al. A giant among dwarfs: a new species of galago (Primates:
Galagidae) from Angola. Am J Phys Anthropol. 2017;00:1–14.
doi:10.1002/ajpa.23175.
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