kay van damme & hilde eggermont 2011
TRANSCRIPT
CLADOCERA AS INDICATORS
The Afromontane Cladocera (Crustacea: Branchiopoda)of the Rwenzori (Uganda–D. R. Congo): taxonomy, ecologyand biogeography
Kay Van Damme • Hilde Eggermont
Received: 27 April 2011 / Accepted: 11 September 2011 / Published online: 11 October 2011
� Springer Science+Business Media B.V. 2011
Abstract The timely characterization of high-alti-
tude freshwater habitats allows an assessment of the
diversity of its biota and provides the basis for
monitoring community change. In this study, we
investigate the Cladocera fauna of 29 water bodies
(pools, freshwater lakes, and surrounding swamps
sampled at various occasions between 2005 and 2009)
in the Rwenzori Mountains (Uganda, D. R. Congo),
which are part of the East African Sky Island
Complex. All sites except one are located above
3700 m altitude. We include notes on the morphology,
taxonomy, distribution, and ecology of each recorded
taxon and describe a new species of the Alona rustica-
group (Alona sphagnophila n.sp.; Chydoridae). We
found 11 species of which seven are restricted to Lake
Mahoma, the lowest lake in our study area (2990 m)
(Alona affinis barbata, A. intermedia, Alonella exisa,
Alonella nana, Daphnia cf. obtusa, Pleuroxus adun-
cus) and/or Lake Bujuku (Daphnia cf. curvirostris,
P. aduncus) (3900 m). Two taxa (Ilyocryptus cf.
gouldeni, A. sphagnophila n.sp.) are restricted to
Carex/Sphagnum bogs surrounding lakes in the afro-
alpine zone. Pigmented populations of Chydorus cf.
sphaericus occur in all the sites. It is the only
cladoceran species surviving the extreme alpine and
nival conditions in the Rwenzori. The species is joined
by A. guttata at locations at lower altitudes (ca.
3000–4000 m), present in about half of the sites. The
Rwenzori Cladocera fauna is characterized by a strong
extratropical temperate component and a low level of
speciation/endemism. Harboring an impoverished
boreal cladoceran community, Lake Mahoma is given
closer attention. At 2990 m, the lake is a cold-
temperate aquatic island in the tropics and may
function as a stepping stone for Palaearctic taxa. We
introduce a new term for high-altitude, cold-water
habitats in the tropics, which act as climatic islands for
extratropical freshwater faunas, Loffler Islands, in
honor of Dr Heinz Loffler. In comparison to surveys in
1961, we list five new records in Lake Mahoma, which
could indicate cladoceran community changes over
the past few decades at ca. 3000 m in the Rwenzori.
Since the species distributions correlate to temperature
and catchment properties of the lakes, the Rwenzori
cladoceran fauna can be expected as sensitive indica-
tors for local changes.
Electronic supplementary material The online version ofthis article (doi:10.1007/s10750-011-0892-0) containssupplementary material, which is available to authorized users.
Guest editors: H. Eggermont & K. Martens / Cladocera as
indicators of environmental change
K. Van Damme (&) � H. Eggermont
Department of Biology, Ghent University, K.L.
Ledeganckstraat 35, 9000 Ghent, Belgium
e-mail: [email protected]
H. Eggermont
Royal Belgian Institute of Natural Sciences, Freshwater
Biology, Vautierstraat 29, 1000 Brussels, Belgium
123
Hydrobiologia (2011) 676:57–100
DOI 10.1007/s10750-011-0892-0
Keywords Alona sphagnophila n.sp. �Biogeography � Cladocera � Rwenzori Mountains �Taxonomy � Loffler Island � East African Sky Island
Complex (EASIC)
Introduction
Basic faunistic studies of tropical high-mountain lakes
are interesting for more than one reason. (1) Climate
change and the associated glacier retreat can have a
severe impact on high-mountain aquatic ecosystems
and may change the species compositions they harbor
(e.g., Koinig et al., 2002; Eggermont et al., 2010b;
Lami et al., 2010). The loss of permanent ice from
mountain-tops affects regional temperature rise and
causes changes in the ecology of downstream fresh-
water habitats by affecting sediment influx and
nutrient regime (e.g., Schiefer & Gilbert, 2008;
Russell et al., 2009) and heat and water budgets
(e.g., Livingstone et al., 1999; Bajracharya et al.,
2007; Quincey et al., 2007). The timely study of the
aquatic diversity of glaciated mountains provides a
solid reference point for assessing past and future
community change. High-mountain localities suffer
relatively little from direct human interference com-
pared to lowlands, which facilitates the interpretation
of natural changes in the former (e.g., Loffler, 1984).
High-altitude cladoceran communities can be infor-
mative, as the group contains valid indicators for
environmental change, especially among the chydor-
ids (Korhola et al., 2000; Hofmann, 2000; Kamenik
et al., 2007; Chen et al., 2010; Korosi & Smol, 2011).
(2) Isolated high-elevation areas, also known as sky
islands, are important in generating diversity and
allow the study of speciation in parallel with oceanic
islands (e.g., Heald, 1951; Warshall, 1994; McCor-
mack et al., 2009). Sky island habitats allow the study
of evolutionary processes over relatively short geo-
logical time scales, as they are strongly influenced by
the Pleistocene glacial cycles—this glacial-cycle
driven species pump diversification model is gaining
increased attention (McCormack et al., 2009). Trop-
ical mountains in particular have had an important role
as refugia during periods of climate change and may
harbor both ancient relicts as well as recent vicariants
(Hewitt, 1996, 2004). High-mountain lakes are con-
sidered ‘‘cold waters of the tropical belt’’ (Loffler,
1964). The high-altitude lakes of tropical East Africa
are present-day climatic islands, strongly affected by
climatic events during the Pleistocene (Loffler, 1968c,
1984). (3) Due to the limited accessibility of mountain
areas, biodiversity surveys are rare and species
richness may be underestimated. However, high-
mountain lakes, despite being harsh environments
with low average temperature, often higher acidity and
an unusually oligotrophic character compared to
lowland lakes (Loffler, 1964, 1968c), may harbor
interesting cladoceran faunas (Hamrova et al., 2010;
Kotov & Taylor, 2010). The Cladocera, a group of
freshwater microcrustaceans, is a typical group where
the global species richness is underestimated and
progress is limited by taxonomical problems (e.g.,
Forro et al., 2008). Thorough faunistic surveys with
correct identifications are not as common as one might
assume and continuous efforts are needed in order to
interpret biogeography, true diversity and patterns of
endemism in the group (e.g., Frey, 1965; Kotov et al.,
2010). Recent taxonomical revision of populations of
high elevations has revealed significant cladoceran
endemism in South America (Andes: Kotov et al.,
2010) and Africa (Ethiopian Highlands: Kotov &
Taylor, 2010; Fouta Djalon: Van Damme & Dumont,
2009; Drakensberg, e.g., Smirnov, 2007). Cladocera
taxonomy has advanced significantly in the last two
decades, for example, in the most speciose group of
the Anomopoda, the Chydoridae (Van Damme et al.,
2010). A continuation of revisions and updates of
these faunas is important, including that of the high-
altitude habitats (Kotov et al., 2010), in order to
compare diversities and allow better insights in the
cladoceran speciation and biogeography.
The East African Sky Island Complex (abbreviated
as EASIC further in the manuscript), a circular sky
island complex comprising ca. 20 mountains (War-
shall, 1994; McCormack et al., 2009), is a region
where recent updates on invertebrate freshwater
faunas are few and cladoceran endemism has not been
re-evaluated yet. Recent revision of a member of the
Daphnia obtusa-group shows that significant isolation
has occurred in a part of the Ethiopian Highland sky
island complex (Kotov & Taylor, 2010) leading to the
description of a local endemic, previously considered
conspecific with European D. obtusa (Loffler, 1968a,
b, 1984; Green, 1995). Basic studies on East African
mountains date to the sixties and seventies of the
twentieth century. Most are by Heinz Loffler, who
58 Hydrobiologia (2011) 676:57–100
123
wrote a series of papers on tropical high-altitude lakes
and discussed the comparative biogeography of the
freshwater crustacean faunas of mountain lakes in
Africa and South America. Aquatic surveys that
include remarks on Cladocera faunas comprise just a
few lakes from a few localities, namely Mount Kenya
(Loffler, 1964, 1968a, b; Lens, 1978), Rwenzori
(Loffler, 1968a, b), Bale Mountains (Loffler, 1978)
and Mount Elgon (Lowndes, 1931; Brehm, 1935;
Loffler, 1968b). Of these, the crustacean faunas of the
Rwenzori never received proper attention. Loffler
(1968b) remarked that simply too little is known: ‘‘Es
ist aber zu bedenken, daß die Crustaceenfauna des
Ruwenzori-Gebirges, des Mount Meru und des Kili-
manjaro noch viel zu wenig bekannt ist’’. Beside two
small pools, Loffler visited only three real lakes on the
Ugandan side of the Rwenzori range, located along
tourist routes in the Bujuku-Mubuku river drainage
(Lake Mahoma, Lake Bujuku and Lake Irene; Loffler,
1968b). Yet, the Rwenzori Mountains are not poor in
freshwater habitats. The mountain range contains
about 30 named lakes, the majority of which are
located in Uganda (Eggermont et al., 2007). Of the 15
Cladocera species currently known from the EASIC
(Table 1), only five had been reported from the
Rwenzori, and they are considered to show a mix of
biogeographical affinities (Loffler, 1968a, b). Recent
limnological surveys, including previously unex-
plored areas, have now led to detailed descriptions of
the aquatic habitats in the Rwenzori Mountains (Egger-
mont et al., 2007), which allows a more thorough
interpretation of the cladoceran communities.
In this study, we analyse the Cladocera fauna of 18
lakes and 11 pools in the Rwenzori Mountains, the
majority of which are located at or above 3500 m asl
(Fig. 1; Appendix 1 in Electronic Supplementary
material). The purpose of the study is fourfold. (1)
We aim to provide an overview of the Cladocera fauna
of the Rwenzori Mountains, an update and a compar-
ison with earlier species accounts, adding information
on morphology and taxonomy (i.e., revisiting Loffler’s
species accounts). (2) We investigate patterns of
cladoceran biogeography in the EASIC in comparison
with other sky island complexes and determine the
provenance of the species found, hereby revisiting
Loffler’s (1968b, 1984) hypotheses on biogeography.
(3) We discuss the degree of isolation and endemism
of the Rwenzori populations, as far as can be assessed
from morphology, and examine possible factors
influencing dispersal. (4) We investigate the impor-
tance of abiotic factors in structuring the Rwenzori’s
cladoceran communities, and assess their local eco-
logical indicator value.
Study region—The Rwenzori Mountains
(Uganda–D. R. Congo)
A general description of the Rwenzori and its lakes can
be found in in Wetzel (2001), Osmaston (2006) and
Eggermont et al., (2007, 2009). Basic limnology of the
lakes is described in Eggermont et al., (2007) (sum-
marized in Appendix 1 in Supplementary material).
The Rwenzori Mountains lie on the equator along the
border between Uganda and the D. R. Congo, between
Lakes Edward and Albert in the western arm of the
East African Rift System (Fig. 1). It is one of the three
East African mountains that reaches above 5 km
elevation, together with Mount Kilimajaro and Mount
Kenya. Unlike the latter two, the Rwenzori is not an
active volcano but a horst of crustal rock, with
maximum width of 50 km and length of 120 km
(Wallner & Schmeling, 2010). Uplift of the Rwenzori
started as early as 20 Ma ago and elevation of the Lake
Albert rift flanks were prominent at ca. 4 Ma (Plio-
cene), even affecting regional climate (Chorowicz,
2005; Wallner & Schmeling, 2010). The mountain
range has been sculptured by rivers and the repeated
growth of glaciers, resulting in six separate mountains
rising over 4,500 m: Mount Stanley (5,109 m), Speke
(4,889 m), Baker (4,842 m), Gessi (4,715 m), Emin
(4,791 m), and Luigi di Savoia (4626 m). Each of
these consists of several peaks, the highest being
Margharita on Mount Stanley. All mountains were
glaciated until recent times, but ice caps on Mount
Gessi, Emin and Luigi di Savoia have now completely
disappeared. The Rwenzori contains some 30 named
lakes (of which nine are located in the D. R. Congo and
21 in Uganda) and a number of large shallow pools
(Fig. 1; Eggermont et al., 2007). Macrophytes are few
in most lakes, the dominant submerged plants in
African high mountain lakes are mostly Crassula sp.
and Subularia sp., which form meandering crops
(Loffler, 1964). Floating tussocks of Carex runssoro-
ensis can be found in lakes, for example in Lake
Bigata. All lakes in this study (18) occur above
3700 m asl (except for Lake Mahoma at 2990 m), and
range from 0.009 to 11.234 ha in surface area and 3.0
Hydrobiologia (2011) 676:57–100 59
123
Ta
ble
1C
lad
oce
ran
spec
ies
reco
rds
inth
eE
ast
Afr
ican
Mo
un
tain
sb
ased
on
lite
ratu
re
Aber
dar
esa
Mt
Elg
on
aM
t
Elg
on
cM
tK
enyab
Mt
Ken
yac
Kil
iman
jaro
cR
wen
zori
cR
wen
zori
d
Alo
na
affi
nis
barb
ata
Bre
hm
,
1935
=A
lona
barb
ata
Bre
hm
,1935
??
South
ern
Hal
lT
.,U
pper
Thom
son
T.
Hal
lT
.,H
ook
T.,
Upper
Thom
son
T.
L.
Mah
om
aL
.M
ahom
a
Alo
na
cam
bouei
de
Guer
ne
&R
ichar
d,
1893
L.
Hohnel
l
Alo
na
gutt
ata
Sar
s,1862
Hut
T.,
Lar
ge
Hal
lT
.T
win
Tar
n(L
.M
ahom
a)W
ides
pre
ad
Alo
na
inte
rmed
iaS
ars,
1962*
L.
Mah
om
a
Alo
na
sphagnoph
ila
n.s
p.*
L.
Kopel
lo,
L.
Nsu
ranja
Alo
nel
laex
cisa
(Fis
cher
,1854)
??
Nar
oM
oru
T.
L.
Mah
om
a
Alo
nel
lanana
(Bai
rd,
1850)*
(L.
Mah
om
a)
Cer
iodaphnia
reti
cula
ta(J
uri
ne,
1820)
?S
acre
dL
.
Chyd
orus
cf.
sphaer
icus
(O.F
.M
ull
er,
1776)
??
Wid
espre
adW
ides
pre
adL
.Mah
om
a,
L.
Buju
ku
Wid
espre
ad
Daphnia
cf.
curv
irost
ris
Eylm
ann,
1887
L.
Buju
ku
L.
Buju
ku
Daphnia
doli
choce
phala
Sar
s,1895
??
L.
Hohnel
l,E
mer
ald,
Ell
is,
Nan
yuki
T.
Daphnia
magna
Str
aus,
1820
Maw
enzi
T.
Daphnia
cf.
obtu
saK
urz
,1875
Sir
imon
Tra
ckP
.(2
820
m)
Ench
ante
dL
.,N
aro
Moru
T.
L.
Mah
om
aL
.M
ahom
a
Ilyo
cryp
tus
sord
idus
(Lie
vin
,1848)
Upper
Thom
son
T.,
Upper
Kam
iT
.,
South
Hal
lT
.,L
arge
Hal
lT
.
Ench
ante
dL
.
Ilyo
cryp
tus
cf.
gould
eni
Wil
liam
s,
1978*
L.
Kopel
lo
Karu
alo
na
karu
a(K
ing,
1853)
Sir
imon
Tra
ckP
.(2
820
m)
Macr
oth
rix
hir
suti
corn
isN
orm
an&
Bra
dy,
1867
Tel
eki
T.,
South
and
Lar
ge
Hal
lT
.,
Oblo
ng
T.,
Sir
imon
Tra
ckP
ool
Tyndal
lT
.,U
pper
Kam
iT
.
Maw
enzi
T.
Ple
uro
xus
aduncu
s(J
uri
ne,
1820)*
L.
Mah
om
a,
L.
Buju
ku
Sim
oce
phalu
sex
pin
osu
s(D
eGee
r,
1778)
?E
nch
ante
dL
.
aB
rehm
(1935
),b
Len
s(1
978
),c
Lo
ffler
(1968a,
b,
c)an
dth
isdst
udy.
Eth
iopia
nB
ale
Mounta
ins
not
incl
uded
(conta
inth
een
dem
icD
.iz
podva
la,
see
Koto
v&
Tay
lor,
2010).
?,
Pre
sence
but
loca
lity
unsp
ecifi
ed;
*,
new
reco
rds
for
the
Rw
enzo
ri.
L.
Lak
e,P
.P
ool,
T.
Tar
n.
Loca
liti
esbet
wee
nbra
cket
sin
dic
ate
that
only
asi
ngle
cara
pac
ew
asfo
und,
no
live
spec
imen
60 Hydrobiologia (2011) 676:57–100
123
to 37 m in depth (Fig. 1; Appendix 1). They can be
largely divided into two groups (see Eggermont et al.,
2007 for details): (1) Group I lakes located near or
above 4000 m (3890–4487 m) with some direct input
of glacial meltwater and surrounded by rocky catch-
ments or alpine vegetation (Lobelia, Senecio and
Carex spp.); and (2) Group II lakes located mostly
below 4000 m (2990–4054 m), remote from glaciers
Fig. 1 Topographic map of the central Rwenzori mountain
range showing glaciers, river drainages and location of the 18
lakes (black) and 11 pools (grey squares) under study (modified
after Eggermont et al., 2007): 1 Batoda, 2 Kopello, 3 Bigata, 4Africa, 5 Kanganyika, 6 Katunda, 7 Lower Kachope, 8 Middle
Kachope, 9 Upper Kachope, 10 Upper Kitandara, 11 Lower
Kitandara, 12 Bujuku, 13 Lac du Speke, 14 East Bukurungu, 15Nsuranja, 16 Mahoma, 17 Irene, 18 Ruhandika; 19 Balengek-
ania, 20 Salomon, 21 Zaphanas, 22 Zaphania, 23 Tuna Noodle,
24 Josephat 25 Mbahimba 26 Kamsongi 27 Muhesi 28 Mutinda
29 Baguma. The location of the Rwenzori range in Africa is
marked with an asterisk in the inset map
Hydrobiologia (2011) 676:57–100 61
123
and surrounded by Ericaceous vegetation (Erica,
Hagenia, Hypericum, and Sphagnum spp.) and/or
bogs.
The Group I lakes are mildly acidic to neutral clear-
water lakes (surface pH: 5.80–7.82; Secchi depth:
120–280 cm) with often above-average dissolved ion
concentrations (18–52 lS/cm). These lakes are strongly
oligotrophic to mesotrophic (TP: 3.1–12.4 lg/l; Chl a:
0.3–10.9 lg/l) and phosphorus-limited (mass TN/TP:
22.9–81.4). Circulation is different in lakes above
3800–4000 m, lacking any stable stratification because
of the relatively slight differences in the density of water
within the thermal range (Loffler, 1964, 1984). Group II
lakes are mildly to strongly acidic (pH: 4.30–6.69) and
the waters are stained by dissolved organic carbon (DOC:
6.8–13.6 mg/l) and have modest transparency (Secchi-
disk depth: 60–132 cm). They are typical ‘‘brown-water
lakes’’ that dominate at higher latitudes (Loffler, 1964),
with high acidity and low productivity. With a few
exceptions, all Rwenzori lakes were recently formed by
glacial activity (de Heinzelin, 1962; Osmaston, 2006).
The rock pools above 4400 m are formed by glacial
scouring below the headwall of former glaciers; those at
lower elevations have marsh or river features.
The aquatic fauna is poor. For example, isopods
and amphipods do not occur in the East African
high-mountain lakes, freshwater mollusk species are
very few, consisting mainly of Pisidium, in contrast
to the South American mountain faunas (Loffler,
1964). The Rwenzori has no fish and few aquatic
insects besides Diptera (Loffler, 1964; Eggermont
et al., 2009). Diversity in zooplankton in the East
African Mountains is considered ‘‘strikingly poor’’
(Loffler, 1964).
Climate data on the Rwenzori are summarized in
Temple (1961) and Osmaston (1965), the basis for this
paragraph. The Rwenzori Mountains act as a con-
denser, drawing up hot moist air from the surrounding
plains and precipitating the water as snow, rain and
mist (Eggermont et al., 2009). The Rwenzori are
wetter than other East African mountains, with annual
rainfall varying with altitude from 2000 to 3000 mm
and heaviest on the eastern Uganda slope which faces
the prevailing winds. On the Uganda side heavy rain
can occur any time of the year, but the most rainy
periods (wet seasons) are from mid-March to May and
from September to mid-December. The equatorial
position of the mountain range creates daily air
temperature oscillations between -5 and 20�C in the
Alpine and Nival zones, an order of magnitude greater
than the seasonal variation in maximum daytime
temperature. Occasional night-time freezing occurs
from *3000 m altitude (the present-day boundary
between Bamboo and Ericaceous zones); at 4000 m
(the Ericaceous-Alpine zone boundary) freezing
occurs on 80–90% of the nights (Rundel, 1994). The
Rwenzori climate, as a cool, moist island rising from
the dry tropical plains, has encouraged the develop-
ment of a unique variety of terrestrial animals and
plants, including numerous endemic species (summa-
rized in Eggermont et al., 2009). The Rwenzori have
been awarded a national park status in both Uganda
and the D. R. Congo and is a UNESCO World
Heritage site.
Materials and methods
We analyzed a total of 123 samples collected from 18
lakes and 11 pools (i.e., on average six samples per
lake, and one per pool) during both seasons, the wet
season (May 2007) and/or the dry season (July 2005;
July 2006 and January 2009; Appendices 1–2 in
Supplementary material); resampling on various occa-
sions was done to evaluate possible effects of season-
ality and interannual variability. Samples were
collected using a 50 lm-mesh plankton net, instantly
fixed in formaldehyde (3%) or ethanol ([90%), and
kept at 4�C. Water volumes sampled in the littoral
zones were at least several cubic meters and additional
vertical hauls by boat were carried out in the deeper
waters and pelagic areas. Each of the samples was
classified according to habitat types relevant to
Cladocera; more specifically, we distinghuished
between: (1) accessible lake littoral (i.e., with access
to the open water); these samples were taken by boat or
on foot in vegetated, sandy, muddy and/or rocky areas;
(2) lake pelagic; these samples were taken by boat in
the middle of the lake; (3) lake bog; these samples
were taken by boat or on foot in Carex–Sphagnum
swamps surrounding the lakes, at least 2 m from the
lake margin; (4) pool samples, from shallow rock
pools. Water depth was measured with a handheld
depth sounder Echotest II, data for lake depths in
Eggermont et al., (2007). Surface water oxygen (O2),
surface water temperature (SWTemp), specific con-
ductivity (K25) and pH are single (mid-lake) mea-
surements taken at 10 cm water depth with a Hydrolab
62 Hydrobiologia (2011) 676:57–100
123
Quanta multiprobe at the time of sampling and used as
basic limnological data for the Rwenzori lakes (Eg-
germont et al., 2007). Dissolved organic carbon
(DOC), total phosphorus (TP), total nitrogen (TN)
and chlorophyll a (chl a) were determined as described
in Eggermont et al., (2007). In the case of multiple
sampling dates, we used the average of all measure-
ments made. Mean annual air temperatures (MA-
Temp) were in a few cases derived directly from on-
site temperature loggers, yet in most cases were
calculated from a region-specific tropical lapse rate
model (see Eggermont et al., 2010a for details). Fish is
absent in all lakes.
Ordination techniques were used to identify the
principal environmental gradients structuring the
species data (allowing to delineate ecological indica-
tor value). The latter were expressed as presence-
absence data and only taxa occurring in at least two
sites were considered. Forward selection of environ-
mental variables was used to identify which variables
explained the greatest amount of variance in the
species assemblages. Priority was given to variables
with known ecological relevance. Environmental
variables intitially taken into account are MATemp,
K25, pH, DOC, TP, TN, water depth, and Chl a. Of
these, MATemp, K25, TP, water depth and Chl a were
log-transformed in order to alleviate their skewed
distribution. We further added a set of categorical
variables representing the dominant vegetation type in
each lake catchment, namely: bare rocks (Nival),
alpine vegetation (Alpine), alpine vegetation domi-
nated by Carex swamp (Alpine*), Ericaceous vegeta-
tion (Erica), Ericaceous vegetation dominated by
Carex swamp (Erica*), and a mix of montane and
bamboo forest. These categorical variables were
included as supplementary variables. Hence, these
variables do not change the ordination, but were
projected in the ordination space to facilitate the
interpretation of the results. SWTemp data and
elevation were not used since these variables were
highly correlated with MATemp (for the relationships
between the environmental variables, see also Egger-
mont et al., 2007). O2 data were lacking for the pools,
hence this variable was also excluded from the
analyses. Pools for which no environmental data were
available (Salomon’s pool, Zaphana’s pool, Josephat’s
pool and Baguma’s pool) were excluded. Given a short
(\1 SD) gradient length in detrended correspondence
analysis (DCA; Hill & Gauch, 1980), we used
redundancy analysis (RDA) to explore the relation-
ships between the presence-absence of species and the
environmental variables. Ordinations were performed
using the package CANOCO v.4.5 (ter Braak &
Smilauer, 2002) and corresponding plots were made
with CANODRAW v.4.0.
Drawings of the species were made with a camera
lucida mounted on a Kyowa microscope. For orien-
tation of limbs and numbering of setae, there are
different methods (Kotov et al., 2010). We use a
clockwise numbering for limbs two to five, and from
epipodite to gnathobase (away from epipodite) for
setae in exopodite and endopodite. Filter comb setae
are indicated by letters and sensilla indicated as such;
limbs are oriented with ventral side up. Representative
specimens were photographed with a Leica digital
camera mounted on an Olympus microscope, and
presented here as digital composites of stacked
images, each retaining elements in focus (Helicon-
FocusTM
image software). A collection of sealed and
labeled slides and vials containing all species dis-
cussed herein, has been deposited as the ‘‘Rwenzori
Cladocera’’ at the Royal Belgian Institute for Natural
Sciences (RBINS), Brussels, Belgium, under the
Accession Number RBINS IG 31.623; types of
A. sphagnophila n.sp. under Accession Number IG
31.3685 at the same institute. Sample codes in
Appendix 2 in Supplementary material and species
descriptions refer to the bulk collection, provisionally
stored at the Limnology Unit, Department of Biology,
Ghent University, Belgium.
Results
Species account
Order Anomopoda Sars, 1865
Family Chydoridae Dybowski & Grochowski, 1894
emend. Frey, 1967
Subfamily Chydorinae Dybowski & Grochowski,
1894 emend. Frey, 1967
Alonella (Alonella) excisa (Fischer, 1854)
(Alonella excisa species complex)
Material examined: Four parthenogenetic females from
the littoral zone in Lake Mahoma (00�20.7340N,
Hydrobiologia (2011) 676:57–100 63
123
29�58.1020E, 2990 m elevation); coll. on 27.VII.
2006 by H. Eggermont; sample 135b. Three undis-
sected females from Lake Mahoma mounted on slides,
coll. on 07.V.2007 by H. Eggermont, sample 135b;
and 17 females from Lake Mahoma in 90% ethanol in
glass tube, coll. on 07.V.2007 by H. Eggermont,
sample 135b deposited in RBINS collection under
Accession Number IG 31.623.
Morphology Small chydorine recognized by
hexagonal ornamentation with fine striation on the
valves and one or two blunt denticles in the
posteroventral corner (Fig. 2D). Specimens from the
Rwenzori Mountains correspond in morphology to
European populations (described in Alonso, 1996;
Smirnov, 1996). Size of Lake Mahoma females
0.38 mm (n = 4). Specimens are pigmented, but a
darker pigmentation is not unusual in Alonella excisa.
Distribution This is the first record of A. excisa in
the Rwenzori Mountains (not found here by Loffler,
1968b). We found it only in Lake Mahoma, where the
species is abundant in the lake littoral. A. excisa is
reported worldwide, but can be considered a species
complex (Alonso, 1996), for example, Neotropical
records (e.g., Hudec, 1998; Elıas-Gutıerrez et al.,
Fig. 2 Chydoridae of the
Rwenzori Mountains (for A.sphagnophila n.sp. see
Figs. 4, 5). All specimens
are adult parthenogenetic
females, RBINS Accession
Number IG 31.623.
A Chydorus cf. sphaericus(O.F. Muller, 1776), habitus
adult parthenogenetic
female, specimen from Lake
Kopello. B idem,
postabdomen. C idem, first
limb. D Alonella excisa(Fischer, 1854), from Lake
Mahoma; E Pleuroxusaduncus Jurine, 1820, Lake
Bujuku. F Alona affinisbarbata Brehm, 1935, Lake
Mahoma. G Alonaintermedia Sars, 1862, Lake
Mahoma. H Alona guttataSars, 1862, Lake Mahoma.
I Alona guttata with
tuberculate carapace, Lake
Kopello. Scale bar indicates
100 lm except for B–
C (50 lm)
64 Hydrobiologia (2011) 676:57–100
123
1999) likely belong to a different species. Alonso
(1991) notes that A. excisa is likely not even a single
entity in Spain. A. excisa is originally described from
the vicinity of St. Petersburg, European Russia
(Fischer, 1854) and is widespread in Europe
(Smirnov, 1996). It occurs at higher altitudes in
Europe and is, for example, very abundant in the
Pyrenees (Alonso, 1996). In the African lowlands, the
species is known from North Africa (Tunesia/Algeria;
Gauthier, 1928), Lake Chad (Rey & Saint-Jean, 1968),
the East African Rift (Tanzania/Kenya in von Daday,
1910; Lake Malawi in Fryer, 1957), Nigeria (Green,
1962; Okogwu, 2009), Fouta Djalon Mountains
(Dumont, 1981) and Mali (Dumont et al., 1981). A.
excisa has occasionally been reported from lowland
Uganda lakes (Knockaert, 2002; Rumes, 2010) and D.
R. Congo (Brehm, 1939). In South Africa (e.g., Cape
Flats; Sars, 1916), A. excisa is considered a Palaearctic
element (Smirnov, 2008). In East African mountains,
it is known from Mount Elgon (Brehm, 1935; Loffler,
1968b) and Mount Kenya (Loffler, 1968b; Table 1). In
fact, Loffler (1968b) considered A. excisa locally the
most abundant chydorid on Mount Kenya, even more
common than C. sphaericus: ‘‘die eigenen
Aufsammlungen weisen diesen Chydoriden als
haufigen Bewohner ostafrikanischer Hochgebirge
aus’’. In Mahoma, this species has the second
highest abundance in the littoral, after C. cf.
sphaericus.
Ecology In Europe, A. excisa, likely a complex even
here, has a broad ecological range (Alonso, 1996;
Flossner, 2000) yet it shows a clear preference for acid
waters (pH around 5.5) and is considered an
acidobiontic species and may tolerate strongly acidic
conditions (as low as pH 3.3), often associated with
Sphagnum (Fryer, 1968, 1993; Krause-Dellin &
Steinberg, 1986; Duigan, 1992). Considered a north-
temperate species in Harmsworth’s (1968) latitudinal
temperature classification. In the Rwenzori, it occurs
at a pH of 5.75 and an altitude of 2990 m, restricted to
the littoral zone of Lake Mahoma (Appendix 2 in
Supplementary material).
Alonella (Nanalonella) nana (Baird, 1850)
Material examined: One valve from the littoral zone in
Lake Mahoma (00�20.7340N, 29�58.1020E, 2990 m
elevation), coll. on 07.V.2007 by H. Eggermont, sample
135a, mounted on slide, deposited in RBINS IG 31.623.
Morphology Smallest species of the Chydorinae,
with strong continuous striation on the valves and a
single denticle in the posteroventral corner. Length of
the valve, 0.18 mm. Hudec (2010) suggested a new
subgenus for this species, Nanalonella Hudec, 2010,
so the Rwenzori specimen can be referred to as
Alonella (Nanalonella) nana (Baird, 1850). This
species cannot be confused with A. excisa, the latter
being much larger and with hexagonal valve striation.
Distribution We found a single carapace of A. nana
in Lake Mahoma, which is the first record of A. nana
in the East African mountains. A. nana is restricted in
distribution to the Holarctic region, with a few records
from Asia (Smirnov, 1996). It is extremely rare in
Africa (e.g., Egypt: Dumont & El-Shabrawy, 2008)
and considered a Palaearctic element in South Africa
according to Smirnov (2008), who found it in 1% of
samples he studied from the region.
Ecology In the Rwenzori, the species was found at a
pH 5.25 and an altitude of 2990 m in Lake Mahoma
(Appendix 1 and 2 in Supplementary material). A. nana
is an adaptable species, yet it is typical for oligo-
dystrophic bogs and mires in Europe. It is often associated
with Sphagnum (e.g., Duigan, 1992; Nevalainen &
Sarmaja-Korjonen, 2008), tolerating a pH as low as 3.2,
with an optimum around 5.25 (e.g., Duigan, 1992).
Considered as subarctic in Harmsworth’s (1968)
temperature tolerance classification. Note: we found no
complete or live specimens in the Rwenzori, only one
carapace.
Chydorus cf. sphaericus (O.F. Muller, 1776)
(Chydorus sphaericus species complex)
Material examined: Five adult parthenogenetic females
and one male from the pelagic zone of Lake Nsuranja
(00�17.5790N, 29�54.5010E, 3718 m elevation), coll. on
06.VII.2005 by K. Van Damme, sample 12a. Five
parthenogenetic females from the littoral of Lac du Speke
(00�24.3210N, 29�52.8690E, 4235 m elevation), coll. on
15.VII.2006 by H. Eggermont, sample 111. Five parthe-
nogenetic females from the open water of Zaphania’s
pool (00�18.3850N, 29�53.0830E, 4224 m elevation),
coll. on 13.VII.2005 by K. Van Damme, sample 52a.
Hydrobiologia (2011) 676:57–100 65
123
Fifteen parthenogenetic females from the pelagic zone
of Lake Bigata (00�18.3960N, 29�53.5400E, 3983 m
elevation), coll. on 11.VII.2005 by K. Van Damme,
sample 39. Ten parthenogenetic females from the bogs
bordering Lake Kopello (00�18.6120N, 29�53.
5040E, 4017 m), coll. on 12.VII.2005 by K. Van Damme,
sample 44. Five parthenogenetic females from the littoral
of Lake Bujuku (00�22.6880N, 29�53.5760E, 3891 m),
coll. on 11.VII.2006 by H. Eggermont, sample 100a.
Deposited in collection at RBINS under Accession
Number IG 31.623: Two undissected males and 19
undissected females from Lake Nsuranja (see above)
mounted on slides, coll. on 06.VII.2005 by K. Van
Damme, sample 12a; ten undissected females from
Zaphania’s pool (see above) mounted on slides, coll.
13.VII.2005 by K. Van Damme, sample 52a; ca. 200
females and ten males from Lake Nsuranja (see above) in
90% ethanol in glass tube, coll. on 06.VII.2005 by K. Van
Damme, sample 12a; ca. 100 females from Lac du Speke
(see above) in 90% ethanol in glass tube, coll. on
15.VII.2009 by L. Audenaert, sample L30 and ca. 100
females from Zaphania’s Pool (see above) in 90% ethanol
in glass tube, coll. on 13.VII.2005 by K. Van Damme,
sample 52a.
Morphology Body size of the adult parthenogenetic
female ranges between 0.42 and 0.64 mm. Size ranges
were measured for four localities (Lac du Speke, Lake
Bigata, Lower Kitandara and Upper Kachope), for at
least 35 adult parthenogenetic females per population,
with eggs in brood pouch: Lower Kitandara, from 0.50
to 0.64 mm, average of 0.55 mm (n = 55); Bigata,
from 0.44 to 0.55 mm, average 0.49 mm (n = 55);
Upper Kachope, from 0.42 to 0.59 mm, average
0.50 mm (n = 36); Lac du Speke, from 0.44 to
0.56 mm, average 0.50 mm (n = 35); color from
transparent to mocha-brown pigmentation, remains
after shedding the exuvia. Rostrum with divided apex,
labrum with elongate narrow tip (variability noted by
Loffler, 1968b). Postabdomen with deep preanal
corner, postanal margin round; nine to twelve
marginal preanal (and anal) teeth that are slender
and straight, with similar orientation; basal spine on
basal claw conical to slender, accompanied by a
slender secondary spine more than half as long as
distal spine (Fig. 2B). Two hook-like, thicker bent
setae and one slender seta present on the inner distal
lobe (IDL), typical for the C. sphaericus-group
(Fig. 2C). Comparison (including adult males from
Nsuranja, the only local gamogenetic population
encountered in this study) with populations from
Belgium and line drawings of Iberian specimens
(Alonso, 1996) and true C. sphaericus in Frey (1980),
including postabdomen and limbs of parthenogenetic
females (Fig. 2A–C), shows that specimens from the
Rwenzori morphologically belong to the C.
sphaericus complex and are morphologically close
to C. sphaericus s.str. sensu Frey (1980). Identification
of C. sphaericus populations should be approached
with care, as morphological and genetic variability in
the Palaearctic populations is insufficiently known.
Originally described from Denmark (Frey, 1980), the
C. sphaericus complex remains morphologically
unrevised, even in Europe. This complex is a
taxonomical nightmare of species with little
morphological (e.g., Frey, 1980; Belyaeva, 2003) yet
significant molecular divergence (e.g., Belyaeva &
Taylor, 2009), a cryptic diversity that can be expected
in chydorid species groups (Frey, 1982, 1986, 1987;
Van Damme, 2010). The Rwenzori populations merit
further study, pending revision of the species complex.
Although morphologically similar to European
populations, they show a few striking features: (i) A
larger average body size in basically all lakes (on
average 0.51 mm, and up to 0.64 mm in Lower
Kitandara vs. an average size of 0.35 mm and
maximum size of 0.45 mm in well studied
Palaearctic populations (Frey, 1980; Alonso, 1996;
Belyaeva, 2003). Only 6.8% of the 141 specimens
measured from the four sites listed above were smaller
than 0.45 mm. Such a marked difference in size
ranges, without overlap, may indicate local adaptation
and speciation. In earlier studies of the C. sphaericus
complex, size range differences, even though subject
to environmental conditions, prompted further
investigation, leading to the delineation of separate
species (Frey, 1980). (ii) A thick carapace shell with
dark chocolate-brown pigmentation. Color remains
after shedding of the valves. Loffler (1968b) noticed
that his specimens of the C. sphaericus complex from
Mount Kenya and Elgon were remarkably dark,
particularly in Enchanted Lake (Mount Kenya) and
specimens have a different labrum. Pigmentation
variability in the C. sphaericus complex is a
population trait, influenced by local UV-conditions;
in high-altitude lakes ([4000 m) of the Himalayas,
pigmentation of C. sphaericus s.l. is common (e.g.,
Manca et al., 1994, 1998). (iii) Marginal denticles on
66 Hydrobiologia (2011) 676:57–100
123
the postabdomen are nine to twelve in the Rwenzori
populations, with postanal portion round and
markedly different from anal portion; these teeth are
parallel in orientation; in C. sphaericus s.str. these
denticles are 7 to 12 (commonly 8–10) and the shape
of the postanal portion is less marked from the anal
region and marginal teeth are not parallel in
orientation (Frey, 1980). The larger number of
denticles could be related to the relatively larger size
of the animals.
Distribution Locally, C. cf. sphaericus is the
dominant cladoceran in the Rwenzori Mountains,
found in all waterbodies studied and at high
abundancies. It is the only cladoceran in 50% of the
Rwenzori lakes and found in all pools (Table 1;
Appendix 2 in Supplementary material). The C.
sphaericus complex is considered cosmopolitan, but
true diversity and biogeography remain unknown
because of the taxonomical difficulties (Frey, 1980;
Belyaeva & Taylor, 2009). In the African lowlands, C.
sphaericus occurs in North (Algeria/Tunesia,
Gauthier, 1928; Senegal, de Guerne & Richard,
1892; Egypt, Richard, 1894; Gurney, 1911), West
(Cameroon, Brehm, 1937; Chiambeng & Dumont,
2005) and South Africa (Harding, 1961; Frey, 1993a;
Smirnov, 2008). It is absent from the Ugandan crater
lakes at the foot of the Rwenzori Mountains, despite
intensive sampling (Rumes, 2010). A few records
from the regional lowlands exist, namely by von
Daday (1910) from East Africa and by Fryer (1957)
from Malawi. C. sphaericus is abundant in high
mountain regions worldwide ([3000 m elevation)
(Flossner, 1972; Cruz, 1981; Manca et al., 1994). In
Afromontane regions, the C. sphaericus complex is
widespread on Mount Elgon (Brehm, 1935; Loffler,
1968b) and Mount Kenya (Loffler, 1968b; Lens, 1978;
Table 1). Loffler (1968b) called C. sphaericus the
dominant Cladocera species of the East African high-
mountain lakes, which he recorded in 25% of all
waters studied. We can confirm its dominance in the
waters throughout the Rwenzori.
Ecology The most abundant cladoceran species in
the Rwenzori Mountains, C. cf. sphaericus occurred in
all habitat types (Appendix 2 in Supplementary
material). It is equally common between wet
Sphagnum in the bogs, as it is in pools, in the littoral
or the pelagic of lakes. We found only one
gamogenetic population (males and females) in Lake
Nsuranja, whereas all other populations are
parthenogenetic. The C. sphaericus complex is
known to have a broad ecological tolerance
(Smirnov, 1971; Frey, 1980; Flossner, 2000), and
has been named ‘‘a specialist in tolerance’’ (Belyaeva
& Deneke, 2007). It has a broad tolerance for pH, but
prefers slightly acidic waters (pH *6.00) and may
tolerate water with a pH as low as 3.00, allowing it to
survive under extreme conditions (Lowndes, 1952;
Flossner, 1972; Fryer, 1993; Belyaeva & Deneke,
2007). For example, in alpine lakes in the Tatra
Mountains this species is extremely common, local
acidification events having led to the extinction of all
cladoceran species except for C. sphaericus (Horicka
et al., 2006; Sacherova et al., 2006). In high-altitude
lakes, it is often one of the few animals to thrive, up to
even 5436 m in the Himalaya (Manca et al., 1994).
Studies have shown C. sphaericus to be a fast, strong
colonizer in newly formed habitats, with high
dispersal capacities even among chydorids, most
recently illustrated by Louette & De Meester (2004,
2005). Temperature classification according to
Harmsworth (1968) is arctic. In the Rwenzori, C.
cf. sphaericus occurs at a pH between 3.78 and
7.28, in all water types and at altitudes ranging from
2990 to 4573 m. It is the dominant and often only
inhabitant of lakes in the alpine zone in the
Rwenzori. In some lakes, like Kopello, local
abundances are high enough to observe this
chydorid’s biomass in the open water.
Pleuroxus aduncus Jurine, 1820 (Pleuroxus aduncus
species complex)
Material examined: Two parthenogenetic females
from the pelagic zone of Lake Bujuku (00�22.6880N,
29�53.5760E, 3891 m elevation), coll. on 11.VII.2006
by H. Eggermont, sample 102. One parthenogenetic
female from the littoral of Lake Mahoma (00�20.7340,29�58.1020, 2990 m), coll. on 07.V.2007 by H.
Eggermont, sample 135b, deposited complete on slide
in RBINS collection IG. 31.623.
Morphology Shape of the postabdomen and the
habitus (Fig. 2E) leave no doubt that the Rwenzori
populations of Pleuroxus belong to the globally
widespread P. aduncus species complex. Partheno-
genetic females from Bujuku have a length of
Hydrobiologia (2011) 676:57–100 67
123
0.48 mm (n = 2). Two to four denticles in
posteroventral corner and labral keel with indentation.
The second antennae have three long terminal setae of
similar size in outer branch, two long and one short (by
half) terminal setae on the inner branch. The species
complex is partially revised, with several taxa recently
delineated (Smirnov et al., 2006) like the South African
P. carolinae (Methuen, 1910). Rwenzori specimens are
close to the populations depicted in Alonso (1996) from
Spain and correspond to the key in Smirnov et al., (2006)
leading to P. aduncus, but the details, variability and
cryptic diversity of European populations of true
P. aduncus remain unknown. Smirnov (2008) notes a
Pleuroxus sp. of the P. aduncus-group from South
Africa, yet since no description of the variability in
European populations exist, the identity of similar
forms, such as the Rwenzori populations, is uncertain.
However, Smirnov (2008) notes an important difference
between P. aduncus from Europe and P. aduncus-like
species from South Africa related to the length of the
terminal setae in the second antennae. The setae are of
equal size in the undescribed South African congener,
but unequal in the Palaearctic populations, in one
antennal branch. The Rwenzori specimens from Lake
Mahoma and Bujuku have a clearly shorter terminal seta
on the endopod. Hence, for this diagnostic character,
they are different from the South African P. aduncus-
like species sensu Smirnov (2008), but similar to the
European, true P. aduncus.
Distribution We found P. aduncus only in Lake
Bujuku (pelagic) and Lake Mahoma (littoral)—the
first record of Pleuroxus from East African mountain
lakes (Table 1; Appendix 2 in Supplementary
material). Populations attributed to P. aduncus are
rare, but occur in a few Ugandan lowland lakes at the
foot of the Rwenzori Mountains (Knockaert, 2002;
Rumes, 2010); in Lake Naivasha, Kenya (Jenkin,
1934; as P. aduncus var. makaliensis) and in
Cameroon (Chiambeng & Dumont, 2005). Detailed
distribution of P. aduncus s.str., originally described
from the vicinity of Geneva (Switzerland) is unknown
until thorough revision is carried out, but this may be
considered a European species (Frey, 1993b).
Ecology In Europe, P. aduncus is a low and medium
altitude species of large, and well-vegetated alkaline
waters ([pH 6.8) in high supply of Ca? (20.8 mg l-1)
(Krause-Dellin & Steinberg, 1986; Fryer, 1993;
Alonso, 1996; Flossner, 2000). The typical habitat
preferences in Europe contrast with its occurrence in
the Rwenzori lakes Bujuku (3891 m and pH 6.39) and
Mahoma (2990 m and pH 5.75), indicating that these
specimens might 1. belong to a closely related taxon,
with different adaptations or 2. considering the low
number, conditions do not allow the species to thrive
locally and these are ephemeral arrivals. Species
related to P. aduncus are tolerant for extreme
conditions at high altitudes and among the very few
Chydoridae successful in the subantarctic arc
(P. wittsteini Studer, 1878) and the high Andes
above 4000 m (P. hardingi Smirnov et al., 2006 and
P. fryeri Kotov et al., 2010) (Smirnov et al., 2006;
Kotov et al., 2010).
Subfamily Aloninae Dybowski & Grochowski, 1894
emend. Frey, 1967
Alona guttata Sars, 1862
Material examined: Ten parthenogenetic females
from the littoral zone of Lake Kopello (00�18.6120N,
29�53.5040E, 4017 m elevation); coll. 12.VII.2005 by
K. Van Damme; sample 43a and 44. Ten parthenoge-
netic females from the littoral zone of Lake Nsuranja
(00�17.5790N, 29�54.5010E, 3718 m elevation); coll.
06.VII.2005 by K. Van Damme; samples 3a, 4, 6 and
10. Three parthenogenetic females from the littoral
zone of Lake Mahoma (00�20.7340N, 29�58.1020E,
2990 m elevation); coll. 27.VII.2006 by H. Egger-
mont; samples 129 and 135a. Five parthenogenetic
females from the littoral zone of Lake Bujuku
(00�22.6880N, 29�53.5760E, 3891 m elevation); coll.
11.VII.2006 by H. Eggermont; sample 101a. Speci-
mens deposited in RBINS collection: I.G. 31623: Two
parthenogenetic females mounted on slide and 55
parthenogenetic females in 90% ethanol in glass tube
from Lake Mahoma (see above), coll. 12.VII.2009 by
L. Audenaert, samples 159 and 157. Comparative
material: ten parthenogenetic females of Alona guttata
from a pond at Heusden, Belgium; and A. guttata
Lectotypes Sars, Zool. Mus. Oslo, Accession Number
F9036, Mp137.
Morphology Size range: 0.30–0.35 mm (Lake
Nsuranja). A small Alona (Figs. 2H–I, 3A) with
relatively short marginal setae and a narrow, elongate
postabdomen (Fig. 3B) compared to A. sphagnophila
68 Hydrobiologia (2011) 676:57–100
123
n.sp (Fig. 4A, J). Carapace with and without tubercles.
Postabdomen (Fig. 3B) of Rwenzori specimens with
seven to eight postanal denticles, two larger distally;
three to five clusters of denticles in anal portion; in
shape, a deep preanal portion and dorsal and ventral
postanal margin parallel with ventral margin, and not
strongly protruding. Labral keel with indentation.
Comparison with European populations suggests the
Rwenzori population falls within the variability of
A. guttata. A. guttata is another unsolved species
complex with more than one species in Europe
(Sinev, 1999b; Sarmaja-Korjonen & Sinev, 2008;
Van Damme et al., 2010). A thorough revision of the
cosmopolitan A. guttata group is lacking and future
studies, assessing variation versus speciation, may
reveal closer affinities and status of the Afromontane
populations. Sars (1916) described A. crassicauda
Sars, 1916 from South Africa, of which the status and
detailed morphology remain unknown (Van Damme
et al., 2010).
Distribution Locally, A. guttata is the second-most
common chydorid in the Rwenzori waterbodies, found
in 50% of all the lake localities, and in one pool
(Appendix 2 in Supplementary Material). A. guttata
has been suggested a cosmopolitan species (Sinev,
1999b), yet complexity of its nomenclature worldwide
and recent separation of new species illustrate that care
should be taken in considering these populations
identical (Van Damme et al., 2010). A. guttata has
been recorded from Mount Kenya (Loffler, 1968b;
Lens, 1978; Table 1) and from Ugandan crater lakes at
the foot of the mountain range, although infrequent (3/
61 lakes, only four(!) specimens; Rumes, 2010). The
species has been reported from Sudan (von Daday,
1910), Lake Chad (Rey & Saint-Jean, 1969), D.
R. Congo (Brehm, 1939), Lake Malawi (Fryer, 1957),
South Africa (Smirnov, 2008) and Cameroon
(Chiambeng et al., 2006). A name for South African
populations exists (A. crassicauda), although Smirnov
(2008) also reports true A. guttata from South Africa.
Except for specimens in Lake Mahoma (Fig. 2H), all
Rwenzori populations have tuberculated valves
(Figs. 2I, 3A). Loffler (1968b) recorded a single
tuberculated carapace from Lake Mahoma that he
assigned to A. guttata var. tuberculata (in a footnote),
but suggested that it may well belong to another Alona
with tuberculate forms, e.g., related to A. monacantha
Sars, 1901 (now genus Coronatella; Van Damme
et al., 2010) or A. verrucosa Sars, 1901 (now genus
Anthalona, Van Damme et al., 2011), both of which
have representatives in the African lowlands. No
representatives of the latter two taxa are found in our
Rwenzori material and these are not cold-tolerant
species. We therefore consider Loffler’s initial
attribution of the valve to A. guttata Sars, 1862
correct (note that live specimens were absent in his
samples).
Ecology Alona guttata is the second-most common
chydorid in Rwenzori (see above). The species is
restricted to lake littoral and/or Carex–Sphagnum bogs
in these mountains, with highest abundances in acidic,
brown waters such as Lake Bigata, Nsuranja and Lake
Africa. It occurs at a pH ranging from 4.30 (Lake
Nsuranja; abundant) to 6.39 (Lake Bujuku) and
altitudes between 2990 m (Mahoma) and 4017 m
(Kopello), with one occurrence in Zephania’s Pool at
4224 m, but otherwise absent above 4017 m. In
Europe, A. guttata occurs in a wide range of
habitats, with preference for acidic uplands (pH \5;
Fryer, 1993). In Sweden, it has been recorded at a pH
as low as 3.8 (Berzins & Bertilsson, 1990). A. guttata
is closely associated with vegetation, in particular
Sphagnum moss (Duigan, 1992; Duigan & Birks,
Fig. 3 Alona guttata Sars, 1862. A Habitus adult parthenoge-
netic female from Lake Nsuranja; B idem, postabdomen
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123
Fig. 4 Alona sphagnophila n.sp., adult parthenogenetic
females, collected between Sphagnum in Carex/Sphagnum bogs
bordering Lake Kopello, Rwenzori Mountains (N00�18.6120,S29�53.5040, 4054 m elevation), on 12.VII.2055 by K. Van
Damme; RBINS Accession Number IG 31.3685: A lateral view,
B body outline with ornamentation (tubercles), C posteroventral
corner of carapax, D head shield with head pores, E–F details of
head pores, G labral keel, H first antenna, I second antenna,
J postabdomen, K–L idem, basal claw, M postabdomen of
Alona rustica Scott, 1895 from Norway. Differences with the
postabdomen of A. sphagnophila n.sp. include: 1 length of basal
spine and basal spinules, 2 length of marginal postanal teeth, 3shape postanal dorsal margin (tapering or not), 4 anal denticles
70 Hydrobiologia (2011) 676:57–100
123
2000; Flossner, 2000). North temperate species
according to Harmsworth (1968) temperature
classification. Populations of the A. guttata species
complex (like C. sphaericus) are among the few
chydorids to successfully colonize high latitudes (e.g.,
Greenland, Røen, 1992; Svaldbard, Nevalainen et al.
2011) and high altitudes (e.g., Altai Mountains;
Belyaeva, 2003), up to 5220 m in the Himalaya
(Manca et al., 1994; Manca & Comoli, 2004).
Alona sphagnophila n.sp. (Alona rustica species
complex)
? Alona cf. rustica in Frey (1993a)
Material examined: Six adult parthenogenetic females
from the Carex–Sphagnum bogs bordering Lake
Kopello (00�18.6120N, 29�53.5040S, 4017 m eleva-
tion); coll. on 12.VII.2005 by K. Van Damme, sample
44. Five adult parthenogenetic females from the
Carex–Sphagnum bogs bordering Lake Nsuranja
(00�17.5790N, 29�54.5010S, 3718 m elevation), coll.
on 06.VII.2005 by K. Van Damme, samples 6 and 10.
Comparative material: Specimens were compared
with A. rustica Scott, 1895 from Finland (coll.
B. Walseng), Norway (coll. L. Nevalainen) and
Belgium (coll. K. Van Damme); and to A. iheringula
(Kotov & Sinev, 2005) from Lencoıs Maranhenses,
Brazil (coll. K. Van Damme), in collection UGent.
Type material: Holotype: undissected, parthenoge-
netic female, mounted in glycerol on a glass slide,
labeled ‘‘Alona sphagnophila n.sp. holotype’’, depos-
ited in RBINS collection under Accession Number IG.
31.685, Loc. Lake Kopello Bog (00�18.6120N,
29�53.5040S, 4054 m elevation), coll. 12.VII.2055
by K. Van Damme, sample 44. Paratypes in RBINS
under Accession Number IG. 31.685: seven undis-
sected females in 90% ethanol in glass tube.
Type locality: Between Sphagnum in Lake Kopello
Carex bogs, Rwenzori Mountains, Uganda,
00�18.6120N, 29�53.5040S, 4054 m elevation.
Etymology: The name ‘‘sphagnophila’’, from the
bryophyte Sphagnum and -philos, refers to close
association with Sphagnum, a peculiar ecological trait
of the A. rustica-group, and the preferred habitat of the
species described herein.
Description of adult parthenogenetic female Habitus
(4A–B). Medium-sized animals, 0.42–0.48 mm,
yellow to brown in color. Carapace rectangular with
moderately arched dorsal margin. Ventral carapace
margin rather concave, with deepest ventral point
around midline. Posteroventral corner round, without
notch (Fig. 4C). Dorsal keel absent. Tuberculate
carapace (Fig. 4B), though not all specimens. Head.
Ocellus slightly smaller than eye (Fig. 4A–B). Head
shield (Fig. 4D) about 1.4 times as long as wide, with
relatively short blunt rostrum. Aesthetascs on first
antenna reaching tip of rostrum (Fig. 4A). Three main
head pores (Fig. 4D–F) small and of same size,
narrowly connected; lateral pores closer to main
head pores than to lateral margin of headshield, at
about two IP distance from the midline. Lateral pores
round (Fig. 4E) to small transverse (typical of
A. rustica-group), with small tubular sacks under-
neath (Fig. 4F). Carapace (Fig. 4B). Ornamentation
consisting of parallel, well developed tubercles, no
fine striation (not all specimens), tubercles arranged in
10 to 14 lines. Posterior margin wavy. Marginal setae
long, differentiated into three groups: anterior group of
about 22 long setae, followed by a median group of
about 14 setae, and a third group of about 35 setae.
Row of setae decreasing in size toward the
posteroventral corner, and followed by spinules, of
which the first are long, reaching beyond the margin
(Fig. 4C).
Labrum (Fig. 4G). Labral keel in lateral view
relatively short with wavy margin and broadly obtuse
tip without indentation. Group of long ventral setules
on labral keel, and four to five lateral rows of shorter
spinules. Antennules (Fig. 4H). About two times as
long as wide, sensory seta implanted at one third from
apex. Short setules on margin in four groups. Aes-
thetascs little shorter than antennular body, subequal
in length. Second antennae (Fig. 4I). Setae on anten-
nal basis as long as first segment and with long setules
in distal halves. Basal spine small, conical. Spinal
formula 001/101, setal formula 113/003. First exopod
seta on antenna rather thick; on external side of second
exopod segment, group of fine parallel spinules. Spine
on first endopod segment not reaching half of second
endopod segment; main terminal spines on endo- and
exopod well developed and about as long as ultimate
segment. Terminal setae subequal in length (Fig. 4A).
Postabdomen (Fig. 4J). Relatively rectangular,
widest at preanal angle, and with protruding dorso-
distal margin. Postabdomen does not narrow strongly
distally. Length 2–2.5 times as long as wide. Ventral
Hydrobiologia (2011) 676:57–100 71
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72 Hydrobiologia (2011) 676:57–100
123
margin shorter than anal and postanal margin. Anal
and postanal margins of similar length and longer than
preanal margin. Anal margin straight to moderately
concave, postanal margin completely straight, distal
margin protruding with deep dorsodistal notch. Prea-
nal corner weakly developed, triangular, protruding
just beyond postanal margin. Eight to nine teeth on
postanal margin, merged with small setules on anterior
margin. Third tooth (from basal claw to anal margin)
largest. Lateral fascicles arranged in eight groups in
postanal portion; each group consists of 10 to 15
spinules arranged parallel, with the longest placed
medially (giving groups a conical appearance). Three
clusters of marginal denticles in two to three trans-
verse rows in anal portion. Three ventral groups of
setules, oriented posteriorly. Terminal claw (Fig. 4K–
L). Shorter than anal margin, evenly to strongly
curved. Well-developed basal spine, about as long as
claw width at base and about a third of claw length.
Group of seven to ten short basal spinules.
Six pairs of limbs. First limb (Fig. 5A–D). Epipodite
round without long projection reaching beyond limb
base. First endite with two marginal setae and one short
dorsal seta (Fig. 5B), second endite (Fig. 5C) with three
setae of which two longer (and subequal in size), and third
endite with four setae (Fig. 5A). Outer distal lobe (ODL)
with one slender seta longer than largest seta on inner
distal lobe (IDL; Fig. 5D); IDL with three setae, shortest
naked; armature of two largest IDL setae fine unilateral
setulation in distal half, no strong denticles or spines.
Accessory seta present near base ODL, short and
plumose. Five to six anterior setule groups with more
than four fine straight spiniform setules. Ejector hooks
relatively short and subequal, and gnathobase elongated
with setulated apex (Fig. 5A).
Second limb (Fig. 5E–H). Exopodite (Fig. 5E) with
short seta bearing few long apical setules. Endites with
eight slender scrapers decreasing in length toward
gnathobase; first two scrapers largest; third to fifth
scrapers smaller but of similar length; sixth to eight
scrapers again smaller, with seventh scraper stoutest
and with shorter, thicker denticles (Fig. 5F); reduced
anterior seta present at the base of the first scraper,
minute. Gnathobase (Fig. 5G) with a ‘brush’ consist-
ing of short spinules, and three setae: first, a bent seta;
second, a plump seta with small denticles in distal half;
and third, a simple naked seta. Filter comb (Fig. 5E)
with seven setae of which only the first short (one third
the size of the second) and brushlike, with setules
implanted around its distal half (Fig. 5H).
Third limb (Fig. 5I–L). Pre-epipodite and epipodite
round, lacking projections (Fig. 5I). Exopodite
(Fig. 5I) with quadrangular corm, implanted with
rows of minute denticles on inner side and seven large
marginal setae in 2 ? 5 arrangement; first seta longer
than second but both short; third seta shorter than sixth
seta; fourth and fifth seta both short, 1/4th of sixth seta;
seventh seta shorter than sixth; all these setae are
plumose, except for sixth and seventh being pappose
in the proximal half and unilaterally implanted with
short denticles in distal half (Fig. 5J). External endite
(Fig. 5I) with three setae (10–30) of which first two
scraper-like, of similar size and with minute element
in between, third (30) shorter and with long setules;
four well developed plumose setae on inner side (100–400) of same length. Internal endite with one naked
element and four small setae with curved apex (100–500
in Fig. 5K) preceding gnathobase. Gnathobase with a
bottle-shaped sensillum and short plumose seta with
two naked elements at its base (Fig. 5L). Filter comb
with seven long setae (Fig. 5I).
Fourth limb (Fig. 5M–P). Pre-epipodite oval, and
epipodite oval-round with long projection (Fig. 5M).
Exopodite (Fig. 5M–N) square, implanted with rows
of minute denticles on inner side and with six marginal
setae; first three setae longest; fourth less than half of
third seta; fifth and sixth setae little longer than fourth,
and also narrower than others, with fine short setules
on distal two thirds. Between third and fourth exopo-
dite setae, there is a strongly setulated hillock where
setules continue downwards on the external exopodite
corm, almost like a reduced twisted seta; thus far, this
character has never been recorded for the A. rustica-
group. Endite (Fig. 5O–P) with marginal row of four
Fig. 5 Alona sphagnophila n.sp., adult parthenogenetic
females, limb morphology. Specimens collected between
Sphagnum in Carex/Sphagnum bogs bordering Lake Kopello,
Rwenzori Mountains (N00�18.6120, S29�53.5040, 4054 m
elevation), on 12.VII.2055 by K. Van Damme; RBINS
Accession Number IG 31.3685: A first limb, B idem, first
endite, C idem, second endite, D idem, ODL-IDL, E second
limb, F idem, seventh scraper, G idem, gnathobase, H idem, first
filter seta. I third limb, J idem, seventh exopodite seta, K idem,
endite, L idem, gnathobase, M fourth limb, N idem, exopodite,
O idem, endite, P idem, first and second flaming torch setae, Q–
R fifth limb, S sixth limb. as accessory seta, ds dorsal seta, en1first endite, en2 second endite, eh ejector hooks, ep epipodite, exexopodite, fc filter comb, gn gnathobase, gn gnathobase seta,
IDL inner distal lobe, il inner lobe, ODL outer distal lobe,
p process, pep pre-epipodite, s, ss sensillum
b
Hydrobiologia (2011) 676:57–100 73
123
setae (10–40); first scraper-like and longest, with strong
denticles in distal half; following three setae like a
flaming torch, with thick base, and reducing in size
toward gnathobase, and one marginal round naked
sensillum (between 40and gns in Fig. 5O). Gnathobase
with one long setae, bent over endite and two reduced
naked elements; on inner side, three long plumose
setae (100–300) gradually increasing in size toward
gnathobase (Fig. 5O); filter comb with five slender
setae. Endite implanted with groups of small denticles
on outer margin.
Fifth limb (Fig. 5Q–R). Pre-epipodite round with
round apex and implanted with long setules. Epipodite
round with long projection not reaching beyond limb
margin. Exopodite heart-shaped, about twice as long
as wide, with deeply concave expanded margin
between setae three and four and implanted with rows
of minute denticles on inner side. Exopodite is almost
bilobed; four exopodite setae, first three long of which
first two oriented dorsally, about as long as exopodite
length; second exopodite seta longest; fourth exopo-
dite seta as thick as other setae and one-third of the
third seta. Inner portion of limb with triangular inner
lobe with long terminal setules; two thick endite setae
(10–20), first seta two times as long as second seta;
behind second endite seta, a small naked element
(sensillum?). Gnathobase with two naked elements
and filter comb with three long setae.
Sixth limb. Present (Fig. 5S). Large and oval with
one row of small denticles on inner surface. Marginal
setules in three to four different groups.
Male and ephippial females. Unknown
Differential diagnosis Alona sphagnophila n.sp. is
close in morphology to the Palaearctic A. rustica Scott,
1895 and to the Neotropical A. iheringula (Kotov &
Sinev, 2005). Comparison with descriptions of A.
rustica and A. iheringula in Sinev (2001) (originally A.
iheringi Sars 1901) shows several differences: A.
sphagnophila n.sp. differs from A. iheringula in the
presence of a convex wavy labral keel and more lateral
setule rows, a shorter spine on the first endopod
segment of the second antenna (shorter than half the
second segment) and a relatively longer basal spine in
the postabdomen with a group of long basal setules. In
A. rustica (Fig. 4M), the basal spine and setules are
also shorter compared to A. sphagnophila n.sp. The
marginal postanal teeth of both A. iheringula (see Van
Damme & Dumont, 2010) and A. rustica are longer
than those of A. sphagnophila n.sp., and their lateral
head pores are situated relatively closer to the main
pores with larger ‘‘sacks’’ (Frey, 1965; Alonso, 1996;
Sinev, 2001). Limb differences between A. sphagnophila
n.sp. and the other two species are relatively small. The
third to fifth exopodites are nearly identical, but
epipodites four and five in A. sphagnophila n.sp. have
long fingerlike projections, as in A. iheringula (see Sinev,
2001; Van Damme & Dumont, 2010). On the second
limb of A. sphagnophila n.sp., the first two scrapers are
shorter than in A. rustica, third scraper is relatively
narrower and the seventh scraper has more teeth.
Interestingly, sixth limb differs in shape: in A. rustica
and A. iheringula it is much shorter and rounder than it is
in A. sphagnophila n.sp. (compare with Sinev, 1999a).
Note that tubercles on the valves in chydorids are
considered a variable trait, even within a population (e.g.,
Duigan, 1992). In closely related species, tubercles may
be expressed or not and this character is no longer
considered as diagnostic at the species level (Van Damme
et al., 2010).
Distribution In the Rwenzori Mountains, we only
found A. sphagnophila n.sp. in Lakes Kopello and
Nsuranja. A. sphagnophila n.sp. is the first African
representative of the A. rustica-group. Its closest
relatives are the Palaearctic A. rustica rustica Scott
1895; the Nearctic A. rustica americana Flossner &
Frey 1970; the North American A. bicolor Frey, 1965;
and the Neotropical A. iheringula Kotov & Sinev,
2005 (Van Damme et al., 2010). A. sphagnophila n.sp.
is not necessarily a montane endemic. Populations of
A. cf. rustica reported in South Africa by Frey (1993a),
noted as A. rustica in Smirnov (2008), could
theoretically belong to the same species—a revision
of lowland African populations attributed to A. rustica
is lacking, but the species is extremely rare.
Ecology We found A. sphagnophila n.sp. only in
Sphagnum–Carex bogs surrounding lakes Kopello
(4017 m) and Nsuranja (3834 m), not in the lake
littoral (Appendix 2 in Supplementry Material). The
lakes themselves have a pH of 4.30 and 5.07,
respectively, but that of the bogs may well be lower
(not measured). The species was particularly abundant
when squeezing out partially submerged Sphagnum
moss. This may suggest that A. sphagnophila n.sp. can
survive in semi-terrestrial conditions, also known for
Bryospilus Frey, 1980. Association with Sphagnum is
74 Hydrobiologia (2011) 676:57–100
123
known for the closely related A. rustica (Fryer, 1968,
1993; Duigan, 1992; Duigan & Birks, 2000; Flossner,
2000) and tolerance of lower pH levels are known for
both A. rustica in Europe (Fryer, 1993; Duigan &
Birks, 2000) and for A. iheringula in Brazil (Van
Damme & Dumont, 2010), both of the A. rustica
species complex to which the new species belongs. The
current species, A. sphagnophila n.sp., is typically
associated with this environment, in this case Rwenzori
Sphagnum bogs.
Alona affinis barbata Brehm, 1935 or Alona barbata
Brehm, 1935 (Alona affinis species complex)
? Alona martensi Sinev, 2009 in Sinev (2009)
Alona affinis var. barbata Brehm, 1935 in Sinev
(1997: Fig. 4E–F)
Material examined: One parthenogenetic female from
the littoral zone of Lake Mahoma (00�20.7340N,
29�58.1020E, 2990 m elevation), coll. on 27.VII.2006
by H. Eggermont, sample 129, mounted on slide,
deposited in RBINS collection IG. 31.623. One
parthenogenetic female from the littoral zone of Lake
Mahoma, coll. on 07.V.2007 by H. Eggermont, sample
135. Comparative material: Adult parthenogenetic
females of A. affinis from pond in Heusden, Belgium,
Europe, coll. K. Van Damme.
Morphology Rwenzori specimens 0.8 mm in length
(Fig. 2F). First antenna with a group of four to five
long setae (Fig. 6C), as in A. affinis barbata Brehm,
1935, described from Mount Elgon as A. affinis var.
barbata (Fig. 6D). As Smirnov (1971) (see Van
Damme et al., 2010), we consider A. affinis barbata
at least a subspecies of A. affinis, not a variety, but the
limited number of specimens does not allow a
complete redescription here. One of two specimens
had malformations of the postabdomen (Fig. 2F),
indicating suboptimal conditions in chydorids
(Smirnov, 1971). Comparison between A. affinis
barbata Brehm, 1935 and A. affinis affinis (Leydig,
1860) (see also drawings in Alonso (1996) and Sinev
(1997, 2009)), revealed the following differences:
(i) Main head pores of A. affinis barbata are situated
further apart and less than one interpore distance from
the posterior head shield margin (Fig. 6A–B); (ii) The
antennule of A. affinis barbata has a group of four to
five long setules (the so-called ‘‘beard’’ which has led
to Brehm’s choice of the name barbata; Fig. 6C–D),
instead of one or two shorter setules here in European
A. affinis affinis (Sinev, 1997; Fig. 6E); (iii) First limb
of A. affinis barbata has the shortest inner distal lobe
(IDL) seta only moderately developed and not
strongly curved (Fig. 6F), whereas A. affinis affinis
always has strongly chitinized and hook-like IDL seta
(Fig. 6G), this is a marked difference; (iv) A. affinis
barbata has relatively shorter fourth exopodite seta on
the fourth limb (Fig. 6H) than A. affinis affinis
(Fig. 6I) and the epipodites of limbs three to five
have long projections (Fig. 6J) instead of short bumps
in A. affinis affinis (Fig. 6K); (v) The postabdomen of
A. affinis barbata has a basal group of five to seven
strong setules (Fig. 6L) whereas A. affinis affinis only
has four to five thicker spines (Fig. 6M). Finally, the
general shape of the postabdomen is also more
rounded distally in A. affinis barbata (Fig. 6L). In
conclusion, we think Brehm’s form from Mount
Elgon, with the characteristic antennular setulation,
occurs in the Rwenzori, and it should be considered at
least a separate subspecies, maybe a candidate for a
full species, Alona barbata Brehm, 1935.
The characters mentioned here, which set apart the
Rwenzori specimens from the European A. affinis
populations, are diagnostic for a recently described
species in the A. affinis species complex, Alona
martensi Sinev, 2009 from the Drakensberg Moun-
tains, South Africa (Sinev, 2009). Populations from
Mount Elgon, type locality of A. affinis barbata,
should be investigated, but it means that the name
Alona martensi Sinev, 2009 could be invalid and a
junior synonym of Alona affinis barbata Brehm, 1935,
or, if raised to full species status, of Alona barbata
Brehm, 1935. Morphology of limbs (P1 IDL, P4
exopodite), postabdomen (basal spinules) and the first
antenna (very typical!) of the few specimens investi-
gated here, lean toward the rejection of A. martensi.
However, some characters differ (shape of postabdo-
men, PP/IP distance). As we had only two specimens,
of which only one with a ‘‘normal’’ postabdomen,
more specimens and a detailed comparison of limb
characters is needed between the Drakensberg and
Mount Elgon populations to make a clear decision—
we have now no clear idea about the variability of A.
barbata and it is likely that both populations (Rwenz-
ori and Drakensberg) originate from the same stock,
yet may have been separated long enough to diverge.
Whatever the name, considering the characters men-
tioned above (Fig. 6), the Drakensberg Mountain
Hydrobiologia (2011) 676:57–100 75
123
Fig. 6 Comparison between Alona affinis barbata Brehm,
1935 or A. barbata Brehm, 1935 (adult parthenogenetic female
from Lake Mahoma: A, B, C, F, H, J, L) and Alona affinis affinis(Leydig, 1860) (parthenogenetic female from Belgium: E, G, I,
K, M). Arrows indicate diagnostic characters of A. affinisbarbata Brehm, 1935. A Head pores barbata, B head shield
barbata, C first antenna barbata, D first antenna of barbata from
Mount Elgon, after Brehm (1935), E first antenna affinis, F inner
(IDL) and outer (ODL) distal lobe on first limb of barbata,
G idem, affinis, H fourth limb with exopodite setae four to six in
barbata, I idem, affinis, J epipodite of fourth limb, barbata,
K idem, affinis, L postabdomen, barbata, M idem, affinis
76 Hydrobiologia (2011) 676:57–100
123
populations depicted by Sinev (2009) and the Rwenz-
ori specimens, are closest in morphology within the A.
affinis-species group and markedly different from the
European A. affinis.
Distribution We found two specimens of A. affinis
barbata in the littoral of Lake Mahoma (Appendix 2 in
Supplementary material). This taxon was recorded
from the same locality by Loffler (1968b, as A. affinis;
Table 1). In the East African mountains, A. affinis is
reported from Mount Elgon (Brehm, 1935; Loffler,
1968b; Table 1), Mount Kenya (Loffler, 1968b) and
the Gebel Marra Mountains in Sudan (Sinev, 1997).
Members of the A. affinis species complex are virtually
absent from the African lowlands, but reported from
West Africa (Dumont et al., 1981; Chiambeng et al.,
2006) and South Africa (Sars, 1916). In East Africa,
Thomas (1961) reported A. affinis from Ugandan
swamps at 2130 m altitude. It is, however, not certain
that these are identical to the barbata discussed herein.
A form similar to A. affinis barbata is reported from
Mexico (Sinev, 1997). There are no records of A. affinis
barbata in the Palaearctic region or African lowlands.
If A. martensi is a junior synonym, the distribution of
A. affinis barbata extends into the Drakensberg
Mountains (South Africa), but in any case both forms
can be considered as closely related.
Ecology In Europe, true A. affinis has a broad
ecological range. This species is predominantly an
inhabitant of lowland, well-vegetated alkaline waters
(Flossner, 2000), but it may tolerate strongly acidic
upland areas (pH \5; Fryer, 1993). True A. affinis is
considered subarctic, in Harmsworth’s (1968)
temperature classification. In the Rwenzori, the few
specimens of A. affinis barbata were not in optimal
condition (one deformed); the conditions in Lake
Mahoma at the time of sampling, or the current
habitat, could be suboptimal for the species.
Alona intermedia Sars, 1862
non Alona intermedia sensu Alonso (1996)
Material examined: Five parthenogenetic females from
the littoral of Lake Mahoma (00�20.7340N, 29�58.1020E,
2990 m asl), coll. on 27.VII.2009 by H. Eggermont,
sample 129. Specimens deposited in RBINS under
Accession NUmber IG. 31.623: two undissected adult
females, mounted on slides and 13 females in 90%
ethanol in glass tube, from Lake Mahoma, coll. on
12.VII.2009 by L. Audenaert, sample 159. Comparative
material Five adult parthenogenetic females from Fin-
land, coll. by L. Nevalainen. Ten adult parthenogenetic
females, Okavango Delta, coll. H.J. Dumont and R. Hart,
from collection at UGent.
Morphology Body size 0.36–0.38 mm (Fig. 2G).
We compared Rwenzori specimens with populations
from terra typica Scandinavia and from South Africa,
and found a difference in lengths of distal spines in the
three distalmost lateral fascicle groups: in ‘‘true’’ A.
intermedia and Rwenzori populations, these spines are
long, reaching over the marginal denticles by at least
one third their length. In South African populations,
these lateral spines are much shorter, barely reaching
over the marginal denticles. Populations described
from Spain by Alonso (1996) correspond to the South
African populations, whereas populations from
Cameroon (Chiambeng et al., 2006) are more similar
to the North European A. intermedia. Although subject
to variability, the relative length of lateral spines on the
postabdomen relative to the marginal denticles, can be
a valid diagnostic feature in Alona-like chydorids (e.g.,
in Anthalona, Van Damme et al., 2011), but further
research of comparative limb morphology is needed to
confirm the presence of two different species
(Mediterranean-Ethiopian vs. Palaearctic).
Distribution This is the first record of A. intermedia
for East Africa, including lowlands—we found it only in
Lake Mahoma in the Rwenzori. A. intermedia s.l. has
previously been recorded from lowlands of South Africa
(Sars, 1916; Frey, 1993a; Smirnov, 2008) and West
Africa (Chiambeng et al., 2006) but, as mentioned
earlier, the South African populations may not be
identical to true A. intermedia. A. intermedia has been
recorded worldwide (e.g., Idris, 1983; Flossner, 2000),
but caution should be taken as the species complex has
not yet been revised (Smirnov, 1971; Chengalath, 1987;
Van Damme et al., 2010). True A. intermedia described
from Norway is considered a Holarctic species with a
boreo–alpine to arctic–alpine distribution (Fryer, 1993;
Flossner, 2000); in Europe, it is surviving in relict
populations in moorland and mountain locations
(Flossner, 1972 in Duigan, 1992).
Ecology In Europe, A. intermedia prefers oligo-
trophic, acidic waters (pH\6; Flossner, 2000; pH\7;
Hydrobiologia (2011) 676:57–100 77
123
Krause-Dellin & Steinberg, 1986). In Plastic Lake,
Canada, populations attributed to A. intermedia thrive in
moderate vegetation cover and muddy substrate
(Tremel et al., 2000). In the Rwenzori, A. intermedia
occurs at a pH of 5.75 and an altitude of 2990 m, in the
littoral of Lake Mahoma (Appendix 2 in Supplementary
material).
Family Ilyocryptidae Smirnov, 1992
Ilyocryptus cf. gouldeni Williams, 1978
(Ilyocryptus silvaeducensis species complex)
Material examined: Eight parthenogenetic females from
Lake Kopello Bog, near the inlet (00�18. 6120N, 29�53.
5040E, 4017 m elevation), coll. on 12.VII.2005 by K. Van
Damme, sample 44. Specimens in RBINS Accession
Number IG. 31.623: three females on 90% ethanol in
glass tubes and one dissected female mounted on slide, all
from Lake Kopello Bog between Sphagnum, coll. on
12.VII.2005 by K. Van Damme, sample 44.
Morphology Rwenzori Ilyocryptus populations have
doubled preanal teeth on the postabdomen without
adjacent setules (Fig. 7A–B). Number of doubled teeth
varies between specimens (at least one, but never all).
Only three species of the Ilyocryptidae have this char-
acter state and they all belong to the I. silvaeducensis-
group (I. cuneatus, I. silvaeducensis, and I. gouldeni;
Kotov & Stifter, 2005; Kotov & Elias-Gutierrez,
2009). The Rwenzori specimens all have incomplete
molting, long ventral setules on base of basal claw
(Fig. 7A) and antennal swimming setae unilaterally
armed with long setules on the distal segments
(Fig. 7E). This combination of characters fully
corresponds with I. gouldeni Williams, 1978, which
is now well described (Kotov & Stifter, 2006). In
addition, Rwenzori specimens have six setae in the
gnathobase of the fifth limb, an unmistakable character
for I. gouldeni. The I. silvaeducensis-group, to which I.
cf. gouldeni belongs, is unrelated to the South African
endemic species I. martensi and I. africanus (Kotov &
Stifter, 2005).
Distribution We found I. cf. gouldeni only in the
Sphagnum-Carex bogs surrounding Lake Kopello and
exuviae in a pool connecting the latter lake to Lake
Africa. Real I. gouldeni is common in North America,
and in tropical areas (like Mexico) found only in
oligotrophic, high-elevation lakes (1500–4680 m)
(Kotov & Stifter, 2006). I. silvaeducensis-group
populations are reported from the African continent,
but need re-evaluation (Kotov & Stifter, 2006; Kotov
& Elias-Gutierrez, 2009). Hence, we prefer to assign
the populations to Ilyocryptus cf. gouldeni of the I.
silvaeducensis-group, and we cannot exclude the
possibility that the Rwenzori specimens belong to an
undescribed species. In any case, the Rwenzori
populations are closer in morphology to the Nearctic
I. gouldeni than to any other species described in the
genus, including the Palaearctic I. silvaeducensis or I.
cuneatus.
Ecology In the Sphagnum–Carex bogs (Kopello;
Appendix 2 in Supplementary material), where the
species occurs sympatrically with Chydorus cf.
sphaericus and A. sphagnophila n.sp. In Europe, I.
silvaeducensis is a benthic inhabitant of Sphagnum
bogs, frequently sympatric with I. sordidus (Flossner,
2000; Kotov & Stifter, 2006); the latter species was
reported by Loffler (1968b) from Enchanted Lake on
Mount Kenya (Table 1).
Family Daphniidae Straus, 1820
Daphnia (Daphnia) cf. obtusa Kurz, 1875 (Daphnia
obtusa species complex)
Material examined: Ten parthenogenetic females
from the pelagic of Lake Mahoma (00�20.7340N,
Fig. 7 Ilyocryptus cf. gouldeni Williams, 1978, selected
characters of adult parthenogenetic female from Lake Kopello:
A postabdomen, B double preanal tooth on preanal margin, C–
D marginal valve setae, E asymmetric setule armature of lateral
swimming seta of second antenna
78 Hydrobiologia (2011) 676:57–100
123
29�58.1020E, 2990 m elevation), coll. on 27.VII.2006
by H. Eggermont, sample 131. Specimens deposited in
RBINS Rwenzori collection: 25 females on 90%
ethanol in glass tube, and five undissected females
mounted on slides, all from the pelagic of Lake
Mahoma, coll. on 12.VII.2009 by L. Audenaert,
sample L160.
Morphology Head broad rectangular, extending
dorsally about three times eye diameter from the
dorsal contour of the eye (Fig. 8A–B). No ocular
depression in lateral view (Fig. 8B). Ocellus minute
and without pigmentation (Fig. 8C). Rostrum with
narrow apex, oriented dorsoventrally (Fig. 8B–C).
First antenna protruding past a short broad mound,
with aesthetascs reaching just beyond rostral apex.
Body size 1.5–1.8 mm. Unpigmented. Long setules in
the median frontal region of the carapace a pointed
rostrum, a small blunt caudal projection in the
posterior valve corner (no spine). Juvenile females
may have an acute short caudal spine. Ventral body
margin strongly convex. Abdomen with three dorsal
processes, first longest, at least four times longer than
second, and longer than postabdominal basal claw.
Postabdomen with relatively parallel dorsal and
ventral margins, slightly tapering distally, with
convex anal margin and straight preanal margin,
both of similar size. Eight to nine anal teeth, gradually
increasing distally. Basal claw relatively short (shorter
than preanal margin), with three dorsal pectens,
proximal with eight to nine teeth, medial pecten with
eight to ten large teeth, about twice the size of the
proximal pecten, and distal pecten with numerous fine
teeth, not reaching apex of the claw. Longest teeth in
medial pecten about as long as claw thickness at base.
Status All characters of the Daphnia of Lake
Mahoma correspond to the D. obtusa species group.
Yet, a few remarkable features of the Mahoma
population include: (i) head broadly rectangular with
high dorsal portion and a strongly elongate, narrow
rostral tip, oriented downwards; antennular aesthetascs
reaching rostral tip or just beyond (Fig. 8A–C); (ii)
postabdomen with long spines in the second pecten and
a short basal claw Fig. 8E); and (iii) a very broad and
blunt caudal projection, not a spine, in adult females
(Fig. 8A–B). We therefore indicate the Mahoma
population as D. cf. obtusa, noting that future
revision of African populations of D.obtusa s.str.
may reveal cryptic taxa (Kotov & Taylor, 2010). The
Rwenzori population differs from a recently described
Ethiopian Highland endemic of the D. obtusa species
complex, D izpodvala (Kotov & Taylor, 2010) in:
(i) shape of the postabdomen, which is strongly
tapering in D. izpodvala and relatively parallel in the
Rwenzori population. Also, the median pecten on the
basal claw is more strongly developed in Rwenzori and
there are relatively fewer anal teeth. (ii) Head without
supraocular depression in Rwenzori specimens unlike
D. izpodvala (no ocular ‘‘dome’’). Rostrum of
Rwenzori specimens is longer than that in D.
izpodvala and pointing ventrally. Ocellus in
D. izpodvala is clearly developed, but not so in
Rwenzori specimens.
Because of the complex nomenclature, with names
available for South African populations (e.g., D.
propinqua Sars, 1916, synonymised in Benzie, 2005)
(Kotov & Taylor, 2010), assignment of the Rwenzori
populations will require a larger revision (including
molecular surveys) of African members of the D.
obtusa group. Most likely, more than one species are
present in the region, which are now all grouped under
the same name.
Distribution Locally, this species only occurs in
Lake Mahoma (Appendix 2 in Supplementary
material), reported from the same locality by Loffler
(1968b). The Daphnia (Daphnia) obtusa group is
reported from all continents save Antarctica and well
studied in the Palaeartic (Benzie, 2005), yet little is
known of the affinities of African and Asian
representatives, which may belong to separate clades
(Kotov & Taylor, 2010). Ideas on distribution are
limited by understanding of true diversity in the group.
Discovery of new species is not uncommon
(Adamowicz et al., 2004, 2009; Kotov & Taylor,
2010). The D. obtusa group has been reported from
Mount Kenya (Loffler, 1968b; Lens, 1978; Mergeay
et al., 2005) and from high-altitude lakes in West and
South Africa (Green & Kling, 1988; Green, 1995; refs
in Benzie, 2005; Kotov & Taylor, 2010). Loffler
(1968b) notes ephippia of this species in the sediment
of Lake Mahoma. Loffler (1978) recorded D. obtusa
in the Bale Mountains of Ethiopia, now considered a
local endemic (Kotov & Taylor, 2010), which is
clearly different from the Rwenzori population.
Hydrobiologia (2011) 676:57–100 79
123
Fig. 8 Daphnia species of the Rwenzori, Daphnia cf. obtusaKurz, 1875 from Lake Mahoma and D. cf. curvirostris Eylmann,
1887 emend. Johnson, 1952 from Lake Bujuku. A–E Daphniacf. obtusa, parthenogenetic females from Lake Mahoma: A–
B habitus, arrow indicating obtuse caudal projection, C head,
arrow indicating ‘‘nose’’-like rostrum, D terminal claw, with
strong middle pecten, E postabdomen with relatively short
terminal claw (arrow). F–S Parthenogenetic females of
Daphnia cf. curvirostris from Lake Bujuku (F–K adults, L–
S juveniles). F–G Habitus, ovigerous parthenogenetic female,
H head, arrow points to rostrum and minute denticles, I terminal
claw, J distal marginal teeth, K postabdomen, L juvenile
female, M Daphnia cf. curvirostris, neonate, arrow points to
nuchal organ (left) and tail spine (right), N nuchal organ after
micrograph neonatem, O juvenile female, head, P terminal
claw, Q postabdomen, R inner pecten with cu‘rved distal
denticle, S long caudal spine
80 Hydrobiologia (2011) 676:57–100
123
Ecology In Europe, D. obtusa favors alkaline
conditions at low elevation, but it may tolerate
weakly acidic conditions (Fryer, 1993). In Rwenzori,
D. cf. obtusa occurs at a pH of 5.75 and an altitude of
2990 m, restricted to the pelagic of Lake Mahoma. D.
obtusa is also a rapid and successful disperser among
cladocerans, able to successfully invade new habitats
within a few months (Louette & De Meester, 2004,
2005).
Daphnia (Hyalodaphnia) cf. curvirostris Eylmann,
1887 emend. Johnson, 1952 (Daphnia longispina-
group)
Material examined: Thirty adult parthenogenetic
females from the littoral and pelagic of Lake Bujuku
(00�22.6880N, 29�53.5760E, 3891 m elevation), coll.
on 11.VII.2006 by H. Eggermont, samples 100a, 101a,
102. Specimens in RBINS collection IG. 31.623: ca.
30 females on 90% ethanol in glass tubes, and five
undissected females mounted on slides, from the
pelagic of Lake Bujuku, coll. on 14.VII.2009 by L.
Audenaert, sample L23.
Morphology The Rwenzori population of Daphnia
curvirostris has a rostrum with broad apex and pointed
tip, pointed ventrally (Fig. 8F–H), a postabdomen
with well-developed pectens on basal claws, including
a strong median pecten of the pulex-type (Fig. 8I). The
rostrum is strongly protruding, blunt and has a small
row of setules on the tip. The antennules small not
protruding mound, but aesthetascs just exceeding tip
of rostrum (Fig. 8H). Ocellus pigmented (Fig. 8H).
Body 1.8–2.0 mm, with small caudal spine, between
one-fifth and one-fourth of carapace length.
Unpigmented. Ventral body outline convex. The
caudal spine varies in length but is always well
developed (in adult females about the same length as
the distance from rostral tip to centre of compound eye
and serrated) (Fig. 8F–G). In juveniles, caudal spine
relatively longer, between a third to half body length
(Fig. 8L–M) and serrated (Fig. 8S). Three processes
on abdominal segments (in Fig. 8G), of which the first
is very long and curved, longer than the anal margin
and twice as long as the postabdominal claw, second
and third are small processes; second process is less
than a fourth in length of the first process.
Postabdomen. In shape, tapering distally with ventral
margin relatively convex. Preanal margin longer than
anal margin and slightly concave, with distinct preanal
angle, but postanal angle not developed (Fig. 8K).
Thirteen to sixteen dorsal strong spines on anal and
postanal margin (Fig. 8K), increasing in size distally,
distalmost strongly curved and with thick basis
(Fig. 8J). Postabdominal claw with three pectens on
dorsal margin, proximal pecten with twelve to 15 fine
teeth; medial pecten with seven to nine strong teeth,
shorter than claw width at base, and a distal pecten
with numerous fine teeth, about a third in length of the
teeth in medial pecten and covering most of the claw
length (not tip); three transverse pecten rows, of which
proximal most conspicuous (Fig. 8I). The proximal
pecten consists of nine to 12 teeth in juvenile
specimens, with a remarkable, thick distal tooth in
the group (Fig. 8R). Juvenile females have a long and
relatively robust caudal spine and resemble adult
Daphnia longispina. The D. curvirostris-group is a
genetically monophyletic clade (Kotov et al., 2006)
that belongs to the D. longispina-group and long
spines in juvenile female Daphnia are a well-known
defence against copepods (e.g., in D. middendorfiana,
see Benzie, 2005), which are common in Lake Bujuku.
Status True D. curvirostris was recently redescribed
by Ishida et al. (2006) and several new species in the
group have been separated and described in detail
since (Kotov et al., 2006; Juracka et al., 2010). The
Rwenzori population corresponds to Palaearctic D.
curvirostris in morphology as redefined by Kotov in
Ishida et al. (2006), but a few characters indicate that
care should be taken in considering the Bujuku
population as completely identical: (i) processes on
abdomen with relatively longer first (most anterior)
process than in Palaearctic populations and a stronger
size reduction of second and third abdominal
processes, (ii) aesthetascs on first antenna exceeding
rostral tip; although rostral shape is variable, (iii)
medial pecten on basal claw has relatively fewer (up to
nine) spines (in true D. curvirostris more than ten), (iv)
distinct preanal angle on postabdomen, which is more
typical for D. sinevi Kotov et al., 2006, but not for true
D. curvirostris (see Kotov et al., 2006; Ishida et al.,
2006).
Distribution Within our study area, this species was
only found in Lake Bujuku (Appendix 2), where it was
also recorded by Loffler (1968b; Table 1).
D. curvirostris is a Palaearctic species complex,
Hydrobiologia (2011) 676:57–100 81
123
sporadically found in Africa, North America and
Mexico (Benzie, 2005; Ishida et al., 2006; Nandini
et al., 2009). It has been reported from African
lowland Lake Naivasha (Kenya; between the years
1940 and 1955), identified from ephippia in the
sediment (Mergeay et al., 2004, 2005), Lake Kivu
(Harding, 1957) and from East African high-altitude
ranges (Green, 1995; Mergeay et al., 2005). Diversity
in the D. curvirostris complex is larger than assumed,
as confirmed by recently described species from the
Eastern Palaearctic (Russia and Japan; Kotov et al.,
2006) and Central Europe (Czech Republic; Juracka
et al., 2010). Records from the African continent, in
particular, need detailed molecular and morphological
study for an assessment of true status (Ishida et al.,
2006). We reject the presence of D. longispina s.l. in
Lake Bujuku mentioned in Mergeay et al. (2005,
p. 272); the latter record derived from a confusion with
the younger stadia of D. cf. curvirostris. Loffler
(1968b) noted that D. curvirostris was represented in
the Rwenzori by a purely asexual population, and the
author did not encounter ephippia in the sediments.
Our samples contained a few (pseudo-)ephippial
females but without eggs, and we did not find any
ephippia or notice any males.
Ecology Daphnia curvirostris prefers neutral waters
but records are known from the Palaearctic, with pH
tolerances as low as 4.4 (Flossner, 2000; Benzie,
2005). Closely related species can survive at high
altitudes, such as D. longispina, mentioned from the
Himalaya (Manca et al., 1994: Fig. 3).
Species diversity and distribution
We recorded a total of 11 taxa, of which seven are
restricted to Lake Mahoma (A. affinis barbata, A.
intermedia, Alonella exisa, A. nana, Daphnia cf.
obtusa, P. aduncus) and/or Bujuku (Daphnia cf.
curvirostris, P. aduncus). Two taxa are restricted to
one or two other sites (Ilyocryptus cf. gouldeni in Lake
Kopello bog; and A. sphagnophila n.sp. in Lake
Kopello- and Lake Nsuranja bog). Two remaining
species are widespread. Chydorus cf. sphaericus was
the most dominant and widespread species (i.e.,
present in all sites, regardless of habitat type),
followed by A. guttata, particularly common in the
lake littoral zones and bogs. The littoral samples are
more diverse than the bog- and pelagic samples (eight,
four, and four species, respectively).
The RDA species–environmental plot and sample–
environmental plot (Fig. 9) visualize the main trends
in our dataset, with in fact only four species (C. cf.
sphaericus, A. guttata, A. excisa, and P. aduncus).
Forward selection and Monte Carlo permutation tests
retained the following variables: Depth, MATemp,
TP, TN and pH. The first two axes captured 52.8% of
variation in faunal data. Depth, MATemp, pH, and TP
appeared to be strongly related to RDA axis 1
(correlation coefficients of 0.59, 0.52, -0.54, and -
0.47, respectively), and TN seemed to be strongly
correlated to RDA axis 2 (0.50). Chydorus cf.
sphaericus, occurring in all lakes and pools, plots in
the center of the species plot (Fig. 9b). Group I lakes
and pools holding this species only, are plotted in the
left quadrants (Fig. 9a). These sites are surrounded by
Ericaceous vegetation and/or bogs, and are typified by
lower nutrient values, lower temperatures, and rela-
tively higher pH. The group II lakes, in the (mainly
upper) right quadrants (Fig. 9a), additionally hold
A. guttata (Fig. 9b). These lakes are characterized by
relatively higher temperature and nutrient content, but
lower pH; they are surrounded by rocky catchments
and/or alpine vegetation. The presence of P. aduncus
groups Lake Mahoma and Bujuku, located in the upper
right quadrant (Fig. 9a); A. sphagnophila n.sp. occurs
only in the Kopello and Nsuranja bogs, located in the
upper right quadrants (Fig. 9).
In the majority of lakes, interannual/seasonal
variation is limited: the same species were recorded
during the various seasons and years, and in visibly the
same dominance (Appendix 2 in Supplementary
material). Exceptions include Lake Mahoma and
Bujuku. In Lake Mahoma, there were differences in
the abundance of Chydorus cf. sphaericus (visibly
more abundant in the wet season of 2007), A. excisa,
Daphnia cf. obtusa and A. intermedia. The latter
species were present in higher numbers during the dry
seasons of 2006 and 2009. In Lake Bujuku, P. adun-
cus and A. guttata were only recorded during the dry
season in 2006, although the same habitats were
visited in later years (2007 and 2009).
Note on physiological adaptations
Rwenzori populations of Chydorus cf. sphaericus
showed pigmentation in various degree, with the
82 Hydrobiologia (2011) 676:57–100
123
darkest specimens found in Group I lakes and rock
pools at high altitude. Strongly pigmented forms
attributed to C. sphaericus are also known from Mount
Elgon and Mount Kenya (Loffler, 1968b). Cuticular
pigmentation in Cladocera is not uncommon, partic-
ularly in alpine and arctic environments and induced
as an adaptation to harmful UV-B waves. It is known
for Chydorus (e.g., Loffler, 1968b; Manca et al., 1994)
as well as for Daphnia (Hebert & Emery, 1990; Manca
et al., 1994; Hessen et al., 1999; Tollrian & Heibl,
2004), and often less expressed in dark waters as
humic substances absorb a part of the UV-B (Hessen
& Sorensen, 1990; Bracchini et al., 2010). Like Loffler
(1964), we did not find any pigmented forms of
Daphnia in the Rwenzori. This could be related to the
fact that Daphnia only occurs in Lake Mahoma, at
intermediate elevation and therefore less exposed to
UV-radiation; and in Lake Bujuku, belonging to the
brown-water Group II lakes. An additional factor may
be the timing of colonization and the amount of local
adaptation (the Rwenzori populations may be rela-
tively young). In contrast, the endemic Daphnia of the
Ethiopian Bale Mountains is strongly pigmented
(Kotov & Taylor, 2010). Besides the latter endemic,
no pigmented Daphnia populations occur in the
African Mountains, in contrast to high-mountain
forms in South America (e.g., Daphnia peruviana)
and Asia (e.g., D. tibetana) (Loffler, 1964).
A second physiological feature of the Rwenzori
Cladocera is the presence of long epipodite projections
on the limbs of all chydorids (e.g., compare A. affinis
barbata (Fig. 6J) with A. affinis affinis from a neutral
water (Fig. 6K). The length of the epipodite projection
is used sometimes in chydorid taxonomy to distinguish
between closely related species (e.g., A. rustica and A.
iheringula; Sinev, 2001), but is subject to intraspecific
variability (Kotov et al., 2004). We noted this feature
regardless of the species in the Rwenzori, and
therefore hypothesize that this could also be induced
by conditions related to ion uptake efficiency, such as
a combination of high acidity and low mineral content,
which is typical of these localities. Epipodites are
known to contain special cells involved in ion
transport, much like the nuchal organ (Aladin & Potts,
1995), and larger projections may therefore aid
osmoregulation. Neonates of D. curvirostris (Lake
Fig. 9 RDA site–environmental biplot (a) and species–envi-
ronmental biplot (b) of the Cladocera species of the Rwenzori.
Lake numbers include: 1 Batoda, 2 Kopello, 3 Bigata, 4 Africa,
5 Kanganyika; 6 Katunda, 7 Lower Kachope, 8 Middle
Kachope, 9 Upper Kachope, 10 Upper Kitandara, 11 Lower
Kitandara, 12 Bujuku, 13 Speke, 14 East Bukurungu, 15
Nsuranja, 16 Mahoma, 17 Irene, 18 Ruhandika, 19 Balengek-
ania, 20 Zaphania, 21 Tuna Noodle, 22 Mbahimba, 23Kamsongi, 24 Muhesi, 25 Baguma. *Numbers differ from
Figure 1 and Appendix 1 because not all lakes were taken into
consideration in the analysis
Hydrobiologia (2011) 676:57–100 83
123
Bujuku), show large and well developed nuchal cells,
visible even without staining (see Fig. 8M–N).
Discussion
Species records and diversity
Former species records in the Rwenzori included
A. affinis, Chydorus sphaericus, Daphnia curvirostris,
Daphnia obtusa (under these names originally, but see
taxonomical remarks above; Loffler, 1968b; Lens,
1978; Table 1) and A. guttata, known from a single
carapace from Mahoma (Loffler, 1968b). Additions to
the Cladocera fauna, found in this study, are A. inter-
media, A. sphagnophila n.sp., A. excisa, A. nana,
Ilyocryptus cf. gouldeni, and P. aduncus. All previ-
ously recorded taxa were retrieved and the Rwenzori
Cladocera fauna more than doubled, now counting
eight chydorids, two daphniids and a single ilyocryp-
tid. P. aduncus is the first record of the genus in the
East African Mountains, and we also found one new
species (A. sphagnophila n.sp.) belonging to the Alona
rustica-group. Comprehensive comparison between
populations from the Rwenzori with specimens from
the terra typica, might reveal more new species, as our
understanding of cladoceran biogeography on the
African continent is limited by taxonomical issues.
The Sphagnum-bound Ilyocryptus cf. gouldeni, for
example, found in Lake Kopello bog, is closest in
morphology to the Nearctic I. gouldeni, a species that
occurs in high-elevation sites in the Neotropics (Kotov
& Stifter, 2006). This is a candidate for a yet unnamed
species, perhaps conspecific with African populations
designated as I. cf. silvaeducensis (Kotov & Stifter,
2006; Smirnov, 2008). The two Daphnia populations
in the Rwenzori also deserve closer attention. Subtle
morphological differences may suggest a speciation in
the Mahoma population, diverging from D. obtusa
s.str., originally described from Germany. Without
detailed revision of the D. obtusa-group in the Old
World, which harbors a larger diversity than currently
described (Kotov & Taylor, 2010), the status is unclear.
Several names are available in Africa. Benzie (2005)
lists two South African species as synonyms of
D. obtusa: D. tenuispina Sars, 1916 and D. propinqua
Sars, 1895. Korınek (2002), for example, regards
D. propinqua as a valid taxon. Since several species of
the D. obtusa complex are present in the Holarctic and
Neotropics (Benzie, 2005), Sars’ names from the
African continent may indicate more than just syn-
onyms (Kotov & Taylor, 2010). D. cf. curvirostris
from Bujuku seems very close to true Palaearctic
populations, but morphological and molecular delin-
eation of species in this cluster remain unresolved
(Ishida et al., 2006). Phenotypic plasticity, hybridisa-
tion, intercontinental introductions and poor original
taxonomic descriptions in Daphnia limit our under-
standing of species boundaries in the genus (Taylor &
Hebert, 1993; Schwenk et al., 2000; Kotov et al., 2006;
Nilssen et al., 2007). Morphological assessments
would benefit from molecular screening, to clarify
the provenance and phylogenetic relationships of the
Rwenzori populations.
The number of species of the Rwenzori (11) is
higher than that recorded in the Aberdares (Kenya; two
species; Brehm, 1935), Mount Kilimanjaro (Kenya-
Tanzania; two species; Loffler, 1968b), Mount Elgon
(Uganda; five species; Brehm, 1935; Loffler, 1968b)
and the Bale Mountains (Ethiopia; ca. six species;
Loffler, 1978; Kotov & Taylor, 2010). Species richness
is comparable to that recorded on Mount Kenya
(Kenya; 12 species; Loffler, 1968b; Lens, 1978).
Overlap between the Rwenzori and Mount Kenya
consists of four species only: A. affinis barbata,
A. guttata, A. excisa, and Chydorus (cf.) sphaericus.
There are differences in relative abundance as well.
A. guttata is now the second-most abundant cladoc-
eran species in the Rwenzori, yet seems rare on Mount
Kenya according to literature (three tarns; Lens, 1978).
The opposite is true for A. affinis barbata and A. exc-
isa. These two species were considered common on
Mount Kenya by Loffler (1968b), but they are
restricted in the Rwenzori to Lake Mahoma with
A. affinis barbata very rare (only two specimens, in
several sampling campaigns). Daphnia dolichocepha-
la and Macrothrix hirsuticornis, known from both
Mount Elgon and Mount Kenya (Loffler, 1968b;
Table 1), lack in the Rwenzori. Besides dispersal-
related factors, and a different degree of isolation of
each mountain range, discussed below, the abiotic
environment in the Rwenzori mountain lakes could
serve as an explanation. Rwenzori lakes are distinctly
more acidic and dark (Eggermont et al., 2007) than the
Mount Kenya lakes and therefore other communities
can be expected (Eggermont, unpublished data).
However, insular species compositions such as high-
altitude cladoceran communities remain partly
84 Hydrobiologia (2011) 676:57–100
123
unpredictable due to stochastic processes. Widespread
and common representatives of the Macrothricidae,
Moinidae, Bosminidae (e.g., Bosmina), several Chy-
doridae (e.g., Acroperus harpae, Camptocercus, Ley-
digia, Graptoleberis) and Daphniidae genera (e.g.,
Simocephalus, Ceriodaphnia) also lack in the Rwenz-
ori, although acid- and cold-tolerant species of these
groups could hypothetically survive here.
Afromontane lakes are expected to be less diverse
than lowland lakes in the Afrotropics, which may
easily contain 20–50 Cladocera species (Rey & St-
Jean, 1969; Dumont, 1994; Chiambeng & Dumont,
2005). Lowland lakes often sustain higher food quality
and -quantity, warmer temperatures, diverse macro-
phyte stands and a lower degree of isolation, thus
increased chances for colonization, contributing to
higher Cladocera diversity, yet are also subject to
higher competition and predation (Dumont, 1994).
At least five factors negatively influence the diver-
sity and dispersal of Cladocera in the Rwenzori: First,
most sites in our study are located close to or above
4000 m elevation and are subject to the harsh climate
conditions at this elevation (see Study region).
Although none of the investigated sites had an ice
cover during our visits, the mid-day surface water
temperature is generally low and night freezing occurs
(range of *2.0–9.1�C, excluding the warmer Lake
Mahoma at 2990 m). We therefore can expect species
that can tolerate conditions of lakes at high altitudes. C.
sphaericus, A. affinis, A. guttata, A. rustica, A. excisa
and A. nana, of which populations or close forms are
present in the Rwenzori, are among the few chydorids
to remain when it has become too cold, too acid and too
low in conductivity for other species, for example, in
high-altitude lakes of the Himalaya (Manca & Comoli,
2004), or during Late Glacial periods in Europe, like
the Younger Dryas (Lotter et al., 1997; Hofmann,
2000; Duigan & Birks, 2000). In temperate lakes
during the Younger Dryas, chydorid communities only
consisted of a few species that now dominate under
arctic/subarctic conditions (Harmsworth, 1968; Hof-
mann, 2000). In the high Arctic, only members of the A.
guttata and C. sphaericus species groups may remain,
with shifts in dominance between the two (e.g.,
Nevalainen et al., 2011). Hofmann (2003) showed that
during extreme cold periods in Europe, the dominant
chydorid assemblages that survived in alpine lakes,
consisted only of a few species (including A. guttata) of
which A. affinis, A. excisa, A. nana, C. sphaericus, and
A. harpae were the five most frequent (at Gerzensee,
Switzerland). Of the few chydorids that survived under
these extreme conditions, populations or closely
derived forms (of A. guttata, A. excisa, A. nana, C.
sphaericus, and A. affinis) are found today in Lake
Mahoma in the Rwenzori. During Glacial periods in
the Pleistocene, these were the most common species
in temperate zones and therefore the chances for
recruitment were also relatively higher than at present.
In temperate lakes in Europe, these species were
replaced by a wider diversity of chydorids as soon as
temperatures went up (Hofmann, 2003). Stenothermic,
warmth-adapted Chydoridae common in East African
lowlands (like Dunhevedia, Ephemeroporus, Leberis,
Karualona, Anthalona, Chydorus parvus, and Alona
cambouei) cannot survive under such conditions.
Second, diverse macrophyte stands are poorly devel-
oped (to absent) in most Rwenzori lakes above
4000 m, limiting opportunities for phytophilous
groups such as chydorids. Third, the majority of sites
are highly dilute (\60 lS/cm) and acidic (mild to
strong; pH range 4.30–6.69). Relatively few animals,
Cladocera included, tolerate pH levels below ca. 5.7
due to osmotic stress and in dilute acidic waters, uptake
of ions against steep concentration gradients like Na?
becomes problematic (Fryer, 1993), the composition of
chydorids markedly changes with pH (Krause-Dellin
& Steinberg, 1986; Fryer, 1993). The remaining
species are well adapted to these conditions. Fourth,
the Rwenzori are geologically young and the majority
of lakes considered in our study were formed only in
the Holocene (see below), so any possible in situ
speciation should be considered within this short time
range, which is very short for Cladocera. Finally,
suggested by Loffler (1968c), an impoverished crus-
tacean fauna in the Rwenzori could be attributed to the
low abundance of migrating waterfowl, limiting the
possibility of zoochorous dispersal and colonization
from lower altitudes as well as inter-lake dispersal (see
further). For example, passive dispersal is higher in the
Andes than in East Africa, with only about three
species of waterfowl in the latter and over twenty in the
former (Loffler, 1968c).
Influence of abiotic (local) and dispersal-related
(spatial) factors
Local processes (such as abiotic factors, predation and
competition) and spatial configuration of lakes (taking
Hydrobiologia (2011) 676:57–100 85
123
dispersal pathways into account) play a role in shaping
aquatic communities (Leibold et al., 2004; Leibold &
Norberg, 2004). The importance of abiotic factors is
illustrated here in the ordination plots (Fig. 9), which
show that the Cladocera communities of brown-water,
acidic lakes and surrounding swamps (2990–4054 m;
Group II lakes) differ from those in the (ultra-)
oligotrophic clear-water lakes of the Alpine zone
(3890–4487 m; Group I lakes). Most Rwenzori lakes
are simply too species-poor in cladocerans and the
conditions too extreme to speak of extensive commu-
nities. Most sites are characterized by one to two
species only.
Cladoceran diversity typically declines with altitude
(Rautio, 1988) and with an increase of pH (Krause-
Dellin & Steinberg, 1986) and no more than 1–4 species
per site should be expected at altitudes above 3200 m
(Patalas, 1964). In a comparison of four lakes in the
Alps, Hofmann (2000) noted that the most distinct loss
of cladoceran diversity occurred at 1500 m, the highest
loss at 2290 m. In the Rwenzori, between ca. 3000 and
4000 m, the number of species drops from eight
(Mahoma, 2990 m) to four-two species (e.g., three
species in Nsuranja, 3718 m). Higher up in the Rwenz-
ori, lakes sustain little more than the ubiquitous C. cf.
sphaericus: it is the only cladoceran that remains in most
localities above ca. 4020 m. In fact, Group I lakes,
except for Lake Bujuku, hold only Chydorus cf.
sphaericus, whereas Group II lakes are characterized
by at least one more species, A. guttata.
Several factors are known to structure Cladocera
communities (e.g., macrophytes: Declerck et al., 2005;
DOC: Siebeck 1978; nutrients: Bos & Cumming,
2003; temperature: Bottrell, 1975; pH: De Sellas et al.,
2008). Shifts in abundances between C. sphaericus
and A. guttata in mountain lakes typically occur with
changes in temperature and complexity of the littoral
(Hofmann, 2000; Duigan & Birks, 2000; Manca &
Comoli, 2004). In the high Arctic (Svaldbard Archi-
pelago), Nevalainen et al. (2011) showed that the
presence of aquatic mosses and high organic content
tilts the balance toward the A. guttata group, which
disappeared completely as soon as the lake produc-
tivity dropped and was replaced after the early
Holocene by C. sphaericus type (as the only remaining
species, even today). The presence of A. guttata in the
Rwenzori is related to the relatively higher complexity
of the littoral zone, higher temperatures, higher
nutrient content, and lower average pH (due to higher
DOC) and can thus serve as a local indicator species
for such conditions. Therefore, not only altitude and
temperature regime structure the cladoceran commu-
nities in the Rwenzori—also lake characteristics play
a role. This is well known in other studies of
cladoceran communities in mountain lakes and should
be taken into consideration when using them as
indicators for temperature change (e.g., Lotter et al.,
1997; Kamenik et al., 2007). Altitudinal distribution
does not always coincide with their classification
according to cold tolerance (see Harmsworth, 1968) as
cladoceran community responses to temperature
changes are not always predictable (Lotter et al.,
1997; Hofmann, 2000; Duigan & Birks, 2000). In the
Rwenzori, A. guttata occurs higher up than A. excisa,
although according to the latitudinal temperature
classification by Harmsworth (1968), the opposite
would be expected. It is clear that temperature alone is
insufficient to explain the local cladoceran altitudinal
distribution and the community shifts between the
Rwenzori and Mount Kenya, with different relative
abundances and altitudinal distributions for example
of A. excisa, A. guttata, and A. affinis barbata—local
and spatial factors should be taken into account.
Two Rwenzori lakes have markedly different com-
munities. Lake Mahoma and Lake Bujuku are charac-
terized by species restricted to these lakes (Lake
Mahoma: A. affinis barbata, A. intermedia, Alonella
exisa, A. nana, Daphnia cf. obtusa, P. aduncus; Lake
Bujuku: D. cf. curvirostris, P. aduncus) besides the
locally widespread A. guttata and C. cf. sphaericus. The
presence of two different Daphnia species is striking.
The genus is rare in the tropics compared to temperate
regions and bound to higher altitudes in Africa
(Dumont, 1994; Green, 1995; Mergeay et al., 2005).
In tropical Africa only few species are known to occur
from around 3000 m or higher (Loffler, 1968b, 1984;
Green, 1995): D. pulex, D. ‘‘obtusa’’, D. dolichocep-
hala, D. magna, D. curvirostris and D. izpodvala
(Kotov & Taylor, 2010). As mentioned earlier, care
should be taken in regarding these as conspecific with
Palaearctic populations—the primary reason being low
taxonomical resolution, a persistent problem (Kotov &
Taylor, 2010). The restricted occurrence of Daphnia
species within an extensive mountain range to one or
just a few lakes has been reported before (Petrusek
et al., 2007; Nilssen et al., 2007).
Why do communities in Lake Mahoma and Lake
Bujuku differ? We propose a few (not mutually
86 Hydrobiologia (2011) 676:57–100
123
exclusive) possibilities. (1) Lake Mahoma is the only
lake in the Rwenzori at ca. 3000 m elevation, the
lowest in this study. It experiences significantly
warmer temperatures than the lakes in the alpine and
nival zones (MATemp of 10.0�C versus an average of
3.6�C in the other sites). Its littoral habitat is more
complex, with various substrate (sandy, rocky and
muddy bottoms) and macrophytes (submerged, emer-
gent and floating) (Eggermont et al., 2007), providing
a variety of niches which can sustain larger chydorid
communities (Whiteside & Harmsworth, 1967). More
algae are present in Mahoma when compared to the
other lakes (‘greenish color’ in Eggermont et al., 2007)
promoting phytoplankton grazers like Daphnia. These
factors might explain the relatively more diverse
cladocera composition of Lake Mahoma, but cannot
explain the peculiar community of Lake Bujuku,
lacking a well-developed littoral zone and being
significantly higher (at 3891 m), thus colder.
(2) Geographical location may play a role. For
example, Loffler (1968b) noted striking differences in
freshwater crustacean species composition on Mount
Kenya between lakes on the western and the eastern
side and attributed this to cloudiness and direct solar
radiation. Most probably, microclimatic conditions
can not fully account for the additional species in
Mahoma and Bujuku. More important could be the
direct accessibility, in other words the relatively lower
degree of isolation of these lakes, and hence higher
chance to be visited by migratory birds when
compared to other Rwenzori lakes. Lake Mahoma
and Bujuku are both located in the eastern part of the
range and accessible through the Mubuku-Bujuku
river valley, whereas all other sites but one (Lake
Bukurungu), are surrounded by peaks and/or high
mountain ridges which may constitute efficient barri-
ers for dispersal agents. To the east of the Rwenzori
range lie Mount Kenya and Mount Kilimanjaro,
therefore exchange of species between these mountain
areas is not unlikely (for example, A. excisa is very
common on Mount Kenya, and absent in the Rwenzori
except for Lake Mahoma). During all our visits to
Lake Mahoma (four; 2005–2009), we noted the
African black duck Anas sparsa, which indicates that
this lake can be frequented by waterfowl, perhaps
relatively more often, compared to other lakes, and
that therefore, the input from zoochorous dispersal
could be significantly higher. The aquatic mollusc
Pisidium, present in Lakes Mahoma and Bujuku, is
also known to be distributed by waterfowl (Malone,
1964; Rees, 1965); during our campaigns, Pisidium
was absent from all Rwenzori lakes except for
Mahoma, Bujuku and Lower Kachope. Also Hemip-
tera occur only in Lakes Mahoma and Bujuku. There is
one other lake located in this eastern portion of the
Rwenzori (Lake Bukurungu), but it is isolated by
mountain ridges in the north (including Mt Gessi) and
east (Portal Peaks); the cladoceran species composi-
tion here consists of C. cf. sphaericus and A. guttata
only.
(3) Age (origin) of lake basins is also an important
factor determining the distribution of Cladocera as it
relates to the timing and possible duration of invasion.
Most Rwenzori lakes were formed by glacial activity,
i.e., they were created after a glacial valley was
dammed by terminal or recessional moraines, or they
occupy glacially scoured basins. During the Last
Glacial Maximum (LGM, 21 kyears BP), the local
snowline extended down to 3000 m (Mahaney, 1989).
Since most lakes are located above 3700 m, they are
likely of Holocene age (e.g., Lower Kitandara formed
at *7530 BP; Livingstone, 1967), and hence could
not be invaded earlier. At least some of the lake basins
were formed after glacier retreat following the Little
Ice Age (de Heinzelin, 1962) or even more recent (i.e.,
*60 years or less; Osmaston, 2006), their basin
exposed by recent glacier recession (e.g., Lake
Ruhandika at the foot of Speke glacier and Lake Irene
below Speke glacier). As regards origin, Lake Maho-
ma, at 2990 m located within the LGM terminal
moraine, is extraordinary in that its size, shape and
depth suggest that its basin was formed after the
thawing of a block of ice that detached from the
retreating glacier (i.e., a kettle lake; Wetzel, 2001) at
least *17,900 years ago (Livingstone, 1967). In this
respect, Lake Mahoma is unique in the tropics
(Loffler, 1968c). Most of the lakes at some distance
from the central peaks (e.g., Kachope lakes, Lake
Katunda, Kopello), would date somewhere between
the older Mahoma and Lower Kitandara, assuming
that the high central peaks could support a large
glacier system longer than the lower peaks (James
Russell, personal communication). The relatively
older age of Mahoma and the fact that it was formed
at the border of a terminal moraine (thus able to be
directly colonized from nearby freshwater habitats at
the time), might contribute to its peculiar species
composition. However, most of its species could not
Hydrobiologia (2011) 676:57–100 87
123
establish in other Rwenzori lakes. This is possibly due
to a combination of generally low accessibility of
migratory birds for most Rwenzori lakes, the hostile
habitat conditions at higher elevations discussed
earlier, and perhaps high competition with locally
adapted populations of Chydorus cf. sphaericus and
A. guttata in the limited littoral (‘‘Monopolization
Hypothesis’’; De Meester et al., 2002). Lake Bujuku
was not formed by glacial activity, but from damming
by a landslide down the slope of Mt. Baker in the last
millennium (Livingstone, 1967). The fact that it holds
Daphnia cf. curvirostris, suggests a recent invasion,
perhaps even from the African lowlands (D. curviros-
tris occurred briefly in East African lowland lakes in
1940–1955; Harding, 1957; Mergeay et al., 2004,
2005).
Biogeography of the Rwenzori Cladocera
Taxonomic uncertainties and the lack of basic surveys
of the African Cladocera fauna, the Afromontane
species in particular, complicate biogeographical
assessments. Based on inventories from Mount Kili-
manjaro, Mount Kenya, Mount Elgon and Rwenzori,
Loffler (1968b) distinguished six biogeographical
distribution patterns for the aquatic Crustacea of the
East African mountains based on 33 copepod, 24
ostracod, 13 Cladocera, and one Anostraca species: (1)
Cosmopolitan species (11.3%); (2) Tropical euryther-
mic species, occurring at all elevations in the tropics
(32.4%); (3) Tropical stenothermic species, restricted
to high-elevation sites in tropics (39.4%); (4) Extra-
tropical species from the northern and southern
hemisphere (4.2%); (5) Extratropical species from
the northern hemisphere (8.5%); and (6) Extratropical
species from the southern hemisphere (4.2%).
An assignment of the Rwenzori species to each of
these groups is not straightforward and Loffler’s
biogeographical patterns should be re-examined tak-
ing taxonomical insights since 1970 into consider-
ation. It is uncertain if true cosmopolitan Cladocera
species even exist (Frey, 1987; Xu et al., 2009) and
molecular data now confirms how common regional-
ism is in this group (e.g., C. sphaericus complex,
Belyaeva & Taylor, 2009; Daphnia obtusa complex:
Kotov & Taylor, 2010; etc.)—the latter is not surpris-
ing, as non-cosmopolitanism, continental endemism
and cryptic speciation in the Cladocera have been
shown extensively by Frey over 30 years ago (1980;
1986; 1987) based on morphology—molecular studies
in the cladocerans sometimes ‘rediscover’ Frey’s
widely accepted hypotheses on non-cosmopolitanism
that can be applied to any widespread cladoceran
species group. A truly surprising find would be a real
cosmopolitan cladoceran species.
Whereas a significant proportion of species in
Loffler’s assignment (32.4%) are tropical eurytherms
occurring at all elevations, this is not obvious in the
Rwenzori Cladocera, save perhaps in Ilyocryptus cf.
gouldeni, unrelated to other afromontane Ilyocryptus
species described from southern Africa by Kotov &
Stifter (2005). Instead, the Rwenzori Cladocera fauna
lacks an afrotropical character but holds a significant
extratropical component.
All of the recorded species can be attributed to
species complexes that are cosmopolitan or cold-
temperate/boreal and widespread in the northern
hemisphere. Several are typical for higher latitudes
and were the dominant species during colder periods
in temperate lakes (see earlier). The Rwenzori popu-
lations can be considered as conspecific with, or very
closely related to, species from the northern latitudes.
For most species, closest relatives are extremely rare
to absent in tropical lowland Africa. Conspecificity of
several species is unclear until detailed group revi-
sions are made. A. intermedia, P. aduncus, and
A. nana are three examples of Palaearctic elements
in the Rwenzori Mountains, extremely rare in sur-
rounding lowlands and not found (yet) on other
African mountains. These three chydorids have also
been suggested as true Palaearctic elements in South-
ern Africa (Smirnov, 2008). Additional candidates for
extratropical Palaearctic forms are A. excisa, A. gut-
tata, Chydorus cf. sphaericus, D. cf. curvirostris and
Daphnia cf. obtusa, all close to populations in the
northern hemisphere and extremely rare in the African
lowlands. Biogeographically, A. excisa, A. guttata and
C. cf. sphaericus are interesting, as they are present on
the nearby sky island Mount Kenya (Loffler, 1968b). If
more endemics would be revealed in the future, there
is no doubt that these can be considered of Palaearctic
origin. Morphology might indicate a possible onset of
speciation in at least two species (C. cf. sphaericus and
D. cf. obtusa). Isolation and speciation is distinctly
present in A. affinis barbata or A. barbata, which
might be a true Afromontane endemic that now occurs
in Mount Elgon, Mount Kenya, Rwenzori and—if A.
martensi would turn out to be a junior synonym—the
88 Hydrobiologia (2011) 676:57–100
123
Drakensberg. Belonging to the A. affinis-group, a
species complex that is virtually absent in the African
lowlands, the (sub)species A.barbata and the nearly
identical A. martensi (whether a synonym or not), are
clearly different from the Palaearctic stock, not simply
a variety as Sinev (1997) suggested. Finally, A.
sphagnophila n.sp. and D. cf. curvirostris, belong to
species groups that are nearly absent from African
lowlands and are not known from other African
mountain localities. Although A. sphagnophila n.sp.
has not yet been recorded from other African moun-
tains, it is not certain if this is a local Rwenzori
endemic. Its preferred habitat (Spagnum–Carex
swamps) occurs on several East African mountains.
However, because of the more humid conditions in the
Rwenzori compared to the other mountains, the Carex
fens in the Rwenzori are almost constantly flooded
(Rejmankova & Rejmanek, 1995), which constitutes
ideal habitat conditions, not present in other mountains
of the EASIC.
We may consider the species composition of the
Rwenzori Cladocera fauna a result of recruitment from
temperate regions. Presence of Palaearctic elements
into Southern Africa complicates tracing the exact
origin of the Rwenzori Cladocera (north or south). The
fauna has an overall Palaearctic character, resulting
from immigration rather than in situ evolution. Lake
Mahoma harbors a chydorid community that is typical
for an acid boreal lake, albeit an impoverished one (see
below), or of a temperate lake during periods of
extreme cold in Europe (e.g., Younger Dryas; Hof-
mann, 2003). The question is now whether Lake
Mahoma is a Pleistocene refuge or can still be actively
colonized (e.g., by P. aduncus) and if so—from
where. As for most island faunas, in this case sky
islands, species composition in the Rwenzori is
unpredictable. Island faunas depend on chance and
founder effects (Boileau et al., 1992). However, it is
clear that the area of recruitment for these animals is
from temperate/boreal zones, not from tropical low-
land areas. We can expect a similar scenario for Mount
Kenya. Palaearctic–Afrotropical disjunctions are well
known in Cladocera, but have only recently gained
attention. Boreal cladoceran ‘freshwater pockets’ in
Africa are now known from three regions: (i) West
African tropical rainforests. In West Africa, Chiamb-
eng & Dumont (2005) suggested eight boreal species
in rainforests in Cameroon, among which a typical
northern hemisphere chydorid species, Monospilus
dispar. Chiambeng et al. (2006) report several addi-
tional Palaearctic species from the rain forests in
Cameroon, among which true A. affinis and A. inter-
media. Occurrences such as Monospilus are rare, with
very few specimens mentioned in each report, sug-
gesting relict populations (Chiambeng & Dumont,
2005). (ii) South African lowlands. In South Africa,
Hart & Dumont (2006) reported Lathonura, a strictly
Holarctic genus, from the Okavango Delta and
Smirnov (2008) listed 18 Palaearctic species in the
South African cladoceran fauna, of a total of 112
(16%), with low frequencies of occurrence (e.g.,
Megafenestra aurita, A. nana). Ecological conditions
are unsuitable for these temperate species when
entering tropical waters, for example due to predation
pressure (Hart & Dumont, 2006. (iii) the East African
Mountains (Loffler, 1968b; this study). We can now
confirm boreal elements (or closely derived forms) in
the Cladocera fauna of the EASIC.
The Rwenzori populations attributed to C. cf.
sphaericus or even Daphnia cf. obtusa could well
belong to separate species, following future revisions.
Considering the high cryptic diversity in these groups,
a certain degree of isolation is even likely, but such
designations will not change the interpretation of the
data presented here. For most Rwenzori species, the
phenotypically closest relatives are all rare to absent in
the African lowlands, but most common in northern
temperate zones. Morphological differences with
representatives of the northern temperate zone, if
present, are mostly subtle and speciation can be
considered relatively recent in terms of Cladoceran
evolution, which is well accepted as an old group
characterized by morphological stasis. Over a hundred
thousand years is considered not a significant time at
all for morphological divergence in the Cladocera
(Frey, 1962). Isolation in the Andes, in contrast, is
much older and has led to a strong morphological
divergence of Cladocera from their lowland relatives,
even leading to an endemic chydorid genus and
several endemic species (Kotov et al., 2010). Loffler’s
(1984) hypothesis that tropical high-mountain crusta-
cean fauna in East Africa is comparable in endemism
to South American and Asian mountains, is hereby
rejected for the Rwenzori Mountains. Recruitment of
the Andes was likely from lowland refuge areas in
Patagonia and Cladocera speciation likely took place
before colonization of the high-altitude aquatic hab-
itats; some relicts are thought to have a Mesozoic
Hydrobiologia (2011) 676:57–100 89
123
signature (Mergeay et al., 2008; Kotov et al., 2010) .
Of the 19 species from ten waterbodies found in the
Andes, Kotov et al. (2010) concluded that half are
endemic species with significant morphological diver-
gence. In fact, even temporary high-altitude peatlands
in the South American Cordillera, hold unusually high
cladoceran diversities for high-altitude sites, the
Andes being a biodiversity hotspot (Coronel et al.,
2007). This is in sheer contrast with our finding—we
counted 11 species from 29 waterbodies and few
endemics of low morphological divergence. The
diversity, as well as the local speciation, as far as
can be derived from morphology, is clearly lower in
the Rwenzori. We are of course uncertain of the
genetic divergence of the Rwenzori populations from
Palaearctic stocks, which is not completely expressed
in the phenotype. But we are certain that a different
colonization scenario should be considered for the
aquatic microcrustaceans of the EASIC in comparison
to the South American Cordillera, a comparison that
intrigued Loffler (1964, 1968c).
The recruitment of taxa of the African mountains
from temperate zones is well studied in other groups.
In the afromontane flora, 80% is endemic at the
species level and 13% is north-temperate in origin;
among the endemics, Tertiary relicts as well as recent
immigrants (500–100 k.y.) are considered (Hedberg,
1969; Koch et al., 2006; Assefa et al., 2007). For the
genera Arabis, Lychnis, Carex, Ranunculus and
Alchemilla, the Holarctic is considered the most
important source for the cool-adapted African high-
mountain floras, where speciation and even radiation
have taken place (Assefa et al., 2007; Popp et al., 2008;
Gehrke & Linder, 2009). Our finding of common,
widespread Palaearctic taxa or closely related forms of
A. excisa, A. nana, A. guttata, A. intermedia, A.
rustica, Chydorus sphaericus, Daphnia obtusa and
D. curvirostris, all extremely rare in the African
lowlands, shows that the penetration of temperate
freshwater elements into the EASIC has occurred.
Ilyocryptus cf. gouldeni seems surprising as its closest
relative is a typical North American taxon—its
presence in the Rwenzori agrees with biogeographical
patterns in plant taxa, where disjunctions with North
America are not uncommon (Gehrke & Linder, 2009).
Whereas colonization from northern temperate zones
is likely for most species, we should also consider the
presence of perhaps a true Afromontane endemic A.
barbata (reaching as far as the Drakensberg
Mountains, if A. martensi would appear a junior
synonym) that might form a small barbata-subcom-
plex within the A. affinis group; local endemism is
possible, with A. sphagnophila n.sp., a species which
shows sufficiently strong morphological divergence
from Palaearctic populations to consider it a separate
taxon, although the species group is typical for the
north temperate zone. Whether original colonization
pre-dates the Pleistocene is unclear, but the level of
speciation in the Rwenzori Cladocera, as far as can be
estimated from morphological divergence and taxon
uniqueness, is low compared to the situation in the
Andes. Isolation of the Rwenzori Cladocera has not
been sufficiently strong (and long) for deep morpho-
logical divergences.
Several authors (e.g., Osmaston, 1998) suggested
that the endemism in the Afroalpine zones may not
have been a steady adaptive response to the environ-
ment, but instead resulted from glacial cycles that
repeatedly expanded and compressed, allowing rapid
expansion and speciation for the stressed Afroalpine
populations. More recently, this ‘‘species pump’’
model of diversification in sky islands, driven by
Pleistocene glacial cycles, is being reconsidered (Mc-
Cormack et al., 2009). Separation of endemic cladoc-
eran lineages in some of the African Mountains took
definitely place before the Pleistocene, as in the
Ethiopian Bale Mountain endemic Daphnia (Kotov
& Taylor, 2010), or perhaps in the Afromontane
A. affinis barbata, but it is unlikely in the young
Rwenzori. The two Daphnia populations in the
Rwenzori do not show a level of divergence (as D.
izpodvala). For example, the Rwenzori D. cf. obtusa
lacks the ocular dome of D. izpodvala and is not
pigmented in contrast to the latter, and generally more
similar in morphology to the Palaearctic, true D.
obtusa. We find no endemics of a comparable level of
divergence as the Bale Daphnia, in the Rwenzori.
Extratropical montane elements, in this case Palaearc-
tic forms, could either be glacial relicts that survived in
suitable habitats during the Pleistocene (Hewitt, 1996,
2000, 2004), or they could still be continuously
supplied from the north (Europe) and south (South
Africa) via suitable stepping stones and/or bird flyways
between Europe and Africa. The mean annual temper-
ature during Pleistocene glaciations in the East African
Mountains was lower by 5 to 6�C (Porter, 2001) and
snowlines were pushed down by 570–1000 m (Kaser
& Osmaston, 2002) relative to the present. Vegetation
90 Hydrobiologia (2011) 676:57–100
123
belts shifted downslope, extending the afroalpine and
ericaceous zone to 1000–1500 m lower than today, to
ca. 3200 m altitude (Mahaney, 1989; Gottelli et al.,
2004), therefore occupying much larger areas. For
example, the extensive Carex–Sphagnum bogs, the
habitat of A. sphagnophila n.sp., can be considered old
and its occurrence has been more continuous, covering
larger areas through time compared to the lake sites,
allowing these habitats to function as important refuge
habitats for acid-tolerant cladoceran species. Only
when including the entire faunal transition zone of
which the lower boundary may have reached to ca.
2200 m, chances for dispersal increased between the
individual mountain ranges and the northern hemi-
sphere. Highlands at that elevation now lie scattered
throughout the East African region and stepping stones
might have occurred both among the eastern (Mount
Elgon, Mount Meru) and western (Rwenzori, Virunga)
mountains flanking the Rift, and the three Ethiopian
massifs to the North (e.g., vegetation belts; Assefa
et al., 2007). The idea that north–south aligned
mountain ranges form climatic bridges from high to
low latitudes for aquatic faunas, a ‘climatic highway’
in South America yet fragmented into sky archipelagos
in Africa, is not new, elegantly formulated by Loffler
(1968c, 1984). Individual afroalpine lakes are ephem-
eral on geological time scales; during Quaternary ice
ages, most of their basins have repeatedly been
occupied by glaciers, and water balance may not
always have been positive enough to fill them (the
Afrotropics were cooler and drier during glaciations,
e.g., Bonnefille et al., 1990). The occurrence of
permanent open waterbodies within the altitudinal
range of suitable abiotic conditions, would have been
(and still is) a limiting factor for dispersal of some
freshwater taxa (e.g., Eggermont & Verschuren, 2007
on chironomids). However, the presence of permanent
open-water lakes is not a necessary condition for the
survival of aquatic biota such as Cladocera, which may
as easily (or even better) thrive in small shallow waters
and marshes, temporary as well as permanent, as long
as the conditions are there for their arrival and survival.
Despite a long-term instability of cold-water habitats in
the tropics, the existence of a suitable climate fresh-
water corridor (we could tentatively call it here
‘‘Loffler’s bridge’’, after his analogy with mountains
as climatic bridges for freshwater habitats; see Loffler,
1984) connecting northern and southern temperate
regions in Africa during the Pleistocene, is possible.
Such a corridor should have been strongly frag-
mented during interglacials, as is presently the case—
leaving suitable habitats, like the unique Lake Maho-
ma, the oldest of the Rwenzori lakes, as refuge as well
as possible stepping stone. In honor of H. Loffler, who
spent decades studying the limnology of high mountain
lakes, we tentatively introduce a term for such high-
altitude cold-water islands in the tropics: Loffler
Islands. The definition is as follows. A Loffler Island
is a cold-water (i.e. water generally below 10�C)
freshwater habitat, situated at high altitudes between
the Tropic of Cancer and the Tropic of Capricorn. As
Loffler studied mainly lakes at altitudinal zones above
the ericaceous belt (3200 m up), corresponding to von
Humboldt’s Tierra helada and Tierra fria (Loffler,
1984), this altitude could serve the definition of high-
altitude waters in the strictest sense. However, it should
not be seen as a strict rule, as this is a biogeographical
term and not purely geographical. Suitable habitats for
cold-water species to survive in tropical freshwater
pockets, are found at lower heights, as the exact lower
margin of Loffler Islands will depend on local climatic
conditions, a subject which needs further investigation.
Temperatures of such cold-water islands in the tropical
belt should be low, with an annual average of 10�C or
lower. Lake Mahoma in the Rwenzori, which is an
unmistakable example of a Loffler Island, is situated at
ca. 3000 m. More important, a Loffler Island should
harbor a significant extra-tropical component in its
freshwater fauna.
Loffler (1968c) suggested that regardless of when
insular populations in the East African Mountain lakes
may have become established, they must now be
isolated, assuming that no means of dispersal and no
climatic corridor of stepping stones exists in modern
times. Compared to the other East African mountain
ranges, the Rwenzori is indeed poor in migratory birds
yet not completely devoid of them (Loffler, 1964,
1968c). Birds could still serve as potential dispersal
agents for Cladocera. The fact that lakes in the Rift,
particularly those located above 1200 m, may sporad-
ically hold cold-tolerant Cladocera taxa of Palaearctic
origin (e.g., P. aduncus, A. guttata; Rumes, 2010;
Daphnia curvirostris; Mergeay et al., 2004, 2005) may
suggest that these lakes can serve as temporary
stepping stones, at least for some species, until they
disappear again through competition and predation.
Lake Mahoma, the only lake below 3700 m asl in our
study, may function as an active ‘relay station’.
Hydrobiologia (2011) 676:57–100 91
123
Colonization attempts of temperate taxa might even
happen frequently (i.e., populations may briefly form),
but since healthy populations can only form when
founders can adapt well to the local conditions and can
compete with present populations that occupy the
existing niches (e.g., De Meester et al., 2002), species
may not always become established and significant
eggbanks are not always formed. As several (five!) of
the Cladocera species, we found here were not
recovered in Lake Mahoma by Loffler (1968b) in the
sixties (see below), recruitment from temperate zones
or nearby stepping stones, such as Mount Kenya or
further south, from South Africa, could be an ongoing
process. A. affinis barbata in this lake may well have
derived from Mount Kenya or Mount Elgon, where the
species is common, and ongoing dispersal between
Loffler Islands of the EASIC could be equally possible
for A. excisa and for C. cf. sphaericus, which
complicates tracing their origin.
The conditions of Lake Mahoma are favorable for
the survival of cold-adapted Cladocera that occur in
temperate zones. The altitude at which this lake is
found (2990 m), is not too high (no extreme climatic
conditions of the alpine lakes that leads to stronger
reduction of diversity) and not too low (no competition
with afrotropical taxa) and it has a well-developed
littoral. As predation is an important limiting factor for
cold-water Cladocera to survive in the tropics (Hart &
Dumont, 2006), the absence of fish in the Rwenzori is
a plus. Present-day freshwater habitats in tropical
Africa between roughly 2000–3000 m, could still be
used by temperate cladoceran species as stepping
stones, given that the abiotic and biotic conditions are
favorable for their survival, a viable eggbank is
formed and localities are accessible to dispersal
agents. Within this altitudinal range, conditions higher
up the mountain slopes might be better in terms of
biotic factors (colder so less predation and competition
from tropical taxa), but abiotic conditions become
harsher, so only the toughest, best adapted (cold- and
acido-tolerant) species survive. For the chydorids, the
same species (or the original stocks for the Rwenzori
populations) were dominant in temperate lakes during
Quaternary cold periods (see above). C. sphaericus
became a dominant species, declining in abundance
and replaced by species with more specific character-
istics, depending on the littoral development of lakes
(e.g., development of Sphagnum stands; Duigan &
Birks, 2000), including those at higher altitudes.
Locally common species like C. cf. sphaericus
and A. guttata show that dispersal of chydorids
within the Rwenzori is possible (and perhaps aided
by humans along the trekking routes up the moun-
tains). C. cf. sphaericus has colonized all freshwater
habitats in the range, including pools at 4570 m, at
the foot of glaciers of Mount Stanley. Daphnia does
not occur in the Rwenzori besides Lakes Mahoma
and Bujuku and few Cladocera survive in our study
area above 4020 m except for C. cf. sphaericus.
Eggbanks, vital to the dispersal in Cladocera, may
not be formed for all species. Daphnia ephippia
occur in the sediments of Lake Mahoma (Loffler,
1968b, and own observations) yet lack in Bujuku. In
this respect, the populations in Bujuku might show
an analogy with Daphnia in arctic regions, where
obligate parthenogenesis is an important life history
strategy in diploid-polyploid Daphnia (e.g., Weider,
1987; Hebert & McWalter, 1983) yet life history
strategies and polyploidy in the Afromontane Daph-
nia has not been studied yet. Although Daphnia cf.
curvirostris has colonized Lake Bujuku somewhere
in the last millennium and current conditions allow
a population to survive for half a century at least,
the animals are unable to disperse from here if no
eggbank is present. Gamogenetic populations and/or
ephippia in the Rwenzori lakes are known from two
occasions only (D. cf. obtusa in Mahoma and C. cf.
sphaericus in Lake Nsuranja). We did not find
A. excisa out of Lake Mahoma in the Rwenzori,
although this species is very common in Mount
Kenya and Mount Elgon and locally abundant in
Mahoma.
Did aquatic communities in the Rwenzori change
since 1961?
Loffler (1968b) mentions samples from five localities
in the Rwenzori: Lake Mahoma, a Sphagnum-bog near
Mahoma, Lake Bujuku, Lake Irene and a rock pool
nearby, taken between 14 and 19 January 1961. In the
author’s study, live specimens of A. excisa, A. nana,
A. guttata, A. intermedia and P. aduncus were all
absent in the Rwenzori. In our samples of 2005–2009,
these five species are present and make up 42% of the
total current cladoceran richness in Lake Mahoma.
P. aduncus and A. guttata were not found by Loffler in
Lake Bujuku in 1961 and the author reports
C. sphaericus from two (unspecified) out of five
92 Hydrobiologia (2011) 676:57–100
123
Rwenzori sites he investigated (Loffler, 1968b), in
contrast to our finding of the species in at least three of
these sites (very abundant in Mahoma, Bujuku and
Irene). Loffler (1968b), who also looked for cladoc-
eran remains in the top sediments of these sites, found
only a single (!) carapace of A. guttata in Mahoma, a
species that we found common in both Mahoma and
Bujuku, well represented now by both live specimens
in the littoral as well as carapaces in the top sediment.
Did Loffler miss these chydorids? Seasonal variability
is insufficient to explain the absence of the species in
1961. Loffler’s samples were collected in the dry
season (January). This period was covered during at
least three sampling campaigns between 2005 and
2009 in the current study and relative abundances of
the chydorids were actually higher during this season.
Relative abundances and sampling intensity can play a
role, yet Loffler found the littoral species A. ‘‘affinis’’,
which is extremely rare in all our samples (we found
only two specimens; listed as A. affinis barbata),
whereas he did not record A. excisa, A. guttata and
A. intermedia which were abundant in our samples
and the carapaces are very abundant (hence Loffler
would have seen them in the sediments).
Are we witnessing changes in Cladocera com-
munities of the Rwenzori lakes over 44–48 years?
Sampling bias and stochastic shifts are likely, yet
actual ecosystem changes should not be excluded.
The Rwenzori lakes are sensitive to climate change
(Eggermont et al., 2007, 2010b), e.g., a temperature
rise in East Africa of 0.6�C occurred since 1901
(Cullen et al., 2006). Situated at lower altitude,
zooplankton communities of Lake Mahoma may be
relatively more susceptible to the environmental
changes of the past few decades. These species may
have become more abundant and competitively
stronger as the current conditions (i.e., increased
water temperatures and productivity/nutrient con-
tent) better coincide with their ecological/habitat
preferences. As shown in the RDA analysis, the
Rwenzori populations of A. guttata are indicative for
relatively higher water temperatures and nutrient
contents. Such species-specific characteristics play
an important role in local rarity versus abundance of
cladocerans (see the ‘‘rarity concept’’ in Hessen &
Walseng, 2008). Changes in the cladoceran com-
munity, if really present, apparently concern chy-
dorids only, which leave well-recognizable remains
(carapace, headshields) in lake sediments. Downcore
sediment analysis can provide a definite answer
whether these species were overlooked in 1961, and
whether Lake Mahoma was recently colonized by
any of the new records, or if these species derive
from a dormant seedbank. The two known Daphnia
populations in the Rwenzori have definitely per-
sisted in Lake Mahoma and Lake Bujuku since 1961
and remain restricted to these two localities.
Conclusions
(1) The Cladocera fauna of the Rwenzori Mountains
is characterized by (i) low endemism, (ii) low
diversity, and (iii) extratropical temperate ele-
ments. The fauna has an overall Palaearctic
character and includes at least one Afromontane
taxon (A. affinis barbata or A. barbata) and a
new species (A. sphagnophila n.sp.), the latter
from high altitude Carex/Sphagnum bogs. Both
these species derived from species groups that
are common in temperate regions yet virtually
absent in African lowlands, which is typical for
the Rwenzori Cladoceran fauna. Other species
could be candidates for separation (or assign-
ment under forgotten names) pending species
group revisions, e.g., in the genera Daphnia,
Ilyocryptus, Chydorus; yet, morphological diver-
gence is very low. D. cf. obtusa from the
Rwenzori is not closest to the Ethiopian moun-
tain endemic of its species cluster and not as
diverged in morphology, therefore speciation in
the Ethiopian highlands has occurred indepen-
dently from the East African Mountains. Based
on the phenotypes, Rwenzori Cladocera diver-
sity and endemism appear lower than in the
recently well-revised Cladocera fauna of the
South American Andes.
(2) We found 11 species of Cladocera, comparable
to the recorded diversity on Mount Kenya (12
species). Seven species are new records for the
Rwenzori and five of them occur in Lake
Mahoma. The new findings in Mahoma could
result from sampling bias or might indicate
actual changes in faunal composition over the
last 40–50 years. The two Daphnia populations
in the Rwenzori have been present since 1961
and are restricted to these localities.
Hydrobiologia (2011) 676:57–100 93
123
(3) Whereas C. cf. sphaericus is the only species in
alpine and nival lakes above 4020 m (group I),
the more acid, brown-water lakes (group II) at
lower altitude additionally contain A. guttata.
The apparent preference of A.guttata for rela-
tively higher water temperatures, higher nutrient
conditions and DOC content suggests that future
climate change (warming) could lead to a local
expansion.
(4) Lake Mahoma harbors a peculiar cladoceran
species composition within the study region and
the lake can be considered a cold-temperate/
boreal freshwater island in the tropics. The
locally different community in the Rwenzori
can be attributed to its lower elevation (warmer
conditions), more extensive littoral, higher
accessibility to the east and/or older origin.
Accessibility is considered an important factor to
account for the species composition in Lake
Bujuku as well. Freshwater habitats in the
African Rift between 2000 and 3000 m may still
play an important role in the dispersal of aquatic
fauna, functioning as temporary stepping stones
for temperate eurythermic, cold-tolerant species.
We introduce a name for high altitude cold-water
islands of the tropical belt, Loffler Islands, a
conceptual term in honor of Dr Heinz Loffler,
aimed to facilitate the study of these habitats and
our future understanding of the dispersal and
speciation of the aquatic biotas found within.
Acknowledgments The fieldwork was conducted under
Uganda NCST research clearances EC540 and NS21, and
Uganda Wildlife Authority permits UWA/TBDP/RES/50 and
UWA/TDO/33/02, with logistic support from Rwenzori
Mountaineering Services. The authors Kamusongi (KVD) and
Mbahimba (HE) thank Ilse Bessems, Leen Audenaert, Halewijn
Missiaen, James Russell, Jessica Tierney, and Dirk Verschuren
for field assistance. L. Nevalainen and B. Walseng are thanked
for comparative material of A. rustica from Scandinavia. We
thank Els Ryken for assistance in preparing the collection and
body measurements of C. cf. sphaericus. We are further grateful
to referees Dr. P. J. Juracka and Dr A. Yu Sinev for constructive
comments. This research was sponsored by the Salomon Fund of
Brown University (US), US National Geographic Society (grant
7999-06), Fund for Scientific Research of Flanders, the Leopold
III-fund for Nature Exploration and Conservation (Belgium),
and the Stichting Ter Bevordering van het Wetenschappelijk
Onderzoek in Afrika (Belgium). H.E. was supported by the
Research Foundation and the Federal Science Policy of Belgium
(Action 1).
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