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: kay.vandamme@gmail.com

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

Hydrobiologia (2011) 676:57–100 69

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

123

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).

References

Adamowicz, S. J., P. D. N. Hebert & M. C. Marinone, 2004.

Species diversity and endemism in the Daphnia of Ar-

gentinia: a genetic investigation. Zoological Journal of the

Linnean Society 140: 171–205.

Adamowicz, S. J., A. Petrusek, J. K. Colbourne, P. D. N. Hebert

& J. D. S. Witt, 2009. The scale of divergence: a phylo-

genetic appraisal of intercontinental allopatric speciation in

a passively dispersed freshwater zooplankton genus.

Molecular Phylogenetics and Evolution 50: 171–205.

Aladin, N. V. & W. T. W. Potts, 1995. Osmoregulatory capacity

of the Cladocera. Journal of comparative physiology B.

Biochemical Systematic and Environmental Physiology

164: 671–683.

Alonso, M., 1991. Review of Iberian Cladocera with remarks on

ecology and biogeography. Hydrobiologia 225: 37–43.

Alonso, M., 1996. Crustacea, Branchiopoda. In Ramos, M. A.

(ed.), Fauna Iberica, Vol. 7. Museo Nacional de Ciencias

Naturales, CSIC, Madrid: 486 pp.

Assefa, A., D. Ehrich, P. Tabernet, S. Nemomissa & C.

Brochmann, 2007. Pleistocene colonization of afroalpine

sky islands by the arctic-alpine Arabis alpina. Heredity 99:

133–142.

Bajracharya, B., A. B. Shrestha & L. Rajbandari, 2007. Glacial

lake outburst floods in the Sagarmatha region. Hazard

assessment using GIS and hydrodynamic modeling.

Mountain Research and Development 27: 336–344.

Belyaeva, M., 2003. Littoral Cladocera (Crustacea: Branchio-

poda) from the Altai mountain lakes, with remarks on the

taxonomy of Chydorus sphaericus (O.F. Muller, 1776).

Arthropoda Selecta 12: 171–182.

Belyaeva, M. & R. Deneke, 2007. Colonization of acidic mining

lakes: Chydorus sphaericus and other Cladocera within a

dynamic horizontal pH gradient (pH 3–7) in Lake Senf-

tenberger See (Germany). Hydrobiologia 594: 97–108.

Belyaeva, M. & D. J. Taylor, 2009. Cryptic species within the

Chydorus sphaericus species complex (Crustacea: Clado-

cera) revealed by molecular markers and sexual stage

morphology. Molecular Phylogenetics and Evolution 50:

534–546.

Benzie, J. A. H., 2005. The Genus Daphnia (including Daph-niopsis) (Anomopoda: Daphniidae). Guides to the Identi-

fication of the Continental Waters of the World. Backhuys

Publishers, Leiden: 360 pp.

Berzins, B. & J. Bertilsson, 1990. Occurence of limnic micro-

crustaceans in relation to pH and humic content in Swedish

water bodies. Hydrobiologia 199: 65–71.

Bonnefille, R., J. C. Roeland & J. Guiot, 1990. Temperature and

rainfall estimates of the past 40,000 years in equatorial

Africa. Nature 346: 347–349.

Bos, D. G. & B. F. Cumming, 2003. Sedimentary Cladocera

remains and their relationship to nutrients and other lim-

nological variables in 53 lakes from British Columbia,

Canada. Canadian Journal of Fisheries and Aquatic Sci-

ences 60: 1177–1189.

Bottrell, H. H., 1975. The relationships between temperature

and duration of egg development in some epiphytic

Cladocera and Copepoda from the River Thames. Reading,

94 Hydrobiologia (2011) 676:57–100

123

with a discussion of temperature functions. Oecologia 18:

63–84.

Boileau, M. G., P. D. N. Hebert & S. S. Schwartz, 1992. Non

equilibrium gene-frequency: divergence persistent founder

effects in natural populations. Journal of Evolutionary

Biology 5: 25–39.

Bracchini, L., A. M. Dattilo, V. Hull, S. A. Loiselle, L. Nanni-

cini, M. P. Picchi, M. Ricci, C. Santinelli, A. Seritti, A.

Tognazzi & C. Rossi, 2010. Spatial and seasonal changes in

optical properties of allochthonous and allochthonous

chromophoric dissolved organic matter in a stratified

mountain lake. Photochemical and Photobiological sci-

ences 9: 304–314.

Brehm, V., 1935. Crustacea, I. Cladocera und Euphyllopoda.

Mission Scientifique de l’Omo 2. National Museum of

Natural History 2: 141–166.

Brehm, V., 1937. Cladoceren und Ostracodcn aus Angola. Ar-

chiv fur Hydrobiologie 32: 488–505.

Brehm, V., 1939. Cladocera. Exploration du Parc National

Albert-Mission H. Damas (1935–1936) 7: 3–12.

Chen, G. J., C. Dalton & D. Taylor, 2010. Cladocera as indi-

cators of trophic state in Irish Lakes. Journal of Paleolim-

nology 44: 465–481.

Chengalath, R., 1987. The distribution of chydorid Cladocera in

Canada. Hydrobiologia 145: 151–157.

Chiambeng, G. Y. & H. J. Dumont, 2005. The Branchiopoda

(Crustacea: Anomopoda, Ctenopoda & Cyclestheridae) of

the rain forests of Cameroon, West Africa: low abundance,

few endemics and a boreal-tropical disjunction. Journal of

Biogeography 32: 1611–1620.

Chiambeng, G., S. Sebaze, T. Youmbi & O. Njifonjou, 2006.

Description of the genus Alona Baird, 1843 (Crustacea:

Anomopoda: Chyoridae) from the rainforest of Cameroon,

Central-West Africa. Journal of the Cameroon Academy of

Sciences 6: 81–90.

Chorowicz, J., 2005. The East African rift system. Journal of

African Earth Sciences 43: 379–410.

Coronel, J. S., S. Declerck & L. Brendonck, 2007. High-altitude

peatland temporary pools in Bolivia house a high cladoc-

eran diversity. Wetlands 27: 1166–1174.

Cruz, L., 1981. Estudio de la comunidad zooplanctonica de un

lago de alta montana (La Caldera, Sierra Nevada, Gra-

nada). PhD dissertation, University of Granada, Granada,

Spain: 180 pp.

Cullen, N. J., T. Molg, G. Kaser, K. Hussein, K. Steffen & D.

R. Hardy, 2006. Kilimanjaro glaciers: recent areal extent

from satellite data and new interpretation of observed 20th

century retreat of glaciers. Geophysical Research Letters

33: L16502.

Declerck, S., J. Vandekerckhove, L. Johannson, K. Muylaert, J.

M. Conde-Porcuna, K. Van Der Gucht, C. Perze-Martinez,

T. Lauridsen, K. Schwenk, G. Zwart, W. Rommens, J.

Lopez-Ramos, E. Jeppesen, W. L. Vyverman, L. Bren-

donck & L. De Meester, 2005. Multi-group biodiversity in

shallow lakes along gradients of phosphorus and water

plant cover. Ecology 86: 1905–1915.

De Guerne, J. & J. Richard, 1892. Cladoceres et Copepodes

d’eau douce des environs de Rufisque. Memoires de la

Societe zoologique de France 5: 526–538.

de Heinzelin, J., 1962. Carte des extensions glaciares du

Rwenzori (versant Congolais). Biuletyn Peryglacjalny 11:

133–139.

De Meester, L., A. Gomez, B. Okamura & K. Schwenk, 2002.

The monopolization hypothesis and the dispersal-gene

flow paradox in aquatic organisms. Acta Oecologica 23:

121–135.

De Sellas, A. M., A. M. Patterson, J. N. Sweetman & J. P. Smol,

2008. Cladocera assemblages from the surface sediments of

South Ontario (Canada) lakes and their relationships to mea-

sured environmental variables. Hydrobiologia 600: 105–119.

Duigan, C. A., 1992. The ecology and distribution of the littoral

freshwater Chydoridae (Branchiopoda, Anomopoda) of

Ireland, with taxonomic comments on some species.

Hydrobiologia 241: 1–70.

Duigan, C. A. & H. H. Birks, 2000. The late-glacial and early-

Holocene palaeoecology of cladoceran microfossil

assemblages at Krakenes, western Norway, with a quanti-

tative reconstruction of temperature changes. Journal of

Paleolimnology 23: 67–76.

Dumont, H. J., 1981. Cladocera and free-living Copepoda from

the Fouta Djalon and adjacent mountain ares in West

Africa. Hydrobiologia 85: 97–116.

Dumont, H. J., 1994. On the diversity of the Cladocera in the

tropics. Hydrobiologia 272: 27–38.

Dumont, H. J. & G. M. El-Shabrawy, 2008. Seven decades of

change in the zooplankton (s.l.) of the Nile Delta Lakes

(Egypt), with particular reference to Lake Borullus. Inter-

national Review of Hydrobiology 93: 44–61.

Dumont, H. J., J. Pensaert & I. Van de Velde, 1981. The crus-

tacean zooplankton of Mali (West Africa). Hydrobiologia

80: 161–187.

Eggermont, H. & D. Verschuren, 2007. Taxonomy and diversity

of Afroalpine Chironomidae (Insecta: Diptera) on Mount

Kenya and the Rwenzori Mountains, East Africa. Journal

of Biogeography 34: 69–89.

Eggermont, H., J. M. Russell, G. Schettler, K. Van Damme & D.

Verschuren, 2007. Physical and chemical limnology of

alpine lakes and pools in the Rwenzori Mountains

(Uganda-Congo). Hydrobiologia 592: 151–173.

Eggermont, H., K. Van Damme & J. Russell, 2009. Rwenzori

Mountains (Mountains of the Moon): headwaters of the

White Nile. In Dumont, H. J. (ed.), The Nile: Origin,

Environments, Limnology and Human Use. Monographiae

Biologicae. Springer, Berlin: 243–261.

Eggermont, H., O. Heiri, J. Russell, M. Vuille, L. Audenaert &

D. Verschuren, 2010a. Chironomidae (Insecta: Diptera) as

paleothermometers in the African tropics. Journal of Pa-

leolimnology 43: 413–435.

Eggermont, H., D. Verschuren, L. Audenaert, L. Lens, J. Rus-

sell, G. Klaassen & O. Heiri, 2010b. Limnological and

ecological sensitivity of Rwenzori mountain lakes to cli-

mate warming. Hydrobiologia 648: 123–142.

Elıas-Gutıerrez, M., J. Ciros-Perez, E. Suarez-Morales & M.

Silva-Briano, 1999. The freshwater Cladocera (orders

Ctenopoda and Anomopoda) of Mexico, with comments on

selected taxa. Crustaceana 72: 171–186.

Fischer, S., 1854. Abhandlung uber einige neue oder nicht genau

gekannte Arten von Daphniden und Lynceiden, als Beitrag

Hydrobiologia (2011) 676:57–100 95

123

zur Fauna Russlands. Bulletin de la Societe Imperiale des

Naturalistes de Moscou 27: 423–434.

Flossner, D., 1972. Krebstiere, Crustacea. Kiemen-und Blat-

tfusser, Branchiopoda. Fischlause, Branchiura. Die Tier-

welt Deutschlands 60: 501 pp.

Flossner, D., 2000. Die Haplopoda und Cladocera (ohne Bos-

minidae) Mitteleuropas. Backhuys Publishers, Leiden.

428.

Forro, L., N. M. Korovchinsky, A. A. Kotov & A. Petrusek,

2008. Global diversity of cladocerans (Cladocera; Crusta-

cea) in freshwater. Hydrobiologia 595: 177–184.

Frey, D. G., 1962. Cladocera from the Eemian interglacial of

Denmark. Journal of Palaeontology 36: 1133–1153.

Frey, D. G., 1965. Differentiation of Alona costata Sars from

two related species (Cladocera, Chydoridae). Crustaceana

8: 159–173.

Frey, D. G., 1980. On the plurality of Chydorus sphaericus (O.

F. Mueller) (Cladocera, Chydoridae) and designation of a

neotype from Sjaelso, Denmark. Hydrobiologia 69:

83–123.

Frey, D. G., 1982. Questions concerning cosmopolitanism in

Cladocera. Archiv fur Hydrobiologie 93: 484–502.

Frey, D. G., 1986. The non-cosmopolitanism of chydorid

Cladocera: implications for biogeography and evolution. In

Heck, K. L. & R. H. Gore (eds), Crustacean Biogeography.

Balkema, Rotterdam: 237–256.

Frey, D. G., 1987. The taxonomy and biogeography of the

Cladocera. Hydrobiologia 145: 5–17.

Frey, D. G., 1993a. The penetration of cladocerans into saline

waters. Hydrobiologia 267: 233–248.

Frey, D. G., 1993b. Subdivision of the genus Pleuroxus(Anomopoda, Chydoridae) into subgenera worldwide.

Hydrobiologia 262: 133–144.

Fryer, G., 1957. Freeliving freshwater Crustacea from Lake

Nyasa and adjoining waters. Part II. Cladocera and Conc-

hostraca. Archiv fur Hydrobiologie 53: 223–239.

Fryer, G., 1968. Evolution and adaptive radiation in the Chy-

doridae (Crustacea: Cladocera). A study in comparative

functional morphology and ecology. Philosophical Trans-

actions of the Royal Society London Series B 795: 221–385.

Fryer, G., 1993. The Freshwater Crustacea of Yorkshire.

A Faunistic and Ecological Survey. Yorkshire Naturalists’

Union and Leeds Philosophical and Literary Society, UK.

Gauthier, H., 1928. Cladoceres et Ostracodes de l’Afrique du

Nord. Bulletin de la Societe d’Histoire Naturelle de l’Af-

rique du Nord 19: 69–79.

Gehrke, B. & H. P. Linder, 2009. Scramble for Africa: pan-

temperate elements on the African high mountains. Pro-

ceedings of the Royal Society B 276: 2657–2665.

Gottelli, D., J. Marino, C. Sillero-Zubriri & S. M. Funk, 2004.

The effect of the last glacial age on speciation and popu-

lation structure of the endangered Ethiopian Wolf (Canissimensis). Molecular Ecology 13: 2275–2286.

Green, J., 1962. Zooplankton of the river Sokoto: the Crustacea.

Proceedings of the Zoological Society of London 138:

415–453.

Green, J., 1995. Altitudinal distribution of tropical planktonic

Cladocera. Hydrobiologia 307: 75–84.

Green, J. & G. W. Kling, 1988. The genus Daphnia in Camer-

oon, West Africa. Hydrobiologia 160: 257–261.

Gurney, R., 1911. On some freshwater Entomostraca from

Egypt and the Soudan. Annals and Magazine of Natural

History 8: 25–33.

Hamrova, E., V. Golias & A. Petrusek, 2010. Identifying cen-

tury-old long-spined Daphnia: species replacement in a

mountain lake characterised by paleogenetic methods.

Hydrobiologia 643: 97–106.

Harding, J. P., 1957. Crustacea: Cladocera. Exploration hydro-

biologique du lac Tanganyika (1946–1947). Resultats

Scientifiques 3: 55–89.

Harding, J. P., 1961. Some South African Cladocera collected

by Dr A.D. Harrison. Annals of the South African Museum

46: 35–46.

Harmsworth, R. V., 1968. The developmental history of Blel-

ham Tarn (England) as shown by animal microfossils, with

special reference to the Cladocera. Ecological Monographs

38: 223–241.

Hart, R. C. & H. J. Dumont, 2006. A Holarctic taxon in the

Ethiopian region: a first record of Lathunola (Crustacea:

Cladocera: Macrothricidae) for the Okavango swamps of

subtropical Africa. South African Journal of Science 101:

565–567.

Heald, W. F., 1951. Sky islands of Arizona. Natural History

60(56–63): 95–96.

Hebert, P. D. N. & C. J. Emery, 1990. The adaptive significance

of cuticular pigmentation in Daphnia. Functional Ecology

4: 703–710.

Hebert, P. D. N., & D. B. McWalter, 1983. Cuticular pigmen-

tation in arctic Daphnia: adaptive diversification of asexual

lineages? American Naturalist 122: 286–291.

Hedberg, O., 1969. Evolution and speciation in a tropical high

mountain flora. Botanical Journal of the Linnean Society 1:

135–148.

Hessen, D. O., J. Borgeraas, K. Kessler & U. H. Refseth, 1999.

UV-B susceptibility and photoprotection of Arctic Daph-nia morphotypes. Polar Research 18: 345–352.

Hessen, D. O. & B. Walseng, 2008. The rarity concept and the

commonness of rarity in zooplankton. Freshwater Biology

53: 2026–2035.

Hessen, D. O. & K. Sorensen, 1990. Photoprotective pigmen-

tation in alpine zooplankton populations. Aqua Fennica 20:

165–170.

Hessen, D. O. & N. A. Rukke, 2000. UV radiation and low

calcium as mutual stressors for Daphnia. Limnology and

Oceanography 45: 1834–1838.

Hewitt, G. M., 1996. Some genetic consequences of the ice ages

and their role in divergence and speciation. Biological

Journal of the Linnean Society 58: 247–276.

Hewitt, G. M., 2000. The genetic legacy of the Quaternary ice

ages. Nature 405: 907–913.

Hewitt, G. M., 2004. Genetic consequences of climatic oscil-

lations in the Quaternary. Philosophical Transactions of the

Royal Society B Biological Sciences 359: 183–195.

Hill, M. O. & H. G. Gauch, 1980. Detrended correspondence

analysis. An improved ordination technique. Vegetatio 42:

47–58.

Hofmann, W., 2000. Response of the chydorid faunas to rapid

climatic changes in four alpine lakes at different altitudes.

Palaeogeography, Palaeoclimatology, Palaeoecology 159:

281–292.

96 Hydrobiologia (2011) 676:57–100

123

Hofmann, W., 2003. The long-term succession of high altitude

cladoceran assemblages: a 9000-year record from Sag-

italsee (Swiss Alps). Journal of Paleolimnology 30:

291–296.

Horicka, Z., E. Stuchlık, I. Hudec, M. Cerny & J. Fott, 2006.

Acidification and the structure of crustacean zooplankton

in mountain lakes: the Tatra Mountains (Slovakia, Poland).

Biologia Bratislava 61(Suppl 18): 121–134.

Hudec, I., 1998. Anomopoda (Crustacea: Branchiopoda) from

some Venezuelan tepuis. Hydrobiologia 377: 205–211.

Hudec, I., 2010. Fauna Slovenska III. Anomopoda, Ctenopoda,

Haplopoda, Onychopoda (Crustacea: Branchiopoda),

VEDA. Vydavatel stvo Slovenskej adademie vied,

Bratislava.

Idris, B. A. G., 1983. Freshwater Zooplankton of Malaysia

(Crustacea: Cladocera). Monograph. University Pertanian,

Malaysia: 153 pp.

Ishida, S., A. A. Kotov & D. J. Taylor, 2006. A new divergent

lineage of Daphnia (Cladocera: Anomopoda) and its

morphological and genetical differentiation from Daphniacurvirostris Eylmann 1887. Zoological Journal of the

Linnean Society 146: 385–405.

Jenkin, P. M., 1934. Reports on the Percy Sladen Expedition to

some Rift Valley Lakes in Kenya in 1929. VI. Cladocera

from the Rift Valley Lakes in Kenya. Annals and Magazine

of Natural History 13: 137–308.

Juracka, P. J., V. Korınek & A. Petrusek, 2010. A new central

European species of the Daphnia curvirostris species

complex, Daphnia hrbaceki sp. nov (Cladocera, Anomo-

poda, Daphniidae). Zootaxa 2718: 1–22.

Kamenik, C., K. Szeroczynska & R. Schmidt, 2007. Relation-

ships among recent Alpine Cladocera remains and their

environment: implications for climate-change studies.

Hydrobiologia 594: 33–46.

Kaser, G. & H. Osmaston, 2002. Tropical Glaciers. Cambridge

University Press, Cambridge.

Knockaert, A. 2002. Distribution of crustacean zooplankton

(Cladocera) along a salinity gradient of crater lakes in

western Uganda. Unpublished Diss. Master of Science in

Advanced Studies In Marine And Lacustrine Sciences,

Ghent.

Koch, M., C. Kiefer, D. Ehrich, J. Vogel, C. Brochmann & K.

Mummenhoff, 2006. Three times out of Asian Minor: The

phylogeography of Arabis alpina L. (Brassicaceae).

Molecular Ecology 15: 825–839.

Koinig, K. A., C. Kamenik, R. Schmidt, A. Agusti-Panareda, P.

Appleby, A. Lami, M. Prazakova, N. Rose, O. A. Schnell,

R. Tessadri, R. Thompson & R. Psenner, 2002. Environ-

mental changes in a alpine lake (Gossenkollesee, Austria)

over the last two centuries: the influence of air temperature

on biological parameters. Journal of Paleolimnology 28:

147–160.

Korhola, A., J. Weckstrom, L. Holmstrom & P. Erasto, 2000. A

quantive Holocene climate record from diatoms in northern

Fennoscandia. Quaternary research 54: 284–294.

Korınek, V., 2002. Cladocera. In Fernando, C. H. (ed.), A Guide

to Tropical Freshwater Zooplankton. Blackhuys Publish-

ers, Leiden: 69–122.

Korosi, J. B. & J. P. Smol, 2011. Distribution of cladoceran

assemblages across environmental gradients in Nova

Scotia (Canada) lakes. Hydrobiologia 663: 83–99.

Kotov, A. A. & M. Elias-Gutierrez, 2009. A phylogenetic

analysis of Ilyocryptus Sars 1862 (Cladocera: Ilyocrypti-

dae). International Review of Hydrobiology 94: 208–225.

Kotov, A. A. & A. Y. Sinev, 2005. Notes on Aloninae Dybowski

& Grochowski 1894 emend. Frey 1967 (Cladocera:

Anomopoda: Chydoridae): 3. Alona iheringula nom. nov.

instead of A. iheringi Sars 1901, with comments of this

taxon. Arthropoda Selecta 13: 95–98.Kotov, A. A. & P. Stifter, 2005. Notes on the genus Ilyocryptus

Sars, 1862 (Cladocera: Anomopoda: Ilyocryptidae). 7.

Two new species from South Africa, with first record of

Ilyocryptus from rockpools. Arthropoda Selecta 14:

219–228.

Kotov, A. A. & P. Stifter, 2006. Family Ilyocryptidae (Bran-

chiopoda: Cladocera: Anomopoda). Guide to the Identifi-

cation of the Macroinvertebrates of the Continental Waters

of the World. Blackhuys Publishers, Leiden: 172 pp.

Kotov, A. A. & D. J. Taylor, 2010. A new African lineage of the

Daphnia obtusa group (Cladocera: Daphniidae) disrupts

continental vicariance patterns. Journal of Plankton

Research 32: 937–949.

Kotov, A. A., T. Garfias-Espejo & M. Elıas-Gutierrez, 2004.

Separation of two Neotropical species: Macrothrix super-aculeata (Smirnov, 1982) versus M. elegans Sars, 1901

(Macrothricidae, Anomopoda, Cladocera). Hydrobiologia

517: 61–88.

Kotov, A. A., S. Ishida & D. J. Taylor, 2006. A new species of

the Daphnia curvirostris (Crustacea: Cladocera) complex

from the eastern Palearctic with molecular phylogenetic

evidence for the independent origin of neckteeth. Journal

of Plankton Research 28: 1067–1079.

Kotov, A. A., A. Y. Sinev & V. L. Berrios, 2010. The Cladocera

(Crustacea: Branchiopoda) of six high altitude water bod-

ies in the North Chilean Andes, with discussion of Andean

endemism. Zootaxa 2430: 1–66.

Krause-Dellin, D. & C. Steinberg, 1986. Cladoceran remains as

indicators of lake acidification. Hydrobiologia 143:

129–134.

Lami, A., S. Turner, S. Musazzi, S. Gerzi, P. Guillizzoni, N.

L. Rose, H. D. Yang, G. J. Wu & R. Q. Yang, 2010. Sed-

imentary evidence for recent increases in production in

Tibetan plateau lakes. Hydrobiologia 648: 175–187.

Lens, P., 1978. Study of the Crustacea Entomostraca of Mount

Kenya. Unpublished Licentiate thesis. Ghent University, in

Dutch: 105 pp.

Leibold, M. A. & J. Norberg, 2004. Biodiversity in metacom-

munities: plankton as complex adaptive systems? Lim-

nology and Oceanography 49: 1278–1289.

Leibold, M. A., M. Holyoak, N. Mouquet, P. Amarasekare, J.

M. Chase, M. F. Hoopes, R. D. Holt, J. B. Shurin, R. Law,

D. Tilman, M. Loreau & A. Gonzalez, 2004. The meta-

community concept: a framework for multiscale commu-

nity ecology. Ecology Letters 7: 601–613.

Livingstone, D. A., 1967. Postglacial vegetation of the

Rwenzori mountains in Equatorial Africa. Ecological

Monographs 37: 26–51.

Livingstone, D. M., A. F. Lotter & I. R. Walker, 1999. The

decrease in summer surface water temperature with alti-

tude in Swiss alpine lakes: a comparison with air temper-

ature lapse rate. Arctic, Antarctic and Alpine Research 31:

341–352.

Hydrobiologia (2011) 676:57–100 97

123

Loffler, H., 1964. The limnology of tropical high-mountain

lakes. Verhandlungen Internationale Vereinigung der

Limnologie 15: 176–193.

Loffler, H., 1968a. Die Hochgebirgseen Ostafrikas. Ho-

chgebirgsforschung 1: 1–65.

Loffler, H., 1968b. Die Crustaceenfauna der Binnengewasser

Ostrafikanischer Hochberge. Hochgebirgsforschung 1:

107–170.

Loffler, H., 1968c. Tropical high mountain lakes. Their distri-

bution, ecology and zoogeographical importance. Collo-

quium Geographicum 9: 57–76.

Loffler, H., 1978. Limnological and Paleolimnological data of

the Bale Mountain lakes. Verhandlung International Ve-

rein Limnology 20: 1131–1138.

Loffler, H., 1984. The importance of mountains for animal

distribution, species speciation, and faunistic evolution

(with special attention to inland waters). Mountain

Research and Development 4: 299–304.

Lotter, A. F., H. J. B. Birks, W. Hofmann & A. Marchetto, 1997.

Modern diatom, cladoceran, chironomid, and chrysophyte

cyst assemblages as quantitative indicators for the recon-

struction of past environmental conditions in the Alps.

I. Climate. Journal of Paleolimnology 18: 395–420.

Louette, G. & L. De Meester, 2004. Rapid colonization of a

newly created habitat by cladocerans and the initial build-

up of a Daphnia-dominated community. Hydrobiologia

513: 245–249.

Louette, G. & L. De Meester, 2005. High dispersal capacity of

cladoceran zooplankton in newly founded communities.

Ecology 86: 353–359.

Lowndes, A. G., 1931. A small collection of Entomostraca from

Uganda, collected by Mr. G.R. Hancock. Proceedings of

the Zoological Society London 101: 1291–1299.

Lowndes, A. G., 1952. Hydrogen ion concentration and the

distribution of freshwater Entomostraca. Annals and

Magazine of Natural History 12: 58–65.

Mahaney, W. C., 1989. Quaternary and Environmental

Research on the East African Mountains. Balkena,

Rotterdam.

Malone, C. R., 1964. Dispersal of aquatic gastropods via the

intestinal tract of waterbirds. Nautilus 44: 135–139.

Manca, M. & P. Comoli, 2004. Reconstructing long-term

changes in Daphnia’s body size from subfossil remains in

sediments of a small lake in the Himalayas. Journal of

Paleolimnology 32: 95–107.

Manca, M., P. Cammarano & T. Spagnuolo, 1994. Notes on

Cladocera and Copepoda from high altitude lakes in the

Mount Everest Region (Nepal). Hydrobiologia 287:

225–231.

Manca, M., D. Ruggiu & P. Panzan, 1998. Report on a collection

of aquatic organisms from high mountain lakes in the

Khumbu Valley (Nepalese Himalayas). Memorie dell’Is-

tituto italiano di Idrobiologia 57: 77–98.

McCormack, J. E., H. Huang & L. L. Knowles, 2009. Sky

islands. In Gillespie, R. G. & D. Clague (eds), Encyclo-

pedia of Islands. University of California Press, Berkeley,

CA: 839–843.

Mergeay, J., D. Verschuren, L. Van Kerckhoven & L. De Me-

ester, 2004. Two hundred years of a diverse Daphniacommunity in Lake Naivasha (Kenya): effects of natural

and human-induced environmental changes. Freshwater

Biology 49: 998–1013.

Mergeay, J., D. Verschuren & L. De Meester, 2005. Daphniaspecies diversity in Kenya, and a key to the identification of

their ephippia. Hydrobiologia 542: 261–274.

Mergeay, J., X. Aguilera, S. Declerck, A. Petrusek, T. Huyse &

L. De Meester, 2008. The genetic legacy of polyploid

Bolivian Daphnia: the tropical Andes as a source for the

North and South American D. pulicaria complex. Molec-

ular Ecology 17: 1789–1800.

Nandini, S., M. Silva-Briano, G. Garcıa, S. Sarma, A. Ada-

bache-Ortiz & R. de la Rosa, 2009. First record of the

temperate species Daphnia curvirostris Eylmann, 1887

emend. Johnson, 1952 (Cladocera: Daphniidae) in Mexico

and its demographic characteristics in relation to algal food

density. Limnology 10: 87–94.

Nevalainen, L. & K. Sarmaja-Korjonen, 2008. Intensity of

autumnal gamogenesis in chydorid (Cladocera, Chydori-

dae) communities in southern Finland, with a focus on

Alonella nana (Baird). Aquatic Ecology 42: 151–163.

Nevalainen, L., K. Van Damme, T.P. Luoto & V.-P. Salonen, 2011.

Fossil remains of an unknown Alona species (Chydoridae,

Aloninae) from a high arctic lake in Nordlandaustet (Svald-

bard) in relation to glaciations and Holocene environmental

history. Polar Biology. doi:10.1007/s00300-011-1077-z.

Nilssen, J. P., A. Hobaek, A. Petrusek & M. Skage, 2007.

Restoring Daphnia lacustris G.O. Sars 1862 (Crustacea:

Anomopoda): a cryptic species in the Daphnia longispinagroup. Hydrobiologia 594: 5–17.

Okogwu, O. I., 2009. Seasonal variations of species composition

and abundance of zooplankton in Ehoma Lake, a floodplain

lake in Nigeria. Revue d’Hydrobiologie Tropicale 58:

171–182.

Osmaston, H. A., 1965. The past and present climate and veg-

etation of Rwenzori and its neighbourhood. PhD thesis,

Oxford: 238 pp.

Osmaston, H. A., 1998. The influence of the Quaternary history

and glaciations of the Rwenzori on the present landscape

and ecology. In Osmaston, H., J. Tukahirwa, C. Basalirwa

& J. Nyakaana (eds), The Rwenzori Mountains National

Park, Uganda. Proceedings of the Rwenzori Conference.

Department of Geography, Makerere University, Kampala,

Uganda: 370–388.

Osmaston, H. A., 2006. Guide to the Rwenzori Mountains of the

Moon. Rwenzori Trust, UK: 288 pp.

Patalas, K., 1964. The crustacean plankton communities in 52

lakes of different altitudinal zones of northern Colorado.

Verhandlungen der Internationalen Vereinigung fur The-

oretische und Angewandte Limnologie 15: 719–726.

Petrusek, A., M. Cerny, J. Mergeay & K. Schwenk, 2007.

Daphnia in the Tatra Mountain lakes: multiple colonization

and hidden species diversity revealed by molecular mark-

ers. Fundamental and Applied Limnology 169: 279–291.

Popp, M., A. Gizaw, S. Nemomissa, J. Suda & C. Brochmann,

2008. Colonization and diversification in the African ‘sky

island’ by Eurasian Lychnis L. (Caryophyllaceae). Journal

of Biogeography 35: 1016–1029.

Porter, S. C., 2001. Snowline depression in the tropics during the

last Glaciation. Quaternary Science Reviews 20:

1067–1091.

98 Hydrobiologia (2011) 676:57–100

123

Quincey, D. J., S. D. Richardson, A. Luckman, R. M. Lucas, J.

M. Reynolds, M. J. Hambrey & N. S. Glasser, 2007. Early

recognition of glacial lake hazards in the Himalaya using

remote sensing datasets. Global and Planetary Change 56:

137–152.

Rautio, M., 1988. Community structure of crustacean zoo-

plankton in subarctic ponds-effects of altitude and physical

heterogeneity. Ecography 21: 327–335.

Rejmankova, E. & M. Rejmanek, 1995. A Comparison of Carexrunssoroensis Fens on Ruwenzori Mountains and Mount

Elgon, Uganda. Biotropica 27: 37–46.

Rees, W. J., 1965. The aerial dispersal of mollucsa. Proceedings

of the Malacological Society London 36: 269–282.

Rey, M. J. & L. Saint-Jean, 1968. Les Cladoceres (Crustaces,

Branchiopodes) du Tchad (Premiere note). Cahiers OR-

STROM, Serie Hydrobiologie 2: 79–118.

Rey, J. & L. St-Jean, 1969. Les Cladoceres (Crustaces Bran-

chiopodes) du Tchad (Deuxieme note). Cahier

O.R.S.T.R.O.M., series Hydrobiologie 3: 21–42.

Richard, J., 1894. Cladoceres recueillis par le M. le Dr Barrois

en Palestine en Syrie et en Egypte (mars-juin 1890). Lille 6:

360–378.

Røen, U., 1992. Review of Greenlandic species of Alona Baird,

1850, with descriptions of three new species (Cladocera:

Chydoridae: Aloninae). Steenstrupia 18: 101–109.

Rumes, B., 2010. Regional diversity, ecology and palaeoecol-

ogy of aquatic invertebrate communities in East Africa

lakes. Unpublished PhD, Ghent University.

Rundel, P. W., 1994. Tropical alpine climates. In Rundel, P. W.,

A. P. Smith & F. C. Meinzer (eds), Plant Form & Function.

Cambridge University Press, Cambridge: 21–44.

Russell, J. M., H. Eggermont, R. Taylor & D. Verschuren, 2009.

Paleolimnological records of recent glacier recession in the

Rwenzori Mountains, Uganda-DR Congo. Journal of Pa-

leolimnology 41: 253–271.

Sacherova, V., R. Krskova, E. Stuchlık, Z. Horicka, I. Hudec &

J. Fott, 2006. Long-term change of the littoral Cladocera in

the Tatra Mountain lakes through a major acidification

event. Biologia, Bratislava 61(Suppl 18): 109–119.

Sarmaja-Korjonen, K. & A. Y. Sinev, 2008. First records of

Alona werestchagini Sinev in Finland-Subfossil remains

from Subarctic lakes. Studia Quaternaria 25: 43–46.

Sars, G. O., 1916. The fresh-water Entomostraca of the Cape

Province (Union of South Africa). Part 1: Cladocera.

Annals of the South African Museum 15: 303–351.

Schiefer, E. & R. Gilbert, 2008. Proglacial sediment trapping in

recently formed Silt Lake, Upper Lillooet Valley, Coast

Mountains, British Columbia. Earth Surface Processes and

Landforms 33: 1542–1556.

Siebeck, O., 1978. Ultraviolet tolerance of planktonic crusta-

ceans. Verhandlungen der Internationalen Vereinigung

Limnologie 20: 2469–2473.

Schwenk, K., D. Posada & P. D. N. Hebert, 2000. Molecular

systematics of European Hyalodaphnia: the role of con-

temporary hybridization in ancient species. Proceedings of

the Royal Society of London Series B––Biological Sci-

ences 267: 1833–1842.

Sinev, A. Y., 1997. Review of the affinis-group of Alona Baird,

1843, with the description of a new species from Australia

(Anomopoda Chydoridae). Arthropoda Selecta 6: 47–58.

Sinev, A. Y., 1999a. Alona costata Sars, 1862 versus related

palaeotropical species: the first example of close relations

between species with a different number of main head

pores among Chydoridae (Crustacea: Anomopoda).

Arthropoda Selecta 8: 131–148.

Sinev, A. Y., 1999b. Alona werestschagini sp. n., new species of

genus Alona Baird, 1843, related to A. guttata Sars, 1862

(Anomopoda, Chydoridae). Arthropoda Selecta 8: 23–30.

Sinev, A. Y., 2001. Redescription of Alona iheringi Sars, 1901

(Chydoridae, Anomopoda, Branchiopoda), a South

American species related to A. rustica Scott, 1895. Hyd-

robiologia 464: 113–119.

Sinev, A. Y., 2009. Cladocerans for the Alona affinis (Leydig

1860) group from South Africa. Zootaxa 1990: 41–54.

Smirnov, N. N., 1971. Chydoridae fauny mira. Fauna USSR.

Rakoobraznie, 1(2), Leningrad, 531 pp. (English transla-

tion: Chydoridae of the World. Israel Program for Scien-

tific Translations, Jerusalem, 1974).

Smirnov, N. N., 1996. Cladocera: the Chydorinae and Sayciinae

(Chydoridae) of the World. In Dumont, H. J. (ed.), Guides

to the identification of the microinvertebrates of the con-

tinental waters of the world volume 11. SPB Academic

Publishing, Amsterdam: 197 pp.

Smirnov, N. N., 2007. Pleuroxus-like Chydorids (Crustacea:

Anomopoda) from South Africa, with the description of

Dumontiellus africanus gen. n., sp. n. Hydrobiologia 575:

433–439.

Smirnov, N. N., 2008. Checklist of the South African Cladocera

(Crustacea: Branchiopoda). Zootaxa 1788: 47–56.

Smirnov, N. N., A. Kotov & J. S. Coronel, 2006. Partial revision

of the aduncus-like species of Pleuroxus Baird 1843

(Chydoridae Cladocera) from the southern hemisphere

with comments on subgeneric differentiations within the

genus. Journal of Natural History 40: 1617–1639.

Taylor, D. J. & P. D. N. Hebert, 1993. Cryptic intercontinental

hybridization in Daphnia (Crustacea): The Ghost of

Introductions Past. Proceedings of the Royal Society of

London Series B—Biological Sciences 254: 163–168.

Temple, P. H., 1961. A Final Report of the Makerere College

I.G.Y. Expeditions to Rwenzori. Department of Geogra-

phy, Makerere.

ter Braak, C. J. F. & P. Smilauer, 2002. CANOCO Reference

Manual and CanoDraw for Windows User’s Guide: Soft-

ware for Canonical Community Ordination (Version 4.5).

Microcomputer Power, Ithaca, NY.

Thomas, I. F., 1961. The Cladocera of the S wamps of Uganda.

Crustaceana 2: 108–125.

Tollrian, R. & C. Heibl, 2004. Phenotypic plasticity in pig-

mentation in Daphnia induced by UV-radiation and fish

kairomones. Functional ecology 18: 497–502.

Tremel, B., S. E. Frey, N. D. Yan, K. M. Somers & T.

W. Pawson, 2000. Habitat specificity of littoral Chydoridae

(Crustacea, Branchiopoda, Anomopoda) in Plastic Lake,

Ontario, Canada. Hydrobiologia 432: 195–205.

Van Damme, K., 2010. A revision of the genus Alona Baird,

1843 (Crustacea: Branchiopoda: Anomopoda). PhD Dis-

sertation, Ghent University, Belgium: 506 pp.

Van Damme, K. & H. J. Dumont, 2009. Notes on chydorid

endemism in continental Africa: Matralona gen. n., a

monotypic Alonine from the Fouta Djalon Plateau (Guinea,

Hydrobiologia (2011) 676:57–100 99

123

West Africa) Crustacea, Anomopoda. Zootaxa 2051:

26–40.

Van Damme, K. & H. J. Dumont, 2010. Cladocera of the Len-

cois Maranhenses (NE-Brazil): faunal composition and a

reappraisal of Sars’ Method. Brazilian Journal of Biology

70: 755–779.

Van Damme, K., A. A. Kotov & H. J. Dumont, 2010. A checklist

of names in Alona Baird, 1843 (Crustacea: Cladocera:

Chydoridae) and their current status: an analysis of the

taxonomy of a lump genus. Zootaxa 2330: 1–63.

Van Damme, K., A. Y. Sinev & H. J. Dumont, 2011. Separation

of Anthalona gen.n. from Alona Baird, 1843 (Branchio-

poda: Cladocera: Anomopoda): morphology and evolution

of scraping stenothermic alonines. Zootaxa 2875: 1–64.

von Daday, E., 1910. Untersuchungen uber die Susswasser-

Mikrofauna Deutsch-Ostrafrikas. Zoologica, Stuttgart 23:

1–314.

Wallner, H. & H. Schmeling, 2010. Rift induced delamination

of mantle lithosphere and crustal uplift: a new mechanism

for explaining Rwenzori Mountains’s extreme elevation.

International Journal of Earth Sciences 99: 1511–1524.

Warshall P., 1994. The Madrean sky island archipelago: a

planetary overview, pg. 6-18. In De Bano, F. L., P.

F. Ffolliott, A. Ortega-Rubio, G. J. Gottfried, R. H. Hamre,

C. B. Edminster (eds), Rocky Mountain Forest & Range

Experiment Station, Fort Collins, Colorado. Biodiversity &

Management of the Madrean Archipelago: The sky islands

of southwestern United States and Northwestern Mexico,

United States Forest Service Publications, US.

Weider, L. J., 1987. Life history variation among low-arctic

clones of obligately parthenogenetic Daphnia pulex: a

diploid-polyploid complex. Oecologia 73: 251–256.

Wetzel, R. G., 2001. Limnology: Lake and River Ecosystems,

3rd ed. Academic Press, London.

Whiteside, M. C. & R. Harmsworth, 1967. Species diversity in

Chydorid (Cladocera) communities. Ecology 48: 664–667.

Williams, J., 1978. Ilyocryptus gouldeni, a new species of water

flea and the first American record of I. agilis Kurz (Crus-

tacea: Cladocera). Proceedings of the Biological Society of

Washington 3: 666–680.

Xu, S., P. D. N. Hebert, A. A. Kotov & M. E. Cristescu, 2009.

The noncosmopolitanism paradigm of freshwater zoo-

plankton: insights from the global phylogeography of the

predatory cladoceran Polyphemus pediculus (Linnaeus,

1761) (Crustacea, Onychopoda). Molecular Ecology 18:

5161–5179.

100 Hydrobiologia (2011) 676:57–100

123