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competition and/or smothering from introduced spe-

cies (Thom as, 1997; Bogan, 1998; Seddon, 1998;

McAllister et al., 2000; Ponder & Walker, 2003). As

with damming, it is often not just localized damage,

but the cascade of effects both up and downstream

that impact a wide range of communities.

Conservation priorities

Despite signiﬁcant roles in human cultural history,

molluscs, as with many invertebrates, have a poor

public image (Kay, 1995a). This attitude further

impedes allocation of meagre conservation reso urces

in competition with the demands from larger charis-

matic animals and plants (Ponder, 1995; Wells, 1995;

Bouchet & Gargominy, 1998; Seddon, 1998; Ly deard

et al., 2004). The often drab-coloured and uncharis-

matic freshwater species, arguably facing the most

serious risks and most deservedly meriting public

concern and action, are desperately in need of

champions.

Effective management of these threatened re-

sources is often complicated by habitat fragmentation

or political obstacles, as large rivers and lakes are

often transnational. Although often not feasible,

narrow range endemics inhabiting a single stream

or spring are best pres erved within large protected

areas (Ponder, 1995), as many critical sites outside

reserves can be so small that they attract little interest

from conservation agencies and can suffer from edge

effects. Moreover, as noted above, currently recog-

nized species do not necessarily reﬂect natural

evolutionary entities, with clear implications for

devising accurate and effective management strate-

gies based on species-targeted approaches. In

contrast, habitat-based conservation strategies cir-

cumvent many of these problems and may be the

preferred option in many circumstances (e.g., Ponder,

2004b).

Major museum collections are a key component of

understanding the spatial distribution of species, both

past and present (Wells, 1995; Ponder, 1999, 2004b),

but much of this information is not yet accessible to

the global community via computerized databases.

This lack of access hampers or prevents assessm ent

of conservation status by contributors to the Red

List—a vital communication tool between scientists

and conservation strategists and managers, as well as

local or national conservation agencies. Currently,

Mollusc Action Plans, as calle d for by the IUCN

Species Survival Commission (SSC), are limited in

the extent to which they can offer explicit recom-

mendations in comparison with well-known taxa

(e.g., tetrapods) (Bouchet & Gargominy, 1998). With

the limitations discussed above, the magnitude of the

threat of extinction as indicated by the IUCN Red

List of Threatened Species, is certainly a grave

underestimate.

Conserving our molluscan resources will effec-

tively require a multiplicity of approaches, including

research (systematics, ecology, life history, physiol-

ogy, morphology, genetics), inventories (distribution,

population size, biogeography), enhanced database

infrastructure including digitization of signiﬁcant

museum collections, mitigation of human impacts,

active intervention to promote recovery (including

removal of invasive species, captive breeding

programs, re-introdu ction, restoration of habitat),

training in taxonomic expertise and enhanced com-

munication and outreach (Kay, 1995b; Ponder, 1995;

Seddon, 1998; McAllister et al., 2000; Lydeard et al.,

2004). But considering the already-documented

severity of the plight of freshwater gastropods, these

strategies cannot proceed in a step-wise linear

fashion—by then it will be too late (e.g., Wells,

1995; Lydeard et al., 2004; Ponder, 2004b).

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123

FRESHWATER ANIMAL DIVERSITY ASSESSMENT

Global diversity of large branchiopods (Crustacea:

Branchiopoda) in freshwater

Luc Brendonck Æ D. Christopher Rogers Æ

Jorgen Olesen Æ Stephen Weeks Æ Walter R. Hoeh

 Springer Science+Business Media B.V. 2007

Abstract With about 500 known species world-

wide, the large brachiopods are a relatively small

group of primitive crustaceans. With few exceptions

they live in temporary aquatic systems that are most

abundant in arid and semi arid areas. As many

regions remain unexplored and as especially the

number of species in clam shrimps and tadpole

shrimps is underestimated due to difﬁcult identiﬁca-

tion, the species list will increase with future surveys.

The Branchiopoda are monophyletic, but inter-ordi-

nal relationships, as well as many evolutionary

relationships at lower taxonomic levels are still

unclear. Ongoing molecular studies will more accu-

rately depict species diversity and phylogenetic

patterns. With the exception of some anostracan

families, most families are not restricted to the

northern or southern hemisphere or speciﬁc zoogeo-

graphical regions. Large branchiopods are used for

the assessment of the quality and function of

temporary wetlands. Due to the reduction in number

and quality of temporary wetlands, several species

became endangered and are red listed by the IUCN.

Keywords Large branchiopod diversity 

Anostraca  Spinicaudata  Laevicaudata 

Cyclestherida  Notostraca  Temporary pools

Introduction

The crustacean class Branchiopoda (clam shrimp

(Spinicaudata, Laevicaudata, and Cyclestherida),

tadpole shrimp (Notostraca), and cladocerans

[=Phyllopoda] plus fairy shrimp [=Anostraca]) is a

morphologically diverse group of ecologically impor-

tant, largely freshwater organisms that has a fossil

record extending back to the Upper Cambrian

(Walossek, 1993). Breeding systems within the class

Guest editors: E.V. Balian, C. Le

que, H. Segers &

K. Martens

Freshwater Animal Diversity Assessment

Electronic supplementary material The online version of

this article (doi:10.1007/s10750-007-9119-9) contains supple-

mentary material, which is available to authorized users.

L. Brendonck (&)

Laboratory of Aquatic Ecology, KULeuven,

Deberiotstraat 32, Leuven 3000, Belgium

e-mail: Luc.Brendonck@bio.kuleuven.be

D. C. Rogers

EcoAnalysts, Inc., 166 Buckeye St., Woodland, CA

95695, USA

J. Olesen

Zoological Museum, University of Copenhagen,

Universitetsparken 15, Copenhagen Ø 2100, Denmark

S. Weeks

Integrated Bioscience Program, Department of Biology,

The University of Akron, Akron, OH 44325-3908, USA

W. R. Hoeh

Department of Biological Sciences, Kent State University,

Kent, OH, USA

123

Hydrobiologia (2008) 595:167–176

DOI 10.1007/s10750-007-9119-9

are highly varied, including dioecy, androdioecy,

parthenogenesis, and cyclic parthenogenesis (Sass-

aman, 1995; Weeks et al., 2006a, b). Branchiopoda

without cladocerans are commonly known as the

‘‘large branchiopods.’’

Most large branchiopod species rely on seasonal

wetlands such as playas, vernal (rain and snow-melt)

pools, salt ﬂats, and alkali pans, while other species

occur in permanent playas, ﬁshless alkali lakes, and

salt lakes (Dumont & Negrea, 2002). These habitats

are, for the most part, seasonal pools that are dry for a

signiﬁcant portion of the year, or several years

(Dumont & Negrea, 2002).

The vast majority of anostracans are omnivorous

ﬁlter feeders, indiscriminately ﬁltering particles from

the water column with their continually beating

thoracopods (Brendonck, 1993a, b). A few species

are predators on rotifers , copepods, cladocerans, and

other Anostraca (Boudrias & Pires, 2002; Rogers

et al., 2006). The tadpole shrimp are predominantly

benthic and omnivorous, feeding on detritus and

living or dead organisms (Martin, 1992). Clam

shrimp typically feed nonselec tively on detritus and

algae in suspension (Belk, 1982).

Branchiopod crustaceans rely on banks of resting

eggs (or ‘‘cysts;’’ Fig. 1) to bridge periods of drought

or frost (Brendonck, 1996) and to buffer against the

effects of environmental variability. The eggs lay

dormant in the substrate until the pool dries and reﬁl ls

during the subsequent rains. In the temporally

ﬂuctuating environment of temporary aquatic habi-

tats, usually only part of the dormant eggs, if any,

Fig. 1 Various large branchiopod egg morphology: (a) Streptocephalus proboscideus (Anostraca); (b) Streptocephalus indistinctus

(Anostraca); ( c) Eulimnadia cylindrova (Spinicaudata); (d) Streptocephalus ovamboensis (Anostraca), (e) Streptocephalus zuluensis

(Anostraca)

168 Hydrobiologia (2008) 595:167–176

123

hatches during each ﬁll (Hildre w, 1985; Brendonck

et al., 1998). This process can lead to the generation

of an egg bank that can remain viable for decades or

possibly centuries without re-hydration (Belk, 1998),

and can harbor potentially great genetic and species

diversity (Ellner & Hairston, 1994). The external

morphology (shape and ornamentation; Fig. 1) of

eggs is an important taxonomic tool (Mura, 1986;

Belk, 1989; Martin, 1989; Martin & Belk, 1989;

Brendonck et al., 1992; Brendonck & Coomans,

1994a, b). In many cases this allow s the assessment

of the temporary pool communities even when no

water is present.

Large branchiopod crustaceans are arguably the

least known of all macroscopic invertebrates in

temporary inland waters even though they are the

ﬂagship group for these ecosystems and for tempo-

rary pool invertebrates in general (Colburn, 2004).

Species/generic diversity

In many areas of the world, the diversity, species

composition, and conservation status of large bran-

chiopods remain largely unknown. We therefore

expect to discover and describe many new taxa in

these largely unexplored areas (e.g., South America,

northern, western and eastern Africa, Western Aus-

tralia, and Asia).

Anostraca

Anostracans (Fig. 2a) are elongat ed crustaceans,

which lack a carapace and are constantly swimming

on their backs in the water column. The Anostraca are

by far the most taxonomically diverse group at all

levels (Tables 1, 2). There are *300 species on all

continents (including Antarctica; Belk & Brtek, 1995,

1997; Dumont & Negrea, 2 002), currently arranged

in 26 genera and eight families (Tables 1, 2; Weekers

et al., 2002, Rogers, 2002b, 2006). Nearly 1/4 of

these species are known only from the type localities,

or from \3 localities (Belk & Brtek, 1995, 1997).

Additionally, there are *20 undescribed species and

at least one undescribed genus.

Typically, anostracan species are differentiated

based upon the form and ornamentation of the male

second antennae, which are modiﬁed into large

claspers to grasp the female during copulation

(Rogers, 2002a). Linder (1941) demonstrated the

importance of copulatory structures, especially the

male genitalia, in deﬁning genera. Starting from this

base, Belk (1991, 1995), Brendonck (1995), Bren-

donck & Belk (1997), and Rogers (2002b, 2006)

established genital morphology as the deﬁning crite-

ria for anostracan genera. To date, most of the

taxonomy and phylogeny has been based on the

morphology of these antennal and genital characters.

Notostraca

The order Notostraca (tadpole shrimp; Fig. 2c, d) is

composed of the family Triopsidae and includes two

genera (Triops Schrank, 1803 and Lepidurus Leach,

1819; Tables 1, 2) of ‘‘living fossils’’ which have

undergone minimal gross morphological change

since their divergence over 250 million year s ago

(Longhurst, 1955).

The Notostraca exhibit plasticity in external mor-

phology, making the demarcation of species on this

basis a difﬁcult task (Rogers, 2001). The absence of

well-deﬁned criteria allowed taxonomists to describe

many ‘new species’ in such a way that the nominal

species of Triops and Lepidurus amounted to more

than 70 in the 1950s (Longhurst, 1955). Linder

(1952) and Longhurst (1955) reviewed the alpha

taxonomy of the Notostraca and recognized only

about 11 species with a wide geographic distribution.

Until recently, this classiﬁcation was extensively

used ‘‘even attaining the status of dogma’’ (Sassaman

et al., 1997). However, the genetic and molecular

studies of Sassaman et al. (1997), Suno-Uchi et al.

(1997), King & Hanner (1998), and Murugan et al.

(2002) have demonstrated that Linder’s and Long-

hurst’s classiﬁcations have long obscured

understanding of the real species-level diversity of

the Notostraca.

Notostracan systematics is further complicated by

the discovery of different modes of reproducti on

(Sassaman & Weeks, 1993; Sassaman, 1995). The

determination of the mode of reproduction is impor-

tant for the understanding of the variety of species.

Suno-Uchi et al. (1997) studied the three morpho-

species Triops cancriformis, T. granarius, and

T. longicaudatus from Japan, analyzing a segm ent

of the mt16S rRNA gene. They proposed that there

Hydrobiologia (2008) 595:167–176 169

123

are four, not three, phylogenetic species. King &

Hanner (1998) studied a fragment of the mt12S rRNA

gene in four nominal species of Lepidurus from

Canada and the USA, and deduced that there are ﬁve,

not four, reproductively isolated species, one of them

recently described (Rogers, 2001). Using the mt12S-

and mt16S rRNA genes, Murugan et al. (2002)

studied ﬁve Triops populations from Me

xico and

explored the phylogeny of the genus. Analysis of

mt12S rDNA data was in agreement with previous

allozyme studies (Sassaman et al., 1997), and showed

the nominal (morphological) species T. longicauda-

tus to be a mix ture of several species such that, of the

seven Triops American populations studied, six

phylogenetic species can be identiﬁed. These

molecular data, contrary to a phylogenetic proposal

based on morphology (Maeda-Martı

nez et al., 2000),

also indicated that two morphologically and repro-

ductively divergent forms can be grouped into a

single monophyletic clade, and that the Old World

species T. cancriformis may represent a lineage that

is independent from other species in that genus

(Murugan et al., 2002).

Spinicaudata, Laevicaudata, and Cyclestherida

These small, freshwater crustaceans have laterally

compressed bodies enclosed by a bivalved carapace

(Fig. 2b). Although clam shrimp are common

Fig. 2 Habitus of large

branchiopods: (a) adult

male Chirocephalus

diaphanus (Anostraca), (b)

adult Limnadia lenticularis

(Spinicaudata), (c) adult

Triops cancriformis

(Notostraca), (d) adult

Lepidurus apus

(Notostraca). (Drawings

from: Brendonck, 1989)

170 Hydrobiologia (2008) 595:167–176

123

Table 1 Species

distribution of Anostraca, Notostraca, Spinicaudata and Laevicaudata per family in zoogeopgrahic regions

PA NA NT AT OL AU PAC ANT World

Anostraca

110 64 33 56 11 48 1 1 307

Artemiidae 63211110 9

Parartemiidae 0000013+00 13

Branchinectidae 6 24 15 0 0 0 0 1 45

Thamnocephalidae 5 6 16 4 2 32 0 0 62

Streptocephalidae 16 15 0 24 7 2 0 0 56

Branchipodidae 9 0 0 26 0 0 0 35

Tanymastigitidae 80000000 8

Chirocephalidae 61 16 0 1 1 0 0 0 81

Notostraca

77212200 15

Triopsidae 77212200 15

Spinicaudata

*50 *15 *13 *20 *30 23 1 0 *150

Cyzicidae *20 6 2 *7 *10 10 0 0 *90

Leptestheriidae *15 1 *5 *8 *300 0 *37

Limnadiidae *15 *10 *10 *10 *12 13 1 0 *55

Laevicaudata 8 7 13 4 4 2 0 0 36

Lynceidae 8 7 13 4 4 2 0 0 36

PA, Palaearctic; NA, Nearctic; NT, Neotropical; AT, Afrotropical; OL, Oriental; AU, Australasian; PAC, Paciﬁc Oceanic Islands;

ANT, Antarctic

Several taxa are known from more than one region

Table 2 Genus distribution of Anostraca, Notostraca, Spinicaudata and Laevicaudata per family in zoogeopgrahic regions

PA NA NT AT OL AU PAC ANT World

Anostraca 16 11 10 6 6 4 1 1 26

Artemiidae 1 1 1 1 1 1 1 0 1

Parartemiidae 0 0 0 0 0 1 0 0 1

Branchinectidae 1 1 0 1 0 0 0 1 1

Thamnocephalidae 2 3 3 4 2 1 0 0 6

Streptocephalidae 1 1 1 0 1 1 0 0 1

Branchipodidae 2 0 4 0 1 0 0 0 5

Tanymastigitidae 2 0 0 0 0 0 0 0 2

Chirocephalidae 7 5 1 0 1 0 0 0 9

Notostraca 2 2 1 2 1 2 0 0 2

Triopsidae 2 2 1 2 1 2 0 0 2

Spinicaudata 9 5 5 4 6 5 1 0 12

Cyzicidae 3 2 2 1 3 2 0 0 4

Leptestheriidae 3 1 1 1 1 0 0 0 3

Limnadiidae 3 2 2 2 2 3 1 0 5

Laevicaudata 1 2 2 2 1 1 0 0 3

Lynceidae 1 2 2 2 1 1 0 0 3

PA, Palaearctic; NA, Nearctic; NT, Neotropical; AT, Afrotropical; OL, Oriental; AU, Australasian; PAC, Paciﬁc Oceanic Islands;

ANT, Antarctic

Hydrobiologia (2008) 595:167–176 171

123

worldwide, they have not been the subjects of intense

study. A few investigations have assessed their

genetics (Duff et al., 2004), phylogeny and biogeog-

raphy (Hoeh et al., 2006), and reproductive biology

(Weeks et al., 2005, 2006a, b; Scanabissi et al.,

2006), but most attention has been devoted to the

morphological systematics of these animals and

*116 species are currently recognized. The three

orders consist of ﬁve extant families and 19 genera

(Tables 1, 2). Traditionally the genus Cyclestheria

was considered to be part of the Sp inicaudata, but

Olesen (1998) and Spears and Abele (2000) sug-

gested that spinicaudatans are paraphyletic, with

respect to the Cladocera.

The systematics within the Spinicaudata has been

problematic for centuries, and the principal difﬁcul-

ties are still far from being resolved. Presently, the

Spinicaudata is subdivided into three families (Martin

& Davis, 2001) (Tables 1, 2), but the monophyly of

two of these (Cyzicidae and Leptestheridae) is highly

uncertain (the monophyly of the third, Limnadiidae,

is strongly supported; Hoeh et al., 2006). Similar

problems can be found at both the genus and species

levels in all three families. Spinicaudatans are well

known for showing great ‘morphological plasticity’

making species identiﬁcation exceptionally difﬁcult

in some taxa. The usual problems of poor descrip-

tions and lack of type material add to the difﬁculties.

Belk (1989) re-emphasized the importance of the

morphology of the outer covering of the desiccated

resting eggs as a taxonomic character.

Phylogeny

The monophyly of the Branchiopoda has been

strongly supported by recent phylogenetic analyses

(e.g., Spears & Abele, 2000) but inter-ordinal rela-

tionships within the Phyllopoda, as well as many

evolutionary relationships at lower taxonomic levels

throughout the class, have not been clearly elucidated

(e.g., Braband et al., 2002).

In last decades there were interesting rearrange-

ments in the systematics of higher taxa of the

Branchiopoda (Fryer, 1987; Walossek, 1993; Martin

& Cash-Clark, 1995). Clam shrimps, formerly

thought to be one order (the ‘‘Conchostraca’’), have

turned out to be paraphyletic with respect to the

Cladocera (the water ﬂeas; Olesen, 1998; Spears &

Abele, 2000; Braband et al., 2002), and probably also

with respect to the Notostraca (tadpole shrimps;

Stenderup et al., 2006). The ‘‘Conchostraca’’ are now

divided into the Laevicaudata and the Spinicaudata

(Fig. 2b) and the Cyclestherida.

Information on phylogenetic relationships in large

branchiopods is most advanced, but still fragmentary

in anostracans. The anostracan family Streptocepha-

lidae has been subjected to morphological (Hamer

et al., 1994a, b) and morphological-cladistic analyses

(Maeda-Martı

nez et al., 1995a, b). To date there are

only 5 phylogenetic studies using molecular data that

focused on the Anostraca: Branchinella (Remigio

et al., 2003), Parartemia (Remigio et al., 2001),

Streptocephalus (Daniels et al., 2004), and two

studies attempting to resolve familial relationships

(Remigio & Hebert, 2000; Weekers et al., 2002) with

one study focusing on the ordinal relationships (de

Waard et al., 2006). These stud ies generated more

questions about the relationships between the genera

(Rogers, 2002b; Weekers et al., 2002).

Present distribution and main areas of endemicity

Large branchiopods have a worldwide distribution

(Fig. 3), including the polar areas (e.g., the anostr-

acan Branchinecta gaini is rather widespread on the

antarctic peninsula), but reach their maximum abun-

dance and species richness in steppes and deserts,

where temporary water bodies abound. The vast

majority of species are fresh-water; however some

species of Branchinella, Streptocephalus, and Tham-

nocephalus, as well as all species of Parartemia and

Artemia, live in inland saline waters.

Family, generic, and species diversity of large

branchiopods at the level of the main zoogeograph-

ical areas are presented in Tables 1 and 2. Some

anostracan families are endemic to only one of the

areas such as Parartemiidae to Australasia and

Tanymastigitidae (Anostraca) to the Palearctic. Not-

ostracan and clam shrimp families are always

distributed over at least one of the zoogeographical

areas. Except for the former families, not one is

entirely restricted to the southern or northern hemi-

sphere, which would reﬂect a Gondwanaland or

Laurasia origin, respectively.

Some clam shrimp genera like Cyzicus and

Eocyzicus appear to be Laurasian, with their current

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123