JOURNAL OF CRUSTACEAN BIOLOGY, 27(2): 165–183, 2007
MONOPHYLY AND PHYLOGENY OF BRANCHIOPODA, WITH FOCUS ON
MORPHOLOGY AND HOMOLOGIES OF BRANCHIOPOD PHYLLOPODOUS LIMBS
Jørgen Olesen
Zoological Museum, University of Copenhagen, Universitetsparken 15, DK-2100
Copenhagen Ø, Denmark ([email protected])
ABSTRACT
Aspects of the evolution of the branchiopod crustaceans are reviewed and discussed. Despite views to the contrary presented in recent
textbooks, the monophyly of Branchiopoda is defended based on morphological characters. The crown group Branchiopoda is supported/
diagnosed by a set of synapomorphies relating to limb morphology of both larvae and adults, including, among others, a similar naupliar
swimming/feeding apparatus, a similar development of trunk limbs, and a similar morphology of adult trunk limbs with six endites (number
reduced later) and an unsegmented endopod. Phyllopodous limbs are among the most well-known features of Branchiopoda, but it is
uncertain whether the phyllopodous nature of the limbs in itself can be considered a synapomorphy for this group, because the limbs of other
crustaceans, both recent and fossil, also can be characterised as at least partly phyllopodous. Homologies of branchiopod trunk limbs to
those of other crustaceans are discussed; based on similarities to trunk limbs of certain ‘Orsten’ fossils, it is concluded that the large,
undifferentiated ‘corm’ of the limb most likely is an enlarged basis. Within Branchiopoda, strong evidence for a monophyletic Phyllopoda
sensu Preuss (all branchiopods except anostracans) is presented. A monophyletic Diplostraca is also preferred based on morphological
information, and the supporting characters for this group are listed. A remarkable branchiopod crustacean from the Devonian has recently
been described with morphological features combining those of Notostraca and ‘Conchostraca’; it has major significance for the
understanding of early branchiopod evolution. The question of a marine versus freshwater origin of Branchiopoda is discussed.
INTRODUCTION
like?; and 3) what was the habitat of the first branchiopods?
A first step toward answering such questions with some
precision, or at least to place them in a testable framework,
is to produce a robust phylogeny.
There has been much recent focus on the molecular
contribution to the understanding of branchiopod phylogeny
(Taylor et al., 1999; Braband et al., 2000; Spears and Abele,
2002; Stenderup et al., 2006). In contrast, very few fairly
comprehensive morphology-based phylogenetic analyses of
this group are available in the literature, and it is therefore
clear that the potential utility of morphological datasets are
far from being fully explored. Much morphological information of high quality for many taxa is available in
the literature, some of which formed the basis for the first
phylogenetic analyses of Branchiopoda (Olesen, 1998;
Negrea et al., 1999). In particular, much information
concerning internal anatomy still needs to be included and
possibly re-interpreted in a modern phylogenetic context.
Furthermore, although Branchiopoda may be considered
well known compared with many other less accessible
crustacean taxa, new morphological information generated
by new methods in a consistent phylogenetic framework is
needed.
Various papers by Olesen and co-workers have focussed
on the ontogeny of appendages and other external features
as an additional source of information for establishing the
phylogeny of Branchiopoda. The intention has been to study
the ontogeny (larval development, embryology) in detail,
using the same study technique in order to make the results
comparable across taxa, with emphasis on limb morphology
and homologies. Results are now available for all major taxa
of Branchiopoda (Figs. 2, 3), either published or underway
(Olesen, 1999, 2004, 2005; Olesen et al., 2001, 2003;
Branchiopod evolution, phylogeny, and classification have
in recent years attracted considerable interest (Fryer, 1987;
Walossek, 1993; Olesen, 1998, 2004; Negrea et al., 1999;
Taylor et al., 1999; Spears and Abele, 2000; Braband et al.,
2002; Swain and Taylor, 2003; Stenderup et al., 2006).
While the monophyly of Branchiopoda itself is supported by
most workers (for exceptions see below), recent research has
challenged the traditional view of intrinsic branchiopod
systematics. The monophyly of taxa established long ago,
such as Conchostraca (clam shrimps), Spinicaudata, and
Cladocera (water fleas), and accepted without dispute since
the days of Sars, has been called into question. ‘Forgotten’
taxa, such as Diplostraca (bivalved branchiopods) and
Gymnomera (raptorial cladocerans), have been revived
(Walossek, 1993; Olesen, 1998; Braband et al., 2002). Yet
other new concepts have been suggested, such as Cladoceromorpha (constituted of Cyclestherida and Cladocera)
(Olesen et al., 1997; Ax, 1999). In works using a modern
phylogenetic approach (Fig. 1), Spinicaudata, Cladoceromorpha, and Cladocera are generally supported, while the
validity of other taxa like Phyllopoda (sensu Preuss, 1951)
(all branchiopods except anostracans) and Diplostraca is still
being discussed (Olesen, 1998; Negrea et al., 1999; Spears
and Abele, 2000; Braband et al., 2002). For example,
Diplostraca have recently been suggested to be paraphyletic
(Fig. 1) with respect to Notostraca based on molecular data
(Stenderup et al., 2006).
It has been widely accepted in recent years that evolutionary questions are best addressed on the basis of a
well-supported phylogeny. Some interesting questions with
respect to Branchiopoda are: 1) how old is Branchiopoda?;
2) what did the common ancestor of Branchiopoda look
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Fig. 1. Phylogeny of Branchiopoda based on morphological information. The alternative position of the clade Calmanostraca (dashed line and question
mark) is based on recent molecular evidence (see Stenderup et al., 2006). Illustrations: Walossek (1993) (1 and 6), Martin (1992) (2 and 5), Scourfield (1926)
(3), Fayers and Trewin (2003) (6), Sars (1896) (7), Sars (1898) (8), Olesen et al. (1997) (9), Sars (1993) (12), Sars (1902) (13), Sars (1901) (10), Fryer (1974)
(11).
Olesen and Grygier, 2003, 2004). Most existing ideas
concerning the classification of Branchiopoda are based on
external limb morphology (as for other crustaceans). The
mentioned works on branchiopod limb morphology have in
many cases made it possible to re-evaluate the classical limb
characters used in branchiopod systematics. This paper
reviews some of this information. Since the presence of
phyllopodous/foliaceous trunk limbs traditionally has been
considered a key character of Branchiopoda, special attention will be devoted to the ontogeny, morphology, and
phylogenetic significance of this type of limbs. There has
been recent controversial interest for identifying homologies
of branchiopod trunk limbs to those of other Crustacea
(Walossek, 1993; Ferrari and Grygier, 2003; Williams,
2004), which has prompted a re-evaluation of the subject in
this study. Studies addressing limb homologies have a long
tradition in arthropod systematics and extraordinarily much
information is available in old and more recent literature,
e.g., see references in Walossek (1993) and Boxshall
(2004). The present work on branchiopod limb homologies
may prove important in a broader Crustacea/Arthropoda
context, since it attempts to define Branchiopoda based
primarily on limb morphology with more precision than has
been done hitherto.
IS BRANCHIOPODA MONOPHYLETIC?
Brief History of Branchiopoda as a Taxonomic Unit
Whether the taxon Branchiopoda is monophyletic or not
obviously depends on which groups are included in it. As
the taxon was composed originally by Latreille (1817)—
including some taxa we now consider branchiopods
(‘Apus’, ‘Branchipus’, ‘Artemisia’, ‘Eulimene’, ‘Lynceus’,
‘Daphnia’, and ‘Polyphemus’), but also copepods, ostracodes, branchiurans, and even xiphosurans—it was clearly
not monophyletic. The taxa carcinologists presently group
in Branchiopoda (Anostraca, Notostraca, ‘Conchostraca’,
and Cladocera) have been recognised by many authors as
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167
Fig. 2. Ventral views of examples of branchiopod larvae and embryos (Anostraca, Notostraca, Cyclestherida, Spinicaudata, Laevicaudata, Cladocera). The
photographs are not to the same scale; the exact sizes can be seen in the original publications. From Olesen (1999), Olesen et al. (2003), Olesen and Gygier
(2004), Møller et al. (2003, 2004), and Olesen (2005).
forming a natural group together. However, as seen in recent
textbooks, the validity of Branchiopoda is apparently not
universally accepted. Gruner (1993), in his authoritative
update of Kaestner’s (1967) textbook on Crustacea and
other arthropods did not treat Branchiopoda as a distinct
taxon, but instead replaced it with two subgroups given
equal rank, Anostraca and Phyllopoda (the latter comprising
all the non-anostracan branchiopods). This arrangement was
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Fig. 3. Lateral views of examples of branchiopod larvae (Anostraca [first antennae not pictured], Notostraca, Cyclestherida, Spinicaudata, Laevicaudata,
Cladocera). The photographs are not to the same scale; the exact sizes can be seen in the original publications. From Olesen (1999), Olesen et al. (2003),
Olesen and Gygier (2004), Møller et al. (2003, 2004), and Olesen (2005).
probably based on some problematic conclusions of Preuss
(1951, 1957) in his otherwise fine works on trunk limb
morphology.
Preuss (1951, 1957) was the first to argue convincingly
that Notostraca, ‘Conchostraca’, and Cladocera form a
natural group, which he named Phyllopoda. Based on what
he wrongly believed were differences in trunk limb
morphology, and a number of other differences, between
Anostraca and his Phyllopoda, he rejected Branchiopoda as
a natural group. He identified the true exopod in Anostraca
as the ‘endopod’, and the true epipod as the ‘exopod’, and
therefore concluded that the trunk limbs of Anostraca are
very different from those of Phyllopoda. For example, in his
interpretation, the anostracan ‘exopod’ lacks musculature
(because it was actually the epipod or the ‘gill’). This wrong
interpretation was probably caused by the fact that the
endopodal part of the limb in Anostraca is not articulated
to the remaining limb (see Fig. 10B), and he thus named
it ‘endite 6’. However, no such fundamental differences are
present between the trunk limbs of Anostraca and
Phyllopoda. Even if Preuss’ interpretation were true, it
would still not be sufficient evidence to reject Branchiopoda
since there might be other similarities between Anostraca
and Phyllopoda (some are demonstrated below).
Other recent authors besides Gruner (1993) have
seemingly adopted Preuss’ (1951, 1957) flawed conclusions. Ax (1999), probably based partly on Gruner (1993),
left out Branchiopoda as a separate entry, and this caused
the new author team (Ruppert et al., 2004) of the seventh
edition of the Barnes textbook on ‘Invertebrate Zoology’
OLESEN: MONOPHYLY AND PHYLOGENY OF BRANCHIOPODA
also not to treat Branchiopoda as a distinct taxon. This
omission of Branchiopoda in recent influential invertebrate
textbooks is unfortunate. As will be shown below, there are
good reasons for retaining Branchiopoda in any classification of Crustacea, for example as a separate class as in the
scheme of Martin and Davis (2001).
A recent surprise is the placement of the Insecta inside
Branchiopoda (as constituted in the present work) in a
preliminary cladogram by Schram and Koenemann (2004).
In their tree, Insecta branches off between Lepidocaris
rhyniensis Scourfield, 1926 (Lipostraca) and a clade consisting of the recent Branchiopoda. In light of the many
potential synapomorphies between Lepidocaris and the
recent Branchiopoda mentioned below and in Olesen
(2004), which would then have to be considered lost in
the Insecta, I consider this unlikely—at least until convincing synapomorphies between the Insecta and the recent
Branchiopoda, not present in Lepidocaris, have been
identified. To evaluate the hypothesis of Schram and
Koenemann (2004) further, it will be crucial to include in
a revised dataset the potential branchiopod synapomorphies
mentioned in the present work and elsewhere.
To those dealing directly with the branchiopods it may
seem odd that there are such recent examples of works
not recognising Branchiopoda. On the other hand it is clear
that Branchiopoda constitute a rather diverse assemblage
of taxa, about which it is virtually impossible to mention
anything they all have in common that is not at the same
time shared with many other crustaceans. Martin (1992)
precisely described Branchiopoda as constituting ‘a curious
combination of morphological plasticity and evolutionary
stasis’. On this background it is appropriate to attempt
a more precise, synapomorphy-based definition/diagnosis of
Branchiopoda.
Calman’s (1909) Attempt to ‘Define’ Branchiopoda
Calman (1909) was probably the first who recognised
Branchiopoda with its present content. However, his ‘definition’ cannot be directly translated into synapomorphies.
Many later definitions of the branchiopods either repeat
Calman (Tasch, 1969), or seem to be shortened versions of
the same (McLaughlin, 1980). Some attention will therefore
be devoted to Calman’s (1909) list of characters as an
exercise in scrutinising a classical definition in a modern
phylogenetic context. In the following, Calman’s (1909)
defining characters (in quotation marks) are evaluated one
by one. Practically all fall short as synapomorphies.
1. ‘‘Carapace may form a dorsal shield or a bivalve shell
or may be entirely absent’’ (Calman, 1909: 29).
Problem: A carapace is absent in Anostraca and present
in many other crustaceans (of which homologies are
poorly understood). Hence, the character cannot be
considered a synapomorphy of Branchiopoda.
2. ‘‘the number of trunk limbs varies greatly’’ (Calman,
1909: 29).
Problem: The fact that the number of trunk limbs varies
among different groups within Branchiopoda cannot in
itself be used as a synapomorphy.
3. ‘‘the posterior part of the trunk is without limbs and
usually ends in a caudal furca’’ (Calman, 1909: 29).
4.
5.
6.
7.
8.
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Problems: Many other crustaceans have the posterior
part of the trunk without limbs and many branchiopods
have limbs along the entire trunk (Spinicaudata,
Laevicaudata, and Cyclestherida), so this character
can not convincingly be considered a branchiopod synapomorphy. A caudal furcae (¼ caudal rami of telson or
furcal rami) is also present in many other recent and fossil
Crustacea and is therefore a symplesiomorphy.
‘‘the antennules are generally reduced and unsegmented’’ (Calman, 1909: 29).
Problem: Antennular morphology of certain branchiopod fossils, all described after Calman (1909), conflicts
with this character. The antennules of Lepidocaris
rhyniensis (Lipostraca) are three-segmented (Scourfield,
1926) and the antennules of Almatium gusevi (Chernyshev, 1940) (Kazacharthra) apparently have about 10(?)
segments (McKenzie et al., 1991; Walossek, 1993).
Also, the antennules of Rehbachiella kinnekullensis
Müller, 1983 cannot be described as ‘reduced’ and
‘unsegmented’ (Walossek, 1993). Hence this defining
character for Branchiopoda is outdated as it is phrased
above, mostly due to the later discovery of certain wellpreserved fossils. A more detailed approach will be
needed in the future to include information for the
antennules of Branchiopoda.
‘‘the [adult] mandibles have no palp or only a vestige of
one’’ (Calman, 1909: 29).
Problem: Since Calman (1909), Cephalocarida and
Remipedia have been discovered, which also have no
palps as adults. Hence, the absence of a mandibular palp
is not unique to Branchiopoda and it is therefore
uncertain whether it is a (convergent) synapomorphy of
this taxon or whether it is a synapomorphy for a larger
crustacean assemblage.
‘‘the maxillae are reduced or absent’’ (Calman, 1909: 29).
In Lepidocaris, the pair of limbs that are considered to be
the maxillules are not reduced in size, at least not in
males, in which they are claspers. Hence, assuming that
Lepidocaris is correctly placed as an in-group branchiopod (see Fig. 1), reduced maxillules cannot be a synapomorphy of Branchiopoda. In contrast, the reduced
maxillae can well be a synapomorphy of Branchiopoda
(see Schram, 1986 and Schram and Koenemann, 2001 for
another interpretation of Lepidocaris limb homologies
and its phylogenetic position).
‘‘the trunk limbs, which vary greatly in number, are
generally of uniform structure, rarely pediform, generally foliaceous and lobed’’ (Calman, 1909: 29).
Problems: Both the ‘uniform structure’ and the ‘foliaceous and lobed’ nature of the branchiopod trunk limbs
are present in other Crustacea, such as Cephalocarida and
various ‘Orsten’-microfossils. Another point was raised
by Ferrari and Grygier (2003), who demonstrated that
traces of tagmosis exist in spinicaudatan branchiopods.
Trunk limb morphology, homologies, and phylogenetic
significance are treated in more detail below.
‘‘the position of the genital apertures varies greatly’’
(Calman, 1909: 29).
Problem: Variation in the position of the genital
openings cannot in itself be a synapomorphy.
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9. ‘‘the paired eyes are rarely absent’’ (Calman, 1909: 29).
Problem: Paired compound eyes are plesiomorphic for
Branchiopoda (out-group comparison).
10. ‘‘development usually with metamorphosis’’ (Calman,
1909: 29).
Problem: Many crustaceans undergo metamorphosis
during development. For this to be a synapomorphy for
Branchiopoda, it should be specified as a special type of
branchiopod metamorphosis, which is not possible.
Anostraca usually have anamorphic development and
cladocerans (and Cyclestheria) direct development.
Only clam shrimps show something like a metamorphosis, but not a very striking one (see reviews by
Walossek, 2003; and Olesen, 2004).
11. ‘‘young hatched in nauplius or metanauplius stage’’
(Calman, 1909: 29).
Problem: Many crustaceans hatch at a nauplius or
metanauplius stage, so this feature does not qualify as
a branchiopod synapomorphy. Instead, some naupliar
details indeed can be considered branchiopod synapomorphies, but this will be treated in more detail below.
Consequently, the definition of Branchiopoda by Calman
(1909) cannot be translated directly into synapomorphies.
The one or two exceptions pertain to mouthpart reduction,
not morphological novelties originating in this group. This
is for several reasons no great surprise. Calman’s definition
was obviously formulated to include particularly descriptive
characters. New discoveries, especially of fossils since
Calman wrote his textbook, has also diluted the definition
(see updated synapomorphy list below).
Importance of Fossils and Cladistics for
Branchiopod Systematics
For at least two reasons a more detailed approach to
evaluating the monophyly of the branchiopods is necessary.
First, our knowledge of the morphology of various
branchiopods has increased significantly in recent years,
both of larvae and adults, and of both extant and extinct
taxa. Second, in the last decades, phylogenetic methodology
has been refined considerably. A broad definition of
Branchiopoda is thus no longer satisfying. The question of
how to integrate the branchiopod-like fossils in the classification is important, as has been discussed in detail by
Walossek (1993), Walossek and Müller (1998), and Olesen
(2004). These authors, mostly based on concepts presented
by Ax (1985) and Lauterbach (1989), have highlighted
the importance of a precise methodology when combining
extant and extinct branchiopods.
The definition of Branchiopoda supported in this account,
which is also the most practical, flexible, and ‘everlasting’
kind of definition (at least as seen from the perspective of
a ‘neontologist’), is a crown group definition. Branchiopoda
is defined as comprising the latest common ancestor to all
recent branchiopods and all its descendents. This definition
ensures some stability in the composition of Branchiopoda,
since at least all recent taxa are included at any time, but it
also allows for any presently known, or later discovered,
extinct taxa to be included in Branchiopoda if necessary.
Rehbachiella kinnekullesis, for which Walossek (1993)
suggested a branchiopod affinity, can then be treated as
branchiopod stem lineage representative in a Branchiopoda
s. lat. or even in a pan-Branchiopoda, as suggested by Olesen
(2004). The branchiopod synapomorphies mentioned by
Walossek (1993) (ventral sternitic food groove, complicated
filtering system) are in this account recognised as synapomorphies for Branchiopoda s. lat. In contrast, the synapomorphies below deals with the crown-group Branchiopoda
in which Rehbachiella kinnekullensis is not included since it
shares none of the listed characters (see also Olesen, 2004).
Synapomorphies of Branchiopoda
(crown-group or s. str.)
Below follows a list of synapomorphies of the branchiopods. Some of the larval characters were already pointed out
by Sanders (1963) and summarised by Martin (1992), but
have since been explored in more detail (Møller et al., 2003,
2004; Olesen and Grygier, 2003, 2004; Olesen 2004, 2005).
None of the listed features are present in all branchiopods.
1. Larval antenna 1 unsegmented with distal setation only
(Fig. 4).
2. Larval antenna 2 with coxal masticatory spine, which
becomes branched after one of the first molts (Figs. 5, 6,
Olesen, 2004).
3. Larval antenna 2 with long characteristic basipodal seta
with two characteristic rows of long setules (involved in
feeding) (Figs. 5, 6, Olesen, 2004).
4. Larval antenna 2, endopod with distal setation only
(Fig. 6) (first suggested by Sanders, 1963).
5. Larval antenna 2, length of protopod more than one-half
total length of limb (Fig. 2, 6) (first suggested by
Sanders, 1963).
6. Larval mandible with uniramous, three-segmented palp
(basis plus two endopod segments) with largely same
setation in all taxa (Fig. 7, Olesen, 2004).
7. Adult second maxillae significantly reduced. Studied by
Cannon and Leak (1933), but are in need of a restudy.
8. Adult mandible of rolling-grinding type; gnathal edge
consisting only of large molar part (Richter, 2004).
9. Adult trunk limbs with unsegmented endopod (Fig. 10,
Olesen, 2004).
10. Adult trunk limbs with six endites (Fig. 10) (Olesen,
2004). The number of endites reduced further within
Branchiopoda and they are completely absent in various
cladocerans.
11. Larval trunk limbs as rows of lateral limb buds with the
future endites facing ventrally (Fig. 9). The status of
Lepidocaris rhyniensis is uncertain here (see Olesen,
2004).
TRUNK LIMBS OF BRANCHIOPODA—HOMOLOGIES TO OTHER
CRUSTACEAN LIMBS AND PHYLOGENETIC SIGNIFICANCE
Phyllopodous Limbs as a Synapomorphy
of Branchiopoda?
Many treatments of the systematics of the branchiopod
crustaceans have focussed on the characteristic phyllopodous morphology of the branchiopod trunk limbs, and
special attention will therefore be devoted to the morphology of these limbs here. As mentioned above, Calman
(1909), in his definition of Branchiopoda, noted that the
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171
Fig. 4. First antennae of larval and embryonic branchiopods. A, larva of Eubranchipus grubii (Anostraca); B, larva of Triops cancriformis (Notostraca); C,
larva of Leptestheria kawachiensis (Spinicaudata); D, embryo of Cyclestheria hislopi (Cyclestherida); E, embryo of Eurycercus glacialis (Cladocera). From
Olesen (1998), Olesen (1999), Olesen and Grygier (unpublished – L. kawachiensis), and Møller et al. (2003, 2004).
trunk limbs are generally of uniform structure and generally
foliaceous (phyllopodous) and lobed. This characteristic
of the branchiopods has since been repeated in different
versions (Tasch, 1969; McLaughlin, 1980), often as a
defining character. Others have described branchiopod trunk
limbs as ‘multibranched’, ‘posteriorly decreasing in size’,
‘serially similar’ (summarised by Ferrari and Grygier,
2003). However, no matter which way of characterising
branchiopod trunk limbs is preferred of those listed above,
most of the mentioned characteristics also apply to trunk
limbs in other recent crustaceans such as Cephalocarida and
Leptostraca, and ‘Orsten’ fossils like Rehbachiella (Fig.
8A), Bredocaris, and Dala. Hence, the above mentioned
branchiopod limb features (phyllopodous, serially similar,
etc.) are probably symplesiomorphies for Branchiopoda or,
if convergences developed in parallel in Branchiopoda and
other Crustacea, it would need further clarification. Instead,
a more detailed approach is necessary if limb related
synapomorphies of Branchiopoda are to be identified. A
consideration of various limb parts independently with close
attention to homologies is needed. Using this approach, the
trunk limb characteristics considered synapomorphies of
Branchiopoda in this account include the unsegmented
endopod, the six endites, and the lateral, elongate limb buds
of the larvae (from the list above). Whether the presence of
phyllopodous limbs (foliaceous with weakly defined
articulations) in itself is a synapomorphy for Branchiopoda
(in which case it has evolved in parallel to that of other
Crustacea) or is a symplesiomorphy is uncertain.
One should also hesitate using the presence of phyllopodous limbs as a synapomorphy for a larger assemblage of
crustaceans, since such a character would be much too
general and difficult to define precisely. When looking in
detail at phyllopodous limbs of Leptostraca and Branchiopoda, e.g., at the types of setae or the segmentation pattern,
it is not possible to corroborate homologies between these
limbs (Walossek, 1993; Martin and Christiansen, 1995).
Such a general character as ‘trunk limbs being phyllopodous’ should be abandoned in crustacean systematics, since
it includes limb types with a very different morphology.
Homologies of Branchiopod Trunk Limbs to Those
of Other Crustaceans
In this paper, and in my previous papers (Olesen, 1999;
Møller et al., 2003, 2004; Olesen and Grygier, 2003, 2004;
Olesen, 2004), the limb terminology for branchiopod trunk
limbs has basically been the one used by Fryer (1983, 1988)
and Walossek (1993). However, the homologies of the parts
of branchiopod limbs to those of other crustaceans have
over time been subject to quite a few disagreements
(Hansen, 1925; Snodgrass, 1956; Borradaille, 1926; Ferrari
and Grygier, 2003). The disagreements stem from the
phyllopodous and lobate nature of the branchiopod trunk
limbs. It is not a straightforward task to match the various
folds and lobes present in phyllopodous branchiopod limbs
with the distinct segment borders and limb parts (endopod,
exopod, basis, etc.) present in limbs of other crustaceans.
Some recent authors have highlighted these difficulties by
neutrally terming branchiopod limbs ‘branched’ (Williams
and Müller, 1996). However, in line with various other
authors, and in particular Walossek (1993), I believe that
comparative morphology using information available in the
general crustacean literature can bring us far. It is crucial to
consider a variety of taxa and not only a few ‘typical’
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Fig. 5. Naupliar feeding apparatus of branchiopod larvae. A, Eubranchipus grubii (Anostraca); B, Triops cancriformis (Notostraca); C, Eulimnadia
braueriana (Spinicaudata); D, Lynceus biformis (Laevicaudata). From Olesen and Grygier (2003), Møller et al. (2003, 2004), and Olesen and Grygier
(unpublished – L. biformis). Abbreviations: a2, antenna 2; ca, carapace; cox sp, coxal spine (a2); la, labrum; md, mandible.
crustaceans, and, most importantly, information on limb
morphology in the 500 million years old ‘Orsten’
crustaceans must be included.
It is clear that branchiopod trunk limbs at the general level
are homologous to other crustacean limbs. Various typical
crustacean limb parts including the endopod, exopod,
epipod, and endites can be recognised, and the trunk limbs
are basically biramous, patterned along a proximal/distal
axis as are the limbs of other crustaceans. This latter conclusion was also reached by Williams (2004), despite the
proximal/distal axis being directed laterally in early branchiopod ontogenesis. Notwithstanding the ‘multilobate’,
‘polyramous’, or ‘branched’ appearance of branchiopod
trunk limbs, a biramous nature of the limbs is suggested by
at least two types of evidence. 1) Ontogeny: the first limb
parts to become visible in the ontogeny of Cyclestheria
hislopi (Baird, 1859) and Eubranchipus grubii (Dybowski,
1860) are the laterally pointing tips of the future endopod
and exopod (see Fig. 8B; Olesen, 1999; Møller et al., 2004).
2) Fossil record: the ‘Orsten’ crustacean Rehbachiella
kinnekullensis has limbs very much like those of recent
branchiopods, but its limbs are more clearly biramous
(endopod and exopod) (see Figs. 8A, 10A; Walossek,
1993), without epipods. The phylogenetic position of
R. kinnekullensis as an early branchiopod (Fig. 1; Walossek,
1993) and its great age are both good reasons to assume its
type of trunk limb to be ancestral to those of present-day
branchiopods. In essence, only some endopodal segments
and endites of Rehbachiella need to be reduced, and an
epipod to be added (if not epipod secondarily lost in
Rehbachiella). The trunk limbs of Rehbachiella were probably partly phyllopodous (at least with an undifferentiated
basis). The term ‘polyramous’ has sometimes been employed for branchiopod limbs, but this is an unfortunate
term since it hides the biramous origin of the branchiopod
trunk limb. The stenopodous, clearly segmented trunk
limbs of certain predatory cladocerans are secondary
(Olesen et al., 2001).
Some of the disagreements in literature have pertained to
how the branchiopod trunk limbs precisely are homologous
to those of other crustaceans. There has been emphasis on at
least two questions:
1. What is the extent of the endopod? Is it unsegmented and
constituted only of the medio-distal lobe (see Fig. 10), as
advocated by Fryer (1988) and Walossek (1993), or does
it include some of the more proximal median lobes (¼
endites) as suggested for Lepidurus productus (Notostraca) and Caenestheriella gifuensis (Ishikawa, 1895)
(Spinicaudata) by Hansen (1925) and Ferrari and Grygier
(2003), respectively? In some literature the endopod is
even omitted, and the distal median lobe (endite) is
termed ‘endite 6’.
2. What are the homologies of the large, flattened, central
part of the limb, the part on which all the other parts
insert? Hansen (1925), and more recently Ferrari and
Grygier (2003), saw it as subdivided into three parts,
a precoxa, a coxa, and a basis, exactly as in certain
copepod limbs. Snodgrass (1956) and Borradaille (1926)
OLESEN: MONOPHYLY AND PHYLOGENY OF BRANCHIOPODA
173
Fig. 6. Swimming (second) antennae of branchiopod larvae. The photographs are not to the same scale. A, Eubranchipus grubii (Anostraca); B, Triops
cancriformis (Notostraca); C, Caenestheriella gifuensis (Spinicaudata). From Møller et al. (2003, 2004), and Olesen and Grygier (2004). Abbreviations: bas,
basis; cox, coxa; en, endopod; ex, exopod.
had comparable views (see Olesen et al., 2001; Olesen,
2004). Walossek (1993), on the contrary, homologised
this part with the basis of other crustaceans.
As has already been noted above, the original biramous
nature of the branchiopod trunk limbs is well-supported.
However, what is the extent of the endopod? In my view,
the morphology of the trunk limbs of Rehbachiella provides
the strongest clue to answer this question. Walossek (1993)
stressed the clear boundary between the segmented endopod
in the trunk limbs of Rehbachiella and the remaining part
of the limb, the basis (indicated by an arrow on Fig. 10A,
but see also Walossek, 1993 pls. 29:5 and 33:3). I follow
Walossek (1993) in considering this boundary homologous
to a similar boundary between an unsegmented endopod and
the more proximal part of the limb in recent branchiopods,
such as notostracans, laevicaudatans, and various spinicaudatans, but also in the branchiopod fossils Castracollis and
Lepidocaris (boundary marked by arrows in Fig. 10). Given
the phylogenetic position of Rehbachiella and given its
great age, it appears justified to assume that the type of
trunk limbs in recent branchiopods has evolved from a
Fig. 7. Mandibles of branchiopod larvae. A, Triops cancriformis (Notostraca); B, Eulimnadia braueriana (Spinicaudata). From Møller et al. (2003) and
Olesen and Grygier (2003). Abbreviations: bas, basis; en1, endopod segment 1; en2, endopod segment 2.
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 27, NO. 2, 2007
Fig. 8. Trunk limbs of fossil and recent branchiopods. A, yRehbachiella kinnekullenis, left side trunk limbs, median view; B, Cyclestheria hislopi
(Cyclestherida), left side trunk limbs, median view. From Walossek (1993; with permission) and Olesen (1999). Abbreviations: en, endopod; ex, exopod;
thp, thoracopod (Rehbachiella); tl1, trunk limb 1.
Rehbachiella type of limb by a reduction of the endopod and
by a reduction in the number of endites (status of epipod
uncertain; Richter (2002) argues for homology between
branchiopod and malacostracan epipods, which means that
Rehbachiella would have lost the epipod).
The idea of Hansen (1925) and Ferrari and Grygier
(2003) of the branchiopod trunk limb being composed of
a precoxa, coxa, basis, and a three-segmented endopod (six
limb parts) is problematic for several reasons. The idea was
formulated based on study of the limbs of Lepidurus
productus (Hansen, 1925) and Caenestheriella gifuensis and
Leptestheria kawachiensis (by Ferrari and Grygier, 2003),
which all have ‘traditionally’ been interpreted as having five
endites and an endopod along the inner margin (six median
limb parts) in adults, as do other notostracans and
‘conchostracans’. However, anostracans, Lepidocaris, and
Rehbachiella have a higher number of endites along the
inner margin, which, due to the early separation of
Rehbachiella (out-group comparison) from the lineage
leading to the remaining branchiopods, is more likely to
be the ancestral branchiopod condition. In this light, the
comparison between certain limbs of Copepoda and trunk
limbs of in-group branchiopods (see Ferrari and Grygier,
2003), with a reduced number of endites, is probably of less
value. At least the homologies of the copepod limbs in
question and those of branchiopods, e.g., Anostraca, with
a probably more ancestral number of trunk limb endites
should be accounted for. The number of median limb parts
in Anostraca (six endites and one endopod) is simply too
high to be fitted with the copepod limbs in question.
Another problem is the hypothesized presence of transverse
‘presumed boundaries’ in trunk trunk limbs of Caenestheriella giguensis (Spinicaudata) (Ferrari and Grygier, 2003:
fig. 9) of which there are no indication in the animals. In
a typical spinicaudatan trunk limb there are two relatively
clear boundaries that divides trunk limbs transversely (see
Fig. 10I), and it can argued to be simpler only to refer to
those when inferring limb homologies to other Crustacea.
One distinct proximal, transverse boundary is crossing the
limb approximately between where the first and second
endites split medially, and where the exopod inserts laterally
(Fig. 10I, see also drawings by Ferrari and Grygier, 2003).
Immediate distal to the fifth endite is another boundary. As
mentioned above, it seems justified by comparison to
Rehbachiella kinnekullensis to identify this latter boundary
as the boundary between the basis and the endopod (Fig.
10I, arrow). The significance of the proximal boundary is
more uncertain. It may be viewed as a coxa/basis boundary
either homologous or non-homologous to the coxa/basis
boundary seen in the limbs of so many other Crustacea
(see Boxshall, 1997). It is striking that a similar distinct
boundary is present in the Devonian Castracollis wilsonae
(Fig. 10E), which highlights the similarities between this
fossil and the spinicaudatans. When comparing a spinicaudatan trunk limb with a copepod maxilliped, Ferrari and
Grygier (2003) used the specific location at the limbs that
patterns the more distal parts as a reference point, and came
to the conclusion that the spinicaudatan trunk limb has
a three-segmented endopod. However, I have difficulties
matching the copepod maxilliped and the spinicaudatan
trunk limb the way Ferrari and Grygier (2003) suggest. I
find the development of the maxilliped of Temora longicornis (Copepoda) as shown by Ferrari and Ivanenko
(2001) difficult to compare with that of spinicaudatans and
Cyclestheria. As shown by Olesen (1999) in SEM for trunk
limbs of Cyclestheria hislopi, the boundary of the early limb
bud visible first is that between the future endopod and
exopod. The following median limb portions develop
gradually from proximal to distal, and the last parts to
separate from each other are the future endite 5 and the
unsegmented endopod (Fig. 9B, arrow). The view presented
by Ferrari and Grygier (2003), that this small limb portion
(future endite 5 and endopod) should be homologous to the
proximal endopodal segment of the copepod maxilliped (see
Ferrari and Ivanenko, 2001, fig. 15), upon which the authors
homologisation is based, is not very convincing. Furthermore, their homology scheme, which involves a threesegmented branchiopod endopod, will have to be balanced
with evidence in favour of an un-segmented endopod as that
presented above. A convincing homology scheme for
branchiopod limbs to those of other Crustacea will also
have to account for the branchiopod-like ‘Orsten-taxa’ and
perhaps the cephalocarids, which are all far more similar
(and probably closer related) to recent branchiopods than are
OLESEN: MONOPHYLY AND PHYLOGENY OF BRANCHIOPODA
175
Fig. 9. Branchiopod trunk limbs of larvae and embryos in various phases of development. A. Eubranchipus grubii (Anostraca); B, Cyclestheria hislopi
(Cyclestherida); C, Eulimnadia braueriana (Spinicaudata); D, Eubranchipus grubii (Anostraca); E, Eulimnadia braueriana (Spinicaudata); F, Cyclestheria
hislopi (Cyclestherida). From Olesen (1999), Møller et al. (2004), and Olesen and Grygier (2003). Abbreviations: e1 to e6, endites 1 to 6; en, endopod; ep,
epipod; ex, exopod.
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Fig. 10. Trunk limbs of fossil and recent branchiopods compiled from Walossek (1993) and various other authors and are drawn to different scales. Presumed
homologies are indicated by the labelling. Arrows point at articulation between basis and endopod. A, yRehbachiella kinnekullensis (from Walossek, 1993); B,
Anostraca – Branchinecta gaini (from Jurasz et al., 1983); C, yLepidocaris rhyniensis (from Scourfield, 1926); D, Laevicaudata – Lynceus sp. (from Martin et al.,
1986 and Walossek, 1993); E, yCastracollis wilsonae (from Fayers and Trewin, 2003); F, Notostraca – Lepidurus lynchi (from Linder, 1952); G. Kazacharthra
(from Novojilov, 1959); H, Cyclestherida – Cyclestheria hislopi (from Sars, 1887); I, Spinicaudata – Caenestheriella australis (from Sars, 1898; as ‘Estheria
elizabethae’); J, Cladocera – Leptodora kindtii (from Wagner, 1868). Abbreviations: e1 to e6, endites 1 to 6; en, endopod; ep, epipod; ex, exopod.
OLESEN: MONOPHYLY AND PHYLOGENY OF BRANCHIOPODA
the copepods. This was not done by Ferrari and Grygier
(2003). Based on limb studies of branchiopods such as
Lepidurus productus (Notostraca), Hansen (1925) reached
a similar conclusion as that of Ferrari and Grygier (2003)
concerning both the three-segmented status of the limb corm
and the endopod. In contrast to other ‘large’ branchiopods,
notostracan trunk limbs are subdivided into more or less
sclerotised portions, which Hansen (1925) interpreted as
corresponding to segments of other Crustacea. However,
much evidence suggests that notostracan trunk limb
morphology have become modified within Branchiopoda
and that the different sclerotised portions therefore cannot be
fitted with the segments of non-branchiopod crustaceans: 1)
Notostraca has an in-group position within Branchiopoda,
perhaps within a paraphyletic Diplostraca (Stenderup et al.,
2006), and is therefore not the obvious choice for comparing
with taxa outside Branchiopoda; and 2) a well-preserved
Devonian fossil (Castracollis), most likely a notostracan
stemgroup, has no indication of trunk limbs being
subdivided into sclerotic portions as those of notostracans
but instead have trunk limbs more similar to those of
spinicaudatans (Fig. 10E), and 3) none of the branchiopodlike ‘Orsten has trunk limbs similar to the Notostraca.
All in all I find it most likely that the large, proximal,
undifferentiated part of the trunk limb in Rehbachiella, and
by extension in other branchiopods, is an enlarged basis,
homologous to the basis in other crustaceans, and that the
endopod has become unsegmented in the recent branchiopods. It still needs to be clarified whether the unsegmented
endopod has appeared by fusion of its segments, reduction
to a single segment, or in another way.
MONOPHYLY OF PHYLLOPODA?
As noted above, probably the first to suggest that the
Notostraca, ‘Conchostraca’, and Cladocera together form
a natural group was Preuss (1951, 1957). He united these
taxa under the much used name Phyllopoda. Unfortunately,
based on misinterpretations of branchiopod limb homologies, he did not recognise Branchiopoda, but instead treated
his Phyllopoda and Anostraca as two separate taxa (see
above). Walossek (1993) reunited Preuss’ (1951, 1957)
Phyllopoda and Anostraca in Branchiopoda. Both Walossek
(1993) and Martin and Christiansen (1995) reviewed the use
of Phyllopoda as a taxonomic name. Martin and Christiansen (1995) could account for six different ways in which the
term Phyllopoda has been employed; most include all or
a subset of Branchiopoda, occasionally grouped together
with other crustaceans that have foliaceous limbs. Of these
various groupings, only Phyllopoda sensu Preuss (1951)
(all non-anostracan branchiopods) is with some likelihood
monophyletic, while time has shown all other meanings of
Phyllopoda to be para- or polyphyletic, or at least to have
a very uncertain status. It is therefore sensible to retain the
term Phyllopoda in the restricted sense as employed by
Preuss (1951, 1957), Flössner (1972), Walossek (1993), and
various other authors in the past half-century. This, of
course, does not mean that phyllopodous limbs are restricted
to Phyllopoda only. Limbs of anostracans and various other
crustaceans can with equal right be termed phyllopodous.
177
The following list briefly summarizes the characters that
demonstrate why Phyllopoda sensu Preuss (1951) should be
considered monophyletic.
1.
2.
3.
4.
5.
6.
Synapomorphies of Phyllopoda
Trunk limbs with five median endites followed by an
unsegmented endopod (Fig. 10D-I).
Compound eyes internal (Preuss, 1951).
Naupliar eye with four pigmented cups in contrast to
three as in Anostraca (Elofsson, 1966; Martin, 1992).
Telson with a pair of dorsal setae (Fig. 12; Linder, 1945;
Martin and Cash-Clark, 1995).
Oögenesis with three nutrition cells associated with each
oöcyte (Preuss, 1951).
Carapace first arising as ‘paired’ anlagen immediate
behind the head portion, but separate from this (Fig. 11).
[This character is largely similar to Walossek’s (1993)
‘secondary shield’, which has turned out also to be
present also in Notostraca (see Møller et al., 2003) and
therefore is a Phyllopoda character.]
ON A REMARKABLE NEW BRANCHIOPOD FROM THE EARLY
DEVONIAN—THE ORIGIN OF NOTOSTRACA
One of the most important recent discoveries that bear on
the elucidation of branchiopod evolution is the finding and
description of a entirely new Devonian Rhynie Chert
branchiopod, Castracollis wilsonae Fayers and Trewin,
2003, which has been suggested to be a stem group
notostracan (Fayers and Trewin, 2003). As with the
previously described branchiopod from this fauna, Lepidocaris rhyniensis Scourfield, 1926, the material is preserved
in three dimensions and the description is detailed due to
very fortunate preservation. Castracollis rhyniensis combines in a fascinating way typical notostracan and
‘conchostracan’ features. The morphology of the phyllopodous trunk limbs with their five endites and an unsegmented
endopod, the palp-less ‘rolling-grinding’ type of mandible
with a pars molaris occupying the entire gnathal edge, and
the sternitic food groove, leaves no doubt that this animal is
a branchiopod as this taxon is characterised above. The
specific number of five endites (and not six) and the
apparent lack of external eyes suggest that Castracollis
belongs to Phyllopoda. A more precise systematic/phylogenetic positioning of Castracollis is equivocal since it has
similarities both to Notostraca and ‘Conchostraca’. The
notostracan similarities include, as mentioned by Fayers and
Trewin (2003), in particular a many-segmented tail region
with densely set, ring-like segments; even the spine rows
on these body segments are very similar to those of recent
notostracans. Other similarities noted in the original
description, which are less well-defined morphologically,
include a non-filtratory morphology of the anterior series
of trunk limbs and a flattening of the anterior part of the
‘thorax’. According to Fayers and Trewin (2003) the
presence of a cephalo-thoracic shield (carapace), as in other
notostracans, is uncertain.
Similarities of Castracollis to the ‘conchostracans’ and
cladocerans include, in particular, a pair of biramous
swimming antennae, with rami of similar length and with
a similar number of segments (‘symmetrical’ rami). Within
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Fig. 11. Early development of carapace (arrow) in branchiopod larvae and embryos. A, Larva of Triops cancriformis (Notostraca); B, Larva of Eulimnadia
braueriana (Spinicaudata); C, Embryo of Cyclestheria hislopi (Cyclestherida); D, Embryo of Leptodora kindtii (Cladocera). From Olesen (1999), Olesen and
Grygier (2003), Olesen et al. (2003), and Møller et al. (2003). Abbreviations: a1, antenna 1; a2, antenna2; la, labrum; md, mandible; tl1, trunk limb 1.
Branchiopoda, possession of symmetrically biramous swimming antennae by adults, as seen in all the diplostracans
(Spinicaudata, Cyclestherida, and Cladocera), must be
apomorphic, while asymmetric antennal rami (small endopod, many-segmented exopod), as it is seen in branchiopod
larvae, adults of Lepidocaris, Rehbachiella and other
‘Orsten’ crustaceans, and Cephalocarida (out-groups), is
plesiomorphic. Since adults of the anostracans and notostracans have modified antennae, it is not absolutely clear
whether symmetrically biramous antennae is a novelty at the
diplostracan level, or whether such morphology was already
present earlier. Still, it cannot be excluded that the
possession of biramous, symmetrical swimming antennae
in adults is a synapomorphy for Castracollis wilsonae and
Diplostraca, thereby challenging the notostracan (or calmanostracan) affinities of Castracollis.
Turning now to other characters, the presence of two
longitudinal rows of spines dorsally on the telson suggests
a diplostracan affinity because such are present both in the
Spinicaudata and Cladoceromorpha (sometimes very enlarged). Another striking similarity between Castracollis
and certain spinicaudatan ‘conchostracans’ lies in the
specific structure of the trunk limbs. Those of Castracollis
are much more similar to typical spinicaudatan trunk limbs
than they are to any trunk limbs of Notostraca or
Kazacharthra (see Fig. 10). The detailed similarities include:
1) the same general limb proportions; 2) a clear division into
a proximal part (coxa?) bearing the distinct proximal endite,
and a larger distal part (basis?) bearing a lateral exopod, four
median endites, and an unsegmented endopod; and 3) the
presence of similar looking palps on the median endites of
the basis, in spinicaudatans only on the distal-most endite (if
Fig. 12. Anlagen of pair of telson setae in the Notostraca, Cyclestherida, and Cladocera. A, larva of Triops cancriformis; B, embryo of Cyclestheria hislopi;
C, embryo of Leptodora kindtii.
OLESEN: MONOPHYLY AND PHYLOGENY OF BRANCHIOPODA
present at all). One difference is the lack of an epipod in
Castracollis.
Castracollis thus exhibits similarities to both Notostraca
and Diplostraca, especially to Spinicaudata; however, I
tentatively support Fayers and Trewin (2003) in placing
Castracollis on the notostracan line in Calmanostraca (see
Fig. 1). The detailed similarities in tail morphology between
Castracollis and the notostracans are very well defined,
while the similarities between Castracollis and Diplostraca,
especially Spinicaudata, in the morphology of the trunk
limbs and swimming antennae may be explained as
symplesiomorphies (using Lepidocaris or Rehbachiella as
out-groups). If so, it would mean that notostracans have
evolved from an ancestor with many typical ‘conchostracan’
features, such as symmetrically biramous swimming
antennae in adults, and spinicaudatan-like trunk limbs with
palps on the endites. Supporting this notion is the recent
demonstration that a bivalved origin can be traced in the
anlagen of the carapace of Triops cancriformis (Møller
et al., 2003), which look more or less like the carapace
anlagen in Cyclestheria (Cyclestherida), various spinicaudatans, and Leptodora (Cladocera) (see Fig. 11).
In many ways, the notostracans fall outside the general
branchiopod morphology and lifestyle, in being a nonfiltratory animal. Since all their possible close relatives (outgroups) have a filtratory lifestyle, Notostraca must have
evolved from a filtering ancestor. The discovery of
Castracollis gives us a hint as to how this could have
happened, since there is now some indication that the
ancestor of the notostracans was ‘conchostracan’-like. The
implication of this for the monophyly of the diplostracans
will be discussed in a following section.
A remarkable feature of the recent notostracans is the
characteristic external morphology of the gnathal edge of
the mandibles, each with a row of large, distinct cusps
(Richter, 2004) that are adapted for biting (see Fryer, 1988).
This is entirely different from the ‘typical’ branchiopod
mandible, with a characteristic ‘grinding-rolling’ type of
morphology. The latter type of mandible is also found in
Castracollis. Richter (2004) found the notostracan-like type
of mandible also in Laevicaudata and suggested tentatively
a close relationship between these taxa on this basis.
However, if the notostracan affinity of Castracollis is
accepted, it implies an unlikely calmanostracan origin of
Laevicaudata (see next section).
The discovery of Castracollis is indeed remarkable. It is
clearly a branchiopod, but one that cannot be fitted into any
existing group. Instead, Castracollis combines notostracan
and ‘conchostracan’ features, and must, no matter its precise
phylogenetic position, be very close in morphology to the
ancestor of Phyllopoda. Most likely it represents an early
offshoot of the notostracan lineage (Calmanostraca), as was
already suggested by Fayers and Trewin (2003), but
a position as sister group to Diplostraca should not be
excluded from consideration. A third possibility would be to
place the entire clade of Calmanostraca (Notostraca,
Castracollis, and Kazacharthra) inside Diplostraca (Fig. 1,
Laevicaudata and Calmanostraca would shift position).
Such a topology was recently suggested by Stenderup et
al. (2006) based on molecular evidence (without fossils). In
179
the latter scenario all similarities between Castracollis and
‘Conchostraca’ would conveniently be explained as symplesiomorphies, while the similarities between Castracollis
and Notostraca would be synapomorphies.
MONOPHYLY OF DIPLOSTRACA?
Gerstaecker (1866) grouped together various ‘conchostracans’ and cladocerans under the name Diplostraca (referring
to the bivalved carapace). Later the same group was named
Onychura by Eriksson (1934), and this has been followed by
various recent authors. In this account the term Diplostraca
is employed.
Synapomorphies of Diplostraca
1. Larvae/embryos with small, budlike first antennae (Fig.
4C-E).
2. Larval mandibular palp with median setae with setules
arranged in characteristic transverse row (Figs. 5D, 7B)
(Olesen, 2005).
3. Trunk limb exopods in adults with long dorsal lobes,
some of which carry eggs/embryos (Olesen, 1997).
4. Trunk limbs used only for feeding in adults (as opposed
to feeding and swimming, which is plesiomorphic)
(trunk limbs in Laevicaudata provide a minor contribution to swimming).
5. Claspers or hooks on male first (sometimes also second)
pair of trunk limbs (Olesen et al., 1997).
6. Bivalved carapace in adults, covering limbs laterally.
For each character some qualifications must be noted.
Some of the characters must be assumed lost in Cladocera
(2, 3), and others are rather variable (5, 6). A new character
introduced in this work is the presence of budlike first
antennae in larvae or embryos of Spinicaudata and
Cladoceromorpha, as opposed to more elongate first
antennae in larvae of Rehbachiella, Lepidocaris, Anostraca,
and Notostraca. In the free-living larvae of Spinicaudata, the
first antennae are small buds with a characteristic setal
pattern (Olesen and Grygier, 2003, 2004; Pabst and Richter,
2004). A similar morphology is present in presumed freeliving larvae of Cyclestheria hislopi (Botnariuc and Vi~
na
Bayes, 1977). In embryos of various cladocerans, the first
antennae are small buds as well. Olesen (2004) argued for
homology between the larval phase of Spinicaudata (and
other ‘large’ branchiopods) and the ‘embryonic’ phase of
Cladocera. The embryos of Cyclestheria hislopi and
Cladocera are interpreted as embryonised free-living larvae,
something that makes a comparison between spinicaudatan
larvae and cladoceran embryos meaningful. The first
antennae in larvae of Laevicaudata have the form of large,
lateral horns, and are at first glance very different. However,
in the last larval stage, small, bud-like anlagen of the
juveniles first antennae can be seen through the cuticle at the
base of the horns (Gurney, 1926; Botnariuc and Orghidan,
1953; Olesen, 2005).
In adult anostracans and notostracans, and probably also
in Lepidocaris and Rehbachiella, the trunk limbs serve a
double function, being involved in both feeding and swimming. This condition would appear to be plesiomorphic
within Branchiopoda using Rehbachiella as out-group. The
apomorphic state, seen in most diplostracans, is for the trunk
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Fig. 13. Most parsimonious optimisation of general habitat—marine, temporary freshwater pools, or permant freshwater bodies. Only one (evolutionary
successful) colonisation of branchiopods from the sea into freshwater is indicated (Devonian or pre-Devonian), but this may be contradicted by the finding of
a least two marine ‘conchostracans’ from the Devonian and Carboniferous (see text).
limbs to be involved only in feeding (not in swimming).
Laevicaudata are exceptional in that the trunk limbs are to
some extent also involved in swimming (Sars, 1896;
personal observation). This may indicate that Laevicaudata
were an early offshoot within Diplostraca (see below).
Laevicaudata is in fact the taxon of Diplostraca that is
most difficult to place phylogenetically. Olesen et al. (1997)
discussed the various possibilities, and Richter (2004) even
suggested a sister group relationship between Laevicaudata
and Notostraca based on a similarity in the morphology of
the mandibular gnathal edge. Such a position of the
laevicaudatans would require all the diplostracan characters
mentioned above to have been lost in the notostracan line.
Perhaps even more problematic is the discovery of
Castracollis wilsonae which has certain similarities to the
Notostraca, e.g., a notostracan-like tail, but has retained
a ‘typical’ rolling-grinding mandible, as seen in Anostraca
and Spinicaudata. If Laevicaudata were placed directly as
the sister group to Notostraca, Laevicaudata should have
branched off after Castracollis, which already looked
notostracan-like, had done so. Probably this is unlikely.
As highlighted above, there is some evidence of
a ‘conchostracan’-like ancestor of the Notostraca; however,
this does not necessarily violate the monophyly of
Diplostraca. Notostraca and Diplostraca can still be true
sister groups. Should the monophyly of Diplostraca need
reconsideration, then one of the possibilities would be to
place Laevicaudata as the sister group of Notostraca and the
remaining phyllopods, as was recently suggested by
Stenderup et al. (2006) based on molecular data. However,
in this account, a monophyletic Diplostraca is preferred
based on the list of supporting morphological characters
mentioned above.
MARINE OR FRESH WATER ORIGIN OF BRANCHIOPODA?
As is well known, Branchiopoda are predominantly freshwater dwellers. The few truly marine species, mainly
cladocerans, have clearly invaded the sea secondarily. Most
‘large’ branchiopods—fairy shrimps, tadpole shrimps, and
clam shrimps—are adapted to a life style in temporary pools
of different kinds. If this aspect of the lifestyle is mapped on
the phylogeny preferred in this work (Fig. 13), parsimony
suggests that the habitat of the branchiopod ancestor, the
‘ur-branchiopod’, probably constituted small, temporary,
inland pools of some kind. Such a common ancestor would
be older than the Devonian fossils that are clearly branchiopods, such as Lepidocaris rhyniensis, and probably preDevonian as suggested by Tasch (1963). Schram (1986) and
Belk and Schram (2001) mentioned a possible anostracan
from the Silurian.
There is, however, some information indicating a marine
origin of Branchiopoda. Kummerow (1939) mentioned
a ‘conchostracan’ from the Lower Carboniferous that was
fossilised together with marine animals such as trilobites
and brachiopods, and Gross (1934) mentioned one from the
Lower Devonian fossilised along with marine ostracodes.
181
OLESEN: MONOPHYLY AND PHYLOGENY OF BRANCHIOPODA
Tasch (1963) therefore suggested that the Carboniferous
was the ‘time of transition from marine to freshwater for
some conchostracans’. Expressed another way, the presence
of Devonian or Carboniferous marine ‘conchostracans’
could indicate that different groups of Branchiopoda
colonised freshwater independently.
To answer the question of whether Branchiopoda had
a marine or fresh-water origin, a very precise definition of
the taxon is necessary. It is especially crucial to evaluate
whether the supposed marine ‘conchostracans’ can be considered branchiopods according to the definition set up
earlier in this work. This is difficult because this definition
mainly uses limb characters of larvae and adults, which
are known only for very few fossil ‘conchostracans’, and
apparently not for the presumed marine taxa (Gross, 1934;
Kummerow, 1939). The only feature most of these fossils
show is a ‘conchostracan’-like carapace with growth lines.
Some non-marine taxa from the Carboniferous (Orr and
Briggs, 1999) and the Jurassic (Zhang et al., 1990) have
preserved limb features that allow them to be placed in
a recent group of branchiopods, namely the Spinicaudata.
The presence of carapace growth lines has by some authors
been argued (Olesen et al., 1997) to be an apomorphy of
Diplostraca (depending on the position of Laevicaudata),
but lost in Cladocera. In this interpretation fossil ‘conchostracans’ with such carapace lines would be true branchiopods, but not necessarily spinicaudatans. However, to base
a phylogenetic position on only one character such as the
presence of carapace growth lines, when most other
structures are unknown, is highly dubious and should
normally be avoided.
Morphological and molecular studies have shown that
‘Conchostraca’ is paraphyletic (Braband et al., 2002;
Olesen, 2004), perhaps even with respect to Notostraca
(Stenderup et al., 2006). This, together with the high age and
dominance in the fossil record of fossil ‘conchostracans’
compared to other branchiopods, suggests that ‘Conchostraca’ are a kind of stem group to all other branchiopods.
However, without more information on the limb morphology of fossil ‘conchostracans’, this will remain a highly
speculative subject, as will the question of a marine versus
fresh-water origin of the branchiopods.
More evidence from marine ‘conchostracans’ is of crucial
importance. Any future detailed evidence based on such
fossils should be interpreted in the following context. 1) If
well-preserved marine ‘conchostracans’ (or other arthropods, for that matter) are described, which can be shown to
fall within Branchiopoda as defined in this work, then it is
clear that Branchiopoda colonised freshwater more than
once. 2) If, on the other hand, such a branchiopod in-group
position cannot be shown, then it will be simplest to assume
that only one successful colonisation of the branchiopods
into freshwater has taken place. In Fig. 13 this latter interpretation has been followed.
BRANCHIOPOD PHYLOGENY—RECENT ACHIEVEMENTS
Our knowledge about the higher-level phylogeny of
Branchiopoda has in recent years reached a more mature
phase. Fifteen years ago uncertainties were expressed about
nearly all the high-level groups (Cladocera, Conchostraca,
Diplostraca, Phyllopoda, etc.). In the meantime at least some
of these have found strong support (Cladocera, Phyllopoda)
based on both molecular and morphological data, while
others are still being discussed (Diplostraca) or have been
completely rejected (Conchostraca). A new taxon, Cladoceromorpha (Cyclestheria þ Cladocera), has received support in largely all recent phylogenetic treatments. The only
uncertainty left concerning high-level branchiopod phylogeny seems to concern the exact position of Laevicaudata and
Notostraca. Morphological evidence as presented in this
work favour a monophyletic Diplostraca while molecular
evidence is more equivocal. A recent molecular work place
Notostraca inside a paraphyletic Diplostraca (Stenderup et
al., 2006) (indicated tentatively in Fig. 1). More work will
be needed on this aspect to reach consensus.
ACKNOWLEDGEMENTS
Thanks are owed to Ole S. Møller, Jesper T. Stenderup (Zoological
Museum, Copenhagen), and Stefan Richter (Jena, Germany) for many
fruitful discussions on branchiopod evolution. I also thank Dieter Walossek
(Ulm, Germany) for always being willing to share and discuss his ideas on
crustacean phylogeny and limb homologies. This paper combines information from talks given at the Fifth International Large Branchiopod
Meeting (Toodyay, Western Australia, 2004), the Sixth International
Crustacean Congress (Glasgow, Scotland, 2005), and the Fourth International Symposium on the Cambrian System (Nanjing, China, 2005).
Mark J. Grygier, Christopher Rogers, and Frederick Schram provided
helpful reviews of the paper. This study has been supported from the
Danish Natural Science Research Council and has also been a part of
a project at Lake Biwa Museum (Japan) on ‘Research on Large
Branchiopods (Fairy Shrimp, Tadpole Shrimp, Clam Shrimp) Inhabiting
Rice Paddies’ (organised by Mark J. Grygier).
REFERENCES
Ax, P. 1985. Stem species and the stem lineage concept. Cladistics 1:
279-287.
———. 1999. Das System der Metazoa II. Ein Lehrbuch der phylogenetischen Systematik. Fischer, Stuttgart.
Belk, D., and F. R. Schram. 2001. A new species of anostracan from the
Miocene of California. Journal of Crustacean Biology 21: 49-55.
Borradaile, L. A. 1926. Notes upon crustacean limbs. The Annals and
Magazine of Natural History (Series 9) 17: 193-213.
Botnariuc, N., and T. Orghidan. 1953. Phyllopoda. Akademia Republicii
Populare Române, Bucuresti.
———, and N. Vi~na Bayés. 1977. Contribution à la connaissance de la
biologie de Cyclestheria hislopi (Baird), (Conchostraca: Crustacea) de
Cuba, pp. 257-262. In, T. Orghidan (ed.), Résultats des Expéditions
Biospéléogiques Cubano–Roumaines à Cuba, 2. Editura Academiei
Republicii Socialiste Romania, Bucuresti.
Boxshall, G. A. 1997. Comparative limb morphology in major crustacean
groups: the coxa-basis joint in postmandibular limbs, pp. 155-167. In,
R. A. Fortey and R. H. Thomas (eds.), Arthropod Relationships.
Chapman & Hall, London.
———. 2004. The evolution of arthropod limbs. Biological Reviews 79:
253-300.
Braband, A., S. Richter, R. Hiesel, and G. Scholtz. 2002. Phylogenetic
relationships within the Phyllopoda (Crustacea, Branchiopoda) based on
mitochondrial and nuclear markers. Molecular Phylogenetics and
Evolution 25: 229-244.
Calman, W. T. 1909. Crustacea. In, E. R. Lankester (ed.), A Treatise on
Zoology. Part 7. Fascicle 3. Adam and Charles Black, London.
Cannon, H. G., and F. M. C. Leak. 1933. On the feeding mechanism of
the Branchiopoda. Appendix on the mouth parts of the Branchiopoda
Philosophical Transactions of the Royal Society of London B 222: 340352.
Elofsson, R. 1966. The nauplius eye and frontal organs of the nonMalacostraca (Crustacea). Sarsia 25: 1-128.
Eriksson, S. 1934. Studien über die Fangapparate der Branchiopoden nebst
einigen phylogenetischen Bemerkungen. Zoologiske Bidrag från
Uppsala 15: 23-287.
182
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 27, NO. 2, 2007
Fayers, S. T., and N. H. Trewin. 2003. A new crustacean from the Early
Devonian Rhynie chert, Aberdeenshire, Scotland. Transactions of the
Royal Society of Edinburgh 93: 355-382.
Ferrara, F. D., and V. N. Ivanenko. 2001. Interpreting segment homologies
of the maxilliped of cyclopoid copepods by comparing stage-specific
changes during development. Organisms Diversity and Evolution 1:
113-131.
Ferrari, F. D., and M. J. Grygier. 2003. Comparative morphology among
trunk limbs of Caenestheriella gifuensis and Leptestheria kawachiensis
(Crustacea: Branchiopoda: Spinicaudata). Zoological Journal of the
Linnean Society 139: 547-564.
Flössner, D. 1972. Krebstiere, Crustacea. Kiemen und Blattfüsser,
Branchiopoda, Fischläuse, Branchiura. In, Die Tierwelt Deutschlands,
60. VEB Gustav Fischer Verlag, Jena.
Fryer, G. 1974. Evolution and adaptive radiation in the Macrothricidae
(Crustacea: Cladocera): a study in comparative functional morphology
and ecology. Philosophical Transactions of the Royal Society of
London B 269: 137-274.
———. 1983. Functional ontogenetic changes in Branchinecta ferox
(Milne-Edwards) (Crustacea, Anostraca). Philosophical Transactions of
the Royal Society of London B 303: 229-343.
———. 1987. A new classification of the branchiopod Crustacea. Zoological Journal of the Linnean Society 91: 357-383.
———. 1988. Studies on the functional morphology and biology of the
Notostraca (Crustacea: Branchiopoda). Philosophical Transactions of
the Royal Society of London B 321: 27-124.
Gerstaecker, A. 1866-1879. Crustacea (Erste Hälfte). In, H. G. Bronn (ed.),
Die Klassen und Ordnungen der Thier-Reichs, Bd. 5 (Arthropoda).
Abt. 1.
Gross, W. 1934. Eine Estheria aus dem rheinischen Unterdevon. Senckenbergiana 16: 309-313.
Gruner, H. E. 1993. Arthropoda (ohne Insecta). In, Lehrbuch der Speziellen
Zoologie (Begründet von Alfred Kaestner). Gustav Fischer Verlag, Jena,
Stuttgart and New York.
Gurney, R. 1926. The nauplius larva of Limnetis gouldi. Revue der
Gesamte Hydrobiologie und Hydrogeographie 16: 114-117.
Hansen, H. J. 1925. Studies on Arthropoda. II. On the Comparative
Morphology of the Appendages in Arthropoda. A. Crustacea. Gyldendalske Boghandel, Kjøbenhavn.
Jurasz, W., W. Kittel, and P. Presler. 1983. Life cycle of Branchinecta gaini
Daday, 1910 (Branchiopoda, Anostraca) from King George Island, South
Shetland Islands. Polish Polar Research 4: 143-154.
Kaestner, A. 1967. Lehrbuch der Speziellen Zoologie. Bd. 1. Wirbellose,
1. Teil. 2. Auflage. Crustacea. Gustav Fischer, Stuttgart.
Kummerow, E. H. E. 1939. Die Ostracoden und Phyllopoden des deutschen
Unterkarbons. Abhandlungen der Preussischen Landesanstalt Neue
Folge 194: 1-107 7 pls.
Latreille, P. A. 1817. Les Crustacés, les Arachnides, les Insectes. In, Cuvier
G. Le Regne Animal Distribue d’apres son Organisation, pour Servir de
Base a l’Histoire Naturelle des Animaux et d’Introduction a l’Anatomie.
Deterville, Paris.
Lauterbach, K. E. 1989. Das Pan–Monophylum—Ein Hilfsmittel für die
Praxis der Phylogenetischen Systematik. Zoologischer Anzeiger 223:
139-156.
Linder, F. 1952. Contributions to the morphology and taxonomy of the
Branchiopoda Notostraca, with special reference to the North American
species. Proceedings of the United States National Museum 102: 1-69.
Martin, J. W. 1992. Branchiopoda, pp. 25-224. In, F. W. Harrison (ed.),
Microscopic Anatomy of Invertebrates, 9. Wiley-Liss, New York.
———, and G. E. Davis. 2001. An updated classification of the recent
Crustacea. Natural History Museum of Los Angeles County Science
Series 39: 1-124.
———, B. E. Felgenhauer, and L. G. Abele. 1986. Redescription of the
clam shrimp Lynceus gracilicornis (Packard) (Branchiopoda, Conchostraca, Lynceidae) from Florida, with notes on its biology. Zoologica
Scripta 15: 221-232.
———, and C. E. Cash-Clark. 1995. The external morphology of the
onychopod ‘cladoceran’ genus Bythotrephes (Crustacea, Branchiopoda,
Onychopoda, Cercopagididae), with notes on the morphology and
phylogeny of the order Onychopoda. Zoologica Scripta 24: 61-90.
———, and J. C. Christiansen. 1995. A morphological comparison of the
phyllopodous thoracic limbs of a leptostracan (Nebalia sp.) and
a spinicaudate conchostracan (Leptestheria sp.), with comments on the
use of Phyllopoda as a taxonomic category. Canadian Journal of
Zoology 73: 2283-2291.
McKenzie, K. G., P.-J. Chen, and S. Majoran. 1991. Almatium gusevi
(Chernyshev, 1940): redescription, shield-shapes; and speculations on
the reproductive mode (Branchiopoda, Kazacharthra). Paläontologische Zeitschrift 65: 305-317.
McLaughlin, P. A. 1980. Comparative Morphology of Recent Crustacea.
W.H. Freeman and Company, San Francisco.
Møller, O. S., J. Olesen, and J. T. Høeg. 2003. SEM studies on the early
development of Triops cancriformis (Bosc) (Crustacea: Branchiopoda:
Notostraca). Acta Zoologica (Stockholm) 84: 267-284.
———, ———, and ———. 2004. Study on the larval development of
Eubranchipus grubii (Crustacea, Branchiopoda, Anostraca), with notes
on the basal phylogeny of the Branchiopoda. Zoomorphology 123:
107-123.
Negrea, S., N. Botnariuc, and H. J. Dumont. 1999. Phylogeny, evolution
and classification of the Branchiopoda. Hydrobiologia 412: 191-212.
Novojilov, N. 1959. Position systématique des Kazacharthra (Arthropodes)
d’après de nouveaux matériaux des monts Ketmen et Sajkan (Kazakhstan
SE et NE). Bulletin de la Société de Géologie de France 7: 265-269.
Olesen, J. 1998. A phylogenetic analysis of the Conchostraca and
Cladocera (Crustacea, Branchiopoda, Diplostraca). Zoological Journal
of the Linnean Society 122: 491-536.
———. 1999. Larval and post-larval development of the branchiopod clam
shrimp Cyclestheria hislopi (Baird, 1859) (Crustacea, Branchiopoda,
Conchostraca, Spinicaudata). Acta Zoologica (Stockholm) 80: 163184.
———. 2004. On the ontogeny of the Branchiopoda (Crustacea):
contribution of development to phylogeny and classification, pp. 217269. In, G. Scholtz (ed.), Evolutionary Developmental Biology.
Crustacean Issues 15. A. A. Balkema Publishers, Lisse.
———. 2005. Larval development of Lynceus brachyurus (Crustacea,
Branchiopoda, Laevicaudata): redescription of unusual crustacean
nauplii, with special attention to the moult between last nauplius and
first juvenile. Journal of Morphology 264: 131-148.
———, and M. J. Grygier. 2003. Larval development of Japanese
‘conchostracans’: part 1, larval development of Eulimnadia braueriana
(Crustacea, Branchiopoda, Spinicaudata, Limnadiidae) compared to that
of other limnadiids. Acta Zoologica (Stockholm) 84: 41-61.
———, and ———. 2004. Larval development of Japanese ‘conchostracans’: part 2, larval development of Caenestheriella gifuensis
(Crustacea, Branchiopoda, Spinicaudata, Cyzicidae), with notes on
homologies and evolution of certain naupliar appendages within the
Branchiopoda. Arthropod Structure and Development 33: 453-469.
———, J. W. Martin, and E. W. Roessler. 1997. External morphology of
the male of Cyclestheria hislopi (Baird, 1859) (Crustacea, Branchiopoda,
Spinicaudata), with comparison of male claspers among the Conchostraca and Cladocera and its bearing on phylogeny of the ‘bivalved’.
Branchiopoda. Zoologica Scripta 25: 291-316.
———, S. Richter, and G. Scholtz. 2001. The evolutionary transformation
of phyllopodous to stenopodous limbs in the Branchiopoda (Crustacea)—Is there a common mechanism for early limb development in
arthropods?. The International Journal of Developmental Biology 45:
869-76.
———, ———, and ———. 2003. On the ontogeny of Leptodora kindtii
(Crustacea, Branchiopoda, Cladocera), with notes on the phylogeny of
the Cladocera. Journal of Morphology 256: 235-259.
Orr, P. J., and D. E. G. Briggs. 1999. Exceptionally preserved
conchostracans and other crustaceans from the Upper Carboniferous of
Ireland. Special Papers in Palaeontology 62: 1-68.
Pabst, T., and S. Richter. 2004. The larval development of an Australian
limnadiid clam shrimp (Crustacea, Branchiopoda, Spinicaudata), and
a comparison with other Limnadiidae. Zoologischer Anzeiger 243: 99115.
Preuss, G. 1951. Die Verwandtschaft der Anostraca und Phyllopoda.
Zoologischer Anzeiger 147: 49-64.
———. 1957. Die Muskulatur der Gliedmaen von Phyllopoden und
Anostraken. Mitteilungen des Zoologischen Museums Berlin 33: 221257.
Richter, S. 2002. The Tetraconata concept: hexapod-crustacean relationships and the phylogeny of Crustacea. Organisms Diversity and
Evolution 2: 217-237.
OLESEN: MONOPHYLY AND PHYLOGENY OF BRANCHIOPODA
———. 2004. A comparison of the mandibular gnathal edges in
branchiopod crustaceans: implications for the phylogenetic position of
the Laevicaudata. Zoomorphology 123: 31-44.
Ruppert, E. E., S. F. Fox, and R. D. Barnes. 2004. Invertebrate Zoology:
A Functional Evolutionary Approach. Seventh Edition. Brooks Cole
Thomson, Belmont, California, USA.
Sanders, H. L. 1963. The Cephalocarida. Functional morphology, larval
development, comparative external anatomy. Memoirs of the Connecticut Academy of Arts and Sciences 15: 1-80.
Sars, G. O. 1887. On Cyclestheria hislopi (Baird), a new generic type of
bivalve Phyllopoda; raised from dried Australian mud. Christiania
Videnskabs-Selskabs Forhandlinger 1: 1-65.
———. 1896. Beskrivelse af de hidtil kjendte norske Arter af Underordnerne Phyllocarida og Phyllopoda [Descriptions of the Norwegian
species at present known belonging to the suborders Phyllocarida and
Phyllopoda]. In, Fauna Norvegiæ. Bd. I. Christiania.
———. 1898. On some South-African Phyllopoda raised from dried
mud. Archiv for Mathematik og Naturvidenskab B 20: 1-43, 4 pls.
———. 1901. Contributions to the knowledge of the fresh-water
Entomostraca of South America, as shown by artificial hatching from
dried material. Archiv for Mathematik og Naturvidenskab B 23, (3): 1102, 1-12 pls.
———. 1902. On the Polyphemidae of the Caspian Sea. Annuaire du
Musée Zoologique de l’Académie Impériale des Sciences de St.
Petersbourg 7: 31-54, 4 pls.
———. 1993. On the freshwater crustaceans occurring in the vicinity of
Christiania. University Bergen Press (translation of an 1861 handwritten
manuscript, University of Oslo Library).
Schram, F. R. 1986. Crustacea. Oxford University Press, New York.
———, and S. Koenemann. 2001. Developmental genetics and arthropod
evolution: part 1, on legs. Evolution and Development 3: 343-354.
———, and S. Koenemann. 2004. Are the crustaceans monophyletic? pp.
319-329. In, J. Cracraft and M. J. Donoghue (eds.), Assembling the Tree
of Life. Oxford University Press, New York.
Scourfield, D. J. 1926. On a new type of crustacean from the Old Red
Sandstone (Rhynie Chert Bed, Aberdeenshire)—Lepidocaris rhyniensis
gen. et sp. nov. Philosophical Transactions of the Royal Society of
London B 214: 153-187.
Snodgrass, R. E. 1956. Crustacean metamorphoses. Smithsonian Miscellaneous Collections 131: 1-78.
Spears, T., and L. G. Abele. 2000. Branchiopod monophyly and
interordinal phylogeny inferred from 18S ribosomal DNA. Journal of
Crustacean Biology 20: 1-24.
183
Stenderup, J. T., J. Olesen, and H. Glenner. 2006. Molecular phylogeny of
the Branchiopoda (Crustacea)—multiple approaches suggest a ‘diplostracan’ ancestry of the Notostraca. Molecular Phylogenetics and Evolution 41: 182-194.
Swain, T. D., and D. J. Taylor. 2003. Structural rRNA characters support
monophyly of raptorial limbs and paraphyly of limb specialization in
water fleas. Proceedings of the Royal Society of London B 270: 887896.
Tasch, P. 1963. Evolution of the Branchiopoda, pp. 145-157. In, H. B.
Whittington and W. D. I. Rolfe (eds.), Phylogeny and Evolution of
Crustacea. Museum of Comparative Zoology, Special Publication,
Cambridge, Massachusetts.
———. 1969. Branchiopoda, pp. 128-191. In, R. C. Moore (ed.), Treatise
on Invertebrate Paleontology, Part R, Arthropoda 4. The University of
Kansas, Lawrence, Kansas, and The Geological Society of America, Inc.,
Boulder, Colorado.
Taylor, D. J., T. J. Crease, and W. M. Brown. 1999. Phylogenetic evidence
for a single long-lived clade of crustacean cyclic parthenogens and its
implications for the evolution of sex. Proceedings of the Royal Society
of London B 266: 791-797.
Wagner, N. 1868. Hyalosoma dux, a new form of the group Daphnida
(Crustacea Cladocera). Arbeiten der erste Sitzung russ. Naturforscher in
St. Petersburg 1868. Trudy I.S.R.E. Otd Zoologii 218-239. [In Russian.]
Walossek, D. 1993. The Upper Cambrian Rehbachiella and the phylogeny
of Branchiopoda and Crustacea. Fossils and Strata 32: 1-202.
———, and K. J. Müller. 1998. Early arthropod phylogeny in the light
of Cambrian ‘Orsten’ fossils, pp. 185-231. In, G. Edgecombe (ed.),
Arthropod Fossils and Phylogeny. Columbia University Press, New
York.
Williams, T. A. 2004. The evolution and development of crustacean limbs:
an analysis of limb homologies, pp. 169-193. In, G. Scholtz (ed.),
Evolutionary Developmental Biology. Crustacean Issues 15. A. A.
Balkema Publishers, Lisse, Abingdon, Exton (PA), and Tokyo.
———, and G. B. Müller. 1996. Limb development in a primitive
crustacean, Triops longicaudatus: subdivision of the early limb bud gives
rise to multibranched limbs. Development Genes and Evolution 206:
161-168.
Zhang, W., Y. Shen, and S. Niu. 1990. Discovery of Jurassic conchostracans with well-preserved soft parts and notes on its biological
significance. Palaeontologia Cathayana 5: 311-355.
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ACCEPTED: 24 October 2006.