Sexually dimorphic ornamentation in modern spinicaudatans and the taxonomic implications for fossil clam shrimps

Abstract

The phylogenetic studies of clam shrimps (Branchiopoda, Crustacea) demonstrated that the significance of several morphological
characters for classification of branchiopod shells should be critically re-evaluated. Such a venture is particularly
important for integrating the taxonomy of fossil and extant branchiopods. One of the shell characters widely used
in the branchiopod classification is the carapace ornamentation pattern. This character might, however, be significantly
influenced by intraspecific variability and in particular the sexual dimorphism. In this study we investigate the pattern
of ornamentation in extant branchiopods—including differences resulting from sexual dimorphism—in order to assess
its value for branchiopod taxonomy. We examined 184 individuals representing 10 living species belonging to 7 genera,
5 families, and 2 suborders from China, and compared with the results of previous studies. Although some differences
in ornamentation were related to reproductive modes, the basic ornamentation patterns or combinations were stable
within each extant species. We found out that some taxa indeed display sexually dimorphic ornamentations, but their
basic ornamentation patterns or combinations are stable within each species so they do not significantly influence the
taxonomic identification. Integration of data on fossil and extant taxa indicates that similar ornamentation patterns can be
observed on familial level of fossil spinicaudatan branchiopods and indicates therefore that characteristic ornamentation
patterns can help to identify these taxa in the fossil record. In light of the new molecular phylogeny, we re-evaluated the
phylogenetic relationship between fossil and extant spinicaudatan taxa. The resulting tree suggests: (i) paraphyly of the
traditional Eosestherioidea, (ii) an affinity between Ozestheria and Triglypta, and (iii) an affinity between Cyzicus and
Diestheria or Aquilonoglypta.

Full text

Acta Palaeontol. Pol. 67 (2): 475–492, 2022 https://doi.org/10.4202/app.00892.2021
Sexually dimorphic ornamentation in modern
spinicaudatans and the taxonomic implications
for fossil clam shrimps
XIAOYAN SUN and JINHUI CHENG
Sun, X. and Cheng, J. 2022. Sexually dimorphic ornamentation in modern spinicaudatans and the taxonomic implications
for fossil clam shrimps. Acta Palaeontologica Polonica 67 (2): 475–492.
The phylogenetic studies of clam shrimps (Branchiopoda, Crustacea) demonstrated that the significance of several mor-
phological characters for classification of branchiopod shells should be critically re-evaluated. Such a venture is partic-
ularly important for integrating the taxonomy of fossil and extant branchiopods. One of the shell characters widely used
in the branchiopod classification is the carapace ornamentation pattern. This character might, however, be significantly
influenced by intraspecific variability and in particular the sexual dimorphism. In this study we investigate the pattern
of ornamentation in extant branchiopods—including differences resulting from sexual dimorphism—in order to assess
its value for branchiopod taxonomy. We examined 184 individuals representing 10 living species belonging to 7 genera,
5 families, and 2 suborders from China, and compared with the results of previous studies. Although some differences
in ornamentation were related to reproductive modes, the basic ornamentation patterns or combinations were stable
within each extant species. We found out that some taxa indeed display sexually dimorphic ornamentations, but their
basic ornamentation patterns or combinations are stable within each species so they do not significantly influence the
taxonomic identification. Integration of data on fossil and extant taxa indicates that similar ornamentation patterns can be
observed on familial level of fossil spinicaudatan branchiopods and indicates therefore that characteristic ornamentation
patterns can help to identify these taxa in the fossil record. In light of the new molecular phylogeny, we re-evaluated the
phylogenetic relationship between fossil and extant spinicaudatan taxa. The resulting tree suggests: (i) paraphyly of the
traditional Eosestherioidea, (ii) an affinity between Ozestheria and Triglypta, and (iii) an affinity between Cyzicus and
Diestheria or Aquilonoglypta.
Key words: Branchiopoda, Spinicaudata, ornamentation, sexual dimorphism, systematics, taxonomy.
Xiaoyan Sun [xysun@nigpas.ac.cn] and Jinhui Cheng [jhcheng@nigpas.ac.cn] (corresponding author), State Key
labo ratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excel-
lence in Life and Palaeoenvironment, Chinese Academy of Sciences, 39 Beijing Eastroad, Nanjing, 210008, China.
Received 30 March 2021, accepted 15 October 2021, available online 29 March 2022.
Copyright © 2022 X. Sun and J. Cheng. This is an open-access article distributed under the terms of the Creative
Commons Attribution License (for details please see http://creativecommons.org/licenses/by/4.0/), which permits unre-
stricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Introduction
Clam shrimps (Crustacea: Branchiopoda: Laevicaudata,
Spinicaudata, Cyclestherida) are a paraphyletic group of
bivalved crustaceans (Astrop et al. 2020). The suborder
Cyclestherida is thought to be represented by a single extant
species only, has a problematic fossil record in the Middle
Devonian and may represent a sister group to Cladocera
(Hegna and Astrop 2020). The suborder Laevicaudata is
a basal clade of Diplostraca (Branchiopoda: Phyllopoda)
with low phylogenetic diversity and poor fossil record. The
earliest laevicaudatans may date back to the Permian but
the earliest soft-body fossils are known from the Jurassic
(Shen and Chen 1984; Hegna and Astrop 2020). The subor-
der Spinicaudata is a morphologically distinctive and geo-
graphically widespread group that comprises three families
(Cyzicidae, Leptestheriidae, and Limnadiidae). As pioneer
arthropods in freshwater environments during the coloni-
zation of terrestrial environments, the known history of
Spinicaudata dates back to the Early Devonian (Zhang et al.
1976; Chen and Shen 1985; Hegna and Astrop 2020). They
were diverse and abundant in most lacustrine depositional
settings during the Mesozoic.
Spinicaudatans have bivalved carapaces composed
mainly of chitin or chitin-mineral complex (Astrop et al.
2015; Hegna et al. 2020), with the latter easier to preserve
as fossils than the soft parts. There are only few sites with
exceptionally preserved fossil spinicaudatans from the Late

476 ACTA PALAEONTOLOGICA POLONICA 67 (2), 2022
Devonian to Early Cretaceous times, but morphological de-
tails of soft body for particular species delimitation, that
are available in living spinicaudatans, were not preserved
(Hegna and Astrop 2020). Thus, the classification of fos-
sil spinicaudatans is based on the carapace ornamentation
and morphology (Scholze and Schneider 2015; Hegna and
Astrop 2020) following several contributions, which at-
tempted at clarifying the taxonomy of fossil members of this
group (e.g., Novojilov 1954; Tasch 1969; Zhang et al. 1976;
Chen and Shen 1985; Gallego 2010; Gallego and Caldas
2001; Astrop and Hegna 2015). Represented by near 200
genera of 30 fossil families, spinicaudatans exhibit consi-
derable variations in shape, size and carapace ornamen-
tation (Zhang et al. 1976). However, the taxonomic diver-
sity of fossil spinicaudatans was probably overestimated
due to extremely variable carapace morphology related to
phenotypic differences (Rogers et al. 2012), and distinc-
tive sexual variation known from extant families, genera,
and species (Astrop et al. 2012, 2020; Hegna and Rogers
2020). It is still debatable whether the carapace features,
especially the ornamentation on growth bands, are of tax-
onomic importance. Rogers et al. (2012) revised the ex-
tant genera of Limnadiidae and stated that the carapace
morphology of Limnadiidae is not as informative as egg
or telson morphology for species delimitation (Hegna and
Rogers 2020). Nevertheless, the carapace ornamentation is
still used as a key characteristic for inferring the phyloge-
netic relationships between extant and fossil species (Wang
1989; Konstans et al. 2019; Li and Teng 2019; Hegna and
Rogers 2020) though it remains uncertain whether the orna-
mentation is of genetic species-specific character or rather
a manifestation of phenotypic plasticity. Already Mattox
(1957) proposed to abandon the use of carapace features
based on different ornamentation patterns co-occurring in
a single specimen and since then the ornamentation had
not been considered as the principal diagnostic criterion
for taxonomic classification in living species (Tasch 1969;
Scholze and Schneider 2015), albeit some taxonomists con-
tinued to use them (e.g., Stigall and Hartmann 2008; Orlova
and Sadovnikov 2009). These changes in ornamentation in
particular species were interchangeably considered to repre-
sent different responses to environmental factors in subse-
quent ontogenetic phases or fixed genetic differences, thus
reflecting a phylogenetic pattern (Zhang et al. 1976; Chen
and Shen 1985; Wang 1989; Astrop and Hegna 2015; Hegna
2021). In spite of this long-lasting controversy the growth-
band ornamentation has seldom been described for extant
species to address this problem (Barnard 1929; Kobayashi
1954; Ghosh 1982; Timms 2018; Konstans et al. 2019). So
far, morphological differentiation of ornamentation patterns
caused by sexual dimorphism has not been examined. More
data from extant taxa, including comprehensive descrip-
tions of carapace ornamentation, genetic, developmental,
and ecological data should be used to evaluate these hypoth-
eses at both generic and infrageneric levels.
Different amount of information on the carapace mor-
phological features known from fossil and extant species
results in a serious impediment in the integration of these
taxa and low credibility of the taxonomy of the entire group.
Reducing this discrepancy in the amount of taxonomic in-
formation known from these two groups is essential in de-
ciphering the evolutionary history of the clade. A starting
point might be to select and focus on the most appropriate
set of taxonomic characters integrating fossil and extant tax-
onomy that could generate a resolved phylogeny for major
clam shrimp groups. This is, however, challenging due to
the incomplete fossil record of spinicaudatans to the extent
that even distinguishing crown versus stem groups with the
available characters may prove to be impossible (Hegna and
Astrop 2020; Hegna and Rogers 2020). The investigations
of intraspecific variation, such as sexual dimorphism of
carapace shape or ontogenetic changes, have received even
less interest, leading to overestimation of species diversity
(Astrop and Hegna 2015; Hegna and Rogers 2020). Since
the descriptions of carapace morphology and carapace or-
namentation of Recent taxa are only rarely provided, it is
crucial for integration of taxonomy and phylogeny of extant
and fossil taxa that such data are appended.
The integration of molecular phylogenetic studies and
morphological analyses of fossil and extant taxa already al-
lowed to propose some scenarios for the evolutionary his-
tory of the suborder Spinicaudata. Astrop and Hegna (2015)
first proposed a phylogenetic hypothesis integrating living
and fossil spinicaudatan families based on the molecular
phylogeny of Schwentner et al. (2009) and re-evaluated the
evolutionary diagram of Zhang et al. (1976). However, the
phylogenetic relationships between Eocyzicus (Cyzicidae),
Leptestheriidae and Limnadiidae reomained not well re-
solved. Phylogenetic analyses by Schwentner et al. (2020)
recovered the paraphyly of Cyzicidae and Leptestheriidae as
a sister group to Limnadiidae. The phylogenetic hypothesis
needs to be re-evaluated in light of the new phylogeny of
Schwentner et al. (2020) (Hegna and Astrop 2020).
In this study we examined several individuals and taxa
of clam shrimps from China. To clarify the stability of
their carapace ornamentation characters, we focused on the
differentiation of the ornamentation of extant species and
demonstrated the differences of carapace ornamentation
that resulted from sexual dimorphism. We proposed several
patterns in the evolution of carapace ornamentation. We
further investigated taxonomic value of ornamentation and
discussed its implications for taxonomy of the fossil subor-
der Spinicaudata based on the integrated tree incorporating
fossil families into the molecular framework. This study
invites further studies and discussions on the evolutionary
pattern of carapace ornamentation in Spinicaudata.
Institutional abbreviations.—NIGP, Nanjing Institute of
Geology and Palaeontology, Chinese Academy of Sciences,
Nanjing, China.
Other abbreviations.—D, diameter of reticulation; H, height
of carapace; L, length of carapace.

SUN AND CHENG—TAXONOMIC VALUE OF CARAPACE ORNAMENTATION IN BRANCHIOPODA 477
Material and methods
We examined 184 individuals representing 10 living species
belonging to 7 genera, 5 families, 2 suborders (Table 1).
Morphological observations were conducted on 12–20 spec-
imens (males, females, whole body, carapace and dissected
soft body) per species and different populations from natural
ponds, reservoirs and rice fields. In order to assess the tax-
onomic signal of ornamentation, we analysed the morphol-
ogy of extant species combining with results from previous
studies (e.g., Zhang et al. 1976; Chen and Shen 1985; Wang
1989; Astrop 2014). The reported ornamentation patterns on
growth bands of carapace were briefly summarized into 8
common patterns and 10 combinational patterns (Table 1).
We also summarized the general ornamentation patterns in
different families and the implications for integrating fossil
and extant taxa. The terminology was mainly adapted from
Scholze and Schneider (2015) and improved based on infor-
mation from Chen and Shen (1985) and Astrop and Hegna
(2015). Voucher specimens are stored in 96% ethanol and de-
posited in Nanjing Institute of Geology and Palaeontology,
Chinese Academy of Sciences. Specimens were dissected
in glycerine and observed under a light microscope (Zeiss
Stereo Discovery V20). Specimens were critical point dried
and coated with gold, and examined in a stereomicroscope
(SEM, LEO 1530 VP) for ornamentation on growth bands.
Details regarding studied taxa can be found in SOM: table
S1, Supplementary Online Material available at http://app.
pan.pl/SOM/app66-Sun_Cheng_SOM.pdf.
Results
Sexually dimorphic ornamentation was observed in the
adult stages of Ozestheria sp., Cyzicus sp., Eocyzicus orien-
talis Daday, 1913, and Eocyzicus mongolianus Uéno, 1927.
Ozestheria sp. (suborder Spinicaudata): male and female
carapaces can be recognised by conspicuous sexual dimor-
phism of carapace size and shape. Males are usually larger
than females. The mean female carapace H/L ratios range
0.684–0.706, while the mean male carapace H/L ratios range
0.601–0.625. Males are relatively more elongate than the
females. Notably, sexual dimorphism of carapace surface
ornamentation is well developed in this species (Fig. 1). The
ornamentation of male carapace exhibits minute punctae
(D≤0.01mm)restrictedtothelarvalvalves(Fig.1A2), small
reticulations(D≤0.02mm)inthemid-ventralpartofthecar-
apace (Fig. 1A3), radial lirae near the ventral margin of the
carapace (Fig. 1A5), and setae on the margin of the carapace
(Fig. 1A4, A5). Ornamentation in the dorsal part of the cara-
pace is similar to that on the ventral part. The change from
punctae on the larval valves to reticulations in the mid-ven-
tral part of the carapace is abrupt, while the change from re-
ticulations to lirae is gradual. Near the ventral margin of the
carapace, the edges of each mesh protuberate and merge into
a larger undeveloped reticulation, and the radial lirae along
the lower margin of each growth band derive from the bulge
of reticulated ornamentation. The ornamentation of female
carapace present punctae on the larval valves (Fig. 1B2),
small reticulations in the mid-ventral part of the carapace
(Fig. 1B3), and radial fringes near the ventral margin of the
carapace (Fig. 1B4). Furthermore, compared with the male
form, the edges of mesh along the lower margin of each
growth band weakly protuberate in the females (Fig. 1B5).
Cyzicus sp. (suborder Spinicaudata): radial fringe orna-
mentation is present on the larval valves, similar to Ozes theria
pilosa (Rogers et al. 2013) and species of Leptes theriidae.
Smallreticulations(D≤0.02mm)andradialliraearepresent
in the ventral part of the carapace (Fig. 2). The male carapace
has relatively distinct ornamentation on the entire carapace,
including reticulation and reticulate–lirae transition along the
lower margin of the growth band (Fig. 2A2, A3). However, the
female form has an extensive, weak reticulation ornamented
area near the ventral margin (Fig. 2B3).
Eocyzicus orientalis and Eocyzicus mongolianus (subor-
der Spinicaudata): growth bands in the upper to middle parts
of carapace are mainly ornamented with small to medium
reticulations. The female carapace has rows of nodular orna-
mentation on growth bands in the ventral part of the carapace,
absent in the male carapace (Fig. 3). Such sexually dimorphic
ornamentations are not observed in Leptestheria kunmingen-
sis Shu, Rogers, Chen, and Yang, 2015, Leptestheria kawa-
chiensis Uéno, 1927, Eoleptestheria ticinensis (Bal samo-
Cr ivelli, 1859), Lynceus sp., and Eulimnadia sp.
Eulimnadia sp. (suborder Spinicaudata): The carapace
surfaces of Eulimnadia sp. are smooth (Fig. 4A, B).
Lynceus sp. (suborder Laevicaudata): The species pos-
sesses isogonal reticulate ornamentation on the entire car-
apace (Fig. 4C, D), and this pattern is considered as the
basal condition of carapace ornamentation in Spinicaudata,
reflecting a basic reprinting of the underlying epidermal
layer’s cellular structure (Astrop and Hegna 2015).
Discussion
Sexually dimorphic ornamentations.—Spinicaudatans
grow by incomplete moulting. Sexual dimorphism can be
observed on the carapace and appendages during the adult
stage, and carapace shape, and size sexual dimorphism is
common in spinicaudatans. As yet, no certain explanation
about the function of the sexually dimorphic ornamentation
of the carapace in Spinicaudata has been proposed. In this
study, male and female individuals are shown to be mor-
phologically indistinguishable for ornamentation of juvenile
stage, while in the adult stage the male and female individu-
als exhibit sexually dimorphic ornamentation. Specifically,
the male individuals have more elaborate and enhanced or-
namentation in the middle part to the margin of the cara-
pace, which is the main manifestation of sexually dimorphic
ornamentation. The disorganized ornamentation near the
ventral margin of the female carapace might indicate a loss

478 ACTA PALAEONTOLOGICA POLONICA 67 (2), 2022
Table 1. Summary of the reported ornamentation types on growth bands of carapace. Note: The terminology is mainly adapted from the literature of
Scholze and Schneider (2015) and improved by information from Astrop and Hegna (2015), Chen and Shen (1985). The fossil data are merged from Zhang
et al. (1976), Wang (1985), Chen and Shen (1985), Wang et al. (2004), and Liao et al. (2017a). Data of extant species are in bold type and collected from
Astrop (2014), Rogers et al. (2013), Vannier et al. (2003), and this study. Names in bold indicate extant species. Upper: growth bands in the upper part
of the carapace, including larval valve; middle: growth bands in the central part of the carapace; lower: growth bands in the lower part of the carapace.
Pictures of ornamentations are drawn after Scholze and Schneider (2015) and Chen and Shen (1985). D, diameter of ornamentation.
Types of ornamentation Representative taxa
Basic type
smooth surface Palaeolimnadia Raymond, 1946 (Palaeolimnadiidae)
Palaeolimnadiopsis Raymond, 1946 (Palaeolimnadiopseidae)
Eulimnadia dahli Sars, 1896 (Limnadiidae)
Eulimnadia sp. (Limnadiidae)
Paralimnadia badia (Wolf, 1911) (Limnadiidae)
Metalimnadia serratus Mattox, 1952 (Limnadiidae)
punctae
(D≤0.01mm)
Euestheria trotternishensis (Chen and Hudson, 1991) (Euestheriidae)
Aquilonoglypta clinoquadrata Wang in Wang and Liu, 1980 (Auqilonoglyptidae)
Ordosestheria multicostata (Chen in Zhang et al., 1976) (Fushunograptidae)
Triglypta haifanggouensis (Chen in Zhang et al., 1976) (Tryglyptidae)
Imnadia yeyetta Hertzog, 1935 (Limnadiidae)
Cyzicus gynecia (Mattox, 1950) (Cyzicidae)
Cyzicus mexicanus (Claus, 1860) (Cyzicidae)
Cyzicus morsei (Packard, 1871) (Cyzicidae)
reticulation
small reticulation
(D≤0.02mm)
Dictyolimnadia Shen, 1976 (Palaeolimnadiidae)
Echinolimnadia Novojilov, 1965 (Palaeolimnadiidae)
Cyclotuguzites Novojilov, 1958 (Palaeolimnadiidae)
Sajania Novojilov, 1958 (Palaeolimnadiopseidae)
Eolimnadia Chen, 1975 (Perilimnadiidae)
Euestheria Depéret and Mazeran, 1912 (Euestheriidae)
Loxomicroglypta Novojilov and Varentsov, 1956 (Euestheriidae)
Glyptoasmussia Novojilov and Varentsov, 1956 (Euestheriidae)
Cornia Lyutkevich, 1937 (Vertexiinea)
Echinestheria Marliere, 1950 (Vertexiinea)
Eulimnadia texana Packard, 1871 (Limnadiidae)
medium
reticulation (D
0.02–0.07 mm)
Jibeilimnadia Wang, 1981 (Palaeolimnadiidae)
Anyuanestheria Zhang and Chen in Zhang et al., 1976 (Loxomegaglyptidae)
Diaplexa Novojilov, 1946 (Loxomegaglyptidae)
Eocyzicus orientalis Daday, 1913 (Eocyzicidae)
large
reticulation
(D≥0.07mm)
Pseudolimnadia Novojilov, 1954 (Palaeolimnadiidae)
Mesolimnadiopsis Zhang and Chen, 1976 (Palaeolimnadiopseidae)
Loxomegaglypta Novojilov, 1958 (Loxomegaglyptidae)
Paleoleptestheria Novojilov, 1954 (Loxomegaglyptidae)
Nestoria Krasinetz, 1963 (Nestoriidae)
Keratestheria Chernyshev, 1948 (Ipsiloniidae)
Jiliaoestheria Wang in Wang et al., 2004 (Jiliaoestheriidae)
Leptestheria brevirostris (Barnard, 1924) (Leptestheriidae)
Leptestheria rubidgei (Baird, 1862) (Leptestheriidae)
Maghrebestheria maroccana Thiery, 1988 (Leptestheriidae)
isogonal
reticulation
Ulugkemia Novojilov, 1955 (Ulugkemiidae)
Lynceus bioformis (Ishikawa, 1895) (Lynceidae)
Lynceus sp. (Lynceidae)
Cyclestheria hislopi (Baird, 1859) (Cyclestheriidae)
radial fringes
Howellites Bock, 1953 (Fushunograptidae)
Ganestheria Bi and Xie in Chen and Shen, 1982 (Sinoestheriidae)
Jiliaoestheria zhangjiawanensis Wang in Wang et al., 2004 (Jiliaoestheriidae)
Jiliaoestheria nematocomperta (Wang in Wang and Liu, 1980) (Jiliaoestheriidae)
Leptestheria kunmingensis Shu, Rogers, Chen, and Yang, 2015 (Leptestheriidae)
Leptestheria compleximanus (Packard, 1877) (Leptestheriidae)
Leptestheria kawachiensis Uéno, 1927 (Leptestheriidae)
Eoleptestheria ticinensis (Balsamo-Crivelli, 1859) (Leptestheriidae)
radial lirae Orthestheria Chen in Zhang et al., 1976 (Fushunograptidae)
Fushungrapta Wang in Hong et al., 1974 (Fushunograptidae)
Daxingestheria Zhang and Chen in Zhang et al., 1976 (Fushunograptidae)
Nemestheria Zhang and Chen, 1964 (Jilinestheriidae)
Eocyzicus parooensis Richter and Timms, 2005 (Eocyzicidae)

SUN AND CHENG—TAXONOMIC VALUE OF CARAPACE ORNAMENTATION IN BRANCHIOPODA 479
or reduction rather than a gain of complexity in female indi-
viduals. Schwentner et al. (2011) proposed a “lock-and-key”
mechanism between male claspers and female carapace.
The first one or two pairs of trunk limbs of clam shrimps
modified as clasping structures (claspers) are used to fixate
the female on the carapace margin during mating and mate
guarding. Schwentner et al. (2011) suggested that clasper–
carapace interactions played a role in mate recognition in
spinicaudatan Limnadopsis. However, Sigvardt et al. (2017)
have found no clear evidence for the presence of a signal
function in both sexes in some species. The current obser-
vations suggest that behavioral differences may drive the
sexually dimorphic ornamentation and it is likely an exam-
ple of ecological sex-trait, especially wherein males spend
more time in swimming as they search for mates. In this
respect, ornamentation dimorphism may be related to male
investment, that is devoting a larger portion of physiological
costs of investing in reproductive structures, large size or
elaborate ornamentation (Hunt et al. 2017). Also, the males
have stronger carapace calcification than the females due to
the differential physiological costs of eggs and sperms. The
ecological and evolutionary significance of this sexually di-
morphic ornamentation is an unresolved topic and requires
future investigation.
Taxonomic value of ornamentation.—The ornamentation
pattern on carapace has significant implications for inte-
grating fossil and extant species. As follows, we discussed
the general ornamentation patterns in different families and
the implications for integrating fossil and extant taxa.
Three genera, i.e., Leptestheria, Eoleptestheria, Magh-
re bestheria are currently included in the family Lepte sthe-
riidae (Rogers 2020). Leptestheriidae differ from Cyzicidae
in the elongated carapace, broad growth bands, and slight
Basic type
reticulation-lirae transitional
ornamentation
Eosestheria middendorfii (Jones, 1862) (Eosestheriidae)
Triglypta yabraiensis Wang, 2014 (Triglyptidae)
Ozestheria sp. (Cyzicidae)
Cyzicus sp. (Cyzicidae)
Cyzicus gifuensis (Ishikawa, 1895) (Cyzicidae)
Cyzicus tetracerus (Krynicki, 1830) (Cyzicidae)
Cyzicus belfragei (Packard, 1871) (Cyzicidae)
nodules Camerunograpta Novojilov,1957 (Afrograptioidea)
Congestheriella Kobayashi, 1954 (Afrograptioidea)
Limnadiopsis occidentalis Timms, 2009 (Limnadiidae)
Eocyzicus orientalis Daday, 1913 (Eocyzicidae)
Eocyzicus mongolianus Uéno, 1927 (Eocyzicidae)
Combinatorial type
smooth surface (upper),
punctate (lower)
Aquilonoglypta clinoquadrata Wang in Wang and Liu, 1980 (Auqilonoglyptidae)
Qaidamestheria shanshanensis Wang, 1985 (Triglyptidae)
punctae (upper),
radial lirae (lower)
Qaidamestheria dameigouensis Wang, 1983 (Triglyptidae)
Junggarestheria quadrata Wang, 1985 (Polygraptidae)
punctae (upper),
small reticulations (middle),
radial lirae (lower)
Triglypta pingquanensis Wang, 1985 (Triglyptidae)
Triglypta manasica Wang, 1985 (Triglyptidae)
Triglypta tianshanensis Wang, 1985 (Triglyptidae)
Ozestheria sp. (Cyzicidae)
small reticulations (upper),
radial lirae (lower)
Polygrapta Novojilov, 1946 (Polygraptidae)
Huanghestheria Wang in Wang and Liu, 1980 (Vertexiinea)
Yanjiestheria Chen in Zhang et al., 1976 (Eosestheriidae)
Turfanograpta Novojilov, 1958 (Eosestheriidae)
medium reticulations (upper),
radial lirae (lower)
Eosestheria middendorfii Jones, 1862 (Eosestheriidae)
Abrestheria Wang, 1981 (Eosestheriidae)
Eosolimnadiopsis Chen in Zhang et al., 1976 (Palaeolimnadiopseidae)
large reticulations (upper),
radial lirae (lower)
Jiliaoestheria Wang in Wang et al., 2004 (Jiliaoestheriidae)
Sentestheria Wang, 1981 (Sinoestheriidae)
Pseudograpta Novojilov, 1954 (Loxomegaglyptidae)
small–medium reticulations (upper),
small reticulations (lower)
Neimengolimnadiopsis Liu, 1982 (Palaeolimnadiopseidae)
Shipingia Shen in Zhang et al., 1976 (Loxomegaglyptidae)
Pseudestherites Chen in Zhang et al., 1976 (Loxomegaglyptidae)
Jiliaoestheria Wang in Wang et al., 2004 (Jiliaoestheriidae)
Eocyzicus orientalis Daday, 1913 (Eocyzicidae)
radial lirae (upper),
reticulations (lower)
Dimorphostracus Zhang and Chen, 1964 (Dimorphostracidae)
Sinoestheria Zhang, 1957 (Sinoestheriidae)
radial fringes (upper),
small reticulations (lower)
Cyzicus sp. (Cyzicidae)
Cyzicus gifuensis (Ishikawa, 1895) (Cyzicidae)
Cyzicus tetracerus (Krynicki, 1830) (Cyzicidae)
Cyzicus belfragei Packard, 1871 (Cyzicidae)
overlapped reticulations Diestheria Chen in Zhang et al., 1976 (Diestheriidae)
Ozestheria pilosa (Rogers, Thaimuangphol, Saengphan, and Sanoamuang, 2013) (Cyzicidae)

480 ACTA PALAEONTOLOGICA POLONICA 67 (2), 2022

SUN AND CHENG—TAXONOMIC VALUE OF CARAPACE ORNAMENTATION IN BRANCHIOPODA 481
Fig. 2. Ornamentation on the growth bands of carapaces of the extant spinicaudatan branchiopod Cyzicus sp., from Jilin, China. A. NIGP Cr. 141, male,
ornamentation in the larval valve (A1), in the middle part of the carapace (A2), large reticulation and the radial lirae along the lower margin of the growth
band (A3). B. NIGP Cr. 142, female, ornamentation in the larval valve (B1) and in the middle part of the carapace (B2), weakly ornamented area near the
ventral margin (B3).
Fig. 1. Ornamentation on the growth bands of carapaces of the extant spinicaudatan branchiopod Ozestheria sp., from Hebei, China. A. NIGP Cr. 41, male,
carapace in lateral view (A1); ornamentation in the larval valve (A2) and in the ventral part of the carapace (A3), bottom view of spines on the edge of cara-
pace (A4), large reticulation derived from the edges of mesh and the radial lirae along the lower margin of each growth band (A5). B. NIGP Cr. 42, female,
carapace in lateral view (B1), ornamentation in the larval valve (B2) and in the ventral part of the carapace (B3), radial fringes near the ventral margin of
carapace and the dense pilosity on the growth line (B4), undeveloped reticulation derived from the edges of mesh along the lower margin of each growth
band (B5); A1, B1 after Huang and Cai (2016: fig. 5-136d).
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482 ACTA PALAEONTOLOGICA POLONICA 67 (2), 2022
recurvature of the dorsal carapace margin with respect to
the carapace morphology. Leptestheria rubidgei (Baird,
1862) and Maghrebestheria maroccana Thiery, 1988, have
been reported to display irregular reticulate ornamen-
tations (Barnard 1929: 266, figs. d, e; Astrop 2014: 54,
fig. 2.7). Eocyzicus orientalis and E. mongolianus possess
similar reticulate ornamentations on the entire carapace.
However, Leptestheria kunmingensis (Fig. 5), L. kawa-
chiensis (Fig. 6A), and Eoleptestheria ticinensis (Fig. 6B)
display the same ornamentation of radial fringes, which is
consistent with the ornamentation possessed by L. com-
pleximanus (Packard, 1877) (Astrop 2014: 54, fig. 2.7).
Among these species, there are morphological differences
in details of ornamentation. For example, in Leptestheria
kunmingensis (Fig.5A),densepunctae(D ≤ 0.01mm)are
developed between the radial fringes (Fig. 5A2–A4), and
delicate setae are attached to the disto-medial surfaces
and margins (Fig. 5A5, A6, B). However, these features are
Fig. 3. Ornamentations on the growth bands of carapace of the extant spinicaudatan branchiopod Eocyzicus orientalis Daday, 1913, from Xinjiang, China.
A. NIGP Cr. 1, male, ornamentation in the upper to middle parts of the carapace (A1), reticulate ornaments in the ventral part of the carapace (A2), dense
pilosity on the growth lines near the edge of the carapace (A3). B. NIGP Cr. 2, female, ornamentation in the upper to middle parts of the carapace (B1),
rows of nodular ornaments in the ventral part of the carapace (B2), stout setae on the growth lines near the edge of the carapace (B3).

SUN AND CHENG—TAXONOMIC VALUE OF CARAPACE ORNAMENTATION IN BRANCHIOPODA 483
absent in Eoleptestheria ticinensis. Instead, it exhibits a
nearly smooth surface in the ventral part of the carapace,
possessing shallow fringed ornamentation (Fig. 6B2–B4).
The ornamentation pattern of radial fringes with dense
punctae was also observed in the ventral parts of a cara-
pace of Eocyzicus parooensis Richter and Timms, 2005
(Astrop 2014: 54, fig. 2.7). The current results indicate
that reticulate and fringed ornamentations are the basic
ornamentation patterns in Leptestheriidae. The presence of
irregular reticulation in the larval valves and radial fringes,
sometimes with dense punctae, are likely to be shared tax-
onomic features of Leptestheriidae and Eocyzicus, which is
also supported by Astrop and Hegna (2015).
Species belonging to Cyzicus and Ozestheria often have
complex ornamentations. For example, Cyzicus sp. exhi bits
radial fringe ornamentation on the larval valves, with an or-
namentationcombinationofsmallreticulations(D≤0.02mm)
and radial lirae in the ventral part of the carapace. The ra-
dial fringe ornamentation on the larval valves can be ob-
served in Leptestheria kunmingensis and Ozestheria pilosa
(Fig. 7A; Rogers et al. 2013: fig. 3A). In the mid-ventral part
of the carapace of Cyzicus sp., the edges of mesh protuberate
into linearly arranged lirae along the lower margin of each
growth band (Fig. 7B). This ornamentation pattern was also
observed in Cyzicus tetracerus (Krynicki, 1830) (Vannier et
al. 2003: fig. 3B), Cyzicus belfragei (Packard, 1871) (Astrop
2014: fig. 2.5B), and fossil species Diestheria longinqua Chen
in Zhang et al., 1976 of the Early Cretaceous Jehol Biota
(Li et al. 2017: fig. 2.2). The current results using the dioe-
cious Cyzicus sp. showed a similar tendency of variability
in reticulation- lirae transition (Fig. 2). Thus, this ornamen-
tation pattern could be a general morphological character
in the dioecious Cyzicus. The similarities in ornamentation
patterns and carapace shape might suggest a close relation-
ship between the dio ecious Cyzicus and the fossil Diestheria.
For herma phroditic Cyzicus gynecia (Mattox, 1950), growth
bands of carapace were ornamented with punctae or inde-
pendent pits (Astrop 2014), which also appeared in some fos-
sil species, such as Aquilonoglypta clinoquadrata Wang in
Wang and Liu, 1980, Euestheria trotternishensis Chen and
Hudson, 1991, Triglypta haifanggouensis (Chen in Zhang et
al., 1976) and Ordosestheria multicostata (Chen in Zhang et
al., 1976). The pitted ornamentation also occurred in Cyzicus
morsei (Packard, 1871) and androdioecious Cyzicus mexi-
canus (Claus, 1860) (Astrop 2014) and some fossil species of
Palaeorthothemos, Orthothemos, and Estherites (Zhang et al.
1976). Triglyptids were considered to derive from the punc-
ta-bearing Aquilonoglyptidae (Wang 2014). The similarity
Fig. 4. Ornamentations on the growth bands in the extant spinicaudatan branchiopod Eulimnadia sp. and the extant laevicaudatan branchiopod Lynceus sp.
A, B. Eulimnadia sp., from Jiangxi, China. A. NIGP Cr. 161, male, carapace in lateral view. B. NIGP Cr. 162, female, unornamented area near the ven-
tral margin. C, D. Lynceus sp., from Heilongjiang, China. C. NIGP Cr. 173, male, carapace in lateral view. D. NIGP Cr. 174, female, isogonal reticulate
ornamentation in the valve.

484 ACTA PALAEONTOLOGICA POLONICA 67 (2), 2022

SUN AND CHENG—TAXONOMIC VALUE OF CARAPACE ORNAMENTATION IN BRANCHIOPODA 485
Fig. 6. Carapaces and ornamentations of representatives of the extant spinicaudatan family Leptestheriidae. A. Leptestheria kawachiensis Uéno, 1927,
from Hubei, China, NIGP Cr. 101, male, lateral view; left valve, oval outline (A1); growth bands in the upper part of carapace with wide radial fringes
pattern (A2). B. Eoleptestheria ticinensis (Balsamo-Crivelli, 1859), from Jiangsu, China, NIGP Cr. 61, male, lateral view; right valve, oval outline (B1);
growth bands in the ventral part of carapace with shallow fringes pattern, never developing reticulation or punctae between fringes (B2); details of ventral
growth bands with shallow fringes pattern separated with smooth surface (B3, B4).
Fig. 5. Ornamentation pattern on the growth bands of carapaces in the and female of the extant spinicaudatan branchiopod Leptestheria kunmingensis
Shu, Rogers, Chen, and Yang, 2015, from Sichuan, China. A. NIGP Cr. 81, male. B. NIGP Cr. 82, female. Right valve in lateral view (A1); orna mentation
in the larval valve area with anastomosing radial fringes pattern (A2); growth bands ornamentation in the median-ventral valve area (A3); ornamentation
pattern is formed by anastomosing radial fringes occupying the whole growth band and dense punctae developing between fringes; detail of the radial
fringes, depicting dense punctae between the radial fringes (A4); details of carapace growth lines, depicting delicate setae and dense punctae between the
radial fringes (A5, A6, B1, B2).
→

486 ACTA PALAEONTOLOGICA POLONICA 67 (2), 2022
in ornamentations might suggest a close affinity between
hermaphroditic Cyzicus and Aquilonoglypta as suggested by
Astrop and Hegna (2015).
The transition pattern from reticulation to lirae in the
ventral part of the carapace in the Ozestheria differs from
the Cyzicus which has the large undeveloped reticulation.
Australian species of Ozestheria had reticulation, granulated
ornaments, or a combination of punctae and lirae (Timms
2018). The ornamentation pattern of O. pilosa was similar
to species of Diestheriidae, in which transversely enlarged
reticulation overlapped on the lirae ornamentation of each
growth band of the carapace (Rogers et al. 2013). The larger
secondary reticulation was likely originated from the in-
tra-cuticular layer rather than the reticulation from procuti-
cle (Astrop 2014). The ornamentation pattern in Ozestheria
sp. (males, Fig. 1A5), including punctae-reticulation-lirae
combination, the transition from reticulation to lirae, and
the larger undeveloped reticulation, is in line with that of
fossil species Triglypta yabraiensis Wang, 2014 (Wang 2014:
pl. 2: 2). The close morphological resemblance of ornamen-
tations and carapace shape suggests that Ozestheria might
be closely related to Trigly p ta or Tianzhuestheria.
The carapaces of the family Limnadiidae are thin and
lightly mineralized, which commonly resulted in a reticulate
depression on the carapa ce surface, such as Eulimnadia texana
Packard, 1871 (Astrop 2014). However, the carapace surfaces
of most species of Eulimnadia are unornamented (smooth
surface pattern). This pattern also occurs in Metalimnadia
serratus Mattox, 1952, Paralimnadia badia (Wolf, 1911) and
some Triassic fossil species of Paleolimnadiidae (Table 1).
The fossil family Palaeolimnadiopsidae is characterized by
the recurvature of growth lines to form carinate at the pos-
terior-dorsal marginal junction of the carapace. This feature
has also been observed in living species of Limnadopsis.
The ornamentation documented for Palaeolimnadiopsidae
ranged from reticulation to reticulation-lirae combination.
However, the ornamentation possessed by Limnadopsis oc-
cidentalis Timms, 2009, is nodular (Astrop 2014). Imnadia
yeyetta Hertzog, 1935, was reported to exhibit punctae orna-
mentation (Astrop 2014). Nevertheless, this pattern was not
mentioned in the original descriptions of the fossil families
Paleolimnadiidae, Palaeolimnadiopsidae or Perilimnadiidae.
The phenotypic differentiation of ornamentation patter n is
a model to investigate morpho-functional adaptation to some
Fig. 7. Ornamentations on the growth bands in extant spinicaudatans species of Cyzicus Audouin, 1837, Ozestheria Schwentner, Just, and Richter, 2015,
and Diestheria longinqua Chen in Zhang et al., 1976. A. Carapace of Ozestheria pilosa (Rogers, Thaimuangphol, Saengphan, and Sanoamuang, 2013),
from Thailand (after Rogers et al. 2013: fig. 3A). B. Cyzicus gifuensis (Ishikawa, 1895), from Anhui, China, NIPG Cr.121, male; ornamentation in the
ventral part of the carapace (B1) and near the ventral margin of carapace (B2); radial lirae along the lower margin of each growth band (B3).

SUN AND CHENG—TAXONOMIC VALUE OF CARAPACE ORNAMENTATION IN BRANCHIOPODA 487
aquatic environments. Moreover, it might be influenced by
many factors including sexual dimorphism, ecophenotype
and preservation differences. Changes in ornamentation pat-
tern may be related to changes in reproductive modes within
the Cyzicus. For example, the ornamentation pattern of dioe-
cious Cyzicus is composed of fringes and reticulation-lirae
transitional type (Figs. 2, 7), while the ornamentation pat-
tern of androdioecious C. mexicanus consists of fringes and
punctae type (Mattox 1957), and hermaphroditic C. gynecia
consists of punctae (Astrop 2014). Although sexual dimor-
phism is an essential source of intraspecific morphological
variation, the influences on characteristic ornamentation
patterns appear complex.
The basic ornamentation patterns or combinations are
stable within each extant species, even for dioecious species
possessing sexually dimorphic ornamentations. In general,
in animals where speciation process is mainly driven by
sexual and/or natural selection, characters under the in-
fluence of any of these forces will be more informative
than those known to evolve independently of such selection
(Padial et al. 2010). Although differences in ornamentation
patterns are related to changes in reproductive modes within
Cyzicus, such variation will not pose significant problems
for species discrimination.
Some researchers questioned the applicability of or-
namentations because of co-occurrence of different orna-
mentations in a single specimen (Mattox 1957; Scholze and
Schneider 2015). Hegna (2021) suggested that ornamenta-
tions did not vary as wildly and randomly as Scholze and
Schneider (2015) implied. The spinicaudatan carapace is
formed by partial moulting during ecdysis and the outer
surface of the carapace is not shed (Astrop 2014; Hegna and
Astrop 2020). Therefore, the ontogenetic history of each
individual is preserved in the carapace. Ontogenetic differ-
entiation of carapace shape has been observed in all living
species of Spinicaudata (Astrop et al. 2012; Brown et al.
2014). It is necessary to define such ontogenetic variation
of ornamentation within a complete growth series by com-
paring within and between modern species. Ornamentation
pattern would be helpful for interpreting the taxonomic
significance of inter-generic variation in the fossil taxa,
once the stability of ornamentation patterns throughout
the ontogenetic trajectory has been determined. For exam-
ple, Gallego et al. (2020b) studied complex ornamentation
patterns in successive growth bands as a part of detailed
description of fossil clam shrimp species. Our results have
shown that the shared conservative ontogenetic ornamen-
tation patterns existed within different lineages, such as
fringed-reticulated pattern in Leptestheriidae, reticulate
pattern in Eocyzicidae, punctated or reticulated-lirate pat-
tern in Cyzicidae. Konstans et al. (2019) suggested that the
intraspecific variation was minor and ornamentation could
be used for inferring phylogenetic relationships between
living and fossil taxa. They also highlighted the need for
sampling more extant taxa to better understand the evolu-
tionary pattern of ornamentation.
Ornamentation pattern on carapace is of different tax-
onomic importance for superfamilies of clam shrimps. For
example, in the superfamilies Eosestherioidea and Estheri-
teoidea, ornamentation patterns have been used extensively
as a key diagnostic character for high-level taxonomy. The
ornamentation patterns on growth bands in Eosestherioidea
and Estheriteoidea exhibited a wide morphological diver-
sity, which is much richer than the described ornamentation
patterns of living species of Leptestheriidae, Eocyzicidae,
and Cyzicidae. The systematics of Vertexioidea (including
Limnadiidae) mainly relies on a number of diagnostic cara-
pace characters, including carapace outline, size of the lar-
val shell, growth-line pattern, protrusion above the adduc-
tor muscle scars and the recurvature of growth lines at the
postero-dorsal margin, while ornamentation pattern is less
important for taxonomy. Multiple types of ornamentation
were mentioned in the original description of this superfam-
ily (e.g., reticulation, radial fringes, pit, smooth surface and
reticulate-lirae combinational type; Zhang et al. 1976). These
types have been observed in living species of Limnadiidae,
except the types of fringes and reticulate-lirae combination.
The number of and angles between concentric ribs are the
most important diagnostic criteria for taxonomic determi-
nations of Leaniina and Estheriella (Zhang et al. 1976; Chen
and Shen 1985; Scholze and Schneider 2015).
The evolutionary trends of the characteristic ornamen-
tation patterns may be interpreted as a stabilizing solid
selection (both natural and sexual). As mentioned above,
ornamentation pattern is an important character used in
the fossil taxonomy of Spinicaudata. The application of or-
namentation pattern for taxonomy needs to be undertaken
with caution. It is necessary to consider the intraspecific
variation due to sexual dimorphism, and other carapace
features as well. To integrate fossil and extant lineages in a
phylogenetic and macroevolutionary framework, a compre-
hensive data set of extant and fossil clam shrimp together
with a rich diversity of detailed carapace features is needed
for further analysis.
Integrated taxonomy of fossil and extant Spinicaudata.—
Without an integrated phylogenetic hypothesis of fossil and
extant taxa, it is not easy to discuss the evolution and differ-
entiation of carapace ornamentation patterns. Phylogenetic
analyses provide comprehensive insights into the evolution-
ary history of Spinicaudata. Zhang et al. (1976) presented
the first hypothesis of the relationship between spinicau-
datan fossil and extant lineages based on stratigraphic oc-
currence and carapace morphology (e.g., carapace shape,
umbo position, size of larval valves, number and angle of
radial ribs and many sculptures on carapace). Astrop and
Hegna (2015) addressed objections to this hypothesis and
proposed a phylogenetic hypothesis incorporating extant
Spinicaudata with re-evaluated fossil families. They sug-
gested that Limnadiidae was a sister of Perilimnadiidae,
which meant that the changes of carapace characters were
parallel with acquisitions of the traits unique to Limnadiidae

488 ACTA PALAEONTOLOGICA POLONICA 67 (2), 2022
and their related fossil lineages, such as one pair of cari-
nae on the anterior margin in Metalimnadia and the fossil
lineage. Paleolimnadiidae originated in the Late Devonian
when they were represented by some species ornamented
with minute reticulation (Zhang et al. 1976). The overall
evolutionary trend of ornamentation within this family
in the Mesozoic was towards reticulation with different
sizes, smooth carapace, and a combination of reticulation
and lirae. This family was regarded as closely allying with
Limnadia (Tasch 1956; Zhang et al. 1976). Perilimnadiidae
that originated in the late Permian was very similar to
Paleolimnadiidae. The ornamentations documented for
Perilimnadiidae ranged from reticulate to punctate type.
The ancient Eulimnadia lineage seems to be associated with
Paleolimnadiidae rather than with Perilimnadiidae in terms
of smooth ornamentation pattern. However, divergence
time estimates based on the Bayesian relaxed methods
suggested that the earliest limnadiid divergence occurred
around 190.8 Ma and a common ancestor of Eulimnadia and
Metalimnadia around 50 Ma (Bellec and Rabet 2016). Based
on the molecular data, the Eulimnadia lineage might have de-
rived from the Cenozoic representatives of Perilimnadiidae.
Zhang et al. (1976) and Chen and Shen (1985) suggested
that Eulimnadia originated from a Paleocene perilimnadiid
ancestor based on preserved adductor muscle attachment
scars and larger larval valve than that of Paleolimnadiidae.
We accepted this proposal and placed Eulimnadia as a sis-
ter to Perilimnadiidae (Fig. 8). Several molecular analyses
demonstrated that either Limnadia or Imnadia was basal for
extant clade of Limnadiidae and Paralimnadia was a sister
group to Limnadopsis (Bellec and Rabet 2016; Schwentner
et al. 2020). In this sense, Paleolimnadiidae might be poly-
phyletic because of the pervasive morphological homoplasy
of carapace. Schwentner et al. (2020) reconstructed the phy-
logeny of Spinicaudata using four molecular loci. In the
related analyses of basal Limnadiidae, Imnadia was basal in
Limnadiidae, either as the sole sister group of all other taxa
or as the sister to Limnadia. However, the support values
for these alternative topologies were low (value of Bayesian
posterior probability 0.62). Currently, the phylogenetic rela-
tionships of Imnadia and Limnadia are not fully understood.
Leptestheriidae has been considered to derive from the
fossil family Loxomegaglyptidae (Shen 1994; Astrop and
Hegna 2015). Loxomegaglyptidae exhibit large to medium re-
ticulations(D≥0.02mm)orcomplexreticulateornamentation.
Combinations of reticulation and dendritic fringes with dense
punctae are dominant in some genera, such as Pseudograpta
and Defretinia (Chen and Shen 1985). Molecular phylogenetic
analyses by Schwentner et al. (2020) revealed the paraphyly
of Cyzicidae and concluded Leptestheriidae as a sister group
to Limnadiidae. Cyzicidae sensu stricto is the basal clade
of Spinicaudata. Schwentner et al. (2020) established a new
family Eocyzicidae. However, phylogenomic analyses based
on 864 molecular loci data tended to strongly support a sister
group relationship between Leptestheriidae and Eocyzicidae
and Limnadiidae as their closest relative (Schwentner et al.
2018). A sister group relationship between Leptestheriidae
and Eocyzicidae determined with a much larger set of molec-
ular loci was more phylogenetically convincing (Schwentner
et al. 2020). Considering the similarities in ornamentation
patterns and carapace morphology, we agree with the hy-
pothesis of Astrop and Hegna (2015) that the monophyletic
clade Leptestheriidae + Eocyzicidae probably show affinity
with Loxomegaglyptidae. When combined with the sister
group relationship between Leptestheriidae + Eocyzicidae
and Limnadiidae (Schwentner et al. 2018), the traditional
Eosestherioidea is paraphyletic (Fig. 8).
The family Triglyptidae was characterized by three
types of ornamentations: minute punctae, small reticula-
tion and radial lirae. Six genera Tr igl y pta, Tianzhuestheria,
Neopolygrapta, Skyestheria, Dendrostracus, and Cara pa-
cestheria were included in this family (Wang 2014). Wang
(1983) assigned Qaidamestheria to the family Aqui lono-
glyptidae based on the uniform punctae ornamentation.
The carapace shape was defined by the quotient of height/
length of the whole valve and the position of the umbo. The
changes of this feature in intraspecific variation during on-
togeny have been described and quantified, and there was
often an overlap between species (Straškraba 1965; Tippelt
and Schwentner 2018). We agree with Wang (1983) in plac-
ing the Qaidamestheria in the family Aquilonoglyptidae.
Antronestheriidae differed from Triglyptidae in lacking
lirae ornamentation. Euestheriidae possessing small retic-
ulation (D≤0.02mm) was considered paraphyletic encom-
passing an ancestral lineage that gave rise to Ozestheria
(Chen and Shen 1985). The current results suggest the af-
finity between Ozestheria and Triglyptidae. Diestheriidae
has been considered to derive from Eosestheriidae. The
transition of ornamentation from reticulation to lirae and
overlapped reticulation observed in dioecious Cyzicus sug-
gested the affinity to Eosestheriidae and Diestheriidae, and
uniform punctae ornamentations observed in hermaphro-
ditic Cyzicus suggested the affinity to Aquilonoglyptidae
or Orthothemosiidae. The family Orthothemosiidae is con-
troversial because it is considered part of Eosestherioidea
(Zhang et al. 1976; Chen and Shen 1985; Astrop and Hegna
2015; Gallego et al. 2020a). These four families might be
closely related (Fig. 8).
There are some other modifications in the systematic
classification of fossil clam shrimps at the high level of
Fig. 8. Hypothesis of the phylogenetic relationships between fossil and extant taxa of Spinicaudata incorporating molecular framework of Schwentner et
al. (2018) with fossil families sensu Zhang et al. (1976), Chen and Shen (1985), Shen (2003), and Astrop and Hegna (2015). The molecular topology of
extant spinicaudatan taxa from Schwentner et al. (2018) was used as a backbone phylogenetic constraint to construct a framework for fossil taxa. Living
taxa were associated with 11 nodes in the phylogeny of Spinicaudata by carapace morphological characters. The small images of clam shrimps were
adapted from Chen and Shen (1985).
→

SUN AND CHENG—TAXONOMIC VALUE OF CARAPACE ORNAMENTATION IN BRANCHIOPODA 489

490 ACTA PALAEONTOLOGICA POLONICA 67 (2), 2022
taxonomic rank, such as the placement of Afrograptioidea.
This superfamily was recently revised by Shen (2003) and
Liao et al. (2017a) and placed in the suborder Estheriellina
based on the multi-radiating costae and stout tubercles. The
leaiid specimens with soft-tissue body outlines were anal-
ysed by Shen and Schram (2014). The leaiids were promoted
to the suborder Leaiina and placed in the branchiopodan
Diplostraca, based on the ribbed valves and structure of soft
parts. Shen and Schram (2014) also suggested that radial
ribs on the valves probably facilitated a burrowing habbit in
addition to strengthen the valves, which implies the func-
tional significance of ribs. The phylogenitic relationships
among the suborders Spinicaudata, Estheriellina, and Leaiia
still need further investigation (Fig. 8).
Conclusions
The ornamentation pattern is an important character for the
fossil taxonomy of Spinicaudata, especially Eosestherioidea
and Estheriteoidea. Sexual dimorphism is a fundamental
aspect for studies of clam shrimp taxonomy. In this study,
we described the sexually dimorphic ornamentation patterns
in extant species of Spinicaudata and made a preliminary
investigation on taxonomic values assessment of ornamen-
tations. The results indicate that certain sexually dimorphic
ornamentations occur in some species of Spinicaudata, but
the basic ornamentation patterns or combinations are stable
within each extant species, even for dioecious species pos-
sessing sexually dimorphic ornamentations. When integrated
with the sister group relationship between Leptestheriidae +
Eocyzicidae and Limnadiidae in light of the new molec-
ular phylogeny of Schwentner et al. (2018), the traditional
Eosestherioidea is paraphyletic.
Extracting stable taxonomic signal from the external
carapace morphology still presents a major challenge. The
application of ornamentation patterns for taxonomy needs
to be undertaken with caution considering the intraspecific
variation generated by sexual dimorphism. The evolution-
ary relationship between fossil and extant spinicaudatan
lineages is still an open question. To establish a compre-
hensive taxonomic system of clam shrimps, more extensive
sampling of extant taxa and integrative analyses are needed.
Further investigation into both characteristic ornamentation
patterns and quantitative measurements used for taxonomic
identification and taxonomic diagnosis is pending.
Acknowledgements
The authors are grateful to Yanbin Shen (NIGP) for his encourage-
ment and valuable discussion. The authors extend their appreciation
to Gengo Tanaka (Kumamoto University, Kumamoto, Japan), Oscar
Gallego (National University of the Northeast, Corrientes, Argentina)
and Thomas Hegna (State University of New York at Fredonia, USA)
for their valuable comments and suggestions that significantly im-
proved this paper. The authors are also thankful to Yongqiang Mao
and Zhouqing Chen (both NIGP) for their technical support in scan-
ning electron microscope and light microscope photography. This
work was supported by National Natural Science Foundation of
China (41730317), by the research grant of State Key Laboratory
of Palaeobiology and Stratigraphy at Nanjing Institute of Geology
and Palaeontology, Chinese Academy of Sciences, and by Chinese
Academy of Geological Sciences (DD20190009). It is also a contribu-
tion to UNESCO-IUGS IGCP Project 679.
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