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© 2019 The Linnean Society of London, Zoological Journal of the Linnean Society, 2019, XX, 1–17 1
Zoological Journal of the Linnean Society, 2019, XX, 1–17. With 8 figures.
New insights into the evolution of lateral compound eyes
in Palaeozoic horseshoe crabs
RUSSELL D. C. BICKNELL1*,, LISA AMATI2 and JAVIER ORTEGA-HERNÁNDEZ3*,
1Palaeoscience Research Centre, School of Environmental and Rural Science, University of New England,
Armidale, NSW 2351, Australia
2Paleontology, New York State Museum, 222 Madison Avenue, Albany, NY 12230, USA
3Museum of Comparative Zoology and Department of Organismic and Evolutionary Biology, Harvard
University, 26 Oxford Street, Cambridge, MA 02138, USA
Received 6 February 2019; revised 9 June 2019; accepted for publication 13 June 2019
Vision allows animals to interact with their environment. Aquatic chelicerates dominate the early record of lateral
compound eyes among non-biomineralizing crown-group euarthropods. Although the conservative morphology
of lateral eyes in Xiphosura is potentially plesiomorphic for Euarthropoda, synziphosurine eye organization has
received little attention despite their early diverging phylogenetic position. Here, we re-evaluate the fossil evidence
for lateral compound eyes in the synziphosurines Bunodes sp., Cyamocephalus loganensis, Legrandella lombardii,
Limuloides limuloides, Pseudoniscus clarkei, Pseudoniscus falcatus and Pseudoniscus roosevelti. We compare these
data with lateral eyes in the euchelicerates Houia yueya, Kasibelinurus amicorum and Lunataspis aurora. We find
no convincing evidence for lateral eyes in most studied taxa, and Pseudoniscus roosevelti and Legrandella lombardii
are the only synziphosurines with this feature. Our findings support two scenarios for euchelicerate lateral eye
evolution. The elongate-crescentic lateral eyes of Legrandella lombardii might represent the ancestral organization,
as suggested by the phylogenetic position of this taxon in stem-group Euchelicerata. Alternatively, the widespread
occurrence of kidney-shaped lateral eyes in stem-group Xiphosura and stem-group Arachnida could represent the
plesiomorphic condition; Legrandella lombardii eyes would therefore be derived. Both evolutionary scenarios support
the interpretation that kidney-shaped lateral eyes are ancestral for crown-group Euchelicerata and morphologically
conserved in extant Limulus polyphemus.
ADDITIONAL KEYWORDS: euchelicerates – Limulus – synziphosurines – vision – Xiphosura.
INTRODUCTION
Vision is vital for animals and is therefore involved
in multiple functions and complex behaviours, such
as navigation and feeding, and thus has had a major
impact in modelling the ecology of the biosphere
throughout the Phanerozoic (Vannier et al., 2016).
Vision is so important that 95% of extant multicellular
organisms possess some type of active photoreceptor
(Parker, 2011), and eyes have evolved independently
between 40 and 65 times in different lineages (Fernald,
2004; Elofsson, 2006; Cronin & Porter, 2008). The fossil
record of early euarthropods suggests a single origin
for their archetypical lateral compound eyes (LCEs)
consisting of numerous faceted visual units (i.e.
ommatidia) (Paterson et al., 2011; Ortega-Hernández,
2016), but also indicates that these structures have
been lost or otherwise secondarily modified on
innumerable occasions (Harzsch et al., 2006; Miether
& Dunlop, 2016; Strausfeld et al., 2016). Trilobite eyes
are arguably the most iconic examples of LCEs in the
fossil record and have informed our understanding on
the evolution of extinct euarthropod visual systems
substantially (Fordyce & Cronin, 1989; Clarkson et al.,
2006; Schoenemann et al., 2010; Strausfeld et al., 2016;
Scholtz et al. 2019). Although biomineralized LCEs
are also known in aglaspidids (Ortega-Hernández
et al., 2013; Lerosey-Aubril et al., 2017; Siveter et al.,
2018), insights into the function of the visual system
in these problematic euarthropods are more limited,
given that distinct ommatidia and fine ultrastructural
*Corresponding author. E-mail: rdcbicknell@gmail.com,
jortegahernandez@fas.harvard.edu
applyparastyle “fig//caption/p[1]” parastyle “FigCapt”
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2 R. D. C. BICKNELL ET AL.
© 2019 The Linnean Society of London, Zoological Journal of the Linnean Society, 2019, XX, 1–17
detail are not preserved in these fossils. Examples of
LCEs in non-biomineralizing taxa are comparatively
less common but still highly significant and include
the exceptionally preserved visual surfaces of
radiodontans (Lee et al., 2011; Paterson et al.,
2011), numerous stem-group euarthropods (Ortega-
Hernández, 2015; Strausfeld et al., 2016), phosphatized
larvae (Castellani et al., 2012) and euchelicerates
(Poschmann, 2006; Schoenemann, 2006; Schoenemann
& Clarkson, 2008, 2017; McCoy et al., 2015; Miether &
Dunlop, 2016; Poschmann et al., 2016). In this context,
the synziphosurines represent the earliest crown-
group chelicerates that possess LCEs (Lamsdell, 2013),
which, when combined with their early divergent
phylogenetic position, makes them significant for
understanding the early evolution of vision in a major
group of extant euarthropods. However, the fossil
record of LCEs in synziphosurines requires revision.
The evolutionary relationships of synziphosurines
in Euchelicerata remain somewhat controversial,
DarLlandov WPLLo Ems Ei Gi Fras Famenn To urna Visean SerBaMo
Ordovician
Silurian Devonian Carboniferous
DSaKatFloTre
Kasibelinurus
amoricum
Houia
yueya
Bunodes
.sp
Cyamocephalus
loganensis
Pseudoniscus
falcatus
Pseudoniscus
roosevelti
Lunataspis
aurora
Legrandella
lombardii
44
4
41
9
35
9
Myr
Pseudoniscus
clarkei
Limuloides
limuloides
Euchelicerate
Synziphosurine
Figure 1. Stratigraphic occurrence of the studied synziphosurines and euchelicerates.
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EYES IN PALAEOZOIC HORSESHOE CRABS 3
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4 R. D. C. BICKNELL ET AL.
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partly because most representatives are known only
from the dorsal exoskeleton, and there are remarkably
few instances of exceptional limb preservation (Moore
et al., 2005a, b , 2007; Briggs et al., 2012), especially
when compared to true horseshoe crabs (Bicknell et
al., 2019). For example, the suborder Synziphosurina
(sensu Eldredge, 1974), typified by forms that lack a
fused opisthosoma, is now considered paraphyletic
based on the results of recent phylogenetic analyses
and most probably includes stem-group representatives
of Euchelicerata, Xiphosura and Arachnida (Lamsdell,
2013, 2016; Lamsdell et al., 2015). Despite these
limitations, synziphosurines have been studied
for 160 years and are therefore anatomically well
documented. One aspect of their exoskeletal morphology
that has drawn particular interest is the apparent
lack of LCEs in several synziphosurine taxa, making
their representatives ‘mostly blind forms’ according
to the traditional literature (Størmer, 1952: p. 632), a
condition that is generally regarded as secondarily
derived (e.g. Dunlop & Lamsdell, 2017). Reports of LCEs
have become more frequent in recent times (Stürmer
& Bergström, 1981), with taxa such as Bunodes sp.
in Bergström (1975), Cyamocephalus loganensis
Currie, 1927, Legrandella lombardii Eldredge, 1974,
Limuloides limuloides (Woodward, 1865), Pseudoniscus
clarkei Ruedemann, 1916 and Pseudoniscus falcatus
(Woodward, 1868) having been reported to possess
lateral ocular features (Fig. 1; Størmer, 1934; Eldredge,
1974; Bergström, 1975; Dunlop & Selden, 1998; Rudkin
& Young, 2009; Selden et al., 2015). Other forms may
have possessed putative LCEs, including Drabovaspis
complexa (Barrande, 1872), Pasternakevia podolica
Selden & Drygant, 1987, Weinbergina opitzi Richter
& Richter, 1929 and Willwerathia laticeps (Størmer,
1936) (Lehmann, 1956; Chlupáč, 1963, 1965; Stürmer &
Bergström, 1981; Anderson et al., 1998; Krzemiński et al.,
2010; Ortega-Hernández et al., 2010). Problematically,
several of these taxa have not been revised recently, and
thus evidence for LCEs has not been corroborated since
their original description.
Here, we re-examine the morphology of the seven
synziphosurine taxa previously reported to possess LCEs
and present the first direct evidence for LCEs in the
synziphosurine Pseudoniscus roosevelti Clarke, 1902. We
also compare these features with the LCEs of the fossil
crown-group euchelicerates Houia yueya (Lamsdell et al.,
2013), Kasibelinurus amicorum Pickett, 1993, Lunataspis
aurora Rudkin et al., 2008 and the xiphosurid Limulus
polyphemus (Linnaeus, 1758). We use these comparisons
to explore the phylogenetic distribution of different
LCE morphologies in synziphosurines and xiphosurans,
and thus investigate the ancestral condition of ocular
structures in Euchelicerata.
InstItutIonal abbrevIatIons
AM F, Australian Museum, Sydney, NSW, Australia;
AMNH, American Museum of Natural History, New
York City, NY, USA; GSM, Geological Survey of Britain,
Keyworth, Nottinghamshire, UK; MM, Manitoba
Museum, Winnipeg, Manitoba, Canada; NHMUK IA,
The Natural History Museum, London, UK; NIGP,
Nanjing Institute of Geology and Palaeontology, Chinese
Academy of Sciences, Nanjing, China; NYSM, New
York State Museum, Albany, NY, USA; UNE.NHM.Z,
University of New England Natural History Museum
(Zoology Collection), Armidale, NSW, Australia.
MATERIAL AND METHODS
We studied seven species of synziphosurines using
eight specimens with suggested LCEs. Six specimens
were photographed with digital SLR cameras under
reflected light: Bunodes sp. from Bergström (1975)
(NHMUK IA 48425), two Cyamocephalus loganensis
specimens (NHMUK IA 16521, holotype, and
NHMUK IA 25), Limuloides limuloides (GSM
32393), Legrandella lombardii (AMNH 29273,
holotype) and Pseudoniscus falcatus (NHMUK IA
44122, holotype). Two specimens were photographed
with digital SLR cameras under reflected light and
ethanol: Pseudoniscus clarkei (NSYM 19113) and
the newly studied Pseudoniscus roosevelti (NYSM
19112). Three putative xiphosuran taxa with well-
preserved eyes where studied for comparison with
the synziphosurines (Fig. 1). Kasibelinurus amicorum
(AM F 68969, holotype) and Lunataspis aurora (MM
I-4000A, holotype) were photographed under reflected
Figure 2. Cyamocephalus loganensis and Bunodes sp. lacking definitive evidence of lateral compound eyes. A–D,
Cyamocephalus loganensis specimens. A, B, NHMUK IA 25 from the Upper Silurian-aged (Ludlow Series) of England
(?Ludlow Group). A, complete specimen. B, close-up of box in A; white arrow indicates ophthalmic ridge. C, D, NHMUK
IA 16521, (holotype) from the Lower Silurian-aged (Wenlock) ?Patrick Burn Formation, Scotland, UK. C, complete specimen.
D, close-up of box in C; white arrows indicates ophthalmic ridge. E, F, Bunodes sp. depicted in Bergström (1975) (NHMUK
IA 48425) from the Upper Silurian-aged Upper Ludlow Formation(?), England. Possible ophthalmic ridges (white arrow)
that flank a central ridge in addition to other radial ridges. E, complete specimen. F, close-up of box in E, showing putative
evidence for an ophthalmic ridge and the poorly preserved remains of a possible lateral compound eye. Converted to
greyscale. Photograph credit: A–F, Javier Ortega-Hernández.
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6 R. D. C. BICKNELL ET AL.
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light. Houia yueya (NIGP 161923) was photographed
under ethanol. The xiphosurid Limulus polyphemus
(UNE.NHM.Z 272) was documented for comparison
with an extant species.
RESULTS
synzIphosurInes wIthout lateral compound
eyes
Cyamocephalus loganensis
The holotype (NHMUK IA 16521) from the Silurian-
aged (Wenlock) ?Patrick Burn Formation in Scotland
(Anderson, 1999) was originally thought to have an
LCE on the left side of the prosomal shield (Currie,
1927). However, we report no conclusive evidence of
LCEs and only weakly defined ophthalmic ridges
(Fig. 2C, D). Documentation of the more recently
studied Cyamocephalus cf. loganensis specimen
from the Late Silurian (Ludlow) ?Ludlow Group in
England (NHMUK IA 25) shows no evidence for LCEs
(Anderson, 1999). We confirm the lack of LCEs and note
that this specimen has more pronounced ophthalmic
ridges than the holotype (Fig. 2A, B).
Bunodes sp.
NHMUK IA 48425 from the Late Silurian-aged
(Ludlow) Upper Ludlow Formation(?) in England
was originally described has having LCEs along well-
defined ophthalmic ridges (Bergström, 1975). The type
material has not been re-examined since its original
publication. We found no convincing evidence for
LCEs upon revision, but ovate structures on possible
ophthalmic ridges (Fig. 2F) might represent the
location of an ocular structure. Additional material is
required before this aspect of the morphology can be
confirmed. Furthermore, other radial ridges are noted
(Fig. 2E, F).
Pseudoniscus falcatus
The holotype (NHMUK IA 44122) from the Silurian-
aged (Wenlock) ?Patrick Burn Formation, Scotland
(sensu Anderson, 1999) was originally described
and reconstructed with small, kidney-shaped
(reniform) LCEs on ophthalmic ridges (Woodward,
1868). In contrast, Størmer (1952) reconstructed
Pseudoniscus falcatus without LCEs. Reconsideration
of the holotype (Fig. 3A, B) shows no evidence of LCEs,
although prominent ophthalmic ridges are present,
particularly well expressed on the left side of the
prosomal shield.
Limuloides limuloides
This species from the Late Silurian-aged (Ludlow)
Leintwardine Formation, England was originally
described by Woodward (1865), who suggested that on
‘one side of the shield’ along a ridge there might be a
small LCE. This was supported by Bergström (1975:
fig. 1), who reconstructed Limuloides limuloides with
small (millimetric scale), ovate LCEs on the second set
of radial ridges. Reconsidering GSM 32393, we find
no evidence for LCEs, but well-defined radial ridges
(sensu Bergström, 1975) are noted (Fig. 3C, D).
Pseudoniscus clarkei
This species from the Late Silurian-aged (Ludlow,
sensu Gupta, 2014) Vernon Shale from New York State,
USA, was originally described by Ruedemann (1916) as
having small, lunular LCEs. Krzemiński et al. (2010)
doubted that Pseudoniscus taxa possessed any ocular
features. Re-examination of the Pseudoniscus clarkei
specimen (NSYM 19113) shows no evidence for LCEs,
but a prominent ophthalmic ridge is preserved on the
left side of the prosomal shield (Fig. 4A, B).
synzIphosurInes wIth lateral compound eyes
Pseudoniscus roosevelti
The other synziphosurine taxon from the Late Silurian-
aged (Ludlow, sensu Gupta, 2014) Vernon Shale in New
York State, USA was originally described by Clarke
(1902) as being blind. Ruedemann (1916) investigated
more specimens of Pseudoniscus roosevelti than
Clarke and suggested that LCEs were present, but
the legitimacy of his observations was doubted by
Eldredge (1974), Bergström (1975) and, more recently,
by Krzemiński et al. (2010). Re-examination of NYSM
19112 led us to the identification of a prominent
Figure 3. Pseudoniscus falcatus and Limuloides limuloides, which lack evidence of lateral compound eyes (LCEs). A, B,
P. falcatus (NHMUK IA 44122, holotype) from the Silurian-aged (Wenlock)?Patrick Burn Formation, Scotland. No evidence
for an LCE. A, complete specimen. B, close-up of box in A, showing a well-defined ophthalmic ridge (white arrow). C, D,
Limuloides limuloides (GSM 32393) from the Upper Silurian-aged (Ludlow) Leintwardine Formation, England. Note lack
of LCEs. C, complete specimen. D, close-up of box in C, showing the well-defined second radial ridge, which Bergström
(1975: fig. 1) suggested housed the LCE (white dotted line). No evidence for an LCE is noted. Photograph credit: A, B, Javier
Ortega-Hernández; C, D, Simon Harris.
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8 R. D. C. BICKNELL ET AL.
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reniform LCE preserved on the left side of the
prosomal shield (Fig. 4C, D). There is no evidence for
the presence of ophthalmic ridges on the prosoma.
The LCE is 2.1 mm from the anterior, 4.5 mm from
the posterior, 2.2 mm from the lateral boarders and
2.5 mm from the prosomal midline. The LCE outline is
darker than the surrounding specimen, and most of the
posterior 0.3 mm section is completely pigmented. The
eye is 0.5 mm wide and 0.9 mm long. Possible evidence
for ommatidia is also preserved (Fig. 4D), consisting of
a quadruplet of circular lenses on an isolated lateral
patch of dark material, with another lens triplet on the
anterolateral margin of the preserved eye.
Legrandella lombardii
The holotype (AMNH 29273) from the Early Devonian-
aged (Emsian–Eifelian, sensu Hernández et al., 2018)
Icla Formation in Bolivia was originally described as
having slit-shaped LCEs on both sides of the anterior
prosomal shield (Eldredge, 1974). We corroborate this
observation (Fig. 5A, B). Lateral compound eyes are
located ~21 mm from the midline of the prosomal shield
along well-defined ophthalmic ridges. Furthermore, we
report that well-preserved ommatidia are expressed
in the facets of the LCEs (Fig. 5C) (Eldredge, 1974).
At least 26 ovate ommatidia are preserved on the left
LCE. Sizes range between 0.39 and 0.61 mm wide, but
are mostly ~0.6 mm wide.
euchelIcerates wIth lateral compound eyes
Lunataspis aurora
The holotype (MM I-4000A) from the Late Ordovician-
aged (Hirnantian) ?Churchill River Group from Canada
was originally described as having reniform LCEs on
both sides of the prosomal shield (Rudkin et al., 2008).
We corroborate this description and note that the LCE
on the left side is more pronounced than the right (Fig.
5D, E). The LCEs taper anteriorly towards a point and
are located on a weakly developed ophthalmic ridge
(Rudkin et al., 2008). The eye is only slightly darker
than the surrounding specimen. Lateral compound
eyes on MM I-4000A (Fig. 5D) are located 5 mm from
the prosomal midline, 9 mm from the anterior, 5 mm
from the posterior and 6 mm from the prosomal lateral
boarders. The posterior eye section is pigmented and
darker than the anterior (Rudkin et al., 2008). There is
no clear evidence of preserved ommatidia.
Houia yueya
The original description of Houia yueya from the Early
Devonian-aged (Lochkovian) Xishancun Formation
in Yunnan, China reported no conclusive evidence
for LCEs (Lamsdell et al., 2013). On reconsideration
of the taxon by Selden et al. (2015), ovate LCEs
were noted on both sides of the prosomal shield, a
statement that we reaffirm here (Fig. 6A, B). Lateral
compund eyes are 8 mm from the lateral, 10 mm from
the posterior and 4 mm from the anterior boarders
and 4 mm from the prosomal midline. Ophthalmic
ridges are absent. The LCEs have a dark, pigmented
border (Fig. 6B).
Kasibelinurus amicorum
The holotype (AM F 68969), from the Late Devonian-
aged (Famennian, see Holland, 2010) Mandagery
Sandstone in Australia was originally described as
having LCEs on both sides of the prosoma (see Pickett,
1993). We found evidence for only a single LCE,
preserved as an ovate structure on the right prosomal
shield (Fig. 6C–E). Ophthalmic ridges are absent. The
LCE is located 10 mm from the anterior, 10 mm from
the posterior and 18 mm from the lateral boarders and
8 mm from the prosomal midline. The eye has a small
amount of relief (2 mm) when considered in profile
view (Fig. 6E).
Limulus polyphemus
The extant American horseshoe crab has reniform
LCEs with visible ommatidia (Fig. 7A–E; Harzsch
et al., 2006; Miether & Dunlop, 2016; Strausfeld et al.,
2016). Limulus polyphemus LCEs can have > 1000
ommatidia, and Poschmann et al. (2016) suggested an
average lens width of 0.14 mm. This value depends on
the age, size, and sex of a given specimen. This taxon
contrasts with other extant chelicerates that have
more derived eyes and a greatly reduced number of
lenses (Battelle, 2006; Harzsch et al., 2007). Lateral
compound eyes on the studied specimen are located
in the centre of the cephalothorax, 22 mm from the
lateral border on both sides of the cephalothorax and
Figure 4. Examples of Pseudoniscus from the Upper Silurian-aged (Ludlow) Vernon Shale, New York State, USA. A, B,
Pseudoniscus clarkei (NSYM 19113), without any evidence for a lateral compound eye (LCE). A, complete specimen. B, close-up
of box in C, showing well-defined ophthalmic ridge (white arrow). C, D, Pseudoniscus roosevelti (NYSM 19112) displaying
a reniform LCE preserved on the left side of the prosomal shield. C, complete specimen. D, close-up of box in C. Note dark
pigmentation of eye and ommatidia (black arrows). Photograph credit: A, B, Lisa Amati; C, D, Russell Bicknell.
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10 R. D. C. BICKNELL ET AL.
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located along well-defined ophthalmic ridges (Fig. 7D,
E; Bicknell et al., 2018).
DISCUSSION
The fossil record of vision in synziphosurines has
apparently been overstated. Lateral compound
eyes have been reported previously for Bunodes sp.,
Cyamocephalus loganensis, Limuloides limuloides,
Pseudoniscus clarkei and Pseudoniscus falcatus, but
we find little convincing evidence for ocular features
in these taxa, rectifying previous descriptions by
Woodward (1865, 1868) Ruedemann (1916), Currie
(1927) and Bergström (1975) (Figs 1, 8; Table 1),
although additional specimens may further clarify
the presence of LCEs in these taxa. Furthermore,
we conclude that ophthalmic or radial ridges
cannot be used to indicate the presence of LCEs in
synziphosurines because this exoskeletal feature is
widespread within the group, including blind forms
with exceptionally preserved soft tissues (Moore et al.,
2005a, b; Briggs et al., 2012). The LCEs expressed as
dark compressions in Pseudoniscus roosevelti (Fig. 4C,
D) and well-preserved individual ommatidia in the
LCEs of Legrandella lombardii (Fig. 5C) demonstrate
that synziphosurines were not entirely devoid of visual
prowess. It suggests that future fossil discoveries will
probably illuminate the diversity of ocular structures
in these euarthropods. Where LCEs are preserved
in the studied taxa, excluding the three-dimensional
visual facets in Legrandella lombardii, they often
consist of flat impressions that result from taphonomic
compaction. We suggest that most of the fossil taxa
probably exhibited a degree of prosomal curvature and
that the LCEs would have been located on the lateral
margins of the prosoma, similar to extant horseshoe
crabs. It is possible that other taphonomic processes
have dramatically affected the record of LCEs in
early euchelicerates. However, the absence of ocular
structures in synziphosurines might also be indicative
of a true biological signal linked to selection pressures
in the aquatic infaunal environment, because the
fossil record of eurypterids and chasmataspidids
shows that LCEs are commonplace in phylogenetically
more derived taxa with a similar body composition and
preservation potential (Anderson et al., 2014; McCoy
et al., 2015; Miether & Dunlop, 2016). The uneven
occurrence of LCEs in these groups might also reflect
ecological adaptations, as suggested for trilobite
groups that inhabited infaunal environments below
the photic zone, leading to secondary loss of visual
structures (Thomas, 2005).
evolutIonary ImplIcatIons
Our revision of the fossil record of synziphosurine LCEs
carries direct implications for the evolution of these visual
structures in Euchelicerata. Recent reconstructions of
chelicerate phylogeny indicate that synziphosurines and
other early Palaeozoic xiphosurans are not monophyletic
(see Lamsdell, 2013, 2016; Selden et al., 2015; contra
Eldredge, 1974), but rather a paraphyletic assemblage of
taxa that occupy positions as stem-group euchelicerates
(e.g. Legrandella lombardii), stem-group xiphosurans
(e.g. Kasibelinurus amicorum, Lunataspis aurora) or
stem-group arachnids (e.g. Pseudoniscus roosevelti,
Cyamocephalus loganensis, Lamsdell et al., 2015,
Houia yueya) (see Lamsdell et al., 2015: fig. 5; Fig. 8 in
the present paper).
When plotted against the phylogenetic relationships
of early euchelicerates, our data on the occurrence
and shape of LCEs offer some insights into the
evolution of euarthropod vision (Fig. 8). Legrandella
lombardii represents the only member of stem-
group Euchelicerata with LCEs (Figs 5A–C, 8), made
all the more significant by the presence of well-
defined and conspicuous ommatidial lenses (see also
Eldredge, 1974). In contrast, all other taxa in this
position are entirely devoid of ocular structures, but
may have ophthalmic ridges, such as the stem-group
euchelicerates Offacolus kingi Sutton et al., 2002 and
Weinbergina opitzi (Moore et al., 2005a). Critically,
all these blind forms are known from exceptional
deposits; therefore, there is little ambiguity as to
whether taphonomic alteration resulted in the
absence of LCEs. Within stem-group Xiphosura, both
Kasibelinurus amicorum (Fig. 6C–E) and Lunataspis
aurora (Fig. 5D, E) preserve LCEs, but details of
individual ommatidia are indistinct, and in the case
of Kasibelinurus amicorum, completely unknown.
Finally, stem-group arachnids include a combination
Figure 5. Synziphosurine Legrandella lombardii and xiphosuran Lunataspis aurora, with lateral compound eyes (LCEs).
A–C, Legrandella lombardii (AMNH 29273, holotype) from the early Devonian-aged (Emsian–Eifelian) Icla Formation,
Bolivia, with slit-shaped LCEs on both sides of the prosomal shield. A, left lateral view. B, anterior view. White arrow
indicates LCE and close-up in C. C, close-up of left LCE showing ommatidia. Ammonium chloride coated. D, E, Lunataspis
aurora (MM I-4000A, holotype) from the Late Ordovician-aged (Hirnantian) ?Churchill River Group, with a reniform LCE
prominent on the left prosomal shield. D, complete specimen. E, close-up of box in D, showing pigmented LCE and no
evidence for ommatidia. Photograph credit: A, B, Russell Bicknell; C, Melanie Hopkins; D, E, Graham Young.
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EYES IN PALAEOZOIC HORSESHOE CRABS 11
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Figure 6. Houia yueya and Kasibelinurus amicorum, with lateral compound eyes (LCEs). A, B, Houia yueya (NIGP
161923) from the Devonian-aged (Lochkovian) Xishancun Formation, Yunnan, China, with ovate LCEs on both sides of the
prosomal shield. A, complete specimen. B, close-up of box in A, showing LCE (in dotted outline). C–E, Kasibelinurus amicorum
(AM F 68969, holotype) from the Late Devonian-aged (Famennian) Mandagery Sandstone, Australia, with an ovate LCE
preserved on the right prosomal shield. C, complete specimen. D, close-up of box in C, showing lighter coloured LCE (white
dotted outline). E, LCE in D in profile view, showing relief of the minute feature. Photograph credit: A, B, Paul Selden; C–E,
Patrick Smith.
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12 R. D. C. BICKNELL ET AL.
© 2019 The Linnean Society of London, Zoological Journal of the Linnean Society, 2019, XX, 1–17
of blind forms (e.g. Cyamocephalus loganensis,
Bunodes sp., Limuloides limuloides) and taxa
with preserved LCEs, even if they do not contain
indisputable evidence of the individual lenses, such as
Winneshiekia youngae and Houia yueya (Fig. 6A, B).
Pseudoniscus roosevelti (Fig. 4C, D) represents an
important exception in this regard, but it is the only
stem-group arachnid outside of Dekatriata in which it
is possible to observe minute aggregations of tightly
packed lenses (Fig. 8 ). Lateral compound eyes are better
known in phylogenetically more derived stem-group
arachnids, such as chasmataspidids and eurypterids,
although well-preserved discrete ommatidia are
known only for the latter group (Anderson et al., 2014;
Miether & Dunlop, 2016; Strausfeld et al., 2016).
The phylogenetic distribution of preserved LCEs
in early Palaeozoic synziphosurines and xiphosurans
results in two equally plausible hypotheses for
evolution of these visual structures in Euchelicerata.
The fact that Legrandella lombardii is the LCE-
bearing taxon that occupies the earliest divergent
phylogenetic position as a stem-group euchelicerate
(Fig. 8) suggests that the elongate slit-shaped LCEs
with prominent ommatidia might reflect the ancestral
morphology for Euchelicerata. In the alternative
hypothesis, it is possible that the reniform LCEs that
typify extant Limulus polyphemus and several other
Palaeozoic forms represent the ancestral organization
and that the elongate eyes of Legrandella lombardii
are secondarily derived, despite its stem-group
euchelicerate affinities. This second scenario is more
congruent with the stratigraphic age of several key
taxa, because Legrandella lombardii is a Middle
Devonian taxon, whereas Ordovician (Lunataspis
Figure 7. The xiphosurid Limulus polyphemus (UNE.NHM.Z 272), with lateral compound eyes (LCEs). A, dorsal view
of specimen. B, left lateral view of specimen. C, right lateral view of specimen. D, close-up of LCE in B, showing large
ommatidia. E, close-up of LCE in C, showing pronounced ommatidia. Photograph credit: A–E, Russell Bicknell.
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14 R. D. C. BICKNELL ET AL.
© 2019 The Linnean Society of London, Zoological Journal of the Linnean Society, 2019, XX, 1–17
aurora) and Silurian (Pseudoniscus roosevelti) forms
possess the more conventional reniform LCEs. However,
we caution against placing too much emphasis on
the age alone, because several of the taxa occupying
a stem-wards phylogenetic position are Silurian (e.g.
Offacolus kingi, Briggs et al., 2012) or Devonian (e.g.
Weinbergina opitzi), whereas comparatively more
crown-wards taxa are as old as the Ordovician (e.g.
Lunataspis aurora, Winneshiekia youngae).
The possibility that Legrandella lombardii LCEs
might represent a key innovation in euchelicerate eye
evolution carries additional implications pertaining
to the ontogenetic development and ecology of the
structures observed in extant Xiphosurida. The LCEs
of Limulus polyphemus develop in a motif known as the
‘row by row’ type, in which new ommatidia are produced
at the eye edge from a proliferation zone (e.g. Harzsch
& Hafner, 2006). Given that the eye field in the LCEs
Figure 8. Evolution of lateral compound eyes in Palaeozoic Chelicerata. Simplified topology follows Lamsdell (2013, 2016)
and Lamsdell et al. (2015). Question mark (?) denotes lack of definitive evidence for preserved discrete ommatidial lenses
in the compound eyes.
Table 1. Summary of fossil evidence of lateral compound eyes (LCEs) in taxa examined in this study
Taxon Higher
classification
Age Formation LCE information Eye shape
Bunodes sp. Synziphosurine Late Silurian
(Ludlow)
?Upper Ludlow
Formation, England
Possible ophthalmic
ridges with putative
evidence for LCEs
–
Cyamocephalus
loganensis
Synziphosurine Silurian
(Wenlock) and
Late Silurian
(Ludlow)
?Patrick Burn
Formation, Scotland;
?Ludlow Group,
England
No evidence for LCEs,
well-defined
ophthalmic ridges
–
Limuloides
limuloides
Synziphosurine Late Silurian
(Ludlow)
Leintwardine
Formation, England
No evidence for LCEs,
well-defined radial
ridges
–
Pseudoniscus
falcatus
Synziphosurine Silurian
(Wenlock)
?Patrick Burn
Formation, Scotland
No evidence for LCEs,
well-defined
ophthalmic ridges
–
Pseudoniscus clarkei Synziphosurine Late Silurian
(Ludlow)
Vernon Shale, USA No evidence for LCEs,
well-defined
ophthalmic ridges
–
Pseudoniscus
roosevelti
Synziphosurine Late Silurian
(Ludlow)
Vernon Shale, USA Large, well-defined
LCE, no ophthalmic
ridges, ommatidia
present
reniform
Legrandella
lombardii
Synziphosurine Early Devonian-
aged (Emsian–
Eifelian)
Icla Formation, Bolivia Large, well-defined
LCEs and
ophthalmic ridges,
ommatidia present
Slit-like
Lunataspis aurora Euchelicerate Late Ordovician
(Hirnantian)
?Churchill River
Group, Canada
Small, well-defined
LCEs, weakly
developed oph-
thalmic ridge
reniform
Houia yueya Euchelicerate Early Devonian
(Lochkovian)
Xishancun Formation,
China
Well-defined LCEs, no
ophthalmic ridges
Ovate
Kasibelinurus
amicorum
Euchelicerate Late Devonian
(Famennian)
Mandagery Sandstone,
Australia
Small, weakly defined
LCE, no ophthalmic
ridge
Ovate
Limulus polyphemus Xiphosurida Recent – Large, well-defined
LCEs and oph-
thalmic ridges,
ommatidia present
reniform
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EYES IN PALAEOZOIC HORSESHOE CRABS 15
© 2019 The Linnean Society of London, Zoological Journal of the Linnean Society, 2019, XX, 1–17
of Legrandella lombardii is restricted to a thickness
of two, possibly three ommatidia, it suggests that the
anterior proliferation zone would have produced only
a limited number of lenses that would experience
substantial migration along the elongate eye field. The
mechanics of the row by row type of growth tends to
produce a roughly polygonal-shaped eye field (Harzsch
& Hafner, 2006), as observed in the reniform LCEs of
Limulus polyphemus and numerous other Palaeozoic
aquatic euchelicerates (Fig. 4C, 5D). Thus, the loss
of elongate eye morphology that typifies Legrandella
lombardii might result from positive selection for a
more efficient mode of eye growth. From an ecological
perspective, if Legrandella lombardii reliably indicates
a key innovation in stem-group euchelicerate LCEs,
then it suggests a fundamental behavioural shift
relative to more basal, blind forms (e.g. Offacolus kingi,
Dibasterium durgae, Weinbergina opitzi). Given that
the reniform LCEs of Limulus polyphemus play a
crucial role in navigation and mate recognition in
the marine environment (Barlow et al., 1982, 2001;
Barlow, 2009), it is conceivable that blind forms did not
require vision for either of these purposes. However,
as the most diverse and ecologically successful groups
of aquatic chelicerates are typified by complex visual
systems, particularly eurypterids (e.g. Anderson et al.,
2014; McCoy et al., 2015), the presence of LCEs for
object recognition (either prey or mate) would have
conveyed a clear adaptive advantage.
conclusIon
It is not possible to provide a definitive answer with
regard to the precise origin of the euchelicerate LCEs at
this time given the patchy fossil record of these delicate
features. However, our revision of the fossil record of
LCEs in Palaeozoic synziphosurines and xiphosurans
helps to resolve some standing questions on the evolution
of visual structures in this successful euarthropod
group. We posit either that the first appearance of LCEs
in Legrandella lombardii represents a key innovation in
euchelicerate vision, or that the reniform LCEs retained
in Limulus polyphemus are ancestral for at least crown-
group Euchelicerata (Fig. 8) (see discussion by Harzsch
& Hafner, 2006; Harzsch et al., 2006; Strausfeld et al.,
2016), in which case Legrandella lombardii LCEs are
secondarily derived. Furthermore, our findings lend
additional support to idea that LCE reduction is not
synapomorphic for Arachnida (e.g. Paulus, 2004), but
rather that the earliest stem-group arachnids (sensu
Selden et al., 2015) possessed the ancestral reniform
LCEs with numerous lenses, further demonstrated by
the presence of five or more lenses in younger Palaeozoic
and Mesozoic arachnids (see Miether & Dunlop, 2016).
ACKNOWLEDGEMENTS
This research was supported by funding from an
Australian Postgraduate Award (to R.D.C.B.) and a
Charles Schuchert and Carl O. Dunbar Grants-in-Aid
award (to R.D.C.B.). We thank Graham Young, Melanie
Hopkins, Paul Selden, Patrick Smith and Simon Harris
for specimen photographs. We thank David Legg,
David Marshall, Lyall Anderson, and Rachel Wade for
enlightening conversation. Finally, we thank the two
anonymous referees for their insightful review that
thoroughly improved the manuscript.
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