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Until now, the fossil record has not been capable of revealing any details of the mechanisms of complex vision at the beginning of metazoan evolution. Here, we describe functional units, at a cellular level, of a compound eye from the base of the Cambrian, more than half a billion years old. Remains of early Cambrian arthropods showed the external lattices of enormous compound eyes, but not the internal structures or anything about how those compound eyes may have functioned. In a phosphatized trilobite eye from the lower Cambrian of the Baltic, we found lithified remnants of cellular systems, typical of a modern focal apposition eye, similar to those of a bee or dragonfly. This shows that sophisticated eyes already existed at the beginning of the fossil record of higher organisms, while the differences between the ancient system and the internal structures of a modern apposition compound eye open important insights into the evolution of vision.
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Structure and function of a compound eye, more than
half a billion years old
Brigitte Schoenemann
a,b,1
, Helje Pärnaste
c
, and Euan N. K. Clarkson
d
a
Department of Zoology (Neurobiology/Animal Physiology), Biocenter Cologne, D-50647 Cologne, Germany;
b
Institut of Biology Education, D-50931
Cologne, Germany;
c
Kivion MTÜ, Tallinn 13517, Estonia; and
d
Grant Institute, School of Geosciences, University of Edinburgh, EH3 9LJW Edinburgh, Scotland
Edited by Dale Purves, Duke University, Durham, NC, and approved November 3, 2017 (received for review September 25, 2017)
Until now, the fossil record has not been capable of revealing any
details of the mechanisms of complex vision at the beginning of
metazoan evolution. Here, we describe functional units, at a
cellular level, of a compound eye from the base of the Cambrian,
more than half a billion years old. Remains of early Cambrian
arthropods showed the external lattices of enormous compound
eyes, but not the internal structures or anything about how those
compound eyes may have functioned. In a phosphatized trilobite
eye from the lower Cambrian of the Baltic, we found lithified
remnants of cellular systems, typical of a modern focal apposition
eye, similar to those of a bee or dragonfly. This shows that sophis-
ticated eyes already existed at the beginning of the fossil record of
higher organisms, while the differences between the ancient sys-
tem and the internal structures of a modern apposition compound
eye open important insights into the evolution of vision.
compound eye
|
visual system
|
arthropod
|
evolution
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Cambrian
Vision is one of the key factors in triggering evolutionary
changes. In many groups of animals, it is an essential support
for finding social partners for mating and it provides information
about the nature and settings of the environment. The race
between predator and prey and the need to seeand to be
seenor not to be seenwere drivers for the origin and sub-
sequent evolution of efficient visual systems, as well as for pro-
tective shells, systems of camouflage, and many adaptations and
strategies for survival, as the light switch theory(1, 2) formu-
lates. Effective vision was an important tool that aided survival in
the world of competition and selection.
The origin of vision still lies the dark.At the boundary be-
tween the PrecambrianCambrian (541 Ma), there is a sudden
appearance in the fossil record of entirely new organisms that can
be considered as the ancestors of most modern animal groups.
This event, known as the Cambrian Explosionor the Cambrian
Radiation,is a relatively short interval of time [ca. 20 (3, 4)25 (5,
6) My]. The early origins of complex animal life, however, actually
started in the Precambrian to continue during the Cambrian Ex-
plosion and the Great Ordovician Biodiversification Event(7).
Marine invertebrates of the Cambrian Explosion are, for ex-
ample, excellently represented in the Chengjiang Biota of China
(8, 9), Burgess Shale Fauna (10, 11), and Sirius Passet (12, 13), as
Orstenfossils (14, 15) and at other Lagerstätten. Many of
these organisms were equipped with eyes. Primordial single-lens
eyes existed in the lobopodians (16), worm-like creatures with
legs, which are now placed systematically among the Ecdysozoa,
and perhaps even camera eyes were present in the early chor-
dates and vertebrates of Chengjiang. The faunas of this period
were dominated by arthropods, showing basic compound eyes,
but there were also sophisticated lens systems, densely and
hexagonally packed, sometimes with several thousand facets (16
20). Some of these arthropods even possessed a second eye
system, which is typical for modern euarthropods, the ocellar
median eyes (18, 21, 22). Most spectacular were the highly acute
compound eyes of organisms that lived in the slightly younger
Emu Bay Formation of Australia (23, 24). Some of these
compound eyes have been assigned to the most impressive ar-
thropods of their time, anomalocaridids (radiodontids) (24).
The dominant preserved group among the early Cambrian
arthropods, however, was the trilobites, which were well equip-
ped with compound eyes from their very beginning. To have
insight into the internal structures of a lower Atdabanian trilo-
bites eye, an arthropod from one of the earliest of all trilobite
records of the Cambrian, would surely provide us with critical
information about the oldest documentable compound eyes so
far, as well as the state of visual organs at the beginning of the
metazoan fossil record.
Characterization of Schmidtiellus reetae Bergström, 1973 and
its Stratigraphic Assignments
The eye structures studied here are preserved in the holotype
specimen of Schmidtiellus reetae Bergström, 1973 (25) (Fig. 1A),
which is deposited at the Institute of Geology at Tallinn University
of Technology, Estonia, under repository number GIT 294-1.
S. reetae Bergström, 1973 (25) belongs to the group of Ole-
nelloidea (superfamily), occurring on all paleocontinents, that
presumably gave rise to all other groups of trilobites, because they
were simply the only trilobites at the beginning and the first of all
(2629). The origin of trilobites is still unclear in general (2629),
so no further phylogenetic discussion is possible at this point.
In Estonia, the lower Cambrian is represented by shallow
marine terrigenous sediments (clay, silts, and sandstones) of
which the alternations mark several water level low stands and
uplifts (3032). The lower Cambrian sediments accumulated in a
relatively shallow epicontinental basin on the Baltica Paleo-
terrane. Subsequently, different regions of Baltoscandia were
affected by postdepositional heating in different ways. The most
altered sediments are those in Norway, where temperatures
Significance
An exceptionally well-preserved arthropod fossil from near the
base of the lower Cambrian shows the internal sensory struc-
tures of a compound eye, more than half a billion years old.
The trilobite to which it belongs is found in a zone where the
first complete organisms appear in the fossil record; thus, it is
probably the oldest record of a visual system that ever will be
available. This compound eye proved to possess the same kind
of structure as the eyes of bees and dragonflies living today,
but it lacks the lenses that are typical of modern eyes of this
type. There is an elegant physical solution, however, of how to
develop a quality image of modern type.
Author contributions: B.S., H.P., and E.N.K.C. designed research; B.S., H.P., and E.N.K.C.
performed research; B.S. analyzed data; and B.S. and E.N.K.C. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This open access article is distributed under Creative Commons Attribution-NonCommercial-
NoDeriv atives L icense 4. 0 (CC BY-N C-ND).
1
To whom correspondence should be addressed. Email: B.Schoenemann@uni-koeln.de.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1716824114/-/DCSupplemental.
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EVOLUTIONBIOPHYSICS AND
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ranged between 150 °C and 200 °C during the Caledonian
Orogeny (33), while superb preservation of acritarch organic
material in Estonia indicates temperatures well below 100 °C
(34). Here, the cuticular exoskeletons of the trilobites are ex-
ceptionally well preserved in contrast to those in some other
regions of the world, which have been demineralized and may
have vanished altogether.
The nearly complete specimen of S. reetae Bergström, 1973
(25) described here was collected from the Saviranna section
below the beds with Schmidtiellus mickwitzi (Schmidt, 1888) (35)
but above the beds with Rusophycus trace fossils, which sup-
posedly mark arthropod (likely trilobite) traces, and contains
fragmentary unidentified trilobites, possibly also Schmidtiellus.
The alternating successions of clay and silt in the Lükati For-
mation of the Dominopolian regional stage correlate with the
lowermost part of the Atdabanian (22, 3640) or may extend
down into the underlying Tommotian as suggested by the global
acritarch succession (41, 42). Consequently the trilobite de-
scribed here may be older than the fauna represented in the
Chengjiang Fauna,which is correlated to the Qiongzhusian
(43, 44), a stage correlated with the late Atdabanian stage in
Siberian sequences of the middle of the lower Cambrian (4447).
The stratigraphy of the lower lower Cambrian is an object of
intense research and discussion; it is broadly demonstrated and
accepted, however, that the oldest trilobite fossils were preceded
by arthropod (possibly trilobite) traces (40) as reported here. It
has been demonstrated, unequivocally in a very few cases, when
in trace fossils like Rusophycus and Cruziana, trilobite specimens
have actually been found in the trace they were making, but not,
so far as we are aware, for any Cambrian examples as old as the
cases we are referring to [those were upper Cambrian (48)]. S.
mickwitzi (Schmidt, 1888) (35) and S. reetae Bergström, 1973 (25)
belong to an early trilobite assemblage comparable to those of
the oldest assemblages of the lower Atdabanian of Siberia and
lower Ovetian of France, Spain, and Antarctica, or the earliest
trilobites of Morocco [Issendalenian (approximately lower Ove-
tian) (49)] and Laurentia (Montezuman). All these trilobites
are more or less coeval. The early trilobites of China [Nangao
(approximately middle Ovetian, upper Atabanian) (40)] are
slightly younger (5, 39) (Fig. S1).
Baltoscandian trilobites are among the earliest in the world
(40). They occur coevally with the assemblages of the lower
Atdabanian of Siberia [Profallotaspis,Bigotinella,Bigotina (Ole-
nelloidea, at the base of the Atdabanian)], Laurentia (olenellids
of the Fritzaspis zone, uppermost part of the Begadean stage,
which is correlated to the lower Atdabanian of Siberia), the
bigotinid trilobites from southern Europe, Spain, and France
(lower Ovetian, correlated to the lower Atdabanian), and the
assemblages of Antarctica (Lemdadella lower Ovetian stage,
correlated to the lower Atdabanian), while the oldest trilobites
from Morocco (Bigotina,Eofallotaspis,Fallotaspis, and Lemda-
della Issendalenian) and the redlichiid trilobites of China (Aba-
diella,Abadiella zone correlates with the upper Atdabanian) and
Australia (Abadiella) are slightly younger (39, 40).
The Cambrian Explosion or Cambrian Radiation started about
542 Ma (36, 46, 50), and the Cambrian Radiation of rich ar-
thropod faunas is known mainly from rare time windowspre-
serving fossil Lagerstätten. The best known and studied are the
Chengjiang Biota (520 Ma) in China (e.g., refs. 8, 9); Sirius Passet
Biota in Greenland (518 Ma) (e.g., refs. 51, 52); Emu Bay For-
mation on Kangaroo Island, Australia (514 Ma) (e.g., refs. 53,
54); and the biotas of the Kaili Formation in China (510 Ma)
(e.g., refs. 44, 45), or the slightly younger fauna of the middle
Cambrian Burgess Shale Formation in British Columbia, Can-
ada (508 Ma) (e.g., refs. 10, 11); the middle Cambrian Weeks
Formation (late Guzhangian, 497500.5 Ma) in Utah (e.g., refs.
55, 56); and the Orsten fossils (e.g., refs. 14, 15). Meanwhile more
than 50 of these Burgess Shale-type biotas have been described so
far (e.g., ref. 56). The critical point here is that the Baltoscandian
trilobites are older than any of these famous Lagerstätten (Fig. S1).
The cuticle of S. reetae is preserved as calcium phosphate,
which often allows the record of finest details, such as, for ex-
ample, in the filter-feeding branchiopod Rehbachiella kinne-
kullensis from upper Cambrian limestone concretions collected
in southern Sweden, where fine setae and setulae (<1μm) were
shown to be present on its appendages (14).
This is most unlikely to be primary, considering that all other
trilobites have cuticles of calcite set in an organic base (57).
Secondary phosphatization, however, is quite common in trilo-
bites and other Cambrian fossils; cases that come immediately to
mind are the magnificently preserved Orsten crustaceans and
other fossils, with perfectly preserved appendages, from the
Furongian of central Sweden (58, 59). Other examples are the
lower Cambrian bradoriids and eodiscids in perfect preservation
from South China (60). Finally, there is evidence of the preser-
vation of ommatidia in lower Cambrian radiodontans (61), and
the preservation of ommatidia by phosphatization has also been
reported recently in a Jurassic crustacean (62).
The availability of vast quantities of phosphate in the Cam-
brian (63) was apparently set in motion by a massive marine
transgression at the beginning of the Cambrian that generated
substantial upwelling. The phosphorus and other vital elements
that had accumulated on the late Precambrian ocean floors for
millions of years were thus released into the upper waters of the
sea, to be made available both for the formation of organo-
phosphatic shells, as in inarticulated brachiopods, and for the
proliferation of phosphate bacteria, which covered the surfaces
of calcareous and other shells in micrometric deep layers, pro-
ducing a thin but durable shell, replicating outer and inner sur-
faces. Solution-containing carbonate rocks, containing such
fossilized shells in weak acids, release the replicas, which are
then available for study (63). South China was a major center of
such phosphatic replication in lower Cambrian times; however,
by the middle Cambrian, this center had shifted to Australia. It is
likely that phosphatization spread to the inner parts of the shells
in some instances, so that what had been entirely calcite became
Fig. 1. Trilobite S. reetae Bergström, 1973 (25) (GIT 294-1) and its com-
pound eye. (A) Holotype. (B) Head region of A.(C) Fields of view.
(D) Abraded part of the right eye. Arrowheads indicate the ommatidial
columns. (E) Lateral view of the right eye. (F) Schematic drawing of E.
(G) Two visual units (big arrows in D). (H) Schematic drawing of G. (Scale
bars: AC, 1 cm; D, 1 mm; Eand F, 2 mm; and G, 200 μm.)
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solid phosphate. This is what seems to have happened to our
specimen of Schmidtiellus.
Another possibility is that increasingly deep bioturbation in
the early Cambrian disturbed the surface layers of the sediment
and released minerals from the lower layers (64).
Results
Compound eyes of apposition type are typical of modern diurnal
arthropods, whereas more advanced and sensitive systems (su-
perposition eyes) may not have existed before the Devonian
[419.2 ±3.2 Ma358.9 ±0.4 Ma (65)].
Apposition compound eyes are composed of numerous iden-
tically repeated visual units, the ommatidia. Recognizable ex-
ternally as facets, they consist, among the Mandibulata, of a
cuticular corneal lensand a so-called crystalline conefo-
cusing the incident light onto the tip of a central light-guiding
structure, the rhabdom, lying underneath [focal apposition
eye,sensu Land and Nilsson (66)]. In its longitudinal section,
the crystalline cone often forms an approximately triangular
shape. In aquatic systems, the difference in optical density be-
tween water and the organic material that forms the lens is not
high enough to supply the capacity for effective refraction; thus,
normally, it is the crystalline cone instead of the lens that forms
an effective dioptric apparatus. The central rhabdom is part of
the receptor cell system; these cells lie arranged around it like a
rosette. The number of receptor cells is variable and depends on
the species; very commonly, there are eight of them. In a focal
apposition eye, all stimuli within the visual field of each facet are
focused, and thus concentrated on the distal tip of the rhabdom,
averaged to one mean light impression. Screening pigment cells,
differing in number among species, optically isolate the visual
units from each other. Thus, the focal apposition eye as a whole
provides a perceived mosaic-like image (67, 68). The acuity of
such eyes depends, among other factors, on the number of facets:
The more there are, the higher is the quality of the image (in the
same way that pixels define the quality of a computer graphic).
The acuity of the image relates also to the acceptance angle of
the rhabdoms [between 0.8° and 10° for most compound eyes
(69)], and the sensitivity of the eye also depends, among other
factors, upon the latter.
As with all coeval trilobites, S. reetae lived as benthos. Gliding
over the sea floor it had, in common with all (more or less)
contemporary genera of olenellid trilobites, such as Holmia,
Lemdadella,Fallotaspis, and others, reniform eyes with a narrow
slit-like visual surface oriented toward the front and especially
toward the lateral horizon (Fig. 1 B,C,E, and F). Conspicuously,
the top of the eye is covered by a lenseless top surface, the
palpebral lobe,and the visual field does not extend upward
more than 2530° above it. This is a common pattern in early
trilobites generally, but why that is so remains an open question.
It is likely that the vertically narrow visual field limited the dis-
tracting effect of bright light signals from the lower surface of the
water. The horizontal visual field of S. reetae covers 2×124°
(Fig. 1 Band C); thus, the eye was able to scan the seafloor
anterolaterally around the trilobite. There were certainly free-
swimming predators capable of tackling trilobites, which, in a
more or less homogeneous environment on the sea floor, could
be detected already from a distance by this wide, horizontally
directed visual field.
The eye of the specimen investigated here is about 10 mm
long and 4.5 mm wide The lateral aspect of the compound eye
shows that the elongated, crescentic visual surface has just a few
(<100), relatively large lenses (50 μm) (Fig. 1 Eand F).
Functionally, even a small number of such lenses could pick up the
movement of potential predators passing within the field of view,
as a result of change in light intensity detected by one omma-
tidium after another. Thus, the system probably worked as a
movement detector rather than as an image-forming eye, but
also as an obstacle detector when scanning the environment.
In the specimen S. reetae Bergström, 1973 (25) GIT 294-1-1, the
palpebral lobes are present, although their papillated upper sur-
faces are slightly abraded. While all structures are destroyed su-
perficially in the left eye, this is not so with the right eye, which
allows extraordinarily rare insight into its internal structures.
Several internal relicts ranged against the ocular suture may be
seen here, which presumably, on account of their position,
belonged to the lowest part of the eye. There may be as many as
seven of these, some in situ and others slightly displaced (Fig. 1D).
In the best preserved of these (Figs. 1 D,G, and Hand 2 BD
and J), the lenses (1 mm in diameter), broken across, are ex-
tremely flat and thin, showing no convexity (Figs. 1 Gand Hand
2C,D, and J). Beneath the lens lies a basket-like structure,
consisting of spherical elements, perhaps former cells (Figs. 1 G
and Hand 2 BDand J). It is about 460 μm high and probably
about 1.3 mm wide. In its center is a conical tube, broken at its
upper side. The distal surface shows the conical tube to consist of
seven elements of similar but different sizes (50 μm) grouped
around a central core (Figs. 1 Gand Hand 2 BDand J), what
must be a sensory complex in the form of seven radially
arranged, more or less triangularly shaped elements (receptor
cells) grouped around a central structure (rhabdom). This con-
ical tube has a diameter of 160 μmandalengthof338 μm, and
Fig. 2. Internal structures of the functional visual unit. (A) Ommatidium.
Note the cellular elements (relicts of receptor cells) arranged radially around
the central core (relict of the rhabdom). (B) Ommatidium positioned in a
basket. Note the cellular elements (relicts of receptor cells) arranged radially
around the central core (relict of the rhabdom). (C) General aspect of Bfor
interpretation in D.(E) General aspect of Afor interpretation in F.(G) Cross-
section of the ommatidium of the extant crustacean Dulichia porrecta (Bate,
1857) (87) (Crustacea, Amphipoda) (88). (H) Schematic drawing of the ele-
ments of a typical sensory system in the aquatic compound eye in G.(I)
Schematic drawing of a longitudinal section of an ommatidium. (J) Schematic
drawing of the visual unit of S. reetae. b, basket; cc, crystalline cone; L, lens;
om, ommatidium; p, pigment screen; r, rhabdom; sc, sensory (receptor) cells.
(Scale bars: A,B,E,F,andJ, 200 μm; Cand D,100μm; and G,1μm.)
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EVOLUTIONBIOPHYSICS AND
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it connects centrally with a long thin tube that is directed inward
(500 μmlong,70 μm Ø in diameter). The total length cannot
be described because the proximal end of the system plunges
downward outside the bottom of the basket.Distally from the
tube, a regular, triangular element (56 μm high, 350 μm wide)
can be seen, positioned directly below the lens (Figs. 1Gand 2
BDand J). Distally from the tube, a regular, triangular element
(56 μm high, 350 μm wide) can be seen, positioned below the
lens,which slightly covers this triangular element. It can be
interpreted as a kind of crystalline cone because of its triangular
shape (from a side view) and its relative position between lens
and sensory complex. These elements and their arrangement are
typical for compound eyes of the appositional type, as explained
before. The typical position within of the unit of a compound eye
excludes other possibilities for explaining this pattern, formed so
characteristically for an ommatidium. Additionally, at least we
do not know of any plant-based pattern, protozoan structure, or
mineral structure that would be similar.
Close to it, on the left-hand side, and at a distance of about
1 mm from the first, a second conical tube-like structure similar
to the first, although displaced and rotated, can be clearly seen
(Figs. 1 D,G, and Hand 2 A,E,F, and J). It has a total length of
364 μm, and is 208 μm wide. It ends proximally in a small tube
70 μm in diameter, which sinks into the depth of the matrix.
There are seven triangular elements (largest: 70 μm, smallest:
56 μm) that surround a central circular structure (diameter 20 μm).
The difference in the diameter of both tubular systems of
about 48 μm(160 μm vs. 208 μm) can be explained by a
difference in structure: The second system is embraced by a wide
membrane-like sheet, while the sheet of the first system de-
scribed is thinner. Another difference between the two systems is
that inside the seven elements of the first system, just a dark
irregular spot can be seen, while in the second system, dark areas
surrounded by a membrane can be more clearly made out. In
their principal structure, however, both elements are congruent.
This system seems to have a triangular element between the lens
and tubular element also; this, however, appears distorted (Figs.
1Gand Hand 2 E,F, and J).
In comparison to many modern, compact systems, such as
those of bees or dragonflies, the large distance (one systems
diameter is 1 mm) between the ommatidial cones is remark-
able, and may have provided or supported an effective optical
isolation of the individual visual units.
We are aware that due to the limited amount of data, only a
generalized description of the performance of this early eye is
possible. There exist measurable parameters, however, that allow
an approximate estimation, and thus a rough characterization, of
this early visual system. In comparison to terrestrial visual sys-
tems, aquatic vision suffers by the absorbance of light in water;
thus, in principle, the compound eyes of aquatic arthropods, at
the same time of the day, require a higher sensitivity than those
of terrestrial organisms. This is all the more so the deeper the
arthropod lives in the water column. Under low-light conditions,
vision appears very noisybecause the low photon numbers
show relatively large random fluctuations. This improves with
receptors capable of a high photon capture rate. This photon
capture rate can be increased by a wide aperture (lens diameter)
A, a large diameter of the receptor (rhabdom) d, and a sufficient
length of the absorbing structure (rhabdom) x(70, 71). Land (70,
71) defined a fine measure to describe the capacity of a receptor
in a compound eye to capture light: the sensitivity S. It describes
the rate of photons absorbed by each receptor to the number of
photons emitted per steradian by 1 m
2
of an extended stan-
dardized source, and this would enable a comparison between
the ancient visual system investigated here and the sensitivities of
recent arthropods:
S=π
22
·A
f2
·1ekx=0.64 ·ð350=156Þ2·1e0.0069·338
=2.91m2·sr.
[Ssensitivity, (0.64) is derived from the circular shape of the
system (70), Aaperture (μm]), ffocal length, kabsorption co-
efficient of the photopigment [0.69% per micrometer; lobster
(72), after Land 1981 (70)], x(μm) length of the perceiving
structure (rhabdom), here 338 μm (length of the rhabdom ap-
proximates length of the tubular structure, which is interpreted
as an ommatidium).]
For the first discussed system the sensitivity results to 2.91
[m
2
·sr]. Thus, the approximate estimated sensitivity of S. reetae
Bergström, 1973 (25) is very similar to that of the branchiopod
crustacean Artemia salina (Linnaeus, 1758) (73) [S=2.3 [m
2
·sr]
(71)] when it is dark-lightadapted. A. salina is a shallow water
inhabitant, and the results presented here are in accordance with
sedimentological evidence, which indicates that this benthic tri-
lobite inhabited shallow waters also.
An effective parameter describing an eyes light-gathering capacity
is the F-number: F=f/D,wherefis the focal length and Dis the
diameter of the lens. It is familiar to all photographers that cameras
with low F-numbers produce bright images (ref. 69, p. 75). If we
accept that this eye is a focal apposition eye because of the conical
shape of the crystalline cone, the system suggests that the focused
light fell on the tip of the rhabdom; thus, f156 μm. Furthermore if
we take, as discussed, the upper width of the crystalline cone as
aperture A350 μm, the F-number can be calculated as 2.2. This
value matches F-numbers typical for lenses of recent apposition eyes,
which normally show F-numbers of about 2 (69, 70, 71).
As mentioned, the resolution of this early compound eye is
rather low. Because the rhabdom acts as a light-guiding structure,
the light is trapped into the system only up to a critical angle (Φ
crit
),
which is given by arcsin (n
1
/n
2
). The refractive index of sea water is
about n
1
=1.34 (35% salinity, 20 °C), and n
2
=1.361.40 for the
rhabdom (ref. 66, p. 59). The results are an acceptance angle for the
rhabdom of 2030° and overlapping visual fields of each system, as
is quite common in modern compound eyes. The interommatidial
angle (Δϕ) lies at about 10°. In terrestrial systems not suffering from
light absorbance, such as insects, they often range from 15° (74). In
aquatic crustaceans and xiphosurans with apposition eyes, however,
this value is quite common, so we find in the xiphosuran Limulus,
active at night, an interommatidial angle of 8°; for Artemia,a
shallow water branchiopod, an interommatidial angle of 9°, and in
Cirolana, a deep sea isopod, an interommatidial angle of 15° (71).
Thus, an interommatidial angle of 10° is not uncommon in aquatic
arthropods. Due to the interommatidial angle, it is possible to
Fig. 3. H. kjerulfi (Linnarsson, 1871) (85) (Natural History Museum at the
University of Oslo, PMO 73168). (A) Head region of H. kjerulfi.(B) Left eye of
A.(C) Dense facets in B, hexagonally packed. (D) Lateral aspect of the head.
(Scale bars: Aand D, 1 cm; B, 2 mm; and C, 500 μm.)
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estimate the anatomical resolution, which can be defined as the
highest spatial frequency (of a sinusoidal grating) (ν
s
) that is
resolved by such an array of sampling stations (ommatidia): ν
s
=
1/2Δϕ [cycl/rad] (70, 7579), which allows a good comparison with
other investigated systems. The ν
s
results here to 2.87 [cycl/rad],
revealing an anatomical resolution lower than that of Limulus (4.8
[cycl/rad]) but higher than that of Cirolana (1.9 [cycl/rad]) (67).
So, in total, the system of the trilobite S. reetae is in a state
similar to modern aquatic arthropods, even without a lens.
Discussion
In discussion of these findings, it is remarkable that very little
lens structure can be clearly distinguished. There are indications
of round lens-like discs when the eye is studied from the outside,
but from the internal aspect, no convexities that could effectuate
any refraction of light can be made out. Also lens cylinders, such
as in xiphosurans of the genus Limulus (68), cannot be recog-
nized here. Even calcite as typical material for trilobite lenses,
with a high refractive index, may not have been effective enough
to refract light in water if there were not surfaces curved suffi-
ciently enough, forming a real convex lens.Differing from S.
reetae in aquatic crustaceans of today, the refractive element is
commonly built by a massive cellular crystalline cone, often with
an index gradient (70, 71). It is possible that at the time S. reetae
was living in this marine environment, the dioptric apparatus of
these early trilobites was, in some respects, relatively simple. If
the small triangular structure underneath the lens was indeed an
early type of crystalline cone, this might suggest, among other
things, a relationship of the trilobites with the Mandibulata,
because no crystalline cones can be observed in cheliceratae;
alternatively, it may have been an indication of convergent de-
velopment in this special case. The crystalline cone has been
considered to be a synapomorphy of either Mandibulata or
Pancrustacea (8084). To have any refractive power and focus-
ing, even in this ancient system, an index gradient then might be
assumed to have existed.
Different from typical modern apposition eyes, the sensory
apparatus lies in a kind of probably cellular basket. Inside of the
basket-like unit in S. reetae, the seven elements arranged like a
rosette around the central axis (Figs. 1 Gand Hand 2 AFand J)
clearly can be interpreted as relicts of former sensory cells,
grouped around a central fused rhabdom, underneath a small
crystalline cone; it is a typical ommatidium of a focal apposition
eye (70, 71) (Fig. 2 GJ). The arrangement of both systems
described is almost identical: The small differences in diameter
and the covering sheet may arise by diagenetic processes, or the
systems may be of different function but identical principle.
Unlike those of most modern compound eyes, the ommatidial
systems lie very isolated from each other, and pigment cells,
shielding the units against each other optically would not have
been necessary.
One hypothesis may suggest that the circular discs (lenses) had
only been more or less transparent parts of the cuticle, and that,
as explained, the rhabdom itself overtook all light-gathering
functions. This also may explain, why in most early Cambrian
trilobites, where the visual surfaces are preserved, no distinct
facets can be made out in their compound eyes. The very few
visual units of this compound eye (Fig. 1 Eand F), resulting in a
pixilated mode of vision, surely did not provide an image for-
mation but probably functioned as a movement detector dis-
covering objects passing by, but without any detailed impression
of the surroundings in its shallow water environments.
It may be mentioned that another trilobite, Holmia kjerulfi (Lin-
narsson, 1871) (85) from Norway, Botoman Formation, thus just less
than 2 My younger, already had established densely packed com-
pound eyes (Fig. 3), comparable to those of modern dragonflies.
In summary, the oldest compound eye so far known from the
fossil record, which is that of the trilobite S. reetae Bergstrom,
1973 (25), was a focal apposition eye. In its principal structure, it
was simpler than, but otherwise almost identical to, that of the
modern compound eyes of bees and dragonflies living today; thus,
the focal apposition eye is more than half a billion years old.
Materials and Methods
The holotype specimen of S. reetae Bergström, 1973 (25) is deposited at the
Institute of Geology at Tallinn University of Technology, Estonia, under re-
pository number GIT 294-1.
H. kjerulfi (Linnarsson, 1871) (85), described by Kiaer (86), from Tomten,
Ringsaker, Norway, is deposited in the Natural History Museum at the Uni-
versity of Oslo under repository number PMO-73168. The photographs were
taken with a Nikon D7000 camera and a Nikon AZ100 microscope.
ACKNOWLEDGMENTS. We thank Gennadi Baranov for kindly taking the pho-
tographs of S. reetae Bergström, 1973 (GIT 294-1-1) and its compound eye
described here, which made these analyses possible. We thank B. V. Meyer-
Rochow for allowing us to use the photograph in Fig. 2G, and his helpful
discussions. We also thank two anonymous referees, whose comments im-
mensely helped to improve the manuscript. We also thank Prof. N. Strausfeld
and Prof. D. Waloszek for giving us their expertise about the preservation of
the internal structures of the compound eye of this trilobite and its relevance.
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Supplementary resource (1)

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... The internal structure of compound eye units (ommatidia) in chelicerates and mandibulates differs, amongst other points, in that the Mandibulata possess a cellular crystalline cone below each lens. This character, which could inform the phylogenetic placement of trilobites, has recently been suggested to have been present in trilobites 5,7 . Scholtz and coworkers took up this point 6 , and claimed the existence of crystalline cones in two different species of trilobites. ...
... Firstly, however, to assess the relevance of this discussion about the existence of crystalline cones and their significance to trilobite phylogeny, it is necessary to understand how a trilobite compound eye, especially its dioptric apparatus, is constructed. Schoenemann et al. 5 showed that the most common type of trilobite compound eye, the holochroal eye, in principle is a socalled apposition eye, still common in many extant diurnal arthropods, and that this system is more than half a billion years old 5 . A compound eye typically consists of up to several tens, hundreds, or sometimes even thousands of identical units, the ommatidia. ...
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Lensless cameras are a class of imaging devices that shrink the physical dimensions to the very close vicinity of the image sensor by integrating flat optics and computational algorithms. Here we report a flat lensless camera with spatially-coded Voronoi-Fresnel phase, partly inspired by biological apposition compound eye, to achieve superior image quality. We propose a design principle of maximizing the information in optics to facilitate the computational reconstruction. By introducing a Fourier domain metric, Modulation Transfer Function volume (MTFv), we devise an optimization framework to guide the optimal design of the optical element. The resulting Voronoi-Fresnel phase features an irregular array of quasi-Centroidal Voronoi cells containing a base first-order Fresnel phase function. We demonstrate and verify the imaging performance with a prototype Voronoi-Fresnel lensless camera on a 1.6-megapixel image sensor in various illumination conditions. The proposed design could benefit the development of compact imaging systems working in extreme physical conditions.
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The arthropod compound eye represents one of two major eye types in the animal kingdom and has served as an essential experimental paradigm for defining fundamental mechanisms underlying sensory organ formation, function, and maintenance. One of the most distinguishing features of the compound eye is the highly regular array of lens facets that define individual eye (ommatidial) units. These lens facets are produced by a deeply conserved quartet of cuticle-secreting cells, called Semper cells (SCs). Also widely known as cone cells, SCs were originally identified for their secretion of the dioptric system, i.e. the corneal lens and underlying crystalline cones. Additionally, SCs are now known to execute a diversity of patterning and glial functions in compound eye development and maintenance. Here, we present an integrated account of our current knowledge of SC multifunctionality in the Drosophila compound eye, highlighting emerging gene regulatory modules that may drive the diverse roles for these cells. Drawing comparisons with other deeply conserved retinal glia in the vertebrate single lens eye, this discussion speaks to glial cell origins and opens new avenues for understanding sensory system support programs.
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Great progress has been made during the last decades in understanding visual systems of arthropods living today. Thus it seems worthwhile to review what is known about structure and function of the eyes of trilobites, the most important group of marine arthropods during the Paleozoic. There are three types of compound eyes in trilobites. The oldest and most abundant is the so-called holochroal eye. The sensory system represents a typical apposition eye, and all units are covered by one cornea in common. The so-called abathochroal eye (only in eodiscid trilobites) consists of small lenses, each individually covered by a thin cuticular cornea. The schizochroal eye is represented just in the suborder Phacopina, and probably is a highly specialized visual system. We discuss the calcitic character of trilobite lenses, the phylogenetic relevance of the existence of crystalline cones in trilobites, and consider adaptations of trilobite's compound eyes to different ecological constraints. The aim of this article is to give a resumé of what is known so far about trilobite vision, and to open perspectives to what still might be done.
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Burgess Shale-type fossil assemblages provide a unique record of animal life in the immediate aftermath of the so-called “Cambrian explosion.” While most soft-bodied faunas in the rock record were conserved by mineral replication of soft tissues, Burgess Shale-type preservation involved the conservation of whole assemblages of soft-bodied animals as primary carbonaceous remains, often preserved in extraordinary anatomical detail. Burgess Shale-type preservation resulted from a combination of influences operating at both local and global scales that acted to drastically slow microbial degradation in the early burial environment, resulting in incomplete decomposition and the conservation of soft-bodied animals, many of which are otherwise unknown from the fossil record. While Burgess Shale-type fossil assemblages are primarily restricted to early and middle Cambrian strata (Series 2–3), their anomalous preservation is a pervasive phenomenon that occurs widely in mudstone successions deposited on multiple paleocontinents. Herein, circumstances that led to the preservation of Burgess Shale-type fossils in Cambrian strata worldwide are reviewed. A three-tiered rank classification of the more than 50 Burgess Shale-type deposits now known is proposed and is used to consider the hierarchy of controls that regulated the operation of Burgess Shale-type preservation in space and time, ultimately determining the total number of preserved taxa and the fidelity of preservation in each deposit. While Burgess Shale-type preservation is a unique taphonomic mode that ultimately was regulated by the influence of global seawater chemistry upon the early diagenetic environment, physical depositional (biostratinomic) controls are shown to have been critical in determining the total number of taxa preserved in fossil assemblages, and hence, in regulating many of the important differences among Burgess Shale-type deposits.
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The morphology and early ontogeny of Agnostus pisiformis (Linnaeus 1757) is described on the basis of more than a hundred phosphatized, mostly enrolled specimens, etched from nodular limestones of the Upper Cambrian Agnostus pisiformis Zone, Västergötland, Sweden. Gradual, anameric development. with only slight morphological change suggests that most of the recognized structures can be generalized also for later developmental stages up to the adult. The tergal components, cephalic and pygidial shields and two pleurotergites, form a highly symmetrical test, with all rims fitting tightly together when clasped together edge to edge. Complete enclosure of the test may have protected the soft ventrai side, while Agnostus swam actively when the two shields were slightly gaping. Locomotion was effected by the strong exopodites of the second and third cephalic appendages. Most probably the environment in which A. pisiformis lived was a occulent zone at the bottom of the Alum Sea, where the animals swam or floated around, as is also suggested for the other orsten arthropods. Various morphological detaiis of agnostids are simply plesiomorphic, i.e. retained from the groundplan of the Arachnata. Those features which point to a affinitites with the polymerid trilobites are most clearly in the exoskeleton and in the ontogeny. The numerous modi cations of the morphology of A. pisiformis from the general polymcrid trilobite body plan and features hitherto unknown from trilobites and even other arthropods confirm the separate rank of the Agnostina within the Trilobita.
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The recently described radiodontan Lyrarapax unguispinus Cong et al., 2014 from the Chengjiang biota (Cambrian Series 2, Stage 3) highlighted a new morphological type of frontal appendage and unique mouth structures, a functional combination reinforcing the diversification of feeding strategies of radiodontans during the early Cambrian. Here we describe Lyrarapax trilobus n. sp. from the same fossil Konservat-Lagerstätte. The new species differs from L. unguispinus in the morphology and distribution of endites on the frontal appendage and the strengthening structure of the body flaps. The two species resemble each other in body shape (pattern of flap size), neck segment number, cephalic plates, and most importantly a mouth characterized by concentric wrinkled furrows. The latter confirms that a soft mouth without sclerotized plates is a real feature of Lyrarapax and supports the idea that oral structures provide valid diagnostic characters within Radiodonta.
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The early Cambrian Indian Springs biota of western Nevada, USA, exhibits Burgess Shale-type (BST) preservation of a diverse array of animal phyla, including the earliest definitive echinoderms. It therefore provides an important window on animal life during the Cambrian radiation. The objective of this study was to analyse the trace metal palaeoredox geochemistry and bioturbation levels of this BST deposit in order to characterize the palaeoenvironmental conditions in which these animals lived and their remains preserved. A total of 28 rock samples were collected from outcrops at three previously reported intervals of exceptional preservation at the Indian Springs locality, as well as from one interval not exhibiting such preservation. An additional 20 random samples were collected from talus for comparison. In the laboratory, the samples were analysed for trace metal palaeoredox indices (V/Cr and V/(V + Ni) ratios). Bioturbation levels were assessed through X-radiography and petrographic thin sections using the ichnofabric index (ii) method. Additional samples from coeval strata of the Poleta Formation in the White-Inyo Mountains, CA, that lack BST preservation were also analysed with the same methodology. Results indicate that oxic bottom water conditions dominated during deposition of these strata, despite consistently low bioturbation levels. This pattern holds for intervals with BST preservation and those without. Although ephemeral incursions of low-oxygen waters may have taken place, there is no evidence for persistent oxygen restriction in these palaeoenvironments. The low levels of bioturbation indicate limited mixed layer development and a redox boundary near the sediment–water interface, likely allowing post-burial BST preservation to occur even in this setting dominated by oxic bottom waters. Palaeoecological reconstructions and taphonomic hypotheses relating to the Indian Springs Lagerstätte must consider the palaeoredox conditions revealed in this study. With the dispensing of anoxic bottom waters as a requirement for BST preservation, other models proposing a role for clay minerals, the presence of hypersaline brines and the actions of Fe-reducing bacteria as mechanisms for exceptional preservation warrant renewed consideration.
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The Sirius Passet Lagerstätte (SP), Peary Land, North Greenland, occurs in black slates deposited at or just below storm wave base. It represents the earliest Cambrian microbial mat community with exceptional preservation, predating the Burgess Shale by 10 million years. Trilobites from the SP are preserved as complete, three-dimensional, concave hyporelief external moulds and convex epirelief casts. External moulds are shown to consist of a thin veneer of authigenic silica. The casts are formed from silicified cyanobacterial mat material. Silicification in both cases occurred shortly after death within benthic cyanobacterial mats. Pore waters were alkali, silica-saturated, high in ferric iron but low in oxygen and sulphate. Excess silica was likely derived from remobilized biogenic silica. The remarkable siliceous death mask preservation opens a new window on the environment and location of the Cambrian Explosion. This window closed with the appearance of abundant mat grazers later as the Cambrian Explosion intensified.
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Male and female individuals of the Baltic Sea, stalk‐inhabiting amphipod Dulichia porrecta posses eyes that differ in size and organization. Ommatidial numbers also vary, and in adult male and female specimens amount to approximately 80 and 90, respectively. Ommatidial diameters are larger in males (40–45) μm) than in females (approx. 30 μ.m). Externally, female eyes are covered with a dense pelt of approximately 3–4 μm long and 0.01–0.15 μm thick cuticular hairs, interspersed by up to 8 μm long, filament‐containing sensilla of unknown function. An identical structure occurs in males, but there it is less frequent. Eyes of male individuals also have considerably fewer and shorter (0.5 μm) cuticular hairs. Internally, the main difference is the somewhat broader (2.7 versus 2.4 μm) and longer (40–50 versus 32–40 μm) rhabdom in male animals and the significantly greater amount of screening pigment granules in the eyes of females. Anatomical features shared between males and females consist of bipartite crystalline cones, five equally‐contributing retinula cells and their rhabdomeres per ommatidium, a perirhabdomal space and two kinds of screening pigment granules. Ultrastructural derangements of rhabdom or microvilli following several hours of exposure to very bright spotlights are not apparent. The rhabdom length/width ratio for both male and female individuals is very high and, despite their essentially sedentary biology, allies D. porrecta most closely with pelagic amphipod species such as Hyperia and Phronima. It is concluded that from a sensory‐ecological viewpoint D. porrecta is a species that does not require vision for most of its vital functions, but that it does make use of vision in shallower water to evade predators. Males are likely to have more sensitive eyes than females, but those of the latter may posses greater resolution.
Book
Visual ecology is the study of how animals use visual systems to meet their ecological needs, how these systems have evolved, and how they are specialized for particular visual tasks. This book provides the first up-to-date synthesis of the field to appear in more than three decades. Featuring some 225 illustrations, including more than 140 in color, spread throughout the text, the book begins by discussing the basic properties of light and the optical environment. It then looks at how photoreceptors intercept light and convert it to usable biological signals, how the pigments and cells of vision vary among animals, and how the properties of these components affect a given receptor's sensitivity to light. The book goes on to examine how eyes and photoreceptors become specialized for an array of visual tasks, such as navigation, evading prey, mate choice, and communication. A timely and much-needed resource for students and researchers alike, the book also includes a glossary and a wealth of examples drawn from the full diversity of visual systems.
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The last two decades have seen the status of deposits containing soft bodied Cambrian fossils rise from geological curios into one of the foundations of modern thinking on early metazoan evolution and ecology. Some thirty of these soft bodied assemblages or Lagerstätten, resembling the Burgess Shale fauna are now known. One of these is the Lower Cambrian Emu Bay Shale fauna from Kangaroo Island, South Australia. The Emu Bay Shale has been mapped in two localities approx. 8 km (5 miles) apart on the northern coast of Kangaroo Island, at Emu Bay and at Big Gully. Previous investigations into the numerically abundant Lagerstätten fauna at Big Gully have highlighted its unusually pauperate diversity, with only some seven species described. The preservation is also unusual, comprising replacement by iron stained calcite. The fauna is confined to a 10 m thick basal siltstone. The age of the deposit is believed to be mid to upper Botomian and is thus marginally older than Early Cambrian soft bodied assemblages found on the North American continent and predating the better known Middle Cambrian Burgess Shale. In late 1991, a study of the Emu Bay Shale was undertaken to document the palaeontology and palaeoecology of the fauna. Preliminary findings, whilst increasing the number of species, confirm the pauperate diversity of the fauna. The new forms include several specimens of anomalocarid appendages. These not only represent the first occurrence of this form in Australia, but also the first occurrence outside the Burgess Shale of anomalocarid appendages with 11 segments, as compared with the more common and widespread 14 segment appendages. This connection may be important in the light of recent palaeoreconstructions which show the west coast of Canada and eastern Australia in close proximity during the early Cambrian. Also the spatial arrangement of the appendages indicates that anomalocarids may have shoaled and hunted in groups. They appear to have fed on the sea bottom, possibly using their appendages to probe the muddy bottom for shallowly buried prey as well as for capturing and transporting prey to the mouth. The assemblage appears to be dominated by the preservation of hard or permineralized body parts. However, abundant calcified ribbon-like structures concentrated on some bedding planes have yet to be classified. Several exceptionally preserved specimens of Myoscolex appear to have a series of metamerically repeated ‘paddle-like’ appendages, similar to some forms from the Burgess Shale, thus casting doubt on an annelid affinity. The assemblage appears representative of a deep water, low oxygen environment prone to periodic anoxia, possibly similar to the accretionary environment of the Burgess Shale. The Emu Bay Shale at Emu Bay exhibits a shelly assemblage, mostly comprised of disarticulated Hsuaspis exuvia with occasional small Redlichia exuvia and hyolithids. No calcite replacement is evident. The location represents current swept, probably shallow water environment.