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Disparate compound eyes of Cambrian radiodonts reveal their developmental growth mode and diverse visual ecology - Science Advances

Disparate compound eyes of Cambrian radiodonts reveal their developmental growth mode and diverse visual ecology - Science Advances

Disparate compound eyes of Cambrian radiodonts reveal their developmental growth mode and diverse visual ecology - Science Advances
Dec 02, 2020 8 mins, 31 secs

This ≤4-cm sessile eye has >13,000 lenses and a dorsally oriented acute zone.

canadensis has acute stalked eyes (>24,000 lenses each) adapted for hunting in well-lit waters, whereas the suspension-feeding ‘A.’ briggsi could detect plankton in dim down-welling light.

Although a pair of stalked eyes has been recognized in several different radiodont genera (1, 2, 4, 6, 10, 15, 16), only outlines were available until the preserved visual surface was revealed in Anomalocaris from the Emu Bay Shale (Cambrian Series 2, Stage 4) of South Australia (20).

Each stalked eye of Anomalocaris is pyriform, with a visual surface showing a huge number of ommatidial lenses arranged with the hexagonal packing typical of euarthropod compound eyes.

These isolated eyes were first described (21) as that of an unknown arthropod, its visual surface with more than 3000 ommatidia, including a field of enlarged lenses characterized as a “bright zone” (herein referred to as an “acute zone,” discussed below).

We argue that these acute zone–type eyes (21) are most likely those of ‘Anomalocaris’ briggsi, whereas the previously described Anomalocaris eyes (20) are likely those of Anomalocaris aff.

Morphological details of the acute zone–type eye suggest that these eyes are not stalked (as previously thought for all radiodonts) (22, 23) but are sessile and accommodated in the head by well-sclerotized cuticular structures.

The available material shows a considerable size range (Figs. 1 and 2, and table S1) (21), with the largest specimen having a preserved long-axis diameter of 30 mm, but its incompleteness makes this an underestimate of actual size (Fig. 2, A to D); comparing the position of the largest lenses to that of complete specimens showing a medial acute zone, we estimate a diameter of 38 mm (after sediment compaction).

The visual surface is thus entirely surrounded by other cuticular structures (the eye sclerite and marginal rim), indicating that the eyes are sessile and nonstalked, rather than having mobile eye stalks, as previously noted for some radiodonts (22).

The medial position of the acute zone—that is, the area displaying the largest lenses—is consistent with previously documented specimens (21), with lens diameters gradually decreasing to the margin of the visual surface.

New specimens show that especially small lenses are situated along most margins of the visual surface, except in the dorsal region (Figs. 1, A and D, and 2, A to D and G).

The entire visual surface exhibits a high degree of ordering of lenses into rows that confer dense hexagonal packing, although regularity is sometimes perturbed by rows coming into irregular contact at a few lenses, even in the acute zone, thus resulting in an imperfect hexagonal pattern in places (Fig. 1, B and C).

No single specimen shows a complete visual surface to enable a precise count of lenses, but across the available sample, the entire preserved surface is covered in lenses.

95 to 170 μm toward the edge of the visual surface, with some of the smallest preserved lenses at the extreme margin being c.

Notably, the biggest lenses in the Emu Bay Shale acute zone–type eyes (at 335 μm in diameter) far exceed those of any other Cambrian compound eye, apart from the Anomalocaris-type eyes from the Emu Bay Shale described below (21, 22, 24).

These eyes (Fig. 4) (20) are distinguished from those of acute zone–type eyes by their stalked, more elongate, pyriform shape, and much more consistent lens size across the visual surface.

These are larger than the lenses previously reported for SAM P45920 (ranging from c. 70 to 110 μm) (20), indicating that, like acute zone–type eyes, lens size increases throughout growth (Fig. 3B).

Extrapolating average lens counts from 12 separate 1-mm2 areas distributed across the surface of the better preserved of two eyes in SAM P45920a [figure 1d in (20)] yields an estimate of 24,760 lenses on the exposed side of the visual surface (Fig. 3A and table S2); it is likely that the complete three-dimensional visual surface hosted considerably more lenses.

In a similar-sized but incomplete specimen (SAM P52893; Fig. 4C), an estimated 16,250 lenses are preserved on the visual surface (table S2).

The largest Emu Bay Shale Tuzoia specimens with circular eyes preserved in situ show that these visual organs do not reach more than 9 mm in diameter (21, 26), and even the biggest Tuzoia carapaces from this deposit would not be able to accommodate acute zone–type eyes more than 3 cm in diameter.

Correspondingly, acute zone–type eyes represent 21 of the 34 identified eye specimens (~62%), outnumbering those of Anomalocaris type (~38%); as with frontal appendages, a single eye was counted as one specimen, even if preserved as one of a pair [e.g., figure 1a in (20)].

Thus, in terms of relative abundance, the more common acute zone–type eye most likely belongs to ‘A.’ briggsi.

Also, statistical tests for equality of proportions (table S6) between the frontal appendage and eye types suggest that this association is much more likely than the alternative possibility of the Anomalocaris-type eye belonging to ‘A.’ briggsi (and the acute zone–type eye to A. aff. canadensis).

Attribution of the acute zone–type eye to ‘A.’ briggsi thus partly follows from elimination and is congruous with phylogenetic analyses in which ‘A.’ briggsi is united with Tamisiocaris, rather than with Anomalocarididae (6–10).

canadensis and ‘A.’ briggsi in different parts of the radiodont tree and their classification in different families are compatible with their markedly different eyes.

The eye of ‘A.’ briggsi is argued above to be sessile and nonstalked, the visual surface encircled by the eye sclerite and the marginal rim.

As stalked radiodont eyes are situated laterally on the head, we infer the same for the sessile eye of ‘A.’ briggsi (Fig. 5, A and B).

(A and B) ‘A.’ briggsi showing sessile (nonstalked) eyes in lateral and anterior views, respectively, with the acute zone depicted by lighter shading; the dorsal head sclerite and oral cone are conjectural.

The eye sclerite of ‘A.’ briggsi is likely homologous with paired dorsolateral sclerites associated with the stalked eyes of other (nonhurdiid) radiodont taxa.

A dorsolateral position of the eye sclerite and the encircling of the visual surface by the marginal rim at the lateral sides of the head would constrain the acute zone to be oriented dorsally.

This inferred orientation of the eye differs from that hypothetically used to make an analogy to the eyes of robber flies, in which the acute zone is directed anteriorly [figure 1 in (21)].

In the acute zone–type eye of ‘A.’ briggsi, ordering of lenses into rows involves small marginal lenses grading into the enlarged lenses in the acute zone (Figs. 1, A and B, and 2, A to D).

Lenses in the acute zone of some of the biggest specimens are approximately twice as large as those known previously from eyes less than half their size.

Also, both the largest and smallest lenses are bigger in large eyes relative to small ones, suggesting that the small marginal lenses were the most recently added to the visual surface.

The acute zone–type eye of ‘A.’ briggsi is noted above to deviate from precise hexagonal packing of its ommatidia by sporadic irregularity in rows.

However, across the visual surface and especially in or near the acute zone, the hexagonal arrangement of neighboring ommatidia is more precise than observed in the xiphosuran Limulus polyphemus, which shows about one-third of all ommatidia as having more or fewer neighbors than predicted by a hexagonal model (30).

canadensis with more than 24,000 lenses is rivaled only by certain predatory insects such as dragonflies (Fig. 3A) (39, 40), and the enormous lens diameters of ‘A.’ briggsi (up to 335 μm) are matched only by select marine euarthropods, such as some phacopine trilobites (21, 41), Siluro-Devonian pterygotid eurypterids (35), and some modern deep-sea amphipod crustaceans (Fig. 3B) (42).

The previously documented eyes of ‘A.’ briggsi, although small, clearly show a distinct region of enlarged lenses that was originally interpreted as an anteriorly directed “bright zone”—an area of high visual acuity and light sensitivity (21).

In the compound eyes of some insects, such as male blowflies and hoverflies, the large lenses in the bright zone allow for increased light capture but maintain a similar spatial resolution compared with other parts of the visual surface (51, 52).

Because of the compressed and distorted visual surface, plus the absence of internal ommatidial structures in eye specimens of ‘A.’ briggsi, the degree of acuity and sensitivity cannot be determined, so we use the broader term “acute zone.”.

Reinterpretation of the ‘A.’ briggsi sessile eye (Fig. 5, A and B) as having a dorsally oriented acute zone with huge lenses has important implications regarding the habitat and visual capabilities of this species.

The visual ecology of hyperiids has been well studied (42, 55–57) and provides a useful analog for understanding the functional morphology of the ‘A.’ briggsi eye.

In general, as water depth increases and light becomes dimmer, bluer, and more vertically down-welling (i.e., progressively point-like) (58), the eyes become larger and bilobed, with the dorsal lobe having more numerous and enlarged lenses (forming an acute zone with a narrow visual field), resulting in enhanced resolution and photon capture (42, 57).

In Cystisoma, one of the largest and deepest-living hyperiids, only the dorsal lobes are present, with some of the largest individuals (body length, ca. 170 mm) having an enormous visual surface that covers the majority of the head (dorsal exsagittal length, up to 50 mm) and can have huge lenses (>400 μm in diameter) (Fig. 3B) (42, 56).

Notably, ‘A.’ briggsi is an inferred microphagous suspension feeder (7, 9), and so probably used its acute, light-sensitive eyes to detect mesoplanktonic organisms (up to 20 mm in size), especially large-scale swarms, at greater depths during the day and/or in the shallower waters during twilight hours.

However, similar-sized lenses across an extensive visual field indicate that the eyes were more attuned to operating in the scattered (nondirectional) and extended space light of shallower waters (58).

On acute zone–type eyes, acute, intermediate, and marginal zones were defined (each approximately one-third of the total visual surface, their boundaries being gradational), on which repeated counts along lens rows were carried out (133 to 440 lenses per specimen).

The obtained number of lenses per millimeter in each zone was squared and extrapolated to the total surface of that zone, and the three estimates were added to produce a total lens count for each eye.

On Anomalocaris-type eyes, rows of as many ommatidia as possible were counted on each visual surface (150 to 300 lenses per specimen) to obtain the number of lenses per millimeter, which was squared and extrapolated to the total preserved visual surface.

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