Fine-scale appendage structure of the Cambrian trilobitomorph Naraoia spinosa and its ontogenetic and ecological implications

Abstract

Trilobitomorphs are a species-rich Palaeozoic arthropod assemblage that unites trilobites with several other lineages that share similar appendage structure. Post-embryonic development of the exoskeleton is well documented for some trilobitomorphs, especially trilobites, but little is known of the ontogeny of their soft parts, limiting understanding of their autecology. Here, we document appendage structure of the Cambrian naraoiid trilobitomorph Naraoia spinosa by computed microtomography, resulting in three-dimensional reconstructions of appendages at both juvenile and adult stages. The adult has dense, strong spines on the protopods of post-antennal appendages, implying a predatory/scavenging behaviour. The absence of such gnathobasic structures, but instead tiny protopodal bristles and a number of endopodal setae, suggests a detritus-feeding strategy for the juvenile. Our data add strong morphological evidence for ecological niche shifting by Cambrian arthropods during their life cycles. A conserved number of appendages across the sampled developmental stages demonstrates that Naraoia ceased budding off new appendages by the mid-juvenile stage.

Keywords: Cambrian; Chengjiang biota; Naraoia spinosa; arthropod; gnathobase; micro-CT.

Figure 1.

Micro-CT images of a mid-stage juvenile specimen (YKLP 11408) of Naraoia spinosa Zhang & Hou (1985) from the Chengjiang Lagerstätte (Cambrian Series 2, Stage 3). (a) Ventral view of the animal. Green arrowheads indicate folds of arthrodial membrane proximal to the protopods of seventh and ninth appendages, respectively. Green dashed line shows position of posterior margin of head shield. (b) Right fourth appendage, posterior view. (c) Right fifth appendage, posterior view. (d) Right sixth appendage, posterior view. (e) Hypostomal complex and basal parts of first appendages (antennae), ventral view. (f) Enlargement of the area in the green rectangle in (b) but in ventral view. Green arrowheads indicate the two rows of bristles on protopod. (g) Enlargement of the area in the green rectangle of (d). Green arrowheads indicate endites at the sub-apical part of the endopodal podomeres. Note the seta on the endite of the fourth podomere. (h) Ninth appendages, ventral view. Green arrowheads indicate folds of arthrodial membrane proximal to the protopod (see also (a)). (i) Enlargement of the area in the green rectangle of (h). Green arrowheads indicate endopodal setae. (j) Part of left tenth appendage, oblique-ventral view. Green arrowheads indicate endopodal setae. Scale bars, 1 mm for (a), 500 µm for (b–e, h) and 200 µm for (f, g, i, j). ap, anterior plate of the hypostomal complex; an, the nth appendage; en, endopod; enx, endopod of xth appendage; exn, exopod of nth appendage; hs, head shield; ptn, protopod of nth appendage; s, seta; sp, spine; tc, terminal claw; ts, trunk shield; vp, ventral plate of the hypostomal complex. Numerals 1–6 indicate endopodal podomeres. (Online version in colour.)

Figure 2.

Micro-CT images of an adult specimen (YKLP 11409) of Naraoia spinosa from the Chengjiang Lagerstätte. (a) Ventral view of the animal. Green dashed line marks the position of the posterior margin of the head shield, blue dashed line for the anterior margin of the trunk shield. Green arrowheads indicate tiny spines on the posterior margin of the trunk shield. (b) Right second and third appendages, exopods not preserved. (c) Right ninth appendage, exopod not preserved. (d) Left tenth appendage. Green coloration highlights apical setae on endopodal podomeres 1–4. (e) Protopods of right second and third appendages, interior view (green rectangle in (b)). (f) Protopods of left second and third appendages, interior view (one of the green rectangles in (a), viewing from the back side). (g) Protopod of right ninth appendage (green rectangles in (c)) in posterior, interior and anterior views. Blue, red and yellow colorations highlight different rows of spines. (h) Protopod of left 14th appendage in ventral and posteroventral views. (i) Protopod of left 15th appendage in ventral and anteroventral views. (j) Hypostomal complex and basal parts of first appendages (antennae), ventral view. Scale bars, 5 mm for (a), 1 mm for (b–d, j) and 500 µm for (e–i). Abbreviations as in figure 1. Numerals 1–6 indicate endopodal podomeres. (Online version in colour.)

Figure 3.

Line drawings showing differentiation of the appendages of Naraoia spinosa and the difference between juvenile and adult. Left- hand upper: a detailed line drawing of N. spinosa, of early-adult stage of growth (ad.), based on YKLP 11409. Right- hand upper: a detailed line drawing of N. spinosa, of mid-juvenile stage of growth (juv.), based on YKLP 11408. The left-hand side of both the adult and juvenile specimens has been removed to better reveal the morphologies and arrangement of the appendages. The exopods on the left-hand side of both specimens, as well as the proximal-most portion of the left antenna, have also been removed to clearly display the in situ morphologies of the protopods. Morphology of posterior shield and gut morphology, within both the adult and the juvenile, based on fig. 20 of [3]. Right-hand centre: an enlarged line drawing of the hypostomal complex of N. spinosa based on both YKLP 11408 and 11409. General hypostome outline and positioning of frontal organs based on fig. 21 of [3]. Bottom of figure: detailed line drawings exhibiting the protopod morphologies of both mid juvenile (juv.) and early adult (ad.) specimens of N. spinosa based on YKLP 11408 and 11409. No. 1–10, numbered gut diverticula (main specimens) and numbered endopodal podomeres (dissected structures); ad., morphologies pertaining to adult specimens of N. spinosa; am, inferred presence of arthrodial membrane; an, the nth appendage; ap, anterior plate of the hypostomal complex; Ar, shield articulation; enx, the endopod of xth appendage; fo, the lateral frontal organs of the hypostome complex; gd, gut diverticula; gs, genal spine; gt, gut tract; hs, head shield; Hy., hypostome; juv., morphologies pertaining to juvenile specimens of N. spinosa; mfo, medial frontal organ of the hypostomal complex; pt, protopod; sp, spine; tc, terminal claw; ts, trunk shield; vp, ventral plate of the hypostomal complex. Numerals 1–6 indicate endopodal podomeres. (Online version in colour.)