Ontogeny and Dimorphism of Isoxys Auritus (Arthropoda) from the Early Cambrian Chengjiang Biota, South China

GR-01074; No of Pages 8 Gondwana Research xxx (2013) xxx–xxx

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Ontogeny and dimorphism of Isoxys auritus (Arthropoda) from the Early Cambrian Chengjiang biota, South China

Dongjing Fu a,b,c, Xingliang Zhang a,⁎, Graham E. Budd b, Wei Liu a, Xiaoyun Pan d a State Key Laboratory of Continental Dynamics, Early Life Institute and Department of Geology, Northwest University, Xian 710069, PR China b Department of Earth Sciences, Palaeobiology, Uppsala University, Villavägen 16, Uppsala SE-752 36, Sweden c State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, PR China d Coastal Ecosystems Research Station of the Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science, Fudan University, Shanghai 200433, PR China article info abstract

Article history: The morphology of Isoxys auritus Jiang, 1982 is reinterpreted in the light of abundant new specimens from the Received 31 August 2012 Early Cambrian Chengjiang biota, South China. I. auritus was a bivalved arthropod, its shield armed with two Received in revised form 23 May 2013 cardinal spines sub-equal in length. Two morphotypes (shield with and without ornamentation) which are of Accepted 2 June 2013 several original differences were interpreted as sexual dimorphs. 81 specimens examined here, which range Available online xxxx between 4.8 mm and 47.0 mm, represent a successive developmental sequence. The earliest stages were characterized by short cardinal spines, large spherical eyes, a pair of elongated antennulae, and seven pairs Keywords: Arthropoda of post-antennular appendages. The slim antennula is uniramous, consisting of nine articles, each armed Isoxys with short spines. It differs from that of great appendage and lacks any grasping function. During the Dimorphism ontogeny, the body length increases, accompanied by addition of trunk somites and appearance of primary Ontogeny reticulated ornaments, and both cardinal spines become evident. In the fully grown adult, there are up to Chengjiang biota 11 pairs of post-antennular appendages, equipped with the stout endopod composed of 6 or 7 podomeres lacking endites, and a terminal claw; the paddle shaped exopod is fringed with long setae along its posterior margin. Secondary reticulation of the shield has developed inside each primary one; the cardinal spines more elongated; and the ratio of length to height of shield increases. However, the size of eye and antennula relative to the body length signiﬁcantly decreases. Accordingly, intraspeciﬁc variation, including sexual dimorphs and developmental change, is evident in I. auritus. Recognizing such differences is important for detecting possible synonymies in the genus. Furthermore, the ontogenetic changes of I. auritus described here, particularly the postembryonic segment addition and possible allometric growth may also improve our understanding of development of Cambrian arthropods in Burgess-shale type preservation, especially those possessing such a large shield. © 2013 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.

1. Introduction (Williams et al., 1996; García-Bellido et al., 2009a). This distribution spans parts of the Redlichiid, Bigotinid and Olenellid trilobite realms A number of Cambrian Burgess Shale-type Lagerstätten, such as and is restricted to tropical/subtropical regions (Williams et al., the Chengjiang Lagerstätte, demonstrate a high diversity and disparity 1996). of animals in the Early Cambrian, recording the most magniﬁcent Species of Isoxys display considerable provincialism, such as Isoxys episode of “Cambrian explosion”. More than half of the living phyla auritus Jiang, 1982, and they have been considered to be pelagic ani- known from the record at this time, including a considerable number mals by some authors (Vannier et al., 2009). I. auritus was originally of arthropods which are by far the dominant group in Chengjiang erected as Cymbia auritus Jiang, 1982 on the basis of a single specimen biota, accounting for an average of 55.5% of species (Zhao et al., from the Lower Cambrian Helinpu Formation, eastern Yunnan, China, 2012). Isoxys Walcott, 1890 arthropod is an important element of and was synonymized with IsoxysbyConway Morris (1985). The the Early-Middle Cambrian marine fauna, characterized by a large animal is characterized by spines that are subequal in length and by “bivalved” shield and prominent cardinal spines. Paleogeographically a striking micro-ornamented shield (Jiang, 1982; Hou, 1987). Most is present on Laurentia (Canada, USA and Greenland), Siberia, of our knowledge of this species came from the contributions of Gondwana (Spain and Australia) and South China (Yunnan, Guizhou) Hou (1987) and Shu et al. (1995). Recently, I. auritus reached the top 5 most abundant arthropod species in the number of individuals ⁎ Corresponding author. Tel.: +86 29 88303200; fax: +86 2988363659. in Chengjiang Biota (Zhao et al., 2010), and specimens preserved E-mail address: [email protected] (X. Zhang). with much more information allow an expansion of our knowledge

Please cite this article as: Fu, D., et al., Ontogeny and dimorphism of Isoxys auritus (Arthropoda) from the Early Cambrian Chengjiang biota, South China, Gondwana Research (2013), http://dx.doi.org/10.1016/j.gr.2013.06.007 2 D. Fu et al. / Gondwana Research xxx (2013) xxx–xxx of this species. In this paper, we proposed a new interpretation of the ranges from 4.8 mm to 8.5 mm, of which five are approximately 5 mm carapace architecture of I. auritus, and refute the idea that the (Fig. 2A, C, I). Dorsal margin nearly straight, ventral outline semicircular, reticulated ornamentation is the only qualitative diagnostic character the maximum height being in the mid-length of shield. The valve L:H of shield. We also emphasize the differences between the frontal ap- ratio is an average of 1.51 (Fig. 2A, E, I). The antero- and postero-spine pendages among Isoxys species, in order to make sense of interpreta- short, subequal in length, varies from 5.9% of shield length in small tions of their significance at the species level. Furthermore, the work specimens to 14.6% of that in the larger one (Fig. 2; Table 1). Obliquely here is a first attempt to establish ontogenetic sequence in Isoxys, preserved specimens show that the two valves are not articulated with accompanied with supplementary description of the soft anatomy. a hinge in the dorsal side, but a weakly folded trace (Fig. 2H). Ventrally, doublure unrecognized or absent. 2. Material and methods 3.1.2. Eyes New material documented here was collected from eight localities of A pair of large spheroidal eyes projected forwards (Fig. 2A) and the Chengjiang biota, i.e. Chenggong, Chengjiang, Ercai, Erjie, Jianshan, slightly downwards (Fig. 2E). The spherical eye is, in this stage, the Ma'anshan, Shankou and Tanglipo (CG, CJ, EC, EJ, JS, MA, SK, TLP prefix) largest in relation to the body size (average diameter ca. 35% of in eastern Yunnan, China (Fig. 1). These localities occur in the middle body height and 22% of the body length) (Fig. 2; Table 1), and two part of the mudstone-dominated Yu'anshan Member of the Helinpu For- individual layers can be recognized (Fig. 2C, F, H). The light external mation (previously Qiongzhusi Formation), the Eoredlichia–Wutingaspis layer probably representing the cornea and the dark internal core is trilobite Zone of China, which is correlated to the upper Atdabanian better interpreted as remains of retinulae units (Fig. 2F). The eye (Zhangetal.,2001,2008) or the Lower Botoman of the Siberian Platform sphere is connected to the presumed head (ocular segment) with a (Paterson and Brock, 2007), both within the Series 2, Stage 3 of the new stalk, whose length is equal to, and its width is proximately one stratigraphic scheme for the Cambrian. Details of localities were given by fourth of the diameter of the eye (Fig. 2A, C, F). Zhang et al. (2007, fig. 12). All the studied specimens are housed in the Early Life Institute and Department of Geology, Northwest University 3.1.3. Antennula (NWU), Xi'an, China. Of these, 81 entire specimens can be measured The first appendage (antennula) is uniramous, and protruded and some specimens preserved with soft anatomy. Most specimens are beyond the anterior margin of the shield with a nearly straight preserved as partly flattened impressions on slabs of mudstone, showing posture. The largest antennula reaches a size equal to the shield various degrees of compaction. height (Fig. 2A, C), while the proximal part is, basically invisible in Specimens were prepared with fine needles under high magnifica- the cases which show no sign of significant postmortem displace- tion using stereomicroscopes. Fossils were photographed with a Canon ment, although it seems to be inserted into the head just posterior EOS 5D Mark II digital camera and images processed in Adobe Photoshop to the eye stalk (Fig. 2E, I). The antennula consists of nine articles CS 5. Camera lucida drawings were made using a Leica M80 microscope suggested by the median endites (Fig. 2A, E, G), each of which is and prepared with Corel Draw X5. The shield length was measured as drawn out medially into two short spines (Fig. 2G). Articles are the distance between the changes in slope at the base of cardinal spines. subequal in length and taper distally (Fig. 2G). The height is the maximum distance from the dorsal margin to the ventral margin. The method of statistical analysis follows Tanaka et al. 3.1.4. Post-antennular appendages (2009). Morphological terms used for the description of I. auritus follow 7 pairs of appendages behind the antennula occur in two larval Williams et al. (1996), Vannier and Chen (2000) and García-Bellido et al. individuals. Both are laterally compressed and show a complete set (2009b).Theterm‘shield’ is used to designate the exoskeleton that of appendages on the right side. These appendages, preserved as covers the soft body and has no phylogenetic implications. We used simple paddles and imbricated (Fig. 2A), elliptical in outline, slightly antennula to describe the most frontal appendage of I. auritus,since inclined to the sediment surface in a consistent way (Fig. 2C), are most they fail to show any typical features of short great appendage (see probably exopods, though no detail has been preserved. Note also that Discussion section below). the first post-antennula appendage is located very close to the antennula and no gap between them can be seen (Fig. 2C). Endopods 3. Morphological reinterpretation are unclear in the present material. A series of nodes along the trunk position here is tentatively interpreted as a set of mid-gut glands Two morphotypes are recognized in I. auritus, specimens with (Fig. 2H). reticulate pattern on shield referred to morph A (e.g. Fig. 3A, C, E, K) and those without ornaments referred to morph B (e.g. Fig. 3B, D, F, 3.2. Pre-adults H). The ontogeny of I. auritus described here has been broadly divided into three series, approximately corresponding to the larvae, Specimens more than 10 mm, two morphotypes are evident: pre-adults and adults, based on characters of both shield and soft morph A with densely primary-reticulated ornaments, honeycombed anatomy. It seems unlikely that the development of I. auritus can be structure with 3-D aspect of the wall (Fig. 3K) and morph B with described exactly by following the maturation of every feature. The smooth shield (Fig. 3L). The former shows a wider 3-D preserved method of subdivision into more instar stages is more or less doublure (Fig. 4A), while that of the latter is quite narrow (Fig. 4B). arbitrary, since the gap between any two adjacent growth stages in dis- The valve L:H ratio is 2.09 in morph A with the antero-spine 15.2% persal analysis is undetectable (Fig. 5). However, this simplification of shield length, and 2.05 in morph B. For further comparisons makes an easy and efficient method to unravel the major developmental between two morphs see following description of adults. changes in carapace morphology and internal anatomy during ontogeny. On this basis, I. auritus is described following its developmental 3.3. Adults sequence. 3.3.1. Shield 3.1. Larvae The differences between the two morphotypes (ornamented morph A and smooth morph B) are more evident in the adult: 3.1.1. Shield 1) the marginal rim of morph A is wider (ca. 10% of shield height) Six small specimens were examined for this stage. No micro- and three dimensional preserved (Figs. 3A, C, G and 6A, B). In con- ornaments occur on the external surface of the shield. The length of shield trast, it is narrow in morph B (Fig. 3B, D); 2). The anterodorsal furrow

Fig. 1. Simplified geological sketch map of east central Yunnan Province, southwestern China, showing the outcrops of Early Cambrian strata and collecting localities. on the valve of morph A (Fig. 3C, E, G) is unclear in that of morph B; (primary ornamentation) which is ca. 300 μm across (Fig. 3I, J). The 3) the greatest valve height in morph A is generally behind the boundary of each primary hexagon is convex, while that of the mid-length (weakly postplete) (Figs. 3A, C, G and 6A), while the secondary hexagon is concave (Fig. 3J). valve is highest around its mid-length (amplete) in morph B (Fig. 3B, D, F, H); 4) wrinkles are common along ventral margin of 3.3.2. Soft anatomy valve in morph B (Fig. 3B, F, H), presumably where convexity was at The antennulae are slim and rod-shaped. They protruded from the a maximum, suggested a relatively thin and flimsy shield. In addition, anterior margin of shield, extending anteroventrally without curvature. morph A is dominant in number in different localities. The proximal part inserted into the post-ocular segment (Fig. 6A). The anterior spine increases to ca. 30.1% of shield length in both Post-antennular appendages biramous, up to 11 pairs and evenly morphs (e.g. Figs. 3B, C and 5A). The dorsal margin of the shield is spaced (Fig. 6A, B). Details of endopod exposed, especially evident in truly articulated. Two valves, including the spines, articulated along the fourth and fifth appendages. Each endopod consists of six (or possi- a hinge line and could fully separate from each other (Fig. 3G, H). ble seven) podomeres, without any outgrowth like endite or setae Measurements documented between two morphs: the valve length/ (Fig. 6E). Articular membranes developed. Podomeres subequal in height ration of morph A is slightly larger than that of morph B. In length, taper distally without a claw (Fig. 6E). Marginal setae of exopod morph A, length ranges from 10.1 mm to 47 mm, height between present: for detailed description reference should be made to the 4.9 mm and 20 mm. The valve L:H ratio is an average of 2.28, and previous work of Shu et al. (1995). with a good fit(R2 = 0.906, Fig. 5). In morph B, length among 9.6 mm to 46 mm, and height 4.8 mm to 21 mm. Average L:H ratio 4. Discussion is 2.20 (R2 = 0.971, Fig. 5). We analyzed the ontogenetic relationship between valve length and valve height in two morphotypes. The 4.1. Ontogeny and dimorphism results showed isometrical growth in two morphotypes at the confi- dence level of 95% (R2 = 0.928, P b 0.001, b = 1.047). The slopes of Ontogenetic information for fossil arthropods in the Cambrian is the reduced major axis were not significantly discriminated (P = largely restricted to arthropods in an ‘Orsten’-type of preservation 2 0.548, R = 0.937, F1, 70 = 0.364). (Walossek, 1993; Haug et al., 2010; Zhang et al., 2012). Our knowledge In morph A, secondary reticulated ornaments formed by approxi- of other arthropods with Burgess-shale type preservation mostly comes mately 30 adjacent hexagons developed inside of each bigger hexagon from data for trilobites obtained from dorsal hard parts only (Hughes et

Fig. 2. Juvenile individuals of Isoxys auritus Jiang, 1982 from the Lower Cambrian Chengjiang biota, South China. A, The smallest specimen with complete carapace, eyes, antenna slender and long, with nine podomeres and setae, seven pairs of post-antennula appendages, EJ0416; C, the smallest specimen, showing the big eyes, antennula and the following seven pairs of appendages, EJ 0415; B, D, explanatory drawings of A and C; E, note the long antennula, JS149; F, details of the eye in C, showing the eye stalk and the eye sphere with outside layer and inside unite; G, details of the antennula of E, nine podomeres and each with a medium seta; H, the smallest specimen in oblique dorsal view, note the carapace dorsal line, no articulated hinge, except for a weakly fold trace, JS0003; I, the smallest specimen with complete carapace, possible mid-gut glands and adductor muscle, EJ0414; J, Isoxys curvirostratus, showing the great appendage. Abbreviations: am?, possible adductor muscle; an, antennula; co, cornea; es, eye stalk; ey, eye; ex, exopod; f1–9, podomeres of the antennula from the distal to proximal; lv, left valve; mg?, possible mid-gut gland; pf, proximal part of the antennula; ru, retinular units; rv, right valve; se, setae.

Table 1 al., 2008). Recently, some ontogeny information of other taxa was given, Morphological characters in different growing stages of Isoxys auritus Jiang, 1982 the Lower Cambrian Chengjiang biota, South China. especially the developmental changes of the great appendage by Haug et al. (2012). The new observation here based on large number of spec- Character Stage imens with various sizes document ontogenetic changes of shield and Larvae Pre-adults Adults soft parts of bivalve arthropod I. auritus. L/H 1.51 2.07 2.24 Individuals with length less than 5 mm have usually been consid- S/L (%) 5.9 15.2 30.1 ered to be very early juveniles (see Vannier and Chen, 2000, fig. 3E; E/L (%) 35 ? 8.9 Hu et al., 2007, fig. 1D; Vannier et al., 2009, fig. 3i), although the b AP (pair) 7 11 11 earliest larval stage is unknown. This stage is characterized by the OR no pr pr + sr DL fo ? ar short cardinal spines, large eye spheres, elongated antennulae and seven pairs of following appendages. No difference of shield between Abbreviations: L, carapace length; H, carapace height; S, cardinal spine length; E, the two morphs, including any micro-ornament, is discernible in this diameter of eye sphere; AP, post-antennal appendages; OR, ornament pattern; no, none ornaments; pr, primary ornaments; sr, secondary ornaments; DL, dorsal line; fo, stage. The similarity of the shield also supports a close relationship, carapace fold dorsally; ar, two valves articulated dorsally. though they are easy to distinguish from one another later.

Fig. 3. The morphological features of carapace in pre-adults (K–L) and adults (A–J). the left columns A, C, E, G, I–K, morph A, the carapace with the reticulate pattern and wide 3-D preserved doublure; the right column B, D, F, H, L, morph B, smooth carapace without ornaments outside, doublure narrow. A, B, both specimens from Maanshan section, showing carapaces of morph A and morph B, respectively, MA015 and MA042; C, D, both specimens from Chenggong section, representing carapaces of morph A and morph B, CG063 and CG069; E, F, specimens in dorsal view, note the dorsal hinge line of carapace in both morphs, two valves were separated including the antero- and postero-spine along hinge line, MA043 and CG071; G, individual of morph A, two valves specially the cardinal spines apart from each other along the dorsal hinge line, NWUS 91-309A; H, carapace of morph B with disarticulated valves, the upper one is left valve (lv) and the lower is right valve (rv), SK228; I, J, details of carapace outsides in adults in A, showing primary reticulate pattern in honeycombed (I) and secondary reticulate pattern formed by adjacent hexagons (J); K, L, pre-adults in morph A and morph B, respectively. Carapace of morph A developed with primary reticulate pattern and wide doublure (K), morph A smooth, doublure quite narrow (L), CG062 and MA006. Abbreviations: as, anterior spine; fu, anterodorsal furrow on the valve; hl, dorsal hinge line; pr, primary reticulate pattern of carapace; sr, secondary reticulate pattern of carapace.

Subsequently, the body length increases with addition of succes- dimorphism characterizes the bivalved carapace of numerous genera sive trunk somites and the length of both cardinal spines changes of ostracodes and also some crustaceans (Vonk and Nijman, 2006; faster. For the relatively advanced juveniles (pre-adults), spines are Zhang, 2007; Namiotko and Martins, 2008). We believe that the two more evident than in the case of the early stage. In this stage, morphs of I. auritus represent sexual dimorphism differing in morph A is easily distinguished from morph B in its primary reticulate micro-ornamentation of the shield rather than separate species, in ornamentation and a wider marginal doublure (Fig. 4). A reticulated spite of lacking soft-part evidence in morph B specimens. However, carapace was recognized as a fundamental diagnosis for I. auritus in the two morphs are similar in outline, being hardly distinguishable previous work. Any cases without this ornament, though common, from each other in early juvenile stages. The statistical analysis also have been attributed to the poor preservation (Hou, 1987; Shu et showed that the two morphs were not signiﬁcantly discriminated. al., 1995; García-Bellido et al., 2009b). However, the re-examination Furthermore, morph A is always dominant in number among differ- here based on both morphological comparison documents the validi- ent localities, i.e. with a consistent sex ratio. Therefore, we propose ty of morph B, which means the absence of ornaments is by no means the two coexisting morphs representing of sexual dimorphism. a preservational artifact. Fully grown adult are distinguished from juveniles by the qualita- The most common cause of two distinct morphs in a species is tive stability of morphological features, i.e. 11 pairs of trunk append- sexual dimorphism, usually differing in characteristics such as size, ages; and the shield displays delicate secondary reticulation, so that shape and ornamentation (Anderson, 1994). Well-developed sexual changes become restricted to mere growth in size. In addition, adults

trend (Table 1; Fig. 7). Therefore, both positive and negative allometric growths may be present in this case (Table 1).

4.2. Taxonomic implications

Intraspecific variation is evident in at least some of Isoxys species, associated with sexual dimorphs or developmental changes. Accord- ingly, recognizing such differences is important for detecting possible synonymies, especially those that were mainly concerned with the evidence of simple exoskeletons. For example, Isoxys communis Glaessner, 1979 and Isoxys glaessneri García-Bellido et al., 2009a are coexisting species from Emu Bay Shale, with the latter being recognized as a new one on the basis of its small size (García-Bellido et al., 2009a). It is more likely, however, that I. glaessneri represents individuals in early developmental stages of I. communis, when allometric growth is common for Isoxys. This view is also supported by the results of Megacheira, as some of the different species described Fig. 4. Morphological comparison between the carapaces of two morphs in the pre- might, in fact, represent different growth stages of a single species adults, Isoxys auritus Jiang, 1982 the Lower Cambrian Chengjiang biota, South China. Both carapaces bear spines in medium length and ratio of length to height lower (Haug et al., 2012). It would be more confused still if the sexual size than that of the adults. A, morph A, carapace with primary reticulated ornaments dimorphs (SSD, with males and females showing differences in size) and wider doublure; B, morph B, carapace smooth, narrow doublure, the valve is and morphologically differing juveniles are partially coupled. This, highest around its mid-length (amplete). again, diminishes the diagnostic importance of the shield configura- tion without setting up a successive growth sequence and examining any possible dimorphism of Isoxys species. have a higher ratio of length to height and more elongated spines. The length/height ratio of the shield increases with size, and the same ap- plies to the spines in both morphs, though allometry is not evident in 4.3. Antennula of I. auritus is not a grasping great appendage ontogenetic relation analysis. However, the reverse is also true for other organs, i.e. the dimension of eyes and the length of frontal New evidences reported here indicate that anteromost appendage antennula relative to the body size show a significant decreasing of I. auritus can be best interpreted as antennula, as it lacks of any typical features of the great appendage. There are two types of ‘great appendage’, a long one with about 15 short articles (e.g. anomalocaridids) and the short one consisting of a bipartite peduncle and a distal claw-like part (Chen et al., 2004; Liu et al., 2007; Stein, 2010). The key feature of the latter is the elbow joint (as termed by Whittington, 1974), an arthrodial membrane that connects the claw element to the basal part (peduncle), e.g. the structure of great appendage in Occacaris Hou, 1999, Yohoia Walcott, 1912 and Leanchoilia Walcott, 1912. This joint allows for a backward jack-knifing of the claw against the peduncle, i.e. the great appendage can be retracted to bring prey into the vicinity of the mouth. Further- more, the claw can be flexed against the peduncle, which results in the spines being positioned further towards the body (Haug et al., 2012). Alternatively, great appendages can curve dorsally through strongly bending/extending the ample membranes between each spiny articles, so as to catch the prey and bring it to lie close to the mouth, such as in the great appendage of Anomalocaris and the three species of Isoxys known to bear great appendages, Isoxys curvirostratus Vannier and Chen, 2000 (Fig. 2J; Fu et al., 2011), I. communis Glaessner, 1979 (García-Bellido et al., 2009a) and Isoxys acutangulus Walcott, 1908 (García-Bellido et al., 2009b) from Chengjiang, Emu Bay Shale and Burgess Shale, respectively. Either mechanism is a crucial requirement for performing a raptorial function as well as to bring food to the mouth. However, neither elbow joint nor developed article membranes are evident in the antennula of I. auritus, making a strong curve im- possible. In fact, it is always in a straight posture (Fig. 2A, C, E, G), elongated and slender, and also lacks specialized equipment for grasping motion, such as a claw (Fig. 2A, E, G). Therefore, a grasping mechanism as seen in great appendage arthropods, and even some Isoxys species, cannot be assumed for I. auritus, at least not based on Fig. 5. Size distribution of morph A and morph B of Isoxys auritus Jiang, 1982 the Lower the observed morphology. Similarly, the slender antennula of Isoxys Cambrian Chengjiang biota, South China. All 81 specimens collected from eight locali- volucris Williams et al., 1996 with seven articles is also not a raptorial ties (CG, CJ, EC, EJ, JS, MA, SK, and TLP) in eastern Yunnan. Morph A = specimens great appendage (Stein et al., 2010). For further comparisons within with reticulate pattern on carapace; morph B = specimens with smooth carapace; un = juvenile specimens without any recognized ornaments on carapace outsides; the genus Isoxys, such as the shield and trunk appendages see Fu et n = number of measured specimens. al. (2011).

Fig. 6. Soft anatomy of the adults. A, Complete specimen in lateral view, showing the outline of carapace, eye, antennula and the following 11 pairs of biramous appendages, the exopodite with long setae, JS0013; B, the counterpart of JS0013, showing the wide 3-D preserved doublure and trunk appendages; C, D, explanatory drawings of A and B, respectively; E, detail view of the fourth pair of endopods in B, consisting of six or seven podomeres, the joint membranes clear, and neither endites nor distal claw occur. Abbreviations: en, endopod; p1–7, podomeres of endopod from the distal to proximal; 1–11, numbered trunk appendage (1 is the appendage immediately behind the antennula).

5. Conclusions trunk biramous appendages cast doubt on the current taxonomy. In our forthcoming research, the relationships of species in Isoxys Morphological evidence of new specimens of I. auritus in a and their phylogenetic position within Cambrian arthropods will developmental sequence indicates that: be investigated by cladistic analysis.

1. A new morphotype with smooth shield was recognized in our collections from different localities. It differs from the previous Acknowledgments morphotype (shield with reticulated ornament) in several distinc- tive characters. We believe that the two morphs represent the We are grateful to many staffs at the Early Life Institute for joining sexual dimorphs of one species, since they are coexisting, have a in the fieldwork and technical assistance. Thanks also are given to consistent sex ratio in the number of individual and are very sim- Martin Stein (Copenhagen) for the suggestions on the manuscript. ilar in outline, even being hardly distinguishable from each other This work is financed by the Natural Science Foundation of China in earlier developmental stages. (Grants 41272019, 41202007 and 40830208), the Major Basic 2. As mentioned above, the morphology of I. auritus changes through- Research Project of the Ministry of Science and Technology of China out the ontogeny. Postembryonic segment addition (from 7 to 11) (Grant: 2013CB806400), 973 Project of the Ministry of Science and as well as possibly positive and negative allometric growths were Technology of China (Grant: 2013CB837100), State Key Laboratory recognized. Intraspecific variation, including differences of develop- of Palaeobiology and Stratigraphy (Nanjing Institute of Geology mental stages and sexual dimorphs necessitate a re-investigation of and Palaeontology, CAS) (No. 123113) and by the Swedish Research the other Isoxys specimens, as some of the different species Council (VR) to GEB. described might represent different growth stages of a single species. In addition, ontogenetic information of Cambrian arthropods References in Burgess-shale type preservation, especially concerning with soft parts is rare. New observations of ontogeny in I. auritus here must Anderson, M., 1994. Sexual Selection. Princeton University Press, Princeton. Chen, J., Waloszek, D., Maas, A., 2004. A new ‘great-appendage’ arthropod from the help us to understand other potentially related arthropod taxa, Lower Cambrian of China and homology of chelicerate chelicerae and raptorial especially those with a large shield. antero-ventral appendages. Lethaia 15, 3–20. fi 3. According to our investigations, the morphology of the antennula Conway Morris, S., 1985. Cambrian Lagerstatten: their distribution and signi cance. Proceedings of the Royal Society B 311, 49–65. in I. auritus differs from that of the great appendage found in Fu, D.J., Zhang, X.L., Shu, D.G., 2011. Soft anatomy of the Early Cambrian arthropod other Isoxys species, which indicates a sensory function possibly Isoxys curvirostratus from the Chengjiang biota of South China with a discussion associated with feeding, but not grasping. The diversity in feeding on the origination of great appendages. Acta Palaeontologica Polonica 56, 843–852. 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