Over 250 species have been recorded from the Cambrian Series 2, Stage 3 Chengjiang biota of Yunnan Province, China, with Arthropods representing circa 33% of these species. These include taxa with soft anatomy preservation that are instrumental to elucidating early Euarthropod evolution. Among these, Arthropods with a grasping appendage, the so-called great or frontal appendages, are iconic animals of the Chengjiang biota.
In a paper published in the journal Palaeontologica Electonica, Robert O’Flynn and Denis Audo of the Yunnan Key Laboratory for Palaeobiology and International Joint Laboratory for Palaeobiology and Palaeoenvironment at Yunnan University, Mark Williams of the School of Geography, Geology and the Environment at the University of Leicester and the International Joint Laboratory for Palaeobiology and Palaeoenvironment at Yunnan University, Dayou Zhai, also of the Yunnan Key Laboratory for Palaeobiology and International Joint Laboratory for Palaeobiology and Palaeoenvironment at Yunnan University, and Hong Chen, again of the Yunnan Key Laboratory for Palaeobiology at Yunnan University, and Yu Liu, once again of the Yunnan Key Laboratory for Palaeobiology and International Joint Laboratory for Palaeobiology and Palaeoenvironment at Yunnan University, describe a new species of Euarthrapod from the Chengjiang Biota.
The new species is known only from a single specimen with a well-preserved dorsal exoskeleton that is divided into head, thorax, and pygidium, but is most notable for its long frontal appendages that resemble those of Radiodonts and the Euarthropod Kiisortoqia soperi. O'Flynn et al. discuss what happened to the ‘great appendage’ with reference to two possibilities for the evolution of the primary antennae or ‘great appendage’: (1) that limb-like ‘great appendages’ evolved to form chelicerae, i.e. innervated from the deutocerebrum; or (2) that the labrum represents the transformed frontal ‘great appendage’, i.e. innervated from the protocerebrum.
The new species is described from a single specimen recovered from the Yu’anshan Member pf the Chiungchussu Formation at Jiucun Town in Chengjiang County. The Yu’anshan Member is informally divided stratigraphically into four lithologically and palaeontologically distinctive parts. The specimen was recovered from the third stratigraphic interval of the Yu’anshan Member from laminated mudstones
of the early Cambrian (Series 2, Stage 3). It is deposited in the Yunnan Key Laboratory for Palaeobiology at Yunnan University, Kunming, as specimen number YKLP 11421.
The specimen was prepared mechanically with a mounted steel needle under a binocular microscope, where only a small amount of matrix was required to be removed by a gentle scraping action.
Fluorescence microscopy and photography (a Leica DFC7000 T linked to a Leica M205 FA fluorescence stereo microscope) were used to increase the contrast between the specimen (not autofluorescent) and the matrix (weakly autofluorescent). For photographs in natural colour, O'Flynn et al. captured several images with a Digital SLR Camera (a Canon EOS 5DS R and a Nikon D700) fitted with a 100 mm and a 105 mm macro lens, respectively, with extension rings for magnification factors above 1:1. The photographs were mostly captured in cross-polarised light to limit reflection of light and increase contrast. O'Flynn et al. also captured photographs with cropped light (light coming from a low vertical angle, highlighting structures at the surface) from various angles (default: from the top left) to reveal the micro relief of the fossil. The specimen was also investigated with Computed Tomography using a ZEISS Xradia 520 Versa, but no additional structures were revealed using this method.
Measurements were made on digital photographs using the image processing software ImageJ. Morphological characters measured include: (1) the total length, measured from the anterior margin of the head shield to the posterior termination of the tailspine; (2) the head, measured from the anterior margin to the posterior margin of the head shield; (3) tergites one through eight, measured from the anterior margin to the posterior margin of the tergite; (4) the frontal head limb, measured from the distal termination to the proximal margin of the podomeres; and (5) the pygidium, measured from the posterior margin of the posterior-most tergite to the posterior termination.
The new species is named Bushizheia yangi, where 'Bushizheia' derives from Bǔshízhě, the Mandarin for predator: an allusion to Kiisortoqia, from the Kalaallisut (Greenlandic) word kiisortoq, meaning predator, and 'yangi' honours Zhixin Yang, who recovered and prepared the fossil.
The genus Bushizheia is is ascribed to the total group Euarthropoda, as defined by the presence of fully Arthrodised bodies and limbs, because it has sclerotised trunk tergites, sclerotisation of post-antennal appendages, and does not have any isolated tergites in the cephalic segments.
It features a long, frontal grasping appendage that is morphologically like that of Radiodonts, but in combination with a completely Arthrodised body organisation; this distinguishes Bushizheia from all other Euarthropods, except Kiisortoqia.
Bushizheia and Kiisortoqia appear allied to each other by the possession of frontal ‘great appendage’-like head limbs. However, Bushizheia is sufficiently distinct to warrant erection of a monospecific genus. It differs from Kiisortoqia by: (1) Bushizheia has a large pygidium with paired short falcate spines and a terminal tailspine; Kiisortoqia has a small tail shield with neither spines nor a tailspine and twice the number of thoracic tergites; (2) trilobation of thoracic tergites effaced; (3) dorsal spine is present on each podomere of the frontal head limb.
Bushizheia yangi is a Euarthropod with a semi-circular head shield lacking dorsal compound eyes, eight thoracic tergites, and a large, semi-circular pygidium. Frontal head limbs circa 33% of body length, strong, composed of at least 12 podomeres, each with paired spines laterally.
Bushizheia yangi is circa 54 mm long. The habitus is sub-elliptical in dorsal aspect, with a length (anterior margin of the head shield to the posterior termination of the tailspine) of circa 250% of the width (maximum width in the anterior half of the body at the third and fourth tergites). The length of the head shield is circa 20% of the total length. The trunk tapers from the fourth tergite backwards to a large pygidium (the tail shield of the exoskeleton covering the fused posterior segments of the body). The pygidium’s margin is spinose.
The head shield is a simple, semi-circular shield, with smoothly rounded posterolateral margins, and the length is circa 70% of its width.
The trunk consists of eight tergites. The anteriormost three tergites are virtually of equal length; the length is circa 20% of the width. Tergites 3-4 are widest; the width and length of tergites subsequently decrease posteriorly in width and length. Axially, the posterior border of each tergite overhangs the following tergite by circa 17% of its length, but by less abaxially. The first, second, and third tergites are reflexed anteriorly, whereas tergites posterior to that are transverse or reflexed posteriorly. The tergopleurae of the first and second tergites terminate bluntly posterolaterally. The tergopleurae of tergites 3-8 are extended into posterolateral projections.
The pygidium is a semi-circular shield and its length is circa 70% of its width; the margins bear eight paired short falcate spines, which curve very slightly posteriorly. The pleural regions of the pygidium’s anterior-most segment are effaced, but a transverse furrow is visible axially. The tailspine is sub-triangular and incompletely articulated; it is as wide as long, circa 8% of the total length, and circa 30% of the total length of the pygidium.
The frontal head limbs reach a length of circa 33% of the total length of the body: 12 podomeres extend beyond the head shield, each with lateral endites that bear two inward facing setae, and terminal setae that are outward facing. Podomeres 2-7 are of equal length but decrease in width distally.
All visible post-frontal head limb appendages consist of either an endopod or an exopod. The one (incompletely) preserved endopod comprises four narrow podomeres. The two preserved exopods are paddle-shaped flaps, fringed with setae. Martin Stein in his description of Kiisortoqia soperi, identified four cephalic appendiferous segments (a head incorporating the antennular plus three post-antennular limb-bearing segments), considered to be part of the ground pattern of Euarthropoda. The distal exopod of the anteriormost post-frontal head limb appendage of Bushizheia yangi appears beneath the head shield, and may, based on its position, be the fourth cephalic appendage. The limb immediately posterior of this, adjacent to the first trunk tergite, appears to be the first trunk appendage.
Bushizheia yangi is dorsoventrally compressed and lies parallel to lamination; its well-articulated nature (i.e., tergites preserved attached, exopods preserved in situ). This state of preservation, especially the presence of articulated frontal head limbs, suggests limited post-mortem transportation: in, e.g. in extant Crustaceans, antennae can easily disarticulate. Compression wrinkles in the head shield that parallel its margin, suggest localised, weak sclerotisation. It is, therefore, presumed that the head shield was a simple, convex shield, sclerotised but without substantial biomineralisation.
As a result of the state of preservation, not all podomeres of the frontal appendages are accessible for a straightforward description. The exact number of podomeres cannot be established; some are obscured by sediment. Lateral endites can be confirmed for at least podomeres 2-7, 9, 11, 12, and medial endites bearing two firm setae at their tips can be confirmed for at least 4, 5, 7, 11, and 12. Rotation of podomere 2 evinces widely spaced double rows of endites.
Limbs with exopod setae are visible to the right of the two anterior-most thoracic tergites; the exopod of the posterior-most cephalic limb protrudes from beneath the head shield directly adjacent to the border of the head shield and first tergite, and is significantly rotated posteriorly, as is, albeit to a lesser extent the exopod of the first trunk limb. Only a single posteriorly situated endopod is, due to a degradation or complete absence of the overlying tergite, visible. No additional limbs were revealed by palaeontological techniques. The exact number of podomeres in the frontal appendages cannot be ascertained due to poor preservation of the distal-most ones. The proximal portions of the exopods are unavailable for description, so it cannot be established as to whether they were bipartite and divided into proximal and distal portions as in Leanchoilia illecebrosa.
Bushizheia yangi and Kiisortoqia soperi possess a long, grasping frontal appendage very similar to that of the Radiodonts. However, neither of these two species closely resemble Radiodonts. Could the presence of raptorial appendages in Bushizheia yangi and Kiisortoqia soperi be symplesiomorphic, shared by Bushizheia yangi and Kiisortoqia soperi, but also with Radiodonts linked earlier in the clade, to which Martin Stein alluded? Or are they an interesting case of convergence in organisms that are not closely related (not monophyletic), which independently evolved similar traits as a result of having to adapt to similar life habits?
It is beyond the scope of O'Flynn et al.'s study to attempt to solve the Arthropod head problem. Indeed, the preservation of Bushizheia yangi does not allow assessment of the neurological connection of the raptorial appendage. Hence, O'Flynn et al. only compare them to other appendages based on their morphology. Therefore, O'Flynn et al. explore the significance of the raptorial appendage of Bushizheia yangi and Kiisortoqia soperi in the context of some current interpretations of the homology of cephalic Arthropodan appendages; more precisely, the interpretation of the nature of the ‘great appendage’ of Radiodonts.
Many palaeontologists consider that the Radiodonts, and other ‘great appendage’ Arthropods belong to the lineage leading to Chelicerates, and the ‘great appendage’ is homologous to the chelicera. Following this line of reasoning, the presence of the ‘great appendage’ in Bushizheia yangi and Kiisortoqia soperi would, in this case, most likely be homologous to the ‘great appendage’ of radiodonts. The presence of this ‘great appendage’ would tie Bushizheia yangi and Kiisortoqia soperi, and ‘great appendage’ and ‘short-great appendage’ Arthropods together. More precisely, within this group, Bushizheia yangi and Kiisortoqia soperi and Radiodonts would be one of the sister groups of Chelicerates and ‘short-great appendage’ Arthropods. The problem being to reconcile the apparently primitive scarcity of sclerites displayed by Radiodonts with them being included in Euarthropoda, especially when considering that Bushizheia yangi and Kiisortoqia soperi are fully sclerotised. One solution to this problem would be to consider that Radiodonts subsequently lost part of their tergites, perhaps due to their nektobenthic life habits. The sclerotisation of Bushizheia yangi and Kiisortoqia soperi in this scenario would then represent a primitive trait.
Another, currently more widely held view, is that Radiodonts are not Euarthropods, but belong to a series of sister groups to Euarthropods (so called ‘Stem-Group’), which documents the progressive transition from weakly sclerotised, segmented Animals resembling Lobopodians to fully sclerotised Animals, the Euarthropods. However, the results of two important phylogenies supporting this theory were criticised in a 2011 study by Joachim Haug, Dieter Waloszek, Andreas Maas, Yu Liu, and Carolin Haug, due to apparent discrepancies in the coding of some characters and taxa. The debate on the nature of Radiodonts is not closed yet: several phylogenetic analyses published in the last decade support a ‘stem-group’ affinity for Radiodonts. In this scheme, Bushizheia yangi and Kiisortoqia soperi clearly belong to Euarthropods, and in this scenario the appendage similarity is either a convergence with the ‘great appendage’ of Radiodonts, or, the ‘great appendage’ was retained in early Euarthropods, and lost, or modified beyond recognition in most lineages of Euarthropods.
The convergence hypothesis agrees with the interpretation of Graham Budd, who considered the ‘great appendage’ to represent a pre-antennular appendage that was transformed into the labrum in the group including Euarthropods. If the hypothesis that the ‘great appendage’ was lost or reduced into the labrum is accepted, then the presence of ‘great appendage’-like frontal head limbs require convergence. Such convergence can be easily explained if Bushizheia yangi and Kiisortoqia soperi used their frontal head limbs in a fashion like predatory Radiodonts.
Contrary to this last hypothesis, the composition and morphology of the raptorial appendage of Bushizheia yangi bears a striking resemblance to the plesiomorphic state of the raptorial appendage within Radiodonts (i.e. the predatory, microphagous species). Other, probably distantly related species also have a seemingly similar raptorial appendage, e.g. the Bradoriid Kunmingella douvillei. This could give credence to the hypothesis that the great appendage was not reduced in a group including Euarthropods, but rather was lost or reduced in a group within Euarthropods.
In the case of Bushizheia yangi, since O'Flynn et al. do not have access to the ventral surface of the Animal, they cannot describe the position of the raptorial appendage. This prevents observation of the connection of this appendage to the head, and its exact nature. O'Flynn et al. can only hope that better preserved specimens may help to understand this animal better, and perhaps lead to a better understanding of the Arthropod head.
Despite its overall similarity to Kiisortoqia soperi and the morphological similarity of its appendages with those of the Radiodonts, the posterior of the animal is quite different. Disparity between Bushizheia yangi and Kiisortoqia soperi in this regard may well indicate that these are not closely related organisms. On a similar line of thought, similitude between Bushizheia yangi and Trilobitomorphs due to the presence of a pygidium could have been acquired by convergent evolution, an allusion to the conspicuous resemblance of the appendages of Aglaspidid-like Arthropods with those of the Nektaspid Naraoia spinosa. Alternatively, a plesiomorphic pygidium was retained in various Arthropod groups; such a scenario conflicts with several studies in which the presence of the pygidium is synapomorphic for a clade composed by Xandarellida, Nektaspida, Conciliterga, and Trilobita.
Artiopoda (e.g. Xandarellida, Nektaspida, Conciliterga and Trilobita) are arthropods with filiform antennulae. Bushizheia yangi is ipso facto outside Artiopoda, ergo the presence of the pygidium is not synapomorphic for a clade composed by the aforementioned groups. If the interpretation of a plesiomorphic pygidium is correct, this would indicate that this structure was retained in some Arthropod groups (e.g. Bushizheia yangi and Trilobitomorpha) but lost in many others.
A variety of Arthropods from the Chengjiang biota were most likely predators. The frontal head limbs of Bushizheia yangi are sturdy, predatory appendages, reminiscent of the ‘great appendage’ of Radiodonts. The presence of limbs posterior of these frontal head limbs that bear paddle-shaped exopods suitable for swimming could be indicative of a nektobenthic habit. No eyes could be found in the specimen. If the eyes in Bushizheia yangi were situated under the anterior border of the head shield, as in e.g. Leanchoilia illecebrosa, it is possible that they, together with the other ventral features of that area, were not preserved. The alternative hypothesis is that Bushizheia yangi was blind. Although visual perception in animals plays an important role in prey detection, other senses are used by animals in pinpointing their prey; the absence of eyes does not preclude Bushizheia yangi from being a predator. In the case where visual perception is lacking, Bushizheia yangi may have been an ambush predator, lying in wait, and catching unsuspecting prey with its anteroventral raptorial appendage.
Bushizheia yangi possesses a fully arthrodised body and limbs and consequently rests comfortably within the Euarthropoda. The present data neither confirms nor refutes any of the current interpretations of the homology of cephalic arthropodan appendages and although the phylogenetic position of Bushizheia yangi is difficult to resolve because few ventral structures are visible, the many Euarthropod plesiomorphies possessed by the taxon may indicate a basal position of the species, and it demonstrates the importance of fossils in characterising ground patterns.
The dorsoventrally flattened exoskeleton and paddle-shaped exopods that are suitable for swimming suggest a nektobenthic mode of life and Bushizheia yangi likely used its ‘great appendage’-like frontal head limbs for predation.
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