Is Nectocaris pteryx a cephalopod?
The Cephalopoda is one of the most successful molluscan groups. Today, in recess, they are largely represented by Coleoidea (Belemnoidea being the most important fossil subgroup); earlier ammonoids (in the Mesozoic) and nautiloids (in the Palaeozoic) formed the dominant element of nekton. The roots of cephalopods reach the Cambrian, but the phylogenetic and anatomical nature of their first appearance is largely unsolved, which is puzzling as they were preceded in time by the emergence of other major classes of molluscs and most other phyla by the end of Early Cambrian. Therefore, solving the cephalopod ancestry by indicating the most ancient relative of the group, with all certainty, may be one of the most crucial tasks in palaeobiology.
Recently, Smith & Caron (2010) argued that the Middle Cambrian fossil Nectocaris pteryx, previously interpreted either as an arthropod (Conway Morris 1976) or as a chordate (Simonetta 1988), represents the oldest cephalopod relative. Smith & Caron (2010) established their new interpretation on the basis of a great amount of exquisite material at hand, namely complete, soft-bodied specimens of Nectocaris from the famous Middle Cambrian Burgess Shale. Worth noting is that previously the species was known from one specimen only. Despite having many new and exceptionally well-preserved specimens, Smith & Caron (2010) failed not only to show the evidence for the animal to be a mollusc, but also to place it within the currently understood scheme of evolutionary events. We are all aware that extraordinary hypotheses need extraordinary evidence. Here, we point out important issues that significantly weaken, not to say completely undermine, Smith & Caron’s interpretation.
What does Nectocaris need to be called a cephalopod?
The oldest currently known true cephalopods are those of the genus Plectronoceras from the Upper Cambrian, much younger than Nectocaris. They had millimetric shells with a siphuncle and a small number of septa. Such diaphragms exist in a number of groups (not only molluscan). What makes cephalopod a cephalopod is its siphuncle, which could have originated at the extension of the pelagic life style from larvae to adults (Dzik 1981). ‘Monoplacophorans’ such as Hypseloconus were once thought to be ancestral to Plectronoceras by many workers (Yochelson et al. 1973; Peel 1991), but these should probably be better classified as brachiopods (Dzik 2010), with real ancestors somewhere close to ‘hyoliths’ such as Turcutheca (Dzik 2010).
Being much older, the ‘Kraken’Nectocaris does not have either a phragmocone or a shell. Could it be, that the cephalopod shell is not homologous to other molluscan shells, or may be it is a case of secondary loss in Nectocaris– an early, and surprisingly complete? Highly unlikely, given the micro-structural, genetic and ontogenetic unity, as well as the known common ancestry of that element. It is well known that the internal shell in coleoid cephalopods is a derived feature and during their evolution, it became completely reduced, as in recent Octopoda. However, it must be taken into account that the shell reduction in a most advanced cephalopod group such as the octopods occurred late during its evolutionary history (e.g. Boyle & Rodhouse 2005), as easily fossilized octopod shells are known from the Cretaceous (Fuchs et al. 2009). What’s more, the radula, a synapomorphic trait of a really high value, is absent too. Although the radula is lacking in bivalves and some aplacophorans, it is present in the rest of the molluscs including the cephalopods, with only Spirula having its radula absent or vestigial. However, a vestigial or totally reduced radula is believed to result from a secondary reduction (Warnke & Keupp 2005). Therefore, it is highly unlikely that the radula would be totally reduced in ‘early cephalopods’ such as Nectocaris. There is also no reason why it should not fossilized or being unnoticed in the material comprising nearly a hundred of specimens investigated, especially while soft tissues have been preserved. Moreover, molluscan radula are known to have been preserved in older, Lower Cambrian deposits (Butterfield 2008), and the oldest of cephalopod radulas are known to be preserved in Upper Ordovician (Gabbott 1999) and Late Silurian (see Mehl 1984) orthoconic nautiloids.
It appears then that two most important molluscan features (present in all cephalopods) are absent. The same applies to jaws (beaks), widely known in both Palaeozoic ammonoids (e.g. Tanabe & Mapes 1995) and Mesozoic coleoids (e.g. Klug et al. 2009), but which are not present in the putative ‘cephalopod’Nectocaris at all. The lack of beak and the presence of only one pair of frontal tentacle-like appendages seem to be completely incompatible with respect to cephalopod feeding behaviour, which rely on capturing the prey with tentacles, delivering it to the mouth and biting it with the beak (e.g. Hanlon & Messenger 2003; Boyle & Rodhouse 2005). Thus, the prey capturing by Nectocaris using its ‘tentacles’ must have been very inefficient, if not to say impossible, and in spite of the lack of jaw apparatus, its feeding behaviour seemed to be completely different (see below).
Similarities in gill and fin location and structure could well be convergent with any group, and is not considered specific here. The funnel is common to all cephalopods, but the one in Nectocaris is truly evident only in the artistic reconstruction (see Bengtson 2010). To work as a funnel properly, it should not get wider distally, as it does in Nectocaris. Rather, the funnel should have a small cross sectional area, as in Recent cephalopods. Only then, the jet has a considerable force and propels the animal in opposite direction (e.g. Boyle & Rodhouse 2005). The distally widening ‘funnel’ of Nectocaris suggests that this structure evolved for completely different purpose than for jet-propelled movements. Because of the poor preservation of the putative mouthparts in Nectocaris (Smith & Caron 2010), the ‘funnel’ most likely represents a specialized feeding apparatus. Its morphology suggests that it served as ‘probing’ device with a true mouth located most distally, for catching food, probably in the form of small animals. Interesting is the fact that a quite similar structure – in a general outline and orientation – a proboscis feeding apparatus, occurs in pycnogonid marine arthropods, and in its advanced form is known already from the Silurian (see Siveter et al. 2004).
Nectocaris also lacks another characteristic feature of cephalopods, namely the ink sac. The ink sac is known to be preserved in fossil coleoids (e.g. Wilby et al. 2004; Klug et al. 2009) and occasionally in ammonoids (Doguzhaeva et al. 2007), and likely could have been preserved as organic film in Nectocaris as well – that is, if it represents a cephalopod. However, as the ink sac is probably an advanced feature and may not have been present in early Palaeozoic forms, it is not taken into account during the current consideration.
The eyes of Nectocaris, although not discussed extensively by Smith & Caron (2010), may be, just as authors state, truly cephalopod-like; but we have to remember about the extreme number of convergences in that organ, and its appearances multiple (dozens of) times within the Animalia.
So what is the ‘Kraken’, if not a cephalopod?
The presence of lateral flap-like appendages in Nectocaris, two in front of the head, and its stalked eyes resemble those of the anomalocaridids, a group of pelagic predatory ecdysozoan animals that flourished in the seas from the Cambrian to at least the Devonian (Whittington & Briggs 1985; Kühl et al. 2009). The animal bears striking differences to an anomalocaridid as well, with a ‘funnel’ as a necessary derived equivalent of a feeding apparatus of other members of that group. What must be always kept in mind is that only true similarities (apomorphies), and not differences (autapomorphies and convergences) are features that can tell as something about affinities (Van Iten et al. 2006). The similarity of Nectocaris pteryx to cephalopods is only superficial, being restricted to such convergent features as a general body outline, the presence of lateral fins for undulatory swimming and eyes. However, many important differences (see Table 1) deviate from the molluscan lineage. In addition, the phylogenetic position of Nectocaris below the shelled cephalopods (Nautiloidea), as proposed by Smith & Caron (2010, fig. 3), is inconsistent with the known and logical sequence of events in the cephalopod evolution. Therefore, at the present time, it would be safer to consider Nectocaris pteryx as Dinocaridida incertae sedis (Collins 1996). We, however, refrain from doing so at this moment, waiting for more information on the evolution and diversity of anomalocaridids and their relatives, to be established.
Characters | Shelled cephalopods | Coleoids | Nectocaris pteryx |
---|---|---|---|
*reduced in octopods; **may be absent in Spirula. | |||
Shell | External | Internal* | Absent |
Phragmocone and siphuncle | Present | Present | Absent |
Radula | Present** | Present | Absent |
Jaws | Present | Present | Absent |
Mouth | Distinct | Distinct | Indistinct |
Ink sac | Occasionally preserved in ammonoids | Present | Absent |
Frontal appendages (tentacles and arms) | Up to 90 in extant Nautilus, probably 10 in some orthoceratid nautiloids and presumably numerous in ammonoids. | Eight to ten in number | Two only |
Gills | Two pairs in Nautilus and presumably ammonoids | Single pair | Single pair |
Eyes | Camera-like | Camera-like | Camera-like |
Funnel (as locomotory device) | Present | Present | Absent |
Fins | Absent | Present | Present |
Acknowledgements
The constructive comments and suggestions provided by Jerzy Dzik and an anonymous reviewer significantly improved our discussion and made our arguments stronger. This is greatly appreciated.
References
Bengtson, S. 2010: A little Kraken wakes. Nature 465, 427–428.
Boyle, P. & Rodhouse, P.G. 2005: Cephalopods: Ecology and Fisheries, 464 pp. Blackwell Publishing, Oxford.
Butterfield, N.J. 2008: An early Cambrian radula. Journal of Paleontology 82, 543–554.
Collins, D. 1996: The ‘evolution’ of Anomalocaris and its classification in the arthropod class Dinocarida (nov.) and order Radiodonta (nov.). Journal of Paleontology 70, 280–293.
Conway Morris, S. 1976: Nectocaris pteryx, a new organism from the Middle Cambrian Burgess Shale of British Columbia. Neues Jahrbuch für Geologie und Paläontologie, Monatshefte 12, 703–713.
Doguzhaeva, L.A., Mapes, R.H., Summesberger, H. & Mutvei, H. 2007: The preservation of body tissues, shell, and mandibles in the ceratitid ammonoid Austrotrachyceras (Late Triassic), Austria. In Landman N.H., Davis R.A., Mapes R.H. (eds): Cephalopods Present and Past: New Insights and Fresh Perspectives, pp. 221–238. Springer, Dordrecht.
Dzik, J. 1981: Origin of the Cephalopoda. Acta Palaeontologica Polonica 26, 161–191.
Dzik, J. 2010: Brachiopod identity of the alleged Late Cambrian monoplacophoran ancestors of cephalopods. Malacologia 52, 97–113.
Fuchs, D., Bracchi, G. & Weis, R. 2009: New octopods (Cephalopoda: Coleoidea) from the Late Cretaceous (Upper Cenomanian) of Hakel and Hadjoula, Lebanon. Palaeontology 52, 65–81.
Gabbott, S.E. 1999: Orthoconic cephalopods and associated fauna from the late Ordovician Soom Shale Lagerstatte, South Africa. Palaeontology 42, 123–148.
Hanlon, R.T. & Messenger, J.B. 2003: Cephalopod Behaviour, 224 pp. Cambridge University Press, Cambridge.
Klug, C., Schweigert, G., Fuchs, D. & Dietl, G. 2010: First record of a belemnite preserved with beaks, arms and ink sac from the Nusplingen Lithographic Limestone (Kimmeridgian, SW Germany). Lethaia 43, 445–456.
Kühl, G., Briggs, D.E.G. & Rust, J. 2009: A great-appendage arthropod with a radial mouth from the Lower Devonian Hunsrück Slate, Germany. Science 323, 771–773.
Mehl, J. 1984: Radula und Fangarmebei Michelinoceras sp. aus dem Silur von Bolivien. Paläontologische Zeitschrift 58, 211–229.
Peel, J.S. 1991: The classes Tergomya and Helcionelloida, and early molluscan evolution. Grønlands Geologiske Undersøgelse Bulletin 161, 11–65.
Simonetta, A.M. 1988: Is Nectocaris pteryx a chordate? Bollettino di Zoologia 55, 63–68.
Siveter, D.J., Sutton, M.D., Briggs, D.E.G. & Siveter, D.J. 2004: A Silurian sea-spider. Nature 431, 978–980.
Smith, M.R. & Caron, J.-B. 2010: Primitive soft-bodied cephalopods from the Cambrian. Nature 465, 469–472.
Tanabe, K. & Mapes, R.H. 1995: Jaws and radula of the Carboniferous ammonoid Cravenoceras. Journal of Paleontology 69, 703–707.
Van Iten, H., de Moraes Leme, J., Guimarães Simões, M., Marques, A. C. & Collins, A.G. 2006: Reassessment of the phylogenetic position of conulariids (?Ediacaran-Triassic) within the subphylum Medusozoa (phylum Cnidaria). Journal of Systematic Palaeontology 4, 109–118.
Warnke, K. & Keupp, H. 2005: Spirula– a window to the embryonic development of ammonoids? Morphological and molecular indications for a palaeontological hypothesis. Facies 51, 60–65.
Whittington, H.B. & Briggs, D.E.G. 1985: The largest Cambrian animal, Anomalocaris, Burgess Shale, British Columbia. Philosophical Transactions of the Royal Society of London B 309, 569–609.
Wilby, P.R., Hudson, J.D., Clements, R.G. & Hollingworth, N.T.J. 2004: Taphonomy and origin of an accumulate of soft-bodied cephalopods in the Oxford Clay Formation (Jurassic, England). Palaeontology 47, 1159–1180.
Yochelson, E.L., Flower, R.H. & Webers, G.F. 1973: The bearing of the new Late Cambrian monoplacophoran genus Knightoconus upon the origin of the Cephalopoda. Lethaia 6, 275–310.
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Received: 28 July 2010
Accepted: 5 October 2010
Published online: 7 January 2011
Issue date: 1 March 2011
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- The early history of the metazoa—a paleontologist’s viewpoint, Biology Bulletin Reviews.
- A phylogeny of fossil and living neocoleoid cephalopods, Cladistics.
- Ancestry, Origin and Early Evolution of Ammonoids, Ammonoid Paleobiology: From macroevolution to paleogeography.
- The origins of molluscs, Palaeontology.
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- Nectocaris and early cephalopod evolution: reply to Mazurek & Zatoń, Lethaia.
- Cephalopod origin and evolution: A congruent picture emerging from fossils, development and molecules, BioEssays.