The skin of ichthyosaurs

No time for anything new, unfortunately. But I have a lot of old stuff kicking around: here, I've recycled text from my undergrad thesis on ichthyosaurs. I hope you get something out of it. Ichthyosaurs are famous for preserving impressions of soft tissue; these are preserved as black, carbonaceous films, and are known for specimens that come from Solnhofen and Holzmaden in Germany, from Barrow-upon-Soar in England, and from the Wapiti Lake area of British Columbia. Martill (1993) reviewed occurrences of ichthyosaur soft tissue preservation, citing records from the Hettangian, Sinemurian, Toarcian, Callovian and Tithonian of England and Germany [Stenopterygius quadriscissus from Holzmaden shown here].

It remains controversial how these impressions formed. The conventional view is that they are a carbonaceous residue of the animal's skin (McGowan 1991) but Martill (1987) argued that in at least some specimens these body outlines were composed of autolithified mats of prokaryotes and were often modified by preparators to create sharper outlines. Keller (1992) challenged Martill's hypothesis and argued instead that soft tissues were substituted by dense microbial mats and then repaced by calcium phosphate: body outlines were not faked, and Martill's autolithified microorganisms were merely secondary, possibly of recent or subfossil origin (Keller 1992). These opinions are not, it would seem, mutually incompatible and probably both are correct in respective circumstances [note that a similar debate has surrounded fossil feathers: see Vinther et al. 2008].

Ichthyosaurs are often assumed to have had a large, dolphin-like dorsal fin but the evidence for this has been questioned (Martill 1987). Consequently some artists have been advised to exclude them from life restorations (see John Martin's illustrations in Martill (1991), text-fig. 10.4, reproduced below). A large, triangular dorsal fin - the first to be reported - on a Holzmaden ichthyosaur was interpreted by Martill (1987) as a prokaryote-replaced flap of skin torn from the carcass during decomposition, with later examples of dorsal fins being fakes constructed to conform with this outline. Martill (1987) suggested that ichthyosaurs used their small hindfins, rather than a dorsal fin, to prevent roll, and intimated that this may explain why ichthyosaurs retained hindfins throughout their history. Chinese Triassic ichthyosaurs with soft tissues have since indicated that dorsal fin were perhaps present as early as the Triassic* (e.g., Motani et al. 1996), there are too many Jurassic specimens with dorsal fins for them all to be faked, and Martill later changed his mind in any case: in Martill (1993) he stated 'I have little doubt that the dorsal fin and the dorsal lobe of the caudal fin of ichthyosaurs from Holzmaden are genuine features' (p. 85). Faking or embellishment of ichthyosaur soft tissue outlines by preparators is still a problem in some cases though, and it has also afflicted the shape of ichthyosaur tails (McGowan 1990a, 1990b, Riess 1986).

* Since I wrote that text, strange things have happened to the specimen concerned. Motani (2005) reported that 'the [soft tissue] outline was reported to be clear when the specimen was first examined in the early 1990s, but it was less conspicuous by 1995 when it was studied for the 1996 publication, and it was not possible to detect the outline with naked eyes in 1998 when the specimen was examined again' (p. 403).

As noted above, ichthyosaurs retained hindfins throughout their history. This is in contrast to cetaceans which had almost certainly lost external hindlimbs by the Oligocene at the very latest. It is hard to propose an explanation for this difference but presumably it relates to different modes of swimming. Riess (1986) extended his views on ichthyosaur forefins to hindfins and restored them as hydrofoils in some taxa but as simple stabilizers in others (Riess argued that ichthyosaur fins were used like wings in some taxa and that these ichthyosaurs were underwater fliers: for a discussion of this see Did ichthyosaurs fly? on ver 1). As they were comparatively large in some Triassic ichthyosaurs it is probable that they were important in manoeuvring.

Ichthyosaur skin fibres

In recent years, the big deal about ichthyosaur soft tissues has been that fibre-like structures are preserved within the dermis (Lingham-Soliar 1999, 2001) [adjacent image, from Lingham-Soliar (2001), shows skin fibres as preserved in a Stenopterygius. Inset shows close-up of the fibres present between the two arrows. Scale bar = 10 cm]. These have been compared to the fibre-like structures that are also present on some theropod fossils (notably Sinosauropteryx), the implication being that these comparisons exclude the possibility that theropod fibres formed an external, 'fuzzy' integument as is generally thought (Lingham-Soliar 2003). The idea that ichthyosaur and theropod fibres are somehow alike has proved popular among those who argue that theropods cannot be the ancestors of birds (Feduccia et al. 2005).

I am convinced that these comparisons are completely erroneous and misleading. In ichthyosaurs the fibres can be seen to either overlay bone or clearly be deep within the skin (viz, medial to the external skin surface) (Lingham-Soliar 1999, 2001, pers. obs.). Furthermore, most ichthyosaur skin fibres look nothing like the structures seen on the theropods: the only ones that do are arranged in an orthogonal meshwork and are preserved as overlapping layers that, again, were clearly embedded within the dermis of the ichthyosaur (Lingham-Soliar 1999, 2001) [reconstruction of skin fibres as they were arranged in a live ichthyosaur shown here, from Lingham-Soliar (2001)]. The structures in theropods were clearly external to the dermis, and look the same as the fibre-like structures present in taxa that have indisputable vaned feathers (pers. obs.). Structurally the fibre meshworks of ichthyosaurs were interpreted by Lingham-Soliar & Reif (1998) and Lingham-Soliar (1999, 2001) as analogues of the cross-fibre arrays seen in sirenian, cetacean and shark skin. Such cross-fibre arrays appear to assist in keeping the skin of these swimming animals strong, flexible and smooth (and, incidentally, it would be bizarre to expect such skin fibre meshworks to be present in terrestrial vertebrates like dinosaurs).

For more on the structures in theropods, see Feathers and filaments of non-avian dinosaurs, part I.

Thunniform tails

Because quite a lot (comparatively speaking) is known about the shape of the ichthyosaur tail, many speculations have been made about tail function. Thunniform (= tuna-shaped) ichthyosaurs (all of which belong to the clade Parvipelvia: for help with the cladogram go here) are conventionally interpreted as having used their reversed heterocercal tails to generate a down-thrust that compensated for natural buoyancy (McGowan 1973). Taylor (1987) stated that ichthyosaurs were not necessarily lighter than water however (a number of aquatic tetrapods are not) and that, by analogy with reinterpretation of the heterocercal shark tail (Thomson 1976, Thomson and Simanek 1977), proposed that the propulsive force from the tail may have been upwards. McGowan (1992) also compared new models of shark locomotion with those proposed for ichthyosaurs but argued that ichthyosaur bone density appeared to be low, thereby suggesting that they were positively buoyant after all (McGowan 1991, 1992). Bone density is correspondingly low in odontocete cetaceans (Felts 1966).

Shark tails vary considerably in morphology, complexity and behaviour (McGowan 1992) and it has proven difficult to model them in the laboratory. McGowan (1992) emphasised that shark and ichthyosaur tails are not strictly analogous: ichthyosaurs have a larger unsupported lobe than do sharks, ichthyosaur tails are more steeply-angled than those of sharks, and ichthyosaur tail support is bone whereas shark support is cartilage. Cetaceans and scombroids should be seen as better analogues, though there remain discrepancies. Because cetaceans have lungs, unlike scombroids and sharks, they are more like ichthyosaurs in having a variable buoyancy. Scombroids recall ichthyosaurs in having vertical tails that, unlike those of cetaceans, are internally supported by bone. Very high aspect ratios in some scombroids (up to 7 in Thunnus) are unlike those of both cetaceans (5 in Lagenorhynchus [sensu lato: the conventional version of Lagenorhynchus is polyphyletic]) or ichthyosaurs (3.7 in Ichthyosaurus) (Alexander 1989). An extreme is presented by a ratio of 10.26 in sailfish Istiophorus (Fierstine & Walters 1968, McGowan 1992). Motani (2002) showed how extant cruising swimmers (tunas, lamnid sharks and dolphins) correlate tightly with respect to cruising speed, the proportional size of the trailing edge of the caudal fin, and the oscillation speed of the trailing edge of the caudal fin [correlations shown in graphs below, from Motani (2002)]. When he added data from thunniform ichthyosaurs, they also correlated tightly with extant pelagic cruisers. One interesting consequence of this correlation is the inference that thunniform ichthyosaurs had elevated metabolic rates, given that all of their extant analogues do (Motani 2005). Incidentally, did thunniform ichthyosaurs sleep, given that pelagic scombroids and lamnid sharks apparently don't?

The large forelimbs of ichthyosaurs did not streamline into the body. This contrasts with scombroids, where the fins fold back into depressions or slots and thereby present a smooth external surface (Carey et al. 1971), but this cannot used as an argument against scombroid-style axial swimming in ichthyosaurs as the thunniform lamnid sharks do not fold their fins back into the body surface either.

Ichthyosaurs did not evolve a thunniform morphology directly from their terrestrial ancestors of course as the most basal ichthyosaurs were narrow, elongate animals with very high vertebral counts. Later ichthyosaurs modified this plesiomorphic long vertebral column by evolving antero-posteriorly shortened, discoidal vertebrae and deep, fusiform bodies (Motani et al. 1996). On plots of fineness ratio against caudal fin H/L ratio, Chaohusaurus (a grippidian ichthyopterygian) groups with scyliorhinid sharks while parvipelvian ichthyosaurs such as Stenopterygius group with lamnid sharks (Motani et al. 1996). Scyliorhinids and related groups are relatively sedentary, benthic sharks and may provide ecological analogues for ichthyosaurs like the chaohusaurs.

For previous Tet Zoo articles on ichthyosaurs see Did ichthyosaurs fly?, Life in the Oxford Clay sea, and Ichthyosaur wars and marvellous mixosaurs on Tet Zoo ver 1. One day I'll do the story of Alvin vs the swordfish (yes yes, swordfish aren't tetrapods. But it'll be discussed in an article on the swordfish-like eurhinosaurian ichthyosaurs).

Refs - -

Carey, F. G., Teal, J. M., Kanwisher, J. W., Lawson, K. D. & Beckett, J. S. 1971. Warm-bodied fish. American Zoologist 11, 137-145.

Feduccia. A., Lingham-Soliar, T. & Hinchliffe, J. R. 2005. Do feathered dinosaurs exist? Testing the hypothesis on neontological and paleontological evidence. Journal of Morphology 266, 125-166.

Felts, W. J. L. 1966. Some functional and structural characteristics of cetacean flippers and flukes. In Norris, K. S. (ed) Whales, Dolphins and Porpoises. University of California Press (Berkeley & Los Angeles), pp. 255-276.

Fierstine, H. L. & Walters, V. 1968. Studies in locomotion and anatomt of scombroid fishes. Memoirs of the Southern California Academy of Sciences 6, 1-31.

Keller, T. 1992. 'Weichteil-Erhaltung' bei grossen Vertebraten (Ichthyosauriern) des Posidonienschiefers Holzmadens (Oberer Lias, Mesozoikum Süddeutschlands). Kaupia 1, 23-62.

Lingham-Soliar, T. 1999. Rare soft-tissue preservation showing fibrous structures in an ichthyosaur from the Lower Lias (Jurassic) of England. Proceedings of the Royal Society of London B 266, 2367-2373.

- . 2001. The ichthyosaur integument: skin fibers, a means for a strong, flexible and smooth skin. Lethaia 34, 287-302.

- . 2003. Evolution of birds: ichthyosaur integumental fibers conform to dromaeosaur protofeathers. Naturwissenschaften 90, 428-432.

- . & Reif, W.-E. 1998. Taphonomic evidence for fast tuna-like swimming in Jurassic and Cretaceous ichthyosaurs. Neues Jahrbuch fur Geologie und Paläontologie, Abhandlungen 207, 171-183.

Martill, D. M. 1987. Prokaryote mats replacing soft tissues in Mesozoic marine reptiles. Modern Geology 11, 265-269.

- . 1991. Marine reptiles. In Martill, D. M. & Hudon, J. D. (eds) Fossils of the Oxford Clay. The Palaeontological Association (London), pp. 226-243.

- . 1993. Soupy substrates: a medium for the exceptional preservation of ichthyosaurs of the Posidonia Shale (Lower Jurassic) of Germany. Kaupia 2, 77-97.

McGowan, C. 1973. Differential growth in three ichthyosaurs: Ichthyosaurus communis, I. breviceps, and Stenopterygius quadriscissus (Reptilia, Ichthyosauria). Life Sciences Contribution Royal Ontario Museum 93, 1-21.

- . 1990. Problematic ichthyosaurs from southwest England: a question of authenticity. Journal of Vertebrate Paleontology 10, 72-79.

- . 1990. Computed tomography reveals that Eurhinosaurus (Reptilia: Ichthyosauria) does have a tailbend. Canadian Journal of Earth Sciences 27, 1541-1545.

- . 1991. Dinosaurs, Spitfires, & Sea Dragons. Harvard University Press, Cambridge, Mass. & London.

- . 1992. The ichthyosaurian tail: sharks do not provide an appropriate analogue. Palaeontology 35, 555-570.

Motani, R. 2002. Scaling effects in caudal fin propulsion and the speed of ichthyosaurs. Nature 415, 309-312.

- . 2005. Evolution of fish-shaped reptiles (Reptilia: Ichthyopterygia) in their physical environments and constraints. Annual Review of Earth and Planetary Sciences 33, 395-420.

- ., You, H. & McGowan, C. 1996. Eel-like swimming in the earliest ichthyosaurs. Nature 382, 347-348.

Riess, J. 1986. Locomotion, biophysics of swimming and phylogeny of the ichthyosaurs. Palaeontographica Abteilung A 192, 93-155.

Taylor, M. A. 1987. A reinterpretation of ichthyosaur swimming and buoyancy. Palaeontology 30, 531-535.

Thomson, K. S. 1976. On the heterocercal tail in sharks. Paleobiology 2, 19-38.

- . & Simanek, D. E. 1977. Body form and locomotion in sharks. American Zoologist 17, 343-354.

Vinther, J., Briggs, D. E. G., Prum, R. O. & Saranathan, V. 2008. The colour of fossil feathers. Biology Letters doi:10.1098/rsbl.2008.0302