Countershading and Stripes in the Theropod Dinosaur Sinosauropteryx Reveal Heterogeneous Habitats in the Early Cretaceous Jehol Biota

by Fiann M. Smithwick, Robert Nicholls , Innes C. Cuthill, and Jakob Vinther

 

Countershading and Stripes in the Theropod Dinosaur Sinosauropteryx Reveal Heterogeneous Habitats in the Early Cretaceous Jehol Biota

Authors
Fiann M. Smithwick,¹ Robert Nicholls,² Innes C. Cuthill,³ and Jakob Vinther¹³⁴

1  School of Earth Sciences, University of Bristol, Wills Memorial Building, Queens Road, Bristol BS8 1RJ, UK
2  Palaeocreations, 35 Hopps Road, Kingswood, Bristol BS15 9QQ, UK
3  School of Biological Sciences, University of Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TQ, UK
4  Lead Contact

Correspondence
jakob.vinther@bristol.ac.uk

In Brief
Smithwick et al. reconstruct the coloration of the small carnivorous dinosaur Sinosauropteryx. It had a bandit mask and striped tail and was also countershaded (see image). Using 3D models under different light, the authors show that its camouflage would have worked best in an open habitat. Paleocolor can help predict paleohabitat.

Highlights

• We have reconstructed the color pattern of the theropod dinosaur Sinosauropteryx
• Sinosauropteryx exhibited camouflage, including countershading and a bandit mask
• The countershading pattern was most likely associated with an open habitat
• Previously assumed to be forested, Jehol likely included a range of habitat types

Countershading and Stripes in the Theropod Dinosaur Sinosauropteryx Reveal Heterogeneous Habitats in the Early Cretaceous Jehol Biota

Fiann M. Smithwick,^[1] Robert Nicholls,^[2], Innes C. Cuthill,^[3] and Jakob Vinther^[1][3][4]*

1. School of Earth Sciences, University of Bristol, Wills Memorial Building, Queens Road, Bristol BS8 1RJ, UK
2. Palaeocreations, 35 Hopps Road, Kingswood, Bristol BS15 9QQ, UK
3. School of Biological Sciences, University of Bristol, Life Sciences Building, 24 Tyndall Avenue, Bristol BS8 1TQ, UK
4. Lead Contact
   * Correspondence: jakob.vinther@bristol.ac.uk
   https://doi.org/10.1016/j.cub.2017.09.032

SUMMARY

Countershading is common across a variety of lineages and ecological time [1–4]. A dark dorsum and lighter ventrum helps to mask the three-dimensional shape of the body by reducing self-shadowing and decreasing conspicuousness, thus helping to avoid detection by predators and prey [1, 2, 4, 5]. The optimal countershading pattern is dictated by the lighting environment, which is in turn dependent upon habitat [1, 3, 5, 6]. With the discovery of fossil melanin [7, 8], it is possible to infer original color patterns from fossils, including countershading [3, 9, 10]. Applying these principles, we describe the pattern of countershading in the diminutive theropod dinosaur Sinosauropteryx from the Early Cretaceous Jehol Biota of Liaoning, China. From reconstructions based on exceptional fossils, the color pattern is compared to predicted optimal countershading transitions based on 3D reconstructions of the animal’s abdomen, imaged in different lighting environments. Reconstructed patterns match well with those predicted for animals living in open habitats. Jehol is presumed to have been a predominantly closed forested environment [3, 11, 12], but our results indicate a more heterogeneous range of habitats. Sinosauropteryx is also shown to exhibit a "bandit mask," a common pattern in many living vertebrates, particularly birds, that serves multiple functions including camouflage [13–18]. Sinosauropteryx therefore shows multiple color pattern features likely related to the habitat in which it lived. Our results show how reconstructing the color of extinct animals can inform on their ecologies beyond what may be obvious from skeletal remains alone.

RESULTS

Plumage Distribution

To reconstruct the color patterns of Sinosauropteryx, we analyzed three of the best-preserved specimens available (Figures 1A and 1D and S1A). To reconstruct the color patterns accurately, first the distribution of pigmented plumage was described in detail for each specimen (Supplemental Descriptions). Each specimen shows extensive preservation of dark, presumably organically preserved fibers identified as feathers/feather homologs in distinct areas of the animal (Figures 1A and 1D and S1). Alternative interpretations of these structures as degraded skin collagen have recently been shown to be unfounded [19]. Preservation of feathers as organic films is due to the presence of the pigment melanin, and thus only originally pigmented feathers are found preserved in this manner [7, 8]. Visible absence of feathers in certain regions of the fossil is therefore likely due to unpigmented plumage that did not preserve, rather than a true absence of feathers in life [7, 8]. Alternatively, the areas lacking feathers could have been naked (there is no evidence of scales being preserved [19]) but would similarly be inferred to have been unpigmented. Because the feathering likely also served an insulatory role, an extensive distribution seems most plausible. Mapping the distribution of preserved pigmented feathers is therefore considered to reflect the extent of colored plumage on the animal, with other areas being covered by white (unpigmented) feathers.

Color Pattern Reconstruction

Illustrations of NIGP 127586 and NIGP 127587 show the pattern of plumage distribution across the fossils (Figures 1B and 1E). From this distribution, a complete reconstruction was created (Figure 2); this was done blind to any predictions from the modeling of illumination. The consistency of plumage patterns observed across multiple specimens gives confidence to the reconstructed color pattern. The pattern of pigment across the face appears to show a band of pigmented plumage running from the dorsal area of the head anterioventrally, which then angles toward the eye before running to the posterioventral margin of the lower jaw (Figures 3A–3E). The banded tail shows a transition from narrow to widely spaced bands from the proximal to distal regions, with the ventral pigmentation becoming denser toward the end of the tail. The ventral extent of the pigmented plumage, representing the likely countershading transition, appears to be relatively high on the flank, at around two-thirds of the way down the abdomen (Figures 3F–3I).

Predicted Lighting Environment

For countershading to be effective in obliterating 3D cues of an animal’s presence, the pattern of pigmentation from the dorsal to ventral body regions should match the illumination gradient created by the lighting environment in which it lives [1, 3, 5, 6]. This allows the determination of likely habitats of animals based on quantification of color patterns [1, 3]. Those that inhabit open environments with direct lighting conditions generally exhibit a sharp transition from dark to light color high up on the flanks of the body [1, 3]. Conversely, animals inhabiting a more closed habitat with diffuse lighting coming in at many angles often show a smoother gradation from dark to light lower down on the body [1, 3]. To predict the optimal pattern of countershading, we created and photographed 3D models of the abdomen of Sinosauropteryx under different lighting conditions. The reconstructed color patterns based on NIGP 127586 and NIGP 127587 (Figures 2 and 3H–3I) more closely match the pattern of countershading predicted from images of the models taken under direct light conditions than those of diffuse lighting conditions (Figure 4), indicative of animals living in open habitats [1, 3]. The addition of synthetic fur (representing feathers) made little difference to each countershading prediction (Figure 4). For direct overhead sun, the mean predicted transition point to lighter coloration was 72% (95% confidence interval [CI] 61%–83%) of the way from dorsal to ventral side. For direct sun at 30° it was 60% (95% CI 45%–75%), and for diffuse illumination it was 85% (95% CI 81%–88%). Only the direct illumination confidence intervals include the observed transition point (~67%).

DISCUSSION

Color Patterns of the Face

The presence of pigmented feathers surrounding the orbit and running in a band across the face conforms to "bandit masks" seen in many modern birds and mammals [15–18]. Multiple functions have been proposed for bandit masks in modern taxa [13, 14, 16–18]. One such function is as an anti-glare device [15, 18]. Reducing the glare from the feathers around the eye would be particularly useful to an animal living in environments with abundant direct sunlight, as is seen often in diurnal extant birds and mammals [13, 18]. Additionally, it has been suggested that glare is especially high in riparian habitats, because light reflectance is increased by proximity to water, as may have been the case in the lacustrine environment in which Sinosauropteryx fossils were deposited [15]. Pigmented bands that run directly across the orbital region may also help to mask the presence of the eyes as a form of camouflage against both predators and potential prey [20, 21]. Eye stripes are common in modern birds, which most often also have dark eyes, making them likely harder for visual predators or prey to detect, and given that eyes elicit responses from both in many situations, it is a plausible hypothesis [13]. Other possible functions of dark patches around the eyes of extant animals include aposematism and intraspecific signaling [13, 17]. Bandit masks have been suggested as being primarily aposematic in mammalian taxa living in exposed open habitats and are especially prevalent in mammalian carnivores, which co-exist with larger carnivores [17, 22, 23], as is likely to have been the situation for Sinosauropteryx. A number of modern mammals combine bandit masks with defensive nauseous discharges [22], but it is not possible to ascertain whether this was the case with Sinosauropteryx, and aposematism is generally thought to be rare in modern birds [13], making aposematism unlikely in Sinosauropteryx. Alternatively, conspicuous face markings could serve as a warning of a physical deterrent, such as a weapon or armor [17, 22, 23]. Although the theropod had an enlarged claw on each hand [24], the animal's small size makes it unlikely that it posed any real threat to its likely much larger theropod predators, making this function of the bandit mask unlikely.

Function of the Banded Tail

Banded tails are poorly understood in modern animals and likely serve several functions, including social signaling, dazzle camouflage, and outline breaking/disruptive camouflage [15–18]. Banded tails have been proposed as a way of confusing predators or drawing attention away from more vital body parts [18].

The tail of Sinosauropteryx was the longest of any known theropod relative to body length [24]. Due to this length, it is unlikely that the animal could hold it in a perfectly horizontal position consistently, which would be necessary for a countershaded pattern to be effective. This may explain why the tail is banded rather than showing the countershaded pattern seen on the animal's flanks. The great length of the tail in combination with the distinct and presumably conspicuous color bands may be explained as a distraction strategy, a method of attracting attention as far from the less-conspicuous head and body as possible. Alternatively, the banding could have served as a form of disruptive camouflage, as is seen in a number of modern animals, breaking up the outline of the tail to make it less recognizable to potential predators [15–18]. A combined function of camouflage and instraspecific signaling has also been suggested in some extant bird taxa with banded patterns [25]. However, we find no osteological evidence for an ability to lift or pose the tail, which would have limited its utility in display.

Countershading in Sinosauropteryx

A clear darker dorsum and absence of pigmented plumage ventrally, with the light ventral side extending to the tail until at least the tenth caudal vertebra, conforms to what would be expected for countershaded camouflage adapted to reduce detection from visual predators and from potential prey [1, 3–5]. Visual hunting was likely important for predators of Sinosauropteryx. Several tyrannosauroids are contemporaneous with Sinosauropteryx [26]. Although these tyrannosauroids were small for the clade [26], they would likely have been more than capable of tackling the diminutive compsognathid, which appears to have not reached sizes much greater than a meter in length [24]. Modern avian predators rely heavily on their exceptional vision to hunt, and as such it is likely that their forebears, the theropods, also had excellent visual capabilities [27]. It has been shown that a number of tyrannosauroids had visual capabilities similar to modern raptorial birds [28], and as such strong selection for camouflage would have been likely in their prey. In fact, considering that theropods were most likely tri- or tetra-chromatic, like their extant counterparts the tetrachromatic birds [29, 30] and the trichromatic crocodiles [31], the Mesozoic predator-prey dynamic would likely have been much more visual than extant terrestrial biotas in which dichromatic mammals are highest in the food chain. It is therefore not surprising to observe camouflage patterns in a small Cretaceous theropod.

Although many of the vertebrates of the Jehol Biota were arboreal or scansorial, including a number of other theropods [11], owing to its anatomy Sinosauropteryx was likely restricted to an obligate terrestrial habit and thus did not have the option of retreating to the trees to escape predators. Further, color patterns beneficial as camouflage would have aided Sinosauropteryx in hunting its own prey, which likely also relied, at least in part, on visual cues to detect predators. The hypothesis that its color patterning was predominantly driven by a need to remain cryptic is therefore parsimonious in Sinosauropteryx. Alternative explanations for countershading in modern animals, such as thermoregulation, UV protection, and the costs of producing pigmentation, could also play a role in the color patterns observed in Sinosauropteryx. The relative importance of these possible functions and their interplay in modern animals is, however, poorly understood, and thus would be difficult to explore in an extinct animal. Despite potential limitations in our understanding of countershading function in modern animals, the correlation between habitat and countershading pattern nuances has been quantitively shown in numerous extant taxa and was likely also present in the past.

Habitat Preference

The Jehol Biota includes abundant and diverse floral remains alongside its fauna [11, 32]. High paleotemperatures may have aided the development of lush forested habitats thought to have existed in much of the area [11]. Speculation has been made about certain taxa inhabiting more- or less-densely forested areas [11], and owing to the volcanic nature of the deposits it is likely that a mosaic of habitats existed in the region, with open areas occurring among denser forested regions [32]. The paleobotanical record of Jehol shows plants adapted for both arid and humid environments, suggesting climatic fluctuations through time [12]. Because all paleobotanical remains are allocthonous with no in situ plant fossils known, it is likely that different plant communities existed in the regions around the Jehol lakes and further afield [12].

It has been proposed that the larger theropods of Jehol would likely have been found in more open areas, where vegetation was less likely to impede their movement [11]. The countershading pattern of Sinosauropteryx indicates that it, too, inhabited these more open areas where predation pressure may have been significantly higher due to reduced cover than in the closed areas and where background-matching camouflage was more difficult to achieve. A need to reduce conspicuousness relative to the environment would therefore have been important to avoid detection from keen visual predators. The diminutive size of Sinosauropteryx and its relatively high countershading transition adapted for open areas indicates that it lived in habitats with either few plants or very low vegetation cover.

Further insight may come from the lizard in the stomach of NIGP 127587 (Figures 1D and 1E and S2). Of the known Jehol lizard fauna, the preserved skeletal elements most closely match those of Dalinghosaurus, found in the same deposits as Sinosauropteryx (the Yixian Formation) [33, 34]. The tail and hind limbs of Dalinghosaurus are exceptionally long relative to its forelimbs, which in modern lizards is a typical morphology of fast-moving terrestrial runners, potentially capable of bipedal locomotion at high speed [34, 35]. Shorter limbs are generally associated with arboreality [35]. Although the slender ungual phalanges of Dalinghosaurus indicate that it was likely capable of climbing [33], it appears likely it was better suited to living in the same open habitats inferred herein for the theropod.

Most groups of terrestrial vertebrates in Jehol show a strong tendency toward forest-living adaptations [11]. Sinosauropteryx, however, appears to be an exception to this rule. The insight that small theropods like Sinosauropteryx may have inhabited open habitats helps build a clearer picture of the environment in which the Jehol animals lived. Jehol clearly was not only rich taxonomically, but was also likely varied in the habitats available to animals and consisted of a mosaic of environments, which may explain the area’s extraordinary biodiversity [32]. Furthermore, the Jehol biota straddles more than 10 million years and is likely to have fluctuated in vegetation cover and landscape. Arboreal taxa and dinosaurs adapted in their color patterning to closed habitats were present in the forested areas [3, 9, 11] while larger dinosaurs and their smaller cryptically patterned prey explored open areas with less-dense vegetation. The presence of dinosaurs showing camouflage patterns adapted to different habitats indicates that the environment around the Jehol lakes was therefore diverse and varied and hosted different dinosaurian faunas. We have shown how a greater understanding of ancient environments can come from better understanding of the paleoecology of extinct animals through paleocolor reconstructions. This work furthers our understanding of how color patterns have evolved through time and highlights the importance of anti-predator camouflage strategies in deep time.

STAR★METHODS

Detailed methods are provided in the online version of this paper and include the following:

• KEY RESOURCES TABLE
• CONTACT FOR REAGENT AND RESOURCE SHARING
• METHOD DETAILS
  • Institutional Abbreviations
  • Specimen Imaging
  • 2D Illustrations and Plumage Distribution
  • 3D Abdominal Modeling
  • Predicting Lighting Environment
• QUANTIFICATION AND STATISTICAL ANALYSIS
  • Quantification of Countershading Transition
• DATA AND SOFTWARE AVAILABILITY

SUPPLEMENTAL INFORMATION

Supplemental Information includes two figures and Supplemental Descriptions and can be found with this article online at https://doi.org/10.1016/j.cub.2017.09.032.

A video abstract is available at https://doi.org/10.1016/j.cub.2017.09.032#mmc3.

AUTHOR CONTRIBUTIONS

F.M.S. produced all illustrations and the reconstruction in Figure 2A, created and imaged the 3D models, and wrote the manuscript. J.V. devised the project concepts and imaged the fossils. R.N. produced the full art reconstruction in Figure 2B. I.C.C. produced the MATLAB models and performed the statistical analyses of countershading predictions versus the reconstruction. All authors commented on the manuscript.

ACKNOWLEDGMENTS

We would like to thank Yunbai Zhang and Diying Huang for access and help with specimens. We also thank Nick Longrich for discussion. F.M.S. was funded by the Natural Environment Research Council (PhD grant NE/L002434/1).

Received: May 18, 2017
Revised: August 14, 2017
Accepted: September 14, 2017
Published: October 26, 2017

REFERENCES

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2. Thayer, A.H. (1896). The law which underlies protective coloration. Auk 13, 124–129.
3. Vinther, J., Nicholls, R., Lautenschlager, S., Pittman, M., Kaye, T.G., Rayfield, E., Mayr, G., and Cuthill, I.C. (2016). 3D camouflage in an ornithischian dinosaur. Curr. Biol. 26, 2456–2462.
4. Rowland, H.M. (2009). From Abbott Thayer to the present day: what have we learned about the function of countershading? Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 519–527.

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