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. 2017 Dec 28;3(12):e00479. doi: 10.1016/j.heliyon.2017.e00479

Rods and cones in an enantiornithine bird eye from the Early Cretaceous Jehol Biota

Gengo Tanaka a, Baochun Zhou b,⁎, Yunfei Zhang b, David J Siveter c, Andrew R Parker d
PMCID: PMC5772835  PMID: 29387816

Abstract

Extant birds have an extensive spectral range of colour vision among vertebrates, but evidence of colour vision among extinct birds has hitherto been lacking. An exceptionally well-preserved extinct enantiornithine fossil bird from the Early Cretaceous Jiufotang Formation (120 Ma) of Liaoning, China, provides the first report of mineralised soft tissue of a bird eye. Cone cells are identified, which have preserved oil droplets falling between wide ranges of size that can be compared with an extant house sparrow. The size distribution of oil droplets of extant birds demonstrates good correlation between size and the detectable wavelength range of the cone cells: UV-sensitive cones contain the smallest oil droplets, while red-sensitive cones possess the largest. The data suggests that this Early Cretaceous bird could have possessed colour vision.

Keywords: Evolution, Palaeobiology, Biological sciences

1. Introduction

Having evolved from dinosaurs during the Jurassic, birds then diversified during the Cretaceous (e.g., Xu et al., 2014). Extant diurnal birds possess colour vision, involving five types of cone cells that together can discriminate a spectrum from ultraviolet to red (Hart, 2001a; Hart, 2004; Cuthill, 2006; Bowmaker, 2008). The discovery of fossilised melanosomes in some Mesozoic animals suggests that they were adapted to a colourful world in the geological past (Li et al., 2010; Li et al., 2012; Zhang et al., 2010; Barden et al., 2011). However, compelling evidence of colour vision in fossil birds has not been reported because photoreceptors are not usually fossilised. A fossilised visual photoreceptor (Fröhlich et al., 1992; Duncan and Briggs, 1996; Tanaka et al., 2009; Tanaka et al., 2014; Schoenemann and Clarkson, 2013; Vannier et al., 2016) or a mold equivalent (Schoenemann et al., 2012) has only been reported in a total of six fossil taxa: five arthropods and one fish. Thus, examples of fossilised visual photoreceptors from extinct birds would shed light on the retinal anatomy of fossil birds and allow an assessment of whether these taxa also had the ability to distinguish colours. The spectral sensitivity of a cone retinal photoreceptor depends upon its particular combination of an opsin photopigment and a coloured oil droplet, which is located in the distal tip of the inner segment of the cone cell and functions as a cut-off filter for incoming light (Hart, 2001a; Hart, 2004; Bowmaker, 2008; Ohtsuka, 1985; Kram et al., 2010). The filtering of the specific wavelength range is also achieved by the ellipsoid positioned in front of the oil droplet (Wilby et al., 2015). These are found in some fish (e.g. sturgeon and lungfish), amphibians, reptiles, and birds (Bowmaker, 2008; Cheung et al., 2013). The colour of the oil droplets represents the wavelengths of light that are transmitted; e. g., red oil droplets transmit long wavelength (“red”) light, whereas colourless (to the human eye) oil droplets absorb the shortest (UV-A) wavelength light for vision in many animals (Kolb and Jones, 1982). Furthermore, the size of the oil droplet is correlated to its colour: for example, in the dorsal area of turtle retinas, red oil droplets are largest (diameter = 8.5 μm), yellow oil droplets are mid-sized (7.3–7.0 μm), and colourless oil droplets are the smallest (5.2–5.6 μm) (Ohtsuka, 1989). In the mid-peripheral area of the retina of chicken, the size of red oil droplets ranges between 7.9 and 6.1 μm, yellow oil droplets between 6.4 and 3.6 μm, and colourless oil droplets between 3.5 and 2.8 μm (Kram et al., 2010).

The lower Cretaceous (120 Ma) Jehol Konservat-Lagerstätte in western Liaoning, China, yields exquisitely preserved organisms from disparate taxa including feathered dinosaurs, early birds, mammals with hair, complete arthropods, and plants (Zhou et al., 2003). Fine details are preserved because the organic material was originally transported by a pyroclastic density current and sealed within the pyroclastic flow (Jiang et al., 2014). The subadult fossil bird specimen reported herein belongs to a species of Enantiornithes documented from the Early Cretaceous of Liaoning (Chiappe and Walker, 2002).

2. Material and methods

The fossil bird specimen studied herein (Fig. 1a) is a subadult stage of an unmamed enantiornithine species (personal communication with Prof. Zhonghe Zhou, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Science). A small fragment of retina measuring approximately 4 mm2 was removed from the posterodorsal margin of the fossil bird eye using a craft knife (Fig. 1b–d). It was placed on a stub, viewed under a binocular optical microscope (Olympus SZH10), uncoated, and observed in a SEM (Hitachi TM-1000) under a low vacuum at the Aitsu Marine Station of Kumamoto University, Japan. The section of fossilised retinal material was observed using a confocal laser microscope (VK-9500, KEYENCE) at the Kumamoto Industrial Research Institute. An extant house sparrow, Passer domesticus (eye diameter 0.7 cm, body length 10 cm) and a Japanese quail, Coturnix japonica (eye diameter 1.1 cm, body length 15 cm), were selected for comparative purposes because they have a body length and/or eyeball size similar to the fossil bird (eye diameter 0.65 cm). Furthermore, P. domesticus and C. japonica are distantly related (Dobson, 2012), which is preferable for the purpose of excluding phylogenetic constraint.

Fig. 1.

Fig. 1

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An enantiornithine bird from the Jiufotang Formation, Early Cretaceous, Liaoning, China (a–f) and retina of an extant house sparrow Passer domesticus (g,h). (a) Completely preserved specimen (SNHM: 6105). (b) Enlarged eye region of (a) showing eye orbit within the white dotted line, black material (white arrow) and sample point (yellow arrow) of the fragment of (c). (c) Digital microphotograph of an eye fragment. (d) SEM image of an eye fragment. (e) SEM of cone and rod cells with their oil droplets. (f) Labelled image of (e) showing position of oil droplets (red circles), cone (blue solid line) and rod (yellow solid line) cells. (g) SEM image of rods (yellow solid line), cones (blue solid line) and oil droplets (red circles). (h) Transmitted microphotograph of oil droplets. Scale bars: a = 2 cm; b = 5 mm; c,d = 100 μm; e–h = 10 μm.

The freshly-killed P. domesticus and C. japonica were obtained from the company Moukinya. The eyeballs of both birds were removed using a craft knife and fixed in phosphate buffered saline solution (PBS). Each retina was removed from the eyeball in the PBS and was rinsed with fresh PBS. Each retina of the two extant birds was partially freeze-dried for SEM observations.

In order to check for morphological alternations of retinal tissues, another naturally dried house sparrow eye was investigated to provide a control for early diagenesis.

To determine the precise size-colour relationship of the oil droplets of the extant quail and house sparrow, each retinal sheet was removed from the pigment epithelium in PBS by levering with a needle. The retinal fragment was then mounted on a slide glass and covered with a cover slip. The size of the same coloured oil droplets varies between different regions of the same eye (Hart, 2004), so only the retinal sheet removed from the marginal area of the eyeball (similar to that studied in the fossil eye) was used in this study.

The oil droplets were observed under a transmitted light microscope (Olympus CH40) with a digital video camera (Nikon DS-Vi1), and images were captured using ‘Nis-Element v. 4.0’ software. The images were saved as TIFF files using graphic software (Adobe Photoshop, version 7.01). The area of each oil droplet was calculated using area-calculating software in Image J (Rasband, 1977–2012). The colour of the oil droplet was identified by eye under a transmitted light microscope. The cone type, such as ultraviolet sensitive (UVS), short-wavelength sensitive (SWS), medium-wavelength sensitive (MWS), and long-wavelength sensitive (LWS) was determined based on Table 1 of Hart (2001b). The area data was initially preserved as an .xls file. By using free statistical software (Takeyasu, 2011), a Mann-Whitney U test (Faul et al., 2007) was performed to determine whether the values of the areas between different coloured oil droplets in the extant house sparrow were statistically distinguishable. Statistical Power (1-β) was calculated with G*Power software (ver 3.1.9.2) for checking the type II error (Faul et al., 2007). By using the R packages version 3.1.3 (R Development Core Team, 2013), Akaike information criterion (AIC) analysis (Akaike, 1974) was conducted to examine the relative quality of statistical models for a given set of data.

Table 1.

Area of oil droplets in an extant house sparrow Passer domesticus. The cone type to which each oil droplet belongs was determined based on the methods of Kolb and Jones (1982).

No. Cone type Area of oil droplet (μm2) No. Cone type Area of oil droplet (μm2)
1 green 2.9 159 red 2.7
2 green 2.8 160 double 2.6
3 blue 1.1 161 blue 1.8
4 double 2.8 162 double 2.7
5 red 3.8 163 violet 0.6
6 red 3.0 164 double 2.7
7 blue 0.9 165 red 3.6
8 red 3.0 166 blue 0.9
9 green 2.0 167 green 2.8
10 red 3.8 168 red 3.4
11 red 3.6 169 green 2.1
12 blue 1.4 170 violet 0.6
13 green 2.7 171 violet 0.7
14 red 3.2 172 red 4.3
15 red 4.2 173 double 3.1
16 double 3.8 174 double 3.0
17 green 2.3 175 double 2.7
18 double 2.5 176 blue 1.0
19 green 3.1 177 double 2.9
20 green 3.1 178 green 2.3
21 green 2.0 179 violet 0.4
22 green 2.3 180 violet 0.7
23 green 2.7 181 green 3.3
24 green 2.5 182 green 3.0
25 green 2.3 183 violet 0.7
26 green 2.3 184 red 3.9
27 green 2.5 185 violet 0.4
28 green 3.2 186 green 3.2
29 red 3.1 187 double 2.2
30 green 2.4 188 double 3.0
31 green 2.5 189 violet 0.9
32 green 3.0 190 green 2.8
33 green 2.1 191 red 4.1
34 double 2.5 192 double 3.3
35 green 2.2 193 double 3.2
36 violet 0.6 194 double 2.9
37 double 2.2 195 red 3.9
38 green 1.7 196 green 3.2
39 double 2.3 197 double 2.7
40 blue 1.0 198 blue 0.9
41 green 1.9 199 green 3.4
42 double 3.2 200 violet 0.8
43 double 3.4 201 violet 0.9
44 double 2.5 202 violet 0.7
45 double 2.7 203 violet 0.4
46 double 3.4 204 blue 1.2
47 green 3.4 205 red 3.5
48 double 2.9 206 violet 1.0
49 double 3.0 207 double 3.0
50 red 4.2 208 red 3.5
51 double 2.3 209 double 3.1
52 double 2.6 210 green 3.1
53 green 2.9 211 double 2.6
54 double 3.0 212 green 2.5
55 red 4.1 213 blue 0.6
56 red 4.5 214 violet 0.6
57 double 3.0 215 violet 0.5
58 double 3.2 216 violet 0.7
59 double 2.9 217 violet 0.7
60 double 2.9 218 blue 1.1
61 green 2.4 219 violet 0.7
62 red 4.0 220 red 3.9
63 violet 1.1 221 double 2.8
64 double 2.8 222 double 2.8
65 double 3.2 223 double 2.5
66 double 2.5 224 double 3.3
67 violet 0.7 225 blue 0.7
68 violet 0.9 226 double 3.4
69 double 2.2 227 red 3.9
70 red 3.2 228 double 2.6
71 double 2.5 229 red 3.8
72 double 2.1 230 green 3.3
73 red 2.8 231 double 2.8
74 blue 1.6 232 blue 1.4
75 double 2.4 233 red 3.2
76 double 3.2 234 blue 1.0
77 red 3.4 235 green 2.9
78 blue 1.1 236 violet 0.9
79 blue 1.6 237 double 2.3
80 red 3.5 238 violet 0.5
81 double 3.2 239 double 2.7
82 green 3.5 240 double 2.5
83 red 3.4 241 green 2.6
84 double 2.3 242 double 1.9
85 blue 1.4 243 double 2.5
86 blue 1.2 244 double 2.5
87 double 2.8 245 blue 0.4
88 violet 1.0 246 blue 0.8
89 red 2.9 247 double 2.3
90 green 1.5 248 double 2.6
91 green 2.1 249 violet 0.3
92 violet 1.2 250 violet 0.6
93 double 3.3 251 double 2.5
94 double 3.7 252 red 3.5
95 double 2.4 253 double 2.1
96 red 3.4 254 red 3.4
97 double 3.2 255 double 2.7
98 green 2.7 256 violet 0.6
99 red 3.4 257 double 3.2
100 double 2.5 258 violet 0.5
101 blue 1.3 259 double 3.1
102 green 2.8 260 double 2.7
103 blue 1.0 261 violet 0.5
104 red 3.6 262 green 2.8
105 double 2.6 263 violet 0.9
106 violet 1.1 264 double 2.3
107 double 2.9 265 red 4.0
108 blue 0.7 266 violet 0.8
109 red 4.3 267 violet 0.9
110 green 2.7 268 green 2.7
111 green 2.9 269 violet 1.1
112 green 2.7 270 violet 1.0
113 green 2.5 271 green 2.8
114 green 2.0 272 violet 0.8
115 blue 0.9 273 double 3.0
116 green 3.8 274 blue 0.9
117 blue 1.7 275 double 3.2
118 violet 1.1 276 green 2.6
119 violet 1.3 277 violet 0.7
120 violet 1.3 278 violet 0.7
121 violet 1.0 279 double 3.5
122 red 2.9 280 double 3.6
123 double 2.0 281 red 3.9
124 blue 1.3 282 double 2.5
125 violet 1.1 283 green 2.7
126 violet 0.9 284 blue 0.8
127 double 2.5 285 green 3.1
128 red 3.3 286 blue 0.9
129 blue 1.4 287 violet 0.5
130 violet 1.0 288 green 2.6
131 violet 0.8 289 green 3.6
132 green 2.5 290 green 3.5
133 violet 1.0 291 double 2.5
134 red 2.8 292 red 3.9
135 violet 0.5 293 red 3.8
136 double 2.3 294 double 3.0
137 green 2.9 295 green 3.3
138 double 1.9 296 violet 1.2
139 red 3.2 297 green 3.2
140 double 2.6 298 red 3.8
141 double 2.4 299 violet 0.7
142 double 2.7 300 violet 0.7
143 green 2.3 301 double 3.1
144 red 2.5 302 red 3.6
145 double 2.2 303 green 2.5
146 violet 0.9 304 double 3.4
147 red 4.1 305 double 3.0
148 double 3.0 306 double 3.1
149 green 2.4 307 red 3.1
150 red 2.8 308 double 2.7
151 double 3.0 309 double 2.3
152 double 3.0 310 green 2.3
153 green 2.4 311 red 3.3
154 double 3.2 312 double 2.7
155 red 3.0 313 green 2.1
156 red 2.5 314 red 4.0
157 blue 1.2 315 double 3.5
158 double 2.5 316 blue 1.2
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Elemental distribution and spectral patterns were obtained using energy-dispersive X-ray fluorescence (EDXRF) microscopy (XGT-5000 V, HORIBA) at 20 kV accelerated voltage and 5.2 mA probe current, using mono-capillary primary optics to focus the X-ray beam to a diameter of 10 μm. A fragment of fossil retina was attached to an aluminum stage; its position in the vacuum chamber was adjusted using a motorized xyz platform and viewed using three integrated colour video cameras. An area of 256 μm × 200 μm was analysed under full vacuum using 50 mm steps and 200,000 frames to provide two-dimensional distribution maps and spectral patterns of three points for seven elements, Mg, Si, P, K, Ca, Mn and Fe. The EDXRF analyses were performed at the Centre of Advanced Instrumental Analysis, Kyushu University.

All illustrated specimens are deposited in Shanghai Natural History Museum, Branch of Shanghai Science and Technology Museum.

3. Results

The eye of the fossil enantiornithine specimen contains black material, like that of a fossil fish (Tanaka et al., 2014), and fills the eye orbit (Fig. 1a,b). Digital microphotographs and scanning electron micrographs (SEMs) of the black material and adjacent bone reveal morphological differences: the coarse surface of the black material (the area surrounded by a yellow dotted line in Fig. 1c) is clearly distinguished from that of the bone, which has a smooth surface with several Haversian canals (Fig. 1c,d). The black material contains three-dimensional, mineralized outer cones and oil droplets (Figs. 1e,f; 2a,b and 3a,b ). The shape of the cones and droplets is the same as those of the extant house sparrow (Figs. 1e–h; 2a,b,e,f; 3 and 4 ), although the oil droplets in the fossilised material (Figs. 1e,f; 2a,b; 3 and 5b ) lack colour. The diameter of the oil droplets in both the fossil bird and the extant house sparrow ranges from 2 μm to 0.9 μm (Figs. 1e–h; 2a,b,e,f; 3 and 4a,b,e,f). Fossilised pigment epithelium and its fibrous structures (Fig. 2c,d) are also preserved in the distal part of the cone and rod cells; these are comparable to those of the pigment epithelium of the extant house sparrow (Figs. 2g,h and 4g). The fossil cones, rods, and oil droplets are preserved rather flattened (Fig. 2a–d), and look like those of the natural dried extant house sparrow (Fig. 4e–h).

Fig. 2.

Fig. 2

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SEM images of the retinas of an Early Cretaceous enantiornithine bird and an extant house sparrow Passer domesticus. (a) A fragment of the retina of the fossil bird preserving many oil droplets (o) in the upper left region of the broken line, pigment epithelium (p), and rods (r) and cones (c). (b) Magnified image of (a) showing oil droplets (red circles) and pigment epithelium (p), and rods (yellow solid line) and cones (blue solid line). (c) A fragment of the fossil pigment epithelium (p) with preserved fine fibrous structures. (d) An enlargement of the fossil pigment epithelium containing elongate melanosomes (m). (e) Transverse section of the retina of an extant house sparrow. The retina is composed of pigment epithelium (p), cones (c) and rods (r) with oil droplets, an outer nuclear layer (on), and an inner nuclear layer (in) oriented in the proximal-distal plane of the eyeball. (f) A fragment of the retina of an extant house sparrow. Many oil droplets (red circles) were removed from cones. (g) Pigment epithelium (p) of an extant house sparrow. (h) An enlargement of pigment epithelium of an extant house sparrow containing elongate melanosomes (m). Scale bars: a, e = 50 μm; b–d, f–h = 10 μm.

Fig. 3.

Fig. 3

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Unlabelled (a, c) and labelled (b, d) SEM images of an Early Cretaceous enantiornithine bird and an extant house sparrow Passer domesticus. (a, b) A fragment of the retina of the fossil bird. (c, d) A freeze dried fragment of the retina of the house sparrow. Labelled images indicate rods (yellow solid line), cones (blue solid line) and oil droplets (red circles). Scale bar = 10 μm.

Fig. 4.

Fig. 4

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SEM images of the retinas of an Early Cretaceous enantiornithine bird and a natural dried extant house sparrow Passer domesticus. (a) A fragment of the retina of the fossil bird preserving many oil droplets (o) in the upper left region, pigment epithelium (p), and rods (c) and cones (c). (b) Enlarged image of (a) showing oil droplets (red circles), pigment epithelium (p), and rods (yellow solid line) and cones (blue solid line). (c) A fragment of the fossil pigment epithelium (p) with preserved fine fibrous structures. (d) An enlargement of the fossil pigment epithelium containing elongate melanosomes (m). (e) The photosensitive organ of an extant house sparrow that is composed of cones (blue solid line) and rods (yellow solid line) with oil droplets (red circles). (f) An enlargement of (e). Oil droplets (red circles) and cone and rods (c & r) are rather flattened but associated with each other. (g) Pigment epithelium (p) of an extant house sparrow. (h) An enlargement of pigment epithelium (p) of an extant house sparrow containing elongate melanosomes. Melanosomes (m) are distinguished from bacteria (b) by their longer shape. Scale bars: a, e = 50 μm; b–d, f–h = 10 μm.

Fig. 5.

Fig. 5

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A fragment of fossil retina of an Early Cretaceous enantiornithine bird and the distribution of elements within. (a) Digital microphotographs of a retinal region. (b,c) Enlargement of an area observed by laser microscope (b) and SEM (c). (d) Backscattered electron image of (a). (e–i) Distribution of the elements P, Ca, Mn, Fe, and K.

The house sparrow and the extant Japanese quail identifies a common tendency between the frequency distribution of area of oil droplets and their associated cone photoreceptors (cone types in Figs. 6 and 7 ; Tables 1 and 2 ); specifically, the ultraviolet (UVS) and short-wavelength sensitive cones (SWS) are smallest (Figs. 6b, c and 7b, c), the medium-wavelength sensitive cones (MWS) are mid-sized (Figs. 6d and 7d), and the long-wavelength sensitive cones (LWS) are the largest (Figs. 6f and 7f). In both samples from the extant birds, the frequency distribution of the area of the individual oil droplets also correlates with overall cone type (Figs. 6a–f and 7a–f). Further analysis was performed on the extant house sparrow, as it has a similar size range of oil droplets to the fossil bird. The result of a Mann-Whitney U test (Mann and Whitney, 1947) showed that each oil-droplet colour can be distinguished statistically (p < 0.05, 1- β > 0.8), except for the combination of the dark green/red oil droplets (Table 3). The result suggests that four morphological types of oil droplets occur in the extant house sparrow.

Fig. 6.

Fig. 6

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Frequency distribution of area of oil droplets of an extant house sparrow Passer domesticus. (a) Histogram of all oil droplet sizes. (b–f) Histogram of sizes for each type of coloured oil droplet: clear (b), light blue (c), yellow (d), dark green (e), and red (f) (these are correlated with ultraviolet sensitive single cones [UVS], short-wavelength sensitive single cones [SWS], medium-wavelength sensitive single cones [MWS], intermediate sensitive double cones [IWS], and long-wavelength sensitive single cones [LWS], respectively). SD = Standard deviation, CI = Confidence interval.

Fig. 7.

Fig. 7

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Frequency distribution of area of oil droplets of an extant Japanese quail Coturnix japonica. (a) Histogram of all oil droplet size. (b–f) Histogram of sizes for each type of coloured oil droplet: clear (b), light blue (c), yellow (d), dark green (e), and red (f) (these are correlated with ultraviolet sensitive single cones [UVS], short-wavelength sensitive single cones [SWS], medium-wavelength sensitive single cones [MWS], unknown sensitive single cones [UWS], intermediate sensitive double cones [IWS], and long-wavelength sensitive single cones [LWS], respectively). SD = Standard deviation, CI = Confidence interval.

Table 2.

Area of oil droplets in an extant Japanese quail Coturnix japonica. The cone type to which each oil droplet belongs was determined based on the methods of Kolb and Jones (1982).

No. Cone type Area of oil droplet (μm2) No. Cone type Area of oil droplet (μm2)
1 red 5.5 255 violet 0.7
2 violet 1.1 256 red 3.8
3 red 4.5 257 violet 0.5
4 red 3.8 258 violet 0.8
5 red 5.9 259 red 3.1
6 red 4.0 260 violet 0.5
7 green 3.2 261 green 1.7
8 red 5.7 262 double 1.7
9 green 2.4 263 double 2.6
10 green 3.0 264 double 1.7
11 violet 1.0 265 green 1.8
12 green 1.9 266 violet 0.6
13 red 4.9 267 green 1.8
14 blue 1.5 268 green 1.4
15 red 4.6 269 red 3.3
16 green 1.8 270 green 1.0
17 violet 1.0 271 green 1.6
18 red 5.6 272 red 4.6
19 red 4.2 273 green 1.6
20 red 6.2 274 green 1.2
21 red 4.3 275 red 4.6
22 red 4.8 276 green 1.7
23 green 1.9 277 green 1.0
24 green 2.2 278 green 1.1
25 red 4.7 279 blue 0.9
26 red 4.3 280 green 1.1
27 violet 1.1 281 green 1.7
28 blue 1.0 282 green 1.6
29 blue 0.9 283 red 4.1
30 double 3.0 284 green 1.4
31 violet 0.6 285 violet 0.6
32 red 5.1 286 violet 0.4
33 green 2.0 287 red 3.6
34 blue 1.1 288 green 1.5
35 red 4.6 289 violet 0.7
36 green 3.8 290 green 2.4
37 violet 0.9 291 violet 0.7
38 green 2.3 292 green 1.2
39 violet 1.1 293 green 2.1
40 blue 0.7 294 green 1.6
41 double 2.8 295 green 1.8
42 red 4.7 296 green 1.1
43 green 1.1 297 green 1.2
44 green 1.2 298 violet 0.4
45 red 4.3 299 blue 0.7
46 blue 0.8 300 green 1.6
47 green 1.3 301 red 3.8
48 green 1.3 302 green 1.6
49 violet 0.7 303 green 1.9
50 violet 1.3 304 green 2.1
51 red 5.0 305 green 2.1
52 green 2.9 306 violet 0.5
53 double 2.8 307 violet 1.1
54 green 1.8 308 green 1.7
55 green 2.2 309 blue 0.4
56 violet 1.2 310 red 5.9
57 red 4.1 311 green 1.7
58 green 1.5 312 green 1.9
59 violet 1.1 313 green 1.8
60 green 1.7 314 green 1.6
61 green 2.1 315 green 2.2
62 red 5.7 316 red 4.4
63 blue 1.2 317 green 1.5
64 red 4.1 318 red 5.4
65 blue 0.8 319 green 1.7
66 green 1.8 320 green 1.4
67 red 4.0 321 green 1.5
68 double 2.6 322 violet 0.5
69 red 4.3 323 green 1.9
70 green 2.6 324 violet 0.4
71 green 2.2 325 red 4.7
72 green 2.2 326 blue 0.5
73 green 2.0 327 red 5.0
74 blue 0.8 328 green 1.8
75 red 3.5 329 red 5.1
76 violet 0.6 330 green 1.5
77 violet 0.6 331 green 2.7
78 green 1.9 332 green 1.8
79 violet 1.1 333 green 1.7
80 red 3.9 334 green 1.4
81 blue 0.5 335 green 1.5
82 red 4.5 336 red 4.5
83 green 1.9 337 green 1.4
84 green 2.1 338 green 2.2
85 violet 0.8 339 green 2.2
86 red 5.0 340 green 1.5
87 blue 0.7 341 violet 0.8
88 red 3.7 342 green 2.2
89 green 1.7 343 red 5.6
90 green 1.8 344 violet 0.4
91 green 1.5 345 green 2.1
92 violet 0.4 346 blue 0.4
93 red 3.4 347 green 1.7
94 green 2.0 348 green 2.3
95 green 1.6 349 green 1.3
96 blue 1.2 350 violet 0.4
97 green 1.7 351 green 1.6
98 violet 0.6 352 violet 0.6
99 red 4.8 353 violet 0.5
100 green 2.2 354 green 1.5
101 green 1.9 355 green 1.5
102 green 1.4 356 violet 0.4
103 green 2.3 357 green 1.2
104 green 1.7 358 red 4.7
105 red 4.8 359 green 1.7
106 green 1.4 360 green 1.5
107 green 2.0 361 red 5.2
108 double 1.5 362 green 2.3
109 green 1.9 363 double 1.7
110 red 4.8 364 double 1.7
111 red 4.5 365 red 4.7
112 violet 0.8 366 green 1.2
113 green 1.6 367 green 1.8
114 green 2.3 368 green 1.8
115 violet 0.9 369 green 1.6
116 red 3.9 370 green 1.5
117 blue 0.9 371 blue 0.5
118 green 1.9 372 green 1.8
119 red 3.9 373 double 2.1
120 red 4.3 374 green 1.7
121 green 1.7 375 violet 0.5
122 green 1.4 376 red 3.9
123 violet 0.4 377 violet 0.8
124 green 1.9 378 green 1.2
125 green 1.6 379 green 1.7
126 violet 0.4 380 blue 0.5
127 red 4.7 381 green 1.7
128 double 2.7 382 violet 0.5
129 green 1.3 383 double 1.4
130 blue 0.6 384 red 5.2
131 green 1.5 385 green 1.9
132 blue 1.0 386 green 1.1
133 red 4.1 387 red 4.8
134 blue 0.9 388 green 1.4
135 green 1.7 389 green 2.2
136 violet 0.8 390 red 4.6
137 green 2.2 391 blue 0.5
138 red 5.3 392 green 1.8
139 blue 0.9 393 green 2.8
140 green 2.3 394 violet 0.4
141 red 4.9 395 green 1.9
142 blue 0.7 396 violet 0.7
143 green 1.8 397 green 2.7
144 green 1.8 398 red 5.1
145 violet 0.7 399 violet 0.5
146 green 1.8 400 green 2.0
147 violet 0.6 401 green 1.7
148 blue 0.3 402 violet 0.4
149 violet 0.6 403 green 2.4
150 green 1.8 404 double 2.3
151 red 5.6 405 double 2.5
152 green 1.5 406 green 2.3
153 violet 0.7 407 violet 0.6
154 green 2.0 408 blue 0.7
155 violet 0.4 409 green 2.3
156 violet 0.7 410 green 2.1
157 green 1.8 411 red 4.9
158 double 1.6 412 violet 0.4
159 red 4.0 413 blue 0.8
160 green 2.1 414 green 2.3
161 violet 0.5 415 blue 0.5
162 red 3.9 416 blue 0.5
163 blue 0.6 417 green 2.1
164 green 2.1 418 green 2.8
165 violet 0.5 419 red 5.4
166 violet 0.7 420 red 5.0
167 green 1.9 421 red 5.3
168 red 4.8 422 green 2.1
169 violet 0.6 423 violet 0.5
170 double 2.1 424 green 2.3
171 green 1.4 425 red 5.6
172 green 1.8 426 double 2.6
173 violet 0.6 427 violet 0.4
174 green 1.6 428 blue 0.6
175 red 3.9 429 green 2.7
176 green 2.3 430 green 2.4
177 violet 0.7 431 green 2.3
178 violet 0.8 432 green 1.8
179 green 1.5 433 red 3.9
180 red 3.9 434 violet 0.4
181 green 1.7 435 double 2.7
182 green 1.9 436 violet 0.3
183 red 5.8 437 green 1.6
184 green 1.6 438 red 4.0
185 green 1.7 439 red 4.4
186 green 1.4 440 red 4.8
187 red 3.6 441 violet 0.4
188 red 4.4 442 violet 0.4
189 green 1.6 443 double 2.8
190 red 3.9 444 green 1.8
191 blue 0.5 445 green 2.1
192 red 3.9 446 green 2.4
193 blue 1.1 447 red 4.3
194 double 2.1 448 green 1.7
195 red 3.9 449 green 2.0
196 blue 0.6 450 green 1.7
197 green 1.9 451 violet 0.5
198 red 3.7 452 red 4.6
199 green 1.6 453 green 1.8
200 double 1.8 454 green 2.3
201 double 2.8 455 blue 0.4
202 red 3.9 456 green 2.2
203 green 1.4 457 red 5.5
204 blue 0.9 458 green 2.0
205 green 1.9 459 green 2.1
206 green 2.1 460 red 4.6
207 green 1.6 461 green 1.8
208 red 3.8 462 green 2.1
209 red 4.1 463 green 3.3
210 green 1.6 464 blue 0.6
211 blue 0.6 465 violet 0.5
212 blue 0.5 466 green 2.1
213 green 1.4 467 violet 0.6
214 green 1.3 468 red 5.3
215 green 1.7 469 double 2.2
216 red 3.4 470 blue 0.6
217 green 1.8 471 green 2.1
218 green 1.8 472 green 2.3
219 red 3.5 473 red 4.5
220 green 1.8 474 green 1.6
221 green 2.0 475 blue 0.5
222 violet 0.5 476 green 2.4
223 green 1.8 477 green 2.2
224 red 3.7 478 green 2.2
225 green 1.8 479 blue 0.4
226 violet 0.4 480 violet 0.6
227 violet 0.5 481 red 5.3
228 green 1.5 482 double 1.9
229 red 4.2 483 red 5.2
230 blue 0.5 484 green 2.0
231 red 3.8 485 violet 0.5
232 red 4.9 486 green 2.0
233 green 1.4 487 red 5.3
234 green 1.2 488 green 1.5
235 red 4.3 489 violet 0.4
236 green 1.4 490 green 2.6
237 green 1.4 491 double 2.1
238 violet 0.5 492 red 4.6
239 blue 0.5 493 green 1.5
240 red 4.5 494 green 2.1
241 green 1.5 495 green 2.5
242 red 4.8 496 red 5.1
243 blue 0.4 497 violet 0.5
244 red 4.4 498 green 1.7
245 blue 0.8 499 green 2.4
246 violet 0.6 500 red 4.8
247 blue 0.5 501 green 1.7
248 violet 0.8 502 blue 0.7
249 violet 0.6 503 violet 0.4
250 red 3.4 504 green 3.2
251 violet 1.0 505 blue 0.5
252 double 2.1 506 red 5.1
253 red 4.5 507 green 2.0
254 green 1.3 508 red 5.2
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Table 3.

Result of a Mann-Whitney U test of oil droplets of an extant house sparrow Passer domesticus. (a) z score, (b) p-value two-tailed, (c) Statistical power (1 − β).

a clear light blue yellow dark green red
clear
light blue 3.771
yellow 9.378 7.865
dark green 9.947 8.096 0.679 z
red 8.863 7.563 7.079 0.967
b clear light blue yellow dark green red
clear
light blue 0
yellow 0 0
dark green 0 0 0.497 p
red 0 0 0 0.334
c clear light blue yellow dark green red
clear
light blue 0.999
yellow 1.000 1.000
dark green 1.000 1.000 0.252 1-β
red 1.000 1.000 1.000 1.000
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To determine the size (maximum projected area) differences among the fossilised oil droplets, and to assess whether the oil droplet size is comparable with that of the extant house sparrow, we examined the frequency distribution of the maximum projected area of fossil oil droplets and the size range of the oil droplets of the extant house sparrow (Fig. 8). The fossil oil droplets exhibited a broad range of sizes, correlating with the UVS to LWS (Table 4).

Fig. 8.

Fig. 8

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Frequency distribution of the maximum projected area of oil droplets of an Early Cretaceous enantiornithine bird and the range of each oil droplet size in an extant house sparrow. (a) Histogram of fossil oil droplet size based on Table 1. (b) Box-and-whisker diagrams of extant oil droplets size of house sparrow drawn from Fig. 6 and Table 2. The violet, light blue, green, gray, and red ranges correlate with ultraviolet sensitive single cones [UVS], short- wavelength sensitive single cones [SWS], medium-wavelength sensitive single cones [MWS], intermediate sensitive double cones [IWS], and long-wavelength sensitive single cones [LWS], respectively.

Table 4.

Area of oil droplets in an Early Cretaceous enantiornithine bird.

No. Cone type Area of oil droplet (μm2) No. Cone type Area of oil droplet (μm2)
1 - 1.1 98 - 0.7
2 - 0.6 99 - 3.2
3 - 0.9 100 - 1.4
4 - 0.8 101 - 3.4
5 - 1.2 102 - 1.0
6 - 3.7 103 - 1.1
7 - 0.8 104 - 1.1
8 - 0.8 105 - 1.0
9 - 2.4 106 - 1.0
10 - 0.8 107 - 3.2
11 - 2.8 108 - 2.6
12 - 0.6 109 - 1.0
13 - 0.7 110 - 1.0
14 - 2.6 111 - 0.7
15 - 2.6 112 - 0.9
16 - 0.9 113 - 0.9
17 - 0.9 114 - 0.7
18 - 1.2 115 - 0.9
19 - 0.7 116 - 1.1
20 - 3.0 117 - 0.8
21 - 3.2 118 - 2.5
22 - 0.7 119 - 3.2
23 - 0.6 120 - 3.0
24 - 0.7 121 - 1.0
25 - 2.1 122 - 0.9
26 - 0.5 123 - 0.9
27 - 1.0 124 - 0.8
28 - 0.5 125 - 1.2
29 - 0.6 126 - 1.2
30 - 3.6 127 - 1.0
31 - 1.0 128 - 3.2
32 - 3.6 129 - 1.0
33 - 0.7 130 - 1.1
34 - 3.7 131 - 1.3
35 - 1.3 132 - 1.2
36 - 0.8 133 - 0.9
37 - 1.1 134 - 1.8
38 - 0.8 135 - 0.8
39 - 1.1 136 - 1.1
40 - 3.7 137 - 2.7
41 - 0.7 138 - 1.9
42 - 0.8 139 - 4.1
43 - 3.1 140 - 1.5
44 - 4.0 141 - 0.8
45 - 1.0 142 - 0.8
46 - 0.5 143 - 0.9
47 - 1.0 144 - 1.0
48 - 0.9 145 - 1.1
49 - 1.2 146 - 2.5
50 - 2.8 147 - 0.9
51 - 2.8 148 - 0.9
52 - 3.9 149 - 1.3
53 - 1.7 150 - 4.4
54 - 1.0 151 - 2.0
55 - 1.1 152 - 0.8
56 - 0.9 153 - 1.9
57 - 0.9 154 - 2.9
58 - 0.8 155 - 3.2
59 - 1.6 156 - 1.0
60 - 1.4 157 - 0.9
61 - 1.1 158 - 4.5
62 - 4.2 159 - 1.2
63 - 1.3 160 - 1.2
64 - 4.0 161 - 4.2
65 - 0.9 162 - 4.3
66 - 1.0 163 - 0.7
67 - 0.9 164 - 3.2
68 - 1.1 165 - 3.2
69 - 0.9 166 - 1.3
70 - 0.9 167 - 1.1
71 - 0.9 168 - 0.9
72 - 0.9 169 - 2.9
73 - 0.9 170 - 0.9
74 - 0.7 171 - 1.0
75 - 0.5 172 - 1.1
76 - 0.7 173 - 1.1
77 - 0.7 174 - 2.8
78 - 0.7 175 - 0.9
79 - 3.1 176 - 0.9
80 - 4.2 177 - 1.0
81 - 0.7 178 - 0.9
82 - 0.9 179 - 1.0
83 - 0.9 180 - 0.8
84 - 1.3 181 - 0.9
85 - 0.5 182 - 2.4
86 - 3.2 183 - 0.9
87 - 0.9 184 - 2.5
88 - 3.4 185 - 1.0
89 - 4.9 186 - 2.3
90 - 3.7 187 - 0.6
91 - 2.1 188 - 2.5
92 - 0.6 189 - 1.0
93 - 0.8 190 - 2.9
94 - 0.7 191 - 1.1
95 - 3.3 192 - 1.0
96 - 1.3 193 - 2.1
97 - 1.0
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In order to select the relative quality of statistical models for a given set of data (Tables 1, 2 and 4), the Akaike information criterion (AIC) analysis (Akaike, 1974) was carried out (Table 5). The AIC models suggest that the size range of the fossil oil droplets forms one peak (directional asymmetry), the same as those of the extant house sparrow and Japanese quail (Table 5).

Table 5.

Basic statistics and AIC values for the FA, DA, AS, and Skewed AS models to discriminate the type of asymmetry for an enantiornithine fossil bird, house sparrow and Japanese quail. n = number of specimens, SD = standard deviation, FA = fluctuating asymmetry, DA = directional asymmetry, AS = Antisymmetry.

AIC for each model
Specimens n Mean SD FA DA AS Skewed AS
Enantiornithes fossil bird 193 1.59 1.10 804.43 586.50 806.35 588.50
House sparrow (Passer domesticus) 316 2.37 1 1498.4 923.17 1354.08 925.17
Japanese quail (Coturnix japonica) 508 2.16 1.5 2422.4 1841.19 2420.84 1843.19
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Elemental distribution and spectral patterns of the fossil bird sample showed that calcium and phosphate dominated both the retinal and bone areas (Fig. 5), but a higher concentration of phosphate was detected in the retinal area than in the bone area (Fig. 9).

Fig. 9.

Fig. 9

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Elemental spectral patterns of three points of a fragment of fossil retina of an Early Cretaceous enantiornithine bird and the distribution of elements. (a,b) Spectral patterns from retinal region (black coloured area). (c) Spectral patterns from bone region (light-yellow coloured area).

4. Discussion and conclusion

This paper reports a unique case of a preserved retina in a fossil bird, including the only record of avian fossil oil droplets, cones and rods, and pigment epithelium. Furthermore, the fossil cones, rods, and oil droplets were rather flattened (Fig. 2a–d) like those of the natural dried extant house sparrow (Fig. 4e–h). This result suggests that the fossil retina was dried (thereby indicating that the bird had already died) before it was transported into water to become preserved as a fossil. Elemental spectral patterns denoted a higher concentration of phosphate in the retinal area than in the bone area (Fig. 9), indicating that soft tissues were replaced by calcium phosphate under high phosphorus levels in early diagenesis (Maeda et al., 2011; Vannier et al., 2016). These findings provide compelling evidence that the general retinal anatomy of birds was in place 120 Ma. Additionally, the presence of oil droplets of a wide range of sizes indicates that the Cretaceous bird likely possessed colour vision. Further, in terms of the bias towards the smaller end of the potential size distribution, the fossil eye oil droplets are more similar to those of the extant house sparrow than to the extant lizards (Bowmaker et al., 2005).

To extract the size (maximum projected area) differences among fossilised oil droplets, and to determine whether the oil droplet size histogram shows a single peak or not, Silverman’s test (Schwaiger and Holzmann, 2013) was carried out (Fig. 10, Table 4). The result showed that the p value was <0.05 in k = 1, indicating that there were more than two types of oil droplets based on size (Fig. 10). Our examination of the extant house sparrow also indicates that there are at least two types of oil droplets based on size (Fig. 11, p < 0.05 in k = 1). Furthermore, there is a good correlation between the size of an oil droplet and its peak wavelength sensitivity (cone type in Fig. 6); specifically, the ultraviolet (UVS) and short-wavelength sensitive cones (SWS) tend to be distributed in the small size region of the histogram (Figs. 6a–c and 11). However, in a nocturnal bird, the Ural owl Strix uralensis, only pale green-coloured oil droplets have been found (Gondo and Ando, 1995). The result of a Silverman’s test using Fig. 7 of Gondo and Ando (1995), further suggests a single peak (Fig. 12, Table 6, p > 0.05 in k = 1–5). Therefore, the histogram of the fossil bird and extant house sparrow shows two peaks based on Silverman’s test and can be discriminated from the nocturnal bird (Ural owl).

Fig. 10.

Fig. 10

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Frequency distribution of the cross-sectional area of oil droplets of a Cretaceous enantiornithine bird. (a) Histogram of oil droplet size. (b) Kernel density estimation of (a). (c) Result of number of modes (k) and p-values.

Fig. 11.

Fig. 11

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Frequency distribution of the cross-sectional area of oil droplets of an extant house sparrow Passer domesticus. (a) Histogram of oil droplet size. (b) Kernel density estimation of (a). (c) Result of number of modes (k) and p-values.

Fig. 12.

Fig. 12

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Frequency distribution of the cross-sectional area of oil droplets of an extant Ural owl Strix uralensis. (a) Histogram of oil droplet size. (b) Kernel density estimation of (a). (c) Result of number of modes (k) and p-values.

Table 6.

Area of oil droplets in an extant Ural owl Strix uralensis. The area of each oil droplet and its cone type were determined based on the literature given in Gondo and Ando (1995).

No. Cone type Area of oil droplet (μm2) No. Cone type Area of oil droplet (μm2)
1 pale green 5.2 69 pale green 6.8
2 " 6.0 70 " 5.5
3 " 5.4 71 " 6.5
4 " 5.6 72 " 5.6
5 " 6.3 73 " 7.7
6 " 5.8 74 " 6.3
7 " 6.2 75 " 5.9
8 " 7.0 76 " 7.3
9 " 5.8 77 " 6.9
10 " 6.5 78 " 5.2
11 " 4.1 79 " 7.1
12 " 4.9 80 " 6.8
13 " 5.8 81 " 6.6
14 " 5.2 82 " 6.8
15 " 6.9 83 " 5.3
16 " 6.3 84 " 4.4
17 " 6.0 85 " 4.9
18 " 7.2 86 " 6.8
19 " 8.2 87 " 6.8
20 " 6.2 88 " 6.8
21 " 7.3 89 " 3.5
22 " 6.3 90 " 8.1
23 " 6.7 91 " 6.2
24 " 6.2 92 " 5.0
25 " 7.5 93 " 6.4
26 " 6.0 94 " 6.3
27 " 5.8 95 " 6.1
28 " 5.7 96 " 5.8
29 " 6.7 97 " 6.3
30 " 6.4 98 " 6.5
31 " 5.5 99 " 6.7
32 " 5.9 100 " 6.5
33 " 5.2 101 " 8.0
34 " 4.7 102 " 6.8
35 " 6.6 103 " 7.1
36 " 7.5 104 " 6.9
37 " 4.9 105 " 6.3
38 " 6.7 106 " 6.7
39 " 5.4 107 " 6.0
40 " 6.0 108 " 5.5
41 " 5.4 109 " 5.5
42 " 6.1 110 " 8.3
43 " 6.3 111 " 8.4
44 " 5.8 112 " 6.8
45 " 6.0 113 " 6.4
46 " 6.7 114 " 7.1
47 " 6.7 115 " 6.1
48 " 5.0 116 " 6.6
49 " 6.1 117 " 6.7
50 " 7.2 118 " 7.0
51 " 7.0 119 " 6.1
52 " 6.6 120 " 6.3
53 " 6.7 121 " 6.6
54 " 6.3 122 " 6.5
55 " 7.4 123 " 6.4
56 " 7.9 124 " 5.4
57 " 6.4 125 " 6.0
58 " 6.0 126 " 6.1
59 " 6.7 127 " 5.8
60 " 6.3 128 " 6.7
61 " 6.9 129 " 6.5
62 " 6.5 130 " 6.5
63 " 8.2 131 " 6.8
64 " 7.2 132 " 6.1
65 " 6.0 133 " 5.4
66 " 6.5 134 " 4.3
67 " 6.8 135 " 7.2
68 " 6.1
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As inferred from the opsin genes of extant species, tetrachromatic vision first evolved in jawless fish (Bowmaker, 2008). In reptiles and birds, the performance of cone cells is further enhanced by the addition of oil droplets which transmit specific wavelengths only (Stavenga and Wilts, 2014; Loew et al., 2002). Thus, the discovery of oil droplets in the fossil bird specimen here indicates that the complex optical system of cone cells had already been achieved at least by 120 Ma.

On the other hand, single-coloured oil droplets are found in the snowy owl and king penguin (Gondo and Ando, 1995). The snowy owl and king penguin inhabit snow-covered terrain, or water with a high content of blue light, and so the discrimination of multiple colours is not a selection pressure. A single oil droplet type, or filter, is as efficient at detecting objects against such a background as are multiple colour filters.

To conclude, from an examination of its retina, the Cretaceous enantiornithine bird studied here was probably a diurnal species and possessed colour vision. The frequency distribution analysis of oil droplets in the fossil bird eye appears a useful method to aid the reconstruction of its palaeoecology.

Declarations

Author contribution statement

Gengo Tanaka: Conceived and designed the experiments; Performed the experiments; Analyzed and interpreted the data; Contributed reagents, materials, analysis tools or data; Wrote the paper.

Baochun Zhou: Performed the experiments; Analyzed and interpreted the data; Contributed reagents, materials, analysis tools or data; Wrote the paper.

Yunfei Zhang: Contributed reagents, materials, analysis tools or data; Wrote the paper.

David J. Siveter: Analyzed and interpreted the data; Wrote the paper.

Andrew R. Parker: Conceived and designed the experiments; Analyzed and interpreted the data; Wrote the paper.

Competing interest statement

The authors declare no conflict of interest.

Funding statement

This work is supported by the MEXT KAKENHI (Grant no. 16K05592 to Gengo Tanaka); it is also partly supported by the Shanghai Municipal Natural Science Foundation (Grant no. 14ZR1427600 to Baochun Zhou).

Additional information

No additional information is available for this paper.

Acknowledgments

Yasuhisa Henmi and Motohiro Shimanaga (Kumamoto University) kindly provided experimental facilities. B. Z. and Y. Z. thank Xiaoming Wang (Shanghai Science and Technology Museum) for continuous support. Zhonghe Zhou (Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Science), Yuguang Zhang (Beijing Museum of Natural History) and Dongyu Hu (Shenyang Normal University) helpfully commented on the identification of the fossil bird specimen.

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