The earliest tiger beetle from the Lower Cretaceous of China (Coleoptera: Cicindelinae)

Accepted Manuscript The earliest tiger beetle from the Lower Cretaceous of China (Coleoptera: Cicindelinae) Xiangdong Zhao, Xianye Zhao, Lei Chen, Bo Wang PII:

S0195-6671(18)30360-4

DOI:

https://doi.org/10.1016/j.cretres.2018.10.019

Reference:

YCRES 3996

To appear in:

Cretaceous Research

Received Date: 3 September 2018 Revised Date:

19 October 2018

Accepted Date: 21 October 2018

Please cite this article as: Zhao, X., Zhao, X., Chen, L., Wang, B., The earliest tiger beetle from the Lower Cretaceous of China (Coleoptera: Cicindelinae), Cretaceous Research (2018), doi: https:// doi.org/10.1016/j.cretres.2018.10.019. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT 1

The earliest tiger beetle from the Lower Cretaceous of China (Coleoptera:

2

Cicindelinae)

3 4

Xiangdong Zhaoa,b*,, Xianye Zhaoa,c, Lei Chena,c*, Bo Wanga,c,d

RI PT

5 6

a

7

Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment,

8

Chinese Academy of Sciences, 39 East Beijing Road, Nanjing 210008, China.

9

b

University of Science and Technology of China, Hefei 230026, China.

10

c

Shandong Provincial Key Laboratory of Depositional Mineralization & Sedimentary

11

Minerals, Shandong University of Science and Technology, Qingdao, Shandong

12

266590, China.

13

d

14

Chinese Academy of Science, Beijing 100101, China.

M AN U

SC

State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of

TE D

Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology,

15

*Corresponding authors: Xiangdong Zhao ([email protected]); Lei Chen

17

([email protected])

18

20

Abstract

AC C

19

EP

16

Fossil tiger beetles (Carabidae: Cicindelinae) are extremely rare, and little is known

21

about their early evolutionary history. Here we report the earliest known tiger beetle,

22

Cretotetracha grandis gen. et. sp. nov., from the Lower Cretaceous Yixian Formation

23

of China. C. grandis bears several features characteristic of the subtribe

24

Megacephalina, including a large body with total length/width ratio 2.3:1; labium

25

transverse, without median tooth; eyes large; eyes and head together wider than the

26

thorax; prothorax noticeably narrower than elytra; anterior corners of pronotum 1

ACCEPTED MANUSCRIPT 27

noticeably more extended anteriorly than anterior margin of prosternum. It represents

28

the second definite Mesozoic record of Cicindelinae, and extends the further lineage

29

back into the Early Cretaceous.

30

Key words: Cicindelinae, Coleoptera, Early Cretaceous, Inner Mongolia, China

RI PT

31 32

34

1.

Introduction

The Cicindelinae (tiger beetles) is a large familiar group of beetles, with

SC

33

approximately 130 genera and 2000 species (Ball, 2000; Cassola and Pearson, 2000;

36

Arndt et al., 2005; Pearson et al., 2006). The present day distribution of cicindelines is

37

worldwide except for Tasmania, Antarctica, and remote oceanic islands (Pearson,

38

1988; Cassola and Pearson, 2000). Adult cicindelines, ranging from 6 to 70 mm in

39

length, often have large bulging eyes, long, slender legs and sickle-shaped mandibles,

40

and are efficient visual predators occurring on open substrates where they forage on a

41

wide variety of small arthropods including insects, spiders, and small terrestrial

42

crustaceans (Arndt et al., 2005; Pearson et al., 2006). Many species are brilliantly

43

coloured while others are camouflaged, blending in with their habitat (Pearson, 1988).

44

Their beauty, diversity, and fearsome behaviour make them a favorite among

45

collectors worldwide (Pearson et al., 2006). Furthermore, this group is an important

46

component of the ecosystem, and provides excellent models to study ecology,

47

physiology, behaviour, phylogeny, and biogeography (e.g., Pearson, 1988; Pearson

48

and Vogler, 2001; Barraclough and Vogler, 2002; Galián et al., 2007; López-López et

49

al., 2012, 2013), thus making it one of the best studied insect groups.

AC C

EP

TE D

M AN U

35

50

Fossil Cicindelinae are very important for understanding their early evolution by

51

providing valuable information such as times of divergences and extinctions. But the

2

ACCEPTED MANUSCRIPT fossil Cicindelinae are extremely rare (Pearson, 1988; Roschmann, 1999; Cassola and

53

Werner, 2004). The Cenozoic fossil record has been reviewed by Nagano et al. (1982)

54

and Cassola and Werner (2004). Only two Mesozoic Cicindelinae fossils were

55

reported, and both are from the Lower Cretaceous Crato Formation (late Aptian) of

56

Brazil (Cassola and Werner, 2004; Wolf-Schwenninger and Schawaller, 2007).

57

Oxycheilopsis cretacicus Cassola and Werner, 2004, was erected based on a complete

58

specimen, and was attributed to the subtribe Oxycheilina (Cassola and Werner, 2004).

59

The other specimen, however, Alexcarabus megagnathus Martins-Neto, 2002,

60

probably belongs to the family Trachypachidae (Kirejtshuk and Ponomarenko, 2013).

61

In addition, Cicindelinae from the Lower Cretaceous of Liaoning, China were

62

mentioned by Kirejtshuk et al. (2010), but these fossils require formal description.

63

Thus, only one Mesozoic specimen can be confidently attributed to the Cicindelinae.

64

In this paper, we report and characterize the earliest known unambiguous fossil

65

cicindeline (subtribe Megacephalina) from the Early Cretaceous (early Aptian) of

66

China.

67

2.

TE D

M AN U

SC

RI PT

52

Material and Methods

The specimen was collected from the Lower Cretaceous Yixian Formation of

69

Yangshuwanzi Village, Bisiyingzi Township, Ningcheng County, Chifeng City, Inner

70

Mongolia, China (Fig. 1). The Lower Cretaceous Yixian Formation, widespread in

71

western Liaoning, northern Hebei and southern Inner Mongolia, is very famous for

72

yielding some of the earliest angiosperms, feathered dinosaurs, primitive birds and

73

mammals, and abundant well-preserved insects (Zhang et al., 2010). The age of the

74

Yixian Formation is restricted to 129.7-122.1 Ma (Barremian to early Aptian), and the

75

insect-bearing horizon is thought to be the Jianshangou bed (124-122.5 Ma) of the

76

Yixian Formation (Chang et al. 2009; Zhang et al. 2010). Both the Yangshuwanzi and

AC C

EP

68

3

ACCEPTED MANUSCRIPT 77

Liutiaogou fossil localities yield abundant fossil beetles dominated by a variety of

78

scarabs (Wang et al., 2012). The fossils from Yangshuwanzi are preserved in grey or

79

yellow silty mudstone, while rocks from Liutiaogou are sometimes thinner and more

80

fragile. The specimen was examined dry and under alcohol, using a Nikon SMZ1000

RI PT

81

stereomicroscope and drawings were made with the aid of a camera lucida. The

83

photographs were prepared using a digital camera (DXM1200) connected to the

84

above stereomicroscope, and the line drawings were readjusted on photographs using

85

image-editing software (CorelDraw 14.0 and Adobe Photoshop CS). In drawings,

86

dotted lines denote hidden or faintly seen parts. Body length was measured along the

87

midline from the apex of the labrum to the apex of the elytra, and width was measured

88

across the broadest part of elytra. The specimen is deposited in the Nanjing Institute

89

of Geology and Palaeontology (NIGP), Chinese Academy of Sciences.

M AN U

SC

82

91 92

3.

TE D

90

Systematic Palaeontology

We follow the phylogenetic conclusion of Pearson and Vogler (2001) in which the Cicindelinae are arranged here in five tribes: Amblycheilini, Manticorini,

94

Megacephalini, Collyridini, and Cicindelini. Terms and abbreviations for mandibles

95

follow Ball et al. (2011).

97

AC C

96

EP

93

Order Coleoptera Linnaeus, 1758 Family Carabidae Latreille, 1802

98

Subfamily Cicindelinae Latreille, 1802

99

Megacephalini Laporte, 1834

100

Subtribe Megacephalina Laporte, 1834

101

Genus Cretotetracha gen. nov.

4

ACCEPTED MANUSCRIPT 102 103 104

Derivation of name. The generic name is after the period ‘Cretaceous’, and the genus Tetracha Hope, 1838; gender neuter.

105

Type species. Cretotetracha grandis gen. et. sp. nov.; by original designation.

RI PT

106 107

109

Type horizon and locality. Lower Cretaceous Yixian Formation; Yangshuwan Village, Chifeng City, Inner Mongolia, China.

SC

108

110

Diagnosis. Medium body with total length/width ratio 2.3:1. Head with large eyes.

M AN U

111

Labium transverse, without median tooth. Mandibles sickle-shaped, with an apical

113

tooth, two terebral (incisor) teeth. Pronotum transverse, with length/width ratio 1.5:1;

114

anterior corners noticeably extended; base distinctly narrower than width of elytral

115

base. Abdomen as long as meso- and metasternum together; apex of abdomen

116

rounded. Legs long, metatibiae slightly longer than femora.

TE D

112

117

120 121

body.

EP

119

Derivation of name. Specific epithet is from Latin grandis referring to the large

AC C

118

Holotype. NIGP154997, a well-preserved beetle in ventral aspect. From

122

Yangshuwanzi Village, Bisiyingzi Township, Ningcheng County, Chifeng City, Inner

123

Mongolia, China.

124 125

Diagnosis. As for the genus.

126

5

ACCEPTED MANUSCRIPT Description. The holotype is an almost complete adult in ventral aspect (Fig. 2).

128

Body medium, length 18.2 mm, width 8.0 mm. Head and pronotum comparatively

129

short, about two-fifths of body length. Head length (including mandibles) 5.3 mm,

130

occiput width 4.6 mm. Length of head (including mandibles) 1.2 times as long as

131

occiput width. Head capsule narrowing anteriorly from base. Eyes large, convex, a

132

little longer than temples. Antennae inserted at anterior margin of eyes; scape dilated;

133

pedicellum short; first flagllomere slender, slightly longer than scape. Labium

134

distinctly transverse, without median tooth, probably with submarginal setae. Right

135

mandible approximately 4.2 mm long, left mandible approximately 3.3 mm long,

136

large, slightly incurved, with an apical tooth, two small terebral (incisor) teeth.

137

Maxillary palps longer than mandibles (Fig. 3).

M AN U

SC

RI PT

127

Pronotum transverse, length 4.3 mm, maximal width 8.0 mm, 1.9 times as wide as

139

long, widest nearly in the middle; anterior corners noticeably extended; base distinctly

140

narrower than width of elytral base. Prosternum before procoxae 1.2 times longer than

141

procoxae. Prosternal process narrow, as long as procoxae. Mesepimeron short,

142

extending to mesocoxal cavities, slightly widened laterally. Metasternum short;

143

distance between meso- and metacoxae almost as long as mesocoxal length.

144

Metepisterna subtriangular, gradually widened anteriorly. Metacoxae oblique, slightly

145

projecting over abdomen, twice as wide as long. Metacoxal plates slightly longer than

146

coxae, tapering laterally in middle. Abdomen length 8.1 mm, as long as meso- and

147

metathorax together, widened from base to apex of sternum III, then narrowing.

148

Sterna II, III, IV, VI subequal in length; sternum V shortest; last one (sternum VII)

149

approximately twice as long as the preceding one; last sternum subtriangular, 3 times

150

as wide as long. Elytra length 12.4 mm.

151

AC C

EP

TE D

138

Femora uniformly thickened; metafemora 1.1 times as long as mesofemora.

6

ACCEPTED MANUSCRIPT 152

Mesotibiae and metatibiae slender, widened apically. Mesotibial length 5.1 mm,

153

slightly longer than mesofemora. Tarsus length
1.57 mm,
1.04 mm,
0.83 mm,

154


0.82 mm,
0.73 mm. Metatrochanters nearly one-fourth as long as metafemora.

155

Mesotibial length length 6.3 mm, slightly longer than metafemora.

157

Discussion

The new specimen undoubtedly belongs to the subfamily Cicindelinae as shown by the combination of the following characters: long, sickle-shaped mandibles; simple

160

teeth arranged along the inner side of the mandible; antennae attached to the head

161

between the eye and base of the eyes mandibles; long body form with eyes and head

162

together wider than the thorax; long, thin running legs (Pearson et al., 2006).

163

Furthermore, it is attributable to the Megacephalina due to the large body with total

164

length/width ratio 2.3:1; labium transverse, without median tooth; eyes large;

165

prothorax noticeably narrower than elytra; anterior corners of pronotum noticeably

166

more extended anteriorly than anterior margin of prosternum (Pearson et al., 1999).

167

This genus resembles several genera within the subtribe Megacephalina (such as

168

Tetracha Hope and Megacephala Latreille) in the body shape, but the latter always

169

have a longer pronotum.

170

EP

TE D

M AN U

SC

159

AC C

158

4.

RI PT

156

Cretotetracha grandis sp. nov. represents the earliest record of Cicindelinae, and

171

extends the time of origin of the Megacephalina as early as the Early Cretaceous.

172

Large mandibles and long legs suggest that C. grandis was clearly a large, strong

173

predator with high running ability. Although most cicindelines (such as Cicindela) are

174

diurnal and may be out on the hottest days, basal cicindelines (such as Omus,

175

Amblycheila, Tetracha, and Megacephala) are all nocturnal (Pearson, 1988).

176

Therefore, C. grandis was probably a night-active predator too.

7

ACCEPTED MANUSCRIPT More than one hundred years ago, Gissler (1879) speculated Cicindelinae had

177 178

diverged during the Mesozoic. Our fossil provides robust evidence for his hypothesis,

179

and further suggests that Cicindelinae were well diversified by the mid-Cretaceous

180

(Pearson, 1988).

182 183

5.

RI PT

181

Concluding remarks

A new genus and species of Cicindelinae, Cretotetracha grandis gen. et. sp. nov., is described from the Lower Cretaceous Yixian Formation. C. grandis is the earliest

185

record of Cicindelinae and also the second Cretaceous specimen that can be

186

confidently attributed to the Cicindelinae. Our analyses provides evidence that

187

Cicindelinae had diverged during the Mesozoic and extends the time of origin of the

188

Megacephalina as early as the Early Cretaceous.

M AN U

SC

184

189

191

Acknowledgements.

TE D

190

We are grateful to A.G. Ponomarenko and E. Yan for their drawings and discussions on beetle taxonomy and to two anonymous reviewers for useful suggestions to the

193

manuscript. This research was supported by the Strategic Priority Research Program

194

(B) of the Chinese Academy of Sciences (XDB26000000), the National Natural

195

Science Foundation of China (41572010, 41622201, 41688103, 41502019),

196

State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of

197

Geology and Palaeontology, CAS) (No. 183101).

AC C

EP

192

and the

198 199 200 201

8

ACCEPTED MANUSCRIPT References

203

Arndt, E., Beutel, R. G., Will, K. W., 2005. Carabidae Latreille, 1802: 119-146. In

204

Beutel, R. G. and Leschen, R. A. B., (eds). Handbook of Zoology, Vol. IV

205

Arthropoda: Insecta. Part 38. Coleoptera, Vol. 1: Morphology and Systematics

206

(Archostemata, Adephaga, Myxophaga, Polyphaga (partim). Walter De Gruyter,

207

Berlin, New York, 567 pp.

208

RI PT

202

Ball, G. E., 2000. 9. Trachypachidae C. G. Thomson, 1857. 144-146. In Ross, Arnett, R. H., Jr, Thomas M. C., (eds). American Beetles, Volume I: Archostemata,

210

Myxophaga, Adephaga, Polyphaga: Staphyliniformia. CRC Press.

SC

209

Barraclough, T. G., Vogler, A. P., 2002. Recent diversification rates in North American

212

tiger beetles estimated from a dated mtDNA phylogenetic tree. Molecular Biology

213

& Evolution, 19(10):1706-1716.

214

M AN U

211

Boca Raton, Florida, 443 pp.Ball, G. E., Acorn, J. H., Shpeley, D., 2011. Mandibles and labrum-epipharynx of tiger beetles: basic structure and evolution (Coleoptera,

216

Carabidae, Cicindelidae). Zookeys: 147: 39.

TE D

215

Cassola, F., Pearson, D. L., 2000. Global patterns of tiger beetle species richness

218

(Coleoptera: Cicindelidae): their use in conservation planning. Biological

219

Conservation, 95: 197-208.

221 222 223

AC C

220

EP

217

Cassola, F., Werner, K., 2004. A fossil tiger beetle specimen from the Brazilian Mesozoic: Oxycheilopsis cretacicus n. gen., n. sp. Mitteilungen der Munchner Entomologischen Gesellschaft, 94: 75-81.

Chang, S. C., Zhang, H. C., Renne, P. R., Fang, Y., 2009. High-precision 40Ar/39Ar

224

age for the Jehol Biota. Palaeogeography, Palaeoclimatology, Palaeoecology, 280:

225

94-104.

226

Galián, J., Proença, S. J. R., Vogler, A. P., 2007. Evolutionary dynamics of

9

ACCEPTED MANUSCRIPT 227

autosomal-heterosomal rearrangements in a multiple-X chromosome system of

228

tiger Beetles (Cicindelidae). Bmc Evolutionary Biology, 7: 158.

230 231

Gissler, C. F., 1879. The Anatomy of Amblychila cylindriformis Say. Psyche A Journal of Entomology, 2: 233-244. Hope F. W., 1838. The coleopterist’s manual, part the second containing the

RI PT

229

232

predaceous land and water beetles of Linneus and Fabricius. London: H. G. Bohn,

233

xvi + 168 pp. + 3 pl.

Kirejtshuk, A. G., Ponomarenko, А. G., 2013. Taxonomical list of fossil beetles of the

SC

234

suborders Cupedina, Carabina and Scarabaeina (part 1).

236

http://www.zin.ru/animalia/coleoptera/eng/paleosy0.htm (accessed 22.08.18).

237

Kirejtshuk, A. G., Ponomarenko, A. G., Prokin, A. A., Chang, H. L., Nikolajev, G. V.,

M AN U

235

Ren, D., 2010. Current knowledge of Mesozoic Coleoptera from Daohugou and

239

Liaoning (Northeast China). Acta Geologica Sinica (English Edition), 84:

240

783-792.

243 244 245 246 247 248 249

nouveaux et observations sur leur synonomie. Méquinon-Marvis, Paris, 94 pp. Latreille, P. A., 1802. Histoire naturelle, générale et particulière des crustacés et des

EP

242

Laporte de Castelnau, F. L., 1834. Études entomologiques, ou description d’Insectes

insectes: ouvrage faisant suite auxoeuvres de Leclerc de Buffon, et partie du cours

AC C

241

TE D

238

complet d'histoire naturelle rédigé 3. De L’imprimerie de Crapelet, Paris, 467 pp.

Linnaeus, C. 1758. Systema natura per regna tria naturae secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tenth edition. Laurentius Salvius, Holmiae, 824 pp. López-López, A., Hudson, P., Galián, J., 2012. The blackburni/murchisona, species

250

complex in Australian Pseudotetracha, (Coleoptera: Carabidae: Cicindelinae:

251

Megacephalini): evaluating molecular and karyological evidence. Journal of

10

ACCEPTED MANUSCRIPT 252

Zoological Systematics & Evolutionary Research, 50:177-183.

253

López-López, A., Hudson, P., Galián, J., 2013. Recent origin of a chiasmatic sex

254

trivalent in Australian Pseudotetracha tiger beetles. Journal of Zoology, 289:

255

262-269. Martins-Neto, R. G., 2002. Insetos fósseis como bioindicadores em depósitos

RI PT

256 257

sedimentares: um estudo de caso para o Mesozóico sul-americano. Tese de

258

Doutorado, Departamento de Geologia. UNISINOS, 214 pp.

Nagano, C. D., Miller, S. E., Morgan, A. V., 1982. Fossil tiger beetles (Coleoptera:

260

Cicindelidae): review and New Quaternary Records. Psyche, 89: 339-346.

261

Pearson, D. L., 1988. Biology of tiger beetles. Annual Review of Entomology, 33:

263

M AN U

262

SC

259

123-147.

Pearson, D. L., Buestan, J., Navarrete, R., 1999. The tiger beetles of Ecuador: their identification, distribution and natural history (Coleoptera: Cicindelidae).

265

Contributions on Entomology International, 3: 189-210.

266

TE D

264

Pearson, D. L., Knisley, D. B., Kazilek, D. J., 2006. A field guide to the tiger Beetles of the United States and Canada. Identification, natural history, and distribution of

268

the Cicindelinae. Oxford University Press, 227 pp.

270 271

Pearson, D. L., Vogler, A. P., 2001. Tiger beetles: The evolution, ecology and diversity

AC C

269

EP

267

of the cicindelids. Comstock Publishing Associates (Cornell University Press), Ithaca, NY, xiii+333pp.

272

Roschmann, F., 1999. Revision of the evidence of Tetracha carolina (Coleoptera,

273

Cicindelidae) in Baltic amber (Eocene-Oligocene). Estudios del Museo de

274

Ciencias Naturales de Alava, 14: 111-120.

275 276

Wang, B., Zhang, H. C., Ponomarenko, A. G., 2012. Mesozoic Trachypachidae (Insecta: Coleoptera) from China. Palaeontology, 55: 341-353.

11

ACCEPTED MANUSCRIPT 277

Wolf-Schwenninger, K., Schawaller, W., 2007. Coleoptera: Beetles. In Martill, D.,

278

Gunter B., Loveridge R., (Eds.), The Crato fossil beds of Brazil. Cambridge:

279

Cambridge University Press, pp. 340-350.

281

Zhang, H. C., Wang, B., Fang, Y., 2010. Evolution of insects in diversity through the Jehol Biota. Science China Earth Science, 53: 1908-1917.

282 283 284

SC

285

RI PT

280

Figures

287

Fig. 1. Map showing the fossil locality, Yangshuwanzi Village, Bisiyingzi Township,

288

M AN U

286

Ningcheng County, Chifeng City, Inner Mongolia, China.

Fig. 2. Cretotetracha grandis gen. et. sp. nov., photograph and line drawing of

290

holotype NIGP154997, from the Lower Cretaceous Yixian Formation of

291

Liutiaogou. Scale bar represents 5 mm. Ma, mandible; La, labium; Sc, scape; Pe,

292

pedicel; Fl, flagellum; Ge, gena; El, elytron; ProC, procoxa; MesoC, mesocoxa;

293

MesoF, mesofemur; MesoT, mesotibia; MetaC, metacoxa; MetaF, metafemur;

294

MetaT, metatibia; MetaTa, metatarsus.

296 297 298

EP

Fig. 3. Cretotetracha grandis gen. et. sp. nov., holotype NIGP154997. A, mouthparts

AC C

295

TE D

289

in ventral aspect (with line drawing of mandibles); B, line drawing of mandibles in ventral aspect. Scale bar represents 1 mm.

12

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT