Aposematic coloration from Mid-Cretaceous Kachin amber

Abstract

Aposematic coloration is among the most diverse antipredator strategies, which can signal unpleasantness of organisms to potential predators and reduce the probability of predation. Unlike mimesis, aposematic coloration allows organisms to warn their predators away by conspicuous and recognizable colour patterns. However, aposematism has been a regular puzzle, especially as the long-term history of such traits is obscured by an insufficient fossil record. Here, we report the discovery of aposematic coloration in an orthopteran nymph from Mid-Cretaceous Kachin amber (99 million years old). It is attributed to the extinct family Elcanidae and erected as a new genus identified by conspicuous dark/light-striped coloration, four apical spurs on the metatibia, a two-segmented metatarsus and unsegmented stylus. It represents the first fossil orthopteran preserved with aposematic coloration from the Mesozoic, demonstrating that orthopterans had evolved aposematism by the Mid-Cretaceous. Our findings provide novel insights into the early evolution of anti-predator strategies among orthopterans. Together with mimesis, debris-carrying camouflage and aposematism previously reported, our findings demonstrate the relative complexity of prey–predator interactions in the Mesozoic, especially in the Mid-Cretaceous Kachin amber forest.

This article is part of the theme issue ‘The impact of Chinese palaeontology on evolutionary research’.

1. Introduction

Antipredator strategies are prevalent in the biological world, which usually help organisms to avoid detection by predators (e.g. crypsis, plant mimicry and debris-carrying camouflage) or avoid attack after being detected (e.g. aposematism and deimatism) [1]. Aposematism commonly occurs in poisonous or thorny organisms, advertising their unpalatably or inedibility to other animals by signals such as eye-catching coloration, conspicuous sounds or distinct odours [1–5]. A diverse range of organisms have evolved with these traits, including invertebrates, vertebrates and plants, e.g. stinging wasps with black–yellow stripes, toxic poisonous frogs with bright yellow or red coloration and prickly roses with brilliant coloration [4,6–8]. Since the function of conspicuous coloration in toxic lepidopteran larvae and its value was observed by Charles Darwin and Alfred Wallace [9], however, the origin and early evolution of aposematism have been far from clear owing to limited fossil finds. Among the advertising signals, aposematic sounds and odours are extremely difficult to reconstruct and identify, and to date, few insects with aposematic coloration having been reported from the Mesozoic, and more investigation is needed [10,11].

Here, we report a new orthopteran nymph with conspicuous aposematic coloration from Mid-Cretaceous Kachin amber (approx. 99 million years old). Our new find reveals the earliest fossil record of aposematic Orthoptera and demonstrates complex prey–predator interactions in the Mid-Cretaceous forest ecosystem.

2. Material and methods

(a) . Material and deposits

The amber specimen (NIGP181000) described in this paper is housed in the Nanjing Institute of Geology and Palaeontology (NIGP), Chinese Academy of Sciences. The type specimen NIGP181000 is preserved in an oval piece of yellow amber from Mid-Cretaceous Kachin amber (from northern Myanmar), about 32.2 mm maximum length, 25.3 mm maximum width and 6.0 mm maximum thickness. Kachin amber (amber from northern Myanmar) contains the most diverse biota in amber from the Cretaceous [12,13]. Our specimen is from the Angbamo site located in the Kachin Province of northern Myanmar. U–Pb dating of zircons from the volcanoclastic matrix of the amber gave a maximum age of 98.8 ± 0.6 Ma [14], which is also supported by an ammonite trapped in amber [15].

(b) . Imaging and abbreviations

Observations were made using an Olympus SZX7 microscope initially, and then photomicrographs were taken using a Zeiss Stereo Discovery V16 microscope system with ZEN software. Amber pieces were immersed in cedar wood oil in order to reduce image distortion and unwanted reflection when taking photographs through irregularly curved surfaces of the amber. Photographs were stacked using Helicon software in depth-map mode. The figures were prepared with CorelDraw X7 and Adobe Photoshop CC.

General morphological abbreviations are as follow: com, compound eyes; sc, scape; pe, pedicel; flg, flagellomere; mp, maxillary palpus; lc, lacinia; fe, femur; ti, tibia; tar, tarsus; dds, dorsal denticles (spines) on metatibia; ds, spine-like dorsal spur on metatibia; das, metatibial apical spur; vds, ventral denticles (spines) on metabasitarsus; ce, cercus; sty, stylus; I–III, pro-, meso-, metathoracic legs; 1–3, basitarsus, second tarsomere, third tarsomere.

3. Systematic palaeontology

Class Insecta Linnaeus, 1758

Order Orthoptera Olivier, 1789

Superfamily Elcanoidea Handlirsch, 1906

Family Elcanidae Handlirsch, 1906

Genus Monitelcana gen. nov.

Type species. Monitelcana penalveri sp. nov.; here designated.

Etymology. The genus name is a combination of monit- and Elcana.

Diagnosis. Head: compound eyes prominent, with interocular distance approximately equal to the diameter of eyes; ocelli absent; no interspace between two scapes; left lacinia with three apical denticles. Pronotum: with no transverse fold or sulci, only covering base of abdomen. Thoracic legs: pro- and mesofemur with four or five spine-shaped apical lobes; pro- and mesotarsus with two apical spines on basitarsus and second tarsomere; protibia with two apical lobes and two apical spines; metatibia with lobate spine-like spurs on dorsal margin curved along medial edge (right tibia with three pairs, left tibia with three pairs and a proximal single spur); metatibia with four apical spurs; metatarsus two-segmented; distal half of metabasitarsus with two rows of stout denticles (spines) on ventral margin. Abdomen: stylus unsegmented.

Monitelcana penalveri sp. nov.

(figures 1–3)

Figure 1.

Photographs of Monitelcana penalveri gen. et sp. nov. (NIGP181000) from Mid-Cretaceous Kachin amber. (a) Habitus in dorsolateral view. (b) Habitus in ventrolateral view. (c) Photograph of aposematic katydid genus Vestria exhibiting similar aposematic coloration (courtesy of Sebastián Vizcarra). Scale bars: (a,b), 2 mm.

Figure 3.

Details of Monitelcana penalveri gen. et sp. nov. (NIGP181000). (a) Left metathoracic leg. (b) Right metathoracic leg. (c) Right metatarsus. (d) Genitalia. Scale bars: (a,b) 1 mm, (c,d) 0.5 mm.

Etymology. The specific epithet is in honour of Dr Enrique Peñalver (IGME, Madrid) in recognition of his significant contribution to our knowledge of Elcanidae.

Diagnosis. As for genus.

Holotype. NIGP181000 (nymph, male).

Type locality and horizon. Kachin (Hukawng Valley) of northern Myanmar, 98.79 ± 0.62 Ma, Mid-Cretaceous [14].

Description. Head (figure 2a,b): Hypognathous, distinctly vertical; dorsoventrally elongate, approximately triangular in frontal view. Vertex short, with sparse setae. Frons flat, without setae; frontoclypeal sulcus developed, situated medially on face. Compound eyes large and prominent, with no setae, situated high on head capsule; interocular distance approximately equal to diameter of eyes; ocular suture and ocelli absent. Antennae inserted between compound eyes; scape sturdy with dense tiny setae, medial part slightly sunken and gourd-like, with no interspace between two scapes; pedicel distinctly slender and shorter than scape, about one-quarter and two-thirds of scape length and width respectively; flagellum filiform with at least 100 segments, two–four stout setae situated between flagellomeres. Maxillary palpus pentamerous, five segments nearly equal in length; lacinia well developed, left one with three apical denticles. Labial palpus obscured, only apical segment visible.

Figure 2.

Details of Monitelcana penalveri gen. et sp. nov. (NIGP181000). (a) Head and pronotum in dorsolateral view. (b) Head in ventrolateral view. (c) Right prothoracic leg. (d) Left prothoracic leg. (e) Genicular structure of left prothoracic leg. (f) Left mesothoracic leg. Scale bars: (a–f) 0.5 mm.

Thorax (figure 2a). Pronotum large, distinctly saddle shaped with partial setal cover and with a thin rim present on distal part of posterior margin; no transverse fold or sulcus; narrow dorsally and broad laterally, slightly fastigate, covering base of abdomen and curved laterally to approximate level of basal margin of coxae.

Prothoracic leg (figure 2c–e). Coxa robust, with a process partly covering trochanter. Trochanter cylindroid, short and slender, about two times as long as wide, with a process slightly covering femur. Femur slightly thinner than trochanter, covered with dense tiny setae and four non-articulated apical lobes, two larger ones on mesal margin and two minute ones (almost stout spines) on dorsal margin. Tibia more slender than femur, with dense tiny setae and two rows of stout, denticle-like setae on ventral margin; cross-section pentagonal not quadrate, with two non-articulated elongate apical lobes ventrally and two non-articulated minute apical spines dorsally. Tarsus inserted between two apical tibial lobes, dorsoventrally depressed, three-segmented; basitarsus relatively sturdy, with two rows of stout, denticle-like setae and two apical spines on ventral margin; second tarsomere short, about one-third of basitarsus in length, with rows of stout setae and two apical spines (nearly equal to second tarsomere in length) on ventral margin; third tarsomere slightly longer than basitarsus, slightly curved and armed with two long curved claws.

Mesothoracic leg (figure 2f). Coxa not visible. Trochanter short and sturdy, with a process partly covering femur. Femur distinctly more slender than trochanter, of relatively uniform thickness along its length, with covering of dense tiny setae and with five non-articulated apical lobes, three minute ones (almost stout spines) on dorsal margin and two larger ones on mesal margin. Tibia more slender than femur, with covering of dense tiny setae; cross-section quadrate, with two rows of setae on dorsal margin and two rows of denticle-like setae on ventral margin, with two long non-articulated apical spines on ventral margin. Tarsus inserted above two tibial apical spines, three-segmented; basitarsus relatively sturdy, with two rows of stout setae and two non-articulated apical spines on ventral margin; second tarsomere short, about one-quarter of basitarsus in length, with rows of stout setae and two non-articulated apical spines (nearly equal to second tarsomere in length) on ventral margin; third tarsomere longer than basitarsus, slightly curved, armed with two long curved claws.

Metathoracic leg (figure 3a–c). Coxa and trochanter not visible. Femur distinctly inflated, typically orthopteroid, covered with a dense series of stout setae, with eight fine apical spines on dorsal margin, five on each lateral margin. Tibia more slender than femur, with a covering of dense tiny setae and two rows of setae on ventral margin; also with two rows of minute denticles (spines); with several spine-like spurs on dorsal margin, lobate with a median edge and curve along it, margin with denticle-like setae (right tibia with three pairs, left tibia with three pairs and a proximal single spur); and with four non-articulated apical spurs, two dorsal ones long, about two times as long as ventral ones. Tarsus two-segmented; basitarsus relatively sturdy, with two rows of stout setae and a distinct apical spine on dorsal margin, distal half of metabasitarsus with two rows of stout denticles (spines) on ventral margin; second tarsomere shorter than basitarsus in length, strongly curved, with two rows of setae on ventral margin and armed with two long curved claws.

Abdomen (figure 3d). Short and slender, with long setae on the dorsal surface and on sternites; flattened laterally, with eight segments visible. Ninth sternite with pair of thin and long styli; stylus unsegmented with distal long setae. Pair of long dorsal cerci present, sturdier and shorter than styli, base pedicel-like, with long and fine erect setae, including rather long apical setae.

Coloration (figure 1a). Yellow body covered with two brown marks and several black stripes: two almost symmetrical brown marks on vertex; a wide black transverse stripe on pronotum (width 1.38 mm), anterior margin (2.94 mm) along with pronotum anterior margin and posterior margin (0.57 mm) strictly parallel to pronotum posterior margin, forming an inverted trapezoid; a relatively narrow black transverse stripe on pronotum (width 0.72 mm), anterior and posterior margins (4.72 mm) parallel to posterior margin of pronotum; a black transverse stripe (width 0.63 mm) on base of abdomen (about tergites 2 and 3), partly obscured by pronotum; relatively narrow stripe (width 0.58 mm) on posterior of abdomen (about tergites 6, 7 and 8); two oblique stripes on metafemora symmetrically, which can be definitely identified as aposematism. Distance between first and second stripe on pronotum 0.91 mm; width of combination with second stripe on pronotum and first stripe on abdomen 1.25 mm; distance between first and second stripe on abdomen 0.80 mm.

Measurements (in millimetres). Body length 7.50 (excluding antennae). Head height 1.99 dorsoventrally, length 0.54; scape length 0.99, width 0.41, pedicel length 0.29, width 0.25; compound eyes height 0.96, interocular distance 1.11. Prothoracic leg length: femur 2.19; tibia 2.27; tarsus 1.61, basitarsus 0.74, second tarsomere 0.17, third tarsomere 0.70. Mesothoracic leg: femur 2.09; tibia 2.75; tarsus 1.55, basitarsus 0.65, second tarsomere 0.16, third tarsomere 0.74. Metathoracic leg: femur length 6.01, maximal width 1.84; tibia 6.25; tarsus 2.77, basitarsus 1.80, second tarsomere 0.97.

4. Discussion

(a) . Phylogenetic position of Monitelcana gen. nov.

Displaying a morphological combination of features in Caelifera and Ensifera, the extinct family Elcanidae is nevertheless assigned to the Ensifera owing to the long antennae and nymphal characteristics [16–18]. To date, 208 records in 51 species and 17 genera have been reported from the Triassic of America, the Jurassic of Asia and Europe, the Cretaceous of Asia, Europe and Latin America and the Mid-Palaeocene of France [19–21]. Monitelcana gen. nov. can be reliably attributed to Elcanidae based on the following characteristics: prominent compound eyes, long antennae, three-segmented tarsi, saltatorial hind legs, three pairs of distinctive lobate spine-like spurs on metatibia and presence of long, slender paired styli.

The relatively large head and pronotum compared with body size, absence of wings and rudimentary short cerci suggest that the insect is a nymph and early instar. Therefore comparison with adpressions bearing wings is impossible, and only five genera preserved three-dimensionally in amber are suitable for comparison: Longioculus Poinar, Gorochov et Buckley, 2007, Burmelcana Peñalver et Grimaldi, 2010, Elcanonympha Heads et Thomas, 2018 and Ellca Kočárek, 2020 from Mid-Cretaceous Kachin amber, and Hispanelcana Peñalver et Grimaldi, 2010 from Lower Cretaceous Álava amber (northern Spain) [17,22–24]. Monitelcana gen. nov. resembles Hispanelcana in the following characteristics: lacinia with apical denticles, metatibia with four non-articulated apical spurs, metatarsus two-segmented and styli present. However, it differs from Hispanelcana in having two apical spines on the pro- and mesobasitarsus (two apical spurs in Hispanelcana), two apical spines on basitarsus and second tarsomere of pro- and mesotarsus (one apical spur in Hispanelcana), metatibia with lobate spine-like and apically sharp spurs on dorsal margin (spine-like spurs, paddle-shaped and apically rounded in Hispanelcana). The new genus is mainly distinguished from the other four genera in having four and five spine-shaped apical lobes on the pro- and mesofemur, protibia with two apical lobes and two apical spines, metatibia with four apical spurs, metatarsus two-segmented and distal half of metabasitarsus with two rows of stout denticles (spines) on ventral margin. Therefore, a new genus is established.

(b) . Antipredator strategy in fossil orthopteran: aposematism or mimicry?

Monitelcana gen. nov. exhibits a conspicuous coloration: yellow body with two almost symmetrical brown marks on the vertex, two black transverse stripes on the pronotum, two black transverse stripes on the abdomen and two symmetrical oblique black stripes on the metafemora (figure 4). Though the original coloration of the body is almost lost owing to the preservation, it was obviously light-coloured, probably green or yellow, according to extant relatives (katydids and crickets). Having paid the cost of high risk of being detected and attacked, this conspicuous coloration pattern presumably benefited much more in other aspects. The overall appearance of Monitelcana, black stripes distributed on the green or yellow body, mimics that of extant wasps. Though wasp-mimicry exists among extant ensiferans [25], e.g. Aganacris Walker, 1871 mimicing Pepsis Fabricius, 1805, this explanation is illogical for the following reasons: (i) there exists a size difference between Monitelcana and wasps from Mid-Cretaceous Kachin amber; (ii) no wasp model with black stripes on a light body has been reported from Mid-Cretaceous Kachin amber; (iii) Monitelcana is a wingless nymph and faces different predation pressures from flying wasps. Additionally, black stripes also work as disruptive crypsis in insects, including orthopterans, which can make the detection of edges and boundaries more difficult by creating false boundaries in places where no real boundary occurs [1,26,27]. To conceal the insect body effectively, disruptive crypsis is commonly exhibited as very narrow black longitudinal or irregular stripes on orthopteran dorsa, along the axis of the body [28]. Stripes of Monitelcana are transverse and wide, neither narrow nor longitudinal enough to create false boundaries. Therefore, this conspicuous coloration is unlikely to be disruptive crypsis.

Figure 4.

Reconstruction of aposematic orthopteran nymph, Monitelcana penalveri gen. et sp. nov. (NIGP181000).

Excluding the possibility of wasp-mimicry and disruptive crypsis, it is more likely that this colour pattern is an aposematic coloration. First, a dark–light-striped pattern in Monitelcana is a rather effective aposematic signal among insects which can facilitate detection and also presumably speed up avoidance learning [27,29]. Light colours are eye-catching, and black can also enhance the optical contrast against green foliage and resists light transfer in the background [4,27]. Besides, Monitelcana is apparently spiny, armed with plenty of spines on pro-, meso- and metathoracic legs. Spines and denticles on legs are capable of increasing the inedibility due to stabbing or kicking of predators, and are common in orthopterans [30–32]. Therefore, Monitelcana may have avoided attack by predators through advertising the inedibility of the spines. In addition to physical defence, chemical defences are also commonly advertised by aposematic signals as unprofitable or inedibile among orthopterans [33–35]. Thereby, aposematic coloration of Monitelcana might also be associated with poison or distastefulness, which characteristics have already appeared in Mid-Cretaceous Kachin amber [10].

Extant orthopterans often exhibit aposematic coloration, such as in warning-coloured lubber grasshoppers (Romaleidae), which cause emesis in lizard and bird predators, gaudy grasshoppers (Pyrgomorphidae), which are capable of ejecting distasteful chemicals, and dark–light-striped Crayola katydids, which can produce glandular odorants (genus Vestria Stål, 1874) [26,35–37]. Such aposematism can also be found among orthopterans in early instars, demonstrating it is an important element in the whole life history of orthopterans [26,35]. However, compared with plant-like mimesis and crypsis [25,38], aposematism rarely occurs among extant ensiferans. In fact, plant-like mimesis is an ancient survival strategy in prey–predator interaction that dates back to the Permian, while no aposematism has been reported in the fossil record during the evolutionary history of ensiferans [39–41]. The presence of aposematic coloration in Monitelcana penalveri gen. et sp. nov., which is uniformly distributed on the whole body irrespective of different organs, implies that aposematic coloration was an important survival strategy for ensiferans in the Cretaceous. Our find of an elcanid nymph from the Mid-Cretaceous Kachin amber also suggests that, for the first time, orthopterans had evolved aposematism by the Mid-Cretaceous.

(c) . Antipredator adaptations in the Mesozoic

Fossil insects are usually preserved as adpressions or inclusions without lighter pigment colour [42]; structural colour is also infrequently discovered in fossil insects owing to the incomplete preservation of ultrastructure [43–46]. Though three-dimensional insects are preserved in amber, colour has been rarely recorded [47–50]. Thus, the early evolution of aposematism is poorly understood and only observed from simple colour patterns caused by colour differences. The oldest record of aposematism dates back to the Carboniferous, and it relatively flourished during the Cenozoic [43,51]. In Mesozoic ecosystems, aposematism is reported in Kalligrammatidae as adpressions or amber inclusions [52], and in Blattaria from Mid-Cretaceous Kachin amber and Early Cretaceous Lebanese amber [10,11].

In the Mesozoic, especially the Cretaceous before the fifth mass extinction, many new predaceous arthropods (including some spiders, lacewing larvae and ants) and vertebrates (including lizards, birds and mammals) were present [13], and, on the basis of fossils, insects have been reported with several antipredator adaptations. Diverse insect lineages have been discovered with debris-carrying camouflage, including Chrysopoidea, Nymphidae, Ascalaphidae, Myrmeleontidae in Neuroptera, and Reduviidae in Hemiptera [53–55]. Additionally, a wide range of insects evolved with specialized morphologies for mimesis, e.g. false stick insect (Proscopiidae) mimicking twigs with their slender abdomens [56]; adult lacewings (Chrysopoidea) mimicking pinnate-leaved plants with pinnate leaf markings, or mimicking lichen thalli with punctiform black spots [57,58]; larval lacewing mimicking liverworts with expanded lateral plates [59]; and cockroaches mimicking hymenopterans by robust morphologies [60]. Differing from these defences to avoid detection by their predators, aposematism is a secondary defence that takes effect after being detected [1]. Diverse antipredator strategies among insects demonstrate the relative complexity of prey–predator interactions in the Mesozoic, especially in the Mid-Cretaceous Kachin amber forest. The present work only reveals a tip of the iceberg of past ecosystems and more investigation is needed.

Ethics

To avoid any confusion and misunderstanding, we declare that the amber reported in this study is not involved in armed conflict and ethnic strife in Myanmar.

Data accessibility

All data supporting this article have been included in the manuscript.

Authors' contributions

C.X.: substantial contributions to conception and design, acquisition of data, analysis and interpretation of data, drafting the article critically for important intellectual content; C.L.: analysis and interpretation of data, final approval of the version to be published; E.A.J.: revising the article critically for important intellectual content; Y.F.: acquisition of data, final approval of the version to be published; B.W.: substantial contributions to conception and design, acquisition of data, final approval of the version to be published. All authors gave final approval for publication and agreed to be held accountable for the work performed herein.

Competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Funding

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB26000000), the Second Tibetan Plateau Scientific Expedition and Research (2019QZKK0706) and the National Natural Science Foundation of China (42125201, 41688103). E.A.J. thanks the Chinese Academy of Sciences for support under the President's International Fellowship Initiative (PIFI). This is a Leverhulme Emeritus Fellowship Contribution for E.A.J.