Abstract
Animals highly depend on their sensory organs to detect information about their surrounding environment. Among animal sensory organs, those of insects have a notable ability to detect information despite their small size, which might be, therefore, one of the reasons for the evolutionary success of insects. However, insect sensory organs are seldom fossilized in sediments due to their small size and fragility. A potential solution for this problem is the study of exceptionally well-preserved fossil material from amber. Unfortunately, the resolution of existing non-destructive analysis is insufficient to observe details of these micro sensory organs even with amber preservation. Here, we focus on the analysis of the micro sensory organs of an extinct male cockroach (Huablattula hui Qiu et al., 2019) in Cretaceous amber by combining destructive and non-destructive methods. Compared to extant species inhabiting dark environments, H. hui has relatively large compound eyes, and all the antennal sensilla for detecting multimodal information observed here are fewer or smaller. The characteristics of these sensory organs support the diurnality of the bright habitats of H. hui in contrast to many extant cockroaches. Like extant male mantises, grooved basiconic type sensilla exist abundantly on the antenna of the fossilized specimen. The abundance of grooved basiconic sensilla in mantid males results from using sex pheromones, and therefore, H. hui may have likewise used mantis-like intersexual communication. These lines of evidence suggest that the ecology and behavior of Cretaceous cockroaches were more diverse than those of related extant species.
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Data availability
The fossil materials are deposited in the American Museum of Natural History under the assigned number AMNH Bu-SY28. The micro-CT slice images are available from the Figshare Data Repository: https://figshare.com/articles/figure/_CT_slice_image/14601189.
References
Allen LE, Barry KL, Holwell GI (2012) Mate location and antennal morphology in the praying mantid Hierodula majuscula. Aust J Entomol 51:133–140. https://doi.org/10.1111/j.1440-6055.2011.00843.x
Barden P, Herhold HW, Grimaldi DA (2017) A new genus of hell ants from the Cretaceous (Hymenoptera: Formicidae: Haidomyrmecini) with a novel head structure. Syst Entomol 42:837–846. https://doi.org/10.1111/syen.12253
Beccaloni G, Eggleton P (2013) Order blattodea. Zootaxa 3703:46–48. https://doi.org/10.11646/zootaxa.3703.1.10
Bell WJ, Roth LM, Nalepa CA (2007) Cockroaches: ecology, behavior, and natural history. The Johns Hopkins University Press, Baltimore
Bland RG, Slaney DP, Weinstein P (1998) Antennal sensilla on cave species of Australian Paratemnopteryx cockroaches (Blattaria: Blattellidae). Int J Insect Morphol Embryol 27:83–93
Buschbeck EK, Friedrich M (2008) Evolution of insect eyes: tales of ancient heritage, deconstruction, reconstruction, remodeling, and recycling. Evol Educ Outreach 1:448–462. https://doi.org/10.1007/s12052-008-0086-z
Butler R (1973) The anatomy of the compound eye of Periplaneta americana L. - 2. Fine Structure J Comp Physiol 83:239–262. https://doi.org/10.1007/BF00693677
Carle T, Toh Y, Yamawaki Y et al (2014) The antennal sensilla of the praying mantis Tenodera aridifolia: a new flagellar partition based on the antennal macro-, micro- and ultrastructures. Arthropod Struct Dev 43:103–116. https://doi.org/10.1016/j.asd.2013.10.005
Cruickshank RD, Ko K (2003) Geology of an amber locality in the Hukawng Valley, Northern Myanmar. J Asian Earth Sci 21:441–455. https://doi.org/10.1016/S1367-9120(02)00044-5
Ehmer B, Gronenberg W (1997) Proprioceptors and fast antennal reflexes in the ant Odontomachus (Formicidae, Ponerinae). Cell Tissue Res 290:153–165. https://doi.org/10.1007/s004410050917
Engel MS, Grimaldi DA (2004) New light shed on the oldest insect. Nature 427:627–630. https://doi.org/10.1038/nature02291
Evangelista DA, Wipfler B, Béthoux O et al (2019) An integrative phylogenomic approach illuminates the evolutionary history of cockroaches and termites (Blattodea). Proc R Soc B Biol Sci 286:20182076. https://doi.org/10.1098/rspb.2018.2076
Faucheux MJ (2008) Antennal sensilla of the male praying mantid Oxyothespis maroccana Bolivar, 1908 (Insecta: Mantodea: Mantidae): distribution and functional implications. Bull L’institut Sci Rabat Sect Sci La Vie 30:29–36
Faucheux MJ (2009) Sensory and glandular structures on the antennae of Mantis religiosa, Iris aratoria and Rivetina baetica : sexual dimorphism, physiological implications (Mantodea: Mantidae). Bull R Belgian Inst Nat Sci - Entomol 79:231–242
Fujiwara T, Kazawa T, Sakurai T et al (2014) Odorant concentration differentiator for intermittent olfactory signals. J Neurosci 34:16581–16593. https://doi.org/10.1523/JNEUROSCI.2319-14.2014
Fukuda K, Yanagawa A, Tuda M et al (2016) Sexual difference in antennal sensilla abundance, density and size in Callosobruchus rhodesianus (Coleoptera: Chrysomelidae: Bruchinae). Appl Entomol Zool 51:641–651. https://doi.org/10.1007/s13355-016-0441-4
Gao T, Shih C, Labandeira CC et al (2016) Convergent evolution of ramified antennae in insect lineages from the early cretaceous of Northeastern China. Proc R Soc B Biol Sci 283:20161448. https://doi.org/10.1098/rspb.2016.1448
Guo M, **ng L, Wang B et al (2017) A catalogue of Burmite inclusions. Zool Syst 42:249–379. https://doi.org/10.11865/zs.201715
Holwell GI, Barry KL, Herberstein ME (2007) Mate location, antennal morphology, and ecology in two praying mantids (Insecta: Mantodea). Biol J Linn Soc 91:307–313. https://doi.org/10.1111/j.1095-8312.2007.00788.x
Hörnig M, Haug C, Schneider J, Haug J (2018) Evolution of reproductive strategies in dictyopteran insects – clues from ovipositor morphology of extinct roachoids. Acta Palaeontol Pol 63. https://doi.org/10.4202/app.00324.2016
Ishii S (1971) Structure and function of the antenna of the German cockroach, Blattera germanica (L.) (Orthoptera: Blattelidae). Appl Entomol Zool 6:192–197
Keil TA (1997) Functional morphology of insect mechanoreceptors. Microsc Res Tech 39:506–531. https://doi.org/10.1002/(SICI)1097-0029(19971215)39:6%3c506::AID-JEMT5%3e3.0.CO;2-B
Krogmann L, Engel MS, Bechly G, Nel A (2013) Lower Cretaceous origin of long-distance mate finding behaviour in Hymenoptera (Insecta). J Syst Palaeontol 11:83–89. https://doi.org/10.1080/14772019.2012.693954
Labandeira CC (2014) Amber Paleontol Soc Pap 20:163–217. https://doi.org/10.1017/s1089332600002850
Lambin M (1973) Les sensilles de l’antenne chez quelques blattes et en particulier chez Blaberus craniifer (Burm.). Z Zellforsch Mikrosk Anat 143:183–206
Lindgren J, Nilsson DE, Sjövall P et al (2019) Fossil insect eyes shed light on trilobite optics and the arthropod pigment screen. Nature 573:122–125. https://doi.org/10.1038/s41586-019-1473-z
Mao Y, Liang K, Su Y et al (2018) Various amberground marine animals on Burmese amber with discussions on its age. Palaeoentomology 1:91–103. https://doi.org/10.11646/palaeoentomology.1.1.11
Martínez-Delclòs X, Briggs DEG, Peñalver E (2004) Taphonomy of insects in carbonates and amber. Palaeogeogr Palaeoclimatol Palaeoecol 203:19–64. https://doi.org/10.1016/S0031-0182(03)00643-6
Mishra M, Meyer-Rochow VB (2008) Fine structural description of the compound eye of the madagascar “hissing cockroach” Gromphadorhina portentosa (dictyoptera: blaberidae). Insect Sci 15:179–192. https://doi.org/10.1111/j.1744-7917.2008.00199.x
Missbach C, Dweck HKM, Vogel H et al (2014) Evolution of insect olfactory receptors. Elife 3:e02115. https://doi.org/10.7554/eLife.02115
Mizunami M, Yokohari F, Takahata M (1999) Exploration into the adaptive design of the arthropod “microbrain.” Zool Sci 16:703–709. https://doi.org/10.2108/zsj.16.703
Nalepa CA, Maekawa K, Shimada K et al (2008) Altricial development in subsocial wood-feeding cockroaches. Zool Sci 25:1190–1198. https://doi.org/10.2108/zsj.25.1190
Nishino H, Nishikawa M, Mizunami M, Yokohari F (2009) Functional and topographic segregation of glomeruli revealed by local staining of antennal sensory neurons in the honeybee Apis mellifera. J Comp Neurol 515:161–180. https://doi.org/10.1002/cne.22064
Perreau M, Tafforeau P (2011) Virtual dissection using phase-contrast X-ray synchrotron microtomography: reducing the gap between fossils and extant species. Syst Entomol 36:573–580. https://doi.org/10.1111/j.1365-3113.2011.00573.x
Pohl H, Wipfler B, Grimaldi D et al (2010) Reconstructing the anatomy of the 42-million-year-old fossil †Mengea tertiaria (Insecta, Strepsiptera). Naturwissenschaften 97:855–859. https://doi.org/10.1007/s00114-010-0703-x
Qiu L, Wang ZQ, Che YL (2019) First record of Blattulidae from mid-Cretaceous Burmese amber (Insecta: Dictyoptera). Cretac Res 99:281–290. https://doi.org/10.1016/j.cretres.2019.03.011
Riesgo-Escovar JR, Piekos WB, Carlson JR (1997) The Drosophila antenna: ultrastructural and physiological studies in wild-type and lozenge mutants. J Comp Physiol A 180:151–160. https://doi.org/10.1007/s003590050036
Ross AJ (2020) Burmese (Myanmar) amber taxa, on-line supplement v.2020.1. 1–25. https://www.nms.ac.uk/explore-our-collections/stories/natural-sciences/burmese-amber/. Accessed 1 July 2020
Sass H (1983) Production, release and effectiveness of two female sex pheromone components of Periplaneta americana. J Comp Physiol A 152:309–317. https://doi.org/10.1007/BF00606237
Schafer R (1971) Antennal sense organs of the cockroach, Leucophaea maderae. J Morphol 91–103
Schaller L (1982) Structural and functional classification of antennal sensilla of the cockroach, Leucophaea maderae. Cell Tissue Res 225:129–142. https://doi.org/10.1007/BF00216223
Scheffers BR, Joppa LN, Pimm SL, Laurance WF (2012) What we know and don’t know about Earth’s missing biodiversity. Trends Ecol Evol 27:501–510. https://doi.org/10.1016/j.tree.2012.05.008
Sendi H, Hinkelman J, Vršanská L et al (2020a) Roach nectarivory, gymnosperm and earliest flower pollination evidence from Cretaceous ambers. Biologia 75:1613–1630. https://doi.org/10.2478/s11756-019-00412-x
Sendi H, Vršanský P, Podstrelená L et al (2020b) Nocticolid cockroaches are the only known dinosaur age cave survivors. Gondwana Res 82:288–298. https://doi.org/10.1016/j.gr.2020.01.002
Shi G, Grimaldi DA, Harlow GE et al (2012) Age constraint on Burmese amber based on U-Pb dating of zircons. Cretac Res 37:155–163. https://doi.org/10.1016/j.cretres.2012.03.014
Steinbrecht RA, Laue M, Ziegelberger G (1995) Immunolocalization of pheromone-binding protein and general odorant-binding protein in olfactory sensilla of the silk moths Antheraea and Bombyx. Cell Tissue Res 282:203–217. https://doi.org/10.1007/BF00319112
Stork NE (2018) How many species of insects and other terrestrial arthropods are there on Earth? Annu Rev Entomol 63:31–45. https://doi.org/10.1146/annurev-ento-020117-043348
Streinzer M, Huber W, Spaethe J (2016) Body size limits dim-light foraging activity in stingless bees (Apidae: Meliponini). J Comp Physiol A 202:643–655. https://doi.org/10.1007/s00359-016-1118-8
Tanaka G, Parker AR, Siveter DJ et al (2009) An exceptionally well-preserved Eocene dolichopodid fly eye: function and evolutionary significance. Proc R Soc B Biol Sci 276:1015–1019. https://doi.org/10.1098/rspb.2008.1467
Toh Y (1977) Fine structure of antennal sense organs of the male cockroach, Periplaneta americana. J Ultrastruct Res 60:373–394. https://doi.org/10.1016/S0022-5320(77)80021-X
van Hateren JH, Srinivasan MV, Wait PB (1990) Pattern recognition in bees: orientation discrimination. J Comp Physiol A 167:649–654. https://doi.org/10.1007/BF00192658
Vidlička L, Vršanský P, Kúdelová T et al (2017) New genus and species of cavernicolous cockroach (Blattaria, Nocticolidae) from Vietnam. Zootaxa 4232:361–375. https://doi.org/10.11646/zootaxa.4232.3.5
Vršanský P (1997) Piniblattella gen. nov. the most ancient genus of the family Blattellidae (Blattodea) from the Lower Cretaceous of Siberia. Entomol Probl 28:67–79
Vršanský P (2003) Umenocoleoidea — an amazing lineage of aberrant insects (Insecta, Blattaria). AMBA Proj 7:1–32
Vršanský P, Bechly G (2015) New predatory cockroaches (Insecta: Blattaria: Manipulatoridae fam.n.) from the Upper Cretaceous Myanmar amber. Geol Carpathica 66:133–138. https://doi.org/10.1515/geoca-2015-0015
Vršanský P, Quicke DLJ, Rasnitsyn AP et al (2001) The oldest fossil insect sensilla. Publ AMBA/B/21013/ABS/D 1–8
Vršanský P, Oruzinský R, Aristov D et al (2017) Temporary deleterious mass mutations relate to originations of cockroach families. Biology 72:886–912. https://doi.org/10.1515/biolog-2017-0096
Vršanský P, Sendi H, Hinkelman J, Hain M (2021) Alienopterix Mlynský et al., 2018 complex in North Myanmar amber supports Umenocoleoidea/ae status. Biologia 76:2207–2224. https://doi.org/10.1007/s11756-021-00689-x
Watanabe H, Haupt SS, Nishino H et al (2012) Sensillum-specific, topographic projection patterns of olfactory receptor neurons in the antennal lobe of the cockroach Periplaneta americana. J Comp Neurol 520:1687–1701. https://doi.org/10.1002/cne.23007
Watanabe H, Koike Y, Tateishi K et al (2018) Two types of sensory proliferation patterns underlie the formation of spatially tuned olfactory receptive fields in the cockroach Periplaneta americana. J Comp Neurol 526:2683–2705. https://doi.org/10.1002/cne.24524
Yu T, Kelly R, Mu L et al (2019) An ammonite trapped in Burmese amber. Proc Natl Acad Sci U S A 166:11345–11350. https://doi.org/10.1073/pnas.1821292116
Yuvaraj JK, Andersson MN, Anderbrant O, Löfstedt C (2018) Diversity of olfactory structures: a comparative study of antennal sensilla in Trichoptera and Lepidoptera. Micron 111:9–18. https://doi.org/10.1016/j.micron.2018.05.006
Acknowledgements
We thank Dr. Jörg Mutterlose (Ruhr Univ. Bochum) for proofreading the article; Kosuke Tateishi (Fukuoka Univ.) for helpful comment in discussion; Dr. Yoshifumi Yamawaki (Kyushu Univ.) for providing the extant mantis material; Dr. David A. Grimaldi (the American Museum of Natural History) for curating the fossil specimen; Kosuke Nakamura (Hokkaido Univ.) for preparing the thin section; and Kentaro Kobayashi (Nikon Imaging Center) and Noritaka Saito (Tomakomai Industrial Technology Center) for assistance with LSCM and X-ray CT analysis, respectively.
Funding
This work was supported by the Kuribayashi Scholarship and Academic Foundation (2020–2-6) to R. T., the Japan Society for the Promotion of Science (JP20J00159) to S. Y., and the Japan Society for the Promotion of Science (19H02010) and the Canon Foundation (2019–4) to Y. I.
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R. T. and Y. I. designed the study. R. T. prepared and photographed the fossil material. H. W. obtained the images of the extant materials. R. T., H. N., and H. W. discussed the results. R. T. drafted the manuscript, to which H. N., H. W., S. Y., and Y. I. contributed to writing and editing. All authors gave final approval for publication and agree to be held accountable for the content therein.
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Taniguchi, R., Nishino, H., Watanabe, H. et al. Reconstructing the ecology of a Cretaceous cockroach: destructive and high-resolution imaging of its micro sensory organs. Sci Nat 108, 45 (2021). https://doi.org/10.1007/s00114-021-01755-9
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DOI: https://doi.org/10.1007/s00114-021-01755-9