Petal-shaped femoral lobes facilitate gliding in orchid mantises

To glide in forest canopies, arboreal vertebrates evolved various skin-derived aerodynamic structures, such as patagial membranes or webbing, but no comparable structure has been reported from wingless arboreal arthropods. 1 Dudley R. Byrnes G. Yanoviak S.P. Borrell B. Brown R.M. McGuire J.A. Gliding and the functional origins of flight: biomechanical novelty or necessity?. Annu. Rev. Ecol. Evol. Syst. 2007; 38: 179-201 Crossref Scopus (146) Google Scholar ,2 Dudley R. Yanoviak S.P. Animal aloft: the origins of aerial behavior and flight. Integr. Comp. Biol. 2011; 51: 926-936 Crossref PubMed Scopus (60) Google Scholar ,3 Socha J.J. Jafari F. Munk Y. Byrnes G. How animals glide: from trajectory to morphology. Can. J. Zool. 2015; 93: 901-924 Crossref Scopus (44) Google Scholar Orchid mantises (Hymenopus coronatus) have been traditionally considered a textbook example of flower mimicry for ∼200 years due to their highly expanded, petal-shaped femoral lobes. However, the empirical evidence substantiating the petal-mimicry function of the femoral lobes has not been entirely conclusive. 4 O'Hanlon J.C. Li D. Norma-Rashid Y. Coloration and morphology of the orchid mantis Hymenopus coronatus (Mantodea: Hymenopodidae). J. Orthop. Res. 2013; 22: 35-44 Crossref Scopus (13) Google Scholar ,5 O'Hanlon J.C. Orchid mantis. Curr. Biol. 2016; 26: R145-R146 Abstract Full Text Full Text PDF PubMed Google Scholar ,6 O'Hanlon J.C. The roles of colour and shape in pollinator deception in the orchid mantis Hymenopus coronatus. Ethology. 2014; 120: 652-661 Crossref Scopus (12) Google Scholar Observational and experimental evidence suggests that these lobes do not contribute to flower mimicry for luring pollinators 6 O'Hanlon J.C. The roles of colour and shape in pollinator deception in the orchid mantis Hymenopus coronatus. Ethology. 2014; 120: 652-661 Crossref Scopus (12) Google Scholar ,7 Siedlecki M. Spadochronowy lot niektórych owadów – Der Fallschirmflug einiger Insekten. Bull. Int. Acad. Pol. Sci. Lett. 1917; ser B: 230-256 Google Scholar and likely serve other functions. 7 Siedlecki M. Spadochronowy lot niektórych owadów – Der Fallschirmflug einiger Insekten. Bull. Int. Acad. Pol. Sci. Lett. 1917; ser B: 230-256 Google Scholar ,8 Zhao X. Liu J.X. Chen Z.Q. The orchid mantis exhibits high ontogenetic colouration variety and intersexual life history differences. Evol. Ecol. 2023; 37: 569-582 Crossref Scopus (1) Google Scholar After observing their aerial escape initiated with active jumping, we hypothesized that orchid mantises can glide and that their femoral lobes are used for gliding. Through behavioral investigations and morphological analyses, we show that orchid mantis nymphs are excellent gliders, exhibiting the shallowest gliding trajectories observed in terrestrial invertebrates. 9 Yanoviak S.P. Kaspari M. Dudley R. Gliding hexapods and the origins of insect aerial behaviour. Biol. Lett. 2009; 5: 510-512 Crossref PubMed Scopus (52) Google Scholar ,10 Yanoviak S.P. Dudley R. Kaspari M. Directed aerial descent in canopy ants. Nature. 2005; 433: 624-626 Crossref PubMed Scopus (119) Google Scholar ,11 Yanoviak S.P. Munk Y. Kaspari M. Dudley R. Aerial manoeuvrability in wingless gliding ants (Cephalotes atratus). Proc. Biol. Sci. 2010; 277: 2199-2204 Crossref PubMed Scopus (39) Google Scholar ,12 Yanoviak S.P. Munk Y. Dudley R. Evolution and ecology of directed aerial descent in arboreal ants. Integr. Comp. Biol. 2011; 51: 944-956 Crossref PubMed Scopus (27) Google Scholar ,13 Yanoviak S.P. Munk Y. Dudley R. Arachnid aloft: directed aerial descent in Neotropical canopy spiders. J. R. Soc. Interface. 2015; 120534 Crossref PubMed Scopus (22) Google Scholar The lobe extensions on their femoral segments are cambered airfoils, which increase the mantis projected area by ∼36% and play a vital role in the aerodynamic underpinning of the observed gliding. Despite a 165-fold increase in body mass throughout ontogeny, older female mantis nymphs maintained a persistent gliding capability. We further showed a notable 40%–56% reduction in wing loading attributed to the positive size allometry of these lobes, indicating a clear promotion of gliding throughout ontogeny. This is the first documentation of gliding-adapted "leg wings" in a wingless arthropod. The evolution of such structures is potentially common among arboreal arthropods and demands a systematic re-examination.