Jaw Morphology and Fighting Forces in Stag Beetles Jana Goyens1,2,*, Joris Dirckx2 and Peter Aerts1,3

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Jaw Morphology and Fighting Forces in Stag Beetles Jana Goyens1,2,*, Joris Dirckx2 and Peter Aerts1,3 © 2016. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2016) 219, 2955-2961 doi:10.1242/jeb.141614 RESEARCH ARTICLE Jaw morphology and fighting forces in stag beetles Jana Goyens1,2,*, Joris Dirckx2 and Peter Aerts1,3 ABSTRACT large and heavy musculature to bite their rivals forcefully. The jaws of different species of stag beetles show a large variety of Concomitantly, species with high bite forces probably needed to shapes and sizes. The male jaws are used as weapons in fights, and evolve a more robust jaw morphology to enable them to take a firm they may exert a very forceful bite in some species. We investigated in grip on rivals and to avoid mechanical failure (Goyens et al., 2015a). 16 species whether and how the forcefulness of their bite is reflected In sexually dimorphic stag beetle species, males with larger jaws in their jaw morphology. We found a large range of maximal muscle have higher mating rates than males with smaller jaws (Harvey and forces (1.8–33 N; factor of 18). Species investing in large bite muscles Gange, 2006; Lagarde et al., 2005; Okada and Hasegawa, 2005; also have disproportionately large jaw volumes. They use this Okada and Miyatake, 2006; Shiokawa and Iwahashi, 2000). Owing additional jaw volume to elongate their jaws, increasing their to their longer jaws, they can reach further forward in aggressive chances of winning in battles. The fact that this also decreases the battles to grab their opponent and to detach him from the substrate mechanical advantage is largely compensated for by elongated in- (Goyens et al., 2015b). Once detached, the opponent is pushed away ’ levers. As a result, high muscle forces are correlated with elevated or lifted above the winner s head and thrown backwards onto the bite forces (0.27–7.6 N; factor of 28). Despite the large difference in substrate (Goyens et al., 2015b; Shiokawa and Iwahashi, 2000). In ’ the forcefulness of their bite, all investigated species experience addition to the stag beetles jaws being elongated, their enlarged similar Von Mises stresses in their jaws while biting (29–114 MPa; jaw-closer muscles enable high bite forces (Goyens et al., 2014a; factor of 4.0; calculated with finite element simulations). Hence, stag Shiokawa and Iwahashi, 2000). In turn, these high bite forces beetles have successfully adapted their jaw anatomy according to probably require jaws that are robust against bending (Goyens et al., their bite force in fights. 2014b,c). However, these adaptations of stag beetle weaponry come at a cost. First, there are the direct locomotion costs of running and KEY WORDS: Lucanidae, Finite element analysis, Bite force, Animal flying with heavy weapons (the energy cost increases by 38% and weaponry, Mechanical advantage, Jaw length 26%, respectively, in Cyclommatus metallifer males compared with females of the same species; Goyens et al., 2015d,e). Second, stag INTRODUCTION beetles are holometabolous insects, and the growing mandibles have Animal weapons often show a high morphological diversity. This is to compete with other body parts for resources in the pupa (Kawano, exemplified by the jaws of stag beetles, the antlers of cervids and the 1997; Knell et al., 2004). horns of bovids and beetles. The diversification of beetle horns was In this study, we compared the weapon morphology of 16 probably stimulated by the different costs horns pose depending on stag beetle species with a wide range of jaw anatomies and the species’ ecology. For example, horns at the front of the head are associated muscle sizes (see Fig. 1). By combining finite element rare in nocturnal species because they are correlated with smaller (FE) analysis with measurements of bite muscle size, we examined eyes and, therefore, reduced vision (Emlen, 2001). However, for whether and how the jaw morphology of these 16 species is adapted most families, it remains unknown what exactly caused this to withstand deformations while biting. We hypothesized that stag evolutionary diversification (Emlen, 2008), and an in-depth beetles have adapted their jaw morphology according to their bite understanding of the functional morphology of these weapons is force, and that this prevents elevated material stresses that might essential to gain insight into this process. Stag beetles (family cause structural failure in the jaws of species with a more forceful Lucanidae) are an interesting model animal in this regard. Not only bite. do they display a remarkable diversity in the size and shape of male weapons (varying from small, indistinct jaws to impressive jaws that MATERIALS AND METHODS are longer than the rest of the body; see Fig. 1) but also their bite Micro-computed tomography (CT) scans forces are probably equally diverse (considering the range of head We obtained adult male stag beetles of 16 species from nine sizes; see Fig. 1). Hence, the stag beetle family may comprise an different genera, with a large variety of jaw sizes and shapes (see interesting range of different morphological strategies. Depending Fig. 1): Cyclommatus lunifer Boileau 1905 (specimen 1), on their specific fight behaviour, species may need long jaws or Cyclommatus metallifer (Boisduval 1835) (specimen 2a), Dorcus jaws with a specific shape. Furthermore, they may have invested in alcides Vollenhoven 1865 (specimen 3), Dorcus bucephalus (MacLeay 1819) (specimen 4), Dorcus parryi (Boileau 1902) 1University of Antwerp, Laboratory of Functional Morphology, Universiteitsplein 1, (specimen 5), Dorcus titanus (Boisduval 1835) (specimen 6), Antwerp 2610, Belgium. 2University of Antwerp, Laboratory of Biophysics and Hexarthrius parryi Hope 1842 (specimen 7), Lamprima adolphinae BioMedical Physics, Groenenborgerlaan 171, Antwerp 2020, Belgium. 3Ghent (Gestro 1875) (specimen 8), Lucanus cervus (Linneaus 1758) University, Department of Movement and Sport Sciences, Watersportlaan 2, Ghent 2000, Belgium. (specimen 9), Nigidius obesus Parry 1864 (specimen 10), Prismognathus davidis Deyrolle 1878 (specimen 11), *Author for correspondence ( [email protected]) Prosopocoilus bison (Olivier 1789) (specimen 12), Prosopocoilus J.G., 0000-0003-0176-884X giraffa Olivier 1789 (specimen 13), Prosopocoilus mohnikei Parry 1873 (specimen 14), Prosopocoilus senegalensis (Latreille Received 7 April 2016; Accepted 15 July 2016 1817) (specimen 15) and Pseudorhaetus oberthuri Planet 1899 Journal of Experimental Biology 2955 RESEARCH ARTICLE Journal of Experimental Biology (2016) 219, 2955-2961 doi:10.1242/jeb.141614 Fig. 1. Pictures of the heads of the stag beetle specimens used in this study. All specimens are male beetles of a different species, except for specimen 2b. All photos are shown at the same magnification. The scale bar indicates 5 mm. (specimen 16). Further, we acquired a female C. metallifer created and smoothed out a triangulated surface mesh of the individual (specimen 2b). All specimens were purchased from head and calculated its area. Using this head surface area, we authorized commercial dealers (The Pet Factory Germany, www. calculated the muscle force with the muscle stress (muscle force thepetfactory.de; The Bugmaniac, www.thebugmaniac.com; per PCSA) that was previously determined for C. metallifer stag Kingdom of Beetle Taiwan, screw-wholesale.myweb.hinet.net), beetles (Goyens et al., 2014a). This assumes that all species are except for the dead specimen of L. cervus, which was collected in capable of developing the same maximal muscle stress, which is a France [collaboration with Research Institute for Nature and Forest reasonable assumption because muscle stress in C. metallifer males (INBO), permission reference BL/FF-SB 09-03188]. These species is almost identical to that of females (which are not adapted for are not listed on CITES appendices (checklist.cites.org). Except for fighting; 18 and 17 N cm−2, respectively; Goyens et al., 2014a). the L. cervus and C. metallifer specimens, all specimens were dried. Because we only used the morphology of the exoskeleton in our FE simulations of jaw biting analyses, our results are not affected by shrinkage of soft tissue The FE method is a numerical method that can be used for the because of drying. We made micro-CT scans of the male specimens structural analysis of (complex) loaded structures. These structures with a Skyscan 1172 high resolution micro-CT scanner (Bruker are subdivided into a large number of small elements (a mesh), for micro-CT, Kontich, Belgium). The female specimen was scanned by which stresses (Von Mises stresses), strains and displacements are the Centre for X-ray Tomography of Ghent University. The micro- calculated (Bright, 2014; Dumont et al., 2009; Rayfield, 2007). CT scanners were operated at voltages of 59–120 kV and currents of Using the same method that we used to create the surface meshes 117–200 µA, which resulted in a resolution of 11–13 µm. of the heads, we also made surface models of the jaw cuticle for all 16 species. Based on these surface models, we calculated jaw cuticle Bite muscles volume, jaw length (out-lever, hinge–jaw tip) and input lever arm Ross et al. (2005) demonstrated that muscle forces can be applied in length (in-lever, hinge–muscle attachment on jaw; see Fig. 2) in FE analyses by estimating their overall force amplitude from the Amira. By multiplying the muscle force by the mechanical physiological cross-sectional area (PCSA) of the muscle (Ross advantage (in-lever divided by jaw length), we estimated the et al., 2005). For stag beetle bite muscles (i.e. closer muscles of the specimens’ bite forces (Goyens et al., 2014a; Mills et al., 2016). We jaws), the PCSA can be approximated by examining the attachment established scaling relationships between morphological variables area of the muscles on the head (Goyens et al., 2014a). The closer after log–log transformation with the reduced major axis. The muscles diverge from the jaw to the head capsule and have the shape measured slope was considered to be significantly different from the of a 3D cone (Goyens et al., 2014a).
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