Elsevier

Journal of Biomechanics

Volume 47, Issue 2, 22 January 2014, Pages 497-504
Journal of Biomechanics

The exoskeletal structure and tensile loading behavior of an ant neck joint

https://doi.org/10.1016/j.jbiomech.2013.10.053Get rights and content

Abstract

Insects have evolved mechanical form and function over millions of years. Ants, in particular, can lift and carry heavy loads relative to their body mass. Loads are lifted with the mouthparts, transferred through the neck joint to the thorax, and distributed over six legs and tarsi (feet) that anchor to the supporting surface. While previous research has explored attachment mechanisms of the tarsi, little is known about the relation between the mechanical function and the structural design and material properties of the ant. This study focuses on the neck – the single joint that withstands the full load capacity. We combine mechanical testing, computed tomography (CT), scanning electron microscopy (SEM), and computational modeling to better understand the mechanical structure–function relation of the neck joint of the ant species Formica exsectoides (Allegheny mound ant). Our mechanical testing results show that the soft tissue forming the neck joint of F. exsectoides exhibits an elastic modulus of 230±140 MPa and can withstand ~5000 times the ant's weight. We developed a 3-dimensional (3D) model of the structural components of the neck joint for simulation of mechanical behavior. Finite element (FE) simulations reveal the neck-to-head transition where the soft membrane material meets the hard exoskeleton as the critical point for failure of the neck joint, which is consistent with our experiments. Our results further indicate that the neck joint structure exhibits anisotropic mechanical behavior with the highest stiffness occurring when the load path is aligned with the axis of the neck.

Introduction

Insect joints are mechanically distinct from vertebrate joints. Where vertebrates employ stiff components with physical constraints (i.e. ball and socket), insect body and limb segments are connected by soft, membraneous material of varying geometries (Wootton, 1999) to allow for motion. Despite having joints comprised of soft materials, ants are capable of carrying relatively heavy loads. For example, as shown in Fig. 1A and B, Wojtusiak recorded a weaver ant, Oecophylla longinoda (Latreille, 1802), holding a 7 g dead bird, ~1200 times the mass of the ant. Previous work to evaluate the load bearing capabilities of ants, in particular, has focused on attachment mechanisms and performance of the tarsi (feet) and arolium (Federle et al., 2000, Dirks, 2011), and on cooperative retrieval of large prey by multiple species (Yamamoto et al., 2009). This study seeks to relate the mechanical function of the ant, specifically the neck joint, to the material and structural design.

Previous research investigated the mechanical behavior and composite structure of insect cuticle (Barth, 1973, Dalingwater, 1975, Vincent and Wegst, 2004, Lease and Wolf, 2010, Lomakin et al., 2011, Burrows and Sutton, 2012). This work has focused on the composite nature (i.e. fiber reinforcement or laminate structure) or material properties of hard exoskeleton typically using techniques, like nano-indentation, that test local material properties or tensile testing that requires physical or chemical processing of the sample. A few studies have related material properties to functional insect behavior. For example, the physical properties, including layer hardness and fiber orientation, of the gula of beetles in the genus Pachnoda reduce friction during articulation and improve functional toughness (Barbakadze et al., 2006, Muller et al., 2008, Gorb et al., 2002). Previous work relevant to the other specialized materials are species dependent and include characterization of locust inter-segmental membrane (Hepburn and Chandler, 1976), caterpillar integument (Lin et al., 2009), blowfly wings (Ganguli et al., 2010), cockroach trachea (Webster, 2011), and the study of surface structures in files (Gorb, 1997a, Gorb, 2004). Beyond mechanically characterizing cuticle, studies have investigated kinematics of insect locomotion such as walking (Reinhardt et al., 2009, Lipp et al., 2005), swimming (Bohn et al., 2012), flight (Wakeling and Ellington, 1997, Wooton, 1981, Wooton et al., 2003, Wootton, 2009), or jumping (S. Gorb, 2004). However, the relation between the function of insect joints and their mechanical design is largely unexplored.

This work examines the neck of the Allegheny mound ant, Formica exsectoides (Forel, 1886). The neck is the single joint that withstands the full load capacity of the ant. It is comprised of a soft membraneous region bridging stiff exoskeleton of the head and thorax (Fig. 1C). We present an integrative approach of experimentally testing and modeling the mechanical function of the neck joint for intact, live specimens. 3D structural models of internal and external anatomy were created using microCT and used to simulate loading behavior and identify deformation and failure mechanisms.

Section snippets

Insects

Formica exsectoides specimens were collected in Columbus, Ohio and maintained in our lab. Insects were fed fresh mealworms and honey water solution three times per week.

Mechanical tensile tests

Live ant specimens were tested in a custom-built, open centrifuge (Fig. 2A) following previous investigations of attachment forces of arboreal ants (Federle et al., 2000). Based on Wojtusiak (1995), we used 7 g as the minimum performance requirement for the centrifuge. The minimum speed of the centrifuge was calculated using the

Morphology of the neck joint

MicroCT segmentation produced detailed 3D structural models of external and internal features of the neck (Fig. 5), including the tentorium and esophagus, which has a soft, cuticular lining similar to the neck membrane. Mouthparts were omitted from the model for simplicity. Neck membrane was separated from the hard exoskeleton of the head and thorax according to material density (see Fig. 4C); the tentorium was labeled as a continuous structure with the head. ScanIP software was used to measure

Neck mechanical behavior

Experimental and FE results show a positive correlation between displacement and applied loading direction. The simulations reveal that the displacement at lower loads can be attributed to rigid body rotation of the body relative to the head (see FE loading animation in Supplementary materials). The increase in displacement from loading at 0–45° captures the spread in the experimental data. The load angle of two specimens was measured directly after loading (Fig. 9A). The load vs. displacement

Conflict of interest statement

The authors have no conflict of interest.

Acknowledgments

We thank Dr. John Wenzel, Director of the Center for Biodiversity and Ecosystems at the Carnegie Museum of Natural History, and Dr. Joseph Raczkowski of The Ohio State University Department of Entomology for useful insight. We also thank Dr. Noriko Katsube for her mechanics expertise and feedback, Dr. Richard Hart for MicroCT access, and SimpleWare Ltd. for support.

This work was supported in part by The Ohio State University Institute for Materials Research and an NSF graduate research

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