Pedipalp anatomy of the Australian black rock scorpion, Urodacus manicatus, with implications for functional morphology

Russell D. C. Bicknell; Gregory D. Edgecombe; Christopher H. R. Goatley; Glen Charlton; John R. Paterson

doi:10.1071/ZO23044

RESEARCH ARTICLE (Open Access)

Contents Vol 72(2)

Pedipalp anatomy of the Australian black rock scorpion, Urodacus manicatus, with implications for functional morphology

Russell D. C. Bicknell

^A ^B ^* , Gregory D. Edgecombe ^C , Christopher H. R. Goatley ^A ^D ^E , Glen Charlton ^F and John R. Paterson ^A

+ Author Affiliations

- Author Affiliations

^A Palaeoscience Research Centre, School of Environmental & Rural Science, University of New England, Armidale, NSW 2351, Australia.

^B Division of Paleontology (Invertebrates), American Museum of Natural History, New York, NY, 10027, USA.

^C The Natural History Museum, London SW7 5BD, UK.

^D School of Ocean and Earth Science, University of Southampton Waterfront Campus, National Oceanography Centre, Southampton, SO14 3ZH, UK.

^E Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW 2010, Australia.

^F School of Science and Technology, University of New England, Armidale, NSW 2351, Australia.

^* Correspondence to: rdcbicknell@gmail.com, rbicknell@amnh.org

Handling Editor: Paul Cooper

Australian Journal of Zoology 72, ZO23044 https://doi.org/10.1071/ZO23044

Submitted: 26 October 2023 Accepted: 5 April 2024 Published: 13 May 2024

Abstract

Pedipalps – chelate ‘pincers’ as the second pair of prosomal appendages – are a striking feature of scorpions and are employed in varied biological functions. Despite the distinctive morphology and ecological importance of these appendages, their anatomy remains underexplored. To rectify this, we examined the pedipalps of the Australian black rock scorpion, Urodacus manicatus, using a multifaceted approach consisting of microcomputed tomography, scanning electron microscopy, energy dispersive X-ray spectroscopy, and live pinch force measurements. In doing so, we document the following aspects of the pedipalps: (1) the musculature in three dimensions; (2) the cuticular microstructure, focusing on the chelae (tibial and tarsal podomeres); (3) the elemental construction of the chelae teeth; and (4) the chelae pinch force. We recognise 25 muscle groups in U. manicatus pedipalps, substantially more than previously documented in scorpions. The cuticular microstructure – endo-, meso-, and exocuticle – of U. manicatus pedipalps is shown to be similar to other scorpions and that mesocuticle reinforces the chelae for predation and burrowing. Elemental mapping of the chelae teeth highlights enrichment in calcium, chlorine, nickel, phosphorus, potassium, sodium, vanadium, and zinc, with a marked lack of carbon. These elements reinforce the teeth, increasing robustness to better enable prey capture and incapacitation. Finally, the pinch force data demonstrate that U. manicatus can exert high pinch forces (4.1 N), further highlighting the application of chelae in subduing prey, as opposed to holding prey for envenomation. We demonstrate that U. manicatus has an array of adaptions for functioning as a sit-and-wait predator that primarily uses highly reinforced chelae to process prey.

Keywords: Australia, energy dispersive X-ray spectroscopy, micro-computed tomography, microstructure, morphology, musculature, scanning electron microscopy, scorpions, Urodacus manicatus.

References

Abdel-Nabi IM, McVean A, Abdel-Rahman MA, Omran M (2004) Intraspecific diversity of morphological characters of the burrowing scorpion Scorpio maurus palmatus (Ehrenberg, 1828) in Egypt (Arachnida: Scorpionida: Scorpionidae). Serket 9(2), 41-67.
| Google Scholar |

Alexander AJ (1967) Problems of limb extension in the scorpion, Opisthophthalmus latimanus Koch. Transactions of the Royal Society of South Africa 37(3), 165-181.
| Crossref | Google Scholar |

Audouin JV (1826) Explication sommaire des planches d’arachnides de l’Egypte et de la Syrie. In ‘Description de l’Égypte’. Vol. 22. (Ed. J-C Savigny) pp. 291–430. (Histoire Naturelle: Paris)

Beck EJ (1885) Description of the muscular and endoskeletal systems of Scorpio. Transactions of the Zoological Society of London 11, 339-360.
| Google Scholar |

Becker A, Ziegler A, Epple M (2005) The mineral phase in the cuticles of two species of Crustacea consists of magnesium calcite, amorphous calcium carbonate, and amorphous calcium phosphate. Dalton Transactions 10, 1814-1820.
| Crossref | Google Scholar |

Bentov S, Palmer BA, Bar-On B, Shelef Y, Aflalo ED, Sagi A (2021) Reinforcement of bio-apatite by zinc substitution in the incisor tooth of a prawn. Acta Biomaterialia 120, 116-123.
| Crossref | Google Scholar |

Bicknell RDC, Klinkhamer AJ, Flavel RJ, Wroe S, Paterson JR (2018a) A 3D anatomical atlas of appendage musculature in the chelicerate arthropod Limulus polyphemus. PLoS ONE 13(2), e0191400.
| Crossref | Google Scholar |

Bicknell RDC, Paterson JR, Caron J-B, Skovsted CB (2018b) The gnathobasic spine microstructure of recent and Silurian chelicerates and the Cambrian artiopodan Sidneyia: functional and evolutionary implications. Arthropod Structure & Development 47(1), 12-24.
| Crossref | Google Scholar |

Bicknell RDC, Simone Y, van der Meijden A, Wroe S, Edgecombe GD, Paterson JR (2022) Biomechanical analyses of pterygotid sea scorpion chelicerae uncover predatory specialisation within eurypterids. PeerJ 10, e14515.
| Crossref | Google Scholar |

Bowerman RF, Root TM (1978) External anatomy and muscle morphology of the walking legs of the scorpion Hadrurus arizonensis. Comparative Biochemistry and Physiology Part A: Physiology 59(1), 57-63.
| Crossref | Google Scholar |

Casper GS (1985) Prey capture and stinging behavior in the emperor scorpion, Pandinus imperator (Koch) (Scorpiones, Scorpionidae). The Journal of Arachnology 13, 277-283.
| Google Scholar |

Cribb BW, Stewart A, Huang H, Truss R, Noller B, Rasch R, Zalucki MP (2008) Unique zinc mass in mandibles separates drywood termites from other groups of termites. Naturwissenschaften 95(5), 433-441.
| Crossref | Google Scholar |

Cribb BW, Lin C-L, Rintoul L, Rasch R, Hasenpusch J, Huang H (2010) Hardness in arthropod exoskeletons in the absence of transition metals. Acta Biomaterialia 6(8), 3152-3156.
| Crossref | Google Scholar |

Cunha HP, Santos AB, Foerster SÍA, Moura GJB, Lira AFA (2022) Can contrasting habitats influence predatory behavior in tropical forest scorpions? Acta Ethologica 25(2), 107-113.
| Crossref | Google Scholar |

Currey JD, Nash A, Bonfield W (1982) Calcified cuticle in the stomatopod smashing limb. Journal of Materials Science 17(7), 1939-1944.
| Crossref | Google Scholar |

Cutler B, McCutchen L (2006) Heavy metals in cuticular structures of Palpigradi, Ricinulei, and Schizomida (Arachnida). The Journal of Arachnology 34(3), 653-656.
| Crossref | Google Scholar |

Dalingwater JE (1987) Chelicerate cuticle structure. In ‘Ecophysiology of Spiders’. (Ed. W Nentwig) pp. 3–15. (Springer: Berlin)

Durale MS, Vyas AB (1968) The structure of the chela of Heterometrus sp. and its mode of operation. Bulletin of the Southern California Academy of Sciences 67(4), 240-244.
| Google Scholar |

Ehrenberg CG (1828) Phytozoa turbellaria Africana et Asiatica in Phytozoorum Tabula IV et V delineata. In ‘Symbolae physicae, seu icones et descriptiones corporum naturalium novorum aut minus cognitorum quae ex itineribus per Libyam, Aegyptium, Nubiam, Dongalam Syriam, Arabiam et Habessiniam, pars zoologica II, animalia evertebrata exclusis insectis’. (Eds FG Hemprich, CG Ehrenberg) pp. 53–67. (Officina Academica: Berolina)

Farley RD (1999) Scorpiones. In ‘Microscopic anatomy of invertebrates. Vol. 8A: Chelicerate arthropods’. (Eds FW Harrison, RF Foelix) pp. 117–222. (Wiley-Liss: New York)

Fawke JD, Mcclements JG, Wyeth P (1997) Cuticular metals: quantification and mapping by complementary techniques. Cell Biology International 21(10), 675-678.
| Crossref | Google Scholar |

Filshie BK, Hadley NF (1979) Fine structure of the cuticle of the desert scorpion, Hadrurus arizonensis. Tissue and Cell 11(2), 249-262.
| Crossref | Google Scholar |

Fontaine AR, Olsen N, Ring RA, Singla CL (1991) Cuticular metal hardening of mouthparts and claws of some forest insects of British Columbia. Journal of the Entomological Society of British Columbia 88, 45-55.
| Google Scholar |

Gainett G, Klementz BC, Setton EVW, Simian C, Iuri H, Edgecombe GD, Peretti AV, Sharma PP (2024) A plurality of morphological characters need not equate with phylogenetic accuracy: a rare genomic change refutes the placement of Solifugae and Pseudoscorpiones in Haplocnemata. Evolution and Development e12467.
| Crossref | Google Scholar |

Gallant J, Hochberg R (2017) Elemental characterization of the exoskeleton in the whipscorpions Mastigoproctus giganteus and Typopeltis dalyi (Arachnida: Thelyphonida). Invertebrate Biology 136(3), 345-359.
| Crossref | Google Scholar |

Gallant J, Hochberg R, Ada E (2016) Elemental characterization of the cuticle in the marine intertidal pseudoscorpion, Halobisium occidentale. Invertebrate Biology 135(2), 127-137.
| Crossref | Google Scholar |

Gignac PM, Kley NJ, Clarke JA, Colbert MW, Morhardt AC, Cerio D, Cost IN, Cox PG, Daza JD, Early CM, Echols MS, Henkelman RM, Herdina AN, Holliday CM, Li Z, Mahlow K, Merchant S, Müller J, Orsbon CP, Paluh DJ, Thies ML, Tsai HP, Witmer LM (2016) Diffusible iodine-based contrast-enhanced computed tomography (diceCT): an emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues. Journal of Anatomy 228, 889-909.
| Crossref | Google Scholar |

Grams M, Wirkner CS, Runge J (2018) Serial and special: comparison of podomeres and muscles in tactile vs walking legs of whip scorpions (Arachnida, Uropygi). Zoologischer Anzeiger 273, 75-101.
| Crossref | Google Scholar |

Günther A, Drack M, Monod L, Wirkner CS (2021a) A unique yet technically simple type of joint allows for the high mobility of scorpion tails. Journal of the Royal Society Interface 18(182), 20210388.
| Crossref | Google Scholar |

Günther A, Monod L, Wirkner CS (2021b) Comparative morphology of scorpion metasomata: Muscles and cuticle. Arthropod Structure & Development 60, 101003.
| Crossref | Google Scholar |

Harington A (1977) Burrowing biology of the scorpion Cheloctonus jonesii Pocock (Arachnida: Scorpionida: Scorpionidae). Journal of Arachnology 5, 243-249.
| Google Scholar |

Harvey MS, Volschenk ES (2002) A forgotten scorpion: the identity of Buthus flavicruris Rainbow, 1896 (Scorpiones), with notes on Urodacus manicatus (Thorell). Records of the Western Australian Museum 21(1), 105-106.
| Crossref | Google Scholar |

Hillerton JE, Vincent JFV (1982) The specific location of zinc in insect mandibles. Journal of Experimental Biology 101, 333-336.
| Crossref | Google Scholar |

Hillerton JE, Robertson B, Vincent JFV (1984) The presence of zinc or manganese as the predominant metal in the mandibles of adult, stored-product beetles. Journal of Stored Products Research 20(3), 133-137.
| Crossref | Google Scholar |

Holden C (1997) The environmental physiology of the scorpion Urodacus manicatus (Thorell) (Scorpionidae). PhD thesis, University of New England.

Kellersztein I, Cohen SR, Bar-On B, Wagner HD (2019) The exoskeleton of scorpions’ pincers: structure and micro-mechanical properties. Acta Biomaterialia 94, 565-573.
| Crossref | Google Scholar |

Kellersztein I, Greenfeld I, Wagner HD (2021) Structural analysis across length scales of the scorpion pincer cuticle. Bioinspiration & Biomimetics 16(2), 026013.
| Crossref | Google Scholar |

Kennaugh J (1959) An examination of the cuticles of two scorpions, Pandinus imperator and Scorpiops hardwickii. Journal of Cell Science S3-100(49), 41-50.
| Crossref | Google Scholar |

Koch CL (1837) ‘Übersicht des Arachnidensystems. Erstes Heft.’ (C. H. Zeh’schen Buchhandlung: Nürnberg)

Koch LE (1978) A comparative study of the structure, function and adaptation to different habitats of burrows in the scorpion genus Urodacus (Scorpionida, Scorpionidae). Records of the Western Australian Museum 6(2), 119-146.
| Google Scholar |

Kraepelin K (1896) Neue und weniger bekannte Scorpione. Mitteilungen aus dem Naturhistorischen Museum (Mitteilungen aus dem Naturhistorischen Museum (Beiheft zum Jahrbuch der Hamburgischen Wissenschaftlichen Anstalten) 13, 119-146.
| Google Scholar |

Krishnan G (1953) On the cuticle of the scorpion Palamneus swammerdami. Journal of Cell Science S3-94(25), 11-22.
| Crossref | Google Scholar |

Lamoral BH (1971) Predation on terrestrial molluscs by scorpions in the Kalahari Desert. Annals of the Natal Museum 21(1), 17-20.
| Google Scholar |

Lankester ER (1885) On the muscular and endoskeletal systems of Limulus and Scorpio; with some notes on the anatomy and generic characters of scorpions. The Transactions of the Zoological Society of London 11(10), 311-384.
| Crossref | Google Scholar |

Leeming J (2019) ‘Scorpions of southern Africa.’ (Penguin Random House: South Africa)

Lichtenegger HC, Schöberl T, Ruokolainen JT, Cross JO, Heald SM, Birkedal H, Waite JH, Stucky GD (2003) Zinc and mechanical prowess in the jaws of Nereis, a marine worm. Proceedings of the National Academy of Sciences 100(16), 9144-9149.
| Google Scholar |

Linnaeus C (1758) ‘Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis.’ 10 edn. (Laurentius Salvius: Holmiae)

Lowe RM, Farrell PM (2011) A portable device for the electrical extraction of scorpion venom. Toxicon 57(2), 244-247.
| Crossref | Google Scholar |

Luna-Ramirez K, Tonk M, Rahnamaeian M, Vilcinskas A (2017) Bioactivity of natural and engineered antimicrobial peptides from venom of the scorpions Urodacus yaschenkoi and U. manicatus. Toxins 9(1), 22.
| Crossref | Google Scholar |

Malek SRA (1964) A study of a scorpion cuticle: I. The structure and staining reactions of the fully formed cuticle of Buthus quinquestriatus (H. & E.). Proceedings of the Linnean Society of London 175(2), 101–116.

Mallory FB (1900) A contribution to staining methods: I. A differential stain for connective-tissue fibrillae and reticulum. II. Chloride of iron haematoxylin for nuclei and fibrin. III. Phosphotungstic acid haematoxylin for neuroglia fibres. Journal of Experimental Medicine 5(1), 15-20.
| Crossref | Google Scholar |

Manton SM (1977) ‘The Arthropoda: habits, functional morphology and evolution.’ (Oxford University Press: Oxford)

Metscher BD (2009) MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiology 9(1), 11.
| Crossref | Google Scholar |

Michalski H, Harms D, Runge J, Wirkner CS (2022) Evolutionary morphology of coxal musculature in Pseudoscorpiones (Arachnida). Arthropod Structure & Development 69, 101165.
| Crossref | Google Scholar |

Morgan TD, Baker P, Kramer KJ, Basibuyuk HH, Quicke DLJ (2003) Metals in mandibles of stored product insects: do zinc and manganese enhance the ability of larvae to infest seeds? Journal of Stored Products Research 39(1), 65-75.
| Crossref | Google Scholar |

Mutvei H (1978) SEM studies on arthropod exoskeletons II. Horseshoe crab Limulus polyphemus (L.) in comparison with extinct eurypterids and recent scorpions. Zoologica Scripta 6(3), 203-213.
| Crossref | Google Scholar |

Norton RA, Behan-Pelletier VM (1991) Calcium carbonate and calcium oxalate as cuticular hardening agents in oribatid mites (Acari: Oribatida). Canadian Journal of Zoology 69(6), 1504-1511.
| Crossref | Google Scholar |

Ontano AZ, Gainett G, Aharon S, Ballesteros JA, Benavides LR, Corbett KF, Gavish-Regev E, Harvey MS, Monsma S, Santibáñez-López CE, Setton EVW, Zehms JT, Zeh JA, Zeh DW, Sharma PP, Pupko T (2021) Taxonomic sampling and rare genomic changes overcome long-branch attraction in the phylogenetic placement of pseudoscorpions. Molecular Biology and Evolution 38(6), 2446-2467.
| Crossref | Google Scholar |

Pocock RI (1888) XX. – The species of the genus Urodacus contained in the collection of the British (Natural-History) Museum. Annals and Magazine of Natural History 2(8), 169-175.
| Crossref | Google Scholar |

Pocock RI (1898) VIII. – The Australian scorpions of the genus Urodacus, Pet. Annals and Magazine of Natural History 2(7), 59-67.
| Crossref | Google Scholar |

Politi Y, Priewasser M, Pippel E, Zaslansky P, Hartmann J, Siegel S, Li C, Barth FG, Fratzl P (2012) A spider’s fang: how to design an injection needle using chitin-based composite material. Advanced Functional Materials 22(12), 2519-2528.
| Crossref | Google Scholar |

Radosavljevic D, Ada E, Hochberg R (2021) Elemental enrichment of the exoskeleton of the whip spider Phrynus marginemaculatus (Arachnida: Amblypygi). The Journal of Arachnology 49(2), 235-249.
| Crossref | Google Scholar |

Richards AC (1951) ‘Integument of Arthropods.’ (University of Minnesota Press: Minneapolis)

Rubin M, Lamsdell JC, Prendini L, Hopkins MJ (2017) Exocuticular hyaline layer of sea scorpions and horseshoe crabs suggests cuticular fluorescence is plesiomorphic in chelicerates. Journal of Zoology 303(4), 245-253.
| Crossref | Google Scholar |

Runge J, Wirkner CS (2020) Evolutionary and functional substitution of extrinsic musculature in Solifugae (Arachnida). Journal of Morphology 281(12), 1524-1533.
| Crossref | Google Scholar |

Schmidt M, Melzer RR, Bicknell RDC (2022) Kinematics of whip spider pedipalps: a 3D comparative morpho-functional approach. Integrative Zoology 17(1), 156-167.
| Crossref | Google Scholar |

Schofield RMS (2001) Metals in cuticular structures. In ‘Scorpion biology and research.’ (Eds P Brownell, Polis G) pp. 234–256. (Oxford University Press: Oxford)

Schofield R, Lefevre H, Shaffer M (1989) Complementary microanalysis of Zn, Mn and Fe in the chelicera of spiders and scorpions using scanning MeV-ion and electron microprobes. Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms 40, 698-701.
| Crossref | Google Scholar |

Schofield RMS, Nesson MH, Richardson KA (2002) Tooth hardness increases with zinc-content in mandibles of young adult leaf-cutter ants. Naturwissenschaften 89, 579-583.
| Crossref | Google Scholar |

Schofield RMS, Nesson MH, Richardson KA, Wyeth P (2003) Zinc is incorporated into cuticular “tools” after ecdysis: The time course of the zinc distribution in “tools” and whole bodies of an ant and a scorpion. Journal of Insect Physiology 49(1), 31-44.
| Crossref | Google Scholar |

Schofield RMS, Bailey J, Coon JJ, Devaraj A, Garrett RW, Goggans MS, Hebner MG, Lee BS, Lee D, Lovern N, Ober-Singleton S, Saephan N, Seagal VR, Silver DM, Som HE, Twitchell J, Wang X, Zima JS, Nesson MH (2021) The homogenous alternative to biomineralization: Zn- and Mn-rich materials enable sharp organismal “tools” that reduce force requirements. Scientific Reports 11(1), 17481.
| Crossref | Google Scholar |

Shorthouse DJ, Marples TG (1982) The life stages and population dynamics of an arid zone scorpion Urodacus yaschenkoi (Birula 1903). Australian Journal of Ecology 7(2), 109-118.
| Crossref | Google Scholar |

Shultz JW (1989) Morphology of locomotor appendages in Arachnida: evolutionary trends and phylogenetic implications. Zoological Journal of the Linnean Society 97(1), 1-55.
| Crossref | Google Scholar |

Shultz JW (1992) Muscle firing patterns in two arachnids using different methods of propulsive leg extension. Journal of Experimental Biology 162(1), 313-329.
| Crossref | Google Scholar |

Shultz JW (2001) Gross muscular anatomy of Limulus polyphemus (Xiphosura, Chelicerata) and its bearing on evolution in the Arachnida. Journal of Arachnology 29(3), 283-303.
| Crossref | Google Scholar |

Shultz JW (2007) Morphology of the prosomal endoskeleton of Scorpiones (Arachnida) and a new hypothesis for the evolution of cuticular cephalic endoskeletons in arthropods. Arthropod Structure & Development 36(1), 77-102.
| Crossref | Google Scholar |

Simone Y, van der Meijden A (2018) Fast and fine versus strong and stout: a trade-off between chela closing force and speed across nine scorpion species. Biological Journal of the Linnean Society 123(1), 208-217.
| Crossref | Google Scholar |

Simone Y, van der Meijden A (2021) Armed stem to stinger: a review of the ecological roles of scorpion weapons. Journal of Venomous Animals and Toxins including Tropical Diseases 27, e20210002.
| Crossref | Google Scholar |

Simone Y, Chaves C, van der Meijden A, Egeter B (2022) Metabarcoding analysis of different portions of the digestive tract of scorpions (Scorpiones, Arachnida) following a controlled diet regime shows long prey DNA half-life. Environmental DNA 4(5), 1176-1186.
| Crossref | Google Scholar |

Smith GT (1966) Observations on the life history of the scorpion Urodacus abruptus (Scorpionidae), and the analysis of its home sites. Australian Journal of Zoology 14(3), 383-398.
| Crossref | Google Scholar |

Snodgrass RE (1948) The feeding organs of Arachnida, including mites and ticks. Smithsonian Miscellaneous Collections 110(10), 1-93.
| Google Scholar |

Snodgrass RE (1952) ‘A textbook of arthropod anatomy.’ (Cornell University Press: New York)

Soleglad ME, Fet V, Kovařík F (2005) The systematic position of the scorpion genera Heteroscorpion Birula, 1903 and Urodacus Peters, 1861 (Scorpiones: Scorpionoidea). Euscorpius 2005(20), 1-37.
| Crossref | Google Scholar |

Southcott RV (1955) Some observations on the biology, including mating and other behavior, of the Australian scorpion Urodacus abruptus Pocock. Transactions of the Royal Society of South Australia 78, 145-154.
| Google Scholar |

Tadayon M, Younes-Metzler O, Shelef Y, Zaslansky P, Rechels A, Berner A, Zolotoyabko E, Barth FG, Fratzl P, Bar-On B (2020) Adaptations for wear resistance and damage resilience: micromechanics of spider cuticular “tools”. Advanced Functional Materials 30(32), 2000400.
| Crossref | Google Scholar |

Thorell T (1876) I. – On the classification of scorpions. Annals and Magazine of Natural History 17(97), 1-15.
| Crossref | Google Scholar |

van der Meijden A, Kleinteich T (2017) A biomechanical view on stinger diversity in scorpions. Journal of Anatomy 230(4), 497-509.
| Crossref | Google Scholar |

van der Meijden A, Herrel A, Summers A (2010) Comparison of chela size and pincer force in scorpions; getting a first grip. Journal of Zoology 280(4), 319-325.
| Crossref | Google Scholar |

van der Meijden A, Kleinteich T, Coelho P (2012a) Packing a pinch: functional implications of chela shapes in scorpions using finite element analysis. Journal of Anatomy 220(5), 423-434.
| Crossref | Google Scholar |

van der Meijden A, Langer F, Boistel R, Vagovic P, Heethoff M (2012b) Functional morphology and bite performance of raptorial chelicerae of camel spiders (Solifugae). Journal of Experimental Biology 215(19), 3411-3418.
| Crossref | Google Scholar |

van der Meijden A, Lobo Coelho P, Sousa P, Herrel A (2013) Choose your weapon: defensive behavior is associated with morphology and performance in scorpions. PLoS ONE 8(11), e78955.
| Crossref | Google Scholar |

Vohland K, Furch K, Adis J (2003) Contrasting central Amazonian rainforests and their influence on chemical properties of the cuticle of two millipede species – a first study. Tropical Ecology 44(2), 235-241.
| Google Scholar |

Vyas AB (1970) Studies in myology of the scorpion Heterometrus fulvipes Koch. PhD Thesis, Gujarat University.

Walker SM, Schwyn DA, Mokso R, Wicklein M, Müller T, Doube M, Stampanoni M, Krapp HG, Taylor GK (2014) In vivo time-resolved microtomography reveals the mechanics of the blowfly flight motor. PLoS Biology 12(3), e1001823.
| Crossref | Google Scholar | PubMed |

Warburg MR, Rosenberg M (1994) The female reproductive system of the eastern Australian scorpion. Tissue and Cell 26(5), 779-783.
| Crossref | Google Scholar |

Wirkner CS, Prendini L (2007) Comparative morphology of the hemolymph vascular system in scorpions – A survey using corrosion casting, MicroCT, and 3D-reconstruction. Journal of Morphology 268(5), 401-413.
| Crossref | Google Scholar |

Wolf H, Harzsch S (2002) Evolution of the arthropod neuromuscular system. 1. Arrangement of muscles and innervation in the walking legs of a scorpion: Vaejovis spinigerus (Wood, 1863) Vaejovidae, Scorpiones, Arachnida. Arthropod Structure & Development 31(3), 185-202.
| Crossref | Google Scholar |

Woodman JD (2008) Living in a shallow burrow under a rock: gas exchange and water loss in an Australian scorpion. Journal of Thermal Biology 33(5), 280-286.
| Crossref | Google Scholar |

Zhang H, Kellersztein I, Freychet G, Zhernenkov M, Wagner HD, Greer JR (2023) Chemo-mechanical-microstructural coupling in the tarsus exoskeleton of the scorpion Scorpio palmatus. Acta Biomaterialia 160, 176-186.
| Crossref | Google Scholar |

Zhao Z-L, Shu T, Feng X-Q (2016) Study of biomechanical, anatomical, and physiological properties of scorpion stingers for developing biomimetic materials. Materials Science and Engineering: C 58, 1112-1121.
| Crossref | Google Scholar |