Armed stem to stinger: a review of the ecological roles of scorpion weapons

Yuri Simone Arie van der Meijden About the authors

Abstract

Scorpions possess two systems of weapons: the pincers (chelae) and the stinger (telson). These are placed on anatomically and developmentally well separated parts of the body, that is, the oral appendages and at the end of the body axis. The otherwise conserved body plan of scorpions varies most in the shape and relative dimensions of these two weapon systems, both across species and in some cases between the sexes. We review the literature on the ecological function of these two weapon systems in each of three contexts of usage: (i) predation, (ii) defense and (iii) sexual contests. In the latter context, we will also discuss their usage in mating. We first provide a comparative background for each of these contexts of usage by giving examples of other weapon systems from across the animal kingdom. Then, we discuss the pertinent aspects of the anatomy of the weapon systems, particularly those aspects relevant to their functioning in their ecological roles. The literature on the functioning and ecological role of both the chelae and the telson is discussed in detail, again organized by context of usage. Particular emphasis is given on the differences in morphology or usage between species or higher taxonomic groups, or between genders, as such cases are most insightful to understand the roles of each of the two distinct weapon systems of the scorpions and their evolutionary interactions. We aimed to synthesize the literature while minimizing conjecture, but also to point out gaps in the literature and potential future research opportunities.

Keywords:
Chelae; Scorpions; Venom delivery system; Scorpion weapons

Background

Environments where resources are limited increase the competition among their inhabitants. Gaining an advantage in access to resources over competitors raises an individual’s chances to survive and transmit its genes to the next generation. In animals, conflicts may involve a physical antagonistic struggle between individuals. The features that most define the outcome of such competitive conflicts are usually considered “weapons” [11. Emlen DJ. Animal Weapons: The evolution of battle. Blake G, editor. New York: Picador Henry Holt and Co; 2014. ]. Although many definitions of animal weapons are limited to intraspecific competitions, particularly intrasexual competitions [22. Emlen DJ. The evolution of animal weapons. Annu Rev Ecol Evol Syst. 2008 Dec 1;39:387-413.

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-77. Berglund A. Why are sexually selected weapons almost absent in females? Curr Zool. 2013 Aug;59(4):564-8. ], we will here use the broader definition of a weapon as proposed by Lane [88. Lane SM. What is a weapon? Integr Comp Biol. 2018;58:1055-63. ]. In her definition, animal weapons are features that constrain the behavior of another individual either through direct harm or other physical disruption in one or more of three fundamental contexts of usage, namely: (i) predation, (ii) defense and (iii) sexual contests. Animal weapons may thus be classified by their context of usage, but could also be organized by their mode of action, form or evolutionary history [88. Lane SM. What is a weapon? Integr Comp Biol. 2018;58:1055-63. ]. In this review, we will organize the literature on scorpion weapons by context of usage. We will first give examples of each context of usage from across the animal kingdom to provide a comparative background for the discussion of scorpion weapons.

Weapons for predation: prey capture and handling

Weapons are used in predation to seize the prey and reduce its chance to escape by restraining or incapacitating it. The grip of the restraining structures on the body of the prey may be increased by increasing friction, interlocking, penetration, or a combination thereof. Raptorial appendages are therefore often covered with spine-like structures (e.g. praying mantis [99. Prete FR. Prey capture in mantids: the role of the prothoracic tibial flexion reflex. J Insect Behav. 1990;36(5):335-8.

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-1111. Anderson PSL. Making a point: shared mechanics underlying the diversity of biological puncture. J Exp Biol. 2018 Nov 16;221(Pt 22):jeb187294. ], mantis shrimp [1111. Anderson PSL. Making a point: shared mechanics underlying the diversity of biological puncture. J Exp Biol. 2018 Nov 16;221(Pt 22):jeb187294.

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-1313. Blanco MM, Patek SN. Muscle trade-offs in a power-amplified prey capture system. Evolution. 2014 May;68(5):1399-414. ] or several orders of arachnids [1414. McLean CJ, Garwood RJ, Brassey CA. Sexual dimorphism in the Arachnid orders. PeerJ. 2018 Nov 6;6:e5751. ]). Birds that feed on flying insects often have bills with serrated edges [1515. Ornelas JF. Serrate tomia: an adaptation for nectar robbing in hummingbirds? Auk. 1994 Jan 1;111:703-10. ,1616. Gosner KL. Scopate tomia: an adaptation for handling hard-shelled prey? Wilson Bull. 1993 Jan 1;105:316-24. ]. Similarly, sharp teeth, powerful mandibles and claws allow a firm grip on prey by penetrating it [1111. Anderson PSL. Making a point: shared mechanics underlying the diversity of biological puncture. J Exp Biol. 2018 Nov 16;221(Pt 22):jeb187294. ]. Some species instead resort to chemical secretions to reduce the mobility of a prey. Secretions may be sprayed onto the body of the prey and glue it to the substrate (comprehensively reviewed in [1717. Betz O, Kolsch G. The role of adhesion in prey capture and predator defence in arthropods. Arthropod Struct Dev. 2004 Jan;33(1):3-30. ]). Other secretions, such as venoms, are injected and act on the nervous system, paralyzing or killing the victim [1818. Casewell NR, Wüster W, Vonk FJ, Harrison RA, Fry BG. Complex cocktails: The evolutionary novelty of venoms. Trends Ecol Evol. 2013 Apr;28(4):219-29. ].

Weapons for defense

The second main context of usage for animal weapons is defense. Inducing pain or other noxious experiences is one of the most efficient strategies to deter predators from pursuing their intention to assault [1919. Schmidt JO. Chemistry, pharmacology, and chemical ecology of ant venoms. In: Piek T, editor. Venoms Hymenopt. London: Academic press Inc. p. 425-508. 1986.]. To be effective, pain must be caused as quickly as possible, preferably before the predator has inflicted harm on the defending animal. Examples of active counterattacks through mechanical means are bites (most mammals [2020. Caro T. Antipredator defenses in birds and mammals. Caro T, editor. Chicago, IL: University of Chicago Press; 2005. ], squamates [2121. Green H. Antipredator mechanisms in reptiles. In: Gans C, Huey RB editors. Biology of the Reptilia Vol 16, Ecology B, Defense and Life History. New York: Alan R. Liss. p. 1-152. 1988.], arthropods [2222. Eisner T, Eisner M, Siegler M. Secret weapons: defenses of insects, spiders, scorpions, and other many-legged creatures. Michael F, editor. Harward: Harvard University Press; 2005. ]) or pinches (e.g. crustaceans [2323. Wasson K, Lyon BE. Flight or fight: flexible antipredatory strategies in porcelain crabs. Behav Ecol. 2005 Nov;16(6):1037-41. ], arachnids including scorpions [2424. van der Meijden A, Coelho PL, Sousa P, Herrel A. Choose your weapon: defensive behavior is associated with morphology and performance in scorpions. PLoS One. 2013 Nov 13;8(11):e78955. ], insects [22. Emlen DJ. The evolution of animal weapons. Annu Rev Ecol Evol Syst. 2008 Dec 1;39:387-413. ,2222. Eisner T, Eisner M, Siegler M. Secret weapons: defenses of insects, spiders, scorpions, and other many-legged creatures. Michael F, editor. Harward: Harvard University Press; 2005. ]), scratching (amphibians [2525. Blackburn DC, Hanken J, Jenkins FA. Concealed weapons: erectile claws in African frogs. Biol Lett. 2008 May 28;4:355-7. ], mammals [2020. Caro T. Antipredator defenses in birds and mammals. Caro T, editor. Chicago, IL: University of Chicago Press; 2005. ], squamates [2121. Green H. Antipredator mechanisms in reptiles. In: Gans C, Huey RB editors. Biology of the Reptilia Vol 16, Ecology B, Defense and Life History. New York: Alan R. Liss. p. 1-152. 1988.]), stabbing (e.g. ungulates [22. Emlen DJ. The evolution of animal weapons. Annu Rev Ecol Evol Syst. 2008 Dec 1;39:387-413. ,2626. Stankowich T, Caro T. Evolution of weaponry in female bovids. Proc Biol Sci. 2009 Dec 22;276(1677):4329-34. ], swordfish [2727. Penadés-Suay J, Tomás J, Aznar FJ. Fatal impalement of a blue shark Prionace glauca by a swordfish Xiphias gladius. Mediterr Mar Sci. 2017;18:340-3. ]), urticating bristles (e.g. spiders [2828. Battisti A, Holm G, Fagrell B, Larsson S. Urticating hairs in arthropods: their nature and medical significance. Annu Rev Entomol. 2011;56:203-20. ], millipedes [2222. Eisner T, Eisner M, Siegler M. Secret weapons: defenses of insects, spiders, scorpions, and other many-legged creatures. Michael F, editor. Harward: Harvard University Press; 2005. ,2929. Eisner T, Eisner M, Deyrup M. Millipede defense: use of detachable bristles to entangle ants. Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):10848-51. ]) and flagellation (e.g. squamates [2121. Green H. Antipredator mechanisms in reptiles. In: Gans C, Huey RB editors. Biology of the Reptilia Vol 16, Ecology B, Defense and Life History. New York: Alan R. Liss. p. 1-152. 1988.,3030. Arbour VM, Zanno LE. The evolution of tail weaponization in amniotes. Proc Biol Sci. 2018 Jan 31;285(1871):1-7. ]). Passive mechanical defenses may include urticating setae (e.g. lepidopteran larvae [2828. Battisti A, Holm G, Fagrell B, Larsson S. Urticating hairs in arthropods: their nature and medical significance. Annu Rev Entomol. 2011;56:203-20. ]), spines (e.g. Echinoderms [1111. Anderson PSL. Making a point: shared mechanics underlying the diversity of biological puncture. J Exp Biol. 2018 Nov 16;221(Pt 22):jeb187294. ,3131. Inbar M, Lev-Yadun S. Conspicuous and aposematic spines in the animal kingdom. Naturwissenschaften. 2005 Apr;92(4):170-2. ], mammals [1111. Anderson PSL. Making a point: shared mechanics underlying the diversity of biological puncture. J Exp Biol. 2018 Nov 16;221(Pt 22):jeb187294. ,3232. Stankowich T, Campbell LA. Living in the danger zone: exposure to predators and the evolution of spines and body armor in mammals. Evolution. 2016;70(7):1501-11. ] and fishes [1111. Anderson PSL. Making a point: shared mechanics underlying the diversity of biological puncture. J Exp Biol. 2018 Nov 16;221(Pt 22):jeb187294. ,3333. Reimchen TE. Inefficient predators and prey injuries in a population of giant stickleback. Can J Zool. 1988;66:2036-44. ]) or hard and pointed scales (e.g. squamates [3434. Broeckhoven C, Diedericks G, Mouton P le FN. What doesn’t kill you might make you stronger: functional basis for variation in body armour. J Anim Ecol. 2015 Sep;84(5):1213-21.

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-3636. Agosta SJ, Dunham AE. Comment on “How the horned lizard got its horns”. Science. 2004 Oct 8;306(5694):230. ]) that can severely harm a predator if it attempts to handle, bite or ingest it [3333. Reimchen TE. Inefficient predators and prey injuries in a population of giant stickleback. Can J Zool. 1988;66:2036-44. ,3434. Broeckhoven C, Diedericks G, Mouton P le FN. What doesn’t kill you might make you stronger: functional basis for variation in body armour. J Anim Ecol. 2015 Sep;84(5):1213-21. ], or at least increase handling time to a point to be unprofitable for the predator [3737. Pyke GH. Optimal foraging theory: a critical review. Annu Rev Ecol Syst. 1984 Nov;15:523-75. ].

Beyond causing mechanical damage, a uniquely rapid and remote way to cause pain is by electric shock (e.g. eels [3838. Catania KC. The astonishing behavior of electric eels. Front Integr Neurosci. 2019 Jul 16;13:23. ], electric rays [3939. Bennett MVL, Wurzel M, Grundfest H. The electrophysiology of electric organs of marine electric fishes: I. Properties of electroplaques of torpedo nobiliana. J Gen Physiol. 1961 Mar 1;44(4):757-804. ]). Predators can also be deterred by substances that cause pain or are otherwise noxious. Such secretions may be sprayed towards the predator/attacker, like in spitting cobras [4040. Westhoff G, Tzschätzsch K, Bleckmann H. The spitting behavior of two species of spitting cobras. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2005 Oct;191(10):873-81. ,4141. Westhoff G, Boetig M, Bleckmann H, Young BA. Target tracking during venom “spitting” by cobras. J Exp Biol. 2010 Jun 1;213(11):1797-802. ], bombardier beetles [11. Emlen DJ. Animal Weapons: The evolution of battle. Blake G, editor. New York: Picador Henry Holt and Co; 2014. ,4242. Eisner T. The protective role of the spray mechanism of the bombardier beetle, Brachynus ballistarius Lec. J Insect Physiol. 1958 Aug;2(3):215-6. ,4343. Eisner T, Meinwald J. Defensive secretions of arthropods. Science. 1966 Sep 16;153(3742):1341-50. ], vinegarroons [2222. Eisner T, Eisner M, Siegler M. Secret weapons: defenses of insects, spiders, scorpions, and other many-legged creatures. Michael F, editor. Harward: Harvard University Press; 2005. ,4444. Eisner T, Meinwald J, Monro A, Ghent R. Defence mechanisms of arthropods-I. The composition and function of the spray of the whipscorpion, Mastigoproctus giganteus (Lucas) (Arachnida, Pedipalpida). J Insect Physiol. 1961 Aug;6(4):272-98. ], scorpions [4545. Nisani Z, Hayes WK. Venom-spraying behavior of the scorpion Parabuthus transvaalicus (arachnida: Buthidae). Behav Processes. 2015 Jun;115:46-52. ,4646. Newlands G. Scorpion defensive behavior. African Wildl. 1969;23:147-53. ] and some species of millipedes [4747. Eisner T, Alsop D, Hicks K, Meinwald J. Defensive secretions of millipeds. In: Bettini S, editor. Arthropod Venoms. Springer-Verlag Berlin pubname. p. 41-72. 1978.] and ants [4848. Touchard A, Aili SR, Fox EGP, Escoubas P, Orivel J, Nicholson GM, et al. The biochemical toxin arsenal from ant venoms. Toxins. 2016 Jan;8(1):30. ]. Alternatively, noxious chemicals may be secreted from glands located on the skin, like in many amphibians [4949. Daly JW. The chemistry of poisons in amphibian skin. Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):9-13. ,5050. Nelsen DR, Nisani Z, Cooper AM, Fox GA, Gren ECK, Corbit AG, et al. Poisons, toxungens, and venoms: redefining and classifying toxic biological secretions and the organisms that employ them. Biol Rev Camb Philos Soc. 2014 May;89(2):450-65. ]. Finally, noxious secretions may be delivered into the prey’s body through specialized structures like stingers (e.g. hymenopterans [5151. Schmidt JO. Pain and lethality induced by insect stings: an exploratory and correlational study. Toxins (Basel). 2019 Jul 21;11(7):427. ], scorpions [5252. van der Meijden A, Kleinteich T. A biomechanical view on stinger diversity in scorpions. J Anat. 2017 Apr;230(4):497-509. ,5353. Zhao ZL, Shu T, Feng XQ. Study of biomechanical, anatomical, and physiological properties of scorpion stingers for developing biomimetic materials. Mater Sci Eng C Mater Biol Appl. 2016 Jan 1;58:1112-21. ] and stingrays [5454. Barbaro KC, Lira MS, Malta MB, Soares SL, Garrone Neto D, Cardoso JLC, et al. Comparative study on extracts from the tissue covering the stingers of freshwater (Potamotrygon falkneri) and marine (Dasyatis guttata) stingrays. Toxicon. 2007 Oct;50(5):676-87. ]), fangs and mouthparts (e.g. centipedes [5555. Undheim EAB, Fry BG, King GF. Centipede venom: recent discoveries and current state of knowledge. Toxins (Basel). 2015 Mar;7(3):679-704. ], spiders [5656. Foelix RF. Biology of spiders. 3rd ed. Cohen P, editor. New York: Oxford University Press; 2010. ] and snakes [5757. du Plessis A, Broeckhoven C, le Roux SG. Snake fangs: 3D morphological and mechanical analysis by microCT, simulation, and physical compression testing. Gigascience. 2018 Jan 1;7(1):1-8. ]), spines like in many fishes [1111. Anderson PSL. Making a point: shared mechanics underlying the diversity of biological puncture. J Exp Biol. 2018 Nov 16;221(Pt 22):jeb187294. ,5858. Diaz JH. Marine Scorpaenidae envenomation in travelers: epidemiology, management, and prevention. J Travel Med. 2015 Jul-Ago;22(4):251-8. ,5959. Gwee MCE, Gopalakrishnakone P, Yuen R, Khoo HE, Low KSY. A review of stonefish venoms and toxins. Pharmacol Ther. 1994;64(3):509-28. ], nettle cells in cnidarians [6060. Jouiaei M, Yanagihara AA, Madio B, Nevalainen TJ, Alewood PF, Fry BG. Ancient venom systems: a review on cnidaria toxins. Toxins (Basel). 2015 Jun;7(6):2251-71. ] and bony protrusions in amphibians [6161. Heiss E, Natchev N, Salaberger D, Gumpenberger M, Rabanser A, Weisgram J. Hurt yourself to hurt your enemy: new insights on the function of the bizarre antipredator mechanism in the salamandrid Pleurodeles waltl. J Zool. 2010;280(2):156-62. ,6262. Jared C, Mailho-Fontana PL, Antoniazzi MM, Mendes VA, Barbaro KC, Rodrigues MT, et al. Venomous frogs use heads as weapons. Curr Biol. 2015 Aug 17;25(16):2166-70. ]. In these cases, mechanical damage is augmented with a chemical agent.

Other secretions instead have the objective of repelling or confounding rather than hurting a predator. Many insects and arachnids secrete unpalatable quinone or phenolic-based substances [2222. Eisner T, Eisner M, Siegler M. Secret weapons: defenses of insects, spiders, scorpions, and other many-legged creatures. Michael F, editor. Harward: Harvard University Press; 2005. ,4343. Eisner T, Meinwald J. Defensive secretions of arthropods. Science. 1966 Sep 16;153(3742):1341-50. ]. Squamates and mustelids can release repelling secretions [6363. Sherbrooke WC, Middendorf GA. Blood-squirting variability in horned lizards (Phrynosoma). Copeia. 2001;2001(4):1114-22.

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Weapons used in sexual contests

Weapons that often develop as secondary sexual characters are used to obtain or defend reproductive resources, and/or to coerce sexual partners. In dyadic fights, morphological weapons are used in stabbing (e.g. many bovids [11. Emlen DJ. Animal Weapons: The evolution of battle. Blake G, editor. New York: Picador Henry Holt and Co; 2014. ,2626. Stankowich T, Caro T. Evolution of weaponry in female bovids. Proc Biol Sci. 2009 Dec 22;276(1677):4329-34. ,6868. Stankowich T. Armed and dangerous: predicting the presence and function of defensive weaponry in mammals. Adapt Behav. 2012 Dec 14;20:32-43.

69. Geist V. The evolution of horn-like organs. Behaviour. 1966;27:175-214.
-7070. Lundrigan B. Morphology of horns and fighting behavior in the family bovidae. J Mammal. 1996 May 17;77(2):462-75. ], narwhals [7171. Graham ZA, Garde E, Heide-Jørgensen MP, Palaoro AV. The longer the better: Evidence that narwhal tusks are sexually selected. Biol Lett. 2020 Mar 18;16:2-6. ,7272. Silverman HB, Dunbar MJ. Aggressive tusk use by the narwhal (Monodon monoceros L.). Nature. 1980 Mar 6;284:57-8. ], walruses [7373. Miller EH. Walrus ethology. I. The social role of tusks and applications of multidimensional scaling. Can J Zool. 1975;53:590-613. ], elephants [11. Emlen DJ. Animal Weapons: The evolution of battle. Blake G, editor. New York: Picador Henry Holt and Co; 2014. ], rhinoceros beetles [7474. McCullough EL, Tobalske BW, Emlen DJ, Carroll SB. Structural adaptations to diverse fighting styles in sexually selected weapons. Proc Natl Acad Sci U S A. 2014 Sep 8;111(40):14484-8. ]) ramming or pushing (many bovids [11. Emlen DJ. Animal Weapons: The evolution of battle. Blake G, editor. New York: Picador Henry Holt and Co; 2014. ,6868. Stankowich T. Armed and dangerous: predicting the presence and function of defensive weaponry in mammals. Adapt Behav. 2012 Dec 14;20:32-43.

69. Geist V. The evolution of horn-like organs. Behaviour. 1966;27:175-214.
-7070. Lundrigan B. Morphology of horns and fighting behavior in the family bovidae. J Mammal. 1996 May 17;77(2):462-75. ], dung beetles [11. Emlen DJ. Animal Weapons: The evolution of battle. Blake G, editor. New York: Picador Henry Holt and Co; 2014. ,22. Emlen DJ. The evolution of animal weapons. Annu Rev Ecol Evol Syst. 2008 Dec 1;39:387-413. ]), flipping the opponent over (e.g. stag beetles [11. Emlen DJ. Animal Weapons: The evolution of battle. Blake G, editor. New York: Picador Henry Holt and Co; 2014. ,22. Emlen DJ. The evolution of animal weapons. Annu Rev Ecol Evol Syst. 2008 Dec 1;39:387-413. ,7575. Goyens J, Dirckx J, Aerts P. Jaw morphology and fighting forces in stag beetles. J Exp Biol. 2016 Sep 15;219(Pt 18):2955-61. ], tortoises [7676. Mann GKH, O’Riain MJ, Hofmeyr MD. Shaping up to fight: sexual selection influences body shape and size in the fighting tortoise (Chersina angulata). J Zool. 2006;269:373-9. ]) or grappling (cervids [11. Emlen DJ. Animal Weapons: The evolution of battle. Blake G, editor. New York: Picador Henry Holt and Co; 2014. ,6868. Stankowich T. Armed and dangerous: predicting the presence and function of defensive weaponry in mammals. Adapt Behav. 2012 Dec 14;20:32-43.

69. Geist V. The evolution of horn-like organs. Behaviour. 1966;27:175-214.
-7070. Lundrigan B. Morphology of horns and fighting behavior in the family bovidae. J Mammal. 1996 May 17;77(2):462-75. ], crabs [7777. Levinton AJS, Allen BJ. The paradox of the weakening combatant: trade-off between closing force and gripping speed in a sexually selected combat structure. Funct Ecol. 2005;19(1):159-65. ], arachnids [1414. McLean CJ, Garwood RJ, Brassey CA. Sexual dimorphism in the Arachnid orders. PeerJ. 2018 Nov 6;6:e5751. ,7878. Tallarovic SSK. Reproductive and aggressive behaviors in the giant hairy desert scorpion [dissertation]. Corvallis, Oregon. Oregon State University; 2000. ]). The use of chemical weapons to solve intrasexual contests is particularly rare and only known in platypus [7979. Wong ESW, Papenfuss AT, Whittington CM, Warren WC, Belov K. A limited role for gene duplications in the evolution of platypus venom. Mol Biol Evol. 2012;29:167-77. ], amphipods [8080. Takeshita F, Wada S. Morphological comparison of the second gnathopod in males of four caprellid species (Amphipoda: Caprellidae). J Crustac Biol. 2012 Jul 1;32(4):673-6. ] and loris [8181. Rode-Margono JE, Nekaris KAI. Cabinet of curiosities: venom systems and their ecological function in mammals, with a focus on primates. Toxins. 2015 Jul 17;7(7):2639-58. ,8282. Nekaris KAI, Campera M, Nijman V, Birot H, Rode-Margono EJ, Fry BG, et al. Slow lorises use venom as a weapon in intraspecific competition. Curr Biol. 2020 Oct 19;30(20):R1252-3. ].

The weapons of scorpions

Scorpions belong to one of the eleven extant orders of arachnids and are easily recognizable from the other members of the arachnid class by their special set of weapons. Whereas many animals have a single weapon, scorpions possess two separate weapon systems. The pincers or pedipalps that are oral appendages located at the front of the body, and the venom-carrying stinger or telson at the caudal end of the body. Each of them has a different mode of action: mechanical and chemical, respectively. Both weapons are used in all three contexts of usage: predation, defense and sexual contests. The approximately 2,500 species currently described [8383. The Scorpion Files. https://www.ntnu.no/ub/scorpion-files/.
https://www.ntnu.no/ub/scorpion-files/...
] use these two weapon systems in different ways or to different degrees in each of the three contexts of usage, which is reflected in their morphological diversity.

Scorpions are probably among the most ancient arthropods that made a full transition from water to a land-living lifestyle [8484. Howard RJ, Edgecombe GD, Legg DA, Pisani D, Lozano-Fernandez J. Exploring the evolution and terrestrialization of scorpions (Arachnida: Scorpiones) with rocks and clocks. Org Divers Evol. 2019;19:71-86.

85. Wendruff AJ, Babcock LE, Wirkner CS, Kluessendorf J, Mikulic DG. A Silurian ancestral scorpion with fossilised internal anatomy illustrating a pathway to arachnid terrestrialisation. Sci Rep. 2020;10:20441.
-8686. Dunlop JA, Scholtz G, Selden PA. Water-to-land transitions. In: Minelli A, Boxshall G, Fusco G, editors. Arthropod Biology and Evolution. Springer, Berlin: Heidelberg. p. 417-39. 2013.]. In addition, their body plan almost did not change since the Silurian (443-419 Mya) [8787. Waddington J, Rudkin DM, Dunlop JA. A new mid-Silurian aquatic scorpion - One step closer to land? Biol Lett. 2015 Jan;11(1):20140815. ]. They successfully colonized all the continents except Antarctica, which illustrates their extraordinary capacity to adapt to different and sometimes hostile environments, and the versatility of their body plan.

Scorpion weapons

Anatomy and functioning

Knowing the inner structure of an anatomical feature is fundamental to understand its performance and limitations. In this section, we will first review the anatomy literature on the two weapons systems of scorpions: their pincers or pedipalps, and their venom delivery system consisting of the telson at the end of the flexible metasoma. Particular focus will be given to the musculoskeletal system and how it is linked with the structure’s role as a weapon in different contexts. We will only mention other, non-weapon functions, such as the sensory function of both the pedipalps and metasoma, in passing. A separate paragraph will be then dedicated to the production, composition and evolution of scorpion venom.

Overall anatomy

As in all arachnids, the scorpion body can be divided in two tagmata: prosoma and opisthosoma (Figure 1). The prosoma works functionally like a head, containing the several sensory organs and major ganglia of the nervous system. All six pairs of appendages are attached to the prosoma. The first pair is used for feeding and forms the mouth parts or chelicerae. The second pair forms the pedipalps ending in the pincers or chelae. The other four appendages are the walking legs, used for locomotion. The body beyond the prosoma, the opisthosoma, is subdivided in mesosoma and metasoma. The mesosoma is the anterior portion of the opisthosoma and contains the sexual organs, the specialized sensorial pectines, four pairs of book lungs, the cardio circulatory system, and the post-prosomal portion of the digestive tract. The metasoma is a tail-like elongation of the body containing the hindgut and carrying the venomous stinger (telson).

Figure 1.
Overall anatomy of a scorpion (Parabuthus transvaalicus, Buthidae). (A) Dorsal view. (B) Ventral view.

The pincers

The pedipalps are modified appendages developing very early in embryogenesis. Initially situated posterior to the cephalic lobes, pedipalp lobes gradually move anteriorly during the later stages of the embryonic development. After the posterior-anterior migration, the segments forming the pedipalps are recognizable [8888. Farley RD. Matrotrophic adaptations and early stages of embryogenesis in the desert scorpion Paruroctonus mesaensis (Vaejovidae). J Morphol. 1998 Sep;237(3):187-211. ,8989. Farley RD. Development of segments and appendages in embryos of the desert scorpion Paruroctonus mesaensis (Scorpiones: Vaejovidae). J Morphol. 2001 Oct;250(1):70-88. ].

The last two segments of the pedipalp, namely the manus (or tibia) and the movable finger (or tarsus) form the chela. The manus includes the fixed finger and most of the closing muscles [9090. Gilai BYA, Parnas I. Neuromuscular physiology of the closer muscles in the pedipalp of the scorpion Leiurus quinquestriatus. J Exp Biol. 1970;52(2):325-44.

91. Mathew AP. On the movable claw of the pedipalps in Heterometrus scaber. J Anim Morphol Physiol. 1965;12:271-5.
-9292. Dubale MS, Vyas AB. The structure of the chela of Heterometrus sp. and its mode of operation. Bull South Calif Acad Sci. 1968;67:240-4. ] (Figure 2). The movable finger acts as a first-class lever system; it rotates on a fixed axis formed by two joints located at the antero-ventral side of the manus, determining the axis of rotation for the opening and closing of the chela. Although scorpion musculature was first described by Lankester [9393. Lankester ER. On the muscular and endoskeletal systems of Limulus and Scorpio; with some notes on the anatomy and generic characters of scorpions. Zool Soc London. 1885;XI:311-84. ], pedipalp musculature was not included. Gilai and Parnas [9090. Gilai BYA, Parnas I. Neuromuscular physiology of the closer muscles in the pedipalp of the scorpion Leiurus quinquestriatus. J Exp Biol. 1970;52(2):325-44. ] reported the existence of three main bundles of closing muscles in the manus of Leiurus quinquestriatus (Buthidae). Dubale et al. [9292. Dubale MS, Vyas AB. The structure of the chela of Heterometrus sp. and its mode of operation. Bull South Calif Acad Sci. 1968;67:240-4. ] recognized eight muscle bundles in the “tarsus depressor” muscle of the manus in a single specimen belonging to the genus Heterometrus (Scorpionidae). Another closing muscle is located in the next proximal segment, the patella [9090. Gilai BYA, Parnas I. Neuromuscular physiology of the closer muscles in the pedipalp of the scorpion Leiurus quinquestriatus. J Exp Biol. 1970;52(2):325-44. ,9292. Dubale MS, Vyas AB. The structure of the chela of Heterometrus sp. and its mode of operation. Bull South Calif Acad Sci. 1968;67:240-4. ,9494. Snodgrass RE. Arthropod Anatomy. Ithica, N.Y.: Comstock Pub. Associates; 1952. ]. This muscle is composed of long fibered bundles which are mechanically connected to the movable finger by a long ligament [9090. Gilai BYA, Parnas I. Neuromuscular physiology of the closer muscles in the pedipalp of the scorpion Leiurus quinquestriatus. J Exp Biol. 1970;52(2):325-44. ]. In the patella, muscles that adduct and abduct the chela in the frontal plane are also present [9595. Bowerman RF, Larimer J. Structure and physiology of the patella-tibia joint receptors in scorpion pedipalps. Comp Biochem Physiol -- Part A Physiol. 1973;46:139-51. ].

Figure 2.
Rendering of the chela closing muscles of the species Scorpio maurus (Scorpionidae) from synchrotron scan data. (A) Dorsal view. (B) Lateral view. Apodemes connecting the closing muscle in the manus to the movable finger are not shown. Only the ligament connecting the closing muscle in the patella to the movable finger is shown. Movable finger (yellow), cuticle of the manus (transparent blue), manus closing muscles (transparent orange), closing muscle in the patella (red), ligament connecting the closing muscle in the patella to the movable finger (light green), cuticle of the patella (dark green).

Contrary to crustaceans [9696. Yamada SB, Boulding EG. Claw morphology, prey size selection and foraging efficiency in generalist and specialist shell-breaking crabs. J Exp Mar Biol Ecol. 1998 Feb 1;220(2):191-211. ,9797. Govind CK, Mellon D, Quigley MM. Muscle and muscle fiber type transformation in clawed crustaceans. Integr Comp Biol. 1987;27:1079-98. ], scorpion chelae do not have opening muscles [9090. Gilai BYA, Parnas I. Neuromuscular physiology of the closer muscles in the pedipalp of the scorpion Leiurus quinquestriatus. J Exp Biol. 1970;52(2):325-44.

91. Mathew AP. On the movable claw of the pedipalps in Heterometrus scaber. J Anim Morphol Physiol. 1965;12:271-5.
-9292. Dubale MS, Vyas AB. The structure of the chela of Heterometrus sp. and its mode of operation. Bull South Calif Acad Sci. 1968;67:240-4. ], and the movable finger abduction is due to the elastic recoil of resilin in the joint [9191. Mathew AP. On the movable claw of the pedipalps in Heterometrus scaber. J Anim Morphol Physiol. 1965;12:271-5. ,9494. Snodgrass RE. Arthropod Anatomy. Ithica, N.Y.: Comstock Pub. Associates; 1952. ,9898. Govindarajan S, Rajulu GS. Presence of resilin in a scorpion Palamnaeus swammerdami and its role in the food-capturing and sound-producing mechanisms. Experientia. 1974;30:908-9. ,9999. Sensenig AT, Shultz JW. Elastic energy storage in the pedipalpal joints of scorpions and sun-spiders (Arachnida, Scorpiones, Solifugae). J Arachnol. 2004;32(1):1-10. ], the increasing of hydraulic pressure in the manus and an elastic snap-like recoil given by sclerotized plates (arthrodial sternites) located the dorso-posterior interface of the movable finger and the manus [100100. Alexander AJ. Problems of limb extension in the scorpion, Opisthophthalmus latimanus koch. Trans R Soc South Africa. 1967;37(3):165-81. ].

On the surface of the cuticle of the chela, several hair-like structures with chemo- and mechano-sensorial functions are present: trichobothria, located on the whole surface of both chelae, and a little group of sensilla on the tip of the fixed finger, known as the constellation array. For an excellent description and images of these structures, please refer to [101101. Fet V, Soleglad M, Neff D, Brewer M. Constellation array: a new sensory structure in scorpions (Arachnida: Scorpiones). Boletín la SEA. 2006;38(2006):269-78. ,102102. Hoffmann C. Bau und funktion der trichobothrien von Euscorpius carpathicus L. Z Vgl Physiol. 1967;54:290-352. ]. Trichobothria are important for environmental sensing and detection of air-borne stimuli [102102. Hoffmann C. Bau und funktion der trichobothrien von Euscorpius carpathicus L. Z Vgl Physiol. 1967;54:290-352. ], while the constellation array seems to play a role in the detection of chemical cues [101101. Fet V, Soleglad M, Neff D, Brewer M. Constellation array: a new sensory structure in scorpions (Arachnida: Scorpiones). Boletín la SEA. 2006;38(2006):269-78. ,103103. Nisani Z, Honaker A, Jenne V, Loya F, Moon H. Evidence of airborne chemoreception in the scorpion Paruroctonus marksi (Scorpiones: Vaejovidae). J Arachnol. 2018;46(1):40-4. ]. Furthermore, trichobothria placement patterns are extensively used as important taxonomic traits [104104. Vachon M. Sur l’établissement d’une nomenclature trichobothriale uniforme convenant àl’ensemble des scorpions (Arachnides) etl’existence de trois types distincts de trichobothrio-taxie. Comptes Rendus des Séances l’Académiedes Sci. 1972;275:2001-4.

105. Soleglad ME, Fet V. Evolution of scorpion orthobothriotaxy: a cladistic approach. Euscorpius. 2001;2001:1-38.
-106106. Vachon M. Étude des caractères utilisés pourclasser les familles et les genres de scorpions (Arachnides). 1. La trichobothriotaxie en Arachnologie, Sigles trichobothriaux et types de trichobothriotaxie chez les scorpions. Bull du Muséum Natl d’Histoire Nat Paris. 1974;3:857-958. ]. The cuticle on the sides where the fingers come into contact have rows of metal-enriched and hardened denticles [107107. Schofield RMS, Nesson MH, Richardson KA, Wyeth P. 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. J Insect Physiol. 2003 Jan;49(1):31-44. ], most likely friction-enhancing and grip-improving structures [9292. Dubale MS, Vyas AB. The structure of the chela of Heterometrus sp. and its mode of operation. Bull South Calif Acad Sci. 1968;67:240-4. ,108108. Stockmann R. Introduction to scorpion biology and ecology. In: Gopalakrishnakone P, Possani LD, Schwartz EF, Rodríguez de la Vega RC, editors. Scorpion Venoms. Springer, Dordrecht. p. 25-59. 2015.] which, much like trichobothria, are widely used for taxonomic identification [109109. Stahnke HL. Scorpion nomenclature and mensuration. Entomol News. 1970;81:297-316. ].

Venom delivery system

The unique metasoma is undoubtedly a scorpion’s most distinctive feature. Evolved for both predatory and defensive purposes [110110. Sharma PP, Schwager EE, Extavour CG, Wheeler WC. Hox gene duplications correlate with posterior heteronomy in scorpions. Proc Biol Sci. 2014 Oct 7;281(1792):20140661. ], this five-segmented structure carries the venomous telson, which consists of the venom vesicle containing two paired venom glands, and the sharp aculeus (Figure 3).

Figure 3.
Rendering of the internal anatomy of the V metasomal segment and telson from different points of view. (A) Ventral view. (B) Dorsal view. (C) Lateral view. Note that the telson is dorsoventrally inverted in defensive posture, as in the inset photograph. Cuticle of both telson and V metasomal segment is in transparent blue. Within the V metasomal segment there are a pair of dorsal flexor muscles (arthrodio-tergal rectus muscles in orange) and the pair of ventral retractor muscles (lateral arthrodio-sternal muscles in red) and the apodemes (yellow) connecting the two antagonistic muscles to the base of the telson. Within the telson are located the paired venom glands (cyan), each ending with its venom duct (green) and separated by a layer of muscles (salmon) responsible for the squeezing of the venom gland against the cuticle and permitting the venom to flow out of the gland lumen. The species used for this µCT scan is Neochactas delicatus (Chactidae), but the species shown in the inset is Scorpio maurus (Scorpionidae).

Metasomal segments develop later than anterior appendages due to the anterior-posterior migration of the growing region [8888. Farley RD. Matrotrophic adaptations and early stages of embryogenesis in the desert scorpion Paruroctonus mesaensis (Vaejovidae). J Morphol. 1998 Sep;237(3):187-211. ,8989. Farley RD. Development of segments and appendages in embryos of the desert scorpion Paruroctonus mesaensis (Scorpiones: Vaejovidae). J Morphol. 2001 Oct;250(1):70-88. ]. In the early stages of development, the metasomal segments are flattened and undifferentiated and the telson is rounded and bilobed. In the later stages of the development, the metasomal segments swell and the telson tapers distally to form the aculeus [8989. Farley RD. Development of segments and appendages in embryos of the desert scorpion Paruroctonus mesaensis (Scorpiones: Vaejovidae). J Morphol. 2001 Oct;250(1):70-88. ].

The joint architecture and muscle organization together give the metasoma a high degree of freedom of movement [111111. Bowerman RF. A muscle receptor organ in the scorpion postabdomen - II. Reflexes evoked by MRO stretch and release. J Comp Physiol. 1972 Jun;81:147-57. ] which is fully achieved after the second instar [8989. Farley RD. Development of segments and appendages in embryos of the desert scorpion Paruroctonus mesaensis (Scorpiones: Vaejovidae). J Morphol. 2001 Oct;250(1):70-88. ].

The metasoma musculature has been described in [9393. Lankester ER. On the muscular and endoskeletal systems of Limulus and Scorpio; with some notes on the anatomy and generic characters of scorpions. Zool Soc London. 1885;XI:311-84. ,9494. Snodgrass RE. Arthropod Anatomy. Ithica, N.Y.: Comstock Pub. Associates; 1952. ] and partially by [112112. Bowerman RF. A muscle receptor organ in the scorpion postabdomen - I. The sensory system. J Comp Physiol. 1972;81:133-46. ]. The last segment of the mesosoma contains antagonistic muscles causing protraction and retraction of the metasoma (respectively the median antero-posterior muscle and the arthrodio-tergal rectus muscle), and two muscles originating dorso-laterally and inserting ventrally at the base to the first metasomal segment (the arthrodio-tergal obliquus muscles). These last two antagonistic muscles allow the metasoma to be moved laterally. The metasomal segments I, II and III possess the same muscle distribution: ventrally, a large medial bundle (median antero-posterior muscle) and two lateral muscles, (lateral arthrodio-sternal muscles). All these muscles originate on the anterior segment and insert on the posterior one. Dorsally, there are four muscles originating on the cuticle of the anterior segment and inserting at the base of the posterior segment. Two large medial bundles (arthrodio-tergal rectus muscles) and two small oblique ones are located at the side of each segment (arthrodio-tergal obliquus muscles). Segment IV and V each have a different configuration. Metasomal segment IV presents ventrally both the median antero-posterior muscle and the two lateral arthrodio-sternal muscles. Dorsally, only the two arthrodio-tergal rectus muscles are present but differently from the more anterior segments, these muscles are much more elongated and narrower. These muscles have the function to flex and extend the metasoma [112112. Bowerman RF. A muscle receptor organ in the scorpion postabdomen - I. The sensory system. J Comp Physiol. 1972;81:133-46. ]. The V segment has only a pair of dorsal flexor muscles and a pair of ventral retractor muscles responsible for the movement of the telson (respectively named arthrodio-tergal rectus muscles lateral and arthrodio-sternal muscles ) [5252. van der Meijden A, Kleinteich T. A biomechanical view on stinger diversity in scorpions. J Anat. 2017 Apr;230(4):497-509. ] (Figure 3). The telson consists of a bulbous structure, which contains the two venom glands, and which narrows into the aculeus, the curved and sharp stinger through which venom is injected.

The cuticle of the stinger and metasoma is thick and covered by granules and several sensory hair-like structures [106106. Vachon M. Étude des caractères utilisés pourclasser les familles et les genres de scorpions (Arachnides). 1. La trichobothriotaxie en Arachnologie, Sigles trichobothriaux et types de trichobothriotaxie chez les scorpions. Bull du Muséum Natl d’Histoire Nat Paris. 1974;3:857-958. ,113113. Babu KS, Jacobdoss P. Central afferent pathways of long hair sensilla in the ventral nerve cord of the Indian black scorpion, Heterometrus fulvipes Koch. J Comp Physiol A. 1994;174:495-505. ,114114. Foelix R, Erb B, Braunwalder M. Fine structure of the stinger (aculeus) in Euscorpius. J Arachnol. 2014;42(1):119-22. ]. In some scorpion species, many cuticular pits containing chemosensory-like setae are present on the ventral and lateral sides of each metasomal segment. This suggests a possible sensory function of the metasoma in these species, similar to the antennae of insects [115115. Fet V, Fet E, Neff D, Graham M. Metasoma of Orthochirus (Scorpiones: Buthidae): are scorpions evolving a new sensory organ? Rev ibérica Aracnol. 2003;8:69-72. ]. Soleglad et al. [116116. Fet V, Soleglad ME, Brewer M. Laterobasal aculear serrations (LAS) in scorpion family Vaejovidae (Scorpiones: Chactoidea). Euscorpius. 2006;45:1-19. ] identified minute rows of denticles located laterally on the base of the aculeus in some species, called laterobasal aculear serrations. The function of these is still unknown. Some scorpion species belonging to three different families (Buthidae, Diplocentridae and Vaejovidae) can present a sub-aculear tubercule [117117. González-Santillán E, Prendini L. Systematic revision of the North American Syntropine Vaejovid scorpions with a subaculear tubercle, Konetontli González-Santillán and Prendini, 2013. Bull Am Museum Nat Hist. 2015 Sep 24;397:1-78. ] with important taxonomic value [109109. Stahnke HL. Scorpion nomenclature and mensuration. Entomol News. 1970;81:297-316. ] but unknown function [5252. van der Meijden A, Kleinteich T. A biomechanical view on stinger diversity in scorpions. J Anat. 2017 Apr;230(4):497-509. ]. Lourenço [118118. Lourenço WR. The coevolution between telson morphology and venom glands in scorpions (Arachnida). J Venom Anim Toxins incl Trop Dis. 2020;26. https://doi.org/10.1590/1678-9199-JVATITD-2020-0128.
https://doi.org/10.1590/1678-9199-JVATIT...
] suggested that these sub-aculear tubercles may serve as a protection against breakage for particularly long and slender aculei, although simpler reinforcing strategies, such as aculei with a thicker base, already exist within extant scorpions [5252. van der Meijden A, Kleinteich T. A biomechanical view on stinger diversity in scorpions. J Anat. 2017 Apr;230(4):497-509. ].

Venom production and secretion

Scorpion venom is produced in the secretory epithelium of the two non-communicating venom glands located in the telson. These glands are surrounded by muscle layers radially, while their lateral portions are directly in contact with the endocuticle of the telson (Figure 3). This arrangement is quite conserved in all scorpion families [119119. Mazurkiewicz JE, Bertke EM. Ultrastructure of the venom gland of the scorpion, Centruroides sculpturatus (Ewing). J Morphol. 1972;137(3):365-83.

120. Sherwan TA. Morphology and histology of venom gland of Scorpio Maurus Kruglovi (Birula, 1910) (Scorpionidae:Scorpiones). Zanco J Pure Appl Sci. 2015;27(5):25-8.

121. Keegan HL, Lockwood WR. Secretory epithelium in venom glands of two species of scorpion of the genus Centruroides Marx. Am J Trop Med Hyg. 1971 Sep;20(5):770-85.

122. Taib NT, Jarrar BM. Histological and histochemical characterization of the venom apparatus of Palestine yellow scorpion, Leiurus quinquestriatus Hemprich and Ehrenberg 1828. Trop Zool. 1993;6(1):143-52.
-123123. Pawlosky EN. Studies on the organization and development of scorpions. J Cell Sci. 1924;s2-68:615-40. ].

Pawlosky [123123. Pawlosky EN. Studies on the organization and development of scorpions. J Cell Sci. 1924;s2-68:615-40. ] divided the scorpion venom glands into primitive and complex, depending on the absence or presence of folds of the secretory epithelium, respectively. Between the muscles and the venom secretory system, a complex matrix of connective tissue is interposed. In the contact area between the lateral telson cuticle and the secretory epithelium a single or multiple layers of cuboid cells are visible. Interior to the connective layer and the cuboid cells lies the basal membrane where the conically shaped secreting cells are located [119119. Mazurkiewicz JE, Bertke EM. Ultrastructure of the venom gland of the scorpion, Centruroides sculpturatus (Ewing). J Morphol. 1972;137(3):365-83.

120. Sherwan TA. Morphology and histology of venom gland of Scorpio Maurus Kruglovi (Birula, 1910) (Scorpionidae:Scorpiones). Zanco J Pure Appl Sci. 2015;27(5):25-8.

121. Keegan HL, Lockwood WR. Secretory epithelium in venom glands of two species of scorpion of the genus Centruroides Marx. Am J Trop Med Hyg. 1971 Sep;20(5):770-85.

122. Taib NT, Jarrar BM. Histological and histochemical characterization of the venom apparatus of Palestine yellow scorpion, Leiurus quinquestriatus Hemprich and Ehrenberg 1828. Trop Zool. 1993;6(1):143-52.
-123123. Pawlosky EN. Studies on the organization and development of scorpions. J Cell Sci. 1924;s2-68:615-40. ]. The basal part of these cells contains all the organelles, while the apical part is in touch with the lumen of the venom gland and contains several types of toxin-containing granules. In scorpions, toxin secretion is an apocrine mechanism [119119. Mazurkiewicz JE, Bertke EM. Ultrastructure of the venom gland of the scorpion, Centruroides sculpturatus (Ewing). J Morphol. 1972;137(3):365-83. ,121121. Keegan HL, Lockwood WR. Secretory epithelium in venom glands of two species of scorpion of the genus Centruroides Marx. Am J Trop Med Hyg. 1971 Sep;20(5):770-85. ,122122. Taib NT, Jarrar BM. Histological and histochemical characterization of the venom apparatus of Palestine yellow scorpion, Leiurus quinquestriatus Hemprich and Ehrenberg 1828. Trop Zool. 1993;6(1):143-52. ,124124. Zlotkin E, Miranda F, Rochat H. Chemistry and pharmacology of Buthinae scorpion venoms. In: Bettini S, editor. Arthropod Venoms. Springer-Verlag, Heidelberg; Germany. p. 317-69. 1978.,125125. Jarrar BM, AL-Rowaily MA. Histology and histochemistry of the venom apparatus of the black scorpion Androctonus crassicauda (Olivier, 1807) (Scorpiones: Buthidae). J Venom Anim Toxins incl Trop Dis. 2008;14(3):514-26. https://doi.org/10.1590/S1678-91992008000300010.
https://doi.org/10.1590/S1678-9199200800...
], meaning that a portion of the cytoplasm is also secreted into the lumen of the venom gland. Secretory cells seem to be highly specialized in producing one single type of toxin [122122. Taib NT, Jarrar BM. Histological and histochemical characterization of the venom apparatus of Palestine yellow scorpion, Leiurus quinquestriatus Hemprich and Ehrenberg 1828. Trop Zool. 1993;6(1):143-52. ]. Each secretory cell contains granules of only one size and type, confirmed by their uniform reaction to laboratory staining techniques [121121. Keegan HL, Lockwood WR. Secretory epithelium in venom glands of two species of scorpion of the genus Centruroides Marx. Am J Trop Med Hyg. 1971 Sep;20(5):770-85. ,126126. Yigit N, Benli M. The venom gland of the scorpion species Euscorpius mingrelicus (Scorpiones: Euscorpiidae): morphological and ultrastructural characterization. J Venom Anim Toxins incl Trop Dis. 2008;14:466-80. https://doi.org/10.1590/S1678-91992008000300007.
https://doi.org/10.1590/S1678-9199200800...
]. Additionally, these different types of granules can be selectively stained. The high diversity of these granules in terms of their reaction to histological stains confirms that different cells produce a different product or mixture of products [122122. Taib NT, Jarrar BM. Histological and histochemical characterization of the venom apparatus of Palestine yellow scorpion, Leiurus quinquestriatus Hemprich and Ehrenberg 1828. Trop Zool. 1993;6(1):143-52. ,126126. Yigit N, Benli M. The venom gland of the scorpion species Euscorpius mingrelicus (Scorpiones: Euscorpiidae): morphological and ultrastructural characterization. J Venom Anim Toxins incl Trop Dis. 2008;14:466-80. https://doi.org/10.1590/S1678-91992008000300007.
https://doi.org/10.1590/S1678-9199200800...
].

The contraction of the muscles surrounding each venom gland causes the squeezing of the whole gland against the cuticle wall, and the consequent conveying of the venom produced by each gland into a cuticular duct [9494. Snodgrass RE. Arthropod Anatomy. Ithica, N.Y.: Comstock Pub. Associates; 1952. ]. Both ducts pass through almost the whole length of the aculeus, ending independently before the tip of the aculeus. The ovoid openings, similar to those of hypodermic needles, are found on the dorsal side of the aculeus [5353. Zhao ZL, Shu T, Feng XQ. Study of biomechanical, anatomical, and physiological properties of scorpion stingers for developing biomimetic materials. Mater Sci Eng C Mater Biol Appl. 2016 Jan 1;58:1112-21. ,114114. Foelix R, Erb B, Braunwalder M. Fine structure of the stinger (aculeus) in Euscorpius. J Arachnol. 2014;42(1):119-22. ,126126. Yigit N, Benli M. The venom gland of the scorpion species Euscorpius mingrelicus (Scorpiones: Euscorpiidae): morphological and ultrastructural characterization. J Venom Anim Toxins incl Trop Dis. 2008;14:466-80. https://doi.org/10.1590/S1678-91992008000300007.
https://doi.org/10.1590/S1678-9199200800...

127. Yigit N, Benli M. Fine structural analysis of the stinger in venom apparatus of the scorpion Euscorpius mingrelicus (Scorpiones: Euscorpiidae). J Venom Anim Toxins incl Trop Dis. 2010;16:76-86. https://doi.org/10.1590/S1678-91992010005000003.
https://doi.org/10.1590/S1678-9199201000...

128. Polis GA. The biology of scorpions. Polis GA, editor. Stanford: University Stanford; 1990.
-129129. Halse SA, Prideaux PL, Cockson A, Zwicky KT. Observations on the morphology and histochemistry of the venom glands of a scorpion, Urodacus novaehollandiae Peters (Scorpionidae). Aust J Zool. 1980;28(2):173-83. ]. Some authors reported that in Androctonus crassicauda (Buthidae) [125125. Jarrar BM, AL-Rowaily MA. Histology and histochemistry of the venom apparatus of the black scorpion Androctonus crassicauda (Olivier, 1807) (Scorpiones: Buthidae). J Venom Anim Toxins incl Trop Dis. 2008;14(3):514-26. https://doi.org/10.1590/S1678-91992008000300010.
https://doi.org/10.1590/S1678-9199200800...
], Centruroides sculpturatus (Buthidae) [119119. Mazurkiewicz JE, Bertke EM. Ultrastructure of the venom gland of the scorpion, Centruroides sculpturatus (Ewing). J Morphol. 1972;137(3):365-83. ] and Leiurus quinquestriatus (Buthidae), the ducts fuse in the terminal part of the aculeus and end in an unique pore.

Composition and main toxin families

When extracting venom from scorpions, especially when electrostimulation is avoided, it is possible to observe a transparent to milky-opalescent transition in the venom coming out of the aculeus [4545. Nisani Z, Hayes WK. Venom-spraying behavior of the scorpion Parabuthus transvaalicus (arachnida: Buthidae). Behav Processes. 2015 Jun;115:46-52. ,130130. Inceoglu B, Lango J, Jing J, Chen L, Doymaz F, Pessah IN, Hammock BD. One scorpion, two venoms: prevenom of Parabuthus transvaalicus acts as an alternative type of venom with distinct mechanism of action. Proc Natl Acad Sci U S A. 2003 Feb 4;100(3):922-7.

131. Yahel-Niv A, Zlotkin E. Comparative studies on venom obtained from individual scorpions by natural stings. Toxicon. 1979;17(5):435-46.
-132132. Zlotkin E, Shulow A. A simple device for collecting scorpion venom. Toxicon. 1969 Dec;7(4):331-2. ]. The transparent portion of the venom is generally referred to as pre-venom, while the milky, opalescent portion is considered to be the “true” venom [130130. Inceoglu B, Lango J, Jing J, Chen L, Doymaz F, Pessah IN, Hammock BD. One scorpion, two venoms: prevenom of Parabuthus transvaalicus acts as an alternative type of venom with distinct mechanism of action. Proc Natl Acad Sci U S A. 2003 Feb 4;100(3):922-7. ]. The pre-venom and true venom present differences in chemical composition, with pre-venom being richer in ions than the true venom, but not in proteins [130130. Inceoglu B, Lango J, Jing J, Chen L, Doymaz F, Pessah IN, Hammock BD. One scorpion, two venoms: prevenom of Parabuthus transvaalicus acts as an alternative type of venom with distinct mechanism of action. Proc Natl Acad Sci U S A. 2003 Feb 4;100(3):922-7. ,131131. Yahel-Niv A, Zlotkin E. Comparative studies on venom obtained from individual scorpions by natural stings. Toxicon. 1979;17(5):435-46. ]. These differences in composition between pre-venom and true venom are likely related to the differences in their appearance. The two fractions also cause different physiological effects when injected, with pre-venom apparently being less toxic than the overall more effective true venom, but still able to induce paralysis and pain [130130. Inceoglu B, Lango J, Jing J, Chen L, Doymaz F, Pessah IN, Hammock BD. One scorpion, two venoms: prevenom of Parabuthus transvaalicus acts as an alternative type of venom with distinct mechanism of action. Proc Natl Acad Sci U S A. 2003 Feb 4;100(3):922-7. ]. The dichotomy between pre-venom and true venom may be an oversimplification of a continuous or semi-continuous range, with some authors identifying more than two types of venom [131131. Yahel-Niv A, Zlotkin E. Comparative studies on venom obtained from individual scorpions by natural stings. Toxicon. 1979;17(5):435-46. ].

The protein composition of scorpion venom is particularly complex, with more than 4,500 toxins identified so far across all studied species [133133. Grashof DGB, Kerkkamp HMI, Afonso S, Archer J, Harris DJ, Richardson MK, Vonk FJ, van der Meijden A. Transcriptome annotation and characterization of novel toxins in six scorpion species. BMC Genomics. 2019 Aug 13;20:1-10. ]. Nevertheless, scorpion venoms are not only rich in proteins, but also in nucleotides, amines (serotonin or histamine) and mucopolysaccharides, probably due to the apocrine secretion mechanism of the venom gland cells. However, the role these molecules play in toxicity has yet to be clarified. Previous studies have mainly focused on the peptide components of scorpion venoms. Although a complete overview of the scorpion venom literature is outside the scope of this review, in this paragraph we will highlight some of the best known and important classes of bioactive peptide compounds present in scorpion venoms. These cover about the 75% of the total transcripts obtained from venoms of 37 species belonging to seven different families. The remaining quarter of venom compounds is composed of molecules for which either structural domains and/or function are unknown [134134. Cid-Uribe JI, Veytia-Bucheli JI, Romero-Gutierrez T, Ortiz E, Possani LD. Scorpion venomics: a 2019 overview. Expert Rev Proteomics. 2020 Jan;17(1):67-83. ]. For a more comprehensive review of scorpion toxins, refer to [134134. Cid-Uribe JI, Veytia-Bucheli JI, Romero-Gutierrez T, Ortiz E, Possani LD. Scorpion venomics: a 2019 overview. Expert Rev Proteomics. 2020 Jan;17(1):67-83.

135. Possani LD, Becerril B, Delepierre M, Tytgat J. Scorpion toxins specific for Na+ channels. Eur J Biochem. 1999 Sep;264(2):287-300.

136. Quintero-Hernández V, Jiménez-Vargas JM, Gurrola GB, Valdivia HH, Possani LD. Scorpion venom components that affect ion-channels function. Toxicon. 2013 Dec 15;76:328-42.

137. Rodríguez De La Vega RC, Possani LD. Overview of scorpion toxins specific for Na+ channels and related peptides: biodiversity, structure-function relationships and evolution. Toxicon. 2005 Dec 15;46(8):831-44.
-138138. Rodríguez de la Vega RC, Schwartz EF, Possani LD. Mining on scorpion venom biodiversity. Toxicon. 2010 Dec 15;56(7):1155-61. ].

Four main groups of bioactive compounds are currently known to be present in scorpion venoms: ion-channel binding peptides, enzymes, protease inhibitors and host defense peptides (HDP). Proteomic and transcriptomic analyses performed on venoms and venom glands of scorpions belonging to different families have shown that the most abundant fraction of peptides in scorpion venoms is represented by the superfamily of ion-channel binding toxins. Short-chain ion-channel binding toxins (from 20 to 50 amino acid residues), are specifically active on voltage-gated K+ channels. Depending on their length and their folding differences, this class of peptides is further subdivided into several subfamilies. A dedicated database of scorpion toxins active on K+ channels (KScTx) is available at [139139. Kuzmenkov AI, Krylov NA, Chugunov AO, Grishin EV, Vassilevski AA. Kalium: a database of potassium channel toxins from scorpion venom. Database (Oxford). 2016 Apr 17;2016:baw056. ]. The peptides that bind to voltage-gated Na+ channels (NaScTx) have longer chains (50 to 80 amino acid residues). These are classified into α-NaScTx and β-NaScTx, depending on the receptor site they bind to. Calcium channels are targeted by specific scorpion venom peptides known as calcins. These peptides generally compete with the natural ligands of the Ca2+ channels affecting muscular contraction [136136. Quintero-Hernández V, Jiménez-Vargas JM, Gurrola GB, Valdivia HH, Possani LD. Scorpion venom components that affect ion-channels function. Toxicon. 2013 Dec 15;76:328-42. ]. The last members of the family of the ion-channel binding peptides are chlorotoxins (ClTx), altering the conductance of Cl- channels. The toxicological effects of chlorotoxins have been poorly studied so far, but many studies have focused on the potential medical applications of this class of small peptides, especially for the imaging and treatment of aggressive forms of brain cancer generally known as glioma [140140. Lyons SA, O’Neal J, Sontheimer H. Chlorotoxin, a scorpion-derived peptide, specifically binds to gliomas and tumors of neuroectodermal origin. Glia. 2002 Aug;39(2):162-73.

141. Cohen G, Burks SR, Frank JA. Chlorotoxin-A multimodal imaging platform for targeting glioma tumors. Toxins (Basel). 2018 Dec;10(1):1-12.
-142142. Zhao L, Li Y, Zhu J, Sun N, Song N, Xing Y, Huang H, Zhao J. Chlorotoxin peptide-functionalized polyethylenimine-entrapped gold nanoparticles for glioma SPECT/CT imaging and radionuclide therapy. J Nanobiotechnol. 2019;17(30):1-13. ].

Another abundant class of active components of scorpion venoms are the enzymatic toxins. This class of molecules is not as abundant as in other venoms (e.g., snake venom), but its contribution to scorpion venom toxicity is not to be neglected. Phospholipases disrupt the phospholipids in the membranes of cells, causing the lysis of haemocytes and the development of oedemas and release of pro-inflammatory compounds [143143. Krayem N, Gargouri Y. Scorpion venom phospholipases A2: a minireview. Toxicon. 2020 Sep;184:48-54. ]. Another class of enzymes contained in the venom of several scorpion families are the metalloproteases. These proteases are characterized by a bivalent metallic ion (usually the zinc cation) and promote the hydrolysis of proteins present on the cellular membrane. One of the most extensively studied scorpion venom metalloproteases is Antarease. Isolated for the first time from the venom of the Brazilian scorpion Tityus serrulatus (Buthidae), this enzyme causes the hydrolysis of the protein regulating the cleavage of the transport vesicles, thus affecting extra-cellular transports, especially in secretory organs like the pancreas [144144. Ortiz E, Rendón-Anaya M, Rego SC, Schwartz EF, Possani LD. Antarease-like Zn-metalloproteases are ubiquitous in the venom of different scorpion genera. Biochim Biophys Acta - Gen Subj. 2014 Jun;1840(6):1738-46. ]. Hyaluronidases represent another class of enzymes widely present in scorpion venom. These enzymes allow a rapid diffusion of the other bioactive compounds through tissues by degrading the extracellular matrix [145145. Bordon KCF, Wiezel GA, Amorim FG, Arantes EC. Arthropod venom Hyaluronidases: biochemical properties and potential applications in medicine and biotechnology. J Venom Anim Toxins incl Trop Dis. 2015;21:43. doi: 10.1186/s40409-015-0042-7.
https://doi.org/10.1186/s40409-015-0042-...
]. Even if many of the symptoms generated by scorpion envenomation have a neurotoxic nature, envenomation by species belonging to the medically important genus Hemiscorpius (Hemiscorpiidae) represents an important exception. The venom obtained from species belonging to this genus is more similar to snake venom because of the large fraction of enzymes and proteins, and the relatively small fraction of small peptides with affinity for voltage-gated ion channels [146146. Dehghani R, Kamiabi F, Mohammadi M. Scorpionism by Hemiscorpius spp. in Iran: a review. J Venom Anim Toxins incl Trop Dis. 2018;24:1-10. doi: 10.1186/s40409-018-0145-z.
https://doi.org/10.1186/s40409-018-0145-...
,147147. Kazemi-Lomedasht F, Khalaj V, Bagheri KP, Behdani M, Shahbazzadeh D. The first report on transcriptome analysis of the venom gland of Iranian scorpion, Hemiscorpius lepturus. Toxicon. 2017 Jan;125:123-30. ]. Venoms produced by Hemiscorpius species mainly cause cytotoxic effects, and can cause fatal envenomation while causing little to no pain [148148. Mirakabadi AZ. Hemiscorpius lepturus envenomation: manifestations and management with specific antivenom. Arch Razi Inst. 2013;68:91-9. ].

Protease inhibitors are important components of scorpion venoms that selectively degrade the envenomated organism’s proteases, thus preventing the degradation of the venom peptides injected into the organism’s body, thereby increasing venom efficacy and efficiency [149149. Ma H, Xiao-Peng T, Yang SL, Lu QM, Lai R. Protease inhibitor in scorpion (Mesobuthus eupeus) venom prolongs the biological activities of the crude venom. Chin J Nat Med. 2016 Aug;14(8):607-14. ].

Host Defense Peptides (HDPs) are a large family of small peptides that has been found in all arthropods [150150. Sabiá EF, Menezes LFS, De Araújo IFS, Schwartz EF. Natural occurrence in venomous arthropods of antimicrobial peptides active against protozoan parasites. Toxins (Basel). 2019 Sep 25;11(10):563. ]. They are related to the innate immune defenses of these animals, as most of these peptides have antimicrobial action [151151. Harrison PL, Abdel-Rahman MA, Miller K, Strong PN. Antimicrobial peptides from scorpion venoms. Toxicon. 2014 Sep;88:115-37. ]. This class of proteins is generally divided into two main groups, according to the presence or absence of cysteines in the aminoacidic residual chain [152152. Cid-Uribe JI, Menses EP, Batista CVF, Ortiz E, Possani LD. Dissecting toxicity: the venom gland transcriptome and the venom proteome of the highly venomous scorpion Centruroides limpidus (Karsch, 1879). Toxins (Basel). 2019 Apr 30;11(5):247. ]. The effect of this relatively abundant class of peptides on scorpion venom toxicity is still not clear, but cases of haemolysis due to HDPs found in the venom of Pandinus imperator (Scorpionidae) have been reported [153153. Zeng XC, Zhou L, Shi W, Luo X, Zhang L, Nie Y, Wang J, Wu S, Cao B, Cao H. Three new antimicrobial peptides from the scorpion Pandinus imperator. Peptides. 2013 Jul;45:28-34. ], possibly suggesting a disruptive effect on blood-clotting mechanisms.

Scorpion venom evolution

Venoms evolved independently several times in only a small number of animal taxa [1818. Casewell NR, Wüster W, Vonk FJ, Harrison RA, Fry BG. Complex cocktails: The evolutionary novelty of venoms. Trends Ecol Evol. 2013 Apr;28(4):219-29. ] where it may be used differently. Venom may have different ecological roles, and the main drivers of its evolution can be different among taxa. In snakes for instance, is widely accepted that venom evolved mainly for predatory purposes [154154. Ward-Smith H, Arbuckle K, Naude A, Wüster W. Fangs for the memories? A survey of pain in snakebite patients does not support a strong role for defense in the evolution of snake venom composition. Toxins (Basel). 2020 Mar 22;12(3):201.

155. Daltry JC, Wuster W, Thorpe RS. Diet and snake venom evolution. Nature. 1996 Feb 8;379(6565):537-40.
-156156. Lyons K, Dugon MM, Healy K. Diet breadth mediates the prey specificity of venom potency in snakes. Toxins (Basel). 2020 Jan 23;12(2):74. ]. Venom may have evolved due to other demands in different groups. Self-defense has been also proposed as driver of venom evolution in fishes and wasps [157157. Walker AA, Robinson SD, Undheim EAB, Jin J, Han X, Fry BG, Vetter I, King GF. Missiles of mass disruption: composition and glandular origin of venom used as a projectile defensive weapon by the assassin bug Platymeris rhadamanthus. Toxins (Basel). 2019 Nov 18;11(11):673. ,158158. Harris RJ, Jenner RA. Evolutionary ecology of fish venom: adaptations and consequences of evolving a venom system. Toxins (Basel). 2019 Feb;11(2):60. ], intraspecific competition in venomous mammals [8181. Rode-Margono JE, Nekaris KAI. Cabinet of curiosities: venom systems and their ecological function in mammals, with a focus on primates. Toxins. 2015 Jul 17;7(7):2639-58. ], possibly mating behavior in scorpions [128128. Polis GA. The biology of scorpions. Polis GA, editor. Stanford: University Stanford; 1990. ,159159. Tallarovic SK, Melville JM, Brownell PH. Courtship and mating in the giant hairy desert scorpion, Hadrurus arizonensis (Scorpionida, Iuridae). J Insect Behav. 2000;13:827-38. ,160160. Francke OF. The reproductive biology and life history of Megacormus gertschi Diaz (Scorpiones: Chactidae; Megacorminae). J Arachnol. 1979;7:223-30. ] and even for an antimicrobial function in bees [161161. Baracchi D, Francese S, Turillazzi S. Beyond the antipredatory defence: honey bee venom function as a component of social immunity. Toxicon. 2011 Nov;58(6-7):550-7. ].

The origins of scorpion venom represent an ongoing debate. One of the most widely accepted hypotheses is that toxins may have originated from innate, non-toxic peptides, after a process of gene duplication and neofunctionalization and/or exon shuffling [162162. Vonk FJ, Casewell NR, Henkel CV, Heimberg AM, Jansen HJ, McCleary RJR, Kerkkamp HME, Vos RA, Guerreiro I, Calvete JJ, Wüster W, Woods AE, Logan JM, Harrison RA, Castoe TA, Koning APJ, Pollock DD, Yandell M, Calderon D, Renjifo C, Currier RB, Salgado D, Pla D, Sanz L, Hyder AS, Ribeiro JMC, Arntzen JW, van den Thillart GEEJM, Boetzer M, Pirovano W, Dirks RP, Spaink HP, Duboule D, McGlinn E, Kini RM, Richardson MK. The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc Natl Acad Sci U S A. 2013 Dec 17;110(510):20651-6.

163. Hargreaves AD, Swain MT, Hegarty MJ, Logan DW, Mulley JF. Restriction and recruitment-gene duplication and the origin and evolution of snake venom toxins. Genome Biol Evol. 2014 Aug;6(8):2088-95.

164. Wong ESW, Belov K. Venom evolution through gene duplications. Gene. 2012 Mar 15;496(1):1-7.

165. Lynch VJ. Inventing an arsenal: adaptive avolution and neofunctionalization of snake venom phospholipase A2 genes. BMC Evol Biol. 2007 Jan 18;7:2.

166. Whittington CM, Papenfuss AT, Bansal P, Torres AM, Wong ESW, Deakin JE, Graves T, Alsop A, Schatzkamer K, Kremitzki C, Ponting CP, Temple-Smith P, Warren WC, Kuchel PW, Belov K. Defensins and the convergent evolution of platypus and reptile venom genes. Genome Res. 2008 Jun;18(6):986-94.

167. Brust A, Sunagar K, Undheim EAB, Vetter I, Yang DC, Casewell NR, Jackson TNW, Koludarov I, Alewood PF, Hodgson WC, Lewis RJ, King GF, Antunes A, Hendrikx I, Fry BG. Differential evolution and neofunctionalization of snake venom metalloprotease domains. Mol Cell Proteomics. 2013 Mar;12(3):651-63.

168. Zhang S, Gao B, Zhu S. Target-driven evolution of scorpion toxins. Sci Rep. 2015;5(14973):1-13.

169. Wang X, Gao B, Zhu S. Exon shuffling and origin of scorpion venom biodiversity. Toxins (Basel). 2017 Jan;9(1):10.
-170170. Pineda SS, Chin YK-Y, Undheim EAB, Senff S, Mobli M, Dauly C, Escoubas P, Nicholson GM, Kaas Q, Guo S, Herzig V, Mattick JS, King GF. Structural venomics reveals evolution of a complex venom by duplication and diversification of an ancient peptide-encoding gene. Proc Natl Acad Sci U S A. 2020 May 26;117(21):11399-408. ]. For example, some toxins belonging to the KScTx group present a very high level of structural similarity with defensins and HDPs associated with the innate immune system of arthropods [171171. Bontems F, Roumestand C, Gilquin B, Ménez A, Toma F. Refined structure of charybdotoxin: common motifs in scorpion toxins and insect defensins. Science. 1991 Dec 6;254(5037):1521-3.

172. Zhu S, Peigneur S, Gao B, Umetsu Y, Ohki S, Tytgat J. Experimental conversion of a defensin into a neurotoxin: implications for origin of toxic function. Mol Biol Evol. 2014 Mar;31(3):546-59.

173. Meng L, Xie Z, Zhang Q, Li Y, Yang F, Chen Z, Li W, Cao Z, Wu Y. Scorpion potassium channel-blocking defensin highlights a functional link with neurotoxin. J Biol Chem. 2016 Mar 25;291(13):7097-106.
-174174. Froy O, Gurevitz M. Arthropod defensins illuminate the divergence of scorpion neurotoxins. J Pept Sci. 2004 Dec;10(12):714-8. ]. The high similarities between these KScTx toxins and defensins has been used to generate toxigenic compounds able to bind K+ channels by modifying a key sequence in defensins [172172. Zhu S, Peigneur S, Gao B, Umetsu Y, Ohki S, Tytgat J. Experimental conversion of a defensin into a neurotoxin: implications for origin of toxic function. Mol Biol Evol. 2014 Mar;31(3):546-59. ,173173. Meng L, Xie Z, Zhang Q, Li Y, Yang F, Chen Z, Li W, Cao Z, Wu Y. Scorpion potassium channel-blocking defensin highlights a functional link with neurotoxin. J Biol Chem. 2016 Mar 25;291(13):7097-106. ]. The opposite transition, from KScTx to defensin has been observed through experiments of mutagenesis of the genes coding for potassium voltage-gated channel-binding peptides [175175. Zhu S, Gao B, Aumelas A, del Carmen Rodríguez M, Lanz-Mendoza H, Peigneur S, Diego-Garcia E, Martin-Eauclaire MF, Tytgat J, Possani LD. MeuTXKβ1, a scorpion venom-derived two-domain potassium channel toxin-like peptide with cytolytic activity. Biochim Biophys Acta. 2010 Apr;1804(4):872-83. ]. Interestingly, many toxins with high structural similarity with defensins have been found in other venomous taxa as well (reptiles and mammals), increasing the interest in this class of peptides as an evolutionary ancestor of many different toxins [166166. Whittington CM, Papenfuss AT, Bansal P, Torres AM, Wong ESW, Deakin JE, Graves T, Alsop A, Schatzkamer K, Kremitzki C, Ponting CP, Temple-Smith P, Warren WC, Kuchel PW, Belov K. Defensins and the convergent evolution of platypus and reptile venom genes. Genome Res. 2008 Jun;18(6):986-94. ,176176. Fry BG, Roelants K, Champagne DE, Scheib H, Tyndall JDA, King GF, Nevalainen TJ, Norman JA, Lewis RJ, Norton RS, Renjifo C, de la Vega RCR. The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet. 2009;10:483-511. ].

Scorpionism

“Scorpionism” is the word that is commonly used to refer to fatal envenomation caused by scorpion stings [177177. Lourenço W., Cuellar O. Scorpions, scorpionism, life history strategies and parthenogenesis. J Venom Anim Toxins. 1995;1:51-62. doi: 10.1590/S0104-79301995000200002.
https://doi.org/10.1590/S0104-7930199500...
]. Annually, around 1.2 million people are stung by scorpions worldwide, and around 3,250 incidents result in fatal envenomation [178178. Chippaux JP, Goyffon M. Epidemiology of scorpionism: a global appraisal. Acta Trop. 2008 Aug;107(2):71-9. ]. Incidents are mainly concentrated in tropical countries, where scorpionism is an important but still neglected health issue. The hotspots of scorpionism are in Saharan Africa, the southern and eastern regions of Africa, the Middle East (mainly Iran and Turkey), south India, Mexico, Brazil, and the Amazonian basin area (including the Guianas, Venezuela, and northern Brazil) [178178. Chippaux JP, Goyffon M. Epidemiology of scorpionism: a global appraisal. Acta Trop. 2008 Aug;107(2):71-9. ,179179. Santos MSV, Silva CGL, Silva Neto B, Grangeiro Júnior CRP, Lopes VHG, Teixeira Júnior AG, Bezerra DA, Luna JVCP, Cordeiro JB, Gonçalves Jr J, Lima MAP. Clinical and epidemiological aspects of scorpionism in the world: a systematic review. Wilderness Environ Med. 2016 Dec;27(4):504-18. ]. Ward [180180. Ward MJ, Ellsworth SA, Nystrom GS. A global accounting of medically significant scorpions: epidemiology, major toxins, and comparative resources in harmless counterparts. Toxicon. 2018 Sep 1;151:137-55. ] classified 104 species as potentially harmful (101 Buthidae, 2 Hemiscorpiidae and 1 Scorpionidae), but for only 32 of these fatalities were reported.

Ecological role of scorpion weapons in feeding, defense and intraspecific agonism

In this section we will review how both scorpion weapon systems are used in three main contexts of usage: feeding, defense and reproduction.

Scorpion weapons in feeding

Scorpions are nocturnal generalist predators feeding on a wide spectrum of different prey, consuming mostly arthropods, but also including small mammals and reptiles [128128. Polis GA. The biology of scorpions. Polis GA, editor. Stanford: University Stanford; 1990. ,181181. McCormick S, Polis GA. Arthropods that prey on vertebrates. Biol Rev. 1982;57:29-58.

182. Polis GA, McCormick SJ. Scorpions, spiders and solpugids: predation and competition among distantly related taxa. Oecologia. 1986 Dec;71(1):111-6.
-183183. Castilla AM. Interactions between lizards (Podarcis hispanica atrata) and scorpions (Buthus occitanus) in the Columbretes Islands. Bolleti la Soc d’Historia Nat les Balear. 1995;38:47-50. ]. To our knowledge, only two scorpion species are known to have a somewhat specialized diet, apparently preferring spiders as prey items [184184. Toscano-Gadea CA, Costa FG, State S, Province ER, Keyserling L, Costa L. Is Tityus uruguayensis (Buthidae) an araneophagic scorpion? An experimental analysis of its predatory behaviour on spiders and insects. Bull Br Arachnol Soc. 2006 Jan;13:256-64. ,185185. Main BY. Taxonomy and biology of the genus Isometroides Keyserling (Scorpionida). Aust J Zool. 1956;4:158-64. ]. Data about scorpion diet and feeding ecology in the wild is generally sparse [186186. Kaltsas D, Stathi I, Mylonas M. The foraging activity of Mesobuthus gibbosus (Scorpiones: Buthidae) in central and south Aegean archipelago. J Nat Hist. 2008 Jul 31;42:513-27.

187. Polis GA. Prey and feeding phenology of the desert sand scorpion Paruroctonus mesaensis (Scorpionidae: Vaejovidae). J Zool. 1979;188(3):333-46.

188. Miranda R, Bermúdez S, Cleghorn J, Cambra RA. Presas de escorpiones (Arachnida: Scorpiones) de Panamá, con observaciones sobre el comportamiento de depredación. Rev Ibérica Arachnol. 2015;27:115-23.

189. Rodríguez-Cabrera TM, Teruel R, Savall EM. Scorpion predation in Cuba: new cases and a review. Euscorpius. 2020;2020(306):1.

190. Mcreynolds CN. Effect of seasons and scorpion size on the foraging and diet of the striped bark scorpion , Centruroides vittatus ( Buthidae : Scorpiones ) in blackbrush habitat of south Texas. Euscorpius. 2020;2020(323):1-15.
-191191. Davison A, Brown T, Arrivillaga C. Notes on the diet and reproduction of the bark scorpion Centruroides gracilis (Scorpiones: Buthidae) on Utila Island, Honduras. Euscorpius. 2020;2020(314):1-7. ]. Therefore, most of the diet data is based on observations of wild or captive scorpions. Despite this lack of data about diet and feeding ecology, feeding behavior has been studied in almost all scorpion families. Scorpions have very limited vision [128128. Polis GA. The biology of scorpions. Polis GA, editor. Stanford: University Stanford; 1990. ] and prey localization mainly relies on the detection of vibrations and chemical cues. To detect soil-borne vibrations, scorpions rely on slit sensilla, which are mechanoreceptors present on the tarsi of their walking legs [192192. Barth FG, Wadepuhl M. Slit sense organs on the scorpion leg (Androctonus australis L., Buthidae). J. Morphol. 1975 Feb;145(2):209-27.

193. Brownell P, Farley RD. Detection of vibrations in sand by tarsal sense organs of the nocturnal scorpion, Paruroctonus mesaensis. J Comp Physiol A. 1979 Mar;131:23-30.

194. Brownell P, Farley RD. Prey-localizing behaviour of the nocturnal desert scorpion, Paruroctonus mesaensis: orientation to substrate vibrations. Anim Behav. 1979 Feb;27(1):185-93.

195. Brownell PH, Van Leo Hemmen J. Vibration sensitivity and a computational theory for prey-localizing behavior in sand scorpions. Am Zool. 2001;41(5):1229-40.
-196196. Couzjin HWC. Functional anatomy of the walking-legs of Scorpionida with remarks on terminology and homologization of leg segments. Netherlands J Zool. 1975 Jan 1;26(4):453-501. ], and the chemo-mechanic receptors on the pectines, which are also used to detect chemical cues [193193. Brownell P, Farley RD. Detection of vibrations in sand by tarsal sense organs of the nocturnal scorpion, Paruroctonus mesaensis. J Comp Physiol A. 1979 Mar;131:23-30. ,197197. Mineo MF, Del Claro K. Mechanoreceptive function of pectines in the Brazilian yellow scorpion Tityus serrulatus: perception of substrate-borne vibrations and prey detection. Acta Ethol. 2006 Oct 17;9:79-85.

198. Cloudsley-Thompson JL. On the function of the pectines of scorpions. Ann Mag Nat Hist. 1955;8:556-60.

199. Foelix RF, Müller-Vorholt G. The fine structure of scorpion sensory organs. II. Pecten sensilla. Bull Br Arachnol Soc. 1983 Jan 1;6(2):68-74.

200. Edmunds MC, Sibly RM. Optimal sting use in the feeding behavior of the scorpion Hadrurus spadix. J Arachnol. 2010 Apr;38:123-5.

201. Carthy JD. Fine structure and function of the sensory pegs on the scorpion pectine. Experientia. 1966;22:89.

202. Han Z, Chen D, Zhang K, Song H, Wang K, Niu S. Fine structure of scorpion pectines for odor capture. J Bionic Eng. 2017 Oct;14(4):589-99.

203. Wolf H. Scorpions pectines - Idiosyncratic chemo- and mechanosensory organs. Arthropod Struct Dev. 2017 Nov;46(6):753-64.

204. Warburg MR. Qualitative and quantitative analysis of intra-and interspecific behavioural patterns among scorpions qualitative analysis Nebo hierichonticus and Scorpio maurus fuscus. J Ethol. 1998;16:115-21.
-205205. Abushama FT. On the behaviour and sensory physiology of the scorpion Leiurus quinquestriatus. Anim Behav. 1964 Jan;12(1):140-53. ]. Scorpions seem not to use trichobothria to locate their prey by vibration (e.g. a walking prey) [206206. Murayama GP, Willemart RH. Are trichobothria used in terrestrial prey capture by the yellow scorpion Tityus serrulatus Lutz & Mello, 1922 (Buthidae)? Arachnology. 2019Dec;18(3):287-90. ].

Once the prey has been detected, scorpions always use their chelae to grab it. In experiments where both chelae were blocked with wax, scorpions managed to grasp the prey using only the chelicerae [207207. Colombo W. Behavior of Tityus serrulatus (Scorpiones, Buthidae) in captivity. Rev ibérica Aracnol. 2015;27:105-8. ], showing remarkable plasticity of their predatory behavior repertoire [208208. Simone Y, van der Meijden A, Garcia LF, Lacava M, Viera C. Analysis of predatory versatility in females of the scorpion Bothriurus bonariensis (Koch, 1842) (Scorpiones: Bothriuridae): overcoming prey with different defensive mechanisms. J Insect Behav. 2018;31:402-15. ]. Once the prey has been grasped, scorpions may or may not use the stinger to inject venom in their prey to subdue it [187187. Polis GA. Prey and feeding phenology of the desert sand scorpion Paruroctonus mesaensis (Scorpionidae: Vaejovidae). J Zool. 1979;188(3):333-46. ,209209. Rein JO. Prey capture behavior in the East African scorpions Parabuthus leiosoma (Ehrenberg, 1828) and P. pallidus Pocock, 1895 (Scorpiones: Buthidae). Euscorpius. 2003;1895(6):1-8.

210. Bub K, Bowerman RF. Prey capture by the scorpion Hadrurus arizonensis Ewing (Scorpiones: Vaejovidae). Am Arachnol Soc. 1979;7(3):243-53.

211. Casper G. Prey capture and stinging behavior in the emperor scorpion, Pandinus imperator (Koch)(Scorpiones, scorpionidae). J Arachnol. 1985;13(3):277-83.

212. Stahnke HL. Some aspects of scorpion behavior. Bull South Calif Acad Sci. 1966;65:65-80.
-213213. Rein JO. Sting use in two species of Parabuthus scorpions ( Buthidae ). J Arachnol. 1993;21(1):60-3. ]. Stinger use in scorpion feeding behavior is highly correlated with prey size [200200. Edmunds MC, Sibly RM. Optimal sting use in the feeding behavior of the scorpion Hadrurus spadix. J Arachnol. 2010 Apr;38:123-5. ,213213. Rein JO. Sting use in two species of Parabuthus scorpions ( Buthidae ). J Arachnol. 1993;21(1):60-3.

214. Pocock RI. Notes upon the habits of some living scorpions. Nature. 1893;48:104-7.
-215215. Rosin R, Shulow A. Studies on the scorpion Nebo hierochonticus. Proc Zool Soc London. 1963;140:547-75. ] and resistance [200200. Edmunds MC, Sibly RM. Optimal sting use in the feeding behavior of the scorpion Hadrurus spadix. J Arachnol. 2010 Apr;38:123-5. ,209209. Rein JO. Prey capture behavior in the East African scorpions Parabuthus leiosoma (Ehrenberg, 1828) and P. pallidus Pocock, 1895 (Scorpiones: Buthidae). Euscorpius. 2003;1895(6):1-8. ,212212. Stahnke HL. Some aspects of scorpion behavior. Bull South Calif Acad Sci. 1966;65:65-80. ,216216. Albín A, Toscano-Gadea CA. Predation among armored arachnids: Bothriurus bonariensis (Scorpions, Bothriuridae) versus four species of harvestmen (Harvestmen, Gonyleptidae). Behav Processes. 2015 Dec;121:1-7. ], ontogenetic state of the scorpion [211211. Casper G. Prey capture and stinging behavior in the emperor scorpion, Pandinus imperator (Koch)(Scorpiones, scorpionidae). J Arachnol. 1985;13(3):277-83. ,217217. Cushing BS, Matherne A. Stinger utilization and predation in the scorpion Paruroctonus boreus. Gt Basin Nat. 1980;40(2):193-5. ] and chela morphology, with species with robust chelae seldom using the stinger to subdue their prey, using only crushing force to incapacitate the prey [211211. Casper G. Prey capture and stinging behavior in the emperor scorpion, Pandinus imperator (Koch)(Scorpiones, scorpionidae). J Arachnol. 1985;13(3):277-83. ,212212. Stahnke HL. Some aspects of scorpion behavior. Bull South Calif Acad Sci. 1966;65:65-80. ,218218. Mcdaniel M. Notes on the biology of California scorpions. Entomol News. 1968 Oct;79(8):278-84.

219. Schultze W. Biology of the large Philippine forest scorpion. Philipp J Sci. 1927;32(3):375-90.

220. Williams SC. Scorpion bionomics. Annu Rev Entomol. 1987;32:275-95.
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When a scorpion stings the prey, the telson is projected anteriorly with the metasoma, and the aculeus repeatedly touched to the body of the prey until a soft spot suitable for piercing is found [5252. van der Meijden A, Kleinteich T. A biomechanical view on stinger diversity in scorpions. J Anat. 2017 Apr;230(4):497-509. ,187187. Polis GA. Prey and feeding phenology of the desert sand scorpion Paruroctonus mesaensis (Scorpionidae: Vaejovidae). J Zool. 1979;188(3):333-46. ,210210. Bub K, Bowerman RF. Prey capture by the scorpion Hadrurus arizonensis Ewing (Scorpiones: Vaejovidae). Am Arachnol Soc. 1979;7(3):243-53. ,216216. Albín A, Toscano-Gadea CA. Predation among armored arachnids: Bothriurus bonariensis (Scorpions, Bothriuridae) versus four species of harvestmen (Harvestmen, Gonyleptidae). Behav Processes. 2015 Dec;121:1-7. ,222222. Fabre JH. The life of the scorpion. Dodd M, editor. New York: Dodd, Mead and Co; 1923. ,223223. Sarhan M, Sayed AB, Mostafa MA, Yasin AE. Prey-capture behaviour of the Egyptian scorpion Scorpio maurus palmatus (Ehrenberg, 1828) (Scorpiones: Scorpionidae). Serket. 2013;13:201-10. ]. Several authors described that after the first sting, scorpions remain motionless for several minutes, most likely waiting for the neurotoxic effects of the injected venom [200200. Edmunds MC, Sibly RM. Optimal sting use in the feeding behavior of the scorpion Hadrurus spadix. J Arachnol. 2010 Apr;38:123-5. ,210210. Bub K, Bowerman RF. Prey capture by the scorpion Hadrurus arizonensis Ewing (Scorpiones: Vaejovidae). Am Arachnol Soc. 1979;7(3):243-53. ,223223. Sarhan M, Sayed AB, Mostafa MA, Yasin AE. Prey-capture behaviour of the Egyptian scorpion Scorpio maurus palmatus (Ehrenberg, 1828) (Scorpiones: Scorpionidae). Serket. 2013;13:201-10. ,224224. Stewart AK. Observations on prey-capture behavior of Androctonus crassicauda (Olivier, 1807) (Scorpiones: Buthidae) in northern Iraq. Euscorpius. 2006;2006(37)1. ]. If the prey keeps struggling, further stinging events can be observed [208208. Simone Y, van der Meijden A, Garcia LF, Lacava M, Viera C. Analysis of predatory versatility in females of the scorpion Bothriurus bonariensis (Koch, 1842) (Scorpiones: Bothriuridae): overcoming prey with different defensive mechanisms. J Insect Behav. 2018;31:402-15. ,223223. Sarhan M, Sayed AB, Mostafa MA, Yasin AE. Prey-capture behaviour of the Egyptian scorpion Scorpio maurus palmatus (Ehrenberg, 1828) (Scorpiones: Scorpionidae). Serket. 2013;13:201-10. ,225225. Southcott R V. Some observations on the biology, including mating and other behavior, of the Australian scorpion Urodacus abruptus Pocock. Trans R Soc South Aust. 1955;78:145-54. ]. Once the prey is successfully incapacitated, scorpions use their chelae to further manipulate it, with several studies showing that scorpions prefer to orient the prey with the head towards their chelicerae before starting to consume it [187187. Polis GA. Prey and feeding phenology of the desert sand scorpion Paruroctonus mesaensis (Scorpionidae: Vaejovidae). J Zool. 1979;188(3):333-46. ,210210. Bub K, Bowerman RF. Prey capture by the scorpion Hadrurus arizonensis Ewing (Scorpiones: Vaejovidae). Am Arachnol Soc. 1979;7(3):243-53. ,219219. Schultze W. Biology of the large Philippine forest scorpion. Philipp J Sci. 1927;32(3):375-90. ,223223. Sarhan M, Sayed AB, Mostafa MA, Yasin AE. Prey-capture behaviour of the Egyptian scorpion Scorpio maurus palmatus (Ehrenberg, 1828) (Scorpiones: Scorpionidae). Serket. 2013;13:201-10. ,226226. Alexander A. Feeding behavior in scorpions. S Afr J Sci. 1972;68:253-6. ].

The venom is mainly used for prey incapacitation rather than killing the prey. In many insect prey, the loss of muscle control subsequent to scorpion venom injection is evident [227227. Zlotkin E, Kadouri D, Gordon D, Pelhate M, Martin MF, Rochat H. An excitatory and a depressant insect toxin from scorpion venom both affect sodium conductance and possess a common binding site. Arch Biochem Biophys. 1985 Aug 1;240(2):877-87.

228. Zlotkin E. Pharmacology of survival: insect selective neurotoxins derived from scorpion venom. Endeavour. 1987;11(4):168-74.
-229229. Eitan M, Fowler E, Herrmann R, Duval A, Pelhate M, Zlotkin E. A scorpion venom neurotoxin paralytic to insects that affects sodium current inactivation: purification, primary structure, and mode of action. Biochemistry. 1990;29(25):5941-7. ]. Two different types of paralysis induced by the injection of scorpion venom have been described: one is characterized by involuntary contractions of the muscles, while the other is a flaccid paralysis through inhibition of muscle contractions [230230. Zlotkin E, Fraenkel G, Miranda F, Lissitzky S. The effect of scorpion venom on blowfly larvae - A new method for the evaluation of scorpion venoms potency. Toxicon. 1971 Jan;9(1):1-2. ]. These neurotoxic effects are mainly provoked by toxins with high affinity to ion-binding voltage-gated channels [135135. Possani LD, Becerril B, Delepierre M, Tytgat J. Scorpion toxins specific for Na+ channels. Eur J Biochem. 1999 Sep;264(2):287-300. ,136136. Quintero-Hernández V, Jiménez-Vargas JM, Gurrola GB, Valdivia HH, Possani LD. Scorpion venom components that affect ion-channels function. Toxicon. 2013 Dec 15;76:328-42. ,168168. Zhang S, Gao B, Zhu S. Target-driven evolution of scorpion toxins. Sci Rep. 2015;5(14973):1-13. ,231231. Arnon T, Potikha T, Sher D, Elazar M, Mao W, Tal T, Bosmans F, Tytgat J, Ben-Arie N, Zlotkin E. BjαIT: a novel scorpion α-toxin selective for insects - Unique pharmacological tool. Insect Biochem Mol Biol. 2005 Mar;35(3):187-95.

232. Liu L-H, Bosmans F, Maertens C, Zhu R-H, Wang D-C, Tytgat J. Molecular basis of the mammalian potency of the scorpion α‐like toxin, BmK M1. FASEB J. 2005 Apr;19(6):1-24.

233. Gordon D, Martin-Eauclaire MF, Cestèle S, Kopeyan C, Carlier E, Khalifa RB, Pelhate M, Rochat H. Scorpion toxins affecting sodium current inactivation bind to distinct homologous receptor sites on rat brain and insect sodium channels. J Biol Chem. 1996 Apr 5;271(14):8034-45.

234. Gurevitz M, Karbat I, Cohen L, Ilan N, Kahn R, Turkov M, Stankiewicz M, Stuhmer W, Dong K, Gordon D. The insecticidal potential of scorpion β-toxins. Toxicon. 2007 Mar 15;49(4):473-89.

235. Strugatsky D, Zilberberg N, Stankiewicz M, Ilan N, Turkov M, Cohen L, Pelhate M, Gilles N, Gordon D, Gurevitz M. Genetic polymorphism and expression of a highly potent scorpion depressant toxin enable refinement of the effects on insect Na channels and lluminate the key role of Asn-58. Biochemistry. 2005 Jun 28;44(25):9179-87.
-236236. Cohen L, Troub Y, Turkov M, Gilles N, Ilan N, Benveniste M, Gordon D, Gurevitz M. Mammalian skeletal muscle voltage-gated sodium channels are affected by scorpion depressant “insect-selective” toxins when preconditioned. Mol Pharmacol. 2007 Nov;72(5):1220-7. ]. Within the members of the two main families of NaScTx, for example, we can find specific toxins that are highly toxic only to insects [229229. Eitan M, Fowler E, Herrmann R, Duval A, Pelhate M, Zlotkin E. A scorpion venom neurotoxin paralytic to insects that affects sodium current inactivation: purification, primary structure, and mode of action. Biochemistry. 1990;29(25):5941-7. ,237237. Borchani L, Stankiewicz M, Kopeyan C, Mansuelle P, Kharrat R, Cestèle S, Karoui H, Rochat H, Pelhate M, el Ayeb M. Purification, structure and activity of three insect toxins from Buthus occitanus tunetanus venom. Toxicon. 1997 Mar;35(3):365-82. ,238238. Froy O, Zilberberg N, Gordon D, Turkov M, Gilles N, Stankiewicz M, Pelhaate M, Loret E, Oren DA, Shaanan B, Gurevitz M. The putative bioactive surface of insect-selective scorpion excitatory neurotoxins. J Biol Chem. 1999 Feb 26;274(9):5769-76. ], toxins that have a high affinity to murine sodium voltage-gated channels [233233. Gordon D, Martin-Eauclaire MF, Cestèle S, Kopeyan C, Carlier E, Khalifa RB, Pelhate M, Rochat H. Scorpion toxins affecting sodium current inactivation bind to distinct homologous receptor sites on rat brain and insect sodium channels. J Biol Chem. 1996 Apr 5;271(14):8034-45. ,239239. Legros C, Céard B, Vacher H, Marchot P, Bougis PE, Martin-Eauclaire MF. Expression of the standard scorpion alpha-toxin AaH II and AaH II mutants leading to the identification of some key bioactive elements. Biochim Biophys Acta. 2005 May 25;1723(1-3):91-9. ,240240. Jover E, Martin-Moutot N, Couraud F, Rochat H. Scorpion toxins: specific binding to rat synaptosomes. Biochem Biophys Res Commun. 1978 Nov 14;85(1):377-82. ], and toxins that show similar affinity for both insect and murine ion channels [241241. Kopeyan C, Mansuelle P, Martin‐Eauclaire MF, Rochat H, Miranda F. Characterization of toxin III of the scorpion Leiurus quinquestriatus quinquestriatus: a new type of alpha‐toxin highly toxic both to mammals and insects. Nat Toxins. 1993;1(5):308-12. ,242242. Gordon D, Ilan N, Zilberberg N, Gilles N, Urbach D, Cohen L, Karbat I, Froy O, Gaathon A, Roland G, Benveniste M. An “Old World” scorpion β-toxin that recognizes both insect and mammalian sodium channels: a possible link towards diversification of β-toxins. Eur J Biochem. 2003;270(12):2663-70. ]. This differential affinity of venom compounds, and the fact that scorpions are both prey and predators, can potentially explain the differences in toxicity that scorpion venom have on different target organisms [243243. van der Meijden A, Koch B, van der Valk T, Vargas‐Muñoz LJ, Estrada-Gómez S. Target‐specificity in scorpions; comparing lethality of scorpion venoms across arthropods and vertebrates. Toxins. 2017 Oct 4;9(10):312. ]. The calculation of the median lethal dose (LD50), the dose of a venom needed to kill 50% of the test population, is a technique widely used to quantify venom potency [244244. Trevan JW. Error of determination of toxicity. Proc R Soc B. 1927;101:483-514. ]. As scorpions are both prey and predators, measuring the LD50 on different target organisms is needed to investigate the toxicity of scorpion venom for both defensive and offensive purposes. Zlotkin et al. [230230. Zlotkin E, Fraenkel G, Miranda F, Lissitzky S. The effect of scorpion venom on blowfly larvae - A new method for the evaluation of scorpion venoms potency. Toxicon. 1971 Jan;9(1):1-2. ] calculated the LD50 of the venom of several species of Buthids on two different target organisms, and found that when venom from the species Buthus occitanus paris (Buthidae) was injected into fly larvae, the LD50 calculated was the lowest (i.e., highest toxicity), while the same species had the highest LD50 in mice. Similar results have been provided by numerous other studies [241241. Kopeyan C, Mansuelle P, Martin‐Eauclaire MF, Rochat H, Miranda F. Characterization of toxin III of the scorpion Leiurus quinquestriatus quinquestriatus: a new type of alpha‐toxin highly toxic both to mammals and insects. Nat Toxins. 1993;1(5):308-12. ,243243. van der Meijden A, Koch B, van der Valk T, Vargas‐Muñoz LJ, Estrada-Gómez S. Target‐specificity in scorpions; comparing lethality of scorpion venoms across arthropods and vertebrates. Toxins. 2017 Oct 4;9(10):312. ,245245. van der Valk T, van der Meijden A. Toxicity of scorpion venom in chick embryo and mealworm assay depending on the use of the soluble fraction versus the whole venom. Toxicon. 2014 Sep;88:38-43.

246. Zlotkin E, Rochat H, Kopeyan, Miranda F, Lissitzky S. Purification and properties of the insect toxin from the venom of the scorpion Androctonus australis Hector. Biochimie. 1971;53(10):1073-8.
-247247. Zhu L, Peigneur S, Gao B, Zhang S, Tytgat J, Zhu S. Target-driven positive selection at hot spots of scorpion toxins uncovers their potential in design of insecticides. Mol Biol Evol. 2016 Aug;33(8):1907-20. ], showing that LD50 results are only indicative of relative toxicity in the species that was tested, and provide little indication of toxicity in other, even relatively closely related species. Studies on the ecological relevance of scorpion venom should therefore be carried out on the presumed natural target species.

Venom is considered a fast-changing phenotype [248248. Amazonas DR, Freitas-De-Sousa LA, Orefice DP, de Sousa LF, Martinez MG, Mourão RHV, Chalkidis HM, Camargo PB, Moura-da-Silva AM. Evidence for snake venom plasticity in a long-term study with individual captive Bothrops atrox. Toxins. 2019 May;11(5):294. ]. Snake venom, for example, has been seen to change in composition depending on factors like alterations in the animal’s physiological state and diet [249249. Mackessy SP. Evolutionary trends in venom composition in the Western Rattlesnakes (Crotalus viridis sensu lato): toxicity vs. tenderizers. Toxicon. 2010 Jul;55(8):1463-74. ,250250. Casewell NR, Jackson TNW, Laustsen AH, Sunagar K. Causes and consequences of snake venom variation. Trends Pharmacol Sci. 2020 Aug;41(8):570-81. ]. In recent years, changes in scorpion venom composition and production following diet alterations have been recorded [251251. Pucca MB, Amorim FG, Cerni FA, Bordon KDCF, Cardoso IA, Anjolette FAP, Arantes EC. Influence of post-starvation extraction time and prey-specific diet in Tityus serrulatus scorpion venom composition and hyaluronidase activity. Toxicon. 2014 Nov;90:326-36. ,252252. Tobassum S, Tahir HM, Zahid MT, Gardner QA, Ahsan MM. Effect of milking method, diet, and temperature on venom production in scorpions. J Insect Sci. 2018 Jul;18(4):1-7. ]. Pucca [251251. Pucca MB, Amorim FG, Cerni FA, Bordon KDCF, Cardoso IA, Anjolette FAP, Arantes EC. Influence of post-starvation extraction time and prey-specific diet in Tityus serrulatus scorpion venom composition and hyaluronidase activity. Toxicon. 2014 Nov;90:326-36. ] observed different peaks in venom profiles obtained from scorpions belonging to the same species fed with different types of prey, suggesting rapid adaptation of venom composition to different prey types. Similarly, Tobassum et al. [252252. Tobassum S, Tahir HM, Zahid MT, Gardner QA, Ahsan MM. Effect of milking method, diet, and temperature on venom production in scorpions. J Insect Sci. 2018 Jul;18(4):1-7. ] divided scorpions belonging to the same species into groups and fed each group with a different type of prey, observing significant differences in the volume of venom extracted from each group after the same starvation period, suggesting that some prey items are preferable when higher volume of milked venom is required.

In the species Centruroides vittatus (Buthidae), venom toxicity and composition change depending on the ontogenetic state of the animals. Juveniles appear to have less deadly (higher LD50) venom than the adults, at least when using crickets as a target species. This may be mediated by a quantitative rather than qualitative change in expression of the different toxins with ontogenetic state [253253. McElroy T, McReynolds CN, Gulledge A, Knight KR, Smith WE, Albrecht EA. Differential toxicity and venom gland gene expression in Centruroides vittatus. PLoS One. 2017;12(10):1-17. ]. Additionally, scorpions may select different prey according to the amount of venom in their venom glands. Scorpions from which the venom was extracted less than 24 hours before, avoided feeding on larger prey [254254. Silva MA, Silva NA, Lira AFA, Martins RD. Role of venom quantity in the feeding behavior of Jaguajir rochae (Scorpiones: Buthidae). Acta Ethol. acta ethologica; 2019 Mar 9;22:99-104. ].

In other pincered taxa, feeding ecology is an important driver for the evolution of the weapons that first touches the food. In decapods (Crustacea) for example, diet seems to be the main factor determining differences in chela morphology and size [9696. Yamada SB, Boulding EG. Claw morphology, prey size selection and foraging efficiency in generalist and specialist shell-breaking crabs. J Exp Mar Biol Ecol. 1998 Feb 1;220(2):191-211. ,255255. Elner W, Campbell A. Force, function and mechanical advantage in the chelae of the american lobster Homarus americanus (Decapoda: Crustacea). J Zool. 1981 Feb;193(2):269-86.

256. Vermeij GJ. Patterns in crab claw size: the geography of crushing. Syst Biol. 1977;26(2):138-51.

257. Taylor GM. The evolution of armament strength: evidence for a constraint on the biting performance of claws of durophagous Decapods. Evolution. 2001 Mar;55(3):550-60.
-258258. Seed R, Hughes RN. Criteria for prey size-selection in molluscivorous crabs with contrasting claw morphologies. J Exp Mar Bio Ecol. 1995 Nov;193(1-2):177-95. ]. In scorpions, no clear evidence of a similar correlation has been provided yet. However, there may be some rationale to consider diet as a possible driver of scorpion chela evolution. Between different scorpion families, and sometimes even between species belonging to the same genus, chela shape can range from having a stout and robust manus and short fingers to a very slender manus and elongated fingers (Figure 4). Such differences in shape are highly correlated with differences in performance. Pinch force in scorpion species with stouter chelae is much higher than that measured in species having slender chelae [259259. van der Meijden A, Herrel A, Summers A. Comparison of chela size and pincer force in scorpions; getting a first grip. J Zool. 2010;280:319-25. ]. The strongest species also have thicker cuticle [260260. Kellersztein I, Cohen SR, Bar-On B, Wagner HD. The exoskeleton of scorpions’ pincers: structure and micro-mechanical properties. Acta Biomater. 2019 Aug;94:565-73. ], probably to withstand the higher stress generated during maximum bite force [261261. van der Meijden A, Kleinteich T, Coelho P. Packing a pinch: functional implications of chela shapes in scorpions using finite element analysis. J Anat. 2012 May;220(5):423-34. ]. Rupturing the exoskeleton of hard-bodied prey requires exerting a significant amount of force, a feat that scorpions with slender chelae may not be able to accomplish without risking breaking their fingers [261261. van der Meijden A, Kleinteich T, Coelho P. Packing a pinch: functional implications of chela shapes in scorpions using finite element analysis. J Anat. 2012 May;220(5):423-34. ]. Lamoral [262262. Lamoral B. Predation on terrestrial molluscs by scorpions in the Kalahari Desert. Ann Natal Museum. 1971;21(1):17-20. ] reported Opistophthalmus carinatus (Scorpionidae), a very stout-pincered scorpion, sporadically feeding on terrestrial hard-shelled crustaceans when no other food source is available. Baerg [263263. Baerg WJ. Regarding the biology of the common Jamaican scorpion. Ann Entomol Soc Am. 1954 Jun 1;47(2):272-6. ] reported that the fine-pincered Centruroides insulanus (Buthidae) feeds on scarab beetles only if these are deprived of the hard elytra. It therefore seems that chela morphology, via performance, may limit feeding on harder prey.

Figure 4.
Three-dimensional graph showing the relationships between chela morphology and performance. On the X axis is the pinch force (corrected for overall body size), on the Y axis the size-corrected finger length and on the Z axis the size-corrected maximum closing speed of the chela. A representative member of each family is shown in the legend: Hottentotta gentili (Buthidae), Caraboctonus keyserlingi (Caraboctonidae), Pandinoides cavimanus (Scorpionidae), Hadogenes paucidens (Hemiscorpiidae), Bothriurus chilensis (Bothriuridae). Species with relatively longer fingers are faster but also weaker than species having shorter fingers. Since the variables have been corrected for overall body size, no units can be given with the axes.

Whereas in scorpions robust and slender chelae occur in separate species or sexes (see below), in several members of the order Decapoda (Crustacea), a single individual can have one robust (the “crusher”) and one slender chela (the “cutter”) [264264. Govind CK. Asymmetry in lobster claws. Am Sci. 1989 Sep-Oct;77(5):468-74.

265. Brown SC, Cassuto SR, Loos RW. Biomechanics of chelipeds in some decapod crustaceans. J Zool. 1979;188(2):143-59.
-266266. Schenk SC, Wainwright PC. Dimorphism and the functional basis of claw strength in six brachyuran crabs. J Zool. 2001 Aug;255:105-19. ]. The crusher chela produces a larger pinch force than the cutter, and is mainly used to crack and break the hard shells of the prey, while the cutter chela is mainly used for feeding and prey manipulation [256256. Vermeij GJ. Patterns in crab claw size: the geography of crushing. Syst Biol. 1977;26(2):138-51. ]. Decapod species feeding on motile, soft-bodied prey, have more elongated and slender chelae [258258. Seed R, Hughes RN. Criteria for prey size-selection in molluscivorous crabs with contrasting claw morphologies. J Exp Mar Bio Ecol. 1995 Nov;193(1-2):177-95. ]. A similar functional specialization may underlie the chela diversity seen in scorpions. Although scorpions do not have different chela morphologies within one individual as some decapods do, the shape of the chelae can differ between sexes and between species. As in decapods feeding on more fleeting and soft-bodied prey, long chelae may aid in prey prehension by allowing a larger gape at the same opening angle, and a higher closing speed of the tips of the fingers, all else being equal. From consideration of lever mechanics, longer fingers (i.e. a longer out-lever) provide a lower mechanical advantage, therefore less force is transmitted from chela muscles to the tip of the movable finger. We recently found a negative correlation between pinch force and chela closing speed [267267. Simone Y, van der Meijden A. Fast and fine versus strong and stout: a trade-off between chela closing force and speed across nine scorpion species. Biol J Linn Soc. 2018 Jan;123(1):208-17. ], which means that species with a stronger grip are also slower (Figure 4). Faster chelae may be a suitable weapon to hunt fast prey, but lever mechanics limits the maximum pinch force, and thus restricts the bearer to soft rather than hard-bodied prey. The negative relationship between chela pinch force and closing speed may thus be a functional trade-off [268268. Arnold AS, Richards CT, Ros IG, Biewener AA. There is always a trade-off between speed and force in a lever system: comment on McHenry (2010). Biol Lett. 2011 Dec 23;7(6):878-9. ] and allows, or may even be driven by, niche partitioning between different species of scorpions.

Defensive behavior

The chelae and the venom delivery system are not only useful weapons for apprehending and incapacitating prey, but are also very efficient weapons employed in active defense. Experimentally eliciting a defensive response in scorpions can be simple: disturbing a scorpion is usually enough to cause it to show defensive behavior [2424. van der Meijden A, Coelho PL, Sousa P, Herrel A. Choose your weapon: defensive behavior is associated with morphology and performance in scorpions. PLoS One. 2013 Nov 13;8(11):e78955. ,269269. Coelho P, Kaliontzopoulou A, Rasko M, van der Meijden A. A ‘striking’ relationship: scorpion defensive behaviour and its relation to morphology and performance. Funct Ecol. 2017 Apr 3;31(7):1390-1404.

270. Palka J, Babu KS. Toward the physiological analysis of defensive responses of scorpions. Z Vgl Physiol. 1967;55:286-98.
-271271. Miller DW, Jones AD, Goldston JS, Rowe MP, Rowe AH. Sex differences in defensive behavior and venom of the striped bark scorpion Centruroides vittatus (Scorpiones: Buthidae). Integr Comp Biol. 2016 Nov;56(5):1022-31. ], and the most excitable species just need to feel a puff of air to elicit stinging behavior [4545. Nisani Z, Hayes WK. Venom-spraying behavior of the scorpion Parabuthus transvaalicus (arachnida: Buthidae). Behav Processes. 2015 Jun;115:46-52. ]. A more intense attack may be simulated by touching crucial body parts, such as the prosoma [272272. Nisani Z, Hayes WK. Defensive stinging by Parabuthus transvaalicus scorpions: risk assessment and venom metering. Anim Behav. 2011 Mar;81(3):627-33.

273. van der Meijden A, Coelho P, Rasko M. Variability in venom volume, flow rate and duration in defensive stings of five scorpion species. Toxicon. 2015 Jun 15;100:60-6.
-274274. Rasko M, Coelho P, Simone Y, van der Meijden A. How to attack a scorpion: venom metering during a repeated attack. Anim Behav. 2018 Nov;145:125-9. ]. Defensive behavior has been shown to differ between species [2424. van der Meijden A, Coelho PL, Sousa P, Herrel A. Choose your weapon: defensive behavior is associated with morphology and performance in scorpions. PLoS One. 2013 Nov 13;8(11):e78955. ,4646. Newlands G. Scorpion defensive behavior. African Wildl. 1969;23:147-53. ,204204. Warburg MR. Qualitative and quantitative analysis of intra-and interspecific behavioural patterns among scorpions qualitative analysis Nebo hierichonticus and Scorpio maurus fuscus. J Ethol. 1998;16:115-21. ], perceived threat level [275275. Lira AFA, Santos AB, Silva NA, Martins RD. Threat level influences the use of venom in a scorpion species, Tityus stigmurus (Scorpiones, Buthidae). Acta Ethol. 2017 Aug 3;20(2017):291-95. ,276276. Nelsen DR, David EM, Harty CN, Hector JB, Corbit AG. Risk assessment and the effects of refuge availability on the defensive behaviors of the southern unstriped scorpion (Vaejovis carolinianus). Toxins. 2020 Aug 20;12(9):1-21. ] and sex [271271. Miller DW, Jones AD, Goldston JS, Rowe MP, Rowe AH. Sex differences in defensive behavior and venom of the striped bark scorpion Centruroides vittatus (Scorpiones: Buthidae). Integr Comp Biol. 2016 Nov;56(5):1022-31. ,277277. Carlson BE, McGinley S, Rowe MP. Meek males and fighting females: sexually-dimorphic antipredator behavior and locomotor performance is explained by morphology in bark scorpions (Centruroides vittatus). PLoS One. 2014 May 28;9(5):e97648. ,278278. Lira AFA, Almeida FMF, Albuquerque CMR. Reaction under the risk of predation: effects of age and sexual plasticity on defensive behavior in scorpion Tityus pusillus (Scorpiones: Buthidae). J Ethol. 2020 Aug;38(1):13-9. ].

It is important to point out that defensive stinging is very different from predatory stinging [5252. van der Meijden A, Kleinteich T. A biomechanical view on stinger diversity in scorpions. J Anat. 2017 Apr;230(4):497-509. ,269269. Coelho P, Kaliontzopoulou A, Rasko M, van der Meijden A. A ‘striking’ relationship: scorpion defensive behaviour and its relation to morphology and performance. Funct Ecol. 2017 Apr 3;31(7):1390-1404. ]. Defensive strikes are much faster than predatory ones, and do not include the exploratory touching described above. Depending on metasoma morphology, a defensive strike can have an open or folded trajectory [269269. Coelho P, Kaliontzopoulou A, Rasko M, van der Meijden A. A ‘striking’ relationship: scorpion defensive behaviour and its relation to morphology and performance. Funct Ecol. 2017 Apr 3;31(7):1390-1404. ]. Species with a muscular or elongated metasoma tend to be faster and have a more open trajectory. Closed trajectories have been observed in species having shorter pedipalps. However, comparative motion shape analysis is in its infancy, and the reasons for these differences in trajectory shape between species are not yet understood.

Likewise, defensive pinching behavior seems to be different from the predatory grasping of prey. Whereas all scorpions always use their chelae in prey prehension, not all species use their chelae in every defensive case, but sometimes limit their defensive response to stinging only [2424. van der Meijden A, Coelho PL, Sousa P, Herrel A. Choose your weapon: defensive behavior is associated with morphology and performance in scorpions. PLoS One. 2013 Nov 13;8(11):e78955. ]. Warburg [204204. Warburg MR. Qualitative and quantitative analysis of intra-and interspecific behavioural patterns among scorpions qualitative analysis Nebo hierichonticus and Scorpio maurus fuscus. J Ethol. 1998;16:115-21. ] recorded scorpions belonging to different families fight each other to observe the different strategies used in intraguild competition and predation. He observed that scorpion species that have strong chelae rarely used their stinger and were less prone to sting, while species with slenderer chelae controlled the opponent with the chelae but were always searching for a suitable spot to sting. This may indicate some functional trade-off or compensation in defensive use. Some scorpion species use their stout chelae as protective shields, placing them in front of the chelicerae to protect the head from frontal attacks [4646. Newlands G. Scorpion defensive behavior. African Wildl. 1969;23:147-53. ,279279. Harington A. Burrowing biology of the scorpion Cheloctonus jonesii Pockock (Arachnida: Scorpionida: Scorpionidae). J Arachnol. 1978;5(3):243-9. ]. Some of these species are burrowers and rock crevice-dwellers, and use their large chelae to prevent unwelcome visitors to access their burrow [4646. Newlands G. Scorpion defensive behavior. African Wildl. 1969;23:147-53. ].

The use of weapons in defensive behavior is correlated with the perceived threat level and may be different between the two sexes. A more intense threat tends to increase the frequency of defensive stinging [275275. Lira AFA, Santos AB, Silva NA, Martins RD. Threat level influences the use of venom in a scorpion species, Tityus stigmurus (Scorpiones, Buthidae). Acta Ethol. 2017 Aug 3;20(2017):291-95. ,276276. Nelsen DR, David EM, Harty CN, Hector JB, Corbit AG. Risk assessment and the effects of refuge availability on the defensive behaviors of the southern unstriped scorpion (Vaejovis carolinianus). Toxins. 2020 Aug 20;12(9):1-21. ,278278. Lira AFA, Almeida FMF, Albuquerque CMR. Reaction under the risk of predation: effects of age and sexual plasticity on defensive behavior in scorpion Tityus pusillus (Scorpiones: Buthidae). J Ethol. 2020 Aug;38(1):13-9. ,280280. Nisani Z, Curiel R. Antipredator responses of Hadrurus arizonensis (Scorpiones: Caraboctonidae) to chemosensory cue from a mammalian predator. J Arachnol. 2019;47(3):389-91. ] and, in some cases, also the volume of venom delivered ([272272. Nisani Z, Hayes WK. Defensive stinging by Parabuthus transvaalicus scorpions: risk assessment and venom metering. Anim Behav. 2011 Mar;81(3):627-33. ]. However, the opposite trend has also been recorded [274274. Rasko M, Coelho P, Simone Y, van der Meijden A. How to attack a scorpion: venom metering during a repeated attack. Anim Behav. 2018 Nov;145:125-9. ]. In this study, the authors tested how the scorpion, Hadrurus arizonensis (Caraboctonidae), applied its venom defensively during a simulated repeated attack, consisting of 10 consecutive challenges. They found that, surprisingly, the tested specimens invested more venom in the early phases of the threat and that the average volume delivered after 10 consecutive stings was only the 8% of the total yield obtained prior to the beginning of the experiments. Inter-sexual differences have been reported in scorpion defensive behavior. In the sexually dimorphic species Centruroides vittatus (Buthidae), females show higher stinging frequency than males when the metasoma was grabbed to elicit a defensive response [277277. Carlson BE, McGinley S, Rowe MP. Meek males and fighting females: sexually-dimorphic antipredator behavior and locomotor performance is explained by morphology in bark scorpions (Centruroides vittatus). PLoS One. 2014 May 28;9(5):e97648. ]. However, comparable experiments performed with the similarly sexually dimorphic species Tityus pusillus (Buthidae) and Vaejovis carolinianus (Vaejovidae) showed no differences in stinging frequency between sexes [276276. Nelsen DR, David EM, Harty CN, Hector JB, Corbit AG. Risk assessment and the effects of refuge availability on the defensive behaviors of the southern unstriped scorpion (Vaejovis carolinianus). Toxins. 2020 Aug 20;12(9):1-21. ,278278. Lira AFA, Almeida FMF, Albuquerque CMR. Reaction under the risk of predation: effects of age and sexual plasticity on defensive behavior in scorpion Tityus pusillus (Scorpiones: Buthidae). J Ethol. 2020 Aug;38(1):13-9. ].

The defensive sting is known to sometimes take place without any venom expenditure (a “dry sting”). Dry stings are reported in different venomous taxa and associated with defensive behavior [281281. Naik BS. “Dry bite” in venomous snakes: a review. Toxicon. 2017 Jul;133:63-7.

282. Herzig V. Ontogenesis, gender, and molting influence the venom yield in the spider Coremiocnemis tropix (Araneae, Theraphosidae). J Venom Res. 2010 Dec 15;1:76-83.
-283283. Pucca MB, Knudsen C, Oliveira IS, Rimbault C, Cerni FA, Wen FH, Sachett J, Sartim MA, Laustsen AH, Monteiro WM. Current knowledge on snake dry bites. Toxins (Basel). 2020 Oct 22;12(11):668. ]. Even if venom is an efficient weapon in defense, it comes with a high energetic cost and its expenditure has to be carefully metered [284284Morgenstern D, King GF. The venom optimization hypothesis revisited. Toxicon. 2013 Mar 1;63:120-8. ]. Replenishment of the venom glands increases metabolic rate by 21% to 39% for a minimum of 72 hours [285285. Nisani Z, Dunbar SG, Hayes WK. Cost of venom regeneration in Parabuthus transvaalicus (Arachnida: Buthidae). Comp Biochem Physiol A Mol Integr Physiol. 2007 Jun;147(2):509-13. ,286286. Nisani Z, Boskovic DS, Dunbar SG, Kelln W, Hayes WK. Investigating the chemical profile of regenerated scorpion (Parabuthus transvaalicus) venom in relation to metabolic cost and toxicity. Toxicon. 2012 Sep 1;60(3):315-23. ]. This may temporarily make the scorpion a less-efficient predator and makes it more vulnerable to potential attackers [254254. Silva MA, Silva NA, Lira AFA, Martins RD. Role of venom quantity in the feeding behavior of Jaguajir rochae (Scorpiones: Buthidae). Acta Ethol. acta ethologica; 2019 Mar 9;22:99-104. ,275275. Lira AFA, Santos AB, Silva NA, Martins RD. Threat level influences the use of venom in a scorpion species, Tityus stigmurus (Scorpiones, Buthidae). Acta Ethol. 2017 Aug 3;20(2017):291-95. ,285285. Nisani Z, Dunbar SG, Hayes WK. Cost of venom regeneration in Parabuthus transvaalicus (Arachnida: Buthidae). Comp Biochem Physiol A Mol Integr Physiol. 2007 Jun;147(2):509-13. ]. Dry stings, by inflicting pain through mechanical damage, may therefore save the energetically costly resource of venom, while still delivering a painful warning [1111. Anderson PSL. Making a point: shared mechanics underlying the diversity of biological puncture. J Exp Biol. 2018 Nov 16;221(Pt 22):jeb187294. ].

Pain induction is one of the most common strategies applied by living organisms to deter a predator/attacker. Pain could be useful for defensive purposes but, when considering predation, fast pain induction could represent an evolutionary conflict. While on one hand pain induction could be a good strategy to deter predators from pursuing their attack [287287. Schmidt JO. Venom and the good life in tarantula hawks (Hymenoptera: Pompilidae): how to eat, not be eaten, and live long. J Kansas Entomol Soc. 2004 Oct;77(4):402-13. ,288288. Eisner T, Camazine S. Spider leg autotomy induced by prey venom injection: an adaptive response to “pain”? Proc Natl Acad Sci U S A. 1983 Jun;80(11):3382-5. ], on the other hand pain could enhance prey struggling and make establishing a firm grip on the prey more difficult [5151. Schmidt JO. Pain and lethality induced by insect stings: an exploratory and correlational study. Toxins (Basel). 2019 Jul 21;11(7):427. ,154154. Ward-Smith H, Arbuckle K, Naude A, Wüster W. Fangs for the memories? A survey of pain in snakebite patients does not support a strong role for defense in the evolution of snake venom composition. Toxins (Basel). 2020 Mar 22;12(3):201. ,288288. Eisner T, Camazine S. Spider leg autotomy induced by prey venom injection: an adaptive response to “pain”? Proc Natl Acad Sci U S A. 1983 Jun;80(11):3382-5. ]. A venom that is used both to incapacitate prey and deter predators should therefore induce pain in its main predators, and paralysis or death in prey. This requires specific toxins for each of these tasks to be present in the venom.

The pain response is mediated by receptors belonging to the nociception system. These sense and transmit environmental stimuli like changes in temperature, mechanical stress or chemicals concentration to the central nervous system, allowing the organism to take action to avoid further damage. The transient receptor potential (TRP) channels are transducers of the nociception system and associated with the pain-inducing response [289289. Yang F, Cui Y, Wang KW, Zheng J. Thermosensitive TRP channel pore turret is part of the temperature activation pathway. Proc Natl Acad Sci U S A. 2010 Apr 13;107(15):7083-8.

290. Cao E, Liao M, Cheng Y, Julius D. TRPV1 structures in distinct conformations reveal activation mechanisms. Nature. 2013 Dec 5;504(7478):113-8.
-291291. Basbaum AI, Bautista DM, Scherrer G, Julius D. Cellular and molecular mechanisms of pain. Cell. 2009 Oct 16;139(2):267-84. ]. It is not thus surprising that several pain-generating toxins isolated from scorpion venom have a high affinity for TRP channels [134134. Cid-Uribe JI, Veytia-Bucheli JI, Romero-Gutierrez T, Ortiz E, Possani LD. Scorpion venomics: a 2019 overview. Expert Rev Proteomics. 2020 Jan;17(1):67-83. ,292292. Yang S, Yang F, Zhang B, Lee BH, Li B, Luo L, Zheng J, Lai R. A bimodal activation mechanism underlies scorpion toxin-induced pain. Sci Adv. 2017 Aug 1;3:1-9.

293. Hakim MA, Jiang W, Luo L, Li B, Yang S, Song Y, Lai R. Scorpion toxin, BmP01, induces pain by targeting TRPV1 channel. Toxins (Basel). 2015 Sep 14;7(9):3671-87.
-294294. Lin King JV, Emrick JJ, Kelly MJS, Herzig V, King GF, Medzihradszky KF, Julius D. A cell-penetrating scorpion toxin enables mode-specific modulation of TRPA1 and pain. Cell. 2019 Sep 5;178(6):1362-74e.16. ]. Some specialized scorpion predators like grasshopper mice and bats [295295. Rowe AH, Rowe MP. Risk assessment by grasshopper mice (Onychomys spp.) feeding on neurotoxic prey (Centruroides spp.). Anim Behav. 2006 Mar;71(3):725-34.

296. Holderied M, Korine C, Moritz T. Hemprich’s long-eared bat (Otonycteris hemprichii) as a predator of scorpions: whispering echolocation, passive gleaning and prey selection. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2011 May;197(5):425-33.

297. Hopp BH, Arvidson RS, Adams ME, Razak KA. Arizona bark scorpion venom resistance in the pallid bat, Antrozous pallidus. PLoS One. 2017 Aug 30;12(8):1-13.
-298298. Rowe AH, Rowe MP. Physiological resistance of grasshopper mice (Onychomys spp.) to Arizona bark scorpion (Centruroides exilicauda) venom. Toxicon. 2008 Oct;52(5):597-605. ] possess an altered molecular configuration of other voltage-gated channels belonging to the nociception system which provide some immunity to the lethal and algogenic effects of scorpion venom [297297. Hopp BH, Arvidson RS, Adams ME, Razak KA. Arizona bark scorpion venom resistance in the pallid bat, Antrozous pallidus. PLoS One. 2017 Aug 30;12(8):1-13. ,299299. Rowe AH, Xiao Y, Rowe MP, Cummins TR, Zakon HH. Voltage-gated sodium channel in grasshopper mice defends against bark scorpion toxin. Science. 2013 Oct 25;342(6157):441-6. ,300300. Niermann CN, Tate TG, Suto AL, Barajas R, White HA, Guswiler OD, Secor SM, Rowe AH, Rowe PR. Defensive venoms: is pain suffcient for predator deterrence? Toxins (Basel). 2020 Apr 17;12(4):260. ]. The pain-inducing effects of scorpion venom are generally evaluated through injection of aliquots of crude venom into the plantar region of mice hind legs [301301. Chen B, Wang C, Ji Y. Scorpion BmK venom induces nociceptive response of rats by plantar injection. Neurotoxicol Teratol. 2001 Nov-Dec;23(6):675-9. ]. In these tests, pain effects are evaluated by the time the mice spend licking their paws. By using this assay it has been possible to show that buthid scorpion venoms are more painful than venoms of non-buthid scorpions [302302. Rowe AH, Xiao Y, Scales J, Linse KD, Rowe MP, Cummins TR, Zakon HH. Isolation and characterization of CvIV4: a pain inducing α- scorpion toxin. PLoS One. 2011;6(8):e23520. ], and that, in Centruroides vittatus (Buthidae), males are more painful than females [271271. Miller DW, Jones AD, Goldston JS, Rowe MP, Rowe AH. Sex differences in defensive behavior and venom of the striped bark scorpion Centruroides vittatus (Scorpiones: Buthidae). Integr Comp Biol. 2016 Nov;56(5):1022-31. ]. Moreover, even if predators generally prefer to feed on scorpions that inflict less painful stings, significant consumption of more painful species has been reported [300300. Niermann CN, Tate TG, Suto AL, Barajas R, White HA, Guswiler OD, Secor SM, Rowe AH, Rowe PR. Defensive venoms: is pain suffcient for predator deterrence? Toxins (Basel). 2020 Apr 17;12(4):260. ]. When under a strong predatory pressure, however, scorpions can rely on the rapid phenotypic plasticity of their venom to develop an effective defense. When a scorpion is continuously exposed to the presence of a mammalian predator, the production of anti-mammalian toxins in its venom increases [303303. Gangur AN, Smout M, Liddell MJ, Seymour JE, Wilson D, Northfield TD. Changes in predator exposure, but not in diet, induce phenotypic plasticity in scorpion venom. Proc R Soc B Biol Sci. 2017 Sep 27;284(1863):20171364. ].

Some species of the genus Parabuthus (Buthidae) apply their venom externally, as a toxungen rather than a venom [5050. Nelsen DR, Nisani Z, Cooper AM, Fox GA, Gren ECK, Corbit AG, et al. Poisons, toxungens, and venoms: redefining and classifying toxic biological secretions and the organisms that employ them. Biol Rev Camb Philos Soc. 2014 May;89(2):450-65. ]. These species are able to spray their venom toward their attacker, similar to the “spitting” behavior of some cobra species [4545. Nisani Z, Hayes WK. Venom-spraying behavior of the scorpion Parabuthus transvaalicus (arachnida: Buthidae). Behav Processes. 2015 Jun;115:46-52. ,4646. Newlands G. Scorpion defensive behavior. African Wildl. 1969;23:147-53. ,272272. Nisani Z, Hayes WK. Defensive stinging by Parabuthus transvaalicus scorpions: risk assessment and venom metering. Anim Behav. 2011 Mar;81(3):627-33. ,304304. Newlands G. The venom-squirting ability of Parabuthus scorpions (Arachnida: Buthidae). S Afr J Med Sci. 1974;39(4):175-8. ]. The first symptom following contact of the venom with the human eye is immediate pain [304304. Newlands G. The venom-squirting ability of Parabuthus scorpions (Arachnida: Buthidae). S Afr J Med Sci. 1974;39(4):175-8. ]. These “venom-spraying” events are unambiguously voluntary, and their use depends on the level of threat perceived by the scorpion. Nisani and Hayes [4545. Nisani Z, Hayes WK. Venom-spraying behavior of the scorpion Parabuthus transvaalicus (arachnida: Buthidae). Behav Processes. 2015 Jun;115:46-52. ] showed that spraying events occurred only if the scorpions were grabbed with tweezers and not when the defensive response was elicited by simply blowing puffs of air on the animals. Moreover, Parabuthus species have never been reported to spray venom on their prey during feeding trials [209209. Rein JO. Prey capture behavior in the East African scorpions Parabuthus leiosoma (Ehrenberg, 1828) and P. pallidus Pocock, 1895 (Scorpiones: Buthidae). Euscorpius. 2003;1895(6):1-8. ,213213. Rein JO. Sting use in two species of Parabuthus scorpions ( Buthidae ). J Arachnol. 1993;21(1):60-3. ]. Spitting cobras [4040. Westhoff G, Tzschätzsch K, Bleckmann H. The spitting behavior of two species of spitting cobras. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2005 Oct;191(10):873-81. ,4141. Westhoff G, Boetig M, Bleckmann H, Young BA. Target tracking during venom “spitting” by cobras. J Exp Biol. 2010 Jun 1;213(11):1797-802. ,154154. Ward-Smith H, Arbuckle K, Naude A, Wüster W. Fangs for the memories? A survey of pain in snakebite patients does not support a strong role for defense in the evolution of snake venom composition. Toxins (Basel). 2020 Mar 22;12(3):201. ], vinegarroons [4444. Eisner T, Meinwald J, Monro A, Ghent R. Defence mechanisms of arthropods-I. The composition and function of the spray of the whipscorpion, Mastigoproctus giganteus (Lucas) (Arachnida, Pedipalpida). J Insect Physiol. 1961 Aug;6(4):272-98. ,305305. Schmidt JO, Dani FR, Jones GR, Morgan ED. Chemistry, ontogeny, and role of pygidial gland secretions of the vinegaroon Mastigoproctus giganteus (Arachnida: Uropygi). J Insect Physiol. 2000 Apr;46(4):443-50. ], and other animals like bombardier beetles [4242. Eisner T. The protective role of the spray mechanism of the bombardier beetle, Brachynus ballistarius Lec. J Insect Physiol. 1958 Aug;2(3):215-6. ] and earwigs [306306. Eisner T. Defense mechanism of arthropods. II. The chemical and mechanical weapons of an earwig. Psyche. 1960;67:62-70. ] likewise spray toxins to deter attackers/predators, but do not use them to incapacitate their prey.

Another very peculiar defensive use of the metasoma and telson has been observed in some species of the genus Ananteris (Buthidae). When grabbed with tweezers, members of this genus are able to cast off their metasoma which also contains their hindgut [307307. Lira AFA, Sarinho NMS, De Souza AM, Albuquerque CMR. Metasomal autotomy in Ananteris mauryi Lourenço, 1982 (Scorpiones: Buthidae). J Insect Behav. 2014;27:279-82. ,308308. Mattoni CI, García-Hernández S, Botero-Trujillo R, Ochoa JA, Ojanguren-Affilastro AA, Pinto-da-Rocha R, Prendini L. Scorpion sheds “tail” to escape: consequences and implications of autotomy in scorpions (Buthidae: Ananteris). PLoS One. 2015 Jan 28;10(1):1-15. ]. Similarly to autotomized lizard tails, autotomized metasomas continue to move for a few seconds. Differently from lizard tails, no regeneration has been ever observed. Metasoma autotomy decreases predatory success [309309. García-Hernandez S, Machado G. ‘ Tail ’ autotomy and consequent stinger loss decrease predation success in scorpions. Anim Behav. 2020 Sep. ] but it has been observed that acaudate males survived for several months and mated, thus clearly increasing fitness [308308. Mattoni CI, García-Hernández S, Botero-Trujillo R, Ochoa JA, Ojanguren-Affilastro AA, Pinto-da-Rocha R, Prendini L. Scorpion sheds “tail” to escape: consequences and implications of autotomy in scorpions (Buthidae: Ananteris). PLoS One. 2015 Jan 28;10(1):1-15. ].

Mating behavior and sexual dimorphism

While weapons are used for the same purpose by the two sexes in predatory and defensive behavior (be it sometimes to different degrees [277277. Carlson BE, McGinley S, Rowe MP. Meek males and fighting females: sexually-dimorphic antipredator behavior and locomotor performance is explained by morphology in bark scorpions (Centruroides vittatus). PLoS One. 2014 May 28;9(5):e97648. ]), in intraspecific competition and mating behavior, members of each sex may use their weapons to accomplish different tasks.

Male-male antagonism

Adult scorpions change their behavior during the mating season. Males become more vagrant and actively look for a partner [310310. Polis GA, Farley RD. Behavior and ecology of mating in the scorpion, Paruroctonus mesaensis Stahnke (Scorpionida : Vaejovidae). J Arachnol. 1979;7(1):33-46.

311. Benton TG. The ecology of the scorpion Euscorpius flavicaudis in England. J Zool. 1992 Mar;226(3):351-68.
-312312. Tourtlotte G. Studies on the biology and ecology of the northern scorpion, Paruroctonus boreus. Gt Basin Nat. 1974 Sep 30;34(3):167-79. ], which also leads to a higher chance of intrasexual encounters. Literature accurately reporting intrasexual contests between male scorpions is practically non-existent, with the only formal description of one of these events reported for the species Hadrurus arizonensis (Caraboctonidae) [7878. Tallarovic SSK. Reproductive and aggressive behaviors in the giant hairy desert scorpion [dissertation]. Corvallis, Oregon. Oregon State University; 2000. ]. In this species, intraspecific contests are divided into three phases: (i) alert phase, (ii) contact phase, and (iii) contest phase. In the alert phase, the opponents face each other with both pedipalps and metasoma raised up. Differently than when performing defensive alert postures, during the intraspecific alert phase both opponents show unique behaviors like metasoma wagging (personal observation YS in Tityus pachyurus, Buthidae) and a fast shaking of the whole body without leg movements called “juddering”. These behavioral units have been extensively characterized in the literature on scorpion mating behavior [195195. Brownell PH, Van Leo Hemmen J. Vibration sensitivity and a computational theory for prey-localizing behavior in sand scorpions. Am Zool. 2001;41(5):1229-40. ,215215. Rosin R, Shulow A. Studies on the scorpion Nebo hierochonticus. Proc Zool Soc London. 1963;140:547-75. ,313313. Briceño RD, Bonilla F. Substrate vibrations in the scorpion Centruroides margaritatus (Scorpiones: Buthidae) during courtship. Rev Biol Trop. 2009 Nov;57(Suppl 1):267-74. ,314314. Alexander AJ. The courtship and mating of the scorpion, Opisthophthalmus latimanus. Proc Zool Soc London. 1957 Jul;128(4):529-44. ] but, due the lack of studies in this topic, are never reported in male-male competition. During the contact phase, scorpions grab each other with their pedipalps. In the contest phase, they try to grab the metasoma of their opponent or, alternatively, try to flip it on one side [7878. Tallarovic SSK. Reproductive and aggressive behaviors in the giant hairy desert scorpion [dissertation]. Corvallis, Oregon. Oregon State University; 2000. ]. During these contests, no actual stings have ever been reported, and the whole behavior seems to be ritualized. The contest ends when one of the competitors holds its position while the other one retreats [7878. Tallarovic SSK. Reproductive and aggressive behaviors in the giant hairy desert scorpion [dissertation]. Corvallis, Oregon. Oregon State University; 2000. ,315315. Benton TG. Determinants of male mating success in a scorpion. Anim Behav. 1992;43:125-35. ].

Courtship and mating

When a mature male encounters a female, courtship generally happens. Courtship and mating behavior has been extensively studied in several families of scorpions, and a few taxon-specific differences in the various phases of the courtship ritual have been reported (e.g. the presence/absence of cheliceral massage and sexual sting) [128128. Polis GA. The biology of scorpions. Polis GA, editor. Stanford: University Stanford; 1990. ,314314. Alexander AJ. The courtship and mating of the scorpion, Opisthophthalmus latimanus. Proc Zool Soc London. 1957 Jul;128(4):529-44. ,316316. Alexander AJ. Courtship and mating in the Buthid scorpions. Proc Zool Soc London. 1959 Oct;133:145-69. ,317317. Brownell P, Polis G. Scorpion Biology and Research. Brownell P, Polis G, editors. New York: Oxford University Press; 2001. ]. Courtship generally starts with the male approaching the female. The juddering behavior has been observed in different scorpion families in this phase of the mating ritual, and is associated with the production of vibrations that communicate the position of the male to the female, or that help the male control the female’s aggressiveness [195195. Brownell PH, Van Leo Hemmen J. Vibration sensitivity and a computational theory for prey-localizing behavior in sand scorpions. Am Zool. 2001;41(5):1229-40. ,215215. Rosin R, Shulow A. Studies on the scorpion Nebo hierochonticus. Proc Zool Soc London. 1963;140:547-75. ,313313. Briceño RD, Bonilla F. Substrate vibrations in the scorpion Centruroides margaritatus (Scorpiones: Buthidae) during courtship. Rev Biol Trop. 2009 Nov;57(Suppl 1):267-74. ,314314. Alexander AJ. The courtship and mating of the scorpion, Opisthophthalmus latimanus. Proc Zool Soc London. 1957 Jul;128(4):529-44. ]. The male then attempts to grasp the female’s pedipalps. The initiating phase is very dynamic, and involves males using both their weapons to manipulate the female. The chelae are used to establish a firm grip on the female’s pedipalps to control her movements, which is essential for the next phases of the mating. At the same time, in several species the male rubs, clubs, and even stings the female. After this first contact, the male starts to guide the female by performing specific movements in a dance-like ritual called promenade à deux. During this phase, the male moves forward and backwards, dragging the female until he finds a suitable place to deposit the spermatophore. The spermatophore is a stalk-like structure extruded from the male’s genital opening, that serves as a pedestal for the sperm. Once the spermatophore has been deposited, the male guides the female on it, and as soon as the female takes up the sperm package from the spermatophore (leaving only the pedicel anchored to the substrate), the pair separates, ending the mating. This is just a brief illustrative summary of the main phases of scorpion courtship. For more inclusive literature please refer to [159159. Tallarovic SK, Melville JM, Brownell PH. Courtship and mating in the giant hairy desert scorpion, Hadrurus arizonensis (Scorpionida, Iuridae). J Insect Behav. 2000;13:827-38. ,160160. Francke OF. The reproductive biology and life history of Megacormus gertschi Diaz (Scorpiones: Chactidae; Megacorminae). J Arachnol. 1979;7:223-30. ,310310. Polis GA, Farley RD. Behavior and ecology of mating in the scorpion, Paruroctonus mesaensis Stahnke (Scorpionida : Vaejovidae). J Arachnol. 1979;7(1):33-46. ,311311. Benton TG. The ecology of the scorpion Euscorpius flavicaudis in England. J Zool. 1992 Mar;226(3):351-68. ,314314. Alexander AJ. The courtship and mating of the scorpion, Opisthophthalmus latimanus. Proc Zool Soc London. 1957 Jul;128(4):529-44. ,316316. Alexander AJ. Courtship and mating in the Buthid scorpions. Proc Zool Soc London. 1959 Oct;133:145-69. ].

The degree of sexual dimorphism in scorpions is highly variable. Simplifying the classes created by Koch [318318. Koch LE. The taxonomy, geographic distribution and evolutionary radiation of Australo-Papauan Scorpions. Rec West Aust Museum. 1977 Jan;5:83-367. ] on Australo-Papuan scorpions, and later by Polis [128128. Polis GA. The biology of scorpions. Polis GA, editor. Stanford: University Stanford; 1990. ], it is possible to identify two main patterns of sexual dimorphism in scorpions:

  • Differences in body size but not in shape of secondary sexual characters.

  • Differences in shape and size of secondary sexual characters.

Sexual size dimorphism in scorpions has been reviewed by McLean et al. [1414. McLean CJ, Garwood RJ, Brassey CA. Sexual dimorphism in the Arachnid orders. PeerJ. 2018 Nov 6;6:e5751. ], with females being generally larger than males probably due to selection on fecundity and to the direct contribution of developing embryos to body size [277277. Carlson BE, McGinley S, Rowe MP. Meek males and fighting females: sexually-dimorphic antipredator behavior and locomotor performance is explained by morphology in bark scorpions (Centruroides vittatus). PLoS One. 2014 May 28;9(5):e97648. ]. However, few exceptions of male-biased size dimorphism are present, like in the cases of Liocheles australasiae (Scorpiondae) [318318. Koch LE. The taxonomy, geographic distribution and evolutionary radiation of Australo-Papauan Scorpions. Rec West Aust Museum. 1977 Jan;5:83-367. ] and Tityus trinitatis (Buthidae) [316316. Alexander AJ. Courtship and mating in the Buthid scorpions. Proc Zool Soc London. 1959 Oct;133:145-69. ,319319. Kjellesvig-Waering EN. The scorpions of Trinidad and Tobago. Caribb J Sci. 1966;6:123-35. ]. In the scope of this review, the differences in shape and size of secondary sexual characters deserve particular focus.

The greatest differences in shape and size of sexually selected characters in scorpions mainly lie in their weapons. Sexual dimorphic species of scorpions generally present differences in chela shape and/or size between the two sexes. In these species, one of the sexes tends to have more robust chelae, while the other sex generally presents a slenderer chela morphology.

In the members of the families with males having the more robust chelae (e.g., some Buthidae, Scorpionidae), a potential advantage for males may be more space for muscles, and therefore a larger pinch force. This, together with a different distribution and shape of the denticles on the fingers, would provide a firmer grip on the female’s pedipalps during the courtship, or aid to defeat weaker male competitors. A more bulbous chela may also provide less opportunity for male competitors or unwilling females to find purchase.

In some species the males have more elongated and slender chelae than females [320320. Kraepelin K. Die sekundären Geschlechtscharaktere der Skorpione, Pedipalpen und Solifugen. Mitteilungen aus dem Naturhistorischen. Museum Hambg. 1907;25:181-225. ]. This pattern is most extreme in some members of the families Chactidae [321321. González-Gómez JC, Valenzuela-Rojas JC, García LF, Franco Pérez LM, Guevara G, Buitrago S, Cubillos A, Van Der Meijden A. Sexual dimorphism in the biomechanical and toxicological performance in prey incapacitation of two morphologically distinct scorpion species (Chactas sp. and Centruroides sp.). Biol J Linn Soc. 2020;129(1):190-8. ], Scorpionidae [322322. Leeming J. Scorpions of Southern Africa. Hromnik J, editor. Cape Town: Penguin Random House South Africa; 2019. ] and Buthidae [323323. Lourenço WR, Otero Patiño R. Tityus antioquensis sp. n., a new species of scorpion from the Department Antioquia, Central Cordillera of Colombia (Scorpiones, Buthidae), with a checklist and key for the Colombian species of the genus. Entomol Mitteilungen aus dem Zool Museum Hambg. 1998;12:297-307. ,324324. Sánchez-Quirós C, Arévalo E, Barrantes G. Static allometry and sexual size dimorphism in Centruroides margaritatus (Scorpiones: Buthidae). J Arachnol. 2012 Nov 1;40(3):338-44. ]. In sexual dimorphic buthid species, the elongation of both pedipalps and metasoma occurs in the last or second-to-last moult [325325. Farzanpay R, Vachon M. Contribution a l’etude des caracteres sexuels secondaries chez les scorpions Buthidae. Arch Razi Inst. 1988;38(1):47-53. ]. Slenderer chelae are associated with lower bite force in males [321321. González-Gómez JC, Valenzuela-Rojas JC, García LF, Franco Pérez LM, Guevara G, Buitrago S, Cubillos A, Van Der Meijden A. Sexual dimorphism in the biomechanical and toxicological performance in prey incapacitation of two morphologically distinct scorpion species (Chactas sp. and Centruroides sp.). Biol J Linn Soc. 2020;129(1):190-8. ], suggesting that in these cases, selection for higher biteforce is not the main driver determining chela morphology. Studies of the mating ritual of Centruroides margaritatus (Buthidae) and Chactas reticulatus (Chactidae) [324324. Sánchez-Quirós C, Arévalo E, Barrantes G. Static allometry and sexual size dimorphism in Centruroides margaritatus (Scorpiones: Buthidae). J Arachnol. 2012 Nov 1;40(3):338-44. ,326326. Lourenço WR, Andrzejewski V, Cloudsley-Thompson JL. The life history of Chactas reticulatus Kraepelin, 1912 (Scorpiones, Chactidae), with a comparative analysis of the reproductive traits of three scorpion lineages in relation to habitat. Zool Anz. 2003;242(1):63-74. ] show that males of these species use their elongated chelae similarly to other scorpions. To date no functional study has shown which of the potential functions and advantages is the driver for sexual dimorphism of chela size in a particular species. Having such elongated appendages may permit to the two sexes of the same species to feed on different prey and exploit a different foraging niche, lowering inter-sexual competition [321321. González-Gómez JC, Valenzuela-Rojas JC, García LF, Franco Pérez LM, Guevara G, Buitrago S, Cubillos A, Van Der Meijden A. Sexual dimorphism in the biomechanical and toxicological performance in prey incapacitation of two morphologically distinct scorpion species (Chactas sp. and Centruroides sp.). Biol J Linn Soc. 2020;129(1):190-8. ], although this cannot be the primary driver of sexual dimorphism.

In some species of Scorpionidae, Hemiscorpidae and Buthidae, males have a prominent tooth on the dorsal side of the movable finger, which is thought to enhance grip on the female’s pedipalps. Once the female has been grasped, her fingers are generally placed in the space between the manus and the tooth, with the latter blocking the retreating of female’s fingers, thus reducing the chances of them slipping out [327327. Booncham U, Sitthicharoenchai D. Sexual dimorphism in the Asian giant forest scorpion, Heterometrus laoticus Couzijn, 1981. NU Sci J. 2007;4(1):42-52. ]. In Bothriuridae, males present a spine-like apophysis close to a depression present on the surface of their manus. This depression has the function to create a cul de sac for the female’s fingers, distally closed by the apophysis [328328. Maury EA. Sobre el dimorfismo sexual de la pinza de los pedipalpos en los escorpiones Bothriuridae. Bull du Muséum Natl d’Histoire Nat Paris. 1975;215:765-71. ]. A similar depression in the manus, most likely serving the same function, is also present in adult males of Pandinoides cavimanus (Scorpionidae).

The venom delivering system is also a character that may be highly variable in sexually dimorphic species. The general trend is that males have a slenderer, more elongated metasoma, and a more swollen telson than females. Having a longer metasoma has not been related with performance improvements in either locomotion activity or frequency of stinging [277277. Carlson BE, McGinley S, Rowe MP. Meek males and fighting females: sexually-dimorphic antipredator behavior and locomotor performance is explained by morphology in bark scorpions (Centruroides vittatus). PLoS One. 2014 May 28;9(5):e97648. ]. However, a longer metasoma allows faster strikes [269269. Coelho P, Kaliontzopoulou A, Rasko M, van der Meijden A. A ‘striking’ relationship: scorpion defensive behaviour and its relation to morphology and performance. Funct Ecol. 2017 Apr 3;31(7):1390-1404. ] which can be useful in performing quick defensive responses, especially during the mating season, when the increased sexual vagrancy of males increases chances of predator encounters.

A longer metasoma in males may be advantageous during courtship. Males may sting or club the female while keeping her at a greater distance, thus reducing the chances of being stung by an aggressive partner. This behavior most likely has the function of reducing the aggressiveness of a reluctant female [128128. Polis GA. The biology of scorpions. Polis GA, editor. Stanford: University Stanford; 1990. ,159159. Tallarovic SK, Melville JM, Brownell PH. Courtship and mating in the giant hairy desert scorpion, Hadrurus arizonensis (Scorpionida, Iuridae). J Insect Behav. 2000;13:827-38. ,160160. Francke OF. The reproductive biology and life history of Megacormus gertschi Diaz (Scorpiones: Chactidae; Megacorminae). J Arachnol. 1979;7:223-30. ,311311. Benton TG. The ecology of the scorpion Euscorpius flavicaudis in England. J Zool. 1992 Mar;226(3):351-68. ,314314. Alexander AJ. The courtship and mating of the scorpion, Opisthophthalmus latimanus. Proc Zool Soc London. 1957 Jul;128(4):529-44. ,316316. Alexander AJ. Courtship and mating in the Buthid scorpions. Proc Zool Soc London. 1959 Oct;133:145-69. ,329329. Jiao G, Zhu M. Courtship and mating of Scorpiops luridus Zhu Lourenço & Qi, 2005 (Scorpiones: Euscorpiidae) from Xizang province, China. J Venom Anim Toxins incl Trop Dis. 2010;16(1):155-65. doi: 10.1590/S1678-91992010005000010.
https://doi.org/10.1590/S1678-9199201000...
]. Whether venom injection occurs during sexual stings is still not clear. However, Jiao and Zhu [329329. Jiao G, Zhu M. Courtship and mating of Scorpiops luridus Zhu Lourenço & Qi, 2005 (Scorpiones: Euscorpiidae) from Xizang province, China. J Venom Anim Toxins incl Trop Dis. 2010;16(1):155-65. doi: 10.1590/S1678-91992010005000010.
https://doi.org/10.1590/S1678-9199201000...
] hypothesized that males may deliver a “dry” or a “wet” sting according to the level of aggressiveness of the female. Moreover, differences in telson shape [320320. Kraepelin K. Die sekundären Geschlechtscharaktere der Skorpione, Pedipalpen und Solifugen. Mitteilungen aus dem Naturhistorischen. Museum Hambg. 1907;25:181-225. ,327327. Booncham U, Sitthicharoenchai D. Sexual dimorphism in the Asian giant forest scorpion, Heterometrus laoticus Couzijn, 1981. NU Sci J. 2007;4(1):42-52. ,330330. Sentenská L, Graber F, Richard M, Kropf C. Sexual dimorphism in venom gland morphology in a sexually stinging scorpion. Biol J Linn Soc. 2017 Oct;122(2):429-43. ] and venom between sexes have been found in several species of scorpions performing sexual stinging [331331. Yamaji N, Dai L, Sugase K, Andriantsiferana M, Nakajima T, Iwashita T. Solution structure of IsTX: a male scorpion toxin from Opisthacanthus madagascariensis (Ischnuridae). Eur J Biochem. 2004 Oct;271(19):3855-64.

332. Rodríguez-Ravelo R, Batista CVF, Coronas FIV, Zamudio FZ, Hernández-Orihuela L, Espinosa-López G, Ruiz-Urquiola A, Possani LD. Comparative proteomic analysis of male and female venoms from the Cuban scorpion Rhopalurus junceus. Toxicon. 2015 Dec 1;107(Pt B):327-34.

333. D’Suze G, Sandoval M, Sevcik C. Characterizing Tityus discrepans scorpion venom from a fractal perspective: venom complexity, effects of captivity, sexual dimorphism, differences among species. Toxicon. 2015 Dec 15;108:62-72.
-334334. De Sousa L, Borges A, Vásquez-Suárez A, Op den Camp HJ, Chadee-Burgos RI, Romero-Bellorín M, Espinoza J, De Sousa-Insana L, Pino-Garcia O. Differences in venom toxicity and antigenicity between females and males Tityus nororientalis (Buthidae) scorpions. J Venom Res. 2010;1:61-70. ], with male venoms possessing some unique venom components. In the species Scorpio maurus (Scorpionidae) however, females present a more complex venom profile than males [335335. Abdel-Rahman MA, Omran MAA, Abdel-Nabi IM, Ueda H, McVean A. Intraspecific variation in the Egyptian scorpion Scorpio maurus palmatus venom collected from different biotopes. Toxicon. 2009 Mar 1;53(3):349-59. ]. The role of sex-specific toxins in reproductive ecology has not been investigated yet.

Some authors have hypothesized that differences in the length of the metasoma may be useful in sex recognition in case of intraspecific encounters [316316. Alexander AJ. Courtship and mating in the Buthid scorpions. Proc Zool Soc London. 1959 Oct;133:145-69. ,336336. Ross LK. Notes and observations on courtship and mating in Tityus (Atreus) magnimanus Pocock, 1897 (Scorpiones: Buthidae). J Venom Anim Toxins incl Trop Dis. 2009;15(1):43-53. doi: 10.1590/S1678-91992009000100005.
https://doi.org/10.1590/S1678-9199200900...
]. However, metasoma grabbing in the early stages of mating has also been reported in species where the sexual dimorphism is not very marked [159159. Tallarovic SK, Melville JM, Brownell PH. Courtship and mating in the giant hairy desert scorpion, Hadrurus arizonensis (Scorpionida, Iuridae). J Insect Behav. 2000;13:827-38. ].

In Bothriuridae, males possess accessory glands located on the dorsal side of the telson, with the function of producing secretions when the male rubs the metasoma onto the female’s body [337337. Peretti A. Análisis de la etapa inicial del cortejo de Bothirurus bonariensis (Scorpiones, Bothriuridae) y su relación con el reconocimiento sexual. Rev Arachnol. 1995;11:35-45.

338. Peretti A. Relación de las glándulas caudales de machos de escorpiones (Scorpiones, Bothriuridae) con el comportamiento sexual. Rev Arachnol. 1997;12:31-41.

339. Olivero PA, González A, Mattoni CI, Peretti A V. Chemical caressess: geographical variation of male sexual signals in a Neotropical scorpion. Behaviour. 2015;152:1745-63.
-340340. de la Serna de Esteban CJ. Las glándulas tegumentarias del metasoma en algunas especies argentinas de la familia Bothriuridae (Scorpiones). Physis. 1978;94:121-32. ]. According to Peretti [338338. Peretti A. Relación de las glándulas caudales de machos de escorpiones (Scorpiones, Bothriuridae) con el comportamiento sexual. Rev Arachnol. 1997;12:31-41. ], these secretions have the function of increasing female’s receptivity. In Bothriurus bonariensis (Bothriuridae), the composition of these secretions has been found to change depending on the population analysed [339339. Olivero PA, González A, Mattoni CI, Peretti A V. Chemical caressess: geographical variation of male sexual signals in a Neotropical scorpion. Behaviour. 2015;152:1745-63. ]. Another example of sexually dimorphism in telson shape is given by the genus Anuroctonus (Chactidae). Males of this genus have a secondary bulb of unknown function at the base of the aculeus, which is absent in females [128128. Polis GA. The biology of scorpions. Polis GA, editor. Stanford: University Stanford; 1990. ,341341. Soleglad M, Fet V. The systematics of the scorpion subfamily Uroctoninae (Scorpiones: Chactidae). Rev ibérica Aracnol. 2004 Jan:81-128. ].

Conclusion

Scorpions use their chelae and venom delivery system in the most fundamental aspects of their ecology. The two weapon systems of scorpions perform in different contexts of usage (predation, self-defense and intrasexual competition), and in some cases interact. How these interactions evolve in different species, or whether there is a trade-off between the weapon systems, is not yet resolved. Despite recent progress in functional studies, several topics still remain underexplored. Of course, a disproportionate fraction of the literature is devoted to venom research. The importance thereof is unambiguous for advances in human health as potential new medicine, as well as in the treatment of scorpion stings as a neglected health risk. Currently basic information on pedipalp anatomy, diet, functional studies of weapons, and intrasexual interactions are sparse or even absent. With the current increased interest in the functional aspects of scorpion weapons, we hope that also these areas will soon reveal new insights in the fascinating ecology of the scorpion weapon constellation.

Acknowledgements

The authors wish to thank Luis Fernardo García Hernández for the invitation to contribute to the special issue “Arthropods: venoms and biology”. The authors wish to thank Thomas Kleinteich and Renaud Boistel for their help by scanning several scorpion specimens to produce some of the images in this review. Authors are also extremely grateful to Ignazio Avella for his constructive criticism in the early phases of the manuscript writing, Michiel Cozijn for sharing his knowledge about mating behaviour in neotropical scorpions, and Jan Ove Rein for helpfully providing some rare articles from his literature collection.

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  • Availability of data and materials

    Not applicable.
  • Funding

    YS was funded by a PhD scholarship by Fundação para Ciência e Tecnologia (SFRH/BD/136934/2018). AvdM was supported by a grant by Fundação para a Ciência e a Tecnologia under the Programa Operacional Potencial Humano - Quadro de Referência Estratégico Nacional funds from the European Social Fund and Portuguese Ministério da Educação e Ciência (SFRH/BPD/101057/2014).
  • Ethics approval

    Not applicable.
  • Consent for publication

    Not applicable.

Publication Dates

  • Publication in this collection
    03 Sept 2021
  • Date of issue
    2021

History

  • Received
    06 Jan 2021
  • Accepted
    18 Mar 2021
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