Advertisement

The Science of Nature

, 103:56 | Cite as

Similar burrow architecture of three arid-zone scorpion species implies similar ecological function

  • Amanda M. Adams
  • Eugene Marais
  • J. Scott Turner
  • Lorenzo Prendini
  • Berry Pinshow
Original Paper
First Online:

Abstract

Many animals reside in burrows that may serve as refuges from predators and adverse environmental conditions. Burrow design varies widely among and within taxa, and these structures are adaptive, fulfilling physiological (and other) functions. We examined the burrow architecture of three scorpion species of the family Scorpionidae: Scorpio palmatus from the Negev desert, Israel; Opistophthalmus setifrons, from the Central Highlands, Namibia; and Opistophthalmus wahlbergii from the Kalahari desert, Namibia. We hypothesized that burrow structure maintains temperature and soil moisture conditions optimal for the behavior and physiology of the scorpion. Casts of burrows, poured in situ with molten aluminum, were scanned in 3D to quantify burrow structure. Three architectural features were common to the burrows of all species: (1) a horizontal platform near the ground surface, long enough to accommodate the scorpion, located just below the entrance, 2–5 cm under the surface, which may provide a safe place where the scorpion can monitor the presence of potential prey, predators, and mates and where the scorpion warms up before foraging; (2) at least two bends that might deter incursion by predators and may reduce convective ventilation, thereby maintaining relatively high humidity and low temperature; and (3) an enlarged terminal chamber to a depth at which temperatures are almost constant (±2–4 °C). These common features among the burrows of three different species suggest that they are important for regulating the physical environment of their inhabitants and that burrows are part of scorpions’ “extended physiology” (sensu Turner, Physiol Biochem Zool 74:798–822, 2000).

Keywords

Burrows Extended organism Three-dimensional modeling Scorpionidae Temperature gradients 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We thank Stuart Summerfield for the invaluable technical assistance; David Andreen, Golan Bel, and Mike Kirby for their help with calculating burrow tortuosity; Gina and Jacobus Olivier for their incredibly generous hospitality and assistance in the field at Bloukop; Eran Gefen and Yael Lubin for their advice; and three anonymous reviewers for the comments on a previous draft of the manuscript. This research was supported by grant 136/10 from the Israel Science Foundation to BP and Pedro Berliner, Human Frontier Science Program grant RGP0066/2012-TURNER to JST and EM, and by a post-doctoral fellowship from the Jacob Blaustein Center for Scientific Cooperation and a Company of Biologists Travel Grant from the Society of Experimental Biology to AMA. This is paper number 908 of the Mitrani Department of Desert Ecology.

Authors’ contributions

AMA, EM, JST, and BP conceived, designed, and performed the experiments. AMA analyzed the data. LP identified the scorpions. AMA and BP wrote the manuscript and JST and LP edited the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

114_2016_1374_MOESM1_ESM.zip (69.6 mb)
ESM 1 Three-dimensional scans of aluminum casts of burrows of three species of scorpion: Scorpio palmatus in the Negev Desert highlands, Israel (n = 30), Opistophthalmus wahlbergii in the Kalahari Desert, Namibia (n = 19), and Opistophthalmus setifrons in the Central Highlands, Namibia (n = 4). Stereolithography images (.STL) can be viewed using Geomagic Verify Viewer, which is freely available at URL:http://www.geomagic.com/ (ZIP 69.5 mb)

References

  1. Abdel-Nabi I, McVean A, Abdel-Rahman M, Omran M (2004) Intraspecific diversity of morphological characters of the burrowing scorpion Scorpio maurus palmatus (Ehrenberg, 1828) in Egypt (Arachnida: Scorpionida). Serket 9:41–67Google Scholar
  2. Avenant NL, Nel JAJ (1997) Prey use by four syntopic carnivores in a strandveld ecosystem. South African J Wildl Res 27:86–93Google Scholar
  3. Begg CM, Begg KS, Du Toit JT, Mills MGL (2003) Sexual and seasonal variation in the diet and foraging behaviour of a sexually dimorphic carnivore, the honey badger (Mellivora capensis). J Zool London 260:301–316. doi: 10.1017/S0952836903003789 CrossRefGoogle Scholar
  4. Brownell P, Farley RD (1979) Prey-localizing behaviour of the nocturnal desert scorpion, Paruroctonus mesaensis: orientation to substrate vibrations. Anim Behav 27:185–193. doi: 10.1016/0003-3472(79)90138-6 CrossRefGoogle Scholar
  5. Brownell P, van Hemmen JL (2001) Vibration sensitivity and a computational theory for prey-localizing behavior in sand scorpions. Am Zool 41:1229–1240Google Scholar
  6. Bullitt E, Gerig G, Pizer SM et al (2003) Measuring tortuosity of the intracerebral vasculature from MRA images. IEEE Trans Med Imaging 22:1163–1171. doi: 10.1109/TMI.2003.816964 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Çolak M, Karataş A (2013) Shape of burrows built by Scorpio maurus L., 1758 (Scorpiones: Scorpionidae) from Turkey, with description of capture methods. Euscorpius 171:1–7Google Scholar
  8. Crawford C, Riddle W (1975) Overwintering physiology of the scorpion Diplocentrus spitzeri. Physiol Zool 48:84–92CrossRefGoogle Scholar
  9. Dawkins R (1984) The extended phenotype: the gene as the unit of selection. Oxford University Press, Oxford, doi:  10.1016/0162-3095(84)90028-1
  10. De Vries JL, Pirk CWW, Bateman PW et al (2011) Extension of the diet of an extreme foraging specialist, the aardwolf (Proteles cristata). African Zool 46:194–196. doi: 10.3377/004.046.0113 CrossRefGoogle Scholar
  11. Doody JS, James H, Colyvas K et al (2015) Deep nesting in a lizard, deja vu devil’s corkscrews: first helical reptile burrow and deepest vertebrate nest. Biol J Linn Soc 116:13–26. doi: 10.1111/bij.12589 CrossRefGoogle Scholar
  12. Eastwood EB (1978) Notes on the scorpion fauna of the Cape. Part 4. The burrowing activities of some scorpionids and buthids (Arachnida, Scorpionida). Ann South African Museum 75:249–255Google Scholar
  13. Eitel B, Eberle J, Kuhn R (2002) Holocene environmental change in the Otjiwarongo thornbush savanna (Northern Namibia): evidence from soils and sediments. Catena 47:43–62Google Scholar
  14. Gefen E, Ar A (2004) Comparative water relations of four species of scorpions in Israel: evidence for phylogenetic differences. J Exp Biol 207:1017–1025. doi: 10.1242/jeb.00860 CrossRefPubMedGoogle Scholar
  15. Hadley NF (1970a) Water relations of the desert scorpion, Hadrurus arizonensis. J Exp Biol 53:547–58PubMedGoogle Scholar
  16. Hadley NF (1970b) Micrometeorology and energy exchange in two desert arthropods. Ecology 51:434–444CrossRefGoogle Scholar
  17. Hadley NF (1990) Environmental physiology. In: Polis GA (ed) The biology of scorpions. Stanford University Press, Stanford, pp 321–340Google Scholar
  18. Hansell M (1984) Animal architecture and building behavior. Longman, LondonGoogle Scholar
  19. Hansell M (2007) Built by animals: the natural history of animal architecture. Oxford University Press, Oxford, doi:  10.1086/592657
  20. Harington A (1978) Burrowing biology of the scorpion Cheloctonus jonesii Pocock (Arachnida: Scorpionida: Scorpionidae). J Arachnol 5:243–249Google Scholar
  21. Hart WE, Goldbaum M, Côté B et al (1999) Measurement and classification of retinal vascular tortuosity. Int J Med Inform 53:239–252. doi: 10.1016/S1386-5056(98)00163-4 CrossRefPubMedGoogle Scholar
  22. Hembree DI, Johnson LM, Tenwalde RW (2012) Neoichnology of the desert scorpion Hadrurus arizonensis: burrows to biogenic cross lamination. Palaeontol Electron 15:1–34Google Scholar
  23. King D, Green B (1979) Notes on diet and reproduction of the sand goanna, Varanus gouldii rosenbergi. Copeia 1979:64–70CrossRefGoogle Scholar
  24. Kinlaw A (1999) A review of burrowing by semi-fossorial vertebrates in arid environments. J Arid Environ 41:127–145CrossRefGoogle Scholar
  25. Kinlaw A, Grasmueck M (2012) Evidence for and geomorphologic consequences of a reptilian ecosystem engineer: the burrowing cascade initiated by the gopher tortoise. Geomorphology 157–158:108–121. doi: 10.1016/j.geomorph.2011.06.030 CrossRefGoogle Scholar
  26. Koch LE (1970) Predation of the scorpion, Urodacus hoplurus, by the lizard Varanus gouldi. West Aust Nat 11:120–121Google Scholar
  27. Koch L (1978) A comparative study of the structure, function and adaptation to different habitats of burrows in the scorpion genus Urodacus (Scorpionida, Scorpionidae). Rec West Aust Museum 6:119–146Google Scholar
  28. Koch LE (1981) The scorpions of Australia: aspects of their ecology and zoogeography. In: Keast A (ed) Ecol. Biogeogr. Aust. Vol. 2. W. Junk, The Hague, pp 873–884Google Scholar
  29. Kotzman M, Lubin YD, Goldberg M (1989) Activities of a burrow-dwelling scorpion revealed at the surface. Acta Zool Fenn 190:205–208Google Scholar
  30. Krapf D (1986) Contact chemoreception of prey in hunting scorpions (Arachnida: Scorpiones). Zool Anz 217:119–129Google Scholar
  31. Krapf D (1988) Prey localization by trichobothria of scorpions. Proc. Eur. Arachnol. Colloquium, Berlin, pp 29–34Google Scholar
  32. Lamoral BH (1978) Soil hardness, an important and limiting factor in burrowing scorpions of the genus Opisthophthalmus C.L. Koch, 1837 (Scorpionidae, Scorpinida). Symp Zool Soc London 42:171–181Google Scholar
  33. Lamoral B (1979) The scorpions of Namibia (Arachnida-Scorpionida). Annu Natal Museum 23:497–784Google Scholar
  34. Levy G, Amitai P (1980) Fauna Palaestina. Arachnida I: Scorpiones. The Israeli Academy of Sciences and Humanities, JerusalemGoogle Scholar
  35. Martin LD, Bennett DK (1977) The burrows of the Miocene beaver Palaeocastor, Western Nebraska, U.S.A. Palaeogeogr Palaeoclimatol Palaeoecol 22:173–193Google Scholar
  36. McCormick SJ, Polis GA (1990) Prey, predators, and parasites. In: Polis GA (ed) The biology of scorpions. Stanford University Press, Stanford, pp 294–320Google Scholar
  37. Meadows PS, Meadows A (1991) The environmental impact of burrowing animals and animal burrows. Symp Zool Soc London 63:349Google Scholar
  38. Meyer RC (1999) Helical burrows as a palaeoclimate response: Daimonelix by Palaeocastor. Palaeogeogr Palaeoclimatol Palaeoecol 147:291–298. doi: 10.1016/S0031-0182(98)00157-6 CrossRefGoogle Scholar
  39. Mineo MF, Del Claro K (2006) Mechanoreceptive function of pectines in the Brazilian yellow scorpion Tityus serrulatus: perception of substrate-borne vibrations and prey detection. Acta Ethol 9:79–85. doi: 10.1007/s10211-006-0021-7 CrossRefGoogle Scholar
  40. Monod L, Harvey MS, Prendini L (2013) Stenotopic Hormurus Thorell, 1876 scorpions from the monsoon ecosystems of northern Australia, with a discussion on the evolution of burrowing behaviour in Hormuridae Laurie, 1896. Rev Suisse Zool 120:281–346Google Scholar
  41. Navidpour SH, Vazirianzadeh B, Mohammadi A (2015) Burrowing activities of Scorpio maurus townsendi (Arachnida: Scorpionida: Scorpionidae) in province of Khouzestan sw Iran. J Entomol Zool Stud 3:270–274Google Scholar
  42. Newlands G (1972a) Ecological adaptations of Kruger National Park scorpionids (Arachnida: Scorpionides). Koedoe 15:37–48CrossRefGoogle Scholar
  43. Newlands G (1972b) Notes on psammophilous scorpions and a description of a new species (Arachnida: Scorpionida). Ann Transvaal Museum 27:241–257Google Scholar
  44. Newlands G (1978) Arachnida (except Acari). Biogeogr. Ecol. South. Africa, Vol. 2. W. Junk, The Hague, pp 677–684Google Scholar
  45. Oksanen J, Blanchet FG, Kindt R, et al. (2013) vegan: community ecology package.Google Scholar
  46. Polis GA (1990) Ecology. In: Polis GA (ed) The biology of scorpions Stanford University Press, Stanford, pp 247–293Google Scholar
  47. Polis GA, Sissom WD, McCormick SJ (1981) Predators of scorpions: field data and a review. J Arid Environ 4:309–326Google Scholar
  48. Polis GA, Myers C, Quinlan M (1986) Burrow biology and spatial distribution of desert scorpions. J Arid Environ 10:137–146Google Scholar
  49. Prendini L (2001) Substratum specialization and speciation in southern African scorpions: the effect hypothesis revisited. In: Fet V, Selden PA (eds) Scorpions 2001. In Memoriam Gary A. Polis. British Arachnological Society, Burnham Beeches, Bucks, pp 113–138Google Scholar
  50. Prendini L (2005) Scorpion diversity and distribution in southern Africa: pattern and process. In: Huber B, Sinclair BJ, Lampe K-H (eds) African Biodiversity Molecules, Organisms, Ecosystems, Proc. 5th Int. Symp. Trop. Biol. Museum Alexander Koenig, Bonn. Springer, Verlag, New York, pp 25–68Google Scholar
  51. Prendini L, Crowe TM, Wheeler WC (2003) Systematics and biogeography of the family Scorpionidae (Chelicerata: Scorpiones), with a discussion on phylogenetic methods. Invertebr Syst 17:185–259CrossRefGoogle Scholar
  52. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical ComputingGoogle Scholar
  53. Reichman O, Smith S (1990) Burrows and burrowing behavior by mammals. In: Genoways HH (ed) Curr. Mammal. Plenum Press, New York, New York, USA, pp 197–244Google Scholar
  54. Robertson HG, Nicolson SW, Louw GN (1982) Osmoregulation and temperature effects on water loss and oxygen consumption in two species of African scorpion. Comp Biochem Physiol Part A Physiol 71:605–609. doi: 10.1016/0300-9629(82)90210-9 CrossRefGoogle Scholar
  55. Rutin J (1996) The burrowing activity of scorpions (Scorpio maurus palmatus) and their potential contribution to the erosion of Hamra soils in Karkur, central Israel. Geomorphology 15:159–168CrossRefGoogle Scholar
  56. Shachak M, Brand S (1983) The relationship between sit and wait foraging strategy and dispersal in the desert scorpion, Scorpio maurus palmatus. Oecologia 60:371–377CrossRefGoogle Scholar
  57. Shivashankar T (1992) The importance of burrowing for the scorpion Heterometrus fulvipes Koch (Arachnida). J Soil Biol Ecol 12:134–138Google Scholar
  58. Shivashankar T (1994) Advanced sub social behaviour in the scorpion Heterometrus fulvipes Brunner (Arachnida). J Biosci 19:81–90CrossRefGoogle Scholar
  59. Shorthouse D, Marples T (1980) Observations on the burrow and associated behaviour of the arid-zone scorpion Urodacus yaschenkoi (Birula). Aust J Zool 28:581–590CrossRefGoogle Scholar
  60. Skutelsky O (1996) Predation risk and state-dependent foraging in scorpions: effects of moonlight on foraging in the scorpion Buthus occitanus. Anim Behav 52:49–57. doi: 10.1006/anbe.1996.0151 CrossRefGoogle Scholar
  61. Smith G (1966) Observations on the life history of the scorpion Urodacus abruptus (Scorpionidae), and the analysis of its home sites. Aust J Zool 14:383–398CrossRefGoogle Scholar
  62. Stull RB (1988) An introduction to boundary layer meteorology, 1st edn. Kluwer Academic Publishers, DordrechtGoogle Scholar
  63. Svendsen GE (1976) Structure and location of burrows of yellow-bellied marmot. Southwest Nat 20:487–494CrossRefGoogle Scholar
  64. Talal S, Tesler I, Sivan J et al (2015) Scorpion speciation in the Holy Land: multilocus phylogeography corroborates diagnostic differences in morphology and burrowing behavior among Scorpio subspecies and justifies recognition as phylogenetic, ecological and biological species. Mol Phylogenet Evol 91:226–237. doi: 10.1016/j.ympev.2015.04.028 CrossRefPubMedGoogle Scholar
  65. Tare T, Vad N, Renapurkar D (1993) Burrow patterns of the scorpion Heterometrus indus. Med Vet Entomol 7:102–104CrossRefPubMedGoogle Scholar
  66. Tilak R (1970) On an interesting observation on the living habit of Hormurus nigripes Pocock (Ischnuridae: Arachnida). Sci Cult 36:174–176Google Scholar
  67. Toolson E, Hadley N (1977) Cuticular permeability and epicuticular lipid composition in two Arizona vejovid scorpions. Physiol Zool 50:323–330CrossRefGoogle Scholar
  68. Tschinkel WR (2010) Methods for casting subterranean ant nests. J. Insect Sci. 10:88Google Scholar
  69. Turner JS (2000) The extended organism; the physiology of animal-built structures. Harvard University Press, CambridgeGoogle Scholar
  70. Turner JS (2001) On the mound of Macrotermes michaelseni as an organ of respiratory gas exchange. Physiol Biochem Zool 74:798–822. doi: 10.1086/323990 CrossRefPubMedGoogle Scholar
  71. Turner JS, Pinshow B (2015) Transient-state mechanisms of wind-induced burrow ventilation. J Exp Biol 218:170–175. doi: 10.1242/jeb.110858 CrossRefPubMedGoogle Scholar
  72. Venables WN, Ripley BD (2002) Modern applied statistics with S, Fourth. Springer, New YorkCrossRefGoogle Scholar
  73. Von Frisch K (1974) Animal architecture. Harcourt Brace Jovanovich, New YorkGoogle Scholar
  74. White C (2001) The energetics of burrow excavation by the inland robust scorpion, Urodacus yaschenkoi (Birula, 1903). Aust J Zool 49:663–674CrossRefGoogle Scholar
  75. Whitford WG, Kay FR (1999) Biopedturbation by mammals in deserts: a review. J Arid Environ 41:203–230. doi: 10.1006/jare.1998.0482 CrossRefGoogle Scholar
  76. Williams SC (1966) Burrowing activities of the scorpion Anuroctonus phaeodactylus (Wood) (Scorpionida: Vejovidae). Proc Calif Acad Sci 34:419–428Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Amanda M. Adams
    • 1
    • 5
  • Eugene Marais
    • 2
  • J. Scott Turner
    • 3
  • Lorenzo Prendini
    • 4
  • Berry Pinshow
    • 1
  1. 1.Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert ResearchBen-Gurion University of the NegevMidreshet Ben-GurionIsrael
  2. 2.Department of Entomology, National Museum of NamibiaWindhoekNamibia
  3. 3.Department of Environmental and Forest Biology, College of Environmental Science and ForestryState University of New YorkNew YorkUSA
  4. 4.Division of Invertebrate Zoology, American Museum of Natural HistoryNew YorkUSA
  5. 5.Department of BiologyTexas A&M UniversityCollege StationUSA

Personalised recommendations

Cite article

Buy options