Similar burrow architecture of three arid-zone scorpion species implies similar ecological function
- 490 Downloads
- 2 Citations
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 gradientsNotes
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
References
- 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
- Avenant NL, Nel JAJ (1997) Prey use by four syntopic carnivores in a strandveld ecosystem. South African J Wildl Res 27:86–93Google Scholar
- 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
- 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
- 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
- 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
- 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
- Crawford C, Riddle W (1975) Overwintering physiology of the scorpion Diplocentrus spitzeri. Physiol Zool 48:84–92CrossRefGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- Hadley NF (1970a) Water relations of the desert scorpion, Hadrurus arizonensis. J Exp Biol 53:547–58PubMedGoogle Scholar
- Hadley NF (1970b) Micrometeorology and energy exchange in two desert arthropods. Ecology 51:434–444CrossRefGoogle Scholar
- Hadley NF (1990) Environmental physiology. In: Polis GA (ed) The biology of scorpions. Stanford University Press, Stanford, pp 321–340Google Scholar
- Hansell M (1984) Animal architecture and building behavior. Longman, LondonGoogle Scholar
- Hansell M (2007) Built by animals: the natural history of animal architecture. Oxford University Press, Oxford, doi: 10.1086/592657
- Harington A (1978) Burrowing biology of the scorpion Cheloctonus jonesii Pocock (Arachnida: Scorpionida: Scorpionidae). J Arachnol 5:243–249Google Scholar
- 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
- 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
- King D, Green B (1979) Notes on diet and reproduction of the sand goanna, Varanus gouldii rosenbergi. Copeia 1979:64–70CrossRefGoogle Scholar
- Kinlaw A (1999) A review of burrowing by semi-fossorial vertebrates in arid environments. J Arid Environ 41:127–145CrossRefGoogle Scholar
- 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
- Koch LE (1970) Predation of the scorpion, Urodacus hoplurus, by the lizard Varanus gouldi. West Aust Nat 11:120–121Google Scholar
- 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
- 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
- Kotzman M, Lubin YD, Goldberg M (1989) Activities of a burrow-dwelling scorpion revealed at the surface. Acta Zool Fenn 190:205–208Google Scholar
- Krapf D (1986) Contact chemoreception of prey in hunting scorpions (Arachnida: Scorpiones). Zool Anz 217:119–129Google Scholar
- Krapf D (1988) Prey localization by trichobothria of scorpions. Proc. Eur. Arachnol. Colloquium, Berlin, pp 29–34Google Scholar
- 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
- Lamoral B (1979) The scorpions of Namibia (Arachnida-Scorpionida). Annu Natal Museum 23:497–784Google Scholar
- Levy G, Amitai P (1980) Fauna Palaestina. Arachnida I: Scorpiones. The Israeli Academy of Sciences and Humanities, JerusalemGoogle Scholar
- Martin LD, Bennett DK (1977) The burrows of the Miocene beaver Palaeocastor, Western Nebraska, U.S.A. Palaeogeogr Palaeoclimatol Palaeoecol 22:173–193Google Scholar
- 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
- Meadows PS, Meadows A (1991) The environmental impact of burrowing animals and animal burrows. Symp Zool Soc London 63:349Google Scholar
- 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
- 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
- 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
- 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
- Newlands G (1972a) Ecological adaptations of Kruger National Park scorpionids (Arachnida: Scorpionides). Koedoe 15:37–48CrossRefGoogle Scholar
- Newlands G (1972b) Notes on psammophilous scorpions and a description of a new species (Arachnida: Scorpionida). Ann Transvaal Museum 27:241–257Google Scholar
- Newlands G (1978) Arachnida (except Acari). Biogeogr. Ecol. South. Africa, Vol. 2. W. Junk, The Hague, pp 677–684Google Scholar
- Oksanen J, Blanchet FG, Kindt R, et al. (2013) vegan: community ecology package.Google Scholar
- Polis GA (1990) Ecology. In: Polis GA (ed) The biology of scorpions Stanford University Press, Stanford, pp 247–293Google Scholar
- Polis GA, Sissom WD, McCormick SJ (1981) Predators of scorpions: field data and a review. J Arid Environ 4:309–326Google Scholar
- Polis GA, Myers C, Quinlan M (1986) Burrow biology and spatial distribution of desert scorpions. J Arid Environ 10:137–146Google Scholar
- 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
- 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
- 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
- R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical ComputingGoogle Scholar
- 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
- 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
- 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
- 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
- Shivashankar T (1992) The importance of burrowing for the scorpion Heterometrus fulvipes Koch (Arachnida). J Soil Biol Ecol 12:134–138Google Scholar
- Shivashankar T (1994) Advanced sub social behaviour in the scorpion Heterometrus fulvipes Brunner (Arachnida). J Biosci 19:81–90CrossRefGoogle Scholar
- 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
- 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
- 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
- Stull RB (1988) An introduction to boundary layer meteorology, 1st edn. Kluwer Academic Publishers, DordrechtGoogle Scholar
- Svendsen GE (1976) Structure and location of burrows of yellow-bellied marmot. Southwest Nat 20:487–494CrossRefGoogle Scholar
- 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
- Tare T, Vad N, Renapurkar D (1993) Burrow patterns of the scorpion Heterometrus indus. Med Vet Entomol 7:102–104CrossRefPubMedGoogle Scholar
- Tilak R (1970) On an interesting observation on the living habit of Hormurus nigripes Pocock (Ischnuridae: Arachnida). Sci Cult 36:174–176Google Scholar
- Toolson E, Hadley N (1977) Cuticular permeability and epicuticular lipid composition in two Arizona vejovid scorpions. Physiol Zool 50:323–330CrossRefGoogle Scholar
- Tschinkel WR (2010) Methods for casting subterranean ant nests. J. Insect Sci. 10:88Google Scholar
- Turner JS (2000) The extended organism; the physiology of animal-built structures. Harvard University Press, CambridgeGoogle Scholar
- 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
- 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
- Venables WN, Ripley BD (2002) Modern applied statistics with S, Fourth. Springer, New YorkCrossRefGoogle Scholar
- Von Frisch K (1974) Animal architecture. Harcourt Brace Jovanovich, New YorkGoogle Scholar
- White C (2001) The energetics of burrow excavation by the inland robust scorpion, Urodacus yaschenkoi (Birula, 1903). Aust J Zool 49:663–674CrossRefGoogle Scholar
- 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
- Williams SC (1966) Burrowing activities of the scorpion Anuroctonus phaeodactylus (Wood) (Scorpionida: Vejovidae). Proc Calif Acad Sci 34:419–428Google Scholar