Skip to main content
Log in

The supercooling ability of ticks (Acari, Ixodoidea)

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

The supercooling capacity of nine laboratory-held species of ticks originating from different geographical areas, as well as five field-collected species from Germany, was investigated. All but one tick species showed mean supercooling points between about-17 and -23°C, suggesting that the capacity to supercool to temperatures of ≤17°C might be an inherent property of many tick species unrelated to their geographic orgin. Photoperiod did not influence the mean supercooling point in any of the species and there was also no distinct seasonal pattern of supercooling in seasonally acclimatizedDermacentor marginatus. Thus, the supercooling ability was independent of the presence/absence of diapause. The finding of thermal hysteresis inD. marginatus hemolymph raises the question of whether or not anti-freeze proteins are involved in the supercooling capacity of that species. An interspecies comparison revealed a weak negative correlation between relative water content and supercooling point of the ticks and an even weaker correlation between body mass or body water mass and the supercooling point. Since the ticks exhibited low supercooling points both before and shortly after feeding, the blood used as food should lack potent ice nucleators.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

a.s.l. :

above sea level

LD :

longday (17 h light: 7 h darkness)

MP :

melting point

r.h. :

relative humidity

SCP :

supercooling point

SD :

shortday (10 h light: 14 h darkness)

THA :

thermal hysteresis activity

References

  • Balashov YS (1972) Bloodsucking ticks (Ixodoidea)—vectors of diseases of man and animals. Misc Publ Entomol Soc Am 8: 161–376

    Google Scholar 

  • Balashov YS (1989) Ecology of ticks (in Russian). Parazitol Sb 36: 56–82

    Google Scholar 

  • Bale JS (1993) Classes of insect cold hardiness. Funct Ecol 7: 751–753

    Google Scholar 

  • Belozerov VN (1982) Diapause and biological rhythms in ticks. In: Obenchain FD, Galun R (eds) Physiology of ticks. Pergamon Press, Oxford, pp 469–500

    Google Scholar 

  • Berkvens DL, Pegram RG, Brandt JRA (1995) A study of the diapausing behaviour ofRhipicephalus appendiculatus andR. zambeziensis under quasinatural conditions in Zambia. Med Vet Entomol 9: 307–315

    CAS  PubMed  Google Scholar 

  • Block W, Duman JG (1989) Presence of thermal hysteresis producing antifreeze proteins in the antarctic miteAlaskozetes antarcticus. J Exp Zool 250: 229–231

    Article  CAS  Google Scholar 

  • Cannon RJC (1986) Effects of contrasting relative humidities on the cold tolerance of an antarctic mite. J Ins Physiol 32: 523–534

    Google Scholar 

  • Cannon RJC, Block W, Collett GD (1985) Loss of supercooling ability inCryptopygus antarcticus (Collembola: Isotomidae) associated with water uptake. Cryo Lett 6: 73–80

    Google Scholar 

  • Dautel H, Knülle W (1996) Supercooling capacity of the ticksArgas reflexus andIxodes ricinus (Acari, Ixodoidea) from Germany: a comparative study. In: Needham GR, Horn DJ, Mitchell S (eds) Acarology IX: Proceedings. Ohio Biological Survey, Columbus, Ohio (in press)

    Google Scholar 

  • Denlinger DL (1991) Relationship between cold hardiness and diapause. In: Lee RE Jr, Denlinger DL (eds) Insects at low temperature. Chapman & Hall, New York, pp 174–198

    Google Scholar 

  • Doss MA, Farr MM, Rock KF, Anastos G (1978) Index-Catalogue of medical and veterinary zoology. Ticks and tickborne diseases. IV. Geographical distribution of ticks. US Dep Agric Spec Publ No 3

  • Duman JG, Xu L, Neven LG, Tursman D, Wu DW (1991) Haemolymph proteins involved in insect subzero-temperature tolerance: ice nucleators and antifreeze proteins. In: Lee RE Jr, Denlinger DL (eds) Insects at low temperature. Chapman & Hall, New York, pp 94–127

    Google Scholar 

  • Elsey KD (1993) Cold tolerance of the Southern green stink bug (Heteroptera: Pentatomidae). Environ Entomol 22: 567–570

    Google Scholar 

  • Enigk K (1954) On the biology of ticks (in German). Special Publication: Deutscher Entomologentag in Hamburg. Fischer, Jena

    Google Scholar 

  • Feldman-Muhsam B (1949) Hibernation ofHyalomma savignyi (Ixodidae) in Palestine. Bull Entomol Res 40: 305–306

    Google Scholar 

  • Feldman-Muhsam B (1981) Some observations on the hibernation ofRhipicephalus sanguineus in Jerusalem. Proceedings of International Conference on Tick Biology and Control, Grahamstown, South Africa, Rhodes Univ., Grahamstown, pp 205–207

  • Fields PG, McNeil JM (1986) Possible dual cold-hardiness strategies inCisspes fulvicollis. Can Entomol 118: 1309–1311

    Google Scholar 

  • Franks F (1985) Biophysics and biochemistry at low temperatures. Cambridge University Press, Cambridge

    Google Scholar 

  • Fujimoto K (1994) Comparison of the cold hardiness ofIxodes nipponensis andI. persulcatus (Acari: Ixodoidea) in relation to the distribution patterns of both species in the Chichibu mountains. Jpn J Sanit Zool 45: 333–339

    Google Scholar 

  • Gehrken U (1992) Inoculative freezing and thermal hysteresis in the adult beetlesIps acuminatus andRhagium inquisitor. J Ins Physiol 38: 519–524

    Google Scholar 

  • Gehrken U (1995) Correlative influence of gut appearance, water content and thermal hysteresis on whole body supercooling point of adult bark beetles,Ips acuminatus. Comp Biochem Physiol 112A: 207–214

    CAS  Google Scholar 

  • Gehrken U, Southon TE (1992) Supercooling in a freeze-tolerant cranefly larva,Tipula sp. J Ins Physiol 38: 131–137

    Google Scholar 

  • Gothe R, Hamel HD (1973) On the ecology of a German strain ofRhipicephalus sanguineus (Latreille, 1806) (in German). Z Parasitenkd 41: 157–172

    Article  Google Scholar 

  • Hanson SM, Craig GB Jr (1995) Relationship between cold hardiness and supercooling point inAedes albopictus eggs. J Am Mosquito Assoc 11: 35–38

    Google Scholar 

  • Hodkova M, Hodek I (1994) Control of diapause and supercooling by the retrocerebral complex inPyrrhocorus apterus. Entomol Exp Appl 70: 237–246

    Google Scholar 

  • Hoogstraal H (1956) African Ixodoidea. I. Ticks of the Sudan (with special reference to equatorial province and with preliminary reviews to the generaBoophilus, Margaropus andHyalomma). Research report US Naval Medical Research Unit No. 3, Cairo, Egypt. U.S. Government printing office

    Google Scholar 

  • Johnston SL, Lee RE Jr (1990) Regulation of supercooling and nucleation in a freeze intolerant beetle (Tenebrio molitor). Cryobiology 27: 562–568

    Article  Google Scholar 

  • Kahl O (1989) Investigations on the water balance of ticks (Acari: Ixodoidea) in the course of their postembryonic development with special reference to active water vapour uptake of the engorged phases (in German). PhD Thesis, FB Biology, Free University of Berlin

  • Kahl O, Janetzki C, Gray JS, Stein J, Bauch RJ (1992) Tick infection rates withBorrelia: Ixodes ricinus versusHaemaphysalis concinna andDermacentor reticulatus in two locations in eastern Germany. Med Vet Entomol 6: 363–366

    CAS  PubMed  Google Scholar 

  • Keirans JE (1992) Systematics of the Ixodida (Argasidae, Ixodidae, Nuttalliellidae): an overview and some problems. In: Fivaz B, Petney T, Horak I (eds) Tick vector biology. Springer, Berlin Heidelberg New York, pp 3–21

    Google Scholar 

  • Kirchner W (1987) Behavioral and physiological adaptations to cold. In: Nentwig W (ed) Ecophysiology of spiders. Springer, Berlin Heidelberg New York, pp 66–77

    Google Scholar 

  • Knight JD, Bale JS (1986) Cold hardiness and overwintering of the grain aphidSitobion avenae. Ecol Entomol 11: 189–197

    Google Scholar 

  • Knight JD, Bale JS, Franks S, Mathias SF, Baust JG (1986) Insect cold hardiness: supercooling points and pre-freeze mortality. Cryo Lett 7: 194–203

    Google Scholar 

  • Knülle W, Rudolph D (1982) Humidity relationship and water balance of ticks. In: Obenchain FD, Galun R (eds) Physiology of ticks. Pergamon Press, Oxford, pp 43–70

    Google Scholar 

  • Koštal V (1994) Changes in cold-hardiness and supercooling capacity during preimaginal development of the arctiid mothCymbalophora pudica (Lepidoptera: Arctiidae). Cryo Lett 15: 91–98

    Google Scholar 

  • Koštal V, Šimek P (1995) Dynamics of cold hardiness, supercooling and cryoprotectants in diapausing and non-diapausing pupae of the cabbage root fly.Delia radicum L. J Ins Physiol 41: 627–634

    Google Scholar 

  • Larsen KJ, Lee RE Jr (1994) Cold tolerance including rapid cold-hardening and inoculative freezing of fall migrant monarch butterflies in Ohio. J Ins Physiol 40: 859–864

    Article  Google Scholar 

  • Larsen KJ, Lee RE Jr, Nault LR (1993) Influence of developmental conditions on cold-hardiness of adultDalbulus leafhoppers — implications for overwintering. Entomol Exp Appl 67: 99–108

    Google Scholar 

  • Leather SR, Walters KFA, Bale JS (1993) The ecology of insect overwintering. Cambridge University Press, Cambridge

    Google Scholar 

  • Lee RE Jr (1991) Principles of insect low temperature tolerance. In: Lee RE Jr, Denlinger DL (eds) Insects at low temperatures. Chapman & Hall, New York, pp 17–46

    Google Scholar 

  • Lee RE Jr, Baust JG (1987) Cold-hardiness in the antarctic tick,Ixodes uriae. Physiol Zool 60: 499–506

    Google Scholar 

  • McEnroe WD (1984) The effect of snowcover on the American dog tick,Dermacentor variabilis (Say) (Acari: Ixodoidea) population under a harsh winter environment. Z Angew Entomol 97: 481–484

    Google Scholar 

  • McEnroe WD (1990) Stability ofDermacentor variabilis populations (Acari: Ixodoidea). Folia Parasitol (Prague) 37: 340–342

    CAS  Google Scholar 

  • Morewood WD (1992) Cold hardiness ofPhytoseiulus persimilis Athias-Henriot andAmblyseius cucumeris (Oudemans) (Acarina: Phytoseiidae). Can Entomol 124: 1015–1025

    Google Scholar 

  • Nedved O, Windsor D (1994) Supercooling ability, fat and water contents in a diapausing tropical beetle,Stenotarsus rotundus (Coleoptera, Endomychidae). Eur J Entomol 91: 307–312

    Google Scholar 

  • Needham GR, Teel PT (1991) Off-host physiological ecology of ixodid ticks. Annu Rev Entomol 36: 659–681

    Article  CAS  PubMed  Google Scholar 

  • Pugh PJA (1994) Supercooling points and water content in Acari. Acta Ecol 15: 71–77

    Google Scholar 

  • Ring RA, Danks HV (1994) Desiccation and cryoprotection: overlapping adaptations. Cryo Lett 15: 181–190

    Google Scholar 

  • Rojas RR, Charlet LD, Leopold RA (1994) Biochemistry and physiology of overwintering in the mature larva of the sunflower stem weevil,Cylindrocoptorus adspersus (Coleoptera: Curculionidae) in the Northern Great Plains. J Ins Physiol 40: 201–206

    Article  CAS  Google Scholar 

  • Salt RW (1953) The influence of food on cold hardiness of insects. Can Entomol 85: 261–269

    Google Scholar 

  • Salt RW (1963) Delayed inoculative freezing of insects. Can Entomol 95: 1190–1202

    Google Scholar 

  • Shimamda K, Riihima A (1988) Cold acclimation, inoculative freezing and slow cooling: essential factors contribution to the freeze-tolerance in diapausing larvae ofChymomyza costata. Cryo Lett 9: 5–10

    Google Scholar 

  • Skånland HT, Sømme L (1981) Seasonal variation in cold hardiness of the apple psyllidPsylla mali (Schmidb.) in Norway. Cryo Lett 2: 87–92

    Google Scholar 

  • Sømme L (1982) Supercooling and winter survival in terrestrial arthropods. Comp Biochem Physiol 73A: 519–543

    Google Scholar 

  • Sømme L, Strømme A, Zachariassen KE (1993) Notes on the ecology and physiology of the Antarctic oribatid miteMaudheimia wilsoni. Polar Res 12: 21–25

    Google Scholar 

  • Sonenshine DE (1979) Zoogeography of the American dog tick,Dermacentor variabilis. In: Rodriguez JG (ed) Recent advances in acarology, vol II. Acad Press, New York, pp 123–134

    Google Scholar 

  • Sonenshine DE (1988). Diapause in tick vectors of disease. In: Monath TP (ed) The arboviruses: epidemiology and ecology. CRC Press, Boca Raton, Fl, pp 219–244

    Google Scholar 

  • Sonenshine DE (1991) Biology of ticks, vol 1. Oxford University Press, New York

    Google Scholar 

  • Sonenshine DE (1993) Biology of ticks, vol 2. Oxford University Press, New York

    Google Scholar 

  • Tanaka K (1993) Seasonal change in cold tolerance of the house spider,Achaearanea tepidariorum (Araneae: Theridiidae). Acta Arachnol 42: 151–158

    Google Scholar 

  • Tanaka K, Udagawa T (1993) Cold adaptation of the terrestrial isopod,Porcellio scaber, to subnivean environments. J Comp Physiol B 163: 433–438

    Google Scholar 

  • Turnock WJ, Bracken CK (1989). Effects of low non-freezing temperatures on pupae of two species of diapausing, freeze-intolerant insects. Cryo Lett 10: 189–196

    Google Scholar 

  • Tursman D, Duman JG (1995) Cryoprotective effects of thermal hysteresis protein on survivorship of frozen gut cells from the freeze-tolerant centipedeLithobius forficatus. J Exp Zool 272: 249–257

    Article  CAS  Google Scholar 

  • Wilson PW, Leader JP (1995) Stabilization of supercooled fluids by thermal hysteresis proteins. Biophys J 68: 2098–2107

    CAS  PubMed  Google Scholar 

  • Young SR, Block W (1980) Experimental studies on the cold tolerance ofAlaskozetes antarcticus. J Ins Physiol 26: 189–200

    Article  Google Scholar 

  • Zachariassen KE (1985) Physiology of cold tolerance in insects. Physiol Rev 65: 799–832

    CAS  PubMed  Google Scholar 

  • Zachariassen KE, Husby JA (1982) Antifreeze effect of thermal hysteresis agents protects highly supercooled insects. Nature 298: 865–867

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by H. Langer

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dantel, H., Knülle, W. The supercooling ability of ticks (Acari, Ixodoidea). J Comp Physiol B 166, 517–524 (1996). https://doi.org/10.1007/BF02338295

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02338295

Key words

Navigation