Cold hardiness and biochemical response to low temperature of the unfed bush tick Haemaphysalis longicornis (Acari: Ixodidae)

Particle and Fibre Toxicology

Jing-Ze Liu²  Duo Wang²  Hui Wang²  Jie Chen²  Xiao-Long Yang²  Yu-Lan Lu¹  Zhi-Jun Yu² 

[1] Department of Biology, Langfang Normal College, Langfang, Hebei 065000, China;Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology of Hebei province, College of Life Sciences, Hebei Normal University, Shijiazhuang, Hebei 050016, China

关键词: Haemaphysalis longicornis;    Acclimation;    Cold hardiness;    Super-cooling capacity;   

Others  :  1181890
DOI  :  10.1186/1756-3305-7-346

 received in 2014-05-05, accepted in 2014-07-15,  发布年份 2014

【 摘 要 】

Background

The survival of overwintering ticks, is critical for their subsequent population dynamics in the spring, and consequent transmission of tick-borne diseases. Survival is largely influenced by the severity of the winter temperatures and their degree of cold hardiness at the overwintering stage. The bush tick Haemaphysalis longicornis, is widely distributed in China, and can transmit various pathogens that pose serious medical/veterinary problems. In the present study we investigated the effect of low temperature stress to tick survival, super-cooling point and body content of water, glycerol and total protein.

Methods

After various temperature acclimations, the super-cooling point was measured by Ni/CrNi-thermocouples with a precision temperature recorder. Water content was determined from weight loss of the sample exposed to 60°C for 48 h. Glycerol content was determined using Free Glycerol Reagent as directed by the manufacturer, and total protein was determined using the Bradford assay.

Results

The 50% mortality temperatures for the adults and nymphs were -13.7°C and -15.2°C, respectively; and the discriminating temperatures for the adults and nymphs were -16.0°C and -17.0°C, respectively. The super-cooling points of the adults and nymphs were -19.0°C and -22.7°C, respectively. The water content of adult H. longicornis decreased substantially after acclimation at 0°C for 10 d, whereas the nymphs decreased after acclimation at 0°C for 20 d, and the glycerol and proteins of both nymphs and adults were significantly increased (p < 0.01) when stressed at 0°C for 10 d.

Conclusions

In H. longicornis, low temperature stress can enhance its cold hardiness and trigger appropriate responses, including reducing water content, and increasing glycerol and total protein content.

【 授权许可】

   
2014 Yu et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Bale JS: Insects at low temperature: a predictable relationship. Funct Ecol 1991, 5:291-298.
• [2]Dantas-Torres F, Otranto D: Cold-stress response of engorged females of Rhipicephalus sanguineus. Exp Appl Acarol 2011, 54:313-318.
• [3]Brunner JL, Killilea M, Ostfeld RS: Overwintering survival of nymphal Ixodes scapularis (acari: ixodidae) under natural conditions. J Med Entomol 2012, 49:981-987.
• [4]Herrmann C, Gern L: Survival of Ixodes ricinus (acari: ixodidae) nymphs under cold conditions is negatively influenced by frequent temperature variations. Ticks Tick Borne Dis 2013, 4:445-451.
• [5]Denlinger DL: Relationship Between Cold Hardiness and Diapause. In Insects at Low Temperature. Edited by Lee RE, Denlinger DL. New York: Chapman and Hall; 1991.
• [6]Austen JM, Ryan UM, Friend JA, Ditcham WGF, Reid SA: Vector of Trypanosoma copemani identified as Ixodes sp. Parasitology 2011, 138:866-872.
• [7]Estrada-Peňa A, Ayllón N, de la Fuente J: Impact of climate trends on tick-borne pathogen transmission. Front Physiol 2012, 3:1-12.
• [8]Hwang KLH: Physiological Diversity and Temperature Hardening in Adult Tick Dermacentor Variabilis (Acari: Ixodidae). Ph D Thesis: The Ohio State University; 2006.
• [9]Dantas-Torres F: Biology and ecology of the brown dog tick, Rhipicephalus sanguineus. Parasit Vectors 2010, 3:1-11. BioMed Central Full Text
• [10]Neelakanta G, Sultana H, Fish D, Anderson JF, Fikrig E: Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold. J Clin Invest 2010, 120:3179-3190.
• [11]Burks CS, Stewart J, Richard L, Needham GR, Lee RE Jr: The role of direct chilling injury and inoculative freezing in cold tolerance of Amblyomma americanum, Dermacentor variabilis and Ixodes scapularis. Physiol Entomol 1996, 21:44-50.
• [12]Dantel H, Knülle W: The supercooling ability of ticks (acari, ixodoidea). J Comp Physiol B 1996, 166:517-524.
• [13]Stewart RL: Overwintering Ecology and Physiology of Amblyomma Americanum and Dermacentor Variabilis (Acari: Ixodidae) in Central Ohio. Ph D Thesis: The Ohio State University; 1998.
• [14]Dörr B, Gothe R: Cold-hardiness of Dermacentor marginatus (acari: ixodidae). Exp Appl Acarol 2001, 25:151-169.
• [15]Lee JH, Park HS, Jang WJ, Koh SE, Park TK, Kang SS, Kim BJ, Kook YH, Park KH, Lee SH: Identification of the Coxiella sp. detected from Haemaphysalis longicornis ticks in Korea. Microbiol Immunol 2004, 48:125-130.
• [16]Fujisaki K, Kawazu S, Kamio T: The taxonomy of the bovine Theileria spp. Parasitol Today 1994, 10:31-33.
• [17]Guan G, Moreau E, Liu J, Hao X, Ma M, Luo J, Chauvin A, Yin H: Babesia sp. BQ1 (lintan): molecular evidence of experimental transmission to sheep by Haemaphysalis qinghaiensis and Haemaphysalis longicornis. Parasitol Int 2010, 59:265-267.
• [18]Wu XB, Na RH, Wei SS, Zhu JS, Peng HJ: Distribution of tick-borne diseases in China. Parasit Vectors 2013, 6:119-127. BioMed Central Full Text
• [19]Yu X, Liang M, Zhang S, Liu Y, Li J, Sun Y, Zhang L, Zhang Q, Popov VL, Li C, Qu J, Li Q, Zhang Y, Hai R, Wu W, Wang Q, Zhan F, Wang X, Kan B, Wang S, Wan K, Jing H, Lu J, Yin W, Zhou H, Guan X, Liu J, Bi Z, Liu G, Ren J, et al.: Fever with thrombocytopenia associated with a novel Bunyavirus in China. N Engl J Med 2011, 364:1523-1532.
• [20]Kim CM, Kim MS, Park MS, Park JH, Chae JS: Identification of Ehrlichia chaffeensis, Anaplasma phagocytophilum, and A. bovis in Haemaphysalis longicornis and Ixodes persulcatus ticks from Korea. Vector-Borne Zoonot Dis 2003, 3:17-26.
• [21]Chen Z, Yang X, Bu F, Yang X, Yang X, Liu J: Ticks (acari: ixodoidea: argasidae, ixodidae) of China. Exp Appl Acarol 2010, 51:393-404.
• [22]Hoogstraal H, Kaiser MN, Kohls GM: The subgenus persicargas (ixodoidea, argasidae, argas). 4. Argas (P.) robertsi, new species, a parasite of Australian fowl, and keys to Australian argasid species. Ann Entomol Soc Am 1968, 62:535-539.
• [23]Tenquist JD, Charleston W: A revision of the annotated checklist of ectoparasites of terrestrial mammals in New Zealand. J Roy Soc New Zeal 2001, 31:481-542.
• [24]Zheng HY, Yu ZJ, Chen Z, Zhou LF, Zheng B, Ma H, Liu JZ: Development and biological characteristics of Haemaphysalis longicornis (acari: ixodidae) under field conditions. Exp Appl Acarol 2011, 53:377-388.
• [25]Liu J, Liu Z, Zhang Y, Yang X, Gao Z: Biology of Dermacentor silvarum (acari: ixodidae) under laboratory conditions. Exp Appl Acarol 2005, 36:131-138.
• [26]Powell SJ, Bale JS: Low temperature acclimated populations of the grain aphid Sitobion avenae retain ability to rapidly cold harden with enhanced fitness. J Exp Biol 2005, 208:2615-2620.
• [27]Carrillo MA, Cannon CA: Supercooling point variability in the Indian meal moth, Plodia interpunctella (Hübner) (Lepidoptera: pyralidae). J Stored Prod Res 2005, 41:556-564.
• [28]Bradford MM: A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
• [29]Lee RE Jr, Baust JG: Cold-hardiness in the Antarctic tick. Ixodes uriae Physiol Zool 1987, 60:499-506.
• [30]Dautel H, Knülle W: Cold hardiness, supercooling ability and causes of low-temperature mortality in the soft tick, Argas reflexus, and the hard tick, Ixodes ricinus (acari: ixodidae) from Central Europe. J Insect Physiol 1997, 43:843-854.
• [31]Needham GR, Jaworski DC, Chen CP, Lee RE: Cold-hardiness of a laboratory colony of lone star ticks (acari: ixodidae). J Med Entomol 1996, 33:706-710.
• [32]Stark U, Gothe R: Studies on the critical water mass, rehydration capability and potential, acute chill tolerance and supercooling point of Argas (Persicargas) walkerae (acari: ixodidae). Onderstepoort J Vet 2001, 68:11-20.
• [33]Pullin AS, Bale JS: Effects of low temperature on diapausing Aglais urticae and Inachis io (Lepidoptera: Nymphalidae): cold hardiness and overwintering survival. J Insect Physiol 1989, 35:277-281.
• [34]Ma RY, Hao SG, Tian J, Sun JH, Kang L: Seasonal variation in cold-hardiness of the Japanese pine sawyer Monochamus alternates (Coleoptera: cerambycidae). Environ Entomol 2006, 35:881-886.
• [35]Sømme L: Supercooling and winter survival in terrestrial arthropods. Comp Biochem Physiol A Physiol 1982, 73:519-543.
• [36]Kǒtál V: Cryoprotective role of polyols independent of the increase in supercooling capacity in diapausing adults of Pyrrhocoris apterus (Heteroptera: Insecta). Comp Biochem Physiol B: Biochem Mol Biol 2001, 130:365-374.
• [37]Worland MR: The relationship between water content and cold tolerance in the arctic collembola Onychiurus arcticus (Collembola: onychiuridae). Eur J Entomol 1996, 93:341-348.
• [38]Danks HY: The wider integration of studies on insect cold-hardiness. Eur J Entomol 1996, 93:383-403.
• [39]Sømme L: The physiology of cold hardiness in terrestrial arthropods. Eur J Entomol 1999, 96:1-10.
• [40]Ramløv H: Aspects of natural cold tolerance in ectothermic animals. Hum Reprod 2000, 15:26-46.
• [41]Villar M, Popara M, Ayllón N, de Mera IGF, Mateos-Hernández L, Galindo RC, Manrique M, Tobes R, de la Fuente J: A systems biology approach to the characterization of stress response in Dermacentor reticulatus tick unfed larvae. PloS One 2014, 9:e89564.