AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Avian Research Article
PDF (553.1 KB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research | Open Access

Mild spring temperature rising affects the anti-oxidation and immune functions of Asian Short-toed Larks

Na Zhu1, Tingting Liu1, Fei Wang1, Wei Liang2, Shuping Zhang1( )
College of Life and Environment Sciences, Minzu University of China, Beijing 100081, China
Ministry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou 571158, China
Show Author Information

Abstract

Background

Predicting the possibility of severe effects of global warming on animals is important for understanding the ecological consequences of climate change on ecosystem. Spring is the season during which birds have to physiologically prepare for the subsequent breeding period, and unusual spring temperature rising probably becomes a heat stress to the birds which have adapted to the low spring temperature. Therefore, it is necessary to understand the physiological effect of spring warming on the temperate birds.

Methods

Using the activities of blood anti-oxidative enzymes (SOD, CAT, GPx) and the concentrations of serum immunogloblins (IgA, IgY, IgM) as indicators, we compared the anti-oxidative and immune functions of Asian Short-toed Larks (Calandrella cheleensis) captured between 10 and 15 March, 2015 and housed under conditions of 21 ℃ and 16 ℃.

Results

The SOD activities of birds in 21 ℃ group were significantly lower than those in 16 ℃ group on all the treatment days. The CAT activities of the birds in 21 ℃ group were significantly lower than those in 16 ℃ group on the 1st, 5th, 13th, 17 treatment days. The GPx activities of the birds in 21 ℃ group were signifthicantly lower than those in 16 ℃ group on the 1st, 13th and 17th, but significantly higher on the 21st treatment day. The IgA, IgY and IgM concentrations of birds in 21 ℃ group were significantly lower than those in 16 ℃ group on all the treatment days.

Conclusions

This study shows that spring temperature rising negatively influences antioxibative and humoral immune functions, which indicates that spring climate warming might reduce the fitness of the temperate passerine birds which have adapted to the low spring temperature.

Keywords

Mild temperature risingAnti-oxidant capacityImmunityAsian Short-toed LarksSpring

References

 

Alonso-Álvarez C, Pérez-Rodríguez L, Garcia JT, Vinuela J, Mateo R. Age and breeding effort as sources of individual variability in oxidative stress markers in a bird species. Physiol Biochem Zool. 2010;83:110-8.
Crossref Google Scholar
 

Altan N, Se-Dinc A, Sahin D, Kocamanoglu N, Kosova F, Engin A. Oxidative DNA damage: the thyroid hormone-mediated effects of insulin on liver tissue. Endocrine. 2010;38:214-20.
Crossref Google Scholar
 

Altan O, Pabuccuoglu A, Altan A, Konyalioglu S, Bayraktar H. Effect of heat stress on oxidative stress, lipid peroxidation and some stress parameters in broilers. Poult Sci. 2003;44:545-50.
Crossref Google Scholar
 

Atif SM, Gibbings SL, Redente EF, Camp FA, Torres RM, Kedl RM, et al. Immune surveillance by natural IgM is required for early neoantigen recognition and initiation of adaptive immunity. Am J Respir Cell Mol Biol. 2018;59:580-91.
Crossref Google Scholar
 

Azad MA, Kikusato M, Maekawa T, Shirakawa H, Toyomizu M. Metabolic characteristics and oxidative damage to skeletal muscle in broiler chickens exposed to chronic heat stress. Comp Biochem Physiol A. 2010;155:401-6.
Crossref Google Scholar
 

Bar-Shira E, Cohen I, Elad O, Friedman A. Role of goblet cells and mucin layer in protecting maternal IgA in precocious birds. Dev Comp Immunol. 2014;44:186-94.
Crossref Google Scholar
 

Baxter A, Mittler R, Suzuki N. ROS as key players in plant stress signalling. J Exp Bot. 2014;65:1229-40.
Crossref Google Scholar
 

Bencina D, Narat M, Bidovec A, Zorman-Rojs O. Transfer of maternal immunoglobulins and antibodies to Mycoplasma gallisepticum and Mycoplasma synoviae to the allantoic and amniotic fluid of chicken embryos. Avian Pathol. 2005;34:463-72.
Crossref Google Scholar
 

Chin EH, Quinn JS, Burness G. Acute stress during ontogeny suppresses innate, but not acquired immunity in a semi-precocial bird (Larus delawarensis). Gen Comp Endocrinol. 2013;193:185-92.
Crossref Google Scholar
 

Costantini D, Ferrari C, Pasquaretta C, Cavallone E, Carere C, von Hardenberg A, et al. Interplay between plasma oxidative status, cortisol and coping styles in wild alpine marmots Marmota marmota. J Exp Biol. 2012;215:374-83.
Crossref Google Scholar
 

Costantini D, Verhulst S. Does high antioxidant capacity indicate low oxidative stress? Func Ecol. 2009;23:506-9.
Crossref Google Scholar
 

Díaz-Zaragoza M, Hernández-Ávila R, Viedma-Rodríguez R, Arenas-Aranda D, Ostoa-Saloma P. Natural and adaptive IgM antibodies in the recognition of tumor-associated antigens of breast cancer (Review). Oncol Rep. 2015;34:1106-14.
Crossref Google Scholar
 

Erasmus BFN, Van Jaarsveld AS, Chown SL, Kshatriya M, Wessels KJ. Vulnerability of South African animal taxa to climate change. Global Change Biol. 2002;8:679-93.
Crossref Google Scholar
 

Feder ME, Hofmann GE. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol. 1999;61:243-82.
Crossref Google Scholar
 

Flanagan SW, Moseley PL, Buettner GR. Increased flux of free radicals in cells subjected to hyperthermia: detection by electron paramagnetic resonance spin trapping. FEBS Lett. 1998;431:285-6.
Crossref Google Scholar
 

Folguera G, Bastias DA, Caers J, Rojas JM, Piulachs MD, Belles X, et al. An experimental test of the role of environmental temperature variability on ectotherm molecular, physiological and life-history traits: implications for global warming. Comp Biochem Physiol A Mol Integr Physiol. 2011;159:242-6.
Crossref Google Scholar
 

Glover CN. Defence mechanisms: the role of physiology in current and future environmental protection paradigms. Conserv Physiol. 2018;6:coy012.
Crossref Google Scholar
 

Goutte A, Angelier F, Chastel CC, Trouve C, Moe B, Bech C, et al. Stress and the timing of breeding: glucocorticoid-luteinizing hormones relationships in an arctic seabird. Gen Comp Endocrinol. 2010;169:108-16.
Crossref Google Scholar
 

Habibian M, Ghazi S, Moeini MM, Abdolmohammadi A. Effects of dietary selenium and vitamin E on immune response and biological blood parameters of broilers reared under thermoneutral or heat stress conditions. Int J Biometeorol. 2014;58:741-52.
Crossref Google Scholar
 

Hamdoun AM, Cheney DP, Cherr GN. Phenotypic plasticity of HSP70 and HSP70 gene expression in the Pacific oyster (Crassostrea gigas): implications for thermal limits and induction of thermal tolerance. Biol Bull. 2003;205:160-9.
Crossref Google Scholar
 

Hegemann A, Matson KD, Versteegh MA, Tieleman BI. Wild skylarks seasonally modulate energy budgets but maintain energetically costly inflammatory immune responses throughout the annual cycle. PLoS ONE. 2012;7:e36358.
Crossref Google Scholar
 

Huang C, Jiao H, Song Z, Zhao J, Wang X, Lin H. Heat stress impairs mitochondria functions and induces oxidative injury in broiler chickens. J Anim Sci. 2015;93:2144-53.
Crossref Google Scholar
 

Huang T, Wu K, Yuan X, Shao S, Wang W, Wei S, et al. Molecular analysis of the immunoglobulin genes in goose. Dev Comp Immunol. 2016;60:160-6.
Crossref Google Scholar
 

Kannan K, Jain SK. Oxidative stress and apoptosis. Pathophysiology. 2000;7:153-63.
Crossref Google Scholar
 

Kaspers B, Bondl H, Göbel TWF. Transfer of IgA from albumen into the yolk sac during embryonic development in the chicken. J Vet Med A. 1996;43:225-31.
Crossref Google Scholar
 

Li M, Zhu WW, Wang Y, Sun YF, Li JY, Liu XL, et al. Effects of capture and captivity on plasma corticosterone and metabolite levels in breeding Eurasian tree sparrows. Avian Res. 2019;10:16.
Crossref Google Scholar
 

Lin H, De Vos D, Decuypere E, Buyse J. Dynamic changes in parameters of redox balance after mild heat stress in aged laying hens (Gallus gallus domesticus). Comp Biochem Physiol C Toxicol Pharmacol. 2008;147:30-5.
Crossref Google Scholar
 

Marshall AJ, Serventy DL. Inheritance and neuroendocrine adaptations in birds. Gen Comp Endocr. 1962;1:217-26.
Crossref Google Scholar
 

McKechnie AE, Hockey PAR, Wolf BO. Feeling the heat: Australian landbirds and climate change. Emu. 2012;112:i-vii.
Crossref Google Scholar
 

Morales-Suarez-Varela MM, Olsen J, Johansen P, Kaerlev L, Guenel P, Arveux P, et al. Occupational sun exposure and mycosis fungoides: a European multicenter case-control study. J Occup Environ Med. 2006;48:390-3.
Crossref Google Scholar
 

Mujahid A, Yoshiki Y, Akiba Y, Toyomizu M. Superoxide radical production in chicken skeletal muscle induced by acute heat stress. Poultry Sci. 2005;84:307-14.
Crossref Google Scholar
 

Nilsson JA, Raberg L. The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia. 2001;128:187-92.
Crossref Google Scholar
 

Park S, Hwangbo J, Ryu CM, Park BS, Chae HS, Choi HC, et al. Effects of extreme heat stress on growth performance, lymphoid organ, IgY and cecum microflora of broiler chickens. Int J Agric Biol. 2013;15:1204-8.
Google Scholar
 

Peppas I, Sollie S, Josephs DH, Hammar N, Walldius G, Karagiannis SN, et al. Serum immunoglobulin levels and the risk of bladder cancer in the AMORIS Cohort. Cancer Epidemiol. 2019;62:101584.
Crossref Google Scholar
 

Qin X, Liu T, Zhao L, Liang W, Zhang S. Marked daily variation in spring temperature induces variation in Caspase-3, Bcl-2 and HSP60 in Asian Short-toed Larks: how do wild birds maintain cellular homeostasis to cope with the ambient temperature variation? J Ornithol. 2017;158:1025-34.
Crossref Google Scholar
 

Quintana FJ, Cohen IR. The HSP60 immune system network. Trends Immunol. 2011;32:89-95.
Crossref Google Scholar
 

Rose ME, Orlans E, Buttress N. Immunoglobulin classes in the hen's egg: their segregation in yolk and white. Eur J Immunol. 1974;4:521-3.
Crossref Google Scholar
 

Sapolsky RM, Romero L, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev. 2000;21:55-89.
Crossref Google Scholar
 

Silverin B, Wingfield J, Stokkan KA, Massa R, Jarvinen A, Andersson NA, et al. Ambient temperature effects on photo induced gonadal cycles and hormonal secretion patterns in Great Tits from three different breeding latitudes. Horm Behav. 2008;54:60-8.
Crossref Google Scholar
 

Somero GN. The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine 'winners' and 'losers'. J Exp Biol. 2010;213:912-20.
Crossref Google Scholar
 

Stevenson IR, Bryant DM. Climate change and constraints on breeding. Nature. 2000;406:366-7.
Crossref Google Scholar
 

Swanson DL. Seasonal metabolic variation in birds: functional and mechanistic correlates. Curr Ornithol. 2010;17:75-129.
Crossref Google Scholar
 

Tomanek L. Variation in the heat shock response and its implication for predicting the effect of global climate change on species' biogeographical distribution ranges and metabolic costs. J Exp Biol. 2010;213:971-9.
Crossref Google Scholar
 

Welbergen JA, Klose SM, Markus N, Eby P. Climate change and the effects of temperature extremes on Australian flying-foxes. Proc R Soc B. 2008;275:419-25.
Crossref Google Scholar
 

Wiersma P, Selman C, Speakman JR, Verhulst S. Birds sacrifice oxidative protection for reproduction. Proc R Soc Lond B. 2004;271:S360-3.
Crossref Google Scholar
 

Wingfield JC, Smith JP, Farner DS. Endocrine responses of White-crowned Sparrows to environmental stress. Condor. 1982;84:399-409.
Crossref Google Scholar
 

Yang J, Liu L, Sheikhahmadi A, Wang Y, Li C, Jiao H, et al. Effects of corticosterone and dietary energy on immune function of broiler chickens. PLoS ONE. 2015;10:e0119750.
Crossref Google Scholar
 

Zhao L, Gao L, Yang W, Xu X, Wang W, Liang W, et al. Do migrant and resident species differ in the timing of increases in reproductive and thyroid hormone secretion and body mass? A case study in the comparison of pre-breeding physiological rhythms in the Eurasian Skylark and Asian Short-toed Lark. Avian Res. 2017a;8:10.
Crossref Google Scholar
 

Zhao Y, Li M, Sun Y, Wu W, Kou G, Guo L, et al. Life-history dependent relationships between body condition and immunity, between immunity indices in male Eurasian tree sparrows. Comp Biochem Phys A. 2017b;210:7-13.
Crossref Google Scholar
 

Zheng WH, Li M, Liu JS, Shao SL, Xu XJ. Seasonal variation of metabolic thermogenesis in Eurasian tree sparrows (Passer montanus) over a latitudinal gradient. Physiol Biochem Zool. 2014;87:704-18.
Crossref Google Scholar
 

Zulkifli I, Dunnington EA, Gross WB, Siegel PB. Inhibition of adrenal steroidogenesis, food restriction and acclimation to high ambient temperatures in chickens. Poult Sci. 1994;35:417-26.
Crossref Google Scholar
Avian Research
Volume 11 Issue 1,
January 2020
Article number: 12
DOI: 10.1186/s40657-020-00199-5
Cite this article:
Zhu N, Liu T, Wang F, et al. Mild spring temperature rising affects the anti-oxidation and immune functions of Asian Short-toed Larks. Avian Research, 2020, 11(1): 12. https://doi.org/10.1186/s40657-020-00199-5

571

Views

21

Downloads

2

Crossref

N/A

Web of Science

2

Scopus

0

CSCD

Altmetrics
Received: 18 November 2019
Accepted: 26 April 2020
Published: 30 April 2020
© The Author(s) 2020.

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-sa/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
Return