ACTA THERIOLOGICA SINICA >

2021 , Vol. 41 >Issue 4: 416 - 430

DOI: https://doi.org/10.16829/j.slxb.150532

ORIGINAL PAPERS

Effects of visual and olfactory density signals on social stress in Brandt's voles

  • HE Chen ,
  • HUANG Shuli ,
  • LIU Jing ,
  • SONG Yiran ,
  • LU Wei ,
  • ZHANG Zhibin
Expand
  • 1 State Key Lab of Integrated Management of Pest Insects and Rodent, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China;
    2 CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China;
    3 University of Chinese Academy of Science, Beijing 100049, China

Received date: 2021-02-09

  Online published: 2021-04-26

Fold

Abstract

Rodents have the density-dependent behavior-endocrine regulation mechanism.When their population density increases, it will increase social stress, nervous anxiety, aggression behaviors, as well as alter neuroendocrine in the brain.Social stress caused by increased density may involve different senses such as visual, olfactory, touch, hearing, andtaste, however, their distinct effects on social stress have never been evaluated.Our previous study indicates that high population density decreases the expression of oxytocin(OT) in the brain of male Brandt's voles(Lasiopodomys brandtii), increases the expression of arginine-vasopressin(AVP), and increases serum corticosteroid(CORT), which are linked to the increase of aggressive behavior.However, the role of olfactory and visual signals in triggering social stress is unknown.Because the olfactory signal is involved in marking the territory or dominance of animals, while the visual signal is involved in collective cooperation for defending territory against intruders or predators, the social stress effects may be different.We used nest pads and mirrors to simulate olfactory and visual density.To test the distinct effects of olfactory and visual density signals on social stress of Brandt's voles, we analyzed the behavioral(open-field test, elevated plus-maze test, and three-chamber sociability test), body weight, organs, serum physiological indicators, and brain neurotransmitter expression changes.We found that nest-pads treatment groups with high olfactory density decreased OT expression but increased AVP expression in specific brain regions of Brandt's voles, which is similar to the density effect(except for the OT increase in males).This result generally supported the hypothesis that high-density olfactory is the main signal path of density-dependent social stress.High visual density group treatment increased OT expression in males, but decreased expression of glucocorticoid receptor(GR), serum adrenocorticotropic hormone(ACTH), and anxiety behavior in females, supporting the hypothesis that high-density visual is the main signal path for reducing social stress.Our study suggests that visual and olfactory signals play a different, or even opposite role in the density-dependent behavioral or population regulation of social Brandt's voles, which may be beneficial in maintaining an optimal population density or group size.

Key words： Density-dependent; Social stress; Crowding effect; Olfactory density signals; Visual density signals

Cite this article

HE Chen , HUANG Shuli , LIU Jing , SONG Yiran , LU Wei , ZHANG Zhibin . Effects of visual and olfactory density signals on social stress in Brandt's voles[J]. ACTA THERIOLOGICA SINICA, 2021 , 41(4) : 416 -430 . DOI: 10.16829/j.slxb.150532

References

Ader R,Cohen N.1993.Psychoneuroimmunology:conditioning and stress.Annual Review of Psychology,44:53-85.
Amico J A,Challinor S M,Cameron J L.1990.Pattern of oxytocin concentrations in the plasma and cerebrospinal fluid of lactating rhesus monkeys(Macaca mulatta):evidence for functionally independent oxytocinergic pathways in primates.Journal of Clinical Endocrinol Metabolism,71(6):1531-1535.
Apfelbach R,Wiest H,Vasilieva N A.2001.Ferret(Mustela putorius f.furo) odor affects the estrous cycle in Campbell's hamster females(Phodopus campbelli).Wissenschaftliche Mitteilungen aus dem Nieder sterreichischen Landesmuseum,14:147-152.
Bester-Meredith J K,Marler C A.2003.Vasopressin and the transmission of paternal behavior across generations in mated,cross-fostered Peromyscus mice.Behavioral Neuroscience,117(3): 455-463.doi:10.1037/0735-7044.117.3.455.PMID:12802874.
Bian J H,Du S Y,Wu Y,Cao Y F,Nie X H,He H,You Z B.2015.Maternal effects and population regulation:maternal density-induced reproduction suppression impairs offspring capacity in response to immediate environment in root voles Microtus oeconomus.Journal of Animal Ecology,84(2):326-336.doi:10.1111/1365-2656.12307.Epub 2014 Nov 19.PMID:25327547.
Bian J H,Wu Y,Zhou K K.2008.Effects of population density on demography and individual corticosterone level during breeding period in root voles(Microtus oeconomus).Acta Theriologica Sinica,28(2):135-143.(in Chinese)
Boonstra R,Boag P T.1992.Spring declines in Microtus pennsylvanicus and role of steroid hormones.Journal of Animal Ecology,61:339-352.
Brown R E.1991.Effects of rearing condition,gender,and sexual experience on odor preferences and urine marking in Long-Evans rats.Animal Learning and Behavior,19(1):18-28.
Christian J J.1950.The adreno-pituitary system and population cycles in mammals.Journal of Mammal,31:247-259.
Christian J J.1980.Endocrine factors in population regulateon.In:Cohen M N,Malpass R S,Klein H G eds.Biosocial Mechanisms of Population Regulation.Yale University Press.New Haven.Connecticut,USA,55-115.
Chu W,Zhang W,Zhang H M.2016.Effects of a conspecific individual,a mirror image or video on foraging behavior of ICR mice(Mus musculus). Acta Theriologica Sinica,36(4):438-444.(in Chinese)
Dai X,Zhou L Y,Cao J X,Zhang Y Q,Yang F P,Wang A Q,Wei W H,Yang S M.2018.Effect of group density on the physiology and aggressive behavior of male Brandt's voles(Lasiopodomys brandtii).Zoological Studies,57:e35.doi:10.6620/ZS.57-35.
De Boer S F,Koolhaas J M.2005.5-HT1A and 5-HT1B receptor agonists and aggression:a pharmacological challenge of the serotonin deficiency hypothesis.European Journal of Pharmacology,526(1-3):125-139.
De Vries G J,Panzica G C.2006.Sexual differentiation of central vasopressin and vasotocin systems in vertebrates:Different mechanisms,similar endpoints.Neuroscience,138:947-955.
Dielenberg R A,McGregor I S.2001a.Defensive behavior in rats towards predatory odors:a review.Neuroscience and Biobehavioral Reviews,25(7-8):597-609.
Dielenberg R A,Carrive P,McGregor I S.2001b.The cardiovascular and behavioral response to cat odor in rats:unconditioned and conditioned effects.Brain Research,897(1-2):228-237.
Du S Y,Cao Y F,Nie X H,Wu Y,Bian J H.2016.The synergistic effect of density stress during the maternal period and adulthood on immune traits of root vole(Microtus oeconomus) individuals-a field experiment.
Oecologia,181(2):335-346.doi:10.1007/s00442-015-3445-9.
Edgar J L,Seaman S C.2010.The effect of mirrors on the behaviour of singly housed male and female laboratory rabbits.Animal Welfare,19(4):461-471.
Engelmann M,Ludwig M,Landgraf R.1994.Simultaneous monitoring of intracerebral release and behavior:endogenous vasopressin improves social recognition.Journal of Neuroendocrinol,6:391-395.
Fang J M,Sun R Y.1991.Seasonal dynamics of the spatial patterns of Brandt's voles.Acta Ecologica Sinica,11(2):111-116.(in Chinese)
Ferguson J N,Aldag J M,Insel T R,Young L J.2001.Oxytocin in the medial amygdala is essential for social recognition in the mouse. Journal of Neurosci,21(20):8278-8285.
Ferkin M H,Sorokin E S,Johnston R E.1995.Seasonal changes in scents and responses to them in meadow voles:evidence for the coevolution of signals and response mechanisms.Ethology,100:89-98.
Ferkin M H.2019.Scent marks of rodents can provide information to conspecifics.Animal Cognition,22(3):445-452.
Ferris C F,Potegal M.1988.Vasopressin receptor blockade in the anterior hypothalamus suppressed aggression in hamsters.Physiology and Behavior,44:235-239.
Genaro G,Schmidek W R,Franci C R.2004.Social condition affects hormone secretion and exploratory behavior in rats.Brazilian Journal of Medical and Biological Research,37(6):833-840.
Ghosal S,Bundzikova-Osacka J,Dolgas C M,Myers B,Herman J P.2014.Glucocorticoid receptors in the nucleus of the solitary tract(NTS) decrease endocrine and behavioral stress responses.Psychoneuroendocrinology,45:142-153.
Giovenardi M,Padoin M J,Cadore L P,Lucion A B.1998.Hypothalamic paraventricular nucleus modulates maternal aggression in rats:effects of ibotenic acid lesion and oxytocin antisense.Physiology and Behavior,63:351-359.
Gobrogge K L,Liu Y,Young L J,Wang Z.2009.Anterior hypothalamic vasopressin regulates pair-bonding and drug-induced aggression in a monogamous rodent.Proceedings of the National Academy of Sciences of the Unites States of America,106(45):19144-19149.
Goodson J L,Evans A K.2004.Neural responses to territorial challenge and nonsocial stress in male song sparrows:segregation,integration,and modulation by a vasopressin V-1 antagonist.Hormones and Behavior,46:371-381.
Gottfried J A,Zelano C.2011.The value of identity:olfactory notes on orbitofrontal cortex function.Annals of the New York Academy of Sciences,12(39):138-148.
Grandjean J,Corcoba A,Kahn M C,Upton A L,Deneris E S,Seifritz E,Helmchen F,Mann E O,Rudin M,Saab B J.2019.A brain-wide functional map of the serotonergic responses to acute stress and fluoxetine.Nature Communications,10(1):350.
Gromov V S.2007.Spatial ethological structure and evolution of sociality in rodents.Doklady Biological Sciences,412(1).doi:10.1134/S0012496607010152.
GroupⅠ,department of animal ecology,institute of zoology,academia sinica.1979.Investigations on population self-regulation in Brandt's voles-The relationships between population density,adrenal weight and gonadal weight.Acta Zoologica Sinica,25(2):154-167.(in Chinese)
Harrington J E.1976.Recognition fo territorial boundaries by olfactory cues in mice(Mus musculus L.).Z Tierpsychol,41(3):295-306.
Hennessey A C,Huhman K L,Albers H E.1994.Vasopressin and sex-differences in hamster flank marking.Physiology and Behavior,55:905-911.
Huang S,Li G,Pan Y,Song M,Zhao J,Wan X,Krebs C J,Wang Z,Han W,Zhang Z.2020.Density-induced social stress alters oxytocin and vasopressin activities in the brain of a small rodent species.Integrative Zoology.doi:10.1111/1749-4877.12467.
Huo Y,Fang Q,Shi Y L,Zhang Y H,Zhang J X.2014.Chronic exposure to a predator or its scent does not inhibit male-male competition in male mice lacking brain serotonin.Frontiers in Behavioral Neuroscience,8:116.
Jiang Y E,Enkhbold Nanj,Nyamdorj Batsaikhan,Wang D,Yi J,Wurenqimuge,Shan L Y,Du G L,Shi D Z.2012.Study on the habitat characteristics of Brandt's vole.Acta Agrestia Sinica,20(1):179-182.(in Chinese)
Johnson E O,Kamilaris T C,Chrousos G P,Gold P W.1992.Mechanisms of stress-a dynamic overview of hormonal and behavioral homeostasis.Neuroscience and Biobehavioral Reviews,16:115-130.
Karels T J,Boonstra R.2000.Concurrent density dependence and independence in populations of arctic ground squirrels.Nature,408(6811):460-463.
Kulesskaya N,Rauvala H,Voikar V.2011.Evaluation of social and physical enrichment in modulation of behavioural phenotype in C57BL/6J female mice. PLoS ONE,6:e24755.
Landgraf R,Neumann I,Schwarzberg H.1988.Central and peripheral release of vasopressin and oxytocin in the conscious rat after osmotic stimulation.Brain,457(2):219-225.
Leinwand S G,Chalasani S H.2011.Olfactory networks:from sensation to perception.Current Opinion in Genetics and Development,21(6):806-811.
Leroy F,Park J,Asok A,Brann D H,Meira T,Boyle L M,Buss E W,Kandel E R,Siegelbaum S A.2018.A circuit from hippocampal CA2 to lateral septum disinhibits social aggression.Nature,564(7735):213-218.
Li F H,Wang D H,Zhong W Q.2003.Population density and immune function in Brandt's voles(Microtus brandti).Current Zoology,(4):438-444.(in Chinese)
Li G,Yin B,Wan X,Wei W,Wang G,Krebs C J,Zhang Z.2016.Successive sheep grazing reduces population density of Brandt's voles in steppe grassland by altering food resources:a large manipulative experiment.Oecologia,180:149-159.
Li L,Hua Z D,Ren H Y,Bi Y Z,Liu X M,Xiao H W,Zhang L P,Zheng X M.2015.Anesthetic effects of tribromoethanol on mice.Hubei Agricultural Sciences,54(24):6328-6329.(in Chinese)
Lin E J,Choi E,Liu X,Martin A,During M J.2011.Environmental enrichment exerts sex-specific effects on emotionality in C57BL/6J mice.Behavioural Brain Research,216:349-357.
Liu J,Huang S,Li G,Zhao J,Lu W,Zhang Z.2020.High housing density increases stress hormone-or disease-associated fecal microbiota in male Brandt's voles(Lasiopodomys brandtii).Hormones and Behavior,126:104838.
Lubin D A,Elliott J C,Black M C,Johns J M.2003.An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior.Behavioral Neuroscience,117:195-201.
Mastellone V,Bovera F,Musco N,Panettieri V,Piccolo G,Scandurra A,Di Meo C,Attia Y A,Lombardi P.2019.Mirrors improve rabbit natural behavior in a free-range breeding system.Animals(Basel),9(8):533.
Meynen G,Unmehopa U A,van Heerikhuize J J,Hofman M A,Swaab D F,Hoogendijk W J G.2006.Increased arginine vasopressin mRNA expression in the human hypothalamus in depression:A preliminary report.Biological Psychiatry,60:892-895.
Moy S S,Nadler J J,Perez A,Barbaro R P,Johns J M,Magnuson T R,Piven J,Crawley J N.2004.Sociability and preference for social novelty in five inbred strains:an approach to assess autistic-like behavior in mice.Genes,Brain and Behavior,3(5):287-302.
Ostfeld R S,Canham C D,Pugh S R.1993.Intrinsic density-dependent regulation of vole populations.Nature,366(6452):259-261.
Pan Y,Liu Y,Young K A,Zhang Z,Wang Z.2009.Post-weaning social isolation alters anxiety-related behavior and neurochemical gene expression in the brain of male prairie voles.Neuroscience Letters,454(1):67-71.
Popik P,Vos P E,Van Ree J M.1992.Neurohypophyseal hormone receptors in the septum are implicated in social recognition in the rat.Behavioural Pharmacology,3(4):351-358.PMID:11224137.
Qiao X,Yan Y,Tai F,Wu R,Hao P,Fang Q,Zhang S.2014.Levels of central oxytocin and glucocorticoid receptor and serum adrenocorticotropic hormone and corticosterone in mandarin voles with different levels of sociability.Behavioural Brain Research,274:226-234.doi:10.1016/j.bbr.2014.08.020.Epub 2014 Aug 17.PMID:25141210.
Robinson I C,Jones P M.1982.Oxytocin and neurophysin in plasma and CSF during suckling in the guinea-pig.Neuroendocrinology,34(1):59-63.
Rodriguez-Barreto D,Rey O,Uren-Webster T M,Castaldo G,Consuegra S,Garcia de Leaniz C.2019.Transcriptomic response to aquaculture intensification in Nile tilapia.Evolutionary Applications,12(9):1757-1771.
Romero L M.2004.Physiological stress in ecology:lessons from biomedical research.Trends in Ecology and Evolution,19:249-255.
Ross H E,Cole C D,Smith Y,Neumann I D,Landgraf R,Murphy A Z,Young L J.2009.Characterization of the oxytocin system regulating affiliative behavior in female prairie voles.Neuroscience.162(4):892-903.
Sherwin C M.2004.Mirrors as potential environmental enrichment for individually housed laboratory mice.Applied Animal Behaviour Science,87:95-103.
Song C Y,Zhao X L,Yang J,Bai B,Wang C H,Lin B C.1991.Effects of stress on the contents of oxytocin,arg-vasopressin and β-endorphin in hypothalamus,pituitary and plasma in rats.Academic Journal of Second Military Medical University,12:128-131.
Toubas P L,Abla K A,Cao W,Logan L G,Seale T W.1990.Latency to enter a mirrored chamber-a novel behavioural assay for anxiolytic agents.Pharmacology,Biochemistry and Behavior,35:121-126.
Ueno H,Suemitsu S,Murakami S,Kitamura N,Wani K,Takahashi Y,Matsumoto Y,Okamoto M,Ishihara T.2020.Behavioural changes in mice after getting accustomed to the mirror.Behavioural neurology,4071315.https://doi.org/10.1155/2020/4071315.
Valstad M,Alvares G A,Andreassen O A,Westlye L T,Quintana D S.2016.The relationship between central and peripheral oxytocin concentrations:a systematic review and meta-analysis protocol.Systematic Reviews,5:49.
Veenema A H,Neumann I D.2008.Central vasopressin and oxytocin release:regulation of complex social behaviours.Progress in Brain Research,170:261-276.doi:10.1016/S0079-6123(08)00422-6.PMID:18655888.
Wan X,Zhong W,Wang M.1998.New flexible growth function and its application to the growth of small mammals.Growth,Development,and Aging,62(1-2):27-36.PMID:9666354.
Wan X R,Zhang X J,Liu W,Wang G H,Wang M J,Zhong W Q.2007.Social hierarchy and its seasonal changes of marked Lasiopodomys brandtii population.Chinese Journal of Ecology,26(3):359-362.(in Chinese)
Wang D W,Cong L,Wang Y,Liu X H.2010.Population parameters and physiological characteristics of Brandt's vole(Lasiopo-domys brandtii) in breeding and non-breeding seasons.Acta Ecologica Sinica,30(13):3562-3568.(in Chinese)
Wang T T,BaiMa C R,Hai S Z,Wang D.2015.Construction for the ethogram of Brandt's voles(Lasiopodomys brandtii).Acta Agrestia Sinica,23(3):646-652.(in Chinese)
Wang W G,Wu W T,Zhou J B,Yan H M.2011b.The use of the elevated plus maze to analyze anxiety behavior in mice.Chinese Journal of Cell Biology,33(5):466-472.(in Chinese)
Wang W G,Liu Z Z,Wu W T,Wan Y H,Yan H M.2011a.The use of open field test in the behavior analysis of mice.Chinese Journal of Cell Biology,33(11):1191-1196.(in Chinese)
Wynne-Edwards V C.1962.Animal dispersion in relation to social behaviour.Edinburgh:Oliver and Boyd.55s.
Zernig G,Pinheiro B S.2015.Dyadic social interaction inhibits cocaine-conditioned place preference and the associated activation of the accumbens corridor.Behavioural Pharmacology,26(6):580-594.
Zhang J,Zhang Z,Wang Z.2001a.Scent,social status and reproductive condition in Rat-like hamsters(Cricetulus triton).Physiology and Behavior,74:415-520.
Zhang J,Zhang Z,Wang Z.2001b.Males'olfactory discrimination of receptive state of females in Rat-like hamsters(Cricetulus triton).Chemical Signals in Vertebrate,9:385-390.
Zhang J X,Wang Z W,Zhang Z B.1999.Odor preference and behavioral interactions of ratlike hamsters(Cricetulus triton) during the nonbreeding season.Zoological Research,20(3):42-47.(in Chinese)
Zhang J,Zhong W Q.1981.On the colonial structure of Brandt's vole in burrow units.Acta Theriologica Sinica,1(1):51-56.(in Chinese)
Zhang L,Fang J M.1996.Discrimination of male adult Brandt's vole(Microtus brandti) on group odour during nonbreeding period.Acta Theriologica Sinica,16(4):285-290.(in Chinese)
Zhong W Q,Zhou Q Q,Sun C L.1985.The basic characteristics of the rodent pests on the pasture ininner Mongolia and the ecological strategies of controlling.Acta Theriologica Sinica,5(4):241-249.(in Chinese)
Zong S B,Wei S,Su Y X,Zhang H Y,Qiao M Q.2011.Retest reliability test and parameter correlation analysis of elevated plus-maze experiment for anxious rat model.China Medical Herald,8(30):5-7.(in Chinese)
王大伟,丛林,王宇,刘晓辉.2010.繁殖季节和非繁殖季节布氏田鼠种群参数和生理特点的差异.生态学报,30(13):3562-3568.
王涛涛,白玛次仁,海淑珍,王登.2015.布氏田鼠行为谱的构建.草地学报,23(3):646-652.
王维刚,刘震泽,吴文婷,万颖寒,严惠敏.2011a.小鼠动物实验方法系列专题(七)旷场实验在小鼠行为分析中的应用.中国细胞生物学学报,33(11):1191-1196.
王维刚,吴文婷,周嘉斌,严惠敏.2011b.小鼠动物实验方法系列专题(五)应用高架十字迷宫分析小鼠焦虑行为.中国细胞生物学学报,33(5):466-472.
中国科学院动物研究所生态室一组.1979.布氏田鼠种群内部调节的研究——种群密度、肾上腺和生殖腺重量之间的相互关系.动物学报,25(2):154-167.
边疆晖,吴雁,周抗抗.2008.繁殖期根田鼠种群密度对其种群统计参数及个体皮质酮水平的作用.兽类学报,28(2):135-143.
孙儒泳.1985.种群的科学管理与数学模型——动物的盛衰兴亡.上海:上海科学技术出版社,79.
李凤华,王德华,钟文勤.2003.密度因素对布氏田鼠体重增长及免疫功能的影响.动物学报,49(4):438-444.
李莉,华再东,任红艳,毕延震,刘西梅,肖红卫,张立苹,郑新民.2015.三溴乙醇对小鼠麻醉效果的研究.湖北农业科学,54(24):6328-6329.
李健,李梦云,廖成水.2018.实验鼠解剖组织彩色图谱.生物技术通讯,29(3):386.
张立,房继明.1996.非繁殖期成年雄性布氏四鼠对群体气味的辨别.兽类学报,16(4):285-290.
张洁,钟文勤.1981.布氏田鼠洞群内群体结构的研究.兽类学报,1(1):51-56.
张健旭,王祖望,张知彬.1999.非繁殖期大仓鼠对同种气味的反应和个体间的行为关系.动物学研究,20(3):42-47.
房继明,孙儒泳.1991.布氏田鼠空间分布格局的季节动态.生态学报,11(2):111-116.
宛新荣,张新阶,刘伟,王广和,王梦军,钟文勤.2007.布氏田鼠标志种群的社群等级及其季节变化.生态学杂志,26(3):359-362.
宗绍波,魏盛,苏云祥,张惠云,乔明琦.2011.焦虑大鼠模型高架十字迷宫实验的复测信度检验及参数相关性分析.中国医药导报,8(30):5-7.
倪道凤.2010.《嗅觉基础与临床》出版.中国眼耳鼻喉科杂志,10(4):231.
钟文勤,周庆强,孙崇潞.1985.内蒙古草场鼠害的基本特征及其生态对策.兽类学报,5(4):241-249.
储薇,张维,张洪茂.2016.实体、镜像及影像对ICR小鼠取食行为的影响.兽类学报,36(4):438-444.
蒋永恩,Enkhbold Nanj,Nyamdorj Batsaikhan,王登,易津,乌仁其木格,单丽燕,杜桂林,施大钊.2012.布氏田鼠栖息地特征的研究.草地学报,20(1):179-182.
Options
Outlines

/

〈 〉

　青公网安备 63010402000199号 青ICP备05000010号-2
Copyright © ACTA THERIOLOGICA SINICA, All Rights Reserved.
Tel: +86-971-6143617　Fax: +86-971-6143282　E-mail: slxb@nwipb.cas.cn
Powered by Beijing Magtech Co., Ltd.