杂色山雀的反盗食贮食策略
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摘要
盗食现象在贮食动物中非常普遍,种内竞争者或种间竞争者的盗食是贮藏食物丢失的主要原因之一,同时也是贮食动物贮食行为不断进化的重要选择压力,开展反盗食贮食策略的研究有助于阐释贮食行为进化的原因和对贮食鸟类的保护。杂色山雀(Parus varius)秋季有明显的贮食行为,贮食方式为分散贮食。通过人为投食的方法,以投食点为中心,根据贮食点距投食点距离远近设定了被盗高风险区、被盗中风险区和被盗低风险区,研究杂色山雀个体在无潜在盗食者和有潜在盗食者的情况下,在上述3个风险区贮食比例的变化,探讨杂色山雀个体基于自身以及周围环境条件,在权衡取食及贮藏过程中时间及能量的花费和收益后,其反盗食贮食策略的选择。40只杂色山雀个体贮食策略的统计结果表明,不论潜在盗食者出现与否,杂色山雀个体贮食的总体趋势大致相同,即主要将食物贮藏在中风险区,而高风险区和低风险区贮食比例较低;比较种间和种内潜在盗食者出现的情况下与无潜在盗食者时,杂色山雀个体在各贮食风险区的贮食策略:种间及种内潜在盗食者的出现,都会引起被盗高风险区贮食比例降低(种间潜在盗食者:F=3.174,P<0.05;种内潜在盗食者:F=90.475,P<0.05),低风险区贮食比例上升(种间潜在盗食者:F=220.440,P<0.05;种内潜在盗食者:F=15.651,P<0.05);但种间潜在盗食者出现时,杂色山雀个体在被盗中风险区的贮食比例降低(F=143.749,P<0.05),而种内潜在盗食者出现时,杂色山雀个体在被盗中风险区贮食比例不变(F=0.776,P>0.05),即杂色山雀个体对种间潜在盗食者的出现更加敏感,防范盗食的投入更大。此外,分别比较无潜在盗食者、有种间潜在盗食者和有种内潜在盗食者存在的情况下,雌雄杂色山雀个体在各贮食风险区的反盗食贮食策略,发现其结果也明显不同。无潜在盗食者和种内潜在盗食者出现时,雄性杂色山雀为预防灾难性盗食发生而付出的努力较雌性个体高(无潜在盗食者:高风险区t=4.962,df=16.546,P<0.05;中风险区t=﹣0.890,df=29.255,P>0.05;低风险区t=﹣2.166,df=30,P<0.05。有种内潜在盗食者:高风险区t=﹣0.152,df=29,P>0.05;中风险区t=2.352,df=19.568,P<0.05;低风险区t=﹣2.287,df=19.563,P<0.05);种间潜在盗食者出现时,雌雄杂色山雀反盗食贮食策略趋于一致(高风险区t=1.361,df=29,P>0.05;中风险区t=﹣0.194,df=21.529,P>0.05;低风险区t=﹣1.599,df=29,P>0.05)。
The phenomenon of stealing food is very common in hoarding food animals.The hoarding food can be stolen by intraspecific or interspecific competitors,which are one of the main reasons for the loss of hoarding foods.Meanwhile,it is the main driving factor for the evolution of selection on the food storage behavior.Consequently,the study on the hoarding food strategy which avoid being stolen would be useful in uncovering the underlying mechanisms for the evolution of the hoarding food behavior,and protecting the hoarding food birds.The varied tit(Parus varius) has obvious behavior of hoarding food at autumn,and the storage mode is scattered.During October 2014,at Liaoning Province,Dalian,Fairy Cave National Nature Reserve(39°54′00″﹣40°03′00″N,122°53′24″﹣123°03′30″E),in the experimental zone,we chose seven appropriate respectively separated greater than 1 000 m areas.After that,we artificially placed Korean pine seeds,guided and set up one feeding point in each area.Then,with mist net method,we traped varied tits at the fixed feeding points,and released these bird after bird banding and taking the blood(Table 1).In this study,we artificially served the food in seven places and set the food source in the center.According to the distance from the cache site to the food source,the high pilferage risk area,medium pilferage risk area and low pilferage risk area was divided to study the change of hoarding food ratio of varied tits,according to the presence or absence of potential pilferers.We took into account the time and energy′s costs and profits of feeding and storage process to examine the strategy of varied tits in avoiding being stolen food storage strategy.The results showed that the trend in hoarding food strategy of varied tits was roughly similar whether there was potential thieves prey or not.Foods were mainly stored in the medium pilferage risk area,with the high pilferage risk area and low pilferage risk area storage food ratio was relatively low.The presence of interspecific and intraspecific potential pilferers had different and obvious influence on the hoarding food strategy of varied tits.The presence of interspecific and intraspecific potential pilferers decreased the food storage ratio of high pilferage risk area(interspecific potential pilferers:F = 3.174,P < 0.05; intraspecific potential pilferers:F = 90.475,P < 0.05) and increased that of low pilferage risk area(interspecific potential pilferers:F = 220.440,P < 0.05; intraspecific potential pilferers:F = 15.651,P < 0.05).Furthermore,when there was interspecific potential pilferers,the food storage ratio of medium pilferage risk area would be lower(F = 143.749,P < 0.05),but if there was intraspecific potential pilferers,the food storage ratio of medium pilferage risk area would not change(F = 0.776,P > 0.05).This means that the varied tits recognized and prevented from stealing food of interspecific pilferers more than intraspecific potential pilferers.In addition,in the three different situations,the male and the female varied tits′s hoarding food strategies were obviously different(Table 2).When there was no potential pilferers,and there was intraspecific potential pilferers,the male varied tits would took notice and prevented stealing food more than the females(There was no potential pilferers:high pilferage risk area t = 4.962,df = 16.546,P < 0.05; medium pilferage risk area t = ﹣0.890,df = 29.255,P > 0.05; low pilferage risk area t =﹣2.166,df = 30,P < 0.05.There was intraspecific potential pilferers:high pilferage risk area t =﹣0.152,df = 29,P > 0.05; medium pilferage risk area t = 2.352,df = 19.568,P < 0.05; low pilferage risk area t =﹣2.287,df = 19.563,P < 0.05).While there was interspecific potential pilferers,the results show that no significant difference was observed in the hoarding food strategy of the male and female varied tits(high pilferage risk area t = 1.361,df = 29,P > 0.05; medium pilferage risk area t =﹣0.194,df = 21.529,P > 0.05; low pilferage risk area t = ﹣1.599,df = 29,P > 0.05).
The phenomenon of stealing food is very common in hoarding food animals.The hoarding food can be stolen by intraspecific or interspecific competitors,which are one of the main reasons for the loss of hoarding foods.Meanwhile,it is the main driving factor for the evolution of selection on the food storage behavior.Consequently,the study on the hoarding food strategy which avoid being stolen would be useful in uncovering the underlying mechanisms for the evolution of the hoarding food behavior,and protecting the hoarding food birds.The varied tit(Parus varius) has obvious behavior of hoarding food at autumn,and the storage mode is scattered.During October 2014,at Liaoning Province,Dalian,Fairy Cave National Nature Reserve(39°54′00″﹣40°03′00″N,122°53′24″﹣123°03′30″E),in the experimental zone,we chose seven appropriate respectively separated greater than 1 000 m areas.After that,we artificially placed Korean pine seeds,guided and set up one feeding point in each area.Then,with mist net method,we traped varied tits at the fixed feeding points,and released these bird after bird banding and taking the blood(Table 1).In this study,we artificially served the food in seven places and set the food source in the center.According to the distance from the cache site to the food source,the high pilferage risk area,medium pilferage risk area and low pilferage risk area was divided to study the change of hoarding food ratio of varied tits,according to the presence or absence of potential pilferers.We took into account the time and energy′s costs and profits of feeding and storage process to examine the strategy of varied tits in avoiding being stolen food storage strategy.The results showed that the trend in hoarding food strategy of varied tits was roughly similar whether there was potential thieves prey or not.Foods were mainly stored in the medium pilferage risk area,with the high pilferage risk area and low pilferage risk area storage food ratio was relatively low.The presence of interspecific and intraspecific potential pilferers had different and obvious influence on the hoarding food strategy of varied tits.The presence of interspecific and intraspecific potential pilferers decreased the food storage ratio of high pilferage risk area(interspecific potential pilferers:F = 3.174,P < 0.05; intraspecific potential pilferers:F = 90.475,P < 0.05) and increased that of low pilferage risk area(interspecific potential pilferers:F = 220.440,P < 0.05; intraspecific potential pilferers:F = 15.651,P < 0.05).Furthermore,when there was interspecific potential pilferers,the food storage ratio of medium pilferage risk area would be lower(F = 143.749,P < 0.05),but if there was intraspecific potential pilferers,the food storage ratio of medium pilferage risk area would not change(F = 0.776,P > 0.05).This means that the varied tits recognized and prevented from stealing food of interspecific pilferers more than intraspecific potential pilferers.In addition,in the three different situations,the male and the female varied tits′s hoarding food strategies were obviously different(Table 2).When there was no potential pilferers,and there was intraspecific potential pilferers,the male varied tits would took notice and prevented stealing food more than the females(There was no potential pilferers:high pilferage risk area t = 4.962,df = 16.546,P < 0.05; medium pilferage risk area t = ﹣0.890,df = 29.255,P > 0.05; low pilferage risk area t =﹣2.166,df = 30,P < 0.05.There was intraspecific potential pilferers:high pilferage risk area t =﹣0.152,df = 29,P > 0.05; medium pilferage risk area t = 2.352,df = 19.568,P < 0.05; low pilferage risk area t =﹣2.287,df = 19.563,P < 0.05).While there was interspecific potential pilferers,the results show that no significant difference was observed in the hoarding food strategy of the male and female varied tits(high pilferage risk area t = 1.361,df = 29,P > 0.05; medium pilferage risk area t =﹣0.194,df = 21.529,P > 0.05; low pilferage risk area t = ﹣1.599,df = 29,P > 0.05).
引文
Andersson M,Krebs J R.1978.On the evolution of hoarding behavior.Animal Behavior,26(1):707-711.
Brodin A.2007.Theoretical models of adaptive energy management in small wintering birds.Philosophical Transactions of the Royal Society B:Biological Sciences,362(1486):1857-1871.
Carrascal L M,Moreno E.1993.Food caching versus immediate consumption in the nuthatch:the effect of social context.Ardea,81(2):135-135.
Chang G,Xiao Z,Zhang Z.2010.Effects of burrow condition and seed handling time on hoarding strategies of Edward′s long-tailed rat(Leopoldamys edwardsi).Behavioural Processes,85(2):163-166.
Clarke M F,Kramer D L.1994.Scatter-hoarding by a larder-hoarding rodent:intraspecific variation in the hoarding behavior of the eastern chipmunk,Tamias striatus.Anima Behaviour,48(2):299-308.
Clayton N S,Dally J M,Emery N J.2007.Social cognition by food-caching corvids-The western scrub-jay as a natural psychologist.Philosophical Transactions of the Royal Society of London B:Biological Sciences,362(1480):507-522.
Cowie R J,Krebs J R,Sherry D F.1981.Food storing in marsh tits.Animal Behaviour,29(4):1252-1259.
Dally J M,Clayton N S,Emery N J.2006a.The behaviour and evolution of cache protection and pilferage.Animal Behaviour72(1),13-23.
Dally J M,Emery N J,Clayton N S.2005.Cache protection strategies by western scrub-jays,Aphelocoma californica:implications for social cognition.Animal Behaviour,70(6):1251-1263
Dally J M,Emery N J,Clayton N S.2006b.Food-caching western scrub-jays keep track of who was watching when.Science,312(5780):1662-1665.
Emery N J,Clayton N S.2001.Effects of experience and social context on prospective caching strategies by scrub jays.Nature,414(6862):443-446.
Hart E B.1971.Food preference of the cliff chipmunk,Eutamias dorsalis,in northern Utah.Great Basin Naturalist,31(3):182-188.
Higuchi H.1977.Stored nuts castanopsis cuspidata as a food resource of nestling varied tits Parus varius.Japanese Journal of Ornithology,26(1):9-12.
Jenkins S H,Peters R A.1992.Spatial patterns of food storage by Merrian′s Kangaroo rats.Behavioral Ecology,3(1):60-65.
Kaufman D W.1973.Captive Barn Owls stockpile prey.Bird-Banding,44(3):225-225.
Leaver L A,Hopewell L,Caldwell C,et al.2007.Audiences effects on food caching in grey squirrels(Sciurus carolinensis):evidence for pilferage avoidance strategies.Animal Cognition10(1):23-27.
Lee T H.2002.Feeding and hoarding behavior of the Eurasian red squirrel Sciurus vulgaris during autumn in Hokkaido,Japan Acta Theriologica,47(4):459-470.
Lonsdale W M.1993.Losses from seed bank of mimosa pigra:soil micro-organisms vs temperature fluctuations.Journal of Applied Ecology,30(40):654-660.
Male L H,Smulders T V.2007.Hyperdispersed cache distributions reduce pilferage:a field study.Animal Behaviour,73(4),717-726.
Mccarty R,Southwick C H.1975.Food hoarding by the southern grasshopper mouse(Onychomys torridus)in laboratory enclosures.Journal of Mammalogy,56(1):708-712.
Nyby J,Wallace P,Owen K,et al.1973.An influence of hormones on hoarding behavior in the Mongolian gerbil(Meriones unguiculatus).Hormones and Behavior,4(4):283-288.
Smith C C,Reichman O J.1984.The evolution of food caching by bird and mammals.Annual Reviews of Ecology and Systematics,(15):329-351.
Solheim R.1984.Cachiong behavior,prey choice and surplus killing by pygmy owls Glaucidium passerinum during winter,a functional response of a generalist predator.Annales Zoologici Fennici,21(16):301-308.
Vander Wall S B,Balda R P.1981.Ecology and evolution of food-storage behavior in conifer-seed-caching corvids.Zeitschrift fur Tierpsychologie,56(3):217-242.
Vander Wall S B,Enders M S,Waitman B A.2009.Asymmetrical cache pilfering between yellow pine chipmunks and golden-mantled ground squirrels.Animal Behaviour,78(2):555-561.
Vander Wall S B,Jenkins S H.2003.Reciprocal pilferage and the evolution of food-hoarding behavior.Behavioral Ecology,14(5):656-667.
Wauters L A,Suhonen J,Dhondt A A.1995.Fitness consequences of hoarding behavior in the Euroasian red squirrel.Philosophical Transactions of the Royal Society Biological Sciences262(1365):277-281.
Wong R,Jones C H.1985.A coparative analysis of feeding and hoarding in hamsters and gerbils.Behavioural Processes,11(3)301-308.
Yi X F,Steele M A,Zhang Z B.2012.Acorn pericarp removal as a cache management strategy of the Siberian chipmunk,Tamias sibiricus.Ethology,118(1):87-94.
蔡玥,李东来,李其久,等.2014.杂色山雀繁殖期与非繁殖期食物组成及利用.动物学杂志,49(6):811-819.
霍雅鹏,曹军,张宇婷,等.2009.杂色山雀性别分子鉴定方法的研究.辽宁林业科技,1(1):3-13.
鲁长虎.2002.星鸦的贮食行为及其对红松种子的传播作用.动物学报,48(3):317-321.
鲁长虎,吴建平.1997.鸟类的贮食行为及研究.动物学杂志32(5):48-51.
奚长海,李东来,张雷,等.2015.食物和季节因素对杂色山雀贮食行为影响的研究.生态学报,35(15):5026-5031.
赵正阶.2001.中国鸟类志:下卷雀形目.长春:吉林科学技术出版社,709-710.
邹红菲,郑昕,马建章,等.2005.凉水自然保护区普通?贮食红松种子行为观察与分析.东北林业大学学报,33(1):68-70.
Brodin A.2007.Theoretical models of adaptive energy management in small wintering birds.Philosophical Transactions of the Royal Society B:Biological Sciences,362(1486):1857-1871.
Carrascal L M,Moreno E.1993.Food caching versus immediate consumption in the nuthatch:the effect of social context.Ardea,81(2):135-135.
Chang G,Xiao Z,Zhang Z.2010.Effects of burrow condition and seed handling time on hoarding strategies of Edward′s long-tailed rat(Leopoldamys edwardsi).Behavioural Processes,85(2):163-166.
Clarke M F,Kramer D L.1994.Scatter-hoarding by a larder-hoarding rodent:intraspecific variation in the hoarding behavior of the eastern chipmunk,Tamias striatus.Anima Behaviour,48(2):299-308.
Clayton N S,Dally J M,Emery N J.2007.Social cognition by food-caching corvids-The western scrub-jay as a natural psychologist.Philosophical Transactions of the Royal Society of London B:Biological Sciences,362(1480):507-522.
Cowie R J,Krebs J R,Sherry D F.1981.Food storing in marsh tits.Animal Behaviour,29(4):1252-1259.
Dally J M,Clayton N S,Emery N J.2006a.The behaviour and evolution of cache protection and pilferage.Animal Behaviour72(1),13-23.
Dally J M,Emery N J,Clayton N S.2005.Cache protection strategies by western scrub-jays,Aphelocoma californica:implications for social cognition.Animal Behaviour,70(6):1251-1263
Dally J M,Emery N J,Clayton N S.2006b.Food-caching western scrub-jays keep track of who was watching when.Science,312(5780):1662-1665.
Emery N J,Clayton N S.2001.Effects of experience and social context on prospective caching strategies by scrub jays.Nature,414(6862):443-446.
Hart E B.1971.Food preference of the cliff chipmunk,Eutamias dorsalis,in northern Utah.Great Basin Naturalist,31(3):182-188.
Higuchi H.1977.Stored nuts castanopsis cuspidata as a food resource of nestling varied tits Parus varius.Japanese Journal of Ornithology,26(1):9-12.
Jenkins S H,Peters R A.1992.Spatial patterns of food storage by Merrian′s Kangaroo rats.Behavioral Ecology,3(1):60-65.
Kaufman D W.1973.Captive Barn Owls stockpile prey.Bird-Banding,44(3):225-225.
Leaver L A,Hopewell L,Caldwell C,et al.2007.Audiences effects on food caching in grey squirrels(Sciurus carolinensis):evidence for pilferage avoidance strategies.Animal Cognition10(1):23-27.
Lee T H.2002.Feeding and hoarding behavior of the Eurasian red squirrel Sciurus vulgaris during autumn in Hokkaido,Japan Acta Theriologica,47(4):459-470.
Lonsdale W M.1993.Losses from seed bank of mimosa pigra:soil micro-organisms vs temperature fluctuations.Journal of Applied Ecology,30(40):654-660.
Male L H,Smulders T V.2007.Hyperdispersed cache distributions reduce pilferage:a field study.Animal Behaviour,73(4),717-726.
Mccarty R,Southwick C H.1975.Food hoarding by the southern grasshopper mouse(Onychomys torridus)in laboratory enclosures.Journal of Mammalogy,56(1):708-712.
Nyby J,Wallace P,Owen K,et al.1973.An influence of hormones on hoarding behavior in the Mongolian gerbil(Meriones unguiculatus).Hormones and Behavior,4(4):283-288.
Smith C C,Reichman O J.1984.The evolution of food caching by bird and mammals.Annual Reviews of Ecology and Systematics,(15):329-351.
Solheim R.1984.Cachiong behavior,prey choice and surplus killing by pygmy owls Glaucidium passerinum during winter,a functional response of a generalist predator.Annales Zoologici Fennici,21(16):301-308.
Vander Wall S B,Balda R P.1981.Ecology and evolution of food-storage behavior in conifer-seed-caching corvids.Zeitschrift fur Tierpsychologie,56(3):217-242.
Vander Wall S B,Enders M S,Waitman B A.2009.Asymmetrical cache pilfering between yellow pine chipmunks and golden-mantled ground squirrels.Animal Behaviour,78(2):555-561.
Vander Wall S B,Jenkins S H.2003.Reciprocal pilferage and the evolution of food-hoarding behavior.Behavioral Ecology,14(5):656-667.
Wauters L A,Suhonen J,Dhondt A A.1995.Fitness consequences of hoarding behavior in the Euroasian red squirrel.Philosophical Transactions of the Royal Society Biological Sciences262(1365):277-281.
Wong R,Jones C H.1985.A coparative analysis of feeding and hoarding in hamsters and gerbils.Behavioural Processes,11(3)301-308.
Yi X F,Steele M A,Zhang Z B.2012.Acorn pericarp removal as a cache management strategy of the Siberian chipmunk,Tamias sibiricus.Ethology,118(1):87-94.
蔡玥,李东来,李其久,等.2014.杂色山雀繁殖期与非繁殖期食物组成及利用.动物学杂志,49(6):811-819.
霍雅鹏,曹军,张宇婷,等.2009.杂色山雀性别分子鉴定方法的研究.辽宁林业科技,1(1):3-13.
鲁长虎.2002.星鸦的贮食行为及其对红松种子的传播作用.动物学报,48(3):317-321.
鲁长虎,吴建平.1997.鸟类的贮食行为及研究.动物学杂志32(5):48-51.
奚长海,李东来,张雷,等.2015.食物和季节因素对杂色山雀贮食行为影响的研究.生态学报,35(15):5026-5031.
赵正阶.2001.中国鸟类志:下卷雀形目.长春:吉林科学技术出版社,709-710.
邹红菲,郑昕,马建章,等.2005.凉水自然保护区普通?贮食红松种子行为观察与分析.东北林业大学学报,33(1):68-70.