饥饿对中华倒刺鲃幼鱼代谢、个性和集群的影响
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摘要
在自然界中,环境变化、季节更替和人为因素造成食物资源时空分布的不均一性,导致鱼类经常面临食物资源短缺的环境胁迫,对其能量代谢和行为造成一定影响。为考察食物资源短缺下暖水性鲤科鱼类能量代谢、个性与集群行为的应对策略及其可能的内在关联,选取中华倒刺鲃(Spinibarbus sinensis)幼鱼为实验对象,分别测定饥饿组(2周)和对照组(维持日粮)在处理前后实验鱼的标准代谢率(Standard metabolic rate,SMR)、个性行为(勇敢性、探索性和活跃性)以及实验处理后的集群行为(凝聚力和协调性)。研究发现:(1)饥饿组和对照组实验过程中实验鱼SMR均显著下降,但仅饥饿组实验鱼SMR具有重复性;(2)饥饿导致中华倒刺鲃幼鱼勇敢性、探索性、活跃性均显著增加;(3)饥饿导致群体成员间距离缩短,游泳速度及其同步性上升。研究表明:饥饿后的中华倒刺鲃不仅适应性降低SMR以减少能量消耗,而且呈现出更高的勇敢性、探索性和活跃性以利于获取食物资源;饥饿迫使中华倒刺鲃群体提高凝聚力和协调性,可能有助于提高群体的生存能力。
Fishes in natural environments are often affected by food resources as a result of environmental and seasonal changes,and human activities. Feeding is a fundamental physiological function,which provides essential energy for the survival,growth,and reproduction of fishes. We selected juvenile Spinibarbus sinensis( Cyprinidae) to investigate the adaptive responses of energetic metabolism,fish behavior,and shoaling to food shortages and the possible interaction between energetic metabolism and physiology. We first measured the standard metabolic rate( SMR) and fish behavior( including boldness,exploration,and activity) of experimental fish before and after two weeks of treatment( food deprived or fed with maintenance rations). We also measured the schooling behavior( cohesion and coordination) of fish from both starvation and control groups at the end of experiment. The main results of this study are as follows: 1) the SMR decreased significantly in both the starvation and control groups,whereas only the SMR of the food deprived group showed repeatability across the experiment; 2) starvation resulted in significant increases in both boldness and exploration; and 3) starvation elicited shorter individual distances among group members,but higher swimming speed and its synchronization. Therefore,the results of the present study suggested that: 1) to maintain their energy balance,starved fish exhibited higher boldness and stronger exploration for more feeding opportunities,but decreased their maintenance metabolism for energy saving; and2) starved fish shoaled with higher cohesion and coordination to improve their survival.
Fishes in natural environments are often affected by food resources as a result of environmental and seasonal changes,and human activities. Feeding is a fundamental physiological function,which provides essential energy for the survival,growth,and reproduction of fishes. We selected juvenile Spinibarbus sinensis( Cyprinidae) to investigate the adaptive responses of energetic metabolism,fish behavior,and shoaling to food shortages and the possible interaction between energetic metabolism and physiology. We first measured the standard metabolic rate( SMR) and fish behavior( including boldness,exploration,and activity) of experimental fish before and after two weeks of treatment( food deprived or fed with maintenance rations). We also measured the schooling behavior( cohesion and coordination) of fish from both starvation and control groups at the end of experiment. The main results of this study are as follows: 1) the SMR decreased significantly in both the starvation and control groups,whereas only the SMR of the food deprived group showed repeatability across the experiment; 2) starvation resulted in significant increases in both boldness and exploration; and 3) starvation elicited shorter individual distances among group members,but higher swimming speed and its synchronization. Therefore,the results of the present study suggested that: 1) to maintain their energy balance,starved fish exhibited higher boldness and stronger exploration for more feeding opportunities,but decreased their maintenance metabolism for energy saving; and2) starved fish shoaled with higher cohesion and coordination to improve their survival.
引文
[1]lvarez Z,Nicieza A G.Is metabolic rate a reliable predictor of growth and survival of brown trout(Salmo trutta)in the wild?Canadian Journal of Fisheries and Aquatic Sciences,2005,62(3):643-649.
[2]Van Leeuwen T E,Rosenfeld J S,Richards J G.Effects of food ration on SMR:influence of food consumption on individual variation in metabolic rate in juvenile coho salmon(Onchorhynchus kisutch).Journal of Animal Ecology,2012,81(2):395-402.
[3]付世建,曹振东,曾令清,夏继刚,李秀明.鱼类游泳运动---策略与适应性进化.北京:科学出版社,2014:127-128.
[4]Krogdahl A,Bakke-McKellep A M.Fasting and refeeding cause rapid changes in intestinal tissue mass and digestive enzyme capacities of Atlantic salmon(Salmo salar L.).Comparative Biochemistry and Physiology Part A:Molecular&Integrative Physiology,2005,141(4):450-460.
[5]Navarro I,Gutiérrez J.Fasting and starvation.Biochemistry and Molecular Biology of Fishes,1995,4(1):393-434.
[6]Reid D,Armstrong J D,Metcalfe N B.Estimated standard metabolic rate interacts with territory quality and density to determine the growth rates of juvenile Atlantic salmon.Functional Ecology,2011,25(6):1360-1367.
[7]Killen S S.Growth trajectory influences temperature preference in fish through an effect on metabolic rate.Journal of Animal Ecology,2014,83(6):1513-1522.
[8]Beck F,Gropp J.Estimation of the starvation losses of nitrogen and energy in the rainbow trout(Oncorhynchus mykiss)with special regard to protein and energy maintenance requirements.Journal of Applied Ichthyology,1995,11(3-4):263-275.
[9]Auer S K,Salin K,Rudolf A M,Anderson G J,Metcalfe N B.Flexibility in metabolic rate confers a growth advantage under changing food availability.Journal of Animal Ecology,2015,84(5):1405-1411.
[10]Ronning B,Moe B,Bech C.Long-term repeatability makes basal metabolic rate a likely heritable trait in the zebra finch Taeniopygia guttata.Journal of Experimental Biology,2005,208(24):4663-4669.
[11]Burton T,Killen S S,Armstrong J D,Metcalfe N B.What causes intraspecific variation in resting metabolic rate and what are its ecological consequences?Proceeding of the Royal Society B:Biological Sciences,2011,278(1724):3465-3473.
[12]Metcalfe N B,Van Leeuwen T E,Killen S S.Does individual variation in metabolic phenotype predict fish behaviour and performance?Journal of Fish Biology,2016,88(1):298-321.
[13]Steyermark A C,Miamen A G,Feghahati H S,Lewno A W.Physiological and morphological correlates of among-individual variation in standard metabolic rate in the leopard frog Rana pipiens.Journal of Experimental Biology,2005,208(6):1201-1208.
[14]刘欢,李秀明,付世建,曾令清.锦鲫幼鱼标准代谢率与生长性能的关联.水生生物学报,2016,40(4):836-842.
[15]李想,林小涛,宋波澜,李丹,陈国柱.流速对红鳍银鲫幼鱼游泳状态的影响.动物学杂志,2010,45(2):126-133.
[16]Fry F E J.The effect of environmental factors on the physiology of fish.Fish Physiology.In:Hoar WS,Randall DJ,editors.Fish Physiology Volume6.New York:Academic Press.pp.1971,1-98.
[17]Biro P A,Stamps J A.Do consistent individual differences in metabolic rate promote consistent individual differences in behavior?Trends in Ecology&Evolution,2010,25(11):653-659.
[18]曾令清,付成,奚露,彭姜岚,付世建.鳊幼鱼能量代谢和个性行为的个体变异及表型关联.生态学报,2017,37(14):4807-4816.
[19]Ward A J W.Social facilitation of exploration in mosquitofish(Gambusia holbrooki).Behavioral Ecology and Sociobiology,2012,66(2):223-230.
[20]Crusio W E.Genetic dissection of mouse exploratory behaviour.Behavioural Brain Research,2001,125(1/2):127-132.
[21]Pitcher T J,Green D A,Magurran A E.Dicing with death:predator inspection behaviour in minnow shoals.Journal of Fish Biology,1986,28(4):439-448.
[22]曾令清,付世建,曹振东.鲫幼鱼(Carassius auratus)标准代谢个体差异与力竭后代谢特征及行为的关联.生态学报,2016,36(6):1746-1755.
[23]Godin J G J,Clark K A V.Risk-taking in stickleback fishes faced with different predatory threats.Ecoscience,1997,4(2):246-251.
[24]付成,曹振东,付世建.温度和饥饿对鲤鱼幼鱼静止代谢率及自发运动的影响.动物学杂志,2012,47(2):85-90.
[25]Mac Phail R C,Hunter D L,Iron T D,Padilla S.Locomotion and behavioral toxicity in larval zebrafish:background,methods,and data//Mc Grath P.Zebrafish:Methods for Assessing Drug Safety and Toxicity.New York:John Wiley&Sons,Inc.,2011:151-164.
[26]Ward A J W,Herbert-Read J E,Simpson S J.Diets and decisions:the potential use of food protein cues in dietary,sexual and social decisions by mosquitofish.Animal Behaviour,2011,82(4):783-790.
[27]Brown C,Jones F,Braithwaite V.In situ examination of boldness-shyness traits in the tropical poeciliid,Brachyraphis episcopi.Animal Behaviour,2005,70(5):1003-1009.
[28]Killen S S,Marras S,Mc Kenzie D J.Fuel,fasting,fear:routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European sea bass.Journal of Animal Ecology,2011,80(5):1024-1033.
[29]Liu S,Fu S J.Effects of food availability on metabolism,behaviour,growth and their relationships in a triploid carp.Journal of Experimental Biology,2017,220(Pt 24):4711-4719.
[30]Delcourt J,Poncin P.Shoals and schools:back to the heuristic definitions and quantitative references.Reviews in Fish Biology and Fisheries,2012,22(3):595-619.
[31]Miller N,Garnier S,Hartnett A T,Couzin I D.Both information and social cohesion determine collective decisions in animal groups.Proceedings of the National Academy of Sciences of the United States of America,2013,110(13):5263-5268.
[32]Hemelrijk C K,Reid D A P,Hildenbrandt H,Padding J T.The increased efficiency of fish swimming in a school.Fish and Fisheries,2015,16(3):511-521.
[33]Cote J,Fogarty S,Sih A.Individual sociability and choosiness between shoal types.Animal Behaviour,2012,83(6):1469-1476.
[34]Goldenberg S U,Borcherding J,Heynen M.Balancing the response to predation-the effects of shoal size,predation risk and habituation on behaviour of juvenile perch.Behavioral Ecology and Sociobiology,2014,68(6):989-998.
[35]Krause J,Ruxton G D.Living in Groups.Cambridge:Cambridge University Press,2002:87-87.
[36]Fu S J.Effects of group size on schooling behavior in two cyprinid fish species.Aquatic Biology,2016,25:165-172.
[37]Zeng L Q,Zhang A J,Killen S S,Cao Z D,Wang Y X,Fu S J.Standard metabolic rate predicts growth trajectory of juvenile Chinese crucian carp(Carassius auratus)under changing food availability.Biology Open,2017,6(9):1305-1309.
[38]吴慧,唐中华,黄清,况璐,付世建.群体成员大小差异对不同生境鲤科鱼类集群行为的影响.水生生物学报,2017,41(3):552-559.
[39]Mehner T,Wieser W.Energetics and metabolic correlates of starvation in juvenile perch(Perca fluviatilis).Journal of Fish Biology,1994,45(2):325-333.
[40]Fu S J,Xie X J,Cao Z D.Effect of fasting and repeat feeding on metabolic rate in southern catfish,Silurus meridionalis Chen.Marine and Freshwater Behaviour and Physiology,2005,38(3):191-198.
[41]Auer S K,Salin K,Rudolf A M,Anderson G J,Metcalfe N B.Differential effects of food availability on minimum and maximum rates of metabolism.Biology Letters,2016,12(10):20160586.
[42]Garland T Jr,Else P L,Hulbert A J,Tao P.Effects of endurance training and captivity on activity metabolism of lizards.American Journal of Physiology,1987,252(3):R450-R456.
[43]付世建,曹振东,彭姜岚.力竭运动锻炼和饥饿对南方鲇静止代谢率及体重的影响.动物学杂志,2007,42(6):103-107.
[44]Wilson D S.Adaptive individual differences within single populations.Philosophical Transactions of the Royal Society B:Biological Sciences,1998,353(1366):199-205.
[45]Pettersson L B,Br9nmark C.Trading off safety against food:state dependent habitat choice and foraging in crucian carp.Oecologia,1993,95(3):353-357.
[46]Sogard S M,Olla B L.The influence of hunger and predation risk on group cohesion in a pelagic fish,walleye pollock Theragra chalcogramma.Environmental Biology of Fishes,1997,50(4):405-413.
[47]Thünken T,Hesse S,Bakker T C M,Baldauf S A.Benefits of kin shoaling in a cichlid fish:familiar and related juveniles show better growth.Behavioral Ecology,2016,27(2):419-425.
[48]聂广峰.梭鱼早期发育以及间歇性饥饿对其幼鱼消化道组织学及行为的影响[D].上海:上海海洋大学,2015:46-47.
[49]Gwak W S,Seikai T,Tanaka M.Evaluation of starvation status of laboratory reared Japanese flounder paralichthys olivaceus larvae and juveniles based on morphological and histological characteristics.Fisheries Science,1999,65(3):339-346.
[50]Ariyomo T O,Watt P J.Effect of hunger level and time of day on boldness and aggression in the zebrafish Danio rerio.Journal of Fish Biology,2015,86(6):1852-1859.
[51]Bumann D,Krause J,Rubenstein D.Mortality risk of spatial positions in animal groups:the danger of being in the front.Behaviour,1997,134(13/14):1063-1076.
[52]Hansen M J,Schaerf T M,Ward A J W.The influence of nutritional state on individual and group movement behaviour in shoals of crimson-spotted rainbowfish(Melanotaenia duboulayi).Behavioral Ecology and Sociobiology,2015,69(10):1713-1722.
[53]Herbert-Read J E,Krause S,Morrell L J,Schaerf T M,Krause J,Ward A J W.The role of individuality in collective group movement.Proceeding of the Royal Society B:Biological Sciences,2013,280(1752):20122564.
[54]Robinson C J,Pitcher T J.Hunger motivation as a promoter of different behaviours within a shoal of herring:selection for homogeneity in fish shoal?Journal of Fish Biology,1989,35(3):459-460.
[2]Van Leeuwen T E,Rosenfeld J S,Richards J G.Effects of food ration on SMR:influence of food consumption on individual variation in metabolic rate in juvenile coho salmon(Onchorhynchus kisutch).Journal of Animal Ecology,2012,81(2):395-402.
[3]付世建,曹振东,曾令清,夏继刚,李秀明.鱼类游泳运动---策略与适应性进化.北京:科学出版社,2014:127-128.
[4]Krogdahl A,Bakke-McKellep A M.Fasting and refeeding cause rapid changes in intestinal tissue mass and digestive enzyme capacities of Atlantic salmon(Salmo salar L.).Comparative Biochemistry and Physiology Part A:Molecular&Integrative Physiology,2005,141(4):450-460.
[5]Navarro I,Gutiérrez J.Fasting and starvation.Biochemistry and Molecular Biology of Fishes,1995,4(1):393-434.
[6]Reid D,Armstrong J D,Metcalfe N B.Estimated standard metabolic rate interacts with territory quality and density to determine the growth rates of juvenile Atlantic salmon.Functional Ecology,2011,25(6):1360-1367.
[7]Killen S S.Growth trajectory influences temperature preference in fish through an effect on metabolic rate.Journal of Animal Ecology,2014,83(6):1513-1522.
[8]Beck F,Gropp J.Estimation of the starvation losses of nitrogen and energy in the rainbow trout(Oncorhynchus mykiss)with special regard to protein and energy maintenance requirements.Journal of Applied Ichthyology,1995,11(3-4):263-275.
[9]Auer S K,Salin K,Rudolf A M,Anderson G J,Metcalfe N B.Flexibility in metabolic rate confers a growth advantage under changing food availability.Journal of Animal Ecology,2015,84(5):1405-1411.
[10]Ronning B,Moe B,Bech C.Long-term repeatability makes basal metabolic rate a likely heritable trait in the zebra finch Taeniopygia guttata.Journal of Experimental Biology,2005,208(24):4663-4669.
[11]Burton T,Killen S S,Armstrong J D,Metcalfe N B.What causes intraspecific variation in resting metabolic rate and what are its ecological consequences?Proceeding of the Royal Society B:Biological Sciences,2011,278(1724):3465-3473.
[12]Metcalfe N B,Van Leeuwen T E,Killen S S.Does individual variation in metabolic phenotype predict fish behaviour and performance?Journal of Fish Biology,2016,88(1):298-321.
[13]Steyermark A C,Miamen A G,Feghahati H S,Lewno A W.Physiological and morphological correlates of among-individual variation in standard metabolic rate in the leopard frog Rana pipiens.Journal of Experimental Biology,2005,208(6):1201-1208.
[14]刘欢,李秀明,付世建,曾令清.锦鲫幼鱼标准代谢率与生长性能的关联.水生生物学报,2016,40(4):836-842.
[15]李想,林小涛,宋波澜,李丹,陈国柱.流速对红鳍银鲫幼鱼游泳状态的影响.动物学杂志,2010,45(2):126-133.
[16]Fry F E J.The effect of environmental factors on the physiology of fish.Fish Physiology.In:Hoar WS,Randall DJ,editors.Fish Physiology Volume6.New York:Academic Press.pp.1971,1-98.
[17]Biro P A,Stamps J A.Do consistent individual differences in metabolic rate promote consistent individual differences in behavior?Trends in Ecology&Evolution,2010,25(11):653-659.
[18]曾令清,付成,奚露,彭姜岚,付世建.鳊幼鱼能量代谢和个性行为的个体变异及表型关联.生态学报,2017,37(14):4807-4816.
[19]Ward A J W.Social facilitation of exploration in mosquitofish(Gambusia holbrooki).Behavioral Ecology and Sociobiology,2012,66(2):223-230.
[20]Crusio W E.Genetic dissection of mouse exploratory behaviour.Behavioural Brain Research,2001,125(1/2):127-132.
[21]Pitcher T J,Green D A,Magurran A E.Dicing with death:predator inspection behaviour in minnow shoals.Journal of Fish Biology,1986,28(4):439-448.
[22]曾令清,付世建,曹振东.鲫幼鱼(Carassius auratus)标准代谢个体差异与力竭后代谢特征及行为的关联.生态学报,2016,36(6):1746-1755.
[23]Godin J G J,Clark K A V.Risk-taking in stickleback fishes faced with different predatory threats.Ecoscience,1997,4(2):246-251.
[24]付成,曹振东,付世建.温度和饥饿对鲤鱼幼鱼静止代谢率及自发运动的影响.动物学杂志,2012,47(2):85-90.
[25]Mac Phail R C,Hunter D L,Iron T D,Padilla S.Locomotion and behavioral toxicity in larval zebrafish:background,methods,and data//Mc Grath P.Zebrafish:Methods for Assessing Drug Safety and Toxicity.New York:John Wiley&Sons,Inc.,2011:151-164.
[26]Ward A J W,Herbert-Read J E,Simpson S J.Diets and decisions:the potential use of food protein cues in dietary,sexual and social decisions by mosquitofish.Animal Behaviour,2011,82(4):783-790.
[27]Brown C,Jones F,Braithwaite V.In situ examination of boldness-shyness traits in the tropical poeciliid,Brachyraphis episcopi.Animal Behaviour,2005,70(5):1003-1009.
[28]Killen S S,Marras S,Mc Kenzie D J.Fuel,fasting,fear:routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European sea bass.Journal of Animal Ecology,2011,80(5):1024-1033.
[29]Liu S,Fu S J.Effects of food availability on metabolism,behaviour,growth and their relationships in a triploid carp.Journal of Experimental Biology,2017,220(Pt 24):4711-4719.
[30]Delcourt J,Poncin P.Shoals and schools:back to the heuristic definitions and quantitative references.Reviews in Fish Biology and Fisheries,2012,22(3):595-619.
[31]Miller N,Garnier S,Hartnett A T,Couzin I D.Both information and social cohesion determine collective decisions in animal groups.Proceedings of the National Academy of Sciences of the United States of America,2013,110(13):5263-5268.
[32]Hemelrijk C K,Reid D A P,Hildenbrandt H,Padding J T.The increased efficiency of fish swimming in a school.Fish and Fisheries,2015,16(3):511-521.
[33]Cote J,Fogarty S,Sih A.Individual sociability and choosiness between shoal types.Animal Behaviour,2012,83(6):1469-1476.
[34]Goldenberg S U,Borcherding J,Heynen M.Balancing the response to predation-the effects of shoal size,predation risk and habituation on behaviour of juvenile perch.Behavioral Ecology and Sociobiology,2014,68(6):989-998.
[35]Krause J,Ruxton G D.Living in Groups.Cambridge:Cambridge University Press,2002:87-87.
[36]Fu S J.Effects of group size on schooling behavior in two cyprinid fish species.Aquatic Biology,2016,25:165-172.
[37]Zeng L Q,Zhang A J,Killen S S,Cao Z D,Wang Y X,Fu S J.Standard metabolic rate predicts growth trajectory of juvenile Chinese crucian carp(Carassius auratus)under changing food availability.Biology Open,2017,6(9):1305-1309.
[38]吴慧,唐中华,黄清,况璐,付世建.群体成员大小差异对不同生境鲤科鱼类集群行为的影响.水生生物学报,2017,41(3):552-559.
[39]Mehner T,Wieser W.Energetics and metabolic correlates of starvation in juvenile perch(Perca fluviatilis).Journal of Fish Biology,1994,45(2):325-333.
[40]Fu S J,Xie X J,Cao Z D.Effect of fasting and repeat feeding on metabolic rate in southern catfish,Silurus meridionalis Chen.Marine and Freshwater Behaviour and Physiology,2005,38(3):191-198.
[41]Auer S K,Salin K,Rudolf A M,Anderson G J,Metcalfe N B.Differential effects of food availability on minimum and maximum rates of metabolism.Biology Letters,2016,12(10):20160586.
[42]Garland T Jr,Else P L,Hulbert A J,Tao P.Effects of endurance training and captivity on activity metabolism of lizards.American Journal of Physiology,1987,252(3):R450-R456.
[43]付世建,曹振东,彭姜岚.力竭运动锻炼和饥饿对南方鲇静止代谢率及体重的影响.动物学杂志,2007,42(6):103-107.
[44]Wilson D S.Adaptive individual differences within single populations.Philosophical Transactions of the Royal Society B:Biological Sciences,1998,353(1366):199-205.
[45]Pettersson L B,Br9nmark C.Trading off safety against food:state dependent habitat choice and foraging in crucian carp.Oecologia,1993,95(3):353-357.
[46]Sogard S M,Olla B L.The influence of hunger and predation risk on group cohesion in a pelagic fish,walleye pollock Theragra chalcogramma.Environmental Biology of Fishes,1997,50(4):405-413.
[47]Thünken T,Hesse S,Bakker T C M,Baldauf S A.Benefits of kin shoaling in a cichlid fish:familiar and related juveniles show better growth.Behavioral Ecology,2016,27(2):419-425.
[48]聂广峰.梭鱼早期发育以及间歇性饥饿对其幼鱼消化道组织学及行为的影响[D].上海:上海海洋大学,2015:46-47.
[49]Gwak W S,Seikai T,Tanaka M.Evaluation of starvation status of laboratory reared Japanese flounder paralichthys olivaceus larvae and juveniles based on morphological and histological characteristics.Fisheries Science,1999,65(3):339-346.
[50]Ariyomo T O,Watt P J.Effect of hunger level and time of day on boldness and aggression in the zebrafish Danio rerio.Journal of Fish Biology,2015,86(6):1852-1859.
[51]Bumann D,Krause J,Rubenstein D.Mortality risk of spatial positions in animal groups:the danger of being in the front.Behaviour,1997,134(13/14):1063-1076.
[52]Hansen M J,Schaerf T M,Ward A J W.The influence of nutritional state on individual and group movement behaviour in shoals of crimson-spotted rainbowfish(Melanotaenia duboulayi).Behavioral Ecology and Sociobiology,2015,69(10):1713-1722.
[53]Herbert-Read J E,Krause S,Morrell L J,Schaerf T M,Krause J,Ward A J W.The role of individuality in collective group movement.Proceeding of the Royal Society B:Biological Sciences,2013,280(1752):20122564.
[54]Robinson C J,Pitcher T J.Hunger motivation as a promoter of different behaviours within a shoal of herring:selection for homogeneity in fish shoal?Journal of Fish Biology,1989,35(3):459-460.