单独隔离孵化对镇海林蛙蝌蚪生长发育、社交行为和运动表现的影响
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摘要
两栖类胚胎呈卵群一起孵化在反捕食、维持胚胎间的温度平衡和促进胚胎的同步发育等方面具有重要作用。在实验条件下探究孵化条件(单独隔离孵化和卵群一起孵化)对镇海林蛙(Rana zhenhaiensis)蝌蚪的生长发育、社交行为及其运动表现能力的影响。结果表明,孵出2天后,单独隔离孵化组蝌蚪的体长和发育历期均显著大于卵群一起孵化组。以体长为协变量的协方差分析表明,特定体长的单独隔离孵化组蝌蚪的体宽和体重均显著大于卵群一起孵化组的个体。在蝌蚪的活动行为中,单独隔离孵化组蝌蚪在水体上层和中层出现的频次显著小于卵群一起孵化组,而在水体底层的出现频次显著大于卵群一起孵化组。单独隔离孵化组蝌蚪个体的分布面积率、最近邻个体的距离、个体间的距离均显著大于卵群一起孵化组,但个体间的接触频次显著小于卵群一起孵化组。在运动表现方面,单独隔离孵化组胚胎的摆尾搏动频次显著小于卵群一起孵化组。单独隔离孵化组蝌蚪的运动时长和运动频次均显著小于卵群一起孵化组。本研究结果将为无尾两栖类幼期的生长发育规律提供参考数据。
Embryo-clustering incubation plays an important role in anti-predation, maintaining temperature balance between embryos, and promoting hatching synchrony for anurans. In this study, we investigated the effects of two hatching conditions(isolated-incubation and clustered-incubation) on the growth, development, social behavior, and locomotor performance of Rana zhenhaiensis tadpoles under laboratory conditions. Our results showed that both body length and the Gosner development stage of two-day-old hatchlings in a single-embryo treatment were significantly larger than those of the group-embryo treatment. The results of the ANCOVA(with body length as the covariate) analysis showed that both body width and body mass in the group-embryo treatment were significantly lower than those of the single-embryo treatment. For tadpole activity behavior, the occurrence frequency in the upper and middle water layers in the single-embryo treatments were significantly lower than those of the group-embryo treatment, whereas it was significantly greater in the single-embryo treatments than that of the group-embryo treatment in the lower water layers. The proportion of area occupied by tadpoles, the nearest neighbor distance, and the distance among individuals in the single-embryo treatment were both significantly greater than those of the group-embryo treatment, but the contact frequency between pairwise tadpoles was significantly lower than those of the group-embryo treatment. Regarding locomotor performance, we found that activity duration and activity frequency in the single-embryo treatment were significantly lower than those of the group-embryo treatment. These findings should provide valuable reference data on the growth and development of Rana zhenhaiensis, as well as other anuran species.
Embryo-clustering incubation plays an important role in anti-predation, maintaining temperature balance between embryos, and promoting hatching synchrony for anurans. In this study, we investigated the effects of two hatching conditions(isolated-incubation and clustered-incubation) on the growth, development, social behavior, and locomotor performance of Rana zhenhaiensis tadpoles under laboratory conditions. Our results showed that both body length and the Gosner development stage of two-day-old hatchlings in a single-embryo treatment were significantly larger than those of the group-embryo treatment. The results of the ANCOVA(with body length as the covariate) analysis showed that both body width and body mass in the group-embryo treatment were significantly lower than those of the single-embryo treatment. For tadpole activity behavior, the occurrence frequency in the upper and middle water layers in the single-embryo treatments were significantly lower than those of the group-embryo treatment, whereas it was significantly greater in the single-embryo treatments than that of the group-embryo treatment in the lower water layers. The proportion of area occupied by tadpoles, the nearest neighbor distance, and the distance among individuals in the single-embryo treatment were both significantly greater than those of the group-embryo treatment, but the contact frequency between pairwise tadpoles was significantly lower than those of the group-embryo treatment. Regarding locomotor performance, we found that activity duration and activity frequency in the single-embryo treatment were significantly lower than those of the group-embryo treatment. These findings should provide valuable reference data on the growth and development of Rana zhenhaiensis, as well as other anuran species.
引文
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[26] Nicieza A G. Context-dependent aggregation in Common Frog Rana temporaria tadpoles: influence of developmental stage, predation risk and social environment. Functional Ecology, 1999, 13(6): 852- 858.
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[28] Rautio S A, Bura E A, Berven K A, Gamboa G J. Kin recognition in wood frog tadpoles (Rana sylvatica): factors affecting spatial proximity to siblings. Canadian Journal of Zoology, 1991, 69(10): 2569- 2571.
[29] Koike F, Clout M N, Kawamichi M, De Poorter M, Iwatsuki K. Assessment and Control of Biological Invasion Risks. Switzerland: IUCN Publications Services, 2006.
[30] Fan X L, Lin Z H. Vulnerability and behavioral responses of South Chinese anuran tadpoles to native dragonfly (Pantala flavescens) naiads and introduced western mosquitofish (Gambusia affinis). Journal of Freshwater Ecology, 2017, 32(1): 529- 539.
[31] Gosner K L. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 1960, 16(3): 183- 190.
[32] 朱卫东, 任夙艺, 申屠琰, 邹李昶, 王志铮. 水温对棘胸蛙(Paa spinosa)蝌蚪行为及尾部皮肤和肝脏相关功能酶活力的影响. 海洋与湖沼, 2016, 47(1): 245- 252.
[33] Raven C, Shine R, Greenlees M, Schaerf T M, Ward A J W. The role of biotic and abiotic cues in stimulating aggregation by larval cane toads (Rhinella marina). Ethology, 2017, 123(10): 724- 735.
[34] Reques R, Tejedo M. Reaction norms for metamorphic traits in natterjack toads to larval density and pond duration. Journal of Evolutionary Biology, 1997, 10(6): 829- 851.
[35] Laurila A, Kujasalo J. Habitat duration, predation risk and phenotypic plasticity in common frog (Rana temporaria) tadpoles. Journal of Animal Ecology, 1999, 68(6): 1123- 1132.
[36] Kulkarni S S, Gomez-Mestre I, Moskalik C L, Storz B L, Buchholz D R. Evolutionary reduction of developmental plasticity in desert spadefoot toads. Journal of Evolutionary Biology, 2011, 24(11): 2445- 2455.
[37] Mueller P, Diamond J. Metabolic rate and environmental productivity: well-provisioned animals evolved to run and idle fast. Proceedings of the National Academy of Sciences of the United States of America, 2001, 98(22): 12550- 12554.
[38] Bonte D, Van Dyck H, Bullock J M, Coulon A, Delgado M, Gibbs M, Lehouck V, Matthysen E, Mustin K, Saastamoinen M, Schtickzelle N, Stevens V M, Vandewoestijne S, Baguette M, Barton K, Benton T G, Chaput-Bardy A, Clobert J, Dytham C, Hovestadt T, Meier C M, Palmer S C F, Turlure C, Travis J M J. Costs of dispersal. Biological Reviews, 2012, 87(2): 290- 312.
[39] Thompson M B. Nest temperatures in the pleurodiran turtle, Emydura macquarii. Copeia, 1988, 1988(4): 996- 1000.
[40] Spieler M, Linsenmair K E. Aggregation behaviour of Bufo maculatus tadpoles as an antipredator mechanism. Ethology, 1999, 105(8): 665- 686.
[41] Spieler M. Risk of predation affects aggregation size: a study with tadpoles of Phrynomantis microps (Anura: Microhylidae). Animal Behaviour, 2003, 65(1): 179- 184.
[42] Davies N B, Krebs J R, West S A. An Introduction to Behavioural Ecology. Cambridge: Wiley-Blackwell, 2012.
[43] Pfennig D W. “Kin recognition” among spadefoot toad tadpoles: a side-effect of habitat selection? Evolution, 1990, 44(4): 785- 798.
[44] Griffiths R A, Denton J. Interspecific associations in tadpoles. Animal Behaviour, 1992, 44(6): 1153- 1157.
[45] Tejedo M. Size-dependent vulnerability and behavioral responses of tadpoles of two anuran species to beetle larvae predators. Herpetologica, 1993, 49(3): 287- 294.
[46] Hokit D G, Blaustein A R. Predator avoidance and alarm-response behaviour in kin-discriminating tadpoles (Rana cascadae). Ethology, 1995, 101(4): 280- 290.
[47] Bridges C M. Tadpoles balance foraging and predator avoidance: effects of predation, pond drying, and hunger. Journal of Herpetology, 2002, 36(4): 627- 634.
[48] Mathis A, Murray K L, Hickman C R. Do experience and body size play a role in responses of larval ringed salamanders, Ambystoma annulatum, to predator kairomones? Laboratory and field assays. Ethology, 2003, 109(2): 159- 170.
[49] Persons M H. Hunger effects on foraging responses to perceptual cues in immature and adult wolf spiders (Lycosidae). Animal Behaviour, 1999, 57(1): 81- 88.
[2] Courtney S P. The evolution of egg clustering by butterflies and other insects. The American Naturalist, 1984, 123(2): 276- 281.
[3] Buskirk R E. Sociality in the arachnida//Herman H R, ed. Social Insects. New York: Academic Press, 1981: 281- 367.
[4] Boletzky S V. Cephalopod eggs and egg masses. Oceanography and Marine Biology, 1998, 36: 341- 371.
[5] Ishimatsu A, Graham J B. Roles of environmental cues for embryonic incubation and hatching in mudskippers. Integrative and Comparative Biology, 2011, 51(1): 38- 48.
[6] Duellman W E, Trueb L. Biology of Amphibians. Baltimore: Johns Hopkins University Press, 1986.
[7] Radder R S, Shine R. Why do female lizards lay their eggs in communal nests? Journal of Animal Ecology, 2007, 76(5): 881- 887.
[8] McGlashan J K, Loudon F K, Thompson M B, Spencer R J. Hatching behavior of eastern long-necked turtles (Chelodina longicollis): the influence of asynchronous environments on embryonic heart rate and phenotype. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2015, 188: 58- 64.
[9] Aubret F, Bignon F, Kok P J R, Blanvillain G. Only child syndrome in snakes: eggs incubated alone produce asocial individuals. Scientific Reports, 2016, 6: 35752.
[10] Waldman B. Adaptive significance of communal oviposition in wood frogs (Rana sylvatica). Behavioral Ecology and Sociobiology, 1982, 10(3): 169- 174.
[11] Ewert M A, Nelson C E. Metabolic heating of embryos and sex determination in the American alligator, Alligator mississippiensis. Journal of Thermal Biology, 2003, 28(2): 159- 165.
[12] Zbinden J A, Margaritoulis D, Arlettaz R. Metabolic heating in Mediterranean loggerhead sea turtle clutches. Journal of Experimental Marine Biology and Ecology, 2006, 334(1): 151- 157.
[13] Aubret F, Blanvillain G, Kok P J R. Myth busting? Effects of embryo positioning and egg turning on hatching success in the water snake Natrix maura. Scientific Reports, 2015, 5: 13385.
[14] Doody J S, Freedberg S, Keogh J S. Communal egg-laying in reptiles and amphibians: evolutionary patterns and hypotheses. The Quarterly Review of Biology, 2009, 84(3): 229- 252.
[15] Doody J S. Environmentally cued hatching in reptiles. Integrative and Comparative Biology, 2011, 51(1): 49- 61.
[16] Aubret F, Blanvillain G, Bignon F, Kok P J R. Heartbeat, embryo communication and hatching synchrony in snake eggs. Scientific Reports, 2016, 6: 23519.
[17] Spencer R J, Thompson M B, Banks P B. Hatch or wait? A dilemma in reptilian incubation. Oikos, 2001, 93(3): 401- 406.
[18] McGlashan J K, Spencer R J, Old J M. Embryonic communication in the nest: metabolic responses of reptilian embryos to developmental rates of siblings. Proceedings of the Royal Society B: Biological Sciences, 2012, 279(1734): 1709- 1715.
[19] Webster B, Hayes W, Pike T W. Avian egg odour encodes information on embryo sex, fertility and development. PLoS One, 2015, 10(1): e0116345.
[20] Aubret F. Heart rates increase after hatching in two species of natricine snakes. Scientific Reports, 2013, 3: 3384.
[21] Delm M M. Vigilance for predators: detection and dilution effects. Behavioral Ecology and Sociobiology, 1990, 26(5): 337- 342.
[22] O′Donoghue M, Boutin S. Does reproductive synchrony affect juvenile survival rates of northern mammals? Oikos, 1995, 74(1): 115- 121.
[23] Sih A. Predators and prey lifestyles: an evolutionary and ecological overview//Kerfoot WC, Sih A, eds. Predation: Direct and Indirect Impacts on Aquatic Communities. Hanover: University of New England Press, 1987: 203- 224.
[24] Lima S L, Dill L M. Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology, 1990, 68(4): 619- 640.
[25] Gamboa G J, Berven K A, Schemidt R A, Fishwild T G, Jankens K M. Kin recognition by larval wood frogs (Rana sylvatica): effects of diet and prior exposure to conspecifics. Oecologia, 1991, 86(3): 319- 324.
[26] Nicieza A G. Context-dependent aggregation in Common Frog Rana temporaria tadpoles: influence of developmental stage, predation risk and social environment. Functional Ecology, 1999, 13(6): 852- 858.
[27] Blaustein A R, O′Hara R K. Aggregation behaviour in Rana cascadae tadpoles: association preferences among wild aggregations and responses to non-kin. Animal Behaviour, 1987, 35(5): 1549- 1555.
[28] Rautio S A, Bura E A, Berven K A, Gamboa G J. Kin recognition in wood frog tadpoles (Rana sylvatica): factors affecting spatial proximity to siblings. Canadian Journal of Zoology, 1991, 69(10): 2569- 2571.
[29] Koike F, Clout M N, Kawamichi M, De Poorter M, Iwatsuki K. Assessment and Control of Biological Invasion Risks. Switzerland: IUCN Publications Services, 2006.
[30] Fan X L, Lin Z H. Vulnerability and behavioral responses of South Chinese anuran tadpoles to native dragonfly (Pantala flavescens) naiads and introduced western mosquitofish (Gambusia affinis). Journal of Freshwater Ecology, 2017, 32(1): 529- 539.
[31] Gosner K L. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 1960, 16(3): 183- 190.
[32] 朱卫东, 任夙艺, 申屠琰, 邹李昶, 王志铮. 水温对棘胸蛙(Paa spinosa)蝌蚪行为及尾部皮肤和肝脏相关功能酶活力的影响. 海洋与湖沼, 2016, 47(1): 245- 252.
[33] Raven C, Shine R, Greenlees M, Schaerf T M, Ward A J W. The role of biotic and abiotic cues in stimulating aggregation by larval cane toads (Rhinella marina). Ethology, 2017, 123(10): 724- 735.
[34] Reques R, Tejedo M. Reaction norms for metamorphic traits in natterjack toads to larval density and pond duration. Journal of Evolutionary Biology, 1997, 10(6): 829- 851.
[35] Laurila A, Kujasalo J. Habitat duration, predation risk and phenotypic plasticity in common frog (Rana temporaria) tadpoles. Journal of Animal Ecology, 1999, 68(6): 1123- 1132.
[36] Kulkarni S S, Gomez-Mestre I, Moskalik C L, Storz B L, Buchholz D R. Evolutionary reduction of developmental plasticity in desert spadefoot toads. Journal of Evolutionary Biology, 2011, 24(11): 2445- 2455.
[37] Mueller P, Diamond J. Metabolic rate and environmental productivity: well-provisioned animals evolved to run and idle fast. Proceedings of the National Academy of Sciences of the United States of America, 2001, 98(22): 12550- 12554.
[38] Bonte D, Van Dyck H, Bullock J M, Coulon A, Delgado M, Gibbs M, Lehouck V, Matthysen E, Mustin K, Saastamoinen M, Schtickzelle N, Stevens V M, Vandewoestijne S, Baguette M, Barton K, Benton T G, Chaput-Bardy A, Clobert J, Dytham C, Hovestadt T, Meier C M, Palmer S C F, Turlure C, Travis J M J. Costs of dispersal. Biological Reviews, 2012, 87(2): 290- 312.
[39] Thompson M B. Nest temperatures in the pleurodiran turtle, Emydura macquarii. Copeia, 1988, 1988(4): 996- 1000.
[40] Spieler M, Linsenmair K E. Aggregation behaviour of Bufo maculatus tadpoles as an antipredator mechanism. Ethology, 1999, 105(8): 665- 686.
[41] Spieler M. Risk of predation affects aggregation size: a study with tadpoles of Phrynomantis microps (Anura: Microhylidae). Animal Behaviour, 2003, 65(1): 179- 184.
[42] Davies N B, Krebs J R, West S A. An Introduction to Behavioural Ecology. Cambridge: Wiley-Blackwell, 2012.
[43] Pfennig D W. “Kin recognition” among spadefoot toad tadpoles: a side-effect of habitat selection? Evolution, 1990, 44(4): 785- 798.
[44] Griffiths R A, Denton J. Interspecific associations in tadpoles. Animal Behaviour, 1992, 44(6): 1153- 1157.
[45] Tejedo M. Size-dependent vulnerability and behavioral responses of tadpoles of two anuran species to beetle larvae predators. Herpetologica, 1993, 49(3): 287- 294.
[46] Hokit D G, Blaustein A R. Predator avoidance and alarm-response behaviour in kin-discriminating tadpoles (Rana cascadae). Ethology, 1995, 101(4): 280- 290.
[47] Bridges C M. Tadpoles balance foraging and predator avoidance: effects of predation, pond drying, and hunger. Journal of Herpetology, 2002, 36(4): 627- 634.
[48] Mathis A, Murray K L, Hickman C R. Do experience and body size play a role in responses of larval ringed salamanders, Ambystoma annulatum, to predator kairomones? Laboratory and field assays. Ethology, 2003, 109(2): 159- 170.
[49] Persons M H. Hunger effects on foraging responses to perceptual cues in immature and adult wolf spiders (Lycosidae). Animal Behaviour, 1999, 57(1): 81- 88.