不同生境间龟鳖类体型的差异
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摘要
体型是动物重要的形态特征,影响动物的生境利用。为揭示龟鳖类体型与生境之间的关系,通过文献收集331种龟鳖(龟鳖目Tesudines总物种数的98.8%)的最大背甲长及其生境信息,将生境分为海洋、淡水、岛屿性陆地和大陆性陆地4种类型,再将淡水生境分为大静水、大流水、小静水、小流水和所有水域5种亚类型,大陆性陆地生境分为高地、平地和荒漠3种亚类型,从而比较不同生境类型或亚类型之间龟鳖类体型的差异。广义线性混合模型分析结果显示:1)海龟体型最大,岛屿性陆龟次之,淡水龟鳖和大陆性陆龟体型最小,且后两者差异无统计学意义。2)淡水龟鳖类的体型在5种亚类型生境间存在差异,大静水和大流水水域的体型均显著大于小静水和小流水水域,而体型在大静水与大流水水域、小静水与小流水水域之间的差异均无统计学意义,表明淡水龟鳖类体型与水域面积有关,而与水域是静水或流水无关。广布所有水域的淡水龟鳖类体型趋于中间型,且与其他4种亚类型生境中的体型之间的差异均无统计学意义。3)大陆性陆龟的体型从高地到平地再到荒漠有逐渐变大的趋势,但差异无统计学意义。本研究揭示龟鳖类的保护对策需要考虑其体型和生境面积的相关性。
Body size is important to animals because it can affect the habitat use of animals. We collected body size(maximum carapace length) data of 331 turtle species from published literatures which accounted for 98.8% of all 335 turtle species. To understand the evolution of body size, the collected turtle species were divided into 4 habitat types(marine, freshwater, island and mainland), and the freshwater species were further divided into 5 subtypes(large lentic, large lotic, small lentic, small lotic, and all water bodies), and the mainland species were divided into 3 subtypes(highland, lowland and wilderness). The results of generalized linear mixed model showed that sea turtles had the largest body size on average(134.86 cm±70.14 cm), while freshwater turtles(32.60 cm±20.57 cm) and mainland tortoises(27.08 cm±15.77 cm) had the smallest. Island tortoises were intermediate in body size(80.05 cm±37.11 cm). There were no significant differences of body size between the freshwater turtles and mainland tortoises. Moreover, body size was positively correlated with the total area of water bodies in habitat subtypes for freshwater turtles, because the body size of turtles from large lentic(50.30 cm±27.03 cm) and large lotic water bodies(39.86 cm±20.34 cm) were larger than those from small lentic(23.78 cm±7.47 cm) and small lotic water bodies(23.79 cm±10.57 cm), whereas there were no significant differences in turtle body sizes between the large lotic and lentic water bodies as well as between the small lotic and lentic water bodies. However, the freshwater turtles inhabited in all water bodies were intermediate in body size(41.50 cm±32.65 cm) compared to the 4 habitat subtypes as described above. Although there was a trend towards larger body size from highland(24.86 cm± 10.09 cm) to lowland(26.15 cm±20.12 cm), and from lowland to wilderness(39.11 cm±19.43 cm) in mainland tortoises, there were also no significant differences among these habitat subtypes. This study indicated that conservation strategies for turtles should be considered in relation to their body size and habitat area.
Body size is important to animals because it can affect the habitat use of animals. We collected body size(maximum carapace length) data of 331 turtle species from published literatures which accounted for 98.8% of all 335 turtle species. To understand the evolution of body size, the collected turtle species were divided into 4 habitat types(marine, freshwater, island and mainland), and the freshwater species were further divided into 5 subtypes(large lentic, large lotic, small lentic, small lotic, and all water bodies), and the mainland species were divided into 3 subtypes(highland, lowland and wilderness). The results of generalized linear mixed model showed that sea turtles had the largest body size on average(134.86 cm±70.14 cm), while freshwater turtles(32.60 cm±20.57 cm) and mainland tortoises(27.08 cm±15.77 cm) had the smallest. Island tortoises were intermediate in body size(80.05 cm±37.11 cm). There were no significant differences of body size between the freshwater turtles and mainland tortoises. Moreover, body size was positively correlated with the total area of water bodies in habitat subtypes for freshwater turtles, because the body size of turtles from large lentic(50.30 cm±27.03 cm) and large lotic water bodies(39.86 cm±20.34 cm) were larger than those from small lentic(23.78 cm±7.47 cm) and small lotic water bodies(23.79 cm±10.57 cm), whereas there were no significant differences in turtle body sizes between the large lotic and lentic water bodies as well as between the small lotic and lentic water bodies. However, the freshwater turtles inhabited in all water bodies were intermediate in body size(41.50 cm±32.65 cm) compared to the 4 habitat subtypes as described above. Although there was a trend towards larger body size from highland(24.86 cm± 10.09 cm) to lowland(26.15 cm±20.12 cm), and from lowland to wilderness(39.11 cm±19.43 cm) in mainland tortoises, there were also no significant differences among these habitat subtypes. This study indicated that conservation strategies for turtles should be considered in relation to their body size and habitat area.
引文
王剑, 史海涛. 2011. 黄斑巨鳖分布的历史变迁[J]. 动物分类学报, 36(4): 919-924.
张孟闻, 宗愉, 马积藩. 1998. 中国动物志爬行纲(第Ⅰ卷)[M]. 北京: 科学出版社.
Angielczyk KD, Burroughs RW, Feldman CR. 2015. Do turtles follow the rules? Latitudinal gradients in species richness, body size, and geographic range area of the world's turtles: latitudinal gradients in turtles[J]. Journal of Experimental Zoology, Part B: Molecular and Developmental Evolution, 324(3): 270-294.
Arnold EN. 1979. Indian ocean giant tortoises: their systematics and island adaptations[J]. Philosophical Transactions of the Royal Society B: Biological Sciences, 286(1011): 127-145.
Bambach RK. 1993. Seafood through time: changes in biomass, energetics, and productivity in the marine ecosystem[J]. Paleobiology, 19(3): 372-397.
Benson RBJ, Domokos G, Várkonyi P, et al. 2011. Shell geometry and habitat determination in extinct and extant turtles (Reptilia: Testudinata)[J]. Paleobiology, 37(4): 547-562.
Bernard A, Lécuyer C, Vincent P, et al. 2010. Regulation of body temperature by some Mesozoic marine reptiles[J]. Science, 328(5984): 1379-1382.
Berry JF, Shine R. 1980. Sexual size dimorphism and selection in turtle (Order Testudins)[J]. Oecologia (Berlin), 44(2): 185-191.
Bondi CA, Marks SB. 2013. Differences in flow regime influence the seasonal migrations, body size, and body condition of western pond turtles (Actinemys marmorata) that inhabit perennial and intermittent riverine sites in northern California[J]. Copeia, 2013(1): 142-153.
Bonin F, Devaux B, Dupré A. 2006. Turtles of the world[M]. Baltimore: The Johns Hopkins University Press.
Bonnet X, Delmas V, El-Mouden H, et al. 2010. Is sexual body shape dimorphism consistent in aquatic and terrestrial chelonians?[J]. Zoology, 113(4): 213-220.
Claude J, Paradis E, Tong H, et al. 2003. A geometric morphometric assessment of the effects of environment and cladogenesis on the evolution of the turtle shell[J]. Biological Journal of the Linnean Society, 79(3): 485-501.
Claude J, Prichard P, Tong H, et al. 2004. Ecological correlates and evolutionary divergence in the skull of turtles: a geometric morphometric assessment[J]. Systematic Biology, 53(6): 933-948.
Cohen JE, Pimm SL, Yodzis P, et al. 1993. Body sizes of animal predators and animal prey in food webs[J]. Journal of Animal Ecology, 62(1): 67-78.
Collar DC, Schulte JA, Losos JB. 2011. Evolution of extreme body size disparity in monitor lizards (Varanus)[J]. Evolution, 65(9): 2664-2680.
Ernst CH, Barbour RW. 1989. Turtles of the world[M]. Washington DC: Smithsonian Institution Press.
Ernst CH, Lovich J. 2009. Turtles of the United States and Canada (2nd edition)[M]. Baltimore: The Johns Hopkins University Press.
Farlow JO, Pianka ER. 2002. Body size overlap habitat partitioning and living space requirements of terrestrial vertebrate predators: implications for the paleoecology of large theropod dinosaurs[J]. Historical Biology, 16(1): 21-40.
Fish FE, Nicastro AJ. 2003. Aquatic turning performance by the whirligig beetle: constraints on maneuverability by a rigid biological system[J]. Journal of Experimental Biology, 206(10): 1649-1656.
Gaeta JW, Ahrenstorff TD, Diana JS, et al. 2018. Go big or … don't? A field-based diet evaluation of freshwater piscivore and prey fish size relationships[J]. PLoS ONE, 13(3): e0194092. DOI:10.1371/journal.pone.0194092.
Head JJ, Bloch JI, Hastings AK, et al. 2009. Giant boid snake from the Palaeocene neotropics reveals hotter past equatorial temperatures[J]. Nature, 457(7230): 715-718.
Heim NA, Knope ML, Schaal EK, et al. 2015. Cope's rule in the evolution of marine animals[J]. Science, 347(6224): 867-870.
Ireland LC, Gans C. 1972. The adaptive significance of the flexible shell of the tortoise, Malacochersus tornieri[J]. Animal Behaviour, 20(4): 778-781.
Jaffe AL, Slater GJ, Alfaro ME. 2011. The evolution of island gigantism and body size variation in tortoises and turtles[J]. Biology Letters, 7(4): 558-561.
Joyce WG, Gauthier JA. 2004. Palaeoecology of Triassic stem turtles sheds new light on turtle origins[J]. Proceedings of the Royal Society B: Biological Sciences, 271(1534): 1-5.
Li Y, Xu F, Guo Z, et al. 2011. Reduced predator species richness drives the body gigantism of a frog species on the Zhoushan Archipelago in China[J]. Journal of Animal Ecology, 80(1): 171-182.
Linzmeier AM, Ribeiro-Costa CS. 2011. Body size of Chrysomelidae (Coleoptera) in areas with different levels of conservation in south Brazil[J]. ZooKeys, (157): 1-14.
Lomolino MV. 1985. Body size of mammals on islands: the island rule re-examined[J]. American Naturalist, 125(2): 310-316.
Lomolino MV. 2005. Body size evolution in insular vertebrates: generality of the island rule[J]. Journal of Biogeography, 32(10): 1683-1699.
Luschi P, Hays GC, Del Seppia C, et al. 1998. The navigational feats of green sea turtles migrating from Ascension Island investigated by satellite telemetry[J]. Proceedings of the Royal Society B: Biological Sciences, 265(1412): 2279-2284.
Lutz PL, Musick JA. 1997. The biology of sea turtles[M]. Boca Raton, FL: CRC Press.
Malonza PK. 2003. Ecology and distribution of the pancake tortoise, Malacochersus tornieri in Kenya[J]. Journal of East African Natural History, 92(1): 81-96.
Motani R. 2010. Warm-blooded ‘sea dragons’?[J]. Science, 328(5984): 1361-1362.
Mrosovsky N. 1980. Thermal biology of sea turtles[J]. American Zoologist, 20(3): 531-547.
Munteanu VD. 2014. Evolution of the morphology of bottom walking turtles[D]. Lewisburg, PA: Bucknell University.
Palkovacs EP. 2003. Explaining adaptive shifts in body size on islands: a life history approach[J]. Oikos, 103(1): 37-44.
Perry G, Garland T. 2002. Lizard home ranges revisited: effects of sex, body size, diet, habitat, and phylogeny[J]. Ecology, 83(7): 1870-1885.
Persson L, Andersson J, Wahlstrom E, et al. 1996. Size specific interactions in lake systems: predator gape limitation and prey growth rate and mortality[J]. Ecology, 77(3): 900-911.
Principe RE. 2008. Taxonomic and size structures of aquaticmacroinvertebrate assemblages in different habitats of tropical streams, Costa Rica[J]. Zoological Studies, 47(5): 525-534.
Pritchard PCH. 1996. The Galapagos tortoises:nomenclatural and survival status[M]. Lunenburg, MA: Chelonian Research Foundation in association with Conservation International and Chelonia Institute.
Pyron M. 1999. Relationships between geographical range size, body size, local abundance, and habitat breadth in North American suckers and sunfishes[J]. Journal of Biogeography, 26(3): 549-558.
Rivera G, Rivera AR, Dougherty EE, et al. 2006. Aquatic turning performance of painted turtles (Chrysemys picta) and functional consequences of a rigid body design[J]. Journal of Experimental Biology, 209(21): 4203-4213.
Rivera G. 2008. Ecomorphological variation in shell shape of the freshwater turtle Pseudemys concinna inhabiting different aquatic flow regimes[J]. Integrative and Comparative Biology, 48(6): 769-787.
Romer AS. 1967. The vertebrate story[M]. Chicago: University of Chicago.
Stephens PR, Wiens JJ. 2009. Evolution of sexual size dimorphisms in emydid turtles: ecological dimorphism, Rensch's rule, and sympatric divergence[J]. Evolution, 63(4): 910-925.
Tershy BR. 1992. Body size, diet, habitat use, and social behavior of Balaenoptera whales in the gulf of California[J]. Journal of Mammalogy, 73(3): 477-486.
van Dijk PP, Iverson JB, Rhodin AGJ, et al. 2014. Turtles of the world: annotated checklist of taxonomy, synonymy, distribution with maps, and conservation status (7th edition)[M]// Rhodin AGJ, Pritchard PCH, van Dijk PP, et al. Conservation biology of freshwater turtles and tortoises: a compilation project of the IUCN/SSC tortoise and freshwater turtle specialist group. Chelonian Research Monographs No. 5. Lunenburg, MA: Chelonian Research Foundation: 329-479.
van Valen L. 1973. A new evolutionary law[J]. Evolutionary Theory, 1(1): 1-30.
Vermeij GJ. 1994. The evolutionary interaction among species: selection, escalation, and coevolution[J]. Annual Review of Ecology & Systematics, 25(1): 219-236.
Xiao F, Wang J, Shi H, et al. 2017. Ecomorphological correlates of microhabitat selection in two sympatric Asian box turtle species (Geoemydidae: Cuora)[J]. Canadian Journal of Zoology, 95(10): 753-758.
张孟闻, 宗愉, 马积藩. 1998. 中国动物志爬行纲(第Ⅰ卷)[M]. 北京: 科学出版社.
Angielczyk KD, Burroughs RW, Feldman CR. 2015. Do turtles follow the rules? Latitudinal gradients in species richness, body size, and geographic range area of the world's turtles: latitudinal gradients in turtles[J]. Journal of Experimental Zoology, Part B: Molecular and Developmental Evolution, 324(3): 270-294.
Arnold EN. 1979. Indian ocean giant tortoises: their systematics and island adaptations[J]. Philosophical Transactions of the Royal Society B: Biological Sciences, 286(1011): 127-145.
Bambach RK. 1993. Seafood through time: changes in biomass, energetics, and productivity in the marine ecosystem[J]. Paleobiology, 19(3): 372-397.
Benson RBJ, Domokos G, Várkonyi P, et al. 2011. Shell geometry and habitat determination in extinct and extant turtles (Reptilia: Testudinata)[J]. Paleobiology, 37(4): 547-562.
Bernard A, Lécuyer C, Vincent P, et al. 2010. Regulation of body temperature by some Mesozoic marine reptiles[J]. Science, 328(5984): 1379-1382.
Berry JF, Shine R. 1980. Sexual size dimorphism and selection in turtle (Order Testudins)[J]. Oecologia (Berlin), 44(2): 185-191.
Bondi CA, Marks SB. 2013. Differences in flow regime influence the seasonal migrations, body size, and body condition of western pond turtles (Actinemys marmorata) that inhabit perennial and intermittent riverine sites in northern California[J]. Copeia, 2013(1): 142-153.
Bonin F, Devaux B, Dupré A. 2006. Turtles of the world[M]. Baltimore: The Johns Hopkins University Press.
Bonnet X, Delmas V, El-Mouden H, et al. 2010. Is sexual body shape dimorphism consistent in aquatic and terrestrial chelonians?[J]. Zoology, 113(4): 213-220.
Claude J, Paradis E, Tong H, et al. 2003. A geometric morphometric assessment of the effects of environment and cladogenesis on the evolution of the turtle shell[J]. Biological Journal of the Linnean Society, 79(3): 485-501.
Claude J, Prichard P, Tong H, et al. 2004. Ecological correlates and evolutionary divergence in the skull of turtles: a geometric morphometric assessment[J]. Systematic Biology, 53(6): 933-948.
Cohen JE, Pimm SL, Yodzis P, et al. 1993. Body sizes of animal predators and animal prey in food webs[J]. Journal of Animal Ecology, 62(1): 67-78.
Collar DC, Schulte JA, Losos JB. 2011. Evolution of extreme body size disparity in monitor lizards (Varanus)[J]. Evolution, 65(9): 2664-2680.
Ernst CH, Barbour RW. 1989. Turtles of the world[M]. Washington DC: Smithsonian Institution Press.
Ernst CH, Lovich J. 2009. Turtles of the United States and Canada (2nd edition)[M]. Baltimore: The Johns Hopkins University Press.
Farlow JO, Pianka ER. 2002. Body size overlap habitat partitioning and living space requirements of terrestrial vertebrate predators: implications for the paleoecology of large theropod dinosaurs[J]. Historical Biology, 16(1): 21-40.
Fish FE, Nicastro AJ. 2003. Aquatic turning performance by the whirligig beetle: constraints on maneuverability by a rigid biological system[J]. Journal of Experimental Biology, 206(10): 1649-1656.
Gaeta JW, Ahrenstorff TD, Diana JS, et al. 2018. Go big or … don't? A field-based diet evaluation of freshwater piscivore and prey fish size relationships[J]. PLoS ONE, 13(3): e0194092. DOI:10.1371/journal.pone.0194092.
Head JJ, Bloch JI, Hastings AK, et al. 2009. Giant boid snake from the Palaeocene neotropics reveals hotter past equatorial temperatures[J]. Nature, 457(7230): 715-718.
Heim NA, Knope ML, Schaal EK, et al. 2015. Cope's rule in the evolution of marine animals[J]. Science, 347(6224): 867-870.
Ireland LC, Gans C. 1972. The adaptive significance of the flexible shell of the tortoise, Malacochersus tornieri[J]. Animal Behaviour, 20(4): 778-781.
Jaffe AL, Slater GJ, Alfaro ME. 2011. The evolution of island gigantism and body size variation in tortoises and turtles[J]. Biology Letters, 7(4): 558-561.
Joyce WG, Gauthier JA. 2004. Palaeoecology of Triassic stem turtles sheds new light on turtle origins[J]. Proceedings of the Royal Society B: Biological Sciences, 271(1534): 1-5.
Li Y, Xu F, Guo Z, et al. 2011. Reduced predator species richness drives the body gigantism of a frog species on the Zhoushan Archipelago in China[J]. Journal of Animal Ecology, 80(1): 171-182.
Linzmeier AM, Ribeiro-Costa CS. 2011. Body size of Chrysomelidae (Coleoptera) in areas with different levels of conservation in south Brazil[J]. ZooKeys, (157): 1-14.
Lomolino MV. 1985. Body size of mammals on islands: the island rule re-examined[J]. American Naturalist, 125(2): 310-316.
Lomolino MV. 2005. Body size evolution in insular vertebrates: generality of the island rule[J]. Journal of Biogeography, 32(10): 1683-1699.
Luschi P, Hays GC, Del Seppia C, et al. 1998. The navigational feats of green sea turtles migrating from Ascension Island investigated by satellite telemetry[J]. Proceedings of the Royal Society B: Biological Sciences, 265(1412): 2279-2284.
Lutz PL, Musick JA. 1997. The biology of sea turtles[M]. Boca Raton, FL: CRC Press.
Malonza PK. 2003. Ecology and distribution of the pancake tortoise, Malacochersus tornieri in Kenya[J]. Journal of East African Natural History, 92(1): 81-96.
Motani R. 2010. Warm-blooded ‘sea dragons’?[J]. Science, 328(5984): 1361-1362.
Mrosovsky N. 1980. Thermal biology of sea turtles[J]. American Zoologist, 20(3): 531-547.
Munteanu VD. 2014. Evolution of the morphology of bottom walking turtles[D]. Lewisburg, PA: Bucknell University.
Palkovacs EP. 2003. Explaining adaptive shifts in body size on islands: a life history approach[J]. Oikos, 103(1): 37-44.
Perry G, Garland T. 2002. Lizard home ranges revisited: effects of sex, body size, diet, habitat, and phylogeny[J]. Ecology, 83(7): 1870-1885.
Persson L, Andersson J, Wahlstrom E, et al. 1996. Size specific interactions in lake systems: predator gape limitation and prey growth rate and mortality[J]. Ecology, 77(3): 900-911.
Principe RE. 2008. Taxonomic and size structures of aquaticmacroinvertebrate assemblages in different habitats of tropical streams, Costa Rica[J]. Zoological Studies, 47(5): 525-534.
Pritchard PCH. 1996. The Galapagos tortoises:nomenclatural and survival status[M]. Lunenburg, MA: Chelonian Research Foundation in association with Conservation International and Chelonia Institute.
Pyron M. 1999. Relationships between geographical range size, body size, local abundance, and habitat breadth in North American suckers and sunfishes[J]. Journal of Biogeography, 26(3): 549-558.
Rivera G, Rivera AR, Dougherty EE, et al. 2006. Aquatic turning performance of painted turtles (Chrysemys picta) and functional consequences of a rigid body design[J]. Journal of Experimental Biology, 209(21): 4203-4213.
Rivera G. 2008. Ecomorphological variation in shell shape of the freshwater turtle Pseudemys concinna inhabiting different aquatic flow regimes[J]. Integrative and Comparative Biology, 48(6): 769-787.
Romer AS. 1967. The vertebrate story[M]. Chicago: University of Chicago.
Stephens PR, Wiens JJ. 2009. Evolution of sexual size dimorphisms in emydid turtles: ecological dimorphism, Rensch's rule, and sympatric divergence[J]. Evolution, 63(4): 910-925.
Tershy BR. 1992. Body size, diet, habitat use, and social behavior of Balaenoptera whales in the gulf of California[J]. Journal of Mammalogy, 73(3): 477-486.
van Dijk PP, Iverson JB, Rhodin AGJ, et al. 2014. Turtles of the world: annotated checklist of taxonomy, synonymy, distribution with maps, and conservation status (7th edition)[M]// Rhodin AGJ, Pritchard PCH, van Dijk PP, et al. Conservation biology of freshwater turtles and tortoises: a compilation project of the IUCN/SSC tortoise and freshwater turtle specialist group. Chelonian Research Monographs No. 5. Lunenburg, MA: Chelonian Research Foundation: 329-479.
van Valen L. 1973. A new evolutionary law[J]. Evolutionary Theory, 1(1): 1-30.
Vermeij GJ. 1994. The evolutionary interaction among species: selection, escalation, and coevolution[J]. Annual Review of Ecology & Systematics, 25(1): 219-236.
Xiao F, Wang J, Shi H, et al. 2017. Ecomorphological correlates of microhabitat selection in two sympatric Asian box turtle species (Geoemydidae: Cuora)[J]. Canadian Journal of Zoology, 95(10): 753-758.