Volume 41 Issue 2
Mar.  2020
Turn off MathJax
Article Contents
Teddy Angarita-Sierra, Cesar Alejandro López-Hurtado. Exploring the reproductive ecology of the tropical semifossorial snake Ninia atrata. Zoological Research, 2020, 41(2): 157-171. doi: 10.24272/j.issn.2095-8137.2020.015
Citation: Teddy Angarita-Sierra, Cesar Alejandro López-Hurtado. Exploring the reproductive ecology of the tropical semifossorial snake Ninia atrata. Zoological Research, 2020, 41(2): 157-171. doi: 10.24272/j.issn.2095-8137.2020.015

Exploring the reproductive ecology of the tropical semifossorial snake Ninia atrata

doi: 10.24272/j.issn.2095-8137.2020.015
Funds:  This work was supported by the Faculty of Sciences and Project Management Program of the Welfare Office of the Universidad Nacional de Colombia under Grant Nos. 3733, 1150, 1302, 1567, and 3093; Colciencias Scholarship Doctoral Program under Grant No. 6172; Yoluka NGO, Biodiversity and Conservation Research Foundation under Grant No. 001 – 2014; Universidad Manuela Beltrán under act 13072019 and Palmasol S.A. Ac001–2014
More Information
  • Based on histological analyses and field studies, this research describes the reproductive ecology of a population of Ninia atrata snakes inhabiting an oil palm plantation. Furthermore, through a multivariate approach, we explored the main drivers of reproductive output in N. atrata. Results showed that prey abundance and food intake were crucial variables contributing to reproductive output. Multiple linear regression models showed that neonates had high sensitivity (R2=55.29%) to extreme changes in climate, which was strongly related to slug and snail abundance variability and microhabitat quality. Reproductive cycles were markedly different between the sexes, being continuous in males and cyclical in females. Despite this variation, reproductive cycles at the population level were seasonal semi-synchronous. Constant recruitment of neonates all year, multiple clutches, high mating frequency, and continuous sperm production characterized the reproductive phenology of N. atrata. In addition, a significant number of previtellogenic females presented oviductal sperm as well as uterine scars, suggesting a high precocity in the species. The main drivers of reproductive output also differed between the sexes. In females, clutch size and secondary follicle variability were highly related to stomach bolus volume, fat body area, and body mass. In males, height of piles of palm leaves and body mass, rather than intrinsic reproductive traits, were the main drivers of sperm production. Nevertheless, in both cases, the relationship between body mass, prey abundance, and food intake suggests that N. atrata follows the income breeding strategy to compensate for reproductive costs and to maximize fitness.

  • loading
  • [1]
    Akaike H. 1973. Information theory and an extension of the maximum likelihood principle. In: Petrovand BN, Caski F. Proceeding of the Second International Symposium on Information Theory. Budapest: Akademiai Kiado, 1–451.
    [2]
    Alencar LRV, Galdino CAB, Nascimento LB. 2012. Life history aspects of Oxyrhopus trigeminus (Serpentes: Dipsadidae) from two sites in Southeastern Brazil. Journal of Herpetology, 46(1): 9−13. doi: 10.1670/09-219
    [3]
    Almeida-Santos SM, Aguiar LF, Balestrin RL. 1998. Serpentes: Micrurus frontalis (coral snake). Male combat. Herpetological Review, 29: 242.
    [4]
    Almeida-Santos SM, Pizzato L, Marques OA. 2006. Intra-sex synchrony and inter-sex coordination in the reproductive timing of the Atlantic coral snake Micrurus corallinus (Elapidae) in Brazil. Herpetological Journal, 16(4): 371−376.
    [5]
    Almeida-Santos SM, Salomão MG. 2002. Reproduction in neotropical pitvipers, with emphasis on species of the genus Bothrops. In: Schett G, Höggren M, Douglas ME, Greene HW. Biology of the Vipers. Oklahoma: Eagle Mountain Publishing, 445–514.
    [6]
    Almeida-Santos SM, Salomão MG, Peneti EA, Sena PS, Guimarães ES. 1999. Predatory combat a tail wrestling in hierarchical contests of the Neotropical rattlesnake Crotalus durissus terrificus (Serpentes: Viperidae). Amphibia-Reptila, 20: 88−96. doi: 10.1163/156853899X00105
    [7]
    Angarita-Sierra T. 2009. Variatión Geográphic de Ninia atrata en Colombia (Colubridae: Dipsadinae). Papéis Avulsos de Zoologia, 49(2): 277−288.
    [8]
    Angarita-Sierra T. 2014. Hemipenial morphology in the semifossorial snakes of the Genus Ninia and a new species from Trinidad, West Indies (Serpentes: Dipsadidae). South American Journal of Herpetology, 9(2): 114−130. doi: 10.2994/SAJH-D-12-00004.1
    [9]
    Angarita-Sierra T. 2015. Repertoire of antipredator displays in the semifossorial snake Ninia atrata (Hallowell, 1845) (Serpentes: Dipsadidae). Herpetological Notes, 8(2015): 339−344.
    [10]
    Angarita - Sierra T, Lozano - Daza SA. 2019. Life is uncertain, eat dessert first: Feeding ecology and prey-predator interactions of the coffee snake Ninia atrata. Journal of Natural History, 53(23-24): 1401−1420. doi: 10.1080/00222933.2019.1655105
    [11]
    Ávila RW, Ferreira VL, Arruda JA. 2006. Natural history of the South American water snake Helicops leopardinus (Colubridae: Hydropsini) in the Pantanal, Central Brazil. Journal of Herpetology, 40(2): 274−279. doi: 10.1670/113-05N.1
    [12]
    Ávila RW, Kawashita-Ribeiro RA, Ferreira VL, Strüssmann C. 2010. Natural history of the coral snake Micrurus pyrrhocryptus Cope 1862 (Elapidae) from semideciduous forests of western Brazil. South American Journal of Herpetology, 5(2): 97−101. doi: 10.2994/057.005.0204
    [13]
    Balestrin RL, Di-Bernardo M. 2005. Reproductive biology of Atractus reticulatus (Boulenger, 1885) (Serpentes, Colubridae) in southern Brazil. Herpetological Journal, 15(3): 195−199.
    [14]
    Bizerra A, Marques OA, Sazima I. 2005. Reproduction and feeding of the colubrid snake Tomodon dorsatus from South-eastern Brazil. AmphibiaReptilia, 26(1): 33−38.
    [15]
    Blanchardi FN, Finster EB. 1933. A method of marking living snakes for future recognition, with a discussion of some problems and results. Ecology, 14(4): 334−347. doi: 10.2307/1932657
    [16]
    Bonnet X, Bradshaw D, Shine R. 1998. Capital versus income breeding: an ectothermic perspective. Oikos, 83(2): 333−342. doi: 10.2307/3546846
    [17]
    Boretto JM, Ibargüengoytía NR. 2006. Asynchronous spermatogenesis and biennial female cycle of the viviparous lizard Phymaturus antofagastensis (Liolaemidae): reproductive responses to high altitudes and temperate climate of Catamarca, Argentina. Amphibia-Reptilia, 27(1): 25−36. doi: 10.1163/156853806776052119
    [18]
    Boulenger GA. 1885. Second list of reptiles and batrachians from the province Rio Grande do Sul, Brazil sent to the Natural History Museum by Dr. H. van Ihering. Annals and Magazine of Natural History, 5(16): 85−88.
    [19]
    Braz HB, Kasperoviczus KN, Almeida-Santos SM. 2014. Reproductive ecology and diet of the fossorial snake Phalotris lativittatus in the Brazilian Cerrado. Herpetological Journal, 24: 49−57.
    [20]
    Bretona M, Chiaraviglio M. 2003. Reproductive biology, mating aggregations, and sexual dimorphism of the Argentine Boa constrictor (Boa constrictor occidentalis). Journal of Herpetology, 37(3): 510−516. doi: 10.1670/122-02A
    [21]
    Brown GP, Shine R. 2006a. Reproductive ecology of a tropical natricine snake, Tropidonophis mairii (Colubridae). Journal of Zoology, 258(1): 63−72.
    [22]
    Brown GP. Shine R. 2006b. Why do most tropical animals reproduce seasonally? Testing hypotheses on an Australian snake. Ecology, 87(1): 133−143. doi: 10.1890/04-1882
    [23]
    Chevan A, Sutherland M. 1991. Hierarchical partitioning. The American Statistician, 45: 90−96.
    [24]
    Chiaraviglio M. 2006. The effects of reproductive condition on thermoregulation in the Argentina Boa constrictor (Boa constrictor occidentalis) (Boidae). Herpetological Monographs, 20(1): 172−177. doi: 10.1655/0733-1347(2007)20[172:TEORCO]2.0.CO;2
    [25]
    Cope ED. 1868. An examination of the Reptilia and Batrachia obtained by the Orton Expedition to the Equador and the upper Amazon, with notes on other species. Proceedings of the Academy of Natural Sciences of Philadelphia, 20: 96−140.
    [26]
    da Costa-Prudente AL, Costa-Menks A, da Silva FM, Maschio GF. 2014. Diet and reproduction of the Western Indigo Snake Drymarchon corais (Serpentes: Colubridae) from the Brazilian Amazon. Herpetological Notes, 7: 99−108.
    [27]
    Dorcas ME, Willson JD. 2009. Innovative methods for studies of snake ecology and conservation. In: Mullin SJ, Seigel R. Snakes Ecology and Conservation. New York: Cornell University Press, 45–37.
    [28]
    Dos Santos-Acosta MC, Prudente AL, Di-Bernardo M. 2006. Reproductive biology of Tantilla melanocephala (Linnaeus, 1758) (Serpentes, colubridae) from Eastern Amazonia, Brazil. Journal of Herpetology, 40(4): 556−559. doi: 10.1670/0022-1511(2006)40[556:CRBFIW]2.0.CO;2
    [29]
    Erickson BH, Nosanchuk TA. 1977. Understanding Data. New York: McGraw-Hill, 1–351.
    [30]
    Fernández JB, Medina M, Kubisch EL, Scolaro JA, Ibargüengoytía NR. 2017. Reproductive strategies in males of the world’s southernmost lizards. Integrative Zoology, 12(2): 132−147. doi: 10.1111/1749-4877.12224
    [31]
    Fitch HS. 1970. Reproductive cycles in lizards and snakes. Museum of Natural History Miscellaneous Publication, 52: 1−247.
    [32]
    Fox W. 1952. Seasonal variation in the male reproductive system of Pacific Coast garter snakes. Journal of Morphology, 90(3): 481−553. doi: 10.1002/jmor.1050900305
    [33]
    Gaiarsa MP, De Alencar LR, Martins M. 2013. Natural history of Pseudoboine snakes. Papéis Avulsos de Zoologia, 53(19): 261−283.
    [34]
    Gibbons JW, Lovich JE. 1990. Sexual dimorphism in turtles with emphasis on the slider turtle (Trachemys scripta). Herpetological Monographs, 4: 1−29. doi: 10.2307/1466966
    [35]
    Goldberg SR. 2004a. Reproduction in the coffee snake, Ninia maculata (Serpentes: Colubridae), from Costa Rica. Texas Journal of Science, 56(1): 81−84.
    [36]
    Goldberg SR. 2004b. Notes on reproduction in the false coral snakes, Erythrolamprus bizona and Erythrolamprus mimus (Serpentes: Colubridae) from Costa Rica. Texas Journal of Science, 56(2): 171−174.
    [37]
    Goldberg SR. 2006. Reproductive cycle of the salmon-bellied racer, Mastigodryas melanolomus (Serpentes, Colubridae), from Costa Rica. Phylomedusa, 5(8): 145−148.
    [38]
    Gomes CA, Marques OA. 2012. Food habits, reproductive biology, and seasonal activity of the dipsadid snake, Echinanthera undulata (Wied, 1824), from the Atlantic forest in Southeastern Brazil. South American Journal of Herpetology, 7(3): 233−240. doi: 10.2994/057.007.0305
    [39]
    Grey JE. 1841. A catalogue of the species of reptiles and Amphibia hitherto described as inhabiting Australia, with a description of some new species from Western Australia. Journals of Two Expeditions of Discovery in Northwest London: Cambridge Library Collection History of Oceania: 422−449.
    [40]
    Gross J. 2015. Test for Normality. An Online Reference. Version 1.4.0 (16 April 2018). Viena: http://CRAN.R-project.org/package=nortest.
    [41]
    Gualdrón-Durán LE, Calvo-Castellanos MF, Ramírez-Pinilla MP. 2019. Annual reproductive activity and morphology of the reproductive system of an Andean population of Atractus (Serpentes, Colubridae). South American Journal of Herpetology, 14(1): 58−70. doi: 10.2994/SAJH-D-16-00054.1
    [42]
    Guisande-Gonzáles C, Vaamonde-Liste A, Barreiro-Felpeto A. 2014. RWizard. An Online Reference. Version 4.0 16 April 2018). Vigo: http://www.ipez.es/RWizard/Download.html.
    [43]
    Hallowell E. 1845. Descriptions of reptiles from South America, supposed to be new. Proceedings of the Academy of Natural Sciences of Philadelphia, 2: 241−247.
    [44]
    Hartmann MT, Del Grande ML, Da Costa-Gondim J, Mendes MC, Marques OAV. 2002. Reproduction and activity of the snail-eating snake, Dipsas albifrons (Colubridae), in the Southern Atlantic Forest in Brazil. Studies on Neotropical Fauna and Environment, 37(2): 111−114. doi: 10.1076/snfe.37.2.111.8588
    [45]
    Hartmann MT, Marques OAV, Almeida-Santos SM. 2004. Reproductive biology of the southern Brazilian pitviper Bothrops neuwiedi pubescens (Serpentes, Viperidae). Amphibia-Reptilia, 25(1): 77−85. doi: 10.1163/156853804322992850
    [46]
    Hothorn T, Zeileis A, Farebrother RW, Cimmins C, Milo G, Mitchell D. 2017. Testing Linear Regression Models. An Online Referece Version 0.9-35 16 April 2017). Viena: http://CRAN.R-project.org/package=lmtest.
    [47]
    IDEAM (Colombian Institute of Hydrology, Meteorology, and Environmental Studies). 2016. Current weather conditions. An Online Referece (16 Apr. 2017). Bogotá: http://www.ideam.gov.co/web/tiempo-y-clima/prediccion-climatica. (in Spanish)
    [48]
    Ingrasci MJ. 2011. Molecular Systematics of the Coffee Snakes, Genus Ninia (Colubridae: Dipsadinae). Ph. D. Dissertation, University of Texas, Arlington, United States of America.
    [49]
    Iverson JB. 1987. Patterns of relative fecundity in snakes. Florida Science, 50(4): 223−233.
    [50]
    Jan G. 1863. Systematic enumeration of the ophidians belonging to the coronellidae group. Archive for Zoology Anatomy and Physiology, 2(2): 213−330.
    [51]
    Janeiro - Cinquini TRF. 2004. Reproductive capacity of Bothrops jararaca (Serpentes, Viperidae). Iheringia Série Zoologia, 94(4): 429−431. doi: 10.1590/S0073-47212004000400013
    [52]
    Jönsson KI. 1997. Capital and income breeding as alternative tactics of resource use in reproduction. Oikos, 78(1): 57−66. doi: 10.2307/3545800
    [53]
    Krohmer RW, Martinez D, Mason RT. 2004. Development of the renal sexual segment in immature snakes: effect of sex steroid hormones. Comparative Biochemistry and Physiology-Part A: Molecular & Integrative Physiology, 139(1): 55−64.
    [54]
    Lancini AR. 1979. Snakes of Venezuela. Caracas: Arimitano Editors. (in Spanish)
    [55]
    Leão SM, Pelegrim N, De Campos-Nogueira C, Albuquerque-Brandão R. 2014. Natural history of Bothrops itapetiningae Boulenger, 1907 (Serpentes: Viperidae: Crotalinae), an endemic species of the Brazilian Cerrado. Journal of Herpetology, 48(3): 324−331. doi: 10.1670/12-191
    [56]
    Leite PT, Nunes SDF, Kaefer IL, Cechin SZ. 2009. Reproductive biology of the swamp racer Mastigodryas bifossatus (Serpentes: Colubridae) in subtropical Brazil. Zoologia, 26(1): 12−18. doi: 10.1590/S1984-46702009000100003
    [57]
    Linnaeus C. 1758. Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Laurentii Salvii, Holmiæ.
    [58]
    López MS, Giraudo AR. 2008. Ecology of the snake Philodryas patagoniensis (Serpentes, Colubridae) from Northeast Argentina. Journal of Herpetology, 42(3): 474−480. doi: 10.1670/07-087.1
    [59]
    Luna LG. 1968. Manual of histologic staining methods of the armed forces institute of pathology. 3rd edn. New York: McGraw-Hill, 111–112.
    [60]
    Lynch JD. 2015. The role of plantations of the African Palm (Elaeis guiensis JACQ.) in the conservation of snakes in Colombia. Caldasia, 37(1): 169−182. doi: 10.15446/caldasia.v37n1.50992
    [61]
    Marques OAV. 1996. Reproductive biology of the coral snake Erythrolamprus aesculapii Linnaeus (Colubridae), in the Southeastern of Brazil. Revista Brasileira de Zoologia, 13(3): 747−753. doi: 10.1590/S0101-81751996000300022
    [62]
    Marques OAV, Almeida-Santos SM, Rodrigues M, Camargo R. 2009. Mating and reproductive cycle in the Neotropical colubrid snake Chironius bicarinatus. South American Journal of Herpetology, 4(1): 76−80. doi: 10.2994/057.004.0110
    [63]
    Marques OAV, Pizzato L, Almeida-Santos SM. 2013. Reproductive strategies of new world coral snakes, genus Micrurus. Herpetologica, 69(1): 58−66. doi: 10.1655/HERPETOLOGICA-D-12-00091
    [64]
    Marques OAV, Puorto G. 1998. Feeding, reproduction, and growth in the crowned snake Tantilla melanocephala (Colubridae), from southeastern Brazil. Amphibia-Reptilia, 19(3): 311−318. doi: 10.1163/156853898X00214
    [65]
    Mathies T. 2011. Reproductive cycles of tropical snakes. In: Aldridge RD, Sever DM. Reproductive Biology and Phylogeny of Snakes. New Hampshire: CRC Press, 511–550.
    [66]
    McCranie JR, Wilson LD. 1995. Two new species of colubrid snakes of the genus Ninia from Central America. Journal of Herpetology, 29(2): 224−232. doi: 10.2307/1564559
    [67]
    Medina-Rangel GF. 2015. Ninia atrata geographic distribution. Herpetological Review, 46(4): 574−575.
    [68]
    Meneses-Pelayo E, Passos P. 2019. New polychromatic species of Atractus (Serpentes: Dipsadidae) from the eastern portion of the Colombian Andes. Copeia, 107(2): 250−261. doi: 10.1643/CH-18-163
    [69]
    Mesa-Joya FL. 2015. First record of Ninia atrata Hallowell, 1845 (Squamata: Colubridae) from Sierra Nevada de Santa Marta, northern Colombia. Check List, 11(112): 1−3.
    [70]
    Miranda EP, Ribeiro RP Jr., Camera BF, Barros M, Draque J, Micucci P, Waller T, Strüssmann C. 2017. Penny and penny laid up will be many: large yellow anacondas do not disregard small prey. Journal of Zoology, 301(4): 301−309. doi: 10.1111/jzo.12417
    [71]
    Monteiro C, Montgomery CE, Spina F, Sawaya RJ, Martins M. 2006. Feeding, reproduction, and morphology of Bothrops mattogrossensis (Serpentes, Viperidae, Crotalinae) in the Brazilian Pantanal. Journal of Herpetology, 40(3): 408−413. doi: 10.1670/0022-1511(2006)40[408:FRAMOB]2.0.CO;2
    [72]
    Naimi B. 2015. Uncertainty analysis for species distribution models. An Online Reference. Version 1.1 (16 April 2017). Viena: https://cran.r-project.org/web/packages/usdm.
    [73]
    Natera–Mumaw M, Esqueda–Gozález LP, Castelaín–Fernández M. 2015. Snakes Atlas of Venezuela. Santiago de Chile, Dimacofi Negocios Avanzados S.A., 1–441. (in Spanish)
    [74]
    Nogueira C, Sawaya R, Martins M. 2003. Ecology of the pitviper, Bothrops moojeni, in the Brazilian Cerrado. Journal of Herpetology, 37(4): 653−659. doi: 10.1670/120-02A
    [75]
    Parker WS, Plummer MV. 1987. Population ecology. In: Seigel RA, Collins JT, Novak SS. Snakes: Ecology and Evolutionary Biology. New York: MacMillan Publisher Company, 253–301.
    [76]
    Peters WCH. 1861. About new serpents of the king Zoological Museum: Typhlops striolatus, Geophidium dubium, Streptophorus (Ninia) maculatus, Elaps hippocrepis. Monthly Reports of the Royal Prussian Academy of Sciences in Berlin, 1861: 922−925.
    [77]
    Pizzatto L. 2005. Body size, reproductive biology and abundance of the rare pseudoboini snakes genera Clelia and Boiruna (Serpentes, Colubridae) in Brazil. Phyllomedusa, 4(2): 111−122. doi: 10.11606/issn.2316-9079.v4i2p111-122
    [78]
    Pizzatto L, Cantor M, De Oliveira JL, Marques OAV, Capovilla V, Martins M. 2008. Reproductive ecology of dipsadine snakes, with emphasis on South American Species. Herpetologica, 64(2): 168−179. doi: 10.1655/07-031.1
    [79]
    Pizzatto L, Marques OAV. 2002. Reproductive biology of the false coral snake Oxyrhopus guibei (Colubridae) from southeastern Brazil. AmphibiaReptilia, 23(4): 495−504.
    [80]
    Pizzatto L, Marques OAV. 2006. Interpopulational variation in sexual dimorphism, reproductive output, and parasitism of Liophis miliaris (Colubridae) in the Atlantic forest of Brazil. Amphibia-Reptilia, 27(1): 37−46. doi: 10.1163/156853806776052128
    [81]
    Pizzatto L, Marques OAV. 2007. Reproductive ecology of boine snakes with emphasis on Brazilian species and a comparison to pythons. South American Journal of Herpetology, 2(2): 107−122. doi: 10.2994/1808-9798(2007)2[107:REOBSW]2.0.CO;2
    [82]
    Raddi G. 1820. Of some new species of Brazilian reptiles and plants. Memories of Mathematics and Physics of the Italian Society of Sciences Based in Modena, 18: 313−343.
    [83]
    Ramos-Pallares E, Anaya-Rojas JM, Serrano-Cardozo VH, Ramirez-Pinilla MP. 2015. Feeding and reproductive ecology of Bachia bicolor (Squamata: Gymnophthalmidae) in urban ecosystems from Colombia. Journal of Herpetology, 49(1): 108−117. doi: 10.1670/12-261
    [84]
    Rivas JA, Muñoz MC, Burghardt GM, Thorbjarnarson JB. 2007. Sexual size dimorphism and the mating system of the green anaconda (Eunectes murinus). In: Henderson RW, Powell R. Biology of Boas and Pythons. Oklahoma: Eagle Mountain Publishers, 340–362.
    [85]
    Rivas G, Molina CR, Ugueto GN, Barros TR, Barrio-Amorós CL, Kok PJR. 2012. Reptiles of Venezuela: an updated and commented checklist. Zootaxa, 3211: 1−64. doi: 10.11646/zootaxa.3211.1.1
    [86]
    Roze JA. 1966. Taxonomy and Zoogeography of Ophidians from Venezuela. Caracas: Universidad Central de Venezuela, 1–362. (in Spanish)
    [87]
    Saint Girons H, Pfeffer P. 1972. Notes on the ecology of the snakes of Cambodia. Zoologische Mededelingen, 47: 5−87.
    [88]
    Sauvage HE. 1884. On some reptiles from the Museum of Natural History collection. Bulletin Société Philom, 7(8): 142−146.
    [89]
    Scartozzoni RR, Da Graça-Salomão M, Almeida-Santos SM. 2009. Natural history of the Vine Snake Oxybelis fulgidus (Serpentes, Colubridae) from Brazil. South American Journal of Herpetology, 4(1): 81−89. doi: 10.2994/057.004.0111
    [90]
    Schlegel H. 1837. Essay on the Physiognomy of Snake. Descriptive Part. Shonekat M.H, Amsterdam. (in French)
    [91]
    Schneider CA, Rasband WS. Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7): 671−675. doi: 10.1038/nmeth.2089
    [92]
    Seigel RA, Fitch HS. 1984. Ecological patterns of relative clutch mass in snakes. Oecologia, 61(3): 293−301. doi: 10.1007/BF00379625
    [93]
    Shine R. 1991. Intersexual dietary divergence and the evolution of sexual dimorphism in snakes. The American Naturalist, 138(1): 103−122. doi: 10.1086/285207
    [94]
    Shine R. 2003. Reproductive strategies in snakes. Proceedings of the Royal Society B: Biological Sciences, 270(1519): 995−1004. doi: 10.1098/rspb.2002.2307
    [95]
    Shine R, Madsen T. 1997. Prey abundance and predator reproduction: Rats and pythons on tropical Australia floddplain. Ecology, 78(4): 1078−1086.
    [96]
    Silva JL, Vadez J. 1989. Rhythm of activity and period of hatching of some ophidians of the North of Venezuela. Acta Biológica Venezuelica, 12(3-4): 88−96.
    [97]
    Valdujo PH, Nogueira C, Martins M. 2002. Ecology of Bothrops neuwiedi pauloensis (Serpentes: Viperidae: Crotalinae) in the Brazilian Cerrado. Journal of Herpetology, 36(2): 169−176. doi: 10.1670/0022-1511(2002)036[0169:EOBNPS]2.0.CO;2
    [98]
    Vitale F, Svedäng H, Cardinale M. 2006. Histological analysis invalidates macroscopically determined maturity ogives of the Kattegat cod (Gadus morhua) and suggests new proxies for estimating maturity status of individual fish. ICES Journal of Marine Science, 63(3): 485−492. doi: 10.1016/j.icesjms.2005.09.001
    [99]
    Vitt LJ. 1996. Ecological observations on the tropical colubrid snake Leptodeira annulata. Herpetological Natural History, 4(1): 69−76.
    [100]
    Weatherhead PJ, Madsen T. 2006. Linking behavioral ecology to conservation objectives. In: Mullin SJ, Seigel R. Snakes Ecology and Conservation. New York: Cornell University Press, 221–243.
    [101]
    Walsh C, Macnally R. 2015. Hierarchical Partitioning. An Online Reference Version 1.0-4 16 April 2017). Viena: http://CRAN.R-project.org/package=hier.part.
    [102]
    Winne CT, Willson JD, Adrews KM, Reed RN. 2006. Efficacy of marking snakes with disposable medical cautery units. Herpetological Review, 37(1): 52−54.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(10)  / Tables(2)

    Article Metrics

    Article views (2275) PDF downloads(184) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return