Slow life histories in lizards living in the highlands of the Andes Mountains

  • Jorgelina M. Boretto
  • Facundo Cabezas-Cartes
  • Nora R. Ibargüengoytía
Original Paper


In the highlands of the Andes, lizards must balance precisely the allocation of energy for growth and reproduction to ensure their survival. We studied the individuals’ age, growth rates, age at sexual maturity, and maximum life span of the viviparous lizard Phymaturus antofagastensis, endemic of cold and harsh environments at high altitudes in the Andes Mountains of Catamarca province, Argentina. We also estimated key life history parameters like reproductive effort, lifetime reproductive effort, net reproductive rate, and relative reproductive time in P. antofagastensis as well as in other Phymaturus to compare the interplay among growth, maintenance, and reproduction in species that live across a latitudinal and altitudinal gradient. We found that females and males of P. antofagastensis mature late in life, at 6–7 years old, respectively, and some individuals reached 20 years of age. Adult females showed higher specific growth rates than males and an adult life span of 9 years which, due to their biennial reproduction, results in an estimated production of only four litters in life. This species exhibits one of the highest lifetime reproductive efforts described for lizards. Our results indicate the existence of a tradeoff between the number of reproductive events throughout life and reproductive effort devoted to each event in Phymaturus, related to the phylogenetic group. The palluma group shows low reproductive effort but high number of reproductive events throughout their lives, whereas the patagonicus group shows high reproductive efforts in low number of reproductive events.


Age at sexual maturity Longevity Phymaturus Reproductive effort Skeletochronology 



This study was conducted with research grants from Fondo para la Investigación Científica y Tecnológica (PICT-2010-1125; PICT-2014-3100), Consejo Nacional de Investigaciones Científicas y Técnicas (PIP-11420110100033, PIP-11220120100676) and Universidad Nacional del Comahue (04/B196).

Supplementary material

360_2017_1136_MOESM1_ESM.doc (38 kb)
Supplementary material 1 (DOC 38 KB)


  1. Acosta JC, Villavicencio HJ, Blanco GM (2008) Phymaturus antofagastensis (NCN) Diet. Herpetol Rev 39:91Google Scholar
  2. Adolph SC, Porter WP (1993) Temperature, activity, and lizard life histories. Am Nat 142:273–295CrossRefPubMedGoogle Scholar
  3. Andreone F, Guarino FM (2003) Giant and long-lived? Age structure in Macroscincus coctei, an extinct skink from Cape Verde. Amphibia-Reptilia 24:459–470CrossRefGoogle Scholar
  4. Andrews RM (1976) Growth rate in island and mainland anoline lizards. Copeia 1976:477–482CrossRefGoogle Scholar
  5. Angilletta JM Jr, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509CrossRefPubMedGoogle Scholar
  6. Angilletta JM Jr (2006) Estimating and comparing thermal performance curves. J Therm Biol 31:541–545CrossRefGoogle Scholar
  7. Angilletta JM Jr (2009) Thermal Adaptation. A theoretical and empirical synthesis. Oxford University Press, OxfordCrossRefGoogle Scholar
  8. Barbraud C, Weimerskirch H (2001) Emperor penguins and climate change. Nature 411:183–186CrossRefPubMedGoogle Scholar
  9. Beaupre SJ, Duvall D (1998) Variation in oxygen consumption of the western diamondback rattlesnake (Crotalus atrox): implications for sexual size dimorphism. J Comp Physiol B 168:497–506CrossRefGoogle Scholar
  10. Bielby J, Mace GM, Bininda-Emonds ORP, Cardillo M, Gittelman JL, Jones KE, Orme CDL, Purvis A (2007) The fast–slow continuum in mammalian life history: an empirical reevaluation. Am Nat 169:748–757PubMedGoogle Scholar
  11. Bogert CM (1949) Thermoregulation in reptiles, a factor in evolution. Evolution Int J org Evolution 3:195–211CrossRefGoogle Scholar
  12. 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 27:25–36CrossRefGoogle Scholar
  13. Boretto JM, Ibargüengoytía NR (2009) Phymaturus of Patagonia, Argentina: Reproductive biology of Phymaturus zapalensis (Liolaemidae) and a comparison of sexual dimorphism within the genus. J Herpetol 43:96–104CrossRefGoogle Scholar
  14. Boretto JM, Ibargüengoytía NR, Acosta JC, Blanco GM, Villavicencio HJ, Marinero JA (2007) Reproductive biology and sexual dimorphism of a high-altitude population of the viviparous lizard Phymaturus punae from the Andes in Argentina. Amphibia-Reptilia 28:1–7CrossRefGoogle Scholar
  15. Boretto JM, Ibargüengoytía NR, Jahn G, Acosta JC, Vincenti E, Fornés MW (2010) Asynchronic steroid activity of Leydig and Sertoli cells related to spermatogenic and testosterone cycle in Phymaturus antofagastensis. Gen Comp Endocr 166(3):556–564CrossRefPubMedGoogle Scholar
  16. Boretto JM, Cabezas-Cartes F, Tappari F, Méndez-De la Cruz F, Sinervo B, Scolaro JA, Ibargüengoytía NR (2014a) Reproductive biology of Phymaturus spectabilis (Liolaemidae): females skip reproduction in cold and harsh environments of Patagonia, Argentina. Herpetol Conserv Biol 9:170–180Google Scholar
  17. Boretto JM, Cabezas-Cartes F, Kubisch EL, Sinervo B, Ibargüengoytía NR (2014b) Changes in female reproduction and body condition in an endemic lizard, Phymaturus spectabilis, following the Puyehue volcanic ashfall event. Herpetol Conserv Biol 9:181–191Google Scholar
  18. Boretto JM, Cabezas-Cartes F, Ibargüengoytía NR (2015) Energy allocation to growth and reproduction in a viviparous lizard endemic to the highlands of the Andes, Argentina. J Zool 297:77–86CrossRefGoogle Scholar
  19. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach. Springer, New YorkGoogle Scholar
  20. Cabezas-Cartes F, Boretto JM, Acosta JC, Jahn G, Blanco G, Laspiur A, Ibargüengoytía NR (2010) Reproductive biology of Phymaturus cf. palluma: a vulnerable lizard from the highlands of the Andes, San Juan, Argentina. Herpetol Conserv Biol 5(3):430–440Google Scholar
  21. Cabezas-Cartes F, Boretto JM, Ibargüengoytía NR (2015) Age, growth and life-history parameters of an endemic vulnerable lizard from Patagonia, Argentina. Herpetol J 25:215–224Google Scholar
  22. Cabrera AL (1994) Regiones fitogeográficas argentinas. In: Kugler W (ed) Enciclopedia argentina de agricultura y jardinería. Editorial Acme S.A.C.I., Buenos AiresGoogle Scholar
  23. Cagle FR (1950) The life history of the slider turtle, Pseudemys scripta troosti (Holbrook). Ecol Monogr 20:31–54Google Scholar
  24. Castanet J (1978) Les marques de croissance osseuse comme indicateurs de I'age chez les lezards. Acta Zool 59:35–48Google Scholar
  25. Castanet J (1979) Donées comparatives sur la minéralisation des marques de croissance squelettique chez les Vertébrés. CR Acad SCI Paris 289:405–408Google Scholar
  26. Castanet J (1994) Age estimation and longevity in reptiles. Gerontology 40:174–192Google Scholar
  27. Castanet J, Báez M (1991) Identificación de dos especies de lagartos de un yacimiento sub-fósil de la Isla de Hierro (Islas Canarias) con histología osea. Rev Esp Herpetol 5:43–49Google Scholar
  28. Castanet J, Roche E (1981) Détermination de l’âge chez le lézard des murailles, Lacerta muralis (Laurenti, 1768) au moyen de la squelettochronologie. Rev Suisse Zool 88:215–226Google Scholar
  29. Castro SA, Laspiur A, Acosta JC (2013) Variación anual e intrapoblacional de la dieta de Phymaturus cf. palluma (Iguania: Liolaemidae) de los Andes centrales en Argentina. Rev Mex Biodivers 84:1258–1265CrossRefGoogle Scholar
  30. Cei JM (1986) Reptiles del centro, centro-oeste y sur de la Argentina. Herpetofauna de las zonas áridas y semiáridas. Museo Regionale di Scienze Naturali, TorinoGoogle Scholar
  31. Charnov EL (2002) Reproductive effort, offspring size and benefit–cost ratios in the classification of life histories. Evol Ecol Res 4:749–758Google Scholar
  32. Charnov EL (2005) Reproductive effort is inversely proportional to average adult life span. Evol Ecol Res 7:1221–1222Google Scholar
  33. Charnov EL, Warne R, Moses M (2007) Lifetime reproductive effort. Am Nat 170:129–142CrossRefGoogle Scholar
  34. Corbalán V, Debandi G (2014) Resource segregation in two herbivorous species of mountain lizards from Argentina. Herpetol J 24:201–208Google Scholar
  35. Corbalán V, Debandi G, Kubisch EL (2013) Thermal ecology of two sympatric saxicolous lizards of the genus Phymaturus from the Payunia region (Argentina). J Therm Biol 38:384–389CrossRefGoogle Scholar
  36. Córdoba MA, Acosta JC, Villavicencio HJ, Astudillo V (2015) Análisis trófico de Phymaturus punae (Iguania: Liolaemidae): variación estacional y sexual en la región más austral de la puna Argentina. Rev Mex Biodivers 86(4):1004–1013CrossRefGoogle Scholar
  37. Cruz FB, Belver L, Acosta JC, Villavicencio HJ, Blanco G, Cánovas MG (2009) Thermal biology of Phymaturus lizards: evolutionary constraints or lack of environmental variation? Zoology 112:425–432CrossRefPubMedGoogle Scholar
  38. Cubo J, Legendre P, de Ricqlès A, Montes L, de Margerie E, Castanet J, Desdevises Y (2008) Phylogenetic, functional, and structural components of variation in bone growth rate of amniotes. Evol Dev 10:217–227CrossRefPubMedGoogle Scholar
  39. Curtin AJ, Zug GR, Spotila JR (2009) Longevity and growth strategies of the desert tortoise (Gopherus agassizii) in two American deserts. J Arid Environ 73:463–471CrossRefGoogle Scholar
  40. de Magalhães JP, Costa J, Church GM (2007) An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. J Gerontol 62A:149–160CrossRefGoogle Scholar
  41. Debandi G, Corbalán V, Scolaro JA, Roig-juñent SA (2012) Predicting the environmental niche of the genus Phymaturus: are palluma and patagonicus groups ecologically differentiated? Austral Ecol 37:392–400CrossRefGoogle Scholar
  42. Díaz Gómez JM (2009) Historical biogeography of Phymaturus (Iguania: Liolaemidae) from Andean and Patagonian South America. Zool Scr 38:1–7CrossRefGoogle Scholar
  43. Dunham AE (1978) Food availability as a proximate factor influencing individual growth rates in the iguanid Sceloporus merriami. Ecology 59:770–778CrossRefGoogle Scholar
  44. Dunham AE, Miles DB, Resnick DN (1988) Life history patterns in squamate reptiles. In: Gans C, Huey RB (eds) Biology of the reptilia vol 16, ecology B: defense and life history. Alan Liss, New York, pp 441–522Google Scholar
  45. Duvall D, Guillette LJ Jr, Jones RE (1982) Environmental control of reptilian reproductive cycles. In: Gans C, Harvey Pough F (eds) Biology of the Reptilia. Physiology D. Academic Press, London, pp 201–231Google Scholar
  46. Enlow DH (1969) The bone of reptiles. In: Gans C, d’A Bellairs A (eds) Biology of the reptilia. Academic Press, London, pp 45–80Google Scholar
  47. Espinoza RE, Wiens JJ, Tracy CR (2004) Recurrent evolution of herbivory in small, cold-climate lizards: breaking the ecophysiological rules of reptilian herbivory. P Natl Acad Sci USA 101:16819–16824CrossRefGoogle Scholar
  48. Etheridge R (1995) Redescription of Ctenoblepharys adspersa Tschudi, 1845, and the taxonomy of Liolaeminae (Reptilia: Squamata: Tropiduridae). Am Mus Novit 3142:1–34Google Scholar
  49. Guarino FM, Di Già I, Sindaco R (2010) Age and growth of the sand lizards (Lacerta agilis) from a high Alpine population of north-western Italy. Acta Herpetol 5:23–29Google Scholar
  50. Gutiérrez JA, Piantoni C, Ibargüengoytía NR (2013) Altitudinal effects on life history parameters in populations of Liolaemus pictus argentinus (Sauria: Liolaemidae). Acta Herpetol 8:9–17Google Scholar
  51. Habit EM, Ortiz JC (1996) Ciclo reproductivo de Phymaturus flagellifer (Reptilia, Tropiduridae). Bol Soc Biol Concepción (Chile) 67:7–14Google Scholar
  52. Huey RB, Pianka ER (1977) Seasonal variation in thermoregulatory behavior and body temperature of diurnal Kalahari lizards. Ecology 58:1066–1075CrossRefGoogle Scholar
  53. Huey RB, Stevenson RD (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am Zool 19:357–366CrossRefGoogle Scholar
  54. Huey RB, Hertz PE, Sinervo B (2003) Behavioral drive versus behavioral inertia in evolution: a null model approach. Am Nat 161:357–366CrossRefPubMedGoogle Scholar
  55. Hurvich CM, Tsai CL (1989) Regression and time series model selection in small samples. Biometrika 76:297–307CrossRefGoogle Scholar
  56. Ibargüengoytía NR (2004) Prolonged cycles as a common reproductive pattern in viviparous lizards from Patagonia, Argentina: reproductive cycle of Phymaturus patagonicus. J Herpetol 38:73–79CrossRefGoogle Scholar
  57. Ibargüengoytía NR, Acosta JC, Boretto JM, Villavicencio HJ, Marinero JA, Krenz JD (2008) Field thermal biology in Phymaturus lizards: comparisons from the Andes to the Patagonian steppe in Argentina. J Arid Environ 72:1620–1630CrossRefGoogle Scholar
  58. Kubisch EL, Piantoni C, Williams J, Scolaro JA, Navas CA, Ibargüengoytía NR (2012) Do higher temperatures increase growth in the nocturnal gecko Homonota darwinii (Gekkota: Phyllodactylidae)? A skeletochronological assessment analyzed at temporal and geographic scales. J Herpetol 46:587–595CrossRefGoogle Scholar
  59. Lagarde F, Bonnet X, Henen B, Nagy K, Corbin J, Lacroix A, Trouvé C (2003) Plasma steroid and nutrient levels during the active season in wild Testudo horsfieldi. Gen Comp Endocr 134:139–146CrossRefPubMedGoogle Scholar
  60. Leclair R, Castanet J (1987) A skeletochronological assessment of age and growth in the frog Rana pipiens Schreber (Amphibia, Anura) from southwestern Quebec. Copeia 1987:361–369Google Scholar
  61. Martoja R, Martoja-Pierson M (1970) Técnicas de histología animal. Toray-Masson, BarcelonaGoogle Scholar
  62. Martori R, Cardinale L, Vognolo P (1998) Growth in a population of Liolaemus wiegmannii (Squamata: Tropiduridae) in central Argentina. Amphibia-Reptilia 19:1–9CrossRefGoogle Scholar
  63. Meiri S, Brown JH, Sibly RM (2012) The ecology of lizard reproductive output. Global Ecol Biogeogr 21:592–602CrossRefGoogle Scholar
  64. Mesquita DO, Faria RG, Colli GR, Vitt LJ, Pianka ER (2015) Lizard life-history strategies. Austral Ecol 41:1–5CrossRefGoogle Scholar
  65. Morando M, Avila LJ, Perez CHF, Hawkins MA, Sites JW Jr (2013) A molecular phylogeny of the lizard genus Phymaturus (Squamata, Liolaemini): implications for species diversity and historical biogeography of southern South America. Mol Phylogenet Evol 66:694–714CrossRefPubMedGoogle Scholar
  66. Moreno-Klemming J (2002) La evolución de las estrategias vitales. In: Soler M (ed) Evolución, la base de la biología, Chap. 8. Proyecto Sur de Ediciones, MadridGoogle Scholar
  67. Niewiarowski PH (2001) Energy budget, growth rates, and thermal constraints: toward an integrative approach to the study of life history variation. Am Nat 157:421–433PubMedGoogle Scholar
  68. Ogle DH (2011) FSA: fisheries stock analysis. R package version 0.4.30. Accessed 1 July 2014
  69. Olsson M, Shine R (1999) Plasticity in frequency of reproduction in an alpine lizard Niveoscincus microlepidotus. Copeia 1999:794–796Google Scholar
  70. Olsson M, Madsen T, Shine R (1997) Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. P Roy Soc Lond B Bio 264(1380):455–459CrossRefGoogle Scholar
  71. Pereyra EA (1985) Nuevo iguánido del género Phymaturus del noroeste argentino. Bol Asoc Herpetol Argentina 2:4Google Scholar
  72. Piantoni C, Ibargüengoytía NR, Cussac VE (2006) Age and growth of the Patagonian lizard Phymaturus patagonicus. Amphibia-Reptilia 27:385–392CrossRefGoogle Scholar
  73. Prosser CL, Brown FA Jr (1991) Temperature. In: Prosser CL (ed) Environmental and Metabolic Animal Physiology. Editorial Interamericana, Mexico DF, pp 109–165Google Scholar
  74. R Core Team (2014) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Accessed 1 July 2014
  75. Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468CrossRefGoogle Scholar
  76. Roff DA (1992) The evolution of life histories: theory and analysis. Chapman & Hall, New YorkGoogle Scholar
  77. Roitberg ES, Smirina EM (2006) Age, body size and growth of Lacerta agilis boemica and L. strigata: a comparative study of two closely related lizard species based on skeletochronology. Herpetol J 16:133–148Google Scholar
  78. Saint Girons H (1985) Comparative data on Lepidosaurian reproduction and some time tables. In: Gans C (ed) Biology of the Reptilia, Chap. 15. Wiley, New York, pp 35–58Google Scholar
  79. Schoener TW, Schoener A (1978) Estimating and interpreting body-size growth in some Anolis lizards. Copeia 1978:390–405CrossRefGoogle Scholar
  80. Shine R (1980) “Costs” of reproduction in reptiles. Oecologia 46:92–100CrossRefPubMedGoogle Scholar
  81. Shine R (2004) Does viviparity evolve in cold climate reptiles because pregnant females maintain stable (not high) body temperatures? Evol Int J org Evol 58:1809–1818CrossRefGoogle Scholar
  82. Shine R (2005) Life-history evolution in reptiles. Annu Rev Ecol Evol S 36:23–46CrossRefGoogle Scholar
  83. Shine R, Schwarzkopf L (1992) The evolution of reproductive effort in lizards and snakes. Evol Int J org Evol 46:62–75CrossRefGoogle Scholar
  84. Smirina EM, Ananjeva NB (2007) Growth layers in bones and acrodont teeth of the agamid lizard Laudakia stoliczkana (Blanford, 1875) (Agamidae: Sauria). Amphibia-Reptilia 28:193–204Google Scholar
  85. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  86. Stearns SC (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87:476–486CrossRefPubMedGoogle Scholar
  87. Tinkle DW, Wilbur HM, Tilley SG (1970) Evolutionary strategies in lizard reproduction. Evol Int J org Evol 24:55–74CrossRefGoogle Scholar
  88. Valdecantos S, Lobo F, Martínez V (2007) Estimación de edades, tamaño corporal y adquisición de la madurez sexual en dos especies de Liolaemus. (Iguania: Liolaemidae). Cuad Herpetol 21:31–44Google Scholar
  89. Videla F (1983) Hábitos alimentarios en iguánidos del oeste árido de la Argentina. Deserta 7:192–202Google Scholar
  90. Wapstra E, Swain R, O’Reilly JM (2001). Geographic variation in age and size at maturity in a small Australian viviparous skink. Copeia 2001:646–655CrossRefGoogle Scholar
  91. Wikelski M, Ricklefs RE (2001) The physiology of life histories. Trends Ecol Evol 16:479–481CrossRefGoogle Scholar
  92. Williams GC (1966) Adaptation and natural selection. Princeton University Press, PrincetonGoogle Scholar
  93. Zug GR, Vitt LG, Caldwell GP (2001) Herpetology. an introductory biology of amphibians & reptiles. Academic Press, LondonGoogle Scholar

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Authors and Affiliations

  1. 1.INIBIOMA (CONICET–Universidad Nacional del Comahue), San Carlos de BarilocheRío NegroArgentina

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