Phenotypic variability and environmental tolerance shed light on nine-banded armadillo Nearctic invasion

  • Anderson FeijóEmail author
  • Bruce D. Patterson
  • Pedro Cordeiro-Estrela
Original Paper


High phenotypic diversity is an intrinsic attribute of successful invaders, but remains poorly studied. Here, we investigate the role of phenotypic traits in biological invasions using one of the few Neotropical mammal lineages that has successfully invaded the Nearctic, the nine-banded armadillo Dasypus novemcinctus. Specifically, we analyzed cranial phenotypic variation of the nine-banded armadillo, comparing ecological associations throughout its native range with those experienced by invasive populations in the United States. We also compared the climatic conditions faced by native and invader armadillos to determine whether the species has broadened its environmental tolerance or remained within its native climatic pool. Our study shows that D. novemcinctus exhibits pronounced morphological variation through its range and that the phenotypic pattern in newly invaded areas departs from trends of the species in its native range. The morphological differences exhibited by invader armadillos can be related to their reduced reliance on myrmecophagy, with armadillos from temperate open areas in North America exploiting a broader range of dietary items. Moreover, we found the climatic conditions faced by alien armadillos during the initial phases of their Nearctic invasion fell within the native climatic range. In sum, high phenotypic variability and substantial environmental tolerance in the nine-banded armadillo help to explain its nearly ubiquitous distribution across contrasting ecosystems in its native range as well as its successful Nearctic invasion. Our findings underscore the importance of studying the covariation of morphology and climate across native and invasive ranges to understand biological responses in novel environments.


Alien invader Cingulata Myrmecophagy Niche segregation Relaxed selection Skull adaptation 



We are grateful to the following curators and collection managers for permission to examine specimens in their respective collections: Mario de Vivo and Juliana Gualda-Barros (MZUSP); João Alves de Oliveira and Sérgio Maia Vaz (MN); Lena Geise (UERJ); Claudia Guimarães Costa (MCN-M); Fernando Perini (UFMG); Maria Nazareth Ferreira da Silva (INPA); José de Sousa e Silva Jr. and M. Suely Aparecida Marques-Aguiar (MPEG); Jader Marinho-Filho (UNB); Anternor Silva Jr. and Sebastião Pereira (MHNCI); Sergio Althoff and Elisabete Rechenberg (FURB); Alexandre Uarth Christoff (MCNU); Marcia Jardim (MCN); Diego Astúa and Juliana Correia (UFPE); Robert Voss and Eileen Westwig (AMNH); David Flores and Sergio Lucero (MACN); Enrique M. González (MNHN); Raul Maneyro (ZVCM); Itati Olivares (MLP); Mónica Díaz and Rubén Barquez (CML); Isabel Gamarra de Fox (MNHNP); Kathia Rivero (MNK); Isabel Dias (CBF); Víctor Pacheco (MUSM); Claudia Medina and Fernando Forero (IAVH); Hugo López (ICN); Santiago Burneo and Maria Alejandra Camacho (QCAZ); Jorge Brito (MECN); Luis Albuja and Pablo Moreno (MEPN); Javier Sánchez (EBRG); Arnaldo Ferrer (MHNLS); Carmen Ferreira (MBUCV); Stefan Merker (SMNS); Christiane Funk (ZMB_Mam); Daniela Kalthoff (NRM); Frank Zachos and Alexander Bibl (NMW); Marie-Dominique Wandhammer (MZS Mam); and Hans Mejlon (UUZM). We would also like to give special thanks to Noé de la Sancha, Júlio Vilela, and Natalia Cortés Delgado for valuable comments on an earlier version of the manuscript. This work was partially supported by CAPES, CNPq Sanduiche Scholarship (Grant Number 01129/2015-9) at the Field Museum of Natural History, and the AMNH Grants Program (Collection Study). AF is currently supported by Chinese Academy of Sciences President´s International Fellowship Initiative (Grant No. 2018PB0040).

Supplementary material

10530_2019_2085_MOESM1_ESM.docx (419 kb)
Supplementary material 1 (DOCX 420 kb)


  1. Adams DC, Collyer ML, Kaliontzopoulou A (2019) Geomorph: software for geometric morphometric analyses. R package version 3.1.0.
  2. Alhajeri BH, Steppan SJ (2016) Association between climate and body size in rodents: a phylogeny test of Bergmann´s rule. Mamm Biol 81:219–225CrossRefGoogle Scholar
  3. Alvarado-Serrano DF, Luna L, Knowles LL (2013) Localized versus generalist phenotypes in a broadly distributed tropical mammal: how is intraspecific variation distributed across disparate environments? BMC Evol Biol 13:160–176CrossRefPubMedPubMedCentralGoogle Scholar
  4. Anacleto TCS (2007) Food habits of four armadillos species in the Cerrado Area, Mato Grosso, Brasil. Zool Stud 46:529–537Google Scholar
  5. Arteaga MC, Piñero D, Eguiarte LE, Gasca J, Medellín RA (2012) Genetic structure and diversity of the nine-banded armadillo in Mexico. J Mammal 93:547–559CrossRefGoogle Scholar
  6. Audubon JJ, Bachman J (1854) Quadrupeds of North America, 3rd edn. V.G. Audubon, New YorkGoogle Scholar
  7. Bailey V (1905) Biological survey of Texas. North Am Fauna 25:52–107CrossRefGoogle Scholar
  8. Billet G, Hautier L, Thoisy B, Delsuc F (2017) The hidden anatomy of paranasal sinuses reveals biogeographically distinct morphotypes in the nine-banded armadillo (Dasypus novemcinctus). PeerJ 5:e3593CrossRefPubMedPubMedCentralGoogle Scholar
  9. Blackburn TM, Pysek P, Bacher S, Carlton JT, Duncan RP, Jarosík V, Wilson JRU, Richardson DMM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339CrossRefPubMedGoogle Scholar
  10. Bolnick D, Amarasekare P, Araújo MS, Bürger R, Levine JM, Novak M, Rudolf VH, Schreiber SJ, Urban MC, Vasseur DA (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26(4):183–192CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11CrossRefPubMedGoogle Scholar
  12. Cáceres N, Meloro C, Carotenuto F, Passaro F, Sponchiado J, Melo GL, Raia P (2014) Ecogeographical variation in skull shape of capuchin monkeys. J Biogeogr 41:501–512CrossRefGoogle Scholar
  13. Capellini I, Baker J, Allen WL, Street SE, Venditti C (2015) The role of life history traits in mammalian invasion success. Ecol Lett 18:1099–1107CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cardini A, Dunn JE, O’Higgins P, Elton S (2013) Clines in Africa: does size vary in the same way among widespread sub-Saharan monkeys? J Biogeogr 40:370–381CrossRefGoogle Scholar
  15. Ciancio MR, Castro MC, Galliari FC, Carlini AA, Asher RJ (2012) Evolutionary implications of dental eruption in Dasypus (Xenarthra). J Mamm Evol 19:1–8CrossRefGoogle Scholar
  16. Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis. Ecol Lett 14:419–431CrossRefPubMedGoogle Scholar
  17. Feijó A, Cordeiro-Estrela P (2016) Taxonomic revision of the Dasypus kappleri complex, with revalidations of Dasypus pastasae (Thomas, 1901) and Dasypus beniensis Lönnberg, 1942 (Cingulata, Dasypodidae). Zootaxa 4170:271–297CrossRefPubMedGoogle Scholar
  18. Feijó A, Patterson BD, Cordeiro-Estrela P (2018) Taxonomic revision of the long-nosed armadillos, genus Dasypus Linnaeus, 1758 (Mammalia, Cingulata). PLoS One 13:e0195084CrossRefPubMedPubMedCentralGoogle Scholar
  19. Feijó A, Wen Z, Cheng J, Ge D, Xia L, Yang Q (2019a) Divergent selection along elevational gradients promotes genetic and phenotypic disparities among small mammal populations. Ecol Evol 9:7080–7095CrossRefPubMedPubMedCentralGoogle Scholar
  20. Feijó A, Vilela JF, Cheng J, Schetino MAA, Coimbra RTF, Bonvicino CR, Santos FR, Patterson BD, Cordeiro-Estrela P (2019b) Phylogeny and molecular species delimitation of long-nosed armadillos (Dasypus, Cingulata) supports morphology-based taxonomy. Zool J Linn Soc 186:813–825CrossRefGoogle Scholar
  21. Feng X, Papes M (2015) Ecological niche modeling confirms potential north-east range expansion of the nine-banded armadillo (Dasypus novemcinctus) in the USA. J Biogeogr 42:803–808CrossRefGoogle Scholar
  22. Forsman A (2014) Effects of genotypic and phenotypic variation on establishment are important for conservation, invasion, and infection biology. Proc Natl Acad Sci 111:302–307CrossRefPubMedGoogle Scholar
  23. González-Suárez M, Revilla E (2013) Variability in life-history and ecological traits is a buffer against extinction in mammals. Ecol Lett 16:242–251CrossRefPubMedGoogle Scholar
  24. Graves GR (1991) Bergmann’s rule near the equator: latitudinal clines in body size of an Andean passerine bird. Proc Natl Acad Sci 88:2322–2325CrossRefPubMedGoogle Scholar
  25. Gurevitch J, Fox GA, Wardle GM, Inderjit TD (2011) Emergent insights from the synthesis of conceptual frameworks for biological invasions. Ecol Lett 14:407–418CrossRefPubMedGoogle Scholar
  26. Hautier L, Billet G, Thoisy B, Delsuc F (2017) Beyond the carapace: skull shape variation and morphological systematics of long-nosed armadillos (genus Daypus). PeerJ 5:e3650CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hendges CD (2018) Variação ecogeográfica e funcional do crânio de Tayassuidae (Mammalia: Artiodactyla). Unpublished PhD dissertation, University Federal de Santa MariaGoogle Scholar
  28. Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15CrossRefGoogle Scholar
  29. Hijmans RJ (2015) Raster: geographic data analysis and modeling. R package version 2.5–2.
  30. Humphrey SR (1974) Zoogeography of nine-banded armadillo (Dasypus novemcinctus) in the United States. Bioscience 24:457–462CrossRefGoogle Scholar
  31. Jeschke JM, Strayer DL (2005) Invasion success of vertebrates in Europe and North America. Proc Natl Acad Sci 102:7198–7202CrossRefPubMedGoogle Scholar
  32. Jeschke JM, Strayer DL (2006) Determinants of vertebrate invasion success in Europe and North America. Glob Change Biol 12:1608–1619CrossRefGoogle Scholar
  33. Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay G (2002) Tissue origins and interactions in the mammalian skull vault. Dev Biol 241:106–116CrossRefPubMedGoogle Scholar
  34. Klaczko J, Sherrat E, Setz EZF (2016) Are diet preferences associated to skulls shape diversification in Xenodotine snakes? PLoS One 11:e0148375CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kleunen M, Dawson W, Schlaepfer D, Jeschke JM, Fischer M (2010) Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol Lett 13:947–958PubMedGoogle Scholar
  36. Lahti DC, Johnson NA, Ajie BC, Otto SP, Hendry AP, Blumstein DT, Coss RG, Donohue K, Foster SA (2009) Relaxed selection in the wild. Trends Ecol Evol 24:487–496CrossRefPubMedGoogle Scholar
  37. Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier, AmsterdamGoogle Scholar
  38. Loughry WJ, McDonough CM (2013) The nine-banded armadillo. A natural history. University of Oklahoma Press, OklahomaGoogle Scholar
  39. Loughry WJ, Perez-Heydrich C, McDonough CM, Oli MK (2013) Population dynamics and range expansion in nine-banded armadillos. PLoS One 8:e68311CrossRefPubMedPubMedCentralGoogle Scholar
  40. Maestri R, Fornel R, Gonçalves GL, Geise L, Freitas TRO, Carnaval AC (2016) Predictors of intraspecific morphological variability in a tropical hotspot: comparing the influence of random and non-random factors. J Biogeogr 43:2160–2172CrossRefGoogle Scholar
  41. Marchán-Rivadeneira MR, Larsen PA, Phillips CJ, Strauss RE, Baker RJ (2012) On the association between environmental gradients and skull size variation in the great fruit eating bat, Artibeus lituratus (Chiroptera: Phyllostomidae). Biol J Linn Soc 105:623–634CrossRefGoogle Scholar
  42. McDonough C, Loughry WJ (2008) Behavioral ecology of armadillos. In: Vizcaino SF, Loughry WJ (eds) The biology of the Xenarthra. University Press of Florida, Gainesville, pp 291–293Google Scholar
  43. McNab BK (1980) Energetics and the limits to a temperate distribution in armadillos. J Mammal 61:606–627CrossRefGoogle Scholar
  44. McNab BK (2010) Geographic and temporal correlations of mammalian size reconsidered: a resource rule. Oecologia 164:13–23CrossRefPubMedGoogle Scholar
  45. Meiri S, Dayan T (2003) On the validity of Bergmann’s rule. J Biogeogr 30:331–352CrossRefGoogle Scholar
  46. Monteiro LR, Lessa LG, Are AS (1999) Ontogenetic variation in skull shape of Thrichomys apereoides (Rodentia, Echimyidae). J Mammal 80:102–111CrossRefGoogle Scholar
  47. Newman HH (1913) The natural history of the nine-banded armadillo of Texas. Am Nat 67:513–539CrossRefGoogle Scholar
  48. Nogueira MR, Peracchi AL, Monteiro LR (2009) Morphological correlated of bite force and diet in the skull and mandible of phyllostomid bats. Funct Ecol 23:75–723CrossRefGoogle Scholar
  49. Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D’Amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience 51:933–938CrossRefGoogle Scholar
  50. Peres-Neto PR, Jackson DA, Somers KM (2005) How many principal components? Stopping rules for determining the number of non-trivial axes revisted. Comput Stat Data Anal 49:974–997CrossRefGoogle Scholar
  51. Redford KH (1985) Food habits of armadillos (Xenarthra: Dasypodidae). In: Montgomery GG (ed) The evolution and ecology of armadillos, sloths and vermilinguas. Smithsonian Institution Press, Washington, pp 429–437Google Scholar
  52. Redford KH (1986) Dietary specialization and variation in two mammalian myrmecophages (variation in mammalian myrmecophagy). Rev Chil Hist Nat 59:201–208Google Scholar
  53. Reiss KZ (2000) Feeding in myrmecophagous mammals. In: Schwenk K (ed) Feeding: form, function and evolution in tetrapod vertebrates. Academic Press, London, pp 459–486CrossRefGoogle Scholar
  54. Rodríguez MÁ, López-Sañudo IL, Hawkins BA (2006) The geographic distribution of mammal body size in Europe. Glob Ecol Biogeogr 15:185–193CrossRefGoogle Scholar
  55. Rodríguez MA, Olalla-Tárraga MÁ, Hawkins BA (2008) Bergmann´s rule and the geography of mammal body size in the Western Hemisphere. Glob Ecol Biogeogr 17:274–283CrossRefGoogle Scholar
  56. Rohlf FJ (2013) tpsDig, version 2.17. Department of Ecology and Evolution, State University of New York, Stony BrookGoogle Scholar
  57. Rohlf FJ, Corti M (2000) Use of two-block partial least-wquares to study covariation in shape. Syst Biol 49:740–753CrossRefPubMedGoogle Scholar
  58. Rohlf FJ, Slice D (1990) Extension of the Procrustes method for the optimal superimposition of landmarks. Syst Zoo 39:40–59CrossRefGoogle Scholar
  59. Roig VG (1971) Observaciones sobre la termorregulación em Zaedyus pichiy. Acta Zool Lillo 28:13–18Google Scholar
  60. Schiaffini MI (2016) A test of the Resource’s and Bergmann’s rules in a widely distributed small carnivore from southern South America, Conepatus chinga (Molina, 1782) (Carnivora: mephitidae). Mamm Biol 81:73–81CrossRefGoogle Scholar
  61. Schoch RR (2006) Skull ontogeny: developmental patterns of fishes conserved across major tetrapod clades. Evol Dev 8:524–536CrossRefPubMedGoogle Scholar
  62. Sherman HB (1943) The armadillo in Florida. Fla Entomol 26:54–59CrossRefGoogle Scholar
  63. Sikes RS, Heidt GA, Elrod DA (1990) Seasonal diets of the nine-banded armadillo (Dasypus novemcinctus) in a northern part of its range. Am Midl Nat 123:383–389CrossRefGoogle Scholar
  64. Smith KK, Redford KH (1990) The anatomy and function of the feeding apparatus in two armadillos (Dasypoda): anatomy is not destiny. J Zool 222:27–47CrossRefGoogle Scholar
  65. Sol D (2007) Do successful invaders exist? Pre-adaptations to novel environments in terrestrial vertebrates. In: Nentwig W (ed) Biological invasions. Ecological studies. Springer, Berlin, pp 127–141CrossRefGoogle Scholar
  66. Strecker JK (1926) The extension of range of the nine-banded armadillo. J Mammal 7(3):206–210CrossRefGoogle Scholar
  67. Superina M, Boily P (2007) Hibernation and daily torpor in an armadillo, the pichi (Zaedyus pichiy). Comp Biochem Physiol Part A 148:893–898CrossRefGoogle Scholar
  68. Superina M, Pagnutti N, Abba AM (2014) What do we know about armadillos? An analysis of four centuries of knowledge about a group of South American mammals, with emphasis on their conservation. Mamm Rev 44:69–80CrossRefGoogle Scholar
  69. Taber FW (1939) Extension of the range of the armadillo. J Mammal 20:489–493CrossRefGoogle Scholar
  70. Taber FW (1945) Contribution on the life history and ecology of the nine-banded armadillo. J Mammal 26:211–226CrossRefGoogle Scholar
  71. Taulman JF, Robbins LW (1996) Recent range expansion and distributional limits of the nine-banded armadillo (Dasypus novemcinctus) in the United States. J Biogeogr 23:635–648CrossRefGoogle Scholar
  72. Taulman JF, Robbins LW (2014) Range expansion and distributional limits of the nine-banded armadillo in the United States: an update of Taulman & Robbins (1996). J Biogeogr 41:1626–1630CrossRefGoogle Scholar
  73. R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  74. Vázquez D (2006) Exploring the relationship between niche breadth and invasion success. In: Cadotte MW, McMahon SM, Fukami T (eds) Conceptual ecology and invasions biology: reciprocal approaches to nature. Springer, Berlin, pp 307–322CrossRefGoogle Scholar
  75. Wennersten L, Forsman A (2012) Population-level consequences of polymorphism, plasticity and randomized phenotype switching: a review of predictions. Biol Rev 87:756–767CrossRefPubMedGoogle Scholar
  76. Wetzel RM (1985) Taxonomy and distribution of armadillos, Dasypodidae. In: Montgomery GG (ed) The evolution and ecology of armadillos, sloths and vermilinguas. Smithsonian Institution Press, Washington, pp 23–46Google Scholar
  77. Wetzel RM, Gardner AL, Redford KH, Eisenberg JF (2008) Order Cingulata Illiger, 1811. In: Gardner AL (ed) Mammals of South America. 1. Marsupials, xenarthrans, shrews, and bats, vol 1. University of Chicago Press, Chicago, pp 128–157Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Key Laboratory of Zoological Systematics and Evolution, Institute of ZoologyChinese Academy of SciencesChaoyang DistrictChina
  2. 2.Laboratório de Mamíferos, Departamento de Sistemática e Ecologia, CCENUniversidade Federal da ParaíbaJoão PessoaBrazil
  3. 3.Integrative Research CenterField Museum of Natural HistoryChicagoUSA
  4. 4.Programa de Pós-Graduação Em Ciências Biológicas (Zoologia), Departamento de Sistemática e Ecologia, CCENUniversidade Federal da ParaíbaJoão PessoaBrazil

Personalised recommendations