Biological Invasions

, Volume 13, Issue 7, pp 1543–1558 | Cite as

Spatial distribution and performance of native and invasive Ardisia (Myrsinaceae) species in Puerto Rico: the anatomy of an invasion

  • Marcia C. Muñoz
  • James D. Ackerman
Original Paper


Comparisons between native and invasive congeners are potentially useful approaches for identifying characteristics that promote invasiveness. Those traits for which an invasive exhibits superior ecological performance are likely to contribute to its invasiveness. We tested the hypothesis that invasive tree species have better ecological performance in early life cycle stages than native species in forests where they coexist. We studied locally sympatric populations of the invasive Ardisia elliptica and the native A. obovata (Myrsinaceae) in Puerto Rico. We compared spatial distribution, herbivory and growth in seedlings, seed germination in the field and under controlled conditions, and fruit production. We found the distribution of each species was aggregated in the three categories of size (seedlings, juveniles and adults) and the populations partially overlapped. The invasive species was the most abundant species in every category of size. The two species did not differ in percentage of leaf area consumed and seedlings of both species had the same relative growth rate (RGR) in the forest. However, the invasive species had higher germination success in the field, faster mean germination time in the lab and higher fruit production. It appears that the success of A. elliptica is not through escape from pathogens or herbivores, but by a better performance in fruiting and seed germination in the forest.


Invasive species Ardisia Spatial relationships Early growth Seed germination Fruit production 



We thank the staff of Julio Enrique Monagas National Park for permission to conduct research within the Park. We also thank Eliezer Nieves from the Centro Ambiental Santa Ana for providing logistic support in Monagas. We are grateful to all our field assistants: Calip, Francisco Amundaray, Eddie Rosas, Mariyoan Guzman, Estephania Uriarte, Luis Pereira, Nestor Arias and Mariolga Mendoza. We also thank Brenda Betancourt for statistical advice. We also thank Ernesto Medina, Tomas Carlo, Elvira Cuevas, Denny Fernandez del Viso and Jess Zimmerman for their advice throughout this project. This research was funded in part by the Department of Biology, Dean of Graduate Studies and Research, and the Center for Tropical Ecology and Conservation of the University of Puerto Rico, and a grant from the USA National Science Foundation (Elvira Cuevas, project director; HRD-0734826). This work represents part of a thesis by MCM presented to the Department of Biology, University of Puerto Rico, in partial fulfillment of requirements of a M.S. degree.


  1. Ackerly DD (2003) Community assembly, niche conservatism, and adaptive evolution in changing environments. Int J Plant Sci 164:165–184CrossRefGoogle Scholar
  2. Agrawal AA, Kotanen PM, Mitchel CE, Power AG, Godsoe W, Klironomos J (2005) Enemy release? An experiment with congeneric plant pairs and diverse above- and belowground enemies. Ecology 86:2979–2989CrossRefGoogle Scholar
  3. Augspurger CK (1984) Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps, and pathogens. Ecology 65:1705–1712CrossRefGoogle Scholar
  4. Barot S, Gignoux J, Menaut JC (1999) Demography of a savanna palm tree: predictions from comprehensive spatial pattern analyses. Ecology 80:1987–2005CrossRefGoogle Scholar
  5. Beckstead J, Meyer SE, Molder CJ, Smith C (2007) A race for survival: can Bromus tectorum seeds escape Pyrenophora semeniperda-caused mortality by germinating quickly? Ann Bot 99:907–914PubMedCrossRefGoogle Scholar
  6. Bellingham PJ (2000) Resprouting as a life history strategy in woody plants communities. Oikos 89:409–416CrossRefGoogle Scholar
  7. Belote RT, Weltzin JF (2006) Interactions between two co-dominant, invasive plants in the understory of a temperate deciduous forest. Biol Invasions 8:1629–1641CrossRefGoogle Scholar
  8. Bray SR, Kitajima K, Sylvia DM (2003) Mycorrhizae differentially alter growth, physiology, and competitive ability of an invasive shrub. Ecol Appl 13:565–574CrossRefGoogle Scholar
  9. Brock MT, Weinig C, Galen C (2005) A comparison of phenotypic plasticity in the native dandelion Taraxacum ceratophorum and its invasive congener T. officinale. New Phytol 166:173–183PubMedCrossRefGoogle Scholar
  10. Burns JH (2004) A comparison of invasive and noninvasive dayflowers (Commelinaceae) across experimental nutrient and water gradients. Divers Distrib 10:387–397CrossRefGoogle Scholar
  11. Burns JH, Winn AA (2006) A comparison of plastic responses to competition by invasive and non-invasive congeners in the Commelinaceae. Biol Invasions 8:797–807CrossRefGoogle Scholar
  12. Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523PubMedCrossRefGoogle Scholar
  13. Carlo TA, Collazo JA, Groom MJ (2003) Avian fruit preferences across a Puerto Rican forested landscape: pattern consistency and implications for seed removal. Oecologia 134:119–131PubMedCrossRefGoogle Scholar
  14. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  15. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335CrossRefGoogle Scholar
  16. Condit R, Ashton PS, Baker P, Bunyavejchewin S, Gunatilleke S, Gunatilleke N, Hubbell SP, Foster R, Itoh A, LaFrankie JV, Lee HS, Losos E, Manokaran N, Sukumar R, Yamakura T (2000) Spatial patterns in the distribution of tropical tree species. Science 288:1414–1418PubMedCrossRefGoogle Scholar
  17. Connor EF, Faeth SH, Simberloff D, Opler P (1980) Taxonomic isolation and the accumulation of herbivorous insects: a comparison of introduced and native trees. Ecol Entomol 5:205–211CrossRefGoogle Scholar
  18. Crawley MJ (2000) Seed predators and plant population dynamics. In: Fenner M (ed) Seed the ecology of regeneration in plant communities. CABI publishing, USA, pp 167–182CrossRefGoogle Scholar
  19. Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183–211CrossRefGoogle Scholar
  20. Debski I, Burslem DFRP, Lamb D (2000) Ecological processes maintaining differential tree species distributions in an Australian subtropical rain forest: implications for models of species coexistence. J Trop Ecol 16:387–415CrossRefGoogle Scholar
  21. DeWalt SJ, Denslow JS, Ickes K (2004) Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology 85:471–483CrossRefGoogle Scholar
  22. Díaz S, Noy-Meir I, Cabido M (2001) Can grazing response of herbaceous plants be predicted from simple vegetative traits? J Appl Ecol 38:497–508CrossRefGoogle Scholar
  23. Elton C (1958) The ecology of the invasions by animals and plants. Chapman and Hall, LondonGoogle Scholar
  24. Fagerström T, Agren G (1980) Phenological spread in plants: a result of adaptations to environmental stochasticity? Plant Ecol 43:83–86CrossRefGoogle Scholar
  25. FEPPC (2009) List of invasive plant species. Florida Exotic Pest Plant Council. Wildland Weeds 12:13–16Google Scholar
  26. Fogarty G, Facelli JM (1999) Growth and competition of Cytisus scoparius, an invasive shrub, and Australian native shrubs. Plant Ecol 144:27–35CrossRefGoogle Scholar
  27. Goergen E, Daehler CC (2001) Reproductive ecology of a native Hawaiian grass (Heteropogon contortus; Poaceae) versus its invasive alien competitor (Pennisetum setaceum; Poaceae). Int J Plant Sci 162:317–326CrossRefGoogle Scholar
  28. Grotkopp E, Rejmanek Grotkopp M, Rost TL (2002) Toward a causal explanation of plant invasiveness: seedling growth and life-history strategies of 29 Pine (Pinus) Species. Am Nat 159:396–419PubMedCrossRefGoogle Scholar
  29. Heidorn T, Joern A (1984) Differential herbivory on C 3 versus C 4 grasses by the grasshopper Ageneotettix deorum (Orthoptera: Acrididae). Oecologia 65:19–25CrossRefGoogle Scholar
  30. 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
  31. Hubbell S (1979) Tree dispersion, abundance, and diversity in a tropical dry forest. Science 203:1299–1309PubMedCrossRefGoogle Scholar
  32. Jogesh T, Carpenter D, Cappuccino N (2008) Herbivory on invasive exotic plants and their non-invasive relatives. Biol Invasions 10:797–804CrossRefGoogle Scholar
  33. Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8:704–714CrossRefGoogle Scholar
  34. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  35. Kitajima K, Fox AM, Sato T, Nagamatsu D (2006) Cultivar selection prior to introduction may increase invasiveness: evidence from Ardisia crenata. Biol Invasions 8:1471–1482CrossRefGoogle Scholar
  36. Kleunen MV, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245PubMedCrossRefGoogle Scholar
  37. Kobayashi H, Mejía E (2005) The genus Ardisia: a novel source of health-promoting compounds and phytopharmaceuticals. J Ethnopharm 96:347–354CrossRefGoogle Scholar
  38. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204PubMedCrossRefGoogle Scholar
  39. Koop AL (2004a) Differential seed mortality among habitats limits the distribution of the invasive non-native shrub Ardisia elliptica. Plant Ecol 172:237–249CrossRefGoogle Scholar
  40. Koop AL (2004b) Rates of natural herbivory and effect of simulated herbivory on plant performance of a native and non-native Ardisia species. Fla Sci 67:293–302Google Scholar
  41. Koop LA, Horvitz CC (2005) Projection matrix analysis of the demography of an invasive, nonnative shrub (Ardisia elliptica). Ecology 86:2661–2672CrossRefGoogle Scholar
  42. Kraft NJB, Cornwell WK, Webb CO, Ackerly DD (2007) Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am Nat 170:271–283PubMedCrossRefGoogle Scholar
  43. Lambrinos JG (2002) The variable invasive success of Cortaderia species in a complex landscape. Ecology 83:518–529CrossRefGoogle Scholar
  44. Leicht-Young SA, Silander JA, Latimer AM (2007) Comparative performance of invasive and native Celastrus species across environmental gradients. Oecologia 154:273–282PubMedCrossRefGoogle Scholar
  45. Lieberman D, Lieberman M, Hartshorn G, Peralta R (1985) Growth rates and age-size relationships of tropical wet forest trees in Costa Rica. J Trop Ecol 1:97–109CrossRefGoogle Scholar
  46. Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545CrossRefGoogle Scholar
  47. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure explaining species invasions. Trends Ecol Evol 20:223–228PubMedCrossRefGoogle Scholar
  48. Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species. A selection from the Global Invasive Species Database. Published by the Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN), 12 ppGoogle Scholar
  49. Lowman DL (1984) An assessment of techniques for measuring herbivory: is rainforest defoliation more intense than we thought? Biotropica 16:264–268CrossRefGoogle Scholar
  50. Mack RN (1996) Predicting the identity and fate of plant invaders: emergent and emerging approaches. Biol Conserv 78:107–121CrossRefGoogle Scholar
  51. Morrison JA, Mauck K (2007) Experimental field comparison of native and non-native maple seedlings: natural enemies, ecophysiology, growth and survival. J Ecol 95:1036–1049CrossRefGoogle Scholar
  52. Osone Y, Ishida A, Tateno M (2008) Correlation between relative growth rate and specific leaf area requires associations of specific leaf area with nitrogen absorption rate of roots. New Phytol 179:417–427PubMedCrossRefGoogle Scholar
  53. Pascarella JB (1997) Breeding systems of Ardisia Sw. (Myrsinaceae). Brittonia 49:45–53CrossRefGoogle Scholar
  54. Pascarella JB (1998) Resiliency and response to hurricane disturbance in a tropical shrub, Ardisia escallonioides (Myrsinaceae), in south Florida. Am J Bot 85:1207–1215CrossRefGoogle Scholar
  55. Pearcy RW (1989) Plant physiological ecology: field methods and instrumentation. Chapman and Hall, NYGoogle Scholar
  56. Pearman PB, Guisan A, Broennimann O, Randin CF (2007) Niche dynamics in space and time. Trends Ecol Evol 19:149–158Google Scholar
  57. Perry JN, Winder L, Holland JM, Alston RD (1999) Red blue plots for detecting clusters in count data. Ecol Lett 2:106–113CrossRefGoogle Scholar
  58. Quin GP, Keough MJ (2002) Experimental design and data analysis for biologist. Cambridge University Press, USAGoogle Scholar
  59. R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL
  60. Radford IJ, Cousens RD (2000) Invasiveness and comparative life-history traits of exotic and indigenous Senecio species in Australia. Oecologia 125:531–542CrossRefGoogle Scholar
  61. Ranal MA, Garcia de Santana D (2006) How and why to measure the germination process? Revista Brasil Bot 29:1–11CrossRefGoogle Scholar
  62. Rejmanek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661CrossRefGoogle Scholar
  63. Ren MX, Zhang Q-G (2009) The relative generality of plant invasion mechanisms and predicting future invasive plants. Weed Res 49:449–460CrossRefGoogle Scholar
  64. Richardson DM, Pysek P (2006) Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog Phys Geog 30:409–431CrossRefGoogle Scholar
  65. Russo SE, Augspurger CK (2004) Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecol Lett 7:1058–1067CrossRefGoogle Scholar
  66. Schierenbeck KA, Mack RN, Sharitz RR (1994) Effects of herbivory on growth and biomass allocation in native and introduced species of Lonicera. Ecology 75:1661–1672CrossRefGoogle Scholar
  67. Schumacher E, Kueffer C, Tobler M, Gmür V, Edwards PJ, Dietz H (2008) Influence of drought and shade on seedling growth of native and invasive trees in the Seychelles. Biotropica 40:543–549CrossRefGoogle Scholar
  68. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:171–176CrossRefGoogle Scholar
  69. Sher AA, Hyatt LA (1999) The disturbed resource-flux invasion matrix: a new framework for patterns of plant invasion. Biol Invasions 1:107–114CrossRefGoogle Scholar
  70. Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PloS Biol 4:727–731CrossRefGoogle Scholar
  71. Suehs CM, Affre L, Médail F (2004) Invasion dynamics of two alien Carpobrotus (Aizoaceae) taxa on a Mediterranean island: II. Reproductive strategies. Heredity 92:550–556PubMedCrossRefGoogle Scholar
  72. Tanner EVJ, Kapos V, Healey JR (1991) Hurricane effects on forest ecosystems in the Caribbean. Biotropica 23:513–521CrossRefGoogle Scholar
  73. Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. PNAS 97:5948–5953PubMedCrossRefGoogle Scholar
  74. Vila M, Gomez A, Maron JL (2003) Are alien plants more competitive than a test using Hypericum perforatum L. Oecologia 137:211–215PubMedCrossRefGoogle Scholar
  75. Webb CO (2000) Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am Nat 156:145–155PubMedCrossRefGoogle Scholar
  76. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505CrossRefGoogle Scholar
  77. Wenny DG (2001) Advantages of seed dispersal: a re-evaluation of directed dispersal. Evol Ecol Res 3:51–74Google Scholar
  78. Wright SJ (2002) Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130:1–14Google Scholar
  79. Zou J, Siemann E, Rogers WE, DeWalt SJ (2008) Decreased resistance and increased tolerance to native herbivores of the invasive plant Sapium sebiferum. Ecography 31:663–671CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Department of Biology, Faculty of Natural SciencesUniversity of Puerto RicoSan JuanUSA
  2. 2.Center for Applied Tropical Ecology and Conservation, Faculty of Natural SciencesUniversity of Puerto RicoSan JuanUSA
  3. 3.Museo de Ciencias Naturales-INCIVACaliColombia

Personalised recommendations