, Volume 175, Issue 2, pp 725–735 | Cite as

Ontogenetic shifts in plant–plant interactions in a rare cycad within angiosperm communities

  • Juan C. Álvarez-YépizEmail author
  • Alberto Búrquez
  • Martin Dovčiak
Conservation ecology - Original research


Gymnosperms and angiosperms can co-occur within the same habitats but key plant traits are thought to give angiosperms an evolutionary competitive advantage in many ecological settings. We studied ontogenetic changes in competitive and facilitative interactions between a rare gymnosperm (Dioon sonorense, our target species) and different plant and abiotic neighbours (conspecific-cycads, heterospecific-angiosperms, or abiotic-rocks) from 2007 to 2010 in an arid environment of northwestern Mexico. We monitored survival and growth of seedlings, juveniles, and adults of the cycad Dioon sonorense to evaluate how cycad survival and relative height growth rate (RHGR) responded to intra- and interspecific competition, canopy openness, and nearest neighbour. We tested spatial associations among D. sonorense life stages and angiosperm species and measured ontogenetic shifts in cycad shade tolerance. Canopy openness decreased cycad survival while intraspecific competition decreased survival and RHGR during early ontogeny. Seedling survival was higher in association with rocks and heterospecific neighbours where intraspecific competition was lower. Shade tolerance decreased with cycad ontogeny reflecting the spatial association of advanced stages with more open canopies. Interspecific facilitation during early ontogeny of our target species may promote its persistence in spite of increasing interspecific competition in later stages. We provide empirical support to the long-standing assumption that marginal rocky habitats serve as refugia from angiosperm competition for slow-growing gymnosperms such as cycads. The lack of knowledge of plant–plant interactions in rare or endangered species may hinder developing efficient conservation strategies (e.g. managing for sustained canopy cover), especially under the ongoing land use and climatic changes.


Competition Facilitation Habitat tracking Tropical dry forest Water use efficiency 



We thank Alejandro Cueva, Leonel Álvarez, Alma Montaño, Oscar Lopez Bujanda, and Enriquena Bustamante for their technical assistance, and the staff of Sierra de Alamos-Rio Cuchujaqui Biosphere Reserve for providing facilities and logistical support. This study complies with current laws of Mexico. Partial funding was provided by PLACA and Pack summer research grants to J. C. A. Y. and the State University of New York College of Environmental Science and Forestry (SUNY–ESF) funding to M. D.; J. C. A. Y. greatly appreciates the Fulbright-Garcia Robles and CONACYT fellowships for doctoral studies at SUNY-ESF. We are grateful to the handling editor, Truman Young, and three anonymous reviewers for their constructive criticisms that greatly improved the quality and clarity of this manuscript.


  1. Ackerly DD (2003) Community assembly, niche conservatism and adaptive evolution in changing environments. Int J Plant Sci 164:S165–S184CrossRefGoogle Scholar
  2. Álvarez-Yépiz JC, Dovčiak M, Búrquez A (2011) Persistence of a rare ancient cycad: effects of environment and demography. Biol Conserv 144:122–130CrossRefGoogle Scholar
  3. Armas C, Pugnaire FI (2009) Ontogenetic shifts in interactions of two dominant shrub species in a semi-arid coastal sand dune system. J Veg Sci 20:535–546CrossRefGoogle Scholar
  4. Bailey TC, Gatrell AC (1995) Interactive spatial data analysis. Longman, HarlowGoogle Scholar
  5. Bates D, Maecheler M (2011) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42.
  6. Becker P (2000) Competition in the regeneration niche between conifers and angiosperms: Bond’s slow seedling hypothesis. Funct Ecol 14:401–412CrossRefGoogle Scholar
  7. Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193PubMedCrossRefGoogle Scholar
  8. Bond WJ (1989) The tortoise and the hare: ecology of angiosperm dominance and gymnosperm persistence. Biol J Linn Soc 36:227–249CrossRefGoogle Scholar
  9. Boyden S, Montgomery RA, Reich PB, Palik BJ (2012) Seeing the forest for the heterogeneous trees: stand-scale resource distributions emerge from tree-scale structure. Ecol Appl 22:1578–1588PubMedCrossRefGoogle Scholar
  10. Brooker RW (2006) Plant–plant interactions and environmental change. New Phytol 171:271–284PubMedCrossRefGoogle Scholar
  11. Burnham KP, Anderson DR (2002) Model selection and inference: a practical information–theoretic approach. Springer, New YorkGoogle Scholar
  12. Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965CrossRefGoogle Scholar
  13. Cannel MGR, Thornley JHM (1998) Temperature and CO2 responses of leaf and canopy photosynthesis: a clarification using the non-rectangular hyperbola model of photosynthesis. Ann Bot 82:883–892CrossRefGoogle Scholar
  14. Chapin ES III, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64:149–175CrossRefGoogle Scholar
  15. Choler P, Michalet R, Callaway RM (2001) Facilitation and competition on gradients in alpine plant communities. Ecology 82:3295–3308CrossRefGoogle Scholar
  16. Comita LS, Condit R, Hubbell SP (2007) Developmental changes in habitat associations of tropical trees. J Ecol 95:482–492CrossRefGoogle Scholar
  17. Craine JM, Reich PB (2005) Leaf-level light compensation points in shade tolerant woody seedlings. New Phytol 166:710–713PubMedCrossRefGoogle Scholar
  18. Donaldson JS (ed) (2003) Cycads. Status Survey and Conservation Action Plan. IUCN/SSC Cycad Specialist Group. IUCN, GlandGoogle Scholar
  19. Dovčiak M, Frelich LE, Reich PB (2001) Discordance in spatial patterns of white pine (Pinus strobus) size-classes in a patchy near-boreal forest. J Ecol 89:280–291CrossRefGoogle Scholar
  20. Dovčiak M, Reich PB, Frelich LE (2003) Seed rain, safe sites, competing vegetation, and soil resources spatially structure white pine regeneration and recruitment. Can J For Res 33:1892–1904CrossRefGoogle Scholar
  21. Dovčiak M, Frelich LE, Reich PB (2005) Pathways in old-field succession to white pine: seed rain, shade, and climate effects. Ecol Monogr 75:363–378CrossRefGoogle Scholar
  22. Fajardo A, McIntire EJB (2011) Under strong niche overlap conspecifics do not compete but help each other to survive: facilitation at the intraspecific level. J Ecol 99:642–650Google Scholar
  23. Frazer GW, Canham CD, Lertzman KP (2000) Gap Light Analyzer (GLA), Version 2.0: image processing software to analyze true-colour, hemispherical canopy photographs. Bull Ecol Soc Am 81:191–197CrossRefGoogle Scholar
  24. Freestone AL (2006) Facilitation drives local abundance and regional distribution of a rare plant in a harsh environment. Ecology 87:2728–2735PubMedCrossRefGoogle Scholar
  25. Givnish TJ (1988) Adaptation to sun vs. shade: a whole-plant perspective. Aust J Plant Physiol 15:63–92CrossRefGoogle Scholar
  26. Goldberg DE, Rajaniemi T, Gurevitch J, Stewart-Oraten A (1999) Empirical approaches to quantifying interaction intensity: competition and facilitation along productivity gradients. Ecology 80:1118–1131CrossRefGoogle Scholar
  27. Goldberg D, Turkington R, Olsvig-Whittaker L, Dyer AR (2001) Density dependence in an annual plant community: variation among life history stages. Ecol Monogr 71:423–446CrossRefGoogle Scholar
  28. Gómez-Aparicio L, Valladares F, Zamora R (2006) Differential light responses of Mediterranean tree saplings: linking ecophysiology with regeneration niche in four co-occurring species. Tree Physiol 26:947–958PubMedCrossRefGoogle Scholar
  29. González-Astorga J, Vovides AP, Cabrera-Toledo D, Nicolalde-Morejón F (2008) Diversity and genetic structure of the endangered cycad Dioon sonorense (Zamiaceae) from Sonora, Mexico: evolutionary and conservation implications. Biochem Syst Ecol 36:891–899CrossRefGoogle Scholar
  30. Goreaud F, Pélissier R (2003) Avoiding misinterpretation of biotic interactions with the intertype K12-function: population independence vs. random labeling hypotheses. J Veg Sci 14:681–692Google Scholar
  31. Hall JA, Walter GH (2013) Seed dispersal of the Australian cycad Macrozamia miquelii (Zamiaceae): are cycads megafauna-dispersed “grove forming” plants? Am J Bot 100:1127–1136PubMedCrossRefGoogle Scholar
  32. Hegyi F (1974) A simulation model for managing jack-pine stands. In: Fries J (ed) Growth model for tree and stand simulation. Royal College of Forestry, Stockholm, pp 74–90Google Scholar
  33. Hoffmann W, Poorter H (2002) Avoiding bias in calculations of relative growth rate. Ann Bot 90:37–42PubMedCrossRefGoogle Scholar
  34. Holmgren M, Gómez-Aparicio L, Quero JL, Valladares F (2012) Non-linear effects of drought under shade: reconciling physiological and ecological models in plant communities. Oecologia 169:293–305PubMedCentralPubMedCrossRefGoogle Scholar
  35. INEGI (1985) Carta edafológica Ciudad Obregón G12-3, 1: 250000, and Huatabampo G12-6, 1: 250000. INEGIGoogle Scholar
  36. IUCN (2012) IUCN Red List of Threatened Species.
  37. Kinhal V, Parthasarathy N (2010) Nucleated succession by an endemic palm Phoenix pusilla enhances diversity of woody species in the arid Coromandel Coast of India. AoB PLANTS 2010:plq007. doi: 10.1093/aobpla/plq007
  38. Kitajima K (1994) Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98:419–428CrossRefGoogle Scholar
  39. Lindblad P, Costa JL (2002) The cyanobacterial—cycad symbiosis. Biol Environ 102:31–33Google Scholar
  40. Maestre FT, Bautista S, Cortina J, Bellot J (2001) Potential of using facilitation by grasses to establish shrubs on a semiarid degraded steppe. Ecol Appl 11:1641–1655CrossRefGoogle Scholar
  41. Maestre FT, Callaway RM, Valladares F, Lortie CJ (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205CrossRefGoogle Scholar
  42. Marler TE, Willis LE (1997) Leaf gas-exchange characteristics of sixteen cycad species. J Am Soc Hortic Sci 122:38–42Google Scholar
  43. McAuliffe JR (1984) Saguaro nurse tree associations in the Sonoran Desert: competitive effects of saguaro. Oecologia 64:319–321CrossRefGoogle Scholar
  44. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739PubMedCrossRefGoogle Scholar
  45. McIntire EJB, Fajardo A (2009) Beyond description: the active and effective way to infer processes from spatial patterns. Ecology 90:46–56PubMedCrossRefGoogle Scholar
  46. Miriti MN (2006) Ontogenetic shift from facilitation to competition in a desert shrub. J Ecol 94:973–979CrossRefGoogle Scholar
  47. Munguía-Rosas MA, Sosa VJ (2008) Nurse plants vs. Nurse objects: the effects of woody plants and rocky cavities on the recruitment of the Pilosocereus leucocephalus columnar cactus. Ann Bot 101:175–185PubMedCentralPubMedCrossRefGoogle Scholar
  48. Niering WA, Whittaker RH, Lowe CH (1963) The saguaro: a population in relation to environment. Science 142:15–23PubMedCrossRefGoogle Scholar
  49. Nobel PS (2009) Physicochemical and environmental plant physiology. Academic Press/Elsevier, San Diego, pp 1–58Google Scholar
  50. Norstog KJ, Nicholls TJ (1997) The biology of cycads. Cornell University Press, IthacaGoogle Scholar
  51. Pacala SW, Levin SA (1997) Biologically generated spatial pattern and the coexistence of competing species. In: Tilman D, Kareiva P (eds) Spatial ecology: the role of space in population dynamics and interspecific interactions. Princeton University Press, Princeton, pp 204–232Google Scholar
  52. Parker KC (1989) Nurse plant relationships of columnar cacti in Arizona. Phys Geogr 10:322–335Google Scholar
  53. Pérez-Farrera MA, Vovides AP (2004) Spatial distribution, population structure and fecundity of Ceratozamia matudai Lundell (Zamiaceae) in El Triunfo Biosphere Reserve, Chiapas, Mexico. Bot Rev 70:299–311CrossRefGoogle Scholar
  54. Pérez-Farrera MA, Vovides AP, Octavio-Aguilar P, González-Astorga J, de la Cruz-Rodríguez J, Hernández-Jonapá R, Villalobos-Méndez SM (2006) Demography of the cycad Ceratozamia mirandae (Zamiaceae) under disturbed and undisturbed conditions in a biosphere reserve of Mexico. Plant Ecol 187:97–108CrossRefGoogle Scholar
  55. Peters EM, Martorell C, Ezcurra E (2008) Nurse rocks are more important than nurse plants in determining the distribution and establishment of globose cacti Mammillaria) in the Tehuacán Valley, Mexico. J Arid Environ 72:593–601CrossRefGoogle Scholar
  56. Preece LD, Duguid AW, Albrecht DE (2007) Environmental determinants of a restricted cycad in central Australia, Macrozamia macdonnellii. Aust J Bot 55:601–607CrossRefGoogle Scholar
  57. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0.
  58. Ripley BD (1979) Test of ‘randomness’ for spatial point patterns. J R Stat Soc 41:368–374Google Scholar
  59. Runkle JR (1981) Gap regeneration in some old-growth forests of eastern North America. Ecology 62:1041–1051CrossRefGoogle Scholar
  60. Schiffers K, Tielbörger K (2006) Ontogenetic shifts in interactions among annual plants. J Ecol 94:336–341CrossRefGoogle Scholar
  61. SEMARNAT (2002) Norma oficial Mexicana NOM-059-SEMARNAT-2001 protección ambiental-especies nativas de México de flora y fauna silvestres-categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-lista de especies en riesgo. Diario Oficial de la FederaciónGoogle Scholar
  62. Soliveres S, DeSoto L, Maestre FT, Olano JM (2010) Spatio-temporal heterogeneity in abiotic factors modulate multiple ontogenetic shifts between competition and facilitation. Perspect Plant Ecol Evol Syst 12:227–234CrossRefGoogle Scholar
  63. Sprugel DG, Rascher KG, Gersonde R, Dovčiak M, Lutz JA, Halpern CB (2009) Spatially explicit modeling of overstory manipulations in young forests: effects on stand structure and light. Ecol Model 220:3565–3575CrossRefGoogle Scholar
  64. Tewksbury JJ, Lloyd JD (2001) Positive interactions under nurse-plants: spatial scale, stress gradients and benefactor size. Oecologia 127:425–434CrossRefGoogle Scholar
  65. Turner RM, Alcorn SM, Olin G, Booth JA (1966) The influence of shade, soil, and water on saguaro seedling establishment. Bot Gaz 127:95–102CrossRefGoogle Scholar
  66. Valiente-Banuet A, Ezcurra E (1991) Shade as a cause of the association between the cactus Neobuxbaumia tetetzo and the nurse plant Mimosa luisana in the Tehuacan Valley, Mexico. J Ecol 79:961–971CrossRefGoogle Scholar
  67. Valiente-Banuet A, Vital Rumebe A, Verdú M, Callaway RM (2006) Modern Quaternary plant lineages promote diversity through facilitation of ancient Tertiary lineages. PNAS 103:16812–16817PubMedCentralPubMedCrossRefGoogle Scholar
  68. Vovides AP (1990) Spatial distribution, survival and fecundity of Dioon edule (Zamiaceae) in a tropical deciduous forest in Veracruz, Mexico, with notes on its habitat. Am J Bot 77:1532–1543CrossRefGoogle Scholar
  69. Walters MB, Reich PB (1996) Are shade tolerance, survival, and growth linked? Low light and nitrogen effects on hardwood seedlings. Ecology 77:841–853CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Juan C. Álvarez-Yépiz
    • 1
    Email author
  • Alberto Búrquez
    • 2
  • Martin Dovčiak
    • 1
  1. 1.College of Environmental Science and ForestryState University of New YorkSyracuseUSA
  2. 2.Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoHermosilloMéxico

Personalised recommendations