, Volume 184, Issue 1, pp 259–266 | Cite as

Measuring the demographic impact of conspecific negative density dependence

  • Evan C. Fricke
  • S. Joseph Wright
Community ecology – original research


Rare plant species often suffer stronger conspecific negative density dependence (CNDD) in studies that assess the impact of local conspecific density on individual survival. All else equal, this causes a relative disadvantage among rare species that appears inconsistent with the role of CNDD in coexistence. The resolution to this apparent paradox is for lower species abundance to decrease the frequency of conspecific interactions sufficiently to outweigh the disadvantage of stronger CNDD. Whether this occurs in natural systems is untested because existing metrics do not isolate demographic impacts of CNDD, and it is also uncertain for tropical forest trees because the greater spatial aggregation observed in rare species could cause higher frequency of conspecific interactions despite lower abundance on the landscape. We develop a new metric, effective density-dependent mortality (EDDM), to quantify the proportion of individuals that are killed by density-dependent effects. We apply EDDM to a long-term study of seed fall and recruitment at Barro Colorado Island, Panama. Rare species had stronger CNDD but lower conspecific densities, and EDDM increased with abundance. Lower abundance, thus, reduces the frequency of conspecific interaction and, consequently, mortality associated with CNDD. This mechanism allows rare species to avoid a disadvantage-when-rare that would, all else equal, result from stronger CNDD in rare species. Our work provides empirical support for a resolution to the apparently paradoxical findings that rare species experience stronger CNDD and may help reconcile contrasting findings for the relationship between the CNDD strength and abundance.


Advantage-when-rare Coexistence Community compensatory trend Janzen–Connell hypothesis Seed dispersal 



We thank Haldre Rogers, Joshua Tewksbury, Janneke Hille Ris Lambers, and Stefan Schnitzer for helpful discussion and comments on the manuscript. ECF was supported by a National Science Foundation Graduate Research Fellowship and a University of Washington Program on Climate Change Fellowship. Seed production and seedling censuses were funded by the Environmental Sciences Program of the Smithsonian Institution. The forest dynamics plot was founded by SP Hubbell and RB Foster and is now managed by R Condit, S Lao and R Perez under the Center for Tropical Forest Science and the Smithsonian Tropical Research in Panama. Numerous organizations provided funding, principally the U.S. National Science Foundation, and hundreds of field workers have contributed.

Author contribution statement

ECF conceived of the study. SJW collected field data. ECF and SJW designed the analysis and wrote the manuscript.

Supplementary material

442_2017_3863_MOESM1_ESM.docx (240 kb)
Supplementary material 1 (DOCX 240 kb)


  1. Bagchi R, Gallery RE, Gripenberg S, Gurr SJ, Lakshmi N, Addis CE, Freckleton RP, Lewis OT (2014) Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506:85–88. doi: 10.1038/nature12911 CrossRefPubMedGoogle Scholar
  2. Bell T, Freckleton RP, Lewis OT (2006) Plant pathogens drive density-dependent seedling mortality in a tropical tree. Ecol Lett 9:569–574. doi: 10.1111/j.1461-0248.2006.00905.x CrossRefPubMedGoogle Scholar
  3. Bever JD, Mangan SA, Alexander HM (2015) Maintenance of plant species diversity by pathogens. Annu Rev Ecol Evol Syst 46:305–325. doi: 10.1146/annurev-ecolsys-112414-054306 CrossRefGoogle Scholar
  4. Bolker BM, R Development Core Team (2014) bbmle: Tools for general maximum likelihood estimation. R package version 1.0.17. Accessed 1 June 2016
  5. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. doi: 10.1016/j.tree.2008.10.008 CrossRefPubMedGoogle Scholar
  6. Chen L, Mi X, Comita LS, Zhang L, Ren H, Ma K (2010) Community-level consequences of density dependence and habitat associations in a broad-leaved forest. Ecol Lett 13:695–704. doi: 10.1111/j.1461-0248.2010.01468.x CrossRefPubMedGoogle Scholar
  7. Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366. doi: 10.1146/annurev.ecolsys.31.1.343 CrossRefGoogle Scholar
  8. Chisholm RA, Muller-Landau HC (2011) A theoretical model linking interspecific variation in density dependence to species abundances. Theor Ecol 4:241–253. doi: 10.1007/s12080-011-0119-z CrossRefGoogle Scholar
  9. Comita LS, Hubbell SP (2009) Local neighborhood and species’ shade tolerance influence survival in a diverse seedling bank. Ecology 90:328–334. doi: 10.1890/08-0451.1 CrossRefPubMedGoogle Scholar
  10. Comita LS, Muller-Landau HC, Aguilar S, Hubbell SP (2010) Asymmetric density dependence shapes species abundance in a tropical tree community. Science 329:330–332. doi: 10.1126/science.1190772 CrossRefPubMedGoogle Scholar
  11. Condit R (1998) Tropical forest census plots. Springer, RG Landes Company, BerlinCrossRefGoogle Scholar
  12. Condit R, Ashton PS, Baker P, Bunyavejchewin S, Gunatilleke S, Gunatilleke N, Hubbell SP, Foster RB, 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 288:1414–1418. doi: 10.1126/science.288.5470.1414 CrossRefPubMedGoogle Scholar
  13. Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: den Boer PJ, Gradwell G (eds) Dynamics of numbers in populations. Pudoc, Wgeningen, pp 289–312Google Scholar
  14. Connell JH, Tracey JG, Webb LJ (1984) Compensatory recruitment, growth, and mortality as factors maintaining rain forest tree diversity. Ecol Monogr 54:141–164. doi: 10.2307/1942659 CrossRefGoogle Scholar
  15. Detto M, Muller-Landau HC (2013) Fitting ecological process models to spatial patterns using scalewise variances and moment equations. Am Nat 181:E68–E82. doi: 10.1086/669678 CrossRefPubMedGoogle Scholar
  16. Detto M, Muller-Landau HC (2016) Rates of formation and dissipation of clumping reveal lagged responses in tropical tree populations. Ecology 97:1170–1181. doi: 10.1890/15-1505.1 CrossRefPubMedGoogle Scholar
  17. Fricke EC, Tewksbury JJ, Rogers HS (2014) Multiple natural enemies cause distance-dependent mortality at the seed-to-seedling transition. Ecol Lett 17:593–598. doi: 10.1111/ele.12261 CrossRefPubMedGoogle Scholar
  18. Garwood NC (1983) Seed germination in a seasonal tropical forest in Panama: a community study. Ecol Monogr 53:159–181CrossRefGoogle Scholar
  19. Green PT, Harms KE, Connell JH (2014) Nonrandom, diversifying processes are disproportionately strong in the smallest size classes of a tropical forest. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1321892112 Google Scholar
  20. Harms KE, Wright SJ, Calderon O, Hernandez A, Herre EA (2000) Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404:493–495. doi: 10.1038/35006630 CrossRefPubMedGoogle Scholar
  21. HilleRisLambers J, Clark JS, Beckage B (2002) Density-dependent mortality and the latitudinal gradient in species diversity. Nature 417:732–735. doi: 10.1038/nature00809 CrossRefGoogle Scholar
  22. Hubbell SP, Foster RB, O’Brien ST, Harms K, Condit R, Wechsler B, Wright SJ, De Lao SL (1999) Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science 283:554–557. doi: 10.1126/science.283.5401.554 CrossRefPubMedGoogle Scholar
  23. Hubbell SP, Condit R, Foster RB (2005) Barro Colorado Island forest census plot data. Accessed 1 Jan 2013
  24. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528CrossRefGoogle Scholar
  25. Johnson DJ, Beaulieu WT, Bever JD, Clay K (2012) Conspecific negative density dependence and forest diversity. Science 336:904–907. doi: 10.1126/science.1220269 CrossRefPubMedGoogle Scholar
  26. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70. doi: 10.1038/417067a CrossRefPubMedGoogle Scholar
  27. Kobe RK, Vriesendorp CF (2011) Conspecific density dependence in seedlings varies with species shade tolerance in a wet tropical forest. Ecol Lett 14:503–510. doi: 10.1111/j.1461-0248.2011.01612.x CrossRefPubMedGoogle Scholar
  28. LaManna JA, Walton ML, Turner BL, Myers JA (2016) Negative density dependence is stronger in resource-rich environments and diversifies communities when stronger for common but not rare species. Ecol Lett 19:657–667. doi: 10.1111/ele.12603 CrossRefPubMedGoogle Scholar
  29. Lebrija-Trejos E, Wright SJ, Hernández A, Reich PB (2014) Does relatedness matter? Phylogenetic density-dependent survival of seedlings in a tropical forest. Ecology 95:940–951. doi: 10.1890/13-0623.1 CrossRefPubMedGoogle Scholar
  30. Lin L, Comita LS, Zheng Z, Cao M (2012) Seasonal differentiation in density-dependent survival in a tropical rain forest. J Ecol 100:905–914. doi: 10.1111/j.1365-2745.2012.01964.x CrossRefGoogle Scholar
  31. Mack KLM, Bever JD (2014) Coexistence and relative abundance in plant communities are determined by feedbacks when the scale of feedback and dispersal is local. J Ecol 102:1195–1201. doi: 10.1111/1365-2745.12269 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Mangan SA, Schnitzer SA, Herre EA, Mack KML, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–756. doi: 10.1038/nature09273 CrossRefPubMedGoogle Scholar
  33. Queenborough SA, Burslem DFRP, Garwood NC, Valencia R (2007) Neighborhood and community interactions determine the spatial pat- tern of tropical tree seedling survival. Ecology 88:2248–2258. doi: 10.1890/06-0737.1 CrossRefPubMedGoogle Scholar
  34. Uriarte M, Swenson NG, Chazdon RL, Comita LS, Kress WJ, Erickson D, Forero-Montaña J, Zimmerman JK, Thompson J (2010) Trait similarity, shared ancestry and the structure of neighbourhood interactions in a subtropical wet forest: implications for community assembly. Ecol Lett 13:1503–1514. doi: 10.1111/j.1461-0248.2010.01541.x CrossRefPubMedGoogle Scholar
  35. Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, NYCrossRefGoogle Scholar
  36. Visser MD, Bruijning M, Wright SJ, Muller-Landau HC, Jongejans E, Comita LC, de Kroon H (2016) Functional traits as predictors of vital rates across the life-cycle of tropical trees. Funct Ecol 30:168–180. doi: 10.1111/1365-2435.12621 CrossRefGoogle Scholar
  37. Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10. doi: 10.1890/10-0340.1 CrossRefPubMedGoogle Scholar
  38. Webb CO, Peart DR (1999) Seedling density dependence promotes coexistence of Bornean rain forest trees. Ecology 80:2006–2017. doi:10.1890/0012-9658(1999)080[2006:SDDPCO]2.0.CO;2Google Scholar
  39. Wright SJ (2002) Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130:1–14. doi: 10.1007/s004420100809 CrossRefGoogle Scholar
  40. Wright SJ, Muller-Landau HC, Calderón O, Hernández A (2005a) Annual and spatial variation in seedfall and seedling recruitment in a neotropical forest. Ecology 86:848–860. doi: 10.1890/03-0750 CrossRefGoogle Scholar
  41. Wright SJ, Jaramillo AM, Pavon J, Condit R, Hubbell SP, Foster RB (2005b) Reproductive size thresholds in tropical trees: variation among individuals, species and forests. J Trop Ecol 21:307–315. doi: 10.1017/S0266467405002294 CrossRefGoogle Scholar
  42. Yenni G, Adler PB, Ernest SKM (2012) Strong self-limitation promotes the persistence of rare species. Ecology 93:456–461. doi: 10.1890/11-1087.1 CrossRefPubMedGoogle Scholar
  43. Zhu K, Woodall CW, Monteiro JVD, Clark JS (2015) Prevalence and strength of density-dependent tree recruitment. Ecology 96:2319–2327. doi: 10.1890/14-1780.1 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Ecology, Evolution, and Organismal BiologyIowa State UniversityAmesUSA
  2. 2.Smithsonian Tropical Research InstituteBalboaPanama

Personalised recommendations