Differences among species in seed dispersal and conspecific neighbor effects can interact to influence coexistence
Tóm tắt
Seed dispersal is a critical mechanism for escaping specialist natural enemies. Despite this, mean dispersal distances can vary by an order of magnitude among plant species in the same community. Here, we develop a theoretical model to explore how interspecific differences in seed dispersal alter the impact of specialist natural enemies, both on their own and though a trade-off between seed dispersal and enemy susceptibility. Our model suggests that species are more able to recover from rarity if they have high dispersal because (1) seedlings are more likely to escape their parent’s natural enemies, (2) adults are more spread out, reducing the chance that a seed will disperse near conspecifics, and (3) seedlings compete less with kin for open gaps. Differences in dispersal do not produce stabilizing mechanisms—species with low dispersal are purely at a disadvantage and do not gain a novel niche opportunity. However, dispersal-susceptibility trade-offs will be equalizing, as species disadvantaged by low dispersal will benefit from being less susceptible to specialist natural enemies. This mechanism, unlike most mechanisms of dispersal-mediated coexistence, does not require that there is an abundance of empty space: high-dispersers gain an advantage by escaping from their enemies, not by colonizing empty habitat. Our study therefore suggests that differences in dispersal are unlikely to promote diversity on their own, but may strengthen other coexistence mechanisms.
Tài liệu tham khảo
Adler FR, Muller-Landau HC (2005) When do localized natural enemies increase species richness? Ecol Lett 8(4):438–447
Augspurger CK (1983) Seed dispersal of the tropical tree, Platypodium elegans, and the esape of its seedlings from fungal pathogens. J Ecol 71(3):759–771
Augspurger CK, Kelly CK (1984) Pathogen mortality of tropical tree seedlings - experimental studies of the effects of dispersal distance, seedling denisity, and light conditions. Oecologia 61(2):211–217
Barabás G, D’Andrea R, Stump SM (2018) Chesson’s coexistence theory. Ecol Monogr 88(3):277–303
Becker P, Wong M (1985) Seed dispersal, seed predation, and juvenile mortality of Aglaia sp (Meliaceae) in lowland dipterocarp rainforest. Biotropica 17(3):230–237
Beckman NG, Bullock JM, Salguero-Gȯmez R (2018) High dispersal ability is related to fast life-history strategies. J Ecol 106(4):1349–1362
Bever JD (1994) Feedback between plants and their soil communities in an old field community. Ecology 75(7):1965–1977
Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85(5):561–573
Bolker BM, Pacala S (1999) Spatial moment equations for plant competition: understading spatial strategies and the advantages of short dispersal. Am Nat 153(6):575–602
Bullock JM, Mallada González L, Tamme R, Gȯtzenberger L, White SM, Pȧrtel M, Hooftman DA (2017) A synthesis of empirical plant dispersal kernels. J Ecol 105(1):6–19
Chen Y, Jia P, Cadotte MW, Wang P, Liu X, Qi Y, Jiang X, Wang Z, Shu W (2019) Rare and phylogenetically distinct plant species exhibit less diverse root-associated pathogen communities. J Ecol 107(3):1226–1237
Chesson P (1994) Multispecies competition in variable environments. Theor Popul Biol 45 (3):227–276
Chesson P (2000) General theory of competitive coexistence in spatially-varying environments. Theor Popul Biol 58(3):211–237
Chesson P (2003) Quantifying and testing coexistence mechanisms arising from recruitment fluctuations. Theor Popul Biol 64(3):345–357
Chisholm RA, Muller-Landau HC (2011) A theoretical model linking interspecific variation in density dependence to species abundances. Theor Ecol 4(2):241–253
Clark AT, Detto M, Muller-Landau HC, Schnitzer SA, Wright SJ, Condit R, Hubbell SP (2018) Functional traits of tropical trees and lianas explain spatial structure across multiple scales. J Ecol 106 (2):795–806
Clark JS, Silman M, Kern R, Macklin E, HilleRisLambers J (1999) Seed dispersal near and far: patterns across temperate and tropical forests. Ecology 80(5):1475–1494
Cobo-Quinche J, Endara MJ, Valencia R, Muṅoz-Upegui D, Cȧrdenas R E (2019) Physical, but not chemical, antiherbivore defense expression is related to the clustered spatial distribution of tropical trees in an Amazonian forest. Ecol Evol 9(4):1750–1763
Comita LS, Aguilar S, Pėrez R, Lao S, Hubbell SP (2007) Patterns of woody plant species abundance and diversity in the seedling layer of a tropical forest. J Veg Sci 18:163–174
Comita LS, Muller-Landau HC, Aguilar S, Hubbell SP (2010) Asymmetric density dependence shapes species abundances in a tropical tree community. Science 329(5989):330–332
Comita LS, Queenborough SA, Murphy SJ, Eck JL, Xu K, Krishnadas M, Beckman N, Zhu Y (2014) Testing predictions of the Janzen–Connell hypothesis: a meta-analysis of experimental evidence for distance- and density-dependent seed and seedling survival. J Ecol 102(4):845–856
Condit R, Ashton PS, Baker PJ, Bunyavejchewin S, Guantilleke S, Guantilleke 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(5470):1414–1418
Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and rainforest trees. In: Gradwell PJdb G (ed) Dynamics of populations, Centre for Agricultural Publishing and Documentation, Wageningen, pp 298–312
Detto M, Muller-Landau HC (2016) Rates of formation and dissipation of clumping reveal lagged responses in tropical tree populations. Ecology 97(5):1170–1181
Durrett R, Levin S (1994) The importance of being discrete (and spatial). Theor Popul Biol 46(3):363–394
Ellner SP, Snyder RE, Adler PB (2016) How to quantify the temporal storage effect using simulations instead of math. Ecol Lett 19(11):1333–1342
Ellner SP, Snyder RE, Adler PB, Hooker G (2019) An expanded modern coexistence theory for empirical applications. Ecol Lett 22(1):3–18
Freckleton RP, Lewis OT (2006) Pathogens, density dependence and the coexistence of tropical trees. Proc R Soc B-Biol Sci 273(1604):2909–2916
Fricke EC, Wright SJ (2017) Measuring the demographic impact of conspecific negative density dependence. Oecologia 184(1):259–266
Fricke EC, Tewksbury JJ, Rogers HS (2014) Multiple natural enemies cause distance-dependent mortality at the seed-to-seedling transition. Ecol Lett 17(5):593–598
Gillett JB (1962) Pest pressure, an underestimated factor in evolution. In: Taxonomy and geography; a symposium, vol 4, pp 37–46
Gross K (2008) Fusing spatial resource heterogeneity with a competition–colonization trade-off in model communities. Theor Ecol 1(2):65–75
Grover JP (1994) Assembly rules for communities of nutrient-limited plants and specialist herbivores. Am Nat 143(2):258–282
Hastings A (1980) Disturbance, coexistence, history, and competition for space. Theor Popul Biol 18(3):363–373
Hastings A (1983) Can spatial variation alone lead to selection for dispersal? Theor Popul Biol 24(3):244–251
Howe HF (1993) Specialized and generalized dispersal systems - where does the paradigm stand. Vegetatio 108:3–13
Howe HF, Smallwood J (1982) Ecology of seed dispersal. Ann Rev Ecol Syst 13:201–228
Hubbell SP, Condit R, Foster RB (2005) Barro Colorado Forest Census Plot Data
Huntly N (1991) Herbivores and the dynamics of communities and ecosystems. Ann Rev Ecol Syst 22:477–503
Hutchinson GE (1961) The paradox of the plankton. Am Nat 95(882):137–145
Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104 (940):501–528
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417(6884):67–70
Kobe RK, Vriesendorp CF (2011) Conspecific density dependence in seedlings varies with species shade tolerance in a wet tropical forest. Ecol Lett 14(5):503–510
Krishnadas M, Comita LS (2018) Influence of soil pathogens on early regeneration success of tropical trees varies between forest edge and interior. Oecologia 186(1):259–268
Lebrija-Trejos E, Reich PB, Hernȧndez A, Wright SJ (2016) Species with greater seed mass are more tolerant of conspecific neighbours: a key driver of early survival and future abundances in a tropical forest. Ecol Lett 19(9):1071–1080
Levi T, Barfield M, Barrantes S, Sullivan C, Holt RD, Terborgh J (2019) Tropical forests can maintain hyperdiversity because of enemies. Proc Natl Acad Sci 116(2):581–586
Levin SA, Muller-Landau HC, Nathan R, Chave J (2003) The ecology and evolution of seed dispersal: a theoretical perspective. Ann Rev Ecol Evol Syst 34:575–604
Levine JM, Murrell DJ (2003) The community-level consequences of seed dispersal patterns. Ann Rev Ecol Evol Syst 34(1):549–574
Loehle C (1988) Tree life history strategies: the role of defenses. Can J For Res 18(2):209–222
Mack KM, 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(5):1195–1201
Mack KML, Eppinga MB, Bever JD (2019) Plant-soil feedbacks promote coexistence and resilience in multi-species communities. PLOS One 14(2):e0211572
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 (7307):752–755
Miranda A, Carvalho LM, Dionisio F (2015) Lower within-community variance of negative density dependence increases forest diversity. PLOS One 10(5):e0127260
Muller-Landau HC Carson WP, Schuster S (eds) (2008) Colonization-related trade-offs in tropical forests and their role in the maintenance of plant diversity, vol 11. Wiley-Blackwell, Oxford, UK, chap
Muller-Landau HC, Adler FR (2007) How seed dispersal affects interactions with specialized natural enemies and their contribution to the maintenance of diversity. In: Dennis A J, Schupp E W, Green R J, Westcott D A (eds) Seed dispersal: theory and its application in a changing world., CABI, Oxfordshire, UK, pp 407–426
Muller-Landau HC, Wright SJ, Calderȯn O, Condit R, Hubbell SP (2008) Interspecific variation in primary seed dispersal in a tropical forest. J Ecol 96(4):653–667
Murrell DJ, Law R (2003) Heteromyopia and the spatial coexistence of similar competitors. Ecol Lett 6(1):48–59
Plotkin JB, Chave JM, Ashton PS (2002) Cluster analysis of spatial patterns in malaysian tree species. Am Nat 160(5):629–644
Sedio BE, Ostling AM (2013) How specialised must natural enemies be to facilitate coexistence among plants? Ecol Lett 16(8):995–1003
Seidler TG, Plotkin JB (2006) Seed dispersal and spatial pattern in tropical trees. PLoS Biol 4(11):e344
Snyder RE, Adler PB (2011) Coexistence and coevolution in fluctuating environments: can the storage effect evolve? Am Nat 178(4):E76–E84
Stump SM, Chesson P (2015) Distance-responsive predation is not necessary for the Janzen-Connell hypothesis. Theor Popul Biol 106:60–70
Stump SM, Comita LS (2018) Interspecific variation in conspecific negative density dependence can make species less likely to coexist. Ecol Lett 21(10):1541–1551
Stump SM, Johnson EC, Klausmeier CA (2018a) Local interactions and self-organized spatial patterns stabilize microbial cross-feeding against cheaters. J Royal Soc Interface 15(140):20170822
Stump SM, Johnson EC, Sun Z, Klausmeier CA (2018b) How spatial structure and neighbor uncertainty promote mutualists and weaken black queen effects. J Theor Biol 446:33–60
Terborgh J (2012) Enemies maintain hyperdiverse tropical forests. Am Nat 179(3):303–314
Terborgh JW (2015) Toward a trophic theory of species diversity. Proc Natl Acad Sci 112 (37):11415–11422
The MathWorks Inc (2017) MATLAB (R2017b)
The MathWorks Inc (2019) Matlab (2019a)
Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75 (1):2–16
Turelli M (1978) Does environmental variability limit niche overlap? Proc Natl Acad Sci of the United States of America 75(10):5085–5089
Turnbull LA, Levine JM, Fergus AJF, Petermann JS (2010) Species diversity reduces invasion success in pathogen-regulated communities. Oikos 119(6):1040–1046
Usinowicz J (2015) Limited dispersal drives clustering and reduces coexistence by the storage effect. The Am Nat 186(5):634– 648
Visser MD, Bruijning M, Wright SJ, Muller-Landau HC, Jongejans E, Comita LS, de Kroon H (2016) Functional traits as predictors of vital rates across the life cycle of tropical trees. Funct Ecol 30(2):168–180
Wright SJ (2002) Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130(1):1–14
Yu DW, Wilson HB (2001) The competition-colonization trade-off is dead; long live the competition-colonization trade-off. The Am Nat 158(1):49–63
Zhu Y, Queenborough SA, Condit R, Hubbell SP, Ma KP, Comita LS (2018) Density-dependent survival varies with species life-history strategy in a tropical forest. Ecol Lett 21(4):506–515