Current Research in the Muller-Landau Lab
Research in my lab is focused on understanding the forces governing the dynamics and structure of plant populations and communities. We integrate empirical and theoretical approaches to pursue this aim, using empirical studies to characterize patterns at different demographic stages, spatial scales and levels of organization, and using theory to link and explain these patterns. Most of our empirical work is focused on tropical forests, one of the most diverse and complex ecosystems on the planet. We are particularly intrigued by the diversity of tree species and tree life history strategies found in these forests, and hope to contribute to a better understanding of the factors maintaining this diversity.- Seed rain – patterns, causes and consequences
- Specialized natural enemies – influences in theory and practice
- Tree life history strategies, demographic rates, diversity, and forest structure
- The future of tropical forests
Seed rain – patterns, causes and consequences
Understanding seed rain is critical to understanding plant population and community dynamics, especially in tropical forests where reproductive adults of most species are absolutely rare and thus seeds of almost all species arrive at only a small minority of regeneration sites (reviewed in Nathan & Muller-Landau 2000, Trends in Ecology and Evolution). My research investigates patterns of seed rain in tropical forests, their underlying mechanisms (ecological and evolutionary), and their consequences for population and community dynamics (reviewed in Muller-Landau & Hardesty 2005, Biotic Interactions book chapter).
I’ve explored the evolutionary forces acting on seed dispersal strategies in a series of theoretical papers with Simon Levin. Our approach was to use game-theoretic models and tools of adaptive dynamics, together with simulation models, to understand evolutionary pressures in communities of competing species (Levin & Muller-Landau 2000, Comptes Rendus; Levin & Muller-Landau 2000, Evolutionary Ecology Research). We showed how specialized, locally dispersing, natural enemies exert strong selection for dispersal, and argued that they may be one of the most important factors selecting for long-distance dispersal in diverse plant communities (Muller-Landau et al. 2003, Ecology). Together with Jérôme Chave and Ran Nathan, we wrote a comprehensive review of theoretical work concerning the ecology and evolution of seed dispersal (Levin et al. 2003, Annual Review of Ecology and Systematics).
To date, I’ve done most of my empirical research on seed rain in Panama, where I have had the privilege of working with long-term datasets on seed rain within mapped plots collected by my collaborators Joe Wright, Steve Hubbell, Rick Condit and Robin Foster. I refined methods for quantifying the degree to which seedling densities are limited by seed arrival and site conditions, and applied them to multiple species, finding that most species were strongly limited by both factors (Muller-Landau et al. 2002, Seed Dispersal book chapter). I worked with Jim Dalling and Steve Hubbell to specifically assess the importance of seed dispersal in determining the densities of seedlings of pioneer tree species in different canopy gaps; we found that even these relatively well-dispersed species exhibit strong seed limitation (Dalling et al. 2002, Journal of Ecology). I showed how interannual variation in seedfall will in theory reduce seedling establishment in the presence of constant spatial density-dependence, theoretical work that was central to a study with Joe Wright on interannual variation in seedfall and seedling establishment (Wright et al. 2005, Ecology).
With support from the National Science Foundation LTREB program and the Center for Tropical Forest Science, I am also working with collaborators in three additional tropical forests to characterize seed production and dispersal strategies of as many individual tropical tree species as possible, and to make comparisons among sites. Preliminary analyses show that the more diverse sites have higher levels of population and community seed limitation, a result that is partly but not completely explained by higher numbers of rare species, and that the relationship between seed mass and seed production is qualitatively similar but quantitatively variable across sites (Muller-Landau et al. in press, Inside CTFS).
To understand the long-term consequences of seed dispersal patterns for long-lived organisms such as trees, I employ mathematical and simulation models. Jérôme Chave, Simon Levin and I used a spatially-explicit, individual-based model, and mathematical approximations thereof, to explore the consequences of dispersal distance and other factors for community-level patterns of species richness, relative abundance, and spatial variation (Chave et al. 2002, American Naturalisty ). This work showed that dispersal distance was one of the most important factors in determining species diversity in both neutral and non-neutral models incorporating speciation: shorter dispersal distances allow more species to coexist by slowing competitive exclusion. I subsequently contributed to work by Rick Condit and coathors quantifying patterns of spatial turnover within tropical tree communities in Panama and Ecuador. We found that turnover at intermediate scales (100 m – 10 km) was consistent with predictions based on my estimates of seed dispersal distances, but that turnover was too high at small scales and too low at large scales to be explained by seed dispersal alone (Condit et al. 2002 Science; Chave et al. 2002, Science).
In the last few years, I have joined forces with colleagues experienced in building mechanistic models of seed dispersal by wind to develop and validate such models for 50 wind-dispersed tree and liana species in Panama and to use the models to investigate the consequences of dispersal for recruitment at the individual, population and community levels. In this NSF-funded collaboration, I am taking the lead on investigating the ecological consequences of seed dispersal. Wind-dispersed species are a particularly interesting group to study because they face a three-way trade-off between fecundity, dispersal, and establishment governed by diaspore size and the proportional allocation within the diaspore to dispersal structures vs. the seed itself. I will analyze the relative roles of these factors through population-level simulations combining the validated mechanistic models of seed rain with habitat-specific and density-dependent effects on seedling establishment quantified from field studies. I will investigate whether dispersal-related trade-offs stabilize coexistence of wind-dispersed species on BCI through analyses of trait differences among species and simulations of their demographic consequences.
I am especially excited about this wind dispersal research because I believe it offers an unprecedented opportunity to quantify the contribution of competition-colonization trade-offs to diversity maintenance in tropical forests. In a review I recently wrote, I show that empirical data available in tropical forests (and most other plant communities) at this time are insufficient to establish that such trade-offs are anything more than an equalizing force (sensu Chesson 2000) in plant communities (Muller-Landau, in press, Tropical Forest Community Ecology book chapter). The proposed research on seed dispersal by wind offers the possibility of truly testing whether the trade-offs are a stabilizing force as well, and thus whether they might contribute meaningfully to tropical tree species diversity.
Related Publications
Chave, J., H. C. Muller-Landau, and S. A. Levin. 2002. Comparing classical community models: Theoretical consequences for patterns of diversity. American Naturalist 159:1-23.
Chave, J., H. C. Muller-Landau, R. Condit, N. Pitman, J. Terborgh, S. P. Hubbell, and E. G. Leigh. 2002. Beta-diversity in tropical forests - Response. Science 297: 1439a.
Condit, R., N. Pitman, E.G. Leigh, J. Chave, J. Terborgh, R. B. Foster, P. Núñez, S. Aguilar, R. Valencia, G. Villa, H. C. Muller-Landau, E. Losos, S. P. Hubbell. 2002. Beta-diversity in tropical forest trees. Science 295: 666-669.
Dalling, J., H. C. Muller-Landau, S. J. Wright, and S. P. Hubbell. 2002. Role of dispersal in the recruitment limitation of Neotropical pioneer species. Journal of Ecology 90:714-727.
Levin, S. A. and H. C. Muller-Landau. 2000. The evolution of dispersal and seed size in plant communities. Evolutionary Ecology Research 2:409-435.
Levin, S. A. and H. C. Muller-Landau. 2000. The emergence of diversity in plant communities. Comptes Rendus de l’Académie des Sciencias, Sciencias de la Vie 323:129-139.
Levin, S., H. C. Muller-Landau, J. Chave, and R. Nathan. 2003. The ecology and evolution of dispersal: a theoretical perspective. Annual Review of Ecology and Systematics 34:575-604.
Muller-Landau, H.C. In press. Colonization-related tradeoffs in tropical forests and their role in the maintenance of plant species diversity. Tropical Forest Community Ecology. W. P. Carson and S. A. Schnitzer, editors. Blackwell Scientific.
Muller-Landau, H. C., and Hardesty, B. D. 2005. Seed dispersal of woody plants in tropical forests: concepts, examples, and future directions. Pages 267-309 in Biotic Interactions in the Tropics. D. Burslem, M. Pinard, and S. Hartley, editors. Cambridge: Cambridge University Press.
Muller-Landau, H. C., S. J. Wright, O. Calderón, S. P. Hubbell, and R. B. Foster. 2002. Assessing recruitment limitation: concepts, methods and examples for tropical forest trees. Pages 35-53 in Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. J. Levey, W. R. Silva and M. Galetti, editors. Oxfordshire, UK: CAB International.
Muller-Landau, H. C., S. A. Levin, and J. E. Keymer. 2003. Theoretical perspectives on the evolution of long-distance dispersal and the example of specialized pests. Ecology 84(8):1957-1967.
Muller-Landau, H. C., J. W. Dalling, K. E. Harms, S. J. Wright, R. Condit, S. P. Hubbell and R. B. Foster. 2004. Seed dispersal and density-dependent seed and seedling mortality in Trichilia tuberculata and Miconia argentea. Pages 340-362 in Forest Diversity and Dynamism: Findings from a Network of Large-Scale Tropical Forest Plots. E. C. Losos and E. G. Leigh, editors. Chicago: University of Chicago Press.
Muller-Landau, H. C., S. J. Wright, J. K. Zimmerman, Y. Y. Chen, I. F. Sun, R. Condit, R. Foster, S. P. Hubbell, J. V. LaFrankie, S. J. Mazer, S. Noor, M. Silman, J. Thompson, R. Valencia, G. Villa. In press. Seed rain, seed production and seed dispersal in four tropical forests. Inside CTFS.
Nathan, R. and H. C. Muller-Landau. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology and Evolution 15:278-285.
Wright, S. J., H. C. Muller-Landau, O. Calderón, and A. Hernández. 2005. Annual and spatial variation in seedfall and seedling recruitment in a Neotropical forest. Putative mast seeding, seed fate, and El Niño climate fluctuation in a Neotropical forest. Ecology 86(4):848-860.
Specialized natural enemies – influences in theory and practice
Most tropical ecologists believe that one of the most important factors explaining the maintenance of high diversity among tropical trees is the Janzen-Connell effect – decreases in recruitment, growth and survival in areas of high conspecific density attributable to the actions of specialized, locally dispersing,natural enemies (seed predators, pathogens and herbivores). Numerous studies have tested for and found evidence for such density-dependence in tropical forests and other plant communities over the last thirty years (e.g., Muller-Landau et al. 2004, Forest Diversity book chapter; Wills et al. 2006 Science). However, these patterns could in principle also result from niche partitioning, and indeed, are often interpreted as such in temperate communities. Further, we have no way to quantitatively link measurable patterns of spatial density-dependence to contributions to population stabilization or diversity maintenance.
I’m currently conducting theoretical studies to investigate what characteristics of plant species and their natural enemies determine the strength of the population-stabilization and diversity-promoting effects. Using spatially-explicit simulation models and analytical approximations thereof, Fred Adler and I showed that the influences of specialized natural enemies on species coexistence depend critically on the dispersal distances of both plants and natural enemies (Adler & Muller-Landau 2005, Ecology Letters; Muller-Landau & Adler, in revision, Seed Dispersal book chapter). In a manuscript in preparation, we further demonstrate that the contribution of natural enemies to diversity maintenance is not correlated with any quantity measured in traditional field studies of Janzen-Connell effects (Muller-Landau and Adler, in preparation).
These theoretical insights have simulated me to initiate a series of new empirical studies designed to achieve a mechanistic understanding of natural enemy attack and consequent density-and distant-dependent patters of seed predation on the palm species Attalea butyracea in Panama. This study system has numerous advantages: the palm’s stony endocarps persist in the soil for years, and bear the recognizable marks of the fate of the seed inside (a bruchid beetle exit hole, a rodent-chewed hole, or an open germination pore); the bruchid beetle species involved are both large and easy to capture, mark, and rear in the lab; the palm’s crown has a regionally unique shape that allows it to be mapped over large areas from aerial photos; and the palm’s seed dispersal distances vary from long distances in well-protected forests to short distances in heavily poached forests, providing a “natural” experimental manipulation. I am currently conducting preliminary studies including mapping potential study sites and testing protocols in preparation for a larger research effort including a series of observational, experimental, and modeling studies to document and mechanistically explain local patterns of seed predation and their large-scale consequences for seedling recruitment rates in areas of high and low palm density and short and long palm seed dispersal distances.
I am also pursuing meta-analyses of existing datasets on spatial density-dependence with collaborators. Janneke HilleRisLambers and I are proposing an NCEAS working group to quantify and compare patterns of density-dependence at the seed and seedling stage across multiple temperate and tropical forests. By building on my theoretical work with Fred Adler, we hope to first establish the degree to which we can link variation in spatial density-dependence to variation in the underlying mechanism (e.g., movement distances of the natural enemy) and variation in the expected consequences for diversity maintenance. We will then use this theory to interpret interspecific and intersite variation in density-dependence. This variation is evident in recent work with Chris Wills involving analysis of density-dependence of sapling and adult survival in multiple tropical forests in the network coordinated by the Center for Tropical Forest Science (Wills et al. 2006, Science).
Related Publications
Adler, F. R. and H. C. Muller-Landau. 2005. When do localized natural enemies increase species richness? Ecology Letters 8 (4):438-447.
Muller-Landau, H.C. and F. R. Adler. In revision. How seed dispersal affects interactions with specialized natural enemies and their contribution to diversity maintenance. In: Seed Dispersal: Theory and its Application in a Changing World. R. G. Andrew Dennis, Eugene Schupp and David Westcott, editors. Wallingford: CABI Publishing.
Muller-Landau, H. C. and F. R. Adler. In preparation. Diversity-enhancing Janzen-Connell effects: what do our studies really tell us about their role in plant communities? For American Naturalist.
Wills, C., K. E. Harms, R. Condit, D. King, J. Thompson, F. He, H. Muller-Landau, P. Ashton, E. Losos, L. Comita, S. Hubbell, J. LaFrankie, S. Bunyavejchewin, H.S. Dattaraja, S. Davies, S. Esufali, R. Foster, I.A.U.N. Gunatilleke, C.V.S. Gunatilleke, P. Hall, A. Itoh, R. John, S. Kiratiprayoon, S. Loo de Lao, M. Massa, C. Nath, Md. N. S. Noor, A. Rahman Kassim, R. Sukumar, H. S. Suresh, I-F. Sun, S. Tan, T. Yamakura, J. Zimmerman. In press. Non-random processes contribute to the maintenance of diversity in tropical forests. Science.
Tree life history strategies, demographic rates, diversity, and forest structure
Tropical tree species vary widely in their life history strategies both within and among sites (Muller-Landau 2004, Biotropica; Chave et al. in press, Ecological Applications). While variation in some traits is correlated among species, there are several largely independent axis of variation including seed size, leaf size, mature height, and wood density (Ian Wright et al. in press, Annals of Botany). This trait variation among species is important in a number of respects: at the population level, it explains interspecific variation in demography, population structure, and dynamics; at the community level, it can contribute to niche partitioning and thus coexistence; and at the ecosystem level, the distribution of traits within a community affects virtually every whole-system metric including standing biomass and carbon fluxes.
I’m particularly interested in the relationship of functional traits to demography in tropical tree species – e.g., species with higher wood specific gravity have lower growth rates and lower mortality rates (Muller-Landau 2004 Biotropica). I am working with collaborators in Panama and at other sites throughout the Neotropics to collect and analyze data on species’ functional traits and demography (NCEAS working group and CTFS network). We have found consistent but weak relationships between functional traits and sapling and adult growth and mortality at multiple neotropical sites. Ben Gilbert, I and collaborators have also found that there is strong ontogenetic consistency in growth and mortality of tropical trees (Gilbert et al. 2006 Ecology). Thus, knowledge of functional traits may ultimately allow us to know quite a bit about a species’s complete demography. Further, because growth and mortality are inherently linked to size distributions at equilibrium, knowledge of one can provide information about the other in old-growth forests (Wright et al. 2003, Ecology).
Plant traits, demography and size distributions are interrelated not only for individual species, but also at the whole-forest level. In recent work with many collaborators from the Center for Tropical Forest Science’s worldwide network of tropical census plots, I have examined among-site variation in tree growth, mortality and diameter distributions in fourteen tropical forests. Contrary to the predictions of the theory of metabolic ecology, we found that there are no universal scaling relationships of tree growth, mortality or abundance with tree size. We developed a set of alternative predictions that retained some assumptions of metabolic ecology while also considering how availability of a key limiting resource, light, changes with tree diameter. Our predictions for growth and mortality, which incorporated empirical relationships for tree allometry and for vertical gradients in light availability were consistent with observed patterns (Muller-Landau et al. 2006a Ecology Letters). Starting from the general equilibrium relationships of growth, mortality and size distributions, I also analytically derived what size distributions follow from different combinations of growth and mortality functions, and exactly how the parameters of these size distributions are related to parameters of the growth and mortality functions. We found that empirical size distributions were very different from the predictions of metabolic ecology, and were consistent with the predictions of the equilibrium model (Muller-Landau et al. 2006b Ecology Letters). I’m currently working to develop mechanistic models to elucidate how various site and species characteristics ultimately influence forest demographic rates and size distributions. I believe a key factor driving similarities and differences among sites is the relative degree to which large individuals can monopolize resources versus the degree to which their abundance and resource monopolization are limited by other factors such as lethal disturbances and relatively more symmetric resource competition (Weiner et al. 2001, American Naturalist; Stoll et al. 2002, Proceedings Royal Society B).
Related Publications
Chave, J., H. C. Muller-Landau, T. R. Baker, T. A. Easdale, H. Ter Steege, and C. O. Webb. In press. Regional and phylogenetic variation in wood density among 2,456 neotropical tree species. Ecological Applications.
Gilbert, B.G., S.J. Wright, H.C. Muller-Landau, K. Kitajima, A. Hernandez. 2006. Life history trade-offs in tropical trees and lianas. Ecology 87:1281-1288.
Muller-Landau, H. C. 2004. Interspecific and intersite variation in wood specific gravity of tropical trees. Biotropica 36:20-32.
Muller-Landau, H. C., R. S. Condit, J. Chave, S. C. Thomas, S. A. Bohlman, S. Bunyavejchewin, S. Davies, R. Foster, S. Gunatilleke, N. Gunatilleke, K. E. Harms, T. Hart, S. P. Hubbell, A. Itoh, A. R. Kassim, J. V. LaFrankie, H. S. Lee, E. Losos, J.-R. Makana, T. Ohkubo, R. Sukumar, I.-F. Sun, N. Supardi M. N., S. Tan, J. Thompson, R. Valencia, G. Villa Muñoz, C. Wills, T. Yamakura, G. Chuyong, H. S. Dattaraja, S. Esufali, P. Hall, C. Hernandez, D. Kenfack, S. Kiratiprayoon, H. S. Suresh, D. Thomas, M. I. Vallejo, and P. Ashton. 2006a. Testing metabolic ecology theory for allometric scaling of tree size, growth, and mortality in tropical forests. Ecology Letters 9:575-588.
Muller-Landau, H. C., R. S. Condit, K. E. Harms, C. O. Marks, S. C. Thomas, S. Bunyavejchewin, G. Chuyong, L. Co, S. Davies, R. Foster, S. Gunatilleke, N. Gunatilleke, T. Hart, S. P. Hubbell, A. Itoh, A. R. Kassim, D. Kenfack, J. V. LaFrankie, D. Lagunzad, H. S. Lee, E. Losos, J.-R. Makana, T. Ohkubo, C. Samper, R. Sukumar, I.-F. Sun, N. Supardi M. N., S. Tan, D. Thomas, J. Thompson, R. Valencia, M. I. Vallejo, G. Villa Muñoz, T. Yamakura, J. K. Zimmerman, H. S. Dattaraja, S. Esufali, P. Hall, F. He, C. Hernandez, S. Kiratiprayoon, H. S. Suresh, C. Wills, and P. Ashton. 2006b. Comparing tropical forest tree size distributions with the predictions of metabolic ecology and equilibrium models. Ecology Letters 9:589-602.
Stoll, P., J. Weiner, H. Muller-Landau, E. Müller and T. Hara. 2002. Size symmetry of competition alters biomass-density relations. Proceedings of the Royal Society Biological Sciences Series B 269:2191-2195.
Weiner, J., P. Stoll, H. C. Muller-Landau, and A. Jasentuliyana. 2001. The effects of density, spatial pattern and competitive symmetry on size variation in simulated plant populations. American Naturalist 158:438-450.
Wright, I. J. D. D. Ackerly, F. Bongers, K. E. Harms, G. Ibarra-Manriquez, M. Martinez-Ramos, S. J. Mazer, H. C. Muller-Landau, H. Paz, N. C. A. Pitman, L. Poorter, M. R. Silman, C. F. Vriesendorp, C. O. Webb, M. Westoby, S. J. Wright. In press. Relationships among key dimensions of plant trait variation in seven Neotropical forests. Annals of Botany.
Wright, S. J., H. C. Muller-Landau, R. Condit, and S. P. Hubbell. 2003. Gap-dependent recruitment, realized vital rates, and size distributions of tropical trees. Ecology 84:3174-3185.
The future of tropical forests
Tropical forests today are subjected to an array of novel anthropogenic influences whose ultimate consequences are yet unknown. Joe Wright and I recently completed a worldwide analysis of the most obvious influence – deforestation. We concluded that total losses of tropical forest area are likely to be much lower than commonly feared. However, the tropical forests of the future, while still extensive in area, will be largely secondary or degraded – by selective logging, hunting, and effects of climate change, nitrogen deposition, and other global anthropogenic influences (Wright and Muller-Landau 2006, Biotropica and Wright and Muller-Landau in press, Biotropica).
Understanding the impacts of these less obvious anthropogenic influences on tropical forests is a major challenge in both basic and applied ecology. I’m currently working together with graduate student Noelle Beckman, to investigate the effects of defaunation (due to hunting) on seedling recruitment of multiple tree species. Depending on their life history strategies and traits, plant species vary widely in how and with which animals they interact, and thus changes in animal communities will differentially affect plant species. Noelle is investigating how defaunation is differentially impacting seed dispersal and seed predation of tropical tree species varying in seed size (Beckman and Muller-Landau in review, Biotropica. We hypothesized that seed size is a key character because it is correlated with the mode of seed dispersal and susceptibility to vertebrate seed predation and pathogen attack – and also with the degree of shade tolerance, growth and mortality. Thus, shifts in the relative abundances of species with different seed sizes are both likely to occur and likely to have important implications for forest diversity, dynamics, and structure.
Related Publications
Beckman, N. and H. C. Muller-Landau. In review. Differential effects of hunting on pre-dispersal seed predation, primary dispersal and secondary seed removal of two tropical tree species. Biotropica.
Wright, S. J. and H. C. Muller-Landau. 2006. The future of tropical forest species. Biotropica 38(3):287-301.
Wright, S. J., and H. C. Muller-Landau. In press. The uncertain future of tropical forest species (response to Brook et al.). Biotropica.