Tropical tree species assemblages in topographical ... - BES journal

Journal of Ecology 2011, 99, 1441–1452

doi: 10.1111/j.1365-2745.2011.01878.x

Tropical tree species assemblages in topographical habitats change in time and with life stage Rajapandian Kanagaraj1*, Thorsten Wiegand1, Liza S. Comita2,3 and Andreas Huth1 1

Department of Ecological Modelling, UFZ Helmholtz Centre for Environmental Research – UFZ, Permoserstreet 15, D-04318 Leipzig, Germany; 2National Center for Ecological Analysis and Synthesis, 735 State Street, Suite 300, Santa Barbara, CA 93101, USA; and 3Smithsonian Tropical Research Institute, Box 0843-03092, Balboa Ancoń, Republic of Panama´

Summary 1. Recent studies have documented shifts in habitat associations of single tropical tree species from one life stage to the next. However, the community-level consequences of such shifts have not been investigated, and it is not clear whether they would amplify, neutralize or completely alter habitat structuring during the transitions to the adult community. 2. We compared habitat-driven species assemblages at three life stages (i.e. recruitment, juvenile and reproductive stages) and six censuses for tree and shrub species in a fully censused 50-ha plot of Panamanian lowland forest. Habitat types were determined using multivariate regression trees that group areas with similar species composition (i.e. species assemblages) according to their topographical characteristics. 3. Three topographical variables (a topographical wetness index, slope and elevation) were major determinants of species assemblages. When analysing individuals of all life stages together, we found a distinct and temporally consistent structuring of the plot into four dominant habitat types (low and high plateaus, slope and swamp) which was consistent with previous classifications. Basically, the same habitat structuring emerged for the juvenile communities of individual censuses. However, recruits showed a weak and temporally inconsistent habitat structuring. 4. A notable homogenization in species assemblages occurred during the transition from juvenile to reproductive, through both a reduction in the number of species assemblages (in 3 censuses, one large reproductive assemblage covered 93% of the plot, and in others, an additional slope habitat emerged) and a reduction in the classification error. Overall, habitat structuring became noisier and weaker over the 25 years of the study. 5. Synthesis. Our results suggest that mortality processes during the transition from recruits to juveniles must enhance the signal of habitat structuring. However, during the transition to the reproductive stage, species may have lost the advantage of being in the habitat with which they had become associated, or the quality of habitat changed during their life span because of larger climatic changes. The homogeneous assemblages of the reproductive stage could be interpreted as support for neutral theories, but further research is required to unravel the mechanisms behind these intriguing observations. Key-words: environmental heterogeneity, habitat preference, multivariate regression tree analysis, plant population and community dynamics, regeneration niche, species assemblages, topography, tropical forest diversity

Introduction Niche differentiation has been put forth as an explanation for the maintenance of local diversity in multispecies communities (Ashton 1969; Tilman 1982). According to niche theory, spe*Correspondence author. E-mail: [email protected]

cies can coexist if they perform best under different abiotic conditions. If abiotic conditions, such as soil attributes or topography, are spatially structured, their structure will be reflected in species distributions through species–habitat associations at the individual species level (Whittaker 1956). As a consequence, different species assemblages should form at the community level within habitat types. However, habitat

2011 The Authors. Journal of Ecology 2011 British Ecological Society

1442 R. Kanagaraj et al. partitioning in many species-rich (plant) communities may not provide separate niches for hundreds of plant species as required by classical coexistence theory (Valencia et al. 2004), because plants depend on and compete for the same few of resources and acquire them in similar ways (Daws et al. 2002; Silvertown 2004; Comita, Condit & Hubbell 2007). One hypothesis to solve this conundrum is the unified neutral theory (Hubbell 2001), which focuses on adult plants and assumes no niche differences. An alternative hypothesis in the niche context is that coexistence is possible through the partitioning of the ‘regeneration niche’ (Grubb 1977; Tilman 1982). During early life stages, trees may experience their environment as more heterogeneous, e.g. in terms of light availability related to canopy gaps (Ricklefs 1977) or other physical factors, such as soil moisture (Daws et al. 2002; Engelbrecht et al. 2007; Comita & Engelbrecht 2009) or nutrients (John et al. 2007). In addition, previous studies have found that habitat associations of single tropical tree species typically do not form at early life stages (i.e. seed germination and seedling establishment) and that species often show different ecological habitat associations across life stages (Webb & Peart 2000; Paoli, Curran & Zak 2006; Comita, Condit & Hubbell 2007; Lai et al. 2009). Thus, it is not clear whether adult plants conserve a signal of habitat association that they acquired during early life stages or whether shifts in a species’ ecological preferences occur from one life stage to the next. On the community level, the latter may neutralize habitat structuring for adults or generate a habitat structuring different from that of the recruits and juveniles. However, this issue is complicated by the fact that habitat suitability for a given species at a given location may not be static, but could shift in response to long-term variations in climatic conditions or extreme disturbance events such as severe El Ninõ droughts (Condit, Hubbell & Foster 1995). Thus, when looking from the community level, emerging species assemblages associated with certain habitat types may not only shift with life stage but also in time because of supra-annual variability in climatic conditions. An important driver of habitat diversification is topography, which is a first-order control on spatial variation of hydrological conditions that affect the spatial distribution of soil moisture (Harms et al. 2001; Daws et al. 2002; Sørensen, Zinko & Seibert 2006) and nutrients (John et al. 2007), which are crucial for plants. Previous studies conducted at large fully censused tropical forest plots have investigated topographical habitat associations at the level of individual species (e.g. Harms et al. 2001; Gunatilleke et al. 2006; Svenning, Normand & Skov 2006; Comita, Condit & Hubbell 2007; Lai et al. 2009). However, because of sample size limitations, these studies were restricted to the most common species in the community. Here we take a different approach to look at habitat associations. Instead of focusing on individual species–habitat associations, we focus on detection of habitat-driven species assemblages and how they might change with age or size class and through time. The advantage of this approach over individual species associations is that it focuses on the broader picture and allows inclusion of data from all species and not only from more abundant species. This may be particularly

important for understanding habitat partitioning in diverse communities, because rare species, which are typically excluded from individual species–habitat association tests, may be rare because they are habitat specialists. In this study, we assess habitat associations at the community level using multivariate regression tree analysis that groups areas with similar species composition according to their topographical characteristics, thereby defining different habitat types (De’ath 2002; Legendre et al. 2009). We ask whether emerging habitat types and topographical determinants were consistent in time (i.e. census) and with life stage (i.e. recruitment, juvenile and reproductive stages). For this purpose, we use data on tree and shrub species from six censuses conducted in the Barro Colorado Island (BCI) 50-ha Forest Dynamics Plot (FDP), Panama (Fig. 1). Previous species-level studies of seedling and tree stages in the BCI plot found that many species were positively associated with one or more habitats and appeared to exhibit different ecological habitat preferences at the smaller and larger stages (Harms et al. 2001; Comita, Condit & Hubbell 2007). Here we ask whether and how such developmental changes in habitat associations translate into the emergence of local species assemblages at different life stages, and which environmental variables structure the habitats that host different species assemblages. In addition, we use the data from repeated censuses of the BCI plot to assess the consistency of these patterns over time in the light of interannual climatic variation. Given that topographical variation at BCI is not very large, we expect a noisy answer, but the questions of whether different development stages produce the same habitat structuring and whether that is temporally consistent are intriguing. For example, under the regeneration niche hypothesis, we would expect recruitment and juvenile stages to show strong habitat structuring. If neutral theory were true, the adult community should basically form one large species assemblage. Our special interest is to identify the critical life stage transition where the emergent species assemblages change and to explore the role of long-term changes in precipitation regime or disturbances, such as El Ninõ Southern Oscillation (ENSO) events.

Fig. 1. The 50-ha Forest Dynamics Plot of Barro Colorado Island (BCI), Panama, shown with elevation contour lines at 5-m interval (ranging from 120 to 155 m above mean sea level) and a habitat classification after Harms et al. (2001) with the topographically defined habitats high plateau (0.35) Ten slope indicator species were also indicator species for recruits. The three species Chrysochlamys eclipse, Ocotea whitei and Trophis caucana, which were indentified as indicator species for reproductive individuals, were also indicator species for juveniles and two of them also for recruits (Table S7). Swamp Of 51 indicator species of recruits, 24 were found also in the juvenile stage, but only seven species were found both in juvenile and in reproductive stages with Bactris major, Elaeis oleifera and Cassipourea elliptica having the highest indicator value (>0.25; Table S7). Of the 34 indicator species of juveniles, 23 were also indicator species of recruits.

(e.g. Harms et al. 2001; Gunatilleke et al. 2006; Svenning, Normand & Skov 2006; Comita, Condit & Hubbell 2007; Lai et al. 2009). This allowed us to concentrate on emergent, higher-level structures that consider the entire community, including rare species. Using multivariate regression tree analysis, we assessed whether the BCI plot exhibited topographical habitat types (defined by its associated species assemblages) that were consistent across life stages and among censuses. When analysing the entire communities (i.e. individuals of all life stages together), we found a distinct and temporally consistent structuring of the plot into four dominant habitat types (swamp, slope, low plateau and high plateau). Similar habitat structuring emerged for the juvenile communities of individual censuses and the 1990 recruit census. However, recruits showed a weak and temporally inconsistent habitat structuring and yielded models with low predictive accuracy. Thus, recruit species assemblages were statistically detectable but not very much pronounced. Surprisingly, the distinct species assemblages observed for juveniles disappeared almost completely for reproductive individuals. Instead, for half of the censuses reproductive individuals formed one large assemblage that covered 93% of the plot, and in the other censuses, a second major habitat type (occupying 20 indicator species. Nonetheless, the number of indicator species for different habitat types at the recruit and juvenile stages was always higher than that at the reproductive stage (Fig. 4).

Number of indicator species

50

Recruit Juvenile Reproductive

40

30

20

Conclusions Our analysis of habitat-defined species assemblages of tropical tree species suggests that complex changes in species assemblages occur in time and with life stage. Recruits showed a weak and temporally inconsistent habitat structuring, whereas distinct and temporally consistent habitat types (low and high plateaus, slope and swamp) emerged for juveniles. However, a notable homogenization occurred during the transition to the reproductive stage, through both a reduction in the number of species assemblages and a reduction in the classification error of the regression tree analysis. The homogenization in the emerging species assemblages of reproductive individuals suggests that species may have lost the advantage of being in the habitat with which they had become associated as juveniles, or habitat quality changed during their life span. While the weak habitat structuring of the reproductive community agrees with predictions of neutral theories, further research is required to unravel the possibly non-neutral mechanisms behind the intriguing homogenization at the transition from juvenile to reproductive. Our results re-emphasize the need for studies to examine species’ habitat preferences at multiple life stages (Comita, Condit & Hubbell 2007). Comparative studies in other tropical forest plots are required to find out whether our results reflect site idiosyncrasies of the BCI plot, which shows relatively weak habitat associations, or general trends.

10

Acknowledgements 0 High plateau

Low plateau

High-Low plateaus

Slope

Swamp

Habitat type

Fig. 4. Number of indicator species identified for each of four habitat types at recruit, juvenile and reproductive stages in the Barro Colorado Island 50-ha Forest Dynamics Plot, Panama.

The BCI forest dynamics research project was made possible by National Science Foundation grants to Stephen P. Hubbell, support from the Center for Tropical Forest Science, the Smithsonian Tropical Research Institute, the John D. and Catherine T. MacArthur Foundation, the Mellon Foundation, the Celera Foundation, and numerous private individuals, and through the hard work of over 100 people from 10 countries over the past two decades. The plot project is part the Center for Tropical Forest Science, a global network of

2011 The Authors. Journal of Ecology 2011 British Ecological Society, Journal of Ecology, 99, 1441–1452

Habitat-driven tree species assemblages 1451 large-scale demographic tree plots. R.K and A.H were supported by the ERC advanced grant 233066 to T.W. L.S.C acknowledges the support of a postdoctoral fellowship from the National Center for Ecological Analysis and Synthesis, a Center funded by U.S. NSF (Grant #EF-0553768), the University of California, Santa Barbara, and the State of California. Two anonymous reviewers provided helpful suggestions for improving the manuscript.

References Ashton, P.S. (1969) Speciation among tropical forest trees: some deductions in the light of recent evidence. Biological Journal of the Linnean Society, 1, 155–196. Becker, P., Rabenold, P.E., Idol, J.R. & Smith, A.P. (1988) Water potential gradients for gaps and slopes in a Panamanian tropical moist forest’s dry season. Journal of Tropical Ecology, 4, 173–184. Breiman, L., Friedman, J., Stone, C.J. & Olshen, R.A. (1998) Classification and Regression Trees, 3rd edn. pp. 372, CRC Press, Boca Raton, FL. Comita, L.S., Condit, R. & Hubbell, S.P. (2007) Developmental changes in habitat associations of tropical trees. Journal of Ecology, 95, 482–492. Comita, L.S. & Engelbrecht, B.M.J. (2009) Seasonal and spatial variation in water availability drive habitat associations in a tropical forest. Ecology, 90, 2755–2765. Condit, R. (1998) Tropical Forest Census Plots. Springer-Verlag, Berlin. Condit, R., Hubbell, S.P. & Foster, R.B. (1994) Density dependence in two understory tree species in a neotropical forest. Ecology, 75, 671–680. Condit, R., Hubbell, S.P. & Foster, R.B. (1995) Mortality rates of 205 neotropical tree species and the responses to a severe drought. Ecological Monographs, 65, 419–439. Condit, R., Hubbell, S.P. & Foster, R.B. (1996a) Assessing the response of plant functional types in tropical forests to climatic change. Journal of Vegetation Science, 7, 405–416. Condit, R., Hubbell, S.P. & Foster, R.B. (1996b) Changes in a tropical forest with a shifting climate, results from a 50 hectare permanent census plot at Barro Colorado Island in Panama. Journal of Tropical Ecology, 12, 231–256. Croat, T.B. (1978) Flora of Barro Colorado Island. Stanford University Press, Stanford, CA. Daws, M.I., Mullins, C.E., Burslem, D.F.R.P., Paton, S.R. & Dalling, J.W. (2002) Topographic position affects the water regime in a semideciduous tropical forest in Panama. Plant and Soil, 238, 79–90. De’ath, G. (2002) Multivariate regression trees: a new technique for modeling species–environment relationships. Ecology, 83, 1105–1117. De’ath, G. (2006) mvpart: Multivariate Partitioning. R Package Version 1.2–4. [http://cran.r-project.org/i]. Dennis, A.J., Lipsett-Moore, G.J., Harrington, G.N., Collins, E.A. & Westcott, D.A. (2005) Seed predation, seed dispersal and habitat fragmentation: does context make a difference in tropical Australia? Seed Fate: Predation, Dispersal and Seedling Establishment (eds P.M. Forget, J.E. Lambert, P.E. Hulme & S.B. Vander Wall). pp. 117–136, CABI Publishing, Wallingford. Donovan, L.A. & Ehleringer, J.R. (1992) Contrasting water-use patterns among size and life-history classes of a semi-arid shrub. Functional Ecology, 6, 482–488. Dufreˆne, M. & Legendre, P. (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs, 67, 345–366. Engelbrecht, B.M.J., Comita, L.S., Condit, R., Kursar, T.A., Tyree, M.T., Turner, B.L. et al. (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature, 447, 80–82. Faith, D.P., Minchin, P.R. & Belbin, L. (1987) Compositional dissimilarity as a robust measure of ecological distance. Vegetatio, 69, 57–68. Grubb, P.J. (1977) Maintenance of species-richness in plant communities – importance of regeneration niche. Biology Reviews of the Cambridge Philosophical Society, 52, 107–145. Gunatilleke, C.V.S., Gunatilleke, I.A.U.N., Esufali, S., Harms, K.E., Ashton, P.M.S., Burslem, D.F.R.P. et al. (2006) Species–habitat associations in a Sri Lankan dipterocarp forest. Journal of Tropical Ecology, 22, 371–384. Harms, K.E., Condit, R., Hubbell, S.P. & Foster, R.B. (2001) Habitat associations of trees and shrubs in a 50-ha neotropical forest plot. Journal of Ecology, 89, 947–959. Hubbell, S.P. (1979) Tree dispersion, abundance, and diversity in a tropical dry forest. Science, 203, 1299–1309. Hubbell, S.P. (2001) The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press, Princeton. Hubbell, S.P., Condit, R. & Foster, R.B. (2005) Barro Colorado Forest Census Plot Data [http://ctfs.si.edu/datasets/bci].

Hubbell, S.P. & Foster, R.B. (1983) Diversity of canopy trees in a neotropical forest and implications for conservation. Tropical Rain Forest: Ecology and Management (eds S.L. Sutton, T.C. Whitmore & A.C. Chadwick). pp. 25–41, Blackwell Scientific, Oxford. Hubbell, S.P. & Foster, R.B. (1986) Commonness and rarity in a neotropical forest: implications for tropical tree conservation. Conservation Biology: the Science of Scarcity and Diversity (ed. M. Soule). pp. 205–231, Sinauer Associates, Sunderland, MA. John, R., Dalling, J.W., Harms, K.E., Yavitt, J.B., Stallard, R.F., Mirabello, M. et al. (2007) Soil nutrients influence spatial distributions of tropical tree species. Proceedings of the National Academy of Sciences (USA), 104, 864– 869. Lai, J.S., Mi, X.C., Ren, H.B. & Ma, K.P. (2009) Species-habitat associations change in a subtropical forest of China. Journal of Vegetation Science, 20, 415–423. Larsen, D.R. & Speckman, P.L. (2004) Multivariate regression trees for analysis of abundance data. Biometrics, 60, 543–549. Legendre, P., Mi, X., Ren, H., Ma, K., Yu, M., Sun, I. et al. (2009) Partitioning beta diversity in a subtropical broad-leaved forest of China. Ecology, 90, 663–674. Leigh, E.G.J. (1999) Tropical Forest Ecology: A View from Barro Colorado Island. Oxford University Press, Oxford. Leigh, E.G.J., Rand, S.A. & Windsor, D.M. (1982) The Ecology of a Tropical Forest: Seasonal Rhythms and Long-Term Changes. Smithsonian Institution Press, Washington, DC. Leigh, E.G.J., Lao, S., Condit, R., Hubbell, S.P., Foster, R.B. & Perez, R. (2004) Barro Colorado Island forest dynamics plot, Panama. Tropical Forest Diversity and Dynamism: Findings from a Large-Scale Plot Network (eds E. Losos & E.G.J. Leigh). pp. 451–463, University of Chicago Press, Chicago. Losos, E. & Leigh, E.G.J. (2004) Tropical Forest Diversity and Dynamism: Findings from a Large-Scale Plot Network. University of Chicago Press, Chicago. Lusk, C.H. (2004) Leaf area and growth of juvenile temperate evergreens in low light: species of contrasting shade tolerance change rank during ontogeny. Functional Ecology, 18, 820–828. Paoli, G.D., Curran, L.M. & Zak, D.R. (2006) Soil nutrients and beta diversity in the Bornean Dipterocarpaceae: evidence for niche partitioning by tropical rain forest trees. Journal of Ecology, 94, 157–170. Poorter, L., Bongers, F., Sterck, F.J. & Woll, H. (2005) Beyond the regeneration phase: differentiation of height–light trajectories among tropical tree species. Journal of Ecology, 93, 256–267. R Development Core Team. (2007) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. [http://www.R-project.orgi] Ribbens, E., Pacala, S.W. & Silander, J.A. (1994) Recruitment in forests: calibrating models to predict patterns of tree seedling dispersal. Ecology, 75, 1794–1806. Ricklefs, R.E. (1977) Environmental heterogeneity and plant species diversity: a hypothesis. American Naturalist, 111, 376–381. Roberts, D.W. (2006) labdsv: Laboratory for Dynamic Synthetic Vegephenomenology. R Package Version 1.2–2. [http://cran.r-project.org/i]. Schupp, E.W. (1992) The Janzen-Connell model for tropical tree diversity: population implications and importance of spatial scale. American Naturalist, 140, 526–530. Silvertown, J. (2004) Plant coexistence and the niche. Trends in Ecology and Evolution, 19, 605–611. Sørensen, R., Zinko, U. & Seibert, J. (2006) On the calculation of the topographic wetness index: evaluation of different methods based on field observations. Hydrology and Earth System Sciences, 10, 101–112. Svenning, J.C., Normand, S. & Skov, F. (2006) Range filling in European trees. Journal of Biogeography, 33, 2018–2021. Tarboton, D.G. (1997) A new method for determination of flow directions and upslope areas in grid digital elevation models. Water Resource Research, 33, 309–319. Tilman, D. (1982) Resource Competition and Community Structure. Princeton University Press, Princeton, NJ. Valencia, R., Foster, R.B., Villa, G., Condit, R., Svenning, J.C., Hernandez, C. et al. (2004) Tree species distributions and local habitat variation in the Amazon: a large plot in eastern Ecuador. Journal of Ecology, 92, 214–229. Webb, C.O. & Peart, D.R. (1999) Seedling density dependence promotes coexistence of Bornean rain forest trees. Ecology, 80, 2006–2017. Webb, C.O. & Peart, D.R. (2000) Habitat associations of trees and seedlings in a Bornean rain forest. Journal of Ecology, 88, 464–478. Whittaker, R.J. (1956) Vegetation of the Great Smoky Mountains. Ecological Monographs, 26, 1–80.


1452 R. Kanagaraj et al. Windsor, D.M. (1990) Climate and Moisture Variability in a Tropical Forest: Long-term Records from Barro Colorado Island, Panama´. Vol. 29, Smithsonian Institution, Washington, DC. Wright, S.J. (2005) The El Ninõ Southern Oscillation influences tree performance in tropical rainforests. Tropical Rainforests: Past, Present, and Future (eds E. Bermingham, C.W. Dick & C. Moritz). pp. 295–310, University of Chicago Press, Chicago and London. Wright, S.J., Carrasco, C., Calderon, O. & Paton, S. (1999) The El Ninõ Southern Oscillation, variable fruit production, and famine in a tropical forest. Ecology, 80, 1632–1647. Zimmerman, J.K., Wright, S.J., Calderoń, O., Pagan, M.A. & Paton, S. (2007) Flowering and fruiting phenologies of seasonal and aseasonal neotropical forests: the role of annual changes in irradiance. Journal of Tropical Ecology, 23, 231–251. Received 22 December 2010; accepted 7 July 2011 Handling Editor: Thomas Kitzberger

Table S4. Fate of juveniles from different censuses. Table S5. Summary of all MRT analyses based on the life stage classification. Table S6. Summary of all MRT analyses based on the size classification. Table S7. Indicator species for the different habitat types and pooled censuses. Table S8. The indicator species for the different habitat types, censuses and life stages. Figure S1. Maps of the environmental variables used in the analyses.

Supporting Information Additional supporting information may be found in the online version of this article:

Figure S2. Results of the MRT analysis for individual censuses based on size classes. Figure S3. Examples for resulting regression trees.

Appendix S1. Calculation of biotic variables. Table S1. Sample sizes and error of MRT analyses based on the life stage classification. Table S2. Sample sizes and error of MRT analyses based on the size classification.

As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.

Table S3. Fate of recruits from different censuses.
