Letters

approaches to scientic review, such as economic-based and open-access commenting models (http://www.nature. com/nature/peerreview/debate/; [4,5]). We feel that the benets of review recycling far outweigh its limitations, and we hope that it becomes as commonplace in scientic publication and grant writing as are the three Rs in natural resource conservation.
Acknowledgements
We thank the Rohr laboratory, Earl McCoy and Peter Stiling for feedback on this paper. Funds were provided by grants from the US Department of Agriculture (NRI 2009-35102-0543) and the US Environmental Protection Agency (STAR R833835) to J.R.R. and the National Science Foundation (IOS 0920475) to L.B.M.

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References
1 Hochberg, M.E. et al. (2009) The tragedy of the reviewer commons. Ecol. Lett. 12, 24 2 McPeek, M.A. et al. (2009) The golden rule of reviewing. Am. Nat. 173, E155E158 3 Statzner, B. and Resh, V.H. (2010) Negative changes in the scientic publication process in ecology: potential causes and consequences. Freshwater Biol. 55, 26392653 4 Hauser, M. and Fehr, E. (2007) An incentive solution to the peer review problem. PLoS Biol. 5, 703 5 Fox, J. and Petchey, O.L. (2010) Pubcreds: xing the peer review process by privatizing the reviewer commons. Bull. Ecol. Soc. Am. 325333

0169-5347/$ see front matter 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2012.01.012 Trends in Ecology and Evolution, April 2012, Vol. 27, No. 4

Tropical forest warming: looking backwards for more insights

Pieter A. Zuidema1, Roel J.W. Brienen2 and Jochen Schongart3,4
1

Forest Ecology and Forest Management, Centre for Ecosystem Studies, Wageningen University, PO Box 47, 6700 AA Wageningen, Netherlands 2 School of Geography, Leeds University, Woodhouse Lane, Leeds LS2 9JT, UK 3 Max-Planck-Institute for Chemistry, Biogeochemistry Department, P.O. Box 3060, 55020 Mainz, Germany 4 Instituto Nacional de Pesquisas da Amazonia (INPA), Av. Andre Araujo 2936, P.O. Box 478, 69011-970 Manaus-AM, Brazil

In his balanced and much-needed review on the effects of global warming on tropical rainforests, Richard Corlett [1] discussed gaps in knowledge, research needs and corresponding research methods. However, an important and powerful technique for studying the effects of climate change on tropical forests was not mentioned: the analysis of tree rings. Among others, Corlett recommended an increase in the duration of permanent sample plot (PSP) studies and the frequency of re-measurements in those plots. Although PSP studies have been crucial in quantifying increased biomass and elevated dynamics of tropical forests, they have not provided much clarity on the drivers of these changes since the rst reports in the 1990s [2,3]. Undoubtedly, intensication and extension of PSP studies will improve correlations between climatic variations and tree dynamics, but improvements will be slow as time series are extended at the pace of annual (or less frequent) plot re-measurements. The only way to extend time series more rapidly is to look backwards. Tree ring analysis allows this approach by reconstructing annual growth rates over the full lifetime of trees, easily spanning more than a century. Tree ring research in the tropics is not new [4], but its wide application has been hampered by the common belief that tropical forest trees do not produce annual rings. Fortunately, tropical dendrochronology has developed rapidly over the last decade and has revealed that many tree species do form such rings (Figure 1) [4,5]. A quick scan of published studies revealed that annual ring formation has
Corresponding author: Zuidema, P.A. (pieter.zuidema@wur.nl).

now been proven for almost 70 species from tropical lowland rainforests (18004200 mm of rain per year), as listed in Table S1 in the supplementary material online. For these species, the annual character of ring formation was proven using methods that included cambial wounding, radiocarbon (14C) dating, climategrowth relationships and validation of ring counts for trees of a known age. We expect this species list to increase rapidly in the coming years, given that annual ring formation in many more species is currently being tested.

TRENDS in Ecology & Evolution

Figure 1. Example of annual rings in tropical cedar (Cedrela odorata), an Amazonian humid forest species that reaches more than 200 years in age. Photo by RJW Brienen.

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Tree ring studies are highly suitable for evaluating the climate sensitivity of tropical tree growth: they yield accurate measurements of diameter increment, directly reveal the lifetime growth history of trees, and allow additional measurements of stable isotope fractions. Tree ring research in temperate forests has generated important insights into tree responses to temperature, rainfall, solar radiation and other climatic variables. Using the same set of established techniques, tropical tree ring studies have shown sensitivity of tree growth to rainfall [6], air tempera ture [7], El Nino indices [8] and anomalies in sea surface temperature [9] (Table S1 in the supplementary material online). Such climategrowth analyses can be used to project potential tree responses under climate change scenarios [9]. Thus, tree ring data can provide a vital input for the rigorous, quantitative, long-term (multi-decadal) monitoring that Corlett recommends. In addition, tree ring studies can be used to evaluate whether the growth increase observed in PSPs [3] can be corroborated for longer periods. Such long-term growth increases have been observed for several Amazonian species [10], but not in Asian species [11], and are consistent with an expected positive response to increased atmospheric CO2-pressure or nutrient supply. Clarity about the (physiological) causes of growth increases can be obtained by analyzing stable isotopes of carbon (d13C; revealing changes in water-use-efciency [11]) and nitrogen (d15N; revealing changes in nitrogen cycling [12]). Tropical tree ring studies are a valuable addition to PSP-based approaches in evaluating tropical forest sensitivity to climatic changes. These two research techniques provide complementary information. PSPs deliver rates of recruitment, mortality and growth for all species over relatively short periods and at low temporal resolution. Tree ring analyses yield lifetime growth rates and physiological responses to environmental changes for a subset of species, over long periods and at annual resolution. Ideally, both approaches should be combined at the same or nearby sites. We conclude that tree ring research is already contributing to fullling the research needs formulated by Corlett to better understand climate change effects on tropical forests and will increasingly do so in the future.

Trends in Ecology and Evolution April 2012, Vol. 27, No. 4

Acknowledgements
P.A.Z. acknowledges support by the European Research Council (ERC grant #242955); R.J.W.B. was supported by the Gordon and Betty Moore Foundation. We thank William Laurance for comments on a draft version.

Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.tree.2011. 12.007.
References
1 Corlett, R.T. (2011) Impacts of warming on tropical lowland rainforests. Trends Ecol. Evol. 26, 606613 2 Phillips, O.L. et al. (1998) Changes in the carbon balance of tropical forest: evidence from long-term plots. Science 282, 439442 3 Lewis, S.L. et al. (2009) Changing ecology of tropical forests: evidence and drivers. Annu. Rev. Ecol. Syst. 40, 529549 4 Worbes, M. (2002) One hundred years of tree-ring research in the tropics a brief history and an outlook to future challenges. Dendrochronologia 20, 217231 5 Rozendaal, D.M.A. and Zuidema, P.A. (2011) Dendroecology in the tropics: a review. Trees Struct. Funct. 25, 316 6 Brienen, R.J.W. and Zuidema, P.A. (2005) Relating tree growth to rainfall in Bolivian rain forests: a test for six species using tree ring analysis. Oecologia 146, 112 7 Devall, M.S. et al. (1995) Dendroecological analysis of Cordia alliodora, Pseudobombax septenatum and Annona spraguei in central Panama. IAWA J. 16, 411424 ngart, J. et al. (2004) Teleconnection between tree growth in the 8 Scho Amazonian oodplains and the El NinoSouthern Oscillation effect. Global Change Biol. 10, 683692 9 Brienen, R.J.W. et al. (2010) Climate-growth analysis for a Mexican dry forest tree shows strong impact of sea surface temperatures and predicts future growth declines. Global Change Biol. 16, 2001 2012 10 Rozendaal, D.M.A. et al. (2010) Tropical tree rings reveal preferential survival of fast-growing juveniles and increased juvenile growth rates over time. New Phytol. 185, 759769 11 Nock, C.A. et al. (2011) Long-term increases in intrinsic water-use efciency do not lead to increased stem growth in a tropical monsoon forest in western Thailand. Global Change Biol. 17, 10491063 12 Hietz, P. et al. (2011) Long-term change in the nitrogen cycle of tropical forests. Science 334, 664666

0169-5347/$ see front matter 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2011.12.007 Trends in Ecology and Evolution, April 2012, Vol. 27, No. 4

Symbiotic transition of algaecoral triggered by paleoclimatic events?

Dan Tchernov1*, Tali Mass2* and David F. Gruber3*
1

Marine Biology Department, The Leon H. Charney School of Marine Sciences, University of Haifa, Mount Carmel, Haifa 31905, Israel 2 Interuniversity Institute for Marine Science, Eilat 88103, Israel 3 Department of Natural Sciences, City University of New York, Baruch College, Box A-0506, 17 Lexington Avenue, New York, NY 10010, USA

The algaecoral endosymbiosis is a canonical instance of mutualistic interaction, a textbook example of a relation*

Corresponding author: Tchernov, D. (dtchernov@univ.haifa.ac.il). All authors contributed equally.

ship between two species in which each derives benets. The dinoagellate algae accommodate nearly all of the respiratory demands of the coral via the excretion of readily available carbohydrates, and enhance calcication as

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