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Competition from Below for Light and Nutrients Shifts Productivity Among Tropical Species

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Competition from Below for Light and Nutrients Shifts Productivity Among Tropical Species Competition from below for light and nutrients shifts productivity among tropical species John J. Ewela,1 and Mari´a Julia Mazzarinob aDepartment of Biology, University of Florida, Gainesville, FL 32611; and bConsejo Nacional de Investigaciones Científicas y Te´cnicas de Argentina, Universidad Nacional del Comahue, 8400 Bariloche, Argentina Edited by Christopher B. Field, Carnegie Institution of Washington, Stanford, CA, and approved October 3, 2008 (received for review July 24, 2008) Chance events such as seed dispersal determine the potential canopy: Hyeronima alchorneoides, Cedrela odorata, and Cordia composition of plant communities, but the eventual assemblage is alliodora; 1 alien palm, Euterpe oleracea, which has a native determined in large part by subsequent interactions among spe- congener; and 1 native, giant perennial herb, Heliconia imbricata cies. Postcolonization sorting also affects the ultimate composition (all species are referred to hereafter by genus). The intent was of communities assembled by people for restoration, horticulture, to encompass some of the variability within the broad category or conservation. Thus, knowledge of the mechanisms controlling of canopy-tree life form while holding the identity of the interspecific interactions in plant communities is important for monocots (palm and herb) constant. Among other differences, explaining patterns observed in nature and predicting success or Hyeronima (like the 2 monocots) is never leafless whereas the failure of utilitarian combinations. Relationships among species, other 2 tree species are deciduous after attaining age 5–7 yr, especially those from studies of biological diversity and ecosystem Cedrela in the dry season and Cordia in the wet season. Tree functioning, are largely based on studies of short-lived, temperate- seedlings were planted at high density (2,887 plants per hectare) zone plants. Extrapolation to perennial plants in the humid tropics in replicated 0.24-ha plantations (3 per tree species). Trees were is risky because functional relationships among large-stature spe- lightly thinned periodically during the early years of the study to cies change with time. Shifts in competitive relationships among 3 avoid stand stagnation while sustaining complete use of re- life forms—trees, palms, and perennial herbs—occurred during 13 sources. Half of each plantation was retained as a single-species yr in experimental tropical ecosystems. In 2 cases the novel com- community (monoculture), and Euterpe and Heliconia were petitive mechanism responsible for the shift was reduction in added to the other half, creating polycultures. Both monocots crown volume, and therefore light-capturing capability, of over- have very long leaves (Euterpe, Ϸ3m;Heliconia, Ϸ2m)and topping deciduous trees by intrusive growth from below a palm. display their lamina almost vertically, giving them very high leaf In a third case, complementary resource use developed between 2 area. evergreen life forms (overstory tree and palm), probably because of differential nutrient acquisition. Species-level traits and ade- Results quate time for shifts in interspecific relationships to emerge are To assess the performance of individual plant species as well as crucial for predicting community trajectories. entire communities, we used aboveground net primary produc- tivity (ANPP), which integrates net growth and biomass pro- complementarity ͉ diversity ͉ ecosystem functioning ͉ fertile soil ͉ duced but lost during the growth-measurement interval (e.g., as plant competition mortality or litterfall). ANPP increased in all monocultures for the first 3–4 yr, then declined moderately (Hyeronima, from Ϸ30 to 18 Mg haϪ1 yrϪ1; Cedrela, from Ϸ18 to 11 Mg haϪ1 yrϪ1)or esign of sustainable ecosystems, whether for biodiversity oscillated around relatively high levels (Cordia, 15; range 10–21 conservation, economic gain, or restoration of ecosystem D Mg haϪ1 yrϪ1) for the next decade (Fig. 1). These values are at services, involves the assembly of plant communities comprising the middle to high end of the range typically reported for species of high ecological combining ability (1, 2). That com- fast-growing trees in the tropics (4). bining ability is determined by interspecific interactions and The time course of tree ANPP in polycultures was very different refers to the ways and degree to which common resources, from that of monocultures in the case of the deciduous trees Cedrela particularly light, water, and mineral nutrients, are shared. Does and Cordia, whose ANPP in polyculture plummeted dramatically the nature of plant interactions remain relatively constant over after 3 yr, even becoming negative (because of mortality) after 10 time? If not, prediction of combining ability will require either Ϫ Ϫ yr (Cedrela) or dropping to Ϸ1Mgha 1 yr 1 (Cordia). The start of case-specific long-term observation or thorough understanding the decline in tree ANPP in polyculture was synchronous with (in of the mechanisms involved. the case of Cedrela) or briefly preceded (in the case of Cordia) the To examine the stability of plant interactions, and to reveal peak of Heliconia ANPP, at which time Heliconia contributed mechanisms driving any changes observed, we constrained the 30–40% of ecosystem-level ANPP. By stand age 5 yr Heliconia, number of perennial life-form groups in simple experimental which has a basal meristem and whose maximum height is therefore communities while varying the specific identity of 1 of them. The biomechanically constrained, had been overtopped by the dense- study site, a young alluvial terrace at La Selva Biological Station canopied, evergreen Euterpe and no longer contributed to ANPP. in the humid tropical lowlands of Costa Rica, was chosen because Then, Euterpe ANPP soared as deciduous-tree ANPP plummeted, of its exceptionally fertile soil and warm, wet climate. By conducting experiments in an environment where plants expe- rienced few abiotic constraints on growth we achieved results Author contributions: J.J.E. designed research; J.J.E. performed research; J.J.E. and M.J.M. quickly and avoided the delays intrinsic to environments where analyzed data; and J.J.E. and M.J.M. wrote the paper. plant growth is slow or where the ecological clock is reset The authors declare no conflict of interest. annually. This article is a PNAS Direct Submission. The life forms selected are among those most common in 1To whom correspondence should be addressed at: Department of Biology, University of mature forest at La Selva (3) and characteristic of forests in Florida, P.O. Box 118526, Gainesville, FL 32611. E-mail: jackewel@ufl.edu. warm, wet climates on all continents. They are structurally and This article contains supporting information online at www.pnas.org/cgi/content/full/ functionally very different from one another and included 3 0807216105/DCSupplemental. native, fast-growing tree species capable of reaching the forest © 2008 by The National Academy of Sciences of the USA 18836–18841 ͉ PNAS ͉ December 2, 2008 ͉ vol. 105 ͉ no. 48 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0807216105 Downloaded by guest on October 2, 2021 30 A 25 25 A 20 20 15 15 10 5 10 0 5 35 ) 30 B 0 -1 25 yr 25 B -1 20 20 15 15 10 5 10 0 (m) Height ANPP (Mg ha 5 -5 25 C 0 20 25 15 C 10 20 5 15 0 -5 10 12345678910111213 5 Vegetation Age (yr) 0 Fig. 1. ANPP in monocultures and 3-species polycultures dominated by 12345678910111213 different tree species. (A) Hyeronima.(B) Cedrela.(C) Cordia. Open red sym- Vegetation Age (yr) bols, tree in monoculture; filled red symbols, tree in polyculture; star, Helico- nia; diamond, Euterpe; inverted triangle, polyculture total. Values are Fig. 2. Height relationships between tree species and palm (Euterpe, in- means Ϯ SE from 3 blocks. verted triangle). (A) Hyeronima (squares). (B) Cedrela (circles). (C) Cordia (triangles up). Open symbols are trees in monoculture; filled symbols are trees in polycultures. Values are means of all individuals greater than or equal to the making Euterpe the dominant component of Cedrela and Cordia third quartile in each of 3 blocks. SEs are too small to show at this scale. polycultures. In the case of the evergreen Hyeronima, the time course of tree ANPP in polycultures was similar to that of monocultures, but floristic differences between monocultures and polycultures, the monocots responded very differently than when they were differences among species in concentrations of foliar nitrogen grown with the deciduous tree species. Heliconia never contrib- (N) and phosphorus (P) were consistent throughout the 13-yr uted measurably to total ANPP, and Euterpe growth was negli- study, regardless of the community in which they were located: gible for the first 6 yr beneath the Hyeronima canopy. Thereafter tree species alone or in polyculture, and Euterpe and Heliconia Euterpe began to grow more rapidly, eventually boosting eco- grown with any of the 3 tree species (Fig. S3). Foliar N and P system-level ANPP above levels in the Hyeronima monocul- concentrations of all species were high in comparison with data ture—an example of complementary resource use. from many tropical forests (7). Thus, there is no compelling Even through the later years of the experiment, when growth evidence indicating that competition for N or P led to Euterpe of the deciduous trees in polycultures was stunted and many dominance in the Cedrela and Cordia polycultures. individuals died, the trees retained their canopy position as the Reduced light capture proved to be the primary mechanism tallest components in each of their respective polycultures (Fig. causing ANPP of the overtopping Cedrela and Cordia trees to 2). Despite occupying the tallest stratum in these 3-life-form decline: Euterpe reduced the leaf area of both of these tree systems, the leaf area of the deciduous trees dropped well below species by invading their crowns from below. The result was a their values in monocultures while the evergreen Hyeronima reduction in crown volume, and therefore leaf area, of both sustained high values in both monoculture and polyculture (Fig.
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