Distribution and Abundance of Tree Species in Swamp Forests of Amazonian Ecuador

Distribution and abundance of tree species in swamp forests of Amazonian Ecuador

Nigel C. A. Pitman , Juan Ernesto Guevara Andino , Milton Aulestia , Carlos E. Cer ó n , David A. Neill , Walter Palacios , Gonzalo Rivas-Torres , Miles R. Silman and John W. Terborgh

N. C. A. Pitman ([email protected]) and J. W. Terborgh, Center for Tropical Conservation, Nicholas School of the Environment, Duke Univ., PO Box 90318, Durham, NC 27708, USA. NCAP also at: Science and Education, Th e Field Museum, 1400 S. Lakeshore Dr., Chicago, IL 60605-2496, USA. – J. E. G. Andino, Dept of Integrative Biology, 1005 Valley Life Sciences Building no. 3140, Univ. of California- Berkeley, Berkeley, CA 94720-3140, USA. – M. Aulestia and W. Palacios, Herbario Nacional del Ecuador, Casilla 17-21-1787, Avenida R í o Coca E6-115, Quito, Ecuador. – C. E. Cer ó n, Escuela de Biolog í a, Univ. Central del Ecuador, Casilla 17-01-2177, Quito, Ecuador. – D. A. Neill, Univ. Estatal Amaz ó nica, Puyo, Pastaza, Ecuador. – G. Rivas-Torres, Wildlife Ecology and Conservation and Quantitative Spatial Ecology, Evolution, and Environment Program QSE3-IGERT, Dept of Wildlife, Ecology, and Conservation, Univ. of Florida, 110 Newins- Ziegler Hall, PO Box 110430, Gainesville, FL 32611-0430, USA. – M. R. Silman, Dept of Biology, Wake Forest Univ., 1834 Wake Forest Rd., Winston-Salem, NC 27106, USA.

Research to date on Amazonian swamps has reinforced the impression that tree communities there are dominated by a small, morphologically specialized subset of the regional fl ora capable of surviving physiologically challenging conditions. In this paper, using data from a large-scale tree inventory in upland, fl oodplain, and mixed palm swamp forests in Amazonian Ecuador, we report that tree communities growing on well-drained and saturated soils are more similar than previously appreciated. While our data support the traditional view of Amazonian swamp forests as low- diversity tree communities dominated by palms, they also reveal four patterns that have not been well documented in the literature to date: 1) tree communities in these swamp forests are dominated by a phylogenetically diverse oligarchy of 30 frequent and common species; 2) swamp specialists account for Ͻ 10% of species and a minority of stems; 3) most tree species recorded in swamps (Ͼ 80%) also occur in adjacent well-drained forest types; and 4) many tree species present in swamps are common in well-drained forests (e.g. upland oligarchs account for 34.1% of all swamp stems). Th ese observations imply that, as in the temperate zone, the composition and structure of Amazonian swamp vegetation are determined by a combination of local-scale environmental fi lters (e.g. plant survival in permanently saturated soils) and landscape-scale patterns and processes (e.g. the composition and structure of tree communities in adjacent non-swamp habitats, the dispersal of propagules from those habitats to swamps). We conclude with suggestions for further research to quantify the relative contributions of these factors in structuring tree communities in Amazonian swamps.

Th e scientifi c literature describing the tree communities of Ceró n and Reyes 2007, and many others; but see Cornejo Amazonian swamps is scant and largely reducible to four Valverde and Janovec 2006 for an exception). While points. this low diversity is understood to be a consequence of 1) Tree communities in swamps are typically dominated point 1, its root cause may be the small size and insular by one or more species of arboreal palms (Kahn and Mejí a character of swamp habitats (MacArthur and Wilson 1967, 1990, Kahn 1991, Kahn and Granville 1992, and many oth- ter Steege et al. 2001). ers). Th is is most commonly the quintessential Amazonian 3) Th e fl oristic composition and structure of tree swamp palm Mauritia fl exuosa, but several other palms communities in Amazonian swamps can be extremely and dicotyledonous tree species have also been observed as variable from site to site, both within and between regions, dominants (Table 1). and often more so than in adjacent well-drained habitats 2) Tree communities in swamps tend to be less diverse at (Duque et al. 2001, Romero-Saltos et al. 2001, Ancaya local scales than those in adjacent, well-drained forests 2002). Tree communities in swamps also change over time (Richards 1952, 1969, Ducke and Black 1953, Dumont along a variety of successional pathways (Kalliola et al. 1991, et al. 1990, Duivenvoorden 1995, 1996, Pitman et al. Roucoux et al. 2013). Th is spatial and temporal variability 1999, Duque et al. 2001, 2002, Romero-Saltos et al. 2001, in swamp forests is typically explained as a result of spatial Ancaya 2002, Ceró n et al. 2003, Normand et al. 2006, and temporal variation in fl ooding intensity, depth, water

902 Table 1. A list of tree taxa that have been reported to be the single most common species in at least one swamp forest inventory in western Amazonia. Only inventories of trees Ն 10 cm dbh were considered. Species followed by an asterisk have also been reported as common in well-drained forest types in western Amazonia by a variety of authors, including Pitman et al. (2001), Duque et al. (2002), Dick et al. (2003), Cornejo Valverde and Janovec (2006), and Rivas (2006).

Species Region References Palms Mauritia ﬂ exuosa all regions Kahn and Mej í a (1990), Kalliola et al. (1991), Foster et al. (1994, 2000, 2001), Freitas Alvarado (1996a, b), Gr á ndez et al. (2001), Romero-Saltos et al. (2001), Ancaya (2002), Cer ó n et al. (2003), Fine et al. (2006), Vriesendorp et al. (2004, 2006, 2007, 2008), Cer ó n and Reyes (2007), Honorio et al. (2008), Corrales Medina (2010), Garc í a-Villacorta et al. (2010, 2011), Householder et al. (2012), this study, and many others ∗ Euterpe precatoria southern Peru Cornejo Valverde and Janovec (2006) ∗ Iriartea deltoidea eastern Ecuador This study Mauritiella armata eastern Ecuador This study Mauritiella sp. central Peru Foster et al. (2001) ∗ Oenocarpus bataua northern Peru Kalliola et al. (1991), Vriesendorp et al. (2004) ∗ Socratea exorrhiza northern Peru Vriesendorp et al. (2004), Garcí a-Villacorta et al. (2011) Non-palms Ficus trigona southern Peru Ancaya (2002) Lueheopsis hoehnei southern Peru Gentry (1988), Foster et al. (1994) Oxandra polyantha southern Colombia Duque et al. (2001) Sacoglottis ceratocarpa northern Peru Corrales Medina (2010) ∗ Symphonia globulifera northern Peru Pitman et al. (2003a) Tabebuia insignis northern Peru Roucoux et al. (pers. comm.) Sloanea sp. southern Peru Ancaya (2002)

chemistry, and other abiotic factors (as in temperate zone (e.g. seed input from adjacent forest types, the size and shape swamps; Kozlowski [1984], Casanova [2000]), and is of swamp forests, characteristics of the regional species refl ected in various schemes for classifying Amazonian swamp pool), and thus refl ects an outdated view of how ecological vegetation (Prance 1979, Klinge et al. 1990, Kalliola et al. 1991, communities are assembled (Ricklefs 2008 and references Junk and Piedade 2004, Ricaurte et al. 2012; for recent therein). reviews of classifi cation systems see Junk et al. 2011, 2013). Th e current paradigm of Amazonian swamps also 4) Tree communities in Amazonian swamps often suff ers from the long-standing bias in studies of tropical veg- feature species that possess adaptations to life in permanently etation towards highlighting diff erences between samples wet conditions. Th ese include the ability of seedlings to while playing down similarities (Pitman et al. 2001; see survive long periods underwater (De Vries 1997) and the also Gaston 2011). Since the tree communities in well- presence of pneumatophores (Granville 1974) or elaborate drained forests adjacent to swamps tend to be extremely stilt or aerial roots (see also Joly 1991, Armstrong et al. diverse and are rarely dominated to a large degree by a single 1994, Jackson and Colmer 2005, Schö ngart et al. 2005, de species, many researchers have been content to document Oliveira and Joly 2010). diff erences between swamp and non-swamp forest types Th ese four points have dominated the literature on while overlooking some striking parallels. For example, swamp tree communities for so long that the current para- the common perception of swamps as a very distinctive for- digm of Amazonian swamps – an environmentally harsh set- est type sits poorly with the fact that at least fi ve of the ting in which only a handful of highly specialized tree tree species reported to be top dominants in western taxa can prosper – is now well established. According to this Amazonian swamps (Table 1) have also been reported as view, Amazonian swamp forests are primarily assembled common in well-drained forest types there. from the regional species pool by the exclusionary action of In this study, inspired by Ricklefs’ (2008) call to under- a strong environmental fi lter: the anoxic conditions in water- stand how communities are assembled by examining the logged soils, which permit the establishment of specialists distribution and abundance of the species they contain across with morphological adaptations for surviving such condi- the broader landscape, we examined patterns of tree species tions but kill all other species. Another set of fi lters – related distribution, frequency, and abundance in swamp forests to water chemistry, fl ooding intensity, peat depth, peat or and two adjacent well-drained forest types (fl oodplain and soil composition, microtopography, and other such factors upland) at a lowland Amazonian site in eastern Ecuador. – are understood to permit a given species to be dominant Our specifi c questions included: 1) are swamp forests at in certain swamps or at certain times but not in others our site dominated by a suite of frequent and locally (Junk 1982, 1989, Ancaya 2002). common tree species (an ‘ oligarchy ’ ) in the same way that While this paradigm is satisfying in some respects, it is upland forests there are (Pitman et al. 2001, Mací a clearly undeveloped in others. One shortcoming is that it and Svenning 2005)? 2) How many of the tree species grow- gives precedence to processes operating at the local scale ing in swamp forests can be considered swamp specialists? (e.g. seed germination and seedling survival in swamps) over 3) How many species in swamps have also been recorded processes and patterns at the landscape or regional scales in well-drained forests, and how many are common there?

903 Answers to these questions allow us to partition the tree Amazonian forests of Yasun í National Park and the adjacent communities growing in swamps into distributional guilds as Huaorani Ethnic Reserve in eastern Ecuador (hereafter follows: x% of stems belong to species that specialize strictly referred to collectively as ‘ Yasun í ’ ; Fig. 1). Th e remaining on swamps, y% to species that are common in all three forest two upland plots were established in similar forest Ͻ 100 km types, z% to species that prefer well-drained forest types west of Yasun í (see map in Pitman et al. 2001). Th ese sites but occasionally spill over into swamps, and so on. In turn, and their fl ora are among the best studied in the Amazon that partitioning should provide some new ways to (Herrera-MacBryde and Neill 1997, Pitman 2000, Bass think about why certain species are common in swamps and et al. 2010, Pitman et al. 2011). others are not, why the common species in swamps are so According to a new offi cial map of Ecuador ’ s vegetation dominant there, and why local-scale tree diversity is so much (Mapa de Vegetació n del Ecuador 2012), the study area is lower in swamps than in well-drained forest types. As dominated by upland forests (∼ 79% of the total), with Fine et al. (2010) have recently done for white sand forests, a smaller areas, mostly along rivers, covered by swamp forests more general aim is to help place a forest type that is often ( ∼ 19%) and fl oodplain forests (∼ 2%; Fig. 1). Swamp forests viewed as distinct and atypical into a broader context by doc- in our study were defi ned as tree communities growing umenting its connections with the surrounding landscape. on peaty substrate that was saturated at the time of fi eld work and that appeared to remain so year-round. Th ese substrates were composed mostly of decaying plant matter Study site and forest types (a large portion of which appeared to be leaf fragments), under which mineral soil was typically only encountered All swamp and fl oodplain inventories and all but two of the after digging Ͼ 20 cm (and often not encountered at all). upland inventories were carried out in the aseasonal lowland Where mineral soil was found in swamps, laboratory analyses

Figure 1. Th e location of the study plots in western Amazonia. (A) Th e location of Ecuador in South America. (B) Th e location of Yasuní National Park in Ecuador. (C) Th e northwestern portion of Yasuní National Park (black) and the eastern portion of the Huaorani Ethnic Reserve (labeled). (D) Th e locations of 13 of the upland tree plots (U) and all of the swamp (S) and fl oodplain (F) tree plots discussed in the paper. Numerals after a symbol indicate that multiple hectares were inventoried in the same vicinity. Forest type maps are from a recent nationwide classifi cation of forest types (Mapa de Vegetaci ó n del Ecuador 2012). Swamp forest shown here includes both monodominant Mauritia fl exuosa swamps and mixed swamps.

904 indicated that it primarily consisted of clay and silt, as is the established two adjacent 1-ha plots. All swamp and fl ood- case for most soils in Yasuní (% clay Ͼ % silt Ͼ % sand; plain plots measured 100 ϫ 100 m, but some upland plots Pitman unpubl.). were irregularly shaped (Pitman et al. 2001). Th ick, peaty substrates were never seen in upland forests In all plots trunk circumference at 1.3 m was measured (which we defi ned as forests that were never fl ooded) or and stems permanently marked with numbered aluminum fl oodplain forests (forests fl ooded for short periods during tags. (In the Dicaro 3 plot only 200 of the 378 Mauritiella high-water events and otherwise well-drained). All swamp armata stems were measured for circumference, because plots held some standing water during fi eld work, and their densely spiny trunks complicated measurements. Th e shared an additional landscape feature which we did not basal area of that plot was estimated by assuming that all observe in other forest types in Yasuní : sturdy hummocks of unmeasured individuals had the mean circumference value roots, organic matter, and mineral soil at the bases of many of the 200 individuals we did measure.) Circumferences trees, standing as much as 50 cm higher than the surround- were converted to diameters by assuming that stem cross- ing terrain and giving the impression of miniature islands sections were round. surrounded by peat- or water-fi lled depressions. Even these Trees that could not be identifi ed in the fi eld were hummocks, however, were well under the maximum water collected and compared to mounted specimens in the levels in swamps. We did not measure substrate moisture QCNE and QCA herbaria in Quito, Ecuador. Th is was levels during the inventories, and do not have data on the especially eff ective because the QCNE herbaria holds sev- origin, chemistry, seasonality, or hydrology of the waters eral thousand specialist-identifi ed tree specimens collected that fl ood the swamps we sampled. in Yasuní . When a specimen could not be matched to All swamp plots were Ͻ 1 km from rivers and their bor- herbarium material, it was assigned a temporary morpho- ders at least 50 m from swamp edges (i.e. from the nearest species name and treated in analyses as though it were a non-swamp forest type). We did not consciously select cer- named species. A full set of vouchers from the tree plots tain kinds of swamps, but sampled what we found growing was mounted and deposited at QCNE and a subset depos- on saturated soils within the vicinity of the 110-km pipeline ited at MO. All swamp specimens were entered into road that traverses the northwestern corner of Yasun í . Th e the TROPICOS database, under NP collection numbers offi cial map of Ecuadorean vegetation (Mapa de Vegetaci ó n 3466 – 3550 (Tiputini 4A plot), 3951 – 4052 (Tiputini 4B), del Ecuador 2012) distinguishes between two types of 4456 – 4483 (Dicamunpare 1), 4484 – 4526 (Dicaro 3), swamp vegetation in Yasuní National Park: one in which and 4528 – 4589 (Dicamunpare 2). nearly all trees are M. fl exuosa (presumably because fl ooding Th e upland plots described here represent the same there is severe enough to kill all other species; 66 418 ha) dataset described in Pitman et al. (2001, 2002), with the and another in which M. fl exuosa coexists with other tree exception of some taxonomic updates. To assign species to species (presumably because fl ooding is not severe enough plant families, we followed Angiosperm Plant Group con- to fi lter them out; 127 710 ha). All of our plots correspond ventions as of May 2010 (APG II 2003). to the latter category. According to other systems for classifying swamp vegetation, the swamp forests we studied in Yasuní appear to correspond to ‘ palm swamps and forest Analyses swamps ’ sensu Kalliola et al. (1991), ‘ swamp forests ’ sensu Herrera-MacBryde and Neill (1997), ‘ lowland fl ooded To explore abundance patterns in the three forest types, we palm forest’ sensu Palacios et al. (1999), and ‘ forested asked 1) if an oligarchy of common and frequent species swampy wetlands (mixed forests) ’ sensu Junk et al. (2013). dominated swamp forests, 2) how many species could Because our study was carried out in a region where be considered swamp specialists, and 3) how many species neither blackwater rivers nor open, herb-dominated wet- recorded in swamps were also recorded in well-drained forest lands are common, our plots sample a relatively narrow types (fl oodplains and uplands), and how many qualifi ed portion of the full range of Amazonian swamp vegetation as oligarchs in those forest types. (L ó pez Parodi and Freitas 1990, Kalliola et al. 1991). For Following Pitman et al. (2001), we defi ned upland oli- example, nutrient-poor swamps with dense, treelet- garchs as species recorded in a majority of upland plots and dominated vegetation that have been described around at an overall density of Ն 1 individual ha Ϫ 1 in the uplands. Iquitos, Peru (Encarnació n 1985, Garcí a-Villacorta et al. We used the same criteria to identify swamp oligarchs and 2003, 2011), do not appear to occur in Yasun í . fl oodplain oligarchs. For example, swamp oligarchs were species that were recorded in a majority of swamp plots and at an overall density of Ն 1 individual ha Ϫ 1 in swamp plots. Methods Species that qualifi ed independently as oligarchs in all three forest types are referred to in this paper as ‘ super-oligarchs. ’ Field work To identify swamp specialists in this study we used two arbitrary thresholds: one for strict specialists and one for Field work was carried out at four sites in swamps functional specialists. Strict swamp specialists were species (1998 – 1999; Supplementary material Appendix 1), fi ve sites that had an overall density in swamps of Ն 1 individual in fl oodplains (1997– 1999), and 15 sites in the uplands ha Ϫ 1 and were never recorded in the other forest types. (1987– 1999; Fig. 1). At each site we carried out a standard Functional swamp specialists were species that had an overall 1-ha tree inventory of all free-standing trees Ն 10 cm dbh, density in swamps of Ն 1 individual ha Ϫ 1 , for which Ն 80% with the exception of one swamp site (Tiputini 4) where we of all individuals were recorded in swamps, and that did not

905 qualify as an oligarch in a well-drained forest type. Note that plots are given in Supplementary material Appendix 1. With because just 19.2% of all the stems we sampled in the plot the exception of 34 trees that we were unable to identify, the network were in swamps, a species with Ն 80% of its indi- 2983 swamp stems were sorted to 243 species-level taxa viduals in swamps would have ∼ 94% of its individuals in (204 species and 39 morphospecies). Most morphospecies swamps if the same number of stems had been sampled were rare, and together they accounted for 5.6% of swamp in swamps as in non-swamp forest types. stems. Forty species recorded in swamps (16.5% of To check how the results of these arbitrary thresholds all swamp species) were recorded in no other forest type, compared with those of a commonly used method for identi- and these accounted for 31.7% of all swamp stems. Th irty fying the dominant species in a given habitat, we performed of the species that were only recorded in swamps occurred an indicator species analysis (ISA) with the full 25-plot data- in a single plot there, and 17 of those were represented by set to identify species associated with swamps (Dufrê ne and a single tree. Legendre 1997). While the ISA provides some additional context for the results of the arbitrary thresholds, we gave precedence to the latter due to their simplicity and transparency. Swamp oligarchs To summarize the results of the above analyses we quanti- fi ed the proportion of all stems and of all species in swamps Tree communities in swamps were dominated by a strong that qualifi ed for the three categories of distribution and oligarchy. Th irty of the 243 species recorded in swamps abundance described above: strict swamp specialists, func- qualifi ed as oligarchs there, and these accounted for tional swamp specialists, and super-oligarchs. Species that 59.0% of stems and 12.3% of species in swamps. Within did not fall into any of these three categories were classifi ed individual swamp plots, swamp oligarchs accounted for ϭ into one of three additional categories: ‘ too rare’ (species rep- between 38.6 and 86.3% of all stems (average 61.0%). resented by Յ 4 stems in the entire dataset and thus consid- Th e lowest value is from the Dicaro 3 plot, where nearly half ered too rare for their distribution to be characterized), of stems belonged to a non-oligarch palm (Mauritiella ‘ spillover ’ (defi ned arbitrarily as species that were represented armata) which we recorded nowhere else. Th e most common in the entire dataset by Ն 5 stems, Ͻ 13% of which were in swamp oligarchs were the palms Iriartea deltoidea (ranking swamps), and ‘ other ’ (for all other species). Th e Ͻ 13% value no. 1 in abundance in two plots) and Mauritia fl exuosa in the spillover defi nition comes from a binomial probability (ranking no. 1 in two plots; Table 3). Despite the clear calculation based on the fact that swamp stems account for dominance of palms, the 30 swamp oligarchs were a 19% of the entire dataset; that calculation shows that species taxonomically diverse group, including 28 genera in 16 with Ͻ 13% of their stems in swamps are signifi cantly rarer families (Supplementary material Appendix 1). in swamps than expected (p ϭ 0.04). Although a strong oligarchy was observed in swamps, this should not be misinterpreted to mean that community composition and structure were uniform between swamp Results plots. Both composition and structure were more variable between swamp plots than between plots in other forest Structural and ecological attributes of the 25 tree plots are types, as measured by the Sorenson ’ s and Bray – Curtis indices summarized in Table 2, and additional details of the swamp (Table 2).

Table 2. Structural and ecological attributes of the 25 1-ha tree plots studied at Yasuní , Ecuador.

Attribute Swamps Floodplain Uplands No. ha sampled 5 5 15 No. stems sampled 2983 2730 9809 No. species 243 511 986 No. families 39 53 70 Mean stems ha Ϫ 1 597 546 654 Mean species ha Ϫ 1 74 189 239 Mean basal area ha Ϫ 1 (m 2 ) 25.7 27.9 30.2 % stems that belong to single most common species 12.7 6.6 7.8 % stems in 5 most common species 52.1 14.0 14.7 Abundance rank of Iriartea deltoidea 3rd 1st 1st No. forest type oligarchs 30 88 150 % spp. that are forest type oligarchs 12.3 17.2 15.2 % stems that are forest type oligarchs 59.0 55.2 63.0 No. spp. recorded in every plot of the given forest type 2 13 6 No. singletons 109 186 128 % spp. that are singletons 44.9 36.4 13.0 No. spp. recorded in just one plot 162 257 343 No. palm species 10 11 9 No. palm species that are forest type oligarchs 6 7 6 % stems that are palms 57.4 12.0 9.9 Mean Sorenson’ s index between plots within forest type 0.244 0.348 0.376 Mean Bray – Curtis index between plots within forest type 0.239 0.297 0.332

906 Table 3. The ten most abundant tree species in ﬁ ve 1-ha inventories in swamp forests in Yasuní , Ecuador.

Tiputini 4A ind. Tiputini 4B ind. Iriartea deltoidea* * 216 Iriartea deltoidea* * 122 Mauritia fl exuosa* * (S) 65 Attalea butyracea * * (S) 92 Attalea butyracea * * (S) 54 Mauritia fl exuosa* * (S) 56 Euterpe precatoria* * 48 Euterpe precatoria* * 53 Sloanea ‘ bark ’ (NP3478) (S) 24 Isertia rosea (S) 24 ∗∗ Socratea exorrhiza* * 16 Astrocaryum murumuru var. urostachys 19 Cespedesia spathulata (S) 14 Socratea exorrhiza* * 16 Macrolobium angustifolium (S) 9Sterculia apeibophylla 12 Sterculia apeibophylla 8 Apeiba membranacea 9 ∗∗ Astrocaryum murumuru var. urostachys 7 Pterocarpus amazonum/rohrii cf. 7 Dicamumpare 1 ind. Dicaro 3 ind. ∗∗ Mauritia fl exuosa* * (S) 170 Mauritiella armata (S) 378 Euterpe precatoria* * 108 Euterpe precatoria* * 95 ∗∗ Macrolobium angustifolium (S) 44 Oenocarpus bataua 71 Zygia glomerata cf. (S) 44 Macrolobium angustifolium (S) 64 Buchenavia amazonia (S) 11 Sloanea ‘ bark ’ (NP3478) (S) 18 Hieronyma alchorneoides var. estipulosa 11 Hieronyma alchorneoides var . estipulosa 13 Hydrochorea corymbosa 10 Virola surinamensis 11 Cecropia engleriana 10 Lauraceae ‘ palermo ’ (NP4484) (S) 11 Virola peruviana cf. 10 Socratea exorrhiza * * 10 Euphorbiaceae ‘ nondescript ’ (NP4465) (S) 7 Sterculia frondosa 10 Dicamumpare 2 ind. Mauritia fl exuosa* * (S) 68 Triplaris weigeltiana 36 Casearia uleana 28 Key Zygia coccinea var . oriunda 27 boldface ϭ top ten in multiple plots ∗∗ Euterpe precatoria* * 23 ϭ palm Hieronyma alchorneoides var. estipulosa 19 (S) ϭ swamp specialist Cecropia engleriana 18 Pterocarpus amazonum/rohrii cf. 17 Virola pavonis 12 Duguetia spixiana 12

Only two species occurred in all ﬁ ve swamp plots: Euterpe precatoria (Arecaceae) and Macrolobium angustifolium (Fabaceae). Most species recorded in swamps (66.7% of the total) were recorded in just one swamp plot, and most of these occurred as a single individual (Table 2). Nearly half of all species recorded in swamps (44.9%) were singletons.

Swamp specialists

Twelve tree species qualifi ed as strict swamp specialists, and these accounted for 4.9% of swamp species and 30.0% of swamp stems. Nine other species qualifi ed as functional specialists. Together, these 21 species accounted for 8.6% of swamp species and 43.6% of swamp stems (Fig. 2). Th is small guild of swamp specialists was dominated by two palm species: Mauritiella armata (12.7% of all swamp stems) and Mauritia fl exuosa (12.0%; Fig. 3). Indicator species analysis identifi ed 11 species with a positive, statistically signifi cant association with swamp forests, and was thus more stringent in identifying swamp specialists than our arbitrary method. Th ese 11 species accounted for 34.6% of all swamp stems. Eight of the 11 swamp indicators are among the 21 species we defi ned Figure 2. Th e proportions of all species and all stems in fi ve as specialists (fi ve strict and three functional specialists; 1-ha swamp plots in Yasuní , Ecuador, that belong to four diff erent Table 4). Th e other three swamp indicators (Euterpe distributional guilds, or that were too rare (too rare) or too precatoria , Hieronyma alchorneoides , Symphonia globulifera ) eclectic (other) to classify. See the text for guild name defi nitions.

907 Figure 3. A diagram illustrating distributional patterns of tree species across three forest types in Yasun í , Ecuador. (A) Th e proportions of species recorded in each forest type in each of four distributional patterns. For example, the left-hand square represents all species in swamps. Th e rectangular portion labeled ‘ also in fl oodplains and uplands ’ indicates that slightly more than half of all species recorded in swamps were also recorded in both fl oodplain and upland forests. (B) A schematic cross-section of the Yasuní landscape illustrating one commonly observed arrangement of the three forest types there. Th e gray area is peat and the stippled area is a river. (C) Th e proportions of all stems recorded in each forest type that belong to species in each of four distributional patterns. Within each forest type the top four rectangles correspond to the same sequence of distributional patterns shown in that forest type in (A). Th e fi fth, bottom- most rectangle represents unidentifi ed stems. In some categories the most common species is indicated within a rectangle whose size is proportional to that species ’ abundance. were too common in well-drained forests to qualify as (Fig. 3). Most species recorded in swamps (53.1%) were also specialists under our arbitrary thresholds. recorded in both well-drained forest types, and these Sixty species in swamps (24.7% of all species) qualifi ed as accounted for 50.4% of all swamp stems. ‘ spillover ’ taxa, and these accounted for 3.4% of trees in A large proportion of species recorded in swamps were swamps. Sixty-three species (25.9%) were too rare for common in well-drained habitats. For example, 30.8% of their distributional patterns to be classifi ed, and 91 (37.4%) all species recorded in swamps and 53.3% of species that were distributed between swamps and other forest types in a qualifi ed as oligarchs in swamps also qualifi ed as oligarchs in way that placed them in the category ‘ other. ‘ Th ese two one or both well-drained forest types. Th e 51 upland categories accounted for 3.0 and 21.4% of swamp trees, oligarchs recorded in swamps accounted for 34.1% of all respectively (Fig. 2). stems there; comparable numbers for fl oodplain oligarchs Of the 30 swamp oligarchs and 21 swamp specialists, are 50 and 34.2%. Together, 75 species that qualifi ed as oli- nine species qualifi ed as both: fi ve strict specialists and four garchs in at least one well-drained forest type were recorded functional specialists. in swamps, where they accounted for 40.3% of all trees. Th e number of well-drained forest type oligarchs recorded in swamps was higher than expected by chance. For example, Species distributions across forest types if the 174 species that were recorded in both swamps and the uplands were a random selection of the upland tree Th e great majority of species recorded in swamps (83.5%) fl ora, then they would be expected to include 26 of the were also recorded in at least one well-drained forest type, 150 upland oligarchs. Th e observed number was 51 and these species accounted for 68.3% of all swamp stems (chi-squared test, p Ͻ 0.0001). Th e same pattern held for

908 Table 4. Forty-one tree species whose abundances and frequencies in a network of 25 1-ha tree plots at Yasuní , Ecuador, suggest that they are swamp specialists, swamp oligarchs, or both. Species followed by a hash sign (#) showed a signiﬁ cant association with swamp forest in an indicator species analysis. See the text for details.

No. swamp No. swamp Oligarch? Family Speciesind. plots Swamp Uplands Floodplains Specialist? Arecaceae Mauritiella armata 378 1 strict Arecaceae Mauritia fl exuosa # 359 4 1 strict Arecaceae Iriartea deltoidea 343 3 1 1 1 Arecaceae Euterpe precatoria # 327 5 1 1 1 Arecaceae Attalea butyracea 146 2 functional Fabaceae Macrolobium angustifolium # 131 5 1 functional Arecaceae Oenocarpus bataua 76 3 1 1 Fabaceae Zygia glomerata 54 3 1 functional ElaeocarpaceaeSloanea ‘ bark ’ (NP3478)# 52 4 1 strict Euphorbiaceae Hieronyma alchorneoides var . estipulosa #454 1 Arecaceae Socratea exorrhiza 44 4 1 1 Polygonaceae Triplaris weigeltiana 39 3 1 1 functional Arecaceae Astrocaryum murumuru var. urostachys 30 3 1 1 1 Fabaceae Pterocarpus amazonum/rohrii cf. 30 4 1 1 1 Rubiaceae Isertia rosea # 28 4 1 strict Malvaceae Apeiba membranacea 21 4 1 1 1 Myristicaceae Virola pavonis 21 3 1 1 1 Ochnaceae Cespedesia spathulata 21 2 strict Lauraceae Licaria triandra # 20 4 1 functional CombretaceaeBuchenavia amazonia # 18 4 1 functional Malvaceae Sterculia frondosa 18 3 1 1 Urticaceae Coussapoa trinervia # 17 4 1 strict Clusiaceae Symphonia globulifera #1641 Malvaceae Theobroma subincanum 12 3 1 1 1 Lauraceae Lauraceae ‘ palermo ’ (NP4484) 11 1 functional Euphorbiaceae Sapium ‘ garcinia ’ (NP2855) 10 2 functional SapotaceaePouteria ‘ tenuipetiole ’ (NP3323) 9 3 1 1 Combretaceae Buchenavia viridifl ora 8 1 strict Rubiaceae Ferdinandusa guainiae 8 1 strict Annonaceae Unonopsis fl oribunda 731 1 Euphorbiaceae Alchornea ‘ webster ’ (NP4461)# 7 3 1 strict Euphorbiaceae Euphorbiaceae ‘ nondescript ’ (NP4465) 7 1 strict Malvaceae Sterculia colombiana 73111 Moraceae Ficus piresiana 741 Euphorbiaceae Conceveiba 1 (NP1461) 6 3 1 1 Fabaceae Macrolobium acaciifolium 6 2 strict Lecythidaceae Couroupita guianensis 631 1 Sapindaceae Sapindaceae ‘ chalky ’ (NP4560) 6 2 functional Clusiaceae Vismia ‘ myrsinac ’ (NP1490) 5 2 strict Fabaceae Machaerium fl oribundum 531 Sapotaceae Pouteria cuspidata ssp. robusta 531

fl oodplain forest oligarchs: 27 were expected in swamps and while swamp species recorded in fl oodplains but not in 50 observed (chi-squared test, p Ͻ 0.0001). the uplands were relatively common in swamps (Fig. 3). Eight species qualifi ed as oligarchs in all three forest types (Table 4); the expected number under the null model was less than one. Th ese ‘ super-oligarchs ’ accounted for 10.9, Discussion 13,9, and 26.5% of stems in upland, fl oodplain, and swamp forests, respectively (Fig. 2, 4). On average, these species While our data support all four of the well-documented occurred in 83.0% of plots in all forest types. features of Amazonian swamps reviewed in the introduction Species in swamps were more likely to be recorded in of this paper, they also indicate that those features coexist fl oodplain forests than in upland forests, but that trend was side by side with strong and underappreciated patterns of overshadowed by the much stronger trend towards species homogeneity. We begin this discussion by exploring four occurring in all three forest types. Indeed, the number of spe- relatively novel empirical patterns observed in swamps at cies recorded in all three forest types was more than four times our study site. We then proceed to discuss how these four higher than the number of species recorded in swamps and patterns aff ect our understanding of the tree communities fl oodplains but not in the uplands. Swamp species recorded growing in Yasuní swamps. We close by highlighting key in the uplands but not in fl oodplains were very rare in swamps, questions and directions for further research.

909 Figure 4. Th e proportions of all species and stems surveyed in fi ve 1-ha swamp plots in Yasuní , Ecuador, that belong to diff erent categories of oligarchic and non-oligarchic species. Th e category ‘ Oligarchs in all forest types’ consists of the eight species that are members of the swamp oligarchy, the fl oodplain oligarchy, and the uplands oligarchy, while the category ‘ Oligarchs only in swamps’ consists of the 14 species that are members of the swamp oligarchy but not members of the fl oodplain or uplands oligarchies.

Pattern 1: tree communities in swamps are a hectare of swamp forest regardless of whether the particu- dominated by an oligarchy lar dominant in that forest is M. fl exuosa , I. deltoidea , M. armata , or some other species. Th e oligarchy of frequent and locally common tree species For example, even the swamp plot with the most distinc- observed in Yasuní swamps (12.3% of swamp species tive tree community (Dicaro 3, nearly half of whose stems accounting for 59.0% of swamp stems) is similar in scale to belong to a non-oligarch) contained 17 swamp oligarchs, those observed in Yasuní fl oodplains (17.2% spp., 55.2% which together accounted for 38.6% of all stems. We thus stems) and uplands (15.2% spp., 63.0% stems). Just as a predict that the 30 swamp oligarchs identifi ed here will forester capable of identifying just 150 tree species in account for most stems in the majority of forests that the Yasuní uplands could identify half of the standing grow on peaty substrates in Yasuní . Th is prediction is upheld timber there (Pitman et al. 2001), the same forester would by data from Romero-Saltos et al. ’ s (2001) inventory of need only 30 species to do the same in swamp forests. trees Ն 10 cm dbh in fi ve 0.1-ha plots in Yasun í swamps, Furthermore, this rule seems likely to apply across approxi- which found that 62.7% of stems belonged to nine species mately 200 000 ha of swamp forest in Yasun í National identifi ed here as swamp oligarchs. Park. Th is represents additional evidence for the proposi- By contrast, tree communities in many other swamps in tion that strong oligarchic components are a common western Amazonia do not appear to be dominated by the feature of Amazonian tree communities (Pitman et al. 30 swamp oligarchs in Table 4. For example, the list of the 2001; see also Burnham 2002, 2004, Pitman et al. 2003b, 25 most abundant tree species in fi ve 0.1-ha swamp plots in 2013, Vormisto et al. 2004, Mací a and Svenning 2005, Caquet á , Colombia, includes only three of our 30 swamp Mac í a 2008, 2011, Fine et al. 2010). oligarchs (Duque et al. 2001). Th e comparable number While our data indicate that both the composition and for the 19 most abundant tree species in swamps at Pebas, structure of tree communities growing on peaty substrates Peru, is four (Gr á ndez et al. 2001). Th ere is, however, in Yasuní are predictable to some extent, they also make it a small subset of our swamp oligarchs at Yasun í that appear clear that there is nothing uniform about tree community to be abundant in swamps at all three sites (M. fl exuosa , composition and structure in Yasuní swamps. Th e fact that E. precatoria, and V. pavonis), and this suggests that there only two of the 243 species recorded in swamps were may be a core group of tree species that are consistently recorded in all fi ve swamp plots illustrates this very high abundant in swamps at larger spatial scales. plot-to-plot variation. Th e fi ve plots we inventoried in swamps are too small a sample to off er any understanding of this swamp-to-swamp variation, which will in any case Pattern 2: swamp specialists account for very few require rigorous comparable data on variation in abiotic species and a minority of stems in swamps conditions. In the meantime, our data suggest that the obvious swamp-to-swamp variation in composition and struc- Of the 243 species recorded in swamps, 21 met our criteria ture exists side by side with strong predictable components: as swamp specialists. Together, these taxa represent slightly specifi cally, a suite of species that are likely to be present in less than a majority of stems in swamps (43.6%; Fig. 2), and

910 that proportion is lower when specialists are determined via For example, while the pattern is apparent in the published indicator species analysis (34.6%). Taken together with the datasets of three other large-scale inventories in upper large degree of species-level overlap between swamps and Amazonia (Duivenvoorden et al. 2001), it was not reported well-drained forest types (see next section), the tiny number in the articles describing them (Duque et al. 2001, Grá ndez of swamp specialists (Ͻ 2% of all species recorded in our et al. 2001, Romero-Saltos et al. 2001). Reviewing a dataset Yasuní tree inventory) suggests that evolutionary pressures collected in 30 0.1-ha plots in Caquetá , Colombia, and on trees to specialize on the specifi c environmental condi- published as appendices by Duivenvoorden et al. (2001), tions in swamps have been rather weak over the several we found that 60.9% of tree species recorded in palm million years that swamp forests have existed in the upper swamps were also recorded in adjacent well-drained habitats. Amazon (Hoorn et al. 2010). Th e fi gures we calculated for data collected by the same Th e apparently tiny guild of swamp specialists we research group in Ampiyacu, Peru, and Yasun í (a study inde- observed also calls into question the commonly voiced pendent of ours, but sharing some study sites) are 74.2 and idea that habitat heterogeneity and its associated beta diver- 76.7% respectively (Duivenvoorden et al. 2001). For these sity inevitably increase gamma diversity on tropical fi ve studies, spanning 11 degrees of latitude in Ecuador, forest landscapes. If the ∼ 194 000 ha of swamp forests in Peru, and Colombia, the mean proportion of swamp species Yasuní National Park really are contributing Ͻ 30 unique that were also recorded in adjacent well-drained forest types tree species to the regional tree fl ora, it is possible to argue was 76.0%. Th at most of the swamp tree fl ora at a site also that the regional tree diversity would be higher if habitat occurs in well-drained forest at the same site thus appears heterogeneity were lower, i.e. if there were no swamps on to be a general feature of western Amazonian forests. the landscape. Th is is best illustrated by an extrapolation It is worth distinguishing this point from the observation from our data, which suggests that the two most common that well-drained habitats in Amazonia sometimes contain swamp specialists (Mauritia fl exuosa and Mauritiella small patches of poorly drained substrate where swamp armata) should have a combined population of ∼ 86 million species may occur. While we have occasionally observed adult trees in the swamp forests of Yasuní National Park. Mauritia fl exuosa palms growing in small swampy patches on It seems undeniable that if those stems were somehow upland terraces in western Amazonia, such patches were removed from swamps and added to Yasuní ’ s extremely not present in the well-drained plots we studied in Yasun í diverse and specialist-rich upland forests (i.e. by extending and are not the reason for the signifi cant compositional the upland tree species– area curve with an additional 130 overlap that we and others have documented between 000 ha of uplands), they would contribute more than swamps and well-drained forests. two species to the region’ s gamma diversity. Th is is clearly a Th e fi ve studies cited above also agree that the high simplistic extrapolation to a complex question, however, proportion of swamp species occurring in other forest and should not be mistaken for evidence that swamps types is an underestimate, since the small number of plots contribute little to regional diversity. It may be that swamps established at each site will under-sample the true number in Yasun í contribute few specialist trees but a large number of species that grow in multiple forest types there. In of specialist shrubs, vines, or herbs to the regional fl ora. both Caquetá (Duque et al. 2001) and Yasuní (Romero- Alternatively, some of the 139 tree species we characterized Saltos et al. 2001), species-individual curves for woody in this study as ‘ too rare’ or ‘ other ’ may eventually be plants in palm swamps and well-drained forests did not shown to require swamps for their long-term persistence on reach an obvious asymptote. Likewise, Romero-Saltos the landscape. et al. ’ s (2001) inventory of 0.1-ha plots in Yasuní swamps Finally, it is interesting to note that an unusually recorded several species that are considered upland oli- large proportion of the Yasuní swamp specialists listed in garchs in our study but which our own swamp plots Table 4 remain unidentifi ed to species (4 taxa) or genus (3). did not record. Th us, while our study in Yasun í tallied 203 Most of these seven morphospecies have been matched tree species that grow in both swamps and well-drained with fertile specimens that have been deposited in the habitats there, the true number is probably much higher. Missouri Botanical Garden for more than a decade, but a And given that our inventory recorded a total of 596 recent review of their status confi rmed that they are still species growing as adults in swamp and fl oodplain plots unidentifi ed. Th is suggests that the small group of tree at Yasuní , it seems reasonable to suppose that the true species that specialize on swamps may feature a relatively number of fl ood-tolerant tree species in the Amazon basin high rate of undescribed taxa. A similar pattern has been is much higher than Junk’ s (1989) estimate of 1000. observed for the broader swamp fl ora of Peru ’ s southern Th e signifi cant overlap in the tree fl oras of swampy Amazon (J. Janovec pers. comm.). and well-drained habitats suggests that the ability to survive on permanently waterlogged substrates is a feature shared by a large segment of the upper Amazonian tree fl ora. Th is is Pattern 3: Most tree species in swamps also occur not surprising, considering the region’s everwet climate; in adjacent well-drained forest types even soils considered to be very well drained may in fact be saturated for weeks on end during especially rainy periods. Nearly all of the species we recorded in swamps (83.5%) Th is implies that all species in Yasun í are adapted to were also recorded in well-drained habitats. While this is not some extent to waterlogged soil conditions, which in turn a novel observation for Amazonian forests (see Pitman et al. makes it unsurprising that some of the tree species common 1999 for similar fi gures from southern Peru), it is much in well-drained forest types in Yasun í have been character- more widespread than has been reported in the literature. ized as swamp specialists in drier regions of South America

911 (e.g. Tapirira guianensis , Richeria grandis, and Guarea to which their seedlings in swamps are the product of macrophylla in non-Amazonian Brazil, ﬁ de Teixeira and propagules from other forest types, the provenance of these Assis 2011). putative spillover populations in swamps must be considered unknown.

Pattern 4: many tree species in swamps are common in well-drained forests Synthesis and questions for future work

Th e tree species in swamps that are common in well- Th e data presented here suggest that the conventional drained forests fall into two very diff erent categories: picture of Amazonian swamp forests – a forest type domi- 1) a small group of species that are common on both nated by specialist tree species uniquely adapted to very wet waterlogged and well-drained soils, and 2) a large group of soil conditions – is incomplete. We found that while special- species that are rare in swamps but common in other forest ists are unquestionably important in swamps, they are types. accompanied there by two important non-specialist guilds: Th e fi rst group is typifi ed by the eight ‘ super-oligarch ’ one composed of species that are common and frequent species, as well as the eight other swamp oligarchs that across both swamps and well-drained forests (super- are also oligarchs in either upland forests or fl oodplain for- oligarchs) and the other composed of species that are ests (Table 4). Th is overlap of common species between common in well-drained forests but occur only occasionally swamp, fl oodplain, and upland tree communities in Yasuní in swamps (spillover). Indeed, these two non-specialist is most strikingly illustrated by the palm Iriartea deltoidea . guilds account for a much larger proportion of species and Although Iriartea is the most common tree in the region’s a comparable proportion of stems in swamps as the two upland forests (where it averages 45 individuals ha Ϫ 1 ; specialist guilds (strict and functional specialists; Fig. 2). Pitman et al. 2001), its mean density is even higher in Th ese observations help bring our understanding of tree swamps (69 ind. ha Ϫ 1 ), where it ranks as the third most communities in Amazonian swamps up to date with that of common species. Given that the species is also the most wetland plant communities in the temperate zone, where common tree in fl oodplain forests (36 ind. ha Ϫ 1 ), the ques- community composition and structure are commonly tion of habitat preference in Iriartea deltoidea at large understood to depend not merely on local environmental spatial scales in Yasun í seems moot. It would appear that the conditions but also on the age, size, shape, and spatial species is not spilling over from a source to a sink, but is arrangement of swamp habitat (Hors á k et al. 2012), on simply outcompeting other species in dispersing to and the composition and diversity of adjacent, non-swamp establishing in recruitment sites in all three forest types. vegetation (Ashworth et al. 2006, Hettenbergerová and Svenning (1999) reported a similar result for I. deltoidea H á jek 2011), and on the dispersal of propagules both in various microhabitats of a 50-ha upland plot at Yasuní . In between swamps and from outside swamps (Houlahan et al. a study of liana communities at Yasun í , Burnham (2002) 2006). Th ey also point to the somewhat counterintuitive likewise found one species to be the most common in both conclusion that the tree species composition and structure upland and fl oodplain forests: Machaerium cuspidatum of a given Amazonian swamp depend just as strongly on (Fabaceae). It is a high priority to understand the mecha- the tree species composition and structure of the surround- nisms that allow these species to consistently outcompete ing non-swamp forests as they do on the local guild the other Ͼ 1000 woody plant species in eastern Ecuador. of swamp specialists. In turn, this helps explain Terborgh It would also be useful to know how long these super- and Andresen’s (1998) unexpected fi nding that fl ooded oligarchs have dominated Yasun í ’ s forests (i.e. whether an forests in a given region of the Amazon are fl oristically adaptation that evolved relatively recently has allowed them more similar to unfl ooded forests in that same region than to become common by off ering them a temporary escape they are to fl ooded forests in other regions. from natural enemies, or whether they have been outcom- Given our fi nding that a species ’ likelihood of occurring peting competitors for millennia). in a swamp increases with its abundance in non-swamp Th e second and much more diverse group consists of forest types, seed dispersal in particular may play a much species that are relatively rare in swamps but common in more important role than previously appreciated in struc- well-drained habitats. Th is group is typifi ed by the 59 spe- turing Amazonian swamp communities. Very little is known cies that are oligarchs in well-drained habitats (and account about dispersal processes within swamps and between for ∼ 50% of stems there) but not oligarchs in swamps, swamps and well-drained forest types, however, and how where they represent just 6.9% of stems. Th is very diverse they intersect with environmental fi lters in swamps. Much but numerically trivial component of the swamp commu- of the data that is currently absent from the discussion nity could refl ect occasional spillover into swamps of species could be obtained by a combination of descriptive tech- that prefer well-drained habitats (Shmida and Wilson 1985, niques (seed traps, phenological monitoring, seedling plots, Rivas 2006). Given that these species survive to adulthood analyses of genetic structure in populations of species that in swamps, it should not be automatically assumed that occur in both swamp and well-drained habitats) and experi- their tiny spillover populations there represent an ecological mental approaches (transplant and germination experi- sink (i.e. populations that would not persist without ments) along transects extending from well-drained forest the input of propagules from other forest types). Until addi- into mixed and monodominant M. fl exuosa swamp forests. tional studies can determine the extent to which these spe- If the transects in that study were arranged so as to allow cies are capable of regenerating in swamps, and the extent one to separate the eff ects of distance from well-drained

912 habitats from the eff ects of environmental conditions y ecolog í a de plantas. Pontifi cia Univ. Cat ó lica del Ecuador, expected to co-vary with that distance (e.g. peat depth, pp. 275 – 278. fl ooding intensity), it could yield valuable insights regard- Dick, C. W. et al. 2003. Molecular systematics reveals cryptic ing the degree to which environmental mechanisms and Tertiary diversifi cation of a widespread tropical rainforest tree. – Am. Nat. 162: 691 – 703. dispersal are responsible for structuring tree communities in Ducke, A. and Black, G. A. 1953. Phytogeographical notes on tropical forests. the Brazilian Amazon. – An. Acad. Bras. Cienc. 25: 1 – 46. Dufr ê ne, M. and Legendre, P. 1997. Species assemblages and indicator species: the need for a fl exible asymmetrical approach. Acknowledgements – We thank the following people for assistance – Ecol. Monogr. 67: 345 – 366. during the swamp portion of the fi eld work in Yasun í : Humberto Duivenvoorden, J. F. 1995. Tree species composition and Awa, Th omas Delinks, Edmundo Pé rez, Miles Silman, Wepera rain forest – environment relationships in the middle Caquet á Tocari, and Salvador. We are grateful for the hospitality shown to area, Colombia, NW Amazonia. – Vegetatio 120: 91 – 113. our fi eld teams in the Huaorani communities of Dicaro and Duivenvoorden, J. F. 1996. Patterns of tree species richness in Guiyero, and for institutional support during fi eld work from the rain forests of the Middle Caquetá Area, Colombia, NW Yasun í Scientifi c Station, the Tiputini Biodiversity Station, Amazonia. – Biotropica 28: 142 – 158. the Pontifi cia Univ. Cat ó lica del Ecuador, and the San Francisco Duivenvoorden, J. F. et al. (eds) 2001. Evaluaci ó n de recursos de Quito Univ. Rick Condit calculated Sorenson’s similarity vegetales no maderables en la Amazon í a noroccidental. – IBED, scores for all pairwise plot comparisons. Euridice Honorio and Univ. van Amsterdam. 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Supplementary material (Appendix ECOG-00774 at Ͻ www.ecography.org/readers/appendixϾ ). Appendix 1.

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