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

14 Pages·2014·4.63 MB·English

Ecography 37: 001–014, 2014
doi: 10.1111/ecog.00774
© 2014 Th e Authors. Ecography © 2014 Nordic Society Oikos
Subject Editor: Jens-Christian Svenning. Accepted 21 February 2014
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 (cid:2) 10% of species and a minority
of stems; 3) most tree species recorded in swamps ((cid:3) 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 Cer ó 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 Mej í 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 M auritia 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, Cer ó n et al. 2003, Normand et al. 2006, and temporal variation in fl ooding intensity, depth, water
Early View (EV): 1-EV
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 (cid:4) 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), Grá 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)
∗
S ymphonia 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, Sch ö 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, Mac í 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?
2-EV
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 (cid:2) 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 Vegetaci ó 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 sub-
strates 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 (cid:3) 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
Yasun í National Park in Ecuador. (C) Th e northwestern portion of Yasun í 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 M auritia fl exuosa swamps and mixed swamps.
3-EV
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 Yasun í (% clay (cid:3) % silt (cid:3) % sand; plain plots measured 100 (cid:5) 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 M auritiella
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 Yasun í : 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
A ll swamp plots were (cid:2) 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 classi-
fying swamp vegetation, the swamp forests we studied in
Yasun í appear to correspond to ‘ p alm swamps and forest Analyses
swamps ’ sensu Kalliola et al. (1991), ‘ swamp forests ’
sensu Herrera-MacBryde and Neill (1997), ‘ l owland 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 (cid:4) 1 individual ha (cid:6) 1 in the uplands.
Iquitos, Peru (Encarnaci ó 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 (cid:4) 1 individual ha (cid:6) 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 (cid:4) 1 individual
in fl oodplains (1997 – 1999), and 15 sites in the uplands ha (cid:6) 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 (cid:4) 10 cm dbh, density in swamps of (cid:4) 1 individual ha (cid:6) 1 , for which (cid:4) 80%
with the exception of one swamp site (Tiputini 4) where we of all individuals were recorded in swamps, and that did not
4-EV
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 (cid:4) 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 (Dufr ê ne and a single tree.
Legendre 1997). While the ISA provides some additional
context for the results of the arbitrary thresholds, we gave pre-
cedence to the latter due to their simplicity and transparency. Swamp oligarchs
To summarize the results of the above analyses we quanti-
Tree communities in swamps were dominated by a strong
fi ed the proportion of all stems and of all species in swamps
oligarchy. Th irty of the 243 species recorded in swamps
that qualifi ed for the three categories of distribution and
qualifi ed as oligarchs there, and these accounted for
abundance described above: strict swamp specialists, func-
59.0% of stems and 12.3% of species in swamps. Within
tional swamp specialists, and super-oligarchs. Species that
individual swamp plots, swamp oligarchs accounted for
did not fall into any of these three categories were classifi ed
between 38.6 and 86.3% of all stems (average (cid:7) 61.0%).
into one of three additional categories: ‘ too rare ’ (species rep-
resented by (cid:8) 4 stems in the entire dataset and thus consid- Th e lowest value is from the Dicaro 3 plot, where nearly half
of stems belonged to a non-oligarch palm (M auritiella
ered too rare for their distribution to be characterized),
armata ) which we recorded nowhere else. Th e most common
‘ spillover ’ (defi ned arbitrarily as species that were represented
in the entire dataset by (cid:4) 5 stems, (cid:2) 13% of which were in swamp oligarchs were the palms Iriartea deltoidea (ranking
swamps), and ‘ other ’ (for all other species). Th e (cid:2) 13% value no. 1 in abundance in two plots) and M auritia fl exuosa
(ranking no. 1 in two plots; Table 3). Despite the clear
in the spillover defi nition comes from a binomial probability
dominance of palms, the 30 swamp oligarchs were a
calculation based on the fact that swamp stems account for
taxonomically diverse group, including 28 genera in 16
19% of the entire dataset; that calculation shows that species
with (cid:2) 13% of their stems in swamps are signifi cantly rarer families (Supplementary material Appendix 1).
in swamps than expected (p (cid:7) 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 (cid:6) 1 597 546 654
Mean species ha (cid:6) 1 74 189 239
Mean basal area ha (cid:6) 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
5-EV
Table 3. The ten most abundant tree species in fi ve 1-ha inventories in swamp forests in Yasun í , 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) 9 Sterculia apeibophylla 12
Sterculia apeibophylla 8 A peiba 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 S loanea ‘ 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 (cid:7) top ten in multiple plots
Euterpe precatoria* * 23 ∗ ∗ (cid:7) palm
Hieronyma alchorneoides var. estipulosa 19 (S) (cid:7) 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 func-
tional 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: M auritiella armata (12.7% of all swamp
stems) and M auritia 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 Yasun í , Ecuador, that belong to four diff erent
Table 4). Th e other three swamp indicators (E uterpe 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.
6-EV
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 Yasun í 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 propor-
tions 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 (cid:2) 0.0001). Th e same pattern held for
7-EV
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 Species ind. 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
Elaeocarpaceae S loanea ‘ bark ’ (NP3478)# 52 4 1 strict
Euphorbiaceae Hieronyma alchorneoides var . estipulosa # 45 4 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
Combretaceae B uchenavia amazonia # 18 4 1 functional
Malvaceae Sterculia frondosa 18 3 1 1
Urticaceae Coussapoa trinervia # 17 4 1 strict
Clusiaceae Symphonia globulifera # 16 4 1
Malvaceae Theobroma subincanum 12 3 1 1 1
Lauraceae Lauraceae ‘ palermo ’ (NP4484) 11 1 functional
Euphorbiaceae Sapium ‘ garcinia ’ (NP2855) 10 2 functional
Sapotaceae P outeria ‘ tenuipetiole ’ (NP3323) 9 3 1 1
Combretaceae Buchenavia viridifl ora 8 1 strict
Rubiaceae Ferdinandusa guainiae 8 1 strict
Annonaceae Unonopsis fl oribunda 7 3 1 1
Euphorbiaceae Alchornea ‘ webster ’ (NP4461)# 7 3 1 strict
Euphorbiaceae Euphorbiaceae ‘ nondescript ’ (NP4465) 7 1 strict
Malvaceae Sterculia colombiana 7 3 1 1 1
Moraceae Ficus piresiana 7 4 1
Euphorbiaceae Conceveiba 1 (NP1461) 6 3 1 1
Fabaceae Macrolobium acaciifolium 6 2 strict
Lecythidaceae Couroupita guianensis 6 3 1 1
Sapindaceae Sapindaceae ‘ chalky ’ (NP4560) 6 2 functional
Clusiaceae Vismia ‘ myrsinac ’ (NP1490) 5 2 strict
Fabaceae Machaerium fl oribundum 5 3 1
Sapotaceae Pouteria cuspidata ssp. robusta 5 3 1
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 (cid:2) 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 Yasun í 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.
8-EV
Figure 4. Th e proportions of all species and stems surveyed in fi ve 1-ha swamp plots in Yasun í , 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 Yasun í 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 Yasun í uplands could identify half of the standing grow on peaty substrates in Yasun í . 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 (cid:4) 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, Mac í a and Svenning 2005, Caquet á , Colombia, includes only three of our 30 swamp
Mac í a 2008, 2011, Fine et a l. 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 a l. 2001). Th ere is, however,
in Yasun í 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 obvi-
ous 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
9-EV
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, Gr á ndez
of swamp specialists ((cid:2) 2% of all species recorded in our et al. 2001, Romero-Saltos et al. 2001). Reviewing a dataset
Yasun í 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
Yasun í National Park really are contributing (cid:2) 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 (M auritia 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 Yasun í 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– a rea 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 Caquet á (Duque et al. 2001) and Yasun í (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 Yasun í swamps
Finally, it is interesting to note that an unusually recorded several species that are considered upland oli-
large proportion of the Yasun í 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 Yasun í , 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
not surprising, considering the region’s everwet climate;
Pattern 3: Most tree species in swamps also occur
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
10-EV