Journal of Vegetation Science && (2014)

Patterns of tree diversity and composition inAmazonian floodplain paleo-v�arzea forest

Rafael L. Assis, Torbjørn Haugaasen, Jochen Sch€ongart, Juan C. Montero, Maria T.F. Piedade& FlorianWittmann

Keywords

Alluvial dynamism; Amazonia; Floodplain

forest; Neotropics; Paleo-v�arzea; Similarity

analysis; Substrate fertility; Tree diversity

Abbreviations

GNMDS = Global non-metric multidimensional

scaling; ANOSIM = Analysis of similarity

ISA = Indicator species analysis.

Nomenclature

The International Plant Names Index (2012),

http://www.ipni.org (accessed June 2013)

Received 11 December 2013

Accepted 4 August 2014

Co-ordinating Editor: Kerry Woods

Assis, R.L. (Corresponding author,

rafael.assis@nmbu.no) & Haugaasen, T.

(torbjorn.haugaasen@nmbu.no): Department

of Ecology and Natural Resource Management,

Norwegian University of Life Sciences, P.O. Box

5003,�As 1432, Norway

Assis, R.L. , Sch€ongart, J.

(jochen.schongart@inpa.gov.br) &

Piedade, M.T.F (maitepp@inpa.gov.br):

Instituto Nacional de Pesquisas da Amazonia,

Av. Andr�e Ara�ujo 2.936, Manaus-AM, CEP

69.067-375, Brazil

Montero, J.C.

(monterotjuancarlos@gmail.com): Faculty of

Environment and Natural Resources, University

of Freiburg, Tennenbacherstrasse 4, Freiburg

79106, Germany

Wittmann, F. (f-wittmann@web.de):

Biogeochemistry Dep., Max Planck Institute for

Chemistry, Hahn-Meitner Weg 1, Mainz 55128,

Germany

Abstract

Question: In a recent re-classification of Amazonian floodplain types, a new

category was established for paleo-v�arzea. Although the geological basis for this

classification is sound, a key question is whether it can be supported by botanical

criteria, where floodplain paleo-v�arzea forests contain distinct tree assemblages

compared to other major floodplain types.

Location: Central Amazonian floodplains, Brazil.

Methods: We used 41 tree inventories from floodplain paleo-v�arzea, v�arzea

and igap�o forests to perform a meta-analysis. Diversity and richness estimators

were applied at the level of genus and the examination of floristic composition

was performed at family and generic levels. Generic composition across the

three floodplain types was investigated using GNMDS and cluster analysis. Simi-

larity coefficients and ANOSIM were applied to quantify floristic resemblance at

the generic level between forest types. Indicator species analysis (ISA) was used

to identify any indicator genera for the forest types evaluated.

Results: Alpha diversity and generic richness in paleo-v�arzea forest was similar

to v�arzea. Igap�o forest was clearly the least diverse. Family compositionwas sim-

ilar across the three forest types; Fabaceae was the dominant family on all three

floodplains. Pouteria, Licania and Eschweilera presented the highest importance

values in paleo-v�arzea, but these genera were also important in v�arzea and

igap�o. Nevertheless, ANOSIM analyses show that generic composition differed

significantly between the three forest types, and a GNMDS ordination and clus-

ter analysis portrays paleo-v�arzea tree composition as intermediate between

v�arzea and igap�o. ISA revealed that Euterpe, Dipteryx and Goupia were the most

important indicator genera of paleo-v�arzea.

Conclusions: We conclude that paleo-v�arzea floodplain tree assemblages are

dissimilar to those of v�arzea and igap�o, but contain components typical of both

these floodplain types, explaining their intermediate positioning in our analyses.

This floral mix probably allows paleo-v�arzea alpha diversity to be similar to that

of v�arzea.

Introduction

Amazonian floodplains subjected to predictable, long-last-

ing, monomodal flood pulses extend to an area of ca.

600 000 km2 (Melack & Hess 2010), most of which is cov-

ered by forest. Trees are subjected to alternating terrestrial

and aquatic phases (flood pulse, sensu Junk et al. 1989)

with seasonal inundations of up to 230 days�yr�1. Many

physical and ecological processes, such as mineral cycling,

decomposition and forest succession, are influenced by the

flood pulse, and species inhabiting these environments

have developed morpho-anatomical and physiological

adaptations to deal with the seasonal flooding (Parolin

et al. 2004).

1Journal of Vegetation ScienceDoi: 10.1111/jvs.12229© 2014 International Association for Vegetation Science

Several different forest types are recognized within

Amazonian floodplains. An initial classification was based

on hydrochemical (Sioli 1956) and floristic (Prance 1979)

differences. Floodplain forests along white-water rivers,

such as the Amazon mainstem, Purus and Madeira, are

known as v�arzea forests and cover an area of ca.

275 000 km2 (Irion et al. 2010; Melack & Hess 2010).

These rivers carry large amounts of nutrient-rich Tertiary/

Quaternary sediments originating from the Andes or pre-

Andean regions. Due to the seasonal influx of nutrients,

white-water floodplains remain exceptionally productive

(Junk & Piedade 1993). The high content of suspended

sediments induces a highly dynamic system, characterized

by intense sedimentation and erosion processes (Witt-

mann et al. 2004; Peixoto et al. 2009). This alluvial dyna-

mism creates a patchwork of habitats, which together with

highly fertile substrates, are thought to be the underlying

reasons for v�arzea forest having the highest tree species

richness of any floodplain forest worldwide (Wittmann

et al. 2006).

Forests inundated on a seasonal basis by either black- or

clear-water rivers are collectively known as igap�o and

cover ca. 180 000 km2 of the Amazon Basin (Melack &

Hess 2010). These rivers (e.g. Negro, Tapaj�os and Tocan-

tins) originate in Precambrian formations, such as the Gui-

ana Shield and Central Brazilian Shields for black-water

and clear-water, respectively (Irion et al. 2010). They carry

a reduced load of suspended inorganic elements compared

to white-water rivers, and floodplain fertility is therefore

much lower than that of the v�arzea. Furthermore, river-

beds and associated floodplains have low geomorphic

dynamics, being relatively stable over several thousands of

years (Irion et al. 2010).

In addition to v�arzea and igap�o, another floodplain type

was later recognized – floodplain paleo-v�arzea. Floodplain

paleo-v�arzeas were first described by Irion (1976) and have

been referred to as Pleistocene v�arzeas (Irion 1976, 1978;

Klammer 1984), abandoned floodplains (Salo et al. 1986)

or ancient v�arzea (Ayres 1993). They are dated to the

Mid-/Late Pleistocene when, during periods of higher sea

levels, the Amazonian floodplains were much more exten-

sive than today (Irion 1976, 1984; Klammer 1984). During

periods of high sea levels, water from the Amazon river

systemwas effectively dammed. Due to the low inclination

of the basin, lowlands up to 2500 km from the coast were

affected and large areas of the basin were flooded and

dominated by freshwater systems rich in Andean sedi-

ments (Irion et al. 1995). Paleo-v�arzea forest is located on

alluvial Andean deposits abandoned bywhite-water rivers.

They are flooded by small to intermediate black-water

rivers, which transport these once-deposited Andean

paleo-sediments (Irion et al. 2010). The surface substrates

of paleo-v�arzea are therefore less fertile than v�arzea, but

remain more fertile than igap�o (Irion 1978; Schubart

1983). Recent estimates indicate that paleo-v�arzeas cover

at least 125 000 km2, with the largest expanses found in

the states of Amazonas and Par�a in the Brazilian part of the

Amazon (Melack & Hess 2010). Until recently paleo-

v�arzea was not recognized as a distinct floodplain type.

However, applying the above information to a re-classifi-

cation of floodplain types in the Amazon, Junk et al.

(2011) proposed that floodplain paleo-v�arzeas should be

classed as a distinct floodplain category.

The literature on quantitative floristic inventories of

Amazonian floodplain forests is considerable, with several

studies available for v�arzea (e.g. Ayres 1993; Wittmann

et al. 2002; Haugaasen & Peres 2006; Assis & Wittmann

2011), but fewer for igap�o (e.g. Ferreira 1997; Ferreira &

Prance 1998; Parolin et al. 2004; Montero et al. 2014).

Comparative studies in central Amazonian floodplains

show that v�arzea generally support a higher number of

tree species than igap�o (Prance 1979; Kubitzki 1989; Witt-

mann et al. 2010). However, paleo-v�arzea tree assem-

blages are yet to be examined following the new

classification. Junk et al. (2011) suggest species composi-

tion is intermediate between v�arzea and igap�o, containing

floral components from both floodplain types. However,

although the geological basis for a new paleo-v�arzea cate-

gory is sound, no study to date has evaluated the botanical

criteria for this floodplain category.

In this paper, we examine the tree composition of

paleo-v�arzea forest to evaluate the botanical characteristics

of this category of floodplain forest in the Central Amazon.

Our main objective is to investigate patterns of community

assembly across three floodplain forest types: igap�o, v�arzea

and paleo-v�arzea. We used 41 Amazonian floodplain tree

inventories from igap�o, v�arzea and paleo-v�arzea and use

these data to address the following questions: (1) does tree

alpha diversity in paleo-v�arzea differ from v�arzea and

igap�o; (2) which are the most important taxa in each forest

type; (3) what is the degree of floristic similarity between

forest types; and (4) are there any tree genera characteristic

of the different forest types?

Methods

Data preparation

Our database consists of 41 published and unpublished flo-

ristic inventories (App. S1) in floodplain forests from seven

central Amazonian river basins (Fig. 1). We considered

only inventories that met the following criteria: (1) sur-

veyed floodplain forests subjected to predictable, long-last-

ing, monomodal flood pulses; (2) surveyed late

successional stages of floodplain forests (according to

Wittmann et al. 2010), in order to decrease the influence

of different flooding regimes on floristic similarity between

Journal of Vegetation Science2 Doi: 10.1111/jvs.12229© 2014 International Association for Vegetation Science

Tree diversity and composition in paleo-v�arzea forests R.L. Assis et al.

plots; (3) provided data on the number of individuals; (4)

inventoried trees with DBH ≥ 10 cm; and (5) identified

trees at least to genus level. In general, we tried to restrict

our analysis to inventories of a minimum size of 1 ha, but

two inventories comprising <1 ha (0.75 and 0.8 ha) were

included due to the scarcity of data from those regions.

Inventories were categorized following the new classifi-

cation of Junk et al. (2011) as: (1) igap�o forest, flooded by

nutrient-poor black-water; (2) paleo-v�arzea forest, located

on paleo-v�arzea substrates and flooded by black-water riv-

ers of intermediate fertility; and (3) v�arzea forest, flooded

by nutrient-rich white-water rivers. Published material on

Amazonian geomorphology and hydrology (e.g. Martinelli

et al. 1989; Mertes et al. 1996; CPRM 2006; McClain &

Naiman 2008) were thoroughly consulted for an accurate

classification of the inventories.

Due to a large number of morpho-species in the data set

(ca. 35%) our analyses are restricted to family and genus

levels. Previous studies show that tree community patterns

at species and genus levels are very similar (Higgins &

Ruokolainen 2004; Coronado et al. 2009). All genus and

family names were verified and validated using different

sources, such as C.V. Starr Virtual Herbarium (NY) (http://

sciweb.nybg.org), w3Tropicos (http://mobot.mobot.org/

W3T) and The International Plant Names Index (http://

www.ipni.org). Unidentified trees and trees with names

not mentioned in the consulted herbaria were excluded

from the analysis.

Statistical analyses

The alpha diversity was calculated using Fisher’s alpha

coefficient (Fisher et al. 1943) at generic levels, which is

relatively insensitive to sample size and is widely applied to

data from plot-based floristic inventories (e.g. ter Steege

et al. 2000; ter Steege et al. 2003). Differences in alpha

diversity between floodplain types were examined with

Mann–Whitney U-tests, with a significance level at

P < 0.05. To examine the patterns of total genus richness

between forest types, we rarefied the number of genera

based on the number of individuals, rather than samples,

in order to remove the effects of tree density (Gotelli & Col-

well 2001).

Following Wittmann et al. (2006), we calculated the

overall relative importance (ORI) for each family and

genus. This is a modification of the importance value index

(Curtis & McIntosh 1951) and combines the sum of rela-

tive abundance (percentage of total number of trees per

Fig. 1. The Amazon river network derived from SRTM (Shuttle Radar Topography Mission) elevation data at 500-m resolution, showing the selected tree

inventories in the Amazonian floodplains. The distribution of major white-water, black-water and paleo-v�arzea floodplain river basins of the central-western

Amazon are highlighted in yellow, black and red, respectively. Names of the major rivers are shown and the numbers refer to inventory plots listed in

Appendix S1.

3Journal of Vegetation ScienceDoi: 10.1111/jvs.12229© 2014 International Association for Vegetation Science

R.L. Assis et al. Tree diversity and composition in paleo-v�arzea forests

plot) and relative frequency of a genus (number of plots in

which a given genus or family was recorded).

To evaluate patterns of floristic similarity between the

three forest types, we performed global non-metric mul-

tidimensional scaling (GNMDS; Minchin 1987) and hier-

archical clustering analysis with group-average linking

(UPGMA). Both analyses were performed using the Len-

non dissimilarity index (Lennon et al. 2001). Based on a

goodness of fit between the ordination distances and the

original dissimilarity distances (Sheppard plot) and

GNMDS stress values, the Lennon index performed bet-

ter than other indices tested (Bray-Curtis, Jaccard, Simp-

son). The Lennon index is an adjusted form of the

Simpson’s index, and appears to perform better for data

containing species with few occurrences (Chao et al.

2006). All plots were truncated to a standard of 241 ran-

domly chosen trees (the number of trees contained in

the plot with lowest tree density) in order to weight plots

equally.

Two similarity coefficients were calculated for each

forest type: Chao shared estimator (Chen et al. 1995) and

Chao–Sørensen abundance-based estimator (Chao et al.

2005). In the Chao shared estimator coefficient, the

observed number of shared species is augmented by a cor-

rection term based on the relative abundance of the rare

species shared. The Chao–Sørensen abundance-based esti-

mator coefficient is based on the probability that two ran-

domly chosen individuals (one from each of two forest

types) belong to a genus shared by both forest types. In

addition, it estimates the probability of such a genus being

present in both forest types but not detected in one or both

of these. These approaches substantially reduce the nega-

tive bias of traditional similarity indices when working

with incomplete sampling of rich communities (Chao et al.

2005).

An analysis of similarity (ANOSIM) was performed to

examine significant differences in genus composition

between the three forest types. This analysis includes a

nonparametric permutation test equivalent to an ANOVA

for similarity matrices (Clarke 1993), and we used the Len-

non similarity index for the analysis. The ANOSIM was

calculated based on 5928 randomly chosen tree individuals

– the total number of trees from the igap�o inventories,

which was the lowest across the three floodplain forest

types examined.

Indicator species analysis (ISA) was used to determine

whether a specific genus was a good indicator for one of

the three forest types evaluated. For each genus, the analy-

sis provides an indicator value (IndVal; Dufrene & Legen-

dre 1997), which is highest when a genus is present in all

plots of one forest type and absent in all plots of the other

forest types. Statistical significance was tested using a per-

mutation test with 1000 iterations.

Similarity coefficients were computed using EstimateS

(v. 7.5; http://purl.oclc.org/estimates). All other analyses

were performed in R (v 2.14.1; R Foundation for Statistical

Computing, Vienna, AT), using the packages ‘MASS’

(Venables & Ripley 2002) for GNMDS, ‘indicspecies’ (De

C�aceres & Legendre 2009) for ISA and ‘vegan’ (Oksanen

2005) for the other analyses.

Results

Patterns of tree diversity

After excluding unidentified trees and trees with names

not found in the consulted herbaria, a total of 23 016 indi-

viduals were recorded in the 41 inventories (totaling

40.6 ha) belonging to 72 families and 285 genera. Fifteen

individuals (0.06% of the total) were identified only to

family and were used strictly in the family-level analysis.

Table 1 summarizes the information from the 41 invento-

ries according to forest type.

Fisher’s alpha coefficients for v�arzea were similar to

paleo-v�arzea and significantly higher than for igap�o

(Fig. 2). This pattern was also reflected in our rarefaction

curves (Fig. 3), where igap�o also had the lowest generic

richness, whereas generic richness in v�arzea and paleo-

v�arzea was similar (Fig. 3).

Tree assemblage composition

The five most common families were Fabaceae, Euphorbi-

aceae, Lecythidaceae, Sapotaceae and Annonaceae. These

families combined accounted for 47.9% of all trees

recorded and were present among the ten most important

families in all forest types (Table 2). Paleo-v�arzea shared

seven and eight of its ten most important families with

igap�o and v�arzea, respectively. Fabaceae had the highest

overall relative importance (ORI) value in all three forest

types and was the only family present in all inventories.

This family included 17.1% (4064 individuals) of the total

number of trees recorded, but wasmore important in igap�o

than in paleo-v�arzea or v�arzea (Table 2).

The 23 most common genera accounted for half

(50.3%) of all trees. Twenty-two genera were represented

by a single individual, while 49 genera were recorded in

just one inventory plot. Eschweilera, Hevea, Mabea and Pou-

Table 1. Number of inventories, area sampled, number of individuals,

families and genera according to forest type.

Forest Type Number

of Plots

Area (ha) Individuals Families Genera

Igap�o 10 9.7 5928 51 129

Paleo-v�arzea 12 12 7631 59 215

V�arzea 19 18.9 9457 61 229

Total 41 40.6 23,016 72 285

Journal of Vegetation Science4 Doi: 10.1111/jvs.12229© 2014 International Association for Vegetation Science

Tree diversity and composition in paleo-v�arzea forests R.L. Assis et al.

teria were among the most important genera in all forest

types (Table 3). The two most important genera in paleo-

v�arzea were also found among the two most important

genera in igap�o (Licania) and v�arzea (Pouteria).

Thirty genera recorded in paleo-v�arzea were not

observed in the other forest types. They represent 10.5%

of the total number of genera, and 13.9% of genera sam-

pled in paleo-v�arzea. V�arzea had the highest number of

exclusive genera (41.8%) and igap�o the lowest (7.75%).

Almost one-third of the genera (27.5%)were present in all

three floodplain forest types.

Inventories were loosely clustered in the GNMDS ordi-

nation according to floodplain type: igap�o plots were

located towards the left side of the ordination diagram,

v�arzea plots towards the right and paleo-v�arzea in an inter-

mediate position (Fig. 4). The results of the cluster analysis

echo those of the ordination analysis; Node A of the den-

drogram (Fig. 5) embraced eight of the ten igap�o forest

inventories and Node B contained all except one of the

v�arzea inventories. Paleo-v�arzea inventories were found

in both Node A and Node B, but also occupied an entire

sub-node (A–I; Fig. 5).

The ANOSIM confirmed that genus composition was

significantly different between igap�o and paleo-v�arzea

(r = 0.312, P = 0.002), paleo-v�arzea and v�arzea

(r = 0.226, P = 0.003), and igap�o and v�arzea (r = 0.719,

P < 0.001). The similarity coefficients show that paleo-

v�arzea is floristically most similar to v�arzea, although simi-

larity was only marginally higher compared to igap�o for

the Chao–Sørensen estimated coefficient (Table 4).

The ISA revealed several indicator genera for each forest

type (Table 5), but paleo-v�arzea had fewer significant indi-

cator genera (six) than igap�o (12) and v�arzea (19). Four of

the indicator genera in paleo-v�arzea (Goupia, Couratari,

Ecclinusa and Hymenolobium) were unique to this forest

type.

Discussion

Patterns of tree diversity

Paleo-v�arzea forest had similar levels of alpha diversity and

estimated generic richness to v�arzea forest, whereas igap�o

clearly had the lowest diversity. This is consistent with

previous studies showing that v�arzea forest is consistently

0

50

100

150

200

250

0 1000 2000 3000 4000 5000 6000 7000

Rar

efie

d nu

mbe

r of g

ener

a

Number of individuals

Igapó Paleo-várzea Várzea

Fig. 3. Rarefied number of genera (accumulated per 200 individuals) for each forest type. Vertical bars present SE of the mean.

Forest typeIgapó Paleo-várzea Várzea

Fish

er’s

alp

ha

Igapó x paleo-várzeaIgapó x várzeaPaleo-várzea x várzea

U = 44U = 21*

U = 95.58060

4020

Fig. 2. Box plots of mean (�SE) Fisher’s alpha coefficient for each forest

type. Mann–Whiney U results are presented in the figure. Asterisks

represent significance at P < 0.05.

5Journal of Vegetation ScienceDoi: 10.1111/jvs.12229© 2014 International Association for Vegetation Science

R.L. Assis et al. Tree diversity and composition in paleo-v�arzea forests

more species-rich than igap�o forest at the local scale

(Prance 1979). Our analyses suggest that these local obser-

vations also apply to a regional scale, at least in central

Amazonia, since the rarefaction curves (Fig. 3) suggest

that our sample is a reasonable representation of expected

number of genera for each forest type. However, this pat-

tern may be reversed locally in the eastern part of the

Amazon (see Ferreira et al. 2010).

Differences in diversity patterns may be influenced by

substrate characteristics. Wittmann et al. (2006) attributed

higher tree alpha diversity in western Amazonian white-

water floodplains compared to regions further east to

higher substrate nutrient levels in the western part of the

basin, a pattern also described for non-flooded terra firme

forests (ter Steege et al. 2006). It has also been shown that

more fertile substrates present higher productivity and,

consequently, higher turnover of individuals, which in

turn increases tree diversity (Baker et al. 2004).

Patterns of tree diversity may also be affected by differ-

ences in alluvial processes. For example, the intense

alluvial dynamism observed in v�arzea floodplains creates a

Table 2. Ten most important families, listed in descending order of overall relative importance (ORI), in each forest type.

Rank Igap�o R. Ab. R. Fr. ORI Paleo-v�arzea R. Ab. R. Fr. ORI V�arzea R. Ab. R. Fr. ORI

1 Fabaceae 23.98 3.78 27.77 Fabaceae 16.97 3.18 20.16 Fabaceae 13.46 2.96 16.42

2 Lecythidaceae 13.37 3.78 17.16 Sapotaceae 10.18 3.18 13.37 Euphorbiaceae 8.93 2.96 11.89

3 Euphorbiaceae 10.15 3.78 13.94 Euphorbiaceae 9.03 3.18 12.21 Annonaceae 8.46 2.96 11.42

4 Chrysobalanaceae 8.14 3.78 11.93 Chrysobalanaceae 7.58 3.18 10.76 Malvaceae 7.01 2.96 9.97

5 Sapotaceae 5.7 3.78 9.48 Lecythidaceae 7.37 3.18 10.55 Sapotaceae 5.57 2.96 8.53

6 Malvaceae 4.18 3.78 7.97 Annonaceae 6.08 3.18 9.26 Lecythidaceae 5.05 2.8 7.85

7 Annonaceae 3.57 3.78 7.36 Lauraceae 3.54 3.18 6.72 Myrtaceae 4.10 2.96 7.06

8 Lauraceae 2.88 3.78 6.67 Moraceae 3.89 2.73 6.62 Lauraceae 3.14 2.96 6.1

9 Rubiaceae 3.81 2.65 6.46 Myrtaceae 3.36 3.18 6.54 Polygonaceae 2.62 2.96 5.58

10 Melastomataceae 2.8 3.4 6.2 Arecaceae 3.33 2.50 5.83 Moraceae 2.69 2.8 5.5

∑ 1–10 78.63 36.36 115 ∑ 1–10 71.3 30.7 102 ∑ 1–10 61.07 29.28 90.35

∑ 11–51 21.37 63.63 85 ∑ 11–59 28.7 69.3 98 ∑ 11–61 38.93 70.71 109.6

R. Ab, Relative abundance, R. Fr, Relative frequency.

Table 3. Ten most important genera, listed in descending order of overall relative importance (ORI), in each forest type.

Rank Igap�o R Ab. R Fr. ORI Paleo-v�arzea R Ab. R Fr. ORI V�arzea R Ab. R Fr. ORI

1 Licania 6.76 1.94 8.7 Pouteria 6.77 1.5 8.26 Pouteria 4.24 1.32 5.56

2 Gustavia 6.69 1.35 8.05 Licania 6.20 1.5 7.7 Eschweilera 3.56 1.17 4.74

3 Eschweilera 5.92 1.94 7.86 Eschweilera 6.00 1.5 7.5 Pterocarpus 3.24 1.24 4.48

4 Heterostemon 5.87 1.55 7.42 Hevea 3.35 1.5 4.84 Mabea 2.8 1.32 4.12

5 Mabea 4.31 1.55 5.87 Mabea 3.46 1.17 4.64 Tabebuia 3.13 0.95 4.1

6 Hevea 3.82 1.94 5.77 Macrolobium 3.03 1.4 4.42 Guatteria 2.67 1.39 4.07

7 Mollia 3.2 1.74 4.95 Pterocarpus 2.95 1.28 4.23 Hevea 2.56 1.24 3.81

8 Pouteria 2.95 1.94 4.89 Guatteria 2.64 1.39 4.02 Inga 2.17 1.39 3.56

9 Aldina 2.91 1.74 4.66 Eugenia 2.27 1.17 3.45 Licania 2.19 1.24 3.43

10 Ocotea 2.61 1.94 4.55 Euterpe 2.39 0.75 3.13 Virola 2.61 0.8 3.42

∑ 1–10 45.1 17.67 62.76 ∑ 1–10 39.1 6.8 52.2 ∑ 1–10 29.22 12.1 41.4

∑ 11–129 54.9 82.33 137.24 ∑ 11–217 60.9 93.2 147.8 ∑ 11–321 70.78 87.9 158.6

R. Ab, Relative abundance; R. Fr, Relative frequency.

1

23

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5

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7

8 9

10

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2728

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41

IgapóPaleo-várzeaVárzea

0.3

0.2

0.1

0.0

–0.1

–0.2

–0.3

GN

MD

S2

GNMDS1

–0.4 –0.2 0.0 0.2 0.4

Fig. 4. GNMDS ordination diagram based on Lennon dissimilarity

distances from genus abundance and composition at 41 inventory plots

containing 241 randomly chosen tree individuals. Stress = 18.03.

Journal of Vegetation Science6 Doi: 10.1111/jvs.12229© 2014 International Association for Vegetation Science

Tree diversity and composition in paleo-v�arzea forests R.L. Assis et al.

patchwork of forest at various successional stages, thus

increasing beta diversity (Salo et al. 1986; Wittmann et al.

2006). Although we used only late successional forest sam-

ples for our study, these plots may have been influenced

by the proximity of zones in earlier stages of development

by e.g. facilitating seed dispersal into late successional for-

ests. Alternatively, patterns of tree diversity may be associ-

ated with the total area covered by each floodplain type as

the regional species pool increases with area (Rosenzweig

1995; ter Steege et al. 2000; ter Steege et al. 2003).

However, all the above hypotheses fail to explain the

high generic richness in paleo-v�arzea forest. Based on the

intermediate substrate fertility, decreased alluvial dyna-

mism and smaller area of this floodplain type, one would

expect paleo-v�arzea to have lower alpha diversity than

v�arzea forest. Since paleo-v�arzea tree assemblage composi-

tion was found to be intermediate between v�arzea and

igap�o (Fig. 4), thereby supporting the prediction of Junk

et al. (2011), we hypothesize that the high alpha diversity

is maintained due to a mixing of v�arzea and igap�o floras in

this forest type.

Tree assemblage composition

Many families showed similar levels of importance across

all three floodplain forest types. Fabaceae, which is the

most important family in most Neotropical forests (e.g.

3367

1211212022161415452

101389

39262327283513183436171929242532303137403841

A

B

I

II

III

IV

0.3 0.4 0.5 0.6 0.7

DissimilarityIgapóPaleo-várzeaVárzea

Fig. 5. Dendrogram from cluster analysis with group-average linkage

(UPGMA) performed using the Lennon dissimilarity index. Capital letters (A

and B) indicate main nodes, and sub-nodes (I-IV) are indicated with grey

rectangles. Inventory numbers correspond with those in Table 1.

Table 4. Incidence- and abundance-based coefficients of floristic similar-

ity between the three forest types.

Cross-Comparison Chao Shared Estimator Chao–Sørensen

Estimator

Igap�o9 Paleo-V�arzea 123.6 0.89

Igap�o9 V�arzea 101.8 0.74

Paleo-V�arzea9 V�arzea 176.8 0.94

Table 5. List of all significant indicator genera for each forest type accord-

ing to the ISA. Genera are listed in descending order of indicator value (Ind-

Val) within each forest type.

IndVal P

Igap�o

Aldina 0.95 0.005

Mollia 0.92 0.005

Heterostemon 0.88 0.005

Ormosia 0.82 0.015

Peltogyne 0.8 0.005

Calyptranthes 0.76 0.035

Pachira 0.73 0.025

Hirtella 0.7 0.03

Sacoglottis 0.69 0.05

Amphirrox 0.58 0.04

Roucheria 0.55 0.02

Lacunaria 0.5 0.045

Paleo-v�arzea

Euterpe 0.7 0.01

Dipteryx 0.61 0.01

Goupia 0.55 0.01

Couratari 0.5 0.035

Ecclinusa 0.5 0.035

Hymenolobium 0.5 0.045

V�arzea

Cecropia 0.86 0.005

Pseudobombax 0.84 0.005

Ficus 0.8 0.005

Sapium 0.76 0.005

Crataeva 0.69 0.015

Drypetes 0.76 0.005

Himatanthus 0.75 0.005

Luehea 0.74 0.03

Lecointea 0.72 0.005

Matayba 0.72 0.005

Triplaris 0.71 0.02

Spondias 0.65 0.02

Zanthoxylum 0.65 0.015

Symmeria 0.63 0.02

Lacistema 0.61 0.01

Hura 0.61 0.02

Acacia 0.61 0.035

Couroupita 0.56 0.025

Xylosma 0.56 0.025

7Journal of Vegetation ScienceDoi: 10.1111/jvs.12229© 2014 International Association for Vegetation Science

R.L. Assis et al. Tree diversity and composition in paleo-v�arzea forests

Gentry 1988; Terborgh & Andresen 1998; ter Steege et al.

2013), was also the dominant family in igap�o, paleo-v�arzea

and v�arzea. However, Fabaceae was much more important

in igap�o than in the other two forest types. This may partly

reflect the lower number of families recorded in this forest

type, allowing each family to gain higher dominance. It

has also been suggested that legumes are particularly suc-

cessful on nutrient-poor substrates (e.g. igap�o) due to their

high seed mass, providing them with an advantage over

trees from other families with smaller seeds (Janzen 1974;

ter Steege et al. 2006). Other differences at the family level

may also reflect edaphic properties. Lecythidaceae has

been considered amore characteristic family of poorer sub-

strates such as terra firme (Coronado et al. 2009) and igap�o

(Mori et al. 2001). This agrees with our data, where Lecyt-

hidaceae attained its highest ORI value in igap�o.

The results at the generic level reflect those at the fam-

ily level, where many of the most important genera were

shared among the three forest types. However, six genera

were identified as indicators of paleo-v�arzea forest

(Table 5), and four of these were exclusive to this forest

type. We also observe that many genera containing spe-

cies known to occupy early successional stages of flood-

plain forest (e.g. Cecropia, Luehea, Pseudobombax, Symmeria

and Triplaris; Wittmann et al. 2002, 2004) were among

the indicator genera for v�arzea (Table 5). The presence of

these typical pioneer taxa in late successional v�arzea forest

is probably a result of an elevated number of disturbance

events, such as fluvial erosion and gap formation, since

the alluvial dynamism in v�arzea floodplains is much

higher compared to the more stable (less sedimentation

and erosion) paleo-v�arzea and igap�o (Junk et al. 1989;

Wittmann et al. 2004).

Another interesting pattern that emerges from our data

is that some genera important in v�arzea have decreased

importance (lower ORI value) in paleo-v�arzea (e.g. Guat-

teria, Pterocarpus and Virola), whereas some genera impor-

tant in igap�o (e.g. Hevea, Licania and Mabea) were of

similar importance in paleo-v�arzea (Table 3). While the

combination of the above results accounts for the inter-

mediate positioning of paleo-v�arzea forest in the ordina-

tion diagram (Fig. 4), the latter observations may suggest

that paleo-v�arzea is gradually gaining species typical of

igap�o and losing species typical of the more nutrient-rich

and dynamic v�arzea floodplains. This appears consistent

with the interpretation that paleo-v�arzea floodplains are

in a transitional phase between v�arzea and igap�o (Salo

et al. 1986).

However, floristic composition of paleo-v�arzea forest

differed substantially across this ‘transitional’ gradient, and

the degree of similarity between paleo-v�arzea and either

igap�o or v�arzea may depend on several factors. First, more

recent paleo-v�arzea may contain higher abundance of

common v�arzea tree species due to higher substrate fertil-

ity, while older and less fertile paleo-v�arzea contain floral

elements of igap�o. This could explain why some paleo-

v�arzea sites of the present study were clustered close to

igap�o sites, while others were more similar to v�arzea

(Fig. 5) – even though floristic composition of paleo-

v�arzea forest was significantly different to v�arzea and igap�o

according to our ANOSIM. Second, paleo-v�arzea forest

may be more similar to igap�o or v�arzea forest located

nearby due to seed and propagule dispersion. However, an

effect of geographic location remains unclear since paleo-

v�arzea and v�arzea plots in the Japur�a basin can be found in

different nodes of the cluster analysis. Third, previous stud-

ies have shown that flood height and duration influence

patterns of floristic composition (e.g. Worbes et al. 1992;

Ayres 1993; Wittmann et al. 2002, 2004), and small-scale

topographic variation between plots could thus have

affected plot distribution in our ordination and cluster

analyses despite our focus on late successional forest.

In summary, we show that paleo-v�arzea floodplain tree

assemblages are dissimilar to those of v�arzea and igap�o, but

clearly contain many components typical of both these

floodplain types. We also show that diversity in paleo-

v�arzea is equal to that of more nutrient-rich v�arzea, and

this is perhaps due to the coexisting floral components typ-

ical of v�arzea and igap�o. In addition, we hypothesize that

paleo-v�arzea is in a transitional phase between v�arzea and

igap�o, and that this transition from an active to a paleo

floodplain (which includes a reduction in sediment and

nutrient input by rivers, and successional dynamics) pro-

motes significant changes in floristic composition. We sug-

gest that the current paleo-v�arzea assemblages may

progressively becomemore similar to those of igap�o, where

tree species typical of v�arzea forests will gradually be

substituted by species common to igap�o. We do, however,

recognize that our genus-level analysis is coarse and that a

species-level study is necessary to further examine the

trends observed in the current study. Until species-level

identifications can be significantly improved throughout

the basin, such a studywill remain difficult.

Acknowledgements

This research was supported by the INPA/Max Planck

ProjectManaus, the Brazilian Council of Science and Tech-

nology (Universal 479599/2008-4) and PRONEX CNPq-

FAPEAM, �Areas �Umidas, MAUA. RLA is supported by a

doctoral scholarship from the Norwegian State Educational

Loan Fund. We are grateful to Sr. Jos�e Ramos at the

National Institute for Amazonian Research (INPA) Herbar-

ium for assisting with species identifications. Special

thanks to Nat�alia Castro, Celso Rabelo Costa, Jos�e Lima,

Thiago Ilnicki, Jackson de Castro and all the field assistants

Journal of Vegetation Science8 Doi: 10.1111/jvs.12229© 2014 International Association for Vegetation Science

Tree diversity and composition in paleo-v�arzea forests R.L. Assis et al.

who contributed to the present study. We thank Ethan

Householder, James Gilroy, Mark Bush and two anony-

mous reviewers for constructive comments on an earlier

version of this manuscript.

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Supporting Information

Additional Supporting Information may be found in the

online version of this article:

Appendix S1. Tree inventory locations with their

forest type, latitude/longitude, area inventoried, number

of trees, number of species, alpha diversity and data

source.

11Journal of Vegetation ScienceDoi: 10.1111/jvs.12229© 2014 International Association for Vegetation Science

R.L. Assis et al. Tree diversity and composition in paleo-v�arzea forests