Floristic Variation of the Igapó Forests along the Negro River, Central Amazonia

Thesis submitted in partial fulfillment of the requirements of the degree of Dr. rer. nat of the Faculty of Forest and Environmental Sciences Albert-Ludwigs Universität, Freiburg,Germany

by

Juan Carlos Montero Terrazas

Freiburg im Breisgau 2012

Dean: Prof. Dr. Jürgen Bauhus First supervisor: Prof. Dr. Dr. h.c. Albert Reif Second supervisor: Dr. habil. Florian Wittmann Second reviewer: Prof. Dr. Dieter. R. Pelz

Date of Disputation: 13 November 2012

List of Contents

List of Contents List of Contents ...... 1 List of Figures and Tables...... 3 Statement of Originality...... 5 Statement of Contributions to this PhD Thesis ...... 6 Acknowledgements...... 8 Zusammenfassung...... 10 Abstract...... 13 1 General introduction...... 17 1.1 Amazonian floodplain forests ...... 17 1.2 The course of the Negro River: main environmental gradients ...... 19 1.3...... Patterns of floristic variation in Amazonian forests with emphasis on floodplain evidence ...... 21 1.4 Scope and outline of the thesis ...... 22 2 Floristic variation across 600 km of inundation forests (Igapó) along the Negro River...... 26 2.1 Introduction...... 26 2.2 Methods...... 28 2.2.1 Study area...... 28 2.2.2 Floristic inventories...... 30 2.2.3 Data analysis...... 30 2.3 Results ...... 33 2.3.1 Floristic gradients ...... 33 2.3.2 Floristic composition and importance values...... 36 2.3.3 Tree species richness and diversity ...... 38 2.3.4 Floristic resemblance between river sections...... 41 2.3.5 Diversity gradients of igapó across geographical regions and geological zones ...... 41 2.3.6 Comparison of igapó with várzea ...... 42 2.4 Discussion ...... 43 2.4.1 Spatial floristic patterns ...... 43 2.4.2 Floristic composition ...... 45 2.4.3 Species richness and diversity patterns ...... 46 2.4.4 Diversity gradients at continental scale ...... 48 2.4.5 On the relationship between diversity of igapó and várzea ...... 49 2.5 Conclusion...... 50 3 Effect of flooding regime and soils on tree species composition and diversity of igapó forests across the Negro River, central Amazonia ...... 53 3.1 Introduction...... 53 3.2 Methods...... 56 3.2.1 Study area...... 56 3.2.2 Data collection...... 60 3.2.3 Data Analysis...... 62 3.3 Results ...... 64 3.3.1 Variation of flooding regime and soils along the course of the river ...64 3.3.2 Floristic variation between and within river sections...... 65 3.3.3 Environment in relation to tree community parameters ...... 67 3.3.4 Rarity and commonness in response to the flooding gradient...... 68 3.3.5 Diversity patterns along flooding gradients...... 69 3.3.6 Relation between spatial scale and floristic similarity...... 73 3.3.7 Tree composition according to flood tolerance...... 73 3.4 Discussion ...... 75 3.4.1 Environmental heterogeneity along the course of the Negro River ....75

1 List of Contents

3.4.2 Diversity patterns along flooding gradients...... 76 3.4.3 Rarity and commonness...... 78 3.4.4 Tree composition along flooding gradients...... 79 3.4.5 On the effects of geographic distance and environmental (dis)similarity ……………………………………………………………………………...81 3.5 Conclusion...... 82 4 The igapó of the Negro River in central Amazonia: Linking late- successional inundation forest with fluvial geomorphology ...... 85 4.1 Introduction...... 85 4.1.1 Physical setting of the study area...... 87 4.1.2 Study area and scope...... 89 4.2 Methods...... 89 4.2.1 Floristic inventories...... 89 4.2.2 Hydrology and Geomorphology...... 90 4.2.3 Soil sampling ...... 90 4.2.4 Analysis of floristic data ...... 90 4.3 Results ...... 92 4.3.1 Fluvial geomorphology...... 92 4.3.2 Hydrology ...... 94 4.3.3 Floristic differentiation and species composition ...... 95 4.3.4 Species richness and diversity patterns ...... 97 4.3.5 Forest vertical structure ...... 98 4.4 Discussion ...... 100 4.4.1 Relationship between geomorphology, hydrology and igapó forests 100 4.4.2 The Holocene: floodplain evolution and the spatial distribution of the igapó forest ...... 106 4.5 Conclusion...... 107 5 Synthesis and Perspectives...... 110 5.1 Key Findings...... 110 5.2 Implications for classification and conservation of Amazonian wetlands .114 References...... 116 Appendix I ...... 128 Appendix II ...... 130

2 List of Figures and Tables

List of Figures and Tables

Figures

Figure 1.1: The meeting of the white and black waters of the Solimões and Negro rivers. Physiognomy of a typical igapó forest...... 19 Figure 1.2: Location of the Negro River in the Amazonian hydrological network and its confluence with the Solimões River at Manaus in central Amazonia...... 20 Figure 2.1: Location of inventory sites indicated by squares in each river section indicated with circles ...... 29 Figure 2.2: Diagrams of the first two axes of sites DCA ordination ...... 35 Figure 2.3: Species - area curve...... 39 Figure 2.4: Fisher’s alpha index and number of individuals plotted against river sections...... 40 Figure 2.5: Fisher’s alpha diversity in different region across the Amazon...... 42 Figure 2.6: Fisher´s alpha diversity plotted against geological formations...... 42 Figure 2.7: Comparison of species richness (S) and alpha-diversity (α) between igapó (n: 26) and várzea (n: 22) forests...... 43 Figure 3.1: The Negro River basin and its trajectory from the Colombian side until the city of Manaus showing the study areas...... 58 Figure 3.2: River sections showing study sites projected on satellite images with their respective flood pulse patterns...... 59 Figure 3.3: Patterns of seasonal fluctuation at the lower and upper Negro River...... 60 Figure 3.4: Non-metric multidimensional scaling (NMS) ordination diagram according to Bray-Curtis distance...... 65 Figure 3.5: Distribution of singleton species, common species, fisher’s alpha and abundance along the duration of flooding...... 69 Figure 3.6: The relationship between alpha-diversity and singleton species...... 69 Figure 3.7: Person’s correlations between fisher’s alpha index and species richness and duration and height of inundation...... 70 Figure 3.8: Relation between Fisher’s alpha and flooding duration...... 71 Figure 3.9: Relation between Fisher’s alpha coefficient and flooding duration between 1-ha plots ...... 72 Figure 3.10: Similarity of sampling sites as a function of distance...... 73 Figure 4.1: Course of the Negro River and study areas...... 88 Figure 4.2: Reaches of the Negro River...... 92 Figure 4.3: Isolated hills and rocky islands along reach I...... 93 Figure 4.4: The archipelago of Anavilhanas at Reach V...... 94 Figure 4.5: Cluster diagram for the 8 sites (128 plots)...... 96 Figure 4.6: Two distribution patterns of the vertical structure of the igapó forest along the Negro River...... 99 Figure 4.7: Study sites at the upper section (ST) projected on Landsat images showing the main fluvial units...... 101 Figure 4.8: Study sites at the middle (BA) and lower (AN) sections projected on Landsat images showing the main fluvial units...... 102 Figure 4.9: Schematic cross sections of reach III and reach V...... 104 Figure 5.1: Water levels of the hydrological cycle at the Manaus Harbor...... 113 Figure 5.2: Protected areas along the Negro River...... 115

3 List of Figures and Tables

Tables

Table 1.1: Comparison of main physical and chemical characteristics of white, black and clear water rivers...... 18 Table 2.1: Summary of DCA analyses of tree species data...... 34 Table 2.2: The 10 most important families at each river section...... 36 Table 2.3: The 15 most important species at each river section...... 37 Table 2.4: Species richness, alpha diversity and abundance for the four forest communities averaged to 1 ha...... 40 Table 2.5: Similarity matrix of floristic composition...... 41 Table 3.1: Mean flooding height, duration and respective standard deviation at each river section...... 64 Table 3.2: Mean and range of soil chemistry variables and granulometry...... 65 Table 3.3: Species richness and alpha diversity averaged to 1-ha...... 67 Table 3.4 Summary of Pearson correlations between environmental variables and the community parameters...... 68 Table 3.5: Tree species composition according to flooding tolerance classes...... 74 Table 4.1: Indicator species for the five floristic groups...... 97 Table 4.2: Species richness, alpha diversity, abundance and basal area averaged to 1-ha at the three river sections...... 98

4 Statement of Originality

Statement of Originality

I hereby declare that this thesis has never been submitted to another examination commission in Germany or in another country for a degree in the same or similar form. The material in this thesis, to the best of my knowledge, contains no material previously published or written by another person except where due acknowledgement is made in the proper manner.

Juan Carlos Montero Terrazas,

July 2012

5 Statement of Contributions to this PhD Thesis

Statement of contributions to this doctoral thesis

The topic of this thesis was part of the INPA/Max-Planck Project “Wetland Monitoring Working Group” in Manaus, Brazil. The study was designed by me in collaboration with Dr. Florian Wittmann with inputs from my principal supervisor Prof. Dr. Albert Reif. The primary data were collected by my self, logistically supported by the INPA field team. All the results presented are results of my own analyses. I developed the ideas for the manuscripts and wrote all the three main chapterns, general introduction and synthesis of this thesis.

The thesis comprises 5 chapters, including the general introduction and the synthesis. Four of the chapters (in part or full chapters) were written to be published in scientific journals, in some cases in collaboration with coauthors as detailed below:

Chapter 1 was partially adapted and published in Natur, Forschung und Museum, Senckenberg Journal 141 (9/10) 264-273, 2011. The title of publication is “Der Igapo des Rio Negro”.

The results of this chapter were additionally presented as a poster at the International Conference on the Status and Future of the World's Large Rivers April 11-14, 2011, Vienna, Austria.

Chapter 2 was submitted to the Journal Hydrobiologia and accepted on the 28.03.2012 under the title “Floristic variation across 600 km of inundation forests (Igapó) along the Negro River”. Coauthors are Florian Wittmann and Maria Teresa Fernandez Piedade. The paper has been recently published as Online First.

The main findings were also presented as an oral presentation in the 9TH INTECOL International Wetland Conference carried out in Orlando, USA June 3-8, 2012.

Chapter 3 is in preparation. A summary of this chapter “effects of spatial variation and flooding regime on tree species composition and diversity along the Negro River, Central Amazonia” has been sent to the guest editors of the special issue ““Ecology, management and conservation of native forests” at the journal Forest Ecosystem and Management. Coauthors are Florian Wittmann and Albert Reif.

6 Statement of Contributions to this PhD Thesis

The main results of this chapter have been also presented as an oral presentation at the IUFRO Landscape Ecology Conference in Concepción, Chile, 5-12 November 2012.

Chapter 4 was submitted in July 2012 to the Journal of South American Earth Sciences under the title “The igapó of the Negro River in central Amazonia: Linking late-successional inundation forest with fluvial geomorphology. Coauthor is Edgardo Latrubesse, who is also the Guest Editor of the special issue: “Hydro-geomorphologic processes and Quaternary landforms controlling biotic components in South American wetlands”.

This chapter has been selected as an oral presentation by the scientific committee of the 8th IAG International Conference on Geomorphology, to be held in Paris from August 27 to 31, 2013.

Dr. Florian Wittmann was the main scientific advisor, who accompained me during the entire field work phase and contributed key inputs to the structure of chapters two and three. Dr. Edgardo Latrubesse contributed to chapter four. For this chapter, data from the paper Latrubesse & Franzinelly, 2005: The late Quaternary evolution of the Negro River, Amazon, Brazil: Implications for island and floodplain formation in large anabranching tropical systems, Geomorphology was used additionally to my data.

7 Acknowledgements

Acknowledgements

First of all, I would like to thank my first supervisor, Prof. Dr. Albert Reif. His constant interest and support during the elaboration of the thesis was always very helpful and motivating. I am grateful to Prof. Dr. Dieter Pelz who accepted to be the co-corrector of my thesis.

I owe special thanks to Dr. Florian Wittmann from the Max Planck Institute for Chemistry Biogeochemistry. Florian Wittmann was my scientific supervisor; he invited me to participate in this project as part of the wetland working monitoring group at the Brazilian National Institute for Amazonian Research (INPA) in Manaus. We had many fruitful discussions during my field stays in Manaus and I greatly appreciate his support in many bureaucratic aspects regarding my involvement in the INPA project. I greatly appreciate also the support of the INPA/Max Planck Project at Manaus in Brazil, especially the technicians and field assistants (i.e. José Lima, Francisco Quintiliano, Celso and Valdeney: Thanks to you all! Similarly, special thanks go to Maria Teresa Fernandez Piedade, who is the team leader of the wetlands monitoring group at INPA.

I would also like to express my gratitude to Dr. Edgardo Latrubesse who is an associated professor at the University of Austin Texas, Institute of Geography and Environment. He supported me with essential data and productive suggestions for my chapter four. Dr. Marisol Toledo from the Bolivian Institute of Forest Investigation (IBIF), Santa Cruz, Bolivia, helped me with the data analysis and provided suggestions for the outline of the chapters.

During the first two years of the dissertation project, I got a stipend from UEA (Universidade Estadual do Amazonas) in Manaus for which I am very grateful. The INPA/Max Planck Project financed all field work trips. My thanks go also to the Georg Ludwig Hartig Stiftung, which supported a trip to Vienna to attend a scientific conference in which I had the chance to present some of my results. In a similar manner, I am also very grateful to the International Graduate Academy (IGA), University of Freiburg, who supported my attendance to the 9th INTECOL conference in Orlando to present some of the findings of my research.

Special thanks for a wonderful time in Manaus go to my house mates and friends Sinomar, Daniel, Carlos Leandro, Rafael, Farrah and Cidinha: Muito obrigado

8 Acknowledgements zezinhos! My stays in Freiburg were possible to the priceless hospitability of several friends such as Karl-Heinz, Dani, Emiliano, Cristabel, Silvio, Victor Hugo Victor (el mexicano) and Katja. Thanks a lot guys! I am also very thankful to my mother in law, Maja Schürkes, who supported me and my family during the whole research time (especially during my field stays in Brazil) by taking care of my kids. Finally, I am very grateful to my wife Inka Montero who helped with statistical analysis and patiently revised this document.

9 Zusammenfassung

Zusammenfassung

Amazonische Feuchtgebiete bedecken ein Gebiet von ca 2 Millionen km2, und machen damit ungefähr 30% des Amazonasbeckens aus. In Zentralamazonien werden die vorherrschenden Überschwemmungswälder in nährstoffreiche Weißwassergebiete, die „Várzea“ und nährstoffarme Schwarz- oder Klarwassergebiete, die „Igapó“ unterteilt. Igapó Wälder finden sich an Flüssen, die das Guayana-Schild oder das Zentral-Brasilianische Schild paläozoischen und/oder präkambrischen Ursprungs durchfließen.

Der bedeutendste Schwarzwasserwald hat sich entlang des Rio Negro gebildet. Trotz der großen Ausdehnung, ökologischen Bedeutung und wahrscheinlich aufgrund der vergleichsweise geringen ökonomischen Nutzbarkeit herrscht ein Mangel an wissenschaftlichen Daten zu Igapo Wäldern. Floristisches Wissen ist extrem begrenzt im Vergleich mit den Überschwemmungswäldern der Weißwasserflüsse, der Varzea. So bestehen vor allem deutliche Lücken floristischer Forschung in den abgelegeneren Gebieten am mittleren und oberen Verlauf des Rio Negro. Sein Wasser transportiert sehr geringe Mengen an gelöstem Material (Schwebstoffen), enthält jedoch hohe Konzentrationen von Huminstoffen, die dem Fluss die charakteristisch dunkelbraune Farbe verleihen. Die alluvialen Podsolböden sind extrem arm an Nährstoffen, sehr sauer und bilden große unfruchtbare Überschwemmungsgebiete mit wenig autochthoner Primärproduktion.

Der Verlauf des Rio Negro weist hauptsächlich zwei physikalische Gradienten auf: Zum einen schwankt der Wasserstand entlang des Flussverlaufs, hauptsächlich beeinflusst durch einen vorhersagbaren, langen und monomodalen Überschwemmungsrhythmus. Die Überschwemmungsamplituden weisen einen steilen Gradienten von 3,6 m im oberen Flussverlauf (z.B. bei Santa Isabel) bis 9,3 m im unteren Flussverlauf (z.B. bei Anavilhanas) auf, wodurch die Bäume der anstehenden Wälder Überschwemmungen zwischen 50 und 230 Tagen pro Jahr ausgesetzt sind. Die Sedimente entlang des Flusses bilden den zweiten physikalischen Gradienten. Der obere Flussbereich, durch die westliche Ausdehnung des Guayana-Schildes beeinflusst, besteht vor allem aus grobkörnigem unfruchtbarem Material. Der untere Teil weist feinere Sedimente intermediärer Fruchtbarkeit auf. Der unterschiedliche Nährstoffgehalt in diesem Flussabschnitt wird verursacht durch den Branco Fluss, der feinere Sedimente in den Hauptkanal einträgt sowie dem Rückflusseffekt des Solimoes Flusses.

10 Zusammenfassung

Das komplexe Überschwemmungssystem am Rio Negro steht im Zusammenhang mit morphodynamischen Prozessen und der Evolution des Überschwemmungsgebietes vorwiegend während des Holozäns. Seine Dynamik zeigt sich in eindrucksvollen Archipelen wie das Mariuá (im mittleren Flussabschnitt) und dem Anavilhanas (im unteren Abschnitt), den größten, komplexesten Flussarchipelen der Welt. Daher ist es notwendig, den physikalischen Gradienten und die vielschichtigen Zusammenhänge zwischen fluvialer Geomorphologie und der Vegetation entlang des Flussverlaufs im Zusammenhang zu sehen.

Das Hauptziel der vorliegenden Arbeit ist, die floristische Variation der spätsukzessionalen Igapo Wälder entlang des Flussverlaufs zu erfassen. So wurde untersucht, wie die Zusammensetzung der Baumarten, die Diversität und die Waldstruktur auf die Variablen Überschwemmung, Bodenbeschaffenheit und Hydrogeomorphologie entlang des Flussverlaufs reagieren.

Die Untersuchungen konzentrieren sich auf den oberen, mittleren und unteren Rio Negro sowie einen nördlichen Zufluß, den Jufaris Fluss entlang eines 600 km langen Transsektes des Rio Negro im brasilianischen Amazonien. Floristische Daten wurden auf insgesamt 10 Hektar, unterteilt in 160 Untersuchungsflächen von je 625 m2 durch die Erfassung von 6126 Bäumen mit einem dbh > 10 cm aufgenommen.

Die Überschwemmungshöhen wurden mit Hilfe der Wassermarken des Vorjahres an allen untersuchten Bäumen erfasst. Diese Messungen wurden mit dem täglichen Wasserstand des nächstgelegenen Hafens korreliert und so die mittlere Höhe und Dauer der Überschwemmung berechnet. Bodenproben wurden an allen Untersuchungsgebieten genommen, und deren chemische Zusammensetzung und Körnung bestimmt. Die Analyse der Flussgeomorphologie basierte auf Sedimentprofilen und Radiokarbon-Datierungen. Zusätzlich erfolgte eine detaillierte Interpretation der lokalen geomorphologischen Eigenschaften der Untersuchungsgebiete.

Die Ergebnisse zeigen, dass trotz geringer Unterschiede in der mittleren Alpha- Diversität zwischen den Flussabschnitten die Beta-Diversität (Species Turnover) durchwegs hoch ist. Nur wenig Baumarten kommen in mehr als einem Flussabschnitt vor; und die floristische Zusammensetzung wechselt mit den Abschnitten. Dieser abrupte Wechsel in der Artzusammensetzung ist vor allem beeinflusst durch die Artengemeinschaft des Jufaris Zuflusses, durch den die floristischen Diskontinuitäten entstehen. Die Untersuchung in Relation zur Überschwemmungstoleranz zeigte,

11 Zusammenfassung dass keine Art entlang des gesamten Gradienten vorkommt. Dieses Muster könnte dadurch erklärt werden, dass die meisten Arten der Überschwemmungsgebiete bestimmte Präferenzen für topographische Niveaus und Flutamplituden aufweisen. Es erklärt auch, dass nur wenig Generalisten entlang des Flussverlaufs registriert wurden.

Ein geringer Anstieg an Alpha-Diversität findet sich im unteren Abschnitt des Rio Negro, wo die Überschwemmungsdauer und der Anteil feinerer Sedimente zunimmt. Diese Zunahme an Alpha-Diversität kann als Resultat einer höheren Habitatdiversität in diesem Flussabschnitt interpretiert werden. Dies wird auch durch die Hydro- Geomorphologische Analyse bestätigt, die zeigt, dass die Variabilität von Habitaten auf kurzen Distanzen eine große Baumdiversität auf kleinen Inseln konzentriert.

Die unterschiedlichen geomorphologischen Formationen scheinen die strukturellen Muster der Igapowälder zu beeinflussen. Gemischte umweltbedingte und räumliche Effekte erklärten den größten Teil der Variation im Artenvorkommen, wobei die geographischen Effekte alleine einen größeren Einfluss auf Artzusammensetzung zeigen als die umweltbedingten Effekte.

Obwohl klare floristische Gradienten entlang des Flussverlaufs erfasst wurden, macht die geographische Variation und das komplexe physikalische Gefüge des Überschwemmungsgebietes des Rio Negro es schwierig, einzelne Faktoren als Determinanten floristischer Variation zu identifizieren. Die Ergebnisse der Arbeit legen vielmehr nahe, dass eine Kombination verschiedener Faktoren auf unterschiedlichen räumlichen, zeitlichen und maßstäblichen Ebenen die floristische Variation entlang des Rio Negro determinieren. Die beobachtete starke räumliche Variation des Igapo Waldes entlang des Rio Negro empfiehlt eine gleichmäßigere Verteilung von Schutzgebieten in den verschiedenen Flussabschnitten.

12 Abstract

Abstract

The wetlands of the Amazon cover an area of about 2 million km2, corresponding to approximately 30% of the total basin area. In central Amazonia the main floodplain forests are differentiated into nutrient-rich white water “várzea” and nutrient-poor black water or clear water “igapó”. Igapó forests occur along rivers that drain the Paleozoic and/or Precambric Shields of Guyana and Central Brazil such as the Negro River, which forms the largest black-water inundation forests in the world. However, despite its significant extension, ecological importance and probably due to the comparatively low economic importance, there is a lack of scientific data on the igapó forests. In particular, significant gaps in floristic research exist in the remote middle and upper sections of the river and floristic knowledge is extremely limited in comparison with its white-water counterpart várzea.

The waters of the Negro River carry very low quantities of suspended matter, but contain a high concentration of humic acids that give the river its distinctive dark brownish color. The alluvial soils are extremely poor in nutrients and very acidic, resulting in large infertile floodplains of poor autochthonous primary productivity.

The course of the Negro River exhibits two main physical gradients. The first refers to the oscillation of water level along the course of the river, which is mostly governed by a predictable, long and monomodal flood pulse. Thus, flood mean amplitudes exhibit a sharp gradient ranging from 3.6 m at the upper reach (i.e. Santa Isabel) to 9.3 m at lower reach (i.e. Anavilhanas) of the river, subjecting trees to an inundation period of about 50 and 230 days year, respectively.

The second gradient is related to the sediments along the course of the river. The upper reach consists basically of coarser unfertile material influenced by the western extension of the Guiana Shield. The lower reach has finer sediments of intermediate fertility. Here, the influence of the Branco River transporting finer sediments into the main channel and the backward effect of the Solimões River exert important control and lead to changes in the nutrient status at this section of the river.

The construction of the complex floodplain system of the Negro River is related to morphodynamics processes and the evolution of the floodplain mostly during the Holocene. This dynamic resulted in impressive fluvial archipelagos such as Mariuá (middle section) and Anavilhanas (lower section), the largest and complex fluvial

13 Abstract archipelagos of the world. Thus, in addition to considering the physical gradients, the establishment of distinct relationships between the fluvial geomorphology and vegetation distribution along the course of the river becomes necessary.

The overall objective of this study is to assess the floristic variation of late- successional igapó forests along the course of the Negro River. More specifically, it was investigated how tree species composition, diversity and forest structure respond to the variable flooding regime, soil characteristics and hydro- geomorphologic styles along the course of the river. My study focuses on four areas (i.e. upper, middle, lower Negro and the northern tributary Jufaris River) along a 600 km stretch of the Negro River in the Brazilian Amazon. Floristic data was obtained by recording 6126 individual trees of >10 cm of diameter at breast height in 160 plots of 625 m2 each, totalizing 10 hectares of inventories. Flooding data was obtained by measuring inundation height at each tree by using previous year’s water marks on the tree trunks. These measurements were correlated with the daily water-level records at the closest harbor to calculate mean height and length of inundation. Soil samples were collected at each research site and the chemistry and granulometry were analyzed. The analysis of fluvial geomorphology was based on sedimentary profiles and chronologies (radiocarbon). In addition, a detailed interpretation of local geomorphological features was obtained in the study areas.

The results suggest that although mean alpha-diversity may not consistently differ between river sections; species turnover (beta-diversity) is consistently high and significant. Only few tree species occurred in more than one river section, and floristic composition changed abruptly from one section to the other. This change in species composition was particularly influenced by the species pool of the tributary Jufaris River, which displays abrupt floristic discontinuities. The floristic composition in relation to flooding tolerance classes revealed that no single species occurred along the entire flood gradient. This pattern may be explained by the fact that most of the floodplain species have certain preferences for specific topographic levels and flood amplitudes. This may also explain why I found very few generalist species distributed along the course of the river. I detected a slight trend to an increase of alpha-diversity at the lower section of the Negro River (i.e. Anavilhanas), where the duration of flooding and the percentage of finer sediments (silt and clay) significantly increased. I interpreted this increase of alpha-diversity as a response to a major diversity of sampled habitats in this river section. This was confirmed by the hydro- geomorphologic analysis, in which I concluded that variability of well-developed

14 Abstract environments in short distances demonstrates that this high tree diversity concentrates in narrow islands. The different geomorphologic styles appear to control structural patterns of igapó forests. Mixed environmental and spatial effects explained most of the variation of species distribution, but the spatial effect alone had a greater influence on species composition than environmental effects alone.

Although I detected clear floristic gradients along the course of the river, the geographic variation and the complex physical setting of the floodplain of the Negro River make it difficult to identify pure driving forces as determinants of floristic variation. Rather, the results of my investigation suggest that a combination of factors acting at different space, scale and time determine the overall floristic variation along the Negro River.

15 General Introduction

1

GENERAL INTRODUCTION

16 General Introduction

1 General introduction

The Negro River and its large floodplains since a long time have fascinated naturalists and today it is an intriguing place for ecologists and biologists. Early observations by naturalists such as Alexandre Rodriguez Ferreira (1756-1815), Alfred Russell Wallace (1823-1913) and Richard Spruce (1817-1893) already highlighted the complexity of the landscape and the particularity of the flora. Almost two centuries later, despite important progress on Amazonian floodplain research, the flooded forest of the Negro River region has been little investigated. In particular, the remote middle and upper sections lack of ecological research, and floristic patterns are practically unknown. In this thesis, I outline the floristic view of the flooded forest along the Negro River. The thesis, thereby aims at understanding the floristic variation in relation to environmental gradients along the course of the world’s largest black-water river. The floristic data presented are the first on black-water inundation forest based on an extensive quantitative dataset. The results provide essential information for the classification and management of Amazonian floodplains and contribute insights to current discussions on patterns of tree diversity and composition of Amazonian forests.

1.1 Amazonian floodplain forests

Wetlands cover about 2 millions of km2 of the Amazon basin, from which approximately 15 % is covered by seasonally flooded forests (Junk et al., 2011). The most representative types of flooded forests are those periodically by white-water Rivers (várzea) and by clear-water and black-water Rivers (igapó) (Prance, 1979; Pires & Prance, 1985). These rivers are differentiated according to their physicochemical properties and water quality (Sioli, 1956; Table 1.1). Thus, várzea forests occur along the channels that drain the Andes and the Andean foothills, such as the Ucayali-Solimões-Amazon, Purus, Madeira and Madre de Dios Rivers. These rivers are loaded with nutrient-rich sediments and form large fertile floodplains covering approximately 300.000 km2 of the Amazon basin (Junk, 1989).

Black-water Rivers, on the other hand, carry very low quantities of suspended matter, but contain high concentration of humic acids that give the rivers their distinctive dark brownish color (Figure 1.1) and make the waters highly acidic (Junk et al., 2011). The floodplains have an extension of about 100.000 km2 which are extremely poor in nutrients and low autochthonous primary productivity (Furch, 1997). Igapó forests

17 General Introduction occur along rivers that drain the Paleozoic and/or Precambric Shields of Guyana and Central Brazil such as the Negro River, which forms the largest black-water inundation forests in the world (Montero, 2011).

Table 1.1: Comparison of main physical and chemical characteristics of white, black and clear water rivers modified from Sioli (1956) and Junk et al. (2011).

Descriptive attributes Whitewater Blackwater Clearwater Origin Andes range and pre- Precambrian Shields Precambrian Andean valleys and Tertiary Shields of Guiana Amazonian lowlands and Central Brazil Colour Ochre, turbid, muddy Brown olive, “tea like” Green olive “coffee with milk” pH near neutral 6.2-7.2 acidic, 3.8-4.9 variable, 4.5-7.8 Electric 40-100 <20 5-40 Conductivity (μS cm-1) Transparency (Secchi 20-60 cm 60-120 cm >150 cm depth) Humic content (mg/l) low (14.1) high (26.6) low (2.3) Inorganic nutrients rich poor variable

Fertility of substrate and high low low to intermediate water Relationship of Ca, Mg>Na, K Na, K>Ca, Mg variable Alkali earth (Ca, Mg) and alkali (Na, K) cations

-- -- - Dominating anions CO3 SO4 , Cl variable Inundation forest cover Várzea Igapó Igapó

Example of rivers Solimões-Amazon Negro, Jutaí (Brasil) Xingú, Trombetas, (Brasil), Ucayali Nanay (Perú) Manuripi Tapajós, Araguaiá (Perú), Caquetá (Bolivia), Caura (Brasil), Itenez or (Colombia), Madre de (Venezuela) etc Guaporé (Bolivia) Dios (Bol) etc

The majority of studies on Amazonian floodplain forests have concentrated on várzea forests. The floodplains of the Negro River have very low use options; hence economic importance is limited for locals, which probably have generated little attention by research and development agencies. But, its ecological importance represented by endemism, species diversity, food webs, and ecological services among others, is particularly evident. There are few quantitative floristic inventories presented by the scientific literature, all of them performed in the lower section of the Negro River. Thus, there are detailed inventories conducted by Rodrigues (1961); Takeuchi (1962), Keel & Prance (1979) and Revilla (1981). About 20 km northeast of Manaus at the Tarumã-Mirim River, a black-water tributary there are data available from Worbes, (1986); Ferreira, (1991) and Ferreira & Almeida (2005). Approximately

18 General Introduction

100 km upstream at the archipelago of Anavilhanas there are quantitative data by Piedade, (1985); Parolin et al., (2003) and Piedade et al., (2005). In the Jaú National Park (about 200 km NW from Manaus) there are data from Ferreira (1997, 2000). Overall no more than 10 hectares of floristic inventories are available for igapó along the Negro River.

Figure 1.1: The meeting of the white and black waters of the Solimões and Negro rivers, respectively (left, photo: Jochen Schöngart). Physiognomy of a typical igapó forest (right).

1.2 The course of the Negro River: main environmental gradients

The Negro River is the largest black-water river in the world. With a mean annual discharge of 28.000 m3/s the Negro River occupies the sixth place in the world in terms of total discharge, for that reason it is considered part of the selected group of mega-rivers (Latrubesse, 2008). The floodplains of the Negro River and its tributaries cover an area of about 118.000 km2 (Melack & Hess, 2010) and the basin covers more than 600.000 km2 (Latrubesse & Franzinelli, 2005). It flows approximately 2500 km from its headwater at the Colombian side into the Rio Solimões to form the Amazon River south of the city of Manaus (Goulding et al. 2003) (Figure 1.2). Within Brazilian territory the river has a length of ca. 1300 km.

19 General Introduction

Figure 1.2: Location of the Negro River in the Amazonian hydrological network (left) and its confluence with the Solimões River at Manaus in central Amazonia (right).

Due to precipitation seasonality and low inclination of most parts of its catchment and river course, most of the course of the Negro River is governed by a predictable, monomodal flood-pulse (Junk et al., 2011). Thus, flood amplitudes range from 3.6 m at the upper reach to 9.3 m near its lower reach, and subject the floodplain vegetation to periodic inundations lasting from 50 to 230 days per year (Agência Nacional de Águas - ANA). In contrast to the lower and middle sections of the Rio Negro, which show a typical monomodal flood pulse, the upper course experiences bimodal rises mostly governed by ephemeral or flash floods. The existence of unpredictable flood pulses in the upper section is probably enhancing spatial diversity at a landscape scale, due to the local variation of intensity and frequency of flood disturbances. At a local scale, the monomodal and long flood pulse (i.e. lower section) associated with topography and specific soil characteristics may regulate the spatial variation of tree communities which may exhibit predictable ecological traits. However, species diversity could decrease as stress by long flooding period rises.

The second environmental gradient is related to the granulometry and chemistry of sediments along the course of the river. The upper reach consists basically of coarser unfertile material influenced by the western extension of the Guiana Shield. The lower reach has finer sediments of intermediate fertility. Here, the influence of the Branco River transporting finer sediments into the main channel and the backward effect of the Solimões River reconfigure soil gradients at this section of the river resulting in changes in the nutrient status (Junk et al., 2011). The variable flooding regime and differences in alluvial sediments along the course of the river may be fundamental factors influencing the spatial distribution of tree communities (Junk et al., 1989; Rosales et al., 1999; Wittmann et al., 2010; Junk et al., 2011).

20 General Introduction

1.3 Patterns of floristic variation in Amazonian forests with emphasis on floodplain evidence

Identify patterns of floristic variation and understand their causes are perhaps the major challenges that researchers must overcome when studying the distribution of tree communities in the Amazon. Based on empirical evidence across the Amazon, the variation in floristic composition and diversity has long been debated by the relative importance of stochastic (i.e. dispersal assembly) and deterministic (i.e. niche assembly) mechanisms (Hubell, 2001).

Under niche assembly, species composition and relative abundances are closely determined by site environmental characteristics. Thus, the intensity of the environmental filter (e.g. flooding, soil, etc) determines the co-existence of species in a single site. At local scales (< 1 km2) several studies on várzea and igapó have reported that compositional and diversity patterns are predictable in function of severity of flooding. Research has also found pronounced species zonation and continuous increase in species richness and diversity with decreasing inundation height and length (Ferreira, 1997; Worbes, 1997; Wittmann et al. 2006). Similarly, studies have noted that water chemistry is crucial to determine the floristic variations on floodplain forests, especially on confluence areas (Rodrigues, 2007; Rosales et al., 1999). At landscape scale (i.e. along river corridors) the environmental filtering may be strongly influenced by the inputs of sediments and water chemistry of tributary rivers resulting in a discontinuous system. A recent study along a 2500 km long corridor of the Solimões-Amazon River revealed that the effect of flooding on species distribution is less predictable whereas spatial components (e.g. longitude or location of plots) may better explain the floristic variation (Albernaz et al., 2011).

The dispersal assembly view, on the other hand, ignores species’ physiological and ecological peculiarities and assumes that tree communities are assembled by random dispersal. Compositional patterns of local communities, therefore, will be more dependent of surrounding metacommunities and the immigration rate of its constituent species (Hubell, 2001). In the extreme case, where tree community is entirely controlled by dispersal assembly, floristic similarity between sites will decrease with increasing geographical distance and will be independent of any environmental preference and difference. In floodplain forest the extent to which the dispersal assembly mechanism predict floristic variation has been poorly investigated. A study of várzea forest along the Manu River, western Amazonia

21 General Introduction

(Terborgh et al., 1996) showed that a few species were both abundant and widespread (i.e. “oligarchic species” sensu Pitman et al., 1999). A similar pattern has been observed by Wittmann et al. (2010) in várzea in central Amazonia. These authors suggested that species oligarchies are very evident in floodplains due to the high connectivity of riparian corridors.

Recent studies on species distributions based on large datasets and covering large geographic areas across the Amazon (ter Steege et al., 2003; ter Stegge et al., 2006) suggest taking a broad perspective to identify main mechanism shaping tree diversity and composition. Thus, it has been suggested that at a landscape scale (102 - 104 km2) evolutionary and historical processes (e.g. climate and tectonic changes) may determine which species make up the regional species pool (Ricklefs, 1987; ter Steege & Zagt, 2002). In this sense, Latrubesse & Franzinelli (2005) gives special emphasis on the evolutionary history of the geomorphology of river channels, which for the Negro River was particularly intense during the Late Glacial-Holocene. Thus, tree community assemblages and dynamics of the igapó forests may be in function of specific hydro-geomorphology types representing most probably a patchy distribution of habitats along the river channel, which may be expressed at the scale of meters to kilometers.

In general, the complexity of the physical gradients of the Negro River makes difficult to solely rely on pure or isolated driving forces as determinants of floristic variation (e.g. pure deterministic vs pure stochastic). Rather, the physical gradients of the study area suggest that a combination of factors acting at different space, scale and time are determining the overall floristic variation along the Negro River. Therefore, in this work I attempt to find and to collect qualitative and quantitative evidences to better understand this variation.

1.4 Scope and outline of the thesis

I focused on the late-successional igapó forest along a 600 km stretch of the Negro River in the Brazilian Amazon. The study area links the town of Santa Isabel do Rio Negro (upper section) with the archipelago of Anavilhanas at the lower section. Thus, by recording 6126 individual trees of >10 cm of diameter at breast height in 160 plots of 625m2 each, I first assessed the floristic variation of the igapó and later I identified main floristic and structural patterns in response to the flooding regime, soil features and hydro-geomorphology styles along the course of the Negro River.

22 General Introduction

In general, this study will contribute floristic data to a region in which there is a lack of quantitative scientific information and knowledge about the flooded vegetation is limited, especially in the upper and middle sections of the river. This basic information will contribute to the classification of wetlands in the Amazon region, which is an ongoing initiative led by the research consortium Max Planck Institute /INPA at Manaus, Brazil. More specificifically, this study will provide scientific insights about the evolutionary patterns and diversification of the Amazonian landscape, especially the floodplain forests. My study can also give important answers to understand the floristic evolution of the Amazonian forests especially during younger geologic eras (e.g. Holocene). Finally, in response to predicted impacts of climate change on Amazonian wetlands my results will contribute to the understanding of species distribution, adaptation and colonization strategies.

The Chapter 2 outlines the variation of species richness, diversity and floristic composition along the Negro River, including sites on the Jufaris River, which is a northern black-water tributary. The latter with the objective to analyzes the floristic contribution of regional species pools (tributary) to the whole community species pool. In addition, supported by available literature I assess at continental-wide scale alpha diversity patterns across geographical locations and geological formations and finally I compare the results to those of várzea forest from both the Amazon and Orinoco basins. I analyze an extensive data set of 160 plots (summarizing 10 hectares) spread over the upper, middle and lower sections of the Negro River as well as along the tributary Jufaris River.

In Chapter 3 I address main diversity and compositional patterns in relation to flooding gradients and soil characteristics along the main channel of the Negro River. I basically analyze the effect of duration and height of flooding and soil chemistry and granulometry on the tree alpha diversity and species composition at different scales. Thus, I examine the effect along the river channel and also at more restricted scales namely between and within river sections. Finally, I check the relative influence of environmental and geographic distances in determining main floristic patterns. For the purpose of this chapter I analyze the three sampled river sections (i.e. upper, middle and upper) summarizing 128 plots (8 hectares).

Based on an evolutionary perspective of the Negro River channel the Chapter 4 describes and interprets relations between igapó forest, fluvial geomorphology and the spatial evolution of the igapó forest through the Holocene. In particular I

23 General Introduction investigate the effect of geomorphological units and channel patterns on diversity and structural parameters. I conclude discussing patterns of spatial distribution of the igapó forest by introducing a time scale evolutionary approach during part of the Holocene. As in Chapter 2 I analyze the three sampled river sections (i.e. upper, middle and upper) summarizing 128 plots (8 hectares).

The Chapter 5 synthesizes main findings of the thesis and outlines main factors that may better explain the floristic and structural variation of the igapó along the Negro River. I conclude discussing main implications for biodiversity, conservation and sustainable management of the floodplain forests of the Negro River.

24 Floristic gradient

2

FLORISTIC VARIATION ACROSS 600 KM OF INUNDATION FOREST (IGAPO) ALONG THE NEGRO RIVER

25 Floristic gradient

2 Floristic variation across 600 km of inundation forests (Igapó) along the Negro River

2.1 Introduction

The Negro River flows 2500 km from its headwaters in Colombia before discharging into the Solimões River near the city of Manaus (Goulding et al., 2003). It incorporates the two largest fluvial archipelagos in the world, Mariuá and Anavilhanas, located in the middle and lower reaches of the river, respectively. Inundation forests (igapó) occur throughout the main river channel and most of its tributaries. These are considered the largest nutrient-poor black-water forests of the Amazon basin (Montero, 2011).

The waters of the Negro River carry low levels of suspended matter, but contain a high concentration of humic acids that characterize the distinctive dark brownish color (Sioli, 1956). The water pH values range from 3.8 to 5, depending on the site and time of the year (Furch, 1997; Junk et al., 2011). The floodplains of the black- water Rivers are characterized by nutrient-poor soils and low primary productivity (Furch, 1997). Due to seasonal variation in rainfall and generally flat topography of the majority of the catchment area, the Negro River is governed by a predictable, monomodal flood-pulse (Junk et al., 2011). Flood amplitudes range from 3.6 m at the upper reaches to 9.3 m near its lower reaches of the river (Agência Nacional de Águas - ANA) and subject the floodplain vegetation to seasonal flooding, lasting from 50 to 230 days per year (Junk, 1989). The variable flooding regime and differences in water and sediment chemistry determine the tree species composition and diversity patterns along the river channel and are considered important factors influencing the spatial distribution of tree communities (Junk et al., 1989; Rosales et al., 1999; Wittmann et al., 2010; Junk et al., 2011).

To document and understand floristic patterns of forests across landscape scales, inventories usually consist of either long transects (Duque et al., 2003; Tuomisto et al., 2003) or on series of scattered plots (ter Steege et al., 2006; Pitman et al., 2008; Toledo et al., 2011) and record either just location (i.e., longitude, latitude) or environmental variables (i.e., precipitation, nutrients). This approach allows researchers to determine if changes in floristic components (i.e., species composition and richness) or in evolutionary traits (e.g., seed dispersal mechanisms, growth rates

26 Floristic gradient etc.) are related to environmental gradients and niche characteristics at each site. Using this approach, several studies along riverine systems along temperate forests (e.g. Sabo et al., 2005) and Amazonian floodplain forest have described high spatial heterogeneity across riverbanks (Rosales et al., 1999; Wittmann et al., 2006; Albernaz et al., 2011).

Assemblages of biological communities along streams and rivers have been explained by various riverine concepts and their ecological implications. The River Continuum Concept (Vannnote et al., 1980) postulated linear, gradual and predictable changes of physical gradients from headwater regions to the lower reaches. Later, the recognized importance of interruptions in the main channel caused through the confluence of tributaries (Rice et al., 2001) resulted in a new perspective where rivers were interpreted as discontinuous system. This concept emphasizes a patchy distribution of habitats, expressed at the scale of meters to kilometers (summarized in Benda et al., 2004). A comprehensive approach focusing on river-floodplain dynamics was proposed by Junk et al. (1989). These authors argued that the major driving force affecting the biota and biogeochemical processes within a floodplain is the pulsing of rivers, which result in defined wet and dry periods. Thus, the flood pulse determines species composition and diversity patterns along floodplains and is a decisive factor influencing the spatial distribution of tree communities (Rosales et al., 1999; Wittmann et al., 2010).

Most studies in seasonally flooded Amazonian forests have been carried out along white-water rivers (várzea forests sensu Prance, 1979) and have focused on changes in species composition and diversity patterns along vertical gradients (Worbes, 1997; Ferreira, 2000; Rosales et al., 2001; Wittmann et al., 2002; Piedade et al., 2005) rather than spatial gradients along river corridors. Wittmann et al. (2006) provided an extensive dataset showing gradients of species diversity across multiple sites in Amazonian várzea forests. The few studies emphasizing spatial gradients of floristic variation across river corridors found abrupt changes in species composition (Rodrigues, 1997; Rosales et al., 2001; Albernaz et al., 2011).

Despite the considerable extension of the Negro River, only few quantitative floristic inventories have been carried out in igapó forests (Keel & Prance, 1979; Revilla, 1981; Worbes, 1986; Parolin et al., 2003; Parolin et al., 2004; Ferreira & Almeida, 2005; Piedade et al., 2005 and Scudeller & de Souza, 2009). Most of these studies concentrated on the lower Negro River, and inventoried small plots (< 0.5 ha).

27 Floristic gradient

Exceptions are the forest inventories at the National Park Jaú located about 200 km NW of Manaus conducted by Ferreira (1997, 2000) and Ferreira & Stohlgren (1999), who analyzed the effect of flooding on igapó forest of different habitats using three 1- ha plots. Overall, less than 10 ha of floristic inventories are available for igapó forests along the Negro River. Hence, there are still important gaps in the floristic data coverage, especially with regard to its middle and remote upper sections of the Negro River.

In what follows, we present a quantitative floristic inventory of 10 ha in late- successional igapó forest distributed across a 600 km long-corridor of the Negro River in Brazil. The aim of this study is to describe the tree species composition, species richness and diversity and to check how these parameters vary along the river course. In addition, supported by available literature we assess a continental- wide scale alpha diversity patterns and finally we compare our results to those of várzea forest from both the Amazon and Orinoco basins. Specifically, we address the following questions: (a) How do species composition, tree richness and diversity vary within and between study areas (b) Are there alpha-diversity gradients of igapó forests across geographical locations and geological formations? (c) How are species richness and alpha diversity of igapó in relation to várzea?

2.2 Methods

2.2.1 Study area

We focused our study on four areas (i.e river sections) along a 600 km stretch of the Negro River in the Brazilian Amazon, running from the city of Santa Isabel to the Anavilhanas: (1) Santa Isabel (ST, upper section, 00º27'S, 64º46'W), (2) Barcelos (BA, middle section 00°38'S, 63°15'W), (3) the northern tributary lower Jufaris River (JU, middle section, 00°46´S, 62°29´W), and (4) Anavilhanas (AN, lower section, 02°46'S, 60°45'W, lower section) (Figure 2.1).

Annual rainfall in the Brazilian part of the Negro River basin averages 2000-2.200 mm, with a maximum rainfall of over 3.000 mm in the upper section. Mean monthly temperatures vary little over the year and range between 25 and 28°C (Sombroek, 2001). Due to the general high rainfall along the upper Negro River and in its large catchment with an area of approximately 700.000 km2 (Latrubesse, 2008), the water levels of the Negro River undergo seasonal variations, with flood amplitudes ranging from 3.6 m (upper Negro) to 9.2 m (lower Negro). While the flood pulse (Junk et al.,

28 Floristic gradient

1989) in the lower section is strongly monomodal, with highest water levels occurring during May-August, it is slightly bimodal in the upper section, where a second, smaller high-water period frequently occurs during February – April.

Figure 2.1: Location of inventory sites indicated by squares in each river section indicated with circles (ST, upper section; BA and JU, middle section and AN, lower section). Inset shows the location of the Negro River in the Amazon hydrographic system. The satellite image is derived from the SRTM elevation model, Global Land Cover Facility (USGS, 2004)

The substrates in ST, BA and also along the lower tributary JU consist mostly of nutrient-poor sand which originates from the western extension of the Guyana Shield, and the alluvial landscape is characterized by rocky islands and the presence of granite inselbergs close to the river channel (Goulding et al., 1988; Latrubesse & Franzinelli, 2005). The alluvial substrate in the lower section is influenced by the Branco River with its source located in the northern Roraima massif, transporting silt and clayish sediments to the Negro. Below the confluence of the Branco and Negro Rivers, the Anavilhanas archipelago has been formed from substrates characterized by intermediate fertility (Junk et al., 2011). This complex and dynamic network of islands acts as a fine sediment trap and is interpreted as the result of relatively recent, Holocene deposition (Irion et al., 1999).

According to the estimation of the IBGE (2008) there are approximately 75,000 inhabitants in the region, distributed between the three major towns (upper: Santa

29 Floristic gradient

Isabel do Rio Negro; middle: Barcelos; lower: Novo Airão). The local dwellers are mainly caboclos settled along riversides and indigenous groups mainly settled on the upper Negro. The local economy is mainly restricted to the extraction of forest and aquatic resources (Emperarie, 2000; German, 2004), with low agricultural and timber extraction. Non-forest economic activities are also performed in the region, which includes gold mining, gravel extraction and sandstone outcropping for construction (Goulding et al., 1996). Furthermore, commercial fishery, sport fishing and ecotourism are important activities in the region, especially in the lower Rio Negro.

2.2.2 Floristic inventories

Field work was carried out between September 2008 and March 2010 during the low- water periods. In the four study areas, we established 160 quadratic 25 x 25 m (625 m2) plots in late-successional igapó forest totaling an area of 10 ha: (1) Santa Isabel (ST, 48 plots), (2) Barcelos (BA, 36 plots), (3) Jufaris (JU, 28 plots) and Anavilhanas (AN, 48 plots). Due to varying accessibility, the number of plots at each study area differed.

In areas ST, BA and AN we distributed the plots between three sites (i.e., ST1, ST2, ST3), while in the JU area plots were distributed between two sites (Figure 1.1). There were a maximum of 16 plots established per site, corresponding to an area of 1 ha. The upper and lower areas are separated by approximately 600 km, whereas within areas, the sites are separated by a distance of between 5 and 50 km.

All trees ≥ 10 cm diameter at breast height (dbh) were labeled, numbered and dbh measured. Species were identified in the field, and when this was not possible, identified provisionally as morpho-species with voucher specimens collected for later identification at the herbarium of the National Institute for Amazon Research – INPA, Manaus.

2.2.3 Data analysis

To test whether differences in floristic composition between river sections exist, we performed a Multiple Response Permutation Procedure (MRPP, Biondini et al., 1998). The MRPP is a non-parametric measure for testing the hypothesis of no difference between two or more groups of entities. A prerequisite before running the MRPP is that groups must be a priori which for our analysis were defined by plots located on each river section and plots on the tributary river. The computed MRPP

30 Floristic gradient was performed by using Bray-Curtis as distance measure (Bray-Curtis, 1957) which underestimates the influence of outliers (McCune & Grace 2002).

To summarize the spatial heterogeneity of community composition, we performed a Detrended Correspondence Analysis (DCA) on tree species abundance (Jongman et al., 1987). The DCA permits evaluation of beta diversity in terms of standard deviation (length of the gradient) (Duivenvoorden & Lips, 1998; Svenning et al., 2004) and is recommended in the absence of abiotic parameters (Jongman et al., 1987). Analyses were performed using (1) the entire dataset, (2) separately in each of the four sites and (3) excluding the JU plots in order to assess the influence of the Jufaris River´s species pool on the whole tree community. The log-transformed number of individuals per plot was used as a measure of abundance. In order to avoid the over-proportional influence of rare species, only species that occurred in at least two plots were included in the DCA.

The floristic composition was evaluated by examining species and family importance using the Importance Value Index (IVI, Curtis & McIntosh, 1951) and the Family Importance Value (FIV, Mori et al., 1983).Thus, Family Importance Value (FIV) is the sum of relative diversity (Rel Div), relative density (Rel Den) and relative dominance (Rel Dom) as represented by the following formulae:

FIV= (Rel Div) + (Rel Den) + (Rel Dom), where:

Rel Div = (number of species in one family / total species in all plots) x 100

Rel Den = (number of individuals of a family / total individuals in all plots) x 100

Rel Dom= (basal area per family / total basal area in all plots) x 100

The Importance Value Index (IVI) is the sum of relative frequency (Rel Fr), density (Rel Den) and dominance (Rel Dom) of each species. The IVI is represented by the following formulae:

IVI= (Rel Fr) + (Rel Den) + (Rel Dom), where:

Absolute frequency= (number of plots in which species occur / total number of plots) x 100

Rel Fr = (absolute frequency of each species / sum of absolute frequency of species) x 100

Rel Den = (number of individuals of a species / total number of individuals) x 100

Rel Dom= (basal area of a single species / total basal area for all species) x 100

Basal Area= (D2 x π /4) where: D= diameter at breast height (dbh) and π= 3.14159

31 Floristic gradient

Importance values are not influenced either by large numbers of small trees and unequal individual and species numbers per plot (McCune et al., 2002; Wittmann et al., 2006).

Species richness and Fisher's alpha-diversity coefficient (Fisher et al., 1943) were calculated for each plot and river section. Fisher’s index is widely used and is relatively insensitive to sample size thus performing well on tropical forest plots (ter Steege et al., 2000; Chave, 2008). Differences of mean values were compared by using the Welch F-test and a Post-hoc pair-wise comparison using Tukey test. To facilitate comparisons with other studies, values of species richness were standardized to 1-ha. The spatial variation of richness along the river course was investigated by performing a species-area curve. The curve expresses the number of new species in each plot from the lower to the upper river section against the cumulative area of those plots. Total species richness was estimated using the Bootstrap incidence-based and Chao 1 abundance-based richness estimators (Magurran, 2004; Chao, 2005).

The degree of floristic similarity and shared species between river sections and plots was examined by calculating the Chao-Sørensen index for raw data (Chao et al., 2005). This index is based on abundance information and it is appropriate and recommended for data from rapid inventories because it is able more precisely to assess compositional similarity between sites that were undersampled and/or contain many rare species (Chao et al., 2005).

The diversity gradients along geographical regions and geological zones were assessed by plotting Fisher’s alpha coefficient against plots location. Thus, in addition to our results, we compiled available literature on black-water inundation forest across the Amazon and Orinoco basins for which we calculated Fisher’s coefficient (Appendix 1). The plots were classified as plots located in equatorial western Amazonia (WAe), southern western Amazonia (WAs), central Amazonia (CA), northern Amazonia (NA), Orinoco basin (OR) and eastern Amazonia (EA). Similarly, to evaluate the relationship between alpha diversity and geological zones, we overlapped Fisher’s alpha coefficient of each plot over the geological zone in which they occurred. Thus, following the geological map of the Amazon basins by Irion & Morais (2011), plots were sorted in three geological formations (Pre- Cambrian, Tertiary and Pleistocene-Pliocene) representing different bedrock ages.

32 Floristic gradient

Differences in mean values were compared by using Kruskall-Wallis and t-test. Pair- wise comparisons were further assessed using the Mann-Whitney U test.

The relationship of species richness and alpha diversity between igapó and várzea forest was assessed by comparing Fisher’s alpha coefficient and number of species. For igapó we used our results and other published data on black-water systems across the Amazon and Orinoco basins for which values were averaged to 1-ha (Appendix 1). For várzea forest we used data compiled by Wittmann et al. (2006). Significance of mean values was examined by using the t-test and Mann-Whitney U test.

Species richness and diversity were computed with the program PAST v. 2.04 “Paleontological Statistics Software Package for Education and Data Analysis” (http://palaeoelectronica.org/2001_1/past/issue1_01.htm) (Hammer et al., 2001). The number of shared species and similarity matrix was processed by using EstimateS (Version 8.2, R. K. Colwell, http://purl.oclc.org/estimates). Ordination analysis (DCA) and MRPP were performed using the software package PC-ORD version 5.0 (McCune & Mefford 1999). All statistical analyses were carried out with SPSS 16.0 and PAST v. 2.04.

2.3 Results

A total of 6.126 trees were recorded, belonging to 243 species, 136 genera and 48 families. At the plot level (625 m2), the results showed a high variability in families (3 to 17), genera (5 to 24) and species (5 to 25). Values averaged to 1-ha scale showed 612 individuals ha-1, 63 species ha-1, 28 families ha-1 and a basal area of 31.83 m2 ha-1.

2.3.1 Floristic gradients

The MRPP clearly distinguished plots grouped in each river sections and the tributary and identified significant differences in floristic composition among these sites (P< 0.0001). The first axis of the DCA (67% of explained variation) using the entire dataset shows a length of gradient of 5.44 sd of species turnover (Table 2.1). There are few species shared by both ends of the gradient, suggesting high beta diversity (Hill, 1979). Thus, JU and BA have few species in common and occupy the extremes of axis 1 (Figure 2.2a). When JU plots were excluded, the gradient length of the first axis (64% of explained variation) decreased to 4.16 sd (Figure 2.2b,Table 2.1). In

33 Floristic gradient both scatter plots, the second axes have long length of gradients with 5.87 and 4.78 standard deviation units, respectively (Figure 2.2).

Looking at each river section separately, the DCA shows that the JU and BA exert the highest variation, thus increasing beta diversity of the whole dataset. BA had a gradient length of 4.33 and ST and AN of 2.78 and 2.38 respectively, thus reflecting lower beta diversity (Table 2.1). The floristic discontinuity at the middle reach of the river showed by DCA is confirmed with the species-area curve (Figure 2.3), which shows an abrupt change in species numbers. This abruptness is due to the progressive addition of new species from JU plots (plots 85 to 112) and especially plots 81 to 84 at BA. However, the relative position of the species-curve at the end of AN and ST sections tends to stabilize; indicating a low shift in floristic composition.

Preliminary ordinations showed that plots BA 81 to BA 84 at Barcelos and plots JU 17 to JU 28 at the Jufaris River had outlying position due to divergent tree species composition; therefore, these plots were left out for further analyses.

Table 2.1: Summary of DCA analyses of tree species data showing values of the first two axes and inertia of species data DCA Analyses Axis 1 Axis 2 Total inertia of species data Whole dataset

Eigenvalues 0.67 0.42 7.79 Length of gradient 5.44 5.87 Excluding the tributary Jufaris River (JU)

Eigenvalues 0.64 0.38 6.15 Length of gradient 4.16 4.78 River sections Upper reach (ST) Eigenvalues 0.36 0.15 2.97 Length of gradient 2.78 2.60 Middle reach (BA) Eigenvalues 0.66 0.15 2.79 Length of gradient 4.33 1.87 Lower reach (AN) Eigenvalues 0.26 0.19 2.92 Length of gradient 2.38 1.95

34 Floristic gradient

Figure 2.2: Diagrams of the first two axes of sites DCA ordination for all dataset (a) and excluding the tributary river (b). The ordinations are based on log transformed abundance data. The scale marks of the axes are in multiples of the standard deviation (s.d.).

35 Floristic gradient

2.3.2 Floristic composition and importance values

A complete list of all recorded species and their respective families organized by river sections is given in Appendix 2. Most important families and species in each river section are presented in Table 2.2 and Table 2.3, respectively. Few families dominate the composition. Fabaceae was the most important family, which along with Lecythidaceae, Chrysobalanaceae, Euphorbiaceae and Sapotaceae accounted for > 50% of total importance (Table 2.2).

Table 2.2: The 10 most important families at each river section. Relative diversity (rDiv), abundance (rAbu) and dominance (rDom) values are showed in percentages. AAb and BA stand for absolute abundance and basal area (m2), respectively. Families are ranked in order of decreasing importance value. River section Family sp/fam rDiv AAb rAbu BA(m2) rDom FIV (%) (%) (%) (%) Upper section Fabaceae 28 26.17 293 18.59 24.24 26.68 23.81 Santa Isabel Lecythidaceae 6 5.61 487 30.90 19.21 21.14 19.22 (ST) Euphorbiaceae 4 3.74 200 12.69 16.72 18.40 11.61 (n:48; 3 ha) Chrysobalanaceae 7 6.54 100 6.35 3.92 4.31 5.73 Annonaceae 6 5.61 84 5.33 3.83 4.22 5.05 Malvaceae 3 2.80 57 3.62 4.82 5.30 3.91 Lauraceae 4 3.74 43 2.73 4.44 4.89 3.79 Sapotaceae 4 3.74 43 2.73 4.31 4.75 3.74 Melastomataceae 2 1.87 43 2.73 2.00 2.20 2.27 Moraceae 4 3.74 27 1.71 0.56 0.62 2.02 Σ 68 63.55 1377 87.37 84.05 92.50 81.14 Σ 11-33 39 36.45 199 12.63 6.81 7.50 18.86 Middle section Fabaceae 22 25.00 171 9.86 30.63 31.43 22.10 Barcelos (BA) Euphorbiaceae 8 9.09 393 22.66 17.34 17.79 16.51 (n: 32; 2 ha) Chrysobalanaceae 5 5.68 189 10.90 7.75 7.95 8.18 Rubiaceae 3 3.41 224 12.92 5.97 6.12 7.48 Lecythidaceae 5 5.68 90 5.19 6.14 6.30 5.72 Myrtaceae 6 6.82 111 6.40 1.92 1.97 5.06 Lauraceae 3 3.41 82 4.73 5.37 5.51 4.55 Sapotaceae 6 6.82 64 3.69 2.91 2.98 4.50 Annonaceae 3 3.41 51 2.94 5.32 5.46 3.94 Myristicaceae 2 2.27 108 6.23 1.63 1.67 3.39 Σ 63 71.59 1483 85.52 84.97 87.18 81.43 Σ 11-30 16 28.41 47 14.48 8.43 12.82 18.57 Lower section Fabaceae 27 26.47 635 46.32 55.24 59.96 44.25 Anavilhanas Lecythidaceae 7 6.86 196 14.30 6.05 6.57 9.24 (AN) Chrysobalanaceae 7 6.86 78 5.69 3.79 4.11 5.55 (n:48; 3 ha) Annonaceae 4 3.92 55 4.01 4.49 4.88 4.27 Euphorbiaceae 5 4.90 58 4.23 3.20 3.48 4.20 Lauraceae 5 4.90 35 2.55 3.11 3.38 3.61 Moraceae 5 4.90 28 2.04 0.68 0.74 2.56 Sapotaceae 3 2.94 39 2.84 1.35 1.46 2.42 Malvaceae 2 1.96 42 3.06 1.82 1.98 2.33 Olacaceae 4 3.92 17 1.24 1.14 1.23 2.13 Σ 69 68.65 1183 86.00 80.87 87.78 80.57 Σ 11-33 33 31.35 188 14.00 11.26 12.22 19.43 Tributary river Fabaceae 20 24.10 329 22.78 11.46 30.24 25.71 Jufaris (JU) Sapotaceae 5 6.02 198 13.71 4.58 12.08 10.61 (n: 16; 1 ha) Chrysobalanaceae 7 8.43 166 11.50 3.96 10.44 10.12 Euphorbiaceae 8 9.64 131 9.07 2.98 7.87 8.86 Malvaceae 4 4.82 113 7.83 2.54 6.70 6.45 Melastomataceae 1 1.20 117 8.10 2.66 7.03 5.44 Clusiaceae 4 4.82 64 4.43 2.01 5.30 4.85 Humiriaceae 1 1.20 80 5.54 1.82 4.80 3.85 Proteaceae 1 1.20 52 3.60 1.43 3.76 2.86 Lauraceae 4 4.82 11 0.76 0.53 1.41 2.33

Σ 55 66.27 1261 87.33 33.97 89.62 81.07 Σ 11-31 28 33.73 183 12.67 3.93 10.38 18.93

36 Floristic gradient

Table 2.3: The 15 most important species at each river section. Relative frequency (rFre), abundance (rAbu) and dominance (rDom) values are showed in percentages. Species are ranked in order of decreasing importance value. River section Species rFre (%) rAbu (%) rDom (%) IVI (%)

Upper section Gustavia augusta 5.26 17.88 7.56 10.23 Santa Isabel (ST) Hevea brasiliensis 5.64 9.45 12.08 9.06 (n:48; 3 ha) Eschweilera atropetiolata 5.00 7.48 10.62 7.70 Micrandra siphonioides 2.44 2.47 5.70 3.54 Mollia lepidota 3.33 2.92 3.86 3.37 Guatteria sp. 1 2.95 2.35 3.50 2.93 Licania micrantha 2.44 3.55 1.97 2.65 Crudia amazonica 2.56 2.28 3.05 2.63 Mouriri sp. 2.18 2.66 2.19 2.34 Heterostemon mimosoides 2.95 2.73 0.67 2.12 Gustavia sp 2.44 2.66 0.90 2.00 Unonopsis guatterioides 2.69 2.35 0.56 1.87 Licania apetala 2.44 1.90 1.20 1.85 Ocotea cinerea 1.79 1.08 2.57 1.82 Ormosia sp. 1 2.31 1.33 1.80 1.81 Σ 46.41 63.09 58.24 55.91 Σ 16-108 53.59 36.91 41.76 44.09 Middle section Mabea caudata 5.09 12.69 8.50 8.76 Barcelos (BA) Swartzia sp. 1 3.90 2.67 17.89 8.16 (n: 32; 2 ha) Duroia sp. 4.41 13.66 5.87 7.98 Licania heteromorpha 4.92 7.35 5.86 6.05 Ocotea sp. 1 4.41 4.68 4.95 4.68 Virola calophylla 3.90 6.96 1.73 4.20 Amanoa sp. 2.72 5.60 3.79 4.03 Guatteria sp. 1 3.06 2.99 5.44 3.83 Hevea brasiliensis 3.57 2.60 3.00 3.06 Aldina heterophylla 0.68 0.39 6.42 2.50 Eschweilera sp. 1 2.04 1.37 3.73 2.38 Mollia lepidota 2.55 2.28 1.78 2.20 Naucleopsis sp. 2.21 1.37 2.95 2.17 Micropholis sp. 2.55 2.08 1.42 2.02 Eschweilera atropetiolata 2.21 2.54 1.06 1.94 Σ 48.21 69.22 74.41 63.95 Σ 16-79 51.79 30.78 25.59 36.05 Lower section Aldina heterophylla 4.72 8.61 40.04 17.79 Anavilhanas (AN) Heterostemon mimosoides 6.67 20.93 5.71 11.10 (n:48; 3 ha) Eschweilera aff. amazoniciformis 5.83 7.73 4.54 6.04 Peltogyne excelsa 2.92 3.50 4.80 3.74 Licania apetala 3.06 3.28 2.55 2.96 Tachigali venusta 3.47 3.28 1.77 2.84 Gustavia augusta 3.19 4.01 0.93 2.71 Guatteria aff. olivacea 2.50 1.46 4.07 2.67 Mollia speciosa 2.78 2.55 1.38 2.24 Ocotea cinerea 2.22 1.75 1.87 1.95 Tapirira guianensis 1.81 1.31 2.32 1.81 Aspidosperma nitidum 1.94 1.31 1.67 1.64 Virola surinamensis 1.67 1.17 1.89 1.58 Micrandra siphonioides 1.39 1.31 1.99 1.56 Swartzia macrocarpa 2.08 1.46 0.62 1.39 Σ 46.25 63.67 76.12 60.01 Σ 16-102 53.75 36.33 23.88 39.99 Tributary river Mouriri angulicosta 4.55 8.10 7.03 6.56 Jufaris (JU) Sclerolobium chrysophyllum 4.55 4.50 5.75 4.93 (n: 16; 1 ha) Sacoglottis guianensis 4.33 5.54 4.80 4.89 Pterocarpus rohrii 1.73 5.82 6.89 4.81 Aldina heterophylla 4.55 3.05 6.38 4.66 Pouteria elegans 3.46 5.06 3.63 4.05 Micropholis egensis 2.81 4.85 3.77 3.81 Caraipa sp. 2.60 3.95 4.85 3.80 Panopsis sessilifolia 3.90 3.60 3.76 3.75 Mollia speciosa 1.73 5.12 4.14 3.67 Manilkara huberi 2.81 3.67 4.40 3.63 Licania micrantha 2.81 4.29 3.68 3.60 Licania apetala 3.68 3.19 3.06 3.31 Amanoa gracillima 0.87 4.71 3.97 3.18 Ormosia excelsa 2.81 2.42 1.69 2.31 Σ 47.18 67.86 67.80 60.95 Σ 16-57 52.82 32.14 32.20 39.05

37 Floristic gradient

The most species-rich genera were Swartzia (11 species), Pouteria (8 species), Eschweilera (7 species), Ocotea (6 species), and Ormosia and Zygia (5 species each). These genera accounted for 14.2% of all recorded species (data not shown).

The Importance Value Index (IVI) of the species indicated a high floristic variation between river sections (Table 2.3). Only few species, including Gustavia augusta, Heterostemon mimosoides, Hevea brasiliensis and Aldina heterophylla occurred in more than one river section. At Santa Isabel (ST) the 15 most important species accounted for 56% of the IVI. Gustavia augusta (10.23%) is the most important specie followed by Hevea brasiliensis (9.06%) and Eschweilera atropetiolata (7.70%). Other relatively important species at ST are Mollia lepidota, Licania micrantha and Crudia amazonica which all together accounted for 8.65% of the total IVI (Table 2.3). The 15 most important species at the Barcelos (BA) accounted for 63.95% of the total IVI. In contrast to the ST plots, there are no species that clearly stand out among the others as the most important. The most important species is Mabea caudata (8.76%) followed by Swartzia sp. (8.16%) Duroia sp. (7.98%), Licania heteromorpha (6.05%) and Ocotea sp. (4.68%).

At Anavilhanas (AN) the most important species is the emergent legume Aldina heterophylla (17.79%), followed by Heterosthemon mimosoides (11.10%) Eschweilera cf. amazoniciformis (6.04%) and Peltogyne exclesa (3.74%). These species accounted for 38.67%, while the remaining species have less than 3% of IVI. The floristic composition at JU was distinct. The most important species is Mouriri angulicosta followed by Sclerolobium chrysophyllum and Sacoglottis guianensis. These species accounted for 16.38 % of the importance, but did not occur in the other river sections.

2.3.3 Tree species richness and diversity

Species richness estimations for the whole dataset are presented in the Figure 2.3. The estimators Bootstrap (ocurrence data) and Chao 1 (abundance data) accounted for 263 and 255 species, indicating that the sampled species represent 92% and 95% of the estimated species richness, respectively. Both richness estimators reached an asymptote at 250 species representing an inflection at an area of 6 ha which corresponds to 96 plots (Figure 2.3).

38 Floristic gradient

Figure 2.3: Species - area curve accumulating new tree species occurring in 625 m2 from upper to the lower reach of the Negro River, including the tributary Jufaris River. The curve show the major discontinuity at the middle reach, where plots BA 81 to BA 84 exert the greatest influence.

Comparing species richness between river sections the Welch F test shows a significant difference (F= 7.46, P<0.001). A Welch F test (F=7.52, P<0.001) and the post-hoc pair-wise comparison (Tukey test) detected significant differences between BA and JU, (P <0.001) and AN, (P=0.007). The Tukey post-hoc test revealed significant difference between AN 2 and ST 2, BA 1, BA 2 and AN 1 (all with P < 0.001). Although both JU and BA plots are located in the same river section the Tukey post-hoc test revealed significant differences in species richness between these sites (JU compared with BA 1 P= 0.03; BA 2, P= 0.02). There were no statistically significant differences between ST and BA plots (P >0.05).

The Welch test further showed significant differences in alpha-diversity across the river sections (F=6.28, P < 0.001). A Tukey post-hoc test revealed significant differences between JU and ST (P=0.01) and highly significant difference compared with AN (P=0.001). However, values did not differ significantly between ST and AN (P=0.88). When performing intra-site comparison the Welch F test detected significant differences (F= 9.42, P < 0.001). However, pair-wise comparisons determined by the Tukey post-hoc test revealed that except for ST 1 (P=0.198), the ST 2 and AN 1 sites presented a significant difference compared with the other sites

39 Floristic gradient

(P < 0.001). These two sites have the highest diversity values averaged per hectare (as indicated by the Fisher’s alpha coefficient (Table 2.4).

Table 2.4: Species richness, alpha diversity and abundance for the four forest communities averaged to 1 ha. N is the number of individuals, S is the total number of species registered and α is Fisher’s index of diversity (Fisher et al., 1943) defined by S= α *ln(1+n/ α).

Sites Fisher’s index River section N S (α)

Upper section ST 1 504 64 19.43 Santa Isabel (ST) ST 2 500 67 20.81 (n: 48; 3 ha) ST 3 573 60 16.88 Middle section BA 1 722 68 18.41 Barcelos (BA) BA 2 808 57 13.99 (n: 32; 2 ha) Lower section AN 1 468 79 27.24 Anavilhanas (AN) AN 2 398 51 15.54 (n: 48; 3 ha) AN 3 505 63 18.99 Tributary Jufaris river (JU) JU 593 57 15.44 (n: 16; 1 ha)

For better comparisons species richness and alpha-diversity were extrapolated to 1 ha (Table 2.2). Thus, at this level, species richness did not show much variation; values ranged from 57 species ha-1 at BA 2 and JU to 79 species ha-1 at AN 1 (Table 2.2). The average value for the whole sample was 63 tree species ha-1. The Fisher’s alpha coefficient confirmed that AN 1 and ST 2 were overall the most diverse (P < 0.001), however, these sites also presented the lowest number of individuals in the whole dataset (Table 2.4, Figure 2.4). Although species composition was highly variable between river sections, species richness and alpha-diversity averaged to 1- ha were rather constant, with a slight increase in the upper and lower sections (ST and AN, respectively).

Figure 2.4: Fisher’s alpha index and number of individuals plotted against river sections. ST (n: 48, Santa Isabel), BA (n: 32, Barcelos), JU (n: 16, Jufaris) and AN (n: 48, Anavilhanas). Error bars, SD.

40 Floristic gradient

2.3.4 Floristic resemblance between river sections

Floristic similarity (Chao-Sørensen) of species composition between river sections averaged 0.35 (0.26-0.63). AN and ST were the most similar river sections (63% of similarity, 49 shared species), whereas JU and AN were the less similar (26% of similarity, 14 shared species) (Table 2.5). JU was the most distinct forest community. At this site the average floristic similarity between plots amounted to 0.24 (range = 0.19 – 0.42).

Table 2.5: Similarity matrix of floristic composition between (a) 1-ha scale and (b) river sections based on Chao-Sørensen index. Highest and lowest values of floristic similarities are highlighted in grey.

a) Chao-Sørensen index 1-ha plots AN1 AN2 AN3 BA1 BA2 JU ST1 ST2 ST3 AN 1 1 0.85 0.9 0.35 0.36 0.28 0.65 0.51 0.55 AN 2 38 1 0.96 0.45 0.54 0.25 0.46 0.53 0.54 AN 3 46 40 1 0.4 0.41 0.32 0.73 0.53 0.6 BA1 20 13 16 1 0.88 0.35 0.58 0.6 0.55 BA2 18 12 14 46 1 0.42 0.52 0.41 0.41 JU 13 9 13 12 13 1 0.37 0.19 0.31

Shared species ST1 29 17 23 29 22 14 1 0.94 0.81 ST2 27 17 23 26 19 12 39 1 0.89 ST3 27 17 22 27 22 10 35 39 1 b)

River section Anavilhanas Barcelos Jufaris Santa Isabel Anavilhanas (AN) 1 0.47 0.26 0.63 Barcelos (BA) 29 1 0.27 0.60 Jufaris (JU) 14 14 1 0.31

Shared species Santa Isabel (ST) 49 42 17 1

The floristic resemblance within river sections showed high similarity. Thus, at AN, BA and ST sites, the similarity index showed an average of 62% of similarity and over 35 of shared species (Table 2.5). These findings suggest that geographical distance may be an important factor determining floristic similarity within river sections. However, we also found that closer sites are not always more floristically similar. There is less floristic similarity between JU and BA, which are ca. 100 km apart (35% of similarity, 12 shared species) than similarity between AN 1 and ST 2 (51% of similarity, 27 shared species) which are located approximately 600 km apart.

2.3.5 Diversity gradients of igapó across geographical regions and geological zones

When, quantifying spatial gradients of alpha-diversity by comparing Fisher’s alpha of all igapó studies, the Kruskal-Wallis test was not significant (P-value= 0.06).

41 Floristic gradient

Nevertheless, pair-wise comparisons (Mann-Whitney test) indicated significant differences between some regions (Figure 2.5; Figure 2.6). Highly significant difference (P-value= 0.01) was found between plots in the southern Western Amazonia (n: 5, WAs) and northern Amazonia (n: 5, NA).

80 80 10

60 60

40 40 Fisher´s alpha

Fisher´s alpha 20 20

0 0 Tertiary Pleistocene- Pre-Cambrian WAs WAe CA OR NA EA Pliocene Region Geological zone

Figure 2.5: Fisher’s alpha diversity in Figure 2.6: Fisher´s alpha diversity plotted different region across the Amazon. WAs = against geological formations. Tertiary: southern western Amazonia, WAe = tertiary lowlands, Pleistocene-Pliocene: equatorial western Amazonia, CA = central youngest bedrocks and Pre-Cambrian: oldest Amazonia, OR = Orinoco basin, NA = bedrocks including Brazilian and Guyana northern Amazonia and EA = eastern Shields. Data of geological formations derived Amazonia. from Irion & Morais (2011).

Although alpha-diversity among the three geological formations was different, it was not significant (P-value 0.30). Mean values of Fisher’s α increased from oldest to youngest geological formations from 18.04 upon the Pre-Cambrian Shield (n: 12), to 20.38 upon Tertiary Lowlands (n: 9) and 25.60 upon the Pleistocene-Pliocene formation (n: 23) (Figure 2.6).

2.3.6 Comparison of igapó with várzea

The comparison of tree species richness (S) and alpha-diversity (Fisher’s α) between igapó (n=26) and várzea (n=22) across the Amazon and Orinoco basins indicated higher mean values in the várzea than in the igapó (Figure 2.7). Species richness and Fisher’s alpha were 81.45 and 29.66 in the várzea, and 74.27 and 23.63 in the igapó, respectively. However, the t-test did not show significant differences (S: t=0.75, two tailed P-value= 0.46; Fisher’s α: t= 1.20, two tailed P-value= 0.23). The difference in species richness and diversity was also tested with the Mann-Whitney U test. Although ranks of várzea are higher for both species richness and Fisher’s

42 Floristic gradient alpha, no significant differences were detected (S: 2 tailed P-value = 0.38; Fisher’s α: 2 tailed P-value = 0.33).

When comparing only data from our data at 1-ha scale (n: 9) with floristic inventories in the várzea we also did not find significant differences (two tailed P-values S= 0.16; Fisher’s α= 0.12). Except for the AN 1 plot at the lower Rio Negro, the values of species richness and alpha-diversity registered in our study are below the means calculated for all igapó sites across the Amazon and Orinoco basins.

160 23 14 80 140 23 ) 120 α 60 100

80 40

60

Fisher´s alpha ( Fisher´s alpha 20 Species richness (S) richness Species 40

20 0

Igapó Várzea Igapó Várzea Forest type Forest type

Figure 2.7: Comparison of species richness (S) and alpha-diversity (α) between igapó (n: 26) and várzea (n: 22) forests. Data for igapó are derived from Appendix 1. Várzea quantitative inventories across the Amazon were compiled by Wittmann et al. 2006. Only inventories standardized at 1-ha and trees ≥ 10 cm DBH were considered. The box plots show the median, quartiles and extreme values (outliers: cases with values between 1.5 and 3 box lengths from the upper or lower edge of the box, depicted as an open circle; extreme cases: values more than 3 box lengths from the upper or lower edge of the box, depicted as a star).

2.4 Discussion

2.4.1 Spatial floristic patterns

In agreement with other studies we consistently found evidence for floristic discontinuity and heterogeneity in species composition along the river course (Rosales et al., 1999; Albernaz et al., 2011). The most important species at each river section shape a unique species pool while no significant differences in species richness and Fisher’s alpha between sites were detected. Moreover, species composition at different sites appears to change abruptly from one river section to the next. These results are in accordance with the hypotheses of homogeneity and ecological determinism, which are two of the most debated hypotheses describing spatial tree distribution at landscape scales in Amazonian rain forests. Although our

43 Floristic gradient objectives are not to test these two hypotheses, in what follows we discuss our main findings of the study.

According to the homogeneity hypothesis, forests are in essence uniform and dominated by a small proportion of species, forming predictable associations or “species oligarchies” which are relatively constant over huge geographical areas (Pitman et al., 2001; Terborgh et al., 2002). This is reflected in our results by the fact that 62.3% of individuals belong to the 30 most abundant species. Likewise, at each river section, above 60% of relative abundance values are composed by only 15 species. The presence of species oligarchies for trees and other life forms has been well documented in terra firme forests (Pitman et al., 2001; Vormisto et al., 2004; Macía & Svenning, 2005; Macía, 2011; but see Toledo et al., 2011 for criticism). For várzea forests, Wittmann et al. (2010) suggested that species oligarchies are even more evident than in terra firme due to the high connectivity of riparian corridors. Based on the occurrence and distribution of the 186 most common Amazonian várzea tree species, according to Wittmann et al. (2010), oligarchies are mainly composed of generalist species (90 %) which occur also in other neotropical ecosystems, while the remaining 10 % are endemic species (sensu Ricklefs, 1990) that dominate large areas along river courses.

However, despite the connectivity between river sections in our study, data exhibited a particular set of few species that dominates each river section, indicating a marked geographical/environmental gradient and high species turnover. This leads us to discuss the second view that explains the spatial distribution of trees across the Amazon. Tree communities appear to be assemblages related to local ecological determinism. This hypothesis argues that forests are a mosaic in which species distributions change continuously along environmental gradients. Thus, the environment (e.g. soil texture or height and duration of flooding) constitutes strong filters, determining which and how many species are present in the community (Gentry, 1988; Tuomisto et al., 2003; Higgins et al., 2011). These predictions are consistent with our results in three aspects: 1) the clear assemblage of plots into four river sections exhibiting highly significant differences in floristic composition; 2) the comparatively high beta diversity detected (Hill, 1979); and 3) the lack of overall dominant species with occurrence in all river sections.

A few studies on Neotropical floodplain forests have shown a significant floristic discontinuity along the course of water bodies. In a recent floristic study on várzea

44 Floristic gradient along ca. 2800 km corridor of the main course of the Solimões-Amazon River, Albernaz et al. (2011) identified three main biogeographic regions defined by significant compositional differences along the course of the river. The authors further concluded that these regions were delimitated by a strong floristic variation caused mainly by the effect of geographical position on species composition. In the Orinoco basin, Rosales et al. (2001) found an abrupt change in species composition along a 260 km corridor of the lower Caura River (black-water) with floristic components from both várzea and igapó forests. This pattern was interpreted by the authors as a response of the influence of the rich nutritional status of the Orinoco on the lower Caura. The biogeochemical gradient with the input of fertile sediments may control the occurrence of igapó and várzea tree species. Similarly, in central Amazonia Rodrigues (2007) found a marked floristic gradient between igapó and várzea along 45 km of the Amanã Lake, concluding that the soil chemistry is the main driver influencing tree species distribution.

Although our study areas are located along the same riverine system, we did not observe a transition of tree composition between sites at the lower reach and others upstream. In addition to the large geographic distances between study areas, this abruptness might be a response to the variable flooding regime along the course of the Negro River. Thus, flood amplitudes increase from the upper (3.6 m) to the lower (9.3 m) sections of the River, subjecting igapó trees to periodic flooding lasting from 50 to 230 days year -1, respectively. Furthermore, spatial floristic patterns may be determined by the status of alluvial soils (i.e. chemistry and granulometry), which may change in function of the position of the river and the influence of tributaries along the entire course (Prance, 1979; Kubitzki, 1989, Junk et al., 2011). Finally, channel dynamics and geomorphology may also exert certain influence on the floristic variation along the course of the Negro River (Salo et al., 1986; Latrubesse & Francinelli, 2005; Wittmann et al., 2004; Peixoto et al., 2009).

2.4.2 Floristic composition

At the family level Fabaceae, Lecythidaceae, Chrysobalanaceae, Euphorbiaceae and Sapotaceae are the most important families at each river section. While Fabaceae is widely distributed across different forest types in the Amazon, Lecythidaceae and Chrysobalanaceae are particularly abundant and relatively richer in species in the eastern Amazonia and the Guianas (Gentry, 1990; ter Steege et al., 2000; Honorio- Coronado et al., 2009). Mori (2001) points out the huge diversity of species of Lecythidaceae in black-water systems. This author reported that 38 species of

45 Floristic gradient

Lecythidaceae are present in the Negro River basin, suggesting that this area is perhaps an endemism and distribution centre for this family. Other important families are Annonaceae, Malvaceae, Rubiacae and Sapotaceae, the latter is ranked among the top most important families along the Jufaris River and seems to be most abundant family in Central Amazonia (ter Steege et al., 2000; Honorio-Coronado et al., 2009). At the generic level, with the exception of Ocotea, the most diverse genera in our dataset are originated in the Neotropics and are widely distributed in lowland rainforest (Gentry, 1993; ter Steege et al., 2006; Pitman et al. 1999). The influence of the Guyana Shield may be revealed by the presence of the genera Henriquezia, Micrandra, Macrolobium, Heterostemon, Mollia, Swartzia, Cynometra, Simaba and Peltogyne.

The floristic composition at the Jufaris River (JU) varies markedly from the other river sections. This is a black-water northern tributary that flows through savanna-like white-sand flooded vegetation thus determining its particular tree composition. Altogether, the 57% of species occurring at Jufaris were only reported at this site (Appendix 2). In fact, most important species (Mouriri angulicosta, Sclerolobium chrysophyllum and Sacoglottis guianensis) also occur on white-sand and terra firme forests (Stropp, 2011) and they were not recorded in other river sections of this study or other studies along the Negro River. According to Kubitzki (1989) resemblance of flooded forests by black-water Rivers with savanna vegetation on oligotrophic white sand is caused by the water chemistry which appears to be the most important factor driving floristic differentiation in Amazonian igapó.

2.4.3 Species richness and diversity patterns

The results indicate that species richness and alpha diversity tend to be slightly higher at Anavilhanas than in the other river sections. This is mainly due to the influence of the plot AN 1 with 79 species ha-1 and a Fisher’s alpha coefficient of 27.24. The tendency of a higher richness and diversity at the lower reach of the Negro River has also been reported by other studies at Tarumã-Mirim (Worbes 1986, Parolin et al., 2004) and also at Anavilhanas (Parolin et al., 2003; Piedade et al., 1985; Piedade et al., 2005). That this region is characterized by high species richness and diversity may be partially explained by the presence of finer sediments, which are slightly more fertile than those upstream (Junk et al., 2011). Increased soil fertility at AN may permit conditions for the development of higher beta-diversity, resulting in higher species richness and alpha-diversity. This explanation, however, is challenged by a study on the Jaú River (north-western tributary, upstream from

46 Floristic gradient

Anavilhanas) which recorded the highest species richness (≥ 10 cm dbh) reported for the igapó of Amazonian black waters (Ferreira, 1997). Along three different habitats (lake, river margin and stream) this author recorded 44, 103 and 137 species ha-1, respectively. The author further attributed the difference in species richness between habitats to the variation of flooding duration, without emphasizing possible causes for the overall high species richness in this sector of the Negro River.

Although Barcelos (BA) and Jufaris (JU) have the highest number of individuals per hectare, they have the lowest alpha-diversity indicating that the number of individuals is not the proximate driver of diversity at these river sections. This pattern has also been reported by other studies in igapó (Ferreira 1997, Gribel et al., 2009) and várzea (Schöngart, 2003, Campbell et al., 1992). A reasonable explanation for this pattern can be found in the characteristics of forest succession. Although we focused on mature forest, there are no studies that determine tree ages and addresses successional stages in our sampling areas. The common factor in these forest types is probably the limited availability of resources, which may lead to an interspecific competition resulting in a low alpha diversity (Tilman, 1982). Thus, spatial heterogeneity in the availability of limiting resources can generate a mosaic of species composition (Terborgh et al., 2002). Therefore, in contrast to Condit et al. (1996) and besides other possible causes (i.e. succession), our results suggest that the number of tree species per unit area in the nutrient-poor igapó forest tends to decrease with increasing number of individuals present in a sample.

At a regional scale, non-flooded rainforests adjacent to the Negro River basin host one of the richest tree communities in Amazonia. A single hectare of terra firme in this region can hold up 285 tree species with dbh ≥ 10 cm (Oliveira & Mori, 1999), while várzea forests can reach up to 142 species ha-1 (Wittmann et al., 2002) and white-sand forest around 100 species ha-1 (Stropp et al., 2011). Our findings, however, show an average of 63 species ha-1 confirming that the late-successional igapó forests along the Negro River is one of the poorest mature forest types per unit area in the Amazon. This is also confirmed by the Fisher’s alpha coefficient calculated for each river section which ranged between 13.99 (Barcelos) and 27.24 (Anavilhanas).

The key to understand the variation of diversity patterns along the course of the river lies in processes that act on a regional and local level. Thus, at regional scale (along the river) the driving forces shaping diversity may be geographic distance and the

47 Floristic gradient influence of adjacent forest types, while at local scale (lateral gradient) environmental filters such as flooding and soil fertility may play a key role in determining diversity patterns. The former may help to explain the slight increase in species richness and diversity in the lower Negro River, indicating that the species pool at the Anavilhanas sites can draw from a larger regional species pool. Thus, due to the proximity and connectivity with the Solimões-Amazon River and the influence of the Branco River, the resemblance of our species pool at Anavilhanas with várzea may increase while decreasing at sites further upstream. A recent study comparing tree communities on white-sand forest between upper and lower Negro basin (Stropp et al., 2010) found also a strong variation and a highest local tree alpha diversity at the lower Negro river basin. Similarly, gradients of tree alpha diversity of terra firme forests increase along the Negro River from northwest (upper) to southeast (lower) (Amazon Tree Diversity Network: collective authors ATDN 2011).

2.4.4 Diversity gradients at continental scale

Data on terra firme and várzea forests suggest a trend of increasing alpha-diversity from east to west (ter Steege et al., 2003; Wittmann et al., 2006). For igapó forests our comparison show that plots at equatorial western Amazonia (WAe) and Orinoco (OR) present a slight tendency to have higher alpha diversity than in the other regions. The two opposite extreme of the region, southern western Amazonia (WAs) and eastern Amazonia (EA) present the lowest alpha diversity, whereas central (CA) and north Amazonia (NA) plots have intermediate values. When considering alpha diversity in relation to the age of the bedrock, plots occurred on older formations (Guyana and Brazilian Pre-Cambrian Shields) show the lowest alpha diversity. Plots occurring on younger bedrocks mostly influenced by Andean sediments (Sombroek, 2000) present the highest alpha diversity.

The fact that plots on Pre-Cambrian bedrocks is less diverse than younger geological formations may be partly explained by the nutrient status of the soils. In agreement with earlier studies, our comparisons indicate a gradual decrease of alpha diversity while increasing the age the geological formations. This pattern may reflect a transition from recently deposited and nutrient-rich sediments of Andes origin in the west to older weathered and nutrient-poor soils in the East (Irion et al., 1984; ter Steege et al., 2006, Pitman et al., 2008, but see Higgins et al., 2011 for critics). In this dynamic, the uplift of the Andes and its effect on regional climate greatly reconfigured the drainage patterns creating a vast influx of sediments into the basin

48 Floristic gradient

(Hoorn et al., 2010), which spread over hundreds or thousands of kilometers toward the West (Higgins et al., 2011).

In this scenario, the flooded landscape of the lower reaches of the lower Negro has been formed by very young Holocene deposits, in which its floodplains have experienced a more dynamic fluvial geomorphology than middle and upper sections. For example, in the Holocene 10 meters thick fine sediment was deposited in large parts of the lower Negro valley during high sea level stages (Irion et al., 2010). In contrast, the middle and above all the upper sections are characterized by a more stable landscape (E. Latrubesse, pers.comm.), where the bed loads is mostly composed of white supermature quartz sand (Latrubesse & Franzinelli, 2005).

Preliminary results of the Hybam project (Hydro-geodynamics of the Amazon Basin) across the Amazon basin revealed that at Santa Isabel region (upper Negro River) at the Serrinha station, the Silicate concentrations have the lowest values compared to other places in the Amazon basin. This is probably due to the high proportion of podzols and arenosols covering this region, which are mature and highly weathered soils, therefore with a very low capacity to release dissolved materials into the river (Moquet, 2011). With all, the lower section of the Rio Negro has continuously received fine-grained sediments and its hydro geomorphology dynamic is recent, while the middle and upper sections are more stable environments. This dynamic played a crucial role in determining the current pattern of tree diversity of igapó and ruled the distribution and establishment of endemic species.

2.4.5 On the relationship between diversity of igapó and várzea

It has been debated whether várzea or igapó forests are more diverse. On the one hand, comparisons between both forest types near Manaus (Worbes, 1986, 1997), at the Floresta National de Caxiuanã and Gunma National Park both in Pará (Ferreira et al., 2005; Ferreira et al., 2010) and Viruá Park, Roraima (Gribel et al., 2009) indicate higher species richness in igapó forests. On the other hand, the tendency that species richness is lower in igapó than in várzea is supported by Ayres (1993) and Prance (1987). In addition, other recent comparative studies in central and western Amazonia also reported that igapó is poorer in species than várzea (Haugaasen et al., 2006 at the lower Purús River; Inuma 2006 in the Amanã Sustainable Development Reserve and Mostacedo et al., 2006 in northern Bolivian Amazon). The fact that várzea is richer than igapó is further supported by Wittmann

49 Floristic gradient et al. (2010) who estimated over 1000 tree species occurring on várzea being by far the most species-rich floodplain forests worldwide.

Although we did not detect significant differences between means, our results support the hypothesis that várzea´s species richness and alpha diversity are higher than igapó. However, forest types of the Rio Negro (beta diversity) tend to increase due to the influence of tributary rivers by adding new species. In this sense, Kubitzki (1989) argued that despite local species diversity being higher in the várzea than in the igapó, the flora of the former is more uniform than that latter, which seem to have higher regional differentiation. This is supported by our results, in which the Jufaris River contributed 47 species, those representing 19% of the total species pool in our dataset.

Despite hydrological connectivity between the igapó of the Negro River and white- water rivers, only 34% of all recorded igapó species in this study (identified at species level) were described to occur in várzea forests, the remaining species occur in terra firme, white-sand forests or wet savannas. Wittmann, et al. (2010) reported that in western Amazonia around 60% of the 186 most important várzea tree species are shared between várzea and terra firme, while only 12% occur in Amazonian igapó (data mainly from the lower Negro). The authors further concluded that there are more várzea species shared with floodplains in the Orinoco basin in Venezuela (51%), which is not hydrological connected to Amazonian várzea than with igapó forests of the Negro River. These numbers suggest that the geographic position is an important driver of floristic dissimilarity between terra firme and alluvial floodplain forests as observed by Terborgh & Andresen (1998). Thus, tree communities of inundated forests tend to more closely resemble those of terra firme forests within the same geographical region than those of inundation forests in adjacent regions (Terborgh & Andresen, 1998).

2.5 Conclusion

Our results suggest that although mean alpha measures of diversity may not consistently differ between river sections, species turnover (beta diversity) is consistently high and significant. The significant floristic contribution of tributary rivers (e.g. Jufaris River) to the overall species pool suggest that beta-diversity of igapó forests along the Negro River tends to increase as a function of regional species pools. Species richness and alpha diversity revealed that the late-successional igapó forest of the Negro River is one of the poorest floodplain forest types in the Amazon.

50 Floristic gradient

The effect of spatial distance combined with the variable flooding regime, status of the alluvial soil and fluvial geomorphology along the course of the River may control the floristic variation of the igapó forests. On a continental scale, our data show a trend of increasing diversity along an east to west gradient. Plots situated in the western equatorial Amazonia and the Orinoco show the higher alpha diversity; whereas plots located on the eastern edges of the Amazon region have the lowest values of alpha diversity. When overlapping plots on geological zones we found a gradual decrease of alpha diversity while increasing the age the geological formations, indicating the strong influence of bedrocks and derived soils as controlling factors of diversity patterns across the Amazon.

The floristic data presented in this study are the first of their kind on black-water flooded forest which are based on an extensive quantitative dataset, thus substantially increasing the floristic knowledge of igapó forests. This information constitutes the first attempt to describe the floristic variation in terms of species composition and diversity of the igapó forest along the course of the Negro River thus filling a research gap on Amazonian floodplains. We suggest caution with the results as these reveal the interpretations of the late-successional stage of the igapó forests without considering early successional stages or tree communities along the border zone on the river banks. The results contribute essential data for the classification and management recommendations of Amazonian wetlands, which is an initiative lead by the wetland monitoring working group at the Brazilian National Institute of Amazon research (INPA). Similarly, our main findings constitute the starting point to seek answers to for example why the igapó is so poor in tree species and what are the causes that determine the abrupt changes in species composition along the course of the river.

51 Effect of flooding and soil on igapó

3

EFFECT OF FLOODING REGIME AND SOIL ON TREE DIVERSITY AND COMPOSITION OF IGAPO FORESTS ACROSS THE NEGRO RIVER, CENTRAL AMAZONIA

52 Effect of flooding and soil on igapó

3 Effect of flooding regime and soils on tree species composition and diversity of igapó forests across the Negro River, central Amazonia

3.1 Introduction

On large river floodplains the pulsing system of rivers exerts a strong influence on the floristic composition and vegetation dynamics. This is underlined by the Flood Pulse Concept (FPC, Junk et al., 1989) which provides a unique framework for understanding ecological structures and functions in periodically flooded systems (Junk, 2005). The FPC explains how periodic flooding imposes a drastic impact on the biota and biogeochemical processes inside the floodplain. The concept predicts that the nutrient status along the floodplain is dependent upon the amount and quality of dissolved and suspended solids of the parent river, implying an internal mechanism of nutrient transfer between the terrestrial and the aquatic phase (Junk & Wantzen, 2004; Junk, 2005). A key character of the flood pulse in central Amazonia is its predictability and long duration. As consequence, organisms, for example trees, respond combining a set of morphological and physiological strategies to survive weeks or months under partial or total submergence (Kozlowski, 1984; Worbes, 1997; Parolin, 2009; Parolin et al., 2010). These survival strategies, expressed by the floodplain trees, are clear demonstrations that in a constrained aquatic-terrestrial environment, flooding stress may be a strong driver of adaptive evolution (Jackson & Colmer, 2005). Therefore, the pulsing system of large rivers, such as the Negro, shapes the flooding and soil gradients, which control the establishment and growth of trees, and may therefore be a strong predictor of tree diversity and species composition along river corridors and lateral river-floodplain connections.

In Amazonian floodplain forests, the relationship between floristic patterns and flooding regimes has been well documented. Based on data collected in várzea (white-water floodplains) and igapó (mainly on lower Negro River) studies have identified that the factors determining species distribution and diversity patterns along lateral gradients can be mainly attributed to the flood tolerance of species and to a lesser degree to edaphic conditions. Thus, as tolerance differs among species, these differences are reflected by vegetation zonation restricting species to a certain range of the flooding gradient. Likewise, several authors have noted that species richness and diversity increase with decreasing height and duration of inundation (Keel & Prance, 1979; Junk, 1989; Duivenvoorden & Lips, 1991; Ferreira, 1997; Worbes,

53 Effect of flooding and soil on igapó

1997; Wittmann et al., 2002, Wittmann et al., 2006, Rosales et al., 2001; Piedade et al., 2005).

On igapó forests, the increase of species richness with decreasing height of inundation was reported by Inuma (2006) at the Amanã lake (Amanã Sustainable Development Reserve). This author analyzed species richness of trees ≥10 cm diameter at breast height (d.b.h) in three different inundation levels and found a linear increase from 26 species (height: 7-5 m) to 35 and 44 species at inundation levels of 5–3 m and 3–1 m, respectively. Similarly, at the Jaú River, which is a north-western tributary of the Negro River, Ferreira (1997) found a significant influence of the duration of inundation period on species richness in three different plots, each of them representing different habitats. Thus, tree species richness increased from the plot lake (266 days year -1, 10 species) to the plot river (162 days year -1, 35 species) and plot stream (62 days year -1, 40 species). The author also found a high dominance and abundance of few species in plots where the period of inundation is longer (i.e. plot lake) and life conditions are quite extreme (Ferreira, 1997). The pattern of increasing species richness with decreasing height and duration of inundation observed for trees has also been reported for saplings and seedlings in várzea forests (Wittmann & Junk, 2003; Oliveira-Wittmann et al., 2007; de Assis & Wittmann, 2010). According to the aforementioned empirical evidence, flooding superimposes the influence of other abiotic and biotic factors, in which the duration of inundation may exert the major role.

However, despite the observed strong impact of the flooding regime on tree distribution and diversity, some studies have concluded that flooding alone cannot predict floristic variation of igapó forests, but other abiotic factors must be considered (Ferreira & Parolin, 2011). On the lower Rio Negro, data have demonstrated that substantial differences in height and duration of flooding between two similar forest types separated approximately 200 km do not necessarily lead to marked differences in species richness (Ferreira & Stohlgren, 1999; Ferreira, 2000; Ferreira & Almeida, 2005). Conversely, under identical flood stress (height and duration) along a 48 km- long transect on the Amanã Lake, species composition and distribution changed abruptly (Rodrigues, 2007). In both cases, differences in topography and soil fertility were mentioned as the primary determinants of floristic variation. Similar patterns have also been documented by other studies on floodplain forests and riverine systems outside of the Amazon basin, where topography and soil were identified as

54 Effect of flooding and soil on igapó important factors structuring tree communities (southern Brazil: Oliveira-Filho et al., 1994; Budke et al., 2007; temperate black-water river: Burke et al., 2003).

Two recent studies, at different spatial scales suggest that flooding may not be the only factor explaining the variation of tree species richness along river corridors and lateral gradients. At a regional scale a study based on an extensive inventory of trees >10 d.b.h, on late-successional forest along ~ 600 km corridor of the Negro River (Montero et al., in press) found no substantial differences in tree species richness between the studied sites. Despite sharp gradients of flood amplitude and differences of soil granulometry along the studied area (Junk et al., 2011) the authors reported almost constant values of tree richness averaged to 1-ha. In contrast, high species turnover reflected by changes in species composition along the course of the river was observed. At the lower Rio Negro, Ferreira & Parolin (2011) analyzed the effect of duration of inundation on tree species richness along lateral gradients (local scale) including seedlings and saplings across different topographic levels. The authors found no significant influence of inundation on the species richness, suggesting that patterns of tree species richness along lateral gradients are controlled by a more complex set of factors. Instead, the authors found a distinctive set of species dominating major topographic levels indicating differences in physiological tolerance of species to flooding (Parolin, 2009).

In general, it is reasonable to suggest that frequency, depth and length of flooding associated with soil heterogeneity are playing substantial roles in the spatial structuring of tree species composition and diversity along the igapó forest. However, it would appear that these roles operate differently according to the scale of observation. Thus, at a landscape scale the igapó along the course of the river reveals high floristic heterogeneity where in addition to flooding the geographical position seems to be a major force affecting composition and diversity (Montero et al., in press). At a local scale, it seems that a combination of environmental determinism (mostly governed by flooding and soil) and dispersal-assembly processes (i.e. random dispersal) have the major control over the assemblage of tree communities and may be better predictors of species composition and diversity (Hubbell, 2001; Chave, 2008). Therefore, given that controlling forces are acting at multiple scales and in order to unravel the contribution of flooding and soil, which shape the regional and local floristic patterns, we suggest an analysis of tree species diversity and composition at the scale at which they are more relevant (Stropp et al., 2009).

55 Effect of flooding and soil on igapó

The stretch of the Negro River studied exhibit a strong variation in water-level amplitudes which increases from the upper (short amplitudes) to the lower reach (high amplitudes) of the river. The existence of short amplitudes in the upper reach may probably enhance spatial diversity at the landscape scale, by allowing the colonization of less flood tolerant species which gradually develop adaptations to periodic floods (Wittmann et al., 2010). At the lower reach, on the other hand, the high flood amplitude, long duration and finer soils may increase spatial heterogeneity and consequently diversity of habitats, which can contribute significantly to the regional species pool. However, species diversity could also decrease as flood stress rises.

In this study, our overall aim was to investigate the floristic variation of late- successional igapó forests along environmental gradients across the Negro River. Thus, by monitoring the duration and level of inundation on ca. 4500 individual trees we examined variation of tree species richness, alpha diversity and composition along 600 km long corridor of inundation forests. We also analyzed the variation of soil characteristics and its effects on diversity and composition. Finally, we assessed to what extent spatial separation and environmental factors explain the floristic variation along the course of the river. By investigating three river sections with variable flooding regime, we addressed the following research questions: (a) How do flooding regime and soil characteristics vary along the course of the river? (b) What are the patterns of alpha diversity and tree species composition in relation to the duration and height of flooding between and within river sections? (c) How is the proportional number of common and rare species related to alpha diversity and to what extent does this relationship changes along flooding gradients? and (d) What is the influence of relative importance of soil, flooding and geographic distances in explaining floristic resemblance between river sections?

3.2 Methods

3.2.1 Study area

The course of the Rio Negro

The Rio Negro flows approximately 2500 Km from its headwater at the Colombian side until discharge into the Solimões River (Goulding et al., 2003). More than 80% of the Rio Negro basin is in Brazil, the rest lies in Colombia and Venezuela (Figure 3.1). Within Brazilian territory, the Negro flows approximately 1200 km and receives

56 Effect of flooding and soil on igapó more than 500 small rivers and streams. The major tributary is the Branco River at the lower basin which is a clear water river of intermediate fertility (Junk et al., 2011). The floodplains of the Negro River and its tributaries cover an extension of about 118,000 km2 (Melack & Hess, 2010) and the catchment area covers approximately 600,000 km2 (Latrubesse, 2008). Due to the lack of information the total area of late- successional igapó forests has not yet been estimated. For the study area, however, based upon the Global Land Cover 2000 map (Bartholomé & Belward, 2005) we roughly estimated an area of 2985 km2 covered by late-successional forest. Annual precipitation in the Brazilian part of the Negro basin averages 2000-2.200 mm, with maxima of > 3.000 mm in its upper section. Mean monthly temperatures vary little over the year and range between 25 and 28°C (Sombroek, 2001).

Study sites

We focused on the late-successional inundation forests along the margins of the Negro River within Brazilian territory. The study area spans a stretch of ~ 600 km between Santa Isabel do Rio Negro (upper reach) and the archipelago of Anavilhanas (lower reach) in central Amazonia. Along this stretch we selected three areas (i.e. river sections): (1) downstream of Santa Isabel (ST, upper reach), (2) upstream of Barcelos (BA, middle reach) and (3) at the Anavilhanas archipelago (AN, lower reach), downstream of the town of Novo Airao (Figure 3.1). The upper area (3 sites) had two transects located on the left bank and one on an island in front of the village Serrinha at the mouth of the river Aiuana. At the middle area 2 sites were located on the right bank near the mouth of the Cuiuni River. The lower area was located at the Anavilhanas archipelago with 3 sites located between the mouth of the Igarapé Angelim and the town of Novo Airão. Detailed information of plots location, inhabitants and resources use options along this stretch is given in Montero et al. (in press).

Physical gradients

In the major part of the study area the course of the river drains Tertiary and Quaternary lowlands (Irion et al., 1997). However, at the upper section the presence of remnant isolated hills are reminders of the western extension of the ancient Guiana Shield. In comparison with várzea forests the hydro-morphological organization and dynamic of the floodplain is relatively simple (Junk et al., 2011) and morpho-sedimentary processes suggest rather a stable system. The only exception is at the lower section (i.e. Anavilhanas), which has been greatly affected by an

57 Effect of flooding and soil on igapó increase of land elevation and associated backwater effect of the Solimões-Amazon especially during the early Holocene (Latrubesse & Francinelli, 2005; Irion et al., 2010). In general, the rocks and derived soils of the Rio Negro are acidic and extremely poor in chemicals associated with nutrients (Sioli, 1984). The Negro River transports only 11.5 tons/km2 per year of sediment yield into the Solimões-Amazon system (Latrubesse et al., 2005), which is an insignificant quantity of material considering that this river is the sixth largest river in the world in term of mean annual discharge.

Figure 3.1: The Negro River basin and its trajectory from the Colombian side until the city of Manaus showing the study areas: upper section (Santa Isabel, ST); middle section (Barcelos, BA) and lower section (Anavilhanas, AN) (adapted from Goulding et al., 2003). Inset shows the location of the Negro River in central Amazonia.

Flooding and edaphic gradients

From a hydrological point of view the course of the Negro River displays two main gradients. The first suggests a variation in water-level amplitude which increases from the upper to the lower reach of the river. Thus, mean annual amplitudes vary between 3.6 m in the upper Negro River (Santa Isabel) and 9.2 in the lower section (Manaus), corresponding to an inundation period from 50 to 230 days respectively (Figure 3.2).

58 Effect of flooding and soil on igapó

Figure 3.2: River sections showing study sites projected on satellite images (Landsat 5. WGS - 84) with their respective flood pulse patterns. Hydrograms indicate annual mean water level, minima and maxima values. Mean amplitude increases from Santa Isabel (3,67m) to the Anavilhanas (9,32m) corresponding to an inundation period from 50 to 250 days, respectively. Data source: Agencia Nacional das Aguas (ANA).

In contrast to the lower and middle sections of the Negro River, which show a typical monomodal flood pulse (Junk et al., 1989) with highest water levels occurring during May-August, the upper section experiences bimodal rises governed by ephemeral flood rises where a second, smaller high-water period frequently occurs during February to April.

59 Effect of flooding and soil on igapó

Figure 3.3: Patterns of seasonal fluctuation at the lower and upper Negro River. Arrows at the upper section show the bimodal pattern. Data source: Agencia Nacional das Aguas (ANA).

The second gradient is related to the granulometry and chemistry of sediments along the course of the river. The upper reach (Santa Isabel) consists basically of coarser unfertile material influenced by the western extension of the Guiana Shield. The lower reach (Anavilhanas) has finer sediments of intermediate fertility. Here, the influence of the Branco River transporting finer sediments into the main channel and the backward effect of the Solimões River exert important control and changes in the nutrient status at this section of the river (Junk et al., 2011).

3.2.2 Data collection

Floristic inventories

Field work was carried out between September 2008 and March 2010 during the low- water periods. In the three study areas, we established 128 quadratic 25 x 25 m (625 m2) plots in late-successional igapó forest totaling an area of 8 ha: (1) Santa Isabel (ST, 48 plots), (2) Barcelos (BA, 36 plots) and (3) Anavilhanas (AN, 48 plots). In areas ST and AN we distributed the plots between three sites (i.e., ST1, ST2, ST3),

60 Effect of flooding and soil on igapó while in the BA area plots were distributed between two sites. There were a maximum of 16 plots established per site, corresponding to an area of 1 ha. The upper and lower areas are separated by approximately 600 km, whereas within areas, the sites are separated by a distance of between 5 and 50 km.

All trees ≥ 10 cm diameter at breast height (d.b.h.) were labeled, numbered and dbh measured. Species were identified in the field, and when this was not possible, identified provisionally as morpho-species with voucher specimens collected for later identification at the herbarium of the National Institute for Amazon Research – INPA, Manaus.

Environmental data

Duration and height of inundation

Within each plot inundation height at each tree by using previous year’s water marks on the tree trunks were measured. These measurements are correlated with the daily water-level records at the closest harbor to calculate mean height and period of inundation. Thus, for ST, flooding duration was calculated by relating data of the neighboring water gauge Serrinha (1978-2006) located 20 km east to the city of Santa Isabel. For BA, flooding duration was calculated by relating data of the water gauge at the city of Barcelos (1968-2006), and for AN we used data of the water gauge at Manaus (1903-2006). For each river section we estimated the mean amplitude (cm) while at plot and subplot levels we calculated the mean values of duration of the aquatic phase (days year -1) and flood level (cm). We also estimated for each species the mean duration of flooding (days year -1) and long-term mean maximum height of the inundated part of the trunk.

Soil sampling

In each 1-ha samples at 3 sites were collected from the first 30 cm of topsoil below the litter layer using a bucket auger (plant material was excluded). Samples were air- dried in the field and pooled for each plot. Chemical and granulometry characteristics were determined at the EMBRAPA soil laboratory following the protocol suggested by Silva (1999). The following chemical properties were analyzed: pH, macronutrients (Ca, Mg, K and Na), micronutrients (Fe, Zn and Mn), and concentration of P, N and Al. Concentration of OM (%) and granulometry (% of sand, silt and clay) were also analyzed.

61 Effect of flooding and soil on igapó

3.2.3 Data Analysis

Non-metric multidimensional scaling (NMS) was used to visualize spatial distribution of river section’s tree composition along river gradients (Kruskal, 1964). This ordination method explores the variability in species composition between plots allowing to detected major gradients in the data set (McCune & Grace, 2002). The NMS was carried out with individuals per plot, which were log transformed before running the analysis. The Bray-Curtis dissimilarity distance (Sørensen quantitative) was used to compute the resemblance matrix between plots (Krebs, 1989). To test whether difference in floristic composition between river sections exist, we performed a Multiple Response Permutation Procedure (MRPP, Biondini et al., 1998).

The environment-forest relationship was analyzed by using Pearson product moment correlations to search associations between edaphic variables (chemistry and granulometry) and flooding variables (length and level) with tree community parameters. We firstly derived five tree community parameters which measure or significantly influence species diversity in each plot: (1) abundance (total number of individuals), (2) number of singleton or rare species (represented by only one individual per plot), (3) number of common species (with >10% individuals in plot), (4) species richness (total number of species per plot) and (5) Fisher’s alpha diversity index. The Shapiro-Wilk normality test revealed that no single variable significantly diverted from normal distribution. To correct multiple comparisons we used the Bonferroni correction method.

After preliminary regressions, we detected high correlations between the length and height of inundation as well as between species richness and Fisher´s alpha coefficient (Fisher et al., 1943). Therefore, we removed the height of inundation and species richness. To check how alpha diversity (Fisher´s alpha) relates to the duration of flooding we performed simple linear regressions using Pearson correlations at multiple scale levels. Thus, we measured the strength of the associations using the whole dataset (128 plots), a subset for each river section (ST: 48 plots, BA: 32 plots, AN: 48 plots) and within river section (ST: 3 sites x 16 plots, BA: 2 sites x 16 plots, AN: 3 sites x 16 plots).

To examine tree distribution patterns and to determine differences in species composition and identify species associations along the flooding gradient we used two strategies: (1) Indicator Species Analysis (ISA) was first used to evaluate significant preferences at each river section (Dufrene & Legendre, 1997). The ISA

62 Effect of flooding and soil on igapó combines both abundance and frequency information independently for each species in the dataset, resulting in an indicator value (IV%), which ranges from zero (no indication) to 100 (perfect indication). The species with IV >25% can be considered as a strong indicator of a certain group (Dufrene & Legendre, 1997). A Monte Carlo permutation test with 4999 randomizations was used to test the significance of the indicator value (Dufrene & Legendre, 1997). (2) We generated five flooding tolerance classes spanning the entire flooding gradient. Each class represents the number of days per year (day year -1) tree are subjected to inundation: (1) < 50 days, (2) 50 - 100 days, (3) 100 - 150 days, (4) 150 – 200 days and (5) > 200 days. Species and its respective botanical families were then ranked according to the abundance. Mean and range of flooding length for each species was calculated.

Mantel test was used to evaluate possible spatial autocorrelations between similarity scores and the geographic locations of the plots (Sokal & Rohlf, 1995). Thus, the floristic similarity matrix between 1-ha plots and river sections was calculated using the Chao-Sørensen index (derived from Montero et al. in press), whereas the geographic matrix was generated by calculating geographical distances in kilometers between 1-ha plots. The test basically correlates the two matrices and evaluates the magnitude and direction of relationships between them (Sokal & Rohlf, 1995). The Mantel test is a popular tool when analyzing the relative effects of spatial and environmental factors on tree community assemblages.

Species richness and diversity were computed with the program PAST v. 2.04 “Paleontological Statistics Software Package for Education and Data Analysis” (http://palaeo-electronica.org/2001_1/past/issue1_01.htm) (Hammer et al., 2001). Singleton species were calculated by using EstimateS (Version 8.2, R. K. Colwell, http://purl.oclc.org/estimates). Classes of flooding length were performed in MS Access 2003. Ordination (NMS), ISA, MRPP test and Mantel test were computed using PC-ORD version 5.0 (McCune & Mefford 1999). All statistical analyses (e.g. significance and normality tests) were carried out with SPSS 16.0 and PAST v. 2.04.

63 Effect of flooding and soil on igapó

3.3 Results

3.3.1 Variation of flooding regime and soils along the course of the river

The study area shows a large environmental variation as expressed by the flooding duration and height, soil chemistry and granulometry (Table 3.1, Table 3.2). At the study sites mean annual height vary between 0.70 m at Santa Isabel (ST, upper section) and 2.70 m at Anavilhanas (AN, lower section), which correspond to mean inundation periods of 81 and 173 days year -1 respectively. Thus, considering only the duration of flooding, the AN plots are subjected to 5-6 months of high water each year, whereas plots at ST experiences 2-3 months of inundation yearly. The height of inundation shows more variability along the course of the river. Trees are yearly flooded from ca. 20 cm at Santa Isabel to 420 cm at Anavilhanas (Table 3.1).

Table 3.1: Mean flooding height, duration and respective standard deviation at each river section. The calculations are based on records from Serrinha station n: 25 years; Barcelos station n: 30 years and Manaus n: 104 years. Source: Agencia Nacional das Aguas (ANA). Parameters Santa Isabel (ST) Barcelos (BA) Anavilhanas (AN) ( n: 48) (n: 32) (n: 48) Flooding duration (days year-1) Mean (range) 81 (124 – 40) 132 (147 – 116) 173 (224 – 126) Standard deviation 17.46 8.65 24.33 Height of flooding (cm) Mean (range) 70 (147 – 19) 243 (275 – 217) 273 (416 – 165) Standard deviation 31.30 14.22 64.59 Welch F test detected high significance between the means of river sections P < 0.001 F: 255.5.

The soil characteristics show significant differences between river sections in most of the variables as determined by one-way ANOVA and Welch F test (Table 3.2). The granulometry revealed a remarkable difference in the mean percentage of sand between ST and AN, the latter sites exhibited 15-fold less content than the former. Silt and Clay content, however, are higher at Anavilhanas than in Santa Isabel (Table 3.2)

In terms of soil chemistry, there was no statistically significant differences in the phosphorus content between river sections (P-value = 0.25,Table 3.2). In particular, we found substantial differences in mean values in the content of Ca, Al and organic matter (MO).

64 Effect of flooding and soil on igapó

Table 3.2: Mean and range of soil chemistry variables and granulometry at the eight 1-ha plots along the Negro River. Santa Isabel (ST) Barcelos (BA) Anavilhanas (AN) P-value ( n: 8) (n: 30) (n: 9) (ANOVA*) Soil features Mean (range) Chemistry pH (H20) 4.41 (4.70 – 4.02) 3.99 (4.34 – 3.77) 3.96 (4.14 – 3.79) < 0.001 P (mg kg-1) 7.25 (11.00 – 3.00) 7.00 (13.13 - 4.38) 5.77 (9.00 – 3.00) 0.25 N (%) No data 0.29 (0.49 – 0.13) 0.17 (0.24 – 0.12) < 0.001*

O.M. (%) 2.46 (3.17 – 1.43) 5.31 (8.82 – 2.46) 4.08 (7.41 – 2.06) < 0.001 K (cmol (+) kg-1) 0.11 (0.24 – 0.07) 0.17 (0.25 – 0.13) 0.11 (0.19 – 0.05) < 0.001 Ca (cmol (+) kg-1) 0.13 (0.16 – 0.11) 0.01 (0.03 – 0.00) 0.05 (0.07 – 0.04) < 0.001* Mg (cmol (+) kg-1) 0.07 (0.09 – 0.05) 0.09 (0.11 – 0.07) 0.10 (0.15 – 0.08) 0.006* Al (cmol (+) kg-1) 2.65 (4.34 – 1-16) 7.55 (9.71 – 5.36) 3.75 (4.14 – 3.36) < 0.001* Granulometry Sand (%) 34.66 ( 67.8 – 3.95) No data 2. 61 (4.85 – 1.08) 0.011* Silt (%) 35. 98 (48.30 – 19.17) No data 48.13 (51.09 – 43.82) 0.027* Clay (%) 29.34 (52.70 – 11.70) No data 49.25 (54.75 – 44.05) 0.007* * Homogeneity of variances was not met, and the Welch F test was applied.

3.3.2 Floristic variation between and within river sections

The two dimensional NMS ordination (stress= 0.18) revealed a geographic/ environmental gradient in tree species composition along the axis 2. This axis describes a strict separation between ST and AN river sections. These sections are separated approximately by 500 km in distance and they exhibit contrasting flood pulse patterns, suggesting a geographic or/and flooding gradient. The axis 1 shows a separation between the middle section plots (BA) and AN-ST plots, however, there are some plots of BA which tend to be closer to ST suggesting probably an influence of geographic distance (Figure 3.4).

Figure 3.4: Non-metric multidimensional scaling (NMS) ordination diagram according to Bray- Curtis distance. Dots represent the 128 plots (625 m2 each).

65 Effect of flooding and soil on igapó

A summary of species richness and alpha diversity values standardized at 1-ha for each site at each river section is presented in Table 3.3. Comparing species richness between in the whole dataset the Welch F test shows a statistically significant difference (F= 7.46, P< 0.001). A post-hoc pairwise comparison (Tukey test) detected significant differences between BA plots and AN (P=0.007). Between sites there was also a statistically significant difference as determined by Welch F test (F=7.52, P<0.001). A Tukey post-hoc test revealed highly significant difference between site AN 2 compared to ST 2, BA 1, BA 2 and AN 1 (all with P < 0.001). There were no statistically significant differences between Santa Isabel (ST) and Barcelos (BA) sites (P >0.05).

When, comparing mean values of alpha diversity we found statistically significant differences (Welch test. F=6.28. P < 0.001). However, a Tukey post-hoc test revealed no significance differences between Santa Isabel (ST) and Anavilhanas (AN) communities (P=0.88). Comparing values between sites the Welch F test detected very high significant differences (F= 9.42. P < 0.001). But pairwise comparisons determined by the Tukey post-hoc test revealed that except for ST 1 (P=0.198), the ST 2 and AN 1 sites presented a very significant difference compared with the other sites (P < 0.001). The latter two sites have the highest diversity values averaged per hectare as indicated by the Fisher’s alpha coefficient (Table 3.3). Out of 166 species registered in the dataset the Indicator Species Analysis (ISA) identified 42 species (25%) to have significant preference for one river section (Monte Carlo test, P <0.01). Thus, there are 14, 19 and 9 indicator species for ST, BA and AN, respectively (data not shown). Among indicator species two Lecythidaceae at Santa Isabel such as Gustavia augusta and Eschweilera atropetiolata and two Fabaceae at Anavilhanas, namely Heterostemon mimosoides and Aldina heterophylla stand out. At Barcelos the ISA identified the major number of indicator species (19) with the highest Indicator Value (IV) recorded in the dataset. Here, Duroia sp. (Rubiaceae) presents the highest IV followed by Licania heteromorpha (Chrysobalanaceae) and Mabea caudata (Euphorbiaceae), the latter two families seem to be particular important along the floodplain of the Negro River. Detailed descriptions on how the floristic composition varies along the course of the river and important species and families at each river section are presented in Montero et al. (in press).

66 Effect of flooding and soil on igapó

Table 3.3: Species richness and alpha diversity averaged to 1-ha at the three river sections. Indicator species with the highest IV for each river section are shown. Data on height and duration of inundation are based on three harbors located at Manaus (lower); Barcelos (middle) and Serrinha-Santa Isabel (upper) (Source: Agencia Nacional das Aguas, ANA).

River section Plots Duration of Height of Fisher’s Indicator species and code inundation inundation S index (α) (IV %) plot size (days year-1) (cm)

Upper section Santa Isabel ST 1 90 (70 – 124) 86 (40 – 147) 64 19.43 Hevea brasiliensis (60%) (ST) ST 2 74 (40 – 100) 65 (19 – 110) 67 20.81 Gustavia augusta (59%) 48 x 625 m2 (3 ST 3 78 (71 – 92) 56 (33 – 95) 60 16.88 Eschweilera atropetiolata (54%) ha)

Middle section Duroia sp. (81%) Barcelos (BA) BA 1 131 (116 – 147) 242 (217 - 242) 68 18.41 Licania heteromorpha (79%) 32 x 625 m2 (2 BA 2 133 (116 – 147) 244 (218 – 273) 57 13.99 Mabea caudata (78%) ha)

Lower section Anavilhanas AN 1 186 (146 – 198) 308 (209 – 345) 79 27.24 Heterostemon mimosoides (69%) (AN) AN 2 186 (157 – 224) 307 (222 – 416) 51 15.54 Eschweilera aff. amazoniciformis (67%) 48 x 625 m2 (3 AN 3 146 (126 – 165) 202 (165 – 243) 63 18.99 Aldina heterophylla (59%) ha)

S is the total number of species registered per site. α is Fisher’s index of diversity defined by S= α *ln(1+n/ α). Indicator species were obtained at the river section level. IV represents indicator value, which ranges from zero (no indication) to 100 (perfect indication). The species with IV >25% can be considered as a strong indicator of a certain group.

3.3.3 Environment in relation to tree community parameters

The Pearson product-moment correlation tests revealed a number of significant associations mostly between flooding and soil features and between these two environmental variables and abundance (all at significance levels of P< 0.01, Table 3.4). The tree community parameters (singleton and common species, richness and Fisher’s alpha) were not significantly correlated with flooding. However, organic material (OM) was negatively correlated with species richness (r= - 0.25, P< 0.05). Notably, rare species (singleton) were not significantly associated with any edaphic variable, but common species was weakly and positively correlated with concentration of Aluminum (r=0.21, P< 0.05). Surprisingly, comparing the granulometry and tree community parameters between upper (Santa Isabel) and lower (Anavilhanas) sections, Pearson correlations revealed weak associations. Common species were significantly correlated (P< 0.05) with the content of sand (r= - 0.21) and clay (r= 0.25). Species richness negatively correlated with the content of clay (r= - 0.23, P< 0.05).

67 Effect of flooding and soil on igapó

Table 3.4 Summary of Pearson correlations between environmental variables (soil chemistry, granulometry and flooding) and five community parameters describing tree diversity (species richness and Fisher’s alpha) and horizontal structure (abundance, singleton species and common species) Flooding Flooding Species Singleton Common Parameters duration Abundance Fisher’s alpha height (cm) richness species species (days/year) Flooding height 1.00 Flooding duration 0.964** 1.00 Abundance - 0.439** - 0.425** 1.00 Species richness - 0.120 - 0.150 - 0.542** 1.00 Singleton species 0.025 - 0.016 0.230* 0.867** 1.00 Common species 0.045 0.075 - 0.198 - -0.504** 1.00 0.496** Fisher´s alpha 0.181 0.119 - 0.037 0.660** 0.852** - 0.443** 1.00 pH (H20) - 0.880** - 0.901** 0.331** 0.166 0.086 - 0.149 - 0.063

O.M. (%) 0.808** 0.802** - 0.436** - 0.259* -0.163 0.191 - 0.029 K (cmol (+) kg-1) 0.289** 0.272** - 0.215* 0.034 - 0.046 0.106 0.143 Ca (cmol (+) kg-1) - 0.854** - 0.865** 0.300** 0.142 - 0.018 - 0.013 - 0.089 Mg (cmol (+) kg-1) 0.907** 0.904** -0.389** - 0.170 - 0.072 0.087 0.085 Al (cmol (+) kg-1) 0.654** 0.682** - 0.264** - 0.124 - 0.105 0.216* 0.042 Sand (%) - 0.739** - 0.767** 0.302** 0.166 0.107 - 0.211* - 0.023 Silt (%) 0.694** 0.726** - 0.230* - 0.093 - 0.063 0.163 0.079 Clay (%) 0.755** 0.779** - 0.355** - 0.237* - 0.156 0.252* - 0.042 Two-tailed significance levels of correlation coefficients are marked with asterisks * P < 0.05, ** P < 0.01,

3.3.4 Rarity and commonness in response to the flooding gradient

The Figure 3.5 shows the distribution of rare species (singleton), common species (>10% of total individuals), abundance and Fisher’s alpha coefficient distributed along the flooding gradient. We found a positive correlation between abundance and duration of flooding at intermediate flooded sites (i.e. BA plots) which was highly significant (r= 0.52. P> 0.002), whereas alpha diversity (Fisher’s coefficient) presented a negative association with flooding duration (r= - 0.38. P= 0.03). In fact, at BA values averaged to 1-ha show the lowest alpha diversity and the highest tree density (Table 3.3).

68 Effect of flooding and soil on igapó

80

Abundance 70 Singleton species

Common species 60

Fisher´s alpha coefficient

50

40

30

20 Number of species/individualsNumber

10

0 0 50 100 150 200 250 Flooding duration (days/year)

Figure 3.5: Distribution of singleton species (only one individual per plot) common (species with > 10% of individuals in plot), fisher’s alpha and abundance along the duration of flooding (days/year).

The number of singleton species strongly correlated with fisher’s alpha coefficient (r= 0.82. P<0.001), indicating that alpha diversity along the course of the Negro River may be in function of rare species (Figure 3.6). The number of common species, however, was negatively correlated with flooding, although the strength of the associations was very weak and no significance was detected (all flooding gradient P > 0.70). There was a weak negative correlation between rare species (singleton) and duration of flooding detected at the less flooded sites (i.e. ST plots), which was not statistically significant (r = - 0.23. P= 0.11).

20 r = 0.82, P< 0.001, n=128 18 16 14 Figure 3.6: The 12 relationship 10 between alpha 8 diversity and 6 number of

Singleton species Singleton 4 singleton 2 species (rare 0 species). 0 5 10 15 20 25 30 35 40 45 Fisher´s alpha coefficient

3.3.5 Diversity patterns along flooding gradients

Pearson correlations determined strong positive associations between species richness and fisher’s alpha diversity index (r=0.66. n=128) and between duration and

69 Effect of flooding and soil on igapó height of inundation (r=0.96. n=128). In both cases, the correlations were statistically significant (P<0.001, Figure 3.7). Consequently, from now on we use flooding duration (days year -1) as the predictive variable and Fisher’s alpha coefficient (α) as the response variable. The former exert a more decisive influence in structuring tree communities while the latter additionally to the number of species considers number of individuals at each plot.

45 r=0.66, P<0.001, n=128 40 35 30 25 ha coefficient

p 20 15 10 Figure 3.7: Person’s 5 correlations between (a) Fisher´s al Fisher´s 0 fisher’s alpha index and 0 5 10 15 20 25 30 species richness and (b) duration and height of Spe cie s ri chne ss inundation. Floristic data are derived from 128 2 (a) plots of 625m each at Santa Isabel (n=48). 250 r= 0.96, P<0.001, n=128 Barcelos (n=32) and Anavilhanas (n=48). ) s y 200 Mean height and da

( duration of flooding at each plot have been 150 calculated from Table 3.1.

duration duration 100 g 50 Floodin 0 0.00 0.50 1.00 1.50 2.00 2.50 3.00 3.50 4.00 4.50 Flooding height (m)

(b)

When examining all data combined we found a weak positive correlation between Fisher’s alpha diversity and duration of inundation, but this association is not statistically significant (r = 0.11. n = 128. P = 0.28). This result indicates that along the entire flooding gradient there is a slight trend to increase diversity and (species richness) while increasing the duration of flooding (Figure 3.8a). At river sections level, however, the results suggest different correlation patterns. The ST (mean 81 days year -1) and BA (mean 132 days year -1) river sections show weak negative correlations of duration of flooding with fisher’s alpha (ST: r= - 0.14, P=0.32; BA: r= -

70 Effect of flooding and soil on igapó

0.37. P=0.034) while Anavilhanas (AN mean 173 days year -1) duration of flooding and fisher’s alpha are positively correlated (r= 0.32. P=0.027) (Figure 3.8b).

45 40 r = 0.11, P=0.21, n=128 35 30 25 ha coefficient

p 20 15 10 5 Fisher´s al Fisher´s 0 0 50 100 150 200 250 Flooding duration (days/ year)

Figure 3.8: Relation (a) between Fisher’s alpha and flooding duration (a) combining all dataset and 45 (b) at each river section. 40 35 30 Barcelos (BA, n=32) r = - 0.37, P=0.034 25 ha coefficient

p 20 15 Santa Isabel (ST, n=48) 10 Anavilhanas (AN, n=48) r = - 0.14, P=0.32 5 r = 0.32, P=0.027 Fisher´s al Fisher´s 0 0 50 100 150 200 250 Flooding duration (days/year)

(b)

A comparison between river sections confirms the trend of increasing diversity while increasing the duration of flooding at the lower section. Thus, at Anavilhanas (AN) we calculated the highest alpha diversity (α= 38.17) but also the lowest alpha diversity (α= 3.32) at the plot level. This variation may be explained by the facts that the AN plots are distributed over a larger flooding gradient. Although weakly correlated, our results at Barcelos (BA) and Santa Isabel (ST) indicate a decrease of alpha diversity with increasing duration of inundation. This pattern was statistically significant at BA (P=0.034), while at ST the correlation coefficient was not significant (P=0.32). In general, along the entire flooding gradient (24 to 224 days year -1) the AN (lower Negro River) and Santa Isabel (upper Negro River) plots exhibit the highest values of alpha diversity.

71 Effect of flooding and soil on igapó

35

30 ST3 25 ST2 ST1 20

15

10

5 Fisher´s alphacoefficient 0 0 20 40 60 80 100 120 140 Flooding duration (days/year) a)

25 BA2 20 BA1

15 Figure 3.9: Relation 10 between Fisher’s alpha coefficient and 5 flooding duration

Fisher´s alphacoefficient between 1-ha plots at 0 (a) ST, (b) BA and (c) 100 120 140 160 AN Flooding duration (days/year) b)

45 40 AN2 35 AN3 30 AN1 25 20 15 10 5 Fisher´s alphacoefficient Fisher´s 0 0 20 40 60 80 100 120 140 160 180 200 220 240 Flooding duration (days/year) c) A further comparison between at 1-ha scale revealed no significant difference in the duration of flooding between BA 1 and BA 2 (P=0.57), suggesting that these sites occupy a smaller flooding range (Figure 3.9b). Similar pattern is observed at ST, in which plots are overlapped along the flooding gradient. However, the duration of flooding at AN plots show rather very significant differences (AN: P<0.001, except AN1 vs AN2). Thus, for example AN 1 occupies a small flooding gradient ranging from 180-200 days and AN 3 likewise, occupies a range that varies 125 – 165 days with few overlapping plots between them (Figure 3.9c). This may suggest that we sampled a greater number of different habitats at Anavilhanas.

72 Effect of flooding and soil on igapó

3.3.6 Relation between spatial scale and floristic similarity

The Mantel test indicated a negative association between geographic distance and floristic similarity. Both the asymptotic approximation method (r = - 0.590 P < 0.001) and randomization method (Monte Carlo test, 999 permutations, r= - 0.590, P= 0.003) indicate that the association is highly significant. The observed correlation, therefore, suggests that the matrix entries are negatively associated where floristic distance (Chao-Sørensen index) decrease with increasing geographic separation. Thus, the data show highest floristic similarity within river sections, while similarity decreases between river sections. However, inter-site similarities (e.g. AN 3 vs ST 1, AN 2 vs ST 3) are higher than BA in relation to AN and ST plots, despite being more closer between them (Figure 3.10).

1 Figure 3.10: Similarity r = - 0.59, P< 0.005 0.8 of sampling sites as a function of distance 0.6 represented in kilometers between 1- 0.4 ha plots. Inter- similarity matrix is Inter-site sim ilarity 0.2

(Chao-Sørensen index) (Chao-Sørensen based on Chao- 0 Sorensen index and is 0 100 200 300 400 500 600 derived from Montero Distance (km) et al. (in press).

3.3.7 Tree composition according to flood tolerance

The species composition in relation to inundation classes suggests a distinct variation in the distribution of tree species along a flooding gradient (Table 3.5). Lecythidaceae and Fabaceae are the most dominant families being present at each inundation class. Among the top five most abundant species at each inundation classes none occurs along the entire flood gradient. Our data, however, indicate the presence of few generalist species such as Gustavia augusta and Heterostemon mimosoides; the former was only absent in the intermediate flooded class (100-150 days year -1), while the latter was absent in the less flooded class (up to 50 days year -1). These two species are the most abundant in the entire data set.

73 Effect of flooding and soil on igapó

Table 3.5: Tree species composition according to flooding tolerance classes. The duration of flooding is presented in days per year. Mean, maximum, minimum and standard deviation values are provided for each species. Total number of species, families and number of individuals per classes are highlighted in bold. Duration of flooding (days Classes Species Family N year-1) max mean min sd Gustavia augusta L. Lecythidaceae 30 40 29.53 18 9.77 Crudia amazonica Spruce ex Benth. Fabaceae 9 40 31.11 18 11.01 Up to 50 days/ Unonopsis guatterioides R.E. Fr. Annonaceae 8 35 24.37 18 8.79 year Mollia lepidota Spruce ex Benth. Malvaceae 7 40 23.57 18 9.62 Gustavia sp. Lecythidaceae 7 40 31.57 18 9.53 Σ 47 Σ 20 Σ 137 Gustavia augusta L. Lecythidaceae 230 100 79.21 68 7.80 Hevea brasiliensis (Willd. ex A. Juss.) Euphorbiaceae 127 100 82.01 68 9.01 Müll. Arg. 50 – 100 Eschweilera atropetiolata S.A. Mori Lecythidaceae 108 100 80.64 70 8.07 days/year Licania micrantha Miq. Chrysobalanaceae 50 100 83.18 68 9.84 Mollia lepidota Spruce ex Benth. Malvaceae 37 100 81.67 70 7.98 Σ 101 Σ 32 Σ 1275 Duroia sp. Rubiaceae 210 145 136.03 114 7.31 Mabea caudata Pax & K. Hoffm. Euphorbiaceae 193 145 133.35 103 8.63 100 - 150 Heterostemon mimosoides Desf. Fabaceae 133 147 133.88 102 10.45 days/year Licania heteromorpha Benth. Chrysobalanaceae 113 145 130.78 102 8.92 Virola calophylla (Spruce) Warb. Myristicaceae 97 147 126.38 102 9.50 Σ 126 Σ 34 Σ 1966 Heterostemon mimosoides Desf. Fabaceae 173 200 174.63 153 15.60 Eschweilera aff. amazoniciformis S.A. Lecythidaceae 90 200 180.54 153 13.03 Mori 150 - 200 Aldina heterophylla Spruce ex Benth. Fabaceae 82 200 181.91 153 13.17 days/year Gustavia augusta L. Lecythidaceae 54 200 178.87 156 11.90 Tachigali venusta Dwyer Fabaceae 29 197 177.86 153 13.22 Σ 109 Σ 33 Σ 1035 Eschweilera aff. amazoniciformis S.A. Lecythidaceae 12 232 221.08 209 7.82 Mori Heterostemon mimosoides Desf. Fabaceae 10 222 215.00 209 5.55 > 200 days/ Aldina heterophylla Spruce ex Benth. Fabaceae 8 229 216.87 208 8.46 year Swartzia macrocarpa Spruce ex Benth. Fabaceae 5 232 225.40 214 6.84 Mollia speciosa Mart. Malvaceae 4 237 221.75 214 10.34 Σ 27 Σ 15 Σ 72

When comparing class 1 (flooded up to 50 days year -1) with class 5 (flooded > 200 days year -1) we found two interesting patterns. At the class 1 no species zonation was observed, rather we identified several species and genera which are widely distributed across terra firme forest. For example: Dialium guianense, Pseudolmedia aff. laevigata and the genera Toulicia, Roucheria, Lindackeria and Diplothropis (data not shown). In the highly flooded class, on the other hand, most species belong to

74 Effect of flooding and soil on igapó few families, and species zonation is more evident. Good examples are Aldina heterophylla, Eschweilera aff. amazoniciformis and Swartzia macrocarpa which are able to tolerate up to 230 days of inundation each year.

The total species richness and tree density show their highest values at the intermediate duration of flooding (class 3: 100 – 150 days year -1). Within this class 1966 individuals belong to 126 species, which represent 44% and 76% of the total dataset, respectively are inundated up to 150 days each year. As flooding tolerance classes reaches its opposite ends total values of species richness and abundance decrease. Thus, at the class 1 there were 47 species and 137 individuals inundated less than 50 days year -1, in which the top most abundant tolerate a mean value of approximately 1 month. Interestingly, more than 50% of the species at this class are singletons with only one individual per class. In the class 5 we estimated 27 species and 72 individuals subjected to long lasting flooding periods of approximately 7 months each year.

3.4 Discussion

3.4.1 Environmental heterogeneity along the course of the Negro River

Few studies have documented the variation of the flooding regime and soil characteristics of the Negro River (but see Goulding, 1988). Excepting the lower section of the river (e.g. Worbes, 1997; Ferreira, 1997) to our knowledge no study has related abiotic factors with tree composition and diversity on late-successional forests along the course of the Negro River. Recently, Junk et al. (2011) have argued that the influence of the Branco River transporting finer sediments into the main channel give rise to changes in soil fertility determining an edaphic gradient. Thus, below the Branco River confluence (i.e. Anavilhanas) the igapó is of intermediate fertility and may share more species with várzea, while at the infertile middle and upper sections the igapó forest has a distinct floristic composition. These authors further reported that flood amplitudes along the Negro River decrease from 4 m at the upper section to 10 m at the confluence with the Solimões River, the latter represent one of the highest amplitudes across the Amazon basin. According to Irion et al. (2010) the lower section of the Negro River (i.e. Anavilhanas) has been substantially affected by Pleistocene sea level changes which increased the floodplain areas and contributed to the current status of soil quality. Indeed, the mouth of the Negro River is considered as a large Ria Lake (discharge area) that has

75 Effect of flooding and soil on igapó not yet been filled in with sediments after the last sea-level low stand (Irion et al., 2010). In the upper sections, however, most stable morphodynamics equilibrium conditions have been achieved where an anabranching channel and erosional– relictic island system relatively efficiently convey water and sediment (Latrubesse & Franzinelli, 2005).

Our texture soil data confirm a higher content of finer sediments at the lower section. The content of silt and clay significantly increased at Anavilhanas (AN) while the content of sand presents the highest value at Santa Isabel (ST). Despite highly significant differences between soil chemistry of river sections, we observed that at Anavilhanas only Mg and OM increased significantly while pH decreased. The flood pulse pattern in most of the river is monomodal, long and predictable. However, the upper section (Santa Isabel) exhibits unpredictable floods subjecting trees to shorter flooding duration and therefore less stress. In this river section, both overflow magnitude and rates of change are controlled by stochastic flood events.

Consequently, considering marked environmental heterogeneity associated with large spatial separation between river sections, we expected to have significant effects of environment and space on tree species composition and diversity. Instead, we did not find significant differences in alpha diversity between lower (i.e. AN) and upper sections (i.e. ST) and floristic similarity between these two regions was rather high. The distinct flora at the upper sections suggested by Junk et al. (2011) and other authors (Kubitzki, 1989; de Oliveira, 2001) may be attributed to the occurrence of few endemic species. However, the floristic composition of the late-successional stage at Santa Isabel does not support a marked floristic distinctiveness between upper and lower sections.

3.4.2 Diversity patterns along flooding gradients

A number of studies on Amazonian floodplain forests have documented the extent to which flooding regime affects species diversity of trees >10 cm d.b.h. These studies, however, considered mostly forest communities of different successional stages, habitats and topographical levels. Thus, it has been reported a significant increase of tree species richness and alpha diversity with decreasing height and duration of flooding (igapó: Ferreira, 1997; Worbes, 1997; Ferreira & Stohlgren, 1999; Inuma, 2006; várzea: Campbell et al., 1992; Ayres, 1993; Wittmann et al., 2006). These authors have concluded that tree species richness and diversity are highly dependent on flooding regime, in which the level of flooding tolerance may be a condition for

76 Effect of flooding and soil on igapó species to be successful in floodplain forests. However, comparing river sections, our results do not support these findings. We interpreted the flooding-diversity relationship as directional responses of trees to variation in the duration of flooding. Thus, as duration of flooding decreases towards the upper section of the river (Santa Isabel, 81 (124-40) days year -1) we expected a more or less linear increase of species diversity. Instead, we found a slight trend to increase diversity at the lower section (Anavilhanas, 173 (224-126) days year -1).

Within river sections alpha diversity at AN positively correlated with duration of flooding, confirming the highest diversity in the lower section. However, data at BA (significant association) and ST (weak and no significant association) support the general pattern reported by other studies that diversity tends to decrease as the duration of flooding increases. Thus, at Anavilhanas we estimated a Fisher’s alpha coefficient of 20.60, while the less diverse site (Barcelos) presented an alpha value of 16.20. These alpha diversity values are below average diversity estimated for várzea forest, placing the igapó as one of the poorest inundation forests across the Amazon (Montero et al., in press). When comparing 1-ha plots within river sections, we observed that sites with similar duration of flooding had significant differences in alpha diversity, especially at AN. For instance, identical mean duration of flooding at AN 1 and AN 2 (186 days year -1) resulted in 27.24 and 15.54 fisher’s alpha coefficients, respectively. Although less clear, similar patterns at ST and BA were detected, being the most remarkable at BA sites. Here almost similar mean duration of flooding for BA 1 (131 days year -1) and BA 2 (133 days year -1) resulted in 18.41 and 13.99 fisher’s alpha coefficients, respectively. The above listed results suggest a multi-scale effect of flooding on diversity, which may be related to other abiotic factors such as soils and hydro-geomorphologic heterogeneity.

It has been proposed that diversity may be higher in headwaters due to geographic isolation which favors speciation, while downstream species diversity decrease as flood stress rises (Junk, 2005). Although one site at Santa Isabel presented high alpha diversity, overall we found highest diversity at the lower section of the river (i.e. Anavilhanas). This may be partially explained by the homogenization effect of floods (river connectivity) and river confluences effects (Thomaz et al., 2007; Osawa, 2010). The former enhances the exchange of sediments and organisms between different habitats, while the latter suggest abrupt changes of volume and water chemistry at down-confluence areas (Benda et al. 2004; Junk et al. 2011). A long-lasting connectivity associated with hydro-ecological dynamics may promote the

77 Effect of flooding and soil on igapó arrangement of a complex network of habitats, consequently increasing alpha diversity. Therefore, the observed highest diversity at Anavilhanas may be explained by a biogeochemical gradient due to influence of the Branco River transporting finer sediments and the backwater effects of the Solimões River, which has been very intense in the late Pleistocene and Holocene (Rosales et al., 2001; Latrubesse & Franzinelli, 2005).

The comparative low alpha diversity presented at Barcelos and the trend of increasing alpha diversity towards less flooded (Santa Isabel) and more flooded sites (Anavilhanas) may be partially explained by the spatial distribution of plots in relation of the flooding gradient within each river section. The 1-ha plots BA 1 and BA 2 merge into a spatially homogeneous cluster of subplots, which apparently respond to the flooding gradient equally. On the other hand, most of the plots in ST and especially in AN respond to a specific range along the entire flooding gradient, indicating a greater diversity of habitats sampled. Thus, AN 1 occupies a small flooding gradient ranging from 180-200 days and AN 3 likewise, occupies a range that varies 125 – 165 days per year.

3.4.3 Rarity and commonness

It has been suggested that higher species richness and alpha diversity could be due to the relative increase in the proportion of rare species (Rosenzweig, 1995; Pitman et al., 2002; Laurance et al., 2010; Davidar et al., 2005). We found that Fisher’s alpha coefficient increased significantly with rarity (singleton species), confirming that the alpha diversity along the Negro River may be in function of the proportional number of rare species as expected. In contrast to the common pattern in which alpha diversity is in function of tree density (ter Steege et al., 2003) our results show that the number of individuals (abundance) does not significantly influence Fisher’s alpha diversity. This pattern is more significant in the middle section (BA), where we recorded the highest abundance (808 individuals ha -1) but also the lower Fisher’s alpha coefficient (α = 13.99, summarized in Montero et al., in press).

Although weakly associated the common species peaked on sites with the highest concentration of aluminum and abruptly decreased in sites with the highest concentration of coarser sediments. This finding is in line with Pitman et al. (2002) who found only weak associations between edaphic variables and the most common “oligarchies” species registered in western Amazonia. The number of rare species did not show significant associations with any of environmental variables, suggesting

78 Effect of flooding and soil on igapó that perhaps random dynamics or dispersal limitation are playing a major role with the distribution of these species (Hubbell, 2001).

Nevertheless, at river section level we detected an increase of the number of rare species with decreasing duration of flooding at the upper Negro River. This may be explained by the flood pulse pattern at this river section, which is characterized by short, unpredictable and ephemeral inundations giving thus the conditions for the establishment of terra firme species (Wittmann & Junk, 2003), which are “in transit” to either become adapted to floodplain areas or go extinct. According to Wittmann et al., 2010, the gradual adaptation to the new environment and the creation of effective competitive mechanisms lead to a stage in which species reach a “point of no return” that is, they are no longer competitive in non-flooded environments and therefore, become endemic to the floodplains. An evidence for the previous arguments is that we recorded many genera and species that are widely abundant in terra firme forest and were not registered in the other river sections.

3.4.4 Tree composition along flooding gradients

The effect of flooding duration is an important driver of species composition in floodplain forests and plays a key role in determining characteristic species associations and plant communities (Hueck, 1966; Junk, 1989; Ayres, 1993). Low- lying tree communities are affected by long, predictable and monomodal flood pulse, while highest levels are affected by flood pulses of short duration and low amplitude (Junk et al., 2011). Thus, on várzea floristic composition along flooding level gradient is clearly marked by different plant communities which represent a successional sequence from pioneer to climax stages (Junk, 1989; Campbell et al., 1992). At low lying sites exposed to ca. 300 days year -1 occur stand of shrubs communities, while the tree line coincides with an average of 230 days year -1 (Junk, 1989; Worbes et al., 1992; Worbes, 1997). Besides flooding gradient, on the lower Negro River, Worbes (1997) distinguished tree species composition along gradual plant communities according to clayish and sandy soils. On clay soils, this author further differentiated between low level communities (> 150 days year -1), mid level communities (> 75 < 150 days year -1) and high level communities (< 90 days year -1).

Our analysis significantly differentiated three main groups of tree communities representing the river sections, indicating a marked difference in floristic composition. However, the interpretation of species zonation may be difficult since each river section exhibits different flood amplitudes and in addition, we sampled at similar

79 Effect of flooding and soil on igapó topographic level making difficult the detection of species zonation within river sections.

Despite this restriction, we detected significant preferences of certain species to different river sections and flooding tolerance classes. The Indicator Species Analysis (ISA) identified 14 indicator species at Santa Isabel (e.g. Gustavia augusta IV: 60%), 19 species at Barcelos (e.g. Duroia sp. IV: 81%) and 9 species at Anavilhanas (e.g. Heterostemon mimosoides IV: 69%). The lowest number of indicators species computed in the latter region may be explained by the comparatively larger flooding gradient at this river section. The larger the range of the flooding gradient, the greater the diversity of habitats, therefore, few species may exhibit a significant preference for this river section. Opposite pattern is observed at Barcelos where we recorded the highest number of indicator species.

The floristic composition in relation to flooding tolerance classes revealed that no single species occurred along the entire flood gradient. This may be explained by the fact that most species are restricted to specific topographic levels and flood amplitudes (see Wittmann et al., 2010; Ferreira et al., 2011). Thus, at highest flooding tolerance classes (>150 days year -1) three species are particular abundant namely Heterostemon mimosoides, Escheweilera aff. amazoniciformis and Aldina heterophylla, whereas at the less flooded classes (< 100 days year -1) Gustavia augusta and Mollia lepidota are dominant species. At the intermediate flooding class ( > 100 < 150 days year -1) we found an even more restricted species distribution pattern, in which the top two most abundant species are exclusively present at this class (Duroia sp. and Mabea caudata). At the family level, Lecythidaceae and Fabaceae are dominant and widely distributed along the entire flooding classes, with the exception of the intermediate class where Rubiaceae, Euhphorbiaceae and Chrysobalaneae stand out.

With the exception of Heterostemon mimosoides, Aldina heterophylla and Eschweilera atropetiolata, which have a distribution restricted to the Negro River basin, the indicator species showed at each river section and the most abundant in each flooding tolerance classes are widely distributed on floodable and terra firme habitats across the Amazon and Orinoco basins (Montero et al., in press). This may be partially in line with Wittmann et al., (2006) who found that despite high disturbance and fine scale geomorphological heterogeneity várzea forests are dominated by a high proportion of generalist species widely distributed.

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3.4.5 On the effects of geographic distance and environmental (dis)similarity

In Manu’s National Park Terborgh et al. (1996) found that mature várzea forests tend to converge in tree species composition, despite considerable distances between sampled sites and interpreted this as evidence that random dynamics with dispersal limitation are not the major forces determining species composition. Along the várzea of the Solimões-Amazon River Albernaz et al. (2011) found mixed effects of environment and space on overall floristic variation, however, the authors identified that spatial effect alone had a greater influence on species composition. In agreement with some studies (Potts et al., 2002; Vormisto et al., 2004) we found that within river sections floristic similarities between 1-ha plots increases with decreasing geographic distance as expected.

Intriguingly, we also found higher floristic similarity (> 50%) between upper (ST) and lower (AN) plots, which are located ca. 500 km away than these two in relation with plots at BA located at the middle section. In addition, there is no significant difference in alpha diversity between AN (α= 20.59) and ST (α= 19.04). The contrasting flood pulse and geographic distance between the upper and lower plots make it difficult to discuss possible causes of the observed high floristic resemblance between these two regions. However, we have noted that the Barcelos sites show a particular floristic composition mostly dominated by a suite of few species that only occurred in these plots. Furthermore, Montero et al. (in press) found extremely high beta diversity (length of gradient > 4 s.d.) at this river section. These insights may indicate that probably the Barcelos sites may be influenced by a particular fluvial morphology or landform which substantially stands out from the other river sections.

We therefore conclude that at regional scale geographical position and the influence of surrounding forest types are stronger predictors of floristic composition (Kubitzki, 1989; Terborgh & Andresen, 1998; Montero et al., in press), while at local scale a mixed effect of flooding and spatial variation seems to play a key role in determining tree composition. However, as emphasized by Chase (2007) the relative importance of environmental filtering versus stochastic variations depends on the severity (i.e. stress) of the environmental filter operating in local habitats. At this scale, thus, the duration of flooding may act as a filter of species assembly and community composition, preventing the colonization of species from the regional pool that are unable to tolerate long lasting flooding periods in the local habitat, thus resulting in a more deterministic community structure. When various species have the same

81 Effect of flooding and soil on igapó pattern of geographic distribution, it is unlikely that it is due to their biology, the influence of geographic barriers or the effect of extreme harsh environments for long term periods influenced speciation (Morell, 1996).

3.5 Conclusion

This study contributes insights on how tree alpha diversity and composition respond to the duration of flooding along the course of the Negro River. The results and discussions are a first attempt to explain the forest-environment relationship along a 600 km long corridor of inundation forest and contribute to current scientific discussion about factors shaping diversity and composition across the Amazon region.

At landscape-scale (i.e. between river sections) we detected a slight trend to increase alpha diversity at the lower sections where the duration of flooding and the percentage of finer sediments (silt and clay) significantly increased. Surprisingly, we found the highest floristic similarity between upper (ST) and lower (AN) plots, which are located ca. 500 km away than these two in relation with plots at BA located at the middle section. The latter sites are composed by a suite of few dominant species which are not present in the other river sections. This pattern indicates that other predictors (e.g. fluvial geomorphology) seem to control tree assemblages at this river section and underlines the patchy arrangement of the Negro River channel.

In contrast to other studies and what we expected, the existence of an unpredictable and short flood pulse pattern in Santa Isabel (upper Negro River) does not significantly increase alpha diversity. Instead, the short duration and unpredictability seems to influence the presence of a highest number of singleton species (i.e. rare species), which are less tolerant to long periods of flooding. These species, likewise, are widely distributed on terra firme forest and they do not occur in the other river sections.

At more restricted scales (i.e. within river sections and flooding classes) the results show more clear patterns of the effect of flooding on species diversity and tree composition. Our data confirm that Anavilhanas present the highest alpha diversity per unit area and this may be caused by a major diversity of sampled habitats. This spatial heterogeneity increases diversity by creating patches of different serial stages, containing different functional groups. With the exception of Heterostemon mimosoides, Aldina heterophylla and Eschweilera atropetiolata which are restricted

82 Effect of flooding and soil on igapó to the Negro River basin, most top dominant species presented in the flooding tolerance classes are widely distributed in várzea and terra firme forests. Fabaceae and Lecthidaceae are present along the entire flooding gradient.

In contrast to many studies across the Amazon, our results suggest that at landscape scale when the sampled environmental gradient is long (as our study area) the only use of environmental variables tend to be a poor predictor of species richness and alpha diversity. This may explain why we found little variation in alpha diversity along the course of the river and may lead to believe that mixed effects of geographical position of the plots, ecological filtering and stochastic processes are acting at different scales. At local scale it seems that there are deterministic patterns in the species richness and alpha diversity. However, compositional patterns such as which species or families make-up a tree community are to a large extent deterministic and predictable in function of the severity of the environmental filter; whereas, how common the species are and how they are assembled together into different communities may be predicted by stochastic forces.

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4

THE IGAPO OF THE NEGRO RIVER IN CENTRAL AMAZONIA: LINKING LATE-SUCCESSIONAL INUNDATION FOREST WITH FLUVIAL GEOMORPHOLOGY

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4 The igapó of the Negro River in central Amazonia: Linking late-successional inundation forest with fluvial geomorphology

4.1 Introduction

In central Amazonia the prevailing floodplain forest is differentiated into nutrient-rich white-water “várzea” and nutrient-poor black water or clear water “igapó” (Prance, 1979). These forests are mostly affected by long and predictable flood pulse subjecting trees to extended inundation periods of up 8 months and to flooding amplitudes of 10 m or more (Junk, 1989). This dynamic imposes a strong impact on plant assemblages whose species composition and structural patterns are continuously changing along the river channel (Rosales et al., 2001; Wittmann et al., 2004; Albernaz et al., 2011; Montero et al., in press).

Most white-water rivers have their catchment area in the Andes and are loaded with nutrient-rich sediments. Várzea floodplain covers approximately 300.000 km2 from which only about 30% of this area is covered by forest (Junk & Furch, 1993).The Solimões-Amazon, Purus, Madeira and Madre de Dios are some examples of white- water rivers. In contrast, black-water and clear-water Rivers carry low loads of suspended matter and solutes, resulting in a scarcity of nutrients. Igapó forests mostly occur along black and clear water rivers that drain the Paleozoic and/or Precambric shields of Guyana and Central Brazil. The floodplain of these rivers could cover about 100,000 km2 but due to the lack of precise information, the area covered by igapó forest has not yet been estimated. Examples of clear-water Rivers are the Tapajós and Xingú while the main example of black-water River is the Negro River, which form the largest black-water inundation forest in the world (Montero, 2011).

Physiognomically and floristically the igapó display substantial differences from várzea (Prance, 1989). The vertical structure of the igapó is shorter and less stratified than its white-water counterpart. The canopy height averages about 15-20 m with few emergent trees up to 30 meters. Woody lianas and palms are almost absent. Analysis of growth behaviour has found that tree ages of species for more or less the same diameter are more than twofold higher in the igapó (maximum age >500 years) than in várzea (maximum age < 200 years) (Schöngart et al., 2005; Fonseca-Junior et al., 2009). In terms of tree species richness, the igapó of the Rio Negro with an average of 63 sp ha-1 is one of the poorest forest types in the Amazon and comparable with várzea (142 sp ha-1) is by far the poorest inundation forests in the

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Amazon. In terms of tree composition, Aldina heterophylla, Heterosthemon mimosoides and Eschweilera atropetiolata are dominant species and particularly restricted to the Negro basin. The Chrysobalanaceae, Lecythidaceae and Euphorbiaceae appear to be particular characteristic along the Negro River (Montero et al., in press).

On Amazonian floodplain forests several studies on species distribution have shown to be closely associated with variation in topography and sedimentation rates (Hughes, 1997; Wittmann et al., 2002). Only a few previous studies, however, have related mosaics of floodplain communities (i.e. succesional stages) to river morphology and, to our knowledge, no study has previously focused the effects of fluvial geomorphology at local and landscape scale on species richness and forest structure along the inundation forest of the Rio Negro.

The objective of this paper is to describe and interpret relations between igapó forest, fluvial geomorphology and the spatial evolution of the igapó forest through the Holocene, along the Negro River. We investigate the effect of geomorphological units of the floodplain and channel patterns, and their effect on spatial distribution patterns of igapó forest. In particular, we address the hydro-geomorphology (HGM) styles at local scale (1-ha scale) and landscape scale (along the channel-floodplain system) and how they control species richness, composition and forest structure of late- succesional forests. In addition, we examine the relationship of HGM with other abiotic predictors of vegetation patterns such as height and duration of inundation and sediments grain size and soil fertility.

We examine the hypothesis that hydro-geomorphological units tend to have similar species composition sharing most of indicator species while species richness and structural patterns may respond to other abiotic factors such as both, intrinsic “state” variables ( soil chemistry or grain size, for example) and active hydrogeomorphologic dynamics (hydrological regime, erosional-depositional processes, etc). Therefore, this study aimed to: (1) to delineate the hydro-geomorphologic units along the Negro River; (2) to characterize tree composition, species richness, abundance, basal area and vertical structure at each geomorphologic unit; and (3) to analyse the relationship between the hydro-geomorphological dynamics and 4) to introduce a time scale evolutionary approach during part of the Holocene.

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4.1.1 Physical setting of the study area

With a mean annual discharge of about 32.000 m3/s and a drainage area of ca. 600.000 km2, the Negro River is the second largest-discharge tributary of the Amazon after the Madeira River (Filizola, 1999). This tropical giant ranks sixth in the world in water discharge and for that reason it was considered part of the selected group of mega-rivers (Latrubesse et al., 2005; Latrubesse, 2008). The Negro River flows approximately 2500 Km from its headwater at the Colombian side until discharging into the Solimões River at the city of Manaus (Figure 4.1). More than 80% of the Negro basin is in Brazil, the rest lies in Colombia and Venezuela.

The basin of the Negro River has one of the highest annual rainfalls across the Brazilian Amazon. The region receives an annual average rainfall of 2.000-2.200 mm, though this increases to over 3.000 mm in the upper sections near the equator. Mean monthly temperatures vary little over the year and range between 25°C and 28°C (Sombroek, 2001). The basin is scarcely inhabited and according to the estimation of the IBGE (2008) there are approximately 90.000 inhabitants in the entire region, mainly concentrated on the four major cities Saõ Gabriel da Cashoeira, Santa Isabel, Barcelos and Novo Airão. Within the Brazilian territory, the Negro receives more than 500 small tributary rivers and streams but a remarkable one is the Branco River at the lower basin, which originates from the northern Roraima massif and transports sand and finer sediments into the Negro (Sioli, 1984; Goulding et al., 2003; Latrubesse & Franzinelli, 2005). The floodplains of the Negro River and its tributaries cover an extension of about 118,000 km2 (Melack & Hess, 2010).

The Negro River is the typical black-water river of the Amazon basin, with olive- brown to coffee-brown colored water and transparencies from 1.3 to 2.3 m because of dissolved humic substances (Sioli, 1984).The river transports just 8 Mt/year of suspended sediment to the Solimões–Amazon (Filizola, 1999), an insignificant quantity of suspended load in relation to the huge water discharge. The bed load is composed of white supermature quartz sand (Franzinelli & Potter 1983; Latrubesse & Franzinelli, 2005). Fine sediments are formed by kaolinitic clays rich in iron and sands derived from weathered rocks of the Precambrian crystalline basement or Paleozoic and Mesozoic sedimentary rocks. The more conspicuous present-day active landforms along the Negro are sand bars.

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Figure 4.1: Course of the Negro River and study sites: upper section (Santa Isabel do Rio Negro, ST); middle section (Barcelos, BA) and lower section (Anavilhanas, AN) (adapted from U.S. Geological Service, 2006). Inset shows the location of the Negro River in central Amazonia.

The vegetation of the Negro basin is very well preserved and the local economy is mainly restricted to the extraction of non-timber forest resources and fishery (Emperarie, 2000; German, 2004), while agriculture and timber extraction is less important. The forests appeared to be undisturbed by humans, although the rubber boom (1850-1920) and various economic short booms between 1930-1990 motivated an intensive extractive uses of non-timber species such as Couma utilis and the latex of various Sapotaceae members such as Manilkara, Pouteria, Chrysophyllum and Micropholis (Emperarie, 2000). Non-forest economic activities are also performed in the region, which include gold mining, gravel extraction and sandstone outcropping for construction (Goulding et al., 1996). Furthermore, sport fishery and ecotourism are important activities in the region, especially along the lower Negro section near the city of Manaus.

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4.1.2 Study area and scope

The study area comprises a 600 km stretch of the river within Brazilian territory, from the city of Santa Isabel (NW) to the Anavilhanas archipelago (SE, Figure 4.1). We selected three study sites along this course of the river: Santa Isabel (00º27'S, 64º46'W, upper section, ST), Barcelos (00°38'S, 63°15'W, middle section, BA) and Anavilhanas (02°46'S, 60°45'W, lower section, AN) (Figure 4.1). Along this stretch, based upon the GLC 2000 land cover map (Bartholomé & Belward, 2005) we roughly estimated an area of 2985 km2 covered by late succesional igapó forest.

4.2 Methods

Our combined hydro-geomorphological- vegetation approach is based on the combination of remote sensing and geomatic products, sedimentary and soil analysis, processing of hydrological data, botanic surveys and the correlation of the age of the floodplain units with the kind of vegetation occurring on them. It is important to remark that the authors had been developing field work along the whole Negro for more than a decade. In the particular case of the floristic data presented here field work was carried out between September 2008 and March 2010 during the low-water periods.

4.2.1 Floristic inventories

Overall, 128 plots (25 x 25 m each) were established in late-successional igapó forest, totaling an area of 8 ha. In each site (ST, BA, and AN), we distributed the plots to three forests (i.e., ST1, ST2, ST3) that were apart by distances of 5-50 km and randomly placed at a different position along the flooding gradient (low, intermediate, and highly flooded). Numbers of plots established accounted for 48 in ST and AN (each 3 ha), respectively, and 32 in BA (2 ha).

All trees ≥ 10 cm diameter at breast height (dbh) were labeled, numbered, and measured in dbh. Tree heights of all trees were determined using a clinometer (Suunto, Vaanta, Finland). Species were indentified in the field, and when this was not possible, identified provisionally as morpho-species with voucher specimen collected for later identification at the herbarium of the National Institute for Amazon Research – INPA, Manaus.

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4.2.2 Hydrology and Geomorphology

Three gauge stations operated by ANA were analyzed: Serrinha, Barcelos and Manaus. Daily stages were processed. Within each plots inundation height at each tree by using previous year’s water marks on the tree trunks were measured. These measurements are correlated with the daily water-level records at the closest hydrometric station to calculate mean height and period of inundation. Thus, for ST plots, flooding duration was calculated by relating data of the neighboring Serrinha gauge station (1978-2006) located 20 km east to the city of Santa Isabel do Rio Negro. For BA plots, flooding duration was calculated by relating data of the water gauge at the city of Barcelos (1968-2006) and for AN plots we used data of the water gauge at Manaus (1903-2006). Mean values of duration and height of inundation were estimated for each species and 1-ha plots.

We used as a base for our analysis the geomorphological units, the sedimentary profiles and chronologies (radiocarbon) described by Latrubesse & Franzinelli (2005). In addition, the interpretation of local geomorphological features was obtained in areas studied in detail for floristic inventories.

4.2.3 Soil sampling

In each 1-ha samples at 3 sites were collected from the first 30 cm of topsoil below the litter layer using a bucket auger (plant material was excluded). Samples were air- dried in the field and pooled for each plot. Chemical and granulometry characteristics were determined at the EMBRAPA soil laboratory following the protocol suggested by Silva (1999). The following chemical properties were analyzed: pH, macronutrients (Ca, Mg, K and Na), micronutrients (Fe, Zn and Mn), and concentration of P, N, Al and relation C/N. Concentration of OM (%) and granulometry (% of sand, silt and clay) were also analyzed.

4.2.4 Analysis of floristic data

The grouping analysis between plots was performed by a hierarchical clustering using the method of Unweighted Pair Group Method with Arithmetic Mean (UPGMA) and quantitative Sorensen (Bray-Curtis) as similarity index (Krebs, 1989). We excluded outliers and rare species which for the present purpose are represented by 1 individual in the entire sample.

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To determine significant differences in species composition and identify species associations for each identified group of plots we calculated the Indicator Species Analysis (ISA) (Dufrene & Legendre, 1997). The ISA combines both abundance and frequency information independently for each species in the dataset, resulting in an indicator value (IV%), which ranges from zero (no indication) to 100 (perfect indication). The species with IV >25% can be considered as a strong indicator of a certain group (Dufrene & Legendre, 1997). A Monte Carlo permutation test with 4999 randomizations was used to test the significance of the indicator value (Dufrene & Legendre, 1997).

Species richness and Fisher's alpha-diversity coefficient (Fisher et al., 1943) were calculated for each plot. Species richness is the number of species per unit area, while Fisher’s alpha index is a parametric measure that assumes that the abundance of species follows the log series distribution (Fisher et al., 1943; Magurran, 2004). Fisher’s index is widely used and is relatively insensitive to sample size thus performing well on tropical forest plots (ter Steege et al., 2000; Chave, 2008). Differences of mean values were compared by using the Welch F-test and a Post- hoc pair-wise comparison using Tukey test.

The vertical structure was described using the total height of each tree measured in meters, in which the number of stems was distributed according to height classes. Thus, we defined 7 classes ranging from < 5m height to > 30 m height, each class separated by 5 m. The basal area was calculated for each tree by using the following formulae: D2 x π /4, where: D= diameter at breast height (d.b.h) and π= 3.14159.

Cluster analysis, species richness, diversity were computed with the program PAST v. 2.04 “Paleontological Statistics Software Package for Education and Data Analysis” (http://palaeo-electronica.org/2001_1/past/issue1_01.htm) (Hammer et al. 2001). Indicator Species Analysis (ISA) was performed with PC-Ord v.5.0 (McCune & Mefford 1999). All statistical analyses were carried out with SPSS 16.0 and PAST v. 2.04.

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4.3 Results

4.3.1 Fluvial geomorphology

On the basis of geomorphologic style and structural control, the Rio Negro can be divided into six reaches (Latrubesse & Franzinelli, 2005) (Figure 4.2).

Figure 4.2: Reaches of the Negro River (I, II, III, IV, V and VI) and study sites (ST 1-3), (BA 1-2) and (AN 1-3). Numbers 1-4 indicate the nodal points. Localities: SI: Santa Isabel do Rio Negro, BA: Barcelos and MA: Manaus. (adapted from Latrubesse & Franzinelli, 2005).

Reach I is the upper basin sourcing a large part of the sedimentary load and the water discharge. The river follows tectonic control by fractures on the crystalline rocks of the Precambrian Shield that are aligned approximately along E–W lineaments. The more conspicuous features along the channel in Reach I are rapids and big rocky islands formed of crystalline rocks outcropping along the channel (Figure 4.2) (Latrubesse & Franzinelli, 2005). The uppermost site in our dataset (ST2) is located in Reach I which is distributed along a marginal area.

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Figure 4.3: Isolated hills and rocky islands formed of crystalline rocks are remarkable along reach I

Reach II starts at Nodal Point 1 where the anabranching pattern of the river begins in alluvial sediments that form a wide Holocene floodplain. Reach II is characterized by the occurrence of a well-developed lower terrace. The plots ST1 and ST3 are located along this reach. Reach III begins where the river turns to an approximate NW–SE alignment that coincides with tectonic lineaments and crosses mainly Paleozoic and Cretaceous sedimentary rocks. It extends for approximately 275 km up to Nodal Point 2, 7 km downstream of the Rio Branco and Rio Negro confluence. Its most spectacular geomorphic element is the Mariuá archipelago and a huge asymmetrical terrace, which appear on the left side practically all along reach III. The plots BA1 and BA2 are located along this reach, near the confluence of southern tributaries which form swamps. Reach IV extends between Nodal Points 2 and 3 and is characterized by the occurrence of some rock outcrops in the channel and because it is a narrow zone.

Reach V coincides with a wide channel belt between Nodal Points 3 and 4, crossing Cretaceous rocks of the Alter do Chaõ Formation. It is characterized by a truly remarkable large archipelago of muddy islands named Anavilhanas (Figure 4.4). Plots AN1, AN2 and AN3 are distributed along this reach. Reach VI runs from Nodal Point 4 to the confluence of the Negro and Solimões Rivers. The virtual absence of islands or other distinctive fluvial landforms in the channel is the main characteristic of this reach.

In terms of geomorphology style the Negro River develops a dominant anabranching pattern from Reach II to the mouth. At the most complex multi-channel patterns of reaches III and V, impressive fluvial archipelagos such as Mariuá and Anavilhanas,

93 Fluvial geomorphology the largest and most complex fluvial archipelagos of the world, develops (Latrubesse & Franzinelli, 2005; Latrubesse, 2008; Montero, 2011).

Figure 4.4: The archipelago of Anavilhanas at Reach V is composed by a complex network of channels, islands and lakes (Photo courtesy of Michael Goulding).

Fluvial terraces had been identified in the Negro River (Latrubesse & Franzinelli, 1998, 2005). The oldest recognizable Late Pleistocene alluvial unit is the Upper Terrace of Middle Pleniglacial age (ca. 65–25 ka) (reach I), tentatively correlated with the oldest terrace identified on the left bank of reach III. At that time, the river was mainly an aggradational bed load system carrying abundant quartz sand, a product of more seasonal conditions in the upper catchment. The late glacial (14–10 ka) is represented by lower finer-grained terraces along the upper basin (reach I), which was recognized in the Tiquié, Curicuriarý, and Vaupes rivers. At that time, the river carried abundant suspended load as a response to climatic changes associated with deglaciation. The huge Anavilhanas and Mariua archipelagos are mainly formed by very young Holocene deposits.

4.3.2 Hydrology

We analyzed the stage record. To compare stage oscillation at three locations along the Rio Negro, hydrograph data at Santa Isabel (Serrinha) , Barcelos, and Manaus. Considering that the stations are not related to an absolute datum, the stage data were arbitrary referred to a 0 (zero) value corresponding to the lowest recorded value of the series for each station. As noted by Meade et al. (1991), stage heights in the lowermost reaches of the Negro are in agreement with the backwater effect of the Solimões–Amazon River that extends as far upstream as Moura, 300 km upriver

94 Fluvial geomorphology from the Amazon confluence. The Manaus station indicates that stage fluctuations in the lower Rio Negro are in phase with the Solimões–Amazon River stage fluctuations (Sternberg, 1987; Richey et al., 1989). In Manaus, the river oscillates up to 15–16 m with an average of ~11 m, whereas 470 km upstream of the confluence at Barcelos (reach III), the average oscillation is ~ 6.6m, while in Serrinha (reach II, Santa Isabel do Rio Negro) ~700 km upstream of the confluence, the average oscillation is ~5.6 (Latrubesse & Franzinelli, 2005). The lowest stages in reach III occur in October– November, but downstream, the lowest stages occur in February–March.

While the river continues to fall in December and January in reach III, downstream (reaches V and VI), the river begins to rise (Meade et al., 1991). These differences in the behavior of water stage demonstrate how the Rio Negro is differentiated into several reaches with particular hydrological behavior. The stage oscillation being least at Barcelos than downstream, is associated with the downstream reduction of secondary peaks and the smoothing of the hydrograph, but also is produced by the reservoir effect of the large tectonic block of reach III and the existence of the Mariuá archipelago.

4.3.3 Floristic differentiation and species composition

The cluster analysis presented in figure 4.5 shows three large groups of plots, which represents the floristic stands associated with upper (ST), middle (BA) and lower section (AN) of the Negro River. However, at ST the dendrogram makes a further separation of two groups of plots, in which ST 1 (group 1) is separated from ST 2 and ST 3 (group 2). Similarly, at Anavilhanas sites (AN) the analysis separated the plot AN 1 (group 4) from AN 1 and AN 2 (group 5). The plots at Barcelos (group 3) present the highest floristic similarity sharing approximately 60% of the species. Within river sections the Bray-Curtis similarity index indicates an average of 52%, however, as expected the floristic similarity for the whole dataset is rather low accounting for only 15% (Figure 4).

95 Fluvial geomorphology

Figure 4.5: Cluster diagram for the 8 sites (128 plots) based on the quantitative Sorensen (Bray-Curtis) similarity index and group mean average (UPGMA) as linkage method.

The Indicator Species Analysis (ISA) combining relative abundance with frequency of each species identified characteristic species at each floristic group. Thus, out of 166 species registered in the dataset the ISA identified 43 species with significance preference for one or more groups (Indicator Value > 25%; Monte Carlo test, P< 0,001). The group 3 represented by the plots BA 1 and BA 2 at Barcelos (middle Negro River) has the greatest number of indicator species (n:18), most of which are only present in these sites. At Anavilhanas, on the other hand, at the plots AN 2 and AN 3 (group 5) the ISA identified only three indicator species. The legume Heterostemon mimosoides is the only species with indicator values (IV) presented in each group of the dataset, although it has more preference for the plots at the lower section of the Negro River (Table 4.1).

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Table 4.1: Indicator species for the five floristic groups: (1) ST1, (2) ST 2- ST 3 (Santa Isabel); (3) BA 1 – BA 2 (Barcelos); (4) AN 1 and (5) AN 2 – AN 3 (Anavilhanas). Only species with an indicator value IV>25% are considered as indicators of a certain group. P- value < 0.01 has a significant preference for one group. Species with indicator value in more than one group are accentuated in bold. Species ST 1 ST 2 – ST 3 BA 1 – BA 2 AN 1 AN 2 – AN 3 p-value (1) (2) (3) (4) (5)

Licaria micrantha 84 0 0 1 0 0.0002 Mouriri sp. 81 1 0 0 0 0.0002 Simaba sp. 48 2 0 0 0 0.0002 Hevea brasiliensis 36 36 14 0 0 0.0002 Cynometra bauhinifolia 32 7 2 0 0 0.0004 Roucheria punctata 31 0 0 0 0 0.0002 Guatteria sp. 29 7 23 0 0 0.0010 Aspidosperma sandwithianum 28 0 0 0 0 0.0004 Eschweilera atropetiolata 21 42 9 0 0 0.0002 Gustavia augusta 16 42 0 14 3 0.0002 Gustavia sp. 5 37 0 0 0 0.0002 Hevea brasiliensis 36 36 14 0 0 0.0002 Pterocarpus sp 2 2 33 0 0 0 0.0004 Crudia amazonica 4 25 0 1 5 0.0002 Duroia sp. 0 0 81 0 0 0.0002 Ocotea sp 1 0 0 81 0 0 0.0002 Swartzia sp 1 0 0 72 0 0 0.0002 Licania heteromorpha 2 2 69 1 0 0.0002 Mabea caudata 1 0 64 8 1 0.0002 Malouetia tamarquina 0 0 56 0 0 0.0002 Amanoa sp. 0 0 50 0 0 0.0002 Virola calophylla 9 1 44 3 0 0.0002 Laetia procera 0 0 41 0 0 0.0002 Naucleopsis sp. 0 0 41 0 0 0.0002 Eschsweilera sp 1 0 0 38 0 0 0.0002 Swartzia sp 2 0 0 38 0 0 0.0002 Micropholis sp. 0 0 36 0 4 0.0002 Diospyros sp. 0 1 33 0 0 0.0004 Eugenia sp 1 0 0 31 0 0 0.0002 Macrolobium angustifolia 0 0 31 0 0 0.0004 Pterocarpus sp 1 0 0 31 0 0 0.0002 Sacoglottis sp 1 0 0 26 1 0 0.0002 Eschweilera aff.amazoniciformis 0 6 0 50 26 0.0002 Tachigalia venusta 0 0 1 39 15 0.0002 Swartzia macrocarpa 0 0 0 37 6 0.0002 Hevea spruceana 0 0 0 31 2 0.0036 Amphirrox sp. 0 1 0 28 5 0.0002 Heterostemon mimosoides 6 4 2 27 45 0.0002 Naucleopsis ternstroemiiflora 0 0 0 25 1 0.0004 Pouteria glomerata 0 9 0 25 0 0.0002 Heterostemon mimosoides 6 4 2 27 45 0.0002 Aldina heterophylla 0 1 1 24 39 0.0002 Eschweilera aff.amazoniciformis 0 6 0 50 26 0.0002

4.3.4 Species richness and diversity patterns

In order to make the results comparable all sites at each river section have been averaged to 1-ha plots. The total number of trees per hectare ranged from 468 AN 1 to 808 at BA 2 (P<0.001). Similarly, species richness (S) experience variation among plots; values ranged from 57 species ha -1 at the BA 1 site to 79 species ha -1 at AN 1. The latter being the richest plot in the dataset. The Tukey post-hoc test revealed significant difference between AN 2 and ST 2, BA 1, BA 2 and AN 1 (all with P <

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0.001). There were no statistically significant differences between ST and BA plots (P >0.05).

Table 4.2: Species richness, alpha diversity, abundance and basal area averaged to 1-ha at the three river sections. Data on height and duration of inundation are based on three harbors located at Manaus (lower); Barcelos (middle) and Serrinha-Santa Isabel (upper) (Source: ANA).

River section Plots Height of N Basal area Duration of inundatio Fisher’s and inundation S (m2/ha) (days year-1) index (α) plot size (cm)

Upper section Santa Isabel ST 1 90 (70 – 124) 86 (40 – 147) 64 19.43 504 28.57 (ST) ST 2 74 (40 – 100) 65 (19 – 110) 67 20.81 500 31.16 48 x 625 m2 (3 ST 3 78 (71 – 92) 56 (33 – 95) 60 16.88 573 31.15 ha)

Middle section Barcelos (BA) BA 1 131 (116 – 147) 242 (217 - 242) 68 18.41 722 51.00 32 x 625 m2 (2 BA 2 133 (116 – 147) 244 (218 – 273) 57 13.99 808 42.41 ha)

Lower section Anavilhanas AN 1 186 (146 – 198) 308 (209 – 345) 79 27.24 468 26.87 (AN) AN 2 186 (157 – 224) 307 (222 – 416) 51 15.54 398 36.39 48 x 625 m2 (3 AN 3 146 (126 – 165) 202 (165 – 243) 63 18.99 505 28.86 ha)

S and N are the total number of species and individuals, respectively registered per plot. α is Fisher’s index of diversity defined by S= α *ln(1+n/ α).

The Fisher’s alpha coefficient confirms the AN 1 plot (α: 27.24) at the Anavilhanas archipelago, as the most diverse in the entire dataset (Table 4.2). A Tukey post-hoc test revealed, however, no significant difference between ST and AN (P=0.88), although these sites are separated by more than 500 kilometers. But pair-wise comparisons determined by the Tukey test also revealed that ST 2 and AN 1 plots presented a significant difference compared with the other sites (P < 0.001). These plots have the highest diversity values averaged per hectare (Table 4.2). With the highest abundance (808 ind/ha-1) in our dataset the BA 2 plot scored the lowest alpha diversity (α: 13.99). Comparing mean values of basal area the one-way ANOVA test revealed significant differences between plots (F (7.58), P < 0.001). In particular, strong differences were detected by pair-wise comparisons after taking the plots BA1 and BA 2 (Tukey test, P < 0.001) compared to the other plots.

4.3.5 Forest vertical structure

The vertical structure is represented by the distribution of the number of individuals for each height classes. The results varied considerably between river sections. In

98 Fluvial geomorphology particular, we observed two remarkable different patterns of distribution at the forest stands of Santa Isabel and Barcelos, located along the upper and middle Negro River, respectively (Figure 4.6). At the forest stands in Santa Isabel (plots ST 1, ST 2 and ST 3) the mean height averaged 18 m (s.d. 2.46) and 80% of individuals are relatively uniformly distributed between the height-range 5 to 25 m. At Barcelos plots (BA 1 – BA 2), however, the mean height averaged 12.64 m (s.d. 1.60) and most of the trees (78%) are grouped only in two height classes (5-10 m and 10-15m). These forest stands also is characterized by the presence of very few emergent trees, which gives rise to shape a nearly homogeneous and continuous canopy. In contrast, due to the presence of a highest number of emergent trees and undefined strata, the forest stands at Santa Isabel seems to resemble the vertical structure of terra firme forest.

Figure 4.6: Two distribution patterns of the vertical structure of the igapó forest along the Negro River. The number of individuals (abundance) is distributed in function of height classes at Santa Isabel (ST1, ST2, ST3, above) and Barcelos (BA1, BA2, below).

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4.4 Discussion

4.4.1 Relationship between geomorphology, hydrology and igapó forests

Plot ST 2 is located on a slightly elevated laterally accreted stable zone that had blocked a small northern tributary system, the Daraá River (Figure 4.7). The area is close to older rocks (“terra firme”) that sustain non alluvial vegetation. A relatively short duration flood period (~73 days year-1), the possible influence of influx and dispersion through the laterally blocked valley plus the proximity to the “terra firme” could contribute to sustain one of the highest alpha diversity per hectare (α: 20.81) registered for the whole sample. The fact that this plot is closer to adjacent non- flooded forest may influence the physiognomy of the vertical structure, which is stratified in indistinguishable forest layers and present the highest density of emergent trees in the entire dataset. Although in little proportions, the floristic composition at ST 2 reveals the occurrence of several species and genera (e.g Dialium guianense, Pseudolmedia laevigata and the genera Toulicia, Roucheria and Diplothropis, data not shown) typical to terra firme forest, which according to Montero et al. (in press) are in evolution or “in transit” to be establish along the floodplains.

The plot ST 3 is located on a laterally accreted zone on the right banks of the Negro River (Figure 4.7). This huge area of sedimentation was generated by the complex anabranching pattern of the Negro which had been filling up the proximal reach I since the late glacial (Latrubesse & Franzinelli, 2005). The area underwent a relatively short period of floods (~78 days year-1), is composed by paleoisland morphology with older abandoned channels that currently support lakes and swamps. The vegetation collection of ST 3 was taken on the highest areas of this lateral floodplain units, which explains why the arboreal vegetation at this point experience low flood duration. However, the averaged alpha-diversity per hectare is pretty low (α: 16.88) and a low sub-plot alpha diversity variability exist (standard deviation= 2.61). The low diversity found in this plot may be explained by the low variability of the micro topography and the influence of the paleo swamps, which display less dynamic and are not hydrologically connected during low water periods. The tree composition shows the greatest abundance of alluvial species typical for black-water floodplains such as Gustavia augusta, Eschweilera atropetiolata and Hevea brasiliensis.

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ST 1

ST 2

ST 3

Figure 4.7: Study sites at the upper section (ST) projected on Landsat images showing the main fluvial units. LFP: Lateral floodplain, TER: Terraza, T-NFP: Tributary-Negro floodplain, TF: Tierra firme. (Source: Global Land Cover Facility. Landsat 5, WGS-84, zone 20).

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BA

AN

Figure 4.8: Study sites at the middle (BA) and lower (AN) sections projected on Landsat images showing the main fluvial units. LFP: Lateral floodplain, T-NFP: Tributary-Negro floodplain, TF: Tierra firme and DW: Death water (Source: Global Land Cover Facility. Landsat 5, WGS-84, zone 20).

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The geomorphologic situation is different in ST 1, which is located in an island in a complex anabranching reach of the Negro river (Figure 4.7). The elongated island is relatively small, 2.75 km in length and with a maximum of 0.65 km in width. A prominent v-shaped sand bar under colonization by pioneer vegetation is present in the island head, on the upstream bank. The plot ST 1 is subjected to 90 days year -1 of inundation and approximately 0.86 cm of flooding height. This flooding regime associated with the complex anabranching pattern at this site may explain the lowest density of trees (504 ind/ha) and basal area (28m2/ha) registered in this river section. These values are only comparable with those recorded at Anavilhanas. However, the averaged 1-ha alpha diversity increases to α: 19.43 and the variability among sub- plots is relatively high (standard deviation= 6.65). The Indicator Species Analysis (ISA) identified only 8 species with significant preference for this site. Two of them Licaria micrantha and Mouriri sp. have the highest indicator values (IV: 84% and 81%, respectively) for the whole dataset.

Plots BA 1 and BA2 are located in an area classified as lateral floodplain, large flat muddy areas of sedimentation (Figure 4.8) (Latrubesse & Franzinelli, 2005). At a first glance, both plots show similar characteristics with approximately 130 days year -1 under flood conditions, high density (BA 1: 722 ind/ha and BA 2: 808 ind/ha), the highest values of basal areas in the dataset (51.0 m2/ha and 42.41 m2/ha, respectively) and shorter vertical structure than the others sites (average heights BA 1: 13.21 m and BA 2: 12.08 m) (Figure 4.9).

However, both localities show different geomorphologic characteristics and influences. Plot BA 2 is located upstream of a small tributary, which flows almost parallel to the main trunk of the Negro; then its origin was exclusively related to the Negro River morphodynamics. However, the area of sedimentation of plot BA 1 is the combination of the blocked valley effect of the small tributary and the Cuiuni River, which is one of the largest southern tributary of the Negro River. Lateral sedimentation of the Negro blocked this area that evolved from a backswamp to almost an infield and vegetated areas with two like-yazoo rivers (Figure 4.8). The lower Cuiuni River is characterized by an inactive meander fluvial belt that is currently reusing the ancient meandering belt. The system is poorly integrated and branches, lakes and swamps interconnect in an intricate network. At the original confluence the river turns towards the SE along more than 20 km interconnecting channels generated by itself and paleochannels of paleoislands of the Negro river. Although the Plot BA 1 is localized in a very marginal area of this geomorphologic

103 Fluvial geomorphology units, we consider that the influence of the tributaries have been influencing the vegetations characteristics and stile of sedimentation.

For example, the influence of the Cuiuni River may be a decisive factor for a greatest diversity observed at BA 1. In this site we registered 69 species ha-1 and calculated an alpha diversity of 18.41 in comparison to 57 species ha -1 and alpha diversity of 13.99 registered at BA 2. The latter plot is the poorest site in our dataset and perhaps one of the poorest 1-ha plots in neotropical floodplain mature forests. In terms of tree composition, the influence of species pool from tributary rivers was extensively discussed by Montero et al. (in press). These authors quantitatively demonstrated that the Barcelos sites presented the highest species turnover (beta diversity) in the whole dataset, due to the occurrence of species that were only present in these sites. For example, the top indicator species Duroia sp, Ocotea sp and Swartzia sp. occurred only in the Barcelos sites. All aforementioned suggest that not only environmental factors are shaping diversity and compositional patterns of the igapó forest along the Negro River, rather geographical position (i.e. tributaries influence) and geomorphologic dynamics are playing a crucial role.

Figure 4.9: Schematic cross sections of reach III (Barcelos sites) and reach V (Anavilhanas sites). Inset in cross sections 1 and 2 represents average values at Barcelos (BA), inset in cross section 3 represents average values at Anavilhanas (adapted from Latrubesse & Franzinelli, 2005).

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Downstream the plots AN 1, AN 2 and AN 3 show different characteristics. The Anavilhanas Islands are a very complex archipelago formed of fine sediment and covered by vegetation. They begin in reach IV but extend downstream to reach V where the wider valley is more favorable to formation (Figure 4.2; Figure 4.8). During the high flow season, these islands are completely flooded, but in the dry season, it is possible to observe banks that in some islands are very steep and up to 5-7 m in height. The islands are characterized by a somewhat phantom morphology formed by a narrow levee-like deposit of fine sediment, which surrounds a semi-circular island head and extends downstream as long as two lateral tails (Latrubesse & Franzinelli, 2005).

Plots AN 1, AN 2 and AN 3 are covered by more than 3m of water during the flood season and the duration of floods varies between 146 days year -1 and 186 days year -1 (Figure 4.9). The forest stands at Anavilhanas present a slightly smaller density of trees and basal area than the other sites. Plots AN 2 and AN 3 present the lowest species richness (51 and 63 species ha -1, respectively) values and also relatively low values of alpha diversity (α: 15.44 and 18.99, respectively). In contrast, AN 1 is richest site at Anavilhanas, reaching 79 species ha-1 and alpha diversity value of 27.24; the latter values are the highest for the whole plots. However the variability among sub-plots is significant and higher than in the Mariua region (i.e BA) (St dev. =5.6 and 6.1 for AN 2 and AN 3 and 7.7 for AN 1). This can be explained for a high variability of well-developed environments in short distances and concentrated in small areas. These results are significant because demonstrates that this high biodiversity concentrates in very narrow islands no wider than 200- to 500m.

The lack of studies in Amazonian floodplains with emphasis on late successional stages along river corridors does not allow reliable comparisons from previous studies in other regions with our findings. The majority of information in the Amazon has been generated in non-flooded habitats. Local scale elevation zonation may play an important role in structuring species composition as observed along lower-lying areas of várzea being dominated by herbaceous species rather than trees (Junk & Piedade, 1993).

Our analysis, however, did not detect a clear effect of the geomorphology on species composition but it is influencing species richness, abundance, basal area and vertical structure. In terms of species composition the major compositional patterns of igapó forests are largely in function of the geographic position of studied sites along the

105 Fluvial geomorphology course of the river. Thus, the inputs of sediment and species pools by tributary rivers are crucial factors in determining tree species assemblages. Moreover, our results indicate that a simple hydro-ecological approach strongly based on the only analysis of hydrological variables may fail in explaining the different patterns on the Igapo forest. Instead, it seems that a combination of factors acting at different scale, space and time are controlling the floristic variation of the igapó forests along the Negro River.

Diversity patterns and forest structure may be better predicted by fluvial geomorphic processes, which operate at smaller spatial scales. The construction of complex floodplains in megarivers such as the Rio Negro is related to the morphodynamics (depositional and erosional processes) but also to the evolution of the floodplain during the Holocene. These floodplains are created and maintained not just by fluctuations of water discharge as traditionally postulated by the eco-hydrological approach promoted by aquatic ecologists but also for the variety of morphological styles and evolution of the system.

4.4.2 The Holocene: floodplain evolution and the spatial distribution of the igapó forest

An evolutionary model for the Negro river floodplain was presented by Latrubesse & Franzinelli (2005). The model considers: a) The river has behaved as a progradational system since ~14 ka (lateglacial), infilling downstream a sequence of structurally controlled sedimentary basins or compartments, generating alluvial floodplains and complex anabranching channel systems. b) Reach II and III were the first to be filled, both accumulating mainly sand. The sedimentation of fine deposits increased downstream in reach III. Reach V has acted almost entirely as a fine sediment trap. c) The lowermost reaches of the Negro (V and VI) have been greatly affected by a rising base level and associated backwater effect from aggradation of the Amazon during late glacial and recent times. d) Suspended sediment load declined about 1.5 ka, prior to the lower part of this basin becoming infilled. Most stable mordphodynamics equilibrium conditions have been achieved in the Holocene in reaches IIb and IIIa, where an anabranching channel and erosional–relictic island system relatively efficiently convey water and sediment. Reaches IIIb and V never achieved

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equilibrium conditions during the Holocene, and they are currently characterized as incomplete floodplains with large areas of open pounded water. e) Both archipelagos (Anavilhanas and Mariuá) are very recent, but the sedimentological of and geomorphologic characteristics of these archipelagos are different. The radiocarbon dating recorded in the islands varies between ~3.7 ka BP and ~1 ka BP, At approximately 1000 BP, the supply fine sediments practically ceased and the sedimentation of clay and silt in the Rio Negro stopped. However, the Mariuá basin continues to be active trapping sand coming from upstream.

When correlating the vegetation with the morpho-evolutionary model exposed above, we can assume that, the Igapó vegetation in the Negro river is mainly related to Holocene deposits and that its evolution and expansion followed spatially and temporally the morpho-sedimentary gradient from upstream to downstream during the Late glacial-Holocene. The average age of the Igapó forest communities should be slightly older in the upper reaches than in the lower reaches and the area of coverage of the Igapó forest in the Negro was increasing in the basin since the Late glacial until arrive to a similar coverage than today ca. 1000 BP.

4.5 Conclusion

This study demonstrates a high floristic variation along the course of the Negro River, revealed by abrupt changes in tree species composition between river sections. Moreover, within river sections, our data suggest the presence of more or less discrete tree assemblages whose indicator species form a unique species pool. These spatial patterns may be explained by the geographic position of the studied sites along the course of the river (i.e. between river sections) while the heterogeneity of the fluvial geomorphology of the Negro River channel may only partially explain the floristic variation within river sections.

We postulated that similar geomorphologic units tend to have similar species composition sharing most of indicator species while species richness and vertical structure may be in function of other intrinsic variables such as status of soil and flooding regime. However, we observed mixed effects of hydro-geomorphologic dynamics, status of alluvial soil and flooding as drivers in the organization of igapo´s tree communities. Thus, despite the BA 1 and BA 2 sites exhibit almost similar characteristics in flooding regime, species composition and vertical structure, the

107 Fluvial geomorphology rather different geomorphology styles appears to control the contrasting species richness recorded in these sites. A similar pattern has been observed at the archipelago of Anavilhanas (lower Negro River). Here the sites AN 1 an AN 2 with almost identical flooding regime and the closeness between both sites exhibit rather different indicator species and contrasting values of species richness, density and basal area. This variability of well-developed environments in short distances and concentrated in small areas demonstrates that this high biodiversity concentrates in narrow islands. This variation of habitats may also explain the highest diversity we recorded in this river section.

The evolutionary approach suggest that the floodplain forest of the Negro River reached the present day distribution very recently, probably no very much before than 1000 BP. The prograding alluvial system of the Negro river generated a time- space gradient from upstream to downstream. In addition to the general Negro’s morphologic and ecological gradients from downstream to downstream, the input of sediments and the construction of alluvial areas by tributaries also had been playing a role in the botanic differentiations of the Igapo forest. The morphological characteristics of the islands and laterally accreted zones, the nature of the sediments (dominantly fine or mixed sand-fine facies), the time duration of floods and the internal morphological components (swamps, scrolls, levees, etc), which produce relief variability in the major fluvial landforms (islands and laterally accreted sediments) introduce more variability and locally modify the general upstream- downstream general gradients.

Our results show that the best approach to understand the distribution of the complex vegetation patterns in complex floodplain of large rivers is a combination of the typical methods applied in botanic collections, ecological analysis and hydro- ecological approaches, with the combination of a geomorphologic methodological approach which introduce a better comprehension of the temporal and spatial evolutionary analysis and a logic rationale to understand the vegetation distribution and variability in function of major landforms, relief variability, soil distributions, hydrology and the internal variability of local scale landforms. Thus, spatial patterns of tree species turnover provide valuable insights into how biological communities may respond to climate and environmental changes, and constitute essential information to the design of protected area networks for conservation.

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5

Synthesis and Perspectives

109 Synthesis and Perspectives

5 Synthesis and Perspectives

In central Amazonia the igapó forest is periodically flooded by the nutrient-poor black water of the Negro River forming the world’s largest black-water inundation forests (Montero, 2011). The complexity of the physical environment along the course of the river and the ecological importance represented by endemism, species diversity and ecological services make probably this region a unique black-water system. However, possibly due to the comparatively low economic importance of igapó forests there is a lack of scientific data. In particular, the floristic knowledge is fairly limited in comparison with its white-water counterpart várzea. The floristic data presented in this dissertation are the first on black-water inundation forest which are based on an extensive quantitative dataset. This information constitutes the first attempt to describe the floristic variation in relation to environmental variables along the course of the Rio Negro filling thus a research gap on Amazonian floodplain areas. I suggest caution with the interpretation of the results as these reveal the explanation of the late-successional stage of the igapó forests without considering early successional stages.

In what follows I first present the key findings of each research chapter highlighting the factors that may better explain the floristic and structural variation of the igapó forests. Afterwards, I conclude by deriving implications for biodiversity conservation and the sustainable management of the floodplain forests along the Negro River.

5.1 Key Findings

 Only few tree species occurred in more than one river section, and floristic composition changed abruptly from one section to the other. Tree species richness ranged from 57 to 79 species ha-1, and alpha-diversity was highest (27.24) in the lower river section upon sediments of Pliocene-Pleistocene origin. I found a gradual decrease in species richness with increasing age of the geological formations. However, when compared to other floodplain forests, igapó forest is relatively species-poor, which may be the result of general low nutrient availability in alluvial substrates of the Negro River (Chapter 2).  The significant floristic contribution of the tributary Jufaris River to the overall species pool suggests that beta diversity of igapó forests along the Negro River may increase as a function of regional species pools. Thus, beta

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diversity in igapó may well be as high as in its whitewater counterparts (Chapter 2).  The flooding regime and granulometry of alluvial soil display a significant variation along the course of the river. Flood amplitudes range from 3.6 m (upper section) to 9.2 m (lower section) subjecting trees to inundation periods of 81 days year -1 and 173 days year -1, respectively. The percentage of finer sediments significantly increased in the lower section, while coarser soils were significantly more abundant in the upper section of the river (Chapter 3).  I found only a slight trend to increase alpha diversity in the lower section of the Negro River (i.e. Anavilhanas) where the duration of flooding and percentage of finer sediments significantly increased. At more restricted scales (i.e. within river sections) the analysis confirmed that the Anavilhanas sites have the highest alpha diversity per unit area, which could also be explained by the comparative major spatial heterogeneity observed at this river section (Chapter 3).  The floristic composition in relation to flooding tolerance classes revealed that no single species occurred along the entire flood gradient. This pattern may be explained by the fact that most of floodplain species have certain preferences for specific topographic levels and flood amplitudes. This may also explain why I found very few generalist species distributed along the course of the river (Chapter 3).  By assessing the relationship of fluvial geomorphology with igapó forests I found a trend that geomorphologic styles seem to control species richness and some structural parameters. In the lower section (i.e. Anavilhanas) sites with identical flooding regime and status of soil and separated by only few kilometers exhibited different indicator species and contrasting values of species richness, density and basal area. This can be explained by the high variability of well-developed geomorphologic units in short distances and concentrated in small areas. In the middle Negro River (i.e. Barcelos) I recorded the highest tree density (average: 765 ind/ha) and the lowest tree- heights (average: 12.6 m) in the whole dataset, which may be explained by the particular type of geomorphology characterized by large flat muddy areas of sedimentation as result of the blocked valley effect of the tributary Cuiuni River (Chapter 4).  The construction of complex floodplains in mega-rivers such as the Negro is related to the morphodynamics (depositional and erosional processes)

111 Synthesis and Perspectives

associated with the evolution of the floodplain during the Holocene (Chapter 4).

Although I detected clear floristic gradients along the course of the river, the geographic variation and the complex physical setting of the floodplain of the Negro River make it difficult to identify and to rely on pure driving forces as determinants of floristic variation. Rather, the results of my investigation suggest that a combination of factors acting at different space, scale and time are determining the overall floristic variation along the Negro River. Here, two types of mechanisms may account for this variation: dispersal-assembly mechanisms that invoke differences in stochastic rates of speciation, extinction and dispersal; and niche-assembly mechanisms that invoke species differences, species interactions and environmental heterogeneity (Hubell, 2001). However, distinguishing between these two mechanisms and understanding how they interact requires the explicit consideration of macroecology. Therefore, to test the relative influence of regional species pools on the Negro River’s species pool, more empirical data along other tributary rivers and similar adjacent habitats are needed. Similarly, an explicit consideration of the local processes such as the dispersion strategies used by indicator species under different flooding and variable spatial distributions is essential. This may lead us to understand the fine-grain variability, and will enable better prediction of future patterns.

My results also suggest that a comprehensive approach to understand the distribution of the complex vegetation patterns in complex floodplains such as the igapó of the Negro River is a combination of the typical methods applied in vegetation sciences with the combination of a geomorphologic methodological approach. This combination of approaches introduces a better comprehension of the temporal and spatial evolutionary analysis and a logic rationale to understand the vegetation distribution and variability in function of major landforms, soil distributions and hydrology. Thus, by integrating the past into macroecological analyses will sharpen our understanding of the underlying forces for contemporary floristic patterns along the inundation forests of the Negro River.

The main contribution of my research is to provide insights to current debates about compositional and diversity patterns along Amazonian floodplain forests. However, my results may also constitute essential information about species distribution patterns in response to predicted impacts of climate change in Amazonian wetlands. Thus, current climate data in the Amazon region show drastic increases in the

112 Synthesis and Perspectives frequency and severity of floods and droughts, which are particularly significant in the Negro River basin (Lewis et al., 2011; Marengo et al., 2011). For example, water levels registered by the harbor authority at Manaus in March 2012 are the highest ever recorded at this period of the year in the last 110 years (Figure 5.1).

Figure 5.1: Water levels of the hydrological cycle at the Manaus Harbor (1903-2011). The yellow and red lines show water levels registered in 2009 and 2012, respectively. Data: SNPH (Superintendência Estadual de Navegação, Portos e Hidrovias, Manaus; Figure: Jöchen Schöngart).

Although there are uncertainties if this extreme flood is due to climatic change or just respond to the natural hydrological regime variability, species composition, abundance and forest dynamics along the flood gradient may change. Major impacts, however, can be expected on the seedling establishment and tree growth behavior (Maria Teresa Piedade, pers.com). A more conclusive scenario on the impacts of a changing hydrological regime and climate is still difficult since tree species respond differently as showed by my results.

Another scenario, in which the unusual intensity and frequency of droughts was observed over a period of only 5 years in the Amazon (2005 and 2010) has alarmed the scientific community (Lewis et al., 2011). These extreme events caused the Negro River to fall to its lowest level on record. For many species, the effects of drought can be as important as flooding for survival and growth, particularly at the seedling phase of establishment, ultimately influencing species composition (Parolin et al., 2010). Therefore, in the context of climate change and predicted decreases in precipitation in the Amazon Basin, the effects of drought on species distribution in floodplain forests should not be overlooked (Parolin et al., 2010).

113 Synthesis and Perspectives

5.2 Implications for classification and conservation of Amazonian wetlands

In general, the design and establishment of conservation units are usually determined by a set of factors such as politics, economics (Constanza et al., 1997) and ecological significance among others. In relation to the latter factor, information on vegetation types and the distribution of its species are basic information to delimit boundaries of specific habitats. In this sense and considering the Amazonian context, ongoing studies led by the wetland monitoring working group at the Brazilian National Institute for Amazonian research (INPA) are aimed at classifying these wetlands according to their climate, hydrology, hydrochemistry and botanical parameters (Junk et al., 2011). This classification, according to these authors, should be considered as a first step of a more detailed classification; therefore a subdivision into easily distinguishable units is required, based on scientific criteria, which allows addressing specific regulations to specific habitats for an efficient management. Thus, classification systems for the Pantanal and the várzea forest have been recently developed (Nunes da Cunha & Junk, 2011). Based on the Negro River floodplain, a classification scheme of the igapó is in advanced state of development where my floristic data provide essential information, especially in the middle and upper sections of the river.

A next step is to categorize the igapós at a continental-wide scale. As presented in the chapter 2 and Appendix 1 igapó forests are distributed across the Amazon and Orinoco basins, however, due to the origin there may be substantial differences mostly in the hydrochemistry. Western igapós are originated or flow through palm swamps (i.e. Mauritia excelsa swamps), transporting Andean sediments of the Tertiary, while central and eastern igapós occur along rivers that drain Precambric Shields of Guyana and Central Brazil. These differences in water chemistry and sediments associated with the geographical position may result in different floristic and structural patterns, for which a classification is required.

114 Synthesis and Perspectives

Figure 5.2: Protected areas along the Negro River (Source: IPAM Institute de Proteao Ambiental do Estado do Amazonas, SDS: Secretaria de Estado do Meio Ambiente e Desenvolvemento Sustentable. 2009)

Probably due to the comparatively limited land use options the floodplains of the igapó along the Negro River present a favorable status of conservation. Protected areas are well represented by indigenous land in the upper section of the river and by federal and state protected areas in the lower section (Figure 5.2). The archipelago of Anavilhanas is completed covered by a state protected, while the entire middle section and part of the upper section are without protected areas (Figure 5.2). My data indicate that the middle section presented the highest beta diversity (species turnover) over a large spatial scale. I further conclude arguing that the inputs of species pools of tributary rivers into this river section may be responsible for this high beta diversity. In the future this data may help to carefully plan the establishment of additional protected areas in the middle section of the Negro River. Conservation planning thus will need to recognize the particularity of this section of the Negro River, considering the amount of northern-southern tributaries and above all where they come from.

115 References

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127 Appendix I

Appendix I

Summary of studies on igapó forests across the Amazon and Orinoco basins. Regions are represented by EA: eastern Amazonia, CA: central Amazonia, WAe: equatorial western Amazonia, WAs: southern part of western Amazonia, NA: northern Amazonia, and OR: Orinoquia. The geology is represented by Pre-Cambrian formations, Tertiary lowlands and Pleistocene-Pliocene formations. Data of geological formations derived from Irion and Morais (2011).

Size No. of No. of Fisher’s Site River Region Geology Reference (ha) trees species alpha Bolivia Manuripi WAs Tertiary 1 542 54 14.92 Montero (Pando) (2002) Manurimi WAs Tertiary 2 1230 94 23.68 Bolivia Aguas WAs Tertiary 1 586 44 11.02 Cominsky et (EBB-Beni) negras al. (1998) Peru Nanay WAs Tertiary 0.5 265 47 16.06 Pacheco (Iquitos) (2008) Ecuador Yasuní WAe Tertiary 1 556 101 36.11 Cerón et al. (Yasuní) (2000) Ecuador Güeppi WAe Tertiary 1 525 66 19.96 Cerón et al. (Cuyabeno) (2003a) Ecuador Limoncocha WAe Tertiary 1 381 69 24.63 Cerón et al. (Limoncocha) lake (2003b) Colombia Cahuinarí WAe Tertiary 0.7 623 107 37.02 Duivenvoorden (mid. & Lips (1993) Caquetá) Venezuela Tawadu OR Pre- 1 653 96 31.04 Castellanos (Caura basin) Cambrian (1998)

Venezuela Caura OR Pre- 1,7 999 103 28.82 Knab-Vispo (lower Caura) Cambrian et al. (1999)

Guyana Moruca OR Pre- 1 550 94 32.06 Van Andel (Santa Rosa) Cambrian (2001)

Gunma Park Igarapé EA Pleistocene- 1 ca.500 153 75.02 Ferreira et al. (Pará) Tracuateua Pliocene 24(20x20) (2010)

Ferreira EA Pleistocene Point. 200 30 9.78 Ferreira et al. Pena station Curuá - transect (2005) (Pará) Pliocene (10 x 5) O deserto Xingu EA Pre- 0.5 220 40 14.31 Campbell et al. (Pará) Cambrian (1986) CA Pre- 1 252 21 5.44 Cambrian

Lower CA Pre- 1 271 30 8.62 Ferreira & Tapajós Tapajos Cambrian Prance (1988) (Pará) CA Pre- 1 489 24 5.29 Cambrian

Viruá Park NA Pre- 1 1125 69 16.22 (Roraima) Cambrian Gribel et al Iruá NA Pre- 1 516 60 17.58 (2009) Cambrian

Amanã Igarapé CA Pleistocene 1 546 119 46.91 (RDSA) Taboca - Ayres (1993) Amazonas Pliocene Amanã lake CA Pleistocene 1.06 700 98 31.01 Rodrigues (mixed - (2007) water) Pliocene Amanã lake CA Pleistocene 0.75 472 106 42.51 - Inuma (2006) Pliocene

128 Appendix I

CA Pleistocene 0.75 442 88 33.00 - Pliocene

Lower Purus Uauaçú CA Pleistocene 3 2049 99 21.72 Haugaasen & (Amazonas) lake - Peres (2006) Pliocene Anavilhanas Rio Negro CA Pleistocene 0.50 460 64 20.02 Piedade - (1985) Pliocene Anavilhanas Rio Negro CA Pleistocene 0.50 462 73 24.39 Piedade et al. - (2005) Pliocene Anavilhanas Rio Negro CA Pleistocene 0.15 267 51 18.71 Parolin et al. - (2003) Pliocene CA Pleistocene 0.21 172 61 33.74 Worbes (1986) - Pliocene CA Pleistocene 0.1 162 44 19.87 Tarumã Tarumã - Mirim Mirim Pliocene Parolin et al. CA Pleistocene 1.5 43 10 4.09 (2004) - Pliocene CA Pleistocene 1 777 44 10.01 - Ferreira (1997) Pliocene

CA Pleistocene 1 941 103 29.48

Jaú - Jaú Park Pliocene

CA Pleistocene 1 1111 137 41.01 - Pliocene Anavilhanas Lower Rio CA Pleistocene 3 1371 102 25.47 Negro - (64/ha) Pliocene Barcelos Middle Rio CA Pleistocene 2 1530 79 17.66 Negro - (62/ha) Pliocene Present study Middle Negro Jufaris CA Pleistocene 1 593 57 15.54 - Pliocene Santa Isabel Upper Rio NA Pre- 3 1577 108 26.27 Negro Cambrian (63/ha)

129 Appendix II

Appendix II List of families, scientific names, and number of individuals per species in the four study areas. The taxonomy has been checked in the Tropicos database (http://www.tropicos.org/). Classification, follows APGIII flowering plants classification. AN: Anavilhanas, BA: Barcelos, JU: Jufaris, ST: Santa Isabel.

River sections Family Species AN BA JU ST number of individuals Anacardiaceae Tapirira guianensis Aubl. 18 1 Annona sp. 1 5 Duguetia sp. 1 2 Duguetia sp. 2 4 Duguetia uniflora (DC.) Mart. 15 Guatteria aff. olivacea R.E. Fr. 20 Annonaceae Guatteria cf.subsessilis Mart. 13 9 2 Guatteria sp. 1 46 37 Tetrameranthus sp. 3 Unonopsis guatterioides R.E. Fr. 18 37 Xylopia parviflora (A. Rich.) Benth. 2 Xylopia sp. 1 1 Xylopia sp. 2 2 Aspidosperma nitidum Benth. ex Müll. Arg. 18 2 5 Apocynaceae Aspidosperma sandwithianum Markgr. 6 Himatanthus sucuuba (Spruce ex Müll. Arg.) Woodson. 5 Malouetia tamaquarina (Aubl.) A. DC. 26 Aquifoliaceae Ilex inundata Poepp. ex Reissek. 2 Arecaceae Astrocaryum jauari Mart. 1 15 Bignoniaceae Tabebuia barbata (E. Mey.) Sandwith. 3 24 Burseraceae Protium sp. 20 Caryocaraceae Caryocar glabrum Pers. 7 4 1 Celastraceae Maytenus guyanensis Klotzsch ex Reissek. 6 Salacia impressifolia (Miers) A.C. Sm. 1 1 Chrysobalanaceae Couepia bracteosa Benth. 15 Couepia krukovii Standl. 1 Couepia macrophylla Spruce ex Hook. f. 9 Couepia sp. 7 Hirtella physophora Mart. & Zucc. 5 Hirtella racemosa Lam. 12 22 1 Hirtella sp. 1 1 Licania apetala (E. Mey.) Fritsch. 45 64 46 30 Licania heteromorpha Benth. 5 114 11 10 Licania micrantha Miq. 3 3 62 56 Licania sp. 1 1 1 Parinari excelsa Sabine. 3 Parinari parvifolia Sandwith. 5 Parinari sp. 1

130 Appendix II

River sections Family Species AN BA JU ST number of individuals Calophyllum brasiliense Canbess. 11 2 2 Caraipa grandifolia Mart. 7 2 Caraipa sp 10 57 6 Clusiaceae Garcinia madruno 2 Havetiopsis flavida 3 Tovomita choisyana 1 3 Vismia aff sprucei 11 Buchenavia capitata 10 Buchenavia grandis Ducke. 3 Combretaceae Buchenavia sp. 1 5 1 Buchenavia sp. 2 2 Diospyros aff. poeppigiana A.DC. 2 Diospyros glomerata Spruce. 1 Ebenaceae Diospyros sp. 16 2 Diospyros vestita Benoist. 1 Sloanea cf. floribunda Spruce ex Benth. 6 2 Sloanea cf. terniflora (Sessé & Moc. ex DC.) Standl. 5 Elaeocarpaceae Sloanea grandiflora Sm. 7 Sloanea sp. 1 Emmotaceae Emmotum acuminatum Miers 2 Erythroxilaceae Erythroxylum mucronatum Benth. 1 Erythroxylum sp. 19 2 Alchornea discolor Poepp. 3 14 4 Amanoa gracillima W.J. Hayden. 68 Amanoa sp. 87 Croton lanjouwensis Jabl. 2 1 Hevea brasiliensis (Willd. ex A. Juss.) Müll. Arg. 40 13 149 Hevea guianensis Aubl. 1 Hevea spruceana (Benth.) Müll. Arg. 15 9 Mabea caudata Pax & K. Hoffm. 20 195 32 8 Mabea sp. 1 Maprounea guianensis Aubl. 25 2 Micrandra siphonioides Benth. 18 30 39 Euphorbiaceae Pera cf. bicolor (Klotzsch) Müll. Arg. 2 Pogonophora schomburgkiana Miers ex Benth. 4 Acosmium nitens (Vogel) Yakovlev. 4 9 Aldina heterophylla Spruce ex Benth. 118 6 44 5 Andira sp. 2 Campsiandra comosa Benth. 1 3 14 Copaifera sp. 6 Crudia amazonica Spruce ex Benth. 13 2 1 36 Cynometra bauhiniifolia Benth. 6 29 Cynometra marginata Benth. 6 Cynometra spruceana Benth. 10 7 Dalbergia sp 1 Dialium guianense 4 Diplothropis sp 2 7 Fabaceae Dipteryx sp. 2

131 Appendix II

River sections Family Species AN BA JU ST number of individuals Heterostemon mimosoides Desf. 287 18 43 Hydrochorea corymbosa (Rich.) Barneby & J.W. Grimes 1 Hydrochorea marginata (Spruce ex Benth.) Barneby & J.W. Grimes 8 Hydrochorea sp. 1 1 6 2 Inga alba (Sw.) Willd. 1 Inga sp. 1 1 8 Inga sp. 2 1 Macrolobium acaciifolium (Benth.) Benth. 8 2 1 Macrolobium angustifolium (Benth.) R.S. Cowan 12 Macrolobium limbatum Spruce ex Benth. 11 5 10 Macrolobium sp. 1 6 Microlobium sp. 2 Ormosia discolor Spruce ex Benth. 6 Ormosia excelsa Benth. 35 Ormosia sp. 1 3 21 Ormosia sp. 2 3 Ormosia sp. 3 7 Parkia discolor 1 5 Peltogyne cf. catingae Ducke 1 Peltogyne excelsa Ducke 48 20 16 Peltogyne sp 8 Platymiscium sp 1 Pterocarpus rohrii Vahl 5 84 Fabaceae (cont) Pterocarpus sp. 1 16 Pterocarpus sp. 2 21 Sclerolobium chrysophyllum Poepp. 65 Sclerolobium sp. 2 Swartzia argentea Spruce ex Benth. 1 2 Swartzia auriculata Poepp. 7 Swartzia corrugata Benth. 2 Swartzia laevicarpa Amshoff 2 Swartzia macrocarpa Spruce ex Benth. 20 Swartzia polyphylla DC. 4 Swartzia reticulata Ducke 15 19 12 Swartzia sp. 1 41 Swartzia sp. 2 17 Swartzia sp. 3 8 Swartzia sp. 4 3 Tachigali sp. 1 2 Tachigali venusta Dwyer 45 4 2 Taralea oppositifolia Aubl. 16 8 Vatairea guianensis Aubl. 8 1 Vatairea sp. 1 20 Zygia inaequalis (Humb. & Bonpl. ex Willd.) Pittier 2 Zygia juruana (Harms) L. Rico 3 2 9 Zygia latifolia (L.) Fawc. & Rendle 7 Zygia sp. 1 4 Zygia sp. 2 1

132 Appendix II

River sections Family Species AN BA JU ST number of individuals Sacoglottis guianensis Benth. 80 Humiraceae Sacoglottis sp. 1 1 10 Ixonanthaceae Ochthocosmus barrae Hallier f. 26 Licaria chrysophylla (Meisn.) Kosterm. 2 Mezilaurus itauba (Meisn.) Taub. ex Mez 1 Nectandra amazonum Nees 3 5 5 Ocotea aciphylla (Nees) Mez 4 Lauraceae Ocotea cinerea van der Werff 24 3 17 Ocotea cymbarum Kunth 4 6 2 17 Ocotea megacarpa van der Werff 2 Ocotea sp. 1 72 Ocotea sp. 2 4 Eschweilera aff. Amazoniciformis S.A. Mori 106 33 Eschweilera albiflora (DC.) Miers 5 Eschweilera atropetiolata S.A. Mori 39 11 118 Eschweilera bracteosa (Poepp. ex O. Berg) Miers 12 3 Eschweilera pseudodecolorans S.A. Mori 1 Lecythidaceae Eschweilera sp. 1 21 Eschweilera sp. 2 2 Gustavia augusta L. 55 12 282 Gustavia hexapetala (Aubl.) Sm. 6 Gustavia sp. 42 Lecythis cf.barnebyi S.A. Mori 9 Lecythis sp. 1 14 15 7 Linaceae Roucheria punctata (Ducke) Ducke 11 Roucheria sp. 1 4 Loganiaceae Strychnos jobertiana Baill. 1 Malpighiaceae Blepharandra heteropetala W.R. Anderson 3 Burdachia prismatocarpa A. Juss. 2 Bombacopsis nervosa (Uittien) A. Robyns 27 Bombacopsis sp. 1 9 Lueheopsis rosea (Ducke) Burret 10 Malvaceae Mollia lepidota Spruce ex Benth. 35 46 Mollia speciosa Mart. 35 74 Pachira aff. insignis (Sw.) Sw. ex Savigny 7 Pachira cf.aquatica Aubl. 2 Quararibea sp. 2 Miconia sp. 14 1 Melastomataceae Mouriri angulicosta Morley 117 Mouriri sp. 1 42 Meliaceae Guarea sp. 1 9 2 Trichilia sp. 9 13 Brosimum sp. 13 Brosimum utile (Kunth) Oken ex J. Presl 1 Ficus sp. 1 2 Moraceae Helianthostylis sp. 1 Maquira sp. 4 Naucleopsis aff. ternstroemiiflora (Mildbr.) C.C. Berg 8

133 Appendix II

River sections Family Species AN BA JU ST number of individuals Naucleopsis glabra Spruce ex Pittier 2 Moraceae (cont) Naucleopsis sp. 21 Pseudolmedia aff. laevigata Trécul 11 Pseudolmedia sp. 13 Myristicaceae Virola calophylla (Spruce) Warb. 5 107 15 Virola surinamensis (Rol. ex Rottb.) Warb. 16 1 13 Myrsinaceae Cybianthus sp. 2 Calyptranthes aff. crebra McVaugh 4 16 12 Calyptranthes cuspidata DC. 1 12 2 Calyptranthes multiflora Poepp. ex O. Berg 6 7 Myrtaceae Calyptranthes sp. 1 39 3 Eugenia sp. 1 37 Eugenia sp. 2 6 Eugenia sp. 3 7 Nyctaginaceae Neea sp. 1 1 Ochnaceae Lacunaria sp. 1 2 2 Quiinna sp. 1 1 Chaunochiton kappleri (Sagot ex Engl.) Ducke 3 Heisteria aff. acuminata (Humb. & Bonpl.) Engl. 5 1 Olacaceae Heisteria sp. 1 1 8 Heisteria sp. 2 1 Minquartia guianensis Aubl. 8 4 Opiliaceae Agonandra silvatica Ducke 9 Pentaphylacaceae Ternstroemia dentata Spreng. ex DC. 20 Polygonaceae Coccoloba charitostachya Standl. 1 Proteaceae Panopsis sessilifolia (Rich.) Sandwith 52 Panopsis sp. 2 Duroia sp. 222 5 Faramea torquata Müll. Arg. 1 1 Henriquezia nitida Spruce ex Benth. 5 Rubiaceae Palicourea sp. 3 Warszewiczia sp. 1 Homalium sp. 73 Laetia corymbulosa Spruce ex Benth. 8 Salicaceae Laetia procera (Poepp.) Eichler 27 1 Lindackeria sp. 2 Sapindaceae Cupania sp. 24 3 Toulicia sp. 10 Chrysophyllum sanguinolentum (Pierre) Baehni 1 Manilkara huberi (Ducke) A. Chev. 53 Micropholis egensis (A. DC.) Pierre 70 Micropholis sp. 7 32 Pouteria aff. glomerata (Miq.) Radlk. 12 1 14 Pouteria caimito (Ruiz & Pav.) Radlk. 8 Pouteria elegans (A. DC.) Baehni 20 11 73 19 Pouteria gamblei (C.B. Clarke) Baehni 2 Pouteria sp. 1 16 Sapotaceae Pouteria sp. 2 2

134 Appendix II

River sections Family Species AN BA JU ST number of individuals Pouteria sp. 3 1 Sapotaceae (cont) Pouteria sp. 4 2 Simaba guianensis Aubl. 7 Simaroubaceae Simaba sp. 1 31 Styracaceae Styrax tessmannii Perkins 1 Cecropia sp. 1 1 Urticaceae Pourouma sp. 2 Amphirrox sp. 15 2 Violaceae Leonia aff. racemosa Mart. 3 Rinorea racemosa (Mart.) Kuntze 11 Erisma aff. Bracteosum Ducke 6 Vochysaceae Qualea sp. 1 Vochysia cf.vismiifolia Spruce ex Warm. 5

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