FACULTE DES SCIENCES Département de Biologie des Organismes

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FACULTE DES SCIENCES

Département de Biologie des Organismes

Laboratoire d’Ecologie végétale et Biogéochimie

VEGETATION PATTERNS AND ROLE OF EDAPHIC HETEROGENEITY ON PLANT COMMUNITIES IN SEMI-DECIDUOUS FORESTS FROM THE CONGO BASIN

Par

AMANI YA IGUGU Aimé-Christian

Thèse présentée en vue de l’obtention du grade de Docteur en Sciences

Année académique: 2010-2011

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VEGETATION PATTERNS AND ROLE OF EDAPHIC HETEROGENEITY ON PLANT COMMUNITIES IN SEMI-DECIDUOUS FORESTS FROM THE CONGO BASIN

Par

AMANI YA IGUGU Aimé-Christian

Composition du jury :

Prof. Pierre Meerts (Promoteur, Université Libre de Bruxelles)

Prof. Nyakabwa Mutabana (Co-Promoteur, Université de Kisangani-R.D. Congo) Prof. Jean Lejoly (Université Libre de Bruxelles)

Prof. Nausicaa Noret (Université Libre de Bruxelles) Prof. Patrick Mardulyn (Université Libre de Bruxelles) Prof. Gilles Colinet (Université de Gembloux)

Prof. Steven Dessein (Jardin Botanique de Meise)

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To my late grandfather Edouard IGUGU who instilled in me the love of Nature

To my parents Gervais IGUGU and Françoise FURAHA who gave me the opportunity to study natural sciences

To my wife Justine KITUMAINI and my daughter Christine FURAHA who strengthened me to fulfill these studies

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Abstract and thesis outline

Vegetation patterns and role of edaphic heterogeneity on plant communities in semi- deciduous forests from the Congo Basin

Contrary to the other forest ecosystems in the Democratic Republic of Congo (D.R. Congo), semi-deciduous forests have so far attracted little attention and studies regarding their ecological aspects remain sketchy. Yet semi-deciduous forests are among the most important non-flooded ecosystems in the Congo Basin and their importance is high, both ecologically and economically. They are home to a variety of species, some of them being exploited for timber by forest companies acting in the region. There is a constant need to focus on their composition and diversity, and to understand factors shaping their communities.

Moreover, as of present interest in the other tropical forests, the role of substrate as a major environmental factor still needs to be assessed. Many studies have focused on the impact of soil features in tropical rainforest ecosystems worldwide and pointed out the importance of edaphic variables on the distribution of trees within the tropics. However, such an approach is not developed in the numerous forest ecosystems found in the D.R. Congo. This is also the case for studies focusing on distance decay which expresses species turnover (beta-diversity) within plant communities. Within the Congo Basin, and particularly in the surroundings of Kisangani (D.R. Congo), semi-deciduous forests are established on contrasted habitats marked by sandy and clay substrates. Interestingly, there is a growing interest to focus on phylogenetic structures of ecological communities and though examples are numerous in other tropical forests, such an attempt has not yet been undertaken in the Congolese forests.

Using a sampling method broadly inspired from the synusial phytosociology approach, we examined plant communities within each of the forest layers composing the overstorey (canopy and emergent trees) and the understorey (shrub and herbaceous layers).

In order to bring a clear understanding of our study and particularly our results, this dissertation is subdivided into eight main chapters. In Chapter 1, we present a general introduction providing an insight of our main concepts. Our plant communities are viewed in a common understanding of tropical rainforests and in the context of the present main

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interests of tropical ecology. Then follows the Chapter 2 which describes the major details one needs to know when the Congo Basin is concerned. In this chapter, we also provide a summarized view of our main objectives, these latters being separately developed in chapters dealing with the results. Floristic parameters of the considered semi-deciduous forests are provided in Chapter 3, as well as an insight on phytosociological aspects, as expressed by the three phytosociological plant groups recognized in the overstorey. In Chapter 4, we present a case study of a community located in a particular zone of our study area where sandy and clay substrates encounter over a steep textural gradient. We then analyze species distribution patterns within each of these two substrates, with particularities in the interface zone. We also describe the spatial structure of the considered edaphic variables, based on the Moran’s index. The relationships between soil features and species within the forest layers are exposed in Chapter 5. We show that some of the species found in the considered semi-deciduous forests are more related to a type of soil than another, defining some “edaphic specialists” species while many others can be considered

“generalists”. Chapter 6 focuses on the role of distance on species turnover in these plant communities, as well as the relative importance of the spatial variations of environmental conditions. Spatial distance effect in the considered plant communities is marked by a decrease of floristic similarity with the geographical distance. In Chapter 7, we focus on the phylogenetic patterns occurring in plant communities within forest layers. All forest layers showed a pattern of spatial phylogenetic clustering meaning that species cohabiting within a same plot are more related than species from distant plots. Finally, a general discussion of the results is provided in Chapter 8. Then follow references of authors cited and appendices.

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Résumé et subdivision de la thèse

Caractéristiques de la végétation et impact de l’hétérogénéité édaphique sur les communautés végétales dans les forêts semi-caducifoliées du Bassin du Congo

Contrairement aux autres écosystèmes forestiers de la République Démocratique du Congo (R.D. Congo), peu d’études ont jusque-là été menées dans les forêts semi-caducifoliées.

Celles-ci constituent pourtant une part importante des forêts de terre ferme dans le Bassin du Congo et leur intérêt est capital, aussi bien sur le plan écologique qu’économique. Les forêts semi-caducifoliées renferment des espèces variées dont certaines sont exploitées pour leur bois par des compagnies forestières actives dans la région. Il existe un besoin permanent de connaître l’écologie de ces forêts et comprendre l’action des facteurs environnementaux sur l’organisation de la végétation dans ces écosystèmes.

Dans beaucoup d’études forestières dans le monde tropical, le rôle du substrat sur l’organisation de la végétation est de plus en plus pris en compte et certaines recherches ont montré l’influence des variables édaphiques sur la distribution des espèces sous les tropiques. Cependant, de telles approches demeurent rares dans les forêts congolaises. Il est à noter que les forêts semi-caducifoliées qui font l’objet de la présente étude dans les environs de Kisangani (R.D. Congo) sont établies sur des substrats hétérogènes, parfois marqués par une répartition discontinue du substrat argileux et sableux. Par ailleurs, des approches intégrant le rôle de la distance géographique sur la végétation (le turnover des espèces ou diversité bêta) ne sont pas développées. Et pendant que de nouvelles approches prenant en compte les aspects phylogénétiques connaissent un essor dans d’autres écosystèmes tropicaux, pareilles initiatives font encore défaut dans le Bassin congolais et plus particulièrement dans les forêts congolaises.

Sur base d’une méthode inspirée des approches de la phytosociologie synusiale, nous avons examiné les aspects de la végétation dans quatre différentes strates : strates arborescentes supérieure et inférieure, strate arbustive et strate herbacée.

Pour une bonne présentation de notre sujet et surtout des résultats, le travail a été subdivisé en huit grands chapitres. Une introduction générale est fournie dans le Chapitre 1 dans lequel sont exposés la plupart des concepts utilisés. Les forêts semi-caducifoliées y sont également présentées dans le contexte général des forêts denses humides tropicales. Les

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particularités physiques et biotiques propres au Bassin du Congo, où a lieu la présente étude, sont exposées dans le Chapitre 2 ainsi qu’une vue d’ensemble des différents objectifs qui sont plus largement discutés dans des chapitres appropriés. La partie propre aux résultats commence par le Chapitre 3 qui présente des détails sur la composition floristique des forêts semi-caducifoliées en étude ainsi que des aspects phytosociologiques, sur base des relevés des strates arborescentes supérieures qui définissent trois groupements distincts. Au Chapitre 4, nous examinons la situation dans une zone de contact entre sols sableux et argileux dans un des sites étudiés. Les particularités spécifiques propres à chaque type de sol sont fournies ainsi que la situation dans la zone d’interface séparant les deux sols. La structure spatiale des différentes variables édaphiques est également indiquée, en utilisant l’indice de Moran. La réponse des espèces vis-à-vis de l’hétérogénéité édaphique sur l’ensemble du jeu de données est détaillée dans le Chapitre 5. Certaines espèces montrent une préférence pour un type de sol que pour un autre, tandis que la plupart d’autres se révèlent être plutôt indifférentes. C’est dans le Chapitre 6 qu’est analysé le rôle de la distance géographique sur la composition floristique dans les différentes communautés végétales. Il s’observe une baisse de la similarité floristique, en fonction de l’accroissement de la distance géographique. La structure phylogénétique des communautés végétales dans les forêts semi-caducifoliées en étude est analysée au sein du Chapitre 7. D’une manière générale, on remarque un signal d’agrégation phylogénétique spatiale indiquant que les espèces cohabitant au sein des mêmes relevés sont plus apparentées (plus proches de l’arbre phylogénétique) que des espèces issues des relevés différents. Une discussion générale des résultats intervient dans le Chapitre 8. Enfin, viennent les références bibliographiques et les diverses pages d’annexes.

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List of figures

Chapter 1 :

Figure 1. Soil horizons and their main characteristics………5

Figure 2. Soil profile showing horizons in a lateritic soil in tropical and equatorial zones………6

Figure 3. An example of ternary plot used to determine soil textural class from the percentages of sand, silt, and clay in the soil………..7

Figure 4. Schematic representation of direct and indirect control of SOM stability by soil invertebrates……….12

Figure 5. A hierarchical model of factors that determine soil processes. Activities and diversity of soil organisms by a hierarchical organization of biotic and abiotic factors…………13

Figure 6. Schematic representation of community assembly in case of a single stable equilibrium and in a case of multiple stable equilibria………18

Figure 7. Types and origins of community phylogenetic patterns………..22

Figure 8. Terrestrial ecoregions on the globe. Tropical rain forests are located into three continents: America, Africa and SE Asian……….23

Figure 9. An example of stratification in a tropical forest………27

Chapter 2:

Figure 1. A world map showing the location of the Congo Basin………30

Figure 2. The Congo River inside the D. R. Congo……….……….31

Figure 3. The Congo River and its drainage network………32

Figure 4. Image of the Congo River flowing through a tropical rain forest………..33

Figure 5. Number of dry months per year in the Congo Basin………..34

Figure 6. Precipitation map in Central Africa……….35

Figure 7. Soil humidity map of the Congo Basin………..36

Figure 8. Location of the Central Congo Basin within the D.R. Congo……….37

Figure. 9. The Cuvette Centrale in the Congo Basin and its ecoregions……….38

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Figure 10. Land cover map of the D.R. Congo showing 18 land cover classes………39

Figure 11. Soil map of the D.R. Congo showing the dominance of ferralsols in the Central Congo Basin………40

Figure 12. Portion of the soil map of the world showing the distribution of xanthic ferralsols in the Central Congo Basin………..41

Chapter 3:

Figure 1. Sampling design showing the 4 layers (A, Ad, ar, H)……….49

Figure 2. 10 dominant species in the upper forest layer………55

Figure 3. 10 species characterizing the lower arborescent forest layer……….55

Figure 4. 11 most representative species in the understorey (shrub layer)……….56

Figure 5. Relative frequency of the most representative herbaceous species………..57

Figure 6. Number of trees in diametric classes………57

Figure 7. Diametric structures as observed on sandy and clay substrates………58

Figure 8. Variations between the number of species and the number of individuals in the woody forest layers……….58

Figure 9. CA showing the 3 plant groups identified after a phytosociological analysis……….………..60

Figure 10. CCA expressing the relation between plots and edaphic variables in the 3 phytosociological groups showed in figure 9……….61

Chapter 4:

Figure 1. Schematic disposition of subplots on sandy and clay soils separated by an interface zone……….73

Figure 2. Concrete representation of plots in the sampling area………74

Figure 3. Principal component analysis representing all the subplots and the correlation between edaphic variables……….79

Figure 4. Mean densities of the 15 dominant species in the overstorey (a: A-stratum; b: Ad- stratum)………82

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Figure 5. Factorial plans 1-2 (horizontal-vertical) of a correspondence analysis performed on the abundance matrix of the A-stratum and Ad-stratum, including subplots of the interface………..83-84 Figure 6. Factorial plan 1-2 (horizontal-vertical) of a canonical correspondence analysis

computed with data from abundant species……….85

Chapter 5:

Figure 1. Differences in textural features between plots and sites………97

Figure 2. Species accumulation curves within the woody forest layers showing differences in species composition due to substrate effect……….98

Figure 3a. Species rarefaction curves in the upper arborescent layer………..99

Figure 3b. Species rarefaction curves in the lower arborescent layer………..99

Figure 3c. Species rarefaction curves in the shrub layer……….100

Figure 4. Comparison of the local diversity (Fisher alpha index) between sandy and clay substrates within the woody forest layers (Yoko and Biaro sites) ………..100

Figure 5. Comparison of the local diversity (Fisher alpha index) between sandy and clay substrates in the woody forest layers (all the 3 sites)………..101

Figure 6a. Important species (based on their Importance Value Index) characterizing the clay soils in the upper arborescent layer (Yoko)……….104

Figure 6b. Important species (based on their Importance Value Index) characterizing clay soils in the lower arborescent forest layer (Yoko)………104

Figure 7a. Important species (based on their Importance Value Index) characterizing sandy soils in the upper arborescent layer (Yoko)……….………105

Figure 7b. Important species (based on their Importance Value Index) characterizing sandy soils in the lower arborescent forest layer (Yoko)………105

Figure 8a. Species characterizing clay soils in the upper arborescent layer in Biaro……….106

Figure 8b. Species characterizing clay soils in the lower arborescent layer in Biaro……….106

Figure 9a. Important species (based on their Importance Value Index) characterizing sandy soils in the upper arborescent layer in Biaro………..107

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Figure 9b. Important species (based on their Importance Value Index) characterizing sandy soils in the lower arborescent forest layer in Biaro………107 Figure 10a. Important species characterizing the upper arborescent forest layer in Yangambi………..108 Figure 10b. Important species characterizing the lower arborescent forest layer in Yangambi………..108 Figure 11a. Canonical Correspondence Analysis with species from the upper arborescent layer and edaphic variables……….110 Figure 11b. Canonical Correspondence Analysis with species from the lower arborescent layer and edaphic variables……….111 Figure 11c. Canonical Correspondence Analysis with species from the shrub layer and edaphic variables………112 Figure 11d. Canonical Correspondence Analysis with species from the herbaceous layer and edaphic variables………113

Chapter 6:

Figure 1a. Correspondence Analysis for the upper arborescent layer………128 Figure 1b. Correspondence Analysis for the lower arborescent layer……….129 Figure 1c. Correspondence Analysis applied to the shrub layer………129 Figure 2. Principal Component Analysis expressing the edaphic variables effect on plant communities………..130 Figure 3a. Variation in the species composition between substrates and among substrates in the upper arborescent layer………131 Figure 3b. Variation in the species composition between substrates and among substrates in the lower arborescent layer………132 Figure 3c. Variation in the species composition between substrates and among substrates in the shrub layer……….132 Figure 4. Variation of the species composition on sandy soils in the overstorey……….133 Figure 5. An example of distance decay in a plant community from Costa Rica………137

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Figure 6. An example of distance decay in terra firme forests from Panama, Ecuador and

Peru………..137

Chapter 7:

Figure 1a. Spatial phylogenetic indices and their general trend through distance (upper arborescent layer)………..147

Figure 1b. Spatial phylogenetic indices and their general trend through distance (lower arborescent layer)………..147

Figure 1c. Spatial phylogenetic indices and their general trend through distance (shrub layer)………147

Figure 2. Patterns of the abundance phylogenetic structure (PAD) in woody forest layers………..148

Figure 3. Changes in species relatedness (PIst index) with spatial distance in forest layers...151

Chapter 8:

Figure 1. Percentages of floristic variability explained by environmental factors in the woody forest layers...155

Figure 2. Variation of the density of the 6 most dominant trees in woody forest layers………160

Figure 3. Variation in the frequency of the 6 most dominant trees in forest layers………161

Figure 4. An illustration of the importance of environmental filtering in the process leading to species establishment………163

Photo 1. Collection of Non Timber Forest Product: an example of the Marantaceae species………166

Photo 2. Evidence of forest clearing by fire in the Congo Basin………167

Photo 3. Evidence of forest destruction for agriculture in the Congo Basin……….167

Photo 4. Evidence of forest destruction for fire woods in the Congo Basin……….……168

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List of tables

Chapter 3:

Table 1. Plot parameters and variation of taxa in forest layers………52

Table 2. Family relative diversities in the upper arborescent forest layer………..53

Table 3. Relative diversities of families in the lower arborescent layer……….53

Table 4. Inventoried families in the shrub layer and their relative diversities………54

Table 5. Families and their number of species in the herbaceous layer……….54

Table 6. Species diversity in the woody forest layers………..59

Chapter 4 :

Table 1. Mean values (± SD among plots) of the edaphic variables on each soil type with tests of spatial autocorrelation……….78

Table 2.Tests of spatial autocorrelation (Mantel test between matrices of Moran’s I index and the logarithmic distance) for each edaphic variable………..80

Table 3. Changes in species composition (abundances expressed by the number of recorded trees) for species encountered in the two forest layers………81

Chapter 5:

Table 1a. Edaphic variables between plots located in Yoko………96

Table 1b. Edaphic variables between plots located in Biaro………..96

Table 1c. Edaphic variables between plots located on sandy soils in Yangambi………..96

Table 2. Diversity patterns driven by edaphic heterogeneity (Yoko and Biaro)………97

Tableau 3. Correlations between species abundances and soil textural values (Yoko and Biaro)………103

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Chapter 6:

Table 1. Diversity in the woody forest layers……….125 Table 2a. Correlations between soil variables and diversity indices in the upper forest layer (Yoko and Biaro)………..126 Table 2b. Correlations between soil variables and diversity indices in the lower arborescent layer (Yoko and Biaro)……….127 Table 2c. Correlations between soil variables and diversity indices in the understory (Yoko and Biaro)……….127 Table 3. Mantel tests showing results from correlations between the matrix of floristic similarity and spatial distance (distance effect) as well as between the matrix of floristic similarity and ecological distance (soil effect) (Yoko and Biaro)………133 Table 4. Mantel tests showing results from correlations between the matrix of floristic similarity and spatial distance (distance effect) on sandy soils (all 3 sites)………134

Chapter 7:

Table 1. Phylogenetic diversity and distinctness of species between forest layers……….146

Table 2. Community phylogenetic structuring in forest layers………..146 Table 3. Patterns of phylogenetic structure driven by substrate differentiation………..149

Chapter 8:

Table 1. Chart of the effect of soil pH on nutrient availability………156

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List of appendices

Appendix 1. Plant checklist: Species and families are given………199 Appendix 2. Local names of some surveyed species……….212 Appendix 3. Cluster analysis of a matrix containing 30 plots and 242 species (overstorey)………..……….215 Appendix 4. Phytosociological groups of overstorey’s species: synoptic table…..……….216 Appendix 5. Tests of spatial autocorrelation (Mantel test between matrices of Moran’s I index and the logarithmic distance) for the most representative species according to soil type and in the interface zone………..220 Appendix 6. Correlations between species abundances and soil textural values in the upper arborescent layer (Yoko and Biaro)………221 Appendix 7. Correlations between species abundances and soil textural values in the lower arborescent layer (Yoko and Biaro)………225 Appendix 8. Floristic parameters of species in the upper arborescent layer: clay soils

(Yoko)………..231 Appendix 9. Floristic parameters of species in the lower arborescent layer: clay soils

(Yoko)……..………233 Appendix 10. Floristic parameters of species in the upper arborescent layer: sandy soils (Yoko)………..237 Appendix 11. Floristic parameters of species in the lower arborescent layer: sandy soils (Yoko)………..239 Appendix 12. Floristic parameters of species in the upper arborescent layer: clay soils (Biaro)……….242 Appendix 13. Floristic parameters of species in the lower arborescent layer: clay soils (Biaro)……….244 Appendix 14. Floristic parameters of species in the upper arborescent layer: sandy soils (Biaro)……….246 Appendix 15. Floristic parameters of species in the lower arborescent layer: sandy soils (Biaro)……….248

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Appendix 16. Floristic parameters of species in the upper arborescent layer (Yangambi)………..250 Appendix 17. Floristic parameters of species in the lower arborescent layer (Yangambi)………..252 Appendix 18. Phylogenetic tree of the most representative species in the upper arborescent layer……….255 Appendix 19. Phylogenetic tree of the most representative species in the lower arborescent layer……….256 Appendix 20. Phylogenetic tree of the most representative species in the shrub layer……….257 Appendix 21. Phylogenetic tree of species in the herbaceous layer……….258 Appendix 22. Portion of the D.R. Congo’s land cover map showing the location of plots in Yangambi………..259 Appendix 23. Portion of the D.R. Congo’s land cover map showing the location of plots in Yoko……….260 Appendix 24. Portion of the D.R. Congo’s land cover map showing the location of plots in Biaro……….261

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Acknowledgements

The fulfillment of this thesis is just one tinier drop in the huge scientific ocean of knowledge marked by many more prior works in the field of human endeavor. It is also an expression of combined positive actions and incentives from too many persons.

The particular circumstances in which I undertook my PhD program deserve to be mentioned. Everything started with Professor Jean Lejoly and Professor Nyakabwa Dominique-Savio, before I could continue with Professor Pierre Meerts. The scientific supervision of my works was conducted by Professor Olivier Hardy who provided all the statistical support I needed for data analysis.

My special thanks are therefore addressed to my four Supervisors who held me in their hands, guided my shaking steps, showed me the way and finally taught me to walk.

Professor Pierre Meerts kindly accepted to supervise this work, just after Professor Jean Lejoly retired. He provided me with very useful comments and fruitful suggestions that helped to improve the work. Professor Jean Lejoly initiated the study and actively spent some times with me in the forests to test the methodological approach used for data collection. Professor Nyakabwa Mutabana Dominique-Savio also initiated the study and always supervised my works when I was his student in the Democratic Republic of Congo (D.R. Congo). He introduced me to the science of Botany and helped me develop and sharpen my existing love for plants and majestic forests. I had the good luck and privilege to meet with Professor Olivier Hardy, particularly in the very beginning when everything was totally vague in my brain. He kindly introduced me to his numerous statistical skills, fully considered me as one of his privileged students, kindly accepted my limited background during the infinite discussions and never got angry when I was confused and completely overwhelmed.

I also owe a special debt of gratitude to all my jury members who actively read the first version of my work and who improved it with their relevant comments and remarks.

My PhD program could never have been achieved without financial supports I got from the Belgian Technical Cooperation (BTC). I sincerely thank the BTC and its dynamic team which combined actions in D.R. Congo and in Belgium. I particularly thank Ms Liesbet Vastenavondt

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and Mr Nicolas Brecht who replaced her. I am also grateful to Mr Jean-Claude Kakudji and Ms Angèle Mowa Kapundu.

My field works also received an important grant from the Center for International Forestry Research (CIFOR), through its project REAFOR. This is the opportunity to thank Dr Robert Nasi for his support in helping me getting that grant. My thankful feelings are also addressed to Professor Ndjele Léopold and Professor Mate Mweru Jean-Pierre who coordinated the project REAFOR and provided me with support I needed during field work.

I would like to express my gratitude to the staff of the Université Officielle de Bukavu (D.R.

Congo) for all the administrative support I got, in time, for my traveling in and outside the country and remain grateful to many colleagues who actively supported me. I always had very constructive discussions with Professor Muhigwa Bahananga who always encouraged me, first as his student and finally as his colleague. Professor Charles Kahindo never failed to enquire about my progress and always provided incentives and advice.

Many other persons helped me very much during our numerous discussions. Never shall I forget all the support I got from my friend Jason Vleminckx with whom I spent time in the forest during data collection campaigns and who was always available for me to discuss data analysis and to prepare scientific papers. I also was kindly approached by Professor Thomas Drouet who guided me during my soil analyses and who read my manuscripts several times with so much fruitful suggestions. Dr Bruno Senterre discussed the methodology with me and provided me with important references. I got constructive comments on my proposal from Dr Vincent Freycon (CIRAD) and interesting exchanges with Dr Ingrid Parmentier (ULB, Belgium). During a Tropical Biology Association one month training course, I benefited from experiences from Dr James Vonesh (University of Florida, USA), Dr Clive Nuttman (University of Cambridge, UK), Professor Munishi Pantaleo (Sokoine University, Tanzania) and Dr Jette Knudsen (Lund University, Sweden).

Many thanks to Professor Eric Van Ranst (Ghent University, Belgium) for the new soil map of the D.R. Congo and to Mr Franck Theeten (Royal Museum for Central Africa, Belgium) for the GIS assistance. I do not forget Professor Marius Gilbert (ULB, Belgium) for his statistical course during which I had the opportunity to get introduced to R software. I remain grateful to Professor Paul Brioen (Belgian Royal Library) for scanning some of the books I needed.

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During my long absences from home, I met with very hospitable people. I therefore thank very much Professor Honorine Ntahobavuka, Professor Hippolite Nshimba, Dr Kahindo Jean- Marie, Janvier Lisingo, Sindani, Pasteur Mayani Aston, Joseph Makana, Richard Lokoka, C.T.

Lomba, Assumani Dieu Merci, Frank Bapeamoni, Sylvain Kumba, Prosper Sabongo, Robert, Consolate Kaswera, Carine Aliango, Brown Mungindo and many other persons I met in Kisangani while collecting my data. I also met many kind-hearted persons during my stays in Brussels who helped me either socially or scientifically. I particularly would like to express my gratitude to Serge Yedmel, Dominique Dumont, Pascal Mannes, Philippe Ghysels, Barbara Liberski, Olivier Lachenaud, Joseph Bigirimana, Gilles Dauby, Piet Stoffelen and Raymond Vleminckx.

Many friends of mine provided me with strong support and I thank very much Dodo Kishingoko Brave, Alphonse Balezi, Dr Céphas Masumbuko, Papa Lunanga, Jules Basimine, Dominique Bikaba, Micheline Kani-Kani and Chantal Shalukoma.

My sincere gratitude goes to my family members who provided me with both support and inspiration. Endless thanks to my parents Gervais Igugu and Françoise Furaha, my brothers Ricky Ombeni, Arsène Safari Bob, Musimwa Albert, my sisters Charlène Ilunga, Rolande Zawadi, Bintu Dada and Christelle Nabintu, and all the numerous others. I will never forget my godfather Dr Léonard Mubalama and his whole family, my uncle Dénis Igugu, my cousins John Kahekwa and Delphin Murhula and also thank my family in law, particularly my father Jacques Madarhi and my brother Kasereka Bishikwabo.

Finally, the very best of my gratitude goes to my wife Justine Kitumaini who successfully managed to cope with her pharmaceutical studies and home duties during my long and repeated absences and who kindly tolerated my changing moods due to my long stressful stays in forests. My thoughts always went to my beloved daughter Christine Furaha who, I hope, will forgive me to have disappeared from home (and keeping her far from my direct love, assistance and support) at that particular moment when she only was thirty-six days old.

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Chapter 1 General introduction

Understanding ecological patterns of the vegetation in semi-deciduous forests in the Congo Basin requires that the situation be viewed in the general context of tropical rainforests and mechanisms leading to their organization.

In this chapter, we present some of the main ecological concepts explaining species occurrences in tropical forests. Important details on these particular ecosystems are also presented.

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I. PATTERNS OF SPECIES OCCURRENCE

1.1. Conditions and resources for species occurrence

Ecologists recognize that the distribution of a species is a consequence of environmental factors acting on it. As stated by Brown and Lomolino (1998), each species is particularly marked by a restricted geographic range, in which it encounters a limited range of environmental conditions. According to the same authors, the most obvious patterns on which depends the distribution of organisms refer to the variation in the physical environment and are therefore different according to the considered habitat. In terrestrial habitats these patterns are determined by climate and soil type whereas in aquatic habitats the distribution of organisms is mainly controlled by variation in temperature, salinity, light and pressure.

Understanding the distribution and abundance of a species requires many things to be known, one of them being the resources that it requires and the effects of environmental conditions acting on it. Following Begon et al. (1990), a condition is defined as an abiotic environmental factor which expresses variation both in space and time, and to which organisms are differently responsive. Conditions always define ecological ranges expressing a minimum, a maximum and an optimum concentration (which represents the level of a condition at which a given species performs best). These three ecological ranges give rise to the notion of limiting factor, one of the common ecological concepts.

As defined by Tilman (1982), resources stand for all things consumed by a given organism.

The life of a plant requires a multitude range of resources. These include light (solar radiation), carbon dioxide (CO2), water and mineral nutrients. While carbon dioxide is fixed through leaves (accepted by the ribulose diphosphate -RDP- molecule during photosynthesis), water and mineral nutrients are taken from the soil thanks to roots. Begon et al. (1990) emphasize that the mineral resources that a given plant must obtain from the soil (or, in the case of aquatic plants, from the surrounding water) include macronutrients (i.e. those needed in relatively large amounts) – N, P, S, K, Ca, Mg and Fe – and some trace elements – e.g. Mn, Zn, Cu and Bo. Contrary to the other resources, solar radiation is generally considered to be the unique source of energy that green plants can use in their metabolic activities. It is also considered to be a factor which plays a key role in shaping

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natural communities because light partitioning and its availability represent a fundamental cause leading to different vegetation layers (defining the overstorey and the understorey).

1.2. Soil and climate as patterns for species occurrences

Considering climate, the global distribution of rainfall is one of the major patterns controlling the occurrence of plants and vegetation worldwide, and this leads to the largely known concept of biome, an important notion expressing the hierarchical organization of living matter. In the particular case of tropical regions, it is believed that the cooling of ascending warm air laden with water vapor results into heavy rainfall particularly occurring at low and middle elevations, where rain forest and cloud forest are located (Brown and Lomolino 1998). Moreover, the type of soil is one of the three ingredients (as well as climate and history of disturbance) on which depends primarily the type of vegetation covering a region (Brown and Lomolino 1998).

At a general point of view, scientists agree that the mechanisms leading to soil formation are complex. Both biotic and abiotic processes play an important role, in respect to the different interactions that exist mainly between soil and plants. A general consensus is that soil is formed by the weathering of rock and the accumulation of organic material originating both from dead and decaying organisms. On the other hand, physical processes (freezing and thawing, water and wind erosion) act to break down the parent material. The biotic processes (representing the role of living organisms) mentioned above are various and the scope of their actions is fully dependent upon the nature of the considered organism. For examples, lichens can hasten the weathering of rock whereas decaying corpses of plants and animals may alter the chemical composition of the soil (Brown and Lomolino 1998; Cline 1977; Lal 2004). In this process, living animals can also impact the soil chemical properties through their physiological evacuations and burrowing animals can mix the soil and aerate it.

Technically known as pedogenesis, the formation of soil involves two processes, weathering and development of soil profile (Kapoor 2007). As stated above, the weathering of rocks to form soils involves physical, chemical and biological processes. The particular relationships between soil and soil biota are exposed in paragraph 1.6.

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Brown and Lomolino (1998) distinguish four major processes (regarded as pedogenic regimes) considered to produce the primary, or zonal, soil types within habitats:

podzolization (temperate deciduous and coniferous forests), laterization (tropical forests), calcification (arid grasslands and shrublands) and gleization (waterlogged tundra). In the humid tropics, experiencing high temperatures and heavy rainfall, the role of microbes and other organisms is important: they rapidly break down dead organic material and therefore little humus can accumulate.

Laterization, also called ferralitization (van Schuylenborgh 1971) represents the weathering process occurring in tropical soils and during which soils are depleted of silica and bases while being enhanced with aluminum and iron oxides. In the tropics, it is generally considered that silica and many cations (e.g. K+, Na+, Ca²⁺) are easily leached from soils not only as the consequence of the high solubility of base cations in the soil solution (Bern et al.

2005) but also because of the heavy rainfall (Brown and Lomolino 1998). Tropical soils are therefore highly weathered and acidified. This acidification represents an ongoing pedogenetic process driven by proton sources (which actively intervene in mineral weathering reactions) such as acidic deposition, nitrification, the dissociation of carbon and organic acids, and excess cation uptake by vegetation in forest ecosystems (Fujii et al. 2011).

1.3. The importance of soil physical properties

Soil is expected to influence the life of plants, through its texture and its structure. Soil structure is often expressed as the degree of stability of aggregates. The process of aggregation results from the rearrangement, flocculation and cementation of particles.

(Kettler et al. 2001; Lal 2004). Soil structure and texture vary as a function of soil age (Lohse and Matson 2005). Soil structure influences its porosity as well as its permeability. It is generally considered that permeability is usually greatest in sandy soils compared to clayey soils which, conversely, express the highest porosity. These two factors are responsible for soil drainage capacity and also control moisture availability in a given soil (Gabler et al.

2009).

The weathering process of rocks over a period of time results in the formation of different horizons (soil layers) which form the soil profile representing the vertical section of a soil

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from top to bottom (fig. 1). Soil horizons express differences in their properties: texture of mineral particles, color of the soil, microbial activities, water holding capacity and percentage of organic matter (Kapoor 2007; Gabler et al. 2009).

Fig. 1. Soil horizons and their main characteristics. O horizon represents a layer of organic debris and humus. A horizon is referred to as the topsoil and contains decomposed organic matter. E horizon occurs in some soils with strong eluviations processes. B horizon is a zone of accumulation where much of the materials removed from A and E horizons are deposed. The C horizon is the weathered parent material from which the soil has developed. R horizon stands for the unchanged parent material (source: Gabler et al. 2009).

These horizons and the pedogenetic processes that form them vary widely from a soil to another (van Schuylenborgh 1971; Kapoor 2007; Townsend et al. 2008; Gabler et al. 2009).

For the particular case of laterite resulting from the laterization process in humid tropical and subtropical climates, the O horizon is absent (fig. 2) and the A horizon offers particular chemical properties: fine soil particles are lost, as well as the majority of minerals and bases (except for iron and aluminum compounds which are insoluble mainly due to the absence of organic acids), a situation which results into a reddish and almost porous topsoil. Moreover,

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the B horizon in a lateritic soil has rather a high concentration of illuviated materials than is the A horizon (Gabler et al. 2009).

Soils in the humid tropics correspond to the group of ferralsols in the FAO classification (World Reference Base), also known as oxisols in the USDA system (van Schuylenborgh 1971;

Moormann and Breemen 1978; van Wambeke et al. 1983; FAO 2006). They are deeply weathered, red or yellow, and express diffuse horizon boundaries with a clay assemblage strongly marked by low-activity clays (mainly kaolinite) and a high content of sesquioxides (Moormann and Breemen 1978; FAO 2006).

Soil texture determines the rate at which water drains through a saturated soil. The field capacity of a soil is defined as the water held by soil pores against the force of gravity. Based on this field capacity, soil texture also influences how much water is available to the plant.

Compared to sandy soils, clay substrates are generally recognized to have a greater water holding capacity given that pores of sandy soils are much wider, which leads much of the water to drain away (Begon et al. 1990; Berry et al. 2007). Soil texture is also considered to affect soil erodibility (susceptibility to erosion) which is proportional to the percentage of silt and clay particles. Differences in soil texture also impacts the availability of organic matter considered to breaks faster in sandy soils holding higher amounts of oxygen available for

Fig. 2. Soil profile showing horizons in a lateritic soil following the soil-forming regime (laterization) that occurs in tropical and equatorial zones (source: Gabler et al.

2009).

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decomposition in the light-textured sandy soils. Following their textural features, chemical properties differ from a soil to another. For example, the cation exchange capacity of a soil increases with percent clay and organic matter which also control the pH buffering of a soil (its ability to resist pH change upon lime addition). (Berry et al. 2007).

Soil texture is subdivided into classes, according to portions of sand, silt and clay (fig. 3).

Sand, the largest particle of the soil, is visible to the eye. Sand particles are between 2 and 0.05 millimeters in diameter. Medium-sized soil particles are called silt; their particles are between 0.05 and 0.002 millimeters in diameter. Clay forms the smallest particles, less than 0.002 millimeters in diameter (Presley and Thien 2008).

Fig. 3. An example of ternary plot used to determine soil textural class from the percentages of sand, silt, and clay in the soil (Presley and Thien 2008; Fernandez-Illescas et al. 2001; Berry et al. 2007).

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1.4. Factors controlling species distribution in tropical forests

In comparison to temperate regions where temperature and water stress control the distributions of species, in tropical regions most studies focusing on species distributions, particularly in lowland forest, make links directly with rainfall or associated soil fertility gradients (Veenendaal and Swaine 1998).

Many studies have focused on factors controlling species distributions throughout the tropics with numerous interesting examples from America and Asia, as well as from the African continent. For the particular case of the African tropical forests, among the most interesting studies are those reported from Ghana (Hall and Swaine 1981; Hawthorne 1996).

The distribution of species following soil nutrients and other environmental factors was also examined in different parts of the tropical world (e.g. Swaine 1996; Sollins 1998; John et al.

2007; Peh et al. 2011).

It is believed that a relationship may exist between soil fertility gradients and rainfall gradients as a consequence of a long history of higher rainfall which leads to cumulative leaching of plant nutrients in tropical rainforests. However, the way in which soil fertility influences species distribution (and particularly the importance of soil nutrients) is still very debatable (Grubb 1995; Sollins 1998). An important question remains to disentangle between the effects of soil properties and those from the numerous other environmental factors. For example, analyzing species occurrence in relation to soil fertility and annual rainfall in Ghana, Swaine (1996) noted that a large proportion of species express preferences for particular rainfall and soil fertility conditions, regardless of their distributions and thus suggested that both soil fertility and seasonal drought may limit the distribution of tree species, in the particular case of west African forests. In the wet tropics, species response to drought conditions is generally considered to limit species distributions (Turner 1990; Fisher et al. 1991). Important studies established correlations between annual rainfall and species distributions as well as diversity gradients (Swaine 1996; Gentry 1988; Bongers et al. 1999;

Bongers et al. 2004; Hall and Swaine 1976; ter Steege et al. 2006) whereas others report the role of soil moisture as one of the key factors on which depend associations of tropical species (Sollins 1998; Webb and Peart 2000; Davidar et al. 2007). However, though water availability is considered to be the most important factor controlling species occurrences in

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the tropics, the underlying mechanisms are still unclear (Engelbrecht and Kursar 2003;

Poorter and Markesteijn 2007; Engelbrecht et al. 2007; Kursar et al. 2008).

1.5. The role of soil on plant communities in tropical forests

Within the tropical rainforests, the soil is generally considered to be very nutrient poor or infertile. This infertility is due to the fact that tropical soils are very ancient (more than 100 million years old) and the heavy rains wash mineral out of the soils, leaving them more acidic and nutrient poor. Therefore, the only reason plant life is so lush is because plants store the nutrients in themselves rather than getting them from the soil and when plants decay, other growing plants tap the nutrients from the dead matter and reuse nutrients left over from that plant. However, there are some fertile patches of soil in the rainforest, but they are scattered throughout the thick vegetation. The topsoil is only 2.5 to 5 centimeters deep.

Because of their long exposure to heat and condensed sunlight, tropical soils turn into red clay. ( http://library.thinkquest.org/C0113340/text/biomes/biomes.rainforest.soil.html) The possibility that soil factors might control species occurrence in tropical forests has long intrigued researchers (Sollins 1998) and evidence exists that soil features actually play a major role in shaping plant communities in tropical rain forests. As reported by Clark et al.

(1995), a growing number of studies have demonstrated strong effects of edaphic heterogeneity on floristic composition within tropical forest communities (e.g. Ashton 1969; Oliveira-Filho et al. 1994). The role of soil nutrients on tropical species has been elucidated by many authors (e.g. Newberry et al. 1986; John et al. 2007; Peh et al. 2011) and, as reported by Yamada et al. (2006), evidences of association of tree species with physical (edaphic and/or topographic) habitats are commonly observed in tropical rain forests.

Sollins (1998) identified a number of soil properties considered to be the most important in influencing species composition in lowland rainforests. Phosphorus availability is the first of them and others are (in decreasing order of importance) Aluminum toxicity, drainage, water- holding capacity and availability of potassium, calcium and magnesium. However, a particular attention is put on phosphorus, generally regarded as the most important limiting nutrient in tropical forests (Vitousek and Sanford 1986; Silver 1994). Moreover, tropical soils are believed to be ancient soils and because of the high rainfall in the tropics, they are

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labeled poor nutrient soils which also experience a low pH. Evidence exist that low pH values highly influence the soil chemistry by increasing the solubility of some cations which in turn can lead to increased toxicity caused by H+, Al and Mn, as well as a reduced uptake of most other nutrients (Cuenca et al. 1990; Marshner 1991). Therefore, toxicity and cation deficiency are thus as likely as phosphorus deficiency to limit species.

Studies have reported habitat specialization in tropical forests (e.g. Fine et al. 2005; Yamada et al. 2007). According to Baltzer et al. (2005), the fact that many tropical tree species express a nonrandom distribution among edaphic patch types suggests that edaphic heterogeneity strongly influences species diversity. These authors give interesting examples of edaphic specialization within the tropics: Harms et al. (2001) found that some of the Panamanian species showed significant habitat associations characterized by edaphic factors whereas in Malaysia, Thomas (2003) who also focused on the impact of soil features on plant composition reported a case of edaphic specialization.

Explanations for this edaphic specialization in tropical forests have been proposed (Baltzer et al. 2005): 1) greater tolerance to high concentrations of trace metals by some species (which often give rise to some rare and endemic species); 2) biotic interactions (e.g. herbivory and mycorrhizal associations) which may contribute to tree species habitat associations; 3) species differ in ability to withstand conditions of limiting resource availability that vary among soil types (terms referred to as the ‘‘resource-use efficiency hypothesis’’).

However, the influence of edaphic factors differs according to spatial scales (Clark et al.

1999), also considered to affect differently species interactions and the use of resources (Sterner et al. 1986; Clark et al. 1999; Condit et al. 2000; Wright 2002). At mesoscales (≈ 1–

100 km²) and landscape scales (10² to 10⁴ km²), tropical forest landscapes represent a mosaic of edaphic types, expressing levels of heterogeneity and spatial segregation and therefore the effects of dispersal and habitat factors on species distributions and community structure are relatively easily quantified. The impact of spatial scale becomes less evident at the local scale (< 1 km²) because the spatial aggregation patterns of species that result from both limited dispersal and habitat heterogeneity coincide in ways that make it difficult to disentangle their relative importance to local community structure (John et al. 2007).

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1.6. Soil properties and the role of edaphic biological communities

Soil is considered to be one of the most diversified terrestrial habitats. Estimations report that a single gram of soil is home to several thousands of bacterial species and diversified fungal communities about which only little is known (Torsvik et al. 1994). Among these soil microorganisms are the nitrogen-fixing bacteria (Rhizobium spp.) and other organisms capable of diazotrophy (e.g. Frankia spp.). Also, some fungi species are very important in the mineralization processes thanks to their symbiotic association with roots of vascular plants (mycorrhizae). The soil fauna is also lush with many species of protozoa, nematodes, earthworms, and other invertebrate groups forming the microfauna, mesofauna and macrofauna (Hawskworth and Mound 1991; Lavelle et al. 1992; Torsvik et al. 1994; Giller et al. 1997; Lavelle 1997; Wolters 2000). The distribution of the microfauna (ø < 0.2 mm) is limited to the water film around surfaces whereas the mesofauna (0.2 ≤ ø ≤ 2 mm) particularly colonize the pore systems of soils. The macrofauna, which are the largest of the three (ø > 2 mm), represent the only group capable of breaking through physical barriers of soils (Wolters 2000).

Several interactions exist between soil and these biological communities (soil biota). They are generally considered to be responsible for the improvement of edaphic properties (aggregate stability and porosity) due to root dynamics, macrofaunal activity (Manlay et al.

2000) and contribute to the conservation of nutrients in the plant biomass (Abbadie et al.

1992). Furthermore, they are very active in the transformation of the available litter and the macrofauna (represented by termites and earthworms) are generally labeled ecosystem engineers (Lavelle 1997) because of their ability to modify the soil environment through their mechanical activities. Conversely, the activities of soil biota are directly controlled by edaphic properties and other environmental factors such as temperature, water potential and substrate availability (Babbar and Zak 1994; Bohlman et al. 1995; Holland et al. 2000;

Davidson and Jansenss 2006).

Several authors focused on relationships between soil biological communities and their impact on soil properties (Lavelle et al. 1998; Kappler and Brune 1999; Wolters 2000;

Mathuriau and Chauvet 2002; Bossio et al. 2003; Cleveland et al. 2003; Reynolds et al. 2003;

Milton and Kaspari 2007; Schroll et al. 2006; Cleveland et al. 2006a) and particularly pointed

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out the importance of soil organic matter (SOM) on which depend both physical (stability, porosity) and chemical (pH and cation exchange capacity) properties of a given soil (Wild 1995; Asadu et al. 1997; Manlay et al. 2002). Moreover, SOM determines its biological fertility because it is the main source of energy for soil biota and its importance as a reserve for nutrients required by plants, and ultimately by the other living creatures which depend on them (Brown et al. 1994; Jobbágy and Jackson 2000; Wolters 2000; Craswell and Lefroy 2001) and without which the Earth’s surface could only represent a sterile mixture of weathering minerals (Craswell and Lefroy 2001).

It has been proven that edaphic animals affect the physico-chemical properties of soils through their important role in the cycling of nutrients. Furthermore, evidence exists that invertebrates influence almost every level of decomposition cascade and contribute to the stabilization and destabilization of SOM and therefore affect soil processes both directly and indirectly (Wolters 2000, fig. 4).

Fig. 4. Schematic representation of direct and indirect control of SOM stability by soil invertebrates (source:

Wolters 2000).

More important is the active role of soil microorganisms in the numerous biochemical processes that occur in the soil (nutrient mineralization, nutrient cycling, decomposition and composition of organic matter, decomposition of xenobiotics, etc.) and that are mediated by intracellular and extracellular enzymes produced by microorganisms (Waldrop et al. 2000;

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Weitz et al. 2001; Matson et al. 2002; Acosta-Martinéz et al. 2007; ) in accordance with soil environmental factors (soil moisture, temperature, pH, oxygen and organic carbon concentration).

Definitely, soil biotic factors play a key role in the stability of soil properties and conserve an important place in the processes generating them (fig. 5). Abiotic factors (climate, soil conditions) and biotic factors (human and animal activities) influence the vegetation (productivity and structure) which in turn exerts an impact on soil biota through availability, quality and distribution of organic resources (Giller et al. 1997).

Fig. 5. A hierarchical model of factors that determine soil processes. Activities and diversity of soil organisms by a hierarchical organization of biotic and abiotic factors (after Giller et al. 1997).

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1.7. Habitat differentiation and species distribution: edaphic ecotypes

Environmental heterogeneity often leads to phenotypic differences which occur between individuals from the same species following their distribution and adaptation to different environmental conditions. If those differences are genetically based, the different populations adapted to contrasting habitat conditions are referred to as ecotypes. The ecotype concept represents the genotypic response of a species to environmental factors (Clary 1979). An ecotype is a population or a group of populations that have evolved particular traits in response to natural selection under specific habitat conditions (Briggs and Walters 1997).

Fundamentally, three main groups of ecotypes can be distinguished: climatic, edaphic and biotypic (cenotic). Edaphic ecotypes are those whose distributions are strongly influenced by edaphic conditions which produce sharp discontinuities in edaphic features and generate edaphic endemics (Rajakaruna et al. 2003; Harris and Rajakaruna 2009) because closely related taxa become distinguished by their distinct edaphic tolerances (Rajakaruna 2004).

Physical and more importantly chemical properties of the soil may be a source of differentiation between populations pertaining to the same species and which adapt to different habitats, a situation which can further result into sympatric speciation (Kruckeberg 1986; Hardy and Senterre 2007; Campbell and Reece 2007).

Examples of edaphic ecotypes have been reported by many authors and several approaches were developed worldwide to investigate the degree of ecotypic differentiation by evaluating germination and/or growth patterns of seeds and seedlings placed in different habitats (O’Reilly et al. 1985; Heywood and Levin 1985; Wang and McDonald 1992; Van Rossum et al. 2003; Dawson et al. 2007; Schechter and Bruns 2008; Dechamps et al. 2011) A consequence of edaphic heterogeneity is that habitats differ in terms of nutrient availability and other ecological features (pH, temperature, moisture, etc.) and these environmental differences might result in variable selection pressures which can cause edaphic ecotypes to arise from different edaphic conditions (Wang and McDonald 1992).

FACULTE DES SCIENCES Département de Biologie des Organismes