Biodiversity and Biomass of Algae in the Okavango Delta

420 Pages·2014·9.22 MB·English

Biodiversity and Biomass of Algae
in the Okavango Delta (Botswana),
a Subtropical Flood-Pulsed Wetland

Thesis submitted for the degree of
Doctor of Philosophy

by

LUCA MARAZZI

University College London

Department of Geography
University College London
December 2014
I, LUCA MARAZZI, confirm that the work presented in this thesis is my own.
Where information has been derived from other sources, I confirm that this has been
indicated in the thesis.

LUCA MARAZZI

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ABSTRACT

In freshwater bodies algae provide key ecosystem services such as food and water
purification. This is the first systematic assessment of biodiversity, biomass and
distribution patterns of these aquatic primary producers in the Okavango Delta
(Botswana), a subtropical flood-pulsed wetland in semiarid Southern Africa.
This study delivers the first estimate of algal species and genera richness at the

Delta scale; 496 species and 173 genera were observed in 132 samples. A new
variety of desmid (Chlorophyta) was discovered, Cosmarium pseudosulcatum var.
okavangicum, and species richness estimators suggest that a further few hundred
unidentified species likely live in this wetland. Rare species represent 81% of
species richness and 30% of total algal biovolume. Species composition is most
similar within habitat types, thus varying more significantly at the Delta scale.
In seasonally inundated floodplains, algal species / genera richness and diversity are
significantly higher than in permanently flooded open water habitats. The annual
flood pulse has historically allowed more diverse algal communities to develop and
persist in these shallower and warmer environments with higher mean nutrient
levels and more substrata and more heterogenous habitats for benthic taxa. These
results support the Intermediate Disturbance Hypothesis, Species-Energy Theory
and Habitat Heterogeneity Diversity hypotheses. Higher algal biodiversity supports
higher algal biomass in the floodplains, where species form three-dimensional
communities of attached and periphytic algae requiring more nutrients than
phytoplankton assemblages. Multivariate analyses demonstrate that habitat type,
flooding frequency and conductivity most importantly influence the relative
abundance of algal species, genera and phyla in the Okavango Delta.
This study’s findings highlight how the preservation of water level fluctuations and
habitat heterogeneity is crucial to maintaining biodiverse and thus resilient food
webs in this unique ecosystem which faces increasing anthropogenic threats, such
as global warming and upstream water abstraction plans.
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Acknowledgments

I wish to thank Anson W. Mackay, my Principal Supervisor, for giving me the great
opportunity of undertaking this Ph.D. and for constantly advising me throughout my
research; Vivienne Jones, my Subsidiary Supervisor for her constructive criticism
and suggestions and Sophie des Clers and Lars Ramberg who co-supervised me in
the early-mid phases of the project for their advice and encouragements. I gratefully
acknoweldge my colleague Nqobizitha Siziba who collected numerous samples of
algae during the periods when I could not be in Botswana (July and October 2009);
Ponde Kauheva, Richard Mazebedi, Thomas Davidson, Ewan Shilland, Ben
Goldsmith and the Okavango Research Institute staff for their work during the
sampling campaigns and UCL laboratory staff for support on microscope work. My
thanks also go to: the Royal Geographical Society, the UCL Geography Department
and Graduate School and the UK DEFRA Darwin Initiative for funding fieldtrips to
the Delta in April/May 2009 and February/March 2010; Barbara Leoni and Letizia
Garibaldi (University of Milano Bicocca) for organizing the introductory course on
phytoplankton identification in February 2009; Brian Whitton and David John for
organizing the advanced course on phytoplankton identification in July 2011 and
for their interest in my research; David Williamson and Chris Carter for providing
me with very useful drawings and pictures of desmids from our samples. I also want
to thank: Responding To Climate Change, Mouseion Limited, Campbell Harris
Tutors, Greater London Tutors and my A-level and GCSE students and their parents
as well as UCL staff members for providing me with work experiences to self-fund
my Ph.D.; Jan Axmacher and Gina Clarke for advice on diversity data analyses and
phytoplankton microscopy. I thank my colleagues Victoria Shepherd and Matt
Owen for very useful discussions on my work and other colleague-friends for
having shared tips, joys and frustrations during our respective Ph.D. adventures,
especially in the good old days in the microscope-room. Last, but definitely not
least, I wish to thank all my family - Carlo, Angela, Sara, Alba, Valter, Lisa,
Giorgio, Anna - and my fiancée Efe for the great support they have been giving me
throughout these years. This Thesis is dedicated to my grandparents Luciano,
Giorgio and Olga and my great-aunt Paola who are always in my heart.

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Table of contents

List of figures..................................................................................................................8
List of tables..................................................................................................................12
GLOSSARY OF KEY TERMS AND ABBREVIATIONS.......................................14

CHAPTER 1 – WETLANDS AND ALGAE
1.1. OVERVIEW OF THE THESIS...........................................................................17
1.2. WETLANDS..........................................................................................................18
1.2.1. Wetland environment............................................................................................20
1.2.2. Ecosystem services and economic value................................................................20
1.2.3. Threats and conservation........................................................................................21
1.2.4. Flood-pulsed wetlands.............................................................................................23
1.2.5. Subtropical wetlands...............................................................................................25
1.3. MAIN FEATURES OF ALGAE..........................................................................29
1.3.1. Morphology and definitions................................................................................29
1.3.2. Algal cell structure, life and reproduction strategies.........................................31
1.3.3. The role of algae in aquatic food webs...................................................................33
1.3.4. Algae as providers of ecosystem services...............................................................35
1.4. BIOGEOCHEMICAL CYCLES: THE ROLE OF ALGAE............................41
1.5. ENVIRONMENTAL DRIVERS OF ALGAL DISTRIBUTION.....................43
1.5.1. Geography and space...............................................................................................43
1.5.2. Limnology............................................................................................................44
1.5.3. Seasonality and flood-pulse.................................................................................46
1.5.4. Habitat structure.................................................................................................47
1.6. THEORETICAL FRAMEWORK FOR THE THESIS....................................49
1.6.1. Intermediate Disturbance Hypothesis (IDH).........................................................50
1.6.2. Resource Competition Theory (RCT)....................................................................53
1.6.3. Species-Energy Theory (SET).................................................................................55
1.6.4. Habitat Heterogeneity Hypothesis (HHH).............................................................56

CHAPTER 2 – STUDY REGION: THE OKAVANGO DELTA
2.1. THE OKAVANGO RIVER BASIN.....................................................................57
2.1.1. Geography and climate.......................................................................................58
2.1.2. Socio-economic aspects.......................................................................................60
2.1.3. Threats................................................................................................................61
2.1.4. Scenarios.............................................................................................................62
2.2. THE OKAVANGO DELTA.................................................................................64
2.2.1. Geology, topography and soil.............................................................................65
2.2.2. Climate and hydrology.......................................................................................66
2.2.3. Water chemistry and quality..................................................................................69
2.2.4. Hydroecology......................................................................................................70
2.2.5. Biodiversity.........................................................................................................72
2.2.6. Ecosystem services and socio-economic aspects.................................................75
2.3. AIM, RESEARCH QUESTIONS AND OBJECTIVES....................................78

CHAPTER 3– STUDY SITE, FIELD AND LABORATORY METHODS
3.1. STUDY SITES AND SAMPLING CAMPAIGNS.............................................84
3.1.1. Habitat classifications.........................................................................................97
3.2. SAMPLING OF ALGAE......................................................................................99
3.3. ALGAL ANALYSES...........................................................................................100
3.3.1. Sub-sample preparation...................................................................................101
3.3.2. Counting technique and strategies...................................................................103
3.3.3. Identification of algae.......................................................................................104
3.3.4. Algal traits..............................................................................................................104
3.4. ESTIMATION OF ALGAL BIOVOLUME.....................................................104
3.5. LIMNOLOGICAL VARIABLES......................................................................112
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3.6. PARAMETRIC AND NON PARAMETRIC STATISTICAL TESTS...........116
3.7. DIVERSITY MEASURES..................................................................................116
3.8. UNIVARIATE AND MULTIVARIATE STATISTICAL ANALYSES.........123

CHAPTER 4 - ALGAL FLORA AND LIMNOLOGY OF THE OKAVANGO
DELTA
4.1. PREVIOUS RESEARCH IN THE DELTA......................................................131
4.2. AIMS AND RATIONALE..................................................................................134
4.3. RESULTS: ALGAL COUNTS...........................................................................135
4.4. RESULTS: ABUNDANT AND RARE TAXA..................................................140
4.5. RESULTS: ALGAL FLORAS IN THE OKAVANGO REGION..................143
4.6. RESULTS: ALGAL TRAITS..........................................................................144
4.6.1. Cell arrangement....................................................................................................145
4.6.2. Cell length................................................................................................................145
4.6.3. Motility....................................................................................................................147
4.6.4. Metabolic traits.......................................................................................................147
4.7. RESULTS: LIMNOLOGICAL VARIABLES.................................................149
4.7.1. Correlations between limnological variables.......................................................150
4.7.2. PCA: environmental gradients in the Delta.........................................................154
4.7.3. Statistical tests on variables measured in both campaigns.................................159
4.7.4. Statistical tests on variables measured only in Campaign 1...............................175
4.7.5. Statistical tests on variables measured only in Campaign 2...............................180
4.8. DISCUSSION.......................................................................................................182
4.8.1 Algal counts and floras........................................................................................182
4.8.2. Algal traits...............................................................................................................190
4.8.3. Limnology of the Okavango Delta.....................................................................192
4.9. SUMMARY..........................................................................................................197

CHAPTER 5 – ALGAL BIODIVERSITY AND BIOMASS PATTERNS
AND CONTROLS
5.1.INTRODUCTION................................................................................................198
5.1.1. Taxon richness and diversity of algae...................................................................198
5.1.2. Factors determining biodiversity of algae............................................................200
5.1.3. Total algal biovolume and its controls..................................................................201
5.1.4. Species richness - biovolume relationship............................................................213
5.2. RESULTS....................................................................................................................207
5.2.1. Species and genera richness..................................................................................207
5.2.2. Diversity indices......................................................................................................220
5.2.3. Taxon richness estimators.................................................................................228
5.2.4. β-diversity and species composition similarity..................................................230
5.2.5. Total algal biovolume.............................................................................................236
5.2.6. Algal species richness - biovolume relationship..................................................248
5.3. DISCUSSION.......................................................................................................258
5.3.1. Interpretation of algal taxon richness and diversity...........................................259
5.3.2. Interpretation of algal biovolume patterns..........................................................277
5.3.3. Interpretation of the the species richness - biovolume relationship..................286
5.4. SUMMARY..........................................................................................................293

CHAPTER 6 – ENVIRONMENTAL CONTROLS OF ALGAL TAXON
DISTRIBUTION IN THE DELTA
6.1. INTRODUCTION........................................................................................................294
6.1.1. Factors influencing the distribution of algae........................................................295
6.1.2. Chapter aims............................................................................................................296
6.2. RESULTS.............................................................................................................299
6.2.1. Limnological controls of algal phyla species richness and biovolume...............299
6.2.2. RDA: environmental controls of algal taxon distribution..................................304
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6.2.3. VPA results: environment and spatial location...................................................310
6.2.4. Species Response Curves........................................................................................313
6.3. DISCUSSION.......................................................................................................323
6.3.1. Environmental controls of species richness and total biovolume.......................323
6.3.2. Environmental controls of the distribution of algae in the Delta.......................328
6.3.3. Individual algal taxon responses to limnological conditions...............................330
6.4. SUMMARY..........................................................................................................333

CHAPTER 7 – CONCLUSIONS..............................................................................334

REFERENCES...........................................................................................................343

APPENDIX A. Descriptions of algal phyla...........................................................................387
APPENDIX B. Full list of the algal species observed in the Okavango Delta...................398
APPENDIX C. List of algal genera observed not included in the species list....................409
APPENDIX D. Site numbers displayed in boxplots in chapters 4 and 5............................412
APPENDIX E1. Micrographs of algal species observed in the Okavango Delta...............413
APPENDIX E2. Micrographs of algal species observed in the Okavango Delta...............414
APPENDIX F. List of common taxa to different algal studies in the Okavango Delta....415
APPENDIX G. List of additional species and varieties identified by David
Williamson in a subset of samples from Campaign 2................................420
APPENDIX H. Marazzi, L. (2013): Okavango Delta - Biodiversity of
Microalgae, precious invisible plants...........................................................421
APPENDIX I. Williamson D.B. and Marazzi L.. 2013. A new Cosmarium
(Chlorophyta, Desmidiaceae) variety from the
Okavango Delta, Botswana..........................................................................424

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List of figures

Figure 1.1. Global wetlands map................................................................................................19
Figure 1.2. Five major threat categories and their interactive impacts on freshwater
biodiversity...............................................................................................................22
Figure 1.3. Scheme of the flood pulse concept with five snapshots of an annual
hydrological cycle.....................................................................................................24
Figure 1.4. Seasons of the Inter-Tropical Convergence Zone (ITCZ) in January and July on
map of major wetlands of the world.........................................................................26
Figure 1.5. Conceptual scheme of the role of algae in food webs..............................................34
Figure 1.6. Framework for integrated assessment and valuation of ecosystem functions,
goods and services.....................................................................................................37
Figure 1.7. Schematic representation of the Intermediate Disturbance Hypothesis....................50
Figure 1.8. Conceptual model of the interaction between resource supply and biofilm
composition in two hypothetical 3D communities growing on inert substrates
under high (community A) and low (community B) resource supply......................53

Figure 2.1. Map of the Okavango River Basin............................................................................58
Figure 2.2. Map of the Okavango Delta at high flood (28th July 2009) and low flood
(10th February 2010)..................................................................................................67
Figure 2.3. Map of the Okavango Delta channels.......................................................................68
Figure 2.4. Monthly and annual average discharge measured at Mohembo...............................68
Figure 2.5. Main biogeochemical processes in water and islands in the Delta...........................69
Figure 2.6. Diagram of the relationship between topography and vegetation classes in the
Delta..........................................................................................................................71
Figure 2.7. Different vegetation types in three sites: a) Okavango river in the
Panhandle; b) lagoon in Boro and c) occasionally flooded floodplain in
Santantadibe.............................................................................................................73
Figure 2.8. Outline of the Thesis results chapters.......................................................................83

Figure 3.1. Map of the sampling sites and regions in the Okavango Delta.................................85
Figure 3.2. Water discharge at Mohembo, Northern Panhandle, in the years of sampling.........85
Figure 3.3. Map of the Okavango Delta showing the location of sampling points
in Campaign 2...........................................................................................................88
Figure 3.4. a) Field assistant Ponde Kauheva sampling from a canoe in
an occasionally flooded floodplain in Boro; b) Nqobizitha Siziba
and myself filtering a composite sample for zooplankton analysis.......................100
Figure 3.5. Sedimentation chambers: 5, 10, 15 mL...................................................................101
Figure 3.6. Examples of HOF models for a pH gradient...........................................................130

Figure 4.1. Number of algal units counted in all the samples...................................................135
Figure 4.2. Percentage of algal units per phyla in the two datasets...........................................138
Figure 4.3. Accumulation curve of genera and species identified in the samples analysed......140
Figure 4.4. The 20 most abundant algal taxa / groups observed in this study...........................141
Figure 4.5. Number of species and genera in relation to their occurrence frequency...............142
Figure 4.6. Number of algal species, genera and other taxonomic groups found in each
occurrence frequency class......................................................................................142
Figure 4.7. Frequency of algal cell arrangement types across: a) regions;
b) flood classes; c) habitats.....................................................................................145
Figure 4.8. Frequency of average cell length classes across: a) regions; b) flood classes;
c) habitats...............................................................................................................146
Figure 4.9. Frequency of motility traits across: a) regions; b) flood classes; c) habitats..........147
Figure 4.10. Frequency of metabolic traits across: a) regions; b) flood classes; c) habitats.....148
Figure 4.11. Screeplot of PCA axes (red) and broken stick (black) axes in all the samples.....155
Figure 4.12. Screeplot of PCA axes (red) and broken stick (black) axes in Campaign 1.........156
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Figure 4.13. PCA biplot of environmental variables in Campaign 1........................................157
Figure 4.14. Screeplot of PCA axes (red) and broken stick (black) axes in Campaign 2.........158
Figure 4.15. PCA biplot of environmental variables in Campaign 2........................................158
Figure 4.16. Water temperatures across regions in a) Campaign 1; b) all the samples.............162
Figure 4.17. Water temperature across seasons in a) Campaign 1; b) Campaign 2;
c) all the samples...................................................................................................163
Figure 4.18. Water temperature across flood classes in all the samples...................................163
Figure 4.19. Water temperature across habitats in all the samples...........................................164
Figure 4.20. Water depth across regions in a) Campaign 1 and 2) all the samples...................164
Figure 4.21. Water depth across flood classes in a) Campaign 1 and b) all the samples..........165
Figure 4.22. Water depth across seasons in all the samples......................................................165
Figure 4.23. Water depth across habitats in all the samples......................................................166
Figure 4.24. Conductivity across regions in a) Campaign 1; b) Campaign 2; c) all the
samples..................................................................................................................167
Figure 4.25. Conductivity across flood classes in a) Campaign 1; b) all the samples..............168
Figure 4.26. Conductivity across seasons in all the samples....................................................168
Figure 4.27. Conductivity across habitats in a) Campaign 1; b) all the samples......................169
Figure 4.28. Conductivity across floodplain types in a) Campaign 1; b) all the samples.........169
Figure 4.29. Dissolved Oxygen across regions in a) Campaign 1; b) all the samples..............170
Figure 4.30. Dissolved Oxygen across flood classes: a) Campaign 1;
b) Campaign 2; c) all the samples........................................................................170
Figure 4.31. Dissolved Oxygen across seasons in a) Campaign 2; b) all the samples..............171
Figure 4.32. Dissolved Oxygen across habitats in all the samples............................................172
Figure 4.33. Dissolved Oxygen across floodplain types in all the samples..............................172
Figure 4.34. pH across regions in a) Campaign 1; b) all the samples.......................................173
Figure 4.35. pH across seasons in Campaign 1.........................................................................173
Figure 4.36. pH in across flood classes in all the samples........................................................174
Figure 4.37. pH across floodplain types in all the samples.......................................................174
Figure 4.38. Total Phosphorus across seasons in Campaign 2..................................................175
Figure 4.39. Dissolved Organic Carbon across regions in Campaign 1....................................176
Figure 4.40. Dissolved Organic Carbon across flood classes in Campaign 1...........................176
Figure 4.41. SiO across regions in Campaign 1.......................................................................177
2
Figure 4.42. SiO across flood classes in Campaign 1..............................................................177
2
Figure 4.43. Cations across regions in Campaign 1..................................................................178
Figure 4.44. Anions across regions in Campaign 1...................................................................178
Figure 4.45. Cations across seasons in Campaign 1..................................................................178
Figure 4.46. Cations across flood classes in Campaign 1.........................................................179
Figure 4.47. Chlorophyll a across within-floodplain habitats in Campaign 2..........................180
Figure 4.48. Turbidity across flood classes in Campaign 2......................................................181
Figure 4.49. Turbidity across floodplain types..........................................................................181
Figure 4.50. Micrographs of some of the common species of diatoms observed
in the Delta............................................................................................................186
Figure 4.51. Micrographs of some of the common species of green algae and
of one Cryptophyta genus observed in the Delta...................................................187

Figure 5.1. Species (a) and genera (b) richness across seasons in Campaign 2........................208
Figure 5.2. Species richness across flood years in all the samples............................................209
Figure 5.3. Species (a) and genera richness (b) across habitats in Campaign 2........................210
Figure 5.4. Species (a) and genera (b) richness across regions in all the samples....................210
Figure 5.5. Species (a) and genera (b) richness across flood classes in all the samples...........211
Figure 5.6. Species (a) and genera richness (b) across seasons in all the samples....................211
Figure 5.7. Species (a) and genera richness (b) across habitats in all the samples...................212
Figure 5.8. Species richness of algal phyla across regions.......................................................213
Figure 5.9. Species richness of: a) Bacillariophyta, b) Chlorophyta across regions.................214
Figure 5.10. Species richness of algal phyla across seasons in all the samples........................214
Figure 5.11. Species richness of: a) Bacillariophyta, b) Chlorophyta across seasons..............215
Figure 5.12. Species richness of algal phyla across flood years...............................................217
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Figure 5.13. Species richness of algal phyla across flood classes............................................217
Figure 5.14. Species richness of: a) Bacillariophyta, b) Chlorophyta across flood classes......218
Figure 5.15. Species richness of Euglenophyta across floodplain types...................................218
Figure 5.16. Species richness of algal phyla across habitats.....................................................219
Figure 5.17. Species richness of: a) Bacillariophyta, b) Chlorophyta across habitats..............219
Figure 5.18. Shannon Diversity for a) species and b) genera across regions............................220
Figure 5.19. Shannon Evenness for a) species and b) genera across regions............................221
Figure 5.20. Shannon Diversity for a) species and b) genera across flood classes...................221
Figure 5.21. Shannon Evenness for a) species and b) genera across flood classes...................222
Figure 5.22. Shannon Diversity for a) species; b) genera across seasons.................................222
Figure 5.23. Shannon Diversity for species across flood years.................................................223
Figure 5.24. Shannon Evenness for a) species; b) genera across seasons.................................223
Figure 5.25. Shannon Evenness for species across flood years................................................224
Figure 5.26. a) Shannon Diversity and b) Shannon Evenness for species across habitats........225
Figure 5.27. Shannon Diversity for species across within-floodplain habitats.........................227
Figure 5.28. Average number of species identified and not found across regions....................229
Figure 5.29. Average number of genera identified and not found across regions.....................230
Figure 5.30. β-diversity within a) region, b) flood class, c) habitat and d) season...................231
Figure 5.31. Mean number of shared species and similarity (Bray-Curtis distance)
between samples in the same region.....................................................................233
Figure 5.32. Mean number of shared species and similarity (Bray-Curtis distance)
between samples in different regions....................................................................233
Figure 5.33. Mean number of shared species and similarity (Bray-Curtis distance)
between samples in the same flood class..............................................................234
Figure 5.34. Mean number of shared species and similarity (Bray-Curtis distance)
between samples in different flood classes...........................................................234
Figure 5.35. Mean number of shared species and similarity (Bray-Curtis distance)
between samples in the same habitat.....................................................................235
Figure 5.36. Mean number of shared species and similarity (Bray-Curtis distance)
between samples in different habitats....................................................................235
Figure 5.37. Total biovolume across regions in Campaign 1....................................................237
Figure 5.38. Total biovolume across habitats in Campaign 2...................................................238
Figure 5.39. Total biovolume across within-floodplain habitats in Campaign 2......................238
Figure 5.40. Total biovolume across regions in all the samples...............................................239
Figure 5.41. Total biovolume across habitats in all the samples...............................................240
Figure 5.42. Total biovolume of a) Bacillariophyta; b) Chlorophyta; c) Cyanophya;
d) Euglenophyta and e) Xanthophyta across regions............................................243
Figure 5.43. Total biovolume across seasons in all the samples...............................................244
Figure 5.44. Biovolume of a) Bacillariophyta; b) Chrysophyta; c) Cyanophyta;
d) Euglenophyta; e) Xanthophyta across seasons.................................................245
Figure 5.45. Biovolume of a) Bacillariophyta; b) Chlorophyta; c) Cyanophyta;
d) Euglenophyta; e) Xanthophyta across flood classes........................................247
Figure 5.46. Biovolume of a) Bacillariophyta; b) Chlorophyta; c) Cyanophyta across
habitats...................................................................................................................248
Figure 5.47. Total biovolume vs species richness in all the samples........................................249
Figure 5.48. Total biovolume vs species richness in XAK.......................................................250
Figure 5.49. Total biovolume vs species richness across regions.............................................251
Figure 5.50. Total biovolume vs species richness across flood classes....................................252
Figure 5.51. Total biovolume vs species richness in Apr/May.................................................252
Figure 5.52. Total biovolume vs species richness across seasons.............................................253
Figure 5.53. Total biovolume vs species richness across all habitats........................................254
Figure 5.54. Total biovolume vs species richness in a) OW and b) MV habitats.....................254
Figure 5.55. Total biovolume vs species richness in floodplains in Campaign 2.....................256
Figure 5.56. Biovolume vs species richness of: a) Bacillariophyta and b) Chlorophyta..........257

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