interactions among freshwater macrophytes and …...interactions among freshwater macrophytes and...
TRANSCRIPT
Interactions among freshwater macrophytes and
physical-chemical-biological processes in Lake Chini,
Malaysia
Zati Sharip,
B. Chem. Eng. (Hons.) & M.Sc.
Universiti Teknologi Malaysia
This thesis is submitted in fulfilments of the requirement for the degree of
Doctor of Philosophy of The University of Western Australia
School of Environmental Systems Engineering
School of Plant Biology
December 2011
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Abstract
Aquatic vascular plants that grow within the littoral and pelagic environment are an
important element of shallow lake and wetland ecosystems. Alteration of the natural
environment, mostly human-induced, is rapidly changing the natural ecological
processes and altering biotic factors including aquatic plant community composition in
wetlands all over the world. This thesis examined the macrophyte communities in Lake
Chini, a shallow floodplain wetland in Malaysia: specifically how physical-chemical and
biological processes were related to plant community dynamics and changes of
macrophyte dominance, from the native floating-leaved species (Nelumbo nucifera) to
non-native submerged macrophytes (Cabomba furcata).
Whole-lake vegetation surveys and statistical models were used to analyse
spatially and temporally the macrophyte community composition and the environmental
variables that influence their structure. The lake can be divided into distinct quasi-
independent sub-basins. Temperature and dissolved oxygen measurements were
conducted in benthic chambers and free water at two separate sub-basins and
mathematical calculations were employed to describe (1) the influence of convective
circulation, driven by horizontal temperature gradient and thermal structure on the
nutrient transport in the system, and (2) oxygen dynamics and differences in primary
production among habitat and macrophyte communities.
Overall, this study found that the macrophyte community in Lake Chini is highly
dynamic with possible alternate states dominated by floating-leaved and submerged
species. The flood regime has a strong effect in controlling the variation in plant
community dominance. Spatial variation in plant community composition was influenced
by total depth, nutrient concentration and substrate. C. furcata appears adapted to
annual floods, and its invasion affected the diversity and plant community composition in
this wetland.
Additionally, both floating-leaved and submerged vegetation contributed to thermal
structure and water exchange dynamics in the system. Weak density-driven flow was
induced by the differential temperature gradient between the open water and the littoral
areas dominated by floating-leaved plants. Additionally, depth variation between the near
littoral zone and the open pelagic region induced physical circulation that could improve
nutrient delivery to the submerged C. furcata bed. In addition to the effects of the
macrophyte, lake physical characteristics such as shape and surrounding topography
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influenced the variation of thermal stratification and mixing dynamics between the lake
segments at different water levels.
Oxygen dynamics differed between the two plant communities. Gross primary
production rates and biomass accumulation were higher in C. furcata sites and
ecosystem production contributed to increased carbon fixation in the system. High
consumption of DO by sediment communities and microflora associated with C. furcata
beds increased respiratory activities. An increase in abundance of the invasive
submergent C. furcata throughout the pelagic zone affected net ecosystem production
and biomass accumulation. The potential for shifts in macrophyte dominance from
floating-leaved to submergent species has important implications for the overall
dynamics of the lake.
v
Statement of originality
The research presented in this thesis is an original contribution to the field of limnology,
invasion and vegetation ecology. I hereby declare that all materials presented in this
thesis are original except where due acknowledgement has been given, and have not
been submitted for the award of any other degree or diploma. The body of this thesis
(Chapter 2-4) is presented as a series of papers for journal publication, and some
repetition of the literature review, details of study area and methodology have therefore
been necessary. As the author of all material within this thesis, I am completely
responsible for all data analysis and mathematical calculation, presentation and written
text contained herein. In addition, I performed all vegetation surveys, field
experimentation and secondary data collection.
My supervisors have been included as authors as they provided supervision and
reviewed all manuscripts preparation. The first manuscript has been reviewed and
revised, so the material presented herein incorporates some of the reviewers‟
suggestions. Shon Schooler also contributed in the conceptual design of the vegetation
survey and participated in the first fieldwork in September 2009. Justin Brookes from
University of Adelaide contributed in the configuration, calibration and deployment of
the benthic chamber experiments in April 2010. Matthew Hipsey also contributed in the
calibration of sensors and participated in the field experiments in April 2010.
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Acknowledgements
In the name of Allah the most gracious the most merciful. All praise is due to Allah for
giving me the inspiration to start this PhD journey and providing His blessings and
guidance by bestowing all the strength that I need to persevere and finish this thesis.
First and foremost, I am grateful to Malaysian Ministry of Natural Resources (MoNRE)
and Environment and Public Service Department of Malaysia for providing me the
opportunity to do this PhD through the MoNRE PhD and Masters Program Scholarship.
I would like to thank National Hydraulic Research Institute of Malaysia (NAHRIM) for
their full support and funding for all my fieldworks. Thanks to NAHRIM for permitting me
to use their data.
I would like to thank Dr. Shon Schooler, Dr. Matt Hipsey and Prof. Richard Hobbs for
their willingness to accept me as their student and continuously supported me by
reviewing all my work. It was a privilege to learn from experts in their respective fields
and to be able to reconcile both worlds of limnology and ecology. I sincerely appreciate
their trust in me by allowing me a large degree of freedom to define and undertake my
research. I thank Dr. Shon Schooler, who not only provided valuable supervision but
gave me the first insight on invasive species and provided indispensable suggestion
concerning the biological analysis and statistical validity of my research work. I thank
Dr. Matthew Hipsey and Prof. Richard Hobbs, who not only served as coordinating
supervisors and managing my academic supervision arrangements but provided
invaluable guidance and direction on my thesis.
I would like to acknowledge the continuous and unconditional support, love and prayers
I received from my dad and mum, Sharip Mamat and Tejah Husop. Thank you for
providing the moral support and taught me about faith, patience and perseverance
during the difficult periods of my candidature. Thanks to my sister for being a constant
reader of my work. Also thanks to my brother for all his help.
I am grateful to Ir. Dr Salmah Zakaria who has encouraged, inspired and given me the
opportunity to continue my PhD. Also thanks to Juhaimi Jusoh for his personal support
and Ir. Ahmad Jamalluddin Shaaban who has continuously supported my work.
viii
I would like to thank the Economic Planning Unit, Prime Minister‟s Department of
Malaysia and Pahang State Government for providing me the permission to conduct
this research in Lake Chini, Malaysia.
I want to acknowledge the technical support team of National Hydraulic Research
Institute of Malaysia, particularly Ahmad Taqiyuddin Ahmad Zaki for all his coordination
and assistances in the field. Also, the personal effort, in relation to field data collection,
by Shon Schooler, Matthew Hipsey, Juhaimi Jusoh, Justin Brookes, Brendan Busch,
Bashirah Mohd Fazli, Fadhil Mohd Kassim, Farhan, Ab Hadi, Haffiz and Jeyaprakash is
highly appreciated.
I am grateful to Prof. Marti J. Anderson for her statistical advise and Prof. Bob Clarke &
Ray Gorley for providing the multivariate statistic workshop using PRIMER-
PERMANOVA which forms the analysis for the first paper. I thank Dr. Joanne
Edmonston and Dr. Krystyna Haq for their invaluable feedback on the academic writing
of the introduction and conclusion chapters.
I am thankful for many useful discussions with Sutomo, Revalin Herdianto, Zhenlin
Zhang, and Ana Ruibal regarding various statistical analysis and MATLAB simulation.
Thanks to all those students whom I shared office, and for their friendship and
interesting conversation. Thanks also go to the Centre for Ecohydrology for the
administration of my study. Special thanks to Ecological Restoration and Intervention
Ecology Group (ERIE) led by Prof. Richard Hobbs for all the interesting discussion and
presentation on the research and management challenges in dealing with restoration
ecology and invasive species. Appreciation also goes to every individual, who has
helped and supported me, either through provision of papers, data and ideas.
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Dedication
This work is dedicated to my dad and mum, Sharip Mamat and Tejah Husop, whose
trust, love and support throughout the years have been unbounded.
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Preface
The main body of this thesis is comprised of three chapters, (Chapter 2-5) each of
which is a paper written with the intention to be suitable for publication in peer-reviewed
scientific journals. Each chapter is a stand-alone manuscript, which includes abstract,
independent introduction, literature review, methods, results, discussions and
conclusions sections. In addition, each chapter is independently referenced to
acknowledge the contributions of previous related works. Each paper is presented with
the original internal headings, figures and tables however, for ease of reading and flow,
the formatting in the thesis is uniform. Headings, figures and tables are numbered in
the thesis style.
The introductory Chapter 1 presents the motivation, background and scope of the study
and links the individual publications.
Chapter 2 has been published in Biological Invasion as
Sharip, Z., Schooler, S.S, Hipsey, M.R. and Hobbs, R.J. (2011) „Eutrophication,
agriculture and water level control shift aquatic plants in Lake Chini, Malaysia‟,
Biological Invasions. DOI: 10.1007/s10530-011-0137-1
Chapter 3 is the expanded version of the paper that has been accepted for oral
presentation at the Lake Sustainability Conference 2010 and has been accepted for
publication in International Journal of Design, Nature, and Ecodynamics under the title
„Physical circulation and spatial exchange dynamics in a shallow floodplain wetland‟.
Appendix 2 provided the abridged version of Chapter 3 that has been peer-reviewed
and presented at Lake Sustainability Conference 2010 with the appendix is formatted
according to the original final proof.
Chapter 4 will be submitted for publication in Hydrobiologia under the title „Metabolism
differences among habitat and macrophyte communities in a tropical lake’
The major outcomes of this work are summarized and discussed in Chapter 5, which
include recommendation for future works.
The material presented in this thesis is a synthesis of my own ideas and the work
undertaken by myself in consultation with my supervisors Dr. Shon S. Schooler, Dr.
Matthew R. Hipsey and Prof. Richard J. Hobbs.
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Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
xiii
Contents
Abstract .................................................................................................................. iii
Statement of originality .......................................................................................... v
Acknowledgements .............................................................................................. vii
Dedication .............................................................................................................. ix
Preface ................................................................................................................... xi
Contents ............................................................................................................... xiii
Chapter 1 - Introduction ......................................................................................... 1
1.1 Background and motivation ................................................................................... 1
1.2 Lake Chini, Malaysia .............................................................................................. 6
1.3 Research objectives and approach ...................................................................... 7
1.4 Logistical considerations ........................................................................................ 9
1.5 Thesis outline ........................................................................................................10
Chapter 2 - Eutrophication, agriculture and water level control shift aquatic plant
communities from floating-leaved to submerged macrophytes in Lake Chini,
Malaysia ................................................................................................................ 11
2.1 Abstract ..................................................................................................................11
2.2 Introduction ............................................................................................................12
2.2.1 Study Area ...........................................................................................................13
2.2.2 Study organisms .................................................................................................15
2.3 Methods and materials .........................................................................................16
2.3.1 Overview ..............................................................................................................16
2.3.2 Plant community sampling ................................................................................16
2.3.3 Environmental variables ....................................................................................17
2.3.4 Statistical Analysis..............................................................................................17
2.4 Results ....................................................................................................................19
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
xiv
2.4.1 Catchment and hydrological changes............................................................. 19
2.4.2 Spatial distribution of aquatic plants ............................................................... 20
2.4.3 Environmental variables potentially influencing macrophyte distribution .. 26
2.5 Discussion ............................................................................................................. 29
2.6 Acknowledgement ................................................................................................ 34
Chapter 3 – Physical circulation and spatial exchange dynamics in a shallow
floodplain wetland ................................................................................................36
3.1 Abstract .................................................................................................................. 36
3.2 Introduction ............................................................................................................ 37
3.3 Methods ................................................................................................................. 38
3.3.1 Study site ............................................................................................................. 38
3.3.2 Field measurements .......................................................................................... 39
3.3.3 Analysis of physico-chemical structure and heat budgets calculation ....... 41
3.4 Results ................................................................................................................... 43
3.4.1 Meteorology and physical-chemical structure ............................................... 43
3.4.2 Heat budget and water exchange ................................................................... 51
3.5 Discussion ............................................................................................................. 54
3.5.1 Temperature structure and water exchange .................................................. 54
3.5.2 Implications of physical-chemical coupling to macrophyte dynamics ........ 57
3.6 Conclusion ............................................................................................................. 58
3.7 Acknowledgements .............................................................................................. 58
Chapter 4 – Metabolism differences among habitat and macrophyte communities
in a tropical lake ....................................................................................................59
4.1 Abstract .................................................................................................................. 59
4.2 Introduction ............................................................................................................ 60
4.3 Methods and materials ........................................................................................ 62
4.3.1 Experimental design and water quality measurements ......................... 62
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
xv
4.3.2 Benthic metabolism (specific processes, small scale) ...........................63
4.3.2.1 Benthic chamber deployments ...............................................................63
4.3.2.2 Estimates of diurnal productivity ............................................................63
4.3.2.3 Estimates of MPB respiration and production ......................................63
4.3.3 Net ecosystem metabolism .........................................................................64
4.3.3.1 Diel oxygen measurements ....................................................................64
4.3.3.2 Estimates of free water metabolism ......................................................64
4.3.4 Data analysis .................................................................................................65
4.4 Results ....................................................................................................................65
4.4.1 Oxygen fluxes and water quality measurement .......................................65
4.4.2 Diurnal productivity .......................................................................................68
4.4.3 MPB and microflora respiration and production ......................................69
4.4.4 Free water productivity ................................................................................70
4.5 Discussion...................................................................................................................71
4.5.1 Oxygen fluxes and water quality dynamic ................................................71
4.5.2 Diurnal productivity .......................................................................................73
4.5.3 MPB and microflora respiration and production ......................................73
4.5.4 Free water productivity ................................................................................74
4.6 Conclusion .............................................................................................................75
4.7 Acknowledgements ..............................................................................................76
Chapter 5 – General discussion and conclusion ................................................ 77
5.1 Summary of research findings ............................................................................77
5.2 Discussion ..............................................................................................................79
5.3 Implications for wetland and lake management ...............................................82
5.4 Original contributions ............................................................................................84
5.5 Study limitations and recommendations for future work .................................85
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
xvi
5.6 Conclusion ............................................................................................................. 88
References ............................................................................................................89
Appendix 1: Supporting document for Chapter 2 ............................................. 108
Appendix 1a: List of methods for laboratory analysis .............................................. 108
Appendix 1b: Supporting information.......................................................................... 109
Appendix 2: Conference Paper .......................................................................... 112
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
1
Chapter 1 - Introduction
1.1 Background and motivation
Aquatic macrophytes, including submergent, emergent, floating and floating-leaved
species (Cronk and Fennessy 2001; Schulthorpe 1967), not only characterise shallow
floodplain riparian systems, lakes and wetlands but also play a central functional and
structural role in these endangered ecosystems (Jeppesen et al. 1997; Scheffer 2004).
Macrophytes shape aquatic habitats by affecting physico-chemical properties of the
water, metabolic production, biotic interactions and community structures (Jeppesen et
al. 1997). Worldwide, the composition of many of these endangered ecosystems is
rapidly changing as a result of environmental stressors, mostly human-induced, which
have led to the degradation of the natural environment and altered their resilience to
change. These environmental changes make wetlands particularly more vulnerable to
invasive species.
Research in invasion ecology has shown that the expansion of invasive species can be
a product of environmental changes (Didham et al. 2005; MacDougall and Turkington
2005). Naturalised plants start to produce reproductive offspring in large numbers when
certain environmental requirements are met, and if there are no inhibitory factors they
become invasive (Richardson and Pysek 2006). The presence of invasive species in
aquatic systems affects both ecosystem functioning and abiotic-biotic interactions
(Chapin et al. 1997), that eventually alters community structure and ecosystem function
(Didham et al. 2005; Ehrenfeld 2003; Farrer and Goldberg 2009; MacDougall and
Turkington 2005). The invasive species could also provide competitive pressures that
cause a decline in native species abundance and diversity (Hobbs and Huenneke
1992; MacDougall and Turkington 2005; Zedler and Kercher 2004).
A recent review by Ehrenfeld (2010) has also shown that the impacts of certain
invasive species on ecosystem dynamics are complex and involve multiple interacting
pathways and site-to site differences. Increasingly, research shows that modification of
physical environments by invading species leads to their dominance (Crooks 2002;
Cuddington and Hastings 2004; Farrer and Goldberg 2009). A small number of studies
have also shown that invasive species alter biogeochemistry by modifying soil
environments and nutrient pools (Ehrenfeld 2004; Farrer and Goldberg 2009;
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
2
Weidenhamer and Callaway 2010) or accumulating litter (Farrer and Goldberg 2009;
Vaccaro et al. 2009).
Wetlands, are particularly susceptible to invasion (Zedler and Rhea 1997). Being the
low-lying component in any catchment, wetlands become a basin for accumulation of
nutrients and sediment entrained in surface run-off from the surrounding catchment,
which contributes to invasibility by the invaders (Zedler and Kercher 2004). Numerous
studies have reported the factors and processes that affect macrophyte composition
and dominance in wetlands in temperate climates (Baldina et al. 1999; Brinson and
Malvarez 2002; Busch and Smith 1995; Coops and Doef 1996; Lougheed et al. 2001;
Nilsson and Svedmark 2002; Tallis 1983). Most studies have shown that macrophyte
composition and dominance is linked to eutrophication (Egertson et al. 2004;
Gunderson 2001; Lougheed et al. 2008), water level regulation (Catford et al. 2011;
Van Geest et al. 2005; Whyte et al. 2008), drought (Greening and Gerritsen 1987),
water level fluctuations (Baldina et al. 1999; Hudon 1997, 2004; Kunii and Maeda
1982), and thermal pollution (Allen and Gorham 1973; Gallup and Hickman 1975).
Other studies have shown that macrophyte composition and dominance can change as
a result of factors such as sedimentation and fertilizers (Kercher and Zedler 2004),
stabilised water levels and phosphorus addition (Boers and Zedler 2008; Herrick and
Wolf 2005), eutrophication and acidification (Roelofs 1983), and eutrophication and
invasion (Kercher et al. 2007).
Less is known, however, about the driving mechanisms and processes that are able to
cause a shift in macrophyte dominance in wetlands in tropical settings. Invasion by
invasive Mimosa pigra have been reported to affect biodiversity in Kakadu National
Park, Australia as a result of high dispersal rates (Cook et al. 1996; Cowie and Werner
1993). Invasion of African grass has also been reported in a tropical freshwater marsh
in La Mancha, Veracruz, Mexico as a result of the species inherent ability to use water
efficiently and produce high amounts of biomass (Rosas et al. 2005). A few invasive
plant species have also caused serious problems in many rivers, reservoir, lakes and
wetlands in Malaysia including Salvinia molesta (Baki et al. 1991; Mansor 1996),
Eichhornia crassipes, Lemna perpusilla, and Pistia stratiotes (Mansor 1996), Hydrilla
verticillata (Baki 2004), and Mimosa pigra (Mansor and Crawley 2011). Massive growth
of these aquatic weeds has been associated to high nutrient concentrations (Mansor
1996), which occur as a result of agriculture and aquaculture activities (Baki 2004).
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
3
Understanding how ecosystem processes influence macrophytes is complicated by the
fact that macrophytes are highly variable elements within aquatic systems (Carpenter
and Lodge 1986), and differences in site availability, species availability, and species
performance alters vegetation dynamics (Pickett and Cadenasso 2005; Pickett and
McDonnell 1989). The pathways and causal relationships between invasive species
and changes in ecosystem processes and properties, are still poorly understood
(Levine 2003).
Cabomba spp. is one of the macrophytes that have become invasive in many parts of
the world and presents a serious threat to the health of rivers, lakes and wetlands
(Hogsden et al. 2007; Mackey and Swarbrick 1997; Schooler et al. 2009; Wilson et al.
2007; Xiaofeng et al. 2005; Zhang et al. 2003). The ecological impact of the invasion of
this species, if not controlled, includes disruption of navigation and recreational
activities, replacement of native species, reduction of biodiversity and water quality
(Hogsden et al. 2007; Mackey and Swarbrick 1997; Wilson et al. 2007; Zhang et al.
2003). As cost-effective measures to control Cabomba populations are not currently
available (Wilson et al. 2007), further understanding of the ecological niche of this
species is imperative.
There is limited understanding of Cabomba populations in introduced areas, in
particular how this invasive macrophyte affects, and is itself affected, by the area‟s
physical processes and abiotic regimes. There is also limited understanding of the
production rates of Cabomba in introduced areas and how they compare with the
native communities they are displacing. Past studies have shown that Cabomba
populations are species that have high ability to adapt to new environments, are
persistently competitive and able to spread rapidly (Hogsden et al. 2007; Zhang et al.
2003). With the increased in interest in invasion by introduced species, a better
understanding of Cabomba invasion would assist managers in managing this aquatic
plant. The aim of this study is to gain a broader understanding of the mechanisms and
processes driving Cabomba invasion and subsequent shifts in plant community
dominance in an invaded ecosystem, and to ultimately facilitate better management
and restoration of wetland systems.
Studies of species dominance are receiving increasing interest due to their influence on
community assemblages and environmental conditions (Frieswyk et al. 2007;
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
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McNaughton and Wolf 1970). Dominance, defined in this context as the most abundant
species in an ecosystem, can exert control over the other species present
(McNaughton and Wolf 1970). MacDougall and Turkington (2005) argues that to
understand species dominance requires an understanding of the connection between
the mechanisms triggering the abundance of the dominant species and the mechanism
limiting the occurrence of other species. Understanding the causes of dominance is
important as dominant species not only influence environmental conditions, but also
affects the physical and biological processes that characterise ecosystem functioning
(Frieswyk et al. 2007).
Numerous physical processes causing transport and mixing in lakes have been well
documented (Imberger and Patterson 1990; Imboden and Wuest 1995; Socolofsky and
Jirka 2004). However, studies that examine how biological-physical coupling or
chemical-physical coupling relate to aquatic macrophytes are limited. In recent years,
there has been an increasing amount of literature that shows that thermal gradients
drive convective exchanges in lakes, in particular as a result of depth variation (Forrest
2008; Horsch and Stefan 1988; James and Barko 1999; James et al. 1994; Monismith
et al. 1990; Palmarsson and Schladow 2008). Studies by James and Barko (1991)
have highlighted the importance of night time convective circulation in transporting
littoral phosphorus to the pelagic zone. Schladow et al. (2002) have also shown that
vertical penetration of cold-dense littoral water is an important mechanism in
transporting oxygen from the surface of the lake to the bottom.
Vegetation also alters the hydrodynamic motions induced by physical processes and
affects the overall physical circulation of lakes. Floating plants were found to modify the
intrusion of convective motions (Coates and Ferris 1994), and submerged macrophytes
were found to shape the thermal structure (Rooney and Kalff 2000). Macrophyte beds
also strengthen temperature stratification and reduce the mixed layer depth (Herb and
Stefan 2005). Herb and Stefan (2004) have shown that natural convective mixing
during night-time cooling was not affected by the presence of submerged macrophytes,
while wind-driven mixing during the day was significantly attenuated in dense, full-
depth macrophyte beds resulting in higher maximum surface temperatures. Studies of
the influence of natural convection and water exchange on macrophyte species
dominance are rare, and in particular the influence of submerged macrophytes
compared to the influence of floating-leaved plants on this process is largely unknown.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
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Studies on biological processes such plant productivity, which are the essence of plant
physiology, have been very well established (Talling 1961). The majority of plant
productivity measurements have been based on standing crops and biomass
production (Westlake 1963). Since its application to the study of rivers, spring and coral
reefs by Odum in the 1950s (Odum 1956), diel changes in dissolved oxygen (DO)
concentrations have been used to estimate rates of production and respiration in
aquatic ecosystems (Staehr et al. 2010a) in both temperate and tropical regions
(Melack and Fisher 1983; Melack 1982; Talling 1957; Talling 2004). Diel DO changes
have also been used to assess the productivity in the Malaysian lakes, Lake Bera
(Ikusima and Furtado 1982) and Paya Bungor (Yusoff et al. 1984). However, these
studies did not address how the metabolism of the benthic communities is impacted by
a shift in macrophyte assemblages.
As the growth rate of species in communities depends on the rate of their primary
production or metabolism (Westlake 1963), it therefore follows that alteration in species
composition would lead to changes in productivity (Chapin et al. 1997). Lauster et al
(2006) showed metabolic differences between littoral and pelagic habitats when
different species were present. In Hanson et al. (2003), increases in gross primary
production (GPP) and respiration of plants were shown to be influenced by dissolved
organic carbon and nutrient enrichment. However, to date no study has ever been
conducted to assess how the metabolism of invasive plant communities compares to
that of native communities in tropical wetland systems, and this could potentially be an
important mechanism that contributes to their dominance.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
6
1.2 Lake Chini, Malaysia
The study site for this research is Lake Chini, a shallow floodplain wetland in the state
of Pahang, Malaysia. The system, divided into twelve small lake sub-basins with a total
surface area of about 2 km2, is the second largest freshwater lake in the country. The
lake changed its size and depth seasonally; remaining shallow with mean depth around
1.9 m during the dry period throughout most of the year and expanding to double its
normal size during the monsoon months (Nov – Jan). The wetland was dammed in
1995 by the construction of a weir at the confluence of the Chini and Pahang Rivers
which altered the natural flow pattern. The wetland experienced a larger flood, where
the mean depth tripled in 2007.
Past studies have shown this lake is ecologically and social-economically important
because it is an eco-tourism destination and home to a number of endemic and
endangered species (Idris et al. 2005; Sharip and Jusoh 2010). However, a number of
environmental changes have been documented including land use and hydrological
alteration (Idris et al. 2005; Sharip and Jusoh 2010), which has affected water quality
and the hydro-ecological dynamics of the ecosystem.
Initial studies indicated that the wetland‟s ecosystem is degraded (Sharip and Jusoh
2010). Numerous studies in this floodplain wetland, however, have been focused on
the water quality issues specifically in relation to eutrophication (Idris and Abas 2005;
Muhammad-Barzani et al. 2008; NAHRIM 2007; Sharip and Jusoh 2010; Shuhaimi-
Othman and Lim 2006; Shuhaimi-Othman et al. 2007). These water quality changes
are thought to have contributed to the replacement of native floating-leaved species of
macrophytes (Nelumbo nucifera) by an introduced submerged species (Cabomba
furcata) (Idris 2007; Sharip and Jusoh 2010; Shuhaimi-Othman et al. 2007).
However, no studies have been carried out to assess the processes involved in the
observed shift of N. nucifera to C. furcata, or the processes that are likely to control
macrophyte domination in this system including the role of the introduced species (C.
furcata). It is of paramount importance to investigate the nature of the degradation and
the underlying dynamics of the ecosystem in order to suggest effective management
and restoration measures (Hobbs and Harris 2001; Hobbs and Richardson 2011; King
and Hobbs 2006). As the Cabomba population, in general, has been naturalised in
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
7
Malaysia (Chew and Siti-Munirah 2009), this is particularly important as invasion by this
species may have far-reaching ecological impacts for the region.
Studies on the hydro-ecological dynamics of this lake, however, have been very
limited. In a study by NAHRIM (2007), it has been shown that the main driving forces of
water flow in a shallow system such as Lake Chini were wind, river through-flow, and
the density gradient formed by differences in water temperature distribution. Density
gradients and wind motion were important mechanisms during both the normal and dry
seasons (NAHRIM 2007). However, further studies have not been carried out to
examine the exchange mechanisms induced by horizontal density gradients that affect
the patterns of observed water quality and nutrient concentrations. It is hypothesized
that these mechanisms may contribute towards the shift in macrophyte dominance in
the system and further work on understanding these processes is required. As this
wetland is very shallow with macrophytes present in a large proportion of the area,
such information will provide a better understanding of the importance of this physical
process towards the dynamics of the macrophyte community composition.
Further, despite the significance of macrophytes in wetlands, few studies have shown
the importance of macrophytes in contributing to primary productivity in shallow
swamps (Barko et al. 1977; Ikusima 1978; Ikusima and Furtado 1982; Wetzel 1992a),
and in particular how this may vary between an invasive or a native population. The
abundant growth of submerged C. furcata in many of the sub-basins of Lake Chini
could drive the primary productivity in the wetland (Sharip and Jusoh 2010). However,
no studies have been carried out on the primary production of the macrophyte
communities in Lake Chini, specifically the production rates of submerged C. furcata
and the associated benthic community changes. Differences in plant community growth
could contribute to further shifts of macrophyte composition and dominance.
1.3 Research objectives and approach
This study was broadly focused on providing a better understanding of vegetation and
invasion ecology, and freshwater ecology and limnological processes. Specifically, this
study aims to better understand the factors and processes controlling macrophyte
dominance in a shallow tropical floodplain wetland, with the ultimate goal of informing
management of the introduced species (C. furcata). It specifically explores the
dynamics of the abiotic-biotic interactions in the system and the physical processes
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
8
contributing to the transport of resources and biological processes. Further,
understanding the abiotic-biotic interaction and the ecosystem processes allows
wetland administrators and managers to more effectively restore and manage the
wetland ecosystem.
The main research questions, specific to Lake Chini Malaysia, addressed in this thesis
were:
Which environmental variables are associated with patterns of N. nucifera and
C. furcata abundance?
Does the invasion by C. furcata negatively affect the diversity of N. nucifera
dominated communities?
How do the N. nucifera and C. furcata communities affect the thermal structure
and convective circulation, and the subsequent patterns of nutrient distribution?
How do the circulation patterns and phosphate concentrations change as the
water levels change in response to seasonal flooding?
How do the rates of primary production and metabolism between communities
dominated by N. nucifera and C. furcata differ?
How does C. furcata affect the overall net ecosystem metabolism?
Overall, what factors control the shift in aquatic plant communities from
dominance of floating-leaved macrophytes N. nucifera to submerged
macrophytes C. furcata?
In order to answer these questions, the overall aim of the present study was therefore
to provide a comprehensive assessment of the water quality and macrophyte
community in Lake Chini and to characterise the ecosystem processes that contribute
to the changes in macrophyte composition and structure observed in the system. This
overall aim was addressed by three studies. In the first study, the system as a whole
was examined by investigating the historical context linked with environmental changes
in the system. The existing macrophyte communities within the studied area and the
environmental processes that affect the community composition were also analysed.
Whole-lake vegetation surveys, water quality testing and sediment sampling were
carried out in September 2009 prior to the monsoon. Vegetation surveys and water
quality testing was repeated in April 2010 after the monsoon. The vegetation surveys
addressed the temporal and spatial changes of plant communities within the whole lake
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
9
system, and examined the role of the monsoon on the wetland communities and the
environment.
In the second and third study, the two processes that affect the two main macrophytes
species during their initial growth stage were addressed. The processes were studied
at two separate lake sub-basins, one dominated by N. nucifera and another dominated
by C. furcata. High frequency data loggers were deployed in April 2010 to understand
the physical structure and community metabolism of the site. As thermal induced
forcing has been identified as an important physical driver in this shallow system
(NAHRIM 2007), this physical process was specifically examined in the second study.
Additional measurements of temperature were taken in March 2011 to explore the
temperature gradient and circulation pattern due to unexpected flooding. In the third
study, the ecosystem metabolism and primary production and respiratory rates of the
communities dominated by the two macrophytes were examined. These biological
processes were explored using oxygen data from two benthic chambers experiments
and sonde measurements deployed in free water in the littoral and pelagic zones of the
lake.
In all studies, water samples, biomass measurement and sediment were analysed at
an external analytical laboratory. The first study was followed up by multivariate
statistical analysis while the second- and third studies were supported by mathematical
calculations and data analysis techniques.
1.4 Logistical considerations
Future research of changes in macrophyte composition in floodplain wetlands may
focus on the hydro-ecological dynamics of the system associated with the main river. In
the present study it was not feasible to undertake this research due to time constraints
and the scope of the PhD studies. The remoteness of the study site placed a number of
additional logistical constraints on the study. Long-term experiments could not be
conducted as the study site was a long way from analytical facilities. Instrument
malfunction as a result of the challenging tropical environment, unexpected flooding
and human-interference also limited the studies. Vegetation surveys were only carried
out twice, before and after monsoons. Benthic experiments were only able to be
conducted for about 4-days during a dedicated campaign, with one-day diurnal primary
productivity measurement ultimately used due to difficulties in deployment of
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
10
instruments and limitations in instrument availability and functioning. Yet, the available
data collected over the study period still enabled investigation of the ecological
processes possibly controlling the shift of macrophyte dominance in this system.
1.5 Thesis outline
This thesis is presented as a series of scientific papers and consists of five chapters.
Chapter 1 presents the context for the study, the objectives, and the approach
used and the background review of the current and historical literature for the research
paper presented in Chapter 2-4.
Chapter 2 presents a comprehensive assessment and statistical
characterisation of the observed pattern of the macrophyte communities in Lake Chini
with a focus on the distributions of N. nucifera and C.furcata and the environmental
changes. The chapter develops a conceptual model of the ecological changes that
shape the potential macrophyte alternate stable states.
Chapter 3 focuses on the physical processes in particular the physical
circulation induced by the thermal structure and how it influences the water quality in
the habitat and control nutrient delivery for submerged macrophyte production. The
purpose of this chapter is to illustrate the importance of exchange dynamics between
lakes dominated by different vegetation.
Chapter 4 focuses on the biological processes associated with dissolved
oxygen dynamics, and in particular the metabolic differences between the habitats and
the associated communities dominated by N. nucifera and C.furcata.
The final synthesis chapter (Chapter 5) summarises and discusses all findings
of Chapter 2-4. The chapter also provides concluding remarks on the management
implications arising from the findings of this study, study limitations and
recommendations for future work.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
11
Chapter 2 - Eutrophication, agriculture and water level control
shift aquatic plant communities from floating-leaved to
submerged macrophytes in Lake Chini, Malaysia1
2.1 Abstract
In this study we: 1) present a quantitative spatial analysis of the macrophyte
communities in Lake Chini with a focus on the biogeographical distributions of the
native Nelumbo nucifera and the invasive Cabomba furcata; 2) examine the
environmental changes that affect plant community composition; and 3) outline a
conceptual model of the variation of ecological processes that shape the macrophyte
communities. Plant species cover, biomass of C. furcata and N. nucifera, and water
quality and environmental variables were measured before and after monsoonal floods
in September 2009 and April 2010. Permutational multivariate analysis was used to
examine the significance of the invasion of C. furcata at different spatial scales.
Relationships between plant species cover and environmental variables before and
after flooding were examined using principal coordinates analysis and non-parametric
multivariate multiple regressions. Our findings suggest that 1) Variation in plant
communities was significant at the lake scale and the distribution of plant species
changed after annual floods. 2) Invasion by C. furcata significantly affected the overall
plant community composition. 3) C. furcata biomass increased after the monsoonal
season, which indicates that C. furcata is adapted to flooding events and that it is
becoming increasingly abundant. 4) In addition to the strong monsoonal effect, total
depth, nutrient concentration, and sediment type were important environmental
variables that significantly affected plant community composition. The macrophyte
community in Lake Chini is highly dynamic. The spatial and temporal plant community
dynamics are associated with flood regime, water quality, and substrate. Human-
induced changes in these parameters are likely shifting the macrophyte dominance
from floating-leaved to submerged species.
Keywords
Ecological alteration, eutrophication, floodplain wetland, invasive aquatic plant, lotus,
water fanwort
1 Have been published in Biological Invasions Journal
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
12
2.2 Introduction
Floodplain lakes and wetlands are continuously subjected to environmental stressors
that affect their plant community composition and structure. Human-induced alterations
such as eutrophication have been reported to result in change of dominance from
rooted and floating-leaved plants, (which typically characterise undeveloped wetlands
(Lougheed et al. 2008) and natural environments (Radomski 2006)), to assemblages
made up of floating plants and more tolerant emergent species (Lougheed et al. 2008),
from submerged plants to emergent species (Egertson et al. 2004) or from submerged
plants to floating plants (Bini et al. 1999). Changes in the hydrological regime have also
been responsible for transition in wetland macrophyte communities. Van Geest et al.
(2005) and Whyte et al. (2008) reported that floodplain lakes along the Lower Rhine
and Lake Erie coastal wetlands switched from floating-leaved dominance to emergent-
dominance following decline of the water level. In the Murray-Darling Basin, Australia,
regulation and damming of the river changed the hydrology of fringing floodplain
wetlands and subsequently altered ecological processes that affected macrophyte
diversity and species composition (Kingsford 2000).
Infestation of non-native species in such changing environments alters community
structure and ecosystem function (Ehrenfeld 2003; Farrer and Goldberg 2009;
MacDougall and Turkington 2005) and patterns of succession. The dynamic patterns of
vegetation and community succession following transition from a native species
assemblage to an invaded community are influenced by site availability and the
species differential availability and performance (Pickett and McDonnell 1989). Multiple
perturbations, such as nutrient enrichment and alteration of food-web structure, reduce
ecological resilience, alter feedback mechanisms, and may subsequently induce a
sudden shift of dominance (Carpenter and Cottingham 1997; Folke et al. 2004).
Understanding the key mechanisms that drive shifts of plant community dominance is
crucial to facilitate management and restoration.
This study reports the plant community alteration that has occurred in a tropical
floodplain wetland system, Lake Chini, Malaysia, in response to a shift in plant species
dominance from a floating-leaved species (Nelumbo nucifera) to a submerged species
(Cabomba furcata), as previously observed by Shuhaimi-Othman et al. (2007). The
appearance of C. furcata, a non-native species, was first reported in 1998 (Wetland
International 1998) and its abundance was noted to have spread to other lakes within
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
13
the wetland basin in 1999 (Gan and Bidin 2005). It has currently reached infestation
proportions (Chew and Siti-Munirah 2009) and is severely impacting on the natural and
cultural heritage values of the wetland. What has triggered this infestation and shift of
plant community dominance away from the once stable Nelumbo community is not
known. Unfortunately, past studies of the plant communities in Lake Chini were not
based on quantitative data, which hinders the understanding of how the changes in the
macrophyte community composition and structure relate to variability in environmental
properties. This is compounded by limited hydrological and water quality data available
from which to build a baseline understanding of the system. To the authors‟ knowledge,
there is also no specific research that has been carried out elsewhere in the world on
the change of dominance between Nelumbo and Cabomba species. Clearly, a
thorough understanding of different plant response to ecological changes needs to
consider alterations to key environmental attributes that characterise the ecosystem. It
is therefore the aim of this paper to: 1) to present a quantitative spatial analysis of the
macrophyte communities in Lake Chini with a focus on the biogeographical
distributions of N. nucifera and C. furcata; 2) to examine the environmental changes in
Lake Chini that may affect the plant community composition; and 3) to outline a
conceptual model of the variation of the ecological processes that shape macrophyte
distribution to assist in management of Lake Chini to meet conservation goals. The
work is based on review of data from the available literature and a comparative
analysis of baseline ecological survey work conducted in September 2009 and April
2010.
2.2.1 Study Area
Lake Chini is the second largest freshwater lake in Malaysia. It is a small (~2 km2)
alluvial riparian swamp system that is located within the Pahang River floodplain (Fig.
1). The lake is comprised of 12 small lakes that are inter-connected by natural
channels. Due to its close proximity to the main river, the lake‟s size and depth
changes significantly seasonally, remaining shallow (mean depth 1.9 m) during the dry
period throughout most of the year and expanding to double its normal size during the
monsoon months (Nov – Jan). Extensive beds of floating-leaved and emergent
macrophytes form an important feature of the lake, and similar to other wetlands,
account for a large proportion of the total primary production (Ikusima and Furtado
1982). N. nucifera once covered a substantial part of the surface water and large
blooms of its lotus flower led to the lake becoming a tourist attraction. Due to its
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
14
ecological importance and ecotourism value, Lake Chini was designated as a
UNESCO Biosphere reserve in 2009. However, the extensive presence of C. furcata in
Lake Chini in 2007 disrupted navigation and has since diminished its tourism potential
(Chew and Siti-Munirah 2009). There is a need to understand the factors that influence
the differences in macrophyte dominance in order to rehabilitate and manage Lake
Chini‟s environment for eco-tourism purposes, and concomitantly retaining its
ecological diversity.
Figure 1: Location of Lake Chini in peninsular Malaysia with inset showing the lake
system. Lake outlet is located between Lakes 4 and 5
Alteration of the land use in both the catchment and the lake environment, facilitated by
socio-economic pressure over the past 20 years, has affected the lake ecosystem.
Logging and conversion of forested area to agricultural land has increased (Shuhaimi-
Othman et al. 2007), and such practices are known to affect hydrological processes
(Bruijnzeel 1991). In 1995, a weir was constructed at the downstream end of Chini
River, at the confluence of the Chini and Pahang Rivers, in order to maintain higher
lake water levels for year-round navigability (Shuhaimi-Othman et al. 2007). This
altered the natural flood pulse and pattern of water level fluctuation and may affect the
macrophyte community structure.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
15
2.2.2 Study organisms
Nelumbo spp. and Cabomba spp. come from different life form groups which differ in
structure, morphology, physiology, and habitat (Cooke et al. 2005; Schulthorpe 1967),
and subsequently their adaptation to the environment. N. nucifera is an Asiatic floating-
leaved plant that is native to Malaysia (Schulthorpe 1967). N. nucifera and its American
relative, Nelumbo lutea, comprise the only two species in the family Nelumbonaceae.
They have roots and rhizomes in the sediment, connected by petioles to floating and
emergent leaves (Cronk and Fennessy 2001). Rapidly growing petioles, attached in the
middle of the leaf blade, allow the leaves to rise with increasing water levels (Nohara
and Tsuchiya 1990). Nelumbo spp. grows well at depths of 1.5-2 m (Baldina et al.
1999; Schulthorpe 1967) up to a maximum depth of approximately 3 m (Kunii and
Maeda 1982; Unni 1971). They can grow in both acidic and alkaline water (Meyer
1930). They absorb nutrients from sediment and propagate by seeds and rhizomes.
The preferred substrate is benthic soil comprised of mainly gray, loamy mud (Kunii and
Maeda 1982).
In contrast, Cabomba is a genus of submerged macrophytes consisting of five species
that originate from the Americas (Orgaard 1991). Several species in the genus have
been introduced to water bodies around the world and the distribution exhibits a wide
latitudinal range from cold temperate to tropical waters (Schooler et al. 2009). As for
most introduced Cabomba populations, C. furcata was probably introduced to Malaysia
through the aquarium trade (Orgaard 1991) and has become naturalised in Lake Chini
within the last decade (Chew and Siti-Munirah 2009). C. furcata, in its native range,
grows in an environment that experiences fluctuating water levels, from dry periods to
periods of high water levels (Orgaard 1991). It commonly grows rooted at 2-3 m water
depth (Orgaard 1991), although Cabomba caroliniana has been found rooted at depths
up to 6 m (Schooler and Julien 2006). It grows well in acidic water, preferably at pH 4-6
(Orgaard 1991; Sanders 1979). Cabomba spp. uptake nutrients directly from the water
through shoots, leaves, and stems (Wilson et al. 2007) and have been observed to
grow well in nutrient rich water (Oki 1994). Cabomba spp. can also exist in turbid water
(Sanders 1979), prefer fine and soft substrates, and primarily propagate through
vegetative reproduction by means of stem fragmentation (Schooler et al. 2009).
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
16
2.3 Methods and materials
2.3.1 Overview
In order to assess changes within the Lake Chini catchment, data on land use and
surface phosphate concentration were collected from the available literature (Division
of Agriculture 1966; DARA 1992 unpubl. data, Shuhaimi-Othman et al. 2007). Data on
adjacent land use were available in the literature from 1975 to 2007 while data on
surface phosphate concentration were available from 1994 to 2007. Water level data
were obtained from the Drainage and Irrigation Department of Malaysia and the
National Hydraulic Research Institute of Malaysia. Hydrological records were available
from 2007-2010. Field measurements were carried out at Lake Chini on 26-28
September 2009 involving a survey of plant community abundance and composition
and measurement of water quality and sediment properties. Twelve main stations were
selected at each lake for intensive water quality and sediment sampling. Similar plant
abundance and water quality surveys were undertaken on 12-14 April 2010 to examine
the after-effect of the monsoonal flood on the abiotic variables and biotic communities.
2.3.2 Plant community sampling
The abundance of aquatic plant species within the lakes was assessed as plant cover.
Plant cover was visually estimated from a boat by an experienced observer within 1 m2
quadrats at each site along 2-4 transects within each lake. Two quadrats were
recorded at each site. Three to five sites were assessed in each transect, depending
on the transect length which range between 70 to 500m. Transect positions were
randomly selected, beginning in the centre of each lake, and arranged perpendicular to
the shoreline. The coordinates for each site were marked using Garmin GPSMap 60
model CSx (Garmin International, Kansas, USA) and downloaded into the Garmin
MapSource ® mapping software version 6.13.7. The surveyed positions were overlaid
on a satellite image (IKONOS 2006) using GIS software (Arcview ver. 3.3, ESRI,
Redlands, CA, USA). Specimens of plant samples were sent to the local herbarium
(Forest Research Institute of Malaysia and UKMB) for taxonomic identification.
Biomass measurements of C. furcata and N. nucifera were carried out where dense
beds of the respective plants grew along gradual slopes. One transect was selected at
each aquatic plant bed, where the quadrats were haphazardly positioned through these
beds, beginning at the shoreline and extending to the centre of the lakes. Using
SCUBA, three samples were taken, first at 0.25m, then at each successive 0.5m depth
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
17
increment, from 0.5m to either: a) the depth where the plants no longer grew or b) the
deepest point in the lake. Plant samples were collected using a quadrat (0.25 m2), then
washed and coiled, and placed into individual plastic bags. The plants were then stored
in cool container, and transported to the laboratory within 24 hours. Plant samples were
dried to constant weight in a drying oven at 103oC and the dry weights were recorded
to 0.01g.
2.3.3 Environmental variables
In-situ profiles of temperature, pH, dissolved oxygen (DO), turbidity, specific
conductivity and depth were taken at all surveyed sampling points using a YSI 6600
multi-parameter sonde. Water samples were collected using a Van Dorn sampler at 12
main stations located around the centre of each lake at 2-depths (surface and bottom
levels). Additional samples were taken near the surface (0.5 m) at selected sites having
dense macrophyte beds, mainly either C. furcata or N. nucifera. Water samples were
analysed for phosphate (PO43-), ammonium (NH4
+) and nitrate (NO3-) in accordance
with standard methods (APHA 1992) as listed in Appendix 1b. All the water samples
were placed in a cooler box (temperature ≤4oC) and transported to the laboratory within
24 hours. Sediment samples were collected using a Van Veen Grabber, stored in a
transportation box, and sent to the laboratory for sediment texture analysis (British
Standards Institution 1990). An additional distance measure, the distance from the
centre of each lake to the weir, was obtained from the coordinates and the satellite
image. Distance from the weir was ranked prior to analyses.
2.3.4 Statistical Analysis
To provide a quantitative spatial analysis of the macrophyte communities in Lake Chini,
we first used non-metric multidimensional scaling (NMDS), based on the Bray-Curtis
dissimilarity matrix (Clarke 1993) to visualise multivariate patterns among the plant
species cover within the 12 lakes, across the two seasons. To extract meaning from
the axes produced in NMDS, we performed principal coordinates analysis (PCoA) in
PERMANOVA to correlate environmental variables with the ordination axes (Anderson
et al. 2008; Anderson and Willis 2003). In this analysis, we used Pearson correlation to
highlight linear relationships between individual variables across the plot. Principal
component analysis (PCA), which projected samples to maximise their variance, was
applied to reduce the number of observed variables and summarize the pattern of the
correlation between total depth, temperature, pH, dissolved oxygen, turbidity,
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
18
conductivity, phosphate, nitrate, ammonium, %silt/clay content and rank distance from
weir. NMDS and PCA were based on lake averages. We then used linear regression to
illustrate the relationship between C. furcata cover and diversity. The Shannon-Weiner
Index of Diversity, calculated from mean lake abundance (cover) in September and
April, was used as the measure of plant diversity.
A hierarchical experimental design composed of three factors, i.e. lake (L: fixed),
transect (T: random, nested in L) and site (S: random, nested in L and T) and percent
C. furcata cover as covariate was used to characterize the effects of invasion by C.
furcata on the macrophyte community composition in Lake Chini. Permutational
multivariate analysis of variance, PERMANOVA (Anderson 2001a; Anderson et al.
2008) was performed on a basis of zero adjusted Bray-Curtis dissimilarity matrix
(Clarke et al. 2006) for the rest of the other species cover dataset to test whether
invasion by C. furcata significantly affected plant community composition at the spatial
scale of lake, transect and site (quadrat). The complex nature of the wetland
morphology and the subsequent plant assemblages and hydrological restriction during
our study led to an un-balanced replicated study design. All the analyses were
performed separately for data collected in September 2009 and April 2010, which
characterise the community assemblages before and after the monsoon season,
respectively.
Nonparametric multivariate multiple regression, DISTLM was employed to model the
relationship between the multivariate species matrix and the 11 environmental
variables. The individual variable was initially examined in the marginal test (excluding
other variables) and then subjected to a forward selection procedure (BIC selection
criterion) with sequential tests to determine the predictor variables that explain the
variation in the data. Significance was performed by 9999 permutations of residuals
under the reduced model (Anderson 2001b).
Wilcoxon Signed Rank Tests were performed to determine significant differences
between biomass harvested in September and April. Plant cover data were square-root
transformed, while biomass values and the water quality variables were natural log
transformed to improve normality. All Wilcoxon Signed Rank Tests were performed in
SPSS 16.0 (SPSS Inc.). Multivariate methods (NMDS, PCA, PCO, PERMANOVA and
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
19
DISTLM) were conducted in PRIMER 6 (Plymouth Marine Laboratory, Plymouth, UK)
and PERMANOVA+ (Plymouth Marine Laboratory, Plymouth, UK).
2.4 Results
2.4.1 Catchment and hydrological changes
Landscape changes within the Lake Chini catchment were apparent, changing from a
forested area in 1966 (Division of Agriculture 1966) to agricultural land with patches of
deforestation. Agricultural practices in the form of oil palm plantations and rubber
estates accounted for only 280 ha (5.6%) of the catchment area in 1992 (DARA 1992
unpubl. data) and this increased to a total of 807 ha (16.2%) in 2004 (Shuhaimi-
Othman et al. 2007) (Fig. 2a). Increased water surface phosphate concentration was
evident, from average of 0.01 mg/L in 1998 to around 0.06 mg/L in 2010 (Fig. 2b). A
decrease in surface phosphate between yr 2008-2010 could be associated to flushing
of nutrient from the lake by a large flood event in 2007.
0
5
10
15
20
1960 1970 1980 1990 2000 2010 2020Ag
ricu
ltu
ral l
and
-use (
%)
Year
0
0.02
0.04
0.06
0.08
0.1
1960 1970 1980 1990 2000 2010 2020
Me
an
ph
osp
ha
te
co
nce
ntr
atio
n (
mg
/L)
Year
(a)
(b)
Figure 2: Historical changes in (a) agriculture land use fraction and (b) mean
phosphate concentration (mg/l) at the water‟s surface. Phosphate concentrations from
2009 and 2010 were taken during the present survey. Historical data sources are listed
in the method
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
20
Historical data on water levels (Fig. 3) showed the influence of the Pahang River on
Lake Chini surface water level during monsoon months. The variability of the lake
water level in relation to fluctuation of the river water level was reduced by the weir
structure with the lake level increasing slightly with the Pahang River level. Further rise
in Pahang River level inundated the wetland and subsequently increased the lake
surface level.
9
10
11
12
13
14
15
16
17
18
25/10/2007 14/11/2007 4/12/2007 24/12/2007 13/01/2008 2/02/2008 22/02/2008
Wate
r le
ve
l (m
)
Pahang River level 2007-2008 Lake Chini level 2007-2008
Pahang River level 2009-2010 Weir height
Figure 3: Comparison between the Pahang River level and Lake Chini water level. Both
water levels were approximately referred to mean sea level
2.4.2 Spatial distribution of aquatic plants
A total of 17 plant species, native and non-native, were recorded from the 137
surveyed sites over the 12 lakes (Table 1). We found that Pandanus helicopus, C.
furcata, N. nucifera, Scirpus spp. and Lepironia articulata are the most abundant
species in the lake system. Comparison between prior surveys of macrophyte diversity
in the literature and the present survey indicate the presence of previously undetected
species (see Table S1 in supporting information).
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
21
C. furcata and N. nucifera coverage differed between the 12 lakes (Fig. 4 and Fig. 5). C.
furcata remained widely established in the absence of N. nucifera in Lake 12 and Lake
10, and appeared in another lake (Lake 2), where it was previously not found during
the September (pre-flood) sampling. The N. nucifera population has increased in all
lakes where it was present in 2009, and in particular in lakes that were located closer to
the Pahang River. Diversity in lakes decreased with increasing C. furcata abundance
(Fig. 6) in September (t12=10.276, P<0.001).
Table 1: List of macrophytes recorded in the present survey in September 2009
LAKE
Species (scientific name) 1 2 3 4 5 6 7 8 9 10 11 12
Submerged macrophyte
Cabomba furcata* + + + + + + + + + +
Utricularia gibba + + + + + + + + +
Chara sp. +
Floating macrophyte
Salvinia molesta* +
Rooted, Floating-leaved
Nymphea pubescens lotus + + +
Nelumbo nucifera + + + + + + + +
Emergent
Lepironia articulata + + + + + + + + + +
Eriocaulon sexangulare +
Scirpus grossus + + + + + + +
Pandanus helicopus + + + + + +
Eleocharis ochrostachys + + +
Lycopodiella cerniea (cernua) +
Cyperus pilosus +
Pragmites communis + +
Lygodium microphyllum +
Panicum Repens + + + + + + + + + + * Introduced species
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
22
Figure 4: Comparison of C. furcata and N. nucifera coverage before and after
monsoonal flooding
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
23
C. furcata
N. nucifera
Figure 5: Mean cover of C. furcata and N. nucifera by lake and by sampling date. Error
bars are ± SE
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
24
Y =-0.049x+0.675;
R2=0.130
Y+=-0.110x+1.344;
R2=0.507
Mean C. furcata cover (sqrt)
Figure 6: Regression of C. furcata cover against Shannon-Weiner Diversity Index (H‟).
Symbols indicate sampling month: +September, ● April
The PERMANOVA detected significant variability at the “lake” spatial scale. The factor
“transect” and “site” were pooled since they were the factors with negative estimates
for component of variance and a higher p-value (Anderson 2001b; Anderson et al.
2008). PERMANOVA tests (Table 2) showed that differences between invaded and un-
invaded plant assemblages were highly significant, both in September and April.
Differences in the composition of invaded and un-invaded sites were stronger in
September compared to April, indicating the influence of the monsoonal flood on the
macrophyte community composition.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
25
Table 2: Permutational multivariate analysis of the effects of invasion, lake, transect
and site on plant community abundance
PERMANOVA tests
Source of variation df SS MS F P(perm)
September 2009 Invasion 1 19590 19590 12.475 0.0001*** Lake 11 46222 4202 2.676 0.0001*** Pooled 134 210430 1570.3 Total 146 276240 April 2010 Invasion 1 13991 13991 11.202 0.0003*** Lake 11 50843 4622.1 3.701 0.0001*** Pooled 134 167370 1249 Total 146 232200 df degree of freedom, SS sum of squares, MS mean squares, ***=p<0.001
Mean C. furcata biomass from both sampling periods was correlated with depth (r = -
0.773, P=0.042) (Fig. 7). A Wilcoxon Signed Rank Test indicated an increase in
biomass from Sept to April; z=-2.201, P=0.028 (two-tailed). The magnitude of
differences in the means was large and the median score on the biomass increased
from Sept (15.1 g/m2) to April (318 g/m2). The highest C. furcata and N. nucifera
biomass were sampled in April at depth of 0.5 m and 1.5 m with biomass 934.7 g/m2
and 62.7 g/m2 respectively.
0
5
10
15
20
0.25 0.50 1.00 1.50 2.00 2.50 2.80 3.00
Me
an
bio
mass (
g/m
2)
Depth (m)
(a) Mean C. furcata biomass in Sept 2009
0
200
400
600
800
1000
0.25 0.50 1.00 1.50 2.00 2.50 2.80 3.00
Me
an
bio
ma
ss (
g/m
2)
Depth (m)
(b) Mean C. furcata biomass in April 2010
Figure 7: Relationship between depth and mean C. furcata biomass. Biomass is the
mean dry weight sampled in all quadrats at that depth
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
26
2.4.3 Environmental variables potentially influencing macrophyte
distribution
PCA, employing Euclidean distance, indicated a consistent linear combination of
variables making up the principal components. The first three eigenvalues explained
69% of the variance; the first component corresponded to 34% variance and second
component explained 20% of the variance. Plots of the first two components showed
separation of the dataset before monsoon to the dataset after the monsoon, which
indicated the influence of flooding on the water quality (Fig. 8). The separation of sites
by sampling date along axis 1 was primarily correlated with nitrate concentration and
total depth and along axis 2 was correlated to phosphate, turbidity and pH. Details on
the environmental variables are given in supporting information (Table S2).
-4 -2 0 2 4
PC1
-4
-2
0
2
4
PC
2
MonthSept
April
S1
S2
S10
S11
S12
S8
S9
S3
S4
S5
S6
S7
A1
A2
A10
A11
A12
A8
A9
A3A4
A5
A6
A7
Total depth
Temperature
Conductivity
pH
Turbidity
DO
PO4
NH3NNO3
%silt/clay
Distance to weir
Figure 8: PCA biplots of the average values of the environmental variables by sampling
month. Number indicates lake
The results of DISTLM tests (Table 3) revealed a positive match between the
environmental variables and species assemblages in the Lake Chini dataset. Total
depth explained ~42.6% of the variation in the composition of the plant assemblages in
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
27
September 2009 and 26.5% of the community variation in April 2010. Phosphate,
temperature, nitrate, %silt/clay and conductivity contributed a further 26.2% of the
variance in September 2009, while distance from weir, dissolved oxygen, ammonium
and temperature together explained about 24% of the variance in April 2010.
The phosphate concentrations sampled in all areas having dense C. furcata and N.
nucifera beds were very low (non-detectible) in September, while in April, nitrate
concentrations were low in the plant beds (Fig. 9). PCoA results indicate C. furcata was
associated with lakes having a higher silt/clay percentage and increasing distance from
the weir, whereas N. nucifera was found in lakes having lower silt/clay content (Fig. 10).
0
20
40
60
80
100
0.0 0.1 0.2 0.3 0.4
Co
ve
r (%
)
PO4 concentration (mg/L)
(a) C. furcata
Sep-09 Apr-10
0
20
40
60
80
100
0.0 0.1 0.2 0.3 0.4
Co
ve
r (%
)
PO4 concentration (mg/L)
(b) N. nucifera
Sep-09 Apr-10
0
20
40
60
80
100
0.0 1.0 2.0 3.0 4.0 5.0
Co
ve
r (%
)
NO3 concentration (mg/L)
(c) C. furcata
Sep-09 Apr-10
0
20
40
60
80
100
0.0 1.0 2.0 3.0 4.0 5.0
Co
ve
r (%
)
NO3 concentration (mg/L)
(d) N. nucifera
Sep-09 Apr-10
Figure 9: Relationship between dominant species cover and phosphate and nitrate
concentration
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
28
Table 3 Results of the DISTLM analysis on the Lake Chini dataset in September 2009
and April 2010
Sequential tests
Variable BIC Pseudo-F P % Var %Cum
September 2009
+Log(Total depth+1) 418.50 42.957 0.0001*** 42.55 42.55
+Log(PO4+1) 416.35 6.2481 0.0019** 5.68 48.23
+Log(Temperature+1) 411.99 8.4811 0.0003*** 6.81 55.04
+Log(NO3+1) 410.58 5.2837 0.006** 3.94 58.98
+%silt/clay 408.41 5.9403 0.0039** 4.07 63.04
+Log(Conductivity+1) 402.51 9.6054 0.0001*** 5.67 68.71
April 2010
+Log(Total depth+1) 438.49 20.917 0.0001*** 26.505 26.51
+Rank distance to weir 435.97 6.6387 0.0008*** 7.667 34.17
+Log(DO+1) 435.90 4.0264 0.0151* 4.416 38.59
+Log(NH4+1) 434.72 5.0482 0.004** 5.163 43.75
+Log(Temperature+1) 431.25 7.2604 0.0008*** 6.667 50.42
BIC Bayesian Information Criterion, %Var percentage of variance in species data
explained, % Cum cumulative percentage of variance explained *=p<0.05, **=p<0.01,
***=p<0.001
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
29
-60 -40 -20 0 20 40 60
PCO1 (61.2% of total variation)
-80
-60
-40
-20
0
20
40
PC
O2
(1
8.2
% o
f to
tal
var
iati
on
)
Dominant species
0
1
2
3S1
S2
S10S11
S12
S8S9S3
S4
S5
S6 S7
A1A2A10A11
A12
A8
A9
A3
A4
A5
A6
A7
Depth
Temp
CondpH
Turb
DO
PO4
NH4NO3
%silt/clay
RDis
Figure 10: PCoA plot of plant species abundance and environmental variables.
Symbols represent main species: triangles, N. nucifera; diamonds, N. nucifera and C.
furcata; squares, C. furcata, circles, other species. Number indicates lake; Letter
indicates sampling month: S=September, A=April. Water quality variables were natural
log-transformed
2.5 Discussion
Similar to other lakes and wetlands around the world, human land-use practices to
address socio-economic needs are affecting Lake Chini, resulting in alteration of
habitat and biotic communities. The results of this study document landscape and
water quality changes in Lake Chini. Change in the surrounding terrestrial landscape
from forested areas to agricultural land could alter runoff quantity and quality, and in
particular may possibly increased nutrient input into the lake and the suspended
sediment load and subsequent deposition. Hydrological alteration further induces
ecological changes by stabilising the lake water levels, reducing the flood disturbance
regime, and affecting the flood timing and duration (Nilsson and Svedmark 2002).
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
30
Spatial variation in the abundance and distribution of the studied plant species between
the lakes was apparent. The cover of C. furcata observed in September 2009 was
lower compared to observations in 2007 (before the intermediate size flood event)
(Sharip pers. observation, Chew and Siti-Munirah 2009, Sharip and Jusoh 2010).
However, both cover and biomass increased from September 2009 to April 2010 which
indicated that it may be in the process of re-spreading. Dissimilarities between lakes
within invaded and un-invaded sites could result from the complex interaction among
different forcing mechanisms and ecological processes that dominate during the
different seasons. This invasion is having a significant impact on the overall plant
community diversity. Early growth phase after seasonal disturbance could explain the
weak correlation between C. furcata abundance and diversity in April. Increased C.
furcata biomass after the monsoonal season indicates that the plants survived from the
previous year and then grew rapidly, probably due to the availability of resources
during and after the floods. The sustained growth of such invasive species could affect
the plant community structure and reduce the establishment of other species (Santos
et al. 2011).
The spatial and temporal variation of water quality parameters described here are
consistent with the results of prior studies that examined the water quality in Lake Chini
(Shuhaimi-Othman et al. 2007). The nutrient levels were high, suggesting that nutrient
enrichment is a concern and may have a strong impact on the composition of the plant
community and the population dynamics of C. furcata and N. nucifera in Lake Chini.
The mean phosphate concentration in Lake Chini was high in both sampling months.
Shuhaimi-Othman et al. (2007) suggest that the increase in phosphate concentration at
Lake Chini is attributed to run-off from agriculture areas and settlement (Shuhaimi-
Othman et al. 2007). Higher phosphate concentration in the water column after flooding
could also be attributed to P-release from sediments during high water (Boers and
Zedler 2008).
Trace values of phosphate in areas where C. furcata was abundant suggest that it may
have been consumed by the plants. Studies have shown Cabomba spp. absorb
nutrients directly from the water through shoots, leaves, and stems (Wilson et al. 2007)
and nutrient rich water may have promoted high C. furcata abundance in Lake Chini.
There was a decreasing trend of phosphate concentration from pelagic to littoral
regions in September, while in April, the decreasing trend from pelagic to littoral
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
31
regions was apparent for nitrate concentration. Physical processes that control the
exchange of these constituents from the pelagic to the littoral zone should be further
investigated, since differential temperature gradients between the zones were noted
and may control nutrient delivery to dense C. furcata beds. In addition, the switch from
detectable nitrate and undetectable phosphate in September, before the monsoonal
floods, to undetectable nitrate and detectable phosphate after the floods in dense
macrophyte beds suggests a change in nutrients limiting macrophyte growth.
A change in sediment characteristics in Lake Chini was apparent with increased silt
content compared to earlier findings (Abas et al. 2005). Deposition of silty materials is
most likely enhanced from run-off and erosion from an increasingly cleared catchment.
An increase in silt content in the substrate makes the site more suitable for Cabomba
spp. growth as it more closely resembles the substrate characteristics of both its native
range and areas where it is highly invasive (Schooler et al. 2009). N. nucifera
preferance for mud loamy subtrate (Kunii and Maeda 1982) explains the negative
correlation between N. nucifera abundance and %silt/clay content. Negative correlation
between N. nucifera abundance and distance to weir and positive correlation between
N. nucifera abundance with turbidity may be associated with floods. The Pahang river,
like many tropical rivers, contains high suspended sediment ranging from 1-152 mg/L
(Sulaiman and Hamid 1997). The suspended solid, derived from erosion of the alluvial
and podzolic soil in the river basin (Panton 1964), is composed largely of loamy clay,
which is not only suitable for N. nucifera growth but also easily resuspended when
disturbed. Depending on the timing, duration and flood amplitude, the floating leaves of
N. nucifera elongate petioles to extend above the turbid water to reduce the impact of
flooding (Nohara and Kimura 1997; Nohara and Tsuchiya 1990).
The statistical analysis clearly indicated that water depth was an important
environmental variable for both submerged C. furcata and floating-leaved N. nucifera.
The association of depth to variation in C. furcata abundance and biomass agrees with
the finding of previous studies of another Cabomba species, C. caroliniana (Schooler
and Julien 2006). High C. furcata cover and density were found in shallower areas and
abundance decreased with depth. The decrease in lake water level during the dry
season (as apparent in April sampling), which happens after the monsoonal flood,
coincides with the initial plant growth phase and may contribute to the re-zonation of
plant establishment towards the centre of the lake where a more suitable water depth is
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
32
apparent. Water depth is strongly associated to light penetration (Spence 1982), which
is essential for submerged plant growth. A decrease in water level alters the light field
across the benthos and can lead to an increase in temperature as more heat is
absorbed by smaller volume of water. As the system becomes shallower, the
hypolimnion may disappear and result in reduced stratification and increased dissolved
oxygen at depth. The high concentration of ammonium in April could be associated
with the flood (Shuhaimi-Othman et al. 2007) and result in the observed increases in C.
furcata biomass. C. furcata showed higher primary production in rainy seasons where
waters contains high ion, nutrient concentrations and low transparency (M. Pezzato,
pers. comm.).
The change in floristic communities may be the result of the large flood event that
occurred in December 2007. The influence of inflow from the Pahang River and the
different flooding effect during the monsoon season may have affected the ecological
processes and subsequently the composition and distribution of the plant community
since significant differences in plant abundance was apparent between the two
seasons. Different magnitudes of floods have been reported to exhibit different effects
to wetland ecosystems (Hughes 1997; Richardson et al. 2007); intermediate size floods
influence plant community distribution while small annual floods affect plant species
abundance (Nilsson and Svedmark 2002). The changes in distribution and abundance
of C. furcata and N. nucifera indicates dynamic population shifts which may be largely
influenced by the annual flooding cycle. Flooding events may disrupt the substrate and
dislodge plants. This could increase the spread of C. furcata, which can grow from
stem fragments. Results from this study, in conjunction with historical observations,
suggests that the distribution and abundance of N. nucifera is constantly shifting and is
currently expanding, despite recent changes in sediment structure and eutrophication.
Based on our results we have developed a conceptual model of ecological variation in
Lake Chini that describes how alteration of the lake ecosystem is associated with the
combination of disturbances (Fig. 11), which are known to enhance biological invasion
(Hobbs 1991). The installation of the weir structure has changed the biological and
physical characteristics of the lake by altering the hydrological processes and
disturbance regimes. Together with continuous alteration of the surrounding landscape,
and eutrophication and siltation pressures increasing the availability of nutrients in the
water and silt content in the sediment, the ecological community is adapting to the new
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
33
state. Where non-native species are involved, research has shown that disturbance will
enhance invasions when it is also associated with an increase in the availability of
limiting nutrients (Hobbs 1989). The stabilised water depth, and increasing nutrient
availability in water and silt content in the subtrate has facilitated the invasion of C.
furcata in the wetland. The extent of the effects of engineering intervention (damming)
in causing a rapid proliferation of the invasive species in Lake Chini is consistent with
changes in riparian vegetation (Richardson et al. 2007). In this shallow floodplain
wetland, the change of the dominant aquatic vegetation from N. nucifera to C. furcata
has been dramatic and has occurred within a period of less than 10 years.
The occurrence of regime shifts or alternative stable states are acknowledged in
different kinds of freshwater ecosystems (Dent et al. 2002; Folke et al. 2004). Floating
plant dominance has been recognised as a new stable state associated with
eutrophication over a state characterised by submerged plant in tropical lakes (Scheffer
et al. 2003). In contrast to shallow lakes where alternative stable states are primarily
between macrophytes and algae, wetland systems where macrophytes dominate
primary production exhibit different multiple states. Nutrient enrichment has shifted
freshwater marshes in the Everglades from wetlands dominated by sawgrass to cattail
marshes (Gunderson 2001). Changing patterns of macrophyte dominance between N.
nucifera and C. furcata implies the possibility of two alternate stable states in Lake
Chini. Floating-leaved plants, such as N. nucifera, are better competitors for light,
carbon and nutrients from the sediment, and once re-established after intermediate
size floods, they may have competitive advantage to spread when the natural flow
regime is re-established due to flooding by the Pahang River as a results of frequent
high intensity rainfall in the Pahang river basin. However, submerged species, such as
C. furcata, are superior competitors for nutrients in the water column (Gunderson
2001), and continuing eutrophication will likely increase its abundance and spread in
the system and eventually could cause a shift of dominance.
Macrophyte occurrence and dominance is characterised by species life history traits
and environmental conditions (Pickett and McDonnell 1989). Being able to vegetatively
propagate abundantly via fragmentation increases spread rates for Cabomba spp.,
particularly after disturbance events where plants are broken (such as from propellers).
This, along with eutrophication and river damming, contributes to making Cabomba
spp. invasive in many parts of the world (Mackey and Swarbrick 1997; Schooler et al.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
34
2009; Wilson et al. 2007). This study, which based on one seasonal cycle, indicates
dynamic patterns of aquatic vegetation with possible multiple states in the Lake Chini
ecosystem with the floods and nutrient dynamics as important drivers for shifts in
dominance. Continuing observation of the aquatic plant communities and the
environmental variables, however, will further illustrate the successional patterns in
this lake system. This is particularly relevant to C. furcata, as it appears to have the
ability to re-colonize and grow rapidly following a flood event, which may be linked to its
observed proliferation.
There is no prior knowledge of C. furcata being invasive in other countries. The
infestation of C. furcata in Lake Chini, if not controlled, may disrupt its ecosystem
function and impact its natural diversity. Continued research is essential in order to
recommend proper management measures. Further research should concentrate on:
1) nutrient cycling and exchange of nutrients between pelagic and littoral zones and
between lakes, (2) primary production of the main macrophytes and their relationship to
water quality, (3) role of flood variability on plant community structure, and (4)
alternative measures for sustainable rehabilitation and management of the lake
ecosystem to prevent further loss of plant diversity.
2.6 Acknowledgement
Funding for Z. Sharip was provided by the Malaysian Ministry of Natural Resources
and Environment scholarship. We thank Juhaimi Jusoh and Ahmad Taqiyuddin Ahmad
Zaki for acquisition of data, assistance during field experiments and the coordination of
financial support. The National Hydraulic Research Institute of Malaysia (NAHRIM)
provided data, and financial assistance for the field experiments. We thank Dr. Marti J.
Anderson for her statistical advice. Two anonymous reviewers contributed constructive
and informative comments and suggestions.
35
Figure 11: Conceptual model of ecological changes, feedback mechanisms and multiple states in Lake Chini. Dotted line indicate processes that can
move the system from one state to the other
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
36
Chapter 3 – Physical circulation and spatial exchange
dynamics in a shallow floodplain wetland2
3.1 Abstract
This paper examines spatial patterns of water exchange based on water temperature
variation between littoral and pelagic zones and compares the patterns in a series of
shallow lakes at different water levels. Exchange patterns were assessed by
developing isotherms along the transects and estimating the surface energy budget
using the vertical temperature profile and time-series measurements. Our results
indicate the presence of density-driven flow induced by the differential temperature
gradient between littoral areas, which are dominated by either floating-leaved or
submerged vegetation, and the open pelagic region. Persistent stratification was noted
in the narrower lakes, which is thought to be due to the presence of dense submerged
vegetation that attenuates wind-driven turbulence. In addition, variation of thermal
stratification and mixing dynamics between these lakes at different water levels has
corresponding effects on the biological and chemical regime. The circulation
contributes to increased transport of the phosphate that we believe could favour
submerged species and subsequently induce shifts of macrophyte community
composition. The results of this study have implications for the rehabilitation and
management of lake ecosystems.
Keywords: convective circulation, density driven flow, floating-leaved plant, Lake Chini,
shallow wetland, submerged macrophytes, thermal stratification, water exchange
2 Have been accepted in International Journal of Design, Nature, and Ecodynamics
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
37
3.2 Introduction
Convective circulation induced by density gradients resulting from horizontal depth
variation has been demonstrated to be an important exchange mechanism of
phosphorus (Horsch and Stefan 1988; James and Barko 1991), and mercury
(Palmarsson and Schladow 2008) between the littoral and pelagic zones, nutrients
between side embayment and the main basin of reservoir (Monismith et al. 1990), and
pollutants between a fringing wetland and lake (Nepf and Oldham 1997). A
temperature gradient develops when shallow littoral areas and deeper pelagic zones
receive the same incoming solar radiation but distribute it differently over their
respective volumes (Dale and Gillespie 1977b; Horsch and Stefan 1988; MacIntyre and
Melack 1995; Monismith et al. 1990). Several studies have also shown that aquatic
plants are able to induce convective motion by promoting differential shading and by
attenuating wind in shallower regions, which can further lead to horizontal and vertical
gradients in temperature (Coates and Ferris 1994; Dale and Gillespie 1977a; Herb and
Stefan 2004; Lovstedt 2008; Lovstedt and Bengtsson 2008; Nepf and Oldham 1997;
Waters 1998).
Studies on the convective exchange between vegetated littoral regions and pelagic
zones have been focused on emergent vegetation communities (Nepf and Oldham
1997) such as reed beds (Lovstedt 2008; Lovstedt and Bengtsson 2008) and Typha
stands (Waters 1998), and floating species such as Azolla spp. and Lemna spp.
(Coates and Ferris 1994). In all of these studies, a horizontal density gradient develops
as the surface water underneath or within the vegetation becomes colder than the
adjacent open water due to shading, and subsequently induces overflow of warmer
pelagic water along the surface towards the plant bed during the day. The resulting
horizontal temperature gradient induced by differential shading also differs with the
density of the vegetation bed (Lovstedt and Bengtsson 2008; Waters 1998).
From an ecological perspective, exchange flows generated by differential heating can
contribute to replacement of nutrients taken up by the macrophytes (Coates and Ferris
1994). However, despite the potential significance of this process in shaping the
ecological dynamics of wetland macrophyte communities, studies on the effect of
convective exchange induced by different types of macrophytes, for example rooted
floating-leaved plants or submerged species, have been limited. In an earlier study, we
identified differential nutrient gradients between the littoral and pelagic zones in Lake
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
38
Chini, a tropical floodplain wetland in Malaysia (Sharip et al. 2011a), and it was
hypothesized that this may have been influenced by temperature differences between
the two zones and associated exchange between them. In particular, the circulation
patterns induced by the thermal gradient could potentially regulate transport of
nutrients to dense submerged beds of the highly invasive macrophyte, Cabomba
furcata (Sharip et al. 2011a), and subsequently promote the proliferation of this species
due to its ability to uptake nutrients through stems and shoots (Wilson et al. 2007).
The aim of this study is to examine the convective exchange pattern resulting from
differential cooling and heating in a shallow floodplain wetland and its effect on water
quality dynamics in the system that could contribute to the shifts of macrophyte
community composition that have been previously documented (Sharip et al. 2011a).
Specifically, we identify how horizontal exchange flows are affected by dominance of
two different types of aquatic plants along the littoral areas and also investigate the
variation in the circulation pattern in two sub-basins in the wetland at different water
levels. This is achieved by (1) describing the spatial and temporal variations in thermal
structure, light climate and phosphate concentrations in the two lakes of the wetland
system during low- and high- water level or flooding, (2) estimating the surface energy
budgets and the convective flow rates between the littoral zone and open water at two
sites, and (3) using this information to assess the implications of physical-chemical
coupling to macrophyte responses and the density gradient induced by differential
shading by vegetation between the littoral and pelagic zones as an important
mechanism for transport of nutrients to C. furcata beds, and subsequently the
promotion of invasion of the species in the wetland system. This study also provides an
improved understanding of the water circulation induced by differential heating and
cooling in areas dominated by different types of aquatic plants, namely emergent
floating leaved plants versus submerged macrophytes.
3.3 Methods
3.3.1 Study site
Lake Chini, Malaysia, is a shallow wetland located within the Pahang River floodplain,
which exhibits characteristics of a system that suggest multiple ecological regime shifts
driven by flood and nutrient delivery (Sharip et al. 2011a). The wetland comprises a
series of 12 inter-connected lakes, has a total surface area of 1.69 km2 and an average
depth of 1.9 m [16], with its littoral areas extensively dominated either by stands of the
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
39
floating-leaved plant (Nelumbo nucifera) or submerged species (C. furcata). To
maintain water level for year-round navigability, a weir was constructed downstream
end of Chini River in 1995, which connects the wetland with the main river (Sharip and
Jusoh 2010; Shuhaimi-Othman et al. 2007).
3.3.2 Field measurements
Surveys were carried out on 19-24 April 2010 to investigate the exchange flows
between the littoral and pelagic region. Transects were positioned in two lakes; Lake 1
linking the open pelagic region to littoral area dominated by floating-leaved vegetation,
and Lake 12 linking pelagic zone to a littoral area dominated by submerged vegetation
(Fig. 1).
1
23
4
12
34
Lake 1
Lake 12
Lake 5
Figure 1: Lake Chini and location of temperature monitors (star)
Thermistor chains were deployed at two locations within the pelagic zone (Station 3
and Station 4) in Lake 1 and Lake 12 and at one location in Lake 5; each anchored at
the top on buoy and kept taut to the bottom by a weight. The three sites were selected
to represent lakes dominated by N. nucifera (Lake 1), dominated by C. furcata (Lake
12) and dominated by both species and subjected to direct flooding due to its close
proximity to the weir (Lake 5). Four TPS WP82 temperature-dissolved oxygen sensors
(TPS Pty Ltd, Brisbane Australia) were deployed at the littoral zone; one sensor was
deployed at the open water near the edge of the macrophyte bed at approximately 0.2-
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
40
m depth (Station 2), and another three sensors inserted at the top of benthic chambers
(Station 1) with a 12 V submersible pump used to re-circulate the water within the
chamber to maintain similar water conditions as outside. Thermistors recorded
temperatures at intervals and depth as in Table 1. Vertical profiles of photosynthetically
active radiation (PAR) and temperature-depth were made with a LiCOR sensor (Li-
192SA) and a YSI 6600 multi-parameter profiler. The temperature sensors were
calibrated together in a container at varying temperature, either before or after field
experiments. Temperature data were corrected where necessary with the mean
temperature so that the maximum differences between any loggers do not exceed
0.15oC. Linear interpolation was used to calculate hourly interval values where
necessary. Water samples were collected at surface- and bottom levels at each lake
for analysis of phosphate, nitrate and dissolved organic carbon in accordance with
standard methods (APHA 1992). Additional vertical profiles of temperature and light
were also carried out using YSI 6600 multi-parameter probe and LICOR sensor on 29-
30th March 2011 during a high water level period. The profiling was carried out around
mid-noon and early morning where differential heating and differential cooling would
likely to occur (Smith et al. 1995).
Table 1: Temperature monitors in Lake Chini
Sensor Parameter Recording
interval
(min)
Depth (m) Lake
Hobo
RBR
D-Opto
TPS sensors
Hydrolab
Temperature
Temperature
Temperature, DO
Temperature, DO
Temperature, DO, pH,
Chlorophyll
15
1
1
10-20
15
0.5, 1.0, 2.0
1.0
0.5
0.15-0.25
1.0
1,5,12
1,12
1,12
1,12
1,12
Hourly meteorological data were obtained from a weather station positioned in the
centre of Lake 1, and the Muadzam Shah meteorological station located about 40 kms
south of the study site. The on-lake weather station recorded solar radiation, wind
speed, air temperature, relative humidity, and precipitation. Due to the failure of the
wind speed and air temperature sensors, the wind speed and air temperature data
were collected from the Muadzam Shah Station. To include the localized lake-effect, air
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
41
temperature and wind speed values at the lake were calculated from the Muadzam
Shah Station using a linear regression between data from the two sites at times when
both were available. The air temperature and wind speed data between the on-lake
weather station and Muadzam Shah meteorological station were highly correlated
(r2=0.87, n=2880, p<0.001 and r2=0.53, n=356, p<0.001). Mean air temperature at
Lake Chini (26C) was significantly lower by 4.5% (t=15.1, df=5338.5, p<0.001) than
mean air temperature the Muadzam Shah Station, and this could be due to
microclimatic differences caused by the surrounding topography and the mediating
effect of the water-body.
3.3.3 Analysis of physico-chemical structure and heat budgets calculation
Spatial distribution of water temperature, and phosphate concentrations along the
transects were generated using SURFER (version 9.0; Golden Software, Inc.) with
kriging as the gridding method. Convective exchange patterns were assessed by
generating contours over the transects using the temperature data recorded by
thermistor probes and temperature-depth profile data measured over 45-min intervals
or less as described in Smith et al. (1995).
The atmospheric heat fluxes calculation were computed in Matlab R2008a (The
MathWorks) using a bulk aerodynamic approach applied to the available
meteorological data (MacIntyre et al. 2002; Tennessee Valley Authority 1972; Verburg
and Antenucci 2010). The two lakes were assumed to have similar meteorological
parameters. The overall heat budget calculation was calculated according to Lovstedt
and Bengtsson (2008):
.0
0 QsensibleLatentnet
h
P HHHRzt
TC
(1)
where, ρ0 is the density of water (kg/m3), Cp is the specific heat capacity for water,
4.18x103J/(kg K), h is the water depth (m), ∂T is the average temperature change (oC)
over the time step, ∂t (s), z is the vertical distance from surface (m), Hlatent is the heat
loss by latent heat fluxes (W/m2), Hsensible is heat loss by sensible heat transfer (W/m2),
and HQ is the lateral heat flux between the open water and the vegetation bed. The
incoming net solar radiation, Rnet (W/m2), was calculated according to:
.ionbackradiatlongwaveshortwavenet HHHR (2)
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
42
where the short wave radiation is estimated as:
.)1( inshortwave SH (3)
Here Sin is the short wave incoming radiation (W/m2), α is the albedo or the reflectance
of the solar radiation and was taken as 0.05 from water surface (Shaw 1994) and 0.16
from the floating-leaved, water lily (Cooley and Idso 1980). The incoming long wave
radiation and the long wave back radiation was calculated according to:
.)17.01(42
awalongwave TCH (4)
.)/(642.0 7/1
aaa Te (5)
.4
wionbackradiat TH (6)
where σ is the Stefan-Boltzman constant (=5.67x10-8 W K-4 m-2), εa is emissivity of air,
ea is the vapour pressure of the air (Pa), C is the fraction of cloud cover, Ta is the air
temperature (K), Tw is the surface water temperature (oK) and ε is the surface
emissivity (=0.97 for water (Shaw 1994) and =0.98 for the aquatic plant vegetation
(Lovstedt and Bengtsson 2008)).
The sensible and latent heat fluxes, Hsensible and Hlatent, were estimated using the bulk
aerodynamic transfer method based on the wind speed and specific humidity gradient.
To address the strong effect of the thermal inertia of the water over the diel scales
(MacIntyre et al. 2002), neutral values of the transfer coefficients at 10 m,
CDN=1.0x10-3, CHN=1.35x10-3 and CEN=1.35x10-3 (MacIntyre et al. 2002), were
corrected for non-neutral atmospheric stability effects at the relevant measurement
height following Monin-Obukhov similarity theory (Amorocho and DeVries 1980;
MacIntyre et al. 2002). In this study, sensible heat transfer coefficient (CH) was
assumed the same as latent heat transfer coefficient (CE) in keeping with the literature
(Imberger and Patterson 1990; MacIntyre et al. 2002; Verburg and Antenucci 2010).
The roughness length for momentum was considered in the formulation of the stability
functions for stable conditions (Imberger and Patterson 1990) with a cut-off of stability
parameter, |zL-1|<15 imposed following the limits set in Imberger et al. (1990). The
stability calculations were iterated until the Monin-Obukhov length scale (L), which is a
ratio of the reduction of potential energy as a result of wind mixing and the
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
43
development of atmospheric stratification due to the heat flux, converged to within
0.001% between iterations (MacIntyre et al. 2002; Verburg and Antenucci 2010).
The exchange flow, Q (m3 s-1m-1) is derived from Lovstedt and Bengtsson (2008):
.. 0 QTTCLH plantopenPQ (6)
We assume the energy fluxes within the littoral bed were distributed evenly. To
eliminate the influence of density gradient induced by depth variation, heat fluxes were
calculated based on temperature measurements between Station 1 and Station 2 in
each lake. The estimation of the heat fluxes covered the whole one-day cycle for Lake
1 and only the differential heating (day) phase in Lake 12 due to sensor failure. To
check the reliability of the lateral heat flux estimation, the averaged-temperature as a
function of time was calculated at Station 2 using the atmospheric surface fluxes for the
open water and lateral heat fluxes transported from Station 1, and compared with the
measured temperature data (20-min interval) in the area (Lovstedt and Bengtsson
2008).
The dissolved oxygen dynamic pattern will be described elsewhere. Vertical
attenuation coefficients were calculated using the formula in Kirk (1983) to evaluate
light availability for submerged macrophytes. Analysis of means and T-Tests were
performed in PASW Statistic 18 (SPSS Inc.).
3.4 Results
3.4.1 Meteorology and physical-chemical structure
The weather during the April 2010 experiment was at its driest condition with no outflow
as lake level was lower than the weir height. The skies were occasionally cloudy but no
rainfall was recorded during the two days thus inflows into the lakes were negligible. No
information of groundwater was available to account for the temperature differences
however this is thought to have a negligible influence. Wind speed was generally low
during the days with an average wind speed of around 0.8 m/s. Wind speeds were near
zero throughout the nights (Fig. 2a).
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
44
19/04 20/04 21/04 22/04 23/040
1
2
3
4
5
Win
d s
peed (
m/s
)
19/04 20/04 21/04 22/04 23/04
25
30
35
40
Tem
pera
ture
(oC
)
Lake 1 Lake 12
Figure 2: Variations in (a) wind speed (b) air temperature and surface water
temperature at Lake Chini during the experiment period in April 2010.
Air temperature cooled from a maximum of 30.4C at 1600 h on 20 April to 23.7C at
0600h on 21 April (Fig. 2b). Air temperature was lower than the surface water
temperature (measured at 0.5 m from surface) in both lakes, which has been frequently
observed in tropical lakes and wetlands (Furtado and Mori 1982; Ganf 1974; MacIntyre
and Melack 1984; MacIntyre et al. 2002; Verburg and Antenucci 2010). According to
Verburg and Antenucci (2010), the lower air temperature than the surface water can
cause an increase in atmospheric instability and subsequently an increase in sensible
and latent heat loss and affect differential heating and cooling of the surface the water.
High temperature within the littoral zone vegetation dominated by the floating-leaved
plant, N. nucifera, was consistent with past studies (Coates and Folkard 2009). The
surface water temperature in the littoral area dominated by N. nucifera (Station 1)
reached 1.3C warmer than the adjacent open water (Station 2), which could be due to
sparse N. nucifera cover (13%) in the area and shallower depth for heat absorption.
Mean surface water temperatures were higher than the mean air temperature at the
littoral and pelagic zones in both lakes (p<0.001). Mean temperature differences
between the water-plant surface and the air were higher in the littoral zone of Lake 12
compared to Lake 1, with values of 5.4 and 4.9C, respectively. Higher surface
temperatures above submerged beds could be associated to absorption of solar
radiation at the upper part of the water column. Differential heating during the day was
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
45
apparent along both transects generating overflows from shallow littoral region to the
pelagic zone as shown by the slanting contour in Fig. 3a and Fig. 3b. A weak
metalimnion, as represented by the 31.8C to 32.6C contours, develop in Lake 1 at
the pelagic region between the 0.5- and 1.0-m depths. Around noon on 20th April,
differential heating began to develop in Lake 12, as the water temperature at the littoral
(Station 1) was nearly 2C greater than those in the upper 0.5 m layer of the pelagic
water at Station 4 (Fig. 3b).
Figure 3: Longitudinal and vertical variations in water temperature on 21st April in (a)
Lake 1 at around 1535, (b) Lake 12 at around 1220, (c) Lake 1 at around 0954, (d)
Lake 12 at around 1750. Numbers and bars at top temperature profile correspond to
station.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
46
The surface water temperature cooled more rapidly at the littoral site compared to the
pelagic zone in both lakes during the night between 20 - 22 April 2010. Movement of
cooler littoral water as an underflow current into the deeper pelagic zone is shown by
the position of the 30.7C isotherm (Fig. 3c). In Lake 12, the littoral area cooled sooner
than the pelagic water which could be due to shading by the high-canopy forest where
movement of cooler water starts to develop by late afternoon. Intrusion of cool water
appeared to move away from the lake bed in Lake 12 as shown in the slanting contour
at the surface (Fig. 3d), which could be associated to the presence of a dense
monospecific submerged macrophyte bed (Station 3). The water at the surface and
bottom layer also remained separated at Station 3 (Fig. 4c), which was in contrast to
the pelagic zone (Station 4) (Fig. 4d) where the surface layer was completely mixed
with the bottom layer.
16:48 19:12 21:36 00:00 02:24 04:48 07:12 09:36 12:00 14:24 16:4828
30
32
34
T (
oC
)
Lake 1 - Station 3
Surface (0.5 m)
Bottom (1.0 m)
16:48 19:12 21:36 00:00 02:24 04:48 07:12 09:36 12:00 14:24 16:4828
30
32
34
T (
oC
)
Lake 1 - Station 4
Surface (0.5 m)
Mid- (1.0 m)
Bottom (2.0 m)
16:48 19:12 21:36 00:00 02:24 04:48 07:12 09:36 12:00 14:24 16:4828
30
32
34
T(o
C)
Lake 12 - Station 3
Surface (0.5 m)
Bottom (1.0 m)
16:48 19:12 21:36 00:00 02:24 04:48 07:12 09:36 12:00 14:24 16:4828
30
32
34
T (
oC
)
Lake 12 - Station 4
Surface (0.5 m)
Mid- (1.0 m)
Bottom (2.0 m)
(c)
(d)
Figure 4: Variation in water temperature between the littoral zone and pelagic zone on
20-21 April 2010 (Lake 1) and on 21-22 April 2010 (Lake 12)
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
47
Over the daily cycle, stratification and vertical mixing patterns were clearly different
between the lakes (Fig. 5). A pattern of diurnal stratification during the day and
complete mixing at night were apparent in Lake 1 and Lake 5, whereas stratification
persisted in Lake 12, with the exception on the morning of 22 April, where the mixed
layer did not reach 2-m. As the magnitude of the wind stress was similar throughout the
period, the lower solar radiation on the previous days (mean=252.8 W/m2) may have
contributed to the deepening of the mixed layer depth to the 2-m layer. A similar
phenomenon was described by (MacIntyre and Melack 1988).
Figure 5: Thermistor time series at the pelagic zone, at (a) Lake 1 (b) Lake 5, and (c)
Lake 12 between 20-24 April 2010.
In contrast to the thermal structure during low water level, a distinct pattern of
stratification was observed in both Lake 1 and Lake 12 during high water level (Fig. 6).
Stratification persisted in Lake 1 with heat been entrained at the upper layer above the
1.5 m depth causing strong metalimnion to develop between the 0.5 and 1.5-m depths
(Fig. 6a). Heat loss during the night induces cooler and denser surface temperature
which led to deepening of the surface mixed layer by morning as shown by the
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
48
reference contour (26oC) (Fig. 6b). Conversely, the temperature structure in Lake 12
indicates that the littoral area experienced isothermal mixing that induced differential
temperature between the littoral zone and the pelagic zone and the subsequent
intrusion of cold water into the stratified pelagic water (Fig. 6d). Shading by high
canopy forest along lake fringes could contribute to isothermal littoral temperature at
the littoral zone. Steedman et al. (1998) showed that riparian shading reduces the
littoral water temperature and this can cause unstable density gradient to develop as
dense cold water sinks to the bottom (Folkard 2008).
Differences in light penetration were apparent between the low- and high water periods
in both lakes (p<0.001). During low water periods, PAR reached ca. 0 µmols-1m-2 near
the bottom of the submerged stands (Station 3). As qualitatively observed in Lake 12,
wind-driven motion was attenuated over the dense submerged C. furcata stand where
its shoots and floating-leaves covering the surface water. The vertical attenuation
coefficient, Kd (PAR) in Lake 12 (Kd= 1.54 m-1) was not statistically higher (p>0.01) than
in Lake 1 (Kd= 1.47 m-1) during this period, which in contrast to high water period where
Kd (PAR) in Lake 1 (Kd= 2.92 m-1) was significantly higher (p<0.001) than in Lake 12
(Kd= 1.61 m-1). Higher Kd (PAR) in Lake 12 during low water level could be attributed to
humic substances generated by decomposition of plant matter [26]. This is consistent
with mean DOC concentration which were higher in Lake 12 (74.6 ± 5.7 mg/L)
compared to Lake 1 (33.8 ± 25.5 mg/L). The direct inflow of the turbid water of Pahang
River and Gumum River into Lake 1 (Sharip pers. observation) could contributed to
high Kd (PAR) in this lake during the high water period which reduce light availability for
submerged C. furcata. Mean turbidity in Lake 1 (43.1±24.0 NTU) was significantly
higher than Lake 12 (5.2±3.6 NTU) (p<0.001). Higher mean turbidities above 30 NTU in
this lake were associated to flooding by the Pahang River (Shuhaimi-Othman et al.
2007).
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
49
Figure 6: Longitudinal and vertical variations in water temperature in Lake 1 at around
1540 h on 29th March, at 0820 h on 30th March, and in Lake 12 at 1400 h on 29th March
and at 0910 h on 30th March 2011.
In both lakes, phosphate concentrations were high in the littoral areas as compared to
the pelagic zone (Fig. 7a and Fig. 7b). Phosphate concentration in both lakes
increased with water level (Fig. 7c and Fig. 7d). The pattern of phosphate
concentration in Lake 1 during high water level shows that phosphate concentrations
were higher at Station 3, which is along the deepest area of Lake 1 where the Gumum
River flows. Gumum River, which provides the main outflow from the heavily
agricultural catchment areas, could be the source for the high phosphate concentration
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
50
in this lake. Higher phosphate concentration near the substrate in Lake 12 during high
water period could be associated to nutrients release from sediments or mineralisation
of litters (Carpenter 1980; Shilla et al. 2006).
Figure 7: Longitudinal and vertical variations in phosphate concentration (mg/L) in Lake
1 on (a) 22nd April 2010, (b) 29th March 2011, and in Lake 12 on (c) 22nd April 2010, (d)
29th March 2011
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
51
3.4.2 Heat budget and water exchange
The boundary layer above the air-water interface was unstable (zL-1<0) over the period
of 20-23 April 2010 (Fig. 9a & Fig. 9b) causing a higher transfer coefficient than neutral
values (Fig. 9c & Fig. 9d). As transfer coefficients were a function of wind speed, drag
(CD) and heat exchange (CH and CE) coefficients increases as wind increases and z/L
decreases, and, according to MacIntyre et al. (2002), as exchange coefficient increase
buoyancy effects becomes larger and tend to dominates. The hourly averages of the
sensible heat fluxes were small compared with past studies in prairie wetlands [36] and
ranged between -41W/m2-4W/m2. Strong sensible heat fluxes (H) were found mostly in
the early morning. Evaporative heat losses (E) were high during noon and late
afternoon with a maximum value of -270W/m2 in Lake 1 and -208 W/m2 in Lake 12 (Fig.
9e & Fig. 9f). Net radiation reached 790 W/m2, and was an important heat flux that
influences the heating and cooling of the water.
Using the method in Verburg and Antenucci (2010), where roughness lengths of
momentum for smooth flow were used to parameterize the transfer coefficient for wind
speed less than 5 m/s (Smith 1988), mean E were found lower by 9% in Lake 1 and
7.3% in Lake 12 while H was higher by 1.2% in Lake 1 and 3.8% in Lake 12. As the
solar energy from the incoming solar radiation during the day was still larger than these
atmospheric surface fluxes, the stratification and horizontal density gradient were
therefore primarily controlled by differential heating induced by solar insolation.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
52
21/04 22/04 23/04 24/04 25/04-20
-10
0
10
z/L
21/04 22/04 23/04 24/040.000
0.002
0.004
0.006
Tra
nsfe
r coef.
CH CD
21/04 22/04 23/04 24/04-300
-200
-100
0
Surf
ace f
lux (
W/m
2)
E
H
LW
21/04 22/04 23/04 24/04 25/04-20
-10
0
10
z/L
21/04 22/04 23/04 24/040.000
0.002
0.004
0.006
Tra
nsfe
r coef.
CH CD
21/04 22/04 23/04 24/04-300
-200
-100
0
Surf
ace f
lux (
W/m
2)
E
H
LW
21/04 22/04 23/04 24/04
0
500
1000
Net
flux (
W/m
2)
Net f lux total surf ace f lux
21/04 22/04 23/04 24/04
0
500
1000
Net
flux (
W/m
2)
Net f lux total surf ace f lux
Figure 9: Air column stability, z/L in (a) Lake 1 and (b) Lake 12; Heat (CE) and
momentum (CD) transfer coefficient corrected for atmospheric stability in (c) Lake 1 and
(d) Lake 12; surface heat fluxes for the open water in (e) Lake 1 and (f) Lake 12.
Surface heat flux components: sensible heat (H), latent heat (E) and net long wave
radiation (LW), and net heat fluxes in the open water in (g) Lake 1 and (h) Lake 12. Net
heat fluxes components: total surface flux (sum of E, H and LW) and net heat flux.
The water temperature distribution within the floating-leaved plant bed was based on
the average temperature from the three sensors that spread along the transect in the
littoral areas (Station 1). The horizontal temperature difference over the study period
was more than 1oC/m for 37% of the time during the day and 25% of the time during
the night. This means the two areas could be recurrently circulated by the convective
currents. We adopted similar approach as in Smith et al. (1995) and Stefan et al.
(1989) in estimating the lateral heat fluxes by simplifying that the exchange flow by
differential heating occurs in the upper half of the water column and a return flow at the
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
53
bottom. Correspondingly, the exchange flow by differential cooling was assumed to
occur in the lower half of the water column with surface return flow. The atmospheric
heat fluxes and lateral heat transfer between the pelagic and littoral zone in Lake 1 is
shown in Fig. 10a. The measured and calculated depth-averaged temperature (Fig.
10b) indicates that the calculated temperature was reasonably predicted by the heat
budget estimation especially during the differential heating period (p<0.001). Wind
speeds and atmospheric temperature were lowest during the night which led to a highly
unstable boundary layer that could enhance vertical transport and affect the estimation
of the latent and sensible heat fluxes.
The floating-leaved vegetation also affects the energy budget by altering the solar
radiation penetration into the water by surface absorption during the day and lowers the
evaporation heat loss from the surface water (Shaw 1994). Correspondingly, the
estimation of the latent heat fluxes has the largest uncertainties (Lovstedt and
Bengtsson 2008) as plant surfaces not only evaporate but also transpire depending on
the vapor pressure of the surrounding (Shaw 1994). The evapotranspiration over the
plant surfaces depend on the physiological aspect of the species (Lafleur 1990).
N. nucifera has through-flow system which provides efficient transport of convective
flow of gases (Konnerup et al. 2011), subsequently complicates the calculation of the
latent and sensible heat fluxes.
The water exchange between the littoral region covered by aquatic plants and the open
water were derived from the lateral heat flux estimation, which is the heat difference
between the surface heat fluxes and the measured temperature changes. Our results
show the presence of a weak convective current due to differential heating and cooling
between littoral and pelagic zones. The mean lateral heat fluxes were approximately -
155 W/m2 and 160 W/m2 during mid-afternoon and early morning respectively. This
corresponds to a mean current of 1.6 cm/s induced by differential heating between the
floating-leaved N. nucifera stand and open water (Lake 1), and 1.9 cm/s induced by
differential cooling. This result is consistent with findings by Coates and Folkard (2009),
who found weak thermally-driven motion within the littoral zone induced by shading by
the floating-leaved Nymphaea alba based on measurement of the turbulence field
within the vegetative littoral zone (VLZ). To confirm our estimation of the current flow,
the horizontal velocity scale for the vertically mixed water column as described by
Monismith et al. (1990) was calculated, and the velocity of the convective current by
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
54
differential heating was approximately 1.4 cm/s, which is close to the calculated
velocity based on the surface energy budgets.
14:24 19:12 00:00 04:48 09:36 14:2428
30
32
34
T (
oC
)
14:24 19:12 00:00 04:48 09:36 14:24-400
-200
0
200
400
Heat
Flu
x (
W/m
2)
(a)
14:24 19:12 00:00 04:48 09:36 14:2428
30
32
34
Time of the day
T (
oC
)
(b)
Figure 10: (a) Heat fluxes within the floating-leaved bed on 20-21 April 2010. Heat flux
components: net radiation (dashed line), sensible heat (dotted line), latent heat (thin
line) and lateral heat (solid line). (b) Measured temperature (solid line), and calculated
temperature (star) at open water and littoral temperature (dotted line)
By estimating the hydraulic residence time (t=V/Q) according to Stefan et al. (1989),
the results suggest that the mean areal convective flow induced by differential cooling
and heating could exchange the whole volume of water within the floating-leaved bed
in 1 h and 1.5 h respectively. In contrast to Lake 1, the convective current due to
differential heating was smaller in Lake 12, with a mean velocity of 0.3 cm/s.
3.5 Discussion
3.5.1 Temperature structure and water exchange
Steep temperature gradients were observed between the littoral and pelagic areas in
this floodplain wetland and contributed to the convective circulation between the two
zones. Surrounding topography and macrophyte abundance in the system influenced
the onset and pattern of differential heating and cooling between lakes. Shading by
riparian forest has been shown to reduce littoral temperature in boreal lakes (Steedman
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
55
et al. 1998), and the early onset of differential cooling at the littoral area of Lake 12
could be associated to the high-canopy forest surrounding the lakes causing early
movement of cooler water towards the pelagic zone. Depth variation and shape of the
lake contributed further to the pattern of differential heating and cooling, resulted to
overflows from shallow littoral region to the pelagic zone during the day and movement
of cooler littoral water as an underflow current into the deeper pelagic zone during the
night (Horsch and Stefan 1988; Monismith et al. 1990). Pattern of movement of cool
water in this lake appears to be shaped by the presence of thick monospecific stands
of a submerged macrophyte. Compared to findings by Herb and Stefan (2004), our
study shows the presence of dense submerged vegetation affects the circulation
pattern induced by the horizontal density gradient.
Stratifications were marked in both lakes during high water level. In contrast to Lake 1,
where stratification persisted at both littoral and pelagic zones by the morning period,
pattern of isothermy observed in Lake 12 at the littoral zone during high water level
could be induced by shading by riparian forest. Few studies have shown the role of
shape and surrounding topography in influencing lake stratification and mixing regime
(MacIntyre and Melack 1984; Melack 1984) which could explain the thermal pattern in
this wetland. Similar patterns of persistent thermal stratification have been documented
in other floodplain lakes in the Amazon River during high water level (Coates and
Folkard 2009; MacIntyre and Melack 1984; Melack 1984). Marked differences of the
light climate in Lake 1 during high water level could be associated with increased
turbidity in the water column, contributed largely from flooding by the turbid Pahang
River (Shuhaimi-Othman et al. 2007). Increased turbidity probably induces temperature
stratification, where penetration of solar radiation reduced to a smaller depth with
surface temperature rise as more heat absorbed at the upper water column and the
bottom temperature falls and becomes colder (Imberger and Patterson 1990).
The estimated flow at the littoral was different between sites due to the different
vegetation effects. Generally, floating-leaved species would alter the amount of
radiation entering the water column by physically covering the water surface with its
leaves (Folkard and Coates 2010). The interception of the radiation would reduce the
depth averaged temperature within the water column (Lovstedt and Bengtsson 2008).
Higher littoral temperature within the floating leaved bed could be attributed to the low
percent cover by N. nucifera floating leaves over the surface water. In addition, N.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
56
nucifera stands have emergent leaves, with stems elongated above the water, and this
may affect the light climate. The presence of a dense monospecific stand of C. furcata
enhances daytime stratification in the water column as has been observed in past
studies (Coates and Ferris 1994; Dale and Gillespie 1977a). The plant leaves
underneath the water surface may have prevented light penetrating deeper into the
water column, causing cooler temperatures to develop relative to the pelagic zone
(Coates and Ferris 1994). Surface water above the macrophytes has higher
temperature as a result of attenuated wind-driven mixing and interception of solar
heating at the surface water (Coates and Ferris 1994; Monismith et al. 1990). The
water surface temperature between 0900 – 1800 h was on average 2.5oC warmer in
the littoral zone dominated by submerged species. Temperature gradients of more than
1oC/m would give rise to density differences that can significantly reduce both vertical
and horizontal mixing (Stefan et al. 1989).
The horizontal density flow found in this work was within the rates of convective
currents caused by differential heating and cooling as estimated in past studies; 1 cm/s
between open water and stands of Typha (Waters 1998), 1.5-2.8 cm/s between open
water and reed beds (Lovstedt 2008; Lovstedt and Bengtsson 2008), 3-5 cm/s between
the wetland and lake (Nepf and Oldham 1997), and 2-3.5 cm/s (Palmarsson and
Schladow 2008) and 0.4-11 cm/s (Monismith et al. 1990) between shallower and
deeper water. It should be emphasized that the estimation of the exchange flow in this
study were based on Monin-Obukhov similarity theory which breaks down as wind
speeds decrease to nearly wind-less free convection (Beljaars 1995; Deardorf 1972)
and this could have an effect on the night-time heat flux calculations. Some cautions
are necessary on the values of the estimated current induced by differential cooling as
heat flux calculation during the night rely on latent and sensible heat fluxes under low
wind conditions. Further study is necessary to estimate the heat flux under free
convection within the floating-leaved stand using reliable wind speed measurement
over the water-plant surface at the littoral zone and to determine the associated
exchange flow between vegetated and open water during cooling period.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
57
3.5.2 Implications of physical-chemical coupling to macrophyte dynamics
The temperature structure implies a potential feedback mechanism, which could
support the occurrence of alternative states. Reduced floating leaf cover allows
increased heating of the water and the high temperatures and mortality would then
increase decomposition and nutrient release. This nutrient release could promote
submerged C. furcata to grow within the N. nucifera bed.
The induced horizontal density gradient could improve transport of phosphate from the
littoral area to other areas in the pelagic zones. The circulation pattern provides an
increase in dispersion of nutrient allowing for the growth of submerged macrophytes
within the area. As Cabomba populations can uptake nutrients through stems and
shoots (Wilson et al. 2007), the improved nutrient delivery to submerged macrophyte
bed in other areas by horizontal transport may promote the proliferation of submerged
C. furcata in the wetland. The undercurrent may transport nutrients to submerged C.
furcata that grow in deeper pelagic areas (Sharip et al. 2011a) during the night and
early morning, and the available resource could be used by the plant for
photosynthesis during the day for its growth, increasing its abundance.
Additionally, the increase in water column turbidity and thermal stratification in this
wetland, in particular, during the flooding by the main river could lead to anoxic
conditions and subsequently an increase in nutrients. Pattern of persistent thermal
stratification in other floodplain lakes during high water level caused anoxia (Melack
and Fisher 1983) and elevated concentrations of nutrients (MacIntyre and Melack
1988). Anoxic conditions near surfical sediment would likely enhance P-mobilization
(Boers and Zedler 2008) and have the potential to contribute to internal eutrophication
due to enhanced P release from sediments. High phosphate concentrations in the two
lakes during high water level were attributed by different sources of nutrient with run-off
from agriculture area (Shuhaimi-Othman et al. 2007) that flows into the nearby river
and mineralisation of the dominant submerged plant litters (Carpenter 1980; Shilla et
al. 2006) possibly explains the elevated phosphate level in Lake 1 and Lake 12
respectively. The availability of nutrients in the lake after flooding could contribute
further to elevated abundance of submerged macrophytes in the system (Sharip et al.
2011a). The thermal structure in floodplain lakes during low- and high water affects the
oxygen and nutrient dynamics in the water column (Melack and Fisher 1983; Monismith
et al. 1990), which could be an important factor shaping the productivity in the wetland
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
58
system. Further study should investigate the oxygen dynamic, which is influenced by
the temperature structure as shown by numerous studies (MacIntyre and Melack 1988;
Melack and Fisher 1983), and how it relates to production by the macrophyte in this
wetland.
3.6 Conclusion
This study documents the contribution of aquatic vegetation to thermal structure and
water exchange dynamics. The horizontal density gradient may also be affected by
rooted floating-leaved vegetation and submerged vegetation. Floating-leaved
vegetation creates shading and alters the light climate that could induce convective
motion while submerged vegetation affects the light and temperature pattern by
reducing light penetration, increasing stratification and altering the circulation pattern
which affects the water quality in the lakes. A rise in the water level altered the thermal
gradient and the exchange dynamics and mixing in the lake system and the variation in
physical characteristics of the lake affected the temperature and convective circulation.
This horizontal density gradient and water exchange has important implications for
nutrient cycling in this shallow lake system. A change of macrophyte dominance from
floating leaved to submerged macrophyte affects the physical circulation and exchange
flow and contributes towards improved delivery of constituents such as phosphate and
other nutrients to C. furcata beds. The increased availability of resources could further
promote growth of this submerged species and subsequently contributes to invasion in
the wetland system. The findings from this study have implications for the rehabilitation
and management of the wetland.
3.7 Acknowledgements
The first author gratefully acknowledges the support from National Hydraulic Research
Institute of Malaysia (NAHRIM) for permission to use their data and provision of
financial assistance for the field experiments. Thanks to Ahmad Taqiyuddin Ahmad
Zaki for his assistance and coordination during all field surveys and Justin Brookes for
provision of sensors and assistance during April field experiment.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
59
Chapter 4 – Metabolism differences among habitat and
macrophyte communities in a tropical lake3
4.1 Abstract
Aquatic macrophytes differ in their primary productivity and their responses to
environmental changes which in turn modify their biological processes specifically their
eco-physiological dynamics. Different macrophyte species have different growth and
respiratory rates (i.e. metabolism) and this is reflected in the amount of dissolved
oxygen (DO) produced or removed and subsequent changes in DO dynamics in the
water column. This study assessed the dynamics of DO concentration fluctuation
between wetland habitats dominated either by Nelumbo nucifera or Cabomba furcata,
with the aim of estimating the primary production and respiratory rates of the two main
aquatic macrophyte communities in the system. The study adopted benthic chambers
to measure the process rates of benthic metabolism of the macrophyte communities,
including determination of the contribution of microflora and microphytobenthos (MPB)
to the total production of the C. furcata community bed. The free-water metabolism
estimation method was also to look at net ecosystem scale production and respiration
in the littoral and pelagic zones of sub-lakes dominated by the different vegetation
communities. The gross primary productivity (GPP) for the littoral area dominated by
N. nucifera and C. furcata communities were slightly different 3.07 ± 0.48 g O2 m-2d-1
and 3.55 ± 0.34 g O2m-2d-1. The MPB had lower mean GPP and higher community
respiration (R) rates (478.1 mg O2 m2 h-1 and 363.7 mg O2 m
2 h-1 respectively) than C.
furcata (562.7 mg O2 m2 h-1 and 100.3 mg O2 m2 h-1). The free water metabolism
estimation shows the littoral zone in Lake 1, dominated by the floating-leaved species,
was autotrophic (GPP/R>1) while the littoral zone in Lake 12, dominated by the
submerged vegetation, was heterotrophic (GPP/R<1). The pelagic zones in both
lakes, however, were heterotophic. An increase in abundance of the invasive
submergent C. furcata into the pelagic zone increased community production and
respiration and affected net ecosystem production.
3 To be submitted to Hydrobiologia Journal
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
60
Keywords
Aquatic plants, benthic-pelagic coupling, diel oxygen dynamic, community metabolism,
macrophyte productivity, microphytobenthos
4.2 Introduction
Macrophytes that grow along depth gradients are important ecological components of
productive wetland ecosystems (Wetzel 1992a; Wetzel 1992b), and can shape aquatic
habitat and strongly control ecosystem processes (Rasmussen et al. 2011). Past
studies have shown that emergent vegetation and epiphytic algae on submerged plants
contribute the largest contribution to the overall productivity in many wetlands (Barko et
al. 1977; Howardwilliams and Allanson 1981; Ikusima 1978; Ikusima and Furtado 1982;
Wetzel 1992a; Wetzel 1992b). Macrophyte production is defined as the rate of the
amount of organic carbon produced by plants per unit area (Westlake 1963). The
organic matter produced by aquatic macrophyte productivity subsequently affects the
dissolved oxygen (DO) dynamics in the water column and these changes are often
used to measure variability in the net metabolism of the wetland (Barko et al. 1977;
Howardwilliams and Allanson 1981; Ikusima and Furtado 1982; Penfound 1956; Wetzel
1992a; Wetzel 1979).
Macrophytes with different structure, morphology and physiology respond differently to
the surrounding environment which controls their gross primary production and
respiration. Emergent and floating-leaved species utilise solar energy for
photosynthesis and uptake atmospheric carbon dioxide and release oxygen into the
atmosphere through their internal stomata (Cooke et al. 2005; Longstreth 1989;
Schulthorpe 1967; Wetzel 1990), and subsequently persistent low DO levels were
found in the surface water under their canopies (Caraco and Cole 2002; Frodge et al.
1990). In contrast, submerged macrophytes, with their thin and dissected submerged
leaves, depend on the supply of carbon from the water, either in the form of dissolved
carbon dioxide or bicarbonate ions (Sand-Jensen 1987; Schulthorpe 1967), and they
can produce more oxygen in the water (Caraco et al. 2006; Goodwin et al. 2008;
Hamilton et al. 1995; Melack and Fisher 1983; Takamura et al. 2003).
According to Quinn et al. (2011), native or non-native species of the same life form also
respond differently to the environment due to their inherent differences in ability to
capitalize on anthropogenic disturbance. This functional trait causes variation in a
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
61
species response to environmental change, which can either contribute to ecosystem
stability or trigger further functional modification (Chapin et al. 1997). Ecosystem
processes, such as productivity, are therefore expected to change as a result of
alteration in species composition (Chapin et al. 1997).
Vegetation dynamics have been reported in Lake Chini, Malaysia between the two
dominant species, the native floating-leaved Nelumbo nucifera and the non-native
submergent Cabomba furcata with a possible shift in macrophyte dominance from
floating-leaved to submerged species (Sharip et al. 2011a). Further assessment of the
productivity of the dominant species (Sharip and Jusoh 2010; Sharip et al. 2011a) will
provide better understanding of the changes in the vegetation and the consequential
alteration of biological processes due to the presence of the non-native species in this
wetland.
To our knowledge no previous research has investigated the primary production of C.
furcata in introduced areas in Malaysia such as in Lake Chini. Populations of a closely
related species, Cabomba caroliniana, in introduced areas were reported to differ from
populations in native ranges (Schooler et al. 2009); they frequently develop thick
monospecific stands (Schooler et al. 2009; Wilson et al. 2007) like many other wetland
invaders (Zedler and Kercher 2004). Studies that have examined the impact of
ecosystem processes by non-native species within the introduced range are also
limited (Ehrenfeld 2010).
Diel changes in dissolved oxygen (DO) are influenced by not only physical and
chemical processes, but also the biological processes of the biotic communities (Kemp
and Boynton 1980; Melack and Fisher 1983). Caraco and Cole (2002) showed the
contrasting impacts of native and non-native species to DO dynamics in their habitat.
As invasive plants have been indicated to respond to the influx of resources by
increasing their growth rates (Zedler and Kercher 2004), the altered ecosystem
processes affect the DO signal in the water column. Therefore, understanding the DO
dynamics can give a better assessment of the macrophyte community metabolic rates,
and the ability for C. furcata to increase abundance and exert dominance in the
system.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
62
In this study, we 1) describe the DO dynamics and the associated water quality in Lake
Chini, Malaysia; 2) estimate net productivity and respiratory rates of the communities
dominated by a native floating-leaved species (N. nucifera) and an introduced
submerged macrophyte (C. furcata); 3) estimate the microflora and microphytobenthos
(MPB) production within the C. furcata bed; and 4) estimate the net ecosystem
production in lakes dominated by N. nucifera (Lake 1) and C. furcata (Lake 12). The
study is focused on the productivity of the two macrophyte communities during their
early growth phase, which is after the monsoon season in particular, since C. furcata
seems to have increased its growth from the previous year‟s flood pulse (Sharip et al.
2011a).
4.3 Methods and materials
4.3.1 Experimental design and water quality measurements
Two sets of benthic metabolism experiments were performed at Lake Chini, Malaysia
on 19th-23rd April 2010 using benthic chambers and in-situ DO loggers. The first
experiment was set up to study the habitat and macrophyte community primary
production over a diurnal cycle in two differing lakes; Lake 1 is dominated by N.
nucifera (floating-leaved) and Lake 12 is dominated by C. furcata (submerged species).
The second experiment was set up to study C. furcata metabolism in particular, and to
separate the production and respiration signal of the plants from the production and
respiration of MPB and sediment microorganisms within the littoral zone of Lake 12.
The experiment took place on 22 April 2010 between the periods of 10 am to 6 pm.
Free water DO measurements were obtained by deploying a several oxygen loggers,
both within the littoral and pelagic zones of each lake, and this data was subsequently
used to estimate net ecosystem metabolism rate, described below. In addition, pH and
chlorophyll concentration were recorded by the multi-parameter probe at the centre of
each lake. The locations of the experiments and type of sensors used and parameters
measured are detailed in Chapter 3.
Water samples were collected at all sites and analysed for PO4, NO3, NO2, total
phosphorus, total nitrogen, DOC and chlorophyll-a concentration following APHA
(1992). At the end of 24 h cycle, additional water samples were only collected from the
benthic chambers dominated by N. nucifera and analysed for PO4, NO3, NO2, total
phosphorus, total nitrogen and DOC. Water samples were not collected from the
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
63
benthic chambers dominated by C. furcata due to failure of the battery connecting the
pumps to the chambers.
4.3.2 Benthic metabolism (specific processes, small scale)
4.3.2.1 Benthic chamber deployments
In the littoral areas, benthic chambers consisting of Perspec domes with an internal
base diameter of 28.5 cm and volume of approximately 10 L, were used in triplicates
(Aldridge et al. 2009). They were gently pushed into the substrates to avoid sediment
disturbance in each lake. A 12-V submersible pump was used to re-circulate the water
within the chambers. The TPS WP82 sensor was inserted into the top of each chamber
to measure DO and temperature at 20-minute intervals to capture a complete day-night
cycle. At the end of the 24 hrs, vegetation from each chamber dominated by C. furcata
was harvested and dried to constant weight, while benthic chambers from the littoral
areas dominated by N. nucifera were removed and re-deployed at another sites
dominated by C. furcata to estimate the effect of C. furcata plant biomass. At the end of
the second experiment, vegetation were also harvested from chambers containing C.
furcata plants and dried to constant weight.
4.3.2.2 Estimates of diurnal productivity
Net ecosystem productions (NEP) and community respiration (CR) of the littoral
macrophytes were estimated based on oxygen differences between the initial and final
concentrations (mmol O2 m-2 h-1) in chambers as described in Bott et al. (1978) and
Longphuirt et al. (2007): NEP (or R) O2 = ΔO2 V / s. Δt, where ΔO2 is the change in DO
(mg L-1), V is the volume of water enclosed by the benthic chamber (L), s is the surface
area (m2), and Δt is the incubation time (min). NEPday were calculated for each 20 min
interval from 60 min past dawn to 20 min before dusk. We calculated R for every 20
min interval from 20 min before dusk until 60 min past dawn and divided the results by
time length (h) to produce estimates for hourly rate of ecosystem respiration during
night-time. This study assumed that Rday is equal to Rnight, and the hourly rates were
multiplied by 24 hours to estimate Rdaily. GPP is the sum of Rday and NEPday and
NEP=GPP-Rdaily.
4.3.2.3 Estimates of MPB respiration and production
The DO changes in chambers at sites with bare sediments (ie. vegetation removed)
were compared with chambers at sites with sediment and C. furcata plants; together
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
64
the data was used estimate the difference between sediment microflora and MPB, and
C. furcata production. The chambers were left for 3 hours under light conditions and
then covered with black plastic for dark incubations for another 3 hours. Net production
was estimated based on the increase in oxygen under light condition and community
respiration was calculated based on the decline in oxygen under the dark condition.
NEP and R for MPB were estimated for each 20 min interval over the 3 h light- and
dark- incubation period respectively. GPP for C. furcata was calculated as the
difference between the GPP in chambers having plants, and chambers without plants.
4.3.3 Net ecosystem metabolism
4.3.3.1 Diel oxygen measurements
In the littoral water, a TPS WP82 DO-temperature sensor was deployed at about 20 cm
below the surface. In the pelagic waters, sondes were deployed at two sites at each
lake in pelagic waters (Sharip et al. 2011b) to measure the free water DO. A D-Opto
logger (Zebra-Tech Ltd, Nelson, New Zealand) and a multi-parameter profiler-hydrolab
model DS5X (Hach environmental, CO, USA), were deployed at approximately 0.5-m
depth and 1-m depth respectively. The sondes were first deployed at Lake 1 for two-
days for simultaneous oxygen and temperature measurements, and then redeployed to
Lake 12 to record similar data over a two day period.
4.3.3.2 Estimates of free water metabolism
We estimated metabolism for the pelagic zone from the oxygen signal using a similar
method as described in Hanson et al. (2003) and Lauster et al. (2006). This method
assumes NEP20min=ΔO2-D, where ∆O2 is the change in oxygen concentration over 20
min, and D is the gas exchange through diffusion in this period estimated as D=k (O2-
O2sat). NEPday were calculated for each 30 min interval from 30 min past dusk until 30
min before dawn to reduce the error. Estimation of D is based on the assumption of a
vertically well-mixed epilimnion over the survey period. The oxygen exchange
coefficient, k was calculated from a gas piston velocity K600 and Schmidt numbers (Sc)
according to Jahne et al. (1987) and Staehr et al. (2010b). As the wind speed during
the experiment was very low (Sharip et al. 2011b), K600 were estimated using the low
wind equation of Cole and Caraco (1998). We assume a neutrally stable boundary
layer and use the wind speed referenced to 10 m height above the surface.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
65
We calculated R for every 30 min interval from 30 minute past dusk until 30 min before
dawn and divided the results by time length (h) to produce estimates for the hourly rate
of ecosystem respiration during the night-time. The half-hour buffers were considered
to reduce the estimation errors in R due to inflection in gas curve around dusk and
dawn (Hanson et al. 2003) and the interference from photosynthesis at low light
(Markager and Sand-Jensen 1989). During darkness, GPP=0 and the change in
oxygen is the sum of respiratory at night and air-water exchange through diffusion.
During the day, the change of oxygen is caused by the difference between GPP,
daytime R and D. Similarly, Rday is assumed to equal to Rnight, and the hourly rates were
multiplied by 24 hours to produce Rdaily (Cole et al. 2000; Hanson et al. 2003; Lauster et
al. 2006). The sum of NEPday and Rday provide the GPP for mixed layer metabolism.
4.3.4 Data analysis
Production and respiration rates were converted to carbon units following the method
described in Bott (2007) and using the photosynthetic quotient for tropical habitats of
1.35 (Westlake 1963) and respiratory quotient of 0.85 (Furtado and Mori 1982). GPP
for C. furcata was converted to dry weight unit by dividing with the average biomass
(DW/m2). All analyses of means and test of differences were performed in PASW
Statistic 18 (SPSS Inc.).
4.4 Results
4.4.1 Oxygen fluxes and water quality measurement
Diel changes of DO in benthic chambers were apparent in both lakes (Figure 1),
regardless of whether they were dominated either by the submerged species or
floating-leaved plants. Diel DO changes between the two sites showed that the rates
of oxygen consumed were increased in the littoral communities. The reduction in DO
concentrations from noon to evening were apparent in the littoral area dominated by
submerged species with depletion of oxygen in all chambers during the night and early
morning. Rapid increases in DO shortly after dawn were not detected even though
dissolved CO2, produced by respiratory activities during the night, would likely be large
in the chambers. DO concentrations during the day were correlated to solar radiation
due to plant photosynthetic requirements with sharp increases in DO concentrations in
all chambers from morning to noon. DO fluxes at littoral areas within the floating-leaved
stands changed more dramatically with solar radiation due to the littoral community‟s
direct exposure to sunlight. DO fluxes in the submerged bed tended to stabilise during
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
66
noon after it reached the DO level at the air-water interface. Mean DO concentration in
chambers at sites dominated by N. nucifera was 3.0±1.9 mg/L, significantly higher
(t=9.6, df=424, p<0.001) than the mean DO concentration in chambers at sites
dominated by C. furcata which was 1.4±1.6 mg/L.
-100
0
100
200
300
400
500
600
700
-50
0
50
100
150
200
250
14:52 19:40 00:28 05:16 10:04 14:52
So
lar
rad
iati
on
(W
/m2)
O2μ
mo
l li
ter
-1
Time of day (h)
Nn1 Nn2 Nn3 Cf1 Cf2 Cf3 FW Solar
Figure 1: Diel DO measurement; Nn1, Nn2, Nn3 (sondes deployed in benthic
chambers within N. nucifera bed), Cf1, Cf2, Cf3 (sondes deployed in benthic chambers
within C. furcata bed), FW (sonde deployed at free water in the littoral area).
DO values in chambers between Lake 12 with and without plants (C. furcata) showed
significant differences between light and dark incubations (p<0.001) (Figure 2).
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
67
0
20
40
60
80
100
120
140
10:33 12:21 14:09 15:57 17:45
02 µ
mo
l li
ter-
1
Time of day (h)
Cfwp1 Cfwp2 Cfwp3 Cfwo1 Cfwo2 Cfwo3 FW
Figure 2: Diel DO measurement; Cfwp1, Cfwp2,Cfwp3 (sondes deployed in benthic
chambers with plant), Cfwo1, Cfwo2, Cfwo3 (sondes deployed in benthic chambers
without plants), FW (sonde deployed at free water in the littoral area)
The amplitudes of the changes in DO concentrations in free water were significantly
differed between littoral and pelagic areas (p<0.001) (Figure 3a). Higher DO values
were found in Lake 1 at 0.5m depth. Conversely, the amplitudes of DO concentration in
pelagic water of Lake 12 showed a different trend between the two depths. A higher
DO amplitude at 0.5-m depth could be associated to the presence of dense submerged
macrophytes stand. Mean DO in pelagic zone in Lake 1 was 7.4±0.5 mg/L, also
significantly higher (t=35.9, df=672, p<0.001) than the mean DO in pelagic zone in
Lake 12 which was 5.7±0.8 mg/L. DO concentrations at all sites were correlated with
temperature (r = 0.598, p<0.001).
Significant differences between lakes were apparent in chlorophyll concentration and
pH values (p<0.001). Time series profile in the pelagic zone at 1-m depth also showed
higher variability in pH and chlorophyll concentration in Lake 1 compared to Lake 12
(Figure 3b and Figure 3c). Differences in mean chlorophyll concentrations and pH were
much lower in the pelagic zone of Lake 12 (t=75.8, df=224, p<0.001) and (t=51.3,
df=216, p<0.001). The mean chlorophyll-a concentration, however, was higher in Lake
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
68
12 (7.6 ± 5.1μg/L), compared to Lake 1 (5.4 ±1.2 μg/L) with highest chlorophyll-a
concentration found near the dense C. furcata beds.
Differences in PO4, NO3, NH4 and DOC concentration before and after diel cycle at
Lake 1 were not statistically significant (p>0.05). Mean above-ground dry weights for C.
furcata was 23.5 g DW/m2.
20/04 21/040
100
200
DO
(um
ol/L)
Lake 1
0.2m
0.5m
1.0m
22/04 23/040
100
200
DO
(um
ol/L)
Lake 12
0.2m
0.5m
1.0m
20/04 21/044
5
6
7
pH
22/04 23/044
5
6
7
pH
20/04 21/040
5
10
Chl (u
g/L
)
22/04 23/040
5
10
Chl (u
g/L
)
Figure 3: Sondes measurement in the pelagic zone on 19th - 21st April 2010 (Lake 1)
and on 21st – 23rd April 2010 (Lake 12), (a) diel DO concentration (μmol/L) (b) pH (c)
chlorophyll concentration (μg/L)
4.4.2 Diurnal productivity
Lowest values of NEP were found at the littoral area compared to the pelagic zone in
both lakes. NEP at littoral sites dominated by N. nucifera and C. furcata bed were
negative (Table 1). Lower GPP in sites dominated by the native N. nucifera (3.07 ±
0.48 g O2 m-2 d-1) was not statistically different (p>0.05) from GPP in sites dominated
(a)
(b)
(c)
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
69
by the non-native C. furcata (3.55 ± 0.34 g O2 m-2 d-1). We found NEP was much less
negative in sites dominated by the submerged species, which is comparable with the
study by Lauster et al. (2006). Both littoral zones dominated by either the floating-
leaved species or submerged vegetation were heterotrophic (GPP/R<1) while the
pelagic zones were autrotophic (GPP/R>1).
Table 1: Diurnal productivity estimated from the benthic chamber deployments. Error
bars are ± SD
Parameter GPP,
g O2 m-2 d-1
(g C m-2 d-1)
R,
g O2 m-2 d-1
(g C m-2 d-1)
NEP,
g O2 m-2 d-1
(g C m-2 d-1)
GPP/R Mean
T
- Lake 1
N. nucifera
3.07 ± 0.48
(0.85 ± 0.03)
4.02 ± 0.17
(1.28 ± 0.06)
-0.93
(-0.42)
0.77
31.2
- Lake 12
C. furcata
3.55 ± 0.34
(0.99 ±0.10)
3.73 ± 0.75
(1.19 ± 0.24)
-0.17
(-0.20)
0.97
31.7
4.4.3 MPB and microflora respiration and production
The mean GPP in sites having the combined C. furcata, microphytobenthos and
sediment community were higher (p<0.01) compared to the mean GPP measured from
sites with bare sediments and MPB (i.e., vegetation removed). Comparison between
sediments and C. furcata showed MPB and microflora had a lower mean NEP (p<0.01)
compared to C. furcata. In contrast, the MPB and microflora bed had a higher
respiration rate (p<0.05) compared to C. furcata. Photosynthetic activity by C. furcata
contributed to higher DO in chambers having macrophytes. Lower DO in chambers of
bare sediments (without plants), specifically during the night, indicates higher DO
consuming activities. The GPP and R of C. furcata were 562.7 mg O2 m-2 h-1 (23.9 mg
O2 g-1 DW h-1) and 100.3 mg O2 m2 h-1. The value of the GPP obtained using this
method is much higher than the simple technique method (Vollenweider 1969), which
calculate NEP and R based simply on changes in DO concentration between initial DO
values and final DO values (light- and dark- incubation). The GPP calculated using the
equation of Vollenweider (1969) was 62.5 mg O2 m-2 h-1.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
70
Table 2: Comparison of MPB/sediment vs C. furcata productivity. Error bars are ± SD
Parameter GPP,
mg O2 m-2 h-1
(mg C m-2 h-1)
R,
mg O2 m-2 h-1
(mg C m-2 h-1)
NEP,
mg O2 m-2 h-1
(mg C m-2 h-1)
C. furcata + sediment
+ MPB
1040.8 ± 158.5
(331.8 ± 44.0)
464.0 ± 184.4
(147.9 ± 51.2)
576.9 ± 140.6
(160.2 ± 39.1)
Sediments + MPB 478.1 ± 208.7
(152.4 ± 58.0)
363.7 ± 148.9
(115.9 ± 41.4)
114.4 ± 129.3
(31.8 ± 35.9)
C. furcata 562.7 100.3 462.4
4.4.4 Free water productivity
The estimated k600 in this study was at the average of 0.55±0.06 (SE). We used a
constant value of 0.55 m d-1 as the basis for the diffusion calculation. This value is
about 10% larger than the values used in past studies (Lauster et al. 2006). Few
studies have shown the uncertainties in the estimation of k (Staehr et al. 2010a), an
over estimate in k resulted in an underestimate of R, which would affect NEP but this
error was more apparent in an unproductive lake. Tropical swamps, such as Lake
Chini, are a highly productive systems (Howard-williams and Gaudet 1985; Ikusima
and Furtado 1982; Sharip and Jusoh 2010; Westlake 1963), so this study does not
investigate variability in errors of k. Air-water exchanges were low in both lakes with
mean diffusion 0.15 g O2 m-2 h-1 in Lake 1 and 0.18 g O2 m
-2 h-1 in Lake 12.
The mean NEP for both the littoral and pelagic zone was positive for both lakes. In the
pelagic zones, GPP in Lake 12 was higher (p<0.05) than GPP in Lake 1. In the littoral
zones, GPP in Lake 12 was lower (p<0.05) than GPP in Lake 1. The ratios of GPP/R
were negative in Lake 12 in both littoral and pelagic zones which indicates
heterotrophy. While in Lake 1, the ratio of GPP/R was negative in the pelagic zone and
positive in the littoral zone.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
71
Table 3: Gross primary production (GPP), respiration (R) and NEP for littoral and
pelagic sites in free water. Error bars are ± SD
Parameter GPP,
g O2 m-2 d-1
(g C m-2 d-1)
R,
g O2 m-2 d-1
(g C m-2 d-1)
NEP,
g O2 m-2 d-1
(g C m-2 d-1)
GPP/R Mean
T
Littoral
- Lake 1
- Lake 12
8.19
(2.28)
4.10
(1.14)
7.71
(2.46)
-2.37
(-0.76)
0.48
(-0.18)
6.48
(1.90)
1.06
-1.72
31.1
30.7
Pelagic
- Lake 1
- Lake 12
1.81
(0.50)
3.69
(1.02)
-1.91
(-0.61)
-0.94
(-0.30)
3.72
(1.11)
4.63
(1.32)
-0.95
-3.95
31.8
30.8
4.5 Discussion
4.5.1 Oxygen fluxes and water quality dynamic
Diel DO dynamics in the benthic chambers were evident in both lakes indicating the
metabolism of the benthic communities in producing and consuming DO. The decrease
in DO concentration in chambers having the submerged C. furcata communities was
more rapid due to the contribution of microphytobenthos within the communities that
depleted DO in the chambers. Formation of fluffy organic-rich sediments through plant
litter contributed to higher rates of decomposition of organic matter (Esteves et al.
1994) that consumes DO. Reduced DO at the sediment-water interface could caused
DO to be exhausted in chambers after periods longer than 12 h (Ibarra-Obando et al.
2004). The lags of DO after sunrise could be associated with a high consumption of DO
by decomposition of organic matter exceeding phosynthetic activities by the two plant
species under low light conditions.
Lower amplitude of diel DO in the pelagic waters were driven by wind-induced mixing.
However, wind speeds were mostly low (<2 ms-1) in this wetland (Sharip et al. 2011)
which could contribute to low air water exchanges and under-saturation of DO. Similar
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
72
under-saturation values have been reported in other floodplain lake, the Lake Calado
(Melack and Fisher 1983). Correspondingly influx of DO from the atmosphere could be
suggested as major source of DO (Melack and Fisher 1983) in this wetland.
Temperature is one of the main environmental factors regulating photosynthetic
process (Sand-Jensen 1989). Our study shows strong correlation between temperature
and DO concentration consistent with past studies (Staehr and Sand-Jensen 2007;
Staehr et al. 2010b). High temperature decreases the DO solubility and has a strong
effects on the metabolic rates including increases respiratory rates (Cooper 1975;
Howard-williams and Gaudet 1985; Rasmussen et al. 2011) and GPP (Rasmussen et
al. 2011). Higher surface temperature at the littoral areas (Sharip et al. 2011) could
partly explain the high community respiration at these sites.
Diel variability of pH in the pelagic water of Lake 1 suggested a productive system
where photosynthethic activities exceeded respiration during the day resulting in
increases in pH (Cole and Prairie 2010). Dominant respiratory activities during the night
decreases pH (Cole and Prairie 2010). Steady pH values ~5 were observed throughout
the day in Lake 12. Esteves et al. (1994) found a similar lack of diel pattern in pH
values in Lake Mussura, Amazon, and suggested the homogeneous pattern in pH
values was attributed to the lower thermal stability of the water column and smaller
phytoplankton biomass. This low pH value is within the range of pH preferred by other
Cabomba species (Schooler et al. 2009). Many studies have shown that pH and
dissolved CO2 were correlated with Cabomba abundance (Camargo et al. 2006;
Sanders 1979; Schooler et al. 2009; Tarver and Sanders 1977). Lower pH increases
dissolved CO2 availability and subsequently increases Cabomba biomass and
abundance (Schooler et al. 2009).
Lake 1 indicates diel variation of the chlorophyll concentration time series which could
be attributed to the phytoplankton photosynthetic activites (Esteves et al. 1994).
However, higher chlorophyll-a concentrations over the transect in Lake 12 also
suggests the contribution of the attached algae and utricularia-periphyton assemblages
in the total primary productivity.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
73
4.5.2 Diurnal productivity
This study provides estimation of the photosynthetic and respiratory rates of the two
studied aquatic plant species communities during the early growth period. The findings
of this study shows that NEP were consistently negative in the littoral areas in both
lakes, which implies that the littoral zone consumes more organic matter and
subsequently tending toward a net heterotrophy (Lauster et al. 2006; Van de Bogert et
al. 2007). The positive NEP at the pelagic areas implied that this area tends toward net
autotrophy, and this compares with results by Barbosa et al. (1989), Lauster et al.
(2006) and Van De Bogert et al. (2007).
Our findings shows littoral communities dominated by submerged C. furcata vegetation
has higher mean GPP and lower mean R than littoral communities dominated by N.
nucifera, which could be due to higher abundance of the introduced species (Sharip et
al. 2011). The mean biomass of the submerged species were 10-fold than the mean
biomass of the floating-leaved vegetation. The dense monospecific stands of C. furcata
could explain this high above-ground biomass compared to floating-leaved species
where biomass accumulates in the rhizome. Dense communities of submerged
macrophytes and attached algae have high rates of photosynthesis in light and
respiration in the dark (Sand-Jensen 1989). Martin et al. (2007) also found higher
community respiration by invasive Crepidula fornicata species in European Bays in
sites having a high density stand (>1000 individuals/m2). Lower mean R in C. furcata
sites was associated to depletion of DO in the chambers by early morning period.
The GPP of C. furcata within its native sites, based on incubation of isolated shoot
method, ranged between 6.5-17.5 mg O2 g-1 DW h-1 (Camargo et al. 2006). In this
study, mean GPP for C. furcata communities, which was based on an in-situ oxygen
exchanges in light and dark enclosures, was much higher (23.9 mg O2 g-1DW h-1) than
the GPP within its native areas. The higher values could be associated to higher
production in the introduced areas, however, the DO fluxes measured was not
corrected for contribution by the attached algae or periphyton which could affect the
actual calculation.
4.5.3 MPB and microflora respiration and production
In the second experiments at the C. furcata sites, higher GPP in chambers having the
submerged macrophytes compared to chambers with bare sediment could be
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
74
contributed by the plant‟s photosynthetic activities. Conversely, higher respiration in
chambers having bare sediments indicated the strong contribution of the
decomposition of organic matter and respiration by microphytobenthos and microflora
community in the sediment. Sediments at C. furcata sites were fluffy, consisted
probably by clumps of masses containing detritus, algal mat and utricularia-periphyton
communities.
Utricularia spp. have been found to co-occur with C. furcata in many parts of this
wetland and were highly correlated with the submerged species (Sharip unpublished
data) and have been reported to form large clumps in tropical wetlands (Ikusima and
Furtado 1982; Lim and Furtado 1974; Schulthorpe 1967) and subtropical swamps
(Bosserman 1983; Greening and Gerritsen 1987). Utricularia mass reached maximum
density during the dry season in Tasek Bera, another shallow lake located about 50 km
away from Lake Chini (Lim and Furtado 1974). Heavily attached with rich epiphytic
algal community (Ikusima and Furtado 1982), this mass appeared brown and starts to
senesce in April (Lim and Furtado 1974) and could contribute to fluffy masses in this
system. This high organic matter decomposition consumes more oxygen which
contributes to higher respiratory activity. Algal mats have been shown to differ with
over-story vegetation with net primary productivity varying between 0.8 to 1.4 times of
the vascular plant (Zedler 1980). However, the NEP ratio of sediment communities,
including the algal mat, to C. furcata was only 0.25.
4.5.4 Free water productivity
This study confirms previous findings that differences in types of macrophytes can
contributed to metabolism differences among lakes (Caraco and Cole 2002; Lauster et
al. 2006). In addition, the results indicate that biotic communities affect the ecosystem
processes (Chapin et al. 1997). According to Ehrenfeld (2010), process rates would be
affected by the alteration in the abundance of species that differ in their structure and
traits. As C. furcata and N. nucifera have different structure, morphology and
physiology, the increasing abundance of C. furcata in the system (Sharip et al. 2011)
could contribute to modification of the plant‟s primary productivity and the overall rate of
carbon fixation in the system.
The results in this study shows both pelagic and littoral zones in Lake 12 which were
dominated by C. furcata, appeared to be heterotrophic (GPP/R<1) at the time of
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
75
sampling. Hanson et al. (2003) associated heterotrophy to high mean DOC exceeding
> 10 mg/L. Mean DOC concentration was found to be higher in Lake 12 (Sharip et al.
2011), which could contribute to this heterotrophy condition. However, limited data
caused insignificant correlation between NEP and DOC and other nutrient variables to
associate the heterotrophy to DOC. Higher GPP and R in the littoral zone of Lake 1
could be caused by higher advection associated to convective motion or movement of
water by a nearby river.
Our study assumed mixed layer metabolism in the pelagic zone. Recent studies have
shown that metabolism can be affected by physical processes such as internal waves
(Hanson et al. 2008; Kemp and Boynton 1980; Melack and Fisher 1983) and
microstratification (Coloso et al. 2010) at smaller scales of minutes to hours. These
physical processes were not quantified in this study and could affect the estimates of
metabolism in the pelagic zone.
The results of this study showed that the GPP and biomass accumulation were higher
in C. furcata bed than the N. nucifera stand. Increasing abundance and density of C.
furcata in many parts of the lake basins (Sharip et al. 2011) indicates that C. furcata is
increasing its production rates. Although our results support the assertion that the
wetland is shifting to submerged macrophyte dominance (Sharip et al. 2011) based on
the growth rate of the non-native species, quantifying the wetland response to shift of
macrophyte dominance and ecosystem succession requires long-term measurements
of the macrophyte growth (Staehr and Sand-Jensen 2007) spanning over decade
timescales (Carpenter and Lodge 1986).
4.6 Conclusion
This study is the first comparison of primary production between N. nucifera and C.
furcata communities in Lake Chini, Malaysia. This study also provides the first
estimation of production rates of the submerged C. furcata in its introduced range. The
results of this study indicate that the benthic communities are an important component
structuring the oxygen dynamics and subsequently the water quality in the system. The
high rate of carbon fixed by the introduced species, C. furcata into the sediment
indicates that the species is affecting further the ecological processes and may be a
contributing factor related to its increasing dominance in the system.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
76
4.7 Acknowledgements
The first author gratefully acknowledges the support from National Hydraulic Research
Institute of Malaysia (NAHRIM) for provision of data and financial assistances for the
field experiments.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
77
Chapter 5 – General discussion and conclusion
This thesis provides a better understanding of the current state of macrophyte
composition in Lake Chini, Malaysia, with a particular focus on the factors that
contribute to the relative abundance of the native floating-leaved macrophyte N.
nucifera and the invasive submerged macrophyte C. furcata. The impact of the physical
and biological processes that contribute to shifts in dominance of these macrophytes
when invasive species are present was also assessed in two studies. This chapter
summarises and discusses the results of these studies focusing on the characterisation
of macrophyte composition, physical and biological properties of the lake system, and
the associated management implications. Overall, this thesis contributes to an
improved understanding of the ecosystem processes that control the shift of
macrophyte dominance.
5.1 Summary of research findings
Chapter 2 placed the present issue of invasion in the context of the changes in Lake
Chini, Malaysia from 1975 to 2007. Conversion of lands to agricultural areas has
occurred and surface water phosphate concentrations have increased. In addition, in
1995 a weir was constructed in Chini River, downstream of the lake, and water level
fluctuations have subsequently reduced. This could cause a significant reduction of N.
nucifera communities as observed in the literature. Since a large flood of 2007, N.
nucifera has returned to the lake and C. furcata has spread widely to the lake sub-
basins. Currently, the plant communities were found to be highly variable in the lakes,
both spatially and temporally, potentially driven by flood and nutrient dynamics. The
main environmental variables that were found to affect their composition were depth,
nutrient concentration and sediment type.
The results presented in Chapter 2 also indicated that invasion by C. furcata strongly
associated to the overall plant community assemblages, with plant diversity decreasing
as the abundance of C. furcata increases. The observation that C. furcata biomass
increased after the monsoonal season suggests that C. furcata can establish quickly
after flooding events and may become increasingly abundant. Based on this data a
conceptual model of variation in ecological processes was developed. This model
indicated that possible alternate states can exist where the lake becomes dominated by
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
78
either the N. nucifera or C. furcata, and the changes in dominance of these species
and the associated feedback mechanism that shapes the stable states are influenced
by flooding regimes and nutrient concentrations. Recurrence of flooding creates a
turbid and low nutrient environment that could provide the feedback that gives N.
nucifera advantage over C. Furcata, while low water fluctuation and nutrient-rich waters
could provide the feedback for C. furcata to become dominant over N. nucifera.
The results from Chapter 3 indicate that both N. nucifera and C. furcata contribute to
the thermal structure and water exchange dynamics of the wetland system. The
floating-leaves of N. nucifera created shading that produced a differential temperature
gradient between littoral areas and open pelagic regions. This temperature differential
induced a density driven flow. The dense monospecific stands of C. furcata increased
stratification and appeared to alter the circulation pattern by causing changes in
movement of cool water intrusion, and improved delivery of constituents to other C.
furcata beds.
The water exchange dynamics of the wetland system was also influenced by patterns
of horizontal and vertical mixing dynamics. The horizontal mixing dynamics were
affected by the physical characteristics of the lake, including its shape, depth and
surrounding topography, which influenced the onset of differential cooling and heating.
The vertical mixing pattern changed during high-water periods with marked increases
in turbidity and thermal stratification. Also, phosphate was observed to increase
possibly due to run-off from agriculture areas, mineralisation of the dominant
submerged plant litters during high-water period and internal eutrophication.
Chapter 4 compared the gross primary productivity (GPP) of the littoral areas and the
overall lake production. The microphytobenthos associated with C. furcata communities
had lower mean rates for Net Ecosystem Production (NEP) and higher mean rates for
community respiration (R). The production rate of C. furcata in this system, as
measured using an in-situ oxygen exchange in light and dark enclosures, was higher
than the production rate of C. furcata reported in its native areas using an incubation of
isolated shoot method.
The overall lake production indicates higher NEP in Lake 12, which was dominated by
the C. furcata than in Lake 1, which was dominated by N. nucifera. In this study, Lake
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
79
12, was heterotrophic (GPP/R<1) in both littoral and pelagic zones while Lake 1 was
heterotrophic (GPP/R<1) in the littoral zone and autrotophic (GPP/R>1) in the pelagic
zone. An increase in abundance of C. furcata throughout the pelagic zone increased
community production, R and NEP.
5.2 Discussion
This study hypothesises that dynamic vegetation in the Lake Chini ecosystem has
possibly two alternate stable states that are dominated by either N. nucifera or C.
furcata. These alternative states are thought to be influenced by the flood regime and
resource availability in this floodplain wetland. According to the conceptual model of
ecological processes that was developed, if natural flow could be re-established in this
system, the stable state dominated by N. nucifera would be more likely to predominate
as this macrophyte can better tolerate flooding and fluctuating water levels than C.
furcata. The flushing out of available nutrients by high magnitute and high frequency
floods, and the increased duration of turbid environments may weaken invasion of this
submerged species by limiting both the light and nutrients availability for its growth.
This process which weakens C. furcata growth, provides an internal feedback
mechanism that can strengthen N. nucifera dominance. In contrast, the increase in
nutrient availability as a result of continuing landscape alterations and reduction in the
flushing out of available nutrients by a reduction in flood magnitude as a result of fixed
structures or weir, may strengthen the potential for invasion by C. furcata. These
processes which strengthen C. furcata growth provide an internal feedback
mechanisms that weaken N. nucifera dominance and sustain the invaded state. Other
studies have shown the importance of internal feedbacks mechanism in sustaining
ecosystem states (Scheffer and Carpenter 2003; Suding et al. 2004; Suding and Hobbs
2009; Zedler 2009). In Zedler (2009), for example, invasion of Phalaris arundinacea
could be reduced when feedbacks that maintain the natural state such as processes
that thicken sedge meadow canopy and diminish the potential for seedling
establishment is strengthened while invasion of Phalaris arundinacea could be
increased when feedbacks in the sedge meadow state is weakened. Further studies
should explore and test the potential feedback mechanisms that drive the alternate
stable states in this system.
C. furcata was more dominant and more widespread than N. nucifera in the sub-basins
of this wetland. C. furcata also appeared to be adapted to annual flooding events,
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
80
which implies that the invasive species could grow more rapidly than N. nucifera
following a flood event due to abundance of available nutrients. The ability of C. furcata
to adapt to annual flooding, quickly re-establish biomass and uptake nutrients from
water and sediments are attributes that may contribute to its invasive capacity. Studies
have shown that species with multiple attributes such as these have enhanced
invasiveness (Zedler and Kercher 2004). In contrast, N. nucifera dominated in lake
sub-basins that were closer to the weir and were therefore more directly affected by the
floods. The presence of the weir reduces the frequency of small to medium magnitude
floods into the wetland. Floods that exceed the weir height and are short in duration will
reach the nearby lakes where N. nucifera is abundant.
The results of this study shows the importance of water depth and sediment type in
influencing the macrophyte composition and structure of Lake Chini, which are
consistent with past findings. Water depth and substrate type have been identified as
some of the key environmental factors that affect Cabomba abundance in Australia
(Schooler and Julien 2006; Schooler et al. 2009). Fluctuating water levels have also
been found to sustain the dominance and seasonal variations in Nelumbonaceae in
temperate lakes and ponds such as Lake Kasumigaura (Nohara and Tsuchiya 1990),
Ojaka-ike Pond, Chiba Japan (Kunii and Maeda 1982), Old Woman Creek, Lake Erie
(Whyte 1996) and Volga Elta, Russia (Baldina, Leeuw et al. 1999).
From the results in Chapter 2, it is shown that invasion by introduced C. furcata affects
plant community composition and reduces diversity. This is consistent with numerous
studies that have shown the negative effect of invasion on diversity (Kercher and
Zedler 2004; Schooler et al. 2006). This decrease in diversity could lead to positive
feedbacks that ultimately lead to community collapse (Simberloff and Von Holle 1999),
enhanced invasion and facilitate further increases in abundance of invasive species
(Hobbs and Huenneke 1992; Schooler et al. 2006). The replacement of specific
species that differ in their environmental responses could further reduce ecosystem
resilience (Ehrenfeld 2010) and trigger irreversible shifts towards monospecific
communities (Folke et al. 2004).
This study also shows that eutrophication is a concern in Lake Chini since phosphate
concentrations were consistently high in these wetlands. This is consistent with past
studies (Sharip and Jusoh 2010; Sharip and Yusop 2007; Shuhaimi-Othman and Lim
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
81
2006). In other temperate wetlands, eutrophication pressures have also been shown to
make aquatic ecosystems more susceptible to invasion (Galatowitsch et al. 1999;
Zedler and Kercher 2004).
The results from Chapter 3 and Chapter 4 have important implications for the
management of wetland ecosystems. Macrophyte presence affected not only the
thermal structure of the ecosystem but also the pattern of physical circulation in the
system. The temperature structure affects the DO dynamic and contributes to internal
eutrophication and nutrient release from sediment. The physical circulation induced by
the horizontal density gradient can facilitate the transport of nutrients that promote the
growth and abundance of submerged invasive macrophytes. The increase in C. furcata
abundance as a result of rapid production rates further alters the thermal structure and
physical processes. Herb and Stefan (2004) have shown that submerged macrophytes
attenuate wind and increased stratification, which diminishes the wind-induced forcing
and increases thermal-induced forcing. This maybe is a possible positive feedback
mechanism for C. furcata that enables it to increase its dominance.
This study highlights the importance of understanding the historical context and system
dynamics of wetland ecosystems before recommending management or restoration
measures. Based on the vegetation dynamics found in this study, it can be
hypothesised that the Lake Chini wetlands have some resilience to alternate states of
dominance and may not reach the dynamic threshold limit causing an irreversible shift
or novel ecosystem. Further studies are required to determine the resilience of the
wetland to shifts in dominance and quantify the dynamic threshold limit of the
ecosystem. This study also contributes to an improved understanding of how physical-
chemical-biological processes interact in shallow floodplain wetlands. All of these
processes need to be considered in order to ensure successful management
measures.
Overall, the description of macrophyte dynamics presented here provides further
evidence of the complexity of the wetland ecosystem and its susceptibility to change as
a result of invasion by invasive species. Chapter 3 and 4 show that ecoystem
processes are influenced by changes in C. furcata dominance. The Cabomba
population has been naturalised in Malaysia (Chew and Siti-Munirah 2009) and have
been found in many parts of the country (Chew and Siti-Munirah 2009; Salim et al.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
82
2009). Since its introduction C. furcata was likely to be a passenger in Lake Chini
where it probably proliferates under favourable conditions. However, the construction of
the weir and the resulting hydrological changes in this system, and ongoing landscape
changes and the resulting increase in resource availability has provided the ecological
niche for increased growth of C. furcata. Under these conditions, C. furcata is more
competitive than N. nucifera. The high production rates enable C. furcata to rapidly
increase its biomass with availability of nutrients and expand its coverage in the
wetland. In addition, the presence of dense C. furcata stands could affect the physical
circulation and provide better spread of nutrients for its advantage. Therefore, the
ecosystem processes identified here suggest that C. furcata in Lake Chini is possibly
changing its role from a passenger to a driver of ecological change.
This invasive species was also observed to drive changes in benthic communities by
forming fluffy organic-rich sediments through its litter. This attracts high
microphytobenthos activity which could benefit itself since it has been shown that the
formation of litter can drive plant community changes that promote invasive species
dominance (Farrer and Goldberg 2009). The driver model suggested by MacDougall
and Turkington (2005) indicates that removal of invasive species could cause a direct
increase in species richness and abundance of the native species. The return of the
native N. nucifera and disappearance of C. furcata in sites dominated by N. nucifera
since the flood 2007 seems to support the driver model and warrant further study.
5.3 Implications for wetland and lake management
The results of this study hypothesised that the resilience of the Lake Chini ecosystem
and its ability to resist change depends on the flood regimes and nutrient dynamics,
which are both influenced by climatic conditions and the surrounding landscape.
Despite the possible dominance of N. nucifera or C. furcata, continuous landscape
alteration, if not controlled, can lead to increases in nutrients availability. These
nutrients in the water column may contribute to internal feedback mechanisms that
favour C. furcata dominance due to its possible inherent ability to outcompete N.
nucifera for these nutrients.
Additionally, the expansion of C. furcata species based on biomass accumulation and
rapid production rates could have serious implications for the management, restoration
and conservation of this wetland. As C. furcata populations increase, they could reduce
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
83
plant diversity and reduce the integrity or eventually replace the native plant
community. It could also change the benthic community composition and affect oxygen
dynamics and water quality which would indirectly further alter biological diversity and
lead to a structural change of higher trophic levels. Expansion of C. caroliniana
population in Kasshabog Lake was found to affect the epiphytic algae, and promote a
new habitat for certain macroinvertebrates (Hogsden et al. 2007). Changes in benthic
macroinvertebrates associated with submerged macrophyte dominance have been
observed to cause an increase in waterfowl and certain type of fishes (Hargeby et al.
1994).
Because Lake Chini is an important eco-tourism site in Malaysia, the dense infestations
of monospecific stands of the submerged species could also act to disrupt navigation
and recreational activities, affect the ecosystem services such as transport services,
eco-tourism and fisheries activities (Sharip and Jusoh 2010), and disrupt the aesthetic
and cultural values.
A number of methods have been used to manage and control Cabomba population.
Previous studies have shown that physical method such as shading (Schooler 2008)
and benthic barriers (Wilson et al. 2007) can be successful in controlling Cabomba
populations in small areas. However, the abundance of invasive species observed in
this study extends to almost half of the wetland. Therefore, this method may not be
cost-effective in controlling C. furcata in the Lake Chini system. Mechanical removal
can also be used to manage invasive species but this method is highly disruptive, non-
selective (Wilson et al 2007), and short-term, as re-infestation has been observed
(Australian Water Technologies 1999). As Cabomba population propagate through
vegetative reproduction by means of stem fragmentation (Schooler et al. 2009), the re-
invasion of C. furcata in this area would lead to immediate expansion of the invasive
species due to its rapid growth.
Understanding the pattern of convective circulation could assist in development of
chemical methods to manage C. furcata invasion. Smith et al. (1993) suggests
circulation patterns produced by differential heating and cooling and the short
residence times should be considered when developing herbicide application
strategies. However, despite herbicides such as diquat and endothall being commonly
used for lake and reservoir management, they are relatively expensive (Cooke et al.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
84
2005) and often have detrimental effects on wetland biodiversity. Given the sensitivity
and high biodiversity status of Lake Chini, this option is not considered to be ideal.
Application of lime may be more effective in managing this invasive species. Liming will
increase the pH level and shift inorganic carbon equilibrium to bicarbonate (HCO3-)
dominance (James 2011) which reduces the growth of submerged species such as
Cabomba population, which probably prefers free CO2 for their photosynthetic carbon
supply (James 2011; Sanders 1979). Liming has been suggested as a useful
management method for C. caroliniana (James 2011; Sanders 1979), but has not yet
been tried for C. furcata (Mackey 1996). Wilson et al. (2007) suggest liming may be a
practical control measure if size, isolation, and chemistry of the water body is suitable.
In experimental tanks, the addition of lime has been shown to effectively suppress
Cabomba (James 2011). In mesocosm experiments and in field trials, liming has also
been effective in reducing other submerged macrophyte abundance and biomass
(Chambers et al. 2001; James 2008; Prepas et al. 2001). Better understanding of the
circulation patterns in the system, as provided by this study, could improve C. furcata
control by helping determine liming contact times.
The conceptual model developed in this study showed that N. nucifera dominance
could be re-established if natural flow is also re-established. This natural flow could be
re-established by managing land-use alteration and catchment drainage practices to
control the overall catchment hydrology and subsequently flooding into the system. A
more proactive management approach to establish natural flow is to consider the water
level control structure and regulation of flood waters into the system to enable more
regular flow into the system to allow more frequent flooding. However, further studies
need to be carried out to better understand how managing water levels could be used
as means to reduce the dominance of Cabomba.
5.4 Original contributions
The original contributions of this study were the:
Provision of the first spatial and temporal quantitative analysis of the shift from a
native floating-leaved macrophyte (N. nucifera) to an invasive submerged
macrophyte (C. furcata) in a tropical lake system, and in particular its
relationship to human-induced environmental changes.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
85
Examination of the role of monsoonal flooding in facilitating the invasion of
submerged aquatic plants.
Novel examination of the processes influencing invasion by C. furcata, and
measurement of its effects on the native plant community. C. furcata has not
previously been reported to be invasive in any other country.
Introduction of a conceptual model of the variation in ecological processes that
shape macrophyte distribution in floodplain systems. This model can be applied
to other pulsed floodplain wetlands and systems to assist in management of the
system towards conservation objectives.
Examination of the roles of different types of macrophytes in influencing
temperature gradients and horizontal density currents and the associated roles
of convective exchange in nutrient transport that promotes invasion.
Provision of the first estimation of exchange mechanisms induced by differential
temperatures between floating-leaved stands and open water.
Provision of the first estimation of primary production by Cabomba species,
specifically C. furcata in an introduced area.
Provision of the first estimation of microphytobenthos and microflora production
associated with C furcata bed in an introduced area.
Combination of high resolution biological and physico-chemical measurements.
The set of techniques used in the field comprised an original suite of water
quality measurements that provide a comprehensive biophysical study of the
system.
5.5 Study limitations and recommendations for future work
This thesis concentrated on understanding the ecosystem processes that control the
possible shift of macrophyte dominance in the shallow floodplain wetlands of Lake
Chini, Malaysia. Time-frame and logistical issues, however, limited the findings of this
research to some degree. The study was based on vegetation surveys that were only
carried out before and after monsoons, and therefore conclusions that have been
drawn represent only one seasonal cycle. The metabolism experiments were also only
performed for a limited time period after the monsoon and may not be representative of
conditions throughout the year. Data collection over a longer time period may provide a
more complete understanding of the pattern of vegetation dynamics and invasion by
the submerged species.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
86
A greater understanding of the possible ecosystem processes driving the shift in
macrophyte dominance will assist in the formulation of successful management
strategies. Options for further work to build on the findings reported here could be
obtained by:
Continuing the spatial and temporal vegetation surveys and metabolism
experiments to better define the vegetation dynamics between the two possible
alternate states and the succession pattern of C. furcata invasion.
Continuing the vegetation surveys and metabolism analysis would allow
development of a better understanding of the progression of invasion and
successional patterns in this system under a more diverse range of
environmental conditions. Studies have shown that succession or shift between
alternate stable states will occur when ecosystems exceed a dynamic threshold
(Scheffer and Carpenter 2003; Suding and Hobbs 2009). Long-term monitoring,
together with controlled experiments, and modelling would allow further
exploration of the feedback mechanisms and alternate states (Scheffer and
Carpenter 2003) to determine the threshold(s) of ecological transition.
Extending the study to assess the influence of flood variability on the dynamics
of the plant communities.
This study did not examine the impact of flood frequency, magnitude or duration
on the plant species composition however the results did show a major
difference in the plant community after the 2009 flooding season and therefore
identified this as a significant driver of change. Flood variability, which is
exacerbated by changes in land-use that affects the hydrology, may exert
positive or negative feedback on the two plant species.
Applying multiple modelling approaches to identify options for restoring the
wetland ecosystem.
This study did not include simulation of mechanistic vegetation models. Further
modelling could be carried out to unravel the mix of environmental conditions
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
87
that lead to species dominance, and confirm the possible alternate stable
states. Such a model would not only lead to better insights into the control of
vegetation growth, but also would allow us to explore options to assist
restoration and management efforts in this system. In addition, these
mechanistic models could be coupled with structural dynamic modelling
(Jorgensen 2010) to (i) analyse changes in ecological structure, species
composition and spatial species dynamics (Jorgensen 1992; Mooij et al. 2010),
(ii) model biodiversity and ecological niches (Jorgensen 2010), (iii) discriminate
potential mechanism of species appearance and disappearance and species
adaptation with environmental changes (Wootton 1994). Increasingly,
uncertainties in ecological models have been noted in several ecological
research areas (Jorgensen 2007) such as habitat sustainability and
management and climate change. Therefore the application of multiple
modelling approaches to identify options for wetland restoration would be
beneficial (Mooij et al. 2010).
Extending the study to assess the extent of landscape changes on the
ecosystem for effective management and restoration aimed at conservation and
sustaining ecosystem services.
Landscape alteration can contribute to the intermittent influx of nutrient and
sediment (Hobbs 2000) into low lying catchment areas, such as wetlands.
Nutrient and sediment influx can also become a sink for material accumulation
and contribute to invasibility by invaders (Zedler and Kercher 2004). Historical
data analysis as shown in this study indicates the importance of landscape
changes in contributing to increased resource availability and the potential
relationship of this with the invasive species. Further assessment of continuing
landscape changes will provide a better understanding of hydrological dynamics
and the overall physical environment that affects the physical processes and
ecosystem function.
Extending the study to assess the overall food-web and potential top-down
ecosystem processes.
Changes in plant dominance and invasion may have an impact on the overall
food-web that could affect shifts in macrophyte dominance. Changes in water
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
88
quality have been shown to affect the distribution of benthic macroinvertebrates
distribution and reduce biological diversity (Idris and Abas 2005; Sharip and
Jusoh 2010). Further studies on macroinvertebrates, such as grazers and
predators, may provide a better understanding of grazer-plant interactions.
Further studies of biodiversity, including the biodiversity of fishes, birds, and
microbial communities, would provide a better understanding of the overall
ecosystem functioning and how increased pressure from C. furcata is impacting
on biodiversity values of the site.
5.6 Conclusion
This study has shown the dynamics of the macrophyte community in wetland
ecosystem of Lake Chini, Malaysia with possible alternate states dominated by floating-
leaved N. nucifera and submerged species C. furcata. The transition in plant
community dominance in this wetland ecosystem appears to be influenced by flood
regimes and nutrient dynamics. Invasion by C. furcata reduced the diversity of the plant
community and also appeared to affect the convective circulation of the ecosystems.
Increased physical circulation could improve nutrient transport to the advantage of C.
furcata. This invasive macrophyte also increased the net ecosystem production in the
ecosystem and appears to being changing from a passenger of ecological change to a
driver of ecological change. These changes not only have significant effects on the
overall plant community composition in Lake Chini but also affect the lakes both
ecologically and socio-economically. Overall, this study has significant implications for
understanding the wetland systems worldwide.
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
89
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Appendix 1: Supporting document for Chapter 2
Appendix 1a: List of methods for laboratory analysis
1. Phosphate (PO43-) – APHA 4500 P (F)
2. Nitrate (NO3-) – APHA 4500 NO3- (H)
3. Ammonium (NH4+) - APHA 4500 – NH3 (G)
4. Particle size distribution – BS 1377
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
109
Appendix 1b: Supporting information
Table S1: List of species in Lake Chini, Malaysia recorded in the literature Table S2: Mean values (± SE) of environmental variables
Sharip, Z., Interactions among freshwater macrophytes and physical-chemical-biological processes in Lake Chini, Malaysia
110
Table S1: List of species at Lake Chini recorded in the literature Plant species name 1987
a 1992
b 1998
c 2001
d 2009
e
Submerged Macrophyte
Cabomba furcata* + + +
Utricularia aurea + + +
Utricularia punctata + +
Utricularia gibba +
Utricularia sp. + +
Hydrilla verticillata + + + +
Cryptocoryne cordata +
Najas indica +
Chara sp. + +
Blyxa aubertii ssp. Echinosperma +
Hydrostemma kunstleri +
Aponogeton undulatus + + +
Floating macrophyte
Salvinia molesta + + + +
Ipomoea aquatica +
Azolla pinnata +
Rooted, Floating leaves
Barclaya kunstleri + + +
Nymphaea pubescens + + + + +
Nelumbo nucifera + + + + +
Emergent macrophyte
Lepironia articulata + + + + +
Eriocaulon sexangulare + + + +
Ericaulon longifolium + +
Thoracostachyum bancanum + + + +
Scirpus grossus + + + +
Pandanus helicopus + + + + +
Nepenthes gracilis + + + +
Flagellaria indica + + +
Melastoma malabatrichum + +
Eleocharis ochrostachys + + + +
Eleocharis acicularis + +
Bacopa monnieri +
Cerotopteristhalictroides + +
Fimbristylis globulosa + +
Fimbristylis acuminata + +
Fimbristylis miliacea + +
Cyperus sp. 1 +
Cyperus sp. 2 +
Cyperus sp. 3 +
Cyperus sp. 4 +
Cyperus pilosus +
Scleria sp. 1 +
Scleria sp. 2 +
Scleria terrestris + +
Polygonum sp. +
Echinochloa sp. +
Lycopodium cernuum L. + + +
Phragmites communis +
Lygodium microphyllum +
Panicum repens +
* was previously known as Cabomba piauhyensis
a Department of Wildlife & National Parks
b DARA
c Wetland International d
Gan & Bidin e
present survey
111
Table S2 Mean values (± SE) of environmental variables
Lake
Variable 1 2 3 4 5 6 7 8 9 10 11 12
Sep-09
Total depth (m) 1.5±1.0 1.3±0.7 1.1±0.7 1.4±1.1 0.9±0.7 1.0±0.5 1.1±0.5 0.9±0.3 1.2±0.6 1.3±0.8 1.4±0.8 1.8+1.0
Temperature(oC) 30.7+0.2 30.8±0.2 30.5±0.4 30.3±0.2 30.0±0.9 31.7±0.2 31.6±0.5 32.8±0.9 32.1±0.8 31.0±0.4 31.4±0.8 31.1±0.6
Conductivity (µS/cm) 23.3±0.5 24.0±0.4 23.0±1.1 22.0±0.0 23.4±0.5 22.9±0.4 18.7±1.9 26.7±2.1 30.7±2.8 26.0±0.0 26.4±0.8 21.7±0.8
pH 6.2±0.3 5.8±0.1 6.6±0.8 5.6±0.1 5.8±0.3 6.0±0.3 6.0±0.4 5.9±0.5 5.5±0.2 5.9±0.2 6.7±0.5 5.8±0.1
Turbidity (NTU) 19.3±10.0 35.3±65.4 23.7±12.2 20.1±19.1 14.4±4.6 19.5±15.9 17.3±20.5 13.4±4.2 16.0±9.3 12.3±6.4 10.8±1.9 10.7±2.5
DO (mg/l) 6.6±0.4 5.7±0.7 5.1±0.9 4.2±0.4 5.0±0.9 7.0±0.2 6.4±1.1 7.0±1.7 6.5±0.8 6.1±0.8 6.4±0.4 6.4±0.4
PO4 (mg/l) 0.089±0.047 0.054±0.045 0.057±0.029 0.054±0.033 0.042±0.043 0.042±0.028 0.020±0.014 0.025±0.011 0.025±0.011 0.042±0.028 0.024±0.013 0.046±0.028
NH4 (mg/l) 0.062±0.018 0.034±0.011 0.042±0.018 0.025±0.010 0.010±0.007 0.030±0.015 0.016±0.014 0.028±0.004 0.026±0.009 0.028±0.004 0.023±0.005 0.025±0.010
NO3 (mg/l) 1.094±0.277 0.896±0.249 0.976±0.098 0.618±0.085 0.765±0.110 0.283±0.339 0.432±0.537 0.790±0.179 0.786±0.080 0.858±1.457 0.410±0.640 0.673±0.025
Apr-10
Total depth (m) 1.1±0.9 0.8±0.7 0.9±0.7 1.0±0.8 0.8±0.6 0.7±0.4 0.8±0.4 0.7±0.3 0.9±0.5 0.9±0.7 1.2±0.6 0.9±0.6
Temperature(oC) 31.7±0.5 32.6±0.6 31.9±0.8 30.6±0.4 30.1±1.3 33.8±0.4 34.8±1.4 32.2±1.6 32.5±0.5 34.2±1.1 33.8±0.8 32.4±1.2
Conductivity (µS/cm) 29.0±0.0 27.6±0.5 26.3±3.1 27.1±1.1 28.6±0.9 28.1±1.0 29.5±1.1 29.3±2.2 31.7±3.1 35.8±3.1 38.8±6.4 25.1±1.9
pH 7.6±0.6 6.6±0.2 6.2±0.3 6.2±0.3 7.7±0.8 6.9±0.2 8.0±0.2 7.3±0.8 6.7±0.3 7.3±0.4 6.8±0.3 6.2±0.3
Turbidity (NTU) 23.9±13.9 66.6±134.6 168.2±593.6 17.8±6.5 592.9±867.9 24.1±8.7 21.2±10.5 25.6±15.2 32.8±27.7 391.7±773.7 21.8±21.2 414.6±781.6
DO (mg/l) 6.8±0.2 6.8±0.4 6.3±0.8 4.3±1.6 5.0±1.3 7.8±0.4 7.5±0.6 6.0±1.8 6.1±1.1 6.4±2.0 7.4±0.9 5.7±1.2
PO4 (mg/l) 0.008±0.003 0.121±0.053 0.033±0.016 0.028±0.035 0.153±0.170 0.132±0.063 0.033±0.045 0.009±0.010 0.052±0.105 0.033±0.038 0.075±0.030 0.024±0.038
NH4 (mg/l) 0.287±0.578 0.194±0.225 0.038±0.074 0.099±0.063 0.109±0.096 0.076±0.159 0.302±0.195 0.018±0.035 0.097±0.051 0.638±0.589 0.805±0.530 0.120±0.140
NO3 (mg/l) 0.007±0.003 0.006±0.002 0.006±0.002 0.010±0.000 0.010±0.000 0.009±0.002 0.010±0.000 0.009±0.002 0.006±0.002 0.018±0.021 0.008±0.015 0.005±0.000
%silt/clay 0.737 0.833 0.852 1.286 1.065 0.980 0.727 0.863 1.359 1.400 1.824 1.325 Rank distance to weir 8 5 3 1 2 4 6 7 11 9 10 12
112
Appendix 2: Conference Paper
113
Physical circulation and spatial exchange
dynamics in a shallow floodplain wetland
Z. Sharip1,2,3
, M. R. Hipsey1,4
, S. S. Schooler5
& R. J. Hobbs2
1Centre for Ecohydrology, School of Environmental Systems Engineering,
The University of Western Australia, Australia 2School of Plant Biology, The University of Western Australia, Australia 3National Hydraulic Research Institute of Malaysia, Malaysia
4School of Earth and Environment, The University of Western Australia,
Australia 5CSIRO Ecosystem Sciences, Australia
Abstract
This paper examines spatial patterns of water exchange based on water
temperature variations between littoral and pelagic zones; and compares the
patterns in lakes with different depths. The data were collected at Lake Chini,
Malaysia which comprises a series of shallow lakes connected by natural
channels. Our results indicate that the density-driven flow induced by the
differential temperature gradient between littoral areas, which are dominated by
either floating-leaved or submerged vegetation, and the open pelagic region
appeared to be an important transport mechanism for the exchange of dissolved
constituents between the zones. Persistent stratification in the narrower lakes
could be due to the presence of dense submerged vegetation that attenuates wind-
driven turbulence. Additionally, variation of thermal stratification and mixing
dynamics between these lakes has corresponding effects on the biological and
chemical regime. The circulation contributes to the spatial differences of the
water quality that could favour submerged species and subsequently induce
shifts of macrophyte community composition. The results of this study have
implications for the rehabilitation and management of lake ecosystems.
Keywords: convective circulation, density driven flow, floating-leaved plant,
lake Chini, shallow wetland, submerged macrophytes, thermal stratification,
water exchange.
114
1 Introduction
Circulation induced by horizontal density gradients resulting from depth
variation has been demonstrated to be an important exchange mechanism of
phosphorus between the littoral and pelagic zones, [1, 2], and nutrients between
side embayments and the main basins (Monismith et al [3]) of lakes. A
temperature gradient develops when shallow littoral areas and deeper pelagic
zones receive the same incoming solar radiation but distribute it differently over
their respective volumes [1, 3–5]. Differential heating created through shading
by aquatic plants can also induce convective motion [6–9]. Studies on the
convective exchange between a vegetated system and littoral zones, however,
have been focused on reed beds (Lovstedt and Bengtsson [7]), typha stands
(Waters [9]) and floating species such as Azolla sp. and Lemna sp. (Coates and
Ferris [6]). In all the above studies, a horizontal density gradient develops as the
surface water underneath or within the vegetation becomes colder than the
adjacent open water due to shading and subsequently induces overflow of
warmer pelagic water towards the plant bed at the surface during the day. Studies
on the effect of a horizontal thermal gradient and the associated convective
exchange induced by different types of macrophytes, specifically the rooted
floating-leaved plants and the submerged species, have been limited.
Differential nutrient gradients between the littoral and pelagic zones were
noted in Lake Chini by Sharip et al [10] and it is hypothesized that it may have
been controlled by the temperature differences between the two zones. In particular, the circulation induced by the thermal gradient may regulate transport
of nutrients to dense submerged Cabomba furcata beds (Sharip et al [10]) and
subsequently enable this species to proliferate in the system due to its ability to
uptake nutrients through stems and shoots (Wilson et al [11]).
The aim of this study is to examine the convective exchange pattern resulting
from differential cooling and heating between the littoral zone and the open
pelagic zone from two sites within a shallow floodplain wetland that are
dominated by different types of aquatic plants. The objective is to understand the
influence of the convective exchange pattern on water quality changes which
could contribute to the shifts of macrophyte community composition we
observed in the system (Sharip et al [10]). We analyzed temperature, light and
nutrient profiles and estimate the induced flow between the littoral zone and
main lake body at the two sites. The study was carried out in Lake Chini,
Malaysia, a shallow wetland located within the Pahang River floodplain, which
exhibits characteristics of a system having multiple ecological regime shifts
(Sharip et al [10]). The lake has a surface area of 1.69 km2
and an average depth
of 1.9 m (Sharip et al [12]) with its littoral areas extensively dominated either by
the floating-leaved plant (Nelumbo nucifera) or submerged vegetation (C.
furcata).
115
2 Methods
2.1 Field measurements
Surveys were carried out on 19–24 April 2010 to investigate the exchange flows
between the littoral and pelagic region. Transects were positioned in two lakes;
Lake 1 linking the open pelagic region to littoral area dominated by floating-
leaved vegetation, and Lake 12 linking pelagic zone to a littoral area dominated
by submerged species (Fig. 1). Thermistor chains were deployed at the centre of
three lakes; each anchored at the top on buoy and kept taut to the bottom by a
weight for long-term temperature measurements.
Figure 1: Lake Chini and location of temperature monitors along transect
(inset).
Thermistors recorded temperatures at intervals and depth as in Table 1.
Vertical profiles of Photosynthetically Active Radiation (PAR) and temperature
were made with a light sensor (LI-190 Quantum sensor) and a YSI 6600 multi-
parameter profiler, respectively. Water samples were collected at each station for
analysis of phosphate and nitrate. Linear interpolation was used to calculate
hourly interval values where necessary.
Hourly recorded meteorological data were obtained from an on-lake weather
station and the nearby Muadzam Shah meteorological station. Additional
temperature-depth profiles were carried out using YSI 6600 multi-parameter
probe on 28–30 March 2011 during a high water-level period.
116
Table 1: Temperature monitors in Lake Chini.
Sensor Parameter Recording
interval (min)
Depth (m) Lake
Hobo
RBR
D-Opto
TPS sensors
Temperature
Temperature
Temperature, DO
Temperature, DO
15
1
1
10–20
0.5, 1.0, 2.0
1.0
0.5
0.15–0.5
1,5,12
1,12
1,12
1,12
2.2 Analysis of physico-chemical structure and heat budget calculations
We assessed convective exchange patterns by generating contours (SURFER,
version 9.0; Golden Software, Inc) over the transects as in Smith et al [13] using
the temperature data recorded by thermistor probes and temperature-depth profile
data measured over 45-min intervals or less.
The atmospheric heat transfer was computed using the available
meteorological data and employed a standard bulk aerodynamic method as
describe by the Tennessee Valley Authority [14], with the neutral transfer
coefficients corrected for atmospheric stability and measurement height. The two
lakes were assumed to have similar meteorological parameters.
The overall heat budget calculation and exchange flow was based on eq. (1)
and (2) in Lovstedt and Bengtsson [7]:
.0
0 QsensibleLatentnet
h
P HHHRzt
TC
(1)
.. 0 QTTCLH plantopenPQ (2)
where ρ0 is the density (kg/m3), Cp is the specific heat capacity for water, 4.18 x
103J/(kg K), h is the water depth (m), ∂T is the average temperature change (
oC),
∂t is the time step (s), z is the vertical distance from surface (m), Rnet is the net
solar radiation (W/m2), Hlatent is the latent heat transfer (W/m
2), Hsensible is
the sensible heat transfer (W/m2), and HQ is the lateral heat flux between the
open water and the vegetation bed, and Q is the net exchange flow. The averaged- temperature as a function of time was calculated from eq. (1) using the initial temperature as in Lovstedt and Bengtsson [7] and compared with the measured temperature data (20-min interval) in the area. Heat fluxes were calculated based on temperature measurements between Station 1 and Station 2 in each lake. The estimation of the heat fluxes covered the whole one-day cycle for Lake 1 and only the differential heating (day) phase in Lake 12 due to sensor failure. The dissolved oxygen dynamic pattern will be described elsewhere.
117
3 Results and discussions
3.1 Meteorology and physico-chemical structure
Wind speed was generally low during the experiments in April 2010 with
average wind speed recorded around 0.8 m/s. Wind speeds were zero throughout
the night on 20–22 April 2010 (Fig. 2a). Thus, wind-driven exchanges were not
driving the transport mechanism during this period. The skies were occasionally
cloudy but no rain was recorded during the two days. Inflows and outflows of the
surface water and groundwater were not considered in the estimation.
Figure 2: Variations in (a) wind speed (b) air temperature (thin line) and
surface water temperature (dotted line) during surveys conducted in
April 2010.
Air temperature cooled from a maximum of 32.2oC at 1600h on 20 April to
24.6oC at 0600h on 21 April (Fig. 2b). A lower air temperature compared to
surface water temperature during the night can cause an increase in atmospheric
instability and subsequently an increase in sensible and latent heat loss (Verburg
and Antenucci [15]). This atmospheric condition was suitable for differential
cooling and differential heating to develop.
Mean surface water temperatures in the littoral were higher than the mean
water temperature in the pelagic zones in both lakes until late afternoon. High
temperature within the littoral zone vegetation dominated by the floating-leaved
plant, N. nucifera, was consistent with past studies (Coates and Folkard [16])
which could be due to sparse N. nucifera cover (13%) in the area. Surface water
temperature in the littoral cooled more rapidly at the littoral site compared to the
pelagic zone in both lakes during the night; causing movement of cooler littoral
water into the deeper pelagic zone by 0800h (Fig. 3c and 3g). However, intrusion
of cool water appeared to move away from the sediment in Lake 12 as shown in
the slanting contour at the surface (Fig. 3f) at 2200h, which could be caused by
the presence of a dense submerged macrophyte bed (Station 3) where the
temperature was slightly higher than the surrounding water (Fig. 3g) at 0800h.
118
Figure 3: Longitudinal and vertical variations in water temperature on 20–21 April in Lake 1 at (a) 1800 h, (b) 2200 h, (c) 0800 h,
(d) phosphate concentration (mg/L) and Lake 12 at (e) 1800 h, (f) 2200 h, (g) 0800 h (h) phosphate concentration
(mg/L).
119
The water at the surface and bottom layer also remained separated at Station 3 (Fig. 4c), which was in contrast to the pelagic zone (Station 4) (Fig. 4d) where the surface layer was completely mixed with the bottom layer. PAR at Station 3
reached ca. 0 µmols-1
m-2
within the submerged stands where wind-driven motion was attenuated (personal observation). The presence of dense C. furcata bed enhances daytime stratification in the water column matched with past studies
[17, 18]. In contrast to findings by Herbs and Stefan [18], our study shows the presence of dense submerged vegetation affects the circulation pattern induced by the horizontal density gradient.
Figure 4: Variation in water temperature in Lake 1 on 20–21 April 2010 (a)
Station 3, (b) Station 4, and in Lake 12 on 21–22 April 2010, (c)
Station 3, (d) Station 4.
120
In both lakes, phosphate concentrations were high in the littoral areas
compared to the pelagic zone (Fig. 3 d and Fig. 3h) and the induced horizontal
density gradient could improve transport of phosphate to other areas. The
circulation pattern provides a better spread of nutrients for the growth of
submerged macrophytes within the area.
Over the daily cycle, stratification and vertical mixing patterns were clearly
different between the lakes (Fig. 5). A pattern of diurnal stratification and
complete mixing at night were apparent in Lake 1 and Lake 5, whereas
stratification persisted in Lake 12, with the exception on the morning of 22 April,
where the mixed layer didn’t reach the 2-m layer. In contrast to thermal pattern
during low water level, a distinct pattern of stratification in both Lake1 and Lake
12 during high water level were driven by high turbidity which altered the
thermal gradient and the exchange dynamics and mixing in the lake system.
Stratification in these lakes could lead to anoxic conditions and subsequently an
increase in nutrients.
Figure 5: Thermistor time series at the pelagic zone, at (a) Lake 1, (b) Lake 5,
and (c) Lake 12 between 20–24 April 2010.
3.2 Water exchange
Solar radiation was high during the day, reaching 900 W/m2
and thus net radiation was an important heat flux that influenced the heating and cooling of the water. The predicted sensible heat fluxes were small and ranged between -3
to 12 W/m2. The latent heat fluxes were high during late afternoon. The
calculated temperature profile showed a similar trend with the measured temperature profiles (not shown). Significant differences (p<0.001) between the measured and calculated values could be due to the estimation of latent heat
121
fluxes which, as found by Lovstedt and Bengtsson [7], were difficult to predict.
Comparisons are being made with different methods as in Verburg and
Antenucci [15] and Lovstedt and Bengtsson [7] and using corrected
meteorological data to enhance the localized lake-effect to improve the
atmospheric heat budget estimation.
The results show the presence of convective currents due to differential
heating and cooling between littoral and pelagic zones. The estimated convective
current between floating-leaved vegetation stands and open water (Lake 1) was
2.6 cm/s. The estimated convective current due to differential heating by
submerged vegetation (Lake 12) was around 0.4 cm/s. The convective currents
were within the rates of differential heating between shallower and deeper water
estimated in Monismith et al [3] which was 0.4–11 cm/s.
4 Conclusions
This study documents the contribution of aquatic vegetation to thermal structure
and water exchange dynamics. The horizontal density gradient may also be
affected by rooted floating-leaved vegetation and submerged vegetation.
Submerged vegetation affects the temperature pattern by increasing stratification
and altering the circulation pattern which affects the water quality in the lakes.
The convective current due to differential heating and cooling between littoral
and pelagic is an important exchange mechanism that has important implications
for nutrient cycling, and subsequently shifts of macrophyte composition, in this
shallow lake system.
Acknowledgements
The first author gratefully acknowledges Ahmad Taqiyuddin Ahmad Zaki for his
assistance and coordination during all field experiments and Justin Brookes for
provision of sensors and assistance in the field. The National Hydraulic Research
Institute of Malaysia (NAHRIM) provided data, and financial assistance for the
field experiments.
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