Download Population Dynamics of the Zuurberg Cycad and the Predicted

Population Dynamics of the Zuurberg Cycad
and the Predicted Impact of Climate Change
By
Karishma Singh
Submitted in fulfillment of the requirements for the
degree of Magister Scientiae in the Faculty of Science at
the Nelson Mandela Metropolitan University
January 2012
Supervisor: Prof E.E. Campbell
Co-Supervisor: DR D.R. du Preez
DECLARATION
I, Karishma Singh (204043743), hereby declare that the dissertation for Masters
in Science is my own work and that it has not previously been submitted for
assessment or completion of any postgraduate qualification to another University
or for another qualification.
Karishma Singh
Table of Contents........................................................................................i
List of Figures.............................................................................................iii
List of Tables...............................................................................................iv
List of Plates.................................................................................................v
Acknowledgements.................................................................................vi
Abstract..........................................................................................................vii
Chapter 1: Introduction.................................................................................1
Chapter 2: Literature Review......................................................................4
2.1 Cycad biogeography, morphology, anatomy and physiology,
conservation and demography......................................................................4
2.1.1 Cones...............................................................................................5
2.1.2 Stem.................................................................................................6
2.1.3 Roots...............................................................................................6
2.1.4 Leaves.............................................................................................7
2.1.5 Toxicity............................................................................................8
2.1.6 Photosynthesis.............................................................................8
2.2 South African genera.................................................................................9
2.2.1 Encephalartos Lehm....................................................................9
2.2.2 Stangeria T.Moore......................................................................13
2.3 Pollination and Seed-dispersal..............................................................14
2.4 Propagation and Germination................................................................16
2.5 Conservation Status.................................................................................17
2.6 Demography...............................................................................................19
2.7 Climate Change.........................................................................................20
2.2.1 The causes and effects of Climate Change..........................20
2.7.2 What does climate change mean for C3 plants?..................22
Chapter 3: Materials and Method............................................................23
3.1 Demography...............................................................................................23
3.1.1 Study Sites...................................................................................23
3.1.2 Field Measurements...................................................................28
3.1.3 Data Analysis...............................................................................39
3.2 Germination................................................................................................30
3.3 Photosynthetic physiology.....................................................................30
Chapter 4: Results........................................................................................31
4.1 Demography...............................................................................................31
4.2 Growth Rates.............................................................................................36
4.3 Germination................................................................................................37
4.4 Photosynthetic Physiology.....................................................................39
Chapter 5: Discussion.................................................................................41
Chapter 6: Conclusion and Recommendations.................................50
References......................................................................................................52
Appendix A......................................................................................................62
Appendix B......................................................................................................65
ii
List of Figures
Figure 1: Distribution of Encephalartos longifolius in the Eastern Cape.........................13
Figure 2: The locality of the three study sites chosen for demographic study the cycad
Encephalartos longifolius (Jacq.) Lehm.....................................................................24
Figure 3: Vegetation map showing the dominant vegetation types in all three study sites
according to STEP (Vlok and Brown 2006) and Mucina and Rutherford
(2006)....................................................................................................................26
Figure 4: Frequency of plant height of Encephalartos longifolius at (a) Kaboega, (b)
Zuurberg, (c) Woodridge, measured in June 2010.......................................................32
Figure 5: The relationship between height and age at (a) Kaboega, (b) Zuurberg, (c)
Woodridge measured in June 2010............................................................................34
Figure 6: : Relationship between plant diameter and height at (a) Kaboega, (b) Zuurberg,
(c) Woodridge.........................................................................................................35
Figure 7: Frequency of change in plant height of Encephalartos longifolius at Kaboega,
measured in July 2011.............................................................................................36
Figure 8: Change in plant height in juvenile and adult plants of Encephalartos longifolius
at Kaboega, measured berween June 2010 and July
2011......................................................................................................................37
Figure 9: Overall germination of Encephalartos longifolius under controlled conditions
over a 1 year period.................................................................................................38
Figure 10: Germinated Encephalartos longifolius seeds under controlled
conditions..............................................................................................................38
iii
Figure 11: The number of rotten Encephalartos longifolius seeds at three different
moisture conditions................................................................................................39
Figure 12: The photosynthesis-irradiance relationship of Encephalartos longifolius
seedlings (Vertical bars = ± S.E., n = 3) (Harrison et al.
1985).....................................................................................................................40
Figure 13: The photosynthesis–temperature relationship of Encephalartos longifolius
seedlings (Vertical bars = ± S.E., n=3)........................................................................40
Figure 14: Fossil records of cycad abundance with changing temperature and carbon
dioxide levels through geological time (Plass 1956; Buckley
1999).....................................................................................................................45
Figure 15: Projections of past, present and future temperature levels and carbon dioxide
concentrations according to the IPCC, 2007 Assessment Report and Midgley et al.
2007......................................................................................................................46
Figure 16: The relationship between plant height and age at all three study sites
combined...............................................................................................................65
List of Tables
Table 1: Encephalartos species endemic to the Eastern Cape......................................11
Table 2: A Shapiro-Wilks test for normality for the demographic data collected at all three
sites......................................................................................................................31
iv
List of Plates
Plate 1: Lignotuber on Encephalartos longifolius stem in response to
fire........................................................................................................................62
Plate 2: Leaning-over effect of Encephalartos longifolius.............................................62
Plate 3: Encephalartos longifolius trampled and knocked over by large
mammals...............................................................................................................63
Plate 4: Encephalartos longifolius cone damaged by baboons.....................................63
Plate 5: The base of Encephalartos longifolius stem impacted on by
porcupines.............................................................................................................64
v
Acknowledgements
I would like to thank the following people and organizations:
•
Prof EE Campbell (Supervisor) for giving me an opportunity to do this project, as well
as for her constant support, guidance and understanding throughout the project.
•
DR D.R Du Preez (Co-Supervisor) for his assistance with GIS, physiology,
experiments and other additional information as well his dedication and sacrifices
towards my physiology experiments
•
Nelson Mandela Metropolitan University and Prof Andrew Leitch for providing me
with funding for my project.
•
Prof RM Cowling for allowing me to come along on his honours excursions.
•
The honours class of 2010 and 2011 for their assistance with sampling.
•
The Botany Department for making it possible for me to complete my studies.
•
The staff of the Ria Olivier Herbarium for their assistance in helping me obtain the
relevant information.
•
The South African National Biodiversity Institute (SANBI); the South African National
Parks (SANParks) and the Department of Economic Affairs Environment and
Tourism (DEAT) for providing me with permits to sample in the respective study
sites.
•
Ian Ritchie at Kaboega for allowing me to tag and measure the cycads as well as
driving me to the cycad locality.
•
MR Neave Campbell at Woodridge College for allowing me to tag and measure the
cycads on his property as well as access to the property at any given time.
•
My colleagues Adriaan, Anusha, Chan, Clayton, Merika, Nuette, Sibulele and
Wynand for helping me with sampling and providing me with assistance throughout
my project.
.
vi
Abstract
Cycads first appeared about 300 million years ago and historical data indicates that they
survived fluctuations of global temperature and carbon dioxide concentrations and
reached peak abundance during periods where temperature and carbon dioxide
concentrations were much higher than the present conditions as well as the predicted
increased levels. With Africa being one of the most vulnerable regions to climate change
and in the absence of an evaluation of predicted impacts of climate change on cycads,
this study aims to contribute to our understanding of responses of Encephalartos
longifolius to increased temperature. Encephalartos longifolius (Jacq.) Lehm is an
Eastern Cape endemic and like most cycads has been around for millions of years with
very little change to its basic structure. Photosynthetic rates showed E.longifolius
seedlings have C3 photosynthesis and even under stress they do not switch over to CAM
photosynthesis. The photosynthetic rates of seedlings showed a typical C3 -plant type
response under elevated carbon dioxide levels. Increased temperatures could be
detrimental to the species but coupled with elevated carbon dioxide levels the growth of
Encephalartos longifolius are postulated to outweigh the negative impacts of increased
temperatures. Whilst climatic conditions in the Eastern Cape might not impact the
abundance of Encephalartos longifolius, the species however is declining rapidly to the
present near-threatened status. Demographic studies revealed a high percentage of
juvenile numbers in the wild; however juvenile plants are impacted on by animals
thereby jeopardizing their survival. Adult plants are heavily impacted on by animals; this
reduces the probability of new offspring being produced. Cycads are also very slow growing which is the primary cause of their ruin in the wild. Encephalartos longifolius
grows at just over approximately 1 cm per year with growth being more rapid in the
juvenile plants. Once juvenile plants reach approximately 60 cm they stop growing in
diameter but only get taller. Seed germination is also a very slow process with an
optimum temperature of 28°C and a growth medium of at least 50% moisture.
Regardless of the Eastern Cape predicted to become the hottest province in South
Africa as a result of climate change, cycads will be able to adapt to the changing
environment and conservation plans should focus on animal and human impacts that are
the major force causing decreasing abundance of Encephalartos longifolius in the wild.
vii
Key words: cycads, photosynthetic rates, climate change, demographic studies,
slow-growing, predicted impacts, C3 photosynthesis.
viii
Chapter 1
Introduction
Cycads are known as the most primitive living seed bearing plants belonging to an
ancient order the Cycadales (Chamberlain 1919; Giddy 1974). Cycads belong to a group
of plants known as gymnosperms (plants which bear naked seeds) and their
reproductive organs are produced in cones (Chamberlain 1919) Cycads are divided into
three families namely Cycadaceae, Stangeriaceae and Zamiaceae which are distributed
in the temperate and tropical regions of both the Southern and Northern hemisphere on
the continents of: Asia, Africa, Central America and Australia (Anderson et al. 2007;
Giddy 1974). In South Africa the two common genera of cycads are Encephalartos
Lehm. and Stangeria T.Moore (Chamberlain 1919), with Encephalartos being the largest
genus having 37 South African species of which 15 are found in the Eastern Cape and 8
are endemic to the province (Giddy 1974; Germishuizen et al. 2006). The key to
distinguishing between the Encepharlartos species is the morphology of the median
leaflets i.e leaves occuring at the middle of the leaf stalk (Giddy 1974).
Encephalartos longifolius (Jacq.) Lehm is also known as the Zuurbeg cycad chosen as
the study species (Giddy 1974; Donaldson 2003). This most attractive foliage species
has long leaves, and stems are mostly erect with height ranging between 4 m and 6 m
and diameter of between 30 cm and 55 cm. Grows well in full sun and adequate
moisture conditions where the soil is not too damp, and is semi-hardy to frost
(Chamberlain 1919; Giddy 1974; Donaldson 1997). Encephalartos longifolius like most
cycads are slow-growing (Chamberlain 1919). The seeds of are nutrient rich and are
heavily predated by monkeys, baboons, birds and rodents (Donaldson 1993).
Like most cycads Encephalartos longifolius is an endangered species and according to
the 1997; 2006 and 2010 IUCN Red List of threatened plants 82% of the world’s cycads
were listed as threatened and is suffering a major extinction crisis (Anderson et al.
2007). Some species are dying out naturally (Donaldson 2003) but the major extinction
factor is human activities, therefore permits are needed for possession of cycads (Giddy
1974; Donaldson et al. 2003).
1
Cycads have survived for over 300 million years with little change in their basic structure
and neither fire nor drought presents any real threat to their survival (Giddy 1974).
Some cycads have CAM photosynthesis but the majority of the South African species
have C3 photosynthetic pathway (D.R. du Preez, pers.comm). Cycads first appeared
during the late Carboniferous period and early Permian periods where temperatures and
carbon dioxide levels are similar to that of the present and began to flourish in
abundance (Microsoft Encarta 2005). The carboniferous period was then followed by a
glaciations period which caused a slight decline in cycad abundance, however the
populations recovered and it was during the Jurassic period that cycads reached their
peak abundance (Chamberlain 1919; Plass 1956). Historically the earth has been much
hotter and drier and carbon dioxide concentrations were much higher compared to the
present (Plass 1956), however after the last cold period which ended about 15 000 years
ago the earth continued to get warmer and warmer with much larger risks compared to
changes that have occurred during the past decades (Scholze et al. 2006; IPCC, 2007).
In the next 200 years global temperatures are estimated to increase by 1.5 -5.5ºC as a
result of increased greenhouse gas emissions and have become one of the most
important issues concerning scientists with a number of predictable environmental
impacts (Marshak 2005; IPCC, 2007). Atmospheric carbon dioxide in particular is rising
at an alarming rate and such a rate of increase will have far reaching effects on the
earth’s resources especially primary production as primary production depends on the
balance between respiration and photosynthesis (Turpie et al. 2002). According to the
South African Country Study on Climate Change temperatures in South Africa are
predicted to increase by 2.5ºC by the year 2050 which could result in major changes in
the rainfall patterns, a strain on water resources, lower yields in food production and far
reaching impacts on the biodiversity of plants in particular (Midgley et al. 2007; DEDEA,
2011). It is predicted that the impact of elevated carbon dioxide levels on C3 plants will
result in an increase in the efficiency of photosynthesis, thus accelerating plant growth,
however whilst C3 plants will show an increase in photosyntheesis in correlation with
initial carbon dioxide increase over time photosynthesis will level out even though carbon
dioxide continues to increase (Cheng et al. 2000; Ehleringer and Cerling 2002).
2
The aim of the study was to predict the impacts of climate change on Encephalartos
longifolius (Jacq) Lehm. The objectives of the study were to determine population
vulnerability, plant growth rates, and using germination rates predict what impact climate
change in the Eastern Cape will have on Encephalartos longifolius. The hypothesis of
the study is that the change in climate predicted for the Eastern Cape will have no effect
on the survival of Encephalartos longifolius.
3
Chapter 2
Literature Review
2.1 Cycad biogeography, morphology, anatomy, physiology,
conservation and demography
Cycads are an ancient group of gymnosperms that can be divided into three families
namely Cycadaceae, Zamiaceae and Stangeriaceae- the extant Cycadales
(Chamberlain 1925; Donaldson et al. 2003). They are restricted to tropical and
subtropical regions of Asia, South Africa, North and South America and Australia where
they are well adapted to survive adverse environmental conditions (Chamberlain 1925;
Whiting 1963). In Africa there are currently 69 recognized cycad species (Donaldson et
al. 2003). The largest genus Encephalartos as well as Stangeria which is the smallest
genus are both endemic to Africa (Giddy 1974; Donaldson et al. 2003). On the African
continent cycads are distributed throughout 16 countries as well as on the Indian Ocean
islands of Madagascar, Seychelles, Comores and Zanzibar (Donaldson et al. 2003;
Anderson et al. 2007). South Africa stands as the most important center for diversity with
more than 50% of the known African cycads found in the country (Donaldson et al.
2003).
Cycads are an interesting group because they are morphologically intermediate between
fern and flowering plants in evolution (Hertrich 1951). Cycads have survived for over the
past 300 million years with little modification to their basic structure and it’s for this
reason they are referred to as living fossils (Chamberlin1919; Giddy 1974). Fossil
records for cycads extend at least the late Carboniferous early Permian period (about
300-315 million years ago) (Chamberlain 1919; Donaldson et al. 2003).
There are many misconceptions of the age of individual plants (Hertrich 1951; Giddy
1974) but the age of cycads are generally estimated by counting the number of whorls of
persistent leaf bases on the stem (Giddy 1974). All cycads are slow-growing plants and
most of the species are arborescent meaning that they can either produce a single trunk
which is marked with rings of growth after attaining a certain height (Chamberlain 1919;
4
Hertrich 1951). The slow growth rate and reproduction of cycads is the primary cause of
their ruin in the wild. Cycads were once found worldwide during the early1800’s to the
mid 1900’s (Brenner et al. 2003).
A probable explanation for the long term survival of cycads is that they can survive
drought and fire and are remarkably resistant to predators and pathogens; and are well
equipped against environmental threats due to their ability to biosynthesize a variety of
protective and secondary compounds such as glycosides and non-protein amino acids
(Brenner et al. 2003). They thrive in habitats of moderate moisture, neutral or slightly
acidic substrates and abundant sunlight (varies from species to species), with many
species being adapted to low rainfall areas as excessive moisture causes root damage
(Donaldson 1997).
2.1.1 Cones
Cycads are dioecious and it is not possible to determine the sex without the presence of
cones (Chamberlain 1919; Giddy 1974). Male and female cones occur on separate
plants and are succulent consisting of a fleshy axis with numerous spirally attached
sporophylls (Chamberlain 1919; Giddy 1974; Tang 1987). The seed cone sporophylls
bear two ovules (Giddy 1974). The pollen cones are more slender compared to the seed
cones. Male cones appear compact at first and later elongate with maturity to reveal the
microsporangia or pollen sacs on the under surface of the sporophylls after which the
pollen is shed once the pollen sacs are mature (Chamberlain 1919; Giddy 1974). In
majority of the species the female cones are usually shorter, broader and sometimes
nearly globular while the male cones are erect and triangularly shaped (Chamberlain
1919; Hertrich 1951). Cone appearance varies according to species and climatic
conditions, male and female cones first start appearing towards the end of summer (late
February) and grows steadily for about three months before attaining maximum size
(Hertrich 1951).
Plants are generally considered to be poikilothermic but they possess a number of
physiological and morphological features that enable them to maintain tissue
temperatures that differ from atmospheric temperatures (Tang 1987). In cycads
endogenous heat production (thermogenesis) is widespread and common among male
5
cones whilst female cones exhibit very weak thermogenesis (Tang et al. 1987).
Thermogenesis in male cones is known to occur in a circadian pattern during pollen
shedding and this is the general pattern in all male cones because the basic morphology
of male cycad cones is similar across all genera (Chamberlain 1925).
2.1.2 Stem
Cycads stems are usually unbranched however when branching occurs in the columnar
types this is a result of an injury to the stem (Giddy 1974). Stems are thick and slowgrowing and branching rarely occurs but in the event of branching up to 10 stems may
originate from a single base (Chamberlain 1919; Giddy 1974). The age of cycads can be
estimated by counting the armor of leaf bases on the trunk however some species for
example Encephalartos longifolius have heavy stems that become compressed as a
result of the weight and may reduce the visibility of leaf bases over time (Chamberlain
1919; Giddy 1974). Stem injury also allows for the plant to be more susceptible to
pathogens and rotting (Whiting 1963; Giddy 1974; Vorster et al. 2004). Leaning over of
the stem is often visible in some of the taller cycads, this is because the root system is
not very extensive and the plants are heavy so as they get tall enough to be affected by
the wind they tend to lean over (Chamberlain 1919).
Externally the stems of cycads consist of a thick layer of spirally arranged persistent
leafbases and internally there is a large pith in the center surrounded by a corky layer
and a thin layer of wood even though they are known to be hardy plants (Chamberlain
1919; Whiting 1963; Giddy 1974). Mucilage canals are found in all parts of the plant
particularly in structures such as the cortex, the pith, leaves and sporophylls (Giddy
1974). The stems of cycad seedlings in particular possess lignotubers (a swelling at the
base of the stem just above the soil level) that helps the seedling survive fires by
sending out new growth if the top growth is damaged (Chamberlain 1925; Donaldson
2003).
2.1.3 Roots
Cycad seedlings have taproots which soon form several lateral branches which end in
smaller fibrous roots that extends down to great depts. providing the plant with small
amount s of water when the surface soil is very dry (Chamberlain 1919). Subterranean
6
(below the surface) cycad species have very large tuberous roots which are probably
climatic adaptation and columnar species do have stems for water storage (Giddy 1974).
An apogeotropic root (roots that grow upwards and form coralloid masses just above the
surface of the soil) is an unusual feature in cycads (Chamberlain 1919). This feature
allows for roots to contain a symbiotic blue-green alga Anabaena (Chamberlain 1919;
Giddy 1974), that assist the plant by nitrogen fixation and assimilation therefore allowing
the plant to live on nutrient poor soils (Giddy 1974; Whiting 1963). Studies have shown
that the symbiotic algae in the roots fix up to 38 Kg of atmospheric nitrogen per hectare
per year (Whiting 1963). The depth and size of roots provide the plant with anchorage
and support during heavy winds however as plants get taller they are more prone to
leaning over due to heavy winds (Chamberlain 1919; Whiting 1963). The roots system
also contributes to the plants survival during fires, (Whiting 1963).
2.1.4 Leaves
Cycad leaves are an attractive feature which gives the plant its popularity as a
decorative plant (Chamberlain 1919). Leaves consist of a strong central stalk or rachis
from which numerous leaflets are produced (Chamberlain 1919). Leaves are neither
strictly alternate nor opposite and when they overlap the overlapping maybe either
upwards or downwards and the leaves of mature plants appear in whorls (Chamberlain
1919; Giddy 1974). The shape, margins and colour of the leaflets varies from species to
species providing distinguishing characters between species (Giddy 1974). The new
leaves are very delicate and susceptible to injury but once they reach maturity and attain
their full size the tissues harden and leaves become hard and leathery and extremely
strong and resistant to moisture and dryness extremes (Chamberlain 1919; Giddy 1974).
The length of the leaves vary from a few centimeters in the smallest plants to about 1-2
m in the larger plants (Whiting 1963). Leaves may persist for up to 5 years before a new
set arises and once the new set arise the old leaflets turn yellow and fall off but the
leafstalks may remain for several years before falling out (Chamberlain 1919). These
persistent leafbases constitute the outer layer of the stem known as the characteristic
armor that serve to protect the stem from the hazards of fire as well as provides an
estimate of plant age (Chamberlain 1919; Giddy 1974). The structure of the epidermis of
the leaflet is also adapted to the hot dry climate in which many species grow. It consists
of a highly cutinized upper surface that is almost impervious to water while the stomata
7
or pores on the under surface of the leaflet are closed except when the air is moist, this
feature is adapted to minimize water loss and aids the plant surviving low moisture
supply (Chamberlain 1919; Whiting 1963; Giddy 1974).
2.1.5 Toxicity
Cycads for many years have been a food source for people and animals, however the
toxicity of the plant is very high (Chamberlain 1919; Whiting 1963, Giddy 1974). The
plant is known to contain numerous toxic ingredients such as cycasin and macrozamin
that is lethal to the consumer and when ingested continuously could result in irreversible
paralysis of the extremities (Whiting 1963). The poisonous properties of the South
African cycads Encephalartos is mainly found in the cones and seeds of the genus
(Chamberlain 1925; Giddy 1974). In the seeds the kernels of all species have been
tested and proven to be extremely toxic, the toxic effect resides primarily in the liver of
the consumer; other organs such as the stomach, lungs and heart tissue also showed
signs of damage when a post mortem conducted on a rabbit that consumed kernels as
part of an experiment was examined (Giddy 1974). Similar research has shown that
sheep and cows also have negative effects from consuming young cycad cones and in
some cases it resulted in the animal’s death (Schneider et al. 2002). There are no known
cases of poisoning following ingesting cycad seeds and cones in humans; however
children are warned to take precaution in consuming the plant.
2.1.6 Photosynthesis
There are three photosynthetic pathways that exist amongst terrestrial plants namely:
C3, C4 and CAM photosynthesis (Ehleringer and Cerling 2002). The photosynthetic
pathway of cycads is either CAM or C3 photosynthesis, however most South African
species are C3 plants (D.R. du Preez, pers comm). C3 photosynthesis is a multi step
process because two molecules of the phosphoglyceric acid (PGA) are formed when
carbon dioxide combines with ribulose bisphosphate (RuBP), a 5-carbon molecule, in a
reaction catalyzed by an enzyme known as RuBP carboxylase (Ehleringer 1979). The
initial product formed in this pathway is PGA, a 3-carbon molecule and the energy
sources used to drive this pathway are ATP and NADPH that come from the light
reactions of photosynthesis (Ehleringer 1979). This pathway is also known as the most
primitive pathway and one of its major disadvantages is a process known as
8
photorespiration (a process that takes place in the light in which carbon dioxide is
evolved from photosynthetic tissues), however further research has shown that
photorespiration arises because the enzyme RuBP carboxylase has an oxygenase
activity as well as a carboxylase activity (Ehleringer 1979; Ehleringer and Cerling 2002).
Therefore this oxygenase activity of RuBISCO is dependent on [CO2/O2] ratio and
temperature and as result of this the efficiency of the C3 pathway increases as
atmospheric carbon dioxide increases (Ehleringer and Cerling 2002).
Crassulacean Acid Metabolism (CAM) is also another photosynthetic pathway employed
by some cycads (REF). CAM photosynthesis is a modified form of C4 photosynthesis
where C4 photosynthesis can be described as morphological and biochemical
elaboration of the C3 pathway where CO2 is first combined with phosphoenolpyruvate
(PEP) catalysed by the enzyme PEP carboxylase to form a 4-carbon molecule called
oxaloacetic acid (OAA) (Ehleringer 1979). In CAM photosynthesis both the catalytic
enzymes from the C3 and C4 pathways are present in the same cells, but the RuBP
carboxylase is active during the day when the stomata is closed and CO2 taken up
during the night is fixed and PEP carboxylase is active during the night when the
stomata is open allowing for the enzyme to fix atmospheric CO2 (Ehleringer 1979). A
disadvantage of CAM photosynthesis is that as a result of only nocturnal stomatal
opening, the maximum rate of photosynthesis is much lower compared to that of C3 and
C4 plants, however CAM plants are better adapted to survive extreme periods of drought
than C3 and C4 plants (Ehleringer 1979).
2.2 South African genera
2.2.1 Encephalartos Lehm
The genus Encephalartos belongs to the family Zamaiceae Horan. and are Cycadalean
plants with radiospermic seeds borne in compact cones with a central axis (Anderson et
al. 2007). Previously there were sixteen species of Encephalartos that were confined to
South Africa and at present there are 37 species found in South Africa (Chamberlain
1925; Germishuizen et al. 2006). All species in this genus are classified as long-lived
plants with the average adult span varying from 150 years to > 1000 years depending on
9
the species (Donaldson 2008). Like all cycads Encephalartos are dioecious plants and in
the female cones the megasporophylls woody and peltate bearing a single pair of lateral
ovules whereas in the male cones pollen is produced in simple cones with
sporangiophores peltate and cones having two lateral lobes each bearing several
abaxial, di-to tetrasporangiate and a shortly stalked synangia (Chamberlain 1919;
Anderson et al. 2007). The cones of the species Encephalartos longifolius are the
heaviest of all the South African species with the female cones weighing up to about 36
kg and produce about 600 seeds whereas the male cone is much smaller and weighs
about 30 kg (Whiting 1963; Donaldson 1993).
The leaflets of Encephalartos are pinnate with a central leafstalk with numerous leaflets
that have parallel veins (Chamberlain 1919; Giddy 1974). Young leaves are covered in
fine hairs that disappear as the plant matures, and stems are mostly erect and grow up
to 10 m or more in height and are characterized by densely packet persistent leaf bases
(Chamberlain 1919; Whiting 1963; Giddy 1974).
The distribution of this genus ranges from tropical to warm-temperate and is widespread
through central and northern South America, Australia and central and southern Africa.
In South Africa most occur in the Eastern and Western Cape, Kwa-Zulu Natal, and in the
Free State regions (Germishuizen et al. 2006; Giddy 1974). The Eastern Cape Province
is one of several centers of diversity for the genus and 8 species are endemic to the
province (Table 1) (Giddy 1974; Donaldson 2003; Vorster et al. 2004; Germishuizen et
al. 2006):
10
11
tree
altensteinii
cycad
arenarius R.A.
cycad
horridus
Broadest leaves in the genus,
Albany
cycad
Zuurberg
cycad
Encephalartos
latifrons Lehm.
Encephalartos
longifolius
cycad
princeps R.A.
Dyer
cycad
s River
trispinosus
(Hook) R.A.
Bushman’
Encephalartos
Dye4r
Small size plant, single bushy
Kei River
Encephalartos
diameter
in height and 35-40 cm in
Branched reclining stems, 1-3 m
Medium to large size plant.
cm in diameter
stem, 1-4 m in height and 30-40
and 30-55 cm in diameter
(Jacq.) Lehm.
multi-stemmed, 1-6 m in height
Most attractive foliage, erect
30-45 cm in diameter
multi-stemmed, 1-3 m in height,
in height and 30-40 cm in
(Jacq.) Lehm.
single to multi stemmed, 1-3 m
Medium, low growing plant,
Blue
Encephalartos
stemmed, 1-3 m in height and 2035 cm in diameter
cycad
cycadifolius
Vulnerable
Vulnerable
Near Threatened
Critically endangered
Endangered
moisture conditions
sunlight and low
Grows well in full
moisture
sunlight and low
Grows well in full
moderate moisture
sunlight and
Grows well in full
climatic conditions
Adapted to hot dry
frost- hardy
sunlight and is
Grows well in full
completely frost -
sunlight and is
Grows well in full
not frost-hardy
Medium size plant, single to multi
rare blue in colour
shade and high
Grows well in half
semi-hardy to frost
sunlight or shade;
Grows well in full
Comments
moisture conditions.
Least concerned
Endangered
Vulnerable
List 2010 (SANBI 2011)
according to the IUCN Red Data
National conservation status
20-30 cm in diameter, green or
stemmed, 1-2 m in height, and
Medium size plant, multi
cm in diameter
time, 4-5 m in height and 30-40
initial erect trunk reclines over
Medium to large evergreen plant ,
Description
(Jacq.) Lehm.
Bedford
Encephalartos
Dyer
KwaQaba
Encephalartos
Lehm.
Bread
Name
Common
Encephalartos
Species
Table 1: Encephalartos species endemic to the Eastern Cape
Habitat requirements for Encephalartos species include forest, savanna and grassland,
and thicket with savanna having the greatest species diversity and species within this
habitat have a high tolerance limit to a range of conditions (Donaldson 2008). Species
found occurring in the thicket, grassland and forest habitats are specific to these
habitats.
In South Africa most Encephalartos species have a decreasing population trend and are
classified as vulnerable to critically endangered (SANBI, 2011).
Encephalartos longifolius(Jacq.) Lehm which was the species of focus for this study is
also an Eastern Cape endemic commonly known as Suurberg cycad is widely distributed
in the southwestern parts of the province (Figure 1). This species was one of the first
cycads to be scientifically recorded in South Africa in 1772 by Carl Peter Thunberg
(Donaldson et al. 2003). According to the IUCN Red Data List in 1978 there were
approximately 4500 wild plants of E.longifolius in the Eastern Cape, however as a result
of human impacts the wild populations has been declining ever since and currently there
are <700 plants left in the wild (IUCN, 2010). Encephalartos longifolius currently has a
near threatened conservation status and if the population continues to decline the
species will soon become endangered to critically endangered (SANBI, 2011).
12
Eastern
Cape
Figure 1: Distribution of Encephalartos longifolius in the Eastern Cape.
2.2.2 Stangeria T.Moore
This genus was classed with ferns until the cones were discovered and only one species
Stangeria eriopus (Kunze) Nash is endemic to South Africa (Chamberlain 1919).
Belonging to the family Stangeriaceae which is a small family that has originated from
Gondwana, Stangeria are perennial, fern-like herbs with subterranean, tuberous,
branched or unbranched stems (Donaldson et al. 2003; Anderson et al. 2007). The stem
may sometimes branch into 10 to12 heads and each head may produce a cone at the
same time (Giddy 1974). Leaves are pinnate with taenopteroid venation or with many
parallel veins and margins maybe serrated, entire of deeply fringed according to the
locality (Giddy 1974; Anderson et al 2007). Male and female cones are silvery pubescent
at first becoming brownish upon maturity. Female cones are much bigger than the male
cones but both have overlapping cone scales (Giddy 1974).
13
Stangeria eriopus is found in eastern coastal grassland and forest habitats and is
distributed in the Eastern Cape and Kwa-Zulu Natal (Giddy 1974; Germishuizen et al.
2006).
2.3 Pollination and Seed-dispersal
Pollination usually occurs in March or April when the microstrobulus elongates to its
maximum length and pollen is shed from the microsporangia (Donaldson 1997). Cones
first emerge during January to February (Donaldson 1997). Female cones start
disintegrating between September and November when seeds are released (Donaldson
1997). Seed germination occurs immediately after the cone bursts and seeds are
released (Giddy 1974). Cycads do not exist in isolation and many of their known
interactions with other species are specific to one or few cycad species (Donaldson et al
2003). Over the years research has shown that cycads have evolved symbiotic
interactions with arbuscular mycorrhizae and nitrogen fixing blue-green algae (Whiting
1963; Giddy 1974). Seed dispersal by vertebrates and invertebrates as well as
environmental factors heavy rains and in particular wind is central to individual species
biology and ecosystem function (Tiffney 2004). Dispersal has many advantages to the
species such that it allows for seeds to escape from potential predators, seed
colonization at favourable growth sites, and competition reduction between parent and
the offspring and between siblings (Tiffney 2004). Seed dispersal also influences
distribution of individual taxa and plant community structure (Tiffney 2004).
Cycads are postulated to be only wind-pollinated (Chamberlain 1925) and as a result of
male and female cones occurring on separate plants, a male and female plants must
cone at the same time and grow close enough to one another for wind pollination to be
effective in order to produce a fertile seed in the wild (Giddy 1974). Wind pollination
forces the pollen grains between the open apical scales from where they gradually shift
spirally downwards through the center axis of the cone (Giddy 1974). As a result of wind
dispersal of pollen immense an amount of pollen is wasted (Giddy 1974). Nevertheless
wind dispersal and pollination is highly effective when it does occur. A study conducted
by Donaldson (1997) showed that there was a significant decrease in seed set when
wind was excluded from the experiment in comparison to wind inclusive experiments.
14
In contrast, some have suggested a role for Insects in cycad pollination (Giddy 1974;
Schneider et al. 2002), however this is highly doubtful because for example bees
collecting pollen on male cones show no evidence of visiting female cones growing
nearby because female cones do not produce pollen and in the event that they are found
on female cones it is probably incidental (Giddy 1974). The role of pollination by certain
weevils for example a curculionid weevil Antliahinus zamiae is also doubtful because
they are found mainly on female cones where they seek out the young immature seeds
in which they lay their eggs (Giddy 1974; Schneider et al. 2002). However subsequent
experimental studies have showed that insects do play an important role in cycad
pollination for example Suinyuy et al (2009) found that three beetle species namely
Metacucujus encephalarti, Erotylidae sp. and Porthetes hispidus are potential pollinators
of a South African cycad Encephalartos friderici-guilielmi Lehm. Insects are known to
play a significant role in dispersal, as pollen may sometimes get stuck on the legs or
body of insects and carried over variable distances where the fate of the pollen is
unpredictable (Schneider et al. 2002).
Other fauna such as birds, dassies, baboons, vervet monkeys and fruit-eating bats all
feed on cycads and indirectly aid in pollination or seed dispersal (Giddy 1974). Baboons
and monkeys often remove the entire cycad cone and carried some distance away from
the mother plant where the fleshy pulp is consumed and poisonous kernels are spat out,
this often results in extensive damage to the meristamatic tissue of the cones (Giddy
1974).
Several bird species particularly the Crowned Hornbill, the Brown-necked (Cape) Parrot
and the Trumpeter Hornbill also aid in pollination/dispersal by breaking down the cones
with their sharp beaks and exposing the drupaceous red seeds or by carrying away
seeds over long distances and eating them during the halts on the way to the roosting
site (Giddy 1974).
Hand pollination of cycads has become popular over the years especially amongst
cycad growers who wish to increase their seed stocks (Giddy 1974). Hand pollination
aims to achieve what wind pollination does however this is dependent on correct timing
and acquiring of pollen (Giddy 1974). Hand pollination can be achieved by collecting
15
large quantities of pollen and refrigerating it, after which it can be lightly sprinkled on the
female cone, however this methodology does not always guarantee viable seed
production (Dehgan and Yeun 1983).
As a result of seed predation mast-seeding in cycads evolved (Janzen 1971). Mastseeding is a phenomenon in which synchronous seed production of seeds occurs within
a plant population in one year followed by a long interval in which few or no seeds are
set (Janzen 1971). This phenomenon is said to have evolved as a behavioral defense
against predators because large amounts of seed production at a single time allows for
predation satiation therefore during the period between the mast years predator
numbers are said to decline as there is a shortage in their food resource (Ballardie and
Whelan 1986).
Seed dispersal however is very important to the species because it provides survival for
the species such as in response to environmental changes it provides a mechanism for
geographic migration in plant populations; it allows the plant, seeds and seedlings in
particular to escape from predators; it provides seeds with the ability to spread over
large areas therefore allowing for cross-pollination to occur as well as distance also
inhibits the spread of pests in new generations; competition between parent and
offspring and amongst siblings is also reduced (Tiffney 2004).
2.4 Propagation and Germination
Propagation of cycads can be achieved by growing cycads from seeds or offsets and
branches (Giddy 1974). Growing cycads from seeds usually occurs when the seed is
viable (fully developed and fertile). Fertility of seeds can be determined in the following
ways (Giddy 1974): 1) immersing seeds in deep water after removing the fleshy
covering, infertile seeds will float whilst heavier fertile seeds will sink to the bottom; 2) cut
seeds open longitudinally and see whether a fertile embryo is present, a fertile embryo is
attached to a thin tightly coiled suspensor and extends to about half the seed length
whilst an infertile embryo has an empty hollow at the micropylar end of the seed. Cycads
are known as prolific seed producers with individual female cones producing
approximately 500 seeds per season (The Cycad Newsletter, 2007). Seeds have an
16
inner stony portion called the sclerotesta and an outer fleshy layer called the sarcotesta,
with both portions being separated by a paper-thin membrane (Whiting 1963). Seeds are
usually grayish-brown in colour and the size of a pecan nut, this feature appears to be
constant for a given species (Whiting 1963; Giddy 1974).
Seed germination is often a very slow process and three separate dormancies are
involved in germination such as: 1) The inhibitory effect of the fleshy coat; 2) the embryo
that needs to reach maturity before the seed can germinate; and 3) the thick stony
(sclerotesta) layer which is thick and prevents entry of water into the seed (Dehgan
1983). Seed germination in the wild is dependent on environmental variables and
symbiotic relationships whereas laboratory germination is dependant on temperature
and moisture and these two parameters vary from species to species (Dehgan 1983).
Propagating cycads from suckers that form at the base of the adult plants involves
opening the hole alongside the stem until the entire stem of the sucker and its roots are
exposed and then carefully sliced off with the use of a sharp-bladed spade (Giddy 1974).
Cuttings are then treated with fungicide and left for a few days to allow damaged
portions to dry out before being planted (Giddy 1974).
2.5 Conservation status
Cycads are group of plants that have global conservation significance, with 40% of the
world’s cycads falling into globally recognized biodiversity hotspots, and a staggering
82% of the world’s cycads species being listed as threatened (Donaldson 2003). In
South Africa cycads are classified as protected or specially protected plants. The
sustainable utilization of wild populations has been adopted at regional, national and
provincial level (Donaldson et al. 2003). In the past Gauteng declared all cycads
Specially Protected Plants and required those whom had cycads in their possession to
apply for a permit, however Gauteng was not the only province to protect cycads, other
provinces and strict protective laws and heavy penalties were laid down by the Nature
Conservation Ordinances of each province (Giddy 1974). Currently due to an increase in
declining cycad numbers, cycads are listed in the CITES (Convention on International
Trade in Endangered Species) Appendix 1 which states that a permit is required for
17
import and export of all cycad species and permission is required from national and
regional authorities such as DEAT, SANBI and SANParks involving any activities on wild
populations (CITES, 2003).
Cycads have been and are still under threat of extinction despite the many attempts
made to conserve the plants and their habitats. The threatened status of African cycads
was recently revised as part of a global revision and as part of the 2010 IUCN Red List
of Threatened Plants and according to the most recent data three South African cycad
species are extinct in the wild, 12 taxa are critically endangered, 4 are classified as
endangered and 10 as vulnerable, with a further 4 taxa classified as near threatened and
only 4 as being of least concern (SANBI, 2011).
Some cycad species are dying out naturally, but the major threat to the survival of
cycads is humans. Human activities have long been responsible for the decline in cycad
numbers (Giddy 1974; Donaldson 2003). Some of these activities include (Osborne
1995; Donaldson 2003):
• Habitat destruction
• Alien vegetation
• Traditional use of species for medicinal or magical purposes
• Trade in wild plant collections
• Urban and rural land demands
• Removal of plants by collectors or traders
• Road and dam construction
• Agricultural development and afforestation.
18
2.6 Demography
Demographic studies are an important tool in assessing the population viability of cycad
populations and are beneficial in cycad conservation because the main goal of the study
is to estimate the growth rate, (increase or decrease in population numbers), of the
population and the extinction probabilities (Gallego 2007). Demographic studies of
cycads was poorly understood in the past because they are time consuming, labor
intensive and data can be inaccurate but regardless of this it has now become a
powerful conservation tool because it is simple to implement and allows for long-term
monitoring of individuals within a population (Miguel et al. 2006; Gallego 2007). Survival
and fecundity are the most important parameters in estimating growth rate where
survival can be estimated by the probability of seedlings becoming adults over a set
period of time, this is achieved by measuring the height and diameter of a set number of
individuals as well as counting the leaf bases for an indication of the age of an individual
(Clarke and Clarke 1987; Giddy 1974; Gallego 2007). Fecundity can be estimated by the
probability of adults producing offspring that survive well into the seedling stages this is
achieved by counting the number of seeds that germinated from seeds produced in the
previous reproductive season, counting the proportion of seed-producing females in the
population and, estimating the average number of seeds produced per female (Clarke
and Clarke 1987; Miguel et al. 2006; Gallego 2007). For effective implementation of
management plans and long-term conservation strategies demographic studies must be
conducted for a minimum period of three years on a single population with regular
monitoring intervals (Miguel et al. 2006; Gallego 2007). Apart from providing useful
information for conservation demographic studies can also contribute towards many
aspects of cycad biology such as herbivory rates, the role of disturbance, and the growth
of new leaves (Clarke and Clarke 1987; Gallego 2007).
19
2.7 Climate Change
2.7.1 The causes and effects of climate change
Global temperatures and carbon dioxide levels have fluctuated throughout history. The
carboniferous period was the only geological period in which global temperatures and
carbon dioxide levels were similar to that of the present (average temperatures of 12°C
past compared to15.5°C of the present); (CO 2 levels of 350 ppm in the past and 390ppm
in the present) (Plass 1956; Buckley 1999; IPCC, 2007). At present global warming is
one of the most important issues concerning scientists. The issue focuses on the
increasing accumulation of greenhouse gases especially carbon dioxide in the
atmosphere caused by industrial activities, and deforestation (IPCC, 2007; Sheikh and
Gorte 2008). Since the 1800’s industrial activity has steadily increased and so has the
atmospheric carbon dioxide levels and global temperature (IPCC, 2000). The impact of
human activity on atmospheric carbon dioxide levels and other greenhouse gases has
become one of the most debated topics of all time. The burning of fossil fuels (oil, natural
gas and coal) and clearing of vegetation are the most common impacts that result in the
increase of atmospheric carbon dioxide (IPCC, 2000).
Global temperature is predicted to increase by an additional 1.5°C and 5.5ºC over the
next century (IPCC, 2007). The projected temperature increase is a global average with
some areas being cooler and some being hotter. Higher temperatures will occur at high
latitudes (the poles), inlands, and in the interiors of continents (IPCC, 2007). According
to the Third Assessment Report of the Intergovernmental Panel on Climate Change
(IPCC, 2001), Africa is one of the most vulnerable continents in the world to climate
change. During the 20th century average surface temperatures have already increased
by approximately 0.7° C and are predicted to increa se further by the end of the century
(IPCC, 2007). In South Africa the Eastern Cape Province is expected to experience the
highest temperature increases towards the north-west interior and along the coast the
lowest increases are likely to occur (Midgley et al. 2007; Johnston et al. 2011). Average
surface temperatures for the Eastern Cape are expected to increase by approximately 2°
C by 2050 with major impacts on the environmental, social and economic aspects of the
province (DEDEA, 2011; Johnston et al. 2011). Temperature increases could result in
increased intensity in droughts and increases in evaporation rates, as well as changes in
the regions rainfall patterns (Johnston et al. 2011).
20
Analysis of bubbles trapped in ice indicates that carbon dioxide concentration in the
atmosphere has varied widely during the last 1700,000 years and closely parallels
variation in global temperatures (Molles 2008). Atmospheric carbon dioxide
concentrations are expected to increase by double its current levels by the 21st century
and these increases will not only affect the global climate but it will also affect the
structure and processes of ecological systems from populations to landscapes (IPCC,
2007; Midgley et al. 2007). It has also been predicted that larger amounts of atmospheric
carbon dioxide could increase the rate of photosynthesis in areas with adequate water
and soil nutrients. This could counter global warming because it would remove carbon
dioxide from the troposphere therefore helping to slow global warming (Miller 2007).
However recent studies have indicated that this counter current effect would be
temporary due to the following reasons (Miller 2007): 1) increased photosynthetic rates
would slow down as plants reach maturity and take up less carbon dioxide from the
atmosphere, 2) carbon dioxide stored by plants would be returned to the atmosphere in
the same composition when plants die, decompose or burn, 3) increased photosynthetic
rates decrease the amount of carbon stored in the soil because more carbon dioxide is
utilized for photosunthesis , and 4) tree growth might temporarily slow carbon dioxide
emissions in the southern hemisphere but will probably increase carbon dioxide
emissions in the northern hemisphere because the northern hemisphere has a higher
deforestation rate.
While the exact nature of increases in temperature and carbon dioxide concentrations is
not known there are predicted outcomes such as:
•
Melting ice and snow (IPCC, 2007)
•
Sea level rise, which will result in further global impacts (IPCC, 2007)
•
Changing ocean currents (IPCC, 2007)
•
Warmer and more acidic seas (IPCC, 2007)
•
Inundation of coastal areas (IPCC, 2007)
•
Increased mortality of coral building reefs (IPCC, 2007)
•
Food production may increase in some areas and decrease in others (IPCC,
2007
21
•
Release of carbon dioxide and methane from arctic soils, accelerating global
warming (IPCC, 2007)
With focus on cycads the following outcomes of climate change could impact the plants
in a positive or negative way:
•
Increased frequency of intense storms (IPCC, 2007).
•
More intense and more frequent heat waves in temperate regions (IPCC, 2007).
•
Increased summer drought in semiarid regions (IPCC, 2007).
•
Dieback of forests due to increased incidents of disease and insect attack (IPCC,
2007).
•
Increased wildfires in dry regions (IPCC, 2007).
•
Widespread extinction of plant and animal species (IPCC, 2007).
•
Changes in precipitation and weather extremes (IPCC, 2007).
2.7.2 What does climate change mean for C3 plants?
C3 plants will show an exponential rise in photosynthesis in response to increasing
temperatures, but once the plant reaches its optimum temperature photosynthesis will
start decreasing (Ward et al. 1999; Kim et al. 2007). This decrease in photosynthesis
(CO2 uptake) is a result of decreased enzymatic activity of RUBISCO therefore reducing
the ability to fix carbon dioxide thus stimulating photorespiration (O2 uptake) (Ehleringer
and Cerling 2002). Temperature increases are unfavorable to C3 plants, however climate
change involves and increase in temperature and carbon dioxide concentrations which
occur concomitantly (Ward et al. 1999; Kim et al. 2007), therefore C3 plants will be
favoured as a result of increased CO2 concentrations because the increase in C3
photosynthetic efficiency that takes place under elevated atmospheric carbon dioxide
levels will outweigh the reduction of photosynthesis that is attributable to higher
temperatures (Sage 1996; Ward et al. 1999; Ehleringer and Cerling 2002). Higher levels
of carbon dioxide will increase the efficiency of photosynthesis, thus accelerating plant
growth; however while C3 plants will show increased productivity in correlation with initial
carbon dioxide increase, productivity will eventually level off over time despite a further
carbon dioxide increase (Tissue et al. 1995). A possible explanation for this is that
increased photosynthesis would slow as plants reach maturity and take up less carbon
dioxide from the atmosphere (Cheng et al. 2000; Norikane et al. 2010).
22
Chapter 3
Materials and Methods
A demographic study of Encephalartos longifolius was conducted to determine the
health of the population in the Eastern Cape. Germination experiments were set up to
determine germination requirements of the species and the photosynthesis pathway of
cycads were determined by measuring the gaseous exchange of Encephalartos
longifolius seedlings. Photosynthetic rates were also used to determine the influence of
elevated temperatures and carbon dioxide levels on cycad seedlings and projection
models of elevated temperatures and carbon dioxide concentrations through geological
time was used to predict the impact future climate changes will have on cycads.
3.1 Demography
Selection of study sites were dependent on the presence of wild populations of
Encephalartos longifolius, as well as the permission granted by the landowners and
conservation authorities to work on the property and with the plants.
3.1.1 Study Sites
The three study sites chosen were Kaboega, Zuurberg Mountain Range and Woodridge
College (Figure 2) which were all within the Eastern Cape region and apart from having
the presence of Encephalartos longifolius in common the study sites differed from each
other.
23
Woodridge
Figure 2: The locality of the three study sites chosen for demographic
study of the cycad Encephalartos longifolius (Jacq.) Lehm.
• Kaboega
The Kaboega area (Figure 2) is surrounded by the Greater Addo National
Elephant Park. It lies on the Kaboega River against the Northern slopes of the
Zuurberg Mountains, surrounded by rugged mountains and densely aromatic
vegetation. It is a hydrographic area situated at 33° 21' S and 25º 22’ S (R.M.
Cowling, pers.comm). Kaboega is an arid to semi-arid area receiving a mean
annual rainfall of about 455 mm per year. Rainfall patterns tend to be evenly
distributed throughout the year with two peaks occurring in February to March
and October to November (I. Ritchie, pers.comm). The temperature is highly
variable with a summer maximum of 32ºC and minimum of 15ºC and a winter
maximum of 15ºC and minimum of 5ºC with frost occurring frequently in winter (I.
Ritchie, pers.comm)
24
This Kaboega area is home to many wildlife species such as baboons, kudu,
bushbuck, vervet monkeys, hartebeest and many other small mammals as well
as many bird species (I. Ritchie, pers.comm). The vegetation of the area
according to STEP (Vlok and Euston-Brown 2002) and Mucina and Rutherford
(2006) as illustrated in Figure 3 includes:
•
Suurberg Quartzite Fynbos
This vegetation type occurs on the mountain slopes and plateaus on sandy
soils and the typical structural type are grassy fynbos with localized patches
of dense ericaceous and proteoid fynbos. On south-facing slopes this
vegetation type can be replaced by thicket vegetation as a result of overprotection from fire or replaced by grassland due to over-burning. This
vegetation type has a least threatened conservation status and endemic taxa
found in it are Oldenburgia grandis (small tree), and Euryops hypnoides, E.
polytrichoides (low shrubs) (Mucina and Rutherford 2006).
•
Albany Thicket
A brief description of this vegetation type includes: it is very dense, semisucculent, thorny and forest-like with an average height of 2-3m. Dominant
species found in Albany Thicket are Olea africana subsp. africana (Wild
olive), Allophylus decipiens (false current), Gymnosporia buxifolia (spike
thorn), Schotia latifolia (bosboerboon), and Euphorbia triangularis (tree
euphorbia) (Mucina and Rutherford 2006).
•
Southern Mistbelt Forest
This vegetation type occurs in the ravines and on mountain slope
This vegetation type is described as multi-layered i.e. it has two layers of tall
trees, followed by a dense shrubby understorey and a well-developed herb
layer. Trees are usually 15-20m tall and grow on soils that are loamy deep
soils with a high nutrient status. This vegetation type has a least threatened
conservation status and endemic species occurring are Herbs: Plectranthus
rehmannii, P. elegantululus, Streptocarpus candidus, S. bolusii, S. silvaticus,
S. fanniniae, Pyrrosia africana and tall shrub: Eugenia zuluensis (Mucina and
Rutherford 2006).
25
Albany Thicket
Kowie Thicket
Southern Mistbelt Forest
Sundays Thicket
Suurberg Quartzite Fynbos
Van Stadens Forest Thicket
Woodridge
Figure 3: Vegetation map showing the dominant vegetation types in all
three study sites using STEP (Vlok and Euston-Brown 2002) and Mucina
and Rutherford (2006).
•
Zuurberg Mountain Range
The Zuurberg Mountain (Figure 2) is a major landscape feature that forms part of
the Greater Addo National Elephant Park and is situated at 33° 21’ 4” S and 25º
44’ 38” E in the Eastern Cape (Kerley and Boshoff 1997). Height above sea level
varies between 250 m to 970 m. Mean annual rainfall of the area is
approximately 722 mm per year with peaks in rainfall pattern during spring and
autumn (Vlok et al. 2003). Winter months are driest and during the summer
months thunderstorms occur which can be the cause for lightening fires. Summer
temperatures reach a maximum of about 29ºC and a minimum of about 19ºC
(Kerley and Boshoff 1997).
Zuurberg is home to many wildlife species such as baboons, impala, bushback,
vervet monkeys, and many small mammals and in past times megaherbivores
such as elephants and black rhino were present in the area (Kerley and Boshhoff
1997; Kamineth 2004).
The dominant vegetation type found at Zuurberg is
26
•
Sunday’s Thicket (Figure 3)
Species occurring in this vegetation type include: tree euphorbias (Euphorbia
triangularis) and Kiepersoi (Cussonia spicata) that emerge above the tree
canopy; abundant species sneezewood (Pteroxylon obliquum), wild olive
(Olea europaea subsp. europaea), bosboerboon (Schotia latifolia);
characteristic species Hippobromus pauciflorus and spekboom (Portulacaria
afra) only occurs on the driest sites and is never dominant. (Pierce and
Mader 2006).
•
Kowie Thicket (Figure 3)
This vegetation type has a least threatened conservation target and occurs
mainly on steep, north-facing dry slopes with soil types ranging from clayey
over the Darlington Dam; sandstone and shale (Wittenberg group); and Algoa
group calcareous sandstone in the south. Vegetation found on moister southfacing slopes support thorny thickets that are dominated by shrubs (Carissa,
Putterlickia, Azima, Gymnosporia), low evergreen trees (Euclea, Pappea,
Cussonia, Hippobromus, Schotia, Ptaeroxylon) and fewer succulent trees abd
shrubs. Endemic taxa found in the vegetation include Faucaria nemorosa
(succulent herb), Wahlenbergia kowiensis (herb), and Albuca crudenii
(Geophytic herb). Kowie Thicket is bioclimatically the core of the Albany
Thicket Biome and the major node of the Albany Centre of Endemism. The
location of this vegetation type is adjacent to a wide variety of other
vegetation types namely: Albany Coastal Belt, Suurberg Shale Fynbos,
Albany Broken Veld, Suurberg Quartzite Fynbos, Great Fish Noorsveld,
Southern Coastal Forest and Eastern Cape Thronveld. Co-occurring of
species from different vegetation types may result from these overlapping
areas which are indicative of varying floristic influences on this vegetation.
The description of Kowie Thicket was according to Mucina and Rutherford
(2006).
27
•
Woodridge College
The Woodridge College (Figure 2) is a private co-educated school in the Eastern
Cape situated along the N2 highway on the edge of the Van Stadens River gorge
near a small town called Thornhill which is roughly about 40 km between Port
Elizabeth and Jeffrey’s Bay (Woodridge official website 2010). The College is
situated on a beautiful country estate, where its environment is actively used for
outdoor activities and environmental awareness programmes (Woodridge official
website 2010). Woodridge also runs various projects such as establishment of
an organic vegetable garden, recycling, and the setting up of cameras for leopard
monitoring in the Baviaan’s Kloof (W. Berrington, pers.comm).
The climate at Woodridge is the similar to Port Elizabeth in that it varies
considerably. The Port Elizabeth area has both summer and winter rainfall
however the maximum rainfall is experienced during winter due to its westerly
position, where it catches the tail end of the cold fronts that bring winter rainfall to
the Western Cape (Schovell 2007).
The Woodridge College is situated on a plateau which drops steeply into the Van
Stadens River gorge (W. Berrington, pers.comm). The vegetation of the plateau
was formally grassland which has now been transformed to alien invasive
vegetation due to high human impacts (W. Berrington, pers.comm). The
dominant vegetation type of this study area is:
•
Van Stadens Forest Thicket Mosaic (Figure 3)
This vegetation type is a mosaic thicket that consists of a complex mixture of
Gamtoos thicket and subtropical forest species. The dominant species
occuring in this vegetation type include: dominant trees Cape chestnut
(Calodendrum capense) and red current (Rhus chirindensis) and the rare tree
Steculia alexandri is characteristic. Tree euphorbias (Euphorbia triangularis)
are present but are never dominant (Mucina and Rutherford 2006).
3.1.2 Field measurments
At each of the study sites approximately 50 cycads were tagged and measured. Plants
were randomly selected and the number of plants measured was dependant on the
28
number of individuals present at each of the study sites. Plants were individually tagged
by nailing numbered metal plates to the middle of the trunk using 25 mm long nails
thereby making it minimally conspicuous to animals in the area. Once tagged the height,
and diameter were measured, and the age of the plant was recorded by counting the
number of leaf base whorls.
In the Kaboega area plants were tagged and measured on the south-facing slopes that
are moister than the north-facing slopes. Initial measurements were taken in June 2010
during periods of high rainfall (396 mm per year) and temperatures ranged between 7°C
and 13°C (SA Weather Service, 2010). After a year m easurements of the same
individuals were taken in July 2011 during periods of medium rainfall and temperatures
ranged between 16°C and 22°C.
In the Zuurberg area species were also measured on the south-facing slopes. Because
tagging was not permitted a diagram of plant positions was drawn at the time of the
initial measurements taken in June 2011 during periods of high rainfall and heavy winds,
with temperatures ranging from 17°C and 20°C. Follo w-up measurements were taken at
the end of November 2011 with temperatures ranging between 16°C and19°C.
In the Woodridge area species were tagged and measured in April 2011 during periods
of minimal rainfall and surrounding temperatures ranging between 22°C and 25°C.
Follow up measurements were taken at the end of November 2011, temperatures
ranging between 19°C and 22°C.
3.1.3 Data Analysis
The frequency of height classes for the plants at each of the study sites was analysed
using 20 cm bin sizes. Plants ranged from less than 5 cm to 219 cm in height.
The relationship of height and diameter and age was determined using the number of
leaf base whorls as a measure of age (Giddy 1974).
Prior to statistical analysis data was tested for normality using Shapiro-Wilks test in
Statistica ® 10.0.
29
A Kruskal-Wallis test fro multiple independent samples was used to determine if there
was a significant difference in the population size structure of the three study sites.
3.2 Germination
Encephalartos longifolius seeds were soaked in distilled water for 2 days to remove the
fleshy outer layer and then soaked in fungicide for 3 days after which they were soaked
in distilled water for a further 4 days to allow for imbibition. Seeds were then potted into
20 seed trays containing vermiculite. Each tray contained 10 seeds, and was placed in a
dark growth cabinet with temperatures ranging from 28°C to 33°C. The germination
process started in September 2010 and seeds were watered twice a week using a spray
bottle to prevent any disturbance to the vermiculite. Each of the seed trays were
numbered and trays 1-15 were placed away from the heat source, and trays 16-20 were
placed close to the heat source in order to determine the effect of heat on germination.
In February 2011 each of the seed trays was wrapped with commercial cling wrap in
order to keep the humidity constant.
3.3 Photosynthetic physiology
Five seedlings were used to determine whether Encephalartos longifolius has C3 or CAM
metabolism. Photosynthesis-Irradiance relationships were determined at midday and
light was measured from 0-1500 µmol m-2 s-1. The effect of temperature on
photosynthesis was determined by exposing five seedlings to a range of different
temperatures in a growth chamber starting with an initial temperature of 20°C.
Temperature was adjusted every 3 days by 3°C. An AD C LCpro+ portable
photosynthesis system Infrared Gas Analyser (IRGA) was used to determine the
photosynthetic rates and irradiance. The cuvette used was a broad chamber that had an
area of 6.25 cm2 and all measurement were conducted at a light intensity above the Ik
value i.e. 200 µmol m-2 s-1. The carbon dioxide concentration inside the chamber was
approximately 421 ppm which was close to the average atmospheric concentrations.
The photosynthesis-irradiance relationship was presented using the Harrison et al.
(1985) PI Curve.
30
Chapter 4
Results
4.1 Demography
Demographic data were non-parametric at all three sites (Table 2).
Table 2: A Shapiro-Wilks test for normality for the demographic data collected at
all three sites
Sites
Kaboega
Zuurberg
Woodridge
Statistical
W
p
W
p
W
p
Height
0.892
<0.05
0.875
<0.05
0.931
<0.05
Diameter
0.890
<0.05
0.958
<0.05
0.921
<0.05
Age
0.900
<0.05
0.874
<0.05
0.911
<0.05
parameters
The Zuurberg and Woodridge populations had more juveniles (<60 cm tall) in
comparison to Kaboega (Figure 4). Only the Zuurberg population had a J-shaped
demography (Figure 4b) indicative of a growing population. At Kaboega juvenile
numbers comprised only a quarter of the population (12 individuals < 60 cm tall) (Figure
4a). The population is growing at Kaboega, however the number of offspring produced
per reproductive season is low. The Zuurberg population, by contrast, had almost 60%
of the population as juveniles (Figure 4b, 28 individuals). Juvenile were also abundant in
the Woodridge population (almost 40% of the population, Figure 4c). Gaps in the height
classes could be a result of individuals being destroyed by animal impacts, human
activities or fires.
A Kruskal- Wallis test showed that there was a significant difference between the height
of the populations at Kaboega and Zuurberg (H= 7.59; N= 100; p< 0.05).
31
>220
200-219
180-199
160-179
140-159
120-139
100-119
12
>220
200-219
180-199
160-179
140-159
120-139
>220
200-219
180-199
160-179
140-159
120-139
100-119
80-99
60-79
40-59
a
100-119
12
80-99
60-79
40-59
20-39
12
80-99
60-79
14
40-59
14
20-39
0-19
Frequency (number of individuals per
height class)
14
20-39
0-19
Frequency (number of individuals
per height class)
16
0-19
Frequency (number of individuals
per height class)
16
N = 50
10
8
6
4
2
0
Height classes (cm)
b
10
N = 50
8
6
4
2
0
Height (cm)
16
c
10
N = 43
8
6
4
2
0
Height (cm)
Figure 4: Frequency of plant height of Encephalartos longifolius at (a) Kaboega,
(b) Zuurberg, (c) Woodridge, measured in June 2010.
32
There was a significant correlation between plant height and age at all three study sites
(Figure 5, Kaboega: R= 0.92, N = 50, p < 0.05; Zuurberg: R= 0.97, N = 50, p < 0.05;
and Woodridge: R= 0.95, N = 43, p < 0.05). As a result height can be used as a
predictor of age without having to count the number of rings of leaf bases to obtain the
age. There was a significant correlation between plant height and age at all three study
sites combined (Figure 16, Appendix B: R= 0.93, N= 143, p < 0.05). As a result of this
the relationship between plant height and age can be applied to all Encephalartos
longifolius plants and other Encephalartos species with similar life histories.
The relationship of diameter and height (Figure 6) also showed a significance correlation
at Zuurberg: (R= 0.459; N= 50; p < 0.05); and Woodridge: (R= 0.671, N= 50; p < 0.05).
In these populations plants grew thicker as they got taller but only up until approximately
60 cm after which the diameter did not increase further even though the stem continued
to grow taller.
33
a
450
y = 0.9155x + 17.193
400
Height (cm)
350
300
250
200
150
100
50
0
0
50
100
150
200
250
300
350
400
450
Age (Years)
250
b
y = 1.0542x + 11.639
Height (cm)
200
150
100
50
0
0
50
100
150
200
250
Age (Years)
250
c
y = 1.185x + 17.937
Height (cm)
200
150
100
50
0
0
50
100
150
200
250
Age (Years)
Figure 5: The relationship between height and age at (a) Kaboega, (b) Zuurberg,
(c) Woodridge measured in June 2010.
34
Diameter at breast height (cm)
160
a
140
y = -0.0181x + 110.13
120
R = 0.008
2
100
juveniles
80
adults
60
y = 1.4365x + 11.519
40
R = 0.6336
Linear (juveniles)
2
Linear (adults)
20
0
0
50 100 150 200 250 300 350 400 450
Height (cm)
Diameter at breast height (cm)
200
b
180
160
y = 0.5931x + 73.337
140
R = 0.1658
2
120
juveniles
100
adults
80
Linear (juveniles)
60
40
y = 0.4279x + 65.303
20
R = 0.0773
Linear (adults)
2
0
0
Diameter at breast height (cm)
250
50
100
150
Height (cm)
200
250
c
200
y = -0.1006x + 158.33
2
R = 0.0277
150
Juveniles
Adults
100
Linear (Juveniles)
y = 0.2672x + 86.562
50
Linear (Adults)
2
R = 0.0218
0
0
50
100
150
200
250
Height (cm)
Figure 6: Relationship between plant diameter and height at (a) Kaboega, (b)
Zuurberg, (c) Woodridge.
35
4.2 Growth Rates
Using the regression of height and age growth rates Encephalartos longifoilus can be
calculated as 1.1 cm + 0.1 cm (S.E.) per year (Figure 5). This low growth rate is
confirmed by using the follow-up measurements of plants at Kaboega that showed that
only 18% of the population increased in height, 76% of the population had no height
increase and 6% of the individuals in the population were destroyed as a result of animal
impacts (Figure 7). The 18% of individuals with a height increase were mainly juvenile
plants (Figure 8). At Zuurberg and Woodridge there was no significant increase in plant
height over the short period Zuurberg: H= 0, N= 100, p < 0.05; Woodridge: H= 0.014, N=
86, p < 0.05).
80
Height Frequency (%)
70
60
50
40
30
20
10
0
0
1
2
Height (cm)
Figure 7: Frequency of change in plant height of Encephalartos longifolius at
Kaboega, measured in July 2011.
36
2.5
Height (cm)
2
1.5
1
0.5
0
0
50
100
150
200
250
300
350
400
450
Height (cm)
Figure 8: Change in plant height in juvenile and adult plants of Encephalartos
longifolius at Kaboega, measured between June 2010 and July 2011 (Vertical Bars
= +S.E.).
4.3 Germination
For the first five months of the germinating period no seeds germinated (Figure 9)
because moisture conditions were too low (a soil moisture of 35% of dry mass). Once
moisture conditions were increased (raised to 76%) seeds began to germinate. There
was a steady increase in germination for the next three months (Figure 9), after which no
further germination occurred.
Germination was higher at 28°C (Figure 10), compare d to 33°C, because higher
temperatures resulted in lower moisture conditions (28%). The germination success
decreased as temperature increased and soil moisture decreased (Figure 10).
High moisture conditions resulted in more seeds germinating however due to a longterm persistence of high soil moisture conditions rotting of seeds occurred (Figure 11).
At a low percentage moisture content no rotting occurred (Figure 11), indicating that high
temperatures rapidly lower soil moisture content therefore making germination
conditions unfavorable. Whilst high moisture levels maybe beneficial to seed germination
too much moisture can also be detrimental to the seed in the long-term.
37
The overall germination rate of Encephalartos longifolius was only 19.5% (Figure 9).
Germination Rate (%)
25
20
15
10
5
t
Se
pt
em
be
r
Au
gu
s
Ju
ly
Ju
ne
ay
M
Ap
ril
ar
ch
M
ct
ob
er
No
ve
m
be
r
Ja
nu
ar
y
Fe
br
ua
ry
O
Se
pt
em
be
r
0
Months (September 2010-2011)
Figure 9: Overall germination of Encephalartos longifolius under controlled
conditions over a 1 year period.
35
Frequency (%)
30
25
20
15
10
5
0
28
29
31
33
Temperature (°C)
Figure 10: Frequency of germinated Encephalartos longifolius seeds under
controlled conditions.
38
Number of seeds rotted
12
10
8
6
4
2
0
28
35
76
Soil moisture content (%)
Figure 11: The number of rotten Encephalartos longifolius seeds at three different
moisture conditions.
4.4 Photosynthetic physiology
Seedlings of Encephalartos longifolius have C3 photosynthesis (Figure 12) – they fix
carbon in the day. The saturation irradiance of Encephalartos longifolius seedlings was
600 µmol m-2 s-1 (Figure 12).
Photosynthesis increased exponentially with an increase in temperature (Figure 13, solid
line). The optimum temperature for Encephalartos longifolius was 33°C after which
photosynthesis declined (Figure 13, dotted line).
39
Figure 12: The photosynthesis-irradiance relationship of Encephalartos
longifolius seedlings (Vertical bars = ± S.E., n = 3) (Harrison et al. 1985).
Figure 13: The photosynthesis–temperature relationship of Encephalartos
longifolius seedlings (Vertical bars = ± S.E., n=3).
40
Chapter 5
Discussion
The photosynthetic response of Encephalartos longifolius to increased temperatures
was as expected for C3 ornamental or woody plants (Sage 1996; Ehleringer and Cerling
2002). Whilst temperature increases photosynthesis this is only as short-term response
of the plant and as the temperature approaches the plants optimum range,
photosynthesis (CO2 uptake) begins to level out (Marler and Willis1997). This is a
typical response of a C3 plant (Sage 1996; Ehleringer and Cerling 2002) but differs from
the response of CAM plants that are more adapted to high temperatures by fixing carbon
dioxide at night when temperatures are much lower, therefore CAM plants have a much
higher water use efficiency because stomata are closed during the day (Ehleringer 1979;
Nobel and Hartsoc. 1986; Drennan and Nobel 2000).
The temperature rise predicted for the Eastern Cape together with predicted decreases
in rainfall will increase the severity of droughts (Midgley et al. 2007). In response to
drought cycads will have increased stomatal closure therefore reducing photosynthesis
and transpiration and lowering the cost of growth (Ward et al. 1999). Other responses of
C3 woody plants to drought include senescing and dropping of many older leaves
thereby resulting in large reductions in leaf area in order to minimize water loss (Marler
and Willis 1997; Ward et al. 1999). As a result of drought the high temperatures and low
moisture conditions are expected to be detrimental to seed germination of Encephalartos
longifolius. The germination trials of this study found that Encephalartos longifolius
germinates best at temperatures between 28°C-30°C a nd moisture conditions between
50% and 75%. The predicted increased transpiration rates as a result of increased
temperature could result in reduced seed moisture content that could contribute to seed
dormancy (Giddy 1974). If germination takes long to be initiated seed dormancy will
persist and eventually result in infertility (Giddy 1974; Dehgan 1983) this coincides with
the initial slow germination rates of this study.
Increase in wildfires is also associated with predicted temperature rise (IPCC, 2007) and
studies done by Donaldson (1995) showed that Encephalartos species have a high
41
incidence of mast-seeding in response to fire (Janzen 1971). This was comparable to
the demographic data collected at the Kaboega study site in which low juvenile numbers
resulted from fires that swept the Southern slopes approximately 8 years ago triggering
mast-seeding (I. Ritchie, pers comm). Other studies have found fire to have a
deleterious effect on Australian cycad species seeds (Hill 2003). While no such data
exist for Encephalartos longifolius it is assumed that intensity in wildfires could be a
critical factor in the long-term viability of the population especially if seeds and seedlings
are killed by fire thereby disrupting regeneration. Seedlings are sometimes more
susceptible to fire due to the possession of lignotubers (a swelling at the base of the
stem just above the soil level) that helps them survive fires by sending out new growth if
the top growth is damaged (Plate 1, Appendix A) (Chamberlain 1925). Adults are also
vulnerable to fires which probably account for the gaps in the older classes as recorded
at Kaboega (Chamberlain 1925; Donaldson 2003).
Whilst C3 plants may be disadvantaged in hot dry climates due to photorespiration Zuo
et al. (2004) found little effect of increased temperature on the function of the
chloroplasts of Cycas multipinnata and Cycas panzhihuaensis which was indicative of
cycads adapting to the prevailing climatic conditions. The exponential photosynthesis
response of Encephalartos longifolius to temperature increases is too simplified to derive
conclusions of climate change impacts on cycads especially since climate change does
not only involve temperature rise but it also involves a rise in carbon dioxide
concentrations. It is predicted that as a result of global carbon dioxide concentrations
rising at an alarming rate global temperature will also rise (IPCC, 2007), therefore the
rise is carbon dioxide and temperature are going to occur concomitantly (IPCC, 2001;
Kim et al. 2007). While temperature increases in the Eastern Cape seem to be
unfavorable to C3 plants, a rise in carbon dioxide concentrations also need to be taken
into consideration since it is the basic raw material that plants require for photosynthesis
(Ehleringer 1979). Based on the typical response of C3 woody plants to elevated
temperature assumptions were made that Encephalartos longifolius will follow the similar
C3 response to elevated carbon dioxide concentrations. An increase in carbon dioxide
concentrations is postulated to favor plant growth and development especially in C3
plants (Ehleringer and Cerling 2002). Even though Encephalartos longifolius showed an
exponential rise with increasing temperature, the temperature optimum for plant growth
42
will be much higher in response to predicted elevated CO2 concentrations and
photorespiration will be inhibited therefore making photosynthesis much more efficient
(Ward et al. 1999; Kim et al. 2007). Elevated carbon dioxide levels will also mitigate the
impacts of drought by producing a more convoluted root system which will ease the
accessibility of water therefore increasing water use efficiency (Ward et al. 1999). The
roots of Encephalartos longifolius are well known for their symbiotic relationship with
blue-green alga Anabaena. As a result of elevated carbon dioxide concentrations this
symbiotic relationship will be enhanced and will help the plant to adapt to hot dry climatic
conditions (Saxe et al. 1998). Newton et al. (1994) also found that the enhancement of
this symbiotic relationship by elevated CO2 concentrations will be of great benefit to
slow-growing plants and cycads are well known for their slow-growth rates (Chamberlain
1919). This was comparable to the data of this study that showed that Encephalartos
longifolius grew just over 1.1 cm per year and then only in the juvenile plants. Growth
and biomass of Encephalartos longifolius is also assumed to increase as a result of
increased carbon dioxide levels because according to Norby et al. (1999) carbon dioxide
is essential for wood formation in woody plants therefore increased concentrations of
carbon dioxide will speed up wood formation and thickening resulting in greater plant
height and diameter. Increased carbon levels will also contribute to more active and
extensive root systems, as well as further enhance cone and seed production and leaf
stomatal density (Atwell et al. 2003; Yazaki et al. 2005).
Increased carbon dioxide levels are presumed to be beneficial to cycad growth, however
these are only short-term responses as for all C3 woody plants and in the long-term
photosynthesis will eventually reach equilibrium as plants reach maturity and take up
less carbon dioxide regardless of further CO2 increases (Tissue et al. 1995; Cheng et al.
2000; Norikane et al. 2010).
Whilst increased carbon dioxide concentrations might prove to be more beneficial to C3
plants in comparison to temperature by outweighing the effects of increased
temperatures the interaction of these two climate variables need to be considered for
possible climate change impacts on plants. The outcomes of the interaction of these two
variables on the Eastern Cape environment according to the predictions of the IPCC
(2007) and Midgley et al. (2007) may prove to be a disadvantage to Encephalartos
43
longifolius over time. Whilst there is no data to support this theory a possible impact of
climate change on the Eastern Cape environment that could impact Encephalartos
longifolius is the intense frequency of storms which would result in an extreme leaningover effect of the taller plants in the population (Plate 2, Appendix A) due to its nonextensive root system (Chamberlain 1919).
Based on theoretical understanding and historical data the hypothesis of this study was
accepted. Cycads existed in a time when temperature and carbon dioxide levels were
much higher than either the present (Figure 14) and the levels predicted for the future
(Figure 15). When cycads first appeared in the late Carboniferous period the average
global temperatures were 12°C and carbon dioxide co ncentrations were 350 ppm which
is similar to the present temperature of 15.5°C and carbon dioxide concentration of 390
ppm (Figure 14 and Figure 15) (Plass 1956; Buckley 1999; IPCC, 2007). During the first
glaciations period when global temperatures and carbon dioxide concentrations rapidly
decreased this resulted in a decrease in cycad abundance (Figure 14); however when
temperature and carbon dioxide concentrations began to raise again in the late Permian
period, cycad abundance started to increase in a recovery phase (Figure 14) (Buckley
1999). It was during the Jurassic period that cycads reached their peak abundance were
average temperatures were about 25°C and carbon dio xide concentrations about 1200
ppm, after their numbers began to decline and this continues to the present (Figure 14)
(Plass 1956; Buckley 1999).
44
Figure 14: Fossil records of cycad abundance with changing temperature and
carbon dioxide levels through geological time (Plass 1956; Buckley 1999).
A comparison of past and present climatic conditions reveal that even though the
average global temperature and carbon dioxide concentrations of the Jurassic period
were much higher than that of the present (Figure 15), cycads still reached their peak
abundance at that time thereby indicating that they were well adapted to such
conditions.
45
Figure 15: Projections of past, present and future temperature levels and carbon
dioxide concentrations according to the IPCC, 2007 Assessment Report and
Midgley et al. 2007.
Even though global temperatures and carbon dioxide levels are expected to increase in
the future with average temperatures of about 21°C and carbon dioxide concentrations
of about 1000 ppm (Figure15) , historically the earth has been much hotter and drier and
had a higher concentration of carbon dioxide compared to present times, therefore
assumptions can be made that future increases in temperature and carbon dioxide
levels as outlined in (Figure 15) will not impact on the abundance of existing cycad
populations.
Based on the studies of McElwain (1998) on stomatal data, it is believed that cycads
were well adapted to fluctuations in temperature and carbon dioxide levels and were
able to acclimate themselves to the changes in these two climatic variables thereby
allowing them to persist in the environment for many years. Regardless of predicted
climate changes in the Eastern Cape Encephalartos longifolius will not be directly
impacted by this change because increase in temperature and carbon dioxide
concentrations will occur gradually over time, therefore allowing the species to adapt and
acclimate to the changes, as predicted for cycad Dioon edule to fluctuations in CO2
levels and stress induced conditions (Vovides et al. 2002).
46
Encephalartos longifolius is a near threatened species and whilst climate change may
not directly impact the species there are many other factors that are contributing to its
declining population numbers especially in the wild. The demographic data of this study
attempted to determine the vulnerability of the species in the wild by using the presence
of juvenile numbers as an indicator of the health of the population with more juveniles
indicating a healthy and growing population and fewer juveniles indicating an unhealthy
population (Gallego 2007). Juvenile numbers at Kaboega were low. A preliminary study
of the health of cycad species Encephalartos longifolius in 2008 showed the population
to be healthy with a large number of juveniles present (Wakeford et al. 2008). Two years
later the initial results of this study showed a rapid decline in juvenile numbers, and a
further decline the year after. Juvenile numbers at Zuurberg and Woodridge were fairly
high which indicates these populations are healthy. Ruling out the impacts of climate
change the major drivers to this decreasing population trend of Encephalartos longifolius
are human and animal impacts. Whilst this study did not focus on human and animal
impacts, data from past studies and visual observance was used to explain the
population trends found at the three study sites.
The animal impacts at Kaboega on cycad species include: trampling and knocking over
by large mammals (Plate 3, Appendix A); baboons having the highest impact as they
feed on cones and seeds therefore preventing seeds from germinating (Plate 4,
Appendix A); warthogs dig out seedlings to consume roots and bulbs; and porcupines
eat mainly at the base of the trunk therefore making it more vulnerable to be knocked
over by large mammals (Plate 3 and Plate 5, Appendix A) (R.M. Cowling, pers.comm; I.
Ritchie, pers.comm). As a result of such animal impacts the declining juvenile population
could also be a result of the mast-seeding phenomenon in which a large amount of
seeds are produced synchronously within a plant population in one year followed by an
interval in which few or no seeds are set in order to minimize predator satiation (Janzen
1971). This theory was tested by Donaldson (1993) on the genus Encephalartos in
which he found that low levels of seed predation resulted from species that produced
seeds sporadically. Encephalartos longifolius reproduces sporadically which is
contributing to this declining juvenile number because even though mast-seeding is
effective in limiting predator impacts on the plant, the survival of the seed is very low and
sometimes germination does not occurs (Ruth et al. 1986; Li et al. 2007).
47
Animal impacts at Zuurberg were of a lesser extent than Kaboega, the results of this
study for Zuurberg showed a bimodal distribution pattern in height classes which
coincides with the results found by Kamineth (2004) on the impacts of megahebivores
on tree euphorbias. The presence of megaherbivores in an area results in larger
individuals being felled rather than juveniles, juveniles would eventually mature into
reproductive adults and produce a cohort of juveniles and the ages of these cohorts
would depend on the absence of the megaherbivores from the area. Megaherbivores
were present in the area before the 1750’s (Kamineth 2004), which is almost about 261
years ago which explains the gaps in the older height classes (200-219 cm), and no
cycad older than 220 years was encountered in this study (personal observations). Apart
from the impacts of megaherbivores other animals such as baboons and porcupines
also impact the species but to a much lesser extant in comparison to Kaboega
(Donaldson 2008).
Animal impacts are not always a disadvantage to the population. Some impacts prove to
be quite beneficial to the population especially in terms of seed dispersal (Giddy 1974).
Birds in particular are well-known for the role in seed dispersal as they carry seeds away
from the parent plant over long distances (Giddy 1974). The results of this study at the
Woodridge population support this theory because the population of cycads at
Woodridge had a very scattered distribution (Giddy 1974; Tiffney 2004; personal
observations). Dispersal increases the seeds chances of survival as it allows seeds to
escape from potential predators and pests; it reduces parent-offspring and sibling
competition and seeds are spread over large areas (Tiffney 2004), which would explain
the high juvenile numbers at Woodridge.
Apart from animal impacts, human impacts are one of the major threats responsible for
declining wild populations and removal of plants for trade is the most common human
impact (Osborne 1995; Donaldson 2003). As expected, wild populations are vulnerable
to human impacts. In 1978 the IUCN records showed that approximately 4500
Encephalartos longifolius plants were present in the wild, currently this number has
declined between 50% and 70% (Anderson et al. 2007; Donaldson 2003; Donaldson
2008). In the past plants at Zuurberg were removed for the following purposes: trade to
collectors, used in private collections as ornamental plants, medicinal uses and for illegal
48
seed harvesting and selling of seedlings. Currently the remaining individuals have
tracking devices inserted into their trunks which has been effective in minimizing removal
rates (Wilson, pers.comm). Low adult numbers and gaps in the adult height classes at
Woodridge are a result of habitat destruction during previous years; however restricted
access to the school and continued monitoring has contributed to the currently high
juvenile numbers (W. Berrington, pers.comm).
The threats of climate change on Encephalartos longifolius are poorly understood,
however the response of C3 plants to elevated temperatures and carbon dioxide
concentrations coupled with historical data and responses of other cycad species to
environmental stress indicate that Encephalartos longifolius will be able to adapt to the
predicted climate change for the Eastern Cape and persist in the environment for the
next 200 years, but particular concern needs to be given to the threats of human and
animal impacts on the abundance of wild populations.
49
Chapter 6
Conclusion and Recommendations
The main focus of this study was to gain insights on the potential impacts of predicted
climate change in the Eastern Cape on Encephalartos longifolius and the results of this
study can be used as a baseline study for all South African cycads since very little is
known about the photosynthetic physiology of these extraordinary plants.
Like all cycads Encephalartos longifolius is very-slow growing which is often the primary
cause of their decline in the wild. Seeds that take long to germinate often lose their
viability and seedlings that take long to mature are more susceptible to predator attacks,
however the concomitant relationship between predicted increase in temperature and
carbon dioxide could prove to be beneficial to the plants growth rate. Low juvenile
numbers in the wild are also a matter of concern for the long-term persistence of the
plants in the environment.
The data of this study has shown that Encephalartos longifolius has a typical C3
response to increasing temperatures and elevated carbon dioxide concentrations. Whilst
increased temperatures may be detrimental to the plant coupled with elevated carbon
dioxide levels this could prove to be beneficial to the plant; however these responses will
only be short-term. The impacts of climate change on cycads is poorly understood but
based on historical data cycads tend to be well adapted to handle fluctuating
environmental conditions and stress. Over the years cycads have acclimated to climatic
changes and will continue to do so in the future. The primary feature of cycads are their
extensive root system that allows them to adapt to periods of drought and low moisture
and its symbiotic relationship with soil microbes provides survival for the plant in nutrient
poor soils. Predicted climate change for the Eastern Cape is concluded to have no
impact on the survival of Encephalartos longifolius, however the population is declining
in the wild and based on present knowledge animal and human impacts are a major
cause of concern for the plants ruin in the wild.
50
Although this study serves as a preliminary investigation into the population dynamics of
Encephalartos longifolius and its response to predicted climate change in the Eastern
Cape it has been very valuable in identifying the physiology of cycads and the major
contributors to declining plant numbers in the wild therefore this study can be used as a
baseline study for other South African Encephalartos species with similar life histories. I
recommend the following for future studies and effective conservation measures:
•
Photosynthetic physiology of cycads needs to be investigated in greater
depth with particular focus on South African cycads.
•
Experiments need to be set up in order to directly assess animal impacts on
wild populations.
•
Monitoring should be designed to enable an assessment of population size
and age-structure dynamics; coning and mast-seeding events; and the
response of seeds, seedlings and adult plants to fires.
•
Habitat condition should be assessed especially in relation to alien invasive
abundance.
•
Experiments need to be set up to monitor pollinator abundance and
movements which could provide useful information for increasing seed
production in ex situ conservation.
Cycads are an extraordinary group of plants that can persist in our environment for many
years to come provided that threats to their survival are minimized as best possible.
51
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61
Appendix A
List of Plates
Plate 1: Lignotuber on Encephalartos longifolius stem in response to fire.
Plate 2: Leaning-over effect of Encephalartos longifolius
62
Plate 3: Encephalartos longifolius trampled and knocked over by large mammals
Plate 4: Encephalartos longifolius cone damaged by baboons
63
Plate 5: The base of Encephalartos longifolius stem impacted on by porcupines.
64
Appendix B
Additional Graph
500
450
400
Age (Years)
350
y = 0.9202x - 9.1828
300
250
200
150
100
50
500
450
400
350
300
250
200
150
100
50
0
0
Height (cm)
Figure 16: The relationship between plant height and age at all three study sites
combined.
65