Download `Pre-dispersal losses and dispersal of seeds in the Desert Biome

‘Pre-dispersal losses and dispersal of seeds in
the Desert Biome’.
Table of Contents
1.
Introduction .................................................................................................................... 2
2.
Seed losses in an arid environment ............................................................................... 2
3.
Counteracting of pre-dispersal hazards .......................................................................... 5
4.
Low seed sets and sparse populations .......................................................................... 7
5.
Seed predation and dispersal strategies ........................................................................ 8
6.
Seed predation and population dynamics .................................................................... 10
7.
Favoured seed dispersal strategies.............................................................................. 11
8.
The role of antitelechory in arid regions ....................................................................... 12
9.
Phase II dispersal vs. Phase I dispersal in arid environments ...................................... 13
10.
The role of dispersal effectiveness and reliability in seed dispersal success in arid
environments ...................................................................................................................... 14
11.
References ............................................................................................................... 16
List of Figures
Figure 1: Population dynamics in response to predation (Crawley, 2000)…………10
1
1. Introduction
Deserts are characterised by extreme variation in climatic conditions. Of all the biomes
in Southern Africa, the Desert Biome has the lowest annual precipitation and also the
highest variability in precipitation (Mucina & Rutherford, 2006). Thus desert plants
have to optimally utilise the very limited time when conditions are suitable for
development (Van Rheede van Oudshoorn et al. 1999).
Desert plants also have adaptations relating to seed dormancy, which has been
observed to be highly variable, depending on environmental conditions such as
nutrient levels, soil moisture and temperature (Cowling et al. 1997).
An important factor which influences desert plants is the minimum amount of
precipitation necessary to initiate germination. Furthermore, desert plants have also
adapted to their environment through specialised modes of seed dispersal. The mode
of dispersal in turn influences germination patterns (Cowling et al.1997).
Seed dispersal methods count among the most important factors which influence
community structure and dynamics. Seeds in desert environments can be dispersed
by various methods, including dispersal by faunal species such as invertebrates, birds
and small mammals. Desert plants also show different adaptations for short range and
long range dispersal, often on the same parent plant. This optimises the chances of
seeds to be distributed to favourable micro-habitats (Cowling et al. 1997).
Thus desert plants have many unique adaptations relating to seed dormancy,
dispersal methods, germination patterns and seed structure, which allow them to
optimally adapt to this environment of extreme variability. In the following sections,
these adaptations will be discussed in detail.
2. Seed losses in an arid environment
Seed losses can in occur both the pre- and post-dispersal phases of the reproductive
cycle of plants in arid environments. This is primarily caused by biotic and abiotic
factors.
2
Biotic factors
Seed predation is the most important biotic factor which causes seed loss in plants.
Mammals, invertebrates, birds, pathogens and fungi are the primary predators of
seeds. Predation can occur during different life stages of the plant (i.e. pre-dispersal
and post-dispersal), and different predators are responsible for seed loss during these
stages. During the pre-dispersal stage (seed development), the most influential
predators are invertebrates. Furthermore, seeds and potential seeds are also lost due
to larger herbivores consuming fruits, flowers and seed heads (Chambers &
Macmahon, 1994).
Parasitism due to larvae within seeds or inflorescences also cause seed loss in the
pre-dispersal phase of development (Fenner & Thompson, 2005).
If a seed has not been dispersed to a safe locality following Phase I dispersal, it is
susceptible to predation, and therefore, seed loss. In the seed bank, seeds are
susceptible to fungi, pathogens and larger vertebrates which are able to dig for seeds
(Chambers & Macmahon, 1994).
Abiotic factors
Abiotic factors which cause seed loss include crushing, deep burial, burning,
waterlogging and crushing. These abiotic factors interact with biotic factors and
contribute to seed loss, and have an important effect on plant population dynamics
(Chambers & Macmahon, 1994).
Seed sets, in relation to fruit sets (where many fruit may contain few seeds or vice
versa) also contributes to seed loss. Annual plants usually have a higher seed
percentage in relation to fruit set. This usually occurs as a response to environmental
conditions (Fenner & Thompson, 2005). Incomplete pollination of fertile ovules also
contributes to seed loss, and is also a response to environmental conditions where
pollinating agents may be less prolific or effective (Fenner & Thompson, 2005).
Furthermore, fertilised ovules may be aborted during unfavourable conditions,
reducing the reproductive cost to the parent plant, but leading to seed loss (Fenner &
Thompson, 2005).
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Central to the above paragraph are environmental (abiotic) factors. Unfavourable
conditions lead to a limitation in reproductive resource allocation which has an effect
on seed development. Thus unfavourable conditions will limit available resources,
limiting seed development or causing ovule abortion, resulting in seed loss (Fenner &
Thompson, 2005).
Abiotic factors have an important effect on germination of seeds, and failed
germination contributes to seed loss. Unusual or variable climatic conditions can
cause mortality in germinating seeds, and therefore seed loss. High soil moisture can
stimulate germination, but continued high soil moisture can cause waterlogging of the
seed and subsequently death. Unseasonal events (such as rain during the dry season)
can stimulate seed germination, but the subsequent dry conditions will result in seed
mortality. Furthermore, seeds may be established in a suitable habitat for germination,
but conditions may not be favourable for continued survival, resulting in death
(Chambers & Macmahon, 1994).
Arid environments
Thus, taking the above into account, arid environments such as deserts pose many
challenges to seeds in both the pre- and post-dispersal stages of development. The
highly variable nature of environmental conditions in deserts (unpredictable
precipitation, long dry spells and extreme heat) has an effect on seed development.
Unusual events such as the current high rainfall in the Namib may stimulate high seed
production because favourable conditions are created and resources are abundant.
The high volumes of seeds may however be significantly decreased due to mortality
caused by waterlogging, infections by fungi and pathogens and a possibly very
prolonged dry spell after the rains, resulting in failed germination.
Post-dispersal risks to seeds in arid environments include predation by birds and
invertebrates such as ants which results in seed losses. Furthermore, seed loss due
to fungi, failed germination and pathogens are also significant contributors (Chambers
& Macmahon, 1994).
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3. Counteracting of pre-dispersal hazards
One of the most hazardous phases in the plant’s lifecycleis the pre-dispersal phase of
seeds. Firstly, only a small proportion of the ovules develop into viable seeds.
Furthermore, pollination failure, limiting resources, seed predation and genetic defects
also contribute to pre-dispersal seed loss (Fenner & Thompson, 2005)
Thus plants have adapted to these challenges through evolutionary processes in order
to optimise their chances of successful seed production and dispersal, which are
discussed below (Fenner & Thompson, 2005).
Fruit and seed set
In many plant species, only a certain percentage of flowers develop into fruits. In
addition, the fruits that do develop have highly variable seed sets (number of seeds
within individual fruit). Annual plants seem to have a higher seed set percentage than
perennials (Fenner & Thompson, 2005).
Although the seed set may be partially determined by genetic factors, it seems that
environmental factors also play a significant role. Plants tend to produce excess
flowers and therefore a large amount of potential fruits and seeds. When
environmental conditions are favourable the plant is able to optimally exploit the
occasion by producing large volumes of seeds. Limiting fruit and seed development
can save significant amounts of resources when environmental conditions are
unfavourable. The same principle applies to predation, whereby the plant is able to
reproduce even after predation has occurred through the excess in potential seeds
(Fenner & Thompson, 2005).
Incomplete pollination
Only some of the ovules in plant populations are pollinated and in turn fertilised. This
can be a response to unfavourable environmental conditions, where limited pollination
produces limited fruit and, in turn, limited seed production (Fenner & Thompson,
2005). By employing this strategy, plants are able to avoid allocating precious
resources to seed development when conditions are unfavourable.
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Ovule abortion
The phenomenon of ovule abortion is another strategy where potentially inferior
offspring are eliminated and the potential for self-pollination is decreased, thus
increasing fitness. This strategy can also be applied when environmental conditions
are unfavourable (Fenner & Thompson, 2005). Thus the pre-dispersal hazard of
producing too many seeds or seeds of inferior genetic quality is decreased in severity
and probability.
Resource limitation
Developing seeds compete for resources within the parent plant from their early origins
where fruits compete with other fruits within inflorescences and ovules compete with
ovules within fruits (Fenner & Thompson, 2005).
Environmental factors such as nutrient and water availability further influence this
process. When resources are readily available, competition within the parent plant will
be less severe. However, once resources decrease, competition increases, and seed
sets decrease (Fenner & Thompson, 2005). This prevents formation of fruit and seeds
when conditions are unfavourable, preventing the unnecessary loss of seeds when
dispersed.
Pre-dispersal seed predation
Seed predation before dispersal is one of the major factors contributing to seed loss.
One of the ways to counteract predation is by producing smaller inflorescences. The
disadvantage of this is that the inflorescence attracts less pollinators (Fenner &
Thompson, 2005). Flowering regimes also influence seed predation, whereby plants
counteract predation by flowering at times during the season when potential predators
are less active (Fenner & Thompson, 2005).
These strategies all aim to prevent pre-dispersal seed loss due to predation, thereby
increasing the probability of survival of the plant population.
Strategies for arid environments
When taking the above into account, it is clear that there are many strategies which
plants in arid environments can utilise to prevent pre-dispersal hazards. Annual plants
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form a significant part of the makeup of the desert plant community. They tend to
produce higher seed sets that perennials, and when conditions are favourable, they
are able to exploit the situation by producing many seeds. In addition, when conditions
are unfavourable, seed sets can be reduced.
Due to the highly variable conditions in deserts, seed losses can be extremely high.
Plants can counteract this by aborting ovules, thus limiting fruit and in turn seed
production. Desert plants can also limit seed predation by limiting the size of
inflorescences by ants and small mammals.
4. Low seed sets and sparse populations
In general, density dependent effects are negative, i.e. the higher the population
density, the higher the mortality rates and the lower reproductive rates due to
increased competition. Very small or sparse populations tend to produce smaller seed
sets, and seed fertility tends to be lower than in denser populations. Plants at the edge
of denser communities show similar traits in terms of seed production One explanation
for this is that less pollinators visit these isolated and/or sparse communities, and in
turn less pollen is available for fertilisation. Furthermore, seed predators may be less
prevalent in sparser communities. Sparse communities may also be a result of
unfavourable environmental parameters, and thus produce lower seed sets. Habitat
fragmentation, a significant threat to conservation, also has the effect of lowering seed
production in plant communities (Fenner & Thompson, 2005).
All of the above contribute to lower pollination incidents, less genetic variability and in
turn lower seed volumes with less vigour and fitness. This in turn means that the fertility
levels of such communities may be below the critical level for regeneration and
subsequent survival (Fenner & Thompson, 2005).
The Allee effect describes the formation of an aggregation of organisms where a
positive effect on survival rates is observed. In plants this means that seed production
is higher, competitive ability increases and fertility rates are higher. In desert
communities where environmental factors influence reproduction greatly, and plant
communities tend to be isolated and sparse, the Allee effect can counteract the above
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effects and increase survival rates to form a self-sustaining population (Fenner &
Thompson, 2005).
5. Seed predation and dispersal strategies
In desert environments, rodents and ants are the most prolific seed predators because
of their harvesting and hoarding activities. Therefore, many plants have adapted to
this association which is both antagonistic and mutualistic (Van Rheede Van
Oudshoorn et al. 1999). The main advantage of dispersal by animals is that they are
mobile and may cause seeds to be distributed significant distances away from the
parent plant. In addition, seeds may also be distributed into the immediate vicinity
through invertebrates. Seeds also have a larger chance of being distributed to
favourable habitats because the animal vectors inhabit or migrate through similar
habitats to where the seed was originally consumed (Stiles, 2000).
Seed predators are able to actively or passively transport seeds externally and
internally (Stiles, 2000). The transport methods are discussed below:

Active external
Seeds are selected for caching, and are thus transported by animals such as ants
and rodents and stored for long periods. Not all seeds are necessarily consumed,
and are thus able to germinate provided that they can survive the long storage
period through dormancy. These seeds are normally lightweight (Stiles, 2000).

Passive internal
Seeds are consumed as part of other food sources or of the parent plant itself and
distributed by the animal. These seeds are normally able to survive the digestive
process of the animal vector (Stiles, 2000).

Active internal
Seeds are actively consumed by animals for food. Therefore, an association
develops between the seed plant and the animals which utilise its seeds. Factors
such as location of the seed on the parent plant, morphological characteristics,
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ability to survive the digestive process, nutritional value and presence/absence of
toxins influence the type of association (Stiles, 2000).
It would appear that the relationship between plants and animals in terms of seed
dispersal is a co-evolutionary one, but the relationship seems to be unbalanced, and
thus still evolving towards a stable state (Fenner & Thompson, 2005).
However, some relationships do seem to exist between animal size and seed size.
Where ants are the primary dispersers, seeds need to be small and light enough to be
carried by the ants. Where the seed is to pass through the digestive tract of the
disperser, the seed needs to be small enough to pass through the mouth and throat
of the animal (Stiles, 2000).
Seed placement on the parent plant is also a function of the target dispersal species.
For example, where rodents such as mice are the primary targets, the seeds are easily
accessible for them and are also attractive in terms of size (Stiles, 2000).
Another challenge that the seed faces is the actual predation process, where risks
such as crushing by the teeth of the predator are present. Some fruits such as
strawberries contain multiple hard seeds of which only some are crushed and others
pass through the digestive system unharmed. Other plants may have irritants such as
spiky hairs on the actual seed pods, causing the predator to drop the pod with only
some of the seeds being consumed (Stiles, 2000).
The processes in the gut of predators also influence the morphology of seeds adapted
to this means of dispersal. Seeds need to be able to survive extended periods within
the digestive systems of dispersing animals to still be able to germinate once passing
through. Seeds adaptations include hard, indigestible outer shells which are resistant
to digestive enzymes and grinding within the digestive system. Seeds may also benefit
from the digestive process through added nutrients in the animal’s faeces once
defecated, and the actual digestive process may also be an important part of the
germination process of some seeds (Stiles, 2000).
Animals may also be attracted to seeds due to their nutrient content in the form of fats,
proteins and carbohydrates. This can influence which animals select certain seeds as
a food source. This then forms part of the mutualistic relationship between certain
plants and animals which act as dispersal agents (Stiles, 2000).
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Strategies in arid environments
In arid environments such as deserts, ants and rodents are the primary predators of
seeds (Van Rheede van Oudshoorn et al., 1999). The process where seeds are
dispersed by ants is known as myrmecochory. Species which rely on dispersal by ants
have an oily structure known as an elaiosome which attract ants as a source of food.
The ants then consume this and the intact seed is discarded on the ‘refuse dump’ of
the nest. This then allows for germination. The sites where the seeds are discarded
often have high nutrient values, providing favourable conditions for germination and
growth. Plants may also shed their seeds at certain times to facilitate the predation by
ants rather than rodents by coinciding shedding with the peak activity time of the ants.
The process of myrmecochory is also an effective way of dispersing seeds without
having to allocate excessive resources (Stiles, 2000).
Rodents tend to collect larger seeds which are higher in nutrients (Van Rheede van
Oudshoorn et al., 1999). Thus larger seeds attract rodents, and plants relying on
rodent dispersal will produce larger seeds to ensure effective distribution to favourable
germination sites.
6. Seed predation and population dynamics
Seed predation has an important effect on population dynamics, depending on the
density of the community. The figure below and subsequent text aims to explain the
dynamic.
Plant recruitment
Microsite limited
Predator limited
Seed limited
Seed input
Figure 1: Population dynamics in response to predation (Crawley, 2000).
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As can be seen from the figure above, when seed densities are low as in low density
plant communities, seed predators have a significant effect on recruitment. Plants are
not able to compensate for high seed predation values because they are not able to
produce enough seed. At intermediate seed densities, recruitment will increase
because production is largely equal or more than predation values. When high
volumes of seeds are produced, the predation effect is largely negated, and
recruitment is dependent on microsite conditions and competition for resources within
the community (Crawley, 2000).
In arid environments, plant communities tend to be more sparse and open. Microsite
limitation tends to have a less significant influence on the population dynamic, along
with seed limited recruitment. Most studies indicate that changes in the recruitment
dynamic of plant populations seem to be short term changes, rather than a specific
response to seed predation (Crawley, 2000).
However, the removal of seed predators from specific populations in arid environments
have shown significant increases in species which seeds are preferred by the
predators, thus having a marked change in the population dynamic (Van Rheede van
Oudshoorn et al.1999).
7. Favoured seed dispersal strategies
The methods of seed dispersal in plants are as varied as the environments which
plants grow in, and are also influenced by these environments. The main methods of
dispersal, along with their advantages, in arid environments are discussed below.
Wind dispersal (Anemochory)
Studies by Van Rooyen et al. (1990) in Namaqualand indicated that seeds of the
majority of plant species in this arid environment are mainly adapted for
anemochorous dispersal. This method of dispersal is present in most of the world’s
vegetation types, wind is especially prevalent in deserts due to the extreme
temperature differences during the day. It was also found that the period of highest
seed release (dissemination) was during the period when wind velocities were the
highest, thus utilising the suitable conditions optimally.
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Water dispersal (Hydrochory)
In the same study by Van Rooyen et al. (1990), it was found that hydrochory is a less
important mode of seed dispersal. The reason for this is the highly variable and
unpredictable precipitation events in arid environments. Indirect dispersal occurs in
flood events when seeds are transported with flood water. Some species possess
open capsules out of which seeds splatter when raindrops fall into the cups.
Discharge dispersal (Autochory)
Some species were found to have the ability to disperse their seeds autochorically
(van Rooyen et al. 1990). This method is more prolific in regions with open or sparse
cover, as is found in desert environments.
Animal dispersal (Zoochory)
Zoochory was found to be more prevalent among taller shrubs and trees where seeds
are less cryptic and more accessible to animals (van Rooyen et al. 1990). However
the abundance of species utilising zoochory was found to be low throughout regional
arid environments. This is probably a result of the low abundance of dispersal agents
in the form of animals.
No dispersal technique (Atelechory)
A number of species were found to have no specific dispersal technique (van Rooyen
et al. 1990). This is probably a response to harsh desert conditions and associated
high seed mortality. Furthermore, long range dispersal may be limited in its
advantages, and dispersal in the immediate vicinity of the parent plant may be more
favourable (van Rooyen et al. 1990).
8. The role of antitelechory in arid regions
Antitelechory or atelechory refers to the phenomenon where a plant has no specific
method or specialised adaptation for seed dispersal. Possible reasons for this
occurrence are (Van Rheede Van Oudshoorn et al. 1999).
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
Phylogenetic and morphological restraints on the development of dispersal
structures;

No or few advantages of long range dispersal;

More frequent dispersal compensates for smaller dispersal range;

Secondary dispersal can achieve the same spatial distribution as primary
dispersal;

Trade-offs in resource allocation for development of long range dispersal devices;
and

Long range dispersal may be achieved even though the plant does not possess
the means of long range dispersal.
Long range dispersal has few advantages in arid environments because local
conditions are more favourable (local community is already established) and the
further away from the parent site the seed travels, the more severe environmental
variation becomes (Van Rheede Van Oudshoorn et al. 1999).
Further advantages are higher resistance to predators, increased seed bank and seed
dormancy, germination within the correct growing season and increased local
establishment and greater resilience (Van Rheede Van Oudshoorn et al. 1999).
Antitelechory also has the effect of clumping, which in turn has the advantage of
increasing intraspecific competition (Allee-effect) and in turn increasing the fitness and
resilience of the community (Van Rheede Van Oudshoorn et al. 1999).
Thus antitelechory is favoured by desert plants because it optimises growth where
conditions are already suitable instead of long range dispersal which may lead to
scattered communities which are less resilient.
9. Phase II dispersal vs. Phase I dispersal in arid environments
Phase I dispersal (Primary dispersal) describes the process of seed dispersal directly
from the parent plant to the soil surface. Most seeds are distributed in the immediate
vicinity of the parent plant, decreasing in abundance as the distance from the parent
site decreases (Van Rheede Van Oudshoorn et al. 1999).
13
Phase II dispersal (Secondary dispersal) describes the redistribution of the seed from
its primary location by secondary biotic and abiotic vectors. Seeds can be distributed
horizontally (along the soil surface) or vertically (burial) (Van Rheede Van Oudshoorn
et al. 1999).
In desert environments, wind is the primary secondary dispersal agent. Seeds are
transported by the wind across open areas and accumulate, together with organic
material and soil, under trees, shrubs and in depressions, creating fertile areas for
germination. Seeds which are dispersed in areas of higher cover are less susceptible
to being distributed by the wind than those falling in sparse or exposed areas.
Furthermore, horizontal secondary dispersal occurs through water and animal vectors.
Vertical dispersal occurs through burial by soil through animal activities, sedimentation
(through soil transported by wind and/or water) (Van Rheede Van Oudshoorn et al.
1999).
Thus Phase II dispersal is more important than Phase I dispersal in terms of
determining the patterning of desert plant communities, especially when taking
antitelechory (which is favoured by desert plants) into account, whereby seeds are
transported from the parent site by secondary dispersal.
10. The role of dispersal effectiveness and reliability in seed
dispersal success in arid environments
The dispersal of seeds has several advantages (Van Rheede Van Oudshoorn et al.
1999). Some of the ecological and evolutionary advantages of dispersal by seeds are:

Increased potential and opportunity for colonizing of potentially suitable
localities;
14

Reduced competition between parents and offspring;

Reduced competition between plants of the same generation;

Reduced chance of inbreeding;

Reduced chance of predation of offspring; and

Reduced mortality because of avoidance of source threats.
The following hypotheses (Colonization and Escape) describe the advantages and
disadvantages of dispersal further (Van Rheede Van Oudshoorn et al. 1999).
Colonization hypothesis
This hypothesis postulates that seeds are dispersed as widely as possible so that the
likelihood that suitable sites are colonized is maximized. In desert environments,
suitable sites may be few and far between, and seed dispersal in whatever form
increases the chances of seeds finding their way to suitable sites. In deserts, all seeds
are dispersed in some way, be it primarily or secondarily. Thus at least some seeds
find their way to suitable localities through adaptations to their extreme environment
(Van Rheede Van Oudshoorn et al. 1999).
Directed dispersal is a theory which is closely related to the colonization hypothesis.
It is centred around the theory that plants have certain adaptations to their environment
which allows seeds to be dispersed to suitable locations. Directed dispersal is common
in many desert plants through antitelechory, myrmecochory and zoochory (Van
Rheede Van Oudshoorn et al. 1999).
Escape hypothesis
This hypothesis compares the success of seeds which are distributed close to the
parent plant versus seeds distributed further away (Van Rheede Van Oudshoorn et al.
1999). Some of the advantages of distant distribution are:

Reduced competition between offspring and between parent plants and offspring;

Avoiding threats which may be present at the parent colony; and

Reduced chances of inbreeding.
In the previous sections, it was determined that desert plants, although favouring
antitelechory, have adapted to the threats of the parent site in order to survive threats
such as predation. Competition between siblings and parents increases fitness of the
colony through the Allee-effect, thus creating more resilient communities.
Furthermore, some level of inbreeding may benefit the community through the
persistence of suitable genes (Van Rheede Van Oudshoorn et al. 1999).
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11. References
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and fates of seeds and their implications for natural and managed systems.
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(ed.) Seeds: the ecology of regeneration in plant communities, pp. 157-182.
CABI, Wallingford.
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FENNER, M. & THOMPSON, K. 2005. The ecology of seeds, pp. 32-46. Cambridge
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FENNER, M. & THOMPSON, K. 2005. The ecology of seeds, pp. 47-75. Cambridge
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JORDANO, P. 2000. Fruit and frugivory. In: M. Fenner (ed.) Seeds: the ecology of
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LOUDA, S.M. 1989. Predation and the dynamics of seed regeneration. In: M.A. Leck,
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VAN ROOYEN, M.W., GROBBELAAR, N. & THERON, G.K. 1990. Life form and
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