over 70% of monocot families are predomi- nantly clonal. When considered on an area- covered basis, clonal species are important.
For example, the ten most widespread species in Britain are clonal and together they cover 19% of the landmass (Callaghan et al., 1992). While individual ramets may have shorter life spans, genets may survive for thousands of years and cover thousands of square metres (Cook, 1985). Clonality is com- mon in perennials but not annuals or bienni- als. Many of the worst weeds are clonal.
Clonality is a successful strategy in sta- ble but harsh conditions, such as in the Arctic (van Groenendael et al., 1996;
Peterson and Jones, 1997). Historically, clon- al families have had greater success during periods of climatic stress. Their current dis- tribution reflects their habitat preferences.
For example, in Central Europe, clonal plants tend to be in colder, wetter, nutrient poor habitats (Klimesˇ et al., 1997).
Mechanisms of clonal growth
Both herbaceous and woody plants can be clonal. For herbaceous plants, the classifica- tion of clonal structures is based on: the tis- sue of origin (stem or root), the position of the growing tip (above or below ground), the structure of storage organs (bulbs or tubers), and the length and longevity of the connec- tions (spacers) between ramets (Klimesˇ et al., 1997) (Fig. 5.4). Definitions of clonal struc- tures are given in Table 5.3. A clonal plant may possess one or many of these character- istics. Wallaby grass (Amphibromus scabri- Table 5.3.Definitions of structures common in clonal species with weed examples.
Term Definition Examples
Creeping stems
Rhizome A horizontal, underground structure Bermudagrass, Cynodon dactylon connecting ramets. It may bear roots Quackgrass, Elytrigia repens and leaves and it may be cordlike or Kentucky bluegrass, Poa pratensis
fleshy Field horsetail, Equisetum arvense
Stolon and runner An above-ground, horizontal branch Bermudagrass, Cynodon dactylon (stolon) or stem (runner) connecting Redtop grass, Agrostis stolonifera ramets or plantlets. Roots and Strawberry, Fragariaspp.
shoots develop from nodes Crabgrass, Dactylis glomerata Tuber An underground storage organ formed Yellow nutsedge, Cyperus esculentus
from the stem or root and lasting Purple nutsedge, Cyprus rotundus only one year. New tubers are Field horsetail, Equisetum arvensis formed each year from different
tissue Shoot bases
Bulb A fleshy underground storage organ Wild onion, Allium vineale composed of leaf bases and swollen Lily, Liliumspp.
scale leaves Wild garlic, Allium sativum
Bulbit A small bulb developing from an Wild onion, Allium vineale above-ground shoot either in place Wild garlic, Allium sativum of a flower (vivipory) or on a lateral
shoot
Corm A non-fleshy underground storage Buttercup, Ranunculus bulbosus organ formed from the swollen base Oat grass, Arrhenatherum etatius of the stem
Root suckers
Above-ground shoots that emerge Canada thistle, Cirsium arvense from creeping roots, tap roots or Field bindweed, Convolvulus arvensis root tubers
valvis), for example, produces rhizomes and corms in addition to flowers (Cheplick, 1995).
Clonal reproduction of woody plants long has been exploited by nursery workers.
It allows growers to bypass the stages of seed production, seed germination and seedling establishment, decreasing both the time and mortality rate inherent in these stages of growth. The mechanisms of woody clonali- ty differ somewhat from herbaceous clonal growth. New ramets develop from woody individuals either when shoots (trunk, branch and twigs) bear a root primordia, or
when roots bear a shoot bud (Fig. 5.5). The most common types of clonality in woody plants are through sprouting of roots (root suckers) and from layering of branches and stems when they come in contact with soil.
Root suckering is exhibited almost exclu- sively by angiosperms, whereas gym- nosperms are more likely to layer.
Costs and benefits of clonal growth
As with agamospermy, there are costs and benefits associated with clonal reproduc-
(a) (b)
(c)
(d)
(e)
(f)
Fig. 5.5.Examples of how clonal growth occurs in woody plants. Shown are (a) layering from drooping branches, (b) sprouting rhizomes, (c) reiteration by aerial shoots or from within roots, (d) basal rooting of coppice shoots, (e) suckering from root buds, and (f) rooting of freehanging roots (Jeník, 1994; with permission of the Institute of Botany of the Czech Academy of Sciences).
Table 5.4.Costs and benefits of vegetative reproduction.
Description Benefit
Increased growth rate New individuals (ramets) bypass the seedling stage and are capable of rapid growth that will increase survivorship and reproductive potential
Movement to better environment Creation of new ramets allows the genet to move spatially and thus invade new, possibly better environments. This buffers the genet from spatial variability
Sequestering of biological space The occupation of space and increased potential to capture resources will decrease the chance of invasion by other species
Lower mortality New ramets have a lower mortality rate than seedlings Invasion potential Movement of large genets increases potential to invade and
displace competitors. Ramets that remain attached can draw resources from a wide patch supporting the invasion front Increased resource acquisition Spreading plants have a high potential to invade nutrient rich
environments. This may be of benefit in spatially or temporally heterogeneous habitats
Buffering of temporal variability Storage organs increase survival during stressful periods and changing environments
Risk aversion to the genet The risk to a genet is spread among the ramets
No ‘cost of sex’ Creation of ramets does not incur the costs associated with sexual reproduction.
Persistence Some clones are extremely long lived Costs
Loss of genetic recombination Lack of genetic recombination through sexual reproduction means the benefits from novel genotypes are lost Vulnerable to disturbance Spatial integrity of clones can make them more vulnerable to
large scale disturbances such as floods, fire and frost heave Mortality of individual ramets Nutrients are shared among ramets, therefore survivorship of
an individual ramet may be decreased in favourable habitat Transmission of disease A disease may be able to spread throughout the portions of a
genet that remain connected
Decreased sexual reproduction The creation of new clones decreases the allocation of resources to sexual reproduction
tion (Table 5.4). One of the main benefits to clonal growth is that it allows the individual to bypass the juvenile stage of growth nec- essary for individuals that reproduce by seeds. The seedling stage is often where the highest mortality occurs for plants. Thus, new clonal individuals have a higher growth rate, lower mortality and can take up ‘bio- logical space’ that might otherwise become occupied by competitors. A second general benefit to clonal growth is that new ramets can move into other habitats allowing the genet to invade new space or enter into a bet- ter environment while maintaining a pres- ence in the ‘old’ habitat. The main cost to
clonal reproduction is that there is no new genetic recombination, which reduces an individual’s ability to adapt to new environ- ments. In addition, if ramets remain attached, it more likely that the entire genet may be killed by disturbance, disease or herbicides.
Ecological aspects: the phalanx vs. guerrilla strategies
Two general types of clonal growth are guer- rilla and phalanx (Lovett Doust, 1981) (Fig.
5.3). Guerrilla-type growth forms loosely
packed, often linear patches. Guerrilla growth is a foraging strategy that maximizes movement of a species into new habitats.
Such species are likely to invade new habi- tats and vacate other ones over the course of a season (Hutchings and Mogie, 1990). For example, at your local golf course or in your own lawn, redtop grass (Agrostis stolonifera) will spread by sending ground level stems (stolons) into an area that is occupied by other plants. Once there, the stolons produce new shoots that, in turn, produce more stolons for further colonization. At first, only a few stems of redtop grass appear as if by stealth, but eventually the habitat area is taken over as more stolons and shoots are produced.
Phalanx-type growth is the result of slow growing, branched clones which form dense patches. Phalanx growth exploits space by maximizing the occupation of a site and deterring invasion from other species.
Such species form dense monocultures with individuals of approximately equal size.
Patches have little movement over the course of a season (Hutchings and Mogie, 1990). Often, peripheral (younger) ramets are dependent on interior (older) ramets for resources while interior ramets flower and set fruit (Waller, 1988). Quackgrass spreads in a phalanx pattern.
Ecological aspects of clonality
Species persistence
Clonal species often have the ability to per- sist at the edges of their distribution because they are not dependent on sexual reproduc- tion. This pattern is thought to occur because seed production requires higher temperatures than clonal growth, and because fewer appropriate pollinators are found in stressful habitats (Abrahamson, 1980). Japanese knotweed (Fallopia japonica), for example, is distributed widely in north- ern Europe and North America, and yet seed production has never been observed in places like Britain or the USA (Brock et al., 1995). Therefore, preventing seed produc- tion may not be enough to eradicate a weed
because it may survive and spread through clonal growth.
Clonal species may form remnant pop- ulations when conditions become unsuit- able for seed production. Arctic dwarf birch (Betula glandulosa), for example, forms clonal stands at the northern edge of its dis- tribution in sites where the species was once widely distributed (Hermanutz et al., 1989).
Even populations that appear entirely clon- al may revert to sexual seed production when conditions improve and isolated clon- al stands can act as seed sources for recolo- nization when conditions improve. Whorled wood aster (Aster acuminatus) remains in small clonal populations under forest canopy, but produces seed when a canopy gap opens (Hughes et al., 1988).
Woody plants that are clonal benefit from better physical stability and protection from most risks (e.g. fire, wind and herbi- vores) (Peterson and Jones, 1997). Peripheral ramets may protect inner ones by buffering them from damage. In addition, if a distur- bance removes the above-ground biomass, then sprouts from an existing rootstock will provide a ‘sprout bank’ (Ohkubo et al., 1996). Species with root sprouts have a bet- ter chance of establishing than species reliant on seeds.
Physical and physiological integration of ramets
Ramets may remain physically attached through connectors (e.g. stolons or rhi- zomes) or they may fragment into inde- pendent parts. The degree of ramet integra- tion can vary from highly integrated compact patches to fragmented genets form- ing only loose associations. Separation of ramets occurs naturally when specialized tissues (called ‘plantlets’) are abscised or when parts of the plant are separated through decay of the tissue that connects them. Separation also occurs through frag- mentation caused by disturbance. In agri- cultural systems, for example, tillage will fragment quackgrass rhizomes.
The longevity of connections between ramets determines the success of reproduc- tion, exploitation and persistence of the genet (van Groenendael et al., 1996)
(Table 5.5). When ramets remain integrated, they continue to share resources. For exam- ple, older established ramets may support younger ones, during early establishment, by sending resources to them. Integration ben- efits the entire genet because it increases the longevity of the clone and prolongs the occupation of the site.
The benefits of remaining integrated increase in heterogeneous environments (Wijesinghe and Handel, 1994). Genets with integrated ramets effectively live in two or more places at once, because each shoot sec- tion is anchored in a different microhabitat (Alpert and Stuefer, 1997). Having multiple rooting sites reduces the risk to the intact genet, because resources can be shared between ramets and, therefore, ramets in poorer sites are supported by ones in better sites. Sharing resources may result in less biomass accumulation of individual ramets, but total biomass of the genet will increase.
Genets that remain integrated are typi- cal of nutrient poor environments (van Groenendael et al., 1996). Integrated clones tend to interact more intra-clonally than with other species. Ramets of woody species remain integrated for long periods of time and this results in woody clones being long lived and spreading extensively. In fact, the largest plant is argued to be a clonal patch of trembling aspen (Populus tremuloides) found in Utah, USA. A single male clone contains approximately 47,000 trees (ram- ets) and covers 43 ha (Grant, 1993).
Integrated ramets may ‘specialize’ or create a ‘division of labour’ (Alpert and Stuefer, 1997). Resources within a genet can be re-allocated quickly because of pheno-
typic plasticity. This allows genets to exploit nutrient-rich sites by rapidly increasing ramet density in a localized microhabitat (Hutchings and Mogie, 1990) or modifying root and shoot structure to optimize resource use within their environment (de Kroon and Hutchings, 1995; van Groenendael et al., 1996).
Genets are more likely to fragment in nutrient rich environments and this allows them to colonize and monopolize large tracts of land. Examples of fragmenting species include bracken fern, (Pteridium aquil- inum), Kentucky bluegrass (Poa pratensis) quackgrass and white clover (Trifolium repens); these all form larger patches in open habitats with adequate moisture (Jonsdottir and Watson, 1997).
In heterogeneous environments with both nutrient-rich and nutrient-poor micro- habitats, the genets may fragment but the fragments are much smaller in size because the microhabitat is smaller than in consis- tently nutrient-rich environments. Tall gold- enrod (Solidago altissima), Canada golden- rod (Solidago canadensis), eastern lined aster (Aster lanceolatus) and New York aster (Aster novi-belgii) are examples of species that produce small fragments and form small patches in moderately disturbed, shaded environments. While fragmented genets allow for greater colonization, the trade-off is that such species are less likely to spread to new, favourable habitats because they concentrate their resources in one place (Hutchings and Mogie, 1990). The lower colonization ability is ironic because frag- mented genets often must be better interspe- cific competitors than integrated genets.
Table 5.5.Costs and benefits associated with maintaining physiological integration among ramets (based on text in Jonsdottir and Watson, 1997).
Benefits Costs
Support new ramets Cost of maintaining rhizomes, stolons and other Buffering environmental heterogeneity and stress connecting tissue
Resources sharing, division of labour among Higher risk of genet mortality and extinction
ramets Resource dilution
Regulation of competition among ramets through the control of ramet production
Recycling of resources
This occurs because when ramets fragment, the genet will encounter other species more often than its own ramets.
Sexual Reproduction in Asexually Reproducing Species
Clonal reproduction rarely occurs to the total exclusion of sexual reproduction, although there are examples of this, such as Japanese knotweed. Clonal growth may occur at the expense of seed production (creeping buttercup, Ranunculus repens, and Canada goldenrod). A trade-off occurs between these two methods of reproduction because only a finite amount of resources is available to allocate to reproduction (Abrahamson, 1980). The allocation of resources to sexual vs. asexual reproduction will change over the life of the genet.
Sexually and asexually produced offspring will have different genetic and ecological characteristics (Table 5.6). For example, off- spring produced through sexual reproduc- tion will differ genetically from their parents and, have the ability to disperse, but suffer a high mortality rate in the seedling stage.
Offspring produced asexually will develop immediately and have a low mortality rate, but have less dispersal potential.
In some cases there can be individual plants reproducing sexually and asexually alongside conspecific (same species) indi- viduals that are reproducing only one way.
For example, individuals of the introduced
wild garlic (Allium vineale) produce a stalk which has either only sexually reproducing flowers, only asexual bulbits (bulbs pro- duced on shoots where the flowers normal- ly are located) or both, in addition to pro- ducing two types of bulbs at their base (Ronsheim and Bever, 2000). The relative allocation of resources to bulbs, bulbits and flowers is under strong genetic control, as genotypes do not vary allocation patterns in response to nutrient addition.
Seedling recruitment may occur only at some times during the life of a clonal species. For example, seedling recruitment of Canada goldenrod occurred only in the first 3–6 years after colonization, and suc- cessful genets were established mainly in the first year (Hartnett and Bazzaz, 1983).
This pattern of recruitment is called ‘initial seedling recruitment’ (ISR). It results in a population with an even age structure because new individuals are recruited at approximately the same time. ISR genets may be long-lived because once established they can be virtually immortal unless a dis- turbance kills the entire genet.
White clover is an example of the oppo- site type of recruitment pattern where there is continual recruitment of new genets into the population via seed production (Barrett and Silander, 1992). This type of recruit- ment is called repeated seedling recruit- ment (RSR). Such populations have an uneven age structure. Following a distur- bance, some genets die making room for new recruitment of genets. RSR genets have Table 5.6.Expected differences between asexually produced and sexually produced offspring (adapted from Williams, 1975, and Abrahamson, 1980).
Asexual offspring Sexual offspring
Mitotically standardized Meiotically diversified
Produced continuously Produced seasonally
Develop close to parent Can be widely dispersed
Develop immediately Can be dormant
Develop more directly to reproductive stage Develop more slowly from seedling stage to reproductive stage
Environment and optimum genotype predictable Environment and optimum genotype unpredictable from those of parent since they are genetically because genetic recombination has occurred the same as parent
Low mortality rate High mortality rate – especially during seedling stage.
shorter life spans because they are continu- ally being replaced (Eriksson, 1993). Of course, many species are likely to be located along a continuum between ISR and RSR.
Table 5.7 summarizes the life history traits associated with ISR and RSR patterns.
Case history: Plantain pussytoes – a species with agamospermy, clonal reproduction and
sexual reproduction
Plantain pussytoes (Antennaria parlinii) is a herbaceous perennial in eastern North America that reproduces via both sexual and agamospermic seeds and clonally through stolons. Asexual populations tend to be more prevalent in disturbed early suc-
cessional sites (fields and pastures), where- as sexually reproducing populations tend to be in less disturbed sites (open woods and old fields).
Michaels and Bazzaz (1986) compared demographic characteristics and resource allocation of sexual and asexual popula- tions of plantain pussytoes (Table 5.8).
Asexual individuals had higher fecundity rates because they produced more, but smaller seeds; however, seedling survivor- ship was lower. Clonal growth was high in asexual populations with more ramets being produced; however, stolon length and sur- vivorship were decreased. Sexual popula- tions produced long-lived wandering stolons that allowed the genet to persist in spatially and temporally unpredictable envi- Table 5.7.Expected life-history trends for clonal plants, in relation to their seedling recruitment patterns:
initial seedling recruitment (ISR) and repeated seedling recruitment (RSR) (from Eriksson, 1989).
ISR RSR
Key features in recruitment phase Dispersal Competitive ability
Genetic diversity in local population Low High
Prospects for evolution of locally adapted population Low High Genetic age-structure in local population Even-aged Variable
Genetic life span Long Variable
Spatial context for including genetic population dynamics Large scale Small scale
Table 5.8.Comparison of seed production, seedling establishment and clonal growth in populations of sexual (female plants only) and asexual (agamospermic) pussytoes (Antennaria parlinii) (from data in Michaels and Bazzaz, 1986, 1989).
Sexual Agamospermic
Stage Factor populations populations
Seed production Seed number/inflorescence 252 seeds 389 seeds
Seed massa approx. 77 µg approx. 68 µg
Inflorescences/plant Fewer More
Seedling survivorship Midsummer 47% 22%
End of growing season 7% 4%
Ramet demography Ramet production (no. ramets/ 2.3 2.8
genet)
Ramet survivorship 85% 68%
Stolon length (cm/genet) 8 cm 5 cm
Biomass Total biomass More Less
Allocation to reproduction Less More
Response to increase in Little change in More towards
resources biomass allocation reproduction
aEstimated from graphed data.