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1.  Plant traits and ecosystem effects of clonality: a new research agenda 
Annals of Botany  2014;114(2):369-376.
Background
Clonal plants spread laterally by spacers between their ramets (shoot–root units); these spacers can transport and store resources. While much is known about how clonality promotes plant fitness, we know little about how different clonal plants influence ecosystem functions related to carbon, nutrient and water cycling.
Approach
The response–effect trait framework is used to formulate hypotheses about the impact of clonality on ecosystems. Central to this framework is the degree of correspondence between interspecific variation in clonal ‘response traits’ that promote plant fitness and interspecific variation in ‘effect traits’, which define a plant's potential effect on ecosystem functions. The main example presented to illustrate this concept concerns clonal traits of vascular plant species that determine their lateral extension patterns. In combination with the different degrees of decomposability of litter derived from their spacers, leaves, roots and stems, these clonal traits should determine associated spatial and temporal patterns in soil organic matter accumulation, nutrient availability and water retention.
Conclusions
This review gives some concrete pointers as to how to implement this new research agenda through a combination of (1) standardized screening of predominant species in ecosystems for clonal response traits and for effect traits related to carbon, nutrient and water cycling; (2) analysing the overlap between variation in these response traits and effect traits across species; (3) linking spatial and temporal patterns of clonal species in the field to those for soil properties related to carbon, nutrient and water stocks and dynamics; and (4) studying the effects of biotic interactions and feedbacks between resource heterogeneity and clonality. Linking these to environmental changes may help us to better understand and predict the role of clonal plants in modulating impacts of climate change and human activities on ecosystem functions.
doi:10.1093/aob/mcu113
PMCID: PMC4111380  PMID: 24948670
Carbon cycling; clonal plant ecology; effect traits; functional traits; litter decomposition; nutrient; ramet; response–effect trait framework; spacer; spatial heterogeneity; water retention
2.  Trampling, defoliation and physiological integration affect growth, morphological and mechanical properties of a root-suckering clonal tree 
Annals of Botany  2012;109(5):1001-1008.
Background and Aims
Grazing is a complex process involving the simultaneous occurrence of both trampling and defoliation. Clonal plants are a common feature of heavily grazed ecosystems where large herbivores inflict the simultaneous pressures of trampling and defoliation on the vegetation. We test the hypothesis that physiological integration (resource sharing between interconnected ramets) may help plants to deal with the interactive effects of trampling and defoliation.
Methods
In a field study, small and large ramets of the root-suckering clonal tree Populus simonii were subjected to two levels of trampling and defoliation, while connected or disconnected to other ramets. Plant responses were quantified via survival, growth, morphological and stem mechanical traits.
Key Results
Disconnection and trampling increased mortality, especially in small ramets. Trampling increased stem length, basal diameter, fibrous root mass, stem stiffness and resistance to deflection in connected ramets, but decreased them in disconnected ones. Trampling decreased vertical height more in disconnected than in connected ramets, and reduced stem mass in disconnected ramets but not in connected ramets. Defoliation reduced basal diameter, leaf mass, stem mass and leaf area ratio, but did not interact with trampling or disconnection.
Conclusions
Although clonal integration did not influence defoliation response, it did alleviate the effects of trampling. We suggest that by facilitating resource transport between ramets, clonal integration compensates for trampling-induced damage to fine roots.
doi:10.1093/aob/mcs006
PMCID: PMC3310488  PMID: 22314757
Biomechanics; clonal integration; defoliation; drylands; grazing; Populus simonii; resource sharing; root connections; root severing; trampling
3.  Partial mechanical stimulation facilitates the growth of the rhizomatous plant Leymus secalinus: modulation by clonal integration 
Annals of Botany  2011;107(4):693-697.
Background and Aims
Mechanical stimulation (MS) often induces plants to undergo thigmomorphogenesis and to synthesize an array of signalling substances. In clonal plants, connected ramets often share resources and hormones. However, little is known about whether and how clonal integration influences the ability of clonal plants to withstand MS. We hypothesized that the effects of MS may be modulated by clonal integration.
Methods
We conducted an experiment in which ramet pairs of Leymus secalinus were subjected to three treatments: (1) connected ramet pairs under a homogeneous condition [i.e. the proximal (relatively old) and distal (relatively young) ramets were not mechanically stressed]; (2) connected ramet pairs under a heterogeneous condition (i.e. the proximal ramet was mechanically stressed but the distal ramet was not); and (3) disconnected ramet pairs under the same condition as in treatment 2. At the end of the experiment, we harvested all plants and determined their biomass and allocation.
Key Results
Clonal integration had no significant influence on measured traits of distal L. secalinus ramets without MS. However, under MS, plants with distal ramets that were connected to a mother ramet produced more total plant biomass, below-ground biomass, ramets and total rhizome length than those that were not connected. Partial MS exerted local effects on stimulated ramets and remote effects on connected unstimulated ramets. Partial MS increased total biomass, root/shoot ratio, number of ramets and total rhizome length of stimulated proximal ramets, and increased total biomass, root weight ratio, number of ramets and total rhizome length of connected unstimulated ramets due to clonal integration.
Conclusions
These findings suggest that thigmomorphogenesis may protect plants from the stresses caused by high winds or trampling and that thigmomorphogenesis can be strongly modulated by the degree of clonal integration.
doi:10.1093/aob/mcr012
PMCID: PMC3064544  PMID: 21303785
Clonal plants; heterogeneous habitats; resource translocation; thigmomorphogenesis
4.  Arbuscular mycorrhizal fungi reduce effects of physiological integration in Trifolium repens 
Annals of Botany  2009;104(2):335-344.
Background and Aims
One of the special properties of clonal plants is the capacity for physiological integration, which can increase plant performance through mechanisms such as resource sharing and co-ordinated phenotypic plasticity when plants grow in microsites with contrasting resource availabilities. However, many clonal plants are colonized by arbuscular mycorrhizal fungi (AMF). Since AMF are likely to reduce contrasts in effective resource levels, they could also reduce these effects of clonal integration on plasticity and performance in heterogeneous environments.
Methods
To test this hypothesis, pairs of connected and disconnected ramets of the stoloniferous herb Trifolium repens were grown. One ramet in a pair was given high light and low nutrients while the other ramet was given high nutrients and low light. The pairs were inoculated with zero, one or five species of AMF.
Key Results
Pairs of ramets grown without AMF developed division of labour and benefited from resource sharing, as indicated by effects of connection on allocation to roots, accumulation of mass, and ramet production. Inoculation with five species of AMF significantly reduced these effects of connection, both by inhibiting them in ramets given high nutrients and inducing them in ramets given high light. Inoculation with one species of AMF also reduced some effects of connection, but generally to a lesser degree.
Conclusions
The results show that AMF can significantly modify the effects of clonal integration on the plasticity and performance of clonal plants in heterogeneous environments. In particular, AMF may partly replace the effects and benefits of clonal integration in low-nutrient habitats, possibly more so where species richness of AMF is high. This provides the first test of interaction between colonization by AMF and physiological integration in a clonal plant, and a new example of how biotic and abiotic factors could interact to determine the ecological importance of clonal growth.
doi:10.1093/aob/mcp130
PMCID: PMC2710896  PMID: 19493856
Arbuscular mycorrhizal fungi; biomass allocation; clonal plant; division of labour; environmental heterogeneity; light availability; nutrients; white clover
5.  Germination of Dimorphic Seeds of the Desert Annual Halophyte Suaeda aralocaspica (Chenopodiaceae), a C4 Plant without Kranz Anatomy 
Annals of Botany  2008;102(5):757-769.
Background and Aims
Suaeda aralocaspica is a C4 summer annual halophyte without Kranz anatomy that is restricted to the deserts of central Asia. It produces two distinct types of seeds that differ in colour, shape and size. The primary aims of the present study were to compare the dormancy and germination characteristics of dimorphic seeds of S. aralocaspica and to develop a conceptual model of their dynamics.
Methods
Temperatures simulating those in the natural habitat of S. aralocaspica were used to test for primary dormancy and germination behaviour of fresh brown and black seeds. The effects of cold stratification, gibberellic acid, seed coat scarification, seed coat removal and dry storage on dormancy breaking were tested in black seeds. Germination percentage and recovery responses of brown seeds, non-treated black seeds and 8-week cold-stratified black seeds to salt stress were tested.
Key Results
Brown seeds were non-dormant, whereas black seeds had non-deep Type 2 physiological dormancy (PD). Germination percentage and rate of germination of brown seeds and of variously pretreated black seeds were significantly higher than those of non-pretreated black seeds. Exposure of seeds to various salinities had significant effects on germination, germination recovery and induction into secondary dormancy. A conceptual model is presented that ties these results together and puts them into an ecological context.
Conclusions
The two seed morphs of S. aralocaspica exhibit distinct differences in dormancy and germination characteristics. Suaeda aralocaspica is the first cold desert halophyte for which non-deep Type 2 PD has been documented.
doi:10.1093/aob/mcn158
PMCID: PMC2712381  PMID: 18772148
Borszczowia; cold desert halophyte; physiological seed dormancy; seed germination; Suaeda
6.  Adaptation of Rhizome Connections in Drylands: Increasing Tolerance of Clones to Wind Erosion 
Annals of Botany  2008;102(4):571-577.
Background and Aims
Wind erosion is a severe stress for plants in drylands, but the mechanisms by which plants withstand erosion remain largely unknown. Here, the hypothesis is tested that maintaining rhizome connections helps plants to tolerate erosion.
Methods
Five transects were established across an inland dune in Inner Mongolia, China, and measurements were made of leaf number, biomass per ramet and rhizome depth of Psammochloa villosa in 45 plots. In 40 × 40 cm plots of P. villosa on another dune, the top 15 or 30 cm of sand was removed for 1·5 or 3 months to simulate short- and long-term moderate and severe erosion, respectively, with untreated plots as controls, and the rhizomes at the edges of half of the plots were severed to mimic loss of rhizome connections.
Key Results
Leaf number and biomass per ramet showed quadric relationships with rhizome depth; when rhizomes were exposed to the air, the associated ramets either died or became very weak. Ramet number, leaf number and biomass per plot decreased with increasing erosion severity. Rhizome connections did not affect these traits under control or short-term erosion, but increased them under long-term erosion.
Conclusions
Rhizome connections alleviated the negative effects of erosion on P. villosa, very likely because the erosion-stressed ramets received water and/or photosynthates translocated from those connected ramets that were not subject to erosion. This study provides the first evidence that maintaining rhizome connections helps plants to tolerate erosion in drylands.
doi:10.1093/aob/mcn119
PMCID: PMC2701773  PMID: 18621966
Clonal integration; inland-dune grass; Psammochloa villosa; resource sharing; rhizome severing; wind erosion
7.  Clonal Integration Affects Growth, Photosynthetic Efficiency and Biomass Allocation, but not the Competitive Ability, of the Alien Invasive Alternanthera philoxeroides under Severe Stress 
Annals of Botany  2008;101(5):671-678.
Background and Aims
Many notorious alien invasive plants are clonal, but little is known about some roles and aspects of clonal integration. Here, the hypothesis is tested that clonal integration affects growth, photosynthetic efficiency, biomass allocation and competitive ability of the exotic invasive weed Alternanthera philoxeroides (Amaranthaceae).
Methods
The apical parts of Alternanthera were grown either with or without the lawn grass Schedonorus phoenix (tall fescue) and their stolon connections to the basal parts grown without competitors were either severed or left intact.
Key Results
Competition greatly reduced the maximum quantum yield of photosystem II (Fv/Fm) and growth (biomass, number of ramets and leaves, total stolon length and total leaf area) of the apical Alternanthera, but not the biomass of S. phoenix. Stolon connections significantly increased Fv/Fm and growth of Alternanthera. However, such effects on growth were smaller with than without competition and stolon connections did not alter the relative neighbour effect of Alternanthera. Stolon connections increased Alternanthera's biomass allocation to roots without competition, but decreased it with competition.
Conclusions
Clonal integration contributed little to Alternanthera's competitive ability, but was very important for Alternanthera to explore open space. The results suggest that the invasiveness of Alternanthera may be closely related to clonal integration.
doi:10.1093/aob/mcn005
PMCID: PMC2710179  PMID: 18250108
Alien species; alligator weed; Alternanthera philoxeroides; chlorophyll fluorescence; clonal invasive plants; competition; physiological integration; Schedonorus phoenix
8.  Possible Role of Pectin-containing Mucilage and Dew in Repairing Embryo DNA of Seeds Adapted to Desert Conditions 
Annals of Botany  2007;101(2):277-283.
Background and Aims
Repair of damage to DNA of seed embryos sustained during long periods of quiescence under dry desert conditions is important for subsequent germination. The possibility that repair of embryo DNA can be facilitated by small amounts of water derived from dew temporarily captured at night by pectinaceous surface pellicles was tested. These pellicles are secreted during early seed development and form mucilage when hydrated.
Methods
Seeds of Artemisia sphaerocephala and Artemisia ordosica were collected from a sandy desert. Their embryos were damaged by gamma radiation to induce a standard level of DNA damage. The treated seeds were then exposed to nocturnal dew deposition on the surface of soil in the Negev desert highlands. The pellicles were removed from some seeds and left intact on others to test the ability of mucilage to support repair of the damaged DNA when night-time humidity and temperature favoured dew formation. Repair was assessed from fragmentation patterns of extracted DNA on agarose gels.
Key Results
For A. sphaerocephala, which has thick seed pellicles, DNA repair occurred in seeds with intact pellicles after 50 min of cumulative night dew formation, but not in seeds from which the pellicles had been removed. For A. ordosica, which has thin seed pellicles, DNA repair took at least 510 min of cumulative night dewing to achieve partial recovery of DNA integrity. The mucilage has the ability to rehydrate after daytime dehydration.
Conclusions
The ability of seeds to develop a mucilaginous layer when wetted by night-time dew, and to repair their DNA under these conditions, appear to be mechanisms that help maintain seed viability under harsh desert conditions.
doi:10.1093/aob/mcm089
PMCID: PMC2711012  PMID: 17495979
Adaptation strategy; Artemisia; desert dew; DNA repair; pectin; pellicle; seed survival
9.  Wind-Dragged Corolla Enhances Self-Pollination: A New Mechanism of Delayed Self-Pollination 
Annals of Botany  2007;100(6):1155-1164.
Background and Aims
Delayed self-pollination is a mechanism that allows animal-pollinated plants to outcross while ensuring seed production in the absence of pollinators. This study aims to explore a new mechanism of delayed self-pollination facilitated by wind-driven corolla abscission in Incarvillea sinensis var. sinensis.
Methods
Floral morphology and development, and the process of delayed self-pollination were surveyed. Experiments dealing with pollinator and wind exclusion, pollination manipulations, and pollinator observations were conducted in the field.
Key Results
Delayed self-pollination occurs when the abscising corolla driven by wind drags the adherent epipetalous stamens, thus leading to contact of anthers with stigma in late anthesis. There is no dichogamy and self-incompatibility in this species. The significantly higher proportion of abscised corolla under natural conditions as compared with that in wind-excluding tents indicates the importance of wind in corolla abscission. When pollinators were excluded, corolla abscission significantly increased the number of pollen grains deposited on the stigma and, as a result, the fruit and seed set. Only half of the flowers in plots were visited by pollinators, and the fruit set of emasculated flowers was significantly lower than that of untreated flowers in open pollination. This species has a sensitive stigma, and its two open stigmatic lobes closed soon after being touched by a pollinator, but always reopened if no or only little pollen was deposited.
Conclusions
This delayed self-pollination, which involved the movement of floral parts, the active participation of the wind and sensitive stigma, is quite different from that reported previously. This mechanism provides reproductive assurance for this species. The sensitive stigma contributes to ensuring seed production and reducing the interference of selfing with outcrossing. The pollination pattern, which combines actions by bees with indirect participation by wind, is also a new addition to ambophily.
doi:10.1093/aob/mcm209
PMCID: PMC2759251  PMID: 17881336
Ambophily; anther movement; Bignoniaceae; corolla abscission; delayed self-pollination; Incarvillea sinensis var. sinensis; reproductive assurance; stigma closure
10.  Large Clones on Cliff Faces: Expanding by Rhizomes through Crevices 
Annals of Botany  2007;100(1):51-54.
Background and Aims
Large clones of rhizomatous plants are found in many habitats, but little is known about whether such clones also occur on cliff faces where environmental conditions are extremely harsh and heterogeneous.
Methods
Using molecular (intersimple sequence repeat, ISSR) markers, the genotypic composition of a cliff-face population of Oxyria sinensis in Sichuan, China, was investigated.
Key Results
The 98 O. sinensis ramets sampled belonged to 12 different genotypes (clones). The three most frequent clones were represented with 45, 22 and 12 ramets, respectively; the remaining nine were represented with only one to five ramets. The three largest clones spanned at least 2·7 m in the vertical direction and 4·6–6·9 m in the horizontal direction on the cliff face.
Conclusions
On the cliff face, large clones of O. sinensis are formed by rhizomes growing along the crevices. Expansion by rhizomes may help O. sinensis to exploit the patchy resources and support establishment and growth of new ramets. Moreover, rooted ramets connected by rhizomes may effectively reduce the susceptibility of O. sinensis to rock fall and erosion and thus greatly improve the chances for long-term survival. The multi-clone structure indicates that sexual reproduction is also important for the long-term persistence of O. sinensis populations on cliffs.
doi:10.1093/aob/mcm086
PMCID: PMC2735296  PMID: 17525100
Cliff ecology; clonal diversity; clonal growth; genet distribution; Oxyria sinensis; rhizomatous plants

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