Cleistogamy as a bet‐hedging strategy in Oxalis acetosella, a perennial herb

1 Phenology and reproduction were studied in three populations of the cleistogamous herb Oxalis acetosella during three growing seasons, in order to see how the balance between chasmogamous (CH) and cleistogamous (CL) reproduction varies with temporal and spatial environmental variation and with plant size. The numbers of CH and CL flower buds, flowers, immature capsules and mature capsules were counted per ramet, ramet sizes were estimated, and mature capsules were collected for seed counts.
2 Both CH and CL flower numbers were positively correlated with ramet size expressed as leaf number, but the correlation was much stronger in the CL phase. CL flower production also varied significantly between years and sites. Thus, CL production in O. acetosella was not independent of resources and climatic variation.
3 When the effects of year and site were taken into account, the probability of an individual flower developing into a mature fruit was not higher in the CL phase than in the CH phase.
4 CL production was affected by fertilization success in the CH phase. Ramets with one or more CH flowers left unfertilized generally produced more CL buds than ramets with all their CH flowers fertilized. The former group also tended to have more seeds per CL capsule.
5 Since reproductive success in the two phases varies in different temporal and spatial patterns, cleistogamy in O. acetosella is considered to be a bet‐hedging strategy optimizing reproductive output in fluctuating environments.
6 The findings of this study are in conflict with the general view on cleistogamy as a fail‐safe mechanism for back‐up seed production, unaffected by variations in resource supply and environmental conditions.     

Population dynamics in Oxalis acetosella: the significance of sexual reproduction in a clonal, cleistogamous forest herb

I studied demography in three populations of the clonal, cleistogamous herb Oxalis acetosella during three growing seasons, to assess the impact of seedling recruitment relative to ramet recruitment on its population dynamics. I followed each plant in permanent plots, and stage-classified it according to origin (sexually or vegetatively derived) and reproductive status. I calculated between-year transition probabilities, and sexual and vegetative fecundities, and used them in projection matrix analyses to simulate the development of populations and obtain the elasticity of each life-history event.
In general, non-flowering adults was the most numerous stage class and flowering new ramets the rarest, whereas the proportions of the other stage classes varied among populations and years. The negative correlation between plant density and survival was not very strong, and mortality seemed to be largely density-independent. Simulated population growth rates (λ) indicated that one of the populations is declining and the other two are growing, although slowly. The highest elasticities were usually those of stasis in adult plants, whereas elasticities of other matrix entries were low and highly variable. λ was positively correlated with the elasticities of seedling production and survival but negatively correlated with the elasticity of adult survival, indicating that seedling recruitment is more favourable for population growth than is adult stasis. There were no correlations between λ on the one hand and the elasticities of ramet production and survival on the other.
The results suggest that recruitment from seedlings is important for the growth and long-term maintenance of O. acetosella populations, as a complement to the rather low vegetative propagation. In this context cleistogamy is an adaptive strategy, maximizing total seed output.     

Offspring Performance in Oxalis acetosella, a Cleistogamous Perennial Herb

Abstract: Seed weight, seed germination, seedling survival, and juvenile/adult fitness in chasmogamously (CH) and cleistogamously (CL) derived offspring of Oxalis acetosella were compared during three growing seasons, to test hypotheses of fitness differences between the offspring types accounting for the maintenance of cleistogamy. In plots at three field sites, CH and CL seeds originating from all sites were sown to compare the performance of offspring growing in their habitat of origin and offspring growing in new habitats. Seeds were also sown in pots in a common garden, to test for effects of sibling competition. CL seeds had significantly lower germination than CH seeds in the field, possibly because of lower mean seed weight due to later flowering. Since the outcrossing rate in the CH flowers of O. acetosella is not known, it is uncertain whether the lower CL germination is a consequence of inbreeding depression. CH seeds had higher germination if sown at their home sites than at new sites, while for CL seeds this made no difference; this contradicts the local adaptation hypothesis for cleistogamy. No other fitness differences were found between the offspring types, and the findings did not support the sibling competition or local adaptation hypotheses. We suggest that the maintenance of the dimorphic reproductive system in O. acetosella is not explained by offspring characteristics, but rather by the two flowering phases complementing each other in maximizing annual seed production in the face of environmental variability. It is, therefore, important to include temporal and spatial variation in studies of reproductive strategies.     

Genetic effects of habitat fragmentation in Viola pubescens (Violaceae), a perennial herb with chasmogamous and cleistogamous flowers

The reproductive biology of a plant species is important in the response of populations to habitat fragmentation, especially if plant-pollinator interactions are disrupted. The genetic effects of forest fragmentation were examined in the common understorey herb Viola pubescens, a species that produces self-pollinated cleistogamous (CL) flowers and potentially outcrossing chasmogamous (CH) flowers. Using allozymes, we measured genetic variation in different sized populations. These were located in woodlots of various sizes (0.5-40.5 ha) and distances from one another (0.3-46 km) within the agricultural landscape of central Ohio in the Midwestern United States. Changes in forest cover of each woodlot within the past 180 years were determined from historical sources and aerial photographs. Woodlot and population sizes were significantly and positively correlated with measures of genetic variation (A, P, HO and HE), with variation highest in populations in the largest woodlot population and lowest in the smallest woodlot population. Most large woodlots resulted from fluctuations in forest cover over the past 60 years, while smaller fragments remained the same size. Overall, populations in Crawford County were genetically differentiated from one another (theta = 0.34), but there was no relationship between genetic and geographical distance. Preliminary evidence for a single year indicated a high rate of outcrossing in most populations. Despite the CH/CL reproductive advantage and apparent outcrossing, populations of V. pubescens in small woodlots remain susceptible to potentially detrimental effects of fragmentation such as genetic drift and reduced levels of genetic variation.     

Epidermal focussing and effects on light utilization in Oxalis acetosella

lmage analysis was used to quantify the lateral heterogeneity of the radiation field within the palisade of Oxialis acetosella L. leaves. Oxalis acetosella epidermal cells focus light up to four times incident irradiance, resulting in regions of high and low internal fluenec rate within the palisade. Chlorophyll fluorescence from leaves irradiated with directional light was found to originate primarily from palisade cell chloroplasts located within focal zones. When the internal radiation field was made more homogeneous by using diffuse light or by coating the leaf with a layer of mineral oil to eliminate epidermal focussing, the characteristics of the chlorophyll fluorescence signal were altered: non-photochemical quenching (qN) increased, while relaxation of qN was slowed. This indicates that upper palisade chloroplasts may fine-tune their light utilization to the intra leaf light microenvironment.     

Seasonal dynamics in a yeast population on the Oxalis acetosella L. leaves

Analysis of an epiphytic yeast population on the leaves of the evergreen common wood sorrel Oxalis acetosella L. throughout a year showed that the density and the species composition of this population underwent regular seasonal changes. There were almost no yeasts on the young spring leaves. However, the yeast population on the mature leaves tended to increase in the autumn, reaching a maximum after the formation of continuous snow cover. Then the yeast population on the leaves tended to decrease, reaching a minimum in the spring. The species diversity of the yeasts was maximum in the autumn. The population of the epiphytic yeast species Cystofilobasidium capitatum, Rhodotorula fujisanensis, Leucosporium scottii, and Cryptococcus flavus peaked in the autumn. On the other hand, the population of the widespread epiphytic species Cryptococcus laurentii on the wood sorrel leaves peaked in January. The relative abundance of the red-pigmented phytobionts Rhodotorula glutinis and Sporobolomyces roseus virtually did not change throughout the year. The relative abundance of the euribiotic species Cryptococcus albidus showed irregular monthly variations. The data obtained show that the epiphytic microbial population of various plants can be comprehensively studied only by analyzing this population throughout the vegetative period of the plants.     

Geographic and temporal variation in the ant–seed dispersal assemblage of the perennial herb Helleborus foetidus L. (Ranunculaceae)

Spatio-temporal variations in the composition of the animal interactive assemblages may result in variations in selective pressures on the plants. In ant–seed dispersal mutualisms, the study of the magnitude of spatial and temporal variation of ant assemblages is rarely studied, limiting inferences and generalizations on the evolution of this mutualism. Here, we describe the ant–disperser assemblage of the myrmecochorous herb Helleborus foetidus in 14 populations across the Iberian Peninsula, and dissect the variation in the assemblage into spatial and temporal components as a first step to evaluate the evolutionary potential of this interaction. The ant–visitor assemblage of H. foetidus was mainly represented by species of Formicinae and it was highly diverse and variable in composition and function. Ants behaving as legitimate dispersers and those with mixed behaviour numerically dominated the assemblage compared with elaiosome consumers. The magnitude of the spatial variation was higher than the temporal variation, suggesting that the relative frequency of each functional group will be more foreseeable among years in each population than among populations. At the expense of further analysis of the effects of such variation on dispersal success, we can envisage a selection mosaic scenario, where local adaptive responses of plants might arise as a result of local variations in the specific composition and function of the assemblage.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 135–150.     

Explosive seed dispersal in two perennial Mediterranean Euphorbia species (Euphorbiaceae)

The distance of explosive dispersal, its pattern in time, and the relative importance of autochory have been studied in two diplochorous species: Euphorbia boetica and E. nicaeensis. The seeds of E. boetica released by explosive dispersal reached a median distance of 156 cm and a maximum of almost 8 m, while the distances reached by the seeds of E. nicaeensis were lower: a median of 132 cm and a maximum of 5 m. The differences in explosive dispersal distance between species seem to depend on both seed mass and caruncle retention. The seeds of both species present a caruncle, but in E. boetica this is tiny, and in most cases is shed during the explosion of the capsules. The distances reached by the seeds of these species, dispersed just by capsule explosion, were similar to or greater than the distances to which ants disperse seeds in the Mediterranean sclerophyllous vegetation. Diplochorous plants may maximize either the distance of primary dispersal or that of secondary dispersal. Given that the seeds of E. boetica, that lose their caruncles, are not gathered by myrmecochorous ants, the results suggest that E. boetica maximizes its primary dispersal distance, whereas E. nicaeensis favors its secondary dispersal.     

Leaf longevity of Oxalis acetosella (Oxalidaceae) in the Catskill Mountains, New York, USA

Leaf habit correlates with multiple physiological traits. Understanding ecophysiology is therefore dependent on knowledge of leaf habit. A variety of leaf habits exists within forest understory plant communities. Oxalis acetosella is one such understory plant and has long been considered a wintergreen, meaning that it keeps a set of leaves for one full year, replacing them with a new set during spring. To assess the leaf habit of O. acetosella and place it into a classification scheme of leaf habits, leaves of four populations of O. acetosella were repeatedly censused for two years in a northern hardwood forest of the Catskill Mountains, New York, USA. New leaves developed and old leaves senesced throughout the year, yielding a continual replacement of leaves and a summer peak in leaf number. Leaves that developed in the fall and winter had longer maximum life spans than leaves that developed during the summer. The name "seasonalgreen" is suggested to describe the continual development, senescence, and presence of leaves and annual peak in leaf number within O. acetosella. The functional significance of this leaf habit in this species and the possibility of its presence in other species deserve further study.     

Size-dependent gender modification in a hermaphroditic perennial herb

The size-advantage model predicts that hermaphroditic organisms adjust sex allocation depending on their resource status. We investigated the relationship between size and sex allocation in the co-sexual perennial herbs Trillium erectum and Trillium grandiflorum at two sites in southern Ontario, Canada by measuring pollen and ovule production and biomass allocation at flowering and fruiting. In both species, there was a strong relationship between size and gender; larger plants allocated proportionately more biomass to female reproduction and produced fewer pollen grains relative to ovules than smaller plants. Variation in gender was better explained by size than age, although age and size were correlated. While the relationship between size and gender was similar between species, T. erectum allocated proportionately more to female reproduction than T. grandiflorum, independent of size. In the absence of pollen limitation, there was no evidence of secondary adjustment of gender at fruiting. The results are discussed in the context of models predicting size-dependent gender modification in animal-pollinated plants. Evidence about the pollination and seed dispersal biology of Trillium spp. suggests that the relative effects of local mate and resource competition may be important in driving size-dependent sex allocation in these species.     

A new rain-operated seed dispersal mechanism in Bertolonia mosenii (Melastomataceae), a Neotropical rainforest herb

Although widespread among fungi, lichens, liverworts, and mosses, seed dispersal mechanisms operated by rain are unusual among flowering plants. Generally speaking, two mechanisms are involved in seed dispersal by rains: the splash-cup and the springboard. Here we describe a new seed dispersal mechanism operated by rain in a Neotropical rainforest herb Bertolonia mosenii Cogniaux (Melastomataceae). The study was carried out at the lowland Atlantic rainforest, southeastern Brazil. We experimentally demonstrate that rain is necessary to release the seeds from the capsules through what we call "squirt-corner" seed dispersal mechanism: when a raindrop strikes the mature fruit, the water droplet forces the seeds outward to the angles (corners) of the triangular capsule and the seeds are released. As far as we know squirt-corner represents a new rain-operated seed dispersal mechanism, and a novel seed dispersal mode both for Melastomataceae and for flowering plants from Neotropical forests.     

Sexual reproduction and seed dispersal pattern of annual and perennial Zostera marina in a heterogeneous habitat

The sexual reproduction of annual and perennial Zostera marina was investigated in Moon Lake, Shandong, China. Based on the disturbance and stress regimes, the Z. marina beds were classified into five types: intertidal annual (IA) and perennial (IP) eelgrass patches, subtidal patch area (PA), meadow margin (MM) and meadow center (MC). Seed dispersal was investigated using artificial seagrass units in the five areas and another two areas [adjacent bare area and Zostera japonica meadow (Zj)]. Total and flowering shoot density and aboveground biomass of flowering shoots per unit area were higher in PA and MM, and lower in IA and IP, whereas the total biomass per unit area in MC showed the highest value. Reproductive effort (RE) in IA showed negative response to intertidal stress, while in perennial IP, PA and MM it showed significantly positive response to anthropogenic or natural disturbances. The density-based RE in perennial IP, PA and MM was 1.1-, 5.1- and 5.1-fold higher than that in MC, while in annual IA it was 0.46-fold lower. Additionally, the biomass-based RE in IP, PA and MM was 1.8-, 3.5- and 3.8-fold higher than that in MC, while the RE in IA was 0.84-fold lower. The estimated seed production per unit area was much greater in PA (60,793 ± 9,843 seeds m^?2) and MM (43,414 ± 8,718 seeds m^?2) than in IA (416 ± 83 seeds m^?2), IP (3,820 ± 1,470 seeds m^?2) and MC (9,779 ± 631 seeds m^?2), while the seed density ranged from 24 ± 6 to 584 ± 56 seeds m^?2. Results suggested that in response to disturbances and stress, Z. marina in subtidal areas increased their RE and seed production and thus seeds were available to be dispersed into areas where seed production was limited.     

Seasonal Dynamics in a Yeast Population on Leaves of the Common Wood Sorrel Oxalis acetosella L.

Analysis of an epiphytic yeast population on the leaves of the evergreen common wood sorrel Oxalis acetosella L. throughout a year showed that the density and the species composition of this population underwent regular seasonal changes. There were almost no yeasts on the young spring leaves. However, the yeast population on the mature leaves tended to increase in the autumn, reaching a maximum after the formation of continuous snow cover. Then the yeast population on the leaves tended to decrease, reaching a minimum in the spring. The species diversity of the yeasts was maximum in the autumn. The population of the epiphytic yeast species Cystofilobasidium capitatum, Rhodotorula fujisanensis, Leucosporium scottii, and Cryptococcus flavus peaked in the autumn. On the other hand, the population of the widespread epiphytic species Cryptococcus laurentii on the wood sorrel leaves peaked in January. The relative abundance of the red-pigmented phytobionts Rhodotorula glutinis and Sporobolomyces roseus virtually did not change throughout the year. The relative abundance of the euribiotic species Cryptococcus albidus showed irregular monthly variations. The data obtained show that the epiphytic microbial population of various plants can be comprehensively studied only by analyzing this population throughout the vegetative period of the plants.     

Development of microsatellite markers in a clonal perennial herb,Convallaria keiskei

We developed eight polymorphic microsatellite simple sequence repeat (SSR) loci from genomic DNA of a clonal perennial herb, Convallaria keiskei, using a dual‐suppression‐polymerase chain reaction (PCR) technique and an improved technique. These markers with four to 10 alleles per locus identified 29 genotypes in 82 samples collected from a population in Hokkaido, Japan. The observed and expected heterozygosities ranged from 0.241 to 0.862 and from 0.639 to 0.825, respectively. These SSR markers will be available to identify genets and evaluate genetic diversity of C. keiskei.     

Age-specific, density-dependent and environment-based mortality of a short-lived perennial herb

Density-independent and density-dependent processes affect plant mortality. Although less well understood, age-specific mortality can also play an important role in plant mortality. The goal of this study was to analyse several factors accounting for mortality in the Mediterranean short-lived perennial herb Lobularia maritima. We followed three cohorts of plants (from emergence to death) during 4 years in field conditions. We collected data on plant mortality of the effect of biotic agents (moth larvae and mycoplasma-like organisms, MLOs) and environmental variables. We also estimated density-dependent relationships affecting the fate of seedlings and adults. Results show that cohorts differed in their survival curves and ageing significantly increased mortality risk. Seedling mortality was density-dependent whereas adult mortality was not affected by density. MLO infection led to higher plant mortality whereas moth larvae attack did not affect plant mortality. In general, seedlings and adult plants experienced the highest mortality events in summer. We found, however, weak relationships between weather records and plant mortality. Age and size structures were not correlated. Overall, this study provides a comprehensive review of age-specific, density-dependent and density-independent factors that account for mortality of L. maritima plants throughout their life cycle in field conditions, highlighting the fact that age is an important factor in determining plant population dynamics.     

Effects of flower dimorphism and light environment on arbuscular mycorrhizal colonisation in a cleistogamous herb

Although it is known that floral dimorphism contributes to the maintenance of mixed breeding systems, the consequences of producing progeny of a contrasting genetic background and seeds with differential resource allocation has been practically ignored regarding establishment of belowground organisms–plant interactions. This article evaluates the combined effect of floral dimorphism with cross type and light environment on interactions between Ruellia nudiflora and arbuscular mycorrhizal fungi (AMF). R. nudiflora produces cleistogamous (CL) flowers that exhibit obligate self‐pollination and chasmogamous (CH) flowers with facultative self‐ (CHs) or cross‐ (CHc) pollination. We evaluated the establishment of the plant–AMF interaction in progeny derived from each floral type, under two light conditions (shaded versus open). We established different scenarios depending on the existence of inbreeding depression (ID) and whether the differential resource allocation (DRA) to CH and CL flowers affected the R. nudiflora–AMF interaction. We predicted that under shaded light conditions there might be an intensification of ID, having a negative effect on AMF colonisation. The percentages of hyphae and vesicles in the harvested roots was significantly higher in the shaded plants (F ≥ 4.11, P < 0.05), while progeny of CHc and CHs presented a higher percentage of hyphae and vesicle colonisation compared to CL progeny (F = 15.26, P < 0.01). The results show that DRA to CH flowers and light availability both determines the establishment of R. nudiflora–AMF interaction. The results also suggest that even under stressful light conditions, endogamy does not affect this interaction, which may explain the success of R. nudiflora as an invasive species.     

Secondary seed dispersal of Erodiophyllum elderi,a patchily distributed short‐lived perennial in the arid lands of Australia

We investigated secondary dispersal of propagules of Erodiophyllum elderi (Asteraceae), a short‐lived perennial plant growing in small patches in the arid lands of southern Australia. In spite of its importance for population dynamics, secondary dispersal is a little understood process. We monitored the dispersal of 2280 large woody capitula (seed heads) released in six E. elderi patches for 9 months. Colour‐coded seed heads were located at night using UV light and their distance and direction from the release point were measured. Over the 9‐month period, more seed heads moved, and those that did, moved further in areas with high herbivore activity. Overall dispersal distance across the ground was limited to less than 30 m. Dispersal patterns were related to the topographical slope at the release site: seed heads moved further, and more dispersed on steeper slopes unless the steep slopes had sandy soil in which case seed heads were buried, caught or there was reduced sheet water flow limiting their dispersal potential. After several months, seed head dispersal virtually ceased as seed heads became stuck in the debris and soil after heavy rains or further dispersal became unlikely when seed heads reached locally low‐lying areas. Secondary dispersal patterns suggest two distinctly different influences associated with the presence of herbivores: the direct movement of seed heads by trampling from sheep (an introduced herbivore) and the indirect effect of a reduced standing biomass from grazing. Reduced vegetation cover allows seed head redistribution via sheet water flow during large rainfall events.     

Linking vital rates to invasiveness of a perennial herb

Invaders generally show better individual performance than non-invaders and, therefore, vital rates (survival, growth, fecundity) could potentially be used to predict species invasiveness outside their native range. Comparative studies have usually correlated vital rates with the invasiveness status of species, while few studies have investigated them in relation to population growth rate. Here, I examined the influence of five vital rates (plant establishment, survival, growth, flowering probability, seed production) and their variability (across geographic regions, habitat types, population sizes and population densities) on population growth rate (λ) using data from 37 populations of an invasive, iteroparous herb (Lupinus polyphyllus) in a part of its invaded range in Finland. Variation in vital rates was often related to habitat type and population density. The performance of the populations varied from declining to rapidly increasing independently of habitat type, population size or population density, but differed between regions. The population growth rate increased linearly with plant establishment, and with the survival and growth of vegetative individuals, while the survival of flowering individuals and annual seed production were not related to λ. The vital rates responsible for rapid population growth varied among populations. These findings highlight the importance of both regional and local conditions to plant population dynamics, demonstrating that individual vital rates do not necessarily correlate with λ. Therefore, to understand the role of individual vital rates in a species ability to invade, it is necessary to quantify their effect on population growth rate.