Waterlogging responses in dune,swale and marsh populations of Spartina patens under field conditions

Summary Soil waterlogging responses were examined in three Spartina patens populations along a steep flooding gradient in coastal Louisiana. Root anatomy and physiological indicators of anaerobic metabolism were examined to identify and compare flooding responses in dune, swale and marsh populations, while soil physicochemical factors were measured to characterize the three habitats. Soil waterlogging increased along the gradient from dune to marsh habitats and was accompanied by increases in root porosity (aerenchyma). Aerenchyma in marsh roots was apparently insufficient to provide enough oxygen for aerobic respiratory demand, as indicated by high root alcohol dehydrogenase activities and low energy charge ratios. Patterns of root metabolic indicators suggest that dune and swale roots generally respired aerobically, while anaerobic metabolism was important in marsh roots. However, in each population, relatively greater soil waterloging was accompanied by differences in enzyme activities leading to malate accumulation. In dune and swale roots under these circumstances, depressed adenylate energy charge ratios may have been the result of an absence of increased ethanol fermentation. These trends suggest that: 1) Aerenchyma formation was an important, albeit incomplete, long-term adaptation to the prevalent degree of soil waterlogging. 2) All populations adjusted root metabolism in response to a relative (short-term) increase in soil waterlogging.     

Physiological Integration among Clonal Ramets during Invasion of Disturbance Patches in a New England Salt Marsh

Resource sharing between ramets growing across environmentalresource gradients may have important consequences for clonalplant populations and community dynamics. As the clonal saltmarsh grasses, Spartina patens and Distichlis spicata, vegetativelycolonize disturbance-generated bare patches, they span steepgradients in soil salinity and available sunlight. Examinationof water relations and carbon translocation in the field andgreenhouse revealed that connected ramets of these marsh grassesshare water and carbon in response to gradients in resourceavailability. Ramets colonizing disturbance patches rely uponphysiological integration with connected parent ramets to overcomewater stress associated with hypersaline patch environments.In addition, upon establishment inside a bare patch, daughterramets may translocate carbon back to shaded parent ramets inthe surrounding vegetation outside of patches. Physiological integration of ramets colonizing disturbance-generatedbare patches and parent ramets outside of patches may explainthe predominance of vegetative invasion over sexual recruitmentin marsh succession. Hypersaline soil conditions, which inhibitseedling recruitment into patches, have little effect on thesuccess of clonal colonizers that can import water from parentramets. This success appears to be due to the ability of clonalmarsh grasses to translocate water and carbon products betweenramets growing across opposing gradients in resource availability.Copyright1995, 1999 Academic Press Clonal integration, Distichlis spicata, halophytes, salt marsh ecology, secondary succession, Spartina patens     

Clonal integration in Ranunculus reptans: by‐product or adaptation?

We studied fitness consequences of clonal integration in 27 genotypes of the stoloniferous herb Ranunculus reptans in a spatially heterogeneous light environment. We grew 216 pairs of connected ramets (eight per genotype) with mother ramets in light and daughter ramets in shade. In half of the pairs we severed the stolon connection between the two ramets at the beginning of the experiment. During the experiment, 52.7% of the ramet pairs with originally intact connection physically disintegrated. We detected significant variation among genotypes in this regard. Survival of planted ramets was 13.3% higher for originally connected pairs. Moreover, there was significant variation among genotypes in survival, in the difference in survival between plant parts developing from mother and daughter ramets, and in the effect of integration on this difference. In surviving plants connection between ramets decreased size differences between mother and daughter parts. Variation among genotypes was significant in growth and reproduction and marginally significant in the effect of physiological integration on growth and reproduction. Connected daughter ramets had longer leaves and internodes than daughters in severed pairs indicating that integration stimulated plant foraging in both the vertical and the horizontal plane. Observed effects of integration on fitness components in combination with genetic variation in maintenance and effects of connection indicate that clonal integration in R. reptans has the capability to evolve, and therefore suggest that clonal integration is adaptive. If genetic variation in integration is common, future studies on clonal integration should always use defined genetic material and many clones to allow extrapolation of results to population and wider levels.     

PHENOTYPIC PLASTICITY IN POLYGONUM PERSICARIA. I. DIVERSITY AND UNIFORMITY IN GENOTYPIC NORMS OF REACTION TO LIGHT

Several aspects of genotype-environment interaction may act to modulate natural selection in populations that encounter variable environments. In this study the norms of reaction (phenotypic responses) of 20 cloned genotypes from two natural populations of the annual plant Polygonum persicaria were determined over a broad range of controlled light environments (8%-100% full sun). These data reveal both the extent of functionally adaptive phenotypic plasticity expressed by individual genotypes, and the patterns of diversity among genotypes for characters relevant to fitness, in response to an environmental factor that is both highly variable within populations and critical to growth and reproduction.     

THE COADAPTATION OF PARENTAL AND OFFSPRING CHARACTERS

Parents often have important influences on their offspring's traits and/or fitness (i.e., maternal or paternal effects). When offspring fitness is determined by the joint influences of offspring and parental traits, selection may favor particular combinations that generate high offspring fitness. We show that this epistasis for fitness between the parental and offspring genotypes can result in the evolution of their joint distribution, generating genetic correlations between the parental and offspring characters. This phenomenon can be viewed as a coadaptive process in which offspring genotypes evolve to function with the parentally provided environment and, in turn, the genes for this environment become associated with specific offspring genes adapted to it. To illustrate this point, we present two scenarios in which selection on offspring alone alters the correlation between a maternal and an offspring character. We use a quantitative genetic maternal effect model combined with a simple quadratic model of fitness to examine changes in the linkage disequilibrium between the maternal and offspring genotypes. In the first scenario, stabilizing selection on a maternally affected offspring character results in a genetic correlation that is opposite in sign to the maternal effect. In the second scenario, directional selection on an offspring trait that shows a nonadditive maternal effect can result in selection for positive covariances between the traits. This form of selection also results in increased genetic variation in maternal and offspring characters, and may, in the extreme case, promote host-race formation or speciation. This model provides a possible evolutionary explanation for the ubiquity of large genetic correlations between maternal and offspring traits, and suggests that this pattern of coinheritance may reflect functional relationships between these characters (i.e., functional integration).     

Multivariate selection shapes environment-dependent variation in the clonal morphology of a red seaweed

Within-individual strategies of variation (e.g., phenotypic plasticity) are particularly relevant to modular organisms, in which ramets of the same genetic individual may encounter diverse environments imposing diverse patterns of selection. Hence, measuring selection in heterogeneous environments is essential to understanding whether environment-dependent phenotypic change enhances the fitness of modular individuals. In sublittoral marine habitats, competition for light and space among modular taxa generates extreme patchiness in resource availability. Little is known, however, of the potential for plasticity within individuals to arise from spatially-variable selection in such systems. We tested whether plasticity enhances genet-level fitness in Asparagopsis armata, a clonal seaweed in which correlated traits mediate morphological responses to variation in light. Using the capacity for rapid, clonal growth to measure fitness, we identified aspects of ramet morphology targeted by selection in two contrasting light environments and compared patterns of selection across environments. We found that directional selection on single traits, coupled with linear and nonlinear selection on multi-trait interactions, shape ramet morphology within environments and favor different phenotypes in each. Evidence of environment-dependent, multivariate selection on correlated traits is novel for any marine modular organism and demonstrates that seaweeds, such as A. armata, may potentially adapt to environmental heterogeneity via plasticity in clonal morphology.     

VARIATION IN REACTION NORMS AMONG POPULATIONS OF THE GRASS BOUTELOUA RIGIDISETA

Recent research has emphasized the importance of investigating the reaction norms of quantitative traits to understand evolution in natural environments. In this study, genetic differences in reaction norms among eight populations of the grass Bouteloua rigidiseta were examined using clonal replicates of genotypes planted in a common garden with two levels of competition (single B. rigidiseta without competition and single B. rigidiseta surrounded by four Erioneuron pilosum). The populations were found to be genetically differentiated for a variety of traits. Differences in reaction norms of size-specific fecundity (spikelet clusters per tiller number) were detected among the populations: some showed little response to competition; in others size-specific fecundity was much greater in the absence of competition. This divergence in reaction norms among these populations may be the result of past selection (including the cost of plasticity), or genetic drift.     

Edaphic diatom communities associated with Spartina alterniflora and S. patens in New Jersey

Edaphic diatoms inhabiting the sediments beneath dwarf Spartina alterniflora Loisel. and S. patens (Ait.) Muhl. in Great Bay salt marsh, Tuckerton, New Jersey were collected from 24 September 1974 through 20 August 1975. Of the 91 taxa encountered, 8 were endemic to the dwarf S. alterniflora habitat and 42 endemic to the S. patens habitat. The edaphic diatom community associated with S. patens was comprised of a much greater number of taxa and possessed higher values for species diversity (H') and evenness (J') than the community associated with dwarf S. alterniflora. The salinity of the marsh surface showed a completely opposite trend, being greatly reduced at the S. patens habitat. A highly significant relationship (P < 0.001) between the number of diatom taxa and marsh surface salinity at the S. patens habitat was demonstrated by a least squares regression. This finding led to the conclusion that the dissimilarity in the structure of the two edaphic diatom communities was primarily due to the very low marsh surface salinities at the S. patens habitat from January through June, and that this sustained. low-salinity regime allowed a very large number of taxa to coexist only in the S. patens community. Comparison of the diatom flora of Great Bay salt marsh with that of a Delaware marsh studied previously by the author showed that 67.0% of the 91 taxa encountered in New Jersey also occur on the Delaware marsh.     

POPULATION DIFFERENTIATION FOR PHENOTYPIC PLASTICITY IN THE STELLARIA LONGIPES COMPLEX

Population differentiation for phenotypic plasticity of 12 morphological and reproductive traits was investigated in five populations of the Stellaria longipes complex including a population of the sand dune endemic S. arenicola. Population differentiation was detected for the mean (genotypic) value, amount of plasticity, and pattern of plasticity of traits. Average amount of plasticity was not related to degree of isozyme variability in the populations. Differentiation for pattern of plasticity was much more common than for amount. The direction and extent of divergence among populations was dependent on which of the three trait aspects was under consideration (mean, amount of plasticity, pattern of plasticity) and did not reflect their similarity as revealed by enzyme electrophoretic data. It was concluded that trait means, amounts of plasticity, and patterns of plasticity are independent of one another during evolutionary divergence and may be influenced by mosaic selection.     

LIFE-CYCLE COMPONENTS OF SELECTION IN ERIGERON ANNUUS: II. GENETIC VARIATION

Genetic variation for seedling and adult fitness components was measured under natural conditions to determine the relative importance of the seedling stage for lifetime fitness in Erigeron annuus. Variation in lifetime reproductive success can result from both the persistent effects of genetic variation expressed among seedlings and from variation in adult fitness components. Analysis of covariance was used to separate the stage specific from the cumulative effects of genetic variance expressed earlier in the life cycle. E. annuus produces seeds through apomixis, which allowed measurement of the fitness of replicate genotypes from germination through the entire life cycle. There were significant differences among genotypes for date of emergence, seedling size, survivorship and fecundity, but heritabilities were low, indicating slow response to selection. For all characters, environmental components of variance were one to two orders of magnitude larger than genetic variance components, resulting in broad sense heritabilities less than 0.1. For seedling size and fecundity, all of the genetic variance was in the form of genotype-environment interactions, often with large negative genetic correlations across environments. In contrast, genotypes differed in mean survivorship through one year, but there were no genotype-environment interactions for viability. Genetic differences in viability were primarily expressed as differences in overwinter survivorship. Genotype × environment interactions among sites and blocks were generated early in the life cycle while the genotype × environment interactions in response to competitive environment (open, annual cover, perennial cover) first appeared in adult fecundity. Genetic variation in lifetime fitness was not significant, despite a fourfold difference in mean fitness among genotypes.     

Morphological flexibility across an environmental gradient in the epiphytic orchid,Tolumnia variegata: complicating patterns of fitness

Deceit‐pollinated orchid species show substantial variation in floral traits, which may be maintained by genetic drift or various forms of selection, or may reflect phenotypic plasticity. We explored how much plasticity occurs in both vegetative and floral traits of Tolumnia variegata (Oncidiinae, Orchidaceae) across two different light environments in Puerto Rico using data from a reciprocal transplant experiment. We also examined how fruit set, a measure of reproductive success and a surrogate for fitness, is associated with this morphological variation, and whether it changes over time. Tolumnia variegata responded to environmental variables in multiple ways. Vegetative characters were more plastic than those associated with sexual reproduction. Transplant effects accounted for significant variation in flower length, lip length, number of inflorescences, peduncle length, leaf length and the total number of ramets, but responses were not always consistent among years. Phenotypic selection on morphological characters was dependent on plant location. The trends detected were complex, and often inconsistent across years, probably as a result of wetter and drier years than average. Overall fruit set was quite variable among plants, averaging 15%, with no significant differences among sun and shade plants. Although reproductive success was similar among sites, habitat heterogeneity and annual variation had an effect on morphological expression, which sometimes modified the trajectories of phenotypic selection. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163 , 431–446.     

Sexual reproduction is light-limited as marsh grasses colonize maritime forest

Climate change is driving abiotic shifts that can threaten the conservation of foundation species and the habitats they support. Directional range shifting is one mechanism of escape, but requires the successful colonization of habitats where interspecific interactions may differ from those to which a species has adapted. For plants with multiple reproductive strategies, these range-edge interactions may alter the investment or allocation toward a given reproductive strategy. In this study, we quantified sexual reproduction of the clonal marsh grass Spartina patens across an inland colonization front into maritime forest being driven by sea-level rise. We find that flowering is variable across S. patens meadows, but consistently reduced in low light conditions like those of the forest understory. Observational surveys of S. patens flowering at four sites in the Delmarva Peninsula agreed with the results of two experimental manipulations of light availability (shading experiment in S. patens-dominated marsh and a forest dieback manipulation). These three approaches pinpointed light limitation as a principal control on S. patens flowering capacity, suggesting that light competition with taller upland species can suppress S. patens flowering along its upland migration front. Consequently, all propagation in shaded conditions must occur clonally or via seeds from the marsh, a reproductive restriction that could limit the potential for local adaptation and reduce genetic diversity. Future research is needed to determine whether the lack of flowering is the result of a trade-off between sexual and clonal reproduction or results from insufficient photosynthetic products needed to achieve either reproductive method.     

EVALUATION OF PROLINE ACCUMULATION IN THE ADAPTATION OF DIVERSE SPECIES OF MARSH HALOPHYTES TO THE SALINE ENVIRONMENT

Proline accumulation by eight major species of salt marsh halophytes was examined under growth chamber and field conditions. When the plants were exposed to increasing salinities in the growth chamber, they accumulated proline after a threshold salinity had been reached. Three general patterns were apparent. Limonium carolinianum (Walt.) Britt. and Junius roemerianus Scheele began to accumulate proline at 0.25 m NaCl with accumulations up to 63.6 μmoles per gram fresh weight at higher salinities. The C₄ grasses, Spartina alterniflora Loisel., Spartina patens (Aiton) Muhl., and Distichlis spicata (L.) Greene, had threshold salinity levels around 0.5 m NaCl and accumulated proline to 27.4 μmoles per gram fresh weight. The succulents, Salicornia bigelovii Torr., Salicornia virginica L., and Borrichia frutescens (L.) DC, did not accumulate proline until very high salinities (0.7 m) were reached. Water stress imposed by polyethylene glycol instead of NaCl caused similar proline accumulation in the species studied, but to different extents. Field measurements of proline content and soil salinities correlated well with the findings from growth chamber experiments. Rates of proline accumulation and breakdown in L. carolinianum were sufficient for osmotic adjustment by the plant to the changes in interstitial salinity in the marsh. The significance of proline accumulation as an adaptation to the salt marsh environment was species specific. We suggest that proline accumulation is of considerable importance in L. carolinianum and J. roemerianus, important to the C₄ grasses at certain times and in certain locations in the marsh, and of little importance in the succulents.     

CLONAL INTEGRATION ACROSS A SALT GRADIENT BY A NONHALOPHYTE,HYDROCOTYLE BONARIENSIS (APIACEAE)

This study examined the benefits associated with resource sharing among interconnected ramets spanning a soil salinity gradient. Clones of Hydrocotyle bonariensis, a rhizomatous dune perennial, expand into salt marsh communities from surrounding upland dune systems in coastal North Carolina. In rhizome-severing experiments conducted under both field and laboratory conditions, Hydrocotyle was shown to proliferate ramets under saline conditions, provided that these ramets were connected to other ramets growing in nonsaline conditions. Ramets that benefited from resource integration did not appear to be affected by local salt exposure in that these ramets were morphologically similar to those grown under nonsaline conditions. Supporting ramets incurred no net cost in terms of biomass or ramet production, but there was an increased percent allocation to roots and rhizomes. Ramets grown in saline conditions without the benefit of clonal integration showed high mortality and produced little or no net clonal growth. It is likely that the acropetal movement of water allowed Hydrocotyle clones to ameliorate the heterogeneous saline conditions associated with coastal environments.     

PHENOTYPIC PLASTICITY IN PHLOX. I. WILD AND CULTIVATED POPULATIONS OF P. DRUMMONDII

We investigated the changes in amounts and patterns of phenotypic plasticity which have arisen in the Texas annual Phlox drummondii during domestication. Character means and plasticities were compared for five populations: a wild population, three cultivated varieties (a Tall cultivar and two Dwarf cultivars), and a population of an escaped Tall cultivar naturalized in Texas. To measure plasticity, we scored the responses of 10 characters to six treatments and analyzed both the amount and direction of plastic response. Wild plants are phenotypically distinct from the Tall and Escaped cultivar and from the two Dwarf cultivars. Despite its substantial phenotypic divergence from the Wild population, the Tall cultivar's plasticity has changed little during domestication. Traits most strongly correlated with fitness show the least change in their plasticities. The two Dwarf varieties have very similar plasticities, despite strong phenotypic divergence from the Tall population and despite the fact that they were derived from different Tall lines. This suggests that indirect selection on phenotypic plasticity related to selection for the Dwarf habit has resulted in the characteristic plasticity of the Dwarf lines. The Escaped cultivar has substantially different plastic responses from those of the Wild or cultivated populations.     

How will warming affect the salt marsh foundation species Spartina patens and its ecological role?

Foundation species structure environments and create refuge from environmental stress. In New England high salt marsh, the grass Spartina patens is a foundation species that reduces salinity, anoxia, desiccation, and thermal stresses through canopy shading and root proliferation. In a factorial S. patens-removal and warming field experiment, foundation species removal strongly impacted every aspect of the community, reiterating the important role of the foundation species S. patens in the high marsh. Given this central role, we hypothesized that facilitation by the foundation species would be even more important under warmer conditions by ameliorating more severe thermal stress. However, the ecological role of S. patens was unaffected by experimental warming, and, independent of the presence of the foundation species, warming had only weak effects on the salt marsh ecological community. Only the foundation species itself responded strongly to warming, by significantly increasing aboveground production in warmed plots. Apparently, amelioration of thermal stress is not as important for salt marsh ecosystem function as S. patens’ moderation of salinity and desiccation stresses. From these experimental results, we anticipate that climate change-associated thermal stress will not greatly affect S. patens-dominated high marsh communities. In contrast, foundation species loss, an emergent conservation issue in Atlantic salt marshes, represents a critical threat to salt marsh ecosystem function.     

EXPERIMENTAL STUDIES OF THE EVOLUTIONARY SIGNIFICANCE OF SEXUAL REPRODUCTION. III. MATERNAL AND PATERNAL EFFECTS DURING SEEDLING ESTABLISHMENT

To determine whether genetic differences in fitness components exist among seeds and seedlings in a natural population, weighed propagules of six parents of Anthoxanthum odoratum from a reciprocal diallel cross were planted into the parental source population, a mown field. Seed families of maternal genotypes differed in germination success, while paternal families showed no detectable differences. Differential germination success could not be attributed to propagule weight. Seed families ranked differently in germination percentage in different blocks. No survivorship differences among parental seed families could be detected. There were significant cross × block × germination and cross × block × survivorship interactions; different crosses performed better or worse in different blocks. In some cases, crosses sired by different fathers within a maternal seed family differed in germination or survivorship, suggesting that natural selection may be capable of discriminating among juvenile genotypes within a maternal family despite the presence of large overall maternal effects. These results indicate that seedling establishment may differ according to genotype and that microsite heterogeneity may maintain genetic variation in juvenile traits in natural plant populations.     

Mosaic microecological differential stress causes adaptive microsatellite divergence in wild barley, Hordeum spontaneum, at Neve Yaar, Israel.

Genetic diversity at 38 microsatellite (short sequence repeats (SSRs)) loci was studied in a sample of 54 plants representing a natural population of wild barley, Hordeum spontaneum, at the Neve Yaar microsite in Israel. Wild barley at the microsite was organized in a mosaic pattern over an area of 3180 m2 in the open Tabor oak forest, which was subdivided into four microniches: (i) sun-rock (11 genotypes), (ii) sun-soil (18 genotypes), (iii) shade-soil (11 genotypes), and (iv) shade-rock (14 genotypes). Fifty-four genotypes were tested for ecological-genetic microniche correlates. Analysis of 36 loci showed that allele distributions at SSR loci were nonrandom but structured by ecological stresses (climatic and edaphic). Sixteen (45.7%) of 35 polymorphic loci varied significantly (p < 0.05) in allele frequencies among the microniches. Significant genetic divergence and diversity were found among the four subpopulations. The soil and shade subpopulations showed higher genetic diversities at SSR loci than the rock and sun subpopulations, and the lowest genetic diversity was observed in the sun-rock subpopulation, in contrast with the previous allozyme and RAPD studies. On average, of 36 loci, 88.75% of the total genetic diversity exists within the four microniches, while 11.25% exists between the microniches. In a permutation test, G(ST) was lower for 4999 out of 5000 randomized data sets (p < 0.001) when compared with real data (0.1125). The highest genetic distance was between shade-soil and sun-rock (D = 0.222). Our results suggest that diversifying natural selection may act upon some regulatory regions, resulting in adaptive SSR divergence. Fixation of some loci (GMS61, GMS1, and EBMAC824) at a specific microniche seems to suggest directional selection. The pattern of other SSR loci suggests the operation of balancing selection. SSRs may be either direct targets of selection or markers of selected haplotypes (selective sweep).     

Effect of Nitrogen, Phosphorus and Potassium Additions on Plant Biomass and Soil Nutrient Content of a Swale Barrier Strand Community in Louisiana

Fertilization of a swale plant community with various levelsand combinations of nitrogen, phosphorus and potassium resultedin increased plant growth. Nitrogen addition produced the greatestincrease in biomass. At some high nitrogen levels, phosphoruslimited plant production. Potassium fertilization did not influenceplant growth. Phosphorus fertilization decreased the levelsof soil calcium, magnesium and manganese. A shore-perpendiculargradient in apparent saltwater inundation influenced soil pHand the concentrations of iron, phosphorus, and magnesium. Fertilizer effects, swale Scirpus americanus, Spartina patens, nitrogen limitation     

Growth of tissue culture–regenerated salt marsh monocots in a simulated marsh field plot: Implication for wetland creation and restoration

Phenotypically and genetically variable salt marsh plants are needed for wetland creation and restoration efforts. Selected tissue culture regenerants of five salt marsh monocots, Spartina patens, Spartina alterniflora, Juncus gerardi, Juncus roemerianus, and Scirpus robustus, were planted in a simulated marsh field plot that was flood-irrigated with 10 ppt salt water to compare their phenotypic variation for potential use in wetland projects. Plant growth was evaluated after one growing season. Phenotypic variation among regenerants was found in S. alterniflora, S. patens and J. gerardi, indicating the occurrence of somaclonal variation. In S. alterniflora, significant differences occurred among regenerants in stem density. In J. gerardi, significant differences occurred in height and clone circumference. In S. patens, two of the nine regenerants exhibited higher biomass and stem density than some of the other regenerants. By using the random amplified polymorphic DNA (RAPD) technique, genome DNA variation in S. patens regenerants was detected. Genetic variation not only occurred among phenotypically different regenerants, but also among those phenotypically similar for the characteristics measured. Tissue culture–regenerated plants often have desirable genetic characteristics and adaptability as a result of somaclonal variation and may enable a species to perform its ecological functions in created or restored wetlands where ideal environments cannot be achieved. Thus, some previously unrestorable sites may be restorable or marginal marshes made more productive.