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Ecology |
Department of Biology, University of Louisiana at Lafayette, Lafayette, Louisiana 70506 USA
Received for publication February 1, 2002. Accepted for publication June 4, 2002.
ABSTRACT
Saltwater intrusion into wetland ecosystems has destroyed or damaged many native plant populations. Iris hexagona is a salt-sensitive species that exhibits intraspecific variation in salinity tolerance. To investigate the effect of salinity on flowering, we exposed I. hexagona collected from natural populations to salt treatments in a common garden. Experimental salinity additions strongly delayed flowering phenology, but the effect was not apparent until the second year, when less than 4 g/L NaCl delayed flowering up to 3 d. In the field, soil salinity and flowering phenology varied substantially within I. hexagona populations. Iris flowers are receptive to pollinators for 2 d or less, therefore a 3-d delay could affect outcrossing dynamics, and ultimately, the evolutionary ecology of iris populations. Salinity also had a carryover effect; prior salinity exposure delayed flowering in irises that had been replanted in freshwater conditions for 6 mo. This is an important result because it suggests that episodic stress (such as tropical storms) can influence performance well after the stress has disappeared. Our research further underscores the importance of long-term studies because a 1-yr experiment would have failed to reveal the strong effects of salinity that emerged in the second year.
Key Words: flowering phenology • freshwater wetlands • glycophyte • phytohormones • salinity stress
Flowering is a life history trait determined by plant genotype, the environment, and the interaction between them (Rathcke and Lacey, 1985
). The timing of flower production can be critical for the evolutionary ecology of plant populations (Augspurger, 1981
; Fox, 1990b
). Synchronized flowering can increase the effective population size, reduce genetic structure, and maximize outcrossing (Augspurger, 1981
; Primack, 1985
). In contrast, asynchronous flowering can impede gene flow (Primack, 1985
; Cruzan et al., 1994
) and reduce reproductive success (Rathcke and Lacey, 1985
; Fox, 1990a
). In addition to genetic mechanisms, flowering is also affected by environmental factors such as photoperiod (Shitaka and Hirose, 1998
), temperature (Price and Waser, 1998
; Sandvik and Totland, 2000
), herbivory (Jackson, 1966
; Marquis, 1988
; English-Loeb and Karban, 1992
; Pilson, 2000
), and water stress (Fox, 1990a
, 2001
; Kelly, 1992
; Bram and Quinn, 2000
; Stanton, Roy, and Theide, 2000
).
Wetland plants are heavily impacted by saltwater intrusion, which can destroy or damage sensitive populations (Pezeshki, DeLaune, and Patrick, 1990
; Krauss et al., 2000
). However, some wetland species exhibit intraspecific variation in salinity tolerance, and it is particularly important to understand the effects of salinity on plants that can survive saline conditions (Allen, Chambers, and Pezeshki, 1997
; Hester, Mendelssohn, and McKee, 1998
; Seliskar and Gallagher, 2000
). Iris hexagona (Walter) is indigenous to coastal wetlands and has become an important model for ecological and evolutionary research (Bennett and Grace, 1990
; Arnold, Hamrick, and Bennett, 1993
; Burke et al., 2000
). This native Louisiana species occurs primarily in freshwater and brackish wetlands, and observations of these populations indicate that they exhibit high mortality due to saltwater intrusion. However, several populations inhabit brackish marsh environments, making I. hexagona a good species for studying ecological responses to environmental stress.
Salinity is a growing environmental concern in wetland communities (Twilley et al., 2001
), but we know very little about how salt exposure affects flowering in natural plant populations. Drought stress has been observed to delay flowering (Fox, 1990a
, 2001
; Kelly, 1992
; Bram and Quinn, 2000
; Stanton, Roy, and Theide, 2000
); since salinity and drought cause similar osmotic responses in plants (Levitt, 1980
), we hypothesized that salinity should produce flowering delays. In Louisiana, salinity stress is often episodic because it results from tropical storms. Because clonal plants can retain the effects of previous environmental conditions for subsequent generations of ramets (Schwaegerle, McIntyre, and Swingley, 2000
), we determined whether salinity had a carryover effect on floral phenology. We conducted common garden experiments to test these predictions and imposed two different salinity regimes on I. hexagona collected from natural populations: (1) continuous exposure to salinity and (2) salinity treatment followed by a return to freshwater conditions.
MATERIALS AND METHODS
Natural history
Iris hexagona Walter (Iridaceae) is a perennial species indigenous to freshwater marshes of the southern Atlantic and Gulf coasts and is widely distributed in Louisiana, USA (Viosca, 1935
). Flowers appear from late March to late April and are pollinated by Bombus spp. (Caillet and Mertzweiller, 1988
; Cruzan and Arnold, 1993
). Flowers are very short-lived and are available to pollinators for a maximum of 2 d. Iris hexagona produces large seed capsules containing 40–60 seeds and also reproduces vegetatively through sympodial rhizomes. Salinity tolerant I. hexagona occur on Marsh Island, a 300-km2 intermediate salt marsh located between the Vermilion Bay and the Gulf of Mexico, 10 km south of mainland Louisiana (29.79° N, 91.78° W).
Field salinity levels
To determine surface water salinity at Marsh Island, we used data obtained from hourly measurements conducted by The State of Louisiana Department of Wildlife and Fisheries (E. Mouton, State of Louisiana Department of Wildlife and Fisheries, personal communication) on a YSI model 30 SCT salinity meter (YSI, Yellow Springs, Ohio, USA). Data were averaged from hourly readings taken at four sites from 1997 to 2001. We also monitored soil interstitial salinity at our sites by inserting a probe to a depth of 20 cm, extracting soil water with a syringe, and measuring the sample with an Orion 125 conductivity meter (Orion Research, Beverly, Massachusetts, USA). To compare temporal and spatial variation, we measured surface water and interstitial soil salinity on 5 March 1999, 6 June 2000, and 26 September 2000 at four I. hexagona sites. At each site we obtained salinity levels at three locations on a 7-m transect from the bank, as well as the surface water adjacent to the bank.
The common garden
We conducted two experiments to investigate the effects of salinity on I. hexagona flowering phenology. In March 1997, we established a common garden at the University of Louisiana Center for Ecology and Environmental Technology (CEET) in Carencro, Louisiana. We collected plants from ten widely separated sites on Marsh Island and planted them in 30 227-L plastic tubs filled with Mississippi alluvial topsoil. Tubs were large enough to prevent crowding of irises. We used Instant Ocean (Aquarium Systems, Mentor, Ohio, USA), a nitrate- and phosphate-free synthetic sea salt, to establish and maintain salinity levels in the supplemental salinity tubs, and the soil was kept saturated throughout the experiment. Salinity levels were recorded weekly and adjusted as necessary to maintain salinity treatments.
Experiment 1
This experiment tested the effects of site of collection and 12 mo of continuous exposure to salinity on I. hexagona flower phenology. Ten tubs each were randomly assigned to a low, medium, or high salinity treatment (0.2 ± 0.4 g/L, 2.0 ± 1.2 g/L, and 3.7 ± 1.8 g/L salinity, respectively; means ± 1 SE). The treatment salinities reflected island surface water salinity levels in the months when irises flower (Fig. 1). Each tub contained random combinations of marked plants from three sites, and each site (N = 10) x salinity (N = 3) combination was replicated three times. The low salinity tubs did not receive supplemental salt. Irises planted in the common garden in March 1997 flowered in April 1998. From 9 April until 26 April we monitored every flower produced and recorded the date of sepal opening. After flowering, plants remained in the salinity treatments until October 1998, when they were carefully excavated and placed in fresh water. Plants grew in fresh water for 2 mo and were then replanted into tubs for the second experiment.
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Data analysis
To examine the differences in flowering phenology, we used survival analysis with a Cox regression model, which conducts a chi-square test with one degree of freedom (SAS PROC PHREG, version 8.2; SAS Institute, 2001
). Effects of both salinity and collection site were included in the analyses. Survival analysis is commonly used for survival (Allison, 1995
; Hardin, Willers, and Wagner, 1996
), flowering (Fox, 1990a
,b
, 2001
), germination (Platenkamp and Shaw, 1993
; Fox, 2001
), and pollination data (Muenchow, 1986
). We employed the COVSANDWICH option of PHREG because it generates robust standard errors for nonindependent observations (Lee, Wei, and Amato, 1992
), such as flowers produced by a single stalk.
RESULTS
Field salinity levels
Water salinities vary monthly on Marsh Island in a consistent pattern. Water salinity data from one iris site are presented to illustrate temporal variation (Fig. 1). Salinity is lowest in the spring, averaging 2.8 ± 0.3 g/L in April when irises flower. The highest levels occur from August to November and average 8.0 ± 0.5 g/L. Interstitial soil salinity is higher than water salinity and also varies considerably (Fig. 2). Temporal and spatial variation within the 7-m site transects exceeded variation between the sites, which were separated by 1–5 km. Similar to water salinity, the lowest soil salinity occurs in the spring, which is the time of flowering for I. hexagona. The annual rise in salinity from 1997 to 2000 coincided with a drought in southern Louisiana, which ended in 2001.
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2 = 1.43, P = 0.23, df = 1; high vs. low 2 = 1.55, P = 0.21, df = 1; Fig. 3A). While flowering responses in plants collected from different sites were highly variable (maximum difference of 7 d; compare sites 6 and 7 in Fig. 3B), the ten sites did not differ significantly in the timing of flower production (2 = 2.15, P = 0.14, df = 1).
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2 = 5.22, P = 0.02, df = 1), where median flowering dates differed by as much as 3 d and the rate of flower opening was faster in lower salinities (Fig. 4). The delay in flowering phenology between the low and high groups was significant during this year (2 = 5.12, P = 0.024, df = 1, sequential Bonferroni 
= 0.025) and was in the same direction as the low and high treatments in experiment 1. A significant carryover effect is indicated by plants in the medlow treatment flowering later than plants in the low treatment (2 = 5.80, P = 0.016, df = 1, sequential Bonferroni = 0.017), suggesting that the saline environment of the previous year still affected plants in the medlow treatment. There was no significant delay between the high and medhigh salinity treatments (2 = 0.9, P = 0.34, df = 1, sequential Bonferroni = 0.05). As in experiment 1, plants from different sites did not differ in their pattern of flower production (2 = 0.27, P = 0.60, df = 1).
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Although other researchers have observed a delay in flowering with increased salinity levels (Blits and Gallagher, 1991
; Stanton, Roy, and Theide, 2000
), this is the first study we know of that experimentally tests the effect of salinity on the flowering phenology of a native wetland species. Iris hexagona is salt-sensitive but exhibits intraspecific variation in tolerance, as indicated by observations of mainland freshwater populations that exhibited drastic dieback due to storm-derived saltwater intrusion. Our study demonstrates that relatively low levels of salinity can delay flowering by as much as 3 d (Fig. 4). Salinity-induced flowering delays have been observed in wild mustard (Sinapis arvensis), an annual, non-wetland, salt-sensitive species (Stanton, Roy, and Theide, 2000
), as well as in the salt-tolerant marsh species Cakile edentula (Boyd and Barbour, 1986
) and Sporobolus virginicus (Blits and Gallagher, 1991
). Although little is known about how salinity stress shapes life history evolution of natural populations of glycophytes, there is some evidence that it can enhance evolutionary potential and genetic diversity (Stanton, Roy, and Theide, 2000
). This is certainly possible in I. hexagona, which, despite delayed flowering, produces significantly more seeds when exposed to increased salinity (Van Zandt, 2001
).
The impact of salinity stress
The effect of salinity on I. hexagona flowering phenology was both delayed and persistent. Although a significant salinity effect did not appear until the second year (experiment 2) of exposure (Fig. 4), the effects persisted in plants returned to freshwater conditions for 6 mo (the medlow group in experiment 2). This observation has particular relevance for coastal populations that typically experience wide variation in salinity (Adam, 1990
). Fluctuations in salinity can create windows of opportunity for sensitive developmental stages such as seeds (Houle et al., 2001
), but our study suggests that mature plants retain the effects of salinity even during periods of low stress.
A carryover effect on phenology could explain the lack of significant treatment differences in experiment 1. Since all plants were collected from saline environments, their phenological responses in the first experiment may have been more strongly influenced by natural site salinity than experimental salinity. Such a carryover effect was observed in the clonal sedge Eriophorum vaginatum, in which growth and clonal propagation were influenced by the parental environment, independent of plant mass (Schwaegerle, McIntyre, and Swingley, 2000
). Our study extends this observation by revealing that prior exposure to environmental stress can affect sexual traits of clonal plants. It also demonstrates the value of long-term experiments when examining performance in perennial plants, as a 1-yr experiment would have failed to reveal the strong I. hexagona responses to salinity that appeared in the second year.
Mechanisms of delayed phenology
Because salinity exerts multiple stresses on plants, including osmotic imbalance, nutritional deficits, and cellular toxicity (reviewed in Levitt, 1980
; Wang, Mopper, and Hasenstein, 2001
), it may be difficult to identify the specific mechanisms that alter life history shifts in important traits such as flowering phenology. One potentially important factor facilitating delayed flowering in I. hexagona could be reduced belowground biomass. Excavation of all common garden plants in October 1998 revealed that salinity-treated plants had a 30% reduction in belowground biomass compared to plants grown in low salinity (Van Zandt, 2001
). A reduction in energetic reserves of this magnitude could impede the development of floral structures and delay anthesis. However, salinity did not have a negative effect on the total number of flowers produced, and while plant biomass was positively correlated with flower number, it was not a strong predictor of flower production (r2 = 0.01–0.14; Van Zandt, 2001
).
Phytochemical analyses of irises in our common garden indicated that salinity strongly alters the concentration of hormones in flower stalks and other plant tissues (Wang, Mopper, and Hasenstein, 2001
). Both abscisic acid (ABA) and jasmonic acid (JA) were up-regulated in irises exposed to salinity (Wang, Mopper, and Hasenstein, 2001
). Jasmonic acid moderates the effects of salinity (Moons et al., 1997
) and osmotic stress (Creelman and Mullet, 1995
; Finch-Savage, Blake, and Clay, 1996
), as well as controls the opening of florets in rice (Zeng et al., 1999
). Similarly, ABA induces genes involved in osmotic stress protection (Serrano and Gaxiola, 1994
) and inhibits germination (Skriver and Mundy, 1990
; Baskin and Baskin, 1998
). Because these hormones are induced by salinity in I. hexagona and have known stress and reproductive functions, they may enable iris to flower despite the salinity stress, albeit with a slight delay. The increased seed production observed in the high salinity group (P. A. Van Zandt et al., unpublished manuscript) could also be a response to the elevated JA.
Consequences for individuals and populations
In the common garden experiment, small differences in salinity caused flowering asynchrony of several days. There is sufficient variation in soil salinity within natural I. hexagona populations (Fig. 2) to result in similar phenological delays. In fact, during the 19 April salinity measurement, individual irises at different sites displayed a mixture of reproductive stages, ranging from flower buds to newly opened flowers to developing seed capsules. Because flowering in I. hexagona coincides with seasonal lows in salinity (Fig. 1), phenological differences within sites may exceed differences between sites.
The timing of sexual reproduction is a critical component of plant life history that affects fitness (Schemske, 1977
; Marquis, 1988
), species interactions (Augspurger, 1981
; Evans, Smith, and Gendron, 1989
; English-Loeb and Karban, 1992
), and evolution (Primack, 1985
; Fox, 1990b
; O'Neil, 1997
). In freshwater I. hexagona populations that exhibit natural variation in flower availability, a greater number of available flowers was shown to increase outcrossing rates (Cruzan et al., 1994
). Since I. hexagona flowers are receptive to pollinators for 2 d or less (P. A. Van Zandt, unpublished data), a 3-d delay in flowering could eliminate gene flow between asynchronous plants. The levels of asynchrony produced by small differences in salinity could not only impact recombination opportunities, it could determine the effective size of the entire population. However, the importance of the salinity-mediated carryover effect demonstrated in this study could also moderate this effect.
Theory predicts that plant genotype and the environment determine patterns of sexual reproduction (Rathcke and Lacey, 1985
), but environmental forces can override genetic traits (Fox, 1990a
; Kelly, 1992
), even when selection for synchrony is strong (Augspurger, 1981
; O'Neil, 1997
). Consistent variation in salinity among sites would amplify existing genetic variation among isolated I. hexagona and further subdivide the populations genetically (Stanton, Galen, and Shore, 1997
). However, there is equal or greater variation in salinity within salt-marsh sites than between sites separated by substantial distance. Salinity appears to prevent reproductive synchrony among plants growing in proximity, which should promote genetic heterogeneity within iris populations and maintain genetic heterozygosity in stressful environments where adaptive plasticity is necessary for survival.
FOOTNOTES
1 We thank E. Bullard, G. Fox, and especially P. Savarese for providing SAS advice, and J. Smith, L. Schile, J. Singleton, K. Hasenstein, E. Milligan, S. Smyers, and M. Tobler for help with establishing and maintaining the experimental garden. Edmond Mouton and the State of Louisiana Department of Wildlife and Fisheries generously shared Marsh Island salinity data. Helpful comments from M. Peterson, J. Grace, K. Hasenstein, A. Agrawal, P. Leberg, J. Neigel, and two anonymous reviewers improved earlier versions of this manuscript. This research was supported by a UL Lafayette Ph.D. Fellowship, Sigma Xi Grants in Aid of Research, and an American Iris Society Scholarship to P.V.Z., and by National Science Foundation grants DEB-96-32302 and DEB-97-43938 to S.M. 
2 Author for correspondence and reprint requests, current address: Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, Ontario M5S 3B2, Canada (vanzandt{at}botany.utoronto.ca
)
LITERATURE CITED
Adam P. 1990 Salt marsh ecology. Cambridge University Press, Cambridge, UK
Allen J. A. J. L. Chambers S. R. Pezeshki 1997 Effects of salinity on baldcypress seedlings: physiological responses and their relation to salinity tolerance. Wetlands 17: 310-320[ISI]
Allison P. D. 1995 Survival analysis using the SAS system: practical guide. SAS Institute, Cary, North Carolina, USA
Arnold M. L. J. L. Hamrick B. D. Bennett 1993 Interspecific pollen competition and reproductive isolation in Iris. Journal of Heredity 84: 13-16
Augspurger C. K. 1981 Reproductive synchrony of a tropical shrub: experimental studies on effects of pollinators and seed predators on Hybanthus prunifolius (Violaceae). Ecology 62: 775-788[CrossRef][ISI]
Baskin C. C. J. M. Baskin 1998 Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, New York, New York, USA
Bennett B. D. J. B. Grace 1990 Shade tolerance and its effect on the segregation of two species of Louisiana iris and their hybrids. American Journal of Botany 77: 100-107[CrossRef][ISI]
Blits K. C. J. L. Gallagher 1991 Morphological and physiological responses to increased salinity in marsh and dune ecotypes of Sporobolus virginicus (L) Kunth. Oecologia 87: 330-335[CrossRef][ISI]
Boyd R. S. M. G. Barbour 1986 Relative salt tolerance of Cakile edentula (Brassicaceae) from lacustrine and marine beaches. American Journal of Botany 73: 236-241[CrossRef][ISI]
Bram M. R. J. A. Quinn 2000 Sex expression, sex-specific traits, and the effects of salinity on growth and reproduction of Amaranthus cannabinus (Amaranthaceae), a dioecious annual. American Journal of Botany 87: 1609-1618
Burke J. M. M. R. Bulger R. A. Wesselingh M. L. Arnold 2000 Frequency and spatial patterning of clonal reproduction in Louisiana iris hybrid populations. Evolution 54: 137-144[CrossRef][ISI][Medline]
Caillet M. J. K. Mertzweiller 1988 The Louisiana iris: the history and culture of five native American species and their hybrids. Texas Gardener Press, Waco, Texas, USA
Creelman R. A. J. E. Mullet 1995 Jasmonic acid distribution and action in plants: regulation during development and in response to biotic and abiotic stress. Proceedings of the National Academy of Sciences of the USA 92: 4114-4119
Cruzan M. B. M. L. Arnold 1993 Ecological and genetic associations in an Iris hybrid zone. Evolution 47: 1432-1445[CrossRef][ISI]
Cruzan M. B. J. L. Hamrick M. L. Arnold B. D. Bennett 1994 Mating system variation in hybridizing irises: effects of phenology and floral densities on family outcrossing rates. Heredity 72: 95-105[ISI]
English-Loeb G. R. Karban 1992 Consequences of variation in flowering phenology for seed head herbivory and reproductive success in Erigeron glaucus (Compositae). Oecologia 89: 588-595[ISI]
Evans E. E. C. C. Smith R. P. Gendron 1989 Timing of reproduction in a prairie legume: seasonal impacts of insects consuming flowers and seeds. Oecologia 78: 220-230[CrossRef][ISI]
Finch-Savage W. E. P. S. Blake H. A. Clay 1996 Desiccation stress in recalcitrant Quercus robur L. seeds results in lipid peroxidation and increased synthesis of jasmonates and abscisic acid. Journal of Experimental Botany 47: 661-667
Fox G. A. 1990a Components of flowering time variation in a desert annual. Evolution 44: 1404-1423[CrossRef][ISI]
Fox G. A. 1990b Drought and the evolution of flowering time in desert annuals. American Journal of Botany 77: 1508-1518[CrossRef][ISI]
Fox G. A. 2001 Failure-time analysis: studying times-to-events and rates at which events occur. In S. M. Scheiner and J. Gurevitch [eds.], Design and analysis of ecological experiments. Oxford University Press, Oxford, UK
Hardin J. M. J. L. Willers T. L. Wagner 1996 Nonparametric multiple comparisons of survivorship distributions. Journal of Economic Entomology 89: 715-721[ISI]
Hester M. W. I. A. Mendelssohn K. L. McKee 1998 Intraspecific variation in salt tolerance and morphology in Panicum hemitomon and Spartina alterniflora (Poaceae). International Journal of Plant Sciences 159: 127-138[CrossRef][ISI]
Houle G. H. L. Morel C. E. Reynolds J. Siegel 2001 The effect of salinity on different developmental stages of an endemic annual plant, Aster laurentianus (Asteraceae). American Journal of Botany 88: 62-67
Jackson M. T. 1966 Effects of microclimate on spring flowering phenology. Ecology 47: 407-415[CrossRef][ISI]
Kelly C. A. 1992 Reproductive phenologies in Lobelia inflata (Lobeliaceae) and their environmental control. American Journal of Botany 79: 1126-1133[CrossRef][ISI]
Krauss K. W. J. L. Chambers J. A. Allen D. M. Soileau Jr. A. S. DeBosier 2000 Growth and nutrition of baldcypress under varying salinity regimes in Louisiana, USA. Journal of Coastal Research 16: 153-163[ISI]
Lee E. W. L. J. Wei D. Amato 1992 Cox-type regression analysis for large number of small groups of correlated failure time observations. In J. P. Klein and P. K. Goel [eds.], Survival analysis, state of the art, 237–247. Kluwer Academic, Dordrecht, The Netherlands
Levitt J. 1980 Responses of plants to environmental stresses, vol. II. Academic Press, New York, New York, USA
Marquis R. J. 1988 Phenological variation in the neotropical understory shrub Piper arieianum: causes and consequences. Ecology 69: 1552-1565[CrossRef][ISI]
Moons A. E. Prisen G. Bauw M. V. Montagu 1997 Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell 92: 243-259
Muenchow G. 1986 Ecological use of failure time analysis. Ecology 67: 246-250[CrossRef][ISI]
O'Neil P. 1997 Natural selection on genetically correlated phenological characters in Lythrum salicaria L. (Lythraceae). Evolution 51: 267-274[CrossRef][ISI]
Pezeshki S. R. R. D. DeLaune W. H. Patrick Jr 1990 Flooding and saltwater intrusion: potential effects on survival and productivity of wetland forests along the US Gulf Coast. Coastal Forest Ecology Management 33/34: 287-301
Pilson D. 2000 Herbivory and natural selection on flowering phenology in wild sunflower, Helianthus annuus. Oecologia 122: 72-82[CrossRef][ISI]
Platenkamp G. A. J. R. G. Shaw 1993 Environmental and genetic maternal effects on seed characters in Nemophila menziesii. Evolution 47: 540-555[CrossRef][ISI]
Price M. V. N. M. Waser 1998 Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology 79: 1261-1271[CrossRef][ISI]
Primack R. B. 1985 Patterns of flowering phenology in communities, populations, individuals, and single flowers. In J. White [ed.], The population structure of vegetation, 571–593. Dr. W. Junk, Dordrecht, The Netherlands
Rathcke B. E. P. Lacey 1985 Phenological patterns of terrestrial plants. Annual Review of Ecology and Systematics 16: 179-214[CrossRef][ISI]
Sandvik S. M. O. Totland 2000 Short-term effects of simulated environmental changes on phenology, reproduction, and growth in the late-flowering snowbed herb Saxifraga stellaris L. Ecoscience 7: 201-213[ISI]
SAS Institute. 2001 SAS/STAT software; version 8.2. SAS Institute, Cary, North Carolina, USA
Schemske D. W. 1977 Flowering phenology and seed set in Claytonia virginica (Portulacaceae). Bulletin of the Torrey Botanical Club 104: 254-263[CrossRef][ISI]
Schwaegerle K. E. H. McIntyre C. Swingley 2000 Quantitative genetics and the persistence of environmental effects in clonally propagated organisms. Evolution 54: 452-461[ISI][Medline]
Seliskar D. M. J. L. Gallagher 2000 Exploiting wild population diversity and somaclonal variation in the salt marsh grass Distichlis spicata (Poaceae) for marsh creation and restoration. American Journal of Botany 87: 141-146
Serrano R. R. Gaxiola 1994 Microbial models and salt stress tolerance in plants. Critical Reviews in Plant Sciences 13: 121-138
Shitaka Y. T. Hirose 1998 Effects of shift in flowering time on the reproductive output of Xanthium canadense in a seasonal environment. Oecologia 114: 361-367[CrossRef][ISI]
Skriver K. J. Mundy 1990 Gene expression and response to abscisic acid and osmotic stress. Plant Cell 2: 503-512
Stanton M. L. C. Galen J. Shore 1997 Population structure along a steep environmental gradient: consequences of flowering time and habitat variation in the snow buttercup, Ranunculus adoneus. Evolution 51: 79-94[CrossRef][ISI]
Stanton M. L. B. A. Roy D. A. Thiede 2000 Evolution in stressful environments. I. Phenotypic variability, phenotypic selection, and response to selection in five distinct environmental stresses. Evolution 54: 93-111[CrossRef][ISI][Medline]
Twilley R. R. E. J. Barron H. L. Gholz M. A. Harwell R. L. Miller D. J. Reed J. B. Rose E. H. Siemann R. G. Wetzel R. J. Zimmerman 2001 Confronting climate change in the Gulf Coast region. Prospects for sustaining ecological heritage. Union of Concerned Scientists, Cambridge, Massachusetts, and Ecological Society of America, Washington, D.C., USA
Van Zandt P. A. 2001 The ecological and evolutionary responses of Iris hexagona to salinity stress. Ph.D. dissertation, University of Louisiana at Lafayette, Lafayette, Louisiana, USA
Viosca P., Jr. 1935 The irises of southeastern Louisiana: a taxonomic and ecological interpretation. Journal of the American Iris Society 57: 3-56
Wang Y. S. Mopper K. H. Hasenstein 2001 Effects of salinity on endogenous levels of ABA, IAA, JA, and SA in Iris hexagona. Journal of Chemical Ecology 27: 327-342[CrossRef][ISI][Medline]
Zeng X. C. X. Zhou W. Zhang N. Murofushi T. Kitahara Y. Kamuro 1999 Opening of rice floret in rapid response to methyl jasmonate. Journal of Plant Growth Regulators 18: 153-158
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