flowering and biomass allocation in u.s. atlantic coast spartina alterniflora

1

American Journal of Botany 102 ( 5 ): 1 – 676 , 2015 ; http://www.amjbot.org/ © 2015 Botanical Society of America

A M E R I C A N J O U R N A L O F B OTA N Y R E S E A R C H A R T I C L E

Salt marshes are one of the most common intertidal habitats on the U.S. Atlantic and Gulf coasts, providing many valuable ecosystem services ( Chapman, 1960 ; Costanza et al., 2008 ; Barbier et al., 2011 ). Despite their importance, they are threat-ened by both direct and indirect human impacts such as ditch-ing, fi lling, impounding, and eutrophication ( Bromberg and Bertness, 2005 ; Gedan, Silliman, and Bertness, 2009 ; Deegan

et al., 2012 ). On the U.S. Atlantic coast, Spartina alternifl ora Loisel (smooth cordgrass) is the species responsible for ini-tial salt marsh colonization and the ongoing maintenance of the seaward edge of established salt marshes ( Redfi eld, 1972 ; Bertness, 1991 ; Bertness and Hacker, 1994 ). Like many aquatic plants, S. alternifl ora reproduces both through water-dispersed seeds and clonally via belowground rhizomes. It has generally

1 Manuscript received 5 December 2014; revision accepted 22 April 2015.

The authors thank A. Angermeyer, L. Brin, H. Booth, J. Carlton, A. Crosby, J. Gallagher, D. Johnson, R. Johnson, E. Lamb, M. Palmer, K. Raposa, D. Sax, D. Seliskar, E. Watson, C. Weidman, C. Wigand, and the staff at Rhode Island Medical Imaging, Waquoit Bay National Estuarine Research Reserve, Prudence Island National Estuarine Research Reserve, St. Jones River National Estuarine Research Reserve, Fire Island National Seashore, Assateague Island National Seashore, Rachel Carson National Estuarine Research Reserve, ACE Basin National Estuarine Research Reserve, and the Plum Island Long-Term Ecological Research Program for their invaluable assistance. This work was supported in part by an Ecology and Evolutionary Biology Dissertation Development Grant through Brown University to S.C.C. This research (or a portion thereof) was conducted in the National Estuarine Research Reserve System under an award from

FLOWERING AND BIOMASS ALLOCATION IN U.S. ATLANTIC COAST SPARTINA ALTERNIFLORA 1

SARAH C. CROSBY 2,3,6 , MORGAN IVENS-DURAN 2,7 , MARK D. BERTNESS 2 , EARL DAVEY 4 , LINDA A. DEEGAN 2,3 , AND HEATHER M. LESLIE 2,3,5

2 Brown University, Ecology and Evolutionary Biology, Box G-W, Providence, Rhode Island 02912 USA; 3 Marine Biological Laboratory, Ecosystems Center, 7 MBL Street, Woods Hole, Massachusetts 02543 USA; 4 U.S. EPA, Offi ce of Research and

Development, National Heath and Environmental Effects Research Laboratory, Atlantic Ecology Division, Narragansett, Rhode Island 02882 USA; and 5 Brown University, Institute at Brown for Environment and Society, Box 1951, 85 Waterman Street,

Providence, Rhode Island 02912 USA

• Premise of the study: Salt marshes are highly productive and valuable ecosystems, providing many services on which people depend. Spartina alternifl ora Loisel (Poaceae) is a foundation species that builds and maintains salt marshes. Despite this spe-cies’ importance, much of its basic reproductive biology is not well understood, including fl owering phenology, seed produc-tion, and the effects of fl owering on growth and biomass allocation. We sought to better understand these life history traits and use that knowledge to consider how this species may be affected by climate change.

• Methods: We examined temporal and spatial patterns in fl owering and seed production in S. alternifl ora at a latitudinal scale (along the U.S. Atlantic coast), regional scale (within New England), and local scale (among subhabitats within marshes) and determined the impact of fl owering on growth allocation using fi eld and greenhouse studies.

• Key results: Flowering stem density did not vary along a latitudinal gradient, while at the local scale plants in the less sub-merged panne subhabitats produced fewer fl owers and seeds than those in more frequently submerged subhabitats. We also found that a shift in biomass allocation from above to belowground was temporally related to fl owering phenology.

• Conclusions: We expect that environmental change will affect seed production and that the phenological relationship with fl owering will result in limitations to belowground production and thus affect marsh elevation gain. Salt marshes provide an excellent model system for exploring the interactions between plant ecology and ecosystem functioning, enabling better predic-tions of climate change impacts.

Key words: biomass allocation; fl owering; phenology; seed supply; Spartina alternifl ora .

the Estuarine Reserves Division, Offi ce of Ocean and Coastal Resource Management, National Ocean Service, National Oceanic and Atmospheric Administration to S.C.C. Additional funding was provided to S.C.C. by the National Park Service George Melendez Wright Climate Change Fellowship, to H.M.L. from the ADVANCE Program of Brown University (National Science Foundation Grant no. 0548311), and to L.A.D. from the National Science Foundation (DEB-1354494, OCE-1238212) and the Northeast Climate Science Center (DOI-G12AC00001, DOI-G13AC00410).

6 Author for correspondence (e-mail: [email protected]). Current address: Harbor Watch, Earthplace, The Nature Discovery Center, Westport, Connecticut 06880, USA

7 Current address: Biological Sciences, California Polytechnic State University, San Luis Obispo, California 93407, USA

doi:10.3732/ajb.1400534

http://www.amjbot.org/cgi/doi/10.3732/ajb.1400534The latest version is at AJB Advance Article published on May 20, 2015, as 10.3732/ajb.1400534.

Copyright 2015 by the Botanical Society of America

http://www.amjbot.org/cgi/doi/10.3732/ajb.1400534

2 • V O L . 1 0 2 , N O. 5 M AY 2 0 1 5 • A M E R I C A N J O U R N A L O F B OTA N Y

been presumed that asexual reproduction predominates in salt marshes and that their plant populations are composed of a limited number of clones ( Richards et al., 2004 ), but studies demonstrating high levels of genetic diversity indicate the sig-nifi cance of seedling establishment in S. alternifl ora popula-tions ( Richards et al., 2004 ; Travis et al., 2004 ). Despite its importance, several critical characteristics of this species’ life history are not well understood, including the timing, magni-tude, and spatial variation in seed production and the allocation of biomass to growth, as well as its clonal and sexual modes of reproduction. Because of the role this species plays in marsh creation and maintenance, understanding growth and reproduc-tion in S. alternifl ora is crucial for predicting where marshes may be gained or lost in the future.

Like all organisms, S. alternifl ora undergoes trade-offs in en-ergy allocation between competing physiological processes (e.g., growth and reproduction) and between different repro-ductive modes ( Levins, 1968 ). As temperatures increase, salt marshes are predicted to be more productive ( Turner, 1976 ; Kirwan et al., 2009 ). However, it is not known how increased production will be allocated between growth and reproduction, or how temperature effects on phenology might infl uence growth allocation. Marsh elevation is maintained by S. alterni-fl ora as its aboveground biomass slows tidal water and in-creases sediment deposition ( Redfi eld, 1972 ; Stumpf, 1983 ) while its belowground growth builds up, over time, as peat ( Bricker-Urso et al., 1989 ; Turner et al., 2000 ). As the growing season lengthens and temperatures rise, there is potential for increased productivity either above or below ground (or both), but it is not yet clear how biomass will be allocated between these competing modes.

Phenological events, such as the timing of fl owering, are of-ten initiated by environmental cues, including threshold tem-peratures ( Seneca and Broome, 1972 ; Seneca and Blum, 1984 ). Thus, shifts in plant phenology are expected with climate change ( Cleland et al., 2007 ; Steltzer and Post, 2009 ). Stress-induced fl owering also occurs in many plant species ( Wada and Takeno, 2010 ; Takeno, 2012 ), and the magnitude of stress expe-rienced by S. alternifl ora is expected to increase, including heat and edaphic stress resulting from rising temperatures ( Stocker et al., 2013 ). However, it is not yet known how these environ-mental changes might affect multiple aspects of S. alternifl ora biology.

The goals of the present study were to (1) quantify temporal and spatial patterns in S. alternifl ora fl owering and seed pro-duction and (2) determine the relationship between fl owering phenology and aboveground versus belowground biomass al-location. Spartina alternifl ora is found in many salt marsh sub-habitats, including creek banks, intermediate marsh elevations (such as the banks of ditches and upland of creeks) and high-marsh pannes. Submergence frequency differs among these subhabitats, which can drive variations in soil salinity and tem-perature ( Pennings and Bertness, 2001 ). Further, the geographic range of S. alternifl ora spans the U.S. Atlantic coast from Maine to Florida, providing a unique opportunity to consider trends in fl owering across a large natural temperature gradient where both growing-season length and environmental condi-tions vary. We hypothesized that the onset and extent of sexual reproduction in S. alternifl ora was correlated to environmental gradients across marshes and that this variation would drive dif-ferences in the magnitude of reproductive potential among marshes and marsh subhabitats. We further predicted that (1) fl owering phenology would be related to temporal trends in the

allocation of biomass, (2) the cessation of aboveground alloca-tion would coincide with fl ower production, and (3) allocation of belowground biomass would occur primarily after fl ower production. We used a multiscale approach, including investi-gation of fl owering time and magnitude along the U.S. Atlantic coast (latitudinal scale), across New England marshes (regional scale), and among subhabitats within a marsh (local scale), and we coupled these surveys with a greenhouse mesocosm ex-periment to study fl owering phenology. Finally, we quantifi ed temporal changes in aboveground and belowground biomass allocation using multiple analytical techniques (including re-peated CT scans of living plants and fi eld surveys) to determine the allocation to elevation-building belowground biomass lead-ing up to, during, and following fl owering.

MATERIALS AND METHODS

Latitudinal-scale fl owering phenology and magnitude — In the fi eld, the density of fl owering stems was quantifi ed in 2010 and 2011 at eight salt marshes along a 9 ° latitudinal gradient from Massachusetts to South Carolina, USA (Waquoit Bay, Massachusetts [MA]: 41.580 ° N, 70.521 ° W, Prudence Island, Rhode Island [RI]: 41.625 ° N, 71.324 ° W, Fire Island, New York [NY]: 40.689 ° N, 72.992 ° W, Dover, Delaware [DE]: 39.089 ° N, 75.437 ° W, Lewes, DE: 38.788 ° N, 75.167 ° W, Assateague Island, Maryland [MD]: 38.201 ° N, 75.162 ° W, Beaufort, North Carolina [NC]: 34.723 ° N, 76.675 ° W, and Bennett’s Point, South Carolina [SC]: 32.558 ° N, 80.439 ° W). Within intermediate height-form (40–50 cm) S. alternifl ora monocultures ≥ 1 m away from a creek, we counted the number of stems and fl owering stems ( n = 8 per site, in 0.25-m 2 quadrats spaced ≥ 1 m apart) and measured the heights of 10 randomly selected stems per plot. Each of the eight marshes studied experiences semidiurnal tides. We standardized the sampling area at each marsh by submergence frequency, such that the S. alter-nifl ora monocultures sampled at each were submerged <20% of the time per tidal cycle. Submergence frequency at each site was quantifi ed by measuring tidal height above the marsh surface at high tide in the sampling area, compar-ing the height of the water at high tide to the nearest available tide gauge, and then using the water heights and tide gauge data to determine the amount of time that that area of the marsh is submerged per tidal cycle. All areas sampled within each of the eight marshes thus experienced similar submergence fre-quency even when tidal range and marsh slope differed.

A mesocosm study to quantify fl owering phenology and magnitude using plants from a subset of the latitudinal gradient of marshes was also conducted in a greenhouse at Brown University during March–October 2010. Cores of S. alter-nifl ora ( n = 8) were collected for the experiment from fi ve marshes (our MA, RI, DE [Dover], NC, and SC sites) in March 2010. An 8-cm-diameter manual sedi-ment corer with a serrated edge was used to collect the plants to a depth of 20 cm, taking care to preserve aboveground shoots. Cores were taken ≥ 0.5 m apart. The individual plugs with the surrounding sediment were then planted in individual, uniquely identifi ed PVC pots with potting soil. These plants were fl ooded (to 5 cm above the soil surface) and drained with 15 ppt salt water daily. The duration of the simulated high tide was ~1 hr. This once-daily fl ooding differed from the two daily high tides experienced by the plants in their source populations. We quantifi ed the density and height of stems in each pot every 2 wk.

Regional and local-scale fl owering phenology and magnitude — Surveys were also conducted in 2011 at three New England salt marshes separated by <140 km (Site 1: Prudence Island, RI; Site 2: Waquoit Bay, MA; and Site 3: Plum Island, MA) to consider the impact of local-scale (i.e., within-marsh) dif-ferences in inundation and resulting edaphic conditions on reproduction. At each of these marshes, 10 permanent 1-m 2 plots were established in each of four S. alternifl ora subhabitats (creek-bank, ditch-bank, intermediate, and panne) using a stratifi ed random design. Plots at each site were located within an area of <2 ha, and all plots were ≥ 2 m apart. These subhabitats were selected for study because of differences in submergence frequency and duration resulting from within-marsh elevation gradients. Creek-bank subhabitats are most fre-quently submerged, the intermediate and ditch-bank subhabitats experience intermediate submergence, and the high-marsh panne subhabitats are sub-merged the least frequently ( Pennings and Bertness, 2001 ).

These New England–focused surveys were conducted every 2 wk in June and July, weekly in August (during observed peak fl owering period), and once

S PA R T I N A A LT E R N I F LO R A F LO W E R I N G A N D B I O M A S S • V O L . 1 0 2 , N O. 5 M AY 2 0 1 5 • 3

each in September and October. These surveys were designed to quantify within-marsh, across-marsh, and across-season differences in fl owering. Dur-ing each survey, the 40 plots per marsh were sampled for stem density (stems/10 cm 2 ) and stem height of 10 randomly selected stems. When fl owers were pres-ent, total infl orescence density (fl owering stems/m 2 ) and the height and infl o-rescence length of up to 10 randomly selected fl owering stems were measured. Infl orescence length (cluster of seed-forming spikelets at the top of each fl ower-ing stem) was measured from the base of the fi rst spike to the tip of the highest spike as a proxy for seed production ( Mullins and Marks, 1987 ).

Biomass allocation laboratory study — In May 2013, at the start of the growing season, 30 individual cores were collected from a monospecifi c, inter-mediate height-form (40–50 cm) swath of S. alternifl ora from Prudence Island, RI (with a minimum spacing of 0.5 m between samples). As in the 2010 meso-cosm study, an 8-cm-diameter manual corer was used and the cores were planted in individual, uniquely identifi ed 16-cm PVC pots with potting soil. One PVC pot fi lled with only the soil matrix (soil blank) was used as a control for the CT-scan image analysis (described below). The plants were grown for 6 mo in a greenhouse mesocosm (located at the Environmental Protection Agency Atlantic Ecology Division in Narragansett, RI) and fl ooded and drained twice daily with local seawater. The inundation regime differed between the 2010 and 2013 mesocosm studies, with the 2013 study more closely approximating the natural inundation regime of the source marshes (semidiurnal).

Growth in S. alternifl ora was measured over the course of the local growing season to determine the impact of fl owering phenology on aboveground and belowground biomass allocation. Biomass was quantifi ed using both nonde-structive laboratory-based and destructive fi eld-based methods. First, using CT scans of sediment cores, we made repeated belowground biomass measure-ments on the same live plants grown in the greenhouse over the course of the 2013 summer season, which enabled us to tightly correlate belowground pro-duction to aboveground reproductive phenology. This approach allowed us to quantify belowground biomass through time without disturbing the growing plants ( Perez et al., 1999 ; Davey et al., 2011 ). By using this method, we could also more precisely track biomass allocation in the plants, thereby reducing the effect of intramarsh spatial variability associated with destructive fi eld sam-pling. This method allowed for greater precision because it allowed repeated measurements on the same plants over time, whereas fi eld studies using tradi-tional destructive sampling methods require the use of different plants at each biomass measurement.

Every 2 wk from June to October, 12 of the potted cores were removed at “low tide,” transported to a scanning facility (Rhode Island Medical Imaging), CT-scanned, and then returned to the greenhouse. This entire process took ~4 hr. The same 12 cores were scanned each time so that belowground biomass could be tracked for each plant throughout the growing season and related to the aboveground phenology of each pot. The remaining 18 potted cores were not scanned and served as controls to determine the impact of the transport and CT scan on growth. The densities of live and dead stems, the height of fi ve ran-domly selected stems, the density of fl owers, and infl orescence length of each fl owering stem were quantifi ed for each core monthly during the experiment. After the last CT scan in late September, all plants were removed from their pots, aboveground biomass was clipped from the top of each core, and the be-lowground core was separated into 10-cm sections with depth. Each below-ground section and the aboveground biomass were washed over a 2-mm mesh sieve, manually separated into live and dead components, dried to a constant mass (at 60 ° C), and measured to the nearest 0.01 g.

CT-scan data were analyzed to quantify belowground biomass in each core over time. CT scans of the sediment cores produce a digital image based on core material density differences ( Perez et al., 1999 ). Calibration rods of known den-sity were inserted into a subset of fi ve cores during the CT scanning (following Davey et al., 2011 ). These rods were used to digitally calibrate the images and allow the volume of roots and rhizomes to be calculated. After the scanned im-ages were cropped to remove the PVC pot and rods from the images, the calibra-tion rods were analyzed (OsiriX version 5.7.1 64-bit, Pixmeo Sarl) and the total volumes of live roots and rhizomes were quantifi ed from the cropped images us-ing ImageJ ( Rasband, 2014 ; again following Davey et al. (2011)) . The scanned and analyzed soil blank was used to remove any volumetric contributions of the surrounding soil matrix from the calculated root and rhizome volumes.

Biomass allocation fi eld study — To complement the laboratory study de-scribed above, we also quantifi ed aboveground and belowground plant biomass from sediment cores ( n = 10; diameter = 8 cm, depth = 20 cm) taken biweekly from an intermediate-height S. alternifl ora monoculture at Waquoit Bay (Falmouth, MA)

during June–September 2011, with a minimum spacing of 0.5 m between samples. Prior to the observed initiation of fl owering, 10 cores were taken per sampling. Once fl owering began, cores were taken from within fl owering ( n = 10) and non-fl owering ( n = 10) patches. These cores were washed, sorted, dried, and measured for biomass in the laboratory using the same destructive biomass techniques as those described above to generate a time-series of belowground biomass data in relation to the onset of fl owering. Because stems were selected for harvest ran-domly in the fi eld, individual plants were not tracked for phenological changes over time. Consequently, we did not know the timing of fl ower initiation for the plants sampled in the fi eld as precisely as we did for the CT-scanned plants.

Data analysis — The data were tested for the appropriate statistical assump-tions and analyzed in JMP version 10 (SAS Institute, Cary, NC). Linear regres-sion was used to test for a relationship between fl owering stem density and site latitude, and between fl owering stem height and infl orescence size. Analysis of variance (ANOVA) was used to test for differences among sites in the proportion of fl owering stems in the mesocosm experiment (arcsine transformation applied for normality). For the proportion and density of fl owering stems in the fi eld sur-veys and the time series of stem height and biomass allocation (CT scan and fi eld) data, a rank-transformed ANOVA ( Conover and Iman, 1981 ) was used because we could not achieve a normal distribution with the data after applying multiple traditional transformations. Means ± SE are reported throughout.

RESULTS

Latitudinal-scale fl owering phenology and magnitude — The latitudinal fi eld survey revealed no relationship (using linear re-gression) between mean density of fl owering stems and site lati-tude (2010: y = 0.58 × + 7.24; F 1, 6 = 0.047, P = 0.84, R 2 = 0.009; 2011: y = 1.23 × − 23.45; F 1, 6 = 0.326, P = 0.59, R 2 = 0.05). An outlier from Assateague Island, MD, in 2010 (162 ± 26.8 fl ower-ing stems m −2 ) was not included in the analysis. Northern marsh S. alternifl ora (from MA, RI, and Dover, DE) fl owered earlier than plants from more southern marshes (from NC and SC) in the 2010 mesocosm experiment, and a greater proportion of the north-ern plants had fl owered by the end of September 2010 ( Fig. 1 ) .

Fig. 1. Proportion of pots ( n = 8) of Spartina alternifl ora with fl owering stems in a greenhouse mesocosm from fi ve salt marshes on a latitudinal gradi-ent along the U.S. Atlantic coast (Waquoit Bay, MA; Prudence Island, RI; Do-ver, DE; Beaufort, NC; and Bennett’s Point, SC; see text) during summer 2010. Sampling dates were not evenly spaced and have been condensed.


Plants from RI began fl owering in early July, and fl owering for MA and DE plants began in early August. Plants from NC and SC did not fl ower until the end of September. Among the repli-cates that fl owered in the greenhouse, we did not detect a differ-ence among marshes in the proportion of fl owering stems (arcsine-transformed ANOVA; F 4, 19 = 2.50, P = 0.09). In the 2010 mesocosm, the mean stem heights across the sites were 46.5 ± 3.9 cm for MA, 58.4 ± 3.2 cm for RI, 75.2 ± 4.4 cm for DE, 74.4 ± 8.6 cm for NC, and 78.8 ± 7.1 cm for SC. The mean live stem densities were 22 ± 2.2 stems per core for MA, 13.1 ± 1.9 stems for RI, 10.1 ± 1.4 stems for DE, 6.4 ± 0.8 stems for NC, and 5.5 ± 0.7 stems for SC.

Local and regional-scale fl owering phenology and magni-tude — In the local and regional fi eld surveys, the proportion (rank-transformed ANOVA; F 11, 106 = 9.20, P < 0.0001) and density of fl owering stems (rank-transformed ANOVA; F 11, 106 = 8.66, P < 0.0001) varied among subhabitats and across marshes within New England at the end of September 2011 ( Fig. 2 ) . At sites 2 and 3, creek-bank subhabitats had the highest proportion and density of fl owering stems. At Site 1, fewer fl owers tended to be observed across all subhabitats than at Sites 2 and 3. Also, all of the Site 1 subhabitats had a similar proportion of fl owering stems and density of fl owers. Across all three marshes, there was a positive linear relationship between the height of fl owering stems and infl orescence size ( y = 0.13 ×

+ 5.75; F 1, 200 = 380.99, P < 0.0001, R 2 = 0.66), which we used as a proxy for seed production ( Fig. 3 ) . Taller stems (primarily found on creek banks) had larger infl orescences, which sug-gests that they produced more seeds ( Mullins and Marks, 1987 ) than shorter stems (primarily found in pannes).

We observed differences in the timing of fl owering within and among northern marshes in the fi eld ( Table 1 ) . Timing of the onset of fl owering was most different at the local scale be-tween the creek-bank and high-marsh panne subhabitats at Site 1, where fl owering occurred in the panne subhabitats >1 mo earlier than in the creek-bank subhabitats. Less within-marsh variation was found at Site 2 (where fl owering occurred in the panne and creek-bank subhabitats at the same time) and Site 3 (where fl owering in the creek-bank subhabitats preceded fl ow-ering in the panne subhabitats by ~2 wk). Although the timing of the fi rst appearance of fl owers varied, all subhabitats in all three of the New England marshes had fl owering plants by mid-August ( Table 1 ).

Aboveground and belowground biomass allocation — We observed a decrease in belowground biomass between late June and late July, consistent with translocation for aboveground green-up ( Fig. 4 ) . Later in the season, when fl owering began, we observed coincident increases in belowground biomass. We found similar patterns in biomass in the fi eld and greenhouse plants ( Fig. 4 ). The differences we observed among the fi eld belowground biomass measurements over time were not sig-nifi cant (rank-transformed ANOVA; F 6, 52 = 1.63, P > 0.05, R 2 = 0.18). However, signifi cant differences were found among the CT-scanned plants (rank-transformed ANOVA; F 6, 48 = 17.00, P < 0.0001, R 2 = 0.71). Temporal changes in the relationship between mean stem height and root and rhizome volume were also tracked in the greenhouse plants ( Fig. 5 ) . Signifi cant differences were found, over time, in the percent change in bio-mass for the CT-scanned plants (rank-transformed ANOVA;

Fig. 2. Differences in Spartina alternifl ora fl owering in four subhabitats at three marshes in New England, USA, at the end of September 2011. Site 1 was located in Prudence Island, RI; Site 2 was located in Waquoit Bay, MA; and Site 3 was located in Plum Island, MA (see text). (A) Proportion of stems with fl owers (rank-transformed ANOVA; F 11, 106 = 9.20, P < 0.0001). (B) Density of fl owering stems (rank-transformed ANOVA; F 11, 106 = 8.66, P < 0.0001). Letters indicate signifi cantly different pairs (Tukey-Kramer HSD test; P < 0.05). Error bars represent SE.

Fig. 3. The mean Spartina alternifl ora infl orescence length vs. mean fl ow-ering stem height at three marshes in New England, USA, including four sub-habitat types (creek bank, intermediate, ditch bank, panne). Linear regression revealed a signifi cant relationship between stem height and the length of the infl orescence ( y = 0.13 × + 5.75; F 1, 200 = 380.99, P < 0.0001, R 2 = 0.66). Error bars represent SE.


F 5, 41 = 26.99, P < 0.0001, R 2 = 0.79) and in the percent change in stem height (rank-transformed ANOVA; F 4, 34 = 19.82, P < 0.0001, R 2 = 0.73). The greatest increase in belowground growth was observed at the fi rst time point after fl owering, which was also when stem height change dropped to zero ( Fig. 5 ). The largest increases in stem height occurred early in the growing season; and after fl owering, the stems did not grow taller.

DISCUSSION

Using a combination of fi eld and greenhouse studies, we quantifi ed S. alternifl ora fl owering variation along the U.S. At-lantic coast and determined how fl owering phenology is related to temporal shifts in biomass allocation. Here, we focus on these local to latitudinal patterns and their potential relationship with seed production. We then explore the resulting implica-tions for genetic diversity, as well as the potential implications of these patterns in fl owering and biomass allocation on the fu-ture resilience of these ecosystems.

Flowering magnitude — We did not observe variation in the density of fl owers with latitude, despite higher southern temperatures and latitudinal differences in day length over the growing season. The absence of a latitudinal difference could be due to the fact that our study was conducted in the intermediate height-form of S. alternifl ora , which may have narrowed the possible response effect. The intermediate height-form is fl ooded regularly, and thus the typically higher-stress edaphic conditions seen in the higher elevations of warmer southern marshes may have been dampened. We do not know whether there were differences in clone size with latitude, or in the number of flowering stems produced per clone, that might have affected seed viability along this gradient. How-ever, previous work by Daehler and Strong (1994) found no

difference in reproductive success between culms in large and small clones.

On the local scale, fl owering also differed along environmen-tal gradients, although not in a consistent pattern at all sites. At Sites 2 and 3, we found an increased density of fl owers and greater proportion of fl owering stems in the more frequently sub-merged (i.e., lower edaphic stress) subhabitats ( Fig. 2 ). Spartina alternifl ora found in the higher-stress pannes is a stunted growth-form compared with plants in lower-elevation subhabitats, and we found that these shorter stems produced smaller infl orescences (i.e., suggesting fewer seeds). The creek bank plants produced a higher density of fl owers and also produced larger infl orescences on each fl owering stem ( Fig. 3 ). As a result, plants found in high-stress subhabitats may have contributed fewer seeds per unit area than other zones in the marsh. Work by Mullins and Marks (1987) found a similar relationship in the congener S. anglica , where areas of the marsh with taller fl owering stems produced longer infl orescences and more seeds.

The magnitude of fl ower and seed production varied both within and across the three New England marshes. Flowering occurred in <5% of the stems across all Site 1 subhabitats, and the maximum proportion of fl owering stems in any marsh subhabitat was <25% ( Fig. 2 ). A low proportion was similarly observed in our latitudinal surveys. The average proportion of fl owering stems in the intermediate height-form across the 8 study sites was 6.5 ± 2.5% in October 2010 and 2.5 ± 0.8% in October 2011. A low proportion of fl owering stems is similarly seen in Spartina foliosa × alternifl ora hybrids ( Ayres et al., 2008 ), as well as in Phragmites australis ( McKee and Richards, 1996 ). Spartina alternifl ora can produce >2000 seeds/m 2 ( Callaway and Josselyn, 1992 ), though many of the seeds produced are not viable ( Fang, 2002 ). Large reproductive output is similarly observed in other aquatic plants, such as seagrass ( Silberhorn et al., 1996 ) and mangroves ( Clarke, 1992 ). Ocean-dispersal-based life history strategies such as these tend to favor the production of

TABLE 1. Mean density of Spartina alternifl ora fl owering stems (SE below each in parentheses) at 10 permanent plots in each of four marsh subhabitats at three northern marshes ( n = 120 plots per marsh). Site 1 was located in Prudence Island, RI; Site 2 was located in Waquoit Bay, MA; and Site 3 was located in Plum Island, MA, USA (see text).

Study site Plot type Late June Early July Late July August week 1 August week 2 August week 3 August week 4 Late September

Site 1 Creek 0 0 0 0 0 3.1 11.6 43.2(1.5) (4) (12.3)

Intermediate 0 0 0 0 0.9 5.5 15.4 27.4(0.4) (2.4) (6) (9.2)

Ditch 0 0 0 0 1.5 5.2 7.1 32.4(1.1) (4.7) (3.1) (15.1)

Panne 0 4.7 4.7 6.5 22.5 62.4 67.7 96.4(0.3) (2.6) (2.1) (6.3) (18.5) (17.6) (29.9)

Site 2 Creek 0 0 0 4.6 23.2 77.6 83.2 312(2.6) (9) (26.2) (17.7) (60)

Intermediate 0 0 0 0 0 4.4 24.4 64.8(1.4) (6.2) (31.1)

Ditch 0 0 0 0 0.5 8.9 14.5 65.5(0.4) (4.7) (4.5) (12.6)

Panne 0 0 0 0.5 3.8 12.3 22 67.2(0.3) (1.5) (2.9) (4.1) (13.7)

Site 3 Creek 0 0.4 15.5 26.4 38 144.5 89.5 173(0.4) (12.3) (16.1) (12.3) (29.2) (8.6) (18)

Intermediate 0 0.7 24.8 28.6 60.4 121.3 90.7 116(0.7) (11) (9.1) (16.7) (25.4) (14.3) (15.1)

Ditch 0 0 0 1.2 0.6 22 21.4 35.2(1.2) (0.6) (19.8) (11.7) (22.4)

Panne 0 0 5.8 13.9 35.2 98 83.4 106(3.5) (6.1) (12.1) (23.9) (17.6) (23.4)


large numbers of offspring to compensate for losses during trans-port ( Gaines and Bertness, 1992 ; Pechenik, 1999 ; Hedgecock and Pudovkin, 2011 ).

Reproductive allocation in plants can be infl uenced not only by local conditions (including competition with co-occurring individuals), but also by genotype ( Bazzaz et al., 1987 ). Be-cause the typical areal coverage of individual S. alternifl ora clones is not yet known, it is unclear how many seeds might be produced by the same clone or how seed production varies among genotypes. These aspects of the life history strategy of S. alternifl ora merit further study, and additional genetic work in this species may help elucidate some of these character-istics ( Richards et al., 2004 ; Blum et al., 2007 ; Hughes and Lotterhos, 2014 ).

Flowering phenology — On a latitudinal scale, northern S. alternifl ora fl owered earlier than southern S. alternifl ora in a greenhouse mesocosm, and more of the northern plants fl ow-ered by the end of the northern growing season ( Fig. 1 ). This is consistent with previous work that found that fl owering oc-curred in a north-to-south sequence ( Seneca, 1974 ). The order of fl owering by latitude has been retained in a mesocosm when S. alternifl ora is grown from seed ( Somers and Grant, 1981 ). In our study, we transplanted existing clones of S. alternifl ora and found that the northern plants still fl owered earlier in the season than southern plants, despite alteration of the southern plants’ photoperiod and temperature conditions ( Fig. 1 ), which does not suggest an impact of maternal effects on fl owering time. We ob-served a similar trend at a smaller spatial scale. The northernmost

marsh in our regional study, Site 3, reached its peak proportion of fl owering stems earlier than Sites 1 and 2.

The trend in fl owering phenology may result from latitudinal differences in the length of the growing season, since more northern plants senesce earlier, allowing less time for the com-pletion of seed production in later-fl owering plants. Thus, a se-lective pressure may exist for earlier fl owering in the north that does not exist in the south, where the growing season can be weeks to months longer. However, previous work has also shown that S. alternifl ora plants that fl owered later in the grow-ing season had higher rates of seed set and germination ( Fang et al., 2004b ), which may result from the greater diversity of pollen sources as more clones fl ower ( Fang et al., 2004a ). Thus, later fl owering can lead to an increased output of viable seeds. As temperatures rise, it is possible that southern S. alternifl ora genotypes will migrate northward, which could result in later fl owering coincident with the lengthening growing season. Al-ternatively, rising local temperatures may favor later-fl owering genotypes already present in the plant populations.

Local differences in phenology and seed production are fun-damental to our understanding of the creation and maintenance of local genetic diversity. On local to regional scales, we ob-served differences in initial fl owering among marsh subhabitats of ≤ 1 mo ( Table 1 ). Contrary to responses reported for other plant species ( Wada and Takeno, 2010 ; Takeno, 2012 ), we did not observe consistent evidence of stress induction of fl owering at the within-marsh scale ( Table 1 ). At Site 1, the fi rst fl owers were observed in early July in S. alternifl ora panne plants, whereas the less stressed creek-bank plants did not fl ower until

Fig. 4. In situ live belowground biomass of Spartina alternifl ora in 2011 (dashed line and gray squares: belowground live biomass; plants from Mas-sachusetts) and in CT-scanned plants grown in a greenhouse mesocosm in 2013 (solid line and black squares: belowground live volume of roots and rhizomes; plants from Rhode Island). Gray circle indicates the onset of fl ow-ering in both environments. Belowground biomass differed over time in the mesocosm plants (rank-transformed ANOVA; F 6, 48 = 17.00, P < 0.0001, R 2 = 0.71), but not those measured in situ (rank-transformed ANOVA; F 6, 52 = 1.63, P > 0.05, R 2 = 0.18). Values not indicated by the same letter were sig-nifi cantly different for the CT-scan data (Tukey-Kramer HSD test; P < 0.05). Error bars represent SE.

Fig. 5. Mean percent change in aboveground (stem height; dashed line, gray squares) and belowground (root and rhizome volume; solid line, black squares) growth over time for the 2013 greenhouse mesocosm S. alternifl ora plants that fl owered during the experiment. Gray circle indicates the time of fi rst fl owering. Signifi cant differences were found among the percent change in biomass (rank-transformed ANOVA; F 5, 41 = 26.99, P < 0.0001, R 2 = 0.79) and stem height (rank-transformed ANOVA; F 4, 34 = 19.82, P < 0.0001, R 2 = 0.73). Values not in-dicated by the same letter were signifi cantly different for the CT-scan biomass data (Tukey-Kramer HSD test; P < 0.05), and italicized letters similarly indicate signifi cant differences in stem height. Error bars represent SE.


the third week of August ( Table 1 ). Because this species is wind pollinated ( Fang, 2002 ), cross-pollination would be inhibited between these subhabitats if fl owering is offset in time, as we observed at Site 1. Yet the fi rst fl owers at Site 2 were observed in creek-bank and panne plants simultaneously ( Table 1 ), and so cross-pollination appears more likely. Spartina alternifl ora exhibits protogynous fl owering, with its stigmas becoming re-ceptive for pollination and then becoming shriveled within a few days, and pollen shed occurring 2–5 days after stigma emergence in the same fl oret ( Fang, 2002 ). Differences in fl ow-ering time on the order of weeks are thus suffi cient to prevent cross-pollination, because each infl orescence is receptive to pollen over a much shorter period. Additionally, given that S. alternifl ora is somewhat self-incompatible, mismatches in the timing of fl owering across clones could decrease the number of viable seeds by reducing the number of potential pollen donors ( Somers and Grant, 1981 ; Fang, 2002 ). Thus, differences in fl owering time between subhabitats could infl uence the number of viable seeds produced by that marsh.

Biomass allocation and phenology — We predicted that fl owering phenology would be related to temporal trends in the allocation of growth. Our results supported this hypothesis, with growth of aboveground biomass and seed production pre-dominating through the midsummer, aboveground growth ces-sation coinciding with fl owering, and belowground allocation increasing after the onset of fl ower production ( Fig. 4 and 5 ). If fl owering phenology is coincident with this allocation shift as our data suggest, then belowground biomass accumulation will occur predominantly during the window of time between fl ow-ering and senescence. Future predictions of salt marsh growth and accretion should thus consider not only the impact of the length of the growing season, but also the growth conditions and length of this specifi c part of the plant’s life cycle when belowground allocation predominates.

Implications for salt marshes facing climate change — With sea-level rise, the proportion of the marsh that is frequently fl ooded and dominated by tall (and more fecund) S. alterni-fl ora will increase in some areas ( Donnelly and Bertness, 2001 ). However, S. alternifl ora cannot survive total submer-gence, and productivity and seed output ceases above a cer-tain frequency of inundation ( Morris et al., 2002 ). Thus, below a certain elevation, increasing submergence itself is also a stressor that decreases seed output. Depending on the magni-tude and rate of low-marsh drowning, in the short term some marshes may have a greater seed output as larger areas of the marsh are submerged more frequently. However, in salt-marsh systems that maintain their relative elevation, increas-ing salinity and thermal stress could drive the production of smaller infl orescences, as was observed in the high-marsh panne subhabitats. Thus, we expect that changing environ-mental stressors will affect reproductive potential. Our work suggests that the balance between the impacts of increased inundation and increased stress on seed production will de-pend on whether marshes maintain their elevation in relation to sea level ( Craft et al., 2009 ; Kirwan et al., 2010 ), and how the proportion of the marsh area occupied by S. alternifl ora and its different height-forms changes over time ( Donnelly and Bertness, 2001 ).

Salt marsh plants are limited to a specifi c elevation range in relation to sea level by a combination of physiological processes

and interspecifi c interactions. As a result, they must maintain their elevation as sea level rises. Our data show that below-ground peat accumulation is concentrated after fl owering, and it is critical to consider the allocation shift that we observed with fl owering in the context of a climate change–driven lengthen-ing of the growing season. If fl owering begins to occur later (as is currently seen in more southern marshes) without a suffi cient extension of the growing season, less belowground biomass will accumulate prior to senescence. In marshes with a high sediment supply, such as some in the southeastern United States, later fl owering and an earlier start to the growing season may be benefi cial for elevation gain if more growth is concen-trated aboveground to increase sediment capture. However, in peat-based systems where belowground growth is the most im-portant driver of elevation gain, this increase in aboveground productivity would not be expected to drive increases in the rate of accretion. However, this relationship will be further com-plicated by day length as the growing season lengthens, owing to an interactive effect of temperature and light on fl owering ( Seneca and Broome, 1972 ; Seneca and Blum, 1984 ).

Natural systems worldwide are facing multidimensional ef-fects of climate change that threaten the ecosystem services they provide to people. Salt marshes provide an excellent model system for exploring the linkages between population-level ecological dynamics and ecosystem functioning, which will enable us to better predict future impacts. Our data sug-gest that sea-level rise and rising temperatures could affect seed production and belowground biomass accumulation in S. alternifl ora , with implications for the resilience of salt-marsh ecosystems.

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