RESEARCH ARTICLE
A M E R I C A N J O U R N A L O F B OTA N Y
FLOWERING AND BIOMASS ALLOCATION IN U.S. ATLANTIC COAST SPARTINA ALTERNIFLORA1 SARAH C. CROSBY2,3,6, MORGAN IVENS-DURAN2,7, MARK D. BERTNESS2, EARL DAVEY4, LINDA A. DEEGAN2,3, AND HEATHER M. LESLIE2,3,5 2Brown
University, Ecology and Evolutionary Biology, Box G-W, Providence, Rhode Island 02912 USA; 3Marine Biological Laboratory, Ecosystems Center, 7 MBL Street, Woods Hole, Massachusetts 02543 USA; 4U.S. EPA, Office of Research and Development, National Heath and Environmental Effects Research Laboratory, Atlantic Ecology Division, Narragansett, Rhode Island 02882 USA; and 5Brown 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 alterniflora Loisel (Poaceae) is a foundation species that builds and maintains salt marshes. Despite this species’ importance, much of its basic reproductive biology is not well understood, including flowering phenology, seed production, and the effects of flowering 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 flowering and seed production in S. alterniflora 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 flowering on growth allocation using field and greenhouse studies. • Key results: Flowering stem density did not vary along a latitudinal gradient, while at the local scale plants in the less submerged panne subhabitats produced fewer flowers 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 flowering phenology. • Conclusions: We expect that environmental change will affect seed production and that the phenological relationship with flowering 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 predictions of climate change impacts. Key words: biomass allocation; flowering; phenology; seed supply; Spartina alterniflora.
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 threatened by both direct and indirect human impacts such as ditching, filling, impounding, and eutrophication (Bromberg and Bertness, 2005; Gedan, Silliman, and Bertness, 2009; Deegan
et al., 2012). On the U.S. Atlantic coast, Spartina alterniflora Loisel (smooth cordgrass) is the species responsible for initial salt marsh colonization and the ongoing maintenance of the seaward edge of established salt marshes (Redfield, 1972; Bertness, 1991; Bertness and Hacker, 1994). Like many aquatic plants, S. alterniflora 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
the Estuarine Reserves Division, Office 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
American Journal of Botany 102(5): 669–676, 2015; http://www.amjbot.org/ © 2015 Botanical Society of America
669
670 • 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 O TA 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 significance of seedling establishment in S. alterniflora populations (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, magnitude, 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 reproduction in S. alterniflora is crucial for predicting where marshes may be gained or lost in the future. Like all organisms, S. alterniflora undergoes trade-offs in energy allocation between competing physiological processes (e.g., growth and reproduction) and between different reproductive 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 influence growth allocation. Marsh elevation is maintained by S. alterniflora as its aboveground biomass slows tidal water and increases sediment deposition (Redfield, 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 flowering, are often initiated by environmental cues, including threshold temperatures (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). Stressinduced flowering also occurs in many plant species (Wada and Takeno, 2010; Takeno, 2012), and the magnitude of stress experienced by S. alterniflora 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 environmental changes might affect multiple aspects of S. alterniflora biology. The goals of the present study were to (1) quantify temporal and spatial patterns in S. alterniflora flowering and seed production and (2) determine the relationship between flowering phenology and aboveground versus belowground biomass allocation. Spartina alterniflora is found in many salt marsh subhabitats, including creek banks, intermediate marsh elevations (such as the banks of ditches and upland of creeks) and highmarsh pannes. Submergence frequency differs among these subhabitats, which can drive variations in soil salinity and temperature (Pennings and Bertness, 2001). Further, the geographic range of S. alterniflora spans the U.S. Atlantic coast from Maine to Florida, providing a unique opportunity to consider trends in flowering across a large natural temperature gradient where both growing-season length and environmental conditions vary. We hypothesized that the onset and extent of sexual reproduction in S. alterniflora was correlated to environmental gradients across marshes and that this variation would drive differences in the magnitude of reproductive potential among marshes and marsh subhabitats. We further predicted that (1) flowering phenology would be related to temporal trends in the
allocation of biomass, (2) the cessation of aboveground allocation would coincide with flower production, and (3) allocation of belowground biomass would occur primarily after flower production. We used a multiscale approach, including investigation of flowering 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 experiment to study flowering phenology. Finally, we quantified temporal changes in aboveground and belowground biomass allocation using multiple analytical techniques (including repeated CT scans of living plants and field surveys) to determine the allocation to elevation-building belowground biomass leading up to, during, and following flowering. MATERIALS AND METHODS Latitudinal-scale flowering phenology and magnitude—In the field, the density of flowering stems was quantified 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. alterniflora monocultures ≥1 m away from a creek, we counted the number of stems and flowering stems (n = 8 per site, in 0.25-m2 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. alterniflora monocultures sampled at each were submerged
A M E R I C A N J O U R N A L O F B OTA N Y
FLOWERING AND BIOMASS ALLOCATION IN U.S. ATLANTIC COAST SPARTINA ALTERNIFLORA1 SARAH C. CROSBY2,3,6, MORGAN IVENS-DURAN2,7, MARK D. BERTNESS2, EARL DAVEY4, LINDA A. DEEGAN2,3, AND HEATHER M. LESLIE2,3,5 2Brown
University, Ecology and Evolutionary Biology, Box G-W, Providence, Rhode Island 02912 USA; 3Marine Biological Laboratory, Ecosystems Center, 7 MBL Street, Woods Hole, Massachusetts 02543 USA; 4U.S. EPA, Office of Research and Development, National Heath and Environmental Effects Research Laboratory, Atlantic Ecology Division, Narragansett, Rhode Island 02882 USA; and 5Brown 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 alterniflora Loisel (Poaceae) is a foundation species that builds and maintains salt marshes. Despite this species’ importance, much of its basic reproductive biology is not well understood, including flowering phenology, seed production, and the effects of flowering 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 flowering and seed production in S. alterniflora 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 flowering on growth allocation using field and greenhouse studies. • Key results: Flowering stem density did not vary along a latitudinal gradient, while at the local scale plants in the less submerged panne subhabitats produced fewer flowers 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 flowering phenology. • Conclusions: We expect that environmental change will affect seed production and that the phenological relationship with flowering 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 predictions of climate change impacts. Key words: biomass allocation; flowering; phenology; seed supply; Spartina alterniflora.
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 threatened by both direct and indirect human impacts such as ditching, filling, impounding, and eutrophication (Bromberg and Bertness, 2005; Gedan, Silliman, and Bertness, 2009; Deegan
et al., 2012). On the U.S. Atlantic coast, Spartina alterniflora Loisel (smooth cordgrass) is the species responsible for initial salt marsh colonization and the ongoing maintenance of the seaward edge of established salt marshes (Redfield, 1972; Bertness, 1991; Bertness and Hacker, 1994). Like many aquatic plants, S. alterniflora 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
the Estuarine Reserves Division, Office 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
American Journal of Botany 102(5): 669–676, 2015; http://www.amjbot.org/ © 2015 Botanical Society of America
669
670 • 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 O TA 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 significance of seedling establishment in S. alterniflora populations (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, magnitude, 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 reproduction in S. alterniflora is crucial for predicting where marshes may be gained or lost in the future. Like all organisms, S. alterniflora undergoes trade-offs in energy allocation between competing physiological processes (e.g., growth and reproduction) and between different reproductive 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 influence growth allocation. Marsh elevation is maintained by S. alterniflora as its aboveground biomass slows tidal water and increases sediment deposition (Redfield, 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 flowering, are often initiated by environmental cues, including threshold temperatures (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). Stressinduced flowering also occurs in many plant species (Wada and Takeno, 2010; Takeno, 2012), and the magnitude of stress experienced by S. alterniflora 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 environmental changes might affect multiple aspects of S. alterniflora biology. The goals of the present study were to (1) quantify temporal and spatial patterns in S. alterniflora flowering and seed production and (2) determine the relationship between flowering phenology and aboveground versus belowground biomass allocation. Spartina alterniflora is found in many salt marsh subhabitats, including creek banks, intermediate marsh elevations (such as the banks of ditches and upland of creeks) and highmarsh pannes. Submergence frequency differs among these subhabitats, which can drive variations in soil salinity and temperature (Pennings and Bertness, 2001). Further, the geographic range of S. alterniflora spans the U.S. Atlantic coast from Maine to Florida, providing a unique opportunity to consider trends in flowering across a large natural temperature gradient where both growing-season length and environmental conditions vary. We hypothesized that the onset and extent of sexual reproduction in S. alterniflora was correlated to environmental gradients across marshes and that this variation would drive differences in the magnitude of reproductive potential among marshes and marsh subhabitats. We further predicted that (1) flowering phenology would be related to temporal trends in the
allocation of biomass, (2) the cessation of aboveground allocation would coincide with flower production, and (3) allocation of belowground biomass would occur primarily after flower production. We used a multiscale approach, including investigation of flowering 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 experiment to study flowering phenology. Finally, we quantified temporal changes in aboveground and belowground biomass allocation using multiple analytical techniques (including repeated CT scans of living plants and field surveys) to determine the allocation to elevation-building belowground biomass leading up to, during, and following flowering. MATERIALS AND METHODS Latitudinal-scale flowering phenology and magnitude—In the field, the density of flowering stems was quantified 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. alterniflora monocultures ≥1 m away from a creek, we counted the number of stems and flowering stems (n = 8 per site, in 0.25-m2 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. alterniflora monocultures sampled at each were submerged
