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Systems Biology and the Seagrass Paradox: Adaptation, Acclimation, and Survival of Marine Angiosperms in a Changing Ocean Climate

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Abstract

Predicting adaptive fitness to any environment requires mechanistic understanding of environmental influence on metabolic networks that control energy assimilation, growth, and reproduction. Although the potential impacts of environment on gene products are myriad, important phenotypic responses are often regulated by a few key points in metabolic networks where externally supplied resources or physiological reaction substrates limit reaction kinetics. Environmental resources commonly limiting seagrass productivity, survival, and growth include light and CO2 availability that control carbon assimilation and sucrose formation. Phosphate availability can also be important in oligotrophic tropical environments, particularly in the presence of carbonate sediments. Temperature and macronutrient oversupply (eutrophication) can act as confounding stressors, particularly in temperate environments. Photoacclimation can be regulated by electron transport pathways residing in the chloroplast stroma, but stress responses are often manifest by the expression of generalized stress response proteins, both of which appear to be affected by temperature and CO2 availability. A systems approach is employed to explore (1) the responses of seagrasses to the combined impacts of environmental limiting factors that control fundamental physiological processes leading to whole-plant performance; (2) sediment diagenetic processes that facilitate nutrient remineralization, carbon sequestration, and toxin neutralization; (3) interactions with other organisms induced by trophic cascades; and (4) impacts of human-induced climate change that affect system dynamics at numerous points in the network.

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References

  • Ackerman J (2006) Sexual reproduction of seagrasses: pollination in the marine context. In: Larkum A, Orth R, Duarte C (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht

    Google Scholar 

  • Al-Moghrabi S, Goiran C, Allemand D, Speziale N, Jaubert J (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral-dinoflagellate association II. Mechanism for bicarbonate uptake. J Exp Mar Biol Ecol 199:227–248

    Article  CAS  Google Scholar 

  • Arp W (1991) Effects of source-sink relations on photosynthetic acclimation to elevated CO2. Plant Cell Environ 14:869–876

    Article  CAS  Google Scholar 

  • Backhausen J, Scheibe R (1999) Adaptation of tobacco plants to elevated CO2: influence of leaf age on changes in physiology, redox states and NADP-malate dehydrogenase activity. J Exp Bot 50:665–675

    Article  CAS  Google Scholar 

  • Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339

    Article  CAS  PubMed  Google Scholar 

  • Batiuk R, Bergstrom P, Kemp M, Koch E, Murray L, Stevenson J, Bartleson R, Carter V, Rybicki N, Landwehr J, Gallegos C, Karrh L, Naylor M, Wilcox D, Moore K, Ailstock S, Teichberg M (2000) Chesapeake Bay submerged aquatic vegetation water quality and habitat-based requirements and restoration targets: a second synthesis. Chesapeake Bay Program Office, Annapolis, MD

    Google Scholar 

  • Beer S, Koch E (1996) Photosynthesis of marine macroalgae and seagrasses in globally changing CO2 environments. Mar Ecol Prog Ser 141:199–204

    Article  Google Scholar 

  • Beer S, Rehnberg J (1997) The acquisition of inorganic carbon by the seagrass Zostera marina. Aquat Bot 56:277–283

    Article  CAS  Google Scholar 

  • Berner R, Scott M, Thomlinson C (1970) Carbonate alkalinity in the pore waters of anoxic marine sediments. Limnol Oceanogr 15:544–549

    Article  CAS  Google Scholar 

  • Björk M, Uku J, Weil A, Beer S (1999) Photosynthetic tolerances to desiccation of tropical intertidal seagrasses. Mar Ecol Prog Ser 191:121–126

    Article  Google Scholar 

  • Bodensteiner L (2006) The impact of light availability on benthic oxygen release by the seagrasses Thalassia testudinum (Banks ex König) and Zostera marina (L.). MS thesis, San Jose State University, San Jose

    Google Scholar 

  • Borum J, Pedersen O, Greve TM, Frankovich TA, Zieman JC, Fourqurean JW, Madden CJ (2005) The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. J Ecol 93:148–158

    Article  CAS  Google Scholar 

  • Bruggeman FJ, Westerhoff HV (2007) The nature of systems biology. Trends Microbiol 15:45–50

    Article  CAS  PubMed  Google Scholar 

  • Brush M, Nixon S (2002) Direct measurements of light attenuation by epiphytes on eelgrass Zostera marina. Mar Ecol Prog Ser 238:73–79

    Article  Google Scholar 

  • Buapet P, Rasmusson LM, Gullström M, Björk M (2013) Photorespiration and carbon limitation determine productivity in temperate seagrasses. PLoS One 8:e83804

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bulthuis D, Woelkerling W (1983) Biomass accumulation and shading effects of epiphytes on leaves of the seagrass, Heterozostera tasmanica, in Victoria, Australia. Aquat Bot 16:137–148

    Article  Google Scholar 

  • Burdige D, Hu X, Zimmerman R (2010) The widespread occurrence of coupled carbonate dissolution/reprecipitation in surface sediments on the Bahamas Bank. Am J Sci I310:492–521

    Article  CAS  Google Scholar 

  • Burdige D, Zimmerman R (2003) Impact of seagrass density on carbonate dissolution in Bahamian sediments. Limnol Oceanogr 47:1751–1763

    Article  Google Scholar 

  • Burdige D, Zimmerman R, Hu X (2008) Rates of carbonate dissolution in permeable sediments estimated from pore-water profiles: the role of sea grasses. Limnol Oceanogr 53:549–565

    Article  CAS  Google Scholar 

  • Burdige DJ (2006) Geochemistry of marine sediments. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Campbell J, Fourqurean J (2013) Effects of in situ CO2 enrichment on the structural and chemical characteristics of the seagrass Thalassia testudinum. Mar Biol 160:1465–1475

    Article  CAS  Google Scholar 

  • Carr J, D’Odorico P, McGlathery K, Wiberg P (2010) Stability and bistability of seagrass ecosystems in shallow coastal lagoons: role of feedbacks with sediment resuspension and light attenuation. J Geophys Res 115:G03011

    Article  Google Scholar 

  • Cebrián J, Enríquez S, Fortes M, Agawin N, Vermaat J, Duarte C (1999) Epiphyte accrual on Posidonia oceanica (L.) Delile leaves: implications for light absorption. Bot Mar 42:123–128

    Article  Google Scholar 

  • Celebi B (2016) Potential impacts of climate change on photochemistry of Zostera marina L. PhD, Old Dominion University, Norfolk

    Google Scholar 

  • Celebi B, Cemal Gucu A, Ok M, Sakinan S, Alkoglu E (2006) Hydrographic indications to understand the absence of Posidonia oceanica in the Levant Sea (Eastern Mediterranean). In: Gambi M, Borg J, Buia M, Di Carlo G, Pergent-Martini C, Pergent G, Procaccini G (eds) Proceedings of the mediterranean seagrass workshop. Biologia Marina Mediterranea

    Google Scholar 

  • Cotrufo M, Ineson P, Scott Y (2002) Elevated CO2 reduces the nitrogen concentration of plant tissues. Glob Chang Biol 4:43–54

    Article  Google Scholar 

  • Cummings M, Zimmerman R (2003) Light harvesting and the package effect in Thalassia testudinum Koenig and Zostera marina L.: optical constraints on photoacclimation. Aquat Bot 75:261–274

    Article  Google Scholar 

  • Dalla Via J, Sturmbauer C, Schönweger C, Sötz E, Mathekowitsch M, Stifter M, Reiger R (1988) Light gradients and meadow structure in Posidonia oceanica: ecomorphological and functional correlates. Mar Ecol Prog Ser 163:267–278

    Article  Google Scholar 

  • Dattolo E, Ruocco M, Brunet C, Lorenti M, Lauritano C, D'Esposito D, De Luca P, Sanges R, Mazzuca S, Procaccini G (2014) Response of the seagrass Posidonia oceanica to different light environments: insights from a combined molecular and photo-physiological study. Mar Environ Res 101:225–236

    Article  CAS  PubMed  Google Scholar 

  • den Hartog C, Kuo J (2006) Taxonomy and biogeography of seagrasses. In: Larkum A, Orth R, Duarte C (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht

    Google Scholar 

  • Duarte C (1991) Seagrass depth limits. Aquat Bot 40:363–377

    Article  Google Scholar 

  • Duffy J (2006) Biodiversity and the functioning of seagrass ecosystems. Mar Ecol Prog Ser 311:233–250

    Article  Google Scholar 

  • Duffy JE, Reynolds PL, Boström C, Coyer JA, Cusson M, Donadi S, Douglass JG, Eklöf JS, Engelen AH, Eriksson BK, Fredriksen S, Gamfeldt L, Gustafsson C, Hoarau G, Hori M, Hovel K, Iken K, Lefcheck JS, Moksnes P-O, Nakaoka M, O'Connor MI, Olsen JL, Richardson JP, Ruesink JL, Sotka EE, Thormar J, Whalen MA, Stachowicz JJ (2015) Biodiversity mediates top–down control in eelgrass ecosystems: a global comparative-experimental approach. Ecol Lett 18(7):696–705

    Article  PubMed  Google Scholar 

  • Durako M (1993) Photosynthetic utilization of CO2(aq) and HCO3 in Thalassia testudinum (Hydrocharitacae). Mar Biol 115:373–380

    Article  Google Scholar 

  • Eriksson BK, Ljunggren L, Sandström A, Johansson G, Mattila J, Rubach A, Råberg S, Snickars M (2009) Declines in predatory fish promote bloom-forming macroalgae. Ecol Appl 19:1975–1988

    Article  PubMed  Google Scholar 

  • Evans AS, Webb KL, Penhale PA (1986) Photosynthetic temperature acclimation in two coexisting seagrasses, Zostera marina L. and Ruppia maritima L. Aquat Bot 24:185–197

    Article  Google Scholar 

  • Faber P, Evrard V, Woodland R, Cartwright I, Cook P (2014) Pore-water exchange driven by tidal pumping causes alkalinity export in two intertidal inlets. Limnol Oceanogr 59:1749–1763

    Article  CAS  Google Scholar 

  • Faber P, Kessler A, Bull J, McKelvie I, Meysman F, Cook P (2012) The role of alkalinity generation in controlling the fluxes of CO2 during exposure and inundation on tidal flats. Biogeosciences 9:4087–4097

    Article  CAS  Google Scholar 

  • Falkowski P, Raven J (2007) Aquatic photosynthesis. Princeton, Princeton, NJ

    Google Scholar 

  • Field C, Mooney H (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givnish T (ed) On the economy of plant form and function. Cambridge University Press, Cambridge

    Google Scholar 

  • Goldhaber M (2003) Sulfur-rich sediments. In: Mackenzie F (ed) Treatise on geochemistry. Elsevier, Amsterdam

    Google Scholar 

  • Gould S (1978) The panda’s peculiar thumb. Nat Hist 87:20–30

    Google Scholar 

  • Greening HS, Cross L, Sherwood E (2011) A multiscale approach to seagrass recovery in Tampa Bay, Florida. Ecol Restor 29:82–93

    Article  Google Scholar 

  • Hall-Spencer J, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner S, Rowley S, Tedesco D, Buia M-C (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99

    Article  CAS  PubMed  Google Scholar 

  • Hanke G, Holtgrefe S, König N, Strodtkötter I, Voss I, Scheibe R (2009) Use of transgenic plants to uncover strategies for maintenance of redox homeostasis during photosynthesis. In: Jean-Pierre J (ed) Advances in botanical research, vol 52. Elsevier, Amsterdam, pp 207–251

    Google Scholar 

  • Hartog CD, Loenhoud PJV, Roelofs JGM, Van de Sande JCPM (1979) Chromosome number from three seagrasses from the Netherlands Antilles. Aquat Bot 7:267–271

    Article  Google Scholar 

  • Heck KL, Carmthers TJB, Duarte CM, Hughes AR, Kendrick G, Orth RJ, Williams SW (2008) Trophic transfers from seagrass meadows subsidize diverse marine and terrestrial consumers. Ecosystems 11:1198–1210

    Article  Google Scholar 

  • Hemminga M, Mateo M (1996) Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar Ecol Prog Ser 140:285–298

    Article  Google Scholar 

  • Higgs ND, Newton J, Attrill MJ (2016) Caribbean spiny lobster fishery is underpinned by trophic subsidies from chemosynthetic primary production. Curr Biol 26(24):3393–3398

    Article  CAS  PubMed  Google Scholar 

  • Holmer M, Nielsen R (2007) Effects of filamentous algal mats on sulfide invasion in eelgrass (Zostera marina). J Exp Mar Biol Ecol 353:245–252

    Article  CAS  Google Scholar 

  • Hu X, Burdige D (2008) Shallow marine carbonate dissolution and early diagenesis: implications from an incubation study. J Mar Res 66:489–527

    Article  CAS  Google Scholar 

  • Hu X, Cai W (2011) An assessment of ocean margin anaerobic processes on oceanic alkalinity budget. Global Biogeochem Cycles 25(3):GB3003

    Article  CAS  Google Scholar 

  • Hughes BB, Hammerstrom KK, Grant NE, Hoshijima U, Eby R, Wasson K (2016) Trophic cascades on the edge: fostering seagrass resilience via a novel pathway. Oecologia 182:231–241

    Article  PubMed  Google Scholar 

  • Hüner N, Dahal K, Hollis L, Bode R, Rosso D, Krol M, Ivanov A (2012) Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited. Front Plant Sci 3:1–12

    Article  CAS  Google Scholar 

  • Invers O, Zimmerman R, Alberte R, Perez M, Romero J (2001) Inorganic carbon sources for seagrass photosynthesis: an experimental evaluation for bicarbonate use in temperate species. J Exp Mar Biol Ecol 265:203–217

    Article  CAS  Google Scholar 

  • Jackson M, Ishizawa K, Ito O (2009) Evolution and mechanisms of plant tolerance to flooding stress. Ann Bot 103:137–142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang Z, Huang X, Zhang J (2010) Effects of CO2 enrichment on photosynthesis, growth and biochemical composition of seagrass Thalassia hemprichii (Ehrenb.) Aschers. J Integr Plant Biol 52:904–913

    Article  CAS  PubMed  Google Scholar 

  • Karez R, Englebert S, Sommer U (2000) ‘Co-consumption’ and ‘protective coating’: two new proposed effects of epiphytes on their macroalgal hosts in mesograzer-epiphyte-host interactions. Mar Ecol Prog Ser 205:85–93

    Google Scholar 

  • Kim TY, Sohn SB, Kim YB, Kim WJ, Lee SY (2012) Recent advances in reconstruction and applications of genome-scale metabolic models. Curr Opin Biotechnol 23:617–623

    Article  CAS  PubMed  Google Scholar 

  • Klumpp D, Salita-Espinosa J, Fortes M (1992) The role of epiphytic periphyton and macroinvertebrate grazers in the trophic flux of a tropical seagrass community. Aquat Bot 43:327–349

    Article  Google Scholar 

  • Koch M, Bowes G, Ross C, Zhang X-H (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Chang Biol 19:103–132

    Article  PubMed  Google Scholar 

  • Kuo J, den Hartog C (2006) Seagrass morphology, anatomy and ultrastructure. In: Larkum A, Orth R, Duarte C (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht

    Google Scholar 

  • Lamb JB, van de Water JAJM, Bourne DG, Altier C, Hein MY, Fiorenza EA, Abu N, Jompa J, Harvell CD (2017) Seagrass ecosystems reduce exposure to bacterial pathogens of humans, fishes, and invertebrates. Science 355:731–733

    Article  CAS  PubMed  Google Scholar 

  • Larkum A, Orth R, Duarte C (eds) (2006) Seagrasses: biology, ecology and conservation. Springer, Dordrecht

    Google Scholar 

  • Lawson S, Wiberg P, McGlathery K, Fugate D (2007) Wind-driven sediment suspension controls light availability in a shallow coastal lagoon. Estuar Coasts 30:101–112

    Article  Google Scholar 

  • Les D, Cleland M, Waycott M (1997) Phylogenetic studies in Alismatidae, II: evolution of marine angiosperms (seagrasses) and hydrophily. Syst Bot 22:443–463

    Article  Google Scholar 

  • Leuschner C, Landwehr S, Mehlig U (1998) Limitation of carbon assimilation of intertidal Zostera noltii and Z. marina by desiccation at low tide. Aquat Bot 62:171–176

    Article  CAS  Google Scholar 

  • Levering J, Broddrick J, Dupont C, Peers G, Beeri K, Mayers J, Gallina A, Allen A, Palsson B, Zengler K (2016) Genome-scale model reveals metabolic basis of biomass partitioning in a marine diatom. PLoS One 11:e0155038

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Losee R, Wetzel R (1983) Selective light attenuation by the periphyton complex. In: Wetzel R (ed) Periphyton of freshwater ecosystems. Dr. W. Junk, Dordrecht

    Google Scholar 

  • Mazzella L, Alberte RS (1986) Light adaptation and the role of autotrophic epiphytes in primary production of the temperate seagrass, Zostera marina L. J Exp Mar Biol Ecol 100:165–180

    Article  Google Scholar 

  • McLeod E, Chmura G, Bouillon S, Salm R, Björk M, Duarte C, Loevlock C, Schlesinger W, Silliman B (2011) A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front Ecol Environ 9:552–560

    Article  Google Scholar 

  • McPherson M, Hill V, Zimmerman R, Dierssen H (2011) The optical properties of Greater Florida Bay: implications for seagrass abundance. Estuar Coasts 34:1150–1160

    Article  Google Scholar 

  • McPherson ML, Zimmerman RC, Hill VJ (2015) Predicting carbon isotope discrimination in eelgrass (Zostera marina L.) from the environmental parameters—light, flow, and [DIC]. Limnol Oceanogr 60:1875–1889

    Article  Google Scholar 

  • McRoy C, Hellfrich C (eds) (1977) Seagrass ecosystems: a scientific perspective. Marcel Dekker, New York

    Google Scholar 

  • Moore K, Jarvis J (2008) Environmental factors affecting summertime eelgrass diebacks in the lower Chesapeake Bay: implications for long-term persistence. J Coast Res 55:135–147

    Article  Google Scholar 

  • Moore K, Shields E, Parrish D, Orth R (2012) Eelgrass survival in two contrasting systems: role of turbidity and summer water temperatures. Mar Ecol Prog Ser 448:247–258

    Article  Google Scholar 

  • Neckles H, Koepfler E, Haas L, Wetzel R, Orth R (1994) Dynamics of epiphytic photoautotrophs and heterotrophs in Zostera marina (eelgrass) microcosms: responses to nutrient enrichment and grazing. Estuaries 17:597–605

    Article  Google Scholar 

  • Odum H (1983) Systems ecology. An introduction. Wiley, New York

    Google Scholar 

  • Olsen JL, Rouzé P, Verhelst B, Lin Y-C, Bayer T, Collen J, Dattolo E, De Paoli E, Dittami S, Maumus F, Michel G, Kersting A, Lauritano C, Lohaus R, Töpel M, Tonon T, Vanneste K, Amirebrahimi M, Brakel J, Boström C, Chovatia M, Grimwood J, Jenkins JW, Jueterbock A, Mraz A, Stam WT, Tice H, Bornberg-Bauer E, Green PJ, Pearson GA, Procaccini G, Duarte CM, Schmutz J, Reusch TBH, Van de Peer Y (2016) The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530:331–335

    Article  CAS  PubMed  Google Scholar 

  • Orth JD, Thiele I, Palsson BO (2010) What is flux balance analysis? Nat Biotechnol 28:245–248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orth R, Carruthers T, Dennison W, Duarte C, Fourqurean J, Heck K, Hughes A, Kendrick G, Kenworthy W, Olyarnik S, Short F, Waycott M, Williams S (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996

    Article  Google Scholar 

  • Orth R, Moore K (1983) Chesapeake Bay: an unprecedented decline in submerged aquatic vegetation. Science 222:51–53

    Article  CAS  PubMed  Google Scholar 

  • Orth RJ, Montfrans JV (1984) Epiphyte-seagrass relationships with an emphasis on the role of micrograzing: a review. Aquat Bot 18:43–69

    Article  Google Scholar 

  • Palacios S, Zimmerman R (2007) Response of eelgrass (Zostera marina L.) to CO2 enrichment: possible impacts of climate change and potential for remediation of coastal habitats. Mar Ecol Prog Ser 344:1–13

    Article  Google Scholar 

  • Pedersen O, Binzer T, Borum J (2004) Sulphide intrusion in eelgrass ( Zostera marina L.) Plant Cell Environ 27:595–602

    Article  CAS  Google Scholar 

  • Penhale PA (1977) Macrophyte-epiphyte biomass and productivity in an eelgrass (Zostera marina L.) community. J Exp Mar Biol Ecol 26:211–224

    Article  CAS  Google Scholar 

  • Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8:33–41

    Article  CAS  PubMed  Google Scholar 

  • Pfannschmidt T, Yang C (2012) The hidden function of photosynthesis: a sensing system for environmental conditions that regulates plant acclimation responses. Protoplasma 249:125–135

    Article  CAS  Google Scholar 

  • Phillips R, McRoy C (eds) (1980) Handbook of seagrass biology: an ecosystem perspective. Garland STPM Press, New York

    Google Scholar 

  • Pregnall AM, Smith RD, Kursar TA, Alberte RS (1984) Metabolic adaptation of Zostera marina (eelgrass) to diurnal periods of root anoxia. Mar Biol 83:141–147

    Article  CAS  Google Scholar 

  • Procaccini G, Beer S, Björk M, Olsen J, Mazzuca S, Santos R (2012) Seagrass ecophysiology meets ecological genomics: are we ready? Mar Ecol 33:522–527

    Article  Google Scholar 

  • Ralph P, Polk S, Moore K, Orth R, Smith W Jr (2002) Operation of the xanthophyll cycle in the seagrass Zostera marina in response to variable irradiance. J Exp Mar Biol Ecol 271:189–207

    Article  CAS  Google Scholar 

  • Raven J (2010) Inorganic carbon acquisition by eukaryotic algae: four current questions. Photosynth Res 106:123–134

    Article  CAS  PubMed  Google Scholar 

  • Raven JA, Beardall J (2014) CO2 concentrating mechanisms and environmental change. Aquat Bot 118:24–37

    Article  CAS  Google Scholar 

  • Retallack G (2001) A 300-million year record of atmospheric carbon dioxide from fossil plant cuticles. Nature 411:247–248

    Article  Google Scholar 

  • Sand-Jensen K (1977) Effect of epiphytes on eelgrass photosynthesis. Aquat Bot 3:55–63

    Article  CAS  Google Scholar 

  • Sand-Jensen K, Revsbech N, Jørgensen B (1985) Microprofiles of oxygen in epiphyte communities on submerged macrophytes. Mar Biol 89:55–62

    Article  Google Scholar 

  • Short F, Matso K, Hoven M, Whitten J, Burdick D, Short C (2001) Lobster use of eelgrass habitat in the Piscataqua River on the New Hampshire/Maine border, USA. Estuaries 24:277–284

    Article  Google Scholar 

  • Short F, Polidoro B, Livingstone S, Carpenter K, Bandiera S, Bujang J, Calumpong H, Carruthers T, Coles R, Dennison W, Erftmeijer P, Fortes M, Freeman A, Jagtap T, Kamal A, Kendrick G, Kenworthy J, La Nafie Y, Nasution I, Orth R, Prathep A, Sanciango J, van Tussebroek B, Vergara S, Waycott M, Zieman J (2011) Extinction risk assessment of the world’s seagrass species. Biol Conserv 144(7):1961–1971

    Article  Google Scholar 

  • Short F, Wyllie-Echeverria S (1996) Natural and human-induced disturbance of seagrasses. Environ Conserv 23:17–27

    Article  Google Scholar 

  • Short FT, Neckles HA (1999) The effects of global climate change on seagrasses. Aquat Bot 63:169–196

    Article  Google Scholar 

  • Smith RD, Dennison WC, Alberte RS (1984) Role of seagrass photosynthesis in root aerobic processes. Plant Physiol 74:1055–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith RD, Pregnall AM, Alberte RS (1988) Effects of anaerobiosis on root metabolism of the seagrass Zostera marina L. (eelgrass). Mar Biol 98:131–141

    Article  CAS  Google Scholar 

  • Tomasko DA, Corbett CA, Greening HS, Raulerson GE (2005) Spatial and temporal variation in seagrass coverage in Southwest Florida: assessing the relative effects of anthropogenic nutrient load reductions and rainfall in four contiguous estuaries. Mar Pollut Bull 50:797–805

    Article  CAS  PubMed  Google Scholar 

  • Trocine R, Rice J, Wells G (1981) Inhibition of seagrass photosynthesis by ultraviolet-B radiation. Plant Physiol 68:74–81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Montrfrans J, Wetzel R, Orth R (1984) Epiphyte-grazer relationships in seagrass meadows: consequences for seagrass growth and production. Estuaries 7:289–309

    Article  Google Scholar 

  • van Tussenbroek BI, Villamil N, Márquez-Guzmán J, Wong R, Monroy-Velázquez LV, Solis-Weiss V (2016) Experimental evidence of pollination in marine flowers by invertebrate fauna. Nat Commun 7:12980

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Voesenek LACJ, Bailey-Serres J (2015) Flood adaptive traits and processes: an overview. New Phytol 206:57–73

    Article  CAS  PubMed  Google Scholar 

  • Woodward F (2002) Potential impacts of global elevated CO2 concentrations on plants. Curr Opin Plant Biol 5:207–211

    Article  CAS  PubMed  Google Scholar 

  • Xue X-G, Long S, Ort D (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Mar Sci 61:235–261

    Google Scholar 

  • Zimmerman R (2003) A biooptical model of irradiance distribution and photosynthesis in seagrass canopies. Limnol Oceanogr 48:568–585

    Article  Google Scholar 

  • Zimmerman R (2006) Light and photosynthesis in seagrass meadows. In: Larkum A, Orth R, Duarte C (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht

    Google Scholar 

  • Zimmerman R, Alberte R (1996) Effect of light/dark transition on carbon translocation in eelgrass Zostera marina seedlings. Mar Ecol Prog Ser 136:305–309

    Article  Google Scholar 

  • Zimmerman R, Cabello-Pasini A, Alberte R (1994) Modeling daily production of aquatic macrophytes from irradiance measurements: a comparative analysis. Mar Ecol Prog Ser 114:185–196

    Article  Google Scholar 

  • Zimmerman R, Caffrey J (2002) Chapter 8. Primary producers. In: Caffrey J, Brown M, Tyler W, Silberstein M (eds) Changes in a California estuary: a profile of elkhorn slough. Elkhorn Slough Foundation, Moss Landing, CA

    Google Scholar 

  • Zimmerman R, Hill V, Celebi B, Jinuntuya M, Ruble D, Smith M, Cedeno T, Swingle W (2017) Experimental impacts of climate warming and ocean carbonation on eelgrass (Zostera marina L.) Mar Ecol Prog Ser 566:1–15

    Article  Google Scholar 

  • Zimmerman R, Hill V, Gallegos C (2015) Predicting effects of ocean warming, acidification and water quality on Chesapeake region eelgrass. Limnol Oceanogr 60:1781–1804

    Article  CAS  Google Scholar 

  • Zimmerman R, Kohrs D, Alberte R (1996) Top-down impact through a bottom-up mechanism: the effect of limpet grazing on growth, productivity and carbon allocation of Zostera marina. Oecologia 107:560–567

    Article  PubMed  Google Scholar 

  • Zimmerman R, Kohrs D, Steller D, Alberte R (1997) Impacts of CO2-enrichment on productivity and light requirements of eelgrass. Plant Physiol 115:599–607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmerman R, Kohrs D, Steller DL, Alberte R (1995) Carbon partitioning in eelgrass. Regulation by photosynthesis and the response to daily light-dark cycles. Plant Physiol 108:1665–1671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmerman R, Smith R, Alberte R (1987) Is growth of eelgrass nitrogen limited? A numerical simulation of the effects of light and nitrogen on the growth dynamics of Zostera marina. Mar Ecol Prog Ser 41:167–176

    Article  Google Scholar 

  • Zimmerman RC, Smith RD, Alberte RS (1989) Thermal acclimation and whole plant carbon balance in Zostera marina L. (eelgrass). J Exp Mar Biol Ecol 130:93–109

    Article  CAS  Google Scholar 

  • Zupo V, Buia M, Mazzella L (1997) A production model for Posidonia oceanica based on temperature. Estuar Coast Shelf Sci 44:483–492

    Article  Google Scholar 

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Acknowledgments

Thanks to Manoj Kumar and Peter Ralph for inviting this contribution to this book. Financial support was provided by the US National Science Foundation (Awards OCE-1061823 and OCE-1635403).

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Correspondence to Richard C. Zimmerman .

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Zimmerman, R.C. (2017). Systems Biology and the Seagrass Paradox: Adaptation, Acclimation, and Survival of Marine Angiosperms in a Changing Ocean Climate. In: Kumar, M., Ralph, P. (eds) Systems Biology of Marine Ecosystems. Springer, Cham. https://doi.org/10.1007/978-3-319-62094-7_8

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