Photosynthesis and daily metabolic carbon balance of the invasive Caulerpa racemosa var. cylindracea (Chlorophyta: Caulerpales) along a depth gradient
DOI:
https://doi.org/10.3989/scimar.2011.75n4803Keywords:
Caulerpa racemosa, carbon balance, invasive species, photosynthesis, depth, MediterraneanAbstract
The photosynthetic plasticity of the invasive green alga Caulerpa racemosa v. cylindracea (hereafter C. racemosa) has been proposed as a relevant mechanism determining its successful performance on Mediterranean benthic assemblages over broad depth gradients. In the present study, the photosynthetic performance of C. racemosa was evaluated through a carbon balance approach at three invaded sites with contrasting depths (11, 18 and 26 m) and light regimes. At each sampling depth, photosynthesis vs irradiance (P vs E) curves were performed on C. racemosa fronds and daily net productivity values were obtained by the numerical integration of P vs E models with continuous recording of irradiance measured on the sea floor. Photosynthetic responses were consistent with those typically exhibited by shade-adapted macroalgal species and other Mediterranean populations of C. racemosa: a significant reduction in maximum photosynthesis (Pmax) occurring at an intermediate depth (18 m) and a higher photosynthetic efficiency (α) and lower dark respiration rate (Rd) at the deepest sampling depth. Mean values of daily net C balance obtained from the deeper site were only 15% lower than those obtained from the shallower site, despite the severe reduction in light availability. This daily net carbon gain was ca. 29% higher than would be expected if photosynthetic adjustments did not occur in the deeper algal population. The evidence provided by these data support the hypothesis of photoacclimation in C. racemosa as an effective mechanism to optimize algal productivity across depth gradients in the Mediterranean Sea.
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References
Argyrou, M., A. Demetropoulos and M. Hadjichristophorou. – 1999. Expansion of the macroalga Caulerpa racemosa and changes in softbottom macrofaunal assemblages in Moni Bay, Cyprus. Oceanol. Acta, 22: 517-528. http://dx.doi.org/10.1016/S0399-1784(00)87684-7
Balata, D., L. Piazzi and F. Cinelli. – 2004. A comparison among assemblages in areas invaded by Caulerpa taxifolia and Caulerpa racemosa on a subtidal Mediterranean rocky bottom. Mar. Ecol., 25(1): 1-13. http://dx.doi.org/10.1111/j.1439-0485.2004.00013.x
Baly, E.C.C. – 1935. The kinetics of photosynthesis. Proc. R. Soc. Lond. Ser. B Biol. Sci., 117: 218-239.
Boudouresque, C.F. and M. Verlaque . – 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar. Poll. Bull., 44: 32-38. http://dx.doi.org/10.1016/S0025-326X(01)00150-3
Bulleri, F. and L. Benedetti-Cecchi. – 2008. Facilitation of the introduced green alga Caulerpa racemosa by resident algal turfs: experimental evaluation of underlying mechanisms. Mar. Ecol. Prog. Ser., 364: 77-86. http://dx.doi.org/10.3354/meps07484
Cayabyab, N.M. and S. Enríquez. – 2007. Leaf photoacclimatory responses of the tropical seagrass Thalassia testudinum under mesocosm conditions: a mechanistic scaling-up study. New Phytol., 176: 108-123. http://dx.doi.org/10.1111/j.1469-8137.2007.02147.x PMid:17696981
Cebrian, E. and E. Ballesteros. – 2009. Temporal and spatial variability in shallow and deep water populations of the invasive Caulerpa racemosa var. cylindracea in the western Mediterranean. Estuar. Coast. Shelf Sci., 83: 469-474. http://dx.doi.org/10.1016/j.ecss.2009.04.026
Cecherelli, G. and D. Campo. – 2002. Different effects of Caulerpa racemosa on two co-ocurring seagrasses in the Mediterranean. Bot. Mar., 45: 71-76. http://dx.doi.org/10.1515/BOT.2002.009
Chisholm, J.R.M. and J.M. Jaubert. – 1997. Photoautotrophic metabolism of Caulerpa taxifolia (Chlorophyta) in the NW Mediterranean. Mar. Ecol. Prog. Ser., 153: 113-123. http://dx.doi.org/10.3354/meps153113
Dunton, K.H. and D.M. Shell. – 1986. Seasonal carbon budget and growth of Laminaria solidungula in the Alaskan High Artic. Mar. Ecol. Prog. Ser., 31: 57-66. http://dx.doi.org/10.3354/meps031057
Falkowski, P.G. and J.A. Raven. – 1997. Aquatic photosynthesis. Blackwell Scientific Publishers, Oxford.
Flagella, M.M., M. Lorenti and M.C. Buia. – 2008. Temperature response in a shallow-water Mediterranean population of Caulerpa racemosa var. cylindracea (Caulerpales, Chloropyta), and a possible strategy of season anticipation. Bot. Mar., 51(4): 278-284. http://dx.doi.org/10.1515/BOT.2008.037
Gacia, E., C. Rodríguez-Prieto, O. Delgado and E. Ballesteros. – 1996. Seasonal light and temperature responses of Caulerpa taxifolia from northwestern Mediterranean. Aquat. Bot., 53: 215-225. http://dx.doi.org/10.1016/0304-3770(95)01001-7
Gatusso, J.P. and J. Jaubert. – 1985. Photosynthesis and respiration of Caulerpa racemosa (Chlorophyceae, Caulerpales) grown in aquaria: Effects of light and temperature. Bot. Mar., 28: 327-332. http://dx.doi.org/10.1515/botm.1985.28.8.327
Gómez, I., G. Weykam, H. Klöser and C. Wiencke. – 1997. Photosynthetic light requirements, metabolic carbon balance and zonation of sublittoral macroalgae from King George Island (Antarctica). Mar. Ecol. Prog. Ser., 148: 281-293. http://dx.doi.org/10.3354/meps148281
Gómez, I. – 2001. Ecophysiology of antartic macroalgae: effects of environmental light conditions on photosynthetic metabolism. Rev. Chil. Hist. Nat., 74: 251-271.
Johansson, G. and P. Snoeijs. – 2002. Macroalgal photosynthetic responses to light in relation to thallus morphology and depth zonation. Mar. Ecol. Prog. Ser., 244: 63-72. http://dx.doi.org/10.3354/meps244063
Kirk, J.T. – 1994. Light and Photosynthesis in Aquatic Ecosystems. Cambrige University Press. Cambridge.
Klein, J. and M. Verlaque. – 2008. The Caulerpa racemosa invasion. A critical review. Mar. Poll. Bull., 56: 205-225. http://dx.doi.org/10.1016/j.marpolbul.2007.09.043 PMid:18061625
Klein, J.and M. Verlaque. – 2009. Macroalgal assemblages of disturbed coastal detritic bottoms subject to invasive species. Estuar. Coast. Shelf Sci., 82: 461-468. http://dx.doi.org/10.1016/j.ecss.2009.02.003
Littler, M.M., D.S. Littler, S.M. Blair and J.N. Norris. – 1986. Deep-water plant communities from an unchartered seamount off San Salvador Island, Bahamas: distribution, abundance and primary productivity. Deep-Sea Res., I 33: 881-892. http://dx.doi.org/10.1016/0198-0149(86)90003-8
Lobban, C.S. and P.J. Harrison. – 1997. Seaweed ecology and physiology. Cambridge University Press, Cambridge.
Matta, J.L. and D.J.Chapman. – 1991. Photosynthetic responses and daily carbon balance of Colpomenia peregrina: seasonal variations and differences between intertidal and subtidal populations. Mar. Biol., 108: 303-313. http://dx.doi.org/10.1007/BF01344345
Markager, S. and K. Sand-Jensen. – 1992. Light requirements and depth zonation of marine macroalgae. Mar. Ecol. Prog. Ser., 88: 83-92. http://dx.doi.org/10.3354/meps088083
Markager, S. and K. Sand-Jensen. – 1994. The physiology and ecology of light-growth relationships in macroalgae. In: F.E. Round and D.J. Chapman (eds.), Progress in Phycological Research, pp. 209-298. Biopress, Bristol.
Ohba, H., H. Nashima and S. Enomoto. – 1992. Culture studies on Caulerpa (Caulerpales, Chlorophyceae) III. Reproduction, development and morphological variation of laboratory-cultured C. racemosa var. peltata. Bot. Mag. Tok., 105: 589-600. http://dx.doi.org/10.1007/BF02489433
Pérez-Lloréns, J.L., J.J. Vergara, R.R. Pino, I. Hernández, G. Peralta and F.X. Niell. – 1996. The effect of photoacclimation on the photosynthetic physiology of Ulva curvata and Ulva rotundata (Ulvales, Chlorophyta). Eur. J. Phycol., 31: 349-359. http://dx.doi.org/10.1080/09670269600651581
Peterson, R.D. – 1972. Effects of light intensity on the morphology and productivity of Caulerpa racemosa (Forskål) J. Agardh. Micronesica, 8: 63-86.
Piazzi, L., G. Cecherelli. and F. Cinelli. – 2001. Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar. Ecol. Prog. Ser., 210: 149-159. http://dx.doi.org/10.3354/meps210149
Piazzi, L., A. Meinesz and M. Verlaque. – 2005. Invasion of Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) in the Mediterranean Sea: an assessment of the spread. Cryptog. Algol., 26: 189-202.
Piazzi, L. and D. Balata. – 2008. The spread of Caulerpa racemosa var. cylindracea in the Mediterranean Sea: An example of how biological invasions can influence beta diversity. Mar. Environ. Res., 65: 50-61. http://dx.doi.org/10.1016/j.marenvres.2007.07.002 PMid:17904216
Quinn, G.P. and M.J. Keough. – 2002. Experimental designs and data analysis for biologists. Cambridge University Press, Cambridge.
Ramus, J., F. Lemons and C. Zimmerman. – 1977. Adaptation of light-harvesting pigments to downwelling light and the consequent photosynthetic performance of the eulittoral rockweeds Ascophyllum nodosum and Fucus vesiculosus . Mar. Biol., 42(4): 293-303. http://dx.doi.org/10.1007/BF00402191
Raniello, R., M. Lorenti, C. Brunet and M.C. Buia. – 2004. Photosynthetic plasticity of an invasive variety of Caulerpa racemosa in a coastal Mediterranean area: light harvesting capacity and seasonal acclimatation. Mar. Ecol. Prog. Ser., 271: 113-120. http://dx.doi.org/10.3354/meps271113
Raniello, R., M. Lorenti, C. Brunet and M.C. Buia. – 2006. Photoacclimation of the invasive alga Caulerpa racemosa var. cylindracea to depth and daylight patterns and a putative new role for siphonaxanthin. Mar. Ecol., 27: 20-30. http://dx.doi.org/10.1111/j.1439-0485.2006.00080.x
Riechert, R. and C.J. Dawes. – 1986. Acclimation of the green alga Caulerpa racemosa var. uvifera to light. Bot. Mar., 29: 533-537. http://dx.doi.org/10.1515/botm.1986.29.6.533
Robledo, D. and Y. Freile-Pelegrín. – 2005. Seasonal variations in photosynthesis and biochemical composition of Caulerpa spp (Bryopsidales, Chlorophyta) from the Gulf of Mexico. Phycologia, 44: 312-319. http://dx.doi.org/10.2216/0031-8884(2005)44[312:SVIPAB]2.0.CO;2
Rosenberg, G., D.S. Littler, M.M. Littler and C. Oliveira. – 1995. Primary production and photosynthetic quotients of seaweeds from Sao Paulo State, Brazil. Bot. Mar., 38: 369-377. http://dx.doi.org/10.1515/botm.1995.38.1-6.369
Ruitton, S., M. Verlaque and C.F. Boudouresque. – 2005. Seasonal changes of the introduced Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) at the northwest limit of its Mediterranean range. Aquat. Bot., 82: 55-70. http://dx.doi.org/10.1016/j.aquabot.2005.02.008
Ruitton, S., M. Verlaque, G. Aubin and C.F. Boudouresque. – 2006. Grazing on Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) in the Mediterranean Sea by herbivorous fishes and sea urchins. Vie Milieu, 56: 33-41.
Ruiz, J.M. and J. Romero. – 2001. Effects of in situ experimental shading on the Mediterranean seagrass Posidonia oceanica. Mar. Ecol. Prog. Ser., 215: 107-120. http://dx.doi.org/10.3354/meps215107
Ruiz, J.M., L. Marín-Guirao, J. Bernardeau-Esteller, A. Ramos-Segura, R. García-Muñoz and J.M. Sandoval-Gil. – 2011. Spread of the invasive alga Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) along the Mediterranean coast of the Murcia Region (SE Spain). Anim. Bio. Cons., 34: 73-82.
Terrados, J. and J.D. Ros. – 1992. The influence of temperature on seasonal variation of Caulerpa prolifera (Forsskal) Lamouroux photosynthesis and respiration. J. Exp. Mar. Biol. Ecol., 162: 199-212. http://dx.doi.org/10.1016/0022-0981(92)90201-K
Tomas, F., E. Cebrian and E. Ballesteros. – 2011. Differential herbivory of invasive algae by native fish in the Mediterranean Sea. Estuar. Coast. Shelf Sci., 92: 27-34. http://dx.doi.org/10.1016/j.ecss.2010.12.004
Streftaris, N. and A. Zenetos. – 2006. Alien Marine Species in the Mediterranean – the 100 ‘Worst Invasives’ and their impact. Medit. Mar. Sci., 7(1): 87-118.
Vázquez-Luis, M., P. Sánchez-Jerez and J.T. Bayle-Sempere. – 2008. Changes in amphipod (Crustacea) assemblages associated with shallow-water algal habitats invaded by Caulerpa racemosa var. cylindracea in the western Mediterranean Sea. Mar. Environ. Res., 65: 416-426 http://dx.doi.org/10.1016/j.marenvres.2008.01.006 PMid:18342365
Verlaque, M., C. Durand, J.M. Huisman, C.F. Boudouresque and Y. Le Parco. – 2003. On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta). Eur. J. Phycol., 38: 325-339. http://dx.doi.org/10.1080/09670260310001612592
Walker, D.A. – 1985. Measurement of oxygen and chlorophyll fluorescence. In: J. Coombs, D.O. Hall, S.P. Long and J.M.O. Scurlock (eds.), Techniques in bioproductivity and photosynthesis. Pergamon Press, Oxford.
Williams, S.L. and W.C. Dennison. – 1990. Light availability and diurnal growth of a green macroalga (Caulerpa cupressoides) and a seagrass (Halophila decipiens). Mar. Biol., 196: 437-443. http://dx.doi.org/10.1007/BF01344324
Yokohama, Y. and T. Misonou. – 1980. Chlorophyll a:b ratios in marine benthic algae. Jap. J. Phycol., 28: 219-223.
Zimmerman, R.C., A. Capello-Pasini and R.S. Alberte. – 1994. Modeling daily production of aquatic macrophytes from irradiance measurements: a comparative analysis. Mar. Ecol. Prog. Ser., 114: 185-196. http://dx.doi.org/10.3354/meps114185
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