ESTONIAN ACADEMY
PUBLISHERS
eesti teaduste
akadeemia kirjastus
PUBLISHED
SINCE 1952
 
Proceeding cover
proceedings
of the estonian academy of sciences
ISSN 1736-7530 (Electronic)
ISSN 1736-6046 (Print)
Impact Factor (2020): 1.045

Effect of short-term elevated nutrients and mesoherbivore grazing on photosynthesis of macroalgal communities; pp. 93–103

Full article in PDF format | doi: 10.3176/proc.2014.1.12

Authors
Merli Pärnoja, Jonne Kotta, Helen Orav-Kotta

Abstract

Marine macroalgal communities are among the most productive habitats worldwide. They provide energy and matter to higher trophic levels and support other important functions for ecosystems and services for human society. To date it is not clear to what extent irradiance, nutrient loading, and mesoherbivores regulate the primary productivity of a community. In a factorial field experiment we evaluated the interactive effect of short-term pulses of elevated nutrients and of the activity of grazers on the photosynthesis (in terms of the rate of oxygen production per unit mass) of communities dominated by the perennial Fucus vesiculosus and the ephemeral Cladophora glomerata in the northern Baltic Sea. This experimental manipulation had no effect on the community dominated by F. vesiculosus. A 12-hour addition of herbivores decreased the photosynthetic production of the macroalgal community dominated by C. glomerata in spring but increased its production in summer. The simultaneous addition of nutrients and herbivores in summer reversed the effect. A 4-times longer manipulation had no effect on the C. glomerata production. Differences in the responses between separate and interactive effects imply that the photosynthetic production of a community cannot be predicted by separate effects of the same variables. Our experiment also indicated that macroalgal communities dominated by F. vesiculosus covered by epiphytic macrophytes performed stably under different stress regimes and could buffer moderate short-term disturbances due to elevated nutrient loads and/or herbivory of either natural or human origin.


References

 

Bergström, L., Berger, R., and Kautsky, L. 2003. Negative direct effects of nutrient enrichment on the establish­ment of Fucus vesiculosus in the Baltic Sea. Eur. J. Phycol., 38, 41–46.
http://dx.doi.org/10.1080/0967026031000096236

Binzer, T. and Middelboe, A. L. 2005. From thallus to communities: scale effects and photosynthetic per­formance in macroalgae communities. Mar. Ecol. Prog. Ser., 287, 65–75.
http://dx.doi.org/10.3354/meps287065

Binzer, T. and Sand-Jensen, K. 2002. Production in aquatic macrophyte communities: a theoretical and empirical study of the influence of spatial light distribution. Limnol. Oceanogr., 47, 1742–1750.
http://dx.doi.org/10.4319/lo.2002.47.6.1742

Binzer, T., Sand-Jensen, K., and Middelboe, A. L. 2006. Community photosynthesis of aquatic macrophytes. Limnol. Oceanogr., 51, 2722–2733.
http://dx.doi.org/10.4319/lo.2006.51.6.2722

Bracken, M. E. S. and Nielsen, K. J. 2004. Diversity of intertidal macroalgae increases with nitrogen loading by invertebrates. Ecology, 85, 2828–2836.
http://dx.doi.org/10.1890/03-0651

Bracken, M. E. S., Gonzalez-Dorantes, C. A., and Stacho­wicz, J. J. 2007. Whole-community mutualism: associated invertebrates facilitate a dominant habitat-forming seaweed. Ecology, 88, 2211–2219.
http://dx.doi.org/10.1890/06-0881.1

Carpenter, R. C. 1985. Relationships between primary pro­duction and irradiance in coral reef algal communities. Limnol. Oceanogr., 30, 784–793.
http://dx.doi.org/10.4319/lo.1985.30.4.0784

Chalup, M. S. and Laws, E. A. 1990. A test of the assumptions and predictions of recent microalgal growth models with the marine phytoplankter Pavlova lutheri. Limnol. Oceanogr., 30, 583–596.
http://dx.doi.org/10.4319/lo.1990.35.3.0583

Cheshire, A. C., Westphalen, G., Wenden, A., Scriven, L. J., and Rowland, B. C. 1996. Photosynthesis and respira­tion of phaeophycean-dominated macroalgal communities in summer and winter. Aquat. Bot., 55, 159–170.
http://dx.doi.org/10.1016/S0304-3770(96)01071-6

Copertino, M. S., Cheshire, A., and Waitling, J. 2006. Photo­inhibition and photoacclimation of turf algal communities on a temperate reef, after in situ trans­plantation experiments. J. Phycol., 42, 580–592.
http://dx.doi.org/10.1111/j.1529-8817.2006.00222.x

Dodds, W. K. 1991. Community interactions between the filamentous alga Cladophora glomerata (L.) Kuetzing, its epiphytes, and epiphyte grazers. Oecologia, 85, 572–580.
http://dx.doi.org/10.1007/BF00323770

Duffy, J. E. and Hay, M. E. 2000. Strong impacts of grazing amphipods on the organization of a benthic community. Ecol. Monogr., 70, 237–263.
http://dx.doi.org/10.1890/0012-9615(2000)070[0237:SIOGAO]2.0.CO;2

Elser, J. J., Bracken, M. E. S., Cleland, E. E., Gruner, D. S., Harpole, W. S., Hillebrand, H. et al. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett., 10, 1135–1142.
http://dx.doi.org/10.1111/j.1461-0248.2007.01113.x

Ensminger, I., Hagen, C., and Braune, W. 2000. Strategies providing success in a variable habitat: II. Eco­physiology of photosynthesis of Cladophora glomerata. Plant Cell Environ., 23, 1129–1136.
http://dx.doi.org/10.1046/j.1365-3040.2000.00619.x

Falkowski, P. G. and LaRoche, J. 1991. Acclimation to spectral irradiance in algae. J. Phycol., 27, 8–14.
http://dx.doi.org/10.1111/j.0022-3646.1991.00008.x

Field, C. B., Behrenfeld, M. J., Randerson, J. T., and Fal­kowski, P. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science, 281, 237–240.
http://dx.doi.org/10.1126/science.281.5374.237

Fong, P., Fong, J. J., and Fong, C. R. 2004. Growth, nutrient storage, and release of dissolved organic nitrogen by Enteromorpha intestinalis in response to pulses of nitrogen and phosphorus. Aquat. Bot., 78, 83–95.
http://dx.doi.org/10.1016/j.aquabot.2003.09.006

Fujita, R. M. and Edwards, R. L. 1989. Assessment of macro­algal nitrogen limitation in a seasonal upwelling region. Mar. Ecol. Prog. Ser., 53, 293–303.
http://dx.doi.org/10.3354/meps053293

Häder, D.-P. and Figueroa, F. L. 1997. Photoecophysiology of marine macroalgae. Photochem. Photobiol., 66, 1­–14.
http://dx.doi.org/10.1111/j.1751-1097.1997.tb03132.x

Hauxwell, J., McClelland, J., Behr, P. J., and Valiela, I. 1998. Relative importance of grazing and nutrient controls of macroalgal biomass in three temperate shallow estuaries. Estuaries, 21, 347–360.
http://dx.doi.org/10.2307/1352481

Hayward, P. J. 1988. Animals on Seaweeds. Richmond Publish­ing Company, Richmond.

Hemmi, A., Mäkinen, A., Jormalainen, V., and Honkanen, T. 2005. Responses of growth and phlorotannins in Fucus vesiculosus to nutrient enrichment and herbivory. Aquat. Ecol., 39, 201–211.
http://dx.doi.org/10.1007/s10452-004-3526-z

Johansson, G. and Snoeijs, P. 2002. Macroalgal photosynthetic responses to light in relation to thallus morphology and depth zonation. Mar. Ecol. Prog. Ser., 224, 63–72.
http://dx.doi.org/10.3354/meps244063

Kevekordes, K. 2001. Toxicity tests using developmental stages of Hormosira banksii (Phaeophyta) identify ammonium as a damaging component of secondary treated sewage effluent discharged into Bass Strait, Victoria, Australia. Mar. Ecol. Prog. Ser., 219, 139–148.
http://dx.doi.org/10.3354/meps219139

Kikvidze, Z., Khetsuriani, L., Kikodze, D., and Calla­way, R. M. 2006. Seasonal shifts in competition and facilitation in subalpine plant communities of the central Caucasus. J. Veg. Sci., 17, 77–82.
http://dx.doi.org/10.1111/j.1654-1103.2006.tb02425.x

King, R. J. and Schramm, W. 1976. Photosynthetic rates of benthic marine algae in relation to light intensity and seasonal variations. Mar. Biol., 37, 215–222.
http://dx.doi.org/10.1007/BF00387606

Kotta, J. and Orav, H. 2001. Role of benthic macroalgae in regulating macrozoobenthic assemblages in the Väina­meri (north-eastern Baltic Sea). Ann. Zool. Fennici, 38, 163–171.

Kotta, J. and Witman, J. 2009. Regional-scale patterns. In Marine Hard Bottom Communities (Wahl, M., ed.), pp. 89–99. Springer-Verlag, Berlin, Heidelberg.
http://dx.doi.org/10.1007/b76710_6

Kotta, J., Paalme, T., Martin, G., and Mäkinen, A. 2000. Major changes in macroalgae community composition affect the food and habitat preference of Idotea baltica. Int. Rev. Hydrobiol., 85, 693–701.
http://dx.doi.org/10.1002/1522-2632(200011)85:5/6<697::AID-IROH697>3.0.CO;2-0

Kotta, J., Torn, K., Martin, G., Orav-Kotta, H., and Paalme, T. 2004. Seasonal variation of invertebrate grazing on Chara connivens and C. tomentosa in Kõiguste Bay, NE Baltic Sea. Helgoland Mar. Res., 58, 71–76.
http://dx.doi.org/10.1007/s10152-003-0170-2

Kotta, J., Orav-Kotta, H., Paalme, T., Kotta, I., and Kukk, H. 2006. Seasonal changes in situ grazing of the meso­herbivores Idotea baltica and Gammarus oceanicus on the brown algae Fucus vesiculosus and Pylaiella littoralis in the central Gulf of Finland, Baltic Sea. Hydrobiologia, 554, 117–125.
http://dx.doi.org/10.1007/s10750-005-1011-x

Kotta, J., Lauringson, V., Martin, G., Simm, M., Kotta, I., Herkül, K., and Ojaveer, H. 2008a. Gulf of Riga and Pärnu Bay. In Ecology of Baltic Coastal Waters (Schiewer, U., ed.), pp. 217–243. Springer-Verlag, Berlin, Heidelberg.
http://dx.doi.org/10.1007/978-3-540-73524-3_10

Kotta, J., Paalme, T., Püss, T., Herkül, K., and Kotta, I. 2008b. Contribution of scale-dependent environmental vari­ability on the biomass patterns of drift algae and associated invertebrates in the Gulf of Riga, northern Baltic Sea. J. Mar. Syst., 74, S116–S123.
http://dx.doi.org/10.1016/j.jmarsys.2008.03.030

Kotta, J., Orav-Kotta, H., and Herkül, K. 2010. Separate and combined effects of habitat-specific fish predation on the survival of invasive and native gammarids. J. Sea Res., 64, 369–372.
http://dx.doi.org/10.1016/j.seares.2010.05.006

Lapointe, B. E. 1985. Strategies for pulsed nutrient supply to Gracilaria cultures in the Florida Keys: interactions between concentration and frequency of nutrient pulses. J. Exp. Mar. Biol. Ecol., 93, 211–222.
http://dx.doi.org/10.1016/0022-0981(85)90240-0

Lauringson, V. and Kotta, J. 2006. Influence of the thin drift algal mats on the distribution of macrozoobenthos in Kõiguste Bay, NE Baltic Sea. Hydrobiologia, 554, 97–105.
http://dx.doi.org/10.1007/s10750-005-1009-4

Lester, W. W., Adams, M. S., and Farmer, A. M. 1988. Effects of light and temperature on photosynthesis of the nuisance alga Cladophora glomerata (L.) Kutz from Green Bay, Lake Michigan. New Phytol., 109, 53–58.
http://dx.doi.org/10.1111/j.1469-8137.1988.tb00218.x

Littler, M. M. 1980. Morphological form and photosynthetic performances of marine macroalgae: tests of a functional/form hypothesis. Bot. Mar., 22, 161–165.

Lobban, C. S. and Harrison, P. J. 1994. Seaweed Ecology and Physiology. Cambridge University Press, Cambridge.
http://dx.doi.org/10.1017/CBO9780511626210

Lundberg, P., Weich, R. G., Jensén, P., and Vogel, H. 1989. Phosphorus-31 and nitrogen-14 NMR studies on the uptake of phosphorus and nitrogen compounds in the marine macroalgae Ulva lactuca. Plant Physiol., 89, 1380–1387.
http://dx.doi.org/10.1104/pp.89.4.1380

Mann, K. H. 2000. Ecology of Coastal Waters: With Implica­tions for Management. Blackwell Science, Massachusetts.

Middelboe, A. L. and Binzer, T. 2004. Importance of canopy structure on photosynthesis in single- and multi-species assemblages of marine macroalgae. Oikos, 107, 422–432.
http://dx.doi.org/10.1111/j.0030-1299.2004.13345.x

Middelboe, A. L., Sand-Jensen, K., and Binzer, T. 2006. Highly predictable photosynthetic production in natural macroalgal communities from incoming and absorbed light. Oecologia, 150, 464–476.
http://dx.doi.org/10.1007/s00442-006-0526-9

Necchi, O. 2006. Photosynthetic responses to temperature in tropical lotic macroalgae. Phycol. Res., 52, 140–148.
http://dx.doi.org/10.1111/j.1440-1835.2004.tb00322.x

Orav-Kotta, H. and Kotta, J. 2004. Food and habitat choice of the isopod Idotea baltica in the northeastern Baltic Sea. Hydrobiologia, 514, 79–85.
http://dx.doi.org/10.1023/B:hydr.0000018208.72394.09

Orav-Kotta, H., Kotta, J., Herkül, K., Kotta, I., and Paalme, T. 2009. Seasonal variability in the grazing potential of the invasive amphipod Gammarus tigrinus and the native amphipod Gammarus salinus in the northern Baltic Sea. Biol. Invasions, 11, 597–608.
http://dx.doi.org/10.1007/s10530-008-9274-6

Paalme, T., Kukk, H., Kotta, J., and Orav, H. 2002. ‘In vitro’ and ‘in situ’ decomposition of nuisance macroalgae Cladophora glomerata and Pilayella littoralis. Hydrobiologia, 475/476, 469–476.
http://dx.doi.org/10.1023/A:1020364114603

Pedersen, M. F. and Borum, J. 1996. Nutrient control of algal growth in estuarine waters. Nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macro­algae. Mar. Ecol. Prog. Ser., 142, 261–272.
http://dx.doi.org/10.3354/meps142261

Pickering, T. D., Gordon, M. E., and Tong, L. J. 1993. Effects of nutrient pulse concentration and frequency on growth of Gracilaria chilensis plants and levels of epiphytic algae. J. Appl. Phycol., 5, 525–533.
http://dx.doi.org/10.1007/BF02182511

Pugnaire, F. I. and Luque, M. T. 2003. Changes in plant interactions along a gradient of environmental stress. Oikos, 93, 42–49.
http://dx.doi.org/10.1034/j.1600-0706.2001.930104.x

Ridder, B. 2008. Questioning the ecosystem services argument for biodiversity conservation. Biodivers. Conserv., 17, 781–790.
http://dx.doi.org/10.1007/s10531-008-9316-5

Sala, E. and Graham, M. H. 2002. Community-wide distribu­tion of predator–prey interaction strength in kelp forests. Proc. Natl. Acad. Sci. USA, 99(6), 3678–3683.
http://dx.doi.org/10.1073/pnas.052028499

Sand-Jensen, K., Binzer, T., and Middelboe, A. L. 2007. Scal­ing of photosynthetic production of aquatic macro­phytes – a review. Oikos, 116, 280–294.
http://dx.doi.org/10.1111/j.2006.0030-1299.15093.x

Schaffelke, B. 1999. Short-term nutrient pulses as tools to assess responses of coral reef macroalgae to enhanced nutrient availability. Mar. Ecol. Prog. Ser., 182, 305–310.
http://dx.doi.org/10.3354/meps182305

Schmitz, O. J. 2008. Herbivory from individuals to eco­systems. Annu. Rev. Ecol. Evol. Syst., 39, 133–152.
http://dx.doi.org/10.1146/annurev.ecolsys.39.110707.173418

StatSoft, Inc. 2008. Electronic Statistics Textbook. StatSoft, Tulsa, OK, http://www.statsoft.com/Textbook (accessed 15. 08. 2008).

Stengel, D. B. and Dring, M. J. 1998. Seasonal variation in the pigment content and photosynthesis of different thallus regions of Ascophyllum nodosum (Fucales, Phaeophyta) in relation to position in the canopy. Phycologia, 37, 259–268.
http://dx.doi.org/10.2216/i0031-8884-37-4-259.1

Tait, L. W. and Schiel, D. R. 2011. Dynamics of productivity in naturally structured macroalgal assemblages: importance of canopy structure on light-use efficiency. Mar. Ecol. Prog. Ser., 421, 97–107.
http://dx.doi.org/10.3354/meps08909

Tomczak, M. T., Müller-Karulis, B., Järv, L., Kotta, J., Mar­tin, G., Minde, A. et al. 2009. Analysis of trophic networks and carbon flows in south-eastern Baltic coastal ecosystems. Prog. Oceanogr., 81, 111–131.
http://dx.doi.org/10.1016/j.pocean.2009.04.017

Turpin, D. H. 1991. Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J. Phycol., 27, 14–20.
http://dx.doi.org/10.1111/j.0022-3646.1991.00014.x

Wallentinus, I. 1978. Productivity studies on Baltic macro­algae. Bot. Mar., 21, 365–380.
http://dx.doi.org/10.1515/botm.1978.21.6.365

Wallentinus, I. 1984. Comparison of nutrient uptake rates for Baltic macroalgae with different thallus morphologies. Mar. Biol., 80, 215–225.
http://dx.doi.org/10.1007/BF02180189

Worm, B. and Sommer, U. 2000. Rapid direct and indirect effects of a single nutrient pulse in a seaweed–epiphyte–grazer system. Mar. Ecol. Prog. Ser., 202, 283–288.
http://dx.doi.org/10.3354/meps202283

Worm, B., Lotze, H. K., and Sommer, U. 2000. Coastal food web structure, carbon storage, and nitrogen retention regulated by consumer pressure and nutrient loading. Limnol. Oceanogr., 45, 339–349.
http://dx.doi.org/10.4319/lo.2000.45.2.0339

Ylla, I., Romani, A. M., and Sabater, S. 2007. Differential effects of nutrients and light on the primary production of stream algae and mosses. Fund. Appl. Limnol., 170, 1–10.
http://dx.doi.org/10.1127/1863-9135/2007/0170-001

 


Back to Issue