Geographically distinct Ceratophyllum demersum populations differ in growth, photosynthetic responses and phenotypic plasticity to nitrogen availability
Benita Hyldgaard A B , Brian Sorrell A , Birgit Olesen A , Tenna Riis A and Hans Brix A
+ Author Affiliations
- Author Affiliations
A Department of Bioscience, Plant Biology, Aarhus University, Ole Worms Allé 1, Building 1135, 8000 Aarhus C, Denmark.
B Corresponding author. Email: benita.hyldgaard@biology.au.dk
Functional Plant Biology 39(9) 774-783 https://doi.org/10.1071/FP12068
Submitted: 28 February 2012 Accepted: 10 July 2012 Published: 27 August 2012
Abstract
Two geographically distinct populations of the submerged aquatic macrophyte Ceratophyllum demersum L. were compared after acclimation to five different nitrogen concentrations (0.005, 0.02, 0.05, 0.1 and 0.2 mM N) in a common garden setup. The two populations were an apparent invasive population from New Zealand (NZ) and a noninvasive population from Denmark (DK). The populations were compared with a focus on both morphological and physiological traits. The NZ population had higher relative growth rates (RGRs) and photosynthesis rates (Pmax) (range: RGR, 0.06–0.08 per day; Pmax, 200–395 µmol O2 g–1 dry mass (DM) h–1) compared with the Danish population (range: RGR, 0.02–0.05 per day; Pmax, 88–169 µmol O2 g–1 DM h–1). The larger, faster-growing NZ population also showed higher plasticity than the DK population in response to nitrogen in traits important for growth. Hence, the observed differences in growth behaviour between the two populations are a result of genetic differences and differences in their level of plasticity. Here, we show that two populations of the same species from similar climates but different geographical areas can differ in several ecophysiological traits after growth in a common garden setup.
Additional keywords: acclimation, hornwort, phenotypic plasticity, photosynthesis, submerged macrophyte.
References
Allen ED, Spence DHN (1981) The differential ability of aquatic plants to utilize the inorganic carbon supply in fresh waters. New Phytologist 87, 269–283.| The differential ability of aquatic plants to utilize the inorganic carbon supply in fresh waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlt12ltbY%3D&md5=773dc81d2b976bde1ec1d0826a134284CAS |
Atkin OK, Loveys BR, Atkinson LJ, Pons TL (2006) Phenotypic plasticity and growth temperature: understanding interspecific variability. Journal of Experimental Botany 57, 267–281.
| Phenotypic plasticity and growth temperature: understanding interspecific variability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFKnsg%3D%3D&md5=bc8d68dea1808b40ff98b85be7d7dd3fCAS |
Baruch Z, Goldstein G (1999) Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii. Oecologia 121, 183–192.
| Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii.Crossref | GoogleScholarGoogle Scholar |
Clayton J, Edwards T (2006) Aquatic plants as environmental indicators of ecological condition in New Zealand lakes. Hydrobiologia 570, 147–151.
| Aquatic plants as environmental indicators of ecological condition in New Zealand lakes.Crossref | GoogleScholarGoogle Scholar |
Clevering OA, Brix H, Lukavská J (2001) Geographic variation in growth responses in Phragmites australis. Aquatic Botany 69, 89–108.
| Geographic variation in growth responses in Phragmites australis.Crossref | GoogleScholarGoogle Scholar |
Cook CDK (1990) Origin, autecology, and spread of some of the world’s most troublesome aquatic weeds. In ‘Aquatic weeds: the ecology and management of nuisance aquatic vegetation’. (Eds AH Pieterse, KJ Murphy) pp. 31–38. (Oxford University Press: New York)
Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecology Letters 14, 419–431.
| Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Dawson FH, Warman EA (1987) Crassula helmsii (T. Kirk) cockayne: is it an aggressive alien aquatic plant in Britain? Biological Conservation 42, 247–272.
| Crassula helmsii (T. Kirk) cockayne: is it an aggressive alien aquatic plant in Britain?Crossref | GoogleScholarGoogle Scholar |
de Winton MD, Champion PD, Clayton JS, Wells RDS (2009) Spread and status of seven submerged pest plants in New Zealand lakes. New Zealand Journal of Marine and Freshwater Research 43, 547–561.
| Spread and status of seven submerged pest plants in New Zealand lakes.Crossref | GoogleScholarGoogle Scholar |
Duarte CM (1992) Nutrient concentration of aquatic plants – patterns across species. Limnology and Oceanography 37, 882–889.
| Nutrient concentration of aquatic plants – patterns across species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmsFSmu74%3D&md5=2d7e554d05be78d9127b96cea94a7d36CAS |
Durand LZ, Goldstein G (2001) Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii. Oecologia 126, 345–354.
| Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii.Crossref | GoogleScholarGoogle Scholar |
Eggert A, Visser RJW, Van Hasselt PR, Breeman AM (2006) Differences in acclimation potential of photosynthesis in seven isolates of the tropical to warm temperate macrophyte Valonia utricularis (Chlorophyta). Phycologia 45, 546–556.
| Differences in acclimation potential of photosynthesis in seven isolates of the tropical to warm temperate macrophyte Valonia utricularis (Chlorophyta).Crossref | GoogleScholarGoogle Scholar |
Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446, 1079–1081.
| Resource-use efficiency and plant invasion in low-resource systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksFekurc%3D&md5=4f45cd652bc12cb24a196e7cc93edcabCAS |
Goulder R, Boatman DJ (1971) Evidence that nitrogen supply influences the distribution of a freshwater macrophyte, Ceratophyllum demersum. Journal of Ecology 59, 783–791.
| Evidence that nitrogen supply influences the distribution of a freshwater macrophyte, Ceratophyllum demersum.Crossref | GoogleScholarGoogle Scholar |
Hansen DL, Lambertini C, Jampeetong A, Brix H (2007) Clone-specific differences in Phragmites australis: effects of ploidy level and geographic origin. Aquatic Botany 86, 269–279.
| Clone-specific differences in Phragmites australis: effects of ploidy level and geographic origin.Crossref | GoogleScholarGoogle Scholar |
Hulme PE (2008) Phenotypic plasticity and plant invasions: is it all Jack? Functional Ecology 22, 3–7.
| Phenotypic plasticity and plant invasions: is it all Jack?Crossref | GoogleScholarGoogle Scholar |
Hyldgaard B, Brix H (2012) Intraspecies differences in phenotypic differences: invasive versus non-invasive populations of Ceratophyllum demersum. Aquatic Botany 97, 49–56.
| Intraspecies differences in phenotypic differences: invasive versus non-invasive populations of Ceratophyllum demersum.Crossref | GoogleScholarGoogle Scholar |
Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnology and Oceanography 21, 540–547.
| Mathematical formulation of the relationship between photosynthesis and light for phytoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XlvVaisbc%3D&md5=7d72287c031c8993061625b4867cc9ecCAS |
Kennedy TL, Horth LA, Carr DE (2009) The effects of nitrate loading on the invasive macrophyte Hydrilla verticillata and two common, native macrophytes in Florida. Aquatic Biology 91, 253–256.
| The effects of nitrate loading on the invasive macrophyte Hydrilla verticillata and two common, native macrophytes in Florida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVKntbfJ&md5=9c55e111298fbbce520d9943abe30429CAS |
Les DH (1989) The evolution of achene morphology in Ceratophyllum (Ceratophyllaceae), IV. Summary of proposed relationships and evolutionary trends. Systematic Botany 14, 254–262.
| The evolution of achene morphology in Ceratophyllum (Ceratophyllaceae), IV. Summary of proposed relationships and evolutionary trends.Crossref | GoogleScholarGoogle Scholar |
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
| Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhs1Cgu78%3D&md5=46881071f2fd7b31c9d89c1d4bdb8a57CAS |
Lockwood JL, Hoopes MF, Marchetti MP (2007) ‘Invasion ecology.’ (Blackwell Publishing Ltd.: Oxford, UK)
Maron JL, Vilà M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecological Monographs 74, 261–280.
| Rapid evolution of an invasive plant.Crossref | GoogleScholarGoogle Scholar |
McKinley DC, Blair JM (2008) Woody plant encroachment by Juniperus virginiana in a semiarid native grassland promotes rapid carbon and nitrogen accrual. Ecosystems 11, 454–468.
| Woody plant encroachment by Juniperus virginiana in a semiarid native grassland promotes rapid carbon and nitrogen accrual.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltlSnu7g%3D&md5=dc025f10a5feb59d9866b716c36289e2CAS |
Pattison RR, Goldstein G, Ares A (1998) Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. Oecologia 117, 449–459.
| Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species.Crossref | GoogleScholarGoogle Scholar |
Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters 9, 981–993.
| Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions.Crossref | GoogleScholarGoogle Scholar |
Richardson DM, Pysek P, Rejmanek M, Barbour MG, Panetta FD, West CJ (2000) Naturalization and invasion of alien plants: concepts and definitions. Diversity & Distributions 6, 93–107.
| Naturalization and invasion of alien plants: concepts and definitions.Crossref | GoogleScholarGoogle Scholar |
Riis T, Lambertini C, Olesen B, Clayton JS, Brix H, Sorrell BK (2010) Invasion strategies in clonal aquatic plants: are phenotypic differences caused by phenotypic plasticity or local adaptation? Annals of Botany 106, 813–822.
| Invasion strategies in clonal aquatic plants: are phenotypic differences caused by phenotypic plasticity or local adaptation?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCltLzI&md5=a58382c497e2e48d9dc33765835ab881CAS |
Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annual Review of Ecology and Systematics 32, 305–332.
| The population biology of invasive species.Crossref | GoogleScholarGoogle Scholar |
Sand-Jensen K (1989) Environmental variables and their effect on photosynthesis of aquatic plant communities. Aquatic Botany 34, 5–25.
| Environmental variables and their effect on photosynthesis of aquatic plant communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXltlSltL0%3D&md5=1205f203b28e804e83751edfd8612e9cCAS |
Santamaría L, Figuerola J, Pilon JJ, Mjelde M, Green AJ, De Boer T, King RA, Gornall RJ (2003) Plant performance across latitude: the role of plasticity and local adaptation in an aquatic plant. Ecology 84, 2454–2461.
| Plant performance across latitude: the role of plasticity and local adaptation in an aquatic plant.Crossref | GoogleScholarGoogle Scholar |
Schwarz AM, Hawes I, Howard-Williams C (1996) The role of photosynthesis/light relationships in determining lower depth limits of Characeae in South Island, New Zealand lakes. Freshwater Biology 35, 69–80.
| The role of photosynthesis/light relationships in determining lower depth limits of Characeae in South Island, New Zealand lakes.Crossref | GoogleScholarGoogle Scholar |
Smart MR, Barko JW (1985) Laboratory culture of submersed freshwater macrophytes on natural sediments. Aquatic Botany 21, 251–263.
| Laboratory culture of submersed freshwater macrophytes on natural sediments.Crossref | GoogleScholarGoogle Scholar |
Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends in Plant Science 5, 537–542.
| Phenotypic plasticity for plant development, function and life history.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7gvVenuw%3D%3D&md5=f3effe5a6531cd544687f90f478c051fCAS |
Valladares F, Sanchez-Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. Journal of Ecology 94, 1103–1116.
| Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications.Crossref | GoogleScholarGoogle Scholar |
Weiner J, Campbell L, Pino J, Echarte L (2009) The allometry of reproduction within plant populations. Journal of Ecology 97, 1220–1233.
| The allometry of reproduction within plant populations.Crossref | GoogleScholarGoogle Scholar |
