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Differences in the Growth and Physiological Response of Eight Aquatic Botany 139 (2017) 25–31 Contents lists available at ScienceDirect Aquatic Botany jou rnal homepage: www.elsevier.com/locate/aquabot Differences in the growth and physiological response of eight Myriophyllum species to carbon dioxide depletion a a,b,∗ Emin Dülger , Andreas Hussner a Stress Physiology and Photosynthesis of Plants, Heinrich-Heine-University, Düsseldorf, Germany b Institute of Botany, Heinrich-Heine-University, Düsseldorf, Germany a r a t i b s c t l e i n f o r a c t Article history: The growth and photosynthesis of submerged aquatic plants is often limited by the CO2 availability in − Received 27 June 2016 their habitats, but about 50% of all submerged plants are able to use HCO3 as an additional carbon Received in revised form 13 February 2017 − source. This ability to use HCO3 provides a competitive advantage over non-CO2-users under CO2 limit- Accepted 16 February 2017 ing conditions. Here, we studied the growth and physiological response of eight Myriophyllum species (M. Available online 21 February 2017 spicatum, M. triphyllum, M. heterophyllum, M. papillosum, M. variifolium, M. tetrandrum, M. tuberculatum, M. − − verticillatum) to CO2 and HCO3 use conditions. Physiologically, plants acclimated to HCO3 use showed Keywords: − higher net photosynthetic rates under both CO2 and HCO3 use conditions than plants grown under high CO2 and bicarbonate − Photosynthesis CO2 conditions. Furthermore, we found significant differences in the HCO3 use capacity between the Growth Myriophyllum species. The long-term exposure to high CO2 conditions during growth caused an accumu- Mass fraction lation of starch within the leaves, while the chlorophyll content decreased. Moreover, plants allocated Starch more biomass into roots and reduced the leaf biomass under CO2 enrichment. The growth rates illustrate − Pigments that M. spicatum is the most efficient HCO3 user out of the tested Myriophyllum species, followed by M. triphyllum and M. heterophyllum. The other five studied Myriophyllum species showed only a minor or no − − HCO3 use capacity. We conclude, that the HCO3 use capacity varies greatly even within a single genus, − and that the HCO3 use capacity, among others, is an important trait of strong competitive submerged plants. © 2017 Elsevier B.V. All rights reserved. 1. Introduction induced CO2 limitation in dense macrophyte stands (Santamaria, 2002). Aquatic plants have evolved various adaptations to cope The growth of submerged aquatic plants is determined by var- with CO2 depletion. Morphologically, their thin and fine dissected ious abiotic and biotic parameters, including temperature, light, leaves and the low chlorophyll content per surface area increase nutrients and carbon availability (Sand-Jensen, 1989). Unlike in ter- the diffusional uptake of CO2, and some submerged plants are able restrial habitats, the dissolved inorganic carbon (DIC) availability of to take up carbon via their root system (Winkel and Borum, 2009). freshwater ecosystems varies over a wide range between and even Physiologically, about 50% of all submerged plants have carbon con- within water bodies (Maberly et al., 2015), and the CO2 availability centration mechanisms, like the single cell C4 or the crassulaceen itself is influenced by the water pH, which determines the portion of acid metabolism (CAM) (Bowes, 2011). Long-term exposure to CO2 − 2− CO2, HCO3 and CO3 within the DIC pool (Pedersen et al., 2013). enrichment revealed, beside the effect of increased growth rates, Even though inland waters are often supersaturated with CO2 increased leaf dry matter content (LDMC, Hussner and Jahns, 2015), in comparison with water in equilibrium with the atmosphere decreased specific leaf area (Madsen et al., 1996) and increased (Raymond et al., 2013), the CO2 availability of freshwater habi- allocation of biomass to roots (Madsen et al., 1996; Hussner et al., tats often gets limited for submerged aquatic plants due to the low 2015, 2016). Moreover submerged plants acclimated to CO2 deple- CO2 diffusion rate in water and the high uptake of CO2 by primary tion had higher chlorophyll content (Hussner and Jahns, 2015) and − producers, which increases the water pH and can lead to self- increased affinities to both CO2 and HCO3 , but strong differences − in the HCO3 use capacity between species occur (Maberly and Madsen, 1998, 2002; Maberly et al., 2015; Hussner et al., 2016). Furthermore, even within a single species, the growth conditions ∗ − Corresponding author at: Universitätsstr. 1, Geb. 26.13.O2.R32, D-40225 Düs- affect the HCO3 affinity of plants (Madsen et al., 1996; Hussner seldorf, Germany. Tel.: +49 211 8114290. and Jahns, 2015). However, submerged macrophytes with the abil- E-mail address: [email protected] (A. Hussner). http://dx.doi.org/10.1016/j.aquabot.2017.02.008 0304-3770/© 2017 Elsevier B.V. All rights reserved. 26 E. Dülger, A. Hussner / Aquatic Botany 139 (2017) 25–31 cates the important role of the CO2 availability on submerged plant performance and the competitive strength of submerged plants. Within the genus Myriophyllum, recent studies revealed strong − differences in the HCO3 capacities of M. spicatum, M. aquaticum and M. heterophyllum and M. verticillatum (Maberly and Madsen, 2002; Eusebio Malheiro et al., 2013; Hussner and Jahns, 2015). In this study, we compare the growth and physiological acclimation of eight Myriophyllum species to ambient air CO2 and elevated CO2 conditions, including species known as strong competitors (M. spi- catum and M. heterophyllum) and six less competitive species (M. papillosum, M. tetrandum, M. triphyllum, M. tuberculatum, M. vari- ifolium and M. verticillatum). Besides the general effects on growth rate and physiology, we focused on various plant traits (dry mat- ter content and mass fractions) which have rarely been considered in aquatic plant research to date, but are widely accepted in ter- restrial plant research as indicators for plant growth responses to environmental changes (Poorter et al., 2012). Based on recent find- − ings, we hypothesize that (i) the capacity for HCO3 utilization varied strongly between the Myriophyllum spp., (ii) the acclimation − to CO2 or HCO3 use causes growth and physiological responses in submerged Myriophyllum species and (iii) that plant traits provide valuable information on the submerged aquatic plant response to changes in the environmental conditions. Fig. 1. The relative growth rate (RGR) of eight Myriophyllum spp. grown under LC 2. Materials and methods (low CO2) and HC (high CO2) conditions for 35 days. Mean ± SE of four replicates are shown. Asterisks indicate significant differences between the LC and HC treat- 2.1. Plant material ment of each species (Tukey’s multiple comparisons of means). The F-values and level of significances for differences between the different carbon treatments (C), × between the species (S) and their interaction (S C) are given from two-way ANOVA. The plant material used was taken either from laboratory cul- (Significance levels: *p-value < 0.05, **p < 0.01, ***p-value < 0.001, ****p < 0.0001.) tures at the Heinrich-Heine-University of Düsseldorf (M. spicatum and M. heterophyllum) or was provided from laboratory cultures − at the Plant Protection Service in Wageningen, The Netherlands ity to use HCO3 have a major competitive advantage over species (M. triphyllum, M. tetrandum, M. papillosum, M. tuberculatum and restricted to CO2 use under CO2-limiting conditions, and show M. variifolium, provided by Dr. J. van Valkenburg). higher growth rates when CO2 limitation occurs, e.g. during the day − For precultivation, plants were grown under standard condi- in dense macrophyte stands. Consequently, the ability for HCO3 tions in 30 l aquaria, filled with a standard medium for general use is considered as one of the major determinants of the distri- aquatic plant purposes (Smart and Barko, 1985) and a water pH of bution of submerged aquatic plants in their habitats (Sand-Jensen, 7.05 ± 0.08, rooted in a nutrient rich sediment. In each aquarium, 1989; Maberly and Madsen, 1998, 2002). − water was filtered by small aquarium filters (type 2213, Eheim, Spencer and Bowes (1990) were the first to link HCO3 use and Deizizau, Germany). Plants grew in a 16/8 h light/dark cycle at room potential plant invasiveness. In a review of alien aquatic plants ◦ temperature of 23 C, and a photon flux density of about 60 ␮mol in Europe, it was noted that almost all successful and fast grow- −2 −1 photons m s . For the experiments, plants were taken out of ing alien submerged aquatic plant species in Europe have a carbon − these precultures and the apical tips of the plants were used for the concentrating mechanism (CCM) and are thus able to use HCO3 studies, except for M. verticillatum where freshly sampled turions (Hussner, 2012), which acts as an competitive advantage over (sampled from the Heider Bergsee near Cologne) were used for the non CO users under CO limitation. These include species with 2 2 experiments. known CCMs, such as single cell C4 Hydrilla verticillata and Ege- ria densa, as well as species with less well described CCMs, like Elodea canadensis, Elodea nuttallii, Lagarosiphon major, Vallisneria 2.2. Growth conditions spiralis or Myriophyllum heterophyllum (Bowes, 2011; Hussner et al., 2016). A number of these submerged aquatic plant species with a For the experiments, unrooted shoot apices of 10 cm in length type of CCM belong to the Hydrocharitaceae family, which might were taken from the precultures, with initial dry masses of be a reason for the large number of fast growing species and strong 0.027 ± 0.002 g (M. variifolium) to 0.052 ± 0.004 g (M. heterophyl- competitors within this family. lum). The freshly collected turions of M. verticillatum had an initial However, the success of a given species depends on both species dry mass of 0.173 ± 0.016 g. The initial dry masses of the plant − traits and habitat characteristics, and the advantage of HCO3 use in parts were calculated based on the dry mass to fresh mass ratio ◦ submerged plants is only present under CO2 limitation.
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