Typha Domingensis Pers. Growth Responses to Leaf Anatomy and Photosynthesis As Inﬂuenced by Phosphorus

Aquatic Botany 122 (2015) 47–53

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Typha domingensis Pers. growth responses to leaf anatomy and photosynthesis as inﬂuenced by phosphorus

Karina Rodrigues Santos, Marcio Paulo Pereira, Ana Carolina Gonc¸ alves Ferreira, Luiz Carlos de Almeida Rodrigues, Evaristo Mauro de Castro, Felipe Fogaroli Corrêa, Fabricio José Pereira ∗

Universidade Federal de Lavras, Departamento de Biologia, Campus Universitário, Lavras, State of Minas Gerais 37200-000, Brazil article info abstract

Article history: Cattail (Typha domingensis Pers.) can show intense growth depending on phosphorus (P) eutrophication. Received 7 July 2014 We verify how P enrichment and deficiency influence T. domingensis growth and the relationship with Received in revised form 23 January 2015 anatomical and physiological modifications. Vegetative T. domingensis plants were grown for 60 days in Accepted 27 January 2015 a modified nutrient solution in five P levels: 0, 0.20, 0.40, 0.60 and 0.80 mM. Plant growth was evaluated Available online 29 January 2015 at the end of the experiment. Leaf fragments were collected and fixed in F.A.A.70 and sectioned in bench- top microtome. Sections were stained with safrablau solution, mounted in slides and photographed Keywords: with an optical microscope. Images were evaluated in UTHSCSA-Imagetool software which was used Cattail Eutrophication to measure leaf tissues. Leaf gas exchanges were evaluated 30 and 60 days after the experiment started. Ecological anatomy The data were submitted to one-way ANOVA and regression analyses or means were compared using Ecophysiology the Scott–Knott test. Plants showed more growth in a P-rich nutrient solution. T. domingensis showed different biomass partitioning under P levels, with an increasing leaf biomass allocation for higher P levels and a lower rhizome investment. For higher P levels, plants showed increased photosynthesis, stomatal conductances and transpiratory rates. However, the highest concentration promoted a decrease in these characteristics. The leaves of T. domingensis showed larger stomata, thicker palisade parenchyma and an increased phloem proportion under higher P levels. Our results suggest that the increased growth of T. domingensis in P-rich conditions may be related to increased photosynthesis; this characteristic is limited to anatomical traits such as palisade parenchyma and stomatal modifications. © 2015 Elsevier B.V. All rights reserved.

1. Introduction ments. Miao et al. (2000) also described the increased population growth of T. domingensis under P enrichment. At the same time, Typha domingensis Pers. (Typhaceae), is a native species in South T. domingensis may be important for P removal from P-rich envi- America and it may show intense vegetative expansion colonizing ronments as it has been used in constructed wetlands for this wide areas (Martins et al., 2007). T. domingensis may be important purpose (Chen and Vaughan, 2014). However, Escutia-Lara et al. to the animals living in these environments (Silveira et al., 2012) (2009, 2010) reported no responses to P enrichment in T. domin- and in phytoremediation (Hegazy et al., 2011). gensis growth. Uncontrolled growth of T. domingensis has been reported to There have been few studies concerning the anatomical char- be the result of phosphorus (P) enrichment of the environment acteristics of T. domingensis. Henry (2003) described the leaves of (Newman et al., 1998; Li et al., 2010), notably in the everglades. T. domingensis showing stomata on both the adaxial and abaxial This P enrichment may lead to the decline of previously dominant surfaces and sclerenchyma fibers between palisade parenchyma native species. As an example, Macek et al. (2010) reported the groups. Likewise, monocotyledon plants of some species experienc- almost-complete reduction of the Eleocharis spp. population when ing P deficiency show poorly developed leaf tissues (Kavanová et al., competing with T. domingensis in nitrogen- and P-rich environ- 2006). Physiological traits in T. domingensis are poorly understood but Miao et al. (2000) reported higher photosynthetic potential in T. domingensis plants growing in P-rich environments. Likewise, previous studies have described that anatomical leaf modifica- ∗ Corresponding author. Tel.: +55 3538291616; fax: +55 3538291341. tions such as higher mesophyll thickness and stomatal number E-mail address: [email protected]fla.br (F.J. Pereira). http://dx.doi.org/10.1016/j.aquabot.2015.01.007 0304-3770/© 2015 Elsevier B.V. All rights reserved. 48 K.R. Santos et al. / Aquatic Botany 122 (2015) 47–53 can be related to increased photosynthesis (Nikolopoulos et al., by counting new shoots each day and the final number of shoot for 2002; Pereira et al., 2011). Therefore, the differences between T. each replicate was calculated after 60 days. domingensis growth responses in previous studies may be related to different anatomical (stomatal and chlorophyll parenchyma in 2.3. Anatomical evaluation leaves) and physiological (photosynthetic rate) adaptations of this species under different P levels. We aim to verify how P enrichment For the anatomical analysis, fragments in the middle of fully and deficiency influence T. domingensis growth and the relationship developed leaves were fixed in a solution of formaldehyde, acetic with anatomical and physiological modifications. acid and 70% ethanol (F.A.A. 70) for 72 h and then stored in 70% ethanol until further analysis (Kraus and Arduin, 1997). Paradermal leaf sections were obtained using steel blades on both the abax- 2. Experimental ial and adaxial surfaces and the sections were cleared with 50% sodium hypochlorite, rinsed in distilled water twice for 10 min, 2.1. Plant materials and experimental design stained with 1% aqueous safranin, and mounted on slides with 50% glycerol (Johansen, 1940). Cross sections were obtained at the T. domingensis plants were collected in the southeastern region middle leaf region and root maturation zone using the LPC model of Brazil in Alfenas, Minas Gerais State, 21◦2544S, 45◦5649W, (Behringer, Belo Horizonte, Brazil) bench-top microtome. Sections from natural wetlands. Plants collected in environment comprised were cleared with 50% sodium hypochlorite, rinsed twice in dis- of rhizomes (25 cm length and 3 cm of diameter) and about ten tilled water for 10 min, stained with safrablau solution (1% safranin leaves. The plants were washed with tap water and grown in a and 0.1% astra blue in a 7:3 ratio) and mounted on slides with 50% greenhouse in a nutrient solution (Hoagland and Arnon, 1940)at glycerol. The slides were photographed using a BX 60 model (Olym- 40% ionic strength for 60 days to obtain acclimatized clone plants. pus, Tokyo, Japan) with a digital camera (Canon A630; Canon Inc., The clone plants were standardized according to size (rhi- Tokyo, Japan). For each replicate, we evaluated five sections and zomes showing about 15 cm length) and number of leaves (about five fields for each section. five leaves), all clone plants were at the same age and in the UTHSCSA-Imagetool software was used for image analysis. We vegetative stage. There were no inflorescences or new clones in measured the following parameters: NSaD = number of stomata plants used in experiment. Plants were placed in polypropylene per field, NCaD = number of epidermal cells per field, POLaD = polar vases (38 × 53 × 8 cm) containing 4 L of modified nutrient solu- diameter of the stomata, SEDaD = equatorial diameter of the stom- tion at 20% ionic strength with increasing P levels (0.0, 0.2, 0.4, ata, SDaD = stomatal density (stomata per mm2), PERaD = stomatal 0.6 and 0.8 mM). The experiment was carried out under these ratio between POL/EQU, SIaD = stomatal index, NSaB = number conditions for 60 days and nutrient solution was replenished in of stomata per field, NCaB = number of epidermal cells per 15 days intervals, nutrient levels was monitored with handheld field, POLaB = polar diameter of the stomata, SEDaB = equatorial condutivimeter (Mettler–Toledo, Greifensee, Switzerland). There- diameter of the stomata, SDaB = stomatal density (stomata per fore, plants at the end of the experiment were 120 days old mm2), PERaB = stomatal ratio between POL/EQU, SIaB = stomatal and showed no inflorescences remaining at the vegetative state. index, AbE = abaxial epidermis thickness, AdE = adaxial epidermis Phosphorus levels in P-rich environments are reported for some thickness, MF = mesophyll thickness, PPaD = palisade parenchyma Brazilian wetlands such as the 1800 ␮gPg−1 water as reported by thickness from adaxial side, PPaB = palisade parenchyma thick- Borges et al. (2009) and Canadian hypertrophic wetlands may reach ness from abaxial side, SP = spongy parenchyma thickness, PP/SP 0.2 mM P (White et al., 2000). Likewise, Steinbachová-Vojtískováˇ ratio = palisade and spongy parenchyma ratio, DV = distance et al. 2006 considered 0.999 mM a hypertrophic concentration for between vascular bundles in the mesophyll, BSC = diameter of the phosphorus and Wang et al. (2013) state that 25 mg L−1 is an bundle sheath cells and PAE = proportion of aerenchyma gaps in extremely high phosphorus level. Therefore, we classify the 0.6 the leaves (area/area). and 0.8 levels as P-rich environments and 0.2 and 0.0 mM of P as P-poor solution. The nutrient solution comprised from concentra- 2.4. Gas exchange evaluation tions described by Hoagland and Arnon (1940) using the following salts: NH4H2PO4, Ca(NO3)2, Mg(NO3)2, KNO3,K2SO4, FeSO4·7H2O, We evaluated the leaf gas exchange characteristics using an H2BO3, MnSO4·H2O, ZnSO4·7H2O, CuSO4·5H2O, H2MoO4·H2O. infrared gas analyzer (IRGA), LI-6400XT model (Li-COR Biosciences, The experimental design was completely randomized with five Lincoln, Nebraska, USA). The gas exchange evaluation was per- treatments and six replicates and the parcel constituted of one plant formed twice at 30 and 60 days after the beginning of the for each replicate. experiment and two fully expanded leaves were evaluated for each replicate. The evaluation started at 10 am. and the photosynthetic photon flux density (PPFD) was fixed at 1000 ␮mol m2 s−1 in the 2.2. Growth evaluation device chamber. Thus PPFD was chosen from previous light satu- ration tests to these plants and to avoid photoinhibition or a lack Growth evaluation was performed by measuring the leaves, of radiation. We additionally evaluated the stomatal conductance roots and stem dry mass on an analytical balance at the end of (gs), transpiration rate (E), photosynthetic rate (A) and the ratio the experiment. Dry mass was obtained by drying the plant parts between internal and external carbon (Ci/Ca). in an oven at 45 ◦C for 48 h. Leaf area was measured at the end of the experiment by photographing the leaves and measuring their 2.5. Statistical analysis area using UTHSCSA-Imagetool software (The University of Texas Health Science Center, San Antonio, Texas, USA). The physiological The data were subjected to MANOVA and principal component growth indices were calculated as described by Hunt et al. (2002) analysis (PCA) was performed previous to F test and multiple com- and the relative growth rate (RGR) and the leaf area ratio (LAR) were parison analysis. PCA was performed in order to select the most obtained. The net assimilation rate (NAR) was obtained by multi- significant variables among our data. Eigenvalues were used to plying (RGR × LAR). Biomass partitioning was calculated for each highlight significant factors. All factors showing Eigenvalues of 1.0 organ by dividing its dry mass by the entire plant dry mass; the or higher were assumed as significant. Factors were added to obtain results were expressed as a percentage (%). Expansion was assessed 85% or higher values for explained variability. Significant variables K.R. Santos et al. / Aquatic Botany 122 (2015) 47–53 49

Fig. 1. Growth characteristics of T. domingensis cultivated at different P levels in the nutrient solution. The bars correspond to the standard errors. Means followed by letters in panel D do not differ according to the Scott–Knott test at p ≤ 0.05.

were selected to F test and multiple comparisons of means, how- stomatal density (Fc = 2.41, p = 0.49 and mean = 452 stomata mm−2) ever, previous to F test, data was subjected to Shapiro–Wilk test on the leaves’ abaxial sides. However, P promoted anatomical mod- for normal distribution and Lavene test for variance homogeneity. ifications on most of the evaluated traits on the leaves’ abaxial Statistical significance was presumed for p < 0.05 and regression sides. Increasing P levels promoted larger stomatal polar diame- analysis was conducted. Principal component analysis was per- ters (Fig. 3A), a higher polar-to-equatorial diameter ratio (Fig. 3B) formed in Statistica software and F test as well as regression and an increased stomatal index (Fig. 3C). Likewise, the stomatal analysis was preformed using Sisvar statistical software. ratio between the polar and equatorial diameters increased with higher P concentrations (Fig. 3D), as did the stomatal index (Fig. 3E). 3. Results However, the stomatal density showed no changes with P concentrations (Fc = 2.00; p = 0.09) and was characterized by an average of −2 Higher P concentrations promoted more vegetative growth. At 423 stomata mm . 60 days, T. domingensis plants exposed to higher P concentrations The thickness of the epidermis from both leaf sides was not ≤ ≥ had produced more new plants proportional to the P level in the modified by the P level (Fc 0.866, p 0.48); the mean epidermis ␮ ␮ nutrient solution (Fig. 1A). Phosphorus also increased the biomass thickness from the abaxial side was 12.62 m and 12.34 m for the production of each plant, leading to plants at least three times larger adaxial side. The palisade parenchyma thickness of the abaxial side than plants grown in the solution lacking P (Fig. 1B). Higher P levels showed no changes induced by P level (Fc = 0.61, p = 0.65), showing ␮ also accounted for differences in plant biomass partitioning in dif- an average value of 84.23 m. However, the palisade parenchyma ferent plant organs. As shown in Fig. 1C, T. domingensis decreased from the adaxial side was increased with P concentration in the the biomass allocated to rhizomes but increased its investment in nutrient solution but was reduced for higher P levels (Fig. 3F). The leaf production with increasing P levels. leaf vascular bundles of T. domingensis from both the adaxial and Net photosynthesis increased in T. domingensis plants exposed abaxial sides showed increased phloem areas proportional to the to higher P levels in the nutrient solution. Plants showed higher applied P level (Fig. 3G). However, the xylem proportion on the vas- photosynthetic rates until a P level of 0.4 mM in the solution; the cular bundles from the adaxial side decreased with P concentration photosynthetic rates dropped in the higher concentrations tested (Fig. 3H) and showed no modifications on the abaxial side (Fc = 1.86, (0.8 mM), as shown in Fig. 2A. Likewise, the stomatal conduc- p = 0.12, mean = 20.32%). tance increased with increasing P levels until the 0.4 mM solution; T. domingensis leaves in transversal sections revealed a thin reduced conductances were observed in higher concentrations single-layered epidermis on both the abaxial and adaxial sides (Fig. 2B). A very similar result was observed in the transpiration, (Fig. 4). Three cell layers of palisade parenchyma were found close which showed increasing values until the 0.4 mM level and reduced to the epidermis of the abaxial and adaxial sides (Fig. 4). Between means in the plants exposed to higher P levels (Fig. 2C). the palisade parenchyma layers, large spongy parenchyma areas Paradermal sections of T. domingensis leaves reveal stomata on were found showing big aerenchyma gaps (lacunae). Collateral both the adaxial and abaxial sides. Stomata show two bean-shaped vascular bundles containing xylem and phloem were distributed guard cells as well as two parallel subsidiary cells on both sides among the palisade parenchyma on both leaf sides. These vascular of the longer stomatal axis. Epidermal cells show many differ- bundles have fibers and a bundle sheath comprising parenchyma ent shapes and very straight cell walls that lack sinuosities. The (Fig. 4). This leaf structure was observed in all P treatments; the stomata are randomly distributed along the surface on both sides number of cell layers of tissues, as well as the arrangement of cells, of the leaves. Quantitative analysis revealed no modifications to was not modified by the P levels tested. Even plants grown for the equatorial diameter (Fc = 1.32, p = 0.26; mean = 10.81 ␮m) and 60 days in the solution lacking P exhibited well-developed tissues 50 K.R. Santos et al. / Aquatic Botany 122 (2015) 47–53

Fig. 2. Leaf gas exchanges of T. domingensis cultivated at different P levels in the nutrient solution. The bars correspond to the standard errors. on both their adaxial and abaxial sides (Fig. 4A and F), although studies, we found that T. domingensis can increase its biomass allo- differences in cell size were evident in some tissues (Fig. 4). cation to leaves under higher P levels in the nutrient solution; this effect may be related to a larger leaf area useful for photosynthesis 4. Discussion and enhanced plant growth. Balemi (2009) reported no modification, or even reduced net Higher plant growth is often reported for plants exposed to P photosynthesis, in potato plants depending on genotype. In field enrichment such as Potamogeton crispus (Wang et al., 2013) and conditions, Miao et al. (2000) found increased photosynthesis for even T. domingensis (Li et al., 2010; Macek et al., 2010). However, T. domingensis plants growing in P-rich sites. Stress conditions Escutia-Lara et al. (2010) reported no modifications to T. domin- may limit the net photosynthesis of T. domingensis; Chen and gensis growth with varying P enrichment. We observed increased Vaughan, 2014 reported lower photosynthesis for T. domingen- vegetative growth and individual biomass production in T. domin- sis plants exposed to higher inundation depth, which decrease P gensis promoted by P enrichment in the nutrient solution. This uptake in plants. We found reduced photosynthesis levels for both finding is very similar to of the results of previous works reported lower and higher P levels. This fact suggests that P deficiency alone in the literature. However, discrepant results in the literature may does not limit T. domingensis photosynthesis, but some other addi- be related to P concentration because, as will be discussed later, tional factor may be related to the higher levels of photosynthesis. physiological and anatomical modifications in higher P levels may According to Zhou and Han (2005), the two factors that limit help to explain the differences observed in previous studies. photosynthesis are light and CO2 availability. Therefore, reduced We found a clear modification in biomass partitioning of T. stomatal conductance values and transpiration with higher P lev- domingensis related to P level. Since roots are important for P uptake els in T. domingensis leaves suggest that higher P levels promote and are produced by T. domingensis rhizomes, low P levels pro- stomatal limitations to CO2 uptake, reducing photosynthesis. Sto- moted a higher rhizome allocation of biomass. This fact may lead matal data support this statement because we found larger stomata to a larger number of roots for P uptake. This result may be related to in plants growing in higher P concentrations but reduced stomatal an increased number of thinner roots that are more efficient at tak- sizes in highest P concentration. Since stomata are related to CO2 ing up nutrients (Roose and Fowler, 2004; Simˇ unek˚ and Hopmans, uptake and may improve photosynthesis under stress conditions 2009). (Pereira et al., 2011), larger stomata may be related to larger areas Increased P levels promoted higher leaf biomass allocation on for gas exchange, enhancing photosynthesis. T. domingensis, leading to larger photosynthetic areas and higher Shen et al. (2006) postulated that P plays a role in signaling sto- plant and population growth. The shoot biomass of T. domingensis matal development related to the calcium network in Arabidopsis was evaluated by Escutia-Lara et al. (2010), who found no impact thaliana. We found an increased stomatal index in T. domingensis of P level on this trait. However, when grown under eutrophic and leaves exposed to higher P levels but no changes in stomatal den- hypertrophic conditions when all macronutrients were enriched, sity. This finding may be related to the larger stomata produced T. angustifolia showed a larger biomass allocation to shoots and by P enrichment, which took up more room on leaves, leading to a a larger number of leaves (Steinbachová-Vojtískováˇ et al., 2006). similar stomatal density even with more stomata developing from Natural environments showing higher P levels promoted higher the protodermis. This result supports the hypothesis that P plays growth rates and leaf biomass allocations in T. domingensis plants a role in stomatal development, increasing the stomatal number (Miao et al., 2000). In fact, Grace and Wetzel (1981) attributed in P-rich conditions. This response is important to T. domingensis the larger capacity to growth and competition of T. latifolia to T. thereby promoting increased CO2 uptake and photosynthesis. angustifolia due to its broader leaves which developed a larger Another important anatomical trait in T. domingensis that was photosynthetic area. Despite divergent data reported by previous modified by P enrichment was palisade parenchyma thickness. K.R. Santos et al. / Aquatic Botany 122 (2015) 47–53 51

Fig. 3. Anatomical leaf characteristics of T. domingensis cultivated under different P levels in the nutrient solution. A–E: stomatal characteristics; F–H: tissue characteristics at transverse sections. A–C: abaxial side; D–E: adaxial side. The error bars indicate standard errors. The error bars correspond to standard errors.

Cell elongation of some monocotyledon leaves such as Lolium Increased phloem development may be an important character- perene may be limited to low P availability (Kavanová et al., istic of stress tolerance by enhancing plant growth capacity (Pereira 2006). Chiera et al. (2002) reported thinner palisade parenchyma et al., 2011). Furthermore, an increased phloem proportion may be in soybean leaves under P stress. Therefore, a P limitation may related to the larger growth to T. domingensis in a P-rich solution explain the lower palisade parenchyma thickness in nutrient solu- because this tissue is responsible for the transport of photosynthe- tions lacking this element. However, the palisade parenchyma sis products to sink organs. thickness was strongly reduced in plants growing in P levels of 0.6 Despite all of the anatomical improvements caused by higher P and 0.8 mM. A larger leaf thickness is related to an enhanced pho- levels, another important result we observed was the capacity of T. tosynthesis potential (Shipley et al., 2005), which may be related domingensis to develop functional leaves even in solutions lacking to the larger size of chlorophyll parenchyma. Likewise, the pho- P. As reported by Chiera et al. (2002), leaves in low-P solutions tosynthetic limitation on T. domingensis in both higher and lower showed poorly developed tissues, even after only 16 days of P stress. P conditions may also be related to the reduction of palisade We observed that T. domingensis leaves showed well-developed parenchyma thickness. leaf tissues after 60 days of P stress. This result indicates a strong 52 K.R. Santos et al. / Aquatic Botany 122 (2015) 47–53

Fig. 4. Transverse sections of T. domingensis leaves cultivated under different P levels in the nutrient solution. A–E: abaxial side of the leaves; F–J: adaxial side of the leaves. A and F = 0.00, B and G = 0.20, C and H = 0.40, D and I = 0.60 and E and J = 0.8 mM of P in the nutrient solution. gp = ground parenchyma, pp = palisade parenchyma, ep = epidermis, vb = vascular bundle, x = xylem, p = phloem. The scale bars correspond to 100 ␮m. K.R. Santos et al. / Aquatic Botany 122 (2015) 47–53 53 tolerance for P stress; T. domingensis develop as smaller plants Hegazy, A.K., Abdel-Ghani, N.T., El-Chaghaby, G.A., 2011. Phytoremediation of but show functional organs only with the P stored in rhizomes. industrial wastewater potentiality by Typha domingensis. Int. J. Environ. Sci. Technol. 8, 639–648. All of our results suggest that T. domingensis growth is enhanced Henry, R., 2003. Ecótonos nas Interfaces dos Ecossistemas Aquáticos. Rima, São by higher P levels and that this increase is related to photo- Carlos, pp. 349. synthesis and anatomical improvements. However, our findings Hoagland, D.R., Arnon, D.I., 1940. Crop production in artificial culture solutions and in soils with special reference to factors influencing yield absorption of are dependent on the P concentration in the nutrient solution, inorganic nutrients. Soil Sci. 50, 463–483. leading to the findings distinct from those reported in previous Hunt, R., Causton, D.R., Shipley, B., Askew, A.P., 2002. A modern tool for classical studies. plant growth analysis. Ann. Bot. 90, 485–488. Therefore, T. domingensis growth is dependent of P concen- Johansen, D.A., 1940. Plant Microtechinique, second ed. New York, Mc Graw-Hill. Kavanová, M., Lattanzi, F.A., Grimoldi, A.A., Schnyder, H., 2006. Phosphorus tration as follows: low P levels reduce growth by limiting leaf deficiency decreases cell division and elongation in grass leaves. Plant Physiol. production and photosynthesis; in despite excess P also limits 141, 766–775. photosynthesis. This clearly shows a limit for P efficiency on T. Kraus, J.E., Arduin, M., 1997. Manual Básico em Métodos em Morfologia Vegetal. EDUR, Seropédica. domingensis growth. This may be related to contrasting results in Li, S., Lissner, J., Mendelssohn, I., Brix, H., Lorenzen, B., McKee, K.L., Miao, S., 2010. previous works (Miao et al., 2000; Escutia-Lara et al., 2010; Li et al., Nutrient and growth responses of cattail (Typha domingensis) to redox 2010) because experiments under low or too high P levels may lead intensity and phosphate availability. Ann. Bot. 105, 175–184. Macek, P., Rejmánková, E., Leps,ˇ J., 2010. Dynamics of Typha domingensis spread in to similar effects. Likewise, the photosynthesis limitation in low or Eleocharis dominated oligotrophic tropical wetlands following nutrient excess P levels is related to anatomical modifications in palisade enrichment. Evol. Ecol. 24, 1505–1519. parenchyma and stomata in leaves. Martins, A.P.L., Reissmann, C.B., Favaretto, N., Boeger, M.R.T., Oliveira De, E.B., 2007. Capacidade da Typha dominguensis na fitorremediaç ão de efluentes de tanques de piscicultura na Bacia do Iraí – Paraná. Rev. Bras. Eng. Agr. Amb. 11, 324–333. Acknowledgements Miao, S., Newman, S., Sklar, F.H., 2000. Effects of habitat nutrients and seed sources on growth and expansion of Typha domingensis. Aquat. Bot. 68, 297–311. Newman, S., Schuette, J., Grace, J.B., Rutchey, K., Fontaine, T., Reddy, K.R., Pietrucha, The authors thank CNPq (Conselho Nacional de Desenvolvi- M., 1998. Factors influencing cattail abundance in the northern Everglades. mento Científico e Tecnológico [National Counsel of Scien- Aquat. Bot. 60, 265–280. tific and Technological Development], CAPES (Coordenação de Nikolopoulos, D., Liakopoulos, G., Drossopoulos, I., Karabourniotis, G., 2002. The relationship between anatomy and photosynthetic performance of heterobaric Aperfeiç oamento de Pessoal de Nível Superior [Coordination for leaves. Plant Physiol. 129, 235–243. the Improvement of Higher Education Personnel]), and FAPEMIG Pereira, F.J., Castro, E.M., Oliveira, C., Pires, M.F., Pasqual, M., 2011. Mecanismos (Fundaç ão de Amparo à Pesquisa do estado de Minas Gerais anatômicos e fisiológicos de plantas de aguapé para a tolerância à [Minas Gerais State Research Support Foundation]) for funding and contaminaç ão por arsênio. Planta Dan. 29, 259–267. Roose, T., Fowler, A.C., 2004. A model for water uptake by plant roots. J. Theor. Biol. research grants awarded to complete the present study. 228, 155–171. Shen, Z., Wang, G., Liu, Z., Zhang, H., Qiu, M., Zhao, X., Gan, Y., 2006. Network regulation of calcium signal in stomatal development. Acta Pharmacol. Sin. 27, References 950–958. Shipley, B., Vile, D., Garnier, E., Wright, I.J., Poorter, H., 2005. Functional linkages Balemi, T., 2009. Effect of phosphorus nutrition on growth of potato genotypes between leaf traits and net photosynthetic rate: reconciling empirical and with contrasting phosphorus efficiency. Afr. Crop Sci. J. 17, 199–212. mechanistic models. Funct. Ecol. 19, 602–615. Borges, A.C., Sanders, C.J., Santos, H.L.R., Araripe, D.R., Machado, W., Patchineelam, Silveira, T.C.L., Rodrigues, G.G., Souza, G.P.C., Würdig, N.L., 2012. Effect of Typha S.R., 2009. Eutrophication history of Guanabara Bay (SE Brazil) recorded by domingensis cutting: response of benthic macroinvertebrates and macrophyte phosphorus flux to sediments from a degraded mangrove area. Mar. Pollut. regeneration. Biota Neotrop. 12, 122–130. Bull. 58, 1739–1765. Simˇ unek,˚ J., Hopmans, J.W., 2009. Modeling compensated root water and nutrient Chen, H., Vaughan, K., 2014. Influence of inundation depth on Typha domingensis uptake. Ecol. Modell. 220, 505–521. and its implication for phosphorus removal in the everglades stormwater Steinbachová-Vojtísková,ˇ L., Tylová, E., Soukup, A., Novická, H., Votrubová, O., treatment area. Wetlands 34, 325–334. Lipavská, H., Cíˇ zková,ˇ H., 2006. Influence of nutrient supply on growth Chiera, J., Thomas, J., Rufty, T., 2002. Leaf initiation and development in soybean carbohydrate, and nitrogen metabolic relations in Typha angustifolia. Environ. under phosphorus stress. J. Exp. Bot. 53, 473–481. Exp. Bot. 57, 246–257. Escutia-Lara, Y., Gómez-Romero, M., Lindig-Cisneros, R., 2009. Nitrogen and Wang, L., Yang, T., Zhu, D., Hamilton, D., Nie, Z., Liu, L., Wan, X., Zhu, C., 2013. phosphorus effect on Typha domingensis Presl. rhizome growth in a matrix of Growth and turion formation of Potamogeton crispus in response to different Schoenoplectus americanus (Pers.) Volkart ex Schinz and Keller. Aquat. Bot. 90, phosphorus concentrations in water. Aquat. Ecol. 47, 87–97. 74–77. White, J.S., Bayley, S.E., Curtis, P.J., 2000. Sediment storage of phosphorus in a Escutia-Lara, Y., Barrera, E., Cruz, Y.M., Lindig-Cisneros, R., 2010. Respuesta a la northern prairie wetland receiving municipal and agro-industrial wastewater. adición de nitrógeno y fósforo en el crecimiento de Typha domingensis y Ecol. Eng. 14, 127–138. Schoenoplectus americanus. Bol. Soc. Bot. Mex. 87, 83–87. Zhou, Y.M., Han, S.J., 2005. Photosynthetic response and stomatal behaviour of Grace, J.B., Wetzel, R.G., 1981. Habitat partitioning and competitive displacement Pinus koraiensis during the fourth year of exposure to elevated CO2 in cattails (Typha): experimental field studies. Am. Nat. 118, 463–474. concentration. Photosynthetica 43, 445–449.