Elsevier

Agricultural Water Management

Volume 149, February 2015, Pages 102-114
Agricultural Water Management

Optimization of culturing conditions and selection of species for the use of halophytes as biofilter for nutrient-rich saline water

https://doi.org/10.1016/j.agwat.2014.11.001Get rights and content

Highlights

  • Cultivation of halophytes was optimized to increase efficiency of a plant biofilter.

  • A nitrate-N concentration of 10 mg l−1 is necessary for reasonable biomass production.

  • Addition of iron in chelated form is necessary.

  • Several tested species have potential to serve as biofilter and valuable co-products.

  • Application: halophytic vegetable plants can be grown in marine aquaponic systems.

Abstract

Salt-tolerant plants can be used as biofilters for nutrient-rich saline water such as aquaculture process water. Tripolium pannonicum (Jacq.) Dobrocz. was used to determine optimal culturing conditions for an efficient biofilter performance in terms of nutrient recycling by plant uptake. This performance was evaluated by taking different parameters into account, such as biomass production, plant nitrogen and phosphorus uptake as well as physiological parameters and decrease of nitrate-N and phosphate-P concentrations in the experimental fluid. Afterwards, additional plant species known as edible were studied to follow the idea of generating valuable co-products beside the use as biofilter. It was shown that a nitrate-N concentration of at least 10 mg l−1 is necessary for reasonable biomass production. A phosphate-P concentration of 0.3 mg l−1 is sufficient, but higher concentrations promote the uptake of phosphate-P. The addition of iron in chelated form is required for the growth of healthy plant biomass; the addition of manganese is beneficial but not implicitly necessary. Salt concentrations lower than seawater salinity promote biomass production and nutrient uptake. The use of a hydroponic culture system is more suitable than sand or expanded clay culture if controlled conditions and nutrient recycling are desired. The five weeks experiment to compare different halophyte species in 0.24 m2 tanks with nine plants each resulted in above ground fresh weight of 185 to 398 g and total uptake of nitrogen and phosphorus of 0.6 to 2.1 g and 0.1 to 0.4 g, respectively. All tested species have potential to serve as biofilter and source for valuable co-products. A promising application is the growth of halophytic vegetable plants in marine aquaponic systems.

Introduction

Several plant species and different types of natural and constructed wetlands are successfully applied for purification of municipal and industrial wastewater or effluents from agroindustry and aquaculture (Kadlec and Knight, 1996, Verhoeven and Meulemann, 1999, Vymazal, 2010). Operating plant biofilters is a low cost opportunity to mitigate the impact of effluents on the environment. The load of nutrients, heavy metals and organic substances in wastewater that cause hypertrophication and toxification of surrounding ecosystems is reduced. Additionally, some of the applied plant species can be used to produce a valuable co-product due to their market value, for example as vegetable, fodder, energy crop or source for valuable metabolites.

An interesting field for the application of plants as biofilter and valuable co-product is aquaculture. The cultured fish and invertebrate animals retain only some of the nitrogen and phosphorus administered with the feed. These excess nutrients can be reduced by plants grown in a filter bed. Watten and Busch (1984) published results from experimental trials on fish and tomato culture in a recirculating aquaculture system (RAS). The system was composed of a fish tank, a settling tank, a trickling biofilter, and the hydroponic bed for the culture of tomatoes. This basic layout is used for several studies that combine freshwater aquaculture with hydroponic culture of plants (aquaponics) and in several studies the plant biofilter is concurrently used for the production of valuable vegetables, such as lettuce, spinach, tomato, cucumber, and pepper (Lennard and Leonard, 2006, Graber and Junge, 2009, Roosta and Mohsenian, 2012, Petrea et al., 2013). Marine aquaculture is a novel source for saline effluents with rising importance because of the increasing demand for sea food (FAO, 2012). Also some industrial, agricultural or municipal wastewater is saline. Plant species often used in filter beds are very sensitive to salt and the use of salt-tolerant plant species becomes mandatory. Those halophytes tolerate salinities up to seawater salinity and above, depending on the species. Several studies investigated the use of halophytes as biofilter for different nutrient-rich saline effluents (Grieve and Suarez, 1997, Klomjek and Nitisoravut, 2005, Wu et al., 2008). Studies on the application of halophytes as biofilter for aquaculture process water are summarized by Buhmann and Papenbrock (2013a). Recently, Diaz et al. (2013) demonstrated a good performance of various halophyte species in a saline drainage water reuse system. Additionally to the promising application of halophytes as biofilter and valuable co-product it is highly beneficial to foster the use of saline water for agricultural production because freshwater is a declining resource in many regions of the world (FAO, 2008, FAO, 2012, Rozema and Schat, 2013).

There are several studies describing the potential of halophytes as vegetable or as raw material for fodder and to provide secondary metabolites that can be used for pharmaceuticals, functional foods, nutraceuticals, and technical implementations (Ksouri et al., 2011, Buhmann and Papenbrock, 2013b). A challenge for the combination of nutrient-rich saline wastewater purification by halophytes with the production of a valuable co-product is the limited knowledge about the cultivation of halophytes. Recently, different aspects for the cultivation of the edible halophyte genera Salicornia and Sarcocornia have been described (Ventura et al., 2010, Ventura et al., 2011a, Ventura et al., 2011b, Katschnig et al., 2013, Ventura and Sagi, 2013). Other halophyte species like Tripolium pannonicum (Jacq.) Dobrocz., Plantago coronopus L. and Crithmum maritimum L. also have potential as saline vegetable crops and initial studies on cultivation have been performed (Ben Amor et al., 2005, Koyro, 2006, Koyro et al., 2011, Ventura et al., 2013). Factors that influence the successful cultivation of salt-tolerant plant species, such as salinity, nutrient concentration, light conditions and availability of micronutrients, can also influence the performance of the respective halophyte biofilter (Kadlec and Knight, 1996, Verhoeven and Meulemann, 1999, Vymazal, 2010, Buhmann and Papenbrock, 2013a). Due to the limited information about the culture of halophytes it is substantial to determine optimal culturing conditions and suitable species for the use of halophytes as biofilter and valuable co-product before application.

The objective of this study was to identify (i) optimal culture conditions and (ii) suitable species for the application of halophytes as biofilter for nutrient-rich saline effluents and as valuable co-product. The composition of an actual effluent is fixed and possibly not optimal for plant growth. For our simulation experiments an artificial effluent was used as a plant culturing solution based upon the composition of the process water of a modern marine RAS described in Orellana et al. (2013). The system in Orellana et al. (2013) contains artificial sea water, a nitrifying biofilter is used to convert nitrogenous excretory products of the fish to nitrate-N which then is the main nitrogen source for plant production. Plant available dissolved nitrogen and phosphorus are abundant in concentrations around 100 mg NO3-N l−1 and 1 to 15 mg PO4-P l−1. Results of this study should be relevant to prepare the application of a halophyte biofilter in such a modern marine RAS, but also assignable to other applications. Contrary to many other studies on plant biofilters, the important criterion for an efficient halophyte biofilter in this study was a high percentage of nutrient recycling through plant uptake of nitrogen and phosphorus in form of nitrate and phosphate, and the conversion of these nutrients into valuable marketable biomass. Other processes within the halophyte biofilter, like bacterial conversion of nutrients and adsorption to the substrate, were less favoured because they only remove and not recycle the nutrients. We conducted greenhouse experiments with artificial seawater as a basis for plant nutrient solution. T. pannonicum was used as a model species to determine optimal conditions regarding substrate, salinity, nitrate-N and phosphate-P concentration and addition of iron and manganese. Finally, the biofilter capacity of different halophyte species with market potential was compared under optimized conditions.

Section snippets

Plant material

For some of the species, seeds were collected at the North Sea, Jade Bay, Germany: Atriplex portulacoides L. (53°29′13N; 8°03′16″E), Salicornia dolichostachya Moss (53°29′13N; 8°03′16″E) and two different seed collections of T. pannonicum (53°29′13N; 8°03′16″E, ecotype 1 (et1) and 53°26′19″N; 8°09′49″E, ecotype 2 (et2)). Seeds of P. coronopus were ordered at Jelitto Staudensamen GmbH (Schwarmstedt, Germany). For the species Lepidium latifolium L. and Atriplex halimus L. one specimen was ordered

Results

ESUBSTRATES was conducted to find the best mode of culture in terms of nutrient recycling and production of valuable biomass. Plants cultured in expanded clay and hydroponic culture showed a higher gain of biomass and uptake of nitrogen than those cultured in sand, but not significantly (Table 1). The hydroponic culture treatment displayed a significantly higher uptake of phosphorus than the other two treatments (p < 0.001, Table 1). Plants grown in hydroponic culture and in expanded clay had a

Salt-tolerant Tripolium pannonicum grows well in hydroponic culture

In ESUBSTRATES plants performed similarly well in expanded clay and hydroponic culture regarding growth and nitrogen uptake. But phosphate-P uptake was much higher in hydroponic culture than in both substrate cultures. The lower phosphate-P uptake in expanded clay and sand culture could be due to adsorption of phosphate-P to substrate particles and precipitation causing a lower plant availability of phosphate-P (Johansson Westholm, 2006). Substrate culture and expanded clay culture lead to a

Conclusions

Halophytes have a high potential for their use as new crop plants for saline agriculture and as biofilters in different applications. Several studies directly investigate the functioning of a halophyte biofilter within the application where many factors play a role. To selectively investigate the influence of specific factors we conducted experiments under controlled conditions simulating application to learn before the transfer. Basic cultivation techniques and putative growth limitations have

Acknowledgements

We would like to thank the gardeners Yvonne Leye and Lutz Krüger for taking care of the plants and Rebecca Hosang, Pamela von Trzebiatowski and Julia Volker for valuable technical assistance. The project was financially supported by the Deutsche Bundesstiftung Umwelt (DBU) (AZ27708/1-3).

References (68)

  • H.W. Koyro

    Effect of salinity on growth, photosynthesis, water relations and solute composition of the potential cash crop halophyte Plantago coronopus (L.)

    Environ. Exp. Bot.

    (2006)
  • H.K. Lichtenthaler

    Chlorophylls and carotenoids: pigments of photosynthetic biomembranes

    Methods Enzymol.

    (1987)
  • A.J. Lymbery et al.

    Efficacy of a subsurface low wetland using the estuarine sedge Juncus kraussii to treat effluent from inland saline aquaculture

    Aquacult. Eng.

    (2006)
  • H.R. Roosta et al.

    Effects of foliar spray of different Fe sources on pepper (Capsicum annum L.) plants in aquaponic system

    Sci. Hortic.

    (2012)
  • J. Rozema et al.

    Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture

    Environ. Exp. Bot.

    (2013)
  • O. Schneider et al.

    Analysis of nutrient flows in integrated intensive aquaculture systems

    Aquacult. Eng.

    (2005)
  • D.C. Sikawa et al.

    The hydroponic production of lettuce (Lactuca sativa L.) by using hybrid catfish (Clarias macrocephalus × C. gariepinus) pond water: potentials and constraints

    Agric. Water Manage.

    (2010)
  • M. Shpigel et al.

    Constructed wetland with Salicornia as a biofilter for mariculture effluents

    Aquaculture

    (2013)
  • Y. Tal et al.

    Environmentally sustainable land-based marine aquaculture

    Aquaculture

    (2009)
  • C.G.J. Van Bussel et al.

    The chronic effect of nitrate on production performance and health status of juvenile turbot (Psetta maxima)

    Aquaculture

    (2012)
  • J. Van Rijn et al.

    Denitrification in recirculating systems: theory and applications

    Aquacult. Eng.

    (2006)
  • Y. Ventura et al.

    Molybdenum as an essential element for improving total yield in seawater-grown Salicornia europaea (L.)

    Sci. Hortic.

    (2010)
  • Y. Ventura et al.

    Effect of seawater concentration on the productivity and nutritional value of annual Salicornia and perennial Sarcocornia halophytes as leafy vegetable crops

    Sci. Hortic.

    (2011)
  • Y. Ventura et al.

    Effects of day length on flowering and yield production of Salicornia and Sarcocornia species

    Sci. Hortic.

    (2011)
  • Y. Ventura et al.

    Halophyte crop cultivation: the case for Salicornia and Sarcocornia

    Environ. Exp. Bot.

    (2013)
  • J.T.A. Verhoeven et al.

    Wetlands for wastewater treatment: opportunities and limitations

    Ecol. Eng.

    (1999)
  • B.J. Watten et al.

    Tropical production of tilapia (Sarotherodon aurea) and tomatoes (Lycopersicon esculentum) in a small-scale recirculating water system

    Aquaculture

    (1984)
  • Y. Wu et al.

    Constructed mangrove wetland as secondary treatment system from municipal wastewater

    Ecol. Eng.

    (2008)
  • H.L. Atwood et al.

    Survival and growth of pacific white shrimp Litopenaeus vannamei postlarvae in low-salinity and mixed-salt environments

    J. World Aquacult. Soc.

    (2003)
  • P.R. Alder et al.

    Mechanistic approach to phytoremediation of water

    Ecol. Eng.

    (2003)
  • N.R. Baker

    Chlorophyll fluorescence: a probe of photosynthesis in vivo

    Annu. Rev. Plant Biol.

    (2008)
  • A. Buhmann et al.

    An economic point of view of secondary compounds in halophytes

    Funct. Plant Biol.

    (2013)
  • X.G. Chen et al.

    Growth of a lettuce crop at low ambient nutrient concentrations: a strategy designed to limit the potential for eutrophication

    J. Plant Nutr.

    (1997)
  • DIN (Deutsches Institut für Normung e. V.) 38406-5

    Deutsche Einheitsverfahren zur Wasser-, Abwasser- und Schlammuntersuchung; Kationen (Gruppe E), Bestimmung des Ammonium-Stickstoffs (E 5)

    (1983)
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