Saline crops, from halophyte research to sea vegetable markets

INTELLICROPS

Saline crops, from halophyte research to sea vegetable markets Joost Bogemans, L谩szl贸 Erdei

Saline crops, from halophyte research to sea vegetable markets Joost Bogemansa, László Erdeib Abstract A spin-off company was established in 1999 from EU research on the cultivation, selection and domestication of a selection of halophytes. The mission of the company has always been focused on plant breeding, selection and seed production. Salicornia europaea and Aster tripolium were, from the beginning, the key products of the company. Today the range of sea vegetable species has been extended with Salicornia bigelovii, Salsola komarovii, Salsola soda, Crithmum maritimum, Plantago coronopus, Beta maritima, Crambe maritima and Mertensia maritima. Among them, different races are under development with respect to marketable characteristics (e.g. shape, yield, pest resistance…)

At an early stage, the company established cultivation systems and had the reclamation of saline soils as a primary task. Later, new cultivation systems were deployed to fit horticultural needs (e.g. improving non-seasonality, greenhouse cultivation, mechanization); today we give new growers advice in establishing the new crops. Grower-adapted cultivation systems are setup from hydroponics over saline soil reclamation and highlighting facets like salinity and irrigation control, mineral nutrition under salt regimes and advice on the particular saline crop.

Simultaneously with the introduction of new halophyte crops and appropriate cultivation systems, a marketing development was built up to highlight interesting features of sea vegetable crops such as taste, functional components, ease of use. to new consumers. This review focuses on the establishment of a sea vegetable market under advanced agro-food markets . Introducing new halophyte crops to less developed agro food markets need different approaches but is not made easier . In terms of developing new applications from saline crops (forage, cosmetics, environmental issues, biofuel) a marketing strategy should be focused on the derived products, bearing in mind that the consumer compares and decides.

Intellicrops bvba, Abdijstraat 14, 9400 Ninove, Belgium Department of Plant Biology, University of Szeged, Közép fasor 52, 6726 Szeged, Hungary *Corresponding author.

Tel.: +32 54329093; fax: +32 54331175.

E-mail addresses: joost.bogemans@scrops.com (J.Bogemans), erdei@bio.u-szeged.hu (L.Erdei) published by Intellicrops bvba , Ninove 2012 ©

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Saline Crops, from halophyte research to sea vegetable markets 1.From research to spin-off.

From 1993 until 1996 an EU research project running under the name ‘Saline crops. A contribution to the diversification of the production of vegetable crops by research on the cultivation methods and selection of halophytes.

(AIR3-CT92-0198)’,whose overall objective was to domesticate a number of plant species, naturally growing in saline or brackish soils that are locally gathered for consumption as a vegetable in the EU (Huiskes, Lemeur et al.

1997). Species of Salicornia, Aster tripolium., Beta maritima. and Crambe maritima were envisaged. Three of the species are harvested from wild populations along European coastal areas, but in the case of Crambe maritima (Sea kale) the cultivation disappeared in the 20th century. The aim of the project was to develop commercial agricultural products that could be cultivated as horticultural crop. As research topics the focus was on new cultivation methods, breeding and the reclamation of saline soils.

Research institutes from the Netherlands (NIOO) , Belgium (UGent and VUB Brussels) and Portugal (IBET, EAN) were involved with The Foundation for Marine Cultures Oosterchelde (SMCO, the Netherlands) coordinating the project. Experimental field plots were established in Burg-Haamstede (Netherlands), Aveiro and Leziria (Portugal) and .in a later stage the project was partially reinforced with an EU-Phare project on "Oxygen toxicity and abiotic stress in crops” (H 9112-0163) under the direction of Prof. Dr. László Erdei (University of Szeged, Hungary) (Sági and Erdei 2002). The work plan comprised: germination and propagation, primary production, nutrition and salinity, selection and breeding, crops production in the field and pests and diseases.

According to the work plan promising results were obtained with Aster tripolium and Beta maritima. At the end of the "Saline Crops" project, the specie Salicornia was still difficult to control in terms of germination and growth. The research on Crambe was abandoned at that time as new cultivation and propagation systems were setup by Péron (Peron 1987). Given the progress that was made with Aster tripolium a spin-off company was established in 1999

Fig. 1 Aster tripolium selection trial. EU project Saline Crops 1993-1996 .Experimental field Burgh Haamstede with its founders Prof. Dr. László Erdei (University of Szeged, Hungary) and Dr. Joost Bogemans (VUB Brussels, Belgium). It was the start of a journey with ups and downs.

In 1999 Scrops nv was established. At a time when venture capital was readily available, we easily found commercial partners . Together with one of the commercial partners a cultivation field was found in Portugal. This ancient rice field flooded for years by sea water was reclaimed and the flooded field turned into a dry compact lime soil. Due to the conversion from anaerobic to aerobic soil conditions, we had to start with a soil pH of 3.5. A lot of liming was needed to cultivate Sea aster (Aster tripolium L.) as the first sea vegetable crop. Although in the years thereafter the field was flooded three times more due to heavy rains or the weakness of the natural ditchesand twice destroyed by cattle through poor fencing, the work proved the use of halophytes as forage crops. The field had to be abandoned and although the Salicornia greenhouse cultures, were successful, the resources of Scrops were depleted.

In 2004 the founders continued the activities under Intellicrops bvba . The activities were focused on seed production and consultancy. In 2007 a partial transfer of technology was realised through the establishment of Serra Maris bvba. Serra Maris is today the seed company for sea vegetable seeds. Intellicrops still has its role as developer of non-food applications and runs the management of Serra Maris bvba. Today Serra Maris operates in an international context by setting up cultures in France, Great Britain, the Netherlands, Portugal, Turkey, Israel and the delivery of seeds to the US and Japan.

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Bogemans J and Erdei L. From having a tentative start with only two crops (Salicornia spp. and Aster tripolium L.) we are today dealing with twelve saline crops and working on different races among them. The evolution of the sea vegetable seed business and its forthcoming sea vegetable products can serve as a case study in how to deal with markets and the marketing of new saline crops. Here the different sea vegetables products will be briefly discussed. We define sea vegetables as a range of edible halophytic crops as they all refer to vascular plants.

2. Salicornia Salicornia or samphire (syn. glasswort) was already mentioned in medieval times as a medicinal plant (Blankaart 1698). The plant was primarily denoted as a famine food but gained popularity with time. Whereas in the Netherlands the use of Salicornia was primarily as vegetable, in France the pickling of Salicornia in vinegar is a traditional business. In the Netherlands and France the wild harvest was and is still limited by a system of permits. In the nineties early attempts to make from Salicornia an oil crop came to a dead end (Glenn, Hicks et al. 1996).

Projects in Mexico and Saudi Arabia developed the market for fresh Salicornia in Europe and started to offer Salicornia during the European winter season. The import from Saudi Arabia disappeared but in the last five years Israel became a big exporter of Salicornia . According to previous marketing studies and data , the market of Salicornia in the Benelux alone easily exceeds 300 ton fresh product. A year-round supply or non-seasonality of Salicornia was an important step in the dissemination of the crop. The introduction of cultivated Salicornia by EU growers does not seem to influence the current market as they organized their proper sales. Wholesale prices vary from 6 to 7 Euro/ kg in the Netherlands. A consumer easily pays 18 to 21 Euro/kg in the shop or supermarket. The above mentioned factors are an indication of a non-saturated market in fresh Salicornia tips.

Serra Maris anticipates the development of this market with an offer of seeds of Salicornia europaea . Three races

Fig. 2 Salicornia europaea L. are regularly used in production, which differ in response to flooding resistance, shape, color or yield. Although the nomenclature of Salicornia is still a topic of debate among taxonomists (Teege, Kadereit et al. 2011) , for the distribution of seeds we refer to the nomenclature of the GRIN database (Germplasm Resources Information Network (IRRI 1985)(IRRI 1985)) a database commonly used among plant breeders. Within the customer basis of Serra Maris the cultivation of Salicornia is almost completely switched towards artificial systems of hydroculture or hydroponics. Sa-

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Saline Crops, from halophyte research to sea vegetable markets linity control, adapted mineral nutrition, appropriate light conditions and sowing planning are all elements by which the grower can control growth and extend the growing season. The type of cultivation we propose is similar to the cultivation of micro greens or baby leaf production. A dense stand of Salicornia is established. The erected young tips can then easily been cut in the non-lignified zone of the crop.

The introduction of a mechanic harvesting machine resulted in a boost for the dissemination of the Salicornia cultures.

Depending on the type of cultivation one can expect 20-30 ton FW/ha .

3. Aster tripolium Aster tripolium L. or Sea aster is found on the higher levels on the sea shore. They are mainly flooded by sea water at spring tides. The use of Aster tripolium as vegetable is almost exclusive to the Netherlands, where like Salicornia it was considered as a famine food. The young leaves, 6 to 10 cm long, can be cut early in spring and are considered as a replacement for the Salicornia tips that only emerge in early June. The non-seasonal offer through import from Israel and Portugal gives this product opportunities for a broader familiarization.

Aster tripolium has some interesting characteristics. The yield of young leaves can reach 35 - 50 ton FW/ha, harvested in 6-7 cuttings (Martins, Duvekot et al. 1997). Young leaves are rich in protein and amino acids in the very young stage of the crop. Values of 1.6 to 2% protein on dry weight basis were recorded. Sea aster is generally cooked like spinach and may be mixed with common spinach in order to add texture and a salty taste.

Fig. 3 Aster tripolium L.

Fig. 4 Salsola soda L.

4. Salsola We are currently dealing with two types of Salsola. Salsola komarovii Iljin.(Heywood 1999; 2010) and a European variant of Salsola soda is locally known in Italy as “agretti,” , “barbe di frati” or “Barilla” (1990; Coiffard 1991). Salsola komarovii called “Oka Hijiki” in Japan is known as the oldest vegetable crop there., having been collected along shores for more than 3000 years Oka Hijiki has long needle like leaves with a crispy bite and is best consumed fresh.: it e is not that salt resistant , however salinity brings up a sharp flavor, giving rise to the name “Sea mustard”.

The market is still to be explored but with the internationalization of the European cuisine (e.g. sushi business) will certainly gain more attention. The nomenclature of Salsola komarovii Iljin. is still under debate and is referred as Salsola soda in the GRIN database .

The name of Barilla refers to the glass industry in Medieval time. Plants like Salicornia and Salsola were cut and burnt.

The ash was used as the soda for glass industry. As a vegetable the young shoots were collected and sold in bunches. The

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Bogemans J and Erdei L.

Fig. 5 Crithmum maritimum

Fig. 6 Crambe maritima

“agretti” type is fleshier than the “oka hijiki” type and is sometimes referred as the Italian Salicornia 5 Crithmum maritimum Crithmum maritimum is known as “rock samphire” in the United Kingdom or as “Criste marine” in France (Coiffard 1991; Cornara, La Rocca et al. 2009). Crithmum maritimum is especially known in the Mediterranean basin. The plant is rich in more than 23 different volatile oils. We can consider Crithmum as an aromatic potherb. The plant was harvested in France along the rocky shores in Brittany (France) and sold on the London markets. A traditional use was to blend leaves in butter and serve it on a fish plate. On the isle of Mallorca Crithmum leaves are pickled in vinegar. The use as a potherb was not known in Italy , instead it was known as a phyto-veterinary product.

6. Crambe maritima Sea kale was a traditional crop in France and Great Britain, typically produced bythe large gardens of castles and manors . The crop is cultivated for the shoots forced under terracotta pots. As the cultivation became too intensive for a short supply period on the market, the crop almost disappeared. The crop comes again into consideration by the work of Péron but we had to wait for a revival until Crambe maritima was positioned as sea vegetable. king on the forcing of roots like it exists for Brussels endives (Chicorum intybus L.) This approach will certainly help in making Crambe maritima towards a non-seasonal crop and by doing so improving its marketing .

7. Beta maritima Sea beet or Beta maritima is found on the higher places on the shores. The soils are saline but the plant is not flooded regularly by seawater. Sea beet has a tradition of use in Portugal and Great Britain where the plant is locally gathered. The saline environment make the leaves of sea beet tougher and improves the texture when cooking. With a saline and nutty taste, sea beet is an ideal winter sea vegetable crop. As the crop has some tradition in the UK demand for that seeds are growing in this region.

Fig. 7 Beta maritima

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Saline Crops, from halophyte research to sea vegetable markets The cultivation is merely in open soil and forced under dark conditions from November till April. Serra Maris is wor 8. Marketing of sea vegetables There are still a number of halophyte plants (Plantago coronopus L., Mertensia maritima L., Atriplex prostrata L. ‌. ) that are explored within the range of sea vegetables. However we have to bear in mind that the introduction of new edible halophytic crops should fit within the EU regulation 258/97 on novel foods and novel foods ingredients.

Through the enumeration of the various sea vegetables, the salinity of the growing medium plays an important role in building up a quality. The saline environment is responsible for the salty taste, influences the shape, texture or brings up some typical flavors. In setting up the cultivation, the grower looks to find an optimal mix between production and quality.

Salicornia can be grown under seawater conditions but in greenhouse conditions this could mean an extension of the growing period with 4 to 6 weeks and hampering the rotation system at extra costs.

As the salty taste denotes a quality marker, consumers have a changing behavior with respect to the salty tast e . British consumers are not so fond of a dominant salty taste whereas for Dutch and French enjoy the preponderant salt in the vegetables . In describing the different products the non-seasonality is an important element in building up a market. The almost constant availability of a product on the shelves draws the attention of the consumer. Another peculiar characteristic of sea vegetables like Salicornia and Aster tripolium lies in its convenience factor. Today markets are oriented towards ease of use (e.g. readymade lettuce mixtures, pre-cut green beans) and cooking. Sea vegetables like samphire , sea aster, sea kale have this advantage , they need only some short stir frying to accompany a dish.

Moreover the sea vegetables we mentioned have all a strong ethno-botanical background that can be used by a marketer to draw the attention of the customer.

Another factor which is not yet fully exploited in the marketing sea vegetables is the aspect of functional ingredients.

Sea vegetables can be a source of polyunsaturated oils, protein , carbohydrates, vitamins (Rasing, Luyten et al. 2002) the aspect of their richness in micro-elements like zinc, iodine, iron or selenium is underestimated.

Sales or production numbers on sea vegetable are nonexistent or outdated. We can only guess that the market is not yet saturated. As fruits and vegetables are long-term products once established - Products like Asparagus, egg plant , broccoli just got a boost the last ten years on the EU market- we can expect that the market of Salicornia has potential to grow.

The appreciation for taste and shape of fruit and vegetables can change along with time. It’s up to the plant breeder to

Fig. 9 Salicornia production field the Netherlands 8

Bogemans J and Erdei L. select new and better products to keep the markets going on.

9. Marketing halophyte products The above description of the sea vegetable market applies within the context of Europe According to Jansen and van Tilburg (1997) , the agro-food markets can be divided into five different stages of development (primitive, emerging, intermediate, industrialized and advanced). The EU market can be positioned into the advanced stage. For every stage the authors defined typical characteristics for supply, input markets, demand and market function. Considering less organized distribution channels, restrained access to seed and fertilizers products, the demand for product differentiation is much lower with respect to a lower developmental stage. This means that after the example of the introduction of halophytic food for compensating the malnutrition of micro-elements in regions with a less developed agro-food stage will need a more intensive marketing approach.

Besides edible crops, many studies and developments have been realized in order to demonstrate the use of halophytes. The potential of halophytes as forage crops has been widely studied (Gihad and El Shaer 1992; Le Houérou 1992; Malcolm 1996) . Clear cut solutions are found in literature, yet we are awaiting commercialization. Another current issue is the use of halophytes as biofuel. According to a recent study the scope of commercialization is not seen within the first decade. Without judging the feasibility of the potential halophytic products we must realize that in view of an average consumer their time framework is merely focused on immediate needs and any decision process will be directed by factors like availability, price or special features. These factors are only part of a total marketing mix but need some considerations in terms of establishing a “halophyte” based enterprise.

In order to draw the attention of a consumer, a product with special characteristics or properties is likely to be successful on the market . Threats for a starting company are related to the protection of the intellectual properties in order to secure the marketable product. The more the “halophyte” product is technology-based the more a starting company must be aware of alternative technologies that could shortcut the technology. A permanent innovation should be the motive for such a company.

To be and to stay on the market requires an almost continuous availability of the product. Halophyte-based products are the result of a primary production and special agricultural technologies. If cultivation hampers and/or yields work out badly the supply of the products is at risk. The further the marketable product is down the production chain the slower will be the response to counteract the need for raw materials. Establishing a stock of raw materials is sometimes a solution but represents a cost even before the product is sold.

Price is another important aspect that defines the marketable “halophyte” product. The more exclusive the product is, the higher the freedom to settle the price. If the halophyte product is, however, positioned among basic commodities (e.g. biofuel, feed products) the price of the halophyte product must be competitive with available products .

10. Marketing saline agriculture All elements of the marketing mix as partially described above define the “halophyte” product with its unique selling properties (USP). Considering the saline agricultural practices as part of the unique selling properties of a “halophyte” product is not relevant. Saline agriculture or more precisely saline agricultural biotechnology is more focused on the production process instead of the product itself.

In promoting its products Serra Maris is offering seed material and cultivation technology with consultancy. Within any product chain of “saline” raw materials the production technology plays an important role. The transfer of this technology should be considered as a marketable “services” product on itself and part of the “halophyte” product.

Also with respect to the technology, the use of Salicornia sp. is often used as model to emphasis the extreme boundaries wherein saline agriculture can work. Though the exceptional physiological characteristics of the plant, the crop has limitations in offering “halophyte” products. In promoting saline agriculture - besides the technology - more emphasis should be put on the diversity of potential halophyte crops and the wide range of preferable unique products.

11. Acknowledgement The authors wish to thank the organizers of the workshop “Sustainable cultivation and exploitation of halophyte crops in a salinizing world’ held at the Vrije Universiteit in Amsterdam on the 18th and 19th April 2012. Supported by COST FA0901.

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Saline Crops, from halophyte research to sea vegetable markets

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National Germplasm Resources Laboratory, Beltsville, Maryland.

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(1990). “Notes on Economic Plants. Barilla (Salsola soda, Chenopodiacea).” Economic Botany 44(3): 9.

(2010). “COUNTRY REPORT ON THE STATE OF PLANT GENETIC RESOURCES FOR FOOD AND.” from http:// www.fao.org/docrep/013/i1500e/Japan.pdf. .

Blankaart, S. (1698). Den Nederlandschen Herbarius, Stafleu’s wetenschappelijke uitgever maatschappij B.V. Alphen aan de Rijn/Brussel.

Coiffard, L. (1991). “A historical survey of the medicinal and alimentary use of Crithmum maritinum.” Rev Hist Pharm (Paris) 38(290): 313-317.

Cornara, L., A. La Rocca, et al. (2009). “Traditional uses of plants in the Eastern Riviera (Liguria, Italy).” Journal of Ethnopharmacology 125(1): 16-30.

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Halophytes as a resource for livestock and for the rehabiltation of degraded lands. V. R. Squires and A. T. Ayoub. Dordrecht, Kluwer Academic Publishers: 77 - 96.

Glenn, E., N. Hicks, et al. (1996). Seawater irrigation of halophytes for animal feed. Halophytes and biosaline agriculture. R. Choukr-Allah and C. V. Malcolm. New-York, Marcel Dekker, INC.: 221 - 236.

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Huiskes, A. H. L., R. Lemeur, et al. (1997). Final report 1996 Summary A contribution to the diversification of the production of vegetable crops by research on the cultivation methods and selection of halophytes. EC contract AIR3-CT92-0198: 1-11.

Le Houérou, H.-N. (1992). Forage halophytes and salt tolerant fodder crops in the Mediterranean Basin. Halophytes as a resource for livestock and for the rehabiltation of degraded lands. V. R. Squires and A. T. Ayoub. Dordrecht, Kluwer Academic Publishers: 123-138.

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Martins, C., S. Duvekot, et al. (1997). Cultivation methods of some halophytic crops. A technical report. Final report - Part 4 - A contribution to the diversification of the production of vegetable crops by research on the cultivation methods and selection of halophytes. EC contract AIR3-CT92-0198: 487 - 496.

Peron, J.-Y. (1987). “4665031 Clone of the sea kale (Crambe Maritima L.), and process for vegetative propagation thereof: Jean-Yves Peron, Angers, France assigned to Ecole Nationale d£3 Ingenieurs des Travaux.” Biotechnology Advances 5(2): 420.

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Sági, B. and L. Erdei (2002). “Distinct characteristics of two subspecies of Aster tripolium L.” Acta Biol. Szeged 46(34): 257-258.

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