Strawberry production in forced and protected culture in Europe as a response to climate change

Transcription

1 Strawberry production in forced and protected culture in Europe as a response to climate change Davide Neri 1, Gianluca Baruzzi 2, Francesca Massetani 1, and Walther Faedi 2 1 Dipartimento di Scienze Agrarie, Alimentari e Ambientali, Università Politecnica delle Marche, Via Brecce Bianche Ancona, Italy ( d.neri@univpm.it); and 2 Consiglio per la Ricerca e la Sperimentazione in Agricoltura, Forlì, Italy. Received 15 December 2011, accepted 5 April Neri, D., Baruzzi, G., Massetani, F. and Faedi, W Strawberry production in forced and protected culture in Europe as a response to climate change. Can. J. Plant Sci. 92: In Europe, the production of strawberry for fresh market in forced and protected conditions is increasing. These techniques were initially aimed at enhancing the earliness of Junebearing short day varieties. Nowadays, the objective is to have year-round fruit availability, forcing and preserving strawberry crops against adverse weather conditions. The new high-quality low-chilling varieties widely expanded winter spring strawberry production in the Mediterranean climate with autumn planting, while the diffusion of day-neutral everbearing varieties increased springsummer yields in more continental climates, avoiding the extremely cold winter with spring planting. Finally, the use of tray-plants significantly increased late summerfall strawberry production with summer programmed planting. The present review analyzes the recent evolution of strawberry cultivars and cultivation systems under plastic tunnels and in greenhouses. The physiological effects on plant architecture and propagation are discussed. In conclusion, we can affirm that strawberry growers are facing climate change with innovations in cultivated varieties and cultural techniques, and by the integration of the different production areas, with their specific optimum yield seasons, to continuously fulfill the demands of the European market. Key words: Fragariaananassa, forcing and protecting systems, plant propagation, flower induction, plant architecture, stress Neri, D., Baruzzi, G., Massetani, F. et Faedi, W Strawberry production in forced and protected culture in Europe as a response to the climate change. Can. J. Plant Sci. 92: En Europe, la culture force e et sous serre du fraisier est en augmentation. Les techniques de forçage visent, initialement, a` accroıˆtre la pre cocite des variétésa` jour court. Aujourd hui, le but est d obtenir une disponibilite de fruits pendant toute l anne e sur les marche s europe ens, en forc ant et en pre servant les cultures de fraisiers contre les conditions météorologiques de favorables. Les nouvelles variétés a` faibles besoins en froid ont e tendu la production de fraises pour la re colte en hiverprintemps sous des conditions Me diterrane ens. La diffusion croissante des variétés remontantes à jour neutre augmente la re colte en printempse té sous des climats continentaux. L utilisation des plants en mot permet une augmentation de la production de fraises en fin étéautomne. L e volution re cente des cultivars de fraisier et de techniques dans les tunnels en plastique et dans les serres seront ici analyse s ainsi que leurs effets physiologiques sur l architecture des plantes et sur les syste` mes de propagation. On peut conclure que les producteurs de fraises font face au changement climatique par l innovation des varie te s et des techniques, et par l inte gration des zones de production diffe rentes pour combler continuellement les marche s europe ens. Mots clés: Fragariaananassa, systèmes productifs (hors saison), propagation, induction florale, architecture de la plante, stress During the past 40 years, the cultivated area, varieties and cultural techniques of the European strawberry industry have changed considerably. The general tendency has been to maximize the harvest period. This is now being achieved in the different growing regions through the use of (i) new ever-bearing varieties (especially in centralnorthern Europe), (ii) low-chilling June-bearing varieties (in southern Europe), (iii) specialized growing techniques and (iv) crop protection and forcing systems. To protect the crop against temporary inclement weather conditions, single or multiple light plastic tunnels are generally used, with limited influence on the plant growing cycle. To advance or delay the harvest period, plastic and glass houses are the most common forcing systems (Castilla 2002). The recent evolution of strawberry cultivars and cultivation systems under protection and forcing systems has been reviewed in the perspective of a changing climate. For strawberry cultivation, Europe can be divided into three wide areas with different climate conditions: Northern Europe with severe winters, normally characterized by snow covering; Central Europe with occasionally severe winters and relatively mild autumns and springs; Southern Europe with mild winters where the temperature is almost never lower than 08C. Abbreviations: A, big bare-rooted plants; DN, day-neutral; JB, June-bearing; LD, long day; SD, short day; TP, tray-plants; WB, waiting bed (plants) Can. J. Plant Sci. (2012) 92: doi: /cjps

2 1022 CANADIAN JOURNAL OF PLANT SCIENCE In northern Europe (Scandinavian countries and the Baltic Republics), strawberry cultivation is currently practiced in almost ha [Food and Agriculture Organization (FAO) 2011]. After a constant increase in strawberry acreage during the 1970s and the 1980s, there is now a contraction phase, which started in the mid- 1990s (Fig. 1). The northern strawberry industry differs from the rest of Europe, because strawberry fields commonly last for 24 yr, while in the rest of Europe, strawberry cultivation is annual or for a shorter period. The traditional harvest period is in late spring or early summer, and it is very short. Most strawberry fields are traditionally cultivated as open field, although plastic tunnel protection allows a significant earliness. The purpose of this protection is also to prevent strawberry plants from possible damage by severe cold, especially during full blossom in early spring. In limited areas (around 10 ha) soilless forced culture has been introduced. This technique requires the use of fertigation and heating systems in order to maintain plant growth and avoid frost damage during winter, and the high costs of heating limit its diffusion. The dominant varieties are the high chilling Junebearing (JB) type. In open field, the most cultivated varieties are cold-resistant Polka, Sonata, Honeoye, Bounty, Senga Sengana and Korona, while, in forced conditions (and soilless systems), the most frequent is the high fruit quality Elsanta (80%), followed by Darselect (15%) and Lambada (5%). In central Europe, the two main strawberry-growing countries are Poland and Germany (FAO 2011). In Poland, almost ha are currently cultivated with strawberry. There was a significant increase in acreage in the 1970s, the 1980s and partially in the 1990s, while the cultivated area has held steady during the past Surface (ha) North South Center + Poland decade. Nowadays, the change is from the traditional growing culture for frozen fruits toward fruit production for the fresh market. The traditional variety, Senga Sengana, has mostly been replaced by Elsanta, Kent, Honeoye and, recently, by the new ever-bearing varieties. In Poland, production under plastic tunnel is still not widely used. In Germany, almost ha are cultivated with strawberry and North Rhine-Westphalia and Baden- Wu rttemberg are the two main areas. The June-bearing varieties Elsanta and Darselect and the ever-bearing Charlotte and Evie 2 are the most widespread cultivars. Germany is the only European country that has registered a vast acreage increase in the past decade. In particular, protected culture under plastic, multiple, and single tunnels, has been greatly expanded, reaching 35% of the total acreage. It is worth noting that this protection has made possible the expansion of the harvest season, particularly in the earlier period, allowing an increase in the consumption of domestic strawberry in competition with imports from the Mediterranean areas. The forcing systems, using greenhouses, are operated in very limited areas in south Germany, with the aim of obtaining very early production, which is greatly appreciated by consumers, who prefer a local product, even though it is out of season. In any case, open field production is still very important, and it includes traditional spring and early-summer production, and the innovative so-called 60-day programmed cultures for late summer and autumn production with summer planting of flower differentiated fridge-stored plants (waiting bed, A and tray). Also, the new ever-bearing varieties with spring planting are increasing, which are able to bear fruit during the whole of the summer until the autumn Space of time (year) Fig. 1. Evolution of cultivated strawberry acreages in Europe (FAO 2011) The values are averages of 3 years.

3 NERI ET AL. * FORCED AND PROTECTED STRAWBERRY PRODUCTION IN EUROPE 1023 During the past few years, in Belgium and the Netherlands (Fig. 2) the forcing culture has progressively developed and it currently covers 10% of the total acreage (FAO 2011). Elsanta is the dominant variety (Lieten 2005; 90% of protected culture), followed by Darselect, used in very early forcing systems, and by the new ever-bearing cultivars Camarillo, Albion and Charlotte. To avoid infection by soil-borne pathogens, about 30% of protected cultures is soilless. Recently the strawberry production cycle was shortened in forcing culture using the 60-day programmed culture, with different planting dates, and this system has been expanding to meet the off-season market demand. Also, in the United Kingdom, the strawberry acreage under plastic multiple tunnels has greatly increased, reaching over 2000 ha. A great expansion of soilless culture is also being recorded. Elsanta is the most cultivated June-bearing variety followed by Sonata. The new ever-bearing varieties such as Evie2, Ava, Everest, Elsinor, Jubilee and Camarillo represent about 35% of the production (Lieten 2011). In France, in the past decade, the acreage of cultivated strawberry has shown a drastic reduction ( 30%; FAO 2011), while soilless culture under multiple tunnels has increased considerably, especially in southern areas for extra-early production (January February). The early June-bearing variety Gariguette is still the most cultivated (60%), followed by Darselect (25%). The most popular ever-bearing varieties are Mara de Bois and Charlotte, which are grown only in protected culture (single or multiple tunnels). In southern Europe, Huelva (southern Spain) is the most important strawberry production area, although in the past decade, the local strawberry acreage has been considerably reduced, from ha in 2000 to about 6500 ha at the moment (Lopez Aranda, personal communication). Recently, because of the limitations of soil fumigants, soilless culture has been increasing rapidly, reaching 130 ha. The whole cultivated area is protected under plastic tunnels (Fig. 3) Fig. 2. Forced strawberry production in the Netherlands a few days after planting the programmed tray-plants. Fig. 3. Forced strawberry production in multiple tunnels in Huelva (southern Spain). Photo courtesy Lopez Aranda. with autumn plantation of freshly dug plants to have winterspring production. In the past, micro-tunnels (generally protecting two rows, in this area) were predominant, but growers have recently moved to the macro-tunnels (actually 85% of the protected areas) to obtain earlier ripening and less fruit decay, caused by Botritys cinerea, during the beginning of the harvest, when rain is relatively frequent. The harvest season in Huelva is from January to June. The main varieties are the low-chilling June-bearing Sabrosa-Candonga (40% of the total acreage, slightly decreasing), followed by Splendor (22%, stable) and Camarosa (22%, strongly decreasing). The new varieties, Florida Fortuna, Benicia and Antilla, are rapidly entering the Spanish variety standard. In Italy, the acreage of cultivated strawberry has decreased considerably in the past two decades. It was around ha in the 1970s and has now reached 3500 ha, holding steady during the past 2 yr (Centro servizi ortofrutticoli Ferrara 2011; Istituto Nazionale di Statistica 2011). The two main production areas are the northern regions (with a climate similar to central Europe), where high chilling varieties are cultivated, and the southern regions (with mild climate conditions), suitable for low-chilling varieties. Over the years, the two production zones have evolved differently: in the south, where all the fields are protected by single and multiple tunnels (since the 1970s), the decrease in strawberry cultivation has been very low, while in the North, where the use of protection developed more slowly, the decrease in cultivated acreage was dramatic. The only northern zones that have not been affected by this decrease in the past decade are those protected by plastic tunnels (as in Verona with the autumn culture ; Fig. 4). The other areas (e.g., Cesena), which have traditionally grown strawberry in open field, have recorded a strong reduction. In the mild Mediterranean climate, with the protection of plastic tunnels, the harvest period is very long (about 6 months) and production is very high.

4 1024 CANADIAN JOURNAL OF PLANT SCIENCE Fig. 4. Protected strawberry cultivation in single and multiple high tunnels in northern Italy. Thus, although the area of strawberry cultivation in north-central Europe is far greater than in southern Europe (Spain and Italy), the entire production from the two main areas does not differ very much. As a paradigm, in Italy, from the peak of the expansion of strawberry culture in the 1980s until now, protected acreages have held steady, while open field areas have undergone a strong reduction (Fig. 5). PROTECTION AND FORCING TECHNIQUES AIMED AT REDUCING CLIMATIC RISKS: DESCRIPTION OF THE FEATURES OF DIFFERENT REGIONS TO EXTEND HARVEST SEASON In northern countries, protected culture with unheated plastic tunnels is particularly risky because this type of tunnel allows considerable early blooming, but does not provide enough protection for strawberry flowers or, eventually, the plants, if the temperature falls far below Surface (ha) C. Spring frost can irreparably damage fruiting, or reduce the quality (i.e., cat face fruits). In this climate, only greenhouse production using forcing systems (artificial light and heating) may allow production of strawberry for an extended time during the winterspring period. In central European countries, two types of protection systems are widespread. The first helps plants from damage caused by rain, hail, wind and sun, with limited influence on picking earliness. Light and inexpensive plastic tunnels are adopted only with uncovered sides. In this kind of tunnel application, the plants are not affected at the physiological level because of the shorter period of protection and also because of a very limited greenhouse effect. For June-bearing varieties in traditional annual culture, the planting period is JulyAugust, with flower induction and differentiation in SeptemberOctober, dormancy in autumnwinter and the very short harvest period in the spring; the protection is set over the crop when the plants start blooming after winter. In this case, the temperature and relative humidity must be controlled at blooming, because pollen viability and germination are known to be affected by these two factors (optimal ranges, although depending on varieties, are 20308C and 5060% relative humidity). The risk of reduced pollen fertility is high in high temperatures (308C or more), and this can cause damage in the form of misshapen and malformed fruit. For ever-bearing varieties, the planting time is generally in the spring using standard cold-stored plants, flower induction and differentiation are continuous and the harvest season is extended into the summer and the fall. Therefore, single or multiple tunnels are used to protect crops from damage caused by inclement weather conditions in the summer (rain, hailstorm, sun damage). Shading nets are increasingly used over the plastic tunnels to avoid Protected culture Open field Time (year) Fig. 5. Protected culture and open field culture in Italy (Istituto Nazionale di Statistica 2011; Centro servizi ortofrutticoli Ferrara 2011).

5 NERI ET AL. * FORCED AND PROTECTED STRAWBERRY PRODUCTION IN EUROPE 1025 damage from excessive sunlight, and in some cases shading nets alone are also needed to protect the fruits in the open field (Fig. 6). The second system is adapted to advance earliness. It requires heavy structures made of single or multiple tunnels of various lengths and sizes depending on the climate conditions of the area (windy, snowy, etc.). They are generally covered during winter, when the plants have satisfied their specific chilling requirements. This advances ripeness by about a month compared with open field cultivation. The tunnels are equipped with opening mechanisms providing the necessary ventilation (Montero et al. 2009). Monitoring of temperature and relative humidity is very important during blooming. Better temperature control can be obtained by opening and closing sprinkler irrigation on the leaves inside the tunnel. Shadow nets or lime application over the plastic film are used to prevent sun damage at picking time. This protection system also allows first production in early autumn by planting already induced plants in the summer and covering the tunnel during blooming in the autumn. The date of the first harvest depends on the planting date; on average it is 4045 d after planting. To encourage a second picking season after the winter, covering is continued during wintertime, but the tunnels are open to satisfy plant chilling requirements. After chilling, the tunnels are completely covered to force the plants. In southern Europe, with mild Mediterranean winters, the autumn planting time is between the end of September and the end of October, depending on the area and plant type. After planting, the multiple tunnels have to be covered with plastic before the night temperature drops below 108C to keep the plants growing (forcing system) during autumn and winter. If very lowchill June-bearing varieties are used for this system, the first picking time can be advanced to November December, and production can be maintained during the whole of the winter and spring. Fig. 6. Protection with shading nets to avoid sun burn in summer cultivation. In order to avoid flower and fruit frost damage, the use of this system is confined to mild-winter conditions with temperatures never going below 08C. In some areas (like Metaponto and Piana del Sele, in Italy) where low temperatures (near 08C) may occasionally occur in wintertime, a double film cover is used, to avoid frost damage and stop plant growth. VARIETAL INNOVATION FOR EXPANDING BERRY PRODUCTION SEASON Strawberry is a species in which the interaction between genotype and environment is particularly important and a variety can hardly be adapted to cultural areas having different climate conditions. Moreover, to cope with extremely variable weather at single locations, breeders need to develop new cultivars that are adapted to multiple environments and multiple cropping systems (Dale 2009). Therefore, the evolution of strawberry varieties is particularly dynamic, and around the world, many active breeding programs continuously offer a wide range of new varieties to growers. One of the most important current objectives is to extend the harvest season. Basically, this has been achieved following two main physiological approaches: (i) introducing low-chilling June-bearing varieties able to bear fruit for longer periods during the winter and spring seasons, particularly suited for southern environments, and (ii) breeding ever-bearing varieties for springsummer production, particularly suited for north-central Europe. Both genotypes (low-chilling June-bearing and ever-bearing varieties) take advantage of cultural protection systems that prevent weather damage to achieve their fruiting potential. Moreover, forcing cultural systems can allow varieties with lowchilling requirements to grow successfully, even in northern areas (as for the new cultivar Nora successively cultivated in northern and southern Italy). Appreciably, due to the combination of new varieties and protection techniques, European strawberry production lasts 12 months and may be defined as all-yearround (Table 1). Winter production starts in January in southern areas (Spain and southern Italy) with varieties having a medium low-chilling requirement (Sabrosa Candonga, Camarosa, Florida Fortuna, Florida Festival, etc.) and it continues till June. In central Europe, production starts at the end of winter with 60 day forced cultures in southern France and in Belgium using high chilling varieties (Gariguette, Clery and Darselect), and it continues with traditional protected systems in the spring and summer using different high chilling varieties (Alba, Clery, Darselect, Elsanta). In the summer, there is also the protected production of ever-bearing cultivars (Evie 2, Charlotte, Elsinore, etc.). The 60 day programmed cultures with June-bearing varieties (Eva, Roxana, Clery), having high chilling requirements, can give good yields in any period after the cold storage of the plants. If the 60 day

6 1026 CANADIAN JOURNAL OF PLANT SCIENCE Table 1. Year-round strawberry production in Europe Jan. Feb. Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec. JB (open field) JB (open field) JB (protected and open field) North JB JB (fall), DN JB (fall), DN JB (60 day), DN JB (60 day), DN JB (60 day), DN JB (protected and open field) JB Centre JB (forced) JB (forced) JB JB lowchilling JB lowchilling JB lowchilling JB lowchilling JB lowchilling JB lowchilling South JB lowchilling June-bearing programmed plants [big bare-rooted plants (A), waiting bed plants (WB) and tray-plants (TP)], depending on the propagation system) are planted in JulyAugust, they can bear fruits at the end of the summer to the beginning of autumn. In this case, the plants can be maintained quiescent during the winter and recovered for a second harvest period in the spring of the following year. For north Europe in open field production, in order to provide environmentally resilient cultivars for the sustainability of future fruit production, breeders require accurate and high-throughput phenotyping protocols for the identification of the varying levels of chill requirement in the available germplasm (Jones and Brennan 2009). TECHNICAL INNOVATION FOR PROGRAMMING THE HARVEST SEASON Plant propagation techniques can modulate many abiotic factors and modify growing conditions, leading to the control of intrinsic plant vigor and development, such as stolon formation, crown branching, flower induction and differentiation. Moreover, different types of plants can be stored in a cold room (at 1.58C) for 2 to 10 months, or even longer, with very limited damage, even though damage increases with time of storage. As a consequence, the plant structure (architecture), the yield potential and the time of fruit ripening can be programmed in the nursery and appropriately maintained in the cold storage facilities up to transplanting in protected or forced systems, or even in open fields. Knowing the plant dimension and architecture (number of inflorescences and flowers per inflorescence, and their phenological phase) after propagation, the amount of chilling (already satisfied and what is missing), the day length and the growing degree hours available after planting, the potential fruit production (entity and quality of the production and earliness and duration of the harvest period) can be planned in a predictable way. According to the desired production system in the nursery and after transplanting, growing techniques can be changed and modulated for any specific genetic material, type of propagation and cultural techniques, such as planting date, fertigation system and forcing conditions. TYPE OF PLANT PROPAGATION AND CROP PRODUCTION CYCLES In the past, when cultivation was polyennial, barerooted freshly dug stolon plants (fresh plants; Fig. 7) of June-bearing varieties were transplanted in the autumn or spring, depending on winter climate (hardiness zone). Subsequently, when annual production systems with a short harvest period (about 30 days) in the spring became very common, bare-rooted stolon plants were dug in the winter and cold stored (frigo plants) until summer planting (in JulyAugust). In this case, the root

7 NERI ET AL. * FORCED AND PROTECTED STRAWBERRY PRODUCTION IN EUROPE 1027 Fig. 7. Freshly dug plants from a highland nursery in Spain. Photo courtesy Lopez Aranda. system mainly serves to overcome the transplanting shock and subsequently degenerates and is rapidly substituted after planting, while leaves are eliminated before storage. The frigo plants have only one terminal bud (crown) with a single inflorescence, differentiated in the preceding year before the cold storage period. Generally the flowers have poor quality and are partially damaged by the long storage period, but the vegetative aptitude (stolon formation) remains very high. To stimulate plant set after planting and lateral bud formation (new crowns), stolons and flowers must be removed. In this way, the growth period at the end of the summer and during the autumn can allow the formation of an increasing number of lateral buds (Savini et al. 2005), with good flower differentiation (Figs. 8 and 9). Therefore, the yield per plant in the following spring can be very high, with big fruits and a short harvest season. The annual system, with single spring production, was able to increase the average fruit size and to reduce labor cost. In fact, for ever-bearing varieties, the frigo plants are usually transplanted in March. In this case, yield is delayed, but it continues from the beginning of July until October. The first inflorescences are removed in Mayearly June to promote plant set and strong initial vegetative growth. The frigo plants suffer from transplanting (i.e., in SeptemberOctober) only when they are stored for too long, and are not able to grow well and thus to properly differentiate flowers. For this reason, in order to have production starting in December or January in mild climates (in Mediterranean conditions such as south Italy and Spain) fresh bare-rooted plants are substituted for the frigo plants. In this case, the varieties are lowchilling and fast growing in the autumn. The fresh plants are from high-elevation Spanish nurseries or from central Europe (mainly Poland). In both cases the plants are dug from the nursery, graded, transported and planted in the production fields as fresh plants within 23 days. In nurseries, the runner plants undergo important physiological changes (carbohydrate accumulation in the crown, hardening, flower induction, and partial chill satisfaction) in early autumn as a result of exposure to chill ( B78C). In general, a high-quality fresh plant, with proper management will produce large, well-shaped, high-quality fruit during an extended harvest season (JanuaryJune). Nowadays, to program the out-of-season production in central Europe, different types of programmed plants (for 60 day cultures) are increasingly used: tray-plants (TP), waiting bed (WB), and A. To produce trayplants, the stolons are harvested from the mother plants and planted in August in trays filled with a peat substrate (Lieten 2000). In the nursery, the tray-plants are characterized by very rapid growth in late summer and early autumn. The new runners eventually formed after planting in the tray must be removed quickly in SeptemberOctober. At the same time in autumn, adequate thermo-photoperiodic conditions for floral induction must be provided if not naturally occurring. Then, after the growth ceases due to low temperatures (November to January), the tray-plants (Fig. 10) are moved with all the substrate into the climate-controlled chambers at low temperature ( 28C) for cold storage until they are planted for programmed production. After cold storage (up to several months) the tray plants are ready for planting in different seasons because they are already well flower induced and do not need additional chilling. The stolons prepared in the summer can last longer in the nursery fields with favorable conditions and plastic tunnel protection (WB plants) in order to form more than one differentiated crown per plant and to obtain a potential production of g of fruit per plant, once they are planted in the field or in protected conditions. They are stored with bare roots under the same refrigeration conditions as the tray-plants and planted in sequence from the end of April until the middle of July. They are suitable for late cropping systems, with harvest from early July to September for annual cropping outdoors and during the autumn under plastic tunnels. With later planting in spring summer conditions, yield can decrease because of high temperatures. Plant performance intermediate between frigo plants and WB plants can be obtained selecting big plants from the nursery after flower differentiation (commercial class A or A frigo plants) and cold storing in the same refrigerated condition. A plants show a good potential to produce after transplanting, but generally less than 400 g fruit per plant. They are generally planted in MayJune, extending the cropping season from the beginning of July until the end of August (Faby 1996). It is possible to set a second planting date with Aplants or tray-plants of particular cultivars, after the end of the first crop.

8 1028 CANADIAN JOURNAL OF PLANT SCIENCE Fig. 8. Strawberry crop producing cycles. (A) Spring production with frigo plants; (B) winter, spring production with fresh plants; (C) fall, winter, spring production with fresh plants; (D) out of season production with tray-plants. Plant architecture shows significant modification as a consequence of the date of forcing. The plants respond to environmental signals, such as low temperatures, in different ways depending on the physiological phase of different organs and their relative positions (Sugiyama et al. 2004). As an example, axillary meristems at maximum level of dormancy (middle of September in France) do not develop secondary shoots after placing the plants in the greenhouse. As the chilling requirement is increasingly satisfied, the axillary meristems initiate new secondary shoots, but when the temperature is too cold (delayed placing in the greenhouse after the end of October) lateral growth can be penalized (Savini et al. 2006a). In the nursery and in the field, several different techniques are available to control plant growth, which can interfere with the plant propagation techniques. Removal of part of the leaves stimulates compensatory growth of the plant (Hansen 1996) and shoot formation in the basal part of the crown, with potential inflorescences coming from existing meristems; plant vigor and fruiting increase (Guttridge et al. 1960). Small coldstored plants transplanted without leaves have small vegetative growth compared with larger tray, waitingbed or frigo plants transplanted with initial leaves (Palha et al. 2012). Plant defoliation after repotting produces low nutritional status that can reduce the number of flowers and then inflorescence size. Plant deblossoming increases leaf (Daugaard 1999) and runner production in some cultivars (Scott and Marth 1953; Robertson and Wood 1954; Moore and Scott 1965), while other cultivars require combined deblossoming and defoliation, and in some genotypes flower removal does not promote runner production (Waithaka 1985). Removal of runners stimulates and hastens branch crown development (Hancock 1999). Planting date does not affect vegetative growth, whereas later planting dates in autumn production systems (Palha et al. 2012) can increase the number of flowers and inflorescences. Early transplanting stimulates shoot formation and flower differentiation, whereas late transplanting reduces crop load. Advancing

9 NERI ET AL. * FORCED AND PROTECTED STRAWBERRY PRODUCTION IN EUROPE 1029 Fig. 9. Strawberry architecture of different plant types. (A) Frigo plant planted in July; (B) fresh plant planted in September (modified from Savini et al. 2005). the plugging date of June-bearing plants [short day (SD) plants] to early July can induce the plants to flower early (Takeda and Newell 2007) instead of growing transplants in artificial, SD and low-temperature conditions in late summer (Verheul et al. 2006, 2007). When the formation of shoots stimulates prolonged and not simultaneous fruit production, delayed planting is necessary. When delayed transplanting is needed, the plants must already be differentiated from the nursery. Small planting distance (high density) affects lateral shoot growth, giving an advantage to the uppermost buds. PLANT ARCHITECTURE AND CONTROL OF FLOWER DIFFERENTIATION The reproductive and vegetative behavior of strawberry plants is known to be sensitive not only to temperature and photoperiod, but also to several agronomic and nutritional factors, such as mineral nutrition and water supply (Guttridge 1985), which determine the growth rate and the presence of stress. Programmed environmental conditions may control plant growth and development, and assume a key function in determining plant quality in relation to different internal physiological factors of the plants, interacting with the physiological processes which lead to flower induction and differentiation. Agronomic and nutritional factors may establish which kind of growth (vegetative or reproductive) needs to be strengthened. The knowledge of environmental and growth factors that affect the generative and vegetative behavior of the plants is therefore strategic to improve yield and fruit quality by anticipating or delaying flower induction and determining inflorescence number and dimension. Plant architecture, which describes the spatial distribution of vegetative and reproductive organs and their developmental phase, is therefore useful to evaluate plant quality and to predict production (time and quantity). Furthermore, tray-plants propagated under different growing conditions in the nursery, coming from different nurseries or growing systems and countries may show differences in plant vigor and fruit production. The formation of a different number of lateral flower buds and the modified ability of the plant to form new shoots along the central axis are also linked to different developmental phases of floral buds (Kurokura et al. 2005; Van Delm et al. 2009). Environmental factors interact with plant physiology and architecture mainly through the modification of whole-plant vigor. As a consequence, planned and controlled water stress or differently balanced fertigation can be effective means of inducing and controlling flower formation. Fig. 10. Tray plant before the cold storage period. PHOTOPERIOD, LIGHT INTENSITY AND QUALITY The photoperiod is a primary environmental factor controlling the transition from vegetative to reproductive growth in strawberry, and cultivars are usually classified on the basis of the photoperiod sensitivity of their flowering characteristics. Artificial light or lightproof coverings can be used to alter light availability

10 1030 CANADIAN JOURNAL OF PLANT SCIENCE and thus the occurrence of flower differentiation and the plant architecture (Bosc and Demené 2009), according to the specific needs of each plant genotype. For instance, flower induction and blooming ability can be delayed by the application of long day (LD) conditions on short day (SD) plants (Bosc et al. 2012). Flower initiation in June-bearing SD strawberries may be regulated by light quality (Collins 1966; Vince-Prue and Guttridge 1973) and intensity. Thus, climate change, to some extent, can be mitigated using covering nets that affect the intensity and quality of the light reaching the plants. As an example, a reduction in light intensity (85% shading) along with the associated lower temperature can increase flower induction, but only during the period of reducing day-length (Kamakura and Shishido 1985). As well, increasing the amount of shade on the plant may induce a reduction in crown dimension (Wright and Sandrang 1995) as well as the number of leaves and inflorescences (Awang and Atherton 1995), whereas increasing light intensity can enhance flower differentiation (Dennis et al. 1970; Chabot 1978). Photo-selective nets placed over the plants may select the light signal that stimulates flower initiation. In fact, the spectral composition of the irradiation appears to quantitatively affect flower bud initiation (Takeda 2012). In particular, red and blue nets prevent flower initiation (Takeda 2012). Light quality interacts with the responsiveness to photoperiod. LD conditions do not delay floral initiation if the extended lighting is with red light, but do delay floral initiation with far red or a combination of low red/far red (Vince-Prue and Guttridge 1973; Kadman-Zahavi and Ephrat 1974; Guttridge 1985). Fig. 11. Relation between photoperiod and temperature to induce reproductive (flower induction) or vegetative development (modified from Ito and Saito 1962). TEMPERATURE CONTROL Temperature affects the response of flower induction to photoperiod in both SD and day-neutral (DN) cultivars (Fig. 11). Temperature is considered to be as important as photoperiod for flowering at high latitudes, where long photoperiods prevail (Heide 1977). Temperature also affects the rate of flower initiation and the number of flowers within the inflorescences without significant control of photoperiod. Flower bud formation takes place in a range of optimal temperatures and can be totally (Ito and Saito 1962; Chabot 1978) or partially (Okimura and Igarashi 1997; Verheul et al. 2006) inhibited at prolonged high temperatures, higher than 268C (Durner et al. 1984) or 308C (Ito and Saito 1962; Chabot 1978; Durner and Poling 1988; Okimura and Igarashi 1997). In warm areas, such as at tropical to equatorial latitudes, strawberry can be commercially grown only in the highlands, where temperatures are lower. Moreover, natural daily fluctuation of temperatures (26.7/15.68C day/night) induces earlier flower formation compared with a constant temperature of 218C (Hartmann 1947), or higher (35/258C) day/night temperatures (Bish et al. 1996). Fluctuating temperatures can be artificially applied to reproduce natural environment in forced conditions or to manipulate flower induction (Reichart 1973; Chabot 1978; Durner et al. 1984; Bish et al. 1997) in specific climate areas. Climate changes can increase summerautumn night temperature (Palencia et al. 2009; Sønsteby and Heide 2009) that often are sub-optimal in cold areas. Temperatures below 15.68C delay flower differentiation (Darrow 1966). Cold temperatures (below 7108C) effective in overcoming dormancy (chilling) may induce strong vegetative growth (Guttridge 1958; Voth and Bringhurst 1958; Pringer and Scott 1964; Wahdan and Waister 1984; Tehranifar et al. 1998). Cold treatments can be applied to avoid the decrease in vegetative vigor in greenhouse strawberry production. Exposure to chilling to a certain extent reduces flower induction and stimulates floral differentiation (Durner and Poling 1987), along with leaf number and runner formation (Bringhurst et al. 1960; Porlingis and Boynton 1961; Piringer and Scott 1964; Bailey and Rossi 1965; Guttridge 1969; Braun and Kender 1985; Rice 1990; Kahangi et al. 1992; Lieten 1997; Tehranifar and Battey 1997). In warm regions, chilling preceding the optimum digging date in the nursery may be advantageous for early fruit production, while extra chilling after the optimum digging date may reduce flowering (Durner and Polling 1988). A lack of cold can be compensated by artificial lighting (Van Delm et al. 2012), especially in the greenhouse. During prolonged cold storage (frigo plants) widely applied for programmed cultivations, sugar and starch content can decline and this is correlated with a decrease in the number of emerging inflorescences and flowers (Molot and Leroux 1973; Kinet et al. 1993; Dradi et al. 1996; Sønsteby and Hytonen 2005) mainly below the last expanded leaf (Bosc et al. 2012). Further, the stress related to the duration of cold storage may result in earlier flowering (Lieten et al. 1995).

11 NERI ET AL. * FORCED AND PROTECTED STRAWBERRY PRODUCTION IN EUROPE 1031 LOCATION Like transplanting, environmental conditions for propagation can also be modulated by changing the location (altitude and latitude). Plants can be propagated under favorable conditions for floral induction in northern areas and then transplanted in southern areas to stimulate floral organ formation and development. The location of the nursery affects flower induction, which takes place earlier at higher altitudes (Savini et al. 2006b), whereas environments with a long photoperiod and relatively high temperature minimize flower induction and promote vegetative growth, resulting in a different number of flowers per plant (Savini et al. 2006b). In tropical climates at low altitude (higher temperature), plants show reduced vegetative growth and develop fewer leaves compared with plants at higher altitudes (Riyaphan et al. 2005). In the Alps, transplanting from a high to a low altitude allows a longer flower induction and differentiation period with the production of more flowers per plant and earlier fruit harvest (Savini et al. 2006b). Thus, fresh plants from Spanish highland nurseries ( m) are dug up in the first 10 days of October and transplanted to southern Italy or Spain in order to provide good fruit production beginning in February (Savini 2003). In southern Italy, the majority of flower differentiation takes place in 2nd and 3rd order buds on the extension crown because the mild weather during the autumn allows a prolonged period favorable to differentiation. In this condition, vegetative growth may be easily resumed using a flashlight or gibberellin application (Aspuria and Fujime 1995; Robert et al. 1999). The location of cultivation notably modifies the ability of the plant to form new crowns along the principal axis, for instance more crowns in central and northern Italy and fewer in the south, which has a warmer winter. Conversely, the total number of inflorescences per plant increases going south. In southern Italy, later planting, under cooler temperatures and short photoperiods, which are favorable to flower differentiation, caused less vegetative growth and the formation of only one extension crown per plant. Moreover, in northern Italy, the inflorescence in the primary bud has a greater number of flowers (1314 per inflorescence) in comparison with the south (around 10 per inflorescence; Savini 2003). This behavior could be due to the prolonged favorable conditions for differentiation that are common in northern Italy during the growth of the primary buds at the beginning of autumn. This favorable period is drastically shorter during secondary bud differentiation because of the early arrival of the cold in autumn. In the south, the time for differentiation has a tendency to sustain a constant differentiation for the whole of the warm autumn, and both orders of inflorescence have a similar number of flowers (Savini 2003). Planning strategies and techniques with fresh plants also allow the control of the vegetative and generative behavior of the plants. Large thermal fluctuation between day and night and low summer temperatures (high altitude) are favorable conditions for fresh plant production in nurseries: flower induction takes place early and leads to more inflorescences than in the lowlands. These conditions in tray-plants also stimulate vegetative growth (Savini et al. 2006a). Changing growing areas thus makes it possible to program the synchronicity and the duration of cropping. NUTRIENT SUPPLY Nutrient level and type of substrate strongly influence the growth and architecture of the plant (Savini 2003; Savini and Neri 2004). In particular, the relative ratio between nitrogen and phosphorus content plays an important role in the control of vegetative equilibrium. Nutrient supply throughout the growing season allows the control of the number and degree of development of the inflorescences. In particular, timing of nitrogen supply affects flower initiation in different ways, and the amounts of nitrogen increase the inhibition or stimulation effect. In relation to the predictable interaction with plant architecture and growth, the nutritional protocol should be managed in different ways during propagation in the nursery and during plant growth. High nitrogen availability can stimulate both stolon and shoot formation, depending upon the supply time and plant growth rate (Savini 2003; Savini and Neri 2004). When the growth of the apex is fast, due to excess nitrogen in fertilization, stolon formation is induced and flower induction can be negatively affected (Fujimoto 1972; Furuya et al. 1988; Matsumoto 1991; Yamasaki et al. 2002) causing a delay in flower differentiation or totally preventing flower formation (Yamasaki et al. 2002). If high nutrient supply stimulates vigor after apex growth is stopped, axillary latent meristems are reactivated to growth, and generate shoots in the basal part of the crown increasing the total number of possible inflorescences (the so called vampire buds ). Later fertilization can stimulate shoot formation in the upper portion of the plant, bearing less developed flowers compared with terminal primary inflorescence, increasing the total number of inflorescences, with a longer cropping time. With a continuous supply of nutrients, lateral shoot outgrowth takes place from the apical part and continues downwards, whereas, if the fertigation is suspended for 12 wk when the growth is maximum, shoot formation occurs exclusively from apical buds and flower differentiation is advanced (Fig. 12; Savini 2003). Therefore, reduced nutritional level depresses vegetative growth and can promote flower induction (Guttridge 1985) and production of more flowers. Plants under low nitrogen availability seem to increase their sensitivity to inductive conditions (Strik 1985; Battey et al. 1998; Lieten 2002). They can initiate flower buds after a few

12 1032 CANADIAN JOURNAL OF PLANT SCIENCE Fig. 12. Time sequence of plant architecture of Gariguette in relation to nutrient supply technique. (A) Under continuous fertigation and (B) with suspension of nutrition (modified from Savini 2003). Capital letters represent progressive stages of flower bud development, according to the primary flower, from A primary flower primordium to H formed primary flower with yellow anthers. days of induction treatment, but very low nutrient supply during flower induction and differentiation could cause the meristem to revert from reproductive to vegetative growth (van den Muijzenberg 1942). The plants could also reduce the number of flowers and the inflorescence size, apparently because of initiation failures (Anderson and Guttridge 1982). Too little nitrogen during flower differentiation until mid-october prevents the further development of initiated flowers that cannot produce fruits, even with high nutrient conditions during the other growth phases of the plant. Reduction after mid-october does not affect fruit production. With reduced nutrition at the end of summer until mid-september, crowns do not become big, but floral initiation is favored and fruit numbers can increase, with more quaternary and quinary flowers on first and second truss (inflorescence) and more secondary and tertiary flowers on second and third truss (Lieten 2002). If the nutritional deficiency persists after induction, it may affect the regular formation of the flower and inflorescence (Strik 1985; Battey et al. 1998; Lieten 2002), and reduce the yield potential of the plant. Nutrients applied at the beginning of inductive thermo-photoperiod conditions (Sønsteby et al. 2009) delay flower bud initiation more than delayed application (Yamasaki and Yano 2009). Temporary suspension of fertigation during flower induction of tray-plants advances the differentiation of terminal flower bud with positive effects on inflorescence development and flower number (Savini 2003), while continuous high nutrition delays flower initiation and may induce some defects in primary berries (Yoshida 1992; Lieten 2002). Malformed fruits are reduced if high nitrogen supply is delayed after sepal differentiation. After flower bud initiation, the differentiation of the floral organs requires more nitrogen (Yamasaki et al. 2002). Starting nutrient application after September can strongly reduce crown size. In the nursery, early reduced nitrogen application (7.5 kg N ha 1 ) followed by increased supply (double the amount) at the end of August or in September and decreased nitrogen application in October may advance flower initiation in comparison with low, or high, constant nitrogen supply from the beginning of August (Desmet et al. 2009). The source of nutritional factors can also interact with plant growth; the addition of organic matter (cattle, poultry, sheep or manure) stimulates production of leaves and accelerates flowering date compared with conventional fertilizer (Abu-Zahra and Tahboub 2008). Finally, all this evidence suggests that the nutritional status should be carefully modified in relation to climate change to develop an efficient strategy for plant propagation and to better program strawberry production. WATER SUPPLY Different water regimes have no effects on the duration of fruit production (Dwyer et al. 1987; Serrano et al. 1992). However, sufficient water supply is essential for an acceptable yield, but water stress after the beginning of flowering may allow flower induction, even under unfavorable environmental conditions (Naumann 1961). This is particularly important during bud differentiation and flower and fruit development. Higher yield can be obtained by providing a better water supply during flower bud initiation and differentiation, e.g., autumn compared with spring irrigation (Naumann 1964). Water deficits ( 0.03, 0.05 and 0.07 MPa) can reduce fruit production due to decreased mean fruit weight and diminished fruit number (Davies and Albrigo 1983; Gehrmann 1985; Pen uelas et al. 1992; Serrano et al. 1992). This may be related to the fact that branch crown development is dependent on water supply and is inhibited under strongly reduced water