- Email: [email protected]
Timing of fruit removal affects concurrent vegetative growth and subsequent return bloom and yield in olive (Olea europaea L.)
Scientia Horticulturae 123 (2010) 469–472
Contents lists available at ScienceDirect
Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti
Timing of fruit removal affects concurrent vegetative growth and subsequent return bloom and yield in olive (Olea europaea L.) Arnon Dag a,*, Amnon Bustan a, Avishai Avni a,b, Isaac Tzipori a, Shimon Lavee b, Joseph Riov b a
Gilat Research Centre, Agricultural Research Organization, Ministry of Agriculture, Mobile Post Negev 85280, Israel The Kennedy-Leigh Centre for Horticultural Research, The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot 76100, Israel
b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 19 April 2009 Received in revised form 11 October 2009 Accepted 23 November 2009
Olive (Olea europaea) demonstrates a high tendency toward alternate fruit production, with significant negative consequences on the industry. Fruit load is one of the main cause-and-effect factors in the phenomenon of biennial bearing, often disrupting the balance between reproductive and vegetative processes. The objectives of the present study were to identify the time range during which heavy fruit load reversibly interrupts the reproductive processes of the following year. The linkage between timing of fruit removal, vegetative growth, return bloom, and fruit yield was studied. Complete fruit removal in cv. Coratina until about 120 days after full bloom (August 15) caused an immediate resumption of vegetative growth. The new shoots grew to twice the length of those on trees that underwent later fruit removal. Moreover, a full return bloom, corresponding with high subsequent yields, was obtained by early fruit removal, while poor or no bloom developed on late-defruited or control trees. Thus, the critical time to affect flowering and subsequent fruiting in the following year by fruit thinning occurs in olive trees even weeks after pit hardening—much later than previously suggested. Furthermore, the data indicate that flowering-site limitation, due to insufficient or immature vegetative growth during the Onyear, is a primary factor inducing alternate bearing in olive. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Alternate bearing Floral induction Fruit load Fruit thinning
1. Introduction Olive (Olea europaea L.) exhibits a high tendency toward alternate fruit production. Being an industry-dependent commodity, the economic impact of biennial bearing, particularly in oil olives, is highly significant (Lavee, 2006). Alternate bearing is intimately related to the basic processes of fruiting, such as flower bud differentiation, fruit set and abscission, and fruit growth (Goldschmidt, 2005). In olive, as in many other fruit trees that display biennial bearing, the syndrome is first expressed by the intensity of the bloom; there is hardly any flowering following a heavily cropped On-year, and conversely—an Off-year is tailed by profuse flowering (Monselise and Goldschmidt, 1982; Lavee, 1996; Goldschmidt, 2005). Thus, research into alternate bearing in this species should focus on the early phases of the reproductive process. Olive fruits develop on inflorescences arising from buds borne on shoots grown in the previous year (Lavee, 1996). Sanz-Corte´s et al. (2002) suggested that floral induction occurs in the summer, 7–
* Corresponding author at: Gilat Research Centre, Agricultural Research Organization, Ministry of Agriculture, Mobile Post Negev 85280, Israel. Tel.: +972 8 9928630; fax: +972 8 9926485. E-mail address: [email protected] (A. Dag). 0304-4238/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.scienta.2009.11.014
8 weeks after full bloom, at about the time of pit hardening (endocarp sclerification) in the concurrent season’s fruit. Indeed, a more recent work (Andreini et al., 2008) could already distinguish between On and Off axillary buds in July, close to pit hardening. At that time, accumulation of the cytokinin zeatin was observed only in meristems of Off axillary buds together with a strong RNA signal, both considered early indicators of floral initiation. Nevertheless, olive shoots often grow throughout the summer, so that the buds developing in the leaf axils along the shoot are of diverse ages, some emerging after pit hardening. Nevertheless, all of the buds on well-lignified parts of the shoot can potentially differentiate to form inflorescences (Lavee, 2006). Floral bud development in olive is governed by plant growth substances and various secondary metabolites delivered from other plant organs (Badr et al., 1970; Ferna´ndez-Escobar et al., 1992; Lavee, 1996; Fabbri and Benelli, 2000; Baktir et al., 2004; Ulger et al., 2004), and is also strongly affected by winter temperature regime (Martin, 1989; Rallo and Martin, 1991; Rallo et al., 1994; Lavee, 1996; Orlandi et al., 2004). Cuevas et al. (1994) showed that heavy fruit load impairs the floral quality of the following bloom, presumably through incomplete bud differentiation. Experiments involving deliberate seed abortion (Stutte and Martin, 1986) or removal of young developing fruit (Ryan et al., 2003) demonstrated the negative influence of
470
A. Dag et al. / Scientia Horticulturae 123 (2010) 469–472
phenolic compounds induced by the developing seed or fruit on floral bud differentiation. A high positive correlation was shown between fruit load and the level of chlorogenic acid in the leaves in mid-summer. Injection of chlorogenic acid into scaffolds during winter, but not in the following early spring (Lavee et al., 1986), reduced flower bud differentiation by more than 50% (Lavee, 2006). This bulk of evidence suggests that the concurrent developing fruit directly inhibits the metabolism leading to reproductive induction and differentiation of the buds for the potential yield in the following year. Adequate development of new shoots is essential for the successive reproductive process, as these serve as the platform for new buds. As a consequence of heavy fruit load, the vegetative growth of olive trees tends to be slow and fleeting, whereas under a light crop it is vigorous throughout the season (Connor and Fereres, 2005; Lavee, 2006). Thus, the vicious circle of biennial bearing is undoubtedly the consequence of an imbalance between the vegetative and reproductive phases of the tree. The balance between these two phases may often be interrupted by environmental factors, such as unfulfilled winter chilling requirements (Rallo and Martin, 1991; Rallo et al., 1994) or spring heat waves (Lavee, 2006), which radically reduce fruit load, thereby triggering the circle by inducing an Off-year. Once initiated, the main method of breaking biennial bearing is On-year fruit thinning (Dag et al., 2009). Strong interactions between developing fruit, shoot vigor, and the induction and differentiation of floral buds have been described in olive trees with regard to biennial bearing (Lavee, 2006). However, better resolution of the time course of the processes involved, and particularly the identification of points of no return in the subsequent reproductive development, is still needed. In the present study, complete fruit removal at different times during the season was employed to identify the critical time at which heavy fruit load prevents reproductive development in the following year, and to study the linkage between fruit removal, vegetative growth, return bloom, and fruit yield in olive trees during the season, in the context of biennial bearing. 2. Materials and methods 2.1. Experimental site and design The experiment was conducted in a commercial olive (cv. Coratina) orchard planted in 2002 (at 7.0 m 3.5 m spacing) in an arid area near Kibbutz Revivim in the Negev highland desert of Israel. The mean annual precipitation is <100 mm between November and February and it is unpredictable; the orchards are drip-irrigated throughout the year to reach a total of 900 mm. Fertilizers are supplied continuously through the irrigation water at 200, 30, and 300 kg ha 1 year 1 of N, P and K, respectively. Forty-eight uniform heavily producing trees were selected and tagged on June 6, 2006, after the final fruit load had been determined. The trees were randomly assigned to the different treatments, six trees (replicates) per treatment (date of fruit removal). Accordingly, all fruits were manually removed from the trees on June 6, July 12, August 15, October 17, November 8, and December 6, 2006 (days of year [DOY]: 157, 193, 227, 290, 312, and 346, respectively), and January 11, 2007 (DOY: 11). The eighth treatment consisted of trees whose fruits were not removed, serving as a control.
length, and branching) were followed once a month. Sunlight interception by the canopy was quantified during the noon hour of a clear day in the following spring (March 12, 2007), using an AccuPAR PAR/LAI Ceptometer, Model LP-80 (Decagon Devices). Each tree was measured once, with the device located horizontally at the center of the tree, about 0.4 m above the ground, where the trunk splits to main branches Each measurement inside the canopy was preceded by an above-canopy one. All measurements were normalized to the mean light interception of the 6 control trees thus determining the relative canopy density (RCD). The intensity of the return bloom was evaluated on April 15, 2007, using a blind test in which two external surveyors independently ranked each experimental tree from 0 (no bloom) to 5 (heavy bloom). The subsequent year’s fruits were harvested from individual trees on November 4–6, 2007 onto nets using mechanical combs, gathered, and weighed. A sample of 100 fruits was taken from each tree to determine the average fruit weight, and number of fruits per tree was calculated. Data were analyzed using JMP 7.0 software (SAS Institute). Effect of treatments on yield parameters and RCD were analyzed using a one-way ANOVA model (Tukey–Kramer multiple comparisons test). 3. Results and discussion Developing olive fruit has been reported to have a marked negative effect on the subsequent developmental processes that are required for flowering in the following year (Lavee et al., 1986; Stutte and Martin, 1986; Cuevas et al., 1994; Ryan et al., 2003; Lavee, 2006). Most previous studies have dealt mainly with floral bud induction and differentiation. Evidently, however, the number of new shoots developing in a year during the growing season, and particularly the number of new internodes, determine the number of available buds for floral induction. The number of such buds is the primary determinant of reproductive capacity in the following year. In the present study, complete manual fruit removal was applied once a month during the season in young ‘Coratina’ trees. The effect of fruit removal on the shoot growth was significant: until about 120 days after full bloom (DAFB) (late August), the earlier the fruit was removed, the more vigorous the shoot growth (Fig. 1). The heavy fruit load significantly suppressed shoot growth: as soon as this restraint was lifted by fruit removal, vegetative
2.2. Measurements On June 6, 2006, four representative shoots per tree, two on each side of the rows, were tagged 15 cm from the tip on all experimental trees, and their growth parameters (shoot elongation, internode
Fig. 1. Effect of manual fruit removal on different dates after full bloom during an Onyear, starting on June 6, 2006 (50 days after full bloom), on shoot elongation of olive trees (cv. Coratina). Values are means of 24 shoots (four per tree). Bars indicate SE.
A. Dag et al. / Scientia Horticulturae 123 (2010) 469–472
Fig. 2. Effect of manual fruit removal at different times after full bloom in an On-year, starting on June 6, 2006 (50 days after full bloom—DAFB), on the relative canopy density (RCD) of olive trees (cv. Coratina) in the following spring (March 12, 2007). Values are means of six trees. Bars indicate SE. Means headed by different letters are significantly different at P 0.05 (Tukey–Kramer multiple comparisons test).
growth resumed, resulting in approximately twice the shootelongation increment compared to trees defruited later in the season. In all treatments, shoot growth almost ceased at about 180 DAFB. After that time, fruit removal was too late to enable significant reinduction of vegetative growth. Relative canopy density (RCD) values measured in the following spring, prior to bloom (Fig. 2) closely correlated with the shoot growth measurements during the season, confirming the overall influence of fruit removal on the vegetative growth. Although renewed vegetative growth following fruit thinning (Ferna´ndez-Escobar et al., 1992) or embryo killing (Stutte and Martin, 1986) has been demonstrated, the effectiveness of reducing fruit number on vegetative growth was limited to the period until pit hardening, less than 2 months after full bloom. Our data show that the negative impact of fruit load on concurrent vegetative growth can be reversed considerably later by fruit removal, up to 4 months after full bloom (Fig. 1). Since no significant influence has been observed on the length of the new internodes (data not shown), it is presumed that the measured shoot elongation has brought about to a significant increment in the number of internodes, and most likely—in the number of new buds per tree. Thus we show here, that the potential for flowering and fruiting in the following year can be completely restored when fruit in the On-year is removed, up to 120 DAFB. It is difficult to distinguish between the inhibitory effect of developing fruit on vegetative growth and their direct influence on floral bud initiation and development. Several authors have suggested that flower bud induction occurs in early July, 7–8 weeks after full bloom, at around the time of pit hardening (SanzCorte´s et al., 2002; Andreini et al., 2008). In the present study, fruitlet removal until 120 DAFB provided high blooming scores in the subsequent spring; however, fruit removal at any later date had only a minor effect on the flowering rates, which were nevertheless significantly higher than the null bloom of the control trees (Fig. 3). These results demonstrate clearly that the buds on the newly developing shoots (induced to grow by fruit removal up to 120 DAFB) had the capacity to differentiate, 1 or 2 months later than assumed before. Thus, consideration should be given to the relationship between flower bud induction and the developmental stage of the shoots bearing the buds and that of the buds themselves. Shoot growth and development is a prolonged process hence the population of new axillary buds on a tree at any given time is rather
471
Fig. 3. Effect of manual fruit removal at different times after full bloom in an Onyear, starting on June 6, 2006 (50 days after full bloom—DAFB), on the following bloom of olive trees (cv. Coratina), ranked (0—no bloom to 5—heavy bloom) on April 15, 2007. Values are means of six trees SE.
heterogeneous with respect to their responsiveness to inducive or inhibitory effects. It follows that floral induction of the whole population of new buds is likely to be scattered throughout the season, even though this is considered a finite event for the individual bud (Lavee, 2006). The bud population is subject to various regulatory effects, among which may be age, location, and vicinity of an individual bud to developing fruit. As a rule, the earlier the fruit removal the more new buds are released from the inhibitory influence. Nevertheless, a fair amount of buds remain responsive to inducive factors and may differentiate even if fruit removal takes place relatively late (Fig. 3). It could therefore be concluded that alternate bearing is controlled indirectly by the number of buds, but also directly by the readiness of each individual bud to differentiate at a given time. It is also possible that a second notable period of induction, which may restore or strengthen the effect of earlier ones, occurs during the autumn (Troncoso et al., 2010). Adequate number of responsive buds and their subsequent differentiation are indeed prerequisites but they cannot guarantee fruit yield. In our study, the fruit yields corresponded to the extent of the bloom: high yields (>50 kg tree 1) were obtained in trees that had undergone fruit removal until 120 DAFB in the previous season (Table 1). In contrast, fruit removal after this time gave rise to much lower yield levels (7–13 kg tree 1). It should be noted that even extremely late (January 11, 2007) fruit removal brought about a slight increase in flowering and subsequent (though negligible) fruit production, whereas no fruit was obtained in the control trees (no fruit removal at all). The difference in fruit load between the
Table 1 Effect of timing of fruit removal (in brackets: day of year) in cv. Coratina on fruityield parameters in the following year. Date of fruit removal June 6, 2006 (157) July 12, 2006 (193) August 15, 2006 (227) October 17, 2006 (290) November 8, 2006 (312) December 6, 2006 (346) January 11, 2007 (11) Control
Fruit load (fruit tree 1)
Fresh fruit weight (g fruit
23,853a 24,407a 21,352a 2876b 2755b 1743b 148c 0d
2.34b 2.40b 2.61b 4.39a 3.93a 4.05a 3.24ab –
1
)
Yield (kg tree
1
)
55.8a 58.7a 55.8a 12.6b 10.8b 7.1b 0.5c 0.0d
Within each column data followed by different letters are significantly different according to the Tukey–Kramer multiple comparison test (P < 0.05).
472
A. Dag et al. / Scientia Horticulturae 123 (2010) 469–472
two groups (fruit removal before and after 120 DAFB) had a clear effect on fruit size, which was significantly smaller in the early defruited, high-yielding trees (Table 1). To conclude, the requisite existence of new, mature and therefore responsive buds seems to be the main factor determining the return bloom and yield in the following year. Therefore, flowering-site limitation, which was suggested by Goldschmidt (2005) as one of the three major reasons for alternate bearing in fruit trees, appears to be most relevant in olive. The developing fruits appear to predominantly affect vegetative growth, limiting it during the On-year. The practical consequences of the present study are still unclear. The commercial harvest of oil olives usually takes place not earlier than mid-October, too late for the essential resumption of new vegetative growth. Table olives, in contrast, are usually harvested earlier, from the beginning of September and indeed, their tendency toward alternate bearing is generally smaller and often correlates with time of harvest (Lavee, 1996). Our results indicate that the opportunity to influence biennial bearing by fruit thinning in olives is viable until at least 120 DAFB, much later than previously estimated. Acknowledgement Our thanks are due to Halutza olive farm for providing their orchard for this study. References Andreini, L., Bartolini, S., Guivarc’h, A., Chriqui, D., Vitagliano, C., 2008. Histological and immunohistochemical studies on flower induction in the olive tree (Olea europaea L.). Plant Biol. 10, 588–595. Badr, S.A., Hartmann, H.T., Martin, G.C., 1970. Endogenous gibberellins and inhibitors in relation to flower induction and inflorescence development in the olive. Plant Physiol. 46, 674–679. Baktir, I., Ulger, S., Himelrick, D.G., 2004. Relationship of seasonal changes in endogenous plant hormones and alternate bearing of olive trees. HortScience 39, 987–990.
Connor, D.J., Fereres, E., 2005. The physiology and adaptation of yield expression in olive. Hort. Rev. 31, 155–229. Cuevas, J., Rallo, L., Rapoport, H.F., 1994. Crop load effects on floral quality in olive. Sci. Hortic. 59, 123–130. Dag, A., Bustan, A., Avni, A., Lavee, S., Riov, J., 2009. Fruit thinning using NAA shows potential for reducing biennial bearing of ‘Barnea’ and ‘Picual’ oil olive trees. Crop & Pasture Science 60, 1124–1130. Fabbri, A., Benelli, C., 2000. Flower bud induction and differentiation in olive. J. Hort. Sci. Biotechnol. 75, 131–141. Ferna´ndez-Escobar, R., Benlloch, M., Navarro, C., Martin, G.C., 1992. The time of floral induction in olive. J. Am. Soc. Hort. Sci. 117, 304–307. Goldschmidt, E.E., 2005. Regulatory aspects of alternate bearing in fruit trees. Italus Hortus 12, 11–17 (in Italian). Lavee, S., 1996. Biology and physiology of the olive. In: Blazquez, J.M. (Ed.), World Olive Encyclopaedia. Plaza and Janes SA, Barcelona, Spain, pp. 61–105. Lavee, S., 2006. Biennial bearing in olive (Olea europaea L.). Olea FAO Olive Network 25, 5–13. Lavee, S., Harshemesh, H., Avidan, N., 1986. Phenolic acids—possible involvement in regulating growth and alternate fruiting in olive trees. Acta Hortic. 179, 317–328. Martin, G.C., 1989. Olive flower and fruit population dynamics. Acta Hortic. 286, 141–146. Monselise, P.S., Goldschmidt, E.E., 1982. Alternate bearing in fruit trees. Hort. Rev. 4, 128–173. Orlandi, F., Garcia-Mozo, H., Vazquez-Ezquerra, L., Romano, B., Dominguez, E., Galan, C., Fornaciari, M., 2004. Phenological olive chilling requirements in Umbria (Italy) and Andalusia (Spain). Plant Biosys. 138, 111–116. Rallo, L., Martin, G.C., 1991. The role of chilling in releasing olive floral buds from dormancy. J. Am. Soc. Hort. Sci. 116, 1058–1062. Rallo, L., Torreno, P., Vargas, J.A., Alvarado, J., 1994. Dormany and alternate bearing in olive. Acta Hortic. 356, 127–136. Ryan, D., Prenzler, P.D., Lavee, S., Antolovich, M., Robards, K., 2003. Quantitative changes in phenolic content during physiological development of the olive (Olea europaea) cultivar Hardy’s Mammoth. Int. J. Food Chem. 51, 2532–2538. Sanz-Corte´s, F., Martı´nez-Calvo, J., Badenes, M.L., Bleiholder, H., Hack, H., Llacer, G., Meier, U., 2002. Phenological growth stages of olive trees (Olea europaea). Ann. Appl. Biol. 140, 151–157. Stutte, G.W., Martin, G.C., 1986. Effect of killing the seed on return to bloom of olive. Sci. Hortic. 29, 107–113. Troncoso, A., Garcia, J.L., Lavee, S., 2010. Evaluation of the present information on the mechanisms leading to flower bud induction, evocation and differentiation. Acta Hortic., in press. Ulger, S., Sonmez, S., Karkacier, M., Ertoy, N., Akdesir, O., Aksu, M., 2004. Determination of endogenous hormones, sugars and mineral nutrition levels during the induction, initiation and differentiation stage and their effects on flower formation in olive. Plant Growth Reg. 42, 89–95.
Contents lists available at ScienceDirect
Scientia Horticulturae journal homepage: www.elsevier.com/locate/scihorti
Timing of fruit removal affects concurrent vegetative growth and subsequent return bloom and yield in olive (Olea europaea L.) Arnon Dag a,*, Amnon Bustan a, Avishai Avni a,b, Isaac Tzipori a, Shimon Lavee b, Joseph Riov b a
Gilat Research Centre, Agricultural Research Organization, Ministry of Agriculture, Mobile Post Negev 85280, Israel The Kennedy-Leigh Centre for Horticultural Research, The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, Rehovot 76100, Israel
b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 19 April 2009 Received in revised form 11 October 2009 Accepted 23 November 2009
Olive (Olea europaea) demonstrates a high tendency toward alternate fruit production, with significant negative consequences on the industry. Fruit load is one of the main cause-and-effect factors in the phenomenon of biennial bearing, often disrupting the balance between reproductive and vegetative processes. The objectives of the present study were to identify the time range during which heavy fruit load reversibly interrupts the reproductive processes of the following year. The linkage between timing of fruit removal, vegetative growth, return bloom, and fruit yield was studied. Complete fruit removal in cv. Coratina until about 120 days after full bloom (August 15) caused an immediate resumption of vegetative growth. The new shoots grew to twice the length of those on trees that underwent later fruit removal. Moreover, a full return bloom, corresponding with high subsequent yields, was obtained by early fruit removal, while poor or no bloom developed on late-defruited or control trees. Thus, the critical time to affect flowering and subsequent fruiting in the following year by fruit thinning occurs in olive trees even weeks after pit hardening—much later than previously suggested. Furthermore, the data indicate that flowering-site limitation, due to insufficient or immature vegetative growth during the Onyear, is a primary factor inducing alternate bearing in olive. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Alternate bearing Floral induction Fruit load Fruit thinning
1. Introduction Olive (Olea europaea L.) exhibits a high tendency toward alternate fruit production. Being an industry-dependent commodity, the economic impact of biennial bearing, particularly in oil olives, is highly significant (Lavee, 2006). Alternate bearing is intimately related to the basic processes of fruiting, such as flower bud differentiation, fruit set and abscission, and fruit growth (Goldschmidt, 2005). In olive, as in many other fruit trees that display biennial bearing, the syndrome is first expressed by the intensity of the bloom; there is hardly any flowering following a heavily cropped On-year, and conversely—an Off-year is tailed by profuse flowering (Monselise and Goldschmidt, 1982; Lavee, 1996; Goldschmidt, 2005). Thus, research into alternate bearing in this species should focus on the early phases of the reproductive process. Olive fruits develop on inflorescences arising from buds borne on shoots grown in the previous year (Lavee, 1996). Sanz-Corte´s et al. (2002) suggested that floral induction occurs in the summer, 7–
* Corresponding author at: Gilat Research Centre, Agricultural Research Organization, Ministry of Agriculture, Mobile Post Negev 85280, Israel. Tel.: +972 8 9928630; fax: +972 8 9926485. E-mail address: [email protected] (A. Dag). 0304-4238/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.scienta.2009.11.014
8 weeks after full bloom, at about the time of pit hardening (endocarp sclerification) in the concurrent season’s fruit. Indeed, a more recent work (Andreini et al., 2008) could already distinguish between On and Off axillary buds in July, close to pit hardening. At that time, accumulation of the cytokinin zeatin was observed only in meristems of Off axillary buds together with a strong RNA signal, both considered early indicators of floral initiation. Nevertheless, olive shoots often grow throughout the summer, so that the buds developing in the leaf axils along the shoot are of diverse ages, some emerging after pit hardening. Nevertheless, all of the buds on well-lignified parts of the shoot can potentially differentiate to form inflorescences (Lavee, 2006). Floral bud development in olive is governed by plant growth substances and various secondary metabolites delivered from other plant organs (Badr et al., 1970; Ferna´ndez-Escobar et al., 1992; Lavee, 1996; Fabbri and Benelli, 2000; Baktir et al., 2004; Ulger et al., 2004), and is also strongly affected by winter temperature regime (Martin, 1989; Rallo and Martin, 1991; Rallo et al., 1994; Lavee, 1996; Orlandi et al., 2004). Cuevas et al. (1994) showed that heavy fruit load impairs the floral quality of the following bloom, presumably through incomplete bud differentiation. Experiments involving deliberate seed abortion (Stutte and Martin, 1986) or removal of young developing fruit (Ryan et al., 2003) demonstrated the negative influence of
470
A. Dag et al. / Scientia Horticulturae 123 (2010) 469–472
phenolic compounds induced by the developing seed or fruit on floral bud differentiation. A high positive correlation was shown between fruit load and the level of chlorogenic acid in the leaves in mid-summer. Injection of chlorogenic acid into scaffolds during winter, but not in the following early spring (Lavee et al., 1986), reduced flower bud differentiation by more than 50% (Lavee, 2006). This bulk of evidence suggests that the concurrent developing fruit directly inhibits the metabolism leading to reproductive induction and differentiation of the buds for the potential yield in the following year. Adequate development of new shoots is essential for the successive reproductive process, as these serve as the platform for new buds. As a consequence of heavy fruit load, the vegetative growth of olive trees tends to be slow and fleeting, whereas under a light crop it is vigorous throughout the season (Connor and Fereres, 2005; Lavee, 2006). Thus, the vicious circle of biennial bearing is undoubtedly the consequence of an imbalance between the vegetative and reproductive phases of the tree. The balance between these two phases may often be interrupted by environmental factors, such as unfulfilled winter chilling requirements (Rallo and Martin, 1991; Rallo et al., 1994) or spring heat waves (Lavee, 2006), which radically reduce fruit load, thereby triggering the circle by inducing an Off-year. Once initiated, the main method of breaking biennial bearing is On-year fruit thinning (Dag et al., 2009). Strong interactions between developing fruit, shoot vigor, and the induction and differentiation of floral buds have been described in olive trees with regard to biennial bearing (Lavee, 2006). However, better resolution of the time course of the processes involved, and particularly the identification of points of no return in the subsequent reproductive development, is still needed. In the present study, complete fruit removal at different times during the season was employed to identify the critical time at which heavy fruit load prevents reproductive development in the following year, and to study the linkage between fruit removal, vegetative growth, return bloom, and fruit yield in olive trees during the season, in the context of biennial bearing. 2. Materials and methods 2.1. Experimental site and design The experiment was conducted in a commercial olive (cv. Coratina) orchard planted in 2002 (at 7.0 m 3.5 m spacing) in an arid area near Kibbutz Revivim in the Negev highland desert of Israel. The mean annual precipitation is <100 mm between November and February and it is unpredictable; the orchards are drip-irrigated throughout the year to reach a total of 900 mm. Fertilizers are supplied continuously through the irrigation water at 200, 30, and 300 kg ha 1 year 1 of N, P and K, respectively. Forty-eight uniform heavily producing trees were selected and tagged on June 6, 2006, after the final fruit load had been determined. The trees were randomly assigned to the different treatments, six trees (replicates) per treatment (date of fruit removal). Accordingly, all fruits were manually removed from the trees on June 6, July 12, August 15, October 17, November 8, and December 6, 2006 (days of year [DOY]: 157, 193, 227, 290, 312, and 346, respectively), and January 11, 2007 (DOY: 11). The eighth treatment consisted of trees whose fruits were not removed, serving as a control.
length, and branching) were followed once a month. Sunlight interception by the canopy was quantified during the noon hour of a clear day in the following spring (March 12, 2007), using an AccuPAR PAR/LAI Ceptometer, Model LP-80 (Decagon Devices). Each tree was measured once, with the device located horizontally at the center of the tree, about 0.4 m above the ground, where the trunk splits to main branches Each measurement inside the canopy was preceded by an above-canopy one. All measurements were normalized to the mean light interception of the 6 control trees thus determining the relative canopy density (RCD). The intensity of the return bloom was evaluated on April 15, 2007, using a blind test in which two external surveyors independently ranked each experimental tree from 0 (no bloom) to 5 (heavy bloom). The subsequent year’s fruits were harvested from individual trees on November 4–6, 2007 onto nets using mechanical combs, gathered, and weighed. A sample of 100 fruits was taken from each tree to determine the average fruit weight, and number of fruits per tree was calculated. Data were analyzed using JMP 7.0 software (SAS Institute). Effect of treatments on yield parameters and RCD were analyzed using a one-way ANOVA model (Tukey–Kramer multiple comparisons test). 3. Results and discussion Developing olive fruit has been reported to have a marked negative effect on the subsequent developmental processes that are required for flowering in the following year (Lavee et al., 1986; Stutte and Martin, 1986; Cuevas et al., 1994; Ryan et al., 2003; Lavee, 2006). Most previous studies have dealt mainly with floral bud induction and differentiation. Evidently, however, the number of new shoots developing in a year during the growing season, and particularly the number of new internodes, determine the number of available buds for floral induction. The number of such buds is the primary determinant of reproductive capacity in the following year. In the present study, complete manual fruit removal was applied once a month during the season in young ‘Coratina’ trees. The effect of fruit removal on the shoot growth was significant: until about 120 days after full bloom (DAFB) (late August), the earlier the fruit was removed, the more vigorous the shoot growth (Fig. 1). The heavy fruit load significantly suppressed shoot growth: as soon as this restraint was lifted by fruit removal, vegetative
2.2. Measurements On June 6, 2006, four representative shoots per tree, two on each side of the rows, were tagged 15 cm from the tip on all experimental trees, and their growth parameters (shoot elongation, internode
Fig. 1. Effect of manual fruit removal on different dates after full bloom during an Onyear, starting on June 6, 2006 (50 days after full bloom), on shoot elongation of olive trees (cv. Coratina). Values are means of 24 shoots (four per tree). Bars indicate SE.
A. Dag et al. / Scientia Horticulturae 123 (2010) 469–472
Fig. 2. Effect of manual fruit removal at different times after full bloom in an On-year, starting on June 6, 2006 (50 days after full bloom—DAFB), on the relative canopy density (RCD) of olive trees (cv. Coratina) in the following spring (March 12, 2007). Values are means of six trees. Bars indicate SE. Means headed by different letters are significantly different at P 0.05 (Tukey–Kramer multiple comparisons test).
growth resumed, resulting in approximately twice the shootelongation increment compared to trees defruited later in the season. In all treatments, shoot growth almost ceased at about 180 DAFB. After that time, fruit removal was too late to enable significant reinduction of vegetative growth. Relative canopy density (RCD) values measured in the following spring, prior to bloom (Fig. 2) closely correlated with the shoot growth measurements during the season, confirming the overall influence of fruit removal on the vegetative growth. Although renewed vegetative growth following fruit thinning (Ferna´ndez-Escobar et al., 1992) or embryo killing (Stutte and Martin, 1986) has been demonstrated, the effectiveness of reducing fruit number on vegetative growth was limited to the period until pit hardening, less than 2 months after full bloom. Our data show that the negative impact of fruit load on concurrent vegetative growth can be reversed considerably later by fruit removal, up to 4 months after full bloom (Fig. 1). Since no significant influence has been observed on the length of the new internodes (data not shown), it is presumed that the measured shoot elongation has brought about to a significant increment in the number of internodes, and most likely—in the number of new buds per tree. Thus we show here, that the potential for flowering and fruiting in the following year can be completely restored when fruit in the On-year is removed, up to 120 DAFB. It is difficult to distinguish between the inhibitory effect of developing fruit on vegetative growth and their direct influence on floral bud initiation and development. Several authors have suggested that flower bud induction occurs in early July, 7–8 weeks after full bloom, at around the time of pit hardening (SanzCorte´s et al., 2002; Andreini et al., 2008). In the present study, fruitlet removal until 120 DAFB provided high blooming scores in the subsequent spring; however, fruit removal at any later date had only a minor effect on the flowering rates, which were nevertheless significantly higher than the null bloom of the control trees (Fig. 3). These results demonstrate clearly that the buds on the newly developing shoots (induced to grow by fruit removal up to 120 DAFB) had the capacity to differentiate, 1 or 2 months later than assumed before. Thus, consideration should be given to the relationship between flower bud induction and the developmental stage of the shoots bearing the buds and that of the buds themselves. Shoot growth and development is a prolonged process hence the population of new axillary buds on a tree at any given time is rather
471
Fig. 3. Effect of manual fruit removal at different times after full bloom in an Onyear, starting on June 6, 2006 (50 days after full bloom—DAFB), on the following bloom of olive trees (cv. Coratina), ranked (0—no bloom to 5—heavy bloom) on April 15, 2007. Values are means of six trees SE.
heterogeneous with respect to their responsiveness to inducive or inhibitory effects. It follows that floral induction of the whole population of new buds is likely to be scattered throughout the season, even though this is considered a finite event for the individual bud (Lavee, 2006). The bud population is subject to various regulatory effects, among which may be age, location, and vicinity of an individual bud to developing fruit. As a rule, the earlier the fruit removal the more new buds are released from the inhibitory influence. Nevertheless, a fair amount of buds remain responsive to inducive factors and may differentiate even if fruit removal takes place relatively late (Fig. 3). It could therefore be concluded that alternate bearing is controlled indirectly by the number of buds, but also directly by the readiness of each individual bud to differentiate at a given time. It is also possible that a second notable period of induction, which may restore or strengthen the effect of earlier ones, occurs during the autumn (Troncoso et al., 2010). Adequate number of responsive buds and their subsequent differentiation are indeed prerequisites but they cannot guarantee fruit yield. In our study, the fruit yields corresponded to the extent of the bloom: high yields (>50 kg tree 1) were obtained in trees that had undergone fruit removal until 120 DAFB in the previous season (Table 1). In contrast, fruit removal after this time gave rise to much lower yield levels (7–13 kg tree 1). It should be noted that even extremely late (January 11, 2007) fruit removal brought about a slight increase in flowering and subsequent (though negligible) fruit production, whereas no fruit was obtained in the control trees (no fruit removal at all). The difference in fruit load between the
Table 1 Effect of timing of fruit removal (in brackets: day of year) in cv. Coratina on fruityield parameters in the following year. Date of fruit removal June 6, 2006 (157) July 12, 2006 (193) August 15, 2006 (227) October 17, 2006 (290) November 8, 2006 (312) December 6, 2006 (346) January 11, 2007 (11) Control
Fruit load (fruit tree 1)
Fresh fruit weight (g fruit
23,853a 24,407a 21,352a 2876b 2755b 1743b 148c 0d
2.34b 2.40b 2.61b 4.39a 3.93a 4.05a 3.24ab –
1
)
Yield (kg tree
1
)
55.8a 58.7a 55.8a 12.6b 10.8b 7.1b 0.5c 0.0d
Within each column data followed by different letters are significantly different according to the Tukey–Kramer multiple comparison test (P < 0.05).
472
A. Dag et al. / Scientia Horticulturae 123 (2010) 469–472
two groups (fruit removal before and after 120 DAFB) had a clear effect on fruit size, which was significantly smaller in the early defruited, high-yielding trees (Table 1). To conclude, the requisite existence of new, mature and therefore responsive buds seems to be the main factor determining the return bloom and yield in the following year. Therefore, flowering-site limitation, which was suggested by Goldschmidt (2005) as one of the three major reasons for alternate bearing in fruit trees, appears to be most relevant in olive. The developing fruits appear to predominantly affect vegetative growth, limiting it during the On-year. The practical consequences of the present study are still unclear. The commercial harvest of oil olives usually takes place not earlier than mid-October, too late for the essential resumption of new vegetative growth. Table olives, in contrast, are usually harvested earlier, from the beginning of September and indeed, their tendency toward alternate bearing is generally smaller and often correlates with time of harvest (Lavee, 1996). Our results indicate that the opportunity to influence biennial bearing by fruit thinning in olives is viable until at least 120 DAFB, much later than previously estimated. Acknowledgement Our thanks are due to Halutza olive farm for providing their orchard for this study. References Andreini, L., Bartolini, S., Guivarc’h, A., Chriqui, D., Vitagliano, C., 2008. Histological and immunohistochemical studies on flower induction in the olive tree (Olea europaea L.). Plant Biol. 10, 588–595. Badr, S.A., Hartmann, H.T., Martin, G.C., 1970. Endogenous gibberellins and inhibitors in relation to flower induction and inflorescence development in the olive. Plant Physiol. 46, 674–679. Baktir, I., Ulger, S., Himelrick, D.G., 2004. Relationship of seasonal changes in endogenous plant hormones and alternate bearing of olive trees. HortScience 39, 987–990.
Connor, D.J., Fereres, E., 2005. The physiology and adaptation of yield expression in olive. Hort. Rev. 31, 155–229. Cuevas, J., Rallo, L., Rapoport, H.F., 1994. Crop load effects on floral quality in olive. Sci. Hortic. 59, 123–130. Dag, A., Bustan, A., Avni, A., Lavee, S., Riov, J., 2009. Fruit thinning using NAA shows potential for reducing biennial bearing of ‘Barnea’ and ‘Picual’ oil olive trees. Crop & Pasture Science 60, 1124–1130. Fabbri, A., Benelli, C., 2000. Flower bud induction and differentiation in olive. J. Hort. Sci. Biotechnol. 75, 131–141. Ferna´ndez-Escobar, R., Benlloch, M., Navarro, C., Martin, G.C., 1992. The time of floral induction in olive. J. Am. Soc. Hort. Sci. 117, 304–307. Goldschmidt, E.E., 2005. Regulatory aspects of alternate bearing in fruit trees. Italus Hortus 12, 11–17 (in Italian). Lavee, S., 1996. Biology and physiology of the olive. In: Blazquez, J.M. (Ed.), World Olive Encyclopaedia. Plaza and Janes SA, Barcelona, Spain, pp. 61–105. Lavee, S., 2006. Biennial bearing in olive (Olea europaea L.). Olea FAO Olive Network 25, 5–13. Lavee, S., Harshemesh, H., Avidan, N., 1986. Phenolic acids—possible involvement in regulating growth and alternate fruiting in olive trees. Acta Hortic. 179, 317–328. Martin, G.C., 1989. Olive flower and fruit population dynamics. Acta Hortic. 286, 141–146. Monselise, P.S., Goldschmidt, E.E., 1982. Alternate bearing in fruit trees. Hort. Rev. 4, 128–173. Orlandi, F., Garcia-Mozo, H., Vazquez-Ezquerra, L., Romano, B., Dominguez, E., Galan, C., Fornaciari, M., 2004. Phenological olive chilling requirements in Umbria (Italy) and Andalusia (Spain). Plant Biosys. 138, 111–116. Rallo, L., Martin, G.C., 1991. The role of chilling in releasing olive floral buds from dormancy. J. Am. Soc. Hort. Sci. 116, 1058–1062. Rallo, L., Torreno, P., Vargas, J.A., Alvarado, J., 1994. Dormany and alternate bearing in olive. Acta Hortic. 356, 127–136. Ryan, D., Prenzler, P.D., Lavee, S., Antolovich, M., Robards, K., 2003. Quantitative changes in phenolic content during physiological development of the olive (Olea europaea) cultivar Hardy’s Mammoth. Int. J. Food Chem. 51, 2532–2538. Sanz-Corte´s, F., Martı´nez-Calvo, J., Badenes, M.L., Bleiholder, H., Hack, H., Llacer, G., Meier, U., 2002. Phenological growth stages of olive trees (Olea europaea). Ann. Appl. Biol. 140, 151–157. Stutte, G.W., Martin, G.C., 1986. Effect of killing the seed on return to bloom of olive. Sci. Hortic. 29, 107–113. Troncoso, A., Garcia, J.L., Lavee, S., 2010. Evaluation of the present information on the mechanisms leading to flower bud induction, evocation and differentiation. Acta Hortic., in press. Ulger, S., Sonmez, S., Karkacier, M., Ertoy, N., Akdesir, O., Aksu, M., 2004. Determination of endogenous hormones, sugars and mineral nutrition levels during the induction, initiation and differentiation stage and their effects on flower formation in olive. Plant Growth Reg. 42, 89–95.