Directory UMM :Data Elmu:jurnal:S:Scientia Horticulturae:Vol82.Issue3-4.Dec1999:
Scientia Horticulturae 82 (1999) 217±226
Photoperiod and temperature effect on growth of
strawberry plant (Fragaria ananassa Duch.):
development of a morphological test
to assess the dormancy induction
Fabien Roberta,*, Georgette Risserb, Gilles PeÂtela
a
Physiologie InteÂgreÂe de l'Arbre Fruitier (Unite associeÂe INRA Bioclimatologie-UniversiteÂ
Blaise Pascal) 24, avenue des Landais, F-63177 AubieÁre Cedex, France
b
INRA, Station d'AmeÂlioration des Plantes MaraõÃcheÁres, BP 94, 83143
Montfavet Cedex, France
Accepted 24 March 1999
Abstract
At the end of summer, the diminution of photoperiod and temperature cause a decrease of
vegetative growth and the dormancy of strawberry plants. Although the decrease in vegetative
growth can be measured morphologically, no test is able to evaluate the decrease in growth potential
(i.e. during the dormancy induction) nor its possible influence on vegetative growth. On the one
hand, to estimate this influence biometrically, we have correlated photoperiod and temperature
decreases with the vegetative growth decrease of some strawberry cultivars observed in the field.
Results have confirmed the major role of photoperiod, temperature and the effect of growth
potential decrease on vegetative growth. Moreover, the results showed that the decrease of
vegetative growth was an early event at the end of summer which depended upon strawberry
cultivar. On the other hand, we have measured petiole length under standard climatic conditions in a
growth chamber, after natural summer and autumnal exposures. Observations of strawberry plants
under these conditions revealed a decrease of their growth potential which also depended upon
strawberry cultivar. Results also confirmed the possible action of growth potential decrease on the
vegetative growth at the end of summer. Consequently, the observation of strawberry plants under
standard conditions can be used, as a test, to assess the exact moment of dormancy induction.
# 1999 Elsevier Science B.V. All rights reserved.
Keywords: Dormancy; Fragaria; Growth; Morphological test; Petiole length; Strawberry
* Corresponding author. Tel.: +33-4-73-40-79-06; fax: +33-4-73-40-79-16
E-mail address: frobert@cicsun.univ-bpclermont.fr (Fabien Robert)
0304-4238/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved.
PII: S 0 3 0 4 - 4 2 3 8 ( 9 9 ) 0 0 0 5 4 - 0
218
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
1. Introduction
Effects of environmental factors on the vegetative growth of strawberry plants
are well documented. At the end of summer, the decrease of vegetative growth is
caused mainly by changes in photoperiod (day length) and temperature changes
(Darrow and Waldo, 1934; Arney, 1956; Piringer and Scott, 1964; Heide, 1977;
Durner et al., 1984). The measurement of petiole length appears to be the best
parameter to evaluate vegetative growth (Chouard, 1946; Bailey and Rossi, 1964;
Jonkers, 1965; Risser and Robert, 1993). The photoperiod and temperature
decreases cause other effects on strawberry development, such as the decrease of
runner production (Smeets, 1980), flower induction (Dennis et al., 1970; Durner
and Poling, 1987) and the induction of dormancy (Darrow and Waldo, 1933;
Guttridge, 1968). This last effect causes physiological changes in strawberry
plants, resulting in a low level of growth potential which prevents any vegetative
growth development in autumn (Arney, 1955). Later, strawberry plants recover
vegetative and floral vigour under a chilling effect in autumn and winter
(Chouard, 1956; Guttridge, 1958; Risser and Robert, 1993).
Until now, no test was available to assess the decrease of growth potential at the
end of summer (dormancy induction). Moreover, because the growth potential
change occurs during the decrease of vegetative growth (directly imposed by
photoperiod and temperature changes), no direct morphological observations can
reveal the influence of this change on vegetative growth. In actual strawberry
farming, determining the period of this dormancy is important. So, in this study,
in order to control the major role of photoperiod and temperature on vegetative
growth, and thus to reveal the possible influence of the growth potential decrease
on vegetative growth during the induction of dormancy, the petiole lengths of
strawberry plants were measured under field conditions and correlated with
photoperiod and temperature values. Finally, to have a practical test to determine
dormancy induction, the growth potential of some strawberry cultivars cultivated
in controlled climatic conditions was evaluated by petiole length measurements
and the validity of this test was discussed.
2. Materials and methods
2.1. Plant material
In Avignon (438560 N, 48490 E), young strawberry plants (Fragaria ananassa
Duch.) were planted in pots (1.45 10ÿ2 m3, natural compost) and they were left
outside from the 2 August in a nursery. Observations were made on the cultivars
Favette, Valeta, Redgauntlet and Selva from August to November.
In Clermont-Ferrand (458470 N, 3870 E), young strawberry plants were planted
in June in pots (1.78 10ÿ2 m3; compost of sphagnum, pH 6.5) and left outside,
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
219
exposed to the natural climate in a nursery. Observations were made on the
cultivars Favette, Elsanta, Redgauntlet and Selva from July to November.
2.2. Observations of strawberry plants in the field
Vegetative growth changes were evaluated by measuring petiole lengths: the
new growing petioles were marked at regular dates (seven in Avignon and nine in
Clermont-Ferrand) by colour threads and their lengths were measured when the
petioles were fully grown. The averages of the petiole lengths marked by the
same colour thread were computed.
To evaluate the influence of climatic factors on the growth changes, the petiole
lengths marked at regular dates (L), were considered as the dependent variable.
They were regressed against two independent variables: photoperiod (P) and
temperature (T). The regression equation was as follows: L aP bT c,
where c is constant. We used a two-step estimation in order to avoid the
collinearity between photoperiod and temperature. The temperature variable was
regressed against the photoperiod variable and the residue (resT) of this
regression was saved and then used to replace the temperature variable in the
above equation. The residue that is obtained represents the effect of temperature
on the length of petioles which is not explained by photoperiod. We therefore
obtained L aP b resT c. For these measurements, the reference date was
the date the leaf emerged from the bud's sheath. For photoperiod, we used
photoperiod at the emerged date (P0) of the petiole or at 10, 20, 30, 40 and 50
days before emergence (Pÿ10, Pÿ20, Pÿ30, Pÿ40, Pÿ50), or at 10 and 20 days after
emergence (P10, P20). For temperatures (in 8C), we used day temperatures
(TD), night temperatures (TN), average of day and night temperatures (T) or
difference between day and night temperatures (TDÿN) for various periods: at the
emerged date of the petiole (0), average of 10, 20 or 30 days before emergence (0/
ÿ10; 0/ÿ20; 0/ÿ30), average of 10 or 20 days after emergence (0/10; 0/20),
average of 10±30 days before emergence (ÿ10/ÿ30) and average of 20±40 days
before emergence (ÿ20/ÿ40).
2.3. Observations under standard climatic conditions
Favette, Elsanta, Redgauntlet and Selva plants of cultivars were obtained and
stocked as those in field conditions in Avignon before they were transferred into a
growth chamber at various dates (photoperiod): D1 5 July (15 h 20); D2 16
July (15 h 05); D3 30 August (13 h 16) and D4 4 November (10 h 10). The
growth chamber conditions were 25/15 18C (day/night) with a 12 h light
photoperiod (artificial metal halogen lighting 270 30 mmol mÿ2 sÿ1), in 80%
relative humidity. Vegetative growth changes of strawberry plants were evaluated,
220
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
as in the field, by measuring the length of the full-grown petioles which emerged
only after the transfer of plants to the growth chamber.
Growth potential changes of strawberry plants were evaluated two months after
the transfer of plants into the growth chamber, by comparing the petiole length
measurements of different series.
2.4. Statistical analysis
For the field observations, petiole length averages were tested for each cultivar,
using a multiple range test (p < 0.05; StateGraphic software). For multiple
regressions, the significance level for each term was reported.
For observations under standard climatic conditions, the regressions between
the averages of each cultivar were computed.
3. Results
3.1. Observations of strawberry plants in the field
Petiole length measurements of strawberry plants observed under natural
conditions revealed the decrease of vegetative growth. In Avignon (Table 1), a
decrease in petiole lengths was noted from 16 August for cultivars Valeta,
Redgauntlet and Selva plants, and from 30 August for cultivar Favette. This
decrease was rapid for all cultivars, and led to short petioles for Favette, Valeta
and Redgauntlet plants at the beginning of autumn. In Clermont-Ferrand
(Table 2), petiole lengths of cultivars Elsanta and Selva remained long from 26
June to 16 August, whereas those of Favette and Redgauntlet decreased sooner,
from 2 August to 11 July, respectively. As measured in Avignon, the petiole
Table 1
Petiole lengths (in mm) of strawberry plants (average of four petioles) observed under natural
climatic conditions in Avignon (458560 N, 48490 E)
Emerged date of petioles
Cultivars
Favette
Valeta
Redgauntlet
Selva
8/16
8/30
9/13
9/27
10/11
10/25
11/08
133a
145a
82b
58b
30c
24c
23c
149a
109b
76c
48d
25e
23e
21e
23a
75b
54bc
40c
28d
20de
20e
135a
111ab
78b
70bc
51c
44d
42d
Note: For each cultivar, the values followed by different letters are significantly different at the
0.05 probability level.
221
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
Table 2
Petiole lengths (in mm) of strawberry plants (average of seven petioles) observed under natural
climatic conditions in Clermont-Ferrand (458470 N, 3870 E)
Emerged date of petioles
6/26
7/02
7/11
7/22
8/02
8/16
9/15
9/30
10/15
Cultivars
Favette
Elsanta
Redgauntlet
Selva
96a
102a
108a
91ab
88b
71c
49d
36e
27f
98a
85a
110a
100a
93a
89a
48b
38c
28d
128a
122a
91b
96b
96b
77c
50d
39e
29f
147ab
136ab
159a
132ab
133ab
130bc
116c
97d
81e
Note: For each cultivar, the values followed by different letters are significantly different at the
0.05 probability level.
length of cultivar Selva plants remained more important than those of the other
cultivars. The small difference between petiole growth changes in Avignon and in
Clermont-Ferrand was due to a temperature variation between the two cities:
warmer in Avignon than in Clermont-Ferrand at the same dates, the photoperiod
being approximately comparable.
Regression analysis revealed that the photoperiod 30 days before the emerged
date of the petiole (Pÿ30) and the mean of day and night temperatures 20 days
after the emerged date of the petiole (T0/20), were the most influential factors for
all the cultivars (Table 3). So, the relation between petiole length, photoperiod
and temperature values, can be formulated as L aPÿ30 b resT0/20 c,
where resT0/20 is the residual term obtained from the regression of T0/20
(dependent variable) against Pÿ30 (independent variable). These analyses show a
clear influence of other photoperiods which should be due to the fact that
photoperiod variations were closely linked in this season.
3.2. Observations under standard climatic conditions
Petiole length measurements of strawberry plants transferred into the growth
chamber at various dates were analysed. They showed different vegetative
changes for the four cultivars (Fig. 1):
± For cultivar Favette, growth of petioles was reduced after D1 (5 July), D2 (16
July) and D3 (30 August) transfers, whereas it was maintained for `Selva'
plants. For `Elsanta' and `Redgauntlet', petiole lengths decreased rapidly after
transfer.
222
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
Table 3
The best determinants of the length of petioles are estimated as L aPÿ30 b resT0/20 c
R2
Site
Cultivar
c
a
Cl-Fd
Favette
Elsanta
Selva
Redgauntlet
ÿ286.7
ÿ275.7
ÿ135.9
ÿ313.9
40.41c
40.4c
60.26c
60.45c
7.37b
6.28c
2.63
6.93b
0.7c
0.79c
0.43c
0.72c
Avignon
Favette
Valeta
Selva
Redgauntlet
ÿ388.8
ÿ382.7
ÿ245.5
ÿ270.0
20.58c
50.56c
20.4c
50.4c
3.55a
7.7a
4.55a
10.4b
0.77c
0.83c
0.62c
0.8c
b
Note: The coefficients (a and b) of the independent variables (Pÿ30 and T0/20) are reported in the
table. Significances of the partial implication of independent variables are indicated between
brackets. For Clermont-Ferrand (Cl-Fd), n 9 and for Avignon, n 7.
a
p < 0.05.
b
p < 0.01.
c
p < 0.001.
± In the last series (D4; 4 November), all petiole lengths of the four cultivars
remained short after transfer.
The comparison of petiole lengths of the different series two months after
transfers (56 days for D1, 59 for D2, 56 for D3 and 63 for D4) revealed a rapid
decrease of the growth potential for cultivars Favette and Elsanta at the end of
summer, whereas Redgauntlet and Selva cultivars maintained growth until
autumn (Fig. 2). Regressions between petiole lengths of cultivars confirm the
similarity, e.g. `Favette' against `Elsanta', r 0.98 (p < 0.05); `Redgauntlet'
against `Selva', r 0.97 (p < 0.05); `Favette' against `Selva', r 0.77 (p > 0.05);
`Favette' against `Redgauntlet', r 0.8 (p > 0.05); `Elsanta' against `Selva',
r 0.79 (p > 0.05); `Elsanta' against `Redgauntlet', r 0.77 (p > 0.05).
4. Discussion
The effect of photoperiod and temperature changes on growth decrease of
strawberry plants had been shown by some authors (Darrow and Waldo, 1934;
Arney, 1956; Piringer and Scott, 1964; Gosselink and Smith, 1966; Heide, 1977;
Durner and Poling, 1987). Although the measurement of petiole length appears to
be the best parameter to evaluate vegetative growth, no test is available to assess
the autumnal decrease of growth potential during the induction of dormancy.
In our study, the evaluation of vegetative growth of several strawberry cultivars
observed in the field, through petiole length measurements, showed different
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
223
Fig. 1. The final lengths of the petioles that emerged after plant transfers from outdoors to a growth
chamber at various dates. A: D1 5 July; B: D2 16 July; C: D3 30 August and D: D4 4
November.
224
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
Fig. 2. The final lengths of the petioles that emerged two months after plant transfers from outdoors
to a growth chamber at various dates. D1 5 July; D2 16 July; D3 30 August and D4 4
November.
morphological responses to photoperiod and temperature variations at the end of
summer (Tables 1 and 2). `Redgauntlet' plants exhibited a precocious vegetative
growth decrease. Length decreases of the successive growing petioles were less
important for `Selva' and `Elsanta' compared to other cultivars. So, cultivars are
differently sensible to environmental factors for their vegetative growth
behaviour, as for flowering (Darrow and Waldo, 1934; Arney, 1956; Durner et
al., 1984) or runner production (Piringer and Scott, 1964; Dennis et al., 1970;
Durner and Poling, 1987). The results obtained here confirm the major role of
photoperiod and temperature in the decrease of vegetative growth (Table 3).
According to these results, it appears that photoperiod 30 days before the
emergence of the petiole (Pÿ30), and, to a lesser extent, temperature during
growth of the petiole (T0/20), had the greatest influence on petiole development
(Table 3). The biometrical analyses confirm the major role of photoperiod and
temperature on petiole growth decrease, but they also reveal that these factors
cannot explain totally this decrease. So, the unexplained part of the influence
should be due, at least partly, to internal factors, notably for `Selva' which is less
influenced by external factors.
The change in growth potential under photoperiod and temperature decreases
(dormancy induction) should be the major internal factor contributing to the
decrease of vegetative growth. To reveal this change, we evaluated the growth
potential of strawberry plants during their vegetative growth decrease: the
observation of strawberry plants transferred to standard climatic conditions (from
15 h 20 (D1), 15 h 05 (D2) and 13 h 16 (D3) to 12 h 00 in growth chamber) at
different times showed different growth responses (Fig. 1(A)±(C)). The last
transfer (D4) had no effect on the growth of petioles, even if the photoperiod
conditions of the growth chamber were longer than those of field (Fig. 1(D)). In
these conditions, the physiological state of the strawberry plants may be the main
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
225
cause of this morphological response, petiole length depending upon the growth
potential. Also, two months after transfer, petiole length comparisons between the
different series of strawberry plants (Fig. 2) confirmed the growth potential
decrease that was induced in late summer in `Elsanta' and `Favette'. So, these
standard climatic conditions could reveal the growth potential of the strawberry
plants and could be used as a test to reveal the dormancy induction of these
plants.
Our results confirm the possibility of a major influence of growth potential on
vegetative growth. In the field, this influence occurred with the additional effect
of natural factors. If natural factors are able to influence growth potential and
vegetative growth, growth responses to these factors are different. For example, in
Avignon, the vegetative growth decrease of `Redgauntlet' plants started on 16
August (Table 2), whereas the growth potential decrease occurred after 30 August
(Fig. 3). The dormancy induction, through growth potential decrease, was later in
the season than the vegetative growth decrease, which could imply drastic
physiological changes.
We conclude that vegetative growth decrease is an early phenomenon in the
summer. Moreover, the results have shown the major role of photoperiod and
temperature in the development of the petiole which was different for different
cultivars, but also the effect of growth potential decrease on this vegetative
growth. Petiole measurements of strawberry plant transferred from outdoors into
a growth chamber have confirmed these differences between cultivars. The same
measurements made two months after transfer have permitted the evolution of the
growth potential of these plants to be assessed. So, these standard climatic
conditions could be used to test the dormancy induction of strawberry plants.
Acknowledgements
The authors gratefully thank the ``Centre InterreÂgional de Recherche et
d'ExpeÂrimentation de la Fraise'' for its contribution in equipment and the
``Centre Technique Interprofessionnel des Fruits et LeÂgumes'' for financial
support. We also thank Mrs Lenne for her corrections and suggestions.
References
Arney, S.E., 1955. Studies of growth and development in the genus Fragaria. IV. Winter growth.
Ann. Bot. 74, 265±276.
Arney, S.E., 1956. Studies of growth and development in the genus Fragaria. VI. The effect of
photoperiod and temperature on leaf size. J. Exp. Bot. 7, 65±79.
Bailey, J.S., Rossi, A.W., 1964. Effect of fall chilling, forcing temperature and day length on the
growth and flowering of Catskill strawberry plants. Proc. Amer. Soc. Hort. Sci. 7, pp. 245±252.
226
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
Chouard, P., 1946. About effect of photoperiod on growth (in French). C.R. Acad. Sci., Paris 223,
1174±1176.
Chouard, P., 1956. Forcing and temperature-photoperiod preparations. In: Tournier and Constans
(Eds), Dormancy and inhibition of seeds and buds (in French). Centre de Docum. Univ., Paris,
pp. 1±160.
Darrow, G.M., Waldo, G.F., 1933. Photoperiodism as a cause of the rest period in strawberries.
Science 77, 353±354.
Darrow, G.M., Waldo, G.F., 1934. Responses of strawberry varieties and species to duration of the
daily light period. USDA Tech. Bul. 453, 1±31.
Dennis, F.G., Lipecki, J., Kiang, C.L., 1970. Effects of photoperiod and other factors upon
flowering and runner development of three strawberry cultivars. J Amer. Soc. Hort. Sci. 95, 750±
754.
Durner, E.F., Poling, E.B., 1987. Flower bud induction, initiation, differentiation and development
in the `Earliglow' Strawberry. Sci. Hort. 31, 61±69.
Durner, E.F., Barden, J.A., Himelrick, D.G., Poling, E.B., 1984. Photoperiod and temperature
effects on flower and runner development in day-neutral, junebearing, and everbearing
strawberries. J. Amer. Soc. Horti. Sci. 109, 396±400.
Gosselink, J.G., Smith, C.R., 1966. Vegetative growth responses of strawberry plants to differing
photoperiods. Hort. Res. 7, 24±33.
Guttridge, C.G., 1958. The effect of winter chilling on the subsequent growth and development of
the cultivated strawberry plant. J. Hort. Sci. 33, 119±127.
Guttridge, C.G., 1968. Hormone physiology of growth regulation in strawberry. In: Plant growth
Regulators, S.C.I. Monograph. 31, pp. 157±169.
Heide, O.M., 1977. Photoperiod and interactions in growth and flowering of strawberry. Physiol.
Plant. 40, 21±26.
Jonkers, H., 1965. On the flower formation, the dormancy and the early forcing of strawberries.
Med Landbwg Wageningen 65, 1±71.
Piringer, A.A., Scott, D.H., 1964. Interrelation of photoperiod, chilling, and flower-cluster and
runner production by strawberries. J. Amer. Soc. Hort. Sci. 84, 295±301.
Risser, G., Robert, F., 1993. What cold treatments promote growth in strawberry?. Acta Hortic. 48,
381±383.
Smeets, L., 1980. Effect of temperature and daylength on flower initiation and runner formation in
two everbearing strawberry cultivars. Sci. Hortic 12, 19±26.
Photoperiod and temperature effect on growth of
strawberry plant (Fragaria ananassa Duch.):
development of a morphological test
to assess the dormancy induction
Fabien Roberta,*, Georgette Risserb, Gilles PeÂtela
a
Physiologie InteÂgreÂe de l'Arbre Fruitier (Unite associeÂe INRA Bioclimatologie-UniversiteÂ
Blaise Pascal) 24, avenue des Landais, F-63177 AubieÁre Cedex, France
b
INRA, Station d'AmeÂlioration des Plantes MaraõÃcheÁres, BP 94, 83143
Montfavet Cedex, France
Accepted 24 March 1999
Abstract
At the end of summer, the diminution of photoperiod and temperature cause a decrease of
vegetative growth and the dormancy of strawberry plants. Although the decrease in vegetative
growth can be measured morphologically, no test is able to evaluate the decrease in growth potential
(i.e. during the dormancy induction) nor its possible influence on vegetative growth. On the one
hand, to estimate this influence biometrically, we have correlated photoperiod and temperature
decreases with the vegetative growth decrease of some strawberry cultivars observed in the field.
Results have confirmed the major role of photoperiod, temperature and the effect of growth
potential decrease on vegetative growth. Moreover, the results showed that the decrease of
vegetative growth was an early event at the end of summer which depended upon strawberry
cultivar. On the other hand, we have measured petiole length under standard climatic conditions in a
growth chamber, after natural summer and autumnal exposures. Observations of strawberry plants
under these conditions revealed a decrease of their growth potential which also depended upon
strawberry cultivar. Results also confirmed the possible action of growth potential decrease on the
vegetative growth at the end of summer. Consequently, the observation of strawberry plants under
standard conditions can be used, as a test, to assess the exact moment of dormancy induction.
# 1999 Elsevier Science B.V. All rights reserved.
Keywords: Dormancy; Fragaria; Growth; Morphological test; Petiole length; Strawberry
* Corresponding author. Tel.: +33-4-73-40-79-06; fax: +33-4-73-40-79-16
E-mail address: frobert@cicsun.univ-bpclermont.fr (Fabien Robert)
0304-4238/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved.
PII: S 0 3 0 4 - 4 2 3 8 ( 9 9 ) 0 0 0 5 4 - 0
218
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
1. Introduction
Effects of environmental factors on the vegetative growth of strawberry plants
are well documented. At the end of summer, the decrease of vegetative growth is
caused mainly by changes in photoperiod (day length) and temperature changes
(Darrow and Waldo, 1934; Arney, 1956; Piringer and Scott, 1964; Heide, 1977;
Durner et al., 1984). The measurement of petiole length appears to be the best
parameter to evaluate vegetative growth (Chouard, 1946; Bailey and Rossi, 1964;
Jonkers, 1965; Risser and Robert, 1993). The photoperiod and temperature
decreases cause other effects on strawberry development, such as the decrease of
runner production (Smeets, 1980), flower induction (Dennis et al., 1970; Durner
and Poling, 1987) and the induction of dormancy (Darrow and Waldo, 1933;
Guttridge, 1968). This last effect causes physiological changes in strawberry
plants, resulting in a low level of growth potential which prevents any vegetative
growth development in autumn (Arney, 1955). Later, strawberry plants recover
vegetative and floral vigour under a chilling effect in autumn and winter
(Chouard, 1956; Guttridge, 1958; Risser and Robert, 1993).
Until now, no test was available to assess the decrease of growth potential at the
end of summer (dormancy induction). Moreover, because the growth potential
change occurs during the decrease of vegetative growth (directly imposed by
photoperiod and temperature changes), no direct morphological observations can
reveal the influence of this change on vegetative growth. In actual strawberry
farming, determining the period of this dormancy is important. So, in this study,
in order to control the major role of photoperiod and temperature on vegetative
growth, and thus to reveal the possible influence of the growth potential decrease
on vegetative growth during the induction of dormancy, the petiole lengths of
strawberry plants were measured under field conditions and correlated with
photoperiod and temperature values. Finally, to have a practical test to determine
dormancy induction, the growth potential of some strawberry cultivars cultivated
in controlled climatic conditions was evaluated by petiole length measurements
and the validity of this test was discussed.
2. Materials and methods
2.1. Plant material
In Avignon (438560 N, 48490 E), young strawberry plants (Fragaria ananassa
Duch.) were planted in pots (1.45 10ÿ2 m3, natural compost) and they were left
outside from the 2 August in a nursery. Observations were made on the cultivars
Favette, Valeta, Redgauntlet and Selva from August to November.
In Clermont-Ferrand (458470 N, 3870 E), young strawberry plants were planted
in June in pots (1.78 10ÿ2 m3; compost of sphagnum, pH 6.5) and left outside,
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
219
exposed to the natural climate in a nursery. Observations were made on the
cultivars Favette, Elsanta, Redgauntlet and Selva from July to November.
2.2. Observations of strawberry plants in the field
Vegetative growth changes were evaluated by measuring petiole lengths: the
new growing petioles were marked at regular dates (seven in Avignon and nine in
Clermont-Ferrand) by colour threads and their lengths were measured when the
petioles were fully grown. The averages of the petiole lengths marked by the
same colour thread were computed.
To evaluate the influence of climatic factors on the growth changes, the petiole
lengths marked at regular dates (L), were considered as the dependent variable.
They were regressed against two independent variables: photoperiod (P) and
temperature (T). The regression equation was as follows: L aP bT c,
where c is constant. We used a two-step estimation in order to avoid the
collinearity between photoperiod and temperature. The temperature variable was
regressed against the photoperiod variable and the residue (resT) of this
regression was saved and then used to replace the temperature variable in the
above equation. The residue that is obtained represents the effect of temperature
on the length of petioles which is not explained by photoperiod. We therefore
obtained L aP b resT c. For these measurements, the reference date was
the date the leaf emerged from the bud's sheath. For photoperiod, we used
photoperiod at the emerged date (P0) of the petiole or at 10, 20, 30, 40 and 50
days before emergence (Pÿ10, Pÿ20, Pÿ30, Pÿ40, Pÿ50), or at 10 and 20 days after
emergence (P10, P20). For temperatures (in 8C), we used day temperatures
(TD), night temperatures (TN), average of day and night temperatures (T) or
difference between day and night temperatures (TDÿN) for various periods: at the
emerged date of the petiole (0), average of 10, 20 or 30 days before emergence (0/
ÿ10; 0/ÿ20; 0/ÿ30), average of 10 or 20 days after emergence (0/10; 0/20),
average of 10±30 days before emergence (ÿ10/ÿ30) and average of 20±40 days
before emergence (ÿ20/ÿ40).
2.3. Observations under standard climatic conditions
Favette, Elsanta, Redgauntlet and Selva plants of cultivars were obtained and
stocked as those in field conditions in Avignon before they were transferred into a
growth chamber at various dates (photoperiod): D1 5 July (15 h 20); D2 16
July (15 h 05); D3 30 August (13 h 16) and D4 4 November (10 h 10). The
growth chamber conditions were 25/15 18C (day/night) with a 12 h light
photoperiod (artificial metal halogen lighting 270 30 mmol mÿ2 sÿ1), in 80%
relative humidity. Vegetative growth changes of strawberry plants were evaluated,
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F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
as in the field, by measuring the length of the full-grown petioles which emerged
only after the transfer of plants to the growth chamber.
Growth potential changes of strawberry plants were evaluated two months after
the transfer of plants into the growth chamber, by comparing the petiole length
measurements of different series.
2.4. Statistical analysis
For the field observations, petiole length averages were tested for each cultivar,
using a multiple range test (p < 0.05; StateGraphic software). For multiple
regressions, the significance level for each term was reported.
For observations under standard climatic conditions, the regressions between
the averages of each cultivar were computed.
3. Results
3.1. Observations of strawberry plants in the field
Petiole length measurements of strawberry plants observed under natural
conditions revealed the decrease of vegetative growth. In Avignon (Table 1), a
decrease in petiole lengths was noted from 16 August for cultivars Valeta,
Redgauntlet and Selva plants, and from 30 August for cultivar Favette. This
decrease was rapid for all cultivars, and led to short petioles for Favette, Valeta
and Redgauntlet plants at the beginning of autumn. In Clermont-Ferrand
(Table 2), petiole lengths of cultivars Elsanta and Selva remained long from 26
June to 16 August, whereas those of Favette and Redgauntlet decreased sooner,
from 2 August to 11 July, respectively. As measured in Avignon, the petiole
Table 1
Petiole lengths (in mm) of strawberry plants (average of four petioles) observed under natural
climatic conditions in Avignon (458560 N, 48490 E)
Emerged date of petioles
Cultivars
Favette
Valeta
Redgauntlet
Selva
8/16
8/30
9/13
9/27
10/11
10/25
11/08
133a
145a
82b
58b
30c
24c
23c
149a
109b
76c
48d
25e
23e
21e
23a
75b
54bc
40c
28d
20de
20e
135a
111ab
78b
70bc
51c
44d
42d
Note: For each cultivar, the values followed by different letters are significantly different at the
0.05 probability level.
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F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
Table 2
Petiole lengths (in mm) of strawberry plants (average of seven petioles) observed under natural
climatic conditions in Clermont-Ferrand (458470 N, 3870 E)
Emerged date of petioles
6/26
7/02
7/11
7/22
8/02
8/16
9/15
9/30
10/15
Cultivars
Favette
Elsanta
Redgauntlet
Selva
96a
102a
108a
91ab
88b
71c
49d
36e
27f
98a
85a
110a
100a
93a
89a
48b
38c
28d
128a
122a
91b
96b
96b
77c
50d
39e
29f
147ab
136ab
159a
132ab
133ab
130bc
116c
97d
81e
Note: For each cultivar, the values followed by different letters are significantly different at the
0.05 probability level.
length of cultivar Selva plants remained more important than those of the other
cultivars. The small difference between petiole growth changes in Avignon and in
Clermont-Ferrand was due to a temperature variation between the two cities:
warmer in Avignon than in Clermont-Ferrand at the same dates, the photoperiod
being approximately comparable.
Regression analysis revealed that the photoperiod 30 days before the emerged
date of the petiole (Pÿ30) and the mean of day and night temperatures 20 days
after the emerged date of the petiole (T0/20), were the most influential factors for
all the cultivars (Table 3). So, the relation between petiole length, photoperiod
and temperature values, can be formulated as L aPÿ30 b resT0/20 c,
where resT0/20 is the residual term obtained from the regression of T0/20
(dependent variable) against Pÿ30 (independent variable). These analyses show a
clear influence of other photoperiods which should be due to the fact that
photoperiod variations were closely linked in this season.
3.2. Observations under standard climatic conditions
Petiole length measurements of strawberry plants transferred into the growth
chamber at various dates were analysed. They showed different vegetative
changes for the four cultivars (Fig. 1):
± For cultivar Favette, growth of petioles was reduced after D1 (5 July), D2 (16
July) and D3 (30 August) transfers, whereas it was maintained for `Selva'
plants. For `Elsanta' and `Redgauntlet', petiole lengths decreased rapidly after
transfer.
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F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
Table 3
The best determinants of the length of petioles are estimated as L aPÿ30 b resT0/20 c
R2
Site
Cultivar
c
a
Cl-Fd
Favette
Elsanta
Selva
Redgauntlet
ÿ286.7
ÿ275.7
ÿ135.9
ÿ313.9
40.41c
40.4c
60.26c
60.45c
7.37b
6.28c
2.63
6.93b
0.7c
0.79c
0.43c
0.72c
Avignon
Favette
Valeta
Selva
Redgauntlet
ÿ388.8
ÿ382.7
ÿ245.5
ÿ270.0
20.58c
50.56c
20.4c
50.4c
3.55a
7.7a
4.55a
10.4b
0.77c
0.83c
0.62c
0.8c
b
Note: The coefficients (a and b) of the independent variables (Pÿ30 and T0/20) are reported in the
table. Significances of the partial implication of independent variables are indicated between
brackets. For Clermont-Ferrand (Cl-Fd), n 9 and for Avignon, n 7.
a
p < 0.05.
b
p < 0.01.
c
p < 0.001.
± In the last series (D4; 4 November), all petiole lengths of the four cultivars
remained short after transfer.
The comparison of petiole lengths of the different series two months after
transfers (56 days for D1, 59 for D2, 56 for D3 and 63 for D4) revealed a rapid
decrease of the growth potential for cultivars Favette and Elsanta at the end of
summer, whereas Redgauntlet and Selva cultivars maintained growth until
autumn (Fig. 2). Regressions between petiole lengths of cultivars confirm the
similarity, e.g. `Favette' against `Elsanta', r 0.98 (p < 0.05); `Redgauntlet'
against `Selva', r 0.97 (p < 0.05); `Favette' against `Selva', r 0.77 (p > 0.05);
`Favette' against `Redgauntlet', r 0.8 (p > 0.05); `Elsanta' against `Selva',
r 0.79 (p > 0.05); `Elsanta' against `Redgauntlet', r 0.77 (p > 0.05).
4. Discussion
The effect of photoperiod and temperature changes on growth decrease of
strawberry plants had been shown by some authors (Darrow and Waldo, 1934;
Arney, 1956; Piringer and Scott, 1964; Gosselink and Smith, 1966; Heide, 1977;
Durner and Poling, 1987). Although the measurement of petiole length appears to
be the best parameter to evaluate vegetative growth, no test is available to assess
the autumnal decrease of growth potential during the induction of dormancy.
In our study, the evaluation of vegetative growth of several strawberry cultivars
observed in the field, through petiole length measurements, showed different
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
223
Fig. 1. The final lengths of the petioles that emerged after plant transfers from outdoors to a growth
chamber at various dates. A: D1 5 July; B: D2 16 July; C: D3 30 August and D: D4 4
November.
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F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
Fig. 2. The final lengths of the petioles that emerged two months after plant transfers from outdoors
to a growth chamber at various dates. D1 5 July; D2 16 July; D3 30 August and D4 4
November.
morphological responses to photoperiod and temperature variations at the end of
summer (Tables 1 and 2). `Redgauntlet' plants exhibited a precocious vegetative
growth decrease. Length decreases of the successive growing petioles were less
important for `Selva' and `Elsanta' compared to other cultivars. So, cultivars are
differently sensible to environmental factors for their vegetative growth
behaviour, as for flowering (Darrow and Waldo, 1934; Arney, 1956; Durner et
al., 1984) or runner production (Piringer and Scott, 1964; Dennis et al., 1970;
Durner and Poling, 1987). The results obtained here confirm the major role of
photoperiod and temperature in the decrease of vegetative growth (Table 3).
According to these results, it appears that photoperiod 30 days before the
emergence of the petiole (Pÿ30), and, to a lesser extent, temperature during
growth of the petiole (T0/20), had the greatest influence on petiole development
(Table 3). The biometrical analyses confirm the major role of photoperiod and
temperature on petiole growth decrease, but they also reveal that these factors
cannot explain totally this decrease. So, the unexplained part of the influence
should be due, at least partly, to internal factors, notably for `Selva' which is less
influenced by external factors.
The change in growth potential under photoperiod and temperature decreases
(dormancy induction) should be the major internal factor contributing to the
decrease of vegetative growth. To reveal this change, we evaluated the growth
potential of strawberry plants during their vegetative growth decrease: the
observation of strawberry plants transferred to standard climatic conditions (from
15 h 20 (D1), 15 h 05 (D2) and 13 h 16 (D3) to 12 h 00 in growth chamber) at
different times showed different growth responses (Fig. 1(A)±(C)). The last
transfer (D4) had no effect on the growth of petioles, even if the photoperiod
conditions of the growth chamber were longer than those of field (Fig. 1(D)). In
these conditions, the physiological state of the strawberry plants may be the main
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
225
cause of this morphological response, petiole length depending upon the growth
potential. Also, two months after transfer, petiole length comparisons between the
different series of strawberry plants (Fig. 2) confirmed the growth potential
decrease that was induced in late summer in `Elsanta' and `Favette'. So, these
standard climatic conditions could reveal the growth potential of the strawberry
plants and could be used as a test to reveal the dormancy induction of these
plants.
Our results confirm the possibility of a major influence of growth potential on
vegetative growth. In the field, this influence occurred with the additional effect
of natural factors. If natural factors are able to influence growth potential and
vegetative growth, growth responses to these factors are different. For example, in
Avignon, the vegetative growth decrease of `Redgauntlet' plants started on 16
August (Table 2), whereas the growth potential decrease occurred after 30 August
(Fig. 3). The dormancy induction, through growth potential decrease, was later in
the season than the vegetative growth decrease, which could imply drastic
physiological changes.
We conclude that vegetative growth decrease is an early phenomenon in the
summer. Moreover, the results have shown the major role of photoperiod and
temperature in the development of the petiole which was different for different
cultivars, but also the effect of growth potential decrease on this vegetative
growth. Petiole measurements of strawberry plant transferred from outdoors into
a growth chamber have confirmed these differences between cultivars. The same
measurements made two months after transfer have permitted the evolution of the
growth potential of these plants to be assessed. So, these standard climatic
conditions could be used to test the dormancy induction of strawberry plants.
Acknowledgements
The authors gratefully thank the ``Centre InterreÂgional de Recherche et
d'ExpeÂrimentation de la Fraise'' for its contribution in equipment and the
``Centre Technique Interprofessionnel des Fruits et LeÂgumes'' for financial
support. We also thank Mrs Lenne for her corrections and suggestions.
References
Arney, S.E., 1955. Studies of growth and development in the genus Fragaria. IV. Winter growth.
Ann. Bot. 74, 265±276.
Arney, S.E., 1956. Studies of growth and development in the genus Fragaria. VI. The effect of
photoperiod and temperature on leaf size. J. Exp. Bot. 7, 65±79.
Bailey, J.S., Rossi, A.W., 1964. Effect of fall chilling, forcing temperature and day length on the
growth and flowering of Catskill strawberry plants. Proc. Amer. Soc. Hort. Sci. 7, pp. 245±252.
226
F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226
Chouard, P., 1946. About effect of photoperiod on growth (in French). C.R. Acad. Sci., Paris 223,
1174±1176.
Chouard, P., 1956. Forcing and temperature-photoperiod preparations. In: Tournier and Constans
(Eds), Dormancy and inhibition of seeds and buds (in French). Centre de Docum. Univ., Paris,
pp. 1±160.
Darrow, G.M., Waldo, G.F., 1933. Photoperiodism as a cause of the rest period in strawberries.
Science 77, 353±354.
Darrow, G.M., Waldo, G.F., 1934. Responses of strawberry varieties and species to duration of the
daily light period. USDA Tech. Bul. 453, 1±31.
Dennis, F.G., Lipecki, J., Kiang, C.L., 1970. Effects of photoperiod and other factors upon
flowering and runner development of three strawberry cultivars. J Amer. Soc. Hort. Sci. 95, 750±
754.
Durner, E.F., Poling, E.B., 1987. Flower bud induction, initiation, differentiation and development
in the `Earliglow' Strawberry. Sci. Hort. 31, 61±69.
Durner, E.F., Barden, J.A., Himelrick, D.G., Poling, E.B., 1984. Photoperiod and temperature
effects on flower and runner development in day-neutral, junebearing, and everbearing
strawberries. J. Amer. Soc. Horti. Sci. 109, 396±400.
Gosselink, J.G., Smith, C.R., 1966. Vegetative growth responses of strawberry plants to differing
photoperiods. Hort. Res. 7, 24±33.
Guttridge, C.G., 1958. The effect of winter chilling on the subsequent growth and development of
the cultivated strawberry plant. J. Hort. Sci. 33, 119±127.
Guttridge, C.G., 1968. Hormone physiology of growth regulation in strawberry. In: Plant growth
Regulators, S.C.I. Monograph. 31, pp. 157±169.
Heide, O.M., 1977. Photoperiod and interactions in growth and flowering of strawberry. Physiol.
Plant. 40, 21±26.
Jonkers, H., 1965. On the flower formation, the dormancy and the early forcing of strawberries.
Med Landbwg Wageningen 65, 1±71.
Piringer, A.A., Scott, D.H., 1964. Interrelation of photoperiod, chilling, and flower-cluster and
runner production by strawberries. J. Amer. Soc. Hort. Sci. 84, 295±301.
Risser, G., Robert, F., 1993. What cold treatments promote growth in strawberry?. Acta Hortic. 48,
381±383.
Smeets, L., 1980. Effect of temperature and daylength on flower initiation and runner formation in
two everbearing strawberry cultivars. Sci. Hortic 12, 19±26.