Pollination requirement of carob trees Ceratonia Siliqua grown under semiarid conditions.
Mediterranean conditions  provide an excellent environment for wild and cultivated trees [1,41]. These trees serve as shelter and food to many species of animals which feed on its nectar, pollen, leaves and fruits [34,28]. The value of the carob tree has increased as a result of its multipurpose use such as Arabic confectionery and drinks, animal feed and human food, microbial protein and as a raw material for industrial processing [39,34,28].
Lower fruit and seed sets is common in Leguminosae species despite the high number of produced flowers [12,25]. One case of this being Leguminosae species that have indeterminate inflorescence types, e.g., Caesalpinia eriostachys, Myrospermum frutescens, and Lathyrus vernus [3,13]. The pattern of fruits and seeds set in some plant species often decreases from base to apex of the inflorescence [19,22] and this pattern is often attributed to competition of developing fruits for nutritional resources [30,19]. Furthermore, a pattern of a higher fruit production in the central zone of the raceme, as observed in Myrosmodes cochleares, Epilobium dodonaei, and E. fleischeri species, were rather attributed to pollinators' activity [5,31,11]. While in other species there was no consistent fruiting pattern related with position within the inflorescence [40,11]. Fruit distribution on the racemes is controlled by resource limitations [3,11]. The order of flower opening determines the order of pollination; and subsequently the order of ovary growth and hormones produced by developing seeds cause the mobilization of resources into the fruit .
In Jordan, Carob trees grown mainly in the highlands such as Irbid, Ajloun, Al Salt and Amman, have become characterized by cold winters and hot dry summers. These species and genera have adapted to harsh conditions and produce high numbers of male and female flowers but exhibit a low percentage of fruiting per raceme in both wild and cultivated population. This phenomenon of a pollination failure could be attributed to insect pollinator factor, environmental factor or plant factor . Since honey bee colonies are available as insect pollinators with the prevalence of hot dry conditions generally each year, the plant factor may interfere with fruit and seed set but have not been evaluated. Thus, this study was performed to evaluate the response of plant pollination to flowering load and to assess the compatibility of hermaphrodite flowers produced by some Ceratonia Siliqua trees.
MATERIALS AND METHODS
The study was conducted as part of Jordan University of Science and Technology (JUST) campus in northern Jordan, Ramtha (520m altitude). The site is characterized by an arid climate of mild rainy winters and dry hot summers. In the last 10 years, the mean annual rainfall was 211mm. Average rainfall in the years 2008 and 2009 was 224mm and 195mm, respectively. The mean maximum air temperature during August was 36[degrees]C and the mean minimum air temperature during January was 9[degrees]C.
Flower order (remove part racemes flowers):
To study the effect of flowers order on fruit and seed set on the same raceme; four healthy trees were randomly selected with many healthy branches bearing dense flower buds. On each tree, 48 mature racemes were randomly labeled, resulting in a total of 192 racemes. Honey bee workers as well as other insect visitor in the area had access to flowers and wind pollination was also possible. Each raceme was divided into three parts named early part, intermediate part and late part. These racemes were subjected to the following treatments:
Removal of late (Apical) flowers:
16 racemes were randomly selected and marked. From each raceme, the flowers that appeared on the apical part were removed and called hereafter as removal of late flowers. The raceme flowers were exposed to insect as well as wind pollination. The manipulated racemes were subsequently monitored weekly, and pod harvesting was taken later as the pods showed brown color.
Removal of late and intermediate flowers:
16 Racemes were randomly selected and marked. From each raceme, the flowers that appeared on the apical and intermediate parts were removed and called hereafter as removal of late and intermediate flowers. The manipulated racemes were subjected to the same practices as mentioned earlier.
16 Racemes were randomly selected and marked. These racemes were left without any removal of their flowers, and they served as the control. These racemes were called hereafter non removal flowers. The manipulated racemes were subjected to the same practices as mentioned earlier.
To assess self-compatibility of Ceratonia Siliqua pollen grains and to evaluate the role of insect pollinators in pod and seed set, the following treatments were conducted on Ceratonia Siliqua trees producing hermaphrodite flowers:
Self pollinated flowers:
16 Racemes were randomly selected before the flowers opened, and then were marked and covered with gauze bags (2 mm mesh size) to exclude pollinators in the field and prevent invasion of other undesirable pollen grains. The net bagging was removed from racemes 4 weeks later. The manipulated racemes were subsequently monitored weekly, and pod harvesting was taken later as the pods showed brown color and fruit and seed dry mass were measured.
Cross pollinated flowers:
16 Racemes were randomly chosen, marked, and had their flower anthers removed. Racemes were hand pollinated with pollen grains of other trees by wiping another flower with mature stamens over the stigma. Pollen supplementation was repeated twice at two days interval. The same pollen source was always used for the same tree. The manipulated racemes were subjected to the same practices as mentioned earlier.
Geitonogamy pollinated flowers:
16 Racemes, before the flowers opened, were randomly selected, then marked and had their flower anthers were removed. Racemes were hand pollinated with pollen from another raceme on the same tree. The manipulated racemes were subjected to the same practices as mentioned earlier.
16 Racemes were randomly selected and marked. These racemes were left without any additional pollen grains and they served as control. These racemes were subjected to the same practices as mentioned earlier.
Number of pods per raceme:
The number of flowers per racemes was defined by carefully counting the female flower from the selected mature racemes. The number of pods was counted directly from the mature racemes. To prevent missing fruits that could fall off the racemes and would be missing in the counting, a fruit trap (a basket made of cloth mesh held with wire) was placed directly under the racemes. Pod set ratio was estimated as the ratio of the number of pods/number of female flowers per racemes.
Pod Length and weight:
Collected pods were air dried for 4 weeks and kept at 48C[degrees] before analyses. Pod length was measured using a graduated tape. Pod weight was measured using a top-loading balance.
Seed numbers and weight per pod:
Each pod was decorticated manually by hand in laboratory and the level of seed set was recorded. 10 seeds were taken randomly for each replicate and their weight was measured using a top-loading balance.
Mature seeds were collected and tested for viability using scarification method. 30 seeds were collected randomly from each replicate. Seeds were placed in Petri dishes and left in darkness for one week. Seeds were considered viable if the germination happen.
Data were subjected to analysis of variance (ANOVA). This experiment was planed as Complete Randomized Design (CRD) with four-replications. The collected data was analyzed using SAS . Least Significant Differences (LSD) was used to compare between means of treatments at 0.05 probability level.
Results of non- removed flowers indicated that the pod set of late flowers (2.19) was significantly higher than that of intermediate (0.63) and early flowers (0.35). Furthermore, the differences between early, intermediate, and late flowers were always significant. Average percentage of matured pods of late flowers (17.95%) was also significantly higher than that of intermediate (5.21%) and early flowers (2.58 %). The removal of the late flowers significantly improved the fruit set of both the intermediate and early flowers (Table 1). The removal of late and intermediate flowers led to a marked improvement in the fruit set of early flowers (early zone flowers) compared to other treatments
Table 2 shows number of hermaphrodite flowers per raceme, average numbers of matured pods per raceme, and percentages of matured for Ceratonia Siliqua trees exposed to four pollination treatments. On average, hermaphrodite trees produced 26 female flowers per raceme. There were no significant differences in average number of matured pods per raceme, percentage of matured and aborted pods between bagged self pollinated flowers, cross pollinated flowers, Geitonogamy, and open pollinated flowers.
Table (3) shows pod length, pod weight, seeds number per pod, weight of ten seeds, and percentage of viable seeds per pod. The removal treatments as well as non- removal of flowers did not significantly increase both pod length and weight. Removal of late flowers and removal of both late and intermediate flowers produced on average 9.18 and 8.59 seeds per pods respectively, while non removed flowers produced significantly more seeds per pod (11.6 Seeds/Pod). Removal of late flowers and removal of both late and intermediate flowers treatments significantly increased 10 seeds weight (1.77 and 1.83 gm respectively) and seed germination percentage (90% and 81% respectively) as compared to non- removed flowers treatment.
Open pollination either freely or cross pollinated by hand affected some studied pod and seed characteristics (Table 4). Open pollination through cross pollinated flowers produced longer pods (13.3cm and 14.5 cm, respectively), more pod weight (9.09 gm and 9.83 gm respectively), more seeds per pod (10.9 seeds and 10.1 seeds per pod respectively) and higher seed germination percentage (82% and 94% respectively) than did self pollinated and geitonogamy flowers. Self pollinated flowers and geitonogamy flowers produced significantly higher 10 seed weight (1.55 gm and 1.52 gm respectively) as compared to cross (1.18 gm) and open pollinated flowers (1.19 gm).
Ceratonia Siliqua trees produced a high number of flowers and most of these flowers were unable to develop into a mature pod. Flowers produced at the base or in the middle part of the racemes were unable to develop into mature pods. However, those produced later at the apical of the racemes had a higher probability of setting pods. The abortion of early Agave mckelveyana flowers is an obligate result when these flowers have a pollen supplementation added . Furthermore, the fruit set in Lathyrus vernus was not improved even after outcross pollen was added to the late flowers . The arrangements of the ripe fruits observed under natural pollination were maintained under removal of early and intermediate flowers. The probability of a flower to develop into a mature pod was higher for late and intermediate flowers than for early flowers. Stephenson  reported that in many plant species the apical flowers of the raceme had a higher probability of being converted into pods than those situated closer to the base and the arrangement of the ripe fruits in the racemes followed a very well-defined pattern. The physiological background for this phenomenon is unknown .
In contrasts to such pattern of fruit, Ehrlen  and Diggle  found that a large number of Leguminosae have fruit production that is higher at the base of the inflorescence. The earlier pollination of the basal flowers, whose transformation into fruit would limit later fruit set, and on the other hand, the more favorable position of basal fruits with respect to resources [19,11].
Flower-removal experiments indicated that the pod and seed set of the left over flowers get better after the removal of early flowers from Ceratonia siliqua inflorescences. Removing late flowers significantly increase fruit set and seed production of either intermediate or early flowers. Moreover, Removal of late and intermediate flowers significantly increases the fruit set of early flowers. Medrano et al.,  and Wyatt  found that such improvement of fruit set of early flowers could be attributed to flowers order effect; that early opening flowers have basically lower maximum fruit set than late-opening flowers. This proposes that late flowers may act as ovary reserves and compete for nutrition on the same raceme . Similar results have been found in other plant species with flowers grouped into inflorescences, such as Calochortus leichtlinii, Lavandula stoechas, Lathyrus vernus, Banksia spinulosa, Prunus mahaleb and Aquilegia caerulea [17,21,13,35,15,9]. The variations in the quality of pollen arriving at flowers may responsible for variations in pod and seed set among flowers within the same inflorescences [30,19]. This variation in the quality of pollen may be due to the movement of insect pollinators, arrangement of flowers development, and to the temporal overlap of male and female opening [10,9].
Hermaphrodite trees grown in Jordan also produce a high number of flowers per raceme (26 flowers/raceme), but set very low pods even when self-pollinated with pollen on the same flower and/or the same tree or crossed with pollen from other trees. These results are in agreement with Bosch et al.,  who also found that the percentage of flowers that set fruit was the same, whether two or four single flowers were handpollinated. Moreover, hermaphrodites and female cultivars did not differ considerably in post-anthesis drop . The production of flower numbers is especially noticeable in hermaphrodite species; it is also found in species with other reproductive systems . The hermaphrodite species produce high numbers of flowers to improve the male function and , to improve the female function , to increases the attractiveness for pollinators , comprise an ovary pool against unforeseeable loss of flowers [14,15,16] and to improve plant control over the quality of its progeny .
Supplementary hand-pollinated flowers had higher pod set and seed number per pod than did open pollinated flowers, but had the same pod length and weight. It seems that during the early flowering months, the flowers received the appropriate quality and quantity of pollen. This led to the improvement of pod initiation and growth. Pollen is an important source of hormones. Its deposition on the stigma initiates ovary growth that results in a higher pod weight . Seeds most likely control fruit growth via the mobilization of nutrients required for their own growth and for the development of the surrounding fruit tissue .
Low pod numbers of supplementary and open pollinated flowers per raceme may cause a competition among ovaries for nutrients but this competition does not affect pod characteristics [3,15,20]. Both bees and supplementary hand pollination carry enough pollen to the stigma of each flower, resulting in a non-significant difference in seed number produced per pod . Failure of seed development may be due to several reasons such as the insufficient quantity of pollen on the stigma or quality restraints like lack of viability or germ inability. Also, 10-seed weight and seed viability were improved under open pollinated pollination treatments as compared to supplementary treatments. It seems that the open pollinated Ceratonia siliqua flowers received more suitable quality and quantity of pollen. If pods are initiated with suitable pollen and have a low seed number, they may have a higher growth rate and weight . Bertin  reported that unfavorable pollen sources may cause large numbers of homozygous deleterious allele combinations, resulting in many embryo abortions, which may affect their viability. Kozlowski and Pallardy reported that apple fruits containing only few seeds often fail to achieve full size and tend to be abscised early. Furthermore, there is a threshold seed number below which it is not advantageous for the plant to mature fruits. In apple, the threshold varies with the year and the number of fruits developing .
Received 25 September 2014
Received in revised form 26 October 2014
Accepted 25 November 2014
Available online 31 December 2014
The research was financially supported by the Deanship research / Jordan University of Science and Technology, Irbid, Jordan (Project no. 134/2010). Also our sincere appreciation goes to Al- Balqa Applied University, As-Salt, Jordan, for providing the laboratory facilities.
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(1) Abd Al-Majeed Al-Ghzawi, (2) shahera Zaitoun, (1) Malek Alwedyan
(1) Department of Plant Production, Faculty of Agriculture, Jordan University of Science and Technology, P. O. Box 3030, Irbid, Jordan. Mobile: 00962795289605
(2) Department of Plant Production and Protection, Faculty of Agricultural Technology, Al-Balqa' Applied University, Al-Salt, Jordan. Mobile: 00962795576112
Correspondence Author: Abd Al-Majeed Al-Ghzawi, Department of Plant Production, Faculty of Agriculture, Jordan University of Science and Technology, P. O. Box 3030, Irbid, Jordan. Mobile: 00962795289605 E-mail: firstname.lastname@example.org
Table 1: Distribution of matured pods over different racemes zones following three pollination treatments for flowers of Ceratonia Siliqua. Treatment Fruit set zone Average Average no. % of no. of of matured matured flowers/ pod/ raceme pods raceme Non- removed Late 12.2 a 2.19 a 17.95 a (Control) Intermediate 12.1 a 0.63 b 5.21 b Early 12. 0 a 0.35 b 2.92 b Remove Late Intermediate 13.07a 1.92 a 14.69 a Early 12.74a 0.69 b 5.42 b Remove Late & Early 12.56a 1.90 a 15.13 a Intermediate L S D1 ( 0.05 ) ns 0.304 4.2 LSD (0.05): Fisher's least significantly difference to compare treatment means, means not followed by same letter are significantly different at P [less than or equal to] 0.05. Table 2: Number pod per raceme, fruit matured, and fruit set following four pollination treatment in hermaphrodite flowers of Ceratonia Siliqua. Treatment Average no. Average number % of of flowers/ of matured matured raceme Pod/ raceme Pods Self pollinated 27.13 a 2.38 a 8.77 a Cross pollinated 28.06 a 1.88 a 6.70 a Geitonogamy 26.88 a 2.0 a 7.44 a Open pollinated 27.75 a 2.19 a 7.89 a LSD1 ( 0.05 ) ns ns ns LSD (0.05): Fisher's least significantly difference to compare treatment means, means not followed by same letter are significantly different at P [less than or equal to] 0.05. Table 3: The effect pollination treatment on pod and seed characteristics of Ceratonia Siliqua trees. Treatment Pod Seed characteristics characteristics Length Weight Seed No. Weight of per pod 10 seeds (cm) (g) (g) Remove Late 13.3 a 12.3a 9.18 b 1.77 a Remove of Late & Intermediate 12.6 a 10.1 a 8.59 b 1.83 a Non- removed 14.3 a 13.1 a 11.6 a 1.64 b LSD ( 0.05 ) ns ns 2.04 0.107 Treatment Viable seeds per fruit (%) Remove Late 90 a Remove of Late & Intermediate 81 a Non- removed 63 b LSD ( 0.05 ) 0.128 LSD (0.05): Fisher's least significantly difference to compare treatment means, means not followed by same letter are significantly different at P [less than or equal to] 0.05. Table 4: The effect pollination treatment on Pod and seed characteristics of hermaphrodite Ceratonia Silliqua trees. Treatment Pod Seed characteristics characteristics Length Weight Seed No. Weight of per pod 10 seeds (cm) (g) (g) Self pollinated 11.9 b 7.15 b 9.03 b 1.55 a Cross pollinated 14.5 a 9.83 a 10.1 a 1.18 b Geitonogamy pollinated 12.3 b 8.28 b 9.08 b 1.52 a Open pollinated 13.3 a 9.09 a 10.9 a 1.19 b LSD (0.05) 1.09 1.30 0.93 0.32 Treatment Seed germination (%) Self pollinated 57 b Cross pollinated 94 a Geitonogamy pollinated 64 b Open pollinated 82 a LSD (0.05) 0.13 LSD (0.05): Fisher's least significantly difference to compare treatment means, means not followed by same letter are significantly different at P [less than or equal] 0.05.
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|Author:||Ghzawi, Abd Al-Majeed Al; Zaitoun, shahera; Alwedyan, Malek|
|Publication:||Advances in Environmental Biology|
|Date:||Nov 1, 2014|
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