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MORPHOLOGICAL AND PHYSIOLOGICAL SEED CHARACTERISTICS OF TAURUS FIR (Abies cilicica /Ant. et Kotschy/Carriére) IN TURKEY
MORFOLOŠKA I FIZIOLOŠKA SVOJSTVA SJEMENA CILICIJSKE JELE (Abies cilicica /Ant. et Kotschy/Carriére) U TURSKOJ
Mustafa Yilmaz, Tefide Yüksel
Summary
Taurus fir (Abies cilicica /Ant. et Kotschy/ Carriére) is a tree species mostly found in the Taurus mountains in Turkey. The objective of this study was to determine the morphological and physiological characteristics of the seed of the Taurus fir. The seeds were collected from five different provenances of natural distribution, including Göksun, Saimbeyli, Kozan, Anamur, and Bucak. In the laboratory, for each of the different provenances, we measured the1000-seed weight; the length, width, and thickness of the seeds; and the weights of the individual seeds. The morphological characteristics of the seeds varied according to their provenances. To determine the necessary duration of pre-chilling, we attempted to germinate the seeds from each of the five different provenances, after pre-chilling at 4 °C for 0, 2, 4, and 6 weeks. We determined that the optimum pre-chilling duration was six weeks. In order to determine the optimum germination temperature, the seeds from three provenances were subjected to a germination test at each of four different temperatures (12, 16, 20, and 24 °C) after three different pre-chilling durations (2, 4, and 6 weeks). This resulted in various germination rates and speeds. The seeds germinated best at 20 °C and 24 °C.
Keywords: Abies cilicica, seed, dormancy, pre-chilling, germination
Introduction
Uvod
The Taurus Fir (Abies cilicica /Ant. et Kotschy/ Carriére), a shade-tolerant tree growing to 35 m, is found only in Turkey, Syria, and Lebanon. Their distribution is limited in Lebanon and Syria, and the largest concentration is in southern Turkey, primarily in the deep valleys and north-facing slopes of the Taurus Mountains, at elevation from 1150 m to 2000 m (Bozkuş 1988). The wood of A. cilicica has been utilized for many different purposes, including furniture, paneling, boxes, packaging, boards, and toys. The ecological amplitude of this species is comparatively limited (M’Hirit 1999). A. cilicica is represented by two subspecies (Davis 1965-1985; Yaltırık 1993): (1) A. cilicica subsp. cilicica occurs in the eastern part of its range, and it is identified by its buds, which have no resin, and by the hairy shoots it forms when young; (2) A. cilicica subsp. isaurica Coode et Cullen has glabrous shoots when young and resinous buds, and is distributed in the West Taurus (Browicz 1982).
There are about 40 species of fir, and they are generally sensitive to environmental effects (Yaltırık 1993; Edwards 2008). In recent decades, a decline in the number of fir

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species has been recorded in many locations and species throughout the northern hemisphere (Raftoyannis et al. 2008; Kvitko et al. 2011; Politi et al. 2011; Ficko et al. 2011). Loss of the Taurus Fir is also of current concern in the Taurus Mountains (Kanat and Laz 2005).
The reproductive system of the various species of Abies is generative, and the natural regeneration period depends on the production of seed, the proportion of those seeds that are sound, the germination rate, and the successful formation of seedlings (Owens and Molder 1985; Crawford and Oliver 1990; Rawat et al. 2008). Seed dormancy is very prevalent in Abies seeds, and cold-moist stratification is often applied in order to eliminate this (Gogala and Vardjan 1989; Edwards 1996; Jensen 1997). On the other hand, the correct germination temperature is generally very effective at causing germination, and a wide temperature range implies seed vigor (Grabe 1976; Yilmaz 2008).
The Taurus Fir has the largest cones and seeds among all fir trees (RBG Kew 2014), but neither the morphological nor the physiological characteristics of its seeds have been extensively studied. Understanding how the seeds of this species vary between the different provenances of this species is important both in theory and in practice.
In this study, both the morphological (length, width, thickness, and weight) and physiological (dormancy level and pretreatments) characteristics of the seed of the Taurus Fir were investigated for the seeds collected from five different provenances. The effects of temperature on the germination behavior were also checked for the seeds of three provenances.
Material and Methods
Materijali i metode
Seed materials – Sjemenski materijal
The seeds were collected from five different provenances in southern Turkey in October, 2009 (Table 1; Figure1). Of species collected at the five provenances, three of them were A. cilicica subsp. cilicica, eastern distribution, and two of them were A. cilicica subsp. isaurica Coode et Cullen, western distribution. The seeds were air dried to 6 % MC, which took about a week, and they were then refrigerated in closed bottles until used.
Measurement of morphological characteristics – Izmjera morfoloških svojstava sjemena
50 seeds from each provenance were randomly selected and measured. For each seed, four traits (length, width, thickness, and weight) were measured. 1000-seed weights were also calculated from 800 (8 × 100) seeds according to the ISTA (1996) rules.
Dormancy Level and Pretreatment Requirements – Stupanj dormantnosti i predsjetvena priprema
To find out the dormancy level and the pre-chilling requirement of the species, seeds from five different populations (Table 1) were subjected to 0 (control), 2, 4, and 6 weeks (w) pre-chilling at 4 °C. Pretreatments were applied in plastic bottles covered with perforated aluminum foil in the dark. The top of the bottle was covered with perforated aluminum foil to allow for gas exchange. During the pretreatments,

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the bottles were weighed weekly to check for altered moisture content of the seeds, and distilled water was added by spraying, if needed. The germination tests were performed on two-layered filter paper in 15-cm diameter Petri dishes with 150 (3 × 50) seeds at 20 °C. Seeds were rinsed with distilled sterile water for five minutes prior to the germination test. The seeds were considered germinated when their radicles protruded 3 mm and showed geotropism. The Petri dishes were examined every two days, and the germinated seeds were counted and removed. Germination tests were terminated on day 28.
The effects of temperature – Utjecaj temperature
To determine the effect of temperature on the germination response, seeds from 3 different provenances (Bucak, Kozan, Saimbeyli) were pre-chilled without media for 2, 4, and 6 w in a refrigerator (4 °C). Pre-chilling was applied in the plastic bottles covered with perforated aluminum foil in the dark. Seeds were subjected to germination tests at 12 °C, 16 °C, 20 °C, and 24 °C after the pre-chilling treatments.
Germination Parameters – Parametri klijanja
In the germination tests, the germination percentage (GP) and mean germination time (MGT) were calculated according to the following formulas (Bewley et al. 2013):
               
where GP (%) is the germination percentage, ni is the number of germinated seeds at week i, and N is the total number of incubated seeds per test; and
               
where MGT is the mean germination time, ti is the number of weeks from the beginning of the test, and ni is the number of germinated seeds recorded on week t(i).
Statistical Analyses – Statistička analiza
The data on seed weight, seed length, thickness, width, germination percentage, and mean germination time were analyzed using ANOVA. The treatment means were tested by Duncan’s multiple range test. The percent values (GP) were normalized by transformation by the arcsine square root (), prior to the variance analyses.
Results
Rezultati
Morphological Characteristics – Morfološka svojstva sjemena
The average 1000-seed weight for the five provenances was 169.7 g at about 6 % MC. There were significant differences between provenances in terms of seed dimensions and weights (Table 2). The average seed length, width, thickness, and weight were 14.26 mm, 7.13 mm, 4.44 mm, and 0.170 g, respectively. The weight of the seed from Bucak was distinctly heavier than those from the other provenances.
Dormancy Level and Pretreatment Requirements – Stupanj dormantnosti i predsjetvena priprema
There were apparent differences between the pre-chilling treatments in terms of the percentage of seeds that germinated at 20°C (Table 3; Figure 1). Pre-chilling treatments of 2 and 4 w were insufficient, but 6 w of pre-chilling was found to totally eliminate seed dormancy and led to the highest GP.
The average GPs were 35.6 %, 55.7 %, 63.6 %, and 79.6 % after treatment with 0-w (control), 2-w, 4-w, and 6-w pre-chilling, respectively. About half of the seeds germinated without any pre-chilling. Following the 2-w and 4-w pre-chilling durations, some of the ungerminated were found to be sound, but after the 6-w pre-chilling, the ungerminated seeds were found to be either decayed or infected.

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The dormancy level differed by provenance. The seeds from Saimbeyli reached their maximum GP after 2 w of pre-chilling, while those from the other s required about 6 w of pre-chilling for the dormancy to be completely removed. We also note that, after 6 w of pre-chilling, the GPs of the seeds from the various provenances differed.
There was a distinctive difference between the GPs for the seeds from different provenances after fully eliminating dormancy by pre-chilling for 6 w. The A. cilicica subsp. cilicica seeds from the Göksun, Saimbeyli, and Kozan provenances demonstrated the highest GPs, while the overall GPs of Anamur and Bucak (A. cilicica subsp. isaurica) were lower than those of other populations due to a lower germination potential (Table 2).
The pre-chilling duration also significantly affected the germination speed. The longer the pre-chilling period, the faster the germination occurred. Average MGT was 16.5, 13.2, 12.3, and 9.1 d at control (0-w), 2-w, 4-w, and 6-w duration of pre-chilling, respectively (Table 3). Population factor was also effective on the MGT. In general, the seeds of eastern populations (A. cilicica subsp. cilicica) germinated faster than those of western populations (A. cilicica subsp. isaurica).
The average GP and MGT for each of the five populations are clearly seen in Figure 2. With an increasing duration of pre-chilling, the average GP increases and the average MGT decreases.
Figure 3 clearly shows that the dormancy is less deep in the Saimbeyli and Göksun populations. After six weeks of pre-chilling, the germinations curves clearly fall into two groups. The eastern Taurus populations (those from Saimbeyli, Kozan, and Göksun) formed relatively similar germination curves, which show similarities in terms of the physiological characteristics of their seeds. Similarly, the western populations (Anamur and Bucak) demonstrated curves that were identical in terms of rate and speed of germination.

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Effects of temperature on the germination behavior after different durations of pre-chilling – Utjecaj temperature na klijavost sjemena nakon različitog trajanja stratifikacije
In general, the effect of temperature, the duration of pre-chilling, the provenance of the population, and their interactions affected the GP and MGT (Table 5). Both pretreatment and population significantly affected the germination percentage of A. cilicica seeds. The pretreatment × population interaction effect was also found to be significant for GP.
After different durations of pre-chilling, the Taurus fir seeds had different GPs. The highest (76.2 %) and the lowest (56.3 %) were obtained after pre-chilling for 6 w and 2 w, respectively.
On average, these three populations reached their highest germination rates at 20 °C and 24 °C; there was no significant difference between the rates of germination at 20 °C and 24 °C. Similarly, at germination temperatures of 12 °C and 16 °C, there was no statistically significant difference between the percentages of germination. The germination percentages at 12 °C and 16 °C were significantly lower than those at 20 °C and 24 °C (Table 6).
There were significant differences between provenances in terms of the overall average percentage of germination. The seeds from Saimbeyli reached the highest germination percentage (89.3 %), while the seeds with the lowest germination percentage (38.2 %) were from Bucak.
A pre-chilling interval of 4 w and 2 w seems to be sufficient for Kozan and Saimbeyli, respectively, due to the reduced depth of their dormancy. On the other hand, germination rates generally increased as the duration of pre-chilling was extended.

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The duration of pre-chilling, the temperature, the provenance of the population, and the interactions between these factors significantly affected the MGT (Table 7). The average mean germination time varied according to the different periods of pre-chilling. The lowest rate and fastest speed of germination occurred after 2-w and 6-w of pre-chilling, respectively.
In this study, we saw that temperature had a large effect on germination speed. As the temperature increased, the germination accelerated. Therefore, the lowest rate and fastest speed of germination occurred at 12 °C and 24 °C, respectively. The plotted curves (Figure 6) clearly show that germination occurs at a faster rate with increasing temperature and with increased duration of pre-chilling.
The average germination speeds also greatly varied according to the seeds’ provenances. MGTs were 7.7 d, 11.9 d, and 16.1 d for Saimbeyli, Kozan, and Bucak, respectively.
Discussion
Rasprava
Abies species demonstrate great variation in terms of seed weight. A. cilicica has the largest seeds (both in terms of weight and dimensions) among the Abies genus (Young and

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Young 1992; RBG Kew 2014). The average 1000-seed weight was 169.7 g, while that of A. sachalinensis (F. Schmidt) Mast. var. gracilis (Kom.) Farjon, the lightest seeds, was 4.2 g. In another study (Keskin and Şahin 2000), the 1000-seed weight of A. cilicica was found to be 139.1 g and 226.0 g in poor and mast seed years, respectively. The 1000-seed weight of A. nordmanniana (Steven) Spach subsp equi-trojani (Asch. et Sinb.) Coode et Cullen and A.n. subsp. bornmuelleriana (Mattf.) Coode et Cullen, other Abies taxa in Turkey, were 63.2 g (Aslan 1982) and 82.9 g (Turna et al. 2010), respectively.
There was a great variation between and within the provenances in terms of the morphological traits of the seeds. The average length, width, thickness, and weight of a seed were 14.26 mm, 7.13 mm, 4.44 mm, and 0.170 g, respectively. Similar variations are generally due to different genetic characteristics, environment, and events during the period of seed development (Leishman et al. 2000; Desai 2004).
We found that, for seed from all five provenances, 6 w of pre-chilling fully eliminated dormancy and produced an overall average germination percentage of 79.6 %. The average GP in Abies seeds is less than that of many other conifer species due to empty and insect-infected seeds (Edwards 2008). Keskin and Şahin (2000) obtained about 50 % GP at 23 °C to 25 °C in A. cilicica seeds.
The real germination capacity of the dormant seeds is generally seen after the full elimination of dormancy (Copeland and McDonald 1999; Baskin and Baskin 2001; Smith et al. 2002). After pre-chilling for 6 w, which fully removed dormancy, the provenances divided into two groups in terms of GP and germination speed (Figure 3). The average GP of A. cilicica subsp. isaurica seeds (Anamur and Bucak) was significantly lower than that of A. cilicica subsp. cilicica (Kozan, Saimbeyli, Göksun). Further research over several consecutive years is needed to determine the true differences between the two subspecies.
In general, germination accelerates with increased temperature and increased duration of pre-chilling (Edwards 2008; Yilmaz 2008 and 2010). Similarly, we found that germination speeds increased with the duration of pre-chilling and an increase in the germination temperature (Table 6, 7; Figure 4).
This study clearly revealed that the seed of A. cilicica has non-deep physiological dormancy. The fresh (no pre-chilling) seeds from the provenances of Göksun and Saimbeyli demonstrated relatively high percentages of germination. On the other hand, the GPs of non-chilled seeds from the other three provenances (Kozan, Anamur, Bucak) were very low, due to physiological dormancy. The dormancy depth changes each year depending on the timing of collecting the cones (Fenner and Thompson 2005). Since these cones were all collected late in autumn before natural dispersal, the dormancy depth may be reduced because they were still on the trees. Studies over several consecutive years of A. cilicica seeds from the same provenance are likely to give more meaningful information about the depth of dormancy.
The duration of pre-chilling necessary to fully remove dormancy varied by the provenances. Although 2 w pre-chilling was sufficient for the seeds from Saimbeyli, the seeds from Kozan required 4 w pre-chilling to achieve full elimination of dormancy. Seeds from the other three provenances required 6 w of pre-chilling to attain full removal of dormancy. Based on the results of these five provenances, pre-chilling for 4 w to 6 w can be recommended for A. cilicica seeds; this is in agreement with the average pre-chilling requirement of Abies seeds, 4 w to 8 w (Gosling 1999;

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Edwards 2008; RBG Kew 2014). A. cilicica seeds can germinate at low temperatures either on or under snow (Irmak 1961; Avsar and Ayyıldız 2004) or during the pre-chilling process in a refrigerator (4 °C). In order to avoid pregermination during the pre-chilling, the moisture content of the seeds can be lowered to about 85 % to 90 % of the maximum level, which is enough for the pre-chilling process but the shortage of moisture prevents germination (Suszka et al. 1996; Poulsen 1996).
Germination temperatures greatly affect the germination parameters (Schmidt 2000). In this study, the seeds of A. cilicica from all three provenances demonstrated better germination performance (germination percentage and germination speed) at 20 °C and 24 °C. The range of the germination temperature widens after dormancy is removed (Yilmaz 2008). Similarly, after 4 w or 6 w of pre-chilling, higher GPs occurred at 12 °C and 16 °C. In general, 20 °C and 24 °C seem to be the most appropriate temperatures for A. cilicica seeds. Where there is a risk of fungal infection, 20 °C is preferred.
The natural distribution of A. cilicica is primarily in Turkey, and this species is one of the important species in Turkish forests. However, in recent decades, many individuals of this species have been dying off. Abies species are generally very susceptible to climate change and environmental stress. Moreover, widespread insect attacks have been observed on A. cilicica in the past decades. Therefore, future research on the seed storage and raising of A. cilicica is very important for the ex-situ conservation of the species.
Conclusions
Zaključci
A. cilicica is mainly distributed in Turkey. The species has the largest seeds both in terms of weight and dimensions among Abies species. The average 1000-seed weight, seed length, width, and thickness were 169.7 g, 14.26 mm, 7.13 mm, and 4.44 mm, respectively. The study demonstrated that the seed of A. cilicica has non-deep physiological dormancy. The seed required about 2–6 w of pre-chilling for dormancy removal depending on the provenances. The overall average germination percentage was 79.6 %. The seeds presented better germination performance at 20 °C and 24 °C and 20 °C should be preferred due to fungal infection risk at 24 °C. The average GP of A. cilicica subsp. isaurica seeds was surprisingly lower than that of A. cilicica subsp. cilicica. Further research over several consecutive years is recommended to conclude differences between the two subspecies. The studies on the storage of A. cilicica seeds are also needed for the ex-situ conservation of the species.
Acknowledgment
Zahvala
This study was supported by Kahramanmaras Sutcuimam University Scientific Research Unit, Project number: 2010/1-1M.

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Sažetak
Cilicijska jela (Abies cilicica /Ant. et Kotschy/ Carriére) vrsta je koju u Turskoj nalazimo uglavnom u gorju Taurus. Cilj istraživanja bio je odrediti morfološka i fiziološka svojstva sjemena taurske jele. Sjeme je sakupljano sa pet različitih područja njena prirodnog rasprostranjenja, kako slijedi: Göksun, Saimbeyli, Kozan, Anamur, and Bucak. Na uzorku svake od pet provenijencija u laboratoriju je mjerena: težina 1000 sjemenki, duljina, širina i debljina sjemena i težina pojedinačne sjemenke. Morfološki parametri pokazali su određeni stupanj varijacije u odnosu na uzorkovane provenijencije. Da bi se odredilo potrebno vrijeme stratifikacije, naklijavano je sjeme testiranih provenijencija nakon stratifikacije od 2, 4 i 6 tjedana pri temperaturi od 4 °C. Sjeme je potom stavljano u klijalice u 4 različita temperaturna režima (12, 16, 20, and 24 °C). Rezultati su bili različiti u smislu klijavosti i brzine klijanja. Najbolja klijavost postignuta je pri temperaturama od 20 i 24 °C.
Ključne riječi: Abies cilicica, sjeme, dormantnost, stratifikacija, klijanje