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Ecology |
2School of Biological Sciences, University of Kentucky, Lexington, Kentucky 40506-0225 USA 3Fakultas MIPA, Universitas Bengkulu, Bengkulu 38371, Indonesia 4Department of Agronomy, University of Kentucky, Lexington, Kentucky 40546-0091 USA
Received for publication March 30, 2000. Accepted for publication February 8, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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autumn winter spring sequence of temperature regimes germinated, whereas none of those subjected to a winter spring sequence did so. That is, cold stratification is effective in breaking dormancy only after seeds first are exposed to a period of warm temperatures. Likewise, embryos grew at cold temperatures only after seeds were exposed to warm temperatures. Thus, the seeds of S. orbiculatus have nondeep complex morphophysiological dormancy. As a result of dispersal phenology and dormancy-breaking requirements, in nature most seeds that germinate do so the second spring following maturity; a low to moderate percentage of the seeds may germinate the third spring. Seeds can germinate to high percentages under Quercus leaf litter and while buried in soil; they have little or no potential to form a long-lived soil seed bank.
Key Words: Caprifoliaceae • cold stratification • germination phenology • imbibition curve • morphophysiological seed dormancy • Symphoricarpos orbiculatus • warm stratification
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). These are distinguished on the bases of (1) permeability or impermeability of the seed (or fruit) coat to water, (2) whether the embryo is fully developed or underdeveloped at seed maturity, and (3) whether the embryo is physiologically dormant or nondormant (Nikolaeva, 1977
; Baskin and Baskin, 1998
). Although the seed germination biology of many plant species has been investigated (Nikolaeva, Rasumova, and Gladkova, 1985
; Baskin and Baskin, 1998
), much confusion remains concerning the type of dormancy found in some genera. A case in point is the genus Symphoricarpos.
Symphoricarpos belongs to the Caprifoliaceae, a family with underdeveloped embryos that must grow before germination can occur. According to Martin (1946)
, seeds (true seed plus endocarp, see below) of species in this genus have linear embryos that do not extend the full length of the seed; they are underdeveloped. Previous studies on various taxa of Symphoricarpos, reviewed below, suggest that the embryo is dormant at maturity and that it requires warm stratification (or soaking in concentrated sulfuric acid) followed by cold stratification for dormancy break and growth (Flemion, 1934
; Flemion and Parker, 1942
; Pelton, 1953
). This type of dormancy in which the embryo is both physiologically dormant and underdeveloped is called morphophysiological dormancy (MPD). Yet, studies on the same species also state that the seed and/or fruit coat(s) is (are) impermeable to water (Pfeiffer, 1934
; Flemion and Parker, 1942
; Evans, 1974
), i.e., the seeds have physical dormancy (PY). However, a combination of MPD and PY is not known to occur in seeds (Baskin, Baskin, and Li, 2000)
. Unfortunately, previous studies have not fully characterized the seed biology of any Symphoricarpos species. Thus, it is unclear what type of seed dormancy occurs in the genus.
In a previous study, seeds of S. racemosus var. laevigatus (S. albus var. laevigatus) and S. racemosus (S. albus var. albus) overwintered out-of-doors did not germinate in the first spring; however, 50% of them germinated the second spring (Pammel and King, 1924
; Adams, 1927
). Seeds sown in a greenhouse (not subjected to cold winter temperatures) failed to germinate in both the first and second springs (Adams, 1927
). In laboratory experiments, nontreated seeds of S. racemosus kept at various temperatures up to 4 yr germinated to a maximum of only 10% (Flemion, 1934
). However, a treatment consisting of a sequence of (1) soaking seeds in concentrated sulfuric acid for various lengths of time, (2) keeping them for 2–4 wk at 25°–30°C, and (3) placing them at 5°C for several months resulted in up to 90% germination (Flemion, 1934
). More recently, Piper (1986)
obtained only 16–18% germination in seeds of S. albus var. laevigatus kept at 5°C for 500 d and Gilbert (1995)
failed to get any seeds of this species to germinate after various treatments.
Seeds of S. orbiculatus sown in autumn and overwintered out-of-doors in Iowa did not germinate the first spring, whereas up to 90% of them did so the second spring. However, seeds sown in summer germinated in both the first and second springs (Pammel and King, 1924
; Flemion and Parker, 1942
). In laboratory studies, a maximum of 74% germination was obtained during incubation at 10°C for 5 yr, but only 10% germination at 1°, 5°, 15°, and 20°C. On the other hand, seeds given warm followed by cold stratification or pretreated with concentrated sulfuric acid prior to the stratification treatments germinated to 58–72% (Flemion and Parker, 1942
).
Pelton (1953)
demonstrated that the dormancy-breaking requirements of S. occidentalis are similar to those reported for S. racemosus and S. orbiculatus. Thus, seeds of S. occidentalis must be soaked in concentrated sulfuric acid or given warm followed by cold stratification to come out of dormancy. Further, he showed that low temperatures favor germination of nondormant seeds of this species.
In these studies, embryos in intact seeds of S. racemosus (Flemion, 1934
), S. orbiculatus (Flemion and Parker, 1942
), and S. occidentalis (Pelton, 1953
) grew only during the low temperature phase of the dormancy-breaking protocol, i.e., after the seeds first were given a warm moist temperature treatment and/or soaked in concentrated sulfuric acid. Thus, seeds of these three species have MPD of the nondeep complex type (sensu Nikolaeva, 1977
; Baskin and Baskin, 1998
). On the other hand, the seed and/or fruit coats of the three species have been reported to be impermeable to water. Specifically, the "seed coat" (apparently true seed coat–endocarp complex) (Flemion and Parker, 1942
), endocarp (Evans, 1974
), and true seed coat (Pfeiffer, 1934
) have been suggested to be impermeable. Thus, seeds of Symphoricarpos also might be physically dormant and require a treatment (such as acid scarification) to make them permeable.
The overall objective of this study was to more fully characterize the ecological aspects of the germination biology of S. orbiculatus Moench [S. symphoricarpos (L.) MacM.] than heretofore has been done for any species in the genus. Specifically, the study determined (1) whether the seed and/or fruit coats are water impermeable, (2) the temperature requirements for dormancy break and embryo growth, (3) the effect of gibberellic acid on germination and embryo growth, and (4) the phenology of both seed germination and embryo growth under near-natural temperature regimes. This is the first study to investigate all four of these aspects of the germination biology in a species of Symphoricarpos.
There are 
15–17 species of Symphoricarpos in North America and one species in China (Mabberley, 1997
). Like other species of the genus (Pelton, 1953
; Gilbert, 1995
), S. orbiculatus is a deciduous nanophanerophyte (small shrub) (Gibson, 1961
) that reproduces extensively by rhizomes (Aldous, 1935
; GPFA, 1986
). The geographical range of the species is from Connecticut to Florida, west to South Dakota, Colorado, and northern Mexico (Jones, 1940
; Steyermark, 1963
; Ferguson, 1966
; GPFA, 1986
; Gleason and Cronquist, 1991
). General types of habitats described for the species include disturbed and/or second growth upland and lowland woodlands, woodland margins, pastures, dry or rocky soil, ravines, and stream banks. Symphoricarpos orbiculatus is an important shrub in the middle to late stages of primary succession in limestone (cedar) glades of middle Tennessee, i.e., glade shrub red cedar/shrub red cedar forest red cedar/hardwood forest (Quarterman, 1950
). Voss (1996)
reported that in Michigan, where the species is not native, it apparently has escaped from cultivation to various types of disturbed habitats such as railroad embankments and roadsides. In the Chicago, Illinois, region (not native), it has escaped to disturbed wooded areas including a wooded floodplain (Swink and Wilhelm, 1979
). It is "... a native species often cultivated and widely escaped ..." in West Virginia (Strausbaugh and Core, 1978
).
Fruits of S. orbiculatus mature in September and are dispersed from late autumn to the following spring (Jones, 1940
; Evans, 1974
; S. N. Hidayati, personal observation). The fruit is a drupe (Pfeiffer, 1934
; Fukuoka, 1972
), consisting of a fleshy exocarp and mesocarp and a hard, fibrous endocarp that is united permanently with the seed coat (Pfeiffer, 1934
) (Fig. 1). Thus, the word "seed" in this paper refers to the true seed plus endocarp, which is the germination unit in Symphoricarpos. Each fruit usually has two fertile seeds that are convex on one side and almost flat on the other. Symphoricarpos orbiculatus is the only taxon in the genus with red fruits.
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; Kartesz, 1994
). Thus, currently accepted nomenclature for species mentioned in this study includes S. albus var. albus, S. albus var. laevigatus, S. mollis, S. occidentalis, and S. orbiculatus. |
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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50 plants of S. orbiculatus at Camp Nelson, Jessamine County, Kentucky, USA. At the time of collection, fruits were ripe and purplish or dark red. After each collection date, seeds were separated from the pulp (exocarp and mesocarp) and allowed to dry in the laboratory for 3–5 d before studies were initiated.
Imbibition
Rate of water uptake was monitored for scarified and for nonscarified seeds (1996 collection). Three replications each of 100 scarified (individually with a single-edge razor blade) and of 100 nonscarified seeds were placed on Whatman Number 1 filter paper moistened with distilled water in 9-cm diameter glass petri dishes and kept in the laboratory at room temperature, 23°C. Initial (to) seed mass was determined for air-dried seeds that had been wetted for 2 min, blotted dry, and weighed to the nearest 0.1 mg. Thereafter, following this procedure, seed mass was determined at 1-h intervals for the first 12 h, and then every 24 h for the next 156 h. Percentage water uptake was calculated as actual increase in seed mass based on seed mass at to:
 | (1) |
Increase in mass of the seed plus endocarp germination unit may not necessarily indicate that water has penetrated the seed coat. It seems logical that water could be imbibed only by the fibrous endocarp (e.g., see Pfeiffer, 1934
), which would increase seed mass, thus giving the false impression that it had entered into the seed. Thus, to determine whether water actually penetrates into the seed, a free-hand longitudinal section was made of several seeds (using a razor blade) that had been soaked in Amann's solution (lactophenol with cotton blue) (Gurr, 1965
) for 2 d or for 2 wk. These sections were checked for staining of endosperm and embryo under a microscope at a magnification of 100x.
Germination studies
Freshly matured seeds (i.e., seeds recently removed from pulp) were placed on moist soil in 5.5-cm diameter plastic petri dishes; three replications of 50 seeds each were used for each test condition. Soil used was a 3 : 1 (v/v) mixture of limestone-derived soil and river sand. All dishes were wrapped with plastic film to restrict water loss during incubation and stratification.
Experiments were conducted in temperature- and light-controlled incubators and in a refrigerator. The incubators were set at 12:12 h daily alternating thermoperiods of 15°/6°, 20°/10°, 25°/15°, 30°/15°, and 35°/20°C. These thermoperiods approximate mean daily maximum and minimum monthly air temperatures in Kentucky and adjacent states (Wallis, 1977
): March and November, 15°/6°; April and October, 20°/10°; May, 25°/15°; June and September, 30°/15°; and July and August, 35°/20°C. The daily photoperiod in the incubators was 14 h, extending from 1 h before the beginning of the high-temperature period to 1 h after the beginning of the low-temperature period. The refrigerator was set at a constant temperature of 5°C. Cool white fluorescent tubes, which produced a photon flux density at seed level of 40 µmol·m–2·sec–1, 400–700 nm, were used as the light source in the incubators (20 W) and in the refrigerator (15 W). The 25°/15°C thermoperiod was used for warm stratification and 5°C for cold stratification, since they are near optimal for many species whose seeds require warm or cold temperatures, respectively, to come out of dormancy (Stokes, 1965
; Nikolaeva, 1969
).
Protrusion of the radicle was the criterion for germination. Nongerminated seeds were checked under a dissecting microscope at the end of the experiment to determine whether the embryos were white and firm, indicating viability, or whether they were brown and soft, indicating nonviability. A tetrazolium test (Grabe, 1970
) confirmed that white embryos were alive and that brown (even light brown) ones were not.
Initial germination experiments
In the first experiment, the effect of warm or cold stratification on germination of 1996 collected seeds was evaluated. Seeds were warm or cold stratified in light for 0, 2, 4, 6, 8, 10, or 12 wk and then incubated in light at the five thermoperiods for 2 wk. The control for the stratification treatments was nonstratified seeds incubated in light at each thermoperiod for 14 wk. In the second experiment, the effect of warm followed by cold stratification or of cold followed by warm stratification on germination of 1996 collected seeds was determined. Seeds were warm (or cold) stratified in light for 12 wk and then cold (or warm) stratified in light for 0, 2, 4, 6, 8, 10, or 12 wk, after which they were incubated at the five thermoperiods for 2 wk. The control for the stratification treatments was nonstratified seeds incubated in light at each thermoperiod for 26 wk. Seeds in the controls were examined for germination at 2-wk intervals for the duration of the studies. Water was added as needed to the dishes.
Effect of gibberellic acid (GA3) on germination and embryo growth
Fifty seeds collected in 1996 were placed on two sheets of Whatman Number 1 filter paper in each of 25 9-cm diameter glass petri dishes. The paper was moistened with distilled water or with 10, 100, or 1000 mg/L gibberellic acid (GA3), as potassium salt, dissolved in distilled water. For germination, three dishes (replicates) of 50 seeds each were used for the distilled water control and for each of the three concentrations of GA3. These 12 dishes were checked for germination after incubation in light for 2, 6, and 12 wk. For embryo growth, length was determined for embryos dissected from 50 seeds (one dish) that had been incubated in distilled water and in each of the three concentrations of GA3 for 2, 6, and 12 wk (12 dishes total). Finally, initial embryo length (0 wk) for the control and for the three concentrations of GA3 is based on 50 embryos dissected from seeds (one dish) that had been kept on moist filter paper at room temperature (23°C) for 24 h. Dishes were wrapped with plastic film to retard loss of water and then incubated in light at 25°/15°C.
Effect of simulated sequence of seasonal temperature regimes on embryo growth, dormancy break, and germination
The purpose of this experiment was to monitor germination and embryo growth of seeds (1996 collection) in a simulated sequence of natural seasonal temperature regimes following dispersal in the field. The sequence began with either cold (5°C) or warm (25°/15°C) temperatures (Table 1). Dishes were monitored for germination at 2-wk intervals throughout the experiment, at which times any seedlings present were counted and discarded. Embryo growth also was monitored in seeds during incubation in this sequence of temperature regimes. Initial lengths were determined for embryos in 50 freshly matured seeds that had been incubated on moist filter paper at room temperature (23°C) for 24 h. The mean of these measurements served as the embryo length at time 0 for the two treatments and for the four controls. Thereafter, in each of the two treatments (Table 1) lengths of 50 embryos were measured at the end of each temperature regime in the sequence, whereas in each of the four controls embryo lengths were measured only at the end of 36 wk.
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23°C, relative humidity 50–60%). Three replications of 300 seeds of each collection were placed on soil in 20 x 30 x 9 cm metal flats and covered with dead oak (Quercus) leaves. Soil used was a 3 : 1 (v/v) mixture of limestone-derived top soil and river sand. The flats were placed in a nontemperature-controlled greenhouse (i.e., no heating or air conditioning, windows kept open all year). At weekly intervals, leaves were lifted, and seedlings, if present, were counted and removed from the flats. During summer (1 May–31 August), soil in the flats was watered once each week, and during the remainder of the year it was watered daily unless frozen. Temperatures in this greenhouse are near those outdoors throughout the year in the Lexington, Kentucky, area (Baskin and Baskin, 1985
). Continuous thermograph records were made inside a weather instrument shelter in the greenhouse, and mean maximum and mean minimum temperatures for each week of the studies were calculated from them. Unpublished data on the germination phenology of seeds of S. orbiculatus collected from Raven Run Nature Sanctuary, Fayette County, Kentucky, on 4 December 1977 and on 8 April 1979 by C. C. and J. M. Baskin are included (Table 2). Seeds collected in 1977 were sown on 5 December 1977 and those collected in 1979 on 9 April 1979. Data were obtained using the same methods and the same nonheated greenhouse as used for germination phenology studies of seeds collected in 1995 and in 1996.
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7 cm deep in a portion of a natural population of S. orbiculatus in the Raven Run Nature Sanctuary, Fayette County, Kentucky. One bag of seeds each from the greenhouse and Raven Run was chosen randomly and exhumed on the first day of March, May, September, and December 1997 and of March and May 1998. For each exhumation date, the bag of seeds was cut open and germinated (seedlings) and nongerminated seeds were counted. The study was terminated when all bags had been exhumed, in May 1998.
Statistical analyses
Means and standard errors were calculated for germination percentages (based on numbers of viable seeds) and for embryo lengths. Means were compared by analyses of variance (ANOVAs) and by protected least significant difference tests (PLSDs, P = 0.05) (SAS, 1985
). A one-way ANOVA was used to test the effect of the sequence of temperature regimes on germination percentages and on embryo growth, and a two-way ANOVA was used to test the effects and interaction of GA3 concentration and length of incubation on embryo growth. The square root of the percentage of germination was arcsine-transformed for analyses.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Initial germination experiments
No freshly matured seeds germinated during 2 wk of incubation in light. Further, no seeds germinated during 2 wk of incubation at 15°/6°–35°/20°C following cold, warm, cold plus warm, or warm plus cold stratification.
Effect of GA3 on germination and embryo growth
No seeds germinated in any of the three treatments or in the control during 12 wk of incubation at 25°/15°C in light (Table 3). Gibberellic acid also did not have much effect on embryo growth, although GA3 concentration, incubation length, and their interaction were significant (P 
0.0021). Maximum embryo length attained was 0.69 ± 0.01 mm (mean ± 1 SE) after 12 wk of incubation in 1000 mg/L GA3 at 25°/15°C (Table 3). Thus, embryo length increased only 21%.
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100% between seed maturity and germination (Fig. 3).
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20°/10°C (4 wk) 15°/6°C (4 wk) 5°C (12 wk) 15°/6°C (4 wk), and then 100% of the seeds germinated at 15°/6°C (Fig. 3a). In contrast, seeds placed initially at 5°C did not germinate until after they were exposed to the sequence of temperatures: 5°C (12 wk) 15°/6°C (4 wk) 20°/10°C (4 wk) 25°/15°C (12 wk) 20°/10°C (4 wk) 15°/6°C (4 wk) 5°C (12 wk) 15°/6°C (4 wk) 20°/10°C (4 wk), and then they germinated to 96% at 20°/10°C (Fig. 3b). No seeds germinated in any of the four controls.
Phenology of germination
The previously unpublished data from a study on the germination phenology of S. orbiculatus by C. C. and J. M. Baskin show that seeds of this species sown in December 1977 germinated in spring 1979, while those sown in April 1979 germinated in spring 1980 and in spring 1981 (Table 2). In the present study, seeds sown in December 1995 and in March 1996 did not germinate until spring 1997 and spring 1998 (Table 2). The same pattern occurred for seeds sown in December 1996 and in March 1997, except that no additional seeds germinated in the third spring after sowing.
A few seeds sown in the greenhouse in December 1996 and in March 1997 germinated in early March 1998 (Fig. 4). However, peak germination for seeds sown in March 1997 occurred between 15 and 23 March 1998, when mean weekly maximum and minimum temperatures were 12.1° and 6.2°C, respectively, and for those sown in December 1996 between 8 and 15 April 1998, when mean weekly maximum and minimum temperatures were 17.9° and 7.6°C, respectively.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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spring summer autumn winter spring, or of spring summer autumn winter spring conditions. Those that germinate the third year after maturity are exposed to a sequence of one additional seasonal cycle condition. In contrast to the short-term retention of the fruits on plants of S. orbiculatus in the field, some fruits of S. occidentalis may not fall from the shrubs until the fourth year after they mature, during which time "...the nutlets remain very dormant ...", (Pelton, 1953
). According to Gilbert (1995)
fruits on plants of S. albus var. laevigatus in Sheffield, England (introduced here) are dispersed from the time of maturity in August until the following January. In S. orbiculatus, 100% of the seeds collected from plants in autumn/winter were viable, whereas only 55% of those collected in spring were alive (S. N. Hidayati, personal observation).
The reason that seeds of S. orbiculatus do not germinate until the second year is that they must be exposed to warm summer followed by cold winter temperatures. However, neither 12 wk warm or 12 wk cold stratification alone nor 12 wk cold plus 12 wk warm or 12 wk warm plus 12 wk cold stratification broke dormancy in this species. Thus, none of the seeds subjected to any of these four treatments germinated after 2 wk of incubation over the 15°/6°–35°/20°C range of temperature regimes. On the other hand, seeds exposed to the sequence of 12 wk at 25°/15°C 4 wk at 20°/10°C 4 wk at 15°/6°C 12 wk at 5°C came out of dormancy and germinated to 100% at simulated early spring (March, 15°/6°C) temperatures (Fig. 3a). Apparently, seeds given 12 wk warm plus 12 wk cold stratification did not germinate at any of the five incubation regimes because they were not kept at low temperatures for a long-enough period of time for the embryos to become fully elongated. In a study by Flemion and Parker (1942)
, seeds of S. orbiculatus kept in a moist medium at 25°C for 12 or 16 wk and then transferred to 5° or 10°C for 6 mo germinated (at 5° or 10°C) to 72%.
Cold stratifying seeds at 5°C without first giving them a warm stratification treatment had no effect on either embryo growth or seed germination (Fig. 3b). Only after the seeds received a sequence of warm and cold stratification and then were transferred to a simulated spring temperature regime did they germinate, to 96% at simulated spring (April, 20°/10°C) temperatures (Fig. 3b). On the other hand, none of the seeds of this species kept continuously on a moist substrate at 5°, 15°/6°, 20°/10°, or 25°/15°C had geminated after 56 wk (see Table 1). A warm cold temperature sequence previously has been shown to be required to overcome dormancy in seeds of S. racemosus (Flemion, 1934
), S. orbiculatus (Flemion and Parker, 1942
), and S. occidentalis (Pelton, 1953
). However, Flemion and Parker (1942)
also reported that S. orbiculatus seeds eventually will germinate to fairly high percentages, without a warm treatment, if kept continuously at 10°C for a long period of time in moist peat moss.
Seeds of S. orbiculatus have underdeveloped linear embryos (Martin, 1946
) that must grow before they can germinate. The embryo is 25% of the length of the seed at maturity. Rate of embryo growth in seeds receiving a warm (25°/15°C) stratification period increased after they were transferred to 20°/10°C and then to lower temperatures in the sequence (Fig. 3a). In contrast, embryo length did not increase (or increased, very little) in seeds receiving a cold stratification period until after they were given a warm and then a second cold stratification period followed by 15°/6°C and 20°/10°C (Fig. 3b). A requirement for a warm treatment before exposure of seeds to low temperatures previously has been shown to be required for embryo growth in S. orbiculatus (Flemion and Parker, 1942
), S. racemosus (Flemion, 1934
), and S. occidentalis (Pelton, 1953
). However, none of these studies monitored the phenology of embryo growth.
It seems that a warm followed by a cold treatment may be a general requirement for breaking dormancy in seeds in S. orbiculatus over its geographic range. Seeds collected in New York (Flemion and Parker, 1942
), Kentucky (this study), and Tennessee (S. N. Hidayati, unpublished data) required exposure to a warm cold temperature sequence before they germinated. In the case of the unpublished data of Hidayati, no seeds of S. orbiculatus collected in Lewis County, Tennessee, and planted in the nonheated greenhouse in Lexington, Kentucky, in early November 1996 germinated until spring 1998; 301 of 900 (33%) seeds germinated. No additional seeds of this seed lot germinated in spring 1999 or in spring 2000.
Gibberellic acid has been used in attempts to promote germination of seeds with MPD, and its effects vary with the type of MPD (Baskin and Baskin, 1998
). Regardless of the GA3 concentrations in which seeds of S. orbiculatus were incubated, they failed to germinate after 12 wk at 25°/15°C in light, and embryos grew very little (Table 3). Thus, since seeds of S. orbiculatus (1) have underdeveloped embryos that grow only at cold temperatures, (2) require warm plus cold stratification for dormancy break, and (3) do not come out of dormancy with GA3 treatment, they have nondeep complex MPD (Nikolaeva, 1977
; Baskin and Baskin, 1998
).
Seeds of other members of the Caprifoliaceae have MPD, but of a different type. Those of Lonicera fragrantissima, Sambucus canadensis, and S. pubens have deep simple MPD; they require warm plus cold stratification to come out of dormancy, and embryos grow better at warm than at cold temperatures. In contrast, seeds of L. japonica and S. racemosa require cold stratification only to come out of dormancy, and embryos require cold temperatures for growth; thus, they have intermediate complex MPD (Hidayati, Baskin, and Baskin, 2000a, b
). A portion of the seeds of Diervilla lonicera (Hidayati, Baskin, and Baskin, 2000c)
, L. maackii, and L. morrowii (Hidayati, Baskin, and Baskin, 2000b)
has morphological dormancy and another portion has nondeep simple MPD.
Both the endocarp (Flemion and Parker, 1942
; Evans, 1974
) and true seed coat (Pfeiffer, 1934
) of Symphoricarpos species have been reported to be impermeable to water. The apparent reason for ascribing water impermeability to the seed coat–endocarp complex in this genus is that the first phase of dormancy-breaking requirements can be accomplished either by keeping seeds for 2–3 mo in a warm, moist medium or by soaking them in concentrated sulfuric acid for 30 min–1 h. These results have been interpreted to mean that the seed-covering layers are water impermeable and thus are rendered permeable by fungal action during warm, moist storage and by concentrated sulfuric acid during soaking (Flemion and Parker, 1942
; Pelton, 1953
; Evans, 1974
).
Nontreated seeds (true seed plus endocarp) of S. racemosus took up 30% moisture, and seeds kept for 4 mo in a moist medium at 25°C or soaked in concentrated sulfuric acid for 75 min and then kept in moist peat moss at 5°C for 2.3 mo took up 40% moisture (dry seeds had a moisture content of 4.7%) (Flemion, 1934
). However, in the same paper Flemion says that, "In order to induce germination in seeds of S. racemosus it is necessary that the seed coat be disintegrated." Flemion (1934)
referred to "an inhibiting effect of the seed coat" but does not say that the seed is water impermeable. However, Flemion and Parker (1942)
stated that dormancy in seeds of S. orbiculatus is due to hard impermeable seed coat (apparently referring to true seed coat plus endocarp) and to dormancy of the embryo, which is similar to the type of dormancy in seeds of S. racemosus.
Pfeiffer (1934)
noted that there is a break (gap) in the fibrous layers in the placental region of the endocarp of S. racemosus (Fig. 1). Further, she stated that the fibrous layers of the true seed coat are permeable to water, but that the inner cuticle is impermeable, thus inhibiting penetration of water through the seed coat and into the endosperm. In her study, a dilute solution of methylene blue did not penetrate through the true seed coat of seeds soaked in it for a maximum time of 2 d. Pfeiffer found that the fibrous endocarp of seeds kept in moist peat moss at high temperatures (25° or 30°C) were invaded by fungi, and the cell walls of the fibrous endocarp became thinner and softer. In contrast, fungi did not invade the endocarp of seeds kept at 5°C, and thus the endocarp did not soften. Pfeiffer (1934)
concluded that, prior to its decomposition, the endocarp prevents germination by acting as a mechanical (and not a water impermeable) barrier.
A major disagreement we have with this mechanical barrier model for seeds of Symphoricarpos is because the endocarp does not disintegrate during the process of embryo growth and radicle emergence. Mechanical dormancy, which Baskin and Baskin (1998)
view as a component of physiological dormancy, is caused by the resistance of the seed covering layers to embryo expansion and thus to germination. When the embryo becomes fully nondormant, it can exert enough force to break through the mechanical barrier. Thus, it seems unlikely that the endocarp of Symphoricarpos seeds is acting as a mechanical barrier to embryo growth and germination. Moreover, the endocarp of seeds of S. orbiculatus subjected to the simulated sequence of seasonal temperature regimes (Fig. 3) did not appear to soften or disintegrate during the high-temperature (25°/15°C) phase of dormancy break. The seeds (true seed plus endocarp) remained firm throughout the high (and low) temperature regimes in the sequence (S. N. Hidayati, personal observation).
Pelton (1953)
summarized the results of studies on seed dormancy in S. racemosus (Flemion, 1934
; Pfeiffer, 1934
) and in S. orbiculatus (Flemion and Parker, 1942
) clearly and succinctly. Thus, "Both of these species have a double dormancy requiring for germination both a breakdown of the mechanically restricting endocarp and impermeable integument, and the afterripening and development of the minute embryo" (Pelton, 1953
). However, obviously, seeds of S. orbiculatus are not water impermeable. Initially air-dry intact (nonscarified) seeds of this species kept on a moist substrate for 7 d imbibed water equal to 35% of their air-dry mass, and there was no difference in water uptake between mechanically scarified and nonscarified seeds (Fig. 2). Further, Amann's solution readily entered the seeds via the seed coat in the placental region. And finally, neither the seed coat nor the endocarp of Symphoricarpos has the correct anatomy to be impermeable to water. That is, the water-impermeable palisade layer found either in the true seed coat or pericarp of the germination unit of species with physical dormancy (Baskin and Baskin, 1998
; Baskin, Baskin, and Li, 2000
) is not present in those of the germination unit of Symphoricarpos (Pfeiffer, 1934
). Thus, seeds (true seed plus endocarp) of S. orbiculatus do not require a scarification pretreatment to imbibe water, unlike those of species with water-impermeable seed (or fruit) coats, i.e., physical dormancy (Baskin and Baskin, 1998
; Baskin, Baskin, and Li, 2000
). In fact, no taxon of Caprifoliaceae is known to have physical dormancy (Baskin and Baskin, 1998
; Baskin, Baskin, and Li, 2000
).
Seeds of S. orbiculatus have a long dispersal/dormancy-breaking period. Seeds collected and sown in December or in March/April did not germinate the first spring following sowing (dispersal), but were delayed in germinating until either the second or third spring (Table 2). The germination season extended from late February to late April (Fig. 4). Investigations on S. orbiculatus (Flemion and Parker, 1942
) and on S. racemosus (Adams, 1927
) found that seeds sown out-of-doors in September or November did not germinate the first spring but did so the second spring. On the other hand, seeds of S. orbiculatus sown out-of-doors during June or August germinated in both the first and second springs (Flemion and Parker, 1942
). Moreover, seeds of S. racemosus sown in a greenhouse (not subjected to cold winter temperatures) failed to germinate (Adams, 1927
). Apparently, seeds sown out-of-doors received enough exposure to warm temperatures to complete the first part of the dormancy breaking process before they were exposed to cold winter temperatures. In contrast, those planted in the greenhouse were not exposed to the warm plus cold temperature sequence required to break dormancy, and thus they failed to germinate.
In spite of a long dormancy-breaking period, S. orbiculatus seeds do not appear to remain viable beyond the third spring after dispersal. Seeds sown in winter 1977, winter 1995, or spring 1996 did not survive beyond the third germination season, and those sown in winter 1996 or spring 1997 did not survive beyond the second germination season (Table 2). Moreover, seeds of S. orbiculatus germinated to high percentages under Quercus leaf litter and while buried in soil (Fig. 3). Thus, S. orbiculatus seeds apparently do not form a long-lived soil seed bank. Pelton (1953)
also concluded that S. occidentalis did not form a long lived soil seed bank. Morgan and Neuenschwander (1987)
found a large seed bank (mean ± 1 SD = 247 ± 427 seeds/m2) for S. mollis and a small one (3 ± 13 seeds/m2) for S. albus (var. laevigatus ?) in soil samples taken in uncut 70-yr-old mixed-conifer stands in Idaho. However, they believed that the seeds probably had been produced recently by fruiting of these two understory shrubs.
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FOOTNOTES |
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5 Author for reprint requests, current address: Department of Biology, P.O. Box 60, Middle Tennessee State University, Murfreesboro, Tennessee 37132 USA (snhida{at}hotmail.com
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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