Seasonal variation in dormancy and light sensitivity in ...

Seasonal variation in dormancy and light sensitivity in buried seeds of eight annual weed species

Can. J. Bot. Downloaded from www.nrcresearchpress.com by UNIVERSITY OF ILLINOIS on 09/08/13 For personal use only.

Per Milberg and Lars Andersson

Abstract: W e recorded germination in three different light environments (light, dark, and after a short light exposure) in eight annual weed species. Seeds were buried outdoors at the end of November 1994 and exhumed monthly from March 1995 to April 1996. All species exhibited substantial seasonal changes in dormancy level, and the patterns suggest that seeds of Papaver rhoeels germinate strictly in the autumn; Cc~psellubursa-pastoris, Descrlrc~irlinsophic~, Spergula arvensis, and Urticcl w e n s mainly in the autumn; Cl~enopocliurrisuecicurn strictly in the spring; and Mcltricc~rin perjGorata mainly in the spring. Lnpsclrla cornrnurlis showed inconsistent dormancy changes over the year. All species had acquired a light requirement for germination after being in the soil, and in many cases the short light exposure (1050 pmol . m-?) was enough to fulfil this requirement. T h e demonstrated seasonal changes in light sensitivity in several of the species will have to be taken into account in attempts to photocontrol weeds. By using the short-light treatment, w e were able to detect seasonal dormancy changes that would not have been obvious by testing for germination in only light and darkness. Hence, light is not a simple dichotomous factor in its effect o n germination. Key words: dormancy, germination, light, seed, Sweden, weed.

RCsurnC : Les auteurs ont enregistre la germination selon trois environnements lumineux (lumikre, obscuritC, et brCve exposition h la lumikre) chez huit espkces d e mauvaises herbes annuelles. Les graines ont CtC enterrCes h I'extCrieur h la fin d e novembre 1994 et dCterrCes chaque mois, d e mars 1995 h avril 1996. Toutes les espkces montrent des modifications saisonnikres bien marquCes quant au niveau d e la dormance et les patrons suggkrent que les graines du Papaver rhoeas ne germent qu'h I'automne, les Cnpsellu bursa-pastoris, Descurclirlia sophin, Spergula nrverlsis et Urtica urerls surtout h I'automne, le Clzerlopodinrn suecicurn seulement au printemps. le Mcltricclrin perfornta surtout au printemps, alors que le Lnpsancl cornrnnrlis rnontre des changements irriguliers d e la dormance au cours d e I'annCe. Aprks un sCjour dans le sol, toutes les espkces ont acquis un besoin d e lumikre pour germer et dans plusieurs cas. une courte exposition h la lumikre (1050 pmol . m-?) suffit pour remplir ce besoin. On devra prendre en compte les modifications saisonnikres dCmontrCes dans la sensibilitC h la lumikre des espkces, lorsqu'on tentera d e maitriser ces mauvaises herbes par la lumitre. En utilisant le court traitement lurnineux, les auteurs ont pu ddceler des modifications saisonnikres d e la dormance qui n'auraient pas Ctd dvidentes en mesurant la germination seulement en pleine lurnikre ou h I'obscuritC. ConsCquemment la lumikre n'est pas un simple facteur dichotome quant h ses effets sur la germination. Mots clis : dormance, germination, lumikre, graine, Sukde, mauvaise herbc [Traduit par la rCdaction]

Introduction Seeds of many annual weeds in temperate regions exhibit annual changes in dormancy. For example, during one season of the year seeds may not germinate when tested over a range of conditions and are thus dormant, whereas during another season of the year seeds may germinate over a wide range of conditions and are thus nondormant (Baskin and Baskin 1989a). Seeds of many species go into and out of dormancy each year in response to seasonal changes in environmental conditions, especially temperature, and this is called a dormancy cycle (Baskin and Baskin 1985). Seeds of some annual species are nondormant in autumn, whereas those of other species are nondormant in spring (Hikansson 1983; Froud-Williams et al. 1984; Baskin and Baskin 1985; Bouwmeester and Karssen 1989), and such species are often Received March 10, 1997.

P. Milberg and L. Anderson. Department of Crop Production Science, Swedish University of Agricultural Sciences, Box 7043, 7 5 0 0 7 Uppsala, Sweden. Can. J. Bot. 75: 1998-2004 (1997)

referred to as winter annuals and summer annuals, respectively. These changes in dormancy affect weed distribution among crops depending on their sowing date (Andersson and Milberg 1997). Seasonal dormancy cycles have been documented for seeds from a wide range of habitats among species that can accumulate in persistent soil seed banks (Baskin et al. 1989, 1993; Baskin and Baskin 1994; Milberg 1994a, 1 9 9 4 ~ ) . The detection of dormancy cycles depends on the conditions under which germination experiments are conducted. For example, for some species it is possible to demonstrate seasonal changes if tests are conducted under suboptimal temperature regimes but not when they are conducted under optimal regimes (Baskin and Baskin 1981, 1990b, 1994). In other cases, dormancy cycles were detectable in darkness but not in light (Baskin and Baskin 1981; Milberg 1994b). In this paper, we report how possible dormancy cycles in annual weeds were expressed in different light regimes. Our interest originated from the fact that the number of seedlings of annual weeds emerging was less when arable soil was tilled at night or under a covered implement, i.e., in darkO 1997 NRC Canada

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Milberg and Anderson

Table 1. Collection site and percent germination of recently harvested seeds under light and dark conditions in the batches included in the study.


Percent germination Species

Family

Capsella bursa-pastoris (L.) Medicus Chetlopodiutn suecicum J. Murr. Descuraitzia sophia (L.) Webb ex Prantl Lapsatza cotntnutzis L. Matricaria perforata MCrat Papaver rhoeas L. Spergula arvensis L. Urtica w e n s L.

Cruciferae Chenopodiaceae Cruciferae Compositae Compositae Papaveraceae Caryophyllaceae Urticaeae

Region of seed collection

Light

Dark

Sandvik, ~ s t e r ~ o t l a n d Ljngtorp, Ostergotland Vadstena, Ostergotland Normlosa, ste ergot land Halmbyboda, Uppland Odeshog, ~ s t e r ~ o t l a n d VirH, Sodermanland Sandvik, ~ s t e r ~ o t l a n d

Note: Values in parentheses are number of seeds.

ness, than when tilled in daylight (Ascard 1994; Scopel e t al. 1994). Previous experiments have s h o w n that most annual weeds respond t o short light exposures ( < 1 s of full daylight), at least under s o m e circumstances (Milberg e t al. 1996), and that milliseconds of daylight is sufficient t o stimulate germination in s o m e seeds (Scopel e t al. 1991; Milberg 1997). T h i s means o f weed photocontrol is highly unpredictable (Niemann 1996; references in Ascard 1994). W e hypothesized that the stimulatory effect of a short light exposure might b e seasonally dependent. In the present experiment, seeds o f eight annual weeds w e r e stored f o r 3 - 17 months in soil under natural temperature conditions and their germination w a s assessed a t different light regimes: light, darkness, and 5 s o f light followed b y darkness.

Materials and methods Seeds and storage conditions Eight annual weed species were included in thc study (Table I) and the seeds were collected in southern Sweden on 1-5 August 1994 (Matricaria perforata on 24 Aug.). The seeds of each species were dried at room temperature (22 2°C) for about 10 days, then gently cleaned by blowing and sifting, discarding nonviable-looking seeds. The seeds were then kept in open plastic containers at 22.5 f 1°C and about 30% RH. To provide data on light requirement of recently harvested seeds, batches of 100 seeds were distributed onto filter paper (two sheets of Munktell 1003, 90 mm diameter) previously wetted with deionized water (4.0 mL) in plastic Petri dishes (90 mm diameter). Two replicate dishes were subjected to 14 h of light per day (dishes sealed with parafilm) or darkness (wrapped in aluminium foil), and kept at a daily fluctuating temperature (4 and 18°C). Sealing dishes in this way prevents water loss, and the amounts of filter paper and water used ensure that the seeds remain under moist conditions for many weeks even if germination and seedling elongation occur. The experiment commenced in mid-September (7 weeks after collection of seven of the species) and was terminated after a month. Germination, i.e., radicle emergence, in the light treatment was noted on several occasions when germinants were removed. The dishes wrapped in aluminium foil were not opened until the end of the experiment. Ungerminated seeds were inspected and assigned to one of the two categories "dead" or "alive" based on the degree of mould growth, seed firmness, and endosperm properties. After 14 weeks of dry storage, batches of 100 seeds were put into fine mesh polyester bags (5 x 5 cm). Species were grouped by stapling one bag from each of four species. Three of these batches of bags from one group were then buried together in peat soil

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(70% Sphagnutn peat and 30% sand, pH 7. I, 0.005% nitrate) in a plastic container (10 x 10 cm and 7 cm high) with drainage holes. The container was placed in the centre of a white Mitscherlich pot (6.3 L) filled with a sandy soil. These pots were weighed and 0.02 kg) by adding or removing adjusted to equal weight (7.50 soil. The seeds were then at a depth of 10 cm in the soil. The pots were covered with a lid and placed in racks ca. I m above ground, outdoors at the Swedish University of Agricultural Sciences campus south of Uppsala on 24 November 1994. In two similar pots filled with soil, we recorded the temperature at seed level (one recording every 96 min with TINYTALK-TEMP logger; Orion Components Ltd., Chichester, England). To ensure that equal moisture conditions were maintained throughout the study, pots were weighed on 2 June, 20 July, and I1 August 1995 and adjusted to equal weight, if needed, by adding water.

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Treatments At monthly intervals, from 1 March 1995 to I April 1996, we tested the germination of exhumed seeds in the light, in the dark, and after a short light exposure. On each occasion, two pots (replicates) of each group of species were used. If the soil in the pots was frozen, the pots were taken indoors for thawing the day before treatment: after ca. 6 h at room temperature, the pots were put at 3OC and kept there until the treatments the following day. The bags were exhumed in complete darkness and two of the three sets of bags in each pot were distributed onto filter paper in a Petri dish (as described above). One dish of each species was wrapped in two layers of aluminium foil (dark treatment). The other dish was exposed to light for 5 s (described bclow) before being wrapped in two layers of aluminium foil. The third set of bags from each pot was inspected (in light) for seeds that had germinated while in the soil. The contents of the bags were placed in Petri dishes (as described above), which were then sealed with parafilm. In the short light exposure treatment, seeds in the dishes (without lids) were exposed to a photon flux density (PAR) of 210 f 10 pmol . m-' . s-I for 5 s (red light (R) 18 I pmol . m-' . s-I; far-red light (FR) 23 1 pmol . m-' . s-'; ratio R:FR of 0.85). The light source was a xenon bulb (OSRAM XBO 150 W l l ) with a Bausch and Lomb armature. The light bulb was placed in an aircooled, light-proof box. Seeds were exposed by letting light in through a hole, and the time of the exposure was measured with a stopwatch.

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Germination conditions The 48 Petri dishes of each germination experiment were placed in 16 stacks with the full-light treatment dishes (sealed with parafilm) on top. They were kept in an incubator with diurnal temperature fluctuations of 8.3-8.5"C and 17.5-18.0°C for 12 h each. The O 1997 NRC Canada


Fig. 1. Temporal variation in seed germination in three different light environments for (A) Papaver rhoeas, (B) Capsella bursa-pastoris, ( C ) Descurainia sophia, ( D ) Spergula antensis, ( E ) Urtica urens, (F) Lapsana cornmunis, (G) Matricaria pe$orata, and ( H ) Cherzopodiurn suecicwn. Seeds were collected in August and buried in soil in November 1994 and stored outdoors. Two seed batches of 100 seeds were exhumed monthly from 1 March 1995 to 1 April 1996 and were subjected to a full-light treatment with light for 12 h . day-' (o),5 s of light followed by darkness (o), o r a dark treatment (+). Lines connect the mean of the two replicates.

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Mar. Aor. May June July Aug. Sepl. Ocl. Nov. Dec. Jan. Feb. Mar. Apr.


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Fig. 2. Temporal variation in daily minimum (solid line) and maximum (broken line) temperatures at seed depth (10 cm) from 29 November


1994 to 1 April 1996.

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full-light treatment coincided with the period with the higher temperatures and was provided by fluorescent tubes (LUMA 25W) for 12 h . d-I (R:FR of ca. 7). The photon fluence rate (PAR) varied over time between 10 and 40 prnol . m-' . s-' because of an unnoticed tube failure. (A test, in April 1996, with parallel seed batches of seven of the spccies showed no significant differences ( p > 0.05) in germination between 8.0-8.5 and 40-42 prnol . m - 2 . S-I,) Thc germination experiment lasted for about 30 days and seeds that had germinated in the light treatment were counted and removed on three to five occasions. When the light treatment was terminated, the remaining seeds were inspected and considered as dead or alive (as above). The dishes wrapped in aluminium foil were only opened when the experiment was terminated. If there had been little germination, seedlings were counted and the remaining seeds assigned to the categories dead or alive. However, in several cases the substantial germination in the short-light treatment made it impossible to count individual seedlings. Instead, the number of germinated seeds was estimated by subtracting the average number of dead seeds, in the light- and dark-treatment dishes, from the number of seed coats and nonviable seeds.

Viability Since a fixed number of seeds had been buried, we calculated the percentage of viable seeds remaining in the full-light treatment (in the other treatments, some seeds were lost during handling in the dark). We evaluated possible trends over time in the proportion of viable seeds with Spearman's rank correlation.

Results Seasonal variation in germination All species exhibited seasonal changes in germination percentages in at least two of the treatments, and there was little germination in darkness on most occasions for all species (Fig. 1). Papaver rhoeas showed very distinct germinability changes over time in all three treatments. Germination occurred almost exclusively from 1 July to 1 January, with most germination occurring from September to December (Fig. 1A). In both light treatments, seeds of Capsella bursa-pastoris germinated most from July onwards, with a drop during the second winter and with substantial germination during the second late winter and spring (Fig. 1 ~ ) ~.e r m i n a t i o nwas consistently greater after the short-light exposure than in the full-light treatment.

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Seeds of Descurainia sophia did not germinate during the first spring and summer. Germination from September onwards was substantial in both light treatments, with some decrease during the winter (Fig. 1C). Seeds of Spergula arvensis germinated from March to December but least, in both light treatments, in March and April (Fig. ID). In the second spring, it was difficult to distinguish between dead and ungerminated but viable seeds. In Urtica urens, the pattern was complex (Fig. 1E). Germination in the dark Occurred only in the spring of both years, whereas in the full-light treatment this was when germination was the lowest. After the short-light exposure, germination was substantial throughout the year, but dropped during the winter and second spring. From July onwards, Lapsana communis germination was complete in the full light, and almost so after the short-light exposure (Fig. IF). Germination was lowest during the first spring. Seeds of M. pe$orata germinated at close to 100% in the light throughout the year (Fig. 1G). In the dark and after short-light exposure, however, germination varied over the year and was lowest from May to November. In the second spring, germination in the dark was > 7 0 % . Seeds of Chenopodium siiecicum germinated well from March to June, after which germination was drastically reduced. During the following winter, seeds became germinable again (Fig. 1H). This dormancy pattern was evident in all three light environments. The temperature regime under which the seeds were stored varied substantially over time: minimum -23.5"C and maximum 33.0°C, and the daily average ranged from - 19.5 to 24.3"C. The first winter was milder than the second (Fig. 2). The location of the seeds, 1 m above the ground, probably resulted in exposure to lower minimum temperatures compared with what seeds near the soil surface experience, since the latter, at least during parts of the winter, would have been covered by snow. Viability The viability among the buried seeds did not decrease significantly (Spearman's rank correlation: p > 0.05) for five of the species (Capsella bursa-pastoris, D. sophia, Lapsana communis, M. pe$orata, and S. arvensis). For Chenopodium

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Fig. 3. Change in viability with time in seeds buried in November 1994 and stored outdoors. Two batches of 100 seeds were exhumed monthly from 1 March 1995 to 1 April 1996. Only the species that showed significant decreases over time are shown, namely (A) Clzerlopodi~trn suecicurn, (B) Papaver rhoeas, and (C) Ur-tica urens.

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Mar. Apr. May June July Aug. Sept. Oct. Nov. Dec. Jan. Feb Mar. Apr. suecicum, P. rhoeas, and U. urerzs there was a significant decrease ( p < 0.001, 0.01, and 0.001, respectively). In Chenopodiurn suecicum there was a sharp decline during the late spring (95 to 80%; Fig. 3A). In P. rhoeas, there was a gentle decline over time, with a sharp drop from February to April in the second spring (from 90 to 75 %; Fig. 3B). The proportion of viable seeds of U. urens was reduced to less than 50% during the experiment. The decline was moderate until the second spring when it dropped substantially (from 75 to less than 50%; Fig. 3C).

Discussion Seasonal dormancy changes versus experimental conditions All eight species showed at least some changes in percent germination over time. In three species (P. rhoeas, Fig. 1A; D. sophia, Fig. 1C; Chenopodiurn suecicum, Fig. lH), variation ranged from 0 to >SO%, suggesting changes from very strong to very weak dormancy. In the other species, some germination occurred throughout the year and reached more than 90% during at least a part of the year and in at least one of the three treatments. This suggests seasonal changes from conditional dormancy to nondormancy (in terms of Baskin and Baskin 1989a), an aspect previously documented in some of the weed species included in our study (Baskin and Baskin 1989b, 1989c; Bouwmeester and Karssen 1993a, 19938).

The possibility of detecting seasonal changes in dormancy depends on the experimental conditions used. Therefore, investigators have often tested for germination at several temperatures (Baskin and Baskin 1994), with and without nitrate (Bouwmeester and Karssen 1993a), or in light and darkness (Baskin and Baskin 1981, Milberg 1994b). In the present study, by testing under three light conditions, we clearly showed that not only can the presence-absence of light be important but also the type of light treatment will influence the expression of dormancy changes. In some cases we were able to detect seasonal patterns that would not have been obvious by testing in only light and darkness (Figs. lE, 1G). That the germination percentages varied tremendously over time and depended on the conditions chosen in the experiment shows two things. First, any definition of dormancy that does not distinguish it from the phenomenon of germination will become quite complex, since both the temperature and light conditions used have an overriding influence on the germination percentages. We advocate a seed dormancy definition that is strictly a seed character and not related to one specific germination condition (Vleeshouwers et al. 1995). Hence, many experiments in different environments are needed for a full characterization of the dormancy level. Second, light is not a dichotomous factor (with or without) but is much more complex and its effect on germination probably depends on both quality and quantity. @ 1997 NRC Canada



Thus, in our view, a light requirement is not a form of dormancy, but merely just another indication of the dormancy level of the seeds. One aspect to consider when evaluating the present study is the timing of seed burial. Seeds were buried after 14 weeks of dry storage, whereas seeds in a field situation should normally have been incorporated in the soil at an earlier date. This difference in initial storage could possibly have affected the seasonal changes detected.

Light sensitivity Seeds of some of the species did not require light when fresh (Table 1); however, after being buried in the soil, light greatly promoted germination of all species (Fig. 1). Induction of light sensitivity by burial seems to be a common feature among weed species (Wesson and Wareing 1969; Froud-Williams et al. 1984; Scopel et al. 1991) and presumably also in species from other habitats. It is probably one of the main factors facilitating the buildup of persistent soil seed banks (Pons 1991; Milberg 1 9 9 4 ~ ) .This obligate light requirement was alleviated for some seeds during periods of weak seed dormancy (P. rhoeas from October to December, Fig. 1A; Capsella bursa-pastoris and D. sophia during the second spring, Figs. 1B and 1C; and M. perforata and Chenopodium suecicum during the first and second springs, Figs. l G and 1H). This is in accordance with the pattern found in many species (Baskin and Baskin 1980, 19896, 1989c, 1989d, 1990a, 1994). Urtica urens was therefore a puzzling exception in our study because the seeds germinated in the dark only during a period in which germination in the light was low (Fig. 1E). In several cases in the present study there was more germination after the short-light exposure than in the full-light treatment (Figs. lB, ID, 1E). 'This is somewhat surprising, but it should be kept in mind that the treatments are not directly comparable, since the type of light source differed (fluorescent tube vs. xenon bulb). Therefore, it is difficult to know if the full-light treatment actually inhibited germination or if the light quality of the short-light exposure was better for germination. Although weed harrowing in darkness often results in fewer seedlings of annual weed species (Hartmann and Nezadal 1990; Jensen 1992, 1995; Ascard 1994; Scopel et al. 1994), this is not always the case (references in Ascard 1994; Niemann 1996). From the results of the present study, it is obvious that the timing of the soil disturbance as well as the composition of the weed flora will determine the outcome of tilling in the dark. For example, our data on M. perforata (Fig. 1) suggest that the emergence of this species would be greatly reduced in March and April (large difference between germination in darkness and after short-light exposure), whereas only moderately so from May to November (smaller differences between the two treatments). It should be kept in mind that there is often a large degree of phenotypic variability in light sensitivity among seed populations of the same species (Milberg et al. 1996). In addition, light sensitivity might vary depending on the pregermination conditions that the seeds have experienced. This variability will influence seedling emergence in the field, since the soil seed bank consists of seeds differing in age and, thus, with different histories of environmental influence.

Furthermore, it is possible that seasonal dormancy patterns might vary between seed batches (Panetta and Randall 1993) and depend on the soil environment.

Viability loss Most annual weed species are known to have seeds that can survive for several years in the soil (Milberg 1990), and therefore it is not surprising that there was no substantial decrease in viability for most of our weed species (with the exception of U. urens and possibly S. awensis). Seeds of M. perforata, Chenopodium album, P. rhoeas, and Capsella bursa-pastoris have been shown to survive for decades in the soil (Toole and Brown 1946; Madsen 1962; Lewis 1973; Kivilaan and Bandurski 1981; Chancellor 1986). Other less well-known species have also survived for several years: S. arvensis for > 10 years (Salzmann 1954), D. sophia for > 10 years (Conn and Deck 1995), U. urens for > 6 years (Roberts and Feast 1973), and L. cominunis for > 5 years (Roberts and Neilson 1981). In the present experiment, empty and soft seeds were designated as nonviable. Thus, the decreased number of viable seeds in some cases could be the result of either seeds germinating while they were buried in the pots or seeds decomposing. If the former is true, the drops in number of viable seeds (Fig. 3) should coincide with increased germination in the dark treatment (Fig. 1) as well as with suitable temperatures for germination outdoors (Fig. 2). For Chenopodium suecicum, there was an apparent drop in the number of viable seeds remaining late in the first spring (Fig. 3A). This drop coincided with the end of a period suitable for substantial germination in the dark (Fig. 1H) and an increased soil temperature (Fig. 2). It is reasonable to assume that many seeds germinated in the soil up until that time. Had the experiment been continued for another couple of months we might have seen a similar pattern in the second spring in Chenopodium suecicum, D. sophia, and M. perforata, since all three showed substantial germination in the dark during this period. Acknowledgements The Swedish Council for Forestry and Agricultural Research supported this study. We are grateful to Angela Noronha and Ya Schang for their assistance in the experiments and to Carol Baskin and referees for commenting on the text.

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