Ecological Modelling 222 (2011) 626–636

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Ecological Modelling
journal homepage: www.elsevier.com/locate/ecolmodel

Prediction of germination rates of weed species: Relationships between

germination speed parameters and species traits
Antoine Gardarin a , Carolyne Dürr b , Nathalie Colbach a,∗
a
INRA, AgroSup Dijon, Université de Bourgogne, UMR 1210 Biologie et Gestion des Adventices, 21000 Dijon, France
b
INRA, UMR 1191 Physiologie Moléculaire des Semences, 49000 Angers, France

a r t i c l e i n f o a b s t r a c t

Article history: In fields, the timing of weed emergence flushes is mostly related to the timing and rate of seed germina-
Received 1 February 2010 tion, which depend on seed dormancy level, soil temperature and water potential conditions as well as
Received in revised form soil tillage and crop sowing date. Seed germination parameters are essential in weed dynamics models
15 September 2010
to account for the effects of soil conditions on weed demography. Since these parameters are difficult
Accepted 7 October 2010
to measure, our objective was to test the possibility of estimating them from easily accessible informa-
Available online 17 November 2010
tion. Seed germination parameters (germination lag-time, time to mid-germination and mid-germination
rate) were measured or collected from the literature for 25 weed species with contrasted seed character-
Keywords:
Base temperature
istics. Correlations were then searched for between these parameters and morphological, chemical and
Dormancy physiological seed traits as well as seed dormancy level. The dormancy level was positively correlated
Germination lag with speed of germination parameters. Earliness of germination was positively correlated with seed lipid
Germination rate content and the seed area to mass ratio. Germination was also earlier and faster in species with a high
Lipid content base temperature for germination. These relationships explained about half the observed variability in
Area to mass ratio germination speed parameters but should be further tested before being used to predict the germination
Seed behaviour of weed species in the field in different seasons.
© 2010 Elsevier B.V. All rights reserved.

1. Introduction ulated by a large number of different weed species. Such models

Models to quantify the effects of cropping systems on weed
dynamics are necessary to develop innovative cropping systems to
reduce the use of herbicides and preserve the biodiversity of fauna
and flora (Freckleton and Stephens, 2009). Such models consist of
a succession of key life stages (e.g. non-dormant seeds, germinated
seeds, emerged seedlings, etc.) linked by functions that depend on
the effects of the cropping system in interaction with the climate
and soil environment (Vleeshouwers and Kropff, 2000; Colbach
et al., 2006; Sester et al., 2007). Weed seed germination (starting
with the uptake of water by the quiescent dry seed and terminat-
ing with the elongation of the embryonic axis, Bewley, 1997) is a
key process because it determines both the amount of weeds that
could potentially emerge and the timing of their appearance in the
field. To date, weed dynamics models have been developed only for
a very small number of species even though fields are often pop-
∗ Corresponding author at: UMR 1210 Biologie et Gestion des Adventices, INRA,
17 rue Sully, BP 86510, 21065 Dijon cedex, France. Tel.: +33 03 80 69 30 33;
fax: +33 03 80 69 32 62.
E-mail addresses: Antoine gardarin@yahoo.fr (A. Gardarin),
carolyne.durr@angers.inra.fr (C. Dürr), Nathalie.Colbach@dijon.inra.fr (N. Colbach).
should therefore be extended to a wider flora in order to predict
the effects of integrated weed control strategies on whole weed
communities in the long term.
In weed dynamics models, germination is usually modelled as
a function of hydro-thermal conditions, the proportion of non-
dormant seeds, and parameters that are specific to the species being
modelled (Colbach et al., 2005), including base temperature and
base water potential for germination (described in detail in a pre-
vious study, Gardarin et al., 2010b). Seasonal variations in seed
dormancy (i.e. the inability to germinate even in favourable con-
ditions) over time have also been widely studied in many weeds
(Lonchamp et al., 1984; Baskin and Baskin, 1989; Bouwmeester
and Karssen, 1993) and are related to variations in the amplitude
of the permissive range of temperatures and water potentials for
germination (Batlla and Benech-Arnold, 2007). However, few stud-
ies have compared germination rates of weed seeds while taking
into account variations in their dormancy in the soil (as opposed
to dry-stored seeds in laboratory conditions), as such studies are
expensive and time-consuming.
An innovative approach would be to correlate species traits to
predict the behaviour of a wide range of species (Keddy, 1992).
Following the definition of Violle et al. (2007), a trait is any mor-
phological, physiological or phenological feature measurable at

0304-3800/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.ecolmodel.2010.10.005
 A. Gardarin et al. / Ecological Modelling 222 (2011) 626–636
Table 1
Correlations found in the literature between seed traits and the germination rate of wild or cropped species.
Seed traits or other characteristics Correlation with the seed germination rate
Seed physical characteristics
Spherical, multicoloured or Negative
mucilaginous seeds
Presence of a pappus, Positive
hygroscopic awns or hairs, or
conical shape
Mass Negative
Mass No effect
Mass Negative (weak tendency)
Mass No consistent pattern in the populations and
species studied
Mass Positive
Seed chemical characteristics
Lipid content Negative in anoxic conditions
Soluble sugar contents High fructose accumulation rate and raffinose
decreasing rate during germination increased
germination rate
Soluble sugars contents Negative
(raffinose and stachyose)
Other
Base temperature for seedling Positive
emergence in the field
the individual level. Seed traits have been linked with seedling
establishment in wild species (Weiher et al., 1999). Based on this
principle, model parameters which are difficult to measure could be
inferred from easily accessible seed traits using generic functions
established with a few contrasting model species representative
of the diversity of the weeds (Gardarin et al., 2009). We already
established such relationships for the prediction of pre-emergence
seedling growth (Gardarin et al., 2010a).
A critical analysis of existing germination literature led to
the identification of several seed characteristics related to ger-
mination. Table 1 summarizes various inter and intra-specific
relationships found in the literature between morphological, chem-
ical and physiological seed characteristics on the one hand, and
the seed germination rate on the other. The seed germination rate
was found to be correlated with the species base temperature for
germination. According to Angus et al. (1981), the thermal time nec-
essary for germination and emergence of crop species decreased
with an increase in species base temperature. Similar correlations
have been reported for the growth of different kinds of organisms
(e.g. insects, arachnids, Trudgill et al., 2005) and could be relevant
for weed seed germination. Secondly, based on the study of 400
species of Britannic flora, Grime et al. (1981) observed that the
germination rate was associated with the shape of the seed, and
that smaller and more elongated seeds had higher germination
rates. The intra-specific effect of seed mass on germination rate
differs with the species studied and no clear pattern is apparent
(Milberg et al., 1996; Baloch et al., 2001). A maize seed imbibition
model revealed that the proportion of the imbibed seed surface
was strongly correlated with the seed imbibition rate (Bruckler,
1983a,b) and consequently with the germination rate. Therefore,
if we assume that the amount of water required by a given seed
depends on its mass, the area to mass ratio could influence the seed
imbibition rate. Finally, the seed germination rate may also depend
on reserve mobilization, which is necessary for germination and
early seedling growth. The composition of the seed reserves, their
protein, lipid and soluble sugar contents, varies greatly between
genera and families (Earle and Jones, 1962; Kuo et al., 1988). It
is often suggested, although to our knowledge not demonstrated,
that a high soluble sugar content in the seed reserves supplies
rapidly available energy for the embryo and favours rapid germi-
nation (Dierking and Bilyeu, 2009). Kuo et al. (1988) observed an
increase in germination rates in relation with the disappearance
of raffinose and accumulation of fructose in cotton, soybean and
627
Species studied Source
400 species of the British Isles flora Grime et al. (1981)
400 species of the British Isles flora Grime et al. (1981)
400 species of the British Isles flora Grime et al. (1981)
64 wetlands species Shipley et Parent, 1991
Abutilon theophrasti Baloch et al. (2001)
Lithospermum arvense, Anchusa arvensis Milberg et al. (1996)
Alopecurus myosuroides Colbach and Dürr (2003)
12 cropped species Raymond et al. (1985)
Phaseolus aureus, Glycine max, Kuo et al. (1988)
Gossypium arboreum
Glycine max Obendorf et al. (2008)
30 cropped species Angus et al. (1981)
mung bean, three species contrasted in their raffinose saccharide
contents. Al-Ani et al. (1985) showed for crop species with a wide
range of seed lipid contents that a high seed lipid content increased
their sensitivity to low oxygen partial pressure during germination.
In addition to these traits, germination speed varies consider-
ably with the level of seed dormancy, more in weed species than
in crop species. Slow germination rates (i.e. the proportion of ger-
minated seeds per unit of time) have been shown to be correlated
with low final germination percentages of highly dormant seeds
(Courtney, 1968; Vleeshouwers, 1997; Colbach et al., 2006). Highly
dormant seeds also present long germination lags (i.e. the time from
water uptake to the first germinated seed in the seed lot) and lower
germination rates (Shipley and Parent, 1991).
The objective of the present study was to search for relationships
between the parameters influencing germination speed (i.e. ger-
mination lag-time, time to mid-germination and mid-germination
rate) and morphological, chemical and physiological seed traits.
Relationships were searched for using germination experiments
on 14 weed species in which the above-mentioned traits were con-
trasted and which were representative of the weed flora found
in north-western European cropping systems. Their seeds were
buried and then excavated in different seasons in the field to
account for variations in seed dormancy over time. They were then
put to germinate in light vs. darkness to account for light condi-
tions for surface vs. buried seeds in the field. The experiments were
completed with data from the literature to increase the number of
species analysed.
2. Material and methods
Experiments consisted in burying seed bags and then excavating
them every two or six months over a period of two years in order
to measure changes in seed germinability due to variations in seed
dormancy level.
2.1. Seed burial and recovery
Seeds of 14 weed species commonly found in fields in
north-western Europe with intensive cropping systems, and with
contrasting seed traits (seed mass, nature of reserves, etc.) were
collected at full maturity in 2006 in fields near Dijon (47.317◦ N,
5.017◦ E, 220 m altitude) in Burgundy, France, except Arabidopsis
thaliana for which no seeds could be harvested in 2006. Imme-
 628
Table 2
Species studied, experimental conditions for the seed lot burial and germination experiments, and range of germination speed parameters estimated from fitting equation.

Species Presence of Burial date Periodicity Germination Periods where final

A. Gardarin et al. / Ecological Modelling 222 (2011) 626–636

soil (100 g) of seed germination
in the bags recovery percentages were

Temperature Light conditions Range of final Range of lag time Range of time to Range of Low High
(◦ C) germination TT0 (◦ C days) mid-germination germination rates
proportions m TT50 (◦ C days) at
mid-germination
(◦ C−1 days−1 )
Capsella bursa-pastoris (L.) Medik. No 16 June 2 months 15 Light and dark 0.06–0.58 12–73 26–91 0.0059–0.1422 June November
Galium aparine L. Yes 18 July 2 months 15 Light and dark 0.07–1 25–101 30–192 0.0004–0.0100 April November
Matricaria perforata Mérat No 18 July 2 months 15 Light and dark 0.46–0.99 18–66 33–85 0.0050–0.1026 July 06 Aug.06–June 08
Amaranthus hybridus L. No 13 September 2 months 25 Light and dark 0.09–1 10–35 14–79 0.0011–0.8199 October April
Polygonum lapathifolium L. Yes 27 September 2 months 25 Light and dark 0.07–0.99 14–77 23–97 0.0005–0.0795 September March
Arabidopsis thaliana (L.) Heynhnh No 18 July 6 months 15 Light 0.95–0.97 37–79 61–107 0.0157–0.0220 July 06–April 08
Avena fatua L. Yes 4 July 6 months 15 Light 0.11–0.98 26–55 28–91 0.0021–0.0506 April June
Papaver rhoeas L. No 4 July 6 months 15 Light 0.11–0.32 81–103 106–127 0.0016–0.0240 July 06–October April 08
07
Echinochloa crus-galli Beauv. No 1 August 6 months 15 Light 0.24–0.98 38–45 40–74 0.0074–0.0304 October May
Chenopodium album L. No 18 September 6 months 15 Light 0.09–0.56 31–46 33–111 0.0016–0.0123 October May
Fallopia convolvulus Loeve Yes 27 September 6 months 20 Light 0.08 56 79 0.0026 September April 08
06–October 07
Polygonum aviculare L. No 2 October 6 months 20 Light 0–0.04 Not estimated Not estimated Not estimated October
06–March 08
Ambrosia artemisiifolia L. No 11 October 6 months 20 Light 0.53–0.89 18–31 31–38 0.0188–0.0469 October April
Digitaria sanguinalis (L.) Scop. No 11 October 6 months 25 Light 0.13–0.90 30–31 30–46 0.049–0.6134 October May
 A. Gardarin et al. / Ecological Modelling 222 (2011) 626–636
diately after collection, samples of 100–300 seeds were placed in
nylon (Tergal) bags (mesh size 400 ␮m). For large seeds, 100 g of
field soil (15% moisture content) was added to prevent direct con-
tact between the seeds (Table 2). Seed bags were placed at the
bottom of openwork baskets, with three bags of one species per
basket. The baskets were filled with soil and, in 2006, were buried
at a depth of approximately 30 cm corresponding to the bottom
of the ploughed layer. Every two months over the next two years,
two baskets (six bags) of five species (Table 2) were randomly cho-
sen to be excavated, one for germination tests in the light and
another one for the tests in the dark. In the latter case, immedi-
ately after excavation, the basket was placed in two opaque bags
without removing the soil from the bags to keep them in continuous
darkness. For these five species, seeds were recovered frequently
in order to precisely detect seasonal variations in the seed germi-
nation rate. For the other nine species, one basket was recovered
(only for germination tests in the light) approximately every six
months to study germination when seeds were either most or least
dormant (Table 2).
2.2. Seed germination tests
The seed germinability of each species was assessed after seed
collection, at the beginning of the burial experiment, and then at
each recovery date. For the species recovered every two months,
germination was studied in either constant light or in total dark-
ness. If necessary, seeds were manually recovered one by one from
the soil with which they were mixed. One hundred seeds from
each bag were laid out on pleated paper (pleated strips, 113 g m−2 ,
doublefolds, 110 mm × 20 mm). The pleated paper was placed in a
plastic box with 40 mL of deionised water to obtain non-limiting
water conditions. There were three boxes per species and light
condition at every recovery date. Boxes were closed hermetically
to avoid water loss and placed in an incubator at a temperature
close to the optimum temperature of each species (Montégut, 1975;
Webster, 1979, Table 2). The incubators were illuminated with
six fluorescent lighting tubes (Osram, L 18 W/77, 20 ␮mol m−2 s−1
each).
Seeds were set to germinate at constant temperature. The ampli-
tude of alternating temperature can have a major effect on the
germination rate and final percentage of the species (Baskin and
Baskin, 1998; Taab and Andersson, 2009). In our study, the effect
of alternating temperatures on the speed of germination was indi-
rectly accounted for via the integration of the percentage of total
germinating seeds in the statistical analyses as an explanatory vari-
able (see Section 2.7).
Seed bags destined for germination in darkness were handled
in a dark room lit by a green inactinic lamplight with no stimu-
lating effect on germination, as shown by Colbach et al. (2002).
Boxes were wrapped in two sheets of aluminium foil and placed
in the same incubator. The germination conditions of each species
are summarised in Table 2. The temperature of each incubator was
recorded and used for data analysis (see Section 2.4).
Seed germination was assessed daily during the first week after
water was added and then regularly until the end of germina-
tion, over a period of at least four weeks. Seeds set to germinate
in darkness were observed under green light. Germination assess-
ment consisted in counting (and eliminating) the number of newly
germinated seeds, i.e. those with a protruding root.
2.3. Seed viability tests
After the final measurement, ungerminated seeds were treated
with gibberellin (0.29 mmol L−1 ) and, if required by the species,
stratified to overcome dormancy according to the literature
(Webster, 1979). Seed germination was then recorded each week
629
Fig. 1. Meaning of the different germination time-course parameters Example of
Galium aparine: seeds were recovered on 29th January 2009 and germinated in the
dark (symbols) with fitted time-course Eq. (2).
for one month. The remaining ungerminated seeds were dissected
(crush test, Sawma and Mohler, 2002) to distinguish viable dormant
seeds from unviable seeds.
The total number of viable seeds set to germinate was the sum
of the number of germinated seeds (before addition of gibberellin)
plus the number of viable seeds remaining at the end of the exper-
iment (germinated after addition of gibberellin and viable seeds
identified in the crush test).
2.4. Germination time courses
A germination time course is considered here as the cumulated
proportion of germinated seeds with thermal time after the addi-
tion of water. The three seed lots exhumed from each basket were
considered as pseudo-replicates and were pooled for data analysis.
Germination time courses were determined for each combination
of the factors concerned (species, exhumation date and light con-
dition). For each germination time course, the thermal time TT[i]
(◦ C days) was calculated each day i, after addition of water, with
the following equation (Garcia-Huidobro et al., 1982):
TT[i] = TT[i − 1] + (T [i] − Tb ) (1)
where T[i] is the temperature (◦ C) of day i and Tb the base temper-
ature (◦ C) for germination of the corresponding species (Table 3).
Base temperatures were either measured in a previous study using
the x-intercept method (Gardarin, 2008) or taken from the lit-
erature. No data were available for Papaver rhoeas and Fallopia
convolvulus. For these species, base temperature was estimated at
0.8 and 4.3 ◦ C, respectively, using a relationship between the date of
emergence onset of the species in spring and the base temperature
proposed by Gardarin et al. (2010b).
The cumulated proportion of germinated seeds G[i] was calcu-
lated as the number of seeds having germinated up to day i divided
by the total number of viable seeds. An equation adapted from
Weibull (1959) was fitted to G[i] with thermal time TT[i] for each
germination time course (Fig. 1):
G[i] = 0, if TT[i] < TT0 ,
⎡  b ⎤
TT [i] − TT0
⎢ −logn (2)·
TT50 − TT0 ⎥
G[i] = m ⎢1 − e ⎥ + error, if TT[i] ≥ TT0 (2)
⎣ ⎦
where m is the final proportion of germinated seeds equivalent
to the proportion of non-dormant seeds. TT0 is the germination
630 A. Gardarin et al. / Ecological Modelling 222 (2011) 626–636

Table 3
Seed traits measured in 25 weed species.

Species Seed dry mass Area Area-mass ratio Lipid content Protein content Base temperature
(± SD, mg) (± SD, mm2 ) (± SD, mm2 /mg) (± SD, %) (± SD, %) (± SE, ◦ C)

Alopecurus myosuroides 2.3 ± 0.67 6.523 2.8 14.5 ± 0.46 22.7 ± 0.03 0.06
Amaranthus hybridus 0.4 ± 0.07 1.4 3.7 8.5 ± 0.04 15.5 ± 0.10 8.8 ± 1.110
Amaranthus retroflexus The traits measured in A. hybridus were used since A. hybridus and A. retroflexus are very similar and frequently 15.021
considered as a belonging to the same single species.
Ambrosia artemisiifolia 4.6 ± 1.30 5.1 ± 0.88 1.1 22.3 ± 0.08 9.5 ± 0.00 3.6 ± 1.114
Arabidopsis thaliana (L.) Heynh. 0.029 0.123 5.5 41.9 23.5 ± 0.05 3.011
Avena fatua 18.5 ± 6.66 17.523 0.9 8.9 ± 0.18 8.4 ± 0.02 2.2 ± 1.213 , 0.48
Beta vulgaris ssp. vulgaris 12.5 15.6 1.3 21.3 ± 1.72 23.7 ± 0.34 3.515
Capsella bursa-pastoris 0.1 ± 0.02 0.4 23
3.1 39.1 ± 0.28 23.3 ± 0.03 4.5 ± 1.714
Centaurea cyanus 5.3 5.2 ± 1.18 1.0 28.4 ± 0.27 16.9 16 2.2 ± 0.514
Chenopodium album 0.6 1.4 ± 0.18 2.5 9.4 ± 0.09 14.2 ± 0.13 5.8 ± 0.513 , 228
Datura stramonium 7.2 ± 1.14 7.8 ± 0.96 1.1 32.1 ± 0.05 18.416,24 10.44
Digitaria sanguinalis 0.6 ± 0.09 2.0 ± 0.29 3.5 4.3 ± 0.28 16.6 ± 0.13 9.9 ± 2.522,19,25
Echinochloa crus-galli (L.) P. 2.2 ± 0.46 4.1 ± 0.71 1.8 6.3 ± 0.12 13.5 ± ± 0.08 6.2 ± 0.614
Beauv.
Fallopia convolvulus (L.) A. Löve 6.5 ± 1.39 7.4 ± 0.47 1.1 3.5 ± 0.10 14.6 ± 0.05 4.3
Galium aparine 7.4 ± 2.39 5.4 ± 1.72 0.7 3.7 ± 0.08 11.5 ± 0.08 2.526
Geranium dissectum 2.1 ± 0.36 2.3 ± 0.24 1.1 21.4 ± 0.80 24.2 ± 0.13 −1.5 ± 1.314
Matricaria perforata 0.3 ± 0.08 0.223 0.8 19.4 ± 0.13 15.3 ± 0.00 2.0 ± 0.714
Papaver rhoeas 0.1 0.323 2.4 43.6 ± 0.24 23.0 ± 0.03 0.8
Polygonum aviculare 1.5 ± 0.59 3.1 ± 1.27 2.1 4.2 ± 0.28 11.9 ± 0.03 0.017
Polygonum lapathifolium 2.0 ± 0.58 5.0 2.5 5.5 ± 0.01 11.0 ± 0.01 5.8 ± 1.014
Polygonum persicaria 1.99,18,20,28 The traits of Polygonum lapathifolium were used since these two species are relatively close. 3.228
Solanum nigrum 0.83,7,9 1.823 2.4 25.12,7,24 18.32,7,24 11.5 ± 0.713
Spergula arvensis 0.43,5,9,20,28 0.623 0.3 11.51 14.59 3.727
Stellaria media 0.4 0.8 ± 0.08 2.1 5.91 17.92,24 1.412
Veronica hederifolia 3.5 ± 1.48 4.0 ± 1.09 1.1 15.6 ± 0.27 15.6 ± 0.01 0.2 ± 0.214

Sources: 1 (Aitzetmüller et al., 2003); 2 (Barclay and Earle, 1974); 3 (Benvenuti et al., 2001); 4 (Benvenuti and Macchia, 1993); 5 (Bouwmeester and Karssen, 1992); 6 (Colbach
et al., 2002); 7 (Earle and Jones, 1962); 8 (Fernandez-Quintanilla et al., 1990); 9 (Flynn et al., 2006); 10 (Granger and Guillemin, 2004); 11 (Granier et al., 2002); 12 (Grundy
and Mead, 2000); 13 (Guillemin et al., 2008); 14 (Gardarin et al., 2010b); 15 (Gummerson, 1986); 16 (Jones and Earle, 1966); 17 (Kruk and Benech-Arnold, 2000); 18 (Lutman
et al., 2002); 19 (Masin et al., 2005); 20 (Milberg et al., 2000); 21 (Oryokot et al., 1997); 22 (Sartorato and Pignata, 2008); 23 (Sevic, 2003); 24 (Schroeder et al., 1974); 25
(Steinmaus et al., 2000); 26 (Van der Weide, 1993); 27 (Vleeshouwers, 1997); 28 (Vleeshouwers and Kropff, 2000).

lag, i.e. the thermal time (◦ C days) from the addition of water
to the first germination. TT50 is the time to mid-germination, i.e.
the thermal time necessary to obtain m/2 germinated seeds. b is
a shape parameter correlated with the germination rate at mid-
germination. Fitting was carried out using proc NLIN of SAS (SAS
Institute Inc., Cary, North Carolina, USA, 1999). R2 were calculated
as 1 − (sum of error squares)/(total corrected sum of squares). No
fitting was done when less than 5% of the seeds germinated.
The germination rate at mid-germination (v50 , in ◦ C−1 days−1 )
was calculated using the derivative of Eq. (2) at mid-germination
TT50 :
m · b · logn (2)
v50 =
2 · (TT50 − TT0 )
2.5. Germination time courses taken from literature
To increase the number and range of species analysed, additional
data were taken from the literature. We only used germination time
courses obtained in similar conditions to the protocol described in
Sections 2.1–2.3 (optimal temperature and water potential condi-
tions) and for which the final proportion of germination (level of
dormancy) was known. However, for most of the species, germina-
tion was measured on seed lots which had not been buried in the
soil. Details on these supplementary time courses are summarized
in Table 4. When available, values for germination parameters (TT0 ,
TT50 and v50 ) were taken directly from the paper concerned. Oth-
erwise, the parameters were estimated graphically. Germination
speed parameters expressed per day or per hour were converted
into thermal time using the base temperature given in the same
paper if possible.
The final dataset consisted in germination time courses mea-
sured for 14 species buried in the field completed by literature data
for 18 species (including 11 new species), resulting in a total of 25
species. Finally, there were up to four different sources of data (from
our experiments or from the literature) for each species.
2.6. Seed trait measurements
Seed traits were measured on samples taken from the same seed
lots as those buried in the soil. The seed dry mass of each species
was measured individually on 100 seeds dried at 80 ◦ C for 48 h.
Individual photos of 100 seeds were taken with a camera (pixel
size between 2.25 and 4.18 ␮m depending on the species) and the
morphological features were computed on a binary image using
(3) the method previously described by Muracciole et al. (2007). Seed
area, in two dimensions, was then determined by image analysis
(Majumdar and Jayas, 2000; Muracciole et al., 2007).
For seed composition analyses, seeds enclosed in thick seed
coats were dehulled. The outer seed coat of Avena fatua L., Alopecu-
rus myosuroides and Echinochloa crus-galli, and the floral parts of
Beta vulgaris ssp. vulgaris were removed. Seeds of other species were
kept intact and their dispersule (i.e. the seed or the fruit with all its
attached structures) was analysed. Seeds were dried at 80 ◦ C for
48 h and two seed samples were taken from each species. Seeds
weighing less than 3 mg were milled to fine powder in a rotary
grinder (ZM 200, Retsch) and a ball mill (diameter 10 mm, Pro-
labo) was used for larger seeds. Nitrogen content was measured
using the Dumas procedure (Hansen, 1989) and multiplied by 6.25
to estimate the seed protein content (Mariotti et al., 2008). Lipid
content was determined, following Jensen et al. (1972) by dis-
solving seed lipids in hexane:isopropanol (3:2, v/v), centrifuging
and collecting the supernatant, then evaporating the solvent with
a rotary evaporator. The lipids remaining in the tube were then
weighed. Missing trait values were completed with data from the
literature.
 A. Gardarin et al. / Ecological Modelling 222 (2011) 626–636 631

Table 4
Seed germination data used to increase our experimental dataset.

Species Source Seed storage characteristics Germination Other germination Number of Range of final
temperature conditions germination germination
(◦ C) kinetics proportions

Alopecurus myosuroides
Amaranthus retroflexus
Amaranthus retroflexus
Amaranthus retroflexus
Ambrosia artemisiifolia
Avena fatua
Avena fatua
Beta vulgaris ssp. vulgaris
Capsella bursa-pastoris
Centaurea cyanus
Centaurea cyanus
Chenopodium album
Chenopodium album
Datura stramonium
Echinochloa crus-galli
Galium aparine
Geranium dissectum
Polygonum lapathifolium
Polygonum persicaria
Polygonum persicaria
Solanum nigrum
Solanum nigrum
Spergula arvensis
Stellaria media
Stellaria media
Veronica hederifolia
Colbach et al. (2006) Buried in the soil and recovered 15 Light and dark 12 0.08–0.95
after 1, 4, 5, 13, 16, 17 and 23
months
Ghorbani et al. (1999) Storage at ambient temperature 20 and 30 Light 2 0.40–0.80
Gardarin (2008) Storage at ambient temperature 30 and 27.5 Light 2 0.97–1
See also Granger and
Guillemin (2004)
Oryokot et al. (1997) Storage at 5 ◦ C From 12 to 33 Light 1 1
Gardarin (2008) Storage at ambient temperature 27.5 3 weeks of 1 0.60
stratification at
4 ◦ C—light
Fernandez-Quintanilla Storage at ambient temperature 15 and 20 Light 2 0.71–0.80
et al. (1990)
Gardarin (2008) Storage at ambient temperature 10 Light—imbibition 1 0.71
See also Guillemin et al. with KNO3 (1%)
(2008)
Sester et al. (2006) Buried in the soil and recovered 15 Light and dark 12 0.05–0.67
after 1, 4, 5, 13, 16, 17 and 23
months
Gardarin (2008) Storage at ambient temperature 30 Light 1 0.58
Gardarin (2008) Storage at ambient temperature 20 Light—imbibition 2 0.79–0.81
with KNO3 (1%)
Unpublished—seeds from Storage at ambient temperature 15 Light 6 0.89–0.98
cultivated field, Chizé,
France (2006)
Gardarin (2008) Storage at ambient temperature 25 Light—imbibition 3 0.29–0.88
See also Guillemin et al. with KNO3 (1%)
(2008)
Vleeshouwers and Kropff Buried in the soil From 5 to 30 Light 1 1
(2000)
Unpublished—seeds from Storage at 4 ◦ C and low air 25 Light 3 0.94–0.96
experimental plots, Dijon, moisture content
France, 2006
Gardarin (2008) Storage at ambient temperature 22.5 Light 1 0.85
Van der Weide (1993) Buried in the soil From 4 to 18 Light 1 1
Gardarin (2008) Storage at 4 ◦ C and low air 15 Light 5 0.97–1
moisture content
Gardarin (2008) Storage at ambient temperature 30 Light 1 0.73
Vleeshouwers (1997) Buried in the soil 15, 20 and 25 Light 3 0.95
Vleeshouwers and Kropff Buried in the soil From 5 to 30 Light 1 1
(2000)
Gardarin (2008)
See also Guillemin et al., Storage at ambient temperature 30 Light 1 0.48
2008
Wagenvoort and Opstal Storage at ambient temperature 20 Light 1 0.70
(1979)
Vleeshouwers and Kropff Buried in the soil From 5 to 30 Light 1 1
(2000)
◦
Grundy et al. (2000) Storage at 4 C 14, 16 and 18 Light 3 0.86–1
Unpublished—seeds from Storage at 4 ◦ C and low air 15 Light 6 0.05–0.12
experimental plots, Dijon, moisture content
France, 2004
Gardarin (2008) Storage at 4 ◦ C and low air 15 Dark 1 0.56–0.70
moisture content

2.7. Relationships between germination speed parameters and to a multiplicative model, which more satisfactorily accounts for
seed traits multiplicative interactions between the factors:
logn (germination parameter) = intercept
Linear models were used to study relationships between the

+ ˛trait logn (trait) + seed reserves categories effect

seed germination speed parameters (TT0 , TT50 , b and v50 ) on the

traits catégories (4)

one hand, and seed traits, dormancy and experimental conditions
+ logn (trait) · category effect + logn (m) + light effect + error
(light vs. darkness) on the other hand. Seed traits consisted in seed
mass, area, lipid and protein content, area to mass ratio and the traits·categories

species base temperature for germination. For the analysis of the
effect of lipid content, two groups of species were distinguished:
lipid-rich seeds (seed lipid content superior to 30%) and lipid-poor
seeds. Seed dormancy was added to the model as a covariable and
was characterized by the final proportion of germinated seeds m.
Explained and explanatory quantitative variables were logn -
transformed before analysis, the linear model thus being equivalent
where ˛trait are regression parameters. Base temperature was
transformed by adding the constant 2 to obtain positive values
and make the logn -transformations possible. The contribution of
each effect to the variance explained by the model was computed
using type III sum of squares. Statistical analyses were performed
using PROC REG (option BACKWARD) of SAS (SAS Institute Inc.,
Cary, North Carolina, USA, 1999). Only factors that were significant
632 A. Gardarin et al. / Ecological Modelling 222 (2011) 626–636
at ˛ = 0.05 were kept. Models comprising the significant variables
were then compared using Akaike’s Information Criterion (AIC)
and the model with the lowest AIC was considered to be the best
(Akaike, 1973). The elimination of variables stopped when the AIC
did not change by more than the absolute value of 2 and included
the lowest number of variables.
3. Results
3.1. Fitting the non-linear equation to observations of
germination time courses
The data consisted of a total of 111 observed germination time
courses for which Eq. (2) could be fitted (example Fig. 1), with R2
values between 0.96 and 1. However, some species presented a
very high level of dormancy at one or several recovery dates and
did not germinate sufficiently (proportion less than 0.05) to allow
the calculation of germination course parameters. For this reason
Polygonum aviculare was excluded from all analyses.
3.2. Seasonal variations in germination speed parameters
Important seasonal variations were observed in the final ger-
mination proportions due to seasonal changes in seed dormancy
levels (Table 2). These were most visible when seeds were recov-
ered every two months. The seed dormancy level varied widely
depending on the time of burial and on the species concerned
(Table 2, Fig. 2): the maximum variations in the final germination
proportion were observed in Polygonum lapathifolium, from 0.07 to
0.99 depending on the burial dates, while in Matricaria perforata
the germination proportion was always high. For the latter species,
the estimation of germination speed parameters was thus possible
at each recovery date: the germination lag (TT0 ) and the time to
mid-germination (TT50 ) increased in spring when the final propor-
tion of germinated seeds (i.e. the proportion of non-dormant seeds)
and the germination rate (v50 ) at mid-germination decreased, and
vice-versa during summer.
Fig. 2. Variations in the lag time TT0 ( ), time to mid-germination TT50 ( ), germination rate v50 ( ) and final germination percentage () of Matricaria perforata. Seeds
were buried 30 cm deep in June 2006 and were recovered every two months to assess their germination at 15 ◦ C in the light. Each dot represents the mean of three seed bags
each containing 100 seeds.
3.3. Interspecific variations in germination speed parameters
The germination time courses also varied widely in the different
species even when species were compared at their lowest levels of
dormancy. Fig. 3 shows germination time courses obtained when
dormancy was lowest during the two years of the experiment.
Species such as Echinochloa crus-galli or Papaver rhoeas germinated
more slowly and in lower proportions than Amaranthus hybridus or
M. perforata. The species also differed considerably in their values of
TT0 and TT50 . Even when the final proportion of seed germination
was 1, A. hybridus seeds only took 16 ◦ C days to reach mid-
germination while Arabidopsis thaliana seeds required 61 ◦ C·days.
When completing the experimental results with 74 germina-
tion time courses taken from the literature (Table 4), giving a total
dataset of 185 germination time courses for 25 weed species, inter-
specific variations increased. TT50 varied from 11 to 436 ◦ C days.
The germination rate v50 varied from a proportion of 0.0004 (Gal-
ium aparine) to 0.82 (Amaranthus hybridus) germinated seeds per
unit of thermal time. In both datasets (our experiment with buried
seeds and data from the literature), germination speed parame-
ters remained comparable for a given species; for instance, in both
datasets, Ambrosia artemisiifolia and Centaurea cyanus reached mid-
germination at approximately 33◦ C days and Chenopodium album at
70◦ C days.
3.4. Seed traits
Seed traits for comparing species were either measured in the
present study or, when available, taken from the literature. The
measured trait values are summarized in Table 3. Seed dry mass
varied widely, from 0.02 mg in Arabidopsis thaliana to 18.6 mg
in Avena fatua. Species also displayed contrasted seed reserves.
Monocotyledonous species had low lipid contents, from 4 to
14%. Four dicotyledonous species (Arabidopsis thaliana, Capsella
bursa pastoris, Datura stramonium and Papaver rhoeas) presented
a seed lipid content above 30% and their protein contents were
also among the highest. These species were grouped for statistical
analysis as lipid-rich seeds while the other species were considered
as lipid-poor seeds.
 A. Gardarin et al. / Ecological Modelling 222 (2011) 626–636 633

Fig. 3. Fitted germination time courses in the light and at optimal temperatures (see Table 2) when species were at their lowest dormancy level. Seeds were buried 30 cm
deep in 2006 and were recovered every two or six months to study their germinability (the date of recovery is indicated after each species name). Polygonum aviculare and
Fallopia convolvulus were not represented because their seeds remained strongly dormant throughout the experiment. Symbols only serve to differentiate curves and do not
represent actual data points.

Table 5
Correlation between species traits, dormancy level, and germination speed parameters. Regression parameters and R2 of linear model [4] analysed with PROC GLM of SAS.

Explanatory variable

Proportion of Base Seed lipid content (g g−1 ) Area to mass Total R2

non-dormant temperature for ratio of seeds
seedsa germination (◦ C) (mm2 mg−1 )
Intercept logn (m) logn (Tb + 2) logn (lipid), if logn (lipid), if logn
lipid content lipid content (area/mass)
<0.30 ≥0.30

Predicted variables
Germination lag (◦ C days)
logn (TT0 ) 3.56 −0.18 −0.39 −0.23 −1.19 −0.30
Partial R2 0.07 0.08 0.13 0.08 0.41
◦
Time to mid-germination ( C days)
logn (TT50 ) 4.45 −0.25 −0.79 −0.29 −0.86 ns
Partial R2 0.07 0.33 0.16 0.46

Germination rate at mid-germination (◦ C−1 day−1 )

logn (v50 ) −4.77 1.07 1.53 0.50 0.56 ns
Partial R2 0.27 0.25 0.05 0.59

ns: not significant.

a
Proportion of germinated viable seeds in the seed lot for which germination parameters were determined.

Base temperatures for germination ranged from −1.5 ◦ C (Gera-

nium dissectum) to 15.0 ◦ C (Amaranthus hybridus). They were below
5 ◦ C in autumn and winter germinating species and reached 10 ◦ C
in summer germinating species.

3.5. Relationships between seed traits, dormancy and

germination speed parameters

Seed traits and dormancy level explained 41–59% of the vari-

ability in germination speed parameters (Table 5). For each of the
parameters TT0 , TT50 and v50 , the same seed traits were included in
each model with a highly significant effect. Germination was earlier
and faster in non-dormant seeds lots, i.e. TT0 and TT50 decreased
and v50 increased with an increase in the values of m (proportion
of non-dormant seeds). The effect of seed dormancy was great-
est for v50 (high partial R2 ), which justified the introduction of m
as a covariable. Base temperature for germination was similarly Fig. 4. Time from the addition of water to mid-germination (parameter TT50 ) as a
correlated with germination, i.e. TT0 and TT50 decreased and v50 function of species base temperature for germination. Germination results on filter
increased with an increase in the species base temperature (Fig. 4). paper with seeds exhumed at a depth of 30 cm in the field every two or six months
() and data compiled from the literature (♦). Each base temperature value corre-
Base temperature was the factor that explained the largest propor-
sponds to one species, the data points for a given species correspond to different
tion of variance in TT0 and TT50 . seed recovery dates.
634 A. Gardarin et al. / Ecological Modelling 222 (2011) 626–636
The higher the seed lipid content, the earlier and faster the ger-
mination, the highest slope being for lipid-rich seeds (exceeding
30% lipid content). Lipid content was highest for TT0 and TT50 .
Germination lag was the only parameter that increased with an
increase in the seed area to mass ratio, although the contribution
of this factor was small.
The other seed traits (seed mass and protein content) and the
effect of seed exposure to light during germination had no sig-
nificant influence on the germination speed parameters analysed.
Although the shape parameter b of the Weibull equation varied
between species, no consistent relationship was found with any of
the seed traits described in Section 3.4.
Results of fitting to the Eq. (4) were analogous, whether the
whole data set (including literature data, Table 5) was used, or only
data from the species we studied in our experiments (results not
shown). However, the effects of seed lipid content and of the sur-
face to mass ratio were not significant when only the species we
studied were used because of the smaller range of these traits in
our species panel. In all cases, the values of the different regression
parameters were very similar to those shown in Table 5.
4. Discussion
The combination of extensive germination experiments and
the critical selection of previous results from the literature pro-
duced a dataset of germination time courses for a large number
of weed species with contrasted germination characteristics and
seed traits. To our knowledge, the present summary quantita-
tive analysis of such a dataset for weed seed germination has
not previously been attempted. Many general conclusions based
on analyses of the present dataset are not new and are con-
sistent with earlier reports in the literature. For instance, the
relationships between germination time-course parameters and
dormancy observed here have already been reported in literature
for a large range of species (Lonchamp and Gora, 1980; Baskin and
Baskin, 1985; Bouwmeester, 1990). Similar approaches have been
attempted in the past but only at an intraspecific scale (Hilhorst
and Toorop, 1997; Batlla et al., 2003). The novelty of the present
work was to quantify these relationships for predictive purposes at
the multi-species scale.
Our comprehensive dataset also enabled us to compare a vari-
ety of species, and our general observations are also consistent
with those of previous studies. The earlier and faster germination
of Amaranthus hybridus than in Galium aparine confirmed observa-
tions by Lauer (1953). The main result of the present work was to
correlate interspecific differences in germination timing and rates
with species traits. A relationship between earliness of germination
and the seed lipid content was found, which to our knowledge, has
not previously been observed. However, a reverse correlation was
found between seed lipid content and germination rate, but at low
dioxygen concentrations (Al-Ani et al., 1985; Raymond et al., 1985).
The relationship between TT0 and TT50 and lipid content observed
here was valid for species over a large range of seed lipid contents,
varying from 3.5% (Fallopia convolvulus) to 43.6% (Papaver rhoeas).
This trait appears to be relatively constant in a given species. Indeed,
the seed lipid contents measured here are similar to those reported
in the literature (Earle and Jones, 1962; Jones and Earle, 1966;
Barclay and Earle, 1974).
In contrast, no relationship was found with seed protein content.
This characteristic was less contrasted than lipid content among the
species we studied. Moreover, total seed protein content strongly
depends on seed production conditions (Fawcett and Slife, 1978).
For instance, we measured a seed protein content of 23% in Capsella
bursa-pastoris, whereas values of 12% (Schroeder et al., 1974) and
33% (Jones and Earle, 1966) were reported in the literature. More-
over, specific protein contents (such as those involved in repairing
processes and reserves mobilization, Bewley, 1997) could be more
appropriate for establishing correlations with germination charac-
teristics.
The second seed trait to be positively correlated with germi-
nation, TT0 , was the area to mass ratio. We hypothesized that
germination timing partly depended on the time required for seed
imbibition. Imbibition should be faster in seeds with a large area for
water to enter relative to seed water demand, probably linked to
seed mass. However, although logical, the present correlation only
explains a small proportion of the variability in the germination
rate and should be tested on a larger number of species.
Germination was also shown to be faster in species with a high
base temperature for germination. This effect could a priori appear
as an artefact resulting from the use of thermal time with differ-
ent base temperatures, because less thermal time is accumulated
to reach a given proportion of germination when thermal time is
summed with an increased base temperature. However, this corre-
lation remained unchanged when the analysis was performed with
time units expressed in days, independently of the calculation of
thermal time (results not shown). Moreover, a similar correlation
has already been reported for the emergence of crop species (Angus
et al., 1981) and the development of invertebrates (Trudgill et al.,
2005). This relationship indicates that species requiring high tem-
perature germinate faster than those germinating earlier at low
temperatures. This could be considered as an ecological adapta-
tion of late germinating species to develop faster and to compete
with early germinating species. Thus, both types of species achieve
germination and subsequently grow and develop in quite a similar
time considering the range of temperatures in which they each ger-
minate in field conditions. In order to explain this trade-off between
base temperature and thermal time required for a particular pro-
cess, Trudgill et al. (2005) suggested a mechanism based on the fact
that enzymes are more efficient at high temperatures.
In the present analysis, germination speed parameters were
not correlated with the presence vs. absence of light during the
experiment. However, numerous studies have reported faster ger-
mination in the light for several weeds (Jensen, 1995; Milberg,
1997; Colbach et al., 2002; Batlla and Benech-Arnold, 2005). In
the present work, the effect of light on the speed of germina-
tion was taken into account indirectly via the correlation with the
proportion of germinated seeds, which was usually higher when
the seeds were exposed to light. Indeed, the role of light as a
dormancy-terminating factor favouring an increment in percent-
age germination of light-requiring species is widely reported in the
literature (Andersson et al., 1997; Milberg and Andersson, 1998;
Benech-Arnold et al., 2000). The analysis of seasonal variations in
the final germination percentages was the objective of a different
study and was not analysed here.
Although several of the factors we studied had a highly sig-
nificant effect, a large proportion of variability in germination
remained unexplained. Part of this variability may result from
genetic differences in seed germination timing between seed popu-
lations (e.g. Christal et al., 1997), but the main source of variability
between seed lots is seed production conditions (Andersson and
Milberg, 1998; Luzuriaga et al., 2006; Swain et al., 2006), e.g. crop
sowing date, soil fertilization, or climatic conditions. The model
resulting from our study could be improved by the study of other
seed traits such as soluble sugar contents or seed coat characteris-
tics that control the entry of water into the seed during imbibition.
Such relationships could be used to estimate germination speed
parameters for species that were not analysed in the present study.
Nor did we consider seasonal variations in base temperature within
a species associated with changes in dormancy in the present study,
as we did not have sufficient data to use other values than a constant
one. Such variations have been described only in a small num-
 A. Gardarin et al. / Ecological Modelling 222 (2011) 626–636
ber of species (Batlla and Benech-Arnold, 2007) and are difficult
to extrapolate to the wide range of weed species we studied.
The weed flora present in a particular field result from several
factors linked with the cropping system in interaction with seed
germination. The date of seed germination, and then emergence,
is important for future crop-weed competition and the ability of
the weed to replenish the seedbank. Relationships for predicting
germination behaviour aimed at being integrated as part of a com-
prehensive weed dynamics model including many other life cycle
processes. Multi-species weed dynamics models could be used to
evaluate different crop management techniques, as well as to pre-
dict the long-term shifts in weed flora resulting from modifications
in cropping systems in a large range of environmental conditions.
Acknowledgements
The present work was financed by INRA (Département Environ-
nement et Agronomie) and the Region of Burgundy. The authors
are grateful to Hugues Busset, Émilie Cadet and Arnaud Coffin for
their technical assistance, Christophe Salon and Anne-Lise Santoni
(UMR LEG), Annick Matejicek (UMR BGA) and Lionel Bretillon and
Stéphane Gregoire (UMR FLAVIC) for seed reserve analysis and to
the Station Nationale d’Essais des Semences and Vincent Murracciole
for seed image analysis. We also thank one reviewer for his detailed
comments that helped us improve this paper.
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