SEED GERMINATION BIOLOGY OF
SPINELESS HOPSAGE: BETWEENPOPULATION DIFFERENCES IN
DORMANCY AND RESPONSE TO
TEMPERATURE
Susan E. Meyer
Rosemary L. Pendleton
ABSTRACT
collections from warmer winter sites. Similar but more
complex relationships have been found for several Intermountain perennial herb species, including penstemons,
flax, and yarrow. All of these species are generalists that
occur over a wide range of soil types as well as climates.
In the present study, the aim was to examine betweenpopulation variation in germination pattern as a function
of climate at the seed collection site for an edaphically
specialized chenopod shrub, spineless hopsage (Grayia
brandegei). In previous studies with other shrub species
we have found that germination patterns vary as a function of climate, not as a function of taxonomic relatedness
within a species. This suggests that selection pressure for
an appropriate germination timing mechanism is strong,
so that differentiation among populations may take place
over few generations. If this is true for spineless hopsage,
we would expect differentiation as a function of climate to
be easily detectable.
Spineless hopsage (Grayia brandegei) is an edaphically
restricted chenopod shrub that occurs over a range of climates within the Colorado Plateau and adjacent areas.
Seed germination patterns for collections from six locations were related to winter severity at the collection site.
Cold-winter collections were generally more dormant and
germinated more slowly at low temperature than warmwinter collections. Bract removal decreased dormancy, but
relative differences among collections were maintained.
Results suggest ecotypic differentiation among populations
with regard to establishment strategy.
INTRODUCTION
Seedling establishment is a critical stage in the plant
life cycle, especially for species that reproduce largely
from seed (Angevine and Chabot 1979). In semiarid systems the seasonal window for successful establishment is
often narrow, so that mechanisms for timing germination
appropriately become more important (Rathcke and Lacey
1985).
One approach to elucidating these timing mechanisms
in relation to climate is to compare germination patterns
among populations of species that occur over a range of
climatic types (Meyer and others 1987; Thompson 1973).
This has the effect of holding most other aspects of life
history essentially constant in the comparison, facilitating
the detection of climate-related variation (Venable 1984).
In work with rubber rabbitbrush (Chrysothamnus nauseosus) and big sagebrush (Artemisia tridentata), clear
relationships between collection site climate characteristics and seed geFmination patterns have emerged (Meyer
and others 1989; Meyer and Monsen, in press; Meyer
and Monsen, this proceedings). Collections from heavysnowpack, cold-winter sites tend to be more dormant at
autumn temperatures and to germinate more slowly under temperatures representing snowpack conditions than
METHODS
Seed collections were made during September of 1987
and 1988 at six locations in Utah and Wyoming (table 1).
Collection sites were selected on the basis of seed availability; seed is produced only sporadically at many locations. The 1987 seed was stored unsealed under laboratory conditions for approximately 3 months prior to
the initiation of the first series of experiments. When
the seed had been in laboratory storage approximately
5 months, half of each lot was placed in deepfreeze storage at -80 octo halt afterripening processes. After 9
additional months (14 months total) another series of
experiments was carried out on both freezer-stored and
laboratory-stored seed. Experiments on 1988 seedlots
were carried out after approximately 3 months in laboratory dry storage.
Spineless hopsage fruits are one-seeded and are borne
in papery bracts. For experiments using intact (bracted)
fruits, filled fruits were selected on a light table. For
experiments using debracted fruits, bracts were removed
using gentle hand rubbing, and sound fruits were selected
by hand following blowing to remove bract debris.
For each experimental treatment, four replications of
25 fruits were used. The fruits were placed on top of two
germination blotters in 100-mm plastic petri dishes. The
dishes were incubated in the dark but were exposed to
Paper presented at the Symposium on CheatgTass Invasion, Shrub DieOff, and Other Aspects of Shrub Biology and Management, Las Vegas, NV,
April 5-7, 1989.
Susan E. Meyer and Rosemary L. Pendleton are Ecologists at the
Intermountain Research Station, Forest Service, U.S. Department of
Agriculture, Shrub Sciences Laboratory, Provo, UT 84606.
187
This file was created by scanning the printed publication.
Errors identified by the software have been corrected;
however, some errors may remain.
Table 1-Collection information for spineless hopsage seed collections used in germination
experiments
Location
Aneth, UT
Antelope Valley, UT
Baggs, WY
Grand Wash, UT
Henrieville, UT
Long Canyon, UT
Latitude
37°19'N
39°13'N
41°02'N
38°15'N
37°34'N
37°54'N
Longitude
109°19'W
111°45'W
107°40'W
111°14'W
112000'W
111°15'W
Elevation
Mean January
temperature
Meters
oc
1,455
1,660
1,940
1,750
1,850
1,660
cool-white fluorescent light during reading, and were
watered as necessary to maintain moist conditions. Germinated seedlings were counted and removed at least
weekly. Radicle protrusion was the criterion for germination. At the end of each experiment ungerminated fruits
were evaluated using tetrazolium chloride or cut test
procedures to determine viability (Association of Official
Seed Analysts 1988). Because tetrazolium staining and
cut testing gave comparable results in the first experiment, a cut test was used in all subsequent work. Germination percentages were converted to a percentage of
viable seed basis for each experimental unit (petri dish)
prior to analysis.
In the first experiment, intact and debracted fruits of
the 3-month-old 1987 collections were incubated at 15,
20, 25, and 30 oc constant temperature for 4 weeks. The
3-month-old 1987 collections were also incubated at 1 °C
for 15 weeks. The 15-week low-temperature incubation
period was followed by a 2-week incubation period at
15 oc prior to viability evaluation of ungerminated fruits
in this and other low-temperature experiments.
At the end of 14 months in storage, the deepfreezestored seed (5 months old in terms of afterripening) and
the laboratory-stored seed (14 months old) were subjected
to additional experiments. Intact and debracted fruits of
each of the four 1987 collections were incubated at 15 °C
for 4 weeks and at 1 °C for 15 weeks to examine the effects of seed age on dormancy and germination rate in
the cold.
Intact and debracted fruits of the 3-month-old 1988
collections were also incubated at 15 °C for 4 weeks and
at 1 °C for 15 weeks. In addition, a chill experiment using
intact fruits only was performed. Fruits were imbibed on
blotters in petri dishes as before and subjected to 0, 2, 4,
and 8 weeks of chilling "at 1 °C prior to incubation for
4 weeks at 15 °C.
Analysis of variance was carried out using appropriate
designs for the constant temperature experiment, the
experiment examining the effects of seed age on germination at 15 °C, and the chill experiment. Data were
arcsine-transformed prior to analysis, but original untransformed values are given in the figures.
Results of the low-temperature germination experiments were examined using linear regression techniques.
Number of weeks to 30 percent germination at 1 °C was
interpolated from rate curves for each seedlot and treatment. This value was plotted against mean January
temperature at each seed collection site. Mean January
-0.6
-3.9
-8.3
-2.2
-3.3
-1.1
Collection
years
1987
1987,88
1987,88
1988
1988
1987
temperature was obtained by interpolation on isotherm
maps and corroborated with data from nearby weather
stations when available (Water Information Center 1974).
Regression analysis was also used to examine the relationship between seed dormancy at 15 °C and collectionsite mean January temperature. Data from 1987 and
1988 collections were pooled for this analysis as well as
for analysis oflow-temperature germination response of
3-month-old bracted fruits.
RESULTS
In the first germination experiment, main effects due
to incubation temperature, bract removal, and seed collection were all highly significant (table 2). Germination
was highest at low (15 °C) and high (30 °C) temperatures
with depression at intermediate temperatures (fig. 1).
Table 2-Analysis of variance probability levels for significance of main effects and interactions F values
in germination experiments on incubation temperature, seed age, and prechill. Values are
reported as not significant (n.s.) if probability
values exceed 0.05
Source of variation
Probability level
Incubation temperature experiment
Temperature main effect
Seed collection main effect
Bract main effect
Temperature x collection
Temperature x bract
Collection x bract
Temperature x collection x bract
0.0001
.0001
.0001
.0001
n.s.
.0042
n.s.
Seed age experiment
Seed age main effect
Seed collection main effect
Bract main effect
Seed age x collection
Seed age x bract
Collection x bract
Seed age x collection x bract
0.0001
.0001
.0001
.0009
n.s.
.0084
.0001
Prechill experiment
Prechill main effect
Seed collection main effect
Prechill x seed collection
188
0.0001
.0001
.0369
100
1.&.1
(!)
~
•
80
discernible. The anomalous behavior of the Grand Wash
collection obscures the pattern. This intermediate-winter
collection was as dormant as the cold-winter Baggs collection without chill, but responded dramatically to a chill
as short as 2 weeks (fig. 5). Collections made in different
years from the same location behaved similarly.
Germination rate in the cold was significantly correlated with collection-site mean January temperature
when 3-month-old bracted fruits were tested and data
from both years of collection were combined (fig. 7). The
relationship was stronger for 1987 than for 1988 collections. The cold-winter Baggs collections germinated more
slowly than the warm-winter Aneth and Long Canyon
collections. Collections from intermediate sites showed
more variation.
o 15 •c
~
IZ25I
2o•c
25•c
30 •c
1.&.1
(.)
0:::
1.&.1
60
a..
z
0
~
40
ffi
20
:i
(!)
0
MEAN
INTACT FRUITS
DEBRACTED FRUITS
Figure 1-Mean germination response (averaged
across four 1987 collections) to a range of constant temperatures for intact and debracted fruits
of spineless hopsage.
100
1.&.1
(!)
~
Debracted fruits germinated better than intact fruits at all
temperatures and showed a similar pattern of temperature
response. All seed collections showed considerable dormancy, especially when fruits were left intact.
Seed collections showed contrasting responses to temperature (fig. 2). The warm-winter Aneth collection was
least temperature sensitive, with only a minor depression
at intermediate temperatures, while the Long Canyon collection showed a major depression. The Antelope Valley
collection germinated best at 15 °C, showing depressed
germination at all higher temperatures. The cold-winter
Baggs collection showed the opposite response, germinating best at the highest temperature. Temperature response patterns for each collection were similar for intact
and debracted fruits.
Dormancy at 15 oc decreased significantly as a function
of seed age (table 2). The effect was similar for intact
and debracted fruits, although debracted fruits were less
dormant overall (fig. 3). Seed collections afterripened
at different rates (fig. 4). Intact fruits of the Aneth collection were almost completely nondormant when tested at
14 months, while Baggs intact fruits were still 50 percent
dormant. Debracted fruits of all but the Baggs collection
were essentially nondormant at 14 months.
Dormancy of 3-month-old 1988 collections was significantly decreased by chill, although the efficacy of chill
varied by seed collection (table 2). An 8-week chill removed most dormancy in the Grand Wash, Henrieville,
and Antelope Valley collections, while the cold-winter
Baggs collection responded poorly to short and intermediate chill periods (fig. 5). When the 1988 Baggs collection
was removed from the 15-week low-temperature experiment and incubated at 15 °C, it germinated fully, indicating that longer chill was the requisite for complete removal
of dormancy.
Seed collections from warm-winter sites generally
showed less dormancy than cold-winter collections when
tested at 15 °C as 3-month-old intact fruits (fig. 6). Although the relationship between collection-site mean
January temperature and germination of intact fruits
at 15 oc was not statistically significant, a trend is
o
•
~
80
IZ25I
15 •c
2o•c
2s•c
30 •c
1.&.1
(.)
ffi
60
a..
z
0
~
40
0:::
20
:i
1.&.1
(!)
0
AN
LC
AV
AN
BA
INTACT FRUITS
LC
AV
BA
DEBRACTEO FRUITS
Figure 2-Germination response to a range of
constant temperatures for intact and debracted
fruits of four 1987 accessions of spineless hopsage. (AN= Aneth, LC =Long Canyon, AV =
Antelope Valley, BA = Baggs.)
DEBRACTED FRUITS
INTACT FRUITS
CJ 3MONTHS
-
5MONTHS
~
14MONTHS
Figure 3-Mean germination percentage (averaged across four 1987 collections) at 15
for
intact and debracted spineless hopsage fruits
after 3, 5, and 14 months in laboratory dry
storage.
oc
189
2251 MEAN
100
.
50
0
~
R-SQUARED - 0.282 n.L
-
..- 40
80
60
30
40
20
•
10
•
•
0+------.~------r------.-------r--------,
AN
LC
IN
1M
AN
Cl 3 lotONTHS
-
LC
AV
-10
1M
5UONTHS
-
100
z
~
~
0
e
1988 COLLECTlONS
15
•..-
-
80
z
0
~ 10
60
2
ffi
0
~
-2
0
!<
I
-4
Figure 6-Germination response at 15 oc for
eight collections of spineless hopsage plotted as
a function of mean January temperature at the
seed collection site.
0
Ill)
-6
.A. 1987 COLLECTIONS
I5:SI 14 lotONTHS
Figure 4-Germination response at 15 oc for
intact and debracted fruits of four 1987 spineless
hopsage collections after 3, 5, and 14 months in
laboratory dry storage. (AN = Aneth, LC = Long
Canyon, AV =Antelope Valley, BA =Baggs.)
.
-8
COLLECTION SITE MEAN JANUARY TEMPERATURE (•c)
DEBRACTED FRUITS
INTACT FRUITS
·",..,~
40
5
~
20
(/)
:1&::
~
R-SQUARED - 0.45:S.
~ 0~--~----~--~----~--~
HV
GW
AV
-10
-8
-6
-4
-2
COLLECTION SITE MEAN JANUARY TEMPERATURE (•c)
BA
Cl NO CHILL
-
2-WEEK CR.1.
1111 8-WEEK CHU
.A. 1H7 COUECTIONS
•
0
1811 COUECTlONS
Figure 5-Germination response at 15 oc after
prechill at 1 oc for four 1988 collections of spineless
hopsage. (HV = Henrieville, GW = Grand Wash,
AV =Antelope Valley, BA =Baggs.)
Figure 7-Weeks to 30 percent germination at
1 oc for eight collections of spineless hopsage
plotted as a function of mean January temperature at the seed collection site.
Seed age and fruit debracting had marked effects on
the germination rate of some 1987 collections in the cold
(fig. 8). When 3-month-old fruits were tested, the relationship between collection-site mean January temperature
and germination rate in the cold was significant for both
intact and debracted fruits. After 5 months in storage,
the relationship for debracted fruits was no longer significant. After 14 months in storage there was little variation among collections for either intact or debracted fruits.
Most of the change in the plotted regression lines is due
to change in the cold-winter Baggs collection, whose lowtemperature germination rate was strongly accelerated
both by increasing seed age and by debracting.
DISCUSSION
The general germination pattern for spineless hopsage
is basically similar to patterns for many other chenopod
shrubs of the Intermountain area. The seeds are often
largely dormant, at least at temperature regimes characteristic of the season of dispersal, but become more garminable over relatively short periods in dry storage. Such
results have been reported for winterfat (Ceratoideslanata),
with afterripening periods of as little as 1 to 3 months sufficient for complete dormancy removal (Springfield 1972).
Many species of Atriplex (saltbush), including fourwing
saltbush (A canescens) (Springfield 1970), desert holly
(A hymenelytra) (Kay and others 1988), and broadscale
190
-
10
•r-
~
~
'010
-
INTACT FRUITS 3 MONTHS
(,)
RSQUARED•0.857•
a
-l5
RSQUARED•0.90g.
~
f5C)
~
4
UJ
2
~
2
0
-10
~
-5
10
s•
z 8
:i 6
6
~
I
DEBRACTED FRUITS J MONTHS
0
I ...
~
•....
z
0
~ ...
~
~
~
~
4
2
en
~
I
~
~
-5
--
10
•
i
RSQ~0.282
a
s•...
-
n.a.
~
8
I
~
~
I
2
0
-10
0
5
DEBRACTED FRUITS 14 MONTHS
RSQUARED-O.a40t
a
8
...
I ...
2
~
0
-10
-5
10
INTACT FRUITS 14 MONTHS
(,)
z
0
5
0
5
RSQUAR£0•0.552 n.a.
8
:i 6
0
DEBRACTED FRUITS 5 MONTHS
•....
RSQUARED•O.a61 •
8
i
!i
-5
u-10
INTACT FRUITS 5 UONTHS
a
0
-10
5
0
~
-5
0
5
I
COLLECTION SITE UEAN JANUARY TEMPERATURE (ec)
2
0
-10
-5
0
5
COLLECTION SITE UEAN JANUARY TEUPERATURE (-t)
Figure 8-Weeks to 30 percent germination at 1 oc plotted as a function of mean January temperature for intact and debracted fruits of four 1987 spineless hopsage collections placed in cold incubation after 3, 5, and 14 months of laboratory dry storage.
and Mojave Desert collections of spiny hopsage are nondormant, while Belcher (1985) mentioned that fresh
seed often requires chilling to break dormancy. Similarly,
Springfield (1970) reported that dormant northern New
Mexico collections of fourwing saltbush do not respond to
chill, while data generated in our laboratory indicate that
cold-winter central Utah collections show increasing germination with chills up to 25 weeks in duration.
Germination response to temperature also varies
among seed collections within species such as fourwing
saltbush (Springfield 1970) and spiny hopsage (Wood and
others 1976). Optimum temperatures are usually low,
(A obovata) (Edgar and Springfield 1977), also undergo
afterripening in dry storage. The ability to respond to
short moist chiii as a substitute for dry afterripening is
also common in many of these shrubs. Examples include
Gardner saltbush (A gardneri) (Ansley and Abernethy
1985), winterfat (Allen and others 1987), and spiny hopsage (Grayia spinosa) (Belcher 1985).
Between-population variation in germination attributes
of chenopod shrubs is also frequently encountered, although systematic study of this variation is less frequent
(Meyer and others 1987). For example, Wood and others
(1976) reported that the seeds of several Lahontan Basin
191
Johnson, G. B.; Raven, P. H., eds. Topics in plant population biology. New York: Columbia University Press:
188-206.
Ansley, R. J.; Abernethy, R. H.1985. Environmental factors influencing Gardner saltbush seed dormancy alleviation. Journal of Range Management. 38: 331-335.
Association of Official Seed Analysts. 1988. Rules for
testing seeds. Journal of Seed Technology. 12(3).
Belcher, E., ed. 1985. Handbook on seeds of browseshrubs and forbs. Gen. Tech. Publ. R8-TP8. Atlanta,
GA: U.S. Department of Agriculture, Forest Service,
Southern Region.
Edgar, R. L.; Springfield, H. W. 1977. Germination characteristics ofbroadscale: a possible saline-alkaline site
stabilizer. Journal of Range Management. 30: 296-298.
Kay, B. L.; Graves, W. L.; Young, J. A. 1988. Long-term
storage of desert shrub seed. Mojave Revegetation
Notes 23: 1-22. Davis, CA: University of California,
Davis, Agronomy and Range Science.
Meyer, S. E.; McArthur, E. D.; Jorgensen, G. L. 1989.
Variation in germination response to temperature in
rubber rabbitbrush (Chrysothamnus nauseosus: Asteraceae) and its ecological significance. American Journal
of Botany. 76: 981-991.
Meyer, S. E.; McArthur, E. D.; Monsen, S. B. 1987. Infraspecific variation in germination patterns of rangeland
shrubs and its relationship to seeding success. In:
Frasier, G. W.; Evans, R. A., eds. Seed and seedbed
ecology of rangeland plants: Proceedings of the symposium; 1987 April 21-23; Tucson, AZ. Springfield, VA:
U.S. Department of Agriculture, Agricultural Research
Service: 82-92.
Meyer, S. E.; Monsen, S. B. [In press]. Habitat-correlated
variation in mountain big sagebrush (Artemisia tridentata ssp. vaseyana) seed germination patterns. Ecology.
Philippi, T.; Seger, J. 1989. Hedging one's evolutionary
bets, revisited. Trends in Ecology and Evolution. 4:
41-44.
Rathcke, B.; Lacey, E. P. 1985. Phenological patterns of
terrestrial plants. Annual Review of Ecology and Systematics. 16: 179-214.
Springfield, H. W. 1970. Germination and establishment
offourwing saltbush in the Southwest. Res. Pap. RM55. Fort Collins, CO: U.S. Department of Agriculture,
Forest Service, Rocky Mountain Forest and Range Experiment Station. 48 p.
Springfield, H. W. 1972. Winterfat fruits undergo afterripening. Journal of Range Management. 25: 69-70.
Thompson, P. A. 1973. Geographical adaptations of seeds.
In: Heydecker, W., ed. Seed ecology. London: Butter
worths: 31-58.
Venable, D. L. 1984. Using intraspecific variation to study
the ecological significance and evolution of plant life
histories. In: Dirzo, R.; Sarukhan, J., eds. Perspectives
in plant population ecology. Sunderland, MA: Sinauer
Associates: 166-187.
Water Information Center. 1974. Climates of the States.
II. Western States. Port Washington, NY: Water Information Center. 975 p.
Wood, M. K.; Knight, R. W.; Young, J. A. 1976. Spiny hopsage germination. Journal of Range Management. 29:
53-56.
however, and the bimodal response to temperature seen
in spineless hopsage is unusual. It somewhat resembles
the response of rubber rabbitbrush, which is nondormant
at high temperatures but often dormant at intermediate
temperatures characteristic of autumn, as well as at
lower temperatures (Meyer and others 1989). Chill removes this conditional dormancy, so that germination
at low temperature ultimately surpasses intermediatetemperature germination, resulting in a bimodal temperature response. To invoke this explanation for spineless
hopsage, the 15 °C regime would need to be within the
chilling range for this species.
Variation in spineless hopsage germination response
to temperature makes sense from an ecological viewpoint.
Seeds of warm-winter populations such as Aneth are relatively nondormant and are programmed to germinate
opportunistically with regard to temperature. They probably germinate during the fall rains and spend the relatively mild winter as seedlings. Seeds of cold-winter
populations such as Baggs may be germinable at high
temperature soon after dispersal, but they are largely
dormant under prevailing temperature regimes and at
tern peratures found under snowpack. They probably
become germinable in early spring after experiencing
winter chill. Seeds of collections from sites with less predictable winters are less predictable in their germination
response. These populations probably have more phenotypic plasticity in germination response, as a bet-hedging
strategy in the face of environmental uncertainty
(Philippi and Seger 1989).
The role of dry afterripening under field conditions for
this species is not known. It may be part of the predictive
dormancy mechanism, or it may be a process that is not
ecologically relevant because field seedbed conditions
trigger germination through other processes (such as
chill) before dry afterripening can come into play. It
is not known whether there is any seedbank carryover
from year to year, but the fact that relatively short chill
renders most seeds germinable suggests that this is unlikely in most years. It is possible that some dormancyinduction mechanism functions in the field to increase the
probability of seed carryover, but we have no laboratory
evidence that this might be so.
Between-population variation in germination patterns
in spineless hopsage appears to be correlated with variation in climatic conditions at the seed collection site.
This suggests strong selection pressure for adaptive
germination-timing strategies in response to climate, a
result consistent with findings for other autumn-fruiting
Intermountain shrubs with wide ranges of climatic adaptation. Field-emergence experiments with collections
from a wider selection of sites would clarify the role of
variation in germination patterns in the establishment
strategy of this species.
REFERENCES
Allen, P. S.; Meyer, S. E.; Davis, T. D. 1987. Determining
seed quality ofwinterfat (Ceratoides lanata [Pursh]
J. T. Howell). Journal of Seed Technology. 11: 7-14.
Angevine, M. W.; Chabot, B. F. 1979. Seed germination
syndromes in higher plants. In: Solbrig, 0. T.; Jain, S.;
192