Seed weight variation of wyoming sagebrush in Northern Nevada
Carlos A. Busso* and Barry L. Perryman**
* Departamento de Agronomia-CERZOS (CONICET), Universidad Nacional del Sur, Bahia Blanca, Buenos Aires, Argentina
** Department of Animal Biotechnology, College of Agriculture, Biotechnology and Natural Resources, Mail Stop 202,
University of Nevada, Reno, Nevada, USA.
Address correspondence to: Dr. Carlos A. Busso. Departamento de Agronomia-CERZOS (CONICET), Universidad Nacional del Sur, Altos del Palihue, (8000) Bahia Blanca, Pcia. Buenos Aires, ARGENTINA. Fax: (+54-291) 459 5127. E-mail: cebusso@criba.edu.ar
ABSTRACT: Seed size is a crucial plant trait that may potentially affect not only immediate seedling success but also the subsequent generation. We examined variation in seed weight of Wyoming sagebrush (Artemisia tridentata ssp. wyomingensis Beetle and Young), an excellent candidate species for rangeland restoration. The working hypothesis was that a major fraction of spatial and temporal variability in seed size (weight) of Wyoming sagebrush could be explained by variations in mean monthly temperatures and precipitation. Seed collection was conducted at Battle Mountain and Eden Valley sites in northern Nevada, USA, during November of 2002 and 2003. Frequency distributions of seed weight varied from leptokurtic to platykurtic, and from symmetry to skewness to the right for both sites and years. Mean seed weight varied by a factor of 1.4 between locations and years. Mean seed weight was greater (P<0.05) in 2003 than in 2002 at both sites. This can partially be attributed to 55% greater precipitation in 2003 than 2002, since mean monthly temperatures were similar (P>0.05) in all study situations. Simple linear regression showed that monthly precipitation (March to November) explained 85% of the total variation in mean seed weight ( P=0.079). Since the relationship between mean monthly temperature (June-November) and mean seed weight was not significant (r2=0.00, P=0.431), this emphasizes the importance of precipitation as an important determinant of mean seed weight. Our results suggest that the precipitation regime to which the mother plant is exposed can have a significant effect on sizes of seeds produced. Hence, seasonal changes in water availability would tend to alter size distributions of produced offspring.
Keywords: Artemisia tridentata ssp. wyomingensis. Climate effects. Rangeland restoration. Seed size.
Introduction
Wyoming big sagebrush (Artemisia tridentata ssp. wyomingensis Beetle and Young) has a wide ecological
amplitude (Beetle and Johnson, 1982) in the western
United States. It helps prevent erosion, provides wildlife
habitat and forage, and improves rangeland aesthetics
(Vale, 1974). Knowledge about the ecophysiology
of Wyoming sagebrush will contribute to a more efficient
use of this species in degraded rangeland restoration
activities of the Intermountain West Region of North
America. Western rangelands cannot be restored without
native plant materials.
Seed size is a crucial plant trait, associated with
the ability of species to disperse and establish, seed water
relations and carrying attributes of the adult plant such
us growth form and plant height (Leishman et al., 2000).
Moreover, carry-over effects have been described for
some species: plants originating from smaller seeds produce smaller seeds than those originating from larger
seeds (Ahmed and Zuberi, 1973). Seed size may potentially
affect not only immediate seedling success but
also the subsequent generation (Wulff, 1986b). The effect
is usually inversely proportional to seed number
per unit biomass, across species in a given community
(Henery and Westoby, 2001). Giles (1995) proposed that it is not a particular seed size that characterizes a genotype
but a particular distribution of size.
Considerable variation in seed size has been reported
across shrub populations within a species, and
even within populations (Vaughton and Ramsey, 1998).
Since most species exhibit continuous variation in seed
size (Manasse and Stanton, 1991), it has been suggested
that the within-plant seed size variation may have
evolved as a strategy in a spatially or temporally unpredictable
environment where a single intermediate seed
size has low fitness (Silvertown, 1984).
Maier et al. (2001) concluded that climatic conditions
supporting widespread pulses of big sagebrush
[Artemisia tridentata Nutt.; a regionally dominant shrub
species over large areas of the Intermountain West
(McArthur et al., 1979)] establishment on native sites
should be examined in greater depth. They reported
strong evidence that precipitation variables significantly
affect high levels of seedling recruitment on native,
undisturbed big sagebrush sites throughout Wyoming.
Additionally, successful recruitment of big sagebrush
is partially dependent on seed viability (McDonough
and Harniss, 1974). Determination of specific precipitation
and temperature conditions favorable for greater
seed sizes in big sagebrush are then of primary importance.
Greater seed sizes often contribute to better sagebrush
seedling establishment (Geritz, 1995). Infrequent
patterns of sagebrush seedling establishment have been
attributed, at least in part, to periods of unfavourable
weather (Lommasson, 1949), but little supporting evidence
has been available.
It is likely that temporal and spatial patterns of seed
size variation in plant species, with subsequent consequences
in seedling establishment, would reflect climatic
fluctuation (Wulff, 1986a). Thus, we hypothesized that
a major fraction of the temporal variability in seed
weight variation could be explained by variations in the
regional climate. Analysis of such frequency patterns
will permit the identification of particular climatic elements
that influence, for example, reproductive success.
These climatic elements should be related to particular
physiological or ecological processes within the population.
The analysis will serve, for example, to test existing
hypotheses about the causes of recruitment variability
in this species.
Our goal was to examine the current unexplored
within-species variation in seed weight in Wyoming
sagebrush. This shrub was chosen because it is an excellent
candidate species for rangeland restoration. The
working hypothesis was that a major fraction of spatial
and temporal variability in seed weight variation could
be explained by variations in mean monthly temperatures
and precipitation. The specific objective was to determine
seed weight distribution, and effects of monthly
precipitation and mean monthly temperature on mean
seed weight in populations of Wyoming sagebrush.
Materials and Methods
Study Area
Seed collection was conducted at two sites during
2002 and 2003: Izzenhood Ranch Site and Eden Valley
Site. Mature Wyoming sagebrush stands were sampled
near Battle Mountain, Lander County, Nevada (116°58'
N, 40°57' W), and Winnemucca, Humboldt County,
Nevada (117°23' N, 41°12' W). The first site was in the
BLM Elko District, approximately 40 km north/northwest
of the town of Battle Mountain, Nevada (NV). The
second site was in the BLM Winnemucca District, between
the Hot Springs Range and Osgood Mountains,
approximately 38 km north/northwest of the town of
Golconda, NV.
At Izzenhood Ranch, the study area consisted of
approximately 23 ha of Bureau of Land Management
(BLM) land with 0-2% slope. Elevation was between
1350-1740 m. Enko-Shabliss-Orvada was the predominant
soil series association (very fine sandy loam and
fine sandy loam). Vegetation composition included Wyoming
big sagebrush, Thurber needlegrass (Stipa
thurberiana Piper) and Indian ricegrass (Achanatherum
hymenoides [Roem. and Schult.]) (USDA-NRCS, 1992);
cheatgrass (Bromus tectorum L.) and tumblemustard
(Sisymbrium altissimum L.) dominated this site. Mean
annual precipitation is 203-254 mm (USDA-NRCS,
PRISM Climate Mapping Project, 1998). At Eden Valley
site, the research area consisted of approximately 42 ha
of BLM land on a 0-8% east-facing hillslope. Elevation
was between 1500-1740 m. Hunnton-Zevadez-Enko was
the predominant soil series association (very fine sandy
loam and fine sandy loam). The vegetation composition
for the site included: Wyoming big sagebrush, Sandberg
bluegrass (Poa secunda Presl.), and Bottlebrush
squirreltail (Elymus elymoides [Raf.] Swezey) (USDANRCS,
1992). As in the first site, cheatgrass and
tumblemustard were dominant. Average annual precipitation
is between 254 and 305 mm (USDA-NRCS,
PRISM Climate Mapping Project, 1998).
Within each site and year, seed collection stands
were selected for similar size of Wyoming big sagebrush
plants, similar cover and topography, and absence of excessive grazing or other disturbances. Sites were also
selected to minimize supplemental moisture or subsurface
runoff due to microsite influences to reduce variations
in demography between sites (Bonham et al.,
1991). Climatic data, as monthly values of temperature
(June-November) and precipitation (March-November)
for the periods 2002 and 2003 were obtained from National
Weather Service climate stations located in Battle
Mountain and Paradise Valley, the closest to the sampled
sites. Temperature or precipitation values were taken
beginning in June or March, respectively, because
flowerstalks or initiation of leaf growth were reported
for this species during these months in Nevada (Everett et al., 1980). November was used as the endpoint because
seed collections were initiated. Although climatic
conditions at individual sites undoubtedly differ from
those at the weather stations, the direction and magnitude
of major climatic variations should be similar
throughout the area.
Field and laboratory methods
Seeds were sampled from a minimum of 100 randomly
selected, similar-size sagebrush plants at each
location and year. At the first site, sampling was conducted
along a transect of at least 10 km because of the
patchy distribution of sagebrush. In Eden Valley, sampling
was conducted along a 5 km-transect.
Fruits were air-dried and stored at 4ºC until use
(Welch et al., 1996). Seeds (achenes) were then hand
picked using a magnifier glass, and stored in paper bags
at 4 °C until tested. Seed size was measured as dry
weight. The seed-weight distribution of each population
was described by its mean, skewness and kurtosis
(Sokal and Rohlf, 1981). The relationship between mean
seed weight at each site and year versus cumulative precipitation
(March to November) or mean monthly temperature
(June to November) was studied using simple
linear regression.
Statistical analysis
The experiment was organized in a completely randomized block design arranged in a 2 x 2 factorial. Treatments included 2 sites and 2 years. Seed weight differences between years and sites were tested using two-way ANOVA and a Fisher's (protected) least significant difference test was utilized for mean separation when F tests indicated that a variable was significant (P<0.05). Data were tested for normality and homoscedasticity of variance following Neter and Wasserman (1974). Monthly precipitation (March to November) and mean monthly temperatures (June to November) were used as independent variables in simple linear regression analysis and mean seed weight was employed as the dependent variable. The relationship between mean seed weight for each site (dependent variable) and seed number per unit seed biomass was also analyzed using regression analysis.
Results and Discussion
Seeds from both locations in 2002 and 2003 showed different seed weight frequency distributions (Fig. 1). The 2002 sample (n=880) from Eden Valley had a mean seed weight of 0.248 ± 0.002 mg seed-1 (mean ± 1 SEM), was significantly leptokurtic with a pronounced peak (kurtosis=1.80 ± 0.1651; P<0.01), and was skewed to the right (skew=0.77 ± 0.0826; P<0.01). A leptokurtic curve has more items near the mean and at the tails, with fewer items in the intermediate regions relative to a normal distribution with the same mean and variance (Sokal and Rohlf, 1981). Positive kurtosis indicates that there were more seeds near the mean than expected for a normal distribution. Skewness to the right indicated that there were more seeds that weighed less than the mean than would be expected for normal distribution. Seeds in the larger sample (n=938) at Eden Valley in 2003 averaged 0.302 ± 0.003 mg seed-1. The frequency distribution was symmetric (-0.1 ± 0.08; P>0.05) and significantly platykurtic (-0.56 ± 0.16; P<0.01). A platykurtic curve has fewer items at the mean and at the tails than the normal curve but has more items in intermediate regions. The 2002 population in Battle Mountain had a mean seed weight of 0.298 ± 0.003 mg seed -1 (n=976), was significantly platykurtic (kurtosis= -0.38 ± 0.1568; P<0.05), and was skewed to the right (skew=0.29 ± 0.0784; P<0.01). Finally, the 2003 sample in Battle Moutain had a mean seed weight of 0.337± 0.003 mg seed-1 (n=912). Its frequency distribution was symmetric (0.06 ± 0.0811; P>0.05) and significantly platykurtic (kurtosis= -0.46 ± 0.1622; P<0.01). The great range of seed weights within each population seed crop can be interpreted as an adaptive characteristic, generating a more homogeneous seed rain than would otherwise be the case with a narrower range of seed weights.
FIGURE 1. Frequency distribution of seed weight of Artemisia tridentata spp. wyomingensis from population samples in (a) Eden Valley, 2002 (n=880), (b) Eden Valley, 2003 (n=938), (c) Battle Mountain, 2002 (n=976) and (d) Battle Mountain, 2003 (n=912) in northern Nevada. Note the change of scale on the Y axis for each of the 4 populations.
The seed weight coefficient of variation for the 4
populations were 26.31% for Eden Valley, 2002; 28.68%
for Eden Valley 2003; 28.52% for Battle Mountain,
2002, and 31.75% for Battle Mountain, 2003. This was
comparable to the average coefficient of variation (28%) documented in a review of data for 39 species (Michaels et al., 1988). Variation in seed size may be the result of
a myriad of factors (Wulff, 1986a). For example, Winn
(1991) suggested that plants may not have the capability
of producing a completely uniform seed weight, simply
as a result of variations in resource availability (i.e.,
soil moisture) during seed development. The range of
size variation among seeds is expected to increase if
individual seeds compete for resources during development
(Rees, 1996). It is very unlikely that a plant, even
if one seed weight was always superior, could produce
exact copies of this particular seed weight. If allocation
of resources to developing seeds proceeds as long as
there are resources to allocate, and the possibility to
adjust the number of developing seed is limited, the result
will be a variation in seed weight. Therefore, the
simple theoretical expectation of a single optimal offspring
size (Smith and Fretwell, 1974) may have to be
replaced with explanations for the maintenance of variation per se. Considerable variation in seed weight has
been reported within shrub populations (Vaughton and
Ramsey, 1998).
Seed weight was greater (P<0.05) in 2003 than in
2002 at both sites (Table 1). It was also greater in Battle
Mountain than in Eden Valley in both years (Table 1).
The greatest percentage of seeds was between >0.20-
0.25 mg seed-1 in Eden Valley in 2002 (33.5%), >0.25-
0.35 mg seed-1 in Eden Valley in 2003 (43.4%), >0.25-
0.35 mg seed-1 in Battle Mountain in 2002 (43.9%), and >0.3—0.4 mg seed-1 in Battle Mountain in 2003
(36.4%). However, there were a greater number of seed
size ranges in Battle Mountain in 2003 than at any other
site in both years (Fig. 1). These findings may be partially
explained because the amount of precipitation
(March-November) was > 23% greater in Battle Mountain
during 2003 than at any other site in 2002 and 2003
(Table 1). Geritz (1995) reported that the range of seed
sizes increases as the total amount of resources available
to plants increases. Other studies of seed size variation
and factors influencing seed size have also reported
results obtained from 2 years and two sites (Wulff,
1986a; Vaughton and Ramsey, 1998).
TABLE 1.
Total precipitation (March-November), mean monthly temperatures (June-November)
and seed weight variation (n=880-976) between years and Artemisia tridentata ssp.
wyomingensis sites. Each value is the mean ± SEM for temperature and seed weight.
Giles (1995) reported that a seed, regardless of its initial size, is capable of regenerating the same mean size. Johannsen's data (1903) also showed that the same variation is regenerated. This suggests that it is not a particular seed size that is inherited but a distribution of sizes, and that the mean alone, is insufficient to describe the seed size of a genotype. Position effects within the inflorescence are, at least in part, agents creating these size distributions and they ensure that seed size variation is produced every generation. This is why the expected reduction in seed size variance is not observed in spite of strong selection on seed size under natural conditions. A common observation is that characteristics related to fitness are positively correlated with seed size, such that larger seeds have the higher fitness (Geritz, 1995). This observations has been used as an assumption in several theoretical models (McGinley et al., 1987) that predict a reduction of seed size variance, due to strong selection towards seeds of a similar and larger size, should be observed. This should occur as frequencies of genotypes producing seeds of favoured sizes increase at the expense of genotypes producing seeds of other sizes, if variation in seed size, and consequently variation in fitness is genetically determined. Unfortunately, these expectations are not borne out; high levels of variation in seed size are continuosly produced in natural populations. That is why one of the central questions in seed size evolution studies is despite the striking differences in fitnesses of plants growing from seeds of different sizes, why the predicted reduction in seed size variance is not observed. One explanation is that the variation in the seed size produced by a plant genotype may be highly environmental. For example, we found that monthly precipitation (March-November) explained 85% of the total variation in mean seed weight (Fig. 2). However, the relationship between mean monthly temperature (June-November) and mean seed weight was not significant (r2=0.00, P=0.431), since mean monthly temperature during that period was similar (P>0.05) in both sites and years. Wulff (1986a) reported that exposure of Desmodium paniculatum L. parent plants to higher temperatures during growth and seed development significantly reduced the mean seed weights. Our results emphasize the importance of amount and periodicity of precipitation as a major determinant of seed size. Wulff (1986a) also found that a reduced water supply significantly reduced seed weight in Desmodium paniculatum L. with respect to the controls. Assuming that seed size is limited either directly or indirectly by the availability of resources or current photosynthesis, it is not surprising that seed size should be reduced in conditions of reduced water availability, since it affects photosynthetic rates (Boyer, 1976). Infrequent patterns of sagebrush seedling establishment have been attributed, at least in part, to periods of unfavourable weather (Lommasson, 1949), although Maier et al. (2001) reported that recruitment is different from germination. There are models that predict variance in seed size should decrease in natural populations due to strong selection towards seeds of a similar and larger size. However, the fact that seeds of different sizes germinate, grow and reproduce at different rates in the same environment (Stanton, 1984; Wulff, 1986 b,c; Andersson, 1996) suggests that seed size variation could be advantageous in varying environments.
FIGURE 2. Relationship between precipitation and seed weight in Artemisia tridentata spp. wyomingensis in northern Nevada. Each symbol is the mean of n=880 [Eden Valley (EV) 2002], n=938 (EV 2003), n=976 [Battle Mountain (BM) 2002] and n=912 (BM 2003).
Mean seed weight was correlated to seed number per unit biomass. The greater the mean seed weight (MSW) on each site, the lower the seed number per unit seed biomass (SN/UB) (MSW=0.575 - 0.0816 SN/UB; r2=0.99; P=0.004). This result was similar to that reported by Henery and Westoby (2001) on various shrub species in Australia.
Conclusions
Our results suggest that the precipitation regime to which the mother plant is exposed can have a significant effect on the sizes of seeds produced.
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