Flowering Phenology and Diversity of Dicots in Desert-Shrub
Grassland,
© 2004 R.M. Chew
Abstract.
_____ The timing and magnitude of flowering
of a suite of 32 dicot annuals and perennials in a degraded grassland invaded
by desert shrubs was recorded over 13 years (1987-1999). Flowering was related to weekly rainfall and
sum of degree days in six phenological seasons: winter (germination of annuals,
dormancy of perennials), early spring (vegetative growth and limited
flowering), late spring (major spring flowering),
early summer (no, or limited flowering), late summer (major summer flowering),
fall (little or no flowering, senescence and dormancy). Each season varied relative to itself through
the years from extremely wet to extreme drought and extremely cold to extremely
warm. Each year was unique in its
pattern of six seasons. Most minimum and maximum values occurred 1994-1999.
Fourteen
species flowered only in spring, 4 only in summer, 13 spring and summer, and 1
in fall. Flowering periods overlapped, but the times of maximum bloom were
often significantly separated. The duration of a species’ flowering was a
function of the time of its first bloom.
Durations peaked in late spring and then declined; durations
progressively declined in summer.
Regression
models were constructed for each species total flowering (Nt) in relation to the independent
variables of each seasonal rainfall and temperature sum, in the current year
and previous year. Total flowerings of
18 of the 32 species were significantly predictable from rainfall and
temperature, 6 for both their spring and summer flowerings. The number of significant
seasonal variables in a predictive regression ranged from 1 to 5 with a median
of 3. The first two variables to enter a model accounted for an average of 88%
of the variability of Nt
(range 56-100%).The whole models had an average adjusted R2 of 0.93. No two species
had the same first two predictive variables. For the two predominant predictive
variables, 24 of 45 are for the current year and 21/45 for the previous year;
Precipitation is a dominant variable in 31/45 and temperature sum 14/45.
At
least 15 different phenological patterns of flowering can be proposed for the
32 plant species, based on responses such as specific time of flowering,
dependence on rain in a particular season, in the present or previous year,
biseasonal flowering, seasonal flexibility, and the nature of the species:
annual, type of perennial, evergreen, deciduous succulent, and time span
between vegetative growth and flowering. In years when there was prolonged low
moisture index, based on low precipitation and / or high temperature sum, there
was not only failure of flowering, but senescence and even death of large
proportions of some species populations. There were some hierarchies of
recovery of species.
Considering
what is now known about the genetics of flowering in Arabidopsis, it is
reasonable to speculate that the biodiversity of the dicots in this semiarid
community is a result of the interaction of the great variety of rainfall and
temperature conditions, season to season and year to year, with the many
phenotypes of the available plants, as they have assembled into the community
in the short term and further adapted in the long term.
INTRODUCTION
The
annual sequence of plant phases from germination through vegetative growth,
flowering, dispersal of seeds and senescence is one of the most striking
aspects of nature, and it entices one into the observation of nature. The utility of phenological research has
expanded until it is essential for understanding the functioning of ecosystems
(
Temperature,
moisture and photoperiod are major clues determining blooming, but there is
little documentation for individual species.
Much effort has gone into trying to relate adaptation of flowering times
to different climatic patterns (Fox, 1989), and to pollinators, predators,
pathogens, competitors and nutrients (Rathcke and Lacey, 1985). As the
latter authors state (p. 191), “In general there are many more hypotheses
about ultimate factors that may mold flowering times than there are thorough
studies that permit testing them”.
The detailed studies of single species by Fox (1989) and LeBuhn (1998) illustrate the difficulties of determining
even the proximate factors.
The
study of perennials and annuals requires different perspectives. Perennials
have a flexibility of development due to stored resources in persisting plant
parts and can remain vegetative or flower.
Each year annuals have the complexities of germination, survival of
seedlings, vegetative growth, flowering, setting seeds, and dispersal of seeds
to seed banks in the soil. Whereas
annuals in semiarid sites usually germinate after light but extended rains,
which occur in most years, perennial shrubs may germinate only after short but
heavy summer rains, followed by sufficient subsequent rain, a pattern that
occurs less frequently (Went, 1949). There are a number of studies of flowering
of annuals: in the
Long-term
data sets have led to some general conclusions: (1) flowering can be predicted
from data on rainfall and air temperature, (2) often rainfall and temperature
have opposite effects, (3) the most important events occur 1-4 mo or more before
blooming, and (4) sometimes predictive formulae cannot explain failures of
flowering due to isolated extreme conditions, e.g. droughts and
freezes, which can affect blooming for years afterwards (Turner and Randall,
1987; Fitter et al, 1995; Sparks and Carey, 1995). I will use a 13 yr data set
to test these general conclusions. Here I document the flowering times and
magnitude of blooming of annual and perennial dicots of a semiarid community
with the objectives of: (1) defining the seasonal patterns of blooming for the
species, (2) analyzing the patterns of flowering magnitude in relation to
annual variation of rainfall and air temperature, and (3) assessing the
differences of species’ phenologies as the basis for plant diversity.
METHODS
SITE____ The study site is a 9.3 ha cattle exclosure
that was established July1958 in the San Simon Valley, 8 km north of Portal,
Cochise County, Arizona. The site is 1.5
km east of the foothills of the
WEATHER____ Air temperature, 5 cm
above ground, was recorded continuously, 1980-1999, from a thermal element
inside a 76 cm long x 48 cm wide x 71 cm high shelter with shade screen sides,
with double roofs 8 cm apart. Mean daily air temperatures were calculated from
field records [(max + min) / 2] and summed over weekly periods asdegree-days
above 0o C.
I
used 0o C as the threshold for biological activity
of all plant species, although there is almost no information on thresholds for
the species of the site. The threshold for flowering may
be10o for Larreaand
some other shrubs in the
Daily
rainfall, 1980-1999, was measured in a rain gauge with an internal cylinder
graduated in 0.01 inch increments to hold 1 inch total as delivered from a 10.5
cm funnel . Overflow from the graduated cylinder went into a surrounding 10.5
cm cylinder with a capacity of 28 cm of rainfall. In 1980 and 1984-1987 rainfall was also
recorded from a tipping-bucket rain gauge.
PHENOLOGICAL SEASONS____ For analysis of
plant and weather data I divided the year into six phenological seasons. These were based retrospectively on
generalities of the data for plant growth and flowering over 13 years:
(1) winter, weeks
45-4 (calendar days 309-28), ca.
November-January, a period of dormancy of perennials and germination of spring
annuals;
(2) early spring,
weeks 5-16 (days 29-112), ca. February-mid April, a period of vegetative
growth, but before the start of blooming of most species;
(3) late spring,
weeks 17-26 (days 113-182), ca. late April-June, the period of the major spring
flowering;
(4) early summer,
weeks 27-30 (days 183-210), ca. July, generally before the start of summer
flowering and germination of summer annuals;
(5) late summer,
weeks 31-39 (days 211-273), ca. August-September, the time of major summer
flowering;
(6) fall, weeks
40-44 (days 274-308), ca. October, little or no flowering, senescence or entry
into dormancy.
TRANSECT COUNTS____ I walked a
standard rectangular path (121.8 m x 152.4 m) and counted the flowering
individuals within 2 m of the center of the path ____ an area of 0.216 ha. The number of transect counts varied from 14
a year to 22 a year, depending on the time of
first and last blooming of any species.
Counts were made every 7 to 14 days. I counted a plant as blooming
regardless of its number of flowers, which reduces the information that would
be obtained if the magnitude of blooming of individual plants were noted. To do the latter would have limited the size
of transect that could have been used and the time-span of the study.
I
originally planned to limit observations to 7 yr (1987-1993), but because of
the occurrence of unusual weather conditions, I added censuses in summer 1994,
spring 1995 and summer 1996. During continuing unusual years of 1997-1999 full,
consistent counts could not be made to establish total counts (Nt) for phenological
seasons, but there were enough counts to establish numbers for peak weeks (Np).
Counts
were compiled by weeks from wk 1 (Jan 1-7) to wk 52 (Dec 25-31). Numbers were
interpolated for weeks when no count was made. The first day of blooming was
assumed to be the first day of the week in which flowers were first observed,
and the last day of blooming as the last day of the week when flowers were last
observed. The total number (Nt) for a phenological
season involves counting some individuals more than once as flowers persist
from week to week and as new flowers are produced, but the count is still a
measure of the magnitude of flowering of a species. Usually there was one week when the number of
individuals flowering was considerably in excess of adjacent weeks (peak week, Np).
GERMINATION QUADRATS____In winter 1997 I
established eight circular 1 m2 quadrats, two randomly
positioned along each side of the rectangular walking transect. These were used to follow the number of
germinating plants, and their progression to fruiting. Each quadrat
was divided into quarters. In two randomly chosen quarters germinating
individuals were removed as counted; in the other quarters they were marked
with toothpicks and left in place for further development.
ANALYSIS OF COUNTS____ I analyzed the
data for total seasonal counts of flowering individuals of a species (Nt) for their relationship to the independent
variables of rainfall and air temperature sum of appropriate phenological
seasons by forward multiple stepwise regression using the JMP Program, Version
3.1 (SAS Institute 1995). The variables
chosen by the stepwise procedure were made into a model by the least squares
program associated with the stepwise regression. Information from the
model-constructing program provided correlation values (R2) forNtwith each variable entered, and an adjusted correlation (AR2) for the whole model of n variables.
A model was rejected if it did not have an acceptable normality of
residuals, a constant variance of residuals, and acceptably low multiple collinearity, as indicated by the program. A model was also rejected if there was so
little variation among the Ntvalues of some years that they functioned as a “single” point
in determining the regression plot, or if there were years that were so
exceptionally high that they biased the plot.
Models were constructed for the Nt
values versus rainfall and temperature of the current year, and for the current
year plus the previous year. Models were
constructed for the years 1987-1993, and for these 7 yr plus data for spring
1995, or plus summers 1994 and 1996, depending on when a species flowered.
The
multiple stepwise regression procedure has obvious defects: (1) It can be confounded by correlations among independent
variables. (2) Because of the number of variables allowed into the selection
process when Ntis regressed
against the cur-rent plus previous year, there is the possibility, but not
necessity, of spurious correlations.
However, the procedure has the advantage that its predictions are
“transparent” suggestions of the predictability of Nt in terms of rainfall
and temperature, rather than the “less transparent” information
from procedures such as principal components analysis and lagged correspondence
analysis. The multiple stepwise procedure is retained here for its heuristic value in
suggesting hypotheses to be tested by experimentation.
Stepwise
multiple regression has been used successfully in the analysis of other
long-term data sets: (1) for shrubs in the Mojave Desert (Turner and Randall,
1987); (2) by Fitter et al. (1995), for data taken over 36 yr in one location
in England, who were able to fit regressions of first flowering date to
temperature for 219 of 243 species; (3) by Sparks and Carey (1995), who found
significant relationships with mean annual temperature and annual rainfall for
13 plant species in a data set extending over two centuries; (4) by Epstein et
al. (1997) who found relationships
explaining 67-81% of the variation in production of grasses of the US Great
Plains on the basis of mean annual temperature and rainfall; (5) by French and
Sauer (1974) in a study of the phenophases of three species of grasses.
RESULTS
RAINFALL____ Rainfall was biannual (Table 1 ). Winter and
early spring rains were gentle and widespread over a broad area and provided 35.8% of
the average annual total. Late spring
rains provided only 7.6%; early and late summer rains, predominantly
thundershowers, provided 50.8% of the total, and fall (October) was a hiatus of
lower rainfall, 5.8%. Variation in
regional and global weather patterns resulted in exceptionally wet and dry
phenological seasons in some years. The
interannual coefficient of variation ranged from 0.53 for early summer to 0.91
for late spring (Table 1). Variability resides in the
shorter time periods of the phenological seasons. Over broader time periods there is less
interannual variability, to the point where annual rainfall has a coefficient
of only 0.30. Winter-spring rainfall is
significantly greater in
Although
four of the five years of records from a tipping bucket rain gauge were before
the present study began (Table 2), they are assumed to be representative of the
pattern for the site; 66.5 % of the rain
events were less than 5 mm, but provided
21.9% of the average annual rainfall. Only
33 rains were > 20 mm, and those in July-September provided 31.4% of the
annual rainfall, versus 21.5 % by such events in all other months. The extremes
of the distribution are of special interest.
Although rains < 5 mm may not directly affect plant growth, Sala and Lauenroth (1982)
concluded they are important because they affect decomposition and nutrient
processing, which occur principally near the soil surface. They found that rains of 5 mm did directly
affect the physiology of Boutelouagracilis in
semiarid grassland for at least 2 days.
Summer storms > 22 mm can be sufficiently intense (0.25-1.32 mm / min) to cause runoff (Hawkinson,
1968). Fourteen storms of this
intensity were recorded by the tipping bucket rain gauge in five yr. Winter rains of even 70 mm were of too great
a duration to cause runoff. The light
rains of winter are made more effective for plants by the lower evaporation
then; the heavier rains of summer are made less effective by runoff.
TEMPERATURE SUMS____ Degree day summations
for phenological seasons (Table 3) are inherently less
variable than rainfall, with coefficients of variation ranging from only 0.03
in early summer to 0.15 in winter. Most
of the variability was in the fall through early spring. Although temperature sum is less variable
than rainfall, a small change of temperature sum may be as biologically
important as a large change in rainfall (e.g.
Scifres and Brock, 1969).
CATEGORIZATION OF SEASONS_____ To ease conceptualization,
I categorized seasons with respect to rainfall as very wet (W*), wet (W), moist
(m), normal (N), dry (d), drought (D)
and extreme drought (D*), and, with respect to temperature sum, as very hot
(H*), hot (H) , warm (wm), normal (No), cool (c), cold (C), very
cold (C*) (Table 4). The categorization was based on the
percentile distributions of values for each season across the 13 years in
Tables 1 and 3: W* and H* are values >90% quartile; W and H = 75-90%; m and
wm = 62.5-75%, N and No = 62.5-37.5 %; d and c
=25-37.5%; D* and C* <10% quartile. The categorization within a season is
relative only to itself. For example:
extreme wet (W*) is 147-154 mm rain for the winter season, but 262-297 mm for
late summer. The biological effect of
extreme drought and extreme wet will depend upon the season of its
occurrence. The categorizations of Table 4 make clear the season-to-season variation within
years and the interannual variation within a season. No combination is repeated in the 13 yr
tabulated.
THE PLANT COMMUNITY____
The 32 species
that were censused (Table 5) are listed according to
three categories of maximum densities of flowering individuals. A few species that did not bloom in at least
4 yr in the period 1987-1993 are omitted. Except for Astragalus spp. and Lepidium lasiocarpum the
omitted species are annuals that were present erratically or in very small
numbers, although some of these were exceptionally abundant in 1995 (see
later). The community is predominantly Compositae (12 of the 24 species with
densities >400 stems / ha) and perennials (21 of the 32 species).
The
censused dicots are predominantly perennials: 2 shrubs (Sh,
Table 5), which were up to1.5 m high; 2 subshrubs (SSh) of < 0.5 m height; 4 suffrutescents
(SP), still smaller and only slightly woody; and 11 herbaceous perennials (HP).
Ten censused species were annuals (A).
The
times of blooming of species (Table 5) as established by
censuses are: spring only (Sp), spring and summer (Sp/Su), and summer only
(Su), with some minor cases (Sp* and Su*) when less than 5% of blooming
individuals were counted in the other season. The dominance of spring flowering
by annuals (Table 6) is almost significantly different
from random (X2 = 5.33, 0.10> P >
0.05, df = 2). There was no
difference for perennials. All the annuals listed in Table 5 germinate in
winter, and then bloom in the spring, except Eriogonum Abertianum,
which does not bloom until summer. There are few summer-germinating annuals on
the site, none of which was abundant enough to be listed in Table
5.
SPECIES BLOOMING PERIODS ____ Spring flowering begins with an herbaceous perennial with a long tap root,
Cymopterus
multinervatus, and an annual, Draba cuneifolia (Table 7).
Thirteen other spring-only species (one Sp*) are scattered throughout the
spring period, among 13 species that bloom both spring and summer. The year ends with 3 perennials (one Su*) and
one annual that bloom only in late summer and 1 shrub that blooms only in fall.
The
average beginnings of spring blooming progress from day 61 to 147. The average
duration of blooming of species in spring (Fig. 1a)
increases from day 60 to day105 and then declines to day 150. The second degree
polynomial regression for this relationship is:
Y (days duration) = -92.934 + (2.72219 x ave 1st day) - (0.01348 x ave 1st
day2), which has an F value with probability of
0.072.
The average duration of summer flowering
progresses from day 196 to day 254 (Fig. 2a) with a
significant decline from beginning to end. The 2nd degree polynomial regression
is:
Y =
1592.06 - (12.9558 x ave 1st day) + (0.02703 x ave 1st day2). P > F =
0-.046.
The mean duration of blooming was not
significantly different for annuals and perennials, but was significantly less
for cacti, which have only a few flowers per plant and flowers that persist only one or a few days.
COMMUNITY PATTERNS OF BLOOMING____ The rainfall
and temperature sum categorizations of Table 4 were used
to generalize soil moisture indices (MI) for spring and summer of each year (Table 8). Rainfall categories, as they related to the input
of water to the soil, were assigned arbitrarily values of: W* = 3, W = 2, m = 1.
N = 0, d = -1, D = -2, D* = -3 Temperature sum categories, as they related
to evaporation of soil moisture, were given half the weight of the rainfall categories:
C* = 1.5, C = 1, c = 0.5, No = 0, wm = -0.5, H = -1,
H* = -1.5. The earliest blooming of plant species in spring was compared to
moisture indices summed for winter and early spring; earliest summer blooming
was compared to MI values summed for late spring and early summer.
The
eight spring annuals bloomed earliest in years with soil moisture indices in
the middle range of values (2.5 to -1.5) (Table 8). Earliest bloomings did not occur in years
with high MI (5.0 to 3.0), nor lowest MI (-5.5). The distribution of species bloomings
was highly significantly different from random (X2 = 30, df = 7, P <
0.005). In two years with earliest
bloomings (1995, 1989) the contribution of winter to the summed MI was positive
(1.5-2.0 respectively) but early spring was negative (-1.0, -3.0). In 1988 both winter and early spring
were positive MI (0.5 and 2.0 respectively).
The earliest bloomings of 17 perennials were spread over the range of MI
values (except the lowest, -5.5) with a tendency towards medium to low values
(2.5 to -1.5), which was marginally significant (X2 = 12.9, df 7, 0.10> P < 0.05). In spring no annuals bloomed in 1990 when MI
was -5.5; 71% of perennials also failed to bloom that year.
In
summer, with data for only three species of annuals, there was no significant
difference of distribution of earliest blooming from random. Likewise for 16 perennials (in both cases X2 0.50 > P > 0.25).
When
the magnitude of flowering (Nt) of species
is compared to the moisture
This
attempt to find community patterns in flowerings is, of course, confounded by
the adaptations of the phenotypes of individual species, which are dealt with
next.
FLOWERING
CHARACTERISTICS OF INDIVIDUAL SPECIES
WEEK OF FIRST BLOOM____ The week of first bloom each year was
regressed against rainfall and temperature sum of appropriate phenological
seasons for the 14 species that had a range of variation of first flowering of
at least 5 weeks during the years of observation (Table 10). Variables were significantly predictive of
first week of spring blooming for two of three annuals; blooming was advanced
for Baileyamultiradiata by an increase in
winter precipitation, and advanced for Gilia longifora by
increase in temperature sum in early spring. Only one of nine spring-flowering
perennials,
First
summer flowering was significantly predictive for one of three summer annuals; Baileya;flowering was advanced by increase in early
summer precipitation. Five of eight perennials were significantly predictive by
summer rainfall or temperature sum (Table 10). Gutierrezia, which does most of its vegetative
growth in winter and does not bloom until early or late summer, showed
complicated predictive relation- ships; first bloom was delayed by increased
late spring rainfall and advanced by higher late spring temperature sum, but
was advanced by increased early summer rainfall and retarded by higher early
summer temperature sum.
MAGNITUDE OF TOTAL BLOOM (Nt)____ For almost all speciesthere
was considerable variation in the number of flowering individuals censused from
year to year (Tables 11a and 11b).
These detailed data are provided for the use of anyone wishing to do a
different analysis than provided herein.
For 18 species (Table 11a) the data for
1987-1994 provided significant whole models for the regression of Nt based on rainfall
and temperature sum. For nine species (Table 11b) there
was no significant relation-ship, but the data for five species show remarkable
low and high values of Nt
in the “exceptional years” 1994-1996.
For
the 18 species of Table 11a the models of Nt are highly
significant with AR2 > 0.86 in all but one
case. Models have a median of three independent variables (range 1-5). For spring bloomings (Table
12), Nt is
predicted by a mixture of variables of the current year (10 of 24) and previous
year (14/24); the latter variables range from the previous fall through the
previous early spring. Only one annual and three perennials are principally
predicted only by current year variables. Five perennials are predicted
principally by previous year variables. Precipitation is a dominant variable in
17 of 24 cases, whereas temperature sum is so in 7 of 24.
For
summer bloomings (Table 13) variables of the current
year are more often predominantly predictive (14/21) than those of the previous
year (7/21), as compared with spring data.
Precipitation is predictive in 14 of 21 cases (7+, 7-) and temperature
sum 7/21 (2+, 5-). In one case, the number of Gilia
flowering in spring is the second most predictive variable of Gilia summer Nt,
the only species for which this is true.
Spring Nt was made an independent
variable only for models of summer
flowering.
There
is no case in which two species have the same predictive relationship for the
two most significant variables. Aster hirtifolius
and Dyssodia acerosa do
share the same two variables (Table 12) but for one of
them (Pfall*) the relationship is different.
“EXCEPTIONAL” YEARS”_____ In early
1994 it was sensed that the year was unusually dry__flowering
by spring species was zero or nearly so (Table 11a, b). Censusing of Nt was then extended to summer 1994, spring 1995
and summer 1996. For spring 1994 and 1996 no censuses were necessary, except
for a few species, since there was no or very little flowering; The symbol (*)
represents a “census” of zero in these cases Limited observations of phenology continued
through 1999. In comparison to
1987-1993, 1994-1999 were exceptional in one way or another. Five of the six
minimum values of rainfall for the six phenological seasons occurred in
1994-1999 (Table 1). The lowest total annual rainfall
occurred in 1994. Every seasonal maximum for temperature sum occurred
1994-1999, with the highest annual total being in 1999 (Table
3). Minimum rainfalls together with
maximum temperature sums suggest low soil moisture 1994-1999 except as
ameliorated by the second highest late summer rainfall in 1995. The coincidence
of certain plant phenologies with the different precipitation and temperature
sum patterns of 1994-1999 are very suggestive of cause and effect.
Year
1994 was distinctive in having warm to very hot
weather (wm, H, H*, Table 4) from winter through fall.
Annual rainfall was a minimum in 1994; only early spring and late summer were
normal rainfall (N) while other seasons were dry (d or D). There were several negative consequences for
flowering: (1) There was a failure of spring flowering
more complete than after the 1990 spring drought (62 mm total for winter
through late spring for 1990, Table 1, compared to 101 mm
for 1994. Larrea tridentata was
the only species that bloomed sufficiently to be censused, and unexpectedly had
its maximum spring Nt in1994 (Table 11a). (2) Progressive leaf stress and senescence and
some mortality of subshrubs was observed May through July. (3) Although rains
began July 7, recovery of shrubs delayed their blooming by an average of 29
days (range 10-50 d) beyond their average beginning times. A first summer census was not needed until
August 24. (4) Success of summer
flowering was varied (Tables 11a, 11b). Only a few seedlings of the biseasonal
annuals, Baileya and Gilia longiflora survived from winter to bloom. Conversely, five biseasonal perennials had an
average or above average summer Nt so that
the community aspect was dominated by the flowers of Zinnia, Parthenium
and Menodora. Summer-only
perennials varied: two bloomed near average; GutierreziaNtwas only 4% of its summer
maxi-mum (to be expected because of its winter-spring vegetative growth),
whereas fall-blooming Flourensia had its
maximum bloom. (5) Although Gutierrezia appeared to have greened-up normally through
early spring, by Nov. 425 of 472 individualswere
dead. Although even moderate mortality
of stems had not been observed previously for subshrubs, by Nov. 15.6% of Zinnia appeared dead; 25.5% of Dalea appeared
completely dead and 50% had some dead stems.
In
1995 weather was
unusual in the way in which seasonal temperature sums enhanced or counteracted
seasonal rainfalls, as they could affect soil moisture from winter through
fall: (Table 4): WNo, NH, D*C, NC, WH, DH*. Annuals
and most perennials responded in opposite ways. Winter rainfall was the second
highest value (136 mm) and was equitably distributed over 13 of 14 weeks. Species that were keyed to winter rainfall
were very successful: (1) Seven annuals had spring flowerings that ranked first
for all years. (2) Four annuals were present that had not been censused before,
two of which had not been recorded for the site (Table 14).
(3) Eleven annuals bloomed 2.2 wk earlier than on average (range 1-4 wk). (4)
Two early flowering species, the geophytes Cymopterus
and Dichelostema had their maximum spring Nt along with Dyssodia acerosa, which showed an ability to respond to
rainfall regard-less of season. Spring/summer perennials bloomed very poorly,
with five species failing to bloom, or almost so (Tables
11a, 11b). Consequently no census was made in
summer.
In
1996: The drought, very warm (D,H*) of fall 1995 continued as a stress into
the (D,H) of winter 1996, and dry, warm (d,wm) of
early spring, even more severe than 1994. The above average rainfall (W) of
late spring was partly offset by the maximum temperature sum (W,H*), which gave
way to a normal early summer. Shrubs (Larrea, Flourensia)
and subshrubs (Dalea, Parthenium, Zinnia) showed leaf stress until they
began to green-up at the end of early spring. Almost all species had negligible
spring blooms in 1996, as in 1994. The
years differed in the varied responses of summer flowerings (Table
11a). Dyssodia pentachaeta bloomed in record numbers in 1996, but
failed to bloom in 1994.
In
1997 only spot censuses were made.
In 1997 every seasonal combination of
Observation
of the number and development of seedlings in 17 1-m2 quadrats was begun Jan 1997. Seedling numbers were exceptionally high in
relation to 1998-1999. In 10 quadrats in which
seedlings were removed as they appeared, there was an average of 193 + 41 (SD)
seedlings produced / m2 (range 32-487) which
were of 13 + 5 species (5-21). In seven quadrats in which seedlings were allowed to remain and
develop, there was a mean maximum number of 151 + 77 seedlings / m2 (85-305), of 16 + 3 species (12-20). Most of the seedlings belonged to
six annuals: Baileya multiradiata, Draba cuneifolia, Gilia longiflora, G. sinuata, Eriastrum diffusum, and Eriogonum Abertianum,
and one herbaceous perennial, Bahia absinthifolia. After they had bloomed and set seeds,
some Baileya persisted as rosettes into the next year, the only instance of its
biannual potential. There was no
germination of summer annuals.
Year
1998 had strong contrasts. Early spring was extremely wet and cold, and
then late summer had the maximum drought and maximum temperature sum
recorded. Flourensia cernua and all subshrubs except Dalea retained
green leaves through a normal winter and began new growth in early spring.
Blooming was censused only at the start of late spring, W 17 and 18. Dalea then
had exceptional Nt and the overwintering
rosettes of Baileya produced a record
bloom. Other species were
unexceptional. However, seedling
production was greatly reduced below 1997.The seven species that averaged 151
seedlings / m2 in 1997 produced only 6.7
/ m2 in 1998.
Ten other species together produced 1.0 seedling / m2 , but these did not survive more than 2 wk.
Year
1999.A deficit of rainfall and above
normal temperature sum persisted from late summer 1998 through late spring 1999
(Table 4). Rainfall was a minimum in early spring and
nearly so in late spring (Table 1) and temperature sum
was a maxi-mum in winter and early spring (Table 3).
Although shrubs and subshrubs retained green leaves through the warm winter to
wk 2, there was then progressive senescence and failure of new growth. Dalea had lost all its leaves by Dec. and by June
appeared to be dead. Gutierrezia had 50% of
plants with brown leaves by early Jan. and by June all individuals appeared
dead. The evergreen Larrea began to turn yellow in Feb.- Mar. and its
paired leaflets folded together and were covered by excessive resin. Parthenium, Zinnia and Flourensia were almost leafless by June. With the first substantial rains in early
July there was a hierarchy of recovery from drought. Larrea immediately became bright
green, leaflets unfolded and enlarged and flower buds appeared. week 28. Parthenium began
to expand its few surviving leaves wk 27, new leaves appeared directly from old
stems wk 28 and were near full size wk 29 , and growth of new stems began wk
30. Zinnia did
not show greening of its grey leaves until wk 29 and had new stem growth wk
30. By wk 32 Parthenium, Zinnia and
Flourensia had “robust” stem
growth that seemed greater than previously judged. In contrast Dalea had
developed only a few leaves by wk 31 and only slowly leafed out to a usual
extent. Most Gutierrezia
died; only 4.4% of individuals had sparse leaf regrowth.
Only
two seedlings of spring annuals germinated in winter 1999 in all quadrats. However, there was germination and survival to
blooming and fruiting of summer annuals, an average of 16.5 plants / m2 of 30 different species. Most of these (59%) were of three species: Euphorbia capitella (35%), E. revoluta (10%) and Baileya
(14%). Fifteen of the 30 species were
found in only one of 17 quadrats, as one or two
seedlings; three bloomed that had not been recorded for the site. Twenty
species did not develop to the point where they could be identified.
DISCUSSION
Variations of
rainfall and temperature are generally considered to be the most important
variables affecting flowering of plants in a semiarid environment. Some authors
consider nitrogen and precipitation to be the two major determinants of the
diversity and abundance of desert annuals (e.g. Fox,1989; Guo
and Brown, 1996). Net primary production and net N mineralization both increase
with mean annual precipitation in the Central Grassland region of the
However,
determination of flowering is a complicated subject for analysis, since
“The opening of the flower is an observed endpoint preceded by a complex
of chemical and growth processes which are little understood” (Lindsey
and Newman, 1956:813). The switch of meristem from vegetative to reproductive growth is
under control of genes that are just beginning to be identified.
The
genome of Arabidopsis has greatly advanced the understanding of the
control of flowering (see review by Simpson and Dean, 2002: “Arabidopsis,
the Rosetta Stone of flowering time”).
Much experimental work has shown that in Arabidopsis there are
multiple gene pathways that control flowering time. These can be influenced by extrinsic factors
such as winter temperature, ambient temperature during growth, photoperiod,
light quality and intensity, as well as endogenous autonomic pathways
associated with aging. The multiple
pathways can be integrated in different ways, changing the predominance of one
pathway or another. Mutations occur at
many points with an effect on timing of flowering and other phenophases of
plant development. This provides
considerable plasticity and diversity to flowering control. Broadly applied
within a community of plant species with similar genetic plasticity and
diversity, this could be the basis for adaptation of different species to
various aspects of the environmental spectrum and possibly an important
determinant of community species diversity.
WHAT IS
THE CIRCUMSTANTIAL EVIDENCE FOR THE PRESENT FLORAL DIVERSITY BEING DUE TO
ENVIRONMENTALLY DRIVEN ADAPTATION?
(1) The life forms of the
plants display a considerable diversity that is more finely drawn than the
gross categories of Table 5, i.e.
“shrubs” (large size to 1.5 m height), subshrubs (smaller than
“shrubs”), “suffrutescents”
(still smaller, and with minimal woodiness of stems) and “herbaceous
perennials”. The last undoubtedly have many subtle phenotypic
variations. This spectrum of forms can
well be the result of long-term adaptations of previous phenotypes.
(2)
The present site provides a great variety of precipitation and
temperature sum combinations within six basic phenological seasons (Tables 1,3,4), which are based on the general patterns of germination,
growth, flowering and senescence of species of the plant community. These
combinations can well be selective forces on adaptation of life form and
physiology of the species of plants.
(3) Although there is much overlap of the
flowering periods of species, there is a definite temporal progression of the
peak flowerings of species, with some distinction of spring-flowering species
based on winter-early spring rains, and summer-flowering based on the summer
rains (Table 7, Figs 1a, 1b,
1c and ,2a, 2b, 2c).For six cases, pairs of species that were next to each
other in their times of maximum Nt were
compared by the simple method suggested by Estabrook
et al. (1982) for testing the statistical difference between phenologies. In all cases the species’ phenologies
were significantly different at P < 0.01, because of differences in the
shape of their phenological curves and differences in timing. These comparisons were for Cymopterus vs. Dichelostema spring
1995; Draba vs. Giliasinuata spring
1992; Aster vs. Dyssodia acerosa spring 1992; Gilia longiflora vs. Baileya
summer 1991; G. longiflora vs. Bahia summer
1988; G.longiflora vs. Eriogonum summer
1991.
(4)
The duration of flowering of a species (Figs 1, 2) has some dependence on when it begins to flower. The patterns for spring and summer suggest
they are due to the interaction of rainfall and temperature sum patterns. In spring the successive duration of
flowering increase from the middle of early spring (d 60) to the end of early
spring (d 113) and then decline through late spring. Increasing duration might be based on the
benefits of linearly increasing temperature sum (Fig. 1c)
and an adequate soil moisture due to accumulated
rainfalls of winter and early spring.
Declining rainfall through early spring (Fig. 1b) and
depletion of soil moisture by transpiration and evaporation, accelerated by
increasing temperature sums may then constrain the length of flowering. In summer the progressive decline of duration
of flowering follows the linear decline of temperature sum (Fig,
2c), in spite of the peaking of rainfall in late summer (Fig.
2b). Each plant species is brought into the spring and summer sequence
according to what triggers its first flowering for which there are both
rainfall and temperature predictors (Table 10).
(5) The timing and magnitude of flowering
can in many cases be predicted by rainfall and/or temperature sum conditions of
prior and current phenotypic seasons.
(a) Of the 9 annual species that bloom in
spring, the Nt of only 4 are significantly
predictive; all 3 annuals that bloom in summer are significantly predictive.
(b) Of the 7 perennials blooming in spring,
only 2 were predictive; of 11 species flowering both spring and summer 8 were
predictive; of 4 species flowering summer and Fall, 3 were predictive.
(6) The distribution of predictive variables
for the plant community as a whole (Tables 12. 13) suggest several relationships on a community-wide basis:
(a) Predictive variables occur equally in
the previous year and current year: 42% and 47% respectively for annuals and
52% and 48% for perennials. The previous
year variables for annuals must act on seed banks, as is possible in a variety
of ways (e.g. Harper 1977: 61-110).
The high importance of variables of the previous year is surprising. However, Dunnett et
al. (1998), in a 38-year study of vegetation dynamics in relation to weather,
found correlations of first day of flowering “generally evenly
distributed” over lag periods of 0, 1 and 2 yr.
(b) In two cases an annual, Gilia longiflora, is significantly affected by a current
variable other than rainfall or temperature;
spring flowering is inversely related to the simultaneous flowering of
the perennial Bahia, and summer Nt of G.
longiflora is positively related to the magnitude of its spring
flowering. LeBuhn
(1998) has shown that there are three flowering phenotypes in G. longiflora: individuals that flower only in spring,
individuals that flower both spring and summer, and those that flower only in
summer. The ratio of these phenotypes in
the field varied from year to year.
(c) Annuals are equally affected by
variations in rainfall and temperature sum: 52% and 47% respectively. For perennials it is 64% and 36% respectively.
(d) The sum of positive relationships with
precipitation (+P) and inverse relationships with temperature sum (-T) is 13
cases out of 17 for annuals, and 32 of 50 for perennials. Of course, increased rainfall and decreased
temperature sum combine to increase soil moisture, whereas the combination of
-P and +T interact to reduce soil moisture.
(7) Examination of the seasonal distribution
of the two most predictive variables for individual species shows that:
(a) Although annuals germinate in winter, none
showed a significant relationship to current winter rain or temperature.
Apparently, below a certain threshold of winter rain there will be little or no
germination and flowering, above that threshold there is no relationship of
amount of winter rain to flowering Nt. Three perennials had a
relationship to winter rain: Houstonia and Dyssodia acerosa a
positive relationship and Larrea a negative relationship.
Rainfall is inversely related to Nt ,
in 8 cases as one of the two most predictive variables (Tables
12, 13):
for
spring Nt -Pfall*
Aster
-PwinterLarrea
for
summer Nt -PearlySu*
(A) Eriogonum
-PearlySp*
and -PlateSu Menodora
-PearlySpParthenium
-PearlySu Dalea
-PearlySu Dyssodia acerosa
-PearlySp* Zinnia
In all but one case the inverse relationship is
effected before the phonological season of flowering; in one case it is during
the flowering season.
In 20 cases rainfall is directly related to flowering Ntas one of the two most important predictive variables:
for spring Nt +PearlySp
(A) Phacelia
+PlateSp* and
+PlateSu* (A) Malacothrix
+PlateSp* Aster
+PlateSp*Dalea
+PearlySp D. pentachaeta
+Pwinter Houstonia
+PearlySu* and +PearlySp Bahia
+PearlySp* Krameria
+PlateSp Larrea
+PlateSu*
and +PlateSp Opuntia
In 7
cases the effect occurs in the prior year and hence well before
flowering (6 perennials and 1 annual).
4
effects are before current year
flowering (one A).
1
is during flowering season (Larrea).
for summer Nt +Pfall*
and +PearlySp (A) Baileya
+Pwinter Gutirrezia
+PearlySp Houstonia
+PlateSu*
+PlateSu Parthenium
+Pwinter D. acerosa
2 cases are prior year (one A).
4
are current yr before flowering (1 A).
1
case is during winter vegetative growth (Gutierrezia).
1
is during flowering time.
General
observations during 1994-1999, “exceptional years” show some
general community responses.
(1)
When there is a negative soil moisture index (MI) continuing from the previous
fall, or current winter on into spring, as in 1994, 1996 and 1999, there is failure of spring flowering of
annuals and perennials.
(2)
If the negative MI continues through late spring (1996) or on through fall
(1994) there are obvious signs of stress in leaves, leaf senescence and death
of stems and individual plants. If there is return of normal early summer
rainfall (1996) there can then be recovery of perennial plants and even high or
record Nt by some species. There is a hierarchy
of recovery of plants from stress: Larrea, Parthenium, Zinnia, Flourensia, then
Dalea.
(3)
High winter rainfall (2nd highest in 1995) can produce exceptional flowerings
by annuals, with appearance of rare species, (Table 14), in spite of negative moisture indices in early and late
spring (1995). Spring moisture deficits
can then be followed by failure of summer flowering, in spite of normal or wet
summer (1995).
(4)
Years with a wet and / or warm fall on into following winter can allow the
facultative evergreeness of shrubs and subshrubs on into spring (1997, 1998,
1999).
(5) Results for winter germination of
annuals were ambiguous. Germination was high in 1997, after a W,Nofall
1996 and d,H winter 1997. In 1998, germination was
down to 4% of that of 1997, after a d,C* fall and N,No
winter. Only two seedlings were censused in 1999 after an N,H fall and d, H*
winter.
(6)
There was germination of summer annuals only in 1999 when summer rainfall was
at its maximum and moisture index was a maximum of +4.5 for
the 13 years of record. (Germination was not censused before 1997.)
WHAT ARE
THE POSSIBLE DIFFERENT PHENOLOGICAL
NICHES
OF THESE PLANT SPECIES?
Overall, for all species that have predictable
relationships to independent variables (Tables 12, 13), there
is no case in which species have the
same two most predictive variables! It
is as if, for flowering Nt, each of these
species has its own adaptive niche of rainfall and temperature sum spread over
six phenological seasons of the current and previous year.
I
suggest that for this site there are at least 15 categories of plants, with
regard to their pattern of flowering.
This variety of responses parallels the multiplicity of ways in which
desert annuals disperse their seeds and germinate (Gutterman,
1994) and recruit seedlings (Harper, 1977).
Abd El-Ghani (1997)
found six different patterns of phenological behavior
among 10 species in runnels and wadis of
SPRING-ONLY BLOOMING PLANTS_____
(1) Early blooming annuals with no
significant relationships to rainfall and temperature: The three earliest
blooming winter annuals (Table 7) flowered erratically in
small numbers and their census data did not provide significant predictive
models. They may be limited by spatial distribution of suitable microsites for
recruitment of seedlings. When
conditions for germination and survival are marginal, they bloomed only in
small scattered spots. Widespread blooming occurred only under very favourable
conditions. The earliest flowering
annual, Draba cuneifolia (DC,
Table 11b) did not exceed a spring total bloom of 207
until 1995 when Nt was 192,000. This production based on the soil seed bank
was possibly triggered by the 1995 winter rainfall, which not only ranked
second in amount, but had the most even weekly distribution of rain of any
winter. The warm early spring may also have been a factor. Gilia sinuata (GU Table 11b) and LesquerellaGordoni (LG)
behaved similarly.
(2) Rain-dependent
early spring-blooming annuals. Phaceliacrenulata (PC Table
11a), which did not begin to bloom until late in early spring (wk 14), had
a marginally significant relationship to rainfall in the current early spring (Table 12).
The current year flowering of MalacothrixFendleri (MF)
had a strong relationship to rainfall of late spring and late summer of the previous
year. There are several ways in which the prior conditions could have
conditioned seeds in the seed bank to produce flowering in the next year (Gutterman, 1944; Harper, 1977),
(3) Early
spring-blooming geophytes: Cymopterus multinervatus (CM), the earliest flowering perennial,
and Dichelostema pulchellum (D)
flowered erratically 1987-1993. Both
species had exceptional blooms in spring 1995 (Table 14). Some of these flowering individuals may have
developed from seed, however they probably grew from buds in a soil
bud-bank. Some geophytes have a delay in
a juvenile stage be- fore blooming (Harper, 1997:689). Young plants with a
single leaf were observed emerging with winter annuals in 1997, but did not
bloom; only individuals with more leaves flowered.
(4) Succulents:
Opuntia phaeacantha (OP)
density was very low and its flowers were open only a few days, but individuals
were obvious and were accurately censused.
Spring Ntwas significantly predicted by rainfall in late summer of the previous
year and in the current late spring (Table 12). Storage of water during the previous summer
is probably important for the plants’ survival of desiccating conditions
before the next spring, which can be acute in some years as in 1998-1999.
Few O. spinosior
and Echinocereus flowered.
(5) Perennial
subshrubs with significant relationship to previous year: Spring bloom of both Aster
hirtifolius (AH) and Dalea
(6) Herbaceous
perennials with no significant relationships: Erigeron divergens(ED) had spring Nt
ranging from 0 to 417; there was no significant regression model. This may be
due to the fact that the distribution of Erigeron was
limited by some factors to only two or three patches within the census transect
in each year.
FOR SPRING AND SUMMER FLOWERING SPECIES_____
(7)
Annuals with biseasonal flowering: Gilia longflora (GL) is exceptional in that all plants
germinate in winter, but then have some individuals
that flower only in the spring, some that flower only in the summer, and some
that flower in both seasons. There may
be a genetic basis for these phenotypes (LeBuhn,
1998). In the present site flowering of G. longiflora was negatively related
to temperature sum in both spring and summer (Tables 12, 13). Variation of summer flowering was partly
predicted by a positive relationship to spring bloom (R2 = 0.30); possibly a spring success of blooming by biseasonal
individuals results in their summer success also. Or, it may have been some other interaction
of the three phenotypes. LeBuhn (1998), who worked at a location 6 km south of the
present site, found that the ratio of flowering of the three phenotypes was
quite different in two successive years.
Baileya multiradiata (BM) bloomed predominantly in the
summer (81% for years 1987-1994 (Table 11a). When there were exceptionally warm winters,
individuals overwintered in a rosette stage and flowered the next spring, i.e.
were faculatively biennial, as in
1998-1999. Flowering is predicted by a
mix of variables of the previous and current years (Tables
12, 13).
(8) Herbaceous
perennials with seasonal emphasis: Krameria lanceolata (KL) and Dyssodia pentachaeta (DP)
bloomed predominantly in the spring (61% and 73% respectively), when they had
predictive relationships to conditions in the previous year (Table
12), particularly rainfall in early spring.
Neither had a significant summer mod-el.
(9) Subshrubs
with no definite seasonal bias: Dyssodia acerosa (DA) seemed to be able to flower after almost
every rainy period regardless of season. Overall, spring Nt
was significantly related to the previous spring and summer, favored by
rainfall then and adversely affected by temperature. Summer Ntwas positively related to rainfall in winter of the current year, but was
inversely related to early summer rain-fall.
Zinnia pumila
(ZP) bloomed predominantly in summer, when Nt was significantly related to conditions
of the previous year. Spring flowering
was erratic and had no significant model.
(10)
Evergreen shrub with seasonal emphasis but seasonal flexibility: Larrea tridentata
(LT) is the principal shrub that invaded this degraded grassland site, mainly
in the period 1938-1948 (Chew and Chew,
1965). In 1959 its canopy covered 17.4%
of the ground and was 84.1% of the total plant cover.Larrea
is present in two states: as scattered individual shrubs and as clumps of large
shrubs on and around the abandoned mounds of the kangaroo rat, Dipodomys,
an inhabitant of the original grassland (Chew and Whitford,
1992). The data herein are for the
blooming of the scattered shrubs. The predominant spring bloom of Larrea tridentata
was significantly predicted by a positive relationship to rainfall in late
spring (R2 = 0.62), which
is its main blooming period, and a negative relationship to winter rainfall (R2 = 0.31). The
“special” characteristics of Larrea may depend on its
evergreeness. When Larrea are
given supplemental water in spring, a
greater proportion of assimilate is allocated to
vegetative growth and a reduced proportion to reproduction, whereas water-stressed
plants allocate more to reproduction (Cunningham et al.,1979). The same may occur in relation to natural variations of
winter-spring rainfall. In 1990, when
winter rainfall was at a minimum (7
consecutive wk without rain) and spring bloom of many perennials was low or
zero, Larrea had its second largest spring bloom, Nt = 28, and then had its only
marked summer bloom, Nt = 90, 90% of which occurred in W
31 after the early summer rains. This is consistent with the observation of
Showalter et al. (1999) that plants that were experimentally water-deprived had
significantly more flowers than other individuals. Larrea had the phenotypic plasticity to
respond to the summer rainfall in 1990, although it did not so in 1988, when
winter rainfall was much higher than in 1990.
SUMMER ONLY BLOOMING SPECIES._____
(11) Summer-flowering
annual: The phenology of Eriogonum Abertianum (EA) has been studied in detail by Fox
(1989) at sites in the
(12) Subshrub
with winter vegetative growth and summer flowering: Gutierrezia sarothrae (GS) is a weedy perennial in degraded
grasslands; its success is partly due to its early regrowth of leaves in
winter, before any other perennial. Gutierrezia germinates in winter along with the
winter annuals. Variation of summer
bloom was largely explained by a direct relationship with winter rainfall (R2 = 0.66). The overall model is
suspect because it depends on four other variables in the current year. The early vegetative growth must survive as
the basis for summer reproduction, which does not always happen. In the extreme drought and heat of early
summer 1994 (Table 4) 90% of Gutierrezia died
and population density was still reduced in 1996. Again, in the dry winter-late spring of 1999
only 4.4% of individuals survived from winter into summer.
(13) Subshrub
with spring vegetative growth: Parthenium incanum (P) is
facultatively winter deciduous, usually retaining only a few small terminal leaves through
winter. New leaf and then stem growth
occurs in early spring. Variation off
summer bloom, which reaches its peak in W 36-41, is mainly predicted by
rainfall of late summer (R2 = 0.61), with some
negative effect of rainfall in early spring.
Possibly in some years water can pool up in the shallow soil over the
caliche layer and partly drown the roots of Parthenium, limiting later
vegetative and reproductive growth. A
defoliation of Parthenium was observed 29 Aug.
1987 that was possibly due to large rainfalls in July and Aug. (106 mm,
W29-31). However, no defoliation
occurred after even larger rains in 1988 (204 mm W33-36) and 1990 (116 mm
W33-34).
(14)
Herbaceous perennial: Menodora scabra (MS)
bloomed principally in the summer, with <5% of individuals flowering in
spring. Summer Nt
is predicted by an inverse relationships to precipitation in early spring of
the previous year (R2 = 0.66) and rainfall of
the current late summer (R2 = 0.14).
FALL BLOOMING SPECIES. _____
(15) Flourensia cernua (FC)
was remarkable for its delay of flowering (days 279-305 on average) until fall
and early winter, as herein defined as phenological seasons. Flourensia flowered in only 4 yr, 1989-1991 and
then maximally in 1994 (Nt = 125), for
no obvious reason.
POTENTIAL
FOR SPECIES INTERACTION
The Nt values for
individual species (Table 11) show the great variety of
species’ responses to the variable weather through the years. There was
no clear general pattern of responses by the plant community, except to very
low moisture availability. A prime
example of phenological differences, and even possible interaction among
species was that of two spring-summer blooming annuals, Gilialongiflora and Baileya multiradiata,
and the spring-summer herbaceous
perennial,
None
of these species bloomed in spring 1990.
Then from 1990-1995: (1) Bahia had its
maximum bloom in the wet (W) late summer 1990, after the drought, drawing upon
resources in its roots. There was no
competition for soil resources from annuals then, since they had not
germinated. However, thereafter both spring
and summer flowering of
These
species contrast markedly in their recovery of flowering after failures to
bloom in 1990 and 1994, and in their subsequent success. The flowering of annuals, based on seed
banks, was more successful than that of the herbaceous perennial, and their
successes coincided with a decline of flowering of Bahia. Guo and Brown
(1997) concluded that there is a negative interaction between spring and winter
annuals at their research site 8 km from the present site. There may also be a negative interaction
between spring-summer flowering annuals and herbaceous perennials. The genetic
programming of these species must interact,
probably in several ways, with the changing independent variables of
weather to produce the observed differences in flowering. Differences in
genetic programming were obvious in the sequences of germination and plant development observed in
1 m2
quadrats 1997-1998 (to be
reported in detail elsewhere). Five
annual species were present together as small seedlings by Feb. 6, 1997. Additional seedlings of all species were
added through Apr. 16-25 in an 11 wk span of germination. April 11 there were 41/ m2 Baileya and 18/ m2 G. longiflora. The advantage
Gilia may have over Baileya is
that while the latter was still in a rosette stage on April 11, Gilia, not
a rosette-forming species, had be-gun stem growth and some plants were in
flower bud and flower, thus
“getting a jump” on the use of soil resources for
reproduction. The perennial Bahia did not
renew above ground growth until March 21-25, but then grew rapidly, and some
plants were in flower bud by Apr.11. Gutterman (1994) emphasized the variety of ways species
differ in their germination. Phillipi (1993a), who worked on germination of six species
of annuals 8 km from the present site, found that seeds that do not germinate
in a first year may germinate the second
year, under “the same
conditions”; that the fraction of
seeds germinating is not the same in the 2nd year; and that germination under
good conditions after a bad year differs among species. Inouye (1989), working in the Sonoran Desert,
found that the removal of seedlings as they appeared led to more germination,
as compared to control plots. I did not
find this to occur in 1997-1998, when seedlings were removed from two quarters
of each 1 m2quadrats
while none was removed in the other two quarters (control).
OTHER
INDEPENDENT VARIABLES
It is
instructive to briefly consider the possible effect of several other factors on
species phenologies.
Light,_____ Photoperiod and
the annual cycle of light intensity undoubtedly have a role in determining the
sequence of the blooming of the present species (Table 7),
but because of their interannual reliability they are not a variable affecting
Nt. Photoperiod has been
suggested to affect flowering of spring-only desert species (Acker-man and
Bamberg, 1974), and species in deserts with two rainfall periods (Fox,
1990). It has been documented as a cue
for flowering in Cercidium microphyllum (Bowers and Dimmitt,
1994). If temperature is adequate,
photoperiod can have a role in the germination of some desert annuals (Gutterman, 1994). In
Arabidopsis a hexokinase coordinates intrinsic
signals with extrinsic light intensity to affect flowering and many other plant
processes (Moore et al., 2003).
Pollinators._____ It is unlikely that pollinator abundance can
cause variations in the amount of blooming, except as variation in pollinator availability
affects seed set and thus the size of the seed bank and future germination.
There has been much study of the effect of pollinators on the timing of
blooming and patterns of interspecies flowering, but effects are seldom
demonstrated (Schemske et al., 1978). There is no
unambiguous example of adaptation of phenology to pollinators in U.S. desert
ecosystems, except for Fouquieria splendens (Waser, 1979).
This
is not unexpected in the context of a semiarid site, where it would be
difficult for plant populations that are influenced by the inconstant weather
of a site to track the presence of pollinators, also influenced by weather
variation. LeBuhn
(1998) studied the pollination of Gilia (=Ipomopsis) longiflora at
a site 6 km SSE of the present study plot.
Of the 671 visits of potential pollinators in 1994 and 1995, 99% in the
spring and 71% in summer were by hawk moths (Sphingidae)
and 1% and 19% respectively were solitary bees of three genera. The long-tongued moths are able to get the
nectar at the bottom of the 10-50 mm-long corolla tubes. Gilia might
be expected to flower in coordination with its predominant pollinator, but
information is not available on the timing of Sphingidae
presence and abundance.
Many
species of bees visit the flowers ofLarrea tridentata
and 22 species of solitary bees feed only on Larrea
nectar and pollen (Hurd and Linsley,
1975), so there should be no problem of pollination of this species. Insects sweeps in the present site (Chew,
unpublished) demonstrated the presence of many species of insects that are
documented as important pollinators by Proctor, Yeo
and Lack (1996), and hence available to the plant community.
Granivores. _____ Granivorous ants and
rodents have a well documented effect on the composition and abundance of
desert annual assemblages at a location 8 km SE of the present study site
(Brown and Heske, 1990; Samson et al ., 1992; Guo and Brown, 1996).
However, granivores cannot be an important independent variable in the
interannual variation of flowering of annuals unless there is considerable
variation of granivore numbers year-to-year.
This can occur, as it did on a degraded desert grassland site in New
Mexico very similar to the present site (Whitford,
1976). However, such a potential effect would probably be damped out due to
time lags in the responses of annuals, as found by
Samson et al . (1992). On the present site there has been a decline of granivorous rodents through 35 years (Chew,
unpublished).
CONCLUSIONS
I
think it is reasonable to speculate that the biodiversity of the dicots of this
semiarid ecosystem is a function of the interaction of the great variety of
rainfall and temperature conditions, year to year, with the many phenotypes of
the available plants, as they have assembled into the community in the short
term and possibly further adapted in the long term. The different plant phenotypes provide a
spread of blooming times over the year and have adaptations that fit the
different intra-annual and inter-annual
variations of rainfall and temperature in successive phenological seasons
through the year. The complications of variations of germination and of
physiology of allocation of resources, and some preemptive competition of
resources give shifting advantages within the mix of species.
The
general conclusions of Turner and Randall (1987) and others are largely
confirmed. The magnitude of flowering of
a majority of species can be predicted from rainfall and air temperature. These variables often have opposite effects.
Sometimes predictive models can accommodate years of exceptional high or low
rainfall. The significant predictive variables usually occur well before the
period of blooming, even in the previous year.
DEDICATION
This article
is dedicated to my father, Harry A. Chew, who introduced me, unknowingly, to
ecology, through the observation of the blooming times of wild flowers in the
deciduous woodlands of West Virginia.
ACKNOWLEDGMENTS
Revision
of this article has greatly benefited from comments by the Editor and two
anonymous reviewers of The American Midland Naturalist. Discussions through the years with Walter G.
Whitford, James H. Brown, Fred B. Turner and Thomas Valone have been an ongoing stimulus
LITERATURE
CITED
Abd El-Ghani, M. M. 1997. Phenology of ten
common plant species in western
Ackerman, T. L. and S. A. Bamberg. 1974.
Phenology studies in the Mojave Desert at RockValley
(Nevada Test Site). p. 215-226 In:: H. Leith (ed.). Phenology
and seasonality modeling. Ecological Studies, Vol. 8, Springer-Verlag, New York.
_______________., E. M.
Romney, A. Wallace and J. E. Kinnear. 1980. Phenology
of desert shrubs in southern Nye County, Nevada.Great
Basin Nat. Mem.,
4:4-23.
Andrade, E. R. and W. D. Sellers. 1988. El Nino and its effect on precipitation in
Arizona and western New Mexico. J. Climatol.,
8:403-410.
Beatley, J. C. 1974. Phenological events and their environmental triggers in
Bowers, J. E. and M. A. Dimmitt. 1994.
Flowering phenology of six woody plants in the northern SonoranDesert.
Bull. TorreyBot. Club,
121:215-227.
Brown, J. H. and E. J. Heske.
1990. Control of a desert-grassland transition by a keystone rodent guild.
Science , 250:1705-1707.
Burke, I. C., W. K. Lauenroth
and W. J. Parton. 1997. Regional and temporal
variation in net primary productivity and nitrogen mineralization in
grasslands. Ecology , 78:1330-1340.
Chew, R. M. 1982. Changes
in herbaceous and suffrutescent perennials in grazed and ungrazed desertified
grassland in southeastern
____________and A. E.
Chew. 1965. The primary productivity of a desert shrub (Larrea tridentata) community.
Ecol. Monogr.,
35:355-375.
____________and W. G. Whitford. 1992. A long-term positive effect of
kangaroo rats (Dipodomys spectabilis)
on creosotebushes (Larrea tridentata). J. Arid Environ..,
22:375-386.
Cunningham, G. L., J. P. Syvertsen,
J. F. Reynolds and J. M. Willson. 1979. Some effects
of soil-moisture availability on above-ground production and reproduction in Larrea tridentata
(DC) Cov.Oecologia,
40:113-123.
Dahm, C. N. and D.
I. Moore. 1994. The El Nino/Southern Oscillation phenomenon at the Sevilleta long-term ecological research site. p. 12-21
In: D. Greenland (ed.), El Nino and
long-term ecological research (LTER) sites. Pub.
No.18, LTER Network Office, Univ. of Washington, Seattle.
Diaz, H. F. and V. Markgraf.
1992. Historical and paleoclimatic aspects of the
Southern Oscillation. Cambridge University Press, Cambridge, UK.
Dunnett, N. P., A. J.
Willis, R. Hunt and J. P. Grime. 1998. A 38-year study of relations between
weather and vegetation dynamics in road verges near Bibury,
Glouchestershire. J. Ecol.., 86:610-623.
Epstein, H. E., W. K. Lauenroth,
I. C. Burke and D. P. Coffin. 1997. Productivity patterns of C3 and C4 functional types in the
U. S. Great Plains.Ecology , 78:722-731.
Estabrook, G. F., J. A.
Winsor, A. G. Stephenson and H. F. Howe. 1982. When
are two
phenological
patterns different? Bot. Gaz.,
143: 374-378.
Fitter, A. H., R. S. R. Fitter, I. T. B.
Harris and M. H. Wlliamson. 1995. Relationships
between first flowering date and temperature in the flora of a locality in
central England. Funct. Ecol., 9:55-60.
Fox, G. A. 1989. Consequences of
flowering-time variation in a desert annual: adaptation and history. Ecology,
70:1294-1306.
____________1990.
Components of flowering time variation in a desert annual.Evolution ,
44:1404-1423.
French, N. and R. H. Sauer. 1974.
Phenological studies and modeling in grasslands. p. 227-236 .
In: Leith, H. (ed.) Phenology and
seasonality modeling. Springer-Verelag, New York.
Guo, Q. and J. H.
Brown. 1996. Temporal fluctuations and experimental effects in desert plant
communities. Oecologia , 107:568-577.
____________1997. Interactions between winter and summer annuals in the ChihuahuanDesert. Oecologia,111:123-128.
Gutierrez, J. R. and W. G. Whitford. 1987. Chihuahuan Desert
annuals: importance of water and nitrogen. Ecology ,
68:2032-2045.
Gutterman, Y. 1994. Strategies of seed dispersal and germination in plants inhabiting
deserts. Bot. Rev.,
60:373-425.
Harper, J. L. 1997. Population biology of
plants. Academic Press, New York. 892 p.
Hawkinson, R. O. 1968.
Cover, soil, and microrelief characteristics which
influence runoff on a desert grassland range. M.S. Thesis. Univ. Arizona,
Tucson. 91 p.
Hurd, P. D. and E.
G. Linsley. 1975. The principal Larrea
bees of the southwestern United
States (Hymenoptera: Apoidea). Smithson. Contr. Zool. , No. 193, 74 pp.
Inouye, R. S. 1989. Density-dependent
germination response by seeds of desertannuals.Oecologia, 46:235-238.
____________, G. S. Byers
and J. H. Brown. 1980. Effects of predation and competition on survivorship,
fecundity, and community structure of desert annuals. Ecology, 61:1344-1351.
Kearney, T. H., and R. H. Peebles. 1960.
Arizona flora.2nd ed. With supplements. Univ. California
Press, Berkeley. 1085 p.
Kemp, P. R. 1983. Phenological
patterns of ChihuahuanDesert plants in relation to
the timing of water availability. J. Ecol., 71:427-436.
LeBuhn, G. 1998. The evolutionary significance of bimodal flowering in Ipomopsis longiflora.
Ph. D. dissertation. Univ.
Leith, H. (ed.) 1974. Phenology and seasonal
modeling. Ecological Studies Vol.8.Springer-Verag,
Lindsey, A. A. and J. E. Newman. 1956. Use
of official weather data in springtime temperature analysis of an Indiana
phenological record. Ecology, 37:812-823.
Lyons, E. E. and G. A. Fox (organizers).
1996. Symposium: Timing is everything: new perspectives on the ecology and
evolution of floral phenology. Bull. Ecol. Soc. Am. , 77.
Menzel, A. and P. Fabian. 1999. Growing season extended in Europe. Nature,
397:659.
Moore, B., L. Zhou, F. Rolland, Q. Hall, W.
Cheng, Y. Liu, I. Hwang, T. Jones and J. Sheen. 2003. Role of the Arabidopsisglucose
sensor HXK1 in nutrient, light, and hormonal signaling.
Science ,300:332-336.
Pake, C. E. and D.
L. Venable. 1995. Is coexistence of SonoranDesert
annuals mediated by temporal variability in reproductive success? Ecology,
76:246-261.
____________1996. Seed
banks in desert annuals: implications for persistence and coexistence in
variable environments. Ecology,
77:1427-1435.
Philippi, T. 1993a. Bet-hedging germination
of desert annuals: beyond the first year. Am. Nat., 142:474-487.
____________ 1993b. Bet-hedging
germination of desert annuals: variation among populations and maternal effects
inLepidium lasiocarpum. Am. Nat.., 142:488-507.
Proctor, M., P. Yeo
and A. Lack. 1996. The natural history of pollination. Timber Press, Portland, Oregon.
Rathcke, B. J. and E.
P. Lacey. 1985. Phenological patterns of terrestrial
plants. Annu. Rev. Ecol. Syst.,
16:179-214.
Sala, O. E. and W.
K. Lauenroth. 1982. Small rainfall events: an
ecological role in semiarid regions.Oecologia,
53:301-304.
Samson, D. A., T. E. Philippi,and
D. W. Davidson. 1992. Granivory and competition as
determinants of annual plant diversity in the ChihuahuanDesert.
Oikos, 65:61-80.
SAS INSTITUTE, INC.. 1995. JMP Version 3.1.
SAS Institute, Inc., Cary, NC.
Schemske, W. E., M. F.
Willson, M. N. Melampy, L.
J. Miller, L. Verner, K. M. Schemske
and L. B. Best. 1978. Flowering ecology of some spring woodland herbs. Ecology,
59:351-366.
Scifres, C. J. and J.
H. Brock. 1969. Moisture-tempeerature interrelations
in germination and early seedling development of mesquite. J. Range Manage., 22:43-37.
Showalter, T. D.,
Simpson, G. G. and C. Dean. 2002.
Arabidopsis, the Rosetta Stone of Flowering
time? Science , 296:285-289.
Sparks, T. H. and P. D. Carey. 1995. The
responses of species to climate over two centuries: an analysis of the Marsham phenological record, 1736-1947. J. Ecol.,
83:321-329.
Turner, F. B. and D. C. Randall. 1987. The
phenology of desert shrubs in southern Nevada. J. Arid
Environ., 13:119-128.
Waser, N. M. 1979.
Pollinator availability as a determinant of flowering time in ocotillo (Fouquieria splendens)
. Oecologia , 39:107-121.
Went, F. W. 1949. Ecology of desert plants.
II. The effect of rain and temperature on germination and growth. Ecology,
30:1-13.
Whitford, W. G. 1976. Temporal fluctuations in density and diversity of desert rodents.
J. Mammal., 57:351-369.
Whitford, W. G. and J.
R. Gutierrez. 1989. Effects of water and nitrogen supplementation on phenology,
plant size, tissue nitrogen, and seed yield of Chihuahuan Desert
annual plants. Southwest. Nat., 34:546-549.
-----------------------------
Note: Italics are not used herein because they are not
compatible with certain makes of computers when referencing web-site
material. Scientific names are
underlined.
Table 1.
Rainfall (mm) by phenological
seasons. Mean is based
on 13 y of data 1987-1999.
Underlined numbers are minimum and maximum for
each season.
Season | Mean | cv | 1987 | 1988 | 1989 | 1990 | 1991 | 1992 | 1993 | 1994 | 1995 | 1996 | 1997 | 1998 | 1999 |
Winter | 80.2 | 0.57 | 125 | 94 | 69 | 11 | 80 | 154 | 122 | 42 | 136 | 17 | 54 | 97 | 42 |
Early
Spring | 46.1 | 0.55 | 42 | 59 | 18 | 21 | 63 | 57 | 38 | 46 | 45 | 29 | 53 | 112 | 16 |
Late
Spring | 26.8 | 0.91 | 34 | 25 | 4 | 30 | 19 | 91 | 29 | 13 | 3 | 48 | 42 | 6 | 4 |
Early
Summer | 64.7 | 0.53 | 106 | 87 | 69 | 75 | 67 | 84 | 19 | 15 | 51 | 67 | 19 | 52 | 130 |
Late
Summer | 114.2 | 0.65 | 80 | 297 | 66 | 210 | 102 | 73 | 84 | 96 | 162 | 46 | 162 | 24 | 92 |
Fall | 20.4 | 0.88 | 23 | 62 | 30 | 22 | 8 | 6 | 19 | 8 | 4 | 49 | 10 | 22 | 2 |
YEAR | 352.4 | 0.3 | 410 | 624 | 256 | 369 | 341 | 465 | 311 | 220 | 401 | 256 | 340 | 313 | 286 |
Distribution of 287 rainfall events over 5 y (1980, 1984-1987). | ||||||
0.1-2.5
mm | 2.6-5
mm | 5.1-10
mm | 10.1-15
mm | 15.1-20
mm | >20
mm | |
Frequency
of event | 0.491 | 0.174 | 0.153 | 0.07 | 0.05 | 0.056 |
Average
proportion of annual rainfall | 0.102 | 0.117 | 0.208 | 0.159 | 0.151 | 0.262 |
Temperature
summation (degree days C) by phenological seasons. |
Underlined values
are maximum and minimum for each season. |
Season | MEAN | cv | 1987 | 1988 | 1989 | 1990 | 1991 | 1992 | 1993 | 1994 | 1995 | 1996 | 1997 | 1998 | 1999 |