WETLANDS, Vol. 22, No. 2, June 2002, pp. 347–354
q 2002, The Society of Wetland Scientists
TILLER POPULATION DYNAMICS AND PRODUCTION ON
SPARTINA DENSIFLORA (BRONG) ON THE FLOODPLAIN OF THE
PARANÁ RIVER, ARGENTINA
Ricardo L. Vicari, Sylvia Fischer, Nora Madanes, Stella M. Bonaventura, and Verónica Pancotto
Departamento de Ciencias Biológicas
Facultad de Ciencias Exactas y Naturales
Universidad de Buenos Aires
Pabellón II, Ciudad Universitaria
C1428EHA Buenos Aires, Argentina
E-mail: [email protected]
Abstract: Tiller dynamics and net aerial primary productivity (NAPP) were studied in permanent sample
plots of Spartina densiflora at Otamendi Natural Reserve (Buenos Aires Province, Argentina) from June
1996 to December 1997. Emergence, growth, senescence, survival, biomass dynamics, and tiller productivity
were analyzed. These population attributes varied seasonally during the first study year, whereas variations
were not detected in the subsequent year. Tiller density increased slightly during the first twelve months,
attaining 2445 6 869 tillers·m22, then remaining constant until the end of the study period. Senescence rate
was lower than emergence rate on most sampling occasions. Cohorts originated in different seasons showed
distinct survival curves. The life span of tillers was at least 18 months. Green biomass reached maximum
values (771 6 410 g·m22) during the first year but decreased during the last six months of observations.
Annual NAPP was 1450 6 566 g·m22·y21. Average productivity rate was higher in the first year than in the
second year. The decrease in the population density of tillers of S. densiflora and the increase in its senescence rate were more likely related to grazing and flooding than to population dynamics.
Key Words:
densiflora
tiller population dynamics, primary production, non-destructive method, salt marsh, Spartina
INTRODUCTION
(Mitsch and Gosselink 1993), S. alterniflora grows in
areas adjacent to the estuary or the sea, while S. densiflora replaces Spartina patens (Aiton) Muhl., occupying the highest areas of the marsh. Riverine marshes
are dominated by S. densiflora.
Coastal marshes in the province of Buenos Aires
undergo tidal action and seawater flooding. Our study
site is a marsh located in the Lower Delta of the Paraná
River flood plain. This delta forms the lower section
of Del Plata Basin, one of the largest South American
basins together with those of the rivers Amazon and
Orinoco (Kandus 1998). This S. densiflora salt marsh
can be classified as a salt marsh formed in a deltaic
area, mainly developed where a large river approaches
its lowest energy coasts, and where the main source
of mineral silt is riverine (Mitsch and Gosselink 1993).
The flooding levels and periodicity that affect the research area are determined by the combination of the
hydrologic regime of the river and rainfall. In this way,
it is probable that the system accumulates nutrients
contributed by precipitation, overland flow, and
ground water (Westlake et al. 1998). The saline environments in this site are related to the presence of
marine sediments laying at a very shallow depth that
Spartina spp. is among the most important plant
taxa found in salt marshes, which are among the most
productive ecosystems on earth (Mitsch and Gosselink
1993). Salt marshes are found in middle and high latitudes along intertidal shores throughout the world.
Different plant associations dominate in different
coastlines, but the ecological structure and function of
salt marshes is similar worldwide. According to Chapmans work (Mitsch and Gosselink 1993) Spartina sp.
is dominant, or at least present, in the following geographical groups of salt marshes: northern Europe,
northeastern and western North America, eastern Asia,
Australia, and South America. Our study site presents
some similarities with those of eastern North America,
mainly the subgroups of New England and Coastal
Plain (Mitsch and Gosselink 1993).
Two types of Spartina marshes are found in Buenos
Aires Province: estuarine or coastal, and riverine. The
first type attains its maximum extent in Samborombón
Bay, where Spartina densiflora Brong. and Spartina
alterniflora Loiseleur dominate. Resembling the salt
marshes of the Atlantic Coast of North America
347
348
were deposited during the Querandinense period of
marine ingression in the early Holocene (Iriondo and
Scotta 1978).
The aerial primary productivity of these ecosystems
depends on their exposure to tidal activity and on
freshwater flow, which produces variations in salinity
and nutrient supply. The extent of the growing season
and the availability of solar energy are also important,
and both are directly related to latitudes having warm
climates (Mitsch and Gosselink 1993). The duration of
the growing season is of primary importance in the
productivity of Spartina. When this genus develops in
zones having a short active growing period, most photosynthetic products accumulate inside underground
structures and are used at the beginning of the spring
growth. On the other hand, in warm climate regions,
photosynthesis occurs practically year-round, and underground accumulation does not take place (Gallagher 1983).
Spartina densiflora is a matted perennial gramineae
with strong short rhizomes; it grows in salt marshes
along the southern coasts of Brazil, Uruguay, Argentina, and Chile (Cabrera 1970). These populations develop mainly through vegetative growth, via the underground interconnected tillers. Due to the difficulty
in differentiating true individuals (genets) of S. densiflora, this species can be treated as a population of
leaves and stems (modules) or ramets (Begon et al.
1996). Following this approach, the different secondary and tertiary axes, or tillers of a ‘‘genet’’ acquire
identical biological meaning as modules of growth belonging to a given clone. Therefore, the productivity
of the population is given by total births, growth, and
deaths of individual tillers (Dai and Weigert 1996).
The emergence and death of tillers depend on the
length of the growing season, soil fertility, particular
weather features, grazing, etc. Consequently, knowledge of the dynamics of tiller populations may reveal
important aspects of the performance of marsh species,
whereas the number of tillers in relation to their biomass can help at understanding total annual productivity (Westlake et al. 1998).
Very little is known about the general functioning
of marsh systems in Argentina, and nothing has been
published so far on tiller population dynamics and productivity in S. densiflora. Therefore, based on the
above-mentioned arguments, we propose the following
questions. Are new tillers produced year round? Do
emergence and senescence rates of tillers vary
throughout the year? How long is the life span of tillers? Is life span related to the emergence time? Is net
aerial primary productivity related to the production of
new tillers? Our work intends to answer these questions through a demographic analysis and a study of
the biomass dynamics of S. densiflora tillers by means
WETLANDS, Volume 22, No. 2, 2002
of a non-destructive method applied on permanent
sample plots.
MATERIALS AND METHODS
Study Site
The study was carried out from June 1996 through
December 1997 in the Otamendi Natural Reserve
(348109S, 588489W) (Figure 1). This 2380-ha reserve
lies within a warm, humid climate zone, where the
annual mean temperature is 16.38C (22.68C January
mean, 10.58C July mean), and the annual accumulated
rainfall varies between 900 and 1000 mm. Frosts are
frequent during the fall-winter period (INTA 1998).
The greater part of the study site is an extensive alluvial plain of a flat-concave relief dominated by freshwater marshes. In the studied salt marsh, S. densiflora
is absolutely dominant over associated species also
adapted to damp, saline environments, such as Limonium brasiliense ((Boiss.) O. Kuntze), Salicornia virginica (L.), and Atriplex hastata (L.). The studied
community occupies a 440-ha area of clayish and
marshy soils, whose salinities range from 10 to 35 ppt
(Chichizola 1993). This is characteristic of winter
floods originated by seasonal rains and insufficient
drainage, owing to the closeness of the ground-water
table to the surface. The floods produced by the Paraná
River only take place during extraordinary events usually related to ‘‘El Niño’’ (Kandus 1997). During the
summer months, soils remain relatively dry (Bonfils
1962).
An important faunal component in this S. densiflora
salt marsh was the wild guinea pig Cavia aperea, Erxleben 1777. The activities of these strict herbivores,
such as feeding and establishment of trails, produce
severe damage to habitat structure during the winter
(Dalby 1975, Bilenca et al. 1995).
Demographic Analysis
A demographic analysis was conducted by counting
the tillers present in five permanent 10 3 10 cm sample plots randomly established. Counts were conducted
every 30 days in the spring-summer season (September to March) and every 90 days in the autumn-winter
season (April to August). All tillers were tagged at
their bases with self-adhesive tape at the beginning of
the study period. Newly emergent tillers were tagged
on each subsequent sampling date. Tillers that were
not recorded on three consecutive dates were considered as dead individuals.
Vicari et al., SPARTINA DENSIFLORA POPULATION DYNAMICS AND PRODUCTION
349
Figure 1. Location of the study site in the Otamendi Natural Reserve (Argentina). This reserve is located in the flood plain
of the Paraná de las Palmas River, a Paraná River tributary that forms the southeastern boundary of the Paraná Delta.
Biomass Dynamics and Production
All tillers present in each one of the permanent sample plots were measured from their bases to the tip of
their longest leaf, their phenological condition recorded (green, standing dead, partially standing dead, or
reproductive) and signs of herbivory examined. A
height-weight regression was calculated from tillers
harvested on each sampling date from 625-cm2 plots,
near the permanent sample plots. These tillers were
taken to the laboratory to be measured (height from
the base to the tip of the longest leaf) and weighed
after oven drying (72 hours at 608C).
The minimum least squares regression equation obtained was
Log10DW (g) 5 1.930 3 Log10 H (cm) 2 3.703
(R2 5 0.77, p,0.001, n 5 990),
where
DW 5 dry weight and H 5 height.
The total biomass of the permanent sample plots
was estimated by summing the dry weights of tillers
calculated from height data using the regression equation. Daily productivity rates were estimated by summing the positive growth of each individual tiller in
each quadrat, divided by the number of days in the
sampling interval, and then averaged for the five sample plots. The amount of unconsumed material that fell
to the ground was estimated as the sum of the reduced
biomass of individual tillers, calculated from the
length decrease of individual tillers divided by the
number of days in the period, and then averaged for
the five sample plots. A part of the total reduced biomass is made up of the biomass cut by wild guinea
pigs, which was estimated on each sampling date. Net
aerial primary productivity (NAPP) was calculated by
adding the positive growth of all individual tillers in
each quadrat on each sampling period and then averaged for the five sample plots. Annual NAPP was calculated by adding inclusive growth periods between
August 1996 and August 1997. The percentages of
green, standing dead and reproductive S. densiflora
material on each sampling date were estimated by harvesting a 50 3 50 cm plot located at few meters from
the permanent sample plots. These fractions were then
separated, oven dried (72 hours at 608C), and weighed.
Average biomass and productivity, as well as life
span in 10 3 10 cm sample plots, were converted into
g·m22 values by multiplying by the S. densiflora cover
percentage. Cover was estimated through the point
method on 50 3 10 m (one point every 50 cm) random
lines located in the area of permanent sample plots
(Mueller Dombois and Ellenberg 1974).
350
WETLANDS, Volume 22, No. 2, 2002
Figure 3. Survival curve of Spartina densiflora tillers from
the Otamendi Natural Reserve (Argentina) population. Diamonds indicate the depletion curve (sensu Harper 1977). The
other curves represent the survival of tiller cohorts that
emerged on each sampling date.
Figure 2. A) Density variation of Spartina densiflora tillers
from the Otamendi Natural Reserve (Argentina); B) Birth
and death rates of Spartina densiflora tillers from the same
population. Error bars represent means 6 1 SD (n 5 5).
Data Analyses
Since data were not normally distributed, differences among variables were tested by using the non-parametric Friedman Anova. The Wilcoxon Matched Pairs
Test was used to compare pairs of dates. Average values are presented with their respective standard deviations (Zar 1984).
RESULTS
Demographic Analysis
Tiller density showed a significant steady increase
during the first eleven months (p , 0.05, n 5 5, Z 5
2.02) (Figure 2A); starting from 1746 6 501 tillers·m22
in June 1996, it attained 2445 6 864 tillers·m22 in May
1997. Density remained relatively constant after June
1997.
Tiller production occurred during the entire study
period (Figure 2B). The emergence rates of tillers during the August–December periods of both study years
were not significantly different. The emergence rate of
new tillers exceeded 1.2 tillers·m22·day21 from the
spring of 1996 until the winter of 1997, showing a
maximum production in the February–March 1997 period (5.6 tillers·m22·day21 on average). This rate decreased significantly (p , 0.05, n 5 5, Z 5 2.02) starting from the fall of 1997 and continued until the August–September period (early spring). The minimum
value (0.3 tillers·m22·day21) corresponded to August
1997. The emergence rate of new tillers was significantly higher (p , 0.05, n 5 5, Z 5 2.02) in February–
March 1997 than during the rest of the study period.
Tiller senescence rate was generally lower than the
emergence rate, with senescence rates reaching significantly higher values in February–March 1997 (3.8 tillers·m22·day21, p , 0.05, n 5 5, T 5 0, Z 5 2.02), in
coincidence with the emergence rate peak. Tiller emergence and senescence rates were associated on most
sampling dates (Figure 2B). Senescence rate did not
show a significant increase towards the end of the
study period.
Reproductive material was only observed at the beginning of the fall (March and May 1997). Three tillers
out of 293 present in the quadrats flowered in March,
whereas six out of 327 flowered in May. This represents an overall flowering of only 1.4% of tillers (9
out of 620). Nine of the flowering tillers were present
at the beginning of the study, and another one emerged
afterwards (February 1997).
Tiller Survival
The survival curves of S. densiflora tillers throughout the study period are shown in Figure 3. The spring
cohorts of 1996 (starting in September) showed an initial senescence rate greater than the rest of the cohorts;
therefore, fewer tillers correspond to these cohorts. By
contrast, the summer cohorts of 1997 (starting in February) and the winter cohorts of 1996 showed no mortality during the seven months following tiller birth.
Mortality was either very low or non-existent and independent of birth time for all of the cohorts starting
in the fall of 1997. Those tillers present at the beginning of the study period that represent a depletion
curve (sensu Harper 1977) survived until the last sampling date.
Vicari et al., SPARTINA DENSIFLORA POPULATION DYNAMICS AND PRODUCTION
Figure 4. Dynamics of the aerial biomass of Spartina densiflora tillers from the Otamendi Natural Reserve (Argentina) population. Error bars represent means 6 1 SD (n 5 5).
Biomass Dynamics and Production
Seasonal Changes in Green Biomass. The green biomass of S. densiflora showed a peak (725 6 485
g·m22) in June 1996 (Figure 4), a significant decrease
(475 6 345 g·m22, p , 0.05) in August 1996, and a
subsequent increase reaching maximum values (771 6
410 g·m22) in February 1997. From this date on, biomass started to decrease, and during the last six
months, the values recorded were lower than the corresponding season of the previous year. Standing dead
material and green biomass showed opposite behaviors
since they were calculated as percentages of the standing crop. Throughout the study period, dry biomass
was never less than 56% of total biomass. Total biomass remained relatively constant during the first study
year. Starting in the winter of 1997, biomass diminished rapidly down to values close to 50% of the May
figures for the same year.
Growth and Death Rates of Aerial Biomass. Biomass
production occurred during the entire study period
(Figure 5). The annual growth rate started to increase
in August of 1996, remaining high until May 1997.
The maximum growth rate (7.6 6 2.4 g·m22·day21) was
attained between October and December 1996 (spring
and summer), while the minimum rate (0.28 6 0.21
g·m22·day21) was recorded between August and October (early spring of 1997). Growth rates decreased
slightly during the period of greatest productivity (December through February) and then increased from
mid February to March.
Tiller senescence increased gradually throughout the
study period, except for the peak recorded between
July and August 1996 (Figure 6). During the first
months of the study, the decrease in total biomass was
associated with senescence rate. From December 1996
through October 1997, we recorded an uninterrupted
increase in the rate of biomass loss due to herbivores.
351
Figure 5. Seasonal changes in the aerial biomass growth
rate of Spartina densiflora tillers from the Otamendi Natural
Reserve (Argentina) population. Error bars represent means
6 1 SD (n 5 5).
From October to December 1997, the cutting rate by
herbivores was lower than in the seven previous
months (fall and winter); therefore, the increased rate
of biomass loss derived from an increased tissue death
rate. The annual NAPP calculated from August 1996
through June 1997 was 1450 6 566 g·m22·year21.
DISCUSSION
Demographic Analysis
Tiller Dynamics. As observed in tropical climates
(Westlake et al. 1998), the tiller densities recorded in
the Otamendi Natural Reserve remained relatively
high and stable throughout the year (at least 1755 live
tillers·m22). However, Westlake et al. (1998) indicate
that, in warm climates regions like our study site, salt
marshes are stable only during short periods. The high
tiller densities observed in our case may be attributed
to the moderating influence of the Paraná River on the
regional climate and to the stability of the flood plain
that surrounds the study site (Hoffman and Garcı́a
1968). The absence of periodic flood pulses or other
Figure 6. Seasonal changes in senescence rate of aerial biomass of Spartina densiflora tillers from the Otamendi Natural Reserve (Argentina) population. Error bars represent
means 6 1 SD, n 5 5).
352
disturbances may be responsible for the stability of this
salt marsh. As observed by Castellanos et al. (1998)
in Spartina maritima (Curtis) Fernald, from a stable
Mediterranean salt marsh, in our study site, the maintenance of a relatively constant density derives from
the counterbalance of tiller senescence by new tiller
production (Figure 2B). Westlake (1980) pointed out
that any site-species combination has a potential maximum biomass that is reached when so much biomass
has accumulated that respiration by the underground
parts, the stems, and the lower shaded leaves, balances
the photosynthesis by the upper canopy, and further
growth is impossible unless non-productive biomass is
lost. This is often achieved by sloughing the older
leaves or through the death of individual shoots or
plants. As pointed out by Lovett-Doust (1981), this
phenomenon has been reported in several demographic
studies and might follow from one of two scenarios:
either the increased density due to new births caused
the increase in death rate or the reduced density resulting from deaths allowed more births. In our case,
we could not determine whether density-dependence
was due to new tiller emergence or senescence.
Tiller Survival. The low senescence rate of the winter
cohorts of this tiller population may result from a
strong contribution of nutrients from the reserves of
the underground tissues (Lytle and Hull 1980a, b, Gallagher and Howarth 1987). Similar trends have been
observed by Dai and Wiegert (1996) in populations of
Spartina alterniflora, especially in the tall forms of
Georgia marshes growing in well-oxygenated soils of
low salinity. The same authors also state that populations developing in highly saline soils with low oxygen
due to water logging, have a higher initial death rate
probably because tillers of the tall population had more
nourishment from larger underground reserves. The
survival of the herein-studied cohorts of S. densiflora
exceeded 18 months. Such a period is longer than the
survival rate reported for the tall form of S. alterniflora
in Georgia marshes (Dai and Weigert 1996) but similar
to that of S. maritima in a stable sward site in a Mediterranean salt marsh (Castellanos et al. 1998). The
similar survival rates of S. densiflora (this study) and
S. maritima (southwestern Spain) may result from the
stability of both sites, where no significant open space
was available for colonization. As pointed out by Castellanos et al. (1998) the individual cohorts followed
more or less parallel tracks, with a low, constant risk
of mortality during the two years of observations. In
our case, poor flowering may be related to the high
density and long life of S. densiflora tillers, as observed on S. maritima by Castellanos et al. (1988) and
in other perennial herbaceous species (Harper 1977).
WETLANDS, Volume 22, No. 2, 2002
Figure 7. Precipitation and temperature values corresponding to Otamendi Meteorological Station (INTA 1998), located at approximately 5 km from the study site. Black bars:
average values for the 1979–1995 period, white bars: values
for 1996, squared bars: values for 1997.
Biomass Dynamics and Production
Seasonal Changes of Green Biomass. The greatest
values of green aerial biomass of S. densiflora are
comparable to the green aerial biomass of S. alterniflora reported for different locations in the U.S. (Turner 1976, Gallagher et al. 1980, Dai and Weigert 1996).
The decrease in biomass and primary productivity observed during the last months of study was linked with
almost permanent flooding of the soils, owing to the
high amount of rainfall (600 mm) accumulated from
September to December 1997 (Figure 7). Such rainfall
volume represents 60% of the annual precipitation of
1997, whereas it represents only 33.5% of annual
mean precipitation for the 1979–1995 period (INTA
1998). Prolonged floods may have caused a state of
anoxia or waterlogging in the roots and a consequent
drop in the production of new tillers (Dai and Weigert
1996), thus leading to a decrease in green biomass, a
rise in the tissue death rate (Figure 6), and a large
decrease in production (Figure 5).
Growth and Death Rates of Aerial Biomass. The increasing growth rate from the beginning of the analysis
until March 1997 (Figure 5) coincides with an increase
in new tiller emergence (Figure 2B) but not with a
density increase, indicating that during this period, tillers grow until they attain maximum biomass. A con-
Vicari et al., SPARTINA DENSIFLORA POPULATION DYNAMICS AND PRODUCTION
tinually increasing death rate between February and
December 1997 may be explained by the increasing
cutting rate by herbivores observed during this period
(Figure 6). It is worth mentioning that the non-destructive method used herein allowed us to study biomass
and its demographic processes independently of spatial
heterogeneity. By contrast to harvesting methods, nondestructive techniques made it possible to quantify
production of new biomass throughout the year. Although the low winter growth rates are difficult to
measure because of aerial biomass losses (leaves and
stems), they can be easily tracked through this method,
permitting an accurate assessment of biomass turnover
and a consistent NAPP estimation (Dai and Wiegert
1996). The harvest method applied by other authors
(Kirby and Gosselink 1976, Gallagher et al. 1980) led
to negative production values that have been considered as zero. Although low (close to 1 g·m22·day21),
our winter growth rates were always positive (Figure
5). The same seasonal pattern of growth rate variation,
with lower winter production, has been reported for
salt marshes in southwestern U.S. (Kaswadji et al.
1990, Morris and Haskin 1990).
Net Aerial Primary Productivity
The NAPP values obtained in this study are comparable to those of S. alterniflora in salt marshes of
the Southeastern U.S., assessed by the same method
(Gallagher et al. 1980, Reidenbaugh 1983, Houghton
1985). The high aerial productivity of these salt marshes probably results from the prolonged growing season. We observed that S. densiflora produces new biomass during the whole year, showing only a short period of decline in productivity during the summer (January–February), when the highest production rates are
attained. The falling growth rate detected in the middle
of the summer may be explained by an increased allocation of resources to belowground structures (Gallagher 1983). The study of the distinct demographic
attributes of populations of S. densiflora tillers allowed
us to detect year-to-year differences. Whereas seasonal
variation was evident during the first year, such variation was not observed in the following year. Diminished density and productivity, as well as increased
death rate, were related to unfavorable environmental
conditions, which were linked to the intensity of cutting by herbivores and to flood periods.
CONCLUSIONS
This research provided some insight regarding S.
densiflora tiller dynamics and production in salt
marshes in the Otamendi Natural Reserve. Although
tiller production occurs year-round, production rates
353
varied both seasonally and yearly (if seasons are compared).
The highest production rates were recorded in late
summer, whereas the lowest rates occurred in the winter of the first year. Tiller death rates were also variable, the periods with the highest death rates being
coincident with those with the highest birth rates. The
survival of tiller cohorts fluctuated on a seasonal basis.
This fact may be related to variations in the death rates
of the initial stages of growth. All cohorts, including
those tillers present at the beginning of the study (depletion curve), survived until the end of the observations, that is to say, more than 18 months. NAPP was
linked with new tiller production. The study of the
different demographic attributes of the population of
tillers of S. densiflora allowed us to detect fluctuations
in its behavior from year to year. The seasonal variation observed during the first year was not detected in
the second year.
ACKNOWLEDGMENTS
We thank Dr. Mark Brinson for his critical reading
of the manuscript. This investigation was supported by
the Administración de Parques Nacionales de la República Argentina. We also thank Mr. José Sercombe
for his collaboration in the field tasks and all the technical support staff of the Otamendi Natural Reserve.
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Manuscript received 4 January 2001; revisions received 26 September 2001 and 22 January 2002; accepted 25 February 2002.