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Reproductive traits in four spontaneous Pappophorum vaginatum populations in arid Argentina

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  • Comisión de Investigaciones Científicas (CIC) - Universidad Nacional del Sur

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Arid zones, where native rangelands are common, are essentials for millions of people livelihood. These areas support 50% of the world's livestock and are where 44% of the world's food is grown. In rangelands of Central Argentina, Pappophorum vaginatum is basically the unique, warm-season perennial grass species palatable to grazing livestock. Our major objective was to determine variability in reproductive characteristics among four spontaneous, overgrazed populations (i.e., P1, P2, P3, P4) of that species to identify promissory materials for domestication. Studies were conducted during three consecutive growing seasons within the southwestern part of the Phytogeographical Province of the Monte, in southwestern Buenos Aires, Argentina. Measured reproductive characteristics were related to flowering initiation, seed production and natural reseeding potential. Significant differences were found for flowering initiation and natural reseeding potential, but not for viable anthecia per plant among the four populations of P. vaginatum. This species fructified from the beginning to the end of the studied growing seasons with a great anthecia production per plant. The light weight of these anthecia and their awns would favor a great wind dispersal and most likely the establishment of new seedlings of P. vaginatum. This suggests that sexual reproduction might have a relatively greater importance than asexual reproduction (i.e., tillering) in the persistence of the overgrazed P. vaginatum in the plant communities of the studied region. Selection of plant materials with a late flowering initiation will allow to extend the forage production of a better quality. The variability among and within populations found on this study support the idea that would be promissory to start selection programs to obtain improved germplasm to reincorporate to grasslands of the south of the Phytogeographical Region of the Monte (Argentina) not only to increase livestock production but to recover and maintain biodiversity.
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Acta Oecologica 110 (2021) 103675
1146-609X/Published by Elsevier Masson SAS.
Reproductive traits in four spontaneous Pappophorum vaginatum
populations in arid Argentina
L. Entio
a
, M.M. Mujica
a
, C.A. Busso
b
,
*
, Y.A. Torres
c
a
Facultad Ciencias Agrarias y Forestales-UNLP, Argentina
b
Departamento de Agronomía CERZOS (Consejo Nacional de Investigaciones Cientícas y T´
ecnicas de La República Argentina), Universidad Nacional del Sur (UNS),
8000, Bahía Blanca, Argentina
c
Departamento de Agronomía UNS, Comisi´
on de Investigaciones Cientícas de La Provincia de Buenos Aires, Argentina
ARTICLE INFO
Keywords:
Developmental morphology stages
Argentina
Reproductive traits
Pappophorum vaginatum
ABSTRACT
Arid zones, where native rangelands are common, are essentials for millions of people livelihood. These areas
support 50% of the worlds livestock and are where 44% of the worlds food is grown. In rangelands of Central
Argentina, Pappophorum vaginatum is basically the unique, warm-season perennial grass species palatable to
grazing livestock. Our major objective was to determine variability in reproductive characteristics among four
spontaneous, overgrazed populations (i.e., P1, P2, P3, P4) of that species to identify promissory materials for
domestication. Studies were conducted during three consecutive growing seasons within the southwestern part of
the Phytogeographical Province of the Monte, in southwestern Buenos Aires, Argentina. Measured reproductive
characteristics were related to owering initiation, seed production and natural reseeding potential. Signicant
differences were found for owering initiation and natural reseeding potential, but not for viable anthecia per
plant among the four populations of P. vaginatum. This species fructied from the beginning to the end of the
studied growing seasons with a great anthecia production per plant. The light weight of these anthecia and their
awns would favor a great wind dispersal and most likely the establishment of new seedlings of P. vaginatum. This
suggests that sexual reproduction might have a relatively greater importance than asexual reproduction (i.e.,
tillering) in the persistence of the overgrazed P. vaginatum in the plant communities of the studied region. Se-
lection of plant materials with a late owering initiation will allow to extend the forage production of a better
quality. The variability among and within populations found on this study support the idea that would be
promissory to start selection programs to obtain improved germplasm to reincorporate to grasslands of the south
of the Phytogeographical Region of the Monte (Argentina) not only to increase livestock production but to
recover and maintain biodiversity.
1. Introduction
Grassland cover 40.5% of the total land surface of the world (White
et al., 2000) and has been lived in and use by people throughout human
history (Gibson, 2009). In arid zones, where native rangelands are
common, live approximately 2.5 billion people who depend on this
ecosystem services for their livelihoods (UN EMG, 2010). According to
Gaur and Squires (2018) these arid zones support 50% of the worlds
livestock where 44% of the worlds food is grown. The three greatest
threat to native grassland are agriculture, fragmentation and invasion of
non-native species (Gibson, 2009). Thus, it is crucial to optimize the use
of resources and knowledges, like those informed by Kassahun et al.
(2008), Smith et al. (2010a), T¨
alle et al. (2016), Dubeux Jr. et al. (2017),
Al- bukhari et al. (2018), Muir et al. (2018), Koncz et al. (2020), and
Belesky et al. (2020) in order to harmonize rangeland utilization and
biodiversity conservation.
Production of meat by livestock in 75% of continental Argentina,
characterized by arid and semi-arid zones, is based on grazing of native
vegetation (Busso et al., 2018). Thus, rangelands are important as a
production factor (because they are the main food source for animals)
and a biodiversity reservoir since they provide an ecological or envi-
ronmental service with the subsequent social-economical impact (Muj-
ica, 2010a, b).
Pappophorum Schreb is a grass genus native to the American
* Corresponding author.
E-mail address: cebusso@criba.edu.ar (C.A. Busso).
Contents lists available at ScienceDirect
Acta Oecologica
journal homepage: www.elsevier.com/locate/actoec
https://doi.org/10.1016/j.actao.2020.103675
Received 22 November 2019; Received in revised form 1 November 2020; Accepted 3 November 2020
Acta Oecologica 110 (2021) 103675
2
continent with 10 species, 7 of which live in arid and semiarid zones of
Argentina and boundary regions (Pensiero, 1986). It is considered
mainly autogamous because of the presence of cleistogamy (Campbell
et al., 1983; Pensiero, 1986). Rangelands of central Argentina are
characterized by the scarcity of warm-season, native perennial grasses,
palatable to livestock grazing (Busso et al., 2004). Within this region, at
the South of the Phytogeographical Province of the Monte, one impor-
tant species is Pappophorum vaginatum Buckley (Poaceae). This is basi-
cally the unique palatable perennial grass species during the
warm-season for grazing livestock (Giorgetti et al., 1997). This situa-
tion exposes P. vaginatum to overgrazing and is currently considered as a
decreasing species (Torres et al., 2013a). Within Argentina P. vaginatum
can be found not only in the Phytogeographical Region of the Monte but
also in those of the Pampas, Espinal and southeast of Chaco (Pensiero,
1986).
A valuable contribution for the recovery, maintenance and increase
of biodiversity is the domestication of native and naturalized species
with forage value, and the successful introductions (Mujica, 2010a, b).
In addition, establishment of improved forages, among other technolo-
gies, can substantially increase the stocking rate of semiarid areas in
Argentina (Garbulsky and Deregibus, 2004). Thus, much research has
focused on the study of introduced species adapted to semiarid condi-
tions since several decades (Ferri, 2014). However, the native germ-
plasm of the semiarid region of Argentina is of a special interest and
value in terms of genetic improvement. This is due to its evolutionary
history and adaptation to the climatic and edaphic constraints of such
region (Martin, 2005). Besides, several studies to a global scale have
reported that the native species are the most adequate for ecosystem
restoration in arid and semiarid regions (Waters and Shaw, 2003).
Nevertheless, such species must go through successive steps of evalua-
tion previous to their utilization (Tyler et al., 1987). This includes
studies from their characterization and initial evaluation either at the
greenhouse or at the eld as isolated plants to comparative yield and
grazing studies.
Studies of variability in characteristics of agronomic interest and
elucidation of the strategies of adaptation to biotic and abiotic distur-
bances on the native or naturalized species is of critical importance.
Genetic improvement should focus in combining the effects of natural
selection to the local environment with those coming from articial
selection on agronomic characteristics, specially those linked to the
control of transplanting and the production of forage and seeds (Mujica,
2010a, b). In this sense, various studies were made on native, perennial,
warm-season forage grasses. For example, some of these studies were
related to (1) elucidate strategies of competitive ability on P. vaginatum
(Torres et al., 2013a, b) and Trichloris crinita (Lag.) Parodi (Greco and
Cavagnaro, 2005); (2) study the phenotipic variation for various char-
acteristics of agronomic interest in populations of T. crinita (Kloster
et al., 2016), Setaria lachnea (Pensiero et al., 2011) and P. vaginatum
(Entio et al., 2014b, c), and (3) evaluate the genetic variability on
T. crinita (Cavagnaro et al., 2006). The strategic incorporation of forage,
native species was also studied to recuperate degraded areas (Quiroga
et al., 2009) and increase animal stocking rate (Passera et al., 1992).
More specically, the variability in seed germination and on char-
acteristics related to the initial seedling growth were studied in pop-
ulations of P. vaginatum (Entio et al., 2014b; Entio et al., 2014c).
Additional studies were made on reproductive characteristics on pop-
ulations of Setaria lachnea such as the variability in (1) germination, seed
weight and production, and cleistogamy (Pensiero et al.,1995), and
panicle emergence and fecundity (Pensiero et al., 2011); and (2) ower
phenology, number of panicles and percentage fructication (Exner
et al.,2010).
One important mechanism which contributes to plant species
persistence on rangelands is natural reseeding which depends on viable
seed contribution into the soil seed bank. This was proved at the eld
under grazing conditions; for example, with the variety Aguap´
e of Lotus
tenuis (Entio and Mujica, 2011). The soil seed bank can work as such as
long as the disseminules preserve their viability (Baker, 1989). In
addition, persistance of the soil seed bank is critical because it is a
reserve of accumulated genetic adaptability for the population over
which can act natural selection (Simpson et al., 1989). Perennial grasses
at the Monte form transient soil seed banks; however, such transience
appears to be little associated with losses due to germination (Marone
et al., 2003). The main factor of seed losses can be attributed to pre-
dation by granivores (Marone et al., 2000). Anyhow, Entio et al. (2014a)
suggested a positive effect of ants in the establishment of new seedlings
of P. vaginatum from seeds obtained from plants at the stage of seed
dispersal.
The hypothesis of this study is that there is variability in reproductive
characteristics important for domestication (i.e. owering initiation,
viable seed production, and potential of natural reseeding) among
spontaneous populations of P. vaginatum in the semiarid region of the
Province of Buenos Aires. This will allow to identify promissory mate-
rials with later owering initiation and greater viable seed production
and potential of natural reseeding to select in programs of genetic
improvement to use in grasslands restoration. In this way, an increase in
the abundance of P. vaginatum either by articial sowing, natural
reseeding or both, will be important not only to increase forage avail-
ability for livestock grazing but for the recovery and maintenance of
biodiversity. The objective of this study was to analize the variability of
various reproductive characteristics on four spontaneous native pop-
ulations of P. vaginatum within the semiarid region of the Buenos Aires
Province to identify promissory materials for domestication.
2. Materials and methods
2.1. Study site and sites of seed sampling
This study was conducted during the growing seasons (spring-sum-
mer-fall) of 2013/2014; 2014/2015 and 2015/2016 at the Chacra
Experimental Patagones, Ministry of Agrarian Affairs-Buenos Aires (40
39S; 6254W). A meteorological station located 5 m from the
experimental plots provided climate information during the duration of
the study (20132016) (Table 1).
A voucher/specimen was collected by Nicora, E.G. under the
collection number 6712 on December 29, 1959 in Caseros, Partido de
Daireaux, Buenos Aires, Argentina. It was deposited in the herbarium of
La Plata, Buenos Aires (Fernando O. Zuloaga, personal communication,
Instituto de Bot´
anica Darwinion, Pcia. Buenos Aires). This information is
crutial to ensure the species identication throughout time and the
testimony material of the experiment. Seeds of P. vaginatum were
sampled from four spontaneous populations (P1, P2, P3, P4) in
December 2012 covering the north (P1, P2), center (P3) and south (P4)
of the semiarid region of the Province of Buenos Aires (Fig. 1). Details of
the sampling sites are shown in Table 1.
2.2. Field study
On October 25, 2013, on the rst 2013/2014 growing season, 6
plants of each of 9 genotypes per population (i.e., 9 different plants/
population; pure lines; n =9) were transplanted to eld plots. There
were 0.5 m among each of 9 lines (i.e., 1 line/genotype) x 0.25 m among
each of 6 plants/genotype within each line. A completely randomized
block design using 2 blocks (within which there were 2 replicate plots/
population) was utilized. There was a total of 432 plants for all pop-
ulations [6 plants/genotype x 9 genotypes/population x 4 populations x
2 replicate plots/population]. Each replicate plot/population had 54
plants (i.e., 6 plants/genotype x 9 genotypes/population) (Fig. 2). Irri-
gation was initially applied until ooding each furrow at the beginning
of each month (December, January, February) during the rst summer
to secure plant survival.
L. Entio et al.
Acta Oecologica 110 (2021) 103675
3
2.2.1. Reproductive characteristics
During the studied period, several variables related to reproductive
characteristics were determined. They included determinations of the
(1) total number of reproductive tillers, (2) number of reproductive
tillers at different stages of developmental morphology (Fig. 3), (3)
number of anthecia/panicle/plant, (4) number of anthecia/plant, and
(5) panicle length. Potential reseeding was calculated as described in
Table 2. The number of viable anthecia was determined as a measure of
seed production and quality on all populations. This value was obtained
adjusting the number of anthecia per plant by the percentage of cumu-
lative germination (see Table 2). This latest value was obtained in a
germination study made in the laboratory as described below.
Table 1
Details of seed collecting sites of the studied spontaneous populations of P. vaginatum and climatic details at the experimental site (Patagones) during the study period.
Details Populations
P1 P2 P3 P4
Municipality Saavedra Adolfo Alsina Villarino Patagones
Coordinates 372651.2′′S 372137.6′′S 384932.4′′S 404025.86′′S 62543.06′′ W
62281.2′′W 622752.1′′ W 624313.2′′W
Precipitations (mm): 665.1 665.1 648.5 434.2
- Long-term mean annual 527
- mean annual during the
study
Temperatures (Max/Min)
(C):
14.9 (21.3/8) 14.9 (21.3/8) 15.4 (22.8/9) 14.1 (20.9/7.4)
- Long-term mean annual 14.3 (21.1/7.4)
- mean annual during the
study
Long-term Max/Min
absolute temperature (C)
42.5/12 42.5/12 43.8/11.8 42.1/8.6
Relative humidity (%): 66.25 66.25 63.7 65.5
- Long-term mean annual 68.3
- mean annual during the
study
Typical relief steppe with an
herbaceous stratum
cover
steppe with an
herbaceous stratum cover
undulated steppe with sandy hills, herbaceous
stratum cover and secondary shrub communities
steppe with an open shrub stratum
and a herbaceous stratum
Long-term data: INTA Informa, 2013; Servicio Meteorol´
ogico Nacional (SMN), and Ministerio de Agroindustrias (provincia de Buenos Aires) (MA-BA), 2016.
Data at the experimental site: Ministerio de Agroindustrias (provincia de Buenos Aires) (MA-BA), 2016.
Fig. 1. Geographic location of the seed collecting sites of the studied spontaneous populations of P. vaginatum (June 2020, Google Earth Pro, 7.January 3, 4507).
L. Entio et al.
Acta Oecologica 110 (2021) 103675
4
2.2.2. Plant morphology and survival characteristics
2.2.2.1. Basal area. Plant total crown diameter was measured at a plant
scale to determine total plant basal area. These measurements were
conducted at the sampling dates as detailed in Table 2.
2.2.2.2. Plant survival. The success of transplanting was determined as
the mean percentage of alive plants per plot at the end of the study (i.e.,
in 2016) with respect to the initial number of plants per plot (i.e., in
2013).
2.3. Laboratory study
This experiment was conducted in September 2016 with the seeds
harvested on January 5, 2016 from the cultivated plants. It had a
completely randomized experimental design (n =6) and the experi-
mental unit was a Petri dish (9 cm diameter) with 50 anthecia. Such
anthecia were placed with their covers (lemma and palea) on wet lter
paper to obtain their germination. The lter paper was maintained wet
during the whole study. After 24 h of imbibition, the number of
germinated anthecia (radicle 3 mm) was determined every 24 h
during the study duration. The study nished after four consecutive days
without germination (from day 1822 from imbibition). We determined
the percentage of cumulative germination. Temperature was deter-
mined with a digital thermometer (ThermoMeter TA318). The mean
maximum and minimum temperatures ±1 standard error during the
study in the laboratory were from 22.9 C ±0.4420.1 C ±0.44,
respectively. Such temperatures were within the range of mean monthly
air temperatures measured close to the eld plots during the reproduc-
tive stage of P. vaginatum (data not shown). In addition, a potential
reseeding value was calculated. This value was obtained after adjusting
the number of viable anthecia per plant by the percentage of cumulative
seedling emergence (this latest value was taken from a previous study
under controlled conditions: means =P1: 38%; P2: 52%; P3: 65.5%; P4:
48%; Entio, 2019).
Sampling dates and timing during each growing season, the pre-
dominant developmental morphology stage at each sampling date, and
all reproductive, morphological and plant survival characteristics
determined at each date of sampling are described in Table 2.
2.4. Statistical analyses
The experimental design of the eld studies allowed application of
nested ANOVA (genotypes nested in populations) in a split-plot design
(being the populations the large plot, and the genotypes the subplot)
which allowed to compare most of the variables among populations.
One-way ANOVAs were also used to compare the variables among
populations in the studies under controlled conditions.
When F tests were signicant, mean comparisons were made using
the Tukey test with a signicance level of 0.05. Several variables were
transformed on the eld studies (see details in Table 1) to comply with
the assumptions of normality and homocedasticity of variance (Sokal
and Rohlf, 1984). Non-transformed values are presented in Tables.
All statistical analyses were made using the program Statistica 7.1
(StatSoft, Inc, 2005).
3. Results
3.1. Field study
3.1.1. Reproductive characteristics
On December 10, 2013, late spring of the rst 2013/2014 growing
season, there were signicant differences (p<0.001; P1>P3>P2>P4;
Table 3) among the populations in the total number of reproductive
tillers per plant. There were also signicant differences (p <0.001)
among populations in the number of reproductive tillers per plant (1)
Stage 1 (boot stage; P1>P3>P2>P4; Table 3); (2) Stage 2 (<of 50% of
exposed panicles), values on P1 were greater (p 0.05) than those in the
Fig. 2. Details of the experimental design of the eld essay carried out at the Chacra Experimental Patagones. The distribution of plants within each of the four
randomized plots (P1 to P4) per block is shown. Within each plot there were 9 lines or genotypes and 6 plants per line or genotype (54 plants per plot). A zone of 1 m
around de plots were periodically weeded to avoid radical competence from other plants.
L. Entio et al.
Acta Oecologica 110 (2021) 103675
5
remaining populations, which did not differ (p >0.05) among them
(Table 3); (3) Stage 3 (>of 50% of exposed panicles; p =0,005; Table 3).
Population 1 was signicantly different (p 0,05) to P4. In addition, P2
and P3 did not have signicant differences (p >0.05) to P4 (Table 3).
However, there were no signicant differences (p =0.5) among pop-
ulations in the number of reproductive tillers at Stage 4 (100% of
exposed, immature panicle) (Table 3). Finally, there were signicant
differences (p =0.007) among populations in the number of reproduc-
tive tillers Stage 5 (100% of exposed, mature panicles) per plant. Pop-
ulation 1 was at least 30.4% greater (p 0,05) than the other
populations, which did not differ signicantly (p >0.05) among them
(Table 3). Signicant intrapopulation differences (p 0.05) were
detected for the total number of reproductive tillers per plant (P2) and
for the number of reproductive tillers at Stage 1 (P1) and 3 (P2), and at
Stage 4 (P1, P2).
On February 11, 2014, mid-summer of the 2013/2014 growing
season, there were signicant differences (p =0,002) among the pop-
ulations in the total number of reproductive tillers per plant. P1 were
greater (p 0.05) than those in the remaining populations, which did
not differ (p >0.05) among them (Table 3). For this variable, signicant
intrapopulations differences (p 0,05) were detected in P2.
On November 5, 2014, mid-spring of the second 2014/2015 growing
season, there were not signicant differences (p =0,063) among pop-
ulations in the number of reproductive tillers Stage 1 (boot stage) per
plant (Table 3). There were signicant differences (p <0.001) among
populations for the set of reproductive tillers per plant of Stages from 2
to 5 (Table 3). Thus, P1 was greater than (p 0.05) the remaining
populations. Population 4 was greater than (p 0.05) P2 and P3
(Table 3). In addition, P2 and P3 were not signicantly different (p >
0.05, Table 3). Finally, there were not signicant differences (p =0.186)
among populations in the total number of reproductive tillers per plant
(Table 3). Signicant intrapopulation differences (p 0.05) were
detected for the total number of reproductive tillers per plant (P2) and
for the number of reproductive tillers at Stage 1 (P2, P4).
At the initiation of fructication (December 16, 2014: beginning of
fructication during the second 2014/2015 growing season): (1) There
were not signicant differences (p =0.287) among populations in the
total number of reproductive tillers per plant (Table 3). (2) Populations
differ signicantly (p <0,001) in the length of mature panicle per plant
(Table 3). Thus, P1 was shorter (p 0.05) than the remaining pop-
ulations which were similar (p >0.05) among them (Table 3). (3)
Populations showed signicant differences (p <0.001) in the number of
anthecia per panicle on a plant basis (Table 3). This was because of P3
and P4 were similar (p >0.05) between them, but greater than (p
0.05) P1 and P2; at the same time, P2 was greater (p 0.05) than P1
(Table 3). (4) Finally, populations did not differ (p =0.295) in the
number of anthecia per plant (Table 3). Signicant intrapopulation
differences (p 0.05) were detected for the total number of reproduc-
tive tiller per plant (P2, P3, P4), anthecia per panicle on a plant basis
(P1, P2, P3, P4), and for the number of anthecia per plant (P2).
On January 05, 2016, early summer of the third 2015/2016 growing
season, there were signicant differences (p 0.05) among populations
(1) on the total number of reproductive tillers per plant (Table 3). Thus,
P4 was lower (p 0.05) than the remaining populations which were
similar (p >0.05) among them (Table 3); (2) in the number of repro-
ductive tillers Stage 5 per plant (Table 3). As a result, P1 and P2 were
similar (p >0.05) between them, but greater (p 0.05) than P3 and P4
(Table 3). In addition, P3 and P4 were similar (p >0.05) between them
(Table 3); (3) in the number of reproductive tillers Stage 4 per plant
(Table 3). Thus, P3 was greater (p 0.05) than the remaining pop-
ulations; P1 showed intermediate values, and P2 and P4 were lower (p
0.05) than the remaining populations, and similar (p >0.05) between
them (Table 3). Signicant intrapopulation differences (p 0.05) were
detected for the total number of reproductive tiller per plant (P2), and
number of reproductive tiller at Stage 4 and 5 (P1, P2, P3, P4 and P3, P4,
respectively).
Also, in the rst week of January 2016, there were signicant dif-
ferences (p <0.001) among populations in the panicle length per plant
(Table 3). Thus, while P3 and P1 showed the greatest (p 0.05) and
lowest (p 0.05) values, respectively, P2 and P4 were similar (p >0.05)
between them (Table 3). At this time, populations also differed (p <
0.001) in the number of anthecia per panicle per plant (Table 3). While
P2 and P4 were similar (p >0.05) between them, P3 and P1 showed the
greatest (p 0.05) and lowest (p 0.05) values, respectively (Table 3).
At the same time, there were not signicant differences among pop-
ulations neither in the number of anthecia per plant (p =0.075: Table 3)
nor in the number of viable anthecia per plant (p =0.56; Table 3).
Signicant intrapopulation differences (p 0.05) were detected for the
panicle length (P1, P4), anthecia per panicle on a plant basis (P2, P3,
P4), number of anthecia per plant, and number of viable anthecia per
plant (P2, P4).
Regarding to the number of potential seedlings for natural reseeding
per m
2
, there were signicant differences (p =0.005) among pop-
ulations (Table 3). Population 3 showed the greatest (p 0.05) value, P2
was greater (p 0.05) than P1 and P4 which resulted similar (p >0,05)
between them.
3.1.2. Plant morphology and survival characteristics
3.1.2.1. Basal area. Measurements on the third (September 17, 2014)
and fourth (November 05, 2014) sampling dates, on the second 2014/
2015 growing season, did not indicate signicant differences (p >0.05)
in basal area (mean ±1 E.E.: September 17, 2014 =11.5 ±0.7 cm
2
;
November 05, 2014 =18.4 ±1.1 cm
2
) among populations (Table. 3).
Fig. 3. Details of reproductive tillers at different stages of developmental
morphology in an individual of P. vaginatum.
L. Entio et al.
Acta Oecologica 110 (2021) 103675
6
3.1.2.2. Plant survival. Survival values were high and similar (>95%; p
>0.05; data not shown) among populations on 17 September and 05
November of 2014, on the second 2014/2015 growing season. At the
end of the study in 2016, on the third 2015/2016 growing season, once
again there were no signicant differences (p >0.05) among pop-
ulations in the number of established individuals (Table 3).
3.2. Laboratory study
Results of the germination study made with the seeds harvested on
Jan 5, 2016 showed signicant differences (p 0.05) among pop-
ulations in the percentage of cumulative germination. Population 1
showed a higher (p 0,05) cumulative germination percentage than P2,
P2 was similar (p >0.05) to P3 and P4 (Table 3).
4. Discussion
4.1. Field study
A few weeks before a year from transplanting (i.e., on September 17,
2014: time of the 2014/2015 growing season initiation), all populations
showed high (>95%) and similar (p >0.05) survival values. This would
indicate that the four studied populations would have a similar, high
plant establishment potential under eld conditions. However, we need
to point out that irrigation was applied up to ooding each groove at the
beginning of each month (December 2013, January and February 2014:
late spring and early summer, respectively, of the 2013/2014 growing
season) during the rst summer after transplanting to secure its success.
On Nov 05, 2014, mid-spring of the 2014/2015 growing season, plant
survival was also >95% which conrmed the high and uniform plant
establishment of the studied native species. Torres et al. (2013b) also
determined survival values of 94% (May 2007) and 92.5% (May 2008)
Table 2
Details of the sampling dates and study variables.
Sampling date (Number) Predominant developmental
morphology
Abbreviation Study variable [transformation for statistical analysis]
Timing of each study growing
season
stage
December 10, 2013 (1) Boot stage RTS1 number of Reproductive Tillers Stage 1 per plant (boot stage) number of Reproductive
Tillers Stage 2 per plant (<50% of emerged panicle) [ln (x+0.5)]
RTS2 number of Reproductive Tillers Stage 3 per plant (>50% of emerged panicle) [ln (x+0.5)]
RTS3 number of Reproductive Tillers Stage 4 per plant (immature emerged panicle) [ln
(x+0.5)] number of Reproductive Tillers Stage 5 per plant (mature emerged panicle) [ln
(x+0.5)] the number of Total Reproductive Tillers was calculated per plant
(S1+S2+S3+S4+S5) [(x)]
RTS4
RTS5
Late spring of the rst growing
season (2013/2014)
TRT
February 11, 2014 (2) Mid-summer
of the 2013/2014 growing
season
Seed dispersal mature grain RTS5 see previous description
17 Sept 2014 (3) Early spring of the
2014/2015 growing season
Vegetative growth initiation
(end of winter dormancy)
Bd the Basal diameter was measured per plant (cm)
Nov 5, 2014 (4) Mid-spring of the
2014/2015 growing season
Boot Stage Bd see previous description.
RTS1 see previous description
RTS2-5 the number of Reproductive Tillers S2 to S5 was counted per plant
TRT the Total number of Reproductive Tillers was counted per plant (RTS1+RTS2 to 5)
December 16, 2014 (5) Late spring
of the 2014/2015 growing
season
boot stage; immature grain;
mature grain
TRT AP see previous description [(x)]
PL the number of Anthecia per Panicle per plant (average
APl of 2 panicles per plant) [ln (x+0.5)]
the Panicle Length (cm) was determined per plant (average of 5 panicles per plant)
the number of Anthecia per Plant was calculated (TRT x AP)
Jan 5, 2016 (6) Early summer of the
2015/2016 growing season
Immature grain; mature grain;
seed dispersal
RTS4 see previous description [(x+0.5)]
RTS5 see previous description [(x)]
TRT the Total number of Reproductive Tillers per plant was
AP calculated (S1+S2+S3+S4+S5) [(x)]
PL APl VAPl see previous description [(x+0.5)]
PR see previous description [(x)]
CG see previous description [(x)] the number of Viable Anthecia per Plant was calculated:
APl adjusted by the cumulative germination percentage obtained from a laboratory study
conducted after plant harvesting [(x)] (Entio, 2019) Potential Reseeding per m
2
was
calculated: value VAPl Adjusted by the percentage of cumulative emergence obtained
from a previous study under controlled conditions [(x)] (Entio, 2019)
the percentage of Cumulative Germination
was determined
June 6, 2016 (7) Late fall of the
2015/2016 growing season
Survival the percentage of alive plants was calculated
at the end of the study period
L. Entio et al.
Acta Oecologica 110 (2021) 103675
7
after 1
½
and 2
½
years from transplanting on P. vaginatum within an
exclosure.
By mid September 2014, at the initiation of the 2014/2015 growing
season, plant basal diameter (range =3.713.98 cm), and thus basal
area (range =10.8112.44 cm
2
), were also similar (p >0.05) among
populations. Torres et al. (2013b) reported greater values of basal area
[from 27 (May 2006) to 42 cm
2
(May 2007)] on undefoliated plants of
P. vaginatum growing within an exclosure to domestic herbivory at the
end of their studied growing seasons.
Taking into account the production of total reproductive tillers as an
indicator of initial growth after transplanting [sampling dates (1)
December 10, 2013, and (2) February 11, 2014: late spring and mid-
summer, respectively, of the 2013/2014 growing season], P1 was su-
perior (p 0.05) to the remaining populations (Table 3). In addition,
observing the results obtained on December 10, 2013 it might be that P1
would initiate owering earlier than P2, P3 and P4 because it presented
47.7% more total reproductive tillers early in the reproductive cycle
than the average of the other populations (Tabe 3). Even more, it pre-
sented at least three times more reproductive tillers of Stage 5 (100% of
mature emerged panicle) than the other populations (Table 3).
On December 10, 2013 (late spring of the 2013/2014 growing sea-
son), reproductive tillers of Stage 1 (boot stage) were dominant in all
populations (86.7%, 88.9%, 89.9% and 92.1% from the total repro-
ductive tillers per plant on P1, P2, P3 and P4, respectively). On February
11, 2014 (mid-summer of the 2013/2014 growing season), only repro-
ductive tillers of Stage 5 (100% mature emerged panicle) were observed.
Gil B´
aez et al. (2015) also found signicant differences among
populations of Trichloris crinita in the Monte region taking into account
the number of reproductive tillers per plant (100% mature emerged
panicle) as an indicator of initial growth during the rst reproductive
cycle after the transplanting.
At the beginning of November 2014 (mid-spring of the 2014/2015
growing season), populations did not show differences (p >0,05) in the
number of total reproductive tillers (Table 3). Also, P1 was on average
70% greater (p 0.05) than the other populations in the number of
reproductive tillers S2S5 (Table 2). This result, similarly to that ob-
tained on December 10, 2013, highlighted that P1 was the earliest
population in initiating owering. This was because of P1 had a greater
number of mature reproductive tillers per plant than the other pop-
ulations at the initiation of the reproductive cycle. Exner et al. (2010)
also reported differences in owering initiation among different pop-
ulations of Setaria lachnea. Initiation of the reproductive cycle is an
important variable to take into account in selection programs on forage
species (Allard, 1999). Selection of plant materials with a late owering
period would allow to extend the forage production of a better quality,
because the initiation of owering is associated with a reduction of
forage quality (Pontes et al., 2007). We emphasize that high values of
heredability, and thus a great response to selection, are expected for this
developmental morphology stage (i.e., initiation of owering) in grasses
and other, various families (Weis and Kossler, 2004).
It is critical to take into account seed production on forage species
not only for selected-germplasm seed multiplication but for its subse-
quent natural dispersion. At the same time, seed production of any given
species can also be very important for the persistance of that species via
Table 3
Characteristics evaluated (mean ±SE) during the three-year study on four spontaneous population of P. vaginatum. Different small cap letter within each characteristic
indicate signicant differences (p 0.05) among populations. The test of Tukey was used for mean comparisons.
Character (sampling n) Populations
P1 P2 P3 P4
TRT (1) 15.78 ±0.98 a 10.58 ±0.78 c 13.03 ±0.88 b 8.44 ±0.7 d
RTS1 (1) 13.68 ±0.82 a 9.51 ±0.74 c 12 ±0.78 b 7.5 ±0.68 d
RTS2 (1) 1.06 ±0.2 a 0.49 ±0.14 b 0.44 ±0.14 b 0.54 ±0.28 b
RTS3 (1) 0.64 ±0.2 a 0.38 ±0.14 ab 0.34 ±0.12 ab 0.18 ±0.08 b
RTS4 (1) 0.24 ±0.09 a 0.19 ±0.08 a 0.21 ±0.08 a 0.15 ±0.07 a
RTS5 (1) 0.15 ±0.06 a 0 b 0.03 ±0.02 b 0.05 ±0.04 b
RTS5 (2) 4.63 ±0.64 a 3.4 ±0.6 b 3.34 ±0.5 b 2.8 ±0.48 b
Bd (3) 3.71 ±0.2 a 3.68 ±0.22 a 3.91 ±0.24 a 3.98 ±0.22 a
Bd (4) 5.07 ±0.26 a 4.66 ±0.28 a 4.93 ±0.24 a 4.78 ±0.28 a
TRT (4) 8.75 ±0.7 a 7.24 ±0.62 a 8.17 ±0.64 a 8.08 ±0.64 a
RTS1 (4) 4.66 ±0.46 a 5.26 ±0.56 a 5.89 ±0.54 a 4.96 ±0.52 a
RTS2-5 (4) 4.08 ±0.46 a 1.98 ±0.34 c 2.28 ±0.36 c 3.12 ±0.46 b
TRT (5) 16.83 ±1.5 a 16.72 ±1.63 a 14.42 ±1.4 a 14.45 ±1.5 a
PL (5) 8.86 ±0.22 b 10 ±0.74 a 10.61 ±0.32 a 10.8 ±0.38 a
AP (5) 44.59 ±2.6 c 57.07 ±3.2 b 71.37 ±4.44 a 64.76 ±4.18 a
APl (5) 789.98 ±94.32 a 997 ±126.2 a 1087.9 ±145.4 a 967.85 ±124.6 a
TRT (6) 32.03 ±1.56 a 30.76 ±1.42 a 29.87 ±1.32 a 22.15 ±1.56 b
RTS4 (6) 10.45 ±1.56 b 7.37 ±1.48 c 13.43 ±1.62 a 6.34 ±1.06 c
RTS5 (6) 21.58 ±1.66 a 23.61 ±1.88 a 16.8 ±1.64 b 16.11 ±1.36 b
PL (6) 9.95 ±0.3 c 10.85 ±0.28 b 11.84 ±0.36 a 10.98 ±0.3 b
AP (6) 55.94 ±3.28 c 69.04 ±3.82 b 85.43 ±5.3 a 74.91 ±4.8 b
APl (6) 1890.76 ±214.28 a 2248.42 ±259 a 2672.3 ±184.68 a 1726.9 ±177.22 a
CG (6) 68.33 ±8.14 a 57.33 ±6.58 b 54 ±5.46 ab 64.66 ±5.98 ab
VAPl (6) 1291.95 ±146.42 a 1289 ±148.48 a 1443.04 ±153.7 a 1116.61 ±114.6 a
PR (6) 3954 ±448.16 c 5486 ±631.94 b 7647 ±822.76 a 4311 ±444.72 c
Survival (7) 96.29 ±5.74 a 95.37 ±5.9 a 96.29 ±4.3 a 96.29 ±3.36 a
RTS1: number of Reproductive Tillers Stage 1 per plant (boot stage); RTS2: number of Reproductive Tillers Stage 2 per plant (<50% of emerged panicle); RTS3:
number of Reproductive Tillers Stage 3 per plant (>50% of emerged panicle); RTS4: number of Reproductive Tillers Stage 4 per plant (inmature emerged panicle);
RTS5: number of Reproductive Tillers Stage 5 per plant (mature emerged panicle); TRT: number of Total Reproductive Tillers was calculated per plant
(S1+S2+S3+S4+S5); Bd: the Basal diameter was measured per plant (cm); RTS2-5: the number of Reproductive Tillers S2 to S5 was counted per plant; TRT: Total
number of Reproductive Tillers was counted per plant (RTS1+RTS2 to 5); AP: number of Anthecia per Panicle per plant; PL: Panicle Length (cm) was determined per
plant; APl: number of Anthecia per Plant was calculated (TRT x AP); VAPl: number of Viable Anthecia per Plant; PR: Potential Reseeding per m
2
; Survival: the
percentage of alive plants at the end of the study period.
(1): Late spring of the 2013/2014 growing season; (2): Mid-summer of the 2013/2014 growing season; (3): Early spring of the 2014/2015 growing season; (4): Mid-
spring of the 2014/2015 growing season; (5): Late spring of the 2014/2015 growing season; (6): Early summer of the 2015/2016 growing season; (7): Late fall of the
2015/2016 growing season.
L. Entio et al.
Acta Oecologica 110 (2021) 103675
8
natural reseeding in environments exposed to various product produc-
tion (e.g., meat, milk, wool, etc.) (Entio and Mujica, 2011). Most of the
measured variables on December 16, 2014 and January 05, 2016 (late
spring and early summer of the 2014/2015 and 2015/2016 growing
seasons, respectively) showed the existence of inter and intra population
variability. The sampling on December 16, 2014 was made during the
rst third of the fructication developmental morphology stage of
development in the 2014/2015 growing season. Although the number of
total reproductive tillers (range: 14.416.8) did not show signicant
differences (p >0.05) among populations (Table 3), P1 showed a higher
value than the remaining populations. This shows once again the ten-
dency of P1 to a greater precocity for initiating the reproductive cycle,
with possible implications with regard to forage quality as it was pre-
viously discussed (Pontes et al., 2007). Torres et al. (2013a) reported a
maximum average value of 18 reproductive tillers per plant by mid
December 2006 on undefoliated genotypes of P. vaginatum at the same
study site than ours. Precipitation during their warm-season growing
cycle 2006/2007 (i.e., from October 2006 to May 2007) was 276.4 mm.
On the other hand, despite P1 had a lower (p 0.05) panicle length and
number of anthecia per panicle than the other populations (Table 3), its
production of anthecia per plant was similar (p >0.05) to that on the
remaining populations. This was because P1 showed the greatest num-
ber of reproductive tillers among all four populations (e.g., Table 3).
Measurements on Jan 05, 2016 (early summer of the 2015/2016
growing season) were conducted in the third reproductive cycle from
plant establishment, and at this time plants were in the fructication
stage of developmental morphology. The number of total reproductive
tillers per plant varied between 22 and 32 depending on the population,
and its average was about 80% greater than the average on December
16, 2014 (late spring of the 2014/2015 growing season). Populations 1
and 2 were among the populations with a greater number of total
reproductive tillers per plant; in addition, they were the two populations
with the greatest (p 0.05) number of reproductive tillers Stage 5 per
plant (Table 3). This suggested an earliest initiation of the reproductive
cycle on P1 and P2 than on P3 and P4. Cavagnaro et al. (2006) and Gil
B´
aez et al. (2015) also reported variability on the number of reproduc-
tive tillers per plant between populations of Trichloris crinita. Exner et al.
(2010) also showed variability in such parameter between populations
of Setaria lachnea. On the other hand, P1 was smaller (p 0.05) than the
other populations for panicle length and number of anthecia per panicle
per plant (Table 3). Despite this, its per plant anthecia production was
similar (p >0.05) to that on the other populations (Table 3) because of
its hight reproductive tiller production (Table 3). In this study, mean
panicle length was 10 and 10.9 cm on December 16, 2014 (late spring of
the 2014/2015 growing season) and January 05, 2016 (early summer of
the 2015/2016 growing season), respectively. However, Smith (2010)
and Smith et al. (2010b) reported mean values around 18.520 cm for a
selected material of P. vaginatum. Other studies also reported variability
among populations for various reproductive variables on warm-season
perennial grasses: for (A) owering initiation (Exner et al., 2010);
extension of the period of panicle emergence (Exner et al., 2010; Pen-
siero et al., 2011); percentage of fructication (Exner et al., 2010;
Pensiero et al., 2011); degree of cleistogamy (Pensiero et al., 2011), and
germination responses (Pensiero et al., 2011; 2011) on Setaria lachnea;
and (B) panicle length on Panicum virgatum (Price and Casler, 2014).
With the anthecia harvested on Jan 05, 2016 (early summer of the
2015/2016 growing season), a germination study was conducted. In this
study, cumulative germination varied between 54 and 67% among
populations. Thereafter, there was not variability (p >0.05) among
populations for the number of viable anthecia per plant (range:
11161443), although P3 showed higher values. The mean precipitation
of the study years was 39% greater than the long-term mean annual
precipitation (19812016: 434.2 mm). In addition, it did occur within a
period of humid years (20102016) for the region which mean annual
precipitation (522.6 mm) was greater than 20% of the long-term mean
annual precipitation. Pappophorum spp. Produces twice as much seeds in
humid than in dry years (Pol et al., 2010). However, Pol et al. (2010)
also reported that among seven warm-season perennial grass species,
Trichloris crinita was the only one that signicantly produced more seed
in a dry than in a humid year in the region of the Central Monte in
Argentina.
The number of established individuals per unit surface area was of 8
plants/m
2
, and it did not vary signicantly for any of the populations
until the end of the studied period. Population 3 showed the greatest (p
0.05) potential of natural reseeding with at least 28.3% more seed-
lings in the next generation than the other three populations (Table 3).
This greater potential of natural reseeding on P3, could be associated to
its high values of viable anthecia production per plant (Table 3) and
cumulative emergence (Entio, 2019). Anyhow, all studied populations
of P. vaginatum might achieve a high potential of natural reseeding
considering that the number of potentials seedlings in the next genera-
tion per m
2
was at least almost 500 times greater than the individuals
implanted at the beginign of the study per m
2
(Table 3). Yang et al.
(1988) indicated that the establishment efciencies as a result of natural
reseeding of Dactylis glomerata varied between 0.96 and 5.32% under
different grazing systems. Assuming for P. vaginatum an intermediate
efciency of 3.14%, according our study it might be expected a mini-
mum of 325, 324, 359, and 280 established potential seedlings per m
2
for P1, P2, P3, and P4, respectively.
The results obtained in this study, even taken into account that are
potential values of reseeding, would allow to suppose that sexual
reproduction is critical to explain such a long-term persistance of
P. vaginatum in the rangelands of central Argentina. Asexual reproduc-
tion (tiller production from axillary buds) is the main way of repro-
duction in the rangeland perennial grasses according to Briske and
Richards (1995). However, and in agreement with the results of this
study, Torres et al. (2013a) demonstrated that plants of P. vaginatum
produce abundant anthecia during its growing cycle. These anthecia
plus their awns can have a very good wind dispersal because of their
small size (anthecium =1.53.5 mm +awns: 69 mm: Rúgolo de
Agrasar et al., 2005; Entio, 2019). As a result, Torres et al. (2013a)
proposed that the most relevant form of reproduction (either sexual or
asexual) should be explored in P. vaginatum to explain its wide distri-
bution and persistence to long-term disturbances (i.e., mostly herbivory)
in arid and semiarid zones of central Argentina. An early and high seed
production in P. vaginatum populations would imply a great seed
dispersal that could germinate and establish in appropriate microsites.
Since the studied populations can produce up to around 1400 viable
anthecia per plant (Table 3), it is likely that sexual reproduction has a
relatively greater role than that asexual (i.e., daughter tiller production
per plant) in determining the persistence of P. vaginatum in a region
where grazing, drought and wildres are frequent disturbances (Pel´
aez
et al., 2001; Flemmer et al., 2003). Our results in P. vaginatum thus differ
from the report of Briske and Richards (1995), and they could be
specially true where wild res kill a greater proportion of undesirable
than desirable grasses (Boo et al., 1996), thus leaving potential micro-
sites for the establishment of new plants of P. vaginatum.
Research results showed interpopulation variability for several of the
reproductive characteristics during the years of study, although some of
them also showed intrapopulation variability. This is expected in
autogamous species (Jain, 1976; Loveless and Hamrick, 1984; Ram-
akrishnan et al., 2004) such in Pappophorum spp. because of the presence
of cleistogamy (Campbell et al., 1983; Pensiero, 1986). Further research
will determine if the variation among populations is higher than ex-
pected by drift alone or by distance following a test proposed by Ovas-
kainen et al. (2016).
Finally, this warm-season specie, with high palatability, considered
as decreasingdue to overgrazing and adapted to local environmental
conditions, not only presents a high production of viable anthecia and
natural reseeding potential but presents differences in owering initia-
tion. Selection of plant materials with a late owering initiation will
allow to extend the forage production of a better quality. The variability
L. Entio et al.
Acta Oecologica 110 (2021) 103675
9
among and within populations found on this study support the idea that
would be promissory to start selection programs in order to obtain
improved germplasm suitable to increase livestock production and to
recover and maintain biodiversity in grasslands of the south of the
Phytogeographical Region of the Monte (Argentina).
Author contributions
Author contributions LE and MM conceived and designed the study.
LE and MM performed the study. LE analyzed the data. LE wrote the
manuscript in Spanish and CAB wrote it in English. LE was in charge of
all paper revisions. CAB made all editorial work from the time the
manuscript was submitted to Acta Oecologica until it was nally pub-
lished. All authors approved the nal version. YAT contributed to make
the statistical analysis.
Declaration of competing interest
The authors declare that they have no known competing nancial
interests or personal relationships that could have appeared to inuence
the work reported in this paper.
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