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Journal of Arid Environments 74 (2010) 167172

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Journal of Arid Environments

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Inuences of interyear rainfall variability and microhabitat on the germinable seed bank of annual plants in a sandy Monte Desert
L. Quevedo-Robledo a, b, E. Pucheta b, c, *, Y. Ribas-Fernandez a, b
a

Fellowship from Consejo Nacional de Investigaciones Cientcas y Tecnicas (CONICET), Argentina Departamento de Biologa, Facultad de Ciencias Exactas, Fsicas y Naturales, Universidad Nacional de San Juan, Av. Ignacio de la Roza 590 (O) J5402DCS Rivadavia, San Juan, Argentina c IMBIV-CONICET and Universidad Nacional de Cordoba, CC 495, 5000 Cordoba, Argentina
b

a r t i c l e i n f o
Article history: Received 11 October 2008 Received in revised form 10 March 2009 Accepted 4 August 2009 Available online 2 September 2009 Keywords: Arid ecosystems Growing-season rainfall Seed density Spatial patches Summer annuals

a b s t r a c t
We addressed the effects of growing-season rainfall of two consecutive years and of two microhabitats on seed density and oristic composition of the germinable seed bank of annual plants in a sandy desert. We hypothesised that seed composition and density is affected by the presence of vegetated patches, but that this effect varies according to rainfall. We predict an overall lower soil-seed density with higher values under shrubs after a dry growing season. We found signicant effects of interyear variability and microhabitat on the germinable soil seed bank of annual plants. Twice as many germinable seeds were present in soil after the rainy summer than after the drier summer. Moreover, seed density under shrubs was 1.3 times greater than on bare ground. Although we found no statistic interaction between factors affecting the germinable soil seed density, the relative amount of germinable seeds under shrubs increased after a drier growing season. Species composition showed non-additive effects for the interaction of precedent growing-season rainfall and microhabitat, resulting in four species-assemblages. Altogether, our ndings suggest that shrub patches and rainfall events of the precedent growing season may affect the abundance and identity of ephemeral and annual plant species in the germinable seed bank. 2009 Elsevier Ltd. All rights reserved.

1. Introduction Seed banks play an important role maintaining the dynamics and regeneration of plant communities (Harper, 1977; Skoglund, 1992). They are a crucial component in desert ecosystems and other stressful habitats where favourable conditions for seed germination and seedling establishment are quiet unpredictable both in space and time (Kemp, 1989; Nathan and Muller-Landau, 2003; Meyer and Pendleton, 2005). Annual plants account for a large proportion of total seed density in desert seed banks (Marone and Horno,1997; Bertiller,1998; Guo et al., 1999; Marone et al., 2000; Gutierrez and Meserve, 2003; Figueroa et al., 2004). Seed banks of annual plants may uctuate at hierarchized temporal and spatial scales due to interyear rainfall variability and landscape organization (Pake and Venable, 1996; Ludwig et al., 1999; Caballero et al., 2008a). These features have been

* Corresponding author. Departamento de Biologa, Facultad de Ciencias Exactas, Fsicas y Naturales, Universidad Nacional de San Juan, Av. Ignacio de la Roza 590 (O) J5402DCS Rivadavia, San Juan, Argentina. Tel.: 54 3543441974. E-mail addresses: epucheta@unsj-cuim.edu.ar, edu.pucheta@gmail.com (E. Pucheta). 0140-1963/$ see front matter 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2009.08.002

recognized as important controlling factors for the functioning of arid and semiarid ecosystems (Noy-Meir, 1973; Kemp, 1989; Montana, 1992; Pake and Venable, 1996; Ludwig et al., 1999). Interyear rainfall variability may affect the intensity of germination cycles, growth and productivity of herbaceous plants and shrubs (Noy-Meir, 1973; Jobbagy and Sala, 2000), affecting the soil seed reserves, as well (Kemp, 1989; Pake and Venable, 1996; Mar one and Horno, 1997; Gutierrez et al., 2000). Moreover, regional to global climatic variations, like changes in the magnitude of seasonal rainfall, may affect the accumulation of seeds in soil as previously observed after the inuence of the El Nino-Southern Oscillation (Gutierrez et al., 2000; Marone et al., 2000; Gutierrez and Meserve, 2003). The vegetation in deserts and semideserts is spatially arranged as a two-phase mosaic of shrub patches on a matrix of bare ground (Montana, 1992; Ludwig et al., 1999). These microhabitats usually affect ecosystem functioning, including seed banks (Aguiar and Sala, 1994; Marone and Horno, 1997; Bertiller, 1998; Guo et al., 1998; Pugnaire and Lazaro, 2000; Aerts et al., 2006; Caballero et al., 2008b). Moreover, microhabitats and rainfall may interact exacerbating or counteracting climatic conditions by controlling soil

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moisture, which may initially affect plant performance and repro duction (Noy-Meir, 1973; Fernandez, 2007) and lately soil seed replenishment (Pake and Venable, 1996). The Medanos Grandes sandy desert is one of the driest landscapes of the central Monte, with a particularly low annual rainfall average over the last thirteen years (117 mm, CV 45%). This region was formerly part of a now inactive huge sand sea (erg), occupying more than 1300 km2. Its vegetation is composed of a patchy structure of clumps of woody perennial shrubs and trees clustered into a low-covered matrix of seasonal forbs and grasses. We have shown that some dominant shrubs affect ecosystem properties such as soil decomposition potential, short- to long-term litter decomposition, soil nutrient concentration (Pucheta et al., 2006), and soil seed density and seed depletion rates of the dominant Bulnesia retama shrubs (Ribas-Fernandez et al., 2009). Moreover, we found that the presence of vegetated patches, together with the amount and distribution of seasonal rainfall, may produce nonadditive effects on ecosystem processes like accelerating the rate of litter decomposition under B. retama shrubs (Pucheta et al., 2006). In this study we addressed the effects of two consecutive growing-season rainfall and of two microhabitat types (shrub patches and bare ground) on seed density and oristic composition of the germinable soil seed bank of annual plants. We hypothesised that seed composition and density is affected at a very small scale by the presence of vegetated patches, but that this effect varies between years according to rainfall. We predict overall lower soil seed density and higher seed density under shrubs after a dry growing season. Moreover, we predict overall higher seed densities and higher similarity in seed density between microhabitats after a moister growing season. The main objectives of this study were to evaluate (1) soil seed density and (2) the oristic afnities of the germinable seed bank of annual plants in two microhabitats after two consecutive growing seasons with contrasting rainfall. 2. Methods 2.1. Study site We carried out this study at Medanos Grandes in central Monte desert, southern San Juan, Argentina. The study site (31 46 S, 67 55 W) was located 8 km from Vallecito, at 711 m asl. Annual rainfall in the Monte phytogeographic province can range between less than 100 to more than 300 mm from northern to southern locations, increasing the importance of winter rains along the same gradient (Morello, 1958; Ojeda et al., 1998; Krop et al., 2002). According to Morello (1958), the study area belongs to the driest area of the entire Monte phytogeographic region. The climate is temperate, with hot summers and cool winters, and 70% of the 117.6 mm annual precipitation falling in the warmer months (DecemberMarch). Table 1 shows the quarterly rainfall and temperature data as from December, following the beginning of the growing season. The soils are sandy and deep (> 6 m depth), with a slight southeast faced slope (<6%) that receives ephemeral streams from the Pie de Palo hills.

The vegetation of the area is patchily distributed, with perennial shrubs (up to 40% cover) clustered around soil mounds and herbaceous vegetation, mostly summer annuals and grasses, occupying both interspaces and soil mounds. The dominant vegetation in the study area is a shrubland of B. retama (Gillies ex Hook. and Arn.) Griseb and Larrea divaricata Cav., with a minor presence of Prosopis exuosa DC. f subinermis Burkart. in depressed sites or along ephemeral drainages. Other shrubs are Lycium spp., Capparis atamisquea Kuntze, Senna aphylla (Cav.) H.S. Irwin and Barneby and Bougainvillea spinosa (Cav.) Heimerl. Ephemeral and annual forbs may be found as fast as seven to ten days after rains, but show more shrub canopy-dependence after lower growing-season rainfalls (pers. obs.) as observed for Sclerophylax arnottii Miers, Portulaca grandiora Hook, Portulaca echinosperma Hauman and Chenopodium papulosum (Moq.). Some perennial grasses, such as Aristida mendocina Phil., Pappophorum philippianum Parodi and Pappophorum caespitosum R. Fries are present as rare species. The nomenclature of plant species follows Zuloaga and Morrone (1996, 1999). 2.2. Sampling design 2.2.1. Microhabitats, interyear variability and germinable seed bank To understand the effect of spatial vegetation heterogeneity and the amount of previous rainfall on the germinable soil seed bank of annual plants, we sampled soils from shrub undercanopies and bare ground throughout a two-year study. As most herbaceous species are summer annuals, we sampled soils in the cool season (MayJuly) after seed set but before seed germination. Rainfall data was provided by EEA San Juan INTA (S. Silva, unpublished). We selected an area of 10 ha where we individualised 30 interspersed multi-species shrub patches that were similar in size and composition and 30 adjacent sites on bare ground. After seed dispersal, in late July 2002 and late May 2003, we collected three composite soil samples through the main longitudinal axe of each vegetation patch, and another three composite samples in an area of 4 m2 on bare ground 23 m away from the shrub patches using an iron corer 10 cm in diameter and 5 cm deep. We only sampled the rst 5 cm of soil because in most deserts the most important proportion of seeds is found in the rst 2 or 3 cm (Kemp, 1989; Marone et al., 1998). We stored samples in air-dried opened bags in the dark, at room temperature and a dry atmosphere until processing. We registered the germinable soil seed bank after keeping the samples at 4  C during a 45 day-period, as most seeds germinate after the cold season. Seedling emergence of soil samples was registered in a greenhouse under controlled conditions (12 h light/ 12 h darkness; 2025  C mean temperature), as from October 2002. Samples were spatially distributed at random and incubated in plastic pots (25 30 cm) lled with 2 cm vermiculite and watered as necessary until species identication. We crumbled soils after three months for a new period of plant germination and species identication. We repeated seed bank germination experiment for the second growing season in October 2003.

Table 1 Quarterly rainfall (mm SD) and temperature data ( C SD) recorded at the nearest weather station (26 km away; Las Casuarinas, EEA San Juan INTA) during 13 years (19952007) in a sandy Monte Desert of western Argentina. DJF Rainfall (mm)/(percent of total/CV) Mean max. temperature Mean min. temperature Mean temperature 55.1 29.6 (46.8/53.8) 34.2 1.8 17.0 0.7 25.7 1.2 MAM 36.0 29.7 (30.6/82.5) 25.0 1.0 9.3 1.7 17.4 1.3 JJA 9.8 15.3 (8.3/156.5) 17.3 1.7 0.8 2.4 8.8 2.1 SON 18.6 20.8 (15.8/112) 27.8 2.2 9.2 1.7 18.8 1.8 Annual average 117.6 53.2 (100/45.2) 34.7 2.2 1.7 4.0 17.6 6.9

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2.3. Data analysis To test the hypothesis of no differences between species composition between microhabitats and years, we analysed data by means of multiple response permutation procedures (MRPP; McCune and Mefford, 1999). This procedure calculates two statistics. Initially, a weighted mean within-group distance in species space is calculated using S4rensen distance. Then, a T statistic is calculated as the ratio of the difference between the observed and expected mean distances and the standard deviation of the expected difference. T statistic describes the separation between groups; the more negative the statistic, the stronger the separation between groups. A P-value is used to evaluate the likelihood of achieving the observed difference by chance. To evaluate differences in species occurrence among microhabitats and years, we performed indicator species analyses (Dufrene and Legendre, 1997). This method combines information on the species abundance at particular samples and the faithfulness of occurrence of a species at a particular spatial or temporal position, allowing to test the null hypothesis that the species has no indicator value. First, we calculated an indicator value for each species as the product of their relative abundance and relative frequency. Secondly, we tested the statistical signicance of the higher indicator value (IVmax) for each species using a Monte Carlo method after 1000 iterations. To test for signicance, we set a at 0.05. We used PC-ORD software (McCune and Mefford, 1999) to perform the multivariate analyses. To assess the overall effects of microhabitats, growing seasons and their interaction on total seed bank density, we performed a two-way ANOVA with microhabitat and growing season as xed factors with two levels each. Post-hoc LSD tests with a signicance level of 0.05 were applied to signicant differences. All data were assessed for normality, independence of errors and homogeneity of variance prior to the analyses. Data of total seed bank density had to be log-transformed to meet the assumptions of parametric analyses. We performed general linear models with SPSS 11.0 package. 3. Results The rainfall recorded during the rst growing season, October 2001 to April 2002, was 75.1 mm and was mainly concentrated towards the end of the season, in February. During the second growing season, October 2002 to April 2003, accumulated rainfall was 138.9 mm, with relatively higher rain pulses and a greater number of events (Fig. 1). A thirteen-year record of quarterly rainfall data evidenced a distribution concentrated in the warmest months, which also have the lowest interyear variability (Table 1). There were no events greater than 16 mm during the rst growing season, and only two events greater than 35 mm were

registered for the second growing season. The number of recorded rain events ! 10 mm 25 mm were 2 and 4 for the rst and second growing seasons, respectively. Likewise, the number of rain events under 10 mm was 18 for the rst growing season and 14 for the second. In ve opportunities there were two consecutive rain events during the rst growing season, all of them adding up to less than 8 mm. On the other hand, the second growing season showed 4 two-day consecutive rain events, two of which amounted to more than 21 mm (Fig. 1). 3.1. Inuence of interyear variability and microhabitat on seed bank density We found signicant effects of interyear variability (F 20.9; P < 0.0001) and microhabitat type (F 11; P 0.0013) on the germinable soil seed density of annual plants. The total number of emerged plant individuals per soil sample in second moister growing season (608.1 62.9 seeds m2) was twice the amount registered in the rst rainy season (295.2 36.7 seeds m2). Moreover, total seed density was greater under shrubs (529 46.9 seeds m2) than on bare ground (399.3 74.2 seeds m2) (Fig. 2). No statistic interaction between the preceding rainfall and microhabitat type was found to explain seed bank density (F 3.12; P 0.08). However, the differences in seed density between microhabitats were much lower after the second rainier season, where 55% of seeds were found under shrubs in contrast to the 76% found after a drier growing season. 3.2. Inuence of interyear variability and microhabitat on annual plant composition Fifteen annual plant species were registered in the germinable seed bank during the entire study, all of them natives (Appendix). Five of these plant species emerged exclusively after the rst drier growing season (20012002), but none were exclusive of the second season (20022003). The results of applying the multiple response permutation procedure (MRPP) to the composition of the germinable seed bank showed that microhabitat and the rainfall of the preceding growing season are two important sources of spatial and temporal variation,

Fig. 1. Distribution of daily rain events for two consecutive growing seasons (2001 2002 and 20022003) in a sandy Monte Desert of western Argentina. Arrows show soil seed sampling.

Fig. 2. Seed density of annual plants in the germinable seed bank (seeds m2) after two consecutive growing seasons and from two different microhabitats, in a sandy Monte Desert of western Argentina.

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respectively. The T statistics for seed bank species grouped according to growing season (T 13.17; P < 0.00001) and to microhabitat type (T 5.13; P 0.0013) were both negative and highly signicant. This statistic describes the separation between groups: a more negative value of T indicates a stronger separation between groups. Finally, we evaluated the effect of the interaction between growing season and microhabitat as a source of variation in seed species composition and abundance by MRPP. The four resulting groups of species were signicantly different (T 11.56; P < 0.00001). Indicator species analysis showed 9 species (60% of the total) with a statistically signicant (P < 0.05) afnity to one of the four situations resulting from the combination of two growing-seasons two microhabitats. One group of species, including the short-lived Boopis sp., Tribulus terrestris and Gomphrena mendocina, was indicative of the germinable seed bank of soils under shrubs following the rst drier growing season. Another group, represented by the late summer-species Sclerophylax arnotii, P. grandiora and Chenopodium murale, was indicative of bare ground soils after the rst growing season. On the other hand, three species were associated to the second and moister growing season: Amaranthus standleyanus and Portulaca umbraticola to patchy vegetation soils and C. papulosum to bare ground (Table 2). 4. Discussion The annual precipitation registered for 2001, 2002 and 2003 was 72.7, 102.1 and 99 mm, respectively. However the rainfall of the previous growing-season, which may be strongly associated to the seed set of annual plants, was 75.1 and 138.9 mm for the rst (20012002) and the second growing season (20022003), respectively. Interyear variability between rainy seasons was well below and above the long-term (19952007) average for this season (91 mm). Moreover, the size and frequency distribution of rain events of the both growing seasons was quite different. The number of rain events in the second year was greater, reaching or exceeding the 20 mm threshold for plant growth and reproduction described for most desert annuals (Whitford, 2002). Nevertheless, most of the rain events were low-sized and temporally sparse, typically between 6 and 9 mm. A thirteenyear record of rainfall data showed that more than 77% of the rains were concentrated during the warmer months, between December and March, as observed in other summer deserts (Gutterman, 2002).

4.1. Inuence of rainfall interyear variability and microhabitat on seed bank density We detected a general trend for the abundance of the germinable seed bank expressed in the following sequence: moister year under shrubs > drier year under shrubs > moister year bare ground > drier year bare ground. As previously hypothesised, we observed signicant effects of seasonal rainfall and microhabitat type on seed bank density but we failed to nd any signicant interaction between both factors. Despite this lack of interaction, the soil seed bank density registered under shrubs and on bare soil was very similar after a rainy summer but highly different after a drier growing season, suggesting that rainfall and microhabitat having non-additive effects. If this were true, shrub canopies would be functioning as safe sites for annual plant reproduction when drier environmental conditions limit plant establishment, plant growth and seed set elsewhere, as previously observed for other desert annuals (Pake and Venable, 1996). We found an overall low amount of germinable seeds for annual plants in the seed bank, irrespective to the growing season and patch type considered. Similarly, low soil seed density was also observed in a previous study of a similar sandy desert (unpublished data). In that study, seed densities ranged between 40 and 600 seeds m2 in soil samples associated to the dominant shrubs B. retama (241.6 seeds m2 164.7 SD) and L. divaricata (143.6 seeds m2 97.3 SD), and 0 466 seeds m2 in bare ground samples (150.2 seeds m2 123.3 SD). Most reports on desert seed bank density are based on total seed counts from the direct inspection of soil samples and not on the germinable fraction, resulting in higher seed estimations (Marone and Horno, 1997; Marone et al., 1998; Guo et al., 1999; Gutierrez et al., 2000; Gutierrez and Meserve, 2003). Germinable seed banks have been rarely reported for deserts and semideserts (Ghermandi, 1997; Pugnaire and Lazaro, 2000; Facelli and Temby, 2002; Facelli et al., 2005; Caballero et al. 2008a, 2008b). The soil seed density observed after the rainy summer of 2002 2003 was double the amount following the drier summer of 2001 2002. On the other hand, seed density under shrubs was 1.3 times greater than that observed on bare ground. Positive effects of rainfall (Pake and Venable, 1996; Marone and Horno, 1997; Gutierrez et al., 2000; Marone et al., 2000; Gutierrez and Meserve, 2003) and vegetation patches (Bertiller, 1998; Guo et al., 1998; Pugnaire and Lazaro, 2000; Aerts et al., 2006) on seed bank density have been extensively documented for several deserts. Thus, the association of ephemeral or annual species to shrubs may be considered a common characteristic of deserts (Kadmon and Shmida, 1990; Gutterman, 1994; Tielborger and Kadmon, 1995, 1997; Holzapfel et al., 2006). 4.2. Inuence of rainfall interyear variability and microhabitat on seed bank composition The MRPP analysis showed that interyear variability was signicantly more important than microhabitat type in dening seed bank composition. Moreover, the same analysis showed a signicant interaction between the precedent seasonal rainfall and microhabitat on species composition. These ndings are similar to that reported by Facelli et al. (2005), who showed that specic plant compositions can emerge from the same soil samples subjected to different environmental conditions, describing this as a likely component of the storage effect (Chesson, 2000). Moreover, it has been emphasised that variations in spatial and temporal resource availability is an important factor controlling the seed bank persistence of ephemeral and annual plants in desert ecosystems, promoting their success in highly variable environments (Beatley, 1974; Pake and Venable, 1996; Facelli et al., 2005).

Table 2 Annual plant species from the germinable seed bank of a Monte Desert ecosystem with indicator values (P < 0.05) for different combinations of growing seasons and microhabitats. Growing season, microhabitat type Indicator value (IV) Observed IV Maximum expected IV SD 20012002, shrub patches Boopis sp. Tribulus terrestris Gomphrena mendocina 20012002, bare soil Portulaca grandiora Sclerophylax arnottii Chenopodium murale 20022003, shrub patches Amaranthus standleyanus Portulaca umbraticola 20022003, bare soil Chenopodium papulosum 45.5 9.1 14.7 46.6 44.2 76.5 49.0 29.1 38.4 13.5 4.0 6.6 36.3 31.2 29.0 19.9 14.8 29.1 P

3.13 0.001 1.66 0.033 2.25 0.006 4.38 0.032 4.39 0.010 4.79 0.001 3.89 0.001 3.21 0.003 4.81 0.047

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We found that 60% of the total annual species had a statistically signicant afnity to one of the four situations resulting from the combination of two growing-seasons two microhabitats. A rst group included the short-lived Boopis sp., T. terrestris and G. mendocina, emerging from soils under shrubs after the rst drier growing season. A second group of species emerged from bare ground samples after the same growing season, including the latesummer S. arnotii, P. grandiora and C. murale. Three species were associated to the second and moister growing season: A. standleyanus and P. umbraticola emerged from patch vegetation soils, and C. papulosum from bare ground soils. Despite the signicant indicator species found for each different situation, we do not have enough information on the natural history of the different plant species to generate a plausible explanation for this pattern. For this, specic studies on the autoecology of these annual species are required. However, the previous environmental conditions acting on the seeds of the different species, both in the soil seed bank and those on the mother plants, may change their germinable fractions, as previously observed for some desert annuals (Pake and Venable, 1996; Clauss and Venable, 2000; Tielborger and Valleriani, 2005). This mechanism could partly explain the change in seed density or the apparent absence of seeds from the germinable seed bank, as some species may vary their germinable fraction from zero to more than 50% (Clauss and Venable, 2000). However, species-specic studies on the changes in the germinable fraction of seeds under different environmental conditions are necessary to nd causal explanations for the seed bank variations of annual plant species in this desert. Altogether, our ndings suggest that the presence of shrub patches and the amount and timing of rain events during the precedent growing season might control the abundance and identity of ephemeral and annual plant species in the germinable seed bank. Acknowledgements We are grateful to Daniela Bustos, Mariano Ariza and Aureliano Campoy for their invaluable eld collaboration; to Eduardo Martnez Carretero for plant identication and Monica Ruiz and Alfredo Nequi (EEA San Juan INTA) for their assistance at the laboratory and greenhouse. Sonia Silva (EEA San Juan INTA) kindly provided rainfall data. Adrian Escudero and Guillermo Funes made important comments on earlier versions of the manuscript. This study was partially supported by grants to E.P. from Universidad Nacional de San Juan (CICITCA 21 E/358, 21 E/ 629, 21 E/834). Appendix. Seed density of the germinable seed bank of annual plant species (seeds mL2 SE) after two consecutive growing seasons and from two microhabitat types, in a Monte Desert ecosystem, western Argentina.
Species/ Microhabitat Growing season 20012002 Under shrubs 1.5 1.5 40.9 11.2 4.4 2.4 1.5 1.5 2.9 2.0 11.7 4.7 106.8 22.9 Bare soil 20022003 Under shrubs Bare soil

(continued) Species/ Microhabitat Growing season 20012002 Under shrubs 43.9 15.3 1.5 1.5 29.3 8.2 27.8 8.5 7.3 3.0 8.8 4.9 7.3 3.0 1.5 1.5 297.1 36.4 107.5 17.9 554.7 65.2 Bare soil 14.1 5.3 2.8 2.8 2.8 2.8 5.7 3.8 2.8 2.8 2.8 2.8 20022003 Under shrubs 64.4 17.5 98.0 25.2 159.5 41.8 17.6 6.5 20.5 11.8 2.9 2.0 2.9 2.0 Bare soil 120.0 32.9 178.6 58.9 1.5 1.5 1.5 1.5 5.8 4.6 1.5 1.5 1.5 1.5 1.5 1.5 537.1 102.7

Sclerophylax arnottii Chenopodium murale Amaranthus standleyanus Portulaca umbraticola Chenopodium papulosum Solanum euacanthum Lepidium myrianthum Bouteloua barbata Total seed density

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