Can spatial variation and inter-annual variation in precipitation explain the seed density and species richness of the germinable soil seed bank in a tropical dry forest in north-eastern Brazil?

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Can spatial variation and inter-annual variation in precipitation explain the seed density and species richness of the germinable soil seed bank in a tropical dry forest in north-eastern Brazil? Danielle Melo dos Santos a,∗ , Kleber Andrade da Silva b , Ulysses Paulino de Albuquerque a , Josiene Maria Falcão Fraga dos Santos a , Clarissa Gomes Reis Lopes c , Elcida de Lima Araújo a a

Universidade Federal Rural de Pernambuco, Departamento de Biologia, Área Botânica, Dois Irmãos, CEP: 52171-900 Recife, Pernambuco, Brazil Universidade Federal de Pernambuco, Centro Acadêmico de Vitória, Rua do Alto do Reservatório s/n, Bela Vista, CEP: 55608-680, Vitória de Santo Antão, Pernambuco, Brazil c Universidade Federal do Piauí, Campus Amílcar Ferreira Sobral, BR 343, Km 3,5, Meladão, CEP: 64800-000 Floriano, Piauí, Brazil b

a r t i c l e

i n f o

Article history: Received 31 October 2012 Accepted 22 June 2013 Available online xxx Keywords: Seed bank Caatinga Microhabitat Seed germination Semi-arid

a b s t r a c t The interaction between microhabitat and inter-annual variation in precipitation has an important role on the dynamics of the seed bank and can play a crucial role in survival and maintenance of plant populations in semi-arid environments. We hypothesized that the type of microhabitat and the inter-annual variability in precipitation can explain the richness and density of the seed bank in a semi-arid region in Brazil. The study was conducted in an area of tropical dry forest with shrub-tree physiognomy, locally called caatinga. We collected 35 soil samples in three distinct microhabitats, at the end of rainy and dry seasons, respectively, over three years, totalling 630 samples. The seed bank (richness and seed density) were determined by seedling emergence method. Over the three years, 79 species emerged from the seed bank, 64, 45 and 42 in riparian, non-riparian and rocky microhabitats, respectively. We recorded differences in species richness and average density between microhabitats and between years, with significant statistical interaction between them. Inter-annual precipitation explained 48% and 5% of the variation in richness and seed density, respectively. Spatial variation explained 7% of the species richness and 31% of the density. Our results show that the interaction between spatial variation and precipitation has an important role on the spatial and temporal heterogeneity of the richness and density of seed banks in dry environments. © 2013 Elsevier GmbH. All rights reserved.

Introduction The density of the soil seed bank of a dry environment can vary in space and time (Garwood, 1989; Silva, 2009). Regarding space, the variation can be both horizontal and vertical. There are studies that have separately evaluated seed density in litter and soil at different depths (Mamede and Araújo, 2008; Santos et al., 2010; Silva, 2009) while others have assessed the variation in seed density in soil according to depth without isolating the litter (Cabin and Marshall, 2000; Hérault and Hiernaux, 2004; Ma et al., 2006; Ne’eman and Izhaki, 2009; Quevedo-Robledo et al., 2010). In general, these studies indicate that there is a decrease in seed density with increasing soil depth.

∗ Corresponding author. E-mail address: danmelo [email protected] (D.M. dos Santos).

Horizontally, soil variation can occur at the macro- or microscale. Macro-scale variation may be formed by patches of different vegetation types – e.g. shrubby spots or open areas dominated by herbaceous vegetation (Agra and Ne’eman, 2012; Caballero et al., 2008; Cabin and Marshall, 2000; Ne’eman and Izhaki, 2009; Quevedo-Robledo et al., 2010). Micro-scale variation may occur within the same local or within a plant community due to variation in topography – e.g. rocky, sandy, inclined, sloped or flooded patches (Araújo et al., 2005a; Caballero et al., 2003; Ma et al., 2006; Pessoa, 2007) and/or can also occur as a result of heterogeneity in the community structure above-ground (Gutiérrez et al., 2000; Olano et al., 2005). This variation of habitat may provide greater or lesser retention of seeds in the soil, influencing the species richness and the renewal rates of populations (Lima et al., 2007; Ma et al., 2006; Pérez et al., 2006; Pessoa, 2007; Quevedo-Robledo et al., 2010). On a time scale of years, the density of soil seed varies in response to changes occurring in the distribution of annual

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Please cite this article in press as: dos Santos, D.M., et al., Can spatial variation and inter-annual variation in precipitation explain the seed density and species richness of the germinable soil seed bank in a tropical dry forest in north-eastern Brazil? Flora (2013), http://dx.doi.org/10.1016/j.flora.2013.07.006

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precipitation (Costa and Araújo, 2003; Facelli et al., 2005; López, 2003; Pérez et al., 2006; Peters, 2002; Santos et al., 2010). This is particularly relevant to arid and semi-arid environments that show a marked seasonal climate (Araújo et al., 2007), with welldefined rainy and dry seasons leading to differences in the timing of plants’ fruit and seed production (Amorim et al., 2005; Machado et al., 1997; Pérez et al., 2006; Selwyn and Parthasarathy, 2006; Valdez-Hernández et al., 2010). Recently, a study conducted in a dry forest in north-eastern Brazil’s semi-arid region showed that seasonal differences do not always influence the soil seed bank’s seed density and species richness (Silva, 2009). This is due to unpredictable events (such as rains in the dry season or drought in the rainy season) that can cause a reduction in seed density, which is more strongly driven by trends in precipitation in previous years than by the rains of the current year (Silva, 2009). Together, this evidence indicates that the interaction between microhabitat and climatic seasonality has an important role on the dynamics of the soil seed bank and can promote the survival and maintenance of plant populations in semi-arid environments. However, few studies have directly tested whether the joint action of spatial differentiation and yearly precipitation can influence the species richness and quantity of seeds in the soil seed bank. Thus, assuming that the dynamics of the soil seed bank in semiarid environments reflects the interaction between their spatial and temporal heterogeneity, we hypothesized that the type of habitat and the inter-annual variation in precipitation can explain the richness and density of the soil seed bank in dry environments. To test this hypothesis, this study aims to answer the following questions: (1) Does species richness and seed density differ in response to habitat type and precipitation totals for each year studied? (2) Is there an interaction between total precipitation and habitat type in determining species richness and seed density from the soil seed bank?

Material and methods Description of study area The study was conducted in an area of tropical dry foresta with shrub-tree physiognomy, locally called “caatinga”. The vegetation within the study area is protected within an experimental research station belonging to the Agronomic Institute of Pernambuco – IPA (8◦ 14 18 S, 35◦ 55 20 W, 535 m asl) in the city of Caruaru, Pernambuco state, Brazil. The local climate is seasonal, with an average annual precipitation of 680 mm, absolute minimum and maximum temperatures of 11 ◦ C and 38 ◦ C, respectively, and an average temperature of 22.5 ◦ C. The rainy season usually occurs from March to August, whereas other months are marked by drought. However, sporadic rains can occur in the dry season as can dry spells during the rainy season (Araújo et al., 2007). The total precipitation recorded in the first (March 2005–February 2006; rainy and dry season), second (March 2006–February 2007) and third (March 2007–February 2008) year of present investigation were 733, 586 and 764 mm, respectively. The IPA area is drained by the Olaria creek, a tributary of the Ipojuca river (Araújo et al., 2005a; Reis et al., 2006). According to Alcoforado-Filho et al. (2003), the soil type is eutrophic yellow podzol with rocky outcrops. The soil layer has an average depth of 0–20 cm and exchangeable values of Na, K, Ca, Mg, H and Al of 6, 6, 25, 11, 43 and 3 ␮mol kg−1 , respectively; available P 2.8 mg kg−1 ; and average values of C and N of 16.2 and 1.5 g kg−1 , respectively (Alcoforado-Filho et al., 2003).

Description of microhabitats The IPA experimental station covers 190 ha, most of which is used for livestock and agricultural research activities. The natural vegetation of the entire area was previously occupied by a single patch of natural caatinga, which has now been reduced to approximately 20 ha (Alcoforado-Filho et al., 2003). For 50 years, this 20 ha fragment has been a conserved area, and the transit of domestic animals and the removal of vegetation are not permitted. The study area (habitat – the 20 ha fragment) is gently sloped, almost flat, and has well developed soil, yet rock outcrops and stretches of riparian vegetation can be observed within this habitat. In present study, the rocky outcrops and the stretches of riparian and non-riparian vegetation will be designated by the term “microhabitat” because they are different in terms of the soil water availability and sunlight that reaches the soil, as recorded previously by Araújo et al. (2005a). In other studies, these variations within the same habitat are also called microsites or microhabitats (Seifan et al., 2010; Quevedo-Robledo et al., 2010). The riparian microhabitat corresponds to the strip of gently sloping land on the banks of the Olaria creek, excluding the portion of the streambed where water flows at the time of highest precipitation. In this microhabitat, woody plants are on average 7 m tall and form a relatively closed canopy, with greater shade that keeps the ground moist for months longer compared to other microhabitats. The non-riparian microhabitat corresponds to land with well-formed soil, 150 m off the bed of the creek. Woody plants of that microhabitat have an average height of 5 m, but form a more open canopy, with greater sunlight penetration compared to the riparian microhabitat, and this promotes rapid drying of soil in the dry season. The rocky microhabitat corresponds to locations with small rocks (with areas ranging from 2 to 5 m2 and rock surface heights from 0.1 to 1 m) that occur as distinct scattered outcrops in the non-riparian microhabitat, some being well-shaded by canopies of woody plants and others more exposed to the sunlight. Considering an area of 1 ha made up of non-riparian and rocky microhabitats, about 45% is occupied by the latter. Thus, rocky microhabitats are important for the plant community, as they reduce the space available for the establishment of certain woody species. Although soil formation is not common on the surface of outcrops, depressions and cracks in the rock accumulate small amounts of soil and litter (not measured in this study), which allow soil collection from this microhabitat. Moreover, rocky outcrops also exhibit a thin layer of bryophytes and lichens which favors the retention of a small amount of moisture on the rocks. Some therophytic herbs are able to complete their life cycles and disperse seeds on these rock outcrops. This indicates that the rocky microhabitat has an important ecological role in the community, as it allows for the establishment and substitution of herbaceous populations. Additionally, since these microhabitats need more time to dry out when compared to the non-riparian microhabitat, some herbs can survive in them for longer periods of time during the dry season (Araújo et al., 2005a, 2007; Reis et al., 2006). A previous survey of the plant community that was carried out in the study area (habitat – the 20 ha fragment) recorded 67 woody and 71 herbaceous species (Alcoforado-Filho et al., 2003; Araújo et al., 2005a, 2007; Reis et al., 2006). There was a predominance of Fabaceae, Euphorbiaceae and Cactaceae for the woody component, and Asteraceae, Convolvulaceae, Euphorbiaceae, Fabaceae, Malvaceae and Poaceae among herbaceous plants. The local climatic season determines the deciduousness of the woody flora during the dry season and visibility of therophyte herbs in the rainy season. (Alcoforado-Filho et al., 2003; Araújo et al., 2005a, 2007; Reis et al., 2006). There is no available information on the influence of the spatial variation (microhabitats) on the composition of woody species. The herbaceous species composition differs in the study

Please cite this article in press as: dos Santos, D.M., et al., Can spatial variation and inter-annual variation in precipitation explain the seed density and species richness of the germinable soil seed bank in a tropical dry forest in north-eastern Brazil? Flora (2013), http://dx.doi.org/10.1016/j.flora.2013.07.006

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In addition, to assist in the identification of the plants that did not flower, seeds of the species occurring in the study area were collected and germinated, and seedlings were compared for correct identification. Identification was made by consulting the literature and comparisons with specimens from the Professor Vasconcelos Sobrinho herbarium (PEUFR) and Dárdano de Andrade Lima (IPA), adopting the classification system of Cronquist (1988). Unidentified seedlings were listed as morphospecies. Statistical analysis

Fig. 1. Schematic view of the collection of the soil seed bank (20 × 20 × 5-cm plots) in the vicinity of the fixed 1 × 1-m plots in an area of tropical dry forest in northeastern Brazil.

area, with 42% of floristic similarity between the non-riparian and riparian, 57% between non-riparian and rocky, and 53% between the rocky and riparian microhabitats (Araújo et al., 2005a). Sampling of the seed bank In a previous long-term study, we analyzed the woody vegetation in a 1-ha area of caatinga (Araújo et al., 2005b). Within this 1-ha plot, we also randomly allocated 105 plots of 1 × 1 m for the study of herbaceous vegetation (Araújo et al., 2005a; Reis et al., 2006; Silva et al., 2008) – 35 for each microhabitat (non-riparian, rocky and riparian). Surrounding these plots (1 × 1 m), we collected 35 soil samples per microhabitat at the end of the rainy and dry seasons in three consecutive years (March 2005–February 2008) – a total of 630 samples (Fig. 1). The soil was collected in plots framed by galvanized sheet metal 20 × 20 × 5 cm, including the litter layer, following common methods for soil seed bank studies (Hegazy et al., 2009; Ma et al., 2006; Ne’eman and Izhaki, 2009; Quevedo-Robledo et al., 2010) All samples were packed in plastic bags and labeled for each plot and microhabitat. Within a greenhouse, each sample was placed in a styrofoam tray (20 × 38 × 3 cm) and irrigated daily with no added hormones or nutrients for six months. The trays were kept at an average temperature of 25 ◦ C, and received no photoperiod treatment. The trays were arranged in two rows, with 51 control trays placed between the rows. Control trays, containing autoclaved soil, were for detection of contamination (possible) caused by seed dispersal by wind. The determination of seed density in the soil seed bank was conducted using the seedling emergence method, which does not consider dormant seeds in the sample. Therefore, we investigated the germinable seed bank. This follows the methods of Brown (1992), Christoffoleti and Caetano (1998), and Gasparino et al. (2006), to allow comparisons between studies (Baskin and Baskin, 1989; Caballero et al., 2003; Hegazy et al., 2009; Ne’eman and Izhaki, 2009; Pessoa, 2007). Every day, seedlings emerging from each soil sample were counted, noting the date of germination, plot number and type of microhabitat from which the sample was collected. After emergence, identified seedlings were removed from the trays. Unidentified seedlings were transplanted to plastic bags (five per morphospecies and the remainder removed) and monitored (six months) to obtain reproductive material (herbs) for identification.

We calculated the mean species richness and seed density (viable seed in the soil) in the samples obtained from each season (rainy and dry) per plot of each microhabitat. The averages were used to incorporate the effects of local climatic seasonality, as the soil seed bank in the study area differs significantly in the wet and dry seasons. Thus, the use of seasonal average values allowed to evaluate inter-annual differences in species richness and seed density of the soil seed bank microhabitats. Examples of occurrence of such seasonal differences in the density of the soil seed bank are available in the work of Pessoa (2007), Santos et al. (2010) and Silva (2009). The data were log(x + 1)-transformed prior to the analysis to meet the assumptions of normality and homoscedasticity. Differences in the logarithmic data of species richness and seed density (viable seed in the soil) of the soil seed bank between microhabitats and between years were evaluated with a two-way ANOVA with significance set at P < 0.05 and a posteriori Tukey’s test using STATISTICS 7.0 software. Two-way ANOVA was used because it is an appropriate tool to answer the study’s question, since: (1) precipitation and microhabitat are independent variables in our experimental design and can predict the richness and density of the soil seed bank; (2) soil sampling was carried out with the same type of vegetation over a period of three years, but not in the exact same place (thus they were not repeated measurements). The significance and the explication power (R2 ) of the microhabitat × precipitation interaction and of each single variable in determining the species richness and seed density of the soil seed bank was evaluated with a stepwise linear regression using BioStat 5.0 Results Species richness During the three years of the study, a total of 79 species native to the study area emerged from the soil seed bank samples: 64 species in the riparian, 45 in the non-riparian and 42 in the rocky microhabitats. Of these species, 15 were identified to the family level, five to genus and 51 to species. Only eight were classified as morphospecies. Two species were found exclusively in the rocky microhabitat, four in the non-riparian and 28 in the riparian. Of the species exclusive to each microhabitat, only Portulaca oleracea, which was exclusive to the riparian, occurred in all three years. With the exception of the morphospecies, 57 species were herbaceous (no weeds), 10 were shrubs and four were trees (see Appendix 1). The families with higher species richness during the three study years were Euphorbiaceae, Poaceae, Fabaceae, Malvaceae and Asteraceae for the three microhabitats (see Appendix 1). On average, the species richness of plots (n = 35) ranged from 2 ± 0.9 to 7.9 ± 2.6 (mean ± SD) species in the non-riparian microhabitat, from 2 ± 1.2 to 6.7 ± 2.6 in the rocky microhabitat and from 3.6 ± 1.6 to 6.5 ± 1.6 in the riparian microhabitat, with differences between

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Table 1 Summary table of a two-way ANOVA for the effect of Inter-annual variation in precipitation (Pr) and microhabitat on species richness per plot (20 × 20 × 5-cm) and seed density (viable seed in the soil per plot) in an area of tropical dry forest in north-eastern Brazil (DF – degrees freedom; MS – mean square; F – F-test of Fisher; P < 0.05 – significant differences). Species richness mean

Pr Microhabitat Pr × microhabitat Error

Seed density mean

DF

MS

F

P

DF

MS

F

P

2 2 4 306

4.13 0.51 0.21 0.01

217.2 26.9 11.4

<0.01 <0.01 <0.01

2 2 4 306

10.9 2.36 0.36 0.09

114.2 24.6 3.7

<0.01 <0.01 <0.01

Table 2 Total species numbers (richness R), average species richness per plot (species per habitat and sampling year), mean number of seeds (viable seed in the soil per plot 20 × 20 × 5cm – n = 35) and total density (seeds m−2 – per microhabitats and per year) of a seed bank in an area of tropical dry forest in north-eastern Brazil. Different capital letters among years in the same microhabitats and different lowercase letters among microhabitats in the same year indicate significant differences in species richness and seed density by the a posteriori Tukey’s test at P < 0.05 (SD – standard deviation). Year

Microhabitat

R

Richness species per plot (mean ± SD)

I I I II II II III III III

Non-riparian Rocky Riparian Non-riparian Rocky Riparian Non-riparian Rocky Riparian

35 35 41 20 22 32 22 20 36

7.9 6.7 6.5 3.2 2.0 3.8 2.0 2.0 3.6

± ± ± ± ± ± ± ± ±

2.6Aa 2.6Aa 1.6Aa 1.1Ba 1.2Bb 1.0Ba 0.9Cb 0.8 Bb 1.6 Ba

microhabitats and years of monitoring and significant interaction between them (Tables 1 and 2). Twenty species had a continuous presence in time and occurred in all three years of study (see Appendix 1). Of these twenty species, nine occurred in all three microhabitats, viz. Begonia reniformis (Begoniaceae), Bidens bipinnata (Asteraceae), Delilia biflora (Asteraceae), Dioscorea coronata (Dioscoreaceae), Gomphrena vaga (Amaranthaceae), Panicum trichoides (Poaceae), Phaseolus peduncularis (Fabaceae), Pilea hyalina (Urticaceae) and Talinum triangulare (Portulaceae). We found that the average species richness in the non-riparian microhabitat differed over the three years of the study. There was a marked reduction in richness from the first year to the other years in the rocky and riparian microhabitats (Table 2). Between microhabitats, species richness was similar in the first year. In the second year, the average species richness of the rocky microhabitat was greater than the riparian and non-riparian microhabitats. In the third year, the species richness of the riparian microhabitat was greater (Table 2). Correlations indicated that inter-annual variation in precipitation could explain 48% of species richness within the study area, while microhabitat explained only 7%. In all three years, the joint action (interaction) of the spatial variation (microhabitats) and precipitation explained 55% of the species richness of the soil seed bank (Table 3).

Seed density A total of 7455 seedlings emerged from the soil samples over the three years. The estimated average and the standard deviation (SD) of the soil seed bank’s seed density in the plots ranged from 5.4 ± 5.1 to 78.2 ± 75.0 (n = 35) during the three years of the study and was highest in the rocky microhabitat (Table 2). Significant differences were observed in the average seed density among microhabitats and between years of monitoring, with significant interaction between them (Tables 1 and 2). In all three microhabitats average seed density was higher in the first year than in the second and third years. In the first year the highest average seed density was recorded for the rocky microhabitat. In the second and third year, the average seed density of

Seed density seeds per plot (mean ± SD) 31.8 78.2 30.1 7.3 14 15.1 5.3 20.1 10.8

± ± ± ± ± ± ± ± ±

21.3Ab 75.0Aa 16.7Ab 4.4Bb 9.5Ba 7.6Ba 5.1Bb 24.7Ba 6.0Ba

Total density (seeds m−2 ) 796 1955 753 184 350 377 134 503 270

the non-riparian microhabitat was smallest (Table 2). Inter-annual variation in precipitation explained only 5% of the seed density of the soil seed bank, while the microhabitat parameter explained 31% in the correlations. The interaction between spatial variation (microhabitats) and precipitation contributed 36% explaining in such an approach the seed density of the soil seed bank (Table 3).

Discussion Species richness and seed density versus spatial variation and precipitation The species richness and seed density of the soil seed bank measured in this study were within the range of variation (13–86 species and 5–33,000 seed m−2 ) found in studies conducted in arid and semi-arid environments around the world (Cabin and Marshall, 2000; Guo et al., 1998; Ma et al., 2006; Ne’eman and Izhaki, 2009; Pugnaire and Lazaró, 2000; Quevedo-Robledo et al., 2010). Most of the species found in the seed bank were herbaceous, similar to other arid and semi-arid environments (Caballero et al., 2003, 2008; Guo et al., 1998; Hegazy et al., 2009; Hérault and Hiernaux, 2004; Ma et al., 2006; Ne’eman and Izhaki, 2009). Few species (nine) were present in samples from all three microhabitats in the three years of monitoring, consistent with observations of Silva (2009) in a study of temporal dynamics of the seed bank in the same study area. Seven herbaceous species (Bidens bipinnata, Emilia sp. 1, Gnaphalium spicatum, Callisia repens, Chamaecyse hyssopifolia, Herissantia tiubae and Mollugo verticillata) found in this study were not recorded by studies of Araújo et al. (2005a) and Reis et al. (2006) about local vegetation. The other species are part of the current vegetation of each microhabitat (see Araújo et al., 2005a; Reis et al., 2006). According to Araújo et al. (2005a) and Araújo et al. (unpubl. data), the species composition of herbaceous vegetation of the caatinga can be divided into two groups, one persistent, occurring every year, and another ephemeral, occurring intermittently between years. This may explain the reduced species richness found. However, it is possible that this characteristic is particular to vegetation in

Please cite this article in press as: dos Santos, D.M., et al., Can spatial variation and inter-annual variation in precipitation explain the seed density and species richness of the germinable soil seed bank in a tropical dry forest in north-eastern Brazil? Flora (2013), http://dx.doi.org/10.1016/j.flora.2013.07.006

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Table 3 Summary of stepwise multiple linear regression for the influence of Inter-annual variation in precipitation (Pr) and microhabitats (M) on species richness per plot (20 × 20 × 5cm) and seed density (viable seed in the soil per plot) from the soil seed bank in an area of tropical dry forest in north-eastern Brazil (DF – degrees freedom; F – F-regression; R2 – refers to the proportion of the variability in seedling emergence and species richness set explained by the models; P < 0.05 – significant differences). Sources of variation

Seed density Df

Pr × M M Pr Error Total

2

Species richness F

R2

P

89.9

0.36 0.31 0.05

<0.01 <0.01 <0.01

312 314

semi-arid environments, as there are no studies suggesting that the composition of herbaceous species in seasonal semi-arid environments varies in pulses between years. Studies on the seed bank of other semi-arid environments have found that species richness of the seed bank is higher in wetter years (Aziz and Khan, 1996; Pugnaire and Lazaró, 2000). However, there are also data suggesting that the dynamics of the seed bank incorporate historical variation in total precipitation. Species richness and seed density in soil seed banks seem to be better explained by precipitation data from previous years than by the current year’s precipitation (Silva, 2009), because in semi-arid environments the reproduction of plants reflects the effect of seasonal variation in water resources occurring between years (Araújo et al., 2007; Borchert, 1994; Jolly and Running, 2004; Pérez et al., 2006). This may explain the reduction in species richness found between the first and second years of this study, as the total precipitation of the year preceding the study (2004) was 1064 mm, much higher than the total precipitation of the first year of the study (March 2005–February 2006, 733 mm), the second (March 2006–February 2007, 586 mm) and the third year (March 2007–February 2008, 764 mm). In addition, this study showed that the influence of microhabitat and inter-annual variation in precipitation on species richness and seed density of the soil seed bank differ in the intensity of their effects. While inter-annual variation in precipitation explained 48% of the species richness of the soil seed bank, the parameter ‘microhabitat’ in the correlations explained only 7%. In relation to seed density, we observed the opposite pattern: ‘microhabitat’ explained 31% of seed density, while ‘inter-annual variation in precipitation’ explained only 5% (Table 3). Among microhabitats, the riparian sites showed the highest species richness and the largest number of exclusive species, possibly because this environment (characterized by woody vegetation forming a closed canopy that provides greater shade) has available water for a longer period of time compared to the rocky and non-riparian microhabitats. Variation in water availability between microhabitats has been identified as a significant factor in determining species richness (Caballero et al., 2003; Grubb, 1977; Ma et al., 2006; Hegazy et al., 2009; Silvertown et al., 1999). For example, some studies have reported that woody plants established in disjunct patches can provide specific microhabitat conditions (higher humidity and lower temperature), allowing for greater species richness under the plants’ canopy (Caballero et al., 2008; Quevedo-Robledo et al., 2010; Seifan et al., 2010). Spatial variation in soil hydrological conditions (drying intensity and aeration) can favor greater species richness and biomass production in wetter microhabitats (Silvertown et al., 1999). Spatial variations in the community richness caused by such a “hydrological niche” might occur even in the absence of any obvious topographic variation, because many species are sensitive to variations in the water availability at a micro-scale (Silvertown et al., 1999). Therefore,

Df 2

F

R2

P

197.6

0.55 0.07 0.48

<0.01 <0.01 <0.01

312 314

wetter microhabitats can present high seed retention capacity and may function as regeneration niche for particular taxa (Grubb, 1977). Similar to species richness, seed density in the soil seed bank varies depending on the microhabitat. Micro-scale variation may occur within a plant community due to variation in topography. This variation may provide greater or lesser retention of seeds in the soil influencing the density of the soil seed bank (Caballero et al., 2003; Hegazy et al., 2009; Ma et al., 2006; Mayor et al., 2007; Pessoa, 2007). Until now, no study has found that rocky microhabitats (which usually do not present well-formed soils) exhibit a high seed density, as we did it record in this study. According to Araújo et al. (2005a), these rocky microhabitats not rarely covered with lichens and bryophytes, and they present depressions and crevices. All this may favor the accumulation of soil, litter and moisture. It is possible that the cracks and crevices of the rocks also are structures that specifically contribute to seed retention in this microhabitat, which might explain the high seed density that we recorded. Interaction between spatial variation and annual precipitation influencing species richness and seed density Although data of the inter-annual variation in precipitation explained only 5% of the variation in seed density, and the ‘microhabitat’ term explained only 7% of the variation in species richness, both correlations were significant. The joint action of these factors increases the explanatory power of their effects to 55% on species richness and 36% on the density of seeds (Table 3), confirming the basic hypothesis of present study. The significant interaction between microhabitat and inter-annual variation in precipitation affecting the soil seed bank confirms that spatial–temporal heterogeneity is a factor that strongly influences seed bank dynamics in semi-arid environments (Ma et al., 2006; Pérez et al., 2006; Quevedo-Robledo et al., 2010). In addition to inter-annual variation in precipitation and the effects of microhabitats, factors that are intrinsic (such as period of germination, degree and duration of dormancy, and longevity of seeds) and extrinsic to the species (seed predation before and after dispersion, pathogen attacks) may affect the species richness and density of the seed bank. These factors, although not measured by this study, were present in the three years of our study and might account for the 45% (concerning species richness) and 64% (concerning seed density) of variation that was not explained by inter-annual variation in precipitation and microhabitats. Local conditions are extremely important for the emergence and establishment of plant in the particular habitats (Fayolle et al., 2009; Jurena and Archer, 2003; McLaren and McDonald, 2003; Pérez et al., 2006). It is easier to identify microhabitats than to determine in a quantitative manner the particular conditions characterizing them, because not all physical and chemical variables

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6

that influence the establishment of a species are easily measured. Often, these conditions are defined by biotic and abiotic interactions that can act directly or indirectly, and vary in time and space (Quevedo-Robledo et al., 2010; Seifan et al., 2010). Therefore, in this study ‘microhabitats’ were used as umbrella terms for the totality of these conditions, and the significant correlations found do indeed show that the microhabitats either attenuate or intensify the effects of inter-annual variation in precipitation influencing the seed density of the soil. This is comparable, e.g., with a study done in New Mexico on a single species (Lesquerella fendleri), where inter-annual differences were observed in the number of seeds occurring below the canopy of shrubs and in open areas (Cabin and Marshall, 2000). Their density increased below the canopy of the shrubs in one year and in open areas in another year. Authors of this study explained the findings by arguing that the soil seed bank is not composed only of seeds produced during favorable reproductive periods, and that some species may form a persistent seed bank. Thus, a portion of the seed bank may have been produced in years with more restrictive climatic conditions, but they were stored in the soil, contributing to the density recorded every year. This certainly applies also to the samples from our different habitats, where we did not attempt to distinguish between taxa with a transient and taxa with a permanent seed bank. In summary, our results show that species richness and seed density of the caatinga soil seed bank depends on the interaction between spatial variation and inter-annual variation in precipitation. Conservation measures must therefore consider the different microhabitats, in order to maintain a high biodiversity in this dry environment vegetation. The different microhabitats can preserve and provide a high seed density even of plants that prevail in neighboring vegetation patches, as the data show for the rocky microhabitat (Table 2; Appendix 1). This does not exclude that some species are more or less concentrated in a certain microhabitat – as it was the case of Pseuderanthemum detruncatun, which only occurred in the riparian microhabitat (see Appendix 1). Predictive models of seed availability in the soil (for example, for the restoration of populations) need to incorporate the interactive effect of spatial–temporal heterogeneity in the environment and must consider longer time frames due to the influence of inter-annual climatic variations on local conditions that considerably can change the characteristics of the soil seed bank. Acknowledgements The authors thank the Agronomic Institute of Pernambuco (AIP) for logistics and permission to work on their property; the Graduate Program in Botany – PPGB of the Federal Rural University of Pernambuco – UFRPE for logistical support; the researchers of the Laboratory of Plant Ecology and Ecosystems of the Northeastern – LEVEN for their support, suggestions and assistance in implementing the project; and CNPq for fellowship awards, research productivity scholarships for the researchers and the financial support for the project (process 471805/2007-6 and 477239/2009-9). Appendix 1. Species of seedlings emerging in non-riparian (NR), rocky (RO) and riparian (RI) microhabitats during the three years of the study (1st: March 2005–February 2006; 2nd: March 2006–February 2007; 3rd: March 2007–February 2008) in an area of tropical dry forest in north-eastern Brazil.

Species Acanthaceae Pseuderanthemum detruncatum (Nees & Mart.) Radlk. Amaranthaceae Gomphrena vaga Mart.

Habit

Year

Microhabitats

Herb

1st

RI

Herb

1st 2nd 3rd

NR/RO/RI NR/RO/RI NR/RO/RI

Anacardiaceae Myracrodruon urundeva Allemão Araceae Anthurium affine Schot

Tree

1st 3rd

NR/RI NR/RI

Herb

1st 3rd

RI RO

Asteraceae Bidens bipinnata L.

Herb

Delilia biflora (L.) Kuntze

Herb

Emilia sp. 1 Gnaphalium spicatum (Forssk.) M. Vahl Begoniaceae Begonia reniformis Dryand.

Herb Herb

1st 2nd 3rd 1st 2nd 3rd 3rd 3rd

NR/RO/RI NR/RO/RI NR/RO/RI NR/RO/RI NR/RO/RI NR/RO/RI RI NR/RO/RI

Herb

1st 2nd 3rd

NR/RO/RI NR/RO/RI NR/RO/RI

Herb

1st

RI

Tree

2nd 3rd

RI NR/RI

Shrub

1st 2nd 3rd 2nd 3rd

RI NR/RO/RI NR/RO/RI RI RI

1st 2nd 3rd 1st 2nd 3rd

NR/RO/RI NR/RO/RI NR/RI RO RO/RI RI

1st 3rd 1st 2nd 1st 2nd 1st

NR/RO/RI NR/RI NR/RO NR/RI RI RI RI

Herb

1st 2nd 3rd

NR/RO/RI NR/RO/RI RI

Herb

1st 2nd 3rd 1st 2nd

NR/RO/RI NR/RO/RI NR/RO/RI RO/RI RI

Herb

1st

RI

Herb

1st

NR/RI

Shrub

1st 3rd 1st 3rd 1st 1st 3rd 2nd 3rd

NR NR NR/RI NR/RO/RI NR/RO NR NR/RO NR/RO RI

Boraginaceae Heliotropium angiospermum Murray Burseraceae Commiphora leptophloeos (Mart.) J.B Gillet Cactaceae Cactaceae sp. 1

Cactaceae sp. 2 Cereus jamacaru DC. Commelinaceae Callisia repens (Jacq.) L.

Shrub Tree

Commelina obliqua Vahl

Herb

Convolvulaceae Evolvulus filipis Mart.

Herb

Convolvulaceae sp. 1

Herb

Convolvulaceae sp. 2

Herb

Convolvulaceae sp. 3 Cyperaceae Cyperus uncinulatus Schard. ex Nees

Herb

Dioscoreaceae Dioscorea coronata Hauman

Herb

Dioscorea polygonoides Humb. & Bonpl. ex Willd Euphorbiaceae Bernardia sidoides (Klotzsch) Müll.Arg. Chamaecyse hyssopifolia (L.) Arthur Cnidoscolus urens (L.) Arthur

Herb

Croton blanchetianus Baill.

Shrub

Croton rhamnifolius Kunth Dalechampia scandens L. Euphorbia insulana Vell. Euphorbiaceae sp. 1

Shrub Herb Herb Herb

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Species Fabaceae Anadenanthera colubrina var. cebil (Griseb.) Reis Bauhinia cheilantha (Bong.) Steud. Chaetocalix longiflora Benth. ex A. Gray Desmodium glabrum (Mill.) DC

Phaseolus peduncularis W.P.C Barton Mimosaceae Acacia paniculata Willd.

Habit

Year

Microhabitats

Tree

2nd

RO

Shrub

2nd

NR

Herb

1st

RO

Herb

1st 2nd 3rd 1st 2nd 3rd

NR/RO/RI NR/RO RO/RI NR/RO/RI NR/RO/RI NR/RO/RI NR/RO/RI NR/RO/RI RI RI

Herb

Species Rhamnaceae Ziziphus joazeiro Mart. Rubiaceae Rubiaceae sp. 1

Selaginellaceae Selaginella sulcata (Desv.). Spring Solanaceae Solanaceae sp. 1 Urticaceae Pilea hyalina Fenzel

Mimosaceae sp. 1 Lythraceae Cuphea prunellaefolia A. St. Hill Malvaceae Corchorus hirtus L. Herissantia tiubae (K. Schum.) Brizicky Physaloides stoloniferum (Salzm.) H.C. Monteiro Pseudabutilom spicatum (Kunth.) R.E.Fr

Shrub

1st 2nd 3rd 3rd

Herb

3rd

RI

Verbenaceae Lippia americana L. Vitaceae Cissus sp. 1 Morphospecies 1

Herb Herb

1st 3rd

NR/RO NR/RO/RI

Morphospecies 2 Morphospecies 3 Morphospecies 4

Herb

1st

NR/RO

Morphospecies 5

Herb

Herb

Malvaceae sp. 2 Malvaceae sp. 3 Molluginaceae Mollugo verticillata L.

Herb Herb

NR/RO NR/RO NR NR RI NR/RO/RI NR/RO

Morphospecies 6 Morphospecies 7 Morphospecies 8

Malvaceae sp. 1

1st 2nd 3rd 1st 2nd 1st 1st

Herb

2nd 3rd

RI RI

Herb

1st

RI

Herb

1st 3rd

RI RI

Herb

1st

RI

Herb

1st

NR/RO

Herb

1st 2nd 1st

RI RI NR/RO RI NR/RO/RI NR/RO/RI NR/RO/RI NR/RO/RI NR/RO/RI NR/RI NR/RO/RI RI NR/RO/RI NR RI RI

Moraceae Dorstenia asaroides Hook Orchidaceae Oeceoclades maculata (Lindl.) Lindl. Oxalidaceae Oxalis euphorbioides A. St. Hill Phyllanthaceae Phyllanthus sp. 1 Poaceae Dactyloctenium aegyptium (L.) willd. Enteropogon mollis (Ness) Clayton Panicum maximum Jack. Panicum trichoides Swart

Shrub

Herb Herb Herb

Panicum venezuelae Hack.

Herb

Poaceae sp. 1

Herb

Poaceae sp. 2

Herb

Poaceae sp. 3 Polygalaceae Polygala paniculata L. Portulacaceae Talinum triangulare (Jacq.) Will

Herb

1st 1st 2nd 3rd 1st 2nd 3rd 1st 2nd 3rd 1st 2nd 3rd

Herb

3rd

RI

Herb

Talinum paniculatum Gardner

Herb

Portulaca oleracea L.

Herb

Portulaca sp. 2

Herb

1st 2nd 3rd 1st 2nd 1st 2nd 3rd 1st

NR/RO/RI NR/RO/RI NR/RO/RI RO NR/RO RI RI RI RI

7

Habit

Year

Microhabitats

Tree

3rd

RI

Herb

1st 2nd 3rd

NR/RO/RI RI RI

Herb

3rd

RI

Herb

3rd

RI

Herb

1st 2nd 3rd

NR/RO/RI NR/RO/RI NR/RO/RI

Shrub

3rd

NR

Herb

2nd 1st 2nd 1st 1st 1st 2nd 1st 2nd 2nd 2nd 1st

RI RO RI RI RI NR/RI R/RI NR/RO RI RI RI NR/RO/RI

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