This article appeared in a journal published by Elsevier.

The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elseviers archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright

Author's personal copy

Journal of Arid Environments 73 (2009) 1421

Contents lists available at ScienceDirect

Journal of Arid Environments

journal homepage: www.elsevier.com/locate/jaridenv

Pre- and post-dispersal seed loss and soil seed dynamics of the dominant Bulnesia retama (Zygophyllaceae) shrub in a sandy Monte desert of western Argentina
Y. Ribas-Fernandez, L. Quevedo-Robledo, E. Pucheta*
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

a r t i c l e i n f o
Article history: Received 31 August 2006 Received in revised form 5 December 2007 Accepted 10 December 2007 Available online 29 January 2008 Keywords: Seed bank Seed germination Seed predation Short-term persistence Spatial patches

a b s t r a c t
In deserts and semi-deserts dominant plants seldom rely on a persistent seed bank to ensure their recruitment from sexual reproduction, which is generally based on the seeds produced in the last reproductive event. We studied pre- and post-dispersal seed loss of Bulnesia retama, a dominant shrub of the sandy Monte deserts (western Argentina). We hypothesised that pre- and post-dispersal seed depletion in B. retama regulate soil seed density and in turn decrease soil seed reserves. We also hypothesised that spatial patches induced by standing vegetation and other microsites additionally affect post-dispersal seed loss and soil seed density. We observed that as much as half the total seed production was lost due to pre-dispersal seed predation. Seed dispersal plus predation showed a negative exponential function with 61% of seeds falling during the rst 28 days, and 99% after 90 days, when 34% of the seeds remained inside excluded branches. A signicant patch effect was observed on soil seed density and seed dynamics, with a greater number of seeds and increased seed depletion rates below B. retama shrubs. However, spatial patches did not affect seed germination although they increased with burial time, from 22% to 70% after 75 and 276 days, respectively. Likewise, a similar trend was found in potential seed germination; seeds collected directly from mother plants had a low germination rate (less than 25%), which increased to 75% after 276 days of soil burial. About 15% of the dispersed seeds should persist to the next rainy season, thus contributing to a low-density but persistent seed bank. The delay in seed germination and temporal decrease in soil seed density that we observed for B. retama suggest that a set of mechanisms have been developed promoting germination events whenever soil water is available, at any moment of the year. 2007 Elsevier Ltd. All rights reserved.

1. Introduction In most ecosystems, and particularly in deserts and semideserts, dominant shrubs and trees seldom rely on a persistent seed bank to ensure their recruitment from sexual reproduction, which is generally based on the seeds produced during the last reproductive event (Bertiller, 1998; Figueroa and Jaksic, 2004; Figueroa et al., 2004; Marone et al., 1998, 2000; Meney et al., 1994; Musil, 1991). In these species, plant regeneration only occurs after very favourable climatic conditions, which implies that most seeds are lost and new cohorts will be established few times in their life cycle (Harper, 1977).

* Corresponding author. Tel.: 54 264 4238766. E-mail address: epucheta@unsj-cuim.edu.ar (E. Pucheta). 0140-1963/$ see front matter 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.jaridenv.2007.12.001

Seed dispersal represents a link between seed production and seedling establishment and determines the spatial arrangement of seeds from which a new cohort of plants may arise, hence limiting plant recruitment (Nathan and Muller-Landau, 2003). The seed shadow (Willson and Traveset, 2000), or Phase I dispersal (sensu Chambers and MacMahon, 1994), is the spatial distribution of recently dispersed seeds (or diaspores) around a maternal plant or, more generally, around a source composed of multiple parents. The next stage in seed dispersal is commonly described as Phase II dispersal (Chambers and MacMahon, 1994), which implies the movement of seeds or diaspores to new locations or their incorporation into soil. Despite the fact that extended knowledge describes seed shadow or Phase I dispersal as a leptokurtic function with higher seed density under the maternal plant, deviations may occur due to heterogeneous habitat structure, a common feature of deserts and semi-deserts (Aguiar and Sala, 1999; Debisnki et al., 2001; Pugnaire and Lazaro, 2000). In arid shrublands where

Author's personal copy

Y. Ribas-Fernandez et al. / Journal of Arid Environments 73 (2009) 1421

15

individual shrubs are widely spaced, wind-blown or watertransported soil, nutrients, litter and seeds accumulate under these long-lived shrubs or trees, producing a heterogeneous environment that exerts great inuence on basic ecosystemic processes (Pucheta et al., 2006; Reynolds et al., 1999; Schlesinger and Pilmanis, 1998; Zaady et al., 1998). Moreover, many animals also cause seed redistribution by activities such as predation (Campos and Ojeda, 1997; Herrera, 1995; Milton and Dean, 2001; Villagra et al., 2002), burrowing, digging and seed hoarding (Armesto and Rozzi, 1989; Giannoni et al., 2001). Pre- and post-dispersal seed losses are important forces inuencing plant population dynamics and involve several factors between seed production and the recruitment of an adult plant (Wang and Smith, 2002). An important element of seed depletion is predation by seedeaters, including both pre-dispersal seed preda tion (Calvo-Irabien and Islas-Luna, 1999; Figueroa et al., 2002; Weppler and Stocklin, 2006) and post-dispersal seed predation (Figueroa et al., 2002; Hulme, 1997, 1998; Kelt et al., 2004; Villagra et al., 2002). Other causes of post-dispersal seed loss comprise ineffective germination (Grundy et al., 1999; Van Mourik et al., 2005; Villagra et al., 2002) and seed mortality as a result of ageing and attack by pathogens (Lonsdale, 1993). Most shrubs and long-living perennials usually exhibit minimal dependence on seed banks for their regeneration and protection against climatic uncertainty (Chambers and MacMahon, 1994; Kemp, 1989; Owens et al., 1995) as opposed to most desert annual and ephemeral grasses and herbs (Bertiller, 1998; Guo et al., 1999; Marone and Horno, 1997; Marone et al., 1998). However, a persistent seed bank represented by long-lived perennials has been found in some deserts or semi-deserts (Auld, 1995; Owens et al., 1995), as well as in halophytic communities (Aziz and Khan, 1996). Our objective was to study the fate of Bulnesia retama seeds before and after their dispersal in order to determine whether there is a persistent seed bank for this species. Furthermore, we were interested in the effects of different spatial patches on soil seed dynamics and seed loss due to germination. B. retama is a long-lived perennial shrub or small tree that is the dominant species in the extreme sandy deserts of the Monte phytogeographical region. There are no previous reports on whether this species has a seed bank or if most of the seeds produced each year are lost to seed consumers and germination events, as we suggest based on several previous eld observations. To our knowledge, there are no studies on the factors affecting seed fate and seed dynamics following seed production for dominant shrubs or trees of worldwide deserts and semi-deserts, except for the Monte (Marone et al., 2000; Villagra et al., 2002). However, this topic has been considered in other biomes showing seasonal water shortage, as in Mediterranean ecosystems (Figueroa et al., 2002; Garca-Fayos and Verdu, 1998). The aims of the present study were to study the proportion of seeds lost by pre-dispersal seed predation and to assess the effects of spatial patches created by B. retama, annual plant debris acting as seed traps, and open soils on soil seed dynamics and post-dispersal seed losses due to germination. We hypothesised that pre- and post-dispersal seed depletion in B. retama regulate soil seed density and decrease soil seed reserves. Additionally, we hypothesised that spatial patches induced by standing vegetation and other microsites also affect post-dispersal seed losses and soil seed density. We predict an important pre- and post-dispersal seed loss due to seed predation and seed germination, both affecting soil seed dynamics. Moreover, we expect seed depletion and seed germination rates to be higher beneath shrub canopies and in microsites acting as seed traps compared to those of bare soils given that the opportunities for seed predation and the conditions for germination should be much better in these sites.

2. Materials and methods 2.1. Study species B. retama (Gillies ex Hook et Arn.) Griseb. (Zygophyllaceae), locally known as retamo, has a disjunctive geographical distribution both in Peru and in the Monte (Debandi et al., 2002). This species is a woody aphyllous perennial shrub, 1.53.5 m high, with yellow hermaphroditic owers and schizocarpic fruits containing ve winged seeds (Palacios and Hunziker, 1984). Pollination is entomophilous, although they can self-pollinate; seed output increases after cross-pollination (Debandi et al., 2002). Reproductive phenology generally occurs within 4 months; owering occurs in 45 weeks towards the end of October, fruiting from November to February, and seed dispersal continues for at least 10 weeks after the initial fruit maturation (Debandi et al., 2002). In the present study, the species owered by the end of October 2004, fruits were still immature by mid-November and seed dispersal began slowly during mid-December. 2.2. Study site The study was carried out in the central Monte desert, in the province of San Juan, western Argentina. This area lies within the Monte Phytogeographical Region where the annual rainfall can vary from less than 100 mm in the North to over than 300 mm in the South, with winter rains increasing along the same gradient (Krop et al., 2002; Morello, 1958; Ojeda et al., 1998). The sampling site was an area of 4 ha located in the northwestern margin of Medanos Grandes, an aeolian sand sea (erg), at 599 m a.s.l. and 10 km South of Caucete, where important populations of the studied species are found (31460 0700 S68 020 0700 W). Although most dunes are xed, sand movement can be observed near roads and paths. The mean annual rainfall at the study site, over a period of 30 years, is 90 mm (70 mm) (De Fina, 1992), falling mainly from December (early summer) to May (autumn). The annual rainfall during the previous (2003) and current year of the study (2004) was below (38.5 mm) and above average (136 mm), respectively (Fig. 1). The climate is characterised by being dry, temperate but with cold winters. Mean summer (January) and winter (July) temperatures (over 10 years) are 25.1 and 7.7  C, respectively, with absolute maximum and minimum temperatures of 45 and 10  C, respectively, for the same months (Morello, 1958). The study was carried out on interdunes, at landscape units 5001000 m long and 100200 m wide, occupying over 60% of the total land surface. The dominant species, B. retama, and other plant species are mainly concentrated on interdunes and only occasionally found on dunes. B. retama covers 2535% of the interdune area, producing patches and thus contributing to the spatial heterogeneity. Other organisms, such as burrowing rodents, cacti and herbaceous plants, as well as ant colonies are often found under this species (pers. obs.). Previous observations in the same study site have shown that B. retama positively affects litter decomposition and soil nutrient concentration (Pucheta et al., 2006). Other shrub species, as for example Larrea divaricata Cav., Larrea cuneifolia Cav., Capparis atamisquea Kuntze, Senna aphylla (Cav.) H.S. Irwin & Barneby, Bougainvillea spinosa (Cav.) Heimerl, and the cacti Tephrocactus articulatus var papyracanthus (Phil.) Backeb., are present as subordinates. Annual herbs (Sclerophylax arnottii Miers, Ibicella parodii Abbiatti, Portulaca grandiora Hook, Portulaca echinosperma Hauman, Calicera spinulosa Gillies ex Miers, Morrenia odorata Lindl. and Chenopodium papulosum Moq.) and grasses (Aristida mendocina Phil., Pappophorum philippianum Parodi, Pappophorum caespistosum R. Fries and the alien Schismus barbatus (L.) Thell) are evenly distributed beneath and among the patches, throughout dunes and interdunes, appearing mainly after rains

Author's personal copy

16

Y. Ribas-Fernandez et al. / Journal of Arid Environments 73 (2009) 1421

Fig. 1. Monthly and annual rainfall before and during the study of Bulnesia retama seed production and dispersal in a sandy Monte desert ecosystem of western Argentina. The arrow shows the beginning of the eld study.

with the exception of Panicum urvilleanum Kunth, a perennial rhizomatous grass that grows on sand dunes all the year round. Soils are sandy and very similar in texture between patches and interpatches. The nomenclature of plant species follows Zuloaga and Morrone (1996, 1999, 2007). 2.3. Experimental design In early September 2003, we individualized 20 interspersed owering B. retama individuals that were similar in size and health appearance. Each shrub, including the area within a 10 m radius around the shrub, was considered a replicated experimental plot for three experimental units: (1) undercanopy, (2) annual plant debris microsite and (3) bare soil. 2.4. Seed production On 22 November 2003, we estimated the seed production of 20 individuals by counting the initial number of immature fruits on two average branches approximately 1 m long. We estimated the number of individual fruits and seeds by extrapolating the number of fruits per branch and the number of seeds per fruit to the total number of equivalent branches. The number of seeds per fruit rarely differed from ve. We measured the canopy diameter to estimate seed production from a canopy area basis. In early December, we collected 100 healthy and mature diaspores in order to obtain seed and diaspore size measurements. 2.5. Pre-dispersal seed loss To estimate pre-dispersal seed loss, we performed a mesh gauze experiment designed to exclude seedeaters larger than a 1 mm section (insects and birds). After counting the initial number of immature fruits in November, we covered one of the branches with a mesh (mosquito netting, 11 mm section). We registered seed loss monthly (20 December, 17 January and 22 February) on unexcluded branches until full seed dispersal. We failed to register the number of seeds dispersed inside the netting at periodic intervals, as it was impossible to manipulate the branches due to the fragile diaspore attachment. However, on 22 February we registered the total number of seeds that fell inside the mesh gauze, when a small fraction of seeds still remained attached to the twigs both inside and outside the exclosures. Therefore, we were only able to estimate a seed decay function for the unexcluded branches (dispersal plus predation). Pre-dispersal seed predation was estimated as the difference in seeds remaining inside and outside the exclosures for each individual at the end of the dispersal process.

To estimate the importance of insect attacks to undispersed fruits during the season, we collected 20 fruits per plant in each of the three sampling dates (total number of fruits60) until seed dispersal was completed. At the laboratory, using a dissecting microscope, we registered the percentage of schizocarps with dead seeds seemingly affected by chewing insects and lepidopteron larvae as described by Figueroa et al. (2002). This method represents a different estimate of seed death compared to seed predation that is estimated from the mesh gauze exclusions. We lost one B. retama individual after the second sampling date that was cut off, so after this episode we used 19 replicated plots. 2.6. Spatial patches and seed fate 2.6.1. Initial soil seed density and soil seed dynamics To study the inuence of spatial patches on soil seed reserves, we collected soil samples from the three types of patches detected at the study site once seed dispersal had already begun, on 13 March 2004. In order to study soil seed dynamics, we repeated soil sampling on each experimental plot on 31 July and 26 December 2004, 138 and 283 days later, respectively (3 patch types3 sampling dates19 replicates171 experimental units). We sampled soil (1) under B. retama shrub canopies, hereafter referred to as undercanopies, (2) within buried annual plant litter outside B. retama shrub canopies, hereafter called annual plant debris and (3) on bare ground distant 35 m from a parental shrub, referred to as interpatches. In each of the 19 replicated experimental units, we collected soil in two 3050 cm subsamples, 5 cm deep. Samples were sieved in the eld and the seeds collected were temporarily stored in nylon bags. Back at the laboratory, the seed samples were transferred to paper bags and stored at room temperature in the dark until processed. We only sampled the rst 5 cm of soil because in a preliminary sampling no seeds were evidenced deeper. 2.6.2. Post-dispersal seed loss by germination To study the effects of spatial patches on soil seed loss by germination, we shallow-buried (24 cm deep) 1525 cm mesh bags (11 mm mesh) lled with sand and 50 healthy complete diaspores (seeds with their winged structures), on 20 March 2004. A set of three germination bags was buried in each of 10 replicated experimental units (3 patch types3 sampling dates10 replicates90 experimental units). We collected one third of the germination bags after 75 (5 June 2004), 171 (11 September 2004) and 276 days (26 December 2004). We counted the number of the remaining ungerminated seeds conrmed by the presence of seeds, fruit coats and seedling residues.

Author's personal copy

Y. Ribas-Fernandez et al. / Journal of Arid Environments 73 (2009) 1421

17

To estimate the germination rate of seeds before and after their dispersal, we collected seeds directly from the plants (mother plants) and from the soil after 75, 171 and 276 days with a similar method used to collect the seed bank. In the laboratory, we incubated seeds from each sample on 15 Petri dishes (10 seeds per dish) with lter paper and deionised water, during 30 days in a growth chamber at 21  C under 12 h dark12 h light conditions (4 seed treatments15 replicates60 experimental units). 2.7. Data analysis Pre- and post-dispersal seed loss was assessed using repeated measures ANOVA followed by least signicant difference (LSD) post-hoc tests whenever signicant treatment effects were observed. Pre-dispersal seed loss was evaluated by the best-t nonlinear regression. Germination rates of both eld and laboratory experiments were assessed by repeated measures ANOVA and LSD post-hoc tests. All data were assessed for normality, independence of errors and homogeneity of variance prior to the analyses. Soil seed density data were log transformed to meet the assumptions of parametric analyses (SPSS 5 package; Norusis, 1992). 3. Results 3.1. Seed production and seed weight The seed production of B. retama during 2003 was 31,6004655 (meanS.E.) seeds per individual or 2752342 seeds m2 of canopy projection. The values of seed production varied greatly among the studied individuals, ranging between a minimum of 12,245 and a maximum of 78,750 seeds. Seed and diaspore size and weight are shown in Table 1. 3.2. Pre-dispersal seed loss After 90 study days, pre-dispersal seed loss attributed to seed and/or fruit predation was 34.17.1% of the total seed production. Furthermore, we found an additional 18.71.2% of average seed mortality of seeds still attached to plants, due to partial seed predation by several chewing insects or by lepidopteron larvae. Hence, the estimated total pre-dispersal seed loss, including seed predators and seed mortality caused by insects, was 52.87% of the total seed production. After a period of 90 days, 65.87.2% of the produced seeds were already dispersed. The proportion of pre-dispersal seed mortality due to partial insect consumption signicantly increased with time (F12.0; P<0.001). Prior to complete fruit maturation, in 22 November, 11.81.2% of the seeds collected evidenced signs of insect attack causing seed mortality. This percentage increased to 19.41.9% on 20 December and to 23.41.5% on 17 January 2003, when

39.44.6% and 5.41.8% of the total seed production, respectively, was still available on the plant canopies (Fig. 2). Total seed loss (dispersal plus predation) showed a signicant negative exponential function, with 60.5% of the seeds falling between the rst 28 days of seed dispersal, 34.1% after a second period of 28 days and 5.2%, after the following 36 days (Fig. 3). 3.3. Effects of spatial patches on post-dispersal seed fate 3.3.1. Soil seed reserves and soil seed dynamics On 13 March 2004, the average density of B. retama soil seed reserves was 532.281.1 seeds m2, representing 42.1% of total seed production. Initial soil seed reserves evidenced an important spatial patch effect (F62.5; P<0.0001). A signicantly larger number of seeds were found under B. retama shrubs (1019.6143.3 seeds m2), followed by about half this density in soils with annual plant debris (527.798.6 seeds m2), and a density two orders of magnitude lower in interpatch soils (49.411.1 seeds m2). The effect between-subjects (patch type) (F1449.5; P<0.0001), within-subjects (time after seed dispersal) (F94.3; P<0.0001) and the interaction term (F7.04; P<0.0001) were all signicant. LSD post-hoc contrasts among patch types evidenced higher seed depletion under B. retama compared to soils from annual plant debris and interpatches (P<0.05) (Fig. 4). Despite the signicant interaction found between patch type and time after seed dispersal, soil seed density was similar in undercanopy and annual plant debris soils after 283 days, with 8.6% and 7.2% of seeds remaining, respectively. A different trend was observed for interpatch soils, where seed density increased by 137% after 138 days, and then decreased by 29.5% after 283 days once seed rain ended. The highest percentage of remaining seeds at the end of the dispersal cycle was observed in soils from B. retama undercanopies. 3.3.2. Soil seed loss by germination Seed germination assessed by means of the buried bag method showed non-signicant differences among the three patch types analysed (F0.84; P0.443). However, the germination rate signicantly increased with time, as showed by the within-subject effect (F90.1; P<0.0001) (Fig. 5). Seed losses from soil seed reserves attributable to seed germination accounted for 21.7%, 58.6% and 70.3% after 75, 171 and 276 burial-days, respectively. No

Table 1 Size and weight (meanS.E.; N100) of B. retama seeds and diaspores collected at the study site, a sandy desert in western Argentina Variable Seed Weight (g) Length (mm) Width (mm) Diaspore Mass (g) Length (mm) Width (mm) MeanS.E. 0.0134.20E04 8.2801.66E01 2.5130.037

0.0340.001 22.3870.309 9.4040.113

Fig. 2. Percentage of seed mortality of individual seeds still attached to fruits in Bulnesia retama shrubs. Different letters indicate signicant differences (LSD; P<0.05). Box: interquartile range containing 100% of the data, line across box: median, square dot: mean.

Author's personal copy

18

Y. Ribas-Fernandez et al. / Journal of Arid Environments 73 (2009) 1421

Fig. 3. Exponential regression showing the percentage of remnant Bulnesia retama seeds until seed dispersal completion in the study area. Remnant seeds104.294exp(0.037t); F495.12, P<0.0001, adjusted R20.88.

Fig. 5. Variation of the percentage of seed germination during the rainy season in soils from different spatial patches of the study area. Black: undercanopy soils, grey: annual plant debris, white: interpatch areas. Different letters indicate signicant differences (LSD; P<0.05).

interaction effect was observed between patch type and time since burial for seed germination rates (F1.7; P0.169). The germination rates of seeds collected from mother plants and from increasing soil burial time were signicantly different (F114.7; P<0.0001). Moreover, a positive response in seed germination rate was observed as burial time increased (F399.3; P<0.0001) (Fig. 6(a)), as well as higher responsiveness in initial seed germination rates (incubation time2seed source interaction; F33.4; P0.0001) (Fig. 6(b)).

4. Discussion and conclusions As initially hypothesised, we found that a high proportion of B. retama seeds were lost to pre-dispersal predators and granivores. We also observed that in this species, seed dispersal occurs over the entire rainy season, increasing the probability of germination as well as the establishment of new seedlings all the year around. Germination of recently produced seeds and, more importantly, of those remaining in the soil during winter, were found to be

important causes of seed depletion during a year, irrespective of patch type. Seed production following a dry year in B. retama was similar to the seed production of other woody perennials from more mesic ecosystems (Radford et al., 2001; van Klinken, 2005). It has been suggested that the seed production of most shrubs and trees, including B. retama, in deserts is highly dependent on rainfall (Debandi et al., 2002; Radford et al., 2001; Solbrig and Yang, 1977). However, rainfall-dependence for shrub or tree reproduction could be minimal in plants with dimorphic roots that allow them to obtain water from deeper soils (Ehleringer et al., 1991; Horton and Hart, 1998; Hultine et al., 2004; Torres et al., 2002), as could be the case of the studied species. On the other hand, Fernandez (2007) suggests that desert shrubs or trees may not be strictly dependent on rainfall events but on the water content of the soil which, in turn, depends on a variety of factors besides rainfall. We believe that further research is necessary in order to understand the factors regulating seed production in B. retama. 4.1. Pre-dispersal seed losses A third of the total seed production (33%) did not follow through the dispersal pathway, but ended in pre-dispersal seed and/or fruit predation. A lower proportion of seed loss (18.7%) was due to seed mortality caused by insects, increasing total pre-dispersal seed loss to 53%. In a previous study of the same species, Debandi et al. (2002) reported that insect predation on buds and owers amounted to 80%, strongly reducing fruit production. Considering this result, we estimated that pre-dispersal total reproductive loss (owers plus fruits and seeds) could amount to almost 90%. High pre-dispersal seed depletion has also been reported for other similar ecosystems of the world in both native (Castro et al., 1999; Figueroa et al., 2002) and exotic woody perennials (van Klinken, 2005), reducing seed rain by 3540%. 4.2. Effects of spatial patches on seed fate 4.2.1. Soil seed reserves and soil seed dynamics B. retama fruits matured between November and December. Their seed dispersal signicantly tted to a negative exponential function, with almost 61% of the seeds falling within a period of 28 days, 34% after 56 days, and a remaining 5% after 92 days. This strategy of spreading seeds during the rainy season could reduce

Fig. 4. Soil seed dynamics of Bulnesia retama seed samples (mean number of seeds m2S.E.) from different spatial patches after seed dispersal and until soil seed depletion was almost completed. Black: undercanopy soils, grey: annual plant debris, white: interpatch areas. Different letters indicate signicant differences (LSD; P<0.05) for the interaction between patch type and time since the initial seed bank.

Author's personal copy

Y. Ribas-Fernandez et al. / Journal of Arid Environments 73 (2009) 1421

19

2000; Villagra et al., 2002). Even though long-lived perennials are usually minimally dependent on seed banks for their regeneration and protection against climatic uncertainty (Chambers and MacMahon, 1994; Kemp, 1989), persistent seed banks have been observed for some long-lived desert perennials (Auld, 1995; Owens et al., 1995). We think more studies about seed bank types of dominant shrubs and trees are needed to better understand plant recruitment in deserts and semi-deserts. As expected, the presence of spatial patches was reected in soil seed density. Furthermore, we found different seed depletion rates associated to patch types, with higher depletion rates in B. retama undercanopy and annual plant debris soils. Bare soils evidenced a much lower fraction of the total soil seed reserves. Most studies in deserts and semi-deserts have shown that vegetation patches play an important role shaping soil seed distribution (Bullock and Moy, 2004; Guo et al., 1998; Nathan and Muller-Landau, 2003; Nelson and Chew, 1997), as also observed in other Argentine deserts (Bertiller, 1998; Marone and Horno, 1997). 4.2.2. Soil seed loss by germination Our eld experiment, designed to assess soil seed depletion due to germination (seed burial), showed that patch type and the interaction between patches and burial time had non-signicant effects on the rate of seed germination. However, seed germination signicantly increased with burial time despite the opposite pattern of monthly rainfall observed during the same period. From a total seed loss of 85% at the end of the study in December, we found that 70% of soil seed loss was explained by seed germination and that almost 15% was presumably accounted for by granivory. Seed loss outside burial bags (germination plus seed predation) was higher in B. retama undercanopy and annual plant debris soils, whereas germination was undistinguishable among patch types. These results suggest a higher incidence of factors other than germination, explaining seed depletion under shrub canopies and in microsites by, for example, seed predation. It is generally accepted that seeds under vegetation patches in deserts can support higher granivory rates than bare soils as a result of both higher seed availability (Nelson and Chew, 1997; Price and Joyner, 1997; Wilby and Shachak, 2000) and lower predatory risk (Bowers, 1990; Brown, 1988). However, in order to fully understand the mechanisms explaining post-dispersal seed fate, it is necessary to include spatial seed redistribution (Chambers and MacMahon, 1994). For example, we observed that seed density decreases with time in both undercanopy and plant debris microsites, but it slightly increases in interpatches, suggesting the existence of a spatial redistribution of seeds among patches during Phase II dispersal. The potential germination rate of seeds collected directly from mother plants was less than 25% but increased with burial time to more than 75%, suggesting the presence of physical or morphological seed dormancy mechanisms (Allen and Meyer, 1998; Baskin and Baskin, 1998; Meyer and Pendleton, 2005). This fact reinforces our ndings about delayed seed germination in the eld. Moreover, laboratory experiments also evidenced a faster germination response in seeds buried over a longer period of time and, as we recently observed (unpublished data), nearly 85% of the seeds can germinate after 4 years of room storage. Together, these results suggest that seeds from previous years may respond faster to the sudden presence of available water than currently produced seeds, creating more opportunities for plant recruitment. Our results show that an important proportion of the current seed production is lost to pre- and post-dispersal seedeaters and by seed germination, impoverishing soil seed reserves. The currently produced B. retama seeds can germinate at any moment from March to December (cool season), but higher germination rates may be expected after a longer period of soil seed burial coinciding

Fig. 6. Potential seed germination (%) of seeds collected from different sources (N15) incubated for 12 days under laboratory conditions: (a) cumulative seed germination after 30 days incubation; (b) seed germination dynamics of seeds collected from mother plants (black), soil seed bank 75 days after seed rain completion (SB 75, dark grey), soil seed bank 171 days after seed rain completion (SB 171, light grey), and soil seed bank 276 days after seed rain completion (SB 276, white). Different letters indicate signicant differences (LSD; P<0.05). Box: interquartile range containing 100% of data, line across box: median, square dot: mean.

the time during which seeds are exposed to post-dispersal consumers, increasing the probability of seed germination and seedling establishment after unpredictable rain pulses, as previously described for several annual herbs and grasses (Gutterman, 1972, 2002). At the end of the seed dispersal stage, soil seed density showed a marked spatial pattern with maximum values under B. retama shrubs (>1000 seeds m2), medium values in buried annual plant litter microsites (527 seeds m2), and minimum values on bare soils (49 seeds m2). Moreover, soil seed density signicantly decreased after 138 and 283 days, showing a total seed reserve depletion of almost 85% within a 6-month period, suggesting that the remaining 15% may contribute to the persistent fraction of the soil seed reserves. Most dominant woody perennials in desert and semi-desert areas lack a seed bank or in some cases possess a transient seed bank (Chambers and MacMahon, 1994; Kemp, 1989; Owens et al., 1995). Similar results have been observed for other woody domi nant species from the Monte desert at Nacunan (Marone et al.,

Author's personal copy

20

Y. Ribas-Fernandez et al. / Journal of Arid Environments 73 (2009) 1421 Guo, Q., Rundel, P.W., Goodall, D.W., 1998. Horizontal and vertical distribution of desert seed banks: patterns, causes, and implications. Journal of Arid Environments 38, 465478. Guo, Q., Rundel, P.W., Goodall, D.W., 1999. Structure of desert seed banks: comparisons across four North American desert sites. Journal of Arid Environments 42, 114. Gutterman, Y., 1972. Delayed seed dispersal and rapid germination as survival mechanisms of the desert plant Blepharis persica (Burm.) Kuntze. Oecologia 10, 145149. Gutterman, Y., 2002. Survival Strategies of Annual Desert Plants. Springer, Berlin. Harper, J.L., 1977. Population Biology of Plants. Academic Press, New York. Herrera, C., 1995. Plant-vertebrate seed dispersal systems in the Mediterranean: ecological, evolutionary, and historical determinants. Annual Review of Ecology and Systematics 26, 705727. Horton, J.L., Hart, S.C., 1998. Hydraulic lift: a potentially important ecosystem process. Trends in Ecology and Evolution 13, 232235. Hulme, P.E., 1997. Post-dispersal seed predation and the establishment of vertebrate dispersed plants in Mediterranean scrublands. Oecologia 111, 9198. Hulme, P.E., 1998. Post-dispersal seed predation: consequences for plant demography and evolution. Perspectives in Plant Ecology, Evolution and Systematics 1, 3246. Hultine, K.R., Scott, R.L., Cable, W.L., Goodrich, D.C., Williams, D.G., 2004. Hydraulic redistribution by a dominant, warm-desert phreatophyte: seasonal patterns and response to precipitation pulses. Functional Ecology 18, 530538. Kelt, D.A., Meserve, P.L., Forister, M.L., Nabors, L.K., Gutierrez, J.R., 2004. Seed predation by birds and small mammals in semiarid Chile. Oikos 104, 133141. Kemp, P.R., 1989. Seed banks and vegetation processes in deserts. In: Leck, M.A., Parker, V.T., Simpson, R.L. (Eds.), Ecology of Soil Seed Banks. Academic Press, San Diego, pp. 257281. Krop, A.I., Cecchi, G.A., Villasuso, N.M., Distel, R.A., 2002. The inuence of Larrea divaricata on soil moisture and on water status and growth of Stipa tenuis in southern Argentina. Journal of Arid Environments 52, 2935. Lonsdale, W.M., 1993. Losses from the seed bank of Mimosa pigra: soil microorganisms vs. temperature uctuations. Journal of Applied Ecology 30, 654 660. Marone, L., Horno, M.E., 1997. Seed reserves in the central Monte Desert, Argentina: implications for granivory. Journal of Arid Environments 36, 661670. Marone, L., Rossi, B.E., Horno, M.E., 1998. Timing and spatial patterning of seed dispersal and redistribution in a South American warm desert. Plant Ecology 137, 143150. Marone, L., Horno, M.E., Gonzalez del Solar, R., 2000. Post-dispersal fate of seeds in the Monte desert of Argentina: patterns of germination in successive wet and dry years. Journal of Ecology 88, 940949. Meney, K.A., Nielssen, G.M., Dixon, K.W., 1994. Seed bank patterns in Restionaceae and Epacridaceae after wildre in kwongan in southwestern Australia. Journal of Vegetation Science 5, 512. Meyer, S.E., Pendleton, B.K., 2005. Factors affecting seed germination and seedling establishment of a long-lived desert shrub (Coleogyne ramosissima: Rosaceae). Plant Ecology 178, 171187. Milton, S.J., Dean, W.R.J., 2001. Seeds dispersed in dung of insectivores and herbivores in semi-arid southern Africa. Journal of Arid Environments 47, 465483. Morello, J., 1958. La Provincia Fitogeograca del Monte. Opera Lilloana 2, 5115. Musil, C.F., 1991. Seed bank dynamics in sand plain lowland fynbos. South African Journal of Botany 57, 131142. Nathan, R., Muller-Landau, H.C., 2003. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology and Evolution 15, 278285. Nelson, J.F., Chew, R.M., 1997. Factors affecting seed reserves in the soil of a Mojave Desert ecosystem, Rock Valley, Nye County, Nevada. American Midland Naturalist 97, 300320. Norusis, M.J., 1992. SPSS for Windows. Advanced Statistic Release 5. SPSS Inc., Chicago. Ojeda, R.A., Campos, C.M., Gonnet, J.M., Borghi, C.E., Roig, V.G., 1998. The MaB reserve of Nacunan, Argentina: its role in understanding the Monte Desert biome. Journal of Arid Environments 39, 299313. Owens, M.K., Wallace, R.B., Archer, S., 1995. Seed dormancy and persistence of Acacia berlandieri and Leucaena pulverulenta in a semi-arid environment. Journal of Arid Environments 29, 1523. Palacios, R.A., Hunziker, J.H., 1984. Revision taxonomica del genero Bulnesia (Zygophyllaceae). Darwiniana 25, 299320. Price, M.V., Joyner, J.W., 1997. What resources are available to desert granivores: seed rain or soil seed bank? Ecology 78, 764773. Pucheta, E., Llanos, M., Meglioli, C., Gaviorno, M., Ruiz, M., Parera, C., 2006. Litter decomposition in a sandy Monte desert of western Argentina: inuences of vegetation patches and summer rainfall. Austral Ecology 31, 808816. Pugnaire, F.I., Lazaro, R., 2000. Seed bank and understorey species composition in a semi-arid environment: the effect of shrub age and rainfall. Annals of Botany 86, 807813. Radford, I.J., Nicholas, D.M., Brown, J.H., Kritikos, D.J., 2001. Paddock-scale patterns of seed production and dispersal in the invasive shrub Acacia nilotica (Mimosaceae) in northern Australian rangelands. Austral Ecology 26, 338348. Reynolds, J.F., Virginia, R.A., Kemp, P.R., de Soyza, A.G., Tremmel, D.C., 1999. Impact of drought on desert shrubs: effects of seasonality and degree of resource island development. Ecological Monographs 69, 69106. Schlesinger, W.H., Pilmanis, A.M., 1998. Plantsoil interactions in deserts. Biogeochemistry 42, 169187.

with the beginning of the warm, humid season. The decrease in soil seed density and delay in seed germination evidenced throughout the year suggest that B. retama seeds may show similar germination events at any moment of the year, whenever soil water is available. Acknowledgements This study was partially funded by grants 21 E/358 and 21 E/629 (CICITCA, National University of San Juan) accorded to E.P. Climatic and precipitation data were kindly provided by Fuerza Aerea Argentina. EEA INTA San Juan and INSEMI supplied laboratory facilities for germination experiments. We gratefully acknowledge the participation of M. Hadad, M. Ontivero, V. Moreno, M. Almiron and M. Ariza in the eldwork. Guillermo Funes made important comments on the manuscript. References
Aguiar, M.R., Sala, O.E., 1999. Patch structure, dynamics and implications for the functioning of arid ecosystems. Trends in Ecology and Evolution 14, 273277. Allen, P.S., Meyer, S.E., 1998. Ecological aspects of seed dormancy loss. Seed Science Research 8, 183191. Armesto, J.J., Rozzi, R., 1989. Seed dispersal syndromes in the rain forest of Chiloe: evidence for the importance of biotic dispersal in a temperate rain forest. Journal of Biogeography 16, 219226. Auld, T.D., 1995. Soil seed bank patterns of four trees and shrubs from arid Australia. Journal of Arid Environments 29, 3345. Aziz, S., Khan, M.A., 1996. Seed bank dynamics of a semi-arid coastal shrub community in Pakistan. Journal of Arid Environments 34, 8187. Baskin, C.C., Baskin, J.M., 1998. Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination. Academic Press, San Diego. Bertiller, M.B., 1998. Spatial patterns of the germinable soil seed bank in northern Patagonia. Seed Science Research 8, 3945. Bowers, M.A., 1990. Exploitation of seed aggregates by Merriams kangaroo rat: harvesting rates and predatory risk. Ecology 71, 23342344. Brown, J.S., 1988. Patch use as an indicator of habitat preference, predation risk, and competition. Behavioral Ecology and Sociobiology 22, 3747. Bullock, J.M., Moy, I.L., 2004. Plants as seed traps: inter-specic interference with dispersal. Acta Oecologica 25, 3541. Calvo-Irabien, L.M., Islas-Luna, A., 1999. Predispersal predation of an understory rainforest herb Aphelandra aurantiaca (Acanthaceae) in gaps and mature forest. American Journal of Botany 86, 11081113. Campos, C., Ojeda, R.A., 1997. Dispersal and germination of Prosopis exuosa (Fabaceae) seeds by desert mammals in Argentina. Journal of Arid Environments 35, 707714. Castro, J., Gomez, J.M., Garca, D., Zamora, R., Hodar, J.A., 1999. Seed predation and dispersal in relict Scots pine forests in southern Spain. Plant Ecology 145, 115 123. Chambers, J.C., MacMahon, J.A., 1994. A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annual Review of Ecology and Systematics 25, 263292. Debandi, G., Rossi, B.E., Aranbar, J., Ambrosetti, J.A., Peralta, I.E., 2002. Breeding system of Bulnesia retama (Gillies ex Hook & Arn.) Gris. (Zygophyllaceae) in the Central Monte Desert (Mendoza, Argentina). Journal of Arid Environments 51, 141152. Debisnki, D.M., Ray, C., Saveraid, E.H., 2001. Species diversity and the scale of the landscape mosaic: do scales of movement and patch size affect diversity? Biological Conservation 98, 179190. De Fina, A.L., 1992. Aptitud Agroclimatica de la Republica Argentina. Academia Nacional de Agronoma y Veterinaria, Buenos Aires, Argentina. Ehleringer, J.R., Phillips, S.L., Schuster, W.S.F., Sandquist, D.R., 1991. Differential utilization of summer rains by desert plants. Oecologia 88, 430434. Fernandez, R.J., 2007. On the frequent lack of response of plants to rainfall events in arid areas. Journal of Arid Environments 68, 688691. Figueroa, J.A., Jaksic, F.M., 2004. Seed bank and dormancy in plants of the Mediterranean region of central Chile. Revista Chilena de Historia Natural 77, 201215. Figueroa, J.A., Munoz, A.A., Mella, J.E., Arroyo, M.T.K., 2002. Pre- and post-dispersal seed predation in a mediterranean-type climate montane sclerophyllous forest in central Chile. Austral Journal of Botany 50, 183195. Figueroa, J.A., Teillier, S., Jaksic, F.M., 2004. Composition, size and dynamics of the seed bank in a mediterranean shrubland of Chile. Austral Ecology 29, 574584. Garca-Fayos, P., Verdu, M., 1998. Soil seed bank, factors controlling germination and establishment of a Mediterranean shrub: Pistacia lentiscus L. Acta Oecologica 19, 357366. Giannoni, S.M., Dacar, M., Taraborelli, P., Borghi, C.E., 2001. Seed hoarding by rodents of the Monte Desert, Argentina. Austral Ecology 26, 259263. Grundy, A.C., Mead, A., Burston, S., 1999. Modelling the effect of cultivation on seed movement with application to the prediction of weed seedling emergence. Journal of Applied Ecology 36, 663678.

Author's personal copy

Y. Ribas-Fernandez et al. / Journal of Arid Environments 73 (2009) 1421 Solbrig, O.T., Yang, T.W., 1977. The strategies and community patterns of desert plants: strategies in relation to timing of blooming and fruiting. In: Orians, G.H., Solbrig, O.T. (Eds.), Convergent Evolution in Warm Deserts. Hutchinson & Ross Inc., New York, pp. 8390. Torres, R., Squeo, F.A., Jorquera, C., Aguirre, E., Ehleringer, J.R., 2002. Evaluacion de la capacidad estacional de utilizar eventos de precipitacion en tres especies de arbustos nativos de Chile con distintos sistemas radiculares. Revista Chilena de Historia Natural 75, 737749. van Klinken, R.D., 2005. Total annual seed loss on a perennial legume through predation by insects: the importance of within-season seed and seed feeder dynamics. Austral Ecology 30, 414425. Van Mourik, T.A., Stomph, T.J., Murdoch, A.J., 2005. Why high seed densities within buried mesh bags may overestimate depletion rates of soil seed banks. Journal of Applied Ecology 42, 299305. Villagra, P.E., Marone, L., Cony, M.A., 2002. Mechanisms affecting the fate of Prosopis exuosa (Fabaceae, Mimosoideae) seeds during early secondary dispersal in the Monte Desert, Argentina. Austral Ecology 27, 416421. Wang, B.C., Smith, T.B., 2002. Closing the seed dispersal loop. Trends in Ecology and Evolution 17, 379385.

21

Weppler, T., Stocklin, J., 2006. Does pre-dispersal seed predation limit reproduction and population growth in the alpine clonal plant Geum reptans? Plant Ecology 187, 277287. Wilby, A., Shachak, M., 2000. Harvester ant response to spatial and temporal heterogeneity in seed availability: pattern in the process of granivory. Oecologia 125, 495503. Willson, M., Traveset, A., 2000. The ecology of seed dispersal. In: Fenner, M. (Ed.), Seeds: The Ecology of Regeneration in Plant Communities. CAB International, Wallingford, UK, pp. 85110. Zaady, E., Groffman, P.M., Shachak, M., 1998. Nitrogen xation in macro- and microphytic patches in the Negev Desert. Soil Biology and Biochemistry 30, 449454. Zuloaga, F.O., Morrone, O., 1996. Catalogo de las Plantas Vasculares de la Republica Argentina I. Pteridophyta, Gymnosperamae y Angiospermae (Monocotyledoneae). Missouri Botanical Garden Press, St. Louis, MO. Zuloaga, F.O., Morrone, O., 1999. Catalogo de las Plantas Vasculares de la Republica Argentina II. Dicotyledoneae. Missouri Botanical Garden Press, St. Louis, MO. Zuloaga, F.O., Morrone, O., 2007. Catalogo de las Plantas Vasculares de la Republica Argentina. Instituto Darwinion. <http://www.darwin.edu.ar/Publicaciones/ CatalogoVascII/CatalogoVascII.asp>.