Condiciones y forma de pago. (55 fracción III inciso e) de la Ley)

A resilient seed bank should include seed densities typical of the system, several species from several guilds, and a high proportion of native species. On the other hand, degraded seed banks have altered densities of seeds, few species or guilds and a high proportion of exotic invasive

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species (Frieswyk & Zedler 2006). Both invaded seed banks showed signs of severe degradation, being largely dominated by a few species (Bossuyt & Honnay 2008), namely exotic/invasive species. The exotics Conyza spp. and Gamochaeta pensylvanica, both short-lived species, clearly dominated the seed bank of recently invaded areas, despite not being particularly abundant in the extant vegetation (Marchante et al. 2004), while the long-invaded seed bank was dominated by the perennial A. longifolia accompanied by a few seeds of Carpobrotus edulis, also perennial. The higher longevity of the exotic/invasive species present in the seed banks of long-invaded areas indicates a more long lasting threat to these areas. Seeds of Acacia species, in particular, are known to have very high longevity (Cavanagh 1980; Daws et al. 2007), waiting in the soil for suitable conditions to germinate. On the other hand, the natural seed bank of non-invaded areas were more resilient, having a higher diversity of guilds, low abundances of exotic/invasive species and high proportions of native species, even though only a small proportion were dune specialists. However, the presence of A. longifolia seeds in areas not yet invaded showed that there is a risk of future invasion, especially after a fire event.

When subject to disturbance, seed bank densities of plant communities may show distinct changes, either increasing or decreasing (Pierce & Cowling 1991). In any case, the density of seeds in degraded communities is frequently distinct from that of corresponding unaltered communities (Frieswyk & Zedler 2006), which is corroborated by this study: both the decrease in the density of seeds in long-invaded areas and the increase in total seed density in recently invaded areas (mostly due to the exotic annuals referred to above) (Appendix 4.2) indicates degradation.

Measures of species richness, diversity, attributes of some plant traits, amount of A. longifolia seeds and similarity to non-invaded areas indicate that seed banks in long-invaded areas are more altered than those of recently invaded areas. For instance, Caryophyllaceae were absent and Poaceae were underrepresented in long-invaded seed banks, while both taxa were still well represented in recently invaded and non-invaded seed banks. The discrepancy could be due to the short-lived seeds which characterise several species of both these families. Studies have shown that Cerastium diffusum (Caryophyllaceae) (Mack 1976) and Vulpia fasciculata (Poaceae) (Watkinson 1978) do not accumulate long-lived soil seed banks in dunes. Long-invaded areas are therefore more impoverished of native species and are more likely to be reinvaded following manual clearing or fire. Similar trends have been found in areas invaded by other Acacia species in South Africa (Holmes & Cowling 1997a; Holmes 2002), although invasion ages were not always monitored in those studies. In long-invaded areas, where A. longifolia had been present continuously for at least 20 years, the dense canopy and the thick litter layer has at least curtailed, if not prevented, the deposition of seeds

105 from surrounding areas (e.g. from zoochorous species), as happens in other closed forest systems (Sayer 2006). Zoochorous plant species do not seem to cope well with A. longifolia invasion (Holmes & Cowling 1997b), being underrepresented in invaded areas while remaining frequent in non- invaded areas. In the recently invaded areas, movement of seeds (particularly from anemochorous species) into the area continued because the canopy of A. longifolia was more open (ca. 70%) and the litter layer was more sparse (1.43 ± 0.14 Kg.m-2_{) than in the long-invaded areas (at least 80%} A. longifolia cover and 2.05 ± 0.24 Kg.m-2 _{of litter). The time of invasion would also affect seed bank} traits because the viability of seeds (particularly small seeds) buried for long periods under thick litter layers diminishes (Eckstein & Donath 2005) along with the ability of viable seeds to germinate successfully in thick litter layers (Facelli & Pickett 1991). Noticeably, however, some dune -specific species, e.g. Antirrhinum majus L. cirrhigerum (Ficalho) Franco, with larger and longer-lived seeds (Shah et al. 2008) seem to have either overcome the barriers to immigration into thickets or survived the protracted periods of invasion, being exclusively detected (despite rarely) in long-invaded areas. Their absence in recently invaded areas could be due to the seeds being destroyed by the fire of 1995 and there not being enough time between the fire and sample acquisition for fresh seeds to spread into and accumulate in the invaded patches.

The high proportion of therophytes in the seed banks was expected as their establishment from seed is obligatory (Fenner & Thompson 2005), they are frequent in Portuguese dune ecosystems (Alves et al. 1998; Costa et al. 2000) and include many ‘opportunistic’ species, despite having limited conservation value (some are exotics). Being short-lived annual species that are relatively small, they are largely unable to compete with A. longifolia which is a large perennial species. Nevertheless, if therophytes create a dense cover over the soil surface, they may reduce germination of A. longifolia seeds and provide a transitional cover which will later be replaced by the less-numerous native perennial species in the seed bank. The seeds of perennial species are usually sparse in seed banks and these plants frequently have an ability to propagate from perennating buds located on storage structures as an alternative mean of reproduction (Sternberg et al. 2003). Some natural sand dunes lack persistent seed banks because conditions that induce dormancy (namely poorly aerated soils) are not always met (Owen et al. 2001). Additionally, recruitment of new individuals may have been limited (Thompson & Ceriani 2003) because some species require heat (Buhk & Hensen 2005), smoke (Reyes & Trabaud 2009), passage through animal intestines (Calviño-Cancela 2004) or other cues to induce germination and facilitate seedling emergence (Sternberg et al. 2003; Cottrell 2004). The lack of these types of cues in the glasshouse

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could partially explain why ca. 15% of the seedlings in this study (potentially some perennial species) did not survive to a stage where they could be identified.

Nevertheless, the lack of nanophanerophytes and chamaephytes (long-lived perennials, with many species characteristic of dunes, some with high conservation value), such as Corema album (L.) D. Don and Cytisus grandiflorus (Brot.) DC. (both endemic of the Iberian Peninsula), Herniaria ciliolata Melderis subsp. robusta Chaudhri and Iberis procumbens Lange subsp. procumbens (both endemic in Europe), Crucianela maritima L. and Helichrysum italicum (Roth) G. Don fil. subsp. picardi (Costa et al. 2000; Marchante et al. 2004; Silva 2006), and the very low numbers of other species, including Cistus salvifolius L. and Ulex europaeus L. subsp. latebracteatus (Mariz) Rothm, could also be an indication of a general degradation of seed banks in the studied dunes. Sampling size could also have contributed to the low levels of detection of these species. The deficiency of dune specialists, particularly in non-invaded areas, may be due to the fact that the selected non-invaded areas were not the most “typical” dune system, but rather the only places in the reserve that were located in dune situations that were equivalent to the invaded areas while being free of A. longifolia trees. In these areas graminoid species frequently predominate and apparently largely suppress germination of A. longifolia seeds. The graminoid species that were present (Juncus spp. and Carex arenaria L.) are frequently associated with relatively moist soils, which were also characteristic of some of the long-invaded areas where A. longifolia dominated. Species of Juncus and Carex produce very large amounts of small, long-lived seeds that are abundant in several communities (Bossuyt & Honnay 2008). The presence of these taxa may explain the higher density of seeds when compared to seed banks of other sand dunes systems (7-12 germinable seeds.m-2_{) (Owen et al. 2001).}

Bossuyt & Honnay (2008) analysed numerous community seed banks and support the notion that restoration from natural seed bank is only possible in areas degraded for less than five years. Our study corroborates this, at least partially, showing a decrease in the unaided recovery potential of the system as invasion age increases. Other studies in the SJDNR have shown that other parameters, namely microbiological and chemical properties of the soil in long-invaded stands of A. longifolia are also more altered and take more time to recover than in recently invaded stands (Marchante et al. 2009).