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Keywords:

  • ecosystem resilience;
  • experimental litter removal;
  • Fabaceae/Leguminosae/Mimosaceae;
  • invasion time;
  • long-leafed wattle;
  • long-term monitoring post-clearing;
  • reinvasion post-clearing

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Supporting Information

1. Invasive plants destroy the structure and function of many ecosystems but removal is expensive, so the likelihood of success should be assessed before a major control programme commences. Trial clearings can clarify how best to design and perform broad-scale clearing programmes. Such trials need to consider the range of conditions that might affect the outcome of control operations, not least the duration of invasion before clearing commences, a parameter that has rarely been considered previously.

2. The recovery of plant communities was monitored over 6 years in a Portuguese coastal dune system after the removal of invasive Acacia longifolia plants, together with the underlying litter in half of the cleared areas but not in the remainder. Areas that had been invaded for >20 years (long-invaded) as opposed to <7 years (recently invaded) were compared.

3. After the removal of A. longifolia, recently invaded areas had more exotic plant species but also higher native species richness, plant cover, initial diversity and species turnover rates than long-invaded areas. Generalist native species were initially very abundant in cleared areas but progressively gave way to species more typical of dunes. Six years after clearing, many species that usually occur on dunes were still missing. Therophytes were the most abundant life form immediately after clearing, but nanophanerophytes, chamaephytes and A. longifolia increased with time. Seedlings of A. longifolia were most abundant in long-invaded areas, but litter removal along with plants promoted increased plant species richness and cover and decreased susceptibility to reinvasion.

4.Synthesis and applications. A number of variables can affect the outcome of clearing invasive plant species. For A. longifolia on Portuguese dunes, recently invaded areas should be prioritized and thick litter layers should be removed along with the invader. Even so, recovery of native flora was not complete in this study, and other management actions are needed to supplement clearing operations, for example propagation of native species or prescribed fires to deplete the invasive species seed bank. Although complete restoration of the ecosystem will almost always be impossible, it should be possible in the long term to create an ecosystem with a structure and function that resembles the original habitat.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Supporting Information

Invasive species are considered one of the primary threats to biodiversity (Millennium Ecosystem Assessment 2005) as well as to the integrity and functioning of ecosystems (Hulme 2007), making their removal a necessity in order to protect and restore natural habitats. Before embarking on expensive restoration programmes, the probability of success should be assessed, including both the prospects of reinvasion and the extent to which native plant species will recolonize cleared areas (Zavaleta, Hobbs & Mooney 2001; Reid et al. 2009). Long-term monitoring after control can provide valuable ecological information by revealing how changes in the abundance of species influence the properties and processes of ecosystems, which in turn helps to guide management decisions (Blossey 1999). Although some studies have confirmed the benefits of median to long-term post-clearing assessments on the recovery of native plants (Holmes 2001a), most studies on the effects of invasive plant removal are too truncated to provide meaningful results and/or frequently fail to include the effects of clearing on native plant species (Ogden & Rejmanek 2005; Hejda & Pyšek 2006).

Despite having a high priority for conservation (Habitats Directive 92/43/EEC), dune ecosystems around the world are severely threatened by invasive species, e.g. Chrysanthemoides monilifera subsp. rotundata in Australia (Ens & French 2008), Acacia cyclops in South Africa (Henderson 2001) and Ammophila arenaria in California (Beckstead & Parker 2003). The Portuguese coast is no exception. Pristine dune systems are becoming increasingly rare with native plant species being replaced by several invasive exotic species, including Acacia longifolia (Andrews) Willd (long-leafed wattle) (Fabaceae). This species is the most widespread invader in Portuguese dunes and was introduced early in the 20th century to curb sand erosion (Neto 1993). Besides deliberate planting, its abundance and distribution have increased greatly following fire events (Marchante, Marchante & Freitas 2003) with major impacts on species richness, traits diversity and soil ecology, which escalate with time (Marchante et al. 2008a; H. Marchante, H. Freitas & J.H. Hoffmann, unpublished data). Acacia longifolia, like other Acacia species, is a nitrogen-fixing tree that produces large quantities of slowly decomposing litter, which accumulates in thick layers (Marchante et al. 2008a) beneath the canopy of almost mono-specific, dense stands in dunes, which are otherwise litter-deprived.

Plant litter and its decomposition are considered a vital part of ecosystem functioning, increasingly influencing vegetation structure as litter accumulates (Xiong & Nilsson 1999). In general, litter suppresses the germination of small seeds and seedling establishment, while germination of large seeds and seedling establishment are facilitated. The potential for the major disruption of ecosystems is most evident when invasive plant species that produce large quantities of litter invade ecosystems that naturally have less litter. In such cases, an abnormal accumulation of organic matter persists because there is inappropriate soil fauna and microbiota to decompose it properly (Sayer 2006).

Considering that plant communities are dynamic through time, evaluation of recovery of ecosystems after removal of invasive plants requires median to long-term monitoring. Nevertheless, most studies have been too short to provide meaningful results (Maron & Jefferies 2001; Ogden & Rejmanek 2005; Hejda & Pyšek 2006). Although there are studies that consider the duration of invasion prior to clearing (Holmes & Cowling 1997a,b; Holmes 2002), they are scarce (Strayer et al. 2006). Against this background, we carried out a study to evaluate the recovery of native and exotic plant species over a 6-year period in a coastal dune ecosystem that has been dominated by A. longifolia for different durations. We predicted that the resilience of native communities would decrease as invasion time increased and that removal of litter along with the invader would facilitate recovery of native plant communities. The experiment was established in order to test management solutions and offer concrete recommendations to managers.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Supporting Information

Study Site

The study area was located in the São Jacinto Dunes Nature Reserve (SJDNR), which is located on the central-northern coast of Portugal (40°39′N, 8°44′W). SJDNR covers about 660 ha and is bordered by the Atlantic Ocean to the west and by the Ria de Aveiro estuary to the east. The climate is Mediterranean with Atlantic influence. Historically, the area supported open vegetation characterized by several communities dominated by shrub and herb species and sporadic small trees (Neto 1993).

Acacia longifolia, which was introduced into SJDNR from early in the 20th century to the 1940s to curb movement of sand (Neto 1993), has subsequently proliferated and extensively invaded much of the reserve, particularly triggered by fire events (Marchante et al. 2008a). When this study took place, A. longifolia was dominant over 150 ha and occurred in mixed association with other plant species over 200 ha (Guimarães 2004). Carpobrotus edulis (L.) N. E. Br. and Cortaderia selloana (Schultes) Asch. & Graebner were also invasive in the area but to a lesser extent. Invaded areas in SJDNR can be divided into long-invaded and recently invaded stands. When the study started, there had been dense stands of A. longifolia continuously for more than 20 years in long-invaded areas. The recently invaded areas came about when A. longifolia proliferated over a large area after a natural fire that destroyed about 200 ha of vegetation during the 1995 summer (Silva 1997). These areas had been invaded for <7 years when the study began. Before the fire, the burnt areas were considered not to be invaded as there were only a few scattered individuals of A. longifolia (<5% cover), mostly in the understorey of Pinus pinaster Aiton. The mono-specific, arboreal stands of A. longifolia have caused significant changes in community structure (Marchante, Marchante & Freitas 2003) and ecosystem functioning (Marchante et al. 2008a,b), including deposition of large quantities of leaf litter (Marchante et al. 2008a) and reduction in light at soil level.

Experimental Design

In each of the two invaded areas (long- and recently invaded), a complete randomized block design was used to define five replicated blocks, each including three 100-m2 plots with similar levels of A. longifolia cover. One of three treatments was randomly assigned to one plot in each block: (i) plots cleared of A. longifolia (AR) by cutting the trees with chainsaws at ground level; (ii) plots where A. longifolia trees were removed and the litter layer was also removed (ALR); and (iii) plots with both A. longifolia and litter left intact as untreated controls (A). After treatments had been applied, in October 2002, the conditions in the cleared plots (AR and ALR) were distinctly different from those of untreated plots (A, Table 1); before the treatments, all blocks had conditions similar to the untreated plots (A). Two 2 × 10 m parallel transects, separated by a 2-m gap, were demarcated in each plot. Transects were monitored twice a year (late January/early February and May), from December 2002 to May 2004, and then once every 2 years until May 2008. Plant species present, species cover, number of A. longifolia seedlings and soil litter coverage were measured along each transect.

Table 1.   Characterization of Acacia longifolia cover, leaf litter accumulated and light intensity at soil level (mean ±SE) in areas long- and recently invaded by Acacia longifolia: AR –A. longifolia removed, ALR – both A. longifolia and litter layer removed, and A –A. longifolia maintained. Characterization of undisturbed plots (A) corresponds to conditions observed in all the plots pre-establishment
 AARALR
  1. *After treatment establishment, leaf litter was similar in A and AR; data from Marchante et al. (2008a).

  2. After treatment establishment, light intensity was similar in AR and ALR.

A. longifolia cover (%)Recently invaded±700.00.0
Long-invaded>800.00.0
Leaf litter* (kg m−2)Recently invaded1·43 ± 0·140·0
Long-invaded2·05 ± 0·240·0
Light intensity† (at soil level) (ųmol m−2 S−1)Recently invaded283·6 ± 9·51093·5 ± 19·6
Long-invaded170·2 ± 6·31061·1 ± 11·4

Data Analysis

Recovery of plant communities post-clearing

It was first characterized using measures of species richness, plant cover, Shannon diversity and evenness. Acacia  longifolia was the potential driver of change in the plant community; therefore, it was excluded from the analysis of species richness and plant cover. Pielou evenness index J (from 0 to 1) and Shannon diversity index H’ (from 0 to ≈5, but usually found to fall between 1·5 and 3·5) calculations included A. longifolia as these indexes reflect the presence of a dominant species (Magurran 1988). All parameters were analysed by repeated-measures manova with time post-clearing as a within-subject factor and invasion status and treatment as between-groups factors.

Species traits and species turnover rate in plant communities post-clearing

The species were categorized into biological and ecological attributes, which were classified under traits (Table 2). For each treatment, the area covered by species with a particular attribute was summed and divided by the total area covered by all the species within the trait, to produce a relative abundance of each attribute per treatment. Acacia  longifolia was treated separately.

Table 2.   Plant traits and their respective attributes used to classify the species recorded in the study plots
Plant traitsAttribute descriptionSource
  1. 1 = Field observations; 2 = (Franco & Afonso 1971–2003).

  2. *In species with more than one attribute, the attribute dominant in the studied system was considered.

Biological trait: Raunkaier life forms*Therophyte (annual herbs which survive the unfavourable season as seeds)1, 2
Geophyte (herbs with perennating buds below soil surface)
Hemicryptophyte (herbs with perennating buds at soil level)
Chamaephyte (herbs or woody plants with perennating buds above soil level but below 25 cm)
Nanophanerophyte (shrubs between 25 cm and 2 m)
Microphanerophyte (trees and shrubs between 2 and 8 m)
Ecological trait: Biogeographic distributionExotic & invasive (species introduced in Portugal that become invasive)2
Native & generalist (native species that occur in several different habitats)
Native & dune specialist (native species that are typical from dunes)
Native & dune/generalist (species that occur in both dunes and other sandy soils)

Species turnover rate (TR) was calculated to measure species shifts between May 2003 and 2008, as follows: TR = 0·5 (L + G), where L is the number of species lost and G is the number of species gained during this period (Hilli, Kuitunen & Suhonen 2007). TR differences were analysed with a two-way factorial anova. The time interval represents the changes observed in the full study period, with measurements made each year in the same season being compared to avoid seasonal effects as a source of discrepancy.

Susceptibility to (re)invasion post-clearing

It was based on: (i) the number of A. longifolia seedlings and (ii) A. longifolia cover (saplings and trees), which were analysed by repeated-measures manova with time post-clearing as a within-subject factor and invasion status and treatment as between-groups factors.

In all analyses, mean differences were separated with least squares difference test at 5% level of significance. statistica 6·0 (StatSoft, Inc., 2001, http://www.statsoft.com) was used.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Supporting Information

Recovery of Plant Communities Post-clearing

Over the 6-year period, 83 plant species in 26 families were identified in the survey plots: six were exotics and 77 natives. There were 77 species in recently invaded areas as opposed to 56 species in long-invaded areas, several being unique to each area. More species were found in plots where both A. longifolia and litter were removed (ALR) (74 and 49 in recently and long-invaded plots, respectively) than in areas where only A. longifolia was removed (AR) (64 and 48 in recently and long-invaded plots, respectively). In untreated areas (A), there was approximately half as many species (36 and 26 in recently and long-invaded plots, respectively) as in the cleared areas (Appendix S1 Supporting Information).

A significant interaction between invasion age, clearing treatments and time post-clearing for species cover (F12,60 = 10·82, P < 0·0001) and species richness (F12,60 = 2·67, P = 0·006) was found. In the first two months after clearing, neither plant cover (Fig. 1) nor species richness (Fig. 2) showed clear patterns of change, with some exceptions, e.g. by December 2002, in plots in recently invaded areas where only A. longifolia had been removed (AR), species richness was higher than in all the other plots. There was a significant increase in species cover (Fig. 1) and richness (Fig. 2) in both cleared plots (AR and ALR), which ranged from ca. 20% cover and four species immediately after clearing to more than 80% cover and 12 species by May 2006. Generally, in untreated plots (A), plant cover was sparser and species richness was lower than in cleared plots (AR and ALR) of both invaded areas; both parameters showed little change over time. Plant cover was lower in long-invaded areas compared with recently invaded areas. With time, plant cover in plots where the litter layer was removed (ALR) became significantly higher than in plots where the litter layer was left intact (AR). On the last sampling, there was a significant reduction in plant cover across all cleared plots (Fig. 1).

image

Figure 1.  Changes in plant cover (mean + SE; n = 10) over time after clearing treatments in areas long-invaded and recently invaded by Acacia longifolia: AR –A. longifolia removed, ALR – both A. longifolia and litter layer removed and A –A. longifolia maintained. Different letters above bars indicate significant differences at < 0·05 (least squares difference test).

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image

Figure 2.  Changes in species richness (mean + SE; n = 10) over time after clearing treatments in areas long-invaded and recently invaded by Acacia longifolia. Abbreviations and statistical letters as for Fig. 1.

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After clearing, regardless of litter removal (ALR) or not (AR), fewer species appeared in long-invaded areas than in recently invaded areas (Fig. 2). In long-invaded areas, species richness was higher in plots where the litter was removed (ALR) than in plots where it was left (AR). In recently invaded areas, the species richness was generally similar under the two clearing treatments.

Shannon’s diversity and Pielou’s evenness were significantly lower in untreated plots (A) than in cleared plots, regardless of litter being removed (ALR) or not (AR) (Table 3). By May 2003, both Shannon diversity and evenness of untreated plots (A) were significantly higher in recently invaded areas than in long-invaded areas. Five years later, there was no difference. Soon after clearing (May 2003), plant diversity was lower in plots where A. longifolia was removed alone (AR) than in plots where both the plants and the litter were removed (ALR), but 5 years later, diversity had significantly decreased in ALR and become similar to AR. Evenness was similar between treatments and in general decreased with time.

Table 3.   Diversity measures (Shannon diversity and Pielou’s evenness) over time after clearing treatments in areas long- and recently invaded by Acacia longifolia. Abbreviations and statistical letters as for Fig. 1
Duration of invasionClearing treatmentMonitoring timeShannon (SE)Pielou (SE)
Long-invadedAMay 030·36 (0·08) ab0·23 (0·04) ab
May 060·29 (0·07) a0·21 (0·03) ab
May 080·23 (0·05) a0·16 (0·03) a
ARMay 031·36 (0·12) d0·77 (0·05) fgh
May 061·80 (0·13) ef0·72 (0·04) ef
May 081·82 (0·05) efg0·75 (0·02) efgh
ALRMay 032·06 (0·13) gh0·83 (0·03) hi
May 062·04 (0·11) fgh0·76 (0·03) efgh
May 081·58 (0·17) de0·62 (0·05) d
Recently invadedAMay 030·64 (0·16) c0·35 (0·08) c
May 060·54 (0·14) bc0·29 (0·08) bc
May 080·38 (0·14) ab0·23 (0·07) ab
ARMay 032·14 (0·10) h0·82 (0·02) ghi
May 061·99 (0·15) fgh0·71 (0·04) def
May 081·96 (0·13) fgh0·70 (0·04) def
ALRMay 032·48 (0·06) i0·87 (0·01) i
May 062·04 (0·09) fgh0·73 (0·02) efg
May 081·93 (0·16) fgh0·68 (0·05) de

Species Traits and TR in Plant Communities after Clearing

Analyses of species traits showed more changes in cleared plots (AR and ALR) than in untreated plots (A) (Fig. 3). In the early stages of recovery, therophytes were predominant in the cleared plots. Although their relative abundance declined with time, they remained the most abundant group in almost all the plots (Fig. 3a). The proportions of chamaephytes, nanophanerophytes and A. longifolia increased with time. Several life forms were absent, or rare (relative abundance <1%), in untreated plots (A).

image

Figure 3.  Differences in relative abundance of species traits among invasion age and treatments, in May 2003, 2006 and 2008. Abbreviations as for Fig. 1. The species were categorized according to (a) Raunkaier life forms and (b) biogeographic distribution.

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The majority of species that appeared in cleared plots were natives (Fig. 3b), accounting for over 70% of the cover. In untreated plots (A), A. longifolia dominated without major changes over time, while in cleared plots, it increased continuously. The most abundant species in all of the cleared plots were generalists, including species associated with both dunes and other sandy habitats (dune/generalists) as well as others associated with a wider range of habitats (generalists). In the early phase of recovery, the wide-ranging generalist species were prevalent but decreased with time, while dune/generalists increased with time, especially in long-invaded areas. Several exotic plant species (e.g. Conyza spp., C. selloana and Oxalis pes-caprae L.) were detected in the cleared plots of both long- and recently invaded areas by May 2003, their abundance increasing proportionately with time in recently invaded areas, especially in cleared plots without litter (ALR). The relative abundance of species typical of dunes was highest in cleared plots of long-invaded areas, particularly when only A. longifolia was removed (AR).

Species turnover was affected by invasion time (F1,54 = 9·99, P = 0·003) and clearing treatments (F2,54 = 24·26, P < 0·001) with no interaction between factors (F2,54 = 0·89, P = 0·418). In the 5-year interval following clearing, recently invaded areas showed significantly (P = 0·003) more alteration of species (TR = 5·5 ± 0·5) than long-invaded areas (TR = 3·9 ± 0·4). Species turnover was much higher in cleared areas (AR = 5·7 ± 0·6 and ALR = 6·1 ± 0·4) than in untreated ones (A = 2·2 ± 0·3) (A vs. AR and A vs. ALR, < 0·001). Litter removal did not significantly affect species turnover (AR vs. ALR, P = 0·522).

Susceptibility to Acacia (re)invasion Post-clearing

There was a significant interaction between invasion age, clearing treatments and time after clearing with respect to reinvasion after clearing, based on both the total number of A. longifolia seedlings (F12,60 = 15·31, P < 0·0001) and numbers that survived to become saplings and trees (F2,60 = 2·08, P = 0·032). Counts of A. longifolia seedlings revealed that a high number of viable seeds had accumulated in the soil, with particularly high peaks of germination in cleared plots (AR and ALR) of long-invaded areas (Fig. 4). Recruitment of A. longifolia seedlings was heterogeneous (e.g. ranged from 4 to 165 seedlings m−2 in ALR plots of long-invaded areas, in January 2004). Many of the seedlings did not survive from one monitoring period to the next, but throughout the study, new seedlings were found on every sampling occasion including the last.

image

Figure 4.  Recruitment of Acacia longifolia seedlings (mean + SE m−2; n = 10) over time in long-invaded and recently invaded areas after clearing treatments. Abbreviations and statistical letters as for Fig. 1.

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On average, cover of A. longifolia in untreated plots (A) was 10% higher in long-invaded areas (Fig. 5). The successful reinvasion by A. longifolia (recorded as seedlings that grow to saplings and trees) occurred progressively, and by May 2008, its cover increased significantly in all cleared plots (AR and ALR). About 6 years after clearing, there was a higher cover of A. longifolia in cleared plots where litter had been left (AR) than in plots where litter was removed (ALR).

image

Figure 5.  Percentage cover by Acacia longifolia saplings and young trees over time (mean + SE; n = 10) in long-invaded and recently invaded areas after clearing treatments. Abbreviations and statistical letters as for Fig. 1.

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Supporting Information

How Resilient are Dune Plant Communities after Invasion for Short and Long Periods?

Acacia longifolia is clearly a transformer (sensuRichardson et al. (2000), converting diverse native areas into species-poor, unrecognizable landscapes and altering several biotic and abiotic components (Marchante, Marchante & Freitas 2003; Marchante et al. 2008a,b). This study showed that despite these severe impacts, the original system is still resilient, recovering part of the native communities. However, as the invasion period increases, the system becomes less able to recover, mainly due to an incremental loss of native species. This is probably related to the higher density of the invasive species (Gooden, French & Turner 2009), which prevents immigration of new propagules to replace those that decay and lose viability with age (Marchante, Freitas & Hoffmann 2011). The finding that native species noticeably dominated all cleared areas suggests that at least some degradation thresholds had not yet been crossed (Holmes & Cowling 1997b; King & Hobbs 2006), allowing autogenic recovery after clearing.

After removal of the invader, soil microbiology and chemistry (Marchante et al. 2009), light and litter layer conditions, native seed bank (Marchante, Freitas & Hoffmann 2011) and several components of plant communities gradually recovered and increasingly began to resemble the situation in equivalent uninvaded areas (H. Marchante, H. Freitas & J.H. Hoffmann, unpublished data). Although most of the recovering species were generalists, species characteristic of dunes also reappeared (see Appendix S1 within Supporting Information for species list). This is relevant for conservation, not only because some recovering species are endemic but also because they are components of the original communities. Nevertheless, 6 years after clearing, many species characteristic of dunes were still missing, indicating that dune communities will need a long time to return to their initial states, if ever.

Dune communities are not particularly fire-prone. Nevertheless, in the more interior communities, several species may benefit from fire (Santos, Capelo & Tavares 2010). Some of these species [e.g. Stauracanthus genistoides (Brot.) Samp] were missing post-clearing. Although their absence can be, at least partially, attributed to the absence of burning, other fire-adapted species [e.g. Cistus salvifolius L., Cytisus grandiflorus (Brot.) DC.] germinated prolifically in cleared areas, even without fire.

Decreased resilience with invasion time also occurred in South African ‘fynbos’ invaded by other Acacia species, although in those areas species of the original ecosystem were apparently better represented (Holmes & Cowling 1997b). Conversely, other post-clearing studies have shown higher abundances of exotic species than natives (Ogden & Rejmanek 2005; Hulme & Bremner 2006) and no cumulative increase in species richness with time (Maron & Jefferies 2001). In fact, the seed banks of SJDNR had a higher abundance of exotic short-lived species (Marchante, Freitas & Hoffmann 2011) than was reflected in this field study. This apparent discrepancy was most probably a mismatch because the exotics that were abundant as seeds were not able to provide a persistently high cover in the field.

The high species turnover in recently invaded areas was possibly related to the high degree of variability in the characteristics of species represented in the seed banks (Marchante, Freitas & Hoffmann 2011). The seeds of each species would also require different stimuli for germination, which would consequently stagger the time of appearance of the different species. Additionally, soils of recently invaded areas had lower nutrient content (Marchante et al. 2008a), a condition that is associated with higher species TRs (Warren, Topping & James 2009).

Six years after clearing, changes in species composition were still occurring, e.g. the area covered by the native shrubs Cistus salvifolius and Cytisus grandiflorus increased substantially. This was accompanied by a reduction in plant cover (excluding A. longifolia) and diversity owing to a substantial decline in some generalist species, mainly Poaceae but also Asteraceae (Appendix S1 Supporting Information), that were particularly abundant in plots immediately after clearing. Detection of these late changes confirmed that post-clearing monitoring should continue for longer than has been the case for most analogous studies (Holmes & Cowling 1997b; Ogden & Rejmanek 2005; Hejda & Pyšek 2006).

Is this System Susceptible to (re)invasion after Clearing?

Regrowth from cut stumps of A. longifolia was negligible in the cleared plots, although large-scale clearing of A. longifolia in other areas of SJDNR resulted in higher levels of re-sprouting. The abundance of A. longifolia seedlings, particularly in long-invaded cleared plots, made cleared areas susceptible to reinvasion. Even so, the densities of seedlings were much lower than the densities of seeds in the soil (Marchante, Freitas & Hoffmann 2010), probably due to the absence of fire, which stimulates germination (Pieterse & Cairns 1986). Rapid invasion by A. longifolia after the 1995 fire confirmed the advantage that fire confers on A. longifolia as opposed to most of the native species.

Most A. longifolia seedlings failed to survive to saplings, confirming that estimates of reinvasion should be based on established plants (Downey & Smith 2000; Galatowitsch & Richardson 2005). The successful reinvasion by A. longifolia was highest in cleared plots where litter was left in place and seeds were retained along with elevated soil nutrient levels (Marchante et al. 2008a). This positive feedback has been noted for other Acacia species (Milton 1981) and for other plant species (Vitousek et al. 1987; Ehrenfeld 2003).

Other invasive species (Conyza spp., C. edulis and C.  selloana) were also found in the cleared areas. The cover of C. edulis increased particularly in recently invaded areas; being a species with vegetative reproduction (Roiloa et al. 2009), the clearing operations probably fragmented the plants, thereby enabling propagation and spread. Disturbance caused by clearing operations frequently promotes reinvasion by the target species or by other alien species (D’Antonio & Meyerson 2002; Dodson & Fiedler 2006), emphasizing the need for follow-up control (Galatowitsch & Richardson 2005).

What are the Implications of this Study for Dune Ecosystems’ Management?

In systems where invasions are extensive, persistent and include a substantial seed bank of the invader, such as A. longifolia in the Portuguese dune ecosystems (Marchante, Marchante & Freitas 2003; Marchante et al. 2008a,b), eradication is an unrealistic goal (Mack & Lonsdale 2002). Containment should be a priority as new invasion foci occur several metres from the main thickets (Marchante, Freitas & Hoffmann 2010). These foci are manageable pockets of invasion and should be prioritized for removal (Rejmánek & Pitcairn 2002). The other invasive plants detected after clearing should also be managed along with A. longifolia, before becoming a bigger problem.

Control measures should aim at reducing the abundance of the invader and restoring some of the lost structural and functional components of the ecosystem. Invaded areas should be prioritized, based on the likelihood of successful restoration (i.e. greatest benefit for native biodiversity) and on the conservation value of the areas (Downey et al. 2010). Our study, as others (Holmes & Cowling 1997b), showed that recently invaded areas should be prioritized for control because recovery of both natural vegetation (this study) and soil parameters (Marchante et al. 2009) is likely to be more successful.

After felling of A. longifolia trees, follow-up control is crucial to remove saplings, which, in sand dunes, can be hand-pulled easily before they reach about 40 cm. Most seedlings die in the early stages of growth, and removing them early would be a waste of resources. Moderate-intensity burning, which is more easily achieved when the soil is moist (Holmes 2001b), is another option to eliminate saplings, deplete the invader seed banks and remove the nitrogen-rich litter layer (Pieterse & Cairns 1988; Holmes & Cowling 1997b; Richardson & Kluge 2008). Moderate-intensity burning destroys fewer A. longifolia seeds but is less detrimental for native seed banks and is therefore probably the best option. Monitoring, at least annually, is needed to determine the best time interval for follow-up control, which needs to be repeated. In the case of A. longifolia, 2 years is the time limit after each operation because the trees begin setting seeds by then and preventing the replenishment of the seed bank should be a priority.

Even in recently invaded areas, simply removing the invader does not seem to be sufficient to fully restore the system. As in other invaded systems, additional manipulation is required (King & Hobbs 2006), namely planting of desirable species, removing the litter and/or depleting the invasive seed bank (see Discussion above) (Holmes 2002). Species that are characteristic of dunes and were recorded as scarce or absent should be sown or transplanted to accelerate recovery. This has been successfully achieved in some restoration projects (Hartman & McCarthy 2004). Transplanting of saplings will probably be most successful because these will have a height advantage over the invasive seedlings (Galatowitsch & Richardson 2005). This approach might be limited by a lack of available native species ready to transplant, as has happened elsewhere (French et al. 2008). Several species typical of Portuguese dunes are available in local nurseries. Nevertheless, full assemblages of species are not accessible, and an effort should be made to encourage more propagation effort. Simultaneously, transplanting and seed collection from neighbouring areas can be valuable in restoration actions (Schreck Reis, Carmo & Freitas 2008).

The clearing methods may also have implications for the success of restoration (Holmes & Cowling 1997b; Holmes et al. 2000). Removing thick litter layers is advisable in systems that are naturally litter poor, such as the dunes (Marchante et al. 2008a). The litter may be allelopathic or support animal and microbial species not normally associated with the invaded area, both of which may impede survival of native species (González, Souto & Reigosa 1995; French & Eardley 1997; Vranjic, Woods & Barnard 2000). In this study, litter removal hastened the recovery of native species (Appendix S1 Supporting Information) and decreased reinvasion potential, particularly in long-invaded areas where there was a more substantial litter layer (Marchante et al. 2008a). Conversely, in recently invaded areas, most of the seeds that germinated soon after clearing were accumulated in the shallower litter layer and these were lost with its removal. The lack of seeds in long-invaded litter was probably due to the disruption of recruitment of new seeds (Holmes & Cowling 1997a,b), loss of seed viability with time and failure of small-seeded species to establish (Xiong & Nilsson 1999; Sayer 2006). Myrica faya and Corema album (L.) Don, species typical of dunes, and A. longifolia have relatively large seeds whose seedlings survived germination through the deep litter layers.

The size of the area that is cleared apparently influences the recovery process, with resurgence of A. longifolia less likely and successful recovery more probable when small areas are cleared. Under natural conditions, small gaps are filled more rapidly than larger ones through encroachment of the surrounding vegetation (Fenner & Thompson 2005). Clearing operations over several hectares that took place elsewhere in SJDNR resulted in rapid reinvasion (<2 years) and a much higher density of A. longifolia after control (H. Marchante, personal observation).

Conclusion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Supporting Information

Native sand dune communities that are densely invaded by woody species still have inherent resilience, which decreases as invasion time extends. Regardless of time of invasion, autogenic recovery of cleared areas can be enhanced by active management actions, which maximize and generate synergy between abiotic and biotic components of the system (King & Hobbs 2006). For example, the initial clearing of thickets of the invasive species and the additional removal of the litter layer foster abiotic changes, e.g. light increase and decrease in barriers to germination and disruption of N addition. Such changes will favour desirable, and a few undesirable, species. Subsequent transplantation of missing native species can be used to further encourage re-establishment of the natural communities and simultaneously reduce subsequent reinvasion (Hulme 2006). However, encroachment of the invader after initial control will occur and needs to be curtailed. This can be done on a sustainable basis by using biological control, as has been done successfully in South Africa (Dennill et al. 1999). The full recovery of ecosystems to their original state seems an unrealistic target, although restoration of some of the original species assemblages needed to create system structure and allow some original function seems achievable; however, it may require a long time and a considerable financial commitment.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Supporting Information

The authors thank E. Marchante for fruitful discussions and J. Maia for assistance on species identification. V. Batalha is thanked for consultation on statistics. This research was supported by Portuguese Foundation for Science and Technology and European fund FEDER (project POCTI/BSE/42335/2001 and grant SFRH/BD/24987/2005 to H.M).

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  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
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Supporting Information

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
  10. Supporting Information

Appendix S1. List of native and exotic plant species detected in experimental plots.

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