reproductive versus vegetative recruitment of the invasive tree schinus terebenthifolius:...

Reproductive versus Vegetative Recruitment ofthe Invasive Tree Schinus terebenthifolius:Implications for Restoration on Reunion Island

Jacques Tassin,1,2 Jean-Noel Riviere,3 and Philippe Clergeau4

Abstract

Knowledge of propagation mechanisms is important forunderstanding the invasion ecology and management ofinvasive plants in order to restore invaded lands. Theidentification of recruitment pathways is one of the keysto understanding dispersal mechanisms and determininginvasive plant control strategies. The objective of thisstudy was to characterize the recruitment processes ofSchinus terebenthifolius, one of the most serious plant in-vaders in Reunion Island’s lowlands. Surprisingly, littleattention was given in literature to vegetative propagationby suckering as a dispersal mechanism. Yet, field observa-tions on abandoned farmland and riverbanks combinedwith germination experiments have shown major differen-

ces in recruitment patterns between wet and dry areas. Onabandoned dryland farms, seedling emergence is 35 timesless than on riverbanks and is replaced by suckering. Birdsfacilitated seed germination, but their role in seed dispersal(ornithochory) appeared minor and restricted to the forma-tion of satellite invasion foci. Water movement appears tobe a more efficient vector than ornithochory because it aidsseed transportation (hydrochory), seed germination, andsuckering on riverbanks. Control and restoration programsmust distinguish the two kinds of recruitment that impacton short- and long-distance dispersal.

Key words: colonization, flooding, frugivory, germination,invasion, seed dispersal.

Introduction

Invasive plants pose a significant challenge to the manage-ment and restoration of conservation areas. As a result,considerable research has been aimed at understandinginvasive plant biology and developing control strategies(McFadyen 1998; Marshall et al. 2003; Myers & Bazely2003). The identification of recruitment pathways is one ofthe keys to understanding spread mechanisms and deter-mining invasive plant control strategies. Relevant exam-ples are given on the management of Alliaria petiolata(Anderson et al. 1996), Ligustrum robustum (Lavergneet al. 1999), Psidium cattleianum (Huenneke & Vitousek1990), Rhamnus cathartica (Archibold et al. 1997), orRubus alceifolius (Baret et al. 2003).

Brazilian pepper (Schinus terebenthifolius Raddi) islisted a serious plant invader in Reunion Island’s lowlands(MacDonald et al. 1991). Introduced in 1843 (Trouette1898), it has invaded riverbanks and abandoned farmland,forming nearly monotypic stands in such areas (Cadet1977). This species also invades lowland native vegetation

and can be observed on lava flows (Chevennement 1990;Strasberg 1995).

The invasion pathways of this species on ReunionIsland were unclear. Elsewhere, the dependence ofS. terebenthifolius recruitment on exotic and native birdsis outlined by several authors (Carleton & Owre 1975;Austin 1978; Morton 1978; Ewell 1986; Cronk & Fuller1995; Panetta & McKee 1997). Surprisingly, little atten-tion was given to vegetative propagation by suckering asa dispersal mechanism. In general, the impact of birds asvectors is linked to (1) the dispersal effects (Janzen 1983;Dowsett-Lemaire 1988; Jordano 2000; Mandon-Dalgeret al. 2004) and (2) enhancing the capacity of seed germi-nation (Krefting & Roe 1949; Barnea et al. 1991; Clergeau1992; Tassin & Riviere 2001). However, other mechanismssuch as water or gravity can also serve as vectors of bird-dispersed plant species, as suggested for S. terebenthifoliusby Jones and Doren (1997). We define recruitment as theextension of a population through reproductive or immi-gration processes.

The main aim of this study was to compare the recruit-ment process of S. terebenthifolius between infestation onabandoned farmland and along riverbanks. In addition,we investigated why seedlings of S. terebenthifolius arescarce near invasion patches in abandoned farmland de-spite an abundance of fruiting and feeding by birds (Ewellet al. 1982; Panetta & McKee 1997) and why seedlings aremore common along riverbanks. The development of an

1 CIRAD, Campus international de Baillarguet, TA 10/D, 34398 MontpellierCedex 5, France2 Address correspondence to J. Tassin, email [email protected] CIRAD 3P, 7 chemin de l’IRAT, 97410 Saint-Pierre, La Reunion, France4 INRA-SCRIBE, Campus de Beaulieu, 35042 Rennes Cedex, France

� 2007 Society for Ecological Restoration International

412 Restoration Ecology Vol. 15, No. 3, pp. 412–419 SEPTEMBER 2007

integrated management strategy for this weed on ReunionIsland requires the quantifying of reproductive versusnon-reproductive propagation processes, determiningseed germination processes in the field, and understandingwhy seed germination is rarely observed outside floodedareas. Therefore, in this study, we attempted to answerthe following questions: (1) what is the role of vegetativepropagation in S. terebenthifolius dispersal?; (2) what arethe limitations to seed germination?; and (3) what is therole of birds in seed dispersal?

Methods

Study Area

Reunion Island (lat 21�069S, long 55�369E, 2,512 km2) ispart of the Mascarene Archipelago in the Indian Ocean. Itis of high conservation value, with 30% of its native vege-tation still present (Strasberg et al. 2005), compared to2.5% in Mauritius (Mungroo & Tezoo 1999) and no nativeforest left in Rodrigues. The vegetation is clearly struc-tured along an altitudinal gradient (Cadet 1977; Tassinet al. 2004). Since the first human colonization in the sev-enteenth century, destruction of primitive ecosystems hascaused the extinction of some species and threatened theexistence of many others. At least 11 native species areextinct, 106 are threatened, and 246 are becoming lessabundant (Walter & Gillet 1998). The flora, initially com-prising 600 native species, is currently dominated by 2,000introduced species of which 628 are naturalized and 62highly invasive (MacDonald et al. 1991; Lavergne et al.1999; Tassin et al. 2006). Such invasion pressure is alsoobserved on the other Mascarene Islands (Lorence &Sussman 1986).

Within lowland vegetation, five natural communities ofhigh conservation value have been identified by Strasberget al. (2005), all of them threatened by the invasion ofSchinus terebenthifolius. (1) Coastal vegetation coveringabout 300 ha (fragmented by urbanization) of herblandsand scrublands on rocky cliffs or stony and sandy shore-line is the most widely invaded native lowland habitatby S. terebenthifolius (Cadet 1977), though this speciesappears not to be tolerant to high-saline conditions(Mytinger & Williamson 1987). (2) On the leeward side,discontinuous savannah woodland occurs on 480 ha ofsandy soils. (3) In wide gullies crossing the savannah, dryforest occupies 3,300 ha as remnants up to 800 m abovesea level. Dry forest is characterized by many speciesexhibiting heterophylly and a rare occurrence of epi-phytes, with trees rarely exceeding 7–10 m height. (4)Rainforest remnants on 7,600 ha lie as a continuous can-opy of tall trees that shelter many epiphytes up to 900 mabove sea level on the upward side and up to 1,100 m onthe leeward side. (5) Wetlands extend on 470 ha. Fifty-oneprotected plant species grow in the coastal areas, dry for-est, and lowland rainforest but none is recorded in thesavannah and wetlands.

Monotypic S. terebenthifolius stands represent the finalstage in secondary plant succession on abandoned low-altitude farmland on the leeward side of the island (Cadet1977). This was also observed in Florida (Austin 1978;Jones & Doren 1997).

Plant Description

Schinus terebenthifolius is a large, dioecious shrub or smalltree native to Argentina, Paraguay, and Brazil, which wasintroduced widely in the world because of its ornamentalqualities or for shade (Morton 1969; Nielsen and Muller1980; Mytinger & Williamson 1987). It is a broad-topped,fast-growing tree to 12 m high, with a short trunk usuallyhidden by a dense head of contorted branches drooping atthe tip.

Flowering is strongly synchronous and occurs betweenFebruary and March on Reunion Island; flowers are highlyattractive to bees. Fruit production is abundant and ob-served in April to May, contrasting with most other fleshy-fruited exotic and native species (J.-N. Riviere, personalobservation). Trees are covered with compact masses ofglobular fruit (Morton 1978). The fruit is a bright red drupe,4–5 mm diameter, containing a single, kidney-shaped seedsurrounded by a sticky mesocarp which retracts on dryingand which is covered by an impermeable exocarp.

Field Observations

Five study sites were selected on abandoned farmland andfive on riverbanks. All sites were at altitudes lower than150 m above sea level and positioned on the leeward sideof the island near Saint-Pierre. At each site, eight 2 x 2–mplots were randomly located and permanently marked onthe edge of S. terebenthifolius patches. Plots were at least25 m from each other. Young plants less than 0.50 m tallwere counted and excavated with a hoe to determine ifthey had emerged from a seed or grown as a sucker. Weassumed that suckers less than 0.50 m tall always remaineda connection with the parental plant.

Seed Germination and Seed Viability

Seed germination was investigated in laboratory trials atSaint-Pierre in March and April 2001. To avoid potentialstorage effects on seed germination, only fresh fruit, col-lected near the laboratory, were used. Fruit peduncles atthe same stage of maturity were cut from twigs. Entirefruit with peduncles were used as a control treatmentbecause we observed that fruit were naturally falling withpeduncles attached. We compared the following germina-tion treatments:

(T0) Control, not removing the peduncle.(T1) Removing the peduncle, fresh fruit were delicately

pulled and the peduncle stayed attached to thebranch.

Recruitment of Schinus terebenthifolius in Reunion Island

SEPTEMBER 2007 Restoration Ecology 413

(T2) Removing both peduncle and exocarp, fruit withoutpeduncles were crumpled between fingers, and theexocarp was separated from the fruit in a small con-tainer of water. Floating exocarps were collected,and finally, the fruits were removed to dry. Waterwas used because ethanol can disrupt chemical dor-mancy (Murdoch & Ellis 2000).

(T3) Removing peduncle, exocarp, and mesocarp, fruitwere removed from their peduncle, and the exocarpsoaked in water for 4 hours from 0700 to 1100 hours.They were then briefly washed and rinsed, soakedagain from 1100 to 1700 hours, washed, and rinsedagain. They were soaked once again until the next dayat 0700 hours, then washed, and dried using a cloth.

To assess seed viability, fruit were collected and kept ina cabinet at constant temperature (24�C) and relativehumidity (70%). Seeds were removed from their meso-carp, then sown at the following times after collection:same day, then 2, 4, 8, 16, 32, 64, 128, and 256 days aftercollecting.

Effect of Birds on Seed Germination

The effect of birds on seed germination was investigatedin laboratory trials. Captive Red-whiskered Bulbul(Pycnonotus jocosus) were used for this trial. The bird wasintroduced to Reunion Island in 1973 and rapidly ex-panded its range throughout the island. Its involvement inplant invasions has been observed (Clergeau & Mandon-Dalger 2001; Mandon-Dalger et al. 2004). Wild birds werecaptured near Saint-Pierre and acclimatized in an aviary.A feeding trial was conducted in April 2001, in an aviarywith six individual cages surrounded by Plexiglas panels toavoid fruit loss. Fresh S. terebenthifolius fruit were col-lected nearby. At 7h00, a dish containing 100 fresh fruitswas presented to each bird. When the dish was close toempty, 100 additional fresh fruit were added, at regularintervals until 17h00, after which all rejected fruit werecounted to determine the number of ingested fruit.

Defecated seeds were collected the same day in eachcage and mixed from all six cages. The resulting seed lotwas used to test the effect of fruit ingestion by birds onseed germination (T4). This germination test started in theevening of the same day.

The following day, the retention time of seed in thedigestive system was monitored with four separate birds.At 7h00, a small bunch of S. terebenthifolius fruits wasplaced in each cage. For each individual bird, the meanretention time (MRT) was measured from the first inges-tion to the first defecation (Barnea et al. 1991). The exper-iment was repeated on six consecutive days.

Seed germination trials were carried out in petri dishesusing sterilized sand saturated with tap water. Each treat-ment was replicated four times using four different treesand 25 seeds per tree for each of the three treatments:intact fruits, cleaned seeds, or defecated seeds. To avoid

mold development, all prepared fruits or seeds were sur-face sterilized in an aqueous solution of sodium hypochlo-rite for 1 hour, then removed without rinsing prior tosowing in the petri dishes.

Petri dishes were maintained at 24�C, with 12-hour lightand the sand moisture monitored. Dishes were examineddaily for 30 days, and germinated seeds were counted andremoved. For test (T3) (removing peduncle, exocarp, andmesocarp), we monitored germination for only 25 daysafter sowing. Germination was defined as radicle emer-gence from seed or fruit. Germination data were analyzedusing one-way analysis of variance. Proportions wereangular transformed before analysis, and Bonferroni’s testwas used to compare means (Baskin & Baskin 2001).

Results

Field Observations

The mean number of seedlings was 30.3 times higher onriverbanks than on abandoned farming areas (F ¼ 41.634;p < 0.001), with a maximum of 0.359 seedlings/m2 alongriverbanks (Table 1). The mean number of suckers wasonly 2.5 times higher on riverbanks than on abandonedfarming areas (F-ratio ¼ 10.255, p ¼ 0.002), with a maxi-mum of 0.180 suckers/m2 areas along riverbanks. Observa-tions indicated that suckers on riverbanks were localizedon roots laid bare by erosion. Individuals from suckerswere significantly more numerous than those from seedsin abandoned farming areas (F-ratio ¼ 17.926, p ¼ 0.003).

Germination

Fruit attached to the peduncle did not germinate. Only22% of viable seeds without peduncle (T1) germinatedwithin the 30-day test period (Fig. 1). When the exocarpwas removed (T2), the germination rate increased sig-nificantly to 68% (F[1,16] ¼ 0.116, p < 0.001) within ashorter 14 days period. The difference in total germina-tion was also highly significant between fruit without exo-carp and fruit with the exocarp and mesocarp removed(T3) (F[1,16] ¼ 0.082, p < 0.001) that exhibited 100% germi-nation within 18 days. However, there was no differencebetween the final germination rates of seed without meso-carp (T3) or ingested by birds (T4) (F[1,16] ¼ 1.000, p ¼1.000). The rate of germination was also very similar,seeds without mesocarp germinating within 18 days andseeds ingested by birds germinating within 15 days.

The germination rate of stored seeds (Fig. 2) remainedhigh to 32 days (94%), then decreased (83% after 64 days,72% after 128 days), and dropped to zero after 256 days(8.5 months).

Consumption of Fruits by Birds

Fruit were readily eaten when presented to the cagedbirds. The mean number of fruit consumed per day was


414 Restoration Ecology SEPTEMBER 2007

465.3 ± 55.5, with a maximum of 509 and a minimum of355 fruit per day.

The MRT was 19.7 ± 1.5 minutes (n1 ¼ four birds, n2 ¼six repetitions), with individual values of 15.3 ± 0.2 (bird

1), 15.7 ± 0.3 (bird 2), 16.3 ± 0.4 (bird 3), and 31.5 ± 1.2(bird 4). There was no significant correlation between thenumber of fruit consumed per day and MRT (r ¼ 0.474,p ¼ 0.526).

Table 1. X and standard error of seedlings or suckers found in abandoned farming areas and riverbanks (n ¼ eight 2 x 2–m plots per site).

Seedlings Suckers

Environment Type Site X SE X SE

(1) Abandonedfarming areas

S1–1 0.008 0.011 0.063 0.024S1–2 0.008 0.011 0.047 0.028S1–3 0.000 0.000 0.023 0.024S1–4 0.016 0.015 0.047 0.028S1–5 0.000 0.000 0.023 0.024All sites 0.006 0.010 0.041 0.025

(2) Riverbanks S2–1 0.188 0.085 0.180 0.091S2–2 0.133 0.089 0.117 0.049S2–3 0.359 0.082 0.070 0.035S2–4 0.219 0.065 0.047 0.028S2–5 0.008 0.011 0.109 0.028All sites 0.189 0.089 0.103 0.055

Figure 1. Time course of germination of Schinus terebenthifoliusseeds within intact fruits without peduncle (T1), without exocarp (T2), without

mesocarp (T3), and after ingestion by birds (T4). The treatment consisting in maintaining the peduncle is not represented in the graph, as resulting

in no germination.



Discussion

This study evaluated the different recruitment processesof Schinus terebenthifolius, comparing the edge of inva-sion patches in abandoned farmlands and riverbanks. Ourresults can be summarized as follows: (1) compared tosuckering, reproductive recruitment was higher in floodedareas than sucker, which was more restricted to drierareas; (2) the peduncle, exocarp, and especially the meso-carp of fruit delayed the germination of seeds whose via-bility is less than 8.5 months; (3) removal of the mesocarpon fresh fruit through successive baths in water gave a veryhigh rate of germination; and (4) fruit ingestion and diges-tion of the mesocarp by birds gave similar results to man-ual removal of the mesocarp, even though retention timesby the birds were short.

The Role of Birds in Seed Dispersal

Deprived of coevolved systems playing in its native India,introduced Red-whiskered Bulbul preferentially spreadnon-native fruit-bearing trees and shrubs (Simberloff &Von Holle 1999). A previous study on the effect of thebird species on S. terebenthifolius germination on ReunionIsland showed that it had a significant promotive effect(Mandon-Dalger et al. 2004). Its role in the propagationof Rubus alceifolius and Ligustrum robustum in Mascar-ene Archipelago is also strongly suspected (Vaughan &Wiehe 1939; Cheke 1987; MacDonald et al. 1991).

The essential role of bird species in seed dispersal ofsmall-fruited plant invaders had already been demon-strated in insular habitats of oceanic islands. The exotic

Japanese White-eye (Zosterops japonicus) is the primarydisperser of Myrica faya seeds in the natural areas ofHawaii Volcanoes National Park (Vitousek & Walker1989). In Hawaii, 37% of the major weeds are dispersedby predominantly exotic frugivorous birds (Simberloff &Von Holle 1999). In New Zealand, the widely distributedBlackbird (Turdus merula) is one of the major weed dis-persers (Williams 2006). On the island of Tahiti, the exoticRed-vented Bulbul (Pycnonotus cafer) is considered asa major seed disperser of Miconia calvescens (Meyer1998). Last, the effect of the Pekin Robin (Leiothrix lutea)on the germination of Psidium cattleianum on ReunionIsland has been shown (Tassin & Riviere 2001). In allthese cases, birds spread invasive exotic plants in habitatsthat they could not reach otherwise (e.g., lava flows, islets,cliffs).

Our results are consistent with those of Panetta andMcKee (1997), but we argue the relative importance offrugivory in the recruitment processes of S. terebenthi-folius. Our data clarified the effects of removing the (1)peduncle; (2) peduncle and exocarp; and (3) peduncle,exocarp, and mesocarp on germination rate. We agreewith Panetta and McKee (1997) that increased seed ger-mination through consumption by birds appears to be dueto the removal of the mesocarp because passage throughthe Red-whiskered Bulbul did not significantly increasethe number of seeds that germinated or germinationspeed, compared with seeds from which mesocarp wasremoved manually.

However, we consider that the role of birds in the inva-sion of S. terebenthifolius is limited to the possible forma-tion of satellite foci of infestation (Buchanan 1989; Bass1990). This process is most likely of highest importance onrecent lava flows that are readily invaded by fleshy-fruitedexotic plants (Strasberg 1995). In this harsh environment,no other means of dispersal such as transport by water orsuckering seems possible. Spread of seeds by birds appearsto be less important in other areas, where other recruit-ment processes are also involved. Moreover, becausefruits are not regurgitated but digested by birds, the rela-tive short retention time minimizes the probability thatseed will be moved away from the parent plant. The tran-sit time of seed through Pycnonotus jocosus is shorter thanfor Z. lateralis, which needs 25–30 minutes to defecateingested seeds (Panetta & McKee 1997). This result isconsistent with the argument that highly frugivorous spe-cies process fruits and defecate seeds faster than less frugi-vorous species (Herrera 1984). Another consideration isthat S. terebenthifolius fruits when no other plants producefruit. Therefore, the mobility of foraging frugivorous birdsis restricted within S. terebenthifolius infestations.

The formation of satellite foci is limited by germina-tion rate after deposition and early seedling develop-ment, linked with bird movements and foraging efforts(Jordano 2000), but also with weather conditions. On theleeward side of Reunion Island, rains during the fruitingseason of S. terebenthifolius, up to December, are very

10 100

Days after collecting

0

10

20

30

40

50

60

70

80

90

100G

erm

inat

ion

(%)

Figure 2. Evolution of rate of germination with time following fruit

collecting. Before sowing, mesocarp was removed manually with

water. Smoothing is obtained using least weighted squares (LWS)

method. Days are ordinated using a log scale.



infrequent. Consequently, the chance of deposited seedsgerminating is very low, and most seeds are expected todie before the next rainy season because our studiesshow that no seed survived after 8.5 months. This is con-sistent with previous seed bank studies of S. terebenthifo-lius, where Panetta and McKee (1997) showed that noseed survived after 9 months. Recruitment of S. tereben-thifolius by seed seems dependent on seeds dispersedduring only a few months following fruiting in dry cli-matic conditions. However, on the windward side of theisland, where the climate is wetter, germination andseedling development look more probable during thefirst few months following fruiting.

According to our results, we do not consider that therecruitment of S. terebenthifolius is entirely dependentupon frugivorous birds because we demonstrated that thesoaking of fruit in water for a sufficient time could activategermination. Field data showed that seedlings of S. tereben-thifolius were mainly observed in the vicinity of wetlands orriverbanks and germination trials proved the role of wateron increasing seed germination. Our data are consistentwith the conclusions of Ewell et al. (1982) who worked onareas of the Everglades where water does not flow, andtherefore considered that animal dispersal of S. terebenthi-folius was more important than dispersal by water.

Role of Suckering on Recruitment

Our results show that in dry areas, suckering is by farthe most important recruitment process. Extending fromsatellite foci of infestation, S. terebenthifolius can pro-duce root suckers that can develop without evidence ofdamage to the tree or its root system (Jones & Doren1997). Because of this, the clumping of trees in invasionpatches on abandoned farmlands may be better explainedby suckering (Woodall 1979), rather than by seeding.

Schinus terebenthifolius appears to use two main propa-gation patterns. Vegetative propagation based on suckersdevelopment is exhibited in dry environments, contribut-ing to the extension of infestations, involving strong shad-ing and possibly allelopathic processes that impact onother plant species. Additional genetic studies could beused to reveal the clonal structure of individuals growingin each infestation. On the other hand, in wetlands orflooded areas, propagation is both vegetative and repro-ductive because erosion of the riverbanks by water causessuckers emergence although water breaks the dormancyof seeds by washing the flesh from the fruit and transport-ing them along the river.

Conclusions and Implications

Our results add to previous data on recruitment of Schi-nus terebenthifolius (Austin 1978; Morton 1978; Jones &Doren 1997; Panetta & McKee 1997). They reveal acombination of short-distance recruitment mechanisms(sucker, seed rain around the tree) and long-distance ones

(seed dispersal by birds or river flooding). Seed dispersalby birds is the only process that can explain the speciesoccurrence in harsh environments such as lava flows.

Control and restoration strategies must take intoaccount both short- and long-distance recruitment pro-cesses. In abandoned farmlands, the spread of S. tereben-thifolius from individual trees is promoted by humanactivity, such as plowing, soil removal, or stone pilingaround fields, which promotes suckers formation (Li &Norland 2001). Because of this, we advise against the useof mechanical methods to control the plant as it can leadto suckering. Early detection can be used to prevent inva-sion in farming areas or natural ecosystems (e.g., dryforest, costal areas) through seed dispersal by birds.Eradication of the first seedlings will prevent expansion ofinvasion foci.

Control along riverbanks is more difficult becauserecruitment is assured by water action (increased germina-tion) and water movement (seed dispersal). In this case,suppression of the weed through biological control may bethe preferred option in dense, lower priority infestations.Two insect species, the thrips Pseudophilothrips ichini(Thysanoptera: Phlaeothripidae) and the sawfly Hetero-perreyia hubrichi (Hymenoptera: Pergidae) are potentialcandidates for biological control because they visibly dam-age the plant in its native range and are likely to be hostspecific (Cuda et al. 2004).

Implications for Practice

d Restoration strategies must take into account bothshort- (sucker, seed rain) and long-distance (ornitho-chory and hydrochory) recruitment processes.

d The use of mechanical methods to control the plantis to be avoided because it can promote suckering.

d Early detection can prevent invasion in natural eco-systems through seed dispersal by birds.

d Control along riverbanks needs sites priorization andjustifies biological control.

Acknowledgments

This research was conducted with financial assistance fromRegion-Reunion. We thank E. Bruzzese for revising theEnglish manuscript. We are also grateful to S. Georgerfrom Federation Departmentale des Groupements deDefense contre les Ennemis des Cultures (FDGDEC) forproviding the birds used for experiments. Two anonymousreviewers fine-tuned the quality of the manuscript.

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reproductive versus vegetative recruitment of the invasive tree schinus terebenthifolius:...

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