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Plant Ecology & Diversity

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The effect of native forest replacement by Pinusradiata plantations on riparian plant communitiesin Chile

Ivon R. Gutierrez Flores & Pablo I. Becerra Osses

To cite this article: Ivon R. Gutierrez Flores & Pablo I. Becerra Osses (2017) The effect of nativeforest replacement by Pinus radiata plantations on riparian plant communities in Chile, PlantEcology & Diversity, 10:1, 65-75, DOI: 10.1080/17550874.2017.1294630

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The effect of native forest replacement by Pinus radiata plantations on riparian plantcommunities in Chile

Ivon R. Gutierrez Floresa* and Pablo I. Becerra Ossesa,b

aDepartamento de Ecosistemas y Medio Ambiente, Facultad de Agronomía e Ingeniería Forestal, Pontificia Universidad Católica deChile, Santiago, Chile; bCentro de Ecología Aplicada y Sostenibilidad, Pontificia Universidad Católica de Chile, Santiago, Chile

(Received 6 November 2015; accepted 9 February 2017)

Background: As riparian habitats are legally protected, they have been maintained even in areas where extensivereforestation by exotic species occurred in areas surrounding riparian environments. However, the extent to which theriparian plant communities have been affected by the replacement of native forest on slopes has rarely been investigated.Aims: In this study, we evaluated the effects of replacement of native forest by Pinus radiata plantations, on the diversity andstructure of plant communities of remnant forests preserved in riparian habitats.Methods: We selected five watersheds with native forest and five watersheds where the native forest had been replaced bypine plantations preserving riparian forests and compared composition, diversity and structure of riparian vegetation.Results: In watersheds with pine plantation, riparian forests had lower adult tree density, tree cover, diversity andregeneration and higher shrub cover, diversity of herb species and diversity and richness of exotic species than riparianforests with abutting native forest.Conclusions: The results suggest that the replacement of native forest by pine plantations negatively affects the diversityand structure of riparian forest. However, in other respects (e.g. shrub and climber richness), these habitats are not affectedand they contribute significantly to the biodiversity conservation.

Keywords: diameter structure; forest structure; native riparian vegetation; Pinus radiata plantations; regeneration; speciesrichness; species diversity

Introduction

The large-scale replacement of native forests by planta-tions of exotic tree species in recent decades has resultedin the loss of biodiversity, a rise in invasive species andchanges in water resources (e.g. Parris and Lindenmayer2004; Richardson and Rejmánek 2004; Huber et al. 2010;Altamirano and Lara 2010). In addition to these directeffects, plantations can impact the fragments of remainingnative vegetation (Bustamante and Grez 1995; Bustamanteet al. 2003; Kanowski et al. 2005; Langer et al. 2008).While riparian habitats are preserved to protect watercourses and biodiversity (Boothroyd and Langer 1999;Boothroyd et al. 2004; Langer et al. 2008), these riparianforests frequently remain as fragments, separated fromriparian forests of other watersheds. Vegetation of riparianforests is generally more diverse and complex than vege-tation of surrounding slopes (Naiman et al. 2000; Harperand Macdonald 2001; Granados-Sánchez et al. 2006), isusually more productive (Granados-Sánchez et al. 2006)and plays a fundamental role in hydrological processes(Tabacchi et al. 2000). Riparian forest can be adverselyaffected by factors related to the type and intensity ofmanagement on plantations that surround them as well asby the effects of fragmentation (e.g. edge effects)(Kanowski et al. 2003, 2005).

The establishment of forestry plantations can have dif-ferent effects on riparian vegetation. For example, plantationmanagement practices, such as thinning or pruning, cancause disturbances for riparian vegetation due to the fall oftrees and branches, reducing tree cover (Graynoth 1979;Boothroyd et al. 2004; Langer et al. 2008). All these mechan-ical disturbances can affect regeneration and cause mortalityof individual plants and with this alter the size structure oftree populations. At the same time, the clear-cutting of plan-tation areas implies a period of some years during whichnative riparian vegetation is bordered by open areas, whichcan have significant edge effects through macro- and micro-environmental changes (Chen et al. 1992; Burton 2002;Boothroyd et al. 2004; Harper et al. 2005; Langer et al.2008; Becerra and Simonetti 2013). Newly cleared planta-tion areas are open to an invasion by exotic species (Frankand Finckh 1997; Boothroyd et al. 2004), thus serving assources for exotic species from where they can invade adja-cent riparian habitats. As a consequence of these biotic andabiotic changes in plantation areas, different vegetation attri-butes of remnant riparian forests can be affected. For exam-ple, changes can be expected in the composition of plantspecies, with the richness of exotic species increasing andnative species richness decreasing (Thysell and Carey 2000,2001; Boothroyd et al. 2004; Harper et al. 2005; Langer et al.

*Corresponding author. Email: irgutierrez@uc.cl

Plant Ecology & Diversity, 2017Vol. 10, No. 1, 65–75, https://doi.org/10.1080/17550874.2017.1294630

© 2017 Botanical Society of Scotland and Taylor & Francis

2008; Fuentes-Ramírez et al. 2010). Changes can also beexpected in the density and diversity of regeneration of treespecies, in general, decreasing in riparian forests(Bustamante and Castor 1998; Halpern et al. 1999; Thyselland Carey 2001; Brockerhoff et al. 2003; Harper et al. 2005;Echeverría et al. 2007; Langer et al. 2008). In addition, moreopenings in the canopy of riparian forests can be associatedwith an increase in the density of understorey vegetation(Battles et al. 2001; Kanowski et al. 2003; Ramovs andRoberts 2003; Harper et al. 2005). A reduction in tree canopycover may also produce a decrease in diversity of tree andclimber species and an increase in the diversity of herb andshrub species (Thomas et al. 1999; Battles et al. 2001; Aryaand Ram 2013; Caldeira et al. 2014).

Pinus radiata D. Don is a conifer originating fromCalifornia, USA, and is one of the main species employedin forestry plantations in Chile and in many other countries(Critchfield and Little 1966; Rozzi et al. 1994; Richardson1998; Baker and Murray 2012). Close to 64% of forestplantations in Chile are concentrated between 35° and 38°S ([CONAF] Corporación Nacional Forestal 2011), corre-sponding to the transition zone between Mediterraneantype and Temperate forest zone in South America. Thisforest is characterised by a lower species richness thantropical and subtropical forests, but it has a high level ofendemism (Armesto et al. 1998), and has been classified asa biological hotspot (Myers et al. 2000). Some of the mainthreats to the biodiversity of these forests are forestryplantations with exotic species, agriculture and grazing(Rozzi et al. 1994; Armesto et al. 2001; Lusk et al.2001; Becerra 2006; Echeverria et al. 2006; Altamiranoand Lara 2010).

The effect of replacing native forest with plantations of P.radiata has been studied extensively in Chile, Spain,Australia, New Zealand and South Africa (e.g. Richardsonand Van Wilgen 1986; Schlatter and Otero 1995; Merinoet al. 2004; Parris and Lindenmayer 2004; Williams andWardle 2005; Echeverria et al. 2006; Gómez et al. 2009;Altamirano and Lara 2010; Huber et al. 2010; Meers et al.2010). The main effects reported include biotic and abioticchanges in areas transformed to plantations, such as anincrease in stream outflow rates, owing to less canopy inter-ception, and a higher sediment load (Huber et al. 2010),changes in the chemical characteristics of the soil (Schlatterand Otero 1995), soil loss and compaction (Oyarzun andPeña 1995; Merino et al. 2004), reduced richness of nativespecies (Lindenmayer et al. 2000; Meers et al. 2010;Onaindia et al. 2013) and increased presence of exotic spe-cies in plantations (Frank and Finckh 1997; Brockerhoff et al.2003; Becerra and Simonetti 2013). At the same time, one ofmain collateral effects of replacement of native forests byplantations in remnant native forest areas is greater probabil-ity of invasion by exotic species (Bustamante and Castor1998; Boothroyd et al. 2004; Langer et al. 2008; Rojaset al. 2011), among them, P. radiata (Lindenmayer andMcCarthy 2001; Bustamante et al. 2003; Bustamante andSimonetti 2005; Williams and Wardle 2005; Guerrero and

Bustamante 2007; Baker and Murray 2012; Becerra andMontenegro 2013). Although there have been numerousstudies of fragmentation and replacement of native forests,few studies have focused on the downslope effect of pineplantations on riparian vegetation. In addition, most studieshave compared fragments of native forests and plantationareas in the same locality, while few studies have examinedforest fragmentation and replacement effects at a larger geo-graphic scale, in which different localities and watersheds areincluded. This study assessed the effects of replacing nativeforests on slopes by pine plantations on remnant riparianvegetation in watersheds, covering a major part of the geo-graphic range in the distribution of plantations of P. radiatain Chile. In particular, we assessed the hypothesis that repla-cing native forest by plantations of P. radiata has negativedownslope effects on the diversity and structure of riparianvegetation. Specifically, we predicted a (i) decreased richnessand diversity of trees and climbers and increased speciesrichness of shrubs and herbs, (ii) increased richness anddiversity of exotic species and decreased richness and diver-sity of native species; (iii) lower density and richness of treespecies for different size classes and (iv) increased understorycover, in watersheds with replacement as compared to water-sheds without replacement of native forest.

Materials and methods

Study area

The study was conducted in Chile between 35° and38° S. Ten watersheds were selected, five withoutreplacement of native forest (hereafter “without repla-cement”) and five with replacement by pine tree plan-tations on both slopes (hereafter “with replacement”).In general, the watersheds were distributed in pairs,one with and one without replacement in the samelocality to obtain the same climate range between thetwo types of watersheds (Figure 1). To ensure thatchanges observed in riparian vegetation be attributableto management of P. radiata plantations, all remnantsof riparian vegetation were continuous with the planta-tion. So, there was no separation between riparianvegetation and plantation. According to Gajardo(1994), all the studied sites are classified in theDeciduous Forest Region, a temperate forest areadominated by deciduous species such as Nothofagusobliqua, N. glauca and N. alpina and evergreen speciessuch as N. dombeyi, Cryptocarya alba and Aextoxiconpunctatum, among others (Table 1).

All the watersheds with replacement, previous toplanting P. radiata on the slopes, were covered with nativevegetation (according to the information provided by theowners), so that any changes registered in the watershedswere attributable to the replacement of native forests byplantations of pine trees and the activities associated withtheir management. At the time of conducting the fieldwork, the plantations were between 12 and 18 years old,

66 I. R. Gutierrez Flores and P. I. Becerra Osses

trees had a diameter at breast height (DBH) between 16and 28 cm varied in height between 17 and 25 m, thecanopy cover was between 23% and 46% and all hadexperienced only one rotation. The width of the riparianforest ranged from 12 (Los Potrerillos) to 20 m (ElDuende). None of the watersheds with replacement hadbeen cut recently, with the exception of El Duende, which,in one part of the watershed, had been clear-cut for the firsttime just 1 year before this study.

Sampling design and data collection

The sampling was carried out between August 2013 andJanuary 2015. Within the same locality and month, awatershed with replacement and another without replacementwas sampled, in all, five pairs of watersheds. In eachwatershed, five 10 × 4 m plots were established on each sideof the river (10 in total). The plots were 40 m apart along theriver and were located closer than 5 m from the edge of theriver.

Species richness and diversity. The composition of vascularplant species and the percent cover of every species wereregistered in all the plots. Percent cover was assessed by

visual estimation in each plot (e.g. Lindenmayer andMcCarthy 2001; Pauchard and Alaback 2004; Onaindiaet al. 2013). To do this, we started by recording all speciesin the plot, and then, inform standing in the centre of the plot,estimated the cover of each species (Mueller-Dombois andEllenberg 1974). For species unidentified in the field, vou-cher specimens were deposited in the herbarium of theNatural History Museum of Santiago (Table 1S, supplemen-tal data). For every plot, the Shannon–Wiener index (H) wascalculated (using percent cover data) as a measure of speciesdiversity for each life form (trees, shrubs, herbs and climbers)and origin (native and exotic). Species richness was analysedfor each of life form and origin, for each plot. Unidentifiedspecies were included in the analysis of diversity and richnessonly when it was possible to determine their life form ororigin. Species were classified following Marticorena andQuesada (1985). Species with potential height >5 m wereconsidered trees; ferns were classified as forbs.

Size structure. DBH was recorded for all trees >2 m heightand >5 cm in diameter to evaluate the size structure of treespecies. Four diameter classes were established: C1 (5.1–15cm), C2 (15.1–30 cm), C3 (30.1–50 cm) and C4 (>50 cm).Trees with DBH of <5 cm were classified as regeneration.We distinguished three regeneration classes: seedlings (<0.5m in height), advanced regeneration (0.5–2 m in height) andsaplings (>2 m in height and <5 cm DBH). Differences intree species density and richness between the two watershedtypes were compared for each size class separately.

Stratification. Vegetation cover was recorded for groundvegetation (<1 m height), undergrowth (1–5 m) andcanopy (> 5 m), using the point intercept method, with28 points located at each 1 m in the boundary of everyplot, which yielded cover values for all the plots at everyheight class. No life forms or species were distinguished inthis exercise, only the absence or presence of vegetation.Understorey was represented by the strata <5 m.

Data analysis

We compared watersheds with and without replacement foreach variable using generalized linear models. The analyseswere done in a nested design, where the watershed type (withand without replacement) were considered as the main factorand specific watersheds nested in each watershed type. Wefound a Gaussian distribution of data for Shannon diversityindex and hence we used an “Identity” function, while for thedata of species richness, density and cover, a Poisson dis-tribution we observed and “Square Root” function wereused. All analyses were made in R-3.1.2.

Results

Species richness and diversity

In the watersheds without replacement, 146 species wererecorded, belonging to 119 genera and 80 families. Among

Figure 1. Location of studies areas in the Maule and BiobíoRegions in central southern Chile.

The effect of native forest replacement by Pinus radiata 67

Table

1.Locationan

dcharacteristicsof

watershedsincluded

inthestudy.

Altitude

(ma.s.l.)

Nam

eRegion

Coo

rdinates

Watershed

type

Max

Min

Area(ha)

Clim

ate

Vegetation

Los

Piuqu

enes

Maule

35°48‘49“S

71°11´6“

WWith

outreplacem

ent

2087

660

2087

.87

Tem

perate

mesotherm

alinferior

stenotherm

alsemi-

arid

Mediterranean

Deciduo

usmou

ntainforest

Los

Potrerillo

sMaule

35°31‘44“S

71°11‘55

“W

With

replacem

ent

868

452

913

Tem

perate

mesotherm

alinferior

stenotherm

alsub-

humid

Mediterranean

Las

Arañas

Biobío

37°33‘33“S

73°13‘20“W

With

outreplacem

ent

982

560

142.40

Tem

perate

infra-thermal

stenotherm

alperhum

idMediterranean

Con

cepciónDeciduo

usForest

Los

Cerezos

Biobío

37°34‘05“S

73°16‘58“W

With

replacem

ent

730

224

254.30

Los

Queñes

36°39‘33“S

71°34‘35“W

With

outreplacem

ent

1561

565

1,02

1.60

Tem

perate

mesotherm

alinferior

stenotherm

alsemi-

arid

Mediterranean

Deciduo

usmou

ntainforest

Las

Cabras

Biobío

36°40‘24“S

71°37‘40“W

With

replacem

ent

1168

576

1,12

2.00

Manqu

iBiobío

36°22‘15“S

72°44‘27“W

With

outreplacem

ent

571

7849

2.30

Tem

perate

mesotherm

alstenotherm

alSub

humid

Mediterranean

Maule

decidu

ousforest

Mela

Biobío

36°20‘56“S

72°46‘47“W

With

replacem

ent

558

7545

2.40

Sin

Puerta

Maule

36°02‘46“S

71°19‘21“W

With

outreplacem

ent

1153

520

235.00

Tem

perate

mesotherm

alstenotherm

alsub-hu

mid

Mediterranean

Maule

decidu

ousforest

ElDuend

eMaule

36°03‘30“S

71°20‘48“W

With

replacem

ent

1078

530

353.00

Note:

Clim

atefollo

wsSantib

áñez

andUribe

(199

3)an

dvegetation

follo

wsGajardo

(1994).

68 I. R. Gutierrez Flores and P. I. Becerra Osses

them, 34.9% (51 species) were herbaceous, 26% (38 species)shrubs, 24.7% (36 species) trees and 14.384% (21 species)climbers. In the watersheds with replacement, an identicaltotal number of species were recorded, belonging to 113genera and 71 families, of which 43.8% (64 species) wereherbaceous, 23.3% (34 species) shrubs, 21.9% (32 species)trees and 11% (16 species) climbers (Table 1S). In the water-sheds without replacement, of the 139 species of knownorigin, 5% (7 species) were exotics, while in the watershedswith replacement, of the 142 species of known origin, 16.2%(23 species) were exotics, mainly herbaceous (70%). Someof the native species present in most of the watersheds (atleast six) were Aextoxicon punctatum, Aristotelia chilensis,Citronella mucronata, Cryptocarya alba, Lomatia dentata,Luma apiculata, Chusquea quila, Boquila trifoliata, Cissusstriata, Hydrangea serratifolia, Lapageria rosea andLardizabala biternata. The most common exotic specieswere Rubus ulmifolius, Rosa moschata, Prunella vulgarisand Rumex acetosella.

There was a significantly higher diversity (Shannon–Wiener) of tree species in the watersheds without replacement(P = 0.002), while there was a greater diversity of herbaceousspecies in the watersheds with replacement (P = 0.005). Nosignificant differences were found between the two types ofwatersheds in the diversity of shrub (P = 0.914) and climberspecies (P = 0.767) (Figure 2a). There was a greater richnessof tree species in the watersheds without replacement (P =0.028) and greater richness of herbaceous species in water-sheds with replacement (P = 0.005). No significant differenceswere found in the richness of shrub (P = 0.219) and climberspecies (P = 0.783) between watersheds with and withoutreplacement (Figure 2b).

There was greater diversity of native species (P =0.004) in watersheds without replacement than in thosewith replacement, while there was greater diversity ofexotic species (P < 0.0001) in watershed with replacement(Figure 3a). Similarly, there was significantly greater rich-ness of exotic species in watersheds with replacement (P <0.0001), but there was no significant difference in the

richness of native species between watershed types (P =0.273) (Figure 3b).

Size structure of tree species

There was significantly greater density of individuals of allthe considered DBH classes (P < 0.0001 for every class) inthe watersheds without replacement (Figure 4a). Also,there was significantly greater richness in the class C4 (P< 0.0001) and C3 of tree species (P = 0.002) in watershedswithout replacement, while there were no differences inthe other classes (P = 0.58; P = 0.106 in C1 and C2,respectively) (Figure 4b).

There was a greater density of total regeneration andregeneration of seedlings and saplings in the watershedswithout replacement (P < 0.0001), while in watershedswith replacement there was greater density of advancedregeneration (P < 0.0001) (Figure 5a). There was greaterrichness of species at the level of seedlings (P = 0.003),saplings (P = 0.022) and marginally for total regeneration(P = 0.051) in watersheds without replacement, whilethere was no difference between the two types of water-sheds in the richness of advanced regeneration (P = 0.273)(Figure 5b).

Stratification of vegetation cover

There were no significant differences between watershedswith and without replacement in plant cover at the stratumof <1 m (P = 0.234), while at the stratum 1–5 m, there wassignificantly more cover in watersheds with replacement(P < 0.0001). In contrast, cover in the stratum >5 m wassignificantly greater in watersheds without replacement (P< 0.0001) (Figure 6).

Discussion

The structure of native riparian vegetation differedbetween watersheds with and without replacement of

Figure 2. Species diversity (Shannon index)/plot (a) and species richness/plot (b) per life form (trees, shrubs, herbs and climbers) inwatersheds with and without replacement (mean ± 1 SE). N for each bar = 50. Different letters indicate statistical differences (P < 0.05)between watershed with and without replacement for a single life form.

The effect of native forest replacement by Pinus radiata 69

native forest by pine plantations. There was lower densityof trees with DBH >5 cm and lower cover of the upperstratum in the forest of watersheds with replacement. Thiscould have triggered the increased cover of undergrowth(stratum 1–5 m) observed in watersheds with replacement.Based on the observations of this study, it is possible toassociate one or more causes with these structural differ-ences between the two types of watersheds. A possiblecause is the selective cutting of trees in the native forestremnants (Senbeta and Teketay 2001; Neira et al. 2002),which can be more common in watersheds with planta-tions because the remnant riparian forest are more acces-sible. For example, the wood of species like Gevuinaavellana, Drimys winteri, N. dombeyi, Laurelia sempervi-rens, N. alpina and N. obliqua are widely used in Chile for

diverse purposes, and none of these species, with theexception of N. obliqua, had diameters greater than 30cm in the watersheds with replacement. It is also possiblethat plantation management activities such as thinning,pruning and harvesting could have caused disturbancesin the canopy cover of remnant forests (Boothroyd et al.2004), for example, by falling branches and even adultindividuals of P. radiata (authors’ personal observation). Itis also possible that the native trees in remnant riparianforest fall due to the effect of wind, which is generallymore intense in fragments that are surrounded by an openmatrix, as is the case after the plantations are cut (Burton2002). Edge effects also generally raises the temperatureand reduces the moisture levels of the soil within remnantforest (Didham and Lawton 1999), which may result in

Figure 3. Species diversity (Shannon index)/plot (a) and species richness/plot (b) according to biogeographic origin (native and exotic)in watersheds with and without replacement (mean ± 1 SE). N for each bar = 50. Different letters indicate statistical differences (P < 0.05)between watersheds with and without replacement for a single biogeographic origin.

Figure 4. Density (individuals/ha) (a) and species richness/plot (b) of trees species per DBH class (C1: 5.1–15 cm, C2: 15.1–30 cm, C3:30.1–50 cm, C4: >50 cm) in watersheds with and without replacement (mean ± 1 SE). N for each bar = 50. Different letters indicatestatistical differences (P < 0.05) between watersheds with and without replacement for a single DBH class.

70 I. R. Gutierrez Flores and P. I. Becerra Osses

higher mortality of senescent individuals and thus reducecanopy cover.

The creation of clear-cut spaces and reduced cover asso-ciated with fewer large-diameter trees, in addition to drasticchange in the matrix that surrounds remnant riparian forestwhen plantations are harvested, may result in sharp micro-environmental changes in the remnant forests. These changescan include an increase in light (Burton 2002; Boothroydet al. 2004; Langer et al. 2008), soil moisture reduction and

temperature increases (Didham and Lawton 1999; Pearsonet al. 2002; Pawson et al. 2006), among others. These struc-tural and environmental changes may be related to the differ-ences found in richness, diversity and density of the remnantriparian vegetation between the watersheds with and withoutreplacement (Ramovs and Roberts 2003; Harper et al. 2005;Echeverría et al. 2007). As expected, we observed a reduc-tion in the diversity of native species and increased richnessand diversity of exotic species in watersheds with replace-ment. Plantation areas, especially after being cleared, areoften invaded by exotic plants that can spread to native forestfragments (Frank and Finckh 1997; Kanowski et al. 2005;Langer et al. 2008; Becerra and Simonetti 2013), in this case,remnant riparian forests. Generally, exotic species areadapted to disturbed habitats (Thysell and Carey 2001;Boothroyd et al. 2004), as apparently are the riparian forestsin watersheds with replacement. Also, the forest remnantssurrounded by open areas, like riparian forests when planta-tions have been clear-cut, are more frequently visited bylivestock that act as vectors for the dispersion of exoticspecies (Pauchard and Alaback 2004).

Despite the greater diversity of exotic species inwatersheds with replacement, the regeneration or juve-nile individuals of P. radiata were not registered in anyof the assessed watersheds, although a few adult treeswere present. The absence of invasions of P. radiata inriparian forests, including watersheds with pine planta-tions, may be due to their shade-intolerant character. Itis possible that this species requires more canopy open-ings or much less cover of undergrowth strata to regen-erate (Arévalo and Fernández-Palacios 2005; Williamsand Wardle 2007). Consequently, the riparian forestremnants in watersheds with replacement show certainresistance to the invasion of P. radiata. However, thefew individuals of P. radiata found in riparian forestssuggests that pine invasions can occur, as occurs inother forests neighbouring pine plantations (Estadesand Escobar 2005; Williams and Wardle 2007).

Figure 5. Density (individuals/ha) (a) and species richness/plot (b) of trees species corresponding to each regeneration class(seedling, advanced regeneration and sapling) and total by watershed type (with and without replacement) (mean ± 1 SE). N foreach bar = 50. Different letters indicate statistical differences (P < 0.05) between watersheds with and without replacement for asingle regeneration class.

Figure 6. Cover of three vertical strata <1, 1–5 and >5 m ineach watershed type (with and without replacement) (mean ± 1SE). N for each bar = 50. Different letters indicate statisticaldifferences (P < 0.05) between watersheds with and withoutreplacement for a single stratum.

The effect of native forest replacement by Pinus radiata 71

On the other hand, and also as expected, we observedan increase in herb species in watersheds with replace-ment, which could be triggered by an increase in lightavailability produced by a more open canopy. Similarly,the reduction in richness and density of tree species regen-eration observed in replaced watersheds, mainly at thelevel of seedlings, could be related to disturbances andmicroenvironmental changes, apparently more frequents inwatersheds with replacement. Various studies havereported how these types of changes, especially reductionsin soil moisture and water stress, strongly affect the regen-eration of woody species (Leishman and Westoby 1994;Burton 2002; Franklin et al. 2002; Pearson et al. 2002;Caccia et al. 2009). Bustamante et al. (2006) observedsimilar results in forests of the northern coastal range ofour study region, where the regeneration of tree specieswas reduced in remnant forests (although not correspond-ing to riparian forests in this case) surrounded by P.radiata plantations.

Other mechanisms may also hinder forest regenera-tion in watersheds with replacement. For example, lowerseed production is associated with lower density of adultand larger trees (Simonetti et al. 2001). Also, competi-tion with exotic herbaceous species resulting from theinvasions observed in remnant riparian forest couldreduce regeneration (Hobbs 2001; Kanowski et al.2003; Huth and Wagner 2006; Zhu et al. 2014). Aswell, higher rates of seed predation have been documen-ted in forest remnants like those of watersheds withreplacement (Donoso et al. 2003; Simonetti et al.2006), reducing the density of regeneration. The pre-sence of livestock, which can have negative effects onseedlings (Vazquez 2002), could also have reducedregeneration in riparian forests of watersheds with repla-cement, as cattle and horse faeces and hoof prints werefound in 50% of watersheds without replacement com-pared to 80% of watersheds with replacement.

On the other hand, our results suggest that someattributes of riparian native forests (richness and diversityof shrub and climber species and total richness of nativespecies) are not strongly affected by the replacement ofnative forests on slopes. It is possible that the presence offorestry plantations neighbouring native forest remnantsinstead of permanently open areas has avoided majorchanges in them. Plantations generate less drastic envir-onmental changes than do open areas, as the tree cover islow only for a period of no more than 10 years(Brockerhoff et al. 2003). Ramos et al. (2008) evensuggested that the presence of plantations helps conservenative forests in Chile when compared to areas wherenative forests border on pastures or open areas.Additionally, the plantations established in the studiedwatersheds have had only one rotation, that is, the ripar-ian forest have only been bordered by open areas twice(once for the establishment of the plantation and the otherafter the first harvest). It is possible that after more rota-tions, variables of native vegetation composition or struc-ture will be more affected.

Consequently, the preservation of remnant forests onthe banks of waterways in watersheds with replacement ofnative forest by plantations on slopes (Boothroyd andLanger 1999) plays an important role in the conservationof biodiversity. Several studies have shown that remnantforests contribute to the conservation of biodiversity oftemperate forests in Chile (e.g. Estades and Temple1999; Grez 2005; Bustamante et al. 2006; Simonetti2006; De La Vega and Grez 2008). Given the above,conservation should not be restricted to large-scale areas,especially when large areas are not available for some typeof ecosystem, but rather should include small forest rem-nants (Grez 2005). However, more attention needs to begiven to the increasing invasion of exotic species in smallforest remnants (Pauchard and Alaback 2004; Becerra andSimonetti 2013). So, it is important to consider the breadthof the conserved riparian vegetation (Langer et al. 2008),as well as the management of neighbouring plantations(Pauchard and Alaback 2004), given that they can have apositive effect on invasion processes. Thus, with the aimof strengthening conservation of remnant riparian vegeta-tion, we suggest (1) creating buffer zones between rem-nant vegetation and plantations (Baker and Murray 2012),for example selectively harvesting plantations in areasadjoining fragments, leaving some areas permanentlywith some pine trees on the outer border with native forestfragments (Thysell and Carey 2001; Roberts and Zhu2002) to attenuate microenvironmental changes in thefragments; (2) reducing the internal degradation of rem-nant forests (Rojas et al. 2011) by restricting, for example,the entry of cattle and tree cutting; and (3) developingprotocols prior to the use of machinery in managing plan-tations to avoid causing disturbances in the fragments(Lindenmayer and McCarthy 2001).

Conclusions

The results partially support the proposed hypotheses, withevidence of less diversity and richness of tree species, lessregeneration of native tree species, more exotic species,and greater diversity of herbaceous species in riparianforest remnants of watersheds with replacement. Theseeffects can be attributed to changes at the level of canopycoverage and the density of trees with diameters greaterthan 5 cm in watersheds with replacement and the result-ing environmental changes. On the other hand, the absenceof change in some variables, such as total richness ofnative species, and in particular of shrub and climbingspecies in riparian forests in watersheds with replacement,suggests that remnant vegetation contributes significantlyto the conservation of biodiversity in forestry managementsystems, and consequently, actions should be taken toimprove the conservation of these riparian forest remnants.

Disclosure statementNo potential conflict of interest was reported by the authors.

72 I. R. Gutierrez Flores and P. I. Becerra Osses

FundingThis work was supported by the CONICYT USA, under GrantNumber 2012–0011. Ivon R. Gutierrez Flores was a Masterfellow from PRONABEC – Peru at the time of data collectionand analyses. Pablo I. Becerra Osses thanks project FB 0002–2014.

Supplemental dataSupplemental data for this article can be accessed here.

Notes on contributorIvon R. Gutierrez Flores is a graduate student. She is interested inplant communities and the impact of economic activities onthem.

Pablo I. Becerra Osses is a professor. His main areas of researchinterest are biological invasions and restoration ecology.

References[CONAF] Corporación Nacional Forestal. 2011. Catastro de los

recursos vegetacionales nativos de Chile. Monitoreo de cam-bios y actualizaciones. Periodo 1997-2011. Santiago, Chile.

Altamirano A, Lara A. 2010. Deforestación en ecosistemas tem-plados de la precordillera andina del centro-sur de Chile.Bosque. 31:53–64.

Arévalo JR, Fernández-Palacios JM. 2005. Gradient analysis ofexotic Pinus radiata plantations and potential restoration ofnatural vegetation in Tenerife Canary Islands (Spain). ActaOecológica. 27:1–8.

Armesto JJ, Rozzi R, Arroyo MTK. 1998. Conservation targets inSouth American temperate forests. Science. 282:1271–1272.

Armesto JJ, Smith-Ramírez C, Rozzi R. 2001. Conservationstrategies for biodiversity and indigenous people in Chileanforest ecosystems. Journal of the Royal Society of NewZealand. 31:865–877.

Arya N, Ram J. 2013. Effect of canopy opening on species richnessin P.roxburghii Sarg (Chir-Pine) forests in UttarakhandHimalaya. Indian Journal of Research. 2:206–210.

Baker AC, Murray BR. 2012. Seasonal intrusion of litterfall fromnon-native pine plantations into surrounding native wood-land: implications for management of an invasive plantationspecies. Forest Ecology and Management. 277:25–37.

Battles JJ, Shliscky AJ, Barrett RH, Heald RC, Allen–Diaz BH.2001. The effects of forest management on plant speciesdiversity in a Sierran conifer forest. Forest Ecology andMangement. 146:211–222.

Becerra PI. 2006. Invasión de árboles alóctonos en una cuencapre-andina de Chile Central. Gayana Botanica. 63:161–174.

Becerra PI, Montenegro G. 2013. The widely invasive tree Pinusradiata facilitates regeneration of native woody species in asemi-arid ecosystem. Applied Vegetation Science. 16:173–183.

Becerra PI, Simonetti JA. 2013. Patterns of exotic species rich-ness of different taxonomic groups in a fragmented landscapeof central Chile. Bosque. 34:45–51.

Boothroyd IKG, Langer ER. 1999. Forest harvesting and ripar-ian management guidelines: a review. NIWA TechnicalReport. 56:58.

Boothroyd IKG, Quinn JM, Langer ER, Costley KJ, Steward G.2004. Riparian buffers mitigate effects of pine plantationlogging on New Zealand streams: 1. Riparian vegetation

structure, stream geomorphology and periphyton. ForestEcology and Management. 194:199–213.

Brockerhoff EG, Ecroyd CE, Leckie AC, Kimberley MO. 2003.Diversity and succession of adventive and indigenous vas-cular understorey plants in Pinus radiata plantation forestsin New Zealand. Forest Ecology and Management.185:307–326.

Burton PJ. 2002. Effects of clearcut edges on trees in the sub-boreal spruce zone of Nothwest-Central british Columbia.Silva Fennica. 36:329–352.

Bustamante R, Grez AA. 1995. Consecuencias ecológicas de lafragmentación de los bosques nativos. Ambiente YDesarrollo. 11:58–63.

Bustamante RO, Castor C. 1998. The decline of an endangeredtemperate ecosystem : the ruil (Nothofagus alessandrii) for-est in central Chile. Biodiversity and Conservation. 7:1607–1626.

Bustamante RO, Grez AA, Simonetti JA. 2006. Efectos de lafragmentación del bosque maulino sobre la abundancia ydiversidad de especies nativas. In: Grez AA, Simonetti JA,Bustamante RO, editors. Biodiversidad en ambientes frag-mentados de Chile. Patrones y procesos a diferentes escalas.Santiago (Chile): Editorial Universitaria. p. 83–97.

Bustamante RO, Serey IA, Pickett STA. 2003. Forest Fragmentation,plant regereneration and invasion processes across edges incentral Chile. Ecological Studies. 162:145–160.

Bustamante RO, Simonetti JA. 2005. Is Pinus radiata invadingthe native vegetation in central Chile? Demographicresponses in a fragmented forest. Biological Invasions.7:243–249.

Caccia FD, Chaneton EJ, Kitzberger T. 2009. Direct and indirecteffects of understorey bamboo shape tree regeneration nichesin a mixed temperate forest. Oecologia. 161:771–780.

Caldeira M, Ibáñez I, Nogueira C, Bugalho M, Lecomte X,Moreira A, Pereira J. 2014. Direct and indirect effects oftree canopy facilitation in the recruitment of Mediterraneanoaks. Journal of Applied Ecology. 51:349–358.

Chen J, Franklin JF, Spies TA. 1992. Vegetation responses toedge environments in Old-Growth Douglas-Fir Forests.Ecological Applications. 2:387–396.

Critchfield WB, Little EL. 1966. Geographic distribution of thePines of the World (N° 991). US Department of Agriculture,Forest Service. USA.

De La Vega X, Grez AA. 2008. Composición, riqueza de espe-cies y abundancia de insectos defoliadores de actividad noc-turna asociados a Aristotelia chilensis (maqui) en el bosquemaulino fragmentado. Revista Chilena De Historia Natural.81:221–238.

Didham RK, Lawton JH. 1999. Edge structure determines themagnitude of changes in microclimate and vegetation struc-ture in tropical forest fragments. Biotropica. 31:17–30.

Donoso DS, Grez AA, Simonetti JA. 2003. Effects of forestfragmentation on the granivory of differently sized seeds.Biological Conservation. 115:63–70.

Echeverria C, Coomes D, Salas J, Rey-Benayas JM, Lara A,Newton A. 2006. Rapid deforestation and fragmentation ofChilean Temperate Forests. Biological Conservation.130:481–494.

Echeverría C, Newton AC, Lara A, Rey JM, Coomes DA. 2007.Impacts of forest fragmentation on species composition andforest structure in the temperate landscape of southern Chile.Global Ecology And biogeograpgy. 16(4):426–439.

Estades CF, Escobar MA. 2005. Los ecosistemas de las planta-ciones de pino de la Cordillera de la Costa. In: Smith-Ramírez C, Armesto J, Valdovinos C, editors. Historia, bio-diversidad y ecología de los bosques costeros de Chile.Santiago (Chile): Editorial Universitaria. p. 600–616.

The effect of native forest replacement by Pinus radiata 73

Estades CF, Temple SA. 1999. Deciduos-forest bird communitiesin a fragmented landscape dominated by exotic pine planta-tions. Ecological Applications. 9:573–585.

Frank D, Finckh M. 1997. Impactos de las plantaciones de pinooregón sobre la vegetación y el suelo en la zona centro-sur deChile. Revista Chilena De Historia Natural. 70:191–211.

Franklin JF, Spies TA, Pelt RV, Carey AB, Thornburgh DA, BergDR, Lindenmayer DB, Hermon ME, Keeton WS, Shaw DC,et al. 2002. Disturbances and structural development of nat-ural forest ecosystems with silvicultural implications, usingDouglas-fir forests as an example. . Forest Ecology andManagement. 155:399–423.

Fuentes-Ramírez A, Pauchard A, Marticorea A, Sánchez P. 2010.Relación entre la invasión de Acacia dealbata Link(Fabaceae: mimosoideae) y la riqueza de especies vegetalesen el centro-sur de Chile. Gayana Botanica. 67:188–197.

Gajardo R. 1994. La vegetación natural de Chile. Clasificación ydistribución geográfica. Santiago (Chile): EditorialUniversitaria. p. 163.

Gómez P, Hahn S, San Martín J. 2009. Estructura y composiciónflorística de un matorral bajo plantaciones de Pinus radiataD.Don en Chile Central. . Gayana Botanica. 66:256–268.

Granados-Sánchez D, Hernández-García MA, López-Ríos GF.2006. Ecología de las Zonas Ribereñas. Revista Chapingo.. Serie Ciencias Forestales Y Del Ambiente. 12:55–69.

Graynoth E. 1979. Effects of logging on stream environmentsand faunas in Nelson. New Zealand Journal of Marine andFreshwater Research. 13:79–109.

Grez AA. 2005. El valor de los fragmentos pequeños de bosquemaulino en la conservación de la fauna de coleópterosepígeos. In: Smith-Ramírez C, Armesto JJ, Valdovinos C,editors. Historia, biodiversidad y ecología de los bosquescosteros de Chile. Santiago (Chile): Editorial Universitaria.p. 565–572.

Guerrero PC, Bustamante RO. 2007. Can native tree speciesregenerate in Pinus radiata plantations in Chile? Evidencefrom field and laboratory experiments. Forest Ecology andManagement. 253:97–102.

Gutiérrez AG, Armesto JJAravena JC. 2004. Disturbance andregeneration dynamics of an old-growth north patagonianrain forest in chiloé island,chile. Journal Of Ecology92:598–608.

Halpern CB, Evans SA, Nielson S. 1999. Soil seed banks inyoung, closed-canopy forests of the Olympic Peninsula,Washington: potential contributions to understory reinitia-tion. Canadian Journal of Botany. 77:922–935.

Harper KA, Macdonald SE. 2001. Structure and composition ofriparian boreal forest: new methods for analyzing edge influ-ence. Ecology. 82:649–659.

Harper KA, Macdonald SE, Burton PJ, Chen J, Brosofske KD,Saunders SC, Euskirchen ES, Roberts D, Jaiteh MS, EsseenPA. 2005. Edge influence on forest structure and composi-tion in fragmented landscapes. Conservation Biology.19:768–782.

Hobbs RJ. 2001. Synergisms among habitat fragmentation, live-stock grazing, and biotic invasions in SouthwesternAustralia. Conservation Biology. 15:1522–1528.

Huber A, Iroumé A, Mohr C, Frêne C. 2010. Efecto de planta-ciones de pinus radiata y Eucalyptus globulus sobre elrecurso agua en la Cordillera de la Costa en la región delBiobío. Chile. Bosque. 31(3):219–230.

Huth F, Wagner S. 2006. Gap structure and establishment ofSilver birch regeneration (Betula pendula Roth.) in Norwayspruce stands (Picea abies L. Karst.). Forest Ecology andManagement. 229:314–324.

Kanowski J, Catterall CP, Wardell-Johnson GW. 2005.Consequences of broadscale timber plantations for

biodiversity in cleared rainforest landscapes of tropicaland subtropical Australia. Forest Ecology andManagement. 208:359–372.

Kanowski J, Catterall CP, Wardell-Johnson W, Proctor H, Reis T.2003. Development of forest structure on cleared rainforestland in eastern Australia under different styles of reforesta-tion. Forest Ecology and Management. 183:265–280.

Langer ER, Steward GA, Kimberley MO. 2008. Vegetationstructure, composition and effect of pine plantation harvest-ing on riparian buffers in New Zealand. Forest Ecology andManagement. 256:949–957.

Leishman MR, Westoby M. 1994. The role of seed size inseedling establishment in dry soil conditions – experimentalevidence from semi arid species.pdf. Journal of Ecology.82:249–258.

Lindenmayer DB, McCarthy MA. 2001. The spatial distribution ofnon-native plant invaders in a pine–eucalypt landscape mosaic insouth-eastern Australia. Biological Conservation. 102:77–87.

Lindenmayer DB, McCarthy MA, Parris KM, Pope ML. 2000.Habitat fragmentation, landscape context, and mammalianassemblages in southeastern Australia. Journal ofMammalogy. 81:787–797.

Lusk CH, Donoso C, Jiménez M, Moya C, Oyarce G, Reinoso R,Saldaña A, Villegas P, Matus F. 2001. Descomposición dehojarasca de Pinus radiata y tres especies arbóreas nativas.Revista Chilena De Historia Natural. 74:705–710.

Marticorena C, Quesada M. 1985. Catálogo de la flora vascularde Chile. Gayana. 42:1–157.

Meers TL, Kasel S, Bell TL, Enright NJ. 2010. Conversion ofnative forest to exotic Pinus radiata plantation: responseof understorey plant composition using a plant functionaltrait approach. Forest Ecology and Management. 259:399–409.

Merino A, Fernández-López A, Solla-Gullón F, Edeso JM. 2004.Soil changes and tree growth in intensively managed Pinusradiata in northern Spain. Forest Ecology and Management.196:393–404.

Mueller-Dombois D, Ellenberg H. 1974. Aims and Methods ofVegetation Ecology. New York: Wiley.

Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA,Kent J. 2000. Biodiversity hotspots for conservation priori-ties. Nature. 403:853–858.

Naiman RJ, Bilby RE, Bisson PA. 2000. Riparian ecology andmanagement in the Pacific Coastal Rain Forest. BioScience.50:996–1011.

Neira E, Verscheure H, Revenga C. Chile´s Frontier Forests:conserving a Global Treasure. Chile: Universidad Australde Chile. p. 56.

Onaindia M, Ametzaga-Arregi I, San Sebastián M, Mitxelena A,Rodríguez-Loinaz G, Peña L, Alday JG. 2013. Can under-storey native woodland plant species regenerate under exoticpine plantations using natural succession?. Forest Ecologyand Management. 308:136–144.

Oyarzun CE, Peña L. 1995. Soil erosion and overland flow inforested areas with pine plantations at coastal mountainrange, central Chile. Hydrological Processes. 9:111–118.

Parris KM, Lindenmayer DB. 2004. Evidence that creation of aPinus radiata plantation in south-eastern Australia hasreduced habitat for frogs. Acta Oecologica. 25:93–101.

Pauchard A, Alaback B. 2004. Influences of evaluation, land useand landscape context on patterns of alien plant invasionsalong roadsides in protected areas of South- Central Chile.Conservation Biology. 18:238–248.

Pawson SM, Brockerhoff EG, Norton DA, Didham RK. 2006.Clear-fell harvest impacts on biodiversity: past research andthe search or harvest size thresholds. Canadian Journal ofForest Research. 36:1035–10446.

74 I. R. Gutierrez Flores and P. I. Becerra Osses

Pearson TRH, Burslem DFRP, Mullins CE, Dalling JW. 2002.Germination ecology of neotropical pioneers : interactingeffects of environmental conditions and seed size. Ecology.83:2798–2807.

Ramos C, Simonetti JA, Flores JD, Ramos-Jiliberto R. 2008.Modelling the management of fragmented forests: is it pos-sible recover the original tree composition? The case ofMaulino forest in Central Chile. Forest Ecology andManagement. 255:2236–:2243.

Ramovs BV, Roberts MR. 2003. Understory vegetation and envir-onment responses to tillage, forest harvesting, and conifer plan-tation development. Ecological Applications. 13:1682–1700.

Richardson DM. 1998. Forestry trees as invasive aliens.Conservation Biology. 12:18–26.

Richardson DM, Rejmánek M. 2004. Conifers as invasive aliens:a global survey and predictive framework. Diversity andDistributions. 10:321–331.

Richardson DM, Van Wilgen BW. 1986. Effects of thirty-fiveyears of afforestation with Pinus radiata on the compositionof mesic mountain fynbos near Stellenbosch. South AfricanJournal of Botany. 52:309–315.

Roberts MR, Zhu L. 2002. Early response of the herbaceiouslayer to harvesting in a mixed coniferous-deciduous forest inNew Brunswick, Canada. Forest Ecology and Management.155:17–31.

Rojas I, Becerra P, Gálvez N, Laker J, Bonacic C, Hester A.2011. Relationship between fragmentation, degradation andnative and exotic species richness in an Andean temperateforest of Chile. Gayana Botanica. 68:163–175.

Rozzi R, Armesto JJ, Figueroa J. 1994. Biodiversidad yconservación de los bosques nativos de Chile: unaaproximación jerárquica. Bosque. 15:55–64.

Santibáñez F, Uribe JM. 1993. Atlas Agroclimático de Chile:regiones sexta, séptima,octava y novena. Santiago:Ministerio de Agricultura. p. 99.

Schlatter JE, Otero L. 1995. Efecto de Pinus radiata sobre lascaracterísticas químico-nutritivas del suelo mineral superfi-cial. Bosque. 16:29–46.

Senbeta F, Teketay D. 2001. Regeneration of indigenous woodyspecies under the canopies of tree plantations in CentralEthiopia. Tropical Ecology. 42:175–185.

Simonetti JA, Grez AA, Bustamante RO. 2006. Interacciones yprocesos en el bosque maulino fragmentado. In: Grez AA,

Simonetti JA, Bustamante RO, editors. Biodiversidad enambientes fragmentados de Chile: patrones y procesos adiferentes escalas. Santiago (Chile): Editorial Universitaria.p. 99–114.

Simonetti JA. 2006. Conservación de biodiversidad en ambientesfragmentados: el caso del bosque maulino. In: Grez AA,Simonetti JA, Bustamante RO, editors. Biodiversidad enambientes fragmentados de Chile: patrones y procesos adiferentes escalas. Santiago (Chile): Editorial Universitaria.p. 213–229.

Simonetti JA, Moraes M, Bustamante RO, Grez AA. 2001.Regeneración de Bosques Troicales Fragmentados delBeni, Bolivia. In: Mostacedo B, Fredericksen T, editors.Regeneración y Silvicultura de Bosques Tropicales enBolivia. Santa Cruz (Bolivia): Editora el País. p. 140–155.

Tabacchi E, Lambs L, Guilloy H, Planty-Tabacchi AM, MullerE, Décamps H. 2000. Impacts of riparian vegetation onhydrological processes. Hydrological Processes. 14:2959–2976.

Thomas S, Halpern C, Falk D, Liguori D, Austin K. 1999. Plantdiversity in managed forests: understory responses tothinning and fertilization. Ecological Applications. 9:864–879.

Thysell DR, Carey AB 2000. Effects of forest management onunderstory and overstory vegetation : A retrospective study.PNW-GTR-448. 45pp.

Thysell DR, Carey AB. 2001. Manipulation of density ofPseudotsuga menziesii canopies: preliminary effects onunderstory vegetation. Canadian Journal of ForestResearch. 31:1513–1525.

Vazquez DP. 2002. Multiple effects of introduced mammalianherbivores in a temperate forest. Biological Invasions.4:175–191.

Williams MC, Wardle GM. 2005. The invasion of two nativeEucalypt forests by Pinus radiata in the Blue Mountains, NewSouth Wales, Australia. Biological Conservation. 125:55–64.

Williams MC, Wardle GM. 2007. Pinus radiata invasion inAustralia: identifying key knowledge gaps and researchdirections. Austral Ecology. 32:721–739.

Zhu J, Lu D, Zhang W. 2014. Effects of gaps on regeneration ofwoody plants: A meta-analysis. Journal of Forestry Research.25:501–510.

The effect of native forest replacement by Pinus radiata 75