Conservation of forest biodiversity and ecosystem propertiesin a pastoral landscape of the Ecuadorian Andes

Chloe MacLaren • Hannah L. Buckley •

Roddy J. Hale

Received: 29 April 2013 / Accepted: 14 March 2014 / Published online: 1 April 2014

� Springer Science+Business Media Dordrecht 2014

Abstract High Andean cloud forests are home to a

diversity of unique wildlife and are important provid-

ers of ecosystem services to people in the Andean

regions. The extent of these cloud forests has been

widely reduced through conversion to pasture for

livestock, which threatens the forests’ ability to

support biodiversity and provide ecosystem services.

This paper explores whether impacts on woody plant

biodiversity and four ecosystem properties (woody

plant species richness, juvenile timber tree abundance,

soil organic matter content and soil moisture) from

converting forest to pasture can be mitigated if some

woody forest vegetation is maintained within pastures.

Woody vegetation in pastures was found to conserve

those woody plant species that are more tolerant to

exposure and grazing, but conservation of the high

montane cloud forest community required areas of

forest from which livestock were restricted. The

sampled sites clustered according to woody plant

species cover; these clusters represented a gradient

from pasture with patches of shrubs to mature forest.

Clusters differed in both woody plant species richness

and number of juvenile timber trees whereas soil

organic matter and soil moisture were observed to be

similar among all clusters. This suggests that the

different habitats may have some equivalent

ecosystem properties. We conclude that the presence

of woody vegetation in pastures may reduce some of

the impacts of converting forest to pasture, but should

not be considered a substitute for protecting large

areas of forest, which are essential for maintaining

woody plant species diversity in high Andean cloud

forest.

Keywords Conservation � Ecosystem

properties � Pasture � Forest �Woody vegetation �Andes

Introduction

Natural forests are fundamental to the conservation of

global biodiversity and ecosystem services (Pearce

2001; Lal 2004; Foley et al. 2007). Forests store

carbon (Lal 2004), regulate hydrology, climate and

soil nutrients (Reiners et al. 1994; Pearce 2001; Lal

2004; Foley et al. 2007; Ford et al. 2011), provide

timber, food and medicinal resources (Pearce 2001),

and provide habitat for a large number of species

(Gardner et al. 2009; Baez et al. 2010). However,

forested land is still in demand for agriculture, and

rapid deforestation continues worldwide, leading to

massive biodiversity losses and diminishing ecosys-

tem service provision (Pearce 2001; FAO 2010).

However, several authors are now proposing that these

declines can be mitigated by the use of agroecological

or ‘wildlife-friendly’ farming techniques, which aim

C. MacLaren � H. L. Buckley � R. J. Hale (&)

Department of Ecology, Lincoln University,

PO Box 85084, Lincoln 7647, Canterbury, New Zealand

e-mail: Roddy.Hale@lincoln.ac.nz

123

Agroforest Syst (2014) 88:369–381

DOI 10.1007/s10457-014-9690-9

to allow the persistence of native biodiversity in and

around the farming system (e.g., Scherr and McNeely

2008; Tscharntke et al. 2012).

One form of ‘wildlife-friendly’ farming is the

incorporation or retention of native trees into the

agricultural system to at least partially retain the

habitat attributes of natural forest (e.g., shading,

structural complexity) (Perfecto et al. 2005; Waldron

et al. 2012). In the Andes of Ecuador, it is common

practice to leave scattered remnant trees and forest

patches throughout highland pastoral landscapes, and

many farmers also allow shrubs and trees to

regenerate in their pastures (MacLaren, pers. obs).

This remnant and regenerating woody vegetation

may provide some habitat value for forest biodiver-

sity and conserve some forest ecosystem services

within pastoral landscapes. In this study, we inves-

tigated biodiversity and ecosystem service values of

woody vegetation in pastures of the upper Papallacta

valley, which lies on the eastern slopes of the

Ecuadorian Andes.

The native vegetation of the upper Papallacta valley

is high montane cloud forest, also referred to as ‘elfin

forest’ (Lauer and Rafiqpoor 2000), ‘montane ceja’

(Paniagua Zambrana et al. 2003), ‘high montane

evergreen forest’ (Salgado 2008) and ‘humid high

montane forest’ (Pillajo and Pillajo 2010). High

montane cloud forest is valued for its high biodiversity

(Baez et al. 2010), and is known to provide several

important ecosystem services. For the local people, the

forests are a source of income from tourism (native

charismatic species include the spectacled bear,

Tremarctos ornatus, and the mountain tapir, Tapirus

pinchaque), and a source of traditional resources such

as timber, foods, and medicines (Baez et al. 2010;

Pillajo and Pillajo 2010). These forests are also known

to be important in regulating local hydrology, partic-

ularly in terms of precipitation interception and

infiltration (Ataroff 2002).

Pastoral agriculture is the most widespread cause of

forest loss throughout the Andes (Jokisch and Lair

2002; Sarmiento 2002; Rodrıguez Morales 2009). In

the upper Papallacta valley the only extensive areas of

forest remain on the steep hillsides, and throughout

Ecuador, high montane cloud forest has been almost

entirely cleared from its range (Jokisch and Lair 2002;

Sarmiento 2002). When forest is converted to pasture,

local environmental conditions are altered by the

removal of the canopy cover and the loss of the

biogeochemical interactions between trees and soil

(Reiners et al. 1994; Holl 2006). This resulting open

pasture environment is likely to favour a different set

of plant species than those adapted to sheltered forest

conditions (Reiners et al. 1994). Any regenerating

vegetation in pasture areas is also subject to grazing

(Pettit et al. 1995; Posada et al. 2000), competition

with introduced pasture grasses (Sarmiento 1997), and

regular clearance by farmers, which may further

reduce the number of plant species that are capable

of survival.

The environment of adjacent forest can also be

affected by pasture, via edge effects. These manifest as

variety of changes to the physical environment of the

forest edges, such as increased light levels, and

increased variability in temperature and humidity

(Murcia 1995). Consequently, plant community com-

position is often found to vary between the edges and

interiors of habitat patches, with forest edges tending

to be dominated by a less diverse group of pioneer

species (Oosterhoorn and Kappelle 2000; Saunders

et al. 1991; Laurance et al. 2006; Tabarelli 2008;

Broadbent et al. 2008). Forest fragments that are small

relative to the extent of edge effects can have their

original community entirely displaced by ‘edge’

vegetation (Harrison and Bruna 1999; Tabarelli et al.

2008). Small forest fragments may also be less diverse

due to their size and isolation; smaller fragments

typically contain smaller populations, so there is a

higher probability of extinction through stochastic

processes (Collinge 2009). Isolation reduces the

number of seeds dispersing to a patch from other

patches, because the distance reduces the probability

of seeds arriving at the patch (Tscharntke et al. 2005;

Collinge 2009). Overall, increasing fragmentation of

forested landscapes tends to reduce biodiversity, and

drive the remaining plant communities toward pio-

neer-dominated communities (Tabarelli et al. 2008).

In this study, we aim to quantify the impacts of

agriculture on high montane cloud forest by investi-

gating how the woody plant community varies in

relation to agricultural intensity. Increased agricultural

intensity was represented by decreased vegetation

density (a surrogate for forest clearance) and increased

grazing intensity, as these are major impacts of

pastoral agriculture. Community composition was

also investigated in relation to altitude because this

is a well-known driver of compositional variation in

Andean vegetation (Young 1993; Lauer and Rafiqpoor

370 Agroforest Syst (2014) 88:369–381

123

2000; Salgado 2008). The specific questions addressed

in this study are: (1) how does the high montane forest

community differ between areas of low agricultural

intensity and high agricultural intensity, and (2) is

leaving woody vegetation in pastures an effective

method for conserving forest biodiversity within the

pastoral landscape?

The conversion of high montane cloud forest to

pasture is also likely to affect the ability of these

landscapes to provide ecosystem services. There is

evidence that climax forest communities provide a

greater supply and diversity of ecosystem services

than disturbed pioneer plant communities (Foley et al.

2007; Tabarelli et al. 2008) and that the focus on food

production in agricultural landscapes means other

ecosystem services, such as soil conditioning and

forest resource provision, are marginalised (Foley

et al. 2005). In this study we measured four ecosystem

properties, which are considered to represent the levels

of ecosystem service provision in different vegetation

types: species richness, which is linked to the overall

diversity and stability of ecosystem services

(Tscharntke et al. 2005; Isbell et al. 2011; Quijas

et al. 2012); soil organic matter content, which is a

reflection of soil nutrient status and carbon storage

(Lal 2009; Dominati et al. 2010); soil moisture

content, from which we gain an insight into the effects

of vegetation on local hydrology; and the abundance

of juvenile trees of timber species, which provides an

indication of the future timber supply. All ecosystem

properties were expected to be higher in forested areas

than in pasture areas, but retaining woody vegetation

in pastures could reduce this difference.

Methods

Data were collected between latitudes 0�22012500 and

0�23011000, and longitudes 78�9053500 and 78�11015000.The minimum altitude was 3,355 m.a.s.l, and the

maximum altitude was 3,752 m.a.s.l. All data were

collected from 83, 10 9 10 m (0.1 ha) quadrats

spread along the upper Papallacta valley in layout

aimed to be representative of the different vegetation

types and different levels of agricultural intensity.

Sites were placed at a minimum distance of 50 m apart

to reduce the effects of spatial autocorrelation.

The geographical coordinates and altitude (in

metres above sea level) of each site were recorded

using a Garmin eTrex 20 handheld GPS device.

Within each quadrat, percent canopy cover was

visually estimated from the centre point, and the

number of droppings from cattle, sheep, horses or

goats were counted. The area covered by forest within

a 100 m radius of the sample site was calculated using

ArcMap 10 (ESRI 2011), based on satellite imagery

from Google Earth (2012). The different vegetation

types (including forest, pasture, and pasture with

woody vegetation) were ground-truthed at each site

and at a variety of other points across the study area.

The abundance of every woody plant species

observed was recorded for each sample site. Only

plants taller than 30 cm in height were recorded, so

that only established individuals were included. Plant

species were identified using the illustrated guidebook

by Pillajo and Pillajo (2010), and plants not included

in the guidebook were later identified at the National

Herbarium of Ecuador. The number of juveniles of

potential timber tree species was also recorded at each

site. A juvenile tree was defined as being greater than

30 cm in height but less than 2.5 m in height or less

than 10 cm in breast-height diameter. Species were

designated as potential timber species if they regularly

grow large enough and have sufficiently durable wood

to be useful as a fencepost, or for larger constructions

(Pillajo and Pillajo 2010; pers. obs.). Twelve species

were identified as useful timber resources in the upper

Papallacta valley: Buddleja species, Escallonia myr-

tilloides, Grosvenoria rimbachii, Gynoxys spp., Hesp-

eromeles obtusifolia, Hesperomeles ferruginea,

Miconea bracteolata, Oreopanax ecuadorensis, Sara-

cha quitensis, Sessea crassifolia, and Vallea

stipularis.

At a subset of 40 sites, soil samples were taken from

the centre point and analysed at the Agrocalidad soil

laboratory in Tumbaco, Ecuador, for percent volu-

metric content of organic matter and percent gravi-

metric humidity.

Data analysis

Agglomerative cluster analysis (Bray-Curtis/Sørenson

distance), in conjunction with indicator species ana-

lysis, was undertaken in PC-ORD (McCune and

Mefford 2011) to group sites together based on their

community composition. Differences between each of

the clusters were assessed by calculating an inverse

Morisita-Horn Index, an index that is robust to high

Agroforest Syst (2014) 88:369–381 371

123

variability in plant abundances between sites (Magur-

ran 2004). Values of this index close to 0 indicate high

similarity and values close to 1 indicate low similarity.

Nonmetric multidimensional scaling (NMS) was

used to identify patterns in compositional variation

among sites (following Peck 2010 and Kent 2012).

Regression models were employed to determine which

environmental variables correlated with the changes in

plant community composition represented by each

axis of the NMS ordination. A generalised least

squares (GLS) regression approach was used because

this accounts for autocorrelation in the response

variable (Crawley 2007), which is often present in

ecological datasets where sample sites close together

can be more similar to each other than more distant

sites. One model was developed for each of the

significant NMS axes, with the response variable of

each model being the site scores of each axis from the

NMS ordination. The explanatory variables included

in the model were altitude, percent canopy cover,

livestock dropping density, and the proportion of area

within a 100 m radius of each site covered by forest.

All continuous explanatory variables were standard-

ised to a mean of zero and a standard deviation of one

before entering them into the model, so that the

regression coefficients were not affected by variables

of different scales.

Plots of the residuals and fitted values were used to

test the assumption of a linear relationship between the

explanatory variables and the response, and to check

for homoscedasticity in the response. Normal quan-

tile–quantile (QQ) plots were used to test the assump-

tion of normality in the residuals, and semivariograms

were used to check for the presence of spatial

autocorrelation in the residuals.

Analysis of variance was used to compare levels of

ecosystem properties among the community types

identified by the cluster analysis pairwise comparisons

were made using Tukey’s Honest Significant Differ-

ence in R (R Core Team 2012).

Results

Community types

A total of 65 plant species (Appendix) occurred in the

83 sample sites. Sites were assigned to nine clusters, as

using nine clusters resulted in the highest number of

significant indicator species associated with each

cluster. Four of these clusters contained three or fewer

members, resulting in an insufficient sample size to

determine any characteristic features of those clusters.

For this reason, these four clusters were excluded from

all further analyses.

The five common clusters were given descriptive

names based on some of their defining features: ‘high

altitude disturbed vegetation’, ‘low altitude disturbed

vegetation’, ‘mature forest’, ‘shrubby pasture’, and

‘regenerating pasture’ (Table 1). The ‘high altitude

disturbed’ cluster was found consistently in the upper

part of the valley (above 3,580 m.a.s.l.) and was

labelled ‘disturbed’ as member sites were typically

found in areas exposed to some agricultural pressure,

including pasture with woody vegetation, small forest

fragments, or forest sites near to the edge of forests.

Two points from this cluster were further into the

interior of the forest than the rest of the member sites.

These two sites were both beneath canopy gaps with

percent canopy covers of 50 and 60 %, which were

unusually low for forest sites in the Papallacta valley

study site. The ‘low altitude disturbed’ cluster was also

Table 1 Characteristics of each community type

Cluster Typically

occurs in

%

Canopy

cover

Altitude

(m.a.s.l.)

Mature forest Undisturbed

forest

interior

60–74 3,494–3,679

High altitude

disturbed

vegetation

Forest edges 15–51 3,574–3,634

Small forest

fragments

Pasture with

scattered

trees

Low altitude

disturbed

vegetation

Forest edges 30–66 3,414–3,510

Small forest

fragments

Pasture with

scattered

trees

Regenerating

pasture

Pasture with

scattered

trees

10–18 3,378–3,608

Open pasture

Shrubby pasture Open pasture 0 3,421–3,616

The interquartile range is given for % canopy cover and

altitude

372 Agroforest Syst (2014) 88:369–381

123

found in pasture with woody vegetation, small forest

fragments, or near to the edges of forests, but at lower

altitudes (generally below 3,520 m.a.s.l.). This cluster

contained several points that were inside forest areas;

however, all of these sites were accessible to cattle and

other livestock. The ‘mature forest’ group contained

sites that were located in interior forest locations and

these sites were protected from cattle and livestock

entry by small cliffs or impenetrable thickets of vines

and shrubs (MacLaren, pers. obs). The group labelled

‘shrubby pasture’ was made up of sites that were

essentially open pasture, with a variety of shrubs

present but little or no tree cover. The ‘regenerating

pasture’ cluster was named for its high abundance of

Baccharis latifolia (Table 2), a small tree species that

can regenerate easily in open areas (Pillajo and Pillajo

2010).

None of the community types shared more than

51 % similarity with any other cluster. The ‘mature

forest’, ‘high altitude disturbed’ and ‘low altitude

disturbed’ forests were most similar to one another,

with around 50 % similarity (Table 3). ‘Shrubby

pasture’ sites were most similar to ‘high altitude

disturbed’ sites and ‘regenerating pasture’ was most

similar to ‘low altitude disturbed’ sites, but the

similarity is weak in both cases (both have an inverse

Morisita-Horn index of 0.71, indicating only a 29 %

similarity between community types; Table 3). Sev-

eral species were found to occur significantly more

frequently and abundantly in certain clusters, and

these can be considered indicator species for those

clusters (Table 2). ‘Shrubby pasture’ had no signifi-

cant indicator species (Table 2), suggesting that this

cluster was more defined by a shared absence of

species than the presence of any particular species.

Patterns in community composition

The NMS ordination identified three relevant axes that

described the variation between the species assem-

blages of each plot (Fig. 1). Axis 1 was found to

explain approximately 30 % of the variance, while

both axis 2 and axis 3 explained approximately 20 %

each. Sites within the five common clusters are fairly

well separated in ordination space. Notably, ‘shrubby

pasture’ occurs at low values on axis 1 while ‘mature

forest’ occurs at high values, and ‘high altitude

disturbed’ sites occur at low values of axis 2 while

‘low altitude disturbed’ sites were present at high

values of axis 2. These trends were supported by the

regression models; all measures associated with

agricultural intensity including canopy cover, percent

surrounding forest cover, and number of animal

droppings, were significantly related to the first axis

of the NMS ordination (P \ 0.05; Table 4). Altitude

was significantly related to the second axis

(P \ 0.001; Table 4). No significant variables were

identified for the third axis (Table 4). None of the

three models (one for each axis) were found to violate

any model assumptions.

Table 2 Indicator species associated with each cluster

Cluster Species Growth form Indicator Value P value

Mature forest Calceolaria lamiifolia Climber 52.9 0.03

Munnozia jussieui Climber 51.7 0.02

Oreopanax ecuadorensis Tree 58.7 0.01

Monnina species Tree 45.2 0.04

High altitude disturbed vegetation Gynoxys (small-leafed morphotype) Tree 44.8 0.04

Miconia salicifolia Tree 62.6 0.00

Muehlenbeckia tamnifolia Climber 74.4 0.00

Ribes ecuadorensis Climber 66.1 0.00

Rubus species Climber 45.7 0.00

Salpichroa tristis Climber 46.5 0.01

Low altitude disturbed vegetation Jungia rugosa Climber/shrub 60.4 0.01

Solanum asperolatum Tree 75.2 0.00

Regenerating pasture Baccharis latifolia Tree 44.4 0.04

Shrubby pasture None – – –

Agroforest Syst (2014) 88:369–381 373

123

Table 3 Inverse Morisita-Horn index (beta-diversity) measures for each pairwise comparison of clusters

High altitude disturbed veg. Low altitude disturbed veg. Regenerating pasture Shrubby pasture

Mature forest 0.52 0.49 0.79 0.94

High altitude disturbed veg. 0.56 0.85 0.71

Low altitude disturbed veg. 0.71 0.81

Regenerating pasture 0.89

Values close to 1 indicate dissimilar community composition and abundance between cluster pairs

Fig. 1 The NMS ordination

plots showing community

composition in relation to

the NMS axes. Notable

trends include a shift from

the ‘shrubby pasture’

community type to ‘mature

forest’ along the first axis,

and from ‘high altitude

disturbed vegetation’ to

‘low altitude disturbed

vegetation’ along the second

axis. No particular trends are

obvious in relation to the

third axis, despite the

statistical significance of

this axis in the ordination

Table 4 Regression coefficients (‘Coeff.’) and P values (‘P’) for each explanatory variable in each axis model

Axis 1 Axis 2 Axis 3

Coeff. P Coeff. P Coeff. P

Altitude 0.05 0.250 -0.39 0.000 -0.08 0.146

Canopy cover 0.31 0.000 0.02 0.808 -0.03 0.657

Surrounding forest cover 0.17 0.015 0.08 0.234 -0.1 0.388

Number of droppings -0.15 0.005 0.02 0.741 -0.05 0.206

The three models are listed across the top of the table, and the explanatory variables are in the left-hand column. Positive coefficient

values indicate a positive relationship, negative values an inverse relationship with each NMS axis

374 Agroforest Syst (2014) 88:369–381

123

Fig. 2 Box plots showing

the differences between

groups in a species richness,

b timber regeneration, c soil

organic matter and d soil

moisture content. For

species richness, mature

forest, high altitude

disturbed vegetation and

low altitude disturbed

vegetation) were all

significantly different from

both pasture types (Tukey’s

HSD, P \ 0.001). For

timber regeneration, high

edge forest was significantly

different from all

community types except for

mature forest (Tukey’s

HSD, P \ 0.001). There

were no significant

differences for either of the

soil property measures

Agroforest Syst (2014) 88:369–381 375

123

Ecosystem properties

Significant differences in ecosystem properties among

community types were identified for species richness

(F(4,71) = 18.43, P \ 0.001) and timber regeneration

(F(4,71) = 11.55, P \ 0.001) (Fig. 2). Similar levels of

higher species richness were observed in mature forest,

high-altitude edge and low-altitude edge sites compared

to pasture-dominated sites (Fig. 2a). The three forested

cluster types tended to have higher and more variable

numbers of juvenile woody trees than the pasture-

dominated sites (Fig. 2b). There is some suggestion that

both soil ecosystem properties were lower in pasture

areas and higher in forested areas (Fig. 2c and d), but

these trends were not significant at the 5 % level.

Discussion

Five common and distinct plant community types

were identified in the upper Papallacta valley. Only

one occurred in undisturbed forest (‘mature forest’).

The other four community types were found in areas

influenced by agriculture, ranging from forest edges to

pasture areas with just a few woody shrubs. The

similarity of the plant communities to the mature

forest community decreased as canopy cover

decreased, grazing increased, and isolation from forest

increased. In addition, the number of juvenile trees and

woody plant species richness were higher in plant

communities that were more similar to the mature

forest community. These findings suggest that rem-

nant and regenerating vegetation is most effective for

woody plant biodiversity conservation when the

vegetation is present at high densities, when grazing

is kept to a minimum, and when large areas of forest

are conserved to act as source populations.

Grazing is known to reduce the presence of those

species that are most palatable to livestock and least

resilient to herbivory, whilst favouring an increase in

unpalatable and resilient species (Pettit et al. 1995;

Burns et al. 2011). Given that all member sites of the

mature forest cluster were known to be inaccessible to

cattle, while most disturbed vegetation sites were not, it

appears that grazing is a major edge effect that alters

forest communities within the upper Papallacta valley.

This is supported by the significance of livestock

dropping density, a proxy for grazing intensity, in

explaining vegetation composition (Table 3). Increased

light levels also likely play a role in determining

vegetation composition because canopy cover

explained significant variation, and the only two

disturbed vegetation sites that were not accessible to

cattle were found beneath canopy gaps. Most forest

communities have a suite of light-demanding species

that colonise treefall gaps and other open areas; these

also tend to be the species that survive on forest edges

and in forest fragments (Laurance et al. 2006).

The low levels of disturbance resulting from the edge

effects of grazing and increased light levels around

pastures caused a major change in community compo-

sition from mature forest to disturbed vegetation; neither

of the disturbed communities shared more than 51 %

similarity with mature forest (Table 3). However, the

disturbed plant communities were resilient to further

increases in agricultural pressure; both occurred

throughout areas of pasture with scattered trees, where

canopy cover was often substantially reduced and

grazing pressure often high, as well as in relatively

undisturbed forest edges (Table 1). This finding is

consistent with other studies of community responses to

agriculture, which show that undisturbed forest com-

munities tend to contain a group of highly forest-

dependent species, which disappear from the system

even at very low levels of agricultural intensity, while

other species of the same communities may be resistant

to relatively high agricultural intensity (Perfecto et al.

2005; Phalan et al. 2011; Pineda-Diez et al. 2012).

The amount of forest within a 100 m radius of a site

also affected the plant community structure, with sites

surrounded by greater amounts of forest being more

similar to the mature forest community (Table 3).

Forests provide a source of seeds, and can also be a

source of ecosystem functions such as pollination and

seed dispersal when it provides habitat for the

organisms that carry out these functions (Oosterhoorn

and Kappelle 2000; Jesus 2012). Therefore, these

source effects tend to increase the number and

diversity of species which establish in sites near to

forest in comparison with sites distant from forest

(Tscharntke et al. 2005; Collinge 2009) as found here.

Variation in relation to altitude was most obvious in

disturbed areas rather than in undisturbed forest. The

disturbed plant community in the upper Papallacta

valley is separated into two different community types

by altitude (the ‘low altitude disturbed’ type generally

occurring below 3520 m.a.s.l and the ‘high altitude

disturbed’ type generally occurring above 3580 m.a.s.l)

376 Agroforest Syst (2014) 88:369–381

123

while the mature forest community is found within both

altitudinal bands. This suggests that the creation of open

pasture environments generates more altitudinal varia-

tion than would otherwise be observed. The high

altitude disturbed vegetation was rich in plant species

generally associated with the treeline, or with the alpine

shrublands and grasslands (paramo) above the treeline.

These are more open environments than the forest, and

so plants from these high altitude habitats are likely to be

more suited to colonising edges than lower altitude

species. Without agriculture, the study area would be

entirely forested (it lies below the treeline at

3800 m.a.s.l.) and these open environment species

would not be able to establish, so the overall variation

would be limited to forest species. Such artificial

extensions of paramo species to lower altitudes is

thought to be widespread throughout the Andes as a

result of clearing forest for pasture (Sarmiento 2002).

The trends described so far indicate that forest

clearance and grazing in the upper Papallacta valley

lead to a change away from a mature cloud forest

community to an exposure-tolerant community. How-

ever, it may be possible for populations of some forest

species to survive in pasture under the right circum-

stances. In the regenerating pasture community, the

growth of pioneer plants may be aiding the regener-

ation of a wide range of other species, including forest

species such as O. ecuadorensis. The regenerating

pasture community is dominated by B. latifolia, a

small pioneer tree species that has previously been

found to promote the growth of seedlings of more

sensitive species (Posada et al. 2000). The branched

growth form of B. latifolia means that it protects the

area beneath its canopy from grazing and from

climatic exposure (Posada et al. 2000). Other plants

found in this community type with similar growth

forms (e.g., Berberis grandifolia and Barnadesia

arborea; MacLaren, pers. obs) may perform the same

function. This protection effect has been identified as

important for the regeneration of trees within wooded

pastures in Europe (Uytvanck et al. 2008), and could

be useful to promote the regeneration of forest trees

within pastoral areas of the upper Papallacta valley.

Community types and ecosystem properties

All ecosystem properties indicated higher ecosystem

service provision in mature forest and in both high and

low disturbed vegetation sites than in the pasture

community groups (Fig. 2). Notably, the high level of

timber regeneration occurring in the disturbed plant

communities, which included pasture with scattered

trees and small forest fragments, suggests that main-

taining trees and forest patches within the pastoral

landscape could be beneficial for protecting previ-

ously undisturbed forest from disturbance for timber

removal. The felling of forest trees for fenceposts is

known to be one of the greatest threats to forests

neighbouring agricultural areas of South America

(Murgueitio 2004). Post-and-wire fencing is widely

used in the upper Papallacta valley, so if trees are

completely cleared from pastures then farmers are

likely to seek timber in neighbouring forests.

The higher species richness found in forest frag-

ments and scattered tree communities compared with

open pasture communities may be beneficial to farmers.

Biodiversity is strongly linked to ecosystem service

provision (Quijas et al. 2010; Naeem et al. 2012), and

retaining biodiversity within pastoral areas may have

benefits for ecosystem services such as soil nutrients

(Murgueitio et al. 2011), beneficial insects (Bianchi

et al. 2006), and the productivity and nutritional value

of pasture herbs (Sanchez-Jardon et al. 2010). However,

further research is necessary because the relationship

between biodiversity and ecosystem services is known

to be complex and generally non-linear, with certain

species contributing more services than others

(Tscharntke et al. 2005; Bommarco et al. 2013). The

conservation of specific ecosystem services will require

a detailed knowledge of the relationship of those

services with different species and communities, and

with different land management scenarios.

Although the soil ecosystem properties suggested

that the mature forest and disturbed vegetation com-

munities provide greater organic matter and soil

moisture retention than open pasture communities,

this result was not significant. These ecosystem

properties would benefit from a more thorough study,

as it has been widely found in the literature that tree

cover can increase both soil organic matter and soil

moisture content in agricultural areas (Moreno 2008;

Jose 2009; Murgueitio et al. 2011).

Conclusions

The findings of this study indicate that agricultural

disturbance has had a large impact on the forest

Agroforest Syst (2014) 88:369–381 377

123

vegetation of the upper Papallacta valley and that

conservation of the mature cloud forest community

can only occur in a closed forest environment in

the absence of grazing. Protecting large forest

areas from further clearance should be a priority

for the conservation of high montane cloud forest

throughout the Ecuadorian Andes. It would also

help to encourage farmers to keep livestock out of

forested areas because this would eliminate the

edge effects caused by grazing (Burns et al. 2011).

If large forest areas cannot be protected, then

some of the loss of biodiversity caused by clearing

forest for pasture could be mitigated by retaining

scattered trees and forest fragments. These types

of vegetation are useful for the conservation of

plant species that are tolerant of higher light levels

and of grazing and may also be beneficial to the

farmers in terms of ecosystem services, notably as

a timber supply. In sum, scattered trees and forest

fragments in pastoral areas are a ‘wildlife-friendly’

solution for some species and some ecosystem

services, but the survival of the Andean cloud

forest will depend on the protection of large forest

areas.

Acknowledgments This study would have been impossible

without the advice and logistical assistance received from the

PRAA Project Team (Papallacta) of Care International, under

the auspices of the Ecuadorian Ministry of the Environment.

Thank you also to the communities of Tambo and Jamanco, on

whose properties this research was undertaken. Thanks to Pablo

Dominguez for help in the field, to Diana Fernandez of the

National Herbarium of Ecuador for help with identifying plants,

and to Brad Case for his assistance with spatial data and

calculations. Suggestions and advice from the Lincoln

University Spatial Ecology Group were invaluable during the

planning and analysis of this project. MacLaren was funded by a

Lincoln University postgraduate scholarship. The authors are

grateful to two anonymous reviewers, whose comments

improved this manuscript.

Appendix

Family Genus Species Authority Local name

Rosaceae Acaena elongata L.

Asteraceae Baccharis buxifolia (Lam.) Pers.

Asteraceae Baccharis latifolia (Ruiz & Pav.) Pers. Chilco

Asteraceae Baccharis nitida (Ruiz & Pav.) Pers.

Asteraceae Baccharis prunifolia Kunth Chilco del cerro

Asteraceae Barnadesia arborea Kunth Alfilero

Scrophulariaceae Berberis grandiflora Turcz. Espino amarillo

Pterophyta Blechnum sp.

Melastomataceae Brachyotum ledifolium (Desr.) Triana Zarcilejo blanco

Scrophulariaceae Buddleja sp. Quijuar

Calceolariaceae Calceolaria lamiifolia Kunth Zapatitos

Campanulaceae Centropogon glabrifilis E. Wimm. Hierba de danta

Bambusoideae Chusquea scandens Kunth Bambu

Nyctaginaceae Colignonia ovalifolia Heimerl

Coriariaceae Coriaria ruscifolia L. Shanshi

Asteraceae Dendrophorbium lloense (Hieron ex Sodiro) C. Jeffrey Isca

Asteraceae Diplostephium floribundum (Benth.) Wedd.

Ericaceae Disterigma acuminatum (Kunth) Nied. Yurak muyu

Escalloniaceae Escallonia myrtilloides L.f. Chachaco

Onagraceae Fuchsia spp. Arete de monte

Asteraceae Gnaphalium elegans Kunth

378 Agroforest Syst (2014) 88:369–381

123

continued

Family Genus Species Authority Local name

Bromeliaceae Greigia mulfordii L.B. Sm. Pinuelos

Asteraceae Grosvenoria rimbachii (B.L. Rob) R.M. King & H. Rob. Pussu pato

Asteraceae Gynoxys sp. (large leaves) Piquil

Asteraceae Gynoxys sp. (small leaves) Piquil

Rosaceae Hesperomeles ferruginea (Pers.) Benth Pujın

Rosaceae Hesperomeles obtusifolia (Pers.) Lindl. Wakra manzano

Asteraceae Heterocondylus vitalbae (D.C.) R.M. King & H. Rob.

Clusiaceae Hypericum laricifolium Juss. Romerillo

Solanaceae Jaltomata viridiflora (Kunth) M. Nee & Mione Ushaki

Asteraceae Jungia rugosa Less. Cutzato

Asteraceae Lasiocephalus sp.

Asteraceae Llerasia sp.

Fabaceae Lupinus pubescens Benth. Sacha chochos

Melastomataceae Miconia bracteolata (Bonpl.) DC. Alamoja

Melastomataceae Miconia crocea (Desr.) Naudin Colca

Melastomataceae Miconia salicifolia (Bonpl. ex Naudin) Naudin Sauce

Lamiaceae Minthostachys mollis Griseb. Tipo

Poligalaceae Monnina spp. Azulina

Polygonaceae Muehlenbeckia tamnifolia (Kunth) Meisn. Anku yuyu

Polygonaceae Muehlenbeckia tiliifolia Wedd.

Asteraceae Munnozia jussieui (Cass.) H. Rob & Brettell

Araliaceae Oreopanax ecuadorensis Seem. Pumamaki

Fabaceae Otholobium mexicanum (L.f.) J.W. Grimes

Passifloraceae Passiflora mixta L.f. Sacha taxo

Asteraceae Pentacalia arbutifolia (Kunth) Cuatrec.

Ericaceae Pernettya prostrata (Cav.) DC. Taglli

Piperaceae Piper nubigenum Kunth Luncug

Rosaceae Polylepis pauta Hieron. Arbol de papel

Dennstaedtiaceae Pteridium spp.

Saxifragaceae Ribes ecuadorensis Janczewski Sacha manzano

Rosaceae Rubus spp. Mora

Solanaceae Salpichroa tristis Miers Chulalik

Solanaceae Saracha quitensis (Hook.) Miers

Solanaceae Sessea crassivenosa Bitter.

Campanulaceae Siphocampylus lucidus E. Wimm. Pukunero

Solanaceae Solanum asperolatum Ruiz & Pav. Urku Wantuk

Solanaceae Solanum brevifolium Dunal Mitsa muyu

Solanaceae Solanum nigrescens M. Martens & Galeotti Hierba mora

Ranunculaceae Thalictrum podocarpum Kunth Moradilla

Urticaceae Urtica leptophylla Kunth Ortiga

Valerianaeceae Valeriana microphylla Kunth Valeriana

Elaeocarpaceae Vallea stipularis L. Sacha capuli

Asteraceae Verbesina lloensis Hieron. Mimisca

Agroforest Syst (2014) 88:369–381 379

123

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