Agriculture, Ecosystems and Environment 236 (2017) 221233

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Agriculture, Ecosystems and Environment

journal homepage: www.elsevier.com/locate/agee

Review

Key ecosystem services and ecological intensication of agriculture in

the tropical high-Andean Puna as affected by land-use and climate
changes
Jose L. Rolandoa,b,* , Cecilia Turina , David A. Ramreza,c, Victor Maresa , Jorge Monerrisd ,
Roberto Quiroza,*
a
International Potato Center (CIP), Apartado 1558, Lima, 12, Peru
b
University of Florida, North Florida Research and Education Center, Marianna, FL, 32446, USA
c
Gansu Provincial Key Laboratory of Aridland Crop Science, Crop Genetic and Germplasm Enhancement, Agronomy College, Gansu Agricultural University,
Lanzhou, 730070, China
d
Dpartement des sciences biologiques, Universit du Qubec Montral, Montral, Qubec, H2X 3Y5, Canada

A R T I C L E I N F O A B S T R A C T

Article history:
Received 7 May 2016 High-altitude ecosystems shelter important reserves of biodiversity, water provision and soil organic
Received in revised form 30 November 2016 carbon (SOC) stocks. Climate change, agricultural encroachment, overgrazing, and mining activities are
Accepted 5 December 2016 endangering ecosystems sustainability, particularly in the high-Andean Puna. Increasing food demands
Available online xxx in a region with limited agricultural land calls for agricultural intensication. Ecological intensication of
agriculture is a framework for increasing agricultural productivity by fostering supporting and regulating
Keywords: ecosystem services (ES) while reducing negative environmental impacts. In this review we examine how
Mountain ecosystems agriculture use and disturb the provision of key ES in this ecoregion food, wool and ber provision, soil
Nutrient cycling
fertility, nutrient cycling, soil carbon sequestration, water provision and regulation, genetic resources,
Soil fertility
pest and disease control, pollination regulation and microclimate regulation. We also propose a set of
Water provision
Water regulation technologies, practices and policies to preserve (or restore) the provision of these key ES: long fallowing,
Biodiversity soil amendments, conservation tillage, rotational grazing, grassland ecological restoration, conservation
Carbon sequestration of agrobiodiversity, modern irrigation and water harvesting, plant breeding, climate change mitigation
schemes and payment for ecosystem services, and adapted traditional technologies.
2016 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ................. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 222

2. Puna description . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ................. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223
3. Key ecosystem services related to agriculture in the Puna ................ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
3.1. Food, wool and ber provision . . . . . . . . . . . . . . . ................. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
3.2. Soil fertility and nutrient cycling . . . . . . . . . . . . . . ................. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
3.3. Soil carbon sequestration . . . . . . . . . . . . . . . . . . . . ................. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
3.4. Water provision and regulation . . . . . . . . . . . . . . . ................. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 224
3.5. Genetic resources, pollination regulation, and pest and disease control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
3.6. Microclimate regulation . . . . . . . . . . . . . . . . . . . . . ................. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
4. Main drivers of change . . . . . . . . . . . . . . . . . . . . . . . . . . . ................. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226
4.1. Climate change . . . . . . . . . . . . . . . . . . . . . . . . . . . . ................. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226
4.2. Agricultural intensication and encroachment . . . ................. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227

* Corresponding authors at: International Potato Center (CIP), Apartado 1558,

Lima, 12, Peru.
E-mail addresses: jlrolando@u.edu (J.L. Rolando), r.quiroz@cgiar.org
(R. Quiroz).

http://dx.doi.org/10.1016/j.agee.2016.12.010
0167-8809/ 2016 Elsevier B.V. All rights reserved.
222 J.L. Rolando et al. / Agriculture, Ecosystems and Environment 236 (2017) 221233

4.3. Intensive grazing practices . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227

4.4. Mining activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228
5. How to promote ecological intensication through conservation and restoration of key ecosystem services of the Puna agro-ecosystems? 228
5.1. Long fallow and soil amendments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228
5.2. Conservation tillage and rotational grazing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228
5.3. Grassland ecological restoration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 229
5.4. Conservation of agrobiodiversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230
5.5. Modern irrigation and water harvesting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230
5.6. Plant breeding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230
5.7. Climate change mitigation schemes and payment for ecosystem services . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230
5.8. Traditional technologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230
6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231

1. Introduction of biodiversity, land degradation, release of greenhouse gases, and

One fth of Earth surface is occupied by mountain ecosystems
(excluding large plateaus). They support a quarter of the terrestrial
biodiversity and supply water to approximately half of the global
population (Bierman-Lytle, 2015). An archetypal case of a high
altitude region is the tropical high-Andean Puna (hereafter Puna).
High biological diversity, agrobiodiversity, and endemism (Buy-
taert et al., 2011; de Haan, 2009), large reservoir of soil organic
carbon (SOC) stocks (Gibbon et al., 2010; Segnini et al., 2010), and
water provision to mining, agricultural, energetic, and urban
demands (Buytaert et al., 2011; Buytaert and de Bivre, 2012; Vuille
et al., 2008b) confer a special ecological relevance to this region.
Nevertheless, high-altitude ecosystems are among the most fragile
of the Earth as they show low recovery rates after disturbance
(Bierman-Lytle, 2015). In the Puna, climate change (Section 4.1),
agricultural intensication and crop encroachment (Section 4.2),
overgrazing (Section 4.3), and mining activities (Section 4.4)
jeopardize the functionality of their ecosystems, and the ecosys-
tem services (ES) they provide. However, the ecological relevance
of the Puna is belittled, as evidenced by the limited attention given
when formulating environmental policies, contrasted with the
prominence tropical forests receive.
The Millennium Ecosystem Assessment (2005) categorizes
ES or the benets people get from ecosystems in provisioning,
regulating, supporting and cultural services. Provisioning services
are the products directly obtained from ecosystems (e.g., food,
ber, timber), regulating services are the benets obtained from
the regulation of ecosystem processes (e.g., climate regulation,
water regulation, pest and disease regulation), supporting services
are indirect services, as they are necessary for the production of
provisioning, regulating or cultural services (e.g., soil formation,
nutrient cycling, photosynthesis), and cultural services are
nonmaterial benets people obtain from ecosystems (e.g.,
aesthetic values, recreation and ecotourism, cultural diversity).
For agriculture to be sustainable, regulating and supporting
services on which agriculture is based must be maintained over
time (Bommarco et al., 2013). Depending on management
practices, agriculture might disturb ecosystem processes and thus
the provision of ES in which it relies on (Power, 2010). For example,
crop encroachment into Puna grasslands with high SOC stocks
disturbs soil aggregates stability and promotes the release of
greenhouse gases affecting carbon sequestration and climate
regulation services (Section 4.2). When studying the impact of
agriculture on ES, tradeoffs between different ES affected by
agricultural practices should be assessed (e.g., manure fertilization
enhances soil fertility and nutrient cycling, but releases green-
house gases and might pollute waterbodies) (Power, 2010). In a
fragile ecoregion already characterized by climate extremes,
inadequate agricultural intensication could exacerbate the loss
competition for water (Lal, 2013). Under these circumstances,
ecological intensication of agriculture is a recent approach aimed
at increasing crop yields by preserving the ecosystems processes
that provide supporting and regulating ES for agriculture, and
reducing agricultural negative impacts over the agroecosystem
(Bommarco et al., 2013). Key ES related to Puna agriculture are:
food, wool and ber provision, soil fertility, nutrient cycling, soil
carbon sequestration, water provision and regulation, genetic
resources, pest and disease control, pollination regulation and
microclimate regulation. Soil fertility and nutrient cycle are
affected by the high soil erosivity conditioned by steep topography,
climate and inherent low quality of Andean soils (Romero, 2005).
Soil carbon sequestration is relevant for maintaining the high SOC
stocks in Puna ecosystems (Gibbon et al., 2010). Water provision
and regulation is relevant due to the presence of basin-headwaters
in which agriculture, mines, hydroelectric power plants and urban
centers rely on (Section 3.4). Genetic resources are important as
the Puna is a region with high levels of biological diversity,
agrobiodiversity, and endemism (Section 3.5), while pollination is
important to maintain this diversity. Pest and disease control are
crucial in order to reduce agricultural losses in a region with
already low potential yields (Postigo, 2014). Finally, microclimate
regulation is important in a region where extreme weather events
occur regularly, and which may be boosted by climate change
(Thibeault et al., 2010).
Several review papers discuss the current knowledge of climate
change effects on ecosystem processes and services in the tropical
Andes (Anderson et al., 2009) as well as the effects of climate
change on Andean hydrology (Rabatel et al., 2013; Vuille et al.,
2008b). Also, Fonte et al. (2012) published an extensive review on
soil management practices for the agroecological intensication of
soil fertility in the high Andes. However, a state of the art review of
the ES provided by Puna ecosystems focused on its relation to
agriculture is still missing. Moreover, there is no study that
summarizes information on environmental and agricultural
practices, technologies and policies oriented to the preservation
(or restoration) of ES affected by agriculture in the Puna. The
objective of this review paper is to ll this information gap,
important for environmental and agricultural policy-making in
this ecoregion. The relevance of this study is enhanced by the
fragility of these ecosystems, where current processes jeopardizing
its sustainability co-exist with the need for agricultural intensi-
cation. The review describes the ecology of the Puna (Section 2)
and describes the relevance of key ES for agriculture (Section 3). It
also analyzes how climate change, agricultural intensication, crop
encroachment, overgrazing and mining activities are endangering
the provision of these ES (Section 4), and ends up proposing a set of
agricultural technologies, practices, and policies that could be
instrumental for achieving the ecological intensication of Puna
 J.L. Rolando et al. / Agriculture, Ecosystems and Environment 236 (2017) 221233 223

agriculture (Section 5). The selection of reference papers was based
on authors experience and Google Scholar retrieval using different
combinations of the following keywords: Puna; grasslands;
wetlands; agriculture; Wet Puna; Dry Puna; ecosystem
services; ecological intensication; as well as all of the ES
analyzed and all of the technologies; practices and policies
proposed.
2. Puna description
In this review, tropical high-Andean Puna is dened as the
section of the Central Andes Puna (6
S23
S) above 3500 m asl
(Fig. 1). The region includes ecosystems that are associated with
high plateaus and inter-montane basins (Wilcox et al., 1987). Puna
is subdivided in two different phytoregions, the Moist or Wet Puna
and the Dry or Xerophytic Puna (Josse et al., 2009). This subdivision
is based on a gradient of decreasing precipitation and duration of
the rainy season from northeast to southwest of the Andes.
Grassland and open shrubland ecosystems dominate the Wet and
Dry Puna, respectively (Troll, 1959, cited by Simpson, 1983). The
current condition of landscapes and agro-ecosystems in the Puna,
however, is a resultant of human interventions at work during
several millennia (Young, 2009). Human occupation above 3500 m
asl occurred at least 15000 years Before Present (B.P.) (Baied and
Wheeler, 1993) and in the Peruvian Andes, there is evidence of
agriculture since at least 9000 years B.P. (Dillehay et al., 2007).
The Puna is a region with high spatial and temporal climatic
variability (Garreaud, 2000; Mohr et al., 2014). Precipitation in this
region is seasonal with more than 50% of the rainfall occurring
during the austral summer (December through March) (Vuille and
Keimig, 2004). This happens when the atmospheric circulation
drives air uplift from the lowlands to the east of the Andes
(Garreaud, 1999). In the Wet Puna, annual precipitation ranges
between 500 and 1000 mm, and in the Dry Puna between 300 and
500 mm, decreasing from northeast to southwest in both cases
(Baied and Wheeler, 1993). Interannual precipitation variability is
high and partially explained by reduced precipitation during El
Nio Southern Oscillation (ENSO) warm phase of the cycle and the
opposite situation during the cold phase (Garreaud et al., 2009).
Rainfall pattern in the Puna usually involve a cluster of 410 rainy
days, followed by a dry episode (Garreaud, 1999, 2000), being
rainfall events generally weak (0.54.0 mm h1) and of short-

Fig. 1. Geographical location of the two Puna phytoregions in the Tropical Central Andes above 3500 m asl. Based on Josse et al. (2009). All locations mentioned in the text are
indicated in the map. The glacier area of the Cordillera Blanca was obtained from the GLIMS and NSIDC (2005, updated 2016)GLIMS and NSIDC, 2005GLIMS and NSIDC (2005,
updated 2016) database.
224 J.L. Rolando et al. / Agriculture, Ecosystems and Environment 236 (2017) 221233
duration (Mohr et al., 2014). Air temperature has an almost
inexistent gradient along the equator-to-pole mountain range, in
contrast with what is found in the sub-tropical Andes (Garreaud
et al., 2009). Minimum, mean and maximum annual temperature
range between 5 and 5
C, 8 and 11
C, and 15 and 20
C,
respectively (Lavado Casimiro et al., 2013).
3. Key ecosystem services related to agriculture in the Puna
In this section we review how agricultural activities in the Puna
ecoregion impinge on provisioning, regulating, and supporting ES
(Table 1).
3.1. Food, wool and ber provision
Most of the Puna is covered by natural grasslands dominated by
Poa, Stipa, Calamagrostis, and Festucas species, comprised of low
productivity vegetation associations (Wilcox et al., 1986). The most
common land use is extensive livestock rearing in both communal
and family allocated land, complemented by limited subsistence
cropping practiced in smallholdings of less than 2.5 ha where
potato (Solanum spp.), quinoa (Chenopodium quinoa) and other
Andean crops are cultivated (Dixon et al., 2001). Major livestock in
the Puna include cattle (Bos taurus), sheep (Ovis aries) and camelid
species and free-ranging vicugnas (Vicugna vicugna). In spite of the
marginal productivity of the land, low carrying capacity of natural
rangelands and lack of productivity-enhancing technologies, the
Puna contributes with a substantial amount of meat, wool, alpaca
(Vicugna pacos) ber and dairy products to local, regional and
international markets. It is important to note that cropping in some
Puna areas is evolving to market oriented products, particularly
quinoa and maca (Lepidium meyenii) which are having a high
demand in national and international markets with some trade-
offs with other ES, a process that requires attention through
research and policies.
3.2. Soil fertility and nutrient cycling
Puna soils are generally poor and limited by P concentration,
except in the Altiplano region where they tend to be N- and
C- limited (Fonte et al., 2012; Hofstede, 1995; Pestalozzi, 2000;
Vanek and Drinkwater, 2013). Agriculture in the region is limited
by slow nutrient cycling, where even long fallowed soils (9 years)
need be complemented with additional N-P-K fertilization to
produce satisfactory yields in subsequent cropping seasons
(Pestalozzi, 2000). Even in the North Andean highlands, where
higher temperatures and precipitation lead to faster nutrient
turnover rates, three years of consecutive potato cropping causes a
reduction of more than 50% of N mineralization rates (Sarmiento
Table 1
Ecosystem services provided by Puna ecosystems and its classication according
the Millenium Ecosystem Assessment categories (2003).
Ecosystem service classication
Ecosystem service Provisioning Regulating Supporting
Food, wool and ber provision x 2014). Since the sources of water input to Andean wetlands are
Carbon sequestration x diverse (i.e. glacial melt water, rivers, lakes, ground water and
Water provision x precipitation) and vary according to different conditions, the
Water regulation x
Soil fertility x
Nutrient cycling x scientic information for reliable water management (Maldonado
Pest and disease control x x
Genetic resources x through the transformation and degradation of pollutants
Pollination regulation x (Kandus et al., 2011); many of them generated by mining activity
Microclimate regulation x x
and Bottner, 2002). In Puna croplands, manure and plant residues
are the larger nutrient inputs to soils, while the larger outputs are
crop harvest and soil erosion (Vanek and Drinkwater, 2013).
Romero (2005) found erosion values between 0 and 122 Mg ha1
yr1 in the Peruvian Wet Puna, while Vanek and Drinkwater (2013)
found values between 3 and 34 Mg ha1 yr1 in the Bolivian Dry
Puna, both correlating with slope and land use. It is crucial to
understand the nutrient cycling between cropland and grassland
ecosystems, since livestock grazing native grasslands are the ones
providing manure for crop production (Fig. 2). Manure production
is limited by net primary productivity of native grasslands, which
depends on environmental (e.g., rainfall, temperature, solar
radiation, soil fertility), biological (e.g., plant composition,
photosynthetic strategy, C partitioning, herbivory), and social
(e.g., grazing management, stocking rates, land availability)
drivers.
3.3. Soil carbon sequestration
It is estimated that in the last 150300 years between 25 and
50 Pg of C has been globally released to the atmosphere due to soil
organic matter losses in agricultural lands, mainly due to tillage
(Houghton, 2012, Powlson et al., 2012; West and Post, 2002). In the
Wet Puna, large SOC stocks result from the exceedance of native
grasslands primary productivity over SOC decomposition rate,
which is limited due to cold temperatures (Zimmermann et al.,
2010). Gibbon et al. (2010) reported SOC stocks in the Peruvian Wet
Puna grasslands of 11.9 kg C m2 in the whole soil prole (mean
depth: 32.5 cm), which were as high as the values found in the
Amazonian rainforest soils and about twice their aboveground SOC
stocks. Muoz Garca and Faz Cano (2012) reported a carbon stock
of 23.8 kg C m2 in the soil surface (5 cm depth) of a managed
Bolivian Wet Puna grassland grazed by vicuas above 4500 m asl.
Furthermore, it has been shown that SOC stocks in high Wet Puna
wetlands largely exceed native grasslands C stocks, reaching values
of 30.6 kg C m2 in the 030 cm soil prole of seasonally ooded
wetlands (Segnini et al., 2010).
3.4. Water provision and regulation
Puna glaciers and wetlands supply water provision and
regulation services to the Central Andes, guaranteeing freshwater
availability over this region. The Puna has a glacier area of
2560 km2 (Dyurgerov and Meier, 2005). Just the Cordillera Blanca
(8
300 10
100 S) (Fig. 1), a mountain range in the Peruvian Wet
Puna, contains more than 25% of tropical glaciers worldwide
(Mark et al., 2010). Mountain glaciers are an important source of
water provision and regulation in the Andean region, buffering
the temporal precipitation variability that guarantees water for
domestic, agricultural and industrial uses during the dry season
(Rabatel et al., 2013; Vuille et al., 2008b). Moreover, the water-
related services of the Puna are not only provided to the high-
Andes, but also to the highly populated cities of the Pacic Desert
(Buytaert and de Bivre, 2012). Wetlands also provide a water
buffer function and are important for fresh water provision
during the dry season (Buytaert et al., 2011; Maldonado Fonkn,
hydrology of each system needs to be studied in order to have
Fonkn, 2014). Andean wetlands also regulate water quality
(see Section 4.4).
 J.L. Rolando et al. / Agriculture, Ecosystems and Environment 236 (2017) 221233 225

Fig. 2. Simplied nutrient dynamic in a usual mixed crop-livestock farming system in the Puna. The magnitude of importance of each component is context-dependent on
agro-ecological management practices. Traditionally, crop eld soil nutrition depended primarily on the export of nutrients from grasslands, but with agricultural
intensication, the relevance on chemical fertilizers is increasing. Fallow length modulated two key nutrient outputs at the crop eld level: harvestable organs and soil
erosion. At reduced fallow length, higher losses occur from both of them. During the fallow period, plant residues are decomposed by microbial and fungal activity recycling
nutrients into the soil. In the native grassland/improved pasture land use, soil erosion is modulated by pastoral management (e.g., when overgrazing occurs, soil erosion
increases).
*
Oher losses are fertilizer-related; as leaching, denitrication and ammonia volatilization, which largely depends on fertilizer management and can be avoided with the
application of good agricultural practices.

3.5. Genetic resources, pollination regulation, and pest and disease
control
Tropical mountains are hotspots of biological and agricultural
diversity due to their high spatial and environmental heterogene-
ity. Regarding biological diversity, the Andean region accounts for a
percentage of species endemism of 60% (Buytaert et al., 2011). The
tropical Andes accounts for 6.7% of the total world plant
endemism, being the region with the highest percentage
worldwide (Myers et al., 2000). de Haan et al. (2010) found that
the Andean highland belt between 3800 and 4150 m asl, where
weather extremes are more frequent, presents the highest
diversity of potato and other Andean tubers. For instance, in the
Department of Huancavelica in Central Peru, in-situ conservation
of potato biodiversity, carried out by planting large cultivar
mixtures (chaqru), accounts for at least 406 unique cultivars
(de Haan, 2009). In addition to in-situ conservation of genetic
resources, the maintenance of seed diversity and the spatial
distribution of agro-biodiversity are also sociocultural processes
that have contributed to the high agrobiodiversity of the region
(Pajares Garay and Llosa Larrabure, 2011).
High altitude ecosystems tend to have limited pollination
mediated by biological agents due to their harsh environments.
Therefore, the efcient wind-pollination of Puna grasses drive
their dominance in even isolated alpine areas (Anthelme et al.,
2014). Punas most abundant crops, either do not need pollination
to produce harvestable organs (e.g. potato, oca (Oxalis tuberosa),
maca)- or tend to self-pollinate (e.g. quinoa and other Andean
cereals). Nevertheless, cross pollination in mixtures of different
varieties and even species, as practiced by local peasants, has been
essential to obtain the high Puna agrobiodiversity (Rabinowitz
et al., 1990). The best-documented case is the one regarding potato
agrobiodiversity, where bee species from the Apidae, Colletidae,
and Megachilidae families tended to cross-pollinate different
varieties, subspecies and even species, contributing to the genetic
differentiation of about 3000 different genotypes (Rabinowitz
et al., 1990; Scurrah et al., 2008; Velsquez-Milla et al., 2011).
Pests are considered a major threat for agroecological systems.
In the Puna, global warming inuence changes in the geographical
distribution of potato pests such as the Andean weevil complex
and tuber moths or quinoa moth (Eurysacca melanocampta). The
potato weevil complex consist of 14 species of beetles (Family:
Curculionidae) specialized in feeding from tubers. They are
originally distributed between 2800 and 4700 m asl (Kaya et al.,
2009). Quinoa moth is considered the most devastating pest for
quinoa crops in the Puna of Peru and Bolivia (Rasmussen et al.,
2003). Despite its importance for potato and quinoa in the Puna, to
the best of our knowledge, there are no studies either analyzing or
forecasting changes in the geographical distribution of these
insects. Conversely, it is known that the potato tuber moths
Phthorimaea operculella, Symmetrischema tangolias, and Tecia
solanivora have been shifting their distribution range to the south
during the last 30 years in the tropical Andes (Crespo-Prez et al.,
2015). These moths reduce potato production in the Puna, where
human populations are already under severe environmental,
health and socioeconomic stress (Dangles et al., 2008).
3.6. Microclimate regulation
Agriculture in Puna agroecosystems is usually limited by cold
temperatures and by water availability (Dixon et al., 2001). In this
ecoregion, waterbodies regulate microclimate in both temperature
and rainfall. In the Altiplano, Lake Titicaca has been shown to warm
the local environment by about 4 to 5
C, while increasing
precipitation levels (Bush et al., 2010). The regulation of water
and temperature by waterbodies has been vital for developing
agriculture in the region. Indigenous population has developed
technologies to manage water surpluses to mimic the natural
226 J.L. Rolando et al. / Agriculture, Ecosystems and Environment 236 (2017) 221233

microclimates regulating temperature and soil humidity under
extreme conditions (see Section 5.8). Good-condition high-Andean
grasslands also regulate microclimate by reducing daily tempera-
ture uctuations, critical in a region with high frequency of frost
events (Hofstede et al., 1995).
4. Main drivers of change
4.1. Climate change
It is expected that climate change in the Puna will decrease
water provision due to decreased rainfall and glacier melting
(Magrin et al., 2014) (Table 2). Under both A2 and A1B scenarios, a
precipitation reduction of between 10 and 30% is expected
(Marengo et al., 2011; Minvielle and Garreaud, 2011). Thibeault
et al. (2010) found that the reduction of annual precipitation will
be driven by the shortening of the rainy season; and that
precipitation will be less frequent but more intense, increasing
the risk of ood events and affecting the water regulation service.
Moreover, tropical glaciers are increasing their melting rates due to
higher temperatures and increased absorption of solar radiation
(Perez et al., 2010; Vuille et al., 2003). In the tropical Andean
glaciers, negative mass balances have been more pronounced and
began earlier (since 1976) than other glaciers worldwide (Rabatel
et al., 2013). Interannual variation of glaciers mass loss in Puna
glaciers is higher (lower) during positive (negative) ENSO years,
driven by the hot and dry (cold and humid) wet season (Vuille
et al., 2008a). The Cordillera Blanca, the most important tropical
glacier in the Andes, has already lost 22.4% of its glaciated area
from 1970 to 2003 (Racoviteanu et al., 2008). It has been predicted
that by 2050 these glaciers would further decrease their extension
by 38 to 60%, when compared to 1990s area (Juen et al., 2007). By
the end of the twenty-rst century, the Cordillera Blanca melting
water discharge could cease, causing a severe water scarcity in the
western side of the Tropical Central Andes during the dry season
(Chevallier et al., 2011). In the River Santa basin in the Peruvian
Andes, for example, the annual discharge will be lower than
present by 2 to 30%, differing across watersheds (Baraer et al.,
2012). This scenario is not unique to the Cordillera Blanca glaciers,
but similar trends have been observed all along the Puna (for an
extensive review on glacier current states and projections see
Rabatel et al. (2013) and Vuille et al. (2008b). Special interest
should be focused on smaller extensions glaciers, located below
5400 m asl, since these are the most vulnerable due to their higher
magnitudes of glacier mass loss (Rabatel et al., 2013). Decreasing
glacier water discharges will also end up drying Puna wetlands.
The decrease of water provision and disturbance of water
regulation in the Puna has to be taken seriously as most of the
agriculture in this region is rainfed. In the Peruvian Andes, for
example, about 70% of agricultural land is rainfed (INEI, 2013).
Concerning temperature, Vuille et al. (2015) have found an
increasing temperature trend of about 0.110.20
C decade1 in the
tropical Andes between 3500 and 4500 m asl, driven by an increase
in greenhouse gas concentration. Projected changes in the Andean
Cordillera (above 5500 m asl) under an A2 scenario showed an
estimated increase of between 4.5 and 5.5
C when comparing data
from the 1990s to the 2090s decade (Bradley et al., 2006).
However, in the Bolivian Altiplano, Thibeault et al. (2010) found an
increase in frost events frequency related with the increase of clear
nights during the dry season. The temperature increase in the Puna
is pushing up the altitudinal habitat range of plant communities,
crops and disease vectors, driving farmers to plant crops at higher
altitudes (Postigo, 2014). For instance, Crespo-Prez et al. (2015)
modeling results suggest that Symmetrischema tangolias, a cold
tolerant pest (Dangles et al., 2008), may shift its distribution range
at altitudes between 3000 and 4000 m asl and latitudes between
10 and 25
S, but it may decrease its survival probability at lower
altitudes. In response to warming and incremental pest pressures
at higher altitudes between 3900 and 4350 m asl in the Wet Puna
of Huancavelica (de Haan, 2009), the cultivation of potato, barley
(Hordeum vulgare), tarwi (Lupinus mutabilis), maca and oats (Avena
sativa) is encroaching into native grasslands. This encroachment
into native grasslands upregulates soil respiration and emission of
greenhouse gases due to aggregates disturbance (Section 4.2).
Moreover, dried wetlands expose their large SOC reservoir to the
aerobic atmosphere promoting microbial respiration and green-
house gas emissions.
It is known that climate and management conditions affect
alpaca susceptibility to diseases (Rojas et al., 2016). For instance, a
diarrhea outbreak affected alpaca herds in southern Peru in 2010.
Diarrhea is the most lethal disease in alpacas being responsible for
44% of the mortalities (Rojas et al., 2016). Although climate has

Table 2
Synthesis of climate change projections on precipitation, temperature and glacier area and melt water in the Puna across different scenarios from the IPCC Special Report on
Emissions Scenarios (IPCC-SRES).

Simulated change Location Year Model and IPCC-SRES Reference

Precipitation -10% to 30% Altiplano 2100 11 CMIP3 models, A2 Minvielle and Garreaud
(2011)
-20% to 30% 5
S to 25
S Andes 2100 Eta forced with Marengo et al. (2011)
HadCM3, A1B

Temperature Increase of between 4.5 Tropical Andean Cordillera above From 19900 s to 20900 s 8 GCM, A2 Bradley et al. (2006)
and 5.5
C 5500 m asl
Increase between  4 and Tropical Andes between 3500 and End of the 21 st century PRECIS, A2 Urrutia and Vuille (2009)
5
C depending on the 5000 m asl (20712100)
altitude and location on
the Andean western or
eastern slope

Glacier area 22.4% Cordillera Blanca From 1970 to 2003 Empirical value Racoviteanu et al. (2008)
49% Cordillera Blanca From 1990 to 2080 Not specied, B1 Juen et al. (2007)
75% Cordillera Blanca From 1990 to 2080 Not specied, A2 Juen et al. (2007)

Glacial melt Increased until 2020 to Cordillera Blanca 2100 Based on temperature Chevallier et al. (2011)
water 2050 followed by a only, B2
continuous decrease
44% Cordillera Blanca 1990 to 2080 Not specied, B1 Juen et al. (2007)
69% Cordillera Blanca 1990 to 2080 Not specied, A2 Juen et al. (2007)
 J.L. Rolando et al. / Agriculture, Ecosystems and Environment 236 (2017) 221233
been accepted as an important driver of the proliferation of these
enteric diseases (Rojas et al., 2016), studies analyzing and
forecasting its frequency and severity are still missing. The
development of models such as those proposed by Crespo-Prez
et al. (2015), considering pests and diseases proliferating in the
ecoregion is thus required.
Finally, a thorough assessment of climate and crop yield
modeling is still pending. Notwithstanding, a few exploratory
studies are available. Based on an A1 B emission scenario run up to
the 2030 s in an area that comprises both the Peruvian Wet and Dry
Puna, Sanabria et al. (2014) estimated that the growing season of
rainfed potato, barley and broad bean (Vicia faba) cultivated at
35003850 m asl will be shortened due to increased temperatures.
Although, no signicant yield reduction was predicted in spite of
reduced precipitation (Sanabria et al., 2014). However, Lobell et al.
(2008), based on the B1, A1 B and A2 emission scenarios for the
Andean region at large estimated a decrease in wheat (Triticum
spp.), barley, potato, and maize (Zea mays) yields ranging from 5 to
14% to be expected by 2030. Moreover, Fleisher et al. (2016), tested
different climate change scenarios for the region, using an
ensemble of ten potato models. Key results can be summarized
as follows: 1) warming is expected to decrease tuber yield, on
average, 4% per
C incremented; 2) reduction or increment in
rainfall (/+ 30% of actual) produced changes in the order of minus
4.9 or plus 2.5%, respectively; but in the best of the cases yields
were way below their potential under irrigated conditions; and, 3)
the fertilization effect due to higher CO2 concentration was
estimated as 10% per 100 ppm incremented.
4.2. Agricultural intensication and encroachment
Changes on the way agriculture has been practiced is causing
several environmental impacts in the region, mainly driven by
agricultural intensication in certain areas and crops encroach-
ment into native grasslands. For instance, in the southern Altiplano
of Bolivia, there has been an important expansion of quinoa
cropping area and it has become the most important producing
region in the Andes. Quinoa has transitioned from a subsistence
grain crop to a commercial product cultivated over extended areas
in the at plains of native herb and shrub vegetation. Since the
1970s, quinoa crops have rapidly encroached into native grasslands
and it was estimated that the land surface dedicated to quinoa crop
in Bolivia has increased more than 230% between 1980 and 1990
(FAO-Stat) (Rambal et al., 2015).
In the Wet Puna, in eastern Cusco, Zimmerer (2003) described
an intensication process in rainfed barley between 3000 and
3900 m asl where fallow pastures and native grasslands are being
encroached, and a de-intensication process in the rainfed
plateaus and slopes above 3800 m asl, where the hotspots of local
Andean tubers agrobiodiversity are located. Also in the Peruvian
Wet Puna, maca a reputedly energetic root- has jumped from
being a crop for local consumption to be an export oriented
Table 3
Synthesis of soil carbon stocks means on different ecosystems or land uses in the high-Andean Puna.
Mean soil carbon Depth of soil prole (cm) Ecosystem/Land use
stock (kg C m2)
30.6 0 to 30 Seasonally ooded wetlands
23.0 0 to 30 Permanent ooded wetlands
11.9 To bedrock1
5.8 0 to 15
3.2 0 to 5
3.7 0 to 15
2.9 0 to 5
4.7 0 to 30
1 0 to 5
1 Mean soil depth = 32.5 cm.
227
product mainly to Asian markets. The extension of maca cropping
area in the Junin region has tripled to 6500 ha in only one year
(20142015) at the expense of native grasslands (Gobierno
Regional de Junin, 2015), and a comparative analysis using satellite
imageries of 1987 and 2013 shows that about 30% of native
grasslands were converted into maca cropland in the same study
area (Turin et al., unpublished). As a result, fallow areas have
increased greatly given the nature of maca cultivation (two/three
annual growing seasons per eight years of fallow). Crops
encroaching into native grasslands might reduce its SOC reservoir
due to tillage operation, disturb the hydrologic cycle and reduce
the source of feed for livestock. The impact of tillage in increasing
the emission of greenhouse gases is evidenced by potato cropland
soils in the Peruvian Altiplano presenting only 1 kg C m2 in the top
5 cm and 4.7 kg C m2 down the 030 cm prole (Segnini et al.,
2011). This SOC stock is one third of the SOC stocks found in native
grasslands soils in the same soil prole (Table 3).
Agricultural intensication has also increased water demand
for irrigation, causing landscape drying and desertication (Brandt
and Townsend, 2006). Soil degradation via fertility loss, erosion
and oxidation of soil organic matter is a consequence of
unsustainable agricultural intensication (Gomiero et al., 2011).
This is especially relevant in mountain ecosystems since intensive
agriculture in steep topographies is conducive to soil erosion,
affecting soil quality through nutrient and organic matter loss
(Fonte et al., 2012; Thorne and Tanner, 2002; Vanek and Drink-
water, 2013). Moreover, agricultural intensication has already
modied the soil nutrient cycle in the Puna as some farms are
reducing or even eliminating fallow periods and the nutrient
deciency is compensated with an increased input of chemical
fertilizers and sheep manure (McDowell and Hess, 2012; Perez
et al., 2010; Rocha, 2011).
4.3. Intensive grazing practices
Reduced fallow duration in croplands due to agricultural
intensication is limiting the reclamation of the land into good-
condition grasslands. This process reduces grazing area and leads
to overgrazing of native grasslands (de Haan and Jurez, 2010).
Overgrazing and excessive use of re in the Puna promotes soil
erosion and loss of plant cover and diversity, endangering the
economic value of native grasslands (Catorci et al., 2014). High soil
temperatures which results from less plant cover and increased
soil bulk densities due to overgrazing- accelerates SOC decompo-
sition rates, increasing greenhouse gas emissions (Hofstede, 1995;
Muoz Garca and Faz Cano, 2012). Concerning biological diversity,
the response to grazing ts the intermediate disturbance
hypothesis since moderate disturbance intensities increase plant
species richness and diversity, while high and low levels of
disturbance decrease biological diversity (Catorci et al., 2014). High
levels of disturbance events tend to increase the chances of plant
invasion susceptibility (Gross et al., 2005; Hobbs and Huenneke,
Location Reference
Peruvian Altiplano Segnini et al. (2010)
Peruvian Altiplano
Protected grassland Peruvian Wet Puna Gibbon et al. (2010)
Grazing grassland Bolivian Altiplano Muoz et al. (2013)
Grazing grassland Bolivian Altiplano
Grazing grassland Bolivian Altiplano Muoz Garcia and Faz Cano (2012)
Grazing grassland Bolivian Altiplano
Potato cropland Peruvian Altiplano Segnini et al. (2011)
Potato cropland Peruvian Altiplano
228 J.L. Rolando et al. / Agriculture, Ecosystems and Environment 236 (2017) 221233
1992) leading to a decrease in plant community b-diversity, critical
for a region with a high degree of endemism. Furthermore,
disturbance due to overgrazing decreases overall species richness,
driven by the selection of tolerant and less palatable- species
(Patty et al., 2010).
4.4. Mining activity
The Puna region contains important reserves of copper, gold,
tin, lead, silver, and zinc, which makes Peru an important mineral
producer worldwide (Reichl et al., 2015). Mining activity causes
important social and environmental impacts, particularly on water
resources, due to its high water demand. Mining not only affects
water availability (e.g. wetlands reduction as a consequence of
groundwater extraction) (Devenish and Gianella, 2012; Hinojosa,
2013), but also water quality. The inadequate disposal of mining
waste pollutes water bodies (Cook and Abbott, 2008) and streams
(Salvarredy-Aranguren et al., 2008) with heavy metals, trace
elements and toxic compounds that affect people, livestock, wild
animals and crops (Bundschuh et al., 2012).
5. How to promote ecological intensication through
conservation and restoration of key ecosystem services of the
Puna agro-ecosystems?
In this section we analyze technologies, practices and policies
and relate them to the key ES reviewed in this paper (see summary
in Table 4).
5.1. Long fallow and soil amendments
Long fallow periods and incorporation of soil amendments are
two common practices in Puna farming systems. They contribute
to enhance and restore soil fertility and nutrient cycling. Long
fallow periods enhance C and N microbial activity in soils, which,
with the adequate soil moisture, is a key factor for nutrient
mineralization (Lu et al., 2012; Sarmiento and Bottner, 2002). In the
Bolivian Dry Puna, fallow have positive impacts on soil chemical
properties restoring C and N contents, and being more effective in
longer fallow periods and after slighter cropping perturbations
(Aguilera et al., 2013; Gomez-Montano et al., 2013). Moreover, long
fallows not only enhance soil fertility and nutrient cycling, but also
reduce pest and diseases pressures (de Haan, 2009).
In the Dry Puna of the Bolivian Altiplano, incorporation of
24 ton ha1 of sheep manure as a soil amendment met the N crop
demand in a two year potato-potato as well as in a potato-barley
Table 4
Summary list of suggested technologies, practices or policies and the ecosystem services it promote.
Technology, practice or policy
Agrobiodiversity conservation
Bench terraces
Climate change mitigation schemes
Conservation tillage
Crop rotation
Judicious chemical fertilization
Grassland ecological restoration
Long fallow
Manure and plant-residues application
Modern irrigation (drip irrigation, sprinkler irrigation)
Payment for ecosystem services
Plant breeding
Qocha
Rotational grazing
Waru-Waru
Water harvesting
Wetland restoration
rotation after a long fallow period (Coteaux et al., 2008). In
another study in the same region, Aguilera et al. (2012) found that
10 ton ha1 of either cow or sheep manure increased total N and C,
but only signicantly increased Bray1 P and inorganic N when
mixed with inorganic fertilizers. It was concluded that to achieve
potential yields in this region while maintaining long-term soil
health the judicious application of chemical fertilizers mixed with
organic soil amendments seems to be the best practice to adopt
(Aguilera et al., 2012). In order to overcome the inherent limitation
of P in the Puna environment, Fonte et al. (2012) suggest the
application of rock phosphate, a low quality and cheap source of P
easily found in the Andes. Moreover, adding manure and plant
residues amendments could contribute to increase soil fertility,
protect soil against raindrop impacts during intense rainfalls, and
increase soils water holding capacity and inltration rates.
5.2. Conservation tillage and rotational grazing
Conservation tillage increases soil stability, improving several
soil physical, chemical and biological attributes. It reduces SOC
degradation due to less mechanical disturbance of soil aggregates
(Barbera et al., 2012). Likewise, increased soil stability reduces
soil erosion and run-off rates, conjointly with a reduction in the
formation of soil crust thus increasing water inltration rates
(Thierfelder et al., 2005). Quintero and Comerford (2013) found
that seven years of conservation tillage in a North Andean
location at 3000 m asl increased 50% of SOC concentration in the
whole soil prole (117 cm depth). Regarding Puna agriculture,
only traditional tillage conservation technologies (chiwa and
chacmeo) for potato crop were found in the literature review.
Chiwa consists in the opening of the pasture using a footplough
(chakitaklla), depositing the potato seed at a depth of 1020 cm,
and covering the seed with the removed sod (Oswald et al., 2009).
Chacmeo consists in turning two clods of soil on top of the
grassland to form a row, where the potato seed is planted (Oswald
et al., 2009). In both cases, ridges are built and hilling is performed.
However, we did not nd studies assessing the impact of these
technologies on soil attributes.
A practice to reduce the effect of high grazing pressure on native
grasslands while enhancing animal performance is rotational
grazing. In a Dry Puna study, grasslands species loss was
diminished and grassland condition improved when rotational
grazing was applied (Swinton and Quiroz, 2003). Caas et al.
(2003) found that under high grazing intensities, a common
occurrence in the Puna, animal performance increases under
rotational grazing due to a more efcient use of the forage.
Ecosystem service it promotes
Food provision, genetic resources, pest and disease control, pollination regulation
Soil fertility, water regulation
Carbon sequestration
Food provision, carbon sequestration, soil fertility
Nutrient cycling, soil fertility, food provision, pest and disease control
Food provision, soil fertility
Soil fertility, nutrient cycling, carbon sequestration, water regulation, food, wool and ber provision
Carbon sequestration, nutrient cycling, soil fertility, pest and disease control
Nutrient cycling, soil fertility
Food provision, water regulation
Depends on specic project
Food provision, pest and disease control, water regulation
Food provision, microclimate regulation, water provision and regulation
Carbon sequestration, nutrient cycling, soil fertility, food, wool and ber provision
Food provision, microclimate regulation, water regulation, soil fertility
Water provision and regulation
Carbon sequestration, water regulation, microclimate regulation
 J.L. Rolando et al. / Agriculture, Ecosystems and Environment 236 (2017) 221233 229

5.3. Grassland ecological restoration
An ecosystem is considered functional when the balance
between resource acquisition and resource loss is positive (Tong-
way and Hindley, 2004). Considering this conceptual framework,
the main aim of ecological restoration in drylands is to reduce soil
erosion resource losses- and recover soil functional attributes
such as nutrient cycling, water inltration and soil stability (see
Maestre and Puche, 2009). Although these functional attributes
should trigger the proliferation of plant diversity and complexity of
plant communities, they remain untested in Puna grasslands. At
high degradation levels and low plant cover, structures such as
rocks or branches can facilitate water catching and intercept
sediments mobilized by runoff or wind, hence avoiding water and
eolian erosion and creating soil fertility islands (Tongway and
Ludwig, 1996). These structures can also serve as object
nurseries, increasing seed germination and allowing seedling
survival and recruitment (avoiding excessive radiation and
temperature oscillation) whereas the plant-plant competition is
reduced (Munguia-Rosas and Sosa, 2008). In a Puna grassland
between 3800 and 4700 m asl in Southern Peru, Monerris (2012)
found that microsites close to tussocks of Festuca orthophylla (the
dominant species) and shrubs showed higher values of soil
functional attributes related to nutrient cycling, inltration and
stability, and also of number of shrub seedlings than bare soil
(Fig. 3). This evidence highlights the relevance of using microsites
close to perennial vegetation as functional places for sowing seeds
or seedlings in grassland reclamation programs. This evidence also
illustrates the relevance of perennial plant species in plant
community recovery after disturbance. Furthermore, it has been
observed that plant recruitment increases in sites below perchs
(perch effect, Pausas et al., 2006) that provide shelter for seed
dispersal by bird species. The installation of structures for birds
resting could be tested in the restoration of Puna grasslands.

Fig. 3. A) Average value  standard error (n = 10) of three functional indexes related to soil stability, inltration and nutrient cycling (see details in Maestre and Puche, 2009)
measured in microsites under Festuca orthophylla tussocks, shrubs and bare soil of a Puna grassland located at Salinas y Aguada Blanca National Reserve in Southern Peru
(Monerris, 2012). Different letters mean signicant differences using Mann-Withney test. B) Shrub seedlings growing associated to F. orthophylla tussocks in Salinas y Aguada
Blanca Puna grassland (Photo taken by J. Monerris).
230 J.L. Rolando et al. / Agriculture, Ecosystems and Environment 236 (2017) 221233
Furthermore, the restoration of native grasslands would promote
livestock production and be a source of manure to assure long-
term soil fertility of Puna croplands.
5.4. Conservation of agrobiodiversity
Traditionally, the high climatic heterogeneity of the Puna has
been overcome by strategic and complementary use of altitudinal
agroclimatic belts, crop rotations and the selection of adapted crop
and livestock species and varieties (Altieri and Toledo, 2011). In
addition, biodiversity has played an important role to cope with
abiotic and biotic stresses. For instance, a mixture of native and
improved potatoes reduced the effect of frost in the Bolivian
Altiplano, compared to single variety plots (Condori et al., 2014). In
turn, crop rotations, especially when fallow periods are included,
reduce pest and diseases incidence and increase soil fertility by
restoring SOC and plant-assimilable N (Aguilera et al., 2013; de
Haan, 2009). This is especially relevant under a changing climate
that induces shortages in water availability, and increases
occurrence of extreme climatic events and outbursts of crop pests
and diseases in higher altitudes (Section 4.1; Anderson et al., 2009;
de Haan, 2009; Postigo, 2014). Moreover, it has been suggested that
increased agrobiodiversity, especially at large scales (e.g. agro-
ecosystem and landscape scales) promotes the conservation of the
pollination and pest control services (Jackson et al., 2007). In a Wet
Puna study at the agroecosystem level, Mart and Pimbert (2014)
found that in a multi-cropping and no-pesticide system, pollina-
tion and pest control services were in place. The conservation of
these ecosystem processes in high-altitude belts are important
because the species providing these ES differ from the ones from
lower altitude agroecosystems (Marti and Pimbert, 2014).
In order to conserve agro-biodiversity, local cultural practices
that support seed ow and the formation of reliable networks are
key elements to be enhanced (Zimmerer et al., 2015). Being seed
ow a gender-inuenced process in which women are the
principal actors in intra-community ows and both sexes equally
important in extra-community seed ows (Zimmerer, 2003),
policy making focused in maintaining Andean seed ow should be
gender sensitive. Other activity to promote in-situ agro-biodiver-
sity conservation and increased seed ow is the repatriation of
potato native cultivars from the International Potato Center (CIP)
genebank to Andean local communities (Graddy, 2013).
5.5. Modern irrigation and water harvesting
The implementation of modern irrigation systems increase
water-use efciency, however, it is currently limited by the lack of
public investments (e.g. Roco et al., 2014). Water is a limiting
resource in the region and currently it is not managed in a
sustainable and rational way. In the Peruvian Andes, only 30% of
the agricultural land is under irrigation and out of this percentage,
91.5% is watered by ood irrigation (INEI, 2013). Using the same
amount of water, a larger extension of land could be irrigated if
more efcient irrigation techniques were used (i.e. drip-irrigation,
partial root-zone drying irrigation, or sprinkler irrigation).
Water availability in the region could also be increased with the
practice of water harvesting, a set of different technologies to
collect and store rainfall water in order to use it for agricultural
purposes. These technologies have been widely proposed for arid
and semi-arid environments leading to successful examples of
land rehabilitation of degraded agroecosystems at a landscape
level (Bruins et al., 1986; Godfray et al., 2010). In the Puna, the
usage of water reservoirs and articial wetlands (bofedales) have
been in place for agricultural purposes before the Spanish conquest
of the Americas (Lane, 2014). The size of these water reservoirs are
of between 10 and 15 m in diameter and hold between 100 and
300 m3 of water; while articial bofedales consists in networks of
canals supplying water to Puna wetlands for pastoral activities
(Lane, 2014). The expansion of the wetland area does not only
improve the water provision service, but also regulates water ow
during the dry season, increases water quality and contributes to
soil carbon sequestration due to the high SOC levels of Puna
wetlands.
5.6. Plant breeding
The planting of high-yield commercial cultivars obtained from
plant breeding mixed with local stress-tolerant varieties has been
shown to promote resilience and high yields under the occurrence
of stress events while preserving local agrobiodiversity (Condori
et al., 2010, 2014). Breeding of precocious crop varieties as a
strategy to escape drought events might be instrumental for
coping with the shortening of the rainy season occurring in the
Puna (Valdivia et al., 2010). Also, the selection of resistant varieties
of traditional crops (i.e. quinoa, potatoes, oca, olluco (Ullucus
tuberosus) or mashua (Tropaeolum tuberosum)) might alleviate the
effects of droughts or cold waves in crop production. For instance,
there are quinoa varieties with high drought and frost resistance
(Jacobsen et al., 2003). Furthermore, some of these local varieties
also have high salt tolerance and low nutrient requirements
(Jacobsen et al., 2003) suggesting that they could be used even in
degraded soils.
5.7. Climate change mitigation schemes and payment for ecosystem
services
In spite of the importance of the Puna as a provider of different
environmental services including SOC sequestration in undis-
turbed grasslands and water cycling featuring the role of glaciers
and wetlands- no scheme of compensation for ES has been
implemented in Peru. Although a legislation is in place (i.e.
Peruvian Law No 30215), enforcement is very weak. The lack of
attention to the Puna Region, as opposed to rainforests areas,
which receive most of the attention of environmentalists, does not
facilitate the implementation of incentives for ES. In an attempt to
revert this trend, an inter-institutional effort to generate the
evidence needed to formulate an Andean NAMA (Nationally
Appropriate Mitigation Action) co-led by CIP and the Peruvian
Ministry of the Environment was implemented in 2016. This
agricultural NAMA for the Andes will be oriented to protect the
SOC stocks affected by land-use change from natural grasslands
into exploitative maca elds. Soil carbon sequestration may be as
or even more effective than aboveground carbon sequestration,
and provides an opportunity for grassland conservation or
restoration plans amenable to payment for ES and climate change
mitigation schemes (Farley et al., 2013).
5.8. Traditional technologies
In the Altiplano, which comprises both Wet and Dry Puna, Waru
Waru or raised elds surrounded by ooded ditches, diminish the
high daily temperature extremes through the high specic heat of
water, while maintaining adequate soil moisture even during ood
or drought events (Altieri and Toledo, 2011). Besides providing
microclimate regulation, this technology also increases cultivated
area and soil depth and fertility, since the silt accumulated in its
canal can be incorporated on top of the raised eld (Raymondi
et al., 2012). Spate irrigation, or qocha, is a technology also
developed in the Altiplano, and consists of a complex network or
canals and 2060 m wide soil depressions controlling elds soil
moisture by a system of dikes and dams (Earls, 2006). Furthermore,
there are communal management practices to prevent degradation
 J.L. Rolando et al. / Agriculture, Ecosystems and Environment 236 (2017) 221233
of wetlands through a system of canals, furrows and dams to
expand the wetland area (Castro-Lucic, 2002; Verzijl and Guerrero
Quispe, 2013). These last two technologies are important for water
provision and regulation for agriculture and specically wetland
restoration for preventing SOC oxidation of wetlands highly
organic soils (Section 3.3).
In the Puna, bench terraces are believed to have been in place
since at least 2900 years B.P. (Pajares and Llosa, 2011). Posthumus
and Stroosnijder (2010) found that this technology is able to
increase yields and conserve soils by controlling run-off rates in the
Puna region. There is also empirical evidence that long-standing
terraces sequester SOC, and tend to have greater N and P contents
than non-terraced soils (Sandor and Eash, 1995). In order to make it
economically feasible for peasants to adopt and maintain this
technology over the years, it should be oriented to high market
value crops and accompanied by irrigation, fertilization and crop
rotation (Posthumus and Stroosnijder, 2010). It must be stressed
that the success of this set of ancient Andean agricultural
technologies is not only based on the artifacts themselves but
on the social software behind them, which demands a high degree
of social cohesion to successfully perform the required communal
work to maintain the technologies in place (Altieri and Toledo,
2011; Earls, 2006).
6. Conclusions
The ecological relevance of the Puna region lies in its high
degree of biodiversity, water provision and regulation, high SOC
stocks, and provisioning of farming outputs. Key agriculture-
related ES in the Puna are being affected by climate change,
agricultural intensication and expansion, overgrazing, and
mining activities. Soil fertility tend to be poor in this region being
soil erosion a major threat for soil degradation. Thus, soil
conservation practices, and nutrients replenishment and cycling
are highly required. Related to SOC sequestration, well managed
Wet Puna grasslands and wetlands sequester great amounts SOC.
Thus, national policies to promote Puna grassland and wetland
restoration would be instrumental for climate change mitigation
and water provision and regulation (Table 4). Conservation of
biodiversity and agrobiodiversity needs also to be seriously
addressed due to its relation with pollination regulation, conser-
vation of genetic resources, pest and disease control and food
provision. Water provision, a major limiting resource for crop
production in the region, will be even scarcer in the near-future,
and its buffering capacity during the dry season diminished due to
climate change effects on precipitation, glaciers receding and
wetlands drying up. Thus, application of technologies for water
conservation and harvesting, and efcient modern irrigation
technologies should be promoted. In the Puna, however, enforce-
ment of policies related to climate change mitigation schemes and
payment for ES are still very weak.
Traditional agricultural technologies have been widely used in
the Puna to cope with climatic variability. The selection of varieties
and seed ow between Andean communities promote and
conserve high levels of agro-biodiversity, while traditional local
technologies like bench terraces, qochas or Waru Warus reduce soil
erosion and assure adequate soil moisture and temperature for
crop production. Modern technologies such as judicious chemical
fertilization, modern irrigation, and the planting of high yield
cultivars can be coupled with ancient technologies for a sustain-
able intensication of Puna agroecosystems. Labor and nancial
requirements and economic and environmental performance of
potential technologies should be fully evaluated before consider-
ing them for dissemination among farmers.
231
Acknowledgements
This work was supported by the CGIAR Research Programs on
Climate Change, Agriculture and Food Security (CCAFS) and Root,
Tubers and Bananas (RTB). Authors would like to thank Dr. Carmen
Josse for providing map information in order to limit our study
area. As well as to the two anonymous reviewers who provided
relevant feedback to improve the nal version of this manuscript.
References
Aguilera, J., Motavalli, P.P., Gonzales, M.A., Valdivia, C., 2012. Initial and residual
effects of organic and inorganic amendments on soil properties in a potato-
based cropping system in the Bolivian Andean Highlands. Am. J. Exp. Agr. 2,
641666.
Aguilera, J., Motavalli, P., Valdivia, C., Gonzales, M.A., 2013. Impacts of cultivation
and fallow length on soil carbon and nitrogen availability in the Bolivian Andean
Highland region. Mt. Res. Dev. 33, 391403.
Altieri, M.A., Toledo, V.M., 2011. The agroecological revolution in Latin America:
rescuing nature, ensuring food sovereignty and empowering peasants. J.
Peasant Stud. 38, 587612.
Anderson, E.P., Marengo, J., Villalba, R., Halloy, S., Young, B., Cordero, D., Gast, F.,
Jaimes, E., Ruiz, D., 2009. Consequences of climate change for ecosystems and
ecosystem services in the tropical andes. In: Herzog, S.H., Martnez, R.,
Jrgensen, P.M., Tiessen, H. (Eds.), Climate Change and Biodiversity in the
Tropical Andes. Inter-American Institute for Global Change Research (IAI) and
Scientic Committee on Problems of the Environment (SCOPE), pp. 118.
Anthelme, F., Jacobsen, D., Macek, P., Meneses, R.I., Moret, P., Beck, S., Dangles, O.,
2014. Biodiversity patterns and continental insularity in the tropical high andes.
Arct. Antarct. Alp. Res. 46, 811828.
Baied, C., Wheeler, J., 1993. Evolution of high Andean puna ecosystems:
environment, climate, and culture change over the last 12,000 years in the
Central Andes. Mt. Res. Dev. 13, 145156.
Baraer, M., Mark, B., McKenzie, J., Condom, T., Bury, J., Huh, K., Portocarrero, C.,
Gomez, J., Rathay, S., 2012. Glacier recession and water resources in Perus
Cordillera Blanca. J. Glaciol. 58, 134150.
Barbera, V., Poma, I., Gristina, L., Novara, A., Egli, M., 2012. Long-term cropping
systems and tillage management effects on soil organic carbon stock and steady
state level of C sequestration rates in a semiarid environment. Land Degrad. Dev.
23, 8291.
Bierman-Lytle, P.W., 2015. Climate change impact on high-Altitude ecosystems and
their impact on human communities. In: ztrk, M., Hakeem, K.R., Faridah-
Hanum, I., Efe, R. (Eds.), Climate Change Impacts on High-Altitude Ecosystems.
Springer International Publishing, 289-341.
Bommarco, R., Kleijn, D., Potts, S.G., 2013. Ecological intensication: harnessing
ecosystem services for food security. Trends Ecol. Evol. 28, 230238.
Bradley, R.S., Vuille, M., Diaz, H.F., Vergara, W., 2006. Climate change: threats to
water supplies in the tropical Andes. Science 312, 17551756.
Brandt, J., Townsend, P., 2006. Land use land cover conversion, regeneration and
degradation in the high elevation bolivian andes. Landscape Ecol. 21, 607623.
Bruins, H.J., Evenari, M., Nessler, U., 1986. Rainwater-harvesting agriculture for food
production in arid zones: the challenge of the African famine. Appl. Geogr. 6, 13
32.
Bundschuh, J., Litter, M.I., Parvez, F., Romn-Ross, G., Nicolli, H.B., Jean, J.-S., Liu, C.-
W., Lpez, D., Armienta, M.A., Guilherme, L.R.G., et al., 2012. One century of
arsenic exposure in Latin America: a review of history and occurrence from 14
countries. Sci. Total Environ. 429, 235.
Bush, M.B., Hanselman, J.A., Gosling, W.D., 2010. Nonlinear climate change and
Andean feedbacks: an imminent turning point? Glob Change Biol. 16, 3223
3232.
Buytaert, W., de Bivre, B., 2012. Water for cities: the impact of climate change and
demographic growth in the tropical Andes. Water Resour. Res. 48, W08503.
Buytaert, W., Cuesta-Camacho, F., Tobn, C., 2011. Potential impacts of climate
change on the environmental services of humid tropical alpine regions. Global
Eco. Biogeogr. 20, 1933.
Caas, R., Quiroz, R., Len-Velarde, C., Posadas, A., Osorio, J., 2003. Quantifying
energy dissipation by grazing animals in harsh environments. J. Theor. Biol. 20,
1933.
Castro-Lucic, M., 2002. Local norms and competition for water in Aymara and
Atacama communities. In: Boelens, R., Hoogendam, P. (Eds.), Water Rights and
Empowerment. Van Gorcum Publishers, Assen, the Netherlands, pp. 187201.
Catorci, A., Cesaretti, S., Velasquez, J.L., Malatesta, L., Zeballos, H., 2014. The interplay
of land forms and disturbance intensity drive the oristic and functional
changes in the dry Puna pastoral systems (southern Peruvian Andes). Plant
Biosyst. 148, 547557.
Chevallier, P., Pouyaud, B., Suarez, W., Condom, T., 2011. Climate change threats to
environment in the tropical Andes: glaciers and water resources. Reg. Environ.
Change 11, 179187.
Coteaux, M.M., Herv, D., Mita, D., 2008. Carbon and nitrogen dynamics of potato
residues and sheep dung in a two-Year rotation cultivation in the bolivian
altiplano. Commun. Soil Sci. Plant Anal. 39, 475498.
232 J.L. Rolando et al. / Agriculture, Ecosystems and Environment 236 (2017) 221233
Condori, B., Hijmans, R.J., Quiroz, R., Ledent, J.-F., 2010. Quantifying the expression of
potato genetic diversity in the high Andes through growth analysis and
modeling. Field Crop. Res 119, 135144.
Condori, B., Hijmans, J., Ledent, J.F., Quiroz, R., 2014. Managing potato biodiversity to
cope with frost risk in the high Andes: a modeling perspective. PLoS One 9,
e81510.
Crespo-Prez, V., Rgnire, J., Chuine, I., Rebaudo, F., Dangles, O., 2015. Changes in
the distribution of multispecies pest assemblages affect levels of crop damage in
warming tropical Andes. Glob. Change Biol. 21, 8296.
Dangles, O., Carpio, C., Barragan, A.R., Zeddam, J.L., Silvain, J.F., 2008. Temperature as
a key driver of ecological sorting among invasive pest species in the tropical
andes. Ecol. Appl. 18, 17951809.
de Haan, S., Jurez, H., 2010. Land use and potato genetic resources in Huancavelica,
central Peru. J. Land Use Sci. 5, 179195.
de Haan, S., Nuez, J., Bonierbale, M., Ghislain, M., 2010. Multilevel agrobiodiversity
and conservation of Andean potatoes in Central Peru. Mt. Res. Dev. 30, 222231.
de Haan, S., 2009. Potato Diversity at Height: Multiple Dimensions of Farmer-driven
In-situ Conservation in the Andes. PhD Thesis. Wageningen University, The
Netherlands.
Devenish, C., Gianella, C., 2012. 20 Years of Sustainable Mountain Development in
the Andes from Rio 1992 to 2012 and Beyond. CONDESAN, Lima.
Dillehay, T.D., Rossen, J., Andres, T.C., Williams, D.E., 2007. Preceramic adoption of
peanut, squash, and cotton in northern Peru. Science 316, 18901893.
Dixon, J., Gulliver, A., Gibbon, D., 2001. Farming Systems and Poverty: Improving
Farmers Livelihoods in a Changing World. FAO and World Bank, Rome,
Washington DC, pp. 412.
Dyurgerov, M.B., Meier, M.F., 2005. Glaciers and the Changing Earth System: a 2004
Snapshot. Institute of Arctic and Alpine Research Occasional Paper, vol. 58.
University of Colorado, Boulder, Colorado, USA.
Earls, J., 2006. La Agricultura Andina Ante Una Globalizacin En Desplome. CISEPA-
PUCP, Lima.
Farley, K., Bremer, L., Harden Hartsig, J., 2013. Changes in carbon storage under
alternative land uses in biodiverse Andean grasslands: implications for
payment for ecosystem services. Conserv. Lett. 6, 2127.
Fleisher, D.H., Condori, B., Quiroz, R., Alva, A., Asseng, S., Barreda, C., Bindi, M.,
Boote, K., Ferrise, R., Franke, a.c., Govindakrishnan, P.M., Harahagazwe, D.,
Hoogenboom, G., Kumar, S.N., Merante, P., Nendel, C., Olesen, J.E., Parker, P.
S., Raes, D., Raymundo, R., Ruane, A.C., Stocle, C., Supit, I., Vanuytrecht, E.I.,
Wolf, J., Woli, P., 2016. A potato model intercomparison across varying
climates and productivity levels. Glob. Change Biol. doi:http://dx.doi.org/
10.1111/gcb.13411.
Fonte, S.J., Vanek, S.J., Oyarzun, P., Parsa, S., Quintero, D.C., Rao, I.M., Lavelle, P., 2012.
Pathways to agroecological intensication of soil fertility managements by
smallholder farmers in the Andean highlands. In: Sparks, D.L. (Ed.), Advances in
Agronomy, vol. 116. Elsevier, San Diego, pp. 125162.
GLIMS, NSIDC, updated 2016. Global Land Ice Measurements from Space glacier
database. Compiled and made available by the international GLIMS community
and the National Snow and Ice Data Center, Boulder CO, U.S.A. 2005, 10.7265/
N5V98602.
Garreaud, R.D., Vuille, M., Compagnucci, R., Marengo, J., 2009. Present-day South
American climate. Palaeogeogr. Palaeoclimatol. Palaeoecol. 281, 180195.
Garreaud, R.D., 1999. Multiscale analysis of the summertime precipitation over the
central Andes. Mon. Weather Rev. 127, 901921.
Garreaud, D.R., 2000. Intraseasonal variability of moisture and rainfall over the
South American Altiplano. Mon. Weather Rev. 128, 33373346.
Gibbon, A., Silman, M.R., Malhi, Y., Fisher, J.B., Meir, P., Zimmermann, M., Dargie, G.C.,
Farfan, W.R., 2010. Ecosystem carbon storage across the grassland-Forest
transition in the high andes of manu national park, Peru. Ecosystems 13, 1097
1111.
Gobierno Regional de Junin, 2015. Siembras de los principales cultivos. Campaa
Agrcola: 20132014/2014-2015. Periodo: Agosto Marzo. On-line: http://
agrojunin.gob.pe/index.php/direccion-de-informacion-agraria/estadistica.
Godfray, H.C.J., Beddington, J.R., Crute, I.R., Haddad, L., Lawrence, D., Muir, J.F., Pretty,
J., Robinson, S., Thomas, S.M., Toulmin, C., 2010. Food security: the challenge of
feeding 9 billion people. Science 327, 812818.
Gomez-Montano, L., Jumpponen, A., Gonzales, M.A., Cusicanqui, J., Valdivia, C.,
Motavalli, P.P., Herman, M., Garrett, K.A., 2013. Do bacterial and fungal
communities in soils of the Bolivian Altiplano change under shorter fallow
periods? Soil Biol. Biochem. 65, 5059.
Gomiero, T., Pimentel, D., Paoletti, G., 2011. Is there a need for a more sustainable
agriculture? Crit. Rev. Plant Sci. 30, 623.
Graddy, T., 2013. Regarding biocultural heritage: in situ political ecology of
agricultural biodiversity in the Peruvian Andes. Agric. Hum. Values 30, 587
604.
Gross, K.L., Mittelbach, G.G., Reynolds, H.L., 2005. Grassland invisibility and
diversity: responses to nutrients, seed input, and disturbance. Ecology 86, 476
486.
Hinojosa, L., 2013. Change in rural livelihoods in the Andes: do extractive industries
make any difference? J. Commun. Dev. 48, 421436.
Hobbs, R.J., Huenneke, L.F., 1992. Disturbance, diversity, and invasion: implications
for conservation. Conserv. Biol. 6, 324337.
Hofstede, R., Chilito, E.J., Sandovals, E.M., 1995. Vegetative structure, microclimate,
and leaf growth of a piramo tussock grass species, in undisturbed, burned and
grazed conditions. Vegetatio 119, 5365.
Hofstede, R., 1995. The effects of grazing and burning on soil and plant nutrient
concentrations in Colombian pramo grasslands. Plant Soil 173, 111132.
Houghton, R., 2012. Historic changes in terrestrial carbon storage. In: Lal, R., Lorenz,
K., Httl, R.F., Schneider, B.U., von Braun, J. (Eds.), Recarbonization of the
Biosphere. Springer, Dordrecht, pp. 5982.
INEI, 2013. Resultados Denitivos IV Censo Nacional Agropecuario 2012. INEI,
Ministerio de Agricultura y Riego, Lima.
Jackson, L.E., Pascual, U., Hodgkin, T., 2007. Utilizing and conserving
agrobiodiversity in agricultural landscapes. Agr. Ecosyst. Environ. 121, 196210.
Jacobsen, S.E., Mujica, A., Jensen, C.R., 2003. The resistance of quinoa (Chenopodium
quinoa willd:) to adverse abiotic factors. Food Rev. Int. 19, 99109.
Josse, C., Cuesta, F., Navarro, G., Barrena, V., Cabrera, E., Chacn-Moreno, et al., 2009.
Ecosistemas De Los Andes Del Norte Y Centro. Bolivia, Colombia, Ecuador, Per Y
Venezuela. Secretara General de la Comunidad Andina, Programa Regional
ECOBONA-Intercooperation, CONDESAN-Proyecto Pramo Andino, Programa
BioAndes, EcoCiencia, NatureServe, IAvH, LTA-UNALM, ICAE-ULA, CDC-UNALM,
RUMBOL SRL, Lima.
Juen, I., Kaser, G., Georges, C., 2007. Modelling observed and future runoff from a
glacierized tropical catchment (Cordillera Blanca, Per). Global Planet. Change
59, 3748.
Kandus, P., Quintana, R.D., Minotti, P.G., del Pilar Oddi, J., Baigun, C., Gonzalez Trilla,
G., Ceballos, D., 2011. Ecosistemas de humedal y una perspectiva
hidrogeomrca como marco para la valoracin ecolgica de sus bienes y
servicios. In: Laterra, P., Jobbagy, E., Paruelo, J. (Eds.), Valoracin De Servicios
Ecosistmicos: Conceptos, Herramientas Y Aplicaciones Para El Ordenamiento
Territorial. Instituto Nacional de Tecnologa Agropecuarias. Buenos Aires,
Argentina, pp. 265290.
Kaya, H.K., Alczar, J., Parsa, S., Kroschel, J., 2009. Microbial control of the Andean
weevil complex. Fruit Veg. Cereal Sci. Biotech. 3, 3945.
Lal, R., 2013. Food security in a changing climate. Ecohydrol. Hydrobiol. 13, 821.
Lane, K., 2014. Water technology in the andes. In: Selin, H. (Ed.), Encyclopaedia of
the History of Science, Technology, and Medicine in Non-Western Cultures, , pp.
124.
Lavado Casimiro, W.S., Labat, D., Ronchail, J., Espinoz, J.C., Guyot, J.L., 2013. Trends in
rainfall and temperature in the Peruvian AmazonAndes basin over the last 40
years (19652007). Hydrol. Process 27, 29442957.
Lobell, D.B., Burke, M.B., Tebaldi, C., Mastrandrea, M.D., Falcon, W.P., Naylor, R.L.,
2008. Prioritizing climate change adaptation needs for food security in 2030.
Science 319, 607610.
Lu, X., Yan, Y., Fan, J., Wang, X., 2012. Gross nitrication and denitrication in alpine
grassland ecosystems on the Tibetan Plateau. Arct. Antarct. Alp. Res. 44, 188
196.
Maestre, F.T., Puche, M.D., 2009. Indices based on surface indicators predict soil
functioning in Mediterranean semi-arid steppes. Appl. Soil Ecol. 41, 342350.
Magrin, G.O., Marengo, J.A., Boulanger, J.-P., Buckeridge, M.S., Castellanos, E., Poveda,
G., Scarano, F.R., Vicua, S., 2014. Central and south america. In: Barros, V.R.,
Field, C.B., Dokken, D.J., Mastrandrea, M.D., Mach, K.J., Bilir, T.E., Chatterjee, M.,
Ebi, K.L., Estrada, Y.O., Genova, R.C., Girma, B., Kissel, E.S., Levy, A.N., MacCracken,
S., Mastrandrea, P.R., White, L.L. (Eds.), Climate Change 2014: Impacts,
Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of
Working Group II to the Fifth Assessment Report of the Intergovernmental Panel
on Climate Change. Cambridge University Press, Cambridge, United Kingdom
and New York, NY, USA, pp. 14991566.
Maldonado Fonkn, M.S., 2014. An introduction to the bofedales of the Peruvian
High Andes M.S. Mires Peat 15, 113.
Marengo, J.A., Chou, S.C., Kay, G., Alves, L.M., Pesquero, J.F., Soares, W.R., Santos, D.C.,
Lyra, A.A., Sueiro, G., Betts, R., Chagas, D.J., Gomes, J.L., Bustamante, J.F., Tavares,
P., 2011. Development of regional future climate change scenarios in South
America using the Eta CPTEC/HadCM3 climate change projections: climatology
and regional analyses for the Amazon, So Francisco and the Paran river basins.
Clim. Dynam. 38, 18291848.
Mark, B.G., Bury, J., McKenzie, J.M., French, A., Baraer, M., 2010. Climate change and
tropical Andean glacier recession: evaluating hydrologic changes and livelihood
vulnerability in the Cordillera Blanca. Peru. An. Assoc. Am. Geogr. 100, 794805.
Mart, N., Pimbert, M., 2014. Barter markets for the conservation of agroecosystem
multi-functionality: the case of the chalayplasa in the Peruvian Andes. Int. J. Agr.
Sustain. 5, 5169.
McDowell, J.Z., Hess, J.J., 2012. Accessing adaptation: multiple stressors on
livelihoods in the Bolivian highlands under a changing climate. Global Environ.
Change 22, 342352.
Millennium Ecosystem Assessment, 2005. Ecosystems and Human Well-being:
Synthesis. Island Press.
Minvielle, M., Garreaud, R.D., 2011. Projecting rainfall changes over the south
american altiplano. J. Climate 24, 45774583.
Mohr, K.I., Slayback, D., Yager, K., 2014. Characteristics of precipitation features and
annual rainfall during the TRMM era in the central andes. J. Clim. 27, 39824001.
Monerris, J.J., 2012. Anlisis De La Estructura Y La Funcin De Los Pajonales Sobre
Arenal En La Puna Seca Del Sur De Per MSc. Thesis. Universidad Nacional
Agraria La Molina, Per.
Muoz, M.A., Faz, A., Zornoza, R., 2013. Carbon stocks and dynamics in grazing
highlands from the Andean Plateau. Catena 104, 136143.
Munguia-Rosas, M.A., Sosa, V.J., 2008. Nurse plants vs. Nurse objects: effects of
woody plants and rocky cavities on the recruitment of the Pilosocereus
leucocephalus columnar cactus. Ann. Bot. 101, 175185.
Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B., Kent, J., 2000.
Biodiversity hotspots for conservation priorities. Nature 403, 853858.
Oswald, A., de Haan, A., Sanchez, J., Ccanto, R., 2009. The complexity of simple tillage
systems. J. Agr. Sci. 147, 399410.
 J.L. Rolando et al. / Agriculture, Ecosystems and Environment 236 (2017) 221233
Pajares Garay, E., Llosa Larrabure, J., 2011. Relational knowledge systems and their
impact on management of mountain ecosystems: approaches to understanding
the motivations and expectations of traditional farmers in the maintenance of
biodiversity zones in the Andes. Manage. Environ. Qual.: Int. J. 22, 213232.
Patty, L., Halloy, S.R.P., Hiltbrunner, E., Krner, C., 2010. Biomass allocation in
herbaceous plants under grazing impact in the high semi-arid Andes. Flora 205,
695703.
Pausas, J.G., Bonet, A., Maestre, F.T., Climent, A., 2006. The role of the perch effect on
the nucleation process in Mediterranean semi-arid oldelds. Acta Oecologica-
Int. J. Ecol. 29, 346352.
Perez, C., Nicklin, C., Dangles, O., Vanek, S., Sherwood, S., Halloy, S., Garret, K., Forbes,
G., 2010. Climate change in the high andes: implications and adaptation
strategies for small-scale farmers. Int. J. Environ. Cult. Econ. Soc. Sustain. 6, 71
88.
Pestalozzi, H., 2000. Sectoral fallow systems and the management of soil fertility:
the rationality of indigenous knowledge in the high Andes of Bolivia. Mt. Res.
Dev. 20, 6471.
Posthumus, H., Stroosnijder, L., 2010. To terrace or not: the short-term impact of
bench terraces on soil properties and crop response in the Peruvian Andes.
Environ. Dev. Sustain. 12, 263276.
Postigo, J., 2014. Perception and resilience of andean populations facing climate
change. J. Ethnobiol. 34, 383400.
Power, A., 2010. Ecosystem services and agriculture: tradeoffs and synergies. Phil.
Trans. R. Soc. B 365, 29592971.
Powlson, D.S., Bhogal, A., Chambers, B.J., Coleman, K., Macdonald, A.J., Goulding, K.
W.T., Whitmore, A.P., 2012. The potential to increase soil carbon stocks through
reduced tillage or organic material additions in England and Wales: a case study.
Agr. Ecosyst. Environ. 146, 2333.
Quintero, M., Comerford, N.B., 2013. Effects of conservation tillage on total and
aggregated soil organic carbon in the Andes. Open J. Soil Sci. 3, 361373.
Rabatel, A., Francou, B., Soruco, A., Gomez, J., Cceres, B., Ceballos, J.L., et al., 2013.
Current state of glaciers in the tropical Andes: a multi-century perspective on
glacier evolution and climate change. Cryosphere 7, 81102.
Rabinowitz, D., Linder, C.R., Ortega, R., Begazo, D., Murguia, H., Douches, D.S., Quiros,
C.F., 1990. High levels of interspecic hybridization between Solanum
sparsipilum and S. stenotomum in experimental plots in the Andes. Am. Pot. J.
67, 7381.
Racoviteanu, A.E., Arnaud, Y., Williams, M.W., Ordonez, J., 2008. Decadal changes in
glacier parameters in the Cordillera Blanca, Peru, derived from remote sensing.
J. Glaciol. 54, 499510.
Rambal, S., Ratte, J.P., Mouillot, F., Winkel, T., 2015. Trends in quinoa yield over the
southern bolivian altiplano: lessons from climate and land-Use projections.
Quinoa: Improv. Sustain. Produc. 4762.
Rasmussen, C., Lagnaoui, A., Esbjerg, P., 2003. Advances in the knowledge of quinoa
pests. Food Rev. Int. 19, 6175.
Raymondi, A.M., Delgado Arias, S., Elder, R.C., 2012. Technological solutions for
climate change adaptation in the peruvian Highlands, human and social
dimensions of climate change. In: Chhetri, N. (Ed.), InTech, doi:http://dx.doi.
org/10.5772/50465.
Reichl, C., Schatz, M., Zsak, G., 2015. World Mining Data. International Organizing
Committee for the World Mining Congresses.
Rocha, J., 2011. Agricultural intensication, market participation, and household
demography 2016 in the Peruvian Andes. Hum. Ecol. 39, 555568.
Roco, L., Engler, A., Bravo-Ureta, B., Jara-Rojas, R., 2014. Farm level adaptation
decisions to face climatic change and variability: evidence from Central Chile.
Environ. Sci. Policy 44, 8696.
Rojas, M., Manchego, A., Rocha, C.B., Fornelis, L.A., Silva, R.C., Mendes, G.S., et al.,
2016. Outbreak of diarrhea among preweaning alpacas (Vicugna pacos) in the
southern Peruvian highland. J. Infect. Dev. Ctries. 10, 269274.
Romero, C.C., 2005. A Multi-scale Approach for Erosion Assessment in the Andes.
PhD Thesis. Wageningen University, The Netherlands.
Salvarredy-Aranguren, M.M., Probst, A., Roulet, M., Isaure, M.-P., 2008.
Contamination of surface waters by mining wastes in the Milluni Valley
(Cordillera Real, Bolivia): mineralogical and hydrological inuences. Appl.
Geochem. 23, 12991324.
Sanabria, J., Calanca, P., Alarcn, C., Canchari, G., 2014. Potential impacts of early
twenty-rst century changes in temperature and precipitation on rainfed
annual crops in the Central Andes of Peru. Reg. Environ. Change 14, 15331548.
Sandor, J.A., Eash, N.S., 1995. Ancient agricultural soils in the andes of southern Peru.
Soil Sci. Soc. Am. J. 59, 170179.
Sarmiento, L., Bottner, P., 2002. Carbon and nitrogen dynamics in two soils with
different fallow times in the high tropical Andes: indications for fertility
restoration. Appl. Soil. Ecol. 19, 7989.
Scurrah, M., Celis-Gamboa, C., Chumbiauca, S., Salas, A., Visser, R.G.F., 2008.
Hybridization between wild and cultivated potato species in the Peruvian
233
Andes and biosafety implications for deployment of GM potatoes. Euphytica
164, 881892.
Segnini, A., Posadas, A., Quiroz, R., Milori, D.M.B.P., Costa Saab, S., Martin-Neto, L.,
Vaz, C.M.P., 2010. Spectroscopic assessment of soil organic matter in wetlands
from the high andes. Soil Sci. Soc. Am. J. 74, 22462253.
Segnini, A., Posadas, A., Quiroz, R., Milori, D.M.B.P., Vaz, C.M.P., Martin-Neto, L., 2011.
Soil carbon stocks and stability across an altitudinal gradient in southern Peru. J.
Soil Water Conserv. 66, 213220.
Simpson, B., 1983. An historical phytogeography of the high Andean ora. Rev. Chil.
Hist. Nat. 56, 109122.
Swinton, S., Quiroz, R., 2003. Is poverty to blame for soil, pasture and forest
degradation in Perus altiplano? World Dev. 31, 19031919.
Thibeault, J.M., Seth, A., Garcia, M., 2010. Changing climate in the Bolivian Altiplano:
CMIP3 projections for temperature and precipitation extremes. J. Geophys. Res.
115, D08103.
Thierfelder, C., Amzquita, C.E., Stahr, K., 2005. Effects of intensifying organic
manuring and tillage practices on penetration resistance and inltration rate.
Soil Till. Res. 82, 211226.
Thorne, P., Tanner, J., 2002. Livestock and nutrient cycling in crop-animal systems in
Asia. Agr. Syst. 71, 111126.
Tongway, D.J., Hindley, N.L., 2004. Landscape Function Analysis: Procedures for
Monitoring and Assessing Landscapes with Special Reference to Minesites and
Rangelands. CSIRO, Brisbane, Australia.
Tongway, D.J., Ludwig, J.A., 1996. Rehabilitation of semiarid landscapes in Australia.
I. Restoring productive soil patches. Restor. Ecol. 4, 388397.
Urrutia, R., Vuille, M., 2009. Climate change projections for the tropical Andes using
a regional climate model: temperature and precipitation simulations for the
end of the 21st century. J. Geophys. Res. 114 doi:http://dx.doi.org/10.1029/
2008JD011021.
Valdivia, C., Seth, A., Gilles, J., Garca, M., Jimnez, E., Cusicanqui, J., Navia, F., Yucra,
E., 2010. Adapting to climate change in andean ecosystems: landscapes, capitals,
and perceptions shaping rural livelihood strategies and linking knowledge
systems. Ann. Assoc. Am. Geogr. 100, 818834.
Vanek, S., Drinkwater, L., 2013. Environmental, social, and management drivers of
soil nutrient mass balances in an extensive andean cropping system.
Ecosystems 16, 15171535.
Velsquez-Milla, D., Casas, A., Torres-Guevara, J., Soriano, A., 2011. Ecological and
socio-cultural factors inuencing in situ conservation of crop diversity by
traditional Andean households in Peru. J. Ethnobiol. Ethnomed. 7, 40.
Verzijl, A., Guerrero Quispe, S., 2013. The system nobody sees: irrigated wetland
management and alpaca herding in the Peruvian Andes. Mt. Res. Dev. 33, 280
293.
Vuille, M., Keimig, F., 2004. Interannual variability of summertime convective
cloudiness and precipitation in the central Andes derived from ISCCP-B3 data. J.
Climate 17, 33343348.
Vuille, M., Bradley, R., Werner, M., Keimig, F., 2003. 20th century climate change in
the tropical Andes: observations and model results. Clim. Change 59, 7599.
Vuille, M., Kaser, G., Juen, I., 2008a. Glacier mass balance variability in the Cordillera
Blanca, Peru and its relationship with climate and the large-scale circulation.
Global Planet. Change 62, 1428.
Vuille, M., Francou, B., Wagnon, P., Juen, I., Kaser, G., Mark, B.G., Bradley, R.S., 2008b.
Climate change and tropical Andean glaciers: past, present and future. Earth-
Sci. Rev. 89, 7996.
Vuille, M., Franquist, E., Garreaud, R., Lavado Casimiro, W.S., Cceres, B., 2015. Impact
of the global warming hiatus on Andean temperature. J. Geophys. Res. Atmos.
120, 37453757.
West, T.O., Post, W.M., 2002. Soil organic carbon sequestration rates by tillage and
crop rotation: a global data analysis. Soil Sci. Soc. Am. J. 66, 19301946.
Wilcox, B.P., Bryant, F.C., Allen, B.L., 1986. Grassland communities and soils on a high
elevation grassland of the central Andes of Peru. Phytologia 61, 231250.
Wilcox, B.P., Bryant, F.C., Belaun Fraga, V., 1987. An evaluation of range condition on
one range site in the Andes of Central Peru. J. Range Manage. 40, 141145.
Young, K.R., 2009. Andean land use and biodiversity: humanized landscapes in a
time of change. Ann. Missouri Bot. Gard. 96, 492507.
Zimmerer, K.S., Carney, J.A., Vanek, S.J., 2015. Sustainable smallholder
intensication in global change? Pivotal spatial interactions, gendered
livelihoods, and agrobiodiversity. Curr. Opin. Environ. Sustain. 14, 4960.
Zimmerer, K.S., 2003. Geographies of seed networks for food plants (potato, ulluco)
and approaches to agrobiodiversity conservation in the Andean countries. Soc.
Nat. Resour. 16, 583601.
Zimmermann, M., Meir, P., Silman, M.R., Fedders, A., Gibbon, A., Malhi, Y., Urrego, D.
H., Bush, M.B., Feeley, K.J., Garcia, K.C., Dargie, G.C., Farfan, W.R., Goetz, B.P.,
Johnson, W.T., Kline, K.M., Modi, A.T., Rurau, N.M.Q., Staudt, B.T., Zamora, F.,
2010. No differences in soil carbon stocks across the tree line in the Peruvian
Andes. Ecosystems 13, 6274.