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REVIEW ARTICLE
Ecosystem services in orchards. A review
Constance Demestihas
1,2
&Daniel Plénet
1
&Michel Génard
1
&Christiane Raynal
3
&
Françoise Lescourret
1
Accepted: 21 March 2017
#INRA and Springer-Verlag France 2017
Abstract Arboriculture must maintain acceptable fruit produc-
tion levels while preserving natural resources. This duality can
be analyzed with the concept of ecosystem service. We
reviewed the literature on orchards to explain how ecological
functions modified by agricultural practices provide six ecosys-
tem services - fruit production, climate regulation, soil nitrogen
availability, water regulation, pest and disease control, and pol-
lination -and which indicators could describe them. The major
points are, first, that orchards have a high potential of multiple
services. They can sequester from 2.4 to 12.5 t C/ha/year. Their
perennial character and multi-strata habitat, as well as the op-
portunity of creating diversified hedgerows and cover crops in
alleys, may contribute to a high level of biodiversity and related
services. Second, every service depends on many functions.
Fruit yield, which could reach up to 140 t/ha in apple orchards,
is increased by light interception, carbon allocation, and nitro-
gen and water uptake. Third, agricultural practices in orchards
have a strong impact on ecosystem functions and, consequent-
ly, on ecosystem services. Overfertilization enhances nitrogen
leaching, which reduces soil nitrogen availability for the plant
and deteriorates the quality of drained water. Groundcover in-
creases humification and reduces denitrification and runoff,
thus enhancing soil nitrogen availability and water regulation.
It also enhances biotic interactions responsible for pest control
and pollination. Pruning may increase fruit quality trough a
better carbon allocation but decreases pest control by fostering
the dynamics of aphids.
To study multiple ecosystem services in orchards, we sug-
gest using models capable of simulating service profiles and
their variation according to management scenarios. We then
refer to the available literature to show that conflicts between
provisioning and regulating services can be mitigated by ag-
ricultural practices. Improved knowledge of soil processes and
carbon balance as well as new models that address multiple
services are necessary to foster research on ecosystem service
relationships in orchards.
Keywords Agricultural management .Fruit production .
Climate regulation .Soil nitrogen availability .Wa ter
regulation .Pest and disease control .Pollination .Indicator
Content
1. Introduction
2. Ecosystem services in commercial orchards
2.1. Provisioning service: fruit production in terms of
quantity and quality
2.1.1. Organogenesis
2.1.2. Light interception, carbon assimilation and
allocation
2.1.3. Water and nitrogen effects
2.2. Regulation and maintenance services
2.2.1. Climate regulation: mitigation of green-
house gas emissions
2.2.2. Soil nitrogen availability
2.2.3. Water regulation: hydrological cycle and
water flow maintenance
2.2.4. Pest and disease control
2.2.5. Life cycle maintenance: pollination
3. Assessing and analyzing multiple ecosystem services
in orchards
*Françoise Lescourret
francoise.lescourret@inra.fr
1
PSH, INRA, 84000 Avignon, France
2
CTIFL, Centre de Saint-Rémy, Route de Mollégès,
13210 Saint-Rémy de Provence, France
3
CTIFL, Centre de Lanxade, 41 Route des Nébouts,
24130 Prigonrieux, France
Agron. Sustain. Dev. (2017) 37:12
DOI 10.1007/s13593-017-0422-1
3.1. Using models to quantify indicators of ecosystem
services and their connections
3.2. Analyzing multiple ecosystem service relationships
4. Conclusions
Acknowledgements
References
1 Introduction
Arboriculture today is beset by contradictory demands. On the
one hand, there is a pressing demand regarding the quality of
products. The quality standards of fruits, most of which are
sold to the fresh market, are very high (Codron et al. 2005). At
the same time, on a global scale, the fruit sector is very com-
petitive and yield is a great concern for fruit growers. This has
led to the intensification of production techniques, especially
of pesticide use in orchards worldwide. For example, in 2012,
French apple orchards (Fig. 1a andb)receivedanaverageof
35 pesticide treatments (MAAF 2014). On the other hand,
society has expressed concern about this over-use of agricul-
tural inputs because of their dramatic impact on natural re-
sources and ecosystem functioning, including the pollution
of groundwater, subsoil and the atmosphere, as well as the
decrease in biodiversity (Geiger et al. 2011;Mottesetal.
2014).
Ecologicalintensification is aimed at reconciling high yield
goals with minimal negative impacts on the environment. This
can be done by integrating the management of ecosystem
services into crop production systems (Bommarco et al.
2013). During the 1970s, the term “Ecosystem Service”began
to appear in the scientific literature, but two important publi-
cations in the 1990s, those of Costanza et al. (1997)andof
Daily (1997), were actually responsible for initiating ecosys-
tem service research. In these publications, ecosystem services
were defined as the wide array of conditions and processes
through which ecosystems and their biodiversity confer ben-
efits to humanity. More precisely, the cascade model (Fig. 2)
of Haines-Young and Potschin (2009) places ecosystem ser-
vices in the middle of a ‘production chain’, which links the
entities that define services upstream: biophysical structures
and functions and, downstream, the benefits reaped from the
services, which are their real value.
The Millennium Ecosystem Assessment (Reid et al. 2005)
classified ecosystem services into four categories: regulating,
supporting, provisioning and cultural services. However,
supporting services are means to human ends, and not ends
themselves (Wallace 2007). Based on these considerations,
alternative ecosystem service classifications have been pro-
posed. Most recently, the Common International
Classification of Ecosystem Services (CICES) was confined
to the ecosystem outputs directly consumed or used by a ben-
eficiary, i.e., ‘final’services, and thus excluded the supporting
services linked to ecosystem functions that underpin these
final services (Haines-Young and Potschin 2013).
In sharp contrast to the case of forest ecosystems, which are
known for their ability to sequestrate carbon or regulate the
water cycle (Krieger 2001; García-Nieto et al. 2013), the con-
cept of ecosystem service has not yet been widely used in fruit
orchard research. A major difference between orchard and
forest ecosystems is that in orchards, the focus is on the pro-
duction of consumable and high-quality food, whereas the
multi-functionality of wood-producing forests, which is close
to the ecosystem service concept, has long been recognized.
However, orchards present particular features that could make
them interesting for ecosystem service studies. For example,
the perennial character of trees, the multi-strata habitat and the
plant diversity within the boundaries of orchards (Fig. 1b)
may contribute to a high level of biodiversity (Simon et al.
2010). The potential of carbon sequestration by orchard soils
could be valorized and increased to contribute to greenhouse
gas mitigation (Rodríguez-Entrena et al. 2012).
Managing multiple ecosystem services appears to be a
great challenge for agroecosystems (Zhang et al. 2007). In
orchards, as in other agroecosystems, this requires broad
knowledge about the underlying ecological functions and of
the effect, in turn, of agricultural management on these func-
tions. It should be noted that agricultural practices may impact
ecosystem services positively, but they might also impact
them negatively. This negative impact is called a disservice
by some authors (Power 2010, Zhang et al. 2007). Typically,
in an orchard, pesticide use has negative consequences on the
quality of water (Loewy et al. 2003)oronbiodiversity(Floch
et al. 2009). Pesticides may disturb food webs since they are
not only lethal to crop pests but also to beneficiary insects as
well as pollinators (Biddinger et al. 2013;Geigeretal.2011;
Thompson 2003). Herbicides may also disturb natural nutrient
decomposition by killing beneficiary earthworms, fungi and
bacteria in soil (Oliveira and Merwin 2001; Andersen et al.
2013).
The objective of this review is to describe ecosystem ser-
vices and their management in orchards, based on an analysis
of agroecosystem functioning. This review is based on the
CICES classification. The scale of the study is the plot, which
is composed of trees, alleys, soil, hedges and various biotic
and abiotic elements such as pests, natural enemies, gas, min-
eral elements and water. In the following section, we review
the literature on orchards to explain how ecological functions
modified by agricultural practices provide ecosystem services,
and we discuss which indicators could best describe ecosys-
tem services. We also consider the negative environmental
impacts of agricultural practices. The ecosystem services an-
alyzed include fruit production, climate regulation by mitiga-
tion of greenhouse gas emissions, soil nitrogen availability,
water regulation in terms of hydrological cycle and water flow
maintenance, pest and disease control, and life cycle
12 Page 2 of 21 Agron. Sustain. Dev. (2017) 37:12
maintenance through pollination. Lastly, we present a general
procedure to analyze multiple ecosystem services and their
relationships in orchards, using examples from other crops.
2 Ecosystem services in commercial orchards
The scheme in Fig. 3serves as a guide for the following
description. In this description we focus, for each of the six
selected services and according to the cascade model of Fig. 2,
on the underlying ecosystem functions, the way agricultural
management influences them and which service indicators
could be used. The choice of ecosystem service indicators is
a sensitive issue. Authors agree that they should adequately
characterize the complexity of the ecosystem but be simple
enough to be efficiently monitored and modeled while staying
closely linked to ecosystem services and being predictive of
changes within ecosystem service relationships (Dale and
Polasky 2007; de Groot et al. 2010; van Oudenhoven et al.
2012).
In Fig. 3, many ecosystem functions, which are impacted
by climate and soil composition and structure, transform abi-
otic elements such as nitrogen, carbon or water and/or enable
them to flow through the whole orchard system through other
compartments such as the atmosphere and the groundwater
table and, more globally, towards other surrounding
Fig. 1 a: Apple orchard with
anti-hail nets over the Golden
Delicious variety, in southeastern
France (photo credits: C.
Demestihas). b: Opilion spider
(Hadrobunus grandis)on
Crimson Crisp® apple cultivar
(photo credits: C. Demestihas)
Agron. Sustain. Dev. (2017) 37:12 Page 3 of 21 12
ecosystems. Several connected functions may contribute to
one service –evapotranspiration, carbon assimilation and ni-
trogen uptake are all functions that contribute to fruit produc-
tion. However, one function may also have an impact on many
services. Thus, nitrogen leaching, enhanced by heavy rains
and over-fertilization, reduces soil nitrogen availability for
the plant and deteriorates the quality of drained water.
In Fig. 3, only the major levers of agricultural management
that act upon ecosystem functions are presented. On the one
hand, a single function can be affected by several agricultural
practices. Thus, nitrogen uptake by trees is influenced by
fertilization, cultivar/rootstock choice and groundcover man-
agement. On the other hand, a single agricultural practice can
affect one or more ecosystem functions, thus modifying sev-
eral ecosystem services at the same time. Irrigation affects
functions that contribute to nitrogen availability, water regu-
lation and fruit production. An agricultural practice can also
affect a given function in various ways. Fertilization has con-
trasting effects on nitrogen leaching and uptake by trees de-
pending on whether it is mineral or organic. In addition, as
mentioned above, we consider disturbances to the ecosystem
caused by agricultural practices as a result of pollution.
Fig. 3 Linking agricultural
management (pink boxes),
ecosystem functions (dark green
boxes for plant-related functions,
orange boxes for soil-related
functions and gray boxes for pest-
related functions) and ecosystem
services (light green boxes) in the
orchard agroecosystem. The pink
box, ‘Groundcover management’,
concerns a wide range of options
including legumes, cover crops,
grasses, pruning wood and
senescent leaves left on the ground,
etc. Agricultural management,
ecosystem functions and ecosystem
services are linked by lines and each
color is associated with a function.
Soil composition and structure as
well as climate (violet boxes) are
considered separately from
agricultural practices. Soil is
impacted by groundcover
management as well as weed and
pest control. Climate is considered
to impact all functions
Fig. 2 Relationship between agricultural practices, physical and biological structures, functions, services and benefits according to the “cascade model”
of Haines-Young and Potschin (2009) in an agroecosystem
12 Page 4 of 21 Agron. Sustain. Dev. (2017) 37:12
2.1 Provisioning service: Fruit production in terms
of quantity and quality
Fruit yield isthe result of the number of fruits and fruit mass at
harvest. Fruit mass and fruit quality result from the fruit grow-
ing process, which is mainly driven by carbon. We therefore
analyze the fruit production service in terms of organogenesis
of fruits and leaves, light interception, carbon assimilation and
allocation (Fig. 3). We also consider water and nitrogen effects
since nitrogen and water stress may impact fruit yield and
quality. Temperature determines the phenology of fruit trees
and also impacts crop load and fruit color (Saure 1990), but its
effects will not be discussed in detail in this review.
2.1.1 Organogenesis
Fruit initiation is a complex process. Under temperate cli-
mates, the flower development cycle in fruit trees often lasts
from 9 to 10 months, putting flower buds into dormancy be-
tween two major activity periods: the appearance of floral
primordia in summer and the final flower formation during
the following spring. Several factors impact this initiation:
endogenous or exogenous hormones and, more specifically,
gibberellins, which tend to decrease flower bud formation in
alternately bearing apple cultivars, or ecological conditions
such as temperature (Koutinas et al. 2010). It is hypothesized
that under low light, a reduced number of flower buds are
differentiated (Grappadelli 2003). In order to set fruits, com-
patible pollen grains must be deposited on the stigma. In the
case of self-incompatible or dioecious species, pollinizers
must be compatible with the cultivar being pollinated and
blooming at the same time (Dennis 2003). In this case, the
pollination service (Section 2.2.5.) is crucial since pollen is
primarily transferred by insects such as honey or bumble bees
(Dennis 2003). Agricultural practices such as floral thinning,
which may be of interest to reach an optimal number of fruits
for yield objectives, may use drying agents that disturb the
pollination or fertilization process (Mathieu et al. 2011).
2.1.2 Light interception, carbon assimilation and allocation
Light has an immediate effecton the photosynthetic activity of
fruit trees since the net total dry matter productivity of apple
orchard systems depends on intercepted photosynthetic pho-
ton fluxes ranging from 400 to 700 nm (Wünsche et al. 1996).
The most light-efficient apple orchard configurations have
been reported as being capable of intercepting 60–70% of
available radiation, which may translate into high yields
(Grappadelli 2003) that can reach up to 120 to 140 t/ha
(Lakso et al. 1999) as a theoretical potential. In apple crops,
the mean conversion efficiency of light intercepted to grams of
fruit ranges from 4 to 6.1 g/MJ according to the cultivar, the
rootstock as well as the tree training system (Robinson et al.
1993), but values as low as 2 g/MJ have been assessed
(Robinson et al. 1991).
Planting patterns and training systems are ways of increas-
ing light interception. At the orchard level, a fraction of light
does not reach the tree canopy due to the alleyways main-
tained between rows that make up a large proportion of or-
chard area uncovered by trees (Jackson and Palmer 1980).
Increasing the height of the trees in proportion to the clear
alley width helps alleviate this problem since it results in in-
creasing light interception (Grappadelli 2003). More direct
means consist in decreasing tree spacing through planting
density and changing arrangements since, for example, there
is higher light interception with square tree spacing than with
rectangular tree spacing (Palmer et al. 1992). Natural training
systems used in apple orchards, including centrifugal training
(Lauri 2002), may allow good light penetration but require
highly developed horticultural skills.
Carbon assimilation and allocation depend on complex
source-sink relationships within the tree. Fruits are sinks and
the fruit load is important in this respect. A heavy sink load
promotes the synthesis of soluble sugars that are readily load-
ed into the phloem and transported to sink organs (Klages
et al. 2001). On the contrary, a low demand for carbon en-
hances the accumulation of starch, first in leaves and then in
roots and other woody tissues (Naschitz et al. 2010), inhibiting
photosynthesis. When fruit demand is higher than the poten-
tial carbon supply, the competition between fruits is intensi-
fied and results in fruit abscission (Zibordi et al. 2009), where-
as in the reverse situation, fruit set and growth are favored.
However, self-regulatory mechanisms such as natural fruit
abscission are usually not sufficient to meet market require-
ments for fruit size. In many apple-producing areas, early
removal of flowers and newly-grown fruits are currently used
to reduce competition for photosynthates (Racskó 2006). The
severity and timing of thinning are major factors that impact
crop load, return bloom and, consequently, fruit size and yield.
The carbon source-sink balance may also impact other fruit
quality characteristics. It has been shown that a lower crop
load in ‘Jonagold’apple cultivar results in a higher content
of polyphenols, redder fruit blush, a higher percentage of sol-
uble solids in fruit flesh and better flesh firmness in compar-
ison to fruits from high-cropping trees (Stopar et al. 2002).
The crop load strongly impacts carbon allocation between
different biochemical compounds and, as a result, the profile
of fruit in terms of soluble sugars and acids as shown for peach
fruit (Souty et al. 1999; Génard et al. 2008).
2.1.3 Water and nitrogen effects
Water stress (deficit of water allocation to tree organs; see
Fig. 3) can have serious impacts on carbon assimilation since
shoot expansion is almost linearly reduced by declining mid-
day stem water potentials (Lakso 2003). Furthermore, the
Agron. Sustain. Dev. (2017) 37:12 Page 5 of 21 12
coupled translocation of water and sugars within the tree un-
deniably links water stress to carbon allocation in fruits
(Daudet et al. 2002). A high level of water stress may reduce
fruit size and increase the proportion of dry matter in the flesh
and, consequently, soluble solids in the fruit. Water stress also
tends to increase titrable acidity in ripe fruits, probably
through dilution/dehydration effects and osmotic adjustment
(Etienne et al. 2013). The timing of water stress is important.
Late spring and early summer water stress can have dramatic
effects on fruit set and growth (Lakso 2003). Kilili et al.
(1996) have shown that withholding irrigation late in the sea-
son (104 days after full bloom) improved the quality of
‘Braeburn’apple cultivar in terms of increased total soluble
solids, firmness, soluble sugars and intensified red skin color
without adverse effects on fruit size and yield. These results
were confirmed by Mpelasoka et al. (2001).
Irrigation classically seeks to compensate for water stress.
The irrigation system is of utmost importance. The root sys-
tem distribution depends on the spatial distribution of water
status in the soil (Sokalska et al. 2009) and it has been shown
that under arid conditions, apple roots concentrate under drip
emitters, whereas roots of microjet-irrigated trees are more
widely distributed over the soil volume (Neilsen et al. 2000).
Furthermore, there may be considerable functional variability
across the apple root systems (Green and Clothier 1999). In
addition, the impact of water stress depends on the rootstock
genotype. Inapple crops, highly drought tolerant and sensitive
rootstocks have been described (Atkinson et al. 1998; Lakso
2003).
Nitrogen is required to support the growth of new tissues.
Compared to many other crops, the annual nitrogen require-
ments of fruit trees are relatively small: in the case of apple
trees, 100–120 kg N/ha, for about 45 to 50 t/ha apples
(Greenham 1980; Cheng and Raba 2009). These estimates
correspond to whole nitrogen budgets according to the princi-
ples of Neilsen and Neilsen (2003). Few studies have been
undertaken on fruit tree roots but they suggest that nitrogen
supply could vary widely since root length density ranges
from 525 to 1234 m/m
3
in apple rootstocks (Ma et al. 2013).
Furthermore, nitrogen uptake could be mainly located in the
first 20 cm of soil depth in which the root system seems to be
more predominantly distributed (Ma et al. 2013) and where
nitrogen mineralization occurs. The rooting densities of apple
trees are smaller than those of Poaceae species with which
they compete (Neilsen and Neilsen 2002), especially at the
interface of tree rows and alleys.
Nitrogen supply may have a positive effect on the carbon
source-sink balance and, therefore, on fruit production. As leaf
and whole tree photosynthetic capacity is improved by nitro-
gen supply, the leaf area to fruit ratio increases, leading to
more cells per fruit and to larger fruits (Xia et al. 2009).
Concerning soluble sugars in fruit, the accumulation of
sugars slightly increases with higher N supply as a result of
the improved supply of carbon to fruit or starch degradation
(Xia et al. 2009). According to Raese (1998), repeated appli-
cations of mono-ammonium phosphate or N-P-K fertilizers
may induce fruit disorders and a lower soil pH, while fertil-
izers such as calcium nitrate [Ca(NO
3
)
2
] improve fruit color
and firmness. High nitrogen application could diminish fruit
color and decrease fruit firmness at harvest and during storage
since it increases fruit internal ethylene and respiration
(Fallahi and Mohan 2000; Fallahi et al. 2002;Xiaetal.
2009). System experiments conducted in Washington State
(Peck et al. 2006), which compared organic, integrated and
conventional cropping systems, showed higher fruit firmness
under organic management where the only source of nitrogen
was from cover crop legumes. Contradictory effects of nitro-
gen nutrition on fruit acidity have been reported (Etienne et al.
2013). Regarding nitrogen concentration in fruit, which may
be important for apple wine and cider processing (Alberti et al.
2011;KelkarandDolan2012), Toselli et al. (2000)showeda
positive effect of nitrogen applied at bloom, probably because
fruit in the first stages of its growth successfully competes
with other tree organs for nitrogen accumulation.
Nitrogen management must be correctly driven according
to nitrogen uptake and to nitrogen reserve remobilization in
order to create compromises with possible nitrate
water-pollution. Many single-dose or premature spring fertil-
izer applications may not be efficient if the temperature con-
ditions prohibit nitrate absorption by the roots. Furthermore,
during early spring, nitrogen uptake may be inhibited by ni-
trogen reserve remobilization that occurs at the same time; this
makes early application of nitrogen ineffective (Neilsen and
Neilsen 2002). In addition, this “extra”nitrogen can easily be
leached after a heavy rain (Tagliavini et al. 1996). Agricultural
practices such as fertigation may lower the quantity of applied
nitrogen compared to broadcast applications (Neilsen and
Neilsen 2003), thus contributing to lower leaching (Klein
et al. 1989). Other practices such as foliar nitrogen spraying
may also have the benefit of controlling the timing of nitrogen
supply and potentially reducing the total inputs and losses to
the environment since nitrogen is more directly absorbed by
leaves.
Regarding the service of fruit production in terms of quan-
tity and quality, the choice of indicators (Table 1) is quite
straightforward because standards have been developed for
the fruit supply chain and in the horticultural literature. Yield
is classically used to describe the production in terms of quan-
tity of any crop in multiple service assessment (Dale and
Polasky 2007; Kragt and Robertson 2014; Schipanski et al.
2014; Syswerda and Robertson 2014). The five quality criteria
cited below can be assessed at the plot scale using meanvalues
at harvest, given that the spatial variability of fruit quality is
large (Génard and Bruchou 1992; Taylor et al. 2007). These
criteria cover the concerns of various stakeholders, from fruit
growers to consumers. Fruit mass is a convenient proxy
12 Page 6 of 21 Agron. Sustain. Dev. (2017) 37:12
because it is both a component of yield and the basis to cal-
culate fruit size and fruit size classes that correspond to market
standards. Color grades, titrable acidity and total soluble solids
are standard organoleptic criteria widely used for fruit crops
(e.g., Ebel et al. 1993; Mills et al. 1994; Mpelasoka et al. 2001;
Reganold et al. 2001; Peck et al. 2006). Firmness is used
worldwide (e.g., Mpelasoka et al. 2001;Pecketal.2006)as
a gage of ripeness and, therefore, of fruit harvest.
2.2 Regulation and maintenance services
2.2.1 Climate regulation: Mitigation of greenhouse gas
emissions
There are limited references to greenhouse gas emissions and
mitigation in orchards in the literature. Denitrification and
carbon sequestration in trees and soil, which is a function of
carbon assimilation and allocation (Fig. 3), are two important
ecosystem functions in this respect. Denitrification is the pro-
cess by which nitrates are reduced to nitrous oxide (N
2
O), a
greenhouse gas of which 87% is emitted by agriculture
(CITEPA 2016). Denitrification depends on the physical and
chemical conditions of the soil (organic matter, texture, den-
sity, pH, temperature and humidity) on climate (rainfall and
temperature) and on agricultural practices (Hénault et al.
2013). Consequently, N
2
O emissions are subject to high var-
iability in time and space; at just a few centimeters distance,
emissions can vary one-hundred fold. In orchards, irrigation
systems such as surface drip irrigation may enhance denitrifi-
cation because of an anoxic waterlogged bulb created under
the distribution tubing. Heavy rains during summer - when
soil humidity is already maintained at field capacity –enhance
this anoxic waterlogged bulb. This probably explains the
higher emissions of N
2
O observed under drip irrigation
(1.6 ± 0.7 kg N
2
O-N/ha/year) compared to microsprinkler
irrigation (0.6 ± 0.3 kg N
2
O-N/ha/year) in almond orchards
(Alsina et al. 2013). Moreover, it has been shown that subsur-
face drip irrigation reduced N
2
O emissions compared to sur-
face drip irrigation in olive orchards (Quiñones et al. 2007).
Furthermore, cropping systems using legume-based nitrogen
inputs generally have lower net N
2
O emissions than cropping
systems that rely on synthetic nitrogen fertilizer inputs (Jensen
Tabl e 1 Ecosystem services indicators, units and references
Ecosystem service Indicator (unit) References
Fruit production Fruit mass (g)
Yield (t/ha) Dale and Polasky 2007; Kragt and Robertson 2014;Schipanski
et al. 2014; Syswerda and Robertson 2014
Size (mm)
Color grade Kilili et al. 1996; Mpelasoka et al. 2001;Pecketal.2006
Titratable acidity (% of malic acid) Kilili et al. 1996; Fallahi and Mohan 2000; Mpelasoka et al.
2001;Pecketal.2006; Xia et al. 2009Soluble solids concentration (SSC) (%)
Firmness (N (newton) or kg/cm
2
)
Climate regulation
through GHG
mitigation
Cumulative denitrified nitrogen (kg N
2
O-N/ha/unit time) Kramer et al. 2006; Groffman et al. 2006
C sequestrated in soil and tree (kg C/ha/unit time) Page et al. 2011;Wuetal.2012; Zanotelli et al. 2015
Cumulative amounts of CO
2
emitted by agricultural
operations (kg C/ha/unit time)
Page et al. 2011; Syswerda and Robertson 2014
Soil nitrogen availability Soil organic nitrogen variation (kg N/ha/unit time) Quiñones et al. 2007
Mean, maximal and minimal soil nitrate concentration
over a time period (mg NO
3
-N/kg of dry soil)
Glover et al. 2000
Water cycle regulation
and maintenance
Mean water content in different soil depths
(g H
2
O/100 g of dry soil)
Syswerda and Robertson 2014
Water drainage (mm/unit time) Kragt and Robertson 2014
Concentration of nitrates in drained water (mg NO
3
-N/l) Schipanski et al. 2014; Syswerda and Robertson 2014
Concentration of pesticides in drained water Loewy et al. 2003;Mottesetal.2014
Pest and disease
regulation
Rates of predation by natural enemies, rates of parasitism
by parasitoids
Dib et al. 2010; Boreau de Roincé et al. 2013;Maaloulyetal.
2013;Monteiroetal.2013;Maaloulyetal.2015
Level of injury severity % fruit loss or % leaf loss or LAI
loss
Indicators or models to assess the environmental impact of
pesticides
Gutsche and Rossberg 1997; Bockstaller et al. 2008
Pollination Abundance and diversity of pollinators Nicholls and Altieri 2013
Number of seeds per fruit Volz et al. 1996; Stern et al. 2001; Garratt et al. 2014
% of fruit set
Agron. Sustain. Dev. (2017) 37:12 Page 7 of 21 12
et al. 2012). Ammonia fertilizers have a greater positive im-
pact on denitrification than other types of mineral fertilizers
(Zhu et al. 2013) and fertigation may increase denitrification
(Riga and Charpentier 1999). The production of N
2
O may
also be exacerbated by incorporating material with a low
C/N ratio (Baggs et al. 2000). Since denitrification is promot-
ed by low O
2
concentrations that typically occur in wet soils,
an increase in macroporosity in the top 50 mm decreases N
2
O
production (Deurer et al. 2009). In orchards, there is experi-
mental evidence that agricultural practices such as the use of
cover crops reduce herbicide use or, in the case of organic
orchards, that green-waste composts favor soil macroporosity
in comparison to conventional orchards where mineral fertil-
izers, herbicides and drip-irrigation are used (Deurer et al.
2009).
It can be noted that the use of one technique for mitigating
N
2
O emissions could jeopardize the mitigation of another
GHG emission. For example, using mechanical weeding
may increase macroporosity and, as such, decrease N
2
O emis-
sions while at the same time increasing CO
2
emissions by
using agricultural engines that run on fuel.
Between 400 and 800 Mt. carbon per year could be seques-
tered worldwide in agricultural soils by implementing appro-
priate management practices including the increased input of
crop residues, reduced tillage and dead wood recycling (IPCC
1995;IPCC2003). The prevailing opinion is that the contri-
bution of orchards to carbon sequestration is negligible. This
opinion refers in large part to the small area that orchards
represent in relation to forests and to low tree height in or-
chards - 3 to 4 m on average, compared to 15 m for deciduous
forests in temperate regions (Luyssaert et al. 2007). It is nev-
ertheless important to estimate the contribution of orchards,
especially in regions where they are highly concentrated.
Studies have shown that fruit orchards such as kiwifruit, ap-
ple, peach, orange and olive could sequester from 2.4 to 12.5 t
C/ha/year (Sofo et al. 2005;Pageetal.2011; Montanaro et al.
2017). Orchards may sequester quantities of carbon similar to
those of forests during their first years of life since photosyn-
thesis activity is greater in young trees than in older ones (Wu
et al. 2012). In addition, pruning, which is intensively used in
orchards, helps increase photosynthesis rates. Furthermore, it
has been found that fruit trees have relatively low respiration
rates compared to many other plants due to the low construc-
tion costs of fruit (in the case of apple trees: Lakso et al. 1999;
Zanotelli et al. 2013). This may lead to less carbon loss
through respiration in the overall carbon cycle system.
Zanotelli et al. (2013) compared the net primary productivity
of a natural woody ecosystem of temperate-humid biomes to
that of an apple orchard. They showed that the carbon fluxes
(gross primary production, net ecosystem productivity and
ecosystem respiration) were quantitatively similar in both
cases. The organic carbon produced yearly in the whole tree
can reach up to 8.54 t C/ha at harvest. It is allocated to the
different apple tree organs as follows: 50% to fruits, 13% to
leaves - compared to 30% for deciduous forests, 23% to
aboveground wood, 2% to belowground wood, and 12% to
fine roots (Zanotelli et al. 2013; Zanotelli et al. 2015). Crop
load, planting pattern, training system, rootstock choice and
water and nitrogen stress may heavily impact this allocation.
In a carbon balance approach, it is important to consider
carbon losses. Mechanical or chemical weeding operations as
well as irrigation could increase carbon mineralization in or-
chard soils, creating carbon loss by heterotrophic respiration
of microorganisms. Furthermore, in most cases, carbon in fruit
trees is only temporarily sequestered since the lifespan of an
orchard ranges from 15 to 30 years and the trees are usually
burned without any valorization at the end of their lives. Life
cycle analyses show that carbon emissions may also come
from other sources: CO
2
emissions by engines during weeding
or fertilization might represent as much as 23% of total CO
2
emissions in intensive apple orchards (Page et al. 2011). It is
therefore important to precisely quantify these losses.
Agricultural management of potentially recyclable ele-
ments of orchards such as pruning wood, mowed grasses or
senescent leaves (in the ‘groundcover management’box in
Fig. 3) may help close the carbon biogeochemical cycle.
Carbon content and humus production from the decomposi-
tion of senescent leaves and pruning material have been mea-
sured in young and mature peach and olive orchards. These
studies have demonstrated that significant amounts of carbon
are sequestered in this way, considering the Mediterranean
fruit production surface (Sofo et al. 2005). The use of cover
crops, brassica seed meal and especially wood chips increases
the quantity of humus in orchard soils, creating carbon storage
within the soil. Soil carbon pools have a mean residence time
of 12 years for wood chip groundcover (Teravest et al. 2011).
According to the above, indicators of denitrification and
carbon sequestration would address the climate regulation ser-
vice in orchards in a complementary manner (Table 1).
Quantification of denitrification is hindered by high spatial
and temporal variations (Groffman et al. 2006). Because of
this temporal variation, cumulative amounts of denitrified ni-
trogen over key periods have been proposed for orchards
(Kramer et al. 2006). More globally, cumulative amounts of
denitrified nitrogen could be used over appropriate time
scales, depending on the objective of the study. The most
commonly applied method to measure denitrification is based
on the ability of acetylene (C
2
H
2
) to inhibit the reduction of
N
2
OtoN
2
(Groffman et al. 2006). In the presence of C
2
H
2
,
N
2
O becomes the terminal product of denitrification, which
can then be quantified by measuring N
2
O production.
However, it is now well established that the acetylene inhibi-
tion method underestimates denitrification under aerobic in-
cubation conditions (Butterbach-Bahl et al. 2013) and that it is
better to use other methods. N
2
O efflux can also be measured
using a static chamber method (Folorunso and Rolston 1984;
12 Page 8 of 21 Agron. Sustain. Dev. (2017) 37:12
Matson et al. 1996). Some denitrification measurements have
been made using methods based on labeled
15
N(Myrold
1990). Similarly, the quantities of carbon sequestered in the
soil and in different tree organs at specific time scales have
been used as indicators in orchards (Page et al. 2011;Wuetal.
2012; Zanotelli et al. 2015). For these measurements, tree
excavation is generally required to measure each organ’sbio-
mass, and closed gas exchange systems (e.g., Licor photosyn-
thesis system with soil CO
2
flux chamber) are necessary to
measure CO
2
emissions from the soil. Measurement chambers
are generally an obstacle to farm machinery. In Zanotelli et al.
(2015), soil respiration measurements were therefore conduct-
ed in a parallel independent trial. Syswerda and Robertson
(2014) used a more sophisticated and data-intensive method
that combined these basic indicators and other parameters to
calculate a global warming impact. This impact was calculated
on a multiannual scale for 20 years by combining the net
global warming impact of soil carbon sequestration, agronom-
ic nitrogen fertilizer application, lime application, fuel usage,
nitrous oxide emissions and methane (CH
4
) oxidation for each
of the studied systems. In view of this type of study, indicators
of the direct impact of agricultural practices in terms of CO
2
emissions are necessary. Cumulative amounts of CO
2
emitted
by crop protection products or engines operating in the or-
chard over the growing season can serve as a simple indicator
(Page et al. 2011; Alaphilippe et al. 2013).
2.2.2 Soil nitrogen availability
Nitrogen availability for nitrogen uptake by plants is the dif-
ference between the inputs of mineral nitrogen, i.e., mineral-
ization of fresh organic matter and humus, fertilization and
nitrogen fixation, the losses caused by leaching, volatilization
and denitrification, and the immobilization of nitrogen caused
by humification (Fig. 3;seeSection2.2.1 for denitrification).
These different functions have been extensively described in a
generic manner (Calvet 2003;BotandBenites2005;White
2006). Regarding orchards, the impact of techniques that act
on soil biological activity, which largely contributes to func-
tions that deliver nitrogen, deserves attention. Studies in apple
orchards have shown higher biological activity, which is able
to enhance mineralization, for organic systems that use cover
crops, groundcovers and composts than for conventional ones
that use more herbicides and mineral fertilizers (Tagliavini
et al. 2007; Hoagland et al. 2008; Teravest et al. 2011).
Similarly, the frequent use of cover crops in orchards may
significantly increase the abundance and activity of fungi
and bacteria that enable humification (Six et al. 2006)since
they present high C/N ratios. Biological nitrogen fixation by
legumes such as white clover (Trifolium repens) in the ground
vegetation of orchards may also be a source of nitrogen input
to the system. Some figures have placed biological nitrogen
fixation in soil within a range of 118 to 126 kg N/ha over a
period of two years in apple orchards, depending on the clover
biomass production and ground vegetation management prac-
tices (Goh et al. 1995). The difficulty lies in the quantification
of the potential nitrogen released from these legumes, espe-
cially because other nitrogen cycle functions tend to be inhib-
itory to symbiotic nitrogen fixation. For example, an excess of
nitrate after mineral fertilizer application can create favorable
conditions for denitrification (Haynes and Goh 1980), which
inhibits nitrogen fixation in the soil.
Soil nitrogen may be loss-driven in fluid forms through
leaching. Kramer et al. (2006) placed the amounts of nitrogen
leached annually in apple orchards within a range of 68 μgof
NO
3
-N at a depth of 100 cm in organic systems, to 1092 μg
NO
3
-N at a depth of 100 cm in conventional systems fertilized
with calcium nitrate. Managing these disservices is difficult
since it is generally the soil texture and structure as well as the
climatic conditions that impact nitrogen leaching. However,
leaching can be reduced by fractioning nitrogen inputs
throughout the year and using cover crops in the alleys. The
minimization of nitrogen leaching in orchards must be based
on reducing the presence of NO
3
−
ions at the end of the veg-
etative period (late autumn) since the major risk of water con-
tamination with leaching occurs during winter and in early
spring (Tagliavini et al. 1996).
Volatilization occurs when nitrogen is lost in its gaseous
form, ammonia. These losses depend on soil conditions (pH,
cation exchange capacity, porosity), climatic conditions and
type of manure spreading. The percentage of nitrogen lost by
volatilization in olive orchards receiving 204 kg N/ha/year
was estimated at 1.8% over 7 days, with much higher losses
a few hours after application than a few days later (Fernández-
Escobar et al. 2012). A proportion of the volatilized nitrogen
can be absorbed by the tree, especially by leaves. Boaretto
et al. (2013) showed that leaf absorption of
15
NH
3
volatilized
from fertilizer was higher in a high planting density system
(7%) than in a standard planting density (3%) in orange
orchards.
Nitrogen “recycling”by leaf and pruned wood restitution
to soil makes it possible to close the nitrogen cycle by using
the aboveground biomass production. Labeled nitrogen exper-
iments conducted on apple trees showed that the amount of
nitrogen derived from leaf litter and taken up by trees over a 2-
year period averaged 713 mg nitrogen per tree, which repre-
sented 16% of the nitrogen originally contained in the leaves
that had returned to the soil (Tagliavini et al. 2007).
To describe soil nitrogen availability in orchards (Table 1),
both soil organic nitrogen content and soil nitrate concentra-
tion, which indicate long- and short-term nitrogen availability,
respectively, should be considered. In addition, as a matter of
principle, dynamics should also be considered. The time win-
dow depends on the objective of the study. The detailed dy-
namics are informative (see Quiñones et al. (2007) for an
example in orchards) but they need to be summarized by a
Agron. Sustain. Dev. (2017) 37:12 Page 9 of 21 12
few statistics for ecosystem service studies. For organic nitro-
gen content, a variation rate over the chosen time window
would be relevant because it describes a balance. For nitrate
concentration, minimal, maximal and mean values are classi-
cally used to summarize a dynamic series (Glover et al. 2000).
Concentrations at key periods of plant development and
growth could also be used. Total nitrogen and NO
3
-N soil
concentrations in different soil layers are assessed by routine
soil analyses in orchards. Alternatively to soil nitrate concen-
tration, simulation studies of multiple ecosystem services in
agroecosystems have used nitrogen mineralization as a proxy
for plant nitrogen availability. It is the case of Schipanski et al.
(2014) who averaged daily values of net nitrogen mineraliza-
tion over several rotation cycles of annual crops, and of Kragt
and Robertson (2014) who used the same proxy on a yearly
basis for mixed crop-livestock systems.
2.2.3 Water regulation: Hydrological cycle and water flow
maintenance
According to the CICES, water regulation services correspond
to the capacity to maintain baseline flows for water supply and
discharge. As in the case of soil nitrogen budget, the ecosys-
tem functions implied in the classical water balance approach,
evapotranspiration, infiltration and runoff (Fig. 3), and their
dependence on soil and water conditions, are well known,
whereas the characteristics of orchards imply specificities.
Evapotranspiration is modified by orchard architecture de-
pending on the planting pattern and the training system, which
impact water vapor diffusion resistance (Lakso 2003).
Covering trees with nets may impact evapotranspiration
(Bastías et al. 2011) in addition to the planting pattern and
the training system. Vaissière et al. (2000) showed that the
atmospheric relative humidity increases by 1 to 4% within hail
nets. Various operations act on infiltration and runoff. First, in
orchards with late cultivars, harvest operations could be detri-
mental to infiltration because harvest takes place at periods
during which the soil can be damp and, therefore, more sen-
sitive to wheel traffic and soil packing. Second, within-row
and inter-row soil management are particularly important. In
the orchard rows, pre-emergence herbicide use, which is very
common, creates bare soil, thus decreasing infiltration and
increasing runoff (Merwin et al. 1994). The presence of a
groundcover in alleys is a characteristic feature of orchards,
although it is not systematic. Oliveira and Merwin (2001)
have shown that the infiltration rate was higher on shredded
hardwood bark mulch systems since they confer a better floor
anchoring and increase permeability through organic matter
and macrofauna. In avocado orchards, mixtures of ryegrass
and clover increase soil organic matter due to groundcover
residues and rhizosphere decomposition (Atucha et al.
2013), thus preventing runoff. However, in mowed grass
groundcovers, tractor wheel traffic during mowing could
significantly reduce infiltration (Becerra et al. 2010).
Nevertheless, it has been reported that groundcovers in or-
chard alleys decrease yield and tree growth due to nutrient
and water competition between grasses and fruit trees
(Robinson and O’Kennedy 1978;Atuchaetal.2013). This
could be corrected via appropriate fertilization and irrigation
management, or by applying a new technique known as the
“sandwich”, which consists of tilling the soil on both sides of
the row while leaving a thin strip of groundcover on the inter-
row (Schmid and Weibel 2000). The sandwich technique has
the advantages of the cover crop in alleys while eliminating
the effect of competition from weeds (Garcin et al. 2012).
Thus, it may also reduce the reliance on herbicides that has
detrimental effects both on soil properties (see above) and on
the quality of water at a large scale through runoff.
Decreasing the quantity of water diverted to agriculture,
which exceeds 70–80% of the total in arid and semi-arid zones
(Fereres and Soriano 2007), is a key issue. Modern irrigation
scheduling concepts have been implemented for this purpose
in orchards. Micro-irrigation methods such as micro-aspersion
or drip irrigation are frequently used, usually controlled by
tensiometers. In limited-water regions, fruit growers are now
using techniques that require less water without affecting the
functioning of the crop. These techniques, which go under the
name of ‘regulated deficit irrigation’(Chai et al. 2016), are
largely based on a balance between a better use of soil water,
more specifically considering the soil water reservoir, together
with punctual evapotranspiration reductions at specific stages
of tree development.
Classical indicators of hydrological cycle components are
available and have been widely adopted (e.g., Pistocchi et al.
2008). Two indicators of the water regulation service are rel-
evant for orchards: drainage and soil water content (Table 1).
They are particularly employed in multi-service studies in
agroecosystems. Cumulative values of drainage per year have
been taken as a proxy for water regulation by Kragt and
Robertson (2014). Soil water content, which is indicative of
soil water availability for plants, was used by Syswerda and
Robertson (2014). As in the case of soil nitrogen availability,
seasonal variation should be dealt with using summary statis-
tics or values at key periods that depend on the purpose of the
study. Syswerda and Robertson (2014) used soil water content
in July, the most water-limited time of the growing season in
the conditions of their study. Soil water availability can be
monitored by tensiometers that measure the soil water tension
(bar) or by capacitance probes that indicate soil water status
(in mm). In addition to these quantitative components, water
quality that can be seriously impaired by the use of fertilizers
and pesticides should be considered (Table 1). The concentra-
tions of nitrates and pesticides in drained water could be
targeted since they are standard indicators used to control
the application of regulation policies such as the Water
Framework Directive in Europe. Nitrate concentrations in
12 Page 10 of 21 Agron. Sustain. Dev. (2017) 37:12
drained water have been used in multi-service studies in
agroecosystems (Schipanski et al. 2014; Syswerda and
Robertson 2014). In the case of orchards, the autumn period,
after fruit harvest, is a relevant time for these concentrations.
Nitrogen leaching can be measured by ion exchange resin
lysimeters, as described by Susfalk and Johnson (2002), but
it remains difficult to evaluate nitrogen leaching at the plot
scale.
2.2.4 Pest and disease control
The perennial character of orchards poses a great pest man-
agement challenge since the various organs of the tree struc-
ture provide multiple suitable habitats for arthropod coloniza-
tion (Beers et al. 2003). At the same time, apple trees host the
agents of over 70 infectious diseases (Grove et al. 2003), in-
cluding bacteria and fungi. These agents cause injuries to the
leaves, fruits, branches and twig organs of the tree. In or-
chards, since most of the production is intended for the fresh
product market, damage to fruits is highly prohibitive for fu-
ture sales and may negatively impact the fruit grower’sin-
come. The occurrence and abundance of pests and diseases
depends on biotic interactions such as predation, on species’
niches and on habitat availability, as well as on dispersal.
The economic value of pest predation is more easily esti-
mated than many other services (Power 2010) since it is pos-
sible to directly substitute insecticides with ecosystem services
provided by natural enemies. It was estimated that the control
of native herbivores by insects led to a savings of 4.49 billion
dollars per year in the United States, based on projections of
losses that would accrue if insects were not functioning at their
current level and assuming that 33% of pest control is attrib-
utable to insects (Losey and Vaughan 2006). In the case of
apple orchards, it was estimated that phytoseiid predatory
mites and Forficula auricularia eliminate the need for 1–2
acaricide sprays and 2–3 insecticide applications per annum,
respectively (Cross et al. 2015). The question is which condi-
tions may favor the control of pests by natural enemies in
orchards.
Beneficialinsects require plant resourcesfor habitat supply.
Plants serving as alternative hosts for a parasitoid or predator
of the target crop pest are known as ‘banker plants’(Frank
2010). Complex landscapes with a high density and connec-
tivity of uncultivated, perennial habitats that include banker
plants have shown an increase in natural enemy populations
(Thies 1999). Such landscapes are encountered in orchard
areas (Schäckermann et al. 2015). The permanency of the
orchard system, which enhances stability and resilience,
multi-strata design and the presence of hedgerows, are likely
to favor natural enemy populations (Simon et al. 2010). For
example, a short groundcover in apple orchard alleys may
favor the abundance and predatory behavior of the general
predator Forficula pubescens (Marliac et al. 2015). The
composition of the groundcover may also have an influence.
Flowering plants such as sweet alyssum (Lobularia maritima)
have shown a significant attraction potential for natural ene-
mies, leading to the suppression of wooly apple aphid
(Eriosoma lanigerum) populations (Gontijo et al. 2013).
Wildflower strips are more controversial since some studies
have shown encouraging results on aphid predator enhance-
ment using wildflower strips in apple orchards (Wyss 1995;
Boller et al. 2004;Pfiffneretal.2013), while others do not
show any significant enhancement of aphid predators (Balzan
et al. 2014). Hedgerows, especially mixed ones, have been
shown to significantly increase the predation rate by providing
shelter to natural enemies (Debras et al. 2011; Miñarro and
Prida 2013). The efficiency of phytoseiid predators such as
Amblyseius andersoni,Kampimodromus aberrans and
Neoseiulus californicus for the regulation of apple red mites
(Panonychus ulmi) has been demonstrated in many studies,
most of which are reviewed in Ricard et al. (2012). The ces-
sation of acaricide treatments to control red mites preserves
these predators, as do semi-natural environments with dense,
high and diversified hedges or groves.
Enhancing habitat supply to the natural enemies of pests
may be useless if pesticides are still used as a fallback. Pest
management is still highly dependent on pesticides in or-
chards because of strict market quality requirements. Many
studies have proven the negative effect of pesticides on natural
enemies of pests (Biddinger and Hull 1995; Biddinger et al.
2013; Cumming and Spiesman 2006; Flexner et al. 1986;
Pekár 1999). Monteiro et al. (2013) and Vasseur et al. (2013)
have shown that pesticides may affect the rate of pest preda-
tion within 100-m-wide buffers around the targeted orchard
and that drift during pesticide applications may affect natural
enemies in the surrounding hedgerows.
Other orchard management practices that consist in intro-
ducing ‘planned’plant biodiversity may initiate ecological
processes linked to the niche and dispersal of pests. This is
the case of push stimuli processes that can be performed
through companion planting of repellent plants that emit nat-
ural chemical substances (Parolin et al. 2012). Cover crops in
alleys with aromatic plants such as Centaurea cyanus,
Saturela hortensis, and Agerarum houstonianum in pear or-
chards can reduce the numbers of herbivore pests while in-
creasing the abundance of predators and parasitoids (Song
et al. 2010). The choice of aromatic plants to enhance pest
control nonetheless requires in-depth research on the aromatic
chemical compounds of plants. Other plants known as trap
plants are, by definition, more attractive to pests than cultivat-
ed crops, thus limiting pests to a particular area where they can
be easily controlled by traditional methods (Parolin et al.
2012). They are used in the push-pull strategy of pushing
away a pest from a repellent plant and attracting it to the
border of the cropped field using trap (“pull”)plants
(Ratnadass et al. 2012). In addition, fruit trees provide
Agron. Sustain. Dev. (2017) 37:12 Page 11 of 21 12
resources for pests. Direct modifications of the host plant
driven by agricultural practices may help decrease pest popu-
lations. For example, in peach orchards, decreasing pruning
intensity may lower the degree of green peach aphid (Myzus
persicae) infestation due to the decrease in the proportion of
growing shoots on which aphids develop much better than on
short shoots (Grechi et al. 2008). Similarly, in apple orchards,
rosy apple aphid (Dysaphis plantaginea) infestation signifi-
cantly decreases when the degree of branching, which can
be modified by tree training, increases. The underlying hy-
pothesis is that the number of crossroads related to the
branching degree affects the probability of reaching the target
resource (Simon et al. 2012).
Apple diseases such as apple scab (Venturia inaequalis)
and powdery mildew (Podosphaera spp.) may be managed
using control methods that could avoid the eight to ten fungi-
cide applications per season (Grove et al. 2003)ormore
(MAAF, 2014). Genetic control is the most important lever
to managing diseases. Many genes that confer resistance to
Venturia inaequalis have been identified for apple (Brun et al.
2007). Over 50 scab-resistant cultivars have been released and
are gaining in commercial acceptance, while other horticultur-
al characteristics are being simultaneously improved (Grove
et al. 2003). A breakdown of the resistance coded by Vf, the
most frequently used apple scab resistance gene, has been
found (Parisi et al. 1993). This makes it urgent to diversify
the sources of resistance to apple scab and to define new
breeding strategies.
Mitigating apple scab infection via the plant itself is possi-
ble through different agricultural practices. Leaf wetness is
important for apple scab, as demonstrated by the fact that leaf
wetness duration together with air temperature are used to
assess the level of risk of the disease (Mills and LaPlante
1951). Simon et al. (2006) make the hypothesis that training
systems such as centrifugal training, which have a positive
impact on light interception (Willaume et al. 2004), lead to a
higher degree of aeration within the trees, thus shortening the
wetness periods that lead to scab infection. Concerning irriga-
tion systems, foliage aspersion can favor foliar wetness, cre-
ating ideal conditions for apple scab development and second-
ary contamination by conidia (Olcott-Reid et al. 1981).
Irrigation under foliage is strongly preferred nowadays.
Actions on the inoculum or on the pathogen dispersal en-
able good control of the apple scab infection. It has been
shown that sanitation practices such as leaf litter removal con-
siderably reduce the number of fruit scab lesions at harvest
(approximately 70%) (Gomez et al. 2007), conversely de-
creasing the food stock for the soil detritus cycle (Zanotelli
et al. 2015). Didelot et al. (2007) showed that within-row
mixtures of resistant and susceptible cultivars were effective
in controlling apple scab because they reduced auto-infection,
which is important in the apple tree. Autoinfection is defined
as infection caused by a propagule within the same genotype
unit. In the case of a within-row mixture, the transmission of
apple scab conidia from one tree of a susceptible cultivar to
another tree of the same cultivar was limited, on the one hand,
by the barrier effect due to the presence of a resistant tree
between both and, on the other hand, by the fact that the
distance between both was large in relation to the spatial ex-
tent of propagule dispersion.
According to these examples, plant and insect biodiversity
–as well as agricultural management, which does not neces-
sarily directly target pests but acts via the tree or environmen-
tal conditions –enhance ecological pest control. Even though
the ‘common’strategy still relies on pesticides, fruit growers
are becoming aware of these ecological strategies that can be
combined in order to optimize pest regulation for low envi-
ronmental impacts and efficient protection. They constitute an
essential element of Integrated Pest Management or IPM
(Barzman et al. 2015) that is now mandatory for all crops in
the EU member states (European Parliament 2009).
Various indicators of pest and disease control have been
proposed in the literature, including in studies of multiple
agroecosystem services. Syswerda and Robertson (2014)have
used plant diversity to indicate the delivery of biological con-
trol and, more generally, arthropod habitat and other conser-
vation benefits. It actually seems that they dealt with plant
diversity as a proxy to habitat provision, as in Tsonkova
et al. (2014). Schipanski et al. (2014) used lepidopteran and
carabid activities as proxies for pest suppression and benefi-
cial insect conservation, respectively. These indicators are fair-
ly distant from the service in question. The same comment
applies to the abundance or diversity of natural enemies that
has also been used. The enhanced populations of natural ene-
mies in crops provide no guarantee for effective pest control,
according to the review of Bianchi et al. (2006). Many studies
dealing with insect pest suppression by natural enemies in
orchards have considered rates of predation by natural ene-
mies (e.g., Boreau de Roincé et al. 2013; Monteiro et al. 2013;
Table 1), rates of parasitism by parasitoids (e.g., Maalouly
et al. 2013; Maalouly et al. 2015; Table 1) or rates of parasit-
ism that combine the two processes (e.g., Dib et al. 2010).
However, pest suppression is not pest control and there is a
need to fill the gap between natural pest control, crop damage
and crop yield (Schellhorn et al. 2015). In addition, the above-
mentioned indicators of pest suppression are less suitable for
diseases than for animal pests, and they only deal with top-
down effects, excluding bottom-up regulation forces. We pro-
pose to alternatively consider fruit, shoot or leaf injury with a
degree of cumulative injury severity at harvest (Table 1). This
type of indicator can be easily linked to damage at harvest and
is commonly used in orchards. It should be noted, however,
that in practice, the degree of injury severity may depend not
only on the ability of orchards to ecologically control pests
and diseases, but also on the action of pesticides. Decoupling
these effects is possible experimentally or by modeling, and
12 Page 12 of 21 Agron. Sustain. Dev. (2017) 37:12
even in observational studies provided that additional indica-
tors such as the level of pesticide use are available. In addition,
indicators of the environmental impact of pesticides are nec-
essary. Specific pesticide indicators or ecotoxicological
models have been proposed for this purpose (Gutsche and
Rossberg 1997; Bockstaller et al. 2008; Table 1).
2.2.5 Life cycle maintenance: Pollination
Pollination, the value of which has been estimated at €153
billion (Gallai et al. 2009), is an essential driving force of crop
production. This general statement applies to fruit crops, even
though pollination may sometimes be negatively perceived by
some stakeholders. This is the case of growers of citrus fruit
(particularly tangerine and mandarin orange) in which seeds
develop in the case of cross-pollination, whereas seedlessness
is an important quality characteristic of these fruits (Sykes
2008;Sagoff2011).
Many fruit varieties are not self-pollinating. Insect pollina-
tion services are provided both by wild, free-living organisms
(chiefly bees, but also many butterflies, moths, flies, beetles
and wasps), and by commercially managed bee species (pri-
marily the honey bee, Apis mellifera) (Kremen et al. 2007). A
minimum of four or five strong colonies per hectare is recom-
mended during the bloom period in mature apple orchards
(Dennis 2003). A greater species richness of pollinators may
favor fruit set, and apple growers could economically benefit
from relying on wild bees for pollination. For example, Osmia
cornuta, an alternative pollinator, has a greater tolerance to
inclement weather and a higher rate of stigma contact than
Apis mellifera in fruit crops (Ladurner et al. 2004).
In orchards, the positive effects of cover crop and hedge-
row species richness on the rate of pollination have been dem-
onstrated (Miñarro and Prida 2013; Nicholls and Altieri 2013;
Rosa García and Miñarro 2014). This is in accordance with
the fact that most pollinator species depend on several floral
resources (Miñarro and Prida 2013). The spatial organization
of orchards in the landscape in relation to natural habitat is
also important since it has been shown that fields situated
1.5 km away from natural habitat patches can be expected to
contain only 50% of the pollinator diversity of the fields clos-
est to these patches (Ricketts et al. 2008).
Pesticides may impair bee colonies, especially honeybees,
in terms of learning performance, behavior and neurophysiol-
ogy, thus decreasing pollination (Thompson 2003;Desneux
et al. 2007). In addition to pesticides, hail nets, which are very
common in orchards, may also influence pollination through
the decrease in bee colony weight, which is due, in the first
place, to forager deaths in the nets and, as a consequence, to
swarm death (Vaissière et al. 2000). There is obvious antago-
nism between pollination and pest regulation through pesti-
cides and exclosure nets, which could be overcome by relying
more on biological pest control, as seen in Section 2.2.4.
Indicators of pollination (Table 1) are still in debate
(Vaissière, pers. comm.). Similarly to the case of pest and
disease control, the pollination value of an agroecosystem
can be related to plant diversity. On these bases, Ricou et al.
(2014) proposed a vegetation-based indicator of the pollina-
tion value of field margin flora using floral traits. The abun-
dance and diversity of pollinators, i.e., of the “service pro-
viders”, have also largely been highlighted (e.g., Nicholls
and Altieri 2013). Although they are not direct indicators of
pollination, all these proxies are useful with respect to polli-
nation in the orchard in general, but as far as the fruit trees are
concerned, direct indicators that can be measured or modeled
could be mobilized. Fruit set and the number of seeds per fruit
(for multi-seeded fruits) are common indicators of the efficacy
of pollination in orchards (Volz et al. 1996; Stern et al. 2001;
Garratt et al. 2014). However, fruit set should be considered
with caution and not alone, because pollination is not the only
determinant of fruit set.
3 Assessing and analyzing multiple ecosystem
services in orchards
There are few studies on the assessment of multiple ecosystem
services in agroecosystems (Antle and Capalbo 2002;Heal
and Small 2002; Lescourret et al. 2015). In the following
paragraphs, we propose a two-fold approach to multiple eco-
system service analysis in orchards: using models to quantify
indicators of ecosystem services, and exploring their mutual
relations.
3.1 Using models to quantify indicators of ecosystem
services and their connections
As stated above, the relationships between agricultural man-
agement, ecosystem functions and ecosystem services present
a high degree of complexity. That is why using models can be
of great assistance to analyze these relationships. Models can
provide a direct quantification of ecosystem service indicators
such as those proposed in Section 2, or of indicators of eco-
system functions at a given space and time scale. In addition,
they make simulation of changes in ecosystem service profiles
and relationships possible according to a large panel of fictive
scenarios.There are growing numbers of model-based ecosys-
tem service simulation studies. Thus, Kragt and Robertson
(2014) analyzed the impact of various agricultural practices
on ecosystem services of farm systems in a maize belt in
Western Australia with APSIM, a model that stimulates bio-
physical processes in a crop-pasture system (Keating et al.
2003). They showed that increasing crop residue retention
can jointly increase production value and improve soil carbon
and nitrogen supply. Conversely, increasing the use of peren-
nial pastures in the farming mix creates trade-offs between
Agron. Sustain. Dev. (2017) 37:12 Page 13 of 21 12
production values and non-marketed ecosystem services.
Another example is the simulation study of Tsonkova et al.
(2014) using a model called the ‘Ecosystem Services
Assessment Tool for Agroforestry’(ESAT-A), which was de-
signed to compare ecosystem service provision in different
agroforestry management situations. According to this simu-
lation study, the provision of habitat, soil fertility, water qual-
ity and regulation, and erosion control were greater for alley
cropping systems than for conventional agroforestry systems,
and within alley cropping systems, the more that poplar tree
proportions increased, the higher the provision of ecosystem
services was.
STICS, a widely used dynamic model that simulates the
soil-crop interactions at a daily time step (Brisson et al. 1998;
Brisson et al. 2009), could be a good candidate to represent
agricultural production, climate regulation, soil fertility and
water cycle regulation in response to agricultural management
and pedoclimatic conditions in a unified framework. The main
simulated ecosystem processes are crop growth and develop-
ment, as well as the water and nitrogen balance of the soil-crop
system. This model has already been used for ecosystem ser-
vice analysis. Tribouillois et al. (2016) used STICS to analyze
the effect of cover crops and green manuring on leaching and
nitrogen fixation, respectively, and then on soil nitrogen avail-
ability. The generic character of STICS enables a parameteri-
zation of the model to many crops. It has already been param-
eterized on perennial crops such as grapevine (Vitis vinifera)
(Garcia de Cortazar Atauri 2006) and silvergrass
(Miscanthus × Giganteus) (Strullu et al. 2014). However,
STICS does not address the question of pests and diseases
and their control, and it is necessary to supplement the model
or to couple it with pest models to address the set of ecosystem
services in Fig. 3.
3.2 Analyzing multiple ecosystem service relationships
Ecosystem service relationships are very complex and often
non-linear (Lescourret et al. 2015; Rapidel et al. 2015). They
are commonly classified as synergies (positive relationships)
and trade-offs, also referred to as conflicts (negative relation-
ships). Trade-offs occur when the provision of one ecosystem
service is reduced at the expense of another (Rodríguez et al.
2006). Relationships between ecosystem services may be ex-
plained by highlighting underlying ecosystem functions and/
or the role of management drivers. Positive ecosystem service
relationships may occur whena similar management lever acts
on different functions that underpin the services (Bennett et al.
2009). Thus, pest and disease control and soil fertility are not
functionally related to each other, but they may respond sim-
ilarly to groundcover management. Adding organic material
to the ground habitat of an apple orchard significantly affects
arthropod abundance, leading to more predators and fewer
herbivores (Brown and Tworkoski 2004). The physical
qualities of mulch can affect apple aphid migration
(Damavandian 2000). At the same time, nutrient release from
the decomposition of this organic matter can enhance soil
quality by increasing soil carbon, nitrogen and microbial bio-
mass (Teravest et al. 2011).
In agroecosystems, agricultural production and regulating
services are often in conflict. A conflict may occur when there
is a common function, and the challenge is to find a manage-
ment solution able to mitigate the conflict. For example, in
vineyards, intercropping may mitigate runoff but decrease
grapevine productivity in the event of competition between
intercrops and the grapevine for resources. A simulation study
using the VERDI model (Ripoche et al. 2011) suggested that,
under irregular rainfall distribution, flexible intercropping
management in vineyards can help overcome this trade-off.
This flexible management consisted in maintaining cover
crops with mowing and possibly destroying them when the
available soil water in the field was lower than a reference
value. Similarly, Guilpart (2014) studied the link between
grapevine yield and regulation of fungal diseases through wa-
ter stress at flowering. He has shown that decreasing vegeta-
tive growth (the common function) could enhance powdery
mildew regulation but, at the same time, decrease yield.
However, most of the year n yield is determined by year n-1
conditions, whereas grapevine vegetative development de-
pends only on year n conditions. On this basis, he used sim-
ulation to show that when specific climatic sequences occur (a
wet year followed by a dry year), applying water stress during
flowering could reduce vegetative growth without impacting
yield, leading to win-win scenarios.
It may be difficult to identify a management lever able to
mitigate the conflict between a provisioning and a
functionally-linked regulating service in the case of multi-
lever management acting on various functions, which is a very
common situation. For example, Grechi et al. (2012) com-
pared crop management strategies using a model of the
peach-aphid pathosystem in which, on the one hand, insecti-
cides kill aphids and, on the other, pruning or nitrogen supply
impacts the architecture, growth and quality of vegetative or-
gans and, consequently, yield, fruit quality and pest control by
acting on aphid dynamics. The effect of insecticides on aphid
mortality was evidently predominant, thus obscuring the po-
tential effect of the other cultural methods on the relationship
between provisioning and regulating services.
The analysis of two-sided relationships between ecosystem
services with a small number of common functions and
drivers is obviously limited. Comparing multiple ecosystem
service provisioning across different types of agroecosystems
generates global information on the way specific crop systems
contribute to given profiles of ecosystem services. Syswerda
and Robertson (2014) adopted this approach using data of
long-term experiments in different cropping systems (annual
grain and perennial plants such as alfalfa and hybrid poplar
12 Page 14 of 21 Agron. Sustain. Dev. (2017) 37:12
trees). They observed that perennial systems made a greater
contribution to soil water storage and drainage than annual
grains, except for no-till systems, which equally contributed
to the provision of these two ecosystem services without los-
ing yield. Within perennial systems, poplar seemed to deliver
higher plant species richness than deciduous forests. Among
grain systems, biologically-based systems delivered the
highest number of ecosystem services in a favorable way,
which is in accordance with the findings of Sandhu et al.
(2008,2010). Early successional systems were generally fa-
vorable to greenhouse gas emission mitigation, while poplar
systems presented high provisioning of plant diversity, soil
organic matter and nitrate conservation. Significant correla-
tions between several ecosystem services were identified.
The most significant positive correlation occurred between
drainage and nitrate leaching, and the most negative one was
between global warming impact and plant species richness.
4Conclusions
This review demonstrates that orchards represent relevant sit-
uations for studies on ecosystem service trade-offs and syner-
gies. Agricultural practices in orchards have a strong impact
on several ecosystem functions and, consequently, on ecosys-
tem service relationships. Groundcover management may in-
crease biotic interactions by offering a habitat to natural ene-
mies or repelling crop pests, but it can also avoid runoff and
leaching while increasing soil drainage. Pruning may increase
fruit production but may favor some pests such as apple
aphids as well. Pesticide use remains the most effective pest
control method, but its negative impact on ecosystem services
such as pollination jeopardizes the sustainability of orchard
systems. Irrigation and nitrogen fertilization certainly allow
increased fruit production, but they might impact non-
marketed ecosystem services since they have a direct effect
on functions like leaching and denitrification.
It should be noted that knowledge gaps that could hamper
studies of ecosystem service relationships in orchards exist.
Ecosystem services linked to the soil compartment have been
studied in annual crop systems, but they remain poorly docu-
mented in orchards, in spite of notable exceptions (Montanaro
et al. 2017). Measurements on orchards are quite scarce or
dispersed, particularly for carbon storage in tree organs and
in soil, carbon loss in the atmosphere via respiration rates and
CO
2
emissions from engines and crop protection products.
In addition, this review did not consider the entire range of
ecosystem services and focused on the plot scale. The inter-
ested readers can refer to Montanaro et al. (2017) on the main-
tenance of soil structure and absorption of pollutants in or-
chards. Cultural services were not considered and are difficult
to qualify, but they should not be neglected because fruit trees
have esthetic and cultural values (Baumgärtner and Bieri
2006; Montanaro et al. 2017). Cultural services seem to be
the poor cousin of ecosystem service assessments (Fagerholm
et al. 2016). We have addressed habitat provision, which is
important for biodiversity conservation with respect to pest
enemies, but this issue may be addressed more globally and
at the landscape scale. For instance, it has been shown that
modifying the landscape structure by planting fruit trees may
enhance the connectivity in various taxa (Baumgärtner and
Bieri 2006).
Model-based simulations of a large range of cropping sys-
tems provide the foundation for analyzing ecosystem service
trade-offs and synergies and for finding the desired combina-
tions of ecosystem services (Rapidel et al. 2015) using multi-
objective optimization (Memmah et al. 2015; Ould-Sidi and
Lescourret 2011). However, models that consider multiple
ecosystem service provision are lacking in the case of or-
chards. Fruit tree models and fruit tree pest-predator models
were designed and used to analyze the effect of cropping sys-
tems (Grechi et al. 2012;Lescourretetal.1999;Lescourret
et al. 2010), but they ignored the soil compartment and
addressed a limited range of ecosystem services. Therefore,
developing more sophisticated orchard models that address
multiple ecosystem services and take the impact of soil,
climate and agricultural management into account is still a
challenge. A similar comment was made by Fagerholm et al.
(2016) for agroforestry systems.
The analysis of relationships between agricultural practices
and multiple ecosystem services can be useful for the design
of innovative orchard systems that optimize the provision of
multiple ecosystem services for a large panel of stakeholders.
This design will of course require a strong stakeholder in-
volvement (Fagerholm et al. 2016) and imply new social in-
teractions to balance conflicting objectives. Different stake-
holders may have different perceptions of services, as exem-
plified by the case reported about pollination by Sagoff (2011)
of apiarists and orange growers, the latter being alarmed by
the risks of cross-pollination of oranges by bees. New con-
tracts between social groups have to be established at the
regional or local scale. For example, in Baden-Württemberg
in Germany, the regional government and non-governmental
organizations establish contracts with landowners that deter-
mine ways to manage fruit tree meadows in order to qualify
for the right to market produce under a specific quality label
that generates extra revenue (Thiel et al. 2012). Finally, the
collective dimension of multi-service management in areas
that include a high density of orchards is a new challenge that
opens up new research avenues requiring the cooperation of
the ecological and social sciences (Lescourret et al. 2015).
Acknowledgements This study was funded by an industrial training
agreement through a CIFRE research fellowship from the CTIFL
(Centre Technique Interprofessionnel des Fruits et Légumes) and the
Agron. Sustain. Dev. (2017) 37:12 Page 15 of 21 12
ANRT (Association Nationale de la Recherche et de la Technologie) on
behalf of the French Ministry of Higher Education and Research.
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