Ecological Indicators: Hossein Kazemi, Hermann Klug, Behnam Kamkar T

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Ecological Indicators 93 (2018) 1126–1135

Contents lists available at ScienceDirect

Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Review

New services and roles of biodiversity in modern agroecosystems: A review T


a,⁎ b a
Hossein Kazemi , Hermann Klug , Behnam Kamkar
a
Department of Agronomy, Faculty of Plant Production, Gorgan University of Agricultural Sciences and Natural Resources (GUASNR), PO Box 49189-43464, Gorgan,
Iran
b
Paris-Lodron University of Salzburg (PLUS), Interfaculty Department of Geoinformatics – Z_GIS, Schillerstr. 30, Building 15, 3rd Floor, 5020 Salzburg, Austria

A R T I C LE I N FO A B S T R A C T

Keywords: Ecosystem services and biodiversity are critical to ensure sustainable development of agricultural activities.
Agrobiodiversity Based on available scientific knowledge, high shares of biodiversity are followed by more carbon sequestration,
Agroecosystems reduced soil erosion risk, improved production and food security. This review aims to detect biodiversity services
Biodiversity review in three aspects; (1) providing ecosystem services in modern agroecosystems in response to future challenges, (2)
Climate change
the ability of biodiversity to support agroecosystems, and (3) the agenda for future research on biodiversity. To
Food security
address our research objectives, we conducted a widespread literature search to estimate new services and roles
Sustainable agriculture
of biodiversity in modern agroecosystems. The search was set from the date of the first relevant article until the
end of the year 2017. Biodiversity is measured by many indices. Many recent studies have proposed new
methods and software for biodiversity assessment such as BioFTF, BAT, LaDy and Entropart. According to the
present literature review, biodiversity has a pervasive role in climate change adaptation and mitigation stra-
tegies. Levels of biodiversity, such as genetic, species and ecosystem, can affect pest control in several ways such
as biological control, resulting in complex multi-trophic interactions. The relationships between land use and
biodiversity are fundamental in understanding the links between people and their environment. Two models
have been planned to increase production in agroecosystems whilst minimizing the consequences for biodi-
versity: land sharing and land sparing. Studies have shown how biodiversity can be integrated into Life Cycle
Assessment (LCA) on a global scale. LCA mainly introduces biodiversity as an endpoint category modeled as a
loss in species richness due to the conversion and management of land in time and space. This review shows that
ecological restoration of agroecosystems is generally effective and can be recommended as a way to increase
biodiversity in agricultural ecosystems. The conservation, management, and sustainable use of these services
require specific attention and a coherent global policy approach. In conclusion, to protect biodiversity in
agroecosystems, a policy consonance and strategic support to ecosystems should be considered. This review
suggests that advanced research are needed on relationships between biodiversity and genetic erosion, map of
life, pest control and urban agriculture.

1. Introduction diversity stabilizes the ecological function and allows biogeochemical


systems (e.g. water cycle, flow of greenhouse gases, and carbon se-
Biodiversity is a vital property of ecological systems. It is generally questration), to work in a balanced manner. At the same time, biodi-
explained as a variety of all forms of life in terrestrial, marine, and other versity is directly linked to food production, provision of substances for
aquatic ecosystems (Overmarset al., 2014). Thus, investigations should medicines, and delivery of energy sources. Moreover, some species play
incorporate different levels of biodiversity at genetic, species, or eco- a fundamental role within the spiritual, cultural, and/or religious cer-
system level. This depends on principal observation objectives, eco- emonies. As a result, biodiversity is an irreplaceable good for society
system characteristics and general richness of elements in the eco- (Dirzo and Raven, 2003; Henzen, 2008; UNEP, 1999).
system (Moonen and Bàrberi, 2008). Each species, living within an This review aims to detect biodiversity services in agroecosystems
ecosystem, introduces processes and creates flows of energy, sub- and consider the potential benefits of biodiversity for improved
stances, and materials. Therefore, the disappearance of a single species agroecosystems functioning in the following three aspects:
can lead to irreversible changes and consequently change ecosystem
properties towards undesired directions (Dirzo and Raven, 2003). Life 1) the ability of biodiversity to support ecosystems as modern


Corresponding author.
E-mail addresses: [email protected] (H. Kazemi), [email protected] (H. Klug), [email protected] (B. Kamkar).

https://doi.org/10.1016/j.ecolind.2018.06.018
Received 15 March 2017; Received in revised form 4 June 2018; Accepted 7 June 2018
Available online 20 June 2018
1470-160X/ © 2018 Elsevier Ltd. All rights reserved.
H. Kazemi et al. Ecological Indicators 93 (2018) 1126–1135

Table 1
State of the art biodiversity including its services and roles.
State of the art biodiversity Description Service References
in …

Sustainable agriculture Sustainable agriculture seeks to support farmers’ resources and communities provisioning, supporting, OECD (2001), Schmidt and Wei
by promoting farming practices and methods that are profitable, cultural, supporting (2006)
environmental friendly, and beneficial for communities.
Agrobiodiversity Agrobiodiversity refers to the biodiversity of agroecosystems along with provisioning, supporting, Baudron and Giller (2014), Yao
species of crops and farm animals, the genetic variance within populations, and cultural, supporting and Li (2010)
respective varieties and races.
Urban agricultural (UA) Production of crop and livestock products within cities and towns is referred to provisioning, supporting, Zezza and Tasciotti (2010),
as urban agriculture (UA). cultural, regulating McLain et al. (2012), Lin et al.
(2015)
Pest control Cultural, mechanical, chemical, and biological controls are the most applied regulating, supporting Benbrook (2001), Philpott (2013)
options to overcome diseases and pest.
Food security and health Food security is generally referred to the availability and accessibility of food provisioning, supporting World Bank (1986), Maxwell and
for human. The World Bank defines food security as the access of food to all Wiebe (1999)
people for an active and healthy life at all times.
Carbon sequestration Carbon sequestration is the process involved in carbon capture and the long- provisioning, regulating, Hajjar et al. (2008), Batjes and
term storage of atmospheric carbon dioxide. supporting Sombroek (1997)

agroecosystems, urban agriculture, and sustainable agriculture Therefore, increasing agricultural production in the developing world
ecosystem; and minimizing adverse effects on biodiversity abundance should be
2) the role of biodiversity in providing ecosystem services such as food considered a priority for environment conservation (Baudron and
security, pest control, and ecological restoration, and its effect on Giller, 2014). McCauley (2006), Putz and Redford (2009), and Rands
climate change, land uses, genetic erosion, and carbon sequestra- et al. (2010) have expressed concerns that emphasizing on ecosystem
tion; services might be at the expense of biodiversity conservation, whereas
3) the agenda for future research on biodiversity. others have suggested that markets for ecosystem services would pro-
vide funding for conservation activities.
As a 10,000-year-old treasure in agricultural activities, biodiversity To plan a strategy protecting current biodiversity levels, under-
is the basis and foundation of ecosystem services, essentials to sustain standing the present biodiversity conditions are required. The con-
agriculture and human well-being. Thousands of years of human in- sequences and potential countermeasures from land management and
tervention have led to the current crop and livestock biodiversity. climate change on biodiversity need to be analyzed and the regions
Biodiversity and agriculture are strongly interrelated. While biodi- with priority action should be defined (Booth, 2012).
versity is critical for agriculture, sustainable use of biodiversity corre-
sponds to agricultural structure and function, and thus is an indicator 2. Methods
for farming practices. Indeed, biodiversity is considered as a vital
component of sustainable agriculture from food security, nutrition, and To address our research objectives, we conducted a widespread
livelihoods viewpoints (Schmidt and Wei, 2006). In addition, biodi- literature search to estimate new services and roles of biodiversity in
versity can be used in order to gain a better understanding of dynamics modern agroecosystems. To refine the pool of searched literature that
and resilience of shifting (slash and burn) cultivation systems (Blanco met our criteria, Scopus and Web of Science as two the world’s largest
et al., 2013). citation databases were used. Some papers were identified by in-
Higher carbon sequestration, lower erosion risk and higher pro- vestigative the bibliographies in the review papers and papers that cite
duction are the most important results of high biodiversity stocks these. The search was set from the date of the first relevant article until
(Bullocket al., 2007; Overmarset al., 2014). The biodiversity in agroe- the end of the year 2017. The following keywords were used at each
cosystems can be categorized as either planned or unplanned diversity. query: 1) agrobiodiversity, 2) sustainable agriculture, 3) urban agri-
Planned diversity includes the spatial and temporal arrangement of cultural, 4) pest control, 5) life cycle assessment, 6) carbon sequestra-
domestic plants and animals that farmers purposely include in their tion, 7) ecological restoration, 8) land-use influencing biodiversity, 9)
farming system, e.g. bio-control agents or plant-related nitrogen-fixing effects of climate change on biodiversity, 10) food security, 11) genetic
bacteria (Altieri, 1999; Power, 2013). Unplanned diversity (or asso- erosion, and 12) biodiversity measurement methods. The outcome of
ciated diversity) includes other associated remaining organisms after this review is presented in Results and Discussion sections.
transition of a system to agriculture from the surrounding landscape. A
variety of weeds, herbivores, predators, parasites, and microorganisms 3. Results
are predominantly found in any ecosystem, even a simplified one such
as an agroecosystems (Power, 2013). 3.1. State of the art biodiversity in agricultural systems
Recent studies revealed a global decline in biodiversity (Shoyama
and Yamagata 2014; Baudron and Giller, 2014). Threats and pressures Many key ecosystem services and roles are provided by biodiversity.
on biodiversity increased, during the last decade (Shoyama and They are shown in Tables 1 and 2. To understand of the art and role
Yamagata, 2014). Cropland area in the developed world decreased biodiversity in agriculture, it is necessary to study the status of biodi-
about 50% between 1961 and 1999 (Wik et al 2008; Baudron and versity services in agriculture systems or agrobiodiversity. Biodiversity
Giller, 2014). Globally, the total area of cropland increased by more is one of the basic principles sustainable agriculture, food security and
than 20% in the developing world and this trend is expected to continue health and it is one of the most important elements to manage the
until 2050 (Green et al., 2005; Balmford et al., 2005; Gibbs et al., 2010; systems toward a sustainable agroecosystems. Biodiversity provides
Baudron and Giller, 2014). The most biodiversity–rich areas on the different services in new agricultural systems such as urban agriculture.
earth are located in developing countries. Given the current level of Today, the most important challenges of modern agriculture include
information gained on the role of biodiversity, it is more crucial than pest control, CO2 emissions, and genetic erosion. All practices that in-
ever to reduce the contemporary level of resource degradations. crease diversity in agroecosystems and various time scales can improve

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H. Kazemi et al. Ecological Indicators 93 (2018) 1126–1135

Table 2
Services of biodiversity to ecosystem.
Relationship of biodiversity Description Service References
with …

Life Cycle Assessment (LCA) LCA is a systematical method to assess environmental impacts of products and/or regulating, supporting Baan et al. (2013), Souza et al.
services. It considers all inputs and outputs involved from the generation to the (2015)
waste of a product and/or service in respect to the environment.
Ecological restoration (ER) Ecological restoration is considered a major strategy to improve the provision of regulating, supporting Bullock et al. (2011)
ecosystem services and reversing biodiversity losses.
Land use Land use involves the management and modification of natural environment into regulating, supporting, Haines-Young (2009), Henzen
built environment such as settlements, arable fields, pastures, and managed woods. cultural (2008), Michelsen (2008)
Climate change Climate change is a change in the statistical distribution of weather patterns when regulating, supporting Sahney et al. (2010)
that change lasts for an extended period of time.
Genetic erosion The loss of genetic diversity is known as genetic erosion, which is commonly referred regulating, supporting Wolff (2004)
to as the reduction in the quantities of specimens of a species.

agroecosystems capability to pest control and sequester carbon. Eco- in the case of crops, is referred as landraces) (Amend,et al., 2008).
logical restoration of agroecosystems could be advised as an effective This FAO definition seems to be comprehensive and acceptable in
way to improve biodiversity in these ecosystems. In contrast, most land many scientific communities.
cover/land use changes can effect biodiversity and reduce related
ecosystem services. Also, the biodiversity could be integrated into LCA The status of agrobiodiversity varies in the world. For example,
at global scale, with regard to species richness of a natural reference Overmarset al. (2014) revealed that the state of the overall biodiversity
situation compared to different land use types. Based on available sci- in agriculture is better in the southern and eastern parts compared to
entific knowledge, these services and challenges were reviewed in this the western and northern part of the European Union (EU). They
section. adopted a species-oriented methodology enabling spatially explicit in-
dicator for biodiversity quantification on agricultural lands. The pro-
3.1.1. Agrobiodiversity vided map demonstrates great variety in the state of the biodiversity of
The term ‘agrobiodiversity’ was coined in the 1980s. According to agricultural areas in the EU.
UNCED (1992), it has evolved only in recent years in the wake of the When natural ecosystems are shifting towards agroecosystems,
general biodiversity discourse. Agrobiodiversity is the sub-set of general biodiversity is directly modified (via additions and removals of biota) or
biodiversity directly developed and managed by humans. Analogous to indirectly modified (via the alteration of biogeochemical cycles, hy-
the term biodiversity, agrobiodiversity encompasses different levels. It drological cycles and species habitats) targeted to increase yield for
refers to the biodiversity of agroecosystems along with species of crops human benefit. In turn, undergoing changes in biodiversity will change
and farm animals, and the genetic variance within populations, vari- ecosystem functions and processes via changes in species traits (Webb
eties and races. Soil organisms, insects, fungi, and wild species from off- et al., 2010; Baudron and Giller, 2014).
farm natural habitats as well as cultural and local knowledge on bio- The replacement of abundant species with gene pool poor high-yield
diversity form the basis of the exploitation of biodiversity (Baudron and plant species resulted in a decline of agrobiodiversity (Wolff, 2004).
Giller, 2014). Four principal components of agrobiodiversity exist: The decline in biodiversity is also associated with agricultural man-
agement practices, such as fertilization, irrigation, machinery-driven
1) genetic resources for food and agriculture; weed removal, and pesticide and fungicide applications (Wolff, 2004).
2) biodiversity that supports ecosystem services of agriculture; Furthermore, new high-performance breeds do not need to adapt to
3) abiotic factors, e.g., climate; and short term or long term environmental changes since all of their needs
4) socioeconomic and cultural dimensions (Zimmerer, 2014). are attempting to provide supplementary materials. This trend is sup-
ported through new breeding programs, focusing on increasing further
Agricultural expansion and intensification led to biodiversity loss in yield and production power towards top performers. Attempts focus on
agroecosystems (Tscharntke et al., 2012) and reduction in the types and artificial insemination, multiple ovulation and embryo transferring li-
levels of ecosystem services that people benefit from (Barral et al., vestock and genetically homogenous and high performing plant vari-
2015). Farmland biodiversity is a ground for provision of ecosystem eties. These efforts are expected to exclude a number of individuals
services needed to sustain agriculture per se and the environment as a from breeding programs. Consequently, the genetic distance within
whole (Overmars et al., 2014). According to Yao and Li (2010), agro- populations is expected to increase (Wetterich, 2001; Wolff, 2004).
biodiversity includes all crops and livestock, their wild relatives, and all
interacting and supporting species such as pollinators and symbiotic
agents, in relation with pests, parasites, predators and competitors. In 3.1.2. Biodiversity as a necessity in sustainable agriculture
the current definition, agrobiodiversity refers to a comprehensive Modern agricultural systems have adverse effects on environmental
concept emphasizing crops and livestock (i.e. those are involved in food aspects of production and ecosystem health. Loss of biodiversity due to
production process). The Food and Agriculture Organization (FAO) monoculture is one of these adverse consequences. Maximizing the
explains agrobiodiversity as the variety and variability of animals, yield of a limited number of plant and animal species, in the agri-
plants and micro-organisms that are crucial for food and agriculture, cultural business inevitably weaken and reduce competitiveness with
and which originate from the interaction between the environment, undesired species (OECD, 2001). It is irrefutable that biodiversity and
genetic resources and the management systems and those practices used agriculture are interrelated and could benefit. In contrast to modern
by people. In particular, it contains two categories: agricultural systems, sustainable agriculture enables us to produce food
without limiting future generations' ability to do so. Biodiversity is one
1) the wild relatives of domesticated species (for example, wild re- of the most important elements to manage the systems toward a nature
latives of crop species or species that are genetically usable breeding framework (Pretty, 2008). From ecological perspective, biodiversity is
materials); the basis of survival of the system and could be considered a vital
2) or breeding individuals of plants and domesticated animals (which component of sustainable farming systems.

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3.1.3. Services of biodiversity in urban agricultural (UA) systems conserve biodiversity and meliorate different ecosystem services. Yet,
Production of crop and livestock products within cities and towns is the relationships between biodiversity and biological control in agroe-
referred to as urban agriculture (UA) (Zezza and Tasciotti, 2010). This cosystems have not been settled and most of the mechanisms under-
incorporates the local urban socio-economic and ecological system (Lin lying these relationships remain unclear (Crowder and Jabbour, 2014).
et al., 2015).
Simplified green spaces and intensively developed ecosystems with 3.2. Biodiversity and carbon sequestration
low levels of native biodiversity in urban land use can enhance biodi-
versity and consequently provide functions and services across frag- Different factors such as alleviating soil degradation, agricultural
mented habitats (Lin and Fuller, 2013). These functions and services practices and desertification with conserving soil organic matter in the
e.g. include cultivating, processing, and distributing functions of food in surface layer could enhance the soil’s capability to sequester carbon
or around a village, town, or city within the scope of agroforestry, (Batjes and Sombroek, 1997). Slowing down the soil degradation pro-
aquaculture, beekeeping, and horticulture. In cities, particular biodi- cess and impeding desertification could lead to annual conservation of
versity services can provide services for storm water runoff, mitigation over 0.5–1.5 Pg C globally (Dixon et al., 1994). The practices leading to
of air pollution, contribution of carbon storage and sequestration, and considerable return of soil biomass and soil organic matter are causes of
delivery of improved water quality (McLain et al., 2012; Lin et al., enhanced carbon sequestration in agroecosystems. Thus, all practices
2015). that increase diversity at species and genetic level and various time
In urban agriculture, biodiversity has increasing adverse effects on scales, can improve agroecosystems capability to sequester carbon
some ecosystem functions. For example, particular plants and micro- (Hajjar et al., 2008). The positive relationship between biodiversity and
organism are considered weeds and pathogens respectively and po- carbon stocks has been confirmed with coincidence of variation with
tentially harm native ecosystems and interfere with ecosystem service biomass value and carbon content.
delivery from natural systems (Blitzer et al., 2012; Zhang et al., 2007; Terrestrial ecosystems can save about 2100 Gt carbon in living or-
Lin et al., 2015). ganisms, litter, and soil organic matter globally. This amount is esti-
mated to be three times as much carbon as stored in the atmosphere.
3.1.4. Pest control by biodiversity in agroecosystems For that reason, living organisms play an important role in climate
Agricultural intensification can be defined as an increase in agri- regulation. Carbon storage in ecosystems among other factors depends
cultural production per unit of inputs. Intensification is based on the on the species composition, available soil types, and climate change.
selection of special crops and crop varieties adapted to their spatio- Degradation of the entire (or part of) an ecosystem reduces its cap-
temporal environmental conditions. Thus, the loss of biodiversity has ability to sequester and store carbon. Thus, if the share of carbon
been exacerbated the pest control challenges in agroecosystems (Hill, capturing for climate mitigation is considered important, maintaining
1987). Cultural, mechanical, chemical, and biological controls are the carbon sources is required at global scale (European Commission,
most applied options to overcome pests. With the agricultural in- 2009).
tensification, use of pest biocontrol methods has diminished (Benbrook,
2001). Instead, chemical treatments and the use of genetically modified 3.3. Biodiversity in life cycle assessment (LCA)
organisms have been adopted to control or manage pests (Benbrook,
2001). Thus, natural system control has been shifted to human induced Two approaches are available for the evaluation of the effects of
control mechanisms. These changes increased environmental costs, agricultural activities on biodiversity. The first approach is indicator-
water and groundwater pollution, and higher biodiversity losses in based by landscape heterogeneity and landscape ecological structures,
agroecosystems (Bengtsson et al., 2005; Philpott, 2013). whereas the second shows how biodiversity can be included in LCAs
Natural enemies were considered elements to suppress pests or re- (Jeanneret et al., 2014). LCA is a systematical method to evaluate
duce the damage caused by them. Records from around 300 CE show product or service from environmental aspects (calculating cradle-to-
that Chinese farmers used ants and natural enemies in orange groves to grave environmental impacts). It considers all inputs and outputs in-
control mite populations (Huang and Yang, 1987). Traditional biolo- volved in the generation of a product or service with respect to the
gical control mechanisms were applied to reduce pests, decreased yield, surrounding environmental conditions. The biodiversity concept could
economic loss, and consequently human disasters. In the 1980s, 160 be integrated into LCA at global scale, with regard to species richness of
species of predatory arthropods and 16 insectivorous birds were re- a natural reference situation compared to different land use types (Baan
leased for pest control in the USA (Letourneau et al., 2009). So far, more et al., 2013). An alternative approach is to consider concepts of eco-
than 2000 species have been released worldwide (Philpott, 2013). system scarcity, vulnerability, and conditions in order to maintain
Among the modern agricultural systems, organic farming en- biodiversity in the specific case of forestry (Michelsen, 2008).
counters more variety of pests and insects than conventional agroeco- LCA is mainly considered an endpoint category, modeling the loss of
systems. Crowder et al. (2010, 2012) showed that organic farming species richness through spatial and temporal land use conversion. Real
systems may partly lead to increased richness while having significant dynamics and complexity of the interactions among species and their
positive influences on evenness and abundance in comparison to con- habitats have been taken to simplified land-use modeling approaches
ventional systems. Due to reduced insecticides application or improved (Souza et al., 2015). An expert system was developed by Jeanneret et al.
habitat biodiversity, the positive influences of organic farming systems (2014) to consider LCA impact categories in agricultural productions.
can be important on richness and abundance of organisms (Crowder The developed method is valid for grasslands, arable crops and semi-
and Jabbour, 2014; Bengtsson et al., 2005; Hole et al., 2005). natural habitats of the farming landscape and estimation of the impact
Principally, habitat heterogeneity can strongly benefit pest control of management systems on biodiversity. The use of eleven indicator-
services (Philpott, 2013). A high degree of habitat heterogeneity in species groups provided a differential and comparatively comprehen-
agricultural landscapes can increase the biodiversity of natural enemies sive assessment of the impacts of the agricultural operations on biodi-
in crop fields, and provides stability of resources form natural enemy versity.
populations (Altieri, 1999). This heterogeneity could attract natural
enemies to agroecosystems. To maximize human benefits of farming 3.4. Role of biodiversity in ecological restoration (ER)
systems, identification of species and an integrated consideration of
different aspects of communities such as evenness, and richness are Ecological restoration (ER) is considered a major strategy to im-
required (Crowder and Jabbour, 2014). Crop rotation and integrated prove the provision of ecosystem services and reversing biodiversity
crop-animal based systems are two known options to improve and losses (Bullock et al., 2011). Benayas et al. (2009) were using a meta-

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analysis of 89 restoration assessments revealed that ER led to an in- biodiversity and ecosystem services increased policy action manage-
crease of ecosystem services and biodiversity between 25 and 44%, ment strategies, e.g. through the European Common Agricultural Policy
respectively. on land (Schroter et al., 2005; Haines-Young, 2009). Biodiversity loss
The two strategies are generally implemented through either pas- related to land use and its change is related to nature conservation. This
sive or active restoration. Passive restoration implies the removal of driving force especially applies in developing countries, where the de-
degrading factors, while active restoration involves management ac- mand of natural resources and food are increasing. Therefore it is im-
tions (Morrison and Lindell, 2011) such as adding desired plant species portant to collect data on species richness according to different land
and improving the soil, which both drive secondary succession. How- use types, because land managements considered a human activity with
ever, passive restoration most frequently implicates secondary succes- an incisive impact on biodiversity along with severe influence on other
sion following dereliction of agricultural land in the areas previously environmental elements (Henzen, 2008). In this regard, Xu (1997)
used for crop or livestock farming. ER could be a solution to help re- concluded that the changes in agroecosystems are significantly related
verse global biodiversity losses for those areas, which are facing en- with the various forces related to changes in technology, economic and
vironmental degradation. Finally, a positive correlation could be es- biophysical conditions, and modifications in institutional and social
tablished between biodiversity recovery and ER recovery (Balvanera settings.
et al., 2006). All components affecting biodiversity such as species Land sparing and land sharing have been proposed as two incisive
distribution, species richness and functional groups could also influence models to increase agricultural production along with the alleviation of
on ER components such as erosion control, reforestation, usage of ge- impacts on biodiversity: Land sparing suffers from several restrictions
netically local native species, revegetation of disturbed areas and re- such as:
introduction of native species, which in turn, could link to several in-
digenous ecosystem processes, leading to enhanced provision of a. Yield enhancement may result in reduction of cultivated area.
ecosystem services (Bullock et al., 2007). b. Intensification impacts are more than exclusively the farmed land
Species richness is positively linked to the improvement of several intensively.
ecosystem processes, and related services such as nutrient cycle and c. Many farmers in developing countries do not have access to
biomass production (Balvanera et al., 2006; Bullock et al., 2007). ER of knowledge and income to perform intensive farming.
agroecosystems could be advised as an effective way to improve bio-
diversity in these ecosystems (Barral et al., 2015). Validity of land sharing is supported by many species dependent on
farmlands and habitats managed by humans (Baudron and Giller,
3.5. Land-use influencing biodiversity 2014).
As for land sparing, land sharing faces two main restrictions:
Although land use activities have positive effects on biodiversity of
a region in many cases, land use might also lead to decreasing species (1) The impact of land sharing on biodiversity is often equivocal, and
abundance (Henzen, 2008). The interrelationship between land use and (2) Land sharing generally results in low agricultural yields and may
biodiversity is vital to apperceive the links between people and sur- consequently need more space than intensive farming; or it may
rounding environment (Haines-Young, 2009). even hasten land conversion in ecosystems with higher biodiversity
The biodiversity concept along with the overall richness of species, value (Baudron and Giller, 2014). Low input farming and little or
present in a particular area, covers the diversity of genotypes, func- no agro-chemical application rate also follow land sharing. Ob-
tional groups, communities, habitats and ecosystems. Consequently, tained yield resulted from such practices is generally less than those
there is a complex relationship between biodiversity and land use attained by intensive farming (Connor, 2008; dePonti and Rijk van
(Zeller et al., 2017). These dual relationships are often bilateral and Ittersum, 2012; Baudron, and Giller, 2014).
thus identification and justification of cause and effect relationships are
difficult. In some places, land use plans or land management activities Far from being opposing approaches, land sparing and land sharing
may be crucial for sustaining specific patterns of biodiversity such as should be regarded as different solutions to the same problem (Fischer
urban forest and urban agriculture (Haines-Young, 2009). et al., 2008). Many researchers believe that both approaches are equally
To attain a systemic and systematic conservation plan, assessments important and complement each other in different situations
of lands impact are required (Desmet and Cowling, 2004; Jost, 2009). (Cunningham et al., 2013; Baudron, and Giller, 2014).
These are for example carried out by quantifying and modeling land-
use–biodiversity relationships using species diversity (Alkemade et al., 3.6. Biodiversity for food security and health
2009; Hackman, 2015). The measurement of biodiversity at landscape
scale is performed by assessing species communities in different land- Food security is generally referred to the availability and accessi-
use types. The suitability of land-use systems to conserve the regional bility of food to society. The World Bank defines this phrase as the
species of interest can be used in order to differentiate them. However, access of food to all people for an active and healthy life at all times
the use of different biodiversity measures often leads to ambiguous (World Bank, 1986; Maxwell and Wiebe, 1999). The most commonly
results among scientists and planners (Hackman, 2015). accepted and used definition for it has been coined at the World Food
Several studies have been published methods for the evaluation of Summit; food security exists when all people, at all times, have physical
land use effects on biodiversity. For example, Koellner (2001) devel- and economic access to meet their dietary needs and food preferences
oped methods for the assessment of vascular plant species in relation to for a healthy and active life (Pinstrup-Andersen 2009; Sunderland,
distinct land uses in the region of Central Europe, Denmark, and Ma- 2011).
laysia. Hackman (2015) used a power model and a logarithmic model to Nutrient deficiency is constraint by a large group of the world po-
assess land-use impacts on biodiversity across a landscape and found pulation, especially those living in South Asia and Sub-Saharan Africa.
that the logarithmic model was working better compared to the power This deficiency occurs in spite of receiving sufficient calories, but in-
model when assessing biodiversity in large areas. Thus, when modeling sufficient intake of vitamins and minerals. The positive role of con-
biodiversity, not only the recognition of the appropriate space and time sumption of fruit and vegetables has been widely accepted to reduce
scale but also the overall concept considered is important. nutrient deficiency. Cereals, non-cereal grains, pulses, roots and tuber
Land cover, land use, and biodiversity are interdependent. Any land crops, fruit, various edible seeds, and vegetables are high potential
cover/land use change can effect biodiversity and reduce related eco- crops to provide food security at local and regional levels (Chadha
system services. Besides climate change, these pressures on the et al., 2007). Moreover, some crops with high nutritive value are

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gradually disappearing and are being replaced by high-yielding crops Climate change effects on some agricultural management. For ex-
(Adoukonou-Sagbadja et al., 2006; Kahane, et al., 2015). By 2050, ample, food provision for the people in each given region with poor
agriculture should provide food for almost 9 billion people (Kahane biodiversity resources is one of major challenges in modern agroeco-
et al., 2015). This requires an increase about 60 percent of global food systems. What is the priority action needed? The response to this
production. The World Health Organization (WHO) (2008) reported question will help society to manage the implementation of existing
that over 1.62 billion people (including 600 million children) are suf- plans and developing upcoming plans (Booth, 2012). Walker and
fering from anemia, along with serious deficiencies in essential minerals Schulze (2008) suggested that long-term outlooks in regard to ecolo-
and micronutrients in over a half of them. gical integrity and human well-being need to be applied to practices
Food production is highly dependent on biodiversity and services and policies for sustainability of both commercial and small agroeco-
provided by ecosystems. Although the amount of food supplied by systems.
current agricultural activities is sufficient at global scale, the extent of Biodiversity could be indirectly affected by climate change resulting
practices undermines the capacity of agroecosystems to preserve bio- from clearing land for farming. For example, the share of deforestation
diversity. However, the interdependence of biodiversity and agri- in respect to global CO2 emissions is about 12%. Unfortunately, loss of
culture, and their mutual role to maintain one another have been carbon is followed by loss of the habitats typically with rich diversity
highlighted in literature (e.g. Chappell and La Valle, 2011). Land con- and endemism (West et al., 2013). Liu et al. (2013) estimated biomass,
version and biodiversity have often been considered as two distinct soil quantity and ecosystem organic carbon stocks in four vegetation
subjects in agriculture. In order to provide forth-coming population types typical of Karst ecosystems in south western China, included
with food security, innovative and feasible ways should be sought to shrub grasslands (SG), thorn shrubbery (TS), forest – shrub transition
integrate biodiversity conservation and food production (Sunderland, (FS) and secondary forest (F). The results showed that organic carbon
2011). Maintaining diversity within agroecosystems is not a novel ap- storage of F is higher than the other mentioned ecosystems.
proach, but being performed by many smallholders in many different Based on the prediction proposed by the Intergovernmental (IPCC,
ways throughout the world is unique. The nutritional and livelihood 2014) for 2100, and assuming that the current trends in burning fossil
benefits of diverse production systems are one way to attain food se- fuels will continue as it is, earth surface temperature will increase about
curity. Such systems are also more resilient to climate-induced events or 1.4–5.8 °C. It is impossible to predict how and which species and eco-
other disasters (Kahane et al., 2015). With respect to challenges of food system will be affected by global warming. It is predicted that by 2050
security, richer biodiversity within agricultural systems is increasingly at least one quarter of all the species on land will become extinct as a
recognized as an important element to contribute to sustainable de- consequence of the extreme warming per se. This in turn will results in
velopment ( FAO, 2011). habitats life degradation and cause serious threats. This is especially the
case for those species living in temperature sensitive ecosystems (IPCC,
3.7. Effects of climate change on biodiversity and species response 2014).

Environmental conditions play a crucial role to explain the function 3.8. Genetic erosion and value of plant genetic resources
and distribution of plants in space and time. Climate change is a change
in the statistical distribution of weather patterns when that change lasts The loss of genetic diversity is known as genetic erosion, which is
for an extended period of time. Changes in long-term environmental commonly referred to as the reduction in the quantities of specimens of
conditions lead to considerable impacts on plant diversity patterns a species (Wolff, 2004). For agricultural crops, however, genetic erosion
(Sahney et al., 2010). Changing climatic variables like elevating CO2 is not limited to the reduction in the number of plants of a species or in
concentrations, heat stress, longer drought periods and heavy rainfall the geographic niche of a given species. The loss of genetic variation
events impact functions and the distribution of plants; moreover, among the plants, or specifically the loss of some of the various forms of
changes in the pattern of ‘extreme’ weather events can collectively af- genes are the main source of the variation in appearance and in the life
fect these function and distributions (Watson et al., 2012). cycles of plants (Friis-Hansen, 1999). The term genetic erosion is
Climate change is able to reduce genetic diversity due to directional sometimes used in a narrow sense such as for the loss of alleles or genes,
selection and rapid migration, which could in turn affect ecosystem as well as more broadly, referring to the loss of varieties or even species
functioning and resilience (Botkinet al., 2007). Species can respond to (Schmidt and Wei, 2006).
climate change challenges by shifting their climatic niche along three Nowadays, we are dealing with two important concerns in respect to
non-exclusive axes: space (e.g. range), time (e.g. phenology), and biodiversity in agroecosystems. In addition to replacement of diverse
themselves (e.g. physiology). The response of some species to climate landraces with few or one modern variety, the loss of indigenous
change may constitute an indirect impact on the species that depend on knowledge by farmers to manage their own genetic resources is also
them (Bellard et al., 2012). Climate change has led to phenological considerable (Friis-Hansen, 1999). Directing to less genetically diverse
shifts in flowering plants and insect pollinators, causing mismatches populations leads to more pathogen susceptible ecosystems and other
between plant and pollinator populations that lead to the extinctions of environmental limiting and reducing factors. The varieties involved in
both the plant and the pollinator with expected consequences on the modern agricultural systems may be less competitive than invasive
structure of plant–pollinator networks (Kierset al., 2010). At a higher plants. Overall, genetic erosion can have cascading effects throughout
level of biodiversity, the climate can induce changes in vegetation the ecosystem (Sunderland, 2011).
communities and affect biome integrity. Because of climate changes, In the process of determining the value of genetic resources (which
species may no longer be adapted to the set of environmental conditions are valued by their benefits), both the conservation of particular genes
in a given region and could fall outside its climatic niche (Bellard et al., or genotypes, and the conservation of biodiversity should be taken into
2012). account. Their benefits include resistance to biotic and abiotic stressors
Changing the distribution, phenology and abundance of species lead such as pests, diseases, drought, salinity, and plant stature. Additionally
to inevitable changes in the relative abundance of species and related they positively influence productivity and quality factors such as higher
interactions. These changes are expected to affect the structural, pro- oil or protein content besides culinary and cultural importance. Based
cess-related and functional aspects of ecosystems (Walther et al., 2002). on Schmidt and Wei (2006), global environmental change and more
Species that may no longer be adapted to climate change may expel intensified agroecosystems lead to genetic erosion, especially in Vavilov
from their climatic niche. To protect species as individuals, populations, centers.
or species, they must be equipped with adaptive responses in different The FAO (2010) estimates that about 75% of the genetic diversity of
ways (Bellard et al., 2012). agricultural crops has been degraded during the last century. A US

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survey carried out by the Rural Advancement Fund International (RAFI) tool is a scalar measure that reflects the information provided by the
found that in 75 crop species, 97% of the varieties listed in the old biodiversity profile and allows for ordering communities with different
United States Department of Agriculture catalogues are extinct (Fowler richness. In another study, Cardoso et al. (2015) developed a new tool
and Mooney, 1990). Europe is also vulnerable to loss of biodiversity. (BAT – Biodiversity Assessment Tool), i.e. an R package for the mea-
About 90% of the historical biodiversity of crops in Germany and 75% surement and the estimation of alpha and beta biodiversity in their
of crop varieties in Southern Italy have been lost (Hammer et al., 2002). multiple facets (taxon, phylogenetic and functional). This tool performs
Another example referred to rice crop in Sri Lanka, where 75% of many analyses, based on either species identities or trees, depicting
grown rice varieties are descended from one maternal parent, along species relationships. Using this approach, functions include building
with 62% in Bangladesh, and 74% in Indonesia (Amend et al., 2008). randomized accumulation curves for alpha and beta diversity, alpha
The identity of about 250,000 out of 500,000 species of higher diversity estimation from incomplete samples and the partitioning of
plants in the world have been recognized or designated. Approximately beta diversity in its replacement and richness difference components.
30,000 of these identified species are edible and approx. 7000 have The analysis of interactions between biodiversity and environ-
historically been used as crops or gathered by humans for food. Today, mental characteristics are crucial. Di Battista et al. (2016) applied
only 30 crops have a 95% share of the world's calorie and protein de- functional data analysis to the beta diversity profile for the analysis of
mands. On one hand, wheat, rice and maize alone provide more than the relationship between qualitative variables and a functional re-
half the global plant derived energy intake (FAO, 1991, 1996). sponse. Since the diversity profile is a function of the relative abun-
On the other hand, seven crops (sorghum, millet, potatoes, sweet dance vector in a fixed domain, this method could be helpful to monitor
potatoes, soybeans, sugar cane and sugar beet) provide half of the en- or to identify areas of high environmental risk. Moreover, the proposed
ergy intake at global scale. In spite of the fact that the number of plant approach allows overcoming the limitations of the classical biodiversity
species, which provide the world’s energy and protein, is limited, the indices.
biodiversity within such species is considerable; e.g. more than 100,000 Ricotta et al. (2003) described the computer program “LaDy”
distinct varieties of rice (Friis-Hansen, 1999; Ezcurra et al., 2001; (Landscape Diversity Software), for computing Rényi’s local landscape
Schmidt and Wei, 2006). Gao (2003) reports that increase in Chinese diversity profile on raster land cover maps. LaDy software is based on
population and particularly the rapid growth of market economy since the use of Merchant’s adaptive geographic window, which is designed
the 1980s caused turning the localities of wild rice into cultivated rice to operate on a neighborhood of patches instead of a fixed rectangular
fields, fish ponds, residences, factories, and highways. Therefore, with neighborhood of pixels.
the drastic change in habitats, the existence of wild rice has been ser- Entropart is an R package designed to estimate diversity based on
iously threatened, with most of the populations having disappeared or HCDT entropy (Tsallis entropy) or similarity-based entropy developed
being endangered. by Marcon and Hérault (2015). It allows calculating species-neutral,
Biodiversity, both in terms of growing a number of different crops phylogenetic and functional entropy and diversity, partitioning them
and different varieties of each crop, plays a crucial role in the main- and correcting them for estimation bias. Ricotta and Avena (2003) of-
tenance of household food security, the major production goal of poor fered a simple analytical relation between Pielou’s evenness and land-
farmers' resource. Such crop diversity allows farmers to adapt their scape dominance within the broader context of Hill’s parametric di-
cropping systems to local ecological micro-niches in their fields and to versity family. Within this context, they recommend the use of Hill’s
satisfy household food preferences and also provides protection against diversity number evenness to overcome the shortcomings both of Pie-
pathogens. Also, the extent of genetic variation determines how well a lou’s evenness and the landscape dominance index.
population or species can adapt to environmental challenges such as The agrobiodiversity index is a consistent, long-term monitoring
new crop pests, diseases and drought, among others (Simmonds, tool to measure and manage biodiversity across four dimensions: diets,
1991a,b). production, seed systems, and conservation (Ann Tutwiler, 2016).
Also, genetic erosion could beacon sequence of global environ- Blanco et al. (2015) proposes a novel index to assess agrobiodiversity in
mental change and more intensified modes of crop production (Schmidt systems that mix species, varieties, life forms, and uses. The new index
and Wei, 2006). Plant genetic resources can be improved in many ways was compared with the Shannon and Pielou indexes, which were
such as: gene banks for plants and animals, seed banks, field gene proved accurate for assessing and monitoring agrobiodiversity at the
banks, sperm banks, protected regions, global germplasm reserves, rare species and varietal levels. Shannon and Pielou concluded that the
breeds centers, zoos and modern breeding technology, and re- index is a useful tool for agrobiodiversity monitoring in agricultural
introduction ‘back into the wild’ programs. systems undergoing changes in practices and for achieving a better
understanding of their biocultural resilience.
3.9. Biodiversity measurement methods
4. Discussion
Biodiversity is a key topic in ecological studies. A main drawback in
biodiversity evaluation is that different indicators may lead to different According to the present literature review, biodiversity services are
orderings among communities according to their biodiversity. critical in modern agroecosystems. Increasing biodiversity can favor-
Biodiversity can be measured by many indices such as species richness, ably affect some ecosystem functions. But, current agricultural expan-
evenness, taxonomic indices, Margalef’s index, Simpson’s index, sion and intensification led to biodiversity loss in agroecosystems. In
Shannon-Wiener index etc. In practice, species richness is often used this regard, when natural ecosystems are shifting to modern agroeco-
due to its simplicity. Intuitively, however, the applicability of species systems, biodiversity can be directly or indirectly modified to increase
richness for quantifying species’ response to environmental changes is benefits to agroecosystems. For example, habitat heterogeneity could
questionable because it is sensitive only to events that cause extreme lead to attract natural enemies to agroecosystems. To maximize benefits
changes in species abundance distributions. In conclusion, the mea- of heterogeneity systems, identification of species and an integrated
surement of ecological differences in communities using solely species consideration of different aspects of communities such as evenness, and
richness has been described as ecologically unrealistic (Hackman, richness are essential components.
2015). Many key ecosystem services and roles are provided by biodiversity
Many recent studies have proposed new methods and software for (Tables 1 and 2). These services play a fundamental role in human food
dealing with biodiversity assessment. For example, Di Battista et al. security and health. Promoting the healthy functioning of ecosystems
(2017) proposed the R package BioFTF, which is a tool for statistical ensures the resilience of agriculture as it intensifies to meet growing
biodiversity assessment in the functional data analysis framework. This demands for food production. Climate change and other stresses have

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the potential to make major impacts on some functions, such as polli- security, richer biodiversity within agroecosystems should be increas-
nation and pest regulation services. Learning to strengthen the eco- ingly recognized as an important element to contribute to sustainable
system linkages that promote resilience and to mitigate the forces that development.
impede the ability of agroecosystems to deliver goods and services re- Some studies have shown, how biodiversity can actually influence
mains an important challenge. Agroecosystems managers can build on the loss of genetic diversity (genetic erosion). The extent of genetic
upon, enhance, and manage the essential ecosystem services provided variation determines the state of adaptation of a population or species
by biodiversity in order to work towards sustainable agricultural pro- to environmental challenges such as new crop pests, diseases and
duction. This can be achieved by good farming practices which follow drought. Biodiversity helps farmers matching their cropping systems to
ecosystem-based approaches designed to improve sustainability of local ecological micro-niches in order to provide the household food
production systems (FAO, 2011). requirements and protecting them against pests. Considering genetics
At all times, biodiversity directly provides societal needs to re- erosion as one of the important challenges of the agroecosystems, this
sources and food security. As a result, biodiversity is an irreplaceable review suggests that advanced studies are needed in this subject. Also,
good for human societies and natural ecosystems. It contributes to recent evidence reveal that for extending biological controls strategies
ecological restoration, pest control, higher carbon sequestration, lower in agroecosystems, the relationship between agroecosystems in-
erosion risk, and higher production. Nowadays, scientists believe that tensification, biodiversity and pests control needs to be supported. It
food production is highly dependent on biodiversity and the services should be considered that the loss of diversity of natural enemies in
provided by ecosystems. In addition, genetic erosion and land use agroecosystems increased water and groundwater pollution and en-
change can effect on biodiversity. Based on available scientific knowl- vironmental costs.
edge, there is a complex relationship between biodiversity and land use Geographic information about biodiversity is helpful and crucial to
(Haines-Young, 2009). While land use activity could have positive ef- understand the services that are provided by nature and their potential
fects biodiversity, in most cases, it leads to species degradation. Many changes; however, our knowledge in these respects is unreliable and
researchers suggested that the LCA technique could be used to assess often insufficient. This paper suggests that further studies are needed in
the effects of human activities such as land use on biodiversity (Souza this subject in regions with reduced biodiversity resources.
et al., 2015). LCA principally introduces biodiversity as an endpoint To protect biodiversity in agroecosystems, a policy consonance and
category modeled as a loss in species richness due to the conversion and strategic support to ecosystems need to be framed. This review suggests
management of land in time and space. that the challenges of food security, climate change, genetic erosion,
Recent studies have revealed a global decline in biodiversity. Loss of pest control, carbon restoration and biodiversity loss in agroecosystems
biodiversity due to monoculture is one of adverse effects of modern need a coherent global policy approach. For example, major challenges
agricultural systems. Some activities such as agriculture and forestry in agroecosystems include the need to shift to varieties better adapted
are one of the most important ways to increase the biodiversity in urban to particular components of climate change or to rethink strategies to
land uses. It seems that coming green spaces to typically highly sim- control invasive and pest outbreaks, finding solutions in the increasing
plified, intensively developed ecosystems with low levels of native competition for water between the natural and the agricultural eco-
biodiversity in these land uses (Lin and Fuller, 2013). These urban systems. This paper suggests that more studies are needed in order to
systems could enhance biodiversity and provide some ecological func- improve infrastructures and adapting agroecosystems to meet future
tion and services. Also, biodiversity is the basis of survival of the nat- demands of a growing population living on poorer biodiversity re-
ural systems and could be considered a vital component of sustainable sources.
farming systems. A number of points need to be highlighted. First, other advanced
Considering the current state of biodiversity in the world, the need studies need about ecological restoration of agroecosystems that it can
to reduce the current rate of resource degradation is increasing. Today, be recommended as a way to increase biodiversity in agricultural eco-
we have to use the ability of biodiversity to support modern agroeco- systems. Second, biodiversity can be integrated into LCA on a global
systems by providing numerous services such as food security, carbon scale. Third, map of life attempts to provide best-possible species range
sequestration, pest control, and its effect on climate change and genetic information and species lists for different geographic areas. The map of
erosion reduction rather than focusing on agrochemical substances such life aims to support effective and biodiversity education, monitoring,
as Glyphosat presently under debate in the member states of European research and decision-making by combining a wide range of knowledge
Union. about species distributions and their dynamics. Thus, it can be con-
To protect biodiversity in agroecosystems, a policy consonance and sidered as attractive studies in future. Fourth, the relationships between
strategic support to ecosystems should be considered. This review biodiversity and biological control in agroecosystems have not been
suggests that the challenges of food security, climate change, genetic settled completely, therefore, supplementary research is recommended
erosion, pest control, carbon restoration and biodiversity loss in in this regard. As a final point, it could be concluded that effective
agroecosystems need a coherent global policy approach. For example, improvement and conservation biodiversity in agroecosystems is ur-
major challenges in agronomy include the need to shift to species or gently required. Moreover, policy coordination and strategic support to
varieties better adapted to particular components of climate change or agricultural systems will be considereundeniable necessities in future.
to rethink strategies to control invasive and pest outbreaks, finding
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