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Enhancing biodiversity in cropping systems is suggested to promote ecosystem services, thereby reducing dependency on agronomic inputs while maintaining high crop yields. We assess the impact of several diversification practices in cropping systems on above- and belowground biodiversity and ecosystem services by reviewing 98 meta-analyses and performing a second-order meta-analysis based on 5160 original studies comprising 41,946 comparisons between diversified and simplified practices. Overall, diversification enhances biodiversity, pollination, pest control, nutrient cycling, soil fertility, and water regulation without compromising crop yields. Practices targeting aboveground biodiversity boosted pest control and water regulation, while those targeting belowground biodiversity enhanced nutrient cycling, soil fertility, and water regulation. Most often, diversification practices resulted in win-win support of services and crop yields. Variability in responses and occurrence of trade-offs highlight the context dependency of outcomes. Widespread adoption of diversification practices shows promise to contribute to biodiversity conservation and food security from local to global scales.
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Tamburini et al., Sci. Adv. 2020; 6 : eaba1715 4 November 2020
SCIENCE ADVANCES | RESEARCH ARTICLE
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ECOLOGY
Agricultural diversification promotes multiple
ecosystem services without compromising yield
Giovanni Tamburini1,2*, Riccardo Bommarco1, Thomas Cherico Wanger1,3†, Claire Kremen4,5,
Marcel G. A. van der Heijden6,7, Matt Liebman8, Sara Hallin9
Enhancing biodiversity in cropping systems is suggested to promote ecosystem services, thereby reducing de-
pendency on agronomic inputs while maintaining high crop yields. We assess the impact of several diversification
practices in cropping systems on above- and belowground biodiversity and ecosystem services by reviewing 98
meta-analyses and performing a second-order meta-analysis based on 5160 original studies comprising 41,946
comparisons between diversified and simplified practices. Overall, diversification enhances biodiversity, pollination,
pest control, nutrient cycling, soil fertility, and water regulation without compromising crop yields. Practices
targeting aboveground biodiversity boosted pest control and water regulation, while those targeting belowground
biodiversity enhanced nutrient cycling, soil fertility, and water regulation. Most often, diversification practices
resulted in win-win support of services and crop yields. Variability in responses and occurrence of trade-offs highlight
the context dependency of outcomes. Widespread adoption of diversification practices shows promise to contribute
to biodiversity conservation and food security from local to global scales.
INTRODUCTION
Agricultural expansion and intensification are considered major
drivers of habitat and biodiversity loss, soil and freshwater degradation,
environmental pollution, and greenhouse gas emissions worldwide
(1,2). Implementation of a new crop production paradigm is needed
to take on the local to global challenges of providing food security
for rapidly growing demands from human societies while minimiz-
ing negative impacts on the environment in a world exposed to
global changes (3).
Crop management based on diversification practices that en-
hance key elements of biodiversity has been suggested to reduce
impacts on the environment without negative effects on crop yields
(4). Enhancing the diversity of biological communities, both above and
below ground, can increase resource use efficiency and the stability
of ecosystem production over time (57). Agricultural diversifica-
tion is the intentional addition of functional biodiversity to cropping
systems at multiple spatial and/or temporal scales, and it aims at
regenerating biotic interactions underpinning yield-supporting
ecosystem services (8). It embraces a variety of practices encom-
passing the management of crops, noncrop habitats, soil, and land-
scapes (9). Functional biodiversity can be enhanced by increasing
crop species diversity (e.g., intercropping and crop rotation), in-
creasing noncrop species diversity within and around the fields
(e.g., flower strips, hedgerows, and seminatural habitats), or by in-
oculation of beneficial microorganisms into the soil (e.g., arbuscular
mycorrhizal fungi, N2-fixing bacteria, and growth-promoting
bacteria). Functional diversity below ground can also be supported
and stimulated through addition of organic inputs (e.g., manure and
crop residues) or reducing soil disturbance (e.g., reduced tillage), which
lead to soil stratification and thereby more niches (8, 9). Despite a
rapidly growing body of research assessing the impacts of agricul-
tural diversification practices on biodiversity and related ecosystem
services (7,1012), there is no comprehensive quantitative synthesis
of this information. Consequently, we lack the broader understand-
ing of whether diversification practices are actually capable of
supporting biodiversity and multiple ecosystem services, including
crop yields.
We investigated the impact of multiple agricultural diversifica-
tion practices on biodiversity and related ecosystem services and
compared these with cropping systems with less diverse farming
practices typical of mainstream agriculture. First, we systematically
reviewed published meta-analyses and summarized the number of
reported effect sizes (vote count) to assess the current state of
knowledge, identify research gaps, and explore general patterns. We
included studies based on stringent criteria such as relevance, eligi-
bility, and statistical independence, thereby ensuring the largest
possible primary database with minimum overlap of original studies
(figs. S1 and S2 and see Materials and Methods). Second, to estimate
the overall impact of agricultural diversification on biodiversity and
ecosystem services provisioning, we performed a second-order meta-
analysis on the subset (70%) of the meta-analyses that reported
comparable effect sizes. Second-order meta-analyses are frequently
used in health science but have only rarely been used in ecology or
agricultural research (see Materials and Methods).
We based our systematic review on 98 meta-analyses and 456 effect
sizes based on 6167 original studies (see Materials and Methods).
We grouped the diversification practices into six broad categories
[following (8,9)]. The first five are crop diversification by addition
of crop species in the field over space or time, noncrop diversification
by addition of noncrop habitats within or around the field or in the
surrounding landscape, organic amendment by addition of organic
1Department of Ecology, Swedish University of Agricultural Sciences, Uppsala,
Sweden. 2Department of Soil, Plant and Food Sciences (DiSSPA-Entomology),
University of Bari, Bari, Italy. 3Agroecology, University of Göttingen, Göttingen,
Germany. 4Department of Environmental Sciences, Policy and Management,
University of California, Berkeley, USA. 5Institute for Resources, Environment and
Sustainability, Biodiversity Research Center and Department of Zoology, University
of British Columbia, Vancouver, Canada. 6Plant-Soil-Interactions, Research Division
Agroecology and Environment, Agroscope, Switzerland. 7Department of Plant
and Microbial Biology, University of Zürich, Zürich, Switzerland. 8Department of
Agronomy, Iowa State University, Iowa, USA. 9Department of Forest Mycology
and Plant Pathology, Swedish University of Agricultural Sciences, Uppsala,
Sweden.
*Corresponding author. Email: giovanni.tamburini@uniba.it
†Present address: Westlake University, School of Engineering, Hangzhou, China.
Copyright © 2020
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rights reserved;
exclusive licensee
American Association
for the Advancement
of Science. No claim to
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material to the soil, inoculation by addition of beneficial micro-
organisms into the soil, and reduced tillage (table S1). In addition, we
included organic farming, i.e., production systems free of synthetic
pesticides and mineral fertilizers, as a sixth separate category for
comparison since this is a widely adopted practice in some regions.
In the selected meta-analyses, diversified agriculture was compared
with the relevant control practices typical of mainstream farming,
such as monoculture, short crop rotation, simplified landscapes,
use of mineral fertilizers, and deep tillage (table S1). We divided the
response variables into nine biodiversity/ecosystem service categories
(hereafter, “ecosystem service categories”) (13,14): biodiversity,
water regulation, carbon sequestration, climate regulation, nutrient
cycling, soil fertility, pollination, pest control, and crop yield (table S2).
Water regulation refers to water quality and quantity, climate regu-
lation refers to greenhouse gas dynamics, and carbon sequestration
refers to carbon storage. To describe the effects of diversification
practices on key attributes of cropping systems comprehensively,
we kept soil fertility, nutrient cycling, carbon sequestration, and
climate regulation as separate services, although the first two have
been previously grouped as “maintenance of soil fertility” (14) and
the last two as “climate regulation” (13). In our systematic review,
for each ecosystem service category, we recorded and compared the
number of different responses to diversification (i.e., effect sizes), classi-
fying them as positive, negative, or neutral (i.e., no significant effect).
For the second-order meta-analysis, we selected 69 meta-analyses,
enabling a statistical analysis of 324 effect sizes, based on 5160 original
studies and a total of 41,946 original comparisons. We extracted
global effect sizes, sampling error variances, and their associated
sample sizes, i.e., the number of original comparisons. We trans-
formed effect sizes to a common metric [log of the response ratio
(lnRR)] and conducted multilevel mixed-effects meta-analyses to
explore effects of diversification practices on biodiversity and eco-
system service delivery (see Materials and Methods). We found an
unbalanced occurrence of effect sizes belonging to different ecosystem
service categories across diversification practices and, therefore,
adopted a multiple step hierarchical approach. We first ran a global
model to test whether the mean effect of diversification differed from zero
for different ecosystem service categories with all diversification
practices included (model 1) (see Materials and Methods). Second,
we explored biodiversity and ecosystem service responses to diver-
sification practices mainly targeting functional biodiversity in the
aboveground environment with crop and noncrop diversification
(model 2) and the belowground environment with organic amend-
ment, reduced tillage, and inoculation (model 3). Third, we ran
separate models for practices that had a sufficient number of effect sizes,
which were organic amendment, reduced tillage, and crop diversifica-
tion (models 4, 5, and 6, respectively). All models included sample
size as a weight, thus giving more importance to effect sizes based
on a higher number of original studies and comparisons. The re-
sults from both the systematic review and the second-order meta-
analyses were robust to variations in study quality, inclusion criteria,
and ecosystem service classification and to potential publication bias
(figs. S3 to S6).
RESULTS
Trends from the systematic review
Our systematic review showed that the impact of agricultural diversi-
fication on biodiversity and ecosystem services was predominantly
positive (67% positive effect sizes, 23% neutral effect sizes, and 10%
negative effect sizes; Fig.1), with soil fertility and nutrient cycling
having the highest numbers of positive effect sizes. Crop yield and
climate regulation displayed the highest proportion of negative
responses to diversification practices (16 and 41%, respectively;
Fig.1A). The number of published meta-analyses has increased
exponentially in the past decade, especially global-scale analyses
(fig. S7, A and C). However, we found research gaps for specific
services and practices. The most frequently observed ecosystem
services category was soil fertility with 92 effect sizes, followed by
crop production and nutrient cycling (87 and 84 effect sizes; fig.
S7D). By contrast, pollination, biodiversity, and pest control were
less represented (10, 18, and 29 effect sizes, respectively). The most
examined diversification practices were organic amendment, re-
duced tillage, and crop diversification (146, 118, and 111 effect
sizes), whereas noncrop diversification and inoculation, as well as
organic farming, were less represented (38, 9, and 34 effect sizes)
and need further investigations.
Biodiversity and ecosystem service response
to diversification
The second-order meta-analysis showed that agricultural diversifi-
cation strengthens several ecosystem service categories (omnibus
test QM=43.67; P<0.0001; Fig.2A) while having a neutral effect on
crop yield [lnRR= 0.01; 95% confidence interval (CI)=−0.12 to
0.14]. Diversification practices enhanced biodiversity (lnRR=0.34;
95% CI=0.15 to 0.53), pollination (lnRR=0.28; 95% CI=0.02 to
0.55), pest control (lnRR=0.23; 95% CI=0.04 to 0.41), nutrient
cycling (lnRR=0.18; 95% CI = 0.10 to 0.27), water regulation
(lnRR=0.18; 95% CI=0.07 to 0.28), soil fertility (lnRR=0.17; 95%
CI=0.08 to 0.26) and, marginally, carbon sequestration (lnRR=0.11;
95% CI=−0.01 to 0.23). Climate regulation response did not differ
statistically from a neutral effect (lnRR=0.04; 95% CI=−0.08 to
0.15). Both groups of diversification practices targeting either
the above- or belowground environment enhanced nutrient cycling
and water regulation, but affected the delivery of other services
differently (Fig.2,BandC, and table S4). Diversification practices
targeting the aboveground environment (i.e., crop and noncrop
diversity) increased pest control, whereas diversification practices
targeting the belowground environment (i.e., organic amendment,
reduced tillage, and inoculation) enhanced soil fertility and, mar-
ginally, carbon sequestration (Fig.2,BandC, and table S4). Analyses
of specific practices presented consistent results: organic amendment
increased water regulation, soil fertility, nutrient cycling, and carbon
sequestration, reduced tillage enhanced soil fertility, nutrient cycling,
and (belowground) biodiversity, and crop diversity improved
(aboveground) biodiversity, pest control, nutrient cycling, and
water regulation (table S5).
Trade-offs between crop yield and multiple
ecosystem services
We visualized trade-offs, lose-lose relationships, and win-win rela-
tionships between crop yield and multiple services by plotting com-
binations of effect sizes (15) gathered from the 23 meta-analyses in
which the responses to diversification of crop yield and at least one
other service were analyzed simultaneously (Fig.3). We only found
111 effect size combinations, highlighting that effects of diversifica-
tion on multiple ecosystem services is a major research gap (16). We
found that agricultural diversification mainly promoted win-win
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scenarios, supporting crop yield and the provisioning of a range of
services (63% of the combinations; Fig.3). Most of them are moderate
gains, but the greatest win-win relationships with crop yield include
nutrient cycling and soil fertility. Climate regulation presented in-
stead the highest number of trade-offs, with 50% representing situations
where an increase in yield corresponded to a decrease in climate
regulation provision. In addition, pest control was competing with
yield in some cases.
DISCUSSION
Both the systematic review and the second-order meta-analysis
show that agricultural diversification practices enhance biodiversity
and the delivery of several supporting and regulating ecosystem
services pivotal to crop yield. Crop and noncrop diversification in-
creased the provisioning of pest control and pollination, respectively
(Figs.1,DandE, and 2), which is in line with global results based on
raw primary data (17). Services associated with soil quality, particularly
N effect sizes
All diversification practices
0
25
50
75
N effect sizes
Positive
Neutral
Negative
Crop yield
Soil fertility
Nutrient cycling
C sequestration
Climate
regulation
Water regulation
Pest control
Biodiversity
Pollination
Response
100
0
10
20
30
0
10
20
30
0
10
20
30
N effect sizesN effect sizes
D Crop diversification
B Organic amendment C Reduced tillage
E Noncrop diversification
F Inoculation G Organic farming
A
NCGHG
NCGHG
NCGHG
NCGHG
NCGHG NCGHG
NCGHG
Fig. 1. Vote count reveals that agricultural diversification practices generally have a positive impact on biodiversity and ecosystem services. Number of reported
effect sizes with a significant positive (green), negative (red), or neutral (gray) response to agricultural diversification, overall (A) and to each category of diversification
practice separately (B to G). The systematic review comprises 456 effect sizes from 98 meta-analyses based on 6167 original studies (fig. S1). Diversification practice and
ecosystem service categories were based on classifications following (8, 9) and (13, 14, 27), respectively (tables S1 and S2).
Carbon sequestration (29,16
)
Soil fertility (65,25)
Pest control (14,7)
Pollination (4,3)
Biodiversity (10,7)
Climate regulation (42,18)
Crop yield (62,39)
Soil fertility (65,25)
Nutrient cycling (67,26)
Water regulation (31,17)
Pest control (14,7)
Pollination (4,3)
Biodiversity (10,7)
0.0 0.2 0.4
Effect size (lnRR)
(14,6)
(1,1)
(18,12)
(20,9)
(24,10)
(6,4)
(5,3)
(1,1)
(2,2)
0.0 0.5 1.0
Effect size (lnRR)
–0.5
(15,11)
(3,3)
(41,17)
(43,27)
(44,20)
(37,18)
(25,13)
(3,2)
(0,0)
0.0 0.5 1.0
Effect size (lnRR)
–0.5
Diversification practices targeting
the aboveground (n = 91)
Diversification practices targeting
the belowground (n = 211)
All diversification practices
(n = 324)
BAC
Fig. 2. Second-order meta-analysis shows how agriculture diversification promotes biodiversity and ecosystem services without compromising crop yield
when compared with cropping systems without these practices. (A) All diversification practices included (324 effect sizes and 69 meta-analyses, based on 5160 orig-
inal studies with 41,946 comparisons). (B) Diversification practices targeting the aboveground environment (crop and noncrop diversity; 91 effect sizes and 24 meta-
analyses). (C) Diversification practices targeting the belowground environment (organic amendment, reduced tillage, and inoculation; 211 effect sizes and 55 meta-analyses).
Note the difference in scale of the x axes when comparing (A) with (B) and (C). Organic farming is included only in the global model (A) since it often includes practices
targeting both above- and belowground environments. The number of effect sizes and meta-analyses included in each category are displayed in parentheses. Ecosystem
service categories are classified following (13, 14, 27) (table S2). Error bars represent 95% CIs.
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soil fertility and nutrient cycling, responded in a consistent posi-
tive manner to several diversification practices, mainly to organic
amendment and reduced tillage (Fig.1), and presenting the smallest
variabilities (Figs.2 and 3). This is likely because these services are
largely affected by the soil organic carbon pool, which is typically
promoted by diversification measures (2). Our sensitivity analysis
revealed that the similar responses of soil services were not merely
due to using common indicators or correlations among variables
(e.g., soil organic carbon; table S2), but rather similar responses of
different soil functions and properties (figs. S4 and S5). Diversification
practices also increased both the quality and quantity components
of water regulation provisioning (fig. S6). In particular, practices
targeting the aboveground environment, i.e., crop and noncrop
diversity, greatly enhanced water regulation (Fig.2B), primarily by
increasing water quality by limiting nitrogen leaching loss (table S2).
Differences in effect sizes when separating between above- and below-
ground diversification practices suggest different mechanisms and
processes driving this ecosystem service response to diversification.
The variation in crop yield response to overall diversification
suggests a high degree of context dependency (Figs.1 and 2). It
highlights that there are conditions and practices we need to avoid
but also ample opportunities to reap benefits from diversifica-
tion. For example, our systematic review shows that yield often
decreases under reduced tillage management and organic farming
but generally increases with crop diversification and inoculation
(Fig.1, C,D,F,andG). Moreover, yields have been shown to
improve under reduced tillage in dry climates by retaining crop res-
idues and by applying longer crop rotations (18). The adoption of
appropriate combinations of diversification practices thus holds
great potential to increase yields compared with mainstream farm-
ing. The visualization of the relationships between crop yield and
multiple services reveals that the majority of the win-win situations
(74%) includes soil fertility, nutrient cycling, and water regulation
(Fig.3), probably because practices that improve soil functioning
simultaneously increase resource availability for the crops. A key
aim for the development of locally adapted cropping systems will be
to identify diversification solutions that sustain both crop yield and
multiple ecosystem functions, resulting in win-win outcomes.
The response of climate regulation was highly variable and yielded
the highest number of trade-offs and lose-lose relationships (Fig.3).
These were mostly driven by increased greenhouse gas emissions
caused by the application of organic soil amendments (Fig.1)
(3,19). However, our analysis also demonstrates that organic inputs
promote soil fertility, nutrient cycling, carbon sequestration, and
water regulation, by increasing soil organic carbon, nutrient avail-
ability, and soil water storage and limiting nutrient leaching and
runoff (tables S2 and S5). Soil bacteria and arbuscular mycorrhizal
fungi, which are key contributors to soil functioning, were also
enhanced (fig. S6 and table S2) (6). Organic amendments thus have
complex positive and negative and also cascading effects on the
cropping system and the environment. For example, positive climate
feedbacks can arise because of increased soil respiration caused by
priming effects, where added organic material triggers the degrada-
tion of older soil organic matter, leading to emissions of CO2, but
are mainly driven by the increasing emissions of the far more potent
greenhouse gas nitrous oxide. Organic amendments fuel micro-
organisms with the capacity to produce this gas to such a degree that
the positive climatic effects by increased carbon storage in fertilized
agricultural soils are predicted to be offset by nitrous oxide emissions
already by 2060 (20). It would be valuable to further consider not only
the impacts of organic matter input but also those of production,
such as livestock and cultivation of legumes for feed with large
impact on land-use change and direct greenhouse gas emissions.
This would allow a comprehensive understanding for effects of or-
ganic amendments on climate change. A key challenge for sustain-
able crop production is hence to seek diversification solutions that
simultaneously sustain soil health, crop yield, and mitigation of
climate change.
We show that agricultural diversification promotes biodiversity
and the delivery of ecosystem services without compromising crop
yield. This suggests several pathways for future sustainable food
production and demonstrates how mainstream, high-yielding crop
production can benefit from management that bolsters biodiversity.
Large areas of cropland with monocultures in vast crop fields, such
as in Australia, and North and South America (3), could benefit by
the implementation of longer crop rotations, intercropping, and
higher noncrop species diversity that enhance aboveground bio-
diversity and the provisioning of regulating services, such as pollina-
tion, pest control, and water regulation. Belowground biodiversity
and services associated with soil quality are mainly supported by
organic amendment and reduced tillage. Further, our results indicate
that combining diversification practices is potentially advantageous
for the provisioning of multiple ecosystem services and biodiversity
conservation (Fig.2). This shows promise to reduce crop production
Concomitant ES response (lnRR)
Crop yield
response (lnRR)
−0.4
−0.2
0.0
0.2
0.4
−0.5 0.0 0.5 1.0
Trade-off–1
Trade-off–2
Win-win
Lose-lose
Carbon sequestration (4,3,3)
Nutrient cycling (20,8,8)
Pest control (8,6,4)
Soil fertility (17,4,4)
Water regulation (12,7,7)
Climate regulation (21,16,8)
10%
12%
15%
63%
Biodiversity (1,1,1)
Pollination (1,1,1)
Fig. 3. Agricultural diversification generally promotes win-win scenarios, simultaneously supporting crop yield and the provisioning of a concomitant ecosys-
tem service category. The visualization is based on a subset of meta-analyses, which simultaneously presented the responses to agricultural diversification of crop yield
(y axis) and at least one concomitant ecosystem service (ES) (x axis) (in total 24 studies, 111 pairs of effect sizes). Numbers in red indicate the proportion of effect size
combinations in each quadrate. Points represent combinations of raw effect sizes (lnRR) and the colors correspond to the specific service, as indicated in the box to the
right. Values in parentheses after each service indicate the number of effect sizes for the concomitant service, crop yield, and the number of meta-analyses.
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dependency on agrochemicals and its negative impacts on the en-
vironment, adapt to and hedge risks from climate change, and con-
tribute to global food security.
Overall, agricultural diversification emerges as a general strategy
to reach the sustainable development goals defined by the United
Nations, which basically all are directly or indirectly linked to agri-
culture. Trans- and interdisciplinary research efforts will be required
to tailor economically, socially, and environmentally sustainable
diversification practices to specific cropping systems and local con-
texts. Although recent research shows that diversification can be an
economically viable alternative for farmers also in current food sys-
tems (21), widespread uptake of diversified agriculture needs to be
supported by transformations in the food systems. This involves
investments into the development and spread of evidence-based
knowledge on the efficiency of diversification practices, including
cost-benefit analyses (22), and into the removal of potential barriers
to farmers’ uptake such as up-front costs, access to credit and
appropriate equipment, as well as into supportive technologies and
infrastructure to process and distribute the products. Changes
of market conditions causing imbalanced power relations in the
food value chain (23) and improved targeting of subsidies are
needed to relieve farmers from the price-cost squeeze of high input
and low output prices (24). This would provide farmers with the
decision space, tools, and opportunity to develop and implement
diversification practices based on situated knowledge.
MATERIALS AND METHODS
Systematic review
We focused on meta-analyses rather than on original studies because
they are useful for summarizing scientific evidence and extrapolating
general trends (25). The main advantage is the high level of general-
ization that can be achieved when using a large number of individual
observations already summarized in first-order meta-analyses. More-
over, since a meta-analysis can be conducted only when sufficient
and appropriate quantitative data from original studies are avail-
able, the number of published meta-analyses about a certain topic is
an indicator of the overall understanding of the subject, allowing us
to reveal research gaps (25,26).
Definition of diversification farming practices
and ecosystem services
Diversification practices were defined as intentional addition of
functional biodiversity to cropping systems at multiple spatial and/
or temporal scales (8). The six categories of diversification practices
were based on previous classifications and selected in an expert
workshop to cover the diversification practices found in our sys-
tematic review (table S1). We acknowledge that other classifications
are possible and some management categories overlap. For instance,
organic farming often also includes other diversification practices
as crop rotation and the application of organic amendments.
Numerous concepts and classification systems for ecosystem
services have emerged in the past decades leading to a plurality in
terminology and definitions. We defined ecosystem services as “the
direct and indirect contributions of ecosystems to human well-being”
(14). Building on existing classifications (13,14,27), we identified
eight ecosystem services in the cropping system context: water reg-
ulation, carbon sequestration, climate regulation, nutrient cycling,
soil fertility, pollination, pest control, and crop yield (table S2). The
first seven services affect crop yield directly in the field and also
indirectly by influencing the larger environment around the field.
Some of these services also affect human well-being via other mech-
anisms than their contribution to food production, e.g., carbon
sequestration and clean water.
Literature search and selection criteria
A flowchart of the literature search and selection and study frame-
work is provided in fig. S1 (28). We initiated a literature search us-
ing the Web of Science online database using the search string:
TOPIC =(crop* OR “noncrop” OR intercropping OR “inter-
cropping“ OR “inter cropping” OR compost* OR till* OR “vegetation
strip*” OR agroforest* OR inoculat* OR landscape OR organic OR
fallow OR conventional OR fert* OR reduce* OR rotation OR “catch
crop” OR amend*) AND (“meta-analysis” OR “metaanalysis” OR
“meta-analysis”) AND (divers* OR soil* OR biomass* OR water* OR pol-
lutant* OR sediment* OR fodder OR emission* OR carbon* OR
climat* OR pest* OR “biocontrol” OR weed* OR pollinat* OR fert*
OR energ* OR resistance OR productiv* OR yield*). The search was
then refined for the categories Environmental Sciences, Environ-
mental Studies, Ecology, Agronomy, Agriculture Multidisciplinary,
Plant Sciences, Biodiversity Conservation, Evolutionary Biology, Hor-
ticulture, Multidisciplinary Sciences, Entomology, Biology, and
Soil Sciences. We identified peer reviewed meta-analyses published
until November 2018. We then integrated the literature search with
targeted research strings in Google Scholar (e.g., “meta analysis
AND crop AND “flower strips” OR “hedgerow””). We achieved a
reasonable coverage of grey literature since many of the meta-analyses
were partly based on unpublished data and non- English texts not
indexed in official search engines.
We examined the title and abstract of each article to assess how
well it met our selection criteria. The main selection criterion re-
quired a quantitative assessment of the impact of one or more
diversification practices on any ecological process in the context of
crop production (table S1). This resulted in an initial set of 278 articles,
for which the following additional criteria for inclusion were adopted:
(i) The effect of a diversification practice had to be investigated for
crop species, including biofuel crops, and compared with that of a
control, i.e., farming practices commonly adopted in mainstream
agriculture and standard for that particular crop and region. We
excluded studies on livestock production systems, comparisons of
cropping systems with natural or seminatural ecosystems, and tran-
sitions from crop fields to other habitat types, i.e., afforestation or
crop land abandonment. (ii) The list of original studies included in
the meta-analyses and the origin of grey literature had to be pre-
sented. In five cases, we asked authors to provide the reference list.
We excluded any meta-analyses whose original studies were a subset
of a more recent meta-analysis. (iii) The effect of a diversification
practice on the response variables had to be calculated with meta-
analytic techniques and presented as an effect size. We excluded
studies that mentioned an effect size without specifying how it was
calculated. (iv) We only included the global effects if partial effect
sizes based on subsets of observations were also presented, to avoid
pseudo-replication. For the same reason, if potentially correlated
response variables were investigated, then we made an informed
decision on which variable to select. For instance, if both soil organic
carbon and total soil carbon were presented in the study, then we
chose only soil organic carbon. (v) For multiple effect sizes calculated
for different points across space, e.g., at different soil depths, we
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included only the measures most relevant to crop production, such
as soil organic matter measured between 0- and 30-cm soil depth. A
total of 111 meta-analyses met our criteria.
Statistical independence assessment
Extrapolating general trends from a set of meta-analyses requires
the fundamental assumption that the primary meta-analyses are in-
dependent, i.e., that they are based on different sets of original studies.
However, it is possible that an original study is included in more
than one meta-analysis on a given topic. This happens when differ-
ent meta-analyses ask different questions or when data from older
meta-analyses have been included in more recent analyses. To avoid
this form of pseudo-replication, we examined more than 6300
references (fig. S2) and calculated the proportion of shared original
studies among the selected meta-analyses. We included only meta-
analyses presenting a maximum of 30% of shared original studies
(29). We checked for both the systematic review and the second-
order meta-analysis whether the adoption of more stringent thresh-
olds affected our results (see “Sensitivity analysis” section below). If
two or more meta-analyses shared a higher proportion than 30%,
then we selected the meta-analysis based on the largest number of
original studies (usually the most recent) and discarded the others
(i.e., last, none had a count of overlapping studies beyond 30%).
Meta-analyses presenting shared original studies, but focusing on
different response variables, e.g., effect of tillage management on
soil organic carbon versus effect on yield, were not considered as a
source of pseudo-replication.
Data extraction and response variable assignment
to different ecosystem service categories
A total of 98 meta-analyses met our criteria and were considered
statistically independent. Of the selected meta-analyses, 80% had
<20% shared original studies (mean value for the entire data-
set,11.5%). For each article, we further extracted the geographical
range covered by the original studies, the type of diversification
practice investigated, the response variables measured, and the
number of original comparisons for each effect size (fig. S7). We
also collected additional details for each effect size (where present)
about specific methodologies (data file S1). We categorized the re-
sponse variables of the included meta-analyses in different types of
ecosystem services or biodiversity (table S2). Assignment to catego-
ries was performed by the coauthors according to their expertise in
soil sciences (S.H., M.G.A.v.d.H., and M.L.), biodiversity (S.H.,
C.K., M.G.A.v.d.H., R.B., T.C.W., and G.T.), pollination and pest
control (C.K., R.B., T.C.W., M.L., and G.T.), and microbiology
(S.H. and M.G.A.v.d.H.). While some response variables were di-
rect measures of the final service delivered (e.g., crop yield), others
represented the ecosystem functions underpinning those services
(e.g., soil organic carbon content for soil fertility, and predation for
pest control) or were general indicators (informative proxies) (30)
of the service (e.g., weed and pollinator abundance for weed control
and pollination, respectively). Some of the response variables were
positively related to service provisioning, whereas others were neg-
atively related. For the systematic review, we recorded whether the
effect of a given diversification practice on a particular response
variable was significantly positive, neutral, or significantly negative.
We then adjusted the direction considering the relationship be-
tween each response variable and the correlated service provision.
For example, a significant decrease in carbon dioxide emissions in
response to biochar input was reported as a significant positive
effect of organic amendment on climate regulation.
Many response variables affect or are proxies for multiple cat-
egories of ecosystem services. For example, pollinator diversity
can be considered as a measure of both pollination and biodiversity.
In these cases, we used the same effect size for different ecosystem
service categories. The most frequent instance involved measures
of soil organic matter content categorized as measures of soil
fertility, nutrient cycling, and carbon sequestration (table S2) (31).
We checked for both the systematic review and the second-order
meta- analysis whether the inclusion of repeated effect sizes in
the dataset affected our results (see the “Sensitivity analysis” sec-
tion below). The final dataset comprised 456 effect sizes of which
113 were repeated, from 98 meta-analyses based on 6167 original
studies.
Quality assessment of individual meta-analyses
For each selected meta-analysis, we calculated a methodological
quality index since poorly and inexpertly conducted meta-analyses
can provide biased and misleading results (24,32). We used eight
criteria to assess study quality based on availability and/or clarity in
the presentation of (i) definition of the control group, (ii) literature
search method, (iii) number of original studies, (iv) inclusion/
exclusion criteria of original studies, (v) effect size average and CIs,
(vi) weighting procedure, (vii) heterogeneity assessment, and (viii)
sensitivity control. For each of these eight criteria, a meta-analysis
could receive a score of either 1 (low quality) or 2 (high quality). We
used the sum of the scores as an overall measure of quality, ranging
from 8 to 13 (“low quality”) to 14 to 16 (“high quality”). Our dataset
presented a score ranging from 10 to 16 (14 on average). We checked
for both the systematic review and the second-order meta-analysis
whether the inclusion of low-quality studies in the dataset affected
our results (33) (see the “Sensitivity analysis” section below).
Second-order meta-analysis
For the second-order meta-analysis, we first selected a subset of meta-
analyses that reported comparable measures of effect sizes, such as
the lnRR or closely related metrics (e.g., RR and percentage of change),
where lnRR= ln(XE) − ln(XC) (XE, diversification practice; XC,
mainstream practice). This is the ratio of the outcome of an experi-
mental group (XE) to that of a control group (XC). We excluded studies
reporting metrics based on standardized mean differences (i.e., Hedges d)
or correlation coefficients because they cannot be transformed into
an RR without access to the original data (34). On the basis of these
criteria, we were able to include 69 meta-analyses. From each of these,
we extracted global effect sizes, sampling error variances, and their
associated sample sizes. Sampling error variance is the square of the
standard error (SE), but these estimates are rarely reported. Instead,
a 95% CI of the effect size is usually provided, and half the width of the
95% CI divided by 1.96 is a good approximation to the SE (35,36).
Data were extracted from tables or graphs using GetData Graph
Digitizer 2.26 (http://getdata-graph-digitizer.com/). We transformed
effect sizes of individual meta-analyses to a common metric (lnRR).
Since direct log transformation of an RR (19 effect sizes) can lead to
an overestimation of the effect size, we applied a correction for the
log transformation as ln(RR)=ln(RR) − NSE2 × (2 RR2) − 1, where
N is the number of original comparisons. When higher values of
the effect sizes would mean negative impacts on service provisioning
(e.g., abundance of pest species or CO2 emission), we reversed
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the sign of the response. The final dataset for the second-order
meta-analysis included 324 effect sizes from 69 meta-analyses based
on 5160 original studies and 41,946 original comparisons.
Data analysis
We first ran a multilevel mixed-effects meta-analysis to determine
whether mean effect sizes for different ecosystem service categories
differed from 0 (model 1). We performed the analyses in the meta-
for package (ver. 2.1, rma.mv function) (36) that incorporates both
fixed (moderators) and random effects, allowing us to control for
nonindependence in the data due to multiple effect sizes per meta-
analysis. To account for heterogeneity both between and within studies,
we specified the effect size ID (identifier) and the study ID as random
effects in our model. The model that included a nested random
structure (1|Study ID/Effect size ID) yielded the lowest Akaike
Information Criterion (AIC) score compared with the other candidate
structures (table S3), and it was therefore retained. We included the
number of original comparisons as weight in the model (24,35), giving
more importance to measures based on a higher number of original
studies and comparisons. Last, we included the different types of
biodiversity/ecosystem services as one categorical moderator with
nine levels in the model. The general form of the global model was
lnRR~ES, vi, weight=N, random=~ 1 | Study ID/ Effect size ID
where ES is the ecosystem service categories, vi is sampling error
variance, and N is the number of original comparisons. Including
ES as moderator in the model led to a lower AIC score compared
with the null model (∆AIC=34.17). The model was run without the
intercept to obtain the parameter estimates (mean effect sizes) for
each level of the categorical variable. We did not include the inter-
action between ES and different types of diversification practices
because the number of combinations was too high (38 combination
levels). To further investigate the effects of different diversification
practices on biodiversity and ecosystem service delivery, we analyzed
different subsets of data. We ran two models only considering
diversification practices targeting above- or belowground environ-
ment (model 2: crop and noncrop diversification; model 3: organic
amendment, reduced tillage, and inoculation). Organic management
was not considered because it often includes both practices target-
ing above- and belowground environment (e.g., crop rotation and
organic amendments). We then ran separate models for those prac-
tices with sufficient number of effect sizes, when considering the
number of meta-analyses, the number of effect sizes and their dis-
tribution across explanatory variable’s levels. We hence separately
analyzed organic amendment (model 4, 126 effect sizes), reduced
tillage (model 5, 82 effect sizes), and crop diversity (model 6, 72
effect sizes). Models 2, 5, and 6 included only the effect size ID as
random effect, yielding the lowest AIC compared with the other
candidate structures. We did not include the geographical range
covered by the original studies as an explanatory variable in the
analyses due to the unbalanced distribution of effect sizes across
geographical regions, ecosystem service categories, and diversification
practices. Most of the meta-analyses performed global analyses, and
specific geographical areas were represented by only a few studies.
Fixed factor estimates were considered statistically significant if the
95% CI did not overlap zero. We checked the profile likelihood
plots to ensure the identifiability of the variance components in all
the models (e.g., model 1; fig. S8) (36). All parameter estimates are
reported for the best model run with REML (restricted maximum
likelihood). All analyses were performed in R software.
Publication bias
Publication bias was assessed using Funnel plot and Egger test tech-
niques by using meta-analytic residuals and including in rma.mv func-
tion the precision (1/SE) as a covariate (33,37). We considered analyses
to be biased if the intercept of this regression significantly deviated
from zero, indicating that the overall relationship between the preci-
sion and residuals is asymmetrical. We then calculated Rosenberg’s
fail-safe number to assess the robustness of our results to potential
publication bias (38). Furthermore, we explored whether our results
were driven by influential outliers, defined as effect sizes with hat values
(i.e., diagonal elements of the hat matrix) greater than two times the
average hat value (i.e., influential) and standardized residual values
exceeding 3.0 (i.e., outliers) (39,40). Funnel plot (fig. S3A), Egger test
[intercept, 0.01 (95% CI: −0.07, 0.09, P=0. 8502)], and the Rosenberg’s
fail-safe number (1131528, P<0.0001) showed no sign of publication
bias. The graphical test for influential outliers was also negative (fig. S3B).
Sensitivity analysis
We explored the robustness of the patterns from the systematic review
and the results of the second-order meta-analysis to low-quality data,
repeated effect sizes, and different thresholds of shared original
studies among meta-analyses. We tested four datasets: (i) the com-
plete dataset and three subsets including (ii) only high-quality studies,
(iii) no repeated effect sizes, and (iv) only high-quality studies and
no repeated effect sizes. For each of these, we applied four different
maximum levels of shared original studies (30, 25, 20, and 15%). For the
systematic review, results were highly robust as reflected in the similar
responses patterns for the data subsets (fig. S4). For the second-order
meta-analysis, we reran the analysis for each of the four datasets at dif-
ferent maximum levels of shared original studies. Again, results were
robust as shown by similar effect sizes for the data subsets (fig. S5).
Given the heterogeneity of response variables included in each
ecosystem service category, we tested whether a more stringent
classification would alter the results of the second-order meta-analysis.
We therefore reclassified the response variables into 17 ecosystem
service categories, keeping separated ecosystem functions, physical
properties, variables related to organisms, above- and belowground
variables, etc. For example, soil fertility was divided into soil physical
characteristics, soil nutrient availability and soil organisms, bio-
diversity into above- and belowground biodiversity, water regulation
into water quality and water quantity; climate regulation was divided
into variables related to emissions and uptakes, and crop yield into
crop yield and crop biomass. Results were robust as shown by similar
effect sizes compared to broader classification (fig. S6). The only
deviation from previous results is represented by crop biomass,
which was significantly increased under diversification regimes.
The eight effect sizes included in this category referred to both
above- and belowground biomass. This sensitivity analysis con-
firms that organisms both above- and belowground strongly re-
spond to diversification practices. The exclusion of single or multiple
diversification practices and single or multiple ecosystem service
categories did not affect our results (results not presented).
SUPPLEMENTARY MATERIALS
Supplementary material for this article is available at http://advances.sciencemag.org/cgi/
content/full/6/45/eaba1715/DC1
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Acknowledgments: We thank S. Nakagawa and A. Flöhr for comments and suggestions on
the statistical analyses. Funding: This work was financed by the Swedish research council for
sustainable development FORMAS (grant 941-2015-1792) to S.H. and R.B. Author
contributions: All authors participated in conceiving the idea and designing the study. G.T.
and T.C.W. compiled the dataset. G.T. analyzed the data and led the writing. S.H. and R.B.
supervised the manuscript preparation. All authors interpreted the results and edited the
manuscript. Competing interests: The authors declare that they have no competing interests.
Data and materials availability: All data needed to evaluate the conclusions in the paper are
present in the paper and/or the Supplementary Materials. The dataset used in this study is
available in data file S1. R script files and additional data related to this paper may be
requested from the corresponding author.
Submitted 11 November 2019
Accepted 18 September 2020
Published 4 November 2020
10.1126/sciadv.aba1715
Citation: G. Tamburini, R. Bommarco, T. C. Wanger, C. Kremen, M. G. A. van der Heijden,
M. Liebman, S. Hallin, Agricultural diversification promotes multiple ecosystem services without
compromising yield. Sci. Adv. 6, eaba1715 (2020).
on November 4, 2020http://advances.sciencemag.org/Downloaded from
Agricultural diversification promotes multiple ecosystem services without compromising yield
Liebman and Sara Hallin
Giovanni Tamburini, Riccardo Bommarco, Thomas Cherico Wanger, Claire Kremen, Marcel G. A. van der Heijden, Matt
DOI: 10.1126/sciadv.aba1715
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... Ecologically friendly, agricultural diversification, managing soil, biodiversity and weeds, without compromising yields is not wishful thinking. This was proven in a recent study by Tamburini (Swedish University of Agricultural Sciences) and a team (Tamburini et al., 2020). The group conducted an international study comparing 42,000 examples of diversified and simplified agricultural practices. ...
... The evidence is compelling that instead of monocultures, diversification can reverse the negative impacts of simplified forms of cropping on the environment. However, there is no 'one-size-fitsall' (Tamburini et al., 2020). ...
Article
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With or without humans colonizing species will always be present on earth and continue to play vital roles in stabilizing the earth's ecosystems damaged by the teeming humanity. Therefore, humans need to 'live with weeds' and utilize their colonizing power for beneficial uses. If people well understand the valuable ecological roles and biodiversity values of colonizing species, it will influence the decision-makers and help them develop better policies towards colonizing taxa. Agro-ecology helps us to appreciate the critical roles of colonizing taxa in Nature. Concepts such as 'beneficial weeds' and "middle-way path" to weed management allow us to rethink how we may engage in agriculture more sustainably. A change in thinking is required in Weed Science to recognize weeds, not as a production constraint in agriculture and a threat to farming, all the time. As colonizing species, they are significant bioresource assets. Where the abundance of weeds, at particular times and locations, present problems for other essential and valued human endeavours (such as food production) or natural ecosystems, they need to be appropriately managed. People have done this for millennia. The tools and techniques to do so, to the extent required, are well developed within Weed Science-a formidable discipline. An improved relationship with weeds will develop if they are understood as nothing but colonizing and pioneering taxa, which are adapted to respond to disturbances. Much like humans, they are just opportunistic species. Weeds are no more villainous than humans. The farmland biodiversity discourses, especially in Europe and the U.K., have awakened research communities to explore a more tolerant attitude towards beneficial weeds. Weedy species contribute pollination benefits for bees and food for other insects. Various fauna use them as food and shelter resources. Colonizing species also play critical roles in mitigating soil erosion, water retention, nutrient cycling and replenishment, improving soil health. Weedy congeners (relatives) also promote the evolutionary diversification and genes for hybridization with their crop relatives. Such positive contributions offset, at least partially, the losses to biodiversity that people allege weedy species cause. Biodiversity is too important for society to misunderstand it. Biodiversity is critically important for a healthy planet. Human survival on Planet Earth depends on properly interacting with biodiversity. This includes appreciating the crucial roles colonizing species play.
... Despite the increasing body of theoretical and experimental studies on diversification (Beillouin et al. 2019), addressing its impacts using integrated assessments remains a challenge due to broad concepts and inconsistent definitions as well as a great variety of indicators that are used on different spatial levels and that are associated with different dimensions of system sustainability (Boerema et al. 2017;Bünemann et al. 2018;Hufnagel et al. 2020). For instance, recent reviews on diversification are useful to reveal general trends based on a large database of studies (Beillouin et al. 2019;Hufnagel et al. 2020;Tamburini et al. 2020), but do not combine indicators of ecosystem services with indicators of socio-economic sustainability and resilience capacity of agroecosystems, while the latter are relevant issues for policies and farmers. The use of indicators that compose a comprehensive and systemic framework addressing the multiple components of system sustainability can help not only to align research findings with policy and societal needs, but also to better understand how and to what extent specific diversification strategies such as agroforestry can contribute to multiple aspects of agroecosystems sustainability. ...
... More diversified systems were also reported to enhance the provision of multiple ecosystem services ( Figure 5). The positive effects were especially strong for the ecosystem services: climate regulation, soil erosion control, pest control and carbon sequestration ( Figure 5), which is in line with other studies that report benefits of diversification strategies (McDaniel et al. 2014;Soto-Pinto and Armijo-Florentino 2014;Gomes et al. 2016;Dainese et al. 2019;Tamburini et al. 2020). For instance, higher plant diversity can benefit trophic interactions among insects, leading to higher presence of natural enemies and increased pest control (Wan et al. 2020). ...
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Despite the potential of diversification strategies to achieve sustainability, diversified systems such as agroforestry are still not widely implemented by farmers, which indicates the need to further understand and adequately assess the impacts of diversification to inform the design of complex systems. In this paper, we conduct a systematic literature review focused on agroforestry coffee systems, to assess (i) how current methods and indicators are used to quantify the impact of diversification on multiple dimensions of system sustainability, and (ii) to assess the impact of diversification through coffee agroforestry on multiple dimensions of sustainability. Our analysis was based on 215 selected papers and all the indicators identified could be classified in one of the sustainability dimensions proposed in our framework: ecosystem services (57.2%), biodiversity (35.6%), input use (4%), socioeconomic sustainability (2.7%) and resilience capacity (0.5%). Despite the broad scope of the indicators, individual studies were found to often lack interdisciplinarity and a systemic view on agroecosystems. Besides, not only were there few studies that included the impacts of diversification on input use, socioeconomic sustainability and resilience capacity, but specific biodiversity attributes (e.g. functional diversity, landscape diversity) and ecosystem services (e.g. soil biological quality, water regulation, pollination) were generally underreported. The impact of diversification was more positive than negative in all dimensions of sustainability, with the exception of crop productivity. Yet, diversified systems are associated with reduced costs and high yields can still be achieved in diversified systems with appropriate agricultural management (e.g. adequate number and type of shade trees). Key to reaping the benefits of diversified systems is that the diversity of elements is carefully integrated considering the impact on multiple dimensions of system sustainability. A better understanding of synergies and trade-offs remains crucial for the customized design of diverse and sustainable systems for a variety of geo-climatic conditions.
... Les zones de cultures intensives produisent majoritairement un service de production souvent au détriment des autres services écosystémiques généralement fournis par le couvert végétal classique (Rodríguez et al., 2006). Une adaptation des pratiques culturales comme la mise en place de cultures biologiques, de périodes de jachère ou de diversification des cultures permet de limiter l'impact de ces pratiques sur l'ensemble des SE et dans certains cas pourrait même permettre une amélioration du rendement des cultures Sandhu et al., 2010;Tamburini et al., 2020). Ces pratiques moins intensives permettent la fourniture par les milieux cultivés d'un jeu complet de SE comme médiation des pestes, la régulation du climat, le stockage de carbone ou encore la régulation des flux de bases et des évènements extrêmes Tamburini et al., 2020). ...
... Une adaptation des pratiques culturales comme la mise en place de cultures biologiques, de périodes de jachère ou de diversification des cultures permet de limiter l'impact de ces pratiques sur l'ensemble des SE et dans certains cas pourrait même permettre une amélioration du rendement des cultures Sandhu et al., 2010;Tamburini et al., 2020). Ces pratiques moins intensives permettent la fourniture par les milieux cultivés d'un jeu complet de SE comme médiation des pestes, la régulation du climat, le stockage de carbone ou encore la régulation des flux de bases et des évènements extrêmes Tamburini et al., 2020). Dans le cas de l'application de la méthode aHEP, nous avons considéré les SE fournis par les cultures comme identiques à ceux de milieux prairiaux. ...
Thesis
Les friches industrielles représentent de réelles opportunités pour la création d’espaces naturels mais les méthodes de restauration et d’évaluation des bénéfices environnementaux de ces opérations sont très lacunaires. L’objectif de cette thèse a été, au travers d’un cas d’étude, de palier à ce manque. Les résultats obtenus mettent en évidence que la restauration des technosols de friches industrielles nécessite une approche pluri-compartimentale (végétation et sol) et que les méthodes utilisées actuellement en restauration des sols sont moins efficaces dans des milieux aussi dégradés. Une approche pluridisciplinaire alliant outils d’évaluation économique et indicateurs écologiques a été ajustée permettant l’évaluation des bénéfices environnementaux de tels projets. Des adaptations sont cependant encore nécessaires dans la récolte de données, la sélection des indicateurs et la conception de la méthode pour garantir une meilleure prise en compte du compartiment sol, optimiser l’intégration des objectifs du projet de restauration et des potentiels impacts de la restauration sur les populations locales.
... The importance of biodiversity is confirmed by a recent paper, which reviewed 5,160 original studies comprising 41,946 comparisons between diversified and simplified practices. It showed that, overall, diversification enhances biodiversity, pollination, pest control, nutrient cycling, soil fertility, and water regulation without compromising crop yields (Tamburini et al. 2020). ...
Book
Genetic, ecological and evolutionary research, spanning over several decades, showed that cultivating diversity promotes ecosystem services and its is a viable approach for reducing environmental impact while maintaining and even increasing yields. This research showed that evolutionary populations and dynamic mixtures: a) are able to adapt their phenology to the location in which they are grown; b) evolve becoming more and more productive; c) have a more stable yield over time than uniform varieties; d) become more and more resistant to diseases; and e) control weeds better than uniform varieties. Evolutionary populations and mixtures are able to adapt to climate change and to evolve in response to biotic and abiotic stresses. They are the quickest, most cost-effective, evolving solution to such a complex and evolving problem as climate change, with the additional advantage of increasing yield gains resulting from a combination of natural and artificial selection.
... De même, le porte greffe peut influencer la tolérance de la plante à la sècheresse ( (Prieto et al., 2015 ;. Elles permettent un maintien des rendements (Tamburini et al., 2020) voire une meilleure production (Isbell et al., 2017). Elles permettent également de réduire l'impact environnemental des cultures (Gaba et al., 2015) et peuvent avoir des effets sur la biodiversité associée, la qualité de l'eau et des sols (Beillouin et al. 2021), et l'adaptation aux conditions de production locales ). ...
Technical Report
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Agroecological transition is now seen as a pathway with many opportunities to improve the sustainability and resilience of agricultural systems. Many agricultural policies and recovery plans emphasize this pathway. Agroecology, by maximizing the use of ecological processes and particularly positive interactions between plants and between plants and their abiotic or biotic environment (soil microorganisms in particular), allows the minimization of the use of synthetic inputs (fertilizers and pesticides). To achieve this, it is not enough to seek the best possible use of resources, which would lead to a "weak" agroecology, but it is also necessary to make a qualitative leap in the efficiency of input use, and to redesign low-energy production systems in order to explicitly call upon biological processes that promote soil fertility or the regulation of pests and diseases, in order to move toward a "strong" agroecology (Duru et al., 2014). The Plenary Committee of the CTPS (Permanent Technical Committee on Plant Breeding) asked the Scientific Committee of the CTPS to shed light, based on the scientific and technical literature, on what the agroecological transition implies in terms of variety species, breeding, evaluation, and seed and plant production. Needs and diversity of species, varieties, seeds and plants in an agroecology-based model As agroecology is largely based on increased crop services, it leads to a need for more species, varieties and functional diversity. Diversity can be achieved by growing varietal associations or mixtures of species, but also by arranging a greater diversity of varieties and species in space and time. Minor species, intercropping, and spring species have an important role to play in this diversification. Agroecology is characterized by the increasing dependence of varieties on local conditions. Therefore, more varieties will have to be selected and evaluated for adaptation to specific situations. There are many important traits to select and evaluate in agroecology. They include vigour, phenology, and ability for association. Other diversified traits are also to be considered (including resistance to diseases and other pests). The root compartment is little explored today. Finally, the interactions between the plant and its environment are of importance in agroecology, especially the interactions between varieties and microbiota, which are leading to a broadening of the characterisation of varieties to their holobionts. The agroecological transition multiply the goals of selection (services) and reinforce the need for access to easily modulated and adaptable diversity, which will necessarily move agriculture away from the dominant concept of homogeneity, single variety or pure variety. It may therefore be useful to select a diversity of varietal profiles that are complementary to each other, rather than seeking a very limited number of optimal profiles, and thus enable the creation of more stable and resilient variety portfolios able to make better use of resources, that fluctuate over time, and to limit the impact of occasional stresses that are difficult to predict. For example, having a variety of earliness profiles within the same plot or farm can be an interesting strategy for making the most of resources over a longer period and avoiding accidents in the event of strong and specific stresses. While the evaluation of varieties is generally multi-criteria today (the productivity of varieties is evaluated according to their quality, their resistance to certain pests, or even their production mode), the evaluation of varieties for agroecological systems implies an increase in the number of criteria to be considered. This evaluation will have to take into account all the services expected from crops (including increased soil fertility, carbon storage or the ability to regulate weeds), the diversity of possible uses of crops (including " minor " sectors), practices and growing environments, this diversity being a specificity of agroecological systems.
... One comprehensive global synthesis of 5160 original studies showed that, compared to conventional agriculture, crop diversification significantly increases above-and below-ground biodiversity by, on average, 40%, pollination by 32%, pest control by 26%, nutrient cycling by 20%, water regulation by 20% and soil fertility by 19%, while having a neutral effect on yield (Tamburini et al. 2020). Other reviews show that in diversified farms and landscapes (whether organically farmed or not), ecological outcomes improve while effects on yield vary with contextual factors but are most often higher and more stable than on simplified farms (Beillouin et al. 2019;Ponisio et al. 2015;Rosa-Schleich et al. 2019;Sirami et al. 2019). ...
Article
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Governments are updating national strategies to meet global goals on biodiversity, climate change and food systems proposed in the Convention on Biological Diversity post-2020 framework and agreed at the United Nation’s Climate Change Conference (COP26) and Food Systems Summit (UNFSS). This represents a unique and crucial opportunity to integrate and accelerate food system actions to tackle interconnected global challenges. In this context, agroecology is a game-changing approach that can provide the world’s growing population with nutritious, healthy affordable food, ensure fair incomes to farmers and halt and reverse the degradation of the natural environment. Here, we explore agroecological transition pathways in four case studies from low- and middle- income countries and identify catalysts for change. We find that enabling policy and market environments, participatory action research and local socio-technical support each plays a critical role in stimulating transitions towards agroecology. We propose strategies and priorities for research to better support agroecological transitions using these catalysts of change as entry points. Engagement of governments, private sector, civil society, farmers and farm workers in this research agenda is essential.
... Across crops, field-scale biodiversity is affected by management practices such as tillage system, pesticide use and fertilization type and intensity (Hyvönen and Salonen, 2002;Lüscher et al., 2014;Seifert et al., 2015), which are influenced, but not determined by the crop choice. In general, functional biodiversity can be enhanced through diversification practices that aim at promoting ecosystem services for high yields and reduced reliance on agrochemical inputs (Bommarco et al., 2013;Kovács-Hostyánszki et al., 2017;Tamburini et al., 2020). These practices include, for example, increased crop diversity in fields over space or time (e.g. ...
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Crop choice affects biodiversity within fields due to crop-specific characteristics and management practices. However, there is a lack of studies systematically comparing the biodiversity value of different crops across multiple taxa. This study empirically compared the diversity of plants, pollinators, predatory arthropods, and multi-taxa diversity between seven crop types and long-term environmental fallows in boreal farmland. The effects of crop production method (organic vs. conventional) on biodiversity were also examined. Biodiversity data were collected in 78 fields in Southern Finland. The studied species groups differed in their preferences for crop types and fallows, but none of them was particularly associated to spring cereal (oat), the dominant arable crop in the boreal farmland. Environmental fallows had the highest plant species richness and butterfly abundance, whereas faba bean and oilseed crop fields attracted high numbers of bumblebees. Carabid beetles were most abundant in winter cereal (rye) fields, and spiders in perennial crop types. Multi-taxa diversity was highest in fallows and lowest in spring cereal (oat), ley and cabbage fields. Organic production increased plant species richness across crop types. Hoverflies responded to the interaction of production method and crop type, being most abundant in organically managed faba bean fields. The other species groups and multi-taxa diversity were not affected by the production method. High arable land cover in the surrounding landscape had negative effect on butterflies, solitary bees and carabid beetles within fields. Our results suggest that diversifying cropping systems to include more insect-pollinated crops, winter cereals and pastures, and increasing the area of environmental fallows while maintaining landscape heterogeneity would enhance resource provision for a variety of organism groups in boreal agricultural landscapes.
... For invasive and endemic pests alike, on-farm biodiversity can be harnessed to raise pest mortality levels and curb pest-induced losses (Horrocks et al., 2020). Where relevant, judiciously selected exotic organisms can be introduced to suppress invasive pests (Wyckhuys et al., 2020b), while enhancing (field or farm-level) functional diversity can simultaneously boost pest control and crop yield (Barnes et al., 2020;Tamburini et al., 2020). Varietal resistance, habitat manipulation and semiochemicals equally fortify the resilience of agro-ecosystems (Egan and Chikoye, 2021). ...
Article
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Pests and pathogens inflict considerable losses in global agri-food production and regularly trigger the (indiscriminate) use of synthetic pesticides. In the Asia-Pacific, endemic and invasive organisms compromise crop yields, degrade farm profitability and cause undesirable social-environmental impacts. In this study, we systematically assess the thematic foci, coherence and inclusiveness of plant protection programs of 11 Asia-Pacific countries. Among 23 economically important diseases and 55 pests, survey respondents identified rice blast, rice brown planthopper, citrus greening disease, Tephritid fruit flies and fall armyworm as threats of regional allure. These organisms are thought to lower crop yields by 20–35% and cause management expenditures up to US$2,250 per hectare and year. Though decision-makers are familiar with integrated pest management (IPM), national programs are invariably skewed toward curative pesticide-intensive control. Pesticide reductions up to 50–100% are felt to be feasible and potentially can be attained through full-fledged IPM campaigns and amended policies. To rationalize farmers' pesticide use, decision criteria (e.g., economic thresholds) wait to be defined for multiple crop x pest systems and (participatory) training needs to be conducted e.g., on (pest, disease) symptom recognition or field-level scouting. Efforts are equally needed to amend stakeholder perceptions on ecologically based measures e.g., biological control. Given that several Asia–Pacific countries possess robust techno-scientific capacities in various IPM domains (e.g., taxonomy, molecular diagnostics, socioeconomics), they can take on an active role in regionally coordinated campaigns. As such, one can reinvigorate IPM and ensure that preventative, non-chemical pest management ultimately becomes the norm instead of the exception throughout the Asia–Pacific.
Article
Since the 2000s, there has been an increasing number of returning and migrant farmers across China. In 2012, China initiated a program for fostering professional farmers, which has caused greater changes for farmers and led to an agricultural shift towards commercial production. Migration has been recognized as a crucial factor affecting the diversity of agricultural production. However, scant attention has been paid to how different types of farmers influence agricultural diversification. Therefore, this study examines the influence of migrant farmers, returning farmers, and local non-migrant farmers on food production diversity. This study collected farm-level data on food production and farmers’ characteristics and applied a negative binomial regression model to estimate the impacts of different types of farmers on agricultural development. The results show that farms operated by migrant farmers had a significantly lower level of food production diversity while farms operated by returning farmers had no significant difference in food production diversity, using farms operated by local non-migrant farmers as the reference category. The variation in agricultural production diversity lies in differences in food production purposes, agricultural and market skills, and various risk-related capacities among the different types of farmers. Farm-level production specialization does not necessarily reduce food diversity and agrobiodiversity at the rural community and regional level.
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Human land use threatens global biodiversity and compromises multiple ecosystem functions critical to food production. Whether crop yield–related ecosystem services can be maintained by a few dominant species or rely on high richness remains unclear. Using a global database from 89 studies (with 1475 locations), we partition the relative importance of species richness, abundance, and dominance for pollination; biological pest control; and final yields in the context of ongoing land-use change. Pollinator and enemy richness directly supported ecosystem services in addition to and independent of abundance and dominance. Up to 50% of the negative effects of landscape simplification on ecosystem services was due to richness losses of service-providing organisms, with negative consequences for crop yields. Maintaining the biodiversity of ecosystem service providers is therefore vital to sustain the flow of key agroecosystem benefits to society.
Article
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The diversification of cropping systems encompasses different strategies that may help maintain or enhance the sustainability of agriculture. Thousands of experiments have been carried out around the world since almost five decades to evaluate and compare the performances of various diversification strategies in a wide array of agroecosystems and climates. Although these analyses have been synthesized in a growing number of meta-analyses, the information remains somewhat fragmented. A multicriteria systematic synthesis of worldwide agricultural diversification is still lacking. Here, we review all meta-analyses conducted on crop diversification strategies and produce a detailed overview of their results and of their quality. We identified and analyzed 99 meta-analyses summarizing the results of more than 3700 agronomic experiments on seven crop diversification strategies. Among these strategies, rotation and associated plant species are dominant in the literature followed by intercropping, agroforestry and landscape heterogeneity. Our analysis reveals that rotation and intercropping are associated with yield increases. Agroforestry systematically induces an improvement of biodiversity and soil quality—in particular soil organic carbon. We show that, regardless of the context, a combination of several diversification strategies outperforms any individual strategy. Our review reveals that a significant knowledge gap remains, in particular regarding water use, farmers' profitability, product quality and production stability. Few meta-analyses investigate the performance of landscape heterogeneity and of systems with species other than cereals and pulses. Additionally, we show that most of the meta-analyses studied cannot be considered fully transparent and reproducible. Their conclusions should therefore be interpreted with caution. Our systematic mapping provides a benchmark to guide and improve the relevance and reliability of future meta-analyses in agronomy.
Article
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Increasing global food demand, low grain reserves and climate change threaten the stability of food systems on national to global scales1–5. Policies to increase yields, irrigation and tolerance of crops to drought have been proposed as stability-enhancing solutions1,6,7. Here we evaluate a complementary possibility—that greater diversity of crops at the national level may increase the year-to-year stability of the total national harvest of all crops combined. We test this crop diversity–stability hypothesis using 5 decades of data on annual yields of 176 crop species in 91 nations. We find that greater effective diversity of crops at the national level is associated with increased temporal stability of total national harvest. Crop diversity has stabilizing effects that are similar in magnitude to the observed destabilizing effects of variability in precipitation. This greater stability reflects markedly lower frequencies of years with sharp harvest losses. Diversity effects remained robust after statistically controlling for irrigation, fertilization, precipitation, temperature and other variables, and are consistent with the variance-scaling characteristics of individual crops required by theory8,9 for diversity to lead to stability. Ensuring stable food supplies is a challenge that will probably require multiple solutions. Our results suggest that increasing national effective crop diversity may be an additional way to address this challenge.
Article
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The eighteenth-century Malthusian prediction of population growth outstripping food production has not yet come to bear. Unprecedented agricultural land expansions since 1700, and technological innovations that began in the 1930s, have enabled more calorie production per capita than was ever available before in history. This remarkable success, however, has come at a great cost. Agriculture is a major cause of global environmental degradation. Malnutrition persists among large sections of the population, and a new epidemic of obesity is on the rise. We review both the successes and failures of the global food system, addressing ongoing debates on pathways to environmental health and food security. To deal with these challenges, a new coordinated research program blending modern breeding with agroecological methods is needed. We call on plant biologists to lead this effort and help steer humanity toward a safe operating space for agriculture. Expected final online publication date for the Annual Review of Plant Biology Volume 69 is April 29, 2018. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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International initiatives such as the ‘4 per 1000’ are promoting enhanced carbon (C) sequestration in agricultural soils as a way to mitigate greenhouse gas emissions¹. However, changes in soil organic C turnover feed back into the nitrogen (N) cycle², meaning that variation in soil nitrous oxide (N2O) emissions may offset or enhance C sequestration actions³. Here we use a biogeochemistry model on approximately 8,000 soil sampling locations in the European Union⁴ to quantify the net CO2 equivalent (CO2e) fluxes associated with representative C-mitigating agricultural practices. Practices based on integrated crop residue retention and lower soil disturbance are found to not increase N2O emissions as long as C accumulation continues (until around 2040), thereafter leading to a moderate C sequestration offset mostly below 47% by 2100. The introduction of N-fixing cover crops allowed higher C accumulation over the initial 20 years, but this gain was progressively offset by higher N2O emissions over time. By 2060, around half of the sites became a net source of greenhouse gases. We conclude that significant CO2 mitigation can be achieved in the initial 20–30 years of any C management scheme, but after that N inputs should be controlled through appropriate management.
Article
This article discusses the economic dimensions of agroecological farming systems in Europe. It firstly theoretically elaborates the reasons why, and under what conditions, agroecological farming systems have the potential to produce higher incomes than farms that follow the conventional logic. This theoretical exposition is then followed by a presentation of empirical material from a wide range of European countries that shows the extent to which this potential is being realized. The empirical data draw upon different styles of farming that can be described as ‘proto-agroecological’: approaches to farming that are agroecological by nature, but which may not necessarily explicitly define themselves as agroecological. The empirical material that we present shows the huge potential and radical opportunities that Europe's, often silent, ‘agroecological turn’ offers to farmers that could (and should) be the basis for the future transformation of European agricultural policies, since agroecology not only allows for more sustainable production of healthier food but also considerably improves farmers' incomes. It equally carries the promise of re-enlarging productive agricultural (and related) employment and increasing the total income generated by the agricultural sector, at both regional and national levels. While we recognise that agroecology is a worldwide and multidimensional phenomenon we have chosen to limit this analysis to Europe and the economic dimension. This choice is made in order to refute current discourses that represent agroecology as unproductive and unprofitable and an option that would require massive subsidies.
Article
Diversified Farming (DF) Systems aim to integrate ecological and economic benefits for sustainable agriculture. DF systems can enhance ecological benefits at the farm level and therewith reduce negative environmental externalities. However, diversification may cause economic costs for the farmer. Although considering ecological-economic trade-offs is crucial for integrating biodiversity into agricultural production, ecological and economic benefits of DF practices have rarely been analyzed conjointly. Here, we synthesize published evidence provided by reviews and meta-analyses that evaluate the ecological and economic performance of single DF practices and more complex diversification bundles. Compared to non-diversified farming, DF practices provide substantially greater biodiversity and associated ecosystem services, such as pest and weed control, soil health, nutrient and water management and carbon sequestration. Overall, the ecological benefits for the farmer were partly insufficient to outbalance economic costs in the short term, even though many examples showed that DF practices have the potential to lead to higher and more stable yields, increase profitability and reduce risks in the long-term. Combined DF practices deliver highest ecological and economic benefits on the farm level. Financial instruments are needed to increase the implementation of combined DF practices to adequately reward for the ecological benefits on the farm level.
Article
There is worldwide concern about the environmental costs of conventional intensification of agriculture. Growing evidence suggests that ecological intensification of mainstream farming can safeguard food production, with accompanying environmental benefits; however, the approach is rarely adopted by farmers. Our review of the evidence for replacing external inputs with ecosystem services shows that scientists tend to focus on processes (e.g., pollination) rather than outcomes (e.g., profits), and express benefits at spatio-temporal scales that are not always relevant to farmers. This results in mismatches in perceived benefits of ecological intensification between scientists and farmers, which hinders its uptake. We provide recommendations for overcoming these mismatches and highlight important additional factors driving uptake of nature-based management practices, such as social acceptability of farming.
Article
Meta-analysis is the quantitative, scientific synthesis of research results. Since the term and modern approaches to research synthesis were first introduced in the 1970s, meta-analysis has had a revolutionary effect in many scientific fields, helping to establish evidence-based practice and to resolve seemingly contradictory research outcomes. At the same time, its implementation has engendered criticism and controversy, in some cases general and others specific to particular disciplines. Here we take the opportunity provided by the recent fortieth anniversary of meta-analysis to reflect on the accomplishments, limitations, recent advances and directions for future developments in the field of research synthesis.