sustainability

Review
What Agriculture Can Learn from Native Ecosystems
in Building Soil Organic Matter: A Review
Timothy E. Crews 1, * and Brian E. Rumsey 2
1 The Land Institute, 2440 E. Water Well Rd., Salina, KS 67401, USA
2 Environmental History, University of Kansas, 3650 Wescoe Hall, Lawrence, KS 66045, USA;
brian.rumsey@gmail.com
* Correspondence: crews@landinstitute.org; Tel.: +1-785-823-5376

Academic Editor: Tiziano Gomiero

Received: 30 December 2016; Accepted: 7 April 2017; Published: 11 April 2017

Abstract: Over the last century, researchers and practitioners with diverse backgrounds have
articulated the importance of improving soil organic matter (SOM) contents in agricultural soils.
More recently, climate change scientists interested in CO2 sinks, and agroecologists interested
in ecological intensification have converged on the goal of building SOM stocks in croplands.
The challenge is that agriculture itself is responsible for dramatic losses of SOM. When grassland
or forest ecosystems are first converted to agriculture, multiple mechanisms result in SOM declines
of between 20% and 70%. Two of the most important mechanisms are the reduction in organic
matter inputs from roots following the replacement of perennial vegetation with annual crop species,
and increases in microbial respiration when tillage breaks open soil aggregates exposing previously
protected organic matter. Many agricultural practices such as conservation tillage and integration of
cover crops have been shown to achieve some degree of SOM improvement, but in general adoption
of these practices falls short of accumulating the SOM stocks maintained by grasslands, forests or
other native ecosystems that agriculture replaced. Two of the overarching reasons why native
terrestrial ecosystems have achieved greater soil organic matter levels than human agroecosystems
are because they direct a greater percentage of productivity belowground in perennial roots, and they
do not require frequent soil disturbance. A growing body of research including that presented in this
review suggests that developing perennial grain agroecosystems may hold the greatest promise for
agriculture to approach the SOM levels that accumulate in native ecosystems. We present calculations
that estimate potential soil organic carbon accumulation rates in fields converted from annual to
perennial grains of between 0.13 and 1.70 t ha−1 year−1 .

Keywords: annual; carbon; ecological intensification; microbial respiration; native ecosystem;

perennial; soil organic matter; tillage

1. Introduction
Soils play a central role in the global carbon cycle, storing two to three times as much carbon in
organic forms as there is carbon in the atmosphere [1,2]. Changes in land use and land cover rank
second behind the combustion of fossil fuels as the most important anthropogenic sources responsible
for increasing atmospheric CO2 concentrations [3]. Agriculture in particular has been responsible for
somewhere in the range of 50–78 Pg of C loss to the atmosphere [4,5] This transfer of C represents
about 3.8% of global median estimates for total soil organic carbon (SOC) in terrestrial ecosystems [1],
and it represents about 5.5 years of global CO2 emissions from fossil fuels at 2014 rates [6].
There is considerable interest by climate change scientists in reversing the transfer of carbon from
soils to atmosphere [7]. There is also a great deal of interest from agricultural scientists in this reversal
since the carbon losses from soils originated primarily from the depletion of soil organic matter (SOM)

Sustainability 2017, 9, 578; doi:10.3390/su9040578 www.mdpi.com/journal/sustainability

Sustainability 2017, 9, 578 2 of 18

stocks [8]. In this paper we will discuss SOM, which is 58% carbon, but also includes oxygen, hydrogen,
nitrogen, phosphorus, sulfur and other elements in simple and complex molecules [9]. In some cases,
however, we will refer to SOC, especially when discussing sequestration of atmospheric carbon in
agricultural soils.
Numerous approaches have been suggested for how to re-accumulate in SOM the carbon that
has been lost over time from soils to the atmosphere [7,10,11]. To assess the potential SOM-building
potential of different approaches, it is important to understand the mechanisms driving the depletion
of SOM following the conversion of native ecosystems to agriculture. McLauchlan [8] lists three
mechanisms of agricultural reduction in SOM:

1. The quantity of C inputs to soil are reduced in annual cropping systems compared to perennial
native vegetation.
2. The physical disturbance of tillage increases SOM decomposition rates. It does this in part by
destroying aggregates and physical structure, exposing previously physically protected SOM
to decomposition.
3. Tillage and lack of plant cover on agricultural fields enable soil erosion to occur which can remove
large quantities of SOM.

Based on McLauchlan’s three mechanisms of SOM reduction by agriculture, it follows that the
native ecosystems preceding agriculture generally maintained relatively high quantities of C inputs
into soils, experienced low levels of soil disturbance and maintained year-round vegetative cover
which protected against erosion.
In this review, we will consider proposed changes in agricultural management that have received
the greatest attention for their potential to decrease atmospheric CO2 by increasing SOM stocks.
The review is not intended to be an exhaustive evaluation of each different approach. Rather, we will
explore further the mechanisms by which agriculture causes reductions in SOM compared to native
ecosystems, and we will consider the extent to which different strategies for re-building SOM reverse
these mechanisms.

1.1. Background
Given our current understanding of how organic matter is lost from soils following disturbances
such as tillage, it is safe to suggest that grain agriculture has been responsible for the degradation
of soil through loss of organic matter since its inception [8,12–14]. As we will discuss below,
the acts of disturbing soil through digging or tillage, coupled with the replacement of perennial
vegetation with annual crops, have consistently resulted in SOM depletion [8,14–16]. Nevertheless,
almost all traditional, indigenous farmers were, knowingly or not, careful managers of SOM,
as fertility-generating cover crop rotations, pasture or shrub fallows, and applications of farmyard
manure were essential to maintaining fertility [17,18].
The advent and widespread adoption of synthetic fertilizers in the 20th century allowed farmers
to reduce their intensive management of soil organic matter. No longer was it necessary to laboriously
haul manure from farmstead to fields, or tie up land that could be producing commercial crops
with fertility-building cover crops or pasture rotations. It did not take long before critiques of
industrial agriculture were published, such as Sir Albert Howard’s An Agricultural Testament in
1940 [19] identifying neglect of SOM as a serious mistake. Neglecting SOM translated into reduced
nutrient supply, water holding capacity, disease resistance, soil structure, and greater soil erosion [9,19].
Since Howard’s time, the goal to improve the organic matter content in croplands has been central to
almost every reformist or alternative approach to the industrial model [20–23].
In recent decades, the research community’s most common impetus for improving SOM has
not been the improvement of agroecosystem functioning but rather the transfer of carbon from
CO2 in the atmosphere to stable forms of organic matter in the soil. Since highly industrialized
countries are far from reducing dependency on fossil fuel energy sources, researchers have been
Sustainability 2017, 9, 578 3 of 18

looking for CO2 sinks to help mitigate anthropogenic greenhouse gas increases [7]. Numerous land
management opportunities to sequester carbon have been assessed [8] and global sequestration values
of 0.6–1.2 Pg year−1 or a cumulative cropland sink capacity of 30–60 Pg in the next 50 to 90 years
bracket what many researchers think is possible [9,10].
Critics of targeting soil carbon to mitigate climate change point out that the total global
sequestration potential represents a small percentage of anthropogenic emissions projected by
IPCC models [24]. A recent comprehensive study drawing on field experiments in North America,
Europe and Asia suggests that climate warming could drive the loss of 55 Pg of carbon from upper
soil horizons by 2050, predominantly in arctic and subarctic regions [25]. Thus very aggressive efforts
to sequester C in SOM on farms may be counterbalanced by loses of SOM in tundra for decades
to come. But regardless of the role that farm management might play in the global carbon balance,
improvements in cropland SOM status would profoundly influence food security, especially in less
affluent countries [26].

1.2. SOM and Ecological Intensification

The challenge of feeding over nine billion people while minimizing negative impacts to
soils, water bodies and biodiversity has led many researchers to embrace the idea of ecological
intensification [27,28]. In the twentieth century, agricultural productivity per area of land and per
worker increased substantially in industrialized and many developing countries due to input
intensification in the forms of synthetic fertilizers, pesticides and irrigation [29]. While hugely
successful at increasing yields, input intensification is widely seen as being too costly—economically,
socially and environmentally—to maintain or further increase food production in the twenty first
century [29,30].
Ecological intensification—supplanting the need for purchased inputs with ecological processes
that come about through more sophisticated agroecological design—has been proposed as
an alternative to input intensification [31,32]. As with terms such as sustainable, organic, and biological
that preceded it, ecological intensification has been used to describe a wide range of practices.
The original definition put forth by Cassman [27] focused predominantly on achieving high levels
of resource use efficiency and closing yield gaps through the deployment of technologies such
as variable rate fertilizer application or sprinkler irrigation. Since Cassman’s original paper,
researchers have tapped the discipline of community ecology to identify processes that occur broadly
in native ecosystems that have the potential to improve agroecosystem functions. For example,
community ecologists’ understanding of the relationships between plant diversity and insect or
pathogen populations has been successfully applied to the control of agricultural pests [33,34].
SOM has also received a great deal of attention by those working on ecological intensification of
agriculture because of its multi-faceted influence on crop production [23,33]. SOM is widely known to
positively affect soil fertility and nutrient supplying capacity, soil structure, water holding capacity,
disease suppression and the functioning of the soil microbiome [35]. Yet in spite of the pivotal role
of SOM in ecological intensification, most work to date recommends changes in farm management
that fall short of achieving SOM levels of the native ecosystems that preceded agriculture (Table 1).
Why the shortfall? We suggest there are areas of ecology that help explain the answer, but have
not been applied to agriculture [36]. In the same way the sub-discipline of community ecology
sheds light on the management of pest dynamics in agroecosystems, the sub-discipline of ecosystem
ecology provides insight into SOM dynamics. For example, the process of how newly developing soils
(primary succession) or recently disturbed soils (secondary succession) accumulate SOM has been
studied a great deal, and is directly relevant to improving agriculture.
Sustainability 2017, 9, 578 4 of 18

Table 1. Mean stocks of soil organic matter of major ecosystem types.

Ecosystem Type kg SOM m−2

Tropical forest 17.9
Temperate forest 20.3
Boreal forest 25.7
Woodland and shrubland 11.9
Tropical savanna 6.4
Temperate grassland 33.1
Tundra and alpine 37.2
Desert scrub 9.7
Values derived from Schlesinger [37].

Simply viewed, SOM contents of a soil represents differential rates of organic matter inputs
and losses [38]. Inputs ultimately come from photosynthesis, and in most ecosystems originate from
plants’ roots and shoots growing and senescing on site. Plants are also responsible for supplying
organic matter to soils through symbioses with mycorrhizal fungi [39]. When plants and associated
mycorrhizae die and senesce, the residues are consumed by microbes, which in turn feed a larger food
web of microbes and micro-animals. With time, the belowground food web results in the accumulation
of “necromass” or organic matter comprised to a large extent of microbial tissues that stably bind
to soil particles and resist further decomposition (Figure 1) [40,41]. As plant matter, fungi, bacteria,
nematodes and other members of the soil food web are consumed, carbon-based compounds are
mineralized and released mostly in the form of CO2 to the atmosphere. Surface SOM can also be lost
via selective erosion when slopes are steep or soils are exposed by tillage or herbicides, even on gently
sloping ground [4,8].
A wide range of organic compounds fall into the category of SOM. For many years,
SOM decomposition models emphasized the relative susceptibility of different types of molecules
to microbial attack (e.g., cellulose, humus) as a primary governing factor regulating SOM steady
state dynamics [40,42,43]. Recently this view has been challenged with evidence that environmental
conditions (including the physio-chemical “protection” of organic compounds from microbes and other
organisms in soil aggregates) are at least if not more important than SOM recalcitrance at regulating
rates of decomposition [40,43,44]. That deserts, grasslands, tundra and rainforests accumulate
different amounts of SOM reflects the differential responses of producers (plants) and consumers
(microbes, microfauna, arthropods) to environmental conditions. Temperature and precipitation have
strong but slightly different influences on the activities of both producers and consumers while soil
textural class has greater influence on microbial activity [40]. The SOM levels in tundra and desert
ecosystems illustrate how producers and consumers respond differently to climate. Net primary
productivity of deserts and tundra is similarly low, about 250 and 180 g C m−2 y−1 , respectively [45],
while mature tundra ecosystems accrue almost four times the average SOM as deserts (21.6 vs.
5.6 kg C m−2 , respectively) [37]. Microbial activity is more responsive to the increases in temperature
than plant productivity, resulting in a smaller pool of SOM in deserts [35]. At a finer grain scale,
plant physiognomy, tissue quality and microbial community composition also interact to influence
SOM pool sizes and turnover rates [41,46].
Whether an ecosystem at steady state maintains on average 192 t SOM ha−1 such as a temperate
grassland, or on average 37 t ha−1 as in tropical savannas [37], the conversion of native ecosystems to
annual crop agriculture has the universal effect of reducing SOM levels by 20–70% [15,16]. This decline
in SOM is attributable to changes in both producer and consumer activities. When native vegetation is
replaced with annual crops, net primary productivity frequently declines [47]. But even when total
net primary productivity (NPP) does not decline, the replacement of perennial life-forms with annual
crops results in a decrease in allocation of productivity belowground (BNPP) from ~67% to between
13% and 30% [48,49]. There is growing consensus that root turnover and exudates comprise the most
Sustainability 2017, 9, 578 5 of 18

important source of plant inputs for SOM formation [43]. Therefore the change in allocation patterns
Sustainability 2017, 9, 578 5 of 17
of producers is one explanation for why SOM declines in annual crop agriculture [8,14,50].

Figure 1. Schematic
Schematic overview
overview of of soil
soil aggregate
aggregate formation
formation and and breakdown processes and their effects
on particulate organic matter structure and size. The width of the arrows arrows shows the rate of particulate
particulate
C transfer
transferbetween
betweenpools,pools,asaswell
wellasas
the potential
the potentialforfor
COCO 2 loss during
2 loss the transition.
during the transition.1. Plant litter (e.g.,
1. Plant litter
sloughed roots)roots)
(e.g., sloughed entering the soil
entering thebecomes colonized
soil becomes by bacterial
colonized communities
by bacterial and fungi
communities andand fungibegins
and
to become
begins coated with
to become coated clay particles.
with 2. Macroaggregates
clay particles; (>250 µm)
2. Macroaggregates form
(>250 µm)withformparticulate organic
with particulate
organic(POM)
matter matterin(POM) in their
their core. core;
3. In 3. In ecosystems
ecosystems that are repeatedly
that are repeatedly disturbed disturbed (e.g.,mining,
(e.g., tillage, tillage, mining,
annual
annual cropping)
cropping) macroaggregates
macroaggregates are rapidly
are rapidly destroyed
destroyed and the and the intensely
intensely disturbed
disturbed aggregates
aggregates persistpersist
and
and POM
POM oxidation
oxidation proceeds
proceeds substantially
substantially slower;
slower. 4. Free
4. Free (inter-aggregate)POM
(inter-aggregate) POMcontinues
continuesto tobeberapidly
rapidly
broken down
down to to smaller
smallersizes
sizesinindisturbed
disturbedsystems;
systems;ininless
lessdisturbed
disturbedsystems
systems such
such asasperennial
perennial crops
cropsor
no-till, POM is incorporated into very small aggregates within the macroaggregate,
or no-till, POM is incorporated into very small aggregates within the macroaggregate, further further contributing
to its physicaltoprotection;
contributing its physical5.protection;
Eventually,5.some POM Csome
Eventually, will become
POM C mineral-associated. In disturbed
will become mineral-associated.
ecosystems
In disturbedPOM breakdown,
ecosystems POM loss, and transfer
breakdown, to mineral
loss, and transfer fractions occurs
to mineral very rapidly
fractions and in
occurs very these
rapidly
systems
and POMsystems
in these structure POMhas structure
a younger, more
has plant-like
a younger, molecular
more signature
plant-like which
molecular is dominated
signature which by is
the structure of plant inputs. In ecosystems with minimal disturbance, particulate
dominated by the structure of plant inputs. In ecosystems with minimal disturbance, particulate C C with a molecular
signature
with of older,
a molecular partially
signature of decomposed
older, partiallyCdecomposed
accumulatesCin macroaggregates
accumulates and in the smaller
in macroaggregates and in
aggregates
the smaller therein
aggregates(figure and caption
therein fromcaption
(figure and Grandy andGrandy
from Neff [8]).and Neff [8]).

The
The second
secondexplanation
explanationforforSOM
SOM decline is that
decline microbial
is that accessaccess
microbial to SOM to increases with tillage,
SOM increases with
as soil aggregates
tillage, are broken
as soil aggregates areopen,
broken exposing
open, previously protected organic
exposing previously protectedmatter (Figure
organic matter1)
[11,14,43,51,52]. As a result, carbon losses through microbial respiration increase and
(Figure 1) [11,14,43,51,52]. As a result, carbon losses through microbial respiration increase and nutrients such
as nitrogen
nutrients andas phosphorus
such nitrogen andare mineralized.
phosphorus are Thus in the conversion
mineralized. Thus in theofconversion
native to of agricultural
native to
ecosystems,
agricultural inputs of organic
ecosystems, inputsmatter into the
of organic soil into
matter system
the are
soil reduced,
system areand losses of
reduced, andsoil carbon
losses via
of soil
microbial respiration are increased. In combination, these processes often result in
carbon via microbial respiration are increased. In combination, these processes often result in decadesdecades of a
negative net carbon
of a negative balance
net carbon and and
balance substantial associated
substantial declines
associated in SOM
declines in SOMstocks [16,36].
stocks [16,36].

2. Approaches
Approaches to Rebuilding SOM in Croplands
Due to tillage,
tillage, croplands are estimated to have lost somewhere in the range of 50–78 Pg of carbon carbon
globally [4,53]. This
This figure
figure is important
important because the amount of C that that has
has been
been lost
lost also
also represents
represents the
likely maximum level of sustainable accumulation that can theoretically be achieved with changes in
management.
management. However,
However, LalLal [54]
[54] raises
raises the point that many lands have degraded substantially over
the time they have been farmed, especially through soil erosion. He speculates that these degraded
soils may
mayonly
onlybebeableable to re-capture
to re-capture 50–66%50–66% of thethey
of the SOM SOM they contained
contained before agricultural
before agricultural conversion.
conversion. Others suggest that more than 90% of original SOM could be re-captured [55]. As
discussed above, numerous approaches to re-carbonize soils are receiving research attention, and
almost all rely on an underlying mechanism that addresses the producer-consumer (plant-microbe)
steady state.
Sustainability 2017, 9, 578 6 of 18

Others suggest that more than 90% of original SOM could be re-captured [55]. As discussed above,
numerous approaches to re-carbonize soils are receiving research attention, and almost all rely on
an underlying mechanism that addresses the producer-consumer (plant-microbe) steady state.

2.1. Reducing SOM Losses from Microbial Respiration

Tillage reduction, and especially tillage elimination (no-till), are among the most commonly
implemented practices that may increase carbon sequestration, though recent research and commentary
has called their effectiveness
Sustainability 2017, 9, 578 into question [56,57]. Tillage reduction and elimination are primarily
6 of 17

practiced for 2.1.

other reasons
Reducing SOM than carbon
Losses from sequestration,
Microbial Respiration including reductions in labor requirements and
erosion. The mechanism
Tillage reduction, and especially tillage eliminationcarbon
by which they may promote (no-till), sequestration—reduced
are among the most commonly disturbance
of physio-chemically
implemented protected
practices that SOM—is straightforward
may increase (Figurethough
carbon sequestration, 2). However, comparative
recent research and studies
commentary has called their effectiveness into question [56,57]. Tillage
between till and no-till systems have been confounded by the fact that carbon distribution in soil reduction and elimination are
primarily practiced for other reasons than carbon sequestration, including reductions in labor
profiles begins to change
requirements anddramatically as soonbyaswhich
erosion. The mechanism tillagetheyismayinitiated
promoteor discontinued.
carbon sequestration—For example,
some studiesreduced
have disturbance
found that no-till management
of physio-chemically protectedcanSOM—isincrease carbon(Figure
straightforward levels2).near the soil surface,
However,
comparative studies between till and no-till systems have been confounded
but will lower levels of SOC at greater soil depths [50,58]. In a review of research on no-till and C by the fact that carbon
distribution in soil profiles begins to change dramatically as soon as tillage is initiated or
sequestrationdiscontinued.
in Canada,For VandenBygaart
example, some studies and colleagues
have found that [59] examined
no-till managementthe can
results of almost
increase carbon 100 studies
of sequestration rates.
levels near When
the soil these
surface, but willdata
lower were
levelssorted
of SOC atby sampling
greater depth,
soil depths [50,58]. as
In a done
review by of Baker and
research
colleagues [50], theon no-tillthat
trials and Csampled
sequestration to in30Canada,
cm orVandenBygaart
less reported andancolleagues
average [59]Cexamined the
accumulation rate of
results −of1almost 100 studies of sequestration rates. When these data were sorted by sampling depth,
0.38 t C ha−1asyear . However, for the trials that sampled to depths greater
done by Baker and colleagues [50], the trials that sampled to 30 cm or less reported an average C than 30 cm, the average
was a loss ofaccumulation
0.23 t C harate −1 of year −1 In−1 ayear
0.38 t C. ha 28-year study
−1. However, in Indiana,
for the Gal and
trials that sampled colleagues
to depths [60] found that
greater than
no-till soil C accumulation was over twice ha
30 cm, the average was a loss of 0.23 t C −1 year−1. In a 28-year study in Indiana, Gal and colleagues
as high when measured to 30 cm than when measured to
[60] found that no-till soil C accumulation was over twice as high when measured to 30 cm than when
1 m soil depth.
measured to 1 m soil depth.

Figure 2. Schematic overview of how crop inputs and microbial mineralization interact to influence
Figure 2. Schematic
SOM stocks.overview ofrepresent
Gray squares how crop crop inputs
allocationand microbial
of organic mineralization
matter inputs belowground. interact
The larger to influence
SOM stocks. square
Gray of squares represent
perennial crop allocation
grains (1) reflects of organic
greater belowground matter
allocation inputs
to roots belowground.
compared to annual The larger
grains (2–4).
square of perennial The larger
grains (1) outer square
reflects on the far
greater right (4) reflects allocation
belowground greater organic tomatter
rootsinputs when
compared to annual
annual crop biomass (inner square) is enhanced with addition organic matter inputs from crop
grains (2–4). residues,
The larger outer square on the far right (4) reflects greater organic matter inputs when
cover crops, double cropping or imports of manures or composts from off-site. The grey zig-
annual crop biomass (inner square)
zag lines represent is enhanced
net microbial with of
mineralization addition organic
organic matter matter
inputs. The inputs from crop residues,
double zig-zags
cover crops, represent
doubleenhanced
cropping net microbial
or imports mineralization
of manures associated with the destruction
or composts of soil aggregates
from off-site. The grey zig-zag
caused by tillage. The brown circles represent relative size of SOM pools maintained once the
lines represent net microbial mineralization of organic matter inputs. The double
producers (crops) and consumers [soil microbes and other organisms] approach a steady state.
zig-zags represent
enhanced net microbial mineralization associated with the destruction of soil aggregates caused by
tillage. The brown circles represent relative size of SOM pools maintained once the producers (crops)
and consumers [soil microbes and other organisms] approach a steady state.
Sustainability 2017, 9, 578 7 of 18

Syswerda and colleagues [61] found that no-till agriculture led to an average SOC accumulation
rate of 0.33 t C ha−1 year−1 to 1 m soil depth, but noted that higher variability in SOC at greater
depths can make meaningful measurements difficult. Kravchenko and Robertson [62] used the study
by Syswerda and colleagues [61], to support the argument that the natural variability of carbon
stocks in soils is so great that most studies that have failed to see whole profile treatment differences
between tilled and no-till management have lacked adequate replication to make defensible statistical
comparisons. Baker and colleagues [50] reviewed evidence that reduced tillage reduces root growth,
and therefore carbon deposition, at greater depths. They contend that root growth is inhibited by
lower temperatures, greater resistance to penetration, higher bulk density, and a lower proportion
of aggregates less than 5 mm. Some evidence suggests that any benefits from elimination of tillage
may not accrue for several years. Six and colleagues [63] found that while cessation of tillage led to
immediate increases in SOC levels in humid climates, it did not begin to increase for more than ten
years, on average, in dry climates. While researchers continue to debate the extent of C sequestration
attributable to no-till conversion, it makes good theoretical sense that no-till should increase SOM
levels over tilled systems at least in silt or clay textured soils given the reduction in soil disturbance
and increased protection from microbial attack [14] (Figure 1). That said, the maximum C sequestration
achievable in no-till is expected to fall below that of native perennial ecosystems given the lower
belowground allocation of annual crops (Figure 2).

2.2. Increasing SOM by Increasing Crop Inputs

In contrast to no-till, which has the potential to increase SOM by reducing net microbial
mineralization relative to tilled systems, several management approaches have the potential to improve
SOM stocks by increasing plant inputs (Figure 2). Historically, crop residues have been removed
from fields for animal fodder or eliminated by burning. More recently there has been interest in
using residues as biofuels. Leaving and incorporating crop residues in fields may help build SOM,
but to what extent is unclear. Reviewing 25 experiments from Europe, North America and Australia,
Powlson and colleagues [64] found that annual cereal straw incorporations into soil led to some
increases in SOC levels, but that the increases were frequently insignificant. In contrast, Blanco-Canqui
found significant declines in SOC with the removal of corn stover, regardless of tillage or cropping
system [65].
Another approach to increase organic matter inputs is for farmers to replace periods of bare fallow
with secondary or cover crops. In a review of green-manure cover crops covering 139 plots at 37 sites,
Poeplau and Don [66] found an average sequestration rate of 0.32 t C ha−1 year−1 . West and Post [67]
reported that in wheat-fallow rotations, adding a second planting of wheat, reducing fallow but not
increasing diversity, led to an average accumulation of 0.06 t C ha−1 year−1 . Planting a different crop
(sunflower or legume) in place of the fallow led to a relative increase of 0.51 t C ha−1 year−1 [67].
Soil carbon that is more deeply buried has been shown to be less vulnerable to decomposition [68].
Modern crop breeding has paid little attention to root depth, favoring instead increased yield and ease
of harvest [69,70]. While the root depths of most cultivated crop plants are 1 m or less, there are several
that could potentially be bred for roots to 2 m depth [69,70]. Crop breeding work to increase allocation
to roots in annual species is just underway so there are few C accumulation data to report. However,
Kell posits that crop plants bred for deeper roots could sequester 50 t C ha−1 over an unspecificed
amount of time [69]. This is an optimistic calculation, using the total amount of carbon lost via
agricultural practices as a lower limit for potential sequestration. Besides C accumulation, deeper roots
would also likely provide access to more water and nutrients. However, if aboveground net primary
productivity stays constant, total crop productivity may decline if a larger fraction of plant productivity
is allocated to root production.
Sustainability 2017, 9, 578 8 of 18

2.3. Increasing SOM by Increasing Off-Farm Inputs of Organic Matter

SOM can be increased via additions of off-site inputs such as manure and composted plant
matter [11]. Composted plant matter and manure have long been added to croplands to maintain
fertility e.g., [71], and while they usually increase SOM where they are applied in the short term,
long term improvements without repeated applications are less likely. Increasing SOM through the
application of amendments in one ecosystem typically results in a reduction of SOM where the organic
matter was originally produced [72]. This is perfectly fine if the goal is to subsidize the fertility of
a farm, but not helpful if the goal is net sequestration of atmospheric CO2 . Exceptions may exist
where applications of composted materials prevent the disposal of organic wastes in landfills or
slurry ponds, thus avoiding the production of more potent greenhouse gases methane and nitrous
oxide [73]. The addition of composted materials to croplands will increase SOM on those lands directly,
and often indirectly by increasing crop productivity and associated belowground inputs of organic
matter. However, once additions of compost are discontinued, the soils will be expected to experience
greater loses of carbon through microbial respiration than gains in carbon through crop production,
eventually reaching a steady state similar to what existed before compost was first applied.
Biochar offers a potential exception to the carbon-equilibrium “rule” in which SOM accumulation
is limited by a site-specific relationship between plant production inputs and microbial respiration
loses. Biochar is a compound produced by the partial combustion of organic matter under low oxygen
conditions; a process called pyrolysis. It is highly recalcitrant, leading to a good deal of recent attention
to its potential for sequestering carbon in soils. Recalcitrant C is especially attractive for sequestration
because if applied to soils at levels above their C equilibrium points, it is expected to persist longer by
simple virtue of its resistance to decomposition. Biochar does not occur naturally in large quantities,
and to produce quantities that could offer significant levels of soil carbon sequestration, large amounts
of biomass must be converted into biochar and then applied to soils. Woolf and colleagues [74]
estimate that biochar can potentially offset up to 1.8 Pg C equivalent per year, globally, with half of that
number (0.9 Pg) in the form of carbon sequestered in soil, while using biomass at sustainable levels.
Other fractions of the 1.8 Pg are replacement of fossil fuels by pyrolysis energy (30%) and avoided
emissions of CH4 and N2 O (20%).
Aside from soil carbon sequestration, the main selling point of biochar is its potential to improve
soil tilth and nutrient retention. These benefits are of greatest value in highly weathered soils that occur
mainly in the tropics and sub-tropics. Indeed, biochar is thought to have first been used by indigenous
Amazonian peoples who cultivated highly weathered Ultisols and Oxisols [75,76]. Biochar’s nutrient
content is variable but typically low [76], and since it does not decompose readily, it does not offer
the same level of fertility enhancement as composts or manures. While the extent of cropland that
could be theoretically treated with biochar is almost unlimited [11], the energy required to harvest and
transport biomass coupled with the practicality of producing and distributing the amendment could
significantly limit the land area that receives biochar applications.

3. Perennials Address the Root of the Problem

Crews and colleagues [36] suggest that the agriculture with the greatest potential to re-capture
the SOM of the native ecosystem that preceded it is the one that most closely resembles the native
ecosystem in structure and function. They further suggest that the two features that most dramatically
distinguish the structure of native ecosystems from agricultural ecosystems is that the former is
dominated by perennial, often highly diverse communities, while the latter is dominated by annual,
often low diversity communities. Higher belowground allocation of carbon resources, and reduced soil
disturbance promote the accumulation of SOM in perennial-based ecosystems up to an equilibrium
determined by climate, soil texture and plant tissue chemistry [77]. Studies of soil development
following grassland restoration and the establishment of perennial bioenergy crops have measured soil
C accumulation rates of 0.33–0.96 and 1.09–1.88 t C ha−1 year−1 , respectively (Table 1). Paustian and
colleagues [11] estimate that on the order of 100 million ha of degraded lands could theoretically be
Sustainability 2017, 9, 578 9 of 18

planted to perennial grassland or bioenergy species due to marginal productivity or poor suitability as
cropland. If perennial grain crops were developed to replace annual grain species, the area that could
be planted to perennials today would expand to over one billion hectares [78].
The development of new perennial crop species, while a multi-decadal proposition, is gaining
momentum as a promising approach to change the fundamental nature of ecosystem processes in
agriculture (e.g., Figure 3) [36,79–81]. Improvements in carbon balance, nutrient retention, soil water
uptake efficiency, soil microbiome functions, and weed suppression are predicted as agriculture
based on high soil disturbance
Sustainability 2017, 9, 578 is replaced by ecosystems that require minimal disturbance 9 of 17 [36,82].
The reasons agriculture
why early agriculturalists originally domesticated annual grain crops
(e.g., Figure 3) [36,79–81]. Improvements in carbon balance, nutrient retention, soil water reflect the tools,
energetic constraints and understanding
uptake efficiency, of biological
soil microbiome functions, and weedprocesses
suppression that humans
are predicted had in the Neolithic
as agriculture
basedyears
era, 5000–10,000 on highBP soil[83].
disturbance
In theislast
replaced by ecosystems
century, that require
the sciences minimal disturbance
of evolutionary [36,82].genetics and
biology,
The reasons why early agriculturalists originally domesticated annual grain crops reflect the tools,
plant breeding have constraints
energetic expanded andtremendously, and many
understanding of biological researchers
processes believe
that humans had init
theisNeolithic
now possible
era, to breed
perennial cereal, legume,
5000–10,000 years fiber
BP [83].and
In theoilseed crops
last century, that would
the sciences yield sufficiently
of evolutionary biology, geneticstoand
eventually
plant occupy
breeding have expanded tremendously, and many researchers believe
large areas currently planted to annual species [80,84,85].When considering steps towards greater it is now possible to breed
perennial cereal, legume, fiber and oilseed crops that would yield sufficiently to eventually occupy
agricultural large
sustainability,
areas currently the prospect
planted of increasing
to annual ecological
species [80,84,85].When function
considering through
steps towards perennial
greater crops is
very significant, but sosustainability,
agricultural are discussions of land
the prospect tenure, scale
of increasing of production,
ecological function through energy return
perennial crops onis investment
and diversityvery significant,
of crops at bothbut so are discussions
farm and regional of land tenure,
scales scale of production, energy return on
[86–88].
investment and diversity of crops at both farm and regional scales [86–88].

Figure 3. A Mollisol soil profile from central Kansas USA exposing roots to a depth of 2.5 m from
Figure 3. A Mollisol soil profile
perennial wheatgrass from
on the central Kansas
left (Thinopyrum USA
intermedium) andexposing roots
annual wheat to aaestivum)
(Triticum depth onof 2.5 m from
the right. The
perennial wheatgrass onwheatgrass is being bred to intermedium)
the left (Thinopyrum produce the grain Kernza™
and annual(photo:
wheatJ. Richardson
(Triticumand J.
aestivum) on the
Glover).
right. The wheatgrass is being bred to produce the grain Kernza™ (photo: J. Richardson and J. Glover).
Research undertaken to quantify rates of SOM accumulation under perennial grain proto-crops
that are being currently bred is lacking. However, numerous studies, including many meta-analyses,
Research undertaken
have evaluated SOM to changes
quantify whenrates ofmanaged
lands SOM accumulation under perennial
for annual crop production grain
were converted to proto-crops
that are being currently
perennial bred [89–99].
grasslands is lacking.
Rates However, numerous
of C accumulation studies,
in diverse grassland including many
plantings range meta-analyses,
from
have evaluated0.33–1.01
SOM t hachanges
−1 year−1 in meta-analyses and reviews, whereas high-yielding, low diversity perennial
when lands managed for annual crop production were converted to
grasses for bioenergy have been found to increase SOC in the range of 1.09-1.88 t ha−1 year−1 (Table 1).
perennial grasslands
The range of [89–99].
0.3–0.5 t C haRates
−1 year−1of C accumulation
accumulated in diverse
following adoption grassland
of no-till plantings range from
or other SOM-enhancing
−1 year−1 approaches
0.33–1.01 t hamanagement in meta-analyses and reviews,
described above, whereas
overlaps with the lowhigh-yielding,
end of the carbon low diversity perennial
accumulation
range of perennial
grasses for bioenergy have been found to increase SOC in the range of 1.09-1.88 t ha−1 year−1 (Table 1).
grasslands.

The range of 0.3–0.5 t C ha−1 year−1 accumulated following adoption of no-till or other SOM-enhancing
management approaches described above, overlaps with the low end of the carbon accumulation
range of perennial grasslands.
Sustainability 2017, 9, 578 10 of 18

The wide range of carbon accumulation values reported in Table 2 reflects a combination of
methodological, geographical and biological variation. Two of the greatest methodological challenges
encountered when comparing studies stem from researchers not sampling SOM to the same soil
depth [99,100], and not using a uniform approach to estimate and correct for bulk density differences
across study sites [101]. The geographic variation reflects differences in grassland productivity and
SOM protection driven to a large extent by climate and soil texture [102]. The biological factors that
contribute to wide variation in SOC accumulation include the productivity of the grassland species,
the degree to which soil microbial populations are nutrient limited [103], and years since conversion to
perennial vegetation [102]. Taken together, it is possible to interpret how multiple factors contribute
to the broad differences in measured SOC accumulation rates (Table 2). For example, the contrast in
low accumulation rates for pasture or restored native grasslands versus higher accumulation rates for
bioenergy crops is likely explained by the latter being planted, on average, in more favorable climates,
bred for higher productivity, and more commonly fertilized with nitrogen, which not only increases
productivity, but can also increase microbial biomass and in turn necromass.

Table 2. Summary of field-based estimations of soil carbon accumulation rates in the conversion of
annual agriculture to perennial grassland or perennial bioenergy crops.

Mean C Depths 1 No. Studies

Study Type Geographic Areas Accumulation Sampled or Sites Reference
t ha−1 Year−1 (cm) Included
Annual crops to perennial pasture or restored native grassland
Central Europe, N.
Meta-analysis 0.72 0–30 273 [89]
America, Russia
Meta-analysis Russia 0.96 20 45 [90]
Meta-analysis Tropical to temperate 0.33 5–300 39 [91]
Meta-analysis Americas, UK, Australia 1.01 NR 2 23 [92]
Review N. Midwest USA 0.44–0.5 25 39 [93]
Review W. Canada 0.59 NR 17 [94]
Chronosequences Illinois, USA 0.43 100 16 [95]
Review France 0.50 NR - [96]
Review NR 0.3–1.0 NR - [97]
Annual crops to perennial bioenergy crops
Meta-analysis NR 1.14–1.88 0–150 23 [98]
Meta-analysis N. & S. America, Europe
Miscanthus S. Africa, Asia 1.09 100 13 [99]
Switchgrass 1.28 100 40 [99]
1 when a range is reported, it indicates that multiple soil depths falling within the range were included in the study;
2 NR = not reported.

Potential Soil Carbon Accumulation with Perennial Grains

The numerous studies documenting SOC accumulation in the conversion of tilled croplands to
perennial grasslands have provided a reasonably constrained range of accumulation rates (Table 2).
The studies have also highlighted areas of uncertainty that have considerable bearing on the maximum
SOC accumulation a given agroecosystem is likely to achieve. Chief among the areas of uncertainty
are (1) depth of SOM deposition under different perennial species, and relative stability of deeply
deposited SOM; (2) duration of positive net SOM accumulation following conversion from arable land;
and (3) percentage of SOM accumulated under the original native ecosystem that can be achieved in
the newly established grassland.
To make a rough estimation of how much SOC might be expected to accumulate with a conversion
of annual to perennial grains, we used the following equations that included country-specific data
from FAOSTAT [78] for land area dedicated to grain crops and SOM levels to 30 cm.
Sustainability 2017, 9, 578 11 of 18

C(ha) = %SOC × CLost × CReseq (1)

C(ha) = potential SOC sequestration per ha in kg, %SOC = %SOC mass per unit area,
CLost = Proportion of soil carbon lost via cultivation, CReseq = Percentage of CLost that can
be resequestered.
To calculate potential SOC sequestration per hectare, we multiplied average SOC mass per hectare
(data on a country-level basis, derived from FAOSTAT) by a factor representing the proportion of soil
carbon lost to cultivation (supplied by us, adjusted for different scenarios). This resulting number,
the mass of SOC lost to cultivation, was then multiplied by a factor representing the percentage of SOC
lost to cultivation that could potentially be re-sequestered (again, supplied by us, adjusted for different
scenarios). This provided us with the mass of SOC per hectare that could potentially be sequestered by
conversion from annual to perennial crops.
T = C(ha) × A (2)
T = Total potential soil carbon sequestration in Mg, A = Area (ha) planted to annual grains per
country (cereals, pulses, cotton, annual oilseed).
To make a theoretical projection of the global potential for SOC sequestration by perennial
crops, we multiplied each country’s average potential SOC sequestration per hectare by the country’s
total area planted to annual crops that could hypothetically be replaced one day by perennials,
including cereals, pulses, cotton, and oilseed crops, and then adding the sums for all countries.
Table 3 depicts global estimations of potential soil C accumulation in the transition from annual
to perennial grain crops based on different assumptions for depth of SOM deposition (30 cm vs.
whole profile), duration of positive SOM accumulation (30, 60, 90 years), % of original SOC lost
with cultivation (30 or 50), and % of original SOC accumulation possible (70 or 90). Our calculations
estimate a potential global accumulation of 13–54 Pg C in grain cropland soils of all countries following
conversion to perennial grain agriculture.

Table 3. Coarse estimates of soil C accumulation following the conversion of annual to perennial grain
agroecosystems using a range of assumptions.

SOC Accumulation Year−1

Assumptions Potential C Until Equilibrium Reached
Area
Accumulation
30 Years 60 Years 90 Years
Conservative Global (Pg) 13 0.42 0.21 0.14
Baseline 1 Average t ha−1 11.9 0.40 0.20 0.13

Full profile Global (Pg) 25 0.84 0.42 0.28

C accumulation 2 Average t ha− 1 23.9 0.80 0.40 0.27

50% SOC lost Global (Pg) 21 0.70 0.35 0.23

with conversion 3 Average t ha−1 19.9 0.66 0.33 0.22

90% of potential Global (Pg) 16 0.54 0.27 0.18

Accumulation 4 Average t ha−1 15.3 0.51 0.26 0.17

Maximum Global (Pg) 54 1.80 0.90 0.60

Accumulation 5 Average t ha− 1 51.2 1.70 0.85 0.57
1 conservative baseline assumptions are that 30% of SOC has been lost in conversion to annual agriculture, %SOC

values for 0–30cm soil depth, 70% of the lost SOC can be recovered with a conversion back to perennial crop species.
2 assumptions equal to conservative baseline, except C accumulation to 100cm is assumed to be twice that of 30 cm

[99,100]. 3 assumptions equal to conservative baseline, except percentage loss of SOC following conversion to
annual agriculture is increased from 30 to 50% [4]. 4 assumptions equal to conservative, except soils are expected to
accumulate 90% of the SOC lost in conversion to annual agriculture [55]. 5 cumulaive change in C accumulation
when all three modifications of conservative baseline assumptions are made (full profile, 50% SOC lost, 90% of
potential). Overall model based on 2014 FAOSTAT data for country-specific values of land area in annual row crops,
SOC to 30 cm. Bulk density (BD) conversions were made using the equation BD = 100/(%SOM/0.244) + ((100 −
%SOM)/mineral BD) with SOM = SOC × 1.72 and mineral BD = 1.64 [89,91].
Sustainability 2017, 9, 578 12 of 18

Only the assumptions resulting in maximum C accumulation (54 Pg) fall within the range of
predicted C sinks of 50–78 Pg for cropland soils [4,24]. Using different assumption sets, our calculations
estimate SOC accumulation rates ranging from 0.13 to 1.70 t ha−1 year−1 . This range of values is
similar to the empirically measured range of SOC accumulation rates of 0.33–1.88 t ha−1 year−1 from
grassland and bioenergy studies (Table 2). Possibly the least realistic assumption we make in our
modeling exercise was a linear 90-year time span for approaching SOM steady state. This assumption
resulted in low rates of C accumulation per year, and contrasts with most studies that suggest C
accumulation rates reaching a maximum in the first few decades following conversion to perennials,
and then declining substantially by year fifty [54,55,89,91].

4. The Role of Diversity in Improving SOM

Discussions of SOM dynamics in this paper have primarily focused on the importance of
perennial vegetation in soil development. However, plant diversity is also an important consideration.
Ecologists have firmly established that single species or monoculture plantings of a crop will eventually
decline in productivity due to pathogen load or insect herbivory [104–106]. Growing different plant
functional groups together (e.g., legumes and grasses) can also result in greater productivity due
to niche partitioning or complementarity [107]. To the extent that NPP translates into belowground
organic matter production, diversity in perennial cropping systems is predicted to affect SOM stocks
and rates of accumulation [108].
Crop diversity can also affect SOM through its effect on the quality of organic matter entering
the soil. For example, Ampleman and colleagues [109] compared SOM accumulation in stands
dominated by C4 grasses with more diverse forb-grass prairie mixtures. Soils planted to >66% C4
grasses showed a decline of 0.31 t C ha−1 year−1 over 33 years, whereas the soils planted to forb
dominated and forb-grass mixes increased in SOC at the rate of 0.56 and 0.27 t ha−1 year−1 , respectively.
One explanation for this and similarly low rates of SOC accumulation in other settings is that soil
microbial populations are limited by nutrients, especially N [92]. When soil nutrient availability is
insufficient to meet the stoichiometric ratios of the microbial biomass, many plants appear to be able
to induce mineralization of nutrients held in SOM by priming the rhizosphere with labile carbon
exudates [109]. While this can induce a flush of microbial activity, it is different from stimulating large
microbial populations with more stoiciometrically-balanced inputs which can lead to the accumulation
of necromass and ultimately physio-chemically stabilized SOM [103,110].

5. Conclusions
SOM is widely expected to play a central role in efforts to transition agriculture from an industrial
model where high volumes of energetically expensive and environmentally damaging inputs are
required to achieve a high volume of outputs, to an ecosystem model, where adequate food is produced
within sustainable energy and biogeochemical boundaries of the planet [23,29,36,111]. Yet in spite
of its agreed upon importance, SOM has proven difficult for farmers to build. Few grain-producing
agroecosystems feature SOM levels that match the native ecosystems that preceded them. Why is
this the case? While many questions still exist, ecosystem science has advanced a great deal in
identifying the factors that regulate SOM formation and mineralization. Two processes that contribute
greatly to the accumulation of SOM are the allocation of plant productivity belowground by roots [50],
and the stabilization and protection of organic compounds in soil aggregates [51]. Perennial vegetation
promotes both of these processes. Indeed, perennials are essential for soil and ecosystem development
to progress in almost all native terrestrial ecosystems [36]. In contrast, annual crops allocate a smaller
amount of biomass belowground and they have historically required tillage which breaks apart soil
aggregates and induces microbial mineralization of SOM.
Most approaches to increasing cropland SOM either strive to increase organic matter inputs
(adding cover crops, breeding deep-rooted annuals, amending with biochar) or decrease soil
disturbance (no-till), but the nature of annual crop production makes it difficult to address both
Sustainability 2017, 9, 578 13 of 18

processes. In basic terms, this explains why SOM levels in annual grain agriculture rarely match levels
attained by native ecosystems. Ecosystem theory, and empirical evidence from ex-arable grasslands
and bioenergy crops suggest that perennial grain crops will facilitate SOM accumulation and soil
development similar to what occurs in native ecosystems [36]. There are many challenges to achieving
such a “natural systems agriculture”. For example, it is not yet clear how farmers will facilitate
succession or stand replacement in shifting from one perennial crop to another without inducing
large losses of SOM from tillage [112]. Challenges notwithstanding, an agriculture based on diverse
perennial crops has great potential for improving SOM contents and achieving goals of ecological
intensification and climate change mitigation in agriculture.
Working on the ecological sustainability of agriculture addresses an essential part of rectifying
the food system as a whole, but other parts of the whole need attention as well [113]. For example,
progress will be limited as long as government subsidies promote large-scale industrial production of
a few annual grain crops [88]. The consolidation of corporations that market seeds and other inputs as
well as corporations that purchase and process grain can also profoundly restrict systemic changes in
the food system. Moreover, global governance and economic structures will need to align in order to
advance changes in food systems that are embedded in much larger socio-economic systems [114].

Acknowledgments: The authors would like to thank three anonymous reviewers and Academic Editor Tiziano
Gomiero for comments that significantly improved this paper. Brian Rumsey conducted research that was used in
this paper during a graduate internship at The Land Institute in Spring of 2014. The internship was supported by
the C-CHANGE (Climate Change, Humans and Nature in the Global Environment) NSF IGERT program at the
University of Kansas.
Author Contributions: Crews and Rumsey conceived of the paper together and carried out equal parts of the
literature review. Rumsey undertook the C accumulation calculations in Table 3 using the FAOSTAT database,
and Crews wrote a majority of the manuscript.
Conflicts of Interest: The authors declare no conflict of interest.

References
1. Scharlemann, J.P.W.; Tanner, E.V.J.; Hiederer, R.; Kapos, V. Global soil carbon: Understanding and managing
the largest terrestrial carbon pool. Carbon Manag. 2014, 5, 81–91. [CrossRef]
2. Trumbore, S. Radiocarbon and soil carbon dynamics. Annu. Rev. Earth Planet. Sci. 2009, 37, 47–66. [CrossRef]
3. Vermeulen, S.J.; Campbell, B.M.; Ingram, J.S.I. Climate change and food systems. Annu. Rev. Environ. Resour.
2012, 37, 195–222. [CrossRef]
4. Lal, R. Global potential of soil carbon sequestration to mitigate the greenhouse effect. Crit. Rev. Plant Sci.
2003, 22, 151–184. [CrossRef]
5. Cole, C.V.; Duxbury, J.; Freney, J.; Heinemeyer, O.; Minami, K.; Mosier, A.; Paustian, K.; Rosenberg, N.;
Sampson, N.; Sauerbeck, D.; et al. Global estimates of potential mitigation of greenhouse gas emissions by
agriculture. Nutr. Cycl. Agroecosyst. 1997, 49, 221–228. [CrossRef]
6. Le Quéré, C.; Moriarty, R.; Andrew, R.M.; Peters, G.P.; Ciais, P.; Friedlingstein, P.; Jones, S.D.; Sitch, S.; Tans, P.;
Arneth, A.; et al. Global carbon budget 2014. Earth Syst. Sci. Data 2015, 7, 47–85. [CrossRef]
7. IPCC. Agriculture, Forestry and Other Land Use. In Climate Change 2014 Synthesis Report; IPCC: Geneva,
Switzerland, 2014; Chapter 11.
8. McLauchlan, K. The nature and longevity of agricultural impacts on soil carbon and nutrients: A review.
Ecosystems 2006, 9, 1364–1382. [CrossRef]
9. Weil, R.R.; Brady, N.C. The Nature and Properties of Soils, 15th ed.; Pearson: New York, NY, USA, 2016.
10. Post, W.M.; Izaurralde, R.C.; Jastrow, J.D.; McCarl, B.A.; Amonette, J.E.; Bailey, V.L.; Jardine, P.M.; West, T.O.;
Zhou, J. Enhancement of carbon sequestration in US soils. BioScience 2004, 54, 895–908. [CrossRef]
11. Paustian, K.; Lehmann, J.; Ogle, S.; Reay, D.; Robertson, G.P.; Smith, P. Climate-smart soils. Nature 2016, 532,
49–57. [CrossRef] [PubMed]
12. Hillel, D. Out of the Earth; University of California Press: Berkeley, CA, USA, 1991.
13. Montgomery, D.R. Dirt, the Erosion of Civilization; University of California Press: Berkeley, CA, USA, 2007.
14. Grandy, A.S.; Robertson, G.P. Land-use intensity effects on soil organic carbon accumulation rates and
mechanisms. Ecosystems 2007, 10, 58–73. [CrossRef]
Sustainability 2017, 9, 578 14 of 18

15. Haas, H.J.; Evans, C.E. Nitrogen and Carbon Changes in Great Plains Soils as Influenced by Cropping and Soil
Treatments; USDA Technical Bulletin No. 1164; U.S. Government Printing Office: Washington, DC, USA, 1957.
16. Davidson, E.A.; Ackerman, I.L. Changes in soil carbon inventories following cultivation of previously
untilled soils. Biogeochem. 1993, 20, 161–193. [CrossRef]
17. Mazoyer, M.; Roudart, L. The History of World Agriculture: From the Neolithic Age to the Present Crisis; Earthscan:
London, UK, 2006.
18. Wilken, G.C. Good Farmers: Traditional Agricultural Resource Management in Mexico and Central America;
University of California Press: Berkeley, CA, USA, 1987.
19. Howard, A. An Agricultural Testament; Oxford University Press: London, UK, 1943.
20. Rodale, J.I. Pay Dirt: Farming & Gardening with Compost; The Devin-Adair Company: New York, NY,
USA, 1947.
21. Jackson, W. New Roots for Agriculture; University of Nebraska Press: Lincoln, NE, USA, 1980.
22. Gliessman, S.R. Agroecology. The Ecology of Sustainable Food System; CRC Press: Boca Raton, FL, USA, 2007.
23. Royal Society. Reaping the Benefits; RS Policy Document 11/09; The Royal Society: London, UK, 2009.
24. Sommer, R.; Bossio, D. Dynamics and climate change mitigation potential of soil organic carbon sequestration.
J. Environ. Manag. 2014, 144, 83–87. [CrossRef] [PubMed]
25. Crowther, T.W.; Todd-Brown, K.E.O.; Rowe, C.W.; Wieder, W.R.; Carey, J.C.; Machmuller, M.B.; Snoek, B.L.;
Fang, S.; Zhou, G.; Allison, S.D.; et al. Quantifying global soil carbon losses in response to warming. Nature
2016, 540, 104–108. [CrossRef] [PubMed]
26. Tittonell, P.; Giller, K.E. When yield gaps are poverty traps: The paradigm of ecological intensification in
African smallholder agriculture. Field Crops Res. 2013, 143, 76–90. [CrossRef]
27. Cassman, K.G. Ecological intensification of cereal production systems: Yield potential, soil quality,
and precision agriculture. PNAS 1999, 96, 5952–5959. [CrossRef] [PubMed]
28. Tittonell, P. Ecological intensification: Local innovation to address global challenges. Sustain. Agric. Rev.
2016, 19, 1–34.
29. Foley, J.A.; Ramankutty, N.; Brauman, K.A.; Cassidy, M.S.; Gerber, J.S.; Johnston, M.; Mueller, N.D.;
O’Connell, C.; Ray, D.K.; West, P.C.; et al. Solutions for a cultivated planet. Nature 2011, 478, 337–342.
[CrossRef] [PubMed]
30. Gomiero, T. Soil degradation, land scarcity and food security: Reviewing a complex challenge. Sustainability
2016, 8, 281. [CrossRef]
31. Dore, T.; Makowski, D.; Malezieux, E.; Munier-Jolain, N.; Tchamitchian, M.; Tittonell, P. Facing up to
the paradigm of ecological intensification in agronomy: Revisiting methods, concepts and knowledge.
Eur. J. Agron. 2011, 34, 197–210. [CrossRef]
32. Tittonell, P. Ecological intensification of agriculture—Sustainable by nature. Curr. Opin. Environ. Sustain.
2014, 8, 53–61. [CrossRef]
33. Bommarco, R.; Kleijn, D.; Potts, S.G. Ecological intensification: Harnessing ecosystem services for food
security. TREE 2013, 28, 230–238. [CrossRef] [PubMed]
34. Rusch, A.; Bommarco, R.; Ekbom, B. Conservation biological control in agricultural landscapes.
In Insect-Plant Interactions in a Crop Protection Perspective; Advances in Botanical Research Series; Sauvion, N.,
Calatayud, P.-A., Thiery, D., Eds.; Elsevier: Amsterdam, The Netherlands, 2016; Volume 81.
35. Brady, M.V.; Hedlund, K.; Cong, R.G.; Hemerik, L.; Hotes, S.; Machado, S.; Mattsson, L.; Schulz, E.;
Thomsen, I.K. Valuing supporting soil ecosystem services in agriculture: A natural capital approach. Agron. J.
2015, 107, 1809–1821. [CrossRef]
36. Crews, T.E.; Blesh, J.; Culman, S.W.; Hayes, R.C.; Jensen, E.S.; Mack, M.C.; Peoples, M.B.; Schipanski, M.E.
Going where no grains have gone before: From early to mid-succession. Agric. Ecosyst. Environ. 2016, 223,
223–238. [CrossRef]
37. Schlesinger, W.H. Carbon balance in terrestrial detritus. Annu. Rev. Ecol. Syst. 1977, 8, 51–81. [CrossRef]
38. Johnston, A.E.; Poulton, P.R.; Coleman, K. Soil organic matter: Its importance in sustainable agriculture and
carbon dioxide fluxes. Adv. Agron. 2009, 101, 1–57.
39. Scott, D.A.; Baer, S.G.; Blair, J.M. Recovery and relative influence of root, microbial and structural properties
of soil on physically sequestered carbon stocks in restored grassland. Soil Sci. Soc. Am. J. 2017, 81, 50–60.
[CrossRef]
Sustainability 2017, 9, 578 15 of 18

40. Stockman, U.; Adams, M.A.; Crawford, J.W.; Field, D.J.; Henakaarchchi, N.; Jenkins, M.; Minasny, B.;
McBratney, A.B.; Remy de Courcelles, V.D.; Singh, K.; et al. The knowns, known unknowns and unknowns
of sequestration of soil organic carbon. Agric. Ecosyst. Environ. 2013, 16, 80–99. [CrossRef]
41. Kallenback, C.M.; Frey, S.D.; Grandy, S. Direct evidence for microbial-derived soil organic matter formation
and its ecophysiological controls. Nat. Commun. 2016, 7. [CrossRef] [PubMed]
42. Kleber, M. What is recalcitrant soil organic matter? Environ. Chem. 2010, 7, 1–13. [CrossRef]
43. Schmidt, M.W.I.; Torn, M.S.; Abiven, S.; Dittmar, T.; Guggenberger, G.; Janssens, I.A.; Kleber, M.;
Kogel-Knabner, I.; Lehmann, J.; Manning, D.; et al. Soil organic matter persistence as an ecosystem property.
Nature 2011, 478, 49–56. [CrossRef] [PubMed]
44. Dungait, J.; Hopkins, D.; Gregory, A.; Whitmore, A. Soil organic matter turnover is governed by accessibility
not recalcitrance. Glob. Chang. Biol. 2012, 18, 1781–1796. [CrossRef]
45. Chapin, F.S.; Matson, P.A.; Vitousek, P.M. Principles of Terrestrial Ecology, 2nd ed.; Springer: New York, NY,
USA, 2012.
46. Hobbie, S.E.; Ogdahl, M.; Chorover, J.; Chadwick, O.A.; Oleksyn, J.; Zytkowiak, R.; Reich, P.B. Tree species
effects on soil organic matter dynamics: The role of soil cation composition. Ecosystems 2007, 10, 999–1018.
[CrossRef]
47. Field, C.B. Sharing the garden. Science 2001, 294, 2490–2491. [CrossRef] [PubMed]
48. Saugier, B.; Roy, J.; Mooney, H.A. Estimations of global terrestrial productivity: Converging toward a single
number? In Terrestrial Global Productivity; Roy, J., Saugier, B., Mooney, H.A., Eds.; Academic Press: San Diego,
CA, USA, 2001; pp. 543–557.
49. Johnson, J.M.F.; Allmaras, R.R.; Reicosky, D.C. Estimating source carbon from crop residues, roots and
rhizodeposits using the national grain-yield database. Agron. J. 2006, 98, 622–636. [CrossRef]
50. Baker, J.M.; Ochsner, T.E.; Venterea, R.T.; Griffis, T.J. Tillage and soil carbon sequestration—What do we
really know? Agric. Ecosyst. Environ. 2007, 118, 1–5. [CrossRef]
51. Six, J.; Elliott, E.T.; Paustian, K.; Doran, J.W. Aggregation and soil organic matter accumulation in cultivated
and native grassland soils. Soil Sci. Soc. Am. J. 1998, 62, 1367–1377. [CrossRef]
52. Grandy, A.S.; Neff, J.C. Molecular C dynamics downstream: The biochemical decomposition sequence and
its impact on soil organic matter structure and function. Sci. Total Environ. 2008, 404, 297–307. [CrossRef]
[PubMed]
53. Janzen, H.H. The soil carbon dilemma: Shall we hoard it or use it? Soil Biol. Biochem. 2006, 38, 419–424.
[CrossRef]
54. Lal, R.; Griffin, M.; Apt, J.; Lave, L.; Morgan, M.G. Managing soil carbon. Science 2004, 304, 393. [CrossRef]
[PubMed]
55. Ogle, S.M.; Breidt, F.J.; Paustian, K. Agricultural management impacts on soil organic carbon storage under
moist and dry climatic conditions of temperate and tropical regions. Biogeochemistry 2005, 72, 87–121.
[CrossRef]
56. VandenBygaart, A.J. The myth that no-till can mitigate global climate change. Agric. Ecosyst. Environ. 2016,
216, 98–99. [CrossRef]
57. Powlson, D.S.; Stirling, C.M.; Jat, M.L.; Gerard, B.G.; Palm, C.A.; Sanchez, P.A.; Cassman, K.G.
Limited potential of no-till agriculture for climate change mitigation. Nat. Clim. Chang. 2014, 4, 678–683.
[CrossRef]
58. Dolan, M.S.; Clapp, C.E.; Allmaras, R.R.; Baker, J.M.; Molina, J.A.E. Soil organic carbon and nitrogen in
a Minnesota soil as related to tillage, residue and nitrogen management. Soil Tillage Res. 2006, 89, 221–231.
[CrossRef]
59. VandenBygaart, A.J.; Gregorich, E.G.; Angers, D.A. Influence of agricultural management on soil organic
carbon: A compendium and assessment of Canadian studies. Can. J. Soil Sci. 2003, 83, 363–380. [CrossRef]
60. Gál, A.; Vyn, T.J.; Michéli, E.; Kladivko, E.J.; McFee, W.W. Soil carbon and nitrogen accumulation with
long-term no-till versus moldboard plowing overestimated with tilled-zone sampling depths. Soil Tillage Res.
2007, 96, 42–51. [CrossRef]
61. Syswerda, S.P.; Corbin, A.T.; Mokma, D.L.; Kravchenko, A.N.; Robertson, G.P. Agricultural management
and soil carbon storage in surface vs. deep layers. Soil Sci. Soc. Am. J. 2011, 75, 92–101. [CrossRef]
62. Kravchenko, A.N.; Robertson, G.P. Whole-profile soil carbon stocks: The danger of assuming too much from
analyses of too little. Soil Sci. Soc. Am. J. 2011, 75, 235–240. [CrossRef]
Sustainability 2017, 9, 578 16 of 18

63. Six, J.; Ogle, S.M.; Breidt, F.J.; Conant, R.T.; Mosier, A.R.; Paustian, K. The potential to mitigate global
warming with no-tillage management is only realized when practised in the long term. Glob. Chang. Biol.
2004, 10, 155–160. [CrossRef]
64. Powlson, D.S.; Glendining, M.J.; Coleman, K.; Whitmore, A.P. Implications for soil properties of removing
cereal straw: Results from long-term studies. Agron. J. 2011, 103, 279–287. [CrossRef]
65. Blanco-Canqui, H. Crop residue removal for bioenergy reduces soil carbon pools: How can we offset carbon
loss? BioEnergy Res. 2013, 6, 358–371. [CrossRef]
66. Poeplau, C.; Don, A. Carbon sequestration in agricultural soils via cultivation of cover crops—A
meta-analysis. Agric. Ecosyst. Environ. 2015, 200, 33–41. [CrossRef]
67. West, T.O.; Post, W.M. Soil organic carbon sequestration rates by tillage and crop rotation: A global data
analysis. Soil Sci. Soc. Am. J. 2002, 66, 1930–1946. [CrossRef]
68. Beniston, J.W.; DuPont, S.T.; Glover, J.D.; Lal, R.; Dungait, J.A.J. Soil organic carbon dynamics 75 years after
land-use change in perennial grassland and annual wheat agricultural systems. Biogeochemistry 2014, 120,
27–49. [CrossRef]
69. Kell, D.B. Breeding crop plants with deep roots: their role in sustainable carbon, nutrient and water
sequestration. Ann. Bot. 2011, 108, 407–418. [CrossRef] [PubMed]
70. Kell, D.B. Large-scale sequestration of atmospheric carbon via plant roots in natural and agricultural
ecosystems: Why and how. Philos. Trans. R. Soc. B 2012, 367, 1589–1597. [CrossRef] [PubMed]
71. King, F.H. Farmers of Forty Centuries; Dover Publications: New York, NY, USA, 2004.
72. Schlesinger, W. Carbon sequestration in soils. Science 1999, 284, 2095. [CrossRef]
73. DeLonge, M.S.; Ryals, R.; Silver, W.L. A lifecycle model to evaluate carbon sequestration potential and
greenhouse gas dynamics of managed grasslands. Ecosystems 2013, 16, 962–979. [CrossRef]
74. Woolf, D.; Amonette, J.E.; Street-Perrott, F.A.; Lehmann, J.; Joseph, S. Sustainable biochar to mitigate global
climate change. Nat. Commun. 2010, 1, 1–9. [CrossRef] [PubMed]
75. Sohi, S.P.; Krull, E.; Lopez-Capel, E.; Bol, R. A review of biochar and its use and function in soil. Adv. Agron.
2010, 105, 47–82.
76. Atkinson, C.J.; Fitzgerald, J.D.; Hipps, N.A. Potential mechanisms for achieving agricultural benefits from
biochar application to temperate soils: A review. Plant Soil 2010, 337, 1–18. [CrossRef]
77. Lorenz, K.; Lal, R. Cropland soil carbon dynamics. In Recarbonization of the Biosphere; Lal, R., Lorenz, K.,
Huttl, R.F., Schneider, B.U., von Braun, J., Eds.; Springer: New York, NY, USA, 2012.
78. FAOSTAT. Food and Agriculture Data. Available online: www.fao.org/faostat/en/#home (accessed on
27 December 2016).
79. Glover, J.D.; Reganold, J.P.; Bell, L.W.; Borevitz, J.; Brummer, E.C.; Buckler, E.S.; Cox, C.M.; Cox, T.S.;
Crews, T.E.; Culman, S.W.; et al. Increased food and ecosystem security via pernnial grains. Science 2010,
328, 1638–1639. [CrossRef] [PubMed]
80. Batello, C.; Wade, L.; Cox, S.; Pogna, N.; Bozzini, A.; Choptiany, J. Perennial Crops for Food Security; FAO:
Rome, Italy, 2013.
81. Kantar, M.B.; Tyl, C.E.; Dorn, K.M.; Zhang, X.; Jungers, J.M.; Kaser, J.M.; Schendel, R.R.; Eckberg, J.O.;
Runck, B.C.; Bunzel, M.; et al. Perennial grain and oilseed crops. Annu. Rev. Plant Biol. 2016, 67, 703–729.
[CrossRef] [PubMed]
82. Robertson, G.P.; Hamilton, S.K.; del Grosso, S.J.; Parton, W.J. The biogeochemistry of bioenergy landscapes:
Carbon, nitrogen, and water considerations. Ecol. Appl. 2011, 21, 1055–1067. [CrossRef] [PubMed]
83. Van Tassel, D.L.; DeHaan, L.R.; Cox, T.S. Missing domesticated plant forms: Can artificial selection fill the
gap? Evol. Appl. 2010, 3, 434–452. [CrossRef] [PubMed]
84. DeHaan, L.R.; van Tassel, D.L. Useful insights from evolutionary biology for developing perennial grain
crops. Am. J. Bot. 2014, 101, 1801–1819. [CrossRef] [PubMed]
85. DeHaan, L.R.; Van Tassel, D.L.; Anderson, J.A.; Asselin, S.R.; Barnes, R.; Baute, G.J.; Cattani, D.J.;
Culman, S.W.; Dorn, K.M.; Hulke, B.S.; et al. Pipeline for grain domestication. Crop Sci. 2016, 56, 917–930.
[CrossRef]
86. Gomiero, T. Are biofuels an effective and viable energy strategy for industrialized societies? A reasoned
overview of potentials and limits. Sustainability 2015, 7, 8491–8521. [CrossRef]
87. Lin, B.B. Resilience in agriculture through crop diversification: Adaptive management for environmental
change. Bioscience 2011, 61, 183–193. [CrossRef]
Sustainability 2017, 9, 578 17 of 18

88. Berry, W. The Unsettling of America, Culture and Agriculture; Sierra Club Books: Washington, DC, USA, 1977.
89. Kämpf, I.; Hölzel, N.; Störrle, M.; Broll, G.; Kiehl, K. Potential of temperate agricultural soils for carbon
sequestration: A meta-analysis of land-use effects. Sci. Total Environ. 2016, 566–567, 428–435.
90. Kurganova, I.; de Gerenyu, V.L.; Six, J.; Kuzyakov, Y. Carbon cost of collective farming collapse in Russia.
GCB 2014, 20, 928–947. [CrossRef] [PubMed]
91. Post, W.M.; Kwon, K.C. Soil carbon sequestration and land-use change: Processes and potential.
Glob. Chang. Biol. 2000, 6, 317–328. [CrossRef]
92. Conant, R.T.; Paustian, K.; Elliott, E.T. Grassland management and conversion into grassland: Effects on soil
carbon. Ecol. Appl. 2001, 11, 343–355. [CrossRef]
93. Kucharik, C.J. Impact of prairie age and soil order on carbon and nitrogen sequestration. Soil Sci. Soc. Am. J.
2007, 71, 430–441. [CrossRef]
94. VandenBygaart, A.J.; McConkey, B.G.; Angers, D.A.; Smith, W.; de Gooijer, H.; Bentham, M.; Martin, T.
Soil carbon change factors for the Canadian agriculture national greenhouse gas inventory. Can. J. Soil Sci.
2008, 88, 671–680. [CrossRef]
95. Matamala, R.; Jastrow, J.D.; Miller, R.M.; Garten, C.T. Temporal changes in C and N stocks of restored prairie:
Implications for C sequestration strategies. Ecol. Appl. 2009, 18, 1470–1488. [CrossRef]
96. Arrouays, D.; Balesdent, J.; Germon, J.C.; Jayet, P.A.; Soussana, J.F.; Stengel, P. (Eds.) Increasing carbon stocks
in French Agricultural Soils. In Mitigation of the Greenhouse Effect; Synthesis of an Assessment Report by the
French Institute of Agricultural Research; INRA: Paris, France, 2002.
97. IPCC. Land Use, Land-Use Change and Forestry (LULUCF); Special Report of the Intergovernmental Panel on
Climate Change; Cambridge University Press: Cambridge, UK, 2000.
98. Agostini, F.; Gregory, A.S.; Richter, G.M. Carbon sequestration by perennial energy crops: Is the jury still
out? Bioenergy Res. 2015, 8, 1057–1080. [CrossRef] [PubMed]
99. Qin, Z.; Dunn, J.B.; Kwon, H.; Mueller, S.; Wander, M.M. Soil carbon sequestration and land use change
associated with biofuel production: Empirical evidence. GCB Bioenergy 2016, 8, 66–80. [CrossRef]
100. Jobbagy, E.G.; Jackson, R.B. The vertical distribution of soil organic carbon and its relation to climate and
vegetation. Ecol. Appl. 2000, 10, 423–436. [CrossRef]
101. Lee, J.; Hopmans, J.W.; Rolston, D.E.; Baer, S.G.; Six, J. Determining soil carbon stock changes: Simple bulk
density corrections fail. Agric. Ecosyst. Environ. 2009, 134, 251–256. [CrossRef]
102. Soussana, J.-F.; Loiseau, P.; Vuichard, N.; Ceschia, E.; Balesdent, J.; Chevallier, T.; Arrouays, D. Carbon cycling
and sequestration opportunities in temperate grasslands. Soil Use Manag. 2004, 20, 219–230. [CrossRef]
103. Kirby, C.A.; Arichardson, A.E.; Wade, L.J.; Batten, G.D.; Blanchard, C.; Kirkegaard, J.A. Carbon-nutrient
stoichiometry to increase soil carbon sequesration. Soil Biol. Chem. 2013, 20, 77–86. [CrossRef]
104. Yang, M.; Zhang, Y.; Qi, L.; Mei, X.; Liao, J.; Ding, X.; Deng, W.; Fan, L.; He, X.; Vivanco, J.M.; et al.
Plant-plant-microbe mechanisms involved in soil-born disease suppression on a maize and pepper
intercropping system. PLoS ONE 2014, 9. [CrossRef] [PubMed]
105. Gurr, G.M.; Lu, Z.; Zheng, X.; Xu, H.; Zhu, P.; Chen, G.; Yao, X.; Cheng, J.; Zhu, Z.; Catindig, J.L.; et al.
Multi-country evidence that crop diversification promotes ecological intensification of agriculture. Nat. Plants
2016, 2. [CrossRef] [PubMed]
106. Smith, V.H.; McBride, J.R.; Shurin, J.B.; Bever, J.D.; Crews, T.E.; Tilman, G.D. Crop diversification can
contribute to disease risk control in sustainable biofuels production. Front. Ecol. Environ. 2015, 13, 561–567.
[CrossRef]
107. Cardinale, B.J.; Matulich, K.L.; Hooper, D.U.; Byrnes, J.E.; Duffy, E.; Gamfeldt, L.; Balvanera, P.;
O’Connor, M.I.; Gonzalez, A. The functional role of producer diversity in ecosystems. Am. J. Bot. 2011, 98,
1–21. [CrossRef] [PubMed]
108. Tilman, D.; Hill, J.; Lehman, C. Carbon-negative biofuels from low-input high-diversity grassland biomass.
Science 2006, 314, 1598–1600. [CrossRef] [PubMed]
109. Ampleman, M.D.; Crawford, K.M.; Fike, D.A. Differential soil organic carbon storage at forb and
grass-dominated plant communities, 33 years after tallgrass prairie restoration. Plant Soil 2014, 374, 899–913.
[CrossRef]
110. Richardson, A.E.; Kirby, C.A.; Banerjee, S.; Kirkegaard, J.A. The inorganic nutrient cost of building soil
carbon. Carbon Manag. 2014, 3, 265–268. [CrossRef]
Sustainability 2017, 9, 578 18 of 18

111. Steffen, W.; Richardson, K.; Rockström, J.; Cornell, S.E.; Fetzer, I.; Bennett, E.M.; Biggs, R.; Carpenter, S.R.;
de Vries, W.; de Wit, C.A.; et al. Planetary boundaries: Guiding human development on a changing planet.
Science 2015, 347. [CrossRef] [PubMed]
112. Grandy, A.S.; Robertson, G.P. Initial cultivation of a temperate-region soil immediately accelerates aggregate
turnover and CO2 and N2 O fluxes. Glob. Chang. Biol. 2006, 12, 1507–1520. [CrossRef]
113. Schipanski, M.E.; MacDonald, G.K.; Rosenzweig, S.; Chappell, M.J.; Bennett, E.M.; Kerr, R.B.; Blesh, J.;
Crews, T.; Drinkwater, L.; Lundgren, J.G.; et al. Realizing resilient food systems. Bioscience 2016, 66, 600–610.
[CrossRef]
114. Head, J.W. International Law and Agroecological Husbandry: Building Legal Foundations for a New Agriculture;
Earthscan: New York, NY, USA, 2017.

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