Agroecology and Sustainable Food Systems, 39:500–515, 2015

Copyright © Taylor & Francis Group, LLC

ISSN: 2168-3565 print/2168-3573 online
DOI: 10.1080/21683565.2015.1008777

COMMENTARY

The Strong Perennial Vision: A Response

TIMOTHY E. CREWS and LEE R. DEHAAN

The Land Institute, Salina, Kansas, USA

This article was written as a response to Chris Smaje’s review,

“The Strong Perennial Vision: A Critical Review” [this issue]. In his
review, Smaje argues that society in general, and the research com-
munity in particular should question whether to invest substan-
tially in the development of perennial grains because a) ecological
theory suggests that perennial grains may yield less than annual
grains; b) strong criticisms of annual agriculture are unfounded,
both socially and ecologically; and c) focus on perennial grains
detracts from more important strategies for achieving agricul-
tural sustainability. We counter these three arguments by showing
a) that Grime’s C-S-R theory employed by Smaje is not meaning-
ful when used to predict the “evolvability” of perennial species
under selection in agricultural environments; b) that annual grain
ecosystems have not broadly achieved an acceptable level of ecosys-
tem function or resilience; and c) that perennial grain research is
not currently attracting the attention or resources that other, less
promising and less transformative research efforts garner.

KEYWORDS perennial, grain, C-S-R theory, agroecology

In his review, “The Strong Perennial Vision: A Critical Review,” Chris Smaje
(2015; this issue) perceives three problem areas with the rationale for devel-
oping perennial grain agriculture: a) ecological theory suggests that perennial
grains may yield less than annual grains; b) strong criticisms of annual
agriculture are unfounded, both socially and ecologically; and c) focus on

Address correspondence to Timothy E. Crews, The Land Institute, 2440 E. Water Well Rd.,
Salina, KS 67401, USA. E-mail: crews@landinstitute.org

500
 Commentary: The Strong Perennial Vision: A Response 501

perennial grains detracts from more important strategies for achieving agri-
cultural sustainability (Smaje 2015). By critiquing the strong perennial vision
(SPV), Smaje addresses the community of researchers working on peren-
nial grains in general, but he also singles out research conducted at The
Land Institute in Salina, Kansas (USA), in particular. This is understandable,
because The Land Institute has played a leading role in articulating the ratio-
nale and pursuing the science to develop perennial grains and grow them
in ecologically functional mixtures. Nevertheless, researchers who identify
with or play a role in perennial grain research are diverse, and we cannot
represent any perspectives other than our own. Here, we respond to Smaje’s
critique by dedicating a similar proportion of text to each of three areas he
identified.

1. C-S-R THEORY AND PERENNIAL GRAIN DEVELOPMENT

Smaje claims that the development of perennial grain crops will be difficult
to impossible, largely based on his interpretation of C-S-R theory of plant
strategies. We understand Smaje’s skepticism of perennial grain development
to follow these logical points:

1. Most of the crops upon which civilization depends are annual grains,
which are fundamentally ruderal species. Smaje states that to grow annual
grains, “tillage and fertilization . . . are required precisely in order to create
the necessary conditions for ruderal crops and their syndrome of desired
characteristics to thrive.”
2. Perennial plants, such as those being developed into perennial grains,
are not ruderal plants. Rather, they are either competitors (C) or stress-
tolerators (S).
3. Because perennial species belong to either the C or S groups, they are
classified as having low reproductive allocation (Grime 1977). Therefore,
they cannot produce abundant grain.
4. The C-S-R triangle represents very strict trade-offs. Any attempt to increase
reproductive allocation in perennials will necessarily transform them into
ruderal species that require the same tillage and fertilization currently
necessary for annual grains.
5. An attempt to introduce perenniality into an annual grain crop will
strongly reduce allocation to grain because the plant will now be in a
region of the C-S-R triangle where allocation to seed must be low.

To properly understand C-S-R theory, we must first understand that it is pri-

marily about habitats (Wilson and Lee 2000). Because different habitat types
exist, we can then study what plant types occupy those habitats. In C-S-R
502 T. E. Crews and L. R. DeHaan

theory, there are fundamentally three different habitats (and combinations

of these three) in the natural world, and, therefore, we should look for
three primary plant strategies (and the range between) to occupy those
habitats.
The theory does not address what happens if humans were to create
a new type of habitat never before seen in nature. True, annually cropped
agricultural fields are mimics of highly disturbed sites, so in this sense they
are not truly new. But the reproductive allocation in annual grains is sub-
stantially higher than in wild annuals (Harper 1976). According to Smaje’s
strict tradeoff view of the C-S-R triangle, increased reproductive allocation
could only arise by becoming more ruderal (shorter lived, smaller statured,
and less stress tolerant).
The first assumption Smaje makes is that grain yield increases have come
about by moving crops farther into the ruderal corner of the triangle. Many
grain crops are classified as “competitive ruderals” (Hardwick and Andrews
1983; Grime 2001). These are plants that have reproductive allocations high
enough to place them in the extreme ruderal class, but are too large and late
maturing to be considered ruderals. So grain crops are not high in reproduc-
tive allocation because of their placement on the C-S-R triangle, but rather
in spite of it. Plants are generally not placed at intermediate locations on
the C-S-R triangle because they are perfectly intermediate for all traits, but
rather because they have a mix of traits associated with various corners of
the triangle. Barbour et al. (1987) have stated:

Any attempt to locate a species in the Grime triangular model will result,
as with the r-K continuum, in some conflicting characteristics. For exam-
ple, you may find that a woody plant growing in a resource restricted
habitat has all of the necessary qualities of a stress tolerant competitor
but produces massive numbers of small seeds yearly. Such conflicts are
not unexpected, since such species’ adaptive possibilities are limited by
factors other than those used to describe the life history patterns. . . .
The idea of an identifiable life history pattern is appropriate only at the
general level (Grime 1982). Detailed studies at the physiological and mor-
phological level will reveal an uninterpretable mass of conflicting data.
(emphasis added; 102)

C-S-R theory was never intended to explain all variation. In fact, a study
strongly supporting C-S-R theory found that the first three primary axes of
numerous plant traits only explained 41% of variation between plants (Grime
et al. 1997). Grime (Grime and Pierce 2012) has stated that this unexplained
variation allows each species to exhibit an individual ecology.
As we will see herein, when an ecological theory designed for applica-
tion at the general level is misapplied to predict the evolvability of particular
species under selection by humans, the results are confusing and misleading.
 Commentary: The Strong Perennial Vision: A Response 503

Increased grain yield from modern breeding has not been achieved by
making the crops more ruderal, as Smaje’s model would suggest. In soybean,
new cultivars are more tolerant of the stress induced by high density, and
modern cultivars have reduced leaf area, a trait typical of S-type selection
(Morrison et al. 1999; Cober et al. 2005). In maize, most of the genetic yield
improvement has also been attributed to increased stress tolerance (Tollenaar
and Lee 2002). In general, breeding for yield in densely planted fields is
expected to create more stress tolerant plants with small, upright leaves
(Hardwick and Andrews 1983). Only in particularly short-seasoned habitats
has domestication and selection made crops more ruderal (i.e., Berger and
Ludwig 2014).
Second, Smaje assumes that perennial grain domesticates and existing
annual crops are placed very differently on the C-S-R triangle. After all,
we would not expect the triangle to dictate a tradeoff if the species are
not located in substantially different regions of the triangle. In fact, if we
use Grime’s (1984) C-S-R taxonomy for herbaceous plants, we discover that
both perennials with rapid shoot proliferation and fast growing annuals with
delayed flowering are classified as competitive ruderals. Crop plants are gen-
erally conceived as competitive ruderals that grow quickly, but have a large
leaf area that is useful in excluding weeds (Snapp 2008). The productive
perennial pasture grass Lolium perenne is considered to be a competitive
ruderal (Bol et al. 2002). According to Grime (1977), perennial herbs occupy
all but the very corners of the C-S-R triangle, so it is difficult to understand
how Smaje conceives of perennial herbs necessarily being excluded from
the portion of the triangle occupied by annual grains. In fact, Hodgson et al.
(1999) omitted perenniality from their C-S-R classification system because
both annual and long-lived perennial species are known to occupy ruderal
habitats. If perennial herbs and annual crops can occupy similar space on the
triangle, we do not understand Smaje’s argument that “perennial grain breed-
ing efforts typically involve working to increase sexual allocation against
S-strategy ecological tendencies.”
Third, Smaje’s concept of the categories presented in C-S-R is far stricter
than they are in reality, and this leads to a false understanding of the nature
of tradeoffs. Smaje seems to suggest that because Grime’s (1977) table indi-
cated that species that are not ruderal have a small “proportion of annual
production devoted to seeds” (1174), then no non-ruderal plants will ever
be able to have a high reproductive allocation. This is a misinterpretation of
Grime’s model. As mentioned above, it was never intended to explain every
difference between each species. Rather, it points out interesting patterns.
Although patterns overlap somewhat, allowing for generalizations, ultimately
“There are as many life history patterns as there are species. . .” (Barbour
et al. 1987:103).
To demonstrate the fact that the C-S-R triangle does not stand as
an absolute barrier to high reproductive allocation in perennials, we
504 T. E. Crews and L. R. DeHaan

will provide a few examples. Between perennial and annual Helianthus

species, there was no significant difference in reproductive effort (Hancock
and Pritts 1987). In four separate studies reviewed in Hancock and Pritts
(1987), perennials were found to have lower reproductive effort than
annuals. This confirms the overall trend, for which C-S-R theory is useful.
However, this association is far from absolute. Wild Helianthus annuus,
the progenitor of crop sunflower had a reproductive effort of 24%, while
early successional perennials had reproductive effort up to 39%. Perennial
species from late successional habitats (C-strategy) had reproductive effort
up to 33%. In another study, the perennial goldenrod Solidago nemoralis
had aboveground reproductive effort that in some locations exceeded
50% (Abrahamson and Gadgil 1973), an indication that wild herbaceous
perennials can have reproductive effort in the range of annual grains.
Domestic fruit trees are an excellent case study to determine the degree
to which tradeoffs associated with C-S-R plant types will constrain evolu-
tion. If trees, which are classified as C or S plants by Grime (1977), can
achieve high reproductive allocation in response to selection while remain-
ing perennials, then the C-S-R triangle cannot be used to argue for the
near-impossibility of non-ruderal (perennial) plants with high reproductive
allocation. Although Smaje states that trees cannot be used as examples
of perennials with high reproductive allocation since they have a differ-
ent growth form, he provides no rationale for his unwillingness to interpret
reproductive allocation in domestic trees using the C-S-R model.
Smaje attempts to discredit the example of apple orchards with high
reproductive allocation provided in Van Tassel et al. (2010). First, he claims
that the example is irrelevant because the high reproductive allocation came
about through human management and breeding. Second, he claims that the
high reproductive allocation over a 10-year lifespan of experimental orchards
is not relevant because commercial apple orchards are not grown for this
long.
We will address Smaje’s arguments against using fruit trees as examples
of selection against C-S-R tradeoff for reproductive allocation one at a time.
First, we have argued that it is precisely human management and breed-
ing that will make perennial grains possible (DeHaan et al. 2005). Smaje
appears to have misinterpreted the phrase “domestic prairie.” He seems to
regard future perennial grain crop fields as a literal prairie, where the only
human intervention is harvest. This has not been the vision we have por-
trayed in past publications. Rather, management for high resource availability
is going to be essential to any highly productive agroecosystem. We hope
that as much as possible these resources can come from nutrient cycling
and endogenous sources (Crews 2005). Whatever the situation, we recog-
nize that highly productive systems will require nutrient availability that is
higher than what is typically found in prairie. What is unique about peren-
nial systems is their ability to have high levels of resource availability with
 Commentary: The Strong Perennial Vision: A Response 505

associated high levels of productivity, while limiting resource loss and build-
ing soil quality (Culman et al. 2013). Additionally, selection will be central to
the development of perennial grains, just as it was for domestication of fruit
trees.
Smaje disregards the yields of apple trees based on a speculative refer-
ence that predicted a shorter than normal lifespan for commercial orchards
(Jotic 1997). Evidence is strong that although reproductive allocation in
forest trees is usually less than 10%, breeding and management of apple
orchards have increased reproductive allocation to about 60%, similar to
annual cereals (Cannell 1985). In a study of the first five years of an orchard,
the reproductive allocation was 52%, averaged over the five years (Palmer
1988). There is no reason to believe that non-ruderal species are constrained
by an ecological law that precludes high reproductive allocation, so long as
artificial selection and human management are supplied. Breeding and man-
agement have achieved a three- to six-fold increase in the reproductive effort
of trees; a similar increase in herbaceous plants will be more than adequate
to insure the success of perennial grains (Culman et al. 2010).
Smaje’s review presents an underlying sense that perennial grains must
be nearly impossible to develop because they are less natural than annual
grains. We agree with his idea that primitive annual crops could arise without
conscious human selection. The disturbed environments created by humans
would have been occupied by R-C strategists that conscious human selection
did not have to alter much to bring us modern grain crops. By comparison,
perennial grain development first requires the development of a never-seen-
in-nature environment with high resource availability, little tillage, and with
strict human-directed selection for maximum seed yield over several years.
Smaje seems to believe that because such an environment never before
existed, getting plants to enter this new evolutionary space will be very
difficult. In contrast, we agree with Denison (2007) who argues that humans
will likely have the greatest success in breeding for traits that were never
previously selected for in nature.
Smaje questions whether perennial grains will constitute an ecologically
stable strategy. We agree—annual grains are not ecologically stable in natural
environments and we have no reason to expect perennial grains to be sta-
ble either. Agriculture involves creating new environments and germplasm
that are maintained by human effort in which domestic crops are now a
stable strategy. Left alone, neither modern grain varieties nor future peren-
nial grains would survive if left to compete in native ecosystems. Smaje
seems to suggest the challenge is worse for perennial than for annual grains.
Perhaps, it is difficult to envision an herbaceous perennial system where high
resource availability is maintained, but for this we need to look no further
than modern forage and perennial biofuel systems. Smaje implies a sort of
“evolutionary flywheel” where plant populations tend to keep going in what-
ever direction he believes they were headed on the C-S-R triangle (see arrows
506 T. E. Crews and L. R. DeHaan

on Figure 1 of Smaje [2015; this issue]). He states that “it seems to be an agro-
nomic fact that the dominant trends in crop development have been based
on augmenting the existing ecological tendencies of RC plants, ‘working
with nature, so to speak, whereas perennial grain breeding efforts typically
involve working to increase sexual allocation against S-strategy ecological
tendencies.” Such an interpretation of C-S-R theory has no experimental evi-
dence to our knowledge. Rather, as we have described above, crops have
been moved in various directions on the triangle. Plant strategies evolve in
response to habitats, which are primary in the C-S-R model. If we create
a new, novel habitat that is conducive to perennial grains, we can expect
plants to occupy it, just as fruit trees have occupied the novel orchard envi-
ronment. Although constraints to selection exist, they are better understood
with quantitative genetic models than through the C-S-R model.
C-S-R theory is not useful for predicting plant breeding outcomes, but
it can serve as an informative lens for considering candidate species for
domestication. Domestication may involve moving toward C-R types, but
as with annuals, breeding can combine aspects of all three strategies. Snapp
(2008) states that crop plants with all C-S-R strategies can be identified. Some
grow quickly and are poorly defended against insects (R). Others grow more
slowly with indeterminate flowering, are tolerant of stresses, and may have
toxic seeds that require processing (S). Others, like maize, acquire resources
very effectively to grow rapidly to a large size (C). It is perfectly reasonable to
breed greater stress tolerance or herbivore resistance into an R or C strategist,
making it more S-like.
Bennett et al. (2012) provides a very useful perspective for understand-
ing C-S-R theory as it relates to grain breeding:

There are many reasons why the typical architecture observed in an R-

strategy plant that has been adapted for crop production is less than
optimal. . . . Most crops originate from R-strategy plants, yet breeding
programmes are frequently orientated towards C-strategy plants. In those
countries where land use for crops is marginal and abiotic stress levels are
high, it might be more desirable to select for S-strategy plants. Although
S-strategy plants can be overgrown by competitors in a wild habitat, in
farmed land this is manageable through weed control or less dense seed
planting rates. A crop ideotype would be an S-strategy plant with the
ability of an R-strategy plant to reproduce rapidly when the environmen-
tal conditions become harsh, thus ensuring at least a minimum yield each
year. (3397)

In the case of de novo perennial grain domestication, there is a wide array

of herbaceous species from which to choose, covering most of the C-S-R
triangle (Grime 1977). If one wished to fit the new species into a highly
productive system that is similar to current grain fields in terms of output,
 Commentary: The Strong Perennial Vision: A Response 507

then one might do well to start with a species that has C-S-R position very
similar to current C-R grain crops. But if one is developing a perennial
grain crop for a stressful environment (droughty, saline, or shaded), then
an S-strategist may be a reasonable candidate for domestication. However,
one could also start with a C-R plant and select for increased stress tolerance,
as has been done in annual grains.

2. ANNUAL AGRICULTURE OR SOCIAL REFORM?

In the first paragraph of his SPV critique, Smaje states, “As many analysts
have pointed out, the agricultural practices associated with the cultivation
of annual crops, principally tillage, fertilization, irrigation, and pesticide use,
lead to environmental problems including soil erosion, nutrient leaching and
volatilization, eutrophication of watercourses, loss of soil carbon, salinization,
pest resistance and the overuse of water and energy.” However, by the end
of the review, Smaje pivots in his critique, suggesting that the real problem
of agriculture is not the severely compromised ecosystem that follows from
tillage or chemical treatment of the landscape, but is instead foremost a social
problem. Smaje proposes that development of perennial grains is important
primarily to countries—especially ones with colonial legacies—that foster
large-scale grain production using industrial methods. He contends that most
perennial grain research is taking place in such countries, as an approach to
“rescue an extant agriculture ill-adapted to its ecological context through
technological improvement.” Essentially, Smaje argues that intensive, small-
scale mixed cropping models have proven themselves to be sustainable in
humid temperate areas of Europe, and that the real challenge facing human-
ity is the social problem of how to adapt something like the European model
to other parts of the world.
Social reform has and will continue to be critical as humanity grapples
with the challenges of changing diet, reducing food waste, and managing
the effects of climate change on agriculture, but reform alone will not result
in agricultural sustainability. We agree with Smaje that dramatic levels of soil
erosion and other forms of degradation commonly occur on large-scale grain
producing farms of the United States, Canada, Russia, China, and Australia.
It is ironic because many of these countries are considered to be among
the most agronomically advanced in the world. One simply need look at
the Iowa State Daily Erosion Project Website (2015) after a rainstorm in
spring or fall to see estimates of highly unsustainable rates of soil erosion in
the Midwest in the United States, even from lands under no-till production.
However, while the scale and low crop diversity of industrial grain produc-
tion can exacerbate soil loss and degradation, the history of soil degradation
in agriculture precedes the advent of industrial agriculture by thousands of
years.
508 T. E. Crews and L. R. DeHaan

Before the fossil fuel era, virtually all agricultural regions around the
world featured diversified, small-scale cropping arrangements, frequently
with some integration of perennial species (Mazoyer and Roudart 2006).
Some of these, typically ones that occupied natural or artificial wetlands or
experienced some flooding regime, showed remarkable resilience through
the ages (Hillel 1991). Such systems included Nile floodplain agriculture,
rice paddy systems of Southeast Asia, and the chinampa and raised field
agricultures of Mesoamerica (King 1911; Wilken 1987; Hillel 1991). These
agroecosystems were exceptional. Far more common were agroecosystems
that experienced anything from slight to moderate soil degradation and
reduction of ecosystem functions, to extreme erosion resulting in a collapse
of productivity (Hillel 1991; Montgomery 2007a). Upland soils that literally
fed the rise of civilizations—along the Fertile Crescent, on the Loess Plateau
in central China, across numerous provinces of Italy during the Roman
Empire, as well as parts of the Altiplano in Central Mexico—experienced
rather spectacular levels of soil degradation and erosion, in spite of the
fact that they were small-scale, diversified, labor intensive, locally adapted
farming systems (O’Hara et al. 1993; Montgomery 2007a).
Is Smaje correct in suggesting that diversified small-scale European farms
do not experience the soil loss that seems to plague other parts of the world?
A report in 2000 by the European Soil Bureau suggests the answer is yes,
at least in NW Europe (van der Knijff et al. 2000). The report identified
moderate to high erosion risks in parts of Southern Europe, especially in
Spain, Italy, Greece, and Switzerland. Northwestern Europe has a remarkably
low natural risk of erosion primarily because of low rainfall erosivity—that is,
rainfall events tend to be gentle and even, and enough rain falls to maintain
a land surface cloaked with vegetation. Soil scientist Daniel Hillel (1991)
also asserted that the climate of Western Europe should be credited with the
region’s unusually low erosion risk, and that the farming methods developed
in that context ended up causing serious land degradation when exported to
other regions.

The problem of accelerated erosion leading to rapid loss of topsoil, the

most fertile layer of the soil, is worldwide, and growing worse. It is
exacerbated by modern patterns of land use and mechanized methods
of cultivation. In the main, these methods were developed in Western
Europe, where they resulted in great changes in the landscape, notably
removal of most of the forest cover and drainage of wetlands, but in gen-
eral they did not cause a progressive degradation of the land and water
resources there. The benign temperate-humid climate of Western Europe,
with its relatively gentle rainfall regime, spared Europe—with the notable
exception of some Mediterranean sections—the extreme forms of soil
erosion that occurred in other regions. But when Europeans introduced
their clean-till farming methods to other regions with less benign climates,
sever erosion ensued. (160)
 Commentary: The Strong Perennial Vision: A Response 509

An increased risk of soil erosion is arguably the most serious threat

to sustainable productivity that follows from annual crop production.
Montgomery (2007b) found median soil loss rates in plowed agriculture to
exceed formation rates by ninety-five fold. Native vegetation, in contrast, sus-
tained median loss rates lower than formation rates; a condition necessary
for soil to form.
Aside from soil erosion, there are other important types of soil degra-
dation and reduction in ecosystem functions that occur as a result of annual
soil disturbance and the replacement of perennial with annual vegetation.
As with erosion, these forms of degradation can be exacerbated by scale,
but in most respects are scale-neutral. They occur on farms ranging in size
from 1 to 1000 ha.
Soil organic matter (SOM) declines under annual cropping regimes
because losses of SOM are increased and inputs are reduced. A net increase
in microbial mineralization typically occurs for decades following initial
tillage of a soil (Johnston et al. 2009), and the replacement of perennial
roots with those of annuals reduces belowground allocation of primary pro-
ductivity from more than 50% to approximately 15% (Goudriaan et al. 2001;
Saugier et al. 2001). Tilled agricultural soils lose, on average, 30% of their
soil organic matter before they approach a new equilibrium (Lal 2003), but
the loss value can exceed 50%. It is possible to maintain artificially higher
levels of SOM in tilled fields by importing manures or composts onto a site,
but this increase in SOM comes at the cost of a reduction in soil carbon
inputs somewhere else. The inclusion of cover-cropping or no-till practices
can definitely improve soil organic matter concentrations in some annual
cropping arrangements (Poeplau and Don 2015), but these practices are not
predicted to achieve the SOM levels maintained under successional perennial
vegetation (Grandy and Robertson 2007).
Nutrient retention is one of the ecosystem functions that are seriously
compromised when vegetation is cleared with tillage or herbicides on an
annual basis. The potential for nitrate leaching is greatest when mineral fer-
tilizers are applied to annual crops in excess of current crop demand in
order to meet future demand. However, reliance on organic sources of nitro-
gen (N) to fertilize annual crops, either applied manures or incorporation of
N-fixing cover crops, can also result in substantial leaching of nitrate (Crews
and Peoples 2005). This is because release of N from organic sources into
soils does not tightly coincide with the timing of peak nutrient demand for
annual crops. Nitrogen loss from agriculture into freshwater and then saltwa-
ter is the single greatest cause of over 400 marine dead zones that exist in the
world (Diaz and Rosenberg 2008)—the majority of which occur in northern
and western Europe and along the east coast of the United States.
For years, it has been well established that highly disturbed ecosystems
leak nutrients, while ecosystems further along in succession tend to tightly
retain them (Vitousek and Reiners 1975). The establishment of deep-rooted
510 T. E. Crews and L. R. DeHaan

perennial plant species that take up nutrients over greater time and space
is key to understanding why retention increases. A recent study by Culman
et al. (2013) examined nitrate leaching from plots of annual wheat and the
perennial grain Kernza, fertilized with N from synthetic and organic sources
at agronomically appropriate rates in Michigan (USA). In the establishment
year, the perennial Kernza had comparable nitrate leaching to annual wheat,
and the differences in leaching between organic and synthetic N sources for
either crop type were minor. In year two, nitrate leaching (kg NO3 − N ha−1 )
from the two crop types and nitrogen sources were as follows: annual wheat
+ synthetic-N (27.5), annual wheat + organic-N (17.7), Kernza + synthetic-N
(0.5), and Kernza + organic-N (0.1). These findings suggest that disturbance
is compromising the ecosystem function of nutrient retention to a much
greater degree than plot size (all were small) or management approach
(conventional vs. organic).
Ecosystem functions performed by the belowground microbiome are
more subtly, but no less importantly, impacted by soil disturbance associated
with tillage. Culman et al. (2010) found bacterial and nematode commu-
nities to be significantly different in soils under perennial hay meadows
compared to annual wheat crops. In particular, the soils conditioned by
perennial species had higher populations of plant associate nematodes which
are non-parasitic, and have been reported to increase C and N mineraliza-
tion, microbial activity and plant growth (Culman et al. 2010). In another
comparison of perennial hay meadow and annual wheat soils, Crews and
Brookes (2014) found between 5 and 10 times more phosphorus (P) held
in microbial biomass in the perennial hay meadow soils at Rothamsted in
the United Kingdom. In general, the soils under perennial vegetation main-
tained greater phosphorus held in plant-available forms, and less P tightly
bound to iron and aluminum oxides. A final example of how microbially
mediated ecosystem functions can vary with succession was reported by
Robertson et al. (2014). They presented data from Levine et al. (2011) depict-
ing how methane-consuming soil bacteria (methanotrophs) increased along a
long successional gradient, with the lowest consumption occurring in highly
disturbed agricultural soils. Greater methane consumption in later succes-
sional soils equates to lower emissions of this potent greenhouse gas to the
atmosphere.
These examples support our belief that the development of peren-
nial grains could improve substantially on the ecological integrity of annual
grain agriculture, regardless of scale or management regime. The energetic
benefits of perennial grains will also likely benefit farmers across a wide
range of scales. Labor-intensive, small-scale grain farms stand to benefit from
perennial grain development since less work-energy inputs are expected for
vegetation clearing, plowing and weeding. Increasing the energy return on
investment in grain agriculture could pay off as reliance on fossil energy in
agriculture decreases in the future.
 Commentary: The Strong Perennial Vision: A Response 511

3. PERENNIAL GRAINS AND THE PIE OF LIMITED RESOURCES

The third concern that Smaje raises is that the SPV will divert “attention from
the importance of pursuing more diverse agroecological strategies, including
the weak perennial vision.” Smaje offers no data on trends in funding, litera-
ture published or cited to support this concern. Nor does he substantiate the
perception that groups working on what he calls the strong and weak peren-
nial visions are competing for attention and resources. It is our experience
that most researchers with these visions work together or at minimum sup-
port the work of each other. For example, The Land Institute helped to start
and continues to collaborate with the Green Lands Blue Waters organization
based in Minnesota (USA; http://greenlandsbluewaters.net). The mission of
Green Lands Blue Waters is to increase perennial cover on the landscape,
whether through planting buffer strips, agroforestry, annual cover crops, or
perennial grains.
If one were to query the publication history of this journal and oth-
ers that focus on ecology and agriculture (e.g., Agriculture, Ecosystems and
Environment), it would become clear that the research emphases of agroe-
cologists remain overwhelmingly on cover crops, agroforestry, no-till, buffer
strips, and diversifying annual cropping systems, as opposed to work on
breeding and growing perennial grains. An important funding stream for
perennial biofuel crops has developed over the last two decades in the
United States, European Union, and China, but to our knowledge, there have
been no designated programs on perennial grains by a government funding
agency in any country thus far.

4. CONCLUSION

Assuming that enhancing sustainability through crop breeding (combined

with sustainable management) is a worthy objective, we ask which barrier
is greater—breeding sustainability traits into annual crops, or breeding yield
into inherently sustainable perennial crops. For instance, Bell (2011) has
proposed breeding crops with larger and deeper roots. Hirel et al. (2007)
suggested an array of genetic approaches to increasing N use efficiency.
We believe these efforts will meet with limited success, not because of
where the plants are located on the C-S-R triangle (which is an average value
based on numerous traits), but because the season extension required to use
water, nutrients, and sunlight efficiently cannot be achieved when plants
must start each season from seed. Perennial crops capable of using the avail-
able resources have a unique role to play in sustainability (Asbjornsen et al.
2014).
In 2009, Rockström and colleagues identified planetary boundaries for
nine Earth-system processes that help define our planet’s habitability. They
512 T. E. Crews and L. R. DeHaan

propose that three of the boundaries have already been crossed—climate

change, rate of biodiversity loss, nitrogen cycle—leading to serious stress
on the predictability and dependability of Earth’s life supporting capacities.
Agriculture is squarely in the middle of these boundary overshoots, and
social reform of the food system is unlikely to deliver the biophysical changes
needed to return to what Rockström et al. call a safe operating space for
humanity. Addressing the inherent ecological shortcomings of low diversity
annual crop agriculture is one of the most promising approaches to achieving
a safe operating space.

ACKNOWLEDGMENTS

We would like to think David Van Tassel for his insights, conversations, and
generous contributions to the ideas presented in this article. We also appre-
ciate Chris Smaje’s willingness to have this response published alongside his
original work.

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