Understanding N Fixation by Legume Cover Crops in Organic Vegetable Systems

Final Report for GW06-017

Project Type: Graduate Student
Funds awarded in 2006: $10,000.00
Projected End Date: 12/31/2009
Grant Recipient: University of California, Santa Cruz
Region: Western
State: California
Graduate Student:
Principal Investigator:
Carol Shennan
University of California, Santa Cruz
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Project Information


This project was part of our work to examine asynchronies in N availability and uptake in organic vegetable production on California’s Central Coast. While biological N fixation (BNF) is an important part of N budgets and models, there are no BNF estimates for two important winter legume cover crops, bell beans (Vicia faba) and woollypod vetch (Vicia villosa). We evaluated a key assumption underlying the natural abundance method of estimating BNF, developed regional BNF estimates for bell beans and woollypod vetch, and determined how a range of BNF estimates affects the balance of N budgets for organic vegetable systems.


Legume or legume-mix (e.g., with grasses) cover crops can play a key role in the fertility management of agroecosystems, particularly by providing N through biological N fixation (BNF) with Rhizobium symbionts. Because of its importance, BNF is a necessary component of N budgets, tools used to compare agroecosystem N inputs and outputs and thus determine the potential for N loss via leaching or denitrification and any change in soil N storage. If N budgets show significant surpluses, growers and researchers can consider alternate fertility management practices to reduce potential N loss and thus reduce the negative impacts of N on the environment (Vitousek et al. 1997, Johnson et al. 2007) and human health (Wolfe and Patz 2002, Townsend et al. 2003). Accurate estimates of BNF in N budgets allow the separation of the contribution of atmospheric N from the contribution of soil N to plant growth. Significant underestimates of BNF would underestimate the N surplus of a system, while significant overestimates of BNF would lead to overestimates of N surplus.

In the past 20 years, the 15N natural abundance method (Shearer and Kohl 1986) has gained popularity as a means to estimate BNF. Like the traditional difference method, the natural abundance method compares a legume and a non-fixing “reference” plant grown under the same conditions. The difference method compares the total N content of the legume and reference plant and attributes any difference to BNF. However, the choice of reference species can have a strong influence on the estimate of fixation because it assumes the legume and reference plant have similar spatial and temporal soil N uptake patterns under the same growing conditions. This is dependent on growing conditions, and, as Unkovich and Pate (2000) show in a review of BNF estimation methods, is highly variable among years and can lead to “the unsatisfactory conclusion” that BNF is negative if the legume has lower biomass and total N than the reference plant. Unkovich and Pate (2000) conclude that available data show the difference method to be “unreliable” overall.

Alternately, the natural abundance method compares isotopic signatures (15N/14N, or δ15N) of the legume and reference plant. In N isotope studies, the atmospheric δ15N is set as 0. Biological processes discriminate against 15N, so nutrient pools that are high in biologically-transformed N are enriched (i.e., have a higher δ15N) compared to the atmosphere. In the natural abundance method, the reference plants grown in soil are assumed to have a δ15N signature that integrates the signature of the available soil N over the growing season (Boddey et al. 2000), while N-fixing legumes are assumed to have a signature that combines soil and atmospheric N signatures. Thus BNF is calculated as:

%Ndfa = 100(δ15Nref - δ15Nleg)/(δ15Nref - B)

where %Ndfa is the % of N derived from the atmosphere, δ15Nref is the signature of a non-legume cover crop in field plots, δ15Nleg is the signature of a legume cover crop in field plots, and B is the δ15N signature of a legume when all N is derived from fixation (Shearer and Kohl 1986).

One methodological challenge of the natural abundance method is that, as for the difference method, the choice of reference species can be important. For optimal accuracy of estimating BNF, the reference plant and legume ideally should have similar N uptake patterns, both spatially and temporally, as well as similar growth responses to a given climate and soil environment (Pate et al. 1994). A non-nodulating isoline may be the best candidate because of similarities in growth habit and phenology, however such isolines are not available for many legumes. Instead, a reference plant with N uptake patterns that correlate well with those of the legume may be suitable for use in N budgets. This use of reference species assumes that the pools of N accessed by the legume and reference are the same.

Biological N fixation by winter legume cover crops is an important component of fertility management in organic vegetable systems in California’s Central Coast, particularly as legume-cereal mixes on relatively small (<100 ha) organic farms (Brennan and Smith 2005). Bell beans (Vicia faba, same species as faba beans), woollypod vetch (Vicia villosa ssp. dasycarpa) and other legumes commonly are grown in a mix with cereals, particularly oats (Avena sativa). Growers in the region assume that 50% of cover crop N, or about 60-150 kg N/ha, is fixed annually (J. Leap, pers. comm.). This fixation estimate is a rule of thumb; despite widespread use of legume-oat mixes, there are few specific estimates of N fixation for bell beans and vetch in the Central Coast. As tighter N management is encouraged by regulatory agencies, more accurate estimates based on specific, regional data may help growers track the relative input and output of N sources and minimize potential N loss. We have been working to estimate BNF for bell beans and vetch in the Central Coast. Our initial research indicated that the assumption that the legumes and their reference species used the same N pools may be problematic. We planted vetch, bell beans and two reference species (oats and mustard) in single-species plots in five sites with a range of 1-8 yrs since last compost application. All plots were on the same organic farm to minimize soil type and climatic differences. Aboveground biomass was analyzed for δ15N. The data showed that the number of years since compost application was negatively correlated with δ15N of the reference species but had no relationship with δ15N of the legumes. This indicated that the reference and legume species were accessing different pools of soil N, with the reference species taking up more available N from the compost than the legumes. Following on this, we proposed two main objectives for this project. First, we wanted to determine if the N sources used by the legumes were the same as those used by the reference species. Second, we wanted to determine how different estimates of BNF would affect N budgets for vegetable production systems that use cover crops as part of fertility management.

Project Objectives:

Objective 1. Determine if N sources used by legumes and reference species are the same
To better understand which N sources are used by each species in this system, we proposed two projects:

1. Field experiment: We planned to insert metal sleeves 1 m deep in the soil to create two replicates of eight 0.25-m2 plots at five sites on a single farm that we used for our earlier work. Each set of plots would be planted with oats (non-fixing reference plant) and vetch (legume) grown in four fertility treatments (no, low, moderate and high additional N applied as liquid fish emulsion). Aboveground biomass would be sampled four times and dried, ground plant samples would be submitted to UC Davis for δ 15N analysis, along with soil samples. This would allow us to compare the sources of N each species is using at different points during the growing season.

2. Field observation: We planned to harvest aboveground biomass of 10 individuals of oats, bell beans and vetch at three farms every three weeks during the winter, then analyze the samples for total aboveground N. This would allow us to compare N uptake among the plants during the winter.

Objective 2. Determine how much over- or underestimates of fixation affect the N balance of organic vegetable production systems in this region
We planned to construct an N input and output budget for the farm used in the experiments in Objective 1. We would also use three models to examine N dynamics in local organic vegetable systems. We would then compare budget inputs and outputs to estimate the N balance, as well as the sensitivity of the balance to a range of fixation estimates, based on our previous work. In addition, we would test the models for ability to predict NO3- concentrations in soil and soilwater, and see what changes in fixation estimates cause in the models’ output under average, wetter and drier climate conditions.

Objective 3. Educate growers, researchers and advisors on how much N legume cover crops add to organic vegetable productions in this region and its importance to the system
As part of a network of organic vegetable and strawberry producers, researchers, advisors and NGO and industry representatives from California’s Central Coast, we would share our research findings at our 2-3 meetings each year. We also would publish the results in a research brief through the Center for Agroecology and Sustainable Food Systems at UC Santa Cruz.


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  • Carol Shennan


Materials and methods:

Objective 1.
1. Field experiment. We planted the field experiment outlined above in Dec. 2005 at the Center for Agroecology and Sustainable Agriculture (CASFS) organic teaching and research farm at the University of California Santa Cruz. Instead of inserting metal sleeves in the soil to create replicates, we buried bottomless plastic pots and planted them with oats or vetch, as described above. After planting, we experienced high seed predation in several fields, probably due to birds and rodents, and many of the seedlings that germinated were killed by slug predation in mid to late Dec. A second round of seeds planted in early Jan. also was greatly damaged by slugs. By then much of the fertilizer we had applied had probably been leached during rain events, so we decided to end the experiment and try it again. Meanwhile we had realized that the lack of a response by the legumes to cover crop history in our earlier field studies could indicate high BNF, not just a different use of soil N sources by the legume and reference plants.

We modified and expanded the experiment for the greenhouse to avoid predation problems and to answer two questions. The questions broadened what we were trying to understand in our original objective, examining the overall suitability of reference species and any differences in BNF estimates in sites with different N fertility. The questions were: 1) does %Ndfa vary within and across farm sites (including ones with different compost histories) and with fertility level, and 2) are oats an appropriate reference species for estimating vetch %Ndfa, and 3) if %Ndfa does vary with fertility, can oat biomass or oat total N uptake serve as a proxy for estimating relative soil fertility? If so, fixation estimates used in nutrient budgets or models could be adjusted depending on soil fertility levels.

Seven oat or vetch seeds were planted in late Oct. 2006 in fertility-amended field soil in 983-ml pots (Fig. 1 and 2). Topsoil collected from six farm sites was used as the growing medium; the sites were four fields at the UC Santa Cruz farm (Farm A, including two fields in production ~ 25 years that received compost nine years ago (“main field”) and eight years ago (“rock field”), the farm orchard, which has received no compost, and an uncultivated (“natural”) area, which also has received no compost) and two organic farms in Watsonville, CA (Farms B and C). Prior to planting, the soil in each pot was sieved and mixed with Phytamin organic fertilizer added at the rate of 0, 75, 125 or 200 kg N/ha, with 5 replicates per species x soil source x fertility treatment. After emergence, plants were thinned to 3 per pot.

Plants were destructively harvested 17 weeks after emergence. Plants from each pot were separated into above-and belowground biomass. Roots were washed, and all above- or belowground biomass from each pot was combined. The plants were oven-dried at 70 C for three days, weighed, and ground on a Thomas-Wiley mini-mill. Dried plant matter was analyzed on a continuous flow isotope ratio mass spectrometer at the UC Davis Stable Isotope Lab for δ15N.

We calculated the mean oat and vetch biomass for each soil source x N fertility treatment, but because the 5 replicates of the oats and the vetch in each treatment were fully randomized in their location on the bench, we could not use oat-vetch pairs to calculate 5 %Ndfa estimates and a treatment %Ndfa mean. Instead we used bootstrapping to randomly draw with replacement 5 oat replicates and 5 vetch replicates in each treatment (Resampling Stats for Excel 2003, Statistics.com, Arlington, VA). The new pairs of replicates were used to calculate 5 estimates of %Ndfa and the mean and standard deviation of the %Ndfa for the treatment. A two-way ANOVA for oat biomass was calculated in Excel.

2. Field observation. To determine aboveground biomass and N uptake over the winter, we harvested aboveground biomass of 5 individuals of each cover crop species in oat-legume experimental plots at Farm A and 10 individuals of each cover crop species from Farms B and C in oat-legume fields. The plants were harvested approximately every four weeks from the time of planting in fall through incorporation in 2005-06. Harvested plants were weighed, dried at 70 °C for three days and reweighed to determine dry biomass. The stored plant samples were damaged so we were unable to estimate N uptake. However, we were able to analyze cover crop samples from previous work at Farms A and B (2004-05) and thus examine changes in %N over the season. Samples were analyzed for %N with a vario Max combustion gas analyzer (Elementar Americas, Inc., Mt. Laurel, NJ).

Objective 2.
We worked with the growers at Farms A and B to develop multi-year budgets of N inputs and outputs based on farm records. Inputs included cover crops and other fertility amendments (e.g., compost or feather meal), assuming 50% of the cover crop N was fixed atmospheric N (and therefore a new input). Outputs were removal by harvested crops, using available estimates of crop N content from the literature. To determine how the choice of BNF estimate affects the balance of the N budgets, we calculated the mean annual surplus N for the budgets for BNF estimates from 50 to 95% (based on the range of values we saw in the greenhouse study).

We also are sharing the data with two teams of modelers, one using NDICEA (Nitrogen Dynamics In Crop rotations in Ecological Agriculture) (Habets and Oomen 1994) and the other using DNDC (DeNitrification and DeComposition) (Li et al. 1992, Li 2000), through a collaboration under another USDA-CSREES grant. The results of the modeling efforts are forthcoming.

Research results and discussion:

Objective 1.
1. Greenhouse experiment (previously the field experiment).
Results: In our greenhouse study, we saw little evidence of a relationship between site N fertility and %Ndfa. The four fields at Farm A showed no single, strong relationship between %Ndfa by vetch and fertility treatment, and mean %Ndfa varied widely by field (Fig. 3), with means as low as 14% and as high as 100% (values greater than 100 are biologically impossible). Similarly, when comparing across farms, no striking negative relationship between estimated %Ndfa by vetch and added N was observed, except perhaps for Farm C (Fig. 3), although both Farms B and C had overall high BNF estimates. A two-way ANOVA shows a significant effect of both farm and the farm x fertility interaction, but not N addition (Table 1).

In evaluating oats as a reference species for vetch, we found that mean total above- and belowground oat biomass was negatively correlated with mean total vetch biomass for each site (Fig. 4), although the strength of fit varied. Soils from Farm C had the strongest correlation (y = -0.51x + 21, R2 = 0.90), soils from Farm B had a moderate correlation (y = -0.37x + 18, R2 = 0.39), and the Farm A main field soils had the weakest relationship (y = -0.70x + 15, R2 = 0.25). The relationship between mean vetch %Ndfa and mean oat N uptake varied by site (Fig. 5). Soils from Farm A had a very strong positive correlation (y = 1100x -19, R2 = 0.94) while soils from Farms B and C had weak relationships (Farm B: y = 71x + 85, R2 = 0.17; and Farm C: y = -147x + 87, R2 = 0.03).

Oat biomass was not strongly correlated with site or fertility treatment (Table 2), although the site x fertility treatment effect approached statistical significance at the 95% confidence level. Oat N uptake was not significantly correlated with site or fertility treatment, and did not have a significant site x fertility treatment interaction (Table 3).

Discussion: The lack of a single, strong relationship between site N fertility and %Ndfa may have multiple contributing factors. Rochester and Peoples (2005) saw some evidence of suppression of N fixation by vetch in high mineral N environments, although they refer to research by Kurdali et al. (1996) that showed vetch was a weak competitor for mineral N, which led to high vetch %Ndfa estimates. In the only study we have found on the effect of organic fertility management on N fixation, Oberson et al. (2007) specifically examined the difference in BNF by soybean in the same biodynamic, bioorganic and conventional plots used by Mäder et al. (2002). The authors found the highest %Ndfa in organic systems and conventional systems that received both organic and mineral fertilizers and the lowest %Ndfa in conventional systems with exclusively mineral fertilizers. However, Obserson et al. (2007) also found that although the plants were well nodulated, the %Ndfa estimates were low to medium (24 to 54%) for all cropping systems, with more N removed through harvested grain than was added by BNF. Oberson et al. (2007) suggest that inherently high soil N mineralization and/or low soil P availability of the field site may have limited BNF in all treatments. Farm A generally has high inorganic labile P fractions (Abboud 2002), which may help support the high BNF levels in the main field. The high labile P fractions could also help explain high BNF rates for Farms B and C in the greenhouse study, particularly since Farm B was formerly the site of a dairy and both farms receive animal-derived fertility amendments. However, the high %Ndfa estimates for the orchard (which previously had no legume cover crops) and the natural area (which previously had no legume cover crops or compost applications) may be due to low soil N mineralization. Further studies of N mineralization and P availability over the winter might help elucidate the potential contribution of these factors to the high BNF in the different sites.

Although the BNF estimates in our study were often well above the 50% benchmark commonly used in estimating cover crop N fixation for nutrient budgets, they generally fell within the range of values in the literature. For example, in a six-yr study of winter-planted legumes in rotation with cotton in Australia, both V. villosa and V. faba had generally high fixation estimates, with 89-92%Ndfa for V. villosa and 79-84%Ndfa for V. faba (Rochester and Peoples 2005). Similarly, Kilian et al. (2001) found 69 to 86% Ndfa for faba beans and Rochester and Peoples (2005) found 89 to 92%Ndfa for woollypod vetch over three years.

The high fixation estimates in the greenhouse study were driven by the large difference between the δ15N signatures of the oats and vetch. Although Unkovich and Pate (2000) caution against using cereals as reference species due to differences in root architecture and plant N demand and uptake, the cereals (oats and triticale) and dicots (mustard and phacelia) used in other studies of ours gave similar BNF estimates. Unkovich et al. (1994) performed a sensitivity analysis to test the effect of different reference plant δ15N values on estimated %Ndfa. They showed that for high BNF estimates, which occur when the legume δ15N is close to 0, the reference plant signature has little effect, whereas for low BNF estimates, the reference plant signature has a strong effect. With the low legume δ15N in our studies, reference plant signature generally had little effect on BNF estimates, and under these conditions, oats appear to be a satisfactory reference plant for estimating BNF.

Although oats appear to be suitable as a reference plant in this system, their use as a proxy is not. Because vetch BNF did not vary predictably with N fertility in our greenhouse study, a proxy for use in budgets would be inappropriate. This is especially the case for oats as a proxy, given that oat biomass and N uptake were not correlated with fertility treatment. The lack of oat response to fertility suggests that oat growth may not be limited by soil nitrogen fertility at the fertility levels commonly found in organically fertilized vegetable fields in the region. Similarly, Muurinen et al. (2007) found that oats had high N uptake efficiency that did not vary across years, even though total grain yield varied significantly.

2. Field observation.
Results: Cover crop growth was moderate in Dec. at all three farms. Above-ground biomass increased in Jan. for all three species at Farms B and C and for oats at Farm A, and increased in Feb. for bell beans and vetch at Farm A (Fig. 6). The oats had a similar uptake pattern to bell beans, with the largest increases in aboveground biomass occurring at approximately the same time. Vetch had much lower biomass than oats and bell beans in the last 1-2 months of growth (Fig. 6).

The cover crop samples from 2004-05 showed that the %N content of cover crops varied over the course of the growing season. The mean %N content was generally high early in the season and lower later in the season, when the legumes had higher mean %N than oats (Fig. 7). The final %N ranged from 0.8 to 2.2%.

Discussion: Bell beans and oats had similar increases in biomass over the winter and similar N demand early in the season, indicating that oats may be a good reference species for bell beans, though not for vetch. Although Unkovich and Pate (2000) caution against using cereals as reference species due to differences in root architecture and plant N demand and uptake, oats appear to work well in this case for bell beans, which have vigorous, tall growth.

However, the results from the greenhouse study showed that the field has a large effect on the BNF estimate through its influence on vetch δ15N. In another field study we completed as part of our research program, we found that the choice of reference species had a smaller effect on the magnitude of the estimates than the field itself did. We evaluated four reference species (oats, triticale, x Triticosecale, mustard, Brassica juncea, Pacific Gold cv., and phacelia, Phacelia tanacetifolia) in six fields at the CASFS Farm. Te cereals (oats and triticale) and dicots (mustard and phacelia) used in our field study gave similar BNF estimates. Similarly, in a study of six faba bean cultivars, Kilian et al. (2001) found that although a non-nodulating faba bean cultivar gave fixation estimates that were about 10% lower than those calculated with cabbage or ryegrass as reference plants, the choice of reference plant did not affect the ranking of the six cultivars based on %Ndfa or the quantity of N2 fixed. Likewise, in a study of pasture legumes, Goh (2007) found that matching the reference plant to the legume had less of an effect on %Ndfa estimates (which were 50 to 90%) than differences in season and irrigation did. With the low legume δ15N in the field study, reference plant signature generally had little effect on BNF estimates. For example, signatures of 5.3‰ for oats and 7.1‰ for mustard from the same field led to bell bean fixation estimates of 89 and 92%Ndfa. The effect was stronger when legume δ15N was higher: in that same field, vetch had a much higher δ15N than bell beans (1.73 vs. 0.57‰), and vetch showed a larger difference in %Ndfa based on the two reference species (66% with oats and 75% with mustard).

Objective 2.
Results: Multi-year field-scale N budgets for Farm A (Table 4) and Farm B (Table 5) assuming 50% of legume cover crop N was derived from fixation had positive N balances of 354 and 764 kg N/ha, respectively. Surplus N over time increased substantially for both farms when the estimated contribution from N fixation increased (Fig. 8). Changing the BNF budget line from 50 to 95% Ndfa increased the annual surplus N from 51 to 129 kg N/ha at Farm A and from 153 to 251 kg N/ha at Farm B.

Discussion: Without oat biomass or N uptake as an appropriate proxy, the question remains as to how to determine what the appropriate BNF estimate is to use in N budgets, particularly given the substantial difference in mean annual surplus N in the two budgets we constructed. While choice of reference plant had a relatively small effect on %Ndfa, combining this factor with differences among field sites leads to a range of BNF estimates. However, through these studies we have found that most BNF estimates for these cover crops is well above 50%, meaning N inputs likely have been underestimated. Perhaps the most prudent course of action for budgets including legume cover crops in this region is to use low, medium and high estimates for each legume cover crop to estimate their contribution to N inputs. Thus by developing more accurate estimates of N fixation specific to agroecosystem management methods and climatic conditions we may help growers learn to manage these systems with smaller N surpluses and a lower likelihood of N loss.

Objective 3.
We have shared our findings with the growers and researchers in our network, including the two growers whose farms were research sites for this work. We presented results at the Sustainable Ag Expo in Paso Robles, CA, in Nov. 2007 and at the National Conference on Agriculture and the Environment in Asilomar, CA, in Nov. 2007. These conferences included Central California growers, researchers, and farm advisors. We will continue to share the results at network meetings and other conferences. We also have a draft pamphlet describing these results, particularly the N budgets and the effects of different BNF estimates on N balances, and how to access a web-based tool that will allow growers to construct N budgets for their own production sites. The pamphlet will be printed and distributed through the network, conferences, and the Center for Agroecology and Sustainable Food Systems at UC Santa Cruz.

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Brennan E.B., and R.F. Smith. 2005. Winter cover crop growth and weed suppression on the central coast of California. Weed Technology 19:1017-1024.

Goh K.M. 2007. Effects of multiple reference plants, season, and irrigation on biological nitrogen fixation by pasture legumes using the isotope dillution method. Commun. Soil Sci. Plant Anal. 38:1841-1860.

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Oberson A., S. Nanzer, C. Bosshard, D. Dubois, P. Mäder, and E. Frossard. 2007. Symbiotic N2 fixation by soybean in organic and conventional cropping systems estimated by 15N dilution and 15N natural abundance. Plant and Soil 290:69-83.

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Participation Summary

Research Outcomes

No research outcomes

Education and Outreach

Participation Summary:

Education and outreach methods and analyses:

Publications: This project partially supported two dissertation chapters (both of which will be submitted to journals for publication) and a paper in a forthcoming proceedings:

Monsen, K.L. 2008. Nitrogen input and leaching in the winter in organic vegetable agroecosystems in a Mediterranean climate. Chapter 1 in Managing nitrogen in organic vegetable agroecosystems on California’s Central Coast. University of California Santa Cruz.

Monsen, K.L. 2008. Biological nitrogen fixation estimation in legume cover crops. Chapter 2 in Managing nitrogen in organic vegetable agroecosystems on California’s Central Coast. University of California Santa Cruz.

Monsen, K.L., and C. Shennan. Forthcoming. A tale of two legumes: what isotopes tell
us about optimizing N management with legume cover crops in vegetable systems. To be published in the proceedings of the National Conference on Agriculture and the Environment, Asilomar, CA, 2007.

Education & outreach:
Monsen, K.L., and C. Shennan. 2007. A tale of two legumes: what can isotopes and models tell us about optimizing N management with legume cover crops in organic vegetable systems? National Conference on Agriculture and the Environment. Oral presentation. Asilomar, CA.

Monsen, K.L., and C. Shennan. 2007. Estimating winter cover crop nitrogen fixation on the Central Coast. Sustainable Ag Expo. Oral presentation. Paso Robles, CA.

Monsen, K.L., and C. Shennan. 2007. Lazy legumes or busy beans? High N fixation rates of winter cover crops across soil fertility levels. Ecological Society of America Annual Meeting. Oral presentation. San Jose, CA

Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture or SARE.