Agroecosystem resilience is modified by management system via plant–soil feedbacks

For my post-doctoral research project in the Menalled lab in 2016/2017, I was investigating the effect of farming system, weed competition, disease status, and climate change, on wheat production and soil bacteria during a growing season in Montana. All of these represent potentially stressful conditions, which can hamper plant growth, as well as the amount and type of root exudates they secrete into soil. Plants have a complex relationship with bacteria and fungi in the soil, and will provide sugars in exchange for microbial products. When conditions are harsh enough to threaten plant survival, like during droughts, plants may cut off support to soil microbes, which can cause the community to crash. Similarly, microbial communities may be unsupportive or pathogenic towards plants, and can hamper seed germination, as well as growth or health of plants.

We also wanted to know if adverse conditions during even just a single growing season would affect the microbial community enough to cause a change in plant growth during the next growing season – even if other conditions went back to normal. We took soil from the field at the end of the growing season and set up a greenhouse trial. To examine the impact of the microbial community, we set up paired comparisons where one half had the living field soil, and the other had field soil which had been autoclaved first to kill any microbes. The greenhouse trial involved hundreds of plant pots and thousands of data, and the seed germination and plant growth data was used to evaluate the legacy of stress.

This publication is part of a series, from data collected from a long-term farming experiment in Bozeman, MT, including:


Seipel, T., Ishaq, S.L., Menalled, F.D. 2019. Agroecosystem resilience is modified by management system via plant–soil feedbacks. Basic and Applied Ecology 39:1-9. Article.

Abstract

Designing resilient cropping systems is essential to sustain agricultural production in the face of changing environmental and social pressures. However, the extent to which changes in farm management systems could alter resistance and resilience is largely unknown, especially in response to climate change. Plant and soil microbial community interactions are a vital component of functioning and resilient agroecosystems. The aim of our study was to use winter wheat (Triticum aestivum L.) and pea (Pisum sativum L.) plant–soil feedbacks (i.e. plant species-specific effects on soil biotaand their impacts on subsequent plant growth) as a metric of system resilience and resistance to climate variability in three different farming management systems: 1) a chemical no-till system, 2) an USDA-certified organic system reliant on tillage and 3) an USDA-certified organic system that included sheep grazing with the overall goal of minimizing tillage intensity. Climate conditions soil experienced were ambient, warmer, and warmer and drier and were manipulated in the field using open-top chamber and rain-out shelters. Plant–soil feedbacks were negative for wheat and positive for pea but varied among farming management systems but were less sensitive to climate conditions. Plant–soil feedbacks were lower in magnitude in the tilled organic system indicating more resistance to the accumulation of pathogenic soil microbiotaresulting from repeated cropping of wheat. However, recovery was lower when the crop was pea in the tilled organic indicating slower recovery and less resilience. Results indicate that while increases in crop diversity may promote more resilient agroecosystems, farming management will affect agroecosystem resilience.

Ground Juniperus pinchotii and urea in supplements fed to Rambouillet ewe lambs. Part 2: Ewe lamb rumen microbial communities.

In 2015, while working in the Yeoman Lab, I was invited to perform the sequence analysis on some samples from a previously-run diet study.  The study was part of ongoing research by Dr. Travis Whitney at Texas A & M on the use of juniper as a feed additive for sheep.  Coupled with the animal health and physiology aspect led by Travis, we published two companion papers in the Journal of Animal Science.  We had also previously presented these results at the Joint Annual Meeting of the American Society for Animal Science, the American Dairy Science Association, and the Canadian Society for Animal Science in Salt Lake City, UT in 2016.

The three main juniper species in Texas can pose a problem- while they are native, they have significantly increased the number of acres they occupy due to changes in climate, water availability, and human-related land use.  And, juniper can out-compete other rangeland species, which can make forage less palatable, less nutritious, or unhealthy for livestock.  Juniper contains essential oils and compounds which can affect some microorganisms living in their gut.  We wanted to know how the bacterial community in the rumen might restructure while on different concentrations of juniper and urea.

There was not a large effect of treatment on the rumen bacterial community in lambs (Figure 1B).  There was a change in animal production (feed intake and weight gain) (Whitney, 2017), yet, because bacterial diversity was largely unchanged by the diet, this was likely because the diet treatments reduced feed intake.  Plant secondary compounds, often called dietary toxins, can make it harder for animals to maintain a stable body temperature as they change fermentation in the rumen and how much heat is produced.  This increases the metabolic cost of thermoregulation as animals continuously have to adjust their rate of metabolism to keep their body temperature stable.  To avoid eating too many of these plant compounds, herbivores employ feeding strategies, such as reducing feed intake. It is possible that lambs ingesting high concentrations of juniper in Texas during the late summer simply consumed less supplemental diet in order to reduce toxin- and fermentation-related heat generation.

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Figure 1B Principal coordinate analysis (PCoA) plot comparing OTU abundance in ewe lamb rumen samples over increasing juniper (J) or urea (U) supplementation by % DM. Vectors show significant effects (Pearson’s correlation P > 0.75) treatment, with vector length showing strength of correlation.

That’s not to say that there were no changes to the bacterial community at all; in fact, a number of important bacterial families were increased or decreased by increasing the amount of juniper, increasing the amount of urea, or both (Figure 2).

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Figure 2. Mean rumen bacterial abundance at the family level for ewe lambs on differing juniper (J) and urea (U) supplementations. Families are color coordinated by phylum: Bacteroidetes = red, Firmicutes = blue, Proteobacteria = orange, Spirochaetae = green, and other (dark grey) constitutes families with < 1% total abundance. Families of interest appear on the right side with positive (green) and negative (red) changes indicated as significant (P < 0.05) or trending (0.05 < P < 0.1) according to Student’s T-test.


Ishaq, S.L., Yeoman, C.J., Whitney, T.R. 2017. Ground Juniperus pinchotii and urea in supplements fed to Rambouillet ewe lambs. Part 2: Ewe lamb rumen microbial communities. Journal of Animal Science Oct; 95(10):4587-4599. Article.

Abstract

This study evaluated effects of ground redberry juniper (Juniperus pinchotii) and urea in dried distillers grains with solubles-based supplements fed to Rambouillet ewe lambs (n = 48) on rumen physiological parameters and bacterial diversity. In a randomized study (40 d), individually-penned lambs were fed ad libitum ground sorghum-sudangrass hay and of 1 of 8 supplements (6 lambs/treatment; 533 g/d; as-fed basis) in a 4 × 2 factorial design with 4 concentrations of ground juniper (15%, 30%, 45%, or 60% of DM) and 2 levels of urea (1% or 3% of DM). Increasing juniper resulted in minor changes in microbial β-diversity (PERMANOVA, pseudo F = 1.33, P = 0.04); however, concentrations of urea did not show detectable broad-scale differences at phylum, family, or genus levels according to ANOSIM (P > 0.05), AMOVA (P > 0.10), and PERMANOVA (P > 0.05). Linear discriminant analysis indicated some genera were specific to certain dietary treatments (P < 0.05), though none of these genera were present in high abundance; high concentrations of juniper were associated with Moraxella and Streptococcus, low concentrations of urea were associated with Fretibacterium, and high concentrations of urea were associated with Oribacterium and PyramidobacterPrevotella were decreased by juniper and urea. RuminococcusButyrivibrio, and Succiniclasticumincreased with juniper and were positively correlated (Spearman’s, P < 0.05) with each other but not to rumen factors, suggesting a symbiotic interaction. Overall, there was not a juniper × urea interaction for total VFA, VFA by concentration or percent total, pH, or ammonia (P > 0.29). When considering only percent inclusion of juniper, ruminal pH and proportion of acetic acid linearly increased (P < 0.001) and percentage of butyric acid linearly decreased (P = 0.009). Lamb ADG and G:F were positively correlated with Prevotella(Spearman’s, P < 0.05) and negatively correlated with Synergistaceae, the BS5 group, and Lentisphaerae. Firmicutes were negatively correlated with serum urea nitrogen, ammonia, total VFA, total acetate, and total propionate. Overall, modest differences in bacterial diversity among treatments occurred in the abundance or evenness of several OTUs, but there was not a significant difference in OTU richness. As diversity was largely unchanged, the reduction in ADG and lower-end BW was likely due to reduced DMI rather than a reduction in microbial fermentative ability.


Ishaq*, S.L., Yeoman, C.J., Whitney, T.R. 2016. Ground redberry juniper and urea in DDGS-based supplements do not adversely affect ewe lamb rumen microbial communities. Joint Annual Meeting, Salt Lake City, Utah, July 2016. (accepted talk). Travis Whitney’s companion presentation can be found here.

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Featured Image Credit: National Park Service