# Soil food webs in extreme environments > BIO 448: Geoecology > Spring 2024 > Dr. Yamina Pressler Thank you to Dr. Nishi Rajakaruna for inviting me to give a guest lecture! > [!example] Learning Objectives > - understand what soil food webs are, why they are important and how we study them > - evaluate controls on soil food web structure and function > - explore examples of soil food webs in harsh environments (desert soils, tundra soils, serpentinite soils) # Soils are one of the most biodiverse habitats on Earth! - Soils harbor perplexingly diverse biological communities[^diverse] - diversity is the number of species, taxa, or functional groups - Soils organisms are also incredibly abundant and ubiquitous - abundance is the number of individuals - for example, nematodes are the most abundant animal on earth[^nema] - Organisms within soils cross multiple spatial scales from the very tiny, single celled bacteria to the very large vertebrates like moles! - Check out the [Global Soil Biodiversity Atlas](https://www.globalsoilbiodiversity.org/atlas-introduction) for an excellent description of each group of soil organisms - Andy Murray shares an amazing collection of photos of soil microfauna here: https://www.chaosofdelight.org/ [^diverse]: Bardgett, R., van der Putten, W. Belowground biodiversity and ecosystem functioning. _Nature_ **515**, 505–511 (2014). https://doi.org/10.1038/nature13855 [^nema]: van den Hoogen, J., Geisen, S., Routh, D. _et al._ Soil nematode abundance and functional group composition at a global scale. _Nature_ **572**, 194–198 (2019). https://doi.org/10.1038/s41586-019-1418-6 # Why are soils so biodiverse? >[!question] Discussion question >Based on what you know about the soil environment, why are soils able to support such high levels of biodiversity? - **Spatial heterogeneity:** Soil formation creates diverse habitats and many environmental gradients (pH, redox, substrate quantity and quality) - **Temporal heterogeneity:** Soil organisms can go dormant in response to seasonal and environmental fluctuations - **Biotic and evolutionary mechanisms:** Soil microorganisms have long evolutionary history, short generation times, and potential for horizontal gene transfer that have all led to to speciation # How do we study soil food webs? We begin by classifying soil organisms into groups, and then we can describe interactions between groups. Classification approaches include: - biological (based on evolutionary relatedness) - morphological (based on body size and shape) - ecological (based on habitat and functions) Soil ecologists are interested in evaluating soil food webs in terms of: - structure (who is there and in what abundance) - function (what are they doing, how are they interacting) - dynamics (how do structural and functional properties change over time) Food web descriptions often include several classification approaches to characterize complexity of belowground interactions >[!question] Discussion question >What do soil organisms in the soil do? # Soil organisms interact in complex food webs - Food webs describe trophic interactions - feeding relationships among organisms - Basal resources are detritus, organic matter, and roots that serve as substrate (food) for consumers - Primary consumers are bacteria, archaea, fungi, and root-feeding nematodes - Secondary and tertiary consumers are microarthropods, protozoa, nematodes, and other microfauna - Predators include predatory nematodes and mites # How do we figure out who eats whom? > [!question] Discussion question > How do you think soil ecologists have figured out trophic interactions within the soil food web? - direct observations under a microscope - gut and fecal content analysis[^thimm] - stable isotope studies[^iso] [^thimm]:Thimm T, Hoffmann A, Borkott H, Charles Munch J, Tebbe CC. 1998. The Gut of the Soil Microarthropod _Folsomia candida_(Collembola) Is a Frequently Changeable but Selective Habitat and a Vector for Microorganisms. Appl Environ Microbiol 64:.[https://doi.org/10.1128/AEM.64.7.2660-2669.1998](https://doi.org/10.1128/AEM.64.7.2660-2669.1998) [^iso]:Crotty, F.V., Adl, S.M., Blackshaw, R.P. and Murray, P.J. (2012), Using Stable Isotopes to Differentiate Trophic Feeding Channels within Soil Food Webs[†](https://onlinelibrary.wiley.com/action/showCitFormats?doi=10.1111%2Fj.1550-7408.2011.00608.x#jeu608-note-0001). J. Eukaryot. Microbiol., 59: 520-526. [https://doi.org/10.1111/j.1550-7408.2011.00608.x](https://doi.org/10.1111/j.1550-7408.2011.00608.x) # How do we characterize soil food webs? - To describe soil food webs, we need to extract, quantify, and count soil organisms - There are many techniques to do so depending on the organism of interest that uses principles of their habitat and life history to capture their abundance - We spend a lot of time on the microscope to do this work! # Soil biota interact in complex soil food webs - For example, I studied a complex soil food web in Oklahoma[^pressler] - Trophic interactions lead to ecosystem processes - Soil organisms have been described as the "unseen majority" because they are hidden from view but still regulate many critical ecosystem processes[^unseen] [^pressler]:Pressler, Y., Wilson, G., Cotrufo, M.F. _et al._ Fire return interval influences soil food web structure and stability in an oak-pine savanna. _Plant Soil_ (2024). https://doi.org/10.1007/s11104-024-06646-2 # Trophic interactions help us understand how energy and matter flow through soils - We can use our understanding of soil biota biology to estimate rates of energy and matter flow through a food web - We use energetic efficiencies, C:N ratios, biomass from field samples, and known trophic preferences of each biota group to calculate rates of matter cycling - Hunt et al. 1987[^hunt] describes this approach in detail for the shortgrass prairie [^hunt]:Hunt, H.W., Coleman, D.C., Ingham, E.R. _et al._ The detrital food web in a shortgrass prairie. _Biol Fert Soils_ **3**, 57–68 (1987). https://doi.org/10.1007/BF00260580 # Energetic pathways emerge within soil food webs - We can compartmentalize soil food webs into energetic pathways[^moore]: - fungal pathway is based on recalcitrant litter and slower decomposition rates - bacterial pathway is based on labile litter and faster decomposition rates [^moore]: Moore, J. C., McCann, K., & de Ruiter, P. C. (2005). Modeling trophic pathways, nutrient cycling, and dynamic stability in soils. _Pedobiologia_, _49_(6), 499-510. https://www.sciencedirect.com/science/article/pii/S0031405605000545 [^unseen]: Van Der Heijden, M.G.A., Bardgett, R.D. and Van Straalen, N.M. (2008), The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters, 11: 296-310. [https://doi.org/10.1111/j.1461-0248.2007.01139.x](https://doi.org/10.1111/j.1461-0248.2007.01139.x) # What controls soil food web structure and function? - Soil organisms respond to changes in the soil environment, but the relative importance of each factor differs - Soil pH, organic carbon quality and quantity, and redox status are usually more important than predation and plant species identify for modifying the structure of soil bacterial communities[^fier] - Some soil biota exhibit threshold responses to changes in the environment (e.g. microarthropods and soil pH[^ph]) [^fier]:Fierer, N. Embracing the unknown: disentangling the complexities of the soil microbiome. _Nat Rev Microbiol_ **15**, 579–590 (2017). https://doi.org/10.1038/nrmicro.2017.87 [^ph]:van Straalen, N. M., & Verhoef, H. A. (1997). The Development of a Bioindicator System for Soil Acidity Based on Arthropod pH Preferences. _Journal of Applied Ecology_, _34_(1), 217–232. https://doi.org/10.2307/2404860 >[!question] Discussion question >Where do geology and parent material fit into these factors? - Underlying geologies will influence the formation of soil properties (e.g. texture, structure, nutrient status) # We can learn a lot from studying soil food webs in extreme environments - Studies of soil food webs in extreme environments have helped us understand more complex environments because the number of species in extreme environments (especially deserts) is much lower than temperate systems[^wall] - We will consider soil food webs in three extreme environments: - serpentinite soils - desert soils - tundra soils # Soil moisture, pH, and salt content are related to nematode abundance in Antarctic cold desert soils[^wall] - Differences in environmental parameters are associated with nematode presence and absence - These patterns vary for three different Antarctic nematode genera[^wall] # Climate is an important driver of soil food web structure - Soil microfood webs in the Antarctic Dry Valleys are less specious and complex than food webs in the Chihuahuan desert[^wall] # Mojave desert alluvial fans provide opportunities to study controls on nematode abundance - Treonis et al. 2019[^treo] conducted a study of soil nematode abundance along an alluvial fan in Death Valley National Park >[!question] Discussion question > How would you expect the soil environment to vary along this alluvial fan? # Plant composition & organic matter explain nematode abundance more than geomorphic position - Significantly higher nematode abundance under shrubs than between plants in Mojave desert[^treo] - Organic matter and salinity were the only two soil properties that differed in those two plant locations[^treo] - No differences in nematode abundance were observed between channels and on desert pavement on the alluvial fan[^treo] # Environmental factors that impact plant inputs and organic matter will cascade up to soil food web community composition - Organic matter was the strongest predictor of nematode abundance in Mojave desert soils [^treo] - This suggests a strong bottom-up effect where the availability of substrate (organic matter) controls the population size of nematodes # What makes the Arctic soil environment "extreme"? - In Alaska, permafrost is common at high latitudes and becomes more discontinuous further south - Permafrost soils pose unique challenges to soil biota including freeze-thaw conditions and saturated soil conditions - Organic material accumulates in mats on the mineral soil surface because decomposition rates are slowed by cold temperatures and wet conditions # Arctic soil food webs can be very complex - Koltz et al. 2018[^koltz] characterized the microbial-invertebrate food web in Arctic tundra soils including soil-dwelling biota and organisms living at the soil surface - Nutrient cycling emerges from complex connections between components of the food web [^koltz]:Koltz, A.M., Asmus, A., Gough, L. _et al._ The detritus-based microbial-invertebrate food web contributes disproportionately to carbon and nitrogen cycling in the Arctic. _Polar Biol_ **41**, 1531–1545 (2018). https://doi.org/10.1007/s00300-017-2201-5 # Detrital food web components contribute disproportionately to C and N cycling in Arctic food webs - Much larger biomass of fungivores in soil food web compared to predatory arthropods and canopy dwelling insects[^koltz] # Soil food web structure varies with soil horizon, but trophic heterogeneity is lost with climate warming - Soil food web composition is distinct in surface organic soils, deep organic soils, and mineral soils[^sistla] - However, when these same soils are warmed in a greenhouse experiment, the soil food webs are no longer structurally different[^sistla] - This suggests a "biotic awakening" with climate warming [^sistla]:Sistla, S., Moore, J., Simpson, R. _et al._ Long-term warming restructures Arctic tundra without changing net soil carbon storage. _Nature_ **497**, 615–618 (2013). https://doi.org/10.1038/nature12129 # Serpentinite soil conditions shape nematode diversity and energetic pathways - In a study of soil nematode communities in a temperate broad-leaved forest, Kitagami et al.[^serp] found distinct nematode community structure in serpentinite soils vs non-serpentinite soils - Nematode taxon richness was higher in serpentinite soils (but other biodiversity metrics did not differ between soil types) - Serpentinite nematode communities were dominated by fungal energetic pathway [^serp]: Kitagami, Y., Kawai, K., & Ekino, T. (2021). Soil physicochemical properties shape distinct nematode communities in serpentine ecosystems. _Pedobiologia_, _85_, 150725. https://doi.org/10.1016/j.pedobi.2021.150725 # Why? Let's consider potential mechanisms... >[!question] Discussion question >Based on what you know about serpentinite soils, why might soil conditions impact nematode communities? # Chemical properties of serpentinite soils explain distinct nematode communities - Differences in nematode communities were attributed to higher pH and higher Ni concentrations in the serpentinite soils[^serp] # Serpentinite soil conditions influence plant inputs - Litter from plants growing in serpentinite soils is more recalcitrant (difficult to decompose) than non-serpentinite litters[^decompose] - In Kitagami et al[^serp], serpentinite soils also had higher root biomass than non-serpentinite soils - Because plant litter is a basal resource for soil nematodes, shifts in quality and quantity of litter can lead to changes in nematode community composition - Fungi are able to consume recalcitrant litter in the "slow" cycle [^moore] [^decompose]: Nakamura, R., Kajino, H., Kawai, K. _et al._ Diverse recalcitrant substrates slow down decomposition of leaf litter from trees in a serpentine ecosystem. _Plant Soil_ **442**, 247–255 (2019). https://doi.org/10.1007/s11104-019-04183-x [^wall]: Wall, D. H., & Virginia, R. A. (1999). Controls on soil biodiversity: insights from extreme environments. _Applied Soil Ecology_, _13_(2), 137-150. https://doi.org/10.1016/S0929-1393(99)00029-3 [^treo]: Treonis, A. M., K. A. Sutton, S. K. Unangst, J. E. Wren, E. S. Dragan, and J. P. McQueen. 2019. Soil organic matter determines the distribution and abundance of nematodes on alluvial fans in Death Valley, California. _Ecosphere_ 10(4):e02659. [10.1002/ecs2.2659](https://doi.org/10.1002/ecs2.2659 "Link to external resource: 10.1002/ecs2.2659") # Take home messages - Soil food webs are diverse, complex, and dynamic over space and time - Geology influences the soil environment and plant growth - Soil environment and plant inputs control soil food web structure and function - Extreme environments are ideal systems to study all three # Notes and references