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The detritus-based microbial-invertebrate food web contributes disproportionately to carbon and nitrogen cycling in the Arctic

Polar Biology volume 41, pages 1531–1545 (2018)Cite this article

Abstract

The Arctic is the world’s largest reservoir of soil organic carbon and understanding biogeochemical cycling in this region is critical due to the potential feedbacks on climate. However, our knowledge of carbon (C) and nitrogen (N) cycling in the Arctic is incomplete, as studies have focused on plants, detritus, and microbes but largely ignored their consumers. Here we construct a comprehensive Arctic food web based on functional groups of microbes (e.g., bacteria and fungi), protozoa, and invertebrates (community hereafter referred to as the invertebrate food web) residing in the soil, on the soil surface and within the plant canopy from an area of moist acidic tundra in northern Alaska. We used an energetic food web modeling framework to estimate C flow through the food web and group-specific rates of C and N cycling. We found that 99.6% of C processed by the invertebrate food web is derived from detrital resources (aka ‘brown’ energy channel), while 0.06% comes from the consumption of live plants (aka ‘green’ energy channel). This pattern is primarily driven by fungi, fungivorous invertebrates, and their predators within the soil and surface-dwelling communities (aka the fungal energy channel). Similarly, >99% of direct invertebrate contributions to C and N cycling originate from soil- and surface-dwelling microbes and their immediate consumers. Our findings demonstrate that invertebrates from within the fungal energy channel are major drivers of C and N cycling and that changes to their structure and composition are likely to impact nutrient dynamics within tundra ecosystems.

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Acknowledgements

We thank Gaius R. Shaver, Jim Laundre, and the Arctic LTER for support and coordinating transportation to the study area. We are also grateful to Greg Selby and Rod Simpson for assisting with the sampling and processing of soil samples and Sarah Meierotto, Kiki Contreras, Kathryn Daly, and PolarTREC teacher Nell Kemp for assistance processing the aboveground arthropod samples. Logistic support was provided by Toolik Field Station, University of Alaska, Fairbanks, USA and CH2MHILL; Fig. 1 was generated by the Toolik GIS Office. Funding for this research was provided by the U.S. National Science Foundation (OPP-0908602, 0909507, 0909441, and DEB 1026843 and 1210704), CREOi, and the National Geographic Committee for Research and Exploration.

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Authors and Affiliations

  1. Department of Biology, Washington University in St. Louis, Box 1137, St. Louis, MO, 63130, USA

    Amanda M. Koltz

  2. Department of Biology, University of Texas at Arlington, Arlington, TX, 76109, USA

    Ashley Asmus

  3. Department of Biological Sciences, Towson University, Towson, MD, 21252, USA

    Laura Gough

  4. Natural Resource Ecology Laboratory, Colorado State University, Ft. Collins, CO, 80523, USA

    Yamina Pressler & John C. Moore

  5. Department of Ecosystem Science and Sustainability, Colorado State University, Ft. Collins, CO, 80523, USA

    John C. Moore

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  1. Amanda M. Koltz
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  3. Laura Gough
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  4. Yamina Pressler
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  5. John C. Moore
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Corresponding author

Correspondence to Amanda M. Koltz.

Additional information

This article belongs to the special issue on the “Ecology of tundra arthropods”, coordinated by Toke T. Høye and Lauren E. Culler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

300_2017_2201_MOESM1_ESM.pdf

Supplementary material 1 (PDF 89 kb). Taxon rarefaction curve for surface and canopy communities sampled in July 2013 near Toolik Lake, Alaska. A total of 33 taxa were sampled; Estimates of extrapolated species richness suggest that the surface and canopy community actually contains 40 ± 7.1 taxa, indicating that we were able to capture roughly 82.5% of the aboveground arthropod community with our sampling methods and at this level of taxonomic resolution

300_2017_2201_MOESM2_ESM.pdf

Supplementary material 2 (PDF 41 kb) Designations of functional feeding and trophic groups for all arthropod families sampled from canopy and surface habitats. Trophic groups were used in reporting the biomass and trophic structure of each habitat type (see main text; Fig. 2) and functional feeding groups were used in the energetics-based food web model (Fig. 3; Online Resource 3)

300_2017_2201_MOESM3_ESM.xls

Supplementary material 3 (XLS 45 kb) Parameters used to initialize the energetics-based food web model and the simulated C flow rates between all consumer functional feeding groups within the invertebrate tundra food web. Included are estimates of the C:N ratio, death rate (DR), assimilation efficiency (AE), production efficiency (PE), and biomass (mean and standard deviation) for each functional feeding group. We assumed that detritus, diatoms, lichen, moss, live plant biomass (roots, vascular plants, pollen), and blood were not limiting resources and thus assigned theoretical values of 2,500,000 g C m−2 to detritus, 300,000 mg C m−2 to diatoms, and 300 mg C m−2 to all others. Estimates of C flow rates (mg C m−2 year−1) are from the complete (sampled) food web with assigned feeding preferences (see methods in main text). Zeroes denote no consumptive relationship between groups. Cross-habitat feeding relationships (e.g., between soil- and surface-dwelling organisms or surface- and canopy-dwelling organisms) are indicated by boldface type

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Supplementary material 4 (XLSX 25 kb). Summarized model results from the complete, sampled food web and all food web manipulations. Food web manipulations included not specifying feeding preferences and removing each sampled functional feeding group from the network, one at a time, while holding the rest of the food web constant. The results shown here are the mean and standard errors from 1000 model runs for each food web configuration. Estimates for total C flow and all rates of organic and inorganic C and N cycling are for the entire food web and expressed in mg C or N m−2 year−1. S-min is a measure of stability, estimated by determining the value of ‘s’ needed to ensure that the real parts of all the eigenvalues of the matrix are negative (e.g., Moore and Hunt 1988; de Ruiter et al. 1995; Rooney et al. 2006; Moore and deRuiter 2012). An s-min value of one indicates that the diagonal strength ensuring stability of the food web is dependent solely on the specific death rates of the functional groups. Hence low s-min values (s-min ≤ 1) indicate more stable food webs relative to those with high s-min (s-min ≥ 1)

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Supplementary material 5 (PDF 1410 kb). Differences in the role of the invertebrate community in C consumption and cycling rates of organic and inorganic C and N between the complete, sampled food web versus those without feeding preferences or with individual functional feeding groups excluded (see “Methods” in main text)

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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

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  • DOI: https://doi.org/10.1007/s00300-017-2201-5

Keywords

  • Food web structure
  • Energetic food web model
  • Nutrient cycling
  • C mineralization
  • N mineralization
  • Invertebrate
  • Arctic
  • Tundra