Excretion of nitrogenous waste by soil fauna and assessment of the contribution to soil nitrogen pools

Authors

DOI:

https://doi.org/10.25674/so94iss2id182

Keywords:

nitrogen cycle, ammonia, urea, sustainability, agricultural management

Abstract

The provisioning of nitrogen for plant growth is a key function of soils. Soil fauna primarily affect nitrogen mineralization through their interactions with microorganisms, but the excretion of feces and nitrogenous waste products can also supply plants with a considerable amount of their nitrogen requirements. The influence of soil fauna on soil nitrogen is rarely considered in agricultural soils. High amounts of mineral fertilizers are often applied, which are likely to be leached or denitrified from the soil if the amount of plant-available nitrogen exceeds crop requirements. This has profound consequences for the environment. Thus, we require a better understanding of the role of soil fauna in nutrient cycling to improve fertilizer management and agricultural sustainability. To this end, we review the current state of knowledge on the excretion of nitrogenous waste by soil fauna, focusing on earthworms, enchytraeids, nematodes, springtails, mites, isopods and myriapods. This includes an overview on excretory organs and products, a summary of quantitative measurements of nitrogen excretion and the factors that influence nitrogen excretion. Furthermore, we assess the contribution of soil faunal nitrogen excretion to nitrogen pools in agricultural fields based on mean nitrogen excretion rates and common soil invertebrate biomasses. Our results show that earthworms and nematodes are most likely to contribute agronomically-relevant quantities of nitrogen via excretion. Despite the very preliminary nature of our calculations, our results stress the importance of a better understanding of the role of soil fauna in nitrogen cycling in order to reduce soil-nitrogen losses and improve agricultural sustainability.

References

Abail, Z. & J. K. Whalen (2018): Selective ingestion contributes to the stoichiometric homeostasis in tissues of the endogeic earthworm Aporrectodea turgida. – Soil Biology and Biochemistry 119: 121–127.

Abail, Z. & J. K. Whalen (2019): Nitrous oxide in vivo emission may regulate nitrogen stoichiometry in earthworm body tissues. – European Journal of Soil Biology 91: 25–31.

Adlimoghaddam, A., M. Boeckstaens, A.-M. Marini, J. R. Treberg, A.-K. C. Brassinga & D. Weihrauch (2015): Ammonia excretion in Caenorhabditis elegans: mechanism and evidence of ammonia transport of the Rhesus protein CeRhr-1. – Journal of Experimental Biology 218: 675–683.

Adlimoghaddam, A., M. J. O’Donnell, A. Quijada-Rodriguez & D. Weihrauch (2017): Sodium-hydrogen exchangers in the nematode Caenorhabditis elegans: investigations towards their potential role in hypodermal H+ excretion, Na+ uptake, and ammonia excretion, as well as acid-base balance. – Canadian Journal of Zoology 95: 623–632.

Alberti, G., T. Kaiser & A. Klauer (1996): New ultrastructural observations on coxal glands (nephridia) of Acari. – In: Mitchell, R., D.J. Horn, G.R. Needham, W.C. Welbourn (eds): Acarology IX, Proceedings. – The Ohio Biology Survey, Columbus 1: 309–318.

Alberti, G., A. Seniczak & S. Seniczak (2003): The digestive system and fat body of an early-derivative oribatid mite, Archegozetes longisetosus Aoki (Acari: Oribatida, Trhypochthoniidae). – Acarologia 43: 149–219.

Babuthangadurai, A., A. Jawahar, P. Chitrarasu, S. Alawdeen & B. A. John (2014): Impact of stress on excretion in earthworm (Perionyx excavatus). – Journal of Sustainability Science and Management 9: 128–133.

Bahl, K. N. (1945): Studies on the structure, development, and physiology of the nephridia of oligochaeta VI. The physiology of excretion and the significance of the enteronephric type of nephridial system in Indian earthworms. – Journal of Cell Science s2-85: 343–389.

Bano, K., D. Bagyaraj & R. Krishnamoorthy (1976): Feeding activity of the millipede, Jonespeltis splendidus Verhoeff and soil humification. – Proceedings of the Indian Academy of Sciences-Section B 83: 1–11.

Bayley, M. & M. Holmstrup (1999): Water Vapor Absorption in Arthropods by Accumulation of Myoinositol and Glucose. – Science 285: 1909-1911.

Bayley, M., J. Overgaard, A. S. Høj, A. Malmendal, N. C. Nielsen, M. Holmstrup & T. Wang (2010): Metabolic changes during estivation in the common earthworm Aporrectodea caliginosa. – Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches 83: 541–550.

Bennett, D. (1971): Nitrogen excretion in the diplopod Cylindroiulus londinensis. – Comparative Biochemistry and Physiology Part A: Physiology 39: 611–624.

Bennett, D. & S. Manton (1962): Arthropod segmental organs and malpighian tubules, with particular reference to their function in the Chilopoda. – Annals and Magazine of Natural History 5: 545–556.

Bishop, S. H. & J. W. Campbell (1965): Arginine and urea biosynthesis in the earthworm Lumbricus terrestris. – Comparative Biochemistry and Physiology 15: 51–71.

Bocock, K. (1963): The digestion and assimilation of food by Glomeris. – In: Doeksen, J. & J. van der Drift (eds): Soil organisms. – North-Holland Publishing Company: Amsterdam, the Netherlands: 85–91.

Capelle, C. van, S. Schrader & J. Brunotte (2012): Tillage-induced changes in the functional diversity of soil biota – A review with a focus on German data. – European Journal of Soil Biology 50: 165–181.

Carefoot, T. (1993): Physiology of terrestrial isopods. – Comparative Biochemistry and Physiology Part A: Physiology 106: 413–429.

Cohen, S. & H. B. Lewis (1949): The nitrogenous metabolism of the earthworm (Lumbricus terrestris). – Journal of Biological Chemistry 180: 79–91.

Crotty, F. V., R. Fychan, R. Sanderson, J. R. Rhymes, F. Bourdin, J. Scullion & C. L. Marley (2016): Understanding the legacy effect of previous forage crop and tillage management on soil biology, after conversion to an arable crop rotation. – Soil Biology & Biochemistry 103: 241–252.

Curry, J. P. & D. Byrne (1992): The role of earthworms in straw decomposition and nitrogen turnover in arable land in ireland. – Soil Biology and Biochemistry 24: 1409–1412.

Curry, J. P., D. Byrne & K. E. Boyle (1995): The earthworm population of a winter cereal field and its effects on soil and nitrogen turnover. – Biology and Fertility of Soils 19: 166-172.

Dunger, W. & H. J. Fiedler (1997): Methoden der Bodenbiologie. – Gustav Fischer Verlag, Jena: 539 pp.

Edwards, C. A. & J. R. Lofty (1972): Biology of Earthworms. – Chapman and Hall Ltd, London: 283 pp.

Edwards, C. & P. Bohlen (1996): Biology and Ecology of Earthworms. – Chapman and Hall, London: 426 pp.

Edwards, C. A. (2004): Earthworm Ecology. CRC Press, Boca Raton: 456 pp.

Farzadfar, S., J. D. Knight & K. A. Congreves (2021): Soil organic nitrogen: an overlooked but potentially significant contribution to crop nutrition. – Plant and Soil 462: 7–23.

Fountain, M. T. & S. P. Hopkin (2005): Folsomia candida (Collembola): A “standard” soil arthropod. – Annual Review of Entomology 50: 201–222.

Greenaway, P. (1991): Nitrogenous excretion in aquatic and terrestrial crustaceans. – Memoirs of the Queensland Museum 31: 215–227.

Groenigen, J. W. van, I. M. Lubbers, H. M. J. Vos, G. G. Brown, G. B. D. Deyn & K. J. van Groenigen (2014): Earthworms increase plant production: a meta-analysis. – Scientific Reports 4: 6365.

Groenigen, J. W. van, K. J. van Groenigen, G. F. Koopmans, L. Stokkermans, H. M. J. Vos & I. M. Lubbers (2019): How fertile are earthworm casts? A meta-analysis. – Geoderma 338: 525–535.

Guhra, T., K. Stolze, S. Schweizer & K. U. Totsche (2020): Earthworm mucus contributes to the formation of organo-mineral associations in soil. – Soil Biology and Biochemistry 145: 107785.

Gutierrez-Lopez, M., S. Salmon & D. Trigo (2011): Movement response of Collembola to the excreta of two earthworm species: Importance of ammonium content and nitrogen forms. – Soil Biology & Biochemistry 43: 55–62.

Hartenstein, R. (1968): Nitrogen metabolism in the terrestrial isopod Oniscus asellus. – American Zoologist 8: 507-519.

Hilken, G. & J. Rosenberg (2006): Ultrastructure of the maxillary organ of Scutigera coleoptrata (Chilopoda, Notostigmophora): Description of a multifunctional head organ. – Journal of Morphology 267: 152–165.

Hoese, B. (1981): Morphologie und Funktion des Wasserleitungssystems der terrestrischen Isopoden (Crustacea, Isopoda, Oniscoidea). – Zoomorphology 98: 135–167.

Holmstrup, M. (2014): The ins and outs of water dynamics in cold tolerant soil invertebrates. – Journal of Thermal Biology 45: 117-123.

Hoogen, J. van den, S. Geisen, D. Routh, H. Ferris, W. Traunspurger, D. A. Wardle, R. G. M. de Goede, B. J. Adams, W. Ahmad, W. S. Andriuzzi et al. (2019): Soil nematode abundance and functional group composition at a global scale. – Nature 572: 194-198.

Hopkin, S. P. (1997): Biology of the springtails: (Insecta: Collembola). – Oxford University Press, Oxford: 330 pp.

Hopkin, S. P. & H. J. Read (1992): The biology of millipedes. – Oxford University Press, Oxford: 233 pp.

Hornung, E. (2011): Evolutionary adaptation of oniscidean isopods to terrestrial life: structure, physiology and behavior. – Terrestrial Arthropod Reviews 4: 95–130.

Humbert, W. (1978): Cytochemistry and X-ray microprobe analysis of the midgut of Tomocerus minor Lubbock (Insecta, Collembola) with special reference to the physiological significance of the mineral concretions. – Cell and Tissue Research 187: 397–416.

Kaersgaard, C.; Holmstrup, M.; Malte, H. & M. Bayley (2004): The importance of cuticular permeability, osmolyte production and body size for the desiccation resistance of nine species of Collembola. – Journal of Insect Physiology 50: 5–15.

Kirby, P. K. & R. D. Harbaugh (1974): Diurnal patterns of ammonia release in marine and terrestrial isopods. – Comparative Biochemistry and Physiology Part A: Physiology 47: 1313–1322.

Krantz, G. W. & D. E. Walter (2009): A manual of acarology. – Texas Tech University Press: 807 pp.

Larsen, T. (2007): Unravelling collembolan life belowground: Stoichiometry, metabolism and release of carbon and nitrogen. – PhD Thesis: Plant Nutrition and Soil Fertility Laboratory, Faculty of Life Sciences, University of Copenhagen,Frederiksberg, Denmark: 33 pp.

Larsen, T., J. Luxhoi, J. Magid, L. S. Jensen & P. H. Krogh (2007): Properties of anaerobically digested and composted municipal solid waste assessed by linking soil mesofauna dynamics and nitrogen modelling. – Biology and Fertility of Soils 44: 59–68.

Lassaletta, L.; Billen, G.; Grizzetti, B.; Anglade, J. & J. Garnier (2014): 50 year trends in nitrogen use efficiency of world cropping systems: the relationship between yield and nitrogen input to cropland. – Environmental Research Letters 9: 105011.

Maraldo, K., B. Christensen & M. Holmstrup (2011): The excretion of ammonium by enchytraeids (Cognettia sphagnetorum). – Soil Biology and Biochemistry 43: 991–996.

Marinissen, J. C. Y. & P. C. de Ruiter (1993): Contribution of earthworms to carbon and nitrogen cycling in agro-ecosystems. – Agriculture, Ecosystems & Environment 47: 59–74.

Needham, A. (1957): Components of nitrogenous excreta in the earthworms Lumbricus terrestris, L. and Eisenia foetida (Savigny). – Journal of Experimental Biology 34: 425–446.

Neher, D. A. & M. E. Barbercheck (1998): Diversity and function of soil mesofauna. – Biodiversity in Agroecosystems 27–47.

O’Donnell, M. J. & J. C. Wright (1995): Nitrogen excretion in terrestrial crustaceans. – In: Walsh, P. J. & P. A. Wright (eds): Nitrogen metabolism and excretion. – CRC Press, Inc: 105–118.

Omara, P.; Aula, L.; Oyebiyi, F. & W. R. Raun (2019): World Cereal Nitrogen Use Efficiency Trends: Review and Current Knowledge. – Agrosystems, Geosciences & Environment 2, 180045.

Osler, G. H. R. & M. Sommerkorn (2007): Toward a complete soil C and N cycle: Incorporating the soil fauna. – Ecology 88(7): 1611–1621.

Perry, R. N. & D. J. Wright (1998): The physiology and biochemistry of free-living and plant-parasitic nematodes. – CABI Publishing Series: 438 pp.

Rosenberg, J., A. Sombke & G. Hilken (2011): Chilopoda - excretory system. – In: Minelli, A. (eds): Treatise on zoology - anatomy, taxonomy, biology. The Myriapoda Volume 1. – Brill, Leiden: 177–195.

Rosenberg, J., A. Sombke & G. Hilken (2009): Structure and function of the maxillary nephridium of Lithobius forficatus (Chilopoda, Pleurostigmophora). – Journal of Morphology 270: 1531–1540.

Rothstein, M. (1963): Nematode biochemistry - III. Excretion products. – Comparative biochemistry and physiology 9: 51–59.

Salmon, S. (2001): Earthworm excreta (mucus and urine) affect the distribution of springtails in forest soils. – Biology and Fertility of Soils 34: 304–310.

Schimel, J. P. & J. Bennett (2004): Nitrogen mineralization: Challenges of a changing paradigm. – Ecology 85(3): 591–602.

Schmidt, O. & J. Curry (2001): Population dynamics of earthworms (Lumbricidae) and their role in nitrogen turnover in wheat and wheat-clover cropping systems. – Pedobiologia 45: 174–187.

Shutenko, G. S., B. P. Kelleher, A. J. Simpson, R. Soong, Y. L. Mobarhan & O. Schmidt (2020): Evidence for substantial acetate presence in cutaneous earthworm mucus. – Journal of Soils and Sediments 20: 3627–3632.

Sjursen, H. & M. Holmstrup (2004): Direct measurement of ammonium excretion in soil microarthropods. – Functional Ecology 18: 612–615.

Slotsbo, S.; Sørensen, J. G.; Stary, J. & M. Holmstrup (2017): Field and laboratory studies on drought tolerance and water balance in adult Pergalumna nervosa (Acari: Oribatida: Galumnidae). – European Journal of Entomology 114: 86-91.

Thaden, J. & R. Reis (2000): Ammonia, respiration, and longevity in nematodes: Insights on metabolic regulation of life span from temporal rescaling. – Journal of the American Aging Association 23: 75–84.

Thompson, D. P. & T. G. Geary (2002): Excretion/secretion, ionic and osmotic regulation. – In: Lee, D. L. (eds): The biology of nematodes. – CRC Press, Boca Raton: 291–320.

Tillinghast, E. K. (1967): Excretory pathways of ammonia and urea in the earthworm Lumbricus terrestris L. – Journal of experimental zoology 166: 295–300.

Tillinghast, E. K. & C. H. Janson (1971): Studies on the transition to ureotelism in the earthworm Lumbricus terrestris L. – Journal of Experimental Zoology 177: 1–7.

Tillinghast, E. K., D. C. McInnes & R. A. Duffill (1969): The effect of temperature and water availability on the output of ammonia and urea by the earthworm Lumbricus terrestris L. – Comparative Biochemistry and Physiology 29: 1087–1092.

Weihrauch, D. & M. O’Donnell (2017): Acid-base balance and nitrogen excretion in invertebrates: mechanisms and strategies in various invertebrate groups with considerations of challenges caused by ocean acidification. – Springer International Publishing Switzerland: 306 pp.

Whalen, J. K., R. W. Parmelee & S. Subler (2000): Quantification of nitrogen excretion rates for three lumbricid earthworms using 15N. – Biology and Fertility of Soils 32: 347–352.

Whalen, J. K. & C. Hamel (2004): Effects of key soil organisms on nutrient dynamics in temperate agroecosystems. – Journal of Crop Improvement 11: 175–207.

Wieser, W. (1972): O/N ratios of terrestrial isopods at two temperatures. – Comparative Biochemistry and Physiology Part A: Physiology 43: 859–868.

Wieser, W. & G. Schweizer (1970): A re-examination of the excretion of nitrogen by terrestrial isopods. – Journal of Experimental Biology 52: 267–274.

Wieser, W., G. Schweizer & R. Hartenstein (1969): Patterns in the release of gaseous ammonia by terrestrial isopods. – Oecologia 3: 390–400.

Woodring, J. P. (1973): Comparative morphology, functions, and homologies of the coxal glands in oribatid mites (Arachnida: Acari). – Journal of Morphology 139: 407–429.

Wright, D. J. (1975): Elimination of nitrogenous compounds by Panagrellus redivivus, Goodey, 1945 (Nematoda: Cephalobidae). – Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 52: 247–253.

Wright, D. J. (1998): Respiratory physiology, nitrogen excretion and osmotic and ionic regulation. – In: Perry, R. N. & D. J. Wright (eds): The Physiology and Biochemistry of Free-living and Plant-parasitic Nematodes. – CABI Publishing Series: 103–131.

Wright, J. & M. Odonnell (1993): Total ammonia concentration and pH of haemolymph, pleon fluid and maxillary urine in Porcellio scaber Lattreille (Isopoda, Oniscidea): Relationships to ambient humidity and water vapor uptake. – Journal of Experimental Biology 176: 233–246.

Wright, J., M. Odonnell & J. Reichert (1994): Effects of ammonia loading on Porcellio scaber: Glutamine and glutamate synthesis, ammonia excretion and toxicity. – Journal of Experimental Biology 188: 143–157.

Wright, J., S. Caveney, M. ODonnell & J. Reichert (1996): Increases in tissue amino acid levels in response to ammonia stress in the terrestrial isopod Porcellio scaber Latr. – Journal of Experimental Zoology 274: 265–274.

Wright, J. C. & M. Peña-Peralta (2005): Diel variation in ammonia excretion, glutamine levels, and hydration status in two species of terrestrial isopods. – Journal of Comparative Physiology B 175: 67–75.

Wright, P. A. (1995): Nitrogen excretion: three end products, many physiological roles. – Journal of Experimental Biology 198: 273–281.

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2022-08-01

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Lang, B., & Russell, D. J. (2022). Excretion of nitrogenous waste by soil fauna and assessment of the contribution to soil nitrogen pools. SOIL ORGANISMS, 94(2), 59–83. https://doi.org/10.25674/so94iss2id182

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