Rapid transfer of C and N excreted by decomposer soil animals to plants and above-ground herbivores

Highlights

• Role of soil animals in nutrient cycling seen as indirect, slow, cumulative.

• N, C move rapidly from soil animals (earthworms) to plants and herbivores (aphids).

• Shown with stable isotope tracers under controlled conditions and in field.

• Findings suggest potential shortcut in the N cycle not recognised before.

Abstract

The role of soil decomposer animals in nutrient cycling is commonly seen as indirect, slow and cumulative, through grazing and engineering effects on soil microbes and their mineralization activities. Here, we show that nitrogen (N) and carbon (C) movement from living soil animals to plants and herbivores can be extremely rapid. In two complementary experiments under laboratory and field conditions, we used stable isotope tracers to follow nutrient transfer from earthworms to soil, wheat seedlings, and aphids. Earthworm-derived ¹⁵N and ¹³C was acquired by aphids after 2 h under laboratory conditions, and ¹⁵N after 24 h in the field. Since cleansed earthworms with voided guts were introduced, the main source of this ¹⁵N and ¹³C likely was their highly labelled cutaneous mucus. Based on the rapid tracer appearance in a phloem-feeding herbivore (whose principal N source is free amino acids), we postulate that organic earthworm-excreted compounds, possibly amino acids and acetates, may have been involved. This would suggest a previously unknown shortcut in the terrestrial N and C cycle, however, it requires confirmation through advanced techniques such as compound-specific isotope analysis or liquid chromatography with mass spectrometry. These experimental results suggest that multitrophic linkages from living decomposers in soil to plants and aboveground consumers may happen at much shorter time scales than is generally assumed.