Our global food production system faces the unprecedented challenge of feeding a rapidly increasing world population while simultaneously reducing its environmental footprint1. It is still far from clear whether such a “sustainable intensification”2 can be achieved. In particular, the question of what determines the yield gap between more sustainable forms of agriculture and those of conventional agriculture and how to close that gap, is still widely debated3,4. Earthworms are generally thought to be essential to sustainable agroecosystems. They rank among the most important soil fauna and as ‘ecosystem engineers’ they are instrumental to several ecosystem services the soil provides, such as nutrient cycling, drainage and regulating greenhouse gas emissions5,6. However, it is their supposed ability to stimulate crop growth that might be of foremost relevance to agriculture. This ability was already suggested in an age before artificial fertilizers and mechanization provided a short-cut towards higher crop production7,8.

Although positive effects of earthworms on plant growth have been repeatedly described9,10, quantitative proof has remained elusive and mechanisms through which it might be exerted have never been satisfactorily established. Yet, this information is essential to determine whether earthworms can help to fill the yield gap between sustainable and conventional agriculture. Such an effort has previously been hampered by the wide variety of conditions (climate, soil fertility, crop types, earthworm species and farm management) under which the effects of earthworms have been studied, making it difficult to determine the global effect of earthworms response from individual observations. A quantitative synthesis of results across multiple studies can overcome this problem. Here, for the first time, we use meta-analysis to summarize the effect of earthworms on plant production across the globe (see Methods). We collected 462 data points from 58 studies that were published between 1910–2013 (Supplementary Table 1). Studies include the three main global staple crops (maize, rice and wheat), pastures, as well as many other food crops and were conducted on all continents except Antarctica.

We assessed the generality of the effect of earthworm presence on six key plant response variables: (1) crop yield; (2) aboveground biomass; (3) belowground biomass; (4) total biomass; (5) shoot/root ratio (as a proxy for carbon allocation towards harvestable products); and (6) nitrogen (N) concentration in aboveground biomass (as a proxy for crop quality) (Supplementary Tables 2–5). Earthworm presence significantly increased crop yield by +25%, aboveground biomass by +23%, belowground biomass by +20% and total biomass by +21% (Fig. 1). Shoot/root ratio was not significantly different from zero, indicating no proof of altered carbon allocation towards aboveground plant parts11. Nitrogen concentration in aboveground biomass was also unaffected by earthworm presence (Fig. 1), indicating that crop quality was maintained.

Figure 1 Results of a meta-analysis on the effect of earthworm presence on yield, aboveground biomass, belowground biomass, total biomass, shoot/root ratio and N concentration of aboveground biomass. Effect sizes in all meta-analyses were weighted by the inverse of the pooled variance. The number of observations in each class is shown between parentheses; error bars denote the 95% confidence range. Full size image

Because previous studies suggested that the effect of earthworms differs between crop types9, we tested the effect of earthworm presence on aboveground biomass of the major grain crops and ryegrass. Aboveground biomass was significantly increased in all crops (Fig. 2a), averaging +31% across all grain crops and +24% across all pasture grasses (Fig. 2b).

Figure 2 Influence of crop species, crop type and pasture type on the effect of earthworm presence on aboveground biomass, (a–c). Influence of crop species (a), type of crop/grasses (b) and type of pasture (c) on the effect of earthworm presence. Effect sizes in all meta-analyses were weighted by the inverse of the pooled variance. The number of observations in each class is shown between parentheses; error bars denote the 95% confidence range. Full size image

How do earthworms stimulate plant production? Brown et al.12 proposed 5 possible pathways through which earthworm can positively affect plant growth: (i) biocontrol of pests and diseases; (ii) stimulation of microbial plant symbionts; (iii) production of plant-growth regulating substances; (iv) soil structure changes; and (v) increased nutrient availability. The last two mechanisms were the most consistently mentioned in early literature7. More recent studies suggested earthworm-induced regulation of plant defence mechanisms as additional pathways13,14,15.

However, our results suggest that increased N availability is a dominant pathway by which earthworms stimulate plant growth. We tested this by splitting our data according to fertilizer N application rates (Fig. 3a). When application rates exceeded 30 kg N ha−1 yr−1, the earthworm effect decreased from +19% to +9% and was not significantly different from zero anymore, suggesting that earthworms stimulate plant growth by increasing N mineralization. The effect of earthworms on plant growth in studies applying organic (N) fertilizer (+34%) was significantly stronger than in studies applying inorganic fertilizer (+10%) or no fertilizer (+20%), further implicating increased N mineralization as a major pathway (Fig. 4). Our results are consistent with studies showing the potential of earthworms to increase N mineralization from crop residues and soil organic matter, depending on earthworm community and environmental conditions16,17.

Figure 3 Influence of N fertilization rate and crop residue application rate on the effect of earthworm presence on aboveground biomass, (a–b). Influence of fertilizer N rate (a) and crop residue application rate (b) on the effect of earthworm presence. N fertilization rates include both chemical and organic (manure) fertilizer. Effect sizes in all meta-analyses were weighted by the inverse of the pooled variance. The number of observations in each class is shown between parentheses; error bars denote the 95% confidence range. Full size image

Figure 4 Influence of climate, soil- and experimental parameters on the effect of earthworm presence on aboveground biomass. The number of observations in each class is shown between parentheses; error bars denote the 95% confidence range. Full size image

If N mineralization is the main pathway, the positive effect of earthworms should be smaller for plants capable of symbiotic N 2 fixation. Indeed, for the legume crops in our dataset the earthworm effect ceased to be significant (Fig. 2b). Furthermore, when legumes were present in pastures, the effect of earthworms on pasture productivity disappeared altogether (Fig. 2c).

It is still unclear whether there is any effect of earthworms on nutrients other than N. Although it has been suggested that earthworms increase P availability in their casts18,19, this has not yet been shown to affect plant growth in experimental studies. Legumes, despite their larger need for P than grasses, did not show a positive effect of earthworm presence (Fig. 2b & 2c), which is consistent with a minor role for earthworms on P mobilization.

Both soil organic matter and plant residues can potentially serve as substrates for N mineralization facilitated by earthworms17. To distinguish between the two, we subdivided our dataset in different residue application rate classes (Fig. 3b). Although the earthworm effect on aboveground biomass peaked with +50% at the highest residue application rate, the effect stabilized around +21% at nil and very low residue application rates. This indicates that both soil organic matter and plant residue are sources for earthworm-induced mineralization. Because it has been often suggested that decaying earthworm tissues may be responsible for the observed increased plant N uptake20, we tested for the effect of earthworm survival (Fig. 5a). Earthworm presence did not significantly increase crop yield in experiments with survival rates lower than 50%; therefore the N effect is not an artefact related to decomposing earthworm tissue. This is in line with calculations on the contributions of N released from decaying earthworm tissue in previous experimental studies21, as well as with studies conducted with control treatments receiving dead earthworms22.

Figure 5 Influence of earthworm survival, earthworm density and earthworm ecological category on the effect of earthworm presence on aboveground biomass, (a–c). Influence of earthworm survival during experiment (a), earthworm density (b) earthworm ecological group (c) on the effect of earthworm presence. The number of observations in each class is shown between parentheses; error bars denote the 95% confidence range. Full size image

Although earthworm density had a highly significant effect on aboveground plant biomass, only the highest densities (>400 individuals m−2) differed significantly from lower densities (Fig. 5b). The effect under realistic earthworm densities varied between +10 and +21%. The positive effect was present for all three ecological categories of earthworms that are traditionally distinguished (Fig. 5c).

In experiments where soil was disturbed (that is, homogenized and repacked) prior to the start of the experiment, the earthworm effect on aboveground biomass was almost twice as high as in undisturbed soils (Fig. 4). This result may reflect a beneficial effect of earthworms on restoring the demolished soil structure. As soil structure will be restored after some time, a positive effect of earthworms on plant growth through their effect on soil structure is likely to be a transient effect after soil tillage operations (Fig. 4). Although some studies reported an additional effect of earthworms on plant growth through improving soil structure in undisturbed soil22,23, it generally was difficult to distinguish this effect from increased nutrient availability21. The fact that all three ecological earthworm categories (anecic, epigeic and endogeic), each with distinct burrowing and casting behaviour23,24, had a positive effect on plant growth also argues against soil structure improvement as a major pathway and in favour of enhanced nutrient mineralisation.

Significant positive earthworm effects occur across a range of climate regions, soil textures, soil organic matter contents and soil C/N ratios (Fig. 4). No significant differences were detected between categories of soil organic matter content, possibly because soil organic matter quality was not taken into account. In higher pH soils, the earthworm effect is significantly smaller than in lower pH soils. This may be a confounding effect, since the high pH soils were often linked to systems with low or nil application of residues or organic manure. Earthworm effects were strongest in soils with clay texture and not significant in sandy soils (Fig. 4). This is in marked contrast with an earlier review9 where largest beneficial earthworm effects in tropical regions were achieved on soils with sandy texture.

Which cropping systems would benefit most from earthworms? Because improving N supply in N-limited systems is the main pathway through which earthworms increase plant growth, earthworms are likely to be most beneficial in infertile soils. However, this raises a paradox, because earthworms thrive best in fertile soils with high soil organic matter levels. The paradox disappears in the case of relatively poor soils that depend on crop residue application to maintain soil fertility levels. In those soils, crop residues can serve as food for earthworms and earthworms can increase crop production through increasing N mineralization. This combination of poor soils and reliance on crop residue is particularly found in low-input farming systems in the tropics and to a lesser extent in organic farming systems in the developed world25.

Yet, these systems vary dramatically in terms of habitat quality for earthworms26. In low-input systems in the tropics, low residue quality and residue supply are most likely to be the constraining factor for reaching the full potential of earthworm activity27. Research in these systems should therefore be aimed at judicious use of the limited residue resources available28. Organic farming systems, on the other hand, typically have large application rates of organic manure or high-quality crop residues, providing excellent conditions for earthworm activity29. In those systems, earthworm activity might be crucial in closing the yield gap with conventional agriculture4. Future research in these systems should therefore focus on management strategies to increase earthworm populations. More generally speaking, management practices aimed at sustainable intensification of agriculture should take into account their effect on the earthworm population, because their presence stimulates crop production and will help to bridge the yield gap with conventional agriculture.