Foliar and fungal ¹⁵ N:¹⁴ N ratios reflect development of mycorrhizae and nitrogen supply during primary succession: testing analytical models

Abstract

Nitrogen isotopes (¹⁵N/¹⁴N ratios, expressed as δ¹⁵N values) are useful markers of the mycorrhizal role in plant nitrogen supply because discrimination against ¹⁵N during creation of transfer compounds within mycorrhizal fungi decreases the ¹⁵N/¹⁴N in plants (low δ¹⁵N) and increases the ¹⁵N/¹⁴N of the fungi (high δ¹⁵N). Analytical models of ¹⁵N distribution would be helpful in interpreting δ¹⁵N patterns in fungi and plants. To compare different analytical models, we measured nitrogen isotope patterns in soils, saprotrophic fungi, ectomycorrhizal fungi, and plants with different mycorrhizal habits on a glacier foreland exposed during the last 100 years of glacial retreat and on adjacent non-glaciated terrain. Since plants during early primary succession may have only limited access to propagules of mycorrhizal fungi, we hypothesized that mycorrhizal plants would initially be similar to nonmycorrhizal plants in δ¹⁵N and then decrease, if mycorrhizal colonization were an important factor influencing plant δ¹⁵N. As hypothesized, plants with different mycorrhizal habits initially showed similar δ¹⁵N values (−4 to −6‰ relative to the standard of atmospheric N₂ at 0‰), corresponding to low mycorrhizal colonization in all plant species and an absence of ectomycorrhizal sporocarps. In later successional stages where ectomycorrhizal sporocarps were present, most ectomycorrhizal and ericoid mycorrhizal plants declined by 5–6‰ in δ¹⁵N, suggesting transfer of ¹⁵N-depleted N from fungi to plants. The values recorded (−8 to −11‰) are among the lowest yet observed in vascular plants. In contrast, the δ¹⁵N of nonmycorrhizal plants and arbuscular mycorrhizal plants declined only slightly or not at all. On the forefront, most ectomycorrhizal and saprotrophic fungi were similar in δ¹⁵N (−1 to −3‰), but the host-specific ectomycorrhizal fungus Cortinarius tenebricus had values of up to 7‰. Plants, fungi and soil were at least 4‰ higher in δ¹⁵N from the mature site than in recently exposed sites. On both the forefront and the mature site, host-specific ectomycorrhizal fungi had higher δ¹⁵N values than ectomycorrhizal fungi with a broad host range. From these isotopic patterns, we conclude:(1) large enrichments in ¹⁵N of many ectomycorrhizal fungi relative to co-occurring ectomycorrhizal plants are best explained by treating the plant-fungal-soil system as a closed system with a discrimination against ¹⁵N of 8–10‰ during transfer from fungi to plants, (2) based on models of ¹⁵N mass balance, ericoid and ectomycorrhizal fungi retain up to two-thirds of the N in the plant-mycorrhizal system under the N-limited conditions at forefront sites, (3) sporocarps are probably enriched in ¹⁵N by an additional 3‰ relative to available nitrogen, and (4) host-specific ectomycorrhizal fungi may transfer more N to plant hosts than non-host-specific ectomycorrhizal fungi. Our study confirms that nitrogen isotopes are a powerful tool for probing nitrogen dynamics between mycorrhizal fungi and associated plants.