Intra-trophic isotopic discrimination of 15N/14N for amino acids in autotrophs: Implications for nitrogen dynamics in ecological studies

Authors: TAKIZAWA, YUKO - Hokkaido University; DHARAMPAL, PRARTHANA - University Of Wisconsin; Steffan, Shawn; TAKANO, YOSHINORI - Japan Agency For Marine-Earth Science And Technology (JAMSTEC); OHKOUCHI, NAOHIKO - Japan Agency For Marine-Earth Science And Technology (JAMSTEC); CHIKARAISHI, YOSHITO - Japan Agency For Marine-Earth Science And Technology (JAMSTEC)

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/6/2017
Publication Date: 3/22/2017
Publication URL: https://handle.nal.usda.gov/10113/5695459
Citation: Takizawa, Y., Dharampal, P.S., Steffan, S.A., Takano, Y., Ohkouchi, N., Chikaraishi, Y. 2017. Intra-trophic isotopic discrimination of 15N/14N for amino acids in autotrophs: Implications for nitrogen dynamics in ecological studies. Ecology and Evolution. 7(9):2916-2924. doi: 10.1002/ece3.2866.

Interpretive Summary: Plants serve as the resource base for virtually all terrestrial heterotrophs. As the first “rung” on the trophic “ladder,” it is always assumed that plant trophic position is 1.0. This assumption is particularly important when isotopic analyses are used to assess the position of an organism within the food-chain. However, if the isotopic composition of plant tissues indicate that certain tissues diverge significantly from the assumed position of 1.0, then this has tremendous implications for all the animals consuming these plant tissues. Here, we report that certain deciduous perennial plants produce floral tissues in early spring that are enriched in 15N. This likely derives from the mobilization and sequestration of proteins produced during the previous year. This floral enrichment phenomenon is quite brief in the spring, but demonstrates that the plant is effectively “eating” and “re-assimilating” its own resource pool. Impact: For arthropods and animals consuming floral tissues in early spring (e.g., bees that consume pollen), the enrichment phenomenon in spring flowers will potentially have tremendous impacts on the observed trophic positions of such consumers. This will need to be factored into trophic position assessment among bee species.

Technical Abstract: Metabolic reactions within heterotrophs cause discrimination in their stable nitrogen isotopic composition of amino acids (d15NAA) compared to their diets. Ecologists have exploited this measurable inter-trophic discrimination in the d15NAA value to estimate the trophic positions of heterotrophic animals. Analogous biochemical mechanisms also operate among autotrophs, particularly pronounced in organs without chloroplasts (e.g., flower and root) during periods of low photosynthetic production. This versatile profile potentially generates isotopic discrimination within a single trophic moiety (the parent plant) at the ‘intra-trophic’ level, with increasing the d15NAA values and leading to an overestimation of the trophic position for the plant organs. In the present study, we examined the d15NAA values in spring leaves and flowers from eight deciduous and two annual plants. These plants were classified on the basis of their time of bloom; plants that bloomed when their leaves were absent (Type I) versus plants that bloomed while leaves were already present on the parent plants (Type II). Leaf d15NAA values indicated that both Type I and Type II plants occupied comparable and ecologically relevant mean trophic positions (1.0 ± 0.1). Conversely, the trophic positions of Type I flowers registered a mean of 2.2 ± 0.3, while Type II flowers mirrored the trophic positions of their leaves (1.0 ± 0.1). These results suggest that Type I flowers, being energetically supported by the catabolism of overwintered (stored) amino acids, experience ‘intra-trophic’ isotopic discrimination. Downstream, this results in an elevation of the estimated trophic position of the plant biomass bearing them. In contrast, the active photosynthesis of Type II leaves in the parent plant sustains the bloom of Type II flowers. This precludes catabolically-induced intra-trophic discrimination from affecting the trophic position of Type II flowers. Our findings are the first to report such transient and unique isotopic tendencies in autotrophs, and will be useful to better understand the trophic peculiarities of plants and their consumers alike.