Nitrogen isotope fractionation explains the 15N enrichment of Antarctic cryptogams by volatilized ammonia from penguin and seal colonies
Keywords:
lichen, Moss, nitrogen pathway, nutrient transfer, ocean-land interaction
Abstract
Vegetation near bird and seal rookeries typically has high δ15N signatures and these high values are linked to the enriched δ15N values of rookery soils. However, Antarctic cryptogams are mostly dependent on atmospheric ammonia (NH3) and volatized NH3 from rookeries is severely depleted in δ15N-NH3. So there is an apparent discrepancy between the isotopically depleted source (NH3) and δ15N-enriched vegetation. In this article, we aim to resolve this discrepancy to better understand the mechanisms and processes involved in isotopic changes during nitrogen transfer between Antarctic marine and terrestrial ecosystems. Under laboratory conditions, we quantified whether volatized NH3 affects the isotopic signature of cryptogams. NH3 volatilizing from penguin guano and elephant seal dung was depleted (44–49‰) in δ15N when captured on acidified filters, compared to the source itself. Cryptogams exposed to the volatized NH3 were enriched (18.8–23.9‰) in δ15N. The moss Andreaea regularis gained more nitrogen (0.9%) than the lichen Usnea antarctica (0.4%) from volatilized NH3, indicating a potential difference in atmospheric NH3 acquisition that is consistent with existing field differences in nitrogen concentrations and δ15N between mosses and lichens in general. This study clarifies the δ15N enrichment of cryptogams resulting from one of the most important nitrogen pathways for Antarctic vegetation.
Downloads
Download data is not yet available.
References
Ayres E., van der Wal R., Sommerkorn M. & Bardgett R.D. 2006. Direct uptake of soil nitrogen by mosses. Biology Letters 2, 286–288, doi: 10.1098/rsbl.2006.0455.
Bates D., Mächler M., Bolker B.M. & Walker S.C. 2015. Fitting linear mixed-effects models using lme4. Journal of statistical Software 67, 1–48, doi: 10.18637/jss.v067.i01.
Blackall T.D., Wilson L.J., Theobald M.R., Milford C., Nemitz E., Bull J., Bacon P.J., Hamer K.C., Wanless S. & Sutton M.A. 2007. Ammonia emissions from seabird colonies. Geophysical Research Letters 34, L10801, doi: 10.1029/2006GL028928.
Bokhorst S. & Convey P. 2016. Impact of marine vertebrates on Antarctic terrestrial micro-arthropods. Antarctic Science 28, 175–186, doi: 10.1017/s0954102015000607.
Bokhorst S., Convey P. & Aerts R. 2019. Nitrogen inputs by marine vertebrates drive abundance and richness in Antarctic terrestrial ecosystems. Current Biology 29, 1721–1727, doi: 10.1016/j.cub.2019.04.038.
Bokhorst S., Huiskes A., Convey P. & Aerts R. 2007. External nutrient inputs into terrestrial ecosystems of the Falkland Islands and the maritime Antarctic region. Polar Biology 30, 1315–1321, doi: 10.1007/s00300-007-0292-0.
Cocks M.P., Balfour D.A. & Stock W.D. 1998. On the uptake of ornithogenic products by plants on the inland mountains of Dronning Maud Land, Antarctica, using stable isotopes. Polar Biology 20, 107–111, doi: 10.1007/s003000050283.
Cornelissen J.H.C., Quested H.M., Logtestijn R.S.P., Perez-Harguindeguy N., Gwynn-Jones D., Diaz S., Callaghan T.V., Press M.C. & Aerts R. 2006. Foliar pH as a new plant trait: can it explain variation in foliar chemistry and carbon cycling processes among Subarctic plant species and types? Oecologia 147, 315–326, doi: 10.1007/s00442-005-0269-z.
Crittenden P.D., Scrimgeour C.M., Minnullina G., Sutton M.A., Tang Y.S. & Theobald M.R. 2015. Lichen response to ammonia deposition defines the footprint of a penguin rookery. Biogeochemistry 122, 295–311, doi: 10.1007/s10533-014-0042-7.
Dahlman L., Persson J., Palmqvist K. & Näsholm T. 2004. Organic and inorganic nitrogen uptake in lichens. Planta 219, 459–467, doi: 10.1007/s00425-004-1247-0.
Deniro M.J. & Epstein S. 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351, doi: 10.1016/0016-7037(81)90244-1.
Ellis J.C. 2005. Marine birds on land: a review of plant biomass, species richness, and community composition in seabird colonies. Plant Ecology 181, 227–241, doi: 10.1007/s11258-005-7147-y.
Ellis J.C., Farina J.M. & Witman J.D. 2006. Nutrient transfer from sea to land: the case of gulls and cormorants in the Gulf of Maine. Journal of Animal Ecology 75, 565–574, doi: 10.1111/j.1365-2656.2006.01077.x.
Erskine P.D., Bergstrom D.M., Schmidt S., Stewart G.R., Tweedie C.E. & Shaw J.D. 1998. Subantarctic Macquarie Island—A model ecosystem for studying animal-derived nitrogen sources using 15N natural abundance. Oecologia 117, 187–193, doi: 10.1007/s004420050647.
Greenfield L.G. 1992a. Precipitation nitrogen at maritime Signy Island and continental Cape Bird, Antarctica. Polar Biology 11, 649–653, doi: 10.1007/BF00237961.
Greenfield L.G. 1992b. Retention of precipitation nitrogen by Antarctic mosses, lichens and fellfield soils. Antarctic Science 4, 205–206, doi: 10.1017/S0954102092000312.
Hayasaka H., Fukuzaki N., Kondo S., Ishizuka T. & Totsuka T. 2004. Nitrogen isotopic ratios of gaseous ammonia and ammonium aerosols in the atmosphere. Journal of Japan Society for Atmospheric Environment 39, 272–279, doi: 10.11298/taiki1995.39.6_272.
Heaton T.H.E., Spiro B., Madeline C. & Robertson S. 1997. Potential canopy influences on the isotopic composition of nitrogen and sulphur in atmospheric deposition. Oecologia 109, 600–607, doi: 10.1007/s004420050122.
Herman P.M.J., Middelburg J.J., Widdows J., Lucas C.H. & Heip C.H.R. 2000. Stable isotopes’ as trophic tracers: combining field sampling and manipulative labelling of food resources for macrobenthos. Marine Ecology Progress Series 204, 79–92, doi: 10.3354/meps204079.
Hogberg P. 1997. Tansley review no 95. 15N natural abundance in soil–plant systems. New Phytologist 137, 179–203, doi: 10.1046/j.1469-8137.1997.00808.x.
Huiskes A.H.L., Boschker H.T.S., Lud D. & Moerdijk-Poortvliet T.C.W. 2006. Stable isotope ratios as a tool for assessing changes in carbon and nutrient sources in Antarctic terrestrial ecosystems. Plant Ecology 182, 79–86, doi: 10.1007/s11258-005-9032-0.
Kirshenbaum I., Smith J.S., Crowell T., Graff J. & McKee R. 1947. Separation of the nitrogen isotopes by the exchange reaction between ammonia and solutions of ammonium nitrate. The Journal of Chemical Physics 15, 440–446, doi: 10.1063/1.1746562.
Kuznetsova A., Brockhoff P.B. & Christensen R.H.B. 2017. lmerTest package: tests in linear mixed effects models. Journal of statistical Software 82, 1–26, doi: 10.18637/jss.v082.i13.
Lindeboom H.J. 1984. The nitrogen pathway in a penguin rookery. Ecology 65, 269–277, doi: 10.2307/1939479.
McFarlane D.A., Keeler R.C. & Mizutani H. 1995. Ammonia volatilization in a Mexican bat cave ecosystem. Biogeochemistry 30, 1–8, doi: 10.1007/bf02181037.
Melse W.R. & Ogink W.M.N. 2005. Air scrubbing techniques for ammonia and odor reduction at livestock operations: review of on-farm research in the Netherlands. Transactions of the ASAE 48, 2303–2313, doi: 10.13031/2013.20094.
Mizutani H., Hasegawa H. & Wada E. 1986. High nitrogen isotope ratio for soils of seabird rookeries. Biogeochemistry 2, 221–247, doi: 10.1007/BF021801.
Mizutani H., Kabaya Y. & Wada E. 1985. Ammonia volatilization and high 15N/14N ratio in a penguin rookery in Antarctica. Geochemical Journal 19, 323–327, doi: 10.1007/BF02180160.
Mizutani H. & Wada E. 1988. Nitrogen and carbon isotope ratios in seabird rookeries and their ecological implications. Ecology 69, 340-349, doi: 10.2307/1940432.
Mizutani H. & Wada E. 1985. High-performance liquid chromatographic determination of uric acid in soil. Journal of Chromatography A 331, 359-369, doi: 10.1016/0021-9673(85)80042-X.
Moore H. 1977. The isotopic composition of ammonia, nitrogen dioxide and nitrate in the atmosphere. Atmospheric Environment 11, 1239–1243, doi: 10.1016/0004-6981(77)90102-0.
Nie Y.G., Liu X.D., Wen T., Sun L.G. & Emslie S.D. 2014. Environmental implication of nitrogen isotopic composition in ornithogenic sediments from the Ross Sea region, East Antarctica: Δ15N as a new proxy for avian influence. Chemical Geology 363, 91–100, doi: 10.1016/j.chemgeo.2013.10.031.
Perez C.A., Aravena J.C., Ivanovich C. & McCulloch R. 2017. Effects of penguin guano and moisture on nitrogen biological fixation in maritime Antarctic soils. Polar Biology 40, 437–448, doi: 10.1007/s00300-016-1971-5.
Post D.M., Taylor J.P., Kitchell J.F., Olson M.H., Schindler D.E. & Herwig B.R. 1998. The role of migratory waterfowl as nutrient vectors in a managed wetland. Conservation Biology 12, 910–920, doi: 10.1111/j.1523-1739.1998.97112.x.
R Core Team 2015. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
Robinson D. 2001. δ15N as an integrator of the nitrogen cycle. Trends in Ecology & Evolution 16, 153–162, doi: 10.1016/S0169-5347(00)02098-X.
Song L., Lu H.-Z., Xu X.-L., Li S., Shi X.-M., Chen X., Wu Y., Huang J.-B., Chen Q., Liu S., Wu C.-S. & Liu W.-Y. 2016. Organic nitrogen uptake is a significant contributor to nitrogen economy of subtropical epiphytic bryophytes. Scientific Reports 6, article no. 30408, doi: 10.1038/srep30408.
Zhu R.B., Liu Y.S., Ma E.D., Sun J.J., Xu H. & Sun L.G. 2009. Nutrient compositions and potential greenhouse gas production in penguin guano, ornithogenic soils and seal colony soils in coastal Antarctica. Antarctic Science 21, 427–438, doi: 10.1017/s0954102009990204.
Published
2019-11-19
How to Cite
Bokhorst S., van Logtestijn R., Convey P., & Aerts R. (2019). Nitrogen isotope fractionation explains the <sup>15</sup>N enrichment of Antarctic cryptogams by volatilized ammonia from penguin and seal colonies. Polar Research, 38. https://doi.org/10.33265/polar.v38.3355
Issue
Section
Research Articles
Authors contributing to Polar Research retain copyright of their work, with first publication rights granted to the Norwegian Polar Institute. Read the journal's full Copyright- and Licensing Policy.
