Skip to main content
Log in

Early Goose Arrival Increases Soil Nitrogen Availability More Than an Advancing Spring in Coastal Western Alaska

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

An understudied aspect of climate change-induced phenological mismatch is its effect on ecosystem functioning, such as nitrogen (N) cycling. Migratory herbivore arrival time may alter N inputs and plant–herbivore feedbacks, whereas earlier springs are predicted to increase N cycling rates through warmer temperatures. However, the relative importance of these shifts in timing and how they interact to affect N cycling are largely unknown. We conducted a 3-year factorial experiment in coastal western Alaska that simulated different timings of Pacific black brant (Branta bernicla nigricans) arrival (3 weeks early, typical, 3 weeks late, or no-grazing) and the growing season (ca. 3 weeks advanced and ambient) on adsorbed and mobile inorganic (NH4+–N, NO3–N) and mobile organic N (amino acid) pools. Early grazing increased NH4+–N, NO3–N, and amino acids by 103%, 119%, and 7%, respectively, whereas late grazing reduced adsorbed NH4+–N and NO3–N by 16% and 17%, respectively. In comparison, the advanced growing season increased mobile NH4+–N by 26%. The arrival time by geese and the start of the season did not interact to influence soil N availability. While the onset of spring in our system is advancing at twice the rate of migratory goose arrival, earlier goose migration is likely to be more significant than the advances in springs in influencing soil N, although both early goose arrival and advanced springs are likely to increase N availability in the future. This increase in soil N resources can have a lasting impact on plant community composition and productivity in this N-limited ecosystem.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

Data Availability

The dataset from this manuscript has been uploaded to https://doi.org/10.18739/a22274.

References

  • Bai E, Li S, Xu W, Li W, Dai W, Jiang P. 2013. A meta-analysis of experimental warming effects on terrestrial nitrogen pools and dynamics. New Phytol 199:441–51.

    Google Scholar 

  • Bardgett RD, Manning P, Morriën E, De Vries FT. 2013. Hierarchical responses of plant-soil interactions to climate change: consequences for the global carbon cycle. J Ecol 101:334–43.

    Google Scholar 

  • Bazely DR, Jefferies RL. 1985. Goose faeces: a source of nitrogen for plant growth in a grazed salt marsh. J Appl Ecol 22:693–703.

    Google Scholar 

  • Bazely DR, Jefferies RL. 1989. Lesser snow geese and the nitrogen economy of a grazed salt marsh. J Ecol 77:24–34.

    CAS  Google Scholar 

  • Beard KH, Choi RT. 2017. Data from: Asynchrony in the timing of goose-vegetation interactions: implications for biogeochemical cycling in wet sedge tundra Tutakoke River, Yukon Delta NWR, Alaska, 2014-2016.

  • Beard KH, Choi RT, Leffler AJ, Carlson LG, Kelsey KC, Schmutz JA, Welker JM. 2019a. Migratory goose arrival time plays a larger role in influencing forage quality than advancing springs in an Arctic coastal wetland. PLoS One 14:e0213037.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beard KH, Kelsey KC, Leffler AJ, Welker JM. 2019b. The missing angle: ecosystem consequences of phenological mismatch. Trends Ecol Evol 34:885–8.

    PubMed  Google Scholar 

  • Belay-Tedla A, Zhou X, Su B, Wan S, Luo Y. 2009. Labile, recalcitrant, and microbial carbon and nitrogen pools of a tallgrass prairie soil in the US Great Plains subjected to experimental warming and clipping. Soil Biol Biochem 41:110–16.

    CAS  Google Scholar 

  • Blankinship JC, Hart SC. 2012. Consequences of manipulated snow cover on soil gaseous emission and N retention in the growing season: a meta-analysis. Ecosphere 3:1–20.

    Google Scholar 

  • Boelman NT, Krause JS, Sweet SK, Chmura HE, Perez JH, Gough L, Wingfield JC. 2017. Extreme spring conditions in the Arctic delay spring phenology of long-distance migratory songbirds. Oecologia 185:1–12.

    Google Scholar 

  • Borner AP, Kielland K, Walker MD. 2008. Effects of simulated climate change on plant phenology and nitrogen mineralization in Alaskan Arctic tundra. Arct Antarct Alp Res 40:27–38.

    Google Scholar 

  • Boyer KE, Zedler JB. 1999. Nitrogen addition could shift plant community composition in a restored California salt marsh. Restor Ecol 7:74–85.

    Google Scholar 

  • Brook RW, Leafloor JO, Abraham KF, Douglas DC. 2015. Density dependence and phenological mismatch: consequences for growth and survival of sub-arctic nesting Canada Geese. Avian Conserv Ecol 10:1.

    Google Scholar 

  • Buckeridge KM, Cen Y-P, Layzell DB, Grogan P. 2010. Soil biogeochemistry during the early spring in low arctic mesic tundra and the impacts of deepened snow and enhanced nitrogen availability. Biogeochemistry 99:127–41.

    CAS  Google Scholar 

  • Buckeridge KM, Grogan P. 2010. Deepened snow increases late thaw biogeochemical pulses in mesic low arctic tundra. Biogeochemistry 101:105–21.

    Google Scholar 

  • Burnham KP, Anderson DR, Huyvaert KP. 2011. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35.

    Google Scholar 

  • Carlson LG, Beard KH, Adler PB. 2018. Direct effects of warming increase woody plant abundance in a subarctic wetland. Ecol Evol 8:2868–79.

    PubMed  PubMed Central  Google Scholar 

  • Choi RT, Beard KH, Leffler AJ, Kelsey KC, Schmutz JA, Welker JM. 2019. Phenological mismatch between season advancement and migration timing alters Arctic plant traits. J Ecol 107:2503–18.

    Google Scholar 

  • Clausen KK, Clausen P. 2013. Earlier Arctic springs cause phenological mismatch in long-distance migrants. Oecologia 173:1101–12.

    PubMed  Google Scholar 

  • Cohen JM, Lajeunesse MJ, Rohr JR. 2018. A global synthesis of animal phenological responses to climate change. Nat Clim Change 8:224–8.

    Google Scholar 

  • Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, MacK MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Peñuelas J, Reich PB, Schuur EAG, Stock WD, Templer PH, Virginia RA, Welker JM, Wright IJ. 2009. Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183:980–92.

    CAS  PubMed  Google Scholar 

  • Darrouzet-Nardi A, Steltzer H, Sullivan PF, Segal A, Koltz AM, Livensperger C, Schimel JP, Weintraub MN. 2019. Limited effects of early snowmelt on plants, decomposers, and soil nutrients in Arctic tundra soils. Ecol Evol 9:1820–44.

    PubMed  PubMed Central  Google Scholar 

  • Darrouzet-Nardi A, Weintraub MN. 2014. Evidence for spatially inaccessible labile N from a comparison of soil core extractions and soil pore water lysimetry. Soil Biol Biochem 73:22–32.

    CAS  Google Scholar 

  • DeMarco J, Mack MC, Bret-Harte MS. 2011. The effects of snow, soil microenvironment, and soil organic matter quality on N availability in three Alaskan Arctic plant communities. Ecosystems 14:804–17.

    CAS  Google Scholar 

  • Doane TA, Horwáth WR. 2003. Spectrophotometric determination of nitrate with a single reagent. Anal Lett 36:2713–22.

    CAS  Google Scholar 

  • Doiron M, Gauthier G, Levesque E. 2015. Trophic mismatch and its effects on the growth of young in an Arctic herbivore. Glob Change Biol 21:4364–76.

    Google Scholar 

  • Edwards KA, McCulloch J, Kershaw GP, Jefferies RL. 2006. Soil microbial and nutrient dynamics in a wet Arctic sedge meadow in late winter and early spring. Soil Biol Biochem 38:2843–51.

    CAS  Google Scholar 

  • Fischer JB, Stehn RA, Walters G. 2008. Nest population size and potential production of geese and spectacled eiders on the Yukon-Kuskokwim Delta, Alaska, 2008. Anchorage (AK): U.S. Fish and Wildlife Service, Migratory Bird Management.

    Google Scholar 

  • Fischer JB, Williams AR, Stehn RA. 2017. Nest population size and potential production of geese and spectacled eiders on the Yukon-Kuskokwim Delta, Alaska, 1985-2016. Anchorage (AK): U.S. Fish and Wildlife Service, Migratory Bird Management.

    Google Scholar 

  • Giblin AE, Tobias CR, Song B, Weston N, Banta GT, Rivera-Monroy VH. 2013. The importance of dissimilatory nitrate reduction to ammonium (DNRA) in the nitrogen cycle of coastal ecosystems. Oceanography 26:124–31.

    Google Scholar 

  • Grogan P, Michelsen A, Ambus P, Jonasson S. 2004. Freeze–thaw regime effects on carbon and nitrogen dynamics in sub-arctic heath tundra mesocosms. Soil Biol Biochem 36:641–54.

    CAS  Google Scholar 

  • Grogan P, Zamin TJ. 2018. Growth responses of the common arctic graminoid Eriophorum vaginatum to simulated grazing are independent of soil nitrogen availability. Oecologia 186:151–62.

    PubMed  Google Scholar 

  • Heberling JM, McDonough MacKenzie C, Fridley JD, Kalisz S, Primack RB. 2019. Phenological mismatch with trees reduces wildflower carbon budgets. Ecol Lett 22:616–23.

    PubMed  Google Scholar 

  • Henry HAL, Jefferies RL. 2002. Free amino acid, ammonium and nitrate concentrations in soil solutions of a grazed coastal marsh in relation to plant growth. Plant Cell Environ 25:665–75.

    CAS  Google Scholar 

  • Henry HAL, Jefferies RL. 2003. Plant amino acid uptake, soluble N turnover and microbial N capture in soils of a grazed Arctic salt marsh. J Ecol 91:627–36.

    CAS  Google Scholar 

  • Hobbie JE, Hobbie EA. 2012. Amino acid cycling in plankton and soil microbes studied with radioisotopes: measured amino acids in soil do not reflect bioavailability. Biogeochemistry 107:339–60.

    CAS  Google Scholar 

  • Jonasson S, Michelsen A, Schmidt IK. 1999. Coupling of nutrient cycling and carbon dynamics in the Arctic, integration of soil microbial and plant processes. Appl Soil Ecol 11:135–46.

    Google Scholar 

  • Jones DL, Owen AG, Farrar JF. 2002. Simple method to enable the high resolution determination of total free amino acids in soil solutions and soil extracts. Soil Biol Biochem 34:1893–902.

    CAS  Google Scholar 

  • Jorgenson MT. 2000. Hierarchical organization of ecosystems at multiple spatial scales on the Yukon-Kuskokwim Delta, Alaska, U.S.A. Arct Antarct Alp Res 32:221–39.

    Google Scholar 

  • Jorgenson T, Ely C. 2001. Topography and flooding of coastal ecosystems on the Yukon-Kuskokwim Delta, Alaska: implications for sea-level rise. J Coast Res 17:124–36.

    Google Scholar 

  • Kelsey KC, Leffler AJ, Beard KH, Choi RT, Schmutz JA, Welker JM. 2018. Phenological mismatch in coastal western Alaska may increase summer season greenhouse gas uptake. Environ Res Lett 13:044032.

    Google Scholar 

  • Kölzsch A, Bauer S, de Boer R, Griffin L, Cabot D, Exo KM, van der Jeugd HP, Nolet BA. 2015. Forecasting spring from afar? Timing of migration and predictability of phenology along different migration routes of an avian herbivore. J Anim Ecol 84:272–83.

    PubMed  Google Scholar 

  • Lameris TK, Scholten I, Bauer S, Cobben MMP, Ens BJ, Nolet BA. 2017. Potential for an Arctic-breeding migratory bird to adjust spring migration phenology to Arctic amplification. Glob Change Biol 23:4058–67.

    Google Scholar 

  • Leffler AJ, Beard KH, Kelsey KC, Choi RT, Schmutz JA, Welker JM. 2019. Delayed herbivory by migratory geese increases summer-long CO2 uptake in coastal western Alaska. Glob Change Biol 25:277–89.

    Google Scholar 

  • Lin D, Xia J, Wan S. 2010. Climate warming and biomass accumulation of terrestrial plants: a meta-analysis. New Phytol 188:187–98.

    PubMed  Google Scholar 

  • Martinsen V, Mulder J, Austrheim G, Hessen DO, Mysterud A. 2012. Effects of sheep grazing on availability and leaching of soil nitrogen in low-alpine grasslands. Arct Antarct Alp Res 44:67–82.

    Google Scholar 

  • Mayor SJ, Guralnick RP, Tingley MW, Otegui J, Withey JC, Elmendorf SC, Andrew ME, Leyk S, Pearse IS, Schneider DC. 2017. Increasing phenological asynchrony between spring green-up and arrival of migratory birds. Sci Rep 7:1902.

    PubMed  PubMed Central  Google Scholar 

  • McBride MB. 1989. Surface chemistry of soil minerals. Miner Soil Environ 2:35–87.

    Google Scholar 

  • McLaren JR, Darrouzet-Nardi A, Weintraub MN, Gough L. 2017. Seasonal patterns of soil nitrogen availability in moist acidic tundra. Arct Sci 4:AS-2017-0014.

    Google Scholar 

  • Miller-Rushing AJ, Høye TT, Inouye DW, Post E. 2010. The effects of phenological mismatches on demography. Philos Trans R Soc Lond B Biol Sci 365:3177–86.

    PubMed  PubMed Central  Google Scholar 

  • Miller AJ, Cramer MD. 2005. Root nitrogen acquisition and assimilation. Plant Soil 274:1–36.

    CAS  Google Scholar 

  • Myers-Smith IH, Forbes BC, Wilmking M, Hallinger M, Lantz T, Blok D, Tape KD, Macias-Fauria M, Sass-Klaassen U, Lévesque E, Boudreau S, Ropars P, Hermanutz L, Trant A, Collier LS, Weijers S, Rozema J, Rayback SA, Schmidt NM, Schaepman-Strub G, Wipf S, Rixen C, Ménard CB, Venn S, Goetz S, Andreu-Hayles L, Elmendorf S, Ravolainen V, Welker J, Grogan P, Epstein HE, Hik DS. 2011. Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities. Environ Res Lett 6:045509.

    Google Scholar 

  • Natali SM, Schuur EAG, Rubin RL. 2012. Increased plant productivity in Alaskan tundra as a result of experimental warming of soil and permafrost. J Ecol 100:488–98.

    Google Scholar 

  • Person BT, Herzog MP, Ruess RW, Sedinger JS, Anthony RM, Babcock CA. 2003. Feedback dynamics of grazing lawns: coupling vegetation change with animal growth. Oecologia 135:583–92.

    PubMed  Google Scholar 

  • Person BT, Ruess RW. 2003. Stability of a subarctic saltmarsh: plant community resistance to tidal inundation. Ecoscience 10:351–60.

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. 2017. nmle: linear and nonlinear mixed effects models. R Packag version 31-131. https://CRANR-project.org/package=nlme. Accessed 27 July 2017.

  • Prop J, Vulink T. 1992. Digestion by barnacle geese in the annual cycle: the interplay between retention time and food quality. Funct Ecol 6(2):180–9.

    Google Scholar 

  • Qian P, Schoenau JJ. 1995. Assessing nitrogen mineralization from soil organic matter using anion exchange membranes. Fertil Res 40:143–8.

    Google Scholar 

  • Renner SS, Zohner CM. 2018. Climate change and phenological mismatch in trophic interactions among plants, insects, and vertebrates. Annu Rev Ecol Evol Syst 49:165–82.

    Google Scholar 

  • Rhine ED, Mulvaney RL, Pratt EJ, Sims GK. 1998. Improving the Berthelot reaction for determining ammonium in soil extracts and water. Soil Sci Soc Am J 62:473–80.

    CAS  Google Scholar 

  • Robertson GP, Wedin D, Groffman PM, Blair JM, Holland EA, Nadelhoffer KJ, Harris D. 1999. Soil carbon and nitrogen availability: nitrogen mineralization, nitrification, and soil respiration potentials. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P, Eds. Standard soil methods for long-term ecological research. New York (NY): Oxford University Press. p 258–71.

    Google Scholar 

  • Rogers MC, Sullivan PF, Welker JM. 2011. Evidence of nonlinearity in the response of net ecosystem CO2 exchange to increasing levels of winter snow depth in the High Arctic of northwest Greenland. Arct Antarct Alp Res 43:95–106.

    Google Scholar 

  • Ross MV, Alisauskas RT, Douglas DC, Kellett DK. 2017. Decadal declines in avian herbivore reproduction: density-dependent nutrition and phenological mismatch in the Arctic. Ecology 98:1869–83.

    PubMed  Google Scholar 

  • Ruess RW, McFarland JW, Person B, Sedinger JS. 2019. Geese mediate vegetation state changes with parallel effects on N cycling that leave nutritional legacies for offspring. Ecosphere 10:e02850.

    Google Scholar 

  • Ruess RW, Uliassi DD, Mulder CPH, Person BT. 1997. Growth responses of Carex ramenskii to defoliation, salinity, and nitrogen availability: implications for geese-ecosystem dynamics in western Alaska. Ecoscience 4:170–8.

    Google Scholar 

  • Schaeffer SM, Sharp E, Schimel JP, Welker JM. 2013. Soil-plant N processes in a High Arctic ecosystem, NW Greenland are altered by long-term experimental warming and higher rainfall. Glob Change Biol 19:3529–39.

    Google Scholar 

  • Schimel JP, Kielland K, Chapin FS. 1996. Nutrient availability and uptake by tundra plants. In: Reynolds JF, Tenhunen JD, Eds. Landscape function and disturbance in Arctic Tundra. Ecological Studies (Analysis and Synthesis), vol 120. Berlin: Springer. pp 203–21.

  • Sedinger JS, Herzog MP, Person BT, Kirk MT, Obritchkewitch T, Martin PP, Stickney AA. 2001. Large-scale variation in growth of Black Brant goslings related to food availability. Auk 118:1088–95.

    Google Scholar 

  • Sedinger JS, Raveling DG. 1984. Dietary selectivity in relation to availability and quality of food for goslings of Cackling Geese. Auk 101:295–306.

    Google Scholar 

  • Sedinger JS, Raveling DG. 1986. Timing of nesting by Canada geese in relation to the phenology and availability of their food plants. J Anim Ecol 55:1083–102.

    Google Scholar 

  • Sistla SA, Asao S, Schimel JP. 2012. Detecting microbial N-limitation in tussock tundra soil: Implications for Arctic soil organic carbon cycling. Soil Biol Biochem 55:78–84.

    CAS  Google Scholar 

  • Sistla SA, Schimel JP. 2013. Seasonal patterns of microbial extracellular enzyme activities in an arctic tundra soil: Identifying direct and indirect effects of long-term summer warming. Soil Biol Biochem 66:119–29.

    CAS  Google Scholar 

  • Sjögersten S, Kuijper DPJ, van der Wal R, Loonen MJJE, Huiskes AHL, Woodin SJ. 2010. Nitrogen transfer between herbivores and their forage species. Polar Biol 33:1195–203.

    Google Scholar 

  • Skopp J, Jawson MD, Doran JW. 1990. Steady-state aerobic microbial activity as a function of soil water content. Soil Sci Soc Am J 54:1619.

    Google Scholar 

  • Tiedje JM. 1988. Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB, Ed. Environmental microbiology of anaerobes. New York (NY): Wiley. p 179–244.

    Google Scholar 

  • Uher-Koch BD, Schmutz JA, Wilson HM, Anthony RM, Day TL, Fondell TF, Person BT, Sedinger JS. 2019. Ecosystem-scale loss of grazing habitat impacted by abundance of dominant herbivores. Ecosphere 10:e02767.

    Google Scholar 

  • Weintraub MN, Schimel JP. 2005. The seasonal dynamics of amino acids and other nutrients in Alaskan Arctic tundra soils. Biogeochemistry 73:359–80.

    CAS  Google Scholar 

  • Welker JM, Jonsdottir IS, Fahnestock JT. 2003. Leaf isotopic (d13C and d15N) and nitrogen contents of Carex plants along the Eurasian Coastal Arctic: Results from the Northeast Passage expedition. Polar Biol 27:29–37.

    Google Scholar 

  • White JR, Reddy KR. 2003. Nitrification and denitrification rates of Everglades wetland soils along a phosphorus-impacted gradient. J Environ Qual 32:2436.

    CAS  PubMed  Google Scholar 

  • Wilson DJ, Jefferies RL. 1996. Nitrogen mineralization, plant growth and goose herbivory in an Arctic coastal ecosystem. J Ecol 84:841–51.

    Google Scholar 

  • Zacheis A, Ruess R, Hupp J. 2002. Nitrogen dynamics in an Alaskan salt marsh following spring use by geese. Oecologia 130:600–8.

    PubMed  Google Scholar 

Download references

Acknowledgements

Work was funded by National Science Foundation awards ARC-1304523 and ARC-1304879, and by the Utah Agricultural Experiment Station, Utah State University, and approved as journal paper #9222. R. Choi received support from National Science Foundation award DGE-1633756 and J. Leffler from the South Dakota Agricultural Experiment Station. We thank D. Douglas (USGS) for data on season advancement; N. Dickenson for laboratory resources; S. Durham for statistical advice; K. Foley for field soil measurements; H. Braithwaite, L. Carlson, T. DeMasters, J. Ferguson, R. Hicks, M. Holdrege, K. Lynöe, and S. Walden for field assistance; A. Albee, K. Curtis, and S. Sprouse for laboratory assistance; M. Irinaga, L. Gullingsrud, and L. McFadden at CH2M Hill Polar Services for logistical assistance; Yukon Delta National Wildlife Refuge staff; and the people of Chevak, AK. Permits obtained for this work include—ADF&G permit: 16–23; USFWS NWR special use permit: FF07RYKD0-14-06; USFWS Migratory Bird permit: MB28352B-0; USU IACUC: 2004. Data are published online at the NSF Arctic Data Center (https://doi.org/10.18739/a22274). Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Karen H. Beard.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 4869 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Choi, R.T., Beard, K.H., Kelsey, K.C. et al. Early Goose Arrival Increases Soil Nitrogen Availability More Than an Advancing Spring in Coastal Western Alaska. Ecosystems 23, 1309–1324 (2020). https://doi.org/10.1007/s10021-019-00472-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-019-00472-9

Keywords

Navigation