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Title: Global Patterns and Controls of Nutrient Immobilization on Decomposing Cellulose in Riverine Ecosystems

Abstract

Abstract Microbes play a critical role in plant litter decomposition and influence the fate of carbon in rivers and riparian zones. When decomposing low‐nutrient plant litter, microbes acquire nitrogen (N) and phosphorus (P) from the environment (i.e., nutrient immobilization), and this process is potentially sensitive to nutrient loading and changing climate. Nonetheless, environmental controls on immobilization are poorly understood because rates are also influenced by plant litter chemistry, which is coupled to the same environmental factors. Here we used a standardized, low‐nutrient organic matter substrate (cotton strips) to quantify nutrient immobilization at 100 paired stream and riparian sites representing 11 biomes worldwide. Immobilization rates varied by three orders of magnitude, were greater in rivers than riparian zones, and were strongly correlated to decomposition rates. In rivers, P immobilization rates were controlled by surface water phosphate concentrations, but N immobilization rates were not related to inorganic N. The N:P of immobilized nutrients was tightly constrained to a molar ratio of 10:1 despite wide variation in surface water N:P. Immobilization rates were temperature‐dependent in riparian zones but not related to temperature in rivers. However, in rivers nutrient supply ultimately controlled whether microbes could achieve the maximum expected decomposition rate at a givenmore » temperature. Collectively, we demonstrated that exogenous nutrient supply and immobilization are critical control points for decomposition of organic matter.« less

Authors:
ORCiD logo [1];  [2];  [3]; ORCiD logo [4];  [5];  [6]; ORCiD logo [7]; ORCiD logo [8]; ORCiD logo [9];  [10];  [11]; ORCiD logo [12];  [13];  [1];  [14];  [15];  [16];  [17];  [18];  [19] more »; ORCiD logo [20]; ORCiD logo [21]; ORCiD logo [22];  [23];  [24];  [25];  [26]; ORCiD logo [27];  [28];  [29];  [30]; ORCiD logo [31];  [32]; ORCiD logo [33]; ORCiD logo [34];  [35];  [36];  [37];  [38]; ORCiD logo [39];  [40];  [31];  [41];  [42];  [43]; ORCiD logo [44]; ORCiD logo [45]; ORCiD logo [46]; ORCiD logo [47]; ORCiD logo [48]; ORCiD logo [49];  [50]; ORCiD logo [51];  [52];  [53];  [54];  [55];  [56]; ORCiD logo [57]; ORCiD logo [58];  [59];  [60];  [61]; ORCiD logo [62];  [56];  [63]; ORCiD logo [64];  [63]; ORCiD logo [37];  [65];  [66];  [67];  [29];  [68]; ORCiD logo [69];  [70]; ORCiD logo [71];  [72];  [22];  [57];  [73]; ORCiD logo [33];  [74];  [75];  [76];  [14];  [77];  [64]; ORCiD logo [7];  [78]; ORCiD logo [79]; ORCiD logo [80]; ORCiD logo [81] « less
  1. Kent State Univ., Kent, OH (United States)
  2. Oakland Univ., Rochester, MI (United States)
  3. Univ. of the Basque Country, Donostia (Spain); Ikerbasque, Bilbao (Spain)
  4. Univ., of Coimbra (Portugal)
  5. Univ. of Georgia, Athens, GA (United States)
  6. Universite de Lorraine, Metz (France)
  7. Trent Univ., Peterborough, ON (Canada)
  8. Leibniz Institute of Freshwater Ecology and Inland Fisheries, Stechlin (Germany); Berlin Institute of Technology (Germany)
  9. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  10. Univ. of Central Arkansas, Conway, AR (United States)
  11. Univ. of Southern Mississippi, Hattiesburg, MS (United States)
  12. Michigan Technological Univ., Houghton, MI (United States)
  13. Indiana Univ., Bloomington, IN (United States)
  14. Universidad Nacional Comahue, San Carlos de Bariloche (Argentina)
  15. Univ. of Central Washington, Ellensburg, WA (United States)
  16. Finnish Environment Institute, Helsinki (Finland)
  17. Idaho State Univ., Pocatello, ID (United States)
  18. City of Austin, TX (United States)
  19. Univ. of Applied Sciences and Arts of Southern Switzerland, Canobbio (Switzerland)
  20. Swiss Federal Institute of Aquatic Science and Technology, Dubendorf (Switzerland)
  21. Universidade Federal de Minas Gerais, Belo Horizonte (Brazil)
  22. Univ. of Valencia, Paterna (Spain)
  23. Claude Bernard University Lyon 1, Lyon (France)
  24. Univ. of Applied Sciences and Arts of Southern Switzerland, Manno (Switzerland)
  25. Pontifical Catholic University of Ecuador, Quito (Ecuador)
  26. Montana State Univ., Bozeman, MT (United States)
  27. Univ. Du Quebec a Montreal, Montreal (Canada)
  28. Univ. of Western Australia, Perth (Australia)
  29. Univ. of the Basque Country, Bilbao (Spain)
  30. Marine Institute, Galway (Ireland)
  31. Univ. of Coimbra (Portugal)
  32. Univ. of Valencia (Spain)
  33. Polish Academy of Sciences, Krakow (Poland)
  34. Univ. of Utah, Salt Lake City, UT (United States)
  35. UiT the Arctic University of Norway, Tromsø (Norway); Univ. of Tromsø (Norway)
  36. Charles Darwin University, Casuarina (Australia)
  37. Univ. of Vigo (Spain)
  38. Univ. of San Carlos of Guatemala, Guatamala City (Guatamala); Univ. of Montana, Missoula, MT (United States)
  39. Leibniz Institute of Freshwater Ecology and Inland Fisheries, Stechlin (Germany); Univ. of Canberra (Australia); CSIRO Land and Water, Canberra (Australia)
  40. Univerdiad Mayor de San Andres, La Paz (Bolivia)
  41. Leibniz Institute of Freshwater Ecology and Inland Fisheries, Stechlin (Germany); Potsdam University (Germany)
  42. Univ. of Lorraine, Metz (France)
  43. Federal University of Mato Grosso do Sul,Campo Grande (Brazil)
  44. International Institute for Sustainable Development, Winnipeg (Canada)
  45. Kyushu University (Japan)
  46. Universidad Tecnica Particular de Loja (Ecuador)
  47. Univ. of Yamanashi, Kofu (Japan)
  48. Ontario Tech University, Oshawa (Canada)
  49. Univ. of Nevada, Reno, NV (United States)
  50. Radboud University, Nijmegen (The Netherlands)
  51. Univ. of Agricultural Sciences, Umea (Sweden)
  52. Univ. of Regina (Canada)
  53. Federal University of Santa Catarina (Brazil)
  54. Memorial Univ. of Newfoundland, St. Johns (Canada)
  55. Evergreen State College, Olympia, WA (United States)
  56. Univ. of Wisconsin, Madison, WI (United States)
  57. Univ. of Eldoret (Kenya)
  58. Cornell Univ., Ithaca, NY (United States)
  59. Swedish Univ. of Agricultural Sciences, Uppsala (Sweden)
  60. Federal Univ. of Bahia, Salvador (Brazil)
  61. Univ. of Zagreb (Croatia)
  62. Ehime Univ., Matsuyama (Japan)
  63. Univ. of Oulu (Finland)
  64. Universidad Austral de Chile, Valdivia (Chile)
  65. National Antarctic Scientific Center of Ukraine, Kiev, (Ukraine); National Institute of Science of Ukraine, Kiev (Ukraine)
  66. College of William and Mary, Gloucester Point, VA (United States)
  67. Wageningen University (The Netherlands)
  68. Research Center on Ecosystems of Patagonia Centro de Investigacion en Ecosistemas de La Patagonia, Valdivia (Chile)
  69. Univ. of British Columbia, Vancouver (Canada)
  70. Universidad Del Zulia, Maracaibo (Venezuela)
  71. Univ. of Bucharest (Romania)
  72. Swiss Federal Institute of Aquatic Science and Technology, Dubendorf (Switzerland)
  73. Univ. of Latvia, Riga (Latvia)
  74. Umea University (Sweden)
  75. Universidad de La República (CURE), Maldonado (Uruguay)
  76. Univ. of Life Sciences, Tartu (Estonia)
  77. Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States)
  78. Canadian Rivers Institute, Saint John (Canada); Univ. of Waterloo, ON (Canada)
  79. Univ. of the Sunshine Coast, Maroochydore (Australia)
  80. Soochow Univ. (China); Univ. of Hong Kong, Kowloon (Hong Kong)
  81. US Geological Survey, Reston, VA (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Ecuadorian Ministry of Science; Oakland University Research Development; Huron Mountain Wildlife Foundation; Natural Sciences and Engineering Research Council
OSTI Identifier:
1855646
Alternate Identifier(s):
OSTI ID: 1855300
Grant/Contract Number:  
AC05-00OR22725; DE‐AC05‐00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Global Biogeochemical Cycles
Additional Journal Information:
Journal Volume: 36; Journal Issue: 3; Journal ID: ISSN 0886-6236
Publisher:
American Geophysical Union (AGU)
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES

Citation Formats

Costello, David M., Tiegs, Scott D., Boyero, Luz, Canhoto, Cristina, Capps, Krista A., Danger, Michael, Frost, Paul C., Gessner, Mark O., Griffiths, Natalie A., Halvorson, Halvor M., Kuehn, Kevin A., Marcarelli, Amy M., Royer, Todd V., Mathie, Devan M., Albariño, Ricardo J., Arango, Clay P., Aroviita, Jukka, Baxter, Colden V., Bellinger, Brent J., Bruder, Andreas, Burdon, Francis J., Callisto, Marcos, Camacho, Antonio, Colas, Fanny, Cornut, Julien, Crespo‐Pérez, Verónica, Cross, Wyatt F., Derry, Alison M., Douglas, Michael M., Elosegi, Arturo, Eyto, Elvira, Ferreira, Verónica, Ferriol, Carmen, Fleituch, Tadeusz, Follstad Shah, Jennifer J., Frainer, André, Garcia, Erica A., García, Liliana, García, Pavel E., Giling, Darren P., Gonzales‐Pomar, R. Karina, Graça, Manuel S., Grossart, Hans‐Peter, Guérold, François, Hepp, Luiz U., Higgins, Scott N., Hishi, Takuo, Iñiguez‐Armijos, Carlos, Iwata, Tomoya, Kirkwood, Andrea E., Koning, Aaron A., Kosten, Sarian, Laudon, Hjalmar, Leavitt, Peter R., Lemes da Silva, Aurea L., Leroux, Shawn J., LeRoy, Carri J., Lisi, Peter J., Masese, Frank O., McIntyre, Peter B., McKie, Brendan G., Medeiros, Adriana O., Miliša, Marko, Miyake, Yo, Mooney, Robert J., Muotka, Timo, Nimptsch, Jorge, Paavola, Riku, Pardo, Isabel, Parnikoza, Ivan Y., Patrick, Christopher J., Peeters, Edwin M., Pozo, Jesus, Reid, Brian, Richardson, John S., Rincón, José, Risnoveanu, Geta, Robinson, Christopher T., Santamans, Anna C., Simiyu, Gelas M., Skuja, Agnija, Smykla, Jerzy, Sponseller, Ryan A., Teixeira‐de Mello, Franco, Vilbaste, Sirje, Villanueva, Verónica D., Webster, Jackson R., Woelfl, Stefan, Xenopoulos, Marguerite A., Yates, Adam G., Yule, Catherine M., Zhang, Yixin, and Zwart, Jacob A. Global Patterns and Controls of Nutrient Immobilization on Decomposing Cellulose in Riverine Ecosystems. United States: N. p., 2022. Web. doi:10.1029/2021gb007163.
Costello, David M., Tiegs, Scott D., Boyero, Luz, Canhoto, Cristina, Capps, Krista A., Danger, Michael, Frost, Paul C., Gessner, Mark O., Griffiths, Natalie A., Halvorson, Halvor M., Kuehn, Kevin A., Marcarelli, Amy M., Royer, Todd V., Mathie, Devan M., Albariño, Ricardo J., Arango, Clay P., Aroviita, Jukka, Baxter, Colden V., Bellinger, Brent J., Bruder, Andreas, Burdon, Francis J., Callisto, Marcos, Camacho, Antonio, Colas, Fanny, Cornut, Julien, Crespo‐Pérez, Verónica, Cross, Wyatt F., Derry, Alison M., Douglas, Michael M., Elosegi, Arturo, Eyto, Elvira, Ferreira, Verónica, Ferriol, Carmen, Fleituch, Tadeusz, Follstad Shah, Jennifer J., Frainer, André, Garcia, Erica A., García, Liliana, García, Pavel E., Giling, Darren P., Gonzales‐Pomar, R. Karina, Graça, Manuel S., Grossart, Hans‐Peter, Guérold, François, Hepp, Luiz U., Higgins, Scott N., Hishi, Takuo, Iñiguez‐Armijos, Carlos, Iwata, Tomoya, Kirkwood, Andrea E., Koning, Aaron A., Kosten, Sarian, Laudon, Hjalmar, Leavitt, Peter R., Lemes da Silva, Aurea L., Leroux, Shawn J., LeRoy, Carri J., Lisi, Peter J., Masese, Frank O., McIntyre, Peter B., McKie, Brendan G., Medeiros, Adriana O., Miliša, Marko, Miyake, Yo, Mooney, Robert J., Muotka, Timo, Nimptsch, Jorge, Paavola, Riku, Pardo, Isabel, Parnikoza, Ivan Y., Patrick, Christopher J., Peeters, Edwin M., Pozo, Jesus, Reid, Brian, Richardson, John S., Rincón, José, Risnoveanu, Geta, Robinson, Christopher T., Santamans, Anna C., Simiyu, Gelas M., Skuja, Agnija, Smykla, Jerzy, Sponseller, Ryan A., Teixeira‐de Mello, Franco, Vilbaste, Sirje, Villanueva, Verónica D., Webster, Jackson R., Woelfl, Stefan, Xenopoulos, Marguerite A., Yates, Adam G., Yule, Catherine M., Zhang, Yixin, & Zwart, Jacob A. Global Patterns and Controls of Nutrient Immobilization on Decomposing Cellulose in Riverine Ecosystems. United States. https://doi.org/10.1029/2021gb007163
Costello, David M., Tiegs, Scott D., Boyero, Luz, Canhoto, Cristina, Capps, Krista A., Danger, Michael, Frost, Paul C., Gessner, Mark O., Griffiths, Natalie A., Halvorson, Halvor M., Kuehn, Kevin A., Marcarelli, Amy M., Royer, Todd V., Mathie, Devan M., Albariño, Ricardo J., Arango, Clay P., Aroviita, Jukka, Baxter, Colden V., Bellinger, Brent J., Bruder, Andreas, Burdon, Francis J., Callisto, Marcos, Camacho, Antonio, Colas, Fanny, Cornut, Julien, Crespo‐Pérez, Verónica, Cross, Wyatt F., Derry, Alison M., Douglas, Michael M., Elosegi, Arturo, Eyto, Elvira, Ferreira, Verónica, Ferriol, Carmen, Fleituch, Tadeusz, Follstad Shah, Jennifer J., Frainer, André, Garcia, Erica A., García, Liliana, García, Pavel E., Giling, Darren P., Gonzales‐Pomar, R. Karina, Graça, Manuel S., Grossart, Hans‐Peter, Guérold, François, Hepp, Luiz U., Higgins, Scott N., Hishi, Takuo, Iñiguez‐Armijos, Carlos, Iwata, Tomoya, Kirkwood, Andrea E., Koning, Aaron A., Kosten, Sarian, Laudon, Hjalmar, Leavitt, Peter R., Lemes da Silva, Aurea L., Leroux, Shawn J., LeRoy, Carri J., Lisi, Peter J., Masese, Frank O., McIntyre, Peter B., McKie, Brendan G., Medeiros, Adriana O., Miliša, Marko, Miyake, Yo, Mooney, Robert J., Muotka, Timo, Nimptsch, Jorge, Paavola, Riku, Pardo, Isabel, Parnikoza, Ivan Y., Patrick, Christopher J., Peeters, Edwin M., Pozo, Jesus, Reid, Brian, Richardson, John S., Rincón, José, Risnoveanu, Geta, Robinson, Christopher T., Santamans, Anna C., Simiyu, Gelas M., Skuja, Agnija, Smykla, Jerzy, Sponseller, Ryan A., Teixeira‐de Mello, Franco, Vilbaste, Sirje, Villanueva, Verónica D., Webster, Jackson R., Woelfl, Stefan, Xenopoulos, Marguerite A., Yates, Adam G., Yule, Catherine M., Zhang, Yixin, and Zwart, Jacob A. Fri . "Global Patterns and Controls of Nutrient Immobilization on Decomposing Cellulose in Riverine Ecosystems". United States. https://doi.org/10.1029/2021gb007163. https://www.osti.gov/servlets/purl/1855646.
@article{osti_1855646,
title = {Global Patterns and Controls of Nutrient Immobilization on Decomposing Cellulose in Riverine Ecosystems},
author = {Costello, David M. and Tiegs, Scott D. and Boyero, Luz and Canhoto, Cristina and Capps, Krista A. and Danger, Michael and Frost, Paul C. and Gessner, Mark O. and Griffiths, Natalie A. and Halvorson, Halvor M. and Kuehn, Kevin A. and Marcarelli, Amy M. and Royer, Todd V. and Mathie, Devan M. and Albariño, Ricardo J. and Arango, Clay P. and Aroviita, Jukka and Baxter, Colden V. and Bellinger, Brent J. and Bruder, Andreas and Burdon, Francis J. and Callisto, Marcos and Camacho, Antonio and Colas, Fanny and Cornut, Julien and Crespo‐Pérez, Verónica and Cross, Wyatt F. and Derry, Alison M. and Douglas, Michael M. and Elosegi, Arturo and Eyto, Elvira and Ferreira, Verónica and Ferriol, Carmen and Fleituch, Tadeusz and Follstad Shah, Jennifer J. and Frainer, André and Garcia, Erica A. and García, Liliana and García, Pavel E. and Giling, Darren P. and Gonzales‐Pomar, R. Karina and Graça, Manuel S. and Grossart, Hans‐Peter and Guérold, François and Hepp, Luiz U. and Higgins, Scott N. and Hishi, Takuo and Iñiguez‐Armijos, Carlos and Iwata, Tomoya and Kirkwood, Andrea E. and Koning, Aaron A. and Kosten, Sarian and Laudon, Hjalmar and Leavitt, Peter R. and Lemes da Silva, Aurea L. and Leroux, Shawn J. and LeRoy, Carri J. and Lisi, Peter J. and Masese, Frank O. and McIntyre, Peter B. and McKie, Brendan G. and Medeiros, Adriana O. and Miliša, Marko and Miyake, Yo and Mooney, Robert J. and Muotka, Timo and Nimptsch, Jorge and Paavola, Riku and Pardo, Isabel and Parnikoza, Ivan Y. and Patrick, Christopher J. and Peeters, Edwin M. and Pozo, Jesus and Reid, Brian and Richardson, John S. and Rincón, José and Risnoveanu, Geta and Robinson, Christopher T. and Santamans, Anna C. and Simiyu, Gelas M. and Skuja, Agnija and Smykla, Jerzy and Sponseller, Ryan A. and Teixeira‐de Mello, Franco and Vilbaste, Sirje and Villanueva, Verónica D. and Webster, Jackson R. and Woelfl, Stefan and Xenopoulos, Marguerite A. and Yates, Adam G. and Yule, Catherine M. and Zhang, Yixin and Zwart, Jacob A.},
abstractNote = {Abstract Microbes play a critical role in plant litter decomposition and influence the fate of carbon in rivers and riparian zones. When decomposing low‐nutrient plant litter, microbes acquire nitrogen (N) and phosphorus (P) from the environment (i.e., nutrient immobilization), and this process is potentially sensitive to nutrient loading and changing climate. Nonetheless, environmental controls on immobilization are poorly understood because rates are also influenced by plant litter chemistry, which is coupled to the same environmental factors. Here we used a standardized, low‐nutrient organic matter substrate (cotton strips) to quantify nutrient immobilization at 100 paired stream and riparian sites representing 11 biomes worldwide. Immobilization rates varied by three orders of magnitude, were greater in rivers than riparian zones, and were strongly correlated to decomposition rates. In rivers, P immobilization rates were controlled by surface water phosphate concentrations, but N immobilization rates were not related to inorganic N. The N:P of immobilized nutrients was tightly constrained to a molar ratio of 10:1 despite wide variation in surface water N:P. Immobilization rates were temperature‐dependent in riparian zones but not related to temperature in rivers. However, in rivers nutrient supply ultimately controlled whether microbes could achieve the maximum expected decomposition rate at a given temperature. Collectively, we demonstrated that exogenous nutrient supply and immobilization are critical control points for decomposition of organic matter.},
doi = {10.1029/2021gb007163},
journal = {Global Biogeochemical Cycles},
number = 3,
volume = 36,
place = {United States},
year = {Fri Feb 18 00:00:00 EST 2022},
month = {Fri Feb 18 00:00:00 EST 2022}
}

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journal, November 1986


Changes in nutrient stoichiometry, elemental homeostasis and growth rate of aquatic litter-associated fungi in response to inorganic nutrient supply
journal, July 2017

  • Gulis, Vladislav; Kuehn, Kevin A.; Schoettle, Louie N.
  • The ISME Journal, Vol. 11, Issue 12
  • DOI: 10.1038/ismej.2017.123

Towards a simple global-standard bioassay for a key ecosystem process: organic-matter decomposition using cotton strips
journal, November 2019


Global distribution of atmospheric phosphorus sources, concentrations and deposition rates, and anthropogenic impacts: GLOBAL ATMOSPHERIC PHOSPHORUS
journal, December 2008

  • Mahowald, Natalie; Jickells, Timothy D.; Baker, Alex R.
  • Global Biogeochemical Cycles, Vol. 22, Issue 4
  • DOI: 10.1029/2008GB003240

The relative importance of exogenous and substrate-derived nitrogen for microbial growth during leaf decomposition
journal, July 2013

  • Cheever, B. M.; Webster, J. R.; Bilger, E. E.
  • Ecology, Vol. 94, Issue 7
  • DOI: 10.1890/12-1339.1

A standardized cotton-strip assay for measuring organic-matter decomposition in streams
journal, September 2013


A review of allochthonous organic matter dynamics and metabolism in streams
journal, March 2010

  • Tank, Jennifer L.; Rosi-Marshall, Emma J.; Griffiths, Natalie A.
  • Journal of the North American Benthological Society, Vol. 29, Issue 1
  • DOI: 10.1899/08-170.1

Understanding the dominant controls on litter decomposition
journal, November 2015

  • Bradford, Mark A.; Berg, Björn; Maynard, Daniel S.
  • Journal of Ecology, Vol. 104, Issue 1
  • DOI: 10.1111/1365-2745.12507

Additive effects of experimental climate change and land use on faunal contribution to litter decomposition
journal, April 2019


Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: What lies ahead?
journal, August 2015

  • Classen, Aimée T.; Sundqvist, Maja K.; Henning, Jeremiah A.
  • Ecosphere, Vol. 6, Issue 8
  • DOI: 10.1890/ES15-00217.1

A test of the hierarchical model of litter decomposition
journal, November 2017