Biogeochemistry drives diversity in the prokaryotes, fungi, and invertebrates of a Panama forest
Abstract
Humans are both fertilizing the world and depleting its soils, decreasing the diversity of aquatic ecosystems and terrestrial plants in the process. We know less about how nutrients shape the abundance and diversity of the prokaryotes, fungi, and invertebrates of Earth's soils. Here in this paper we explore this question in the soils of a Panama forest subject to a 13-yr fertilization with factorial combinations of nitrogen (N), phosphorus (P), and potassium (K) and a separate micronutrient cocktail. We contrast three hypotheses linking biogeochemistry to abundance and diversity. Consistent with the Stress Hypothesis, adding N suppressed the abundance of invertebrates and the richness of all three groups of organisms by ca. 1 SD or more below controls. Nitrogen addition plots were 0.8 pH units more acidic with 18% more exchangeable aluminum, which is toxic to both prokaryotes and eukaryotes. These stress effects were frequently reversed, however, when N was added with P (for prokaryotes and invertebrates) and with added K (for fungi). Consistent with the Abundance Hypothesis, adding P generally increased prokaryote and invertebrate diversity, and adding K enhanced invertebrate diversity. Also consistent with the Abundance Hypothesis, increases in invertebrate abundance generated increases in richness. We found little evidence for themore »
- Authors:
-
- Univ. of Oklahoma, Norman, OK (United States). Dept. of Biology, Graduate Program in Ecology and Evolutionary Biology; Smithsonian Tropical Research Institute, Balboa, Ancon (Panama)
- Univ. of Oklahoma, Norman, OK (United States). Dept. of Biology, Graduate Program in Ecology and Evolutionary Biology
- Univ. of Oklahoma, Norman, OK (United States). Dept. of Botany and Microbiology, Inst. for Environmental Genomics
- Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology; Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
- Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology; Santa Fe Inst., Santa Fe, NM (United States)
- Univ. of New Mexico, Albuquerque, NM (United States). Dept. of Biology, and LTER Network Office
- Univ. of Oklahoma, Norman, OK (United States). Dept. of Botany and Microbiology, Inst. for Environmental Genomics; Chinese Academy of Sciences (CAS), Beijing (China). CAS Key Lab. of Environmental Biotechnology, Research Center for Eco-Environmental Sciences
- Smithsonian Tropical Research Institute, Balboa, Ancon (Panama)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1479322
- Grant/Contract Number:
- AC02-05CH11231; EF‐1065844
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Ecology
- Additional Journal Information:
- Journal Volume: 98; Journal Issue: 8; Journal ID: ISSN 0012-9658
- Publisher:
- Ecological Society of America (ESA)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; biogeochemistry; brown food web; richness; soil; tropics
Citation Formats
Kaspari, Michael, Bujan, Jelena, Weiser, Michael D., Ning, Daliang, Michaletz, Sean T., Zhili, He, Enquist, Brian J., Waide, Robert B., Zhou, Jizhong, Turner, Benjamin L., and Wright, S. Joseph. Biogeochemistry drives diversity in the prokaryotes, fungi, and invertebrates of a Panama forest. United States: N. p., 2017.
Web. doi:10.1002/ecy.1895.
Kaspari, Michael, Bujan, Jelena, Weiser, Michael D., Ning, Daliang, Michaletz, Sean T., Zhili, He, Enquist, Brian J., Waide, Robert B., Zhou, Jizhong, Turner, Benjamin L., & Wright, S. Joseph. Biogeochemistry drives diversity in the prokaryotes, fungi, and invertebrates of a Panama forest. United States. https://doi.org/10.1002/ecy.1895
Kaspari, Michael, Bujan, Jelena, Weiser, Michael D., Ning, Daliang, Michaletz, Sean T., Zhili, He, Enquist, Brian J., Waide, Robert B., Zhou, Jizhong, Turner, Benjamin L., and Wright, S. Joseph. Sat .
"Biogeochemistry drives diversity in the prokaryotes, fungi, and invertebrates of a Panama forest". United States. https://doi.org/10.1002/ecy.1895. https://www.osti.gov/servlets/purl/1479322.
@article{osti_1479322,
title = {Biogeochemistry drives diversity in the prokaryotes, fungi, and invertebrates of a Panama forest},
author = {Kaspari, Michael and Bujan, Jelena and Weiser, Michael D. and Ning, Daliang and Michaletz, Sean T. and Zhili, He and Enquist, Brian J. and Waide, Robert B. and Zhou, Jizhong and Turner, Benjamin L. and Wright, S. Joseph},
abstractNote = {Humans are both fertilizing the world and depleting its soils, decreasing the diversity of aquatic ecosystems and terrestrial plants in the process. We know less about how nutrients shape the abundance and diversity of the prokaryotes, fungi, and invertebrates of Earth's soils. Here in this paper we explore this question in the soils of a Panama forest subject to a 13-yr fertilization with factorial combinations of nitrogen (N), phosphorus (P), and potassium (K) and a separate micronutrient cocktail. We contrast three hypotheses linking biogeochemistry to abundance and diversity. Consistent with the Stress Hypothesis, adding N suppressed the abundance of invertebrates and the richness of all three groups of organisms by ca. 1 SD or more below controls. Nitrogen addition plots were 0.8 pH units more acidic with 18% more exchangeable aluminum, which is toxic to both prokaryotes and eukaryotes. These stress effects were frequently reversed, however, when N was added with P (for prokaryotes and invertebrates) and with added K (for fungi). Consistent with the Abundance Hypothesis, adding P generally increased prokaryote and invertebrate diversity, and adding K enhanced invertebrate diversity. Also consistent with the Abundance Hypothesis, increases in invertebrate abundance generated increases in richness. We found little evidence for the Competition Hypothesis: that single nutrients suppressed diversity by favoring a subset of high nutrient specialists, and that nutrient combinations suppressed diversity even more. Instead, combinations of nutrients, and especially the cation/micronutrient treatment, yielded the largest increases in richness in the two eukaryote groups. In sum, changes in soil biogeochemistry revealed a diversity of responses among the three dominant soil groups, positive synergies among nutrients, and–in contrast with terrestrial plants–the frequent enhancement of soil biodiversity.},
doi = {10.1002/ecy.1895},
journal = {Ecology},
number = 8,
volume = 98,
place = {United States},
year = {Sat May 13 00:00:00 EDT 2017},
month = {Sat May 13 00:00:00 EDT 2017}
}
Web of Science
Works referenced in this record:
Long-Term Experimental Evolution in Escherichia coli. I. Adaptation and Divergence During 2,000 Generations
journal, December 1991
- Lenski, Richard E.; Rose, Michael R.; Simpson, Suzanne C.
- The American Naturalist, Vol. 138, Issue 6
Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies
journal, October 2008
- Treseder, Kathleen K.
- Ecology Letters, Vol. 11, Issue 10
Salted roads and sodium limitation in a northern forest ant community
journal, June 2010
- Kaspari, Michael; Chang, Charlotte; Weaver, Johanna
- Ecological Entomology, Vol. 35, Issue 5
Intestinal Microbiota of Millipedes
book, January 2006
- Byzov, Boris A.
- Intestinal Microorganisms of Termites and Other Invertebrates. Soil Biology
Global patterns of plant leaf N and P in relation to temperature and latitude
journal, June 2004
- Reich, P. B.; Oleksyn, J.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 30
Spatial scales of soil bacterial diversity â the size of a clone
journal, May 2004
- Grundmann, Geneviève L.
- FEMS Microbiology Ecology, Vol. 48, Issue 2
Nutrient enrichment increased species richness of leaf litter fungal assemblages in a tropical forest
journal, April 2013
- Kerekes, Jennifer; Kaspari, Michael; Stevenson, Bradley
- Molecular Ecology, Vol. 22, Issue 10
Spatial scale dictates the productivity–biodiversity relationship
journal, March 2002
- Chase, Jonathan M.; Leibold, Mathew A.
- Nature, Vol. 416, Issue 6879
Organism Size, Life History, and N:P Stoichiometry
journal, October 1996
- Elser, James J.; Dobberfuhl, Dean R.; MacKay, Neil A.
- BioScience, Vol. 46, Issue 9
Biogeochemistry and Geographical Ecology: Embracing All Twenty-Five Elements Required to Build Organisms
journal, September 2016
- Kaspari, Michael; Powers, Jennifer S.
- The American Naturalist, Vol. 188, Issue S1
Ecological stoichiometry and the shape of resource-based tradeoffs
journal, February 2006
- Yoshida, Takehito
- Oikos, Vol. 112, Issue 2
Why More Productive Sites Have More Species: An Experimental Test of Theory Using Tree‐Hole Communities
journal, October 1998
- Srivastava, Diane S.; Lawton, John H.
- The American Naturalist, Vol. 152, Issue 4
Potassium- or sodium-efflux ATPase, a key enzyme in the evolution of fungi
journal, April 2002
- Rodrı́guez-Navarro, Alonso; Garciadeblás, Blanca; Benito, Begoña
- Microbiology, Vol. 148, Issue 4
Light, earthworms, and soil resources as predictors of diversity of 10 soil invertebrate groups across monocultures of 14 tree species
journal, January 2016
- Mueller, Kevin E.; Eisenhauer, Nico; Reich, Peter B.
- Soil Biology and Biochemistry, Vol. 92
Comparative Genomic Structure of Prokaryotes
journal, December 2004
- Bentley, Stephen D.; Parkhill, Julian
- Annual Review of Genetics, Vol. 38, Issue 1
The diversity of fungal genome
journal, April 2015
- Mohanta, Tapan Kumar; Bae, Hanhong
- Biological Procedures Online, Vol. 17, Issue 1
Nutrient co-limitation of primary producer communities: Community co-limitation
journal, July 2011
- Harpole, W. Stanley; Ngai, Jacqueline T.; Cleland, Elsa E.
- Ecology Letters, Vol. 14, Issue 9
Addition of multiple limiting resources reduces grassland diversity
journal, August 2016
- Harpole, W. Stanley; Sullivan, Lauren L.; Lind, Eric M.
- Nature, Vol. 537, Issue 7618
The Mineral Nutrition of Wild Plants
journal, November 1980
- Chapin, F. S.
- Annual Review of Ecology and Systematics, Vol. 11, Issue 1
The globalization of N deposition: ecosystem consequences in tropical environments
journal, July 1999
- Matson, Pamela A.; McDowell, William H.; Townsend, Alan R.
- Biogeochemistry, Vol. 46, Issue 1-3
Biogeochemical drivers of Neotropical ant activity and diversity
journal, December 2016
- Bujan, Jelena; Wright, S. Joseph; Kaspari, Michael
- Ecosphere, Vol. 7, Issue 12
Scientific method: Statistical errors
journal, February 2014
- Nuzzo, Regina
- Nature, Vol. 506, Issue 7487
Batrachochytrium Dendrobatidis gen. et sp. nov., a Chytrid Pathogenic to Amphibians
journal, March 1999
- Longcore, Joyce E.; Pessier, Allan P.; Nichols, Donald K.
- Mycologia, Vol. 91, Issue 2
Fine-root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest
journal, August 2015
- Wurzburger, Nina; Wright, S. Joseph
- Ecology, Vol. 96, Issue 8
Variation in aluminum resistance among arbuscular mycorrhizal fungi
journal, August 2004
- Kelly, C. N.; Morton, J. B.; Cumming, J. R.
- Mycorrhiza, Vol. 15, Issue 3
A mechanism of aluminium toxicity to soil bacteria and possible ecological implications
journal, April 1995
- Wood, Martin
- Plant and Soil, Vol. 171, Issue 1
Living in a fungal world: impact of fungi on soil bacterial niche development
journal, September 2005
- Boer, Wietse de; Folman, Larissa B.; Summerbell, Richard C.
- FEMS Microbiology Reviews, Vol. 29, Issue 4
Grassland species loss resulting from reduced niche dimension
journal, March 2007
- Harpole, W. Stanley; Tilman, David
- Nature, Vol. 446, Issue 7137
Factors Influencing Species Composition in Tropical Lowland rain Forest: does soil Matter?
journal, January 1998
- Sollins, Phillip
- Ecology, Vol. 79, Issue 1
The metabolic basis of whole-organism RNA and phosphorus content
journal, August 2005
- Gillooly, J. F.; Allen, A. P.; Brown, J. H.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 33
Earth's global Ag, Al, Cr, Cu, Fe, Ni, Pb, and Zn cycles: GLOBAL METAL CYCLES
journal, April 2009
- Rauch, Jason N.; Pacyna, Jozef M.
- Global Biogeochemical Cycles, Vol. 23, Issue 2
Soil bacterial and fungal communities across a pH gradient in an arable soil
journal, May 2010
- Rousk, Johannes; Bååth, Erland; Brookes, Philip C.
- The ISME Journal, Vol. 4, Issue 10
Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three?
journal, October 2006
- Högberg, Mona N.; Högberg, Peter; Myrold, David D.
- Oecologia, Vol. 150, Issue 4
Grassland productivity limited by multiple nutrients
journal, July 2015
- Fay, Philip A.; Prober, Suzanne M.; Harpole, W. Stanley
- Nature Plants, Vol. 1, Issue 7
Seasonal Changes and Treatment Effects on Soil Inorganic Nutrients Following a Decade of Fertilizer Addition in a Lowland Tropical Forest
journal, January 2013
- Turner, Benjamin L.; Yavitt, Joseph B.; Harms, Kyle E.
- Soil Science Society of America Journal, Vol. 77, Issue 4
The globalization of N deposition: ecosystem consequences in tropical environments
book, January 1999
- Matson, Pamela A.; Mcdowell, William H.; Townsend, Alan R.
- New Perspectives on Nitrogen Cycling in the Temperate and Tropical Americas
Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis
journal, January 2010
- Bobbink, R.; Hicks, K.; Galloway, J.
- Ecological Applications, Vol. 20, Issue 1
Limiting Resources and the Regulation of Diversity in Phytoplankton Communities
journal, May 2001
- Interlandi, Sebastian J.; Kilham, Susan S.
- Ecology, Vol. 82, Issue 5
Separating the influence of resource ‘availability’ from resource ‘imbalance’ on productivity-diversity relationships
journal, June 2009
- Cardinale, Bradley J.; Hillebrand, Helmut; Harpole, W. S.
- Ecology Letters, Vol. 12, Issue 6
The ecology of dust
journal, October 2010
- Field, Jason P.; Belnap, Jayne; Breshears, David D.
- Frontiers in Ecology and the Environment, Vol. 8, Issue 8
Numerical abundance and biodiversity of below-ground taxocenes along a pH gradient across the Netherlands
journal, October 2005
- Mulder, Christian; Van Wijnen, Harm J.; Van Wezel, Annemarie P.
- Journal of Biogeography, Vol. 32, Issue 10
Conditional vulnerability of plant diversity to atmospheric nitrogen deposition across the United States
journal, March 2016
- Simkin, Samuel M.; Allen, Edith B.; Bowman, William D.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 15
Paradox of Enrichment: Destabilization of Exploitation Ecosystems in Ecological Time
journal, January 1971
- Rosenzweig, M. L.
- Science, Vol. 171, Issue 3969
Biogeochemistry and the structure of tropical brown food webs
journal, December 2009
- Kaspari, Michael; Yanoviak, Stephen P.
- Ecology, Vol. 90, Issue 12
Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes
journal, February 2012
- Ramirez, Kelly S.; Craine, Joseph M.; Fierer, Noah
- Global Change Biology, Vol. 18, Issue 6
Functional- and abundance-based mechanisms explain diversity loss due to N fertilization
journal, March 2005
- Suding, K. N.; Collins, S. L.; Gough, L.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 12
Spatial Grain and the Causes of Regional Diversity Gradients in Ants
journal, March 2003
- Kaspari, Michael; Yuan, May; Alonso, Leeanne
- The American Naturalist, Vol. 161, Issue 3
Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems
journal, January 1999
- Smith, V. H.; Tilman, G. D.; Nekola, J. C.
- Environmental Pollution, Vol. 100, Issue 1-3
Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest
journal, August 2011
- Wright, S. Joseph; Yavitt, Joseph B.; Wurzburger, Nina
- Ecology, Vol. 92, Issue 8
Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition: Tropical tree seedling N-P-K responses
journal, October 2011
- Santiago, Louis S.; Wright, S. Joseph; Harms, Kyle E.
- Journal of Ecology, Vol. 100, Issue 2
Seasonal changes in soil organic matter after a decade of nutrient addition in a lowland tropical forest
journal, January 2015
- Turner, Benjamin L.; Yavitt, Joseph B.; Harms, Kyle E.
- Biogeochemistry, Vol. 123, Issue 1-2
Soil–Plant–Animal and Human Interrelationships in Trace Element Nutrition
book, January 1986
- Allaway, W. H.
- Trace Elements in Human and Animal Nutrition
Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems
journal, December 2010
- Ramirez, Kelly S.; Lauber, Christian L.; Knight, Rob
- Ecology, Vol. 91, Issue 12
The fate of phosphorus during pedogenesis
journal, January 1976
- Walker, T. W.; Syers, J. K.
- Geoderma, Vol. 15, Issue 1
Reconciling plant strategy theories of Grime and Tilman
journal, July 2005
- Craine, Joseph M.
- Journal of Ecology, Vol. 93, Issue 6
What is the Observed Relationship Between Species Richness and Productivity?
journal, September 2001
- Mittelbach, Gary G.; Steiner, Christopher F.; Scheiner, Samuel M.
- Ecology, Vol. 82, Issue 9
Multiple nutrients limit litterfall and decomposition in a tropical forest
journal, November 2007
- Kaspari, Michael; Garcia, Milton N.; Harms, Kyle E.
- Ecology Letters, Vol. 0, Issue 0
Basin-Wide Effects of Game Harvest on Vertebrate Population Densities in Amazonian Forests: Implications for Animal-Mediated Seed Dispersal
journal, May 2007
- Peres, Carlos A.; Palacios, Erwin
- Biotropica, Vol. 39, Issue 3
Toward a theory for diversity gradients: the abundance-adaptation hypothesis
journal, April 2017
- Weiser, Michael D.; Michaletz, Sean T.; Buzzard, Vanessa
- Ecography, Vol. 41, Issue 2
A mechanism of aluminium toxicity to soil bacteria and possible ecological implications
book, January 1995
- Wood, Martin
- Plant-Soil Interactions at Low pH: Principles and Management
Population structure and body size of the Sahara blue-eyed pond turtle Mauremys leprosa saharica, from an isolated pond in the Lower Draa Basin, southern Morocco
journal, January 2021
- Loulida, Soumia; Znari, Mohammed; Naimi, Mohamed
- Environmental Science and Pollution Research, Vol. 28, Issue 18
Why More Productive Sites Have More Species: An Experimental Test of Theory Using Tree-Hole Communities
journal, October 1998
- Srivastava, Diane S.; Lawton, John H.
- The American Naturalist, Vol. 152, Issue 4, p. 510
Grassland productivity limited by multiple nutrients
text, January 2015
- Scott, Collins,; Eric, Lind,; Stanley, Harpole, W.
- The University of North Carolina at Chapel Hill University Libraries
Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians
journal, March 1999
- Longcore, Joyce E.; Pessier, Allan P.; Nichols, Donald K.
- Mycologia, Vol. 91, Issue 2
Works referencing / citing this record:
Nutrient limitation of soil microbial processes in tropical forests
journal, November 2017
- Camenzind, Tessa; Hättenschwiler, Stephan; Treseder, Kathleen K.
- Ecological Monographs, Vol. 88, Issue 1
Long‐term nitrogen addition modifies microbial composition and functions for slow carbon cycling and increased sequestration in tropical forest soil
journal, August 2019
- Tian, Jing; Dungait, Jennifer A. J.; Lu, Xiankai
- Global Change Biology, Vol. 25, Issue 10
Antibiotics as chemical warfare across multiple taxonomic domains and trophic levels in brown food webs
journal, September 2019
- Lucas, Jane M.; Gora, Evan; Salzberg, Annika
- Proceedings of the Royal Society B: Biological Sciences, Vol. 286, Issue 1911
The stoichiometric legacy of fire regime regulates the roles of micro‐organisms and invertebrates in decomposition
journal, March 2019
- Butler, Orpheus M.; Lewis, Tom; Rezaei Rashti, Mehran
- Ecology, Vol. 100, Issue 7
Intensive tropical land use massively shifts soil fungal communities
journal, March 2019
- Brinkmann, Nicole; Schneider, Dominik; Sahner, Josephine
- Scientific Reports, Vol. 9, Issue 1
Nutrient Dynamics in Decomposing Dead Wood in the Context of Wood Eater Requirements: The Ecological Stoichiometry of Saproxylophagous Insects
book, January 2018
- Filipiak, Michał
- Saproxylic Insects
Biogeochemistry and forest composition shape nesting patterns of a dominant canopy ant
journal, December 2018
- Bujan, Jelena; Wright, S. Joseph; Kaspari, Michael
- Oecologia, Vol. 189, Issue 1
Prey’s traits mediate a neotropical toad diet
posted_content, November 2018
- McElroy, Matthew T.; Donoso, David A.