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Title: 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 » 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.« less

Authors:
 [1];  [1];  [2];  [3];  [4];  [3];  [5];  [6];  [7];  [8];  [8]
  1. Univ. of Oklahoma, Norman, OK (United States). Dept. of Biology, Graduate Program in Ecology and Evolutionary Biology; Smithsonian Tropical Research Institute, Balboa, Ancon (Panama)
  2. Univ. of Oklahoma, Norman, OK (United States). Dept. of Biology, Graduate Program in Ecology and Evolutionary Biology
  3. Univ. of Oklahoma, Norman, OK (United States). Dept. of Botany and Microbiology, Inst. for Environmental Genomics
  4. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology; Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  5. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology; Santa Fe Inst., Santa Fe, NM (United States)
  6. Univ. of New Mexico, Albuquerque, NM (United States). Dept. of Biology, and LTER Network Office
  7. 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
  8. 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}
}

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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
  • DOI: 10.1086/285289

Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies
journal, October 2008


Salted roads and sodium limitation in a northern forest ant community
journal, June 2010


Intestinal Microbiota of Millipedes
book, January 2006

  • Byzov, Boris A.
  • Intestinal Microorganisms of Termites and Other Invertebrates. Soil Biology
  • DOI: 10.1007/3-540-28185-1_4

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
  • DOI: 10.1073/pnas.0403588101

Spatial scales of soil bacterial diversity – the size of a clone
journal, May 2004


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
  • DOI: 10.1111/mec.12259

Spatial scale dictates the productivity–biodiversity relationship
journal, March 2002

  • Chase, Jonathan M.; Leibold, Mathew A.
  • Nature, Vol. 416, Issue 6879
  • DOI: 10.1038/416427a

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
  • DOI: 10.2307/1312897

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
  • DOI: 10.1086/687576

Ecological stoichiometry and the shape of resource-based tradeoffs
journal, February 2006


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
  • DOI: 10.1086/286187

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
  • DOI: 10.1099/00221287-148-4-933

Light, earthworms, and soil resources as predictors of diversity of 10 soil invertebrate groups across monocultures of 14 tree species
journal, January 2016


Comparative Genomic Structure of Prokaryotes
journal, December 2004


The diversity of fungal genome
journal, April 2015


Nutrient co-limitation of primary producer communities: Community co-limitation
journal, July 2011


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
  • DOI: 10.1038/nature19324

The Mineral Nutrition of Wild Plants
journal, November 1980


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
  • DOI: 10.1007/BF01007574

Biogeochemical drivers of Neotropical ant activity and diversity
journal, December 2016

  • Bujan, Jelena; Wright, S. Joseph; Kaspari, Michael
  • Ecosphere, Vol. 7, Issue 12
  • DOI: 10.1002/ecs2.1597

Scientific method: Statistical errors
journal, February 2014


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
  • DOI: 10.2307/3761366

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
  • DOI: 10.1890/14-1362.1

Variation in aluminum resistance among arbuscular mycorrhizal fungi
journal, August 2004


A mechanism of aluminium toxicity to soil bacteria and possible ecological implications
journal, April 1995


Living in a fungal world: impact of fungi on soil bacterial niche development
journal, September 2005


Grassland species loss resulting from reduced niche dimension
journal, March 2007


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
  • DOI: 10.1073/pnas.0504756102

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
  • DOI: 10.1029/2008GB003376

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
  • DOI: 10.1038/ismej.2010.58

Microbial Evolution in the Wild
journal, April 2012


Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three?
journal, October 2006


Grassland productivity limited by multiple nutrients
journal, July 2015

  • Fay, Philip A.; Prober, Suzanne M.; Harpole, W. Stanley
  • Nature Plants, Vol. 1, Issue 7
  • DOI: 10.1038/nplants.2015.80

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
  • DOI: 10.2136/sssaj2012.0128

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
  • DOI: 10.1007/978-94-011-4645-6_4

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
  • DOI: 10.1890/08-1140.1

Limiting Resources and the Regulation of Diversity in Phytoplankton Communities
journal, May 2001


Separating the influence of resource ‘availability’ from resource ‘imbalance’ on productivity-diversity relationships
journal, June 2009


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
  • DOI: 10.1890/090050

Numerical abundance and biodiversity of below-ground taxocenes along a pH gradient across the Netherlands
journal, October 2005


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
  • DOI: 10.1073/pnas.1515241113

Paradox of Enrichment: Destabilization of Exploitation Ecosystems in Ecological Time
journal, January 1971


Biogeochemistry and the structure of tropical brown food webs
journal, December 2009

  • Kaspari, Michael; Yanoviak, Stephen P.
  • Ecology, Vol. 90, Issue 12
  • DOI: 10.1890/08-1795.1

Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes
journal, February 2012


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
  • DOI: 10.1073/pnas.0408648102

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
  • DOI: 10.1086/367906

Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems
journal, January 1999


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
  • DOI: 10.1890/10-1558.1

Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition: Tropical tree seedling N-P-K responses
journal, October 2011


Seasonal changes in soil organic matter after a decade of nutrient addition in a lowland tropical forest
journal, January 2015


Soil–Plant–Animal and Human Interrelationships in Trace Element Nutrition
book, January 1986


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
  • DOI: 10.1890/10-0426.1

The fate of phosphorus during pedogenesis
journal, January 1976


Give soils their due
journal, February 2015


Reconciling plant strategy theories of Grime and Tilman
journal, July 2005


What is the Observed Relationship Between Species Richness and Productivity?
journal, September 2001


Multiple nutrients limit litterfall and decomposition in a tropical forest
journal, November 2007


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
  • DOI: 10.1111/ecog.02314

A mechanism of aluminium toxicity to soil bacteria and possible ecological implications
book, January 1995


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
  • DOI: 10.1007/s11356-020-12331-5

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
  • DOI: 10.2307/2463354

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
  • DOI: 10.17615/zm6b-t820

Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians
journal, March 1999


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
  • DOI: 10.1002/ecm.1279

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
  • DOI: 10.1111/gcb.14750

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
  • DOI: 10.1098/rspb.2019.1536

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
  • DOI: 10.1002/ecy.2732

Intensive tropical land use massively shifts soil fungal communities
journal, March 2019


Biogeochemistry and forest composition shape nesting patterns of a dominant canopy ant
journal, December 2018


Prey’s traits mediate a neotropical toad diet
posted_content, November 2018