The toughest animals of the Earth versus global warming: Effects of long‐term experimental warming on tardigrade community structure of a temperate deciduous forest

Understanding how different taxa respond to global warming is essential for predicting future changes and elaborating strategies to buffer them. Tardigrades are well known for their ability to survive environmental stressors, such as drying and freezing, by undergoing cryptobiosis and rapidly recove...

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Published in:Ecology and Evolution
Main Authors: Vecchi, Matteo, Kossi Adakpo, Laurent, Dunn, Robert R., Nichols, Lauren M., Penick, Clint A., Sanders, Nathan J., Rebecchi, Lorena, Guidetti, Roberto
Format: Article in Journal/Newspaper
Language:unknown
Published: Academic Publishers 2021
Subjects:
Tardigrades
climate change
experimental
global warming
water bears
Ecology and Evolutionary Biology
Science
Water Bears
Antarctic Science
Tardigrade
Online Access:https://hdl.handle.net/2027.42/168469
https://doi.org/10.1002/ece3.7816
id ftumdeepblue:oai:deepblue.lib.umich.edu:2027.42/168469
record_format openpolar
institution Open Polar
collection University of Michigan: Deep Blue
op_collection_id ftumdeepblue
language unknown
topic Tardigrades
climate change
experimental
global warming
water bears
Ecology and Evolutionary Biology
Science
spellingShingle Tardigrades
climate change
experimental
global warming
water bears
Ecology and Evolutionary Biology
Science
Vecchi, Matteo
Kossi Adakpo, Laurent
Dunn, Robert R.
Nichols, Lauren M.
Penick, Clint A.
Sanders, Nathan J.
Rebecchi, Lorena
Guidetti, Roberto
The toughest animals of the Earth versus global warming: Effects of long‐term experimental warming on tardigrade community structure of a temperate deciduous forest
topic_facet Tardigrades
climate change
experimental
global warming
water bears
Ecology and Evolutionary Biology
Science
description Understanding how different taxa respond to global warming is essential for predicting future changes and elaborating strategies to buffer them. Tardigrades are well known for their ability to survive environmental stressors, such as drying and freezing, by undergoing cryptobiosis and rapidly recovering their metabolic function after stressors cease. Determining the extent to which animals that undergo cryptobiosis are affected by environmental warming will help to understand the real magnitude climate change will have on these organisms. Here, we report on the responses of tardigrades within a five‐year‐long, field‐based artificial warming experiment, which consisted of 12 open‐top chambers heated to simulate the projected effects of global warming (ranging from 0 to 5.5°C above ambient temperature) in a temperate deciduous forest of North Carolina (USA). To elucidate the effects of warming on the tardigrade community inhabiting the soil litter, three community diversity indices (abundance, species richness, and Shannon diversity) and the abundance of the three most abundant species (Diphascon pingue, Adropion scoticum, and Mesobiotus sp.) were determined. Their relationships with air temperature, soil moisture, and the interaction between air temperature and soil moisture were tested using Bayesian generalized linear mixed models. Despite observed negative effects of warming on other ground invertebrates in previous studies at this site, long‐term warming did not affect the abundance, richness, or diversity of tardigrades in this experiment. These results are in line with previous experimental studies, indicating that tardigrades may not be directly affected by ongoing global warming, possibly due to their thermotolerance and cryptobiotic abilities to avoid negative effects of stressful temperatures, and the buffering effect on temperature of the soil litter substrate.Tardigrades are well known for their ability to survive harsh environmental conditions; however, it is not known if they have the potential to ...
format Article in Journal/Newspaper
author Vecchi, Matteo
Kossi Adakpo, Laurent
Dunn, Robert R.
Nichols, Lauren M.
Penick, Clint A.
Sanders, Nathan J.
Rebecchi, Lorena
Guidetti, Roberto
author_facet Vecchi, Matteo
Kossi Adakpo, Laurent
Dunn, Robert R.
Nichols, Lauren M.
Penick, Clint A.
Sanders, Nathan J.
Rebecchi, Lorena
Guidetti, Roberto
author_sort Vecchi, Matteo
title The toughest animals of the Earth versus global warming: Effects of long‐term experimental warming on tardigrade community structure of a temperate deciduous forest
title_short The toughest animals of the Earth versus global warming: Effects of long‐term experimental warming on tardigrade community structure of a temperate deciduous forest
title_full The toughest animals of the Earth versus global warming: Effects of long‐term experimental warming on tardigrade community structure of a temperate deciduous forest
title_fullStr The toughest animals of the Earth versus global warming: Effects of long‐term experimental warming on tardigrade community structure of a temperate deciduous forest
title_full_unstemmed The toughest animals of the Earth versus global warming: Effects of long‐term experimental warming on tardigrade community structure of a temperate deciduous forest
title_sort toughest animals of the earth versus global warming: effects of long‐term experimental warming on tardigrade community structure of a temperate deciduous forest
publisher Academic Publishers
publishDate 2021
url https://hdl.handle.net/2027.42/168469
https://doi.org/10.1002/ece3.7816
long_lat ENVELOPE(-54.431,-54.431,49.600,49.600)
geographic Water Bears
geographic_facet Water Bears
genre Antarctic Science
Tardigrade
genre_facet Antarctic Science
Tardigrade
op_relation Vecchi, Matteo; Kossi Adakpo, Laurent; Dunn, Robert R.; Nichols, Lauren M.; Penick, Clint A.; Sanders, Nathan J.; Rebecchi, Lorena; Guidetti, Roberto (2021). "The toughest animals of the Earth versus global warming: Effects of long‐term experimental warming on tardigrade community structure of a temperate deciduous forest." Ecology and Evolution (14): 9856-9863.
2045-7758
https://hdl.handle.net/2027.42/168469
doi:10.1002/ece3.7816
Ecology and Evolution
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Hohberg, K. ( 2006 ). Tardigrade species composition in young soils and some aspects on life history of Macrobiotus richtersi J. Murray, 1911. Pedobiologia, 50, 267 – 274. https://doi.org/10.1016/j.pedobi.2006.02.004
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Leetham, J. W., McNary, T. J., Dodd, J. L., & Lauenroth, W. K. ( 1982 ). Response of soil nematodes, rotifers and tardigrades to three levels of season‐long sulfur dioxide exposures. Water, Air, and Soil Pollution, 17 ( 4 ), 343 – 356. https://doi.org/10.1007/BF00460102
Li, X., & Wang, L. ( 2005 ). Effect of thermal acclimation on preferred temperature, avoidance temperature and lethal thermal maximum of Macrobiotus harmsworthi Murray (Tardigrada, Macrobiotidae). Journal of Thermal Biology, 30 ( 6 ), 443 – 448. https://doi.org/10.1016/j.jtherbio.2005.05.003
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Stevnbak, K., Maraldo, K., Georgieva, S., Bjørnlund, L., Beier, C., Schmidt, I. K., & Christensen, S. ( 2012 ). Suppression of soil decomposers and promotion of long‐lived, root herbivorous nematodes by climate change. European Journal of Soil Biology, 52, 1 – 7. https://doi.org/10.1016/j.ejsobi.2012.04.001
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spelling ftumdeepblue:oai:deepblue.lib.umich.edu:2027.42/168469 2023-08-20T04:02:37+02:00 The toughest animals of the Earth versus global warming: Effects of long‐term experimental warming on tardigrade community structure of a temperate deciduous forest Vecchi, Matteo Kossi Adakpo, Laurent Dunn, Robert R. Nichols, Lauren M. Penick, Clint A. Sanders, Nathan J. Rebecchi, Lorena Guidetti, Roberto 2021-07 application/pdf https://hdl.handle.net/2027.42/168469 https://doi.org/10.1002/ece3.7816 unknown Academic Publishers Wiley Periodicals, Inc. Vecchi, Matteo; Kossi Adakpo, Laurent; Dunn, Robert R.; Nichols, Lauren M.; Penick, Clint A.; Sanders, Nathan J.; Rebecchi, Lorena; Guidetti, Roberto (2021). "The toughest animals of the Earth versus global warming: Effects of long‐term experimental warming on tardigrade community structure of a temperate deciduous forest." Ecology and Evolution (14): 9856-9863. 2045-7758 https://hdl.handle.net/2027.42/168469 doi:10.1002/ece3.7816 Ecology and Evolution Pelini, S. L., Diamond, S. E., Nichols, L. M., Stuble, K. L., Ellison, A. M., Sanders, N. J., Dunn, R. R., & Gotelli, N. J. ( 2014 ). Geographic differences in effects of experimental warming on ant species diversity and community composition. Ecosphere, 5 ( 10 ), 1 – 12. https://doi.org/10.1890/ES14‐00143.1 Hiltpold, I., Johnson, S. N., Bayon, R. C. L., & Nielsen, U. N. ( 2017 ). Climate change in the underworld: Impacts for soil‐dwelling invertebrates. In S. N. Johnson & T. H. Jones (Eds.), Global climate change and terrestrial invertebrates (pp. 201 – 228 ). John Wiley & Sons Ltd. Hohberg, K. ( 2006 ). Tardigrade species composition in young soils and some aspects on life history of Macrobiotus richtersi J. Murray, 1911. Pedobiologia, 50, 267 – 274. https://doi.org/10.1016/j.pedobi.2006.02.004 IPCC ( 2013 ). Climate change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. IPCC. Knox, M. A., Andriuzzi, W. S., Buelow, H. N., Takacs‐Vesbach, C., Adams, B. J., & Wall, D. H. ( 2017 ). Decoupled responses of soil bacteria and their invertebrate consumer to warming, but not freeze–thaw cycles, in the Antarctic Dry Valleys. Ecology Letters, 20 ( 10 ), 1242 – 1249. https://doi.org/10.1111/ele.12819 Leetham, J. W., McNary, T. J., Dodd, J. L., & Lauenroth, W. K. ( 1982 ). Response of soil nematodes, rotifers and tardigrades to three levels of season‐long sulfur dioxide exposures. Water, Air, and Soil Pollution, 17 ( 4 ), 343 – 356. https://doi.org/10.1007/BF00460102 Li, X., & Wang, L. ( 2005 ). Effect of thermal acclimation on preferred temperature, avoidance temperature and lethal thermal maximum of Macrobiotus harmsworthi Murray (Tardigrada, Macrobiotidae). Journal of Thermal Biology, 30 ( 6 ), 443 – 448. https://doi.org/10.1016/j.jtherbio.2005.05.003 Maclean, I. M., Suggitt, A. J., Wilson, R. J., Duffy, J. P., & Bennie, J. J. ( 2017 ). Fine‐scale climate change: modelling spatial variation in biologically meaningful rates of warming. Global Change Biology, 23 ( 1 ), 256 – 268. Makowski, D., Ben‐Shachar, M. S., Chen, S. H., & Lüdecke, D. ( 2019 ). Indices of effect existence and significance in the Bayesian framework. Frontiers in Psychology, 10, 2767. https://doi.org/10.3389/fpsyg.2019.02767 Meyer, H. A. ( 2006 ). Small‐scale spatial distribution variability in terrestrial tardigrade populations. Hydrobiologia, 558 ( 1 ), 133 – 139. https://doi.org/10.1007/s10750‐005‐1412‐x Neves, R. C., Hvidepil, L. K., Sørensen‐Hygum, T. L., Stuart, R. M., & Møbjerg, N. ( 2020 ). Thermotolerance experiments on active and desiccated states of Ramazzottius varieornatus emphasize that tardigrades are sensitive to high temperatures. Scientific Reports, 10 ( 1 ), 1 – 12. https://doi.org/10.1038/s41598‐019‐56965‐z Newsham, K. K., Hall, R. J., & Maslen, N. R. ( 2020 ). Experimental warming of bryophytes increases the population density of the nematode Plectus belgicae in maritime Antarctica. Antarctic Science, 33, 1 – 9. Oksanen, J., Guillaume, F. B., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P., Henry, M. H., Eduard, S. S., & Wagner, H. ( 2018 ). vegan: Community Ecology Package. R package version 2.5‐3. https://CRAN.R‐project.org/package=vegan Pelini, S. L., Bowles, F. P., Ellison, A. M., Gotelli, N. J., Sanders, N. J., & Dunn, R. R. ( 2011 ). Heating up the forest: Open‐top chamber warming manipulation of arthropod communities at Harvard and Duke Forests. Methods in Ecology and Evolution, 2 ( 5 ), 534 – 540. https://doi.org/10.1111/j.2041‐210X.2011.00100.x Penick, C. A., Diamond, S. E., Sanders, N. J., & Dunn, R. R. ( 2017 ). Beyond thermal limits: Comprehensive metrics of performance identify key axes of thermal adaptation in ants. Functional Ecology, 31 ( 5 ), 1091 – 1100. https://doi.org/10.1111/1365‐2435.12818 Prather, H. M., Casanova‐Katny, A., Clements, A. F., Chmielewski, M. W., Balkan, M. A., Shortlidge, E. E., Rosenstiel, T. N., & Eppley, S. M. ( 2019 ). Species‐specific effects of passive warming in an Antarctic moss system. Royal Society Open Science, 6 ( 11 ), 190744. https://doi.org/10.1098/rsos.190744 Ramazzotti, G., & Maucci, W. ( 1983 ). Il Phylum Tardigrada. Terza edizione riveduta e corretta. Memorie dell´Istituto Italiano di Idrobiologia Dott. Marco Marchi, 41, 1 – 1012. Rebecchi, L., Altiero, T., & Guidetti, R. ( 2007 ). Anhydrobiosis: The extreme limit of desiccation tolerance. ISJ‐Invertebrate Survival Journal, 4, 65 – 81. Rebecchi, L., Boschini, D., Cesari, M., Lencioni, V., Bertolani, R., & Guidetti, R. ( 2009 ). Stress response of a boreo‐alpine species of tardigrade, Borealibius zetlandicus (Eutardigrada, Hypsibiidae). Journal of Experimental Biology, 212, 4033 – 4039. https://doi.org/10.1242/jeb.033266 Rebecchi, L., Cesari, M., Altiero, T., Frigieri, A., & Guidetti, R. ( 2009 ). Survival and DNA degradation in anhydrobiotic tardigrades. Journal of Experimental Biology, 212 ( 24 ), 4033 – 4039. https://doi.org/10.1242/jeb.033266 Simmons, B. L., Wall, D. H., Adams, B. J., Ayres, E., Barrett, J. E., & Virginia, R. A. ( 2009 ). Long‐term experimental warming reduces soil nematode populations in the McMurdo Dry Valleys. Antarctica. Soil Biology and Biochemistry, 41 ( 10 ), 2052 – 2060. https://doi.org/10.1016/j.soilbio.2009.07.009 Sohlenius, B., & Boström, S. ( 1999a ). Effects of climate change on soil factors and metazoan microfauna (nematodes, tardigrades and rotifers) in a Swedish tundra soil–a soil transplantation experiment. Applied Soil Ecology, 12 ( 2 ), 113 – 128. https://doi.org/10.1016/S0929‐1393(98)00168‐1 Sohlenius, B., & Bostrom, S. ( 1999b ). Effects of global warming on nematode diversity in a Swedish tundra soil‐a soil transplantation experiment. Nematology, 1 ( 7 ), 695 – 709. https://doi.org/10.1163/156854199508720 Sohlenius, B., Boström, S., & Jönsson, K. I. ( 2004 ). Occurrence of nematodes, tardigrades and rotifers on ice‐free areas in East Antarctica. Pedobiologia, 48 ( 4 ), 395 – 408. https://doi.org/10.1016/j.pedobi.2004.06.001 Stevnbak, K., Maraldo, K., Georgieva, S., Bjørnlund, L., Beier, C., Schmidt, I. K., & Christensen, S. ( 2012 ). Suppression of soil decomposers and promotion of long‐lived, root herbivorous nematodes by climate change. European Journal of Soil Biology, 52, 1 – 7. https://doi.org/10.1016/j.ejsobi.2012.04.001 Su, Y. S., & Yajima, M. ( 2012 ). Package ‘R2jags’. A Package for Running jags from R. Thakur, M. P., Reich, P. B., Fisichelli, N. A., Stefanski, A., Cesarz, S., Dobies, T., Rich, R. L., Hobbie, S. E., & Eisenhauer, N. ( 2014 ). Nematode community shifts in response to experimental warming and canopy conditions are associated with plant community changes in the temperate‐boreal forest ecotone. Oecologia, 175, 713 – 723. https://doi.org/10.1007/s00442‐014‐2927‐5 Tilbert, S., de Castro, F. J., Tavares, G., & Júnior, M. N. ( 2019 ). Spatial variation of meiofaunal tardigrades in a small tropical estuary (~ 6° S; Brazil). Marine and Freshwater Research, 70 ( 8 ), 1094 – 1104. https://doi.org/10.1071/MF18222 Yan, X., Wang, K., Song, L., Wang, X., & Wu, D. ( 2017 ). Daytime warming has stronger negative effects on soil nematodes than night‐time warming. Scientific Reports, 7, 44888. Andriuzzi, W. S., Adams, B. J., Barrett, J. E., Virginia, R. A., & Wall, D. H. ( 2018 ). Observed trends of soil fauna in the Antarctic Dry Valleys: Early signs of shifts predicted under climate change. 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( 2018 ). Will the Antarctic tardigrade Acutuncus antarcticus be able to withstand environmental stresses related to global climate change? Journal of Experimental Biology, 221 ( 4 ), jeb160622. Guidetti, R., Altiero, T., & Rebecchi, L. ( 2011 ). On dormancy strategies in tardigrades. Journal of Insects Physiology, 57 ( 5 ), 567 – 576. https://doi.org/10.1016/j.jinsphys.2011.03.003 IndexNoFollow Tardigrades climate change experimental global warming water bears Ecology and Evolutionary Biology Science Article 2021 ftumdeepblue https://doi.org/10.1002/ece3.781610.1016/j.pedobi.2006.02.00410.1007/s10750‐005‐1412‐x 2023-07-31T21:21:29Z Understanding how different taxa respond to global warming is essential for predicting future changes and elaborating strategies to buffer them. Tardigrades are well known for their ability to survive environmental stressors, such as drying and freezing, by undergoing cryptobiosis and rapidly recovering their metabolic function after stressors cease. Determining the extent to which animals that undergo cryptobiosis are affected by environmental warming will help to understand the real magnitude climate change will have on these organisms. Here, we report on the responses of tardigrades within a five‐year‐long, field‐based artificial warming experiment, which consisted of 12 open‐top chambers heated to simulate the projected effects of global warming (ranging from 0 to 5.5°C above ambient temperature) in a temperate deciduous forest of North Carolina (USA). To elucidate the effects of warming on the tardigrade community inhabiting the soil litter, three community diversity indices (abundance, species richness, and Shannon diversity) and the abundance of the three most abundant species (Diphascon pingue, Adropion scoticum, and Mesobiotus sp.) were determined. Their relationships with air temperature, soil moisture, and the interaction between air temperature and soil moisture were tested using Bayesian generalized linear mixed models. Despite observed negative effects of warming on other ground invertebrates in previous studies at this site, long‐term warming did not affect the abundance, richness, or diversity of tardigrades in this experiment. These results are in line with previous experimental studies, indicating that tardigrades may not be directly affected by ongoing global warming, possibly due to their thermotolerance and cryptobiotic abilities to avoid negative effects of stressful temperatures, and the buffering effect on temperature of the soil litter substrate.Tardigrades are well known for their ability to survive harsh environmental conditions; however, it is not known if they have the potential to ... Article in Journal/Newspaper Antarctic Science Tardigrade University of Michigan: Deep Blue Water Bears ENVELOPE(-54.431,-54.431,49.600,49.600) Ecology and Evolution 11 14 9856 9863

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