Abstract
Warming of the climate system is unequivocal, that is, stronger warming during night-time than during daytime. Here we focus on how soil nematodes respond to the current asymmetric warming. A field infrared heating experiment was performed in the western of the Songnen Plain, Northeast China. Three warming modes, i.e. daytime warming, night-time warming and diurnal warming, were taken to perform the asymmetric warming condition. Our results showed that the daytime and diurnal warming treatment significantly decreased soil nematodes density, and night-time warming treatment marginally affected the density. The response of bacterivorous nematode and fungivorous nematode to experimental warming showed the same trend with the total density. Redundancy analysis revealed an opposite effect of soil moisture and soil temperature, and the most important of soil moisture and temperature in night-time among the measured environment factors, affecting soil nematode community. Our findings suggested that daily minimum temperature and warming induced drying are most important factors affecting soil nematode community under the current global asymmetric warming.
Similar content being viewed by others
Introduction
Warming of the global land surface, due to the rapid increasing of greenhouse gases, is an indisputable fact. Temperature increased by 0.74 °C over the last century has been documented, and the temperature further increased at a rate of 1–3 °C by 2100 was predicted1. A faster and higher warming during the night than the day, i.e. asymmetric warming, was recognized by long-term meteorological observations and recent climate change scenarios predictions1,2,3. This asymmetric warming is expected to affect the ecological processes of aboveground ecosystem, e.g. plants and their insect herbivores and terrestrial ecosystems carbon budgets4,5. Here raise the question how asymmetric warming will affect the structure and function of underground ecosystems. However, few studies have to date been carried out to examine the influence of the observed asymmetric warming on belowground ecosystems and much remains unknown.
Terrestrial nematodes are an important component of soil fauna and key agents of underground ecosystem’s ecological processes, especially the decomposition of soil organic matter6,7. Furthermore, nematodes are sensitive to environmental disturbances and are suitable indicators of environmental stress6,8,9. It’s very likely that any alterations of nematode communities induced by warming may have a considerable influence on soil ecosystem function, especially though the changes of soil food webs10. Knowledge of the warming controls on soil nematode community is thus needed for improving our understanding soil ecosystem responses to climate change and how to manage the ecosystem sustainability.
Temperature has been evidenced as an important environmental factor affecting nematode community11,12,13,14. However, contradictory responses of soil nematodes to temperature changes in field studies were published. It was proposed that with soil temperature increased by 1 °C could have only small effects on soil nematodes13. The same marginally effect of warming on soil nematode density were reported in recent publications too10,15,16. In addition, negative effect11 or positive effect14,17 of warming on nematode density were reported also. Soil nematodes could be impacted not only directly by warming, but also indirectly via changed soil micro-environment (e.g. drying) or plant functional groups caused by warming15,18. Bakonyi et al.10 ascribed these contradictory results to the different experimental circumstances, nematode species composition, soil type, soil moisture, and so on. Although the contradictory results of different publications, all of them indicated the species specific of nematode genera to warming. Most of these experiments have been conducted under symmetric (diurnal constant) warming. However, responses of soil nematodes to the observed asymmetric warming have been inadequately studied.
In the present study, we examine the effect of asymmetric warming (i.e. daytime warming, night-time warming and diurnal warming) on soil nematodes in field, using infrared heaters to simulate climate warming. We hypothesized that soil nematode would response differently to asymmetric warming and drying caused by warming could be an important factor affecting soil nematode community as the semiarid condition of the study site.
Results
Soil temperature and moisture
Warming significantly increased soil temperature (p < 0.05) and decreased soil moisture (p < 0.05) (Table 1, Supplementary Figs 1 and 2). The maximum temperature increase and the maximum moisture decrease were observed in diurnal warming treatment (24 hW), with an average increase of 1.3 °C, 1.9 °C and 1.5 °C for average daytime temperature (Tday), average night-time temperature (Tnight) and average diurnal temperature (Tdiurnal), respectively, and a decrease of 14.8% of soil moisture (Table 1). Daytime warming (DW) and night-time warming (NW) significantly increased 0.6 °C and 0.6 °C of the Tday and Tnight, respectively. DW and NW significantly decreased soil moisture by 9.0% and 2.2%.
Soil nematodes
Nematodes were dominated by bacterial feeders and fungal feeders, accounting for 89.4% of the total. Acrobeloides was the most abundant nematode, which accounted for 32–47% of the animal in all plots, regardless of treatment, and Paraphelenchus (15–26%) and Acrobeles (11–21%) followed in order.
Nematode populations were significantly affected by asymmetric warming (p < 0.05, Fig. 1 and Supplementary Table 2). Total abundance was significantly decreased in DW and 24 hW, while not significant in NW (Fig. 1). Significant differences were found of nematode functional groups and species to asymmetric warming (Fig. 1 and Supplementary Table 2). Bacterivores and fungivores population were significantly decreased in 24 hW, whereas they were not influenced in NW. DW significantly decreased the density of bacterial feeders, whereas not significant for fungal feeders. All of the three warming treatments significantly decreased the density of plant feeders. Because of low abundance and high variation of omnivore-carnivores, effect of warming on this group was not significant (Fig. 1).
Redundancy analysis (RDA) diagram indicated an opposite effect of soil temperature and soil moisture on soil nematode community, and the measured soil temperature and moisture together explained 16.9% of the variance in nematode community (p < 0.05, Fig. 2). Soil moisture was the most important among the measured environmental variables, which alone explained 8.1% of the variation. In addition, Tnight also explained a significant portion of the variation in nematode community (7.8%, p < 0.05, Fig. 2).
Discussion
We simulated climate asymmetric warming by experimentally heating in day and/or night. Warming treatments changed soil microclimate (soil temperature and moisture). In agreement with our hypothesis, results showed different effects of daytime warming and night-time warming on soil nematodes. We highlight that warming induced drying and daily minimum temperature are most important factors affecting soil nematodes under the current asymmetric warming in Songnen grassland.
As far as we known, there were only two studies studied the effect of night-time warming on soil nematodes, in which showed the same results with the present study. These authors suggested that, the ebb and flow of the different nematode genera maintained the stable population size under NW10,16. It was evidenced that compared to control, the abundance of Acrobeles, Aphelenchoides and Rotylenchus decreased, whereas the abundance of Acrobeloides and Paraphelenchus increased under NW (Supplementary Table 1). Comparable to the results by Simmons et al.11 who reported that a long-term diurnal warming by OTC in Antarctica reduced soil nematode populations, and these authors suggested both the direct and indirect effects by warming induced altering species-specific habitat suitability for soil biota. While, more publications reported positive effects of warming on nematode density14,17. Warming could induce a greater reproduction rate and result in a higher population density14. Additionally, soil warming enhanced the microbial biomass19, which may in turn benefit nematode population, especially microbial-feeding nematodes. All the warming treatments significantly increased soil temperature, regardless of Tday, Tnight or Tdiurnal (Table 1). However, soil warming did not affect (NW), even decreased (DW and 24 hW), soil nematode populations in the present study (Fig. 1). This indicated that temperature is not the determination factor for soil nematode community in the study area.
It is well known that soil temperature and moisture content are among the main abiotic factors which directly or indirectly influence the activity, distribution and population dynamic of nematodes in the soil20,21,22. The increase of soil temperature coincided with a significant decrease of soil moisture (Table 1). Free-living nematodes were highly dependent on free water in soil for locomotion and biological activity, decreasing soil moisture content was expected to be a detrimental factor18,23,24. It was reported that, warming induced water shortage in soil reduced the density of nematodes in a multi-factor global change experiment in grassland18.
According to the differences in nematode responses between DW and NW, the temperature increase rates were almost same, but the soil moisture was greatly different, suggesting that warming-induced soil moisture change was the major driving factor of soil nematodes responses, not the warming. As a result, the sharp decrease of soil moisture caused by warming could be the reason of the decreasing of soil nematodes in DW and 24 hW in the present study.
In field experiments, it is seldom possible to explain and separate the responses of soil nematodes to warming and drying, because of the different responses of nematode species to changes in temperature and moisture10,22. Ordination analysis could be one solution of the issue. In the present study, results of RDA indicated the opposite effect of soil temperature and soil moisture on soil nematode community (Fig. 2). As discussed above, soil temperature positively affect soil nematodes, however, warming induced drying negatively affect soil nematodes. The results of asymmetric warming on soil nematodes possibly was the balance of these two conversely issue.
Our data showed that warming decreased the abundance of plant feeders due to significantly lower abundance of Rotylenchus, indicating the warming sensitivity of this fauna. It’s common that most nematode species were sensitive to environmental changes and the narrow temperature/moisture range often determine the distribution of a particular species25,26. The decrease of plant feeder possibly could increase the ratio between microbial feeding and plant feeding nematodes density [(FF + BF)/PF], as showed in previous publications15,16,27. The warming induced disproportionate responses of nematodes functional groups could have a substantial impact on soil food web dynamics and ecosystem functioning28,29. The significant declining of plant feeders by warming in this study also indicated that warming induced soil drying was fatal for plant feeding nematodes in semiarid-arid system.
Conclusions
The present study was a complementary research in global change biology/ecology, especially in the ecological influence of asymmetric warming. The changes of soil nematodes were due to the integrated effects of temperature and soil moisture changes caused by warming. Warming in the daytime had a stronger negative effect on soil nematodes than warming in the night-time, which was the main finding of the present study. As eigenvalues of RDA axes were not remarkably high, soil nematodes could be affected by other environmental variables, which were not included in our present study. Nevertheless, RDA indicated the significant importance of soil moisture as well as soil temperatures in the night-time on soil nematode community. This suggested, under the current global asymmetric warming and regional characteristics of global warming1, the importance of daily minimum temperature and warming induced drying in underground ecosystem.
Methods
Study site
The research site was located in the Ecological Research Station of Grassland Farming, Changling, Chinese Academy of Sciences, northeast China (44°33′N, 123°31′E, 145 m a.s.l.). The climate is temperate semi-arid continental monsoon. The annual average temperature is about 4.9 °C (with an average of 23 °C in July and −15 °C in January). The frost-free period lasts 140 days per year. The annual precipitation is 300–450 mm, of which 70–80% occurred between July and September, with the annual evaporation of 1500–2000 mm.
Experimental design
The field experiment included three warming treatments: daytime warming (DW, 06:00–18:00), night-time warming (NW, 18:00–06:00) and diurnal warming (24 hW), and one ambient control (C). A randomized block design with 6 replicates was used. A total of 24 plots (3 m × 4 m in size for each) were arranged in a 4 × 6 matrix. The distance between the adjacent plots was 3 m. Plots were warmed by MSR-2420 infrared radiators (2 KW, Kalglo Electronics, Bethlehem, Pennsylvania, USA), which was suspended 2.25 m above the ground. For control plots, ‘dummy’ heaters with the same shape, size and installation as the heaters in the warming plots were set. Warming started on 1 June 2012 and ended on 31 August 2012. Astragalus adsurgens Pall. was planted in the experimental plots. Sensors probes of temperature and humility were buried 5 cm below the soil surface in the centre of 3 random selected plots for each treatment. Soil temperature and humidity were auto-recorded per hour.
Soil sampling and nematode analysis
Nematodes samples were sampled on 31August, 2012. A mixed soil sample of three soil cores (diameter: 5 cm, depth: 5 cm) was collected per plot. 100 g fresh subsamples were used to extract nematodes. A modified sucrose centrifugal flotation method was used for nematode extraction immediately after sampling30. The extracted nematodes were preserved in 4% formaldehyde. One tenth and an average of 150 nematode individuals of each sample was identified and counted under microscope Nikon 80i. Nematodes were identified to the genus level according to the keys/procedures of Bongers31. The functional groups of nematodes (i.e. bacterial feeders, fungal feeders, plant feeders and omnivore-carnivores) were divided according to Yeates et al.32. Nematode density was expressed as individual numbers 100 g−1 dry soil.
Statistical analysis
Soil average daytime temperature (Tday, 06:00–18:00), soil average night-time temperature (Tnight, 18:00–06:00) and soil average diurnal temperature (Tdiurnal) and soil moisture were calculated separately. Densities of total nematodes and four functional groups were calculated (individuals 100 g−1 dry soil).
Repeated measure ANOVA was used to test the effect of asymmetric warming treatments on soil temperature (Tday, Tnight and Tdiurnal) and soil moisture. ANOVA was applied to test the effect of warming on nematodes (total abundance and density of four functional groups). Post-hoc comparisons using Turkey’s LSD test were followed. The data for nematode density were log (n + 1) transformed before analysis. Redundancy analysis (RDA) and an ordination bi-plot were used to visualize the correlation between nematodes and soil temperature and moisture. The significance of the environmental parameters was analyzed by Monte Carlo permutation tests (499 permutations). All analysis were performed with R3.1.2 using the vegan package33, at a significant level α = 0.05.
Additional Information
How to cite this article: Yan, X. et al. Daytime warming has stronger negative effects on soil nematodes than night-time warming. Sci. Rep. 7, 44888; doi: 10.1038/srep44888 (2017).
Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Change history
29 August 2017
A correction has been published and is appended to both the HTML and PDF versions of this paper. The error has been fixed in the paper.
References
IPCC. Climate Change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. (Cambridge University press, 2013).
Vose, R. S., Easterling, D. R. & Gleason, B. Maximum and minimum temperature trends for the globe: An update through 2004. Geophys Res Lett 32, L23822, doi: 10.1029/2005GL024379 (2005).
Zhou, L., Dickinson, R. E., Dai, A. & Dirmeyer, P. Detection and attribution of anthropogenic forcing to diurnal temperature range changes from 1950 to 1999: comparing multi-model simulations with observations. Clim Dynam 35, 1289–1307, doi: 10.1007/s00382-009-0644-2 (2010).
Hooper, D. U. et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486, 105–108, doi: 10.1038/nature11118 (2012).
Peng, S. et al. Asymmetric effects of daytime and night-time warming on Northern Hemisphere vegetation. Nature 501, 88–92, doi: 10.1038/nature12434 (2013).
Bongers, T. & Bongers, M. Functional diversity of nematodes. Appl Soil Ecol 10, 239–251, doi: 10.1016/S0929-1393(98)00123-1 (1998).
Yeates, G. W. & Coleman, D. W. Role of nematodes in decomposition. 55–80 (University of Texas Press, 1982).
Stone, D., Ritz, K., Griffiths, B. G., Orgiazzi, A. & Creamer, R. E. Selection of biological indicators appropriate for European soil monitoring. Appl Soil Ecol 97, 12–22, doi: 10.1016/j.apsoil.2015.08.005 (2016).
Bongers, T. & Ferris, H. Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol Evol 14, 224–228, doi: 10.1016/S0169-5347(98)01583-3 (1999).
Bakonyi, G. et al. Soil nematode community structure as affected by temperature and moisture in a temperate semiarid shrubland. Appl Soil Ecol 37, 31–40, doi: 10.1016/j.apsoil.2007.03.008 (2007).
Simmons, B. L. et al. Long-term experimental warming reduces soil nematode populations in the McMurdo Dry Valleys, Antarctica. Soil Biol Biochem 41, 2052–2060, doi: 10.1016/j.soilbio.2009.07.009 (2009).
Li, Q. et al. Nitrogen addition and warming independently influence the belowground micro-food web in a temperate steppe. Plos One 8, e60441, doi: 10.1371/journal.pone.0060441 (2013).
Dong, Z., Hou, R., Chen, Q., Ouyang, Z. & Ge, F. Response of soil nematodes to elevated temperature in conventional and no-tillage cropland systems. Plant Soil 373, 907–918, doi: 10.1007/s11104-013-1846-2 (2013).
Ruess, L., Michelsen, A., Schmidt, I. K. & Jonasson, S. Simulated climate change affecting microorganisms, nematode density and biodiversity in subarctic soils. Plant Soil 212, 63–73, doi: 10.1023/A:1004567816355 (1999).
Thakur, M. P. et al. 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, doi: 10.1007/s00442-014-2927-5 (2014).
Song, Z. et al. Impacts of night-time warming on the soil nematode community in a winter wheat field of Yangtze Delta Plain, China. J Integr Agr 13, 1477–1485, doi: 10.1016/s2095-3119(14)60807-8 (2014).
Harte, J., Rawa, A. & Price, V. Effects of manipulated soil microclimate on mesofaunal biomass and diversity. Soil Biol Biochem 28, 313–322, doi: 10.1016/0038-0717(95)00139-5 (1996).
Kardol, P., Cregger, M., Campany, C. E. & Classen, A. T. Soil ecosystem functioning under climate change: plant species and community effects. Ecology 91, 767–781, doi: 10.1890/09-0135.1 (2010).
Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173, doi: 10.1038/nature04514 (2006).
Anderson, R. V. & Coleman, D. C. Nematode temperature responses: a niche dimension in populations of bacterial-feeding nematodes. J Nematol 14, 69–76 (1982).
Bakonyi, G. & Nagy, P. Temperature- and moisture-induced changes in the structure of the nematode fauna of a semiarid grassland - patterns and mechanisms. Global Change Biol 6, 697–707, doi: 10.1046/j.1365-2486.2000.00354.x (2000).
Yeates, G. W., Dando, J. L. & Shepherd, T. G. Pressure plate studies to determine how moisture affects access of bacterial‐feeding nematodes to food in soil. Eur J Soil Sci 53, 355–365, doi: 10.1046/j.1365-2389.2002.00466.x (2002).
Briones, M. J. I., Ineson, P. & Piearce, T. G. Effects of climate change on soil fauna responses of enchytraeids, Diptera larvae and tardigrades in a transplant experiment. Appl Soil Ecol 6, 117–134, doi: 10.1016/S0929-1393(97)00004-8 (1997).
Lindberg, N., Engtsson, J. B. & Persson, T. Effects of experimental irrigation and drought on the composition and diversity of soil fauna in a coniferous stand. J Appl Ecol 39, 924–936, doi: 10.1046/j.1365-2664.2002.00769.x (2002).
Ferris, H., Lau, S. & Venette, R. Population energetics of bacterial-feeding nematodes: Respiration and metabolic rates based on CO2 production. Soil Biol Biochem 27, 319–330, doi: 10.1016/0038-0717(94)00186-5 (1995).
Nicholas, W. L. The biology of free-living nematodes. (Oxford University Press, 1984).
Eisenhauer, N., Migunova, V. D., Ackermann, M., Ruess, L. & Scheu, S. Changes in Plant Species Richness Induce Functional Shifts in Soil Nematode Communities in Experimental Grassland. Plos One 6, e24087, doi: 10.1371/journal.pone.0024087 (2011).
Wall, D. H. Global change tipping points: above- and below-ground biotic interactions in a low diversity ecosystem. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 362, 2291–2306, doi: 10.1098/rstb.2006.1950 (2007).
Barrett, J. E. et al. Variation in biogeochemistry and soil biodiversity across spatial scales in a Polar Desert Ecosystem. Ecology 85, 3105–3118, doi: 10.1890/03-0213 (2004).
Freckman, D. & Virginia, R. Extraction of nematodes from Dry Valley Antarctic soils. Polar Biology 13, 483–487, doi: 10.1007/BF00233139 (1993).
Bongers, A. M. T. De Nematoden Van Nederland. Natuurhistorische Bibliotheek van de KNNV, nr. 46, Pirola, Schoorl (1988).
Yeates, G. W., Bongers, T., De Goede, R. G., Freckman, D. W. & Georgieva, S. S. Feeding habits in soil nematode families and genera-an outline for soil ecologists. J Nematol 25, 315–331 (1993).
Team, R. C. R: a language and environment for statistical computing. R Foundation for Statistical Computing (2015).
Acknowledgements
We cordially thank Bing Zhang and Zhen Ni (College of Earth Science Jilin University) and Yingxin Huang (Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences) for their help with the fieldwork. Financial assistance was provided by the National Basic Research Program of China (Nos 2016YFA0602303-1, 2010CB951304), the National Natural Sciences Foundation of China (Nos 41430857, 41201245), and Knowledge Innovation Programs of Chinese Academy of Sciences (KZCX2-YW-BR-16).
Author information
Authors and Affiliations
Contributions
L.S., X.Y. and K.W. wrote the main manuscript text, X.Y. and K.W. prepared figures and tables, L.S. and D.W. designed the experiment and L.S., X.Y., K.W. and X.W. performed the experiment. All authors reviewed the manuscript.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Rights and permissions
This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
About this article
Cite this article
Yan, X., Wang, K., Song, L. et al. Daytime warming has stronger negative effects on soil nematodes than night-time warming. Sci Rep 7, 44888 (2017). https://doi.org/10.1038/srep44888
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/srep44888
This article is cited by
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.