Abstract
Aims
An unresolved question in plant ecology is whether diversity of the aboveground and belowground compartments of a plant community is similar at different neighbourhood scales. We investigated how the similarity between both compartments varies with the aboveground sampling grain and if significant discrepancies exist between aboveground and belowground plant diversity at the maximum similarity scale.
Methods
We fully mapped the aboveground perennial plant community of a 64 m2 plot in a Mediterranean shrubland and analysed this compartment by assessing diversity in 5 to 50 cm radii circles centred in soil cores. We sampled 2.5 cm radius root cores at two different depths and identified plant species by using DNA metabarcoding to characterise the belowground compartment. We quantified differences in species richness, composition and species’ spatial distribution above- and belowground.
Results
The differences between aboveground and belowground communities were affected by the size of the aboveground sampling grain and were minimised when considering a circle of 20 cm radius in the aboveground. We found a significant dissimilarity in richness and composition between the two compartments, with larger differences when considering the deeper soil layer only.
Conclusions
Our results showed that the spatial grain selected to sample a plant community aboveground and belowground is critical to characterise them in a comparable manner. Although their composition is related, species distribution patterns strongly differ, suggesting the simultaneous action of different assembly mechanisms. Our results call for caution when studying community assembly considering only the standing vegetation, since total plant diversity can be underappreciated.
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Abbreviations
- ΔR :
-
Richness dissimilarity.
- J :
-
Jaccard dissimilarity index.
- AR:
-
Aboveground Richness.
- AR5 :
-
Aboveground Richness at 5 cm radius grain.
- AR20 :
-
Aboveground Richness at 20 cm radius grain (similarity peak).
- BR:
-
Belowground Richness.
- BR0 − 30 :
-
Belowground Richness at 0–30 cm of depth.
- BR0 − 10 :
-
Belowground Richness at 0–10 cm of depth.
- BR10 − 30 :
-
Belowground Richness at 10–30 cm of depth.
- OTU:
-
Operational Taxonomic Unit.
References
Adetunji AT, Lewu FB, Mulidzi R, Ncube B (2017) The biological activities of β-glucosidase, phosphatase and urease as soil quality indicators: A review. J Soil Sci Plant Nutr 17:794–807
Agresti A (1990) Categorical data analysis. Wiley, New York
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Anderson JM, Ingram JSI (1993) Tropical soil biology and fertility: a handbook of methods. J Ecol 78:547. https://doi.org/10.2307/2261129
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Bivand RS, Wong DWS (2018) Comparing implementations of global and local indicators of spatial association. Test 27:716–748. https://doi.org/10.1007/s11749-018-0599-x
Bokulich NA, Subramanian S, Faith JJ et al (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59. https://doi.org/10.1038/nmeth.2276
Bray JR (1963) Root production and the estimation of net productivity. Can J Bot 41:65–72
Cardinale BJ, Duffy JE, Gonzalez A et al (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67
Casper BB, Jackson RB (1997) Plant competition underground. Annu Rev Ecol Syst 28:545–570. https://doi.org/10.1146/annurev.ecolsys.28.1.545
Chacón-Labella J, de la Cruz M, Escudero A (2017) Evidence for a stochastic geometry of biodiversity: the effects of species abundance, richness and intraspecific clustering. J Ecol 105:382–390. https://doi.org/10.1111/1365-2745.12710
Cipriotti PA, Aguiar MR (2015) Is the balance between competition and facilitation a driver of the patch dynamics in arid vegetation mosaics? Oikos 124:139–149. https://doi.org/10.1111/oik.01758
Davidson RL (1969) Effect of root/leaf temperature differentials on root/shoot ratios in some pasture grasses and clover. Ann Bot 33:561–569. https://doi.org/10.1093/oxfordjournals.aob.a084308
Deiner K, Bik HM, Mächler E et al (2017) Environmental DNA metabarcoding: Transforming how we survey animal and plant communities. Mol Ecol 26:5872–5895. https://doi.org/10.1111/mec.14350
Deng JM, Wang GX, Morris EC et al (2006) Plant mass-density relationship along a moisture gradient in north-west China. J Ecol 94:953–958. https://doi.org/10.1111/j.1365-2745.2006.01141.x
Dormann F, McPherson CM, Araújo JBM, et al (2007) Methods to account for spatial autocorrelation in the analysis of species distributional data: A review. Ecography (Cop) 30:609–628
Eivazi F, Tabatabai MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606. https://doi.org/10.1016/0038-0717(88)90141-1
Escudero A, Palacio S, Maestre FT, Luzuriaga AL (2015) Plant life on gypsum: a review of its multiple facets. Biol Rev 90:1–18. https://doi.org/10.1111/brv.12092
Frank DA, Pontes AW, Maine EM et al (2010) Grassland root communities: species distributions and how they are linked to aboveground abundance. Ecology 91:3201–3209. https://doi.org/10.1890/09-1831.1
Hartig F (2020) DHARMa: Residual diagnostics for hierarchical (Multi-Level / Mixed) regression models. R package version 0.2.7. http://florianhartig.github.io/DHARMa/. Accessed 17 Apr 2020
Hiiesalu I, Öpik M, Metsis M et al (2012) Plant species richness belowground: Higher richness and new patterns revealed by next-generation sequencing. Mol Ecol 21:2004–2016. https://doi.org/10.1111/j.1365-294X.2011.05390.x
Hilbe JM (2014) Modeling count data. Cambridge University Press, Cambridge
Jones FA, Erickson DL, Bernal MA et al (2011) The roots of diversity: Below ground species richness and rooting distributions in a tropical forest revealed by DNA barcodes and inverse modeling. PLoS One 6. https://doi.org/10.1371/journal.pone.0024506
Kendall M (1976) Rank auto correlation methods, 4th edn. Griffin, Irvine
Kesanakurti PR, Fazekas AJ, Burgess KS et al (2011) Spatial patterns of plant diversity below-ground as revealed by DNA barcoding. Mol Ecol 20:1289–1302. https://doi.org/10.1111/j.1365-294X.2010.04989.x
Kettler TA, Doran JW, Gilbert TL (2001) Simplified method for soil particle-size determination to accompany soil-quality analyses. Soil Sci Soc Amer J 65:849–852
Kress WJ, Erickson DL, Jones FA et al (2009) Plant DNA barcodes and a community phylogeny of a tropical forest dynamics plot in Panama. Proc Natl Acad Sci U S A 106:18621–18626. https://doi.org/10.1073/pnas.0909820106
Levin RA, Wagner WL, Hoch PC et al (2003) Family-level relationships of Onagraceae based on chloroplast rbc L and ndh F data. Am J Bot 90:107–115. https://doi.org/10.3732/ajb.90.1.107
Li Z, Lamb EG, Piper CL, Siciliano SD (2017) Plant belowground diversity and species segregation by depth in a semi-arid grassland. Ecoscience 25:1–7. https://doi.org/10.1080/11956860.2017.1403242
Martens SN, Breshears DD, Meyer CW, Barnes FJ (1997) Scales of aboveground and below-ground competition in a semi-arid woodland detected from spatial pattern. J Veg Sci 8:655–664. https://doi.org/10.2307/3237370
Matesanz S, Pescador DS, Pías B et al (2019) Estimating belowground plant abundance with DNA metabarcoding. Mol Ecol Resour 19:1265–1277. https://doi.org/10.1111/1755-0998.13049
Mokany K, Raison RJ, Prokushkin AS (2006) Critical analysis of root: shoot ratios in terrestrial biomes. Glob Chang Biol 12:84–96. https://doi.org/10.1111/j.1365-2486.2005.001043.x
Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Phosphorus in action. 26:215–243. https://doi.org/10.1007/978-3-642-15271-9
Oksanen J, Blanchet FG, Friendly M, et al (2019) Vegan: community ecology package. R package version 2.5-6
Pärtel M (2014) Community ecology of absent species: Hidden and dark diversity. J Veg Sci 25:1154–1159. https://doi.org/10.1111/jvs.12169
Pärtel M, Hiiesalu I, Öpik M, Wilson SD (2012) Below-ground plant species richness: New insights from DNA-based methods. Funct Ecol 26:775–782. https://doi.org/10.1111/j.1365-2435.2012.02004.x
Price JN, Hiiesalu I, Gerhold P, Pärtel M (2012) Small-scale grassland assembly patterns differ above and below the soil surface. Ecology 93:1290–1296. https://doi.org/10.1890/11-1942.1
R Core Team (2020) R: The R project for statistical computing. https://www.r-project.org/. Accessed 17 Apr 2020
Radojević M, Bashkin VN (1999) Water analysis. In: Radojevic M, Bashkin VN (eds) Practical environmental analysis. Royal Society of Chemistry, Cambridge, pp 138–273
Rewald B, Meinen C, Trockenbrodt M et al (2012) Root taxa identification in plant mixtures - current techniques and future challenges. Plant Soil 359:165–182. https://doi.org/10.1007/s11104-012-1164-0
Schenk HJ, Jackson RB (2002a) Rooting depths, lateral root spreads and below-ground/above-ground allometries of plants in water-limited ecosystems. J Ecol 90:480–494. https://doi.org/10.1046/j.1365-2745.2002.00682.x
Schenk HJ, Jackson RB (2002) The global biogeography of roots. Ecol Monogr 72:311–328. https://doi.org/10.1890/0012-9615(2002)072[0311:TGBOR]2.0.CO;2
Schenk HJ, Callaway RM, Mahall BE (1999) Spatial root segregation: are plants territorial? Adv Ecol Res 28:145–180. https://doi.org/10.1016/S0065-2504(08)60032-X
Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307. https://doi.org/10.1016/0038-0717(69)90012-1
Träger S, Öpik M, Vasar M, Wilson SD (2019) Belowground plant parts are crucial for comprehensively estimating total plant richness in herbaceous and woody habitats. Ecology 100:1–12. https://doi.org/10.1002/ecy.2575
Walter H (1963) The water supply of desert plants. In: Rutter AJ, Whitehead FH (eds) The Water Relations of Plants. John Wiley & Sons, New York, pp 199–205
Yee TW (2010) The VGAM package for categorical data analysis. J Stat Softw 32:1–34. https://doi.org/10.18637/jss.v032.i10
Yeomans JC, Bremner JM (1988) A rapid and precise method for routine determination of organic carbon in soil. Commun Soil Sci Plant Anal 19:1467–1476. https://doi.org/10.1080/00103628809368027
Zornoza R, Mataix-Solera J, Guerrero C et al (2009) Storage effects on biochemical properties of air-dried soil samples from southeastern Spain. Arid L Res Manag 23:213–222. https://doi.org/10.1080/15324980903038727
Acknowledgements
We are grateful to Carlos Díaz (URJC) for his technical assistance during plant recollection in the field and to AllGenetics & Biology (https://www.allgenetics.eu/) for their contribution in molecular and bioinformatics analyses. We also thank the editor and two anonymous reviewers for their comments on the manuscript. Funding was provided by the Ministerio de Economía y Competitividad de España (grant ROOTS CGL2015-66809-P) and by the Comunidad de Madrid (grant REMEDINAL TE-CM, S2018/EMT-4338).
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Silvia Matesanz and Adrián Escudero conceived and designed the study. All authors conducted field and laboratory work. Angela Illuminati analysed the data with extensive input by Jesús López-Angulo and Marcelino de la Cruz. Angela Illuminati wrote the manuscript, with input from all other authors.
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Illuminati, A., López-Angulo, J., de la Cruz, M. et al. Larger aboveground neighbourhood scales maximise similarity but do not eliminate discrepancies with belowground plant diversity in a Mediterranean shrubland. Plant Soil 460, 497–509 (2021). https://doi.org/10.1007/s11104-020-04796-7
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DOI: https://doi.org/10.1007/s11104-020-04796-7