Skip to main content

Advertisement

SpringerLink
Log in

Long-term simulated nitrogen deposition alters the plant cover dynamics of a Mediterranean rosemary shrubland in Central Spain through defoliation

  • (E)merging directions on air pollution and climate change research in Mediterranean Basin ecosystems
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Nitrogen (N) deposition due to anthropogenic pollution is a major driver of the global biodiversity loss. We studied the effect of experimental N and phosphorus (P) fertilization (0, 10, 20, and 50 kg N ha−1 year−1 and 14 kg P ha−1 year−1 over the background deposition levels) on plant cover dynamics of a rosemary (Rosmarinus officinalis L.) shrubland after 8 years of nutrient addition in a semiarid Mediterranean ecosystem from Central Spain. We specifically aimed at testing whether N deposition has the potential to influence the observed expanding trend of woody vegetation into areas dominated by grassland, biological soil crusts, and bare soil. Our results show that N addition loads above 10 kg N ha−1 year−1 reverted the cover dynamics of shrubs. Under N addition conditions, N was no longer a limiting nutrient and other elements, especially P and calcium, determined the seasonal growth of young twigs. Interestingly, N fertilization did not inhibit the growth of young shoots; our estimates point to a reduced rosemary leaf lifespan that is driving individuals to death. This may be triggered by long-term accumulation of N compounds in leaves, suggesting the need to consider the old organs and tissues in long-lived perennial plants, where N toxicity effects could be more mediated by accumulation processes. Shrublands are a widely distributed ecosystem type in biodiverse Mediterranean landscapes, where shrubs play a key role as nurse plants. Therefore, the disappearance of shrublands may accelerate the biodiversity loss associated with other global change drivers, hamper the recruitment of seedlings of woody species, and, as a consequence, accelerate desertification.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alcaraz F, Peinado M, Rivas-Martínez S et al (1987) La vegetación de España. Universidad de Alcala de Henares, Secretaria General, Servicio de Publicaciones

  • Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235

    Article  Google Scholar 

  • Balaguer L, Pugnaire FI, Martínez-Ferri E, Armas C, Valladares F, Manrique E (2002) Ecophysiological significance of chlorophyll loss and reduced photochemical efficiency under extreme aridity in Stipa tenacissima L. Plant Soil 240:343–352

    Article  CAS  Google Scholar 

  • Basto S, Thompson K, Phoenix G, Sloan V, Leake J, Rees M (2015) Long-term nitrogen deposition depletes grassland seed banks. Nature. doi:10.1038/ncomms7185

    Article  Google Scholar 

  • Blanes A, Viñegla B, Merino J, Carreira AJ (2013) Nutritional status of Abies pinsapo forests along a nitrogen deposition gradient: do C/N/P stoichiometric shifts modify photosynthetic nutrient use efficiency? Oekologia 171(4):797–808

  • Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, Fenn M, Gilliam F, Nordin A, Pardo L, de Vries W (2010) Global assessment of N deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20(1):30–59

    Article  CAS  Google Scholar 

  • Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres L, Kunstler G et al (2008) Facilitation in plant communities: the past, the present and the future. J Ecol 96:18–34

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Burriel F, Hernando V (1950) El fósforo en los suelos españoles V Nuevo método para determinar el fósforo asimilable en los suelos. Anales de Edafología y Agrobiología 9:611–622

    CAS  Google Scholar 

  • Bussotti F, Ferrini F, Pollastrini M, Fini A (2014) The challenge of Mediterranean sclerophyllous vegetation under climate change: from acclimation to adaptation. Environ Exp Bot 103:80–98

    Article  Google Scholar 

  • Chapin FS III, Bloom AJ, Field CB, Waring RH (1987) Plant-responses to multiple environmental factors. Boscience 37:49–57

    Article  Google Scholar 

  • Crespo A, Barreno E (1975) Ensayo florístico y ecológico de la vegetación liquénica de los yesos del centro de España (Fulgensietalia desertori). Anal Inst Bot Cavanilles 32:873–908

    Google Scholar 

  • Cuesta B, Villar-Salvador P, Puértolas J, Rey Benayas JM, Michalet R (2010) Facilitation of Quercus ilex in Mediterranean shrubland is explained by both direct and indirect interactions mediated by herbs. J Ecol 98:687–696

    Article  Google Scholar 

  • Dentener F, Drevet J, Lamarque JF, Bey I, Eickhout B, Fiore AM, Hauglustaine D, Horowitz LW, Krol M, Kulshrestha UC, Lawrence M, Galy-Lacaux C, Rast S, Shindell D, Stevenson D, Van Noije T, Atherton C, Bell N, Bergman D, Butler T, Cofala J, Collins B, Doherty R, Ellingsen K, Galloway J, Gauss M, Montanaro V, Müller JF, Pitari G, Rodriguez J, Sanderson M, Solmon F, Strahan S, Schultz M, Sudo K, Szopa S, Wild O (2006) Nitrogen and sulfur deposition on regional and global scales: a multimodel evaluation. Glob Biogeochem Cycles. doi:10.1029/2005GB002672

    Article  Google Scholar 

  • Dias T (2012) Effects of increased nitrogen availability on the structure and functioning of a Mediterránean Basin maquis. Doctoral Thesis. Universidade de Lisboa, Faculdade de Ciências, Departamento de Biologia Vegetal. Lisboa, Portugal

  • Dias T, Clemente A, Martins-Loução MA, Sheppard L, Bobbink R, Cruz C (2014) Ammonium as a driving force of plant diversity and ecosystem functioning: observations based on 5 years’ manipulation of N dose and form in a Mediterranean ecosystem. PLoS One. doi:10.1371/journal.pone.0092517

    Article  Google Scholar 

  • Fenn ME, Baron JS, Allen EB, Rueth HM, Nydick KR, Geiser L (2003) Ecological effects of nitrogen deposition in the western United States. Bioscience 53(4):404–420

    Article  Google Scholar 

  • Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DMA, Michaels F, Porter JH, Townsend AR, Vöosmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226

    Article  CAS  Google Scholar 

  • Garbulsky MF, Filellab I, Vergerb A, Peñuelas J (2014) Photosynthetic light use efficiency from satellite sensors: from global to Mediterranean vegetation. Environ Exp Bot 103:3–11

    Article  Google Scholar 

  • Gimeno-García E, Andreu V, Rubio JL (2001) Influence of Mediterranean shrub species on soil chemical properties in typical Mediterranean environment. Commun Soil Sci Plant Anal 32:1885–1898

    Article  Google Scholar 

  • Gómez-Aparicio L, Gomez JM, Zamora R, Bottinguer JL (2005a) Canopy vs. soil effects of shrubs facilitating tree seedlings in Mediterranean montane ecosystems. J Veg Sci 16:191–198

    Article  Google Scholar 

  • Gómez-Aparicio L, Valladares F, Zamora R, Quero JL (2005b) Response of tree seedlings to the abiotic heterogeneity generated by nurse shrubs: an experimental approach at different scales. Ecography 28(6):757–768

    Article  Google Scholar 

  • Granati L, Varone L (2004) Leaf key traits of Erica arborea L., Erica multiflora L. and Rosmarinus officinalis L. co-occurring in the Mediterranean maquis. Flora 199:58–69

    Article  Google Scholar 

  • Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Article  Google Scholar 

  • Izco J (1972) Coscojares, romelares y tomillares de la Provincia de Madrid. Anal Inst Bot Cavanilles 29:69–108

  • Kanzler M, Böhm C, Freese D (2015) Impact of P fertilisation on the growth performance of black locust (Robinia pseudoacacia L.) in a lignite post-mining area in Germany. Annals of Forest Research 58:39–54

    Article  Google Scholar 

  • Kunstler G, Curt T, Bouchaud M, Lepart J (2006) Indirect facilitation and competition in tree species colonization of sub-Mediterranean grasslands. J Veg Sci 17:379–388

    Article  Google Scholar 

  • Maestre FT, Cortina J (2005) Remnant shrubs in Mediterranean semi-arid steppes: effects of shrub size, abiotic factors and species identity on understorey richness and occurrence. Acta Oecol 27:161–169

    Article  Google Scholar 

  • Maestre FT, Bowker MA, Puche MD, Hinojosa MB, Martínez I, García-Palacios P, Castillo AP, Soliveres S, Luzuriaga AL, Sánchez AM, Carreira JA, Gallardo A, Escudero A (2009) Shrub encroachment can reverse desertification in semi-arid Mediterranean grasslands. Ecol Lett 12(9):930–941

    Article  Google Scholar 

  • Matesanz S, Valladares F (2014) Ecological and evolutionary responses of Mediterranean plants to global change. Environ Exp Bot 103:53–67

    Article  Google Scholar 

  • McIntire EJB, Fajardo A (2014) Facilitation as a ubiquitous driver of biodiversity. New Phytol 201:403–416

    Article  Google Scholar 

  • Moro MJ, Pugnaire FI, Haase P, Puigdefábregas J (1997) Effect of the canopy of Retama sphaerocarpa on its understorey in a semiarid environment. Funct Ecol 11:425–431

    Article  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  Google Scholar 

  • Nardini A, Lo Gullo MA, Trifilò P, Salleo S (2014) The challenge of the Mediterranean climate to plant hydraulics: responses and adaptations. Environ Exp Bot 103:68–79

    Article  Google Scholar 

  • Navarro T, Cabezudo B (1998) Estrategias Fenomorfológicas de Especies de un Matorral Mediterráneo (Andalucía, España). Acta botánica malacitana 23:133–148 ISSN 0210-9506

    Google Scholar 

  • Ochoa-Hueso R, Allen EB, Branquinho C, Cruz C, Dias T, Fenn ME, Manrique E, Pérez-Corona ME, Sheppard LJ, Stock WD (2011) N deposition effects on Mediterranean-type ecosystems: an ecological assessment. Environ Pollut 159:2265–2279

    Article  CAS  Google Scholar 

  • Ochoa-Hueso R, Mejías-Sanz V, Pérez-Corona ME, Manrique E (2013a) Nitrogen deposition effects on tissue chemistry and phosphatase activity in Cladonia foliacea (Huds.) Willd., a common terricolous lichen of semi-arid Mediterranean shrublands. J Arid Environ 88:78–81

    Article  Google Scholar 

  • Ochoa-Hueso R, Stevens CJ, Ortiz-Llorente MJ, Manrique E (2013b) Soil chemistry and fertility alterations in response to N application in a semiarid Mediterranean shrubland. Sci Total Environ. doi:10.1016/j.scitotenv.2013.02.049

    Article  Google Scholar 

  • Ochoa-Hueso R, Maestre FT, de los Ríos A, Valea S, Theobald MR, Vivanco MG, Manrique E, Bowker MA (2013c) N deposition alters N cycling and reduces soil carbon content in low-productivity semiarid Mediterranean ecosystems. Environ Pollut 179:185–193

    Article  CAS  Google Scholar 

  • Ochoa-Hueso R, Manrique E (2014) Impacts of altered precipitation, nitrogen deposition and plant competition on a Mediterranean seed bank. J Veg Sci 25(5):1289–1298

    Article  Google Scholar 

  • Padgett PE, Allen EB (1999) Differential responses to nitrogen fertilization in native shrubs and exotic annuals common to Mediterranean coastal sage scrub of California. Plant Ecol 144:93–101

    Article  Google Scholar 

  • Payne RJ, Dise NB, Stevens CJ, Gowing DJ, BEGIN Partners (2013) Impact of N deposition at the species level. PNAS 110(3):984–987

    Article  Google Scholar 

  • Pesch R, Schröder W, Schmidt G, Gensslerb L (2008) Monitoring N accumulation in mosses in central European forests. Environ Pollut 155(3):528–536

    Article  CAS  Google Scholar 

  • Phoenix GK, Hicks WK, Cinderby S, Kuylenstierna JCI, Stock WD, Dentener FJ, Giller KE, Austin AT, Lefroy RDB, Gimeno BS, Ashmore MS, Ineson P (2006) Atmospheric nitrogen deposition in world biodiversity hotspots: the need for a greater global perspective in assessing N deposition impacts. Glob Chang Biol 12:470–476

    Article  Google Scholar 

  • Puértolas J, Rey Benayas JM, Michalet R (2010) Facilitation of Quercus ilex in Mediterranean shrubland is explained by both direct and indirect interactions mediated by herbs. J Ecol 98:687–696

    Article  Google Scholar 

  • Pugnaire FI, Haase P, Incoll LD, Clark SC (1996a) Response of the tussock grass Stipa tenacissima to watering in a semi-arid environment. Funct Ecol 10:265–274

    Article  Google Scholar 

  • Pugnaire FI, Haase P, Puigdefábregas J, Cueto M, Clark SC, Incoll LD (1996b) Facilitation and succession under the canopy of a leguminous shrub, Retama shaerocarpa, in a semi-arid environment in southeast Spain. Oikos 76:455–564

    Article  Google Scholar 

  • Pugnaire FI, Lázaro R (2000) Seed bank and understorey species composition in a semi-arid environment: the effect of shrub age and rainfall. Ann Bot 86:807–813

    Article  Google Scholar 

  • Qian YL, Fry JD, Upham WS (1997) Rooting and drought avoidance of warm-season turfgrasses and tall fescue in Kansas. Crop Sci 37:905–910

    Article  Google Scholar 

  • Rivas-Martínez S (1987) Memoria del mapa de series de vegetación de España. ICONA, Madrid

    Google Scholar 

  • Rousset O, Lepart J (1999) Shrub facilitation of Quercus humilis (downy oak) dynamics on calcareous grasslands. J Veg Sci 10:493–502

    Article  Google Scholar 

  • Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774

    Article  CAS  Google Scholar 

  • Sardans J, Rodà F, Peñuelas J (2005) Effects of water and a nutrient pulse supply on Rosmarinus officinalis growth, nutrient content and flowering in the field. Environ Exp Bot 53:1–11

    Article  CAS  Google Scholar 

  • Sardans J, Rivas-Ubach A, Peñuelas J (2012) The C:N:P stoichiometry of organisms and ecosystems in a changing world: a review and perspectives. Perspectives in Plant Ecology, Evolution and Systematics 14:33–47

    Article  Google Scholar 

  • Tomaselli R (1977) The degradation of the Mediterranean Maquis. Ambio 6(6) SI The Mediterranean:356–362

    Google Scholar 

  • Tessier JT, Raynal DJ (2003) Use of nitrogen to phosphorus ratios in plant tissue as an indicator of nutrient limitation and nitrogen saturation. J Appl Ecol 40:523–534

    Article  CAS  Google Scholar 

  • Valiente-Banuet A, Verdú M (2007) Facilitation can increase the phylogenetic diversity of plant communities. Ecol Lett 10:1029–1036

    Article  Google Scholar 

  • Valladares F, Laanisto L, Niinemets Ü, Zavala MA (2016) Shedding light on shade: ecological perspectives of understorey plant life. Plant Ecology & Diversity. doi:10.1080/17550874.2016.1210262

    Article  Google Scholar 

  • Van der Waal C, de Kroon H, de Boer WF, Heitkönig IMA, Skidmore AK, de Knegt HJ, van Langeveldem F, van Wieren SE, Grant RC, Page BR, Slotow R, Kohi EM, Mwakiwa E, Prins HHT (2009) Water and nutrients alter herbaceous competitive effects on tree seedlings in a semi-arid savannah. J Ecol 97:430–439

    Article  Google Scholar 

  • Villar R, Merino J (2001) Comparison of leaf construction costs in woody species with differing leaf life-spans in contrasting ecosystems. New Phytol 151:213–226

    Article  Google Scholar 

  • Vivanco MG, Palomino I, Vautani R, Bessaget B, Martín F, Menut L, Jimenez S (2009) Multi-year assessment of photochemical air quality simulation Spain. Environ Model Softw 24:63–73

    Article  Google Scholar 

  • Wagenmakers EJ, Farrell S (2004) Notes and comments: AIC model selection using Akaike weights. Psychon Bull Rev 11(1):192–196

    Article  Google Scholar 

  • Werner C, Correia O, Beyschlag W (1999) Two different strategies of Mediterranean macchia plants to avoid photoinhibitory damage by excessive radiation levels during summer drought. Acta Oecol 20:15–23

    Article  Google Scholar 

  • Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP (2006) Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol 75(5):1182–1189

    Article  Google Scholar 

Download references

Acknowledgements

This research was financially supported by a research grant of the Spanish Ministerio de Economía y Competitividad (BIOMOD CGL-2013-44661-R). Comunidad de Madrid also funded this work through REMEDINAL-3 project (S2013/MAE-2719). The authors are very thankful to the owners of “Finca El Regajal” for their kind permission to work in their property. They are also very thankful to Lucas Lecha for helping during the field and lab work.

Author information

Authors and Affiliations

  1. Museo Nacional de Ciencias Naturales CSIC, Serrano 115 dpdo, 28006, Madrid, Spain

    Ciro Cabal & Esteban Manrique

  2. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, 08544, USA

    Ciro Cabal

  3. Department of Ecology, Universidad Autónoma de Madrid, C/Darwin 2, 28049, Madrid, Spain

    Raúl Ochoa-Hueso

  4. Department of Ecology, Faculty of Biology, Universidad Complutense de Madrid, C/José Antonio Novais 2, 28040, Madrid, Spain

    María Esther Pérez-Corona

Authors
  1. Ciro Cabal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Raúl Ochoa-Hueso
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. María Esther Pérez-Corona
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Esteban Manrique
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ciro Cabal.

Additional information

Responsible editor: Philippe Garrigues

Electronic supplementary material

ESM 1

(DOCX 28 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cabal, C., Ochoa-Hueso, R., Pérez-Corona, M.E. et al. Long-term simulated nitrogen deposition alters the plant cover dynamics of a Mediterranean rosemary shrubland in Central Spain through defoliation. Environ Sci Pollut Res 24, 26227–26237 (2017). https://doi.org/10.1007/s11356-017-8879-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-8879-7

Keywords

Search

Navigation