Simulated climate change reduced the capacity of lichen-dominated biocrusts to act as carbon sinks in two semi-arid Mediterranean ecosystems

Biodiversity and Conservation

Volumn 23, Issue 7, 2014, Pages 1787-1807

  Ladrón de Guevara, Mónica ^a   Lázaro, Roberto ^a   Quero, José L ^b   Ochoa, Victoria ^c   Gozalo, Beatriz ^c   Berdugo, Miguel ^c   Uclés, Olga ^a   Escolar, Cristina ^c   Maestre, Fernando T ^c  

^a DEPARTAMENTO DE ECOLOGÍA FUNCIONAL Y EVOLUTIVA   (Spain)

^b UNIVERSITY OF CÓRDOBA   (Spain)

^c UNIVERSIDAD REY JUAN CARLOS   (Spain)

Author keywords

Chlorophyll fluorescence; Gas exchange; Lichens; Rain exclusion; Semi arid land; Warming

Indexed keywords

CARBON SINK; CHLOROPHYLL; CLIMATE CHANGE; GAS EXCHANGE; LICHEN; MEDITERRANEAN ENVIRONMENT; PHOTOSYNTHESIS; RAINFALL; SEMIARID REGION; SOIL CRUST; WARMING;

ALMERIA [ANDALUCIA]; ANDALUCIA; ARANJUEZ; MADRID [SPAIN]; SORBAS; SPAIN;

EID: 84902375043     PISSN: 09603115     EISSN: 15729710     Source Type: Journal    
DOI: 10.1007/s10531-014-0681-y     Document Type: Article

References (79)

1. AEMET (2013) Valores climatológicos normales (media 1971-2000) http://www. aemet. es/es/serviciosclimaticos/datosclimatologicos/valoresclimatologicos. Accessed on 10th October 2013.
2. Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) International Symposium on Information Theory. Akademia Kiado, Budapest, pp 267-81.
3. 2 concentrating mechanism. J Exp Bot 57: 249-265.
4. Belnap J (2003) Biological soil crusts in deserts: a short review of their role in soil fertility, stabilization, and water relations. Arch Hydrobiol 109: 113-126.
5. Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Proc 20: 3159-3178.
6. Belnap J, Lange OL (eds) (2003) Biological soil crusts: structure, function, and management. Springer, New York.
7. Beysens D, Muselli M, Nikolayev V, Narhe R, Milimouk I (2005) Measurement and modelling of dew in island, coastal and alpine areas. Atmos Res 73: 1-22.
8. 2 exchange by biological soil crusts and grasslands of the semiarid Colorado Plateau, United States. J Geophys Res 116: G03028. doi: 10. 1029/2011JG001643.
9. Čabrajić AJ (2009) Modeling lichen performance in relation to climate: Scaling from thalli to landscapes. PhD thesis, Faculty of Science and Technology, Ecology and Environmental Science, Umeå University, Sweden.
10. Calatayud A, Deltoro VI, Barreno E, del Valle-Tascon S (1997) Changes in in vivo chlorophyll fluorescence quenching in lichen thalli as a function of water content and suggestion of zeaxanthin-associated photoprotection. Physiol Plant 101: 93-102.
11. Castillo-Monroy AP, Maestre FT, Rey A, Soliveres S, García-Palacios P (2011) Biological soil crust microsites are the main contributor to soil respiration in a semiarid ecosystem. Ecosystems 14: 835-847.
12. Cnaan A, Laird NM, Slasor S (1997) Using the general linear mixed model to analyse unbalanced repeated measures and longitudinal data. Stat Med 16: 2349-2380.
13. Corporation Onset (2013) HOBO Pro v2 (U23-00x) manual. Onset Computer Corporation, Bourne.
14. De Castro M, Martin-Vide J, Alonso S (2005) El clima de España: pasado, presente y escenarios de clima para el siglo XXI. In: Moreno JM (ed) Evaluación Preliminar de los Impactos en España por Efecto del Cambio Climático. Ministerio Medio Ambiente, Madrid, pp 1-64.
15. De Philippis R, Vincenzini M (1998) Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev 22: 151-175.
16. del Prado R, Sancho LG (2007) Dew as a key factor for the distribution pattern of the lichen species Teloschistes lacunosus in the Tabernas Desert (Spain). Flora 202: 417-428.
17. Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2013) InfoStat. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. http://www. infostat. com. ar. Accessed 25 Sept 2013.
18. Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5: 459-462.
19. Eldridge D, Greene R (1994) Microbiotic soil crusts-a review of their roles in soil and ecological processes in the rangelands of Australia. Aust J Soil Res 32: 289-415.
20. Escolar C, Martínez I, Bowker MA, Maestre FT (2012) Warming reduces the growth and diversity of biological soil crusts in a semi-arid environment: implications for ecosystem structure and functioning. Philos Trans R Soc B 367: 3087-3099.
21. Friedlingstein P, Prentice IC (2010) Carbon-climate feedbacks: a review of model and observation based estimates. Curr Opin Environ Sustain 2: 251-257.
22. Fry EL, Manning P, Allen DGP, Hurst A, Everwand G, Rimmler M, Power SA (2013) Plant functional group composition modifies the effects of precipitation change on grassland ecosystem function. PLoS One 8: e57027. doi: 10. 1371/journal. pone. 0057027.
23. Garcia-Pichel F, Belnap J (1996) Microenvironments and microscale productivity of cyanobacterial desert crusts. J Phycol 32: 774-782.
24. Garcia-Pichel F, Pringault O (2001) Cyanobacteria track water in desert soils. Nature 413: 380-381.
25. Garcia-Pichel F, López-Córtes A, Nübel U (2001) Phylogenetic and morphological diversity of cyanobacteria in soil desert crusts from the Colorado Plateau. Appl Environ Microbiol 67: 1902-1910.
26. Garcia-Pichel F, Belnap J, Neuer S, Schanz F (2003) Estimates of cyanobacterial biomass and its distribution. Arch Hydrobiol 109: 213-228.
27. Green TGA, Büdel B, Heber U, Meyer A, Zellner H, Lange OL (1993) Differences in photosynthetic performance between cyanobacterial and green algal components of lichen photosymbiodemes measured in the field. New Phytol 125: 723-731.
28. Grote EE, Belnap J, Housman DC, Sparks JP (2010) Carbon exchange in biological soil crust communities under differential temperatures and soil water content: implications for global change. Glob Change Biol 16: 2763-2774.
29. Hájek J, Bartak M, Dubova J (2006) Inhibition of photosynthetic processes in foliose lichens induced by temperature and osmotic stress. Biol Plant 50: 624-634.
30. Housman DC, Powers HH, Collins AD, Belnap J (2006) Carbon and nitrogen fixation differ between successional stages of biological soil crusts in the Colorado Plateau and Chihuahuan Desert. J Arid Environ 66: 620-634.
31. IUSS Working Group WRB (2006) World Reference Base for Soil Resources 2006. World Soil Resources Reports No. 103. FAO, Rome.
32. Jacobs AFG, Heusinkveld BG, Berkowicz SM (1999) Dew deposition and drying in a desert system: a simple simulation model. J Arid Environ 42: 211-222.
33. Johnson SL, Kuske CR, Carney TD, Housman DC, Gallegos-Graves LV, Belnap J (2012) Increased temperature and altered summer precipitation have differential effects on biological soil crusts in a dryland ecosystem. Glob Change Biol 18: 2583-2593.
34. Kappen L (1988) Ecophysiological relationships in different climatic regions. In: Galum M (ed) Handbook of lichenology, vol II. CRC Press Inc., Boca Raton, pp 37-100.
35. 2 exchange of Umbilicaria aprina under extreme light stress in the cold. Oecologia 113: 325-331.
36. Kidron GJ (2000) Analysis of dew precipitation in three habitats within a small arid drainage basin, Negev Highlands, Israel. Atmos Res 55: 257-270.
37. Kidron GJ, Temina M (2013) The effect of dew and fog on the lithic lichens along an altitudinal gradient in the Negev Desert. Geomicrobiol J 30: 281-290.
38. Kranner I, Zorn M, Turk B, Wornik S, Beckett RR, Batic F (2003) Biochemical traits of lichens differing in relative desiccation tolerance. New Phytol 160: 167-176.
39. Laird NM, Ware JH (1982) Random-effects models for longitudinal data. Biornetrics 38: 963-974.
40. Lange OL (2003) Photosynthesis of soil-crust biota as dependent on environmental factors. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function and management. Springer, New York, pp 217-240.
41. 2 exchange of Cladonia convoluta under temperate habitat conditions. Bibl Lichenol 86: 257-280.
42. 2 exchange in the field. Bibl Lichenol 88: 363-390.
43. Lange OL, Green TGA (2005) Lichens show that fungi can acclimate their respiration to seasonal changes in temperature. Oecologia 142: 11-19.
44. Lange OL, Kidron GJ, Büdel B, Meyer A, Kilian E, Abeliovich A (1992) Taxonomic composition and photosynthetic characteristics of the 'biological soil crusts' covering sand dunes in the western Negev Desert. Funct Ecol 6: 519-527.
45. Lange OL, Meyer A, Zellner H, Heber U (1994) Photosynthesis and water relations of lichen soil crusts: field measurements in the coastal fog zone of the Namib Desert. Funct Ecol 8: 253-264.
46. 2 exchange. Flora 192: 1-15.
47. 2 exchange. Funct Ecol 12: 195-202.
48. Lange OL, Green TGA, Heber U (2001) Hydration-dependent photosynthetic production of lichens: what do laboratory studies tell us about field performance? J Exp Bot 52: 2033-2042.
49. 2 exchange of the terrestrial lichen Teloschistes capensis in the Namib fog desert: measurements during two seasons in the field and under controlled conditions. Flora 201: 268-280.
50. Lázaro R, Cantón Y, Solé-Benet A, Bevan J, Alexander R, Sancho LG, Puigdefábregas J (2008) The influence of competition between lichen colonization and erosion on the evolution of soil surfaces in the Tabernas badlands (SE Spain) and its landscape effects. Geomorphology 102: 252-266.
51. Lechowicz MJ (1982) Ecological trends in lichen photosynthesis. Oecologia 53: 330-336.
52. LI-COR (2012) Using the LI-6400/LI-6400XT Portable Photosynthesis System, version 6. LI-COR Biosciences Inc, Lincoln.
53. Maestre FT, Bowker MA, Cantón Y, Castillo-Monroy AP, Cortina J, Escolar C, Escudero A, Lázaro R, Martínez I (2011) Ecology and functional roles of biological soil crusts in semi-arid ecosystems of Spain. J Arid Environ 75: 1282-1291.
54. Maestre FT, Escolar C, Ladrón de Guevara M, Quero JL, Lázaro R, Delgado-Baquerizo M, Ochoa V, Berdugo M, Gozalo B, Gallardo A (2013) Changes in biocrust cover drive carbon cycle responses to climate change in drylands. Global Change Biol 19: 3835-3847.
55. Malek E, McCurdy G, Giles B (1999) Dew contribution to the annual water balances in semi-arid desert valleys. J Arid Environ 42: 71-80.
56. Maphangwa KW, Musil CF, Raitt L, Zedda L (2012) Experimental climate warming decreases photosynthetic efficiency of lichens in an arid South African ecosystem. Oecologia 169: 257-268.
57. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51: 659-668.
58. Palmqvist K, Samuelsson G, Badger MR (1994) Photobiont-related differences in carbon acquisition among green-algal lichens. Planta 195: 70-79.
59. Patterson HD, Thompson R (1971) Recovery of inter-block information when block sizes are unequal. Biometrika 58: 545-554.
60. Pinheiro J, Bates D, DebRoy S, Sarkar D, the R Development Core Team (2013) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3. 1-113.
61. Pintado LG, Sancho JM, Blanquer TG, Green A, Lázaro R (2010) Microclimatic factors and photosynthetic activity of crustose lichens from the semiarid southeast of Spain: long-term measurements for Diploschistes diacapsis. Bibl Lichenol 105: 211-224.
62. Potts M (2001) Desiccation tolerance: a simple process? Trends Microbiol 9: 553-559.
63. 2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59: 1441-1461.
64. Randerson JTF, Hoffman M, Thornton PE, Mahowald NM, Lindsay K, Lee YH, Nevison CD, Doney SC, Bonan G, Stockli R, Covey C, Running SW, Fung IY (2009) Systematic assessment of terrestrial biogeochemistry in coupled climate-carbon models. Global Change Biol 15: 2462-2484.
65. Reed SC, Coe KK, Sparks JP, Housman DC, Zelikova TJ, Belnap J (2012) Chages to dryland rainfall result in rapid moss mortality and altered soil fertility. Nat Clim Change 2: 752-755.
66. Rey A, Pegoraro E, Oyonarte C, Were A, Escribano P, Raimundo J (2011) Impact of land degradation on soil respiration in a steppe (Stipa tenacissima L.) semi-arid ecosistema in the SE of Spain. Soil Biol Biochem 43: 393-403.
67. Smith EC, Griffiths H (1998) Intraspecific variation in photosynthetic responses of trebouxioid lichens with reference to the activity of a carbon-concentrating mechanism. Oecologia 113: 360-369.
68. 2 concentration. Arid Land Res Manage 26: 44-58.
69. Temina M, Kidron GJ (2011) Lichens as biomarkers for dew amount and duration in the Negev Desert. Flora 206: 646-652.
70. Thornton PE, Doney SC, Lindsay K, Moore JK, Mahowald N, Randerson JT, Fung I, Lamarque JF, Feddema JJ, Lee YH (2009) Carbon-nitrogen interactions regulate climate-carbon cycle feedbacks: results from an atmosphere-ocean general circulation model. Biogeosciences 6: 2099-2120.
71. Topp GC, Davis JL (1985) Measurement of soil water content using time-domain reflectometry (TDR): a field evaluation. Soil Sci Soc Am J 49: 19-24.
72. Uclés O, Villagarcía L, Moro MJ, Canton Y, Domingo F (2013a) Role of dewfall in the water balance of a semiarid coastal steppe ecosystem. Hydrol Process 28: 2271-2280.
73. Uclés O, Villagarcía L, Canton Y, Domingo F (2013b) Microlysimeter station for long term non-rainfall water input and evaporation studies. Agric Forest Meteorol 182-183: 13-20.
74. Veste M, Littmann T, Friedrich H, Breckle S-W (2001) Microclimatic boundary conditions for activity of soil lichen crusts in sand dunes of the north-western Negev desert, Israel. Flora 196: 465-476.
75. 2 exchange of biological soil crusts in a semiarid grass-shrubland at the northern transition zone of the Negev desert, Israel. Biogeosciences 5: 1411-1423.
76. Yahdjian L, Sala OE (2002) A rainout shelter design for intercepting different amounts of rainfall. Oecologia 133: 95-101.
77. Zangvil A (1996) Six years of dew observations in the Negev Desert, Israel. J Arid Environ 32: 361-371.
78. Zelikova TJ, Housman DC, Grote ED, Neher D, Belnap J (2012) Biological soil crusts show limited response to warming but larger response to increased precipitation frequency: implications for soil processes on the Colorado Plateau. Plant Soil 355: 265-282.
79. Zheng Y, Xu M, Zhao J, Zhang B, Bei S, Hao L (2011) Morphological adaptations to drought and reproductive strategy of the moss Syntrichia caninervis in the Gurbantunggut Desert, China. Arid Land Res Manage 25: 116-127.