Microbiotic crusts on soil , rock and plants : neglected major players in the global cycles of carbon and nitrogen ?

Microbiotic crusts consisting of bacteria, fungi, algae, lichens, and bryophytes colonize most terrestrial surfaces, and they are able to fix carbon and nitrogen from the atmosphere. Here we show that microbiotic crusts are likely to play major roles in the global biogeochemical cycles of carbon and nitrogen, and we suggest that they should be fur5 ther characterized and taken into account in studies and models of the Earth system and climate. For the global annual net uptake of carbon by microbiotic crusts we present a first estimate of ∼3.6 Pg a−1. This uptake corresponds to ∼6% of the estimated global net carbon uptake by terrestrial vegetation (net primary production, NPP: ∼60 Pg a−1), and 10 it is of the same magnitude as the global annual carbon turnover due to biomass burning. The estimated rate of nitrogen fixation by microbiotic crusts (∼45 Tg a−1) amounts to ∼40% of the global estimate of biological nitrogen fixation (107 Tg a−1). With regard to Earth system dynamics and global change, the large contribution of microbiotic crusts to nitrogen fixation is likely to be important also for the sequestration of CO2 by 15 terrestrial plants (CO2 fertilization), because the latter is constrained by the availability of fixed nitrogen.

It is well known that these communities are able to fix carbon and nitrogen from the atmosphere (Mayland and McIntosh, 1966;Jones, 1970;Bentley, 1987;Beymer and Klopatek, 1991;Lange et al., 1992;Freiberg, 1998;Evans and Johansen, 1999;Juh ász et al., 2002;Belnap, 2003;Boison et al., 2004;Yeager et al., 2007).They produce biomass and they release C-and N-containing compounds like carbohydrates and amino acids to the surrounding ecosystem (Boucher and Nash, 1990;Beymer and Klopatek, 1991;Coxson et al., 1992;Belnap and Lange, 2003;Turetsky, 2003;Dojani et al., 2007;Schmidt et al., 2008).However, their contribution to the global cycles of carbon and nitrogen has not yet been quantified.In this study we calculate and present first estimates of the global annual net uptake of CO 2 and fixation of N 2 by microbiotic crusts.

Methods
From earlier studies of microbiotic crusts we have compiled as many estimates of annual uptake fluxes and surface coverage values as we could find in a thorough literature search.For global upscaling we used median values of the flux data in combination with global estimates of the surface areas of (semi)arid regions and plants, respectively.
All used data and references are tabulated in the Appendix (Tables A1-A9).
Note that we used median rather than arithmetic mean values in order to obtain 6985 conservative estimates.The median values were generally in fair agreement with the corresponding arithmetic mean values, and the relative standard errors of the mean values (relative standard deviation divided by the square root of the number of data points) ranged up to ∼80%.Thus we assume that the presented global estimates are uncertain by a factor of ∼2.

Results and discussion
For the net uptake of carbon by soil crusts in arid and semi-arid regions, we obtained a median flux of ∼16 g m −2 a −1 (Table A1a).Multiplication with the global dry-land area (Table A2) yields an estimate of ∼1.0 Pg a −1 for the net uptake of carbon by BSC in arid and semi-arid regions.With regard to the carbon balance, the reported net uptake values (photosynthesis minus respiration) should be considered as net primary production (NPP) (Chapin et al., 2006).Soil crusts occur also in non-vegetated gaps of grasslands, tundra and steppe formations, sparsely vegetated grounds of temperate and boreal forests, burnt forest areas, formerly permafrosted soils, and previously ice-covered glacier grounds (Forman and Dowden, 1977;Eversman and Horton, 2004;Schmidt et al., 2008).The median net carbon uptake by soil crusts in these areas is ∼23 g m −2 a −1 (Table A1b), and that by rock crusts is ∼8 g m −2 a −1 (Table A1c).Because the global area colonized by non-arid BSC and by rock crusts are not known, we cannot provide a quantitative estimate for their carbon uptake, but obviously any non-zero flux will increase the total amount of carbon taken up by biological crusts to more than the value of ∼1 Pg a −1 given above for arid and semiarid soil crusts alone.
For the net uptake of carbon by epiphytic crusts, we obtained a median flux of ∼28 g m −2 a −1 (Table A3).Multiplication with the corresponding global surface areas of evergreen leaves, branches and stems of trees, and tropical lianas (Tables A4, A5, and A7), assuming coverages of 30-50% (Tables A6 and A7), yields an estimate of ∼2.6 Pg a −1 for the global net uptake of carbon by epiphytic crusts (Table A7).
The total value of ∼3.6 Pg a −1 estimated for the global net uptake of carbon by microbiotic crusts corresponds to ∼6% of the estimated global net carbon uptake by terrestrial vegetation (net primary production, NPP: ∼60 Pg a −1 , Running et al., 2004).To put this flux into perspective: it is of the same magnitude as the global annual carbon turnover due to biomass burning, which has been estimated at 3.6 Pg a −1 (Andreae and Merlet, 2001).
The reported values of biomass in microbiotic crusts are in the range of 1-1200 g m −2 (dry mass) with median values of 260 g m −2 for soil crusts and 130 g m −2 for epiphytic crusts (Table A8).By multiplication of these values with the global areas of dry-lands and forests/shrubs, respectively (Tables A2 and A7) we obtain global estimates of ∼17 Pg for the biomass of BSC in arid and semi-arid regions and ∼6 Pg for the biomass of EPC on evergreen leaves, on branches and stems of trees, and on tropical lianas.The total of ∼23 Pg estimated for the global dry biomass of microbiotic crusts corresponds to ∼10 Pg of carbon (conversion factor ∼2) (Whitman et al., 1998), and thus to ∼2% of the estimated global mass of carbon in terrestrial vegetation (470-650 Pg) (Prentice et al., 2001).Microbiotic crusts do not only fix carbon, but are also able to assimilate atmospheric nitrogen.The reported average fluxes of nitrogen fixation are in the range of 0.1-10 g m −2 a −1 (Table A9).With the median values of ∼0.4 g m −2 a −1 for BSC and ∼0.35 g m −2 a −1 for EPC (Table A9) and using the same surface area values as above, we obtain global estimates of ∼30 Tg a −1 and ∼15 Tg a −1 for nitrogen fixation by BSC and EPC, respectively.Thus, the total rate of nitrogen fixation by microbiotic crusts (∼45 Tg a −1 ) appears to be a major contribution to global biological nitrogen fixation, which is estimated to be about 107 Tg a −1 (Galloway, 2005).Note that nitrogen fixation by microbiotic crusts is likely to be important also for the sequestration of CO 2 by terrestrial plants (CO 2 fertilization), because the latter is constrained by the availability of fixed nitrogen (Reich et al., 2006).

4 Conclusions
Overall, our calculations suggest that microbiotic crusts on soil, rock, and plants are major players in the global biogeochemical cycles of carbon and nitrogen and should thus be considered in climate and Earth system models.Regional and seasonal patterns as well as long-term trends regarding their diversity, abundance and gas exchange with the atmosphere need to be better characterized for a full mechanistic and quantitative understanding of the influence of the biosphere on climate.

Table A6 .
Plant surface coverage by EPC on (a) leaves, (b) needles, and (c) stems and branches.

Table A7 .
Annual net carbon uptake by EPC in forest and shrub areas. e)