Lichen species dominance and the resulting photosynthetic behavior of Sonoran Desert soil crust types (Baja California, Mexico)

More than 35% of the Earth’s landmass is arid to semiarid and soils of these regions are frequently covered by biological soil crusts, BSCs (Pointing and Belnap 2012). They are intimate associations between soil particles, cyanobacteria, algae, microfungi, lichens and bryophytes (Belnap et al. 2003). In such regions BSCs can have a strong influence on ecosystem functioning. In particular they can improve the stability of soils and the resistance to soil erosion by wind and water increases with BSC development independent of the substrate. BSCs also improve soil fertility and influence hydrological cycles. The effects of various types of BSC have been well studied in arid and semi-arid environments and it is in such nutrient and/or water poor environments that they make their greatest impact (Belnap and Lange 2003). By fixing atmospheric carbon, the photoautotrophic components of the BSC can underpin the trophic hierarchy by leaching some fixed carbon into the soils (Dudley and Lechowicz 1987, Dümig et al. 2013) and by themselves being a food resource for heterotrophs. In addition BSC components like free living cyanobacteria and cyanolichens can also fix atmospheric nitrogen and supply this to the communities. These ecosystem services are of special importance in areas where no higher primary producer influences the simple and nutrient poor soils.

Being composed of different organisms does not necessarily mean that they all contribute equally to biomass. Depending on environmental conditions, certain groups of organisms dominate over others, resulting in crusts where most of the biomass is typically either formed by cyanobacteria, by cyano- and/or chlorolichens lichens, or by liverworts or mosses. Although patchiness and pattern formation in time and space of BSCs is a known phenomenon (Belnap et al. 2006), little is known about the factors driving small scale patterns of abundance and distribution (Martinez et al. 2006; Richter et al. 2012). Few studies have dealt with small scale pattern formation of crusts. However, one study revealed a scale-dependent positive correlation between abiotic stress such as water and nutrient availability and co-occurrence of BSC-lichens (Maestre et al. 2009).

Büdel et al. (2009) distinguished between 7 major crust types in their study on South African BSCs. For example BSC-type 4 was defined being a late successional cyanobacterial crust with green algae, cyano- and chlorolichens. However, all crust types showed strong small scale patterns, with different groups of species dominating in certain patches. Soil crust patchiness happens in the scale of square centimeters to square meters and can be a highly dynamic process with time periods in the range of several months for cyanobacteria and algae (Belnap et al. 2006). Since cyanobacteria, cyanolichens, and chlorolichens can vary considerably in photosynthetic properties related to reactivation after desiccation and thallus water content (Lange and Kilian 1985; Lange et al. 1986; 1993), patchiness in species composition most probably also results in considerable patchiness of photosynthetic CO₂-fixation rates. In order to test this hypothesis and to quantify its possible impact we studied the CO₂-uptake patterns of four differently lichen-dominated BSCs from Baja California (Sonoran Desert) under experimentally controlled conditions. The BSC-patches investigated, were each covered by one lichen species only. Two were dominated by the cyanolichens Peltula richardsii or P. patellata, and two by the chlorolichens Psora decipiens or Placidium squamulosum, respectively (see Figure 1).

In addition to the dominating lichen species Psora decipiens, Placidium squamulosum, Peltula patellata and P. richardsii, several other lichen species and 12 free living cyanobacterial species were found at the four BSC collection sites in Baja California. For a complete cyanobacterial and lichen species inventory see Table 1. The experimental material (Figure 1) contained one lichen species only, but was accompanied by free living cyanobacteria (Table 1) on top of the soil between lichen thalli. Their coverage of the total sample area was always less than 2%. While the two chlorolichen-dominated BSCs came from sites with an annual precipitation of 190 and 250 mm, precipitation of the two cyanolichen dominated BSCs sampling sites is roughly half as much, 110 and 120 mm.

Reactivation of the initially dry Psora decipiens (chl) dominated BSC (Figure 1a) became measureable 3 hours after exposure to high air humidity for dark respiration (R) and after 9.5 hours for net photosynthesis (NP). After about 60 hours and through water vapor hydration alone, the lichen attained ca. 37.5% of its maximal CO₂ uptake that was enabled after subsequent moistening of the thalli with liquid water (Figure 2). In a repeat of the reactivation experiment, spraying with water after 72 hour exposure to high air humidity resulted in a water suprasaturation of the crust. As a consequence, the NP curve dropped (Figure 2), and recovered higher CO₂ uptake rates by evaporative water loss for a few hours. In the second run of experiments with drying-down curves after maximal water saturation of the samples, dependence of CO₂ exchange on crust hydration has been quantified (Figure 3). Maximum rates of NP (90-100% of those gained in the second experiment) were reached at crust water content in the range between 0.38 and 0.81 mm precipitation equivalent. At higher degrees of hydration, a strong suprasaturation depression of CO₂ uptake became obvious that reduced NP to 9.7% of its maximal rate in the same experiment (Figure 3).

The initially dry Placidium squamulosum (chl) dominated crust (Figure 1b) showed first reactions of R 4 hours 30 minutes after exposure to high air humidity alone. Net photosynthesis started 24 hours after exposure and reached 14.7% of its maximal CO₂-uptake after subsequent moistening with liquid water (Figure 2). In the second experiments, the drying down curves after maximal water saturation of the crust, maximum rates (90-100%) of NP were determined at crust water content between 0.40 to 0.77 mm precipitation equivalents. At higher degrees of hydration, a moderate suprasaturation depression of CO₂ uptake appeared, that reduced NP to 59.5% of its maximum rates in the same experiment (Figure 3).

The initially dry Peltula richardsii (cyl) dominated crust (Figure 1c) did not show any reaction of R and NP to 72 hours exposure with high air humidity alone (Figure 2). Respiration and NP were only activated by spraying with water after 72 hours exposure to high air humidty (Figure 2). Testing the relation of CO₂ uptake depending on crust water content in the second experimental setup, these crust type reached maximal CO₂ uptake (90-100%) in a range of 0.72 to 1.17 mm precipitation equivalent. Higher degrees of hydration resulted in a moderate suprasaturation depression of CO₂ uptake, reducing NP to 40.3% of its maximal rates (Figure 3).

For the initially dry P. patellata (cyl) dominated crust (Figure 1d), neither reactivation of R, nor activation of NP was observed after exposure to high air humidity alone for 72 hours. Respiration and NP were only reactivated after spraying with liquid water (Figure 2). The second experimental setup revealed with 0.48 to 1.05 mm precipitation equivalent the widest range of crust water content, at which maximal (90-100%) CO₂ uptake was gained. Higher crust water content resulted in a strong suprasaturation depression of CO₂ uptake, which reduced NP to 23.4% of its maximal rates (Figure 3).

The BSCs investigated here all belong to the late successional phase, referring to BSC type 4 (cyanobacterial crust with cyano- and chlorolichens) described by (Büdel et al. 2009) from southwest Africa. The species list given in Table 1 is not representative for the Baja Californian BSCs, as it only lists species found in the samples that were used for the experiments presented here. From own observations and literature we know, that much more lichen-, liverwort-, moss-, cyanobacterial-, and algal-species occur (Flechtner et al. 1998; Rosentreter and Belnap 2003; McCune and Rosentreter 2007). In the present work we focused on the patchiness of photosynthetic performance related to patchiness of dominating lichens species in BSCs at different sites. While R and NP of the two BSC types dominated by cyanolichens could not be activated by high air humidity alone, the two chlorolichen dominated crust types both recovered R and NP at different rates. With high relative air humidity (96%), the Psora decipiens crust reached almost 38% and the Placidium squamulosum crust roughly 15% of their referring maximum rates attained after hydration with liquid water. This is well in accordance with the findings of (Lange and Kilian 1985) and (Lange et al. 1993), who first showed that, in contrast to chlorolichens, cyanolichens of different taxonomical groups cannot be activated with high air humidity alone. The large difference between maximum rates reached and the time for reactivation of NP between the two species (Figure 2, upper graphs) suggest an advantage for Psora decipiens in habitats that regularly experience high air humidity as for example near the coastline.

Studies on the photosynthetic performance of lichens as components of BSCs from temperate regions (Germany) included the species Peltigera rufescens (Weiss) Humb. (cyl), Fulgensia fulgens (Swarz) Elenk. (chl), Diploschistes muscorum (Scop.) R. Sant. (chl), Collema tenax, C. cristatum (L.) Weber (cyl), Cladonia convoluta (Lamb) P. Cout. (chl), C. rangiformis Hoffm. ( (Hahn et al. chl), and Squamarina lentigera 1989; Lange 2000a; Lange and Green 2003, 2004). In all of these studies diurnal courses of photosynthesis under natural conditions, photosynthetic performance at different light intensities, and water content of individual species (separated from other BSC organisms) were investigated (Table 2). It was shown that all chlorolichens investigated like for example Cladonia convoluta could be activated by early morning dewfall. However, for the cyanolichen Collema cristatum in the same habitat at the same time, this event was just enough to reactivate respiration (Lange 2000b). The Psora decipiens and Placidium squamulosum crusts reached maximum NP rates at lower water content (0.3 and 0.44 mm precipitation equivalent) than the Peltula richardsii crust (0.72 mm), while P. patellata (0.48 mm) was more or less similar with the Placidium squamulosum crust.

The relation of high thallus water content and photosynthesis was investigated in the BSC lichens Cladonia convoluta, C. pocillum (Ach.) O.J. Richter (chl), Diploschistes muscorum, Squamarina lentigera, Collema tenax, Toninia sedifolia (Scop.) Timdal ( from steppe vegetation in Germany (Lange et al. chl), and Fulgensia fulgens 1995). In this study four different response types to water suprasaturation were found: type A lichens (Cladonia convoluta, Diploschistes muscorum) with no or almost no CO2-uptake depression, type B lichens (Squamarina lentigera) with only a little depression, type C lichens (Collema tenax, Toninia sedifolia) with a large and increasing depression as the water content increases, and finally the type D lichens (Cladonia pocillum, Fulgensia fulgens) with a strong depression but an inflection so that NP is low but constant. According to this classification, the Psora decipiens and probably the Placidium squamulosum dominated BSCs from our study behave like type D lichens (Figure 3), while the Peltula richardsii and P. patellata dominated BSC types refer to type C.

Using the BSC green algal lichens Diploschistes muscorum and Fulgensia fulgens (Schreber) Norm. (chl), (Lange et al. from a temperate steppe formation, together with the lithophilic D. scruposus 1999) investigated the response of photosynthesis to external CO₂ concentration in interaction with the thallus water content. They showed that indeed a water suprasaturation-induced increase in thallus conductance is responsible for CO₂-uptake depression. When exposed to stepwise elevated external CO₂ concentrations, the effect of CO₂-uptake depression was alleviated, and it eventually disappeared totally (with Fulgensia fulgens at 4500 ppm CO₂, Diploschistes muscorum 1000 ppm, D. scruposus 1500 ppm). This clearly shows that species composition of BSC lichens and therefore their productivity might not only be influenced by temperature as a consequence of global warming, but also and probably to an even larger degree, by increasing ambient air CO₂ concentrations.

Our results show that patchiness of BSC composition (i.e. dominance of single species) is reflected also in patchiness of photosynthetic performance, a phenomenon which seems to be especially important if different functional types of BSC components are involved. This fact might help to interpret soil-crust performance. Thus, as an example, functional patchiness might be part of an explanation for observed differences of soil nutrient availability (soil organic carbon and total nitrogen), that was observed to be significantly different among three desertified grasslands along a degradation gradient, or for the spatial heterogeneity of soil nutrients and respiration of BSC cover in Inner Mongolia (Yu-Chun et al. 2010).

Eldridge and Ferris (1999) reported that the phylogenetic and morphologically closely to Psora decipiens related lichen Psora crenata (Taylor) Reinke (chl), a common BSC component in the Americas and Australia, needs years if not tens of years after disturbance to recover in Australia. Given the important ecological role of BSCs in dry lands of the Earth, also with regard to CO₂-fixation (Elbert et al. 2012), detailed knowledge about the mechanisms determining species composition and BSC development in a spatiotemporal scale, is inevitable.

While the Psora decipiens dominated BSC might have an advantage in habitats with frequent high air humidity (e.g. along the coastline), the cyanolichen dominated BSC-types (Peltula patellata, P. richardsii) might have advantage in dryer sites that are subject to floodings. Placidium squamulosum dominated BSCs are somehow in-between, as they can reactivate NP at least to a small proportion, but, to a lesser degree, also can stand water suprasaturation. However, these theoretical conclusions have to remain speculative and are meant as working hypotheses for continuation of research. As a consequence of our studies, it becomes obvious that investigating photosynthetic carbon gain of BSCs cannot just be performed on small soil crust samples of few square centimeters, but need to cover the full spectrum of BSC patches dominated by different species and species composition.