•Growth in two old forest lichens was studied to evaluate how temporal (seasonal) and spatial (aspect-wise) partitioning of biomass and area growth respond to seasonal changes in light and climate.
•We monitored relative growth rates during annual courses in the cephalolichen Lobaria pulmonaria and the cyanolichen Lobaria scrobiculata transplanted in boreal clear-cut to five fixed aspects in winter, spring, summer, and autumn. For each annual set, growth was quantified in January–March, April–June, July–September and October–December.
•Mean biomass and area increased in all seasons, but growth was highest in July–September. Mass growth did not follow area increment during a year. As a result, mass per area (specific thallus mass (STM)) declined (L. scrobiculata) or stayed constant (L. pulmonaria) in the dark, humid October–December season, whereas it strongly increased in the dry, sunny April–June season. Aspect influenced growth in species-specific ways. Seasonality in biomass growth mainly followed light availability, whereas area growth was strongest during humid seasons.
•The substantial STM changes across seasons, species, and aspects can be explained as passive responses to seasonal climate. However, as STM, according to the literature, is a driver of water storage, recorded changes probably improve fitness by prolonging hydration in places or during times with high evaporative demands.
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Epiphytic lichens comprise a notable, but declining part of the biodiversity in boreal forests. Concern for this spectacular biomass component has stimulated experimental studies to assess biomass accumulation in terms of lichen growth rates (e.g. Dahlman & Palmqvist, 2003; Gaio-Oliveira et al., 2004; Gauslaa et al., 2006, 2007; Coxson & Stevenson, 2007; Larsson et al., 2009). There is a long tradition of measuring radial growth in rosette-forming foliose and crustose lichens, as reviewed by Armstrong & Bradwell (2011). However, many epiphytic lichens do not form rosettes and have growth forms with substantial intercalary growth (e.g. Honegger, 1993) requiring other methods than radial growth measurements. From a functional perspective, thallus area and biomass are important parameters, and assessment of their dynamics can provide new knowledge.
So far, lichen growth has been reported on a range of temporal scales in various habitats. Yet, few studies have quantified seasonal variation in growth of thallus area and biomass simultaneously. A comparison of available seasonal growth studies shows that site- and/or stand-specific factors tend to shape recorded contrasts in growth rates (e.g. Benedict, 1990; Muir & Shirazi, 1997; Kytöviita & Crittenden, 2002; Caldiz, 2004). Thus, growth experiments under more standardized field conditions are needed to understand mechanisms behind lichen responses and variations in seasonal growth patterns. Such basic knowledge has practical importance for modeling studies and for lichen conservation.
Like most photosynthetic organisms in seasonal climates, lichens are known to acclimate temporarily by tuning various functions to seasonal climatic changes (McEvoy et al., 2007; Vráblikováet al., 2006; Lange & Green, 2005). They probably need a high resilience to maximize growth rate and/or survival under fluctuating conditions (Schofield et al., 2003). Lichen growth is often three-dimensional (Gauslaa et al., 2009). Mass growth responds to photosynthesis (Palmqvist, 2000), whereas the area expansion is poorly understood. Changes in specific thallus mass (STM) occur when area and mass do not increase in parallel. STM, a main driver of water-holding capacity in lichens (Gauslaa & Coxson, 2011), may respond to seasonally changing humidity availability and thereby impact lichen fitness. When laminar growth occurs in older thallus portions of Lobaria (Honegger, 1993), evidenced by enlargements of the characteristic reticulate patterns, simultaneous or delayed changes in STM may also occur as increase in thickness or as thinning during area expansion. STM is significantly higher in lichen populations growing in open forests than in those inhabiting shaded habitats (Gauslaa & Coxson, 2011), but it is not known if STM varies in response to seasonally changing evaporative demands. One aim is to quantify changes in STM in studied lichens during an annual cycle in a site with humid autumns and drier springs (Thue-Hansen & Grimenes, 2010).
This study focuses on two epiphytic old forest lichens, the cephalolichen Lobaria pulmonaria which has a green alga as its main photobiont and the cyanolichen Lobaria scrobiculata. These foliose species are used to indicate ecological continuity in boreal forest conservation management. Nevertheless, such lichens can grow fast in clear-cuts and forest edges because they benefit from the higher light intensity than that available in forest stands (Renhorn et al., 1997; Gauslaa et al., 2006, 2007). By running the growth experiment in a boreal clear-cut, we can separate the effects of seasonal climatic patterns from those derived from spatial (Gauslaa & Solhaug, 2001) and temporal (Gauslaa & Solhaug, 2000) variations in canopy cover, and thus reduce unexplained variation in growth. Lichen growth in open sites should, compared with growth inside forests, be more directly linked to physical parameters such as seasonally changing light, temperature and humidity. At high latitudes with low sun, the aspect of lichen-inhabited surfaces is probably important, and the aspect-dependent light exposure changes substantially during a year. Therefore, our two main aims were (1) to quantify seasonal changes in biomass and thallus area during a boreal year, and (2) to analyze how aspect in interaction with season influences the growth of the studied lichens.
Materials and Methods
We collected Lobaria pulmonaria (L.) Hoffm. and Lobaria scrobiculata (Scop.) DC. on 4 July, 6 October, 3 January and 7 April in Namsos, central western Norway (64°20–25′N, 11°16–30′E) in natural old Picea abies-dominated forests with abundant occurrences of both species. Shortly after each collection, lichens were air-dried at room temperature, and transported to the laboratory. Lichens were then cut into pieces consisting of two to six lobes each to standardize the transplant size (L. pulmonaria: DM = 115 ± 1 mg; area = 11.9 ± 0.13 cm2; L. scrobiculata: DM = 132 ± 2 mg; area = 10.0 ± 0.11 cm2; mean ± 1 standard error; n = 480). All thalli were cleaned from attached tree bark and mosses and rinsed in deionized water. They were then pretreated in the hydrated state at low light (photosynthetic photon flux density (PPFD) 15 μmol m−2 s−1; incandescent lamp) and 18°C for 24 h to allow recovery from occasional short-term photoinhibition.
The study site was a clear-cut area located in Ski, eastern Norway, (59°45′N, 10°56′E). Surrounding forest consisted of mixed P. abies stands older than 70 yr. The two study lichens occurred sparsely, but naturally in surrounding forests. The climate was suboceanic with cold winters and mild to warm summers with total precipitation of 931, 1086, 1164 and 997 mm (Thue-Hansen & Grimenes, 2010) in the four annual transplantation periods, respectively (July 2007–July 2008, October 2007–October 2008, January 2008–January 2009, and April 2008–April 2009; Fig. 1b–e, Table 1). These levels of annual rainfall were slightly below normal rainfall in the source habitats. Day length (PPFD > 2 μmol m−2 s−1) varied between 18 h 45 min in summer and 5 h 15 min in winter.
Table 1. Sum of basic climatic data in the seven growth seasons
PPFD (mol m−2)
1PPFD < 2 μmol m−2 s−1.
Thalli were transplanted shortly after collection to the clear-cut. All transplants in one season comprised one set (Fig. 1a). Each annual set was named after the month in which it started. The first set (July) was transplanted in early July 2007. At the end of September, the July set was temporarily brought to the laboratory for measurements. After measurements, the thalli in the July set were re-transplanted at the beginning of October to let the July thalli continue growth in their previous positions in the clear-cut. Simultaneously, the October set, comprising freshly collected thalli from the forest, was transplanted. This procedure continued until the fourth set of new forest transplants had been introduced to the clear-cut in early April the following year (April set), simultaneously with the re-transplantation of the previous July, October, and January sets after laboratory measurements (Fig. 1a). After the first set (July) had repeatedly been transplanted in the field in four subsequent seasons (one complete year), this set was left in the laboratory, while the three remaining sets were re-transplanted to complete their respective annual cycles. The experiment thus started on 4 July 2007 and ended on 27 March 2009. The growth was recorded in each season separately (January–March, April–June, July–September, and October–December; Fig. 1a).
Thalli were fastened by flax thread to 60 plastic meshes. We fastened the basal parts to let young tips hang freely. This allows curling, a natural response to desiccation, providing photoprotection by self-shading (Barták et al., 2006). Each mesh had 16 positions where two thalli from each species and set were randomly positioned. The meshes were attached to the sides, covered with Alnus incana bark, of 12 wooden boxes facing south, west, north and east as well as the top. The top, tilted (25°) to allow water run-off, faced the sun perpendicularly in summer (see Fig. 1 in Gauslaa et al., 2001). The boxes were placed 1.5 m above the ground on randomly positioned wooden sticks. The plastic meshes were attached to the five box sides using plastic staples. Each set consisted of 120 thalli, giving a total of 480 thalli of each species in the experiment. Less than 6% (22 L. pulmonaria and 28 L. scrobiculata) of thalli were lost during the entire study period, with no bias in terms of set or aspect.
Image analysis of hemispherical digital photographs (e.g. Englund et al., 2000) was used to quantify the diffuse and direct irradiance at the five aspects for each month separately. One photograph was taken from a horizontal position on top of each transplantation box, with the magnetic north indicated. Photographs were taken with a Nikon Coolpix 4500 camera with a Nikon Fisheye converter (FC-E8). Images were analyzed using Gap Light Analyzer (gla) version 2.0 software (Frazer et al., 2000), and the results from all five aspects were corrected by comparing predicted irradiance on a horizontal surface with observed irradiance from a quantum sensor (model S-LIA-M003; Onset Computer Corporation, Bourne, MA, USA) connected to a Hobo Microstation Datalogger (model H21-002; Onset Computer Corporation) logging irradiance every 5 min during the entire experimental period.
Area and mass measurements
Thallus area (A) was measured with a leaf area meter (LI3100; Li-Cor, Lincoln, NE, USA) while the thallus was fully hydrated. The transplants were then left to desiccate at room temperature for 48 h before the mass was recorded (± 0.0001 g). Ten additional control thalli were treated similarly and repeatedly weighed together with the transplants. No change in mass occurred in control thalli during the weighing period. The control thalli were then oven-dried for 24 h at 70°C before measuring dry mass (DW). The mass of transplants was corrected to DW by the mass reduction factor of the 10 oven-dried thalli.
Growth was calculated as relative growth rate (RGR = loge(DM2/DM1)/Δt) and relative thallus area growth rate (RTAGR = loge(A2/A1)/Δt, where Δt is the number of days between times t1 (start) and t2 (end) at which DM (g) and A (cm2) were measured) (cf. Evans, 1972). At each mesh the two thalli of the same species and set comprise one observation pair. Each pair mean was treated as one observation. An observation was categorized as an outlier if it had an unexplained high standardized residual (> ± 2.5). Of 480 observations in total per species, < 6% were classified as outliers. Most outliers occurred in July–September, and were distributed both above and below the fitted mean value of treatment combinations.
Transplant growth and change in specific thallus mass (STM = DM/A) were analyzed with a repeated measurement ANOVA. The pairing of two thalli on each net was taken as a random factor nested within aspect and set, and repeatedly measured within the seasons. We analyzed the following factors: species, season and aspect, including all interactions. Differences between factor levels were analyzed using Tukey’s test. Residuals in all analyses had a normal distribution (Anderson–Darling test) and analyses were performed in minitab V 15.
Growth in both species was strongly seasonal (Table 2), with the highest biomass and area growth in the summer season, July–September (Figs 2, 3). RGR and RTAGR were clearly higher in July–September than in April–June. Both periods had long days and high irradiance (particularly April–June; Table 1), but precipitation and night humidity were higher (Fig. 1), and dew events more frequently observed during field visits in July–September. The July–September and October–December periods were humid with similar precipitation and night-time humidity (Fig. 1). Nevertheless, these seasons represented the best and poorest season for mass growth, respectively.
Table 2. ANOVA tables for growth rates (relative growth rate (RGR) and relative thallus area growth rate (RTAGR)) and change in specific thallus mass (STM) in Lobaria pulmonaria and Lobaria scrobiculata
ID : random factor in the repeated measurement ANOVA representing the pairing of two thalli on each net, nested within aspect and set, and repeatedly measured within the seasons.
A × Set
A × S
Set × S
A × Set × S
A × Set
A × S
Set × S
A × Set × S
Lobaria pulmonaria grew more quickly than L. scrobiculata. In L. pulmonaria, RGR and RTAGR were positive in all seasons, whereas L. scrobiculata had a number of slightly negative RTAGR means in the dry April–June season, and negative RGR values in the dark October–December season. The darkest period, October–December (Table 1), was the least productive season for both species in terms of biomass increase (Fig. 2). The January–March season is slightly colder than October–December (Fig. 1). Nevertheless, January–March gave higher mass growth than October–December, probably because light doubles (Fig. 1d) from 4–5% (October–December) to 8–9% (January–March) of the annual irradiance dose (Table 1). With respect to RTAGR, the period with the slowest growth was the dry season, April–June, for L. scrobiculata and the dark season, October–December, for L. pulmonaria, although area expansion in L. pulmonaria was also low in the dry April–June season (Fig. 3).
As RGR and RTAGR exhibited different annual courses, there was a significant seasonal variation in mass accumulation per area, measured as change in STM (Fig. 4; Table 2). The mean start value of STM, representing shade-adapted forest thalli, was 9.75 ± 0.06 mg cm−2 for L. pulmonaria and 13.22 ± 0.08 mg cm−2 for L. scrobiculata (n = 480 for each species). Before transplantation, STM differed between seasons (ANOVA; P < 0.001) from 8.99 ± 0.10 (3 January) to 10.7 ± 0.1 mg cm−2 (4 July) for L. pulmonaria, and from 12.6 ± 0.1 (3 January) to 14.1 ± 0.2 mg cm−2 (6 October) for L. scrobiculata (n = 120). Under clear-cut conditions, the greatest increase in STM occurred during the dry April–June season, with similar percentage increases in the two species. This resulted from high RGR and very low RTAGR, particularly in L. scrobiculata. In the darkest and most humid season (October–December), STM often declined, particularly in L. scrobiculata. Thus, L. scrobiculata had a greater annual variation in STM than L. pulmonaria (Fig. 4), despite its higher pre-transplantation STM level. For L. pulmonaria, STM increased by 0.54 ± 0.02 mg cm−2 (mean ± 1 SE) during the dry April–June season, equivalent to a rise of 5.2%, whereas hardly any change occurred in the dark October–December season (Fig. 4). For L. scrobiculata, the area increments during October–December were substantially higher than the corresponding biomass investments, resulting in significantly declining STM (−0.41 ± 0.03 mg cm−2; Fig. 4), equivalent to a mass reduction of −2.9%.
Aspect-dependent irradiance and growth
Aspect strongly influenced the irradiance in seasonal-dependent ways (Fig. 5). With respect to diffuse radiation (Fig. 5b), the four vertical aspects did not differ from each other, whereas the top had consistently higher diffuse irradiance, particularly in summer. With respect to direct irradiance, the north side received minor amounts in May–July only (Fig. 5c). The east side received less direct irradiance than the west side in nearly all months, whereas the south side received more direct light than the top in the winter and less light in summer.
Before transplantation, there were no significant differences in STM between groups of thalli selected for the five aspects (ANOVA; data not shown), facilitating comparisons of aspect-specific effects. Aspect alone impacted growth rates less than season (Table 2). Lobaria pulmonaria had the lowest RGR at the top position (P < 0.001), and had higher RGR in north-facing than in south- and west-facing thalli (Figs 2, 3; P = 0.003). This trend, following an inverse irradiance gradient (Fig. 5), was clear from January to September, but there was no difference in mass change between the aspects in the dark October–December season with low aspect-dependent variation in irradiance. Area growth was highest at the north and east sides, with the lowest direct irradiance (Fig. 5c), and lowest at the south and top aspects, with the highest direct irradiance (Fig. 5c). Interaction with season was statistically insignificant (Table 2). For L. scrobiculata, aspect significantly affected growth in interaction with other factors only (Table 2). Thalli at the top had significantly higher RGR in the July–September season than those of the other aspects (P = 0.042), except for north-facing thalli, whereas aspect was insignificant in other seasons.
STM responded to aspect in species-specific ways. In L. pulmonaria, aspect had larger impacts on STM than on RGR and RTAGR (Table 2). In the warm and sunny July–September season, L. scrobiculata had a higher increase in STM at the most extreme aspect (top) than at any other aspect (P = 0.04). The contrast to L. pulmonaria was striking, as this species in the dry April–June season had a substantially lower increase in STM at the top compared with the north-, east- and west-facing sides (P < 0.001).
Timing of transplantation
The set (timing of transplantation) strongly affected subsequent growth patterns (Figs 2, 3; Table 2). In each of the two dark seasons, the newly transplanted sets had substantially higher RGR and RTAGR than sets introduced to the clear-cut one or more seasons earlier (Figs 2, 3). There was a lasting positive effect of transplantation in winter, as, in the second season after transplantation, growth rates were also higher in thalli transplanted in autumn–winter than in those transplanted two or three seasons earlier (Figs 2, 3). Growth patterns were different for sets started in warm seasons. For example, the L. pulmonaria set transplanted in April–June tended to be the set with the lowest RTAGR during this dry and sunny period (Fig. 3). In general, the growth of each set followed the common seasonal growth pattern, but the set–season interaction was highly significant (Table 2). For both species across sets there was a statistically significant declining trend from high growth during the first seasons after transplantation to low growth in the last season. This trend, documented in an analysis where the interaction term set × season was replaced by time since the first clear-cut exposure, was highly significant (P < 0.001; data not shown).
The growth data in Figs 2–4 are unique, as repeated simultaneous seasonal changes in biomass and area have not previously been recorded for a large set of lichen thalli. Area increment is rarely recorded in lichen studies, and lichen growth is often considered a synonym for mass growth or radial increment. Traditionally, environmental conditions experienced while thalli are moist have been considered to determine lichen growth (Lange, 2002, 2003b; Jonsson et al., 2008), and the irradiance during hydration explains a substantial part of the variation in lichen biomass increase (Dahlman & Palmqvist, 2003; Gaio-Oliveira et al., 2004).
The diverging annual courses of biomass (Fig. 2) and area growth rates (Fig. 3) provide a basis for better understanding of lichen growth processes. Comparisons of climatic variables (Fig. 1, Table 1) and growth patterns (Figs 2, 3) on a seasonal time-scale suggest that light is a driver of RGR, whereas humidity is required for area expansion (RTAGR). This was previously inferred in a spatial study of L. pulmonaria transplanted in three successional forest stands differing in canopy cover in each of three climatic zones along a macroclimatic humidity gradient from continental to oceanic sites (Gauslaa et al., 2009). Consistent responses along spatial (Gauslaa et al., 2009) and temporal (this study) gradients provide strong support for the view that lichen biomass growth and area growth are different processes. Area expansion is important as it is the only way in which a lichen thallus can increase its light-harvesting area and occupy new space. In view of the strong spatial (Gauslaa et al., 2007) and seasonal (this study) discrepancies in mass and area growth, future modeling studies should include both growth processes.
Our study documents strong seasonal changes in STM in lichens (Fig. 4). The photobiont drives mass growth through its CO2 assimilation (Palmqvist, 2000; Dahlman & Palmqvist, 2003), whereas the mycobiont contributes to area growth in a process that apparently requires hydration to form turgor pressure in expanding hyphae (Money, 2008). Cell expansion growth in plants is determined by cell wall properties and turgor pressure as described by Eqn 1:
(m, the wall extensibility; Ψp, the turgor pressure; Y, the yield threshold which Ψp must exceed to allow growth (e.g. Nobel, 1999).) Lichens already lose their turgor pressure at relative water contents of 43–60% (Beckett, 1995, 1996) which still may allow 50% of maximal net photosynthesis (Tuba et al., 1996). With no turgor pressure, area growth is hardly possible (Eqn 1), causing increased STM when photosynthesis is positive. STM stays fairly constant or decreases in seasons with short days (October–March) and long hydration periods without or with low light (Table 1; Fig. 4). Under such conditions, the carbon gain is low. In April–June when most rain comes during the day (Fig. 1), facilitating photosynthesis, STM increases strongly (Fig. 4). Climatic factors thus seem to drive seasonal changes in STM, consistent with an inducible response by external factors rather than a constitutive intraspecific regulation of thallus thickness. However, we do not know whether this is an active or passive response to prevailing climatic conditions.
According to the study of Gauslaa & Coxson (2011), the water-holding capacity is tightly coupled to STM, and within sites with similar rainfall regimes, STM significantly increases with canopy openness, and thus with increasing evaporative demands. Regardless of whether such responses are actively or passively regulated, an increase in STM may function as a compensatory mechanism to prolong hydration periods in sites with strong evaporative demands. The seasonal course in STM (Fig. 4) is consistent with the hypothesis that such a compensatory mechanism can be a part of seasonal acclimation in lichens. From a life cycle time perspective, STM increases with thallus size (e.g. Dahlman et al., 2002; Dahlman & Palmqvist, 2003; Gauslaa et al., 2009; Larsson & Gauslaa, 2011). In the cyanolichen Degelia plumbea, STM, total thallus thickness, and water-holding capacity are all strongly and positively correlated with thallus size, resulting in a > 10 times longer hydration period in the largest compared with the smallest thallus (Gauslaa & Solhaug, 1998). We can use the data set on juvenile thalli published in Larsson & Gauslaa (2011) to calculate that STM significantly increases with thallus size from 7.5 mg cm−2 in very small thalli (2–4 mm2) of both species to 9.8 and 13.5 mg cm−2 in larger thalli (10–20 cm2) of L. pulmonaria and L. scrobiculata, respectively. Thus, mature thalli may grow quickly in ecological niches where juvenile thalli are unable to establish because their water storage is too low. A size-dependent functional relationship between STM and duration of hydration cycles may explain the frequently reported discrepancy between fundamental and realized ecological niches in lichens (e.g. Antoine & McCune, 2004). Another implication of strongly seasonal STM is that studies of lichen performance need to consider the collection date of sampled thalli.
Cyanolichens, unlike cephalo- and chlorolichens, need liquid water to activate photosynthesis (Lange et al., 1986). They need much more water to become saturated than chlorolichens (Lange et al., 1993). At 90% relative humidity, the green alga Dictyochloropsis reticulate in L. pulmonaria efficiently assimilates carbon in the absence of liquid water, whereas the cyanolichen L. scrobiculata releases carbon, indicating active mycobiont respiration but inactive photosynthesis (Máguas et al., 1995). Thus, cyanolichen respiration in humid air represents a net carbon loss, although the loss is lower than after activation in water (Máguas et al., 1995). If hydration is mostly caused by humid air rather than rain or dew, L. scrobiculata will experience fewer active hours with photosynthesis than L. pulmonaria, but similar periods of fungal respiration. This may explain the lower growth rate in L. scrobiculata. To compensate for an inability to use humid air to photosynthesize, L. scrobiculata has a substantially higher water-holding capacity at a given STM than L. pulmonaria (Gauslaa & Coxson, 2011), presumably because of the gelatinous sheath surrounding their Nostoc cells. The highly significant regressions (r2 = 0.804 and 0.833; n = 120 in L. pulmonaria and L. scrobiculata, respectively) between water-holding capacity and STM (Gauslaa & Coxson, 2011) give computed start water-holding capacity as 24.6 and 14.7 mg H2O cm−2 for our thalli of L. scrobiculata and L. pulmonaria, respectively. Taking the highest annual increase in STM, 2.5 and 1.9 mg cm−2 for the July set for L. scrobiculata (top) and the January set for L. pulmonaria (north; see Fig. 4), respectively, these values would imply an increase in water storage of 8.7 mg H2O cm−2 for the cyanolichen vs 4.7 mg H2O cm−2 for the cephalolichen, equivalent to a 32–35% increase. The stronger increase in STM from the dark, humid October–December season to the sunny, dry April–June season for L. scrobiculata than for L. pulmonaria (Fig. 4) thus probably improves the fitness of the cyanolichen by prolonging hydration periods. The high rise of STM in L. scrobiculata at the extreme top aspect receiving abundant direct sun during summer (Fig. 5; July–September) can similarly be seen as beneficial at strong evaporative demands. Night-time dew providing liquid water is strongest at the top facing the open sky and being subjected to rapid nocturnal cooling (P. Larsson; unpublished field obs.; see also Stoutjesdijk & Barkman, 1987). In open sites, Lange (2003a) has shown that clear days with no rain contribute to a much higher proportion of the annual carbon gain than rainy days for the chlorolichen Lecanora muralis. Higher dew formation and a correspondingly high water-holding capacity probably explain the faster growth of L. scrobiculata at the top than at vertical aspects (Fig. 2). At optimal hydration, L. scrobiculata had much higher CO2 assimilation (2.3 ± 0.1 μmol CO2 m−2 s−1) than L. pulmonaria (0.9 ± 0.1 μmol CO2 m−2 s−1; mean ± SE; P. Larsson, unpublished data). Lobaria pulmonaria (e.g. Gauslaa & Solhaug, 1999), unlike L. scrobiculata (K. A. Solhaug, D. Coxson & Y. Gauslaa, unpublished data), is high-light susceptible. Therefore, it responds in an opposite way to aspect during the dry, sunny April–June season. Strong photoinhibition in L. pulmonaria at the top and south aspects (P. Larsson; unpublished data), also evidenced by localized bleached portions, presumably reduces the potential of this lichen to increase STM (Fig. 4).
In winter (October–December or January–March), newly transplanted thalli grew faster than older transplants that had been exposed for the first time to the clear-cut in summer (April–June or July–September; Figs 2, 3). This is interesting, as temperature and light during winter are low (Fig. 1). Solar radiation-screening compounds may explain the contrast between winter and summer sets. Lobaria pulmonaria and L. scrobiculata use cortical melanins and usnic acid, respectively, to reduce light at the underlying photobiont layer to nonharmful levels (Solhaug & Gauslaa, 2012; Asplund et al., 2010). As these pigments are rapidly induced by UV-B (Solhaug et al., 2003; McEvoy et al., 2006), they were absent or at low concentrations in the transplants when collected in forests, evidenced by a pale ash-gray color in the dry state. After exposure to the clear-cut in the sunny periods of April–June or July–September, these pigments were induced, as evidenced by brown pigmentation in L. pulmonaria and a yellowish color of L. scrobiculata. We believe that the higher growth in newly transplanted thalli in the dark winter is caused by high availability of light at the photobiont layer beneath pigment-deficient and transparent upper cortices in shade-adapted thalli (Gauslaa & Solhaug, 2001). Such an effect was not found during transplantation in the summer months, because the sudden exposure of shade-adapted forest thalli to a sun-exposed environment caused temporarily severe photoinhibition before pigments were formed (e.g. Gauslaa & Solhaug, 2000). We also believe that little or no pigment synthesis in UV-B-deficient winter seasons may have caused elevated growth also in parts of the next transplantation season with low light. In general, lichens function well at low temperatures that normally result in slow metabolic activity implying low respiratory losses and a lower light compensation point (Kershaw, 1985; Lange, 2002). Lichen photosynthesis can be active down to −10°C (Lange, 1965; Green et al., 2002), provided that there is a minimum hydration level. The corresponding lower maximal light-saturated CO2 uptake at low temperatures probably does not matter for winter photosynthesis because light at high latitudes is constantly below light saturation in winter (Fig. 1).
An additional explanation for reduced growth rates with time may be nutrient depletion in transplants taken out of the canopy drip zone which naturally adds leachates to lichens in forests (Goward & Arsenault, 2000). Recent studies have shown that lichen growth may be limited by low phosphorous and/or nitrogen availability (Benner et al., 2007; McCune & Caldwell, 2009; Johansson et al., 2011). However, such mechanisms hardly account for the strong seasonal trends in our study.
In conclusion, growth of L. pulmonaria and L. scrobiculata occurs in all seasons of the year in open boreal sites, although at slower rates in winter than in late summer. Mass and area growth in both species are separated along a temporal scale, resulting in seasonal changes in STM. Growth in mass may not result in area gain during dry and sunny periods, whereas area expansion can occur without detectable mass increase in dark and humid seasons.
We thank the landowner Egil Svarthol for access to the experimental site, and Olga Hilmo and Håkon Holien for suggesting collecting sites for lichen used in this study.